CHAPTER 375 Endovascular Coiling of Intracranial Aneurysms
Supporting Evidence
The Rise of Endovascular Technique
While there were earlier efforts to introduce materials into aneurysms to induce thrombosis,6,7 the use of entirely endovascular techniques to treat intracranial aneurysms began with initial attempts in the 1960s. These treatments included endovascular techniques to occlude parent vessels and the use of detachable balloons, cyanoacrylate, and “pushable” metallic coils to directly occlude aneurysms while preserving the parent artery.8–14 With progressive improvement in angiographic and computer capabilities, the ground work was established for the development of modern methods of endovascular therapies.
The Guglielmi detachable coil was developed in the 1980s with the first use in a human brain aneurysm occurring in 1990.15 The crucial breakthrough that allowed this technology to flourish was the “detachable” component.16 Before this development, platinum coils could be pushed through microcatheters into intracranial aneurysms, but there was no practical way to retrieve or reposition the coils if the initial placement was not satisfactory. With the development of a reliable detachment system, the coils could be positioned, and if needed, easily retrieved or repositioned as desired, to be detached as a permanent implant only when the positioning was deemed acceptable. The clinical trial that resulted in approval from the U.S. Food and Drug Administration (FDA) ran through the early 1990s with FDA approval in 1995. In the years that have followed, increased experience and many incremental technological changes have resulted in further improvements. Multiple coil systems now exist with a wide variety of available coil characteristics and detachment systems. Although there are many coil systems, these recent developments are the direct descendent of the original Guglielmi detachable coils.
With the early experience, however, it was soon apparent that many of the aneurysms that were difficult to treat by surgical clipping were also more difficult than other aneurysms to treat with detachable coils. This problem was most readily apparent for aneurysms that were wide necked and/or large.17–19 Over time, this limitation shifted the dynamic away from viewing detachable coils as a complementary technology fulfilling the unmet need of treating “unclippable aneurysms” to a situation where endovascular techniques were increasingly perceived to be, and used as, a competitive or even replacement technology for surgical clipping. Posterior circulation aneurysms were particularly singled out as aneurysms to be preferentially treated by endovascular means.17,20,21
Throughout the 1990s, the majority of literature published regarding endovascular therapy (EVT) for intracranial aneurysms consisted of single-center, retrospective, self-reported series.22–25 End points varied widely, as would be expected with a developing treatment modality, and lack of a common reporting language made comparisons difficult. As noted previously for reports regarding surgical clipping, the question of publication bias and generalizability of results loomed large. While there was early evidence suggesting that endovascular treatment was protective against subsequent rehemorrhage,26 the recognition that many aneurysms were not completely occluded left concerns regarding the potential risks of delayed recurrence, the need for retreatment, or worse, the possibility of new subarachnoid hemorrhage despite endovascular treatment.27–29
This essential phase, however, laid the groundwork for more sophisticated future analyses. In the course of reporting their case series of unruptured intracranial aneurysms, Roy and coworkers described a simple grading system for classifying the degree of aneurysm occlusion achieved.30 They went on to apply this scale to their overall series of aneurysms, noting that recurrences often occurred more than 1 year after the initial treatment, emphasizing the need for diligent long term follow-up.29
During this period of the late 1990s and early 2000s, as experience and confidence with the use of endovascular techniques were growing, there were at the same time increasingly pointed questions being asked about open surgical treatment of intracranial aneurysms. In particular, the International Study of Unruptured Intracranial Aneurysms (ISUIA) raised questions about both the natural history of unruptured intracranial aneurysms and the safety of surgical clipping.31 In the initial report from this group, published in 1998, the authors suggested that the risk of rupture in untreated aneurysms was much lower than previously thought, and for this reason the study attracted considerable attention and called into question the value of prophylactic surgical clipping of unruptured intracranial aneurysms. However, this study was significantly biased because the aneurysms included in the study were primarily lesions that clinicians felt were better managed by conservative means. This flaw was particularly striking in the initially retrospective study.
In 2003 the ISUIA group published an update of their study and noted a substantial increase in the observed rate of aneurysm rupture, with the updated rates being more consistent with those seen in previously published, well-accepted natural history studies.32,33 The treatment-related morbidity and mortality as evaluated 1 year after treatment remained high, particularly from surgical clipping: 12.6% in patients that had not previously suffered subarachnoid hemorrhage. The morbidity and mortality for endovascular therapy in patients that had not previously experienced subarachnoid hemorrhage was lower at 9.8%, but the patients treated by the two modalities were not matched cohorts. Indeed, the patients treated endovascularly were older, had larger aneurysms, and more posterior circulation aneurysms.
Other evidence was accumulating during this time period similarly suggesting that surgical clipping morbidity and mortality were both higher than generally reported and that outcomes were more likely to be favorable in centers with larger case volumes where endovascular therapy was also available. Johnston and coworkers examined data from university hospitals in the United States looking at discharge disposition of patients having unruptured aneurysms treated either by clipping or endovascular techniques.34 They found that 18.5% of surgically clipped patients died or had been discharged other than to their home but that this undesirable outcome was seen in only 10.6% of the patients treated by endovascular means. Once again, however, it is important to note that these were not matched cohorts. Johnston then looked at a statewide database for the state of California and found similar disparities between the two modalities, again with endovascular therapy having fewer poor outcomes (25% versus 10%) and with fewer in-house deaths (3.5% versus 0.5%).35 A similar review of outcomes for New York State was published in 2003 by Berman and associates. Again in this analysis the hospital volume and propensity of a hospital to use endovascular therapy were both associated independently with better patient outcomes.36 Barker and coworkers and Hoh and associates analyzed nationwide Medicare data regarding surgical clipping and endovascular therapy, respectively, for unruptured aneurysms. These Medicare databases covered the years 1996-2000 and similarly showed better outcomes in larger volume centers and overall fewer poor outcomes in patients treated with endovascular methods.37,38 It is important to reiterate that these studies were not by any means comparing matched patients and that in no way did they suggest that one modality of treatment was better than the other for any individual patient. What was important about these studies was that they helped to quantify treatment-related morbidity and mortality. In addition, they drew attention to the possibility that a comprehensive approach, which included endovascular techniques, may result in overall better outcomes.
Ruptured Aneurysms
The first randomized prospective study looking at endovascular versus surgical treatment of ruptured cerebral aneurysms was published by Koivisto and coworkers in 2000.39 Overall outcome at 1 year was assessed using the Glasgow Outcome Scale. While the small sample size did not show any statistical difference in the two well-matched groups, a good recovery was reported in 40 of 52 (76.9%) of the endovascular patients but in only 38 of 57 (66.6%) of the surgical patients.39 They noted comparable 1-year neuropsychological outcomes among patients that had enjoyed a good recovery but only included patients that could complete all neuropsychological testing in the neuropsychological analysis. In view of subsequent larger studies favoring endovascular therapy by a similar magnitude, but with statistical significance, the possibility of a type II error is possible in this small study.
In 2002, the initial report of the International Subarachnoid Aneurysm Trial was published in the Lancet. The trial was stopped by the steering committee on the basis of interim analysis favoring endovascular therapy over surgical clipping for ruptured aneurysms. The publication of these results has come to represent a watershed moment in aneurysm treatment.40 To be included in this trial, patients were reviewed and deemed appropriate for both treatment modalities. The key finding of this trial was that there were more poor outcomes in patients assigned to surgical clipping as compared to patients treated by endovascular coiling (30.6% versus 23.7%) with relative and absolute risk reductions of 22.6% and 6.9%, respectively. Poor outcome, meaning a clinical outcome of dead or disabled, was defined according to the modified Rankin Outcome Scale (mRS) dichotomized such that a score of 3 or greater constituted a poor outcome. This trial has continued to provide valuable insights as ongoing follow-up has addressed critical questions such as the durability of endovascular treatment. With subsequent follow-up after the 1-year results for all patients were available, the benefit of endovascular therapy over surgical clipping at 1 year was an absolute value of 7.4% fewer poor outcomes.41
What is striking about the BRAT results is the similarity to the ISAT outcomes and indeed to the earlier study by Koivisto and associates.39–41 All three studies indicate a similar magnitude of advantage for endovascular therapy over surgical clipping at the 1-year posttreatment time point. It is important to note that the BRAT cohort included a much higher percentage of poor grade patients and also that significant developments had occurred in endovascular technology between the time of ISAT and BRAT. This latter fact, together with the smaller sample size, may account for the absence of any rehemorrhage events among the endovascularly treated BRAT patients. The general agreement between the two studies suggests that the ISAT results may be more broadly applicable than the ISAT results alone suggest. Equally important, however, is that it is apparent in both studies that there remains an important role for open surgical treatment of ruptured intracranial aneurysms. Intuitively, this role is primarily linked to the technical limitations of endovascular treatment, limitations which are continuously in transition.
While the relatively short-term outcome point of 1 year favors endovascular therapy it is equally important to know whether or not the treatment advantage is durable. Specifically, could the initial benefit demonstrated for endovascular treatment be eroded because of ongoing need for retreatment or recurrent subarachnoid hemorrhage? Again, ISAT provides the best data available regarding this question. In the ISAT analysis, any adverse clinical impact from retreatment or rehemorrhage during the first year was captured in the 1-year outcome results. Retreatment in ISAT was significantly more frequent among patients undergoing endovascular therapy (EVT).42 For purposes of this study patients were analyzed based upon actual treatment rather than according to assigned treatment as had been the case for the outcome analysis. Retreatment was performed in 17.4% of the EVT patients versus 3.8% of the surgically treated patients. Retreatments tended to occur more frequently in younger patients with larger aneurysms and at a later time point than clipped aneurysms. Procedural complications of late retreatment in EVT patients resulted only in transient neurological symptoms with no change in mRS scores. This is consistent with other reports of low morbidity associated with elective retreatments.43–46
A related concern is that of delayed rehemorrhage. Recurrence and retreatment are relatively more common and therefore are often used as a surrogate for the much rarer problem of recurrent subarachnoid hemorrhage. Attempting to address this concern from the ISAT data, Mitchell and coworkers focused on the younger ISAT patients who are facing a longer “at-risk” period following treatment for a ruptured aneurysm. They noted that in the ISAT data, patients younger than age 50 did not have as large an initial benefit from coiling as did older patients, and they questioned whether this smaller initial benefit coupled with a longer at-risk period might eventually erode the initial treatment advantage of endovascular therapy. The observed rate of recurrent hemorrhage after clipping was 0.063% versus 0.21% per patient year for the endovascular patients, giving an excess rehemorrhage rate of approximately 0.15% per patient year for the endovascular patients. The possibility that the lower risk of the initial endovascular procedure could be overcome by recurrent hemorrhage clearly depends on whether or not this rate changes and the life expectancy of the treated patient. While recognizing the speculative nature of the future projections, the authors concluded that for patients younger than age 40 this may be a significant concern.47 For the ISAT group as a whole, however, there remained at 5 years after a subarachnoid hemorrhage a significantly higher mortality rate among the surgically clipped patients as compared to the EVT patients (11% versus 14%) although the proportion of independent survivors was similar among the two groups.48
Unruptured Aneurysms
The problem of the incidental, unruptured aneurysm is in many ways a more complicated and difficult one than that posed by ruptured intracranial aneurysms. Almost no facet of the issue is without significant controversy. The controversies start with the estimation of the natural history risk of unruptured aneurysms, proceed through treatment versus conservative management decisions and continue on to treatment modality, if indeed treatment is recommended. As mentioned earlier in this chapter, these controversies intensified with the reports of the International Study of Unruptured Intracranial Aneurysms in 1998 and 2003. The status quo thinking was challenged by these reports, which suggested both a more benign natural history and a higher treatment risk than had generally been accepted. With the publication of the second of these reports, the natural history risk was revised upward compared with the initial report, and as a result there has been some rapprochement towards previously accepted natural history risk estimates. This natural history hemorrhage risk for an unruptured intracranial aneurysm is now widely agreed to be in the range of 1% per year for aneurysms 7 to 10 mm in diameter.49,50
For larger aneurysms it is clear from the ISUIA reports that the natural history risk is higher and particularly so for posterior circulation aneurysms. For anterior circulation aneurysms sized 7 to 12, 13 to 24, and 25 ml or more in patients without a prior history of subarachnoid hemorrhage, the respective 5-year cumulative rupture rates were 2.6%, 14.5%, and 40%. Similarly for posterior circulation aneurysms in these categories, the cumulative 5-year hemorrhage rates were respectively 14.5%, 18.4%, and 50%.32 Because this study was prospective but not randomized, it should be born in mind that these hemorrhage rates were in patients specifically selected not to undergo treatment and that these hemorrhage rates may be artificially low as a result of this systemic selection bias. In other words, this natural history estimate may in fact represent a “best case” natural history scenario.
Having ascertained an admittedly imperfect estimate of the natural history, the next question to be considered is the risk of treatment. With respect to endovascular treatment, this is fortunately becoming clearer. Prospective, independently adjudicated multicenter studies are being published, and additional similar studies currently underway will help to further define the risk of EVT for patients with unruptured aneurysms. While each study may be focused on a different aspect or technique of aneurysm treatment, cumulatively these studies are providing crucial benchmark data against which treatment alternatives may be compared.51–53 As additional studies are accomplished they will further refine meaningful, reliable benchmark estimates of procedural safety, immediate treatment results, and also the results of ongoing follow-up. Similarly, reporting standards are being promulgated, which will hopefully lead to more uniform and relevant end points making comparison among studies easier.54
The HELPS trial was the first of these multicenter, prospective, randomized, core lab adjudicated studies to report early treatment results. This study included both ruptured and unruptured aneurysms. Coiling was attempted in 499 patients and coils were successfully deployed in 99.2% of patients. Because both ruptured and unruptured aneurysm patients were included, it is difficult from the published data to glean detailed outcome data on the unruptured aneurysm patients alone. The hard end point of mortality within 3 months of treatment of unruptured aneurysms was noted in only in 2 of 218 (0.9%) of unruptured aneurysm patients in the trial. At the time of discharge from the hospital, 184 of 218 (84.4%) World Federation of Neurosurgical Societies (WFNS) Grading Scale 0 patients remained grade 0, while 29 of 218 (13.3%) were discharged in good clinical grade (1 or 2) and only 5 of 218(2.3%) were grade 3 or missing data.52 It is likely that with longer follow-up, which will be reported upon completion of the trial, that many of the patients discharged as WFNS grades 1 or 2 from the hospital will have improved.
Also published in 2008, the multicenter French Society of Neuroradiology ATENA study (Analysis of Treatment by Endovascular Approach of Nonruptured Aneurysms) prospectively evaluated the immediate clinical outcome of endovascularly treated patients with unruptured intracranial aneurysms less than 15 mm in size. There were 739 aneurysms consecutively treated in 700 procedures. Treatment failed in 4.3% of aneurysms and technical adverse events were recorded in 15.4% of patients. Not all technical adverse events resulted in patient morbidity. Thromboembolic events occurred in 7.1% and procedural hemorrhages in 2.6%. These adverse events resulted in neurological deficit in 5.4%, but at 30 days morbidity (defined as a modified Rankin score 2 or greater) and mortality rates were only 1.7% and 1.4%, respectively.53
More difficult to ascertain is the treatment morbidity of surgical clipping of intracranial aneurysms. Although there is an abundance of publications on this topic, there is no convincing consensus. This difficulty in the existing literature was provocatively reviewed by Lee and associates in their analysis of the literature for unruptured intracranial aneurysm treatment.55 These authors examined both the surgical and the endovascular literature for unruptured aneurysms from 1990 through July of 2003 and concluded that publication bias likely accounts for an underestimation of the surgical clipping morbidity and mortality. They additionally concluded that coiling studies were less likely to be subject to factors contributing to inaccurate adverse outcome rates. Higashida and coworkers reviewed a database of publicly available nonfederal hospital records examining treatment of unruptured aneurysms treated during the years 1998-2000. Specific parameters reviewed included adverse outcomes, in-hospital death, length of stay, and hospital charges. There were 2535 unruptured cerebral aneurysm cases evaluated. After multivariate adjustment, neurosurgical cases had 70% greater odds of an adverse outcome, 30% increased hospital charges, and 80% had a longer length of stay compared with endovascular cases (P < .05). It is important to note that there were not randomized patients.56 Other attempts through large databases and meta-analyses have measured morbidity ranging from 10.9% to 18.3% and mortality from 2.1% to 3.2% for surgical clipping of unruptured aneurysms.31,57
Retreatment: Treatment Efficiency
Because of the challenges associated with studying the important, but uncommon event of hemorrhage after EVT, most studies have instead looked to recurrence and retreatment as surrogates for this event in that these latter events may represent risk factors for future hemorrhage. In reality, the clinical significance of recurrence is not clear cut. Indeed, the MAPS trial currently in progress has as a primary end point “Target Aneurysm Recurrence” (TAR), which is a composite end point including rupture of the treated aneurysm, reintervention, and/or neurological death. The objectives of the study include correlating TAR with defined angiographic end points that may ultimately be used to predict the clinically more relevant elements of TAR. But it must be acknowledged that the end point of reintervention is inherently subjective and that there are no agreed upon criteria to trigger this action. It would be expected, for example, that most surgeons would be more likely to re-intervene for a recurrence identified in a younger person than they would be for a recurrence identified in an older or infirm patient. Similarly, it remains unclear as to which recurrences pose clinical risk and which are likely to be stable. Finally, there is considerable subjectivity interpreting angiographic parameters with considerable interuser variability even when well-accepted angiographic scales such as the modified Raymond scale29 or the simpler “same, better, worse” descriptors are used.58 In short, for the foreseeable future it is likely to be difficult to accurately measure the risk of hemorrhage after EVT and surrogate parameters for this outcome are yet to be validated.
In the meantime, clinical practice is likely to be driven by the intuitive belief that all other things being equal it is preferable to have no aneurysm remnant. This means that in clinically appropriate patients angiographic recurrences are likely to be treated. Fortunately, multiple studies have demonstrated that morbidity from retreatment is low.42–44,59,60
Barker F, Amin-Hanjani S, Butler W, et al. In-hospital morbidity and mortality after surgical treatment of unruptured aneurysms in the United States, 1996-2000: the effect of hospital and surgeon volume. Neurosurgery. 2003;52:995-1009.
Campi A, Najib N, Molyneux AJ, et al. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling of clipping in the international subarachnoid aneurysm trial (IAST). Stroke. 2007;38:1538-1544.
Eskridge JM, Song JK. Endovascular embolization of 150 basilar tip aneurysms with Guglielmi detachable coils: results of the Food and Drug Administration multicenter clinical trial. J Neurosurg. 1998;89:81-86.
Graves VB, Strother CM, Duff TA, et al. Early treatment of ruptured aneurysms with Guglielmi detachable coils: effect on subsequent bleeding. Neurosurgery. 1995;37:640-647.
Guglielmi G. History of the genesis of detachable coils: a review. J Neurosurg. 2009;111:1-8.
Guglielmi G, Vinuela F, Dion J, et al. Electrothrombosis of saccular aneurysms via endovascular approach, part 2: preliminary clinical experience. J Neurosurg. 1991;75:8-14.
Guglielmi G, Vinuela F, Duckwiler G, et al. Endovascular treatment of posterior circulation aneurysms by electrothrombosis using electrically detachable coils. J Neurosurg. 1992;77:515-524.
Hoh BL, Rabinov JD, Pryor JC, et al. In-hospital morbidity and mortality after endovascular treatment of unruptured intracranial aneurysms in the United States, 1996-2000: effect of hospital and physician volume. AJNR Am J Neuroradiol. 2003;24:1409-1420.
Johnston SC, Dudley RA, Gress DR, et al. Surgical and endovascular treatment of unruptured cerebral aneurysms at university hospitals. Neurology. 1999;52:1799-1805.
Johnston SC, Zhao S, Dudley RA, et al. Treatment of unruptured cerebral aneurysms in California. Stroke. 2001;32:597-605.
Koivisto T, Vanninen R, Hurskainen H, et al. Outcomes of early endovascular versus surgical treatment of ruptured cerebral aneurysms. A prospective randomized study. Stroke. 2000;31:2369-2377.
Molyneux AJ, Kerr RSC, Stratton I, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomized trial. Lancet. 2002;360:1267-1274.
Molyneux AJ, Kerr RSC, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomized comparison of effects on survival, dependency, seizures, rebleeding subgroups, and aneurysm occlusion. Lancet. 2005;366:809-817.
Raymond J, Guilbert F, Weill A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke. 2003;34:1398-1403.
Serbinenko FA. Balloon catheterization and occlusion of major cerebral vessels. J Neurosurg. 1974;41:125-145.
The CARAT Investigators. Rates of delayed rebleeding from intracranial aneurysms are low after surgical and endovascular treatment. Stroke. 2006;37:1437-1442.
, Unruptured intracranial aneurysms—risks of rupture and risks of surgical intervention. International Study of Unruptured Intracranial Aneurysms Investigators. N Engl J Med. 1998;339:1725-1733.
Van den Bergh WM, Kerr RS, Algra A, et al. International subarachnoid aneurysm trial (ISAT) collaborative group: Risk of recurrent subarachnoid haemorrhage, death or dependence and standardized mortality ratios after clipping or coiling of an intracranial aneurysm in the international subarachnoid aneurysm trial (ISAT): long-term follow-up. Lancet Neurol. 2009;8:427-433.
White PM, Lewis SC, Nahser H, et al. HELPS trial collaboration: Hydrocoil endovascular aneurysm occlusion and packing study (HELPS trial): procedural safety and operator-assessed efficacy results. AJNR Am J Neuroradiol. 2008;29:217-223.
Wiebers DO, Whisnant JP, Huston JIII, et al. International study of unruptured intracranial aneurysms investigators: Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103-110.
1 Dandy WE. Intracranial aneurysm surgery of the internal carotid artery. Ann Surg. 1938;107:654-659.
2 Alvord ECJr, Thorn RB. Natural history of subarachnoid hemorrhage: early prognosis. Clin Neurosurg. 1977;24:167-175.
3 Kurze T. Microtechniques in neurological surgery. Clin Neurosurg. 1964;11:128-137.
4 Drake CG. Bleeding aneurysms of the basilar artery: direct surgical management in four cases. J Neurosurg. 1961;8:230-238.
5 Solomon RA, Fink ME, Pile-Spellman J. Surgical management of unruptured intracranial aneurysms. J Neurosurg. 1994;80:440-446.
6 Werner SC, Blakemore AH, King BG. Aneurysm of the internal carotid artery within the skull: wiring and electrothermic coagulation. JAMA. 1941;116:578-582.
7 Mullan S, Beckman F, Vailati G, et al. An experimental approach to the problem of cerebral aneurysms. J Neurosurg. 1964;21:838-845.
8 Serbinenko FA. Balloon catheterization and occlusion of major cerebral vessels. J Neurosurg. 1974;41:125-145.
9 Kerber CW, Cromwell LD, Zanetti PH. Experimental carotid aneurysms: part 2. Endovascular treatment with cyanoacrylate. Neurosurgery. 1985;16:13-17.
10 Halbach VV, Higashida RT, Hieshima GB, et al. Aneurysms of the petrous portion of the internal carotid artery: results of treatment with endovascular or surgical occlusion. AJNR Am J Neuroradiol. 1990;11:253-257.
11 Higashida RT, Halbach VV, Dormandy B, et al. Endovascular treatment of intracranial aneurysms with a new silicone microballoon device: technical considerations and indications for therapy. Radiology. 1990;174:687-691.
12 Higashida RT, Halbach VV, Dowd C, et al. Endovascular detachable balloon embolization therapy of cavernous carotid artery aneurysms: results in 87 cases. J Neurosurg. 1990;72:857-863.
13 Serbinenko FA, Filatov JM, Spallone A, et al. Management of giant intracranial ICA aneurysms with combined extracranial-intracranial anastomosis and endovascular occlusion. J Neurosurg. 1990;73:57-63.
14 Casasco AE, Aymard A, Gobin YP, et al. Selective endovascular treatment of 71 intracranial aneurysms with platinum coils. J Neurosurg. 1993;79:3-10.
15 Guglielmi G. History of the genesis of detachable coils: a review. J Neurosurg. 2009;111:1-8.
16 Guglielmi G, Vinuela F, Dion J, et al. Electrothrombosis of saccular aneurysms via endovascular approach, part 2: preliminary clinical experience. J Neurosurg. 1991;75:8-14.
17 Guglielmi G, Vinuela F, Duckwiler G, et al. Endovascular treatment of posterior circulation aneurysms by electrothrombosis using electrically detachable coils. J Neurosurg. 1992;77:515-524.
18 Fernandez Zubillaga A, Guglielmi G, Viñuela F, et al. Endovascular occlusion of intracranial aneurysms with electrically detachable coils: correlation of aneurysm neck size and treatment results. AJNR Am J Neuroradiol. 1994;15:815-820.
19 Gruber A, Killer M, Bavinzski G, et al. Clinical and angiographic results of endosaccular coiling treatment of giant and very large intracranial aneurysms: a 7-year, single-center experience. Neurosurgery. 1999;45:793-803.
20 Bavinzski G, Richling B, Gruber A, et al. Endosaccular occlusion of basilar artery bifurcation aneurysms using electrically detachable coils. Acta Neurochir (Wien). 1995;134:184-189.
21 Eskridge JM, Song JK. Endovascular embolization of 150 basilar tip aneurysms with Guglielmi detachable coils: results of the Food and Drug Administration multicenter clinical trial. J Neurosurg. 1998;89:81-86.
22 Murayama Y, Vinuela F, Duckwiler GR, et al. Embolization of incidental aneurysms by using the Guglielmi detachable coil system. J Neurosurg. 1999;90:207-214.
23 Malisch TW, Guglielmi G, Vinuela F, et al. Intracranial aneurysms treated with Guglielmi detachable coil: midterm clinical results in a consecutive series of 100 patients. J Neurosurg. 1997;87:176-183.
24 Debrun GM, Aletich VA, Kehrli P, et al. Selection of cerebral aneurysms for treatment using Guglielmi detachable coils: the preliminary University of Illinois at Chicago experience. Neurosurgery. 1998;19:1176-1178.
25 Cognard C, Weill A, Spell L, et al. Long-term angiographic follow-up of 169 intracranial berry aneurysms occluded with detachable coils. Radiology. 1999;212:348-356.
26 Graves VB, Strother CM, Duff TA, et al. Early treatment of ruptured aneurysms with Guglielmi detachable coils: effect on subsequent bleeding. Neurosurgery. 1995;37:640-647.
27 Mericle RA, Wakhloo AK, Lopes DK, et al. Delayed aneurysm regrowth and recanalization after Guglielmi detachable coil treatment. J Neurosurg. 1998;89:142-145.
28 Horowitz M, Purdy P, Kopitnik T, et al. Aneurysm retreatment after Guglielmi detachable coil and nondetachable coil embolization: report of nine cases and review of the literature. Neurosurgery. 1999;44:712-719.
29 Raymond J, Guilbert F, Weill A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke. 2003;34:1398-1403.
30 Roy D, Milot G, Raymond J. Endovascular treatment of unruptured aneurysms. Stroke. 2001;32:1998-2004.
31 Unruptured intracranial aneurysms—risks of rupture and risks of surgical intervention. International Study of Unruptured Intracranial Aneurysms Investigators. N Engl J Med. 1998;339:1725-1733.
32 Wiebers DO, Whisnant JP, Huston JIII, et al. International study of unruptured intracranial aneurysms investigators: Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103-110.
33 Juvela S, Porras M, Poussa K. Natural history of unruptured intracranial aneurysms: probability of and risk factors for aneurysm rupture. J Neurosurg. 2000;93:379-387.
34 Johnston SC, Dudley RA, Gress DR, et al. Surgical and endovascular treatment of unruptured cerebral aneurysms at university hospitals. Neurology. 1999;52:1799-1805.
35 Johnston SC, Zhao S, Dudley RA, et al. Treatment of unruptured cerebral aneurysms in California. Stroke. 2001;32:597-605.
36 Berman MF, Solomon RA, Mayer SA, et al. Impact of hospital-related factors on outcome after treatment of cerebral aneurysms. Stroke. 2003;34:2200-2207.
37 Barker F, Amin-Hanjani S, Butler W, et al. In-hospital morbidity and mortality after surgical treatment of unruptured aneurysms in the United States, 1996-2000: the effect of hospital and surgeon volume. Neurosurgery. 2003;52:995-1009.
38 Hoh BL, Rabinov JD, Pryor JC, et al. In-hospital morbidity and mortality after endovascular treatment of unruptured intracranial aneurysms in the United States, 1996-2000: effect of hospital and physician volume. AJNR Am J Neuroradiol. 2003;24:1409-1420.
39 Koivisto T, Vanninen R, Hurskainen H, et al. Outcomes of early endovascular versus surgical treatment of ruptured cerebral aneurysms. A prospective randomized study. Stroke. 2000;31:2369-2377.
40 Molyneux AJ, Kerr RSC, Stratton I, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomized trial. Lancet. 2002;360:1267-1274.
41 Molyneux AJ, Kerr RSC, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomized comparison of effects on survival, dependency, seizures, rebleeding subgroups, and aneurysm occlusion. Lancet. 2005;366:809-817.
42 Campi A, Najib N, Molyneux AJ, et al. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling of clipping in the international subarachnoid aneurysm trial (IAST). Stroke. 2007;38:1538-1544.
43 Slob MJ, Sluzewski M, van Rooij WJ, et al. Additional coiling of previously coiled cerebral aneurysms: clinical and angiographic results. AJNR Am J Neuroradiol. 2004;25:1373-1376.
44 Ringer AJ, Rodriguez-Mercado R, Veznedaroglu E, et al. Defining the risk of retreatment for aneurysm recurrence or residual after initial treatment by endovascular coiling: a multicenter study. Neurosurgery. 2009;65:311-315.
45 Renowden SA, Koumellis P, Benes V, et al. 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;29:1401-1404.
46 Henkes H, Fischer S, Liebig T, et al. Repeat endovascular coil treatment in 350 of 2759 intracranial aneurysms: safety and effectiveness aspects. Neurosurgery. 2006;58:224-232.
47 Mitchell P, Kerr R, Mendelow AD, et al. Could late rebleeding overturn the superiority of cranial aneurysm coil embolization over clip ligation seen in the international subarachnoid aneurysm trial? J Neurosurg. 2008;108:437-442.
48 Van den Bergh WM, Kerr RS, Algra A, et al. International subarachnoid aneurysm trial (ISAT) collaborative group: Risk of recurrent subarachnoid haemorrhage, death or dependence and standardized mortality ratios after clipping or coiling of an intracranial aneurysm in the international subarachnoid aneurysm trial (ISAT): long-term follow-up. Lancet Neurol. 2009;8:427-433.
49 Mocco J, Komotar RJ, Lavine SD, et al. The natural history of unruptured intracranial aneurysms. Neurosurg Focus. 2004;17(5):E3.
50 Komotar RJ, Mocco J, Solomon R. Guidelines for the surgical treatment of unruptured intracranial aneurysms: the first annual J. Lawrence Pool memorial research symposium—controversies in the management of cerebral aneurysms. Neurosurgery. 2008;62:183-194.
51 Cloft HJ. Hydrocoil for endovascular aneurysm occlusion (HEAL) study: periprocedural results. AJNR Am J Neuroradiol. 2006;27:289-292.
52 White PM, Lewis SC, Nahser H, et al. HELPS trial collaboration: Hydrocoil endovascular aneurysm occlusion and packing study (HELPS trial): procedural safety and operator-assessed efficacy results. AJNR Am J Neuroradiol. 2008;29:217-223.
53 Pierot L, Spelle L, Vitry F, et al. Immediate clinical outcome of patients harboring unruptured intracranial aneurysms treated by endovascular approach: results of the ATENA study. Stroke. 2008;39:2497-2504.
54 Meyers PM, Schumacher HC, Higashida RT, et al. Reporting standards for endovascular repair of saccular intracranial cerebral aneurysms. Stroke. 2009;40(5):e366-e379.
55 Lee T, Baytion M, Sciacca R, et al. Aggregate analysis of the literature for unruptured intracranial aneurysm treatment. AJNR Am J Neuroradiol. 2005;26:1902-1906.
56 Higashida RT, Lahue BJ, Torbey MT, et al. Treatment of unruptured intracranial aneurysms: a nationwide assessment of effectiveness. AJNR Am J Neuroradiol. 2007;28:146-151.
57 Raaymakers T, Rinkel G, Limburg M, et al. Mortality and morbidity of surgery for unruptured intracranial aneurysms: a meta-analysis. Stroke. 1998;29:1531-1538.
58 Cloft HJ, Kaufmann T, Kallmes DF. Observer agreement in the assessment of endovascular aneurysm therapy and aneurysm recurrence. AJNR Am J Neuroradiol. 2007;28:497-500.
59 The CARAT Investigators. Rates of delayed rebleeding from intracranial aneurysms are low after surgical and endovascular treatment. Stroke. 2006;37:1437-1442.
60 Ries T, Siemonsen S, Thomalla G, et al. Long-term follow-up of cerebral aneurysms after endovascular therapy: prediction and outcome of retreatment. AJNR Am J Neuroradiol. 2007;28:1755-1761.
