ICA Aneurism

Neurol Med Chir (Tokyo) 47, 153¿158, 2007

Internal Carotid Artery Bifurcation Aneurysms: Surgical Experience Sunil Kumar GUPTA, Virender Kumar KHOSLA, Rajesh CHHABRA, Sandeep MOHINDRA, Jaipali Rajeev BAPURAJ, Niranjan KHANDELWAL, Kanchan Kumar MUKHERJEE, Manoj Kumar TEWARI, Ashis PATHAK, and Suresh Naraian MATHURIYA Department of Neurosurgery, Postgraduate Institute of Medical Education and Research, Chandigarh, India

Abstract Internal carotid artery (ICA) bifurcation aneurysms are relatively uncommon and frequently rupture at a younger age compared to other intracranial aneurysms. We have treated a total of 999 patients for intracranial aneurysms, of whom 89 (8.9%) had ICA bifurcation aneurysms, and 42 of the 89 patients were 30 years of age or younger. The present study analyzed the clinical records of 70 patients with ICA bifurcation aneurysms treated from mid 1997 to mid 2003. Multiple aneurysms were present in 15 patients. Digital subtraction angiography films were studied in 55 patients to identify vasospasm and aneurysm projection. The aneurysm projected superiorly in most of these patients (37/55, 67.3%). We preferred to minimize frontal lobe retraction, so widely opened the sylvian fissure to approach the ICA bifurcation and aneurysm neck. Elective temporary clipping was employed before the final dissection and permanent clip application. Vasospasm was present in 24 (43.6%) of 55 patients. Forty-eight (68.6%) of the 70 patients had good outcome, 14 (20%) had poor outcome, and eight (11.4%) died. Patients with ICA bifurcation aneurysms tend to bleed at a much younger age compared to those with other intracranial aneurysms. Wide opening of the sylvian fissure and elective temporary clipping of the ICA reduces the risk of intraoperative rupture and perforator injury. Mortality was mainly due to poor clinical grade and intraoperative premature aneurysm rupture. Key words: subarachnoid hemorrhage, temporary clipping, surgical outcome

internal carotid artery bifurcation aneurysm,

Introduction

cranial aneurysms from June 1997 to July 2003 had an aneurysm arising from the bifurcation of the ICA. Twenty of the 89 patients (22.5%) were aged 20 years or younger and 42 (47.2%) were aged 30 years or younger. During the same period, only 12 (3.1%) of 387 patients with anterior communicating artery (AComA) aneurysms, one (0.4%) of 254 patients with middle cerebral artery (MCA) aneurysms, and two (1.8%) of 111 patients with posterior communicating artery (PComA) aneurysms were aged 20 years or younger, and 46 (11.9%), 19 (7.4%), and 10 (9.0%), respectively, of patients with these aneurysms were aged 30 years or younger. Complete clinical data were available for 70 patients. Forty (57.1%) of these patients were female, two of whom were pregnant at the time of presentation. The Hunt and Hess grading scale was used to assess the neurological status on admission and just prior to surgery. The Hunt and Hess grade at sur-

Internal carotid artery (ICA) bifurcation aneurysms account for approximately 5% of all intracranial aneurysms.1,6,7,15) Various series of ICA bifurcation aneurysms have been described,1–16) with the largest series including 55 patients.16) These aneurysms tend to occur in relatively younger patients,5,8,16) and are considered difficult to treat surgically because of the relationship with the perforators.7,9,15) We present our experience with 89 patients with ICA bifurcation aneurysms.

Clinical Materials and Methods Eighty-nine of 999 patients (8.9%) treated for intraReceived 2007

October 19, 2005;

Accepted

sylvian fissure,

January 29,

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gery was analyzed in this study. Forty-eight (68.6%) of the 70 patients were in Hunt and Hess grades I and II, whereas 22 (31.4%) were in grades III and IV. Fifty-eight (82.9%) of these 70 patients had had one episode of bleeding before surgery, whereas 10 (14.3%) were admitted after two episodes and two (2.9%) after three episodes. Computed tomography was performed in all patients and subarachnoid hemorrhage (SAH) was graded according to Fisher's scale. Forty-eight patients (68.6%) were in grades III and IV.

Surgical Technique ICA bifurcation aneurysms were routinely clipped using the standard pterional craniotomy. However, a few points need emphasis. In approximately half of the patients, the fundus is pointed superiorly and may be embedded in the frontal lobe. Frontal lobe retraction starting with the retractor adjacent to the carotico-optic space can cause premature rupture of the fundus or the aneurysm may become avulsed from the neck. In the beginning of this series, this happened twice. Therefore, we stress wide splitting of the sylvian fissure distal to proximal as the initial and important step to release cerebrospinal fluid and to expose the ICA bifurcation, which almost completely avoids the need for frontal lobe retraction. Sylvian fissure splitting exposes the M1 portion of MCA, which is traced to the ICA bifurcation. Before dissecting the aneurysm, we also expose the A1 segment so that we have complete proximal and distal control. Elective temporary clipping of the ICA before final dissection of the aneurysm neck and fundus is useful and can be helpful in preventing premature rupture of the aneurysm and for better visualization of the relationship between the neck and the perforating vessels. Before applying a temporary clip, we give intravenous mannitol (0.5 g･kg－1･body wt), phenytoin (500 mg), and dexamethasone (4 mg) as neuroprotective agents. It is important to avoid injuring or including the perforators during application of the aneurysm clip. Exposure of the ICA, M1, and A1 before clip application is very helpful in avoiding perforator injury. After temporary clipping, the aneurysm is dissected, especially for identification and preservation of the perforators and recurrent artery of Heubner. Most of the perforators are located on the posterior aspect of the aneurysm. We faced most difficulty in dissection of the neck of posteriorly oriented aneurysms. Dissection of the recurrent artery of Heubner was difficult in patients in whom this artery was related to the neck of the aneurysm and in patients with posterior-

ly oriented aneurysm.

Results The ICA bifurcation aneurysm was located on the left in 42 (60%) of the 70 patients, on the right in 26 (37.1%), and bilaterally in two (2.9%). Thirteen patients had multiple aneurysms including other aneurysms located on the MCA (8 cases), PComA (4), AComA (3), anterior choroidal artery (3), carotidophthalmic artery (1), and basilar top (1). Two of these patients presented with SAH from another aneurysm, and the ICA bifurcation aneurysm was unruptured. Independent review of the digital subtraction angiograms was possible in 55 patients. The size of the aneurysm was Ã10 mm in 38 cases (69.1%), 11–20 mm in 16 (29.1%), and À20 mm in one (1.8%). The aneurysm projected superiorly in 37 cases (67.3%), anteriorly in 11 (20.0%), and posteriorly in seven (12.7%). The superiorly projecting aneurysms, pointed directly superiorly in 23 cases (41.8%), tilted medially towards the A1 in 11 (20.0%), and tilted laterally towards the M1 in three (5.5%). The recurrent artery of Heubner was most often located on the posterior aspect of the aneurysm, and was relatively easier to separate from the aneurysm neck if the aneurysm was tilted towards the M1. Recurrent artery of Heubner was generally present as one of the many perforators related to the aneurysm. Among 20 patients, recurrent artery of Heubner was specifically documented as arising from the A1-AComA junction in 16 patients, from the distal A1 segment in three, and from the proximal A2 segment in one (Fig. 1). The recurrent artery of Heubner terminated posterior to the fundus of the aneurysm in seven patients, posterior to the aneurysm neck in five, and on the superior surface of the aneurysm in five, and passed over the medial border of the aneurysm fundus in three (Fig. 2). Vasospasm occurred in 24 (43.6%) of 55 patients examined. Twenty-one (30.0%) of the 70 patients were operated within 72 hours of the last ictus, four at Ã24 hours, seven at À24–48 hours, and 10 at À48–72 hours, whereas 49 (70.0%) were operated more than 72 hours after the last bleeding episode, 22 at 4–7 days and 27 at À7 days, mainly because of late referral to our hospital. Forty-eight (68.6%) of the 70 patients had good outcome (Glasgow Outcome Scale [GOS] score 5 or 4) whereas 14 (20.0%) patients had poor outcome (GOS score 3 or 2). Eight (11.4%) patients died (Table 1). Three (6.3%) died of the 48 patients with Hunt and Hess grades I and II, two (13.3%) of the 15 with grade III, and three (42.9%) of the seven with

Neurol Med Chir (Tokyo) 47, April, 2007

ICA Bifurcation Aneurysms grade IV (Table 1). Death could be attributed to poor clinical grade (grade IV) in three patients, with the added complication of septicemia and chest infection in one and MCA infarct in another. Death was due to premature intraoperative rupture before any dissection was done in two patients, possibly due to MCA infarct in two, and the cause could not be ascertained in one. Further analysis of the patients who died observed that all deaths occurred during the years 1997–2000, and there were no deaths after 2000. Complete

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clinical data was available for 40 patients from mid 1997 to 2000, whereas clinical details were available for 30 patients from 2000 to mid 2003. Therefore, there was definitely an improvement with experience. We believe that this was largely due to the change in strategy from retracting the frontal lobe to working along the sylvian fissure towards the ICA and aneurysm neck.

Discussion A total of 822 patients with ICA bifurcation aneurysms have been reported in 43 series from 1933 to 2000, of whom 507 were treated surgically.7) The reported incidence of ICA bifurcation aneurysms varies from 5% to 10%.5,7,12,16) In our series, the incidence was 8.9% of all patients operated for intracranial aneurysms. The most striking clinical feature of ICA bifurcation aneurysms is the

Fig. 2 Fig. 1

Table 1

Line diagrams showing the variations in the origin of recurrent artery of Heubner: A1 segment to anterior communicating artery junction (A, n ＝ 16), distal A1 segment (B, n ＝ 3), and proximal A2 segment (C, n ＝ 1).

Line diagrams depicting the various relationships of the recurrent artery of Heubner with the aneurysm: termination posterior to the aneurysm fundus (A, n ＝ 7), on the superior surface of the aneurysm (B, n ＝ 5), and posterior to the aneurysm neck (C, n ＝ 5), and passing over the medial border of the aneurysm fundus (D, n ＝ 3).

Surgical outcome and preoperative clinical grade Glasgow Outcome Scale

Hunt and Hess grade before surgery

n

I II III IV Total

Good

Moderate disability, independent

Severe disability, dependent

Vegetative

Dead

16 32 15 7

10 18 6 0

3 10 1 0

1 2 4 2

0 1 2 2

2 1 2 3

70

34 (48.6%)

14 (20.0%)

9 (12.9%)

5 (7.1%)

8 (11.4%)

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younger age of the patients at the time of rupture, compared to aneurysms at other locations. Patients with rupture of aneurysms at other locations (i.e. AComA, MCA, and PComA) were aged between 40 and 60 years. The mean age of patients with ruptured ICA bifurcation aneurysms was reported as 41 years7) and 48.3 years,2) but was significantly lower at 31.5 years in our patients. In a series of 1012 patients, only 41 patients were aged less than 20 years.16) Among the 55 patients with ICA bifurcation aneurysms, 32 were aged less than 30 years and 16 patients were under the age of 20 years. Almost half (40 of 89) of our patients were 30 years of age or younger, and 20 were 20 years of age or younger. The youngest patient in our series was a 9-year-old girl. The incidence of multiple aneurysms ranges from 19% to 22%.4–8) In contrast, multiple aneurysms occur in 15–47% of patients with ICA bifurcation aneurysm (mean 30%).5,7,16) In our series, 15 (21.4%) of 70 patients had additional aneurysms, two of whom had bilateral ICA bifurcation aneurysms. The presence of male or female predominance varies with the aneurysm site. A series of 1104 cases of ICA aneurysms showed the highest female predominance (1:7.3) in patients with intracavernous aneurysm, and lowest (1:1.6) in patients with ICA bifurcation aneurysms.6) Previous studies have reported male predominance,2,3,11,16) no predominance,7) and female predominance.4) In our series, 40 of 70 patients (57.1%) were female, thus supporting a slight female predominance (1.33:1). The aneurysm fundus may project in the superior, posterior, or inferior directions.16) The aneurysm is usually located more on the MCA or anterior cerebral artery, although no specific relationship to the size of the arteries was recorded.16) The superior projection has been most commonly reported (54.4%), followed by posterior projection (40.4%), and rarely anterior projection (5.3%).2,3,5,11–13) However, one series of 25 cases contained 12 superior, seven anterior, and six posterior projection aneurysms.7) In our series, most aneurysms (37/55, 67.3%) had superior projection, which we feel is important in planning surgical strategy. Our surgical strategy requires opening of the sylvian fissure widely from distal to proximal, to identify the MCA and work towards the ICA bifurcation. We believe that this is the most important step to avoid intraoperative rupture of the aneurysm. We experienced aneurysm rupture secondary to frontal lobe retraction in the early part of the series, and since then have performed wide opening of the sylvian fissure rather than frontal lobe retraction to reach the ICA and the aneurysm

neck. Elective temporary clipping of the ICA prior to the final dissection of the neck and placement of the aneurysm clip is a useful strategy which makes dissection of the aneurysm much safer and easier, and allows better identification of the perforators before final placement of the clip. With experience, we have found that perforator injury is rather uncommon with this technique and ICA bifurcation aneurysms are usually easier to clip. Elective temporary clipping is much better than emergency temporary clipping, which may be needed in the event of intraoperative aneurysm rupture, as the risk of perforator injury is lower. Temporary clipping was previously used in two of nine cases,13) 28 of 29 cases,3) three of 18 cases,4) and eight of 25 cases.7) Temporary clipping must be utilized in difficult cases8) but possibly there is no need to place temporary clips on the parent vessel.11) Induced hypotension is useful even for large aneurysms with no need for temporary clipping.12) We did not use intraoperative hypotension to facilitate clipping in this series. Mortality rate in some of the older series was high, ranging up to 30%,10) but the introduction of microsurgery has resulted in remarkably low rates ranging from 0% to 12%.2,8,9,11,14–16) The most important factor affecting outcome is the clinical grade of the patient prior to surgery. In our series, the overall mortality rate was 11.4%. Patients with good preoperative clinical grade had mortality rate of 6.3%, whereas patients with poor clinical grade had higher mortality. Vasospasm was present in less than half of the patients and there were no statistically significant correlations between the presence or absence of spasm, preoperative clinical grade, and postoperative outcome. The outcome in patients with ICA bifurcation aneurysm is related only to the clinical grade.16) However, vasospasm is elsewhere considered to be the main causative factor of unfavorable outcome.2,3,8,9,11,12) Unfavorable outcome was due to primary brain damage (4/25), vasospasm (2/25), and pneumonia (1/25) in one series.7) Mortality in the present series was caused by poor preoperative grade, intraoperative premature aneurysm rupture, chest infection, and postoperative MCA infarct. We recommend wide opening of the sylvian fissure from distal to proximal, to identify the MCA and approach the ICA bifurcation. Temporary clipping of the ICA prior to final dissection of the aneurysm neck and clip placement is also useful.

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ICA Bifurcation Aneurysms

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Flamm ES: Other aneurysms of the internal carotid artery, in Wilkins RH, Rengachary SS (eds): Neurosurgery, ed 2. New York, McGraw Hill, 1996, pp 2301–2309 Kashiwagi S, Yamashita K, Kato S, Akimura T, Ito H, Harada K, Ihara K: [Surgical treatment of the internal carotid bifurcation aneurysm]. Surgery for Cerebral Stroke 25: 428–433, 1997 (Jpn, with Eng abstract) Kodama N, Koshu K, Minemura K, Suzuki J: Surgical treatment of internal carotid bifurcation aneurysms, in Suzuki J (ed): Cerebral Aneurysms. Tokyo, Neuron, 1979, pp 263–267 Laranjeira M, Sadasivan B, Ausman JI: Direct surgery for carotid bifurcation artery aneurysms. Surg Neurol 34: 250–254, 1990 Lassman LP: Internal carotid artery bifurcation aneurysms, in Pia HW, Langmaid C, Zierski J (eds): Cerebral Aneurysms, Advances in Diagnosis and Therapy. Berlin, Springer, 1979, pp 96–106 Locksley HB: Report on cooperative study of intracranial aneurysms and subarachnoid hemorrhage, section V, part I: Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations: based on 6368 cases in the cooperative study. J Neurosurg 25: 219–239, 1966 Miyazawa N, Nukui H, Horikoshi T, Yagishita T, Sugita M, Kanemaru K: Surgical management of aneurysms of the bifurcation of the internal carotid artery. Clin Neurol Neurosurg 104: 103–114, 2002 Ohno K, Komatsu K, Aoyagi M, Takada Y, Wakabayashi S, Hirakawa K: [Aneurysms of the internal carotid bifurcation]. Surgery for Cerebral Stroke 24: 5–10, 1996 (Jpn, with Eng abstract) Ojemann RG, Heros RC, Crowell RM: Internal carotid artery aneurysms, in: Surgical Management of Cerebrovascular Disease. Baltimore, Williams & Wilkins, 1988, pp 179–198 Perria L, Rivano C, Rossi GF, Viale G: Aneurysms of the bifurcation of the internal carotid artery. Acta Neurochir (Wien) 19: 51–68, 1968 Pian RD, Pasqualin A, Scienza R: Direct microsurgical approach to aneurysms of the internal carotid bifurcation. Surg Neurol 13: 27–37, 1980 Reynier Y, Lena G, Vincentelli F, Vigouroux RP: Anevrysmes de la bifurcation de la carotide interne. Reflexions techniques a propos d'une serie de 10 cas. Neurochirurgie 35: 242–245, 1989 (Fre, with Eng abstract) Sengupta RP, Lassman LP, De Moraes AA, Garvan N: Treatment of internal carotid bifurcation aneurysms by direct surgery. J Neurosurg 43: 343–351, 1975 Spetzler RF, Koos WT, Richling B, Lang J: Aneurysms of the brain, in Spetzler RF, Koo WT (eds): Color Atlas of Microneurosurgery, vol 2. Stuttgart, Thieme, 1996, pp 169–181 Weir B: Carotid bifurcation artery aneurysms, in:

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Aneurysms Affecting the Nervous System. Baltimore, Williams & Wilkins, 1987, pp 456–460 16) Yasargil MG: Aneurysms of internal carotid artery bifurcation (ICBi-aneurysms), in Yasargil MG (ed): Microneurosurgery, vol 2. Stuttgart, George Thieme, 1984, pp 109–122

Address reprint requests to: Sunil Kumar Gupta, M.D., Additional Professor, Department of Neurosurgery, PGIMER, Chandigarh–160 012, India. e-mail: drguptask＠yahoo.com

Commentary The authors are congratulated on a careful analysis of outcome of a large surgical series of internal carotid bifurcation aneurysms. Their wise conclusion relates to the importance of wide opening of the sylvian fissure, and elective temporary clipping to reduce the risks of aneurysm rupture and perforator injury. They share sobering complication rates, with 31.4% of cases resulting in severe disability, vegetative state, or death. Most complications in high grade patients occurred from vasospasm or as direct effect of poor initial clinical grade. But there were 7 of 42 cases in good clinical grade (I or II), or 14.5%, which also resulted in such poor outcome. These complications among good grade patients mostly resulted from premature rupture during surgery and postoperative infarcts. With regard to prevention of premature rupture, the importance of modifying surgical exposure cannot be overemphasized. Bony exposure must include frontal base exposure absolutely flush with the floor of the anterior cranial fossa, and radical resection of the sphenoid ridge as far medially as the superior orbital fissure (we use an orbitozygomatic exposure for giant or particularly ``high'' lesions). The head is initially elevated, and basal cisterns are not emptied early. The frontal lobe is not retracted at all, and in fact not even allowed to fall by gravity, until the sylvian fissure is widely split. This is accomplished from lateral to medial by manipulation of the temporal lobe and with no manipulation of the frontal lobe until after the middle cerebral and internal carotid arteries are exposed and control is established. Only then, and with arachnoidal tethers released, is the frontal lobe gently mobilized and the head of the bed lowered, to allow gravity to help us as we complete the exposure of the neck and the anterior cerebral artery, all the while ensuring that each move does not stretch the aneurysm dome (which is often buried into the frontal lobe). Except in a minority of

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cases where the dome is fully mobilizable in the subarachnoid space, temporary clips are used, not only on the internal carotid artery, but also on the middle cerebral artery. Temporary clipping of the anterior cerebral artery is rarely needed, as the aneurysm will soften enough for clear manipulation to define and sweep away the perforators on the posterior wall and behind the neck. A lateral to medial view through the sylvian fissure is most useful for this. The softening also allows safer clip placement. With these steps, we have been fortunate (and lucky) not to encounter premature rupture during exposure of these lesions in recent years. Sparing the perforators is the next essential step. These occur in three groups, and all three must be looked for and avoided. The first group of perforators arises from the anterior choroidal distal segment of the internal carotid artery, behind the aneurysm neck, and they course superiorly, medially, or laterally. A second group of perforators may include one or more recurrent arteries coursing from the anterior cerebral artery in a medial to lateral direction (i.e. Heubner artery). And a third group of perforators may include one or more arteries coursing from the M1 segment of middle cerebral artery medially. These can usually be easily swept away, so they are not fettered by clip application. The lesson here is to look and see all the way behind the neck and dome. The final task is a clipping strategy to preserve and verify patency of the middle cerebral and anterior cerebral artery orifices, while avoiding residual ``dog

ears'' at the neck. We have been using short tandem clips (including a custom made ultra-short fenestrated clip) more and more for precise reconstruction at such bifurcations. Intraoperative micro-Doppler insonation is essential in every case, and intraoperative angiography in more difficult cases, to ensure patency of these critical parent vessels. These technical challenges and outcome caveats beg the question of whether endovascular treatment can deliver a better outcome for these lesions. Aneurysms at this location, especially when medium or large sized, may often exhibit a broad neck, incorporating the origin of the middle or anterior cerebral arteries. These features and the direct water hammer effect of flow at the carotid summit, often make their endovascular coiling suboptimal or less durable. Newer techniques incorporating a small stent may help in this regard, but morbidity rates and technical feasibility have not been systematically reported. And the risk of early or late parent artery compromise by stent complications or stenosis can be devastating and most unforgiving in this location. The article by Gupta et al. defines a reasonable surgical bar to meet or exceed when assessing these emerging modalities. Issam A. AWAD, M.D., M.Sc., F.A.C.S., M.A. (Hon.) Evanston Northwestern Healthcare Department of Neurological Surgery Northwestern University Feinberg School of Medicine Evanston, Illinois, U.S.A.

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