Neurovascular Imaging: MRI & Microangiography

Neurovascular Imaging Shoki Takahashi (Editor) Neurovascular Imaging MRI & Microangiography Dr. Shoki Takahashi De...

Author: Shoki Takahashi

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Neurovascular Imaging

Shoki Takahashi (Editor)

Neurovascular Imaging MRI & Microangiography

Dr. Shoki Takahashi Department of Diagnostic Radiology Tohoku University Graduate School of Medicine, Seiryo-machi Aoba-ku Sendai, 980-8574 Japan [email protected]

ISBN: 978-1-84882-133-0 DOI: 10.1007/978-1-84882-134-7

e-ISBN: 978-1-84882-134-7

Springer Dordrecht Heidelberg London New York A catalogue record for this book is available from the British Library Library of Congress Control Number: 2010932883 © Springer-Verlag London Limited 2010 Apart from any fair dealing for the purposes of research or private study, or criticism or review, as permitted under the Copyright, Designs and Patents Act 1988, this publication may only be reproduced, stored or transmitted, in any form or by any means, with the prior permission in writing of the publishers, or in the case of reprographic reproduction in accordance with the terms of licenses issued by the Copyright Licensing Agency. Enquiries concerning reproduction outside those terms should be sent to the publishers The use of registered names, trademarks, etc., in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant laws and regulations and therefore free for general use The publisher makes no representation, express or implied, with regard to the accuracy of the information contained in this book and cannot accept any legal responsibility or liability for any errors or omissions that may be made Cover design: eStudio Calamar, Figueres/Berlin Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com)

Preface

The current era is the era of rapidly advancing technologies. My drawing above says in Japanese, “Be sure to grasp the tip of the tail of the horse that is flying in time and space.” Just so, we need to catch up with and grab hold of the tip of the very rapidly advancing technology. We are at a point in time when we can visualize intracranial and spinal arteries and veins, or the neurovascular system, using imaging obtained without significant invasion. This book demonstrates the anatomy of the neurovascular system and images of the pathologic processes that involve these vessels in forms that may be applicable, or at least helpful, to the interpretation of images acquired with such modalities. Many excellent studies that focus on the anatomy of the intracranial arteries have accumulated in the literature. What a pity if we do not take advantage of these archival treasures to interpret images obtained using modern techniques! To utilize them efficiently, I did not hesitate to reproduce a series of engaging figures from the literature. To facilitate the reader’s understanding of the book’s figures and for annotation, consistent abbreviations have been adopted for individual structures and incorporated into the figures without obscuring recognition of the structures indicated. Within this context, I presume that some structures can be discerned without reference to the annotations and that repeating the recognition and referring processes for individual structures may promote

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Preface

memorization. In addition, in order that the direction of the transverse diagrams of the brainstem and spinal cord matches the orientation of modern transverse images, the figures are presented with the anterior orientation on the upper side and the posterior on the lower side. Our presentation reverses the traditional presentation of diagrams and images with the posterior on the upper side and the anterior on the lower side. Finally, I wish to extend my gratitude to all the contributors to this book for their diligent efforts and to colleagues, families, and friends whose encouragement and support helped us bring this project to successful completion. Many thanks go as well to Akio Muto for his gracious help in obtaining necessary publication permissions to reproduce figures, Philips Healthcare for their support for the preparation of this book, Yuki Sugawara for her outstanding secretarial assistance; Nobuo Sasaki and other radiological technologists in the Division of Radiological Science of the Research Institute of Brain and Blood Vessels, Akita, Japan for their help in taking microangiograms of cadaver brains; Tatsuo Nagasaka and other radiological technologists in the MR section of Tohoku University Hospital, Sendai, Japan; and all the radiological technologists in the institutions of the contributors to this book for obtaining MR and CT images; Sadao Yamauchi for his photographic work; and Rosalyn Uhrig for her editorial assistance in the preparation of the manuscript. We were fortunate to work with Denise Roland and the team at Springer-Verlag London, dedicated professionals who guided us with great patience. I dedicate this book to my wife, Reiko, and my children, Teppei and Sayaka.

Shoki Takahashi

Contents

Part I Normal Anatomy of Brain Vessels 1 Intracranial Arterial System: The Main Trunks and Major Arteries of the Cerebrum................................... Shoki Takahashi and Shunji Mugikura

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2 Intracranial Arterial System: Basal Perforating Arteries................................ 53 Shoki Takahashi 3 Intracranial Arterial System: Infratentorial Arteries....................................... 131 Shoki Takahashi 4 Perforating Branches of the Anterior Communicating Artery: Anatomy and Infarction....................................................................................... 189 Toshikatsu Fujii 5 Cerebral Arterial Variations and Anomalies Diagnosed by MR Angiography.......................................................................... 197 Akira Uchino 6 Regional MR Perfusion Topographic Map of the Brain Using Arterial Spin Labeling at 3 Tesla................................................... 241 Shuichi Higano and Takaki Murata 7 Normal Anatomy of Intracranial Veins: Demonstration with MR Angiography, 3D-CT Angiography and Microangiographic Injection Study............................................................. 255 Akio Fukusumi 8 Mapping Superficial Cerebral Veins on the Brain Surface............................... 285 Shuichi Higano

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Contents

Part II Neurovascular Imaging in Pathology 9 Preoperative Visualization of the Lenticulostriate Arteries Associated with Insulo-Opercular Gliomas Using 3-T Magnetic Resonance Imaging............................................................................................... 295 Toshihiro Kumabe, Ryuta Saito, Masayuki Kanamori, Yukihiko Sonoda, Shuichi Higano, Shoki Takahashi, and Teiji Tominaga 10 Ischemic Complications Associated with Resection of Opercular Gliomas.......................................................................... 305 Toshihiro Kumabe, Masayuki Kanamori, Ryuta Saito, Ken-ichi Nagamatsu, Yukihiko Sonoda, Shuichi Higano, Shoki Takahashi, and Teiji Tominaga 11 Imaging and Tissue Characterization of Atherosclerotic Carotid Plaque Using MR Imaging..................................................................... 319 Toshiaki Taoka 12 MR Imaging of Cerebral Aneurysms.................................................................. 345 Noriko Kurihara 13 MR Imaging of Vascular Malformations............................................................ 373 Atsushi Umetsu 14 Cerebral Venous Malformations........................................................................ 395 Akio Fukusumi 15 Thrombosis of the Cerebral Veins and Dural Sinuses....................................... 409 Akio Fukusumi part III Anatomy and Imaging of Spinal Vessels 16 Vessels of the Spine and Spinal Cord: Normal Anatomy ................................. 427 Shoki Takahashi 17 MDCT of the Artery of Adamkiewicz................................................................. 451 Kei Takase and Shoki Takahashi 18 Magnetic Resonance Angiography of the Spinal Cord Blood Supply............. 465 Robbert J. Nijenhuis and Walter H. Backes 19 Magnetic Resonance Imaging of Spinal Vascular Lesions................................ 487 Shuichi Higano Index

. .................................................................................................................. 507

Contributors

Walter H. Backes PhD Department of Radiology University Medical Center Maastricht Maastricht The Netherlands Toshikatsu Fujii, MD PhD Department of Behavioral Neurology and Cognitive Neuroscience Tohoku University Graduate School of Medicine Seiryo-machi Aoba-ku Sendai, 980-857 Japan

Masayuki Kanamori, MD PhD Departments of Neurosurgery and Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan Toshihiro Kumabe, MD PhD Departments of Neurosurgery and Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan

Akio Fukusumi, MD PhD Department of Radiology Takanohara Central Hospital Nara Japan

Noriko Kurihara, MD PhD Department of Radiology National Hospital Organization Sendai Medical Center Sendai Japan

Shuichi Higano, MD PhD Department of Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan

Shunji Mugikura, MD PhD Department of Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan

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Takaki Murata, MD Department of Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan Ken-ichi Nagamatsu, MD Departments of Neurosurgery and Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan Robbert J. Nijenhuis, MD PhD Departments of Radiology University Medical Center Maastricht, Maastricht St. Elisabeth Hospital, Tilburg The Netherlands Ryuta Saito, MD PhD Departments of Neurosurgery and Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan Yukihiko Sonoda, MD PhD Departments of Neurosurgery and Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan

Contributors

Shoki Takahashi, MD PhD Department of Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan Kei Takase, MD PhD Department of Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan Toshiaki Taoka, MD PhD Department of Radiology Nara Medical University Kashihara Japan Teiji Tominaga, MD PhD Departments of Neurosurgery and Diagnostic Radiology Tohoku University Graduate School of Medicine Sendai Japan Akira Uchino, MD PhD Department of Diagnostic Radiology Saitama Medical University International Medical Center Hidaka Japan Atsushi Umetsu, MD PhD Department of Diagnostic Radiology Tokohu University School of Medicine Sendai Japan

Part I Normal Anatomy of Brain Vessels

Intracranial Arterial System: The Main Trunks and Major Arteries of the Cerebrum

1

Shoki Takahashi and Shunji Mugikura

1.1 Introduction To illustrate the anatomy of intracranial arteries, we reviewed the literature and chose many illustrations of brain vessel anatomy to include in the first three chapters. Relevant microangiograms prepared from cadaver brains demonstrate how individual arteries penetrate, course, and distribute in successive sections of the brain [61, 62], and magnetic resonance (MR) images of the brains of volunteers obtained using a Philips Intera Achieva 3.0-T Quasar Dual (Philips Healthcare Best The Netherlands) illustrate the course and distribution of normal intracranial arteries. Anterior circulation of the brain derives from both internal carotid arteries (ICA), and posterior circulation derives basically from the vertebral artery (VA)-basilar artery (BA) system. At the base of the cerebrum, each ICA bifurcates into the anterior (ACA) and middle cerebral arteries (MCA) to supply the cerebral hemispheres anteriorly on the same side. The terminal end of the BA bifurcates into posterior cerebral arteries (PCA) to supply the hemispheres posteriorly (Fig. 1.1). Because the uncus/parahippocampal gyrus and the hippocampal region are parts of the cortex, their arterial supply is also described in this chapter.

1.2 Internal Carotid Artery (ICA) Typically, the common carotid artery bifurcates into the ICA and external carotid artery (ECA) at the third or fourth cervical vertebral level. The ICA comprises several segments from the proximal side enumerated by Bouthillier and associates that follow the direction of blood flow [10, 42]; the communicating segment, as Bouthillier’s group defines, may better be subdivided into communicating (C7) and choroidal (C8) segments as delineated

S. Takahashi (*) Department of Diagnostic Radiology, Tohoku University Graduate School of Medicine, Seiryo-machi, Aoba-ku, Sendai, 980-8574, Japan e-mail: [email protected] S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_1, © Springer-Verlag London Limited 2010

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4

S. Takahashi and S. Mugikura

a

b

ACA

AChA

ACA

PCA

PCA AChA

LSA

MCA

ACoA

BA

PCoA

MCA OA

SCA PCoA BA

AICA PICA

PICA VA ICA

VA

ICA

Fig. 1.1 General outline of the brain arteries (modified from [60]). (a) Anteroposterior (AP) view. (b) Lateral view. ACA anterior cerebral artery; AChA anterior choroidal artery; ACoA anterior communicating artery; AICA anterior inferior cerebellar artery; BA basilar artery; ICA internal carotid artery; LSA lenticulostriate artery; MCA middle cerebral artery; OA ophthalmic artery; PCA posterior cerebral artery; PCoA posterior communicating artery; PICA posterior inferior cerebellar artery; SCA superior cerebellar artery; VA vertebral artery

by Gibo et al. [23] (Fig. 1.2). Fischer’s scheme is often used clinically as well; it numbers the segments of the ICA from the top down against the direction of blood flow and begins the division with the extension of the C1 segment from the terminal bifurcation of the ICA to the origin of the posterior communicating artery (PCoA) and terminates with the C5 or precavernous segment.

1.2.1 Segments of the ICA delineated by Bouthillier et al. (Fig. 1.2) [10, 23] The cervical segment (C1) is the portion of the ICA from the common carotid bifurcation to the entry of the carotid canal. The initial portion of this segment shows a smooth dilation just distal to the origin, which is called the carotid sinus, and is known to be involved in blood pressure regulation. The petrous segment (C2) courses within the carotid canal, consists of an initial vertical portion and subsequent horizontal portion, and gives rise to 3 possible branches−the caroticotympanic, mandibulovidian, and variant stapedial arteries. The lacerum segment (C3) begins at the intracranial entry above the foramen lacerum and ends at the petrolingual ligament, where a small reflection of the periosteum forms a bridge between the lingula of the sphenoid bone anteriorly and the petrous apex posteriorly [10, 46]. The Meckel cave, which contains the trigeminal ganglion, covers the C3 and the ascending part of the next C4 segment laterally [32, 46] (Fig. 1.3).

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1 Intracranial Arterial System: The Main Trunks and Major Arteries of the Cerebrum

a

b

ACA AChA PCoA

ACA

MCA

MCA

C8

C8

OA

C6

AChA

C6 C4

Cavernous

PCoA

C5

C4 C3

Choroidal Communicating Ophthalmic Clinoid

C7

C7

Lacerum

C3

Petrous

C2

C2

Cervical

C1

C1

ECA

CCA

Fig. 1.2 Diagram illustrating the segments of the internal carotid artery (based on the study of Bouthillier et al. [10] with some modification following the Gibo group. [23]). (a) Anteroposterior (AP) view. (b) Lateral view. Division from the proximal side includes the cervical (C1), petrous (C2), lacerum (C3), cavernous (C4), clinoid (C5), ophthalmic (C6), communicating (C7), and choroidal (C8) segments. ACA anterior cerebral artery; AChA anterior choroidal artery; CCA common carotid artery ECA external carotid artery; MCA middle cerebral artery; OA ophthalmic artery; PCoA posterior communicating artery

The cavernous segment (C4) runs within the cavernous sinus and lies bilaterally between the two dural leaves in the parasellar region (Fig. 1.3). Initially, it ascends vertically medial to the Meckel cave and then turns (posterior bend) to run forward. Anteriorly, it makes another turn (anterior bend) upward and posteriorly, pierces the proximal dural ring medial to the anterior clinoid process, and transitions to the clinoid segment. The cavernous segment gives off several small branches, including the meningohypophyseal trunk, the inferolateral trunk, and the capsular artery (Fig. 1.4). The clinoid segment (C5) is short and lies between the proximal and distal dural rings [10]. The ophthalmic segment (C6) extends from the distal dural ring to the origin of the PCoA and gives off the ophthalmic artery and superior hypophyseal arteries.

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a

b DMm

SAS AM

III IV

TL

VI III

PG

MC

IV

AM

ICA VI V1 V2

Cav SS Sph

SAS

CL

TG

DMm DMp ICA PB

V3

Fig. 1.3 Coronal cross-sectional diagrams of the parasellar region (reproduced from [32] but modified on the basis of [34]). (a) Anterior section through the proximal branches of the fifth nerve. (b) Posterior section through the Gasserian ganglion. The approximate cross-sectional planes are illustrated in the inset. According to Kehrli et al. [34], there is no medial dural wall limiting the cavernous sinus. The sinus is limited by mesenchyme-derived fibrous tissue, through which capsular arteries from the ICA pass to the pituitary gland and intercavernous venous channels cross the midline traveling rostrally or caudally to the pituitary gland. Thick unbroken line: meningeal layer of dura (DMm: dura propria); dashed line: arachnoid membrane (AM); dot – dash line: periosteal layer of dura (DMp); dotted area: subarachnoid space (SAS); cross-hatched area: bone. Cav cavernous sinus; CL clivus; ICA internal carotid artery; MC Meckel cave; PB petrous bone; PG pituitary gland; Sph sphenoid bone; SS sphenoid sinus; TG trigeminal ganglion; TL temporal lobe; III oculomotor nerve; IV trochlear nerve; VI abducens nerve; V1 ophthalmic division of fifth nerve; V2 maxillary division of fifth nerve; V3 mandibular division of fifth nerve

The communicating segment (C7) extends from the origin of the PCoA to the origin of the anterior choroidal artery (AChA) [23] and gives rise to the PCoA from the posterior wall of the artery and possibly to a few perforators. The choroidal segment (C8) continues from the origin of the AChA to the terminal ICA bifurcation into the ACA and MCA [23] and gives off the AChA and some perforators from its posterior wall. The entire intracisternal portion of the ICA (C6, C7, and C8) is often called the supraclinoid portion, and the entire winding part comprising the C3 through C8 segments of the ICA is called the carotid siphon.

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a

b MCA

ACA

SOF

ILT

SHyA

CpA

SHyA OA

FRo

AChA

PCoA

FOv

MHT

MMA

OC OA

PGa

MdCA

PGp

TnA

FSp RcAFL

MdCA

LtCA

DROA SOF

ICA

LtCA ILT

FRo AFRo AFOv

TnA

IHyA FOv

AFSp

FSp

MHT RcAFL

MMA

Fig. 1.4 Branches from the carotid siphon (modified from [59]). (a) Lateral view. (b) Bird’s-eye view. ACA anterior cerebral artery; AChA anterior choroidal artery; AFOv artery of the foramen ovale (→ accessory meningeal artery); AFRo artery of the foramen rotundum (→ internal maxillary artery); AFSp artery of the foramen spinosum (→ middle meningeal artery); CpA capsular artery; DROA deep recurrent ophthalmic artery; FOv foramen ovale; FRo foramen rotundum; FSp foramen spinosum; ICA internal carotid artery; ILT inferolateral trunk or inferior cavernous artery; IHyA inferior hypophyseal artery; LtCA lateral clival artery; MCA middle cerebral artery; MdCA medial clival artery; MHT meningohypophyseal trunk; MMA middle meningeal artery; OA ophthalmic artery; OC optic canal; PCoA posterior communicating artery; PGa anterior lobe of the pituitary gland; PGp posterior lobe of the pituitary gland; RcAFL recurrent artery of the foramen lacerum (→ ascending pharyngeal artery); SHyA superior hypophyseal artery; SOF superior orbital fissure; TnA tentorial artery (anastomotic arteries are indicated within parentheses)

1.2.2 The Ophthalmic Artery (Fig. 1.5) The ophthalmic artery typically originates intradurally from the anteromedial or superior aspect of the internal carotid artery (C6) immediately after it penetrates the distal dural ring. Rarely, it arises from the clinoid (C5) or cavernous segment of the ICA (C4) (extradurally). It is divided into 3 segments−intracranial, intracanalicular (within the optic canal), and intraorbital. The intraorbital segment is further subdivided into three: the (1) infraoptic portion coursing forward along the inferolateral aspect of the optic nerve; (2) latero-optic portion crossing over the optic nerve normally along its lateral aspect; and (3) supraoptic portion coursing forward along the superomedial aspect of the optic nerve and ending at the medial angle of the eye, the medial frontal artery superiorly and dorsal nasal artery inferiorly. The latero-optic portion represents the lateral arc of the embryonic arterial ring around the optic nerve (85%) and may be replaced by a medio-optic portion when the medial arc of the arterial ring persists as the lateral arc involutes during development (15%) [26].

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a

b DNaA

MFA SOrA

AFxA

SOrA AEthA LcA

AEthA

MFA

RtA

PEthA

MCiA LCiA angle

ON SOF

ON

DNaA

bend

DROA

PEthA bend

3

IMsA

2

LcA

1

RtA IMsA

ICA

angle

ICA

Fig. 1.5 Diagram illustrating the course and branches of the ophthalmic artery (modified from [59]). (a) Superior view. (b) Lateral view. 1 infraoptic portion of the intraorbital segment; 2 latero-optic portion of the intraorbital segment; 3 supraoptic portion of the intraorbital segment. AEthA anterior ethmoidal artery; AFxA anterior falx artery; DNaA dorsal nasal artery; DROA deep recurrent ophthalmic artery; ICA internal carotid artery; IMsA inferior muscular artery; LcA lacrimal artery; LCiA lateral ciliary artery; MCiA medial ciliary artery; MFA medial frontal artery; OA ophthalmic artery; ON optic nerve; PEthA posterior ethmoidal artery; RtA retinal artery; SOrA supraorbital artery; SOF superior orbital fissure

1.2.3 Anatomy and Aneurysms of the Paraclinoid Region The paraclinoid region needs special description, because exactly locating paraclinoid aneurysms is difficult, but crucial to strategizing management. Although extradural aneurysms are at lower risk of subarachnoid hemorrhage, rupture of an intradural aneurysm is life-threatening and may require treatment.

1.2.3.1 Anatomy of the Paraclinoid Region (Fig. 1.6) Before entering the intradural space, the ICA passes through the thin proximal dural ring, which is continuous with the periosteum of the anterior clinoid process, and the thick and tight distal dural ring, which comprises the dura propria [45]. The segment of the ICA between the two rings is defined as the clinoid or C5 segment. The proximal ring is relatively incompetent and inconstantly admits a variable number of veins from the cavernous sinus; thus, the clinoid ICA may be regarded as transitional between the intracavernous and extracavernous [35].

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a C5

ON

PSph

TbS

ACP

OA

DDR

PG

C6

SHyA

DDR

b

Carotid Cave C6 SHyA

OA ACP

DphS TbS

PG

C5 PDR C4

Cav

Sph

Fig. 1.6 Schematic drawing of the anatomy of the paraclinoid region. (a) Superior view of the sellar region. (b) Coronal section of the left paraclinoid region (modified from [35]). The distal dural ring continues through the superficial dural layer or the dura propria (indicated by the blue line) on the superior surface of the anterior clinoid process and the roof of the cavernous sinus laterally, the dura of the tuberculum sellae anteromedially (dotted line), and with the diaphragma sellae posteromedially. The ring is bounded laterally by the anterior clinoid process, anteriorly by the optic strut, and anteromedially by the tuberculm sellae, but posteromedially lacks bony contact where the carotid cave is located and often contains the subarachnoid space [31]. Note the inclination of the distal ring toward the posteromedial direction, with its anterolateral side marked by the superior border of the anterior clinoid process and its medial side, by the tuberculum sellae. The proximal dural ring is laterally continuous with the deep dural layer or the periosteum of the anterior clinoid process (indicated by green line). (c) Lateral view of the left paraclinoid region (reproduced from [51]). The superficial dural layer with distal dural ring are separated from the deep dural layer and proximal dural ring. The anterior clinoid process is surgically removed, thereby revealing the C5 segment of the internal carotid artery. The notch of the superficial dural layer that forms the dural sheath of the optic nerve is called the falciform fold. II optic nerve; III oculomotor nerve; ACP anterior clinoid process; Cav cavernous sinus; DDR distal dural ring; DphS diaphragma sellae; FF falciform fold; OA ophthalmic artery; PDR proximal dural ring; PG pituitary gland; PSph planum sphenoidale; SHyA superior hypophyseal artery; Sph sphenoid bone; TbS tuberculum sellae

10 Fig. 1.6 (continued)


c II FF C6

ACP

PDR

DDR III

C5

ACS

C4

The distal ring represents the anatomic boundary between the extradural and intradural spaces and is continuous with the diaphragma sellae along its medial aspect [35]. The ring is denser and adheres more tightly to the ICA superolaterally, but adherence is less well defined medially [42]. Further, the ring inclines toward the posteromedial direction, and its anterolateral side is marked by the superior border of the anterior clinoid process and its medial side by the tuberculum sellae [45]. This inclination leads to the generation of a redundant dural recess or pouch, called the carotid cave, at the medial or posteromedial aspect of the distal dural ring between the ICA laterally and the body of the sphenoid bone (tuberculum sellae) anteromedially [31, 35, 36]. The carotid cave is thus situated at the medial or posteromedial aspect of the distal dural ring and may contain the subarachnoid space [45]. The cave should not be confused with the clinoid space, a space that may result between the two rings following surgical removal of the anterior clinoid process and that is situated in the lateral aspect of the ICA and corresponds to the extradural (and extracavernous) space (Fig. 1.6c) [45, 65]. Generally, no arterial branch originates from the C5 segment of the ICA, but the ophthalmic artery can arise extradurally from the segment proximal to the distal dural ring (6%) or, more usually, intradurally from the anteromedial aspect of the ophthalmic segment (C6) [35]. The origin of the ophthalmic artery is commonly used as the angiographic limit between the extradural and intradural ICA [50, 64], but variability in its origin among individuals makes the artery an unreliable landmark. Multiple superior hypophyseal arteries (mean number, 2.3) arise from the posteromedial wall of the proximal half of the C6 segment [35], a few of which may originate from the ICA near the carotid cave [31].

1.2.3.2 Paraclinoid Aneurysms Paraclinoid aneurysm is a term used generically to describe aneurysms of the C5 and C6 (and possibly C4) segments when the exact origins of the aneurysms are unknown [35, 44]. Because of the complexity of the extravascular anatomy of the paraclinoid region, particu-


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larly of the radiotransparent dural folds [64], various attempts have been made utilizing MR imaging to evaluate the exact location of paraclinoid aneurysms [30, 63, 64]. The various types follow (from proximal to distal) (Fig. 1.7) [35, 44]. Transitional paraclinoid aneurysms arise from the extradural ICA (C4 or C5 segment), but project superiorly into the intradural extracavernous subarachnoid space [5] (by reaching such a large size that the dome enters the intradural space and straddles the distal dural ring). Carotid cave aneurysms arise from the posteromedial aspect of the proximal-most C6 and are located below the distal dural ring, which implies an extradural origin, but they extend into the intra- and extradural spaces and can cause subarachnoid hemorrhage [36]. Ophthalmic artery aneurysms usually arise at the origin of the same artery (usually from the dorsal surface of the C6 segment and intradurally, but infrequently, they arise from the C5 segment and extradurally).

a OA aneurysm SHyA aneurysm

Carotid cave aneurysm

b

DDR

OA aneurysm

Posterior carotid wall aneurysm

PDR

Fig. 1.7 Schematic drawing of paraclinoid aneurysms (modified from [35]). (a) Coronal section of the paraclinoid region. (b) Lateral view of the carotid siphon. ACP anterior clinoid process; DDR distal dural ring; OA ophthalmic artery; PDR proximal dural ring

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Posterior carotid wall aneurysms or ventral paraclinoid aneurysms arise from the ventral aspect of the C6 segment and project posterolaterally (the neck is usually intradural, and the dome often projects partially into the cavernous sinus and straddles the distal dural ring) [19]. Superior hypophyseal aneurysms arise distal to the origin of the ophthalmic artery but proximal to the origin of the PCoA (usually from the medial surface of the C6 segment and intradurally).

1.3 The Circle of Willis The circle of Willis is an anastomotic arterial ring that connects the right and left carotid systems (anterior circulation) and the vertebrobasilar system (posterior circulation), thus providing a potential source of collaterals in case of arterial occlusive disorders (Fig. 1.8). The circle comprises the communicating-choroidal (C7–C8) segments of the ICA, the horizontal (A1) segment of the ACA, the anterior communicating artery (ACoA), the PCoA, and the precommunicating (P1) segment of the posterior cerebral artery (PCA). The segments of the A1, ACoA, PCoA, and P1 may normally be hypoplastic (Figs. 1.9 and 1.10); that is, their diameters are no larger than one mm [54]. Rhoton’s group [54, 68] reported that every hemisphere contains both the PCoA and P1 segment of the PCA and that these are inversely related in size on the same side. The PCoA is hypoplastic in 32% of brains (unilateral 26%, bilateral 6%). A well-developed PCoA that is larger than the ipsilateral P1 segment that supplies the predominant bulk of the

Fig. 1.8 Axial microangiogram through the base of the brain, showing the main arteries and circle of Willis with relatively thin posterior communicating artery, but not the anterior communicating artery and P1 segment of the PCA (reproduced from [60]). ACA anterior cerebral artery; AChA anterior choroidal artery; MCA middle cerebral artery; PCA posterior cerebral artery; PCoA posterior communicating artery; SyF sylvian fissure

ACA

MCA

SyF

AChA

PCoA

PCoA Midbrain

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a

ACoA

C7

II

A2

A1 M1

ICA Inf AChA

PCoA MB

P1

OT III P2 SCA

BA

b

(1)

(2) (3)

Fig. 1.9 Variation in the circle of Willis (reproduced from [60]). (a) Normal configuration of the circle of Willis (viewed from below). The circle of Willis comprises the communicating-choroidal (C7–C8) segments of the internal carotid artery (ICA), the horizontal (A1) segment of the anterior cerebral artery (ACA), the anterior communicating artery (ACoA), the posterior communicating artery (PCoA), and the precommunicating (P1) segment of the posterior cerebral artery (PCA). The bluecolored segments of the A1, ACoA, PCoA, and P1 may normally be hypoplastic. Also note that the A1 segment of the ACA courses superior to the optic nerve to join the contralateral A1 at the ACoA. II optic nerve; Inf infundibulum; MB mamillary body; OT optic tract. (b) An example of variation in the circle of Willis. (1) In case of a hypoplastic A1 on the right, the ACoA is well developed, which allows supply of the right peripheral ACA from the left A1 segment. (2) When the left PCoA is hypoplastic, the ipsilateral P1 segment is well developed, which ensures supply of the PCA territory from the basilar artery. When the right P1 segment is hypoplastic (3), the PCoA is well developed or fetaltype on the right, which ensures supply of the PCA territory from the internal carotid artery (ICA)

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a

b

c

d

Fig. 1.10 Magnetic resonance angiography (MRA) of the brain showing variations of the circle of Willis. (a) Frontal view with the left carotid eliminated, and (b) axial MRA show hypoplasia of the right precommunicating segment of the PCA (P1) (large arrow) and continuity of the well-developed posterior communicating artery (PCoA) with the right posterior cerebral artery (fetal-type PCA). On the left, axial MRA shows hypoplasia of the left PCoA and supply of the left PCA from the basilar artery via the well-developed P1. Superior cerebellar artery (small blue arrow). (c) Frontal and (d) axial MRA show hypoplasia of the right horizontal segment of the ACA (A1). Note that the A2 segment of the right ACA is supplied from the well-developed left ACA (arrow) via the anterior communicating artery (ACoA)

PCA territory is designated “fetal-type.” A fetal configuration is observed in 22–40% of hemispheres, arising predominantly from the carotid artery. The posterior circle of Willis is normal in approximately half of cases, that is, the diameter of its left P1 segment is larger than the diameter of its left PCoA if the left PCoA is not hypoplastic, and the diameter of its right P1 segment similarly has a larger diameter than that of the right nonhypoplastic PCoA [54]. Similarly, the ACoA increases in size as the difference in diameter between the right and left A1 segments increases [49], which means the unilateral A1 is hypoplastic. These variations in configuration would induce asymmetric hemodynamic stresses in the arterial wall that may be associated with predisposition to aneurysm development in this part of the cerebral vessels [42, 52] (Fig. 1.11).

15

1 Intracranial Arterial System: The Main Trunks and Major Arteries of the Cerebrum Fig. 1.11 Diagrams illustrating aneurysm development associated with variations in the circle of Willis. (a) Aneurysm development in sites receiving hemodynamic thrust (reproduced from [53]). Saccular aneurysms are presumed to develop at a site of branching, have a turn or curve on the parent artery, and point in the direction that the blood would have gone if the curve at the aneurysm site were absent [53]. For example, a posterior communicating artery aneurysm usually arises from the posterior wall of the internal carotid artery (ICA) and points posteriorly and superolaterally toward the oculomotor nerve. Aneurysm formation and variations in the circle of Willis in (b) a diagram and (c) left anterior oblique MR angiography. Aneurysms of the anterior communicating artery usually occur when one horizontal segment of the ACA (A1) is hypoplastic. With asymmetric development of the A1 segments, the aneurysm most often points anteriorly and away from the side of the dominant A1, i.e., in the direction in which flow would have traveled (arrowhead in (c))

a

MCA

ACA

AChA PCoA

Och

III

ON

OA ICA

b

c

16


1.4 The Main Arteries of the Cerebrum and Their Vascular Territories The cerebrum is supplied by the anterior, middle, and PCA and smaller vessels that include some other branches of the ICA, such as the PCoA and AChA.

1.4.1 The Main Arterial Trunks and Their Branches Major arteries of the ACA, MCA, and PCA are divided into several segments like the main trunk of the ICA, which are shown in Figs. 1.12–1.14 with the names commonly used for their cortical branches [55]. To nourish the cerebrum, each of the main arterial trunks gives rise to the basal perforating arteries proximally and the pial cortical arteries peripherally. The main arterial trunks and their cortical branches are well delineated on MR angiography (MRA), especially when a high-tesla MR system is used (Fig. 1.15).

1.4.2 The Vascular Territories of the Cerebral Arteries Since the pioneering research of Duret (1) and Heubner (2), numerous investigators have performed anatomic and radiographic studies of the distribution of the cerebral arteries, including the basal perforating arteries [1–4, 6–9, 12, 13, 17, 18, 20, 21, 24, 25, 27–29, 33, 39, 47, 48, 56–58, 67]. Figure 1.16 presents representative coronal, sagittal, and transaxial microangiograms that show the course and distribution of major cerebral vessels and their cortical arteries. On the whole, the trunk of the ACA runs along the corpus callosum and its cortical arteries distribute along the medial aspect and partly on the external surface of the frontal and parietal lobes, finally coursing posteriorly toward the parieto-occipital sulcus. The MCA vessels perfuse a large area over the outer surface of the hemisphere, the center of which is located in the sylvian fissure. The PCA vessels supply the inferior medial aspect of the temporal and occipital lobes except the anterior end of the temporal lobe, which is supplied by the MCA, and the uncus, which is supplied by the AChA [9]. The area of the PCA also includes a portion on the outer surface near the midline posteriorly. The inferior fourth of optic radiations are supplied by the PCA and the superior three-fourths, by the MCA [9]. The ACA supplies the rostrum, genu, and body of the corpus callosum, and the PCA supplies the splenium and forceps major. The hippocampal region will be described separately. Figures 1.17–1.20 map the different vascular territories of the main arteries on the surface and on the different sections of the cerebrum as published in the monumental studies of Beevor [8, 9], who simultaneously injected the primary arteries with different-colored dyes under the same pressure to avoid overflow through the anastomoses between the neighboring vascular territories.

17


a A4

CCb CCg

A3

CCs CCr A2 AC A1 MCA ACoA

b

MIFA

AIFA

PIFA

POS PCaA CC

FPA CMA

SIPA

PaCA

IIPA SpA

FOA

Fig. 1.12 Diagram illustrating the anterior cerebral artery (ACA). (a) Segments of the ACA (reproduced from [59]). A1 the horizontal segment that extends from the bifurcation of the internal carotid artery (ICA) to the junction with the anterior communicating artery and takes a horizontal course medially superior to the optic nerve/tract; A2 the infracallosal segment that extends from the junction with the A1 to the turn of the precallosal segment and takes an anterosuperior course within the cistern of the lamina terminalis; A3 the precallosal segment that makes a turn immediately anterior to the genu of the corpus callosum; A4 the supracallosal segment above the body of the corpus callosum, which may be subdivided into anterior and posterior halves. AC anterior commissure; ACoA anterior communicating artery; CCb corpus callosum, body; CCg corpus callosum, genu; CCr corpus callosum, rostrum; CCs corpus callosum, splenium; MCA middle cerebral artery. (b) Cortical vessels of the ACA (reproduced from [59]). The callosomarginal artery represents a common stem of the anterior, middle, and posterior internal frontal arteries, and so on, but may be seen in only half of cases. AIFA anterior internal frontal artery; CC corpus callosum; CMA callosomarginal artery (common stem of the AIFA, middle internal frontal artery (MIFA), posterior internal frontal artery (PIFA), and so on, but may be absent in about half of cases); FOA fronto-orbital artery; FPA frontopolar artery; IIPA inferior internal parietal artery; PaCA paracentral artery; PCaA pericallosal artery; PIFA posterior internal frontal artery; POS parieto-occipital sulcus; SIPA superior internal parietal artery; SpA splenial artery (posterior pericallosal artery)

18


a

b

Superior Trunk of MCA Inferior Trunk of MCA PrCA

CeA APA PPA

PrFA

M4 AngA

M3 LSA

TOA

OFA

PTA TPoA

M2

c

ATA

MTA

Superior Trunk of MCA Middle Trunk of MCA PrCA

CeA

PrFA

APA PPA AngA

M1

TOA

OFA ATA

MTA

PTA

Inferior Trunk of MCA

Fig. 1.13 Diagram illustrating the segments of the middle cerebral artery (MCA). (a) Segments of the MCA (based on [22, 37]). M1 the horizontal or sphenoidal segment that extends from the bifurcation of the internal carotid artery (ICA) to the limen insulae, where the middle cerebral artery (MCA) makes a turn or genu superiorly into the insula; M2 the insular segment that extends from the genu to the circular sulcus of the insula; M3 the opercular segment that extends from the circular sulcus to the turn at the superficial part of the sylvian fissure, running closely along and over the surface of the opercula; M4 the cortical segment that extends from the superficial part of the sylvian fissure to spread over the outer surface of the cortices. (b, c) Cortical vessels of the MCA (reproduced from [55]). The main trunk of the MCA divides in one of three ways: bifurcation into superior and inferior divisions (78%) (b); trifurcation into superior, middle, and inferior divisions (12%) (c); or division into multiple divisions (10%) followed by subdivision into individual cortical arteries [22]. With the bifurcation type, the superior division may supply the orbitofrontal to the posterior parietal areas, and the inferior division may supply the angular to temporopolar areas. The small arteries that arise proximal to the bifurcation or trifurcation and are distributed to the frontal or temporal pole are called “early branches” [22]. AngA angular artery; APA anterior parietal artery; ATA anterior temporal artery; CeA central artery; MTA middle temporal artery; OFA orbitofrontal artery; PPA posterior parietal artery; PrCA precentral artery; PrFA prefrontal artery; PTA posterior temporal artery; TOA temporo-occipital artery; TPoA temporal polar artery

19


a

b

POA

CalA

LPChA MPChA

P4

PITA LPChA

TTA

P3 P2A TPA

TPA TGA CalA

LPChA P2P

PCoA

P1

AITA

AITA

AITA BA

POA

SpA

PCoA

PITA

BA

Fig. 1.14 Diagram illustrating the segments and cortical vessels of the posterior cerebral artery (PCA) (reproduced from [59]). (a) AP view. (b) Lateral view. P1 the precommunicating or interpeduncular segment that extends from the basilar tip to the junction with the posterior communicating artery; P2 the ambient segment that runs within the crural and ambient cisterns to reach the posterior margin of the pulvinar of the thalamus and may divide into equal anterior P2 (P2A) and posterior P2 (P2P) segments at the lateral mesencephalic sulcus (posterior margin of the cerebral peduncle); P3 the quadrigeminal segment that runs within the quadrigeminal cistern to the anterior end of the calcarine sulcus; P4 the cortical segment that spreads along the cortical surface. AITA anterior inferior temporal artery; BA basilar artery; CalA calcarine artery; LPChA lateral posterior choroidal artery; MPChA medial posterior choroidal artery; PCoA posterior communicating artery; PITA posterior inferior temporal artery; POA parieto-occipital artery; SpA splenial artery (posterior pericallosal artery); TGA thalamogeniculate artery; TPA thalamoperforate artery; TTA thalamotuberal artery

1.4.3 The Boundary Zone and Leptomeningeal Anastomoses The boundary zone, also called the watershed zone, forms between two neighboring vascular areas and may be described as superficial and deep; the cortical area between the ACA and MCA and that between the MCA and PCA serve as superficial boundaries, and the region of deep white matter around the lateral ventricle serves as the deep boundary. The cortical arteries most peripherally located in the neighboring territories anastomose with each other over the superficial boundary zones and are called leptomeningeal anastomoses; they can supply retrograde collateral circulation in case of decreased perfusion pressure from proximal obstruction of a vessel (Fig. 1.21). In contrast, the deep boundary zone involves the most peripheral part of the medullary arteries from the pial arteries over the superficial boundary zone and is apart from the most distal portion of the basal perforators (Fig. 1.22). Unlike the pial vessels, the intraparenchymal vessels, such as the medullary arteries and the basal perforators, are essentially end arteries [9]. Although blood vessels within the brain are known to have anastomoses at the

20


a

b

ACA

ACA

OA ICA

M2 M3 M4

AChA

PCoA P2 AITA

MCA

A1

M1

M4

P1

P3 M3

PITA

CalA

A1

C6

M2

M1

POA

C4 C3

C2

Fig. 1.15 Time-of-flight (TOF) magnetic resonance angiography (MRA) partial maximum intensity projection (MIP). MRA was obtained using a 3-T Philips Achieva imager (Philips Medical Systems, Best, the Netherlands) with a standard head coil. Images were acquired using a gradient-echo sequence (3-dimensional T1 fast field echo (3D T1 FFE)) without contrast medium administration at the following parameters: repetition time/echo time/field angle (TR/TE/FA) = 25 ms/3.45 ms/20°; field of view (FOV) = 200 mm; matrix size: 512 × 293 (matrix size: 0.39 × 0.68); reconstruction matrix: 704 × 704 (matrix size: 0.28 × 0.28); slice thickness 1 mm with a gap of 0.5 mm; 150 total slices; sensitivity encoding (SENSE) factor 2.3; acquisition time: 5 min 49 s. (a) Axial image of intracranial MRA with the distal anterior cerebral artery (ACA) vessels trimmed. (b) Anteroposterior (AP) view of the left carotid system. (c) Lateral view of the ACA. (d) Lateral view of the middle cerebral artery (MCA). (e, f) AP and lateral views of the vertebrobasilar system. A1 A1 segment of the anterior cerebral artery; A2 A2 segment of the anterior cerebral artery; A3 A3 segment of the anterior cerebral artery; A4 A4 segment of the anterior cerebral artery; C2 C2 segment of the internal carotid artery; C3 C3 segment of the internal carotid artery; C4 C4 segment of the internal carotid artery; C6 C6 segment of the internal carotid artery; M1 M1 segment of the middle cerebral artery; M2 M2 segment of the middle cerebral artery; M3 M3 segment of the middle cerebral artery; M4 M4 segment of the middle cerebral artery; P1 P1 segment of the posterior cerebral artery; P2 P2 segment of the posterior cerebral artery; P3 P3 segment of the posterior cerebral artery; P4 P4 segment of the posterior cerebral artery ACA anterior cerebral artery; AChA anterior choroidal artery; AICA anterior inferior cerebellar artery; AIFA anterior internal frontal artery; AITA anterior inferior temporal artery; AngA angular artery; APA anterior parietal artery; BA basilar artery; CalA calcarine artery; CeA central artery; FOA fronto-orbital artery; FPA frontopolar artery; ICA internal carotid artery; IIPA inferior internal parietal artery; OA ophthalmic artery; LPChA lateral posterior choroidal artery; MCA middle cerebral artery; MIFA middle internal frontal artery; MPChA medial posterior choroidal artery; PaCA paracentral artery; PCaA pericallosal artery; PCoA posterior communicating artery; PICA posterior inferior cerebellar artery; PIFA posterior internal frontal artery; PITA posterior inferior temporal artery; POA parieto-occipital artery; PPA posterior parietal artery; PrCA precentral artery; PrFA prefrontal artery; SCA superior cerebellar artery; SIPA superior internal parietal artery; SpA splenial artery (posterior pericallosal artery); TOA temporo-occipital artery; VA vertebral artery

21


c

d

PaCA SIPA

PIFA

CeA APA PrCA

MIFA AIFA

IIPA A4

PPA

PrFA AngA

PCaA

A3

FPA

TOA

A2 FOA

AChA

C6

C4 OA

e

PCoA

f POA

POA CalA

MPChA

LPChA

SpA

CalA PITA PITA AITA SCA

PCoA

PCoA

BA AICA

BA

SCA

AITA AICA

PICA

PICA VA

VA

Fig. 1.15 (continued)

capillary level, such anastomoses are insufficient in size and number to maintain tissue viability if arterial occlusion occurs. Generally speaking, the superficial and deep boundary zones are liable to become infarcted in case of hemodynamic insult, such as atheromatous occlusion of the cervical ICA (Fig. 1.23). This would be especially true in the deep boundary zone, which is supplied by the most distal portion of the fine and long medullary arteries, i.e, the most distant zone from a parent artery or a source of blood supply. Although schematic drawings are shown, the cerebral vascular territories vary considerably (Fig. 1.24), and any drawing of vascular territories serves only as an example and does not represent an absolute pattern of vascular supply. The following description is based on the boundary between two neighboring arteries described by van der Zwan et al., who simultaneously injected the primary arteries with different-colored dyes under the same pressure using a method similar to that of Beevor [66].

22 Fig. 1.16 Microangiograms showing the general distribution of major cerebral arteries. (a) Coronal microangiogram shows the terminal bifurcation of the internal carotid artery (ICA) into the anterior (ACA) and middle (MCA) cerebral arteries. The cortical vessels of the MCA are distributed over the insula and the lateral surface of the brain, and those of the ACA, on the medial surface. (b, c) Median sagittal microangiograms of different brains show the distribution of ACA vessels on the medial aspect of the brain. (d, e) Consecutive axial microangiograms of a brain show denser capillary blush along the medial aspect of the temporal and occipital lobes and thalami (arrows), which represent the distribution of the posterior cerebral artery (PCA). This should have been caused by the injection of contrast through a vertebral artery


a

MCA

ICA ACA

b

c

PCA


d

23

e


On the medial surface of the hemisphere, the posterior cerebral area extends beyond the external parieto-occipital sulcus half-way along the parietal lobule so as to join the anterior cerebral area and prevent the middle cerebral area from reaching the median line, which commonly occurs (Fig. 1.17a). Thus, the ACA–PCA boundary is most often located in the precuneus area and less often in the parieto-occipital sulcus. On the superior lateral surface, the ACA-MCA boundary is most often found in the superior frontal sulcus, followed in frequency by the superior frontal gyrus or middle frontal gyrus. The MCA territory extends to the interhemispheric fissure in 30–60% of cases and separates the areas of the ACA and PCA on the superior lateral surface [9, 66]. On the lateral and inferior surface of the temporal lobe, the MCA–PCA boundary is most frequently located in the inferior temporal gyrus and less often in the inferior temporal sulcus. Such variable relationship between arterial distribution and functional vascular areas should be recognized and considered when interpreting clinical images with cerebral infarcts or other pathologies [38].

1.4.4 Arterial Supply of the Uncus/Parahippocampal Gyrus and the Hippocampal Region Because the uncus/parahippocampal gyrus and hippocampal region are parts of the cortex, their vascular supplies are described, and descriptions are based primarily on the studies of Marinkovic et al. [40, 41] and Duvernoy [15].

24


1.4.4.1 The Uncus/Parahippocampal Gyrus The uncal and parahippocampal arteries may originate from the AChA, ICA, MCA, and PCA (Figs. 1.25 and 1.26) [41]. Of these, the vessel supplying both the uncus and the hippocampal formation is called the unco-hippocampal artery, and that supplying the uncus and parahippocampal gyrus is called the unco-parahippocampal artery, and so on. The uncal or unco-parahippocampal branches of the AChA are divided into rostral and caudal vessels; the rostral vessels supply the semilunar and ambient gyri in the rostral uncus, and the caudal vessels supply the caudal uncus (uncinate gyrus, the band of Giacomini, and the uncal apex). The caudal vessel, which corresponds with the uncal branch of the AChA that is often found angiographically, may enter the uncal sulcus where the AChA anastomoses with the anterior hippocampal artery of the PCA [16] and may supply the most rostral part of the hippocampal formation (Fig. 1.26b). The posterior cerebral artery always gives off 2–10 parahippocampal vessels, the largest of which originates within the rostral hippocampo-parahippocampal arterial complex

Fig. 1.17 Distribution of arteries on the outer surface of the cerebral hemisphere (reproduced from Beevor [8]). (a) Medial, (b) lateral, (c) inferior, (d) superior surface of brain. AC anterior commissure; AL ansa lenticularis; Am amygdaloid body; APS anterior perforated substance; Aq aqueduct of Sylvius; CalS calcarine sulcus; CAv calcar avis; CC corpus callosum; CCg corpus callosum, genu; CCs corpus callosum, splenium; Cd caudate nucleus; CdT caudate nucleus, tail; CG cingulate gyrus; ChP choroid plexus; CiS cingulate sulcus; Cl claustrum; Cn cuneus; CoS collateral sulcus; CP cerebral peduncule; CR corona radiata; CS central sulcus; CSO centrum semiovale; EC external capsule; EMdL external medullary lamina; FG fusiform gyrus; Fi fimbria; FM foramen of Monro; Fx fornix; FxCo fornix, column; FxCr fornix, crus; GPe globus pallidus, external segment; GPi globus pallidus, internal segment; Hp hippocampal formation; HS hippocampal sulcus; ICa internal capsule, anterior limb; ICg internal capsule, genu; ICp internal capsule, posterior limb; ICpi internal capsule, posterior limb-inferior part; ICps internal capsule, posterior limb-superior part; ICr internal capsule, retro-lenticular portion; IFG inferior frontal gyrus; IFS inferior frontal sulcus; IPS intraparietal sulcus; ITG inferior temporal gyrus; ITS inferior temporal sulcus; LG lingual gyrus; LGB lateral geniculate body; LOG lateral orbital gyrus; LV lateral ventricle; LVa lateral ventricle, atrium; LVb lateral ventricle, body; LVf lateral ventricle, frontal horn; LVt lateral ventricle, temporal horn; LVo lateral ventricle, occipital horn; MFG middle frontal gyrus; MGB medial geniculate body; MI massa intermedia; MTG middle temporal gyrus; MTT: mammillothalamic tract (Tract of Vicq. d’Azyr); OCh optic chiasm; OR optic radiation; OT optic tract; OTS occipito-temporal sulcus; PC posterior commissure; PHG parahippocampal gyrus; Po pons; PoCG postcentral gyrus; POS parieto-occipital sulcus; PrCG precentral gyrus; PrCn precuneus; PrCS precentral sulcus; Pt putamen; Pu pulvinar of thalamus; RN red nucleus; RSth regio subthalamica; SCo superior colliculi; SeP septum pelucidum; SFG superior frontal gyrus; SFS: superior frontal sulcus; SMG supramarginal gyrus; SN substantia nigra; SPL superior parietal lobule; STG superior temporal gyrus; Sth subthalamic nucleus (Luy’s body); STS superior temporal sulcus; SyF sylvian fissure; Tap tapetum of corpus callosum; TC tuber cinereum; Th thalamus; U uncus; US uncal sulcus; 3V third ventricle.

25


a

CS

CiS

SFG CG

POS

PrCn

CC

Cn CalS

LG PHG

U

FG

SyF

b

SFS

PrCS

CS

PrCG

SPL

Middle cerebral artery

SFG SMG

Anterior choroidal artery

POS

MFG

Anterior cerebral artery

SFS

Posterior communicating artery

IFG

Posterior cerebral artery

STG IFS

SyF STS

c

d

LOG SFG

SyF STS MTG

MFG

SFS CoS

ITS

U

US

CS

PHG FG

PrCS

OTS

PrCG

ITG

PoCG CalS

CS

SPL

CoS

POS

26


a

ChP CS SFG

SFS

PrCG

MFG

PoCG

POS

EMdL

CC

Fx Cd

ICa

Th

ICg

Pt GPe AC

CCs

Cn

Pu Sth

GPi

LG

CalS

CP U

SyF

LVt

APS

b

SFS

CS

SFG

PrCG

PoCG

MFG CR

EMdL Cd CC

ICa GPe

Pt AC

GPi

Cn

LV

ICp CP

Th Fx Pu

Am Hp OT US

LG

CalS

CalS LVt

Fig. 1.18 Distribution of arteries on sagittal sections of the human brain (reproduced from Beevor [8, 9]). (a) One centimeter from the median surface of the hemisphere. (b) 1.5 cm from the median surface of the hemisphere

[41]. There is a reciprocal relationship among these uncal or unco-parahippocampal vessels; if the caudal uncal branch of the AChA is thin, the unco-parahippocampal branch of the PCA is strong (Fig. 1.26d), and vice versa.

1.4.4.2 The Hippocampus The hippocampus is a part of the limbic lobe and the first part of the cortex to initiate differentiation (archaeocortex) [11]; its primary nourishing artery is the PCA, which developed phylogenetically as a derivative of the hippocampal artery (Fig. 1.27) [1].

27


a

b SFS SFG

SyF

ICa Pt AC

APS FxCo

STS

FxCo STS

RSth

Sth CP OT ICr CdT OR

Cd AC AL

MTT

MTT

RN OR

LVt

Hp

ICa

SyF

Cd

LGB MGB

ICr

CdT

SCo

Sth Th Pu Fi SCo Hp

LVo

POS

Cals

Cals

c

d

SFG

IFS

SFS SFG

IFG

SeP

LVf

SyF

Cd

Cd ICa AC

Pt FxCo

Cl EC

ICg

ICr OR

Th PC

ICg

GPi

FxCo

Th

MI ICp ICr OR CdT

Pu

CdT Fi

SeP

Pt GPe

STS GPe GPi

CC

ICa

CCg

SyF

Hp CCs

Pu CCs

FxCr

ChP

LVo POS

CAv POS

Cn

CalS

Fig. 1.19 Horizontal sections of the human brain (reproduced from Beevor [8, 9]). (a) Through the red nucleus with the geniculate bodies. (b) Through the superior colliculi. (c) Through the anterior commissure. (d) Through the most superior part of the globus pallidus. (e) Through the lenticular nucleus. (f) Through the most superior part of the thalamus

28


e

SFS

f

SFG

SFS SFG

MFG

IFS

MFG

CSO CCg

IFG

CSO

Cd

CC SeP

ICa

Pt

CS

LVf

SyF

Cd

SeP

ICg STG Cl

LVb

ICp SyF

Th

EC

Th

CR

STG

Fx

STS

Cd CdT

LVa

OR Tap

CCs

CC

PrCn POS

POS

Cn


a

b SFS IFS

SFG

CS

MFG

IFG CC LV SeP AC

EC

Cd

SeP

CC

EC

Cd

LV

ICa

GPe

Pt

Pt

Cl

SyF

FxCo

ICg

GPi

SyF

GPe

APS

STS

APS

Am OCh

OT

MTG ITG

Fig. 1.20 Coronal sections of the human brain (reproduced from Beevor [8, 9]). (a) Through the anterior commissure (superior median part). (b) Through just posterior to the optic chiasma. (c) Through the tuber cinereum and the genu of the internal capsule. (d) Through the most anterior part of the pons. (e) Through just posterior to the lenticular nucleus. (f) Through the posterior part of the thalamus

29


c

d SFS

SFG

SFS

SFG

CS

PrCG

CS

PoCG LVb CC

LV

Fx FM

Cd

GPe

Cd

SyF

EC

ICp

Th

EC

Cl

OT

SN

PHG

OT

MTG

Po

Hp

CoS

CoS

f

ITG

ITS

OTS

CS

CS PrCG

PrCG PoCG

MTG

FuG

US

e

STS CdT

PHG

ITS

ITG

U

CP

LVt

Cl

GPe

RN

AC

Am

TC

Pt

Sth

GPi

RSth

STG

Th

3V

SyF

Pt

MTT

3V

CC

IPS

PoCG

IPS SMG SyF

ChP

Cd CC

STG

3V RN

U

CP

PHG

Hp FuG

CoS


Fx

MTG

CdT

Cd Hp

MGB

Aq

MTG

ICr

Pu

ICp Fi OT

SN

Cd EMdL

CC

STS

Th

SyF LV

LVt

PHG

ITS

ITS FuG

ITG CoS

ITG OTS

STS

30


Fig. 1.21 Leptomeningeal anastomoses of Heubner (modified from [69]). Arrows indicate the direction of blood flow, and the broken line between the opposed arrows indicates the boundary zone between the neighboring territories ACA

PCoA

ICA

BA

MCA

PCA

a

Fig. 1.22 Coronal (a) and axial (b) microangiograms show that the area around the ventricular lumen and the centrum semiovale are the most distal part of not only the medullary arteries of the anterior (ACA) and middle (MCA) cerebral arteries (arrowheads), but also that part of the basal perforators (arrows)


b


31

32


a

b

Fig. 1.23 A 79-year-old man with watershed infarct. (a, b) Computed tomography (CT) shows infarcts in the superficial boundary zone between the middle (MCA) and posterior (PCA) cerebral arteries (black arrowhead) and in the deep boundary zone between the anterior cerebral artery (ACA) and the MCA (white arrowheads) in the centrum semiovale on the right. The patient had complete occlusion of the right cervical internal carotid artery (not shown)

a

b

c

Fig. 1.24 (a) Axial section through the lower basal ganglia (b) Axial section through the upper basal ganglia (c) Axial section through the lateral ventricular body Schematic drawing showing a composite of the minimum extent of the territories of the anterior (ACA; yellow zone), middle (MCA; pink zone), and posterior (PCA; blue zone) cerebral arteries (modified from [66]). The boundary zone would be located anywhere within the white zones. The figure clearly shows the large varied area in which the boundaries could be located

33


a

b MCA

ACA

PHB-m

ICA

RhS

AChA U-PHB-i

SAnS

TP

AITA RhS

PHB

UB-a PyC

APS

AmG UG UA PHG

AITA

SLG BG

CoS

U AHpA PCA

CoS MITA CoS

FG

PITA

Fig. 1.25 The ventromedial surface of the right temporal lobe (a) and parahippocampal gyrus showing the uncal or unco-parahippocampal branches (b) (b is reproduced from [41]). ACA anterior cerebral artery; AChA anterior choroidal artery; AHpA anterior hippocampal artery; AITA anterior inferior temporal artery (stippled); AmG ambient gyrus; APS anterior perforated substance; BG band of Giacomini; CoS collateral sulcus; FG fusiform gyrus; ICA internal carotid artery; MCA middle cerebral artery; MITA middle inferior temporal artery; PCA posterior cerebral artery; PHB parahippocampal branch of posterior cerebral artery (black); PHB-m parahippocampal branch of middle cerebral artery; PHG parahippocampal gyrus; PITA posterior inferior temporal artery; RhS rhinal sulcus; SAnS semianular sulcus; SLG semilunar gyrus; TP temporal pole; U uncus; UA uncal apex (IL: intralimbic gyrus); UB-a uncal branch of anterior choroidal artery; UG uncinate gyrus; U-PHB-i unco-parahippocampal branch of the internal carotid artery; US uncal sulcus

34


a CiS

SbPS CG IG

CC

Fx

GRA CA AC PTG

PPOS

Isth ACS

Fi BG

SbA

DG CoS

APOS SLG

APS

AmG RhS

UA

UG

PHG

US ERA

PHG

Fig. 1.26 The medial surface of the limbic lobe and the rostral hippocampo-parahippocampal arterial complex. (a) Medial surface of the limbic lobe (reproduced from [14]), (b–d) Variations of the components of the rostral hippocampo-parahippocampal arterial complex (reproduced from [41]). When the unco-parahippocampal complex of the anterior choroidal artery (AChA) predominates, it supplies both the anterior hippocampal head and the parahippocampal gyrus (PHG), and the same complex of the posterior cerebral artery (PCA) remains underdeveloped (b), and vice versa (d). (c) The intermediate form, with the AChA giving off the anterior hippocampal artery. ACA anterior cerebral artery; AChA anterior choroidal artery; AC anterior commissure; ACS anterior part of calcarine sulcus; AHpA anterior hippocampal artery; AmG ambient gyrus; APOS anterior parolfactory sulcus; APS anterior perforated substance; AITA anterior inferior temporal artery; BG band of Giacomini; CA cornu ammonis; CC corpus callosum; CCs corpus callosum, splenium; CG cingulate gyrus; CiS cingulate sulcus; CoS collateral sulcus; DG dentate gyrus; ERA entorhinal area (Brodmann’s area 28); Fi fimbria; Fx fornix; GAR gyri of Andreas Retzius; Hp hippocampal formation; ICA internal carotid artery; IG indusium griseum (supracallosal gyrus); Isth isthmus of cingulate gyrus; LT lamina terminalis; MCA middle cerebral artery; MHpA middle hippocampal artery; PCA posterior cerebral artery; PCoA posterior communicating artery; PHB parahippocampal branch of posterior cerebral artery; PHG parahippocampal gyrus; PPOS posterior parolfactory sulcus; PTG paraterminal gyrus; RhS rhinal sulcus; SbA subcallosal area; SbPS subparietal sulcus; SLG semilunar gyrus; U uncus; UA uncal apex (IL intralimbic gyrus); UB uncal branch; UG uncinate gyrus; US uncal sulcus

35

1 Intracranial Arterial System: The Main Trunks and Major Arteries of the Cerebrum Fig. 1.26 (continued)

b ACA

MCA

AChA

AHpA Hp

U UB PCA ICA PHG

US PHG PCoA PHB

AITA

c

d MHpA

36


a

b PCA

HA enlarging anastomosis

LOA

MCA

enlarging anastomosis mesencephalic or diencephalic Br.

CdDv

CrDv

MOA

ICA

ACA

CdDv ICA

c PCA MCA

ACA

PCoA

BA

ICA

Fig. 1.27 Phylogenetic development of the posterior cerebral artery (schemas drawn based on Abbie’s study [1], reproduced from [59]). In the amphibian stage (a), the internal carotid artery (ICA) divides into caudal (CdDv) and cranial (CrDv) divisions. The antecedents of the anterior (ACA) and middle (MCA) cerebral arteries derive from the cranial division, and the hippocampal artery (HA) develops from the antecedent of the MCA (LOA: lateral olfactory artery).With posterior expansion of the cerebral hemisphere in the reptilian stage (b), the origin of the hippocampal artery moves caudally along the cranial division through enlarging basal anastomoses and dwindling of existing channels, and finally, the posterior cerebral artery (PCA) that is branched from the basilar artery is formed in the mammalian stage (c). BA basilar artery; MOA medial olfactory artery; PCoA posterior communicating artery

Superficial (Leptomeningeal) Hippocampal Arteries The 2–7 superficial hippocampal arteries measure 200–800 mm in diameter [40] and arise mainly from the PCA and to a lesser degree from the AChA (Figs. 1.28 and 1.29) [15, 40]. They are classified as the anterior hippocampal artery, which extends between the uncus and the parahippocampal gyrus and supplies the head of the hippocampus; the middle hippocampal artery, which courses just caudal to the uncus and supplies the body of the hippocampal formation; and the posterior hippocampal artery, which supplies the tail of the formation. The anterior hippocampal artery most often originates from the PCA and the anterior inferior temporal arteries as the rostral hippocampo-parahippocampal arterial complex, but it has been reported to arise from the AChA in 30% of hemispheres [40]. It disappears into the uncal sulcus, where it gives rise to intrahippocampal arteries and vascularizes the hippocampal head [15]. The uncal branch of the AChA frequently anastomoses with the anterior hippocampal artery of the PCA within the uncal sulcus (Fig. 1.26). The middle hippocampal artery is constant and most often arises from the PCA and its temporal arteries and sometimes from the lateral posterior choroidal artery. The posterior hippocampal artery often arises from the splenial artery, a branch of the PCA [15].

37


a

(anterior)

UR

HpD HpH

U SLG

UG

(lateral) HpB

Fi

Sb UA PHG

BG

(medial)

DG Fx LVt

CCs

HpT

IG

LLS

MLS

(posterior)

Fig. 1 28 Vascular supply of the hippocampal formation. (a) Superior view of the hippocampal formation and parahippocampal gyrus (the temporal horn has been opened) (reproduced from [60]). (b) Superior aspect of the parahippocampal gyrus illustrating the hippocampal arteries (modified from [14]). The temporal horn was opened and the fimbria removed (inset). Two arrows in the inset indicate the viewing direction of the main figure (b); the dashed line aa’ indicates the location of the inset coronal section. (c) Coronal section through a part of the body of the hippocampal formation. CA1 through CA4 represent the sectors of the hippocampus (modified from [14]). Arteries: Ana anastomosis between the longitudinal terminal segment of the superficial hippocampal arteries; ITA inferior temporal artery; l-DIHA large dorsal intrahippocampal artery; l-IHA large intrahippocampal artery; l-VIHA large ventral intrahippocampal artery; LTS longitudinal terminal segment of the superficial hippocampal arteries; MHpA middle hippocampal artery; PCA posterior cerebral artery; PHpA posterior hippocampal artery; SbA subicular artery; SpA splenial artery (posterior pericallosal artery); s-DIHA small dorsal intrahippocampal artery; s-VIHA small ventral intrahippocampal artery; StHA straight hippocampal artery of Marinkovic. Structures other than arteries: Alv alveus; AmC ambient cistern; AmW wing of ambient cistern; BG band of Giacomini; BVR basal vein of Rosenthal; CA cornu ammonis; CCs corpus callosum, splenium; ChP choroid plexus (removed); DG dentate gyrus; FDS fimbriodentate sulcus; Fi fimbria; Fx fornix; Hp hippocampal formation; HpB hippocampal body; HpD hippocampal digitations; HpH hippocampal head; HpT hippocampal tail; HS hippocampal sulcus; IG indusium griseum (supracallosal gyrus); LLS lateral longitudinal stria; LVt lateral ventricle, temporal horn; MD margo denticulatus; MDd dentes of margo denticulatus; MDs sulci between dentes of margo denticulatus; MLS medial longitudinal stria; PHG parahippocampal gyrus; Sb subiculum; SLG semilunar gyrus; Tent tentorium cerebelli; U uncus; UA uncal apex (IL intralimbic gyrus); UG uncinate gyrus; UR uncal recess of the temporal horn

38


b HpH

a

a'

HpB SbA FDS

FDS

Fi MD

MHpA

StHA

-IHA

PCA

LTS Sb Ana

s-DIHA

PHpA

SbA

ITA

LTS

-IHA Fi

ChP CA

HpT

AmW BVR AmC PCA

Sb

tent

c Fi CA2

CA

LVt

s-DIHA

s-DIHA CA3

4

DG

1

HS

Alv


s-VIHA SbA

-VIHA

Sb

StHA

MD MDs d

-DIHA

DG

CA

MD

HS

LTS

39


MHpA-L

LPChA LTS

StHA MD MD Fi

Sb MHpA-P

s-IHA

PCA StHA l-IHA

ITA

LTS PHpA-T HS MD

PHpA-S SpA

HpT

Fig. 1.29 Vascular india ink injection. The fimbria (Fi) has been removed to show the margo denticulatus (MD) and superior aspect of the parahippocampal gyrus. This preparation shows several superficial hippocampal arteries with various origins. Bar, 2.9 mm (reproduced from [14]). Fi fimbria (removed); HpT endoventricular aspect of the hippocampal tail; HS hippocampal sulcus; ITA inferior temporal artery; l-IHA large intrahippocampal artery penetrating between the dentes of the MD; LPChA lateral posterior choroidal artery, whose course towards the temporal horn has been cut off (arrow); LTS longitudinal terminal segment of the superficial hippocampal arteries situated along the superficial HS; MD margo denticulatus; MHpA-L middle hippocampal artery arising from a LPChA; MHpA-P middle hippocampal artery arising directly from the PCA; PCA posterior cerebral artery; PHpA-T posterior hippocampal artery arising from a small ITA; PHpA-S posterior hippocampal artery arising from the SpA; Sb subiculum; s-IHA small intrahippocampal artery; SpA splenial artery; StHA straight hippocampal artery of Marinkovic

When the hippocampal arteries reach the hippocampus, they curve to follow the sinuous, longitudinal course parallel to the superficial hippocampal sulcus and the margo denticulatus (longitudinal terminal segment) [15]. Along the longitudinal terminal segment, the hippocampal arteries give rise to numerous intrahippocampal arteries or their stem arteries, which Marinkovic and colleagues called the straight hippocampal arteries that

40


run more or less parallel to each other across the free surface of the dentate gyrus (margo denticulatus) [15, 40]. The subiculum is supplied by numerous subicular branches from the superficial hippocampal arteries and their longitudinal terminal segments as well as the straight hippocampal arteries. The hippocampal arteries richly anastomose with each other. Anastomoses between their longitudinal terminal segments may form a complete arterial arcade along the hippocampal formation, a rather rare finding in humans [15, 40, 43].

a

b

AChA

US

c

d

Fig. 1.30 Microangiograms demonstrating vascular supply of the intrahippocampal arteries. (a) Coronal section through the hippocampal head. In this case, the relatively prominent uncal branch of the anterior choroidal artery (AChA arrow) enters the uncal sulcus, (US), where it gives off numerous intrahippocampal arteries upwards (arrowhead). (b) Coronal section through the hippocampal body show superficial hippocampal artery (large red arrow). Subicular arteries (curved arrow) are noted. The large ventral (solid arrowhead) and dorsal (open yellow arrowhead) intrahippocampal arteries follow the rolling layers of the hippocampus, and very fine arteries that parallel them in between may represent small ventral intrahippocampal arteries. (c) Another coronal section through the hippocampal body show straight hippocampal artery (blue arrow). Subicular arteries (curved arrow) and the large ventral (solid arrowhead) and dorsal (open yellow arrowhead) intrahippocampal arteries are noted. (d) Coronal section through the hippocampal tail shows superficial hippocampal artery (large arrow) and numerous intrahippocampal arteries (arrowheads).


e

41

f

Fig. 1.30 (continued) (e) Axial section microangiogram through the anterior hippocampal region shows anterior and middle hippocampal arteries (arrow) and their longitudinal terminal segments (small blue arrow), from which numerous intrahippocampal arteries originate and display a rake-like appearance (arrowheads). (f ) Sagittal section microangiogram through the hippocampus shows numerous intrahippocampal arteries (arrowheads)

Intrahippocampal Arteries Numerous intrahippocampal arteries arise directly from the longitudinal terminal segments of the superficial hippocampal arteries or their branches, the straight hippocampal arteries, (Fig. 1.30) and can be subdivided into the large ventral, large dorsal, small ventral, and small dorsal intrahippocampal arteries [15, 40]. Both large ventral and large dorsal intrahippocampal arteries enter the hippocampus at the sulci between the dentes of margo denticulatus and follow the rolling layers of the hippocampus (Fig. 1.28c). The large ventral intrahippocampal arteries supply the CA1 and CA2, and the large dorsal intrahippocampal arteries supply the CA4, CA3, the distal part of the dentate gyrus, and sometimes the CA2 [15, 40]. The small ventral intrahippocampal arteries vascularize the proximal part of the dentate gyrus. The small dorsal intrahippocampal arteries vascularize the CA3 and part of the CA4. Because of their rectilinear and parallel path on the surface of the margo denticulatus as far as the fimbriodentate sulcus, Duvernoy referred to the small dorsal intrahippocampal arteries as the “straight” arteries, which was the term first adopted for the stem arteries of intrahippocampal arteries (branches from the longitudinal terminal segment) (Fig. 1.31).

Microangiograms of hippocampal arteries and MR images of infarction of hippocampal region Some of hippocampal arteries can be seen on microangiograms (Fig. 1.30) and infarction involving these arteries may be clinically seen on MR images in patients with infaction in the territory of the PCA (Fig. 1.31).

42 Fig. 1.31 Infarct in the hippocampal region. This 70-year-old man acutely developed memory disturbance. Though he complained of no motor or sensory disturbance, he showed homonymous hemianopsia on the right. Magnetic resonance imaging was performed on day 12. (a, b) Contrast-enhanced axial and coronal T1-weighted images in the subacute stage reveals infarction with irregular contrast enhancement in the hippocampus (arrows in a and b), parahippocampal gyrus, and the medial occipital cortex. Within the hippocampal formation, enhancement is prominent in the CA1, subiculum, and parahippocampal subcortical region on the coronal image (b). (c) Proton-density-weighted coronal image shows high signal in the entire hippocampus and parahippocampal gyrus (arrow in c)


a

b

c


43

Abbreviations 3D 3-Dimensional 3V Third ventricle II Optic nerve III Oculomotor nerve IV Trochlear nerve VI Abducens nerve V1 Ophthalmic division of fifth nerve V2 Maxillary division of fifth nerve V3 Mandibular division of fifth nerve AC Anterior commissure ACA Anterior cerebral artery ACP Anterior clinoid process AChA Anterior choroidal artery ACoA Anterior communicating artery ACS Anterior part of calcarine sulcus AEthA Anterior ethmoidal artery AFOv Artery of the foramen ovale (→ accessory meningeal artery) AFRo Artery of the foramen rotundum (→ internal maxillary artery) AFSp Artery of the foramen spinosum (→ middle meningeal artery) AFxA Anterior falx artery AHpA Anterior hippocampal artery AICA Anterior inferior cerebellar artery AIFA Anterior internal frontal artery AITA Anterior inferior temporal artery AL Ansa lenticularis Alv Alveus AM Arachnoid membrane Am Amygdaloid body AmC Ambient cistern AmG Ambient gyrus AmW Wing of ambient cistern Ana Anastomosis between the longitudinal terminal segment of the hippocampal arteries AngA Angular artery APA Anterior parietal artery APoS Anterior parolfactory sulcus APS Anterior perforated substance Aq Aqueduct of Sylvius ATA Anterior temporal artery A1 Horizontal segment of the ACA BA Basilar artery BG Band of Giacomini BVR Basal vein of Rosenthal

44

CeA CA CalA CalS Cav CAv CC CCb CCg CCr CCs Cd CdDv CdT CG ChP CiS Cl CL CMA Cn CoS CP CpA CR CrDv CS CSO CT DDR DG DMm DMp DNaA DphS DROA EC ECA EMdL ERA FA FDS FF FFE FG


Central artery Cornu ammonis Calcarine artery Calcarine sulcus Cavernous sinus Calcar avis Corpus callosum Corpus callosum, body Corpus callosum, genu Corpus callosum, rostrum Corpus callosum, splenium Caudate nucleus Caudal division Caudate nucleus, tail Cingulate gyrus Choroid plexus Cingulate sulcus Claustrum Clivus Callosomarginal artery (common stem of the AIFA, MIFA, PIFA) Cuneus Collateral sulcus Cerebral peduncule Capsular artery Corona radiata Cranial division Central sulcus Centrum semiovale Computed tomography Distal dural ring Dentate gyrus Meningeal layer of dura Periosteal layer of dura Dorsal nasal artery Diaphragma sellae Deep recurrent ophthalmic artery External capsule External carotid artery Externa medullary lamina Entorhinal area (Brodmann’s area 28) Flip angle Fimbriodentate sulcus Falciform fold Fast field echo Fusiform gyrus


Fi FM FOA FOv FOV FPA FRo FSp Fx FxCo FxCr GAR GPe GPi Hp HpB HpD HpH HpT HS ICa ICA ICg ICp ICps ICpi ICr IFG IFS IG IHyA IIPA ILT IMsA Inf IPS Isth ITA ITG ITS l-DIHA l-IHA l-VIHA LcA LCiA

Fimbria Foramen of Monro Fronto-orbital artery Foramen ovale Field of view Frontopolar artery Foramen rotundum Foramen spinosum Fornix Fornix, column Fornix, crus Gyri of Andreas Retzius Globus pallidus, external segment Globus pallidus, internal segment Hippocampal formation Hippocampal body Hippocampal digitations Hippocampal head Hippocampal tail Hippocampal sulcus Internal capsule, anterior limb Internal carotid artery Internal capsule, genu Internal capsule, posterior limb Internal capsule, posterior limb-superior part Internal capsule, posterior limb-inferior part Internal capsule, retro-lenticular portion Inferior frontal gyrus Inferior frontal sulcus Indusium griseum (supracallosal gyrus) Inferior hypophyseal artery Inferior internal parietal artery Inferolateral trunk or inferior cavernous artery Inferior muscular artery Infundibulum Intraparietal sulcus Isthmus of cingulate gyrus Inferior temporal artery Inferior temporal gyrus Inferior temporal sulcus Large dorsal intrahippocampal artery Large intrahippocampal artery Large ventral intrahippocampal artery Lacrimal artery Lateral ciliary artery

45

46

LG LGB LLS LOA LPChA LSA LT LtCA LTS LV LVa LVb LVf LVt LVo MB MC MCA MCiA MD MdCA MDd MDs MFA MFG MGB MHpA MHT MI MIFA MIP MLS MMA MOA MPChA MR MRA MTA MTG MTT OA OC OCh OFA ON


Lingual gyrus Lateral geniculate body Lateral longitudinal stria Lateral olfactory artery Lateral posterior choroidal artery Lenticulostriate artery Lamina terminalis Lateral clival artery Longitudinal terminal segment of the superficial hippocampal arteries Lateral ventricle Lateral ventricle, atrium Lateral ventricle, body Lateral ventricle, frontal horn Lateral ventricle, temporal horn Lateral ventricle, occipital horn Mamillary body Meckel cave Middle cerebral artery Medial ciliary artery Margo denticulatus Medial clival artery Dentes of margo denticulatus Sulci between dentes of margo denticulatus Medial frontal artery Middle frontal gyrus Medial geniculate body Middle hippocampal artery Meningohypophyseal trunk Massa intermedia Middle internal frontal artery Maximum intensity projection Medial longitudinal stria Middle meningeal artery Medial olfactory artery Medial posterior choroidal artery Magnetic resonance Magnetic resonance angiography Middle temporal artery Middle temporal gyrus Mammillothalamic tract (Tract of Vicq. d’Azyr) Ophthalmic artery Optic canal Optic chiasm Orbitofrontal artery Optic nerve


OR OT OTS PaCA PB PCaA PCA PC PCoA PDR PEthA PG PGa PGp PHB PHB-m PHG PHpA PICA PIFA PITA Po POA PoCG POS PPA PPCaA PPOS PrCA PrCG PrCn PrCS PrFA PSph Pt PTA PTG Pu P1 RcAFL RhS RN RSth RtA SAnS

Optic radiation Optic tract Occipito-temporal sulcus Paracentral artery Petrous bone Pericallosal artery Posterior cerebral artery Posterior commissure Posterior communicating artery Proximal dural ring Posterior ethmoidal artery Pituitary gland Anterior lobe of the pituitary gland Posterior lobe of the pituitary gland Parahippocampal branch of posterior cerebral artery Parahippocampal branch of middle cerebral artery Parahippocampal gyrus Posterior hippocampal artery Posterior inferior cerebellar artery Posterior internal frontal artery Posterior inferior temporal artery Pons Parieto-occipital artery Postcentral gyrus Parieto-occipital sulcus Posterior parietal artery Splenial artery (posterior pericallosal artery) Posterior parolfactory sulcus Precentral artery Precentral gyrus Precuneus Precentral sulcus Prefrontal artery Planum sphenoidale Putamen Posterior temporal artery Paraterminal gyrus Pulvinar of thalamus Precommunicating (P1) segment of the PCA Recurrent artery of the foramen lacerum (→ ascending pharyngeal artery) Rhinal sulcus Red nucleus Regio subthalamica Retinal artery Semianular sulcus

47

48

SAS Sb SbA SbPS SCo SCA s-DIHA SENSE SeP SFG SFS SHyA SIPA SLG SMG SN SOF SOrA SpA Sph SPL SS STG Sth StHA STS s-VIHA SyF T Tap TbS TC TE Tent TG TGA Th TL TnA TOA TOF TPA TPoA TR TTA


Subarachnoid space Subiculum Subicular artery Subparietal sulcus Superior colliculus Superior cerebellar artery Small dorsal intrahippocampal artery (straight artery of Duvernoy) Sensitivity encoding Septum pelucidum Superior frontal gyrus Superior frontal sulcus Superior hypophyseal artery Superior internal parietal artery Semilunar gyrus Supramarginal gyrus Substantia nigra Superior orbital fissure Supraorbital artery Splenial artery (posterior pericallosal artery) Sphenoid bone Superior parietal lobule Sphenoid sinus Superior temporal gyrus Subthalamic nucleus (Luy’s body) Straight hippocampal artery of Marinkovic Superior temporal sulcus Small ventral intrahippocampal artery Sylvian fissure Tesla Tapetum of corpus callosum Tuberculum sellae Tuber cinereum Echo time Tentorium cerebelli Trigeminal ganglion Thalamogeniculate artery Thalamus Temporal lobe Tentorial artery Temporo-occipital artery Time of flight Thalamoperforate artery Temporal polar artery Repetition time Thalamotuberal artery


TP U UA UB UB-a UG U-PHB-i UR US VA

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Temporal pole Uncus Uncal apex (IL: intralimbic gyrus) Uncal branch Uncal branch of anterior choroidal artery Uncinate gyrus (CA3+ Sb) Unco-parahippocampal branch of the internal carotid artery Uncal recess of the temporal horn Uncal sulcus Vertebral artery

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45. Oikawa S, Kyoshima K, Kobayashi S. Surgical anatomy of the juxta-dural ring area. J Neurosurg. 1998;89:250–4. 46. Osborn A. Diagnostic cerebral angiography. Philadelphia: Lippincott Williams & Wilkins; 1999. 47. Ostrowski AZ, Webster JE, Gurdjian ES. The proximal anterior cerebral artery: an anatomic study. Arch Neurol. 1960;3:661–4. 48. Percheron G. The anatomy of the arterial supply of the human thalamus and its use for the interpretation of the thalamic vascular pathology. Z Neurol. 1973;205:1–13. 49. Perlmutter D, Rhoton Jr AL. Microsurgical anatomy of the anterior cerebral-anterior communicating-recurrent artery complex. J Neurosurg. 1976;45:259–72. 50. Punt J. Some observations on aneurysms of the proximal internal carotid artery. J Neurosurg. 1979;51:151–4. 51. Reisch R, Vutskits L, Filippi R, Patonay L, Fries G, Perneczky A. Topographic microsurgical anatomy of the paraclinoid carotid artery. Neurosurg Rev. 2002;25:177–83. 52. Rhoton Jr AL, Fujii K, Fradd B. Microsurgical anatomy of the anterior choroidal artery. Surg Neurol. 1979;12:171–87. 53. Rhoton Jr AL. Anatomy of saccular aneurysms. Surg Neurol. 1980;14:59–66. 54. Saeki N, Rhoton Jr AL. Microsurgical anatomy of the upper basilar artery and the posterior circle of Willis. J Neurosurg. 1977;46:563–78. 55. Salamon G, Huan Y. Radiologic anatomy of the brain. Berlin: Springer; 1976. 56. Shellshear J. The basal arteries of the forebrain and their functional significance. J Anat. 1920;55:27–35. 57. Stephens RB, Stilwell DL. Arteries and veins of the human brain. Springfield, IL: Thomas; 1969. 58. Suzuki M. [Studies on the distribution of the basal branches of human cerebral arteries.] [Jpn]. Sapporo Med J. 1961;19:307–27. 59. Takahashi S. Supratentorial arteries. In: Miyasaka K, editor. Manual of cerebral and spinal angiography. Tokyo: Nankodo; 1997. p. 38–98. 60. Takahashi S. MR imaging anatomy of the brain. Tokyo: Shujunsha; 2005. 61. Takahashi S, Goto K, Fukasawa H, Kawata Y, Uemura K, Suzuki K. Computed tomography of cerebral infarction along the distribution of the basal perforating arteries. Part I: Striate arterial group Radiology. 1985;155:107–18. 62. Takahashi S, Goto K, Fukasawa H, Kawata Y, Uemura K, Yaguchi K. Computed tomography of cerebral infarction along the distribution of the basal perforating arteries. Part II: Thalamic arterial group. Radiology. 1985;155:119–30. 63. Thines L, Delmaire C, Le Gars D, Pruvo JP, Lejeune JP, Lehmann P, et al. MRI location of the distal dural ring plane: anatomoradiological study and application to paraclinoid carotid artery aneurysms. Eur Radiol. 2006;16:479–88. 64. Thines L, Gauvrit JY, Leclerc X, Le Gars D, Delmaire C, Pruvo JP, et al. Usefulness of MR imaging for the assessment of nonophthalmic paraclinoid aneurysms. AJNR Am J Neuroradiol. 2008;29:125–9. 65. Umansky F, Valarezo A, Elidan J. The superior wall of the cavernous sinus: a microanatomical study. J Neurosurg. 1994;81:914–20. 66. van der Zwan A, Hillen B, Tulleken CA, Dujovny M, Dragovic L. Variability of the territories of the major cerebral arteries. J Neurosurg. 1992;77:927–40. 67. Westberg G. The recurrent artery of Heubner and the arteries of the central ganglia. Acta Radiol [Diagn]. 1963;1:949–54. 68. Zeal AA, Rhoton Jr AL. Microsurgical anatomy of the posterior cerebral artery. J Neurosurg. 1978;48:534–59. 69. Zulch K. Some basic patterns of the collateral circulation of the cerebral arteries. In: Zulch K, editor. Cerebral circulation and stroke. Berlin: Springer; 1971. p. 106–22.

Intracranial Arterial System: Basal Perforating Arteries

2

Shoki Takahashi

2.1 Introduction A number of basal perforating arteries (perforators) supply neurologically critical zones, including the basal gray matter and major projecting fiber bundles. Knowledge of perforator anatomy may have clinical significance for neurological analysis in patients with strokes. Furthermore, it may be of importance in determining treatment strategy for cerebral aneurysms: because the perforators are intimately related to aneurysms, which most often involve the base of the brain, great care must be taken during aneurysm surgeries to preserve these vessels. The basal perforators may be divided into three groups: (1) the striate arterial group, which arise from the anterior (ACA) and middle (MCA) cerebral arteries and supply the subcortical telencephalic gray matter (basal ganglia); (2) the thalamic arterial group, or perforators of the posterior circulation, which distribute primarily within the diencephalon; and (3) the anterior choroidal artery (AChA) and carotid branches, which supply the area interposed between the striate arterial and thalamic arterial groups (Fig. 2.1).

2.2 Striate Arterial Group 2.2.1 Medial Striate Arteries (MSA) The horizontal (A1) segment of the ACA gives rise to an average of 7–8 perforating branches [54, 77], the medial striate arteries (MSA), which enter the medial anterior part of the anterior perforated substance above the optic nerve and chiasm [77, 83]. The lateral

S. Takahashi Department of Diagnostic Radiology, Tohoku University Graduate School of Medicine, Sendai, 980-8574, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_2, © Springer-Verlag London Limited 2010

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MPChA

Cd Pt

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TGA

Am

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MCA

ACA

ICA

Ch A

OT

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Fig. 2.1 Outline of the basal perforating arteries (adapted from Aitken, 1928). ACA anterior cerebral artery; AChA anterior choroidal artery; ACoA anterior communicating artery; Am amygdaloid body; BA basilar artery; Cd caudate nucleus; GP globus pallidus; IC internal capsule; ICA internal carotid artery; LPChA lateral posterior choroidal artery; LSA lenticulostriate arteries; MCA middle cerebral artery; MPChA medial posterior choroidal artery; MSA medial striate arteries; OT optic tract; PCA posterior cerebral artery; Pt putamen; RAH recurrent artery of Heubner; TGA thalamogeniculate artery; TPA thalamoperforate artery; Th thalamus; TTA thalamotuberal artery

(proximal) branches of the MSA are larger in number and often in size (average diameter, 325 mm) than the medial branches (average diameter, 122 mm) [54, 77]. These vessels constantly perfuse the region of the anterior hypothalamus and the medial third of the anterior commissure and only occasionally supply the caudate nucleus and globus pallidus [17, 69]. The recurrent artery of Heubner (RAH) usually originates from the ACA at the level of the anterior communicating artery (ACoA) (A1–A2 junction) and courses laterally along the A1 segment of the ACA [4, 69, 77], which may be seen on conventional cerebral angiograms (Figs. 2.2 and 2.3). The RAH may give off two or more vessels to the olfactory system, rectal gyrus and paraterminal gyrus, and finally end up as perforators to supply the basal ganglia. Its extracerebral mean diameter is 662–1,000 mm, and that of the terminal branches, mean, 462 mm [30, 54, 77] (Fig. 2.4). Phylogenetically, the RAH represents the remnant of an anastomotic channel over the tuberculum olfactorium between the ACA and the original stem of the MCA, and it gives rise primarily to the striate arteries, as seen in marsupials and ungulates [3, 98] (Fig. 2.5). In primates, the medial half of this anastomotic channel enlarges so that the ACA supplies the medial striate branches (MSA), and the communication with the MCA eventually disappears (Fig. 2.4). Thus, the ACA eventually supplies regions once fed by the MCA via the enlarged anastomotic channel of the RAH. The remaining posterolateral striate branches, or lenticulostriate arteries (LSA), originate from the MCA. Therefore, the branches of the RAH, which may also be called MSA, and the LSA can be said to represent the same kind of arteries−the MSA, the medial striate branches, and the LSA, the lateral striate, or lenticulostriate branches.

55

2 Intracranial Arterial System: Basal Perforating Arteries

a

b

c

Fig. 2.2 Cerebral angiograms showing the recurrent artery of Heubner (RAH) and lenticulostriate arteries (LSA). (a) Anteroposterior view shows the RAH and its branches (white arrow) and the LSA (black arrow). (b, c) Lateral view with craniocaudal angulation, serial and stereoscopic, shows that the perforators of the RAH and LSA enter the brain together at the anterior perforated substance (black arrows). Because the posterior communicating artery (PCoA) is small, the trunk of the posterior cerebral artery (PCA) is only transiently opacified on initial arterial lateral view (b). On film 0.5 s later (c), however, the PCoA and its perforator (i.e., the thalamotuberal artery) remain filled (open arrowheads) without opacification of the PCA trunk. In such a case with the rudimentary PCoA, therefore, it may appear that the perforator is the only branch of the C7 segment of the internal carotid artery without any apparent PCoA. Anterior choroidal artery (solid arrowhead)

The perforators of the RAH enter the full mediolateral extent in the anterior half of the anterior perforated substance (Fig. 2.6) [83], which may reflect such phylogenetic origin of the RAH as described above. Furthermore, extracerebral anastomosis between the RAH and one of the LSA has been described occasionally [30, 43, 108]. Thus, an accessory MCA, which is an anomalous artery that arises from the ACA to pass into the sylvian

56

a

S. Takahashi

b

Fig. 2.3 The RAH identified on cerebral angiography (reproduced from [98]). A case with an abrupt occlusion of the left middle cerebral artery (MCA) at its origin. Neither the LSA nor the pial vessels of the MCA are opacified; consequently, the course and capillary blush or territory of the RAH are identified. (a) On the AP view, the RAH (arrowheads) originates from the anterior cerebral artery (ACA) at the level of the anterior communicating artery (ACoA) (A1–A2 junction) and extends in a retrograde direction along the A1. After entering the brain, it courses anteriorly and superiorly, following a convex lateral path into the anterior portion of the basal ganglia. (b) On the lateral view, the intracerebral course of the RAH (arrowheads) is roughly parallel to the A2 portion of the ACA, and its distribution is represented by a capillary blush

fissure with the MCA and supplies the cortex in the distribution of the MCA, is suggested to represent a persistent anastomosis between the anterior and middle cerebral arteries over the tuberculum olfactorium [100]. The perforators of the RAH supply the region rostral to the anterior commissure, which includes the anterior portion of the caudate nucleus, anterior third of the putamen, interposed anterior limb of the internal capsule, tip of the outer segment of the globus pallidus, and, less frequently, the anterior hypothalamus [4, 11, 69, 77]. The RAH may also give off some cortical collaterals that supply the paraterminal and rectal gyri, lamina terminalis, anterior perforated substance, olfactory trigone, and caudomedial part of the orbitofrontal cortex [54]. The course and distribution of the striate arteries are observed well on microangiograms (Figs. 2.11–2.16). Perforators from the ACoA are described elsewhere (see Chap. 4 by Fujii).

57


310

290 A2 500 RAH

390

340

860

560

2,000

Fig. 2.4 Diagram showing extra- and intracerebral course and ramification of the RAH (reproduced from [54]) lateral and slightly dorsal and rostral view. Diameters of the RAH and its branches and perforators from the horizontal (A1) segment of the ACA (in black) are indicated by numerals (in microns). Fenestrated ACoA (arrowhead); A2 A2 segment of the right ACA

a

b

Dwindled portion of the anastomotic channel

Anastomotic channel between ACA and MCA Original stem of MCA

ACA OB

Striate branches

RAH

MSA

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OITb OITb

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OCh

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ICA

ICA Pyriform branches of MCA

PCA

Fig. 2.5 Diagram of the phylogenetic development of the RAH drawn based on the study of Abbie [3] (reproduced from [98]). (a) Basal surface of a marsupial forebrain. Note the anastomotic channels between the ACA and the original stem of the MCA, one of which is the predecessor of the RAH. (b) Basal surface of a primate forebrain. The continuation of the ACA channel enlarges and that of the MCA gradually disappears, thus completing the formation of the RAH. ICA internal carotid artery; LSA lenticulostriate arteries; MSA medial striate arteries; OB olfactory bulb; OCh optic chiasm; OlTb olfactory tubercle; PCA posterior cerebral artery

58

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a

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IHF

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RG LOS

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Fig. 2.6 Basal view of the sylvian vallecula showing the perforation sites of basal perforating arteries in the anterior perforated substance (APS) (reproduced from [83]). (a) Entry sites of perforators from the RAH. The optic nerves and chiasm are reflected caudally (inferiorly) to show the medial part of the APS. The two RAH arise near the level of the ACoA, pass laterally above the carotid bifurcation, and give branches to the full mediolateral extent of the APS anteriorly. Left inset: The RAH originates near the junction of the A1 and A2 segments of the ACA. The cross section of the artery at this level is oriented in the transverse plane. These branches arise predominantly from the lateral side of the vessel. Right inset: site of origin of the RAH arising from the A1 segment. The cross section of the artery at this level has an orientation in the sagittal plane. The branches arise predominantly from the superior or posterior–superior surface. (b) Entry sites of the lateral LSA. Because of complex branching, the arteries of the M1 resemble a candelabra as they approach the APS. Inset: They arise predominantly from the posterior, superior, and posterior–superior aspects of the wall. (c) Sites of entry of the individual groups of perforators in the APS. The sites of entry partially overlap, which is most prominent between the perforators of the anterior choroidal artery and the internal carotid artery. The medial striate arteries (MSA) from the horizontal (A1) segment of the ACA enter the brain through posteromedial part of the APS and the LSA, through the posterolateral part; branches of the RAH enter to their full mediolateral extent but are confined predominantly to the anterior half of the APS. A1 perforation site of perforators (MSA) from the A1 segment of the ACA; AChA perforation site of perforators from the anterior choroidal artery; ICA perforation site of perforators from the internal carotid artery; IHF interhemispheric fissure; i-LSA perforation site of intermediate lenticulostriate arteries; Ll limen insulae; l-LSA perforation site of lateral lenticulostriate arteries; LOS lateral olfactory stria; m-LSA perforation site of medial lenticulostriate arteries; MOS medial olfactory stria; OCh optic chiasm OlT olfactory tract; ON optic nerve; OT optic tract; POL posterior orbital lobule; RAH perforation site of perforators from the RAH; RG rectal gyrus

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Fig. 2.7 Histographic representation of the origin of the LSA (reproduced from [108]). The great majority (96%) of the LSA arise along the proximal 17 mm of the MCA

a

CB

b

MCA

ACA ACA

TD

(i)

(ii)

ICA MCA

ICA

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Fig. 2.8 Diagram showing the site of origin and fusion of the LSA (reproduced from [57]). (a) The individual LSA arise from the proximal segment of the MCA as either (i) individual vessels or (ii) sharing a common stem or (iii) from cortical branches (CB)/terminal divisions (TD) or their divisional crotches. (b) Fusion (arrowhead) between a vessel of the LSA and the trunk of the M1 segment. ACA anterior cerebral artery; ICA internal carotid artery

2.2.2 Lenticulostriate Arteries 2.2.2.1 Origin, Course A number of perforating arteries, called the lenticulostriate arteries (LSA), arise from the proximal MCA and enter the brain through the lateral two-thirds of the anterior perforated

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Fig. 2.9 Diagram in AP (a) and lateral (b) views showing the relationship between the site of origin and distribution of the striate arteries (adapted from [105])

Pt CdH CdT

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M1

Fig. 2.10 The relationship between the site of origin along the circumferential wall of the parent MCA vessel and its distribution in the basal ganglia (adapted from [68]). The circle at the bottom represents the cross section of the parent MCA trunk viewed from the lateral side. The artery arising from the anterior wall of the trunk distributes in the more anterior part of the basal ganglia and vice versa. The numerals 1–4 indicate the origin of each artery from the parent MCA trunk in the order from proximal (vessel 1) to distal (vessel 4). The MSA and not the LSA supply the head of the caudate nucleus (CdH). M1 M1 segment of the MCA; CdT caudate nucleus, tail; Pt putamen

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LSA MSA

Fig. 2.11 Coronal microangiogram through the terminal bifurcation of the internal carotid artery. The MSA from the A1 segment of the ACA and the RAH distribute in the inferomedial portion of the basal ganglia (small arrow), whereas the LSA (large arrow) distribute from the M1 segment of the MCA in the superolateral portion of the basal ganglia and run through the putamen, the anterior limb of the internal capsule, and the head of the caudate nucleus. The small vessel that is interposed between the MSA and the LSA may be direct perforators from the internal carotid artery (arrowhead)

substance. They average 9–10.4 (range, 1–21) in number and 100–2,200 mm in diameter at origin [57, 83, 108]. The number and diameter of the LSA correlate inversely; the greater their number, the smaller their diameter, and vice versa [57]. The great majority of the LSA originate along the proximal 17 mm of the MCA trunk (Fig. 2.7) [108]. Although the distinction may be unclear [108], the LSA often divide into medial, intermediate, and lateral groups [83]. The medial LSA, the least constant branches, arise from the MCA just distal to the carotid bifurcation and course directly to enter the anterior perforated substance; the intermediate LSA originate from the middle third of the M1 segment; and the lateral LSA, which are more constant and perhaps larger in diameter than the others, originate from the terminal third of the M1 segment or at the level of the genu of the MCA [57]: Arising most often from the dorsal surface of the MCA trunk, the lateral LSA turn back sharply along the M1 segment with an acute angle at their origin. After coursing medially several millimeters, they curve sharply dorsally and laterally to pierce the anterior perforated substance, thus forming S-shaped loops. Individual vessels of the LSA arise either directly from the MCA trunk or from its cortical branches or terminal divisions or the divisional crotches of these branches and divisions (Fig. 2.8) [57, 108]. Whether the LSA arise from the MCA trunk or from a secondary branch depends on the point where the major division subdivides [43]; larger vessels may divide into several branches before entering the brain substance [43, 83]. The medial LSA enter the anterior perforated substance predominantly in the medial part of the lateral posterior territory; the intermediate LSA, in the central part; and the lateral group, in the lateral part (Fig. 2.6) [83].

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S. Takahashi

a

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RAH MCA

A1 ICA

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Monro

LSA ICA

Fig. 2.12 Coronal microangiograms of the MSA and LSA (reproduced from [98]). (a) Coronal microangiogram through the region of the anterior basal ganglia. Both internal carotid arteries have been retracted inferiorly to demonstrate the cisternal course of the RAH (red arrowhead), which follows a curved or tortuous course along the A1 segment of the ACA. After penetrating the brain, the MSA distribute in the region of the anterior hypothalamus, the anteroinferior portion of the caudate nucleus and putamen, and the interposed anterior limb of the internal capsule. The vessels seen overlying the RAH at the upper aspect of the head of the caudate nucleus represent the terminal portions of the LSA (blue arrow). (b) Section taken more posteriorly through the interventricular foramina. After entering the anterior perforated substance, the LSA (arrow) penetrate the lateral portion of the lenticular nucleus and the superior aspect of the internal capsule and terminate in the caudate nucleus. The ventriculofugal arteries of the LSA cannot be seen (see Fig. 2.31b). The regions lateral to the putamen, consisting of the external capsule, claustrum, and insular cortex, are supplied by the medullary arteries (yellow arrowheads) from the insular segment of the MCA (M2) (insular arteries), not by the basal perforating arteries


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As noted, extracerebral anastomoses between the RAH and one of the LSA have been reported occasionally [30, 43, 108]; a large LSA can arise from the trunk of the MCA and fuse with the trunk [57] (Fig. 2.8).

2.2.2.2 Intracerebral Course and Distribution After entering the brain, the LSA slant laterally, arc around and through the putamen, and course superomedially through the superior part of the internal capsule and much of the caudate nucleus [91]. According to Taveras and Wood’s textbook [105], of the striate arteries that include the MSA (including the perforators of the RAH) and the LSA, the more medially a branch originates from its parent artery, the more anteriorly it distributes in the basal ganglia, and vice versa; on the whole, the branching arteries resemble a fan with its pivot on the anterior perforated substance (Fig. 2.9). However, this rule requires further investigation because it is also reported that the area supplied by each LSA is unrelated to the distance of its origin along the MCA trunk (proximal or distal) from the terminal bifurcation of the internal carotid artery (ICA) [68]. Rather, the supply area is related to its site of origin along the circumferential wall of the parent MCA vessel; the more anterior an artery originates on the MCA wall, the more anterior is its supply of the basal ganglia, and vice versa (Fig. 2.10).

2.2.2.3 Territories The territories of the medial, intermediate, and lateral groups of LSA are not clearly defined. The smaller medial branches have the shortest courses and usually terminate in the lateral segment of the globus pallidus, while the larger lateral LSA supply the putamen, superior part of the internal capsule, and caudate nucleus [29, 91]. Charcot’s artery of cerebral hemorrhage is the name given the prominent lateral LSA [29]. On the whole, the LSA supply the body of the caudate nucleus as well as the superior aspect of its head, the superior part of the internal capsule, the putamen, the lateral segment of the globus pallidus, the substantia innominata, and the lateral half of the anterior commissure [5, 6, 40, 91].

2.2.3 Distribution of the Striate Arteries on Microangiograms The striate arteries that include the perforators of the RAH (MSA) and the LSA diverge into a large part of the corpus striatum on the whole (Figs. 2.11–2.16). Among them, the MSA of the RAH distribute to the inferior part of the anterior basal ganglia. The anterior branches of the LSA distribute superiorly and anteriorly over the area of the RAH, and the posterior branches ascend superiorly and posteriorly and distribute laterally and superiorly over the branches of the anterior choroidal artery. Thus, the MSA supply the inferior portion of the anterior limb of the internal capsule; the anterior choroidal artery supply most of the inferior portion of the posterior limb; and the LSA supply the superior segments of

64 Fig. 2.13 Sagittal microangiograms. (a) Sagittal microangiogram 2-cm thick centered 2 cm to the left of the midline illustrates the anterior course of the RAH and their distribution to the anteroinferior portion of the basal ganglia (arrow). Many of the vessels superior and posterior to the RAH are LSA. Th: thalamus (reproduced from [98]). (b) Sagittal microangiogram 1-cm thick through the lateral portion of the basal ganglia. The LSA diverge superiorly into a large part of the corpus striatum, assuming a fan shape with the apex downward

S. Takahashi

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LSA

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A nt

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A nt

Fig. 2.14 Sagittal microangiogram shows the RAH distributed in the anterior inferior part of the striatum (arrow) (reproduced from [86]). A robust trunk of the RAH (arrow) proceeds anterosuperiorly to the head of the caudate nucleus, giving off tiny rami

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both limbs [2, 7, 8, 11, 112]. The thalamotuberal branches (TTA) of the posterior communicating artery (PCoA) [7, 8] and probably the perforators from the ICA supply the genu and most anterior portion of the posterior limb. Distribution of the striate branches varies by the degree to which the ACA has taken over the territory of the MCA and how much is still supplied by the MCA. To some extent, distributions of the RAH and LSA are balanced; if the RAH vessels are small, the LSA predominate, and vice versa. For example, in the head of the caudate nucleus and the anterior limb of the internal capsule, the areas supplied by the MCA and ACA are complementary [113, 114]. Shellshear [88] described claustral arteries that originate from the lateral end of the M1 segment of the MCA and supply the claustrum and external capsule, but Herman et al. [40] and Stephens and Stilwell [91] refuted the existence of such vessels. Instead, the insular

a

b MSA MSA LSA-1

LSA-3

Fig. 2.15 Contiguous transaxial microangiograms (10-mm sections) traversing the (a) most inferior portion, (b) midportion, (c) top of the corpus striatum and the (d) corona radiata. (e) A diagram of the courses of the medial striate (MSA) (red) and lenticulostriate arteries (LSA) (black) (reproduced from [98]). The branches of the RAH course anteriorly, following a slightly convex path into the anteroinferomedial portion of the corpus striatum (pink arrows). The vertical branches of the LSA, located immediately above the anterior perforated substance, appear as dense spots (arrow LSA-1). Some branches of the LSA course anteriorly (arrow LSA-2) and superiorly and partially overlap the branches of the RAH. Other branches of the LSA (arrow LSA-3) course posteriorly and superiorly into the putamen, the superior portion of the posterior limb of the internal capsule, and the body of the caudate nucleus. Thus, the branches that course posteriorly distribute superiorly and laterally over the region of the anterior choroidal artery in the globus pallidus and inferior aspect of the posterior limb of the internal capsule (not shown). The insular arteries supply the external capsule and claustrum, which are located lateral to the putamen (yellow arrowheads). At the level of the corona radiata (d), the periventricular white matter is supplied by numerous fine medullary arteries from the pial vessels over the opercular cortex

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Fig. 2.16 Transaxial microangiogram shows the area supplied by the MSA (reproduced from [98]). The area supplied by the MSA, including the RAH, appears as a capillary blush following injection of contrast material into the proximal portion of the ACA, which has been tied off just distal to the origin of the RAH. The distribution of the RAH is seen as a capillary blush (arrowheads) posterolateral to the most inferior aspect of the frontal horn, shown as a thin radiolucent zone. The inferior portions of the caudate nucleus and putamen and anterior limb of the internal capsule appear to be included within the capillary blush

arteries, which are medullary arteries of the insular pial arteries, or the M2 segment of the MCA, primarily supply the insular cortex, extreme capsule, and, occasionally, the claustrum and external capsule, but not the putamen [107, 115]. Some of the prominent long insular arteries that originate around the central insular sulcus or in the posterior insular region may partially supply the corona radiata that includes the corticospinal tract. Our injection study also indicated that the insular arteries, but not the basal perforators of the MCA (the LSA), supply all structures lateral to the putamen (Figs. 2.12 and 2.15). Therefore, we find that areas lateral to the putamen are unaffected by infarction involving nearly the entire territory supplied by the LSA (Figs. 2.19 and 2.20). Infarcts in the insular and opercular regions also frequently spare the corpus striatum, but usually involve the claustral region just lateral to the corpus striatum.

2.2.4 Imaging of Infarcts in the Distribution of Striate Arteries Infarcts in the area supplied by the MSA, including the RAH, usually involve an area just posterolateral to the most inferior part of the frontal horn of the lateral ventricle and include the inferior portion of the head of the caudate nucleus and the anterior limb of the internal capsule (Figs. 2.17 and 2.18). Occasionally, however, infarction develops in the more superior portion of the head of the caudate nucleus and the anterior limb of the internal capsule [98]. Neurological symptoms of infarct in the MSA distribution are unclear, perhaps because lesions are frequently accompanied by infarcts or dysfunction caused by impaired circulation

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a

c

e

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f

Fig. 2.17 Infarct in the region of the MSA from the RAH. Magnetic resonance angiograms (MRA) of a 69-year-old woman with clinical diagnosis of depression showed two aneurysms. After surgery for both aneurysms with placement of titanium clips, she exhibited no evident neurological symptoms. (a) Preoperative MRA shows two aneurysms arising at the ACoA (arrow) and at the bifurcation of the right MCA (small arrow). (b) Postoperative MRA shows no aneurysms but provides less visualization of vessels adjacent to the sites of the aneurysms, which may represent susceptibility artifacts. Vasospasm may be present in and around the ACoA (arrow). (c) Postoperative T2-weighted image and (d) sagittal and (e, f) coronal images reformatted from MRA data show an infarct in the right anteroinferior portion of the corpus striatum, probably representing the distribution of the RAH (arrowheads)

2 Intracranial Arterial System: Basal Perforating Arteries Fig. 2.18 (a) Fortyeight-year-old man who developed nausea and vertigo and was apathetic and disoriented at examination. No apparent hemiparesis was present (reproduced from [104]). (a) Axial and (b) coronal T2-weighted images and (c) sagittal T1-weighted image show a lesion (arrows in a, b and c) involving the anteroinferior portion of the basal ganglia just posterior to the inferior-most part of the frontal horn on the left, along the distribution of the MSA

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of other vascular territories of the ACA, such as in the area supplied by perforators from the ACoA (subcallosal artery) or the area of the paracentral lobule that includes the motor area. Patients with infarcts localized to the distribution of the MSA that do not involve the area supplied by the cortical ACA may show mild hemiparesis with brachial predominance and psychosomatic symptoms that include apathetic tendency and decreased volition [15, 23, 61, 98, 117]. Involvement of the anterior portion of the hypothalamus and/or the corpus striatum may cause the psychosomatic symptoms. Figures 2.19–2.22 show extensive LSA lesions and smaller examples limited to anterior or posterior branches of the LSA. In several contiguous axial sections traversing the basal gray matter, infarcts along the LSA distribution are quite small at lower levels but

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larger in higher sections (Fig. 2.20). This finding reflects the superiorly diverse distribution of the LSA but, on axial images, can sometimes cause erroneous diagnosis of multiple small infarcts involving the putamen and paraventricular areas. Computed tomography (CT) and magnetic resonance (MR) imaging appearance of infarcts in the areas supplied by the MSA and LSA may vary by striate artery distribution; for example, an infarct in the area supplied by the MSA (including the RAH) may or may not involve the superior portions of the head of the caudate nucleus and the anterior limb of the internal capsule. Patients show motor disturbances of varying severity, hemihypesthesia, and sometimes aphasia, probably resulting from involvement of the superior portion of both limbs of the internal capsule near the corona radiata.

a

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Fig. 2.19 Extensive infarct in the distribution of the LSA (reproduced from [98]). (a) Preoperative angiogram of a 58-year-old woman shows an aneurysm of the ACoA and another that involves the sphenoidal (M1) segment of the left MCA, just at the origin of two well developed branches of the LSA (small arrows). At surgery, the wall of the MCA aneurysm and its parent artery were lacerated, and both main branches of the LSA were removed when the wall was sutured. She developed severe right hemiparesis, moderate right hemihypesthesia, dysarthria, and slight sensory aphasia following surgery. (b) The postoperative angiogram shows a localized filling defect (large arrow) at the site of the previous aneurysm, seen as narrowing of the sphenoidal portion of the MCA, as well as occlusion of the branches of the LSA. (c–e) Computed tomographic (CT) scans show infarction of nearly the entire distribution of the LSA that involves most of the left corpus striatum and barely spares the anteroinferior portion. Note that the insular cortex and its subjacent external capsule appears unaffected.

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2.3 Anterior Choroidal Artery and Carotid Branches 2.3.1 Anterior Choroidal Artery 2.3.1.1 Phylogenic Development Abbie extensively analyzed the phylogenic development of the anterior choroidal artery (AChA) [2, 3], which begins as a small vessel called the inferior cerebral artery of Dendy that

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Fig. 2.20 Extensive infarct in the distribution of the LSA (reproduced from [95]). A 65-year-old man who developed sudden loss of consciousness, severe right hemiparesis, right hemihypesthesia, and dysarthria. A discrete decrease in intensity on (a), (b) axial, (c) coronal, and (d) sagittal T1-weighted images reveals a well defined infarct (arrows) in chronic stage that involves nearly the entire territory of the LSA on the left. Note that the area just posterolateral to the inferior part of the frontal horn is spared, which corresponds to the area of the MSA. Also note that the upper part of the internal capsule near the corona radiata is involved on coronal image, while the insular cortex and its subjacent external capsule remains unaffected.

distributes to the paleostriatum and the pyriform cortex in the sphenodon, a phylogenically lower reptile (Fig. 2.23). This small vessel runs posteriorly along the optic tract and anastomoses with the caudal division (predecessor of the posterior cerebral artery (PCA) in the crocodile, a higher species of reptile). Because the vessel has no choroidal branches, it is not a true choroidal artery at this stage. Because both the lateral ventricle and choroid fissure assume an arcuate form in mammals as the cerebrum develops, the posterior part of the AChA comes to lie alongside the anteroinferior end of the elongated choroid fissure and acquires some choroidal branches from the PCA, thus completing the AChA in the true sense.

2.3.1.2 Origin and Segments In each of 778 human hemispheres studied by Otomo, the human AChA was present and arose from the ICA in all but a few exceptions [70, 82, 103]. It normally originates from the posterior aspect of the supraclinoid ICA just proximal to the terminal bifurcation of the ICA but distal to the origin of the PCoA. At their origins, the diameter of the AChA ranges from 0.7 to 2.0 mm (mean, 1.2 mm), and that of the PCoA averages 2.1 mm [82]. The AChA consists of the cisternal and plexal segments (Fig. 2.24). The cisternal segment

2 Intracranial Arterial System: Basal Perforating Arteries Fig. 2.21 An infarct in the anterior part of the striatum, representing the anterior branch territory of the LSA (arrows). (a) Axial T2-weighted image and (b) coronal and (c) sagittal proton-density-weighted images

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extends from its origin to the choroidal fissure and measures 20 to 34 mm (mean, 24 mm) long. It initially courses posteromedially, crosses the optic tract from the lateral to the medial side, and runs posteriorly along the medial border of the tract to reach the lateral margin of the cerebral peduncle (Fig. 2.25) [2]. At the anterior pole of the lateral geniculate body, it recrosses the optic tract from medial to lateral to arrive superomedially to the uncus and then passes through the choroidal fissure to supply the temporal portion of the choroid plexus.

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Fig. 2.22 Infarct in the posterior part of the putamen, representing the posterior branch territory of the LSA. (a, b) Axial T2-weighted images and (c) axial, (d) sagittal, and (e) coronal diffusion-weighted images show a small infarct (arrowheads) that involves the posterior end of the putamen inferiorly and the posterior periventricular region superiorly, but not the posterior limb of the internal capsule. The extent of the lesion mildly diverges superiorly

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Fig. 2.23 Schematic drawings show phylogenic development of the AChA (based on the study of Abbie [3] and reproduced from [103]). (a) Sphenodon (phylogenically lower reptile). The AChA begins as a small vessel called the inferior cerebral artery of Dendy (ICAD), which arises from the cranial division of the ICA, courses along the optic tract (OT), and nourishes the posterior part of the OT, a part of the amygdaloid body, and the paleostriatum. (b) Crocodile (higher species of reptile). The ICAD runs more posteriorly along the OT and terminates in caudal division. This vessel is a predecessor of the AChA, although it has acquired no choroidal branches. It must be remembered that in reptiles, the lateral ventricle (LV) has no temporal horn; the choroid fissure is limited to the region of the foramen of Monro; and the choroidal branches of the PCA pass into this region and suffice for its requirements. (c) Marsupial (a mammal). Both the LV and choroid fissure assume arcuate form with expansion and rotation of the cerebrum. Thus, the posterior part of the AChA comes to lie alongside the anteroinferior end of the elongated choroid fissure and acquires some choroidal branches from the PCA to the anteroinferior part of the choroid plexus, thereby completing the AChA. In ascending mammalian scale, as the cerebrum and LV and the functional demands of an enlarging choroid plexus grow, the contribution of the AChA to the choroid plexus progressively increases. ACA anterior cerebral artery; BA basilar artery; CdDv caudal division of the internal carotid artery; ChBr choroidal branch; ChP choroid plexus; CrDv cranial division of the internal carotid artery; ICA internal carotid artery; ICAD inferior cerebral artery of Dendy; LVt temporal horn of the lateral ventricle; LGB lateral geniculate body; LPChA lateral posterior choroidal artery; LV lateral ventricle; MCA middle cerebral artery; OT optic tract; PCA posterior cerebral artery; PCoA posterior communicating artery

76 Fig. 2.24 Lateral carotid angiograms showing the AChA. (a) The AChA originates from the ICA distal to the origin of the PCoA and divides into cisternal and plexal segments by the inferior choroidal point (arrow). The plexal segment comprises medial (small arrow) and lateral (arrowhead) branches. (b) Many fine branches are seen ascending from the cisternal segment (arrowhead). Inferior choroidal point (arrow)

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The plexal segment of the AChA typically gives rise to medial and lateral trunks [53, 106]. The medial plexal trunk courses medially along the attachment of the choroid plexus close to the choroidal fissure, and the lateral plexal trunk runs posteriorly and laterally to reach the free margin of the choroid plexus, ramifying numerous intrachoroidal branches. Some branches of the AChA may pass posterior into the atrium of the lateral ventricle and then forward above the thalamus to supply the choroid plexus of the body of the lateral ventricle as forward as the foramen of Monro [82].

2.3.1.3 Branches, Distribution, and Microangiographic Findings The cisternal part of the AChA gives rise to multiple slender branches that may be divided into superior perforating and superficial cortical arteries [106]. The perforating arteries range in number from 2 to 9 (mean, 4.6) and in diameter between 90 and 600 mm (mean, 317 mm) [50]. They extend into the substance of the brain, coursing on either side of the optic tract or through it (Fig. 2.25) [106]. The more proximal perforators extend superiorly through the posterior part of the anterior perforated substance (Fig. 2.6) [83] into the medial half of the globus pallidus.

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2 Intracranial Arterial System: Basal Perforating Arteries Fig. 2.25 The base of the brain dissected to show the general course and relationships of the AChA (adapted from Abbie [2]). Anastomoses are noted between the AChA and the lateral posterior choroidal artery (LPChA). APS anterior perforated substance; ACA anterior cerebral artery; ChP choroid plexus; CP cerebral peduncle; ICA internal carotid artery; LGB lateral geniculate body; LVt temporal horn of the lateral ventricle; M mamillary body; OCh optic chiasm; OT optic tract; PCoA posterior communicating artery; MCA middle cerebral artery; Pu pulvinar; RN red nucleus; SN substantia nigra

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CP SN

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The more distal perforators are commonly single and larger than other perforators, arise close to the lateral geniculate body and just in front of the temporal horn of the ventricle [50], and extend superiorly to supply the inferior half of the posterior two-thirds of the internal capsule (under the level of the upper border of the globus pallidus), the retrolenticular portion of the internal capsule, and the tail of the caudate nucleus [2, 8, 39, 91, 106] (Figs. 2.26–2.29). These perforators also supply a middle third of the rostral cerebral peduncle, a portion of the substantia nigra, the red nucleus, the subthalamic nucleus, and, sometimes, an adjacent area in the lateral portion of the thalamus [79]. Occasionally, the cisternal segment also gives rise to additional small branches that pass through the choroid fissure to supply the choroid plexus [24]. Although Plets’s group [79] have indicated that the AChA contributes to vascularization of the thalamus via cisternal perforators as well as vessels arising from its plexal portion, their series did not examine infarction involving the AChA. Infarcts of the region of the AChA have been reported [102] primarily to involve the posterior limb of the internal capsule, the internal segment of the globus pallidus, and, possibly, a lateral portion of the ventral lateral nucleus (VL) of the thalamus [79]. However, some authors exclude the thalamus from the AChA territory of supply because vascularization of this territory is only irregular and superficial [16, 76].

78 Fig. 2.26 Sagittal section microangiograms (a) 1.5 cm and (b) 2 cm from the midline (different specimens) (reproduced from [97]). (a) The proximal cisternal part of the AChA (arrow) is shown arising from the posterior aspect of the distal internal carotid artery and giving off a number of fine superior perforating branches (arrowheads). Some other fine vessels anterior to them (open arrowhead) may be direct perforators of the internal carotid fork. (b) Slightly more laterally, fine perforating vessels from the distal cisternal part of the AChA (solid arrowhead) ascend to the regions of the globus pallidus and internal capsule between the striatum (LSA) anteriorly and thalamus (Th) posteriorly. Some other fine vessels anterior to them (open arrowhead) may be carotid perforators. A tiny uncal branch is also shown (small yellow arrow). MCA middle cerebral artery; PCA posterior cerebral artery; U uncus

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The cortical branches of the AChA help supply the uncus, posterior medial part of the amygdaloid body, and, occasionally, the anterior end of the hippocampus, the optic tract, and the lateral horn of the lateral geniculate body and the beginning of the optic radiation [1, 2]. The lateral posterior choroidal artery (LPChA) entirely supplies the medial horn of the lateral geniculate body, and the AChA and LPChA anastomose with each other to supply the intervening hilar region [1, 106]. A reciprocal relationship has been noted between the field of supply of the AChA and the nearby arteries. In cases with a smaller number of AChA perforators, the ipsilateral ICA gives rise to several more perforators than usual that are distributed to the areas commonly supplied by the proximal perforators of the AChA [50, 82]. When the PCoA is absent, which is rare, or very small in diameter, some or most of the hypothalamic (premamillary) arteries

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2 Intracranial Arterial System: Basal Perforating Arteries Fig. 2 27 Coronal section microangiograms through the interpeduncular fossa (reproduced from [97]). (a) The transitional portion of the cisternal and plexal parts of the AChA can be seen (arrow). The most distal part of the cisternal segment of this artery gives off a prominent perforator that ramifies a number of fine branches (arrowheads), which run upwards to penetrate the globus pallidus and the inferior portion of the posterior limb of the internal capsule, barely terminating at the lateral border of the thalamus (Th) but not reaching the lateral ventricular wall. The branches of the AChA also supply the roof of the temporal horn, probably including the tail of the caudate nucleus (long arrow). They may represent a kind of subependymal arteries (SEA) of choroidal arteries. Laterally and superiorly, more robust branches of the lenticulostriate arteries (LSA) distribute in the putamen and the superior part of the internal capsule and reach the caudate nucleus along the lateral wall of the body of the lateral ventricle. The uncal branch (open arrow head) runs downward along the medial margin of the uncus into the uncal sulcus to the head of the hippocampal formation. The proximal part of the PCA is shown. (b) Coronal microangiogram through the most proximal part of the PCA from another specimen again shows very similar features of the AChA. LVt temporal horn of the lateral ventricle

a

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arise from the AChA. Also, rarely, branches usually belonging to the AChA may arise from the PCoA to supply the genu and the anterior third of the posterior limb of the internal capsule [29, 82]. Such inverse relationships occur between the PCA and the AChA in the supply of the cerebral peduncle, subthalamic nucleus, lateral geniculate body, and so on [82]. Anastomoses: The AChA has rich superficial anastomoses with adjacent arteries [82, 106]. Anastomoses with the PCoA occur on the surface of the optic tract and cerebral

80 Fig. 2.28 Contiguous axial section microangiograms of cadaver brain (reproduced from [97]). (a) A section traversing the midbrain shows the course of the AChA (arrow) along the medial margin of the uncus to the choroid plexus (ChP) in the temporal horn of the lateral ventricle. uncal branch (open arrowhead). MSA medial striate arteries. (b) Axial section 1 cm above (a). Minute branches are seen in the posterior limb and retrolentiform portion of the internal capsule and in the globus pallidus (arrowheads) between the basal ganglia anterolaterally and the thalamus (Th) posteromedially. LSA lenticulostriate arteries

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peduncle, with the PCA on the surface of the lateral geniculate body and the uncus of the temporal lobe, and within the choroid plexus (Fig. 2.30). In addition, there are anastomoses with branches from the ICA and MCA in the area of the anterior perforated substance, and on the temporal lobe. These rich anastomoses may explain the inconsistent results with favorable course of the proximal AChA occlusion and the rarity of the classic syndrome described by Abbie [1, 2, 13, 14, 81, 82, 106].

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Fig. 2.29 Structures fed by the AChA (modified from [97]). (a) Coronal section. (b) Lateral view. Am amygdaloid body; Cd caudate nucleus; ChP choroid plexus; CP cerebral peduncle; GP globus pallidus; ICA internal carotid artery; ICp posterior limb of the internal capsule; LGB lateral geniculate body; LPBr lateral plexal branch of the AChA; MPBr medial plexal branch of the AChA; OT optic tract; Pt putamen; RN red nucleus; SN substantia nigra; Sth subthalamus; Th thalamus; U uncus

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Fig. 2.30 Anastomoses of the AChA with the PCoA-PCA system (reproduced from [103]). The AChA has anastomotic channels (1) over the optic tract with branches from the PCoA; (2) over the cerebral peduncle with the proximal PCA; (3) over the pyriform cortex (uncal branches) with the PCA branches (temporal and hippocampal branches); (4) over and around the lateral geniculate body (LGB) with the PCA branches, including the lateral posterior choroidal artery (LPChA); and, finally, (5) in the choroid plexus (ChP) with the LPChA. ACA anterior cerebral artery; ICA internal carotid artery; ITA inferior temporal artery of the posterior cerebral artery; MCA middle cerebral artery; OCh optic chiasm; ON optic nerve; OT optic tract; UB uncal branch of the anterior choroidal artery

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2.3.1.4 Subependymal Arteries (SEA) Marinkovic et al. [51] found tiny vessels that supply the walls of the lateral ventricle, called subependymal arteries (SEA), which they considered to be the ventriculofugal arteries reported by Van den Bergh [109, 111, 112] (Fig. 2.31). Theron’s group similarly described small vessels branching from the medial plexal branch of the AChA to supply the roof of the temporal horn and anterior wall of the atrium as well as the choroid plexus [106]. However, the existence of these tiny vessels was once refuted [67]. According to Marinkovic et al. [51], the SEA arise most often from the plexal segment of the AChA (from 1 to 3 in number) and the LPChA (1–10 in number), at the level of the choroid fissure in both cases. The SEA of the AChA supply the walls of the temporal horn 100%, occipital horn 85%, and atrium 35% [51]; related closely with the inferior ventricular vein, they supply the superolateral wall of the temporal horn (Fig. 2.27a) and, occasionally, the stria terminalis and tail of the caudate nucleus. The SEA of the LPChA perfuse the walls of the occipital horn 15%, atrium 65%, body of the ventricle 100%, and, partially, the frontal horn [51]. At the level of the body of the ventricle, after passing beneath the thalamostriate vein, the SEA may terminate in the caudate nucleus or, occasionally, reach the superolateral angle of the lateral ventricle, whereas penetrating callosal twigs of the pericallosal artery supply the superior angle (callosal wall). The SEA of the medial posterior choroidal artery (MPChA) provide 10% of the nourishment of the body and frontal horn. The branches of the LPChA and the MPChA that supply the dorsal aspects of the thalamus may be included as this kind of vessels. The SEA, or ventriculofugal arteries, can sometimes be observed on microangiograms (Figs. 2.32 and 2.33), and this group of vessels and their extent of supply require further study.

Fig. 2.31 SEA and ventriculofugal arteries. (a) Coronal section of the brain illustrating the SEA in the periventricular region of the lateral ventricle (reproduced from [51]). Note a SEA that arises from a choroidal branch of the lateral ventricle (ChBr). (b, c) Coronal sections of the brain illustrating ventriculofugal arteries (reproduced from [110]). Van den Bergh described two kinds of periventricular centrifugal arteries that penetrate into the brain parenchyma and diverge ventriculofugally and radially towards the centripetal medullary arteries of the cerebrum (from the brain surface) but that do not make anastomoses: (b) terminal branches of the striate arteries around the frontal horn and body of the lateral ventricle and (c) terminal branches originating from choroidal arteries in the atrium and posterior horn of the lateral ventricle. 3V third ventricle; AChA anterior choroidal artery; CalB callosal branch; CCb corpus callosum, body; ChF choroid fissure; ChP choroid plexus; CorA cortical arteries; CR corona radiata; CSO centrum semiovale; Fx fornix; IC internal capsule; ICA internal carotid artery; LPChA lateral posterior choroidal artery; LSA lenticulostriate arteries; LMAn leptomeningeal anastomoses; LVa lateral ventricle, atrium; MdA medullary artery of the cerebrum; MPChA medial posterior choroidal artery; PCalA pericallosal artery; SLA superolateral angle of the lateral ventricle where some SEA terminate occasionally; Th thalamus; VfA ventriculofugal arteries

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Fig. 2.32 Microangiogram demonstrating the subependymal arteries (SEA). Microangiogram shows ventriculofugal arteries, or SEA, bilaterally in the periventricular region along the trigone of the lateral ventricle (arrowheads). In this specimen, these vessels appear to originate from the choroid plexus of the lateral ventricle

2.3.1.5 Clinical Features and Imaging Findings of Infarcts in the AChA Territory Clinical features: Infarct in the AChA territory is rare and can produce a triad of symptoms that include hemiplegia, hemianaesthesia, and homonymous hemianopia; however, the syndrome is most frequently incomplete [16]. Hemiplegia, the most constant clinical manifestation, is caused by the interruption of the corticospinal fibers that descend in the posterior limb of the internal capsule and the cerebral peduncle. Hemianaesthesia, usually incomplete and temporary in this syndrome, is attributable to the involvement of superior thalamocortical radiation [35]. Homonymous hemianopia is generally attributed to involvement of the optic radiation, although the AChA supplies the visual system at three separate loci, including the optic tract, lateral geniculate body, and origin of the optic radiation in the retrolentiform portion of the internal capsule [35]. Superior quadrantanopia can occur when the lateral geniculate body is involved because the upper quadrant of the visual field is represented anterolaterally in that structure, in the area supplied by the AChA. Left-sided spatial neglect may accompany right-sided lesions, and slight disorders of speech may occur with left-sided lesions [16, 35]. Imaging: On CT and MR imaging, the distribution of AChA infarcts varies and is smaller than that found in the injection studies, which may be partially attributable to the rich anastomoses of the AChA with adjacent vessels. On transaxial images, the lesion is generally confined to an arcuate zone between the striatum anterolaterally and the thalamus posteromedially and centered in the posterior limb of the internal capsule, sparing the thalamus medially and encroaching upon the tip of the globus pallidus laterally (Figs. 2.34–2.36). Involvement of the posterior limb of the internal capsule is constant, but that of other structures, such as the uncus, globus pallidus, tail of the caudate nucleus or cerebral peduncle, is only occasional [101]. Furthermore, the thalamus appears to be barely spared posteromedially and only superficially involved, if at all. Extension of lesions in the posterior limb of the internal capsule predominates in its posterior two-thirds and is limited to the inferior portion, not extending to the corona radiata.

2 Intracranial Arterial System: Basal Perforating Arteries Fig. 2.33 Consecutive coronal microangiograms demonstrate the SEA. (a, b) Microangiograms show ventriculofugal arteries in the periventricular region along the temporal horn and trigone of the lateral ventricle (arrowheads). They appear to originate from the choroid plexus or the lateral posterior choroidal artery

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Box 2.1 Does the anterior choroidal artery supply the paraventricular region? Infarction of the AChA has been the subject of several reports that demonstrate lesions on CT or MR imaging. Although a few studies have interpreted infarcts in the territory of the AChA based on angiographic findings [101, 102], more frequently, CT or MR evidence has been used without angiographic or autopsy confirmation [16, 35, 36, 66, 92]. However, the decision to ignore angiographic or autopsy information can lead to erroneous diagnosis of AChA infarcts.

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Mohr et al. [64] pointed out the error of Helgason’s team [37] in including the corona radiata and the paraventricular white matter in the territory of the AChA when they attributed a series of 23 infarcts to AChA occlusion based on CT and/or MR imaging findings without angiographic evidence, and Nelles’s group [66] recently reported that some lesions interpreted as AChA infarction on MR images apparently involved the posterior part of the putamen, extended to a considerably large lesion in the periventricular region of the body of the caudate nucleus and corona radiata, but spared the corticospinal tract in the posterior limb of the internal capsule. We presume, though, that such lesions, which resemble that in Fig. 2.22 with a superiorly diverging extent, would represent infarcts of the posterior branches of the lenticulostriate arteries (LSA) rather than the AChA. We also feel that a lesion that extended to a large involvement in the posterior periventricular region on MR images that was interpreted by Helgason in another report [36] as an infarction in the territory of the AChA actually represented a lesion in the territory supplied by the LSA. Hupperts and Lodder [41] have claimed that infarcts in the AChA territory often extend upward into the posterior paraventricular corona radiata. Although this may rarely be correct, my impression is that it is usually incorrect especially regarding lesions with a considerable extent in the periventricular region [101, 102]: an extensive AChA lesion may certainly extend posterosuperiorly from the posterior limb of the internal capsule (but not the putamen) toward the lateral margin of the lateral ventricular body along the lateral margin of the thalamus as in Fig. 2.35, the lesion usually attenuates superiorly to an only limited extent if any. Coronal microangiograms (Fig. 2.27) reveal that the fine perforating arteries of the AChA apparently do not reach the ventricular wall, whereas the more robust branches of the LSA do traverse the superior part of the internal capsule to reach the caudate nucleus along the ventricular margin. How much the subependymal arteries (SEA) or ventriculofugal arteries contribute to the supply of this region is unclear, but if present, they should derive rather from the LPChA than the AChA. Thus, I rather agree with Mohr’s group that the corona radiata and the paraventricular white matter likely lie outside the supply area of the AChA. To avoid improper conclusions when considering the clinical significance of images of the territories of lesions, such as in determining whether an AChA infarct is small-artery occlusive disease, large artery disease, or cardioembolism, more careful deliberation is needed with accurate knowledge about the supply areas of individual perforators.

2.3.2 Direct Perforators of the Internal Carotid Artery Mentioned only briefly in the literature, these arteries are said to distribute in the region of the genu of the internal capsule [5, 17, 93]. However, their specific course remains to be defined. The supraclinoid portion of the ICA subdivides into ophthalmic (C6), communicating (C7), and choroidal (C8) segments [27] (See Fig. 1.2 in Chap. 1). Of the three, the

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Fig. 2.34 Diagram of the distribution of lesions in 12 angiographically verified cases with an AChA infarct on axial sections through the (a) midbrain, (b) junction of the midbrain and diencephalon, and (c) thalamus (reproduced from [101]). Stippled areas represent individual infarcts; denser portions represent overlapping lesions. Although variable, the lesions are generally distributed in an arcuate zone between the striatum anterolaterally and the thalamus posteromedially. AC anterior commissure; Aq aqueduct of Sylvius; Cbll cerebellum; Cd caudate nucleus; ChP choroid plexus; CP cerebral peduncle; Fx fornix; Hb habenula; Hth hypothalamus; ICa anterior limb of the internal capsule; ICp posterior limb of the internal capsule; LGB lateral geniculate body; M mamillary body; MGB medial geniculate body; PB pineal body; RN red nucleus; SCo superior colliculi; SN substantia nigra; Sth subthalamus; Th thalamus; U uncus; 3V third ventricle

ophthalmic segment (C6) gives off the superior hypophyseal arteries that pass to the optic nerve and chiasm, infundibulum, and floor of the third ventricle [27]. The superior hypophyseal arteries pass to the infundibulum of the pituitary gland and form the circuminfundibular plexus with the infundibular arteries that arise from the PCoA. The communicating segment (C7) gives off no branches in 60% of cases but may give off a few branches that distribute to the optic tract and premamillary part of the floor of the third ventricle. Branches (average four) are most frequent from the choroidal segment (C8) of the ICA, mainly from the posterior surface of the ICA (76%), and these terminate in descending order of frequency at the anterior perforated substance, optic tract, and uncus. The basal perforators of the ICA (ICAp) enter the brain primarily by penetrating the posterior portion of the anterior perforated substance near the optic tract (Fig. 2.6) [83]. They vary from 1 to 6 in number (mean, 3.1) with diameters of 70–470 mm (mean, 243 mm) [59]. They mostly arise from the caudal surface of the choroidal segment of the ICA, with 10% arising directly from the crotch of the ICA (Figs. 2.11 and 2.26). Information is scarce about the intraparenchymal supply area of these perforators, although it appears to be just anterior to the area of the AChA based on report of perfusion of the genu of the internal capsule and adjacent part of the globus pallidus, and the anterior end of the posterior limb of the internal capsule [83]. Only rarely do we encounter discrete infarcts limited to this region (Figs. 2.37 and 2.38).

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a

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c

d

Fig. 2.35 A 70-year-old woman with extensive AChA infarct (reproduced from [101]) who suddenly developed transient left hemiparesis and dysarthria. CT scans obtained soon after the ictus showed no evidence of stroke. (a) AP and (b) lateral views of right carotid angiogram soon after the ictus disclose no evidence of obstructive arterial diseases, but a saccular aneurysm is arising at the terminal portion of the ICA (arrow). The AChA cannot be identified, probably obscured by the overlapping middle cerebral branches. (c) AP and (d) lateral views (with craniocaudal angulation for the purpose of obviating overlap between the anterior choroidal origin and middle cerebral branches) of right carotid angiograms repeated about a week later because her condition worsened disclose complete disappearance of the aneurysm (arrow). The AChA is not opacified. Thus, the AChA was assumed to be occluded in association with spontaneous thrombosis of the aneurysm, which should have arisen at the origin of this artery. Vertebral angiograms did not fill the AChA in a retrograde fashion (not shown). (e–h) Transaxial CT scans show an infarction (blue arrow) in the regions of the uncus, the posterior limb and retrolenticular portion of the internal capsule, a part of the globus pallidus, and the middle third of the cerebral peduncle (yellow arrowhead) on the right side. A calcified nodule in the right sylvian vallecula probably represents an aneurysm (red arrow). The aneurysm was presumed to have spontaneously thrombosed and occluded the parent artery (the AChA), thus causing extensive infarct in the territory of this artery. Dashed lines in (e) and (f) indicate the planes for coronal and sagittal reformatted images (i) and (j). (i) Coronal and (j) sagittal reformatted CT images also show the extent of the lesion (blue arrow), which extends posterosuperiorly from the calcified aneurysm (red arrow) toward the inferior margin of the lateral ventricle

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Fig. 2.36 A 68-year-old woman with a medium-sized infarct of the AChA (reproduced from [101]) who suddenly developed dizziness, right hemiparesis, dysarthria, and right hemihypaesthesia. (a) Transaxial CT, (b) coronal, and (c) sagittal contrast-enhanced T1-weighted magnetic resonance (MR) images obtained in subacute stage. Multiplanar CT and MR images disclose an infarct that mainly involves the posterior limb of the left internal capsule and a part of the left globus pallidus (arrows in (a), (b) and (c)) that reaches the retrolenticular portion of the internal capsule. The lesion appears as an enhancing area on contrast-enhanced T1-weighted images. (d) Lateral view of the left carotid angiogram shows the AChA is not opacified (arrowhead). Vertebral angiography revealed no collateral circulation to the AChA (not shown)

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Fig. 2.37 Infarct in the region of the basal perforators of the internal carotid artery (ICAp) developed in a patient with an aneurysm arising from the terminal bifurcation of the right ICA. (a) Preoperative CT shows subarachnoid hemorrhage in the right sylvian fissure. The patient underwent surgery, and a tiny perforator arising from the terminal part of the ICA was sacrificed. Postoperative CT in (b) acute and (c) chronic stages show a tiny infarct in the region of the genu of the internal capsule (arrow)

2.4 Thalamic Arterial Group 2.4.1 Generalized Anatomy of the Vascular Supply of the Thalamus with Microangiographic Findings Since the report of Duret [18], numerous investigators have studied the arteries of the thalamus both anatomically and radiographically [7, 8, 21, 22, 25, 26, 29, 32, 47, 48, 58, 62, 75, 79, 84, 91, 118]. Several groups of arteries arise from the developmental caudal division of the ICA and supply the thalamus, forming an arc of a circle that enclasps the thalamus [48, 78, 79] (Figs. 2.39 and 2.40). These perforating arteries have many names, and Foix and Hillemand [21, 22] believed their names should indicate the sites of penetration as well as the areas supplied. Based on their proposal, the terms adopted in this book are: thalamotuberal (TTA), thalamoperforate (TPA), thalamogeniculate (TGA), and medial (MPChA) and lateral posterior choroidal arteries (LPChA). Because the branches of the LPChA and AChA intermingle and richly anastomose with each other, they may better be regarded as the choroidal vessels of the lateral ventricle [79]. However, for convenience and because the LPChA is usually the major source of the choroid plexus of the lateral ventricle around the thalamus, we use the term LPChA here. Figure 2.41 diagrams the vascularization of the thalamic nuclei based on Plets’s study of the vascularization of each thalamic nucleus using microangiography and transillumination [78, 79] and our own microangiographic findings (Figs. 2.42–2.45) [99]. We adopt the terminology in Carpenter’s textbook for the thalamic nuclei [10]. Figure 2.46 shows the territories of the thalamic arteries along with those of other perforators on transaxial sections of the brain. The course and distribution of individual thalamic arterial groups are well observed in three dimensions on coronal, sagittal, and transaxial microangiograms.

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Fig. 2.38 Infarct probably in the region of the ICAp found postoperatively in a case with sellar region meningioma (reproduced from [95]). Preoperative contrast-enhanced (a) axial and (b) coronal T1-weighted images show an enhanced tumor in the right sellar region. The ICA (arrow) and the PCoA (arrowhead) on the right side are totally encased by the tumor, both of which are indicated by flow void. Postoperative contrast-enhanced (c) axial and (d) coronal T1-weighted images show a small infarct (arrows) in the region of the genu of the internal capsule. Although unproven, the lesion presumably involves the territory of the region of the ICAp

92 Fig. 2.39 Brain specimen showing the thalamic arteries (reproduced from [94]). (a) Paramedian sagittal section of the brain shows the thalamotuberal arteries (TTA) arising from the PCoA and entering the tuber cinereum (TC) anterior to the mamillary body (M) and the thalamoperforate arteries (TPA) and other interpeduncular fossa arteries entering the posterior perforated substance located posterior to the mamillary body. The internal carotid artery (ICA) is retracted. (b) Sagittal section after removal of the brainstem shows the medial posterior choroidal artery (MPChA) and splenial artery (SpA). The lateral posterior choroidal arteries (LPChA) is not seen. BA basilar artery; Po pons; Th thalamus

S. Takahashi

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Roughly, the TTA distribute in the anterior pole; the TPA, medially and centrally along the lateral wall of the third ventricle; and the TGA, laterally and posteriorly. The MPChA distribute in the posteromedial and dorsomedial portions of the thalamus. The area supplied by the LPChA is not clearly seen but seems to be in the most lateral region of the posterior thalamus (pulvinar) and in the dorsolateral portion [29, 47, 75, 78, 79, 91, 118]. Although these vessels are well established, there is still some disagreement regarding such issues as the supply of the centromedian nucleus (CM) [75, 79]. Similarly, the roles of the AChA in the supply of the thalamus and of the TGA in the supply of the posterior limb of the internal capsule have not been settled [75, 91].

2.4.2 Thalamotuberal Artery Extracerebral: The PCoA emits 4–12 branches (average, 7) along its course, mostly from its superior and lateral surfaces [84]. According to some microanatomical studies, the number and diameter of perforating arteries are relatively constant, regardless of the trunk size of the PCoA [73, 84, 118]; therefore, at surgery, care should be taken to preserve any perforators if hypoplastic segments are divided [84, 118]. When the PCoA is small, carotid


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Fig. 2.40 Diagram of the vascularization of the thalamus (Viewed from lateral). Terminology is taken from Carpenter’s textbook [10] (reproduced from [99]). A anterior nucleus; BA basilar artery; CM centromedian nucleus; DM dorsomedial nucleus; ICA internal carotid artery; LD lateral dorsal nucleus; LGB lateral geniculate body; LP lateral posterior nucleus; LPChA lateral posterior choroidal artery; MGB medial geniculate body; MPChA medial posterior choroidal artery; PCA posterior cerebral artery; PCoA posterior communicating artery; Pu pulvinar; TGA thalamogeniculate arteries; TTA thalamotuberal arteries; VA ventral anterior nucleus; VL ventral lateral nucleus; VPL ventral posterolateral nucleus

angiogram may opacify only the proximal portion of the PCoA and its perforator so that the ICA appears to have a perforating artery rather than a PCoA (Fig. 2.2c). The largest of the perforators of the PCoA enters the brain at the tuber cinereum between the mamillary bodies and the optic tract and distributes within the hypothalamus [33] and thalamus (Fig. 2.47). The vessel is thus called the thalamotuberal (TTA) and, sometimes, the premamillary artery, anterior thalamoperforating artery, or thalamic polar artery [28, 74]. The TTA is commonly single (71.8%) and sometimes double (28.2%) [28] and arises most frequently on the middle [74, 84] or posterior third of the PCoA [28, 91] or, rarely, from the P1 of the PCA. The diameter varies from 280 and 780 mm (average, 493 mm) [28]. The TTA gives off side branches to the hypothalamus, optic tract, mamillary body, and cerebral peduncle, and its extracerebral segment may anastomose with adjacent vessels (Fig. 2.47) [28, 74]. Intracerebral: The TTA supplies important regions of the diencephalon. From a developmental standpoint, it seems reasonable that the perforating branches of the PCoA (i.e., the TTA) should supply part of the diencephalon because the PCoA embryologically represents the most proximal segment of the caudal division of the ICA [42, 71] (see Fig. 1.27 in Chap. 1). The area supplied by the TTA includes the posterior hypothalamus [33], column of fornix, mamillothalamic tract, anterior thalamus, anterior segment of the posterior limb of the internal capsule, and subthalamus [79, 84]. Though the role of the TTA in the supply of the internal capsule has not been emphasized in the literature, both Kolisko [44] and Beevor [7, 8] have shown that the TTA supply a third of the posterior limb below the level of the superior angle of the external segment of the globus pallidus. Furthermore, the TTA may irrigate the medial part of the subthalamus (the substantia nigra, Forel’s field,

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Fig. 2.41 Vascularization of the thalamic nuclei on coronal sections through the (a) anterior nuclei and (b) ventral posterior nuclei (reproduced from [96]). 3V third ventricle; A anterior nucleus; Am amygdaloid body; BA basilar artery; CM centromedian nucleus; DM dorsomedial nucleus; CC corpus callosum; Cd caudate nucleus; CVI cisterna veli interpositi; Fx fornix; Hb habenula; ICA internal carotid artery; LGB lateral geniculate body; LP lateral posterior nucleus; LPChA lateral posterior choroidal artery; LV lateral ventricle; MCA middle cerebral artery; MGB medial geniculate body; MPChA medial posterior choroidal artery; PCA posterior cerebral artery; PCoA posterior communicating artery; Pt putamen; RN red nucleus; Sth subthalamus; TGA thalamogeniculate arteries; TTA thalamotuberal arteries; VL ventral lateral nucleus; VPM ventral posteromedial nucleus

and zona incerta), the optic tract, and ventromedial part of the rostral cerebral peduncle [28]. Within the thalamus, the TTA supply the ventral anterior and ventral lateral thalamic nuclei and anterior portion of the medial nuclei [79]. They may also supply the anterior nucleus and rostral part of the midline and reticular nucleus [28, 91]. Imaging and symptomatology: Infarction in the area supplied by the TTA involves the posterior hypothalamus, anterior pole of the thalamus, and, possibly, the adjacent part of the most anterior portion of the posterior limb of the internal capsule (Figs. 2.48 and 2.49). Ischemia in this region may impair the intellect and memory and cause emotional disturbance, disorientation, thalamic aphasia, and contralateral hemiparesis. Impairment of the intellect and memory and emotional disturbances may be related to involvement of the mamillary body, the mamillothalamic tract, and/or the anterior thalamic nuclei, all of

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Fig. 2.42 Consecutive sagittal microangiograms (reproduced from [99]). (a) Sagittal microangiogram 0.5 cm lateral to the midline (section thickness, 1 cm). The thalamotuberal artery (TTA) ascend in the hypothalamus anterior to the mamillary body (M), but the distal segments are not seen as they deviate laterally toward the anterior portion of the thalamus and the posterior limb of the internal capsule. The prominent vessels that traverse the posterior perforated substance just posterior to the mamillary body (M) and distribute within the anterior portion of the thalamus are the thalamoperforate arteries (TPA). Numerous fine mesencephalic arteries traverse the inferior portion of the posterior perforated substance and distribute within the paramedian zone of the midbrain. (b) Sagittal section 1.5 cm lateral to the midline. Numerous minute vessels distribute to the posterior end of the thalamus, i.e., the pulvinar. These may be called pulvinaric arteries (PuA), which are given off mainly from the MPChA medially and from the LPChA and thalamogeniculate arteries (TGA) more laterally. (c) Sagittal section 2.5 cm lateral to the midline. After arising from the ambient segment of the PCA, the TGA course first superiorly and then anteriorly to supply a large part of the lateral region of the thalamus. LSA lenticulostriate arteries

which constitute part of the neuronal circuit of Papez [72, 99]. Hemiparesis may reflect involvement of the posterior limb of the internal capsule or cerebral peduncle, and ipsilateral Horner syndrome [99] may result from involvement of the posterior hypothalamus and/or anterior thalamic nuclei.

2.4.3 Thalamoperforate Artery (TPA) Extracerebral: The thalamoperforate arteries (TPA), which originate mainly from the P1 segment of the PCA and are part of the interpeduncular fossa arteries, penetrate the

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Fig. 2.43 Consecutive coronal microangiograms (reproduced from [99]). (a) Coronal microangiogram through the hypothalamus (section thickness, 10 mm). After arising from the PCoA (not shown), the proximal course of the TTA is more lateral than that of the TPA. The TTA usually penetrate the premamillary area between the mamillary body and the optic tract (the paramedian perforated substance (PMPS) in Fig. 2.47). They then ascend in the hypothalamus, nearly parallel to the lateral wall of the third ventricle (3V), before diverging superiorly and laterally into the anterior thalamus to reach the internal capsule. By comparison, the lenticulostriate arteries (LSA) distribute farther laterally in the basal ganglia. (b) Coronal section through the proximal (crural) segment of the PCA. The thalamus is well demarcated from the internal capsule as a result of the denser capillary filling within the gray matter. After arising from the interpeduncular segment of the PCA and penetrating the posterior perforated substance, the TPA traverse the midbrain to lie close to the floor and the inferior portion of the lateral wall of the third ventricle posteriorly, then diverge superiorly and laterally into the thalamus, forming a radial pattern. Proximally, the TPA essentially lie in the midline, in contrast to the TTA, which are superimposed on the TPA slightly farther laterally (right side of image). Dorsally, other vessels can be seen arising from the choroidal arteries. The LSA penetrate the putamen, superior portion of the posterior limb of the internal capsule, and body of the caudate nucleus. (c) Coronal section through the ambient segment of the PCA. Branches of the TPA course posteriorly in the paramedian region (arrowhead). The TGA are given off from the ambient segment of the PCA, enter the brain in and between the medial and lateral geniculate bodies, and ascend with a slight lateral convexity. The TGA make a large capillary blush in the lateral portion of the thalamus, and the choroidal vessels make a narrow blush on its dorsal aspect; the MPChA supply the medial portion of the blush and the LPChA supply the lateral portion

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Fig. 2.44 Consecutive coronal microangiograms from another brain. (a, b, c) Consecutive coronal microangiograms through the posterior thalamus in order from anterior to posterior (section thicknesses: (a) and (b) 5 mm; (c) 10 mm, and section (b) is included within section (c)). In addition to the TGA given off from the ambient segment of the PCA, the MPChA and LPChA are well recognized. Passing along the pineal body, the MPChA proceeds anteriorly through the cisterna veli interpositi and give branches to the dorsomedial aspect of the thalamus. The LPChA arises from the PCA and reaches the choroid plexus of the lateral ventricle. It gives off a narrow blush on the dorsal aspect of the thalamus more laterally than the MPChA

r ostral part of the posterior perforated substance (see Fig. 3.22 in Chap. 3) and distribute within the thalamus. They may also be called the posterior thalamoperforating arteries, retromamillary arteries, and interpeduncular perforating arteries. They vary in number from 1 to 10 (average, 2), and diameters of their extracerebral segments measure 100– 750 mm (average, 321 mm) [55]. They mostly arise from the superior and posterior surfaces of the P1, with the most proximal P1 branch originating 2–3 mm distal to the basilar bifurcation [84]. The TPA arise directly from the P1 as a single vessel or as a common stem that ramifies into several branches before entering the brain [55] or may give off side branches to the cerebral peduncle, oculomotor nerve, and mamillary bodies [55]. In their extracerebral course, the TPA frequently have a few small anastomoses among themselves or with adjacent branches of the PCA and basilar and superior cerebellar arteries [58]. Intracerebral: Intraparenchymally, the TPA proximally extend superiorly and posteriorly through the pretectal or subthalamic regions, turn dorsolaterally, and diverge distally in the medioventral portions of the thalamus [55]. As a whole, they distribute in the median and paramedian zones of the midbrain and the medial portion of the thalamus

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adjacent to the lateral wall of the third ventricle. Thus, the TPA supply portions of the cerebral peduncle, substantia nigra, red nucleus, reticular formation, periaqueductal and paraventricular gray matter, trochlear and oculomotor nuclei, oculomotor nerve, pretectal and subthalamic regions, and posterior hypothalamus [34, 55, 84, 118]. Plets emphasized the characteristic angioarchitecture within the thalamus, in which larger branches of the TPA as well as TTA run predominantly in the white matter of the internal medullary lamina and secondarily ramify to the gray nuclear structures [79] to supply the ventral lateral, ventral posterior, and medial nuclei of the thalamus. In a case with a small number of TPA on one side, those on the opposite side take part in supplying blood to the other half of the brainstem and thalamus [55], a variation first described by Percheron (See Fig. 3.23 in Chap. 3) [75].

a

b TTA TTA

TPA

TPA TGA MPChA LPChA

Fig. 2.45 Transaxial microangiograms (reproduced from [99]). (a–c) Consecutive 10-mm microangiograms from the same brain. (d) Ten-millimeter microangiogram from another brain. (a) A section traversing the midbrain show the course and distribution of the fine median and paramedian mesencephalic arteries in the central zone (blue arrowhead). The dense dots in the interpeduncular fossa are most likely the TPA, and those in the posterior hypothalamus (slightly lateral and anterior to the TPA) are the TTA. (b) Section traversing the center of the thalamus. The TPA are distributed in the medial portion of the thalamus, adjacent to the lateral wall of the third ventricle. Just anterior and slightly lateral to the TPA, the TTA supply the anterior pole of the thalamus and the most anterior portion of the posterior limb of the internal capsule. The branches of the TGA are distributed posterolaterally within the thalamus and projected as dense dots in this section by their vertical course; their linear arrangement conforms to the course of the ambient segment of the PCA from which they originate. The MPChA distribute within the posteromedial portion of the thalamus, and the LPChA appear to supply the posterior edge of the thalamus, which is not definitely seen in this specimen. (c) Section traversing the dorsal portion of the thalamus. Proceeding anteriorly in the cisterna velli interpositi, the MPChA gives off lateral branches to supply the dorsomedial portion of the thalamus. Laterally, the LPChA also help supply the dorsal aspect of the thalamus. (d) Section traversing the velum interpositum. The MPChA gives off lateral branches that supply the dorsomedial portion of the thalamus, and laterally, the LPChA may help supply the dorsal aspect of the thalamus just medial to the most dorsal supply of the TGA

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Imaging and symptomatology: Bilateral lesions are frequently observed in the thalami and/ or paramedian zone of the midbrain in cases with impairment of the TPA (Figs. 2.50 and 2.51) [31, 60, 99]. Variations in the mode of origin of the TPA from the PCA may explain this; i.e., in case of a small number of perforators on one side, the opposite side of P1 segment may give rise to a common stem of the TPA (the artery of Percheron), which gives off branches to supply both paramedian territories of the thalami. Occlusion of such an artery can cause paramedian infarcts in both thalami [75]. Alternatively, a single embolus lodged in the tip of the basilar artery (BA) may span short P1 segments of both PCA and cause bilateral obstruction of the origin of the TPA. Because most of the basilar emboli tend to cause multiple lesions following fragmentation and dislocation, the resulting symptoms do not fit the classical pattern; ischemia in this supply area may cause hemiparesis, oculomotor nerve palsy, cerebellar ataxia, rubral tremor, hemiballismus, disorders of attention or disorientation, and memory disturbances. Concomitant involvement of the midbrain may also modify symptoms, manifesting as various oculomotor disturbances, crossed hemiparesis, and cerebellar signs. Memory disturbances and disorientation are frequently noted in such cases, possibly from involvement of the most posterior part of the hypothalamus, including the mamillary body and the anterior and medial nuclei (thalamic dementia) [63, 89, 90, 116]. Akinetic mutism may be observed and probably attributed to involvement of the reticular formation of the midbrain and/or its rostral extension, i.e., the intralaminar nuclei (including the centromedian nucleus) [10, 87].

2.4.4 Thalamogeniculate Artery (TGA) Extracerebral: The thalamogeniculate arteries (TGA) arise from the PCA and enter the brain in and between the geniculate bodies, pulvinar of the thalamus, or brachium of the superior colliculus and distribute within the thalamus [62]. The TGA most often originate

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separately as individual vessels but may share a common stem of origin. They arise most often from the ambient (P2) segment of the PCA trunk, but less often from the quadrigeminal (P3) segment and the temporal, calcarine, or parieto-occipital arteries [62]. They vary from 2 to 12 in number (mean, 5.7) and from 70 to 580 mm in caliber (mean, 345.8 mm) [62]. Side branches of the TGA reach the medial and lateral geniculate bodies, pulvinar, superior collicular brachium, and cerebral peduncle. Extracerebral anastomoses may be present with adjacent vessels, including the MPChA or collicular arteries. Intracerebral: The TGA supply the lateral posterior portion of the thalamus, the medial geniculate body, certain portions of the subthalamus, and, possibly, portions of the internal capsule and lateral geniculate body [9, 31, 34, 62, 118]. More specifically, within the thalamus, the TGA irrigate the rostrolateral portion of the pulvinar, the ventral posterolateral and ventral posteromedial nuclei, the lateral part of the centromedian, and the ventrocaudal part of the ventral lateral nucleus of the thalamus [9, 31, 62, 79]. They occasionally supply portions of the dorsal medial, lateral posterior, parafascicular, and reticular nuclei [62]. The TGA supply the pulvinar in its rostral part, whereas numerous fine arteries mainly from the LPChA laterally and the MPChA medially, termed lateral and medial pulvinaric arteries herein, supply the posterior margin of the pulvinar (Fig. 2.42b). Imaging and symptomatology: Infarcts in the TGA region on imaging are located in the posterolateral part of the thalamus and may partially encroach upon the medial aspect of the posterior limb of the internal capsule (Figs. 2.52 and 2.53). The lesions spare the posterior margin of the pulvinar, which may be supplied by the pulvinaric arteries from the LPChA laterally. Patients typically present with Dejerine-Roussy syndrome (hemiparesis, hemihypesthesia, hemiataxia, hemichorea, and hemiathetosis contralateral to the thalamic infarct); pain and dysesthesia may develop later on the hemianesthetic side [9, 19]. Contralateral hemiparesis is present and usually mild and transient; its resolution may produce cerebellar signs on the

Fig. 2.46 Distribution of the basal perforating arteries on transaxial sections of the brain. Sections passing through the (a) midbrain, (b) mid-thalamus, and (c) dorsal portion of the thalamus and the (d) body of the lateral ventricle. The anatomical drawing is based on Pullicino’s diagrams [80]. A anterior nucleus; AC anterior commissure; AL ansa lenticularis; APd ansa peduncularis; CdB caudate nucleus, body; CdH caudate nucleus, head; CdT caudate nucleus, tail; Cla claustrum; CM centromedian nucleus; CP cerebral peduncle; CR corona radiata; CTT central tegmental tract; Dar nucleus of Darkschewitsch and interstitial nucleus of Cajal; DM dorsomedial nucleus; FxCo fornix, column; GPl globus pallidus, lateral segment; GPm globus pallidus, medial segment; Hb habenula; Hth hypothalamus; IC internal capsule; ICa internal capsule, anterior limb; ICg internal capsule, genu ICp internal capsule, posterior limb; IThP inferior thalamic peduncle; LGB lateral geniculate body; LP lateral posterior nucleus; MGB medial geniculate body; ML medial lemniscus; MLF medial longitudinal fasciculus; MTT mammillothalamic tract; NAc nucleus accumbens; PAq periaqueductal gray matter; POp preoptic area; Pt putamen; Pu pulvinar; RN red nucleus; SCo superior colliculus; SN substantia nigra; SP septum pellucidum; Sth subthalamic nucleus; ThF thalamic fasciculus; VA ventral anterior nucleus; VL ventral lateral nucleus; VPL ventral posterolateral nucleus

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a Pt

NAc

IThP POp

Pt

GPl

FxCo

APd GPm

Hth Sth MTT

CP

CdT

SN

LGB

RN MLF

MGB ML GT

Dar

PAg

SCo

b

CdH ICa Pt

FxCo AC

GPl

AL

GPm

Fsc ThF

MTT VL

ICp

DM VPL

CdT

CM

Hb

P

contralateral side, perhaps from involvement of the red nucleus or ventral lateral nucleus (VL) of the thalamus, both of which receive fibers of the dentato-rubrothalamic tract [10, 99]. Hemihypesthesia is observed with or without thalamic pain, which indicates involvement of the ventral posterior nucleus. Many patients with infarction of the TGA may present with minimal or no disturbance of facial sensation because the medial portion of the ventral posterior nucleus is primarily supplied by the TPA [29]. When infarction is small, pure sensory or sensory motor stroke can result [9]. A unilateral lesion of the medial geniculate body usually causes no clinical manifestation, and visual field deficits from involvement of the lateral geniculate body are rare.

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c MSA (medial striate arteries) from A1 segment of ACA MSA from RAH (recurrent artery of Heubner)

Cla

ICa

Perforators from ACoA (anterior communicating artery)

CdH

LSA (lenticulostriate arteries) Pt

ICg

AChA (anterior choroidal artery) A

VL

ICAp (perforators of the ICA) DM

ICp

LP

TTA (thalamotuberal arteries) P TPA (thalamoperforate arteries)

CdT

TGA (thalamogeniculate arteries) MPChA (medial posterior choroidal artery) LPChA (lateral posterior choroidal artery)

d

White zone in the midbrain tectal region mainly represents the area of collicular arteries (See Figs. 3.24 and 3.25)

Cla

CdB IC / CR


2.4.5 Medial Posterior Choroidal Artery The MPChA arise from the PCA or its branches and enter the roof of the third ventricle. Fujii et al. report 1–3 (average 1.7) MPChA per hemisphere, with the single vessels occurring in half of hemispheres [24]. The vessels arise predominantly from the P2A and

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OCh

ICA

PCoA

APS

AChA b

PS OT TbIA

OpA

TC

a

d TTA

c

M

PdA CP MmA

(Right)

PPS

PMPS f

e PCA

(Left)

Fig. 2.47 Drawing showing the side branches (right, black) and anastomoses of the TTA (left, striped) (reproduced from [28]). The TTA enters a small triangular space surrounded by the mamillary body (M), the cerebral peduncle, and the optic tract, which is called the paramedian perforated substance (PMPS) by Pedroza’s group [74]. Note the side branches to the tuber cinereum, or tuberoinfundibular artery (TbIA), optic artery (OpA), mamillary artery (MmA), and artery to the cerebral peduncle, or peduncular artery (PdA). Also note the anastomoses (black shown on the left) that connect the TTA to the (a) tuberoinfundibular artery (TbIA), (b) perforating branch of the AChA, (c) main trunk of the PCoA, (d) mamillary branches of the PCoA and PCA, (e) main trunk of the PCA, and (f) peduncular branch of the PCA. APS anterior perforated substance; ICA internal carotid artery; OCh optic chiasm; OT optic tract; PdA peduncular artery; PPS posterior perforated PS pituitary stalk; TbIA tuberoinfundibular artery; TC tuber cinereum

P1 of the PCA trunk and less often from the P3, P2P, and branches of the PCA (for PCA segments, see Fig. 1.14 in Chap. 1) [24, 84, 91, 118]. They encircle the midbrain medial to the PCA trunk, turn forward at the side of the pineal gland to enter the roof of the third ventricle, and course in the velum interpositum adjacent to the internal cerebral vein and the opposite MPChA (Fig. 2.54). The cisternal segment measures 0.2–1.4 mm in diameter (average, 0.8 mm) and sends branches to the cerebral peduncle, geniculate bodies, tegmentum, superior colliculi, pulvinar, pineal body, posterior commissure, cerebral cortex of the occipital lobe, and medial thalamus [24]. Especially, it seems that numerous pulvinaric arteries distribute to the medial posterior portion of the pulvinar [29]. The plexal segment that courses within the cisterna veli interpositi splits into medial and lateral branches at the level of the lateral edge of the pineal body [78, 79] (Fig. 2.55). The medial branch continues in the choroid plexus of the third ventricle, supplies the tela

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b

d

Fig. 2.48 TTA infarct (reproduced from [99]). This 52-year-old woman had a ruptured aneurysm at the origin of the PCoA from the right ICA. She exhibited no neurological deficit prior to surgery. (a) The preoperative angiogram shows the aneurysm is obscured by the superimposed distal internal carotid, although the PCoA (arrowhead) and the PCA are well opacified. (b) After the aneurysm was clipped, left hemiparesis with brachial predominance developed together with Horner syndrome on the right. On the angiogram, the PCoA is occluded and the PCA is not opacified. The vertebral angiogram (not shown) demonstrated good opacification of the PCA without retrograde filling of the PCoA on the right. (c-f) Postoperative CT scans show a hypodense area (arrows) in the region of the posterior hypothalamus along the lateral wall of the inferior portion of the third ventricle, the anterior pole of the thalamus, and the most anterior portion of the posterior limb of the internal capsule on the right. Based on the angiographic findings, the lesion was felt to be caused by low perfusion in the territory of the TTA, which arise from the PCoA on the right

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e

f


a

b

axial

coronal

c

sagittal

d

Left CAG, lateral

Fig. 2.49 Infarct in area of distribution of the TTA (reproduced from [104]). This 81-year-old man had right hemiparesis that affected the right side of his face but was more predominant in the upper than lower extremities. A right hemihypesthesia also was present. (a) Axial T2-weighted and (b) coronal and (c) sagittal T1-weighted MR images show an infarct in a region of the left side of the hypothalamus and in the anterior part of the thalamus, possibly extending to the anterior part of the posterior limb of the internal capsule (arrows). (d) Lateral view of a left carotid angiogram shows abrupt occlusion of the left PCoA (arrowhead). Vertebral angiography did not fill both PCoA. These angiographic findings suggest ischemia in the area supplied by the TTA

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choroidea and the stria medullaris, and occasionally sends branches through the foramen of Monro or between the fornix and thalamus to supply the choroid plexus of the ipsilateral and contralateral lateral ventricles [24]. The lateral branch, also called the habenular branch, penetrates the habenula, where it ramifies into three terminal branches that irrigate

a

b

c

d

Fig. 2.50 TPA infarct (reproduced from [104]). This 63-year-old man was admitted in a state of somnolence of 1 week’s duration. Neurological examination revealed disorientation, dysarthria, crossed motor palsy involving the left half of his face and right half of his body, dysdiadochokinesia on the left, and upward gaze palsy; however, sensation was intact. (a–d) CT shows an area of hypodensity (arrows) in the paramedian zone of the junction between the midbrain and diencephalon and the medial portions of the thalami bilaterally (though considerably larger on the right) that is adjacent to the lateral wall of the third ventricle; the hypodense area was interpreted as an infarct involving the distribution of the TPA. (e) Left vertebral angiogram shows a narrow zone in the precommunicating (P1) segment of the right PCA that appears to extend to the tip of the basilar artery (arrowhead) and involve the origin of the TPA

107

2 Intracranial Arterial System: Basal Perforating Arteries Fig. 2.50 (continued)

VAG

e

the paraventricular nuclei, the medial portion of the centromedian nucleus, and the rostromedial part of the pulvinar, which may be regarded as a supply in a ventriculofugal fashion as described in the discussion of the subependymal arteries (SEA) in Sect. 2.3.1.4. (also see Fig. 2.31) [78]. Imaging and symptomatology: Perhaps because of numerous anastomoses with other vessels, infarcts in the territory of the MPChA are rare, but they sometimes involve the pulvinar medially and the dorsomedial aspect of the thalamus (Fig. 2.56). Symptomatology of discrete involvement of the region remains unclear but may be dominated by eye movement disorder from coexisting involvement of the upper midbrain [65].

2.4.6 Lateral Posterior Choroidal Artery The lateral posterior choroidal arteries arise from the PCA or its branches and pass laterally through the choroidal fissure and around the thalamus to enter the choroid plexus of the lateral ventricle. According to the microanatomic study of Fujii et al., typically two or three LPChA are present per hemisphere, and the anterior vessel is largest [24]. The majority arise directly from the PCA trunk (46% from the P2P, 20% from the P2A, and 11% from the P3) (see the PCA segments in Fig. 1.15 in Chap. 1) and the remainder, from branches of the PCA, such as the parieto-occipital and temporal arteries, and even from the MPChA. The anterior LPChA that arises from the P2A passes laterally through the

108 Fig. 2.51 Infarct in the area of the TPA distribution (reproduced from [104]). This 57-year-old woman suddenly became disoriented about location and time. She wanted to eat many times a day and go to her office at midnight, forgot her age, and made errors in performing easy calculations. Her motor and sensory functions were preserved. (a) Axial, (b) coronal, and (c) sagittal contrast-enhanced T1weighted MR images obtained 15 days after onset of ictus show enhanced lesions in the medial part of both thalami (arrows). Note that lesion distribution corresponds well with TPA distribution, particularly on the coronal image (b), extending superolaterally in the thalami

S. Takahashi

a

b

c

c horoidal fissure to supply the choroid plexus of the temporal horn and atrium, and the posterior LPChA reaches the choroid plexus in the posterior part of the temporal horn, atrium, and body of the lateral ventricle. Like the AChA, the LPChA divide into cisternal and plexal segments at the choroidal fissure. The cisternal segment measures 0.2–1.5 mm in diameter (average, 0.6 mm) and sends branches to the thalamus, geniculate bodies, fornix, cerebral peduncle, pineal body, splenium of the corpus callosum, hippocampus, temporal and occipital cortex, and tegmentum and occasionally gives rise to small separate branches that pass through the choroid fissure to supply the choroid plexus [24]. The plexal segment of the LPChA enters the ventricle

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a

b

Fig. 2.52 Thalamogeniculate artery (TGA) infarct (reproduced from [104]). This 67-year-old woman had headaches, vomiting, and dizziness of sudden onset. Neurological examination revealed truncal ataxia with a tendency to fall to the left as well as left-sided hemihypesthesia (including the face) but showed no muscle weakness or visual field defect. (a) CT shows infarction involving the lateral portion of the thalamus on the right (arrow), considered to represent the area supplied by the TGA. The posterior margin of the thalamus (pulvinar) is spared. (b) Vertebral angiogram taken with bilateral retrograde brachial injections shows marked thinning of the posterior ambient segment of the right PCA (arrow), but no obstruction of the cerebellar arteries. Since then, the patient has often had hallucinations that have gradually diminished. Although the truncal ataxia and sensory disturbance persisted, she was ambulatory at discharge about 3 weeks after symptom onset

posterior to the AChA and runs along the medial border of the choroid plexus in the temporal horn, atrium, and body of the lateral ventricle. This segment may leave the choroidal fissure and take a serpentine course in the wing of the ambient cistern (Fig. 2.54). The vessels may send branches through the foramen of Monro or between the fornix and thalamus to the choroid plexus in the third ventricle and, rarely, even through the foramen of Monro to the choroid plexus in the body of the contralateral lateral ventricle [24]. The plexal segment also sends branches to the thalamus and fornix. Within the thalamus, the LPChA supply a large lateral part of the pulvinar (pulvinaric arteries), the dorsal portion of the medial nuclei, and the lateral nuclear group (lateral dorsal and lateral posterior nuclei). There is some disagreement in the arterial blood supply of the anterior nucleus, Plets stating that its main supply is the LPChA [79] and Percheron, the MPChA [76]. Imaging and symptomatology: Infarcts of the LPChA area may involve the lateral part of the pulvinar and the dorsolateral portion of the thalamus (Fig. 2.57). A part of the lateral geniculate body and the hippocampal formation may also be involved. Generally, infarction involving the choroidal arteries is rare, perhaps because of the numerous anastomoses with other vessels in the cisternal and plexal regions. When present, infarction in the LPChA area

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b

c

d

VAG, AP

Fig. 2.53 Thalamogeniculate artery (TGA) infarct in a 65-year-old woman who suddenly developed paresthesia on the left half of her body with left sensory disturbance, left hemiparesis, and left cerebellar ataxia and was clinically suspected of cerebellar infarct on admission. (a) Axial, (b) coronal, and (c) sagittal images show an infarct involving the posterolateral part of the right thalamus (arrow). The posterior margin of the thalamus (pulvinar) is barely spared on both axial and sagittal images, which may represent the vascular territories of pulvinaric arteries of the LPChA and MPChA. No lesion was found in the cerebellum (not shown). Note that the configuration of the lesion is similar to the distribution of the TGA on coronal and sagittal microangiograms (Figs. 2.42c and 2.43c). (d) Vertebral angiography reveals considerable stenosis in the ambient segment of the PCA (arrow), which usually corresponds to the site of origin of the TGA

is usually observed in association with lesions of the TGA [9, 99]; this may be attributable to the proximity of the origin of the two groups of vessels [118]. Neau’s group mapped the territories of the MPChA and LPChA (Fig. 2.58), and described three associated neurological features with LPChA infarcts−visual field defect, sensorimotor dysfunction, and neuropsychological disturbances [65]. The visual field defect in this disorder is explained by involvement of the lateral geniculate body.

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a ON

SHyA ICA A1

ICA A1

MCA PCoA LSA TTA AChA

PCoA P1 BA III

LVt TPA

PCA LGB ChP CoA MGB

PB Pu

LPChA

CCs

MPChA

Fig. 2.54 Microsurgical anatomy of the choroidal arteries. (a) Inferior view with the inferomedial part of the left temporal lobe removed to show the choroidal arteries supplying the choroid plexus of the temporal horn and atrium (reproduced from [24]). The anterior choroidal artery (AChA) crosses the optic tract from lateral to medial in its initial course and from medial to lateral in its distal course to enter the choroid plexus (ChP) in the temporal horn. The lateral posterior choroidal arteries (LPChA) cross the pulvinar to enter the choroid plexus of the temporal horn and atrium. The medial posterior choroidal artery (MPChA) encircles the brainstem medial to the posterior cerebral artery (PCA) before turning forward along the side of the pineal gland and sends branches to the medial geniculate body (MGB) in its course. A long circumflex branch of the PCA, or collicular artery (CoA) also encircles the brainstem medial to the PCA. (b) Posterior view of the lateral and third ventricles after removal of the corpus callosum and fornix to expose the roof of the third ventricle (reproduced from [24]). The upper layer of the tela choroidea has been removed to expose the MPChA that arise from the PCA, pass lateral to the pineal body (PB), and enter the choroid plexus of the third ventricle. They also send branches to the thalamus and the choroid plexus of the lateral ventricle. A1 horizontal (A1) segment of the anterior cerebral artery; AChA anterior choroidal artery; BA basilar artery; ChP choroid plexus; FxCo column of fornix; ICA internal carotid artery; CoA collicular artery; LSA lenticulostriate artery; LGB lateral geniculate body; LPChA lateral posterior choroidal artery; LVt temporal horn of the lateral ventricle; MCA middle cerebral artery; MGB medial geniculate body; ON optic nerve; P1 P1 segment of the posterior cerebral artery; PB pineal body; PCA posterior cerebral artery; PCoA posterior communicating artery; Pu pulvinar; SHyA superior hypophyseal artery; TPA thalamoperforate arteries; TTA thalamotuberal arteries; III oculomotor nerve

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b

FxCo

ChP MPChA Pu

Pu

LPChA

PB

LPChA

PCA

PCA

MPChA-m MPChA-m HbBr

CC

PBBr

ChP(3V) PVBr CMBr PuBr

PVBr

PCBr MPChA CM

PCA ICA

PuBr

Pons BA

CMBr Hb

PBBr

HbBr Pu

MPChA

Fig. 2.55 Distribution of the MPChA (reproduced from [78]). Branches of the MPChA: CMBr branch to the centromedian nucleus; HbBr branch to the habenula (lateral branch of the MPChA); MPChA-m medial branch of the MPChA; PBBr branch to the pineal body; PCBr branch to the posterior commissure; PuBr branch to the pulvinar; PVBr branch to the paraventricular nuclei; CC corpus callosum; BA basilar artery; CM centromedian nucleus; ChP(3V) choroid plexus of the third ventricle; Hb habenula; ICA internal carotid artery; PCA posterior cerebral artery; Pu pulvinar

2.4.7 Vascular Supply of the Choroid Plexus of the Lateral Ventricle The choroid plexuses of the lateral and third ventricles, which continue with each other through the foramen of Monro, are supplied by the anterior, lateral posterior, and medial posterior choroidal arteries, and there is a marked variation in the area of the choroid plexus supplied by the choroidal arteries. In the most common pattern, the AChA supplies a portion of the choroid plexus in the temporal horn and part of the atrium; the LPChA, a portion in the posterior part of the temporal horn, atrium, and body; and the MPChA, in the roof of the third ventricle and a portion of choroid plexus in the body of the lateral ventricle


113

Fig. 2.56 MPChA infarct (reproduced from [104]). (a) Axial, (b) coronal, and (c) sagittal T1weighted MR images of a 59-year-old woman with paresthesia of the right fingers, right hemiparesis, left Horner’s syndrome, and memory disturbance show a lesion in the posterior superomedial aspect of the left thalamus, probably involving the centromedian, dorsal medial, and paraventricular nuclei of the thalamus (arrow). Thalamic dementia was suspected

(Fig. 2.59) [24]. This predominant pattern of choroidal arterial contribution to the choroid plexus may be closely related to the distribution pattern of the subependymal arteries (SEA) from the individual choroidal arteries in the wall of the lateral ventricle as described by Marinkovic et al.: the AChA distributes, in order of frequency, in the walls of the temporal horn, occipital horn, and atrium; the LPChA, in the walls of the body, atrium, occipital horn, and, partially, the frontal horn; and the MPChA, partially in the body and the frontal horn of the lateral ventricle [51]. Supply from different choroidal arteries to individual segments of the choroid plexus frequently overlaps; the choroid plexus in the body of the lateral ventricle may receive branches from each of the three choroidal arteries, but its most frequent supply is from the LPChA and then, the MPChA [24]. The LPChA also occasionally send branches to the choroid plexus on the contralateral side. The sizes of the plexal areas supplied by the AChA and the LPChA are inversely related, as are the areas supplied by the LPChA and MPChA.

2.4.8 Vascular Supply of the Hypothalamus Few studies address the vascularization of the hypothalamus [33, 49], and the following descriptions are based on Marinkovic’s work (Figs. 2.60 and 2.61) [49]. Hypothalamic branches arise from the ACoA and its branch of the subcallosal artery, that is, the median preoptic arteries (MPOpA) that supply the preoptic region and the anterior median

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b

c Fig. 2.57 LPChA infarct (reproduced from [104]). (a–c) Axial T1-weighted MR images of a 73-yearold woman with bilateral tinnitus and frequent vertigo reveal an old infarct in the dorsolateral aspect of the left side of the thalamus, which was interpreted as an infarct involving the supply area of the LPChA (arrows)

c ommissural artery (AMCoA) that gives off branches to the middle part of the lamina terminalis. Perforators from the ACoA are described elsewhere (Chap. 4 by T. Fujii). In addition to the optic arteries (OpA) that pass to the optic nerve and the chiasmatic arteries that irrigate the optic chiasm, the hypothalamic branches that arise from the A1 segment of the ACA comprise the suprachiasmatic artery (SChA) to the suprachiasmatic nucleus, the supraoptic artery (SOpA) to the supraoptic nucleus, and the preoptic arteries (POpA) extending to the preoptic region. The anterior hypothalamic nucleus also probably receives branches from the ACA. The ICA and its main branches, which include the ophthalmic artery and superior hypophyseal arteries, provide the optic and chiasmatic arteries, the posterior median commissural artery (PMCoA), and the tuberoinfundibular arteries (TbIA). The tuberoinfundibular arteries send branches to the pituitary stalk and paraventricular nucleus of the hypothalamus. The PCoA branches into the optic arteries, tuberoinfundibular arteries, TTA, mamillary arteries (MmA), peduncular branches (PdA), and, rarely, the TPA. The tuberoinfundibular arteries (TbIA) of the PCoA may give off side branches to the pituitary stalk, optic tract, and mamillary bodies and enter the hypothalamus to irrigate the arcuate nucleus and the ventromedial and dorsomedial nuclei. The TTA may give off the optic, peduncular, and/or mamillary arteries and enter the brain to supply the posterior hypothalamus, including the lateral aspect of the fornical column and lateral hypothalamic region. The PCA or its branches of the TPA may give rise to the mamillary arteries. The lateral hypothalamic area is perfused

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a

b

d

e

MPChA territory Possible MPChA territory LPChA territory Possible LPChA territory

c

Fig. 2.58 Territories of the LPChA and MPChA (reproduced from Neau and Bogousslavsky [65]). (a) midbrain-thalamus junction, (b) lower thalamus, (c) mid-thalamus, (d) upper thalamus, and (e) body of the lateral ventricle

FM

AChA

Fig. 2.59 The most common supply pattern of the choroid plexus in the third and lateral ventricles by the anterior choroidal artery (AChA), LPChA, and MPChA (bird’s-eye view) (based on the study of Fujii et al. [24]). ChP(LV) choroid plexus of the lateral ventricle; ChP(3V) choroid plexus of the third ventricle; FM foramen of Monro

ChP(3V) ChP(LV) MPChA LPChA

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A2 OlT ACoA

OFrA

OlA AMCoA RAH

A1 PMCoA

APS

POpA SChA OpA

OCh

MCA

SOpA

ON SHyA

ICA

PS

PCoA

TbIA

OpA

TC

OT

MmA M

TTA

TPA CP

PdA

PCA BA

Fig. 2.60 Arterial blood supply of the hypothalamus from the constituents of the circle of Willis, basal view (composite diagram based on the schemes in [49]). A1 horizontal (A1) segment of the ACA; A2 A2 segment of the ACA; ACoA anterior communicating artery; AMCoA anterior median commissural artery; APS anterior perforated substance; BA basilar artery; CP cerebral peduncle; ICA internal carotid artery; LT lamina terminalis; M mamillary body; MCA middle cerebral artery; MmA mamillary artery; OCh optic chiasm; OFrA orbitofrontal artery; OlA olfactory artery; OlT olfactory tract; ON optic nerve; OpA optic artery; OT optic tract; PCA posterior cerebral artery; PCoA posterior communicating artery; PdA peduncular artery; PMCoA posterior median commissural artery; POpA preoptic artery; PS pituitary stalk; RAH recurrent artery of Heubner; SChA suprachiasmatic artery; SHyA superior hypophyseal artery; SOpA supraoptic artery; TC tuber cinereum; TbIA tuberoinfundibular artery; TPA thalamoperforate artery; TTA thalamotuberal artery

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CCr

Fx

CiG

MI SA

AC PO PV

DM-Hy L-Hy PN

MPOpA

AN

SbA A2

MN

ACoA

TPA

SOp POpA/SOpA

OCh CP

PMCoA SHyA

TTA TbIA PCoA

PCA BA

ICA

Fig. 2.61 Arterial blood supply of the hypothalamus and adjacent structures. Midsagittal section of the brain (reproduced from [49]). A2 A2 segment of anterior cerebral artery; AC anterior commissure; ACoA anterior communicating artery; AN anterior nucleus of the hypothalamus; Arc arcuate nucleus of the hypothalamus; BA basilar artery; CCr corpus callosum, rostrum; CiG cingulate gyrus; CP cerebral peduncle; DM-Hy dorsomedial nucleus of the hypothalamus; Fx fornix; ICA internal carotid artery; L-Hy lateral hypothalamic area; MI massa intermedia; MN mamillary nuclei; MPOpA median preoptic artery; OCh optic chiasm; PCA posterior cerebral artery; PCoA posterior communicating artery; PN posterior nucleus of hypothalamus; PMCoA posterior median commissural artery; PO preoptic nucleui, medial and lateral; POpA/SOpA preoptic artery/supraoptic artery; PTG paraterminal gyrus; PV paraventricular nucleus of the hypothalamus; SA subcallosal area; SbA subcallosal artery; SCh suprachiasmatic nucleus; SOp supraoptic nucleus; SHyA superior hypophyseal artery; TbIA tuberoinfundibular artery; TPA thalamoperforate artery; TTA thalamotuberal artery; VM-Hy ventromedial nucleus of hypothalamus

by the tuberoinfundibular arteries of the PCoA and, partially, by the TTA. The posterior hypothalamic nucleus may be irrigated by the TTA, mamillary arteries, tuberoinfundibular arteries of the PCoA, and the TPA. The subthalamic nucleus receives its blood supply from three sources − the PCA mainly via its TPA, the PCoA via its TTA, and the AChA [33]. Abundant anastomoses noted among the extraparenchymal segments of the hypothalamic arteries may help protect the hypothalamus against certain cerebrovascular diseases.

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2.5 Anastomoses Among the Perforating Arteries of the Brain Although the perforating arteries have generally been regarded as end arteries, anastomoses with diameters of 60–400 mm may be found in the extracerebral segments of the basal perforators within the subarachnoid space. They are particularly frequent among the TPA of the PCA (occurring in 80% of all brains) [58], where their diameters are 80–400 mm (mean 146 mm), and among the premamillary arteries (30% of all brains), where their diameters range from 60 to 280 mm [56]. Extracerebral anastomoses may also occur between the RAH and the most medial LSA [30, 43], which may indicate the phylogenetic origin of the RAH and support the hypothesis that the accessory MCA represents a persistent anastomosis between the anterior and middle cerebral arteries over the tuberculum olfactorium [100]. On the other hand, anastomotic channels that involve perforators of the anterior choroidal, middle cerebral, and anterior cerebral arteries are generally rare [56]. Anastomoses in the extracerebral perforators may have clinical implications in obstructive processes of the vessels, although their numbers and diameters may be too small to provide effective collateral circulation, especially in patients with multiple embolism [58]. Intraparenchymally, although the major penetrating arteries may have web-like anastomoses at the precapillary level, the anastomoses have no functional importance, which implicates the nature of these vessels as end arteries [20]. The relationships between the perforating and leptomeningeal arteries are noteworthy [52] because they frequently share a common origin. In addition to their origin in the main trunk of the MCA, basal perforating arteries often arise from the trunk’s terminal division or from early-branched leptomeningeal arteries (Fig. 2.8). Perforators of such origin with a common stem are generally smaller in diameter than their fellow perforators, which arise directly from the trunks of the main cerebral arteries [52]. The opposite situation is found as well, whereby large perforators give rise to leptomeningeal vessels; for example, the RAH frequently gives rise to small leptomeningeal branches to the anterior perforated substance, caudal parts of the rectal gyrus and caudal orbitofrontal cortex, olfactory structures, and so on. The clinical significance of these anatomical features may lie in the cerebrovascular diseases that result from occlusion of a leptomeningeal branch that produces various combinations of infarcts in both cortical regions and deep gray matter.

2.6 Vascular Supply of the Motor Pathway and MR Imaging 2.6.1 Vascular Supply of the Corona Radiata and the Posterior Limb of the Internal Capsule The vascular supply of the posterior limb of the internal capsule and corona radiata has particular clinical significance because the corticospinal tract passes through these areas, and cerebrovascular events frequently occur here. As described earlier, the perforators of the AChA irrigate the inferior portion of the posterior limb of the internal capsule and a

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2 Intracranial Arterial System: Basal Perforating Arteries Fig. 2.62 Arterial supply of the corticospinal tract in the posterior limb of the internal capsule and the corona radiata. AChA anterior choroidal artery; InA insular arteries; LSA lenticulostriate arteries; MdA medullary arteries of the cerebrum

CST MdA

InA AChA

LSA

portion of the cerebral peduncle, whereas the LSA, which are the perforators of the MCA, supply the superior portion of the posterior limb (Fig. 2.62). The medullary arteries of the insular segment of the MCA, i.e., long insular arteries described by Ture’s team [107, 115], and many medullary arteries from the opercular segment and cortical branches of the MCA take part in vascularizing the corona radiata more superiorly [45]. Such knowledge of the angioarchitecture in these regions is crucial for surgical procedures involving tumors of the basal ganglia and/or insulo-opercular tumors, which are discussed elsewhere (Chaps. 9 and 10 by Kumabe and associates).

2.6.2 MR Imaging of the Basal Perforators Although conventional, or digital subtraction, angiography (DSA) is considered the gold standard for angiography, especially for delineating small arteries, including basal perforators, it is highly invasive and often risky, requiring a substantially complex imaging procedure and administration of an iodine contrast medium. Therefore, noninvasive tools for visualizing perforators have long been sought.

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Recently, the LSA have been successfully delineated using 3D time-of-flight MR angiography (3D TOF MRA) on a 7.0-T ultrahigh-field MR system [12, 38]. In our institution, we perform 3D MR imaging on a 3-T scanner (a Philips Intera Achieva 3.0-T Quasar Dual, Philips Healthcare Best The Netherlands) with a standard 8-channel sensitivityencoding (SENSE) head coil [85] and use a gradient-echo sequence (3D T1 fast field echo [46]) with contrast medium administration (0.2 mL/kg) at the following parameters: repetition time/echo time/flip angle (TR/TE/FA) = 35 ms/2.6 ms/25°; field of vision (FOV) = 200 mm; matrix: 512 × 263; reconstruction matrix: 784 × 784; slice thickness 0.8 mm with a gap of 0.4 mm; 170 total slices; SENSE factor 1.4; and acquisition time: 9 min 23 s. We observe source images and reformatted images in cine paging mode (Figs. 2.63 and 2.64) to visualize small vessels and their relationships with lesions such as tumors (see Chap. 9 by Kumabe and associates). The advantage of this method is that almost noninvasively, it provides information on intraparenchymal pathology and depicts the basal perforators that are often critical in supplying the eloquent areas that include the descending motor pathway. Thus, identifying the LSA in relation with adjacent tumors would help preserve them in case of tumor removal. However, the disadvantage of the method is that it requires gadolinium contrast medium, and accompanying veins are also visualized. Additionally, very fine vessels, such as perforators of the AChA and medullary arteries from pial arteries, have not been visualized using this method. Nevertheless, we believe it is clinically useful if undertaken with recognition of such limitations.

a

b

LSA

c

d

TPA

TGA

Fig. 2.63 Coronal MR imaging delineation of the basal perforators. Coronal images (a), (b), (c), and (d), in order from anterior to posterior, delineate the LSA, TPA, and TGA. These vessels are well identified with cine-mode display. Note that accompanying veins are visualized as well

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a

b

TPA

AChA

c

d LSA

TGA MSA

Fig. 2.64 Sagittal MR imaging delineation of the basal perforators. (a–d) Sagittal images in order from medial to lateral again delineate the AChA, LSA, MSA, TPA, and TGA

Finally, on transaxial sections of the brain, as shown in Fig. 2.46, most of the basal gray region is filled with the supply areas of the MSA, LSA, AChA, and several thalamic arteries as well as branches of the terminal portion of the ICA. On the figures, striate arteries from the ACA and MCA irrigate the anterior part; a series of perforators from the posterior circulation irrigate the posterior part; and the AChA and the perforators from the terminal part of the ICA supply the interposed crescent-shaped portion centered in the posterior limb of the internal capsule. As is often the case with the cortical arteries, the exception appears to be the rule in vascularization of this region. There should be a reciprocal relationship between the size of each area supplied and the degree of development of individual groups of arteries. In conclusion, a general knowledge of the relationship of the vessels and basal gray nuclei as well as the distribution of each perforator group will assist interpretation of imaging findings and aid in conducting detailed neurological evaluation in patients with infarction in the region of the basal gray matter.

Abbreviations 3V A A1 A2 AC ACA

Third ventricle Anterior nucleus Horizontal (A1) segment of the ACA A2 segment of the anterior cerebral artery Anterior commissure Anterior cerebral artery

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AChA ACoA AL Am AMCoA AN APd APS Aq Arc BA CalB Cbll CC CCb CCr Cd CdB CdDv CdH CdT ChBr ChF ChP(3V) ChP(LV) CiG Cla CM CP CR CrDv CSO CT CTT CVI Da DM DM-Hy DSA FM Fx FxCo GP GPl GPm

S. Takahashi

Anterior choroidal artery Anterior communicating artery Ansa lenticularis Amygdaloid body Anterior median commissural artery Anterior nucleus of the hypothalamus Ansa peduncularis Anterior perforated substance Aqueduct of Sylvius Arcuate nucleus of the hypothalamus Basilar artery Callosal branch Cerebellum Corpus callosum Corpus callosum, body Corpus callosum, rostral Caudate nucleus Caudate nucleus, body Caudal division of the internal carotid artery Caudate nucleus, head Caudate nucleus, tail Choroidal branch Choroid fissure Choroid plexus of the third ventricle Choroid plexus of the lateral ventricle Cingulated gyrus Claustrum Centromedian nucleus Cerebral peduncle Corona radiata Cranial division of the internal carotid artery Centrum semiovale Computed tomography Central tegmental tract Cisterna veli interpositi Nucleus of Darkschewitsch and interstitial nucleus of Cajal Dorsomedial nucleus Dorsomedial nucleus of the hypothalamus Digital subtraction angiography Foramen of Monro Fornix Fornix, column Globus pallidus Globus pallidus, lateral segment Globus pallidus, medial segment


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Hb Habenula Hth Hypothalamus IC Internal capsule ICA Internal carotid artery ICa Anterior limb of the internal capsule ICAD Inferior cerebral artery of Dendy ICAp Basal perforators of the ICA ICp Posterior limb of the internal capsule IHF Interhemispheric fissure i-LSA Intermediate lenticulostriate arteries InA Insular artery ITA Inferior temporal artery of the posterior cerebral artery IThP Inferior thalamic peduncle LD Lateral dorsal nucleus LGB Lateral geniculate body L-Hy Lateral hypothalamic area LI Limen insulae l-LSA Lateral lenticulostriate arteries LMAn Leptomeningeal anastomoses LOS Lateral olfactory stria LP Lateral posterior nucleus LPChA Lateral posterior choroidal artery LPBr Lateral plexal branch of the AChA LSA Lenticulostriate arteries LT Lamina terminalis LV Lateral ventricle LVa Lateral ventricle, atrium LVt Temporal horn of the lateral ventricle M Mammillary body M1 M1 segment of the MCA (perforation site of the M1 perforators) MCA Middle cerebral artery MdA Medullary artery of the cerebrum MGB Medial geniculate body MI Massa intermedia ML Medial lemniscus MLF Medial longitudinal fasciculus m-LSA Medial lenticulostriate arteries MmA Mamillary artery MN Mamillary nuclei MOS Medial olfactory stria MPChA Medial posterior choroidal artery – CMBr: Branch to the centromedian nucleus; HbBr: Branch to the habenula (lateral branch of the MPChA); MPChA-m: Medial branch of the MPChA; PBBr: Branch to the pineal body; PCBr: Branch to the posterior commissure; PuBr: Branch to the pulvinar; PVBr: Branch to the paraventricular nuclei

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MPBr MPOpA MR MSA MTT NAc OB OCh OFrA OlT OlTb ON OpA OR OT P1 P2 P3 PAq PB PCA PCalA PCoA PdA PMCoA PN PO POL POp POpA PS Pt PTG Pu PuA PV RAH RG RN SA SbA SCh SChA SCo SEA

S. Takahashi

Medial plexal branch of the AChA Median preoptic artery Magnetic resonance Medial striate arteries Mammillothalamic tract Nucleus accumbens Olfactory bulb Optic chiasm Orbitofrontal artery Olfactory tract Olfactory tubercle Optic nerve Optic artery Optic radiation Optic tract Precommunicating segment of the PCA trunk Ambient segment of the PCA trunk Quadrigeminal segment of the PCA trunk Periaqueductal gray matter Pineal body Posterior cerebral artery Pericallosal artery Posterior communicating artery Peducular artery Posterior median commissural artery Posterior nucleus of the hypothalamus Preoptic nucleui, medial and lateral Posterior orbital lobule Preoptic area Preoptic artery Pituitary stalk Putamen Paraterminal gyrus Pulvinar Pulvinaric arteries Paraventricular nucleus of the hypothalamus Recurrent artery of Heubner (perforation site of the RAH) Rectal gyrus Red nucleus Subcallosal area Subcallosal artery Suprachiasmatic nucleus Suprachiasmatic artery Superior colliculus Subependymal arteries


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SHyA Superior hypophyseal artery SLA Superolateral angle of the lateral ventricle SN Substantia nigra SOp Supraoptic nucleus SOpA Supraoptic artery SP Septum pellucidum SpA Splenial artery Sth Subthalamic nucleus (Luy’s body) TbIA Tuberoinfundibular artery TC Tuber cinereum TGA Thalamogeniculate arteries Th Thalamus ThF Thalamic fasciculus TPA Thalamoperforate arteries TTA Thalamotuberal arteries U Uncus UB Uncal branch of the anterior choroidal artery VA Ventral anterior nucleus VfA Ventriculofugal arteries VL Ventral lateral nucleus VM-Hy Ventromedial nucleus of hypothalamus VPL Ventral posterolateral nucleus VPM Ventral posteromedial nucleus

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114. van der Zwan A, Hillen B, Tulleken CA, Dujovny M, Dragovic L. Variability of the territories of the major cerebral arteries. J Neurosurg. 1992;77:927–40. 115. Varnavas GG, Grand W. The insular cortex: morphological and vascular anatomic characteristics. Neurosurgery. 1999;44:127–36; discussion 136–128. 116. Graff-Radford NR, Damasio H, Yamada T, Eslinger PJ, Damasio AR. Nonhaemorrhagic thalamic infarction. Clinical, neuropsychological and electrophysiological findings in four anatomical groups defined by computerized tomography. Brain 1985; 108:485-516. 117. Webster JE, Gurdjian ES, Lindner DW, Handy WG. Proximal occlusion of the antenor cerebral artery. Arch Neurol Psychiatry. 1960;2:19–26. 118. Zeal AA, Rhoton Jr AL. Microsurgical anatomy of the posterior cerebral artery. J Neurosurg. 1978;48:534–59.

Intracranial Arterial System: Infratentorial Arteries

3

Shoki Takahashi

3.1 Introduction The main trunks of the vertebro-basilar system and major cerebellar arteries are characterized by a high degree of variability, which has been the basis of much clinical confusion, whereas the internal vascular patterns of the brainstem are relatively constant [24]. With such characteristics in mind, we review microangiographic findings to identify the course and distribution of individual vessels. To see the vascular territories of individual vascular groups on the axial section of the brain, we refer to the diagrams of the cerebellar arteries from Amarenco’s group [1] and the diagrams of the internal vascular supply of the brainstem from Tatu and associates [27] that are based on the detailed study of Duvernoy [2].

3.2 Vertebral Artery and Basilar Artery The vertebral artery (VA) is the first branch of the subclavian artery, and it is divided into four segments (Fig. 3.1) [21]: the first segment (V1) extends from its origin at the subclavian artery to the transverse foramen of the C6 vertebra; the second (V2) ascends vertically within the transverse foramina from C6 to C2; the third (V3) extends from its exit from the transverse foramen of C2 to its entrance into the spinal canal and pierces the posterior atlanto-occipital membrane; and the fourth (V4) pierces the dura and extends anteromedially and superiorly through the foramen magnum and reaches the junction with its counterpart to form the basilar artery at the level of the pontomedullary sulcus. The left and right VA almost always differ in size, and the left is believed to be predominantly larger [24]. The smaller VA may terminate in the posterior inferior cerebellar artery, in which case, the distal segment is hypoplastic or nonexistent.

S. Takahashi Department of Diagnostic Radiology, Tohoku University Graduate School of Medicine, Seiryo-machi, Aoba-ku, Sendai, 980-8574, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_3, © Springer-Verlag London Limited 2010

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132 Fig. 3.1 Diagrams illustrating the segments of the vertebral arteries (reproduced from [25]). (a) Lateral view. (b) Superior surface of the atlas and the vertebral arteries AICA anterior inferior cerebellar artery; BA basilar artery; C-1 1st cervical verteba; C-2 2nd cervical vertebra; C-6 6th cervical vertebra; PAOM posterior atlanto-occipital membrane; PCA posterior cerebral artery; PICA posterior inferior cerebellar artery; SAPr superior articular process; SbCA subclavian artery; SCA superior cerebellar artery; SVA sulcus arteriae vertebralis; TrFr transverse foramen; TrPr transverse process; VA vertebral artery; V1 1st segment of vertebral artery; V2 2nd segment of vertebral artery; V3 3rd segment of vertebral artery; V4 4th segment of vertebral artery

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The basilar artery (BA) typically ascends along the basilar (pontine) sulcus in the anteromedian aspect of the pons and often deviates to one side; the curvature of the BA tends toward the opposite side of the larger vertebral artery [24]. On the way of the vertebrobasilar system to the terminal bifurcation of the BA, the V4 segment of the VA gives off direct medullary branches, the anterior spinal artery (ASA), the posterior inferior cerebellar artery (PICA), and, sometimes, the posterior spinal artery (PSA), whereas the BA gives rise to the pontine arteries, the internal auditory artery (variable), the anterior inferior cerebellar artery (AICA), the superior cerebellar artery (SCA), and the posterior cerebral

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arteries (PCA) (Fig. 3.2). Figs. 3.3 (sagittal) and 3.4 (axial) are microangiograms of the infratentorial arteries. Probably owing to its complex developmental alterations, the vertebro-basilar system shows a high degree of variability in the major distribution of arteries on the surface of the brain [24]. In contrast, the internal vascular patterns are relatively constant, especially within the brainstem, despite variable surface arteries.

a

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Fig. 3.2 Diagram showing the main branches of the vertebro-basilar system (reproduced from [16]). (a) anterior view (b) lateral view. ChP-4V choroid plexus of the fourth ventricle; AICA anterior inferior cerebellar artery; AICA-cm caudomedial trunk of anterior inferior cerebellar artery; AICA-rl rostrolateral trunk of anterior inferior cerebellar artery; ASA anterior inferior cerebellar artery; BA basilar artery; ChBr choroidal artery of fourth ventricle (choroidal branch); ChP-4V choroid plexus of fourth ventricle; CMdF cerebello-medullary fissure; CMsF cerebello-mesencephalic fissure; III oculomotor nerve; V trigeminal nerve; VI abducens nerve; VII facial nerve; VIII vestibulocochlear nerve; IX glossopharyngeal nerve; X vagus nerve; XI accessory nerve; XII hypoglossal nerve; CP cerebral peduncle; CPF-SL superior limb of the cerebello-pontine fissure; CPF-IL inferior limb of the cerebello-pontine fissure; Fast fastigium of the fourth ventricle; Fl flocculus; FL lateral aperture of the fourth ventricle, foramina of Luschka; ICo inferior colliculus; IMV inferior medullary velum; Li lingula cerebelli; MCP middle cerebellar peduncle; Md medulla oblongata; PB pineal body; PCA posterior cerebral artery; PCoA posterior communicating artery; PICA posterior inferior cerebellar artery; PICA-pm posterior medullary segment of the PICA; Po pons; PoA pontine artery; PrC precentral cerebellar artery; SCA superior cerebellar artery; SCo superior colliculus; SMV: superior medullary velum; PICA-st supratonsillar segment of the PICA; TCH-4V tela choroidea of the fourth ventricle; To cerebellar tonsil; VA vertebral artery

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Fig. 3.3 Microangiogram of the unilateral posterior fossa arteries, lateral view, 2-cm thickness from the midline (reproduced from [26]). 4V fourth ventricle; AICA anterior inferior cerebellar artery; BA basilar artery; PICA posterior inferior cerebellar artery; SCA superior cerebellar artery; VA vertebral artery

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3 Intracranial Arterial System: Infratentorial Arteries Fig. 3.4 Transaxial microangiograms of the arteries of the posterior fossa, 1-cm thickness in order from inferior to superior (reproduced from [26]). Hemispheric branches of the posterior inferior cerebellar artery (PICA) distribute radially from a center on the brainstem over the inferior surface of the cerebellar hemispheres (a). The PICA and the anterior inferior cerebellar artery (AICA) are seen to arise from the vertebral and basilar arteries (BA), respectively (b and c). Over the superior surface of the cerebellum (d and e), a similar pattern of distribution is seen in branches of the superior cerebellar artery (SCA, arrowheads)

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3.3 Main Branches of the Vertebro-basilar System 3.3.1 Posterior Inferior Cerebellar Artery (PICA) The PICA is the most variable of the three cerebellar arteries (PICA, AICA, SCA). Its size is reciprocal to those of the AICA and the contralateral PICA; if one PICA is hypoplastic or absent, the opposite PICA and/or the ipsilateral AICA is larger and nourishes the area normally supplied by the PICA [3]. In 4–15% of individuals, one PICA is entirely absent [3, 17]. The posterior inferior cerebellar artery usually arises from the vertebral artery a few cm proximal to the vertebro-basilar junction and has a sinuous dorsal-ward course around the medulla, typically with caudal and cranial loops.

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3 Intracranial Arterial System: Infratentorial Arteries SCA-v

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Fig. 3.5 Main branches and segments of the cerebellar arteries. 4V fourth ventricle; AICA anterior inferior cerebellar artery; AICA-cm caudomedial branch of the AICA; AICA-rl rostrolateral branch of the AICA; BA basilar artery; ChBr choroidal branch; PICA posterior inferior cerebellar artery; PICA-am anterior medullary segment of the PICA; PICA-lm lateral medullary segment of the PICA; PICA-pm posterior medullary segment of the PICA; PICA-st supratonsillar segment of the PICA; PICA-th tonsillohemispheric branch of the PICA; PICA-v vermian branch of the PICA; PrC precentral cerebellar artery; SCA superior cerebellar artery; SCA-am ambient segment of the SCA; SCA-ap anterior pontine segment of the SCA; SCA-q quadrigeminal segment of the SCA; SCA-v vermian segment of the SCA; SCA-L superior cerebellar artery, lateral branch; SCA-M superior cerebellar artery, medial branch; VA verteberal artery

According to Huang and Wolf [8], the PICA may be divided into several segments (Fig. 3.5): the anterior medullary segment that extends posteriorly to the level of the inferior olive; the lateral medullary segment that extends posteroinferiorly to the attachment of the glossopharyngeal, vagus, and accessory nerves, and corresponds to the descending limb of the caudal loop; the posterior medullary segment that turns from the bottom of the caudal loop, ascends within the cerebello-medullary fissure [16], and corresponds to the ascending portion of the cranial loop; the supratonsillar segment that forms the cranial loop over the medial side of the superior pole of the tonsil; and the terminal cortical segment over the suboccipital surface of the cerebellum [3, 11, 12]. During its circum-medullary course, the posterior inferior cerebellar artery gives off small medullary branches and, usually, the posterior spinal artery, whereas the posterior medullary and supratonsillar segments send branches to the choroid plexus of the fourth ventricle (the medial segment of the choroid plexus in the roof and the medial part of the lateral recess of the fourth ventricle) [3, 11, 12]. The PICA finally divides into two terminal branches, most commonly at the supratonsillar segment−a lateral branch (tonsillohemispheric branch) and a medial branch (vermian branch). The lateral branch supplies the posterior and inferior (suboccipital) surface of the cerebellar hemispheres (tonsil, biventral and inferior semilunar lobules, and, possibly, a part of the superior

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Fig. 3.6 Diagrams showing the territory of the posterior inferior cerebellar artery (PICA) (reproduced from [1]). (a) Posterior and (b) lateral views of the cerebellum. (c–f) transverse sections through the (c) lower medulla, (d) upper medulla, (e) midpons, and (f) upper pons. The territory of the PICA is indicated as a stippled area on each drawing. The transverse lines in (a) and (b) indicate the transverse sections of (c–f). Note that the PICA never supplies the dentate nucleus. Section (c) shows the most constant territory of the PICA. AQ anterior quadrangular lobule; Bi biventral lobule; Ce central lobule; Cu culmen; De declive; Fl flocculus; Gr gracile lobule; HF horizontal fissure; IS inferior semilunar lobule; MCP middle cerebellar peduncle; Md medulla oblongata; No nodulus; Po pons; PQ posterior quadrangular lobule (lobulus simplex); Pyr pyramid of vermis; SS superior semilunar lobule; To cerebellar tonsil; Tu tuber; Uv uvula

semilunar lobule), and the medial branch supplies a portion of the tonsil and the inferior vermis [24]. As seen in the supratentorial arteries, the cerebellar arteries have rich leptomeningeal anastomoses with each other over the cerebellar surface. Figures 3.6–3.9, reproduced from Amarenco and associates’ report [1] are anatomic drawings showing the territories of the cerebellar arteries.

3.3.2 Posterior Spinal Artery (PSA) The PSA usually arises from the PICA and, sometimes, from the vertebral artery [24]. It divides into an ascending and descending ramus (Fig. 3.14). The ascending ramus is more variable and runs upward toward the lower end of the fourth ventricle (calamus scriptorius). The descending ramus courses downward, roughly along the posterolateral sulcus on the dorsal surface of the lower medulla and cord.

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Fig. 3.7 Diagram showing the territory of the lateral and medial branches of the posterior inferior cerebellar artery (PICA) (stippled areas) (reproduced from [1]). (a–d) territory of the lateral branch of the PICA. The lateral branch sometimes supplies the tonsil, but does not participate in supplying the medulla. This territory normally supplied by the lateral branch of the PICA is supplied by a large anterior inferior cerebellar artery (AICA) when the PICA is hypoplastic. (e–h) territory of the medial branch of the PICA. The medial branch supplies the uvula, nodulus, and tonsil and, sometimes, the pyramis and declive. This is the only branch of the PICA that participates in supplying the dorsal part of the medulla (f)

3.3.3 Anterior Spinal Artery (ASA) The vascular root of the ASA typically arises from the most distal portion of the VA (see Fig. 3.20) and descends to meet its counterpart to form a single ASA that runs in the anteromedian sulcus. It gives rise to the anteromedial group of medullary vessels and may continue to the cervical cord and downward.

3.3.4 Anterior Inferior Cerebellar Artery (AICA) The AICA arises from the caudal third of the basilar artery in 75% of people and, sometimes, from the middle third [17]. According to the nomenclature of Naidich’s group, the artery bifurcates just after crossing the sixth nerve into rostrolateral and caudomedial branches [20]. The rostrolateral branch extends to the seventh and eighth nerves rostral to the flocculus, forms a laterally convex loop, the meatal loop, which is directed toward the internal auditory meatus [15], and peripherally enters the horizontal fissure. The caudomedial branch is quite variable in size and runs toward the pontomedullary sulcus and the foramen of Luschka just caudal to the flocculus. When the posterior

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Fig. 3.8 Diagrams show the territory of the anterior inferior cerebellar artery (AICA) (stippled areas) (reproduced from [1]). The AICA supplies the lateral pontine area, middle cerebellar peduncle, and flocculus. When the posterior inferior cerebellar artery (PICA) is hypoplastic, the AICA supplies the territory usually supplied by the lateral branch of the PICA. (a) Posterior and (b) lateral views of the cerebellum. (c–f) Transverse sections through the (c) lower medulla, (d) upper medulla, (e) midpons, and (f) upper pons. (g) Magnified diagram through the midpons and the abducens nucleus. Vn motor and sensory nuclei of trigeminal nerve; VIn abducens nucleus; VII facial nerve; VIIn facial nucleus; VIII vestibulocochlear nerve; VIIIv vestibular nucleus; CTT central tegmental tract; DN dentate nucleus; Fl flocculus; ICP inferior cerebellar peduncle; MCP middle cerebellar peduncle; ML medial lemniscus; No nodulus; SCP superior cerebellar peduncle; SThT spinothalamic tract

inferior cerebellar artery is hypoplastic, the caudomedial branch of the anterior inferior cerebellar artery is well developed and supplies the territory that usually belongs to the lateral branch of the PICA [1]. Thus, the AICA supplies a part of the pons and much of the middle cerebellar peduncle and the anterior or petrosal aspect of the cerebellum

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Fig. 3.9 Diagrams show the territory of the superior cerebellar artery (SCA) (stippled areas) (reproduced from [1]). The brainstem territory of the SCA is limited to the superior pontine tegmentum and includes the superior cerebellar peduncle. The SCA supplies the dentate nucleus exclusively and the inferior semilunar lobule infrequently. (a) Posterior and (b) lateral views of the cerebellum. (c–f) Transverse sections through the (c) lower medulla, (d) upper medulla, (e) midpons, and (f) upper pons, (g) Magnified diagram through the upper pons. IV trochlear nerve; Vms mesencephalic nucleus and tract of the trigeminal nerve; CTT central tegmental tract; LC locus ceruleus; LL lateral lemniscus; ML medial lemniscus; MLF medial longitudinal fasciculus; SCP superior cerebellar peduncle; SThT spinothalamic tract

including the anterior portion of the inferior and superior semilunar lobules, the flocculus, the anterior portion of the quadrangular lobule and the choroid plexus in the cerebello-pontine angle, and the adjacent part of the lateral recess of the fourth ventricle (Fig. 3.8) [3, 24]. As well, the AICA often gives rise to the internal auditory artery and subarcuate artery [15].

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3.3.5 Internal Auditory Artery The internal auditory artery originates from either the anterior inferior cerebellar artery or basilar artery, runs in close association with the facial and vestibulocochlear nerves, gives off a subarcuate artery that runs laterally and penetrates the dura and temporal bone at the subarcuate fossa to supply the middle ear structures [24], and finally enters the internal auditory canal and supplies the labyrinthine structures.

3.3.6 Superior Cerebellar Artery (SCA) The SCA is the most constant of the three cerebellar arteries. It originates from the BA just proximal to the terminal bifurcation or, rarely, as a branch of the posterior cerebral artery. The SCA may be segmented into four, the anterior pontine, ambient, quadrigeminal, and terminal (vermian and hemispheric) segments (Fig. 3.5) [7]. Passing around the upper pons or pontomesencephalic sulcus (usually at the anterior pontine segment), it divides into lateral and medial branches [24], which sometimes arise separately from the basilar artery (double SCAs) [6] and supply the tentorial surface of the cerebellum and the laterotegmental portion of the rostral pons [1, 17]. The lateral branch supplies the superior semilunar lobule, quadrangular lobule, superior cerebellar peduncle, a part of the middle cerebellar peduncle, and, possibly, the cerebellar nuclei. The medial branch gives rise to small twigs to the inferior colliculus and the precentral cerebellar artery [9], or rhomboidal artery [10], which travels down the superior cerebellar peduncle within the cerebello-mesencephalic fissure to reach the dentate and other central nuclei. The medial branch also gives off cerebellar cortical branches that distribute to the medial portions of the superior semilunar and quadrangular lobules and the superior vermis (Fig. 3.9). Additionally, some cerebellar cortical arteries of the SCA give rise to arteries that penetrate deep into the white matter to reach the dentate nucleus [24]. Thus, the dentate nucleus, the most common site of spontaneous cerebellar hemorrhage, is supplied by precentral cerebellar arteries that travel down the superior cerebellar peduncle and by penetrating vessels from the cortical SCA vessels over the superior cerebellar surface. Both come from the SCA (Figs. 3.10–3.12). Although some authors indicate that small branches of the PICA also help supply the dentate nucleus [4, 12], others disagree, reporting that the PICA never supplies the dentate nucleus [1] or that dentate vascularization is carried out by the branches of the SCA with [10] or without [24] reference to the contribution of the PICA. The border zone between the SCA and PICA is presumed to be around the horizontal fissure on the posterior surface of the hemisphere, though, deep within the hemisphere, it may be in the cerebellar white matter.


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Fig. 3.10 Paramedian sagittal microangiograms show the supply of the dentate nucleus. The precentral cerebellar arteries (arrow), which are branches of the superior cerebellar artery (SCA), travel down along the superior cerebellar peduncle within the cerebello-mesencephalic fissure to supply the dentate nucleus, which here shows dense capillary blush. A few other branches from the hemispheric branch of the SCA (arrowheads) course down through the white matter to reach the dentate

3.4 Internal Vascular Supply of the Brainstem 3.4.1 Overview of Brainstem Vessels with Microangiographic Findings Figures 3.13 and 3.14 illustrate the entire system of arteries on the anterior and posterior surfaces of the brainstem [19, 27]. Because the surface-distributing arteries of the brainstem vary in size and distribution, occlusion of the same artery can produce different symptoms in different individuals [24]. Similarly, occlusion of different surface arteries may produce a similar syndrome and/or area of infarction. In contrast to such surface arteries, the penetrating arteries have a relatively fixed pattern [24], and brainstem syndromes tend to be organized based on the more constant internal vascular pattern. Figures 3.15–3.18 are microangiographic images that show how individual arteries penetrate, course, and branch and how they differ at different levels. Unlike the sinuous superficial arteries, the routes of the internal arteries generally look straight. Furthermore, midline sagittal microangiograms (Fig. 3.15) show that the median arteries are compressed ventrally and fanned posteriorly in the mesencephalon and diencephalon, which can presumably be attributed to bending at the cephalic flexure [24]. The inverse pattern

144 Fig. 3.11 Consecutive sagittal microangiograms show the supply of the dentate nucleus. The precentral cerebellar arteries (arrow in a) and a few branches from the hemispheric branch of the superior cerebellar artery (SCA, arrowheads in a and b) are shown to reach the dentate nucleus

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is seen in the pons; the median arteries at the level of the pontomesencephalic junction course posteriorly downward to reach the superior pontine tegmentum, whereas those at the pontomedullary junction go posteriorly upward to reach the inferior pontine tegmentum (Fig. 3.16). Such a vascular pattern may be attributable to the expansion of the pontine basis during development. We describe the vascular supply of the brainstem based on the relatively constant internal pattern reported by Stephens and Stilwell [24] and especially by Duvernoy and associates [2, 27]. They divided the brainstem arteries into anteromedial, anterolateral, lateral, and posterior groups according to the point of arterial penetration into the surface of the brainstem, and these groups may be regarded as equivalent or at least similar to the respective median, paramedian, short circumferential, and long circumferential arterial groups.

3 Intracranial Arterial System: Infratentorial Arteries Fig. 3.12 Coronal microangiograms of the cerebellum show the supply of the dentate nucleus (reproduced from [23]). A few branches from the hemispheric branch of the superior cerebellar artery (arrowheads in a and b) are shown to reach the capillary blush of the dentate nuclei

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Tatu’s team [27] diagrammed the individual vascular territories (Fig. 3.19) based on the study of Duvernoy [2].

3.4.2 Vascular Supply of the Medulla 3.4.2.1 The Anteromedial Group The anteromedial group of medullary arteries arise from the most distal part of the vertebral artery (V4) and the anterior spinal artery and both its vascular roots, and penetrate the anteromedian sulcus and foramen cecum (Fig. 3.20) [13]. They range in number from 1 to 11 (mean, 6.5) and in diameter between 100 and 520 mm [13]. They often have anastomoses with each other, particularly in the region of the foramen cecum, although right-left anastomoses occur infrequently [13]. Commonly observed within the brainstem including the medulla, pons, and midbrain, are the long and short arteries of the anteromedial group

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Fig. 3.13 Anterior view showing the general arrangement of the brainstem and cerebellar arteries (reproduced from [19]). AChA anterior choroidal artery; AICA anterior inferior cerebellar artery; AICA-mcp anterior inferior cerebellar artery, branch to the middle cerebellar peduncle; ALS anterolateral sulcus (preolivary sulcus); AMS anteromedian sulcus; ASA anterior spinal artery; BA basilar artery; CoA collicular artery; FC foramen cecum; ILPA inferolateral pontine artery; IPF interpeduncular fossa; IPMA inferior paramedian mesencephalic arteries (the superior pontine artery, anteromedial group (the PoA-AMs), which enters the interpeduncular fossa (see Fig. 3.16); LMFAi lateral medullary fossa artery, inferior rami; LMFAm lateral medullary fossa artery, middle rami; LMFAp lateral medullary fossa artery, posterior rami; LMFAs lateral medullary fossa artery, superior rami; M mamillary body; MdA-AL medullary artery, anterolateral group; MdA-AM medullary artery, anteromedial group; MPChA medial posterior choroidal arteries; MsA-AL mesencephalic artery, anterolateral group; PCA posterior cerebral artery; PCoA posterior communicating artery; PICA posterior inferior cerebellar artery; PoA-AL pontine artery, anterolateral group, arising from the BA; PoA-AMi inferior pontine artery, anteromedial group, which enters the foramen cecum; PoA-L pontine artery, lateral group; SCA superior cerebellar artery; SCA-L superior cerebellar artery, lateral branch; SCA-M superior cerebellar artery, medial branch; SLPA superolateral pontine artery; SPMA superior paramedian mesencephalic arteries; TPA thalamoperforate arteries; VA vertebral artery; Vm motor root of trigeminal nerve; Vse sensory root of trigeminal nerve

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3 Intracranial Arterial System: Infratentorial Arteries Fig. 3.14 Posterior view of the brainstem showing arteries on the dorsal aspect (after removal of the cerebellum by sections of the cerebellar peduncles) (reproduced from [27]). 4Vf floor of the fourth ventricle; CP cerebral peduncle; ICo inferior colliculus; ICP inferior cerebellar peduncle; MCP middle cerebellar peduncle; MdA-P posterior group of medullary arteries; MSrh median sulcus of the rhomboid fossa; Ox obex; PICA posterior inferior cerebellar artery; PoA-P posterior group of pontine arteries; PSA posterior spinal artery; SCA-L superior cerebellar artery, lateral branch; SCA-M superior cerebellar artery, medial branch; SCP superior cerebellar peduncle; SL sulcus limitans; SMV superior medullary velum

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of perforators. The long arteries are larger and course posteriorly on each side of the midline to reach the floor of the fourth ventricle in the superior medulla, and the smaller short arteries may deviate slightly laterally but do not reach the floor (Figs. 3.16–3.18). On the whole, their supply area includes the medial side of the pyramids, pyramidal decussation, medial lemniscus, medial longitudinal fasciculus, hypoglossal nucleus, central reticular formation, dorsal accessory olivary nucleus, and the medial part of the inferior olivary nucleus [2, 24]. Interestingly, individual vessels do not transgress the midline and do observe a unilateral supply [18]. Some of the vessels of the foramen cecum course in an anterior–posterior direction, but are inclined rostrally to reach the pontine tegmentum [2] and supply the superior end of the hypoglossal nucleus, nucleus prepositus, abducens nucleus, genu of the facial nerve, medial longitudinal fasciculus, tectospinal tract, medial lemniscus, pyramids, and reticular formation [24].

3.4.2.2 The Anterolateral Group The anterolateral group of medullary arteries arises from the anteromedial group and enter the pyramid and the anterolateral sulcus to supply most of the pyramids and the medial part of the inferior olivary nucleus.

148 Fig. 3.15 Sagittal microangiograms of the brainstem arteries. Sagittal section in the midline of the brainstem shows the median arteries penetrating the entire brainstem. Note that the median arteries at the level of the pontomesencephalic junction traverse posteriorly downward to reach the pontine tegmentum (open arrowhead in a), and those at the pontomedullary junction course posteriorly upward to reach the pontine tegmentum (arrowhead in b). Such a vascular pattern may be attributable to expansion of the pontine basis during development [24]. PMdS pontomedullary sulcus (foramen cecum); PMsS pontomesencephalic sulcus

S. Takahashi

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PoA-AMs (IPMA)

PoA-AMm PTg

PoB BA

PoA-AMi

PoA-AMsh

Fig. 3.16 Sagittal section of the pons showing the paths of different pontine arteries (reproduced from [19]). The long anteromedial group of pontine arteries at the intermediate level (PoA-AMs) enter the basilar sulcus or its vicinity and supply the middle pontine tegmentum by a direct penetrating pathway. The anteromedial group of superior pontine arteries (PoA-AMs), also called the inferior paramedian mesencephalic arteries (IPMA), arise from the distal basilar artery and penetrate the lower end of the interpeduncular fossa, and display a characteristic curved and descending pathway to finally supply the superior pontine tegmentum. In contrast, the long anteromedial group of inferior pontine arteries (PoA-AMi) enter the foramen cecum, and reach the inferior pontine tegmentum by a characteristic curved and ascending pathway. BA basilar artery; PoA-AMi inferior pontine artery, anteromedial group; PoA-AMm middle pontine artery, anteromedial group; PoAAMs superior pontine arteries, anteromedial group (also referred to as IPMA inferior paramedian mesencephalic arteries; see above); PoA-AMsh short pontine arteries, anteromedial group supplying the basilar portion of the upper and lower pons; PoB pontine basis; PTg pontine tegmentum

150 Fig. 3.17 Transaxial microangiograms from several different brains of brainstem arteries (in ascending order). (a, b) At the medullary level, one characteristic feature of the arterial supply is the rich vascularization of the lateral medullary fossa posterior to the olive by the numerous lateral group of arteries from several sources (pink open arrowheads). The long lateral arteries reach the fourth ventricular floor of the medulla to supply a portion of the tegmentum lateral to the paramedian region supplied by the long arteries of the anteromedial group.

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b

3 Intracranial Arterial System: Infratentorial Arteries Fig. 3.17 (continued) ( c–e) At the mid-pontine level, the longer arteries of the anteromedial group (yellow arrow), respecting the midline, reach the fourth ventricular floor, and the shorter arteries (yellow arrowhead) go no further than the medial lemniscus, sending rami to the medial zone of the corticospinal tract. Consequent to the opening of the fourth ventricle and the anterior shifting of the lateral structures, the lateral group run almost ventral to dorsal but not lateral to medial (blue arrow) [24], and there are no posterior group of vessels at this level.

c

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151

152 Fig. 3.17 (continued) ( f–h) At the midbrain level, a great number of long and short mesencephalic arteries enter the interpeduncular fossa to supply an extensive area in the median and paramedian region of the midbrain (orange arrows). The lateral and posterior groups of vessels consist of numerous and very fine vessels that vascularize a small territory

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3 Intracranial Arterial System: Infratentorial Arteries Fig. 3.18 Transaxial microangiograms of brainstem arteries (reproduced from [23]). (a, b) At the medullary level, (c) at the pontine level, (d) at the midbrain level. Features of the brainstem arteries described for Fig. 3.3.17 are again shown

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3.4.2.3 The Lateral Group The lateral group of medullary arteries supplies a hollow posterior to the olive, the lateral medullary fossa, which is bounded by the lower margin of the pons or pontomedullary sulcus with the roots of the facial and vestibulocochlear nerves, by the cerebellum and lateral recess of the fourth ventricle, and by the olive (Fig. 3.21) [2]. This region is richly vascularized in and around the retro-olivary sulcus (Figs. 3.17 and 3.18), which is involved in lateral medullary (Wallenberg) syndrome, a clinically well-known disorder. The lateral group of medullary arteries that supply this region may be called lateral medullary fossa arteries, and comprise mainly the direct branches of the VA, and additional branches from the posterior inferior cerebellar artery, BA and AICA (Fig. 3.21) [2, 24]. The supply area includes the spinothalamic and ventral spinocerebellar tracts, internal arcuate fibers, nucleus ambiguus, hypoglossal and vagal nuclei, nucleus of the solitary tract, inferior salivatory nucleus, vestibular nuclei, spinal trigeminal nucleus, dorsal accessory olivary nucleus, and the central reticular formation [2, 24].

3.4.2.4 The Posterior Group The posterior group arises from the posterior spinal artery and PICA. In the inferior or “closed” part of the medulla, below the level of the fourth ventricle, they supply the gracile and cuneate tubercles, nucleus of the solitary tract, vagal nucleus, area postrema, medial vestibular nucleus, and, sometimes, even the trigeminal nucleus [2, 24]. In the superior or “open” part of the medulla, the posterior group is absent.

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a

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ML SThT NA Vsp SoN GN/CN

Fig. 3.19 Serial transverse sections (4-mm thickness) of the brainstem and cerebellum are parallel to a bicommissural plane and show their arterial supply (reproduced from [27]). Vessels AICA anterior inferior cerebellar artery; IPMA inferior paramedian mesencephalic arteries; LMFAs lateral medullary fossa artery, superior rami;PICA posterior inferior cerebellar artery; PoA-AMi inferior pontine artery, anteromedial group; SCA superior cerebellar artery; SPMA superior paramedian mesencephalic arteries Structures other than vessels 3V third ventricle; 4V fourth ventricle; IIIn oculomotor nucleus; IV trochlear nerve; IVn trochlear nucleus; V trigeminal nerve; Vmc mesencephalic nucleus and tract of the trigeminal nerve; Vmo motor trigeminal nucleus; Vse principal sensory trigeminal nucleus; Vsp spinal trigeminal tract and nucleus; VIn abducens nucleus; VII facial nerve; VIIn facial nucleus; VIII vestibulocochlear nerve; VIIIv vestibular nucleus; IX glossopharyngeal nerve; X vagus nerve; Xd dorsal motor vagal nucleus; XIIn hypoglossal nucleus; Aq aqueduct of Sylvius; AQ anterior quadrangular lobule; Bi biventral lobule; CC central canal; Ce central lobule; CeA central lobule, ala; CN cuneate nucleus; CST corticospinal tract; Cu culmen; De declive; DN dentate nucleus; DSCP decussation of the superior cerebellar peduncle (SCP); Fl flocculus; Fo folium of vermis FPT frontopontine tract; GN gracile nucleus; Hth hypothalamus; ICo inferior colliculus; ICP inferior cerebellar peduncle; IO inferior olivary nucleus; IPF interpeduncular fossa; IS inferior semilunar lobule; LC locus ceruleus; LGB lateral geniculate body; LL lateral lemniscus; MCP middle cerebellar peduncle; M mamillary body; ML medial lemniscus; MLF medial longitudinal fasciculus; NA nucleus ambiguus No nodulus; OT optic tract; PoN pontine nucleus; PQ posterior quadrangular lobule (lobulus simplex); Prp nucleus prepositus; PTPT parietotemporopontine tract; Pyr pyramid of vermis; RN red nucleus; SCo superior colliculus; SCP superior cerebellar peduncle; SN substantia nigra; SNc substantia nigra, pars compacta; SNr substantia nigra, pars reticulata; SO superior olivary nucleus; SoN nucleus of the solitary tract; SS superior semilunar lobule; SThT spinothalamic tract; To tonsil; Tu tuber; Uv uvula

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: Anteromedial group :

Anteromedial group of inferior pontine arteries (PoA-AMi), and anteromedial group of superior pontine arteries (PoA-AMs), namely, the inferior paramedian mesencephalic arteries (IPMA)

: Anterolateral group : Lateral group : Superior rami of the lateral medullary fossa arteries (LMFAs) on e-g., : Posterior group : Lateral brach of the PICA : Medial branch of the PICA : AICA : Lateral branch of the SCA : Medial branch of the SCA

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3 Intracranial Arterial System: Infratentorial Arteries MLF

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Fig. 3.20 Diagram showing the anteromedial group of medullary arteries (black) (reproduced from [13]). The anteromedial group of medullary arteries originate from the (a) vertebral artery (VA), (b) vascular root of the anterior spinal artery (ASA-vr), (c) anterior spinal artery (ASA), and (d) anterolateral group of medullary arteries (common stem of the anteromedial and anterolateral groups). VI abducent nerve; XII hypoglossal nerve; BA basilar artery; FC foramen cecum; O inferior olive; PMdS pontomedullary sulcus; Py pyramid of the medulla; VA vertebral artery

3.4.3 Vascular Supply of the Pons 3.4.3.1 The Anteromedial Group The anteromedial group of pontine arteries arise from the basilar artery either directly or by trunks common to the arteries of the lateral group [2, 14]; superior, middle, and inferior subgroups are distinguished [14]. The inferior perforators (PoA-AMi in Figs. 3.13 and 3.16) vary in number from 2 to 5 and in diameter, from 80 to 600 mm, arise from the initial part of the BA and often branch off into individual vessels, penetrate the foramen cecum [14], and intraparenchymally reach the inferior levels of the pontine tegmentum. The middle perforators (PoA-AMm in Figs. 3.13 and 3.16) range in number from 5 to 9 and in diameter, from 210 to 940 mm; those caudal descend along the basilar sulcus, and those rostral ascend [14], both finally entering the pons through the sulcus.

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Po BA LMFAs

AICA

VI

VII

VIII LMFAp

FC Py

O

IX X

PMdS LMF

LMFAm

ROS LMFAi

PICA

VA ALS

Fig. 3.21 Lateral medullary fossa arteries. The lateral group of medullary arteries supply the lateral medullary fossa, which Duvernoy divides into four groups [2]: the inferior rami arise from the VA and PICA (LMFAi); the middle rami also from the VA and PICA (LMFAm); the superior rami from the BA and AICA (LMFAs), taking a central and cranial course toward the inferior pontine tegmentum; the posterior rami from the AICA (LMFAp). VI abducens nerve; VII facial nerve; VIII vestibulocochlear nerve; AICA anterior inferior cerebellar artery; ALS anterolateral sulcus (preolivary sulcus); ASA anterior spinal artery; BA basilar artery; FC foramen cecum; LMF lateral medullary fossa; O inferior olive; PICA posterior inferior cerebellar artery; PMdS pontomedullary sulcus; Po pons; Py pyramid of the medulla; ROS retro-olivary sulcus; VA vertebral artery

The superior perforators vary in number from 1 to 5 and in diameter, from 190 to 800 mm, originate from the terminal basilar artery or the superior cerebellar artery, and reach the interpeduncular fossa, where they form the inferior group of the interpeduncular fossa (IPMA: inferior paramedian mesencephalic arteries in Figs. 3.13 and 3.16). They supply a part of the inferior midbrain and the superior pontine tegmentum (Figs. 3.15 and 3.16) [2, 22]. Extraparenchymal anastomoses are frequently seen among these various anteromedial groups of pontine arteries [14]. Intraparenchymally, these perforators usually divide into short and long intrapontine vessels; the short arteries irrigate the medial part of the corticospinal tract, and the long arteries supply the structures of the pontine tegmentum close to the raphe and fourth ventricle. On the whole, all of the anteromedial groups of perforators supply the medial zone of the corticospinal tract, medial parts of the superior olive,

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medial lemniscus, and median zone of the pontine tegmentum, this latter region including the trapezoid body, central tegmental tract, medial longitudinal fasciculus, and reticular formation.

3.4.3.2 The Anterolateral Group The anterolateral group of pontine arteries arise from the anteromedial group, enter the anterolateral aspect of the pons, and curve around the corticospinal tract to supply its lateral region and thus supply the pontine nuclei [2].

3.4.3.3 The Lateral Group The lateral group of pontine arteries arise from two sources [2]; the superolateral and inferolateral pontine arteries generally arise from the basilar artery, and another lateral group arise from the anterior inferior cerebellar artery. The BA usually gives off the superolateral and inferolateral pontine arteries, which ramify over the lateral surface to penetrate the pons−the superolateral artery above/near the trigeminal nerve and the inferolateral artery below the nerve roots. Intraparenchymally, the lateral group of pontine arteries run almost ventral-dorsal (but not lateral to medial) consequent to the opening of the fourth ventricle and the anterior shifting of lateral structures [24] (Figs. 3.17 and 3.18). They supply the lateral lemniscus, central tegmental tract, and roots of the trigeminal nerve and extend to the principal sensory and motor trigeminal nuclei. The other lateral group of pontine arteries, which arise from the AICA, supply the inferior part of the lateral pontine surface. Some supply the middle cerebellar peduncle, possibly reaching the roots of the trigeminal nerve and the principal sensory nucleus, and others penetrate at the pontomedullary sulcus to form the superior rami of the lateral medullary fossa arteries (Fig. 3.21) [2]. The rami course centrally and upward toward the inferior pontine tegmentum to supply the superior olivary nucleus, facial nucleus, lateral lemniscus, and, sometimes, the lateral parts of the abducent nucleus and central tegmental tract.

3.4.3.4 The Posterior Group In the lower pons, there are no posterior brainstem structures in the region of the fourth ventricle, but at the level of the upper pons, the posterior aspect of the pons comprises the superior cerebellar peduncles (Fig. 3.14). The peduncles are supplied by the posterior group of arteries that derive from the superior cerebellar artery [2], some of which reach the dentate nucleus inferiorly (Fig. 3.10).


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3.4.4 Vascular Supply of the Midbrain 3.4.4.1 Arteries that Encircle and Supply the Midbrain According to Duvernoy’s classification of the midbrain, the anteromedial area consists of the interpeduncular fossa (Fig. 3.22); the anterolateral area consist of the cerebral peduncle, which is limited by the medial and lateral mesencephalic sulci; and the lateral area, which includes the lemniscal trigone posterior to the lateral mesencephalic sulcus and the brachia of the inferior and superior colliculi (Fig. 3.24b). The posterior area consists of the superior and inferior colliculi. The arteries of the midbrain arise from arterial trunks that curve around the mesencephalon and are (in ascending order): the SCA, collicular artery, medial posterior choroidal arteries (MPChA), PCA, and anterior choroidal artery (AChA) [19]. The collicular artery, also called the quadrigeminal or pedunculo-quadrigeminal artery, leaves the PCA near the side of the interpeduncular fossa, closely follows the pontomesencephalic sulcus, and gives rise to an inferior branch to reach the transverse intercollicular sulcus to anastomose with the branches of the SCA, and a superior branch that divides into numerous small rami to form a dense arterial network that covers the superior colliculi (Fig. 3.24) [2]. Frequently, an accessory collicular artery is present that courses as far as the lateral mesencephalic sulcus. The MPChA curves around the cerebral peduncle above the collicular artery, inclines to reach the lateral mesencephalic sulcus inferior to the medial geniculate body, and reaches the posterior surface of the midbrain near the edge of the pulvinar of the thalamus, where it gives off numerous branches to the pretectal area between the pulvinar, habenula, and pineal body. The PCA also courses around the midbrain overlying the collicular artery and the MPChA, but leaves the lateral surface of the midbrain near the medial geniculate body, thereby giving off no posterior branches, so that the MPChA take over the supply of the posterior surface of the superior part of the midbrain [2].

3.4.4.2 The Anteromedial Group The anteromedial group of mesencephalic arteries are made up of the arteries of the interpeduncular fossa. They may be subdivided into three groups [19] −in ascending order, the inferior paramedian mesencephalic arteries (IPMA) that finally reach the superior pontine tegmentum, the superior paramedian mesencephalic arteries (SPMA), and the thalamoperforate arteries (TPA) that supply the thalamus (Fig. 3.22). The TPA and SPMA can originate as single or common trunks from the P1 segment or take on other patterns of branching and entry through the posterior perforated substance as shown in Fig. 3.23. [22].

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a

M 3.25 + - 0.29mm TPA

8.11 + - 1.19mm

III

III

SPMA

IPMA Po Fig. 3.22 Interpeduncular fossa and interpeduncular fossa arteries. (a) Anteroinferior view of the interpeduncular fossa (viewing direction is indicated by an arrow in b) (reproduced from [22]). The interpeducular fossa is defined as the space limited by the mamillary body superiorly, the pontomesencephalic sulcus inferiorly, and the right and left medial mesencephalic sulci laterally from which the oculomotor nerves emerge [2, 22]. Along the base of the interpeduncular fossa behind the mamillary bodies is the posterior perforated substance, which is a depressed punctuated area shaped like a triangle with its base superior and apex inferior. The two distances indicate the length of the base and height of the triangle. (b) Sagittal section of the midbrain illustrating the interpeduncular fossa arteries. Perforators that enter the posterior perforated substance at the interpeduncular fossa, or the interpeduncular fossa arteries, may be divided into superior, middle, and inferior vessels. The superior group are equivalent to the thalamoperforate arteries (TPA) that supply the thalamus; the middle group are the superior paramedian mesencephalic arteries (SPMA); and the inferior group are the inferior paramedian mesencephalic arteries (IPMA), namely the anteromedial group of superior pontine arteries (PoA-AMs), that finally reach the superior pontine tegmentum. Circles in (a) indicate the entrance points of the three groups of the interpeduncular fossa arteries − the TPA, SPMA, and IPMA, respectively. The mesencephalic arteries are smaller and more medial than the TPA [22]. (c) Diagram showing the origin, course, and point of penetration of the IPMA (reproduced from [22]). III oculomotor nerve; IV trochlear nerve; AC anterior commissure; BA basilar artery; CP cerebral peduncle; DSCP decussation of the superior cerebellar peduncle; ICo inferior colliculus; IPF interpeduncular fossa; IPMA inferior paramedian mesencephalic arteries (superior pontine arteries, anteromedial group); M mamillary body; MI massa intermedia; MMS medial mesencephalic sulcus; P1 P1 segment of the posterior cerebral artery; PCA posterior cerebral artery; PCoA posterior communicating artery; Po pons; RN red nucleus; SCA superior cerebellar artery; SCo superior colliculus; TTA thalamotuberal artery

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3 Intracranial Arterial System: Infratentorial Arteries Fig. 3.22 (continued)

b TTA MI AC

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PCoA

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IPMA BA

Po

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BA

The IPMA (PoA-AMs: superior pontine arteries, anteromedial group in Fig. 3.13 and 3.16) arise from arterial trunks originating from the P1 segment, the proximal 7 mm of both SCA, and the last 5 mm of the basilar artery [14, 22] (Fig. 3.22c). The IPMA penetrate the lower angle of the interpeduncular fossa or the superior margin of the pons overhanging the fossa

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a

b

TPA

e

TPA

P1

f

TPA+SPMA

d

c

SPMA

SPMA

h

TPA+SPMA

TPA+SPMA

Fig. 3.23 Variation of the interpeduncular fossa arteries (thalamoperforate (TPA) and superior paramedian mesencephalic (SPMA) arteries) in the pattern of branching and entry through the posterior perforated substance (Reproduced from [22]). (a, b) Single trunk unilateral TPA. (c, d) Single trunk unilateral SPMA. (e) Common trunk unilateral. (f) Common trunk bilateral. (g) Common trunk contralateral

and slant in a rostrocaudal direction (Figs. 3.15 and 3.16) to supply a paramedian part of the inferior midbrain and the superior pontine tegmentum that includes the caudal part of the decussation of the superior cerebellar peduncle, medial part of the medial lemniscus, locus ceruleus, and medial longitudinal fasciculus [2, 5, 22, 24]. The SPMA mainly arise from the P1 segment of the PCA and a few, from the collicular artery or MPChA [2]. They enter the central part of the posterior perforated substance; the longer median arteries course in or near the midline, and the shorter paramedian arteries curve laterally and embrace the red nucleus (Fig. 3.18d) [24]. The SPMA supply the median and paramedian regions of the midbrain, including the decussation of the superior cerebellar peduncle, interpeduncular nucleus, red nucleus, medial zone of the substantia nigra, trochlear and oculomotor nuclei, central tegmental tract, medial lemniscus, medial longitudinal fasciculus, and periaqueductal gray matter [2, 24]. The TPA are described elsewhere (see Sect. 2.4.3 in Chap. 2).


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3.4.4.3 The Anterolateral Group The anterolateral group of mesencephalic arteries arise mainly from the collicular artery and MPChA and to a lesser extent, from the anterior choroidal arteries and the PCA [2, 19], and supply the cerebral peduncle, substantia nigra, medial lemniscus, and, possibly, the lateral part of the red nucleus [2].

3.4.4.4 The Lateral Group The lateral group of mesencephalic arteries comprise branches arising from the medial and lateral SCA, collicular artery, and MPChA and follow the midbrain surface along a straight route until they reach and mainly enter the lateral mesencephalic sulcus (Fig. 3.24) [2, 19]; they supply the spinothalamic tract, medial and lateral lemnisci, mesencephalic nucleus of the trigeminal nerve, central tegmental tract, and the surrounding reticular formation [2, 24]. Arteries of this group to the diencephalon represent the thalamogeniculate arteries.

3.4.4.5 The Posterior Group The posterior group of mesencephalic arteries comprises branches arising from the medial SCA, collicular artery, and MPChA [19]. The branches of the medial SCA form a dense arterial network that cover the superior part of the inferior colliculus and traverse the intercollicular sulcus [2]; the collicular artery forms an arterial network to supply the superior colliculus inferiorly; and the MPChA often supplies the upper part of that structure as well as the medial geniculate body, pretectal region, pulvinar (pulvinar arteries), pineal body, and habenular trigone [2]. Over the collicular surface, there are numerous anastomoses between the branches of the SCA and collicular artery and between the collicular artery and MPChA. However, only a few anastomoses occur between the left and right networks, which seem to be separated by an avascular zone along the vertical intercollicular sulcus [2].

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a Pu LGB MGB BVR

TGA

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LMV MPChA

CoA CoA

SCA -M SCA -M V

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Anterior

Fig. 3.24 Left lateral view of the mesencephalon showing mesencephalic arteries (reproduced from [2]). (a) Left lateral view of the mesencephalon (after removal of the posterior cerebral artery (PCA)). (b) Left lateral view of the mesencephalon (after removal of the cerebellum). The square of dashed lines indicates the field of view in (a). (c) Left lateral view of the mesencephalon showing circumferential arteries of the midbrain: superior cerebellar artery (SCA, red); collicular artery (CoA, green); medial posterior choroidal arteries (MPChA, blue) and thalamogeniculate arteries (TGS, blue); all the veins, black. The PCA is removed. Vessels AcCoA accessory collicular artery; AICA anterior inferior cerebellar artery; BVR basal vein of Rosenthal; CoA (CoA1, CoA2) collicular artery (superior and inferior branches); LMV lateral mesencephalic vein; PrCV precentral cerebellar vein; SCA-L superior cerebellar artery, lateral branch; SCA-M superior cerebellar artery, medial branch; TGA thalamogeniculate artery; TPV transverse pontine vein; VPM vein of the pontomesencephalic sulcus. Other than vessels IV trochlear nerve; V trigeminal nerve; CP cerebral peduncle; ICo inferior colliculus; ICoBr brachium of the inferior colliculus; LGB lateral geniculate body; LMS lateral mesencephalic sulcus; LmTr lemniscal trigone (lateral aspect of the mesencephalon); MGB medial geniculate body; PB pineal body; Pu pulvinar; SCo superior colliculus; SCoBr brachium of the superior colliculus; SCP superior cerebellar peduncle; SMV superior medullary velum

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Fig. 3 25 Diagram representing complementary roles in vascularization of the midbrain. When the horizontal rectangle (heavy line) is regarded as the lateral profile of the midbrain, the territories of individual arteries are arranged as nearly parallel ascending bands. The headings, “Anteromedial,” “Anterolateral,” “Lateral,” and “Posterior,” indicate the groups of mesencephalic arteries. In ascending order from the bottom of the midbrain profile are the territories of the superior cerebellar artery (SCA, red), collicular artery (CoA, green), medial posterior choroidal artery (MPChA, blue), posterior cerebral artery (PCA, light blue), and anterior choroidal artery (AChA)/posterior communicating artery (PCoA, white). For example, as the PCA courses around the midbrain, it gives off many branches in the anterior part, thus covering a large area in the anteromedial group in the profile; however, the PCA leaves the lateral surface of the midbrain near the medial geniculate body on its way toward the temporo-occipital lobe and thereby gives off no posterior branches. At this point, the MPChA take over supply of the posterior surface of the midbrain and cover a large area in the posterior aspect. ICo inferior colliculus; IPF interpeduncular fossa; LMS lateral mesencephalic sulcus; M mamillary body; PB pineal body; PMsS pontomesencephalic sulcus; SCA superior cerebellar artery; SCo superior colliculus; SCP superior cerebral peduncle; TGA thalamogeniculate artery


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3.4.4.6 Complementary Roles in the Vascularization of the Midbrain On the whole, different arteries have complementary roles in vascularizing the midbrain [2]. Because their almost parallel courses incline, the arteries that supply the midbrain serve territories that arrange in ascending bands (Fig. 3.25). In the lowest band, the SCA has a few branches in the anterior part of the midbrain, more in the lateral part, and most in the posterior part; in the highest band, the PCA has most branches in the anterior part, a few in the lateral part, and none in the posterior part. The two intermediate bands are supplied by the collicular artery and MPChA, mainly in the lateral and posterior regions [2]. Additionally, the anterior choroidal artery and posterior communicating artery give off some inconstant arteries that supply the superior levels in the cerebral peduncle.

3.5 Representative Imaging Findings in Cases with Infarcts in the Distribution of the Infratentorial Arteries (Figs. 3.26–3.33) Fig. 3.26 Infarct in the anteromedial group of medullary arteries in a 71-year-old man, who suddenly developed right hemiparesis that excluded the face and, on examination, was revealed to have dyspnea, which was ascribed to bulbar palsy. (a) Axial, (b) coronal, and (c) sagittal T2-weighted images show an infarct as far as the fourth ventricular floor in the left paramedian region of the upper medulla (arrow)

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3 Intracranial Arterial System: Infratentorial Arteries Fig. 3.27 Infarct in the lateral group of medullary arteries and in the posterior inferior cerebellar artery (PICA) distribution of the cerebellum in a 62-year-old man, who suddenly developed headache and vertigo. On examination, symptoms including nystagmus, hoarseness, right cerebellar ataxia, right Horner sign, and crossed and dissociated sensory loss to temperature and pain involving the right face and left trunk of the body led to clinical diagnosis of Wallenberg syndrome. (a) Axial, (b) sagittal, and (c) coronal T1-weighted images obtained a month and a half after symptom onset show an infarct in the right lateral region of the medulla as well as in the inferior medial aspect of the cerebellar hemisphere (blue arrows in (a-c)) that corresponds to the distribution of the medial branch of the posterior inferior cerebellar artery (PICA). The right vertebral artery shows no flow void, but a hyperintense signal (orange arrowheads in (a) and (b)) indicateing its thrombotic occlusion, which was confirmed by angiography

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176 Fig. 3.28 Infarct in the anteromedial group of pontine arteries in a 54-year-old man, who suddenly developed left hemiparesis with gait difficulty and dysarthria. (a) Axial T2-weighted image shows an infarct in the right paramedian region of the pons (arrow), which barely reaches the fourth ventricular floor but does not transgress the midline. (b) Axial microangiogram of the pons. Note that the lesion (a) extends on a path that almost traces the distribution of the anteromedial group of pontine arteries (arrow). The lateral group of pontine arteries are noted by the open arrowhead

Fig. 3.29 Infarct in the lateral group of pontine arteries in a 54-year-old man, who suddenly developed disturbance of consciousness with quadriparesis predominant on the left. Axial T2-weighted image shows an arc-shaped infarct in the right lateral region of the pons (open arrowhead). Note that the lesion extends on a course almost tracing the distribution of the lateral group of pontine arteries in Fig. 3 28b

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3 Intracranial Arterial System: Infratentorial Arteries Fig. 3 30 Infarct in the supply area of the superior paramedian mesencephalic arteries (SPMA) and thalamoperforate arteries (TPA) in a 68-year-old man, who suddenly developed left oculomotor palsy and right hemiparesis. (a–c) Axial T2-weighted images show lesions in the left paramedian region of the midbrain (arrowheads) and in the central zones of both thalami (open arrowheads). (d) Coronal T1-weighted image shows that the larger lesion on the left extends from the paramedian midbrain to the central zone of the thalamus (arrow). Note that this configuration is similar to the distribution of the TPA on coronal microangiograms (see Fig. 2.44b, Chap. 2)

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3 Intracranial Arterial System: Infratentorial Arteries Fig. 3.31 Infarct in the distribution of the posterior inferior cerebellar artery (PICA) in a 69-year-old man. (a) T1-weighted image (b) T2-weighted image. The extent of the linear lesion (arrow) probably represents the distribution of a radially coursing hemispheric branch of the PICA over the lower surface of the cerebellum. Compare with Fig. 3.4a

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180 Fig. 3.32 Infarct in the supply area of the anterior inferior cerebellar artery (AICA) in a 63-year-old man, who suddenly developed vertigo, nausea, left facial paresthesia, and right hemiparesis, and was found to have dysarthria and left cerebellar ataxia (dysmetria). (a) Axial, (b) coronal, and (c) sagittal T2-weighted images show an infarct in the lateral pons and middle cerebellar peduncle and anterior surface of the cerebellar hemisphere on the left (arrows). (d) Anteroposterior (AP) view of right vertebral angiogram shows absence of the left AICA, which indicates occlusion of that vessel (arrow)

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3 Intracranial Arterial System: Infratentorial Arteries Fig. 3.32 (continued)

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182 Fig. 3.33 Infarct in the supply area of the superior cerebellar artery (SCA) in a 60-year-old man, who suddenly developed tinnitus, vertigo, and nausea and was found to have left cerebellar ataxia. (a) Axial proton-densityweighted and (b) coronal and (c) sagittal T2-weighted images show an infarct in the superior surface of the cerebellar hemisphere on the left

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Abbreviations 3V Third ventricle 4V Fourth ventricle 4Vf Floor of the fourth ventricle III Oculomotor nerve IIIn Oculomotor nucleus IV Trochlear nerve IVn Trochlear nucleus V Trigeminal nerve Vms Mesencephalic nucleus and tract of the trigeminal nerve Vmo Motor trigeminal nucleus Vn Motor and sensory nuclei of the trigeminal nerve Vse Principal sensory trigeminal nucleus Vsp Spinal trigeminal tract and nucleus VI Abducens nerve VIn Abducens nucleus VII Facial nerve VIIn Facial nucleus VIII Vestibulocochlear nerve VIIIv Vestibular nucleus IX Glossopharyngeal nerve X Vagus nerve Xd Dorsal motor vagal nucleus XI Accessory nerve XII Hypoglossal nerve XIIn Hypoglossal nucleus AC Anterior commissure AcCoA Accessory collicular artery AChA Anterior choroidal artery AICA Anterior inferior cerebellar artery AICA-cm Caudomedial branch of the AICA AICA-mcp Anterior inferior cerebellar artery, branch to the middle cerebellar peduncle AICA-rl Rostrolateral branch of the AICA ALS Anterolateral sulcus (preolivary sulcus) AMS Anteromedian sulcus Aq Aqueduct of Sylvius AQ Anterior quadrangular lobule ASA Anterior spinal artery BA Basilar artery Bi Biventral lobule BVR Basal vein of Rosenthal CC Central canal Ce Central lobule ChA-4V Choroidal artery of the fourth ventricle

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ChBr Choroidal branch ChP Choroid plexus ChP-4V Choroid plexus of the fourth ventricle CMdF Cerebello-medullary fissure CMsF Cerebello-mesencephalic fissure CoA (CoA1, CoA2) Collicular artery (superior and inferior branches) CP Cerebral peduncle CPF-SL Superior limb of the cerebello-pontine fissure CPF-IL Inferior limb of the cerebello-pontine fissure CST Corticospinal tract CT Computed tomography CTT Central tegmental tract Cu Culmen De Declive DN Dentate nucleus DSCP Decussation of the superior cerebellar peduncle Fast Fastigium of the fourth ventricle FC Foramen cecum Fl Flocculus FL Lateral aperture of the fourth ventricle, foramina of Luschka FPT Frontopontine tract GN/CN Gracile nucleus/cuneate nucleus Gr Gracile lobule HF Horizontal fissure Hth Hypothalamus ICo Inferior colliculus ICoBr Brachium of the inferior colliculus ICP Inferior cerebellar peduncle ILPA Inferolateral pontine artery IMV Inferior medullary velum IO Inferior olivary nucleus IPF Interpeduncular fossa IPMA Inferior paramedian mesencephalic arteries (= PoA-AMs: superior pontine artery, anteromedial group, which enters the interpeduncular fossa and supplies the superior pontine tegmentum) IS Inferior semilunar lobule LC Locus ceruleus LGB Lateral geniculate body Li Lingula cerebelli LL Lateral lemniscus LMF Lateral medullary fossa LMFAi Lateral medullary fossa artery, inferior rami, arising from the VA and PICA LMFAm Lateral medullary fossa artery, middle rami, arising from the VA and PICA LMFAp Lateral medullary fossa artery, posterior rami, arising from the AICA


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LMFAs Lateral medullary fossa artery, superior rami, arising from the BA and AICA LMS Lateral mesencephalic sulcus LmTr Lemniscal trigone (lateral aspect of the mesencephalon) LMV Lateral mesencephalic vein M Mamillary body MCP Middle cerebellar peduncle Md Medulla oblongata MdA-AL Medullary artery, anterolateral group MdA-AM Medullary artery, anteromedial group, arising from the ASA and VA MdA-P Medullary artery, posterior group MGB Medial geniculate body MI Massa intermedia ML Medial lemniscus MLF Medial longitudinal fasciculus MMS Medial mesencephalic sulcus MPChA Medial posterior choroidal arteries MR Magnetic resonance Ms Mesencephalon MsA-AL Mesencephalic artery, anterolateral group MSrh Median sulcus of the rhomboid fossa No Nodulus O Inferior olive Ox Obex P1 P1 Segment of the posterior cerebral artery PB Pineal body PCA Posterior cerebral artery PCoA Posterior communicating artery PICA Posterior inferior cerebellar artery PICA-am Anterior medullary segment of the PICA PICA-lm Lateral medullary segment of the PICA PICA-pm Posterior medullary segment of the PICA PICA-st Supratonsillar segment of the PICA PICA-th Tonsillohemispheric branch of the PICA PICA-v Vermian branch of the PICA PMdS Pontomedullary sulcus PMsS Pontomesencephalic sulcus Po Pons PoA Pontine artery PoA-AL Pontine artery, anterolateral group PoA-AMi Inferior pontine artery, anteromedial group PoA-AMm Middle pontine artery, anteromedial group PoA-AMs Superior pontine arteries, anteromedial group (= IPMA: inferior paramedian mesencephalic arteries) PoA-AMsh Short pontine arteries, anteromedial group PoA-L Pontine artery, lateral group

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PoA-P PoB PoN PQ PrC PrCV Prp PSA PTg PTPT Pu Py Pyr RN ROS SCA SCA-am SCA-ap SCA-q SCA-v SCA-L SCA-M SCo SCoBr SCP SL SLPA SMV SN SNc SNr SO SoN SPMA SS SThT TGA To TPA TPV Tu Uv VA VPM

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Pontine artery, posterior group Pontine basis Pontine nucleus Posterior quadrangular lobule (lobulus simplex) Precentral cerebellar artery Precentral cerebellar vein Nucleus prepositus Posterior spinal artery Pontine tegmentum Parietotemporopontine tract Pulvinar Pyramid of the medulla Pyramid of vermis Red nucleus Retro-olivary sulcus Superior cerebellar artery Ambient segment of the SCA Anterior pontine segment of the SCA Quadrigeminal segment of the SCA Vermian segment of the SCA Superior cerebellar artery, lateral branch Superior cerebellar artery, medial branch Superior colliculus Brachium of the superior colliculus Superior cerebellar peduncle Sulcus limitans Superolateral pontine artery Superior medullary lamina Substantia nigra Substantia nigra, pars compacta Substantia nigra, pars reticulata Superior olivary nucleus Nucleus of the solitary tract Superior paramedian mesencephalic arteries Superior semilunar lobule Spinothalamic tract Thalamogeniculate artery Cerebellar tonsil Thalamoperforate arteries Transverse pontine vein Tuber Uvula Vertebral artery Vein of the pontomesencephalic sulcus


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References 1. Amarenco P, Hauw JJ. Anatomy of the cerebellar arteries. Rev Neurol (Paris). 1989; 145:267–76. 2. Duvernoy HM. Human brainstem vessels. Berlin: Springer; 1978. 3. Fujii K, Lenkey C, Rhoton Jr AL. Microsurgical anatomy of the choroidal arteries. Fourth ventricle and cerebellopontine angles. J Neurosurg. 1980;52:504–24. 4. Gillilan LA. Anatomy and embryology of the arterial system of the brain stem and cerebellum. In: Vinken PJ, Bruyn GW, editors. Handbook of clinical neurology. Amsterdam: North-Holland; 1975. p. 24–44. 5. Goto N. Morphological study of the brain blood vessels: the posterior perforated substance arteries and their sydrome. Nichidai Med J. 1971;30:983–1000 (in Japanese). 6. Hardy DG, Peace DA, Rhoton Jr AL. Microsurgical anatomy of the superior cerebellar artery. Neurosurgery. 1980;6:10–28. 7. Hoffman HB, Margolis MT, Newton TH. The posterior inferior cerebellar artery. In: Newton T, Potts D, editors. Radiology of the skull and brain. St Louis: CV Mosby; 1974. p. 1809–30. 8. Huang YP, Wolf BS. Angiographic features of fourth ventricle tumors with special reference to the posterior inferior cerebellar artery. Am J Roentgenol Radium Ther Nucl Med. 1969;107:543–64. 9. Huang YP, Wolf BS. Angiographic features of brain stem tumors and differential diagnosis from fourth ventricle tumors. Am J Roentgenol Radium Ther Nucl Med. 1970;110:1–30. 10. Icardo JM, Ojeda JL, Garcia-Porrero JA, Hurle JM. The cerebellar arteries: cortical patterns and vascularization of the cerebellar nuclei. Acta Anatomica. 1982;113:108–16. 11. Lister JR, Rhoton Jr AL, Matsushima T, Peace DA. Microsurgical anatomy of the posterior inferior cerebellar artery. Neurosurgery. 1982;10:170–99. 12. Margolis MT, Newton TH. The posterior inferior cerebellar artery. In: Newton T, Potts D, editors. Radiology of the skull and brain. St Louis: CV Mosby; 1974. p. 1710–74. 13. Marinkovic S, Milisavljevic M, Gibo H, Malikovic A, Djulejic V. Microsurgical anatomy of the perforating branches of the vertebral artery. Surg Neurol. 2004;61:190–7; discussion 197. 14. Marinkovic SV, Gibo H. The surgical anatomy of the perforating branches of the basilar artery. Neurosurgery. 1993;33:80–7. 15. Martin RG, Grant JL, Peace D, Theiss C, Rhoton Jr AL. Microsurgical relationships of the anterior inferior cerebellar artery and the facial-vestibulocochlear nerve complex. Neurosurgery. 1980;6:483–507. 16. Matsushima T, Rhoton Jr AL, Lenkey C. Microsurgery of the fourth ventricle: Part 1. Microsurgical anatomy. Neurosurgery. 1982;11:631–67. 17. Mohr JP, Caplan LR. Vertebrobasilar diseases. In: Mohr JP, Choi DW, Grotta JC, Weir B, Wolf PA, editors. Stroke: pathophysiology, diagnosis, and management. Philadelphia: Churchill Livingstone; 2004. p. 207–14. 18. Morris P. Practical neuroangiography. Philadelphia: Lippincott Williams & Wilkins; 2007. 19. Naidich TP, Duvernoy HM, Delman BN, Sorensen AG, Kollian SS, Haake EM. Vascularization of the cerebellum and the brain stem. Duvernoy’s atlas of the human brain stem and cerebelum. Wien: Springer; 2009. p. 159–217. 20. Naidich TP, Kricheff II, George AE, Lin JP. The normal anterior inferior cerebellar artery. Anatomic-radiographic correlation with emphasis on the lateral projection. Radiology. 1976;119:355–73. 21. Newton T, Mani R. The vertebral artery. In: Newton T, Potts D, editors. Radiology of the skull and brain. St Louis: CV Mosby; 1974. p. 1659–709.

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22. Pedroza A, Dujovny M, Ausman JI, Diaz FG, Cabezudo Artero J, Berman SK, et al. Microvascular anatomy of the interpeduncular fossa. J Neurosurg. 1986;64:484–93. 23. Salamon G. Atlas of arteries of the human brain. Paris: Sandoz; 1973. 24. Stephens RB, Stilwell DL. Arteries and veins of the human brain. Springfield, IL: Thomas; 1969. 25. Takahashi S. Imaging of cerebrovascular diseases. Chugai-Igakusha, Tokyo. (in Japanese), 2003; pp.15-56. 26. Takahashi S. MRI of the Brain: MR imaging anatomy of the human brain. Second edition, Shujunsha, Tokyo. (in Japanese), 2005; pp. 263-302. 27. Tatu L, Moulin T, Bogousslavsky J, Duvernoy H. Arterial territories of human brain: brainstem and cerebellum. Neurology. 1996;47:1125-35

Perforating Branches of the Anterior Communicating Artery: Anatomy and Infarction

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4.1 The Anterior Communicating Artery (ACoA) The ACoA connects both proximal parts of the anterior cerebral artery (ACA) and is the fundamental anastomotic part of the circle of Willis. It usually lies above the optic chiasm and within the lamina terminalis cistern. Its average length is 1.2–4.0 mm and average diameter, 1.2–1.7 mm [1, 9, 12, 20, 21]. A normal ACoA, defined as the artery connecting the right and left ACA through a single lumen, is found in only about 40% of cadaver brains [1,20,21]. ACoA anomalies, including plexiform configuration, fenestration, duplication, and other variations, are observed in the other 60%.

4.2 Perforating Branches of the ACoA (Figs. 4.1 and 4.2) During the 1970s, the ACoA was found to have a number of perforating branches [3, 6, 19], a finding reported as well in most recent studies. The average number of perforating branches ranges from 2.2 to 4.1 [20–23] and their average diameter, from 0.25 to 2.1 mm [1, 20–22]. Yaşargil et al. [24] stressed the clinical importance of these perforating branches of the ACoA and called them “the hypothalamic arteries.” Marinković et al. [12] classified them into small and large branches, the large branches including the subcallosal artery and the medial artery of the corpus callosum. Türe’s group [22] divided them into three subgroups, the hypothalamic, subcallosal, and median callosal arteries. Serizawa’s team [20] also classified the perforators into three subgroups, but designated the branches hypothalamic, subcallosal, and chiasmatic.

T. Fujii Department of Behavioral Neurology and Cognitive Neuroscience, Tohoku University Graduate School of Medicine, 2-1 Seiryo-machi, Aoba-ku, Sendai 980-8575, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_4, © Springer-Verlag London Limited 2010

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Fig. 4.1 Schematic drawing of the perforating branches of the anterior communicating artery (ACoA) (adapted from [20], with permission). 1 genu of the corpus callosum; 2 rostrum of the corpus callosum; 3 anterior commissure; 4, anterior cingulate gyrus; 5 paraterminal gyrus; 6 parolfactory gyrus; 7 septum pellucidum; 8 anterior hypothalamus. ACA anterior cerebral artery; Inf infundibulum; LT lamina terminalis; OC optic chiasm; ON optic nerve

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Fig. 4.2 Schematic drawings of the coronal image of the brain showing the plane at the paraterminal gyrus (left) and the plane at the anterior commissure (right) (adapted from [8], with permission). The areas supplied by the perforating branches of the anterior communicating artery, as determined by the infusion of contrast agent, are indicated by crosshatching and identified by numbers: 1 lamina terminalis; 2 mesial anterior commissure; 3 optic chiasm; 4 columns of the fornix; 5 septum; 6 corpus callosum; 7 cingulum; 8 subcallosal area; 9 anterior hypothalamus

The subcallosal branch (also known as the subcallosal artery) is a single artery and the largest of the perforating branches, having a diameter of approximately 0.5 mm [20, 22]. It originates from the posterosuperior or posterior aspect of the ACoA, ascends dorsally into the lamina terminalis cistern, and branches off to the hypothalamic area. This branch perfuses the rostrum and genu of the corpus callosum, anterior cingulate gyrus, subcallosal

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area (or parolfactory area), paraterminal gyrus, septum pellucidum, anterior commissure, and column of the fornix, some of which are part of the limbic system and Papez’s circuit. The most interesting characteristic of the subcallosal branch is its bilateral termination in these areas [20]. The median artery of the corpus callosum (also known as the median callosal artery) terminates beyond the genu of the corpus callosum and nourishes the dorsal part of the cingulate gyrus and, sometimes, the paracentral lobule of the bilateral hemisphere. The artery is observed in 9–30% of cadaver brains [10, 12, 22], and its diameter ranges from 0.4 to 2.1 mm (average 0.9 mm) [22]. This median artery follows the same course as that of the subcallosal artery and supplies the same structures, except that its distal extension reaches the body and, at times, even the splenium of the corpus callosum. According to some authors [12,20,22], the subcallosal and medial arteries of the corpus callosum never arise together. Based on this finding, Serizawa et al. [20] speculated that the two arteries are of the same origin as the embryonic median rostral artery [18]. The ACA is said to be azygos, i.e., not paired, if both the right and left ACA are absent and one median artery of the corpus callosum is present. The hypothalamic branch has an average of 1.8–3.2 arteries with average diameters between 0.15 and 0.23 mm [12, 20, 22]. Most of the hypothalamic branches originate from the posterior or posteroinferior aspect of the ACoA, though they sometimes arise from the subcallosal branch or the median artery of the corpus callosum. The hypothalamic branches vascularize the anterior hypothalamic area and the lamina terminalis and form anastomoses with the subcallosal branch. The chiasmatic branch is observed in only 20% of cadaver brains and has a very small diameter, measuring only 0.1 mm. It originates from the posteroinferior aspect of the ACoA and terminates at the superior surface of the optic chiasm and optic nerves. The chiasmatic area is mainly fed by the branches of the ACA [20].

4.3 Infarcts in the Territory of the Perforating Branches of the ACoA Infarcts in this territory are usually caused by the rupture of ACoA aneurysms and their surgical treatment. However, in patients with ruptured ACoA aneurysms, artifacts from surgical clips make neuroanatomical identification of lesions difficult, especially when computerized tomography (CT) scanning is involved. Recently, though, the use of nonferromagnetic clips has enabled the utilization of magnetic resonance (MR) imaging for lesion identification; although a certain degree of artifact is inevitable, there is much less with MR imaging than with CT scanning. Figure 4.3 shows MR images of a patient with infarcts in the territory of the perforating branches of the ACoA following rupture and surgical treatment of an ACoA aneurysm; the infarcted area includes the midline section of the anterior commissure, columns of the fornix, and left septal area. Severe ischemia of the bilateral hypothalamic areas is rare, probably because of the rich supply of the hypothalamic area by multiple hypothalamic branches and a large subcallosal branch that anastomose together [11, 20].

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Fig. 4.3 Series of T2-weighted magnetic resonance images of a 39-year-old man, who underwent an operation for a ruptured aneurysm of the anterior communicating artery (ACoA). The patient had mild amnesia and decreased spontaneity. These images depict an infarct in the territory of the perforating branches of the ACoA that includes the midline section of the anterior commissure, columns of the fornix, and left septal area. (a) Coronal images. (b) Sagittal images. (c) Axial images. Coronal images are vertical and axial images, parallel to the line connecting the anterior and posterior commissures. The parameters for image acquisition are: repetition time (TR), 2,500 ms; echo time (TE), 15 ms; inversion time (TI), 400 ms; slice/gap, 1 mm/0 mm; field of vision (FOV), 210 mm; flow compensation; imaging performed on Achieva 3.0-T Quasar Dual imager (PHILIPS, Best, The Netherlands)


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4.4 Structures Perfused Mainly by the Perforating Branches of the ACoA (Figs. 4.2 and 4.4) As noted, the perforating branches of the ACoA perfuse the septal area (subcallosal area and paraterminal gyrus), anterior commissure, and column of the fornix as well as the septum pellucidum, rostrum and genu of the corpus callosum, and anterior cingulate gyrus. The septal area is located on the medial surface of the cerebral hemisphere anterior to the lamina terminalis and comprises two gyri (subcallosal area and paraterminal gyrus) and two sulci (anterior and posterior parolfactory sulci). The anterior parolfactory sulcus forms the anterior border of the subcallosal area. The posterior parolfactory sulcus forms the anterior border of the paraterminal gyrus and separates it from the subcallosal area. The anterior cingulate gyrus merges with the superior aspect of the subcallosal area.

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The paraterminal gyrus extends to the inferior surface of the brain and joins the diagonal band of Broca [13]. The medial and lateral septal nuclei are subcortical gray-matter nuclei that lie under the paraterminal gyrus and project substantially to the hippocampus [14]. The diagonal band of Broca begins in the medial part of the septal area, descends through the medial surface of the cerebral hemisphere, and passes vertically in front of the anterior commissure. At the base of the hemisphere, it makes a caudal and lateral turn toward the hippocampus and amygdala. This band is a gray-and-white bridge that carries reciprocal links between the septum and substantia innominata and forms the obliquely oriented posterior-medial border of the anterior perforated substance [13, 15]. The nucleus of the diagonal band of Broca contains cholinergic neurons and maintains reciprocal links with the hippocampus [14]. The anterior commissure is a prominent fiber bundle under the internal capsule and the globus pallidus, and a small part of the pallidum lies under the anterior commissure. Bulk of the fibers of the anterior commissure connect the rostral parts of the bilateral temporal lobes to each other and bind the two olfactory bulbs together [2,15]. The fornix is a fiber bundle that connects the hippocampus with the hypothalamus and various other structures, including the septal area. It passes under the splenium of the corpus callosum and proceeds rostrally over the thalamus. The columns of the fornix curve

Fig. 4.4 Schematic drawing with a slight rotation to expose part of the inferior surface of the brain showing the position of the septal area relative to the corpus callosum, fornix, gyrus rectus, and olfactory tract (adapted from [13], with permission)


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ventrally in front of the interventricular foramen and caudal to the anterior commissure to enter the hypothalamus, where most of the fibers terminate in the mamillary body (i.e., the postcommissural fornix). Other fibers constitute a small precommissural portion of the fornix that terminates in the septal area [16]. Since the 1950s, patients who survive aneurysms of the ACoA have been known to experience amnesia similar to that of Korsakoff’s syndrome with personality changes and decreased spontaneous activity [17]. However, the lesions responsible for these symptoms are unclear because several factors affect the neurobehavioral consequences of surgery for a ruptured ACoA aneurysm and include such variables as the timing and type of surgery, injury caused by the surgery, and complications such as hydrocephalus. This uncertainty raises the possibility that some symptoms of patients with a ruptured ACoA aneurysm are attributable to diffuse brain damage rather than discrete lesions caused by infarction of the perforating branches of the ACoA. Among these symptoms, memory disturbance has been thought to be associated with infarcts of the perforating branches of the ACoA [4, 5, 8]. A recent survey reported that patients with relatively discrete lesions tend to show episodic memory disturbance of varying degree, but do not necessarily show personality changes [7]. The report also suggested the probably crucial role in episodic memory of the septal area and diagonal band of Broca, which are perfused by the subcallosal branch, but it did not exclude the possible involvement of nearby structures, such as the nucleus accumbens, anterior hypothalamus, and the columns of the fornix [7].

References 1. Avci E, Fossett D, Erdogan A, Egemen N, Attar A, Aslan M. Perforating branches of the anomalous anterior communicating complex. Clin Neurol Neurosurg. 2001;103:19–22. 2. Carpenter MB. Core text of neuroanatomy. 4th ed. Baltimore: Williams & Wilkins; 1991. 3. Crowell RM, Morawetz RB. The anterior communicating artery has significant branches. Stroke. 1977;8:272–3. 4. Damasio AR, Graff-Radford NR, Eslinger PJ, Damasio H, Kassell N. Amnesia following basal forebrain lesions. Arch Neurol. 1985;42:263–71. 5. DeLuca J, Chiaravalloti N. The neuropsychological consequences of ruptured aneurysms of the anterior communicating artery. In: Harrison EJ, Owen AM, editors. Cognitive deficits in brain disorders. London: Martin Duntz; 2002. p. 17–36. 6. Dunker RO, Harris AB. Surgical anatomy of the proximal anterior cerebral artery. J Neurosurg. 1976;44:359–67. 7. Fujii T. The basal forebrain and episodic memory. In: Huston JP, ed. Handbook of behavioral neuroscience, Vol. 18, Handbook of episodic memory, Dere E, Easton A, Nadel L, Huston JP. The Netherlands: Elsevier; 2008. p. 343–62. 8. Gade A. Amnesia after operations on aneurysms of the anterior communicating artery. Surg Neurol. 1982;18:46–9. 9. Hernesniemi J, Dashti R, Lehecka M, Niemelä M, Rinne J, Lehto H, et al. Microneurosurgical management of anterior communicating artery aneurysms. Surg Neurol. 2008;70:8–28. 10. Kakou M, Destrieux C, Velut S. Microanatomy of the pericallosal arterial complex. J Neurosurg. 2000;93:667–75. 11. Marinković SV, Milisavljević MM, Marinković ZD. Microanatomy and possible clinical significance of anastomoses among hypothalamic arteries. Stroke. 1989;20:1341–52.

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12. Marinković S, Milisavljević M, Marinković Z. Branches of the anterior communicating artery. Microsurgical anatomy. Acta Neurochir (Wien). 1990;106:78–85. 13. Mark LP, Daniels DL, Naidich TP, Hendrix LE, Maas E. Anatomic moment. The septal area. AJNR Am J Neuroradiol. 1994;15:273–6. 14. Mesulam M-M. Principles of behavioral and cognitive neurology. 2nd ed. New York: Oxford University Press; 2000. 15. Nauta WJH, Feirtag M. Fundamental neuroanatomy. New York: WH Freeman; 1986. 16. Nieuwenhuys R, Voogd J, Van Huijzen C. The human central nervous system, a synopsis and atlas. 3rd revised ed. Berlin: Springer; 1988. 17. Norlen G, Olivecrona H. The treatment of aneurysms of the circle of Willis. J Neurosurg. 1953;10:404–15. 18. Padget DH. The development of the cranial arteries in the human embryo. Contrib Embryol. 1948;32:205–61. 19. Perlmutter D, Rhoton Jr AL. Microsurgical anatomy of the anterior cerebral-anterior communicating-recurrent artery complex. J Neurosurg. 1976;45:259–72. 20. Serizawa T, Saeki N, Yamaura A. Microsurgical anatomy and clinical significance of the anterior communicating artery and its perforating branches. Neurosurgery. 1997;40:1211–8. 21. Tao X, Yu XJ, Bhattarai B, Li TH, Jin H, Wei GW, et al. Microsurgical anatomy of the anterior communicating artery complex in adult Chinese heads. Surg Neurol. 2006;65:155–61. 22. Türe U, Yaşargil MG, Krisht AF. The arteries of the corpus callosum: a microsurgical anatomy study. Neurosurgery. 1996;39:1075–85. 23. Vincentelli F, Lehman G, Caruso G, Grisoli F, Rabehanta P, Gouaze A. Extracerebral course of the perforating branches of the anterior communicating artery: microsurgical anatomical study. Surg Neurol. 1991;35:98–104. 24. Yaşargil MG, Smith RD, Young PH, Teddy PJ. Anterior cerebral artery complex. In: Yaşargil MG, ed. Microneurosurgery, Vol. 1. Stuttgart: Georg Thieme; 1984. p. 92–128.

Cerebral Arterial Variations and Anomalies Diagnosed by MR Angiography

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5.1 Introduction Variations and anomalies in cerebral arteries include persistent primitive vessels that normally regress during early gestation [31] and arteries that normally persist to adult life but regress prematurely. Selective cerebral angiographic studies report numerous such variations and anomalies. Improved MRA image quality using 3-dimensional (3D) time-offlight (TOF) technique permits incidental detection of even small anomalous arterial branches [66]. Although the variations and anomalies may have limited clinical significance, their correct diagnosis during MRA image interpretation is important to interventional neuroradiologists as well as neurosurgeons, who must be familiar with variations and anomalies in vascular anatomy as they prepare for surgery. In this chapter, I present various variations and anomalies of the extra- and intracranial arteries detected by noncontrast 3D-TOF-MRA. Most images presented were obtained using 1.5-tesla imaging units, including the Achieva 1.5-tesla Nova Dual (Philips Medical System, Einthoven, The Netherlands), and most are partial maximum-intensity-projection (MIP) images, which best demonstrate the variations and anomalies.

5.2 Variations and Anomalies of the Common Carotid Artery (CCA) and Internal Carotid Artery (ICA) 5.2.1 Brachiocephalic Trunk Origin of the Left CCA (Bovine Aortic Arch) The left CCA arises at the origin or proximal segment of the brachiocephalic trunk in approximately 10% of patients (Fig. 5.1) to share a common trunk from the aortic arch,

A. Uchino Department of Diagnostic Radiology, Saitama Medical University International Medical Center, 1397-1 Yamane, Hidaka, Saitama, 350-1298, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_5, © Springer-Verlag London Limited 2010

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Fig. 5.1 A 43-year-old man with left common carotid artery (CCA) arising from the brachiocephalic trunk, so-called “bovine aortic arch” (arrow)

variation called “bovine aortic arch.” However, this is a misnomer because the branching pattern of the aortic arch in cattle has a single brachiocephalic trunk originating from the aortic arch that eventually splits into the bilateral subclavian arteries and a bicarotid trunk [24]. In patients with this variation, catheterization to the left CCA is sometimes difficult by the transfemoral approach but relatively easy via the right transbrachial approach [39].

5.2.2 Unusual Level of Bifurcation of the CCA, Absence of the CCA and Absence of the Proximal External Carotid Artery (ECA) The CCA usually divides into the ICA and ECA at the level of the C4 vertebral body. However, bifurcation is rarely low and the main trunk of the ECA is long (Fig. 5.2), and a few cases are reported [4] in which the CCA is absent and the ICA and ECA arise separately from the brachiocephalic trunk or aortic arch (Fig. 5.3). In contrast, CCA bifurcation is congenitally high in some patients, and the main trunk of the ECA is short (Fig. 5.4). High carotid bifurcation may result from atherosclerotic elongation of the CCA in elderly patients. Carotid endoarterectomy, the main surgical treatment of the stenotic origin of the ICA, may be difficult in patients with high carotid bifurcation. Rarely, a nonbifurcating cervical carotid artery results when the main trunk of the ECA is absent [28], and the proximal branches of the ECA arise separately from the CCA (Fig. 5.5).

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Fig. 5.2 A 76-year-old woman with low right carotid bifurcation (C6 vertebral body level, arrow). The main trunk of the external carotid artery (ECA) is long

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Fig. 5.3 A 46-year-old woman with separate origins of the right internal carotid artery (ICA) and ECA. Antero-posterior (a) and left anterior oblique (b) projections show completely duplicated (absent) right CCA (arrow). (Courtesy of Dr. Zenji Ayabe and Dr. Takahashi Yamamoto)

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Fig. 5.4 An 89-year-old woman with high left carotid bifurcation at the C2/3 disc level. The main trunk of the ECA is short (arrow)

5.2.3 Medial Origin and Retropharyngeal Course of the ICA Although the ICA usually originates posterolaterally to the ECA, it arises medially in approximately 10% of patients. Bilateral ICAs that originate medially and take a retropharyngeal course are called “kissing carotids” (Fig. 5.6). Care should be taken during physical examination to avoid misdiagnosing the retropharyngeal ICA as a retropharyngeal tumor.

5.2.4 Congenital Absence or Hypoplasia of the ICA Congenital absence of the ICA is rare; reported incidence is 0.01% (Fig. 5.7) [62]. Computed tomography (CT) of the skull base with bone image or MRA source image aids differential diagnosis of acquired ICA occlusion. Absence of the carotid canal in the petrous bone is diagnosed as congenital absence [35]. In some patients with unilateral absence of the proximal ICA, an intercavernous anastomosis is observed between the bilateral ICAs (Fig. 5.8) [34]. In patients with absent proximal ICA, the persistent trigeminal artery may also be an important collateral (Fig. 5.9). Segmental agenesis of the supraclinoid ICA has also been reported [7]. Segmental agenesis of the bilateral cavernous segment of the ICAs associated with collateral circulations by the unique vasculature of the “carotid rete mirabile” network is extremely rare. The distinctive vessels of this network run between the external and internal carotid systems in lower mammals [15]. In hypoplastic ICA, which may be caused by agenesis of the distal ICA, CT reveals a narrow carotid canal (Fig. 5.10). However, adult patients with an acquired occlusion of the distal ICA during childhood may have a similarly narrow carotid canal.


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Fig. 5.5 A 48-year-old man with absent right proximal ECA that mimics high carotid bifurcation (A, C3 vertebral body level, arrow). Selective right common carotid angiogram (b) shows separately originating proximal branches of the ECA, indicating nonbifurcating cervical carotid artery. The occipital artery arises from the right vertebral artery (c) (Courtesy of Dr. Shoichiro Ishihara)

5.2.5 Aberrant Course of the ICA, Persistent Stapedial Artery The petrous segment of the ICA rarely courses in an abnormal way laterally and makes a hairpin turn. The most lateral portion is located in the middle ear cavity (Fig. 5.11) and seen as a reddish mass deep in the tympanic membrane at physical examination. This variation is probably caused by segmental agenesis of the vertical portion of the petrous ICA and collateral circulation via the inferior tympanic artery and caroticotympanic artery [49]. It is reported most commonly on the right side in females [19], but the reason for this predominance is unclear, and one case is reported of bilateral ICAs with aberrant course [1].

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Fig. 5.6 A 68-year-old man with ICAs of bilateral medial origin and “kissing carotids” (arrow)

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Fig. 5.7 A 79-year-old woman with congenital absence of right ICA (a) The right carotid canal is absent on the magnetic resonance angiographic (MRA) source image (b, arrow)

Persistent stapedial artery - which occurs when the middle meningeal artery arises from the petrous ICA (Fig. 5.12) - is extremely rare, with a histologic incidence of 2 in 1,400 specimens; some arise from the aberrant course of the ICA [73]. Embryologically, the primitive second aortic arch gives rise to the hyoid artery, which gives rise to the stapedial artery near its origin from the internal carotid in the fourth or fifth week of the fetus. When a stapedial artery persists in postnatal life, the foramen spinosum is absent because it gives rise to the middle meningeal artery [73].

5 Cerebral Arterial Variations and Anomalies Diagnosed by MR Angiography Fig. 5.8 A 61-year-old man with congenital absence of proximal right ICA with an intercavernous anastomosis. Antero-posterior (a) and caudo-cranial (b) projections show absent proximal right ICA and a large connecting vessel between the cavernous ICAs (arrows). This anomalous vessel penetrates the sella on the MRA source image (c, arrow)

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Fig. 5.9 A 26-year-old woman with congenital absence of proximal right ICA with collateral circulations via the ipsilateral ECA and persistent trigeminal artery. Antero-posterior projection (a) shows absent proximal right ICA with tortuous collaterals via the ECA (arrow). Lateral projections (b) show large persistent right trigeminal artery (arrow). (Courtesy of Dr. Hideki Sato)

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Fig. 5.10 A 50-year-old man with hypoplastic right ICA (a, arrow). The right carotid canal is extremely narrow on CT (b, arrow)


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Fig. 5.11 A 52-year-old woman with aberrant course of the right ICA (a, arrow). The carotid artery is seen in the middle ear cavity on computed tomography (CT) (b, arrow). (Reprint with permission from [19], Courtesy of Dr. Takao Kodama)

Fig. 5.12 A 2-year-old girl with persistent right stapedial artery (reprint with permission from [73])

5.2.6 Fenestration of the ICA Fusion error during the early embryonic period causes arterial fenestration which is most frequently observed in the vertebrobasilar arterial system. Cerebral fenestrations are seen relatively frequently in patients with cerebral aneurysm or cerebral arteriovenous malformation [38, 54]. ICA fenestration is extremely rare and usually seen at the supraclinoid segment as a small slit-like configuration (Fig. 5.13). It is also rarely seen at the cervical segment and is generally large. Fenestration should be differentiated from arterial dissection, a much more common acquired abnormality of the cervical ICA [11]. Only one case

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Fig. 5.13 A 37-year-old woman with left supraclinoid carotid fenestration (arrow)

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Fig. 5.14 A 71-year-old man with left cavernous carotid fenestration (a, arrow). (Reprint with permission from [52]) selective left internal carotid angiogram clearly shows fenestration (b, arrow). (Reprint from [60] with acknowledgement)

each of intracavernous ICA fenestration (Fig. 5.14) [60] and multichannel fenestrations of the petrous segment of the ICA detected by angiography is reported [26].

5.2.7 Persistent Dorsal Ophthalmic Artery Rarely, the ophthalmic artery arises from the cavernous segment of the ICA and enters into the orbit via the superior orbital fissure (Fig. 5.15). In early gestation, there are ventral and


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Fig. 5.15 A 56-year-old woman with right persistent dorsal ophthalmic artery. The right ophthalmic artery arises from the cavernous ICA (a, arrow) and enters the orbit via the superior orbital fissure (b, arrow)

dorsal ophthalmic arteries. Normally, only the ventral artery persists, arising from the supraclinoid segment of the ICA and entering the orbit via the optic canal. Thus, this anomalous artery is regarded as a persistent dorsal ophthalmic artery. Double ophthalmic arteries are rarely seen angiographically [29].

5.3 Variations and Anomalies of the Anterior Cerebral Artery (ACA) and Anterior Communicating Artery 5.3.1 Carotid-ACA Anastomosis The ACA rarely arises from the ICA at the level of the ophthalmic artery, courses superiorly between the bilateral optic nerves, and then anastomoses with the junction of the anterior communicating artery and the A2 segment (Fig. 5.16). This anomaly has been variously termed carotid-ACA anastomosis, infraoptic course of the ACA, interoptic course of the ACA, and preoptic origin of the ACA. However, because some patients have an ipsilateral A1 segment (Fig. 5.17), this anomalous artery is not a part of the ACA. Thus, the term “carotid-ACA anastomosis” seems most suitable. There is right-sided predominance, but the reason for this is unknown [64]. Few cases of bilateral carotid-ACA anastomoses have been reported (Fig. 5.18). If an ipsilateral normal A1 segment is present and the contralateral A1 is absent, this anastomotic artery may function as an anomalously originated contralateral A1 segment [3].

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Fig. 5.16 A 68-year-old woman with right carotid-anterior cerebral artery (ACA) anastomosis (a) The anomalous artery arises from the right supraclinoid ICA at the level of the ophthalmic artery (arrow). MRA source image shows the anomalous artery ascending in the interoptic space (b, arrow)

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Fig. 5.17 A 73-year-old man with right carotid-ACA anastomosis. Antero-posterior projection (a) and the MRA source image (b) show ipsilateral normal A1 segment (arrows)

5.3.2 Fenestration of the ACA and the Anterior Communicating Artery ACA fenestrations are relatively common, and most frequently observed at the distal A1 segment (Fig. 5.19). Reported MRA incidence is 1.2%, higher than conventional angiographic incidence [18], because the two fenestrated branches usually divide horizontally, the vessels are superimposed on antero-posterior projection, and can be adequately


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Fig. 5.18 A 75-year-old man with bilateral carotid-ACA anastomoses (a) The anomalous arteries ascend in the interoptic space (b, arrows)

Fig. 5.19 A 76-year-old man with left distal A1 fenestration (arrow)

observed on caudo-cranial projection [61]. Fenestrations are also observed at the proximal A2 segment (Fig. 5.20). It is well known that the anterior communicating artery is frequently duplicated or fenestrated during surgery or on autopsy, and 3D digital subtraction angiography (DSA) is useful for its diagnosis [8, 30]. However, because this vessel is small and blood flow in the vessel may be slow, variations of the anterior communicating artery can rarely be identified on MRA (Fig. 5.21).

5.3.3 Persistent Primitive Olfactory Artery The A1 segment of the ACA seldom takes an extremely anteroinferior course and makes a hairpin turn to connect posterosuperiorly to the A2 segment (Fig. 5.22). This anomalous

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Fig. 5.20 A 50-year-old man with left proximal A2 fenestration (arrow)

Fig. 5.21 A 75-year-old woman with anterior communicating artery fenestration (arrow)

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Fig. 5.22 A 70-year-old man with bilateral persistent olfactory arteries. In the lateral projection (a), the bilateral proximal ACAs course antero-inferiorly and make hairpin turns to course posterosuperiorly (arrow). In the caudo-cranial projection (b), the bilateral proximal ACAs are separated, and there is no anterior communicating artery (arrows)


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Fig. 5.23 A 66-year-old woman with azygos (unpaired) ACA. The A2 segment is single (arrow)

artery is formed when the primitive olfactory artery [67], which usually regresses during early gestation, persists and then remains as the recurrent artery of Heubner. Thus, an ipsilateral recurrent artery of Heubner is not seen in patients with a persistent primitive olfactory artery. This anomalous artery can be unilateral or bilateral, and aneurysm may occur at its hairpin turn [51].

5.3.4 Azygos ACA, Bihemispheric ACA A completely fused A2 segment is called an azygos or unpaired ACA (Fig. 5.23); reported MRA incidence is 2.0% [61]. Because the anterior communicating artery is absent in these patients, aneurysm is not seen at the A1–A2 junction, but frequently occurs at the A2–A3 junction, probably from hemodynamic stress [6, 14]. Bihemispheric ACA refers to the presence of asymmetric A2 segments in which the hyperplastic side of A2 supplies the bilateral cerebral hemispheres. This variation is frequent and should not be confused with azygos ACA.

5.3.5 Triple ACAs, Median Artery of the Corpus Callosum “Median artery of the corpus callosum” is the name given to an anomalous branch arising from the anterior communicating artery. The ACA of these patients has a third A2 segment (Fig. 5.24). Reported MRA incidence of triple ACAs is 3.0% [61].

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Fig. 5.24 A 69-year-old man with triple ACA (median artery of the corpus callosum). The A2 segment is triplicated (arrow)

5.4 Variations and Anomalies of the Middle Cerebral Artery (MCA) Figure 5.25 illustrates the several MCA variations.

5.4.1 Duplicated MCA Duplicated MCA is a smaller artery that arises directly from the ICA just proximal to the carotid bifurcation and usually supplies the anterior temporal lobe [20, 50] (Fig. 5.26). Reported MRA incidence is 2.1% [55]. Aneurysm may be seen at the origin of the duplicated MCA [46].

5.4.2 Accessory MCA An accessory MCA is a small artery originating from the ACA; reported MRA incidence is 1.2% [55]. There are 2 types, one arising from the proximal (Fig. 5.27) and the other from the distal portion of the A1 segment (Fig. 5.28). The former should be differentiated from a duplicated MCA. The carotid bifurcation is the junction of the ICA, the larger 3 2 1

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Fig. 5.25 Schematic illustration of several types of middle cerebral artery (MCA) variation. 1 Duplicated MCA; 2 Early bifurcated MCA; 3 Distal A1 origin of accessory MCA; 4 Proximal A1 origin of accessory MCA; 5 Fenestration of MCA

5 Cerebral Arterial Variations and Anomalies Diagnosed by MR Angiography Fig. 5.26 A 60-year-old woman with left duplicated MCA (arrow). (Image obtained using a 3-tesla scanner, Courtesy of Dr. Chihiro Suzuki)

Fig. 5.27 A 77-year-old woman with left accessory MCA arising from the proximal A1 (arrow). (Image obtained using a 3-tesla scanner, Courtesy of Dr. Chihiro Suzuki)

Fig. 5.28 A 72-year-old man with right accessory MCA arising from the distal A1 (arrow)

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(main) MCA, and the ACA [20]. If there are two equally sized MCA branches, it is difficult to distinguish an accessory MCA from a duplicated MCA. An accessory MCA arising from the distal portion of the A1 segment is relatively rare and should be differentiated from the recurrent artery of Heubner. An accessory MCA is larger than the recurrent artery of Heubner and supplies the anterior frontal lobe [44]. The accessory MCA may provide collateral blood supply in a patient with occlusion of the main MCA [21].

5.4.3 Early Bifurcated MCA Bifurcation of the MCA within one centimeter of its origin is called “early bifurcation” [50] and frequently observed; the inferior small branch usually supplies the temporal lobe just as in the case of a duplicated MCA (Fig. 5.29).

5.4.4 Fenestration of the MCA A small slit-like fenestration is rarely detected at the proximal M1 segment that frequently gives rise to the temporopolar artery [10]. Antero-posterior projection usually shows this fenestration well (Fig. 5.30). Reported MRA incidence is 0.15% [70], lower than conventional angiographic incidence of 0.26% [16]. Fenestration of the M2 segment is extremely rare (Fig. 5.31).

5.5 Variations and Anomalies of the Posterior Cerebral Artery (PCA) 5.5.1 Duplicated PCA PCA duplication is rarer than MCA duplication. The temporal and parietooccipital branches rarely originate separately from the posterior communicating artery or P1-P2 junction (Fig. 5.32) [52].

Fig. 5.29 A 21-year-old man with right early bifurcated MCA (arrow)


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Fig. 5.30 A 23-year-old woman with left proximal M1 fenestration (arrow) and small temporal branch arising from the fenestrated segment

Fig. 5.31 A 73-year-old man with left M2 fenestration. The proximal segment of the M2 has a small slit-like fenestration (arrow)

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Fig. 5.32 A 56-year-old woman with right duplicated posterior cerebral artery (PCA). The right PCA is of fetal origin and completely duplicated (a, b, arrows). (Reprint with permission from [52])

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5.5.2 PCA Branch Arising from the Hyperplastic Anterior Choroidal Artery A branch of the PCA sometimes originates from the anterior choroidal artery [45], in which case, the proximal anterior choroidal artery is extremely large, mimicking the duplication of the posterior communicating artery (Fig. 5.33). This variation has four types, the (1) hypertrophic uncal branch, (2) anomalous temporal artery, (3) anomalous occipitoparietal artery, and (4) anomalous temporooccipitoparietal artery [44].

5.5.3 Fenestration of the PCA On MRA, PCA fenestration, seen at the P1 segment (Fig. 5.34), is extremely rare, but reported incidence of a duplicated P1 segment on anatomical study is 0.25% [5]. MRA

Fig. 5.33 A 24-year-old man with left hyperplastic anterior choroidal artery from which a branch of the left PCA arises (arrow)

Fig. 5.34 A 13-year-old boy with left P1 fenestration (arrow)


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detection may be difficult because the P1 is a short segment and may be superimposed with anterior circulation on antero-posterior projection.

5.6 Variations of the Circle of Willis At autopsy, only 21–52% of patients have a completely formed circle of Willis [23].

5.6.1 Unilateral Absence of A1 Segment The diameter of the A1 segment of the ACA is grossly asymmetric, and unilateral A1 is frequently absent; reported MRA incidence is 5.6% [61]. In patients with unilateral A1 absence, increased hemodynamic stress frequently causes aneurysm at the junction of the hyperplastic contralateral A1 and the anterior communicating artery (Fig. 5.35). Thromboembolic infarction of the ACA territories is relatively frequent in such cases because the contralateral A1 is large, with a diameter as large as the M1 segment of the MCA [71]. Because the area of blood supply is narrower, the diameter of the ICA is usually smaller on the side of the A1 absence than on the contralateral ICA.

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Fig. 5.35 A 67-year-old woman with aplasia of the left A1 and bilateral PCAs of fetal origin. Anteroposterior (a) and caudocranial (b) projections show aneurysm at the junction of the right ACA and anterior communicating artery (arrow). The vertebrobasilar arteries are hypoplastic from aplasia of the bilateral P1

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5.6.2 Unilateral or Bilateral Absence of P1 Segment The P1 segment of the PCA is frequently absent unilaterally or bilaterally, and the ipsilateral PCA arises directly from the ICA; reported MRA incidence is 4.0% [23]. This is called fetal type or fetal origin of PCA because it is normally seen during the early fetal stage. Patients with bilateral P1 absence usually have hypoplastic vertebrobasilar arteries.

5.6.3 Unilateral or Bilateral Absence of the Posterior Communicating Artery An MRA study reported approximately 10% of patients with no connection between the ICA and PCA unilaterally or bilaterally [23]. However, MRA may not detect a slowly flowing tiny posterior communicating artery, and acquired occlusion may be confused with this variation.

5.7 Variations and Anomalies of the Vertebrobasilar and Cerebellar Arteries 5.7.1 Variations of the Origin of the Vertebral Artery (VA) The left VA frequently arises directly from the aortic arch (Fig. 5.36), with an incidence of approximately 5%, and sometimes arises from the origin of the left subclavian artery. The aortic origin of the left VA should not be misdiagnosed during catheter angiography as occlusion of the left VA. Dual (duplicated) origin of the VA is seldom seen (Fig. 5.37) [41].

Fig. 5.36 A 61-year-old man with left vertebral artery (VA) arising from the aorta between the left CCA and left subclavian artery (arrow)


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Fig. 5.37 A 76-year-old woman with left VA of duplicated origin (arrow). Image quality of the duplication is insufficient because of slow flow from a stenotic lesion at the proximal left subclavian artery. (Obtained using a 3-tesla scanner)

5.7.2 Anterior Course of the Proximal VA Although the VA usually enters the transverse foramen of the sixth cervical spine, it enters the other transverse foramina in approximately 10% of cases. In patients in whom the VA enters the fifth or fourth transverse foramen, the proximal VA takes an anterior course (Fig. 5.38).

5.7.3 Fenestration of the Extracranial VA, Persistent First Cervical Intersegmental Artery VA fenestrations are seen relatively frequently at both the extra- and intracranial segments, with extracranial fenestrations forming exclusively at the atlantoaxial portion (Fig. 5.39). Reported selective catheter angiographic incidence is approximately 2% [22]. This anomaly is caused by persistence of the distal segment of the first cervical intersegmental

220 Fig. 5.38 A 14-year-old girl with anterior course of the proximal right VA (a, arrow). The right VA is not seen in the right transverse foramen of the C5 vertebra on the axial MRA source image (b, arrow)

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artery. If the normal branch of the fenestrated segment is absent, the VA has an anomalous course, lateral to the C1/2 disk level, and is called a persistent first cervical intersegmental artery (Fig. 5.40). This anomalous VA is frequently seen in patients with Down syndrome [72].


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Fig. 5.39 A 64-year-old man with fenestration of the right extracranial VA at the atlantoaxial level. The lower branch is the persistent first cervical intersegmental artery (arrow)

5.7.4 Cervical Origin of the Posterior Inferior Cerebellar Artery (PICA) The PICA sometimes arises extracranially, originating at the level of C1 or C2. At the C2 level, the PICA arises from the persistent first cervical intersegmental artery (Fig. 5.41); at the C1 level, the PICA arises at the craniocervical junction (Fig. 5.42). This should not be confused with the posterior meningeal artery, which frequently arises from the VA at the level of the craniocervical junction.

5.7.5 Fenestrations of the Intracranial Vertebrobasilar Arteries Fenestrations are frequently seen at the terminal segment of the VA (Fig. 5.43) and the region of the vertebrobasilar junction (Fig. 5.44); they are usually large with lens-like configuration. Basilar artery (BA) fenestrations are also frequently observed at the proximal

222 Fig. 5.40 A 62-year-old man with left persistent first cervical intersegmental artery. Normal VA branch, seen in the case of fenestration, is absent (a, arrow). Lateral projection of CT angiography shows anomalous artery entering the spinal canal at the level of C1/2 (b, arrow)

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5 Cerebral Arterial Variations and Anomalies Diagnosed by MR Angiography Fig. 5.41 A 66-year-old woman with right posterior inferior cerebellar artery (PICA) of cervical origin (C2, arrow) that arises from a persistent first cervical intersegmental artery

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Fig. 5.42 A 49-year-old woman with right PICA of C1 origin (a, b, arrows)

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Fig. 5.43 A 71-year-old man with fenestration of the intracranial large left VA. PICA originating from the C1 level (long arrow) anastomoses with the distal VA (short arrow)

Fig. 5.44 A 61-year-old man with fenestration of the vertebrobasilar junction (arrow)

segment [43] and usually have a small slit-like shape (Fig. 5.45); reported MRA incidence is 2% [57]. This small fenestration mimics an aneurysmal ectasia and is sometimes accompanied by aneurysm [47]. Fenestrations are also seen at the mid and distal segments of the BA (Fig. 5.46). Though extremely rare, total duplication of the BA has been reported [63] (Fig. 5.47). Double fenestrations are also rarely seen horizontally (Fig. 5.48) or longitudinally (Fig. 5.49). BA fenestrations are caused by fusion error of the longitudinal neural arteries during early gestation. The BA is formed from the distal-to-proximal segment, which may be why BA fenestrations are prevalent at the proximal segment.


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Fig. 5.45 A 24-year-old woman with fenestration of the proximal basilar artery (BA) (arrow). The right PICA is hyperplastic

Fig. 5.46 A 55-year-old woman with fenestration of the distal BA (arrow)

5.7.6 Variations and Anomalies of the Cerebellar Arteries The anterior inferior cerebellar artery (AICA) and the ipsilateral PICA are complementary. Frequently, one vessel is not visualized, and if one vessel is hypoplastic, the other is hyperplastic. The bilateral PICAs are also complementary in size. The hyperplastic PICA frequently supplies the posteroinferior portions of the bilateral cerebellar hemispheres. The peripheries of the AICA and PICA occasionally fuse and form a large fenestration [65]. As mentioned, the PICA sometimes arises from the extracranial VA. The superior cerebellar artery (SCA) also shows variation; reported MRA incidence of duplicated SCA is 10% [69] (Fig. 5.50). If the SCA arises from the proximal PCA, the two form a common trunk (Fig. 5.51). Fenestration of the SCA is rare (Fig. 5.52). Extremely tortuous SCA has also been reported [53].

226 Fig. 5.47 A 3-month-old-girl with completely duplicated BA (a, arrow). T1-weighted coronal image also shows BA duplication (b, arrow). Patient also has cleft palate, nasopharyngeal teratoma, and pituitary duplication. (Reprint from [63] with acknowledgement)

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5.8 Carotid-Vertebrobasilar Anastomoses There are four pairs of presegmental arteries during the early embryonic period; proatlantal, hypoglossal, otic, and trigeminal arteries [31]. These anastomoses may persist in adult life and have an overall incidence of 1.0% [25]. Figure 5.53 illustrates the locations and courses of these persistent anastomoses.


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Fig. 5.48 A 45-year-old man with horizontal double fenestrations of the BA (a, b arrows)

Fig. 5.49 A 68-year-old man with longitudinal double fenestrations of the BA (arrows)

Fig. 5.50 A 67-year-old man with left duplicated superior cerebellar artery (SCA) (arrow). (Image obtained using a 3-tesla scanner, Courtesy of Dr. Chihiro Suzuki)

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Fig. 5.51 A 75-year-old man with left SCA arising from the PCA to share a common trunk (arrow)

Fig. 5.52 A 52-year-old man with fenestration of the left SCA (arrow). (Courtesy of Dr. Masatoshi Ito)

5.8.1 Proatlantal Artery Type 1 and Type 2 Type 1 proatlantal artery is an extremely rare anastomosis between the proximal cervical ICA and the extracranial VA [12] (Fig. 5.54).Type 2 proatlantal artery is also an extremely rare anastomosis between the proximal ECA and the extracranial VA (Fig. 5.55). Type 1 is caused by persistence of the proatlantal artery and its course - more anteromedial than that of type 2 - traverses along the anterior aspect of the vertebral bodies to the level of the occipito-atlantal space and enters the foramen magnum to anastomose the VA. Type 2 is caused by persistence of the first cervical intersegmental artery and ascends lateral to the C1 or C2 vertebra obliquely and enters the foramen magnum to anastomose the VA [25]. In patients with congenital gradient in blood pressure between the ECA and

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5 Cerebral Arterial Variations and Anomalies Diagnosed by MR Angiography Fig. 5.53 Schematic illustration of several types of carotidvertebrobasilar anastomoses. 1 Proatlantal artery type 1; 2 Proatlantal artery type 2; 3 Persistent hypoglossal artery; 4 Persistent otic artery ?; 5 Persistent trigeminal artery (PTA); 6 Cerebellar artery arising from the PTA; 7 PTA variant (cerebellar artery arising from the ICA)

7 5

6 4

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2 1

Fig. 5.54 A 55-year-old man with bilateral persistent proatlantal artery type 1 (arrows, right; arrowhead, left) (Reprint with permission from [12])

VA, as seen with proximal VA hypoplasia, collateral circulation from the occipital artery to the distal VA may develop in the form of a type 2 proatlantal artery [33]. Thus, in a patient with a type 2 proatlantal artery, the unilateral VA is usually hypoplastic. In such a case of acquired proximal VA occlusion, acquired collateral circulation to the VA via the occipital artery should not be confused with this rare anomaly. The occipital artery rarely arises from the proximal ICA (Fig. 5.56) and may be a variant of the type 1 proatlantal artery [42], or represent the absence of the main trunk of the ECA.

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Fig. 5.55 An 83-year-old man with left proatlantal artery type 2. Antero-posterior (a) and lateral (b) projections of partial maximum-intensity-projection (MIP) image show large anastomosis between the left occipital artery and the left VA (arrows). The proximal left VA cannot be identified. The right VA is also hypoplastic, and its terminal segment is absent. The lateral-type left persistent trigeminal artery (PTA) is also seen (arrowheads)

5.8.2 Persistent Hypoglossal Artery (PHA) The PHA is the second most common type of carotid-vertebrobasilar anastomoses; incidence is estimated at 0.027–0.26% [13]. It anastomoses between the cervical ICA and the lower portion of the BA via the hypoglossal canal (Fig. 5.57). The presence of an anomalous artery in the hypoglossal canal is an important finding in MRA or CT diagnosis of the PHA [9]. The ipsilateral VA is usually hypoplastic. A PICA fed only by this anomalous artery without connection to the VA is regarded as a PHA variant [49].

5.8.3 Persistent Otic Artery? If it exists, a persistent otic artery should (1) arise in the lateral portion of the petrous canal, (2) run through the internal auditory canal, and (3) join the BA at a caudal point [2]. The


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Fig. 5.56 A 78-year-old man with right occipital artery arising from the ICA. Antero-posterior (a) and left posterior oblique (b) projections of partial MIP image show occipital artery originating anomalously from the ICA (arrows). This occipital artery may be a variant of proatlantal artery type 1 or represent an absent proximal ECA (nonbifurcating cervical carotid artery)

artery’s existence is unclear because previous angiographic studies report the low-lying trigeminal arteries as a persistent otic artery [32, 36].

5.8.4 Persistent Trigeminal Artery (PTA), Lateral Type The PTA is the most frequent carotid-vertebrobasilar anastomosis. It arises from the precavernous or cavernous ICA and anastomoses to the mid portion of the BA. As mentioned, it can arise more proximally, mimicking a persistent otic artery. Reported MRA incidence is approximately 1% [59]. Figure 5.58 illustrates the several types of PTA. According to its course from the ICA to the BA, there are lateral and medial types. The two types can be distinguished by caudo-cranial projection but not by conventional angiography, which is usually taken with antero-posterior and lateral projections. Lateral is more common than medial PTA and runs posteriorly parallel to the trigeminal nerve (Fig. 5.59). PTA is also classified as Saltzman type 1 when the ipsilateral posterior communicating artery is absent. In Saltzman type 2, the ipsilateral P1 segment is absent [66]. The cerebellar artery seldom arises from the lateral-type PTA [68] (Fig. 5.60). If there is a large PTA, the proximal BA and bilateral VAs are usually hypoplastic, because the ICA supplies a large amount of blood via the PTA. The PTA is quite frequently associated with other cerebrovascular disease, such as arteriovenous malformation [58].

232 Fig. 5.57 A 69-year-old man with left persistent hypoglossal artery (PHA) (a, arrow). MRA source image shows this artery in the hypoglossal canal (b, arrow)

A. Uchino

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Fig. 5.58 Schematic illustration of several types of persistent trigeminal artery (PTA) (caudo-cranial projection). 1 Lateral type, Salzman type 2 (ipsilateral P1 hypoplasia); 2 Medial type, Salzman type 1 (ipsilateral posterior communicating artery hypoplasia); 3 PTA variant (cerebellar artery arising from the ICA); 4 Cerebellar artery arising from the lateral type PTA

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3

5 Cerebral Arterial Variations and Anomalies Diagnosed by MR Angiography Fig. 5.59 A 41-year-old woman with right lateral-type PTA (a, arrow). Caudo-cranial (a) and lateral (b) projections show no ipsilateral posterior communicating artery (Saltzman type 1). Vertebrobasilar arteries are hypoplastic. MRA source image shows this artery running lateral to the dorsum sellae (c, arrow)

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Fig. 5.60 (a, b, stereoscopic projection) A 63-year-old man with left lateral-type PTA from which the left SCA arises (arrow)

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Fig. 5.61 A 35-year-old man with left medial-type PTA (a, arrow). There is no ipsilateral P1 segment (Saltzman type 2), and vertebrobasilar arteries are hypoplastic (b) MRA source image shows this artery penetrating the dorsum sellae (c, arrow)

5.8.5 PTA, Medial Type Medial-type PTA arises from the ICA, courses medially, and enters the sella, then turns posteriorly and penetrates the dorsum sellae (Fig. 5.61). Thus, it is called intrasellar [37] or transhypophyseal PTA [27]. In patients with this type of PTA, trans-sphenoidal pituitary surgery is dangerous.

5.8.6 PTA Variants Cerebellar arteries originating from the precavernous or cavernous ICA without connection to the BA are regarded as PTA variants [17, 48]; reported MRA incidence is 0.76% [56]. Because they are small vessels, some may not be detected by MRA; reported selective cerebral angiographic incidence of PTA variants is 0.18% [40]. Among the variants, AICA is


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Fig. 5.62 A 16-year-old girl with right PTA variant (AICA type). The right AICA arises from the ICA without connection to the BA (arrows)

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Fig. 5.63 A 35-year-old man with left PTA variant (PICA type). The anomalous artery cannot be identified as a PICA on MRA (a), but selective left internal carotid angiography clearly demonstrates the artery to be a PICA (b, arrow)

more frequent than SCA or PICA, probably because of the short distance from the PTA to the AICA (Fig. 5.62). In the case of the PTA variant of the PICA, cranio-caudal flow may prevent MRA identification (Fig. 5.63). As mentioned, a cerebellar artery rarely arises from the lateral-type PTA. This rare type of PTA may be misdiagnosed as a PTA variant if stagnant flow in the distal part of the PTA prevents detection of the distal part by MRA (Fig. 5.64). The author thanks Junji Tanaka, MD and Yasuo Sakurai, RT for their assistance in the preparation of MR angiographic images.

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Fig. 5.64 A 78-year-old woman with left PTA that mimics a PTA variant (SCA type) on MRA (a) Selective left internal carotid angiography (b) shows the left SCA arising from the PTA (arrow indicates BA)

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Regional MR Perfusion Topographic Map of the Brain Using Arterial Spin Labeling at 3 Tesla

6

Shuichi Higano and Takaki Murata

6.1 Introduction Arterial spin labeling (ASL) is a noninvasive magnetic resonance (MR) perfusion imaging technique that utilizes magnetically labeled blood as an intrinsic tracer [1, 11, 12]. ASL permits quantitative measurement of cerebral perfusion, [8, 9] and because it requires neither injection of contrast medium nor radiation exposure, the technique allows repetitive acquisitions with independent labeling of the different cerebral arteries to image regional perfusion and thereby provide topographic perfusion maps of each vascular territory[3, 5, 7, 10]. Because regional perfusion imaging (RPI) permits direct evaluation of the topographic distribution of each cerebral artery, it is useful in investigating the many anatomical variations in the circle of Willis in normal subjects and the various types of collateral circulation that may develop via leptomeningeal anastomosis, the circle of Willis, or the external carotid artery in patients with occlusive disease of the cerebral arteries [2, 5, 6, 10]. We briefly review the basic principles of ASL, describe how to create regional perfusion maps, discuss the various patterns of RPI, and compare the technique with magnetic resonance angiography (MRA).

6.2 Basic Principles of ASL and Regional Perfusion Imaging 6.2.1 Basic Principles of ASL ASL relies on the detection of magnetically labeled water protons [1, 12]. The magnetization of inflowing arterial blood is inverted, or labeled upstream of slices for scanning, and

S. Higano (*) Department of Diagnostic Radiology, Tohoku University Graduate School of Medicine, Sendai, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_6, © Springer-Verlag London Limited 2010

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242 Fig. 6.1 Two different arterial spin labeling (ASL) methods, pulsed (PASL) and continuous ASL (CASL). (a) PASL: the magnetization of spins in arterial blood is labeled with a large slab proximal to the imaging planes using a single short (a few milliseconds’ duration) radiofrequency (RF) pulse. (b) CASL: the RF field is applied continuously (for a few seconds) at the level of a plane (labeling slab) through which arterial blood flows. Simultaneously, the field gradient is applied along the artery. As spins in the blood travel through the labeling slab, the magnetization of the spin is successively inverted

S. Higano and T. Murata

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when the inverted spin of the labeled blood reaches the capillaries of the brain tissues, the magnetization of the labeled blood exchanges with that in the capillaries, which prolongs longitudinal magnetization (T1-elongation). Thus, the signal intensity of the tissues reduces in relation to tissue perfusion. Two major techniques, pulsed ASL (PASL) and continuous ASL (CASL), are proposed to invert or label spins: pulsed and continuous methods (Fig. 6.1) [1, 12]. The PASL method employs a short (a few milliseconds’ duration) radiofrequency (RF) pulse to invert the magnetization of the blood in a large volume (slab) (Fig. 6.1a). The CASL method utilizes a continuous RF field for a few seconds to magnetize the blood as it flows through the labeling slab (Fig. 6.1b). Although the longer exposure to the RF pulse with the CASL technique would increase the signal-to-noise ratio (SNR), the PASL method is usually applied at 3 tesla (T) because of the larger specific absorption rate with CASL.

6 Regional MR Perfusion Topographic Map of the Brain Using Arterial Spin Labeling at 3 Tesla

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Fig. 6.2 Principle of the arterial spin labeling (ASL) method. The pulsed ASL method is depicted for demonstration. Two sets of images are acquired, a control set of images without labeling pulse but with signal from the brain parenchyma and a set of labeling images in which water protons are inverted proximally to the imaging planes. The inverted spins that run into the imaging planes related to the blood flow reduce the signal of the labeling image. Subtraction of these two images provides a map of the distribution of the labeled water, which reflects the cerebral blood flow

The decrease in signal induced by labeled blood is very subtle, as low as 1%, and extraction of such subtle signal change requires acquisition of two sets of images−a set of labeling images in which arterial spins are inverted proximally to imaging slices and a set of control images acquired without labeling pulse (Fig. 6.2). ASL perfusion images are obtained by subtracting labeling images from control images [11, 12]. The subtracted images are related to cerebral blood flow.

6.2.2 Regional Perfusion Imaging All other perfusion imaging techniques, including positron emission tomography (PET), single photon emission tomography (SPECT), computed tomographic (CT) perfusion, and MR perfusion using contrast media, provide perfusion maps that reflect all the cerebral arterial territories as a whole. However, because ASL allows repetitive image acquisition without the use of extrinsic tracers (e.g., contrast media), RPI can be performed after separate labeling of each of the three major cerebral arteries, the bilateral internal carotid arteries (ICA), and the vertebro-basilar arteries or posterior circulation, to map individual perfusion territories (Fig. 6.3) [2]. Color-coding the RPI images obtained for each cerebral

244 Fig. 6.3 Two methods of regional perfusion imaging (RPI). (a) Original method: the right internal carotid artery (RICA), left internal carotid artery (LICA), and vertebral arteries (VA) or posterior circulation (POST) are independently labeled to generate perfusion images of each arterial distribution. (b) Dual-vessel labeling method, which contains combined arterial territories of the RICA or LICA and POST (RP, LP). Because the posterior circulation is labeled identically in both arterial spin labeling (ASL) acquisitions, each territory can be calculated as: POST = (LP + RP − |LP − RP|)/2; LICA = LP − POST; RICA = RP − POST


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artery, e.g., red (R) for the right ICA, green (G) for the left ICA, and blue (B) for the posterior circulation, and then combining the images produces RGB-encoded topographic perfusion maps that demonstrate the individual perfusion of each arterial territory. In addition, repetitive acquisition with a certain specific interval after labeling produces images that demonstrate the dynamic sequential change in perfusion [4]. The original RPI method requires independent labeling of the three arteries and 9–12 min for imaging (Fig. 6.3a). Zimine et al. proposed another labeling scheme that would permit simultaneous labeling of the ICA and posterior circulation (dual-vessel labeling method, Fig. 6.3b) [13]. Acquisition of two scans instead of the three required in


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the original method shortens imaging time by two-third. They verified this approach by comparing the original technique with their modified methods in seven healthy volunteers.

6.3 Regional Perfusion Topographic Images in Normal and Pathological Cases The developmental pattern of the circle of Willis varies from person to person. Using the RPI technique of the ASL method, Van Laar et al. investigated the variability in perfusion territories of the major feeding arteries in 115 subjects and found good correlation between perfusion pattern and anatomical variation of the circle of Willis [10]. Images from RPI noninvasively demonstrate hemodynamic change in the territory of perfusion in cases with major arterial occlusive disease and after bypass surgery or endoarterectomy [2, 6]. Figures 6.4–6.8 illustrate five representative cases, including two normal subjects and three with arterial disease. All imaging was performed using a 3-T MR unit (Intera Achieva 3.0 T Quasar Dual; Philips Medical System, Best, The Netherlands) with a 16-element phased-array neurovascular coil. The RPI images were obtained by a dual-vessel labeling method using the following parameters: pulsed star labeling of arterial regions (PULSAR) sequence [3]; repetition time/echo time/flip angle (TR/TE/FA), 4,000 ms/22 ms/35°; 40-ms delay time (TI) with every 300-ms repetitive acquisition; matrix, 64 × 64; 7-mm slice thickness; SENSE factor, 2.5; field of vision (FOV), 240 mm2; labeling slab, 30–50 mm; number of averaging, 88 (44 × 2). Case 1 is a healthy 30-year-old male volunteer (Fig. 6.4). MRA shows the horizontal segments (A1) of the bilateral anterior cerebral arteries (ACA) to be well delineated and almost equal in size, but the bilateral posterior communicating arteries (PCoA) are not so well developed (Fig. 6.4a). The anatomical pattern of the circle of Willis suggests that the territories of the middle cerebral artery (MCA) and ACA of each cerebral hemisphere should be fed by the ipsilateral ICA, and the territory of the posterior cerebral artery (PCA), by the vertebro-basilar artery. The color-coded RPI images confirm this expected perfusion pattern (Fig. 6.4c). Case 2 is a 29-year-old healthy male volunteer whose MRA shows a hypoplastic right A1 segment (Fig. 6.5). RPI reveals that the right ACA territory is fed by the contralateral (left) ICA. Case 3 (Fig. 6.6) is a 60-year-old man with severe stenosis of the left MCA who showed no neurological symptom. MRA (Fig. 6.6a, b) barely delineates the left MCA. The bilateral A1 segments are almost equivalently developed. The distal branches of the left PCA are slightly more dilated than those of the right and work as one of the collateral pathways. On dynamic color-coded RPI images (Fig. 3.6c), most of the territory of the left MCA gradually stains green, indicating that the area is supplied by the left ACA (fed by the left ICA) via leptomeningeal anastomosis. The posterior part of the territory of the left MCA is faintly stained, which suggests decreased perfusion. The left parietal region is stained blue, which shows that the area is fed by the PCA via collateral circulation (Fig. 3.6, lower row, arrows).

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Fig. 6.4 Case 1: typical case of RPI obtained from a healthy volunteer. See text. (a) Axial view of time-of-flight magnetic resonance (MR) angiography. (b) Upper row: T1-weighted images of representative axial planes; lower row: RPI images corresponding to each T1-weighted image. These color-coded perfusion images clearly demonstrate each arterial territory with a different color: red, right internal carotid artery (ICA); green, left ICA; and blue, posterior circulation. Note the right basal ganglia are supplied by the right (red) carotid artery; the left basal ganglia, by the left (green) carotid artery; and the thalami by the posterior cerebral artery (PCA) from the basilar artery (blue)


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Fig. 6.5 Case 2: RPI of a healthy volunteer with a variation of the circle of Willis. See text. Upper row: left, axial view of magnetic resonance angiography (MRA); right, three T1-weighted images. Lower row: left, magnified image of the MRA above; right, three RPI images corresponding to the T1-weighted images above. The horizontal segment (A1) of the right anterior cerebral artery (ACA) is hypoplastic (lower left, arrow). The green of the territory of the right ACA territory means the region is fed by the left internal carotid artery (ICA) (RPI images, arrows)

Case 4 is a 66-year-old woman with occlusion of the right common carotid artery, who was treated by carotid arterial stenting for left proximal common carotid stenosis. MRA of the neck shows occlusion of the right common carotid artery at its origin (Fig. 6.7a), but the right ICA (Fig. 6.7a, large arrow) can be seen, presumably via a collateral pathway from deep cervical and/or ascending cervical arteries (Fig. 6.7a, small arrows) and vertebro-occipital anastomosis. The proximal portion of the left common carotid artery is not visible (Fig. 6.7a, long arrow) because of artifact from the carotid stent (its patency is confirmed by conventional digital subtraction angiography [DSA]). MRA of her head shows comparatively well delineated right MCA that is supposed to be supplied by posterior circulation via PCoA as well as anterograde blood flow from the right ICA (Fig. 6.7 b, c). Fig. 6.7d shows the dynamic color-coded RPI images that correspond to the plane of the T2-weighted image. The blue color of the right MCA territory in the early phase suggests blood flow from posterior circulation via the PCoA. Its subsequent red color implies antegrade slow blood flow from the right ICA. Interestingly, the territory of the right PCA also appears red in the late phase, which should indicate that it is fed by the right ICA as well as the posterior circulation. Although the reason for this phenomenon is unclear, explanations may include that the proximal portion of the dominant right VA appears relatively tortuous, which may slightly decrease perfusion, or that there was some calculation error in the dual-vessel labeling method. Further studies are required to validate this

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method. The green of the territories of the left ACA and PCA suggests that these areas should be fed by the left ICA, which is explained by hyposlasia of the right A1 and the embryonic type of the left PCA. Case 5 is a 65-year-old man who was examined for right hand weakness. MRA revealed occlusion of the left ICA at its origin from the common carotid artery at the neck. The patient underwent surgery for anastomosis between the left superficial temporal artery (STA) and left MCA (STA-MCA anastomosis). Fig. 6.8 presents images from MRA and RPI following bypass surgery. On MRA (Fig. 6.8a, b), the left ICA is not seen, and the left MCA is faintly delineated through collateral flow via the anterior communicating artery (ACoA). A branch of the STA is anastomosed to a branch of the left MCA (Fig. 6.8a, b, yellow arrows).

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Fig. 6.6 Case 3: a patient with severe stenosis of the left middle cerebral artery (MCA). See text. (a) Axial view of magnetic resonance angiography (MRA). (b) Frontal view of MRA deleting posterior circulation. The horizontal segment (M1) of left MCA shows severe stenosis from its origin (small arrows, a, b). The left PCA is dilated to the distal portion (large arrow, a). (c) Left column: T2-weighted image; right four columns: dynamic sequential regional perfusion images (RPI) corresponding to the planes of the T2-weighted images. “t” represents the time (in milliseconds) after labeling

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Fig. 6.7 Case 4: a patient with occlusion of the right common carotid artery. See text. (a) Frontal view of magnetic resonance angiography (MRA) of the neck. The right common carotid artery is not visible, but the right internal carotid artery (ICA, large arrow) can be seen. Small arrows indicate ascending cervical and/or deep cervical arteries. The proximal portion of the left common carotid artery is not visible (long arrow) because of artifact from the carotid stent. (b) Frontal view of MRA of the head (vertebro-basilar arteries are cut off); the right ICA is relatively well delineated. Note hypoplasia of the right horizontal segment (A1) of the anterior cerebral artery (arrow). (c) Axial view of MRA of the head. Note the well developed right posterior communicating artery (large arrow) and embryonic-type left PCA (small arrow). (d) T2-weighted image and dynamic sequential regional perfusion images (RPI) corresponding to the plane of the T2-weighted image

6 Regional MR Perfusion Topographic Map of the Brain Using Arterial Spin Labeling at 3 Tesla Fig. 6.8 Case 5: a patient with occlusion of the left internal carotid artery (ICA), who underwent surgery for anastomosis of the superficial temporal and middle cerebral arteries (STA-MCA anastomosis). See text. (a) Axial view of magnetic resonance angiography (MRA). (b) Semi-frontal view of MRA. Yellow arrows indicate site of anastomosis between the STA and MCA. The patient has an embryonic-type right PCA (white arrow, a). (c) T2-weighted images (upper row) and corresponding planes of regional perfusion images (RPI, lower row). The territory of the right PCA (white arrow) and the anterior part of the territory of the left MCA (small yellow arrow) are red, and the posterior part of the territory of the left MCA is green (large yellow arrow)

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The MRA also reveals an embryonic-type right PCA (Fig. 6.8a, white arrow), meaning that the right PCA is fed from a well developed PCoA and does not communicate with the basilar artery. In the RPI images (Fig. 6.8c), the anterior part of the territory of the left MCA is red (small yellow arrows) and the posterior part, green (large yellow arrows), which suggests that the anterior part is supplied from the right ICA via the ACoA and that the posterior part is perfused by blood from the anastomosis of the STA and MCA. The red stain of the right PCA territory indicates the area is supplied by blood from the right ICA (Fig. 6.8c, white arrows).

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6.4 Conclusions RPI permits noninvasive acquisition of topographic information regarding the blood supply from individual cerebral arteries, the right and left ICA, and the posterior circulation, that has been inaccessible by other imaging methods. The method may clarify hemodynamic changes in circulation in cases with major cerebral arterial obstruction and assist evaluation of indications and results of treatments such as bypass surgery, carotid endarterectomy, or carotid stenting.

References 1. Golay X, Hendrikse J, Lim TC. Perfusion imaging using arterial spin labeling. Top Magn Reson Imaging. 2004;15:10–27. 2. Golay X, Hendrikse J, Van Der Grond J. Application of regional perfusion imaging to extraintracranial bypass surgery and severe stenoses. J Neuroradiol. 2005;32:321–4. 3. Golay X, Petersen ET, Hui F. Pulsed star labeling of arterial regions (PULSAR): a robust regional perfusion technique for high field imaging. Magn Reson Med. 2005;53:15–21. 4. Gunther M, Bock M, Schad LR. Arterial spin labeling in combination with a look-locker sampling strategy: inflow turbo-sampling EPI-FAIR (ITS-FAIR). Magn Reson Med. 2001;46:974–84. 5. Hendrikse J, van der Grond J, Lu H, van Zijl PC, Golay X. Flow territory mapping of the cerebral arteries with regional perfusion MRI. Stroke. 2004;35:882–7. 6. Jones CE, Wolf RL, Detre JA, Das B, Saha PK, Wang J, et al. Structural MRI of carotid artery atherosclerotic lesion burden and characterization of hemispheric cerebral blood flow before and after carotid endarterectomy. NMR Biomed. 2006;19:198–208. 7. Lim C, Petersen E, Ng I, Hwang P, Hui F, Golay X. MR regional perfusion imaging: visualizing functional collateral circulation. AJNR Am J Neuroradiol. 2007;28:447–8. 8. Luh WM, Wong EC, Bandettini PA, Hyde JS. QUIPSS II with thin-slice TI1 periodic saturation: a method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling. Magn Reson Med. 1999;41:1246–54. 9. Petersen ET, Lim T, Golay X. Model-free arterial spin labeling quantification approach for perfusion MRI. Magn Reson Med. 2006;55:219–32. 10. van Laar P, Hendrikse J, Golay X, Lu H, van Osch M, van der Grond J. In vivo flow territory mapping of major brain feeding arteries. Neuroimage. 2006;29:136–44. 11. Wintermark M, Sesay M, Barbier E, Borbély K, Dillon WP, Eastwood JD, et al. Comparative overview of brain perfusion imaging techniques. Stroke. 2005;36:e83–99. 12. Wolf R, Detre J. Clinical neuroimaging using arterial spin-labeled perfusion magnetic resonance imaging. Neurotherapeutics. 2007;4:346–59. 13. Zimine I, Petersen ET, Golay X. Dual vessel arterial spin labeling scheme for regional perfusion imaging. Magn Reson Med. 2006;56:1140–4.

Normal Anatomy of Intracranial Veins: Demonstration with MR Angiography, 3D-CT Angiography and Microangiographic Injection Study

7

Akio Fukusumi

7.1 Cranial Dural Venous Sinuses (Figs. 7.1–7.3) The dural sinuses are situated between two layers of dura mater and consist of a system of channels that collect and drain the intracranial venous blood. They have no valves but contain irregular trabeculae. Most of them are triangular in cross section and therefore noncompressible, except for the cavernous and sigmoid sinuses [6]. The sinuses may be divided into superior and inferior groups. The collecting point of the superior group is the confluence of sinuses, which receives blood from the major part of the brain and drains into the internal jugular veins through the transverse and sigmoid sinuses (Figs. 7.1 and 7.2). The collecting point for the inferior group is the cavernous sinus, where the blood is collected mainly from the sphenoparietal sinus, superficial middle cerebral (Sylvian) veins, orbital veins, and veins on the basal medial part of the brain. The blood then empties into the sigmoid sinus or internal jugular vein via the superior and inferior petrosal sinuses or via the basilar plexus (Fig. 7.3). The pterygoid plexus is another important channel that drains the cavernous sinus. All sinuses and pericranial veins form a communicating system that is able to compensate in the event of localized venous occlusion [24].

7.1.1 Superior Sinus Group 7.1.1.1 Superior Sagittal Sinus The superior sagittal sinus (SSS) runs in the attached convex margin of the falx cerebri and begins near the crista galli, receiving a vein from the nasal cavity when the foramen caecum is patent. However, the initial 10–20 mm of this sinus in the anterior-most part,

A. Fukusumi Department of Radiology, Takanohara Central Hospital, Nara, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_7, © Springer-Verlag London Limited 2010

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Fig. 7.1 Normal anatomy of dural venous sinuses (lateral view). (a) MR venography (3D contrastenhanced time of flight (TOF) MR angiography): 3D gadolinium-enhanced MR angiography (MRA) was performed in the sagittal plane using fast field echo method with fat suppression. The scan was started 30 seconds after a manual intravenous bolus injection of Gd-DTPA (10 mL). Scan parameters: repetition time (TR), 4.5 ms; echo time (TE), 2.3 ms; flip angle, 60°; matrix, 128 × 256; 3 mm slice with 50% overlap reconstruction; field of view (FOV), 22.0 × 22.0 cm. (b) Anatomical diagram of dural venous sinuses. AG arachnoid granulation; BVR basal vein of Rosenthal; CS confluence of sinuses; CvS cavernous sinus; EmV emissary vein; ICV internal cerebral vein; IJV internal jugular vein; IPS inferior petrosal sinus; ISS inferior sagittal sinus; OS occipital sinus; SpPS sphenoparietal sinus; SgS sigmoid sinus; SS straight sinus; SPS superior petrosal sinus; SSS superior sagittal sinus; TS transverse sinus; VG vein of Galen; VL venous lacunae; VP venous pouch

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Fig. 7.2 Normal anatomy of dural sinuses (anterior oblique view). (a) Venous phase of 3D-CT angiography (3D-CTA). (b) Anatomical diagram of dural venous sinuses. (Abbreviations are the same as in Fig. 7.1.)In this case, the superior sagittal sinus (SSS) was prematurely duplicated into right and left limbs, draining into the same-side transverse sinus (TS). The confluence of sinuses thus cannot be indicated.

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Fig. 7.3 Inferior group of dural venous sinuses of cranial base (dorsal view). (a) Venous phase of 3D-CTA combined with cranial base of skull. (b) Schematic drawing of the skull base demonstrating relationships of major dural venous sinuses. BP basilar plexus; CS confluence of sinuses; CvS cavernous sinus; EmV emissary vein; IJV internal jugular vein; IPS inferior petrosal sinus; MS marginal sinus; OS occipital sinus; SOV superior orbital vein; SgS sigmoid sinus; SpPS sphenoparietal sinus; SPS superior petrosal sinus; TS transverse sinus

superior to the foramen caecum, usually consists of fibrous tissue [26], and the first tributaries are mostly ascending cortical veins from the frontal lobes. These veins enter more laterally into the dura than veins located more posteriorly [30]. In some cases, the SSS is atretic anterior to the level of the coronal suture. In such cases, prominent superior frontal veins that course longitudinally and nearly parallel to the attachment of the falx drain upward and posteriorly, converging near the coronal suture to form the SSS [10, 25] (Fig. 7.4). The SSS runs posteriorly along the median sagittal groove of the internal midline surface of the frontal bone, the adjacent medial margin of the bilateral parietal bones, and occipital bone [35]. Near the internal occipital protuberance, the sinus deviates (usually to the right) and continues to become the ipsilateral transverse sinus [16, 31]. The SSS, which shows a triangular shape in cross-section, gradually enlarges as it progresses backwards. The interior presents the openings of the superior cerebral veins, projecting arachnoid granulation, and numerous fibrous bands across the inferior angle. The sinus also communicates by small orifices with irregularly shaped lateral venous lacunae situated in the dura mater near the sinus, usually three on each side: a small frontal lacuna, a large parietal lacuna, and an intermediate-sized occipital lacuna [3–6]. The SSS and its lateral venous lacunae receive some superior cerebral veins and, near the posterior end of the sagittal suture, veins from the pericranium passing through the parietal foramina. The lateral lacunae also receive the diploic and meningeal veins. The lateral lacunae are often so complex as to be almost plexiform, and rarely take the form of simple venous lumen (Figs. 7.5 and 7.6) [1, 6, 20, 28, 35, 52].

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Fig. 7.5 Venous lacunae (lake) [6]. (a) Venous phase of 3D-CTA showing the superior sagittal sinus (SSS), venous lacunae (VL), and superior cerebral veins (SCVs) (ventral view). (b) Schematic of the venous phase of 3D-CTA. SCV1 superior cerebral veins that directly join the SSS; SCV2 superior cerebral veins that pass beneath a VL to join the SSS; SCV3 superior cerebral veins that join both the SSS and a VL; SCV4 superior cerebral veins that join a VL

7.1.1.2 Inferior Sagittal Sinus The inferior sagittal sinus (ISS) runs within or slightly above the free margin of the falx. The ISS begins above the level of the anterior body of the corpus callosum, receiving the blood from the falx cerebri, the medial surface of the cerebral hemisphere, and the corpus

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callosum. The sinus then turns backward to join the vein of Galen behind the splenium of the corpus callosum, becoming the straight sinus [24, 33].

7.1.1.3 Straight Sinus The straight sinus is located in the junction of the falx cerebri and the tentorium cerebelli. From the confluence of the vein of Galen and the ISS, this structure runs posteroinferiorly toward the internal occipital protuberance. The sinus may communicate terminally, but quite variably, with the confluence. Vermian veins and tentorial sinuses from superior cerebellar hemispheric veins may also be received [10, 32].

7.1.1.4 Falcine Sinus (Fig. 7.7) The falcine sinus, a venous pathway located in the falx cerebri, is a normal anatomical structure in the fetus that closes after birth. It is rarely observed in adult population but, when present, is more commonly concomitant with conditions such as

260 Fig. 7.7 Persistent falcine sinus (PFS) on the venous phase of 3D-CTA (oblique view). PFS connects from the vein of Galen (VG) to the superior sagittal sinus (SSS), in a similar manner to the straight sinus (SS) more inferiorly. CS confluence of sinuses; ISS inferior sagittal sinus

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malformations of the vein of Galen, arteriovenous malformation, absence of the corpus callosum, osteogenesis imperfecta, acrocephalosyndactyly, and Chiari II malformation [45, 47].

7.1.1.5 Occipital Sinus (Fig. 7.8) The occipital sinus begins near the confluence of sinuses and runs within the attached edge of the cerebellar falx toward the foramen magnum. Inferiorly, it typically divides into both limbs of the marginal sinus, which drain into the jugular bulbs. The marginal sinus often forms anastomoses with the occipital and external and internal vertebral plexuses. The reported frequency of the occipital sinus in adult dissected cadaveric studies varies from 64.5 to 93% [11, 18, 29, 48]. Large occipital sinuses may represent a persistent configuration in the fetal stage, presumably compensating for hypoplastic posterior dural sinuses as the main draining venous pathways (Fig. 7.8a). The varied configurations of the occipital sinus are believed to derive from the various degrees of development and regression during the later fetal stage from 6 months through to birth [39].

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Fig. 7.8 Transaxial MR venography (3D contrast-enhanced TOF MRA) of persistent occipital sinuses. (a) Bilateral occipital sinuses (OSs) are well developed, supposedly compensating for hypoplastic left transverse sinus (TS). (b) Left large persistent occipital sinus (OS)

7.1.1.6 Confluence of Sinuses The term “confluence of sinuses” refers to the dilated posterior end of the SSS, which often deviates to one side (usually the right) of the internal occipital protuberance and where it turns to become a transverse sinus [16]. The confluence also connects with the straight, occipital, and contralateral transverse sinuses. The size and degree of communication of channels meeting at the confluence are variable (Figs. 7.2 and 7.9). In many instances,

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Fig. 7.9 Normal variations in drainage type of superior sagittal sinus (SSS) into the confluence of sinuses on MR venography (transaxial view) (3D contrast-enhanced TOF MRA) [15]. Draining pattern of the superior sagittal sinus (SSS) into the transverse sinus (TS) is classified into four types. (a) The SSS reaches the centrally located confluence, then divides into bilateral TSs (15%). (b) The SSS prematurely duplicates into right and left channels, each of which drains into the same-side TS (26%). (c) The SSS predominantly drains into the right TS (49%). (d) The SSS predominantly drains into the left TS (10%)

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communication is absent or tenuous. Any sinus involved may be duplicated, narrowed, or widened near the confluence [7, 27, 31].

7.1.1.7 Transverse-Sigmoid Sinus The transverse sinus is usually the largest draining channel among the dural sinuses. The sinus begins as an internal occipital protuberance and runs within the attached margin of the tentorium and within the transverse sulcus of the occipital bone toward the upper margin of the petrosal pyramid. Leaving the tentorium, the structure becomes the sigmoid sinus [10]. The terminal part of the transverse sinus receives the superior petrosal sinus (SPS), which extends within the attached margin of tentorium at the petrous bone (Fig. 7.3). The sigmoid sinus runs medially and inferiorly, taking an S-shaped course within the sigmoid sulcus and resting on the mastoid part of the temporal bone, and reaches the internal jugular vein. Before entering the foramen jugulare, the sigmoid sinus receives the condylar emissary vein, which communicates with the veins of scalp (Figs. 7.1, 7.3, 7.10 and 7.11). As unilateral hypoplasia and/or aplasia of these sinuses are often seen, these variations should be taken into consideration when diagnosing venous sinus thrombosis [54, 55].

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Fig. 7.10 Variations of draining type of the inferior petrosal sinus (IPS). (a) Venous phase of 3D-CTA. (b) Schematic of classification into four types [34, 46]. a IPS anastomoses with the internal jugular vein (IJV), while anterior condylar vein (ACV) is small or absent (45%). b ACV is large and has a prominent anastomosis with the IPS, which also has a junction with the IJV (24%). c IPS exists as several small channels that communicate with both ACV and IJV (24%). d IPS does not join IJV, emptying directly into ACV (7%)

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Fig. 7.11 Pathway of communications for intra- and extracranial venous system (emissary veins) [10, 16]. EmV emissary vein; VPx venous plexus

7.1.2 Inferior Sinus Group (Basal Sinus Group) (Fig. 7.3) The venous channels of the inferior group form an extensive spider web-like network over the undersurface of the brain, centered on the cavernous sinus [10].

7.1.2.1 Cavernous Sinus (Figs. 7.3 and 7.10) The cavernous sinus is a paired venous structure. Anteriorly, it receives the superior and inferior ophthalmic veins and sphenoparietal sinus, and occasionally receives the superficial Sylvian vein directly. Posteriorly, the cavernous sinus drains into the superior and inferior petrosal sinuses. The cavernous sinus further communicates with the pterygoid plexus through the foramina ovale and lacerum [10] (Fig. 7.11).

7.1.2.2 Superior Petrosal Sinus (Fig. 7.3) The SPS connects the posterior part of the cavernous sinus with the lateral end of the transverse sinus at its junction with the sigmoid sinus. Normal blood flow in the SPS is forward, toward the confluence of the SPS and the posterior part of the cavernous sinus at the apex of the petrosal pyramid.

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7.1.2.3 Inferior Petrosal Sinus (Fig. 7.10) The inferior petrosal sinus (IPS) is an important venous pathway that drains venous blood from the cavernous sinus to the internal jugular bulb [34]. Shiu et al. [46] have described four different types of IPS, as illustrated in Fig. 7.10b.

7.1.2.4 Sphenoparietal Sinus (Fig. 7.3) The sphenoparietal sinus courses medially along the undersurface of the lesser wing of the sphenoid bone. This sinus represents the medial continuation of the superficial Sylvian vein and may receive tributaries from the meningeal veins and veins that drain the orbital gyri of the frontal lobe. Three typical patterns of drainage are seen: (1) into the cavernous sinus, (2) into the pterygoid plexus via basal emissary veins (sphenobasal vein), or, (3) posteriorly along the floor of the middle cranial fossa, then passing over the petrous pyramid to drain into the IPS or transverse sinus (sphenopetrosal sinus) [10, 19] (see Sect. 7.2.1.1). The sinus may communicate with the basal vein of Rosenthal via the uncal vein [53].

7.1.2.5 Basilar Plexus (Fig. 7.3) The basilar plexus, also known as the occipital plexus or clival venous plexus, consists of a wide meshed network of intercommunicating channels within the dura on the clivus. This plexus is located between the cavernous and inferior petrosal sinuses and extends to the foramen magnum, then continues to the internal vertebral venous plexus.

7.1.2.6 Emissary Veins (Fig. 7.11) The dural venous sinuses communicate with the extracranial veins by way of emissary veins. These veins traverse the skull via named or unnamed foramina and provide important pathways of collateral blood flow; however, they also possibly allow the spread of infection [10, 16].

7.2 Cerebral and Cerebellar Veins The veins of the brain have no valves and thin walls containing no muscular tissue. These vessels pierce the arachnoid membrane and inner dural layer to open into the cranial venous sinuses. The veins of the brain comprise cerebral and cerebellar veins and veins of the brainstem, and are divided according to their locations into two groups: supra- and infratentorial. Supratentorial veins mainly drain the cerebral hemispheres, while infratentorial veins drain the cerebellum and brainstem.


265

Table 7.1 Veins of the cerebral hemisphere (Modified from Okudera et al. [38]) Superficial cerebral (or cortical) veins or pial veins Superior cerebral veins (or ascending cortical veins) Veins of the lateral convexity side Veins of the medial side Superficial middle cerebral veins (or superficial Sylvian veins) Inferior cerebral veins (or descending cortical veins) Veins of the lateral convexity side Veins of the medial side (which drain into the basal cerebral vein) Veins of the basal or inferior side (which drain into the lateral tentorial, superior petrosal, or transverse sinus) Parenchymal veins Superficial parenchymal veins Intracortical veins Subcortical veins (including arcuate veins) Superficial medullary veins Deep parenchymal veins Deep medullary veins First (or outer) zone of convergence Second (or candelabra) zone of convergence Third (or palmate) zone of convergence Subependymal veins (including the longitudinal caudate veins of Schlesinger) Fourth (or subependymal) zone of convergence Transcerebral and anastomotic cerebral veins

7.2.1 Supratentorial Veins The veins of the cerebral hemisphere are divided into the superficial cerebral veins and parenchymal veins [23, 38, 41] (Table 7.1).

7.2.1.1 Superficial Cerebral Veins Superficial cerebral veins (superficial cortical veins or pial veins) can be divided, from the direction of venous flow, into three groups: superior cerebral veins (ascending cortical veins), superficial middle cerebral veins (superficial Sylvian veins), and inferior cerebral veins (descending cortical veins) (Figs. 7.12 and 7.13).

Superior Cerebral Veins (Ascending Cortical Veins) These veins are composed of medial and lateral group. Medial group veins ascend along the medial surface of the cerebral hemisphere in the interhemispheric fissure (Fig. 7.12) while lateral group veins ascend on the lateral cerebral surface (Fig. 7.13). These two

266

A. Fukusumi

a

PaCV

PMFV

AMPV

CMFV

b PMFV

PMPV

APCV

ISS

PaCV AMPV

PPCV

ICV

PCV

VG

PCV

BVR

AMFV

ICV

ACA

PMPV

PPCV

CMFV APCV

VG

AMFV

Fig. 7.12 Superficial veins of the medial surface of cerebral hemisphere. (a) Midsagittal maximum intensity projection image of MR venography (3D contrast-enhanced TOF MRA). (b) Schematic of veins of the medial surface of the cerebral hemisphere (modified from [35]). Superficial veins of the medial surface drain into the dural sinuses, divided to four directions: (1) tributaries of the superior sagittal sinus (blue), (2) tributaries of the superficial Sylvian vein (red), (3) tributaries of the lateral tentorial sinus or transverse sinus (green), and (4) tributaries of the deep venous system (yellow). ACA anterior cerebral artery; AMFV anteromedial frontal vein; AMPV anteromedial parietal vein; APCV anterior pericallosal vein; BVR basal vein of Rosenthal; CMFV centromedial frontal vein; ICV internal cerebral vein; ISS inferior sagittal sinus; PaCV paracentral vein; PCV posterior calcarine vein; PMFV posteromedial frontal vein; PMPV posteromedial parietal vein; PPCV posterior pericallosal vein; VG great vein of Galen

a PrCV MFV

PFV

CV

Superficial Sylvian vein FPV Vein of Labbe PTV MTV ATV

PrCV

PoCV APV

Vein of Trolard

AFV

Vein of Trolard

b PFV

PPV

CV

PoCV APV

PPV

MFV

OV

OV AFV FPV

Superficial Sylvian vein

PTV MTV ATV Vein of Labbe

Fig. 7.13 Superficial cerebral veins of the lateral surface of the cerebral hemisphere. (a) Lateral view of venous phase of 3D-CTA. (b) Schematic of superficial cerebral veins of the lateral surface of the cerebral hemisphere (modified from [35]). Superficial veins of the lateral surface drain into the dural sinus, divided into three directions: (1) tributaries of the superior sagittal sinus (blue), (2) tributaries of the superficial Sylvian vein (red), and (3) tributaries of the lateral tentorial sinus or transverse sinus (green). AFV anterior frontal vein; APV anterior parietal vein; ATV anterior temporal vein; CV central vein; FPV frontopolar vein; MFV middle frontal vein; MTV middle temporal vein; OV occipital vein; PFV posterior frontal vein; PoCV postcentral vein (vein of Trolard); PPV posterior parietal vein; PrCV precentral vein; PTV posterior temporal vein (vein of Labbe)


267

groups pierce the arachnoid membrane and merge, opening into the SSS. This draining portion of the SSS is called the “bridging vein,” and is often the origin of subdural hematoma following head trauma. Anterior veins open almost perpendicular to the SSS, and the larger posterior veins are directed obliquely forward against the current in the sinus (Fig. 7.14) [35]. This characteristic pattern may represent a mechanism to resist the collapse of the thin-walled cerebral veins that might result from a rise in intracranial pressure [16]. Alternatively, the pattern may be derived from rapid backward growth of the cerebral hemisphere during development and the consequent displacement of vessels, with relative anchoring of openings into the SSS. In the parietal region, several lateral superior cerebral veins may merge into two or three main trunks or into a single trunk known as the vein of Trolard or superior anastomotic vein. This vein, present in about one-third of individuals, connects the SSS with the superficial middle cerebral vein [19, 35] (Fig. 7.13).

Superficial Middle Cerebral Vein (Superficial Sylvian Vein) (Fig. 7.13) The superficial middle cerebral vein drains the opercula and areas adjacent to the lateral cerebral fissure [53]. Variations in the drainage of the superficial middle Sylvian vein are common, showing four major variations with: (1) the vein entering the sphenoparietal sinus draining into the cavernous sinus to the IPS, (2) the vein entering the sphenobasal vein (paracavernous sinus) draining to the pterygoid plexus directly, (3) the vein entering the sphenopetrosal vein with outflow via the transverse sinus, or (4) absence of a definite superficial middle cerebral vein, but instead with drainage into the veins of Trolard and Labbe [19] (Fig. 7.15).

a

FPV

FPV AFV

b FPV: Frontopolar vein

MFV PFV

AFV: Anterior frontal vein MFV: Middle frontal vein PFV: Posterior frontal vein

PrCV

CV PoCV APV PPV

PrCV

PrCV: Precentral vein CV: Central vein PoCV: Postcentral vein (vein of Trolard)

CV PoCV

APV: Anterior parietal vein

APV

PPV: Posterior parietal vein

PPV

OV: Occipital vein

OV

Fig. 7.14 Superior cerebral veins (tributaries of the superior sagittal sinus). (a) Superior view of venous-phase 3D-CTA. (b) Superior view of the cerebral hemispheres showing veins from the lateral surface of the cerebrum entering the SSS (modified from [35])

268

A. Fukusumi

Fig. 7.15 Variations in drainage of the superficial Sylvian vein indicated on CT venography shown on the internal surface of the skull base [19]. 1 Flow from the sphenoparietal sinus (SpPS) to the cavernous sinus (CvS) to the inferior petrosal sinus (IPS). 2 Flow from the sphenobasal vein (SpBaV) to the pterygoid plexus. 3 Flow from the sphenopetrosal vein (SpPeV) to the transverse sinus (TS). 4 Absence of a definite superficial middle cerebral vein, with drainage into the veins of Trolard and Labbe

Inferior Cerebral Veins (Descending Cortical Veins) (Fig. 7.13) The inferior cerebral veins drain the lower portions of the lateral surface of the brain and the undersurfaces of the occipital and temporal lobes. A major trunk over the temporooccipital lateral surface, which may extend from the Sylvian fissure downward and backward to the transverse sinus, is called the vein of Labbe. Angiographically, the vein of Labbe is recognized on the left side in 77% of individuals and on the right in 66% [19]. When the vein of Labbe is large, the vein of Trolard and superficial middle cerebral (Sylvian) vein are often small or absent.

7.2.1.2 Parenchymal Veins Parenchymal veins are divided into three groups: superficial parenchymal veins, deep parenchymal veins, and transcerebral veins [23, 38].

Superficial Parenchymal Veins (Superficial Draining Veins) Superficial parenchymal veins collect the venous blood flow from the cerebral cortex (intracortical veins), subcortical white matter (subcortical veins including arcuate veins), and superficial medullary veins (Fig. 7.16).

269


a

b

Pial v. Intracortical v. Subcortial v. Superficial medullary v. Anastomotic medullary v.

PV Ic SMV Sc Ic

Deep medullary v.

2

DMV

SbF

3

F ICV

SMV

DMV

PC

LV

Ic P

2 4 SGS

Ch

SMV Sc

Arc SMV DMV 1 AMV Arc 2

CG

CC PS

PV

1

TCV

PV

4 LCV

SEV

SOFF

2 SMC

3 CR PesCR

Fig. 7.16 Microangiographical normal venous structure of the cerebral hemisphere. (a) Coronal microangiography of the venous system (10 mm thick) showing parenchymal veins converging towards the superolateral corner of the anterior horn of the lateral ventricle. (b) Schematic in coronal plane showing the venous architecture of the cortex and white matter of the cerebral hemisphere. Modified from [22, 38]. 1 First or “outer” zone of convergence. 2 Second or “candelabla” zone of convergence. 3 Third or “palmate” zone of convergence. 4 Fourth or “subependymal” zone of convergence. AMV anastomotic medullary vein; Arc arcuate vein (or veins of arcuate fibers); CC corpus callosum; Ch choroid plexus; CG cingulate gyrus; CR corona radiata; DMV deep medullary vein; F fornix; Ic intracortical vein; ICV internal cerebral vein; LCV (vessels running in the anterior–posterior direction are represented as multiple dots) longitudinal caudate veins of Schlesinger; LV lateral ventricle; PC pericallosal cistern; PesCR base of the corona radiata; PS posterior septal vein; PV pial veins; SbcaF subcallosal fasciculus; Sc subcortical vein; SEV subependymal vein; SGS subependymal glial substance; SMV superficial medullary vein; SMC substantia medullaris cerebri; SOFF (hatched area) superior occipitofrontal fasciculus; TCV transcerebral vein

270

A. Fukusumi

Intracortical veins: These are numerous, short veins that run outwards (superficially), collecting tiny straight and lateral intracortical twigs, and penetrate the cortical surface at right angles to join the corresponding superficial cerebral veins (pial veins). Subcortical veins: These consist of the superficial medullary segment, the arcuate segment, and intracortical segment, which pierces the cortex outward at right angles to open into a superficial cerebral vein (pial vein). The superficial medullary segment, a very short segment of these veins, originates in the superficial portion of the white matter beneath the arcuate fibers, runs superficially, and penetrates the layers of arcuate fibers at right angles. The arcuate segment (a continuation of the superficial medullary segment) frequently takes a zig-zag course as it pierces the layer of the arcuate fibers. The intracortical segment (a continuation of the arcuate segment) takes a course similar to that of the intracortical veins. Superficial medullary veins: These veins originate within the gyral white matter or anywhere in the centrum semiovale. The superficial medullary veins run superficially and penetrate the cortex at right angles to finally join the pial veins through the intra- or subcortical veins, or sometimes drain directly into the pial veins.

Deep Parenchymal Veins (Deep Draining Veins of the White Matter) Veins of the white matter that drain deeply are called deep medullary veins. These vessels run deeply to join the corresponding subependymal veins, usually at the superolateral corner of the lateral ventricle [23]. The deep medullary veins in the frontoparietal area converge successively in four zones as they traverse the cerebral white matter deeply to join the subependymal venous system [22, 38] (Table 7.1; Fig. 7.16). In the course of the deep medullary veins, three zones of convergence are seen: first (or outer) zone of convergence (bamboo-branch and hat-tree union), second (or candelabra) zone of convergence, and third (or palmate) zone of convergence. Finally, the fourth (or subependymal) zone of convergence is formed toward the subependymal veins (including the longitudinal caudate veins of Schlesinger) [44]. The exact mechanisms underlying the formation of converging zones remain unclear, but the most likely explanation lies in the rapid changes in the course, shape, size, number, and density of the converging medullary veins caused by the rapidly growing and crossing nerve fiber tracts (projection, commissural, and association fibers) during intrauterine and early postnatal life. According to Riley’s atlas [42], white matter fiber tracts of the centrum semiovale in the coronal section are divisible into: (1) the peripheral portion of the corona radiata, the “substantia medullaris cerebri”, (2) the corona radiata, (3) the pes (foot or base) of the corona radiata, and (4) the substantia reticularis coronae radiatae. The subcallosal fasciculus and superior occipitofrontal fasciculus are also indicated in that atlas and are shown to occupy the most medial, major part of the “substantia reticularis coronae radiatae.” The second and third zones of convergence may be formed to conform to the junction between the corona radiata and pes of the corona radiata, and the junction between the pes of the corona radiata and the substantia reticularis coronae radiatae, respectively. The fourth (or subependymal) zone of convergence is located medial to the superior occipitofrontal-subcallosal fascicular complex (the substantia


271

reticularis coronae radiatae). This zone occupies the lateral part of the subependymal glial substance. The longitudinal caudate veins of Schlesinger are located at this site. The first zone of convergence appears to spread over a wide area of peripheral white matter, the generating mechanism of which has not been related to any specific parenchymal structures [22, 38] (Fig. 7.16).

Transcerebral and Anastomotic Cerebral Veins A vein bridging between a superficial medullary vein and a deep medullary vein is called an anastomotic medullary vein. Occasionally, a vein may extend from a pial vein down to a subependymal vein or the longitudinal caudate vein of Schlesinger [44]. Such vessels have been designated as transcerebral veins [21–23, 38] (Table 7.1, Fig. 7.16).

7.2.1.3 Deep Cerebral Veins Including the Vein of the Basal Ganglionic and Thalamic Regions These deep medullary veins mentioned above (see Sect.7.2.1.2.2) drain into the deep venous system, i.e., the internal cerebral vein and basal vein of Rosenthal, together with the venous flow from the basal ganglionic and thalamic regions [21, 23, 37, 40] (Fig. 7.17).

Fig. 7.17 Schematic showing general features of the cranial venous system as quoted from “Radiologic Anatomy of the Brain” [21]. AMV anastomotic medullary vein; BVR basal vein of Rosenthal; CvS cavernous sinus; DMV deep medullary vein; DV diploic vein; EV ependymal veins; ESSV external superior striate vein; ICV internal cerebral vein; ISV inferior striate vein; IVV inferior ventricular vein; LCV longitudinal caudate veins; MV meningeal vein; ScV scalp vein; SeV septal vein; SMV superficial medullary vein; SSV superior striate veins; SSyV superficial Sylvian vein; SChV superior choroidal vein; SSS superior sagittal sinus; TSV thalamostriate vein; TTV temporal tip vein; TCV transcerebral vein; UV uncal vein; VoCGM vein of cortical gray matter

272

A. Fukusumi

Tributaries of the Internal Cerebral Vein (Table 7.2, Fig. 7.18) Tributaries of the internal cerebral vein with some tributaries of the basal vein of Rosenthal are shown in Table 7.2 [21]. Subependymal veins of the lateral ventricle are divided into two groups, medial and lateral (Fig. 7.18b, c). Furthermore, these vessels drain into the internal cerebral vein from three major sites of venous confluence. Anteriorly, the septal vein, thalamostriate vein, anterior thalamic vein, and superior choroidal vein converge toward the interventricular foramen and join the anterior end of the internal cerebral vein. Posteriorly, the direct lateral vein, medial atrial vein, posterior longitudinal hippocampal vein, a connecting vein from the glomus and sometimes the internal occipital vein, unite medially to the atrium and join the posterior part of the internal cerebral, basal cerebral, or great cerebral vein. Inferiorly, the inferior ventricular vein, inferior choroidal vein, anterior longitudinal hippocampal vein, and anterior hippocampal vein join to form a single trunk in the region medial to the inferior end of the choroid fissure, typically joining the basal cerebral vein [53] (Fig. 7.18a, b).

Table 7.2 Tributaries of the internal cerebral vein, partially including tributaries of the basal vein of Rosenthal (Figs. 7.18 and 7.19) [21] Deep medullary veins Subependymal veins Medial group of subependymal veins Septal vein Posterior septal vein Medial atrial veins Hippocampal veins (vein of the inferior horn) Lateral group of subependymal veins Longitudinal caudate vein of Schlesinger Anterior caudate vein Transverse caudate vein Thalamostriate vein Direct lateral vein (surface thalamic vein) Lateral atrial vein Inferior ventricular vein Superior and inferior choroidal veins Thalamic veins Superior striate veins Posterior pericallosal vein Internal occipital vein Pineal vein Internal cerebral vein

273


a

b

DMV

DMV

DMV SeV

ACV

AnoSeV LCV

ACV

ACV TSV ICV IVV

SeV BVR

ACV SChV

TSV ICV

LAV

IVV

LAV

MAV

IChV

VG DLV IOV

MAV

c Pericallosal a.

DMV

Corpus callosum Post. SeV

SSV (Iateral)

Caudate nucleus Chorioid plexus

SChV

Fornix Thalamus

DLV

Choroidal a. SSV (Medial)

ICV

Fig. 7.18 Tributaries of the internal cerebral veins. (a) Susceptibility-weighted image. (b) Diagrammatic representation of the subependymal veins of the lateral ventricle, showing the three major sites of venous confluence. (c) Diagram showing the medial and lateral groups of subependymal veins in coronal section through the bodies of the lateral ventricles. Diagrammatic representation of the subependymal veins of the lateral ventricle, modified from “Radiologic Anatomy of the Brain” [22]. AnoSeV anomalous septal vein; ACV anterior caudate vein; BVR basal vein of Rosenthal; DLV direct lateral vein; DMV deep medullary vein; ICV internal cerebral vein; IChV inferior choroidal vein; IOV internal occipital vein; IVV inferior ventricular vein; LAV lateral atrial vein; LCV longitudinal caudate veins of Schlesinger; MAV medial atrial vein; SChV superior choroidal vein; SeV septal vein; TSV thalamostriate vein

274

A. Fukusumi

Tributaries of the Basal Vein of Rosenthal (Fig. 7.19) The basal vein of Rosenthal can be divided into three major segments: (1) rthe anterior or striate segment, (2) themiddle or peduncular segment; and (3) the posterior or posterior mesencephalic segment. Embryologically, formation of the basal vein of Rosenthal results from sequential changes involving anastomoses, deletions, and reanastomoses of primitive pial venous plexuses. Unsurprisingly, many anatomical variations of this vein are encountered [21, 51].

Veins of the Basal Ganglionic Region (Fig. 7.20a, b) Venous drainage of deep gray and white matter structures in the basal ganglia was microangiographically analyzed by Okudera et al. [15, 37]. According to these studies, veins of the head of the caudate nucleus drain posteromedially into the anterior inferior caudate tributaries of the thalamostriate vein. The globus pallidus, putamen, and internal, external, and extreme capsule are drained via medial and lateral superior and inferior striate (lenticulocapsular) veins. Medial and lateral superior striate (lenticulo-capsular) veins drain into the thalamostriate vein, and medial and lateral inferior striate (lenticulo-capsular) veins drain into the basal vein. The upper and middle portions of the claustrum and external and internal capsules are drained by the lateral superior striate tributaries of the thalamostriate veins and capsuloinsular veins (Fig. 7.20a, b). The capsulo-insular veins run superficially and finally drain into the basal vein of Rosenthal via insular veins. In some instances, through an opercular vein, the vein becomes continuous with the ascending cortical vein. The posterior limb of the internal and external capsule are partially drained posteriorly and open to the subependymal veins of the lateral ventricle (vein of the internal capsule and vein of the external capsule, respectively) (Fig. 7.20c, d).

Veins of the Thalamic Region (Figs. 7.20c, d and 7.21) Based on radio-anatomical studies, thalamic veins were divided into four major drainage groups (superior, inferior, posterior, and anterior thalamic veins) by Giudicelli and Salamon [17], and this classification has generally been used in routine angiographic analysis (Fig. 7.21c). Superimposition of arterial and venous phase data from vertebral angiography disclosed parallelism between the arterial supply and venous drainage of the thalamus, thereby enabling discernment of an orderly pattern in the thalamic circulation. In microangiographic analysis [40], the venous drainage system of the thalamus divides into three major directions: (1) veins of the anterior portion of the thalamus that drain into the internal cerebral vein mainly through the anterior thalamic veins mentioned above and the thalamostriate veins, (2) veins of the superior and medial portions that drain into the superior thalamic veins mentioned above and the subependymal veins of the third ventricle, and continue to the internal cerebral vein and vein of Galen, and (3) veins in the posterior and inferior portions that empty into the basal vein of Rosenthal, mostly through the posterior and inferior thalamic veins named by Giudicelli and Salamon [17] (Fig. 7.20).

275


a

b OfV

1 DMCV

OfV

(1)

2

1

3

3

IVV

ICV

2

ICV

IVV

2 2

1

VG 3 3

IOV

c DMCV

ACV OfV

AIV PrClV CIV PIV

UV ISV

1

PedV

2 3

AHV IVV ALHV

ALML MTCV

IOV

Fig. 7.19 Normal anatomy of the basal cerebral vein and associated tributaries. (a) Venous injected cadaveric specimen. (b) Venous-phase 3D-CTA. (c) Normal anatomy and variations of the basal cerebral vein and its tributaries as quoted from “Radiologic Anatomy of the Brain” [21]. 1: First segment of the basal vein of Rosenthal (BVR). 2: Second segment of BVR. 3: Third segment of BVR. ACV anterior cerebral vein; AHV anterior hippocampal vein; AIV anterior insular vein; ALHV anterior longitudinal hippocampal vein; ALMV anastomotic lateral mesencephalic vein; CIV central insular vein; DMCV deep middle cerebral vein; ICV internal cerebral vein; IOV internal occipital vein; ISV inferior striate vein; IVV inferior ventricular vein; LAV lateral atrial vein; OfV olfactory vein; MTCV medial temporal cortical vein; PedV peduncular vein; PIV posterior insular vein; PrCIV precentral insular vein; UV uncal vein; VG vein of Galen

276

A. Fukusumi

a

b DMV DMV

DMV LCV

DMV

LCV

CdH LV

LSSV SEV

SEV MSSV MISV

IC

MSSV MISV

LISV

LSSV Cla GP Pt LISV IOFF BVR

BVR

c

d

cdH

TCV

LSSV

LV

LSSV TCV Cla EC

Th1

CIV

Th2 Th3

VEC VIC

CIV

GP

Pt

Th1

IC Th2 Th3

VEC

Th

VIC LV

Fig. 7.20 Venous structure in the basal ganglionic and thalamic regions (drawn based on studies by Okudera et al. [37, 40] and Fukusumi et al. [14]). (a) Coronal slice (at the level of the anterior pole of the putamen) of injected specimen from a normal adult. (b) Schematic of the venous structures. (c) Transaxial slice (at the level of the foramen Monro to the pineal body) of injected specimen from normal adult. (d) Schematic of venous structures. BVR basal vein of Rosenthal; CIV capsuloinsular vein; Cla claustrum; CdH head of the caudate nucleus; DMV deep medullary vein; EC external capsule; GP globus pallidus; IC internal capsule; IOFF inferior occipitofrontal fasciculus; LCV longitudinal caudate veins of Schlesinger; LISV lateral inferior striate vein; LSSV lateral superior striate vein; LV lateral ventricle; MISV medial inferior striate vein; MSSV medial superior striate vein; Pt putamen; SEV lateral group of subependymal vein; TCV transverse caudate tributaries; Th thalamus; Th1 group (1) thalamic veins that flow superomedially; Th2 group (2) thalamic veins that flow superiorly; Th3 group (3) thalamic veins that flow inferiorly; VIC vein of the internal capsule; VEC vein of the external capsule


277

7.2.2 Infratentorial Veins (Veins of the Posterior Fossa) (Fig. 7.21) The posterior fossa venous system may be classified most appropriately on the basis of drainage, into the following three groups: (1) superior or galenic draining group, (2) anterior or petrosal draining group, and (3) posterior or tentorial draining group [21]. The nomenclature of veins included in each group is varied [32]. The classification and nomenclature defined by Huang et al. [21], which are based on the anatomical structure and used in many radio-anatomical text books [41], are shown in Table 7.3 and Fig. 7.21. Table 7.3 Veins of the posterior fossa (Fig. 7.21) [21] Superior or galenic draining group Superior cerebellar tributaries Precentral cerebellar vein Superior vermian vein Superior hemispheric veins Mesencephalic tributaries Posterior mesencephalic vein Anterior pontomesencephalic vein Lateral mesencephalic vein Quadrigeminal vein (tectal vein) Anterior or petrosal draining group Tributaries related to the anterior aspect of the brainstem Longitudinal running vein Anterior pontomesencephalic vein Lateral mesencephalic vein Anterior medullary vein Lateral pontine vein Transversely running vein Peduncular vein Transverse pontine vein Vein of the pontomedullary sulcus Tributaries related to the wing of the precentral cerebellar fissure Tributaries related to the cerebellar hemisphere Anterior lateral marginal vein Vein of the great horizontal fissure of the cerebellum Hemispheric veins Tributaries of the cerebellomedullary fissure Retro-olivary (or lateral medullary) vein Vein of restiform body Median tonsillar veins Tributaries related to the posterolatetal fissure (vein of the lateral recess of the fourth ventricle) Posterior or tentorial draining group Tributaries related to the posterior cerebellar notch Inferior vermian veins Tributaries related to the cerebellar hemisphere Superior hemispheric veins Inferior hemispheric veins

278

A. Fukusumi

Superior or galenic draining group Anterior or petrosal draining group Posterior or tentorial draining group

PMV

C

SVV ATV

STV

ITV

PcCV SCuV

PTV QV

SHV

LMV APMV BV

PcCV

SHV

SHV

SHV TPV

IHV

PV SPS

IHV

LPV

IPS

VLR4V ROV

AMV MTV

IVV VRFB

VGHF

Fig. 7.21 Venous structure of the posterior fossa. (a) Lateral view in venous phase of left vertebral angiography. (b) Lateral view of midsagittal MIP image of MR venography (3D contrast-enhanced TOF MRA). (c) Schematic of venous structure of the posterior fossa (quoted from “Radiologic Anatomy of the Brain” [21]). AMV anterior medullary vein; APMV anterior pontomesencephalic vein; ATV anterior thalamic vein; BV brachial vein; IHV inferior hemispheric vein; IPS inferior petrosal sinus; ITV inferior thalamic vein; IVV inferior vermian vein; LMV lateral mesencephalic vein; LPV lateral pontine vein; MTV medial tonsillar vein; PcCV precentral cerebellar vein; PMV posterior mesencephalic vein; PTV posterior thalamic vein; PV petrosal vein; QV quadrigeminal vein (tectal vein); ROV retro-olivary (or lateral medullary) vein; SCuV supraculminate vein; SHV superior hemispheric vein; SPS superior petrosal sinus; STV superior thalamic vein; SVV superior vermian vein; TPV transverse pontine vein; VGHF vein of the great horizontal fissure of the cerebellum; VLR4V vein of the lateral recess of the fourth ventricle; VRFB vein of the restiform body

279


a

b

OEV

OS

LC & PC

OS

MS PC

AC

SOCS

AC PVVP

IJV

VPVA SOCS

DCV IJV

VPVA

VPVA

IJV R

L

Fig. 7.22 Veins of the cranio-vertebral junction. (a) Right lateral view of MR venography (3D contrast-enhanced TOF MRA). (b) Anterior–posterior view of MR venography. (c) Schematic of the veins of cranio-vertebral junction (right lateral view). (d) Schematic of the veins of the craniovertebral junction (anterior view of right half) (drawn based on studies by Caruso [9], Ruiz [43], Takahashi [49]). (a, b) The right internal jugular vein (IJV) is larger than the left in about 70% of cases. On the right side, the large anterior condylar vein (AC), posterior condylar emissary vein (PC), suboccipital cavernous sinus (SOCS), deep cervical vein (DCV) are seen. (c, d) Numerous variations exist in the venous structure of the cranio-vertebral junction. One of the typical types is shown here. The venous structure of the hypoglossal canal contains a venous plexus that connects the inferior petrosal sinus, condylar vein, internal jugular vein, paravertebral venous plexus, and anterior, posterior, lateral condylar emissary veins. The suboccipital cavernous sinus is the venous structure surrounding the horizontal portion of the third segment of the vertebral artery (VA), which extends from the transverse foramen of axis to the dural penetration by the VA. Due to the analogy to the cavernous sinus located in the parasellar region from the perspective of morphological and functional features, this suboccipital anatomical complex was called the “suboccipital cavernous sinus (SOCS)” in a microsurgical anatomical study by Arnautovic et al. [2]. ACC anterior condylar confluent; AC anterior condylar emissary vein; CvS cavernous sinus; DCV deep cervical vein; IJV internal jugular vein; IPS inferior petrosal sinus; LC lateral condylar emissary vein; MV mastoid emissary vein; MS marginal sinus; OV occipital emissary vein; OS occipital sinus; PC posterior condylar emissary vein; PVVP prevertebral venous plexus; SOCS suboccipital cavernous sinus; SJB superior jugular bulb; SPS superior petrosal sinus; SS sigmoid sinus; VA vertebral artery; VPVA venous plexus around vertebral artery

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7.3 Veins of the Cranio-Vertebral Junction (Fig. 7.22) Most of the cerebral venous drainage ultimately collects into the transverse and sigmoid sinuses, continuing to the internal jugular veins as seen on the venous phase of the cerebral angiography performed in a supine position. However, the internal and external vertebral venous systems have been noted to represent the major outflow of cerebral venous drainage in the erect position and outflow through the internal jugular veins is absent or negligible in this position [9, 12, 13, 43, 49]. Bilateral resection of the internal jugular vein is usually well tolerated, indicating an alternative pathway for the vertebral venous system including vertebral veins, which provide cerebral venous drainage in an erect position in monkeys [13]. Valdueza et al. [50] examined the postural dependence of cerebral venous outflow in human beings using color-coded duplex sonography. The internal jugular veins and vertebral veins were examined in the midcervical area to confirm the effect of body posture on blood flow and area of these veins. Measurements were taken with body elevations from 0 to 90°. Postural changes lead to gradual collapse of the internal jugular vein and a smaller contribution to the cerebral venous drainage. Reduction of the cross-sectional area of the internal jugular vein in the upright position has been postulated to occur as a physiological response to maintain cerebral venous blood flow and prevent overdrainage of cerebral blood. However, the increased vertebral venous flow and area are insufficient to compensate for the drop in jugular flow. Valdueza et al. [50] thought the spinal epidural veins were the most probable additional drainage pathways in the upright position. This accumulated evidence suggests that the vertebral venous plexus provides one of the major circulatory compensations allowing humans to remain conscious while sitting and standing. Furthermore, in the erect


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position, this plexus is likely to provide the compensating mechanisms by which cerebral blood drainage is maintained. Free connections with the dural sinuses and emissary veins of the skull, as well as the numerous junctions with the cervical venous plexus, allow blood to flow into the subclavian, axillary, and internal and external jugular veins [12]. Numerous normal variations in the venous structures of the cranio-vertebral junction exist. For example, the hypoglossal canal may contain a venous plexus that connects the inferior petrosal sinus, condylar vein, internal jugular vein, and paravertebral venous plexus. During neurosurgical intervention, particularly for dural arteriovenous fistula involving the hypoglossal canal, selective transvenous embolization is the most effective therapeutic method [36]. For that approach, knowledge of the normal variations of the cranio-vertebral junction is essential [2, 49].

References 1. Andrews BT, Dujnovny M, Mirchandani HG, Ausman JI. Microsurgical anatomy of the venous drainage into the superior sagittal sinus. Neurosurgery. 1989;24:514–20. 2. Arnautovic KI, Al-Mefty O, Pait TG, Krisht AF, Husain MM. The suboccipital cavernous sinus. J Neurosurg. 1997; 86:252–62. 3. Balo J. The dural venous sinuses. Anat Rec. 1950;106:319–25. 4. Bergquist E, Willén R. Cavernous nodules in the dural sinuses, an anatomical, angiographic, and morphological investigation. J Neurosurg. 1974;40:330–5. 5. Browder J, Browder A, Kaplan HA. Benign tumors of cerebral sinuses. J Neurosurg. 1972; 37:576–9. 6. Browder J, Browder A, Kaplan HA. Anatomical relationships of the cerebral and dural venous systems in parasagittal area. Anat Rec. 1973;176:329–32. 7. Browning H. The confluence of dural venous sinuses. Am J Anat. 1953;93:307–29. 8. Capra NF, Anderson KV. Anatomy of the cerebral venous system. In: Kappe JP, Schmidek HH, editors. The cerebral venous system and its disorders. Philadelphia: Grune and Stratton; 1984. p. 1–36. 9. Caruso RD, Rosenbaum AE, Chang JK, Joy SE. Craniocervical junction venous anatomy on enhanced MR images: the suboccipital cavernous sinus. AJNR Am J Neuroradiol. 1999; 20:1127–31. 10. Curé JK, Tassel PV, Smith MT. Normal and variant anatomy of the dural venous sinuses. Semin Ultrasound CT MRI. 1994;15:499–519. 11. Das AC, Hasen M. The occipital sinus. J Neurosurg. 1970;33:307–11. 12. Eckenhoff JE. Physiologic significance of the vertebral venous plexus. Surg Gynecol Obstet. 1970;131:72–7813. 13. Epstein HM, Linde HW, Crampton AR, Ciric IS, Eckenhoff JE. The vertebral venous plexus as a major cerebral venous outflow tract. Anesthesiology. 1970;32:332–7. 14. Fukusumi A, Okudera T, Nakagawa H, Taoka T, Takayama K, Uchida H, et al. Pathogenesis and imaging of medullary venous malformations in the basal ganglionic region (in Japanese). Jpn J Clin Radiol. 1999;44:1412–9. 15. Fukusumi A, Tanaka T, Koh S, Nakagawa H, Taoka T, Takayama K, et al. Anatomical variations of the torcular Herophili evaluated with MR venography (in Japanese). Jpn J Clin Radiol. 2002;47:625–31. 16. Gabella G. Cardiovascular system. In: Williams PL, editor. Gray’s anatomy. 38th ed. NewYork: Churchill Livingstone; 1995. p. 1580–9.

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17. Giudicelli G, Salamon G. The veins of the thalamus. Neuroradiology. 1970;1:92–8. 18. Gotoh N, Koda M. Blood vessels in the central nervous system [in Japanese]. In: Sato T, Akita K, editors. Anatomical variations in Japanese. Tokyo: University of Tokyo Press; 2000. p. 401–9. 19. Hacker H. Superficial sputa tentorial veins and dural sinuses. In: Newton TH, Potts DG, editors. Radiology of skull and brain: angiography, vol 2/book 3. Saint Louis: CV Mosby; 1974. p. 1851–902. 20. Haines DE, Harkey HL, Al-Mefty O. The subdural space: a new look at an out dated concept. Neuroradiology. 1993;32:111–20. 21. Huang YP. Basal cerebral vein, deep cerebral veins, veins of the posterior fossa. In: Salamon G, Huang YP, editors. Radiologic anatomy of the brain. Berlin: Springer; 1976. pp. 127–31, 210–64, 332–90. 22. Huang YP, Okudera T, Fukusumi A, Maehara F, Stollman AL, Mosesson R, et al. Venous architecture of cerebral hemispheric white matter and comments on pathogenesis of medullary venous and other cerebral vascular malformations. Mt Sinai J Med. 1997;64:197–206. 23. Huang YP, Wolf BS. Veins of the white matter of the cerebral hemispheres (the medullary veins). Am J Roentogenol Radium Ther Nucl Med. 1964;92:739–55. 24. Huber P. Cerebral veins, cerebral veins, dural sinuses. In: Huber P, editor. Cerebral angiography. Stuttgart: George Thieme; 1982. pp. 185–221, 221–39. 25. Itoh J. Supratentorial venous system. In: Maki U, Kuru Y, editors. Neuroradiology I. Tokyo: Asakura Shoten; 1979. p. 443–84. 26. Kaplan HA, Browder A, Browder J. Atresia of rostral superior sagittal sinus: associated cerebral venous patterns. Neuroradiology. 1972;4:208–11. 27. Kaplan HA, Browder A, Brower J. Narrow and atretic transverse dural sinuses: clinical significance. Ann Otolaryngol. 1973;82:351–4. 28. Kaplan HA, Browder J, Howard EM, Browder A. Vascular spaces of the middorsal dura mater. Arch Pathol. 1974;97:173–7. 29. Knott JF. On the cerebral sinuses and their variations. J Anat Phys. 1882;16:27–42. 30. Kryayenbühl H, Yaşargil YG, editors. The cerebral veins. In: Cerebral angiography. London: Butterworths; 1968. p. 89 31. Lemay M. Left-right dissymmetry, handedness. AJNR Am J Neuroradiol. 1992;13:493–504. 32. MatsushimaT RAL, Lenkey C. Microsurgery of the fourth ventricle: part I, microsurgical anatomy. Neurosurgery. 1982;11:631–67. 33. McCord GM, Goree JA, Jimenez P. Venous drainage to the inferior sagittal sinus. Radiology. 1972;105:583–9. 34. Miller DL, Doppman JL. Petrosal sinus sampling: technique and rationale. Radiology. 1991; 178:37–47. 35. Oka K, Rhoton AL Jr, Barry M, Rodriguez R. Microsurgical anatomy of the superficial veins of the cerebrum. Neurosurgery. 1985;17:711–48. 36. Okahara M, Kiyosue H, Tanoue S, Sagara Y, Tori Y, Kashiwagi J, et al. Selective transvenous embolization of dural arteriovenous fistulas involving the hypoglossal canal. Interv Neuroradiol. 2007;13:59–66. 37. Okudera T, Huang YP, Fukusumi A, Maehara F. Venous architecture of the basal ganglia with a view toward their venous malformations. In: Bigot JM, Moreau JF, Nahum H, Bellet H, editors. Radiology. International Congress of Radiology. Paris: Elsevier; 1990. pp. 553–61. 38. Okudera T, Huang YP, Fukusumi A, Nakamura Y, Hatajawa J, Uemura K. Micro-angiographical studies of the medullary venous system of the cerebral hemisphere. Neuropathology. 1999; 19:93–111. 39. Okudera T, Huang YP, Ohta T, Yokota A, Nakamura Y, Maehara F, et al. Development of posterior fossa dural sinuses, emissary veins, and jugular bulb: Morphological and radiologic study. AJNR Am J Neuroradiol. 1994;15:1871–83.


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40. Okudera T, Maehara F, Nakamura Y, Utsunomiya H, Ogasawara T, Hayashi T. Radiologic anatomy of the vascularization of the thalamus (in Japanese). Ther Hypertens Cereb Hemorrhage. 1988;3:3–16. 41. Osborn A. Normal vascular anatomy. In: Osborn A, editor. Diagnostic neuroradiology. St Louis: Mosby; 1994. p. 145–53. 42. Riley HA. An atlas of the basal ganglia, brainstem and spinal cord -based on myelin-stained material- 2nd edn. New York: Hafner; 1960. p. 241–318. 43. Ruíz DSM, Philippe G, Rufennacht DA, Delavelle J, Henry F, Fasel JHD. The craniovertebral venous system in relation to cerebral venous drainage. AJNR Am J Neuroradiol. 2002;23: 1500–8. 44. Schlesinger B. The venous drainage of the brain with special reference to the Galenic system. Brain. 1939;62:274–91. 45. Seidenwurm D, Berenstein A, Hyman A, Kowalski H. Vein of Galen malformation: correlation of clinical presentation, arteriography and MR imaging. AJNR Am J Neuroradiol. 1991;12:347–54. 46. Shiu PC, Hanafee WN, Wilson GH. Cavernous sinus venography. Am J Roentogenol Radium Ther Nucl Med. 1968;104:57–62. 47. Strub WM, Leach SJ, Tomsick TA. Persistent falcine sinus in an adult: demonstration by MR venography. AJNR Am J Neuroradiol. 2005;26:750–1. 48. Susa Y. Pattern of the torcular herophili, measurement of sinus lumen and histology of sinus wall (in Japanese). J Nippon Medical School. 1950;27:247–63. 49. Takahashi S, Sakuma I, Omachi K, Otani T, Tomura N, Watarai J, et al. Craniocervical junction venous anatomy around the suboccipital cavernous sinus: evaluation by MR imaging. Eur Radiol. 2005;15:1694–700. 50. Valdueza JM, von Munster T, Hoffman O, Schreiber S, Einhaupl KM. Postural dependency of the cerebral venous outflow. Lancet. 2000;355:200–1. 51. Wolf BS, Huang YP, Newmann CM. The lateral anastomotic mesencephalic vein and other variations in drainage of the basal cerebral vein. Am J Roentogenol Radium Ther Nucl Med. 1963;89:411–22. 52. Virapongse C, Cazenave C, Quisling R, Sarwar M, Hunter S. The empty delta sign: frequency and significance in 76 cases of dural sinus thrombosis. Radiology. 1987;162:779–85. 53. Wolf BS, Huang YP. The subependymal vein of the lateral ventricle. Am J Roentogenol Radium Ther Nucl Med. 1964;91:406–26. 54. Zimmerman RD, Ernst RJ. Neuroimaging of cerebral venous thrombosis. Neuroimaging Clin North Am. 1992;2:463–85. 55. Zouaoui A. Cerebral venous sinuses: anatomical variants or thrombosis? Acta Anat (Basel). 1988;133:318–24.

Mapping Superficial Cerebral Veins on the Brain Surface

8

Shuichi Higano

8.1 Introduction In brain surgery with craniotomy, superficial cerebral veins and venous sinuses can be important landmarks. The neurosurgeon’s preoperative knowledge of the relationship between cerebral gyri/sulci and venous structures and lesions or intended portion of corticotomy from images showing these structures could facilitate surgical planning and operative approach to lesions and avoid injury of venous structures. Such damage could abruptly impair cerebral venous drainage and cause venous infarction and/or associated hemorrhage.

8.2 MR Imaging Techniques Two imaging methods have been proposed that delineate both superficial veins and the brain surface. One is a fusion method that superimposes magnetic resonance (MR) venography on a surface anatomy scanning (SAS) image [5–7], and the other is a rendering method derived from three-dimensional (3D) T1-weighted images [1, 3, 4].

8.2.1 Fusion Method Fusion images are obtained by superimposing MR venography on images obtained by SAS (Fig. 8.1e), a noninvasive MR technique that reveals surface structures of the brain (Fig. 8.1c) [2]. The original method involves acquisition of a thick-slice, two-dimensional

S. Higano Department of Diagnostic Radiology, Tohoku University Graduate School of Medicine, Sendai, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_8, © Springer-Verlag London Limited 2010

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Fig. 8.1 A 44-year-old woman with right medial frontal oligodendroglioma found incidentally. No neurological deficit was noted. (a) Axial T1-weighted image; (b) axial fluid attenuation inversion recovery (FLAIR) image; (c) surface anatomy scanning (SAS) image from the anterosuperior view; (d) magnetic resonance (MR) venography image identical to SAS image (c); (e) fusion image superimposing MR venography on the SAS image; (f) brain surface image obtained by volume-rendering (VR) method as viewed from above; (g) photograph of the brain surface at the operation window (courtesy of Dr. Kumabe, Department of Neurosurgery, Tohoku University Graduate School of Medicine); (h) magnification of image (f). Conventional MR images (a, b) show a swollen medial aspect of the right superior frontal gyrus with T2-elongation. No contrast enhancement is noted. Fusion image (e) is obtained by superimposing 3-dimensional (3D) phasecontrast (PC) MR venography (d) on SAS image (c), which is derived from partial maximum intensity projection (MIP) of a 3D heavily T2-weighted constructive interference in steady-state image in this case. MR venography delineates not only superficial cortical veins but also deep branches of the anterior cerebral arteries and branches of the external carotid artery (d, e, large arrows). The tumor is not so well identified, showing just slight gyral swelling on the SAS and fusion images (c, e, small arrows). The brain surface image by rendering method (f, h) reconstructed from contrast-enhanced magnetization prepared rapid gradient-echo (MP-RAGE) images better delineates the sulci/gyri and cortical veins, which correlates well with the operation view (g). The tumor shows a faint ill-defined area of low signal on this image (f, arrow)

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(2D), heavily T2-weighted image using long repetition (TR) and echo time (TE) spin echo (SE) sequence, which is then displayed with gray-scale reversal in postprocessing. As the conventional long TR SE imaging requires relatively long acquisition time, half-Fourier technique such as half-Fourier single-shot turbo spin-echo (HASTE) and fast SE method has been more commonly used [8]. To demonstrate brain surface structures and superficial cerebral veins simultaneously, Tsuchiya et al. proposed combining SAS images and MR venography. They obtained SAS images with HASTE, then 2D phase-contrast (PC)

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MR venography of identical sections, and added the two sets of images [5–7]. They reported good correlation comparing these images with surgical findings. The fusion method has some limitations. Two-dimensional acquisition fixes image visualization in one direction. To overcome this limitation, both SAS images and MR venography may be obtained with 3D acquisition. Actually, SAS images can be reconstructed to be viewed from different directions by partial maximum intensity projection (MIP) of 3D heavily T2-weighted images, such as constructive interference in steady-state (CISS) or fast imaging with steady-state acquisition (FIESTA) images. MR venography can be obtained using 3D PC technique (Fig. 8.1d), but these 3D acquisition requires longer scan time. The PC method can delineate deep vessels and extracranial vessels, such as branches of the external carotid artery, as well as superficial veins (Fig. 8.1d). A final limitation is that movement of the patient’s head between SAS and MR venography acquisition could cause misregistration of the fused sets.

8.2.2 Rendering Method A surface image can be obtained by removing the skull and scalp from the volumerendering (VR) image of 3D contrast-enhanced T1-weighted images, such as magnetization prepared rapid gradient-echo (MP-RAGE), 3D-spoiled gradient-recalled (SPGR), and 3D T1-fast field-echo (FFE) images. Because cerebral vessels show high signal intensity on source images with contrast enhancement, the VR images can simultaneously demonstrate brain surface structures (gyri and sulci) and cortical veins without fusion. If a lesion on the brain surface, such as a tumor, shows contrast enhancement, it can be visualized simultaneously with high intensity on the surface image. There is no problem of misregistration or contamination of vessels in the depth or on the scalp. Because surface images are derived from 3D source images, the images can be rotated easily on the workstation and viewed from the desired direction. However, this method may be limited by the complexity of removing the skull and scalp [3], a process that might be performed semiautomatically using a more advanced workstation, an option not available in most institutions. Gong et al. recently proposed a simple way to cut off the skull and scalp [1] manually along the signal void band representing the inner table of the skull, which separates the brain surface from the skull (Figs. 8.2 and 8.3). Good anatomical correlation between the rendered brain surface image and operative views has been reported [1, 4]; Gong et al. detected all superficial cerebral veins larger than 2 mm in diameter, 89% of those 1–2 mm, and 56.9% of those 0.5–1 mm [1]. Visualization of the brain surface structures or cortical veins may be affected by effacement of cerebral sulci from brain swelling, dural/meningeal contrast enhancement, or insufficient spatial resolution of source images [1, 4] (Fig. 8.3).

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Fig. 8.2 A 34-year-old man with right parietal glioblastoma, presented with convulsion. (a) Axial T2-weighted image; (b) axial contrast-enhanced T1-weighted image; (c) coronal contrast-enhanced T1-weighted image; (d) brain surface image obtained by VR method, in a projection as viewed from above with slight rightward obliquity; (e) magnified view of the brain surface image corresponding to the operation window (g); (f) the same image as (e) with different window setting; (g) photograph of the brain surface at the operation window (courtesy of Dr. Sonoda, Department of Neurosurgery, Tohoku University Graduate School of Medicine). Conventional MR images (a–c) show an inhomogeneously enhancing nodular tumor with perifocal edema in the subcortical region of the right middle frontal gyrus (a–c). Brain surface images (d–f) clearly demonstrate the enhancing tumor with the surrounding sulci/gyri and cortical veins. The image is well correlated with the operation view (g). The extension of the enhancing tumor deep into the surface can be seen in the surface image with altered window setting (f)

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Fig. 8.3 A 13-year-old boy with right parietal pleomorphic xanthoastrocytoma seen for headache, nausea, and disturbance of the visual field. (a) Axial T2-weighted image; (b) axial contrastenhanced T1-weighted image; (c) coronal contrast-enhanced T1-weighted image; (d) magnified view of the brain surface image corresponding to the operation window (f); (e) same image as (e) with altered window setting; (f) photograph of the brain surface at the operation window (courtesy of Dr. Kumabe, Department of Neurosurgery, Tohoku University Graduate School of Medicine). Conventional magnetic resonance (MR) images (a–c) reveal a well demarcated nodular tumor (large arrow) with strong contrast enhancement associated with a cystic component (small arrows) in the depth of the nodule. Brain surface images (d, e) clearly demonstrate the enhancing tumor and superficial cerebral veins. However, the gyri/sulci around the lesion are not so well visualized, probably due to brain swelling with the superficial subarachnoid space squeezed over the surface. Subcortical tumor extension and the associated cystic component can be demonstrated by changing window setting of the rendered brain surface image (e). The findings of the brain surface images correlate well with the operative view (f). The same numbers in (d) and (e) represent vessels corresponding with each other

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References 1. Gong XY, Higano S, Mugikura S, Umetsu A, Murata T, Kumabe T, et al. Virtually peeling off the skull and scalp: a simple way of mapping the superficial cerebral veins on the brain surface. Stereotact Funct Neurosurg. 2008;86:345–50. 2. Katada K. MR imaging of brain surface structures: surface anatomy scanning (SAS). Neuroradiology. 1990;32:439–48. 3. Narita K, Sasaki M, Sakurada W, Shimizu H, Miura H, Tomura N. Usefulness of three-dimensional MR images of brain tumors for surgical simulation. Nippon Hoshasen Gijutsu Gakkai Zasshi. 2002;58:1632–8 [Article in Japanese]. 4. Narita K, Tomura N, Sasajima T, Sakuma I, Sakurada W, Sasaki M, et al. Three-dimensional surface anatomical scanning with 3D-FSPGR: anatomical conformity with surgical findings. Nippon Hoshasen Gijutsu Gakkai Zasshi. 2005;61:1341–8 [Article in Japanese]. 5. Tsuchiya K, Hachiya J, Hiyama T, Maehara T. A new MRI technique for demonstrating the surface of the brain together with the cortical veins. Neuroradiology. 1999;41:425–7. 6. Tsuchiya K, Hachiya J, Hiyama T, Maehara T, Kassai Y. Combination of surface anatomy MRI and MR venography to demonstrate cerebral cortex and cortical veins on one image. J Comput Assist Tomogr. 1998;22:972–5. 7. Tsuchiya K, Katase S, Hachiya J, Hiyama T, Shiokawa Y. A new technique of surface anatomy MR scanning of the brain: its application to scalp incision planning. AJNR Am J Neuroradiol. 1999;20:515–8. 8. Tsuchiya K, Mizutani Y, Hachiya J. Surface anatomy MR scanning of the brain using HASTE sequences. AJR Am J Roentgenol. 1996;167:1585–7.

Part II Neurovascular Imaging in Pathology

Preoperative Visualization of the Lenticulostriate Arteries Associated with Insulo-Opercular Gliomas Using 3-T Magnetic Resonance Imaging

9

Toshihiro Kumabe, Ryuta Saito, Masayuki Kanamori, Yukihiko Sonoda, Shuichi Higano, Shoki Takahashi, and Teiji Tominaga

Abbreviations 3D CT LSA MR

3-Dimensional Computed tomography Lenticulostriate artery Magnetic resonance

9.1 Introduction Improving the extent of resection and reducing the risk of neurological complications are important goals in the treatment of insulo-opercular gliomas [1–5, 10–13]. Aggressive surgical resection of intrinsic insular gliomas is associated with high rates of gross total resection and low rates of permanent neurological deficits and requires meticulous surgical approach based on the regional insular anatomy [1–5, 8–13]. Interruption of the perforating lenticulostriate arteries (LSA) and long insular arteries that arise from the M2 [8] can damage the descending motor pathways [7] and cause postoperative hemiplegia [4]. Therefore, preservation of the perforating arteries is of utmost importance during surgical resection of insulo-opercular tumors [2, 4, 5, 8].

T. Kumabe (*) Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_9, © Springer-Verlag London Limited 2010

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We discuss the preoperative use of 3-dimensional (3D) high-field (3-tesla [T]) T1weighted magnetic resonance (MR) imaging with contrast enhancement to delineate the LSA and their relationships with insular tumors and demonstrate the clinical uses of the images in determining surgical indications and planning of radical resection of intrinsic insular tumors.

9.2 Three-Dimensional MR Imaging We performed 3D MR imaging with a 3-T scanner (Philips Intera Achieva 3.0-T Quasar Dual; Philips Healthcare Best the Netherlands) using an 8-channel sensitivity-encoding (SENSE) head coil. To delineate the perforating arteries, we administered standard doses (0.2 mL/kg) of gadolinium-based contrast medium, then obtained 3D T1-weighted fastfield-echo sequence employing the following parameters: repetition time, 35 ms; echo time, 2.6 ms; flip angle, 24°; field of view, 20 cm; matrix, 784 × 263; slice thickness, 0.4 mm; and number of slices, 170. For postprocessing, we utilized open-source OsiriX imaging software (Version 2.7.5; free download from http://www.osirix-viewer.com/) running on an Apple Macintosh MacBook Pro (Apple Inc., Cupertino, CA) to transform images into cine images (QuickTime; Apple Inc.). We observed the cine mode images and visually identified enhanced spots in the corpus striatum as LSA based on the known anatomy of these vessels.

9.3 Representative Cases 9.3.1 Case 1 In 1999, a 23-year-old woman lost consciousness for about 5 min with generalized clonic convulsion. She was diagnosed with a right insulo-opercular glioma at a local hospital and referred to our hospital for treatment (Fig. 9.1a). On admission, no neurological deficits were observed. Cerebral angiography demonstrated only the mass effect of the tumor. The LSA were compressed medio-posteriorly, but the tumor border was difficult to clarify (Fig. 9.2). At surgery, the tumor was gelatinous, and the tumor border was relatively easy to define under the operative microscope. Gross total resection of the tumor was performed with preservation of the LSA, which were found to run just inside the tumor (Fig. 9.1b). The histological diagnosis was anaplastic astrocytoma. Her postoperative course was uneventful, and postoperative 3D computed tomographic (CT) angiography showed several LSA running inside the resection cavity (Fig. 9.3). She received adjuvant chemoradiation therapy and for 10 years has continued life without recurrence as before

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Fig. 9.1 Case 1. (a) Preoperative axial T1-weighted magnetic resonance (MR) image with contrast enhancement shows a relatively sharp tumor-brain interface, which is one of the prerequisites for gross total removal of insulo-opercular tumors. (b) Postoperative axial T1-weighted MR image shows gross total resection of the tumor

Fig. 9.2 Case 1. Preoperative right internal carotid angiogram demonstrates an avascular tumor compressing the lenticulostriate arteries medio-posteriorly (arrows), but the tumor-brain relationship is not clear

298 Fig. 9.3 Case 1. Postoperative (a) coronal and (b) sagittal maximumintensity-projection 3-dimensional (3D) computed tomographic angiograms show the lenticulostriate arteries running inside the resection cavity (arrows)

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Fig. 9.4 Case 1. Postoperative (a) coronal and (b) sagittal 3D 3-T T1-weighted MR images with contrast enhancement clearly depict the lenticulostriate arteries branching from the middle cerebral artery. The colors (yellow, green, red, and cyan) of the arrows correspond to the coronal and sagittal images

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symptom onset. Recent 3-T MR imaging disclosed LSA at the medial border of the resection cavity (Figs. 9.4 and 9.5). Image quality of the vessels was better by 3-T MR imaging than by 3D CT angiography, and each of the LSA was traceable on axial, coronal, and sagittal MR images.


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Fig. 9.5 Case 1. Postoperative axial 3D 3-T T1-weighted MR images with contrast enhancement clearly depict the lenticulostriate arteries running at the medial aspect of the resection cavity. The colors (yellow, green, red, and cyan) of the arrows correspond to the arrows in Fig. 9.4. The white arrow indicates the origin of the lenticulostriate arteries

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Fig. 9.6 Case 2. (a) Preoperative and (b) postoperative axial T1-weighted MR images with contrast enhancement show a relatively sharp tumor-brain interface, which enabled gross total resection with preservation of the perforating arteries

9.3.2 Case 2 A 29-year-old woman complained of repetitive transient vertigo and paresthesia of the right extremities. She was diagnosed with left insular glioma at a local hospital and referred to our hospital for treatment (Fig. 9.6a). On admission, no neurological deficits were

300 Fig. 9.7 Case 2. Preoperative (a) coronal and (b) sagittal 3D 3-T T1-weighted MR images with contrast enhancement clearly depict the lenticulostriate arteries branching from the middle cerebral artery. The colors (yellow, orange, red, and magenta) of the arrows correspond to the images

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detected. Three-tesla MR imaging demonstrated the sharp tumor-brain border without encasement of the LSA (Figs. 9.7 and 9.8). The tumor was gelatinous, and its border was relatively easy to define under the operative microscope. Gross total removal of the tumor was performed (Fig. 9.6b). The histological diagnosis was ganglioglioma. She continued her previous life without complications for 2 years. Postoperative 3-T MR imaging revealed preservation of all LSA at the medial aspect of the resection cavity (Fig. 9.9).

9.4 Discussion Preoperative detection of LSA can be very useful in identifying optimal surgical candidates. Cerebral angiography, 3D CT angiography, and MR imaging have been used to visualize LSA, and only cerebral angiography was unable to demonstrate the relationship between the tumor border and LSA, as in our Case 1. Recently, superimposition of tumor volumes defined by preoperative MR imaging onto stereotactic cerebral angiograms (COMPASS Stereotactic System; Compass International Inc., Rochester, MN) could determine whether an insular tumor was located only lateral to or extended medially around the LSA [5]. Since 1992, helical CT technology has developed a new imaging technique for depicting cerebral vascular circulation [6], and the usefulness of 3D CT angiography has been recognized for evaluating vascular structures. However, MR imaging gives more clear and detailed information about tumors, surrounding brain, and their interface (Figs. 9.3–9.5) and should therefore be more useful than CT if its delineation of the vasculature can be improved.


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Fig. 9.8 Case 2. Preoperative axial 3D 3-T T1-weighted MR images with contrast enhancement clearly depict the lenticulostriate arteries running on the medial surface of the tumor. The colors (blue, cyan, green, yellow, magenta, brown, red, and orange) of the arrows correspond to the images and with the arrows in Fig. 9.7

Three-tesla MR imaging is now widely available for clinical use and is superior to 1.5-T imaging; doubled signal-to-noise ratio improves image quality, and more efficient contrast enhancement enables far superior delineation of vessels and tumors. The present and previous studies suggest that a sharp tumor-brain border without encasement of the LSA is a prerequisite for gross total removal of insulo-opercular tumors [2, 4]. In our second case, 3D, 3-T, T1-weighted imaging with contrast enhancement clearly demonstrated theLSA at the anteromedial aspect of the tumor preoperatively and showed the tumorbrain interface to be relatively sharp. Thus, by delineating the tumor-brain interface well and providing noninvasive accurate information about the LSA, 3-T MR imaging enables total resection of insular tumors with preservation of these vessels. Preoperative 3-T MR imaging can promote maximum resection of tumors in the insulo-opercular regions without neurological complications, and the same DICOM data can be utilized for intraoperative neuronavigation.

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Fig. 9.9 Case 2. Postoperative axial 3D 3-T T1-weighted MR images with contrast enhancement clearly depict the lenticulostriate arteries running at the medial aspect of the resection cavity. The colors (blue, cyan, green, yellow, magenta, brown, red, and orange) of the arrows correspond to the images and with the arrows in Figs. 9.7 and 9.8

9.5 Conclusions Preservation of LSA is one of the most important factors for avoiding complications during aggressive resection of insulo-opercular gliomas. 3D 3-T MR imaging with contrast enhancement can visualize LSA, improve the extent of resection, and reduce neurological risk.

References 1. Duffau H, Capelle L, Lopes M, Faillot T, Sichez JP, Fohanno D. The insular lobe: physiopathological and surgical considerations. Neurosurgery. 2000;47:801–10. 2. Hentschel SJ, Lang FF. Surgical resection of intrinsic insular tumors. Neurosurgery. 2005;57 (1 Suppl):176–83. 3. Kumabe T, Nakasato N, Suzuki K, Sato K, Sonoda Y, Kawagishi J, et al. Two-staged resection of a left frontal astrocytoma involving the operculum and insula using intraoperative neurophysiological monitoring−case report. Neurol Med Chir (Tokyo). 1998;38:503–7.


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4. Lang FF, Olansen NE, DeMonte F, Gokaslan ZL, Holland EC, Kalhorn C, et al. Surgical resection of intrinsic insular tumors: complication avoidance. J Neurosurg. 2001;95:638–50. 5. Moshel YA, Marcus JD, Parker EC, Kelly PJ. Resection of insular gliomas: the importance of lenticulostriate artery position. J Neurosurg. 2008;109:825–34. 6. Napel S, Marks MP, Rubin GD, Dake MD, McDonnell CH, Song SM, et al. CT angiography with spiral CT and maximum intensity projection. Radiology. 1992;185:607–10. 7. Takahashi S, Goto K, Fukasawa H, Kawata Y, Uemura K, Suzuki K. Computed tomography of cerebral infarction along the distribution of the basal perforating arteries. Part I: Striate arterial group. Radiology. 1985;155:107–18. 8. Türe U, Yaşargil MG, Al-Mefty O, Yaşargil DC. Arteries of the insula. J Neurosurg. 2000;92: 676–87. 9. Türe U, Yaşargil DC, Al-Mefty O, Yaşargil MG. Topographic anatomy of the insular region. J Neurosurg. 1999;90:720–33. 10. Vanaclocha V, Sáiz-Sapena N, García-Casasola C. Surgical treatment of insular gliomas. Acta Neurochir (Wien). 1997;139:1126–35. 11. Varnavas GG, Grand W. The insular cortex: morphological and vascular anatomic characteristics. Neurosurgery. 1999;44:127–36. 12. Yaşargil MG, von Ammon K, Cavazos E, Doczi T, Reeves JD, Roth P. Tumours of the limbic and paralimbic systems. Acta Neurochir (Wien). 1992;118:40–52. 13. Zentner J, Meyer B, Stangl A, Schramm J. Intrinsic tumors of the insula: a prospective surgical study of 30 patients. J Neurosurg. 1996;85:263–71.

Ischemic Complications Associated with Resection of Opercular Gliomas

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Toshihiro Kumabe, Masayuki Kanamori, Ryuta Saito, Ken-ichi Nagamatsu, Yukihiko Sonoda, Shuichi Higano, Shoki Takahashi, and Teiji Tominaga

10.1 Introduction Recent advanced methods that include neurophysiological brain mapping and monitoring techniques [1–4, 13], use of neuronavigation systems, and intraoperative magnetic resonance (MR) imaging [5, 6, 9, 11] enable total resection of gliomas in the frontoparietal opercular region inferolateral to the hand-digit sensorimotor area. Such procedures have been developed to prevent direct damage to the eloquent cortices and corticospinal tract, but potential damage to the blood supply to the corona radiata from therapeutic procedures and the resultant ischemic complications are little understood. Postoperative diffusion-weighted (DW) MR imaging can be used to identify ischemic complications after glioma resection [14] and can detect restricted diffusion abnormalities after resection in 64% of newly diagnosed gliomas. We reported that immediate postoperative MR imaging that included DW imaging disclosed infarct lesions in all of 11 patients treated for opercular gliomas. In addition, in 3 patients, disruption of the blood supply during surgery produced unexpected extension of the infarct lesions to the descending motor pathway in the corona radiata, which may have impaired long tract functions [7]. Here, we again caution surgeons that resection of opercular glioma can cause mild or severe ischemic complications in the corona radiata.

10.2 Microangiographic Analysis of Vascular Supply to the Corona Radiata In coronal and axial microangiograms of cadaver brains without gross brain pathology, we examined the pial cortical arteries in and around the insulo-opercular region to identify the blood supply to the corona radiata; the reviewed images were taken from

T. Kumabe (*) Departments of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_10, © Springer-Verlag London Limited 2010

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Fig. 10.1 Coronal microangiograms of a cadaver brain through the interventricular foramina. Both the long insular arteries (arrows) that arise from the insular portions of the middle cerebral artery (MCA) and the medullary arteries from the opercular and cortical portions of the MCA as well as the lateral lenticulostriate arteries (LSA) (arrowhead) supply the region of the corona radiata

microangiographic studies of basal perforating artery distribution reported by one of the coauthors in 1985 [15, 16]. Coronal microangiograms showed that the long insular artery and the long medullary arteries from both the opercular and cortical segments of the middle cerebral artery (MCA) that pass over the frontoparietal operculum contribute to supply the corona radiata. The lateral lenticulostriate arteries (LSA supply the adjacent upper part of the posterior limb of the internal capsule (Fig. 10.1). Axial microangiograms showed supply of the corona radiata by many medullary arteries from the MCA (Fig. 10.2). These findings indicate that surgical resection of opercular glioma, even if the insula is not involved, could sacrifice the long insular arteries and the medullary arteries from the opercular and cortical segments of the MCA and finally cause cerebral infarction of the corona radiata.

10.3 MR Imaging Studies We performed preoperative, postoperative, and subsequent follow-up MR imaging using a 1.5-tesla system and conducted postoperative imaging within 72 h of surgery. We obtained T1-weighted images before and after gadolinium administration, T2-weighted images, and

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Fig. 10.2 Axial microangiograms of a cadaver. The medullary arteries (arrows) from the opercular and cortical portions of the MCA course toward the ventricle wall and supply the region of the corona radiata

DW images during the same imaging session without repositioning the patient’s head. Axial DW images were obtained using fat-suppressed, spin echo–echo planar imaging (repetition time, 5,000 ms; echo time, 72 ms; two excitations; slice thickness, 6 mm; gap, 2 mm; matrix, 128 × 128; and field of view, 23 cm2) with three orthogonal directional motion-probing gradients (b = 1,000 s/mm2). Three-dimensional (3D) time-of-flight (TOF) MR imaging was obtained in selected cases using a 3-tesla scanner (Philips Intera Achieva 3.0-T Quasar Dual; Philips Healthcare, Best, The Netherlands) and an 8-channel sensitivity-encoding (SENSE) head coil to identify the perforating arteries. We also acquired 3D T1-weighted fast field echo sequence images after administering the standard dose (0.2 mL/kg) of gadolinium-based contrast medium using the following parameters: repetition time, 35 ms; echo time, 2.6 ms; flip angle, 24°; field of view, 20 cm; matrix, 784 × 263; slice thickness, 0.4 mm; and 170 slices. We postprocessed images on an Apple Macintosh MacBook Pro (Apple, Inc., Cupertino, CA) running OS X and open-source OsiriX imaging software (Version 2.7.5; free download from http://www.osirix-viewer.com/) and carried out transformation into cine images using QuickTime (Apple Inc.). In cine mode, we visually identified highly intense vascular structures in the deep white matter that we considered to represent the LSA and long insular arteries. Although the long insular arteries were still difficult to visualize, even with this high resolution, the assumed long insular arteries could be visualized in some patients with opercular glioma (Fig. 10.3).

308 Fig. 10.3 A 63-year-old man with right frontoparietal anaplastic oligodendroglioma. (a) Preoperative coronal T1-weighted magnetic resonance (MR) image with gadolinium demonstrating heterogeneously enhanced diffuse infiltrative right opercular tumor. (b) Three-tesla 3-dimensional time-of-flight (TOF) coronal MR image depicting the lateral LSA (arrowhead) and presumably the long insular arteries (arrows) medially displaced by the tumor

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10.4 Ischemic Complications Associated with Resection of Opercular Gliomas 10.4.1 Clinical Materials In patients with gliomas in the opercular region around the orofacial primary motor and somatosensory cortices that involved neither the hand-digit area nor the insula, we performed maximum tumor resection using an ultrasonic surgical aspirator (Sonopet; Miwatec Co., Ltd., Tokyo), intraoperative neurophysiological mapping techniques [1–4, 13], and guidance from a neuronavigation system. We carefully dissected and preserved all opercular arteries, and if the tumor infiltrated to the sylvian fissure, we first thoroughly dissected the affected sylvian fissure to identify and preserve the insular and opercular segments of the MCA.


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10.4.2 Representative Cases 10.4.2.1 Case 1 A 69-year-old woman presented with glioblastoma that manifested as left facial seizures followed by left hemiconvulsion. T1-weighted MR imaging with contrast enhancement demonstrated an enhanced mass lesion in the right tongue-to-face primary motor and somatosensory cortices that involved neither the hand-digit area nor the insula (Fig. 10.4a). Neurological and neuropsychological examination revealed no abnormality.

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Fig. 10.4 Case 1. A 69-year-old woman with a right frontoparietal glioblastoma. (a) Preoperative axial T1-weighted MR image with gadolinium demonstrating an irregularly enhanced mass lesion in the opercular region around the central sulcus (arrow). (b) Immediately postoperative axial T2-weighted MR image depicting total removal of the tumor and a new high intensity lesion (arrow) beneath the resection cavity. (c) Immediately postoperative axial (left) and coronal (right) diffusion-weighted (DW) MR images revealing the new lesion (arrows) beneath the resection cavity with reduced diffusion that probably involves the corticospinal tract

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She underwent right frontoparietotemporal craniotomy under general anesthesia. We identified the hand-digit motor area using direct cortical stimulation, thoroughly dissected the sylvian fissure toward the distal end, and exposed the insular surface under the operating microscope. We separated the precentral, central, and anterior parietal arteries from the tumor and preserved them, then resected the lower portion of the tumor toward the deepest portion using the upper limiting sulcus as the anatomical landmark and the information from a neuronavigation system, and removed the tumor stepwise with monitoring of muscle contraction by direct cortical stimulation to the hand-digit motor area (Fig. 10.5). The positive cortical response gradually weakened at the end of the surgery. Postoperatively, almost complete left hemiparesis was observed. MR imaging immediately after surgery showed resection of most of the enhanced lesion, (Fig. 10.4b.) with a remaining ischemic area beneath the resection cavity that involved the descending motor pathway (Fig. 10.4c, d). She did not recover from the left hemiparesis.

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Fig. 10.5 Case 1. Intraoperative photographs and schematic drawing. (a) Intraoperative view before resection with the results of functional brain mapping (1, 2, hand-digit motor). (b) Intraoperative view after tumor resection with preservation of the precentral, central, and anterior parietal arteries. (c) Schematic drawing. The continuous black line indicates the area of craniotomy and the white line, the location of the tumor (resected area in b). Arrows central sulcus; arrowheads sylvian fissure

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10.4.2.2 Case 2 A 53-year-old man presented with anaplastic astrocytoma that manifested as right facial seizures. T2-weighted MR imaging demonstrated a hyperintense lesion in the left opercular portions of the inferior frontal and pre- and postcentral gyri inferolateral to the precentral knob that did not involve the insula (Fig. 10.6a). Administration of contrast medium caused slight heterogeneous enhancement. Neurological and neuropsychological examination revealed no abnormality. The patient underwent left frontoparietotemporal craniotomy when he was awake, which was maintained until tumor removal was completed. Using a neuronavigation system, we inserted a silicone tube into the medial deepest portion to act as a fence post before opening the dura mater [19] (Fig. 10.7a). We identified the motor area of the hand-digit and tongue and the primary sensory sites of the tongue and thumb using direct cortical stimulation, localized speech arrest to the inferior frontal gyrus, anterior to the tumor border and the superior temporal gyrus (Fig. 10.7a), thoroughly dissected the sylvian fissure toward

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Fig. 10.6 Case 2. A 53-year-old man with left frontoparietal anaplastic astrocytoma. (a) Preoperative axial T2-weighted MR images showing a high intensity mass in the left frontoparietal opercular region. (b) Postoperative axial T2-weighted MR images demonstrating gross total resection of the tumor and a new high intensity lesion (arrows) beneath the resection cavity. (c) Postoperative axial DW MR images depicting the new lesion (arrows) with reduced diffusion involving the corona radiata

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the distal end, and exposed the insular surface under the operating microscope. With neuronavigational assistance, we separated and preserved the precentral and central arteries from the tumor and totally removed the tumor up to the motor and sensory area of the tongue and toward the deepest portion using the upper limiting sulcus and the inserted tube as landmarks (Fig. 10.7b). The patient’s motor functions were maintained without interruption until the end of tumor resection. Postoperatively, slight right facial palsy and dysarthria were observed. MR imaging showed the entire lesion was resected but revealed an ischemic area beneath the resection cavity within the corona radiata (Fig. 10.6b, c). Adjuvant therapy consisted of 72 Gy of hyperfractionated radiation to the extended local field. Nimustine hydrochloride (ACNU)

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Fig. 10.7 Case 2. Intraoperative photographs and schematic drawing. (a) Intraoperative view before resection with the results of functional brain mapping (1 hand-digit motor; 2 thumb sensory; 3 tongue sensory; 4 tongue motor; 5, 6 speech arrest). (b) Intraoperative view after tumor resection showing that the lesion across the central sulcus had been resected. (c) Schematic drawing. The continuous black line indicates the area of craniotomy and the white line, the location of the tumor (resected area in b). Arrows central sulcus; arrowheads sylvian fissure

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was administered intravenously at 100 mg/m2 body surface area on the first day of radiation and again 6 weeks later. Two months after surgery, he was discharged to go home with only slight dysarthria.

10.4.2.3 Case 3 A 35-year-old woman presented with oligodendroglioma manifesting as right facial seizures followed by right hemiconvulsion. T2-weighted MR imaging demonstrated a mass lesion in the left opercular portions of the precentral gyrus inferolateral to the precentral knob but not involving the insula (Fig. 10.8a). Neurological and neuropsychological examination revealed no abnormality. The patient underwent left frontoparietotemporal craniotomy while she was awake. Direct cortical stimulation identified the hand-digit, face, and tongue motor area and the

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Fig. 10.8 Case 3. A 34-year-old woman with left frontal oligodendroglioma. (a) Preoperative axial T2-weighted MR images showing a high intensity mass in the left frontal opercular region. (b) Postoperative axial DW MR images depicting a new high intensity lesion (arrow) predominantly anterior to the resection cavity but no massive high intensity lesion involving the corona radiata. (c) Follow-up axial T2-weighted MR images obtained 5 years after surgery demonstrating no recurrence of the tumor and a tiny high intensity lesion (arrow) beneath the resection cavity corresponding to the new high intensity lesion on the postoperative DW MR image (arrow in B)

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Fig. 10.9 Case 3. Intraoperative photographs and schematic drawing. (a) Intraoperative view before resection with the results of functional brain mapping (1 hand-digit motor; 2 face motor; 3 tongue motor; 4 tongue sensory; 5 face sensory; 6 thumb sensory). (b) Intraoperative view after tumor resection showing the lesion anterior to the central sulcus had been resected. (c) schematic drawing. The continuous black line indicates the area of craniotomy and the white line, the location of the tumor (resected area in b). Arrows central sulcus; arrowheads sylvian fissure

thumb, face, and tongue sensory area (Fig. 10.9a). The patient did not wish to continue the neurophysiological mapping, especially of the language function. She then underwent intubation of the trachea and tumor resection under general anesthesia. We dissected the sylvian fissure toward the distal end until the central sulcus and the insular surface were exposed under the operating microscope, separated and preserved the precentral artery from the tumor, and resected the lower portion of the tumor toward the deepest portion using the upper limiting sulcus as the anatomical landmark and neuronavigational assistance. We then removed the tumor stepwise while monitoring muscle contraction by direct cortical and subcortical stimulation to the hand-digit motor area (Fig. 10.9b). Postoperatively, right facial palsy and dysarthria were observed but without disorder of language comprehension or written expression. MR imaging immediately following

10 Ischemic Complications Associated with Resection of Opercular Gliomas Fig. 10.10 Case 3. (a) Preoperative coronal T2-weighted MR image showing a high intensity mass in the opercular region. (b) Follow-up 3-tesla 3-dimensional TOF coronal MR image depicting the lateral LSA (arrowhead) and the presumably preserved long insular arteries (arrows)

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surgery showed gross total resection of the tumor and a limited ischemic area beneath the resection cavity (Fig. 10.8b). Adjuvant therapy consisted of 60 Gy of fractionated radiation to the extended local field. ACNU was administered intravenously at 100 mg/m2 body surface area on the first day of radiation. Two months after surgery, she was discharged to go home with slight dysarthria. She received maintenance ACNU bimonthly for 2 years at an outpatient clinic, and follow-up MR imaging obtained 5 years after surgery disclosed no tumor recurrence and only a limited area of ischemia in the corona radiata (Fig. 10.8c). Three-tesla 3D TOF coronal MR imaging demonstrated a long insular artery running inside the resection cavity (Fig. 10.10).

10.5 Discussion Gliomas involving the nondominant face motor cortex can be safely removed using brain mapping techniques to localize the rolandic cortex and avoid resection of the hand motor cortex and descending subcortical motor pathways [9]. Radical tumor resection of purely

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opercular glioma that does not include the insula can be achieved in the dominant hemisphere without significant lasting morbidity [5]. However, only biopsy is recommended for large dominant insular or opercular-insular tumors because the LSA hinder total resection, and no clear border toward the internal capsule can be found. Report of surgical outcomes of 14 cases of opercular gliomas stressed the importance of intraoperative neuromonitoring as an aid to surgery in the dominant opercular region [11]. Clearly, intraoperative functional brain mapping techniques can help preserve the cortical and subcortical functions, but vascular damage during resection of opercular glioma remains less well understood. Preservation of the arteries penetrating the glioma is one of the most important procedures during glioma surgery. Meticulous anatomical analysis of blood supply to the eloquent areas is essential to avoid permanent deficits. Approximately 85–90% of the insular arteries are short and supply the insular cortex and extreme capsule; 10% are of medium length and supply the claustrum and external capsule as well; and 3–5% are long and extend as far as the corona radiata [18]. Interruption of the blood flow to these long insular arteries during resection of intrinsic insular tumor may result in hemiparesis, so these arteries must be preserved to prevent infarction of the corona radiata [6, 8, 17, 18]. Our microangiographic analysis [7, 15, 16] demonstrated that both the long insular and long medullary arteries from the opercular and cortical segments of the MCA that pass over the frontoparietal operculum supply the corona radiata, and the LSA supply the adjacent upper part of the posterior limb of the internal capsule [7]. Adequate collateral blood supply cannot be expected because the intraparenchymal arterioles, such as the LSA, long insular arteries, and long medullary arteries, are all end arteries without substantial anastomoses with other arteries except under pathological conditions, such as with moyamoya disease. If the impaired arteries supply most of the descending motor pathway within the corona radiata, surgical resection of opercular glioma is likely to cause hemiparesis. Prevention of critical damage to the descending motor pathway within the corona radiata requires accurate knowledge of the vascular anatomy supplying this region. Among the relevant vessels, the long insular arteries are located primarily in the posterior region of the insula [18], most commonly on the posterior half of the central insular sulcus and on the long gyri [17]. Therefore, subcortical resection around the upper limiting sulcus of the posterior region of the insula carries a higher risk of sacrifice of the long insular arteries, which may lead to extensive corona radiata infarction and, ultimately, critical damage to the descending motor pathway. Similarly, wide resection in the anteroposterior and cephalocaudal directions of the opercular region could damage a large number of medullary arteries originating from the opercular and cortical segments of the MCA and passing over the frontoparietal operculum. In our experience, these two maneuvers are the main risk factors for critical infarction in the corona radiata after resection of opercular glioma. Postoperative infarction beneath the resection cavity was obviously limited in our Case 3 compared to Cases 1 and 2 (Figs. 10.4, 10.6, and 10.8). The resected area in Case 3 did not cross the central sulcus but was localized in the precentral gyrus, which permitted removal of the tumor without damage to the long insular arteries that contribute to the vascular supply to the corona radiata (Fig. 10.10). The narrow resected width in the


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anteroposterior direction probably caused less damage to the medullary arteries from the opercular and cortical segments of the MCA than in Cases 1 and 2. In contrast, the infarcted area was largest in Case 1, and the subcortical resection around the upper limiting sulcus of the posterior region of the insula and wide resection in both anteroposterior and cephalocaudal directions of the opercular region caused permanent hemiparesis (Figs. 10.5, 10.7, and 10.9). The smaller infarcted area in Case 2 was possibly attributable to the narrower resection in the cephalocaudal direction (Figs. 10.5 and 10.7). Preoperative detection of the long insular arteries and the medullary arteries may help identify the optimal surgical candidates for opercular gliomas. Knowledge of the relatively sharp margin of the tumor-brain interface together with precise information about these perforating arteries may enable total resection with their preservation. Three-tesla 3D TOF MR imaging with contrast medium can visualize the route of the LSA, improving the extent of resection and reducing the neurological risk for insulo-opercular gliomas [12]. However, thinner vessels, such as the long insular arteries and the medullary arteries from the MCA, are still difficult to visualize. Our present experience suggests that the long insular arteries can barely be visualized in some patients with opercular gliomas (Figs. 10.3 and 10.10). The availability of accurate information on the perforating arteries from 3-tesla MR imaging may change the surgical strategy for opercular gliomas. Reliable methods for avoiding damage to the long insular and medullary arteries within the tumor are not available, but the development of new surgical devices [10] to remove opercular gliomas and preserve thin blood vessels is expected.

10.6 Conclusions The present study demonstrates that damage to the distributing arteries from glioma resection in the frontoparietal opercular region produces ischemic complications beneath the resection cavity within the corona radiata; of particular concern is damage to the long insular arteries and/or medullary arteries from the opercular and cortical segments of the MCA that pass over the frontoparietal operculum.

Abbreviations 3D ACNU DW MCA MR SENSE TOF

3-Dimensional Nimustine hydrochloride Diffusion-weighted Middle cerebral artery Magnetic resonance Sensitivity-encoding Time-of-flight

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References 1. Berger MS. Malignant astrocytomas: surgical aspects. Semin Oncol. 1994;21:172–85. 2. Berger MS, Deliganis AV, Dobbins J, Keles GE. The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer. 1994;74:1784–91. 3. Berger MS, Kincaid J, Ojemann GA, Lettich E. Brain mapping techniques to maximize resection, safety, and seizure control in children with brain tumors. Neurosurgery. 1989;25:786–92. 4. Berger MS, Ojemann GA, Lettich E. Neurophysiological monitoring during astrocytoma surgery. Neurosurg Clin N Am. 1990;1:65–80. 5. Ebeling U, Kothbauer K. Circumscribed low grade astrocytomas in the dominant opercular and insular region: a pilot study. Acta Neurochir (Wien). 1995;132:66–74. 6. Hentschel SJ, Lang FF. Surgical resection of intrinsic insular tumors. Neurosurgery. 2005;57 (1 Suppl):176–83. 7. Kumabe T, Higano S, Takahashi S, Tominaga T. Ischemic complications associated with resection of opercular glioma. J Neurosurg. 2007;106:263–9. 8. Lang FF, Olansen NE, DeMonte F, Gokaslan ZL, Holland EC, Kalhorn C, et al. Surgical resection of intrinsic insular tumors: complication avoidance. J Neurosurg. 2001;95:638–50. 9. LeRoux PD, Berger MS, Haglund MM, Pilcher WH, Ojemann GA. Resection of intrinsic tumors from nondominant face motor cortex using stimulation mapping: report of two cases. Surg Neurol. 1991;36:44–8. 10. Nakagawa A, Kumabe T, Kanamori M, Saito R, Hirano T, Takayama K, et al. Clinical application of pulsed laser-induced liquid jet: preliminary report in glioma surgery] [Article in Japanese. No Shinkei Geka. 2008;36:1005–10. 11. Peraud A, Ilmberger J, Reulen HJ. Surgical resection of gliomas WHO grade II and III located in the opercular region. Acta Neurochir (Wien). 2004;146:9–18. 12. Saito R, Kumabe T, Inoue T, Takada S, Yamashita Y, Kanamori M, et al. Magnetic resonance imaging for preoperative identification of the lenticulostriate arteries in insular glioma surgery. Technical note. J Neurosurg. 2009;111:278–81. 13. Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med. 2008;358:18–27. 14. Smith JS, Cha S, Mayo MC, McDermott MW, Parsa AT, Chang SM, et al. Serial diffusionweighted magnetic resonance imaging in cases of glioma: distinguishing tumor recurrence from postresection injury. J Neurosurg. 2005;103:428–38. 15. Takahashi S, Goto K, Fukasawa H, Kawata Y, Uemura K, Suzuki K. Computed tomography of cerebral infarction along the distribution of the basal perforating arteries. Part I: Striate arterial group. Radiology. 1985;155:107–18. 16. Takahashi S, Goto K, Fukasawa H, Kawata Y, Uemura K, Yaguchi K. Computed tomography of cerebral infarction along the distribution of the basal perforating arteries. Part II: Thalamic arterial group. Radiology. 1985;155:119–30. 17. Tanriover N, Rhoton AL Jr, Kawashima M, Ulm AJ, Yasuda A. Microsurgical anatomy of the insula and the sylvian fissure. J Neurosurg. 2004;100:891–922. 18. Türe U, Yaşargil G, Al-Mefty O, Yaşargil DC. Arteries of insula. J Neurosurg. 2000;92: 676–87. 19. Yoshikawa K, Kajiwara K, Morioka J, Fujii M, Tanaka N, Fujisawa H, et al. Improvement of functional outcome after radical surgery in glioblastoma patients: the efficacy of a navigationguided fence-post procedure and neurophysiological monitoring. J Neurooncol. 2006;78:91–7.

Imaging and Tissue Characterization of Atherosclerotic Carotid Plaque Using MR Imaging

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Toshiaki Taoka

11.1 Introduction The carotid bifurcation is a frequent site for atheromatous diseases, and severe stenosis or occlusion of the bifurcation leads to hypoperfusion of the brain [5]. Progression of carotid artery disease relates closely to future cerebral or coronary infarction; stability of the carotid plaque and degree of carotid stenosis are important factors in disease development and assessment. Diagnosis of unstable plaque (vulnerable plaque) is important because its presence may lead to embolic diseases in the brain. Both the size and composition of plaque influence its stability [13]. Histological characteristics of unstable plaque include a large necrotic core that contains a large amount of cholesterol ester, intraplaque hemorrhage, and/ or infiltration by inflammatory cells. Diagnosis of carotid plaque should be aimed at evaluating the degree of fibrosis, thrombosis, existence of lipid or calcification, and degree of stenosis or plaque thickness. In addition, the Rotterdam Study of more than 4,000 neurologically asymptomatic subjects aged 55 years or older associated carotid plaque with increased risk of stroke, irrespective of plaque location. Study results suggest that carotid plaque in such subjects is a marker of generalized atherosclerosis and a source of thrombotic emboli [20].

11.2 Histopathology of Carotid Plaque The wall of the common carotid artery consists of rich elastic fiber in its media as well as rich connecting tissue at its adventitia. In contrast, the wall of the carotid sinus, a local dilation at the origin of the internal carotid artery that contains baroreceptors, has thinner media

T. Taoka Department of Radiology, Nara Medical University, Kashihara, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_11, © Springer-Verlag London Limited 2010

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and a large luminal space. After branching into the external and internal carotid arteries, the walls of the arteries have less elastic fiber and begin to show more smooth muscle. Atherosclerosis is a chronic inflammatory disease of the large arteries. Several locations are susceptible to atherosclerotic plaque formation, including the aortic arch and the proximal edge of a major branch, such as the carotid or aortic bifurcation. In these areas, turbulence in blood flow may cause less constant shear stress, which represents the dynamic force of blood against the vessel wall. Lowered shear stress begins a cascade that includes activation of monocytes followed by release of tissue proliferation factors, which cause endothelial damage leading to plaque formation. Atherosclerotic plaque develops during the following sequence of events [36]. Endothelial dysfunction marks the earliest change in plaque formation. Increased permeability of the endothelium causes upregulation of endothelial adhesion molecules, which leads to adhesion and then migration of leukocytes into the arterial wall. The accumulation of cholesterol within monocytes and macrophages then leads to the formation of foam cells, referred to as fatty streaks, followed by release of mediators, smooth muscle migration, and platelet adherence and aggregation in the plaque. Platelet-delivered growth factor and other factors cause fibrous caps to form, and apoptosis and/or necrosis cause formation of necrotic cores, including leukocytes, lipids, and debris. Macrophage accumulation also causes lesion expansion. Degeneration of the fibrous cap soon follows. Activation of macrophages leads to proteolytic enzyme release, and hemorrhage from the vasa vasorum or thinning of the fibrous cap leads to plaque rupture and then thrombus formation. Vulnerable plaque, also called risky plaque or easy-to-rupture plaque is characterized by a large lipid core, thin fibrous cap, intraplaque hemorrhage, endothelial erosion, cell infiltration within the fibrous cap, and neovasculature. The American Heart Association classified coronary artery plaque into six types that describe its morphology [40], and the classification also seems to be applicable to carotid plaque (Fig. 11.1). Types I, II, and III plaques are early lesions that may be difficult to evaluate by MR imaging because of spatial resolution. Type IV lesions, called atheromas, have a lipid core that occupies an extensive but well

Fig. 11.1 Characteristic components of atherosclerotic lesions, American Heart Association classifications [40]. Type I lesions are the initial lesions that contain atherogenic lipoproteins that lead to an increase in macrophages, formation of scattered macrophage/foam cells, and adaptive intimal thickening. Type II lesions consist of layers of macrophage/foam cells and fat-laden smooth muscle cells and include lesions referred to as fatty streaks. Type III lesions represent the intermediate stage and contain scattered collections of extracellular lipid droplets that disrupt the consistency of intimal smooth muscle cells; this extracellular lipid is the precursor of the core of extracellular lipid that characterizes type IV lesions. Type IV lesions, called atheromas, can potentially produce symptoms. Type IV lesions show dense accumulation of extracellular lipids that occupy an extensive but well defined region of the intima. In Type V lesions, prominent fibrous connective tissue has formed. Type Va lesions, referred to as fibroatheromas, contain a lipid core and fibrous tissue. Type Vb lesions have a lipid core; other parts of the lesion are calcified. In Type Vc lesions, the normal intima is replaced and thickened with fibrous connective tissue, and the lipid core is minimal or absent (fibrotic lesions). Type VI lesions are referred to as complicated lesions. Type VIa lesions involve disruption of the lesion. Type VIb lesions involve hematomas or hemorrhages. Type VIc lesions involve thrombosis

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11 Imaging and Tissue Characterization of Atherosclerotic Carotid Plaque Using MR Imaging Type I

Intimal thickening Macrophage/Foam cells

Type Va

Fibrous thickening

Type VIa

Disruptions of the lesion surface

Type II

Macrophage/Foam cells: Fatty streaks

Type Vb

Calcification

Type VIb

Type III

Small pools of extracellular lipid

Type IV

Core of extracellular lipid

Type Vc

Lipid core is minimal or even absent

Type VIc

Hemorrhage Thrombotic deposit

defined area and results from the accumulation of extracellular lipids. Type V lesions are defined by the formation of prominent new fibrous connective tissue and classified into three subtypes, Va, Vb, and Vc. Type Va lesions, called fibroatheromas, have a lipid core and fibrous tissue; they will be stable when the fibrous cap is thick but vulnerable to rupture if the cap is not thick. Type Vb lesions have calcification in addition to a lipid core and fibrous tissue. Type Vc lesions do not have a lipid core and represent stable plaque. Type VI lesions are complicated and divided as well into three subtypes: VIa, disruptions of the lesion surface; VIb, hemorrhage (VIb); and VIc, thrombotic deposits.

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11.3 Imaging of Carotid Plaque Imaging methods for evaluating carotid plaque include conventional contrast angiography, CT, surface ultrasonography (US), intravascular ultrasound (IVUS), and MR imaging, each with its advantages and disadvantages (Table 11.1) (Figs. 11.2–11.7).

Table 11.1 Advantages and disadvantages of different imaging methods for the carotid artery Modality Advantages Disadvantages Contrast angiography

High spatial resolution

Invasive (stroke risk) Radiation Contrast-related complications Cannot evaluate vessel wall

Computed tomography

Rapid Can evaluate calcification Available in most institutes

Radiation Contrast-related complications

Surface ultrasound

Noninvasive Can evaluate wall and lumen High resolution

Operator dependent Limited information on chemical status

Intravascular ultrasound (IVUS)

Affinity to PTA procedure Information on histological characteristics High resolution

Invasive (stroke risk)

Noninvasive Can evaluate wall and lumen Less operator dependent Information on chemical/ histological characteristics “One-stop shopping” PTA percutaneous transluminal angioplasty Magnetic resonance imaging

Time required for acquisition Requires high power machine Interpretation is complicated

Fig. 11.2 Carotid plaque and carotid endoarterectomy specimen. (a) Computed tomographic angiography (CTA). (b) Magnetic resonance angiography (MRA). (c–f) MR plaque images (c proton densityweighted image, d double inversion recovery black-blood T1-weighted spin echo image, e T2-weighted image, f 3-dimensional [3D] time-of-flight [TOF] image). (g) Carotid endoarterectomy specimen. CTA shows severe stenosis at the origin of the right carotid artery (a). MR angiography also shows severe stenosis at the origin of the right carotid artery, in which the range of stenosis seems longer (b). Thick plaque formation can be found mainly in the posteromedial wall of the internal carotid artery (c–f arrows). Images (c–e) are black-blood images in which the signal of the luminal blood is suppressed. Image (f) is a bright-blood image in which the luminal blood shows a high signal. High signal on the T1-weighted image and low signal on the T2-weighted image within the plaque were interpreted as a lipid-rich necrotic core. The TOF image shows a band of low signal at the surface of the plaque that indicates a fibrous cap in which disruptions are observed. Carotid endoarterectomy specimen in which fibrous intimal thickening, cholesterol crystal, and media disruption were observed (g)

11 Imaging and Tissue Characterization of Atherosclerotic Carotid Plaque Using MR Imaging

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11.3.1 Contrast Angiography Although angiography is an invasive method in which contrast medium is injected through a catheter, it has been the gold standard for diagnosing disease in the carotid or coronal arteries. The method provides high spatial resolution and can depict the internal cavity of the vessels. By permitting evaluation of arteriosclerosis by degree of stenosis and irregularity of the vessel wall, angiography enables evaluation of plaque disruption in advanced carotid plaque. However, angiography does not permit description of histologic characteristics of the arterial wall, and the projection image may cause underestimation of localized stenosis that is diffused and near circumferential [15]. Stenosis by plaque formation may also be underestimated when there is positive remodeling by arteriosclerosis [17]. Contrast angiographic evaluation of stenosis uses the methods of the North American Symptomatic Carotid Endarterectomy Trial (NASCET) and European Carotid Surgery Trial (ECST) [11, 34]. The NASCET method is easy to perform and provides stable measurements [16]. The ECST method can reflect the actual thickness of the plaque, but it is observer-dependent and tends to indicate a higher degree of stenosis compared with the NASCET method.

11.3.2 Computed Tomography Computed tomography is an invasive method in that it uses ionized radiation, but it can provide high spatial resolution and permits simultaneous evaluation of luminal stenosis and the vessel wall. Advanced multidetector CT (MDCT) imagers can be used for CT angiography (CTA) that enables easy acquisition of high resolution 3-dimensional (3D) images of the vessel lumen. Calcification has been associated with carotid plaque stability, and CT best visualizes vessel wall calcification. Patients with calcium within the plaque are reported to have fewer symptoms of transient ischemic attack and stroke [21], and in patients with stenosis, MDCT study

Fig. 11.3 Magnetic resonance (MR) plaque imaging and virtual histology intravascular ultrasound (VH-IVUS): carotid plaque with lipid core. (a) Conventional right carotid angiography. (b) MRA. (c–h) MR plaque imaging (c Sagittal black-blood T1-weighted image, d TOF, e T1-weighted 3-dimensional [3D] magnetization-prepared rapid acquisition with gradient echo [MPRAGE]. (f) Double inversion recovery black-blood T1-weighted spin echo image. (g) Proton density-weighted image. (h) T2-weighted image with suppression pulse). (i) Surface US. (j) VH-IVUS. Both contrast angiography and MRA show stenosis at the origin of the internal carotid artery (a, b). High signal on the T1-weighted image (c–f, arrows) and low signal on the T2-weighted image (h, arrowhead) within the plaque are interpreted as a lipid-rich necrotic core. A band of low signal at the surface of the plaque on the TOF image indicates a fibrous cap in which disruptions are observed. Surface US can provide geometric information about plaque, information about plaque composition is limited (i). On VH-IVUS, the yellow indicates fatty areas and corresponds to the lipid core (j)

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showed an association between stability and the proportion of carotid plaque calcification, rather than the absolute volume of plaque [32]. However, other reports indicate that calcifications of the vessel wall do not independently predict the severity of ischemia, and future stroke risk cannot be predicted from carotid calcification [14]. Neither can the degree of calcification of the intracranial carotid artery predict the possibility of future cerebral stroke [45]. Besides calcification, lipid cores or intraplaque hemorrhage can be evaluated by CT. Wintermark and associates systematically compared CT images with histologic sections and obtained micro-CT images to determine the CT attenuation associated with each component of atherosclerotic plaque [52]. CT showed good correlation with histologic examination for large lipid cores and large hemorrhages and good detection of ulcerations and precise measurements of fibrous cap thickness. The recently introduced dual-source CT with dual-energy modes can obtain two different energy readings with a single pass. Dual-energy imaging exploits the material specificity of X-ray absorption and the energy dependence of the X-ray to differentiate materials

a

b

c

Fig. 11.4 Magnetic resonance (MR) plaque imaging and virtual histology intravascular ultrasound (VH-IVUS): carotid plaque with thick fibrous tissue. (a) Contrast angiography. (b) CTA. (c) MRA. (d–h) MR plaque imaging (d: Sagittal black-blood T1-weighted image, e: TOF, f: T1-weighted 3D MPRAGE, g: double inversion recovery black blood T1-weighted spin echo image, h: proton density-weighted image, i: T2-weighted image). (j) VH-IVUS. Contrast angiography, CTA, and MRA show stenosis at the origin of the internal carotid artery (a–c). Most of the area within the plaque shows low signal on the T1-weighted image (d–f, arrows) and high signal on the T2-weighted image (i, arrowhead), which was interpreted as fibrous tissue. On VH-IVUS, the green area indicates fibrous tissue (j)


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and characterize tissue. By differentiating iodine from the bone, the dual-energy method can be used to remove bone and calcification from CTA, and such removal has been reported using only a single contrast-enhanced scan without subtraction technique [48].

11.3.3 Ultrasonography 11.3.3.1 Surface Ultrasonography Surface ultrasonographic examination of the carotid artery is noninvasive and can evaluate the status of the vessel wall and luminal flow in real time. The artery is easily accessible by US investigation, and use of a high resolution probe enables observation of the vessel wall

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Fig. 11.5 Magnetic resonance (MR) plaque imaging and virtual histology intravascular ultrasound (VH-IVUS): carotid plaque with intraplaque hemorrhage. (a) CTA. (b) MRA. (c–h) MR plaque imaging (c. Sagittal black-blood T1-weighted image, d. TOF, e. T1-weighted 3D MPRAGE, f. Double inversion recovery black blood T1-weighted spin echo image, g. Proton density-weighted image, h. T2-weighted image with suppression pulse). (i) VH-IVUS. CTA shows severe stenosis at the origin of internal carotid artery (a, arrow), whereas a maximum-intensity-projection (MIP) image of TOF MR angiography shows less severe stenosis (b, arrowhead), which is a pitfall in interpreting the MRA image. The signal at the origin of the carotid artery represents hemorrhage and not flow. High signal on the T1-weighted image (c–g, arrows) and low signal on the T2weighted image (h, arrowhead) are observed within the plaque. These high signal on T1-weighted image are the cause of apparent less severe stenosis on MRA. On VH-IVUS, the red area indicates a hemorrhage (h)


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d

Fig. 11.6 Magnetic resonance (MR) plaque imaging and computed tomography (CT): carotid plaque with calcification. (a–d) MR plaque imaging (a TOF, b T1-weighted 3D MPRAGE). (c) CTA original image, (d) CTA maximum intensity projection image. There is an area of very low signal intensity at the deep area of the plaque represents calcifications (a, b arrows). CTA also depicts these calcifications

as two layers, a layer of low intensity on the luminal side and one of high intensity on the outside. The former layer represents a complex of the intima and media (intima-media complex [IMC]) and the latter, of the adventitia and connective tissue surrounding the artery. The vessel diameter of the carotid artery can be quantified by measuring either the distance between IMCs or between adventitias. Sometimes, the former method cannot be performed because the IMC of the near wall cannot be visualized. Intima-media thickness (IMT), a gauge of the thickness of arterial walls, is reported to increase with the progression of arteriosclerotic disease [35]. Carotid IMT is a strong predictor of future vascular events [29] and can be evaluated using surface US. High resolution carotid US can evaluate tissue characteristics of arteriosclerotic plaque [1]. Stable plaque, which consists mainly of fibrous components, shows homogeneous high intensity, whereas unstable plaque tends to show low intensity. Calcifications appear as acoustic shadows, and intraplaque hemorrhage and atheroma appear as homogeneous areas of low intensity. Although surface US is a noninvasive, highly effective method for evaluating plaque characteristics, it is limited by its dependence on the skill of the observer and, thus, by subjective interpretation of results [39] and by the difficulty in assessing highly positioned plaques.

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Fig. 11.7 Magnetic resonance (MR) plaque imaging and carotid artery stenting. (a–c) MR plaque imaging. (a) T1-weighted image by selective partial inversion recovery [SPIR]. (b) T2-weighted image. (c) Double inversion recovery black-blood T1-weighted spin echo image. (d) Filter device. (e) Histological specimen of the debris. Thick plaque formation is shown at the origin of the left internal carotid artery with high signal on the T1-weighted image (a, c) and low signal on the T2weighted image (b), which is interpreted as plaque with a lipid-rich necrotic core. Carotid artery stenting was carried out using a filter device, in which captured debris was found after the procedure (d). A histological specimen of the debris shows closely aggregated foam cells and cholesterol clefts, which agree with the lipid-rich plaque(e)

11.3.3.2 Intravascular Ultrasonography IVUS is a newly developed imaging method in which a transducer is placed in the arterial lumen using the same technique used in angiography. Although IVUS is invasive, it can be used to acquire high resolution real-time tomographic images of the arterial wall. The diameter of the IVUS transducer is about 1 mm, and spatial resolution is 100–250 mm. Although IVUS can depict the thickness and echogenicity of plaque, information is limited concerning the characteristics of plaque tissue. As in US, acoustic shadows signify calcification, high echogenicity signifies fibrous tissue, and areas of low echo signify intraplaque hemorrhages or lipid cores. IVUS findings obtained during interventional procedures, such as percutaneous transluminal angioplasty (PTA), offer feedback and guidance as the operation is completed. For example, when plaque has a low echoic component, the operator should be aware of emboli caused by the ruptured lipid core or thrombus. Virtual histology intravascular ultrasonography (VH-IVUS) was developed to analyze coronary plaque using spectral analysis of the radiofrequency of US signals. The VH-IVUS


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device is used to create color maps of the fibrous, fibro-fatty, and calcium components and the necrotic core of the plaque that enable detailed assessment of plaque composition. There is some report analyzing the suitability and efficacy of VH-IVUS for the assessment of carotid stenosis [23, 43]. While its accuracy and effectiveness in carotid artery disease is still unclear, potential benefit of this plaque mapping device development will be the prediction of how the carotid plaque will behave at carotid artery stenting (CAS) or percutaneous transluminal angioplasty (PTA). To ensure the safety of these procedures, plaque characteristics must be clearly understood before the procedures are undertaken.

11.3.4 Magnetic Resonance Imaging MR imaging reflects the chemical composition, chemical concentration, water content, or physical status of tissue. For carotid plaque, it provides information unavailable by other methods. It permits the patient to undergo a single procedure to obtain various morphological or functional studies, such as normal anatomical study, diffusion-weighted imaging, or MR perfusion study. Since MR imaging is noninvasive, it is a good method to monitor therapeutic procedures. High resolution in vivo MR imaging measurements of plaque wall thickness have been reported to agree with ex vivo measurements of carotid endarterectomy specimens, and application for follow-up study of plaque thickness has been proposed based on studies examining the mechanisms involved in the growth of atherosclerotic carotid lesions [56].

11.3.4.1 Hardware for MR Plaque Imaging To depict the structure of carotid plaque, MR hardware must allow for high spatial resolution and high signal-to-noise ratio (SNR). A minimum 0.5-mm resolution, which requires high gradient strength, is needed to visualize the vessel wall; a surface coil effectively improves SNR because the coil can be set close to the carotid bifurcation. As the carotid arteries are superficial structures, they are well suited for use with a phased-array coil assembly that consists of surface coils placed on the carotid bifurcation [19]. To suppress motion artifacts, cardiac gating capability is an important feature for the MR scanner. Fat-saturation pulses are necessary to suppress signals from subcutaneous fat, which mainly comprises triglycerides. The pulses do not affect the lipid signal within the plaque because lipids consist primarily of cholesterol esters and free cholesterol, not triglycerides [55]. For clinical imaging of the vessel wall, the MR scanner requires at least 1.5-T field strength to provide high enough SNR to analyze the fine structure of the carotid plaque, and high field (3.0-T) imagers are gaining widespread clinical use. Several studies have focused on carotid plaque imaging using a 3.0-T imager. One demonstrated significant improvement in SNR or contrast-to-noise ratio (CNR) and image quality for high resolution blackblood imaging of carotid arteries at 3 T [58]. Another study on differences in image contrast

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between 1.5- and 3.0-T imagers showed the possibility that the increased susceptibility of calcification and paramagnetic ferric iron in hemorrhages may alter the quantification and/ or detection of carotid plaque [47]. However, the study concluded that the imaging criteria for interpreting the wall of the carotid vessel were the same at 1.5 and 3.0 T. Morphologic measurements are reported to be compatible between 1.5 and 3.0-T images [58].

11.3.4.2 Approaches to MR Plaque Imaging Various technical approaches for evaluating carotid plaque have been proposed, and selection of the appropriate image acquisition technique is essential. Spin-echo sequences are less affected by T2* components and allow comparatively simple interpretation of signal intensity. The gradient-echo sequences used in time-of-flight (TOF) MR angiography [MRA] show mixed signal characteristics of T1- and proton density-weighted factors and are affected by T2* components, which lead to greater emphasis on low signal intensities from hemorrhage, calcification, or fibrosis. Another important choice for MR plaque imaging is whether to use the bright-blood or black-blood method. The two methods have complementary characteristics. In the brightblood method, the high signal represents blood flow within the carotid lumen. The source image of TOF MRA is a commonly used bright-blood plaque image. The bright-blood method is suitable for visualizing: the fine structure of the vessel wall because the vessel lumen is visualized as the high signal; small ulcerations at the surface of the vessel wall that are associated with the generation of thrombi and embolic events; and the fibrous cap at the surface of atherosclerotic plaque. Bright-blood imaging depicts the fibrous cap as a structure with low signal between the high signal of the vessel lumen and the intermediate signal of the plaque core; where the fibrous cap is ruptured, the low signal band bordering the vessel lumen is absent and regions of high signal appear adjacent to the lumen. This information is useful because the incidence of rupture is lower for plaque with a thick fibrous cap that is stable and higher for plaque with a thin or disrupted fibrous cap. In contrast to the bright-blood method, the black-blood method is designed to suppress the signal within the vessel lumen and provide isolated visualization of the signal of the vessel wall, which enables analysis of histological characteristics of the plaque. Various methods are used to suppress the signal from blood flow; the simplest is the presaturation technique, a thinsection spin-echo sequence with flow presaturation at the upper stream of the blood flow [10]. This technique is also applicable to other imaging sequences, such as TOF MRA. Although the presaturation technique is simple and can cover a wide range of vessels, turbulence or delayed flow at the branching area of the carotid artery causes insufficient suppression within the lumen, which produces artifacts that mimic wall thickening or high signal plaque. The double inversion recovery (IR) technique was developed to solve the missed suppression problem [9]. Application of a nonselective IR pulse followed by an IR pulse at the plane of imaging makes the spin within the plane of imaging the original state. Images are acquired when the spin of the blood reaches the null point after being exposed to the initial nonselective IR pulse. Fat suppression and electrocardiography (ECG) gating are applied to this imaging sequence to suppress artifacts from fat or pulsatile movement of the vessel


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wall. Although this double IR technique provides precise and high resolution images, the acquisition time is long and the number of imaging slices is limited. Thus, it is difficult to cover a wide range of vessels using this technique. To overcome this problem, optimized IR techniques have been developed to increase scan efficiency by applying multislice acquisitions and parallel imaging [24]. Another choice for MR imaging of carotid plaque is whether to use 2-dimensional (2D) or 3D acquisition. The 2D spin-echo or fast spin-echo sequence is necessary for satisfactory tissue contrast and precise suppression of the signal from blood flow. However, its use limits the number of slices to avoid unreasonably long acquisition and does not allow easy observation of tortuous arteries. On the other hand, 3D imaging sequence enables a wide range of coverage, and 3D and isovoxel imaging are useful in observing tortuous arteries by making reconstructions perpendicular to the axis of the artery. Bright-blood plaque imaging by TOF MRA is useful for 3D imaging of carotid plaque. Coombs and associates reported on the composition of carotid atherosclerosis visualized by ex vivo high resolution 3D MR imaging [8]. Using fast imaging with steady precession (FISP) sequence to provide the highest spatial resolution and retain a high SNR, they showed that the collagenous cap, calcification, and necrotic core can typically be distinguished using isotropic submillimeter resolution during 3D MR imaging. Magnetizationprepared rapid acquisition with gradient echo (MPRAGE) or MR direct thrombus imaging (MRDTI) are other useful T1-weighted 3D imaging sequences for evaluating carotid plaque [53]. In these IR-prepared 3D gradient-echo sequence images (MPRAGE, MRDTI), an area of high signal is reported to correspond to complicated carotid atherosclerotic plaque that represents high risk plaque containing a hemorrhage/thrombus [31]. These methods can visualize a wide range of vessels within a relatively short acquisition time, and image or signal interpretation is simple. Periodically rotated overlapping parallel lines with enhanced reconstruction (PROPELLER) and BLADE (the same type software; by SIEMENS AG, Erlangen, Germany) are the means of acquiring and reconstructing data that compensate for bulk in-plane patient motion. The two methods acquire data in a series of rotating blades, each of which collects information from the central area of the k-space. When applied to the carotid arteries, this sequence reduces motion artifacts arising from physiological respiratory movements or arterial pulsation. BLADE T2-weighted images and BLADE T1-weighted images can detect atherosclerotic plaque and neighboring turbulent flow, a risk factor for intimal injury. The BLADE sequence enables multislice acquisition that covers the entire carotid bifurcation without cardiac gating, and addition of gating makes available BLADE black-blood images. When multislice BLADE images show positive findings, single-slice BLADE black-blood sequence should be used to assess carotid plaque [22]. Examples of reported protocols for magnetic resonance plaque imaging is provided in Table 11.2 and 11.3 [12, 38].

11.3.4.3 Interpretation of MR Plaque Imaging Yuan and colleagues developed a multi-contrast study for carotid plaque imaging that consists of black-blood imaging (spin-echo-type T1- and T2-weighted images and proton

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Table 11.2 Magnetic resonance imaging parameters used in multicenter and multi-manufacturer protocol [38] 3D-TOF 2D-T1W 2D-PDW 2D-T2W Readout sequence

Gradient echo

FSE or TSE

FSE or TSE

FSE or TSE

TR (ms)

23

800

2,700

2,700

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3.6/4.5/6.3

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44/48/52

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–

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16 × 12

16 × 12

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256 × 192

256 × 192

Number of slices

24 (48)

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2 (1)

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Inflow saturation (arteries and veins)

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7

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Table 11 3 Parameters used in high-resolution multicontrast-weighted magnetic resonance imaging [12] Parameters T1W SE PDW TSE T2W TSE TR (ms)

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1,500

3,944

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40

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256 × 512

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d ensity-weighted image) and bright-blood imaging (TOF MRA). They reported that using multiple contrast weightings is a valid means of detecting and characterizing different plaque components, such as a lipid-rich necrotic core, fibrous tissue, calcifications, thrombus, and the integrity of the fibrous cap in vivo [59, 60] (Table 11.4). Typical histological characteristics of vulnerable plaque include a large lipid-rich/necrotic core with an unstable fibrous cap, which may be thin, ulcerated, or fissured. In their reports, Yuan’s group showed that the lipid-rich/necrotic core without hemorrhage shows iso to high signals to that of salivary glands (structures near the carotid arteries) on T1- and proton density-weighted images, and low to iso signals on T2-weighted images. Fresh or recent hemorrhage at a lipid-rich/necrotic core increases the signal intensity on T1-weighted images and TOF. On T2- and proton density-weighted images, fresh hemorrhages show iso to low signal intensity, whereas recent hemorrhages show high intensity. Old hemorrhages show low to iso signals on T1-weighted images and TOF and low signals on T2- and proton density-weighted images. Calcification shows low intensity on all imaging sequences. Tissue with high signal intensity on T2- and proton density-weighted images shows low to iso signals on T1-weighted images, and TOF images are interpreted as loose fibrous matrix in Yuan’s reports. The fibrous cap is described as having low signal on TOF images and iso signal on T1-, T2-, and proton density-weighted images [58]. They reported that the detection of lipidrich/necrotic core by multicontrast plaque imaging has 87% accuracy, 85% sensitivity, and 92% specificity compared with examination of histologic specimens [59, 60]. The multicontrast study also includes TOF MRA as a bright-blood method. The 3D TOF bright-blood imaging technique is useful in identifying unstable fibrous caps in atherosclerotic human carotid arteries in vivo. On TOF MRA images, a dense collagen-based fibrous cap is described as a hypointense band near the bright lumen. TOF MRA allows differentiation of intact thick fibrous caps, intact thin fibrous caps, and ruptured fibrous caps in vivo in human carotid arteries. Intact thick fibrous caps appear as a thick dark band between a bright lumen and gray plaque core; in sites with ruptured caps, the dark band neighboring the lumen shows a defect on which a bright region of the lumen encroaches. A high level of agreement between TOF MRA findings and the histologic state of the fibrous cap has been shown [18]. This method used by Yuan and colleagues in their multicontrast studies is the milestone for tissue characterization of carotid plaque by high resolution MR imaging, and many Table 11.4 Contrast at magnetic resonance imaging of main components of atherosclerotic plaque [59, 60] Plaque Time of flight T1-weighted IntermediateT2-weighted component weighted Recent hemorrhage

High

High to moderate

Variable

Variable

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Moderate

High

High

Variable

Intimal calcification

Low

Low

Low

Low

Fibrous tissue

Moderate to low

Moderate

High

Variable

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studies in tissue characterization have followed [6, 46, 48]. However, there is some disagreement between studies regarding signal interpretation. High signal on T2-weighted images has been reported by Trivedi’s group [46] to show the fibrous cap of the plaque and by other researchers to indicate a lipid-rich/necrotic core without hemorrhage [48, 54] (Table 11.5). On T1-weighted images, Cappendijk’s team reported the fibrous cap and lipid core to have similar intensity and to be indistinguishable [6]. Fabiano and colleagues reported variable intensity of the lipid core on T1-, T2-, and proton density-weighted images [12] (Table 11.6). One reason for these disagreements may be the difference in actual imaging sequences used. Imaging sequence is not standardized, and the terms “T1-weighted images” or “T2weighted images” may refer to different contrast characteristics by different imaging sequences. For T1-weighted images, most black-blood sequences use cardiac gating, and the repetition time (TR) is set to R wave-to-R wave time (RR time) of the ECG. Of course, RR time differs by study, generally ranging from 800 to 1,200 ms, and differences in RR time = TR result in differences in contrast characteristics. Moreover, even when the RR time is as short as 800 ms, a TR of 800 ms is much too long for the image to be regarded as T1-weighted. At 1.5 T, the TR of T1-weighted images should be less than 500 ms. For T2-weighted images, parameters for imaging differ between reports, which may be the cause of disagreement in interpreting contrast. Trials that aim for standardization between institutes or between scanners are important. Saam and collaborators proposed a standardized multisequence protocol [38] that used a Table 11.5 Findings on magnetic resonance imaging of plaque components [54] Histologic features T1-weighted images T2-weighted images Fibrous cap

Hypointensity

Hypointensity

Fibrosis

Isointensity

Isointensity

Calcification

Hypointensity

Hypointensity

Myxomatous tissue

Isointensity

Hyperintensity

Lipid core with intraplaque hemorrhage

Hyperintensity

Variable

Lipid core without intraplaque hemorrhage

Isointensity

Variable

Table 11.6 Signal intensity of the main tissue type of atherosclerotic plaque [12] Tissue T1-weighted T2-weighted Proton densityweighted Fibrous/loose connective tissue

Gray

Bright

Bright

Fibrous tissue

Gray

Bright/gray

Bright

Calcification

Dark

Dark

Dark

Lipid core

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sequence summarized in Table 11.2, which also employs rather long TR (800 ms) for T1-weighted images. In addition, their study evaluated differences in imaging results obtained by MR scanners from different manufacturers. Using a standardized multisequence protocol and identical phased-array carotid coils, they found comparable reproducibility of quantitative measurements by scanners from General Electric, Siemens, and Philips. Interpretation of findings from multicontrast analysis of carotid plaque is also complicated and time consuming, and a simple method for predicting plaque vulnerability would be useful for applying plaque imaging to daily practice. One approach to this problem is to use a single imaging sequence to judge vulnerable plaque. Yamada and associates used plaque imaging with 3D IR-based T1-weighted images (MPRAGE) and found strong association between the hyperintense signal of the carotid plaque on the MPRAGE images and previous ipsilateral ischemic events [53]. They pointed out that hyperintense signals on MPRAGE persist over several months and suggested that such intense signals represent a potential indicator of risk for subsequent cerebral ischemia. Using a 3D T1-weighted turbo field echo sequence similar to that utilized in Yamada’s report, Cappendijk’s group [7] reported a single contrast study that showed that a 3D T1weighted sequence can detect a lipid-rich necrotic core and that a larger area of high signal, which may represent a lipid-rich necrotic core, has a close relationship with ischemic symptoms. Determining the signals of carotid plaque or plaque composition is not the singular means of assessing plaque vulnerability. Plaque morphology can also be used as a predictor of plaque vulnerability. Using computer simulation and models derived from in vivo high resolution MR imaging, Li and associates performed a structural analysis of the effects of varying fibrous cap thickness, lipid core size, and lumen curvature on plaque stress distributions [28]. They found a close relationship between specific plaque morphology, such as large lumen curvature and thin fibrous cap, and plaque vulnerability.

11.3.4.4 Contrast Enhancement and Functional and Molecular Imaging for Carotid Plaque Evaluation of the carotid artery also requires information beyond the chemical components within the plaque mentioned; inflammation or neovasculature within the plaque, an active biological phenomenon, also needs assessment. Such neovasculature indicates plaque weakness and an increased likelihood of rupture from mechanical stress, such as pulsatile motion or shear stress, as well as intraplaque hemorrhage, and its presence accelerates the formation of advanced plaque lesions by increasing plaque volume and vulnerability and, thereby, the degree of vessel stenosis. Several reports describe the use of contrast enhancement and functional or molecular imaging to evaluate the biological process within carotid plaque. Prior to multiple well known contrast MR studies by Yuan’s group [59, 60], Aoki and fellow researchers examined contrast enhancement for carotid plaque [3, 4] and stressed the usefulness of dynamic contrast enhancement for evaluating neovascularization in atherosclerotic plaque. They suggested that enhancement of the arterial wall on MR images reflects neovascularization resulting from atheromatous arteriosclerosis and may relate to atherosclerosis and the

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development of the vasa vasorum, that is, vessels found in the adventitial layer of arteries, such as the carotid artery [3]. Yuan’s group found higher enhancement associated with the fibrous tissue and the highest with areas of dense neovasculature; that more highly enhanced fibrous tissue can be distinguished from less enhanced necrotic tissue and that fibrous tissue with neovascularization shows very strong contrast enhancement (more than 80% increase of signal intensity) and can be distinguished from fibrous tissue without neovascularization. One of their reports suggests that contrast-enhanced MR imaging is useful in assessing the status of the fibrous cap, especially in predicting plaque destabilization [57]. Investigating a kinetic model of dynamic contrast-enhanced MR imaging, they also found that the model could indicate the location and amount of neovasculature in carotid artery plaque [25]. Another trial evaluated the permeability of the vasa vasorum by observing the transfer constant (Ktrans) of the vessel wall; this constant is a kinetic parameter that indicates the speed of leakage of contrast media from vessels (Fig. 11.8). Adventitial permeability was significantly correlated with the amount of neovasculature, and adventitial Ktrans was associated with a high risk of atherosclerotic complications [26]. Images that provide functional or molecular information about carotid plaque have also been introduced. The function of atherosclerotic macrophages can be monitored using

Fig. 11.8 Permeability of the adventitia and density of the vasa vasolum. The transfer of contrast material from plasma to tissue over time is described by a kinetic model of dynamic contrastenhanced magnetic resonance (MR) imaging. The kinetic model could indicate the location and amount of neovasculature in the carotid artery plaque. The speed of contrast media leakage from vessels significantly correlated with the amount of neovasculature, and the increased speed of leakage from the adventitia was associated with a high risk of atherosclerotic complications


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ultra-small superparamagnetic particles of iron oxides (USPIO) that accumulate within macrophages by phagocytosis. In an experiment in hyperlipidemic rabbits, MR imaging was able to detect susceptibility effects created by a sufficient number of USPIO phagocytosed by macrophages in the atherosclerotic plaque of the aortic wall [37]. An in vivo study in humans showed that accumulation of USPIO in macrophages in predominantly ruptured and rupture-prone atherosclerotic lesions caused decreased signal in the in vivo MR images [27]. However, another report demonstrates no relationship between inflammation as measured by USPIO-enhanced signal changes and the degree of luminal stenosis [44]. New approaches require the use of a fibrin-specific paramagnetic molecular imaging agent to improve detection of occult microthrombi and early detection of vascular microthrombi, factors that predict stroke and heart attack. Effective molecular imaging has been established using fibrin-targeted nanoparticles of such an agent, gadolinium diethylenetriamine pentaacetic acid bis-oleate (Gd-DTPA-BOA), which improved detection and quantification of these occult microthrombi [50]. Angiogenic expansion of the vasa vasorum is a feature of progressive atherosclerosis, and antiangiogenic therapy is one treatment option for early atherosclerosis. Winter and colleagues suggested that antiangiogenic therapies may stabilize or regress plaques, and they introduced a molecular imaging method to visualize angiogenesis [51]. Their study reported that use of alpha (v)beta3 integrin- targeted paramagnetic nanoparticles enables noninvasive assessment of angiogenesis in early atherosclerosis for site-specific delivery of an antiangiogenic drug.

11.3.4.5 Application to Treatment Strategies Carotid endarterectomy is reported to be highly beneficial for patients with recent transient ischemic attacks or with nondisabling strokes and ipsilateral high grade (more than 70%) stenosis of the internal carotid artery [33]. However, because degree of stenosis is not a highly predictive marker of stroke risk, identifying plaque characteristics that are high risk factors may improve risk assessment and decisions regarding surgical or endovascular intervention. One study showed that intraplaque hemorrhage as detected by MR imaging predicts recurrent cerebrovascular events in patients with symptomatic high grade carotid stenosis. Results showed a high negative predictive value for recurrent ischemic events in the absence of intraplaque hemorrhages; their absence reduces the expected benefit from carotid endarterectomy [2]. Targeting surgery or stenting to those who would truly benefit would increase the efficiency of these techniques and reduce adverse effects for those who do not need surgical or endovascular intervention. Carotid stent placement can be performed rather easily when the plaque is stable. However, when the plaque has a thin fibrous cap, intraplaque hemorrhage, or a lipid-rich core, caution is needed and protective devices must be used to avoid cerebral embolism [42]. MR imaging of plaque may also be used to evaluate oral therapies, such as statins. Statins, or 3-hydroxy-3-methylglutaryl coenzyme A-reductase inhibitors downregulate important coregulatory signals involved in interactions between T cells and macrophages/ dendritic cells. Statins appear to be effective in primary stroke prevention, possibly by inhibiting the inflammatory activity of macrophages or the immune response [41]. Intensive

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therapy to lower lipids with statins reduces levels of low density lipoprotein cholesterol and improves plaque volume and composition in patients with cardiovascular disease. Plaque imaging is noninvasive and suitable for follow-up study of statin therapy. In patients with hypercholesterolemia, statins were reported to be associated with a reduction in the percentage of lipid-rich/necrotic cores within plaque as shown on noninvasive MR plaque imaging, whereas the overall plaque burden remained unchanged [47]. An ongoing study in Japan is using MR imaging to evaluate the percentage of change in carotid plaque volume and the change in plaque composition after statin therapy [30].

11.4 Future Perspectives Reliable prediction of future ischemic events and appropriate selection of treatment are the clinical goals for plaque imaging using MR imaging as well as computed tomography, US, and other methods. In particular, among asymptomatic cases with mild or moderate carotid stenosis, only high risk cases should undergo treatment. To achieve this goal, a large number of clinical cases must be examined. MR plaque imaging is expected to be a beneficial method for evaluating carotid plaque, particularly its vulnerability. However, disagreements among reports regarding study performance or image interpretation may require consensus guidelines. Methods of functional or molecular imaging of carotid plaque are expected to provide additional information for achieving clinical goals.

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30. Miyauchi K, Takaya N, Hirose T, Ikeda F, Kawamori R, Ohishi H, et al. Rationale and design of the carotid plaque in human for all evaluations with aggressive rosuvastatin therapy (CHALLENGER trial): evaluation by magnetic resonance imaging. Circ J. 2009;73:111–5. 31. Moody AR, Murphy RE, Morgan PS, Martel AL, Delay GS, Allder S, et al. Characterization of complicated carotid plaque with magnetic resonance direct thrombus imaging in patients with cerebral ischemia. Circulation. 2003;107:3047–52. 32. Nandalur KR, Hardie AD, Raghavan P, Schipper MJ, Baskurt E, Kramer CM. Composition of the stable carotid plaque: insights from a multidetector computed tomography study of plaque volume. Stroke. 2007;38:935–40. 33. North American Symptomatic Carotid Endarterectomy Trial Collaborators. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med. 1991;325:445–53. 34. North American Symptomatic Carotid Endarterectomy Trial (NASCET) Investigators. Clinical alert: Benefit of carotid endarterectomy for patients with high-grade stenosis of the internal carotid artery. National Institute of Neurological Disorders and Stroke Stroke and Trauma Division. Stroke. 1991;22:816–7. 35. Pignoli P, Tremoli E, Poli A, Oreste P, Paoletti R. Intimal plus medial thickness of the arterial wall: a direct measurement with ultrasound imaging. Circulation. 1986;74:1399–406. 36. Ross R. Atherosclerosis–an inflammatory disease. N Engl J Med. 1999;340:115–26. 37. Ruehm SG, Corot C, Vogt P, Kolb S, Debatin JF. Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits. Circulation. 2001;103:415–22. 38. Saam T, Hatsukami TS, Yarnykh VL, Hayes CE, Underhill H, Chu B, et al. Reader and platform reproducibility for quantitative assessment of carotid atherosclerotic plaque using 1.5T Siemens, Philips, and General Electric scanners. J Magn Reson Imaging. 2007;26:344–52. 39. Sabetai MM, Tegos TJ, Nicolaides AN, Dhanjil S, Pare GJ, Stevens JM. Reproducibility of computer-quantified carotid plaque echogenicity: can we overcome the subjectivity? Stroke. 2000;31:2189–96. 40. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation. 1995;92:1355–74. 41. Stoll G, Bendszus M. Inflammation and atherosclerosis: novel insights into plaque formation and destabilization. Stroke. 2006;37:1923–32. 42. Takayama K, Nakagawa H, Iwasaki S, Taoka T, Miyasaka T, Myouchin K, et al. Initial experience of using the filter protection device during carotid artery stenting in Japan. Radiat Med. 2008;26:348–54. 43. Takayama K, Taoka T, Nakagawa H, Myouchin K, Wada T, Sakamoto M, et al. Successful percutaneous transluminal angioplasty and stenting for symptomatic intracranial vertebral artery stenosis using intravascular ultrasound virtual histology. Radiat Med. 2007;25:243–6. 44. Tang TY, Howarth SP, Miller SR, U-King-Im JM, Li ZY, Walsh SR, et al. Correlation of carotid atheromatous plaque inflammation using USPIO-enhanced MR imaging with degree of luminal stenosis. Stroke. 2008;39:2144–7. 45. Taoka T, Iwasaki S, Nakagawa H, Sakamoto M, Fukusumi A, Takayama K, et al. Evaluation of arteriosclerotic changes in the intracranial carotid artery using the calcium score obtained on plain cranial computed tomography scan: correlation with angiographic changes and clinical outcome. J Comput Assist Tomogr. 2006;30:624–8. 46. Trivedi RA, U-King-Im JM, Graves MJ, Horsley J, Goddard M, Kirkpatrick PJ, et al. MRIderived measurements of fibrous-cap and lipid-core thickness: the potential for identifying vulnerable carotid plaques in vivo. Neuroradiology. 2004;46:738–43.


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47. Underhill HR, Yuan C, Zhao XQ, Kraiss LW, Parker DL, Saam T, et al. Effect of rosuvastatin therapy on carotid plaque morphology and composition in moderately hypercholesterolemic patients: a high-resolution magnetic resonance imaging trial. Am Heart J. 2008;155(584):e581–8. 48. Watanabe Y, Nagayama M, Suga T, Yoshida K, Yamagata S, Okumura A, et al. Characterization of atherosclerotic plaque of carotid arteries with histopathological correlation: Vascular wall MR imaging vs. color Doppler ultrasonography (US). J Magn Reson Imaging. 2008;28:478–85. 49. Watanabe Y, Uotani K, Nakazawa T, Higashi M, Yamada N, Hori Y, et al. Dual-energy direct bone removal CT angiography for evaluation of intracranial aneurysm or stenosis: comparison with conventional digital subtraction angiography. Eur Radiol. 2009;19:1019–24. 50. Winter PM, Caruthers SD, Yu X, Song SK, Chen J, Miller B, et al. Improved molecular imaging contrast agent for detection of human thrombus. Magn Reson Med. 2003;50:411–6. 51. Winter PM, Neubauer AM, Caruthers SD, Harris TD, Robertson JD, Williams TA, et al. Endothelial alpha(v)beta3 integrin-targeted fumagillin nanoparticles inhibit angiogenesis in atherosclerosis. Arterioscler Thromb Vasc Biol. 2006;26:2103–9. 52. Wintermark M, Jawadi SS, Rapp JH, Tihan T, Tong E, Glidden DV, et al. High-resolution CT imaging of carotid artery atherosclerotic plaques. AJNR Am J Neuroradiol. 2008;29:875–82. 53. Yamada N, Higashi M, Otsubo R, Sakuma T, Oyama N, Tanaka R, et al. Association between signal hyperintensity on T1-weighted MR imaging of carotid plaques and ipsilateral ischemic events. AJNR Am J Neuroradiol. 2007;28:287–92. 54. Yoshida K, Narumi O, Chin M, Inoue K, Tabuchi T, Oda K, et al. Characterization of carotid atherosclerosis and detection of soft plaque with use of black-blood MR imaging. AJNR Am J Neuroradiol. 2008;29:868–74. 55. Yuan C, Petty C, O’Brien KD, Hatsukami TS, Eary JF, Brown BG. In vitro and in situ magnetic resonance imaging signal features of atherosclerotic plaque-associated lipids. Arterioscler Thromb Vasc Biol. 1997;17:1496–503. 56. Yuan C, Beach KW, Smith LH Jr, Hatsukami TS. Measurement of atherosclerotic carotid plaque size in vivo using high resolution magnetic resonance imaging. Circulation. 1998;98:2666–71. 57. Yuan C, Kerwin WS, Ferguson MS, Polissar N, Zhang S, Cai J, et al. Contrast-enhanced high resolution MRI for atherosclerotic carotid artery tissue characterization. J Magn Reson Imaging. 2002;15:62–7. 58. Yuan C, Kerwin WS, Yarnykh VL, Cai J, Saam T, Chu B, et al. MRI of atherosclerosis in clinical trials. NMR Biomed. 2006;19:636–54. 59. Yuan C, Mitsumori LM, Beach KW, Maravilla KR. Carotid atherosclerotic plaque: noninvasive MR characterization and identification of vulnerable lesions. Radiology. 2001;221:285–99. 60. Yuan C, Mitsumori LM, Ferguson MS, Polissar NL, Echelard D, Ortiz G, et al. In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation. 2001;104:2051–6.

MR Imaging of Cerebral Aneurysms

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12.1 Saccular (Berry) Aneurysm Intracranially, saccular (berry) aneurysms predominate. They are round or lobulated focal eccentric protrusions that usually arise from arterial bifurcations and occasionally arise directly from the walls of nonbranching arteries. An aneurysm may have a narrow neck or arise from a broad-based opening that connects to the parent vessel. Saccular aneurysms develop at the point where the tunica media is congenitally thin or absent and the internal elastica of the arterial wall is extremely fragmented or absent. They develop and expand over time, and hemodynamic stress plays an important role in their formation and growth. Rinne and Hernesniemi estimated that the risk of metachronous aneurysm formation in patients with previous subarachnoid hemorrhage (SAH) is approximately 2 or 3 times larger than risk in the general population [33]. Approximately 90% of aneurysms occur in the anterior portion of the circle of Willis, most commonly in the anterior communicating artery (ACoA) complex (Figs. 12.1 and 12.2). Aneurysms at the middle cerebral artery (MCA) bifurcation and origin of the posterior communicating artery (PCoA) are also common (Figs. 12.3 and 12.4). Between 5 and 10% of intracranial aneurysms occur in the posterior circulation, generally at the top of the basilar artery (BA) (Fig. 12.5), origin of the superior cerebellar artery (SCA) (Fig. 12.6), or origin of the posterior inferior cerebellar artery (PICA). Cerebral aneurysms are frequently associated with various vascular variations, such as fenestration (Fig. 12.7), azygos anterior cerebral artery (ACA), and persistent primitive trigeminal artery (Fig. 12.8). Angiographic and autopsy studies reported the prevalence of intracranial saccular aneurysms between 0.2 and 8.9% of population [3, 7, 15, 30]. Approximately 15–30% of patients with aneurysms have more than one when examined [41]. Risk factors include polycystic kidney disease, smoking, hypertension, aortic coarctation, Ehlers-Danlos syndrome, fibromuscular dysplasia, and family history of saccular aneurysms. In a review of the literature concerning screening for familial aneurysms, Schievink et al. estimated that

N. Kurihara Department of Radiology, National Hospital Organization Sendai Medical Center, 2-8-8 Miyagino, Miyagino-ku, Sendai 983-8520, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_12, © Springer-Verlag London Limited 2010

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346 Fig. 12.1 Common locations of intracranial aneurysms. About 90% of aneurysms arise from anterior portion of the circle of Willis or middle cerebral artery (MCA) bifurcation

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ACA

ACoA

MCA ICA PCoA PCA SCA BA PICA

VA

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Fig. 12.2 Anterior communicating artery (ACoA) aneurysm. Maximum-intensity projection (MIP) image (a) shows subtle protrusion (arrow) at right end of the ACoA. It may be difficult to differentiate focal kinking from an aneurysm, while volume rendering (VR) image (b) proves to be an aneurysm more clearly

in families with more than one affected proband, first-degree relatives have a 17–44% incidence of aneurysms detectable by screening [37]. Although most aneurysms remain small and asymptomatic, occasionally, symptoms develop following rupture with SAH, expansion with mass effect on surrounding structures, or development of thrombus and embolic events.

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12 MR Imaging of Cerebral Aneurysms

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Fig. 12.3 MCA aneurysm. Coronal MR angiography (MRA) (a) demonstrates a small aneurysm (arrow) at bifurcation of rt. MCA, whereas axial image (b) cannot visualize it clearly

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Fig. 12.4 Aneurysm at origin of posterior communicating artery (PCoA). T1- and T2-weighted image (a, b) shows oval flow void (arrow) at left side of the suprasellar cistern. MRA reconstructed by only left-sided vessels (c) shows a large aneurysm protruding posteriorly from the supraclinoid internal carotid artery (ICA). Aneurysm represents lower intensity than the parent vessel probably due to intraluminal turbulent flow. Source image (d) demonstrates that the aneurysm originates from the origin of fine PCoA (arrow)

348 Fig. 12.5 Basilar top aneurysm. MRA of the posterior circulation shows aneurysm (arrow) protruding superiorly at the terminal end of the basilar artery (BA)

Fig. 12.6 Aneurysm at origin of superior cerebellar artery (SCA). MRA of the posterior circulation shows an aneurysm with broad neck (arrow) at the origin of rt. SCA

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Fig. 12.7 Aneurysm at fenestration. Coronal VR image shows an aneurysm (arrow) protruding at proximal end of the distal BA fenestration

Fig. 12.8 Aneurysm of persistent primitive trigeminal artery. This patients presented sudden onset of diplopia. Lateral view of MRA of left-sided vessels demonstrates a large aneurysm (arrow) protruding at the origin of persistent primitive trigeminal artery (arrowheads)

According to the 1990 International Cooperative Study, frequent sites of ruptured aneurysms include the ACoA (39%), internal carotid artery (ICA) (including the PCoA and ophthalmic segment of the ICA) (30%), MCA (22%), and vertebrobasilar circulation (8%) [19, 20]. Aneurysms tend to rupture from their dome, and those that rupture tend to be irregular and have daughter sacs of variable wall thickness. In general, aneurysms that are

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statistically less likely to bleed have diameters smaller than 7 mm, and bleeding likelihood is even less in those with diameters 3 mm or less. However, a fourth of all deaths related to cerebrovascular disease result from SAH after aneurysmal rupture. The high morbidity and mortality from these ruptures demand their accurate detection and appropriate treatment.

12.1.1 MR Imaging The appearance of aneurysms on MR images is quite variable. Signal on spin-echo sequences depends on the direction and rate of intraluminal flow as well as the presence of thrombus and calcification within the aneurymal wall. A patent aneurysm with rapid flow inside is seen as a well delineated mass with high velocity signal loss (flow void) on both T1- and T2-weighted images (Fig. 12.4). Intravenous contrast injection typically does not enhance patent aneurysms with high flow, but aneurysms with slow and turbulent flow may appear iso- or even hyperintense on MR images (Fig. 12.9) and show variable enhancement following contrast

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Fig. 12.9 Large patent aneurysm of rt. ICA. Although T2-weighted image (a) shows large mass with flow void (arrow) at rt. parasellar region, T1-weighted image (b) shows intermediate signal (arrow). Aneurysm exhibits lower intensity than surrounding vessels on MRA (c) and source image (d) due to intraluminal turbulent flow. Lt. ICA and MCA aneurysms are also noted (c, arrowhead)

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Fig. 12.10 ACoA aneurysm with contrast enhancement. Suprasellar region aneurysm (arrow) exhibits heterogenous intensity on both T1- and T2-weighted images (a, b). It shows enhancement following contrast administration (c)

administration (Fig. 12.10). Gradient-refocused sequences show the patent lumen of the aneurysm as a region of high intensity. Partially thrombosed aneurysms demonstrate complex signal. Variably intense multi-laminated clot can be seen surrounding the patent lumen with high velocity signal loss (Fig. 12.11), and occasionally, acutely thrombosed aneurysms may be isointense with the brain parenchyma and mimic intracranial masses.

12.1.2 MR Angiography MR angiography (MRA) is a less invasive tool to evaluate intracranial vasculature. Timeof-flight (TOF) and phase-contrast (PC) imaging are the two major MRA techniques that do not require contrast media. To create angiographic images, TOF imaging uses the inflow of fully magnetized spins into saturated stationary tissue, and PC imaging uses bipolar pulse

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Fig. 12.11 Partially thrombosed aneurysm of rt. MCA T2-weighted image (a) shows low intense mass (arrow) in rt. Sylvian vallecula, whereas T1-weighted image (b) shows low and intermediate mixed intensity (arrow). Although MRA (c) visualizes only patent lumen of the aneurysm (arrow), source and reconstructed images (d, e) demonstrate surrounding thrombosed portion (arrowheads)

sequences to detect the phase shifts caused by blood flowing through magnetic field gradients. As TOF imaging offers better spatial resolution and shorter imaging time than PC imaging, three-dimensional (3D) TOF methods are now commonly used for examination of cerebral aneurysms, and PC imaging is mainly applied to evaluation of cerebral veins. Advances in the postprocessing of MR images and use of high-tesla systems have permitted MRA quality approaching that of digital subtraction angiography (DSA). MRA demonstrates aneurysms as round, oval, or lobulated masses of high signal intensity usually

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arising from an arterial bifurcation. Previous studies have suggested that MRA allows identification of most cerebral aneurysms larger than 3 mm in diameter [9, 12–14, 34–36, 38, 42, 45–47], and aneurysms of 1–2 mm may be detectable [22, 31]. Additionally, MRA may visualize aneurysms that are undetected by DSA. Vascular loops and overlap often prevent accurate identification of aneurysms on DSA, whereas MRA allows retrospective manipulation of 3D data into numerous projections. Thus, such 3D images permit 360° observation of the aneurysms and partially reconstructed images without overlap of surrounding vessels can help depict the aneurysm. Aneurysms of the ACoA are easily demonstrated on rotated images in axial view (Fig. 12.2) and aneurysms of the MCA bifurcation, in coronal view (Fig. 12.3). Partially reconstructed lateral view without overlap of contralateral vessels is useful for evaluating aneurysms of the ICA-PCoA (Figs. 12.4 and 12.12). Source and multiplanar reconstruction (MPR) images can often clarify whether a small protrusion at the ICA-PCoA involves an aneurysm or infundibular dilatation; source and MPR images may depict small aneurysms not seen on projection images (Fig. 12.13). According to Ross and

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Fig. 12.12 Right ICA-PCoA aneurysm. Partial MIP lateral image of only right-sided vessels (a) clearly visualize ICA-PCoA aneurysm (arrow) compared to that of whole vessels (b)

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Fig. 12.13 Infundibular dilatation mimics aneurysm. Lateral MRA (a) shows small protrusion like aneurysm (arrow), however sagittal reconstructed image (b) demonstrates PCoA (arrowheads) connecting to the apex of protrusion, providing diagnosis of infundibular dilatation

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associates, observing source and MPR images in addition to projection images may increase the sensitivity of identifying aneurysms as much as 14% [35]. In clinical practice, it is important to correlate rendered images with source images of MRA. Finding an aneurysm on MRA requires attention to the exact location, size of the entire aneurysm and neck, shape, presence or absence of blebs, direction of the aneurysmal dome, presence or absence of intra-aneurysmal thrombus, and relation to surrounding vessels. Careful observation is also needed of the presence or absence of other aneurysms. Aneurysms in unusual locations, such as at the distal ACA, terminal bifurcation of the ICA, and horizontal or insular portion of the MCA, must not be overlooked. The major reconstruction method of MRA is maximum-intensity projection (MIP), which projects only the brightest pixels along a ray projected through the dataset. An MIP image does not take spatial resolution into account and displays the vasculature without depth cues [5]. Thus, stereoscopic viewing with two images rotated several degrees is recommended. Another common reconstruction method is volume rendering (VR), which incorporates the entire dataset into a 3D image that enables visualization of the vascular surface and intravascular details and preserves spatial relationships [17]. However, an inappropriate threshold setting can result in loss of visualization of some intracranial arteries, particularly small peripheral vessels of low intensity, which can potentially lead to failure in identifying an aneurysm. Detectability of aneurysms is not so different between MIP and VR images. However, some studies have suggested that MRA utilizing the VR technique provides better visualization of intracranial aneurysms than does the MIP algorithm [24, 44] (Fig. 12.2). In particular, VR imaging is excellent in terms of detecting daughter lobules, a substantial indicator of a prior rupture or the threat of a rupture [40] (Fig. 12.14).

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Fig. 12.14 Advantages of VR images to MIP images. MIP image (a) shows aneurysms at left ICA and MCA (arrow). Furthermore, VR image (b) demonstrates small bleb (arrowhead) at anteromedial wall of lt. ICA aneurysm


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Three-tesla (T) MR units have been used increasingly. The stronger magnet approximately doubles the signal-to-noise ratio of 1.5 T. Although 1.5-T MR systems have provided MRA excellent enough to identify small aneurysms, the better spatial resolution and visualization of distal vessels [10] of 3.0-T MRA can provide more reliable and detailed information for treatment planning. Clear depiction of giant (>25 mm) and large aneurysms still permits a challenge for 3D TOF MRA. Intravoxel spin-phase dispersion and saturation associated with slow and turbulent flow often prevent adequate demonstration of entire aneurysms. In addition, the high signal of intraluminal thrombus or perianeurysmall hemorrhage may mimic the flow signal. Both contrast-enhanced 3D images and dynamic contrast-enhanced MRA can be good methods to visualize the lumen with slow flow [16] (Fig. 12.15). Source images of contrast-enhanced 3D TOF MRA can help distinguish thrombus from patent lumen. Dynamic contrast-enhanced MRA eliminates the highly intense thrombus by subtraction of the precontrast images. After aneurysmal clipping, MR is probably the most noninvasive modality for postoperative assessment. Although some ferromagnetic artifacts from clips may interfere with identification of the neck remnant, obscuration of the brain is significantly less than with computed tomography. Endovascular embolization with detachable coils has been used increasingly for both ruptured and unruptured intracranial aneurysms. However, it is generally agreed that long-term follow-up monitoring of coiled aneurysms is mandatory because coil compaction may occur and aneurysms may recur [6, 27, 43]. Yamada and associates reported that TOF MRA targeted to depict coiled intracranial aneurysms was useful for follow-up because it could visualize the residual lumen of the aneurysm better than DSA and was less invasive [48] (Fig. 12.16).

12.2 Dissection and Dissecting Aneurysm Arterial dissection occurs as blood extends into the vessel wall, usually between the intima and media and, rarely, between the media and adventitia. Dissection between the intima and media usually causes luminal narrowing, even occlusion. If intramural hematoma in the false lumen extends toward the adventitia, an aneurysmal dilatation, or “dissecting aneurysm,” forms. Intracranial dissections are more common in the posterior than anterior circulation, in which case patients typically present with suboccipital headache or neck pain. Dissection of one vertebral artery (VA) occasionally extends to the BA and/or contralateral VA (Fig. 12.17). Dissections in the anterior circulation are rare and typically involve the subcallosal segment of the ACA or the distal supraclinoid segment of the ICA, which often extends to the ICA bifurcation and even into the horizontal portion of the MCA. Arterial dissection occurs spontaneously or associated with trauma. Patients with dissection may develop neurological deficits from vessel occlusion, SAH, or mass effect on adjacent structures.

356 Fig. 12.15 Cavernous internal carotid large aneurysm. MRA (a) shows rt. ICA large aneurysm with heterogenous intensity. Most of intraaneurysmal signal is low on source image (b), however homogenously enhanced with contrast administration (c), which suggests slow flow within the aneurysm

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Clinical course is variable. As patients who present with SAH tend to suffer rebleeding, especially within 1 week [2, 26, 39], immediate treatment should be required. The natural course of dissecting aneurysm without SAH is relatively benign [21, 49], and some patients show spontaneous resolution without significant neurological deficit. However, even in patients with ischemic onset, SAH may occur later.

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12 MR Imaging of Cerebral Aneurysms Fig. 12.16 Residual flow within postembolized aneurysm. MRA (a) shows small irregular high intensity (arrow) medial to the lt. ICA. Source image (b) demonstrates residual flow (arrow) around neck of the embolized aneurysm

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12.2.1 MR Imaging Dissection/dissecting aneurysm usually shows various signal changes on MR images. On spin-echo sequences, intramural hematoma has a striking appearance as an eccentric or occasionally circumferential crescentric, curvilinear, or band-like focus of high intensity. The intramural hematoma is more clearly demonstrated on T1- than T2-weighted image; however, acute hematoma usually shows intermediate signal and subacute hematoma shows high intensity that makes it conspicuous (Fig. 12.18).As intraluminal inflow artifacts often simulate intramural hematoma, use of proximal presaturation pulse is indispensable. Residual lumen narrows with time, which reflects absent or diminished flow void; on cross-sectional images, the narrowed lumen is located eccentrically. Another useful finding for dissection is focal arterial dilatation that is disproportionate to the neighboring part of the artery. Nagahata’s team designed basiparallel anatomic scanning (BPAS) MR imaging, the postprocessing of which required only 2-cm thick, heavily T2-weighted coronal imaging parallel to the clivus with gray-scale reversal. It is a quite simple and good method to assess the surface appearance of the vertebrobasilar artery (Fig. 12.19) [28].

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Fig. 12.17 Bilateral VA dissection. Initial MRA (a) shows pearl and string like luminal irregularity of lt. distal VA (arrow) and double lumen with different intensities of rt. VA (arrowheads). Follow-up MRA at 6 months later (b) demonstrates resolution of rt. VA dissection and occlusion of lt. terminal VA distal to posterior inferior cerebellar artery (PICA) origin

12.2.2 MR Angiography Dissection/dissecting aneurysm demonstrates several appearances in MRA. Segmental luminal irregular narrowing with or without neighboring dilatation is frequently seen and corresponds to “string sign” or “pearl and string sign” on conventional angiography (Fig. 12.17); the affected vessel generally shows decreased signal; and fusiform dilatation or luminal narrowing may occasionally be observed (Fig. 12.20). However, these findings are often not pathognomonic for dissection. Observation of an intra-arterial double lumen is diagnostic for dissection. However, MIP imaging rarely demonstrates a double lumen because the lower signal of the false lumen may be lost by the imaging procedure. Thus, assessment of source images should be very important in evaluating the possibility of dissection; their frequent visualization of two separated lumens with different signals is a reliable finding for dissection (Figs. 12.18 and 12.20). Nevertheless, a false lumen without flow usually shows low intensity resembling that of the cerebrospinal fluid (CSF) and may be missed even on source images. In these cases, contrast-enhanced imaging may be useful by demonstrating wall enhancement (Fig. 12.21). Source images sometimes show an intra-arterial linear structure of low intensity that looks like an intimal flap, but distinguishing it from low intensity artifacts caused by turbulent or laminar flow may be difficult [11]. Detection of the enlarged external diameter of the affected vessels is useful in diagnosing dissection; source and MPR images often clarify the regional increase of arterial outer diameter, but MIP images show only narrowing at the same region. Source images provide both anatomical and flow information (Figs. 12.19 and 12.20). Delineation of both vessel

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Fig. 12.18 Chronological signal change of intramural hematoma. The patient presented rt. occipital sudden headache. On the next day, MRA (a) shows irregular stenosis (arrow) of rt. VA just distal to the origin of PICA. On source and coronal multiplanar reconstruction (MPR) images (b, c), the lumen is divided into two different intensities (arrow). T1-weighted image (d) shows diminished flow void of true lumen (arrowhead) displaced by intramural hematoma with intermediate signal (arrow). On follow-up image on the eighth day (e), intramural hematoma turns into high intensity. Narrowed lumen with flow void locates eccentrically

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Fig. 12.19 Comparison BPAS, MRA and source images. Partial MIP MRA image (a) shows focal severe stenosis of rt. VA, whereas BPAS (b) discloses fusiform dilatation of the same site (arrow). Source image (c) also shows focal dilatation with decreased signal (arrow). 3D-heavily T2-weighted image (d) demonstrates separated lumen with different signal (arrow: false lumen, arrowhead: true lumen)

outline and internal separated lumen by 3D spin-echo and 3D heavily T2-weighted images should also contribute to diagnosis of dissection (Figs. 12.19 and 12.21). Continued dynamic change in angiographic findings during the first few months after symptom onset have been reported [21, 39, 49]. Follow-up angiography may reveal definite signs of arterial dissection (pearl and/or string sign, fusiform dilatation, double contrast appearance) that were absent in some cases on initial angiography at admission. Such change indicates the need for follow-up angiography in cases of dissection and even those suspicious for dissection, but conventional angiography is too invasive to perform repeatedly. MRA can also demonstrate the sequential changes of dissection, which are classified into four categories−regression of abnormal findings with only minimal narrowing or irregularity; occlusion; persistent aneurysmal dilatation; and exacerbation of aneurysmal

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Fig. 12.20 Chronological change of dissecting aneurysm. Initial MRA (a) shows focal fusiform dilatation of lt. distal VA (arrow). Source images (b, c) disclose double lumen with different signal. After conservative treatment, the patient sometimes complained headache. MRA obtained after 1 year (d) shows focal dilatation (arrow) almost same as (a), however source images (e, f) demonstrate unquestionable enlargement of dissecting aneurysm, especially false lumen with lower intensity. Then he was treated by VA trapping

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Fig. 12.21 Left VA dissection. MRA (a) shows focal stenosis and continuous dilation of lt. VA (arrow). On source image of stenotic portion (b), low intense false lumen and dilatation of whole diameter may be overlooked, however contrast-enhanced 3D-SPGR image (c) clearly demonstrates arterial dilatation with thick wall enhancement. 3D-heavily T2-weighted image (d) shows intraluminal double lumen with high and low signal

dilatation. In the dynamic period, as long as 2 or 3 months after symptom onset, strict follow-up with MRA is needed until stabilization of the findings for the affected vessel. Although most dissected lesions seem likely to stabilize within a few months, some may require longer observation (Fig. 12.20) [29]. Diagnosis of dissections is more troublesome in the anterior circulation than the posterior. The limited surrounding subarachnoid space makes analysis of source images too complicated. A small finding, such as mild irregularity on MRA or focal arterial signal change on T1-weighted imaging, especially in young patients, requires follow-up study within 1 week for diagnosis (Fig. 12.22).

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Fig. 12.22 Dissection of anterior cerebral artery (ACA). (a) Diffusion-weighted image obtained 4 h after onset of right hemiparesis shows left medial frontal high intense area, compatible with acute infarction. MRA at the same time (b) shows no remarkable abnormality of lt. ACA. However, follow-up MRA after 1 week (c) demonstrates irregular stenosis in the subcallosal portion of lt. ACA (arrow), resulting in diagnosis of dissection. Follow up MRA after 2 month (d) shows remaining irregularity with focal aneurymal dilatation (arrow) while resolution of stenosis

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Dissection must be differentiated from other causes of luminal irregularity or narrowing, such as atherosclerotic disease and arteritis, and unless visualization of a double lumen is clear, differentiation may be difficult. Atherosclerotic disease occurs in the elderly and usually affects the entire arterial system; the outer diameter of arteries is generally not increased. In contrast to dissection, arteritis also involves multiple vessels. Differential diagnosis may be further assisted by the absence of clinical symptoms that suggest acute dissection.

12.3 Fusiform Aneurysm Fusiform aneurysms arise along the arterial trunk with ectasia of the entire vessel circumference, usually occur in atherosclerotic vessels, and are frequently associated with hypertension and advancing age. Damage to the media results in arterial stretching and elongation. Another group of fusiform aneurysm is caused by inherited/ acquired vasculopathies, including Marfan syndrome, Ehlers-Danlos syndrome, neurofibromatosis type 1, vasculitis with viral infection, immunodeficiency disease, and collagen vascular disorders, such as systemic lupus erythematosus (SLE). The nonatherosclerotic fusiform aneurysm occurs in younger patients and is proven to have disrupted or fragmented internal elastic lamina and intima; dissection is a common cause of the acute form. Pathological studies indicate that most fusiform aneurysms are related to dissecting phenomena and that dissection plays a role in their growth [4, 25, 32]. Fusiform aneurysms typically affect the basilar and/or vertebral arteries whether or not they are atherosclerotic (Fig. 12.23). When ectasia of the BA is prominent, the term “megadolichobasilar artery” is used. Fusiform aneurysm is also seen in the anterior circulation and commonly involves the cavernous or supraclinoid ICA (Fig. 12.24). Rupture of a fusiform aneurysm is uncommon.

12.3.1 MR Imaging and MR Angiography MR images usually show enlargement of arterial flow voids for a long segment, but internal signal varies according to flow velocity, turbulence, and presence or absence of clot (Fig. 12.23). On MRA, fusiform aneurysms often have bizarre shapes that include serpentine and giant configurations (Fig. 12.25). Contrast-enhanced study can improve visualization of fusiform aneurysms when slow and turbulent flow induces signal decrease; residual lumen with slow flow strongly enhances.

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Fig. 12.23 Fusiform aneurysm of BA. MRA (a) shows fusiform dilatation along BA (arrow). The aneurysm is represented as high on T1- and mixed intensity on T2-weighed images (b, c). Note right suprasellar artifact induced by aneurysmal clip

Fig. 12.24 Fusiform aneurysm of ICA. MRA shows irregular fusiform dilatation of siphon of lt. ICA (arrow)

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Fig. 12.25 Fusiform aneurysm of bilateral vertebral artery (VA). MRA shows bizarre dilatation of bilateral VA with heterogeneous signal reduction (arrow)

12.4 Infectious Aneurysm Aneurysms of infectious or inflammatory origin are classically referred to as mycotic even in cases unrelated to fungal infection, and they account for 2–4% of intracranial aneurysms. Although the most common cause of infectious aneurysms is infective endocarditis (IE), they may occur associated with other disease, such as congenital heart disease (especially right-to-left shunt), meningitis, septic thrombophlebitis, and direct invasion of the cerebral arteries by adjacent infection. Infectious agents may be bacterial, fungal, or syphilitic, and recently, increased infections have been related to human immunodeficiency virus (HIV) and its associated infections. Infectious aneurysms typically arise peripheral to the first bifurcation of a major vessel and are also seen in distal MCA branches apart from bifurcation. Multiple or bilateral aneurysms are not uncommon, but in a study by Corr et al., 70% of infectious aneurysms were found to be single, and a third of them were located proximal to the first bifurcation of a major vessel [8]. Infectious aneurysms caused by IE are related to impaction of septic emboli in the intima of a peripheral artery and resulting development of arteritis, focal mural necrosis, and aneurysmal dilatation. In those caused by adjacent infection, such as meningitis, the adventitia is involved first, followed by the muscularis and the internal elastic lamina. Most infectious aneurysms are pseudoaneurysms. In infectious aneurysms, headache and fever are the most common presenting symptoms. SAH and parenchymal hemorrhage may occur, and in contrast to noninfectious

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aneurysms, parenchymal hemorrhage and focal signs are more common than SAH, and recurrent bleeding is more frequent [18]. Occasionally, patients may present with cerebral ischemia. Mortality from infectious aneurysm is significantly higher in association with meningitis, fungal etiology, and vertebrobasilar location [18].

12.4.1 MR Imaging and MR Angiography Typical infectious aneurysms have fusiform shape, but saccular lesions are also seen (Fig. 12.26). MRA often cannot delineate infectious aneurysms because they are small, peripherally located, and frequently thrombosed. T2*- and susceptibility-weighted images help by demonstrating thrombosed aneurysm or focal hemorrhage as black dots (Fig. 12.27).

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Fig. 12.26 Infectious aneurysm. Diffusion-weighted image (a) shows high intensity areas representing acute/subacute infarction in bilateral cerebral hemisphere. T2-weighed coronal image (b) shows nodular flow void of lt. frontoparietal region (arrow). High intense area surrounding flow void is also seen. MRA (c) shows lt. distal MCA aneurysm (arrow)

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Fig. 12.27 Infectious aneurysm on T2*-weighted image. The patient was suffering from the infectious endocarditis. T2*-weighted images (a, b) show multiple low intense nodule deep in the cerebral sulci, probably correspond to thrombosed infectious aneurysms

MR images can also help to localize aneurysms by demonstrating associated hemorrhage, infarction, and abscess. Abscesses locate at the gray-white matter junction, accompanying surrounding edema and mass effect. When MR imaging demonstrates evidence of parenchymal or subarachnoid hemorrhage in patients at risk for infectious aneurysms, we should consider the possibility of infectious lesions. Although initial examination may show no abnormality, repeated MRA can demonstrate the development of infectious aneurysms. Sequential studies every 2–3 weeks during and after intravenous antibiotic therapy are recommended [1]. Any growth in aneurysmal size during therapy or persistence after therapy should indicate the need for surgery.

12.5 Traumatic Aneurysm Traumatic intracranial aneurysms are rare, making up fewer than 1% of all intracranial aneurysms, but more than 30% are identified in children. Most are pseudoaneurysms. Traumatic lesions usually occur following direct injury, such as penetrating trauma or contiguous skull fracture, and less frequently as a result of closed head injury, such as shearing injury or impaction of an artery against a dural fold or skull edge. For example, the distal ACA is forced against the falx cerebri, the SCA against the tentorium, and the MCA against the sphenoidal ridge. This action can lead to dissection of the damaged vascular layers that results in expansion of the affected site and formation of an aneurysm. Traumatic aneurysms can present with subacute or delayed bleeding or other complications, typically 1 or 2 weeks after injury but possibly as long as months after. Mortality for

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Fig. 12.28 Traumatic aneurysm of distal ACA. The patient fell down from the fourth floor of the building 1 year ago. T2-weighted sagittal image (a) shows atrophy of the corpus callosum with chronic hemorrhage. MRA (b) shows aneurysm of rt. distal ACA (arrow)

patients harboring these aneurysms may be as high as 50%. Best outcomes are associated with prompt diagnosis and surgical management rather than conservative treatment [23].

12.5.1 MR Imaging and MR Angiography For evaluating vascular lesions in patients who have undergone trauma, MRA should fully cover the distal ACA and its branches (Fig. 12.28). MRA usually visualizes a traumatic aneurysm as a fusiform-shaped mass, but saccular shapes may be seen. T2*- and susceptibility-weighted images can demonstrate subtle hemorrhage over the cerebral surface, which may help to find aneurysms.

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46. White PM, Wardlaw JM, Easton V. Can noninvasive imaging accurately depict intracranial aneurysms? A systematic review. Radiology. 2000;217:361–70. 47. Wilcock D, Jaspan T, Holland I, Cherryman G, Worthington B. Comparison of magnetic resonance angiography with conventional angiography in the detection of intracranial aneurysms in patients presenting with subarachnoid haemorrhage. Clin Radiol. 1996;51:330–4. 48. Yamada N, Hayashi K, Murao K, Higashi M, Iihara K. Time-of-flight MR angiography targeted to coiled intracranial aneurysms is more sensitive to residual flow than is digital subtraction angiography. AJNR Am J Neuroradiol. 2004;25:1154–7. 49. Yoshimoto Y, Wakai S. Unruptured intracranial vertebral artery dissection. Clinical course and serial radiographic imagings. Stroke. 1997;28:370–4.

MR Imaging of Vascular Malformations

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13.1 Arteriovenous Malformation (AVM) 13.1.1 Clinical Overview Arteriovenous malformations (AVMs) are a congenital abnormality in which the arteries and veins on the surface of the brain or in the parenchyma connect directly without capillary vessels. The lesions comprise three components − feeding arteries, a nidus, which replaces the normal arterioles and capillaries with a low resistance high flow vascular bed, and draining veins. Histologically, the veins usually have thickened collagenous walls and appear “arterialized.” The pathological blood vessels are separated by brain parenchyma that often shows gliosis, hemosiderin deposition, and foci of calcification [11, 22]. AVM are generally considered to develop from the malfunction of differentiation of primitive vessels in an embryo at about 3 weeks, can form in any part of the brain, and typically involve the region from the brain surface to the white matter. The malformation shows a conical form based at the brain surface. Ninety percent of these lesions arise in the cerebral hemisphere and the remaining 10%, in the posterior fossa [15, 16, 49]. Intracranial hemorrhage is the most frequent initial presentation of AVM [2]. Brown’s group reported that in 26 patients with AVM, 17 (65%) presented with intracranial hemorrhage; five (19%), with epileptic seizure; and four (15%), without symptoms [8, 9]. Other symptoms include headache, pulsatile tinnitus, and some focal neurological deficit [47]. The most common intracranial hemorrhage due to AVM is cerebral (intraparenchymal), although subarachnoid and intraventricular hemorrhages can occur. Arteriovenous malformations are often found in the second to third decade of life, and most cases develop by age 40 [5, 8]. AVM are the main cause of juvenile primary intracranial hemorrhages and should always be considered in the diagnosis of hemorrhagic apoplexy of young patients, especially in cases with cerebral hemorrhage.

A. Umetsu Department of Diagnostic Radiology, Tokohu University School of Medicine, 1-1 Seiryo-machi, Aoba-ku Sendai, Miyagi 980-8574, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_13, © Springer-Verlag London Limited 2010

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There is much research into the natural history of these malformations. Overall risk of initial bleeding in patients with AVM is 2–3% per year [47]. Mortality from the first hemorrhage is between 10 and 30%, though some data suggest it may be lower, and 10–20% of survivors have long-term disability [47]. Several parameters are reported to correlate with hemorrhagic risk of AVM, but these remain controversial. Seizures [7, 21] or prior hemorrhage [24] and AVM of small maximal diameter [21, 62] or volume [18] may be predictors of higher risk of hemorrhage. The major treatment options for patients with AVM are surgery, transcatheter embolization, radiosurgery, and their combination. Preoperative embolization has become part of AVM therapy, especially for larger lesions [47].

13.1.2 Characteristic Imaging Features and Diagnostic Points of AVM 13.1.2.1 Findings in Cases with and Without Bleeding The diagnostic points in evaluating imaging features of AVMs differ slightly depending on the presence or absence of bleeding. In cases with bleeding, important considerations are the volume of the hematoma, distortion of the brain parenchyma around the hematoma, evidence and degree of increasing intracranial pressure with or without hydrocephalus, and mass effect or brain herniation. These findings can usually be evaluated on conventional plain computed tomography (CT). AVM often exist near the brain surface, an infrequent site of hypertensive cerebral hemorrhage, and should be considered adequately when atypical cerebral hemorrhage, such as subcortical, subarachnoid, or intraventricular hemorrhage, is seen clinically or radiologically. Especially in younger patients, AVM should be a primary candidate, and further examinations, such as CT with contrast agent or magnetic resonance (MR) imaging, are needed. Since compression by large hematomas may conceal abnormal vessels, examination may be necessary after the hematoma is resolved. In cases without hemorrhage, familiarity with characteristic findings of AVM on conventional images is important because nonspecific signs like seizures or progressive neurologic deficits can occur as initial symptoms of AVM. On plain CT, the dilated vessels of AVM may be seen as structures on the brain surface that are isodense or that show slightly high density. Calcification can be noted as high density in the vascular wall or brain parenchyma in about 25–30% of cases [49]. Areas of low density from ischemia or gliosis may appear around the AVM. In some cases, diffuse or localized brain atrophy can be seen. On contrast-enhanced CT, dilated vessels and the AVM nidus strongly enhance.

13.1.2.2 MR Imaging Findings of AVM The signal intensity of AVM on MR imaging depends on the velocity of blood flow in the lesion. Most AVM are delineated as a collection of small low signals on T1- (T1-weighted

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image, T1WI) and T2-weighted (T2-weighted image, T2WI) images because of the phenomenon of flow void. The degree and extent of contrast enhancement of the lesion on conventional spin-echo enhanced T1WI are influenced by both the contrast material used and flow phenomenon. Vessels are probably enhanced with contrast medium on gradient-echo (GRE) T1WI, which has short echo time (TE). GRE 3-dimensional (3D) T1WI sequence with contrast enhancement (T1 CE-fast field-echo (FFE) sequence on a 3-tesla Philips Achieva imager; Philips Medical Systems, Best, the Netherlands) enables detailed observation of AVM. Magnetic resonance angiography (MRA), computed tomographic angiography (CTA), and magnetic resonance digital subtraction angiography (MRDSA) are useful special sequences for evaluating AVM. MRA techniques include time of flight (TOF), phase contrast (PC), and contrast-enhanced first pass. TOF MRA requires no contrast materials, is commonly used in brain MRA, and can usually depict feeders and drainers as dilated vascular structures with high signal and the nidus as a nodular lesion with complicated signals. TOF MRA may not clearly depict slow-flow lesions. Large residual hematomas which show high intensity on T1WI may conceal abnormal vessels. In such cases, phasecontrast and contrast-enhanced methods can be used to reinforce TOF findings. With high spatial resolution, CTA can demonstrate the abnormal vascular structures of AVM, and associated calcification and the anatomical relationship between lesions and adjacent bones are more clearly evaluated on CTA than MRA. With recent advancements in multi-detector row CT scanners, CTA has exceeded MRA in both temporal and spatial resolution. The main fault of CTA is that its use requires contrast medium and radiation exposure. The higher temporal resolution of MRDSA than conventional contrast-enhanced MRA allows evaluation of the hemodynamics of AVM. Like conventional digital subtraction angiography (DSA), MRDSA can demonstrate the sequential appearance of individual AVM components, such as feeders, the nidus, and drainers. A recently developed 3D data acquisition method (4-dimensional (4D) time-resolved angiography using keyhole (TRAK) sequence on a 3-tesla Philips Achieva imager; Philips Medical Systems, Best, the Netherlands) allows acquisition of hemodynamic data with higher spatial resolution and is expected to provide DSA-like images of equal quality to those from catheter angiography in the near future.

AVM Grading System The grading system Spetzler and Martin developed in 1986 to evaluate AVM lesions is widely used [59]. A lesion is assigned one to five points for size (1 point, 6 cm); an additional point is given for location within the eloquent cortex (sensorimotor, language, and visual cortex; hypothalamus and thalamus; internal capsule; brain stem; cerebellar peduncles; deep cerebellar nuclei); and another point is given for deep venous drainage. The score is the sum of the points for each category. The score is thought to correlate with morbidity and surgery outcome; total scores of 1–5 correspond with AVM Grades I–V. Hamilton et al. reported permanent major neurological morbidity rates of 0% for Grades I through III AVM that increase significantly to 21.9% in patients with Grade IV AVM and 16.7% in patients with Grade V AVM [23].

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Although AVM classification and evaluation have been based on the findings of catheter angiography, noninvasive imaging techniques, such as MR imaging, can now provide enough information for Spetzler-Martin grading. The nidus is well delineated on sectional images of conventional MR imaging as an area with punctuated and tortuous structures of increased and decreased signal intensities [42, 46]. The size of the nidus can exactly be measured on MR imaging. Especially on 3D images (for example, T1 CE FFE sequence on Philips scanner) with multiplanar reconstruction, the diameter of the nidus in any direction and the volume can be measured even if the nidus is irregularly shaped. The border of the nidus with adjacent feeding and draining vessels may sometimes be difficult to distinguish. Paging display of MRA source images may aid differentiation: the feeding arteries are usually depicted as larger curvilinear structures with apparent high signal intensity and the draining veins as even more dilated, whereas the nidus is shown as an area of brain substance with aggregation of more minute punctiform and tortuous structures of modestly high signal within it (Fig. 13.1h). MR imaging is very useful in evaluating the neurological eloquence of a lesion’s location. Conventional MR images allow identification of the cerebral gyri and evaluation of their positional relationship with the lesion. Diffusion tensor imaging permits more precise evaluation of white matter by depicting bundles of nerve fibers, such as the pyramidal tract or the visual pathway [40]. Vascular dilatation in the brain parenchyma noted on MR imaging, MRA, or CTA may suggest deep venous drainage, which is directly delineated by MRDSA with high temporal resolution.

Associated Aneurysms Intracranial associated aneurysms are found in about 7–17% of patients with AVM [47]. They may develop on the artery feeding the AVM or at typical locations in the circle of Willis. It is unclear whether the natural history of AVM-associated intracranial aneurysms differs from that of usual aneurysms. As there is no natural historical information regarding this point in the literature, the rationale for treatment of aneurysms not associated with AVM is used [47]. It is very important that neuroradiologists point out associated aneurysms on pretreatment images because AVM and aneurysm may be treated at the same time depending on the location of the lesions.

Follow-Up Study After Treatment Follow-up study is necessary after radiosurgery for AVM because complete obstruction takes 2–3 years [27, 48, 52], and it is necessary to confirm that there is no residual lesion after surgical resection or endovascular treatment. Catheter angiography has been the standard for these follow-up studies [47], but noninvasive imaging, such as MR imaging that includes MRA and/or MRDSA, should be appropriate for the follow-up studies [39].

13.1.3 Case of Arteriovenous Malformation (AVM) A 31-year-old man with no personal or familial history presented with sudden onset of restlessness, followed by consciousness disturbance. Plain CT (Fig. 13.1a–c) shows an inhomo-

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Fig. 13.1 Case of arteriovenous malformation (AVM). (a–c) Axial plain computed tomography (CT). (d) Axial T1WI. (e) Axial T2WI. (f) Axial fluid-attenuated inversion recovery (FLAIR). (g) Axial view of time of flight-magnetic resonance angiography (TOF-MRA) maximum intensity projection. (h) Source image of MRA. (i) Lateral view of magnetic resonance digital subtraction angiography (MRDSA). (j) Color-coded map image

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geneous abnormal structure with slightly high density compared to the gray matter in the left temporo-occipito-parietal area (arrows). The lesion contains many small spotty or nodular calcifications, and tubular structures represent dilated draining veins around the lesion (arrowheads). There is no evidence suggesting acute hemorrhage. Conventional MR images (T1WI, T2WI, and fluid-attenuated inversion recovery (FLAIR); Fig. 13.1d–f) delineate an aggregated small flow void that suggest the nidus and a dilated tubular flow void that represents the feeding arteries and draining veins. Small high signals on T1WI (Fig. 13.1d) reflect calcification. Areas of high intensity on T2WI (Fig. 13.1e) and FLAIR (Fig. 13.1f) of the brain parenchyma in or around the lesion, suggest ischemia or gliosis. Dilated vessels are a characteristic finding of AVM on TOF MRA (axial view of maximum intensity projection, Fig. 13.1g). MRA source image (Fig. 13.1h) demonstrates lower signal intensity of the nidus (arrowheads) and draining veins (arrows) than the feeding arteries (double arrows), which show prominent high intensity. This lower intensity of the nidus and drainers is


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p robably due to the influence of slow and complicated blood flow. Phase-contrast MRA or contrast-enhanced MRA would show the nidus and draining veins with higher signal intensity. MRDSA (4D time-resolved angiography using keyhole (4D TRAK) sequence on a 3-tesla Philips Achieva imager; Philips Medical Systems, Best, the Netherlands; Fig. 13.1i) depicts the nidus (arrowhead) and enlarged draining veins in early phase. A color-coded map image (Fig. 13.1j) shows the direction of the white-matter fibers (red, right-left; green, anterio-posterior; blue, cranio-caudal) derived from diffusion-weighted imaging (DWI) and T2WI using a 3D anisotropy contrast method [43, 60]. The positional relationship is easily evaluated between the lesion and the bundles of important white-matter fibers, such as the blue pyramidal tract (arrows) and the green optic radiation (arrowheads). The lesion involves the optic radiation on the ipsilateral side. This lesion was regarded as grade IV (3 points by size >6 cm and 1 point by location within an eloquent, visual cortex) by Spetzler and Martin grading [59].

13.2 Dural Arteriovenous Fistula (dAVF) 13.2.1 Definition and Overview Dural arteriovenous fistulas (dAVF) are abnormal arteriovenous shunts at the dura or tentorium. Meningeal branches of the internal (ICA) or external carotid arteries (ECAs) dilate to create an abnormal vascular network in the wall of the venous sinus. Nidus formation is not seen [29]. The cause of dAVF is unclear, but they are thought to be acquired secondary to occlusion of the sinus by thrombosis [12, 28], operation, or tumor compression. Stenosis or occlusion of the venous sinus results in the expansion of very small arteriovenous channels and subsequent fistula formation [4, 44]. About 60% of dAVF occur at the transverse/sigmoid sinus and 12%, at the cavernous sinus; they can also occur apart from the sinuses, such as at the frontal base, tentorium, or cerebral convexity [4]. Carotid-cavernous fistula (CCF) involves shunting between the ICA and cavernous sinus and is classified into direct and indirect types by the connection. The direct type is caused primarily by trauma and by aneurysmal rupture and systemic diseases with vascular vulnerability, such as fibromuscular hyperplasia, Ehlers-Danlos syndrome, and neurofibromatosis. In the indirect type, meningeal branches of the ECA or ICA connect to the cavernous sinus; dural AVF at the cavernous sinus is sometimes handled clinically as the indirect type of CCF [36]. Clinical symptoms of dAVF depend on the site of the lesion. Typical clinical features of dAVF of the cavernous sinus include unilateral ocular proptosis, conjunctival hyperemia, pulsatile vascular bruit, external ophthalmoplegia, and ocular pain. The external ophthalmoplegia or ocular pain develops only with the occlusion of draining veins, such as the superior ophthalmic vein. Reduced blood flow through the dAVF shunt often produces milder symptoms in cavernous sinus dAVF than those of direct CCF [36].

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Common symptoms of transverse/sigmoid sinus dAVF include tinnitus, headache, and dizziness [19]. Increased venous pressure from higher shunt volume and retrograde flow can produce consciousness disturbance or convulsion, and intracranial hemorrhage can occur from venous rupture [33]. In a consecutive single-center cohort study, van Dijk’s group reported the annual risk for hemorrhage as 8.1% in patients with dAVF with persistent cortical venous reflux [61]. Intracranial hypertension from impeded venous return can produce headache, visual disturbance, dysarthria, gait disturbance, and cognitive impairment [13, 20, 26]. However, asymptomatic cases of dAVF are also discovered on MR imaging and MRA screening studies [3].

13.2.2 Classification and Treatment Strategies 13.2.2.1 Classification Systems Among many classifications of dAVF that have been advocated, those by Borden’s [6] and Cognard’s [14] teams are commonly used because they categorize the fistulas by their patterns of venous return, which are important for developing therapies. Borden et al. [6] specified three dAVF classifications: Type I: drainage into dural venous sinuses or meningeal veins; Type II: drainage into dural venous sinuses or meningeal veins with retrograde leptomeningeal drainage; and Type III: only retrograde leptomeningeal drainage. Cognard et al. [14] specified five categories: Type I: drainage into a sinus with normal antegrade flow; Type II: drainage into a sinus with reflux; Type III: drainage into a cortical vein without venous ectasia; Type IV: drainage into a cortical vein with venous ectasia; and Type V: drainage into spinal perimedullary veins. They further indicated three subclassifications of Type II, for retrograde venous drainage into: IIa: sinus(es) only; IIb: cortical vein(s) only; and IIa+b: sinus(es) and cortical vein(s). The indication for aggressive treatment for dAVF depends on clinical symptoms and findings of cerebral angiography. Active treatment is usually indicated in cases with massive intracranial hemorrhage, consciousness disturbance, convulsion from hemorrhage or venous congestion, or features of increased venous pressure. Treatment is generally not indicated in cases with minimal symptoms and no demonstrable retrograde venous flow, and an asymptomatic case with no abnormal retrograde venous flow should be followed without therapy. Nevertheless, active treatment should be considered in cases with marked retrograde venous flow even if the patients are asymptomatic [63].

13.2.2.2 Treatment Options and Prognosis dAVF are treated by operation, endovascular therapy, gamma-knife therapy, and their combination. Recent technical advances in endovascular and gamma-knife therapies decrease the need for surgery. The annual rate of mortality is 10.4%, of hemorrhage, 8.1%, and nonhem-


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orrhagic neurological deficit, 6.9%, in patients with dAVF with cortical venous reflux (Type IIb, III, or IV in Cognard’s classification) [61]. In contrast, patients with no venous reflux have good prognoses, and most (98.5%) have benign and tolerable levels of disease [56].

13.2.3 Points and Characteristic Features of Diagnostic Imaging 13.2.3.1 Findings on Conventional Images As described, the clinical signs and severity of dAVF are diverse. In cases with nonspecific signs, like mild headache, dizziness, dementia, consciousness disturbance, or convulsion with no local neurological sign, correct diagnosis is clinically difficult by symptoms only. Such cases require imaging studies for screening and the diligence of the neuroradiologist in pointing out findings that suggest dAVF on conventional images. Even subtle findings should not be overlooked. In most cases of dAVF, the diagnostic ability of plain CT is very limited, except in evaluating volume and associated distribution of hematoma. Rarely, in some cases of dAVF with cortical venous reflux, a particular curvilinear pattern of calcification may be noted in the corticomedullary junction at the bottom of cerebral sulci [35, 64]. In cases with venous congestion, low density on plain CT and high intensity on T2WI of MR imaging reflect brain edema localized in the subcortical area and must not be misunderstood as simply chronic ischemic changes in the brain. In cases of dAVF at the cavernous sinus with relatively high flow, abnormal flow void around the ICA in the cavernous sinus and dilatation of the superior ophthalmic vein may be seen. However, superior ophthalmic veins sometimes appear dilated in healthy subjects; the specificity of this finding is low. Enlargement of the pituitary gland from elevated pressure in draining veins with size normalization after endovascular treatment has been reported [55] and may represent a distinguishing feature of intracranial dAVF. The diagnosis of dAVF on conventional MR imaging is even more difficult in other areas; e.g., dilated cortical veins may be seen as serpentine flow void on the brain surface in cases with cortical venous reflux.

13.2.3.2 MRA and MRDSA for the Diagnosis of dAVF TOF MRA permits visualization of dilated meningeal branches and shunted sinus and veins. Abnormal delineation of the veins and sinus on MRA requires careful scrutiny of MRA source images. Noguchi et al. and Hirai et al. suggested that MRA source images of patients with dAVF depicted multiple curvilinear or nodular structures adjacent to the sinus wall and areas in the sinus, all showing high intensity. Those adjacent to the sinus wall may correspond to meningeal branches of feeding arteries, and those in the sinus may correspond to secondary increased flow via an arteriovenous shunt. These findings have both high sensitivity and specificity [25, 45]. Abnormal findings can only be detected with MRA

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and negative findings, with conventional CT and MR imaging. However, careful diagnosis is important because these findings on MRA can also be seen in healthy subjects [51]. The gold standard in diagnostic imaging of dAVF is catheter angiography, which demonstrates feeding arteries, shunting site, and draining veins in detail. As mentioned, MRDSA has high temporal resolution, and it has become a very useful tool for evaluating the existence of the abnormal shunting flow [34].

13.2.4 Case of dAVF A 66-year-old male patient whose chief complaint was indistinct vision demonstrated papilloedema and elevated intracranial pressure on examination. Conventional T1WI and T2WI images (not shown) indicated no abnormal finding. Maximum-intensity-projection images of TOF MRA (Fig. 13.2a) demonstrated the transverse and sigmoid sinuses with high signal, which suggested abnormally high flow, and both occipital arteries were dilated. MRA source image (Fig. 13.2b) delineated multiple small structures of high intensity adjacent to the sinus wall (arrow) and areas of high intensity in the sinus. MRDSA (Fig. 13.2c) visualized the transverse and sigmoid sinuses in arterial phase and slightly visualized the superior sagittal sinus. Meningeal branches of the occipital arteries were involved in the shunt, and the nidus was not demonstrated. This dAVF was regarded as Type I on Borden classification [6] and Type IIa on Cognard classification [14].

13.3 Vein of Galen Malformation 13.3.1 Clinical Overview The vein of Galen malformation is a vascular abnormality that involves aneurysmal dilatation of the vein. There are two pathophysiological types: (1) arteriovenous shunts in which one or a few arteries connect directly to the dilated vein of Galen and (2) AVM whose nidus is in the thalamus or midbrain [58]. In the first type, which is a vein of Galen malformation by strictest definition, the draining vein is thought to be the embryonic median prosencephalic vein, which should differentiate into the vein of Galen [10]. In the second type, the vein of Galen is dilated by the draining flow of the AVM. Most cases develop during the neonatal period or infancy. The high shunt volume can cause cardiac failure. Obstructive hydrocephalus can result from aqueductal compression by the dilated vein, and communicating hydrocephalus can occur from impaired cerebrospinal fluid (CSF) absorption caused by increased venous pressure. Endovascular embolization is the primary therapeutic choice. Lasjaunias et al. reported that follow-up after endovascular therapy demonstrated that about 70% of the cases in their series were neurologically normal [30].

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Fig. 13.2 Case of dural arteriovenous fistulas (dAVF). (a) Axial view of TOF-MRA maximum intensity projection. (b) Source image of MRA. (c) Lateral view of MRDSA

13.3.2 Points of Diagnostic Imaging On plain CT, a round mass-like lesion with isodensity or slightly high density compared to brain parenchyma is noted in or around the pineal region. On contrast-enhanced CT, the lesion enhances as strongly as normal vessels. Thrombus may exist in the lesion. Hydrocephalus is often accompanied. MR imaging demonstrates a large rounded masslike lesion with varying intensities (flow void to high intensity). MRA also shows a lesion with varying intensities that depend on flow velocity and turbulence.

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13.3.3 Case of Vein of Galen Malformation A. 1-year-old male patient with head trauma and no neurological signs. CT screening scan showed a rounded mass-like lesion of about 2.5 cm in diameter in the upper pineal area. T1WI (not shown) and T2WI (Fig. 13.3a) demonstrated almost no signal in the lesion. Contrast-enhanced T1WI (Fig. 13.3b) demonstrated a flow-related artifact (arrows) in the direction of the phase encoding, which suggested the lesion was a vascular structure. Many flow voids around the structure represented tortuous dilated vessels (Fig. 13.3c, arrow). On MRA (Fig. 13.3d–f), the left and right medial posterior choroidal arteries and thalamoperforate arteries derived from the proximal portion of the bilateral posterior cerebral arteries are dilated and connect to the vascular lesion. The nidus is apparent on the right side. The vascular lesion drains into the straight sinus and persistent falcial sinus.

13.4 Cavernous Malformation 13.4.1 Clinical Overview Cavernous malformation is also called cavernous angioma, cavernous hemangioma, and occult vascular malformation. “Occult” specifies that it is not depicted by catheter angiography, so more lesions have been found with the installation of more CT and MR imaging scanners. Histologically, cavernous malformations comprise closely apposed dilated vascular channels with little or no intervening brain parenchyma, and the channels are often occluded. Cavernous malformations include hematomas of varying stages as well as thrombus and calcification. The malformations have a clear border with the brain parenchyma, with a characteristic peripheral rim of hemosiderin deposition in the surrounding brain tissue. Gliosis is also seen in the surrounding brain. There is no dilated feeding artery or draining vein [22]. Postmortem studies indicate that cavernous malformations account for approximately 5–13% of all cerebrovascular malformations, with estimated total incidence of 0.5% [50]. Familial cases inherited in an autosomal dominant pattern have been reported [37]. An important external factor for malformation is past history of radiation therapy for brain tumor [1]. Eighty percent of lesions are in the cerebral hemisphere [38]. Multiple lesions are found in 15–50%, and 85% of familial cases have multiple lesions [41]. The risk of symptomatic hemorrhage is about 1% per year [67]. Cavernous malformations may manifest asymptomatically as incidental lesions, with seizures, or with hemorrhage and mass effect producing a wide range of neurologic symptoms depending on the location of the lesion [37]. Most patients develop symptoms between the second and sixth decades of life. Patients with significant hemorrhage, neurological focal signs, or uncontrollable epilepsy are candidates for surgery. Cavernous malformations and venous anomalies may coexist;

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Fig. 13.3 Case of vein of Galen malformation. (a) Axial T2WI. (b) Axial T1WI with contrast material. (c) Axial T2WI. (d) Axial view of TOF-MRA maximum intensity projection. (e) Lateral view of TOF-MRA maximum intensity projection. (f) Source image of MRA

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Rabinov reported such association in 8–33% of cases [53], a very important preoperative finding because associated venous anomalies should be left untouched during surgery.

13.4.2 Points of Diagnostic Imaging Plain CT depicts most cavernous malformations as inhomogeneous nodules with mixed low and high densities. Areas of low density represent thrombus or old hematoma, and high density represents calcification or fresh hemorrhage. CT with contrast enhancement shows only slight enhancement in the periphery of the lesions, if any. Compared to findings in other brain tumors, both mass effect and perifocal edema are usually slight in cavernous malformations, a helpful finding for differential diagnosis. Perifocal edema can be seen in the malformation with fresh hemorrhage. MR imaging findings are very characteristic. On T2WI, the so-called “popcorn-like” appearance of small components with high and low signal intensities reflects various stages of hemorrhage. The rim, which is hypointense from hemosiderin deposition, surrounds the lesion on T2WI or GRE T2*WI. The hypointense rim is less prominent on fast spin-echo T2WI, which is commonly used for routine imaging, because of the technique’s lower sensitivity for magnetic susceptibility effect. Therefore, GRE T2*WI is more useful for detecting hemosiderin deposition and delineating the characteristic features of this lesion. This sequence can also detect small multiple lesions. No abnormal vascular finding can be detected on MRA, CTA, MRDSA, and catheter angiography. Susceptibility-weighted imaging (SWI; or Venous BOLD on a 3-tesla Philips Achieva imager; Philips Medical Systems, Best, The Netherlands) is a newly developed technique that maximizes the sensitivity to susceptibility effects by combining a long-TE, high resolution, fully flow-compensated, 3D GRE sequence with filtered phase information in each voxel [31, 57]. The sensitivity of SWI for detecting small cavernous malformations is higher than that of T2WI or T2*WI [17]. As mentioned, it is important that the neuroradiologist detect the coexistence of venous anomalies, which is depicted very clearly on SWI. Yun’s group reported that there is a high probability of cavernous malformations when lesions with recent hemorrhage have perilesional high intensity on T1WI [66]; this finding may be useful for differentiating cavernous malformation from other hemorrhagic lesions although its exact mechanism is unclear.

13.4.3 Case of Cavernous Malformation A 46-year-old male patient suffering from progressing right hemiparesis T1WI (Fig. 13.4a) demonstrated the inhomogeneous high intensity of a mass lesion at the left corona radiata. T2WI (Fig. 13.4b) showed the lesion with mixed high and low intensities and peripheral low intensity. Perifocal edema was represented by slightly low signal on T1WI and high signal on T2WI. Marked low intensity was seen on T2*WI (Fig. 13.4c) and SWI (Fig. 13.4d.). T1WI with contrast material (Fig. 13.4e) showed no enhancement in the cavernous malformation, except for linear enhancement near the lesion that represented venous malformation (arrow).

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Fig. 13.4 Case of cavernous malformation. (a) Axial T1WI. (b) Axial T2WI. (c) Axial T2*WI. (d) Axial susceptibility-weighted imaging (SWI) (partial minimum intensity projection). (e) Axial T1WI with contrast material

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13.5 Capillary Telangiectasia 13.5.1 Clinical Overview Capillary telangiectasias, also called capillary malformations, are usually detected incidentally at autopsy, and their estimated prevalence at autopsy is 0.4% [54]. The lesions are composed of pathologically dilated capillary vessels and intervening brain parenchyma that is normal brain tissue with no gliosis or hemorrhagic change. They are most commonly located in the pons and can sometimes be found in the supratentorial compartment or spine. Most of the lesions are clinically silent [37].

13.5.2 Points of Diagnostic Imaging Capillary telangiectasias have been recognized with increasing frequency as MR scanners have developed and their use has become widespread. The lesions usually show iso/slightly low intensity on T1WI and iso/slightly high intensity on T2WI, and they are often undetectable. On T1WI with contrast material, mild homogenous enhancement is seen. A valuable finding for diagnosis is the marked low intensity of lesions on GRE T2*WI, which is attributed not to hemosiderin deposition, but to the blood oxygen level-dependent contrast that derives from the increase in deoxyhemoglobin from low blood flow in the lesion [32]. Especially, the high spatial resolution of SWI permits detection of this low intensity [65]. Correct differential diagnosis of capillary telangiectasia from other enhancing lesions, such as metastasis, lymphoma, subacute infarction, active demyelination, and cavernous malformation, is quite important because most of these lesions require further examination and treatment, whereas capillary telangiectasia needs no other treatment. Homogenous enhancement without mass effect and change in surrounding brain is a point that differentiates capillary telangiectasia from neoplastic lesions. Low intensity on T2*WI within the lesion, where contrast enhancement is seen, is also important for differentiating capillary telangiectasia from other lesions, including cavernous malformation, which demonstrates a hypointense rim from hemosiderin deposition. Lace-like enhancement shown by some capillary telangiectasias reflects ectatic capillary vessels and aids differential diagnosis.

13.5.3 Case of Capillary Telangiectasia The patient is a 51-year-old woman with no symptoms whose lesion was identified on MR imaging at routine physical examination. The lesion was not confirmed histologically, but capillary telangiectasia was highly suspected based on MR imaging findings. T1WI (Fig. 13.5a) shows irregular slightly low intensity at the lower part of the right caudate

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Fig. 13.5 Case of capillary telangiectasia. (a) Axial T1WI. (b) Axial T2WI. (c) Axial T1WI with contrast material. (d) Axial T2*WI

head. T2WI (Fig. 13.5b) demonstrates mildly high intensity. Mild reticular enhancement is seen on T1WI with contrast material (Fig. 13.5c). Obvious low intensity is depicted inside the enhanced area on T2*WI (Fig. 13.5d).

Abbreviations AVMs CCF CE CSF

Arteriovenous malformations Carotid-cavernous fistula Contrast enhanced Cerebrospinal fluid

390

CT CTA dAVF DSA DWI ECA FFE GRE ICA MR MRA PC SWI T1WI T2WI TE TOF TRAK 3D 4D

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Computed tomography Computed tomographic angiography Dural arteriovenous fistulas Digital subtraction angiography Diffusion-weighted imaging External carotid artery Fast field-echo Gradient echo Internal carotid artery Magnetic resonance Magnetic resonance angiography Phase contrast Susceptibility-weighted imaging T1-weighted image T2-weighted image Echo time Time of flight Time-resolved angiography using keyhole 3-dimensional 4-dimensional

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10. Campi A, Rodesch G, Scotti G, Lasjaunias P. Aneurysmal malformation of the vein of Galen in three patients: clinical and radiological follow-up. Neuroradiology. 1998;40:816–21. 11. Challa VR, Moody DM, Brown WR. Vascular malformations of the central nervous system. J Neuropathol Exp Neurol. 1995;54:609–21. 12. Chaudhary MY, Sachdev VP, Cho SH, Weitzner I Jr, Puljic S, Huang YP. Dural arteriovenous malformation of the major venous sinuses: an acquired lesion. AJNR Am J Neuroradiol. 1982; 3:13–9. 13. Chimowitz MI, Little JR, Awad IA, Sila CA, Kosmorsky G, Furlan AJ. Intracranial hypertension associated with unruptured cerebral arteriovenous malformations. Ann Neurol. 1990; 27:474–9. 14. Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, Casasco A, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology. 1995;194:671–80. 15. Crawford PM, West CR, Chadwick DW, Shaw MD. Arteriovenous malformations of the brain: natural history in unoperated patients. J Neurol Neurosurg Psychiatry. 1986;49:1–10. 16. Crawford PM, West CR, Shaw MD, Chadwick DW. Cerebral arteriovenous malformations and epilepsy: factors in the development of epilepsy. Epilepsia. 1986;27:270–5. 17. de Souza JM, Domingues RC, Cruz LC Jr, Domingues FS, Iasbeck T, Gasparetto EL. Susceptibility-weighted imaging for the evaluation of patients with familial cerebral cavernous malformations: a comparison with t2-weighted fast spin-echo and gradient-echo sequences. AJNR Am J Neuroradiol. 2008;29:154–8. 18. Duong DH, Young WL, Vang MC, Sciacca RR, Mast H, Koennecke HC, et al. Feeding artery pressure and venous drainage pattern are primary determinants of hemorrhage from cerebral arteriovenous malformations. Stroke. 1998;29:1167–76. 19. Fermand M, Reizine D, Melki JP, Riche MC, Merland JJ. Long term follow-up of 43 pure dural arteriovenous fistulae (AVF) of the lateral sinus. Neuroradiology. 1987;29:348–53. 20. Gelwan MJ, Choi IS, Berenstein A, Pile-Spellman JM, Kupersmith MJ. Dural arteriovenous malformations and papilledema. Neurosurgery. 1988;22:1079–84. 21. Graf CJ, Perret GE, Torner JC. Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg. 1983;58:331–7. 22. Graham DI, Lantos PL. Greenfield’s neuropathology. 6th ed. London: Arnold; 1997. 23. Hamilton MG, Spetzler RF. The prospective application of a grading system for arteriovenous malformations. Neurosurgery. 1994;34:2–6; discussion 6–7. 24. Hartmann A, Mast H, Mohr JP, Koennecke HC, Osipov A, Pile-Spellman J, et al. Morbidity of intracranial hemorrhage in patients with cerebral arteriovenous malformation [see comment]. Stroke. 1998;29:931–4. 25. Hirai T, Korogi Y, Ikushima I, Shigematsu Y, Morishita S, Yamashita Y. Usefulness of source images from three-dimensional time-of-flight MR angiography after treatment of cavernous dural arteriovenous fistulas. Radiat Med. 2003;21:205–9. 26. Hurst RW, Bagley LJ, Galetta S, Glosser G, Lieberman AP, Trojanowski J, et al. Dementia resulting from dural arteriovenous fistulas: the pathologic findings of venous hypertensive encephalopathy. AJNR Am J Neuroradiol. 1998;19:1267–73. 27. Karlsson B, Lindquist C, Steiner L. Prediction of obliteration after gamma knife surgery for cerebral arteriovenous malformations. Neurosurgery. 1997;40:425–30. 28. Lasjaunias P, Chiu M, ter Brugge K, Tolia A, Hurth M, Bernstein M. Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg. 1986;64:724–30. 29. Lasjaunias P, Lopez-Ibor L, Abanou A, Halimi P. Radiological anatomy of the vascularization of cranial dural arteriovenous malformations. Anat Clin. 1984;6:87–99. 30. Lasjaunias PL, Chng SM, Sachet M, Alvarez H, Rodesch G, Garcia-Monaco R. The management of vein of Galen aneurysmal malformations [erratum appears in Neurosurgery. 2007;60 (4 Suppl 2):393]. Neurosurgery. 2006;59:S184–94.

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31. Lee BC, Vo KD, Kido DK, Mukherjee P, Reichenbach J, Lin W, et al. MR high-resolution blood oxygenation level-dependent venography of occult (low-flow) vascular lesions. AJNR Am J Neuroradiol. 1999;20:1239–42. 32. Lee RR, Becher MW, Benson ML, Rigamonti D. Brain capillary telangiectasia: MR imaging appearance and clinicohistopathologic findings. Radiology. 1997;205:797–805. 33. Malik GM, Pearce JE, Ausman JI, Mehta B. Dural arteriovenous malformations and intracranial hemorrhage. Neurosurgery. 1984;15:332–9. 34. Meckel S, Maier M, Ruiz DS, Yilmaz H, Scheffler K, Radue EW, et al. MR angiography of dural arteriovenous fistulas: diagnosis and follow-up after treatment using a time-resolved 3D contrast-enhanced technique. AJNR Am J Neuroradiol. 2007;28:877–84. 35. Metoki T, Mugikura S, Higano S, Ezura M, Matsumoto Y, Hirayama K, et al. Subcortical calcification on CT in dural arteriovenous fistula with cortical venous reflux. AJNR Am J Neuroradiol. 2006;27:1076–8. 36. Miller NR. Diagnosis and management of dural carotid-cavernous sinus fistulas. Neurosurg Focus. 2007;23:E13. 37. Mohr JP, Choi DW, Grotta JC, Weir B, Wolf PA. Stroke: pathophysiology, diagnosis, and management. Philadelphia, PA: Churchill Livingstone; 2004. 38. Moran NF, Fish DR, Kitchen N, Shorvon S, Kendall BE, Stevens JM. Supratentorial cavernous haemangiomas and epilepsy: a review of the literature and case series. J Neurol Neurosurg Psychiatry. 1999;66:561–8. 39. Mori H, Aoki S, Okubo T, Hayashi N, Masumoto T, Yoshikawa T, et al. Two-dimensional thick-slice MR digital subtraction angiography in the assessment of small to medium-size intracranial arteriovenous malformations. Neuroradiology. 2003;45:27–33. 40. Mori S, van Zijl PC. Fiber tracking: principles and strategies – a technical review. NMR Biomed. 2002;15:468–80. 41. Moriarity JL, Wetzel M, Clatterbuck RE, Javedan S, Sheppard JM, Hoenig-Rigamonti K, et al. The natural history of cavernous malformations: a prospective study of 68 patients. Neurosurgery. 1999;44:1166–71; discussion 1172–63. 42. Mukherji SK, Quisling RG, Kubilis PS, Finn JP, Friedman WA. Intracranial arteriovenous malformations: quantitative analysis of magnitude contrast MR angiography versus gradientecho MR imaging versus conventional angiography. Radiology. 1995;196:187–93. 43. Nakada T, Nakayama N, Fujii Y, Kwee IL. Clinical application of three-dimensional anisotropy contrast magnetic resonance axonography. Technical note. J Neurosurg. 1999;90:791–5. 44. Nishijima M, Takaku A, Endo S, Kuwayama N, Koizumi F, Sato H, et al. Etiological evaluation of dural arteriovenous malformations of the lateral and sigmoid sinuses based on histopathological examinations. J Neurosurg. 1992;76:600–6. 45. Noguchi K, Melhem ER, Kanazawa T, Kubo M, Kuwayama N, Seto H. Intracranial dural arteriovenous fistulas: evaluation with combined 3D time-of-flight MR angiography and MR digital subtraction angiography. AJR Am J Roentgenol. 2004;182:183–90. 46. Nussel F, Wegmuller H, Huber P. Comparison of magnetic resonance angiography, magnetic resonance imaging and conventional angiography in cerebral arteriovenous malformation. Neuroradiology. 1991;33:56–61. 47. Ogilvy CS, Stieg PE, Awad I, Brown RD Jr, Kondziolka D, Rosenwasser R, et al. Recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. Circulation. 2001;103:2644–57. 48. Oppenheim C, Meder JF, Trystram D, Nataf F, Godon-Hardy S, Blustajn J, et al. Radiosurgery of cerebral arteriovenous malformations: is an early angiogram needed? AJNR Am J Neuroradiol. 1999;20:475–81. 49. Osborn A. Diagnostic cerebral angiography. Philadelphia, PA: Lippincott Williams & Wilkins; 1999.


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Cerebral Venous Malformations

14

Akio Fukusumi

14.1 Classification of Cerebral Vascular Malformations A classification of cerebral vascular malformations based on microscopic features has been made by Russell and Rubinstein [27], into: (1) capillary telangiectases; (2) cavernous angiomas; (3) venous malformations; and (4) arteriovenous malformations. Okazaki [20] categorized three basic types comprising capillary telangiectasia, venous malformation, and arteriovenous malformation, in reference to the artery-capillary-vein continuum. The pathological distinction between capillary telangiectasia and venous malformation is unclear, and what should be considered transitional forms occur not infrequently. McCormick [14] classified these into four major types along with the transitional forms. From a pathophysiological point of view, cerebral vascular malformations may be divided into two major groups: those characterized by high flow and arteriovenous shunts and those characterized by slow flow and infrequent arteriovenous shunts [8, 36]. It should be emphasized that transitional forms between these groups may be encountered, such as venous angiomas with an arterial component and arteriovenous shunting. Different types of cerebral vascular malformation may occasionally coexist in the same area in the same patient (Table 14.1) [7, 8].

14.2 Terminology of Venous Malformations Krayenbuhl and Yasargil introduced the radiologic features of so-called venous angioma, giving the name “arteriovenous racemose angioma” in their textbook “cerebral angiography” in 1968 [10]. In the pre-CT era, cerebral medullary venous malformation (MVM)


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Table 14.1 Pathophysiological classification of cerebral vascular malformations [7] Those that involve feeding arteries and draining veins (easily demonstrable angiographically) Superficial type (pial or superficial AVM): With involvement of mostly cortical gray matter (and subjacent white matter) Deep or central type (deep or central AVM): With involvement of subcortical gray matter and adjacent white matter Medullary type (AVM with medullary component): With involvement of primarily medullary arteries and veins (Classical pyramid-shaped AVMs are mostly a combination of superficial and medullary types) Those that primarily involve capillaries Capillary malformation Rendu-Osler-Weber disease Louis Bar syndrome Those that primarily involve veins Medullary venous malformation With involvement of medullary vein only (Sturge-Weber disease should also be included here) With capillovenous component With medullary arterial component With arterial component (This should not be confused with an AVM with medullary component) Cavernous venous malformation Phlebectasia or varix (most of those cases, if not all, are MVMs) Any combination of the above

was believed to be a rare cerebral lesion. Since the radiological reports of MVMs by Wolf et al. [35] and by Constans et al. [3], using the term “cerebral venous angioma,” a number of publications have appeared describing the typical angiographic features of venous malformations. Huang et al. [8] proposed the term MVM instead of “angioma,” which has the connotation of a neoplasm, because this entity always consists in a part of the malformation involving medullary venous components. Lasjaunias et al. [11] proposed the term “developmental venous anomalies” (DVAs), instead of “venous angiomas,” since the so-called venous angiomas are only “venous deviations.” The term MVM will be used in this chapter.

14.3 Histology Histologically, MVMs consist of two major components: (1) thin-walled vessels of different sizes without significant quantities of smooth muscle or elastic tissue, but usually with thickened and hyalinized walls; and (2) intervening neural tissue [27].

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However, in exceptional cases, gross hemorrhage, hemosiderin deposits indicating previous hemorrhage, focal gliosis, neural ischemia and/or mineralization (usually calcification) may be found within the intervening neural parenchyma or in the vicinity of the lesion [15, 24].

14.4 Etiology Although the precise etiology of MVMs is unknown, these lesions are probably not true vascular malformations, but instead represent extreme anatomic variants or DVAs [11]. Based on microscopic observations, Courville first documented small angiomatous malformations exclusively consisting of veins, which had been discovered incidentally on autopsy [4]. He reported that almost all of them showed a complex drainage system with local stasis of blood in the veins, and called this pattern “a compensatory venous drainage system.” From angiographic observations, Saito and Kobayashi [28] proposed the hypothesis that the venous angioma was an anomaly or “compensatory venous drainage,” secondary to some abnormal venous drainage that might have derived from maldevelopment or occlusion of medullary veins and/or associated tributaries during embryogenesis.

14.5 Symptoms and Treatment Most MVMs are asymptomatic and discovered incidentally on autopsy or from imaging studies. Some may cause clinical symptoms, which may vary primarily according to the location. Supratentorial MVMs present most frequently with epileptic seizures (21–29%) or headache (17%), while focal neurological deficits are less common [8]. The most common symptoms of infratentorial MVMs are gait disturbance and ataxia [8, 12]. Most authors agree that hemorrhage from the MVM is rather unusual [4, 12] and therefore these lesions demonstrate or follow a more benign course than other vascular malformations. The incidence of hemorrhage in MVMs reportedly varies between 16 and 29% [8, 12, 32]. However, considerable controversy exists as to the risk of bleeding from an MVM [1]. The majority of hemorrhagic changes found close to venous malformations have been suggested to instead be attributable to other associated vascular malformations [16, 25]. Therefore, in many instances, an MVM alone probably has little clinical significance, and surgery has been rarely performed only when the lesion coexists with other vascular malformations and/or large hemorrhage [2].

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14.6 Imaging 14.6.1 Angiographic (DSA) Findings with Consideration of the Pathomechanism of MVMs MVMs are clearly depicted angiographically because of the characteristic features in the venous phase. The angiographic appearance of MVMs is described as medusa-like, mushroom-shaped or umbrella-shaped. According to Huang et al. [8], three segments may be distinguished angiographically in each MVM. Segment 1 consists of numerous, dilated medullary veins (resembling the hinged ribs of an umbrella, a caput medusae, or the cap of a mushroom). Segment 2 consists of the dilated central medullary vein (likened to the shank of an umbrella or stalk of a mushroom). Segment 3 consists of a superficial cortical or subependymal vein that finally drains into the dural sinus or Galenic system (Figs. 14.1 and 14.2). Essentially following the assumptions of Courville [4] and Saito and Kobayashi [28] as previously described, Huang et al. [8] postulated that MVMs are caused by compensatory mechanisms for venous occlusion occurring during intrauterine life, or may be caused after birth. From an angiographic perspective, they also divided this anomaly into two types: (1) a superficial drainage type (convexity type) (Fig. 14.1); and (2) a deep drainage type (deep central type) (Figs. 14.2 and 14.3) [8, 36]. The former type might be an end product of aplasia, hypoplasia or thrombosis of a connecting venous segment between the normal deep draining medullary veins and the deep venous system, e.g., a segmental defect or blockage present between the longitudinal caudate veins of Schlesinger [29] and the other subependymal veins, therefore resulting in compensatory dilatation of the superficial medullary veins and their tributaries. The deep drainage type might be derived from a similar defect or blockage at a connecting segment between the superficial draining medullary veins and superficial (cortical) cerebral venous system, or at the level of cortical veins themselves resulting in compensatory dilatation of the deep medullary veins and their tributaries. Indeed, abnormal vessels of MVMs appear to take an identical pattern with the normal angioarchitecture, although more dilated than normal, including medullary veins that can be observed on venous injection specimens of the cerebral hemispheres of normal adults (Figs. 14.1 and 14.2) (see Chap. 7) [9]. From an angiographic perspective, this fact seems to support the proposed pathomechanism mentioned by Huang et al. [8]. Furthermore, cerebral MVMs may be classified topographically into supra- and infratentorial MVMs. Of the supratentorial ones, most deep central MVMs are located in the basal ganglionic and thalamic regions, draining into the deep venous system and finally continuing to the vein of Galen (Fig. 14.4). Infratentorially, cerebellar MVMs of the superficial drainage type usually drain either into the petrosal sinus (anterior drainage) (Fig. 14.5), the confluence of sinuses or lateral sinus (posterior drainage), whereas cerebellar MVMs of deep drainage type drain into the vein of Galen via the precentral cerebellar vein (superior drainage). MVMs of the brainstem usually drain into the petrosal sinus (Fig. 14.6), while those of the deep drainage type drain into the vein of Galen (Fig. 14.7). A small number of MVMs do exhibit atypical angiographic features characterized by dilated medullary arteries and early visualization of medullary veins in the arterial phase.

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Fig. 14.1 Superficial drainage type (convexity type) converging in cerebral white matter. (a) Anterior-posterior (A-P) view of left carotid angiography (CAG), venous phase. (b) Schematic of venous structure of a malformation. (c) Coronal slice of a roentgenogram of an injected specimen from the venous system of normal adult brain. A case involving a 45-year-old woman incidentally discovered on CT following head injury. The components of a venous malformation (a, b) appear to take the pattern of the normally present venous architecture of cerebral white matter (c). In the right medial frontal subcortical region, numerous dilated fine deep medullary veins (1) run deeply like the hinged ribs of an umbrella frame, converging into a single dilated medullary vein (2) in the second or candelabra zone of convergence (large arrow). The direction of flow then reverses outward through the dilated central medullary vein that resembles the shank of an umbrella (transcerebral vein) to reach the surface (2). After reaching the cortex, the vein continues to a superficial cerebral vein (3), which in turn opens into the superior sagittal sinus (SSS). Several other veins, i.e., longitudinally running subependymal veins (longitudinal caudate veins of Schlesinger (LC) seen as many spots in cross-section) that receive numerous fine deep medullary veins (1¢) in the paraventricular area, do not join the subependymal veins but converge on the same single dilated central medullary vein described above (2). In this drainage type, an occlusive process might have occurred in a connecting segment between the deep medullary veins and the adjoining subependymal veins (arrowhead), with resultant dilatation of fine deep draining medullary veins (1, 1¢) that converge into an adjoining central medullary vein (2). One large venous convergence in the center of the white matter (large arrow) and one small convergence in the paraventricular area (small arrow) represent the typical shape of superficial drainage type (double umbrellas, double parachute shape). Note that the thalamostriate vein (TS), is seen on the left, whereas the vein on the right is absent or occluded (broken line) (a)

Both of these findings indicate the presence of increased flow through a lesion with arteriovenous shunts. However, careful observation in the late venous phase would always disclose classical angiographic features, such as the presence of dilated medullary veins and drainage through dilated central medullary or subependymal veins (Fig. 14.8a, b). These lesions have therefore been designated “MVM with an arterial component” by Huang et al. [8], “venous angioma with early filling vessels” by Moritake et al. [17], and “venous angioma with arterial blood supply” by Hirata et al. [6]. Regarding MVM with arteriovenous shunting, this thought to represent a prodrome to AVM by Mullan et al. [18, 19]. They postulate that an AVM may be a fistulized cerebral MVM and that both relate to failed development of the cortical venous mantle. These venous to arteriovenous lesions are suggested to be variants of a common developmental failure during the embryological stages.

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a

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Fig. 14.2 Deep drainage type (deep central type) with venous convergence in cerebral white matter. (a) A-P view of right CAG, venous phase. (b) Schematic of a venous structure of malformation. (c) Coronal slice of a roentgenogram of an injected specimen from the venous system of normal adult brain. A case involving a 55-year-old man presenting with left thalamic hemorrhage. The components of a venous malformation (a, b) also seem take the normally present venous architecture of cerebral white matter (c). Localized dilated fine medullary veins (1) run deeply, converging into a single dilated central medullary vein (2) in the white matter of the cerebral hemisphere. The vein drains into the subependymal vein (3) and opens to the internal cerebral vein. Normally, numerous medullary veins converge 3 times into a single central vein in the white matter (c) with the three converging zones (first to third arrows). Complete or incomplete venous occlusion or hypoplasia of a segment between the superficial drainage system and these three converging zones might have led to formation of a typically shaped MVM (triple wine-glass shape) (a, b). In this case, the longitudinal caudate veins drain into the medial group of subependymal vein, while the thalamostriate vein is not filled (a), possibly owing to a blockage between the longitudinal caudate veins and lateral group of subependymal veins (arrowhead) (a, c) or the subependymal vein itself. Usually, the subependymal vein receiving the dilated deep medullary vein in the MVM takes an unusual detouring course. First arrow: deep medullary veins (1) converge at “the first converging zone.” Second arrow: deep medullary veins (1¢) converge at “the second converging zone.” Third arrow: deep medullary veins (1″) converge at “the third converging zone”

MVM with an arterial component should not be confused with AVM with a medullary component. MVM with an arterial component is primarily a venous anomaly involving numerous dilated medullary veins, probably with shunting from medullary arteries, which is characteristically shown on the arterial phase of angiography. AVM with a medullary component primarily involves both medullary arteries and veins. Classical pyramid-shaped AVMs mostly affect the cortical gray and subjacent white matter, and the shunting involves both medullary arteries and veins (Fig. 14.8c, d).

14.6.2 CT Findings Nonenhanced CT typically shows normal results (67%) or an ill-defined slightly hyperdense area (16%). This hyperdensity is due to localized blood pooling within the venous spaces of MVMs [36]. Calcification in MVMs is seen in about 7% (Fig. 14.4a). The draining central medullary vein may occasionally be seen as a linear high-density structure in 3% [5].

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Fig. 14.3 Deep drainage type (deep central type) without definite convergence in cerebral white matter. (a) Coronal view of T2-weighted imaging. (b) Lateral view of venous phase in right CAG. A 44-year-old woman with headache was incidentally found to have an MVM on MRI. Dilated medullary veins in the right frontal and temporal region (1), run toward the longitudinal caudate vein of Schlesinger (LC) located in the superior lateral corner of the lateral ventricle, converge on some superior striate veins (2) in the basal ganglionic region, draining into the basal vein of Rosenthal (3: BVR) through the inferior striate vein (2¢), and emptying into the great vein of Galen. Diffusely in the frontal and temporal regions, the superficial drainage system (e.g., superficial medullary veins, subcortical veins, intracortical veins and superficial cerebral veins) is almost occluded or hypoplastic (asterisk)

On contrast-enhanced CT (CE-CT), an enhancing tuft of rounded or linear vessels is identified in the cerebral deep white matter. These dilated deep draining medullary veins converge into a single central medullary vein or more that in turn empty into an adjacent dural sinus or subependymal vein (Figs. 14.4b and 14.7a, b). In terms of parenchymal abnormalities associated with MVMs, edema and mass effects are usually absent on CT [31]. In recent years, the rapid development of CT scanner technology including MDCT has enabled clear delineation of vessels by three-dimensional CT angiography (3D-CTA). These advances have also made separate delineation of intracranial arterial and venous systems possible in a single session of contrast material injection (Fig. 14.7c, d). Furthermore, the appearance of four-dimensional CT digital subtraction angiography (4D-CTDSA) using 256 or 320 MDCT may help demonstrate the presence of arteriovenous shunt in MVM with an arterial component.

14.6.3 MR Imaging Since the advent of MR imaging, MVMs has increasingly been detected incidentally. The MR imaging appearance is similar to that observed with CT. However, the sensitivity of

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Fig. 14.4 Cerebral MVM in the basal ganglionic region. (a) Precontrast CT. (b) Contrast-enhanced CT (CE-CT). (c) T1-weighted imaging. (d) T2-weighted imaging. (e) Contrast-enhanced MR imaging (CE-MRI). (f) Susceptibility-weighted image. (g) Trans-axial maximum intensity projection of MR venography (contrast-enhanced time of flight MR angiography). (h) A-P view of venous phase of left CAG. (i) Lateral view of venous phase of left CAG. A case involving a 13-year-old girl presenting with blepharoptosis. On precontrast CT, spotty calcifications are seen in the left head of the caudate nucleus and globus pallidus (arrowheads) (a). Spotty enhancements are seen throughout the whole lentiform nucleus. The left septal vein is absent (broken line) (b). Dilated medullary veins and particularly the central medullary vein are seen as a flow-void on T1and T2-weighted imaging (arrow) (c, d), and linear and spotty enhancement on CE-MRI (e). Susceptibility-weighted imaging (f) and maximum intensity projection of CE-MRA (g) showing almost all features of the MVM. On digital subtraction angiography (DSA) (h, i), enhancement spots on CT correspond to dilated medullary veins (1), which converge into the anterior caudate tributaries of the thalamostriate vein (2), and drain into the thalamostriate vein (3). Left septal vein is absent (broken line) (i). MR imaging (c–g) performed 12 years after CT (a, b) and DSA (h, i). The features of MVM have not changed during this 12-year interval

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MRI in detecting MVM seems superior to CT, without contrast material. MVMs characteristically appear as low signal intensity lesions on both T1- and T2-weighted imaging (Figs. 14.3a, 14.4c, d and 14.6b, c). This low signal intensity is caused by the blood flowing within the medullary veins and draining central medullary vein. The dilated medullary veins and central medullary vein making up the MVMs are usually shown as small low signal spots when the shank of the umbrella for the MVM is perpendicular to the slice plane. Occasionally, larger dilated medullary veins can also be seen as linear low signals (Figs. 14.3a and 14.6b, c). On certain pulse sequences, these dilated medullary veins may appear as high signal intensity structures, probably due to flow-related enhancement (Fig. 14.5b). After contrast administration, the enlarged medullary veins and transcerebral central medullary or subependymal veins are typically seen (Fig. 14.4e) [21, 34]. Concerning brain parenchymal signal abnormalities associated with MVMs, the evidence of gliosis or hemorrhage is present in 10–15% [33]. Coexisting locoregional parenchymal abnormalities in the form of atrophy, signal abnormality, calcification (Fig. 14.4a), cavernous venous malformation (Fig. 14.6) or a combination of these findings have been reported in 64.5% [26].

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Fig. 14.5 MVM in the cerebellar hemisphere. (a) Lateral view of venous phase of left vertebral angiography (VAG). (b) T2-weighted imaging. A case involving a 23-year-old man with left hemiparasis since birth. Numerous dilated medullary veins (1) converge into a single dilated central medullary vein in the lateral corner of the fourth ventricle (2) and drain into the inferior petrosal sinus (3) (a, b). These converging dilated veins appear as a high signal intensity structure, probably due to flow-related enhancement (b)

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Fig. 14.6 MVM in the brain stem coexisting with hemorrhagic cavernous angioma. (a) Sagittal image from maximum intensity projection of CE-TOF MRA. (b) Mid-sagittal slice of T1-weighted imaging. (c) Mid-sagittal slice of T2-weighted imaging. A case involving a 58-year-old man presenting with diplopia. Dilated medullary veins (1) converge on a single dilated vein at the dorsal aspect of the lower pons and then the dilated trans-pontine vein goes forward (2: TPV) and finally drains into the inferior petrosal sinus (a). Cavernous angioma with hemorrhage coexists near the MVM in the dorsal lower pons (arrow) (b, c)

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Fig. 14.7 Deep central located MVM with partial arterial component. (a) CE-CT, transaxial view of cerebellar hemisphere. (b) CE-CT, trans-axial view of midbrain. (c) Arterial phase of 3D-CT angiography (3D-CTA). (d) Venous phase of 3D-CTA. A case involving a 69-year-old man presenting with gait disturbance. Dilated medullary veins in the right cerebellar hemisphere (a), midbrain and bilateral thalamic region (b) converge into clearly dilated central veins, continuing to the precentral cerebellar vein (PcCV) as the common trunk, and emptying into the great vein of Galen (VG) (d). Separate arterial and venous phases of 3D-CTA (c, d) suggest an MVM in the thalamic region with a partial arterial component (arrow). Slight ventricular dilatation is seen, probably due to compression to the aqueduct with a large deep draining vein of the malfomation (b). BA basilar artery; ICA internal carotid artery; PCA posterior cerebral artery; ICV internal cerebral vein; ISS inferior sagittal sinus; SS straight sinus

MVMs can be stereoscopically demonstrated on contrast-enhanced MR angiography due to slow flow lesions (Figs. 14.4g and 14.6a). High-resolution susceptibility imaging (HR SWI) reflecting the blood oxygen level dependent (BOLD) effect is also useful for screening venous lesions and analyzing the venous structure (Fig. 14.4f) [22, 23].

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Fig. 14.8 MVM with an arterial component (a, b) and AVM with a partial medullary component (c, d). (a, b) A case involving a 52-year-old man with a brain tumor. From the early arterial phase (a), numerous dilated fine (probably medullary) arteries in the left anterior parietal white matter (1) converge centrally. A dilated early DV (2) is already seen in the arterial phase. On capillary to early venous phase (b), numerous dilated medullary veins (1¢) probably shunting from medullary arteries (1) converge into a dilated central medullary vein (transcerebral vein) (2) and continue to the superficial cerebral vein (3). (c, d) A case involving a 16-year-old girl presenting with convulsions. This classical pyramid-shaped AVM is a combination of superficial and medullary types. On the early arterial phase of an A-P view of the right CAG (c), dilated middle cerebral arteries (MCAs) and lateral group of the lenticulostriate arteries (LSAs), including medullary arteries in the frontal operculum, are represented as feeding arteries. Distinguishing between medullary arteries and veins is impossible due to A-V shunts. On the late arterial phase (d), a large nidus (N) and DV appear, but have no characteristic features of converging medullary veins like an MVM

14.6.4 Radionuclide Study Single-photon emission computed tomography (SPECT) using N-isopropyl-p-(123I) iodoamphetamine reportedly shows decreased cerebral blood flow (CBF) [13, 30]. A positive correlation has been documented between the location of MVMs and decreased perfusion areas on SPECT imaging. Anomalous venous drainage through an MVM may explain a perfusion disturbance in the surrounding brain, which might have been derived from the previous occlusive process involving surrounding venous structures.

Abbreviations

BOLD CBF DSA DVA 4D-CTDSA HR SWI MDCT

Blood oxygen level dependent Cerebral blood flow Digital subtraction angiography Developmental venous anomaly Four-dimensional CT digital subtraction angiography High-resolution susceptibility imaging Multidetector row CT


MVM SPECT 3D-CTA

407

Medullary venous malformation Single-photon emission computed tomography Three-dimensional CT angiography

References 1. Abe T, Singer RJ, Marks MP, Norbash AM, Crowley RS, Steinberg GK. Coexistence of occult vascular malformations and developmental venous anomalies in the central nervous system: MR evaluation. AJNR Am J Neuroradiol. 1998;19:51–7. 2. Awad IA, Robinson JR, Mohanty S, Estes ML. Mixed vascular malformations of the brain: clinical and pathogenic considerations. Neurosurgery. 1993;33:179–88. 3. Constans JP, Dilenge D, Vedrenne CL. Angiomes veineux cerebraux. Neurochirurgie. 1968; 14:641–50. 4. Courville CB. Morphology of small vascular malformations of the brain. J Neuropathol Exp Neurol. 1963;22:274–84. 5. Fukusumi A, Ishii K, Okudera T. CT diagnosis of cerebral vascular malformation (in Japanese). Jpn J Diagn Imaging. 1985;5:539–53. 6. Hirata Y, Matsukado Y, Nagahiro S. Intracerebral venous angioma with arterial blood supply: a mixed angioma. Surg Neurol. 1986;25:227–32. 7. Huang YP, Okudera T, Fukusumi A, Maehara F, Stollman AL, Mosesson R, et al. Venous architecture of cerebral hemispheric white matter and comments on pathogenesis of medullary venous and other cerebral vascular malformations. Mt Sinai J Med. 1997;64:197–206. 8. Huang YP, Robbins A, Patel SC. Cerebral venous malformations. In: Kapp JP, Schmidek HH, editors. The cerebral venous system and its disorders. Orlando: Grune & Stratton; 1984. p. 373–474. 9. Huang YP, Wolf B. Veins of the white matter of the cerebral hemisphere (the medullary veins). Am J Roentogenol Radium Ther Nucl Med. 1964;92:739–55. 10. Krayenbühl HA, Yaşargil HG. Cerebral angiography. London: Butterworths; 1968. p. 207–23. 11. Lasjaunias P, Burrows P, Planet C. Developmental venous anomalies (DVA): the so-called venous angioma. Neurosurg Rev. 1986;9:233–44. 12. Martin NA, Wilson CB, Stein BM. Venous and cavernous malformations. In: Wilson CB, Stein BM, editors. Intracranial arteriovenous malformations. Baltimore: Williams & Wilkins; 1984. p. 234–45. 13. Matsuda H, Terada T, Katoh M, Ishida S, Onuma T, Nakano H, et al. Brain perfusion SPECT in a patient with a subtle venous angioma. Clin Nucl Med. 1994;19:785–8. 14. McCormick WF. Pathology of vascular malformations of the brain. In: Wilson CB, editor. Intracranial arteriovenous malformation. Baltimore: Williams & Wilkins; 1984. p. 44–63. 15. McCormick WF, Hardman JM, Boulter TR. Vascular malformations (“angiomas”) of the brain, with special reference to those occurring in the posterior fossa. J Neurosurg. 1968;28:241–51. 16. McCormick PW, Spetzler RF, Johnson PC, Drayer BP. Cerebellar hemorrhage associated with capillary teleangiectasia and venous angioma. Surg Neurol. 1993;34:792–9. 17. Moritake K, Handa H, Mori K. Venous angiomas of the brain. Surg Neurol. 1980;14:95–105. 18. Mullan S, Mojtahedi S, Johnson DL, Macdonald RL. Embryological basis of some aspects of cerebral vascular fistulas and malformations. J Neurosurg. 1996;85:1–8. 19. Mullan S, Mojtahedi S, Johnson DL, Macdonald RL. Cerebral venous malformation-arteriovenous malformation transition form. J Neurosurg. 1996;85:9–13. 20. Okazaki H. Malformative vascularlesions. In: Okazaki H, editor. Fundamentals of neuropathology. New York, Tokyo: Igaku-shoin; 1984. p. 62–72.

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21. Osterton B, Solymosi L. Magnetic resonance angiography of cerebral developmental anomalies: its role in differential diagnosis. Neuroradiology. 1993;35:97–104. 22. Reichenbach JR, Jonettz-Mentzel L, Fitzek C, Haacke EM, Kido DK, Lee BCP, et al. Highresolution blood oxygen-level dependent MR venography (HRBV): a new technique. Neuroradiology. 2001;43:364–9. 23. Reichenbach JR, Venkatesan R, Schillinger DJ, Kido DK, Haacke EM. Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology. 1997;204:272–7. 24. Rigamonti D, Drayer BP, Johnson PC, Hadley MN, Zabramski J, Spetzler RF. The MRI appearance of cavernous malformations (angiomas). J Neurosurg. 1987;67:518–24. 25. Rigamonti D, Spetzler RF. The association of venous and cavernous malformations: report of four cases and discussion of the pathophysiological, diagnostic and therapeutic implications. Acta Neurochir (Wien). 1988;92:100–5. 26. Ruiz DSM, Delavello J, Yilmaz H, Gailloud P, Piovan E, Bertramello A, et al. Parenchymal abnormalities associated with developmental venous anomalies. Neuroradiology. 2007;49:987–95. 27. Russell DS, Rubinstein LJ. Pathology of tumors of the nervous system. 4th ed. London: Edwar-Arnold; 1963. p. 116–45. 28. Saito Y, Kobayashi N. Cerebral venous angiomas. Radiology. 1981;139:87–94. 29. Schlesinger B. The venous drainage of the brain with special reference to the Galenic system. Brain. 1939;62:274–91. 30. Tomura N, Inugami A, Uemura K, Hadeishi H, Yasui N. Multiple medullary venous malformations decreasing cerebral blood flow: case report. Surg Neurol. 1991;35:131–5. 31. Truwit CL. Venous angioma of the brain: History, significance, and imaging findings. AJR. 1992;159:1299–307. 32. Valvanis A, Wellauer J, Yaşargil G. The radiological diagnosis of cerebral venous angioma: cerebral angiography and computed tomography. Neuroradiology. 1983;24:193–9. 33. Wilms G, Demaerel P, Marchal G, et al. Gadolinium-enhanced MR imaging of cerebral venous angiomas with emphasis on their drainage. J Comput Assist Tomogr. 1991;15:199–206. 34. Wilms G, Marchal G, Hecke PV, Van Fraeyenhoven L, Decrop E, Baert AL. Cerebral venous angiomas: MR imaging at 1.5 Tesla. Neuroradiology. 1990;32:81–5. 35. Wolf PA, Rosman NP, New PF. Multiple small cryptic venous angiomas of the brain mimicking cerebral metastases. Neurology. 1967;17:491–501. 36. Yaşargil MG. Venous, cavernous and occult angiomas. In: Yaşargil MG, editor. Microneurosurgery III B. Stuttgart: George Thieme; 1988. p. 405–38.

Thrombosis of the Cerebral Veins and Dural Sinuses

15

Akio Fukusumi

15.1 Introduction Cerebral sinovenous thrombosis (CSVT) is a distinct cerebrovascular disorder that, unlike arterial stroke, most often affects young adults and children. CSVT has traditionally been considered uncommon, but many authors have indicated that the disease may occur more frequently than was previously assumed, and simple, noninvasive and reliable diagnostic procedures have thus long been sought. CT findings for this disorder have been investigated by many authors, although that modality appears to have a low sensitivity because of inconstant or nonspecific changes, and cerebral angiography including digital subtraction angiography (DSA) has previously been considered the gold standard for diagnosis [21]. On the basis of the accumulation of numerous MR imaging (MRI) studies on this disorder, however, combined MRI and MR venography seems to offer a rapid and reliable procedure for correct diagnosis.

15.2 Symptoms and Pathogenesis Clinical features of CSVT are variable with nonspecific and unstable symptoms, particularly in the early stage and/or with nonsevere cases. Patients with CSVT typically present with signs of increased intracranial pressure, for example, headache, vertigo, nausea, vomiting, papilledema, and development of diminished levels of consciousness. However, focal neurogenic abnormalities may occasionally be seen, usually as the result of retrograde extension to or isolated involvement of the cerebral veins with infarction or secondary hemorrhage. In such cases, the most common findings are hemiplegia and seizure, while uncommon findings include dysphagia and posterior fossa findings (cranial nerve palsies and loss of cerebellar


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coordination). Psychological symptoms such as neurosis, hysteria, or depression may make the diagnosis difficult [10, 26, 28, 30]. Causes and risk factors associated with CSVT are shown in Table 15.1 [1, 7, 20]. In children, common systemic disorders such as hematologic diseases, infection, or trauma can

Table 15.1 Causes and risk factors associated with cerebral sinovenous thrombosis Infectious disorder Local disease

Intracranial infection (abscess, meningitis, subdural empyema) Local infection (otitis media, mastoiditis, sinusitis, tonsillitis)

Systemic disease

Bacterial infection (sepsis, endocarditis) Viral infection (encephalitis, cytomegalovirus) Parasitetuberculosis Mycoplasma infection

Noninfectious local diseases AVM Dural, AVF Neurosurgical operation Head injury Cerebral hemorrhage, Infarction Brain abscess, Tumor Porencephaly, Aarachnoid cyst Spinal tap, Intrathecal injection, Intracranial hypotension Cannulation of internal jugular vein Cranio-cevical arterial dissection, Radiation therapy Noninfectious systemic diseases Hormonal abnormality Malignancy Dehydration Operation Cardiac disorder Hematogenic disorders

Genetic prothrombotic conditions

Pregnancy/puerperal Oral contraceptives Carcinomatous meningitis Malignant lymphoma

Primary and secondary polycythemia Thrombocythemia Leukemia Anemia including paroxsymal nocturnal hemoglobinuria Antithrombin deficiency Protein C and protein S deficiency Factor V Leiden mutation, Prothrombin mutation

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15 Thrombosis of the Cerebral Veins and Dural Sinuses Table 15.1 (continued)

Acquired prothrombotic conditions Inflammatory bowel disease Collagen vascular diseases/Behçet disease Systemic venous thrombosis Metabolic disease Sturge-Weber syndrome Others

Homocysteinemia caused by gene mutation in methylenetetra-hydrofolate reductase Nephrotic syndrome Antiphospholipid antibody syndrome Homocysteinemia Ulcerative colitis, Crohn’s disease

Diabetes mellitus Neonatal asphyxia Venous injection MDMA (ecstasy) Hyperthyroidism

cause dehydration, which may in turn contribute to CSVT. However, no cause of CSVT is identified in 25% of all cases [16].

15.3 Imaging Radiologic features can be roughly divided into two types: (1) direct evidence of thrombosis and collateral venous drainage; and (2) evidence of complications involving dural sinus thrombosis, often associated with cerebral venous involvement.

15.3.1 Cranial CT The introduction of CT has enabled diagnosis or at least suspicion of this disorder in a noninvasive manner for the first time. CT can identify thrombosed veins, collateral venous channels, and secondary sequelae of the CSVT. Noncontrast CT may directly visualize thrombosed veins or dural sinuses as foci of increased density corresponding with the course of affected veins or dural sinuses (Fig. 15.1a). Occasionally, thrombosed cortical veins are seen as linear high-density areas (“cord sign”) (Fig. 15.2a). On postcontrast scans, the enlarged dural venous lacunae, meningeal venous channels, and collateral venous channels may be enhanced around the relatively hypodense thrombus within the sinus, displaying the so-called “empty delta sign” (Fig. 15.1b) [24]. In the case of veins oriented perpendicular to the axial plane (cortical veins, the great vein of Galen and superior sagittal sinus (SSS)), the focus is seen on successive axial slices, whereas in veins parallel to the scanning plane, such as the internal cerebral veins, medullary veins, straight sinus, and transverse sinus, the linear nature of foci may be apparent on a single slice (Fig. 15.1).

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Fig. 15.1 Classical “empty delta sign” on contrast-enhanced CT and MR imaging (MRI) in thrombosis of the left transverse sinus in a 33-year-old man. (a, b) Pre and postcontrast CT obtained on admission (day 7 after onset). (c–e) Cerebral angiography (on day 7). (c) anterior-posterior view of venous phase of the right carotid angiography (CAG). (d) Left CAG. (e) Left vertebral angiography (VAG). (f–k) MRI (on day 12). (f) T1-weighed imaging. (g) T2-weighted imaging. (h) FLAIR imaging. (i) Postcontrast T1-weighted imaging. (j) AP view of MR venography (3D contrastenhanced TOF MR angiography). (k) Lateral view of MR venography (partial MIP mainly of left hemisphere). The patient presented with severe headache, nausea and vomiting, followed by 7 days of left occipital headache. Precontrast CT (a) on day 7 shows high attenuation of the left transverse sinus, suggesting thrombosis (arrowheads). Postcontrast CT (b) reveals the thrombus as a defect in the lateral portion of the transverse sinus (“empty delta sign”) (arrow). Angiograms (c–e) show nonfilling from the left transverse to the sigmoid sinus. In this situation, distinguishing thrombosis of the left transverse sinus from congenital hypoplasia or aplasia of that sinus may be difficult. However, cordlike contrast collections that “hang in space” are persisting into the late venous phase (arrow), indicating a diagnosis of thrombosed cortical veins associated with thrombosis of left transverse sinus (e). On MRI on day 12, the thrombosed left transverse sinus is of mixed intensity on T1- and T2-weighted and FLAIR imaging (f–h). Postcontrast T1-weighted imaging (i) again shows the “empty delta sign” (arrow) surrounded by enhancing dural leaves, and reveals that thrombosis involves the entire transverse sinus to reach the beginning of the sigmoid sinus. On MR venography (3D contrast-enhanced TOF MRA) (j, k), the left transverse sinus is irregularly narrowed, indicating thrombosis that continues to the sigmoid sinus and mastoid emissary vein (small arrows). The left internal jugular vein may be congenitally hypoplastic (large arrow)

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Indirect evidence includes generalized or asymmetric brain swelling, white matter edema or venous infarction, parenchymal hemorrhage, subdural hematoma, gyral enhancement, and tentorial or falcine enhancement indicating venous stasis or dural hyperemia (Fig. 15.1b) [5]. Parenchymal hemorrhage may emerge as cortical and subcortical hemorrhage and/or hemorrhagic infarction occurring preferentially in the area adjacent to an occluded sinus. In patients with severe disturbance of consciousness, bilateral hemorrhage and/or infarction in the deep gray matter nuclei and upper brainstem often suggest deep venous thrombosis (Fig. 15.3) [23].

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Fig. 15.2 Cortical venous thrombosis with many collateral pathways in a 44-year-old woman who has taken oral contraceptives for 20 years. (a) Precontrast enhanced CT. (b) T1-weighted imaging. (c) FLAIR image. (d) Postcontrast T1-weighted imaging. (e) Coronal view of postcontrast T1-weighted imaging. (f) Axial view of postcontrast T1-weighted imaging. (g) MR venography (3D contrast enhanced TOF MR angiography). (h) Sagittal source image of MR venography. The patient experienced sudden motor weakness of the right upper limb and rigidity that persisted for only 30 min. On precontrast enhanced CT (a) at onset, thrombosed cortical veins are seen as a linear high-density area (“cord sign”) (arrow). Thrombus in the left central vein is shown as iso-intense on T1-weighted imaging (b), hyperintense on FLAIR imaging (c), and as a central linear filling defect of enhancement along with tram-track enhancement on postcontrast T1-weighted imaging (d). Multiplanar (coronal and axial) postcontrast T1-weighted imaging (e, f) shows a cord-like defect (double arrow) within the center of the left central vein with tram track-like enhancement, along with collateral venous pathways through deep draining medullary veins (DMVs) and transcerebral vein (TCV). MR venography (3D contrast-enhanced TOF MR angiography) (g) and the paramedian sagittal source image (h) show cortical venous collateral pathways on the medial surface of the hemisphere (CV) and deep medullary veins (DMV), respectively

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15.3.2 CT Venography The development of multidetector row helical CT (MDCT) has enabled three-dimensional (3D) vascular imaging. Large volumes of tissue may be scanned during peak arterial or venous enhancement with high spatial resolution and triplanar reconstruction clearly demonstrating cerebral veins and sinuses (Fig. 15.3d, e) [14, 17]. CT venography is not affected by flow-related artifacts and is considered superior to MR venography for the identification of cerebral veins and sinuses. This modality also has the advantage of being applicable to uncooperative patients, as acquisition time is much shorter than with MR venography, and this technique is clearly useful for patients in whom MRI is contraindicated. However, problems may exist with bone suppression and narrow optimal timing of image acquisition to minimize arterial and venous superimposition (Fig. 15.3e).

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Fig. 15.3 Thrombosis of the straight sinus in a 76-year-old woman. (a) T1-weighted imaging. (b) T2-weighted imaging. (c) Postcontrast T1-weighted imaging. (d) Postcontrast reconstruction CT. (e) 3D-CT angiography. The patient presented with a gradual decline in activities and level of consciousness and dementia for 3 months, until admission after falling into a coma. CT and MRI were performed on admission. Bilateral thalamic regions show hypointensity on T1-weighted imaging (a), inhomogeneous hyperintensity on T2-weighted imaging (b), and smudgy contrast enhancement on postcontrast T1-weighted imaging (c). Postcontrast midline sagittal reconstruction CT (d) and lateral-view 3D-CT angiography (e) show occlusion of the anterior portion of the straight sinus (arrows)

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15.3.3 MR Imaging The advantages of MRI in the diagnosis of CSVT are apparent almost from the outset. Combining T1- and T2-weighted imaging with MR venography is important (Figs. 15.1, 15.2, and 15.4). This combination will minimize confusion with aplasia or hypoplasia of sinuses and

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Fig. 15.4 Superior sagittal sinus (SSS) thrombosis with subcortical hemorrhage in a 42-year-old woman. (a) T1-weighted imaging on admission. (b) T2-weighted imaging. (c) FLAIR imaging. (d) Diffusion weighted imaging. (e) T2-weighted imaging. (f) FLAIR imaging. (g) Anterior-posterior view of MR venography (3D contrast-enhanced TOF MRA). (h) Lateral view of MR venography (partial MIP, mainly of left hemisphere). (i) T2-weighted imaging after 6 months. (j) A-P view of MR venography. The patient initially presented with convulsions and transient loss of consciousness (first attack). After a 1-month interval, she experienced involuntary movement of the right upper limbs (second attack). MRI obtained on admission (day 4 after second attack) (a–f). T1- (a) and T2-weighted imaging (b), FLAIR (c), and diffusion-weighted imaging (d) reveal subcortical hemorrhage (Hem) and subarachnoid hemorrhage (SAH). T2-weighted (e) and FLAIR (f) imaging through the upper convexity shows cortical infarction in the left fronto-parietal lobe (arrowheads). On all sequences, a high-intensity spot in the SSS indicates thrombus (arrows). In MR venography (3D contrast-enhanced TOF MR angiography) on day 4, A-P (g) and lateral (partial MIP, mainly of left hemisphere) (h) views show irregular defects in the SSS, which continue to the right transverse sinus through the confluence (arrows). The SSS appears diffusely enlarged with dilatation of venous lacunae (VL). Follow-up MRI after 6 months shows resolution of both hyperintense parenchymal lesions and high-intensity spots in the SSS in all sequences, with only a shrunken hemosiderin deposit (Hem) remaining on T2WI (i). MR venography at that time (j) shows re-canalization of SSS, although some remnant thrombi may be present in the posterior portion (arrows)

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flow-related artifacts with thrombus and avoid mistaking hypointense signal of deoxyhemoglobin and intracellular methemoglobin on T2-weighted images with flow void [19, 25]. In the early stages (days 1–5) of acute thrombosis, the flow void is absent and clot within the sinus is isointense on T1-weighted imaging and strongly hypointense on T2-weighted imaging. The signal reflects deoxyhemoglobin in intact red blood cells. On days 6–15 of the subacute stage, the thrombus becomes hyperintense on T1-weighted imaging, but remains hypointense on T2-weighted imaging. As methemoglobin is formed and released after the lysis of red blood cells, signals become hyperintense on both T1- and T2-weighted imaging (Fig. 15.4a, b). After 2–3 weeks, the thrombus progressively becomes isointense on T1-weighted imaging, and some recanalization may occur with reappearance of flow voids.

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15 Thrombosis of the Cerebral Veins and Dural Sinuses Table 15 2 MRI signal intensity of thrombus in dural sinus [3, 6, 12] Stage From onset T1WI

T2WI

Acute stage

Within 1 week

Iso-intensity

Low intensity

Subacute stage

Within 1 month

High intensity

High intensity

Chronic stage

After 1 month

Iso-intensity

High intensity

MR findings for thrombus in the dural sinus are summarized from some reports in Table 15.2 [3, 6, 12]. During this time, signs of development of a collateral circulation involving medullary, cortical, meningeal, emissary, and scalp veins may be seen (Fig. 15.4). Parenchymal abnormalities (i.e., edema, infarction, hemorrhage, and hemorrhagic infarct) are seen more readily as indirect evidence of CSVT on MRI than on CT, possibly with local causes of CSVT (i.e., neoplasm, trauma, meningitis, and extradural inflammatory lesions). A great advantage of MRI is the higher detectability for these processes compared to CT (Figs. 15.2–15.4). Staging of clinical severity has been proposed, according to MR findings, clinical symptoms, and dural sinus pressure (Table 15.3) [22]. In terms of the value of diffusion-weighted imaging (DWI) in CSVT, apparent diffusion coefficient (ADC) values may allow the identification of patients at risk of infarction who Table 15.3 Characteristics of various methods of MR angiography and indications for CSVT [28] Method Advantage Disadvantage Indication 2D-TOF

Shorter acquisition time Good spatial resolution Covers a large FOV Source images are available

In-plane saturation Low resolution Clot may mimic flow

Initial routine exam

2D-PC

Shorter acquisition time Reflects venous flow Corresponds to various flow patterns with VENC

Smaller FOV MIP is not available after exam

Initial routine exam. Follow-up exam

3D-PC

Higher resolution Reflects venous flow

Longest imaging time Needs to preset VENC

Need of high resolution for cortical vein

CE MRV

Shortest acquisition time Large FOV Highest resolution

Needs contrast material Difficulty of start timing of acquisition No reflection of venous flow

Need of high resolution for d-AVF etc. Simultaneously acquired with CE-MRI exam

d-AVF dural arteriovenous fistula; FOV field of view; PC phase contrast; CE-MRI contrastenhanced magnetic resonance imaging; MRV magnetic resonance venography; MIP: maximum intensity projection; TOF time of flight; VENC velocity encoding; CE MRV contrast-enhanced MR venography Three-dimensional contrast-enhanced TOF venography is performed in the sagittal plane using a fast field echo method with fat suppression. The scan is started 30 s after manual intravenous bolus injection of Gd-DTPA (10 mL). Scan parameters: TR, 4.5 ms; TE, 2.3 ms; flip angle, 60°; 128 × 256 matrix; 3-mm slice with 50% overlap reconstruction; FOV 22.0 × 22.0 cm

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may require endovascular treatment [15]. However, this has yet to be confirmed by other sources [4, 18]. In this disorder, venous obstruction results in elevated intracranial pressure, reduced perfusion pressure, and decreased cerebral blood flow. Vasogenic edema predominates first with elevated ADC values [4, 8, 18, 29]. However, areas of decreased ADC may be observed and may also be reversible, presumably reflecting severely decreased cerebral blood flow with neuronal swelling and membrane pump failure without neuronal death. Yoshikawa et al. [29] reported that decreased ADC values were presumed to reflect severe pathological conditions and indicate possible future development of infarction or hemorrhage. In addition, susceptibility effects in areas of hemorrhage or thrombus may complicate ADC calculations (Fig. 15.4).

15.3.4 MR Venography Two-dimensional (2D) time-of-flight (TOF) and 2D- and 3D-phase contrast (PC) sequences may be used without using contrast medium, although each method has both advantages and disadvantages, as shown in Table 15.4 [28]. When the diagnosis of CSVT cannot be confirmed with unenhanced MR venography, 3D contrast-enhanced TOF MRA (MR venography) should be performed and evaluated together with the source images (Figs. 15.1j, k, 15.2g, h and 15.4g, h). In the latter imaging, thrombi can be identified as irregular areas without enhancement or linear enhancing defect within the sinovenous lumen. Thrombi that appear hyperintense on basic T1-weighted source images of MR venography may be confused with a patent lumen that is enhanced. However, such thrombi are usually less intense than the contrastenhanced lumen of a patent sinus, and are thus distinguishable. In conclusion, combined MRI and MR venography would be noninvasive, and offers the most useful procedure for efficient and reliable diagnosis, as is the case also for follow-up studies after thrombolytic treatment (Fig. 15.4k, l) [25].

15.3.5 Cerebral Angiography (DSA) Until the advent of MRI and MRA, angiography was considered the gold standard for diagnosing CSVT, enabling direct visualization of the sinovenous lumen. Recently, Table 15.4 Stage of severity of dural sinus thrombosis [22] Stage Parenchymal change I

No parenchymal change

II

Brain swelling, sulcal effacement and mass effect, no signal change

III

Increased intensity of signal change as mild to moderate edema

IV

Severe edema, with or without hemorrhage

V

Massive edema and/or hemorrhage


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invasive cerebral angiography has ceased to be used for the diagnosis of CSVT alone, and is instead usually performed as a part of local thrombolysis [22]. A thrombosed sinus appears as an empty channel devoid of contrast medium and surrounded by dilated collateral venous channels in the dural leaves. Enlarged medullary veins and other collateral draining channels are often present. Thrombosed cortical veins are seen as cordlike contrast collections that seem to “hang in space,” persisting into the late venous phase (Fig. 15.1e). Intraluminal thrombi may produce linear or meniscoid filling defects. Deep cerebral vein thrombosis is seen as nonfilling of the internal cerebral veins, vein of Galen, or straight sinus with enlarged collateral channels. Overall, a good correlation exists between findings on MR venography and DSA as to the diagnosis of CSVT (Fig. 15.1) [26]. Unfortunately, however, evidence of complications resulting from CSVT, such as brain swelling, infarction, and hemorrhage, cannot be disclosed by the latter modality. A pitfall exists in the case of selective angiography: a dural sinus lumen that is mostly filled with contrast media may be partially cleared or unopacified due to inflow of nonopacified blood from contralateral or adjacent vascular territories where contrast media has not been injected. This should not be mistaken for a defect due to thrombus formation or clot (Fig. 15.1).

15.4 CSVT Associated with Dural Arteriovenous Shunt (AVS) CSVT is sometimes accompanied by dural AVS, particularly at the confluence with the transverse-sigmoid sinuses. Conversely, occlusion or stenosis of the dural sinus is seen in many cases of dural AVS. The relationship between the pathogenesis of dural AVS and major dural sinus thrombosis has been discussed [9], and it has been suggested that dural AVS may represent an acquired lesion caused by CSVT [2, 11]. Osborn [16] pointed out “high-flow vasculopathic changes secondary to AVS” as one of the common predisposing conditions for CSVT. If the CSVT is associated with dural AVS, venous congestion would be more exacerbated and, particularly in the case of venous reflux into cortical veins, clinical severity might be more critical as a result of the much higher venous pressure [13, 27]. In such cases, angiography may provide a more important means to clarify any hemodynamic abnormalities, and to determine therapeutic strategies such as direct operation, endovascular therapy, radiation, systemic intravenous fibrinolytic therapy, or a combination thereof.

Abbreviations ADC AVS CSVT DSA

Apparent diffusion coefficient Arteriovenous shunt Cerebral sinovenous thrombosis Digital subtraction angiography

422

DWI MDCT MRI PC TOF 3D-CTA 2D

A. Fukusumi

Diffusion-weighted imaging Multidetector row helical CT Magnetic resonance imaging Phase contrast Time-of-flight Three-dimensional CT angiography Two-dimensional

References 1. Canhao P, Ferro JM, Bousser LAG, MG SJ, Barinagarrementeria F. Causes and predictors of death in cerebral venous thrombosis. Stroke. 2005;36:1720–5. 2. Chaudhary MY, Sachdev VP, Cho SH, Weitzner Jr I, Puljic S, Huang YP. Dural arteriovenous malformation of the major venous sinuses: an acquired lesion. AJNR Am J Neuroradiol. 1982;3:13–9. 3. Dormont D, Anxionnat R, Evrard S, Louaille C, Chiras J, Marsault C. MRI in cerebral venous thrombosis. J Neuroradiol. 1994;21:81–99. 4. Ducreux D, Oppenheim C, Vandamme X, Dormont D, Samson Y, Rancurel G, et al. Diffusionweighted imaging patterns of brain damage associated with cerebral venous thrombosis. AJNR Am J Neuroradiol. 2001;22:261–8. 5. Einhaupl KM, Masuhr F. Cerebral venous and sinus thrombosis: an update. Eur J Neurol. 1994;1:109–26. 6. Ezura M. Venous thrombosis. In: Takahashi S, editor. Diagnostic imaging of cerebral vascular disease (in Japanese). Tokyo: Cyugaiigakusya; 2003. p. 289–96. 7. Ferro JM, Canhao P, Bousser MG, Stam J, Barinagarrementeria F. Cerebral vein and dural sinus thrombosis in elderly patients. Stroke. 2005;36:1927–32. 8. Forbes KP, Pipe JG, Heiserman JE. Evidence for cytotoxic edema in the pathogenesis of cerebral venous infarction. AJNR Am J Neuroradiol. 2001;22:450–5. 9. Handa J, Yoneda S, Handa H. Venous sinus occlusion with a dural arteriovenous malformation of the posterior fossa. Surg Neurol. 1975;4:433–7. 10. Heckman JG, Tomandl B. Cavernous sinus thrombosis. Lancet. 2003;362:1958. 11. Houser OW, Campbell JK, Campbell RJ, Sundt TM. Arteriovenous malformation affecting the transverse sinus: an acquired lesion. Mayo Clin Proc. 1979;54:651–61. 12. Isensee C, Reul J, Thron A. Magnetic resonance imaging of thrombosed dural sinuses. Stroke. 1994;25:29–34. 13. Ishii K, Goto K, Ihara K, Hieshima GB, Halbach VV, Bentson JR, et al. High-risk dural arteriovenous fistulae of the transverse and sigmoid sinuses. AJNR. 1987;8:1113–20. 14. Khandelwal N, Agarwal A, Kochhar R, Bapuraj JR, Singh P, Prabhakar S, et al. Comparison of CT venography with MR venography in cerebral sinovenous thrombosis. AJR. 2006;187:1637–43. 15. Manzione J, Newman GC, Shapiro A, Santo-Ocampo R. Diffusion- and perfusion weighted MR imaging of dural sinus thrombosis. AJNR Am J Neuroradiol. 2000;21:68–73. 16. Osborne AG, Davis WL, Lacobs J. Intracranial vascular malformations. In: Osborn AG, editor. Diagnostic neuroradiology. St Louis: Mosby; 1994. p. 385–95. 17. Ozsvath RR, Casey SO, Lustrin ES, Alberico RA, Hassankhani A, Patel M. Cerebral venography: comparison of CT and MR projection venography. AJR. 1997;169:1669–707. 18. Peeters E, Stadnik T, Bissay F, Schmedding E, Osteaux M. Diffusion weighted MR imaging of an acute venous stroke: case report. AJNR Am J Neuroradiol. 2001;22:1949–52.


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19. Renowden S. Cerebral venous sinus thrombosis. Eur Radiol. 2004;14:215–26. 20. Stam J. Current concepts. Thrombosis of the cerebral veins and sinuses. N Engl J Med. 2005;352:1791–8. 21. Takahashi S, Higano S, Kurihara N, Kayama T, Sakamoto K. Contrast-enhanced MR imaging of dural sinus thrombosis: demonstration of the thrombosis and collateral venous channels. Clin Radiol. 1994;49:639–44. 22. Tsai FY, Wang AM, Matovich VB, Lavin M, Berberian B, Simonson TM, et al. MR staging of acute dural sinus thrombosis; correlation with venous pressure measurements and implications for treatment and prognosis. AJNR Am J Neuroradiol. 1995;16:1021–9. 23. Ur-Rahman N, Al-Tahean AR. Computed tomographic evidence of an extensive thrombosis and infarction of the deep venous system. Stroke. 1993;24:744–6. 24. Virapongse C, Cazenave C, Quisling R, Sarwar M, Hunter S. The empty delta sign: frequency and significance in 76 cases of dural sinus thrombosis. Radiology. 1987;162:779–85. 25. Vogl TJ, Bergman C, Villinger A, Einhaupl K, Lissner J, Felix R. Dural sinus thrombosis: value of venous MR angiography for diagnosis and follow-up. AJNR Am J Neuroradiol. 1994;162:1191–8. 26. Wang AM. MRA of venous sinus thrombosis. Clin Neurosci. 1997;4:158–64. 27. Willinsky R, Terbrugge K, Montanera W, Mikulis D, Wallace MC. Venous congestion: an MR finding in dural arteriovenous malformations with cortical venous drainage. AJNR Am J Neuroradiol. 1994;15:1501–7. 28. Yoshida D. Venous sinus thrombosis. In: Imaging-head V, Tsuchiya K, editors. Vascular imaging-head and neck (in Japanese). Tokyo: Youdosya; 2008. p. 115–36. 29. Yoshikawa T, Abe O, Tsuchiya K, Okubo T, Tobe K, Masumoto T, et al. Diffusion-weighted magnetic resonance imaging of dural sinus thrombosis. Neuroradiology. 2002;44:481–8. 30. Zimmerman RD, Ernst RJ. Neuroimaging of cerebral venous thrombosis. Neuroimaging Clin N Am. 1992;2:463–85.

Part III Anatomy and Imaging of Spinal Vessels

Vessels of the Spine and Spinal Cord: Normal Anatomy

16

Shoki Takahashi

16.1 Introduction In planning treatment for patients with thoracoabdominal aortic disease, preoperative localization of the Adamkiewicz artery (AKA) may reduce the risk of postoperative ischemic spinal complications. Although intra-arterial catheter angiography has long been the primary method for visualizing spinal arteries, it is invasive and possibly carries angiographic risks and complications such as embolism. In recent years, noninvasive detection of the AKA using magnetic resonance (MR) angiography and computed tomographic (CT) angiography has emerged as a possible alternative to the catheter technique. In this chapter, we briefly review the anatomy of the arteries and veins in the spine and spinal cord using microangiograms reproduced from the study of Thron [10] and schemes published in the literature. Although most of the vessels are too minute to be visualized on imaging, knowledge of their existence and behaviors will help in interpreting imaging of various diseases of the spine and spinal cord as well as thoracoabdominal aortic disease. Microangiograms and diagrams in the transverse plane are placed so as to match the orientation of axial images at clinical imaging.

16.2 Arterial System 16.2.1 Design for the Development of Spinal Cord Arteries (Fig. 16.1) During fetal development, a pair of ventral longitudinal neural arteries on the anterior median surface of the cord join to form an anterior spinal artery (ASA) [5]. The artery is

S. Takahashi Department of Diagnostic Radiology, Tohoku University Graduate School of Medicine, Sendai, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_16, © Springer-Verlag London Limited 2010

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ACA MCA

PCA CrW ICA BA

VA ASA-vr

ASA

AsR DsR RMA Fenestration

RMA

ASA

Fig. 16.1 Design for arterial supply of the brain and spinal cord (reproduced from [8]). Both the basilar artery (BA) and anterior spinal artery (ASA) develop from the fusion of a pair of ventral longitudinal neural arteries on the ventral median surface of the brainstem and the spinal cord; therefore, the ASA may be regarded as a caudal continuation of the BA. Some portions of the fused arterial axis may fuse incompletely, especially at junctures of participating branches from the segmental arteries. The circle of Willis, where both carotid arteries join the arterial axis, may represent the most cranial site of such juncture. At the pontomedullary junction, a small circle is formed by both terminal parts of the vertebral arteries and their bilateral descending vascular roots (ASA-vr) that unite to form the ASA downward. At other levels, possible fenestration and even duplication over some distance can be seen along the ASA. All these may be regarded as examples of such portions of incomplete fusion [5]. In addition, discontinuities may be seen, especially between the upper cervical axis directly supplied by the vertebral artery (VA) and the lower vessel supplied by the segmental tributaries of the deep cervical, ascending cervical, and vertebral arteries [10]. ACA anterior cerebral artery; AsR ascending ramus of the radiculomedullary artery; CrW circle of Willis; DsR descending ramus of the radiculomedullary artery; ICA internal carotid artery; MCA middle cerebral artery; PCA posterior cerebral artery; RMA radiculomedullary artery

16 Vessels of the Spine and Spinal Cord: Normal Anatomy

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analogous to the basilar artery that develops from the fusion of a pair of ventral longitudinal neural arteries on the ventral median surface of the brainstem and can be regarded as a caudal continuation of the basilar artery. The ASA is primarily supplied from or consecutively reinforced from pairs of segmental arteries of the 31 somites at the embryonic stage. Differentiation of these segmental arteries varies at different levels. In the thoracic and upper lumbar regions, the segmental arteries persist as intercostal and lumbar arteries [10], and their anterior and posterior radicular arteries vascularize the spinal cord and nerves. In the cervical and sacral regions, however, the segmental arterial pattern is considerably modified. In the cervical region, three longitudinal (rostro-caudal) anastomotic channels develop outside the spinal canal−the ascending cervical artery in front of the transverse processes, the vertebral artery within the transverse processes, and the deep cervical artery behind the transverse processes, all of which give rise to branches to the spine and spinal cord. Lasjaunias and colleagues likened the arteries of the spinal cord to those of the brain [5], with the radiculomedullary arteries being equivalent to the vertebral and internal carotid arteries and the ASA corresponding to the basilar artery and the circle of Willis. The sulcal (central) arteries, which are central penetrating branches of the ASA at the ventral surface of the cord, represent basal perforators like the thalamoperforate arteries, whereas the coronal arteries that secondarily develop to form the pial network around the cord are cerebral cortical arteries, which develop later as the pallium (cerebral cortex) grows.

16.2.2 Spinal Arteries Individual segmental arteries give off dorsal branches, or dorsospinal arteries, that enter the intervertebral foramina and give off neural and spinal branches within the spinal canal. In the upper 3–5 cervical segments, the dorsospinal arteries derive from the vertebral artery; in the lower cervical region, they may arise from the ascending cervical artery of the thyrocervical trunk or from the deep cervical artery of the costocervical trunk [1] (Fig. 16.2). In the thoracic region, the arteries originate from the posterior intercostal arteries; in the lumbar region, from lumbar arteries and in the sacral region, usually from the lateral sacral arteries or, less commonly, from the middle sacral artery [1]. Other derivatives of segmental arteries include the first and second intercostal arteries that arise from the supreme intercostal artery (Fig. 16.2), and the subcostal artery. In the arterial supply to the C1 and C2 vertebrae at the craniovertebral junction, the ascending pharyngeal artery and occipital artery are also involved. Spinal branches arising from the dorsospinal arteries of the segmental arteries include the retrocorporeal artery that distributes to the posterior surface of the vertebral body and the prelaminar branches that supply the anterior aspect of the lamina (Fig. 16.3). These segmental artery branches within and outside the spinal canal on both sides are connected with each other by transverse and longitudinal anastomotic channels. Especially, retrocorporeal anastomoses on the dorsal aspect of the vertebral body connect descending branches of an upper vertebra and ascending branches of a lower vertebra. This network displays a characteristic rhomboid-shaped vascular ring on anteroposterior (AP) view of intercostal arteriograms (Fig. 16.4a). Intercostal arteriograms often opacify the next adjacent segmental arteries as well via this network, the center of which lies at the intervertebral level.

430 Fig. 16.2 Diagram illustrating the cervicothoracic spine including the supreme intercostal artery (reproduced from [3]). CCA common carotid artery; CCT costocervical trunk; DCA deep cervical artery; ICoA intercostal artery; IThA internal thoracic artery; SICoA supreme intercostal artery; SpBr spinal branch; ThCT thyrocervical trunk; VA vertebral artery

S. Takahashi

DCA CCT

SICoA

ThCT VA CCA

SpBr

CoA (T2)

ICoA (T1, T2) IThA

Ao AVBr

Fig. 16.3 Diagram showing the spinal arteries (reproduced from [8]). Ao aorta; ARA anterior radicular artery; AVBr anterior vertebral branch; DSpA dorsospinal artery (dorsal branch of the intercostal artery); ICoA intercostal artery; ICoA-v intercostal artery, ventral branch; PRA posterior radicular artery; PrLBr prelaminar branch; PVBr posterior vertebral branch; RCA retrocorporeal artery

RCA

DSpA

ICoA

ICoA-v

ARA PRA PrLBr

PVBr

431


a

b

Fig. 16.4 Intercostal and lumbar arteriograms. (a) Left T12 intercostal arteriogram shows retrocorporeal anastomotic channels with typical rhomboid configuration (arrows) (reproduced from [7]). (b) Right L1 lumbar arteriogram shows a well developed radiculomedullary artery, which acutely ascends and bifurcates to ascending (arrowhead) and descending (arrow) rami. The descending ramus is usually larger and displays a hair-pin curve with the trunk of the radiculomedullary artery (reproduced from [8])

16.2.3 Radicular Arteries 16.2.3.1 Classification Although the original 31 bilateral segmental arteries that supply the spinal axis regress during development, at almost every segmental level, radicular branches, called anterior and posterior radicular arteries, can be seen supplying the radix and dura [1, 6]. Coursing along the ventral aspect of individual spinal nerve roots, they pierce the dura and distribute to the anterior and posterior nerve roots as well as the dura. They run further to reach the ventral or dorsolateral surface of the cord at only some levels [10]. Radicular arteries are broadly divided into the radicular artery, radiculopial artery, and radico-medullary artery [5]. The radicular artery (proper) irrigates the nerve root but does not reach the spinal cord, is present at every vertebral level, and comprises anterior and

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posterior radicular arteries. The radiculopial artery courses along the nerve root to reach the surface of the cord, where it connects with the posterolateral spinal artery and pial arterial network, but it does not participate in the supply of the anterior spinal artery (ASA). The radiculomedullary artery reaches the spinal cord and provides a major arterial supply to the spinal cord as the ASA. Of note, Lasjaunias’s group believes [5] that all the classical radiculomedullary arteries that participate in the posterolateral spinal arteries should be considered radiculopial, that they join the dorsolateral pial network more frequently than the ventrolateral network, and that the radiculomedullary arteries are the only sources supplying the ASA. Further, they feel that the posterolateral spinal artery does not correspond to an embryonic vessel like the ASA, but rather, to a secondarily developed longitudinal vessel within the pial network. This resorting may have a clinical significance because embolization of the posterior spinal arteries (and their parent radiculopial artery) is classically considered safer than embolization of the ASA (and its parent radiculomedullary artery) in clinical practice.

16.2.3.2 Radiculopial/Radiculomedullary Arteries and the Adamkiewicz Artery (AKA) An average of 6 (range, 2–14) anterior radiculopial and radiculomedullary arteries contribute to the vascular supply of the spinal cord −2 to 3 for the cervical cord, 2–3 for the thoracic cord, and 0–1 for the lumbosacral cord [10]. An inverse correlation between the number and caliber of anterior radiculopial and radiculomedullary arteries has been noted [10]. The posterior radiculopial and radiculomedullary arteries are smaller in diameter but more numerous than those anterior, numbering 11–16. At the cervical level, the radiculomedullary artery from the lower cervical level (C5–C7) is usually the most predominant and is called the artery of cervical enlargement. The most predominant artery at the thoracic and lumbar level is called the Adamkiewicz artery (AKA), the artery of lumbar enlargement, or the arteria radicularis magna. The AKA most often arises at the lower thoracic or upper lumbar level (T9–T12 in 62%) and on the left side (73%) [10]. Infrequently, radiculopial and radiculomedullary arteries, which are usually thin, arise at the cervicothoracic junction or thoracic level. On angiography, radicular arteries display a steep cranially directed course along the spinal roots (Fig. 16.4b). An anterior radiculomedullary artery approaches the anterior median fissure of the cord and bifurcates into ascending and descending rami, both of which transition to the ASA (Figs. 16.5 and 16.6). Thus, the ASA represents a longitudinal anastomotic channel of ascending and descending rami of neighboring radiculomedullary arteries, as is also the case with the posterior longitudinal arteries [10]. The descending ramus is usually larger than the ascending, although the caliber of the ascending ramus can equal or even exceed that of the descending ramus in the mid- to lower cervical region [10]. Together, the ascending course of a radiculomedullary artery and its descending ramus have the characteristic appearance of a hair-pin curve, which is common for both anterior and posterior vessels. The steep cranially directed course of spinal nerves and radiculomedullary arteries is ascribed to the ascension of the cord relative to the spine during development [10]; the spinal skeleton enlarges much more than neural tissue. The spinal root and its accompanying radiculomedullary artery are fixed at the point of exit from the cord and at the transverse foramen through which they pass [5]. That is considered the reason a radiculomedullary artery shows such an acutely ascending course


433

Fig. 16.5 Diagram of spinal cord arteries (reproduced from [10]). AKA: Adamkiewicz artery; A-RMA anterior radiculomedullary artery; AsCA ascending cervical artery; ASA anterior spinal artery; BCA brachiocephalic artery; CCA common carotid artery; CrAn cruciate anastmosis of the conus medullaris; DCA deep cervical artery; ICoA intercostal artery; VA vertebral artery

on frontal view of spinal angiography; its course is steeper and makes a hair-pin curve at the lower spinal level but has a Y or T shape at the cervical and upper thoracic levels. At the upper and mid-thoracic levels, the radiculomedullary arteries may be too thin for angiographic delineation.

16.2.4 Superficial Arteries of the Spinal Cord The superficial arteries of the spinal cord comprise two systems, the first, the longitudinal trunks, including the ASA and posterolateral and posteromedial spinal arteries, and the second, the pial arterial network.

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a

b

Fig. 16.6 Stereoscopic microangiograms of the spinal cord. (a) anteroposterior (AP) view. (b) Lateral view (reproduced from [5]). Radiculopial and radiculomedullary arteries can be discerned. The Adamkiewicz artery is seen on the left, displaying a hair-pin curve. A relatively large artery caudally (arrow in a and b) that continues with the pial network on the dorsal aspect and not the anterior spinal artery is a radiculopial artery. The anterior spinal artery is a continuous arterial axis along the anterior median fissure with caudal tortuosity that makes an arcade at the tip of the conus, which is called the cruciate anastomosis of the conus medullaris (arrowhead in a and b). The anterior spinal artery gives off a small branch downward along the filum terminale; there is no contribution from the pial network. Lateral view shows sulcal (central) arteries (small yellow arrows in b) at the cervical and lumbar enlargements

435

16 Vessels of the Spine and Spinal Cord: Normal Anatomy Fig. 16.7 Left anterior and superior oblique view of the spinal cord arteries (reproduced from [8]). ARA anterior radicular artery; ASA anterior spinal artery; AsR ascending ramus of the radiculomedullary artery; DsR descending ramus of the radiculomedullary artery; PAN pial arterial network; PLSA posterolateral spinal artery; PRA posterior radicular artery; RA radicular artery; RMA radiculomedullary artery; RPA radiculopial artery; SuA sulcal (central) artery

PLSA ASA (AsR)

SuA

RMA ASA (DsR)

PRA (RPA) PAN

ARA

RA

16.2.4.1 Anterior Spinal Artery (ASA) Deriving from the fusion of a pair of longitudinal arteries, the ASA is a primary nourishing artery of the spinal cord that gives rise to sulcal (central) arteries that pass posteriorly through the anterior median fissure and to a number of delicate coronal arteries that course laterally around the outer surface of the cord and form the pial arterial network (Fig. 16.7) [1]. The ASA extends from the lower end of the basilar artery almost continuously downward along the anterior median aspect of the cord. However, as mentioned, the ASA successively takes the form of anastomotic channels between a descending ramus of a radiculomedullary artery and an ascending ramus of the lower neighboring radiculomedullary artery; therefore, the ASA may be irregular or discontinuous. It anastomoses with the posterior spinal arteries down around the conus, and this is called the cruciate anastomosis of the conus medullaris (synonyms: rami cruciantes, conus arcade, arterial basket anastomosis) (Fig. 16.8). Thron mentioned that the cruciate anastomosis is comparable to the arterial circle of Willis [10].

16.2.4.2 Posterior Spinal Arteries Over the posterior surface of the cord are a pair of posterolateral spinal arteries in and around the posterolateral sulci bilaterally and, less frequently, posteromedial spinal arteries

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Fig. 16.8 Microangiograms showing the cruciate anastmosis of the conus medullaris (reproduced from [10]). (a) anteroposterior (AP) view. (b) Lateral view. The anterior spinal artery is connected with the posterolateral spinal arteries via an anastomosis around the conus

that are more medial. Most rostral, the posterolateral spinal artery usually originates from the posterior inferior cerebellar artery or directly from the intracranial part of the vertebral artery, somewhat lower than the origins of the vascular roots that unite to form the ASA [1]. However, the posterior radiculopial arteries are the primary source of supply to the posterior spinal arteries [5]. Although the posterolateral spinal arteries form more constant longitudinal anastomotic channels than the posteromedial spinal artery does, they often show an


437

irregular pattern with discontinuous portions. Both display a rope-ladder-like appearance, and at some portions, the posteromedial spinal artery may replace the posterolateral arteries. Lasjaunias and associates regarded these posterior longitudinal anastomotic channels as part of the pial arterial network [5].

16.2.4.3 Pial Arterial Network (Vasocoronal Network) The pial arterial network, or vasocoronal network, is the name given to the system of anastomotic channels formed over the surface of the cord between the coronal arteries that arise from the ASA and the branches of the posterior spinal arteries (Fig. 16.7).

16.2.5 Intrinsic Arteries of the Spinal Cord Intrinsic arteries of the spinal cord are divided into a central system represented by the sulcal (or central) artery (synonym: sulco-commissural artery) and a peripheral system made up of numerous small arteries that originate in the pial arterial network that covers the spinal cord.

16.2.5.1 Sulcal (Central) Arteries Many sulcal (central) arteries arise from the ASA; the number varies substantially in different regions of the spinal cord. The densest sequences consist of 7–12 arteries per centimeter in the region of enlargements, with only 2–3 per centimeter in the thoracic region [10]. Individual sulcal arteries pass posteriorly through the anterior median fissure to reach the anterior commissural region of the cord, where each sulcal artery turns to the left or right and distributes unilaterally with a centrifugal pattern, mainly within the gray matter (Figs. 16.9–16.11) [10]. Successive sulcal arteries usually turn alternately to the left or right. Because the sulcal arteries are considered to derive from the branches of the embryonic paired longitudinal neural arteries, this lateralized nature stems from that of analogous branches that supplied either side of the neural axis during the embryonic stage, prior to fusion of the paired longitudinal neural arteries [5]; indeed, in the case of a duplicated (or unfused) anterior spinal axis, each trunk supplies its own side. On axial sections, the territory of this group of vessels occupies more of the area of cervical and lumbar enlargements, where there is more gray matter, than in the thoracic cord, where there is less gray matter. Normally, intraparenchymal anastomoses are absent between two neighboring sulcal (central) arteries, which indicates that the branches of this artery are end arteries. Transparenchymal anastomoses of this group of arteries with superficial arteries rarely occur in the thoracic region [10], although their physiological significance remains unclear.

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VA RMA ASA

SuA

RPA

VCoA

PLSA PAN

Fig. 16.9 Cross-section of the cervical cord showing its internal arterial supply (reproduced from [9]). ASA anterior spinal artery; PAN pial arterial network; PLSA posterolateral spinal artery; RMA radiculomedullary artery; RPA radiculopial artery; SuA sulcal (central) artery; VA vertebral artery; VCoA vasocoronal perforating arteries

16.2.5.2 Peripheral System (Vasocorona) Numerous perforating arteries arise from the pial arterial network, which receives blood supply from both radiculomedullary and radiculopial arteries (Figs. 16.9–16.11). The term vasocorona refers to both the pial arterial network and the numerous perforating arteries that branch from it (vasocoronal perforating arteries) [10].

16.2.5.3 Distribution of the Arteries of the Spinal Cord (Fig. 16.12) The sulcal (central) arteries centrifugally distribute primarily in the region of gray matter at the center of the cross-section of the cord. The supply area includes the anterior horn, intermediate substance, and basal portion of the posterior horn and the anterior funiculus adjacent to the anterior median fissure of the cord. The vasocoronal perforating arteries arising from the pial arterial network centripetally distribute mainly in the white matter located peripherally around the centrally located region of gray matter and in the edge of the anterior horn. Other vessels follow the posterior root of the spinal nerve to reach the gray matter of the apical portion of the posterior horn.

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Fig. 16.10 Microangiograms showing the ASA and sulcal (central) artery (reproduced from [10]). (a) Median sagittal microangiogram of lumbar enlargement shows transition from the Adamkiewicz artery to the anterior spinal artery (arrow). A high density of sulcal (central) arteries arise and course backward and upward. Apparently, the arterial supply of the vessels is much more dominant ventrally than dorsally. (b) Cross-section of the thoracic cord shows that a single sulcal (central) artery unilaterally supplies the cord. An anastomosis between the sulcal artery and the pial arterial network (arrowhead) is observed only in the thoracic region. (c) Cross-section of the lumbar cord (L2 level, 3-mm thick) shows several sulcal (central) arteries stacked within the anterior median fissure that distribute with a centrifugal pattern mainly within the gray matter, bilaterally. A tiny early-branched vessel (arrow) is seen to enter the anterior funiculus and anterior horn. The basal portion of the posterior horn is supplied by the sulcal arteries, and the apical portion is supplied by branches from the pial arterial network over the posterior surface (open arrow). There appears to be a thin anastomotic channel posteriorly (arrowhead). Note the dense capillary network within the gray matter

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Fig. 16.11 Consecutive microangiograms of frontal sections at the level of the lower cervical cord (C6-T1) (reproduced from [10]). (a) Anterior section shows a significant anterior radiculomedullary artery entering at the C7 level. Coronal arteries to the ventral surface of the cord and to the roots emerge from the radiculomedullary artery and anterior spinal artery. (b) Median section shows the sulcal (central) arteries and numerous vasocoronal perforating arteries. Individual sulcal arteries pass to one or the other hemiside of the cord, with the distributions of neighboring arteries alternating from side to side. (c) Posterior section shows the posterolateral (arrows) and posteromedial (arrowheads) spinal arteries form an irregular network with fragmentary chains


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Fig. 16.12 Arterial supply territories on the cross-section at different levels of the cord (modified from [10]). (a) Cervical enlargement, (b) thoracic cord, (c) lumbar enlargement. red: area of the sulcal (central) arteries; pink: area of the anterior spinal artery by way of the pial arterial network and vasocoronal perforating arteries; red + pink: entire area of the anterior spinal artery; light blue: posterior spinal arteries by way of the pial arterial network and vasocoronal perforating arteries shaded: In the anterior aspect of the cord, the shaded zone indicates boundary or double supply area between the sulcal (central) arteries and the vasocoronal perforating arteries deriving from the anterior spinal artery anteriorly; in the posterior aspect of the cord, the shaded zone indicates boundary or double supply area between the sulcal (central) arteries and the vasocoronal perforating arteries deriving from the posterior spinal arteries.

The territory of the sulcal (central) arteries corresponds rather closely to the proportion of gray matter, and both the cross-sectional areas of the cord and the proportion of gray matter differ considerably by vertebral level. Therefore, the areas of the sulcal (central) arteries and the vasocoronal perforating arteries also differ in size in different regions of the spinal cord: at the lumbar enlargement, the sulcal (central) arteries supply approximately 1/3 to 1/2 of the sectional area; their contribution decreases to 1/5 to 1/6 at the thoracic cord and lies between these extremes at the cervical cord. Because the ASA is involved in not only the sulcal (central) arteries but also the pial arterial network that irrigates about a half the surrounding white matter zone, the artery seems to take part in supplying the anterior 2/3 of the entire spinal cord. Important structures supplied by the ASA include the anterior horns, lateral spinothalamic tract, and part of the corticospinal tract.

16.3 Venous System 16.3.1 Spinal Cord Veins The veins that drain the spinal cord comprise two principal groups [1], the intraparenchymal veins and the intradurally located surface veins of the spinal cord. The intraparenchymal veins form from the intrinsic capillaries of the spinal cord, and surface veins within the dura receive the intraparenchymal veins and drain extradurally into veins in the neck, thorax, abdomen, pelvis, and vertebral column as well as into the communicating venous sinuses of the cranial cavity.

442 Fig. 16.13 Diagram showing spinal cord veins (reproduced from [8]). AMSV anterior median spinal vein; PLSV posterolateral spinal vein; PMSV posterior median spinal vein; PVN pial venous network; RdMV radial medullary veins; SuV sulcal (central) vein; TMVA transmedullary venous anastomosis

S. Takahashi AMSV

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16.3.1.1 Intraparenchymal Veins Venous drainage from the central part of the cord is made by the sulcal (central) vein, which, in turn, drains to the anterior median spinal vein (Fig. 16.13). From the peripheral zone of the cord, a number of radial medullary veins drain toward the superficial venous network in the pia mater. Such composition of the intrinsic venous system resembles the arterial distribution, but the venous paths have essentially different orientations; the radial medullary veins are of larger diameter and are longer than the vasocoronal perforating arteries and receive blood not only from the surrounding white matter but also significantly from the periphery of the gray matter. The sulcal (central) veins show no clear dominance over the radial medullary veins and are not as important in the venous drainage as the sulcal (central) artery in the arterial supply of the cord [10]. Additionally, in contrast to the unilaterally directed arteries, the sulcal veins receive blood from both halves of the cord and even anastomose above and below the venules that form adjacent sulcal veins [1].

16.3.1.2 Transmedullary Venous Anastomoses One of the most unique features in the venous system is the frequent presence of transmedullary venous anastomoses. Anastomoses measuring 0.1–0.2 mm thick and connecting the sulcal (central) and peripheral veins are quite common within the cord. In addition, much larger anastomoses (0.3–0.7 mm) run between the superficial longitudinal trunks through

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Fig. 16.14 Microangiograms of spinal cord veins (A anterior; P posterior) (reproduced from [10]). (a) Midline sagittal section of the lower thoracic cord shows sulcal (central) veins are equivalent in size with medullary veins in the posterior funiculus. Note a very large transmedullary anastomotic channel in an anterior–posterior direction (arrowheads). (b) Axial section through the C4 level shows that unlike spinal cord arteries, there is no ventral dominancy between the territories of the sulcal (central) veins and radial medullary veins from the pial venous network. A small transmedullary anastomostic channel extends backward in the midline from a sulcal (central) vein. (c, d) Consecutive axial sections through the T9 level show a prominent transmedullary anastomosis in an anterior–posterior direction in the midline (arrow)

the spinal cord, mostly in anteroposterior direction, and receive the few, if any, veins that drain directly from the spinal cord (Fig. 16.14) [10]. The larger anastomoses are most frequent in the cervicothoracic and upper thoracic regions, where motility of the spinal column is most prominent. Because the larger transmedullary venous anastomoses scarcely

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receive tributaries from the parenchyma and the anastomoses are most dense in the region where motility of the spinal column is most prominent, they could have a certain physiological significance in regulating venous pressure within the cord during movement of the spinal axis. That is, when the ventral veins are compressed owing to movement of the spinal axis, blood quickly and efficiently moves backward via these anastomoses, thereby equalizing venous pressure [10].

16.3.1.3 Superficial Veins Although the great variability of the superficial venous vessels makes their reliable systematization difficult, there seem to be two longitudinally directed vessels, the anterior and posterior median spinal veins, and an irregularly circumferential venous plexus on the cord surface, which is called the coronal venous plexus (venous plexus of the pia mater, venous pial plexus) [1, 10]. The anterior median spinal vein is located along the anterior median fissure and corresponds to the ASA; it receives the sulcal veins and small pial vessels from the anterior and lateral aspects of the cord surface that help to form the coronal venous plexus (Fig. 16.13) [1, 10]. The vein is of largest caliber lumbo-sacrally and proceeds sometimes as a very large terminal vein in 60–70% of all cases, running together with the filum terminale [10]. The posterior median spinal vein, which courses independently of the arteries, is especially large above the thoracolumbar enlargement. The posterior median spinal vein may wander to the left, and then to the right at the dorsal circumference. Thron indicates that its diameter can be especially large in the thoracic region and that the vessel frequently shows varicose or extremely tortuous convolutions [10], which may confuse interpretation of its imaging features with those of disorders with arteriovenous shunt. Posterior spinal veins are variable, having segments with a well developed posterolateral spinal vein and other segments with plexiform pattern. The anterior and posterior longitudinal spinal veins merge radicular or radiculomedullary veins at different levels, course toward the intervertebral foramina with ventral and dorsal roots in a manner resembling that of the radiculomedullary arteries, and join the internal vertebral venous plexus or the intervertebral vein, which exits the vertebral canal through the transverse foramen. The anterior and posterior radiculomedullary veins are largest and most constant at the cervical and lumber enlargements [1, 10].

16.3.2 Vertebral Venous Plexus (Batson’s Venous Plexus) The vertebral venous plexuses include the internal and external vertebral venous plexuses (of Batson); the plexus vessels are extradural but communicate with the veins that drain the


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Fig. 16.15 Axial section through the body of a thoracic vertebra, showing the vertebral venous plexus (modified from [2]). AEVP anterior external vertebral venous plexus; AIVP anterior internal vertebral venous plexus; ARV anterior radicular vein; AzV azygos vein; BVV basivertebral vein; HAzV hemiazygos vein; ICoV intercostal vein; IVV intervertebral vein; PEVP posterior external vertebral venous plexus; PIVP posterior internal vertebral venous plexus; PRV posterior radicular vein; RCV retrocorporeal vein

neural tissue of the spinal cord and with the systemic veins of the thorax, abdomen, and pelvis, as well as the dural sinuses of the skull [1]. The internal vertebral venous plexuses lie within the entire length of the vertebral canal between the dura mater and the vertebrae (Fig. 16.15) and course mainly in a vertical direction to form longitudinal veins that are connected by transverse branches. The anterior internal plexuses are generally more developed than those posterior and lie along the posterior aspect of the vertebral body, whereas the posterior internal plexuses lie anterior

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to the vertebral arches and yellow ligaments. The anterior and posterior internal plexuses communicate freely with each other within the vertebral canal as well as with the external vertebral plexuses [2]. At the craniovertebral junction, the internal plexuses are connected above with intracranial dural sinuses, including the occipital and sigmoid sinuses and emissary veins [2]. The basivertebral veins are thin-walled vessels in the cancellous tissue of the vertebral bodies that converge posteriorly to emerge from the foramina on the dorsal surface of the vertebrae to join the transverse branches of the anterior internal vertebral plexuses, the opening of which may be valved [2]. The basivertebral veins also drain into the anterior external vertebral plexuses through small openings. The anterior internal plexuses laterally transition to retrocorporeal veins, which join the posterior internal plexuses to form intervertebral veins. Outside the spinal canal, the external vertebral venous plexuses consist of anterior and posterior plexuses that freely anastomose with each other (Fig. 16.15) [2]. The external vertebral venous plexuses are best developed in the cervical region, where they anastomose with the vertebral, occipital, and deep cervical veins. The intervertebral veins accompany the spinal nerves through the intervertebral foramina and receive blood from the veins of the spinal cord (anterior and posterior radiculomedullary veins), drain the internal and external vertebral plexuses, and flow into segmental veins or their derivatives, including the vertebral, posterior intercostal, lumbar, and lateral sacral veins; the orifices of the intervertebral veins have valves [2] (Fig. 16.16). Ascending lumbar venography shows characteristic retrocorporeal diamond-shaped channels (Fig. 16.17) that represent the composite appearance of the anterior internal vertebral plexuses of the successive vertebral systems combined via anastomoses.

16.3.3 Vein Valves and a System for Preventing Reflux Both internal and external vertebral plexuses are devoid of valves, which has great clinical relevance, and they anastomose freely with each other and join the intervertebral veins [4]. Whether the basivertebral or intervertebral veins contain effective valves is uncertain, but their reversed blood flow is experimentally indicated to occur [4]. This may explain how intrapelvic malignancy may metastasize to vertebral bodies earlier than to the lungs, the malignant cells spreading into the internal vertebral plexuses when blood flow is reversed by temporarily elevated intra-abdominal pressure, such as from coughing or defecation [4]. Drainage routes of the superficial spinal veins run toward the internal vertebral plexuses, whereas reflux does not occur from Batson’s plexuses into the spinal cord veins [10]. The mechanism of reflux obstruction may consist of an oblique, zigzag course of the vessels combined with marked narrowing of the lumen at the level of the dura, which presumably functions as a valve mechanism [10].

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Fig. 16.16 Venous drainage of the spine (modified from [5]). (a) Anterior view. (b) Lateral view. The inferior vena cava has been retracted ventrally to allow satisfactory visualization of the renal vein. Lower lumbar veins join the common iliac vein downward via the ascending lumbar vein on both sides. On the left, the left ascending lumbar vein opens into the left renal vein as well (LmV*). Segmental veins above the L2 level do not open directly into the inferior vena cava. Instead, the right upper segmental veins flow upward and join the azygos vein; of the left segmental veins above the L2, those below T8 join the hemiazygos vein and those from T3 to T8 join the accessory hemiazygos vein. AHAzV accessory hemiazygos vein; ALV ascending lumbar vein; AzV azygos vein; BCV brachiocephalic vein; HAzV hemiazygos vein; ICoV intercostal vein; IVC inferior vena cava; IVV intervertebral vein; JV jugular vein; LmV lumbar vein; L-RV left renal vein; SV sacral vein; SVC superior vena cava; VV vertebral vein

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Fig. 16.17 Spinal venogram (reproduced from [7]). AIVP anterior internal vertebral venous plexus; ALV ascending lumbar vein; IVC inferior vena cava; IVV intervertebral vein; LSV lateral sacral vein; RCV retrocorporeal vein; IIV internal iliac vein

AIVP RCV IVC IVV

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Abbreviations ACA AEVP AHAzV AIVP AKA ALV AMSV Ao AP ARA A-RMA ARV ASA AsCA AsR AVBr

Anterior cerebral artery Anterior external vertebral venous plexus Accessory hemiazygos vein Anterior internal vertebral venous plexus Adamkiewicz artery Ascending lumbar vein Anterior median spinal vein Aorta Anteroposterior Anterior radicular artery Anterior radiculomedullary artery Anterior radicular vein Anterior spinal artery Ascending cervical artery Ascending ramus of the radiculomedullary artery Anterior vertebral branch


AzV BA BCA BCV BVV CCA CCT CrAn CrW CT DCA DSpA DsR HAzV ICA ICoA ICoA-v ICoV IIV IThA IVA IVC IVV JV LmV L-RV LSV MCA MR PAN PCA PEVP PIVP PLSA PLSV PMSV PRA PrLBr PRV PVBr PVN RA RCBr RCV RdMV

Azygos vein Basilar artery Brachiocephalic artery Brachiocephalic vein Basivertebral vein Common carotid artery Costocervical trunk Cruciate anastmosis of the conus medullaris Circle of Willis Computed tomography Deep cervical artery Dorsospinal artery (dorsal branch of the intercostal artery) Descending ramus of the radiculomedullary artery Hemiazygos vein Internal carotid artery Intercostal artery Intercostal artery, ventral branch Intercostal vein Internal iliac vein Internal thoracic artery Intervertebral spinal artery Inferior vena cava Intervertebral vein Jugular vein Lumbar vein Left renal vein Lateral sacral vein Middle cerebral artery Magnetic resonance Pial arterial network Posterior cerebral artery Posterior external vertebral venous plexus Posterior internal vertebral venous plexus Posterolateral spinal artery Posterolateral spinal vein Posterior median spinal vein Posterior radicular artery Prelaminar branch Posterior radicular vein Posterior vertebral branch Pial venous network Radicular artery Retrocorporeal branch Retrocorporeal vein Radial medullary veins

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Radiculomedullary artery Radiculopial artery Supreme intercostal artery Superior intercostal vein Spinal branch Sulcal (central) artery Sulcal (central) vein Sacral vein Superior vena cava Thyrocervical trunk Transmedullary venous anastomosis Vertebral artery Vasocoronal perforating arteries Vertebral vein

References 1. Clemente C. Developmental and gross anatomy of the central nervous system. In: Gray’s anatomy. 30th American ed. Philadelphia: Lea & Febiger; 1985. pp. 933–1148. 2. Clemente C. The veins. In: Gray’s anatomy. 30th American ed. Philadelphia: Lea & Febiger; 1985. pp. 788–865 (830). 3. Feneis H. Anatomisches Bildworterbuch der internationalen Nomenklatur. 2nd ed. Stuttgart: Georg Thieme; 1982 (Japanese version). 4. Gabella G. Veins of the thorax. In: Williams P, editor. Gray’s anatomy 30th American ed. New York: Churchill Livingstone; 1995. pp. 1591–5. 5. Lasjaunias P, Berestein A. Spinal and spinal cord arteries and veins. Surgical neuro-angiography 3: Functional vascular anatomy of brain, spinal cord and spine. Berlin: Springer; 1990. 6. Manelfe C, Lazorthes G, Roulleau J. [Arteries of the human spinal dura mater]. Acta Radiol Diagn (Stockh). 1972;13:829–41 (cited in [Thron, 1988 #1927]) 7. Miyasaka K. Vessels of the spine and spinal cord (in Japanese). In: Miyasaka K, editor. Manual of cerebral and spinal angiography. Tokyo: Nankodo; 1997. p. 147–66. 8. Takahashi S. MR imaging anatomy of the brain (in Japanese). Tokyo: Shujunsha; 2005. 9. Takahashi S, Yamada T, Ishii K, Saito H, Tanji H, Kobayashi T, et al. MRI of anterior spinal artery syndrome of the cervical spinal cord. Neuroradiology. 1992;35:25–9. 10. Thron A. Vascular anatomy of the spinal cord. Neuroradiological investigations and clinical syndromes. Wien New York: Springer; 1988.

MDCT of the Artery of Adamkiewicz

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Kei Takase and Shoki Takahashi

17.1 Introduction Accurate localization of the artery of Adamkiewicz (AKA) is important in planning surgical or interventional radiological treatment of patients with thoracoabdominal aortic diseases, and preoperative information that localizes this artery may reduce postoperative ischemic spinal complications [3–5, 7–10, 15, 17, 18, 25]. Although the usefulness of conventional angiography is reported [3, 8, 17, 25], various complications of spinal angiography have been described [17, 25]. Noninvasive detection of the AKA using magnetic resonance (MR) imaging and its surgical usefulness have also been reported [2, 4, 5, 7, 9, 10, 13, 15, 26–28], but because the scanning field of view is limited, MR imaging cannot simultaneously demonstrate the entire aorta and intercostal and lumbar arteries with information on the AKA. Effective use of multidetector-row helical computed tomography (MDCT) with a four-slice detector and 2-mm collimation to demonstrate the AKA has been initially reported [20]; however, that study did not focus on patients requiring an aortic vascular graft or stent-graft in the T8–T12 region, where the AKA likely originates and postoperative ischemic spinal complications are likely to occur. Recently, the availability of MDCT with more than 16 detector rows has permitted imaging of the entire aorta and iliac arteries with less than 1-mm collimation. With an adequate scanning protocol, current MDCT allows simultaneous evaluation of the AKA with information of the entire aorta [19], which makes preoperative visualization of the AKA pervasive. Furthermore, new protocols have recently been devised to improve AKA detection [12, 14, 21, 22]. This chapter will review scanning techniques to demonstrate the AKA and the clinical utility of its visualization.

K. Takase (*) Department of Diagnostic Radiology, Tohoku University Graduate School of Medicine, Seiryo-machi, Aoba-ku, Sendai, 980-8574, Japan

S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_17, © Springer-Verlag London Limited 2010

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17.2 Computed Tomographic Imaging of the Artery of Adamkiewicz 17.2.1 Imaging Technique Visualization of the AKA is necessary in patients with aortic disease that includes descending and/or thoracoabdominal disease. Basically, in a single evaluation, we assess information about the AKA, entire aorta, and iliac arteries to obtain most imaging information necessary for aortic surgery. A technique for visualizing the AKA by MDCT imaging has been reported, and the use of MDCT with more than 16 detector rows is thought adequate for the purpose because it allows scanning of the entire aorta with submillimeter collimation during breath hold; this capability is also widely available in major hospitals.

17.2.2 Computed Tomography Protocol We mainly perform scanning on an MDCT system with 16 and 64 detector rows and use the following parameters: 0.5 s/rotation or 0.5-mm collimation, 120 kV tube voltage, and 350 mA current. The patient’s spine is positioned near the isocenter of the CT gantry. Other CT devices require minimal collimation thickness of 0.625 or 0.75 mm. The speed of table movement is set to allow completion of scanning in around 30 (16 detector) or 20 s (64 detector). The patient is instructed to hold his/her breath for approximately 20 s during scanning. When breath-holding is thought to be difficult, the patient is given oxygen to help. If a patient cannot hold his/her breath for the duration of the scan, he/she is instructed to breathe shallowly after breath-holding for a specified time. Before scanning, 120–150 mL of contrast material with iodine concentration of more than 350 mg I/mL is injected via an antecubital vein at a rate of 4.0–5.0 mL/s and followed by 30 mL of saline at the same rate. Total volume of the contrast material should be adjusted according to the patient’s body weight. When a suitable antecubital vein cannot be found, the right external jugular vein should be used for contrast injection. Utsunomiya and colleagues reported that aortic attenuation value of more than 450 Hounsfield units (HU) is adequate for best visualization of the AKA, and injection speed of 1.75 g iodine/s is necessary to achieve adequate contrast enhancement [22]. Scan delay is set by means of an automatic triggering system that is normally part of the current CT scanner equipment [19, 20]. Continuous low dose CT fluoroscopy at the level of the ascending aorta is initiated 10 s after the start of contrast injection. The CT value in a circular region of interest placed in the descending aorta is measured; when the CT value reaches the threshold (absolute CT value of 150 HU), breath-holding is automatically indicated, followed by the start of helical scanning. Axial slices are reconstructed with a 0.5-mm slice thickness (the same thickness as original collimation) at 0.5-mm intervals. To

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evaluate the AKA, setting the reconstruction field of view to the area around the aorta and spine improves in-plane resolution. To evaluate the entire aorta and iliac arteries, another dataset is generated that does not limit the reconstruction field of view (Fig. 17.1).

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Fig. 17.1 Computed tomographic (CT) images of a patient with thoracoabdominal and abdominal aortic aneurysms. (a–i) Images of the artery of Adamkiewicz. (a–f) Consecutive transverse images show the continuity of the anterior spinal artery (arrowheads) and artery of Adamkiewicz (arrows) with the posterior branch of the intercostal artery (large arrow). (g) Oblique coronal multiplanar reconstruction (MPR) image along the artery of Adamkiewicz (arrows) also demonstrates continuity from the anterior spinal artery (arrowheads) through the posterior branch of the intercostal artery (large arrow). (h) Curved planar reformation image of the area along the left eighth intercostal artery delineates the continuity from the aorta, the intercostal artery, its posterior branch, and the artery of Adamkiewicz to the anterior spinal artery. Note the characteristic hairpin-curve appearance of the union of the artery of Adamkiewicz and the anterior spinal artery. (i) Volume-rendering images of the artery of Adamkiewicz and the left eighth intercostal artery (red) superimposed with the aorta (light brown) and transparent bony structures clearly demonstrate the relationship between the aorta and the origin of the parent segmental artery of the Adamkiewicz artery. (j) Volume-rendering images of the entire aorta show information about the aorta and iliac arteries, including the thoracoabdominal aortic aneurysm. (k–n) Images of the anterior radiculomedullary vein. (k–m) Transverse images show the anterior spinal vein (arrowheads) and the anterior radiculomedullary vein. (n) Curved planar reformation image of the area along the intercostal vein shows the continuity of the anterior spinal vein (arrowheads) and the radiculomedullary vein (arrows) to the twelfth intercostal vein (large arrow), which drains into the azygos system. Origin of the artery of Adamkiewicz from the left eighth intercostal artery is also visualized

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17.2.3 Image Processing We usually use a stand-alone workstation (Zio M900 Quadra, Amin, Tokyo, Japan) to process images. To provide vascular surgeons with preoperative information, we routinely generate volume-rendering images of the aorta and iliac arteries that include visualization of its main cervical and abdominal branches. Multiplanar reconstruction (MPR) images that include oblique coronal images with craniocaudal angulations are observed to detect the AKA and show its typical hairpin-curve; curved planar reformation (CPR) images are generated so that the anterior spinal artery and the AKA and its parent artery can be traced over as long a distance as possible (Figs. 17.1–17.6); and volume-rendering images of the AKA and its parent segmental artery superimposed with the aorta and transparent bony structures are also reconstructed to clarify the location of the AKA and origin of the parent artery (Figs. 17.1–17.4).

17.2.4 Identification of the Artery of Adamkiewicz by MDCT 17.2.4.1 Detection of the Artery of Adamkiewicz Because the anterior spinal vein runs very close to the anterior spinal artery near the middle ventral surface of the spinal cord, the anterior radiculomedullary vein and AKA can be

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Fig. 17.2 Computed tomographic (CT) images of a patient with descending aortic aneurysm. (a) Oblique coronal image and (b) curved planar reformation images of the artery of Adamkiewicz . Although the continuity between the posterior branch of the left seventh intercostal artery and the artery of Adamkiewicz was partially obscured at the intervertebral foramen because of proximity to the bone, most of the continuity from the aorta, intercostal artery through the artery of Adamkiewicz , and anterior spinal artery can be traced. No distinct venous structures are enhanced in the spinal canal, intercostal veins, or azygos veins

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Fig. 17.3 Computed tomographic (CT) images of a patient with thoracoabdominal aortic aneurysm. (a) Curved planar reformation image shows the artery of Adamkiewicz originating from the left ninth intercostal artery. (b, c) Volume-rendering images of the (b) right posterior oblique and (c) left anterior oblique view demonstrate the relationship between the artery of Adamkiewicz and the aortic aneurysm. Because the origin of the left ninth intercostal artery that gives off the Adamkiewicz was seen above the level of the thoracoabdominal aneurysm, aortic replacement surgery could be performed without reconstruction of the intercostal arteries, which preserved the left intercostal artery and reducing the total time of the surgery. No postoperative ischemic spinal complications occurred

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Fig. 17.4 Computed tomographic (CT) images of a patient with chronic aortic dissection. (a) Curved planar reformation image demonstrates full continuity of the vascular supply from the aorta through the anterior spinal artery. The artery of Adamkiewicz arises from the seventh intercostal artery. (b) Right anterior oblique volume-rendering image shows 3-dimensional relationship of the artery of Adamkiewicz to the aorta

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Fig. 17.5 Curved planar reformation images generated from computed tomography (CT) of a patient with type B aortic dissection (a) before and (b) after aortic replacement surgery. The artery of Adamkiewicz is supplied by the right ninth intercostal artery originating from the true lumen of the aorta. The patency of the ninth intercostal artery, the artery of Adamkiewicz through the anterior spinal artery, is demonstrated after aortic replacement surgery. Reconstruction of the ninth intercostal artery alone based on preoperative CT information reduced the duration of surgery

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Fig. 17.6 (a) Curved planar reformation image along the line on (b) the axial computed tomographic (CT) image of a patient with type B aortic dissection. The artery of Adamkiewicz supplied by the left ninth intercostal artery originating from the false lumen of the aortic dissection is visualized. Because the left ninth intercostal artery arises near the re-entry site in this case, the Adamkiewicz artery can be visualized. However, the Adamkiewicz artery originating from a false lumen is generally difficult to visualize by CT. Magnetic resonance (MR) angiography may be useful in such cases


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confused. When considerable venous enhancement is seen, differentiation between the arterial and venous structures is necessary to avoid misinterpretation in localization of the AKA [19] (Figs. 17.1, 17.3–17.6). Without such enhancement, the AKA can be considered the enhanced vessel entering the spinal canal through the intervertebral foramen at the level of the segmental artery (intercostal or lumbar artery) and joining the anterior spinal artery at the tip of a typical hairpin curve [20] (Fig. 17.2). If venous enhancement is absent or only slight, a single enhanced vessel on the midline ventral surface of the spinal cord can be mostly regarded as the anterior spinal artery.

17.2.4.2 Differentiating the Spinal Artery and Vein Although differentiation of the radiculomedullary vein and the AKA is clinically important, as noted, the anterior radiculomedullary vein and AKA can be confused because of the proximity of the anterior spinal vein to the anterior spinal artery near the middle ventral surface of the spinal cord (Fig. 17.1). Compared to the AKA, the radiculomedullary vein tends to run longer in craniocaudal direction from the intervertebral foramen to join the anterior spinal vein. A vessel running more than three vertebral spaces can be regarded as a vein [22]. The most reliable method for differentiation is to detect the full continuity of the entire length from the aorta−the segmental artery (intercostal or lumbar artery), its posterior branch, the AKA, to the anterior spinal artery (Figs. 17.1, 17.3–17.6). However the continuity is sometimes obscured at the intervertebral foramen because of close approximation to the vertebral bone (Fig. 17.2). Therefore, high spatial resolution, especially in the craniocaudal direction, and optimal enhancement are required to improve delineation of the full continuity.

17.2.4.3 Visualization of the Artery of Adamkiewicz by MDCT with Intra-Arterial Contrast Injection MDCT with intra-arterial contrast injection (IACTA) achieves strong enhancement of arterial structures and has been used to improve detection of the AKA [14, 21]. The protocol consists of injection of 100 mL of noniodinated contrast material (350 or 370 mg I/mL) via a pigtail catheter placed in the descending aorta at a rate of 5 mL/s followed by start of scanning 4 s after start of injection, with two consecutive scans performed. The advantages of this protocol are that (1) high attenuation in the aorta, especially in its dorsal portion, improves enhancement of the segmental arteries and AKA and, thereby, detection of the continuity between the AKA and segmental artery and (2) the short contrast bolus in the aorta enables two-phase scanning, with vessels more enhanced in the second phase regarded as venous structures. Disadvantages are that the examination is invasive, and evaluation of the entire aorta is impossible.

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17.2.4.4 Rate of Detecting the Artery of Adamkiewicz by MDCT The rate of detection of the AKA by MDCT is reported from 83 to 94% [14, 19, 20, 27]. Although our initial study reported 90% success in visualizing the AKA within the bony spinal canal, the rate of confirming the continuity from the segmental artery through the AKA remained only 32% [20]. Confirmation has improved with the use of better protocols that include, for example, rapid injection of concentrated contrast material, intra-arterial injection, or magnified reconstruction using brain reconstruction algorithm [1, 12, 14, 19, 22]. Continuity to the AKA from the posterior branch of the segmental artery may be obscured by close approximation of the bony structures, a problem that is effectively resolved using smaller collimation with current increased detector-row MDCT and modified reconstruction algorithm. One report achieved 100% success in both detection and confirmation but included patients with disease of the pancreas rather than aortic aneurysm [1]. The lower visualization rate of AKA in patients with thoracoabdominal aortic aneurysm or dissection is tentatively attributed to dilution of the contrast material in the aorta.

17.2.4.5 Clinical Utility of Visualization of the Artery of Adamkiewicz by MDCT Preoperative Visualization of the AKA Before Open Aortic Surgery Preoperative visualization of the AKA has been reported useful in avoiding postoperative ischemic spinal complications [10, 11, 24]. Even with intraoperative reconstruction of the segmental artery that supplies the AKA, factors that include arterial cross-clamping time and perfusion pressure during surgery, embolus, variation of spinal circulation, and others are thought to contribute to postoperative paraplegia [6,16]. However, preoperative imaging information facilitates selective reconstruction of the intercostal or lumbar artery from which the AKA arises and reduces the total time required for cross-clamping during surgery. The effectiveness of selective perfusion of the preoperatively identified AKA during surgery is also reported [10]. Preoperative identification of the origin of the parent artery of the AKA outside the level of the aorta to be replaced during surgery also shortens operation time by eliminating the need to reconstruct the segmental arteries. Only a limited number of institutions perform preoperative imaging of the AKA. Further study is required to validate the utility of preoperative visualization of the AKA and how information regarding the spinal vascular supply should be used to improve the outcome of aortic surgery.

The AKA and Aortic Stent-Graft Insertion Aortic aneurysm and dissection are increasingly treated endovascularly using aortic stentgraft. Paraplegia incidence is much lower with endovascular procedures than with open surgery [23]. Obscuration of the origin of the many segmental arteries by the stent-graft rarely causes ischemic complication in the spine. The lower complication rate in endovascular procedures is possibly explained by maintenance of the blood supply to the radiculomedullary


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arteries by the intersegmental collateral arteries, maintenance of the collateral supply to the segmental arteries during surgery when the aorta is neither clamped nor opened, and maintenance of relatively stable systemic hemodynamics during endovascular treatment. Because severe artifact from the metallic stent-graft makes MR imaging of the spinal arterial supply difficult after surgery, MDCT is generally used to evaluate the vascular supply to the spinal cord [23]. MDCT can evaluate the segmental arteries and AKA even after the stent-graft procedure and, in most cases, shows that the posterior intercostal arteries and their posterior branches remain opacified, probably owing to retrograde c ollateral circulation.

17.2.4.6 Limitations of MDCT in Visualizing the Artery of Adamkiewicz The use of MDCT to visualize the AKA has several drawbacks. Because MDCT requires more contrast material than conventional aortic CT angiography to visualize the AKA, its use is sometimes difficult in patients with decreased renal function. Use of even updated MDCT technique may not allow confirmation of vessel continuity when the AKA and posterior branch of the segmental artery are located very near bony structures. The AKA is also difficult to visualize by CT when its feeding segmental artery originates from a false lumen of the dissected aorta and it is difficult to achieve adequate enhancement of the false lumen. Combined use of MR angiography and CT angiography increases the success rate of visualization in those situations [28]. In conclusion, with the acknowledged limitations, MDCT is useful in simultaneously evaluating both aortic disease and the AKA, and the clinical utility of preoperative localization of the AKA is reported [4, 5, 9, 10]. Further study with more patients will reveal the value of using imaging to obtain preoperative information about the AKA.

Abbreviations AKA CPR CT IACTA MDCT MPR MRA

Artery of Adamkiewicz Curved planar reformation Computed tomography Intra-arterial computed tomographic angiography Multidetector-row helical computed tomography Multiplanar reconstruction images Magnetic resonance angiography

References 1. Boll DT, Bulow H, Blackham KA, Aschoff AJ, Schmitz BL. MDCT angiography of the spinal vasculature and the artery of Adamkiewicz. AJR Am J Roentgenol. 2006;187:1054–60. 2. Backes WH, Nijenhuis RJ, Mess WH, Wilmink FA, Schurink GW, Jacobs MJ. Magnetic resonance angiography of collateral blood supply to spinal cord in thoracic and thoracoabdominal aortic aneurysm patients. J Vasc Surg. 2008;48:261–71.

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3. Fereshetian A, Kadir S, Kaufman SL, Mitchell SE, Murray RR, Kinnison ML, et al. Digital subtraction angiography in patients undergoing thoracic aneurysm surgery. Cardiovasc Intervent Radiol. 1989;12:7–9. 4. Fukada J, Morishita K, Hyodoh H, Kawaharada N, Muraki S, Miyajima M, et al. Descending or thoracoabdominal aortic aneurysm repair without intercostal vessel reconstruction using contrast magnetic resonance angiography: report of two cases. Surg Today. 2002;32:163–6. 5. Fukada J, Morishita K, Kawaharada N, Yamada A, Harada N, Abe T. Less-invasive thoracic aortic aneurysm repair. Ann Thorac Surg. 2002;74:1244–6. 6. Griepp RB, Ergin MA, Galla JD, Lansman S, Khan N, Quintana C, et al. Looking for the artery of Adamkiewicz: a quest to minimize paraplegia after operations for aneurysms of the descending thoracic and thoracoabdominal aorta. J Thorac Cardiovasc Surg. 1996;112:1202–13. 7. Hachiro Y, Kawaharada N, Morishita K, Fukada J, Fujisawa Y, Kurimoto Y, et al. [Thoracoabdominal aortic aneurysm repair after detection of the Adamkiewicz artery by magnetic resonance angiography; a way to shorten operating time and improve outcome]. Kyobu Geka. 2004;57:280–83 [Article in Japanese]. 8. Heinemann MK, Brassel F, Herzog T, Dresler C, Becker H, Borst HG. The role of spinal angiography in operations on the thoracic aorta: myth or reality? Ann Thorac Surg. 1998; 65:346–51. 9. Hyodoh H, Kawaharada N, Akiba H, Tamakawa M, Hyodoh K, Fukada J, et al. Usefulness of preoperative detection of artery of Adamkiewicz with dynamic contrast-enhanced MR. Radiology. 2005;236:1004–9. 10. Kawaharada N, Morishita K, Fukada J, Yamada A, Muraki S, Hyodoh H, et al. Thoracoabdominal or descending aortic aneurysm repair after preoperative demonstration of the Adamkiewicz artery by magnetic resonance angiography. Eur J Cardiothorac Surg. 2002;21:970–4. 11. Minatoya K, Karck M, Hagl C, Meyer A, Brassel F, Harringer W, et al. The impact of spinal angiography on the neurological outcome after surgery on the descending thoracic and thoracoabdominal aorta. Ann Thorac Surg. 2002;74:1870–2. 12. Nakayama Y, Awai K, Yanaga Y, Nakaura T, Funama Y, Hirai T, et al. Optimal contrast medium injection protocols for the depiction of the Adamkiewicz artery using 64-detector CT angiography. Clin Radiol. 2008;63:880–7. 13. Nijenhuis RJ, Jacobs MJ, Jaspers K, Reinders M, van Engelshoven JM, Leiner T, et al. Comparison of magnetic resonance with computed tomography angiography for preoperative localization of the Adamkiewicz artery in thoracoabdominal aortic aneurysm patients. J Vasc Surg. 2007;45:677–85. 14. Nojiri J, Matsumoto K, Kato A, Miho T, Furukawa K, Ohtsubo S, et al. The Adamkiewicz artery: demonstration by intra-arterial computed tomographic angiography. Eur J Cardiothorac Surg. 2007;31:249–55. 15. Ohtsubo S, Itoh T, Okazaki Y, Matsumoto K, Kato A. Selective perfusion of preoperatively identified artery of Adamkiewicz during repair of thoracoabdominal aortic aneurysm. J Thorac Cardiovasc Surg. 2004;127:272–4. 16. Safi HJ, Miller CC III, Carr C, Iliopoulos DC, Dorsay DA, Baldwin JC. Importance of intercostal artery reattachment during thoracoabdominal aortic aneurysm repair. J Vasc Surg. 1998;27:58–66. 17. Savader SJ, Williams GM, Trerotola SO, Perler BA, Wang MC, Venbrux AC, et al. Preoperative spinal artery localization and its relationship to postoperative neurologic complications. Radiology. 1993;189:165–71. 18. Svenson LG, Crawford ES, Hess KR, Cosseli JS, Safi HJ. Experience with 1509 patients undergoing thoracoabdominal aortic operations. J Vasc Surg. 1993;17:357–70. 19. Takase K, Akasaka J, Sawamura Y, Ota H, Sato A, Yamada T, et al. Preoperative MDCT evaluation of the artery of Adamkiewicz and its origin. J Comput Assist Tomogr. 2006; 30:716–22.


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20. Takase K, Sawamura Y, Igarashi K, Chiba Y, Haga K, Saito H, et al. Demonstration of the artery of Adamkiewicz at multi-detector row helical CT. Radiology. 2002;223:39–45. 21. Uotani K, Yamada N, Kono AK, Taniguchi T, Sugimoto K, Fujii M, et al. Preoperative visualization of the artery of Adamkiewicz by intra-arterial CT angiography. AJNR Am J Neuroradiol. 2008;29:314–8. 22. Utsunomiya D, Yamashita Y, Okumura S, Urata J. Demonstration of the Adamkiewicz artery in patients with descending or thoracoabdominal aortic aneurysm: optimization of contrastmedium application for 64-detector-row CT angiography. Eur Radiol. 2008;18:2684–90. 23. von Tengg-Kobligk H, Böckler D, Jose TM, Ganten M, Kotelis D, Nagel S, et al. Feeding arteries of the spinal cord at CT angiography before and after thoracic aortic endografting. J Endovasc Ther. 2007;14:639–49. 24. Wan IY, Angelini GD, Bryan AJ, Ryder I, Underwood MJ. Prevention of spinal cord ischaemia during descending thoracic and thoracoabdominal aortic surgery. Eur J Cardiothorac Surg. 2001;19:203–13. 25. Williams GM, Perler BA, Burdick JF, Osterman FA Jr, Mitchell S, Merine D, et al. Angiographic localization of spinal cord blood supply and its relationship to postoperative paraplegia. J Vasc Surg. 1991;13:23–33. 26. Yamada N, Okita Y, Minatoya K, Tagusari O, Ando M, Takamiya M, et al. Preoperative demonstration of the Adamkiewicz artery by magnetic resonance angiography in patients with descending or thoracoabdominal aortic aneurysms. Eur J Cardiothorac Surg. 2000;18:104–11. 27. Yoshioka K, Niinuma H, Ehara S, Nakajima T, Nakamura M, Kawazoe K. MR angiography and CT angiography of the artery of Adamkiewicz: state of the art. Radiographics. 2006;26 suppl 1:S63–73. 28. Yoshioka K, Niinuma H, Ohira A, Nasu K, Kawakami T, Sasaki M, et al. MR angiography and CT angiography of the artery of Adamkiewicz: noninvasive preoperative assessment of thoracoabdominal aortic aneurysm. Radiographics. 2003;23:1215–25.

Magnetic Resonance Angiography of the Spinal Cord Blood Supply

18

Robbert J. Nijenhuis and Walter H. Backes

18.1 Introduction For many years, catheter angiography was the only diagnostic modality capable of imaging the very small superficial anterior arteries of the spinal cord prior to aortic aneurysm surgery. Since the beginning of the new millennium, non-invasive computed tomography (CT) and magnetic resonance (MR) angiography methods have been developed to depict normal intradural spinal cord arteries [2,6–8,11,15,19,20,23]. New methods were prompted because of several general and patient population-dependent disadvantages of catheter angiography. Besides the general drawbacks of arterial catheterization and the use of potentially nephrotoxic contrast material, catheter angiography carries a 1 to 2% risk of inflicting severe complications, including paraplegia [9]. Moreover, catheter angiography can be difficult to perform as reflected by the highly variable detection rate of the artery of Adamkiewicz (AKA), the largest supplier of the thoracolumbar spinal cord, ranging from 43 to 86% [3,9,22]. Therefore, the development of non-invasive CT and MR angiography techniques was welcomed. The first report on AKA detection emerged in 2000 [23]. Since then, techniques have strongly improved and now include depiction and differentiation of normal spinal cord arteries and veins, an essential capability. We will outline the relevant vascular radiologic anatomy of the spinal cord, describe fast contrast-enhanced MR angiography techniques and compare them with traditional MR angiography techniques and catheter angiography, demonstrate how current MR angiography is able to differentiate spinal cord arteries from veins, and consider possible future developments and potential pitfalls in spinal cord MR angiography.

R.J. Nijenhuis () Department of Radiology, St Elisabeth Hospital, Tilburg, The Netherlands and Maastricht University Medical Centre (MUMC), Maastricht, Hilvarenbeekseweg 50 The Netherlands S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_18, © Springer-Verlag London Limited 2010

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18.2 Vascular anatomy Correct interpretation of radiologic images of the spinal cord vasculature requires in-depth knowledge of the vascular anatomy of the supplying arteries and draining veins. We refer to Chapter 16 (Part 3) for a detailed description. Because most current applications of noninvasive spinal cord angiography only address the anterior thoracolumbar spinal cord surface, we focus on the features of the supplying arteries and draining veins of this particular part of the spinal cord. Figure 18. 1 provides an anatomical drawing of the supply and drainage of the anterior surface of the spinal cord.

18.2.1 Spinal cord arteries The anterior spinal artery (ASA) is located at the midline of the anterior surface of the spinal cord, measures 0.2 to 0.8 mm in diameter [21], and supplies the anterior two-thirds of the spinal cord through central and pial branches. In fact, the ASA is an ensemble of

Fig. 18.1 Coronal anatomical drawing of the largest inlet artery and outlet vein of the thoracolumbar spinal cord. The largest, and therefore considered the most important supplier of the thoracolumbar spinal cord is the Adamkiewicz artery (AKA). This inlet artery, or anterior radiculomedullary artery, originates from a posterior branch of a segmental artery and courses through a typical hairpin turn to the anterior spinal artery (ASA). The anterior median vein drains the blood from the spinal cord to the radiculomedullary veins. The largest of the outlet veins, the great anterior radiculomedullary vein (GARV), connects to a segmental vein that eventually merges with the vena cava. Note the anatomical similarities in the configuration between the Adamkiewicz artery and the GARV, which both exhibit a hairpin-like (intradural) course. However, the Adamkiewicz artery is normally thinner, has a shorter intradural span, and is located more cranially than the GARV. 1, posterior spinal arteries; 2, spinal cord; 3, ASA; 4, anterior median vein; 5, AKA; 6, segmental artery; 7, GARV; 8, aorta; 9, segmental vein; 10, vertebral body; and 11, vena cava. (Backes WH, et al. Advances in spinal cord MR angiography. AJNR Am J Neuroradiol 2008;29:619–631, © by American Society of Neuroradiology).

18 Magnetic Resonance Angiography of the Spinal Cord Blood Supply

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arterial anastamoses. Several anterior radiculomedullary arteries (ARAs) connect to the ASA at different non-predictable segmental levels, each deriving from the posterior branch of a segmental, i.e., intercostal or lumbar, artery that is directly connected to the aorta (Fig. 18.1). The ARAs connect to the ASA in a typical hairpin configuration, thereby forming its characteristic shape. The AKA, or great ARA, is the largest ARA and therefore considered the most important supplier of the thoracolumbar spinal cord [18]; its diameter measures 0.5 to 1.0 mm [21]. The AKA enters the intradural space from a left segmental artery in 70% of cases and between vertebral levels T8 and L1 in most cases [10].

18.2.2 Spinal cord veins The collecting vein on the anterior cord surface is called the anterior median vein (AMV) and often has a larger diameter (0.4 to 1.5 mm) [21] than the adjacent ASA. The AMV drains the blood through several radiculomedullary veins into the segmental, i.e., intercostal and lumbar, veins and then to the vena cava. The great anterior radiculomedullary vein (GARV) is the largest radiculomedullary vein (diameter 0.8 to 2.0 mm) [21] and has, when compared to the AKA, a longer intradural trajectory. In addition, the outlet point of the GARV is usually located inferior to the inlet point of the AKA. However, because the spatial configuration of the GARV more or less resembles that of the AKA, the two are easily confused, and it is important to differentiate them.

18.3 Clinical relevance Currently, there are two patient populations in whom identification of the AKA is of importance; patients suffering from a thoracoabdominal aortic aneurysm that needs surgical repair and patients with spinal cord arteriovenous fistula (AVF). In the first group, preoperative localization of the AKA, the location of which varies between individuals, and preservation of its supply are of relevance to avoid spinal cord ischemia [5,7,8]. The supply to the AKA in patients with aortic aneurysm can be direct or indirect. The direct supply is through the normal anatomical route displayed in Figs. 18.1 and 18.2; indirect supply is by collateral circulation consequent to occlusion by atherosclerotic plaque of the segmental artery connecting to the AKA. The collateral supply may be confined to one level distant to the originally supplying segmental artery or be very extensive (Figs. 18.3, 4). In patients with spinal cord AVF, localization of the AKA prior to treatment is important to prevent disastrous therapeutic outcome because the AKA and AVF may arise from the same segmental artery (Fig. 18.5). Although most patients in these two populations are adults, in children with syndromes that affect the vasculature of the aorta and spinal cord, i.e., Marfan disease, Takayasu arteritis, and vascular spinal cord malformations, localization of the AKA may also be useful. Especially in young patients, the imaging technique should be preferably non-invasive and when possible without radiation exposure.

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Fig. 18.2 Preoperative magnetic resonance (MR) angiography showing an example of the direct segmental supply to the Adamkiewicz artery (AKA) in a 70-year-old male patient with a Crawford type II aortic aneurysm. The segmental artery (SA) supplying the AKA and anterior spinal artery (ASA) is open (i.e., not occluded) and derives at the same vertebral level as the AKA. (Nijenhuis RJ, et al. MR angiography and neuromonitoring to assess spinal cord blood supply in thoracic and thoracoabdominal aortic aneurysm surgery. J Vasc Surg 2007;45:71–78, © by Elsevier Limited).

18.4 MR angiography 18.4.1 Imaging requirements In clinical practice, implementing spinal cord MR angiography to detect the AKA necessitates attention to several imaging requirements. First, high spatial resolution has to be achieved to image the vessels of submillimeter to millimeter size. Second, because of the similar spatial configuration of the AKA and GARV, their differentiation is crucial to avoid misinterpretation. In addition, the GARV has a larger diameter compared to the AKA and is therefore more easily visualized. Thus, inferring what is artery and what is vein solely on the basis of morphology is highly uncertain; separation must be performed on the basis of temporal differences in the enhancement pattern. This implies that the temporal resolution has to be in the order of the arteriovenous transit time of the spinal cord. Studies in healthy subjects using serial catheter angiography indicate an arteriovenous circulation time of approximately 12 s in the lumbar cord [12]. So, allowing for some hemodynamic variation, temporal resolution should be set at least in the order of around 10 s. Finally, a large craniocaudal field of view has to be applied because of the variable segmental supply to the AKA, being either direct or indirect (Figs. 18.2–18.4). Unfortunately, the three requirements are in conflict with each other because improving one usually degrades one or both of the other requirements.


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Fig. 18.3 Preoperative magnetic resonance (MR) angiography showing an example of the collateral (indirect) segmental supply to the Adamkiewicz artery (AKA) in a 63-year-old male patient with a Crawford type I aortic aneurysm. The segmental artery (SA*) directly connecting to the AKA is partially occluded. The AKA is supplied by an intersegmental collateral (COL) which originates from a segmental artery (SA) one vertebral level below. (Nijenhuis et al. MR angiography and neuromonitoring to assess spinal cord blood supply in thoracic and thoracoabdominal aortic aneurysm surgery. J Vasc Surg 2007;45:71–78, © by Elsevier Limited).

18.4.2 Image acquisition techniques Two three-dimensional (3D) contrast-enhanced MR angiographic approaches have been shown successful in localizing the AKA. One uses a rapidly injected bolus of contrast medium, of which mainly the first passage is exploited during a 20 to 40 s period [23]. The other approach employs a long and slow contrast injection with long acquisition times that vary from 4 to 6 min [24]. The main difference is that the fast approach allows separation between intradural arterial and venous enhancement, whereas the slow approach provides higher spatial resolution but does not allow for this differentiation. Both techniques depend on the administration of intravenous contrast medium and spoiled gradient-echo pulse sequences with short echo time (TE) and repetition time (TR). The shortest possible TE (< 10 ms) is required to obtain the strongest signal enhancement by T1 shortening of the blood at high concentrations of gadolinium-based contrast agent. A short TR (< 10 ms) facilitates differentiation of arteries and veins and enables strong suppression of nonenhanced background tissue (including the spine, cerebrospinal fluid, and cord tissue, which all have relatively longer T1 relaxation times than contrast-enhanced blood) to provide bet-

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Fig. 18.4 Preoperative magnetic resonance (MR) angiography showing an extensive collateral network of intersegmental connections. This sagittal view of the aorta is from a 52-year-old male patient with a Crawford type II thoracoabdominal aortic aneurysm (TAAA). The very well developed intersegmental network (white arrowheads) is supplied by only a few lumbar and thoracic segmental arteries (black arrows). The Adamkiewicz artery was localized to derive from the right 9th thoracic segmental artery (white arrow), which, like most of the lower thoracic and upper lumbar segmental arteries, no longer has direct connection with the aorta. These segmental arteries are, however, still patent because they are filled with contrast material. Their supply through an indirect trajectory lowers their signal intensity. Again, such an extensive collateral network provides important trajectories to supply the spinal cord that may preserve spinal cord function. (Backes WH, et al. Magnetic resonance angiography of collateral blood supply to the spinal cord in thoracic and thoracoabdominal aortic aneurysm patients. J Vasc Surg 2008;48:261–271, © by Elsevier Limited).

ter contrast for the vessels of interest. The technique that is most often applied relies on the high contrast that temporarily exists during the passage of a strong contrast bolus between the arteries on the one hand and the veins and background on the other hand. Table 18.1 provides an overview of the MR angiography protocol used at our institution [13,15]. To accommodate imaging of the entire vertebral column in left-right orientation, acquisition times vary between 36 and 52 s depending on the curvature of the spine of the specific patient. These acquisition times are four to five times longer than the expected arteriovenous transit time. However, accurate timing of contrast arrival in the distal aorta, and its synchronization with the acquisition of centric k-space sampling enable optimal exploitation of the period of approximately 10 s during which there is a large difference in signal intensity between the arteries and veins. In this manner, a first phase 3D angiogram can be obtained in which arteries appear brighter than veins. Repeating the acquisition immediately after the first phase, i.e., by dynamic imaging, produces a second phase 3D image in which the signal intensity of arteries and veins is equally bright. This dynamic approach enables differentiation between the inlet artery and outlet vein on the basis of changes in relative signal intensity. The intensity of the artery should be brightest in the first phase and decrease in the second phase, whereas the intensity of the vein should increase from the first to the second phase (Fig. 18.6). In addition, enhancement of the vertebrae in second phase images helps to identify the vertebral levels of the inlet arteries and outlet veins. Another method of differentiation is acquisition of more than two dynamic phases and use acquisition times of less than 25 s per dynamic phase. With this fast approach, accurate timing is no longer necessary because the start of the dynamic acquisition coincides with the injection of the contrast bolus [5,6].


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b

Fig. 18.5 (a–h). Spinal dural arteriovenous fistula (SDAVF) in a 69-year-old male patient, visualized by magnetic resonance (MR) and catheter angiography. Demonstration of a normal artery supplying the spinal cord and the arterialized veins of an SDAVF supplied from the same segmental artery. The sagittal T2-weighted image reveals a signal increase of the thoracolumbar cord and some flow voids at the dorsal aspect of the spinal cord, which raise the suspicion of a vascular spinal cord abnormality (a, small black double arrowheads). Sagittal maximum-intensity projections (MIPs) of the MR angiography examination showing the overview and localization of the dilated veins (b, small black double arrowheads). The coronal target MR angiography MIP demonstrates the feeding segmental artery of the SDAVF at the first lumbar level (L1) (c, grey arrow). The localization of this origin is confirmed by catheter angiography (d). In addition to demonstrating the fistula with dilated veins (small black double arrowheads), catheter angiography shows an anterior radiculomedullary artery supplying the spinal cord (white arrow), which originates from the same segmental vessel (d). On the targeted multiplanar reformation (MPR) image of the MR angiography examination (e), the anterior radiculomedullary artery could be also visualized (white arrow) and localized at the first lumbar level (L1). Please note that the normal spinal cord supplying artery, which is not involved in the arteriovenous (AV) shunt, is very thin on both the catheter and MR angiography images. The anterior spinal artery (white arrow) is also demonstrated on the oblique sagittal target MR angiography MIP (f) and can be separated from the abnormal veins of the SDAVF lying posteriorly (small black arrows). Corresponding catheter angiography projections of the early (g) and late (h) phases for comparison. (Mull M, et al. Value and limitation of contrast-enhanced MR angiography in spinal arteriovenous malformations and dural arteriovenous fistulas. AJNR Am J Neuroradiol 2007;28:1249–1258, © by American Society of Neuroradiology).

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Table 18.1 Magnetic resonance (MR) angiography protocol for the spinal cord Variable Data Field strength

1.5 Tesla

Coil

Synergy spine phased-array coil

Pulse sequence

3D fast gradient recalled echo, with centric K-space filling

Repetition time / echo time / flip angle

6.0 ms / 1.7 ms / 30°

Directions

Frequency-encoding: cranio-caudal Phase-encoding: anterior-posterior Sagittal slices

Field of view / rectangular field of view

£ 50 cm cranio-caudal / 40–70% reduction anterior-posterior

Acquisition time

36 to 52 s per dynamic phase

Contrast administration

0.2–0.3 mmol Gd-DTPA/kg body weight injected at 3 mL/s

Voxel size

~ 0.8 × 0.8 × 1.2 mm

Dynamic phases

³2

Scan delay

Scan delay time of acquisition is set to filling of abdominal aorta, determined by MR fluoroscopy with 2 mL test bolus

Gd-DTPA: gadolinium-diethylene-triaminepentaacetic acid

18.4.3 Image postprocessing and interpretation Next to acquisition of the 3D dataset, skilled and dedicated postprocessing of images is the deciding factor in detecting the AKA, and it is most often accomplished using (curved) multiplanar reformation (MPR) and targeted maximum-intensity projections (MIPs). The first method to analyze the spinal cord is on axial slices and focuses on the anterior cord surface, scrolling through the stack of axial slices and looking for the cross-sectional enhancement of two dot-like small vessels that represent the cross-section of the AKA and the ASA. After identifying the two vessels, creating an MPR along the line that connects the two vessels will display the hairpin configuration of the AKA and ASA (Fig. 18.7). Because only one plane orientation can be chosen, simultaneous display of both vessels may not be possible; even more importantly, the connection to the segmental artery may not be visualized. Visualization of the course of the AKA and connection to the segmental artery can be improved using curved MPR to design a path along the anterior surface of the cord depicted in the sagittal images (Fig. 18.7). The best method for visualizing the connection between the aorta and ASA on curved MPR images is to create a path on the axial images that starts at the aorta and ends at the anterior cord surface in the ASA. However, this is rather time consuming, needs many iterations, and should only be performed when demonstration of the connection of the AKA to the segmental artery fails with the techniques described above.

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b

c

Fig. 18.6 (a–f ). First and second dynamic phase magnetic resonance (MR) angiography images in a 56-year-old male patient with a thoracolumbar aortic aneurysm demonstrate differentiation of the inlet artery from the outlet vein of the spinal cord. On the sagittal-slice maximum-intensity projection (MIP) of the first dynamic phase, the dilated aorta and its branching segmental arteries are selectively visualized with high intensities (a), whereas on the second-phase MIP, they appear less bright and segmental veins are visualized as well (d). Oblique coronal multi-planar reformation images (MPR, white lines) show one segmental artery on each side of the vertebral column at each vertebral level, except at thoracic vertebral level T9, where it is occluded on the first-phase image (b). The second-phase image shows a combination of arteries and veins enhancing at each vertebral level, except for level T9 where only a segmental vein is present (e). The reformation first-phase image targeted to the spinal canal depicts the inlet artery, i.e., the Adamkiewicz artery (white arrow in c). The reformation image of the second phase displays the Adamkiewicz artery with decreased intensity relative to the first-phase image; the draining vein (black arrow) is visualized more caudally (f), and the epidural venous plexus has become enhanced (asterisk). Note that the midline vasculature most likely represents a combination of the anterior spinal artery (ASA) and anterior median vein (AMV), which remain spatially unresolved (arrowheads in c and f). (Backes WH, et al. Advances in spinal cord MR angiography. AJNR Am J Neuroradiol 2008;29:619–631, © by American Society of Neuroradiology).

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Standard use of MIP technique is not effective because the structures surrounding the cord, such as the aorta, segmental arteries/veins, and fat, often appear more brightly enhanced than the spinal cord vessels. Effective use of the MIP technique relies on targeting the MIPs to a carefully selected sub volume of the angiographic dataset. Hyodoh and colleagues [6] recently introduced a novel and time-efficient imaging technique that avoided the need for sub volume targeting, which they named “double-subtraction MIP.” Their technique consisted of five consecutive dynamic phases, each lasting 23 to 25 s, in which oblique-coronal sections positioned along the posterior line of the vertebral body were acquired. After anterior-posterior acquisition, MIPs were computed for all five phases. The first MIP (without any contrast enhancement) was then subtracted from the last four MIPs. The approach saves time because it does not require definition of targeted sub volumes.

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Fig. 18.7 (a–f). Multiplanar reformation (MPR) of a set of three-dimensional (3D) magnetic resonance (MR) angiography images of the spine demonstrating the visualization of the Adamkiewicz artery (AKA) and the anterior spinal artery (ASA, a-c). Two bright dots on the axial section represent the cross-sections through the AKA and ASA (a). The line between these two dots is the new orientation of the MPR (b). The oblique coronal reformation section shows the spinal cord vessels along the anterior surface of the cord (c). Curved MPR of the same 3D image set shows a caudally more extended part of the ASA (d-f). On the sagittal section, the course of the ASA can be identified on the anterior surface of the cord (d) and followed to define the curved MPR (e). The resulting slightly curved plane represents an image that displays the AKA and a larger part of the ASA (f) compared to that in Figure 7c. (Backes WH, et al. Advances in spinal cord MR angiography. AJNR Am J Neuroradiol 2008;29:619–631, © by American Society of Neuroradiology)

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18.4.4 Detection results Yamada and associates [23] were the first to publish on the detection of the AKA using MR angiography, and they reported a detection rate of 67%. Over the years, improved acquisition and postprocessing techniques have raised detection rates as high as 100% [6,14]. Moreover, the two-phase MR angiography technique has been validated with catheter angiography in patients suspected of harbouring a spinal vascular malformation and showed excellent agreement on AKA localization [16] (Fig. 18.8). In addition, MR angiography appears to be reproducible to localize the AKA, which is important for routine clinical assessment [13].

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Fig. 18. 8 (a–c). Coronal projection of a catheter angiogram (a) and multi-planar reformatted magnetic resonance (MR) angiograms of the early (b) and late (c) phases in a 55-year-old male patient with a spinal dural arteriovenous fistula. On the catheter angiogram (a), the supplying segmental artery (SA) L1, Adamkiewicz artery (AKA, white arrow), and anterior spinal artery (ASA, white arrowhead) are shown. The MR angiogram of the early phase (b) shows the supplying SA L1 and the AKA (white arrow). Enhancement of the anterior midline in the early phase (b) above and below the connection of the AKA with the ASA is most likely enhancement of both the ASA (white arrowheads) and the anterior median vein (AMV, black arrowheads). Diminished signal intensity of the AKA in the latephase MR angiogram (c) contrasts with enhancement of the anterior midline that has clearly increased compared to the early phase (b) as a result of increased venous enhancement. The midline enhancement seen in the late phase (c) is most likely combined enhancement of the AMV and ASA. Furthermore, there is enhancement of the venous plexus (asterisks) in the late phase (c) that is not seen in the early-phase MR angiogram (b). Note that the cephalad enhancement above the connection of the AKA with the ASA is depicted only in the MRA images (b, c) and not in the catheter angiogram (a). (Backes WH, et al. Advances in spinal cord MR angiography. AJNR Am J Neuroradiol 2008;29:619–631, © by American Society of Neuroradiology).

18.4.5 Clinical implementation of MR angiography Localization of the AKA prior to aortic aneurysm surgery is probably the most promising application of spinal cord MR angiography. Kawaharada and colleagues [8] were the first to investigate the role of preoperative AKA localization in relation to the incidence of postoperative paraplegia. In their study, using preoperative MR angiography, they detected


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the AKA in 70 out of 86 patients. The surgical protocol only allowed reimplementation when the segmental artery supplying the AKA was in the region of the graft replacement. Paraplegia developed in two of 16 patients in whom the AKA was not detected. This was in contrast to the 70 patients in whom the AKA was located where no complications of paraplegia occurred. Their report provided the first statistically significant result demonstrating the usefulness of preoperative AKA localization. Nevertheless, the importance of preoperative localization of the AKA and its supplying segmental artery is disputed. First, catheter angiography, the standard of reference, cannot detect the AKA in many patients with aortic aneurysm [9,22], probably because of atherosclerotic occlusion of many of the segmental arteries in thoracoabdominal aortic aneurysm patients. This hinders AKA visualization because opacification must then rely on the selective injection of a small amount of contrast agent in segmental arteries remote to the AKA, which may be too weak to enhance a remotely located AKA that is supplied by collateral circulation. Second, some surgeons claim that reimplantation of the segmental supply to the AKA is unnecessary to prevent paraplegia because they believe the collateral blood supply may take over the supply to the spinal cord [4]. To prove that the contribution of the segmental supply to the AKA is indeed functional in patients with thoracoabdominal aortic aneurysm and that revascularization of this segmental supply can be crucial to maintain spinal cord function, we conducted a study in 60 such patients [14]. We correlated the locations of the aortic cross-clamp positions relative to the MR angiographic localization of the AKA and its segmental supply and measured the results of electrophysiologic cord function in terms of motor-evoked potentials (MEP) during surgery. Declines in MEP occurred only in those 14 patients in whom the AKA was, indeed, cross-clamped (100% negative predictive value). A statistically significant (P < 0.01) association was found between intraoperative spinal cord function and the location of the segmental supply to the AKA relative to the positions of the aortic cross-clamps. Knowledge of the location of the segmental supply to the AKA may also be relevant during the surgical procedure, particularly in situations when an aortic segment is opened, multiple segmental arteries are backbleeding, and the MEP decline. Considering the limited time the cord can sustain hypoperfusion, the surgeon should first start to revascularize those arteries that connect to the AKA to minimize the risk of ischemia. This same study showed occlusion at the aortic origin of the segmental artery directly connecting to the AKA in up to 40% of patients. In these cases, the AKA was supplied through an open segmental artery originating one or more levels above or below the occluded segmental artery (Fig. 18.3). Apart from the segmental supply to the AKA, there are alternative routes by which the anterior spinal axis may be supplied. From our own experience [1] and that of others [4], we know that spinal cord function is not always crucially dependent on segmental supply directly connecting to the AKA. Collaterals can take over supply of the spinal cord to maintain cord function. Recently, these collateral pathways have been visualized with MR angiography (Fig. 18.4) and correlated with intraoperative spinal cord MEP [1]. From this study of Backes and colleagues, it is noteworthy that there was a predictive value of 97% for stable spinal cord function when the segmental supply to the AKA was inside the cross-clamped aortic region and connecting collaterals originating from outside the cross-clamped aortic area were noticed by MR angiography. This finding can be of crucial importance for the surgeon during pre- and intraoperative strategic planning and may explain why some surgeons believe that revascularization of the segmental supply to the AKA is unnecessary. Therefore, we believe that preoperative

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Fig. 18.9 (a–e). Spinal dural arteriovenous fistula (SDAVF) in a 61-year-old male patient. Comparison of visualization capabilities of magnetic resonance (MR) and catheter angiography. Sagittal T2-weighted image showing signal voids raising the suspicion of a vascular spinal cord abnormality (a, small black double arrowheads). Sagittal maximum-intensity projection (MIP) of the MR angiography examination showing the overview and localization of the dilated veins (b, small black double arrowheads). In the coronal target MR angiography MIP, the feeding segmental artery of the SDAVF was depicted to derive from the eighth thoracic level (T8) on the right side. Localization of the shunt is at the dural level (c, grey arrow). Catheter angiography (d) provides more spatial resolution and more insight into the dynamic drainage of the dilated vein than MR angiography offers (e). (Backes WH, et al. Advances in spinal cord MR angiography. AJNR Am J Neuroradiol 2008;29:619–631, © by American Society of Neuroradiology).


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imaging in patients with thoracoabdominal aortic disease is useful and should consist of localizing the AKA with its segmental supply and be used to demonstrate possible collateral supply. MR angiography of the spinal cord can also be used as a screening tool to exclude or confirm and locate the presence of an arteriovenous shunt or other type of vascular spinal cord malformation (Fig. 18.9). The use of non-invasive imaging techniques to demonstrate the vascular malformation is extensively discussed in Chapter 19 (Part 3). As mentioned, non-invasive techniques can also be beneficial in children. Ou’s team [17] has reported excellent AKA detection with a 64-slice CT scanner in a series of 40 children. They were able to reduce effective radiation dose to 4 to 7 mSv using tube current modulation and anatomy-based dose regulation. However, MR angiography may be even more child-friendly because it avoids exposure to radiation and potentially nephrotoxic contrast agents. We have used MR angiography in children of different ages and weights, adjusting the amount of contrast agent, and found that even using only 8 mL of gadolinium-based contrast and employing the described 1.5-T protocol [Table 18.1], we can achieve sufficient spatial and temporal resolution to visualize spinal cord arteries and differentiate them from corresponding veins (Fig. 18.10). Although AKA visualization is rarely imperative in children, highly specialized pediatric centers may benefit from a non-invasive preoperative screening (to detect or exclude spinal vascular malformations) or imaging modality that avoids (unnecessary) diagnostic catheter angiography in children.

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Fig. 18.10 (a–c). Sagittal maximum-intensity projection (MIP) as well as first and second dynamic phase magnetic resonance (MR) angiography images in a 2-year-old male patient. Even with the use of only 8 mL of gadolinium-based contrast, differentiation of the spinal cord inlet artery from the outlet veins is achieved. On the sagittal MIP of the first dynamic phase, the dilated aorta and its branching segmental arteries are visualized (a). The curved multiplanar reformation (MPR) of the first phase (b) image targeted to the anterior cord surface depicts the inlet artery, i.e., the Adamkiewicz artery (AKA, white arrow). On the reformation image of the second phase (c), the AKA displays decreased intensity relative to the first phase image (b), whereas the draining veins (black arrows) show increased signal intensity (c). The epidural venous plexus has become enhanced (asterisks). Note that the midline vasculature most likely represents a combination of the anterior spinal artery and anterior median vein, which remains spatially unresolved (arrowhead in b and c).

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18.5 Outlook Spatial resolution is the main limitation of currently available spinal cord MR angiography techniques. We have shown that MR angiography can depict the major anterior supplier of the spinal cord, the AKA, and differentiate it from the similarly shaped great anterior radiculomedullary vein. However, smaller additional anterior and posterior radiculomedullary arteries have not been visualized. Because the use of a 3-T magnet would theoretically provide better signal-to-noise characteristics, its use may deliver the desired spatial resolution for such visualization. Currently, 1.5-T MR imaging systems have one major advantage over current clinical 3-T systems, and that is the availability of a relatively homogeneous magnetic field in a relatively large craniocaudal field of view of 50 cm. As

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Fig. 18.11 (a–e). Comparison of contrast-enhanced magnetic resonance (MR) angiography of spinal cord vessels using gadopentetate dimeglumine (a,b) and blood-pool agent MS-325 (c-e) in the same patient with a thoracoabdominal aortic aneurysm. For both contrast agents, the first- and second phase angiograms (each 40 s, 0.8 × 0.8 × 1.2 mm) are shown depicting the Adamkiewicz artery (white arrow) and the great anterior radiculomedullary vein (black arrow). The main advantage of a blood-pool agent is that it remains in the circulation substantially longer, which allows long acquisition times (6 min) and, thus, high signal-to-noise ratio and/or high spatial resolution (0.4 × 0.4 × 0.8 mm), as demonstrated in the steady-state image (e). Although steady-state images may provide strong improved image quality compared with fast two-phase images, temporal differentiation between inlet artery and outlet vein is not possible. (Backes WH, et al. Advances in spinal cord MR angiography. AJNR Am J Neuroradiol 2008;29:619–631, © by American Society of Neuroradiology).

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noted, such a large field of view is essential when using MR angiography preoperatively in patients with thoracoabdominal disease. Stronger field inhomogeneities near the vertebral bodies at 3 Tesla give rise to susceptibility artefacts that seem to counteract the increase in signal-to-noise ratio. Therefore 3-T MR angiography remains challenging for depicting spinal cord arteries and their supply routes. Another possibility for improving visualization of even smaller spinal cord vessels might be the use of high T1 relaxivity, such as blood-pool contrast agents, which remain in the system longer than traditional gadolinium contrast media. Apart from using the bloodpool agent as a normal contrast agent in a current MR angiography protocol, additional longer acquisitions can be made that allow higher spatial resolution (Fig. 18.11).

18.6 Conclusions Visualization of the AKA and its segmental supply is now feasible in a reliable, reproducible, and non-invasive way with MR angiography. The technique has been validated and enables differentiation between similarly shaped supplying arteries and draining veins of the spinal cord in adults and children. Depending on the patient population, the segmental supply to the AKA may be direct or indirect. Patients with atherosclerosis may have strongly developed collateral supply pathways. Therefore, besides localizing the AKA and its direct or indirect supply, it is important to search for additional collateral pathways that may become important during thoracoabdominal aortic aneurysm surgery. MR angiography can locate different pathways supplying the spinal cord and is useful in the preoperative work-up of patients undergoing surgery for either aortic aneurysm repair or treatment of a spinal cord arteriovenous fistula.

References 1. Backes WH, Nijenhuis RJ, Mess WH, Wilmink FA, Schurink GW, Jacobs MJ (2008) Magnetic resonance angiography of collateral blood supply to the spinal cord in thoracic and thoracoabdominal aortic aneurysm patients. J Vasc Surg 48:261–271. 2. Boll DT, Bulow H, Blackham KA, Aschoff AJ, Schmitz BL (2006) MDCT angiography of the spinal vasculature and the artery of Adamkiewicz. AJR Am J Roentgenol 187:1054–1060. 3. Fereshetian A, Kadir S, Kaufman SL, Mitchell SE, Murray RR, Kinnison ML, Williams GM (1989) Digital subtraction spinal cord angiography in patients undergoing thoracic aneurysm surgery. Cardiovasc Intervent Radiol 12:7–9. 4. Griepp RB, Ergin MA, Galla JD, Lansman S, Khan N, Quintana C, McCullough J, Bodian C (1996) Looking for the artery of Adamkiewicz: a quest to minimize paraplegia after operations for aneurysms of the descending thoracic and thoracoabdominal aorta. J Thorac Cardiovasc Surg 112:1202–1213. 5. Hyodoh H, Kawaharada N, Akiba H, Tamakawa M, Hyodoh K, Fukada J, Morishita K, Hareyama M (2005) Usefulness of preoperative detection of artery of Adamkiewicz with dynamic contrast-enhanced MR angiography. Radiology 236:1004–1009. 6. Hyodoh H, Shirase R, Akiba H, Tamakawa M, Hyodoh K, Yama N, Shonai T, Hareyama M (2007) Double-subtraction maximum intensity projection MR angiography for detecting the


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artery of Adamkiewicz and differentiating it from the drainage vein. J Magn Reson Imaging 26:359–365. 7. Kawaharada N, Morishita K, Fukada J, Yamada A, Muraki S, Hyodoh H, Abe T (2002) Thoracoabdominal or descending aortic aneurysm repair after preoperative demonstration of the Adamkiewicz artery by magnetic resonance angiography. Eur J Cardiothorac Surg 21:970–974. 8. Kawaharada N, Morishita K, Hyodoh H, Fujisawa Y, Fukada J, Hachiro Y, Kurimoto Y, Abe T (2004) Magnetic resonance angiographic localization of the artery of Adamkiewicz for spinal cord blood supply. Ann Thorac Surg 78:846–852. 9. Kieffer E, Fukui S, Chiras J, Koskas F, Bahnini A, Cormier E (2002) Spinal cord arteriography: a safe adjunct before descending thoracic or thoracoabdominal aortic aneurysmectomy. J Vasc Surg 35:262–2680. 10. Koshino T, Murakami G, Morishita K, Mawatary T, Abe T (1999) Does the Adamkiewicz artery originate from the larger segmental arteries? J Thorac Cardiodvasc Surg 117:898–905. 11. Kudo K, Terae S, Asano T, Oka M, Kaneko K, Ushikoshi S, Miyasaka K (2003) Anterior spinal artery and artery of Adamkiewicz detected by using multi-detector row CT. AJNR Am J Neuroradiol 24:13–17. 12. Launay M, Chiras J, Bories J (1979) Angiography of the spinal cord: venous phase. Normal features. Pathological application. J Neuroradiol 6:287–315 [Article in English, French]. 13. Nijenhuis RJ, Gerretsen S, Leiner T, Jacobs MJ, van Engelshoven JM, Backes WH (2005) Comparison of 0.5-M Gd-DTPA with 1.0-M gadobutrol for MR angiography of the supplying arteries of the spinal cord in thoracoabdominal aortic aneurysm patients. J Magn Reson Imaging 22:136–144. 14. Nijenhuis RJ, Jacobs MJ, Schurink GW, Kessels AG, van Engelshoven JM, Backes WH (2007) Magnetic resonance angiography and neuromonitoring to assess spinal cord blood supply in thoracic and thoracoabdominal aortic aneurysm surgery. J Vasc Surg 45:71–78. 15. Nijenhuis RJ, Leiner T, Cornips EM, Wilmink JT, Jacobs MJ, van Engelshoven JM, Backes WH (2004) Spinal cord feeding arteries at MR angiography for thoracoscopic spinal surgery: feasibility study and implications for surgical approach. Radiology 233:541–547. 16. Nijenhuis RJ, Mull M, Wilmink JT, Thron AK, Backes WH (2006) MR angiography of the great anterior radiculomedullary artery (Akamkiewicz artery) validated by digital subtraction angiography. AJNR Am J Neuroradiol 27:1565–1572. 17. Ou P, Schmit P, Layouss W, Sidi D, Bonnet D, Brunelle F (2007) CT angiography of artery of Adamkiewicz with 64-section technology: first experience in children. AJNR Am J Neuroradiol 28:216–219. 18. Skalski JH, Zembala M (2005) Albert Wojciech Adamkiewicz: the discoverer of the variable vascularity of the spinal cord. Ann Thorac Surg 80:1971–1975. 19. Takase K, Akasaka J, Sawamura Y, Ota H, Sato A, Yamada T, Higano S, Igarashi K, Chiba Y, Takahashi S (2006) Preoperative MDCT evaluation of the artery of Adakmkiewicz and its origin. J Comput Assist Tomogr 30:716–722. 20. Takase K, Sawamura Y, Igarashi K, Chiba Y, Haga K, Saito H, Takahashi S (2002) Demonstration of the artery of Adamkiewicz at multi-detector row helical CT. Radiology 223:39–45. 21. Thron A (2002) Vascular anatomy of the spine. In: Byrne J (ed) Interventional Neuroradiology. Oxford University Press, Oxford, pp 19–23. 22. Williams GM, Roseborough GS, Webb TH, Perler BA, Krosnick T (2004) Preoperative selective intercostal angiography in patients undergoing thoracoabdominal aneurysm repair. J Vasc Surg 39:314–321. 23. Yamada N, Takamiya M, Kuribayashi S, Okita Y, Minatoya K, Tanaka R (2000) MRA of the Adamkiewicz artery: a preoperative study for thoracic aortic aneurysm. J Comput Assist Tomogr 24:362–368. 24. Yoshioka K, Niinuma H, Ehara S, Nakajima T, Nakamura M, Kawazoe K (2006) MR angiography and CT angiography of the artery of Adamkiewicz: state of the art. Radiographics 26 (Suppl 1):S63–73.

Magnetic Resonance Imaging of Spinal Vascular Lesions

19

Shuichi Higano

19.1 Introduction Vascular lesions represent only 3–16% of all spinal cord masses [6] and can cause severe neurological deficits or even fatality if not correctly diagnosed and treated in a timely manner. Because vascular lesions of the spine are rare and diverse and their clinical and imaging features often resemble those of other spinal lesions, such as demyelinating diseases, inflammation, and tumors, they may be misdiagnosed at clinical presentation and their appropriate treatment delayed. Although final diagnosis and therapeutic planning still require conventional catheter angiography, recently advanced less invasive imaging modalities, including magnetic resonance (MR) and computed tomographic (CT) angiography (MRA, CTA), allow accurate diagnosis and yield helpful information for the catheter angiography. MR imaging permits noninvasive evaluation of the anatomy and various pathologies of the spine and spinal cord and, combined with MRA, enables early detection and correct diagnosis of spinal vascular lesions. We introduce some common classifications of spinal vascular lesions, explain their characteristic features, discuss diagnostic neuroradiological techniques focusing on MR imaging, and illustrate some representative cases.

19.2 Classification Because spinal vascular lesions comprise disparate and diverse entities, they have been variously named and classified over the years, which has caused considerable confusion. Tables 19.1–19.3 introduce some representative classifications.

S. Higano Department of Diagnostic Radiology, Tohoku University Graduate School of Medicine, Seiryo-machi, Aoba-ku, Sendai, 980-8574, Japan S. Takahashi (ed.), Neurovascular Imaging, DOI: 10.1007/978-1-84882-134-7_19, © Springer-Verlag London Limited 2010

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In 1987, Rosenblum et al. reviewed 81 patients with vascular lesions of the spine, which they classified as intradural arteriovenous malformations (AVMs) and dural arteriovenous fistulas (AVFs) [14]. They further classified intradural AVMs as intramedullary AVMs (juvenile and glomus types) and direct AVFs. They defined dural AVF as an arteriovenous shunt in the intervertebral foramen supplied by a radicular artery along the nerve root sleeve with drainage into the coronal venous plexus. Intramedullary AVMs had a nidus located at least partially within the cord or pia and supplied by medullary arteries. In 1992, Anson and Spetzler proposed a relatively simple and widely used classification that distinguished four types of spinal arteriovenous shunting lesions [1]:

• Type I, dural AVF, present at the dural root sleeve, supplied by the radiculomedullary artery, and draining into the spinal veins.

• Type II, intramedullary glomus-type AVM, forming a compact nidus within the cord supplied by the anterior or posterior spinal artery.

• Type III, juvenile-type AVM, having a large complex nidus with multiple feeding arteries that may be intramedullary and extramedullary and even extraspinal extension.

• Type IV, intradural perimedullary AVF, located adjacent to the cord, supplied by the anterior or posterior spinal artery with direct drainage to the spinal veins, and further subdivided as IV-A, IV-B, or IV-C by increasing shunt size and degree of flow.

In 1997, Bao et al. reviewed neuroradiological images, therapeutic alternatives, and clinical outcomes of 80 cases and developed a more detailed, five-category classification of spinal vascular malformations [2]: intramedullary AVMs (glomus and juvenile); intradural AVFs; dural AVFs; paravertebral AVMs; and Cobb’s syndrome (Table 19.1). Intradural AVFs were further subclassified into three types (Table 19.1). Paravertebral AVMs are lesions involving the paravertebral musculature, nerve root foramen, prevertebral region, and spinal epidural space. Cobb’s syndrome involves more than one structure (spinal cord, dura, vertebrae, paravertebral spaces, and skin) in the same somite. Recently, Spetzler’s group proposed a modified classification of vascular lesions of the spinal cord on the basis of specific anatomical and pathophysiological factors encountered in their treatment of more than 130 cases and review of the relevant literature (Table 19.2) [8, 16]. They first classified spinal vascular lesions into three categories−neoplasms,

Table 19.1 Classification by Bao et al. (1997) Intramedullary AVMs Glomus type Juvenile type Intradural AVFs Type I: small, low flow, single shunt Type II: high flow, single shunt Type III: large, high flow, multiple feeder with markedly dilated veins Dural AVFs Paravertebral AVMs Cobbs syndrome

19 Magnetic Resonance Imaging of Spinal Vascular Lesions

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Table 19 2 Modified classification by Spezler et al. (2002) Neoplastic vascular lesions Hemangiobalsomas Caverous malformations Spinal aneurysm Arteriovenous lesions Arteriovenous fistulas (AVFs) Extradural Inradural Dorsal Type A, single feeder Type B, multiple feeders Ventral Type A, small shunt, slow flow Type B, larger shunt Type C, giant fistula, markedly distended venous network Arteriovenous malformations (AVMs) Extradural-intradural Intradural Intramedullary compact Intramedullary diffuse Conus medullaris

aneurysms, and arteriovenous lesions. Neoplastic vascular lesions included cavernous malformations and hemangioblastomas; spinal aneurysms unrelated to AVMs, which are rare, were classified as an independent category; and arteriovenous lesions were divided into AVFs and AVMs. They subdivided AVFs into extradural and intradural lesions, and intradural lesions as either dorsal or ventral. AVMs were either extradural–intradural or intradural lesions and the intradural lesions, either intramedullary or conus medullaris AVMs [8, 16]. The intramedullary AVMs were further subdivided as compact or diffuse on the basis of the type of nidus. Table 19.3 correlates this modified classification and those aforementioned. Extradural (epidural) AVFs represent a direct connection between an extradural artery and an epidural venous plexus; the feeding artery usually arises from a radicular artery. Development of a high-flow shunt results in engorgement of the venous system, which leads to compression of the spinal cord and/or adjacent nerve roots. Lesions of this category may be partly included in the paravertebral AVMs of Bao’s classification. Intradural dorsal AVFs (Fig. 19.1), which correlated with Type I or dural AVF (Anson, Bao), were divided into Types A and B depending on the number of feeders (Table 19.2). Intradural ventral AVFs (Fig. 19.2), correponding to Type IV, perimedullary AVF (Anson) or intradural AVF (Bao), were divided into Types A, B, or C on the basis of the size and flow of the fistula (Table 19.2). Extradural–intradural AVMs (Fig. 19.3), which include Type III AVMs (Anson), tend to extend along a discrete somite level. Lesions involving entire structures of a particular somite level would correlate with Cobb’s syndrome (Bao). Intramedullary compact AVMs (Fig. 19.4) correlate with intramedullary glomus-type lesions (Bao) and Type II AVMs (Anson). Some juvenile-type (Bao and Rosenblum) or

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Table 19.3 Relationship among the various classifications Spetzler (2002) Bao (1997) Anson (1992) AVFs Extradural Intradural Dorsal Ventral AVMs Extradural–Intradural Intradural Intramedullary compact Intramedullary diffuse Conus medullaris

Rosenblum (1987)

(Paravertebral AVMs) Dural AVFs Intradural AVFs

Type I, dural AVFs Dural AVFs Intradural direct Type II, perimedullary AVFs AVFs

(Cobb’s syndrome)

(Type III, juvenile AVMs)

Intramedullary AVMs Glomus type Juvenile type?

Type II, glomus AVMs (Type III, juvenile AVMs)

Intramedullary AVMs Glomus type Juvenile type?

Fig. 19.1 Diagram of a dural AVF (Type I, intradural dorsal AVF): left, oblique dorsal view; right, axial view. A dural branch of a radicular artery (large arrow) supplies the network of tiny branches (small arrow) that forms a fistula at the nerve root sleeve with drainage into the dilated and serpentine intradural vein dorsal to the spinal cord. (From reference [16], used with permission from the American Association of Neurological Surgeons)


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Fig. 19.2 Diagram of a perimedullary AVF (Type IV, intradural ventral AVF): left, oblique frontal view; right, axial view. A dilated serpentine vein on the anterior surface of the spinal cord is directly derived from the dilated anterior spinal artery (left, large arrow) via the fistula (left, small arrow). (From [3], used with permission from McGraw-Hill)

Fig. 19.3 Diagram of an extradural–intradural AVM: left, oblique frontal view; right, axial view. The lesion, which partly includes Type III or juvenile-type AVM, tends to extend along a discrete somite level. (From reference [16], used with permission from the American Association of Neurological Surgeons)

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ASA

Fig. 19.4 Diagram of an intramedullary compact AVM (Type II, glomus type): left, oblique frontal view; right, axial view. The lesion has a discrete compact nidus in the cord that is fed by a branch (right, arrow) from the anterior spinal artery (ASA). (From reference [16], used with permission from the American Association of Neurological Surgeons)

Type III (Anson) AVMs may belong to the intramedullary diffuse-type lesions (Fig. 19.5). Because the authors found that some AVMs around the conus medullaris fit none of the categories previously described, they proposed a new category, conus medullaris AVMs. These lesions were located in the conus medullaris and cauda equina and had multiple glomus-type niduses or direct arteriovenous shunts with multiple feeders from anterior or posterior spinal arteries and complex venous drainage. Their pathophysiology included venous hypertension, compression by dilated venous structures, ischemia, and hemorrhage. They often simultaneously produce radiculopathy and myelopathy.

19.3 Imaging Techniques MR imaging is the most informative noninvasive modality for evaluating spinal vascular lesions. Abnormal vascular structures, including feeding arteries, dilated draining veins, and AVM niduses, may be well delineated as flow voids or structures with mixed signal within or around the spinal cord and/or extradural spaces. MR imaging also reveals parenchymal abnormality in the spinal cord, such as edema or hemorrhage. The dilated and tortuous vascular structures related to vascular lesions may be better delineated on three-dimensional (3D) heavily T2-weighted imaging sequences, such as constructive


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Fig. 19.5 Diagram of an intramedullary diffuse AVM; left: oblique frontal view, right: axial view. The lesion, which may partly include juvenile-type or Type III AVM, has a loop of AVMs located in and on the cord with multiple feeding arteries. (From reference [16], used with permission from the American Association of Neurological Surgeons)

interference in steady state (CISS), fast imaging employing steady-state acquisition (FIESTA), or 3D-balanced fast field echo [9, 13]. These techniques also aid differentiation between abnormally dilated vessels and pulsation artifacts of the cerebrospinal fluid sometimes found in the subarachnoid space behind the thoracic spinal cord. Spinal MRA using first-pass (or fast) 3D contrast-enhanced technique is the most useful noninvasive method for diagnosing spinal vascular lesions [5, 9, 11, 12]. MRA can reliably detect or exclude various types of arteriovenous lesions of the spine and localize the level of the shunt in some cases, although it may be difficult to determine the specific type of vascular malformations. These findings would provide information useful in focusing subsequent superselective spinal angiography. CT angiography (CTA) by multidetector-row CT can also demonstrate location of lesions, feeding arteries, and dilated draining veins in good consistency with digital subtraction angiography (DSA) findings [4, 9]. Additionally, 3D information from CTA can show relationships between lesions and surrounding bony structures that may assist surgical planning. However, exposure of the patient to radiation is a major disadvantage of CTA and may be relatively extensive because of the possibly wide scanning range from the foramen magnum to the sacrum. Spinal DSA, which has higher temporal and spatial resolution than CTA and MRA, remains necessary to delineate detailed angioarchitectures, hemodynamics, and exact shunt locations and determine the type of vascular lesions.

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19.4 Characteristic Features of Common Spinal Vascular Lesions In this section, we present detailed characteristics of common vascular lesions of the spine: dural AVFs (Type I, intradural dorsal AVFs); perimedullary AVFs (Type IV, intradural ventral AVFs); and intramedullary AVMs. Table 19.4 summarizes the features of these lesions.

19.4.1 Dural AVFs (Type I, Intradural Dorsal AVFs) 19.4.1.1 Synonyms Type I, dural AVF, intradural dorsal AVF, dural fistula, radiculomeningeal fistula, angioma racemosum (venosum), dorsal extramedullary AVM.

19.4.1.2 General Issues Dural AVFs are arteriovenous shunts (fistula, no nidus) inside the dura mater adjacent to the spinal nerve root that are usually supplied by a dural branch of the radicular artery with drainage into the intradural veins on the surface of the spinal cord (Fig. 19.1). They are the most frequent spinal vascular malformation and account for 70–80% of all spinal vascular malformations, typically affecting elderly men (mean age at diagnosis, 55–60 years; male:female ratio, 5:1) [6, 9]. They commonly occur at the thoracolumbar levels, usually from Th5 to L3. They are considered acquired and possibly attributable to thrombosis of the extradural venous plexus [6].

19.4.1.3 Clinical Presentation and Pathophysiology Patients usually present with progressive weakness of the lower extremities that worsens with exercise. Hemorrhage (subarachnoid hemorrhage) is very rare [7, 9]. Venous drainage from the fistula causes increased pressure and engorgement of the pial veins of the spine, resulting in venous hypertension and cord ischemia, which yield chronic progressive myelopathy. Neurologically, there may be both motor and sensory deficits, and location of the arteriovenous shunt often correlates poorly with the clinical level of spinal dysfunction.

>4th decade

Strong (male:female = 5:1)

Acquired

Progressive myelopathy

Venous hypertension, ischemia

No

Nerve root sleeve, intradural

Branch of radicular artery

Thoracolumbar (Th5-L3)

Embolization or surgical resection

Age

Male predominance

Origin

Presentation

Pathophysiology

Nidus

Site of shunt

Feeders

Favorite level

Treatment

ASA anterior spinal artery, PSA posterior spinal artery

8–19%

Most common, 70–80% of spinal vascular lesion

Epidemiology

Embolization or surgical resection depending on fistula size and feeding vessels Subtype A, B: surgery Subtype C: embolization

Lower thoracic, lumbar

Spinal artery (ASA > PSA)

Ventral aspect of the cord

No

Venous hypertension, hemorrhage, cord compression (aneurysm)

Progressive radiculomyelopathy, subarachnoid hemorrhage

Congenital

Minimal

2nd–4th decade

Perimedullary AVFs

Table 19.4 Summary of the features in the three major vascular lesions Features Dural AVFs

Surgical resection, preoperational embolization if necessary

Cervical, thoracic, lumbar

Spinal artery (ASA, PSA)

On or within the cord

Yes

Hemorrhage, vascular steal, cord compression

Acute myelopathy, Pain, progressive myelopathy

Congenital

Minimal

2nd–3rd decade

15–20%

Intramedullary AVMs

19 Magnetic Resonance Imaging of Spinal Vascular Lesions 495

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Venous hypertensive myelopathy is reversible if treated early but may become irreversible over time. Because the clinical symptoms usually progress slowly, diagnosis may take 2–3 years from initial presentation.

19.4.1.4 MR Findings Conventional MR imaging reveals swollen cord, centromedullary hyperintensity on T2-weighted images (Figs. 19.6a, b and 19.7a), and diffuse parenchymal contrast enhancement (Fig. 19.6c) over the affected segments of the spinal cord. Dilated and serpentine veins can be noted along the cord surface, usually more prominent on the dorsal than the ventral surface (Figs. 19.6b and 19.7a, b). Although the reason for this dorsal prominence of venous dilatation has not been clearly described, it may result from (1) the dominant dorsal development of the normal spinal venous system and (2) the anterior spinal veins, which are located subpial and may not easily be dilated largely enough to be visualized on imaging [9]. Among these findings, increased signal in the cord on T2-weighted images is most common and observed in most cases with dural AVF, although this parenchymal hyperintensity is quite nonspecific. Hurst et al. identified peripheral hypointensity on T2-weighted images as a characteristic feature for dural AVFs, which has not been described for other nonhemorrhagic spinal cord lesions (Fig. 19.7a, c) [7]. This hypointense rim may represent slow flow of blood containing deoxyhemoglobin within the dilated capillaries in the marginal zone of the distended spinal cord. Reported in around half of the cases on conventional MR sequences, flow voids around the cord reflect the dilated perimedullary veins, which are considered the most specific MR feature of dural AVFs [7]. These dilated vessels are usually better delineated on 3D heavily T2-weighted imaging sequences (Fig. 19.7b). Spinal MRA is very useful in diagnosing dural AVFs; it can clearly demonstrate the early filling of dilated and tortuous pial veins that confirm the existence of arteriovenous shunting and may localize the level of the shunt in most cases (Figs. 19.6d and 19.7d).

19.4.2 Perimedullary AVFs (Type IV, Intradural Ventral AVFs) 19.4.2.1 Synonyms Type IV, intradural ventral AVFs, intradural AVFs, intradural direct AVFs, spinal cord AVFs.

19.4.2.2 General Issues Perimedullary AVFs are located directly on the spinal cord in the subarachnoid space and fed by the anterior spinal artery (rarely the posterior spinal artery) with drainage into the

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b

d

e

c

Th12

Fig. 19.6 A 66-year-old man with a dural AVF examined for subacutely progressive sensorimotor deficit in both legs followed by urinary and fecal incontinence. The lower thoracic spinal cord shows centromedullary hyperintensity on T2-weighted image (a, b). Curved or coiled flow voids are noted along the dorsal surface of the cord (b). The contrast-enhanced T1-weighted image (c) demonstrates faint enhancement that corresponds to the area of hyperintensity on the T2-weighted image. On contrast-enhanced MRA (d), the network of tiny vessels (large arrow) supplied from the left Th12 radicular artery communicates with the dilated tortuous vein (small arrows). Superselective digital subtraction angiography (DSA) of the left Th12 intercostal artery (e) reveals dural AVF, corresponding to the MRA finding

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perimedullary veins (Fig. 19.2) [6, 10, 16]. They are usually located ventrally and in the midline [16] and may be associated with aneurysm. The lesions are divided into three subtypes on the basis of shunt size and number of feeding arteries (see classification section). The lesions comprise approximately 8–19% of spinal vascular malformations [6]. They are considered congenital, commonly located in the lower thoracic or lumbar region, and usually present in the second to fourth decade.

19.4.2.3 Clinical Presentation and Pathophysiology The most common presentation is progressive asymmetric radiculomedullary signs of lower extremities. About one-third of patients present with subarachnoid hemorrhage [6]. Cord compression by aneurysm or dilated vessels and venous hypertension cause progressive conus/cauda equina syndrome.

19.4.2.4 MR Findings MR imaging demonstrates enlarged vessels as flow voids, usually anterior to the cord, and may show distortion or displacement of the cord by the enlarged vascular structures. Hyperinstensity of the cord on T2-weighted images reflecting cord edema or parenchymal contrast enhancement may be present (Fig. 19.8a, b). Cases with hemorrhage may show evidence of bleeding, including superficial siderosis, which is more prominent on T2*-weighted images. The dilated vessels are better delineated by 3D heavily T2-weighted images such as CISS or FIESTA (Fig. 19.8c) images.

Fig. 19.7 Dural AVF (Type I, intradural dorsal AVF type A) in a 52-year-old man suffering for a few years from chronic progressive weakness of the bilateral lower extremities followed by associated sensory deficits. The lower thoracic cord is swollen and shows centromedullary hyperintensity on T2-weighted image (a, sagital image; (c) axial image at Th10/11 level) from the level of Th8 to L1 vertebral body. The anterior and lower posterior aspect of the T2-hyperintense cord shows a hypointense rim (small arrows, a). Along the dorsal and ventral cord surface, curvilinear, coiled or spotty structures with signal void are noted (large arrows, a, b), suggesting dilated vessels, which are better delineated on a heavily 3D T2-weighted CISS image (b). Contrast-enhanced MRA (d) clearly demonstrates coiled vessels (arrow 1) arising from the right Th6 intercostal artery (arrow 2) that communicate with a dilated tortuous vessel descending along the midline of the spinal canal (arrow 3). The MRA finding corresponds well with the superselective DSA finding of the right Th6 intercostal artery (e), which clearly delineates a dural AVF

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Th6

c

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d 2 1 Th6

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Fig. 19.8 Perimedullary AVF (Type IV, intradural ventral AVF type A) in a 58-year-old man who presented with constipation followed by sensorimotor deficit of both lower extremities. The lower end of the spinal cord, including the conus medullaris, shows swollen and centromedullary hyperintensity on T2-weighted image (a), where mild inhomogeneous contrast enhancement is noted (b). Serpentine vessels showing contrast enhancement are seen among the cauda equina, which are better delineated on 3D heavily T2-weighted CISS image (c). On partial maximum intensity projection (MIP) image of the contrast-enhanced MRA (d), the Adamkiewicz artery (large white arrow) arising from the left Th11 radicular artery communicates with the slightly dilated anterior spinal artery (ASA, small white arrows). At the level of L3/4 (small yellow arrow), the ASA anastomoses with an ascending tortuous vessel (large yellow arrows), suggesting fistula. The sagittal partial MIP image from CTA (e) demonstrates that the ASA (small white arrows), descending along the anterior surface of the cord, communicates with a tortuous dilated vein (large yellow arrows) at the lower level of the L3 vertebral body (small yellow arrow). Serial DSA images (f1–f3) with superselective injection to the left Th11 intercostal artery reveal the communication of the ASA (small white arrows) with a dilated vein (large yellow arrows) via the fistula (small yellow arrows) at the level of L3, which is shown on MRA and CTA. We could not identify the shunting site on either MRA or CTA before DSA in this case, but we could interpret these images as described by retrospective close comparison with DSA images. We could suspect the existence of AVF by means of MR imaging and CTA, and MRA/CTA images provided useful information for performing DSA

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Contrast-enhanced MRA may reveal a dilated anterior spinal artery and tortuous draining veins prominent along the anterior surface of the cord (Fig. 19.8d). In cases with a tiny shunt, contrast-enhanced MRA may fail to demonstrate abnormal vessels.

19.4.3 Intramedullary AVMs 19.4.3.1 Synonyms Type II AVM, Type III AVM (partly)

19.4.3.2 General Issues Intramedullary AVMs are analogous to intracranial AVMs. The nidus of the lesion is on or within the spinal cord, with a single feeding artery or multiple feeding arteries from branches of the anterior or posterior spinal artery (Figs. 19.4 and 19.5). Up to 20% of cases show aneurysmal formation in the feeding artery, which increases risk of hemorrhage [6]. Enlarged draining veins are often noted on both ventral and dorsal surfaces of the cord. The lesions are noted in 15–20% of spinal vascular lesions, considered congenital, and most commonly found in the cervical and upper thoracic region but may develop at any level, including the filum terminale [6, 15]. Average age at diagnosis is the second to third decade [6]. Spetzler et al. subdivided the lesions into compact and diffuse-types depending on the angioarchitecture of the nidus [8, 16]. The compact type (Fig. 19.4) has a discrete compact nidus within the cord, and the diffuse type (Fig. 19.5), a more extensive nidus within and reaching out of the spinal cord. Normal neural tissues may intervene in the intraparenchymal portion of diffuse-type AVMs.

19.4.3.3 Clinical Presentation and Pathophysiology The most frequent clinical presentation includes hemorrhage (>50%) and motor dysfunction [6, 16]. Hemorrhage (subarachnoid hemorrhage, hematomyelia) may arise from the nidus and be associated with aneurysm or draining veins. Acute or progressive myelopathy or pain may result from hemorrhage, cord compression by the nidus and/or dilated vessels, vascular steal, or venous hypertension. The lesions may represent a part of some systemic vascular syndrome, such as RenduOsler-Weber (hereditary hemorrhagic telangiectasia) or Klippel-Trenaunay syndrome [6].

503


19.4.3.4 MR Findings Dilated feeding and/or draining vessels and intramedullary nidus are usually well delineated as flow voids or structures of mixed signal on conventional MR imaging (Fig. 19.9a–d). Ectatic vascular structures may compress the cord. In some cases with a history of intramedullary hemorrhage, evidence of hemorrhage can be seen especially well on T2*-weighted sequences. Parenchymal hyperintensity is often noted adjacent to the nidus on T2-weighted images (Fig. 19.9a, d) and reflects gliosis, edema, or ischemic changes [6]. Contrast-enhanced MRA usually delineates dilated feeding arteries, the nidus, and tortuous draining veins (Fig. 19.9f), which confirms AVMs, but it cannot reliably demonstrate the detailed angioarhitecture and hemodynamic features of lesions [6].

a

b

c

Fig. 19.9 Intramedullary compact (glomus) AVM in a 35-year-old woman who presented with chronically progessive sensory abnormality of the lower extremities and urinary incontinence. MR imaging demonstrates (a–c) a glomerular structure of mixed intensity on the anterior aspect of the cord at the Th12 level (large arrows). Dilated serpentine vessels are noted to be diffuse along the ventral and dorsal surfaces of the cord. The conus medullaris (small arrows, a, c) is swollen, and shows hyperintensity on T2-weighted image (a) and contrast enhancement on contrast-enhanced T1-weighted image (c). The axial T2-weighted (d) and contrast-enhanced CT (e) images at the Th12 level show a glomerular nidus within and on the anterior aspect of the cord. Contrastenhanced MRA (f) reveals a tangled vascular structure (nidus, large arrow) fed by an enlarged anterior spinal artery (ASA, arrow 2) arising from a dilated radiculomedullary artery of the left L1 (arrows 1) and draining into the dilated tortuous veins (arrow 3). The findings correspond well with the DSA image with superselective injection to the right L1 lumbar artery (g)

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References 1. Anson J, Spetzler R. Classificaiton of spinal arteriovenous malformation. Barrow Neurol Inst Quarterly. 1992;8:2–8. 2. Bao YH, Ling F. Classification and therapeutic modalities of spinal vascular malformations in 80 patients. Neurosurgery. 1997;40:75–81. 3. Carter LP, Spetzler RF. Spinal arteriovenous malformations. Surgical treatment. In: Carter LP, Spetzler RF, Hamilton MG, editors. Neurovascular Surgery. New York: McGraw-Hill; 1995. p. 1197–212. 4. Eddleman CS, Jeong H, Cashen TA, Walker M, Bendok BR, Batjer HH, et al. Advanced noninvasive imaging of spinal vascular malformations. Neurosurg Focus. 2009;26:E9. 5. Farb RI, Kim JK, Willinsky RA, Montanera WJ, terBrugge K, Derbyshire JA, et al. Spinal dural arteriovenous fistula localization with a technique of first-pass gadolinium-enhanced MR angiography: initial experience. Radiology. 2002;222:843–50. 6. Hurst RW. Vascular disorders of the spine and spinal cord. In: Atlas SW, editors. Magnetic resonance imaging of the brain and spine. Philadelphia: Lippincott Williams & Wilkins, a Wolters Kluwer business; 2009. p. 1624–46. 7. Hurst RW, Grossman RI. Peripheral spinal cord hypointensity on T2-weighted MR images: a reliable imaging sign of venous hypertensive myelopathy. AJNR Am J Neuroradiol. 2000;21:781–6. 8. Kim LJ, Spetzler RF. Classification and surgical management of spinal arteriovenous lesions: arteriovenous fistulae and arteriovenous malformations. Neurosurgery. 2006;59:S195–201; discussion S3–13. 9. Krings T, Geibprasert S. Spinal dural arteriovenous fistulas. AJNR Am J Neuroradiol. 2009; 30(4):639–48. 10. Krings T, Mull M, Gilsbach JM, Thron A. Spinal vascular malformations. Eur Radiol. 2005; 15:267–78. 11. Mull M, Nijenhuis RJ, Backes WH, Krings T, Wilmink JT, Thron A. Value and limitations of contrast-enhanced MR angiography in spinal arteriovenous malformations and dural arteriovenous fistulas. AJNR Am J Neuroradiol. 2007;28:1249–58. 12. Pattany PM, Saraf-Lavi E, Bowen BC. MR angiography of the spine and spinal cord. Top Magn Reson Imaging. 2003;14:444–60. 13. Ramli N, Cooper A, Jaspan T. High resolution CISS imaging of the spine. Br J Radiol. 2001;74:862–73. 14. Rosenblum B, Oldfield EH, Doppman JL, Di Chiro G. Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulas and intradural AVM’s in 81 patients. J Neurosurg. 1987;67:795–802. 15. Ross JS, Chen MZ. Part V Vascular and systemic disorders. Section 1 vascular lesions. In: Ross JS, Brant-Zawadzki M, Moore KR, Crim J, Chen MZ, Katzman GL, editors. Diagnostic imaging. Spine. Salt Lake City, Utah: Amirsys; 2004. p. 1–45. 16. Spetzler RF, Detwiler PW, Riina HA, Porter RW. Modified classification of spinal cord vascular lesions. J Neurosurg. 2002;96:145–56.

Index

A Aberrant course of the internal carotid artery, 201–205 Absence of the carotid canal, 200 Absence of the common carotid artery, 198–200 Absence of the proximal external carotid artery, 198–200 ACA. See Anterior cerebral artery Accessory collicular artery (AcCoA), 165, 170 Accessory middle cerebral artery, 212–214 AcCoA. See Accessory collicular artery AChA. See Anterior choroidal artery ACoA. See Anterior communicating artery Adamkiewicz artery (AKA), 427, 432–434, 439, 466, 468–470, 474, 476, 478, 482, 483. See also Great anterior radiculomedullary vein ADC. See Apparent diffusion coefficient AICA. See Anterior inferior cerebellar artery AKA. See Adamkiewicz artery Ambient segment, 142 Ambient (P2) segment, 100 Ambient segment of the PCA, 19 Ambient segment of the SCA (SCA-am), 137 Amnesia, 192, 195 Anastomoses, 63, 77, 79–82, 97, 100, 103, 107, 109, 117, 118 Anastomoses of the anterior choroidal artery, 81 Aneurysm development, 14, 15 Anterior cerebral artery (ACA), 3–7, 12–17, 19, 20, 22, 23, 30, 32, 34, 36, 189–191 Anterior choroidal artery (AChA), 4–7, 12, 16, 20, 24, 26, 33, 34, 36, 40, 53, 54, 58, 71, 72, 75–82, 84–90, 92, 102, 103, 108, 109, 111–113, 115, 117–121 infarct, 77, 84–88

Anterior commissure, 190–195 Anterior communicating artery (ACoA), 54, 56–58, 68–70, 113, 114, 116, 117, 189–195 aneurysms, 191, 195 Anterior course of the proximal vertebral artery, 219, 220 Anterior hippocampal artery, 24, 33, 34, 36 Anterior inferior cerebellar artery (AICA), 132–134, 137, 139–142, 146, 155, 163, 164, 170, 180 Anterior median spinal vein, 442 Anterior median vein (AMV), 466, 467, 474, 478, 482 Anterior medullary segment, 137 Anterior medullary segment of the PICA (PICA-am), 137 Anterior perforated substance, 59 Anterior pontine segment, 142 Anterior pontine segment of the SCA, 137 Anterior radicular artery (ARA), 430, 432, 435 Anterior radiculomedullary artery (A-RMA), 432, 466, 471 Anterior spinal artery (ASA), 132, 133, 139, 145, 146, 162, 163, 427–429, 432–441, 444, 466, 468, 471, 474, 476, 478, 482 Anterior thalamoperforating artery, 93 Anterolateral group of medullary arteries, 146, 147, 162 of mesencephalic arteries, 165, 169 of pontine arteries, 164 Anteromedial group of medullary arteries, 139, 145, 162, 173 of mesencephalic arteries, 165 of pontine arteries, 149, 162, 176 A1 of the ACA, 14, 15 A2 of the ACA, 20 A3 of the ACA, 20 507

508 A4 of the ACA, 20 Aortic origin of the left vertebral artery, 218 Apparent diffusion coefficient (ADC), 419, 420 Arterial basket anastomosis, 435 Arterial spin labeling (ASL), 241–253 Arteria radicularis magna, 432 Arteriovenous fistula spinal cord, 467, 484 Arteriovenous malformations (AVMs), 373 grading system, 374 Arteriovenous shunt (AVS), 421 Arteritis, 364, 366 Artery of Adamkiewicz, 451–461 Artery of lumbar enlargement, 432 ASA. See Anterior spinal artery Ascending cervical artery (AsCA), 429, 433, 448 Ascending lumbar vein (ALV), 447, 448 Ascending ramus, 432 Ascending ramus of the radiculo-medullary artery (AsR), 428, 435 ASL. See Arterial spin labeling Astrocytoma, 311 Atherosclerotic disease, 364 Atherosclerotic lesions, 320, 321 Atherosclerotic macrophages, 338–339 Atherosclerotic plaque, 320 Atherosclerotic vessels, 364 AVMs. See Arteriovenous malformations AVS. See Arteriovenous shunt Axial fluid-attenuated inversion recovery (FLAIR), AVMs, 377–378 Azygos ACA, 191 Azygos anterior cerebral artery, 211 Azygos vein, 445, 447 B BA. See Basilar artery Basal perforating arteries, 53–121 Basilar artery (BA), 132–135, 137, 142, 146, 149, 154, 162–164, 166, 428, 429, 435 Basilar artery fenestration, 221 Basiparallel anatomic scanning (BPAS) MR imaging, 357, 360 Basivertebral vein (BVV), 445, 446 Batson’s plexus, 446 Batson’s venous plexus, 444 – 446 Beevor, 16, 21, 24, 26–28 Bihemispheric anterior cerebral artery, 211 Black dots, 367

Index BLADE software, MR Imaging, 333 Blood oxygen level dependent (BOLD), 405 Boundary zone, 19–23, 30, 32 Bovine aortic arch, 197–198 Brachiocephalic trunk origin of the left common carotid artery, 197–198 Bright-blood plaque imaging, 333, 335 C Capillary telangiectasias, 388–389 Capsular artery, 5, 7 Carotid-anterior cerebral artery anastomosis, 207–209 Carotid artery stenting (CAS), 11 Carotid cave, 9–11 Carotid-cavernous fistula (CCF), 379 Carotid endarterectomy, 339 Carotid rete mirabile, 200 Carotid siphon, 6, 7, 11 Carotid stent placement, 339 Carotid-vertebrobasilar anastomoses, 226–236 CAS. See Carotid artery stenting CASL. See Continuous ASL Catheter angiography, 465, 468, 471, 477, 479–481 Caudomedial branch, 139 Caudomedial branch of the AICA, 137, 140 Cavernous malformation, 384–387 Cavernous segment (C4), 4, 5, 7, 10, 11, 20 CBF. See Cerebral blood flow Cerebral blood flow (CBF), 406 Cerebral sinovenous thrombosis (CSVT), 409–411, 417, 419–421 Cerebral vascular territories, 21 Cervical origin of the posterior inferior cerebellar artery, 221 Cervical segment (C1), 4 Charcot’s artery of cerebral hemorrhage, 63 Chiasmatic branch, 191 Choroidal arteries, 72, 79, 82, 96, 109, 111–113, 119 Choroidal segment (C8), 6 Choroidal segment (C8) of the ICA, 86, 87 Circle of Willis, 12–15, 241, 245, 247, 345, 346, 428, 429, 435 CISS. See Constructive interference in steady state Cisternal segment of the anterior choroidal artery, 72, 76, 77 Claustral arteries, 65 Clinoid segment (C5), 5

509

Index Cobb’s syndrome, 488, 489 Collateral spinal cord supply, 470, 479 Collicular artery (CoA), 146, 165, 169, 170, 172, 173 Communicating segment (C7), 6 Compact type, 502 Computed tomographic (CT) angiography, 296 Computed tomography angiography, 466 Computed tomography angiography (CTA), carotid plaque, 325–327 Congenital absence of the internal carotid artery, 200 Constructive interference in steady state (CISS), 492–493, 498, 500 Continuous ASL (CASL), 242 Contrast angiography, carotid plaque, 325–327 Contrast enhancement, carotid plaque MR imaging, 337–339 Conus arcade, 435 Conus medullaris AVM, 489, 492, 503 Coronal venous plexus, 444 Corona radiata, 65, 67, 82, 84, 86, 100, 118–119, 305–307, 311–313, 315–317 Coronary artery plaque, 320 Cortical segment of the MCA, 18 Cortical segment of the PCA, 19 Corticospinal tract, 67, 86, 118, 119 Costocervical trunk (CCT), 429, 430 Cruciate anastomosis of the conus medullaris, 433–436 CSVT. See Cerebral sinovenous thrombosis D 2D. See Two-dimensional Daughter lobules, 354 3D-CTA. See Three-dimensional CT angiography 4D-CTDSA. See Four-dimensional CT digital subtraction angiography Deep boundary zone, 19, 21, 32 Deep cervical artery (DCA), 429, 430, 433 Dejerine-Roussy syndrome, 100 Descending motor pathways, 295, 305, 310, 316 Descending ramus, 431, 432 Descending ramus of the radiculo-medullary artery (DsR), 428, 435 Developmental venous anomaly (DVA), 396, 397 Diagonal band of Broca, 194, 195

Diffuse type, 492, 502 Diffusion-weighted imaging (DWI), 417, 419 Diffusion-weighted (DW) MR imaging, 305–307, 309, 311, 313 Digital subtraction angiography (DSA), 398–400, 402, 409, 420–421 3D images, 353–355 3-dimensional (3D) high-field (3-tesla [T]) T1-weighted magnetic resonance (MR) imaging, 296 Direct cortical stimulation, 310, 311, 313, 314 Dissecting aneurysm, 355–364 Dissection, 355–364, 368 Distal dural ring, 5, 7–12 Distribution of the basal perforating arteries on transaxial sections of the brain, 100 Dorsospinal artery, 430 DSA. See Digital subtraction angiography Dual (duplicated) origin of the vertebral artery, 218 Duplicated middle cerebral artery, 212–214 Duplicated posterior cerebral artery, 214–215 Duplicated superior cerebellar artery, 225, 227 Dural arteriovenous fistulas (dAVF), 379–382 Dural AVF, 488–490, 494, 496–498 DVA. See Developmental venous anomaly DWI. See Diffusion-weighted imaging Dynamic contrast-enhanced MRA, 355 E Early bifurcated middle cerebral artery, 212, 214 Ehlers-Danlos syndrome, 379 End artery, 19 Endovascular embolization, 355, 382 External vertebral venous plexus, 444–446 Extradural-intradural AVM, 489, 491 F Fast imaging employing steady-state acquisition (FIESTA), 493, 498 Fenestration of the anterior cerebral artery and the anterior communicating artery, 208–209 Fenestration of the ASA, 428 Fenestration of the extracranial vertebral artery, 219–221 Fenestration of the internal carotid artery, 205–206 Fenestration of the middle cerebral artery, 212, 214

510 Fenestration of the posterior cerebral artery, 216–217 Fenestration of the superior cerebellar artery, 225, 228 Fenestrations of the intracranial vertebrobasilar arteries, 221–225 Fetal-type, 14 Fetal type or fetal origin of posterior cerebral artery, 218 Fetal-type PCA, 14 Fibroatheromas, 321 FIESTA. See Fast imaging employing steady-state acquisition Flow void, 347, 350, 357, 359, 364, 367 Fornix, 190–195 Four-dimensional CT digital subtraction angiography (4D-CTDSA), 401 Fusiform aneurysm, 364–366 Fusiform dilatation, 358, 360, 361, 365 Fusion method, 285–288 G Giant, 355, 364 Glioblastoma, 309 Great anterior radiculomedullary vein, 466, 467, 483 H Hemiazygos vein, 445, 447 Hemiparesis, 310, 316, 317 High carotid bifurcation, 198, 201 High-resolution susceptibility imaging (HR SWI), 405 Hippocampal artery, 24, 26, 33, 34, 36–42 Horizontal or sphenoidal segment of the MCA, 18 Horizontal (A1) segment of the ACA, 13–15 HR SWI. See High-resolution susceptibility imaging Hyperplastic anterior choroidal artery, 216 Hypoplastic internal carotid artery, 200, 204 Hypothalamic branch, 191 I ICAp, 87, 90, 91 Image postprocessing (spinal cord MR angiography), 473, 476–477 Imaging protocol (spinal cord MR angiography), 470, 473 Infarction, 305, 306, 316, 317 Infectious aneurysm, 366–368

Index Infective endocarditis (IE), 366, 368 Inferior paramedian mesencephalic arteries (IPMA), 146, 149, 155, 163, 165–167 Inferior petrosal sinus (IPS), 255–257, 262–264, 267, 268, 278, 279, 281 Inferior sagittal sinus (ISS), 256, 258–260, 266 Inferolateral pontine artery (ILPA), 146, 164 Inferolateral trunk, 5, 7 Infracallosal segment of the ACA, 17 Infraoptic course of the anterior cerebral artery, 207 Infundibular dilatation, 353 Insular arteries, 62, 65, 67, 119, 316 Insular gliomas, 295, 299 Insular segment of the MCA, 18 Insulo-opercular gliomas, 295–302 Intercavernous anastomosis, 200, 203 Intercostal artery, 467. See also Segmental arteries Intercostal vein, 445, 447 Internal auditory artery, 132, 141, 142 Internal capsule, 54, 56, 61–63, 65, 67, 70, 74, 77–82, 84, 86–96, 98, 100, 104, 105, 118, 119, 121 Internal carotid arteries (ICA), 3–13, 15–18, 20–22, 24, 32–34, 36 Internal vertebral venous plexus, 444, 445, 448 Interoptic course of the anterior cerebral artery, 207 Interpeduncular fossa, 146, 149, 152, 155, 163, 165–168, 172 arteries, 166 Interpeduncular perforating arteries, 97 Intervertebral vein (IVV), 444–448 Intra-arterial double lumen, 358 Intracranial associated aneurysms, 376 Intracranial hemorrhage, 373 Intracranial hypertension, 380 Intradural arteries, 469 Intradural AVF, 488, 489, 496 Intradural dorsal AVF, 489, 490, 494, 498 Intradural perimedullary AVF, 488, 489 Intradural ventral AVF, 489, 491, 494, 496, 500 Intrahippocampal arteries, 36, 37, 39–41 Intramedullary AVM, 488, 494, 502–504 Intramedullary compact AVM, 489, 492 Intramedullary glomus-type AVM, 488 Intramural hematoma, 355, 357, 359

511

Index Intrasellar or transhypophyseal persistent trigeminal artery, 234 Intravascular ultrasound (IVUS), carotid plaque, 322, 324, 330–331 IPMA. See Inferior paramedian mesencephalic arteries IPS. See Inferior petrosal sinus Ischemic complications, 305–317 Ischemic spinal complications, 451, 460 ISS. See Inferior sagittal sinus J Juvenile-type AVM, 488, 491 K Kissing carotids, 200, 202 L Lacerum segment (C3), 4 Large aneurysms, 347, 349, 355, 356 Lateral branch, 137, 139, 142, 146, 147, 170 Lateral branch (tonsillohemispheric branch), 137 Lateral branch of the PICA, 139, 140 Lateral group of medullary arteries, 154, 163, 175 Lateral group of mesencephalic arteries, 169, 172 Lateral group of pontine arteries, 164, 176 Lateral medullary fossa (LMF), 150, 154, 163 Lateral medullary fossa arteries, 146, 154, 155, 163, 164 Lateral medullary segment, 137 Lateral medullary segment of the PICA (PICA-lm), 137 Lateral posterior choroidal arteries (LPChA), 54, 75, 77, 78, 81, 82, 85, 90, 92–94, 107–112 infarct, 110, 114 Lenticulostriate arteries (LSA), 54, 55, 58–63, 82, 111, 119, 295–302, 306–308, 315–317 Leptomeningeal anastomoses, 19–23 Leptomeningeal anastomoses of Heubner, 30 LMF. See Lateral medullary fossa Long insular arteries, 295, 306–308, 315–317 Longitudinal terminal segment, 37, 39–41 LPChA. See Lateral posterior choroidal arteries (LPChA) LSA. See Lenticulostriate arteries

Lumbar artery, 467. See also Segmental arteries Lumbar veins, 447 M Magnetic resonance angiography, 14, 20, 465–484 Magnetic resonance digital subtraction angiography (MRDSA), 374 Magnetic resonance imaging (MRI), 409, 412, 416–420 of the basal perforators, 119–121 carotid plaque, 322–324, 326–331, 334–337 Magnetizationprepared apid acquisition with gradient echo (MPRAGE), 333 Maximum-intensity projection (MIP), 346, 353, 354, 358, 360 MCA. See Middle cerebral artery MDCT. See Multi-detector row CT; Multidetector row helical CT Medial branch, 137–139, 142, 146, 147, 170, 175 Medial branch (vermian branch), 137 Medial branch of the PICA, 139, 175 Medial posterior choroidal arteries infarct, 113 Medial posterior choroidal arteries (MPChA), 54, 82, 92–94, 102–107, 111, 112, 146, 165, 168–170, 172, 173 Medial striate arteries (MSA), 53–59, 80 Median artery of the corpus callosum, 191, 211–212 Medullary arteries, 19, 21, 30, 306, 307, 316, 317 Medullary arteries of the cerebrum, 82, 119 Medullary venous malformation (MVM), 395–406 Megadolichobasilar artery, 364 Meningohypophyseal trunk, 5, 7 Microangiogram, 305–307, 316 Middle cerebral artery (MCA), 3–7, 12, 16–20, 22–24, 30, 32–34, 36, 306–308, 316, 317 Middle hippocampal artery, 34, 36, 39, 40 M1 of the MCA, 18, 20 M2 of the MCA, 18, 20 M3 of the MCA, 18, 20 M4 of the MCA, 18, 20 MPChA. See Medial posterior choroidal arteries MR angiography (MRA), 14, 16, 20, 347–369

512 MR direct thrombus imaging (MRDTI), 333 MRI. See Magnetic resonance imaging MSA. See Medial striate arteries Multidetector CT (MDCT), carotid plaque, 325–326 Multi-detector row CT (MDCT), 401, 416 Multiplanar reconstruction (MPR) images, 353, 354, 358, 359 MVM. See Medullary venous malformation N Neuronavigation systems, 305, 308, 310, 311 Neurophysiological brain mapping and monitoring techniques, 305 Non-bifurcating cervical carotid artery, 198, 201, 231 O Opercular gliomas, 305–317 Opercular segment of the MCA, 18 Ophthalmic artery, 4, 5, 7–12, 20 Ophthalmic segment (C6), 5 OsiriX, 307 OsiriX imaging software, 296 P Paraclinoid aneurysm, 8, 10–12 Paraclinoid region, 8–12 Parahippocampal artery, 24 Parasellar region, 5, 6 Paraterminal gyrus, 190, 191, 193, 194 Paraventricular region, 85–86 Paravertebral AVM, 488, 489 Partially reconstructed images, 353 Partially thrombosed aneurysms, 351, 352 PASL. See Pulsed ASL PC. See Phase contrast PCA. See Posterior cerebral artery PCoA. See Posterior communicating artery Pearl and string sign, 358, 360 Percutaneous transluminal angioplasty (PTA), 330, 331 Perforators of the internal carotid artery, 86–90 Perifocal edema, 386 Perimedullary AVF, 488, 489, 491, 494, 496, 498, 500–502 Periodically rotated overlapping parallel lines with enhanced reconstruction (PROPELLER), 333 Persistent dorsal ophthalmic artery, 206–207

Index Persistent first cervical intersegmental artery, 219–223 Persistent hypoglossal artery (PHA), 229, 230, 232 Persistent otic artery, 229–231 Persistent primitive olfactory artery, 209–211 Persistent stapedial artery, 201–205 Persistent trigeminal artery lateral type, 230–234 medial type, 231, 232, 234 variants, 229, 232, 234–236 Petrous segment (C2), 4 Phase contrast (PC), 419, 420 imaging, 351, 352 Pial arterial network (PAN), 432, 433, 435, 437–439, 441 Pial venous network (PVN), 442, 443 PICA. See Posterior inferior cerebellar artery Plexal segment of the AChA, 76, 82 P1 of the PCA, 12, 13, 19, 20 P2 of the PCA, 19, 20 P3 of the PCA, 19, 20 P4 of the PCA, 19, 20 Posterior cerebral artery (PCA), 3, 4, 12–14, 16, 19, 22–24, 26, 32–34, 36, 37, 39, 41, 132, 133, 142, 165, 166, 168–170, 172, 173 Posterior communicating artery (PCoA), 4–7, 12–16, 19, 20, 34, 36, 55, 65, 72, 75–79, 81, 87, 91–94, 96, 103–105, 111, 114, 116, 117 Posterior group of medullary arteries, 147 Posterior group of mesencephalic arteries, 169, 172 Posterior group of pontine arteries, 147 Posterior hippocampal artery, 36, 37, 39 Posterior inferior cerebellar artery (PICA), 131–140, 142, 146, 147, 154, 155, 163, 175, 179 Posterior median spinal vein (PMSV), 442, 444 Posterior medullary segment, 137 Posterior medullary segment of the PICA, 133, 137 Posterior perforated substance, 165, 166, 168 Posterior radicular artery (PRA), 430, 435 Posterior spinal artery (PSA), 132, 133, 137–139, 147, 154 Posterolateral spinal arteries, 432, 435, 436, 438

Index Posterolateral spinal vein (PLSV), 442, 444 Posteromedial spinal arteries, 433, 435–437 Precallosal segment of the ACA, 17 Precentral cerebellar arteries (PrC), 133, 137, 142, 144 Precommunicating/interpeduncular segment of the PCA, 19 Precommunicating (P1) segment, 12, 13 Prelaminar branch, 429, 430 Premamillary arteries, 78, 93, 118 Preoptic origin of the anterior cerebral artery, 207 PROPELLER. See Periodically rotated overlapping parallel lines with enhanced reconstruction Proximal dural ring, 5, 8, 9, 11 PSA. See Posterior spinal artery P2 segment, 100 Pseudoaneurysms, 366, 368 PTA. See Percutaneous transluminal angioplasty Pulsed ASL (PASL), 242, 243 Pulvinaric arteries, 95, 100, 103, 109, 110 Q Quadrigeminal segment, 142 of the PCA, 19 of the SCA (SCA-q), 137 QuickTime, 307 R Radial medullary veins, 442, 443 Radicular artery (proper), 431 Radicular vein, 445, 446 Radiculomedullary artery (RMA), 428, 431, 432, 435, 438, 440 Radiculomedullary vein, 444, 446, 453, 456, 459 Radiculopial artery (RPA), 431, 432, 434, 435, 438 Recurrent artery of Heubner (RAH), 54–58, 61–65, 67–70, 116, 118, 211, 214 Regional perfusion imaging (RPI), 241–248, 250, 251, 253 Rendering method, 285, 286, 288–291 Retrocorporeal anastomosis, 431 Retrocorporeal artery, 429, 430 Retrocorporeal vein, 445, 446, 448 Retropharyngeal course of the internal carotid artery, 200 Rostrolateral branch, 139

513 Rostrolateral branch of the AICA (AICA-rl), 133, 137 RPI. See Regional perfusion imaging S Saccular (berry) aneurysm, 345–355 Saltzman type 1, 231, 233 Saltzman type 2, 231, 234 SAS. See Surface anatomy scanning SCA. See Superior cerebellar artery SEA. See Subependymal arteries Segmental arteries, 429, 431, 466–471, 473, 474, 478, 479 Segments of the ACA, 17 Segments of the ICA, 4–7, 12 Segments of the internal carotid artery, 5, 13 Segments of the MCA, 18 Segments of the posterior cerebral artery, 12, 13, 20 Seizures, AVMs, 374 Sensitivity-encoding (SENSE), 296 Septal area, 191–195 Single-photon emission computed tomography (SPECT), 406 SLPA. See Superolateral pontine artery Source images, 347, 350, 354–358, 360–362 SPECT. See Single-photon emission computed tomography Spinal vascular lesions, 487–504 SPMA. See Superior paramedian mesencephalic arteries SPS. See Superior petrosal sinus SSS. See Superior sagittal sinus STA-MCA anastomosis, 248, 251 Striate arterial group, 53–71 String sign, 358, 360 Subarachnoid hemorrhage (SAH), 345, 346, 350, 355, 356, 366–368 Subarcuate artery, 141, 142 Subcallosal area, 190, 193 Subcallosal artery, 69, 113, 117 Subcallosal branch, 190, 191, 195 Subependymal arteries (SEA), 79, 82–86, 107, 113 Sulcal (central) arteries, 429, 434, 435, 437–441 Sulcal (central) vein, 442, 443 Sulco-commissural artery, 437 Superficial boundary zone, 19, 32 Superficial cerebral veins, 285–291

514 Superficial (leptomeningeal) hippocampal arteries, 36–41 Superficial hippocampal artery, 36, 37, 39–41 Superior cerebellar artery (SCA), 132–137, 141–147, 155, 163–167, 169, 170, 172, 173, 182 lateral branch, 137, 142, 146, 147, 170 medial branch, 137, 142, 146, 147, 170 Superior hypophyseal arteries, 5, 7, 9, 10, 87, 111, 116, 117 Superior paramedian mesencephalic arteries (SPMA), 146, 155, 165, 166, 168, 177 Superior petrosal sinus (SPS), 256, 257, 262, 263, 278, 279 Superior sagittal sinus (SSS), 255–261, 266, 267, 271 Superolateral pontine artery (SLPA), 146, 164 Supracallosal segment of the ACA, 17 Supraclinoid portion, 6 Supratonsillar segment, 137 Supratonsillar segment of the PICA, 137 Supreme intercostal artery, 429, 430 Surface anatomy scanning (SAS), 285–288 Surface ultrasonography (US), carotid plaque, 322, 327–329 Susceptibility-weighted images, 367, 369 Susceptibility-weighted imaging (SWI), cavernous malformations, 386 T T2*, 367–369 Terminal cortical segment, 137 Terminal segment, 142 TGA. See Thalamogeniculate arteries Thalamic arterial group, 53, 90–117 Thalamogeniculate arteries (TGA), 54, 90, 92–102, 109, 110, 120, 121, 170, 172 infarct, 109, 110 Thalamoperforate arteries (TPA), 54, 90, 92, 95–99, 101, 106, 108, 111, 114, 116–118, 120, 121, 165, 166, 177 infarct, 106 Thalamotuberal arteries (TTA), 54, 55, 65, 90, 92–96, 98, 103–105, 111, 114, 116, 117 infarct, 104 The artery of cervical enlargement, 432 The radiculopial artery, 431, 432, 434, 435, 438 Thoracoabdominal aortic aneurysm, 467, 468, 470, 479, 483, 484

Index Three-dimensional CT angiography (3DCTA), 401, 416 Thyrocervical artery, 429 Time-of-flight (TOF), 307, 308, 315, 317, 351, 352, 355, 412, 414, 417, 419, 420 Time-of-flight (TOF) MRA, 332 TOF. See Time-of-flight TOF MRA. See Time-of-flight MRA Tonsillohemispheric branch of the PICA, 137 TPA. See Thalamoperforate arteries Transmedullary venous anastomoses (TMVA), 442–444 Traumatic aneurysm, 368–369 Triple anterior cerebral arteries, 211–212 Tuberoinfundibular arteries, 103, 114, 116, 117 Two-dimensional (2D), 420 Type I, 488–490, 494, 498 Type I atherosclerotic lesions, 320, 321 Type I dAVF, 380 Type II, 488, 489, 492, 502 Type II atherosclerotic lesions, 320, 321 Type II dAVF, 380 Type III, 488, 489, 491–493, 502 Type III atherosclerotic lesions, 320, 321 Type III dAVF, 380 Type IV, 488, 489, 491, 494, 496, 500 Type IV atherosclerotic lesions, 320, 321 Type 1 proatlantal artery, 228–231 Type 2 proatlantal artery, 228–230 Type V atherosclerotic lesions, 321 Type VI atherosclerotic lesions, 321 U Ultra-small superparamagnetic particles of iron oxides (USPIO), 339 Uncal branch of the AChA, 24, 26, 36 Unco-parahippocampal branches, 24, 26, 33 Unco-parahippocampal complex, 34 Unilateral absence of A1 segment, 217 Unilateral or bilateral absence of P1 segment, 218 Unilateral or bilateral absence of the posterior communicating artery, 218 Unusual level of bifurcation of the common carotid artery, 198–200 V VA. See Vertebral artery Variations and anomalies of the cerebellar arteries, 225–226 Variations of the circle of Willis, 217–218

515

Index Vascularization of the corticospinal tract, 118 Vascularization of the hypothalamus, 113 Vascularization of the midbrain, 172, 173 Vascularization of the thalamus, 77, 93 Vascular supply of the choroid plexus, 112–113 Vasculopathies, 364 Vasocorona, 438 Vasocoronal network, 437 Vasocoronal perforating arteries, 438, 440, 441 Vein of Galen malformation, 382–385 Vein valves, 446 Venous hypertension, 492, 494, 498, 502 Venous hypertensive myelopathy, 496 Venous sinuses, 285

Ventral longitudinal neural arteries, 427–429 Ventriculofugal arteries, 62, 82, 84–86, 107 Vermian branch of the PICA, 137 Vermian segment of the SCA, 137, 142 Vertebral artery, 131–137, 139, 146, 162, 163, 428–430, 433, 436, 438 Vertebral venous plexus, 444–446, 448 Vertebro-basilar system, 131, 133, 136–143 Volume-rendering (VR), 286, 288, 289, 346, 349, 354 Vulnerable plaque, 320–321 W Watershed infarct, 32 Watershed zone, 19

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