OPERATIVE NUANCES Long-term Patient Outcomes After Microsurgical Treatment of Blister-Like Aneurysms of the Basilar Artery BACKGROUND: Blister-like aneurysms (BLAs) are challenging lesions that require unique microsurgical strategies. BLAs are predominantly found along the internal carotid artery; however, BLAs of the basilar artery are a rare subset that requires a modified treatment strategy. OBJECTIVE: To discuss the microsurgical management and review the long-term outcomes of patients with BLAs of the basilar artery. METHODS: We retrospectively reviewed the surgical technique, postoperative results, and long-term outcomes of all patients with basilar artery BLAs treated at our institution from 2005 to 2011. RESULTS: Four patients with basilar artery BLAs were identified over this 6-year interval. All 4 patients were treated by direct microsurgical clipping. A thin layer of cotton reinforcement was used beneath the clip tines to minimize the risk of clip slippage in 2 of 4 patients; 1 patient required adjunctive endovascular stent placement for residual aneurysm after clipping. Complete obliteration of all aneurysms was achieved, and there has been no recurrence at mean clinical follow-up of 72 months (median, 74.5; range, 37-103) and imaging follow-up of 48 months (median, 54; range 12-72). CONCLUSION: Direct clipping with or without cotton reinforcement can obliterate basilar BLAs with excellent long-term outcomes. Clip wrapping is not an option for these lesions given the proximity to perforating branches. Endovascular techniques provide a useful adjunctive strategy; however, risks with antiplatelet therapy in the acute subarachnoid hemorrhage period must be considered. Michael A. Mooney, MD M. Yashar S. Kalani, MD, PhD Peter Nakaji, MD Felipe C. Albuquerque, MD Cameron G. McDougall, MD Robert F. Spetzler, MD Joseph M. Zabramski, MD Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona Correspondence: Joseph M. Zabramski, MD, c/o Neuroscience Publications, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, 350 W Thomas Rd, Phoenix, AZ 85013. E-mail: neuropub@dignityhealth.org Received, December 29, 2014. Accepted, May 20, 2015. Published Online, June 25, 2015. KEY WORDS: Aneurysm, Basilar artery, Blister, Clipping, Endovascular Copyright © 2015 by the Congress of Neurological Surgeons. Operative Neurosurgery 11:387–393, 2015 B lister-like aneurysms (BLAs) are small, hemisphere-shaped defects that arise from nonbranching points of the cerebral arteries and are associated with a high risk of rupture.1-3 In contrast to saccular aneurysms, they consist of a platelet plug covering a thin layer of adventitia, which overlies a defect in the intima and media, WHAT IS THIS BOX? A QR Code is a matrix barcode readable by QR scanners, mobile phones with cameras, and smartphones. The QR Code above links to Supplemental Digital Content from this article. OPERATIVE NEUROSURGERY ABBREVIATIONS: BLA, blister-like aneurysms; GOS, Glasgow Outcome Scale; ICA, internal carotid artery; PED, Pipeline Embolization Device; SAH, subarachnoid hemorrhage Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.operativeneurosurgery-online.com). DOI: 10.1227/NEU.0000000000000866 and they are thought to be secondary to atherosclerosis, hemodynamic stress, dissection, or a combination of these factors.4,5 These lesions are challenging for the cerebrovascular surgeon because of the fragility of the aneurysm wall, as well as their poorly defined necks.3,6-10 Sundt and Murphey originally described BLAs in 1969 in relation to the internal carotid artery (ICA), but BLAs have since been described throughout the cerebral vasculature.11,12 Basilar artery BLAs make up a small subset of all BLAs, and their treatment is further complicated by the anatomy of the region and the proximity of perforating branches.13 Surgical and endovascular approaches to these lesions have been sporadically reported in the literature14-17; however, to our knowledge, no series of these rare VOLUME 11 | NUMBER 3 | SEPTEMBER 2015 | 387 Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited MOONEY ET AL aneurysms with long-term patient follow-up has been reported to date. Herein, we report the outcomes for 4 patients with basilar BLAs treated at our institution and describe our approach for managing these lesions. METHODS Patient Selection We queried a database for all patients with aneurysms treated at our institution between 2005 and 2011 to identify BLAs of the basilar circulation treated with a microsurgical technique. BLAs were defined as shallow, broad-based aneurysms arising from nonbranching sites of the basilar artery, which were diagnosed with cerebral angiograms and confirmed at operative inspection. We limited our search of the database to those treated before 2011 to obtain long-term follow-up on these patients. We reviewed the sex, age, lesion size, symptoms at presentation, treatment modalities used, complications, and outcomes for each patient. The patients’ clinical examinations and imaging studies, operative and angiographic reports, and in- and outpatient records were reviewed. Preoperative and postoperative vascular imaging was obtained by using conventional angiography, computed tomography angiography, or magnetic resonance angiography. Treatment All patients presented here were treated using microsurgery. Electrophysiological monitoring, including electroencephalography and somatosensory evoked potentials, were recorded in all cases. Angiographic intraoperative evaluation was performed by using indocyanine green video angiography. Postoperative angiography was obtained to document aneurysm occlusion and degree of parent vessel stenosis, if present. Aneurysm occlusion was classified as complete with no residual or as incomplete when any untreated residual remained. We do not routinely use temporary clips, intraoperative hypotension, or intraoperative cardiac arrest. Outcomes were measured by using Glasgow Outcome Scale (GOS) scores. Imaging follow-up time points are determined on a case-by-case basis. We use “cotton reinforcement” to indicate the technique of placing cotton beneath the clip tines, as previously described by Barrow and Spetzler.18 Although this technique was originally described to repair intraoperative tears of the aneurysm neck, we have expanded its use to cases where an added layer of friction between the vessel wall and clip tines can help prevent slippage of the clip on these wide-necked, fragile aneurysms.3 RESULTS We identified 4 patients (3 male, 1 female) with a mean age of 52.5 years (range, 35-66 years), each with a diagnosis of a basilar artery BLA. No other aneurysms were detected in any of the patients in this series (Table). The mean size of the base of the BLAs was 2.25 mm (range, 1-4 mm). The mean size of the length of the aneurysm dome was 2 mm (range, 1-2.5 mm). All BLAs were located at nonbranching points on the basilar artery. All patients presented with subarachnoid hemorrhage (SAH). The Hunt-Hess grade at presentation ranged from 1 to 3. Fisher grade was not available for 1 patient who was transferred from an outside hospital; the other 3 patients had scores of 3 or 4. The admission GOS score was used to assess and grade patients at presentation. The mean GOS score on presentation was 4 (median, 4; range, 3-5). The definitive diagnosis of BLA was made using angiography in 4 of 4 patients. In 3 patients, the aneurysms were treated by using a microsurgical technique, and, in 1 patient, a combined microsurgical/ endovascular approach was used. All aneurysms were confirmed to TABLE. Patient Characteristics and Outcomesa Case Age/sex Presenting symptom Dimension (length · width) (mm) Tool for 1 BLA diagnosis Hunt-Hess grade Fisher grade Treatment VPS Vasospasm Admission GOS Discharge GOS GOS last F/U Imaging F/U (mo) Clinical F/U (mo) 1 2 3 4 60/M Headache 2·3 DSA 2 3 Direct clip 1 2 3 4 5 42 83 66/M Headache 1·1 DSA 3 Unknownb Direct clip 1 1 4 3 5 66 66 35/M Seizure 2.5 · 4 CTA 2 4 Cotton clip 1 2 5 5 5 12 37 49/F Headache 2.5 · 1 DSA 1 3 Cotton clip 1 stent 2 2 4 5 5 72 103 a CTA, computerized tomographic angiography; DSA, digital subtraction angiography; F, female; F/U, follow-up; GOS, Glasgow Outcome Scale; M, male; VPS, ventriculoperitoneal shunt. b Original CT from outside facility was not available for this patient. 388 | VOLUME 11 | NUMBER 3 | SEPTEMBER 2015 www.operativeneurosurgery-online.com Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited BASILAR BLISTER-LIKE ANEURYSMS be ruptured on direct intraoperative inspection. Among the patients treated with microsurgical technique alone, 2 aneurysms were directly clipped, and 1 aneurysm was clipped with cotton reinforcement beneath the clip tines. In the single case of combined microsurgical/endovascular treatment, the aneurysm was clipped with cotton reinforcement and the vessel was stented (Figure 1). None of the patients experienced perioperative mortality. Three patients required ventricular shunting and 1 patient experienced clinically significant vasospasm. There was 1 case of treatmentrelated morbidity in a patient who required a subdural-peritoneal shunt for a persistent subdural hygroma. The mean GOS score at discharge was 4.25 (median, 4.5; range, 3-5). All patients were contacted by phone at the time of the study to assess long-term outcomes. At a mean clinical follow-up of 72 months (median, 74.5; range, 37-103), the GOS was 5 in all 4 patients. Postoperative imaging revealed complete obliteration of the aneurysm in 3 of the 4 cases. In 1 patient (case 4), residual FIGURE 1. A, B, case 1, a basilar apex blister-like aneurysm (BLA) that was directly clipped. C, D, case 3, a midbasilar trunk BLA clipped with cotton reinforcement and mild parent artery stenosis after clipping. E, F, case 4, a basilar BLA near the origin of the posterior cerebral artery directly clipped with cotton reinforcement and underwent subsequent Neuroform stenting. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. OPERATIVE NEUROSURGERY VOLUME 11 | NUMBER 3 | SEPTEMBER 2015 | 389 Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited MOONEY ET AL aneurysm was treated by endovascular placement of a Neuroform stent (Boston Scientific, Natick, Massachusetts). A small residual aneurysm persisted immediately after stent placement; however, repeat angiography 1 month later revealed complete obliteration. One patient (case 3) was noted to have mild stenosis of the basilar artery at the site of clipping. Follow-up imaging at a mean of 48 months (median, 54; range, 12-72) revealed no cases of aneurysm recurrence/regrowth. ILLUSTRATIVE CASE Case 3 A 35-year-old man presented to an outside hospital after a tonicclonic seizure, and he was found to have a Fisher grade 4 SAH. An external ventricular drain was placed at the outside hospital, and he was transferred to our institution for further management. He was neurologically intact on admission to our institute. Computed tomography angiogram on admission demonstrated a mid-basilar BLA (Figure 2A and 2B). The patient underwent a right retrosigmoid craniotomy for exploration of the aneurysm. After an attempt at direct clipping, the aneurysm was reinforced with cotton and clipped (see Video, Supplemental Digital Content, http://links.lww.com/NEU/A742). He required ventriculoperitoneal shunt placement for failure to wean the drain, and he was discharged to home on postoperative day 19. On discharge he was neurologically intact. Postoperative computed tomography angiography and follow-up digital subtraction angiography at 1 year demonstrated complete obliteration of the aneurysm with FIGURE 2. A, sagittal computed tomography angiography (CTA) on admission demonstrating an aneurysm along the basilar trunk. B, 3-dimensional reconstruction of the aneurysm from the initial CTA. C, postoperative sagittal CTA demonstrating clip placement and complete obliteration of the aneurysm. D, postoperative digital subtraction angiography of a left vertebral artery injection, Townes view, demonstrating complete obliteration and mild parent artery stenosis from clip placement. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. 390 | VOLUME 11 | NUMBER 3 | SEPTEMBER 2015 www.operativeneurosurgery-online.com Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited BASILAR BLISTER-LIKE ANEURYSMS mild parent artery stenosis adjacent to the aneurysm clip (Figure 2C and 2D). At long-term follow-up of 3 years, the patient is doing well and has returned to work; he is scheduled for repeat imaging follow-up at 5 years. DISCUSSION Incidence and Characteristics The true incidence and natural history of BLAs is difficult to determine. In the absence of rupture, these aneurysms may appear identical to small saccular aneurysms that would be treated conservatively with observation; however, the fragility of their walls and their propensity to rupture distinguishes them from their saccular counterparts. Indeed, short-interval rupture of an incidentally discovered BLA that was thought to be a small saccular aneurysm has been reported.3 Basilar artery aneurysms as a whole make up a small minority of all intracranial aneurysms. In the Barrow Ruptured Aneurysm Trial, patients with basilar trunk or basilar tip aneurysms made up only 5.4% (22/408) of the cases of ruptured aneurysms enrolled in the study.19 BLAs of the basilar artery are clearly a rare subset of basilar artery aneurysms, and over the 7-year study period at our institution, only 4 patients with these lesions were encountered. Additionally, 3 of 4 (75%) of these patients were transferred from outside hospitals for a higher level of care, further demonstrating their rare occurrence. Our limited knowledge regarding BLAs comes from both pathological examination and practical experience. The wall of this type of aneurysm has been described as consisting of a thin layer of adventitia overlying a defect in the intima and media layers.4,20 The fragile nature of BLAs has been associated with relatively high rates of intraoperative or intraprocedural hemorrhage.1-3,9,10,21,22 Microsurgical techniques for treating these lesions have been described, and options include direct clipping, clipping with cotton reinforcement beneath the clip tines, clip wrapping, and vessel sacrifice with or without bypass.3,8,10,11,23 Microsurgical Treatment Early series of microsurgical treatment for BLAs consisted of various clip techniques for ICA BLAs. Nakagawa et al9 published one of the earliest series in 1986. In this report of 8 cases, they were able to achieve direct clipping in 4 patients and clipping with supplementary wrapping (with muscle or fascia) or coating (with cellulose fabric and/or fibrin glue) in the remaining 4. A more recent publication from our own institution highlights our approach to these lesions.3 In the 18 ICA BLAs included in this study, direct clipping was achieved in 12 patients. In cases where this was not possible owing to aneurysm morphology or vessel wall friability, cotton-reinforced clipping was successful in 3 patients, and clip wrapping with Gore-Tex (W.L. Gore & Associates, Inc, Flagstaff, Arizona) was successful in the remaining 3. We recommend cotton-reinforced clipping of BLAs when there is inadequate vessel diameter to allow standard clip application without significant risk that the clip blades will slip OPERATIVE NEUROSURGERY off the aneurysm. In addition to minimizing slippage of the clip blades, the cotton serves as a local reinforcement.18 More recently, our technique for the management of ICA BLAs has evolved to clip wrapping with Gore-Tex.3 BLAs of the basilar artery are exceedingly rare and present a unique neurosurgical challenge. The proximity of these aneurysms to perforating branches differentiates them from their ICA counterparts. Literature describing treatment options for basilar BLAs is extremely limited, likely because of both their rare nature, as well as nonunified terminology to describe these lesions. In 2010, Hauck et al24 described their microsurgical technique for approaching 21 patients with small (,7 mm) basilar apex aneurysms, all of which were directly clipped. Although similarities exist in terms of the exposure of these lesions and visualization of surrounding vessels, these lesions were not BLAs. The majority of aneurysms in this series were unruptured (76%) and all occurred at the basilar apex, with or without involvement of the P1 segment. They were able to achieve favorable outcomes with their approach to these aneurysms, with only 2 cases of intraoperative rupture, and acceptable GOS scores in all patients. In our case series, on the other hand, aneurysms occurred along the course of the basilar trunk or at the basilar apex, and all aneurysms were confirmed to be BLAs intraoperatively. The largest diameter of any aneurysm in our series was 4 mm, and no cases of intraoperative rupture occurred (Table). Our approach to these lesions is a slight variation from our approach to BLAs of the ICA, given the unique anatomic challenges of the region. Clip wrapping is not an option for these aneurysms, as it is for ICA BLAs, because of the extremely narrow window of operative exposure and the presence of perforating branches in proximity to the aneurysm. We continue to attempt direct clipping for all lesions of this type but have found that cotton-reinforced clipping is an excellent strategy for complete obliteration of these lesions. Cotton reinforcement prevents slipping of the clip blades along the often wide base of these aneurysms, while minimizing the degree of parent vessel stenosis necessary for secure clip placement. This strategy was used in 2 of the 4 patients in this series. Clipping with a small degree of parent artery stenosis also remains an acceptable strategy, as illustrated in case 3 (Figure 2). Endovascular Treatment Advances in endovascular treatment strategies have led to alternative approaches to BLAs. However, direct coiling or stentassisted coiling is limited secondary to the wide-based morphology and fragile wall associated with these aneurysms, and high rates of intraprocedural rupture and postprocedure recurrence have been observed.21,22,25,26 Neuroform stent reconstruction and flowdiverting stenting have been explored as potential treatment options. Fiorella et al17 demonstrated the feasibility of Neuroform stent reconstruction for a variety of uncoilable “intradural pseudoaneurysms,” which included 4 cases involving a dissecting aneurysm, postsurgical aneurysm, or pseudoaneurysm of the basilar artery, all of which had ruptured either acutely or subacutely. In the setting of SAH, antiplatelet therapy is VOLUME 11 | NUMBER 3 | SEPTEMBER 2015 | 391 Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited MOONEY ET AL dangerous and often limited in these patients, and, indeed, 2 cases of stent thrombosis occurred in this series owing to insufficient antiplatelet therapy. Aydin et al14 reported their experience with SILK flowdiverting stenting (Balt Extrusion, Montmorency, France) in 11 patients with BLAs, 2 of whom had basilar trunk BLAs. All of these patients presented with SAH, and therapy was delayed 5 days in all patients to allow for dual-antiplatelet therapy before stenting. Although most aneurysms (9/11) were not obliterated with stent placement initially, all BLAs that were examined with angiography (9/9) at the 3-month follow-up were obliterated at that time with good patient outcomes reported. One patient in this series, however, had an ischemic stroke with transient hemiparesis due to stent thrombosis in the setting of antiplatelet agent noncompliance, and 2 others were found to have mild instent stenosis at 3-month follow-up. More recently, Chalouhi et al15 described their experience using the Pipeline Embolization Device (PED, eV3, Inc, Irvine, California) for 8 patients with BLAs, 1 of which arose from the basilar artery. Five of these 8 patients presented with SAH, and all were started on dual-antiplatelet therapy 1 to 13 days from their sentinel bleed. Aneurysm obliteration was achieved in 5 of 6 patients who had relatively short-term follow-up data available (2 weeks to 6 months), and 1 case of “minimal” asymptomatic instent stenosis occurred. Yoon et al27 reported mixed results in their experience with the PED for 11 patients with ruptured ICA blister aneurysms. Although complete obliteration was achieved in 7 of 8 patients with angiographic follow-up, 3 major and 2 minor perioperative complications were reported. Major complications included 1 large ipsilateral middle cerebral artery infarct after PED placement, 1 hemorrhagic infarct leading to death, and 1 ophthalmic artery occlusion leading to blindness. Minor complications included an asymptomatic carotid occlusion after stent thrombosis and an asymptomatic carotid dissection from guide-wire placement. These authors concluded that PED placement is a feasible treatment option for BLAs, even in the setting of acute SAH; however, ischemic and hemorrhagic complications can be encountered after stent placement, and this technique should be further investigated for long-term safety and efficacy. CONCLUSION BLAs are dangerous lesions that pose a significant treatment challenge. BLAs involving the basilar artery are rare but require specific surgical considerations. In our experience, microsurgical clipping is a favorable approach to these aneurysms that can achieve complete obliteration and excellent long-term outcomes. Direct clipping with cotton reinforcement beneath the clip blades is an acceptable strategy for basilar BLAs where direct clipping cannot be achieved. Endovascular techniques may have a role in the treatment of these lesions; however, their long-term safety and efficacy has yet to be proven, and must be weighed against the risk of dual-antiplatelet therapy in patients presenting with acute SAH. 392 | VOLUME 11 | NUMBER 3 | SEPTEMBER 2015 Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Abe M, Tabuchi K, Yokoyama H, Uchino A. 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Arterial suturing followed by clip reinforcement with circumferential wrapping for blister-like aneurysms of the internal carotid artery. Surg Neurol. 2006;66(4):424-428; discussion 428-429. www.operativeneurosurgery-online.com Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited BASILAR BLISTER-LIKE ANEURYSMS 24. Hauck EF, White JA, Samson D. The small “surgical aneurysm” at the basilar apex. J Neurosurg. 2010;112(6):1216-1221. 25. Lim YC, Kim BM, Suh SH, et al. Reconstructive treatment of ruptured blood blister-like aneurysms with stent and coil. Neurosurgery. 2013;73(3): 480-488. 26. Park JH, Park IS, Han DH, et al. Endovascular treatment of blood blister-like aneurysms of the internal carotid artery. J Neurosurg. 2007;106 (5):812-819. OPERATIVE NEUROSURGERY 27. Yoon JW, Siddiqui AH, Dumont TM, et al. Feasibility and safety of pipeline embolization device in patients with ruptured carotid blister aneurysms. Neurosurgery. 2014;75(4):419-429; discussion 429. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.operativeneurosurgery-online.com). VOLUME 11 | NUMBER 3 | SEPTEMBER 2015 | 393 Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited