Clinical Neurology and Neurosurgery 110 (2008) 674–681
Surgical management of giant intracranial aneurysms Bhawani Shankar Sharma a,∗ , Aditya Gupta a , Faiz Uddin Ahmad a , Ashish Suri a , Veer Singh Mehta b a
Department of Neurosurgery, All India Institute of Medical Sciences, New Delhi 110029, India b Paras Hospital, Sushant Lok, Gurgaon, Haryana, India Received 16 August 2007; received in revised form 29 March 2008; accepted 5 April 2008
Abstract Objectives: The natural history of giant intracranial aneurysms is generally morbid. Mortality and morbidity associated with giant aneurysms is also higher than for smaller aneurysms. This study was carried out to assess the demographic profile, presenting features, complications, and outcome after surgical treatment of giant intracranial aneurysms. Patients and methods: A retrospective review of the medical records of all patients with giant intracranial aneurysms treated in the Department of Neurosurgery, Neurosciences Centre, All India Institute of Medical Sciences, New Delhi, from January 1995 through June 2007 was performed. The demographic profiles, presenting features, radiological findings, surgical treatments, and outcomes were assessed. Results: A total of 1412 patients harboring 1675 aneurysms were treated. Out of these, 222 patients had 229 (13.7%) giant aneurysms, and of those, 181 aneurysms in 177 patients were managed surgically while 48 were treated with endovascular therapy. In the patients treated with surgery, common clinical presentations included subarachnoid hemorrhage (SAH) in 110 (62%) cases followed by mass effect in 57 (32%) cases. In patients who presented with SAH, the Hunt and Hess SAH grading was: grade I in 43 (39%), grade II in 40 (36%), grade III in 23 (21%), grade IV in two (2%), and grade V in 2 (2%) patients. One hundred and seven aneurysms (in 103 patients) were treated using direct surgical clipping. Forty-six patients with good collateral circulation were treated by gradual occlusion and ligation of the internal carotid artery (ICA) in the neck with a Silverstone clamp. Another nine patients with good collateral circulation, but persisting symptoms after ICA ligation, required trapping for obliteration of the aneurysm. Eleven patients with poor collateral circulation required extracranial–intracranial (EC–IC) bypass before proximal ICA ligation. A post-operative digital subtraction angiography (DSA) was performed in 118 patients and revealed well-obliterated aneurysm in 106 patients. The total treatment mortality rate was 9%. In the last 5 years, 117 patients were operated on with four operative deaths. Overall, the outcome was excellent in 131 (74.0%), good in 22 (12.4%), and poor in eight (4.5%) cases. Conclusions: It is concluded that 14% of all intracranial aneurysms are giant. The most common clinical presentation is SAH followed by features of an intracranial mass lesion. The cavernous ICA is the most common portion of the ICA affected. Direct surgical clipping is a safe and effective method of treatment and should be considered the first line of treatment whenever possible. With proper case selection, optimal radiological evaluation, and appropriate surgical strategy, it is possible to achieve a favorable outcome in almost 90% of the cases. © 2008 Elsevier B.V. All rights reserved. Keywords: Intracranial aneurysm; Giant; Surgery; Management; Subarachnoid hemorrhage
1. Introduction Intracranial aneurysms larger than 25 mm in maximum diameter are classified as giant [1]. The natural history of giant intracranial aneurysms (GIAs) is generally morbid as a result of hemorrhage, neural compression, and thromboembolic episodes. Left untreated, the majority of patients suffer ∗
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from ruptures of these aneurysms. Once ruptured, the cumulative frequency of rebleed at 14 days is 18.4%. It has been shown that mortality is above 60% within 2 years and 80% of patients with untreated symptomatic GIAs are dead or totally incapacitated within 5 years of diagnosis [2–4]. When an aneurysm grows to giant size, the neck widens and may incorporate the efferent arteries. The lumen usually contains a thrombus and the wall may become calcified. All of these features alone or in combination preclude simple surgical clipping. Endovascular treatment for GIAs is
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not optimal because of lack of relief from mass effect, cost (especially in India) and the high complication rates in broad necked giant aneurysms. The goal of aneurysm obliteration with maintenance of adequate cerebral blood flow (CBF) and relief of mass effect therefore remains a definite surgical challenge [3,5]. Mortality and morbidity associated with GIAs is higher than that for smaller aneurysms [6]. Surgical outcome for GIAs is still unsatisfactory. The reasons for the higher complication rates are the occlusion of perforators or parent arteries by the aneurysm clipping itself, or temporary occlusion of main arteries [6–10]. Furthermore, aneurysms that are most difficult surgically are the ones that offer the lowest probability for a definitive endovascular cure [5,11–14]. Most of the reported experiences of surgery for GIAs are from the west, with practically no reports from South-East Asia. We report our experience with surgical treatments of GIAs at a premier tertiary referral centre in India.
2. Material and methods The medical records of all patients with intracranial aneurysms treated in the Department of Neurosurgery, Neurosciences Centre, All India Institute of Medical Sciences, New Delhi, from January 1995 through June 2007 were reviewed. The demographic profiles, presenting features, radiological findings, surgical treatments, and outcomes were assessed. A total of 1412 patients harboring 1675 aneurysms were treated. Out of these, 222 patients had 229 (13.7%) GIAs. A predominance of female patients was apparent (133 females to 89 males, a ratio of 1.5:1). Of these, 181 aneurysms were managed surgically while 48 were treated with endovascular therapy. The majority presented in the fifth and sixth decades of life with the youngest patient being 3 years old and the oldest 76. All patients underwent CT scans and standard four-vessel (carotid and vertebral) digital subtraction angiographies (DSAs). In patients treated in last 4 years, 3D DSAs were also available. CT scans were done to demonstrate size, calcification, thrombosis, subarachnoid hemorrhage (SAH), intracerebral/intraventricular hemorrhage, and hydrocephalus. Hypertension, metabolic derangements like electrolyte imbalances, hydrocephalus, and vasospasm were treated appropriately.
3. Results In 177 patients treated with surgery, common clinical presentations included SAH in 110 (62%) cases followed by mass effects in 57 (32%) cases. Aneurysms in five patients were detected incidentally (three patients presented with seizures, two with embolic strokes). Symptoms and signs of local mass effects included adjacent cortical dysfunction, failing vision, cranial nerve paresis, and retro-orbital pain. In patients who presented with SAH, the Hunt and Hess SAH grading was: grade I in 43 (39%), grade II in 40 (36%), grade
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Table 1 Aneurysm location Location
Number of aneurysms (181) (number of patients, 177)
Anterior circulation Internal carotid artery Cavernous Clinoidal seg Carotid trunk Bifurcation Middle cerebral artery Anterior cerebral artery
168 151 58 53 22 18 13 4
Posterior circulation Basilar apex Posterior cerebral artery Vertebrobasilar junction Vertebro-PICA
13 4 5 3
III in 23 (21%), grade IV in two (2%), and grade V in two (2%) patients. The site and location of aneurysms is shown in Table 1. There were 168 aneurysms located in the anterior circulation. The cavernous internal carotid artery (ICA) was the most common location in these patients. In 13 patients, aneurysms were located in the posterior circulation. Multiple GIAs were found in six cases. Four patients had mirror image giant clinoidal segment aneurysms, one had mirror image middle cerebral artery (MCA) bifurcation aneurysms, and another had an aneurysm at the MCA and cavernous ICA. The surgical procedures utilized for the aneurysms are shown in Table 2. Direct surgical clipping was used to treat 107 aneurysms (in 103 patients). A post-operative check DSA was performed in 118 patients and revealed well obliterated aneurysms in 106 patients. In the clipping group, a check DSA was performed and revealed well-clipped aneurysms in 76 out of 88 patients. A residual neck was observed in 12 patients. In five of these patients, the residual aneurysm was coiled, and the other seven patients had very small neck remnants and are being followed up with yearly angiograms. Forty-six patients with good collateral circulation as determined by (1) filling of opposite anterior cerebral (ACA) and MCA spontaneously or at cross-compression, (2) adequate filling of posterior communicating artery, and (3) smooth filling of arteries without filling defects were treated by gradual occlusion and ligation of internal carotid artery ICA in the neck with a Silverstone clamp. Parent vessel ligation was never used in the acute phase of SAH. Another nine Table 2 Surgical procedures (181 procedures in 177 patients) Procedure
Number of aneurysms
Direct clipping Cervical ICA ligation Trapping with ligation Trapping with bypass Wrapping Aneurysmorrhaphy
107 46 9 11 7 1
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patients with good collateral circulation and persisting symptoms after ICA ligation required trapping for obliteration of the aneurysm. Eleven patients with poor collateral circulation required extracranial–intracranial (EC–IC) bypass before proximal ICA ligation. A check angiogram in four patients who had neurological deficits following EC–IC bypass showed blockade and/or patent bypass. Fifteen (8.3%) aneurysms ruptured during clipping. All aneurysms were punctured after clipping, and those that presented with mass effects were resected (61 resected aneurysms in all). The average duration of stay in intensive care units was 7 days. Complications that occurred in our surgical series have been discussed in the text. Ten patients developed hydrocephalus after treatment, five of whom required shunts. Nine patients developed meningitis and were managed with an intravenous antibiotic combination of third generation cephalosporin, aminoglycosides, and intrathecal antibiotics (vancomycion or gentamycin). We diagnosed vasospasm with transcranial Doppler in the post-operative period in the intensive care unit. This is treated at our centre with nimodipine, triple-H therapy, intrathecal papavarine and, when required, with endovascular therapy. Twelve patients developed infarcts in the post-operative period and three of these required a decompressive craniectomy and duraplasty/partial lobectomy. There were 16 deaths, resulting in a total treatment mortality rate of 9% in the surgical group of 177 patients. The causes of death are given in Table 3. Eleven of these were either due to vasospasm or infarction secondary to prolonged temporary clip application or kinking of the parent artery or embolus. In the last 5 years, 117 patients were operated on with four operative deaths. The outcome according to surgical procedure performed is indicated in Table 4. We used the Glasgow outcome score (GOS) to evaluate outcome (GOS 1 = excellent, 2 = good, 3/4 = poor, and 5 = dead). Of the surviving patients, the outcome was excellent in 131 (74.0%), good in 22 (12.4%), and poor in 8 (4.5%) cases.
4. Discussion Giant aneurysms constitute 3–13.5% of all intracranial aneurysms, with an incidence averaging 5% in various series [1,6,8,10,15–17]. Here, we observed a slightly higher incidence of nearly 14%. However, in a series of 602 cases of Table 3 Causes of mortality Cause
Number of patients
Infarction Vasospasm Meningitis Spontaneous cerebellar hematoma Transfusion reaction Rupture of contralateral aneurysm
8 3 2 1 1 1
Table 4 Patient outcomes Treatment
Number
Clipping ICA lig Trap with bypass Trapping Wrapping Aneurysmorrhaphy
103 46 11 9 7 1
Total
177
Excellent
Good
Poor
Died
77 39 4 5 6 –
10 4 4 3 1 –
5 2 – – – 1
11 1 3 1 – –
131
22
8
16
Note: in patients on whom more than one surgical procedure was performed, the second procedure is taken into account while assessing outcome.
unruptured intracranial aneurysms reported by Solomon et al. 24% were GIAs [18]. The most common clinical presentation mentioned in previous reports is local mass effect [19,17,20,21]. It has been observed that 25–40% of GIAs present initially with SAH [2,15,10,20]. In our series, SAH was the most common presenting feature, found in two-thirds of the cases. This is in contrast to some previous reports, but is consistent with the report by Gewirtz et al. [22], which described 68% patients presenting with SAH. In a review, Hosobuchi [17] found that 30–80% of patients with GIAs present with SAH. Unruptured giant aneurysms have a higher probability of subsequent rupture and thrombosis, and giant size does not preclude rupture [2,15,16,23]. Intracranial giant aneurysms have a propensity to occur at certain locations. Our observation that 90% of all aneurysms are located in the anterior circulation and the single most common site of rupture of GIAs is the paraclinoid ICA is consistent with previous findings [2,8,19,24]. Drake [15] found vertebro-basilar aneurysms to be most common, a finding which can be explained by selective referrals according to his expertise and a special interest in posterior circulation aneurysms. A complete diagnostic workup is invaluable for proper therapeutic decision-making. The CT scan, MRI, and DSA (with different projections as indicated) are essential. A CT scan is better for detecting calcification, skull base erosion, and size evaluation of the aneurysm as well as the extent of the intramural clot [10,21,25]. MR imaging evaluates associated ischemia, perianeurysmal hemorrhage, and the aneurysm in relation to surrounding neurovascular and other critical structures, such as the brainstem [26]. We have found 3D DSA especially useful in planning surgery, as it permits visualization of the entire aneurysm (i.e., sac, neck, and parent vessel) from all directions. A virtual endoscopic view can also be obtained. This clearly demonstrates the extent of involvement of the parent artery and defines the residual neck [27]. We have obtained digital subtraction angiography in almost all of our patients, as it gives good anatomic pictures and status of collateral circulation. We have recently used Computed tomographic angiography (CTA) and magnetic resonance angiography (MRA) in many of our patients, which provide good images of most aneurysms and in selected cases allow surgical planning and execution without the need for catheter
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angiography. We believe that in the future, these may obviate the need for performing catheter angiography in many patients. The treatment strategy at our centre is decided jointly by a team consisting of Neurosurgeons and Neuroradiologists. It is imperative to carefully consider multiple factors before the mode of treatment is decided upon for an individual patient: clinical presentation, age of the patient, comorbid conditions, the location, morphology, and type of aneurysm (saccular, fusiform, mycotic, or traumatic), hemodynamic factors, and circulation within the normal brain. Pre-operative evaluation of cross-filling of anterior circulation, size, and patency of the posterior communicating artery, patency of the opposite vertebral artery, and appreciation of any anomaly or anatomic variation in circle of willis is important in planning a sound surgical strategy. The goals of aneurysm surgery are to eliminate the aneurysm from the intracranial circulation and maintain patency of the parent vessel and its branches. In our series,
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direct surgical clipping was typically performed as soon as possible, once all medical issues of the patient had been addressed and stabilized. The direct obliteration of the aneurysm with clipping was possible in the majority of our cases as in other series (see Figs. 1 and 2) [3,10,21,20,28]. Selection of the optimal surgical approach and early proximal and distal vascular control are critical to successful surgical treatment. The surgical approach chosen aims to maximize the operative exposure and depends upon the location of the aneurysm. Skull base approaches such as those involving medial petrosectomy, orbitozymatic osteotomy, and condylar resection allow visualization of the parent artery and its branches with minimal retraction [12]. Wide operative exposure using orbitozygomatic osteotomy, incision of the dural ring, resection of the lateral wall of the optic canal, optic strut, and the anterior clinoid process are useful in proximal ICA aneurysms [30,31]. Giant aneurysms require adequate deflation of the aneurysm sac prior to clipping (see Figs. 1 and 2) [20]. The aneurysm wall is dissected
Fig. 1. A 46-year-old male presented with a sudden severe headache and left hemiparesis. A non-contrast CT scan (A) revealed a subarachnoid hemorrhage and right temporal hematoma. Digital subtraction angiography (DSA) revealed a giant partially thrombosed MCA bifurcation aneurysm pointing laterally, inferiorly and anteriorly, with a pseudolobule (B, AP view; C, lateral view). 3D reconstruction image from the post-operative angiography (D) showed a well obliterated aneurysm and patent MCA branches. The patient had no focal deficits at the 2-year follow-up.
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Fig. 2. A 6-year-old boy presented with a sudden severe headache and loss of consciousness. A CT scan (A) revealed diffuse Fisher grade III subarachnoid hemorrhage and a rounded opacity in suprasellar cistern. DSA revealed a giant medially pointing left superior hypophyseal aneurysm (B, AP view; C, lateral view). The patient was operated and the aneurysm was clipped and excised. The post-operative angiogram (D) revealed no residual aneurysm and good filling of ICA branches.
and exposed generously. The aneurysm is trapped, and the thrombus is evacuated from the neck and the clip is then applied. When there is a risk of mass effect, GIAs may require opening and thrombus evacuation after they have been eliminated completely from circulation (see Fig. 2) [20]. Special techniques, such as temporary clipping, serial clipping, evacuation of intraluminal thrombus, tandem or serial fenestrated clipping, clip reconstruction, booster or reinforcing clips are often required. Circumferential excision of the fundus, leaving a 1-cm margin distal to the neck to provide an adequate cuff for subsequent reconstruction, may be required for some GIAs. Temporary proximal clipping softens the aneurysm, avoids premature rupture, permits visualization of perforators, and allows readjustment of the clip or multiple clips in tandem or parallel [3,5,32]. Temporary clipping was used in 52 patients in our series. In our experience, occlusion for less than 15 min and the use of barbiturates and phenytoin usually did not produce sequelae. Presence of flow in the arteries
distal to the trapped aneurysm on intraoperative microvascular Doppler suggested good collateral circulation. The parent artery occlusion time in such cases may be prolonged. However, in the absence of good collateral circulation, when the ischemic interval anticipated is 15–20 min, mild hypothermia (32–33 ◦ C) was used in addition to mannitol, barbiturates, and phenytoin. In one patient with a giant ICA aneurysm, a temporary clip had to be applied for more than 30 min, but because of good collateral circulation, there were no untoward sequelae. In all other patients, the temporary clip time was less then 15 min. A post-surgery CT scan was done on all patients within three days of surgery, or earlier depending upon the clinical situation. Many patients benefited from these CT scans. Post-operative hematomas, hydrocephalus, and infarcts were readily visualized on the CT scan. Five patients underwent VP shunts for post-operative hydrocephalus and three underwent decompressive craniectomy and duraplasty/partial lobectomy for large infarcts causing mass effect. In patients with
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well-established infarcts, triple-H therapy was stopped to avoid their hemorrhagic transformation or swelling. For ICA aneurysms, the surgical options are direct clipping, parent artery ligation, trapping with or without bypass, wrapping, or aneurysmorhaphy. For all other aneurysms, clipping is usually the first choice. Some aneurysms which are not clippable due to incorporation of branches can be treated with wrapping or trapping and a bypass procedure. A parent artery occlusion study at the time of angiography should be done to evaluate the collateral circulation and the possible need for EC–IC bypass, as prolonged temporary clipping may be required or the parent vessel may need permanent occlusion if the aneurysm cannot be clipped directly. In the absence of adequate collateral circulation, we favor revascularization procedures to restore CBF (see Fig. 3)
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[20,28]. In complex fusiform aneurysms, the saphenous vein or radial artery interposition graft, STA-MCA bypass or reimplantation of branches onto the parent artery may be required for preservation of CBF [3,30,33]. An indirect procedure to achieve aneurysm exclusion from the circulation is required in 20–40% of cases, which was also observed in the present series [20,28]. We treat giant cavernous ICA aneurysms with carotid ligation with/without bypass [20]. As seen in our study, internal carotid occlusion is a safe and effective therapeutic method in selected patients with adequate collaterals and should also be considered as an alternative to direct surgical clipping when the latter is deemed too risky [35]. Trapping allows decompression of the thrombus responsible for symptoms in cavernous carotid aneurysms with severe cranial neuropathy that are unresponsive to proximal occlu-
Fig. 3. Left ICA angiogram, lateral view (A) showing a giant, bilobed aneurysm involving cavernous, clinoidal and ophthalmic segments of the left ICA. The ophthalmic artery was arising from the superior lobule of the aneurysm. This 35-year-old woman underwent a left orbito-zygomatic craniotomy, an end-to-side ECA (ascending pharyngeal branch)-to-MCA (superior branch) bypass grafting using radial artery graft, and trapping of the aneurysm proximal to the posterior communicating artery, followed by ICA ligation. The post-operative CT scan (B) showed artifacts from the clip on ICA and radial artery graft. The post-operative check angiogram revealed good patency of the radial artery graft (C) and good filling of MCA branches from the bypass graft (D). The aneurysm was no longer visualized. At the 2-month follow-up, the patient had no neurological deficits.
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sion or in complex distal vertebral artery aneurysms with severe brainstem compression [5]. Twenty patients in our study underwent trapping of aneurysms with good results. Surgical mortality rates vary from 4–21% [8–10,15–17,20–22,28,29,34,36,37,39], averaging 10%, and are inversely proportional to the expertise and experience of the surgeon and operating team. The surgical mortality rate of 9% observed in our series is lower than the average reported in the literature. The most common complication was ischemia [8,10,15]. Excellent/good results in surgically treated patients have been reported in 63–85% of cases [9,16]. The slightly more favorable outcome in 86% of patients observed in our series probably reflects proper case selection, use of good diagnostic and neurosurgical techniques, an experienced surgical team, and a good clinical grade of patients at admission. Endovascular techniques are increasing in importance as alternative therapeutic options in patients with failed operative intervention, poor medical condition, and in surgically difficult (such as those with a heavily calcified neck) or inaccessible GIAs. However, the aneurysms that are most difficult surgically are the ones that offer the least possibility of a definitive endovascular cure [5,11–14]. Endovascular techniques may be used complementary to surgery, and integration of evolving endovascular technology into the microsurgical techniques, including revascularization, can yield the best results in complex giant aneurysms [4,24,37,38,40–42].
5. Conclusion It is concluded that 14% of all intracranial aneurysms are giant. SAH is the most common clinical presentation followed by features of a mass lesion. The cavernous ICA is the most commonly affected portion of the ICA. Direct surgical clipping is a safe and effective method of treatment and should be considered the first line of treatment whenever possible. With proper case selection, optimal radiological evaluation and appropriate surgical strategy, it is possible to achieve a favorable outcome in almost 90% of cases.
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