GENERAL SCIENTIFIC SESSION 4 GENERAL SCIENTIFIC SESSION 4
Open vs Endovascular Approach to Intracranial Aneurysms Robert H. Rosenwasser, MD
V
ascular neurosurgery is a rapidly evolving field, and the nature of the discipline Nohra Chalouhi, MD continues to change. For vascular neuroStavropoula Tjoumakaris, MD surgeons, dual training in microsurgical and Pascal Jabbour, MD endovascular techniques has become the norm, especially in North America. Today, in addition Department of Neurosurgery, Thomas Jefferson University and Jefferson Hos- to microsurgery, neurosurgeons perform endopital for Neuroscience, Philadelphia, vascular procedures to treat a wide range of Pennsylvania intracranial vascular abnormalities, including aneurysms, arteriovenous malformations, ischeCorrespondence: 1-9 Robert H. Rosenwasser, MD, FACS, FAHA, mic stroke, carotid stenosis, and tumors. Jewell L. Osterholm Professor For intracranial aneurysms, the decision to clip and Chairman, or to coil is a complex one. Although randomized Department of Neurological Surgery, controlled trials have been conducted, the quesProfessor of Radiology, tion remains the subject of significant controversy Neurovascular Surgery, Interventional Neuroradiology, and passionate debate at neurosurgical meetMedical Director, ings.10-13 First, it should be stated that, in Jefferson Neuroscience Network, 2014, microsurgical treatment remains the gold Thomas Jefferson University, standard for intracranial aneurysms, and any Jefferson Hospital for Neuroscience, 901 Walnut St, 3rd Floor, other type of treatment must be benchmarked Philadelphia, PA 19107. against this modality in terms of outcome, E-mail: [email protected] morbidity, mortality, cost-effectiveness, and long-term durability. Second, it should be stated Copyright © 2014 by the Congress of Neurological Surgeons. that for ruptured aneurysms that are amenable to both endovascular and microsurgical techniques, there is Level I evidence to support choosing the endovascular option.14 In the past 2 decades, endovascular techniques have evolved at a remarkable pace, while advances in microsurgery have been rather slow. The endovascular coil was originally conceived by Guglielmi in the late 1980s, a major milestone in the treatment of intracranial aneurysms. This was the first time that a device could be deployed into an aneurysm, deposited, detached, and, most important, retrieved if placement was less than ideal. Advances have been made in coil technology since the introduction of the Guglielmi detachable coil in terms of coil shapes, lengths, and bioactivity. Additionally, significant progress has been
The 2013 CNS Annual Meeting presentation on which this article is based is available at: http://bit.ly/ 1hTtObE.
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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.neurosurgery-online.com).
made in intracranial stent technology, improving delivery, navigation, deployment, and possibly also efficacy. The use of stent technology has greatly expanded the range of aneurysms amenable to endovascular therapy and has significantly improved the long-term treatment durability (Figure 1).15 Recently, the introduction of flow diverters has revolutionized the treatment of intracranial aneurysms, especially those that are large/giant and have a complex morphology, although long-term safety data are lacking.15
TRIALS AND STUDIES OF ENDOVASCULAR VS MICROSURGICAL TREATMENT Randomized controlled trials have shown that endovascular coiling is the preferred treatment option for patients with ruptured intracranial aneurysms amenable to both modalities.16-19 The International Subarachnoid Aneurysm Trial (ISAT) is a landmark study that changed the way we manage cerebral aneurysms. The study enrolled 2143 patients with ruptured intracranial aneurysms across 42 neurosurgical centers, mostly in Europe, and randomly assigned them to microsurgical clipping (n = 1070) or endovascular coiling (n = 1073).17 Only patients with aneurysms that were judged to be suitable for either technique were enrolled in the trial. The primary outcome was the risk of death or dependency at 1 year (defined by a modified Rankin Scale [mRS] score between 3 and 6), and secondary outcomes included seizures and rehemorrhage. At 1 year, 250 of 1063 patients (23.5%) in the endovascular arm were dead or dependent vs 326 of 1055 patients (30.9%) in the microsurgical arm. The absolute risk reduction of 7.4% in dependency or death with endovascular therapy reached statistical significance (P = .001). This improvement in outcome is likely attributable to the lower rate of procedural complications in the coiling (8%) vs the clipping (19%) group. The results also showed that the early survival advantage was maintained for up to 7 years and was significant in patients
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FIGURE 1. A wide-necked carotid terminus aneurysm with egress of the middle and anterior cerebral arteries out of the neck of the aneurysm, which clearly would need to be treated with a stent-assisted technique or balloon remodeling technique. This type of configuration has a high recurrence rate unless an adjunct device such as a stent is used in the initial treatment.
treated with endovascular techniques (P = .03). The risk of epilepsy was substantially lower in patients in the endovascular arm, but the risk of rebleeding was higher (2.9% after endovascular repair vs 0.9% after open surgery). The investigators concluded that in patients with ruptured intracranial aneurysms suitable for both treatments, endovascular coiling is more likely to result in independent survival at 1 year and that the benefit continues for at least 7 years. The higher 1-year rehemorrhage rate in the endovascular group of the ISAT compared with the surgical group raised questions whether in the long run the 2 modalities could become equivalent. The results of long-term follow-up of the ISAT were published in 2009. Of 13 rebleeds from the treated aneurysm that occurred .1 year after treatment, 10 were in the coil group and only 3 were in the clipping group (P = .06).20 Although the risk of death at 5 years remained significantly lower in the coiled group (11%) than it was in the clipped group (14%; P = .03), the proportion of patients who were independent was similar in the 2 groups (83% with coiling, 82% with clipping).20 This, according to some, suggests that coiling and clipping are equivalent in the long term (although the benefit with coiling in terms of mortality is clear).11 ISAT was criticized regarding several issues, the most important of which is the potential “cherry-picking” bias because 80% of the patients who were initially screened were eventually excluded (7416 of 9559) from the trial. This begs the question, Are the results generalizable to the 7416 patients who were treated
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outside the study?21 In addition, doubts were raised about the level of expertise of participating neurosurgeons, some of whom clipped ,10 aneurysms per year, as opposed to the interventionalists, who were some of the most experienced in the world. Additionally, the results were statistically significant only for an mRS score of 3 to 6, but not 0 to 1 or 0 to 3. Moreover, it is not appropriate to make generalizations of the results to all intracranial aneurysms because, for example, only 14% of middle cerebral aneurysms were treated with coiling and ,10% of patients with basilar aneurysms underwent microsurgery. Lastly, it is not possible to extend the findings of ISAT to unruptured aneurysms because only patients with subarachnoid hemorrhage (SAH) were enrolled. Despite these potential limitations, ISAT remains a major trial of endovascular vs surgical treatment of intracranial aneurysms, and the impact it had on clinical practice was unprecedented. In fact, the proportion of patients undergoing endovascular treatment of aneurysms has increased since the publication of the ISAT study both in the United States and abroad.22-24 The mortality from SAH has also decreased since publication of ISAT, presumably because of a larger proportion of patients receiving endovascular treatment.23 The increasing use of endovascular techniques has not been limited to ruptured aneurysms in the United States but has also involved unruptured aneurysms.25 This trend indicates that minimally invasive approaches are becoming heavily favored over traditional approaches by patients.26 In our institutional experience at Jefferson Hospital for Neuroscience, 2000 was the last year that more patients were treated by microsurgical than endovascular means. As the years have progressed, more patients have been treated endovascularly primarily because of experience and improvement in neurointerventional technology. The continued referral of patients has maintained our surgical volume, and most important, the patients who are being referred for surgical treatment generally have aneurysms that are more difficult to treat on the basis of our experience. At our institution, we have performed a case-control analysis on 247 patients who crossed over from an endovascular to a surgical approach. Results were controlled for age, neurological grade, medical and surgical comorbidities, and aneurysm site. In patients who were #60 years of age with anterior circulation aneurysms (38% of the group), endovascular and microsurgical interventions yielded similar outcomes. Of the Hunt and Hess grade I and II SAH patients #60 years of age, 9.9% of patients in the endovascular group compared with 11.1% in the microsurgical group had an mRS score between 3 and 6 (difference not statistically different). However, SAH patients with Hunt and Hess grades III and IV and anterior circulation aneurysms showed clear differences between endovascular and surgical outcomes. Twenty-one percent of patients treated endovascularly had an mRS score of 3 to 6 compared with 33% of patients treated microsurgically. In the subgroup of patients who were $60 years of age with posterior circulation aneurysms (156 of 247 patients, 62%), endovascular intervention always had a more favorable outcome compared with open microsurgery.27 Specifically, low-grade SAH
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patients (grades I and II) had an mRS score between 3 and 6 in 12% of the endovascular group compared with 29% of the microsurgical group. Similarly, high-grade SAH patients (grades III and IV) had an mRS score between 3 and 6 in 22% of the endovascular group as opposed to 37% of the microsurgical group. These results are very similar to those of the recently published Barrow Ruptured Aneurysm Trial (BRAT). In the discussion of endovascular vs open surgical treatment of intracranial aneurysms, BRAT deserves mention. BRAT is a prospective randomized controlled trial with an intent-to-treat design that compared endovascular coiling and surgical clipping in patients with ruptured aneurysms.16 In response to the perceived shortcomings of ISAT, the BRAT investigators included all patients with SAH admitted during the study period. Treatment was performed by experienced vascular and endovascular neurosurgeons. A total of 472 patients were enrolled and assigned to clipping (n = 239) or coiling (n = 233). Because crossover was allowed, only 124 (62%) of 199 patients assigned to the endovascular group underwent coiling (the remaining 75 were clipped) while 205 (98%) of 209 patients assigned to the surgical group underwent clipping. As in the ISAT, poor outcomes at 1 year in the BRAT were found to be less common in patients treated with endovascular treatment (23.2% vs 33.7%). Although treatment durability was a significant concern in ISAT, no patient in BRAT experienced a rebleeding episode after endovascular therapy. This improvement in endovascular treatment efficacy is likely the result of recent refinements in embolization techniques and devices. After a follow-up of 3 years in BRAT, the risk of a poor outcome with clipping compared with coiling (35.8% vs 30%) decreased from that observed at 1 year and was no longer significant (P = .25). In addition, aneurysm occlusion (P = .001) and aneurysm recurrence/retreatment (P = .01) were significantly
better after clipping. Although outcomes of posterior circulation aneurysms were significantly better in the coil group, there was no difference in outcome for anterior circulation aneurysms. Criticism of BRAT has focused on the high crossover rate (which is problematic in a randomized trial), the relatively small sample size, and the generalizability of the study findings (Can the same surgical results be achieved with less experienced neurosurgeons?). In an accompanying comment, Molyneux et al28 criticized the design and findings of BRAT, stating that the study did not conform to the standard reporting criteria of clinical trials (set out in the CONSORT [Consolidated Standards of Reporting Trials] criteria) and that the investigators performed subgroup analyses that had not been prespecified in a published protocol, in addition to having a substantial number of missing outcomes and a sample size that was inadequate to draw conclusions. Some have even argued that “the BRAT was not, in fact, a randomized trial, but a registry of patients treated in 1 of 2 ways. . ..”12 Overall, although it has become common today to oppose the findings of BRAT to those of ISAT, it is our belief that the 2 trials yielded comparable results: Endovascular therapy provides a significant outcome benefit for ruptured aneurysms, although in the long term this benefit seems to progressively dissipate. As well stated by Lanzino,13 however, this does not negate the superiority of coiling because no patient would elect to undergo a treatment that requires years to reach equivalent outcomes.
TREATMENT DURABILITY Treatment durability has been the major concern with endovascular treatment of cerebral aneurysms (Figures 2 and 3). The recurrence rate is 24% to 35% for posterior circulation aneurysms, 18% to 32% for middle cerebral artery aneurysms,
FIGURE 2. A 49-year-old female patient who presented as a grade IV improved to grade III with ventriculostomy. A, the frontal view of this aneurysm. Because of the patient’s grade, the aneurysm was treated with an endovascular means. B, the initial films demonstrate adequate occlusion with a balloon-assisted technique; however, at the 60-month follow-up, there was recurrence of the aneurysm at the base (C), and she was treated with microsurgical clip ligation. At this point, the patient essentially went into surgery as a grade 0, having recovered from a quite severe subarachnoid hemorrhage, and the microsurgical exercise was fairly straightforward.
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FIGURE 3. A, an anterior communicating artery aneurysm projecting inferiorly that clearly has a wide neck; however, because of the neurological grade, the aneurysm was treated with coil occlusion. B, there is early recanalization at the base of the aneurysm at the 6-month follow-up. C, the aneurysm was treated microsurgically, leaving the coils in place and occluding only the portion of the aneurysm that had recanalized.
37% for posterior communicating artery aneurysms, 25% for anterior communicating artery aneurysms, 26% for carotid ophthalmic artery aneurysms, 40% for cavernous aneurysms, and 12% to 29% for paraclinoid aneurysms.29 The Cerebral Aneurysm Rerupture After Treatment study identified the degree of aneurysm occlusion after initial coiling as a strong predictor of subsequent hemorrhage, prompting an emphasis on achieving better initial aneurysm occlusion. The use of stenting and balloon remodeling techniques yields higher degrees of aneurysm occlusion and improves treatment durability.30-41 Furthermore, we have found in a comparative study that stent-assisted coiling provides higher occlusion rates with lower retreatment rates and no additional morbidity in wide-necked aneurysms.26 In a follow-up study from the ISAT, the rates of retreatment were compared between the surgical and endovascular arms and
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were found to be significantly higher after coiling.42 Specifically, retreatment was performed in 191 of 1096 patients (17.4%) in the endovascular group vs 39 of 1012 patients (3.8%) in the clipping group. Most retreatments were performed at an early time point after clipping, whereas after coiling, retreatments continued to be performed throughout the follow-up period. This again indicates that clipping provides better treatment durability and raises questions about whether the benefit seen with endovascular therapy can be sustained in the long run. This could be a concern especially in young patients. In fact, surgical clipping is usually preferred in young patients because of its longterm durability. Along these lines, the authors of the ISAT noted that the absolute difference in poor outcome rates between coiling and clipping is lower in patients ,50 years of age (3.3%) than it is for those .50 years of age (10%). They concluded that
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the long-term protection from SAH afforded by surgical clipping could give this treatment modality an advantage in life expectancy over coiling for young patients (,40 years of age).43 In our experience, endovascular therapy is a valuable option for young patients with aneurysmal SAH.44 We recently performed an analysis on 40 patients ,35 years of age (mean, 30 years; range, 17-35 years) who presented to our institution with aneurysmal SAH. Thirty-five patients (87.5%) were treated with coil embolization vs only 5 with craniotomy and clipping. Up to 85% of patients treated with endovascular therapy had a favorable outcome, and no patient experienced a rehemorrhage after endovascular treatment. Although the need for retreatment is considered a disadvantage of endovascular techniques, it should be noted that recoiling in the few cases when it is mandated has a very low complication rate (much lower than the initial treatment) and does not negate the original benefit of endovascular treatment.45 Furthermore, the use of balloon- and stentassisted techniques has significantly improved the durability of endovascular treatment.15,37,40,41 The importance of long-term follow-up in young patients undergoing coil embolization cannot be overemphasized.
NEUROPSYCHOLOGICAL OUTCOMES AND COST-EFFECTIVENESS With regard to neuropsychological outcomes, an interesting study that included patients from the ISAT showed that cognitive impairment occurred in approximately one-third of patients who were not otherwise disabled (mRS score, 0-2) and was more frequent after clipping (38.7%) than after coiling (26.7%; P = .005). Rates of neurocognitive deficits in each assessed domain were greater after clipping, especially for verbal memory (P = .03), processing speed (P = .008), executive skills (P = .06), and spatial working memory (P = .09). Several other studies have also demonstrated the superiority of coiling over clipping in this respect.46-48 These data remind us that quality of life and neurocognition are important factors that are poorly studied in randomized trials and are not reflected by the mRS (which measures mostly functional independence). Cosmesis is also particularly valued by patients, especially those who are young. Hence, it is not surprising that most patients with cerebral aneurysms, especially younger patients, elect to undergo the minimally invasive and less traumatic procedure. Therefore, information on cognitive, psychosocial, and cosmetic outcomes of the 2 interventions is essential when counseling patients and their families. With regard to the cost-effectiveness of the 2 procedures, one may assume that the high cost of the coils and endovascular devices makes coiling a more costly procedure than clipping. However, a study of patients randomized in ISAT analyzing resource use and costs up to 24 months after endovascular and neurosurgical treatment reported that there was no significant difference in costs between the 2 interventions at 12 or 24 months.49 On closer inspection, coiling had higher costs for the initial procedure, for
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the number and length of stay of subsequent procedures, and for follow-up angiograms. However, these higher costs were offset by lower costs related to length of stay for the initial procedure. Likewise, a recent study analyzing inpatient and outpatient costs associated with surgical or endovascular treatment of patients with unruptured aneurysms in the United States found similar overall costs at 2 and 5 years. Although hospital length of stay and costs associated with the initial procedure were higher with clipping, the number of postoperative angiograms and outpatient services used during the follow-up was significantly higher with coiling.50
THE CASE FOR SMALL ANEURYSMS The best treatment modality for patients with small ruptured aneurysms remains unclear. The ISAT investigators excluded all patients with small aneurysms from their study, and the BRAT investigators assigned these patients preferentially to the surgical arm. Small aneurysms pose significant technical challenges to endovascular therapy because of the difficulties in catheterizing the aneurysm, stabilizing the microcatheter, and safely deploying coils. Several authors have reported a high risk of intraprocedural rupture with coiling of small aneurysms.51 For these reasons, surgical clipping has been considered to be the preferred treatment for these lesions. We have recently compared surgical and endovascular options in 161 patients with small ruptured aneurysms treated at our institution (91 with endovascular therapy and 60 with surgical clipping).52 We found a significantly lower rate of procedural complications with endovascular therapy (9.8%) compared with open surgery (23.3%). Importantly, only 3.7% of patients experienced an intraprocedural aneurysm rupture during endovascular treatment. These findings indicate that endovascular therapy, if technically feasible, may serve as a treatment alternative for small ruptured aneurysms, although randomized controlled studies are required to provide definitive information on the best therapeutic approach.
SPECIFIC SITUATIONS The choice between surgical and endovascular options for the treatment of aneurysms should take into consideration several factors, including aneurysm location, configuration, clinical grade, and medical comorbidities (Figure 4). Middle cerebral artery aneurysms pose significant technical challenges to endovascular coiling, and in this particular location, surgical clipping may provide more favorable results.53 Patients with a large intraparenchymal hematoma should undergo open surgery for aneurysm clipping and simultaneous clot evacuation and decompression. It should be noted that in selected patients with aneurysmal SAH and associated intraparenchymal hematoma, endovascular aneurysm obliteration before surgical decompression is also an acceptable alternative that can simplify open surgery to hematoma evacuation and decompression.54 Elderly patients and those presenting with poor neurological grades (Hunt and Hess grades IV and V) are more likely to benefit from
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FIGURE 4. A, a large aneurysm of the posterior carotid wall (left). This patient presented with a grade III subarachnoid hemorrhage, and coiling allowed what appeared to be complete occlusion (right). However, this patient experienced a hemorrhage approximately 12 hours after the complete occlusion with a very poor outcome with an associated ultimate mortality (B). This was most likely due to a ball valve mechanism in which blood was dissecting around the coil mass into the posterior aspect of the aneurysm, which led to a delayed hemorrhage.
an endovascular procedure.53 In a subgroup analysis of ISAT, 72.0% of elderly patients with anterior circulation aneurysms allocated to coiling were independent compared with only 52.0% allocated to clipping (P , .05).55 In our institution, Hunt and Hess grade V patients are generally considered for endovascular management only after clinical improvement with placement of ventriculostomy. Patients with multiple medical comorbidities, bleeding diathesis, or thrombotic disease requiring chronic anticoagulation are also considered for endovascular treatment. Likewise, in basilar tip aneurysms, endovascular therapy has yielded more favorable results than microsurgery.56 In our institution, posterior circulation aneurysms in general and basilar tip aneurysms in particular are almost always treated by endovascular means.30 We have found the use of self-expanding stents to improve treatment durability for basilar tip aneurysms with no added morbidity.57 Proximal posterior inferior cerebellar artery aneurysms are better treated by endovascular means, whereas in distal aneurysms, both modalities provide favorable results.58 In a study from our institution that included 76 patients, coiling of posterior inferior cerebellar artery aneurysms was associated with a morbidity rate of only 2.8%, with favorable outcome at follow-up in 93% of patients with unruptured aneurysms and in 78.7% of those with ruptured aneurysms.58 Patients with multiple intracranial aneurysms and unknown source of bleeding should also be considered for an endovascular procedure. Finally, the presence of significant vasospasm, moderate atherosclerosis, and tortuosity of proximal vessels is usually a contraindication to endovascular treatment.
OUR INSTITUTIONAL PROTOCOL FOR COILING OF RUPTURED ANEURYSMS In our institution, all patients with SAH undergo arterial line and central venous line placement preoperatively. Patients with Hunt and Hess grades III or higher also are monitored with ventriculos-
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tomy and Swan-Ganz catheters. Endovascular procedures are performed under general endotracheal anesthesia and continuous neurophysiological monitoring, including somatosensory evoked potentials and electroencephalography and brainstem auditoryevoked responses. Generally, a half-bolus of heparin (50 U/kg) is administered after deployment of the first coil. The presence of an intraparenchymal hematoma or recent ventriculostomy placement (within the previous 2 hours) limits the use of intraoperative anticoagulation. Aneurysms are treated within 24 hours to avoid the risk of a devastating rehemorrhage.59 Arterial access is obtained through femoral puncture by use of the Seldinger technique, and an arterial sheath is inserted and secured with a stitch. The guiding catheter is introduced and navigated into each studied vessel with the aid of a guidewire. A 6-vessel angiogram, including bilateral external carotid, internal carotid, and vertebral arteries, is required when the source of the SAH is unclear. Three-dimensional angiography allows precise measurements of the aneurysm size and dome-to-neck ratio with accurate depiction of the aneurysm neck and its relation to parent and branching vessels. Aneurysms with a small (,4 mm) neck and a favorable dome-to-neck ratio ($2) can usually be coiled without stent or balloon assistance. Through the guiding catheter, a microcatheter is advanced over a microguidewire and subsequently placed in the aneurysm lumen, preferably away from the neck. Next, coils are deployed under direct angiographic guidance. The mean arterial pressure is lowered by 15% to 20% during coil deployment. Coils of various shapes (helical, spherical), lengths (1-30 mm), diameters, softness, and design (bioactive vs bare platinum) are available. The initial coil is usually complex shaped and fills the aneurysm in a basket-like configuration. Once optimal positioning is achieved, the coil is detached. Additional coils of progressively decreasing size and variable shapes are then deployed until complete aneurysm obliteration is achieved (ie, no aneurysm filling is noted in at least
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3 distinct biplane views and under normal blood pressure). The last “finishing” coils are usually helical shaped to allow better filling of the residual aneurysm. After aneurysm obliteration, the mean arterial pressure is maintained between 90 and 100 mm Hg to prevent vasospasm and thromboembolic events. Stent-assisted coiling requires dual antiplatelet therapy to minimize the thromboembolic risk related to stent placement.60-62 The use of antiplatelets in the setting of SAH, however, may be associated with hemorrhagic complications related to ventriculostomy placement, aneurysmal rebleeding, and potential need for future invasive procedures.3 Balloon remodeling, which relies on a temporarily inflated balloon in the parent artery to prevent coil prolapse and to allow dense coil packing of the aneurysm, can be performed without the use of dual antiplatelet agents, making it another attractive option for treatment of acutely ruptured wide-necked and complex intracranial aneurysms.63 In a recent study from our institution in which we compared the safety and efficacy of stenting and balloon remodeling in 84 acutely ruptured aneurysms, we found that procedural complications (hemorrhagic and thromboembolic) and clinical outcomes did not differ significantly between the 2 techniques.64 These data suggested that stent-assisted coiling was an acceptable alternative to balloon remodeling for complex aneurysms in the acute phase of SAH.
THE EMERGENCE OF FLOW DIVERTERS Flow diverters like the Pipeline Embolization Device (PED) are revolutionary tools for intracranial aneurysms and have generated great enthusiasm in the neurovascular community. Flow diverters provide a physiological approach to the treatment of intracranial aneurysms through a combination of flow redirection and endoluminal vessel reconstruction (from neointimal growth along the vessel). Treatment with flow diverters was initially reserved for large, giant, and otherwise untreatable aneurysms of the internal carotid artery. Recently, at our institution and several other centers, the PED has become a routine first-line treatment for several types of aneurysms in various intracranial locations.34-40 At the Jefferson Hospital for Neuroscience, we have treated .250 aneurysms with the PED since its approval by the US Food and Drug Administration, and we have noted a dramatic decrease in the complication rate after an initial learning curve phase.40 The Pipeline procedure is also much simpler than coil embolization or stent-assisted coiling and requires significantly shorter fluoroscopy and procedure times.65 Moreover, flow diversion is more economical than conventional strategies.66 The safety, practicality, ease of use, high efficacy, and cost benefit of the PED have all led to a dramatic decline in the use of coils, especially for unruptured aneurysms. A case-control study from our institution suggests that the PED is a preferred treatment over traditional strategies for unruptured large and giant aneurysms because it provides higher occlusion rates with no added morbidity or poor outcomes.37 We have also found
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a similar benefit with flow diversion in small unruptured aneurysms of the anterior circulation.67 However, the use of the PED in ruptured aneurysms is generally considered to be controversial because of the need for dual antiplatelet therapy. At our institution, we generally avoid using the PED in patients presenting with SAH, although we have found the PED to be a valuable treatment for blister aneurysms and some other aneurysms that are not amenable to conventional modalities.
CONCLUSION The best technique for treating an aneurysm is the one that will produce the best result for a given patient and is dependent on many factors, including the expertise of the treating team. Management should always be tailored to the individual patient, taking into account all available data (specific for the patient, lesion, and treating team) and using whatever treatment modality is necessary to achieve the best outcomes for our patients. Disclosure Dr Jabbour has been a consultant for ev3, Codman, and Mizuho. Dr Tjoumakaris has been a consultant for Stryker. Dr Rosenwasser has been a consultant for Boston Scientific. Dr Chalouhi reports no disclosures.
REFERENCES 1. Zanaty M, Chalouhi N, Starke RM, et al. Endovascular treatment of cerebral mycotic aneurysm: a review of the literature and single center experience. Biomed Res Int. 2013;2013:151643. 2. Zanaty M, Chalouhi N, Tjoumakaris SI, Rosenwasser RH, Jabbour PM. Endovascular management of cerebral aneurysm: review of the literature. Transl Stroke Res. 2014;5(2):199-206. 3. Amenta PS, Dalyai RT, Kung D, et al. Stent-assisted coiling of wide-necked aneurysms in the setting of acute subarachnoid hemorrhage: experience in 65 patients. Neurosurgery. 2012;70(6):1415-1429; discussion 1429. 4. Chalouhi N, Tjoumakaris S, Starke RM, et al. Endovascular stroke intervention in young patients with large vessel occlusions. Neurosurg Focus. 2014;36(1):E6. 5. Chalouhi N, Campbell P, Makke Y, et al. Treatment of complex intracranial aneurysms with a telescoping stent technique. J Neurol Surg A Cent Eur Neurosurg. 2012;73(5):281-288. 6. 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(4):828-832. 7. Chalouhi N, Dumont AS, Tjoumakaris S, et al. The superior ophthalmic vein approach for the treatment of carotid-cavernous fistulas: a novel technique using Onyx. Neurosurg Focus. 2012;32(5):E13. 8. Chalouhi N, Tjoumakaris S, Dumont AS, et al. Superior hypophyseal artery aneurysms have the lowest recurrence rate with endovascular therapy. AJNR Am J Neuroradiol. 2012;33(8):1502-1506. 9. Jabbour P, Chalouhi N, Tjoumakaris S, et al. Pearls and pitfalls of intraarterial chemotherapy for retinoblastoma. J Neurosurg Pediatr. 2012;10(3):175-181. 10. Nichols DA, Brown RD Jr, Meyer FB. Coils or clips in subarachnoid haemorrhage? Lancet. 2002;360(9342):1262-1263. 11. Bakker NA, Metzemaekers JD, Groen RJ, Mooij JJ, Van Dijk JM. International Subarachnoid Aneurysm Trial 2009: endovascular coiling of ruptured intracranial aneurysms has no significant advantage over neurosurgical clipping. Neurosurgery. 2010;66(5):961-962. 12. Darsaut TE, Raymond J. Barrow Ruptured Aneurysm Trial. J Neurosurg. 2012; 117(2):378-379; author reply 379-380. 13. Lanzino G. The Barrow Ruptured Aneurysm Trial. J Neurosurg. 2012;116(1):133134; discussion 134. 14. Bederson JB, Connolly ES Jr, Batjer HH, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals
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from a special writing group of the Stroke Council, American Heart Association. Stroke. 2009;40(3):994-1025. Chalouhi N, Jabbour P, Singhal S, et al. Stent-assisted coiling of intracranial aneurysms: predictors of complications, recanalization, and outcome in 508 cases. Stroke. 2013;44(5):1348-1353. McDougall CG, Spetzler RF, Zabramski JM, et al. The Barrow Ruptured Aneurysm Trial. J Neurosurg. 2012;116(1):135-144. Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360(9342): 1267-1274. Molyneux AJ, Kerr RS, Yu LM, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366(9488):809-817. Koivisto T, Vanninen R, Hurskainen H, Saari T, Hernesniemi J, Vapalahti M. Outcomes of early endovascular versus surgical treatment of ruptured cerebral aneurysms: a prospective randomized study. Stroke. 2000;31(10):2369-2377. Molyneux AJ, Kerr RS, Birks J, et al. Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up. Lancet Neurol. 2009;8(5):427-433. O’Kelly CJ, Kulkarni AV, Austin PC, Wallace MC, Urbach D. The impact of therapeutic modality on outcomes following repair of ruptured intracranial aneurysms: an administrative data analysis: clinical article. J Neurosurg. 2010;113 (4):795-801. Gnanalingham KK, Apostolopoulos V, Barazi S, O’Neill K. The impact of the International Subarachnoid Aneurysm Trial (ISAT) on the management of aneurysmal subarachnoid haemorrhage in a neurosurgical unit in the UK. Clin Neurol Neurosurg. 2006;108(2):117-123. Qureshi AI, Vazquez G, Tariq N, Suri MF, Lakshminarayan K, Lanzino G. Impact of International Subarachnoid Aneurysm Trial results on treatment of ruptured intracranial aneurysms in the United States: clinical article. J Neurosurg. 2011;114 (3):834-841. Langham J, Reeves BC, Lindsay KW, et al. Variation in outcome after subarachnoid hemorrhage: a study of neurosurgical units in UK and Ireland. Stroke. 2009;40(1):111-118. Smith GA, Dagostino P, Maltenfort MG, Dumont AS, Ratliff JK. Geographic variation and regional trends in adoption of endovascular techniques for cerebral aneurysms. J Neurosurg. 2011;114(6):1768-1777. Shakir HJ, Levy EI. The blunt truth behind coiling vs clipping: consumers as decision-drivers. Neurosurgery. 2014;74(1):E145-E146. Pandey AS, Koebbe C, Rosenwasser RH, Veznedaroglu E. Endovascular coil embolization of ruptured and unruptured posterior circulation aneurysms: review of a 10-year experience. Neurosurgery. 2007;60(4):626-636; discussion 636-637. Molyneux A, Kerr R, Birks J. Barrow Ruptured Aneurysm Trial. J Neurosurg. 2013;119(1):139-141. Chalouhi N, Tjoumakaris S, Dumont AS, et al. Superior hypophyseal artery aneurysms have the lowest recurrence rate with endovascular therapy. AJNR Am J Neuroradiol. 2012;33:1502-1506. Chalouhi N, Jabbour P, Gonzalez LF, et al. Safety and efficacy of endovascular treatment of basilar tip aneurysms by coiling with and without stent assistance: a review of 235 cases. Neurosurgery. 2012;71:785-794. Pierot L, Cognard C, Anxionnat R, Ricolfi F. Remodeling technique for endovascular treatment of ruptured intracranial aneurysms had a higher rate of adequate postoperative occlusion than did conventional coil embolization with comparable safety. Radiology. 2011;258(2):546-553. Piotin M, Blanc R, Spelle L, et al. Stent-assisted coiling of intracranial aneurysms: clinical and angiographic results in 216 consecutive aneurysms. Stroke. 2010;41 (1):110-115. Raymond J, Darsaut TE. Stenting for intracranial aneurysms: how to paint oneself into the proverbial corner. AJNR Am J Neuroradiol. 2011;32(9):1711-1713. Chalouhi N, Chitale R, Starke RM, et al. Treatment of recurrent intracranial aneurysms with the Pipeline Embolization Device. J Neurointerv Surg. 2014;6: 19-23.
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35. Chalouhi N, Satti SR, Tjoumakaris S, et al. Delayed migration of a pipeline embolization device. Neurosurgery. 2013;72(2 suppl operative):ons229-ons234; discussion ons234. 36. Chalouhi N, Tjoumakaris S, Dumont AS, et al. Treatment of posterior circulation aneurysms with the Pipeline Embolization Device. Neurosurgery. 2013;72(6):883-889. 37. Chalouhi N, Tjoumakaris S, Starke RM, et al. Comparison of flow diversion and coiling in large unruptured intracranial saccular aneurysms. Stroke. 2013;44(8): 2150-2154. 38. Chalouhi N, Tjoumakaris SI, Gonzalez LF, et al. Spontaneous delayed migration/ shortening of the Pipeline Embolization Device: report of 5 cases. AJNR Am J Neuroradiol. 2013;34(12):2326-2330. 39. Chitale R, Gonzalez LF, Randazzo C, et al. Single center experience with Pipeline stent: feasibility, technique, and complications. Neurosurgery. 2012;71(3):679691; discussion 691. 40. Jabbour P, Chalouhi N, Tjoumakaris S, et al. The Pipeline Embolization Device: learning curve and predictors of complications and aneurysm obliteration. Neurosurgery. 2013;73(1):113-120; discussion 120. 41. Starke RM, Chalouhi N, Ali MS, et al. Endovascular treatment of very small ruptured intracranial aneurysms: complications, occlusion rates and prediction of outcome. J Neurointerv Surg. 2013;5(suppl 3):iii66-iii71. 42. Campi A, Ramzi N, Molyneux AJ, et al. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT). Stroke. 2007;38(5):1538-1544. 43. Mitchell P, Kerr R, Mendelow AD, Molyneux A. Could late rebleeding overturn the superiority of cranial aneurysm coil embolization over clip ligation seen in the International Subarachnoid Aneurysm Trial? J Neurosurg. 2008;108 (3):437-442. 44. Chalouhi N, Tjoumakaris S, Gonzalez LF, et al. Onyx embolization of a ruptured lenticulostriate artery aneurysm in a patient with moyamoya disease. World Neurosurg. 2013;80:436.e7-436.e10. 45. Renowden SA, Koumellis P, Benes V, Mukonoweshuro W, Molyneux AJ, McConachie NS. Retreatment of previously embolized cerebral aneurysms: the risk of further coil embolization does not negate the advantage of the initial embolization. AJNR Am J Neuroradiol. 2008;29(7):1401-1404. 46. Scott RB, Eccles F, Molyneux AJ, Kerr RS, Rothwell PM, Carpenter K. Improved cognitive outcomes with endovascular coiling of ruptured intracranial aneurysms: neuropsychological outcomes from the International Subarachnoid Aneurysm Trial (ISAT). Stroke. 2010;41(8):1743-1747. 47. Latimer SF, Wilson FC, McCusker CG, Caldwell SB, Rennie I. Subarachnoid haemorrhage (SAH): long-term cognitive outcome in patients treated with surgical clipping or endovascular coiling. Disabil Rehabil. 2013;35(10):845-850. 48. Hadjivassiliou M, Tooth CL, Romanowski CA, et al. Aneurysmal SAH: cognitive outcome and structural damage after clipping or coiling. Neurology. 2001;56(12): 1672-1677. 49. Wolstenholme J, Rivero-Arias O, Gray A, et al. Treatment pathways, resource use, and costs of endovascular coiling versus surgical clipping after aSAH. Stroke. 2008; 39(1):111-119. 50. Lad SP, Babu R, Rhee MS, et al. Long-term economic impact of coiling vs clipping for unruptured intracranial aneurysms. Neurosurgery. 2013;72(6):1000-1011; discussion 1011-1013. 51. Brinjikji W, Lanzino G, Cloft HJ, Rabinstein A, Kallmes DF. Endovascular treatment of very small (3 mm or smaller) intracranial aneurysms: report of a consecutive series and a meta-analysis. Stroke. 2010;41(1):116-121. 52. Chalouhi N, Penn DL, Tjoumakaris S, et al. Treatment of small ruptured intracranial aneurysms: comparison of surgical and endovascular options. J Am Heart Assoc. 2012;1(4):e002865. 53. Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2012;43(6):1711-1737. 54. Tawk RG, Pandey A, Levy E, et al. Coiling of ruptured aneurysms followed by evacuation of hematoma. World Neurosurg. 2010;74(6):626-631. 55. Ryttlefors M, Enblad P, Kerr RS, Molyneux AJ. International subarachnoid aneurysm trial of neurosurgical clipping versus endovascular coiling: subgroup analysis of 278 elderly patients. Stroke. 2008;39(10):2720-2726.
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56. Lusseveld E, Brilstra EH, Nijssen PC, et al. Endovascular coiling versus neurosurgical clipping in patients with a ruptured basilar tip aneurysm. J Neurol Neurosurg Psychiatry. 2002;73(5):591-593. 57. Chalouhi N, Jabbour P, Gonzalez LF, et al. Safety and efficacy of endovascular treatment of basilar tip aneurysms by coiling with and without stent assistance: a review of 235 cases. Neurosurgery. 2012;71(4):785-794. 58. Chalouhi N, Jabbour P, Starke RM, et al. Endovascular treatment of proximal and distal posterior inferior cerebellar artery aneurysms. J Neurosurg. 2013; 118(5):991-999. 59. Kassell NF, Torner JC. Aneurysmal rebleeding: a preliminary report from the Cooperative Aneurysm Study. Neurosurgery. 1983;13(5):479-481. 60. Lopes D, Sani S. Histological postmortem study of an internal carotid artery aneurysm treated with the Neuroform stent. Neurosurgery. 2005;56(2):E416; discussion E416. 61. Ries T, Buhk JH, Kucinski T, et al. Intravenous administration of acetylsalicylic acid during endovascular treatment of cerebral aneurysms reduces the rate of thromboembolic events. Stroke. 2006;37(7):1816-1821. 62. Tähtinen OI, Vanninen RL, Manninen HI, et al. Wide-necked intracranial aneurysms: treatment with stent-assisted coil embolization during acute (,72 hours) subarachnoid hemorrhage: experience in 61 consecutive patients. Radiology. 2009;253(1):199-208.
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63. Chalouhi N, Jabbour P, Tjoumakaris S, et al. Single-center experience with balloon-assisted coil embolization of intracranial aneurysms: safety, efficacy and indications. Clin Neurol Neurosurg. 2013;115(5):607-613. 64. Chitale R, Chalouhi N, Theofanis T, et al. Treatment of ruptured intracranial aneurysms: comparison of stenting and balloon remodeling. Neurosurgery. 2013;72 (6):953-959. 65. 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;6:291-295. 66. Colby GP, Lin LM, Paul AR, Huang J, Tamargo RJ, Coon AL. Cost comparison of endovascular treatment of anterior circulation aneurysms with the pipeline embolization device and stent-assisted coiling. Neurosurgery. 2012;71(5):944-948; discussion 948-950. 67. Chalouhi N, Starke RM, Yang S, et al. Extending the indications of flow diversion to small, unruptured, saccular aneurysms of the anterior circulation. Stroke. 2014; 45(1):54-58.
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Open vs Endovascular Approach to Intracranial Aneurysms Robert H. Rosenwasser, MD
V
ascular neurosurgery is a rapidly evolving field, and the nature of the discipline Nohra Chalouhi, MD continues to change. For vascular neuroStavropoula Tjoumakaris, MD surgeons, dual training in microsurgical and Pascal Jabbour, MD endovascular techniques has become the norm, especially in North America. Today, in addition Department of Neurosurgery, Thomas Jefferson University and Jefferson Hos- to microsurgery, neurosurgeons perform endopital for Neuroscience, Philadelphia, vascular procedures to treat a wide range of Pennsylvania intracranial vascular abnormalities, including aneurysms, arteriovenous malformations, ischeCorrespondence: 1-9 Robert H. Rosenwasser, MD, FACS, FAHA, mic stroke, carotid stenosis, and tumors. Jewell L. Osterholm Professor For intracranial aneurysms, the decision to clip and Chairman, or to coil is a complex one. Although randomized Department of Neurological Surgery, controlled trials have been conducted, the quesProfessor of Radiology, tion remains the subject of significant controversy Neurovascular Surgery, Interventional Neuroradiology, and passionate debate at neurosurgical meetMedical Director, ings.10-13 First, it should be stated that, in Jefferson Neuroscience Network, 2014, microsurgical treatment remains the gold Thomas Jefferson University, standard for intracranial aneurysms, and any Jefferson Hospital for Neuroscience, 901 Walnut St, 3rd Floor, other type of treatment must be benchmarked Philadelphia, PA 19107. against this modality in terms of outcome, E-mail: [email protected] morbidity, mortality, cost-effectiveness, and long-term durability. Second, it should be stated Copyright © 2014 by the Congress of Neurological Surgeons. that for ruptured aneurysms that are amenable to both endovascular and microsurgical techniques, there is Level I evidence to support choosing the endovascular option.14 In the past 2 decades, endovascular techniques have evolved at a remarkable pace, while advances in microsurgery have been rather slow. The endovascular coil was originally conceived by Guglielmi in the late 1980s, a major milestone in the treatment of intracranial aneurysms. This was the first time that a device could be deployed into an aneurysm, deposited, detached, and, most important, retrieved if placement was less than ideal. Advances have been made in coil technology since the introduction of the Guglielmi detachable coil in terms of coil shapes, lengths, and bioactivity. Additionally, significant progress has been
The 2013 CNS Annual Meeting presentation on which this article is based is available at: http://bit.ly/ 1hTtObE.
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made in intracranial stent technology, improving delivery, navigation, deployment, and possibly also efficacy. The use of stent technology has greatly expanded the range of aneurysms amenable to endovascular therapy and has significantly improved the long-term treatment durability (Figure 1).15 Recently, the introduction of flow diverters has revolutionized the treatment of intracranial aneurysms, especially those that are large/giant and have a complex morphology, although long-term safety data are lacking.15
TRIALS AND STUDIES OF ENDOVASCULAR VS MICROSURGICAL TREATMENT Randomized controlled trials have shown that endovascular coiling is the preferred treatment option for patients with ruptured intracranial aneurysms amenable to both modalities.16-19 The International Subarachnoid Aneurysm Trial (ISAT) is a landmark study that changed the way we manage cerebral aneurysms. The study enrolled 2143 patients with ruptured intracranial aneurysms across 42 neurosurgical centers, mostly in Europe, and randomly assigned them to microsurgical clipping (n = 1070) or endovascular coiling (n = 1073).17 Only patients with aneurysms that were judged to be suitable for either technique were enrolled in the trial. The primary outcome was the risk of death or dependency at 1 year (defined by a modified Rankin Scale [mRS] score between 3 and 6), and secondary outcomes included seizures and rehemorrhage. At 1 year, 250 of 1063 patients (23.5%) in the endovascular arm were dead or dependent vs 326 of 1055 patients (30.9%) in the microsurgical arm. The absolute risk reduction of 7.4% in dependency or death with endovascular therapy reached statistical significance (P = .001). This improvement in outcome is likely attributable to the lower rate of procedural complications in the coiling (8%) vs the clipping (19%) group. The results also showed that the early survival advantage was maintained for up to 7 years and was significant in patients
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FIGURE 1. A wide-necked carotid terminus aneurysm with egress of the middle and anterior cerebral arteries out of the neck of the aneurysm, which clearly would need to be treated with a stent-assisted technique or balloon remodeling technique. This type of configuration has a high recurrence rate unless an adjunct device such as a stent is used in the initial treatment.
treated with endovascular techniques (P = .03). The risk of epilepsy was substantially lower in patients in the endovascular arm, but the risk of rebleeding was higher (2.9% after endovascular repair vs 0.9% after open surgery). The investigators concluded that in patients with ruptured intracranial aneurysms suitable for both treatments, endovascular coiling is more likely to result in independent survival at 1 year and that the benefit continues for at least 7 years. The higher 1-year rehemorrhage rate in the endovascular group of the ISAT compared with the surgical group raised questions whether in the long run the 2 modalities could become equivalent. The results of long-term follow-up of the ISAT were published in 2009. Of 13 rebleeds from the treated aneurysm that occurred .1 year after treatment, 10 were in the coil group and only 3 were in the clipping group (P = .06).20 Although the risk of death at 5 years remained significantly lower in the coiled group (11%) than it was in the clipped group (14%; P = .03), the proportion of patients who were independent was similar in the 2 groups (83% with coiling, 82% with clipping).20 This, according to some, suggests that coiling and clipping are equivalent in the long term (although the benefit with coiling in terms of mortality is clear).11 ISAT was criticized regarding several issues, the most important of which is the potential “cherry-picking” bias because 80% of the patients who were initially screened were eventually excluded (7416 of 9559) from the trial. This begs the question, Are the results generalizable to the 7416 patients who were treated
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outside the study?21 In addition, doubts were raised about the level of expertise of participating neurosurgeons, some of whom clipped ,10 aneurysms per year, as opposed to the interventionalists, who were some of the most experienced in the world. Additionally, the results were statistically significant only for an mRS score of 3 to 6, but not 0 to 1 or 0 to 3. Moreover, it is not appropriate to make generalizations of the results to all intracranial aneurysms because, for example, only 14% of middle cerebral aneurysms were treated with coiling and ,10% of patients with basilar aneurysms underwent microsurgery. Lastly, it is not possible to extend the findings of ISAT to unruptured aneurysms because only patients with subarachnoid hemorrhage (SAH) were enrolled. Despite these potential limitations, ISAT remains a major trial of endovascular vs surgical treatment of intracranial aneurysms, and the impact it had on clinical practice was unprecedented. In fact, the proportion of patients undergoing endovascular treatment of aneurysms has increased since the publication of the ISAT study both in the United States and abroad.22-24 The mortality from SAH has also decreased since publication of ISAT, presumably because of a larger proportion of patients receiving endovascular treatment.23 The increasing use of endovascular techniques has not been limited to ruptured aneurysms in the United States but has also involved unruptured aneurysms.25 This trend indicates that minimally invasive approaches are becoming heavily favored over traditional approaches by patients.26 In our institutional experience at Jefferson Hospital for Neuroscience, 2000 was the last year that more patients were treated by microsurgical than endovascular means. As the years have progressed, more patients have been treated endovascularly primarily because of experience and improvement in neurointerventional technology. The continued referral of patients has maintained our surgical volume, and most important, the patients who are being referred for surgical treatment generally have aneurysms that are more difficult to treat on the basis of our experience. At our institution, we have performed a case-control analysis on 247 patients who crossed over from an endovascular to a surgical approach. Results were controlled for age, neurological grade, medical and surgical comorbidities, and aneurysm site. In patients who were #60 years of age with anterior circulation aneurysms (38% of the group), endovascular and microsurgical interventions yielded similar outcomes. Of the Hunt and Hess grade I and II SAH patients #60 years of age, 9.9% of patients in the endovascular group compared with 11.1% in the microsurgical group had an mRS score between 3 and 6 (difference not statistically different). However, SAH patients with Hunt and Hess grades III and IV and anterior circulation aneurysms showed clear differences between endovascular and surgical outcomes. Twenty-one percent of patients treated endovascularly had an mRS score of 3 to 6 compared with 33% of patients treated microsurgically. In the subgroup of patients who were $60 years of age with posterior circulation aneurysms (156 of 247 patients, 62%), endovascular intervention always had a more favorable outcome compared with open microsurgery.27 Specifically, low-grade SAH
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patients (grades I and II) had an mRS score between 3 and 6 in 12% of the endovascular group compared with 29% of the microsurgical group. Similarly, high-grade SAH patients (grades III and IV) had an mRS score between 3 and 6 in 22% of the endovascular group as opposed to 37% of the microsurgical group. These results are very similar to those of the recently published Barrow Ruptured Aneurysm Trial (BRAT). In the discussion of endovascular vs open surgical treatment of intracranial aneurysms, BRAT deserves mention. BRAT is a prospective randomized controlled trial with an intent-to-treat design that compared endovascular coiling and surgical clipping in patients with ruptured aneurysms.16 In response to the perceived shortcomings of ISAT, the BRAT investigators included all patients with SAH admitted during the study period. Treatment was performed by experienced vascular and endovascular neurosurgeons. A total of 472 patients were enrolled and assigned to clipping (n = 239) or coiling (n = 233). Because crossover was allowed, only 124 (62%) of 199 patients assigned to the endovascular group underwent coiling (the remaining 75 were clipped) while 205 (98%) of 209 patients assigned to the surgical group underwent clipping. As in the ISAT, poor outcomes at 1 year in the BRAT were found to be less common in patients treated with endovascular treatment (23.2% vs 33.7%). Although treatment durability was a significant concern in ISAT, no patient in BRAT experienced a rebleeding episode after endovascular therapy. This improvement in endovascular treatment efficacy is likely the result of recent refinements in embolization techniques and devices. After a follow-up of 3 years in BRAT, the risk of a poor outcome with clipping compared with coiling (35.8% vs 30%) decreased from that observed at 1 year and was no longer significant (P = .25). In addition, aneurysm occlusion (P = .001) and aneurysm recurrence/retreatment (P = .01) were significantly
better after clipping. Although outcomes of posterior circulation aneurysms were significantly better in the coil group, there was no difference in outcome for anterior circulation aneurysms. Criticism of BRAT has focused on the high crossover rate (which is problematic in a randomized trial), the relatively small sample size, and the generalizability of the study findings (Can the same surgical results be achieved with less experienced neurosurgeons?). In an accompanying comment, Molyneux et al28 criticized the design and findings of BRAT, stating that the study did not conform to the standard reporting criteria of clinical trials (set out in the CONSORT [Consolidated Standards of Reporting Trials] criteria) and that the investigators performed subgroup analyses that had not been prespecified in a published protocol, in addition to having a substantial number of missing outcomes and a sample size that was inadequate to draw conclusions. Some have even argued that “the BRAT was not, in fact, a randomized trial, but a registry of patients treated in 1 of 2 ways. . ..”12 Overall, although it has become common today to oppose the findings of BRAT to those of ISAT, it is our belief that the 2 trials yielded comparable results: Endovascular therapy provides a significant outcome benefit for ruptured aneurysms, although in the long term this benefit seems to progressively dissipate. As well stated by Lanzino,13 however, this does not negate the superiority of coiling because no patient would elect to undergo a treatment that requires years to reach equivalent outcomes.
TREATMENT DURABILITY Treatment durability has been the major concern with endovascular treatment of cerebral aneurysms (Figures 2 and 3). The recurrence rate is 24% to 35% for posterior circulation aneurysms, 18% to 32% for middle cerebral artery aneurysms,
FIGURE 2. A 49-year-old female patient who presented as a grade IV improved to grade III with ventriculostomy. A, the frontal view of this aneurysm. Because of the patient’s grade, the aneurysm was treated with an endovascular means. B, the initial films demonstrate adequate occlusion with a balloon-assisted technique; however, at the 60-month follow-up, there was recurrence of the aneurysm at the base (C), and she was treated with microsurgical clip ligation. At this point, the patient essentially went into surgery as a grade 0, having recovered from a quite severe subarachnoid hemorrhage, and the microsurgical exercise was fairly straightforward.
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FIGURE 3. A, an anterior communicating artery aneurysm projecting inferiorly that clearly has a wide neck; however, because of the neurological grade, the aneurysm was treated with coil occlusion. B, there is early recanalization at the base of the aneurysm at the 6-month follow-up. C, the aneurysm was treated microsurgically, leaving the coils in place and occluding only the portion of the aneurysm that had recanalized.
37% for posterior communicating artery aneurysms, 25% for anterior communicating artery aneurysms, 26% for carotid ophthalmic artery aneurysms, 40% for cavernous aneurysms, and 12% to 29% for paraclinoid aneurysms.29 The Cerebral Aneurysm Rerupture After Treatment study identified the degree of aneurysm occlusion after initial coiling as a strong predictor of subsequent hemorrhage, prompting an emphasis on achieving better initial aneurysm occlusion. The use of stenting and balloon remodeling techniques yields higher degrees of aneurysm occlusion and improves treatment durability.30-41 Furthermore, we have found in a comparative study that stent-assisted coiling provides higher occlusion rates with lower retreatment rates and no additional morbidity in wide-necked aneurysms.26 In a follow-up study from the ISAT, the rates of retreatment were compared between the surgical and endovascular arms and
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were found to be significantly higher after coiling.42 Specifically, retreatment was performed in 191 of 1096 patients (17.4%) in the endovascular group vs 39 of 1012 patients (3.8%) in the clipping group. Most retreatments were performed at an early time point after clipping, whereas after coiling, retreatments continued to be performed throughout the follow-up period. This again indicates that clipping provides better treatment durability and raises questions about whether the benefit seen with endovascular therapy can be sustained in the long run. This could be a concern especially in young patients. In fact, surgical clipping is usually preferred in young patients because of its longterm durability. Along these lines, the authors of the ISAT noted that the absolute difference in poor outcome rates between coiling and clipping is lower in patients ,50 years of age (3.3%) than it is for those .50 years of age (10%). They concluded that
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the long-term protection from SAH afforded by surgical clipping could give this treatment modality an advantage in life expectancy over coiling for young patients (,40 years of age).43 In our experience, endovascular therapy is a valuable option for young patients with aneurysmal SAH.44 We recently performed an analysis on 40 patients ,35 years of age (mean, 30 years; range, 17-35 years) who presented to our institution with aneurysmal SAH. Thirty-five patients (87.5%) were treated with coil embolization vs only 5 with craniotomy and clipping. Up to 85% of patients treated with endovascular therapy had a favorable outcome, and no patient experienced a rehemorrhage after endovascular treatment. Although the need for retreatment is considered a disadvantage of endovascular techniques, it should be noted that recoiling in the few cases when it is mandated has a very low complication rate (much lower than the initial treatment) and does not negate the original benefit of endovascular treatment.45 Furthermore, the use of balloon- and stentassisted techniques has significantly improved the durability of endovascular treatment.15,37,40,41 The importance of long-term follow-up in young patients undergoing coil embolization cannot be overemphasized.
NEUROPSYCHOLOGICAL OUTCOMES AND COST-EFFECTIVENESS With regard to neuropsychological outcomes, an interesting study that included patients from the ISAT showed that cognitive impairment occurred in approximately one-third of patients who were not otherwise disabled (mRS score, 0-2) and was more frequent after clipping (38.7%) than after coiling (26.7%; P = .005). Rates of neurocognitive deficits in each assessed domain were greater after clipping, especially for verbal memory (P = .03), processing speed (P = .008), executive skills (P = .06), and spatial working memory (P = .09). Several other studies have also demonstrated the superiority of coiling over clipping in this respect.46-48 These data remind us that quality of life and neurocognition are important factors that are poorly studied in randomized trials and are not reflected by the mRS (which measures mostly functional independence). Cosmesis is also particularly valued by patients, especially those who are young. Hence, it is not surprising that most patients with cerebral aneurysms, especially younger patients, elect to undergo the minimally invasive and less traumatic procedure. Therefore, information on cognitive, psychosocial, and cosmetic outcomes of the 2 interventions is essential when counseling patients and their families. With regard to the cost-effectiveness of the 2 procedures, one may assume that the high cost of the coils and endovascular devices makes coiling a more costly procedure than clipping. However, a study of patients randomized in ISAT analyzing resource use and costs up to 24 months after endovascular and neurosurgical treatment reported that there was no significant difference in costs between the 2 interventions at 12 or 24 months.49 On closer inspection, coiling had higher costs for the initial procedure, for
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the number and length of stay of subsequent procedures, and for follow-up angiograms. However, these higher costs were offset by lower costs related to length of stay for the initial procedure. Likewise, a recent study analyzing inpatient and outpatient costs associated with surgical or endovascular treatment of patients with unruptured aneurysms in the United States found similar overall costs at 2 and 5 years. Although hospital length of stay and costs associated with the initial procedure were higher with clipping, the number of postoperative angiograms and outpatient services used during the follow-up was significantly higher with coiling.50
THE CASE FOR SMALL ANEURYSMS The best treatment modality for patients with small ruptured aneurysms remains unclear. The ISAT investigators excluded all patients with small aneurysms from their study, and the BRAT investigators assigned these patients preferentially to the surgical arm. Small aneurysms pose significant technical challenges to endovascular therapy because of the difficulties in catheterizing the aneurysm, stabilizing the microcatheter, and safely deploying coils. Several authors have reported a high risk of intraprocedural rupture with coiling of small aneurysms.51 For these reasons, surgical clipping has been considered to be the preferred treatment for these lesions. We have recently compared surgical and endovascular options in 161 patients with small ruptured aneurysms treated at our institution (91 with endovascular therapy and 60 with surgical clipping).52 We found a significantly lower rate of procedural complications with endovascular therapy (9.8%) compared with open surgery (23.3%). Importantly, only 3.7% of patients experienced an intraprocedural aneurysm rupture during endovascular treatment. These findings indicate that endovascular therapy, if technically feasible, may serve as a treatment alternative for small ruptured aneurysms, although randomized controlled studies are required to provide definitive information on the best therapeutic approach.
SPECIFIC SITUATIONS The choice between surgical and endovascular options for the treatment of aneurysms should take into consideration several factors, including aneurysm location, configuration, clinical grade, and medical comorbidities (Figure 4). Middle cerebral artery aneurysms pose significant technical challenges to endovascular coiling, and in this particular location, surgical clipping may provide more favorable results.53 Patients with a large intraparenchymal hematoma should undergo open surgery for aneurysm clipping and simultaneous clot evacuation and decompression. It should be noted that in selected patients with aneurysmal SAH and associated intraparenchymal hematoma, endovascular aneurysm obliteration before surgical decompression is also an acceptable alternative that can simplify open surgery to hematoma evacuation and decompression.54 Elderly patients and those presenting with poor neurological grades (Hunt and Hess grades IV and V) are more likely to benefit from
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FIGURE 4. A, a large aneurysm of the posterior carotid wall (left). This patient presented with a grade III subarachnoid hemorrhage, and coiling allowed what appeared to be complete occlusion (right). However, this patient experienced a hemorrhage approximately 12 hours after the complete occlusion with a very poor outcome with an associated ultimate mortality (B). This was most likely due to a ball valve mechanism in which blood was dissecting around the coil mass into the posterior aspect of the aneurysm, which led to a delayed hemorrhage.
an endovascular procedure.53 In a subgroup analysis of ISAT, 72.0% of elderly patients with anterior circulation aneurysms allocated to coiling were independent compared with only 52.0% allocated to clipping (P , .05).55 In our institution, Hunt and Hess grade V patients are generally considered for endovascular management only after clinical improvement with placement of ventriculostomy. Patients with multiple medical comorbidities, bleeding diathesis, or thrombotic disease requiring chronic anticoagulation are also considered for endovascular treatment. Likewise, in basilar tip aneurysms, endovascular therapy has yielded more favorable results than microsurgery.56 In our institution, posterior circulation aneurysms in general and basilar tip aneurysms in particular are almost always treated by endovascular means.30 We have found the use of self-expanding stents to improve treatment durability for basilar tip aneurysms with no added morbidity.57 Proximal posterior inferior cerebellar artery aneurysms are better treated by endovascular means, whereas in distal aneurysms, both modalities provide favorable results.58 In a study from our institution that included 76 patients, coiling of posterior inferior cerebellar artery aneurysms was associated with a morbidity rate of only 2.8%, with favorable outcome at follow-up in 93% of patients with unruptured aneurysms and in 78.7% of those with ruptured aneurysms.58 Patients with multiple intracranial aneurysms and unknown source of bleeding should also be considered for an endovascular procedure. Finally, the presence of significant vasospasm, moderate atherosclerosis, and tortuosity of proximal vessels is usually a contraindication to endovascular treatment.
OUR INSTITUTIONAL PROTOCOL FOR COILING OF RUPTURED ANEURYSMS In our institution, all patients with SAH undergo arterial line and central venous line placement preoperatively. Patients with Hunt and Hess grades III or higher also are monitored with ventriculos-
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tomy and Swan-Ganz catheters. Endovascular procedures are performed under general endotracheal anesthesia and continuous neurophysiological monitoring, including somatosensory evoked potentials and electroencephalography and brainstem auditoryevoked responses. Generally, a half-bolus of heparin (50 U/kg) is administered after deployment of the first coil. The presence of an intraparenchymal hematoma or recent ventriculostomy placement (within the previous 2 hours) limits the use of intraoperative anticoagulation. Aneurysms are treated within 24 hours to avoid the risk of a devastating rehemorrhage.59 Arterial access is obtained through femoral puncture by use of the Seldinger technique, and an arterial sheath is inserted and secured with a stitch. The guiding catheter is introduced and navigated into each studied vessel with the aid of a guidewire. A 6-vessel angiogram, including bilateral external carotid, internal carotid, and vertebral arteries, is required when the source of the SAH is unclear. Three-dimensional angiography allows precise measurements of the aneurysm size and dome-to-neck ratio with accurate depiction of the aneurysm neck and its relation to parent and branching vessels. Aneurysms with a small (,4 mm) neck and a favorable dome-to-neck ratio ($2) can usually be coiled without stent or balloon assistance. Through the guiding catheter, a microcatheter is advanced over a microguidewire and subsequently placed in the aneurysm lumen, preferably away from the neck. Next, coils are deployed under direct angiographic guidance. The mean arterial pressure is lowered by 15% to 20% during coil deployment. Coils of various shapes (helical, spherical), lengths (1-30 mm), diameters, softness, and design (bioactive vs bare platinum) are available. The initial coil is usually complex shaped and fills the aneurysm in a basket-like configuration. Once optimal positioning is achieved, the coil is detached. Additional coils of progressively decreasing size and variable shapes are then deployed until complete aneurysm obliteration is achieved (ie, no aneurysm filling is noted in at least
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3 distinct biplane views and under normal blood pressure). The last “finishing” coils are usually helical shaped to allow better filling of the residual aneurysm. After aneurysm obliteration, the mean arterial pressure is maintained between 90 and 100 mm Hg to prevent vasospasm and thromboembolic events. Stent-assisted coiling requires dual antiplatelet therapy to minimize the thromboembolic risk related to stent placement.60-62 The use of antiplatelets in the setting of SAH, however, may be associated with hemorrhagic complications related to ventriculostomy placement, aneurysmal rebleeding, and potential need for future invasive procedures.3 Balloon remodeling, which relies on a temporarily inflated balloon in the parent artery to prevent coil prolapse and to allow dense coil packing of the aneurysm, can be performed without the use of dual antiplatelet agents, making it another attractive option for treatment of acutely ruptured wide-necked and complex intracranial aneurysms.63 In a recent study from our institution in which we compared the safety and efficacy of stenting and balloon remodeling in 84 acutely ruptured aneurysms, we found that procedural complications (hemorrhagic and thromboembolic) and clinical outcomes did not differ significantly between the 2 techniques.64 These data suggested that stent-assisted coiling was an acceptable alternative to balloon remodeling for complex aneurysms in the acute phase of SAH.
THE EMERGENCE OF FLOW DIVERTERS Flow diverters like the Pipeline Embolization Device (PED) are revolutionary tools for intracranial aneurysms and have generated great enthusiasm in the neurovascular community. Flow diverters provide a physiological approach to the treatment of intracranial aneurysms through a combination of flow redirection and endoluminal vessel reconstruction (from neointimal growth along the vessel). Treatment with flow diverters was initially reserved for large, giant, and otherwise untreatable aneurysms of the internal carotid artery. Recently, at our institution and several other centers, the PED has become a routine first-line treatment for several types of aneurysms in various intracranial locations.34-40 At the Jefferson Hospital for Neuroscience, we have treated .250 aneurysms with the PED since its approval by the US Food and Drug Administration, and we have noted a dramatic decrease in the complication rate after an initial learning curve phase.40 The Pipeline procedure is also much simpler than coil embolization or stent-assisted coiling and requires significantly shorter fluoroscopy and procedure times.65 Moreover, flow diversion is more economical than conventional strategies.66 The safety, practicality, ease of use, high efficacy, and cost benefit of the PED have all led to a dramatic decline in the use of coils, especially for unruptured aneurysms. A case-control study from our institution suggests that the PED is a preferred treatment over traditional strategies for unruptured large and giant aneurysms because it provides higher occlusion rates with no added morbidity or poor outcomes.37 We have also found
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a similar benefit with flow diversion in small unruptured aneurysms of the anterior circulation.67 However, the use of the PED in ruptured aneurysms is generally considered to be controversial because of the need for dual antiplatelet therapy. At our institution, we generally avoid using the PED in patients presenting with SAH, although we have found the PED to be a valuable treatment for blister aneurysms and some other aneurysms that are not amenable to conventional modalities.
CONCLUSION The best technique for treating an aneurysm is the one that will produce the best result for a given patient and is dependent on many factors, including the expertise of the treating team. Management should always be tailored to the individual patient, taking into account all available data (specific for the patient, lesion, and treating team) and using whatever treatment modality is necessary to achieve the best outcomes for our patients. Disclosure Dr Jabbour has been a consultant for ev3, Codman, and Mizuho. Dr Tjoumakaris has been a consultant for Stryker. Dr Rosenwasser has been a consultant for Boston Scientific. Dr Chalouhi reports no disclosures.
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63. Chalouhi N, Jabbour P, Tjoumakaris S, et al. Single-center experience with balloon-assisted coil embolization of intracranial aneurysms: safety, efficacy and indications. Clin Neurol Neurosurg. 2013;115(5):607-613. 64. Chitale R, Chalouhi N, Theofanis T, et al. Treatment of ruptured intracranial aneurysms: comparison of stenting and balloon remodeling. Neurosurgery. 2013;72 (6):953-959. 65. 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;6:291-295. 66. Colby GP, Lin LM, Paul AR, Huang J, Tamargo RJ, Coon AL. Cost comparison of endovascular treatment of anterior circulation aneurysms with the pipeline embolization device and stent-assisted coiling. Neurosurgery. 2012;71(5):944-948; discussion 948-950. 67. Chalouhi N, Starke RM, Yang S, et al. Extending the indications of flow diversion to small, unruptured, saccular aneurysms of the anterior circulation. Stroke. 2014; 45(1):54-58.
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