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Microsurgical clipping of large and giant cerebral aneurysms: A single-center contemporary experience
Journal of Clinical Neuroscience 21 (2014) 1424–1427
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Microsurgical clipping of large and giant cerebral aneurysms: A single-center contemporary experience Nohra Chalouhi a, Vismay Thakkar a, Stavropoula Tjoumakaris a, L. Fernando Gonzalez a, David Hasan b, Robert Rosenwasser a, Saurabh Singhal a, Pascal M. Jabbour a,⇑ a b
Department of Neurosurgery, Thomas Jefferson University and Jefferson Hospital for Neuroscience, 901 Walnut Street 3rd Floor, Philadelphia, PA 19107, USA Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
a r t i c l e
i n f o
Article history: Received 23 August 2013 Accepted 29 November 2013
Keywords: Aneurysms Giant aneurysms Large aneurysms Microsurgical clipping Subarachnoid hemorrhage
a b s t r a c t Several treatment strategies are available to manage large and giant cerebral aneurysms, including surgical, endovascular and combined approaches. We present our experience with microsurgical clipping of large and giant aneurysms. A total of 138 patients with 139 aneurysms of which 128 were large (P10 mm) and 11 were giant (P25 mm) were treated at our institution between 2004 and 2011. Data were collected from a prospectively maintained neurovascular database. Of 138 patients, 53 (38.4%) patients presented with subarachnoid hemorrhage (SAH). Peri-operative complications occurred in 16.7% of patients causing permanent morbidity in 4.4% and death in 0.7%. Complete occlusion, as evident on intra-operative angiography, was achieved in all clipped aneurysms (100%). Long-term follow-up angiography showed no recurrence (mean follow-up time, 43.9 months; range: 1–72 months). Favorable outcomes at discharge (Glasgow Outcome Scale score 4 or 5) were noted in 64.1% of SAH patients and 93% of non-SAH patients. Favorable outcomes at follow-up (mean follow up time, 42.5 months) were seen in 96% of patients. In our experience, microsurgical clipping of large and giant aneurysms carries low rates of morbidity and mortality with high rates of favorable outcomes. The excellent durability of surgical treatment stands in stark contrast with the high recurrence rates observed with coiling for this subset of aneurysms. These data suggest that microsurgical clipping continues to be a viable option that can be offered for patients with large and giant aneurysms. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction
2. Methods and materials
Large and giant aneurysms have a poor natural history and usually warrant intervention [1]. These aneurysms pose several challenges to both surgical and endovascular treatment. Endovascular coiling has been proposed as a minimally invasive alternative to surgical clipping for intracranial aneurysms but the rates of morbidity and mortality associated with coiling are not insignificant and angiographic outcomes are suboptimal at best [2,3]. Most surgical series of large and giant aneurysms were conducted more than a decade ago [4–7]. Recent advances in techniques and instrumentation have tremendously improved our ability to safely manage such aneurysms by microsurgical means. We report the results of a single-center contemporary series of large and giant intracranial aneurysms treated with microsurgery.
The study protocol was approved by the University Institutional Review Board. We searched our prospectively maintained database for all patients with large and giant aneurysms (P10 mm) undergoing surgical clipping between 2004 and 2011 at our institution. A total of 138 patients harboring 139 aneurysms were identified. During the same period, 334 large or giant aneurysms were treated by endovascular means (225 aneurysms with conventional coiling; 88 with stent-assisted coiling; 14 with parent vessel occlusion; and seven with balloon-assisted coiling) at our institution. Medical charts, angiographic studies, and CT scans were carefully reviewed. Patients’ age, sex, Hunt and Hess grades and aneurysm locations were recorded. Thromboembolic and ischemic complications were diagnosed clinically (new deficits or change in level of consciousness) or on CT scans or MRI (new infarcts) after excluding confounders such as vasospasm, hydrocephalus, and metabolic disorders. CT scans and MRI studies were typically performed in patients with sudden neurological compromise. Other
⇑ Corresponding author. Tel.: +1 21 5955 7000; fax: +1 21 5503 7038. E-mail address: [email protected] (P.M. Jabbour). http://dx.doi.org/10.1016/j.jocn.2013.11.052 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
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procedural complications, including epidural/subdural hematomas, infections, and post-operative seizures were also reported. Vasospasm was assessed by the development of a focal neurological deficit or change in level of consciousness with confirmatory transcranial Doppler, CT angiography, or digital subtraction angiography, as necessary, and exclusion of other causes. Clinical outcome was evaluated at time of discharge and at follow-up using the Glasgow Outcome Scale (GOS). GOS was determined based on patient’s neurological examination and functional status at discharge, and classified as follows: 1 = deceased, 2 = vegetative state, 3 = severely disabled, 4 = moderately disabled, and 5 = mildly or not disabled. Angiographic follow-up was scheduled at 5 years after the procedure. All procedures were performed by neurosurgeons trained in both microsurgical clipping and endovascular embolization. The decision to treat the aneurysm with microsurgery was based on factors including patient characteristics, aneurysm features, and operator preferences. Patients with a large intra-parenchymal hematoma underwent open surgery for aneurysm clipping and simultaneous clot evacuation and decompression. Patients with advanced age, multiple comorbidities, poor neurological grades, or posterior circulation aneurysms were often preferentially offered an endovascular procedure. Aneurysms with wide necks or unfavorable neck-to-dome ratio and in certain anatomical locations, most typically the middle cerebral artery and the anterior communicating artery, were generally clipped.
Table 1 Aneurysm location in patients with large and giant aneurysms treated with microsurgical clipping Vessel involved
Number
Carotid terminus Paraclinoid Ophthalmic Middle cerebral artery Anterior cerebral artery Anterior communicating artery Posterior communicating artery Vertebral Basilar Posterior inferior cerebellar artery
13 2 3 71 6 33 7 1 1 2
Table 2 Symptoms at presentation in the non-subarachnoid hemorrhage group of aneurysm patients with large and giant aneurysms treated with microsurgical clipping Presentation
% patients
Incidental Headaches Visual symptoms Limb paresthesias Seizures Previous transient ischemic attack/stroke
48 20 7 4 4 2
3.3. Microsurgical treatment 2.1. Surgical clipping
3. Results
Of 139 aneurysms, 135 were clipped whereas four aneurysms were wrapped. Complete aneurysm occlusion as assessed by intra-operative angiography was achieved in all clipped aneurysms (100%). Peri-operative complications occurred in 16.7% of patients (23/138) causing permanent morbidity in 4.4% (6/138) and death in 0.7% (1/138). New post-operative infarcts (within 72 hours of procedure) were found in nine (6.5%) patients; five caused only mild/transient morbidity (3.6%) and four (2.9%) lead to permanent morbidity. Intra-operative aneurysm rupture occurred in one (0.7%) patient (who also developed post-operative infarcts and died). Post-operative collection at the surgical site in the form of epidural or subdural hematoma was seen seven (5%) patients. Post-operative third or sixth nerve palsy was seen in three (2.2%) patients. Cerebrospinal fluid leakage during the post-operative period was diagnosed in three (2.2%) patients and resolved with appropriate surgical closure of the site of leakage. Non-procedural complications are summarized in Table 3.
3.1. Demographics and aneurysm characteristics
3.4. Follow-up clinical and angiographic outcomes
There were 82 (59%) female and 56 (41%) male patients. Mean patient age was 53 years (range: 14–79). Of 138 patients, 127 patients had a large aneurysm (P10 mm) and 11 had a giant aneurysm (P25 mm). Mean aneurysm size was 14.4 mm (range: 10–55 mm). One patient had two large aneurysms (10.3 mm and 23 mm) that were treated. One hundred thirty-five aneurysms (97%) were located in the anterior circulation and four (3%) in the posterior circulation (Table 1).
Seventy patients had a follow-up visit with a mean follow-up time of 42.5 months (range: 6–108 months). Sixty-seven patients (96%) had a favorable outcome (GOS 4 or 5) (Tables 4 and 5). Follow-up angiograms were obtained in 28 patients with a mean follow-up time of 43.9 months (range: 1–72 months). All 28 (100%) aneurysms remained completely occluded at follow-up. There were no episodes of new or recurrent subarachnoid hemorrhages at follow-up.
3.2. Clinical presentation
Table 3 Complications not related to procedure in patients with large and giant aneurysms treated with microsurgical clipping
The procedures were performed under general endotracheal anesthesia and administration of corticosteroids and diuretics. Continuous neurophysiological monitoring, including somatosensory evoked potentials, brainstem auditory evoked responses, and electroencephalography was performed in all patients; motor evoked potentials were monitored at the discretion of the primary surgeon. Different approaches were utilized depending on the location of the aneurysm and operator’s judgment. Patients were placed in burst suppression (six to eight bursts/minute) if temporary clipping was utilized and the mean arterial pressure increased by 10% from baseline. Intra-operative angiography was performed in all patients to document aneurysm obliteration, patency of the parent vessel, and the need for clip readjustment.
Fifty-three patients (38.4%) presented with subarachnoid hemorrhage. Hunt and Hess grades were I in 12 (22.6%) patients, II in nine (17%) patients, III in 20 (37.7%) patients, IV in nine (17%) patients, and V in three (5.7%) patients. Headache was the most common symptom found at presentation in patients with unruptured aneurysms (Table 2).
Complication
Number
Hydrocephalus requiring ventriculoperitoneal shunt Severe vasospasm requiring endovascular treatment Deep vein thrombosis Pulmonary embolism In-hospital seizures
25 8 9 2 3
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Table 4 Glasgow Outcome Scale (GOS) score at discharge in patients with large and giant aneurysms treated with microsurgical clipping GOS
1
2
3
4
5
SAH patients Non-SAH patients
7 3
0 0
12 3
10 11
24 68
SAH = subarachnoid hemorrhage.
Table 5 Hunt and Hess grade and outcomes in patients with large or giant aneurysms treated with microsurgical clipping HH grade
Total patients
Patients with favorable outcomes (GOS 4/5)
Patients with unfavorable outcomes (GOS 1/2/3)
1/2 3/4/5
21 32
95.2% (20 of 21) 43.8% (14 of 32)
4.8% (1 of 21) 56.2% (18 of 32)
GOS = Glasgow Outcome Scale score, HH = Hunt and Hess.
4. Discussion Previously, it was thought that larger aneurysms were less prone to rupture due to the concentric bands of thrombus that were believed to form a protective sheath. However, natural history studies demonstrated that the risk of aneurysm rupture increases significantly with aneurysm size [1,8]. The recently reported Japanese cohort showed that the annual risk of rupture of aneurysms larger than 10 mm was 4.37% and exceeded 33% for those larger than 25 mm [8]. Hence because of their poor natural history, large and giant aneurysms generally warrant intervention. The management of large intracranial aneurysms remains very challenging. Available treatment strategies available include open surgery, endovascular therapy, or a combined approach. Several factors are taken into account when considering treatment options, including patient age, comorbidities, preferences, and aneurysmal factors such as location, size, shape, neck-to-dome ratio, presence of intra-aneurysmal thrombus, aneurysm wall calcification, masseffect on adjacent neural structures, collateral circulation, and presence of critical perforating vessels emanating from the aneurysm wall. The goal of surgical treatment is complete aneurysm obliteration though direct surgical clipping of the aneurysm neck and decompression of the surrounding neural tissue along with preservation of cerebral perfusion and neurological function. Wrapping may be done along with clipping or as an isolated procedure when clipping is not possible due to calcified aneurysmal vessels or critical perforating vessels arising off the aneurysmal wall. In the present study, microsurgical clipping of large and giant aneurysms was performed with a low rate of permanent morbidity. More importantly, no patient had angiographic or clinical evidence of aneurysm recurrence and most patients achieved a satisfactory functional outcome. Similarly favorable results were also reported with microsurgical clipping in experienced hands [9–13]. In the Peerless and Drake series, the mortality rate was 14% and good outcomes were achieved in 58% [11]. Sughrue et al. [11] from the University of California, San Francisco reported on 140 patients with 141 giant aneurysms treated surgically (71% in the anterior circulation) and reported complete or near-complete aneurysm occlusion in 88% with a surgical mortality of 13%. Favorable outcomes at follow-up were seen in 81% of patients. The authors noted a heavy reliance on bypass techniques (in 38%) obviating the need for hypothermic circulatory arrest. They concluded that in experienced hands, excellent results may be achieved with surgery as the ‘‘first-line’’ management approach for such aneurysms. Hauck et al. [14] reviewed clinical data on 62 patients who underwent surgery for unruptured aneurysms (20–60 mm) and reported complete aneurysm occlusion in 90% of patients and near complete occlusion in 5%. The surgical risk in patients younger than 50 years of age was 8% and the risk
increased with advancing age. In a large study of 181 patients, Sharma et al. [15] reported a mortality rate of 9% and a morbidity rate of 12% for giant aneurysms treated surgically with favorable outcomes in 86% of patients. The better results in our series may be related to the inclusion of large aneurysms (which have a lower risk than giant aneurysms) as well as patient selection and technical advancements. Fundamental principles of aneurysm surgery are important to follow during the treatment of such difficult aneurysms. Careful pre-operative planning is of utmost importance. Identification of the aneurysm neck is also very important for successful clipping of a large or giant aneurysm. Preceding temporary proximal and distal flow control helps to soften the aneurysm, allowing better visualization and handling of the aneurysm, thereby decreasing the chances of intra-operative rupture. Flow control also allows the surgeon to perform suction decompression of the aneurysm, aneurysmorrhaphy or aneurysmectomy, when necessary. The clips should be applied perpendicular to the neck of aneurysm and parallel to the parent vessel so as to reduce the risk of inclusion or kinking of the parent vessel into the clip. Care should be taken to avoid inclusion of adherent perforators within the clip. A single large clip applied at the neck of the aneurysm may sometimes prove to be insufficient, especially when the aneurysmal surface is calcified. In this case, the large clip is first applied to the neck, followed by sequential clips down the neck. Thrombus inside the aneurysm may become dislodged to distal arteries while clips are placed. Suction decompression of the aneurysm, aneurysmorrhaphy or aneurysmectomy may help prevent thrombus migration. This also helps to decompress the adjacent neural structures with improvement in compressive symptoms. Once the aneurysm is clipped, indocyanine green angiography or preferably intra-operative digital subtraction angiography (the gold standard) is performed to ascertain optimum occlusion of the aneurysm and patency of the parent and branching vessel [16]. Other surgical approaches include permanent surgical trapping of the proximal parent vessel. This results in thrombosis of the aneurysm through altered intracranial hemodynamics [17]. This treatment can be used only after the patient tolerates a balloon occlusion test because the risk of stroke is as high as 33% in unselected parent vessel sacrifice [18–20]. If a patient does not tolerate the balloon occlusion test, an extracranial–intracranial bypass is required before parent vessel takedown. Proximal vessel sacrifice can also be performed endovascularly with coils alone or recently with a combination of Onyx (ev3 Endovascular, Plymouth, MN, USA) and coils [17,21]. The latter technique appears to reduce the number of coils needed to achieve vessel occlusion, with excellent angiographic and clinical outcomes [21]. 4.1. Microsurgery versus endovascular strategies Endovascular therapy is a well-established treatment for cerebral aneurysms [22–25]. Microsurgery, however, has several advantages over endovascular coiling when it comes to large and giant aneurysms. Higher rates of complete immediate occlusion Excellent durability with exceedingly low recurrence and retreatment rates Allows the surgeon to deflate the aneurysm, remove the thrombus and decompress the surrounding neural tissue. This is most beneficial in patients with compressive symptoms. It should be noted that coiling may also promote satisfactory rates of nerve recovery [26] Subarachnoid blood and blood clots surrounding the ruptured aneurysm can be evacuated Wide necked and complex giant aneurysms can be occluded, which is usually not the case with coiling
N. Chalouhi et al. / Journal of Clinical Neuroscience 21 (2014) 1424–1427
The disadvantages of microsurgery may include a somewhat higher complication rate than coiling, the invasive nature of the procedure, and the risk of injury to neural structures during aneurysm clipping. Coiling of large and giant aneurysms, while commonly employed, has several limitations. Regrowth, reopening and coil compaction are common with endovascular coiling occurring in up to 40% of patients, and follow-up imaging at regular intervals is mandatory [2]. Retreatment rates are also very high and may be cost-prohibitive. Flow diverters have recently been proposed as a more physiologic endovascular treatment of intracranial aneurysms [27–34]. The Pipeline Embolization Device (ev3 Endovascular) is a flow diverter that has gained USA Food and Drug Administration approval for treatment of large and giant aneurysms of the internal carotid artery. Dual antiplatelet (aspirin and clopidogrel) therapy is needed before Pipeline Embolization Device deployment which limits the use of such devices to unruptured aneurysms [35]. Although large and giant aneurysms that are unruptured (except anterior communicating and middle cerebral artery aneurysms) can be treated with flow diversion with favorable clinical and angiographic outcomes, surgical clipping continues to be a good alternative in experienced hands (especially for the middle cerebral artery and anterior communicating artery). Ruptured large and giant aneurysms are not candidates for flow diversion and can either be coiled or clipped. Aneurysms with wide necks, unfavorable morphology for coiling, and those arising from the middle cerebral artery and the anterior communicating artery are typical surgical candidates. Their management needs to be tailored to the individual circumstances of the patient. Aneurysm location, comorbidities, and patient preferences will help determine the best treatment strategy. 4.2. Limitations This study is retrospective and reflects the experience of a single tertiary center. Whether these favorable results can be replicated in smaller centers remains an unanswered question. We also did not include a control group, which precludes any recommendation as to the best treatment strategy in this setting. Low morbidity rates and excellent clinical and angiographic outcomes were achieved with microsurgery in the present study. The excellent durability of surgical treatment stands in stark contrast with the high recurrence rates observed with endovascular coiling. Thus, microsurgical clipping continues to be a viable option that could be offered for patients with large and giant aneurysms. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] ISUIA Investigators. Unruptured intracranial aneurysms–risk of rupture and risks of surgical intervention. International Study of Unruptured Intracranial Aneurysms Investigators. N Engl J Med 1998;339:1725–33. [2] Parkinson RJ, Eddleman CS, Batjer HH, et al. Giant intracranial aneurysms: endovascular challenges. Neurosurgery 2008;62:1336–45. [3] Murayama Y, Nien YL, Duckwiler G, et al. Guglielmi detachable coil embolization of cerebral aneurysms: 11 years’ experience. J Neurosurg 2003;98:959–66. [4] Ausman JI, Diaz FG, Sadasivan B, et al. Giant intracranial aneurysm surgery: the role of microvascular reconstruction. Surg Neurol 1990;34:8–15. [5] Kodama N, Suzuki J. Surgical treatment of giant aneurysms. Neurosurg Rev 1982;5:155–60. [6] Lawton MT, Spetzler RF. Surgical management of giant intracranial aneurysms: experience with 171 patients. Clin Neurosurg 1995;42:245–66.
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[7] Symon L, Vajda J. Surgical experiences with giant intracranial aneurysms. J Neurosurg 1984;61:1009–28. [8] UCAS Japan Investigators, Morita A, Kirino T, et al. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med 2012;366:2474–82. [9] Rodríguez-Hernández A, Sughrue ME, Akhavan S, et al. Current management of middle cerebral artery aneurysms: surgical results with a ‘‘clip first’’ policy. Neurosurgery 2013;72:415–27. [10] Sanai N, Caldwell N, Englot DJ, et al. Advanced technical skills are required for microsurgical clipping of posterior communicating artery aneurysms in the endovascular era. Neurosurgery 2012;71:285–94 [discussion 294–285]. [11] Sughrue ME, Saloner D, Rayz VL. Giant intracranial aneurysms: evolution of management in a contemporary surgical series. Neurosurgery 2011;69: 1261–70 [discussion 1270–1]. [12] van Dijk JM, Groen RJ, Ter Laan M, et al. Surgical clipping as the preferred treatment for aneurysms of the middle cerebral artery. Acta Neurochir (Wien) 2011;153:2111–7. [13] Aydin Y, Cavusßog˘lu H, Kahyaog˘lu O, et al. Clip ligation of unruptured intracranial aneurysms: a prospective midterm outcome study. Acta Neurochir (Wien) 2012;154:1135–44. [14] Hauck EF, Wohlfeld B, Welch BG, et al. Clipping of very large or giant unruptured intracranial aneurysms in the anterior circulation: an outcome study. J Neurosurg 2008;109:1012–8. [15] Sharma BS, Gupta A, Ahmad FU, et al. Surgical management of giant intracranial aneurysms. Clin Neurol Neurosurg 2008;110:674–81. [16] Chalouhi N, Theofanis T, Jabbour P, et al. Safety and efficacy of intraoperative angiography in craniotomies for cerebral aneurysms and arteriovenous malformations: a review of 1093 consecutive cases. Neurosurgery 2012;71: 1162–9. [17] Elhammady MS, Wolfe SQ, Farhat H, et al. Carotid artery sacrifice for unclippable and uncoilable aneurysms: endovascular occlusion vs common carotid artery ligation. Neurosurgery 2010;67:1431–6 [discussion 1437]. [18] Serbinenko FA. Balloon catheterization and occlusion of major cerebral vessels. J Neurosurg 1974;41:125–45. [19] American Society of Interventional and Therapeutic Neuroradiology. Carotid artery balloon test occlusion. AJNR Am J Neuroradiol 2001;22:S8–9. [20] Sorteberg A, Bakke SJ, Boysen M, et al. Angiographic balloon test occlusion and therapeutic sacrifice of major arteries to the brain. Neurosurgery 2008;63:651–60 [dicussion 660–1]. [21] Chalouhi N, Starke RM, Tjoumakaris SI, et al. Carotid and vertebral artery sacrifice with a combination of Onyx and coils: technical note and case series. Neuroradiology 2013;55:993–8. [22] Chen Z, Yang Y, Miao H, et al. Experiences and complications in endovascular treatment of paraclinoid aneurysms. J Clin Neurosci 2013;20:1259–63. [23] Hwang SK, Hwang G, Bang JS, et al. Endovascular Enterprise stent-assisted coil embolization for wide-necked unruptured intracranial aneurysms. J Clin Neurosci 2013;20:1276–9. [24] Kim KH, Cha KC, Kim JS. Endovascular coiling of middle cerebral artery aneurysms as an alternative to surgical clipping. J Clin Neurosci 2013;20: 520–2. [25] Bose RS, Dowling RJ, Yan B, et al. A single centre study of coil embolization of intracranial aneurysms comparing bare platinum and PGLA-coated coils. J Clin Neurosci 2012;19:271–6. [26] Chalouhi N, Theofanis T, Jabbour P, et al. Endovascular treatment of posterior communicating artery aneurysms with oculomotor nerve palsy: clinical outcomes and predictors of nerve recovery. AJNR Am J Neuroradiol 2013;34: 828–32. [27] Chalouhi N, McMahon JF, Moukarzel LA, et al. Flow diversion versus traditional aneurysm embolization strategies: analysis of fluoroscopy and procedure times. J Neurointerv Surg 2013 [Epub ahead of print]. [28] Jabbour P, Chalouhi N, Tjoumakaris S, et al. The pipeline embolization device: learning curve and predictors of complications and aneurysm obliteration. Neurosurgery 2013;73:113–20. [29] Chitale R, Gonzalez LF, Randazzo C, et al. Single center experience with pipeline stent: feasibility, technique, and complications. Neurosurgery 2012;71:679–91 [discussion 691]. [30] Becske T, Kallmes DF, Saatci I, et al. Pipeline for uncoilable or failed aneurysms: results from a multicenter clinical trial. Radiology 2013;267:858–68. [31] Yu SC, Kwok CK, Cheng PW, et al. Intracranial aneurysms: midterm outcome of pipeline embolization device–a prospective study in 143 patients with 178 aneurysms. Radiology 2012;265:893–901. [32] Kan P, Siddiqui AH, Veznedaroglu E, et al. Early postmarket results after treatment of intracranial aneurysms with the pipeline embolization device: a U.S. multicenter experience. Neurosurgery 2012;71:1080–7 [discussion 1087– 1088]. [33] O’Kelly CJ, Spears J, Chow M, et al. Canadian experience with the pipeline embolization device for repair of unruptured intracranial aneurysms. AJNR Am J Neuroradiol 2013;34:381–7. [34] Saatci I, Yavuz K, Ozer C, et al. Treatment of intracranial aneurysms using the pipeline flow-diverter embolization device: a single-center experience with long-term follow-up results. AJNR Am J Neuroradiol 2012;33: 1436–46. [35] Cruz JP, O’Kelly C, Kelly M, et al. Pipeline embolization device in aneurysmal subarachnoid hemorrhage. AJNR Am J Neuroradiol 2013;34:271–6.
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Microsurgical clipping of large and giant cerebral aneurysms: A single-center contemporary experience Nohra Chalouhi a, Vismay Thakkar a, Stavropoula Tjoumakaris a, L. Fernando Gonzalez a, David Hasan b, Robert Rosenwasser a, Saurabh Singhal a, Pascal M. Jabbour a,⇑ a b
Department of Neurosurgery, Thomas Jefferson University and Jefferson Hospital for Neuroscience, 901 Walnut Street 3rd Floor, Philadelphia, PA 19107, USA Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
a r t i c l e
i n f o
Article history: Received 23 August 2013 Accepted 29 November 2013
Keywords: Aneurysms Giant aneurysms Large aneurysms Microsurgical clipping Subarachnoid hemorrhage
a b s t r a c t Several treatment strategies are available to manage large and giant cerebral aneurysms, including surgical, endovascular and combined approaches. We present our experience with microsurgical clipping of large and giant aneurysms. A total of 138 patients with 139 aneurysms of which 128 were large (P10 mm) and 11 were giant (P25 mm) were treated at our institution between 2004 and 2011. Data were collected from a prospectively maintained neurovascular database. Of 138 patients, 53 (38.4%) patients presented with subarachnoid hemorrhage (SAH). Peri-operative complications occurred in 16.7% of patients causing permanent morbidity in 4.4% and death in 0.7%. Complete occlusion, as evident on intra-operative angiography, was achieved in all clipped aneurysms (100%). Long-term follow-up angiography showed no recurrence (mean follow-up time, 43.9 months; range: 1–72 months). Favorable outcomes at discharge (Glasgow Outcome Scale score 4 or 5) were noted in 64.1% of SAH patients and 93% of non-SAH patients. Favorable outcomes at follow-up (mean follow up time, 42.5 months) were seen in 96% of patients. In our experience, microsurgical clipping of large and giant aneurysms carries low rates of morbidity and mortality with high rates of favorable outcomes. The excellent durability of surgical treatment stands in stark contrast with the high recurrence rates observed with coiling for this subset of aneurysms. These data suggest that microsurgical clipping continues to be a viable option that can be offered for patients with large and giant aneurysms. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction
2. Methods and materials
Large and giant aneurysms have a poor natural history and usually warrant intervention [1]. These aneurysms pose several challenges to both surgical and endovascular treatment. Endovascular coiling has been proposed as a minimally invasive alternative to surgical clipping for intracranial aneurysms but the rates of morbidity and mortality associated with coiling are not insignificant and angiographic outcomes are suboptimal at best [2,3]. Most surgical series of large and giant aneurysms were conducted more than a decade ago [4–7]. Recent advances in techniques and instrumentation have tremendously improved our ability to safely manage such aneurysms by microsurgical means. We report the results of a single-center contemporary series of large and giant intracranial aneurysms treated with microsurgery.
The study protocol was approved by the University Institutional Review Board. We searched our prospectively maintained database for all patients with large and giant aneurysms (P10 mm) undergoing surgical clipping between 2004 and 2011 at our institution. A total of 138 patients harboring 139 aneurysms were identified. During the same period, 334 large or giant aneurysms were treated by endovascular means (225 aneurysms with conventional coiling; 88 with stent-assisted coiling; 14 with parent vessel occlusion; and seven with balloon-assisted coiling) at our institution. Medical charts, angiographic studies, and CT scans were carefully reviewed. Patients’ age, sex, Hunt and Hess grades and aneurysm locations were recorded. Thromboembolic and ischemic complications were diagnosed clinically (new deficits or change in level of consciousness) or on CT scans or MRI (new infarcts) after excluding confounders such as vasospasm, hydrocephalus, and metabolic disorders. CT scans and MRI studies were typically performed in patients with sudden neurological compromise. Other
⇑ Corresponding author. Tel.: +1 21 5955 7000; fax: +1 21 5503 7038. E-mail address: [email protected] (P.M. Jabbour). http://dx.doi.org/10.1016/j.jocn.2013.11.052 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
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N. Chalouhi et al. / Journal of Clinical Neuroscience 21 (2014) 1424–1427
procedural complications, including epidural/subdural hematomas, infections, and post-operative seizures were also reported. Vasospasm was assessed by the development of a focal neurological deficit or change in level of consciousness with confirmatory transcranial Doppler, CT angiography, or digital subtraction angiography, as necessary, and exclusion of other causes. Clinical outcome was evaluated at time of discharge and at follow-up using the Glasgow Outcome Scale (GOS). GOS was determined based on patient’s neurological examination and functional status at discharge, and classified as follows: 1 = deceased, 2 = vegetative state, 3 = severely disabled, 4 = moderately disabled, and 5 = mildly or not disabled. Angiographic follow-up was scheduled at 5 years after the procedure. All procedures were performed by neurosurgeons trained in both microsurgical clipping and endovascular embolization. The decision to treat the aneurysm with microsurgery was based on factors including patient characteristics, aneurysm features, and operator preferences. Patients with a large intra-parenchymal hematoma underwent open surgery for aneurysm clipping and simultaneous clot evacuation and decompression. Patients with advanced age, multiple comorbidities, poor neurological grades, or posterior circulation aneurysms were often preferentially offered an endovascular procedure. Aneurysms with wide necks or unfavorable neck-to-dome ratio and in certain anatomical locations, most typically the middle cerebral artery and the anterior communicating artery, were generally clipped.
Table 1 Aneurysm location in patients with large and giant aneurysms treated with microsurgical clipping Vessel involved
Number
Carotid terminus Paraclinoid Ophthalmic Middle cerebral artery Anterior cerebral artery Anterior communicating artery Posterior communicating artery Vertebral Basilar Posterior inferior cerebellar artery
13 2 3 71 6 33 7 1 1 2
Table 2 Symptoms at presentation in the non-subarachnoid hemorrhage group of aneurysm patients with large and giant aneurysms treated with microsurgical clipping Presentation
% patients
Incidental Headaches Visual symptoms Limb paresthesias Seizures Previous transient ischemic attack/stroke
48 20 7 4 4 2
3.3. Microsurgical treatment 2.1. Surgical clipping
3. Results
Of 139 aneurysms, 135 were clipped whereas four aneurysms were wrapped. Complete aneurysm occlusion as assessed by intra-operative angiography was achieved in all clipped aneurysms (100%). Peri-operative complications occurred in 16.7% of patients (23/138) causing permanent morbidity in 4.4% (6/138) and death in 0.7% (1/138). New post-operative infarcts (within 72 hours of procedure) were found in nine (6.5%) patients; five caused only mild/transient morbidity (3.6%) and four (2.9%) lead to permanent morbidity. Intra-operative aneurysm rupture occurred in one (0.7%) patient (who also developed post-operative infarcts and died). Post-operative collection at the surgical site in the form of epidural or subdural hematoma was seen seven (5%) patients. Post-operative third or sixth nerve palsy was seen in three (2.2%) patients. Cerebrospinal fluid leakage during the post-operative period was diagnosed in three (2.2%) patients and resolved with appropriate surgical closure of the site of leakage. Non-procedural complications are summarized in Table 3.
3.1. Demographics and aneurysm characteristics
3.4. Follow-up clinical and angiographic outcomes
There were 82 (59%) female and 56 (41%) male patients. Mean patient age was 53 years (range: 14–79). Of 138 patients, 127 patients had a large aneurysm (P10 mm) and 11 had a giant aneurysm (P25 mm). Mean aneurysm size was 14.4 mm (range: 10–55 mm). One patient had two large aneurysms (10.3 mm and 23 mm) that were treated. One hundred thirty-five aneurysms (97%) were located in the anterior circulation and four (3%) in the posterior circulation (Table 1).
Seventy patients had a follow-up visit with a mean follow-up time of 42.5 months (range: 6–108 months). Sixty-seven patients (96%) had a favorable outcome (GOS 4 or 5) (Tables 4 and 5). Follow-up angiograms were obtained in 28 patients with a mean follow-up time of 43.9 months (range: 1–72 months). All 28 (100%) aneurysms remained completely occluded at follow-up. There were no episodes of new or recurrent subarachnoid hemorrhages at follow-up.
3.2. Clinical presentation
Table 3 Complications not related to procedure in patients with large and giant aneurysms treated with microsurgical clipping
The procedures were performed under general endotracheal anesthesia and administration of corticosteroids and diuretics. Continuous neurophysiological monitoring, including somatosensory evoked potentials, brainstem auditory evoked responses, and electroencephalography was performed in all patients; motor evoked potentials were monitored at the discretion of the primary surgeon. Different approaches were utilized depending on the location of the aneurysm and operator’s judgment. Patients were placed in burst suppression (six to eight bursts/minute) if temporary clipping was utilized and the mean arterial pressure increased by 10% from baseline. Intra-operative angiography was performed in all patients to document aneurysm obliteration, patency of the parent vessel, and the need for clip readjustment.
Fifty-three patients (38.4%) presented with subarachnoid hemorrhage. Hunt and Hess grades were I in 12 (22.6%) patients, II in nine (17%) patients, III in 20 (37.7%) patients, IV in nine (17%) patients, and V in three (5.7%) patients. Headache was the most common symptom found at presentation in patients with unruptured aneurysms (Table 2).
Complication
Number
Hydrocephalus requiring ventriculoperitoneal shunt Severe vasospasm requiring endovascular treatment Deep vein thrombosis Pulmonary embolism In-hospital seizures
25 8 9 2 3
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Table 4 Glasgow Outcome Scale (GOS) score at discharge in patients with large and giant aneurysms treated with microsurgical clipping GOS
1
2
3
4
5
SAH patients Non-SAH patients
7 3
0 0
12 3
10 11
24 68
SAH = subarachnoid hemorrhage.
Table 5 Hunt and Hess grade and outcomes in patients with large or giant aneurysms treated with microsurgical clipping HH grade
Total patients
Patients with favorable outcomes (GOS 4/5)
Patients with unfavorable outcomes (GOS 1/2/3)
1/2 3/4/5
21 32
95.2% (20 of 21) 43.8% (14 of 32)
4.8% (1 of 21) 56.2% (18 of 32)
GOS = Glasgow Outcome Scale score, HH = Hunt and Hess.
4. Discussion Previously, it was thought that larger aneurysms were less prone to rupture due to the concentric bands of thrombus that were believed to form a protective sheath. However, natural history studies demonstrated that the risk of aneurysm rupture increases significantly with aneurysm size [1,8]. The recently reported Japanese cohort showed that the annual risk of rupture of aneurysms larger than 10 mm was 4.37% and exceeded 33% for those larger than 25 mm [8]. Hence because of their poor natural history, large and giant aneurysms generally warrant intervention. The management of large intracranial aneurysms remains very challenging. Available treatment strategies available include open surgery, endovascular therapy, or a combined approach. Several factors are taken into account when considering treatment options, including patient age, comorbidities, preferences, and aneurysmal factors such as location, size, shape, neck-to-dome ratio, presence of intra-aneurysmal thrombus, aneurysm wall calcification, masseffect on adjacent neural structures, collateral circulation, and presence of critical perforating vessels emanating from the aneurysm wall. The goal of surgical treatment is complete aneurysm obliteration though direct surgical clipping of the aneurysm neck and decompression of the surrounding neural tissue along with preservation of cerebral perfusion and neurological function. Wrapping may be done along with clipping or as an isolated procedure when clipping is not possible due to calcified aneurysmal vessels or critical perforating vessels arising off the aneurysmal wall. In the present study, microsurgical clipping of large and giant aneurysms was performed with a low rate of permanent morbidity. More importantly, no patient had angiographic or clinical evidence of aneurysm recurrence and most patients achieved a satisfactory functional outcome. Similarly favorable results were also reported with microsurgical clipping in experienced hands [9–13]. In the Peerless and Drake series, the mortality rate was 14% and good outcomes were achieved in 58% [11]. Sughrue et al. [11] from the University of California, San Francisco reported on 140 patients with 141 giant aneurysms treated surgically (71% in the anterior circulation) and reported complete or near-complete aneurysm occlusion in 88% with a surgical mortality of 13%. Favorable outcomes at follow-up were seen in 81% of patients. The authors noted a heavy reliance on bypass techniques (in 38%) obviating the need for hypothermic circulatory arrest. They concluded that in experienced hands, excellent results may be achieved with surgery as the ‘‘first-line’’ management approach for such aneurysms. Hauck et al. [14] reviewed clinical data on 62 patients who underwent surgery for unruptured aneurysms (20–60 mm) and reported complete aneurysm occlusion in 90% of patients and near complete occlusion in 5%. The surgical risk in patients younger than 50 years of age was 8% and the risk
increased with advancing age. In a large study of 181 patients, Sharma et al. [15] reported a mortality rate of 9% and a morbidity rate of 12% for giant aneurysms treated surgically with favorable outcomes in 86% of patients. The better results in our series may be related to the inclusion of large aneurysms (which have a lower risk than giant aneurysms) as well as patient selection and technical advancements. Fundamental principles of aneurysm surgery are important to follow during the treatment of such difficult aneurysms. Careful pre-operative planning is of utmost importance. Identification of the aneurysm neck is also very important for successful clipping of a large or giant aneurysm. Preceding temporary proximal and distal flow control helps to soften the aneurysm, allowing better visualization and handling of the aneurysm, thereby decreasing the chances of intra-operative rupture. Flow control also allows the surgeon to perform suction decompression of the aneurysm, aneurysmorrhaphy or aneurysmectomy, when necessary. The clips should be applied perpendicular to the neck of aneurysm and parallel to the parent vessel so as to reduce the risk of inclusion or kinking of the parent vessel into the clip. Care should be taken to avoid inclusion of adherent perforators within the clip. A single large clip applied at the neck of the aneurysm may sometimes prove to be insufficient, especially when the aneurysmal surface is calcified. In this case, the large clip is first applied to the neck, followed by sequential clips down the neck. Thrombus inside the aneurysm may become dislodged to distal arteries while clips are placed. Suction decompression of the aneurysm, aneurysmorrhaphy or aneurysmectomy may help prevent thrombus migration. This also helps to decompress the adjacent neural structures with improvement in compressive symptoms. Once the aneurysm is clipped, indocyanine green angiography or preferably intra-operative digital subtraction angiography (the gold standard) is performed to ascertain optimum occlusion of the aneurysm and patency of the parent and branching vessel [16]. Other surgical approaches include permanent surgical trapping of the proximal parent vessel. This results in thrombosis of the aneurysm through altered intracranial hemodynamics [17]. This treatment can be used only after the patient tolerates a balloon occlusion test because the risk of stroke is as high as 33% in unselected parent vessel sacrifice [18–20]. If a patient does not tolerate the balloon occlusion test, an extracranial–intracranial bypass is required before parent vessel takedown. Proximal vessel sacrifice can also be performed endovascularly with coils alone or recently with a combination of Onyx (ev3 Endovascular, Plymouth, MN, USA) and coils [17,21]. The latter technique appears to reduce the number of coils needed to achieve vessel occlusion, with excellent angiographic and clinical outcomes [21]. 4.1. Microsurgery versus endovascular strategies Endovascular therapy is a well-established treatment for cerebral aneurysms [22–25]. Microsurgery, however, has several advantages over endovascular coiling when it comes to large and giant aneurysms. Higher rates of complete immediate occlusion Excellent durability with exceedingly low recurrence and retreatment rates Allows the surgeon to deflate the aneurysm, remove the thrombus and decompress the surrounding neural tissue. This is most beneficial in patients with compressive symptoms. It should be noted that coiling may also promote satisfactory rates of nerve recovery [26] Subarachnoid blood and blood clots surrounding the ruptured aneurysm can be evacuated Wide necked and complex giant aneurysms can be occluded, which is usually not the case with coiling
N. Chalouhi et al. / Journal of Clinical Neuroscience 21 (2014) 1424–1427
The disadvantages of microsurgery may include a somewhat higher complication rate than coiling, the invasive nature of the procedure, and the risk of injury to neural structures during aneurysm clipping. Coiling of large and giant aneurysms, while commonly employed, has several limitations. Regrowth, reopening and coil compaction are common with endovascular coiling occurring in up to 40% of patients, and follow-up imaging at regular intervals is mandatory [2]. Retreatment rates are also very high and may be cost-prohibitive. Flow diverters have recently been proposed as a more physiologic endovascular treatment of intracranial aneurysms [27–34]. The Pipeline Embolization Device (ev3 Endovascular) is a flow diverter that has gained USA Food and Drug Administration approval for treatment of large and giant aneurysms of the internal carotid artery. Dual antiplatelet (aspirin and clopidogrel) therapy is needed before Pipeline Embolization Device deployment which limits the use of such devices to unruptured aneurysms [35]. Although large and giant aneurysms that are unruptured (except anterior communicating and middle cerebral artery aneurysms) can be treated with flow diversion with favorable clinical and angiographic outcomes, surgical clipping continues to be a good alternative in experienced hands (especially for the middle cerebral artery and anterior communicating artery). Ruptured large and giant aneurysms are not candidates for flow diversion and can either be coiled or clipped. Aneurysms with wide necks, unfavorable morphology for coiling, and those arising from the middle cerebral artery and the anterior communicating artery are typical surgical candidates. Their management needs to be tailored to the individual circumstances of the patient. Aneurysm location, comorbidities, and patient preferences will help determine the best treatment strategy. 4.2. Limitations This study is retrospective and reflects the experience of a single tertiary center. Whether these favorable results can be replicated in smaller centers remains an unanswered question. We also did not include a control group, which precludes any recommendation as to the best treatment strategy in this setting. Low morbidity rates and excellent clinical and angiographic outcomes were achieved with microsurgery in the present study. The excellent durability of surgical treatment stands in stark contrast with the high recurrence rates observed with endovascular coiling. Thus, microsurgical clipping continues to be a viable option that could be offered for patients with large and giant aneurysms. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] ISUIA Investigators. Unruptured intracranial aneurysms–risk of rupture and risks of surgical intervention. International Study of Unruptured Intracranial Aneurysms Investigators. N Engl J Med 1998;339:1725–33. [2] Parkinson RJ, Eddleman CS, Batjer HH, et al. Giant intracranial aneurysms: endovascular challenges. Neurosurgery 2008;62:1336–45. [3] Murayama Y, Nien YL, Duckwiler G, et al. Guglielmi detachable coil embolization of cerebral aneurysms: 11 years’ experience. J Neurosurg 2003;98:959–66. [4] Ausman JI, Diaz FG, Sadasivan B, et al. Giant intracranial aneurysm surgery: the role of microvascular reconstruction. Surg Neurol 1990;34:8–15. [5] Kodama N, Suzuki J. Surgical treatment of giant aneurysms. Neurosurg Rev 1982;5:155–60. [6] Lawton MT, Spetzler RF. Surgical management of giant intracranial aneurysms: experience with 171 patients. Clin Neurosurg 1995;42:245–66.
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