Microneurosurgery In 4 Volumes
M. G. Ya§argil Collaborators: P. J. Teddy and A. Valavanis
Contributors: bL M. Duverno...
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Microneurosurgery In 4 Volumes
M. G. Ya§argil Collaborators: P. J. Teddy and A. Valavanis
Contributors: bL M. Duvernoy, H. M. Keller, St. Kubik, M. Marin-Padilla Illustrated by R Roth
III
A AVM of the Brain, History, Embryology, X J L Pathological Considerations, Hemodynamics, Diagnostic Studies, Microsurgical Anatomy
Geotg Thieme Verlag ТЫете Medical Publishers, Inc, Stuttgart • New York New York
PIONEERS OF MEDICINE
Harvey 1578-1657
Marcello Malpighi 1628-1694: "Omne vivum ex ovo"
Thomas Willis 1622-1675
Rudolf Virchow 1821-1902: "Omnis cellula e cellula"
Microneurosurgery in 4 Volumes
M.G.Ya§argil I Microsurgical Anatomy of the Basal Cisterns and Vessels of the Brain, Diagnostic Studies, General Operative Techniques and Pathological Considerations of the Intracranial Aneurysms II Clinical Considerations, Surgery of the Intracranial Aneurysms and Results
III A AVM of the Brain, History, Embryology, Pathological Considerations, Hemodynamics, Diagnostic Studies, Microsurgical Anatomy
III В AVM of the Brain, Clinical Considerations, General and Special Operative Techniques, Surgical Results, Nonoperated Cases, Cavernous and Venous Angiomas, Neuroanesthesia
IV Clinical Considerations and Microsurgery of the Tumors
Georg Thieme Verlag Thieme Medical Publishers, Inc. Stuttgart • New York New York
I
ТУТ Д
AVM of the Brain, History, Embryology, Pathological Considerations, Hemodynamics, Diagnostic Studies, Microsurgical Anatomy M. G. Ya§argil Collaborators: P.J.Teddy, A.Valavanis Contributors: H. M. Duvernoy, H. M. Keller, St.Kubik, M. Marin-Padilla Illustrated by P. Roth 242 partly colored Figures in 808 Illustrations, 34 Tables
1987 Georg Thieme Verlag Stuttgart • New York
Thieme Medical Publishers, Inc. New York
IV Addresses Yajargil, M. G., M.D., Professor and Chairman Neurosurgical Department University Hospital, Zurich
Teddy, P.J., DPhil, FRCS, Consultant Neurosurgeon The Department of Neurological Surgery Oxfordshire Health Authority The Radcliffe Infirmary, Oxford
Duvernoy, H.M., M.D., Professor Laboratoire d'Anatomie Universite de Besangon, Faculte de Medecine Besancon
Valavanis, A., M. D., Professor Department of Neuroradiology University Hospital, Zurich
Keller, H.M., M.D., Ph.D., Professor of Neurology Zurich
Roth, P., Scientific artist Neurosurgical Department University Hospital, Zurich
Kubik, St., M.D., Professor Institute of Anatomy University of Zurich Marin-Padilla, M., M.D., Professor Department of Pathology Dartmouth College Hanover, New Hampshire
Important Note: Medicine is an ever-changing science. Research and clinical experience are continually broadening our knowledge, in particular our knowledge of proper treatment and drug therapy.insofar as this book mentions any dosage or application, readers may rest assured that the authors, editors and publishers have made every effort to ensure that such references are strictly in accordance with the state of knowledge at the time of production of the book. Nevertheless, every user is requested to carefully examine the manufacturer's leaflets accompanying each drug to check on his own responsibility whether the dosage schedules recommended therein or the contraindications stated by the manufacturers differ from the statements made in the present book. Such examination is particularly important with drugs that are either rarely used or have been newly released on the market.
Some of the product names, patents and registered designs referred to in this book are in fact registered trademarks or proprietary names even though specific reference to this fact is not always made in the text. Therefore, the appearance of a name without designation as proprietary is not to be construed as a representation by the publisher that it is in the public domain. This book, including all parts thereof, is legally protected by copyright. Any use, exploitation or commercialization outside the narrow limits set by copyright legislation, without the publisher's consent, is illegal and liable to prosecution. This applies in particular to photostat reproduction, copying, mimeographing or duplication of any kind, translating, preparation of microfilms, and electronic data processing and storage.
© 1987 Georg Thieme Verlag, RudigerstraBe 14, D-7000 Stuttgart 30, Germany Thieme Medical Publishers, Inc., 381 Park Avenue South, New York, N.Y. 10016 Printed in Germany. Typesetting: R. Hurler, D-7311 Notzingen, typeset on Linotron 202; Printed by K. Grammlich, D-7401 Pliezhausen ISBN 3-13-645001-9 (Georg Thieme Verlag, Stuttgart) ISBN 0-86577-258-4 (Thieme Medical Publishers, Inc., New York) 1 2 3 4 5 6
I _____
V
I Acknowledgement
A number of colleagues assisted me in the preparation of this manuscript. To all of them I owe my most sincere thanks. The original groundwork on the section of central AVMs was prepared some time ago by Dr. St. C. Boone. The early work on cerebellar AVMs was done by Dr. R. M. Crowell. Dr. M. D. Lusk composed much of the work on hemodynamics of AVMs. Dr. R.D. Smith, New Orleans, reviewed and compiled the clinical material. Professor P. Kleihues reviewed the section on pathogenesis. Professor R. Meyermann contributed the section on histology and electron microscopic findings. Dr. H. G. Imhof reviewed the statistics regarding hemodynamics. Virtually the entire work was then reorganized and expanded. Many new ideas and concepts were introduced and older ones reevaluated in the light of more recent literature. The manuscripts were then redrafted. In doing this I was helped by my colleagues Professor A. Valavanis and Dr. P.J. Teddy, to whom I owe speciaHhanks. Dr. K. R. Smith, St. Louis, reviewed the manuscript during his visit to Zurich in summer 1986. Final careful review of the entire manuscript with
corrections and proofreading of the galley proofs were then done by Dr. G.F. Cravens, Dr. M.V. Reichman and Dr. M. V. Yancey. The anatomical pictures, figures, and the text were contributed by Professor St. Kubik. Mr. O. Reinhard and his co-workers (Department of Surgical Photography), produced the excellent photographic reproductions for the text. One of the most outstanding contributions to the whole series of these books has been that of Mr. P. Roth. He has done all of the drawings and diagrams and helped me meticulously in preparing the lay-out and the corrections. A very special thanks goes to both Mrs. M. Traber and Mrs. M. Jent who worked wonders with typing of the manuscript, verification of statistics and literature references, and deciphering illegible handwriting. Finally I would like to cordially thank Dr. h.c. G. Hauff, owner of Georg Thieme Verlag, and his staff, especially Mr. R. Zeller, for their help, cooperation and patience in the preparation of these volumes. M.G. Ya$argil
VI
Preface The operative treatment of vascular malformations using microsurgical techniques began in Zurich in January 1967. During the next 20 years, 414 patients with AVM of the brain and 71 with spinal AVM have been treated surgically. In the same time period 86 patients with cerebral AVM were discharged from our department without operation: In 40 cases the AVMs were operable but the patients refused surgery; in 24 cases the risk of neurological deficits delayed the decision for operative intervention until a later time; in 22 cases (22/500 = 4.4%) the lesion was deemed inoperable. The present volumes III A-III В are intended to relate and analyze our experience gained in the evaluation of 414 operated and 86 nonoperated patients with intracranial AVMs, to review what has been accomplished before and since the advent of microsurgical techniques and to identify the problems remaining in the treatment of these often difficult lesions. Other operated intracranial vascular lesions such as cavernomas (22 cases) and venous angiomas (5 cases) of the brain are also covered briefly. Interventional neuroradiological and surgical procedures for the treatment of cranial dural, spinal dural and medullary AVMs, and
of carotid-cavernous fistulae are not included and will form separate subsequent monographs. The third volume, part A, contains: History, embryology, pathological considerations, hemodynamics, Doppler-techniques, neuroradiology, neurosurgical anatomy, microcirculation, anatomy of the calcarine sulcus. The third volume, part B, contains: General operative techniques, the specific treatment and results of surgery for AVMs of specific locations like convexial (frontal, temporal, insular, parietal, occipital and cerebellar) and deep central (limbic system, corpus callosum, striocapsulothalamic, mesodiencephalic, vein of Galen, splenial, plexal, pontine), special and general statistics regarding morbidity and mortality, complications, the follow-up of nonoperated cases, and a chapter concerning the cavernous and venous angiomas and finally a chapter on neuroanesthesia technique, as utilized in Zurich. M. G. Ya$argil
Introduction This volume attempts to provide the basis for an informed approach toward operating upon AVMs and for learning the actual operative techniques favoured by the authors. It is not meant to be a comprehensive review of all that has been written in the past upon the subject. While much of the material is based upon the findings and theories of others, some is also new. Historically, the development of new surgical disciplines has usually created a need for ever more detailed study of the embryology, anatomy, physiology and anesthesia relevant to that field. The particular needs of the surgeon have often stimulated new methods of carrying out these studies. Neurosurgery has been no exception. Initially, there was the need for a general understanding of the gross anatomy and the relationships and physiology of fiber tracts, cranial nerves and cortical structures, which would allow the surgeon to operate with relative safety within the limits imposed by the instrumentation, anesthesia, and illumination available at that particular time. Cerebral angiography has been a real "breakthrough", not only for diagnostic purposes but also for a better understanding of the hemodynamic and therefore the functional anatomy of the central nervous system. Neuroradiological anatomy, with entirely new perspectives was born and stimulated the neurosurgeon to expand his surgical activities. Refined angiography has permitted accurate study of vessels within the living brain, complementing the work of the pure anatomist. Selective and superselective angiographic techniques have been created as well as interventional neuroradiology. Endovascular neurosur-gery was nothing more than the logical consequence of this accelerated development that has occurred within the last 20 years. Again the perspective concerning the anatomy of the central nervous system has been broadened. The introduction of stereotactic techniques has led to the development of precise atlases of deep areas within the brain (Szikla et al. 1977) and now to computerized three dimensional maps of some
of these structures (Salamon and Huang 1980, Unsold et al. 1982)._________________ I At the same time, microtechniques were introduced into neurosurgery. The ability to reach areas, previously deemed inaccessible, with comparative safety, has dictated the need for a new perspective of the microanatomical and topographical relationship of almost every part of the cranial contents. The work of Basset (1952), Huang (1946-1985), Stephens and Stilwell (1969), Duvernoy (1969-1983), Waddington (1974), Newton and Potts (1974), Williams and Warwick (1975), Lang (1981), Seeger (1978,1980, 1984), has given us, in large part, the necessary topographical details. The elegant series of studies by Rhoton and his associates (1976-1985) describe precise microsurgical details of various brain areas, with their corresponding vasculature, from the point of view of the neurosurgeon. These neuroanatomical publications offer, besides profound and scientifically proven knowledge, very detailed geometrical, trigonometrical-arithmetical data concerning lengths and diameters of various bony, nervous and vascular structures, as well as distances between them. These painstaking precise elaborations are essential background information, indispensable for every neurosurgical procedure. These major works, dealing with the brain stem vasculature comprise a precise review of the neurosurgical anatomy of the base of the brain, brain stem and circle of Willis. Our own account of the basal cisterns and circle of Willis has been described in Volume I. ___ __ Unlike the great majority of aneurysms, arteriovenous malformations and cerebral tumors are not confined to the basal regions of the brain. A new perspective must therefore be adopted, namely the awareness that even the deepest structures may often be reached by working carefully within the sulci and fissures of the brain. The basic patterns of these important anatomical structures should now be studied. Detailed accounts of sulcal and fissural anatomy are rare and generally incomplete but neurosurgery would certainly, benefit from more precise studies in the future.
Introduction Introduction
For this reason it seemed necessary to study, analyze and present the brain anatomy in a new concept, from the view point of the sulcal and fissural systems as well as their relation to the vessels. Originally we planned to study the detailed anatomy of these systems in collaboration with Professor Kubik of Zurich, and to include these results in the present publication. This undertaking, however, turned out to be much more time-consuming than originally estimated. The sulcal system showed an amazing degree of variation giving the impression of being a highly irregular system. As this study proceeded, however, it was realized that this irregularity of the sulcal system conforms to certain general principles. Despite the fascinating preliminary observations, we finally decided not to further delay the publication of this volume and to include here only the detailed anatomy of the calcarine sulcus and its variations and to present some representative displays of general sulcal anatomy. From this contribution by Professor Kubik, the reader will certainly become aware of the fascinating world of j sulci. This interesting work will be continued and ' published later. ' Although knowledge of sulcal and fissural anatomy is extremely important for angioma and tumor surgery, an equally detailed knowledge of microvascular anatomy is essential in order to perfect microsurgical techniques. Only with this knowledge can the neurosurgeon fulfil his goal, which is to preserve and protect the brain parenchyma adjacent to the lesion. Since the pioneering work of Heubner (1872) and Duret (1873) on cerebral microvascularization and microcirculation, subsequent generations of anatomists further refined and extended their original concepts. Stimulated by the recent, excellent work of Duvernoy et al. of Besancon, France, we invited Professor Duvernoy to provide a concise chapter on cerebral microvascularization in order to stimulate younger colleagues to pursue the endeavours of modern anatomists. We have been fortunate to have Professor Marin-Padilla of Hanover/New Hampshire, USA, who has contributed a concise chapter on the embryology of brain vessels, also summarizing the history in this field and adding his new ideas regarding the possible formation of cerebral vascular malformations. The development and maldevelopment of the cerebral venous system was intentionally not included in this volume, since this has been comprehensively described by Huang et al. as recently as 1984. As we already noted in the first volume on aneurysms, the detailed anatomy of an AVM can
References p. 369
only be completely and definitely evaluated at microsurgical exploration and not by any imaging technique. Although superselective angiography provides essential information regarding the composition of an AVM, we would like to have even more sophisticated angiographic techniques for even more precise study of the vascular composition and the hemodynamics of the AVM nidus and its compartments; this is already practiced daily by interventional neuroradiologists for vascular lesions of the skull base as well as head and neck. Professor Valavanis of Zurich, who performed all pre- and postoperative neuroradiological procedures since 1978, has been invited to provide the chapter on the neuroradiological evaluation of cerebral vascular malformations, also summarizing the relative role of CT, MRI and angiography. We refused to perform invasive studies to assess the hemodynamics of AVMs in our patients. However, we routinely applied non-invasive Doppler-ultrasound pre- and postoperatively. Professor Keller of Zurich, has contributed a separate chapter on his Doppler-ultrasound technique, summarizing the principles and the results of this method. Modern neurosurgery is inherently dependant on the advances in neuroanesthetic techniques. During the last 20 years, five groups of anesthesiologists were involved in our daily work. The results achieved in the surgical management of intracranial AVMs were also possible thanks to the great effort of our neuroanesthesiologists, especially Drs. M. Curcic and Dr. M. Kis, who have been responsible for neuroanesthesia during the last 10 years. In Volume III В of this series, the surgical techniques and results as well as the neuroanesthetic technique will be presented in detail.
VII
Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement
1 History. . . . . . . . . . . . . . . . . . . . . . . . . . . . A Short History of the Diagnosis and Treatment of Cerebral AVMs . . . . . . . . 3 Pre-17th Century . . . . . . . . . . . . . . . . . . . . 3 17th-19th Century . . . . . . . . . . . . . . . . . . . 3 Treatment of Extracranial AVM in Earlier and Present Time. . . . . . . . . . . . . . . . . . . . 5 Intracranial Angiomas . . . . . . . . . . . . . . . . 5 The Contributions of Virchow and his Contemporaries . . . . . . . . . . . . . 5 Early Clinical Observations on Intracranial AVMs . . . . . . . . . . . . . . . 6 Surgical Treatment of Cerebral AVMs (18891930) . . . . . . . . . . . . . . . . . . . . . 7
Neurosurgical Approaches Prior to the Introduction of Angiography (1928) . . . . . 9 Neurosurgical Treatment of Intracranial AVM Following the Introduction of Angiography (1930) . . . . . . . . . . . . . . 10 The Limitations of Surgery . . . . . . . . . . . 12 Conservative versus Surgical Treatment . . 14 luminary and Outlook . . . . . . . . . . . . . . . . diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . iurgery . . . . . . . . . . . . . . . . . . . . . . . . . .
20 20 20
2 Embryology. . . . . . . . . . . . . . . . . . . . . . Miguel Marin-Padilla A. Embryogenesis of the Early Vascularization of the Central Nervous System . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . Perineural Vascular Territory of the CNS Vasculature . . . . . . . . . . . . . . . Interneural Vascular Territory of the CNS Vasculature . . . . . . . . . . . . . . . Composition and Organization of the Pial Vascular Plexus . . . . . . . . . . . . . . . . Vascular Perforation of the CNS Surface by Pial Vessels . . . . . . . . . . . . . . . . . . . . Vascular Approach and Contact with the CNS Surface. . . . . . . . . . . . . . . . . . . Endothelial Filopodia Perforation of CNS Surface . . . . . . . . . . . . . . . . . . .
23 23
24 31
In Situ Formation of New Intraneural Vessels . . . . . . . . . . . . . . . . . . . . . . . . . 37 Establishment of the VRC and Interneural Vascular Territory . . . . . . . . . . . . . . . . . 37 Intraneural Vascular Territory of the CNS Vasculature . . . . . . . . . . . . . . . 39 Conclusions . . . . . . . . . . . . . . . . . . . . . . . 44
31
В Vascular Malformation of the Central Nervous System. Embryological Considerations
32
Capillary Telangiectasias and Cavernous Angiomas Venous and Arteriovenous Malformations . . 46 Sturge-Weber-Dimitri's Disease . . . . . . . . . 47
32 32
VIII
Contents
3 Pathological Considerations. . . . . . .
49 Enlargement, Growth, and Regrowth of AVMs. . . . . . . . . . . . . . . . . . . . . . . . . .
Pathogenesis . . . . . . . . . . . . . . . . . . . . . . . Classification of Vascular Malformation
Nomenclature . . . . . . . . . . . . . . . . . . . . . . Classification . . . . . . . . . . . . . . . . . . . . . . The Author's Classification . . . . . . . . . . .
58 61
Location of AVMs . . . . . . . . . . . . . . . . . . . 63 Localization . . . . . . . . . . . . . . . . . . . . . . . 63 Localization of the AVM Within the Brain . . 63 I. Surface Lesions (visible on exploration on the surface of the brain) . . . . . . . . 64 II. Deep Lesions (invisible at exploration on the surface) . . . . . . . . . . . . . . . . . 64
Compact and Diffuse Lesions . . . . . . . . . . .
Enlargement . . . . . . . . . . . . . . . . . . . . . . . 140 Growth . . . . . . . . . . . . . . . . . . . . . . . . . . 146 Pseudo-Growth . . . . . . . . . . . . . . . . . . . 146 True Growth of the AVM . . . . . . . . . . . . 155 Spontaneous Thrombosis and Regression of AVMs.. . . . . . . . . . . . . . . . . . . . . . . . .
161
Multiple AVMs . . . . . . . . . . . . . . . . . . . . . 165 Multiple Cerebral AVMs . . . . . . . . . . . . . . 165 Intracranial and Intraspinal AVMs. . . . . . . . 182 Association of Persistent Trigeminal Artery and AVM . . . . . . . . . . . . . . . . . . . . . . . . .
The Nidus. . . . . . . . . . . . . . . . . . . . . . . . . The Concept of Compartments . . . . . . . . . .
138
74 76
Association of Persistent Trigeminal Artery and AVM . . . . . .
182
Sizes, Shapes, and Elements of AVMs . . . . . 85 Sizes of AVM. . . . . . . . . . . . . . . . . . . . . . 85 Shape. . . . . . . . . . . . . . . . . . . . . . . . . . . . 92 Pure Fistulous AVM . . . . . . . . . . . . . . . . 100 Elements of an AVM . . . . . . . . . . . . . . . . . Ill Arterial Feeders. . . . . . . . . . . . . . . . . . . Ill Venous Drainage . . . . . . . . . . . . . . . . . . 118 Sinuses . . . . . . . . . . . . . . . . . . . . . . . . . 138
Intracranial AVM with Stenosis and Occlusion of Major Vessels . . . . . . . . . . 190 Arterial . . . . . . . . . . . . . . . . . . . . . . . . . . 190 Moya-Moya Disease . . . . . . . . . . . . . . . . . 192 Venous . . . . . . . . . . . . . . . . . . . . . . . AVM Associated with Other Pathological Entities Tumors . . . . . . . . . . . . . . . . . . . . . . . . . . 211
Introduction . . . . . . . . . . . . . . . . . . . . . . .
213
Autoregulation . . . . . . . . . . . . . . . . . . . . . 220
4 Hemodynamics. . . . . . . . . . . . . . . . . . . . 214
Normal Perfusion Pressure Breakthrough . . 221
The Physics of Fluids and Blood Flow . . . . . Pressure, Flow, and Resistance . . . . . . . . . . The Nature of Blood . . . . . . . . . . . . . . . . . Laminar versus Turbulent Flow . . . . . . . . . . Tortuosity of Vessels . . . . . . . . . . . . . . . . . Vascular Distensibility . . . . . . . . . . . . . . . .
214 214 215 215 216 216
Comments on the Normal Perfusion Pressure Breakthrough Theory . . . . . . . . . . . . . . . . 222 Effects of AVMs upon Cerebral Function . . . 227
Cerebral Circulation: Functional Anatomy of the Cerebral Circulation . . . . . . . . . . . . . . . . . . . . . . . .
217
Systemic Effects. . . . . . . . . . . . . . . . . . . . 235
Neuronal Innervation. . . . . . . . . . . . . . . . . Microcirculation . . . . . . . . . . . . . . . . . . . .
217 218
Operative Considerations with Regard to Hemodynamics . . . . . . . . . . . . . . . . . . . 237
AVM Structure. . . . . . . . . . . . . . . . . . . . .
218
Enlargement of AVMs . . . . . . . . . . . . . . . .
218
Preoperative Evaluation. . . . . . . . . . . . . . . 237 Operative Techniques . . . . . . . . . . . . . . . . 237 Postoperative Care . . . . . . . . . . . . . . . . . . 239
Local Mass Effect . . . . . . . . . . . . . . . . . . . 227 Obstruction . . . . . . . . . . . . . . . . . . . . . . . 227 Hemorrhage . . . . . . . . . . . . . . . . . . . . . . . 227 Vascular Steal . . . . . . . . . . . . . . . . . . . . . . 228
Contents
IX
5 Diagnosis and Follow-up of Patients with Cerebral AVM using Doppler Ultrasound
I
Herbert M. Keller
6 Neuroradiological Evaluation A. Valavanis Computed Tomography . . . . . . . . . . . . . . .
250
Magnetic Resonance Imaging (MRI) . . . . . .
259
Cerebral Angiography . . . . . . . . . . . . . . . .
260
Technique . . . . . . . . . . . . . . . . . . . . . . . . Erroneous Findings . . . . . . . . . . . . . . . . . . Angiographic Classification . . . . . . . . . . . . Angiographic Investigation. . . . . . . . . . . . .
260 260 267 269
Limitations of Conventional Selective Angiography . . . . . . . . . . . . . . . . . . . . . . . 276 Venous Phase . . . . . . . . . . . . . . . . . . . . . . 280 Associated Aneurysms . . . . . . . . . . . . . . . . 280 Spasm . . . . . . . . . . . . . . . . . . . . . . . . . . . 280 Summary . . . . . . . . . . . . . . . . . . . . . . . . . 283
284 The Collateral Circulation. . . . . . . . . . . . . 333
7Microsurgical Anatomy of the Brain Supratentorial Sulci and Fissures Fissures . . . . . . . . . . . . . . . . . . . . . . . . . . 296
Interhemispheric (Longitudinal) Fissure . . . . Sylvian Fissure . . . . . . . . . . . . . . . . . . . . . Transverse Fissure . . . . . . . . . . . . . . . . . . .
296 298 301
Vascular Patterns Relating to Supratentorial Sulci
Infratentorial Sulci and Fissures . . . . . . . . . 312 Organization of the Cerebral Microcirculation The Venous System of the Brain . . . . . . . . . 327
I Extracranial Arterial Circle . . . . . . . . . . . II Dural Arterial Circle . . . . . . . . . . . . . . . III Basal Cerebral Arterial Circle of Willis .. IV Cortical Interhemispherical and Intrahemispherical Arterial Circle . . . . . V Cerebellar Arterial Circle . . . . . . . . . . . . VI Transcranial Arterial Circle . . . . . . . . . . VII Spinal Arterial Circle . . . . . . . . . . . . . . VIII Vertebrocervical Arterial Circle . . . . . . IX Primitive Arterial Circle . . . . . . . . . . . .
334 334 334 334 334 334 336 336 336
Pathology of Collateral System . . . . . . . . . . 337
The Veins of Posterior Fossa. . . . . . . . . . . . 332
8 Cortical Blood Vessels of the Human Brain H. M. Duvernoy Blood Vessels of the Cerebral Cortex. . . . . . I Pial Vessels . . . . . . . . . . . . . . . . . . . . . . The Pial Arterial Network . . . . . . . . . . . . The Pial Venous Network . . . . . . . . . . . . Pial Vessels: Discussion . . . . . . . . . . . . . .
338 338 338 339 340
Intracortical Vessels. . . . . . . . . . . . . . Blood Vessels of the Cerebellar Cortex . . . . 345
I Pial Vessels . . . . . . . . . . . . . . . . . . . . . . . . II Intracortical Vessels . . . . . . . . . . . . . . . .
345 347
Contents
9 Anatomy of the Calcarine Sulcus 5. Kubik and B. Szarvas Development . . . . . . . . . . . . . . . . . . . . . . 351 Nomenclature of the Various Parts of the Calcarine Sulcus . . . . . . . . . . . . . . . . 351 The Location of the Meeting Point . . . . . . . 352 Anatomical Variations of the Pars Posterior . 352
Pars Anterior of the Calcarine Sulcus. . . . . . Variations in Course . . . . . . . . . . . . . . . . . Connections and Side-Branches . . . . . . . . .
356 357 357
Inner Structure of the Sulcus Calcarinus . . . 357
Measurements. . . . . . . . . . . . . . . . . . . . . . 366 The Relationship Between the Sulcus Calcarinus
Variations in the Terminal Part of the Pars Posterior and the Calcar Avis, Posterior Horn and Optic . . . . . . . . . . . . . . . . . . . . . . . . . 352 Radiation . . . . . . . . . . . . . 366 Side-Branches and Connections . . . . . . . . . 355 References
.......................
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1
History
A Short History of the Diagnosis and Treatment of Cerebral AVMs As attested by F. Henschen (1955) angiomatous malformations and tumors have been, since Virchow's time, a "problem child" of pathologists. Hamby (1958) defined the main problems posed in understanding the pathology of these lesions and his statements are valid even today: "The origin and anatomy of the cerebral angiomas has frustrated pathologists over the years as much as their treatment has baffled surgeons. An extensive literature has developed, replete wjthj3ictur-esque nomenclature based upon attempts to describe the appearance of lesions seen at the operative table or at necropsy. The surgical descriptions are not entirely basic nor accurate because the bulk of the lesion is largely submerged under the cortex and hence invisible to the examiner. The pathologic descriptions have been faulty because of deflation of the lesion at the time of examination by lack of the expansile blood stream that characterizes them in life. Also confusing the picture of the dead lesion are the alterations produced in the component vessels by blood under arterial pressure, which dilates veins and "arterializes" them to withstand the added stress. Vascular resistance being lowered by the shunt, arteries dilate to carry more blood under less than usual pressure, and lose some of their usual characteristics." However, the introduction of cerebral angiography (Moniz 1927) together with the continuing improvements in the quality of angiograms and the remarkable developments in vascular catheterization techniques (Seldinger 1953, Djindjian 1962) has opened up new dimensions in the study of the morphological and hemodynamic aspects of AVMs. This short historical review may help to understand how we have arrived at the present day
interpretations of AVM pathology and development and how modes of treatment have evolved.
Pre-17th Century Descriptions of vascular malformations of the skin and other visible organs such as eye, lips and ear with occasional comments about their often ugly appearance and the difficulty or impossibility of treatment may be seen in some of the earliest recorded historical manuscripts. The Papyrus Ebers (ca. 1500 ВС) contained descriptions of hemorrhoids, skin tumors, hydro-celes, varicose veins and aneurysms. Kharadly (1956) showed that hernias and aneurysms were operated upon even in those times but not AVMs. The warning, "You must keep your hands off — Noli me tangere" is stated in the relevant chapter Г" Virchow cited prominent physicians like Hippokrates, Galen, Celsus, Aetius, Avicenna, and Vidus Vidius, who were dealing with the diagnosis and treatment of different types of external vascular malformations. Von Bramann (1886) showed that Galen and Delia Groce knew of varicose pulsating swellings and took them to be simple arterial aneurysms. Osier (1915) noted that references to vascular malformations are to be found in the works of Antyllus (2nd Century) and Abulcasis (10th Century).
17th-19th Century The great breakthroughs in the understanding of the systemic circulation and of the cerebral circulation were made by Harvey (1628) and Willis (1664) respectively.
4
References p. 369
1. History
William Hunter ( 17 1 8 - 1 7 8 3) (By kind permission of the President and Council of the Royal College of Surgeons of England)
John Hunter (1728-1793)
The work of Harvey and Willis was subsequently complemented by the discovery of the capillary system by Malpighi (1661) and this paved the way for modern theories regarding the evolution and pathology of AVMs. In the following century (1757) William Hunter was able to identify the clinical characteristics and some hemodynamic aspects of extracranial AVMs. In "Observations on arteriovenous malformation, London Medical Observations and Enquiries, 1762" he wrote: "Vascular malformations of the extremities are caused by an abnormal communication between arteries and veins." Enthusiastic phlebotomists of that period prepared two perfect examples of arteriovenous aneurysm for W. Hunter, which he was quick to recognize (cit. Dandy 1928); at the point of communication between the artery and the vein, he recognized a loud hissing bruit and a strong tremulous thrill: large~tortuous sacs were seen to pulsate; the brachial artery was greatly enlarged and serpentine cephalad to the arteriovenous fistula, but distal to it, the artery became smaller than on the other side. He was able to reduce the size of the vein, stop their pulsation and eliminate both the bruit and the thrill by pressing on a localized spot, which he recognized to be the opening between the artery and vein. It was William Hunter who first suggested the term "anastomosis" to denote the union of the two vessels, whereas the term "collateral" was introduced by his
younger brother John Hunter who also ligated the femoral artery in a case with popliteal aneurysm and proved the efficiency of the collateral arterial system. The broad scientific approach concerning the nature of these impressive aberrations began with pathologists and surgeons 200 years ago who described them as '^erectile tumors" and swellings of the skin and organs. The advent of medical journals enabled the scientists to publish their observations. After 1850 the number of publications concerning these erectile tumors increased rapidly. Between the time of William Hunter (1762) and Sonntag (1919), 65 such publications are to be found: Plenck (1776), Bell (1796), Cruveilhier (1816), Meckel (1818), Dupuytren (1834), Vidal (1846), Rokitansky (1846), Virchow (1851), Gerdy (1852), Schuh (1853, 1866), Busch (1854), Luschka (1854), Esmarch (1854), Lebert (1857), Bennet (1854), and Alibert (1871). More detailed information regarding these papers may be found in the works of Heine (1869), Weber (1869), Korte (1880) and Heineke (1882). Pathological classification based upon varied anatomical descriptions was already becoming clumsy and confusing. By 1894 Wagner had collected from the current literature 24 different nomenclatures. In parallel with changing pathological concepts, the surgery of extracranial AVMs was undergoing a gradual evolution.
References p. 369
Treatment of Extracranial AVM in Earlier and Present Time The endeavours of general surgeons in dealing with the dangerous and disfiguring extracranial vascular malformations (scalp, external ear, eyelids, orbits, cheeks, lips, tongue, palate and neck) are most informative for the interested neurosurgeon (Beck, Berger, Billroth, Brodie, von Bruns, Bryant, Busch, Caradec, Clairmont, Dalrvmple, Dupuytren, Emanuel, Enderlen, German. Goldmann, Heineke, Krause, Lefort, Lieb-kin. Nelaton, Pilz, Roth, Russell, Schwalbe, Schwartz). Their methods of treatment have, in the past, included: 1) Injection of the lesion with: ferrous chloride, glycerin, tannin, chlorzin, carbonic acid, alcohol, I Electrocauterization, 5' Ligation, 4) Extirpation. The variety of modern therapy of external vascular malformations (Williams 1983) shows that therapeutic difficulties still remain in the treatment of these easily approachable lesions: 1) Corticotherapy (new born children), 2) Radiotherapy, 3) Electrocoagulation, -i) Cryotherapy, 5) Surgery, h i Use of laser beam, ~i Embolization. As in neurosurgery, the advice of most plastic surgeons is that simple ligation of feeding vessels is inadequate and inadvisable.
Intracranial Angiomas The Contributions of Virchow and his Contemporaries After exhaustive research work on cavernomas of the liver, Rokitansky (1842-46) came to the conclusion that these were eitherjDenign or malignant tumors independent of the surrounding vascular system. Volume 6 of Virchow's Archive (1854) contains 3 remarkable papers: Esmarch (pp. 34-57): "Uber cavernose Blutgeschwulste", Luschka (pp. 458-470): "Cavernose Blutgeschwulste des Gehirns" and Virchow (pp. 526-554): Uber cavernose (erectile) Geschwulste und Teleangiektasien." Esmarch und Luschka fully supported the neoplasia hypothesis of Rpki-I tansky.
Intracranial Angiomas
Luschka provided one of the earliest descriptions of an intracranial arteriovenous anomaly in a patient with a frontal cavernoma. Luschka recognized two types of "Blut-Geschwulste": 1) Telangiectases (non neoplastic) arising due to a metamorphosis of capillary systems. 2) Cavernous tumors (neoplastic) containing large blood-filled compartments. The young Virchow, who was involved with research into infection of blood vessels, also published (1851) a remarkable paper concerning "the dilatation of small vessels". In this paper he described and discussed thoroughly his own observations and thoughts and clearly refuted the hypothesis of Rokitansky. In 1863 Virchow published a comprehensive study which may be called the first real milestone in the history of the AVM. In the 3rd volume of his monograph, 200 pages (pp. 306-496) are devoted to the phenomenon of the physiological and pathological changes of blood vessels in all organs. His descriptions profoundly contradicted contemporary opinion. He described telangiectases, venous, arterial, arteriovenous and cystic angiomas (nowadays angioblas-tomas), and their transitional types, and discussed in detail the pathogenesis of these malformations. He reflected on the atlas of Cruveilhier and the pioneering work of John Bell (The Principle of Surgery, London 1826, Volume 3, pp. 326-383, First Edition, London 1796). Bell described cavernoma, AVM and angioblastoma but gave all of them the nomenclature of "Aneurysm per Anastomosis". Virchow said: "This description is still perfectly valid, (p. 328): Aneurysm per anastomosis is an entire change of structure; it is a dilatation of veins, in which they are forced and enlarged by the diseased action of their corresponding arteries. Those happen in consequence of original malformation, a violent action of arteries, and a mutual enlargement of arteries and veins, while the intermediate substance of the part is slowly distended into large intermediate cells, which are dilated to formidable reservoirs of blood. — The blood is poured into the cells of such a tumor by innumerable arteries: from these the blood is continually following into veins, which receive it with such patent orifices etc. The veins form a conspicious part of such a tumor, but the intermediate cells are an appreciable part of the structure. . . (p. 397). All this proves that it is a tissue of small arteries and veins; it fills not like a varix slowly; its filling is by distinct thrombs; it is filled by its small and numerous arteries, and its swelling is (like the erection of the penis) produced by the pulsation of
1. History
the arteries, stroke after stroke, pouring out their blood into cells." "The tumor is ajxmgeries of active vessels and the cellular substance through which these vessels are expanded, resembles the cellular parts of the penis, the_gills of a turkey cock or the substance of the placenta, spleen worms." It is interesting to speculate as to whether Bell was describing a cavernoma or an AVM. It certainly jspunds like the modern description of an AVM and its nidus. Virchow (1854), cited Gerdy (1852), who differentiated eight types of "erectile tumors" and noted the great number of publications concerning the "erectile tumors" and the difficulties with their classification. He preferred the term of "angioma" which was introduced by J. Hughes Bennet (1854) instead of the term of "angionoma" which was advocated by Follin (1861). He credited to Plenck (1776) the term "cavernoma", a nomenclature well recognized in the German literature (Meckel 1818). Gushing and Bailey (1928) concluded, quite wrongly, that Virchow believed in the neoplastic nature of vascular malformations as proposed by Rokitansky. This error was most likely due to difficulties with translation of'the original papers. Virchow (1863) divided angiomas into cavernous, simple telangiectatic, racemose, and lymphatic types. Racemose angiomas were divided further into arterial and venous types. Page 474 of Virchow's 3rd Volume (1863) relates to a case of a large extracranial parietooccipital AVM in a man from Florence and described by Vidus Vidius in 1665. Virchow commented that this type of malformation originates through accommodation between artery and vein with consequent dilatation of them (arteriectasie and phleb-ectasie, p. 471). They are of congenital origin (p. 475). They may grow or spontaneously regress (p. 482). The following nomenclature has been used: aneurysma per anastomosis (Bell) or aneurysma anastomoseon (v. Walther), aneurysma per transfusionem (Dupuytren 1834) and other authors used the term of aneurysma arteriovenosum, or aneurysma varicosum. Virchow argued (p. 472) that aneurysms would not arise as a result of arteriovenous communication in traumatic cases, therefore the best term would be aneurysma spurium arterio-venosum. Virchow's main concern was not so much nomenclature as the pathophysiology of the lesions. The founder of cellular pathology had a profound interest in pathophysiology. He performed injection studies on the pregnant uterus and placenta and was fascinated by the temporary but enor-
References p. 369
mous increase in capacity of vessels during _gestation. In 1851 he spoke of "The physiologic paradigm in the corpora cavernosa of sex organs and the paradigm of pathology in cavernoma and telangiectasis", and further questioned as to whether one type of angioma can transform into another by changes in flow and pressure or by cellular proliferation.
Early Clinical Observations on Intracranial AVMs Pfannenstiel (1887) and Kaufmann (1897) observed young (22 and 23 years) primipara patients, who died with acute cerebral symptoms. Autopsy study showed a ruptured varicose anomaly of left thalamus opticus and the vena Galeni in one case, and a ruptured varicose anterior callosal anomaly in another. D'Arcy Power (1888) found, a large AVM in the left sylvian fissure at autopsy on a 20-year-old man who had suffered a hemiplegic stroke and died. Steinheil (1894) described the history and pathologicoanatomical findings in a patient (59 years) with a large right frontal AVM which drained partially to the vein of Galen. He may thus be credited as being among the earliest to describe the symptomatology of the disease. Rizzoli 1873 observed a right occipital pulsating swelling in a 9year-old girl. The pulsation disappeared on compression of the left occipital artery. The girl died from an apparent meningitis (perhaps, in fact, from an intracranial hemorrhage). At autopsy she was found to have an AVM of the occipital region (-duralpial) with drainage to the transverse sinus. There was a defect in the occipital region of the skull so that the pulsation in the AVM could be felt externally. The first clinical diagnosis of a cerebral AVM was made by Hoffmann (1898). Isenschmid followed the history of this patient, who was presented to medical colleagues in Heidelberg, and discussed the differential diagnoses (1912). He pointed out that the clinical diagnosis of cerebral angiomas had never before been made. With the onset of operations for brain tumors around 1890, the number of cases of AVM observed clinically, pathologically and surgically began to rise sharply. At that time, contralateral parietal craniotomy for cases of Jacksonian epilepsy occasionally produced an unexpected AVM. Between 1890 and 1936 there were more than 90 reports of around 120 cases of cerebral AVMs. In the cases of Rizzoli (1873), Hoffmann (1898), Isenschmid (1912), Haenel (1926), Eimer and Mehlhose (1927) and in some of the cases of
References p. 369
Dandy (1928) and Cushing and Bailey (1928) the diagnosis was made clinically. The list of authors who published cases of AVM prior to the angiographic era includes: Morris (1871), Rizzoli2 (1873), von Braman (1886), Pfannenstiel (1887), D'Arcy Power (1888), Giordano1 (1890), Guldenarm and Winkler1 (1891), Pean1 (1891), Starr and McCosh1 (1894), Steinheil (1895), LucasChampionniere1 11896), Kaufmann (1897), Emanuel (1898), Hoff-mann2 (1898), Ribbert (1898), Beadles (1899), Shoyer (1900), Struppler (1900), von Bergmann1 (1901), Chipault1 (1902), Deetz (1902), Rotgans and Winkler1 (1902), Kreutz (1903), Bail (1904), Drysdale (1904), Heitmuller (1904), Simmonds (1905), Strominger (1905), Sternberg (1905, 1907), Falk (1906), Lavillette1 (1906), Diirck (1907), Enders (1908), Krause1 1908), Stertzing (1908), Leischner1 (1909), Ranzel (1909), Tuffier1 (1909), Blank (1910), Therman (1910-13), Znojemsky1 (1910), Abrikosoff (1911), Astwazaturoff (1911), Cassirer and Miihsam1 (1911), Isenschmid2 (1912), Schmolck (1912), Wichern (1912), von Eiselsberg and Ranzi1 (1913), Kaiserling (1913), Wischnewski (1913), Castex and Bolo (1914), Leunenschloss (1914), Maklakow1 (1914), Orbison1 (1915), Verse (1918), Bort (1920), Castex and Romano (1920), Schmidt (1920), Bannister (1921), Hammes (1921), Magnus1 (1921), Nonne1 (1921), Campbell and Ballance1 (1922), Deist (1922), Worster-Drought and Ballance (1922), Miiller (1923), Wohak (1923), Elkin (1924), von Lehoczky (1924), Miihsam1 (1924), Rienhoff (1924), Esser (1925), Federoff and Bogorad (1925), Klimesch (1925), Laves1 (1925), Marx (1925), Reid (1925), Dowling (1926), Glo-bus and Strauss (1926), Haenel2 (1926), Klimesch (1926), Leeser (1926), Bregman (1927), Eimer and Melhose (1927), Herzog (1927), Olivecrona and Lysholm1 (1927), Perthes1 (1927), Worster-Drought and Dickson (1927), Buckley (1928), Cushing and Bailey1'2 (1928), Dandy1 (1928), Ruehl (1929), Yates Paine Brockman1-2 (1930), Brock and Dyke (1932), Krug and Samuels (1932), Dimitri and Balado (1933), Levine (1933), Love (1933), Schaltenbrand (1938), Sattler (1939).
1
Diagnosis made at exploration Diagnosis made clinically rest: Diagnosis made at autopsy 2
Intracranial Angiomas
Surgical Treatment of Cerebral AVMs (1889-1930) Most of these early procedures were carried out by general surgeons (Table 1.1). Giordano is credited to have operated upon the first cerebral AVM in 1889. Regarding his original paper, however, it is clear that he simply ligated a pathological vessel on the left parietal surface and did not expose the remainder of the AVM located in the deep subcortical tissue.
Jules Emile Pean (1830-1898) (By kind permission of Prof. H. M. Koelbing, Director of the Institute of Medical History, University of Zurich)
The first complete excision of a cerebral AVM was made 98 years ago by the famous French surgeon Pean. He treated a 15-year-old boy who had suffered a left sided Jacksonian fit, and made a diagnosis of a right sided central tumor. The operation took place in May 1889 and was described thus by Pean: "Au cours de Г operation, nous nous trouvames en presence d'un angiome des meninges en communication avec les sinus longitudinal superieurs. Malgre sa richesse vasculaire, malgre son etendue, la tumeur put etre enlevee en totalite, sans perte de sang, grace au pincement temporaire et defini-tif des vaisseaux variqueux, dilates, erectiles, dont elle etait composee. A ce propos, nous avons recherche, dans la science les faits de ce genre, qui avaient ete publics et nous n'en avons trouve
8
References p. 369
1. History
aucun qui fut exactement semblable, aucun surtout qui cut ete opere." Pean's conclusion is optimistic: "— De meme qu'il existe des angiomes extracraniens communiquants a travers la voute du crane avec le sinus longitudinal superieur, il existe une variete d'angiomes intracraniens communicants egalement avec les sinus longitudinal
Table 1 . 1
superieurs, mais developpes dans 1'epaisseur des meninges et situes entierement a 1'interieure du crane. Les tumeurs sont justiciaries de la trepanation, 1'hemorrhagie et notamment celle due a la communication avec les sinus, et facilement arretee par le pincement temporaire et definitif."
General surgical operations for cerebral AVM
Pean Giordano 1889
Localization
Operation
Follow-up
R central L parietal
Extirpation Ligature of
good good
1889
vein
Guldenarm
1890
R parietal
Partial extirpation
no follow-up
Guldenarm
1891
R parietal dura-varix
Ligature Extirpation
good
Starr and McCosh
1894
L parietal small angioma
Extirpation
good
Lucas-Championniere
1896
R parietal
Extirpation
good
Rotgans et al.
1897
R parietal
Partial extirpation
good
Rotgans et al.
1898
L parietal
Ligature
good
Chipault
1897-1898
L parietal
3 operations, partial
no follow-up
Von Bergmann
1901
L frontoparietal
Ligature
death, hemorrhage
Lavillette
1906
R parietal
Ligature
no follow-up
Krause
1907
L parietal
Ligature
good
Von Eiselsberg and Ranzi
1907-1908
R parietal (2 cases)
Ligature
good
Leischner
1907
L central
Ligature
good
Tuffier
1909
L central
Ligature
good
Znojemsky
1910
Cerebellum
Exploration
death, hemorrhage
Cassirer and Muhsam
1910
R frontoparietal
Extirpation
good
Von Eiselsberg and Ranzi
1913
R paracentral
Ligature of vein
unchanged
Wischnewski
1913
R parietal
Ligature
good
Magnus
1914
L central
Exploration
x-ray, good
Maklakow and Minz
1914
Cerebellum
Exploration
death
Orbison et al.
1915
-
-
-
Nonne
1921
L parietal
Partial extirpation
good
Campbell and Ballance
1922
R parietal
Ligature 2 operations
hemiplegia
Laves
1922
L sylvian fissure
Ligature
death, hemorrhage
Perthes
1923
R parietal
Ligature
good
Yates and Paine
1930
V. Galeni
Exploration
death
Brock and Dyke
1932
R frontoparietal
Exploration
x-ray, good
The original descriptions of these impressive and dramatic attempts to remove cerebral AVMs make fascinating reading.
References p. 369
Neurosurgical Approaches Prior to the Introduction of Angiography (1928) Gushing (1909-1928) and Dandy (1921-1926) each described their operative experiences in 14 and 15 cases respectively, of venous and arteriovenous malformation and added cases from the literature. Both of their series were published in the same year (1928) and reading the original descriptions it seems likely that all their cases were true arteriovenous malformations. Dandy felt that the only way to cure an arteriovenous aneurysm was to ligate the entering arteries or to excise the whole vascular tumor. Earlier, he had lost one patient from hemorrhage during the operation and a second case from intracerebral hemorrhage following total extirpation and he wrote: "But the radical attempt at cure is attended by such supreme difficulties and is so exceedingly dangerous as to be contraindicated except in certain selected cases... As in most cerebral lesions, however, each case should be considered a law unto itself. There are large aneurysms and small ones; those which are mostly arterial, others mainly venous; some are superficial, others deep, some are in highly important areas of the brain, others in portions largely silent. All of these factors, and finally the patient's wishes in the matter, must be weighed. An aneurysm in the left cerebral hemisphere in a right handed person is surely noli me tangere under all conditions. Any attempted cure, even if successful, would almost surely result in disturbances of speech or motor power, or of both... there is more reason to attempt to cure a patient who has an arteriovenous aneurysm in the right hemisphere." Cushing's experience with operations for cerebral angiomas dated back to 1909. Some brief extracts from his excellent operative accounts follow: Case 1: A 39-year-old patient presented with raised intracranial pressure thought to be due to a cerebral neoplasm and was operated upon on 3.2.1909: "Left subtemporal decompression was made... The dura was not particularly tense. When opened a large thin-walled venous lake was disclosed, from which branches spread in various directions... It seemed unwise to attempt it." Case 2: A 4-year-old child with right sided congenital exophthalmos and bulging in the right temporal area; September 4, 1920: "When the dura was reflected there came into view a mass of hugely dilated vessels, evidently veins, which covered the entire temporal lobe. Two of the main vessels were ligated but extirpation was obviously impossible."
Intracranial Angiomas
Case 3: 30-year-old male, operated on March 18, 1921: "A left osteoplastic exploration was made. When the dura was opened an enormous tangle of dilated veins was disclosed spreading upward from about the region of the arm-center. The larger vessels were fully as big as the little finger. The chief emerging vein was ligated but all attempts to get beneath or between the larger vessels were accompanied by so much bleeding that their ligation or extirpation was deemed impossible." Case 4: "April 25, 1921: . . . On reflecting the dura an exceedingly wet brain was disclosed with two huge veins on the surface, one running largely in the sylvian fissure. The other, more vertical, lay in the precentral fissure... Since the operator felt some regrets at not having been more radical in his attacks upon the lesion in the preceding case, a ligature was first thrown around the large descending vein at the point. . . A second ligature was then put on, which must have started trouble from stasis in the main varix which became hardened and swollen... Finally bleeding began to occur from around the sides of the varix and a rupture seemed imminent. There was evidently only one thing to do - to catch the base of the protruding lesion with a large curved clip and to throw a ligature around the whole mass. This desperate step was taken and the cavity, which continued to bleed after the ligature was placed, was finally filled with a slab of muscle taken from the patient's leg, before the excessive venous hemorrhage could be controlled. There had been a sharp fall in blood pressure from which she finally recovered without transfusion. . . As was to be expected, the patient showed a postoperative right hemiplegia and aphasia... Nearly seven years since her operation, regards herself, aside from some remaining weakness of her right arm, as in normal health." Depressed following such an experience Gushing wrote: "One could hardly have chosen a worse place than over the lower motor area of the leading hemisphere in which to attempt the surgical removal of a racemose varix." The untoward results of the procedure in this case resulted in a more cautious attitude when a similar lesion was disclosed in the next patient (left postcentral region): "December 28, 1922: No attempt was made to treat the lesion by ligature or otherwise." Gushing reviewed the poor results of other workers and warned: "The surgical history of most of the reported cases shows not only the futility of an operative attack upon one of these angiomas, but the extreme risk of serious cortical damage which
10
1. History
is entailed... How many less successful attempts, made by surgeons less familiar with intracranial procedures, have gone unrecorded may be left to the imagination." "The lesions, in short, when accidentally exposed by the surgeon, had better be left alone, and how muchj^adiation may accomplish for them is undetermined though there are favourable experiences on record. So long ago as 1914 Wilhelm Magnus of Oslo unexpectedly exposed at operation a venous angioma of the left rolandic region, a decompression was made with the intention of treating the lesion with radium therapy which at that time was known favourably to influence cutaneous angiomas. After treatment, the decompression, which was bulging, receded, and the epileptiform attacks, from which the patient was suffering, became infrequent and finally disappeared ..." The publication of Reichert (1946) is unique, as he reported 15 cases of premotor vascular anomalies causing Jacksonian epilepsy, which were treated successfully by coagulation of the dural and pial vessels of the lesion (1935 to 1941).
References p. 369
Neurosurgical Treatment of Intracranial AVM Following the Introduction of Angiography (1930) As we have seen, surgical excision of AVMs was carried out between 1889 and 1930, both by general surgeons and neurosurgeons. Some of these cases met with success, others ended disastrously. After one or two bad results most surgeons did not risk further attempts at excision. With the advent of cerebral angiography the position began to change, for it became possible not only to diagnose the AVM but also to obtain some idea as to its location, its size and construction and the number of feeding and draining vessels. Angiography, however, was still somewhat primitive and the contrast material imperfect. Only a few angiographic demonstrations of cerebral AVMs were published before 1936 (Dott 1929, Lohr and Jacobi 1933, Moniz 1934 and 1951, Olivecrona and Tennis 1936). Dott provided the first demonstration of the angiographic aspects of cerebral AVMs at the Neurosurgical Conference in Stockholm in 1935. However, the full benefits of cerebral angiography came only with improved techniques which were not widely available until the 1950s. Olivecrona had a disappointing experience in 1923 when exploring for an infratentorial tumor (case 65). He was confronted with a highly vascular AVM and the patient died. In another case (66), Left carotid angiogram showing a frontoparietal AVM. In the monograph of Egas Moniz, "L'Angiographie Cerebrale", Masson, Paris 1934.
Intracranial Angiomas
with right parietal AVM, two surgical attempts remained unsuccessful. In future years Olivecrona (1927) urged caution in attempting surgery for an AVM found unexpectedly at operation. In this respect, his attitude was similar to that of Gushing and Dandy. On May 5, 1932 Olivecrona carried out his first successful radical removal of a left cerebellar AVM on a 37-year-old male. The preoperative diagnosis was tumor or tuberculoma. The stormy operation was performed under local anesthesia, took 8 hours and the patient needed a transfusion of 2000 ml. The postoperative course was uneventful and the patient left the hospital 3 months later. In the next case (a 52-year-old female with right temporal AVM) diagnosis had been made preoperatively and verified on angiography. Olivecrona's 16 cases together with 6 cases operated upon by Tennis and 4 venous angiomas were presented in their classical monograph in 1936 (Bergstrand et al. 1936). Out of 26 cases only 2 dural and 3 parenchyma! AVMs could be extirpated. They were cautions in advising operation saying that "Some polar AVMs and those in silent areas of the right hemisphere have been declared to be extirpable and curable, but in most cases the situation seemed to be unfavourable. A successful removal can be accomplished if all the feeders are eliminated, but this is only possible in a few cases." The authors did not recom-
Diagram of a temporooccipital AVM. Published in "An Introduction to Clinical Anatomy", 1932, London, by Traquair. The angiography was performed by Norman Dott in 1929 with sodium iodide. Also published in the monograph of Egas Moniz, "L'Angiographie Cerebrale", Masson, Paris 1934.
11
mend techniques of cerebral decompression or ligature of the internal carotid artery. Twelve years later Olivecrona published his extensive experience in 64 cases and mentioned also the surgical results of Penfield and Erickson (1941) and Pilcher (1946 a, b) together with the 7 successfully extirpated cases described by Dott in a personal communication Olivecrona and Riives (1948). By 1954 Olivecrona had removed 81 cerebral AVMs with quite exceptional results (Table 1.2). Table 1.2 Olivecrona and Ladenheim (1957)
The overall mortality for the series was 9% (7 cases), but most of these were early cases. In between 1951 and 1956 there was only a single operative death. The opinion that small to moderate sized AVMs in silent areas of the brain should be operated upon while, others in nonsilent areas were better left untouched, found general acceptance among neurosurgeons. Within 25 years (1932-1957) approximately 500 patients with cerebral AVMs had undergone surgery; Olivecrona and Lysholm
12
1. History
1927. Dott 1929, Tonnis 1934, Puusepp 1935, Bergstrand, Olivecrona and Tonnis 1936, Rottgen 1937, Moniz 1938, Seeger 1938, Sorgo 1938, Singleton 1939, Northfield 1940/1941, Krayenbuhl 1941, Penfield and Erickson 1941, Asenjo and Uiberall 1945, Jaeger and Forbes 1946, 1950, Pilcher 1946, Dott 1948, Olivecrona and Riives 1948, Pluvinage 1948, Trupp and Sachs 1948, Norlen 1949, Olivecrona 1949, 1950, Sorgo 1949, McKissock 1950, Pilcher et al. 1950, Sunder-Plass-mann 1950, Basset 1951, Gros and Martin 1951, Kraus 1951, Petit-Dutaillis and Guiot 1951, 1953, Thiebaut et al. 1951, Wechsler et al. 1951, Whitney 1951, Amyot 1953, Arne et al. 1953, Druckemiller and Carpenter 1953, Ebin 1953, Gil-lingham 1953, Krayenbuhl and Ya§argil 1953, Laine and Delandsheer 1953, 1956, Lazorthes and Geraud 1953, McKenzie 1953, Montrieul et al. 1953, Pompeu and Niemeyer 1953, Selverstone and White 1953, Tonnis and Lange-Cosack 1953, Falconer 1954, Logue and Monckton 1954, Martin and Brihaye 1954, Milletti 1954, Pimenta and da Silva 1954, Pluvinage 1954, Scott et al. 1954, Carton and Hickey 1955, Gould et al. 1955, Olsen and Wood 1955, Potter 1955, Hayne et al. 1956, Leppo et al. 1956, Lundberg et al. 1956, Paillas et al. 1956, Paterson and McKissock 1956, Philip-pides et al. 1956, Asenjo et al. 1957, Baker 1957, Hamby 1957, Krayenbuhl and Ya§argil 1957,1958 (90 cases, 26 radical removal), Ley 1957 (23 cases, 9 extirpations), McKissock and Hankinson 1957 (100 cases, 68 operated), Milletti 1957, Niemeyer 1957, Norlen 1957, Olivecrona and Ladenheim 1957 (100 cases, 81 operated), Paterson 1957, Tolosa 1957, Tonnis 1957, Af Bjorkesten 1959, Paillas et al. 1959, Tonnis et al. 1958. The results achieved were remarkable. The mortality for small AVMs was between 0 to 5%, and for moderate sized AVMs was generally between 6 and 10%, although some authors found mortality rates of over 20%. Over 60% of patients returned to a full working capacity after operation and serious morbidity was around 10%. Norlen (1949) was particularly successful in that he was able to remove AVMs totally in 10 patients with no mortality and only a small and temporary morbidity. Norlen's other principal contribution was his statement that "The malformation may cause cerebral circulatory failure. Notice that the arteries of the hemisphere surrounding the AVM, which are hardly seen in the preoperative angio-gram, filled normally with contrast once the AVM has been removed. In most cases the postoperative angiograms show that the enlarged and tortuous proximal feeding vessels returned to a normal diameter usually within 2 or 3 weeks." Follow-
References p. 369
ing on from this concept, Murphy (1954) first described the concept of "^cerebral steal syndrome". The First European Congress of Neurological Surgeons (Brussels 1957) included discussion on experience gained in operating on cerebral AVMs. It was generally accepted that palliative procedures such as decompression, ligation of the carotid artery or partial coagulation and partial removal of the lesion were ineffective and that complete removal should be the aim in all possible cases. There remained uncertainty regarding the operability of small or moderate sized lesions in eloquent areas of the brain and in cases of large AVMs. Nevertheless, the first approaches in this direction were already being made by Laine et al. (1956) and Houdart and Le Besnerais who published their results in 1963.
The Limitations of Surgery Eloquent Areas of the Hemispheres Pluvinage (1954) predicted a tendency towards more radical removal of all AVMs with the size, shape and location of the lesion becoming a secondary problem. Tonnis (Tonnis and Schiefer 1959, Tonnis 1961) carried out careful studies of general and localized blood flow and presented 215 patients with cerebral AVMs in which he had achieved complete removal in 118 cases, with 54 AVMs being in eloquent areas. He felt that total removal of an AVM was certainly possible and was the best form of treatment. Preoperative deficits frequently declined after operation and newly acquired deficits were mostly of a temporary nature. He concluded that 1) The location of an AVM is not a primary reason for inoperability, 2) The preoperative neurological deficits may be reduced after surgery, 3) The mortality in selected cases was 9.5%, 4) Major contraindications to surgery were large voluminous AVMs and elderly patients. Kunicki and Zoltan described their experience at the 1967 Madrid Meeting of the Congress of European Neurological Surgeons: Kunicki had successfully removed 2 AVMs from the motorsensory area and Zoltan described 38 cases of removal of AVMs lying predominantly in the motor cortex or speech areas, in the region of the middle cerebral artery. Of these patients, 4 died postoperatively, and just 2 had mild postoperative neurological disorders. Of 5 patients who had suffered severe hemiplegias following pre-
References p. 369
vious hemorrhage 3 were improved after surgery. These authors felt that the main reasons for their success were that the vessels comprising the anomaly did not contribute in any way to the cerebral circulation and that the parenchyma included within and immediately adjacent to the angioma was functionallyliselessrZoltan (1968) reemphasized this latter point. Further successes in operating upon AVMs in delicate areas of the brain were presented by Petit-Dutaillis et al. (1953), Laine et al. (1956, 1957), Achslogh et al. (1957), Houdart and Le Besnerais (1963), Pertuiset et al. 1963 and Christensen (1967). Deep Seated AVMs Deep seated AVMs lying within the striate, thalamic, parathalamic, limbic, intra- and paraventricular and callosal areas together with most infratentorial AVMs and those within the brain stem had always been generally declared inoperable. However, several surgeons did approach these lesions before microsurgical techniques became available. Olivecrona (1923), David et al. (1934), Alpers and Forster (1945), Boldrey and Miller (1949), Guillaume et al. (1950), Hamby (1952), French and Peyton (1954), Logue and Monckton (1954), McGuire et al. (1954), Carton and Hickey (1955), Strully (1955), Laine et al. (1956, 1957), Leppo et al. (1956), Poppen (1958), Caram et al. (1960), Dereux et al. (1959), Bonnal et al. (1960), Litvak et al. (1960), Pampus et al. (1960), Poppen and Avman (1960), Ralston and Papatheodorou (1960), Odom et al. (1961), Ver-biest (1961), Ciminello and Sachs (1962), Levine et al. (1962), Houdart and le Besnerais (1963), Pertuiset et al. (1963), Castellano et al. (1964), Kunc (1965), Mount (1965), Pool and Potts (1965), Laine and Galibert (1966), Walter and Bischof (1966), Lapras et al. (1968), Milhorat (1970), Montant et al. (1971), Fenyes et al. (1973), Ribaric (1974)________________ t Kunc (1967) declared that: "For arteriovenous' malformations in the basal ganglia and thalamus, ligation of feeding arteries may be the procedure • of choice. This, however, carries the danger of ' producing unintentional infarction owing to the great anatomical variability of the blood vessels at the basal structures of the brain. The same oper-ation can be very successful in one case and produce serious consequences in another. Very good results were achieved with this simple procedure in 2 cases of arteriovenous malformation on the anterior inferior cerebellar artery. To limit the operation to the ligature of supplying arteries is inadequate when the lesion is widespread for the
Intracranial Angiomas
13
arteriovenous shunt will increasingly attract blood from its small tributaries, which very soon become enormously dilated. Radical removal is the only effective method of treatment, if it is feasible." Morello (1967), at the congress in Madrid was of the opinion that "The outlook for patients with angiomas of the basal ganglia is very poor. There are a few accounts of fortunate cases in which the malformation, being small and emerging in the lateral ventricle, could be attacked directly with success, but unfortunately they are often large and cannot be removed." Nevertheless, Schurmann and Brock (1967) stated that "The reservations concerning the surgery of AVMs located in vital brain stem centers remain justified. The operability of such lesions seemed to depend upon site, size and clearcut delineation of the angioma, the number, caliber and source of the afferent vessels also whether their origin be uni- or bilateral, and the age of the patient together with the clinical course and picture of the illness." In 1967 microtechniques (including the operating microscope, bipolar coagulation, microinstruments and suture material) were introduced and the initial experience in 14 cases (including 4 deep seated AVMs) was published in the monograph of Ya§argil (1969). _Splenial and large cerebellar AVMs could be completely removed with good results as presented to the 4th European Congress in Prague 1971. The Symposium in Giessen (1974) was devoted to the problem of cerebral AVMs and the contributions were published by Pia in 1975. The papers showed a tendency toward more active surgery (Lapras 1975), with the introduction of new techniques such as microtechniques (Pia 1975, Bushe et al. 1975), electrothrombosis (Handa et al. 1975), cryosurgery (Walder 1975) and stereotaxy (Riechert 1975). The Sixth International Congress of Neurological Surgery in Sao Paulo (1977) dealt once more with deep seated AVMs of the brain. Kunc gave an excellent survey of the achievement and limitations: "It must be recognized that deep seated AVMs are the cause of greater disability and mortality than those at other sites. Hemorrhages threaten function and vitally important structures." The large series from the Burdenko Institute was presented by Filatov et al. (1978). In 160 cases the AVM was totally removed, in 60 patients endovascular occlusion of the feeding arteries was performed and 56 other patients underwent various palliative procedures. Of 60 deep seated AVMs, 37 were totally removed and in 16 cases balloon
14
1. History
occlusion was performed. There was only one death. Steiner's presentation at this meeting, showing results in 35 patients treated with stereotactically directed gamma rays, was a further milestone in the treatment of AVMs. Lesions up to 3 cm in diameter showed startling resolution after such treatment. Another promising radiation technique, especially for large lesions was presented by Kjellberg et al. (1977) in 33 patients.
Conservative versus Surgical Treatment Cerebral AVMs may now be treated by conventional or loupe surgery, microsurgery, embolization and radiation techniques, either alone, or in combination. With each advance and refinement of these methods, especially together with the improvement of neuroanesthetic techniques, and the increase of our knowledge concerning cerebral hemodynamics, there has followed a greater tendency throughout the world towards intervention in cases of AVM, as soon as the diagnosis has been made. This has lead to a good deal • of uncertainty regarding the natural history of untreated lesions and to a continuation of the uneasy feeling expressed by many authors that in a great many instances the outcome might be more favourable if the patient is left untreated. Until very recently (Crawford et al. 1986) the outcome in untreated cases had usually been described in only a very small number of patients in any given series. Comparison of treated and untreated groups is also made difficult by virtue of possibly selecting out of favourable cases for surgery i.e. patients who might anyway have had a favourable outcome had they been left untreated. Olivecrona and Riives (1948) stated that in the end, probably most, if not all unoperated patients die of hemorrhage or are completely incapacitated. Olivecrona (1957) found that 25% of his untreated patients were to die of further bleeding, one third were to suffer serious morbidity, but that 25% were to remain healthy and almost asymptomatic many years after diagnosis. He stressed that the two groups of operated and non-operated patients could not be compared as they were no doubt selected according to differing points of view. Botterell (1966) pointed out that progressive neurological deterioration may occur even though follow-up arteriography showed no change in the size of an AVM and he contributed this to progressive gliosis of surrounding cerebral tissue.
References p. 369
Paterson and McKissock (1956) stressed that the follow-up of untreated cases in their series did not contribute substantially to the knowledge of what might be termed the natural history of intracranial angiomas, largely because insufficient time had elapsed since their patients had been diagnosed. Yet it was worthy of note that few of them were severely incapacitated even after many years. Although angiomas may, through hemorrhage, lead to death or permanent incapacity, they felt they were much less likely to rupture than intracranial aneurysms/ They felt that Potter (1955) had published figures which lent support to their view; 27% of his patients survived for more than 20 years after the onset of symptoms and more than half of them had only slight disability or none at all. The increasingly aggressive attitude toward the surgical treatment of AVMs raised two controversial and interrelated issues: 1. Many retrospective series, although based on relatively small numbers of patients, seemed to prove that unoperated patients had a better prognosis. 2. The mortality and morbidity rates of operated cases in some series were not low (up to 18%). Svien and McRae (1965) from the Mayo Clinic considered that 85% of patients with angiomas were best treated conservatively. Perret and Nishioka (1966) analyzed 545 cases of AVM in a Cooperative Study and stated that the operative mortality should be less than 10% and the postoperative morbidity should be better than, or comparable to patients treated conservatively, for surgery to be justifiable. They found that the mortality in unoperated cases was 5% and in operated cases was 12%. These authors included palliative surgical treatments such as carotid ligation or partial resection in their surgically treated group. Therefore it is clear that a true comparison between operated and unoperated groups is impossible._____________________._ Г Pool and Potts (1965) collected523_cases from the available literature. They found that the mortality and morbidity of the conservatively treated group was 56%, while that for 187 patients treated by radical excision was only 26%. They suggested that "on the basis of these data, excision of a symptomatic AVM seems advisable whenever surgery can be done with reasonable safety since it offers the best chance of saving a patient from progressive neurological and mental deterioration, epileptic seizures, or death from hemor-rhage. This is because excision improves the circulation to those areas deprived of normal blood
References p. 369
- -Pply by the arteriovenous malformation of nor~dl blood supply and removes the threat of a ser.ous hemorrhage. On the other hand, excision is obviously contraindicated if the patient may become worse after surgery due to his age, condition, or the location and extent of the lesions. Excision of lesions in the occipital lobe or the posterior part of the temporal lobe may, for example, ^ead to permanent homonymous hemianopsia, but :his seems a small price to pay for relief from the threat of progressive brain damage or a fatal •emorrhage./ Under favourable conditions, moreover, an arteriovenous malformation can usually be excised without sacrificing significant amounts of intact tissue, even if this does lie adja;ent to the sensory or motor cortex or involves the dominant temporal lobe." "As a rule children tolerate excision particularly well. Good results can also be expected from excision if the arteriovenous malformation is small and the patient is under 50 years of age and in a good preoperative condition. In patients over 50 years of age the need for excision is less urgent than in younger ones, since progressive enlargement of the arteriovenous malformation is less Likely." They concluded: "In our experience, approximately 75% of patients recover well following excision while some reports indicate even better results." French et al. (1964) considered that "AVMs are not in any sense to be considered new growths, but they may enlarge with time by expansion of jhe vessels and dilatation of aneurysmal sacs". This seemed an important factor to be included in the evaluation of the necessity of surgical excision. On this basis the practice of surgical intervention seemed unquestionably superior to nonsurgical management. However, in 1970, Troupp reported on 137 patients seen between 1942 and 1969 with angiographically verified AVMs. These were not operated upon, except for exploratory craniotomy in 2 cases (Troupp et al. 1969, 1970). At that time, he felt their follow-up figures indicated a more cheerful outcome than that postulated by others, notably Olivecrona and Riives (1948), Pampus et al. (1960) andNorlen (1966). After 7 years Troupp reviewed the same 137 cases and changed his mind somewhat, for only 27 cases were well. Fourteen were described as fair but 28 were disabled and 9 more had died from hemorrhage (total 23). The only factor of interest he could relate concerning the prognosis was the location of the AVM. Of those situated in the frontal, temporal and occipital regions, only 2 patients died from bleeding while 21 of those situated in
Intracranial Angiomas
15
the parietal, central and infratentorial regions ruptured fatally. Drake's observations (1979) concurred with the view that while the initial course of an AVM is reasonably benign, the long-term outcome is less favourable. Waltimo (1973) discussed the increasing size of an AVM in terms of prognosis: In a study of 21 patients with AVM subjected to serial angiograms (with a median time between examinations of 44 months), it was noted that 12 of the lesions increased in size, 8 remained unchanged, and one became smaller. He also found that smaller AVMs were the most likely to increase in size and the largest were the most likely to reduce in size. Hook and Johanson (1958) found that in 12 cases: 8 increased in size, 4 remained unchanged and 1 disappeared and Stein (1984) found in his series that one third increased, one third remained unchanged and one third became smaller. Kelly etal. (1969) followed 33 patients for an average of 15.5 years after their initial hemorrhage from an AVM. There was a mortality rate of 28% and half of the patients had little, if any disability. Fults and Kelly (1984) found that the prognosis for patients presenting with seizures was more favourable than for patients presenting with hemorrhage, and that the mortality associated with recurrent hemorrhage did not increase significantly with successive bleeds. Patients with posterior fossa AVMs fared considerably worse than patients with an AVM located elsewhere in the brain. Pellettieri (1979), however, found that the risk of death in an unoperated group of patients followed over a period at 18 years, to be 2.5 times greater than in an operated group. The prognosis for children with intracranial AVM was not different to that for adults. The size of the AVM did not dictate either the clinical outcome for the patient or the risk of hemorrhage. There seemed to be no correlation between pregnancy (or delivery) and hemorrhage from a cerebral AVM in a female patient. The publication of Pellettieri etal. (1979) was a milestone in the literature on the natural history of the AVM as the authors applied a differential analysis to their cases. By relating the results to 6 or 7 variables (age, sex, AVM-size, AVM-location, symptoms at onset and neurological findings at admission) it was possible to grade each variable with respect to prognostic importance. The most favourable risk factors were age below 40 years, absence of a neurological deficit, a superficial and small AVM in a silent area, female
16
1. History
sex. and SAH at onset. These variables were assigned numerical values, and grouped on a scale ranging from +16 to -16. The AVMs with values of -10 or below were found to have a poor prognosis whether the condition was treated surgically or conservatively. In those ranked -8 or above, surgical treatment was considered to give consistently better results and in the AVMs with risk values between -2 and +2, a significantly better outcome could be expected with surgical or conservative management. Their conclusions probably reflect the opinion of most neurosurgeons: "A favourable combination of variables gives relatively good results with both modes of therapy. Results deteriorate proportionally with falling values on the risk scale in both groups. Although surgery tends to give better results, the difference is only significant within a limited range on the risk scale. This probably explains the controversy between those who advocate surgery and those who prefer conservative treatment." Calica et al. (1984), recently took the idea of risk prediction a step further, using a complicated regression formula involving 14 variables to assess outcome (6). When they applied this formula to their 78 patients with intracerebral AVMs, it divided 85% of them into low (3% became impaired), medium (42% became impaired), and high (94% became impaired) risk groups. Citing the paper of Calica et al., Wilkins (1985) has predicted that it may become possible with additional experience to use computerized paradigms to predict with greater accuracy the outcome of an intracranial AVM without surgery or with any of several possible treatment protocols so that the best approach can be planned. Until then, we must still rely on fragmentary published information about the "natural history" of such lesions and on a realistic assessment of our ever-changing abilities to deal with them surgically. Wilkins felt it had been difficult to assess the natural history of intracranial vascular malformations because they are varied in nature, they are frequently silent clinically, they are often treated when they are discovered and untreated lesions are not often followed in an organized way. We would add to this argument the fact that many published data relate to unsufficiently analyzed cases. We agree also with the remarks of Mohr (1984), "The enormously accumulated studies concerning the natural history of the AVM is retrospective and the rarity of these lesions precludes any definitive prospective study of the natural history. Furthermore, the clinical picture of many of these lesions spans years if not
References p. 369
decades. The remarkable variation of clinical material from center to center has become apparent and with it a hesitancy to offer such experience for publication." Most recently (1986) Crawford et al. reported upon 217 out of a total of 343 patients with cere bral AVMs, who were managed without surgery. He followed them for a mean of 10.4 years and, using life survival analyses, found that there was a 42% risk of hemorrhage, 29% risk of death, 18% risk of epilepsy and 27% risk of neurological defi cit over a 20-year period. This represents the larg est series of untreated cases studied over a long time span. He found, interestingly, that although small AVMs, as described by many authors, are more likely to present with hemorrhage in the first instance (82%) they did not subsequently carry a higher risk of recurrent hemorrhage. The opera tive rate in this series was only 34% with the ten-, dency to leave untreated those AVMs which were large and deep, more posteriorly situated, in the left hemisphere or crossing the midline. However, the authors felt that the size, depth, and possibly the site of the arteriovenous malformations did not significantly affect outcome. The main influencing factors in their opinion were recurrent hemorrhage and increased age at diagnosis. Although the overall mortality at 20 years was 29%, only 65% of the deaths could be attributed directly to the AVM and then most commonly from hemorrhage. The risk of epilepsy is increased with temporal lobejesions. I There are reasons other than those put forward by Mohr which make comparisons between operative and conservative management difficult: a) The inclusion of ligation of extra- or intracra nial vessels, coagulation and partial removal of the lesion and complete removal of the AVM under the term: "operated cases" is incorrect (Paterson and McKissock 1956, Pool and Potts 1965) (Tables 1.3 and 1.4). The retrospective study of the 186 AVM cases of Krayenbuhl (1936-1966) required separa tion of the patients into 3 groups: I Untreated, II Palliative treatment and III Complete remo val of the AVM (Table 1.5). A second analysis 15 years later (1984) clearly proved that the patients with complete removal of the cerebral AVM presented much better late results than the patients in group I-II (Table 1.5).
p. 369
References p. 369
Intracranial Angiomas
17
18
1. History
Twenty-one patients (20%) out of groups I—II had recurrent hemorrhages, whereas group III no case of recurrent hemorrhage occurred. Long-term clinical examinations have shown that only 15% of non-operated cases with large and moderate sized AVMs remain in a good clinical condition. The remainder of the cases develop within the following 10 to 15 years after diagnosis a progressive clinical deterioration characterized either by repeated hemorrhages or a progressive mental and neurological symptomatology ultimately leading to irreversible invalidism or even death. A precise analysis of these cases will be provided in Vol. IIIB. b) Differences in retrospective studies are mainly caused by analyzing collected cases using different criteria applied to unoperated and operated cases. The statistics may give satisfactory information concerning age, sex, symptoms of the patient and size and site of the lesion, but they cannot necessarily provide a guide to treatment, as an "inoperable" lesion for some neurosurgeons, is deemed operable by others. It is remarkable that in some series 30-50% of AVMs are still deemed inoperable. c) Authors with conservative attitudes may argue that the operated cases are "easy" lesions whereas the unoperated patient would be regarded as having more high risk characters (size, site etc.). This argument is only partially correct. Many operated cases are not elective "easy" lesions, but occur as emergency cases because of hemorrhage or progressive neurological and mental deficits. Some patients with "easy" operable lesions refuse surgery as they will not accept any operative risk. Some informed patients prefer to gamble on an early favourable clinical course in order to await further technological advances (Drake 1979). d) Some patients accept surgical risk only after deterioration of their symptoms. Such cases which have been conservatively treated are, however, most often not included in the statistics of unoperated cases, but rather in those of operated cases. Without this recourse to surgery the statistical outlook of unoperated cases might be less favourable. Intracerebral hemorrhage is the most serious complication. Its frequency varies from about 40% to 68% in most series (Pia 1975) with those cases presenting initially with hemorrhage being at greater risk (Crawford et al. 1986). e) As a result of discussion between neurologists, neuropathologists and particularly neurosurgeons, technical developments within the last
References p. 3691
30 years (microsurgery, modern neuroanesthe-l sia, high energy radiation, selective emboli-j zation) have offered new approaches in treat-1 ment. In many publications with large series of operated cases there is no clear separation o f[ statistical data, as to which cases have been operated using conventional surgical technique, pure microsurgical techniques or using combined techniques such as embolization and microsurgery or surgery and radiation. These data are more clearly given in publications of smaller series, especially those concerning the surgery of "deep seated AVMs". f) Other variables have rarely been considered. It is necessary to indicate not just the size of an AVM, in cm2 or cm3, but also its precise construction (single or multiple niduses and compartments, single or multiple AVMs, plexiform, fistulous or diffuse) and its relation to the venous system (Dobbelaere et al. 1979, Vinuela et al. 1985). The precise location should be given not just as frontal, parietal, temporal etc., but as a location within a lobe (polar, dorsal, ventral, lateral, medial, superficial or sulcal etc.). g) Statistics concerning the surgical mortality and morbidity are rarely discussed in detail. Generally, the operative mortality in the collected literature is 11.0% (among this number are large - giant AVMs, deep seated AVMs, patients in condition IV-V, some with large hematomas). The statement that the mortality is 5—6% in good risk cases and 20-30% in poor risk cases is helpful but not sufficient to obtain a proper indication as to individual operability. Useful information has been provided in the series of 81 patients of Haerer (1982) (Tables 1.6 and 1.7).
Table 1.6 Outcome related to treatment: 7-year follow-up of 81 patients (from Haerer, A. F.: in Smith, R.R., A. F. Haerer: Vascular Malformations and Fistulae of the Brain. Raven, New York 1982)
References p. 369 Table 1.7 Outcome related to size of lesion during 7-year follow-up of 81 patients (from Haerer, A. F.: in Smith, R. R., A.F. Haerer: Vascular Malformations and Fistulae of the Brain. Raven, New York 1982)
h) The simultaneous development of three new techniques, microsurgery, embolization and radiation, over the past 20 years has provided, to some extent, healthy competition, yet it has also been exasperating. The success of stereotactic gamma-radiation in the treatment of small to moderate sized AVMs (up to 3 cm in diameter) was and is a factor which reduces just that number of surgically suitable cases for the teaching of young neurosurgeons. In cases of large to giant AVMs, selective embolization and proton beam application are attempts at treatment in otherwise hopeless situations. The results have not as yet been convincing. The information gained from CT, MRI and selec tive angiography concerning size, site, shape, pre cise construction and composition of an AVM, and the studies with Doppler sonography, PET etc. (see Chapter 4: Hemodynamics) still does not allow us to make any prognostic conclusion about the behavior of the AVM with regard to hemor rhage, ischemia, and growth. Statistical studies showing that AVMs are more benign lesions than aneurysms (Crawford et al. 1986) are unsatisfac tory. For a given single patient, nobody can readily predict what is going to happen. The exact risk that these lesions present is far from clear (Symon 1976). It remains a 'perplexing disease' (Fults and Kelly 1984). Over the past 30 years the number of publications on cerebral AVM and the number of operated cases have increased enormously: Anderson and Korbin 1958, Hook and Johanson 1958, Tonnis et al. 1958 (134 cases), Guillaume et al. 1959, Paillas et al. 1959 (70 cases), (80 cases), Poppen 1960, Krenchel 1961 (98 cases), Margolis et al. 1961, Dott and MacCabe 1963, Frugoni and Ruberti 1963 (54 cases), Houdart and Le Besnerais 1963 (44 cases, 3), Sano 1964, Kunc 1965, 1974, 1975, 1977, Pool and Potts 1965 (523 col lected cases), Sharkey 1965, Svien and McRae 1965 (95 cases), Perret and Nishioka 1966 (545 collected cases), Pool 1965, 1968, Schatz and Botterell 1966, Walter and Bischof 1966 (72 cases),
Intracranial Angiomas
19
Henderson and Gomez 1967, Houdart 1967, Carrea and Girado 1968, Castaigne et al. 1968 (53 cases), Kempe 1968, Kunicki 1968, Pertuiset 1968, Verbiest 1968, Weir et al. 1968, French and Chou 1969, Salibi 1969, Vianello 1969, Bartal and Yahel 1970 (43 cases, 37 operated), Maspes and Marini 1970, Milhorat 1970, Muller et al. 1970 (99 cases), Troupp et al. 1970, 1977 (137 cases), Montaut et al. 1971, Perria et al. 1971, Raskind 1971, Amacher et al. 1972 (55 cases), Bushe et al. 1972 (42 cases, 10 operated), Forster et al. 1972 (150 cases between 1930-1960), Green and Vaughan 1972, Krayenbuhl and Ya§argil 1972 (523 cases, 303 operated; 187 extirpated), Pia 1972, Amacher and Shillito 1973, French and Seljeskog 1973, Morello and Borghi 1973 (154 cases, 102 operated), Peserino and Frugoni 1973 (91 cases), Waltimo 1973 (43 cases), Boldrey and Pevehouse 1975, Bushe et al. 1975 (56 cases, 46 operated), Chou et al. 1975, Pia 1975 (124 cases), Sano et al. 1975 (205 cases, 165 operated), Pertuiset et al. 1976, Towfighi et al. 1976, Ya§argil et al. 1976, French 1977, Luessenhop and Gennarelli 1977 (300 cases, 49 operated), Filatov et al. 1978 (588 diagnosed, 276 operated, 160 radical removal, 60 endovascular occlusion, 56 palliative procedures), Juhasz 1978, Kosary et al. 1978 (12 cases), Mingrino 1978 (196 cases, 98 operated), Patterson and Voorhies 1978 (50 cases), So 1978, Vigouroux et al. 1978, Andreussi et al. 1979, Dobbelaere et al. (Laine) 1979 (370 cases), Drake 1979 (166 cases, 140 radically operated), Pellettieri et al. (Norlen) 1979 (166 cases, 119 operated), Pertuiset et al. 1979 (162 cases), Sundt 1979 (38 cerebral cases, It), Wilson et al. 1979 (183 cases, 65 radically operated), Da Pian et al. 1980, Guidetti and Delitala 1980 (145 cases, 95 operated, 92 radically, 50 conservatively), Laine et al. 1980, 1981 (500 cases), Parkinson and Bachers 1980 (100 cases, 90 operated, lOt), Viale et al. 1980, Gerosa et al. 1981. Pertuiset et al. 1981, Aimard 1982 (100 cases), Albert 1982 (178 cases, 140 operated), Debrun et al. 1982 (46 cases, acrylate), Heros 1982. Malis 1982, Martin and Wilson 1982 (116 cases, 16 occl. operated), Patterson 1982, Smith et al. 1982, Suzuki 1982, Graf et al. 1983 (191 cases between 1976-80), Hassler et al. 1983 (35 cases), Ojemann and Crowell 1983, Yonekawa et al. 1983. Black and Farhat 1984, Fujita and Matsumoto 1984, Fults and Kelly 1984 (131 cases, 48 operated between 1979-82), Grisoli et al. 1984, Martin et al. 1984, Rutka and Tucker 1984, Wilson and Stein 1984 (180 cases, 175 radically, 5 subtotally operated, 2t), Adelt et al. 1985 (43 cases), Aoki and Mizutani 1985, Bonnal 1985, Davis and Symon 1985 (129 cases, 69 operated
20
1. History
between 1948-1980, It), Jomin et al. 1985 (128 cases), Salcman et al. 1985, Samson and Batjer 1985. 1985, Waga et al. 1985, Crawford et al. 1986. Drake 1986.
Monographs Comprehensive monographs including history, embryology, anatomy, pathological and clinical considerations, analyses of results in operated and nonoperated patients with intracranial AVMs have been published since 1928 by: Gushing and Bailey 1928, Dandy 1928,
References p. 369
Bergstrand, Olivecrona and Tonnis 1936 (in German), Asenjo and Uiberall 1945 (in Spanish), Olivecrona and Ladenheim 1957 (in English), Ley 1957 (in Spanish), Pool and Potts 1965, Lange-Cosack two separate chapters in Olivecrona and Tonnis: Handbook of Neurosurgery, Vol. IV, 1966, Norlen in Olivecrona and Tonnis: Handbook of Neurosurgery, Vol. IV, 1966, Smith, Haerer and Russel 1982, Ojemann and Crowell 1983, Wilson and Stein 1984, Fein and Flamm 1985.
Summary and Outlook Five aspects of vascular malformations have always been, and still remain, controversial: 1) Pathogenesis, 2) Nomenclature, 3) Classification, 4) Diagnosis, 5) Treatment. The first 3 aspects are discussed on pages 49-61.
Diagnosis A vast increase in the number of angiographic studies performed from 1928 onwards, has given rise to the impression that AVMsbf all types have become more frequent in their presentation to the clinician. Once any of these lesions have become symptomatic it is generally felt that it has become a more dangerous lesion to that patient. Whether this is true for all types of vascular malformation is uncertain. There is even an argument as to the frequency of occurrence of the various types of anomaly. Earlier, it was generally considered that venous and cavernous malformations were rare, but McCormick (1985) in his large pathological series found that the opposite was true and that venous malformations were 10 times more common than the arterial or arteriovenous forms. The next most frequent form of malformation was the cavernoma. Improved angiographic techniques (Constans et al. 1968, Wendling et al. 1976, Preissig et al. 1976) and the routine use of CT scanning and radionucleide scanning (Partain et al. 1979, Fierstien et al. 1979) demonstrated the increasingly frequent occurrence of venous malformations. The incidence of cavernous malformations
has also apparently increased enormously since the intruduction of the MRI scan. Huang et al. (1984) have further revived the 200 year old dispute regarding nomenclature.
Surgery In terms of surgical treatment: a) Decompression (Ray 1941 and others), and extra- or intracranial ligature of carotid arteries are now techniques of the past. Potter's criticism is valid: "The ligature invited arterial blood from somewhere on the 'easy term' of low resistance at the expense of normal brain." b) Radical excision is the surgical goal whenever possible, but must minimize damage to the normal parenchyma and function of the brain. Hypotension, temporary occlusion of involved vessels (Gillingham 1953), identification of afferent and efferent vessels with fluorescein angiography (Feindel et al. 1965), intracranial, intraoperative flow measurement (Nornes and Grip 1980), multiple stage operations (Pertui-set and Sichez 1978) and interdisciplinary attack (embolization by neuroradiologist and removal by neurosurgeon, Stein and Wolpert 1980) are recently available useful technical adjuncts. Stereotactic approaches (Guiot et al. 1960, Riechert and Mundinger 1964, Wijnalda and Bosch 1975, Kandel and Peresedov 1977), electrothrombosis (Handa et al. 1977), and cryosurgery (Walder et al. 1970) have not found widespread acceptance. Techniques of hypothermia, circulatory arrest and circulatory bypass and the use of steroids (Edgerton 1983, Nagamine et al. 1983) have all been employed
references p. 369
with some success. Yet other techniques such as gamma radiation (Steiner et al. 1972), proton beam therapy (Kjellberg 1978) and selective embolization (Brooks 1930, Luessen-hop and Spence 1960, Sano et al. 1965, Djind-jian 1970, Doppman et al. 1971, Serbinenko 1974. Hilal et al. 1974, Wolpert and Stein 1975, Debrun et al. 1975, Russell and Berenstein 1981. Merland et al. 1983, and others) have great potential.
Surgery
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23
2
Embryology Miguel Marin-Padilla
A. Embryogenesis of the Early Vascularization of the Central Nervous System Introduction Тhе Vascularization of the central nervous system (CNS) is a complex process, best described as an integrative vascular metamorphosis continuously adapting to its developmental modifications, Embryonic development of the CNS itself is also complex. It consists of the progressive transformation of a tubular structure (neural tube) into several regions, each with a different and specific structural organization. The Vascularization of each of these regions is an integrated process which adapts to its particular growing structural and functional needs. While these regional vascular differences are clinically and surgically relevant. there are common features in the early vascularization of the CNS shared by all its regions. In the present chapter, common developmental features that characterize the general vascularization of the CNS, rather than regional differences, will be emphasized. The available information concerning anatomic, histologic, pathologic, radiographic, clinical and surgical aspects of the formed CNS vasculature is enormous and can be readily obtained from a variety of books, monographs and review articles Kaplan and Ford 1966, Taveras and Wood 1964, Van den Bergh 1967, Van den Bergh and Vander Eecken 1968, Stephens and Stilwell 1969, Kety 1972, Newton and Potts 1974, Peters et al. 1976, Kautzky et al. 1982, Dudley 1982, McCormick 1983, Ya§argil 1984). Although, information is also available concerning the embryonic development of the CNS vasculature (Mall 1904, Streeter 1918, Padget 1948, 1957, Moffat 1962, Klosovskii 1963, Pessacq and Reissenweber 1972, Hamilton et al. 1972, Bar and Wolff 1972, Gamble 1975, Hauw et al. 1975, Wolff et al. 1975, Pape and Wig-
glesworth 1979) some early aspects of it remain poorly understood. The actual perforation of the CNS surface by embryonic vessels as well as the sequential establishment of its vascular territories needs further investigation. Information is also needed concerning the interrelationships between the development of the CNS vascular territories and that of the meningeal, the Virchow-Robin and the intra-neural glial tissue compartments. Early in embryonic development the neural tube, as a specialized epithelial (neuroectoderm) tissue, lacks an inherent vasculature (Sabin 1917, Streeter 1918, Strong 1961, Hamilton et al. 1972, Marin-Padilla 1985b). Therefore, it should be possible to study the early embryonic Vascularization of any of its regions. The Vascularization of the neural tube follows a caudal-cephalad gradient which is synchronous with that of its ascending differentiation and maturation. In any given region of the developing CNS, embryonic vessels must first surround and organize around (outside of) it; secondly, they must perforate the CNS external basal lamina and marginal glia, which constitute an anatomic barrier; and, thirdly, they must grow within the developing neural tissue while adapting to its growing structural and functional needs. Thus, three different vascular territories must progressively emerge in the early Vascularization of every region of the developing CNS. They are the perineural, the interneural and the intramural vascular territories, respectively. The term "neural" used to describe these three vascular territories encompasses "nervous (neural) tissue". In other words, vascular territories which embryologically evolve outside (peri), in between (inter) and inside (intra) nervous tissue, respectively.
24
2. Embryology
Each vascular territory, though interrelated, evolves sequentially, independently, and within a different and specific tissue compartment. Each territory gives rise to different types of vessels. The main arterial and venous systems of the CNS, which are components of the perineural vascular territory, evolve embedded within the meningeal compartments. Most of the perforating arterioles and venules of the CNS vasculature, which are components of the interneural vascular territory, evolve within the Virchow-Robin compartment (VRC) and hence are outside, "in between" the nervous tissue proper. Thus, the term interneural is introduced to characterize this territory of the CNS vasculature. Finally, the capillaries, apparently the only vessels that penetrate the nervous tissue proper, constitute the intraneural territory of the CNS vasculature. Intraneural capillaries also evolve embedded within a specialized compartment represented by the perivascular glia. The early embryonic development and sequential establishment of each of these three vascular territories will be analyzed in association with the development of the meningeal, the VirchowRobin, and the intraneural perivascular glia compartments, respectively. Since a study of the early vasculogenesis of every region of the CNS would be too complex and beyond the scope of this text, only that of the embryonic cerebral cortex will be considered in detail (see also: Marin-Padilla 1970, 1971, 1978, 1982, 1983). Nevertheless, it should be emphasized that the observations presented and discussed should be fundamentally applicable to the early vascularization of all regions of the CNS.
Perineural Vascular Territory of the CNS Vasculature Vasculogenesis starts in situ from consolidated angioblastic cell islands found throughout the mesoderm, the yolk sac and the body stalk of the young embryo. The cellular elements of these islands seem to undergo progressive cytoplasmic liquefaction (Sabin 1917, 1920) which results in their eventual canalization. However, the process of canalization of these islands as well as that of growing capillaries remains poorly understood and controversial (Manasek 1971). Progressive canalization of the angioblastic islands results in the formation of a precirculatory plexus of primordial vessels which are large, irregular and composed of several endothelial cells joined by tight junctions. They are surrounded by a thin and
References p. 379
often incomplete basal lamina, and grow actively by sprouting. Zones of vascular growth are deprived of basal lamina and their leading endothelial cell or cells produce numerous long filopodia able to advance into the surrounding tissue (see Figs 2.11, 2.12). Blood cells are also believed to evolve from the original angioblasts (Streeter 1918, Sabin 1920) and they are identified very early in the lumen of embryonic vessels. The precirculatory vascular plexuses eventually establish communication through the arterial and venous systems with the heart and blood starts to circulate throughout the embryo. Among the earliest and most prominent vascular plexuses recognized in the developing embryo is the head plexus. It is formed around the cephalic region of the CNS. By the 4th week of human embryonic development the head plexus is already a prominent vascular organization (Streeter 1918, Padget 1948, 1957, Hamilton et al. 1972). By the 6th week of age, some of the main arteries, veins and venous sinuses, which characterize the adult brain, are already recognizable (Fig 2.1). The vascularization of the developing CNS begins at the myelencephalon and ascends progressively through the metencephalon, mesencephalon, diencephalon, striatum and telencephalon (cerebral cortex) which is the last region to be vascula-rized (Streeter 1918, Bar and Wolff 1972, Marin-Padilla 1985b). Therefore, it follows an ascending sequential gradient which keep pace with the CNS ascending differentiation and maturation. By the 7th gestational week of human development early vascularization of the medulla (Fig 2.2A), the pons (Fig 2.2B), the diencephalon, and the striatum (Fig 2.2C) is already underway. However, the cerebral cortex (Fig 2.2D) still lacks its intrinsic vasculature. The human cerebral cortex does not start to vascularize until around the 8th week of embryonic age. Its vascularization follows a ventro-lateral-medial sequential gradient which is synchronous with its advancing differentiation and maturation. The cephalic region of the developing CNS is surrounded by the embryonic meninges. They constitute a prominent and quite large tissue compartment (Fig 2.2). The embryonic meninges are well vascularized before the vascularization of the CNS begins (Figs 2.2, 2.3). Three distinct primordial lamellae: the dura, the arachnoid and the pia mater are recognizable (Fig 2.3). However, there are no distinct separations or tissue spaces between them. The blood vessels of the embryonic meninges can also be separated into three distinct strata (Figs 2.2, 2.3). The outer stratum (Fig 2.3) carries the dural vessels from which the ve-
г^егепсез р. 379
Perineural Vascular Territory
25
sagiftaiis
j 2.1 Reconstruction of the cephalic vascular plexus of a 21 mm human embryo of about 50 days illustrating the organization and distribution of its embryonic vessels. Many of the main arteries, veins and venous sinuses which char-acterize the adult brain can already be recognized. All vessels illustrated are components of the perineural vascular terri-tory of the CNS vasculature. However, the pial vascular plexus is not illustrated. A portion of the cerebral cortex has been removed to demonstrate the vascularization of its choroid plexus, the anterior cerebral artery and the sinus rectus. The thin embryonic cerebral cortex still has no intrinsic vasculature at this age. (From Streeter, G. L: Contr. Embryol. Car-neg Instn8:5, 1918.)
nous sinuses of the CNS evolve. The intermediate | stratum, which is the largest, carries the arachnoi-dal vessels from which the main arterial and venous systems of the CNS evolve. The inner stratum carries the pial vessels from which the pial vascular plexus evolves. The embryonic pial plexus covers the entire surface of the developing CNS, and adapts intimately to its variable external morphology (Figs 2.2, 2.3). Its formation always precedes the intrinsic vascularization of any of the CNS regions (Fig 2.2). All perforating vessels which enter into the various regions of the developing CNS originate from their overlying pial vascular plexus. All meningeal vessels, including the dural, the arachnoidal and the pial vessels, constitute together the perineural vascular territory of the CNS vasculature.
The subsequent development of the head vascular plexus (Fig 2.1) is complex because it actually comprises the concomitant formation of three different but interrelated vascular systems, dural, arachnoidal and pial — strata. The sequential embryonic development of the main arteries, veins and venous sinuses of the perineural vascular territory of the brain has been studied in great detail by several investigators (Streeter 1918, Padget 1948, 1957, Bar and Wolff 1972, Wolff et al. 1975). These studies represent the most complete account of the vasculogenesis of any region of the developing CNS. Figs 2.4 and 2.5 are reproduced from the original works of Padget (1948, 1957). In these diagrams the complete prenatal development of each of the main vessels of the brain can be analyzed and fol-
26
2. Embryology
References p. 379
Fig 2.2 Composite figure illustrating a parasagittal section ( 1 ) of the head of a 50 day human embryo, and a coronal section (2) of the anlage of the cortical choroid plexuses from a younger, 43 day old, human embryo. The parasagittal section illustrates the major regions of the developing brain, the abundant and well vascularized arachnoidal tissue (a), and the pial vascular plexus (p). The lateral (LV), third (III), and fourth (IV) ventricles; and, aqueduct of Sylvius (S) identify the embryonic cerebral cortex, the diencephalon, the cerebellar primordium and the mesencephalon, respectively. The intrinsic vascularization of the medulla (A), the pons (B) and the striatum (C) is already underway while that of the cerebral cortex (D) has not yet started. The abundant arachnoidal tissue (a) and the pial vascular plexus (p) are also illustrated in these four CNS regions. The coronal section illustrates the dural (d), the arachnoidal (a) and the pial (p) vessels around the still unvascularized embryonic cerebral cortex (cc). The cortical pial vascular plexus (p) extends into the anlage of the choroid plexuses (cp) establishing its tela choroidea from which its vascularization will evolve. (From Hamby, W. В.: J. Neurosurg. 1 5 : 65-75, 1958.) H&E preparations, parasagittal section, x20.
r References p. 379
Perineural Vascular Territory
27
Fig 2.3 Camera lucida drawings of the embryonic meninges covering the cerebral cortex of a 50 day human embryo, illustrating its composition and structural organization. Three primordial lamellae are recognized in it. The outer or dural lamella (D) is composed of closely arranged elongated cells which congregate below the developing membranous neurocranium. The intermediate or arachnoidal lamella (A) is composed of loosely arranged stellate cells with long fine cytoplasmic processes with apparently empty spaces between them. The inner or pial lamella (P) has fewer cells and more vessels than the other two and is in contact with the surface of the cerebral cortex. The surface of the cerebral cortex is composed of the closely apposed endfeet (G) of the marginal glia covered by the CMS external basal lamina. Some meningeal vessels have attachments of non-endothelial cells (arrows), which might represent precursors of pericytes and smooth muscle cells, and have circulating blood cells in their lumina. The thickness of the cortical meninges illustrated is approximately 100 micrometers. (Compare with Fig 2.13.)
lowed in detail. It should be emphasized that the illustrations (Figs 2.4,2.5) only represent the prenatal development of the main arterial and venous systems of the brain. They do not supply information regarding the development of the arachnoidal connecting vessels nor of the pial vascular plexus, which are also important components of the perineural vascular territory of the CNS vasculature. The perineural vasculature undergoes an integra-tive development continuously adapting to the changing external morphology of the growing brain. The extraordinary development of the human cerebral cortex represents perhaps the most significant single factor underlying the
remarkable developmental metamorphosis of the intracranial vasculature (Figs 2.4, 2.5). The cerebral cortex evolves from a small vesicle at the anterior end of the brain (Fig 2.2) to a large structure which comes to occupy practically the entire cranial cavity (Figs 2.4, 2.5). The adaptative metamorphosis of arteries and veins to the expanding cerebral cortex are clearly demonstrated in the accompanying illustrations (Figs 2.4, 2.5). It is quite obvious from these illustrations that in the course of embryonic development the location and distribution of the different blood vessels change continuously. This adaptative vascular metamorphosis is the result of continuous and
28
2. Embryology
References p. 379
Fig 2.4 Series of diagrams illustrating the prenatal developmental metamorphosis of the major arterial systems of the human brain. The illustrations are self explanatory. (From Padget, D. H.: Contr. Embryol. Carneg. Instn 32: 207, 1948.) Fig 2.5 Series of diagrams illustrating the prenatal developmental metamorphosis of the major venous systems and sinuses of the human brain. The illustrations are self explanatory. (From Padget, D. H.: Contr. Embryol. Carneg. Instn 34: 79, 1957.)
References p. 379
Perineural Vascular Territory
29
30
2. Embryology
concomitant capillary angiogenesis and capillary reabsorption. The original anastomotic plexus formed by the perineural vessels undergoes continuous remodelling by the addition of new links (angiogenesis) around growing or expanding regions and by the elimination of others (reabsorption) when no longer needed. Undoubtedly, the loose structural organization of the embryonic arachnoidal mesh and its abundance (Figs 2.2, 2.3) provide an ideal tissue substratum for these vascular adaptations. In spite of their obvious significance, the dual embryonic processes of capillary angiogenesis and reabsorption have been little studied and remain poorly understood. However, these processes have been studied in more detail in neovascularization using a variety of experimental models including tumor angiogenesis (Folkman 1976, 1982, Cotran 1982, Hunter and Gabbiani 1982, Glaser and Patz 1983, Sholley et al. 1984). In the course of embryonic development, the arachnoidal mesh is traversed by numerous vessels of various calibers linking the main arteries and veins with the pial vascular plexus (Figs 2.2, 2.3). The size, number, location and distribution of the connecting arachnoidal vessels also undergo continuous developmental modifications and rearrangements by both capillary angiogenesis and reabsorption. Early in development, these vessels are large, irregular, thin walled, and composed of several endothelial cells joined by tight junctions (Fig 2.3). There are no recognizable arteries or veins and all of them appear to be growing actively by sprouting. Later in development, the arachnoidal arteries and veins become surrounded by arachnoidal cells which isolate them from the Table 2.1
Composition and development of the meninges
References p. 379
cerebrospinal fluid (CSF) compartment. The adult arachnoidal vessels thus become enclosed within distinct perivascular tissue spaces which seem to be analogous and continuous with those of other vessels of the body (see Fig 2.13). Furthermore, according to recent observations (Casley-Smith et al. 1976, Krisch and Buchheim 1984, Pile-Spellman et al. 1984) the perivascular spaces of the adult arachnoidal vessels seem to drain independently through the lymphatic system. The simple structural organization of the embryonic meninges is also progressively transformed to accommodate the vascular modifications (Table 2.1, see Fig 2.13). The three original lamellae of the embryonic meninges become eventually duplicated and distinct tissue spaces are formed between them (Table 2.1). The progressive establishment of different meningeal tissue spaces and their association to its vessels are indicative of the acquisition of important functional roles, some of which are not yet clearly understood. The possible functional roles of these meningeal spaces, their relationships to the perivascular spaces, to the cerebrospinal fluid (CSF) compartments, and to the CSF circulation have recently received the attention of several investigators (Andres 1967a,b, Morse and Low 1972, Nabeshina et al. 1975, Oda and Nakanishi 1984, Krisch et al. 1983, 1984). However, the embryonic timing for the establishment of the various meningeal compartments and their association to the development of the perivascular tissue spaces need to be more accurately determined. Although, the pial vascular plexus is a component of the perineural vascular territory of the CNS vasculature, its embryonic development, composi-
p. 379
-tructural organization, and functional role "e best appreciated in conjunction with the .. . .opment of the interneural vascular territory.
Interneural Vascular Territory of the CMS Vasculature
Interneural Vascular Territory
to the changing external morphology of the CNS surface by capillary angiogenesis and reabsorption. The pial vessels are separated from each other by the cytoplasmic processes of pial cells, by fine collagen fibers, and by tissue spaces (Figs 2.6, 2.7, 2.9). The primitive pial cells are elongated elements lacking distinctive features. They are frequently associated with fine collagen fibers and some contain vacuoles in their cytoplasm (Figs 2.6, 2.7). Embryonic pial cells are specific meningeal elements (Andres 1967a.b. Krisch et al. 1983, 1984). They share features of fibroblasts (collagen formation), of mesodermal cells (phagocytosis), and of epithelial cells (formation of epithelial-like lamellae). Pial vessels have a distinct but thin basal lamina which is lacking in zones of active angiogenesis. The leading endothelial cells of its growing vessels have characteristic features. They show considerable membrane activity with the formation of pseudopodia and fine filopodia which project both inside and outside of their lumina (Figs 2.6, 2.7, 2.9). They are also characterized by a prominent and abundant granular endoplasmic reticulum filled with dense and fine granular material (Figs 2.6, 2.7, 2.9). The accumulation of this dense material often causes dilation of the endoplasmic reticulum. Although, the nature of this dense material remains unknown, its association with the advancing endothelial cells of growing capillaries suggests two possibilities. First, it could represent proteinaceous secretion for the formation of the basal lamina of the newly formed vessel, second, this material could be used in the formation of the first lumina (canalization) between the advancing endothelial cells of a growing vessel (Manasek 1971). Further investigation will be necessary to elucidate the nature of this proteinaceous material and its possible role in embryonic angiogenesis. The surface of the embryonic cerebral cortex is composed of the closely apposed glial endfeet of the marginal glia covered by CNS external basal lamina (Figs 2.6, 2.9). The CNS external basal lamina, together with the marginal glia constitute a distinct anatomical barrier which must be perforated by the pial vessels in order to penetrate the nervous tissue.
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2. Embryology
Vascular Perforation of the CNS Surface by Rial Vessels Recent electron microscopic studies (Marin-Padilla 1985a,b) of the early vascularization of the embryonic cerebral cortex have demonstrated the sequential nature of the vascular perforation of the CNS surface by pial vessels. Three fundamental stages have been demonstrated in this type of vascular perforation. First, the pial vessel approaches and establishes direct contact with the surface of the developing CNS. Then endothelial filopodia from these glia-touching vessels perforate through the vascular and the CNS basal laminae and penetrate into the nervous tissue. The original opening enlarges gradually, thus allowing an entire endothelial cell or cells to penetrate into the nervous tissue. Finally, the proliferation of penetrating endothelial cells results in the formation in situ of new intraneural vessels.
Vascular Approach and Contact with the CNS Surface Embryonic pial vessels are separated from the CNS surface by pial cells, tissue space, collagen fibers and by their corresponding basal laminae (Figs 2.6, 2.7, 2.9). Occasionally, some pial vessels approach and establish direct contact with the surface of the CNS (Figs 2.6, 2.7, 2.9). The endothelium of these glia-touching vessels becomes parallel to the surface of the CNS and their corresponding basal laminae establish direct contacts at some points (Fig 2.6, insert). The only appreciable separation between these vessels and the surface of the CNS is that of their corresponding basal laminae (Fig 2.6, insert). The leading endothelial cells of these glia-touching vessels produce numerous filopodia, which project both inside and outside of vessel lumina (Figs 2.6, 2.7, 2.9). Some of the outside projecting filopodia perforate through the vascular basal lamina and establish direct contact with that of the surface of the CNS (Fig 2.6, insert). This type of vascular contact with the surface of the CNS is considered to be a prerequisite for its subsequent perforation.
Endothelial Filopodia Perforation of CNS Surface The actual perforation of the CNS surface is carried out by the endothelial filopodia of glia-touching pial vessels (Figs 2.7, 2.9). This type of filopodial perforation occurs through areas in which the vascular and the CNS basal laminae are in contact (Fig 2.7). The perforating endothelial filopodia seem to be able to disintegrate (digest) both
References p. 380
basal laminae and to pass through them into the nervous tissue (Fig 2.7). The filopodia enter the CNS tissue usually between adjacent glial endfeet (Figs 2.7, 2.9). The penetrating filopodia advance freely into the nervous substance and are deprived of recognizable basal lamina. This type of perforation can be carried out by several filopodia arriving from the leading endothelial cell or cells of the glia-touching capillary. The glial endfeet between the perforating filopodia often undergo swelling, vacuolization and their membrane disintegrate with the formation of myelin figures (Marin-Padilla 1985b). The endothelial filopodia of growing embryonic capillaries are able to perforate through anatomical barrier and to cause focal disintegration of the membrane of the glial endfeet of the CNS surface. Although the nature of this active process remains unknown, proteolytic enzymes, possibly produced by the endothelial filopodia, could participate in it (Ausprunk 1979). Although filopodia have been described in the leading endothelium of growing capillaries in the CNS (Klosovskii 1963, Bar and Wolff 1972, Wolff et al. 1975, Press 1977) and in a variety of experimental situations (Schoefl 1963, Ausprunk and Folkman 1977, Ausprunk 1979, Madri et al. 1983, Sholley et al. 1984) their possible significance and functional role in angiogenesis have been inadequately investigated. At the site of the perforation the vascular and the CNS basal laminae fuse together around the perforating filopodia (Figs 2.7, 2.9). Their fusion creates a central opening through which the leading filopodia and subsequently the entire endothelial cell or cells are able to penetrate into the nervous tissue. The fusion of both basal laminae thus establishes anatomical continuity between the vessel wall and the surface of the CNS. The fusion of both basal laminae also establishes a shallow "pial-funnel" around the perforating vessels (Figs 2.7-2.9). This embryonic pial-funnel will play a significant role in the establishment of the VRC (Figs 2.8, 2.9).
Fig 2.6 Ultrastructural composition and organization of the pial vascular plexus and upper region of the cerebral cortex of a 12 day old hamster embryo. The pial vessels (*) are of differing calibers and are composed of several endothelial cells joined by tight junctions (arrows). The pial vessels are separated from each other and from the cortical surface by pial cells (F), intercellular spaces and fine collagen fibers. The marginal glia (G) covered by the CMS external basal lamina represents an anatomical barrier which must be perforated by the pial vessels. The pial vessel illustrated near the center of the figure approaches the cortical surface and its leading endothelial cells (1 and 2) have filopodia which project inside and outside its lumen. Some of these filopodia
have established contact with the cortical surface. The endothelium of these glial-touching pial vessels becomes parallel to the cortical surface (insert) and the vascular and CMS basal laminae establish contacts at some points. Some filopodia from this gliatouching pial vessel (insert arrows) have perforated through the vascular basal lamina and have established direct contact with that of the cortical surface. This type of contact between the vascular and the CMS external basal laminae is considered to be a prerequisite for the subsequent perforation of its surface by the pial vessels. Few primitive neurons (N) are recognized in layer I. (From Marin-Padilla, M.: J. сотр. Neu-rol. 241: 237-249, 1985), x5500.
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2. Embryology
References p. 380
Fig 2.7 Detail of the perforation of the cortical surface by the leading filopodium (arrow head) of a glia-touching pial vessel (*). The filopodium has perforated the cortical surface between two adjacent glia endfeet (G). The vascular and the CMS external basal laminae fuse around the perforating filopodium creating an opening through which whole endothe-lial cells eventually penetrate into the nervous tissue. The endothelial cell (E) of the upper pial vessel shows the prominent granular endoplasmic reticulum filled with dense material which characterize those of growing capillaries. Also illustrated are the processes of pial cells (F) and the tight junctions (arrows) of the pial vessels. (From Marin-Padilla, M.: J. сотр. Neural. 241: 237-249, 1985), x7000.
Interneural Vascular Territory Fig. 2.8 Detail of the ultrastructure of the newly formed intracortical capillary depicted in the left lower corner insert. Proliferation of penetrating endothelial cells (insert) results in the in situ formation of new intracortical vessels. At the entrance of the vessel a shallow pial-funnel (arrows) is formed between the fused vascular and CNS external basal laminae. This pial-funnel will elongate accompanying the newly formed intracortical capillary into the nervous tissue. It represents an embryonic Virchow-Robin compartment (VRC) and contains cytoplas-mic processes of pial cells, fine collagen fibers and intercellular tissue spaces around the perforating vessel. The embryonic VRC and its vessels become separated from the nervous tissue by new glial processes (G) which become continuous with those of the marginal glia of the cortical surface. This newly formed glial wall is covered by new basal lamina material which becomes continuous with that of the CNS surface. (From Marin-Padilla, M.: J. сотр. Neurol. 241: 237-249, 1985), хЮООО.
35
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2. Embryology
References p. 380
Fig 2.9 Schematic drawings illustrating the three fundamental stages of the vascular perforation of the surface of the embryonic cerebral cortex (G) by pial vessels (P). The following stages (from left to right) are illustrated: a) the early endothelial filopodia perforations; b) the endothelial cell perforation and proliferation with the in situ formation of a new intracortical vessel; and c) the establishment of the Virchow-Robin compartment (VRC). The fusion of the vascular and CMS external basal laminae around the perforating vessel and its participation in the formation of both the pial-funnel and the embryonic Virchow-Robin are also illustrated. The composition and organization of the embryonic VRC viewed in longitudinal and transverse (thick arrow) perspectives are also illustrated. The embryonic VRC represents a perivas-cular tissue space (ICS) formed between the vascular and the CNS basal laminae (BL). It contains the perforating vessel (E) with paravascular cells (P) enclosed within its basal lamina (curved arrows), the cytoplasmic processes of pial cells, and fine collagen fibers. The vessels within the VRCs constitute the interneural vascular territory of the CNS vasculature. At various depths into the nervous tissue the VRC closes off with the fusion of the vascular and the CNS basal laminae into a single layer which surrounds and accompanies the penetrating vessels into the CNS substance. Only capillaries arriving from the vessels of the VRC actually penetrate into the nervous tissue proper. They grow actively establishing short-link anastomotic plexuses throughout the nervous tissue. They constitute the intraneural vascular territory of the CNS vasculature. The three insert drawings (А, В, С) illustrate the type of progressive vascularization observed in the developing cerebral cortex. New pial vessels perforate the cortex between previous perforation sites, thus progressively vascularizing the expanding cerebral cortex. The ependymal cell layer (E) with its multiple mitoses is also illustrated. The composition and structural organization of both the embryonic and the adult VRC (compare with Fig 2.10) are essentially indentical.
References p. 380_______________
in Situ Formation of New Intraneural Vessels
outside of and "in between" the nervous tissue proper, and hence, within the embryonic VRC. However, the leading endothelial cells of perforating vessels continue to advance freely, without recognizable basal lamina, into the developing nervous tissue (Fig 2.9). Different stages of vascular perforations are recognized during early development in all regions of the CNS. In the cerebral cortex, new vascular perforations occur during its entire prenatal development. As the cortex expands, new perforations occur between previous ones, following a sequence which is schematically illustrated in Fig 2.9 (A,B,C, inserts). The formation of the embryonic pial-funnel and its role in the establishment of the embryonic VRC are also illustrated (Fig 2.9). Finally, it is important to emphasize that pial vessels always perforate the external basal lamina and marginal glia of the CNS surface to enter the nervous tissue, but do not perforate them to exit. Therefore, it would seem that in the course of embryonic development the direction of the blood flow eventually determines which vessels will be transformed into entering arterioles, and which into existing venules.
Interneural Vascular Territory
37
Establishment of the VRC and Interneural Vascular Territory The early pial-funnel established around the entrance of the perforating vessel, by the fusion of both basal laminae, undergoes significant modifications in the course of embryonic development (Figs 2.8, 2.9). Between the two fused basal laminae a shallow space is formed which communicates with the tissue spaces of the pia mater. This space elongates downward and accompanies the perforating vessel, for a short distance, into the nervous tissue. It is subsequently invaded by pial cellular elements, fine collagen fibers, and nonendothelial paravascular cellular elements (Figs 2.8, 2.9, arrows). Thus, the original pial-funnel is progressively transformed into a distinct perivascular compartment known as the VRC (Figs 2.8, 2.9). The embryonic VRC becomes progressively walled by new glial processes which are arranged in a manner structurally similar to that of the marginal glia of the CNS surface. Therefore, its vessels remain outside of "in between" the nervous tissue proper (Fig 2.9). The embryonic composition and structural organization of the VRC does not significantly change in the course of embryonic development (Fig 2.10). Both, the embryonic and the adult VRC (Jones 1970) have similar composition and overall organization (compare Figs 2.8 and 2.10). However, the early communication of the embryonic VCR with the pial space is eventually obliterated, as recently pointed out by some investigators (Krisch et al. 1983). As the VRC becomes disconnected from the pial space it is transformed into a specific perivascular compartment entirely outside of the nervous tissue proper. The VRC (Figs 2.9, 2.10) is established between the vessel wall and the glial wall of the nervous tissue. Its embryonic vessels are transformed into arterioles and venules which can reach to considerable depths within the nervous tissue, without penetrating the neural parenchyma (Duvernoy et al. 1981). Although the VRC of the cerebral cortex could reach down as far as the white matter, its vessels remain outside and walled between the nervous tissue (Jones 1970). Therefore, the VRC vessels constitute an important and specific vascular territory of the CNS vasculature. This interneural vascular territory must be distinguished from the perineural and the intraneural territories. The perivascular spaces around the VRC vessels are anatomically independent from the meningeal compartments and from the perivascular glia compartment of the perineural and intraneural vascular territories, respectively. The
38
2. Embryology
References p. 3801 Fig 2.10 Ultrastructural composition and organization of a fully developed Virchow-Robin compartment from the cerebral cortex of an adult cat. Its perivascular tissue space (PS) is clearly visible between the vascular and the CNS basal laminae (BM). This space contains the cytoplasmic processes of leptomeningeal (pial) cells (arrows), collagen fibers and the perforating vessels with perivascular pericytes and/or smooth muscle cells (S) enclosed within their basal laminae. Therefore, the basic composition and structural organization of the Virchow-Robin compartment remain practically unchanged in the course of embryonic development (compare with Fig 2.9). (From Jones, E. G.: J. Anat. [Lond.] 106: 507, 1970), X17000: insert) x2500.
drainage of the VRC is also independent from the meningeal compartments. It seems to be connected with the perivascular tissue spaces of the arachnoidal vasculature, and hence with the lymphatic system (Krisch and Buchheim 1984, PileSpellman et al. 1984). The early development of these anatomical differences undoubtedly results in the acquisition of different and specific functional roles for each of three vascular territories which characterizes the CNS vasculature. The establishment (embryonic timing) and the nature of these different functional roles have not been adequately studied. In the course of embryonic development, as the original pial perforating vessels enlarge they become more directly connected with the arachnoidal vasculature. Some adult perforating vessels lose their original relationship with the pial vascular plexus, thus crossing directly from arachnoid
into the CNS (Fig 2.13). Small perforating arteries and veins as well as arterioles and venules are primarily subjected to these developmental modifications (Figs 2.13, 2.14). As the cerebral cortex increases in thickness, the VRC and its vessels elongate vertically, thus maintaining a perpendicular orientation to its surface (Figs 2.9, 2.13, 2.14). The universal perpendicular orientation of the VRC and its vessels to the surface of the cerebral cortex, as well as their considerable depth, can be best appreciated by vascular injections studies (Fig 2.14) such as those described by Pape and Wigglesworth (1979).
p. 380
Intraneural Vascular Territory
39
This classic method deposits fine silver chromate granules within the membranes of various neural elements, including capillaries, rendering them visible against a transparent background (Figs 2.11, 2.12). Intraneural capillary angiogenesis is extraordinary during the early stages of development of the CNS. Growing endothelial cells produce many long and fine filopodia which advance freely without basal lamina among the neural elements (Fig 2.11). These fine filopodia emanate radially from the original endothelial cell and grow for a considerable distance. Their length ranges between 20 to 40 um and their diameter between 0.3 to 0.6 ^m (Figs 2.11, 2.12). Their vessel at the CNS surface (Fig 2.9). The newly size, length, multidirectional growth, and structural penetrating vessels grow actively establishing short- variability can be clearly appreciated in Golgi link anastomotic plexuses throughout the stained preparations (Figs 2.11, 2.12). The fine substance of the developing CNS (Figs 2.11, 2.12, filopodia of growing capillaries seem to search for 2.14). They give rise to the extensive intraneural developmental clues (angiogenetic factors) which capillary bed which characterizes the nervous tissue will determine the directional growth of the parent (Figs 2.12, 2.14). Together they constitute the vessel (Marin-Padilla 1985b). They are also caintraneural vascular territory of the CNS vascula- pable of perforating through anatomical barriers (CNS surface), and of establishing contacts among ture. Although the newly formed intraneural capillaries them during the formation of anastomotic plexgrow freely at first among the nervous elements, uses (Figs 2.11, 2.12, 2.14). Intraneural capillaries they too eventually become surrounded by peri- form short-link anastomotic plexuses throughout vascular glial processes. Intraneural capillaries are the developing CNS (Fig 2.12). It should be surrounded by a single basal lamina (formed by emphasized, that although intraneural capillary the re-fused vascular and the CNS basal laminae) angiogenesis seems to be a random phenomenon, and by a ring of perivascular glia, separating them the formation and location of their anastomotic from other neural elements. The intraneural peri- plexuses is specific, and always associated with vascular glia constitutes also a specific tissue com- actively growing regions of the CNS (Streeter partment which is anatomically independent from 1918, Bar and Wolff 1972, Marin-Padilla 1985b). that of the VRC. Therefore, the circulating blood In the cerebral cortex, the first recognizable through the intraneural capillaries remains sep- anastomotic plexus is the one formed throughout arated from the neuronal elements by a vascular- the paraventricular matrix zone, the first region of the developing CNS to begin differentiation. glial (blood-brain) barrier. As the VRC gradually elongates vertically, its ves- Anastomotic plexuses are subsequently formed in sels continues to give-off new capillaries which Layers I and VII following the formation of the penetrate the CNS substance at different levels cortical plate (Marin-Padilla 1971, 1978). These (Fig 2.14). The number of penetrating capillaries early anastomotic plexuses undergo continuous arriving from the VRC increases in the course of modification and remodelling by both capillary cortical development. These penetrating capillaries angiogenesis and reabsorption. The progressive establish short-link anastomotic plexuses between remodelling of the intraneural plexuses again contiguous VRCs (Fig 2.14). These anastomotic represents an integrative vascular process plexuses also undergo continuous developmental continuously adapting to the growing structural remodelling by capillary angiogenesis and and functional needs of each particular region of reabsorption. The penetrating capillaries and their the developing CNS (Marin-Padilla 1985b). The anastomotic plexuses constitute the intraneural intraneural anastomotic plexuses evolve by the vascular territory of the CNS vasculature and the addition of new links (capillary angiogenesis) only elements to participate in the so-called throughout growing and differentiating zones and by the removal of other links (capillary blood-brain barrier. Intraneural capillary angiogenesis can best be reabsorption) throughout zones in which they are studied with the rapid Golgi method or with similar no longer needed. procedures (Klosovskii 1963, Chilingarian and Paravian 1971, Press 1977, Marin-Padilla 1985b).
Intraneural Vascular Territory of the CNS Vasculature
40
2. Embryology
Capillary reabsorption is observed throughout the developing CNS. In Golgi preparations, it is characterized by the progressive reduction in the size and caliber of the regressing capillary and the
References p. 380 eventual disappearance of anastomotic links (Fig 2.12). The nature of embryonic capillary regression and reabsorption remains poorly understood and also needs further investigation.
Fig 2.11 Examples of intracortical capillary angiogenesis from rapid Golgi preparations of the cerebral cortex of 13 day hamster embryos. Each illustration represents the tip of a growing intracortical capillary. The leading endothelium of growing capillaries produces numerous radiating filopodia which advance freely, without a recognizable basal lamina, among the neural elements. Their number, size, length, structural variability and multidirectional growth can be readily appreciated in these illustrations. x800.
References p. 380
Intraneural Vascular Territory
41
42
2. Embryology
References p. 380
Fig 2.13 Schematic drawings demonstrating the mature lamellar composition and structural organization of themenin-geal, the Virchow-Robin and the perivascular glial compartments of the cerebral cortex. Also illustrated are their corresponding vascular territories, namely: the perineural, the interneural, and the intraneural, respectively. The blood vessels of the perineural (meningeal) and interneural (Virchow-Robin) territories are enclosed within specific perivascular tissue compartments, while those of the intraneural vascular territory are enclosed by perivascular glia. The Virchow-Robin space closes off with the fusion of the vascular and the CNS basal laminae into a single lamina which accompanies the penetrating capillary into the neural tissue proper. The obliteration of the pial (P) space at the entrance of the Virchow-Robin compartment is also illustrated. D = dura mater, NT = neurothelium, EA = external arachnoid lamella, IA = inner arachnoid, lamella, EP = external pia lamella, IP = inner pia lamella, GL = marginal glia, P = pial space, ICR = intercellular compartments. The insert shows the vascular basal lamina and its relationship to the meningeal, Virchow-Robin and perivascular glial compartments, respectively, as well as the location of the various intercellular tissue compartments. (From Krisch, В., Н. Leonhardt, A. Oksche: Cell. Tiss. Res. 238: 459, 1984.)
jferences p. 380
Intraneural Vascular Territory
43
44
2. Embryology
Conclusions The embryonic vascularization of the CNS is characterized by the sequential development of three independent, though interrelated, vascular territories. In order of appearance and development they are: the perineural, the interneural and the intraneural vascular territories (Table 2.2). Embryologically, each vascular territory evolves and remains within a distinct and specific tissue compartment, namely: the meningeal, the Virchow-Robin and the perivascular glial tissue compartment, respectively. In the course of embryonic development, the vasculature of each of these territories undergoes an integrated metamorphosis, continuously adapting to the growing structural and functional needs of each particular region of the developing CNS. This progressive vascular metamorphosis is the result of continuous remodelling of the original anastomotic plexuses in
References p. 380
which both capillary angiogenesis and capillary reabsorption are active processes. The three vascular territories and the different and specific types of vessels that characterize each one can be easily recognized at any time in the course of embryonic development (Fig 2.14). The separation of the CNS vasculature into three different and specific vascular territories and associated tissue compartments implies significant structural as well as functional differences among them. Undoubtedly, a clear understanding of these structural and functional differences is important and relevant both to the clinician and the neurosurgeon. In this context, it is interesting that only the intraneural capillaries and associated perivascular glia (intraneural vascular territory) are actually involved in the so-called blood-brain barrier, since the meningeal and the VirchowRobin vasculatures actually evolve and remain outside of the CNS substance.
Vascular Malformation of the Central Nervous System
45
Refences p. 380
В Vascular Malformation of the Central Nervous System. Embryological Considerations should be of great significance in the study of these malformations to be able to distinguish and to separate their primary or original features from the secondary or acquired ones. Any pathologic alteration (rupture, hemorrhage or thrombosis) of a vascular malformation will not only transform the affected vessels but the sur rounding tissue as well. A reparative inflamma tory process will take place around the affected vessels resulting in fibrosis and or gliosis and more importantly in the obliteration of the perivascular tissue compartment which originally surrounded the vascular malformation. The secondary obliter ation of the perivascular tissue compartment could lead to confusion about the original location of the malformation and the CNS vascular territory ori ginally involved. Furthermore, the inflammatory process around injured vessels of the original mal formation will result in the formation of many new or secondary vessels. The presence of postinflammatory vessels should be recognized because they could also obscure the original architecture of the vascular anomaly. ___________ The recognition of these facts is important because in the interpretation any type of vascular malformation of the CNS the following aspects must be clearly established: a) type of vessels originally affected; b) vascular territory and perivascular tissue compartment originally involved; and, c) original location of the anomaly. The establishment of these facts is sine qua поп for the understanding of the nature of these vascular malformations as well as for the selection of the most ad-equate During the early vascularization of the CNS three distinct vascular territories evolve sequentially. These have been named: perineural, interneural, and intramural vascular territories respectively, because of their specific relationship to the nervous tissue (see Chapter: Embryogenesis of the Early Vascularization of the Central Nervous System). Each of these three vascular territories is characterized by distinct types of vessels and most importantly by a specific perivascular tissue compartment. These compartments are: the meningeal, the Virchow-Robin, and the perivascular glia, respectively. The three basic types of vascular malformations of the CNS will be analyzed separately and correlated embryologically with the vessels of its different vascular territories and tissue compartments. method for their neurosurgical removal.
46
2. Embryology
Capillary Telangiectasias and Cavernous Angiomas Capillary telangiectasias are small vascular malformations composed solely of abnormally dilated capillaries. They vary greatly in caliber and saccular or fusiform dilatations are common. They lack an anomalous arterial supply and their venous drainage may be dilated but not abnormally so. The actual number of capillaries may not be increased in these malformations. The overlying pia mater and arachnoid are normal. The intervening tissue between the dilated capillaries is normal and both glial and neuronal elements are recognized in it. These vascular anomalies are frequently found in the pons, the cerebral cortex, the cortical white mater and rarely in the spinal cord. Capillary telangiectasias rarely show pathologic alterations such as hemorrhages, thromboses or ruptures. Therefore, they are usually clinically silent and most are found by chance at autopsies. Embryologically, these are vascular malformations which involve only the capillaries of the intraneural vascular territory of the CNS and should be enclosed within the perivascular glial tissue compartment. Cavernous angiomas are large vascular malformations composed of cystic vascular spaces lined by a single layer of endothelial cells. These vascular spaces vary greatly in size and are often very irregular suggesting secondary changes. The vascular spaces of these malformations probably represent abnormal capillaries since no recognizable arteries or veins are found in them. These vascular spaces are structurally similar to those found in capillary telangiectasias. These vascular malformations may be circumscribed but not encapsulated and could be lobulated. Like telangiectasias, they lack either abnormal arterial supply or abnormal venous drainage. They are found in the cerebral cortex, the pons and rarely in the spinal cord. Cavernous angiomas invariably show areas of thromboses with subsequent organization, recent and old hemorrhages with hemosiderin laden macrophages, fibrosis and or gliosis, focal calcification and even areas with bone formation. The overlying pia mater and arachnoids are stained, thickened and fibrosed. All of these changes are obviously the result of pathological (secondary) alterations. There is no normal nervous tissue between the abnormal vessels in these malformations, probably because it has been progressively destroyed. Eliminating the prominent acquired pathologic changes, cavernous angiomas could
References p. 380
represent large telangiectasias, an idea which has been often expressed previously (Russell 1931. Russell and Rubinstein 1977). Embryologically, cavernous angiomas can only be large vascular malformations involving the capillaries of the intraneural vascular territory of the CNS since no distinct arteries or veins have been recognized in them. They could represent large capillary telangiectasias with a greater £r_ojpensity_ to undergo pathologic alterations. These alterations will result in the complete obliteration of the perivascular glial compartment and in the progressive reactive fibrosis and gliosis of the intervening nervous tissue causing its complete destruction. The neurosurgical treatment of cavernous angiomas will necessarily involve the removal of some of the normal nervous tissue around the malformation.
Venous and Arteriovenous Malformations Venous malformations are vascular anomalies composed solely of abnormally dilated and tortuous veins. They may be composed of a single greatly dilated and tortuous vein or of small number of them. They involve primarily the pia-arachnoidal veins and few of its intramedullary tributaries. They can be located in the spinal cord, and occasionally in the drainage territories of the vein of Galen and of the cerebellum. Secondary pathologic alterations including muscular hypertrophy and or hyalinization (fibrosis) of the vessel wall, and thromboses with subsequent organization are frequent findings in these malformations. However, more important alterations are those caused by the compression of the spinal cord by the anomalous veins, and the compression of the nervous tissue by the dilated intramedullary tributary veins. Cord atrophy and ischemic changes are often sequelae in long standing cases. Embryologically, venous malformations are developmental anomalies which involve primarily the veins of the perineural vascular territory of the meningeal (pia-arachnoid) tissue compartment, and also some tributary veins of the interneural vascular territory of the Virchow-Robin tissue compartment. Therefore, uncomplicated venous malformations should be entirely outside the nervous tissue proper and hence liable to their complete microneurosurgical removal. On the other hand, secondary pathological alterations affecting these venous malformation will result in the obliteration of their perivascular tissue compartments
References p. 380
making their neurosurgical treatment more difficult requiring the removal of some of the surrounding unaffected nervous tissue. Arteriovenous malformations are large and complex vascular anomalies composed of abnormally developed arteries and veins. They involve primarily the vessels of the leptomeninges with extension into the fissures and sulci. They could also involve deeper vascular territories of the cortex, midbrain, cerebellum and choroid plexuses. These vascular malformations are also character-ized d by the participation of regional perforating vessels which could also be abnormally developed, tortuous and dilated. The presence and location of the abnormal perforating vessels should always be explored because they could be the cause of serious damage to the nervous parenchyma and must be treated adequately during the micro-neurosurgica[ removal of the malformation. The main arteries and veins leading to and from the malformation are usually dilated and a secondary collateral circulation could be prominent in some of them_______________________ Arteriovenous malformations are subject to pathologic alterations including: ruptures, hemorrhages, trombosis, atrophy, and progressive reparative fibrosis and or gliosis. The arach noid around the malformation as well as the underlying or adjacent nervous tissue show rusty pigmentation and fibrosis or gliosis. Microscopic examination of both the arteries and the veins of these malformation show abnormalities involving their elastic and muscular elements. Some vessels also show atheromas, organized thrombus, focal calcifications and postinflammatory fibrosis or gliosis.
Sturge-Weber-Dimitri's Disease This congenital vascular malformation is characterized by an increase in the number of capillaries and of few small veins throughout the affected pia mater and underlying surface of the cerebral cortex ._ This extensive capillary-venous cerebral malformation is associated with a homolateral cutaneous angioma over the trigeminal nerve distribu-tion. This vascular malformation is also characterized by significant pathologic alterations, severe damage to the nervous parenchyma, and abua-dant mineral granular deposition of calcium and iron. While a pial capillary plexus is a prominent feature during the embryonic vascularization of the CNS, the adult cortical pia mater either lacks or has very few capillaries (Duvernoy et al. 1981). Embryologically, the persistence of the embryonic pial vascular plexus with its numerous connections to the superficial cortical vasculature could explain this type of vascular malformation. There is no adequate neurosurgical treatment for this fortunately rare condition.
Исправленная стр 47
Embryologically, these malformations involve: a) vessels (arteries and veins) from the perineural vascular territory of the CNS within the meningeal tissue compartment; and b) some perforating or emerging vessels (arterioles or venules) from the interneural vascular territory within the VirchowRobin tissue compartment. Therefore, unaffected arteriovenous malformations should lie outside of the nervous tissue proper and should be liable to complete removal by microneurosurgery. On the other hand, in arteriovenous malformations which have undergone pathologic alterations, the meningeal and Virchow-Robin perivascular compartments might be obliterated making their microneurosurgical treatment more difficult since it must involve the removal of the surrounding nervous tissue.
49
3
Pathological Considerations
Pathogenesis The pathogenesis of angioma is generally attributed to maldevelopment of the cerebral vascular system occurring during the second to fifth stage of Streeter's craniocerebral vascularization. However, the underlying anomaly ultimately responsible for the vascular malformation still remains a matter of controversy. Old hypotheses assumed that embryologic fore-runners_of arteries and veins were separate. Based on meticulous injection techniques Evans (1911) was the first to show that a primary vascular plexus existed as a capillary network, preceding the more definable vascular system. In a prgcess called metamorphosis, fusion of some of the channels of this primordial vascular plexus and dissolution of others takes place and ultimately leads to the differentiation of arteries and veins (Dandy 1928). This process of angiogenesis is controlled by hemodynamic and genetic factors. There is a steady development, not only of the arteries and veins, but also of the capillaries during successive embryological development phases. All investigators concerned with the problem of pathogenesis of cerebral vascular malformations uniformly accept that an error of development occurs during this very early metamorphotic phase. Dandy (1928) postulated a retentiqn,of primordial vascular connections between arteries and veins. Olivecrona and Ladenheim (1957) assumed an embryonic agenesis of the capillary system, ultimately resulting in discharge of arterial blood directly into the venous system through a tangle of abnormal vessels of varying caliber. A concept basically similar to that of Dandy was introduced by Kaplan and Meier (1958). Based on observations made in specimens obtained at autopsy, they concluded that arteriovenous malformations within the cerebral hemisphere represent a perpetuation of a primitive arteriovenous
communication, which otherwise would be replaced by an intervening capillary network during the normal embryological development of the cerebral vascular system. Hamby (1958) approached the problem from a hemodynamic jtandpoint, concluding that the basic characteristic of arteriovenous malformations is a lack of vascular resistance in the area involved by the lesion. Since the normal cerebral vasculature resistance is provided by the capillary bed, Hamby's concept is similar to that of Olivecrona and Ladenheim and based on the agenesis of capillaries.________________ ______ Gold et al. (1964) and Lagos (1977) recognized two types of vascular malformation: 1) a direct end-to-end anastomosis between the arteries and veins of normal structure, representing arteriovenous fistulae and 2) a network of poorly differentiated and immature vessels interposed between the arterial and venous system, representing typical arteriovenous malformations,________ Stein and Wolpert (1980) and Warkany et al. (1984) assumed an arrest of normal development of primitive arteries, capillaries and veins, resulted in the formation of direct arteriovenous communications through immature, poorly differentiated vessels, without an intervening capillary bed. Parkinson and Bachers (1980) maintained that the essential feature of arteriovenous malformations is a shunt responsible for the short-circuiting of the arteriocapillary bed and proposed the descriptive definition of a "congenital arteriovenous fis-tulous malformation" occurring as a consequence of a local angioblastic error. Based on Sabin's (1917) original concept of the development of the primitive vascular plexus, Garretson (1985) recently proposed that AVMs arise from persistent direct connections between the future arterial and venous sides of the primi-
50
3. Pathological Considerations
tive vascular plexus, with failure to develop an interposed network. In summary, most of the theories developed to explain the origin of cerebral vascular malformations have in common the hypothetical concept of total agenesis, or poor development of the capillary network. It is known, however, that normal angiogenesis takes place in a capillarofugal direction and that the predisposing factor for the formation of arteries and veins lies within this primordial capillary network. If there is a primary agenesis of the capillary network and therefore of the driving force for the development of arteries and veins, then this territory must be ultimately avascular. If, however, the theory of primary capillary agenesis is not correct, one must assume a secondary destruction or disappearance of capillaries, in order to explain the absence of a capillary network as the pathogenetic mechanism for vascular malformations. Such a secondary destruction would have to occur through the action of a factor having the capacity to destroy capillary vessels after arteries and veins have been formed from them. In such a situation the arteries and veins would then form
direct communications. Fig 3.1A-G Artist's drawing of the different types of cerebral vascular malformations. A Arterial malformation.
В Arteriovenous fistulous malformation.
С Arteriovenous plexiform malformation. D Arteriovenous plexiform micro-malformation. E Cavernous malformation. F Capillary malformation (telangiectasia).
G Venous malformation.
References p. 381
A capillary destroying factor has not yet been found. Also, if this theory of secondary destruction of capillaries is correct, one would expect to see only cases with direct arteriovenous fistulae. rather than all the commonly known varieties of AVMs in which coiling convoluted vessels are interposed between arteries and veins. For this reason it seems appropriate to discuss another hypothesis: There is neither a primary agenesis nor a secondary destruction of capillaries, but a local or regional disease of capillaries. In a given primitive vascular territory, the normal development of capillaries is disturbed, however, these capillaries do not disappear entirely, but proliferate and thereby develop metamorphotic. dysplastic vessels (Luschka 1854. Dandy 1928). This disease may be defined as a 'proliferalive capillaropathy' of unknown origin (Fig 3.1). It isi characterized by maldevelopment of an area of the primordial capillary plexus into metamorpho-tic vessels. These vessels do not fulfil thejiistolog-ic criteria of arteries, jveins or capillaries. It is, in fact, well known, that it is difficult if not impossible to typify histologically the vessels comprising the core of a vascular malformation. These vessels
Terences p. 381
have been called "unidentifiable type of vessels" by Hamby (1958) (Fig 3.2) and "structural hybrids" by Burger and Vogel (1976). In a histologic study of three cases of arteriovenous malformations, Sorgo (1938) classified the vessels constituting the malformation into three main types, according to the composition of their wall. He also found similarities between the wall [of vessels composing arteriovenous malformations and the wall of normal embryonic vessels. Based on bis observations he postulated that at least one of the described types of vessels may well arise from capillaries. The results of recent electron microscopic studies are in accordance with our proposed concept. Meyermann and Yas,argil (1981) found that the ultrastructural composition of small vessels of 41 surgically obtained arteriovenous malformations could be divided into two distinct types; vessels with a closed and vessels with a fenestrated endothelial cell layer. This second type of vessel, char-
Pathogenesis
51
acterized by a fenestrated endothclial coat is clearly abnormal, since fenestrations of endothelial cells do not occur in the normal brain vasculature with exception of the area postrcma, choroid plexus, pineal and pituitary glands, intercolumnar tubercle, and certain nuclei within the hypothalamus (Lee 1971). Another observation of this study was the sprouting of new capillaries in the fibrotic arachnoid surrounding superficial pathological vessels. This finding supports the concept of a proliferative capillaropathy (Figs 3.3, 3.4). Depending on the extension and distribution of the capillary disease involving the primitive vascular plexus, vascular malformations may therefore be defined as localized, multiple or diffuse collections of metamorphotic vessels, abnormal in number, in structure and in function. ______ The result of this primary disease of capillaries is a mal-production and therefore a mal-formation of both arteries (or arterioles) and veins (or venules), i.e. a metamorphotic angiodysplasia or capillaropathy.
52
3. Pathological Considerations
References p. 381 Fig3.3A-B A Sinusoid-type vessels of AVMs are coated by fenestrated endothelial cells. The fenestrae are indicated by arrows. In the normal cerebral vas-culature this type of endothelial coat is only present in certain distinct areas of the CNS. The cytoplasm of the endothelial cells is filled with cross-sectioned filaments and some vacuoles. The arrowhead indicates a so called Weibel-Palade body. This organelle can only be found in endothelia, and is a rare feature in a normal cerebral vessel wall. Bar = 1 цт В Although some gaps in the endothelial cell layer of AVM are demonstrated as in A, some cell contacts of adjacent endothelia are tight as seen in normal cerebral vessels. Bar = 1 |im. By courtesy of Dr. R. Meyer-mann. Fig 3.4 Arteriovenous malformation surgically resected from the left occipital lobe of a 24 year old female patient (see Fig 3.78). Note the considerable variation of vessel size with dilated, partially arteria-lized veins (V) and occasional small arteries (arrow). In the lower half malformed compact vessels with little or no intervening parenchyma prevail, thus resembling a cavernous angioma (Elastica van Gieson, x10). By courtesy of Prof. P. Kleihues, Zurich.
p. 381
Terences p. 381
chyma between the vascular spaces of the malformation, and 3. the state (normal or gliotic) of the intervening neural tissue. Based on these morphological parameters vascular malformations are divided into four main types: 1. arteriovenous malformations 2. venous malformations 3. cavernous malformations and 4. capillary malformations (or telangiectasias) (McCormick 1966).______ Despite this attempt to separate various different forms, certain observations support the hypothesis of a single underlying primary lesion. Transitional forms exhibiting the histologic char-acteristics of more than one of the above men-tioned types are sometimes encountered within the same malformation. It is, in fact, difficult to distinguish histologically between telangiectasia and venous angioma. Also telangiectasias have been reported to be a component of venous angio-mas (McCormick 1966, Manuelidis 1950). Combinations of cavernous and telangiectasias (Roberson et al. 1974), as well as venous angio-mas and arteriovenous malformations (Huang et al. 1984), have been reported to occur within the same malformation. Also multiple lesions of different histologic types can occur in the same individual (McCormick 1966). Although absence of capillaries has usually been described as the hallmark of arteriovenous malfor-
Pathogenesis
53
mations, abnormal proliferation of capillaries may be observed within the malformation or even in adjacent tissue. Hamby (1958) in a unique histologic study of a specimen of an arteriovenous malformation of the brain, demonstrated not an agenesis or absence of capillaries, but a multitude of different types of capillary-like vessels, clearly distinguishable from the entering arteries and the draining thin-walled tortuous veins. These capillary-type vessels found in the central core of the malformation form a complex of coiling and intercommunicating vessels (see Fig 3.2). Dilated capillaries or capillary-like spaces are found in telangiectasias, which are therefore also called capillary malformations, as well as in cav-ernomas (Huang et al. 1984). By the same reasoning certain vascular malformations of the subcutaneous tissue are also called capillarovenous malformations (Merland et al. 1983). In histologic studies of Cabanes et al. (1979) cases of venous angioma with a clear participation of capillaries are demonstrated.
54 исправленная Considerations
3. Pathological
We should also, perhaps, remember Virchow's statement of 1851 - that "one type of angioma can transform into another by changes in flow and pressure or by cellular proliferation". Histologically, the presence or absence of inter vening neural parenchyma, as well as its state (normal or gliotic) are used as parameters for clas sifying vascular malformations. Usually, arteriovenous malformations surround gliotic tissue, ve nous malformations and telangiectasias have nor mal intervening tissue, and cavernous malforma tions contain no intervening parenchyma. Both histologic studies and intraoperative observations show, however, that an intervening neural paren chyma and even gliosis within it may occur with all types of cerebral vascular malformations. Cavernous malformations are classically described as being compact, with the vascular spaces being contiguous with one another and lacking interven ing tissue. During operation on such lesions, however, one may observe through the operating microscope, small cavernous spaces located at the periphery of the mass and being clearly separated from it by brain parenchyma. ви; In a histologic study, Manuelidis (1950) clearly demonstrated neural tissue between the vascular spaces of an otherwise typical case of cavernous angioma. A finding common to all types of cerebral vascular malformation is spontaneous thrombosis, occurring most frequently in the venous space of the lesion. Although such spontaneous thromboses have been most often reported in cases of true AVM, they clearly also occur with the other types, especially venous and cavernous malformations. The histological character of the resected lesions and the relative frequency are given in Table 3.3. Table 3.3
Histological findings in 398 AVMs
Mixed type
374 cases
(94.0%)
More arterial
12 cases
( 3.0%)
More venous
1 2 cases
( 3.0%)
398 cases Not investigated 16 galenic and 2 fistulous lesions.
Hemorrhage, which most frequently occurs in arteriovenous malformations, may also be observed with other types of vascular anomalies. Microscopic hemorrhages with foci of hemosiderin laden macrophages are frequently found in arteriovenous malformations, but may also be seen in venous, cavernous and even capillary-type malformations.
From these pathologic-anatomic observations it becomes evident that cerebral vascular malformations have characteristics in common with respect to their histologic nature, their vascular composition, and regressive changes, irrespective of their type. Using cerebral angiography, the different morphologic types of vascular malformation described above can usually be distinguished (Tables 3.2, 3.4). Arteriovenous malformations typically appear during the arterial phase of the angiogram and are characterized by large feeding arteries, a more or less compact conglomeration of coiled vessels and prominent draining veins. Venous angiomas most frequently appear during the venous phase and are characterized by numerous dilated, linearly arranged medullary veins, producing an umbrella-shaped configuration and converging towards a markedly dilated central paren-chymal vein. Cavernous angiomas may cause an avascular mass effect, but remain invisible with usual angiographic techniques, owing to their slow circulation and the lack of prominent feeding arteries. A blush, representing pooling of contrast material within the vascular spaces of the lesion, may however appear, if either prolonged injection angiography (Numaguchi and Nishikawa 1979) or a repeated injection series (Huang et al. 1984) is performed. In telangiectasias, angiography is usually negative, owing to their small size and their slow circulation time. Occasionally, however, telangiectases may show a small stain or blush during the venous phase of the angiogram (Huang et al. 1984). Although the different morphologic types of cerebral vascular malformation are distinguishable on angiography, certain observations support the concept of a single underlying cause, common to all types of vascular malformation. One may occasionally demonstrate both transitional forms as well as the coexistence of two or more different types of lesion within the same vascular malformation. A pure venous type of malformation was demonstrated angiographically in 1958 by Krayenbuhl and Ya§argil. The histological examination showed no arterial component in the lesion (Fig 3.5). According to Huang et al. (1984) 14% of cases of venous angioma contain fine arteries which form a reticular blush in the arterial phase of the angiogram. This indicates the presence of an arterial or low-flow arteriovenous component in certain venous angiomas. It clearly contradicts the classical definition, according to which venous angiomas lack arteriovenous shunts or an arterial component and become visible only in the late venous phase of the angiogram. Similar observa-
Pathogenesis
References p. 381
55
Fig 3.5 A-C This may be the first angiography demonstration of a venous angioma. (54 year old male presenting with subachnoid hemorrhage. From Krayenbuhl, H., M. G. Ya§argil: Series Chirurgia Geigy 4: 76 1958.) A normal arterial phase of carotid angiography. В Venous phase of carotid angiogram after a SAH shows the lesion in the right temporal lobe. It drains into the dilated basal vein of Rosenthal. In 1958 this malformation was called "Arteriovenous malformation visible only in the venous c Histological examination shows venous malformation with arterial components. mal veins adjacent to the angioma are hypoplastic or even absent and that the adjacent superficial or cortical veins may be poorly developed. Also hypoplasia of the internal cerebral veins, poor development or even absence of certain major subependymal veins and a paucity of superficial cortical veins have occasionally been observed" (Huang et al. 1984). Veins pursuing an unusual course, most probably representing persistent fetal or intrauterine venous structures, are frequently observed angiographically in such cases (Huang et al. 1984). Similar anomalies of the venous system may also be observed in cases of arteriovenous malformation. Unfortunately, angiographic study of the venous drainage patterns of cerebral vascular malformations has been generally neglected (see below). Review of our own angiographic material disclosed an unsuspected 30% incidence of associated anomalies in the venous drainage system of AVMs similar to those reported to occur with venous angiomas (see Vol. Ill B, Table 9.2). Our own operative findings have also demon-
56
3. Pathological Considerations
strated clear overlaps of histological types of malformation within single lesions. There have been AVMs with a predominance of arterial or venous components, cavernous malformations with definite feeders bearing aneurysms, capillary caverno-mas with no visible arterial or venous connections and virtually isolated from surrounding tissue by firm encapsulation, and venous malformations with arterial components found at operation and confirmed histologically but which could not be demonstrated angiographically. Upon comparing the clinical features of the different types of cerebral vascular malformation, it becomes evident, that with the exception of a bruit and some symptoms associated with steal phenomena, which exclusively occur with certain high-flow arteriovenous malformations, all other symptoms such as epileptic seizures, hemorrhage, progressive neurological deficit, and headache, may occur with any type of vascular malformation albeit with some variations in incidence (Table 3.5). There is therefore pathological, anatomical, angiographic, surgical and clinical evidence for a common underlying pathogenesis of all forms of
References p. 381
cerebral vascular malformation, based upon a disease of capillaries. The seemingly distinct forms of cerebral vascular malformation described by pathologists, diagnosed angiographically by neu-roradiologists and operated upon by neurosur-geons represent nothing more than different manifestations of the same disease. This concept supports the theory of van Bogaert (1935), who doubted that the different types of cerebral vascular malformations represent different disease entities,and expressed the opinion that there is only one Angioma-Disease (maladie angiomateuse) with a variety of subgroups. He was able to explain the pathogenesis of this disease by assuming a disturbance in the development of small vessels as the underlying mechanism.
Nomenclature
57
Case 3.5 Clinical features of the different types of cerebral vascular malformations AVM
Venous malformation
Cavernous malformation
Telangiectasis
Patology
Usually gliotic brain parenchyma, but not in compact AVM-cases
Usually normal brain parenchyma
No intervening brain parenchyma
Usually normal brain parenchyma
Patogenesis
Cong. agenesis of capillaries?
Agenesis of connecting Sinusoid change of Dilatation of capillaries venous segment! capillary-venous system
Localiization
Every layer, every site
Cerebral, cerebellar
Everywhere, extrinsic, intrinsic
Rons >
Heredity
Seldom (7 cases in literature)
?
Seldom
?, Rendu-Osler
Unknown
Unknown
?
?
?
7
Associated Seldom Malformatio ns Sex Male > female 1.4 = 1 Age
20-40 years, children seldom
Middle age, children rarely
Middle age
Middle or old age
Multiple
Seldom
Solitary
Solitary > multiple
?
Aneurysm
10%
7
?
1 case (own)
Size
Occult — > giant
Small - large strip
Ovoid 2-5 cm
Very tiny
piape
Spider-, wedge-shaped
Umbrella-, medusaHoneycombed, shaped, mushroom-like mulberry-, raspberrylike
Petechial
binic
Silent = stormy
Silent = acute
Silent = acute
Silent = acute
Skull x-ray Calcification (rare) Calcification (except.) Calcification frequent CT Small > Small > Micro > Small > Small > Small > + + + rarely "blush" MRI Angiography
Occult Occult Occult Occult
Atemodynami Volume increased > c Speed increased >
Normal Normal
Normal Normal
Classification of Vascular Malformation "The classification of the vascular malformations of the brain has been the subject of considerable discussion and the extensive literature on this topic reflects a varying and, at times, confusing nomenclature." (Bebin and Smith 1982, p. 13). The confusion continues and applies not only to vascular malformations of the brain but also to those of all other organs. We agree with Mulliken 11983) "the words to describe the common vascular birthmarks reflect our ignorance of their pathogenesis". There are majors problems with both nomenclature and classification.
Normal Normal
Nomenclature A. Both Greek and Latin roots are used: Vascular malformation (Latin roots), Angiodysplasia (Greek roots). B. The suffix oma (= neoplasm) is commonly used not only for true vascular tumors such as hemangioblastoma, but also for vascular malformations. The use of the suffix osis (e. g. "angiomatosis") has sometimes been inappropriate. The term should be reserved for diffuse or multiple lesions only.
58
3. Pathological Considerations
At the present time the English version of "malformation" has found general acceptance and there is little point in entering further into sophisticated linguistic struggles. Classification As ever more sophisticated means of studying vascular malformations have developed, systems of classification have diversified from the early descriptive terms based purely on gross morphological observation. In some instances, old terminology has been retained, in others changed and in yet further (often simultaneous) publications regrouped under different headings. Noran presented and discussed all the proposed classifications in the literature up to 1945 and concluded: "a comprehensive evaluation of the literature is warranted in order that one may arrive at some correlation between these various nomenclature and classification." Within the last 40 years further new concepts have been proposed. Table 3.6a contains some of the more notable historic and modern classifications, and shows the development of thinking regarding the malformations. Virchow (1863) conducted his own thorough studies and described 4 main types of malformation and stated, as early as 1851: "one type of angioma can transform into another by changes in flow and pressure or by cellular proliferation." The venous anomalies, and plexiform angioma of Dandy's classification (1928) would nowadays be called AVM, and the cyst with angioma in the wall a hemangioblastoma. We assume that he did not describe any "venous angiomas" as now recognized by Huang et al. (1984) and McCormick (1985).
References p. 3821 Table 3.6a Virchow (1863) 1. Angioma simplex Telangiectasia (can change to cavernoma) 2. Cavernous angioma 3. Racemous angioma a. Arterial (aneurysma anastomoseon) b. Venous angioma c. Arteriovenous aneurysm 4. Lymphangioma Dandy (1928) 1. Angioma a. Cyst with angioma in the wall (actually angioblastoma) b. Cavernous angioma c. Plexiform angioma (nowadays a form of AVM) 2. Arteriovenous aneurysm (nowadays a form of AVM) 3. Venous abnormalities (nowadays also AVM) Gushing - Bailey (1928) 1. Hemangioblastoma (true neoplasm) a. Cystic b. Solid a capillary (3 cellular у cavernous (nowadays = cavernous angioma) 2. Angiomatous malformation a. Telangiectasias b. Venous angiomas c. Arterial or arteriovenous angiomas (AVM) Bergstrand - Olivecrona - Tonnis (1936) 1. Angioma cavernosum 2. Angioma racemosum a. Telangiectasias b. Angioma capillare et venosum calcificans (Sturge-Weber disease) c. Angioma racemosum arteriale d. Angioma racemosum venosum e. Aneurysma arteriovenosum 3. Angioblastoma, angioreticuloma or Lindau tumors 4. Angioglioma (!) Turner - Kernohan (1941) (spinal cord) 1. Vascular malformations a. Telangiectasia b. Angioma or hamartoma a angioma venosum P angioma arteriovenosum or Y angioma arteriale 2. Vascular neoplasms a. Capillary a capillary hemangioma |3 hemangioendothelioma Y capillary hemangioblastoma b. Cavernous a cavernous hemangioma p cavernous hemangioblastoma c. Hemangiosarcoma
p. 382
Classification
59
Table 3.6a Continuation
Wyburn-Mason - Holmes (1943) (spinal) 1. True tumors a. Hemangioblastoma a angioreticuloma P extradural hemangioblastoma 2. Malformations a. Telangiectasia b. Venous malformation a secondary venous anomalies (3 venous angioma c. Arteriovenous angioma d. Arterial anomalies Menuelidis (1950) 1. Telangiectasia a. Primary b. Secondary 2. Cavernous hemangioma 3. Venous hemangioma 4. Arteriovenous hemangioma Zuich ( 1 9 5 1 ) 1. Angioreticuloma 2. Malformation a. Cavernous angioma b. Racemous capillary angioma (telangiectasia) c. Capiliar et venous angioma (Sturge-Weber) d. Venous angioma e. Arteriovenous aneurysmatic angioma Asenjo (1953) I. Congenital lesions A. Expansive malformation a. Arteriovenous aneurysm b. Arterial racemous aneurysm c. Venous racemous aneurysm B. Angiosis d. Congenital arterial aneurysm e. Meningeal varix f. Sinus pericranii II. Acquired lesions A. Aneurysms a. Arteriosclerotic b. Mycotic c. Syphilitic B. Carotid-cavernous fistula C. Traumatic aneurysms II. Tumors A. Hemangioblastoma a. Benign b. Malignant B. von Hippel-Lindau disease C. Angiomatous meningioma
Pluvinage (1954) I. Angioreticuloma II. Angioma 1. a. Cavernous angioma b. Telangiectasia 2. Sturge-Weber 3. Venous angioma a. Cerebral varix b. Racemous venous angioma c. Peleton de veines (!) 4. Arterial angioma a. Racemous arterial angioma b. Arteriovenous aneurysm Olivecrona - Ladenheim (1957) Etiology 1. Acquired 2. Congenital a. Anomalous arteriovenous b. Angiomatous arteriovenous Pathology 1. Cavernous 2. Racemous a. Telangiectasia b. Sturge-Weber c. Venous racemous d. Arterial racemous e. Angiomatous arteriovenous Russe/ - Rubinstein (1963) 1. Hemangioblastoma 2. Vascular malformation a. Capillary telangiectasia b. Cavernous angiomas c. Venous and arteriovenous malformation McCormick (1985) (in Fein and Flamm) I. Angioblastoma Angiomas 1. Venous angiomas 2. Capillary angiomas (telangiectasias) 1 1 2 cases 3. AVM 41 cases 4. Cavernous angiomas 5. Transitional 11 cases 5 cases Classification of Plastic Surgeons Kaplan 4 cases (1983) A. Stage 1 (undifferentiated capillary network) 1. Capillary hemangioma 2. Cavernous hemangioma B. Stage 2 (retiform plexus) 1. Diffuse microfistula 2. Localized macrofistula
60
3. Pathological Considerations
References p. 382
Table 3.6a Continuation
C. Stage 3 (mature vascular malformation) 1. Venous hemangioma 2. Venous hypoplasia (Klippel-Trenaunay syndrome) 3. Hemangiolymphangioma (vascular hamartoma) Spira (1983) A. Benign hemangiomas 1. Typical a. Capillary hemangioma b. Cavernous hemangioma c. Mixed-combined hemangioma d. Port-wine stain - nevus flammeus e. Angioma racemosum f. Angiokeratoma (Mibelli) 2. Atypical a. Sclerosing hemangioma b. Pyogenic granuloma c. Spider telangiectasia (nevus araneus) d. Glomus tumor e. Hemangiopericytoma f. Juvenile nasopharyngeal angiofibroma g. Venous lakes B. Syndromes - diseases 1. Rendu-Osler-Weber syndrome 2. Sturge-Weber-Dimitri syndrome 3. von Hippel-Lindau disease 4. Maffucci syndrome 5. Blue Rubber Bleb syndrome 6. Kasabach-Merritt syndrome 7. Klippel-Trenaunay syndrome C. Malignant hemangiomas 1. Angiosarcoma 2. Kaposi sarcoma 3. Dermatofibrosarcoma protuberans Classification of Neuroradiologists Merland et a/. (1983) 1. Pure arterial dysplasia (2 cases) 2. A-V dysplasia (macroscopic shunt) a. Simple direct A-V fistula vertebra-vertebral, vertebra-jugular carotido-cavernous, carotido-jugular b. A-V malformation (60 cases) 3. Capillary and capillary-venous malformation (26 cases) a. Pure capillary (Rendu-Osler) b. Capillary-venous malformation
4. Venous and cavernous ectasias (100 + 4 cases) 5. Additional types a. Unmature angioma of the newborn b. Portwine stain angioma c. Unusual angiomas Hemodynamic Classification 1. Active (large blood flow, direct A-V fistula) high flow 2. Inactive vascular
Huang et al. (1984) I. Those that involve feeding arteries and draining veins (easily demonstrable angiographically) 1. Superficial type (pial or superficial AVM): involving mostly the cortical gray matter (and subjacent white matter) 2. Deep or central type (deep or central AVM): involving the subcortical (or central) gray matter and the adjacent white matter 3. Medullary type (AVM with a medullary component): involving primarily the medullary arteries and veins Classical pyramid-shaped AVMs are mostly a combination of the superficial type and the medullary type II. Those that primarily involve capillaries 1. Cavernous capillary malformation 2. Rendu-Osler-Weber disease 3. Louis-Bar syndrome III. Those that primarily involve veins 1. MVM a. Without an arterial component. Sturge-Weber disease should also be included here b. With an arterial component. (This should not be confused with an AVM with medullary component) 2. Cavernous venous malformation 3. Phlebectasia or varix (most of these cases, if not all, are MVMs) IV. Any combination of the above
References p. 382
Gushing and Bailey (1928) were the first to separate two groups: I. Angioblastoma (true neoplasm), II. Angiomatous malformation. They did not consider cavernous angioma as a separate entity and listed it under angioblastoma. Their venous angiomas would be called AVMs today. Bergstrand et al. (1936) added to the neoplastic £roup the angiogtioma of Roussy and Oberling. These are to a large degree still not accepted, yet appear to have been occasionally identified (Bon-nin et al. 1983). Bergstrand doubted the existence of a true arterial aneurysm as described and illustrated by Simmonds (1905) (Figs 3.5, 3.6).
Classification
61
Huang et al. (1984) noted the wide acceptance of Russel and Rubinstein's (1963) classification. However, they pointed out the disadvantages of attempting to differentiate histologically between many cavernous venous malformations and venous angiomas and showed that some areas within venous angiomas may be similar to capillary malformations or even an AVM. The classification of Huang et al. has put forward new and important elements for consideration. We include the classification of Merland et al. (1983) as a very stimulating view of the external angiomas, seen from the perspective of the inter-ventional neuroradiologist. The classification of Kaplan (1983), Spira (1983) show up the similar problems experienced by plastic surgeons in describing cutaneous malformations.
The Author's Classification Our own classification is based on the relative preponderance and contribution of the various vascular elements, arteries, veins, capillaries» and abnormal channels (Table 3.6c). There may run a spectrum from theoretically completely arterial lesions to completely venous lesions and from large fistulae to extensive convoluted vessels. While the lesions can conveniently be grouped into four primary headings, there are at each level examples of transitional lesions, e.g. AVMs with slow flow or venous malformations with increased flow. Part of the definition of the lesion must rest with dynamic properties related to flow and shunting, which cannot be examined by the pathologist in the resected specimen or at autopsy. We propose the following classification more for practical use in ncuroradiology, neurology and neurosur-gery but hope that neuropathologists will be stimulated to undertake further investigation of these lesions.
62
3. Pathological Considerations
References p. 382
Table 3.6c Authors classification I. Vascular neoplasms 1. Hemangioblastom a a. Cystic b. Solid 2. Angioglioma (mixed and glioma)
hemangioblastoma
3. Angioblastic meningioma 4. Hemangiopericytic meningioma (hemangiopericy-toma of the meninges) 5. Angiosarcoma II. Malformations 1. Telangiectasia 2. Cavernous malformation a. Intrinsic b. Extrinsic 3. Venous malformation a. Cortical b. Subcortical (medullary) a superficial p deep 4. Arteriovenous malformation a. Plexiform (dilated, tortuous pathological vessels with thickened or thinned (or combined) walls, arteriectasia, aneurysms, phlebectasia, varices; they can be cryptic, occult, micro, moderate, large or giant in size. They may be uni- or multilocular. They may have a mono-nidus with mono- or multi-compartments) b. A-V Fistula (direct communication between arteries and venous channels (veins and sinuses) without the interposition of a convolute, a simple: - carotid = cavernous, carotid = jugular, - MCA = v. Labbe or v. Trolard or Sylvii, - АСА = inferior sagittal sinus, - pericallosal artery = v. Galen, - PCA = v. Galen, PCA - transverse or sigm. sinus, - vertebro = vertebral, vertebro = jugular, - AICA = lateral rec. vein or petrosal sinus, - SCA = transverse sinus, - basilar artery = galenic vein P complex: pericallosal + PCA + MCA = v. Galeni, - MCA + dural branches = herophilic sinus or SSS, - PCA + dural branches = herophilic sinus or transverse sinus.
c. Transitional type between a-c a more fistula > less plexiform (network) p more network > less fistula 5. Transitional malformations Combinations 1+2, 1+3, 2+3, 1+2+3, 3+4 (Huang) 1+3+4 (Huang) Vascular malformation and vascular tumor associated! with phacomatosis (Phacomatotic angiomatous diseases) Neurocutaneous syndromes 1. Angioblastoma (angioreticuloma) (von Hippel-Lir-dau) (angioblastomatosis) 2. Encephalofacial angiomatosis = neuro-oculocu-taneous (Sturge-Weber-Krabbe-Dimitri) 3. a. Hereditary hemorrhagic telangiectasia (Rendu-Osler-Weber) (cutaneous, mucosa and visceral capillary malformation) b. Ataxia telangiectasia (Louis-Bar) facial naevus, cerebellar angioma, angioma of the choroid of the eye, defective immune glo-bulin system of the IgA class 4. Encephaloretinofacial } (Wyburn-Mason) angiomatosis J (BonnetDechaume-Blanc) 5. Orbitothalamoencephalic angiomatosis (Bregeat syndrome) 6. Diffuse corticomeningeal capillovenous familial angiomatosis (non calcifying) (DivryVan Bc-| gaert) 7. Cutaneomeningospinal angiomatosis (Cobb) 8. Congenital venous dysplasia (extremities, spinaij (Klippel-Trenaunay-Weber syndrome) 9. Glomangiomatosis (glomus tumor) (Bailey) 10.Dyschondroplasic hemangioma (MaffucciKost 11. Angiokeratosis naeviformis (?) 12. Extensive cavernous hemangioma + thromboc.-| topenia and purpura (KasabachMerritt syndromet 13. Blue Rubber Bleb syndrome 14. Malignant hemangioma
Localization of AVM
p. 382
63
The gliotic area surrounding an AVM may represent the brain reaction to pulsation of the AVM, to ischemia, to microhemorrhage or to a primary developmental phenomenon (lack of an astrocytic layer around vessels, therefore diffusion of metabolites) . It is assumed that because of the dysplasia of a capillary bed, there is no functioning brain tissue within the AVM itself, at least in compact lesions. However, we do not know at what distance from the lesion normal cerebral architecture is preserved and this must vary in each case. A better understanding of the pathophysiology of the lesion thus awaits a more comprehensive embryo-logical and histological analysis. Localization Besides the 'pure' AVM occupying a single intra-cranial compartment we have seen examples of AVMs involving multiple anatomical layers including skin, muscle, bone, dura, arachnoid, brain, and ventricle. The following combinations have been described: If the vascular malformations do indeed represent the result of an early deep fistula with remote effects, it is surprising that the lesions are not multiple more often, as many areas of the vascula-ture would be at risk. Garretson (1985) has categorized cerebral AVMs I which, incidentally are seen most frequently involving branches from the MCA, less often the ACA, and least frequently the PCA) as those involving the epicerebral, transcerebral and sub-ependymal circulations (see also section on micro-circulation). He notes that AVMs involving only the transcerebral (long perforating) arteries are not visible on the surface of the hemisphere yet arterialized veins may frequently be seen owing to the anastomoses between the transcerebral and epicerebral veins. A rare group of AVMs remains confined to the pial surface of the brain stem. Neuropathological studies have shown that brain tissue around an AVM is frequently gliotic and exhibits cystic changes. Besides these subcortical changes which may extend very deep into the white matter there may occasionally be seen cases of severe encephalomalacia with atrophy of gyri or lobules in the neighbourhood of the AVM and also changes of the arachnoid-pia-layer. In some cases this change is combined with hemorrhage, but in others there is no sign of bleeding. The superficial and deep changes are not clearly related to the site or size of the AVM. Neurosur-gical Localization of the AVM WithintheBrain observations do not confirm that gliotic change around AVMs do not always involve all layers of the brain from the convolutions is, as often stated, a "pseudocapsule or surface arachnoid down to the ventricle (Figs 3.7A-B, matrix" in every case. 3.8). From the surgical perspective they may be divided into the following groups and subgroups:
64
3. Pathological Considerations
References p. 382
I. Surface Lesions (visible on exploration on the surface of the brain) 1. Dorsal surface (frontal, ternp., occip., cerebetl.) 2. Basal surface (frontal, ternp., occip., cerebell.) 3. Polar surface (frontal, ternp., occip.)
a. cortical - sub-cortical (Fig 3.9A-C) b. cortical + subcortical + subependymal (intraventricular) (Fig 3.9D)
II. Deep Lesions (invisible at exploration on the surface) 1. Sulcal (all sulci, especially precentral, postcentral, inferior parietal, parietooccipital, calcarine) 2. Fissural lateral (Sylvii) fiss. interhemispheric fiss. transverse fiss . 3. Deep white matter (semiovale center) 4. Deep gray matter (striate, thalamic etc.) 5. Subarachnoidal (cisternal)
6. Intraventricular
a. cortical -lied primarily by perforating arteries of the АСА, MCA, PCA, PcoA, anterior and posterior ch о ro idal_arteries, AICA, PICA, SCA, vertebral and basilar arteries. II 5 Cisternal (Subarachnoidal) (see Fig 3.13B} Although angiography of an AVM of the vein of Galen shows the lesion in the very center of the brain, surgical experience has shown that they lie entirely within the cisternal system. Surgical explorations have further demonstrated that there exist pure cisternal (subaraehnoidal) AVMs which may be paramcsencephalic (ventral or dorsal), parapontine (ventral or ventrolateral within the cerebellopontine angle) and parabulbar (around the medulla oblongata). These paramcdullary superficial AVMs of the brain stem seem to be an intracranial equivalent to some paramedullary spinal AVMs. II 6 Intraventricular (see Fig 3.11) A few totally intraventricular AVMs of the cho-roid plexus within the trigonum are known. These lesions may be approached through jhe corpus eallosum. We have seen 2 cases with an AVM of the tela chorioidea of IITrd ventricle, three cases of lateral ventricle, and two cases of an AVM of the plexus chorioideus of the IVth ventricle.
F i g 3 . 1 1 A - C Surgically observed loca- lization para- and intraventricular AVMs with ostruction of ventricular system. A Anterior catlosal and septal (1}, Fig3.11B, С
70
3. Pathological Considerations
продолжение
Fig3.11B, С
В Paraventricular. С Varix, intraventricular.
As can be proven angiographically, AVMs in groups I la, 2a, За and II la, 2a, За (see page 64) are supplied by cortical arteries rather than perforators whereas in groupsi Ib, 2b, II Ib, 2b, 3, 4, 5, 6 the reverse is true. Cisternal AVMs. particularly vein of Galen malformations, appear to be supplied about equal])' by cortical and perforating vessels (Figs 3.12-13). {Fig 3.12A-D The cerebral and cerebellar AVMs are similarly composed. Angiographically the flow to the AVM can be visualized .from mainly 1 (A), 2 (B) or 3 (C) sources {АСА, MCA, PCA or PICA, AICA, SCA) or only from perforators (D). a = anterior cerebral artery, m = middle cerebral artery,_p__= posterior cerebral artery, d = deep perforators.
References p. 382
Localization of AVM
71
Fig3.13A-d
A Cerebral convexial AVM supplied mainly by cortical branches of АСА, MCA, PCA. Possible participation of dural branches. The perforating feeders very often participate in the supply of the AVM even though they may be invisible angiographically.
B AVM of vein of Galen is usually supplied by both cortical and perforating branches
Fig3.13C, D
72
3. Pathological Considerations
References p. 382
Fig 3.13C Deep, e.g. thalamic, parathalamic AVMs, are mainly supplied by perforating arteries.
Fig 3.13D Infratentorial convexial AVMs are composed similarly to cerebral convexial AVMs. These are mainly suppliec by cortical (SCA, PICA, AICA) and perforating feeding arteries, from basilar artery and its branches.
-eferences p. 382
The Nidus
73
Histologically, the nidus is composed of vein-like structures whose walls are often thickened and hyalinized. These have been termed arterialized veins in that the intima and muscularis are thickened but there is no elastic tissue characteristic of arteries. Saccular (varicose) enlargements may occur in these veins. The walls may also contain calcium or amyloid deposits. Deshpande and Vidyasager (1980) suggest that these structures represent persistent embryonic veins histologically comparable to venous structures found in the 20—80 mm embryo. Brain tissue within the nidus is usually gliotic and may show deposits of hemosiderin from previous microscopic hemorrhages. AVMs can broadly be divided into two main types: those with a single nidus (with all the vascular channels somehow interrelated) and those with more than one nidus in which there are adjacent but individually separated components of the malformation (Table 3.8) (Figs 3.14-3.18).
Table 3.8 Nidus (Epicenter) /.
Single, compact a. Without fistula b. With A-V fistulae of every size (associated with varix) c. Only A-V fistula visible (convoluting invisible)
//. Multifocal (multicentric - polycentric) compact (subdivided into a-b-c as in I) 1. 2. 3. 4. 5. 6.
Unilateral Bilateral Supra-, infratentorial Orbital and cerebral Cutaneous, dural and cerebral (4 and 5 combined)
///. Diffuse (no visible nidus) (non-nidus) (Scattered pathological arteries and pathological veins without recognizable connections (angiogra-phically or at operation) a. b. c. d. e.
Small areas Large areas Entire hemisphere Both hemispheres Supra- and infratentorial
74
3, Pathological Considerations
References p. 382,
The Concept of Compartments In AVMs with a single nidus, a wide spectrum of structural variation is possible, depending on the complexity of arterial supply and venous drainage. Just as one or more arterial branches may feed the lesion, one or more veins may drain it. Arteries may be branches of a single arterial system, may involve two or more cortical arteries such as anterior and middle cerebral arteries, or may be composed of combinations of cortical and perforating arteries (see Fig 3.12A—D). In the case of multiple niduses these may be confluent or separated by brain parenchyma. The blood supply may be provided by one or by different cortical or perforating arterial systems whether or not the niduses are separated by brain tissue. The individual draining veins may converge into one large collecting vein or the venous drainage may be accomplished by separate venous systems. (It seems by definition that there should be one vein for each nidus if it is really to be considered a separate entity). A single compact nidus may be very simply constructed having only one feeder and one or more draining veins (monocompartmental). The elimination of the single feeder leads to collapse of the entire malformation. A single nidus, however, may have considerable complexity with variations depending on the number and type of feeding arteries and draining veins. Either one or more arterial branches may feed the lesion and one or more veins may drain it. Arteries may be branches of a single system of arteries, may involve two or more cortical arteries, or a combination of cortical and perforating arteries.
Fig3.15A-E Single nidus - single compartment. A-B With 1 or 2 cortical feeders with 1 or 2 or more draining veins. C-D With 1 or more cortical feeders and perforating fee ers. E With multiple perforating feeders only.
Fig 3.14A-C Composition of AVM nidus. A Single monocompartmental nidus. В Single multicompartmental nidus. С Multiple niduses.
References p. 382
The Concept of Compartments
75
Fig 3.17A-C Relation of the feeding arteries and draining veins to different compartments of an AVM. A Supplied from same artery with single or 2 compartments, single or multiple veins. В Supplied from 2 arteries, single or multiple compartments and single or multiple draining veins. С Supplied from 3 arteries, single or multiple compartments and single or multiple draining veins. Fig 16A-C Multiple niduses. A Supplied from same artery (e.g. АСА, РСА, MCA). B Supplied from different arteries. C Vith nidus of perforators and subependymal drainage.
Fig 3 18A-E Variations in venous drainage of different compartments. A single cortical feeder and corresponding cortical drainvein. B single cortical feeder and combined cortical and subependymal drainage. C Single cortical feeder, absence of cortical draining vein, drainаgе only towards subependymal system. D Cortical and perforating feeders with expected cortical and subpendymal draining veins. E Possibility of reversed draining system (hitherto unobserved)
76
3. Pathological Considerations
The nidus may be composed of a single or of multiple compartments. These compartments are, however, not anatomical entities. They represent hemodynamic units and this may best be exemplified _as follows: j If angiography by contrast injection into the feed-' ing branches arising from АСА, MCA and PCA shows equal filling of the entire AVM there is no dominance of any system. Each vessel must have equal flow pressure. This is a monocompartmental nidus. At operation, the clipping of one or two feeders does not change the volume or the color of the AVM (see Fig 3.12A-D). However, if in an AVM consisting of three systems of arterial supply А, В and C, and one system is dominant, for example A, then the clipping of the A-system is followed by partial or total collapse and color change (to blue) of the AVM, only for it to refill_and to turn red once more. This happens because the В and С systems are no longer dominanted by the A system pressure. For the operation to be successful both the В and С systems must also be eliminated (see Fig 6.17, Chapter 6). If, after clipping of the A-system a part of the AVM is collapsed and remains collapsed and blue, whereas other smaller or larger parts of the AVM remain red and turgid, this signifies the presence of multiple compartments or even multiple niduses. These may be confluent or may be separated by small nonfunctional or even functional brain parenchyma. Every neurosurgeon will recall that after most operations for AVM it is possible to describe the real construction of the lesion while in a few cases the picture remains confusing. The complexity of composition of AVMs can be enormous. Only superselective angiography with temporary balloon occlusion of individual feeders may provide the neurosurgeon with the necessary information concerning the actual angioarchitecture of AVMs. Interventional neuroradiologists are already using this technique in AVM patients who are candidates for embolization. It should as readily be used for the patients who cannot be embolized, but require operation. Although far more detailed knowledge is yet required it is helpful for the surgeon to know that the following constructions of AVMs are possible: 1. Single compact nidus a. monocompartmental, b. multicompartmental. 2. Multiple compact niduses Each of the niduses may be: a. monocompartmental, b. multicompartmental.
References p. 382
Also, the multiple compact niduses may be located very close together (this is more frequent or they may be located at a large distance from each other (even within another hemisphere, or combined supra- and infratentorial) see Fig 3.193.23. We hope that MRI might yet provide us with more information, especially in those cases belonging to the group of multiple compact niduses, as to whether there is functional brain parenchyma between the niduses. In one of our patients (see Fig 3.21A-H), a large left parietooccipital AVM received feeders from anterior, middle and posterior cerebral arteries as well as through dural-pia^ collateral arteries. MRI in this case showed a large compact AVM without intervening brain tissue The right handed patient had full neurologica function with regard to speech, reading etc. Am attempt at operation would cause her neurological deficit.
Compact and Diffuse Lesions The generally accepted view is that AVMs are usually quite compact with no (or a minimum of normal brain tissue between the pathologic^ loops of the malformation. There would be nc normal brain architecture or capillary bed within the lesion. Residual brain tissue is scarred by gliosis and ma;. contain hemosiderin deposits and calcification Adjacent to the lesion the brain tissue is sometimes also changed, and a separation between normal tissue and AVM may be created by hematoma, cyst or gliosis. The adjacent cortex may b; atrophic and is sometimes functional and sometimes not. This describes a compact AVM havin; single or multiple compartments. However, surgical experience shows that AVMs may differ considerably from this typical description. — There are (even large) AVMs without any atrophy of the adjacent cortex and having nc changes of arachnoidal, cortical, or subcortict layers. — There are AVMs without gliotic changes, without gliotic cleavage around the lesion, withou: pseudocapsule or matrix, but just normal surrounding brain tissue. — There are angiographically well-documente; cases with "non-compact" (or more proper!) diffuse AVMs which are scattered throughou: lobes, one or both hemisphere or even bilaterally in the deep gray matter. In two of our owr cases there were no connections visible between pathological arteries and pathologica veins (see Fig 3.24).
References p. 382
Compact and Diffuse Lesions
77
Fig3.19A-l This 16 year old female patient suffered a stroke and CT showed a large right frontal hematoma which was removed in another hospital An AVM was seen and left in place. A-B Preoperative CT showed cortical-subcortical AVM in the right frontal opercular area extending to the frontal horn.
C-D Right frontal carotid angiogram showed the size and extent of the AVM. The feeding arteries arose from M2 and A2 and supplied the cortical portion of the nidus. A1 branches supplied the subcortical portion of the nidus. i E Lateral view of arterial phase. F Unusually large single vein draining the cortical nidus towards the vein of Labbe. The subcortical nidus drained to the internal cerebral vein via subependymal veins (D). The AVM was completely removed. Fig 3.19 G—I ^
78
3. Pathological Considerations
References p. 382
Fig 3.19G-I Postoperative angiography showed norma' sized middle cerebral artery and anterior cerebral artery as I well as M1 and A1 perforators (G-H). The displacement o' the anterior cerebral artery to the right was due to right frontal atrophy as seen on CT (I). The postoperative course | was uneventful.
References p. 382
Compact and Diffuse Lesions
79
Fig3.20A-D
A--B A 7 year old boy presented with subarachnoid hemorrhage. Vertebral angiography showed an AVM composed of 2 niduses located in the left mediobasal occipital Iobe. Each nidus drained into a different venous system.
Fig 3.20C-D Postoperative angiography and CT after complete removal of the lesion. Preoperative quadrantanopia remained unchanged.
80
3. Pathological Considerations
Fig3.21A-H This 29 year old fema patient presented with chronic headache, cardiac murmur and epileptic seizure. CT (A) and MR (B) showed a giant m formation involving not only the left parietal lobe but also adjacent structures and the corpus callosum. С Left carotid angiogram showed multiple niduses supplied by M1 , M2 M3 branches. The A1 is poorly seen
Compact and Diffuse Lesions
81
82
3. Pathological Considerations
References p. 382j Fig 3.22A-E A A compact AVM at the end ofj the left insula is seen on carotid angiography in a 32 year old patient. В Diffuse type AVM scattered within the left occipital lobe is seen on vertebral angiography The insular AVM is also demcr-strated to be filled through collaterals. Inoperable case! C-Е CT fails to disclose whether there was a single largei nidus or multiple niduses.
Compact and Diffuse Lesions
83
F i g 3.23A-E Large right parietooccipital dorsolateral (A-C) and mediobasal (B-D) AVM with multiple niduses (arrow). The malformation had a dural component supplied by occipital and middle meningeal branches (E). Note absence of saraight sinus. This 55 year old female with mitral stenosis died of a heart infarct following completion of surgery (see cnapter Complications, Vol. Ill B).
84
3. Pathological Considerations
References p. 36:
Fig 3.24A-C
A-B Left carotid angiogram showed a diffuse AVM т frontoparietal paramedian area in a 25 year old male. С Vertebral angiogram showed a further nidus located posterior to the first. Note absence of straight sinus Inoperable case.
Sizes of AVM
References p. 382
85
Sizes, Shapes, and Elements of AVMs Sizes of AVM AVMs may vary enormously in size and the following types may be described: 1. Occult Not seen on angiography, not found at surgery and not demon strated pathologically but assumed present in cases of otherwise unexplained cerebral hemorrhage particularly in young, normotensive patients. 2. Cryptic Invisible on angiography, invisible at surgery. They may be recognized by histological examination if the hematoma is carefully removed and not sucked away. 5. Micro Just visible on angiography, 0.5-1 cm sometimes only as an abnormal
arteriole without draining veins. Sometimes only an abnormal draining vein is seen and the feeding vessels remain undetectable. At other times tiny lesions with classical appearance = pathological arterioles and pathological draining veins. Often invisible to the surgeon. 1-2 cm. 4. Small 5. Moderate 2-4 cm. 46 cm. > 6 6. Large cm. 7. Giant In the latter four groups the arterial component may be more dilated elongated, and tortuous, and therefore more impressive. Alternatively, the venous component may predominate or both may be similar in size and form (8 cases) (Figs 3.25-3.32).
86
3. Pathological Considerations
References p. 382
D Fig 3.26A-D A Left carotid angiography of an 18 year old female shows small AVM supplied by M1 and M2 feeding arteries. Location] is lateral to the caudate nucleus (arrow). В In the later phase, the deep drainage towards the internal cerebral vein is seen (arrow). The AVM could be completely! removed. C-D Preoperative (C) and postoperative (D) CT. The postoperative course was uneventful.
Sizes of AVM
88
3. Pathological Considerations
References p. 38Г
Fig 3.28A-C This 25 year old male patient presenting with subarachnoid and intraventricular hemorrhages. A-B Right carotid angiography demonstrated a small AVM associated with an aneurysm. The AVM is located within • right trigone (arrow). Drainage of the AVM occurs through subependymal veins into the galenic vein. The AVM, wh was compressed by hematoma, was removed through an interhemispheric transcallosal approach. The postopera: course was uneventful. Visual field was preserved. С СТ 7 years after removal of the AVM.
References p. 382
Sizes of AVM
89
Fig 3.29A-C An 8 year old boy presented with subarachnoid hemorrhage. A "Coronal CT showed a small enhancing lesion on the superolateral corner of the left trigone (arrow). В The postoperative coronal CT showed the interhemispheric approach through cingular gyrus to the trigone (arrow). The malformation was completely removed. This approach was chosen in order to avoid any parenchymal damage to the dorsolateral left parietal cortex. С The small AVM was only visible in the arterial phase of left carotid angiogram (arrow). The venous drainage was invis-ible. The postoperative course was uneventful. The visual field was preserved.
Fig 3.30A-B This 23 year old female patient presented with a right parietal hematoma. Carotid angiogram showed a bar ely visible (arrow) AVM. Draining veins were not visible. The AVM and the hematoma were removed by a lateral approach through the deep end of the right lateral Sylvian fissure. Preoperative left hemiplegia improved remarkably, whereas homonymous hemianopia remained unchanged. В Postoperative angiography.
90
3. Pathological Considerations
References p. 382
Fig3.31A-D A A 60 year old male patient presented with subarachnoid hemorrhage and Parinaud syndrome had a small enhancir: nodule located over the left superior colliculus shown on CT (white arrow). В Postoperative CT 2 months after removal of the lesion. C-D Frontal and lateral vertebral angiography showed a barely visible nidus (black and white arrow) with draining veir On lateral vertebral angiography only early filling of the v. Galen and the straight sinus was seen. The 5 x 5 mm AVM was explored and removed through a supracerebellar approach. No additional neurological deficit after operation. Total disappearance of Parinaud syndrome within 6 months.
References p. 382
Sizes of AVM
91
' Fig 3.32A-D This 14 year old boy had subarachnoid hemorrhage. A Carotid and lateral vertebral angiography were normal. AP vertebral angiography showes a small nidus with an early draining vein located over the left dorsal mesencephalon (arrow). Surgery confirmed a small AVM located over the left | superior colliculus. The AVM was radically removed. В Postoperative vertebral angiography. С Preoperative CT showed a small enhancing lesion in the area of the left superior colliculus (arrow). D The postoperative (CT) showed no parenchymal defect in the mesencephalon. The postoperative course was uneventful. No Parinaud syndrome.
92
3. Pathological Considerations
References p. 3
Shape The classically described AVM as a pyramidal, conical or wedge shaped lesion occurs in only about 40% of cases. Their appearance as a transcerebral dissecting structure is always very impressive and therefore frequently used for illustrations. In reality most AVMs, both giant and small have an amorphous, irregular, ameboid shape. They may be described as being more spheroid, oval, globular or striplike, sometimes likened to a bag of worms, a head of a Medusa, or spiderlike. Such literary descriptions express the fears of the neurosurgeon and do not contribute to solving the problem as to how such a lesion can be properly removed. For surgical treatment new perspectives are necessary. We have to analyze the subject in a different way, studying the feeding arteries and draining veins with more attention, comparing the compactness or diffuseness of the lesions, and trying to understand the concepts of "nidus" and "compartments" (Figs 3.33-3.43).
Fig 3.33A-C Right frontal paramedian cortical-subcortical AVM with typical pyramidal shape. Feeding vessels arosr from M3 and A3 as well as from M1 (A-B). The drainage occurred towards an ascending superficial cortical vein as we as through the dilated thalamostriate vein associated with a varix. The internal cerebral vein (C) was hugely dilatec Stenosis of straight sinus. This 35 year old female refused surgery.
References p. 382
Shape
93
Fg3.34A-B
A On frontal view of a right carotid angiogram, the typical pyramidal shape of a parietal cortical-subcortical AVM were seen. Multiple niduses were also visible. The feeding arteries arose from M1, M3 and M4. The AVM drained into both the superficial and deep venous systems. В A lateral angiogram showed a different shape from the frontal view. This was explained by the fact that the AVM was located entirely within the postcentral sulcus. Absence of the straight sinus. This 43 year old male refused surgery.
94
3. Pathological Considerations
A-B Right polar and mediobasal temporal AVM shown on carotid (A) and vertebral angiography (B) with a plexiform appearance of the nidus. The drainaging veins appeared in the late phase of angiography. С СТ showed the exact location and extension of the AVM (arrows). D Postoperative CT. The postoperative course was uneventful in a 29 year old female.
References p. 382
Shape
95
Fig 3.37A-B An unusually shaped plexiform type AVM in the right temporal polar area. A Preoperative angiography. Note pathological vessels with microaneurysms at the origin of participating branches of the transit vessels. B Postoperative angiography showed normal shaped temporal and anterior choroidal arteries. The postoperative course was uneventful in this 30 year old female.
Fig 3.38A-B A 39 year old female presented with chronic headaches and occasional Jacksonian attacks, but no neurological deficit. Left carotid angiogram (A-B) showed dilated M3 and M4 branches supplying a diffuse type AVM of the entire parietal lobe. Any attempt to remove this cortical-subcortical lesion probably would have been followed by Gerst-mann's syndrome. Radiation therapy was refused by the family of the patient. This case has been followed for 12 years as an untreated case. She continues to be plagued by headaches and seizures.
96
3. Pathological Considerations
Fig 3.39A-C This 53 year old patient presented with epi leptic seizures. Right carotid angiogram showed a diffuse AVM scattered within the entire frontal lobe. Inoperable.
Shape
Fig 3.40A-E A 53 year old male patient with right occipital hematoma. Preoperative CT (A), postoperative CT (B). Vertebral angiography (C) showed a dorsal occipital moderatesized AVM (D). Varicose veins drained to the transverse sinus (E). Remarkable in this case was the dilatation of the entire artery of the angular gyrus. The postoperative course was uneventful. The preoperative homonymous hemianopia remained unchanged.
97
98
3. Pathological Considerations
References p.
Shape
99
100
3. Pathological Considerations
References p.
Fig3.43A-B
A This 43 year old patient with cerebellar symptoms progressively disabled and finally bedridden. Vertebral angiography showed a giant AVM of the left cerebelar hemisphere. В On frontal vertebral angiography involvement of the i cerebellar hemisphere was seen as well a varicose dis tation of right cerebellar veins. The lesion could be completely removed in a one stage operation. However.the patient died due to bilateral parietal epidural hematoma which could not be recognized in time. CT-scan was not available in 1974 (see chapter Surgical results, Vol. III B
Pure Fistulous AVM More important is the recognition of the construction of the nidus, i.e. if it is plexiform, mixed plexiform and fistulous or pure fistulous. The following cases (Figs 3.44-3.53) demonstrate pure fistulous type AVMs.
Fig 3.44 Fistula between the middle cerebral artery ( 1 ) and the vein of Labbe (2) (see Fig 82a, p. 143. Yasargil. G. M.: Microsurgery Applied to Neurosurgery. Thieme, Stuttgart 1969).
References p. 378
Fig 3.45A Direct A-V fistula between A3 segment of pericallosal artery and inferior sagittal sinus with drainage to the vein of Galen. (From Smith, R. R., A. F. Haerer, W. F. Russell: Vascular Malformations and Fistulas of the Brain. Raven, New York 1982.)
Shape
101
В Cerebral angiography (lateral images) showed left parietotemporal arteriovenous malformation supplied by a dilated branch of the sylvian bifurcation and draining into the lateral sinus: possible participation of smaller arteries of the sylvian group. (From Stroobant, G., et al.: Neuro-chirurgie 32: 8 1 , 1986.)
Fig 3.46C, D Fig 3.46A-D A A-V fistula between a dilated temporal branch of the left middle cerebral artery and a markedly dilated vein of Labbe, and emptying mainly retrogradely into the rolandic vein (arrow). The connection to the transverse sinus was hypoplastic. В Postoperative angiography.
102 3. Pathological Considerations продолжение
Fig 3.46C Postoperative angiography: venous phase.
Fig3.47A-F A-C A dilated single opercular branch of the left middle cerebral artery with fistulous connection to a varicosely dilated superficial vein was seen in this 37 year old female patient.
References p. 382
Fig 3.46D Postoperative CT. Uneventful postoperative course in 60 year old male.
10
1. History
is entailed... How many less successful attempts, made by surgeons less familiar with intracranial procedures, have gone unrecorded may be left to the imagination." "The lesions, in short, when accidentally exposed by the surgeon, had better be left alone, and how muchjadiation may accomplish for them is undetermined though there are favourable experiences on record. So long ago as 1914 Wilhelm Magnus of Oslo unexpectedly exposed at operation a venous angioma of the left rolandic region, a decompression was made with the intention of treating the lesion with radium therapy which at that time was known favourably to influence cutaneous angiomas. After treatment, the decompression, which was bulging, ^^ecededj and the epileptiform attacks, from which the patient was suffering, became infrequent and finally disappeared ..." The publication of Reichert (1946) is unique, as he reported 15 cases of premotor vascular anomalies causing Jacksonian epilepsy, which were treated successfully by coagulation of the dural and pial vessels of the lesion (1935 to 1941).
References p. 369
Neurosurgical Treatment of Intracranial AVM Following the Introduction of Angiography (1930) As we have seen, surgical excision of AVMs was carried out between 1889 and 1930, both by general surgeons and neurosurgeons. Some of these cases met with success, others ended disastrously. After one or two bad results most surgeons did not risk further attempts at excision. With the advent of cerebral angiography the position began to change, for it became possible not only to diagnose the AVM but also to obtain some idea as to its location, its size and construction and the number of feeding and draining vessels. Angiography, however, was still somewhat primitive and the contrast material imperfect. Only a few angiographic demonstrations of cerebral AVMs were published before 1936 (Dott 1929. Lohr and Jacobi 1933, Moniz 1934 and 1951, Olivecrona and Tennis 1936). Dott provided the first demonstration of the angiographic aspects of cerebral AVMs at the Neurosurgical Conference in Stockholm in 1935. However, the full benefits of cerebral angiography came only with improved techniques which were not widely available until the 1950s. Olivecrona had a disappointing experience in 1923 when exploring for an infratentorial tumor (case 65). He was confronted with a highly vascular AVM and the patient died. In another case (66), Left carotid angiogram showing a frontoparietal AVM. In the monograph of Egas Moniz, "L'Angiographie Cerebrale", Masson, Paris 1934.
102
3. Pathological Considerations
Fig 3.46C
Postoperative angiography: venous phase.
Fig 3.47A-F
A-C A dilated single opercular branch of the left middle cerebral artery with fistulous connection to a varicosely dilated superficial vein was seen in this 37 year old female patient.
References p. SE2
Fig 3.46D Postoperative CT. Uneventful postoperative course in 60 year old male.
эпсез р. 382
r
ig 3.47D-F Postoperative angiography. Uneventful postoperative course.
Shape
103
104
3. Pathological Considerations
References p
Fig 3.48A-F
A-D A fistulous connection between the right anterior temporal artery and a varicosely dilated vein in the temporal pole area, emptied into the ascending frontal and parietal veins in this 35 year old man. The application of a clip on the anterior temporal branch was followed by immediate collapse of the malformation.
References p. 382
Shape
Fig 3.48E-F Postoperative angiography. The postoperative course was complicated by a local epidural hematoma. Full recovery after its removal. Fig 3.49A-H Because of one epileptic seizure and bruit, a CT (A) was performed on this 9 year old patient. It showed a large temporal malformation. В СТ after removal. С Left carotid angiogram shows mainly fistu-lous connections between three dilated branches of middle cerebral artery and a hugely dilated vein of Labbe. D Frontal view of vertebral angiogram showed dilatation of P1 and P2 segments, and the posterior cerebral artery giving off dilated terminal branches to the malformation. The smaller plexiform portion of the AVM was visible only in this view. See also Fig 5.3.
105
106
3. Pathological Considerations
References p. 382
Fig 3.49E The venous phase of vertebral angiography showed varicose dilatation of the draining vein and the unusual fenestration of the torcular Herophili and the internal occipital vein. F-H Angiography performed 6 months after operation confirms the complete removal of the lesion. Note the normal size of the previously dilated draining veins but still dilated middle cerebral artery. Postoperative course was uneventful.
References p. 382
Shape
107
A B Fig 3.50A-B A-V fistula in a 3 year old boy. Vertebral angiography showed a fistulous connection between the basilar artery and the torcular HerophiliJThe available angiograms do not allow precise analysis of the fistula. Inoperable case.
f С
Fig 3.51 A-C In this 11 year old boy who presented with cerebellar symptoms, angiography showed an A-V fistula between the hugely dilated right superior cerebellar artery and the transverse sinus. The transverse sinus seems to be occluded bilaterally. The patient's family refused surgery. The patient died 3 years later.
References p. 382
Shape
107
-ig 3.50A-B A-V fistula in a 3 year old boy. Vertebral angiography showed a fistulous connection between the basilar artery and the torcular HerophilUThe available angiograms do not allow precise analysis of the fistula. Inoperable case.
Fig 3.51 A-C In this 11 year old boy who presented with cerebellar symptoms, angiography showed an A-V fistula between the hugely dilated right superior cerebellar artery and the transverse sinus. The transverse sinus seems to be occluded bilaterally. The patient's family refused surgery. The patient died 3 years later.
108
3. Pathological Considerations
References p. 382
Fig 3.52A-H
A Because of trigeminal neuralgia CT was performed on this 34 year old nurse. It showed an AVM in the left cerebellopontine angle (arrow). В Postoperative CT.
C - Е Vertebral angiography demonstrated fistulous connections between lateral branches of the left superior cerebellar artery and a dilated AICA and the petrosal vein. The petrosal vein emptied through an unusual vein into the straight sinus. F-H Angiography performed 1 . 5 years after operation showed elimination of the fistulae. Postoperative course was uneventful. She married and had 2 children.
References p. 382 Fig 3.52
Shape
109
110
3. Pathological Considerations
References p. 382
Fig 3.53A-G An 18 year old female presented with symptoms of occlusive hydrocephalus. CT showed a dilated vein of Galen (A). В Postoperative CT showed a collapsed vein of Galen. C-Е 4-vessel angiography demonstrated a single fistula between a dilated left posterior cerebral artery and the vein of Galen.
Elements of an AVM
References p. 382
111
Fig 3.53F-G Carotid and vertebral angiography performed 6 months after operation showed elimination of the fistula and the preserved slightly dilated posterior cerebral artery. Postoperative course was uneventful. The visual field was preserved.
Elements of an AVM
Table 3.9
Frequency of involvement by given arteries Left
Arterial Feeders Feeding arteries to the malformation are derived r'rom 5 main groups^ of arteries in the supratento-rial compartment - the anterior, middle, and pos-terior cerebral arteries, the perforating branches of these respective arteries, and the choroidal arteries. Similarly, infratentorial AVMs may be fed from the superior, anterior inferior, and posterior inferior cerebellar arteries, perforating branches of these arteries, and perforating arteries of the basilar and vertebral arteries. Dural branches of the external carotid, internal carotid, and vertebral arteries also contribute feeding _arteries to AVMs.__________________ As any given AVM can derive its feeding arteries from a single artery or a number of arteries there are over 60 possible combinations of feeding vessels for that lesion (Table 3.9).
Right
Total
ACA
85
93
178
MCA
95
99
194
PCA
111
85
196
AchoA
12
10
22
SCA
28
28
56
AICA
19
15
34
PICA
30
19
49
(See Chapter 6)
Cerebral arteries may be related to a malformation in one of three ways: as a terminal feeding artery, a transit (partially participating) feeding artery, or as an artery en passage (non-participating) non-feeding artery (Figs 3.54-3.56).
112
3. Pathological Considerations
References p. 381 продолжение
Fig 3.54 Artist's drawing of the different types of vessels in the vicinity of an AVM which can be recognized only by microsurgical dissection or possibly by superselective angiographic mapping. A terminal artery ends in the nidus (a),a transit artery participating in the supply of the AVM through small terminal branches also gives branches to the normal brain (b), a transit artery following a route close around the AVM but without sending branches to the AVM (c), a single draining vein dividing into 2 branches (d).
Terminal Artery Arteries which terminate directly in the AVM may arise as far proximal as the first segments of the anterior, middle or posterior cerebral arteries, or as distal as the fourth or fifth branchings of these vessels. Marked dilatation and tortuosity of the feeding arteries may give the parent trunks a pathological appearance whereas only branches of these arteries are true terminal arteries. It has been noted on angiography that these large arteries often decrease in caliber following excision of the lesions. Transit Artery with Participation
These arteries are usually enlarged and seem to enter the malformation. In fact, they give off side branches which feed the malformation and they then continue on to supply normal brain beyond. These must be traced to the point where actual branches enter the malformation before definitive ligation is undertaken.
Transit Artery without Participation
These arteries are not enlarged but are running in the vicinity of the AVM and simply share a sulcus or gyms with the AVM and appear to be part of the lesion. They can be completely separated from the AVM. Although superselective angiography has improved preoperative recognition of the types of arteries involved, the decision must often be madeduring operation as to which artery type is present (Figs 3.56-3.58).
References p. 382
Elements of an AVM
113
Fig 3.55A-I
A A large right insular AVM with 2 niduses. Preoperatively it was difficult to understand the true construction of the AVM. B On carotid angiography the middle cerbral artery and its branches seemed to end within the convolutions of the AVM. No distal branches were visible. C Vertebral angiography showed a second nidus with significant dilatation of posterior cerebral artery branches.
Fig 3.55D-I
114
3. Pathological Considerations
References p. 3£
'References p. 382
r
ig 3.55H-I
Pre- and postoperative CT.
Elements of an AVM
115
116
3. Pathological Considerations
Fig 3.56A-C Construction of AVMs. Pure fistulous (A), mixed fistulous plexiform (B) and plexiform (C).
References p. 382
Fig 3.57A-C Further variations of AVMs. A Single large terminal feeder - multiple veins. В Multiple feeders - single vein. С Multiple feeders - multiple veins.
Elements of an AVM
117
118
3. Pathological Considerations
References p. 38*
Fig 3.58 An AVM with 2 transit branches supplying terminal branches to the AVM. A transit artery located on the surface and being therefore immediately recognizable (a), a transit artery looping deeply into a sulcus and giving termin; branches to the AVM in the depth of the sulcus and thus being unrecognized {b} without precise dissection.
Venous Drainage A single large vein often forms the main drainage of an AVM. Drainage starts in the center or toward the_apex of the lesion with the vascular channels of the AVM gradually coalescing into a large vein which finally drains into one of the venous sinuses. The large draining vein is frequently dilated as it emerges from the AVM but then ta pers distally as it courses toward the sinus. In such cases, the drainage is reminiscent of a venous malformation with several veins draining into a large dilated vein. The vein is thus comma shaped with a large origin and a gradual loss of caliber distally (Figs 3.59-3.68). Multiple draining veins may represent one of two configurations. First the large draining vein may divide as it emerges from the nidus of the lesion and the separate branches course toward one sinus or take different directions and drain into different sinuses, such as the superior sagittal and transverse sinuses. Secondly, there may be two or more distinct draining veins, perhaps draining different niduses of the lesion or related in some other way to its internal architecture. Again the course of the multiple veins may be toward one or more collecting sinuses.
Draining vessels are usually divided in to .superficial groups which drain in the sagittal, sphenopari-etal, cavernous, transverse and sigmoid sinuses and deep groups which pass to the subependymal collecting system and subsequently into the internal cerebral veins, basal vein of Rosenthal, internal occipital vein, into the vein of Galen and hence into the straight sinus and torcular or petro-sal sinuses.
Elements of an AVM
References p. 382 Fig 3.59A-B Observed variations of venous drainage. Single draining vein with varix (A) and without varix (B).
A
119
120
3. Pathological Considerations
References p. 38J
Fig 3.60 Artistic drawing of observed variations of supe" ficial and deep draining veins.
Fig 3.61A-B This 40 year old female dentist with a left frontobasal AVM presented with subaractinoid hemorrhage. A-B Note the large main draining vein dividing into a frontal ascending and Sylvian branch.
, References p. 382
Elements of an AVM
121
Fig 3.62C-G
122
3. Pathological Considerations
References p. 382 Fig 3.62C Postoperative angiography confirmed radical removal. D Preoperative MRI. E Postoperative MRI.
References p. 382
Fig3.62F-G Artist's drawing. The AVM was located in the medial surface of the superior temporal gyrus which was not precisely localized by CT or MRI.
Elements of an AVM
123
G
124
3. Pathological Considerations
References p. 382 I
Fig 3.63A-C A 16 year old female patient presented wit*subarachnoid hemorrhage. A-B Carotid angiography showed a left posterior front AVM with a single comma shaped draining vein. С Postoperative angiography. The postoperative course was uneventful.
Elements of an AVM
References p. 382
- : 3.64A-C
Left insular AVM with plexiform
I -3.
A arterial phase. B Single draining vein (of Labbe). C The malformation was completely removed. The postoperative course was uneventful in this 42 year old male.
125
126
3. Pathological Considerations
References p. 382
Fig 3.65A-D A 22 year old female patient with a right parietooccipital cortical-subcortical AVM. Carotid (A) and vertebral (B) angiography. Note the single draining ascending vein. Preoperative (C) and postoperative (D) CT. The malfo--mation was completely removed with an uneventful recovery.
References p. 382
Elements of an AVM
127
Fg 3.66A-B Small left AVM of the head of the caudate nucleus. This 62 year old female refused surgery after present-irg with subarachnoid hemorrhage. A single draining subependymal vein was seen,
:
: 3.67A-D A 36 year old female with a right frontoopercular AVM had a single subarachnoid hemorrhage. A - B Preoperative angiography showed a bizarre venous drainage. Note the single vein.
Fig 3.67C, D
128
3. Pathological Considerations
References p. 382 Fig 3.67C-D Postoperative angiography. Uneventful postoperative course.
:
eferences p. 382
Elements of an AVM
129
3.68A-B This right frontoopercular AVM with a single draining vein, was seen in a 16 year old girl who presented subarachnoid hemorrhage. Uneventful postoperative course.
Posterior fossa AVMs tend to drain toward the v. Galeni or tentorium if they lie in the upper half of the fossa. Those that lie on the ventral cerebellar surface drain toward the petrosal sinuses and those occupying the lower half of the fossa may even drain superiorly toward tentorium or anteriorly toward the petrosal sinuses or in a combined fashion (Fig 3.69). In most cases drainage seems to follow the expected cortical or subcortical vein in the area, but at times bizarre routes of drainage are noted, reflecting either preexisting embryonic channels or perhaps normal small transcerebral venous sys-
tems, which have been expanded by the presence ofjthe malformation/Thus a superficial AVM may at times drain only into the deep venous system, while a deeply placed AVM may unexpectedly drain outward to the superficial venous system and ultimately into the sagittal or transverse sinuses. A lesion virtually adjacent to the superior sagittal sinus may drain into the transverse sinus (Fig 3.74A—B), a posttemporal lesion can drain upward into the superior sagittal sinus (Fig 3.76), and a frontal lesion drain toward the occipital pole and vice versa (Figs 3.73 and 3.78).
130
3. Pathological Considerations
Fig 3.69A-D
A-B A 20 year old female patient presented with a right upper paravermian AVM located in the anterior quadrangular lobe. Note the single dilated draining superior cerebellar vein. C-D Postoperative angiography. The postoperative course was uneventful.
References p. 382
Elements of an AVM
131
Fig 3.70A-G Artistic drawing of some expected (usual) .enous drainage of AVMs in various locations: Frontal and sarietal AVMs usually drain into superior sagittal sinus (A). Cingular-callosal AVMs drain into superior and inferior sagittal sinus and via subependymal veins to internal cereига! veins (B). Callosal AVMs drain into septal and internal cerebral vein (C).
Fig3.70D-G
132
3. Pathological Considerations
Fig 3.70D-E Parietal AVMs may drain into superior sagittal sinus (D) or in transverse sinus (E). F-G Occipital AVMs may drain into transverse sinus (F) or into superior sagittal sinus (G).
References p. 382
Elements of an AVM
References p. 382
133
В
Fig 3.71A-B Artistic drawing of unexpected (unusual) venous drainage of AVMs. Occipital AVM drains anteriorly into cavernous sinus (A). Frontal AVM drains posteriorly into posterior part of superior sagittal sinus (see also Fig 3.73).
Fig 3.72 The well known drawing from the publication of Steinheil 1895 showing an unusual drainage of a frontal AVM.
\
\
134
3. Pathological Considerations
References p. Fig 3.73 Right frontobasal AVM with unusual drainage. The postoperative course was uneventful.
Fig 3.74A-B This right frontal paramedian AVM was found in a 43 year old patient presenting with epileptic seizures (A-B). Note the unusual course of draining vein towards vein of Labbe instead of towards the superior sagittal sinus. The postoperative course was complicated by a local hematoma. Full recovery after 2nd operation.
eferences p. 382
Elements of an AVM
Fig 3.75A-B This AVM of the right paracentral cingular area in a 28 year old male had unexpected drainage to the deep venous system via a thalamostriate vein. Successful removal.
Fig 3.76A-B This left posterolateral temporal AVM in a 53 year old male did not drain as expected, into the sigmoid sinus but rather showed flow reversal through the vein of Labbe to superior sagittal sinus. Successful removal.
136
3. Pathological Considerations
References p.
Fig 3.77A-B A 29 year old male had an intrinsic mesencephalic AVM on vertebral angiography with an unusual course of the draining vein. Inoperable case because of its intrinsic nature.
Fig 3.78A-G This 24 year old student had left occipital headaches and epileptic seizures and showed a left occipital AVM on left carotid angiography (A). B-C Carotid angiography showed a very unusual superficial draining vein ascending retrogradely from occipital to pre-central area.
References p. 382
Elements of an AVM Fig 3.78D-F MRI showed a left occipital lateral AVM. The operation disclosed 2 niduses. G Postoperative CT 1 week after surgery. Visual field was preserved.
137
138
3. Pathological Considerations
References p. 38?
Sinuses
Table 3.10
Just as the venous drainage of any given AVM may be quite anomalous and unexpected, so the sinuses themselves may be altered in one or more of several ways. Flow directions may be abnormal owing to increased pressure of the arterial input of the AVM being reflected in the venous drainage, or to anomalous construction of the sinuses themselves. There may be agenesis or obliteration of the sigmoid, transverse, straight and even sagittal sinuses. With sinus obliteration (in cases with vein of Galen or callosal, thalamic, parathalamic, occipital or cerebellar AVM) embryonic connections which normally involute may persist (Agee and Greer 1967, Handa et al. 1975, Dobbelaere et al. 1979, Vinuela et al. 1985, Jomin et al. 1985). There is frequently a communication between the vein of Galen and the superior sagittal sinus when the straight sinus is occluded (Table 3.10, see also Table 9.2 in Vol. Ill B). (See also Figs 3.1163.126 and Chapter 6, Figs 6.4, 6.5.) As with any high pressure intracranial fistula, flow may be reversed in the veins and reflux back through the sinuses rather than continue forward. Flow reversal has been demonstrated in the straight, transverse and sagittal sinuses (see Fig 4.5A-B and pages 54, 55, 193-211, 217, 224 and Vol. Ill B, Table 9.2).
sss
154
ISS
24
Galenic
176
Transverse
62
Sigmoid
15
Petrosal
31
Sphenoid
13
Cavernous
9
Frequency of involvement by given sinuses
Interestingly, despite the frequent involvement of the ophthalmic venous system with carotid arter\ cavernous sinus fistula, involvement of this venousystem has not been seen in a review of over 80 angiograms of AVMs seen at the University of Zurich in the last 30 years, even when the transverse and sigmoid sinuses were occluded bilaterj ally and venous drainage went through the cavernous sinus. There are only 7 cases in the literature attesting to the rare involvement of ophthalmic I veins in intracranial AVM (Cecile et al. 1971, one case, Dobbelaere et al. 1979, 4 cases, Huang et al. 1984, one case). (See pages 242, 244 and 280.)
Enlargement, Growth, and Regrowth of AVMs Progressive enlargement of AVMs has been referred to in pertinent literature (Olivecrona and Riives 1948, Shenkin et al. 1948, Norlen 1949, Sorgo 1949, Potter 1955, Tonnis and Schiefer 1955, Paterson and McKissock 1956, Padget 1956, Decker and Freislederer 1957, Anderson and Korbin 1958, Hook and Johanson 1958, Perria and Crudeli 1958, Huber 1959, Kaplan et al. 1961, McCormick 1969, 1978, 1985, Kelly et al. 1969, Porter and Bull 1969, Lakke 1970, Isfort 1972, Sundbarg et al. 1972, Waltimo 1973a,b, Spetzler and Wilson 1975, Krayenbuhl 1977, Parkinson and Bachers 1980, Stein and Wolpert 1980, Delitala et al. 1982, Huber 1982, Peeters 1982, Luessenhop 1984, Stein 1984, Wilkins 1985).
In 1948, Olivecrona and Riives reported a 31-yearold patient in whom a second angiogram performed 10 years after the first, showed that the volume of the AVM had increased. In the same year Shenkin et al. (1948) reported a case in which the documented growth interval was 16 years. Tonnis and Schiefer (1955) reported on a 25-yearold patient, who was operated on for a left frontolateral AVM in 1938; two feeding arteries were clipped and the red draining vein collapsed. Sixteen years later (1954) the angiogram showed a large AVM in the same location. Delitala et al. (1982) collected 37 cases from the literature and added one of his own, which showed in 1952 a small left temporal AVM; repeat angiography
References p. 383
Enlargement, Growth, and Regrowth of AVMs
139
Szepan (1977), rejecting the hypothesis of autonomous growth, contended that underlying the increase in size of an angioma is a vicious circle, namely, a disturbance of embryonal development with circulatory disturbance and consequent hemorrhage and thrombosis, together with degeneration of the surrounding zones with an ever-increasing growth of collateral vessels (secondary growth). The incidence of fully documented growth of AVMs in various series may represent only a small fraction of the actual prevalence of progressively enlarging lesions. Such figures as are available from studies of untreated cases are those of Luessenhop (1984) who described a series of 49 untreated patients with AVM. Of these, 51% enlarged, 6% became smaller, and 6% totally disappeared with time. Stein (1984b) mentioned that of 18 untreated patients followed up by serial angiography one third had lesions which enlarged, one third remained constant in size, and one third regressed.________________________ The two main theories put forward to explain enlargement of AVMs are those of the continuing effects of hemodynamic stress upon the thin walled, undifferentiated vessels forming the fistulous shunts (Hook and Johanson 1958, Kaplan et al. 1961, Waltimo 1973b), Huber 1976, Parkinson and Bachers 1980, see also Krayenbuhl 1977, Spetzler and Wilson 1975, Garretson 1985), and enlargement due to repeated, small, clinically silent hemorrhages (Paterson and McKissock 1956^Hamby 1958, Delitala et al. 1982). These hemorrhages would destroy surrounding supportive tissue and thereby allow further vascular dilatation and pseudoaneurysm formation in the malformation. Two other theories which have been considered are those of recruitment of vessels from previously uninvolved tissue (see McCormick 1984) and of autonomous growth of the AVM. Krayenbuhl noted that most patients had their first symptoms in early childhood and small lesions grew far more rapidly than large ones so that increased size of the AVM might be not so much a consequence of enlargement of congenitally pathological vessels but rather of actual growth. In common with Friede (1975) he subscribed to the view that either there was a congenital A-V shunt, the shunt stimulating abnormal growth of the pathological vessels, or that the abnormalities in the structure of the vessels were the cause of the growth, with the shunting merely incidental. Central to the whole concept of the growth of AVMs is the basic underlying cause of the initial development of the malformation. As noted
140
3. Pathological Considerations
above, despite some major flaws in the evidence (late onset of symptoms, absence of familial cases, rarity of associated lesions etc.), this is generally stated to be a congenital failure of development of capillaries at the 3 week embryo stage, thus allowing direct communication between arteries and veins. The poorly differentiated fistulous vessels may dilate and proliferate progressively and there is histopathological evidence to suggest that in many cases there is a lack of normal brain tissue between the folds of the malformation itself. Arteries entering the AVM are said to passively enlarge secondary to high flow volume from the low peripheral resistance of the shunt and the veins to dilate and become increasingly tortuous because of prolonged increase in venous pressure. Although we cannot offer any conclusive supportive evidence we would suggest, on the basis of our own findings, an alternative pathological mechanism to explain the etiology, character, progression and apparent regrowth of intracerebral AVMs. It is conceivable that AVMs result not from a congenital deficiency of capillaries but from an acquired disease involving pathological changes in vessels (starting with the capillaries) originally "programmed" to develop normally during early embryonic life. This process may begin in many cases during the 3rd week of embryogenesis but not become sufficiently widespread or of sufficient severity to produce effects until much later in life. The focal nature of most lesions is difficult to explain, but no more so than on a congenital basis. It would explain the rarity of all the usual associated features of congenital disease. It might also reasonably be held to explain the rarity of multiple lesions and the rarity and odd distribution of associated aneurysms in respect of traditional concepts of hemodynamics. One could suggest that the disease process remains active in some patients but relatively quiescent in others. Although hemodynamic factors and progressive gliosis of surrounding tissue should not be discounted as playing an active role in growth and regrowth and in producing clinical symptoms in cases of AVM, they may yet prove to be largely secondary phenomena in a primary disease process. The congenital aberrations which lead to the formation of telangiectatic lesions and cavernous angiomas are not difficult to appreciate, but a defect of capillary formation allowing direct and simple union of separate arterial and venous systems, even at crossing-points (Padget), is rather more difficult to comprehend. Tentative support for a theory which does not ascribe the characteristics of AVMs to a single
event early in embryogenesis may be gained by ye: more detailed angiographic study. Based on the analysis of the angiograms of the operated and non-operated patients of our serie-(500 cases), two main types and their subgroups o: AVM growth were distinguished:
Growth types of AVMs; 0 Enlargement @ Growth A. Pseudo-growth — incomplete angiographic evaluation (2 cases) — incomplete angiographic visualization (4 cases) — incomplete removal/regrowth (2 cases) B. True Growth (8 cases)
Enlargement In a group of patients with AVM not operated for I at least 5 years after the initial angiographic diag-1 nosis, or having been treated by radiation therapy. I repeat angiography disclosed enlargement of feeding arteries, draining veins or of associated aneurysms an^ varices, ranging from slight tc marked, in almost all cases. Enlargement of the AVM occurred, independent of the patients age as it was observed in both younger and older patients (Figs 3.79-3.81).
s'erences p. 383
Enlargement
141
Fig 3.79A-G CT (A) and carotid angiography (B-C) performed on a 10 year old girl with progressive left hemiparesis demonstrated a strio-capsular AVM. D-E Vertebral angiography showed the right thalamic extension of the lesion. Note the occlusion of the straight sinus С and F). Fig3.79F, G >•
142
3. Pathological Considerations
References p. 3?"
Fig 3.79F-G This inoperable AVM was irradiated in Boston. A repeat angiography performed 3 years later showec change in the size and shape the AVM.
Fig 3.80A-I A slowly growing left thalamic AVM in a 7 year old girl was found after she presented with epileptic seizures. A 1975. В 1977. С 1985. D Vertebral angiography showed the thalamic extension of the AVM.
Terences p. 383
Enlargement
143
E-F Note also the absence of the straight sinus (F) (arrow), and reversed flow through transcerebral channels.
Fig3.80G-l
144
3. Pathological Considerations
References p, :•
Fig 3.80G CT showed the location and extension of the malformation. The 18 year old patient shows progressive hemiparesis. This inoperable AVM was treated in 1977 with conventional radiation. H-l MRI performed 11 years later. Note the dilated contralateral parietal veins (I), due to the occlusion of the straight sinus seen on F.
^ferences p. 383
Enlargement
145
Fig 3.81A-F This 29 year old female patient first presented with subarachnoid hemorrhage in 1970. On right carotid angiography an AVM was found in the right striocapsular area (A). Note the varix on the basilar vein and stenosis of the galenic vein and straight sinus with collaterals to petrosal sinus (B). The patient received conventional radiation. 4 years later repeat carotid angiography (C-D) was performed because of slow but progressive mental deterioration. Angiography shows further growth of this plexiform type AVM as well as enlargement of the venous varix. E-F The growth and enlargement can also be appreciated on frontal views. 1970 (E), 1984 (F). The family refused surgery because the patient had chronic mental changes. This lesion could probably be removed with some risk of hemiparesis.
146
3. Pathological Considerations
Growth This type may be subdivided into two groups; namely "pseudo-growth", in which a variety of factors may stimulate or give on angiography the erroneous impression of growth, and "true growth".
Pseudo-Growth Incomplete Angiographic Evaluation Growth of an AVM may be simulated if the initial angiographic evaluation was incomplete and followed by incomplete removal of the AVM. This applies specifically to AVMs of the temporal, parietal and callosal or paracallosal areas which are usually located in the territories of the internal carotid and vertebro-basilar-posterior cerebral systems. In such cases the neurosurgeon may find and remove the entire AVM. However, if angiographic investigation was incomplete, there is the inherent danger that he will only remove l /i, Vz or 2 /з of the AVM. Repeat angiography performed either as a routine postoperative control or because of recurrence of symptoms will visualize the rest of the AVM, which may be of small or even larger size. Three cases of our own material belong to this group (Fig 3.82).
Fig 3.82A-C
A A 4 year old girl suffered from very severe headache, followed by an attack of unconsciousness lasting for several minutes. Lumbar puncture revealed bloody cerebro-spinal fluid. The right carotid angiogram showed barely discernible microangiomas (arrows). At exploration a huge intraventricular hematoma was evacuated (Dr. del Vivo) from the right lateral ventricle, and a small arterio-venous malformation was seen and removed from the floor of the right frontal horn (1969). Histological examination revealed an arteriovenous malformation. Postopera-tively, a left hemiparesis gradually disappeared. В 6 years later she suffered another hemorrhage, and a right brachial angiogram demonstrated multiple AVMs within the entire corpus callosum. The AVM and a large intracallosal hematoma were removed microsurgically. The postoperative course was uneventful. С Postoperative angiography 3 months later demonstrated that the malformation had been completely excised.
References p. 3fi
*cferences p. 383
Incomplete Visualization of the AVM In cases with large intracerebral hematomas which compress and displace the nidus of the AVM, complete angiographic evaluation may fail to reve al the actual size of the lesion. On surgical
Growth
147
exploration of such cases the hematoma and a portion of the AVM will be removed. However, other portions of the AVM may remain undiscovered and left in place. This was observed in 4 cases of the present series (Figs 3.83-3.85).
Fig 3.83A-D At the age of 14 years, this patient was operated abroad for a left temporal lobe hematoma which was removed. Histology showed an AVM. A-B 4 years later another subarachnoid hemorrhage occured. Angiography showed displacement of middle cerebral branches and a small plexiform tangle (arrow) of pathological arteries (A), as well as an umbrella shaped venous drainage (B). At the second operation a large hematoma was removed along with an AVM in side the superior temporal gyrus. The postoperative course was uneventful. Postoperative CT did not show any pathology. The patient was able to continue his studies. 4 years after the second operation another stroke occurred. C-D Carotid (C) and vertebral (D) angiog-raphy demonstrated a more posteriorly and medially located AVM in the paratrigonal area.
148
3. Pathological Considerations
References p. 383 • Fig3.84A-F This 26 year old enginersuffered a stroke. CT showed a right frontal hematoma (A). В СТ after removal of hematoma and or the AVM.
Fig 3.84C-D On carotid angiography the AVM exhibited unusual venous drainage. The patient fully recovered from a comatose condition but only partially, from a left sided hemiplegia. E-F 2 years later, a repeat angiogram showed tiny pathological vessels within the deep frontal white matter. We believe that this portion of the AVM was compressed by the hematoma and could not be recognized during surgery. We do not believe that this represents regrowth of the AVM. Further surgery is recommended but the patient is reluctant to accept it.
p. 383
Fig 3.85A-E A 24 year old male presented clinically with stroke. MRI showed a large right frontal hematoma (A). In a lower section, a small frontoopercular AVM was seen (B). C-D Arterial and venous phases of carotid angiography showed the compressed AVM with cortical and subependymal drainage. E The hematoma was removed and the compressed AVM located on the basal aspect of the hematoma was believed to have been eliminated. The postoperative course was uneventful. 4 weeks later angiography showed a residual AVM supplied by M1 feeders (E). His present situation is the same as the previous case.
Growth
149
150
3. Pathological Considerations
References p. 383^
Incomplete Removal or Regrowth of the AVM There are mainly two situations in which an AVM may be removed incompletely: 1) Portions of the AVM may be really hidden and thus inaccessible or 2) due to bipolar coagulation technique, the surgeon may dissect through the AVM, leaving some portions of it untouched. In a case with a right frontolateral subcortical AVM the lesion was believed completely removed. This was also confirmed by postoperative angiography, performed one week after operation. Three years later the patient presented with a new intracerebral hemorrhage, located in the area of the removed AVM. Angiography surprisingly revealed a large AVM in the identical location as the initial lesion (Fig 3.86). Two explanations may be given for this phenomenon:
Fig 3.86A-H
A-B This 17 year old female patient's right carotid angiogram revealed a wedged shaped AVM located in the fronta opercular area. It was supplied by arteries arising from M1 and M2 segments of the middle cerebral artery, as well as fror A1 and A2 segments of anterior cerebral artery. The venous drainage occured through a superficial ascending vein anc through the internal cerebral vein. The AVM was removed in 1977.
-erences p. 383
Growth
151
3.86C-D Angiography performed 10 days after operation seemed to show complete removal of the AVM.
Fig 3.86E-F 7 years later another subarachnoid hemorrhage occurred and repeat angiography showed, surprisingly, an AVM identical to that seen on the first angiogram.
Fig 3.86G, H
152
3. Pathological Considerations
References p. 383
Fig 3.86G-H Second operation was also uneventful and angiography (G) and CT (H) performed 4 months later, con firmed the radical removal. This case raises the question of whether there was a true regrowth of the rnalformatio or whether the first removal was incomplete.
References p. 383
Growth
Fig 3.87A-J A 13 year old girl presented with subarachnoid hemorrhage. CT showed an unusually located AVM on the medial surface of the right superior temporal gyrus extending towards the mediobasal temporal lobe (A). Carotid and vertebral angiography (B-D) confirmed the presence of an AVM. The AVM was removed through a sulcal approach. CT 1 week after surgery (E) was interpreted as normal. The repeat CT 6 months later however, showed a suspicious finding within the previous operative field (F).
Fig3.87G-J
153
154
3. Pathological Considerations
References p. 3el
Fig 3.87
This symptom-free patient underwent repeat angiography which showed a small AVM in the same location as before the operation with feeding arteries arising from M1, M2 and P2 segments (G-H). A second operation was performed and the AVM was removed.
Postoperative angiography (I-J) performed 9 months later showed complete disappearance of the AVM. We believe f in this case the AVM was not completely removed at the first operation, despite the fact that the first postoperative С failed to show any pathology. Remarkable in this case is the rapid growing or enlarging tendency of the AVM (at lea according to CT).
References p. 383
Growth
155
AVMs). AVM growth was proven in all cases by both CT and angiography. All cases were characterized angiographically by an increase in diameter of the vessels as well as by a numerical increase of the feeding arteries (Figs 3.88-3.90).
Fig 3.88A-F This 3 year old boy first presented with an episode of subarachnoid hemorrhage. Angiography performed in 1966 was normal (A-B).
Fig3.88C-F
156
3. Pathological Considerations
продолжение References p.
эгепсез р. 383
Growth
157
Fig 3.89A-F
A This 28 year old female patient had been admitted in 1963 at the age of 16 to the neurosurgical clinic of Bern because of a SAH. Left carotid angiography showed a small paracallosal AVM (arrows). No operation was performed. Several acute attacks of bilateral sciatica have occured. They usually cleared up quickly after bed rest but a severe attack followed 12 years later in 1975. The angiographic study by Prof. Huber of Bern, showed marked enlargement of the callosal-splenial and left parasplenial AVM (B-D).
Fig3.89C-F
158
3. Pathological Considerations
References p. 35'
References p. 383
Growth
159
Fig3.90E-l
160
3. Pathological Considerations
References p.
References p. 384
Spontaneous Thrombosis and Regression
161
Spontaneous Thrombosis and Regression of AVMs Spontaneous Thrombosis and Regression Altogether, some 50 cases of spontaneous total or partial regression of intracranial (cerebral and dural) AVMs have been reported over the past 40 years (Norlen 1949, Svien and Peserico 1960, Pecker et al. 1961, Castaigne et al. 1961, Fischer et al. 1969, Lakke 1970, Kushner and Alexander 1970, Abroms et al. 1971, Conforti 1971, Eisenmann et al. 1972, Sukoff et al. 1972, Kirn et al. 1973, Levine et al. 1973, Spetzler et al. 1974, Magidson and Weinberg 1976, Hansen and Soogard 1976, Kendall and Claveria 1976, Scott and Garrido 1977, Dyck 1977, Mabe and Furuse 1977, Bell et al. 1978, Sartor 1978, Endo et al. 1979, Leo et al. 1979, London and Enzmann 1981, Huber 1982, Omojola et al. 1982, Nehls and Pittmann 1982 (see Table I, p. 778), Wharen et al. 1982, Wakai et al. 1983 (see Table on p. 379), Mitnick et al. 1984, Stein 1984a,b, Pasqualin et al. 1985). The regression has been judged to be confirmed either by angiography or by isotope or CT scan. The exact incidence of spontaneous regression is uncertain, although Pasqualin et al. (1985) found total occlusion in 2.2% of their series of 180 intracranial AVMs. Stein (1984b) found that in his series, of the 10% of AVMs which remained unoper-ated, one third became smaller with time. Operative and autopsy findings of a totally throm-bosed AVM, which had been angiographically invisible, together with more recent CT scan evidence of thrombosed AVM (Kendall and Claveria 1976), suggest that, perhaps, spontaneous thrombosis and regression of intracranial AVMs is more common than formerly suspected. However, such findings usually relate to previously unsuspected lesions with no earlier angiographic evidence of their existence. It therefore remains uncertain as to whether these newly-found thrombosed lesions represent an endstage of some other form of regression or even a malformation which had undergone spontaneous occlusion during embryonic development. Spontaneous regressions of AVMs must be differentiated from those achieved by treatment aimed at thrombosis through the use of embolization, glue, ligation and radiotherapy. The difficulty in producing total occlusion of a large AVM by these means perhaps gives some clue as to why spontaneous total thrombosis does not occur more frequently. Pasqualin et al. (1985) concurs with the notion (Conforti 1971, Omojola et al. 1982) that spontaneous complete thrombosis is more likely to occur in small AVMs drained by a single vein. of AVMs.
Case reports are too few in number to draw any firm conclusions as to the distribution of AVMs within the brain or as to the distribution of feeding vessels to lesions undergoing spontaneous resolution. Most reported cases of spontaneous regression of AVM have occurred in adults between the ages of 30 and 60 and the time course for complete occlusion has varied from around 6 months to 21 years. In most instances the regression has been acute with no change in size of the lesion until apparently complete obliteration has occurred. Kushner and Alexander (1970) and Lakke (1970), however, have described gradual (angiographic) regression of intracranial AVMs. The exact mechanisms involved in spontaneous AVM regression are uncertain but the most common is almost certainly that of compression of the lesion (leading to acute intravascular thrombosis) from intracranial hemorrhage. Other possible mechanisms are included in Table 3.11 (see Pasqualin et al. 1985). Sukoff et al. (1972) described a case of spontaneous subtotal acute occlusion of a large AVM fed principally by the MCA. They speculated as to whether the underlying cause of the thrombosis was embolism or possibly atheroma in the MCA induced by hemodynamic changes in the vessel. There was no supportive evidence for either cause and it was felt that retrograde thrombosis from the AVM itself had possibly occluded the vessel. Table 3.11 Possible mechanisms underlying spontaneous regression of intracerebral AVMs 1. Acute thrombosis from intracranial hemorrhage. This may be due to compression from mass effect or edema, or to reduced flow secondary to vasospasm 2. Subacute thrombosis. This may be due to increased blood coaguability or turbulence or to alterations in flow - particularly in dural AVMs 3. Occlusion of feeding vessels from atheroma and embolism 4. Occlusion of draining veins and sinuses 5. Destruction of occult, cryptic and micro AVMs from hemorrhage
162
3. Pathological Considerations
A cautionary note on the interpretation of angiographic features suggesting regression of AVMs in the presence of SAH was recorded by London and Enzmann (1981). Vasospasm secondary to a bleed from one of multiple aneurysms coincidental to a large AVM led to transient changes in vessel caliber suggesting regression of the AVM. Repeat angiography after the vasospasm had resolved showed the AVM in its original form. We have seen one similar case (see Chapter 6, Fig 6.21). Although an AVM which has undergone spontaneous thrombosis/regression may be demonstrated as an incidental finding on CT, or may be clinically silent, those cases in whom thrombosis is secondary to a significant intracerebral bleed are likely to present at the time with the typical symptoms of raised intracranial pressure, focal neurological signs or epilepsy. [There is a high incidence of continuing epilepsy reported by several authors in cases of thromxbosed AVM (Wharen et al. 1982). The surgeon should not become complacent regarding the risk of continuing hemorrhage even after repeated angiography has suggested significant or total regression of an AVM. This is well shown in a case of Huber (1982) (p. 163). See case report (Fig 3.91). In our own series, frequently single thrombosed, white coloured vessels, and in 12 cases (3%), partial AVM thrombosis, have been seen at surgical exploration. There have been two cases among the unoperated group, of spontaneous total occlusion, demonstrated only angiographically. However, in one case the MR showed a persistent AVM (Fig 3.92). The management of seemingly totally thrombosed AVM seen on CT scan will depend upon the age and general condition of the patient, the site of the AVM within the brain and its surgical accessibility, the presence of intractable epilepsy and the angiographic findings. If the scan suggests total thrombosis and the AVM is invisible on angiography, then exploration and extirpation of the lesion to prevent recurrent bleeding seems unwarranted. ) Continuing epilepsy in the face of comprehensive j medical treatment may constitute grounds for excision of the lesion in appropriate cases.
References p. 3841
References p. 384
Spontaneous Thrombosis and Regression
Fig 3.91A-E This was an impressive case of total spontaneous regression of an occipital AVM as demonstrated on successive angiograms. Despite complete angio-graphic disappearance of the AVM, hemorrhage occurred. E CT scan. Massive intraventricular hemorrhage from angiographically invisible AVM containing calcifications. Progressive thrombosis involved a portion of the malformation. The non thrombosed part of lesion fed by the posterior cerebral artery was destroyed by hemorrhage (confirmed at necropsy) (case reported by Huber 1982).
163
164
3. Pathological Considerations
References p.
References p. 385
Multiple Cerebral AVMs
165
Multiple AVMs Even though AVMs are considered to be of developmental origin arising at an embryonic stage, which would make multiple lesions likely, there have been few reports of more than one intracranial AVM arising in any single patient. WyburnMason (1943) called attention to the coexistence of multiple arteriovenous lesions. Ferret and Nishioka mentioned 3 such cases in 1966 but did not elaborate further (angiomas other than true AVMs may have thus been included). Other reports were those of Voigt et al. (1973) and of Schlachter et al. (1980) who described 4 possible multifocal AVMs. In one case, however, a second cryptic lesion was assumed but not radiologically proven, and in 2 of the remaining cases there was no absolute proof that the demonstrated lesion did not represent a single large malformation. Other single case reports include those of Hook and Johanson (1958), Jellinger (1957), and Paterson and McKissock (1956). Tarnaki et al. (1971) described a single patient having AVMs of the scalp, dura, retina, cerebrum and posterior fossa treated by radiotherapy. As stressed by Schlachter et al. (1980), comprehensive neuroradiological investigation is essential to identify multiple lesions, but even then they may be missed if a lesion is partially thrombosed or compressed or is very small. Suspicion may be raised as to the presence of a second "occult" lesion by an area of enhancement or of unexplained atrophy with ventricular dilatation on the CT. Zellem and Buchheit (1985) noted a strong family history of cerebrovascular disease in their case, but were not able to show evidence of AVMs as a cause for cerebral hemorrhage in other members of the family. Multiple telangiectases are well known to occur in the autosomal dominant OslerWeber-Rendu disease but the only recorded cases of multiple anomalies of different types (e. g. combined telangiectasies, cavernoma and venous medullary malformation, medullary venous malformation with cryptic AVM within it) are those described by Huang et al. (1984) and McCormick (1984). McCormick (1985) described 6% of autopsy cases having multiple angiomas but the incidence of AVM among these is not stated.
Multiple Cerebral AVMs Hanieh et al. (1981) described a case of right frontal and left parietal AVM associated with subcutaneous vascular malformations in the hand. Berenstein (1981) reported on a case of angiographically proven bilateral thalamic AVM supplied by the lateral and medial lenticulostriate arteries. Stone et al. (1983) documented a single case of proven biparietal AVMs. Zellem and Buchheit (1985) reported a single case having 3 separate supratentorial AVMs (L frontal, L temporal, R temporal) confirmed angiographically, of which 2 were removed surgically. Multiple intracranial AVMs may be unilateral (within one hemisphere) or bilateral, or in the midline, such as in the corpus callosum. Treatment of multiple AVMs is essentially the same as for single lesions. Each must be regarded as a source of potential recurrent hemorrhage such that the aim should be complete obliteration of those lesions which are amenable to surgical excision or to transvascular occlusion. Of our own cases there were 15 patients (3.0%) of the total observed 500 cases: — Two patients with scattered diffuse AVMs in both hemispheres (Figs 3.93, 3.94), — Two patients with extensive bilateral strio-capsulo-thalamic AVMs (Figs 3.95, 3.96), — One case with left sided thalamic and orbital AVM (Fig 3.97), — One case with supra- and infratentorial parapontine and mesencephalic and orbital AVMs (only the infratentorial AVM could be operated) (Fig 3.98), — Two cases with combined supra- and infratentorial AVMs (Figs 3.99, 3.100), — One case with galenic and mesencephalic AVMs (Fig 3.101), — One patient with left parietal and right thalamic AVMs has been operated in two stages (Fig 3.102), — Two out of three patients with multiple callosal and plexal AVMs have been operated in the same approach (Figs 3.103-3.105), — One patient with left medial temporal AVM who died showed another small angiographically non-visualized AVM on the right frontal lobe at autopsy.
166
3. Pathological Considerations
References p. 385 Fig3.93A-F A 19 year old patient came in with epileptic seizures. A Right carotid angiography showed г diffuse type AVM scattered in fronto-operculo-insular area. It was supplied by middle cerebral artery branches. В Left carotid angiography demonstrated diffuse type callosal and septai AVMs.
References p. 385
Multiple Cerebral AVMs
167
Fig 3.93C-D Frontal view of right and left carotid angiogram showed the diffuse cortical and subcortical AVM being supplied by feeding arteries arising from A1 and M1 segments. E-F Vertebral angiography showed further AVMs in middle callosal and splenial area. The venous phase showed two separate venous systems draining the AVMs. With such extensive AVMs operation could not be recommended.
168
3. Pathological Considerations
References p. 36: Fig 3.94A-C This 30 year old patient with repeated attacks of subarachnoid hemorrhages had bilateral carotid angiography pe-formed in 1974 (A right side, B-C left side) which showed dif fuse type hemispheric bilateral with multiple distal aneurysms. j Inoperable case. Radiation recommended.
References p. 385
Multiple Cerebral AVMs
169
Fig 3.95A-F Four vessel angiography was performed on an
18 year old female patient after subarachnoid hemorrhage. There were multiple (3 or 4) AVMs visible in deep portions of both hemispheres strio-capsulo-thalamic. A Right carotid angiography. В Left carotid angiography. С Vertebral angiography.
Fig3.95D-F
170
3. Pathological Considerations
References p. 385
Fig3.95D-F Frontal view of right, left and vertebral angiography. Irradiation was performed in Boston in 1977. Note the aplasia of the straight sinus and the course of draining veins to ascending parietooccipital median veins. She lives to South America and no follow up is available.
References p. 385
Fig 3.96A-C In another case with bilateral AVMs in the strio-capsulothalamic region, radiation was recommended. Note the aplasia of the straight sinus (C).
Multiple Cerebral AVMs
171
172
3. Pathological Considerations
Fig 3.97A-H A-B A 7 year old boy, with subarachnoid hemorrhage had a diffuse AVM in thalamus shown on left carotid angiography in 1966. No therapy was performed. Note findings suspicious for AVM in the orbit. C-D Repeat left carotid and vertebral angiography performed in 1974 showed enormously enlargement by dilatation of the thalamic AVM. Note also the dilated ophthalmic artery supplying a second plexiform type retrobulbar AVM whiccaused exophthalmos. E-F Carotid (E) and vertebral (F) angiography shows the extension of the AVM within the thalamus. No therapy w a s performed. G CT in 1986 shows a large thalamic lesion and occlusive hydrocephalus. H The MRI in 1986 shows absence of the straight sinus. Severe mental and neurological deterioration, blindness bedridden.
References p. 385
Multiple Cerebral AVMs
173
174
3. Pathological Considerations
Fig 3.98A-D Three AVMs were found in this 16 year old girl. A-B Vertebral angiography showed a lateral prepontine AVM as well as a second AVM in the dorsal mesen-cephalon (arrows).
References p. 385
Fig 3.99A-C This 52 year old patient had two AVMs one supratentorial in the right parietal area, and a second in the territory of the right PICA. The patient refused the surgery.
Multiple Cerebral AVMs
175
176
3. Pathological Considerations
References p. 385
Fig3.100A-B A 37 year old male patient presented with a thalamic and a mesencephalic AVM. No operation was performed. Note the absence of the straight sinus.
Fig 3.101A-B Pre-(A), postoperative (B) angiograms (1976) in a 3 year old boy with AVM of vein of Galen showed afis-tulous connection of the left PCA to the vein of Galen plus a mesencephalic nidus (arrows). He will be radiated in StocK-holm (1986).
References p. 385
Multiple Cerebral AVMs
177
E-F Preoperative brachial angiography showed the right thalamic AVM, whereas the left carotid angiogram did not show the left parietal lesion. Note the stenosis of the straight sinus. Histology confirmed a typical AVM in both locations. The patient remains an invalid as he was preoperatively.
178
3. Pathological Considerations
References p. 385
A-D Carotid (A-B) and vertebral (C-D) angiograms showed a combination of multiple nidus AVMs located within the entire corpus callosum as well as in the choroid plexus of the Illrd ventricle. Each AVM had its own venous drainage.
References p. 385 Fig. 3.103E-G All AVMs were removed in one session through a paramedian frontoparietal osteoplastic craniotomy and interhemispheric approach. This was followed by impressive recovery of a preoperative paraplegic condition and mental retardation of an 8 year old girl la shunt operation was done before craniotomy).
Multiple Cerebral AVMs
179
180
3. Pathological Considerations
References p. 385
Fig3.104A-D
A A combination of multiple AVMs located within the corpus callosum, septum pellucidum and choroid plexus. В Each AVM has its own separate venous drainage towards the superior sagittal sinus, internal cerebral veins, basal veins and petrosal veins. С One part of the AVM drains into the inferior and superior sagittal sinuses, whereas another part drains into the internal cerebral and basal veins, and ultimately towards the petrosal sinus. The straight sinus is poorly visualized. D Removal of all 3 malformations was accomplished through a frontoparietal paramedian craniotomy and interhemispheric approach. Stormy postoperative course ensued with mental deterioration. Slow recovery followed shunting. 9 years after surgery the patient is able to care for himself but is not able to work as a computer engineer. The patient refused postoperative angiogra-phy. CT showed no evidence of AVM (D).
References p. 385 Fig 3.105A-C Carotid and vertebral angiography showed three AVMs: one in the genu of corpus callosum, a second in splenium and third in the choroid plexus in this patient .vho did not accept surgery. Note the stenosis of the straight sinus (arrow) and the unusual redistribution of . snous flow.
Multiple Cerebral AVMs
181
182
3. Pathological Considerations
Intracranial and Intraspinal AVMs Only 7 such cases have been recorded until recently (Wyburn-Mason 1943, Krayenbuhl et al. 1969, DiChiro and Werner 1973, Hash et al. 1975, Hoffman et al. 1976). Parkinson and West (1977) added a rare case of SAH first from intracranial
References p. 385-36f and then intraspinal AVM, each of which was sucl cessfully removed. Hoffman et al. (1976) de-scribed a case of extensive spinal cord AVM and right temporal AVM in a child. In our series there was no such combination. however, 2 patients did present with combined AVMs of medulla oblongata and cervical spinal cord.
Association of Persistent Trigeminal Artery and AVM One might also expect a frequent association of AVMs with other vascular anomalies known to be of congenital origin. With the exception of aneurysms, known to occur in 2.7-16.7% of cases with AVM, other congenital vascular anomalies, such as persistent embryonic caroticobasilar anastomoses are extremely rarely observed. The first case was reported by Krayenbuhl and Ya§argil (1957). Jayaraman et al. (1977) collected and tab-
ulated 11 cases of persistent trigeminal artery associated with an arteriovenous malformation from the literature and added one further case. Among a series of 105 cases of cerebral arterio- venous malformations, Moody and Poppen (19701 observed only one case associated with a persistent trigeminal artery. No occurrence of persistent. trigeminal artery was observed in this series of 500 AVMs.
Association of Aneurysm and AVM The first descriptions of an association between intracranial aneurysm and AVM was credited by Anderson and Blackwood (1959) to Laves in 1925 and Stewart and Ashby in 1930-31. Since then there have been many sporadic reports of these lesions occurring together and several attempts have been made to confirm the various theories which have been postulated to explain this association (Walsh and King 1942, Arieti and Gray 1944, Moniz and Guerra 1953, Christensen and Larsen 1954, Kane and Foley 1954, King et al. 1954, Murphy 1954, Paillas et al. 1956, Paterson and McKissock 1956, Descuns et al. 1956, Ley 1957, BoydWilson 1959, Anderson and Black-wood 1959, Caram 1959, Fine et al. 1960, Gibson and Rocha Melo 1960, Cronqvist and Troupp 1966, Ferret and Nishioka 1966, Locksley 1966, Nocola and Rizzoli 1966, Sakata et al. 1968, Murakami et al. 1971, Shenkin et al. 1971, Arai et al. 1972, Voigt et al. 1973, Fujino et al. 1976, Tsu-chita and Miyazaki 1976, Baba et al. 1977, Fukawa et al. 1977, Onuma et al. 1977, Yamagu-chi et al. 1977, Arabi and Chambers 1978, Higashi et al. 1979, Suzuki and Onuma 1979, Hatanaka et al. 1980, Hashimoto et al. 1980, Niino et al. 1980, Parkinson and Bachers 1980, Takara et al. 1980, Hayashi et al. 1981, Koulouris and Rizzoli 1981, Gamache et al. 1981, Kassell 1981, Malis 1982, Miyasaka et al. 1982, Gacs et al. 1983, Hudgins et
al. 1983, Gardeur et al. 1983, Kikuchi et al. 1984. Okamoto et al. 1984, Garza-Mercado et al. 1984 Waga et al. 1985, Nehls and Carter 1985, Batjer et al. 1986). This topic has already been discussed in
-Terences p. 386
Association of Aneurysm and AVM
183
common developmental vascular abnormality producing both aneurysm and AVM was first propounded by Arieti and Gray (1944). Boyd-Wilson (1959) suggested that the lesions were merely coincidental whereas Paterson and McKissock (1956), Shenkin et al. (1971), and Gacs et al. (1983) support a theory of hemodynamic factors, including the role of a hyperdynamic circulatory state. Gardeur et al. (1983) found 85 cases in the literature, added 8 cases of their own, and discussed the hemodynamic origin of the aneurysms. Okamoto et al. (1984) added 5 cases of their own to 73 cases previously reported in the literature and carried out a statistical analysis, comparing these 78 cases (associated with 119 aneurysms) with over 500 cases of isolated aneurysm from the Cooperative Study. The principal aim was to study the distribution of aneurysm by site and relate this to their occurrence on potential and real feeding vessels in the two populations. Their figures and statistical comparisons are difficult to follow, but they concluded that since the distribution of aneurysms (in the study group) on any given feeding artery to an AVM was greatly in excess of the expected distribution in the absence of an AVM, then there presumably exists an underlying cause, such as hemodynamic stress, in the development of associated aneurysms. Aneurysms occurring at sites well distant from AVMs or their major feeding vessels were felt to be purely coincidental.
Fig 3.106A-B Occurence of associated aneurysms related and unrelated to high flow, a Small aneurysms in the vicinity of AVM. b Aneurysms on a proximal related segment, с Aneurysms on unrelated arteries.
184
3. Pathological Considerations
In Ferret and Nishioka's 37 combined cases (1966) the aneurysms were located on major feeding vessels to the AVM in 37%, well proximal on the feeding vessels in 21% and unrelated to the AVM in 42%. Miyasaka et al. (1982) reviewed the angiograms of 132 consecutive patients with AVM and found 43 aneurysms in 22 of these patients (16.7%). Thirteen patients had single aneurysms. They found that aneurysms were more likely to occur in older patients and in those patients with larger AVMs. They further suggested (based on the findings of Stehbens, 1972) that since the prevalence of AVMs in a large autopsied series of patients with cerebral aneurysms was not significantly higher than in a control group without aneurysm, then the same developmental defect is unlikely to account for both lesions. Similarly, the theory of coincidental association was thought to be unlikely. The distribution of aneurysms and of infundibula on major feeding vessels to the AVMs, remote from the circle of Willis, was such that they concluded that hemodynamic changes in the arteries supplying the malformation must have some role in the etiology of concurrent aneurysm. These conclusions supported the views of Hayashi et al. (1981). Nehls and Carter (1985) described a case of multiple unusual aneurysms (left meningohypophyseal trunk, left ICA, right ICA and MCA) in association with a left occipital AVM. They concluded that the aneurysm on the meningohypophyseal feeder to the AVM may have been produced through hemodynamic changes within this vessel whereas the other nonhemodynamically related aneurysms represented a more generalized tendency toward the formation of vascular lesions in this patient. Our own observations and thoughts (Table 3.13) force us to question some of the conclusions described above. We would make the following points: 1. If increased flow alone factors plays a significant role in the etiology of concurrent aneurysms then we should see far more aneurysms than have been observed either directly related to feeding arteries or even ipsilateral to the AVM (Table 3.14). 2. Similarly, if increased flow were the primary factor, we should see more aneurysms associated with fistulous communications and with giant or large AVMs with high flow rates. Our own figures show that this is not the case (Table 3.13).
References p. 386 Table 3.13 Frequency of type of operated AVM and associated aneurysms AVM patients Number with Frequency aneurysms
Type of AVM Fistula (high flow)
10
0
0
V. of Galen AVM
16
0
0
Giant AVM
17
2
1 1 .8%
Large AVM
142
15
10.5%
Moderate AVM
174
20
1 1. 5%
Small AVM
61
8
13.1%
This present series comprises a total of 500 cases of AVM; 86 of these were not operated, of which 5 had aneurysms (5.8%). Of the 414 operated cases, 45 (10.86%) had associated aneurysms. In 3 cases (0.7%) the aneurysms were totally unrelated to the AVM (contralateral angiographically nonparticipating arteries like ICA, АСА, MCA or PCA) (see Vol. I, p. 312). The remainder were ipsilateral lesions. Some were large, readily evident lesions on angiography and at surgery, while others were smaller and seen only at surgery (presumably not filling readily on angiography owing to abnormal regional flow). These latter lesions, however, were distinguished from common small blebs which are not considered significant. The\ were related to the AVMs as shown in Table 3.14. The term distant implies an aneurysm on a major vessel of the circle of Willis (usual aneurysm site i whereas close implies an aneurysm arising in an unusual position and within 1—2 cm of the AVM. Table 3.14 Size of aneurysm
3-20 mm
Small