Research-Human-Clinical Studies: Editor's Choice
A Multicenter Study of Stent-Assisted Coiling of Cerebral Aneurysms With a Y Configuration
Fargen, Kyle M. MD, MPH*; Mocco, J MD, MS‡; Neal, Dan MS*; Dewan, Michael C. MD‡; Reavey-Cantwell, John MD, MS§; Woo, Henry H. MD¶; Fiorella, David J. MD¶; Mokin, Maxim MD, PhD‖; Siddiqui, Adnan H. MD, PhD||; Turk, Aquilla S. DO#; Turner, Raymond D. MD#; Chaudry, Imran MD#; Kalani, M. Yashar S. MD, PhD**; Albuquerque, Felipe MD**; Hoh, Brian L. MD*
*Department of Neurosurgery, University of Florida, Gainesville, Florida;
‡Department of Neurosurgery, Vanderbilt University, Nashville, Tennessee;
§Department of Neurosurgery, Virginia Commonwealth University, Richmond, Virginia;
¶Departments of Neurosurgery and Radiology, Stony Brook University Medical Center, Stony Brook, New York;
‖Department of Neurosurgery, University at Buffalo, Buffalo, New York;
#Departments of Neurosurgery and Radiology, Medical University of South Carolina, Charleston, South Carolina;
**Department of Neurosurgery, Barrow Neurological Institute, Phoenix, Arizona
Correspondence: Kyle M. Fargen, MD, MPH, Box 100265, Gainesville, FL 32610. E-mail: firstname.lastname@example.org
Received December 13, 2012
Accepted May 30, 2013
BACKGROUND: Stent-assisted coiling with 2 stents in a Y configuration is a technique for coiling complex wide-neck bifurcation aneurysms.
OBJECTIVE: We sought to provide long-term clinical and angiographic outcomes with Y-stent coiling, which are not currently established.
METHODS: Seven centers provided deidentified, retrospective data on all consecutive patients who underwent stent-assisted coiling for an intracranial aneurysm with a Y-stent configuration.
RESULTS: Forty-five patients underwent treatment by Y-stent coiling. Their mean age was 57.9 years. Most aneurysms were basilar apex (87%), and 89% of aneurysms were unruptured. Mean size was 9.9 mm. Most aneurysms were treated with 1 open-cell and 1 closed-cell stent (51%), with 29% treated with open-open stents and 16% treated with 2 closed-cell stents. Initial aneurysm occlusion was excellent (84% in Raymond grade I or II). Procedural complications occurred in 11% of patients. Mean clinical follow-up was 7.8 months, and 93% of patients had a modified Rankin Scale score of 0 to 2 at last follow-up. Mean angiographic follow-up was 9.8 months, and 92% of patients had Raymond grade I or II occlusion on follow-up imaging. Of those patients with initial Raymond grade III occlusion and follow-up imaging, all but 1 patient progressed to a better occlusion grade (83%; P < .05). Three aneurysms required retreatment because of recanalization (10%). There was no difference in initial or follow-up angiographic occlusion, clinical outcomes, incidence of aneurysm retreatment, or in-stent stenosis among open-open, open-closed, or closed-closed stent groups.
CONCLUSION: In a large multicenter series of Y-stent coiling for bifurcation aneurysms, there were low complication rates and excellent clinical and angiographic outcomes.
ABBREVIATION: mRS, modified Rankin Scale
Stent-assisted coiling has become a safe and effective means of treating wide-necked or otherwise difficult-to-treat cerebral aneurysms.1,2 First described for cerebral aneurysms by Chow and colleagues3 in 2004, stent-assisted coiling with 2 stents in a Y configuration (Y stenting) has gained acceptance as an alternative technique to help maintain branching artery patency while treating bifurcation aneurysms. Initial Y-stent case series described the use of crossing open-cell stents (the Neuroform stent; Stryker, Kalamazoo, Michigan); however, recent series have also described the use of closed-cell stents (Enterprise Vascular Reconstruction Device and Delivery System; Codman Neurovascular, Ratham, Massachusetts) or the Solitaire AB device (ev3, Plymouth, Minnesota). Although reports of Y stenting thus far have demonstrated low morbidity and mortality,3-18 the studies have mostly been single-center series. We believe that Y-stent coiling is safe and effective with open-open, open-closed, or closed-closed stent combinations. We report a multicenter series of Y-stent--assisted coiling to improve our understanding of the risks and results after Y stenting with both closed-cell and open-cell stent designs.
PATIENTS AND METHODS
Seven centers (Vanderbilt University, Virginia Commonwealth University, Barrow Neurological Institute, Stony Brook University Medical Center, University at Buffalo, Medical University of South Carolina, and University of Florida) provided retrospective, deidentified data on all consecutive patients with intracranial aneurysm who underwent stent-assisted coiling for an intracranial aneurysm with a Y- or X-stent configuration. All centers obtained institutional review board approval before data submission to the primary center. Postprocedural aspirin-clopidogrel therapy was prescribed according to individual institutional standards of practice. Procedural techniques, clinical follow-up, and timing of angiographic follow-up were not standardized and were based on individual treatment centers.
Each center reported for each patient clinical, procedural, and angiographic data, including aneurysm size and location, stents used, initial and last follow-up angiographic occlusion data (assessed by Raymond grade determined by the neurointerventionist at each center), and clinical follow-up data. In-stent stenosis, retreatments, and all complications were collected and reported. Clinical outcome was defined by modified Rankin Scale (mRS) score at the last follow-up visit as assessed and reported by the treatment center. Statistical analyses (χ2 test, Wilcoxon signed-rank test, logistic regression analyses) were performed with SPSS (IBM, Armonk, New York). Missing data points were excluded from the analysis. A value of P = .05 was chosen to determine statistical significance.
Forty-five patients underwent treatment by Y stenting for 45 cerebral aneurysms at the 7 centers. Demographic and clinical data for patients are given in Table 1. Mean age was 57.9 years (range, 31-81 years; SEM, 1.7 years). Sixty-nine percent of patients were female. Five of the 45 patients (11%) underwent Y stenting for treatment of a ruptured aneurysm; the majority of aneurysms (89%) were unruptured. The majority of aneurysms were located on the basilar apex (87%), with anterior communicating (7%), middle cerebral artery bifurcation (4%), and pericallosal (2%) aneurysms accounting for the remainder. On average, the mean measured aneurysm diameter was 9.9 mm (range, 2-23 mm; SEM, 0.1 mm) with a mean neck size of 6.9 mm (range, 2.5-17 mm; SEM, 0.5 mm). The average dome-to-neck ratio was 1.5 (range, 0.7-4.5; SEM, 0.1).
Most aneurysms were treated with 1 open-cell and 1 closed-cell stent (51%), with 29% treated with open-open stents and 16% treated with 2 closed-cell stents. Of the 42 patients (93%) in whom initial aneurysm occlusion was reported, most patients had either complete occlusion (Raymond grade I, 43%) or a residual neck or dog ear (Raymond grade II, 41%). Procedural complications were low, with 11.1% (5 patients; 2 intraoperative ruptures, 3 technical complications related to stent deployment) having intraoperative complications and 11.1% (5 patients; 3 cranial nerve palsies, 1 basilar transient ischemic attack, and 1 retroperitoneal hematoma) having periprocedural (within 2 weeks) complications. The 3 technical complications related to stent deployment included 1 stent that herniated into the aneurysm, 1 stent migration with the end landing in the aneurysm dome, and 1 event not specified. mRS score at discharge was 0 to 2 in 96% of patients, and most patients were discharged to home (86%) or inpatient rehabilitation (9%). Two patients died during the follow-up period (4.4%), the first secondary to sequelae associated with preoperative aneurysmal subarachnoid hemorrhage and the second as a result of an unrelated event after being discharged with an mRS score of 0.
Clinical follow-up was available in 40 patients (89%), with a mean follow-up of 7.8 months (range, 0-60 months; SEM, 1.8 months). Of those with clinical follow-up after time of discharge, 93% of patients had an mRS score of 0 to 2. Angiographic follow-up was available in 30 patients (64%; mean, 9.8 months; range, 0-60 months; SEM, 2.1 months), with most patients having undergone digital subtraction catheter angiography (70%) or magnetic resonance angiography (27%). Of the 30 patients (67%) with follow-up angiographic occlusion data, the majority of patients had complete occlusion (Raymond grade I, 60%) or residual neck or dog ear (Raymond grade II, 33%). Of the 6 patients with initial Raymond grade III occlusion and follow-up imaging, 5 demonstrated improvement to a better occlusion grade (83%; P = .04).
Three of the 30 aneurysms with angiographic follow-up required retreatment because of recanalization (10%), and 1 aneurysm had recanalization that was monitored conservatively (3.3%). In-stent stenosis of <50% was seen in 5 of the 30 patients with angiographic follow-up (17%), but none of these patients required treatment for the stenosis.
A comparison of open-open, open-closed, and closed-closed stent combinations is given in Table 2. There was no difference in initial or follow-up angiographic occlusion among stent types used (P = .33 and .64, respectively). Because of the low number and nonspecific nature of many of the complications (eg, retroperitoneal hematoma), an analysis of complications and stents used was not performed. In multivariate logistic regression analyses, no difference was seen in the incidence of aneurysm retreatment (P = .99) or in-stent stenosis (P = .80) among stent groups when controlling for age, sex, aneurysm size, smoking status, aneurysm location, and rupture status. Furthermore, there was no difference in clinical outcomes between stent groups (P = .77).
This retrospective study of 45 patients treated with Y-stent--assisted coiling of bifurcation aneurysms at 7 different treatment centers demonstrates excellent aneurysm occlusion results with satisfactory durability, a low rate of complications, and low retreatment rate. These data are particularly encouraging given that many of these aneurysms were wide-necked bifurcation aneurysms, incorporating important branching arteries, and may represent a higher-risk subset of aneurysms than those traditionally treated with stent coiling or primary coiling. In addition, most of the aneurysms treated were basilar apex aneurysms, a location associated with not insignificant risks of surgical morbidity and mortality.19,20 Interestingly, although the number of patients treated with each stent combination was low, there was no apparent difference in radiographic or clinical outcome between those treated with open-open, open-closed, or closed-closed stent designs.
Recent studies of stent-assisted coiling have demonstrated satisfactory safety and efficacy with excellent long-term results.1,2 Stent-assisted coiling has the added benefit of vessel reconstruction, preserving patency of the parent artery while serving as a buttress to prevent coil prolapse and allowing increased packing density.21 Furthermore, there are data to suggest that stent-assisted coiling may promote progressive aneurysm occlusion compared with coiling alone by enhancing endothelialization or through an as-yet undefined flow remodeling process.2,22,23 Additionally, recent reports have suggested that excellent aneurysm occlusion rates may be obtained after stent-assisted coiling with only modest packing densities (12%-22%).24 In the data from this series, a similar trend was seen, with one-third of aneurysms progressing to greater occlusion over the follow-up period, although this trend did not reach statistical significance. Among those with residual dome filling at the conclusion of the initial coiling procedure (Raymond grade III), there was an improvement in occlusion to a better grade in 5 of the 6 patients. Although the number of patients in this group was small, these results appear to coincide with previous reports of incompletely stent-coiled aneurysms progressing to occlusion over time.2,22,23
The Y-stenting technique, in contrast to stent-assisted coiling with a single stent, involves the crossing of a second stent from the parent artery into a branch artery through the interstices of a stent already traveling from the parent vessel into a second branching artery. This strategy allows adequate vascular reconstruction of a bifurcating parent vessel and may prevent coil prolapse and subsequent occlusion of branching vessels. An additional derivation, the “kissing” configuration wherein the stents do not overlap has also been reported with relative success.4,7 Y stenting has been shown to reduce cross-neck flow in computational fluid dynamic simulations of a wide-necked basilar aneurysm more so than half-Y or cross-bar stenting,25 as well as reducing shear stresses inside the aneurysm sac by > 40%.26 For example, the use of Y stenting without adjunctive coiling with 2 closed-cell stents as a means of promoting progressive aneurysm occlusion through flow-diversion has been reported in 8 patients.9
Y-stent coiling was initially described with open-cell stents only because of concerns about the closed-cell stent design limiting the expansion of the second stent at the crossing point. However, recent series, including data presented here, have demonstrated that dual closed-cell stents can be used with results comparable to those with open-open or mixed combinations. A review of the reported literature shows that different stent combinations have yielded low complication rates and excellent aneurysm occlusion (Table 3). Although the number of patients treated with each stent combination in this study was too low to make definitive conclusions on safety and efficacy, there appear to be no significant differences between the stent combination used and angiographic occlusion or patient morbidity.
TABLE 3-a Published ...Image Tools
There are important technical considerations when coiling bifurcation aneurysms with a Y-stent configuration. Y-stent coiling may be performed by first “jailing” the coiling microcatheter within the aneurysm, followed by deploying the stent to protect the branching parent arteries, and then deploying coils via the jailed catheter. Alternatively, coiling may be performed by traversing the stent interstices with the microcatheter after stents have been deployed (coil-through technique) or by coiling the aneurysm first and then deploying stents afterward (coil-stent technique). These techniques have been reviewed in detail recently by Spiotta and colleagues.27 Furthermore, it should be mentioned that nonstent coiling of bifurcation cerebral aneurysms can be performed as an alternative to Y-stent coiling such as with single-balloon or kissing-balloon techniques, which obviate the need for antiplatelet agents. These techniques are limited by the necessary flow arrest that occurs after balloon inflation and the opportunity for coil prolapse or herniation once the balloon is deflated. This study was not designed to compare different stent-coiling strategies based on open- or closed-cell stent designs. Finally, in the era of flow diversion technology, the risk of thrombotic occlusion of the branching artery of a bifurcation when it is jailed by a flow-diverting stent is not yet clear.
A final point worth noting is the low occurrence of thromboembolic complications in this series. Prior series of stent-assisted coiling have indicated thromboembolic rates approximating 4% to 8%.1,2 In the series of 19 Y-stent--assisted coiling cases by Spiotta and colleagues,17 3 intraprocedural (16%) and 2 delayed (11%) thromboembolic occurred. Additionally, Chalouhi and colleagues10 reported equivalent thromboembolic event rates (6%) in both single-stent--assisted and Y-stent--assisted coiling procedures (16 cases) in their series. In our series, all patients were on dual antiplatelet therapy for at least 2 to 6 months after the procedure, depending on individual institutional practices. The benefits of dual antiplatelet therapy in preventing thromboembolic complications during percutaneous coronary intervention are well documented in the cardiology literature.28-30 Dual antiplatelet therapy has recently been suggested to be an important factor in preventing thromboembolic events during neurointerventional procedures,31,32 with series suggesting that platelet function assays may be helpful in identifying patients who are poor clopidogrel responders.31,33 These tests may be particularly relevant during cerebral stenting procedures given that as high as 42% of patients may be clopidogrel nonresponders.31
Wide-necked bifurcation aneurysms represent a difficult subset of aneurysms to treat. By definition, these aneurysms occur at the junction of 2 essential branching arteries that must remain patent after embolization. Oftentimes, particularly for basilar apex aneurysms, there are a number of small perforating vessels originating from the parent vessels that similarly must be preserved. Surgical clipping of basilar apex aneurysms is associated with risks of morbidity and mortality, particularly as a result of inadvertent clipping of brainstem or diencephalic perforators that are inadequately visualized during surgery. Unassisted coiling techniques are frequently dangerous in wide-necked bifurcation aneurysms because of the tendency for coil prolapse into the bifurcating vessels. Balloon-assisted coiling is a potential treatment option, but prolapse or shifting of coils may occur once the balloon is deflated. Placement of a single stent into one of the branches for stent-assisted coiling remains an additional option, although this technique may not adequately protect the patency of the second branching vessel. Flow-diversion stenting is not ideal because this would jail one of the limbs of the bifurcation. Y-stent coiling appears to be the best treatment option for these difficult aneurysms and, from this series and our review of the literature, appears to be an effective technique with a low complication rate.
There are several important limitations to this study. These include its retrospective nature and the absence of an independent core laboratory for imaging review or for the detection of complications or determination of clinical outcome status. Furthermore, the limited number of patients in each stent group with angiographic and clinical follow-up data makes interpretation of the data difficult. Finally, data are dependent on the reporting of events, occlusion, and outcomes by individual centers, which may be subject to bias.
The results of this study are pertinent and generalizable to most centers performing endovascular aneurysm treatment because the devices used, underlying patient characteristics, and treatments expressed here are likely to be similar across most centers.
This retrospective, multicenter series of 45 patients having undergone Y-stent coiling for bifurcation aneurysms demonstrates that intraprocedural and periprocedural complications were low with a low incidence of retreatment and in-stent stenosis. Good outcome (mRS score, 0-2) was obtained in 93% of patients at the last follow-up. There were no significant differences in angiographic occlusion, retreatment, or patient outcomes based on the type of stents used.
Dr Mocco is a consultant for Lazarus Effect and Nfocus and has financial interests in Blockade Medical. Dr Siddiqui has received research grants from the National Institutes of Health, Hemodynamic, and the University of Buffalo; has financial interests in Hotspur, Intratech Medical, StimSox and Valor Medical; is a consultant to Codman & Shurtleff, Inc, Concentric Medical, ev3/Covidien Vascular Therapies, GuidePoint Global Consulting, Penumbra and Stryker; is on the National Steering Committee for Penumbra 3D Separator Trial, speakers’ bureaus for Codman & Shurtleff, Inc and Genentech; and advisory board of Codman & Shurtleff; and has received honoraria from Abbott Vascular, American Association of Neurological Surgeons’ courses, and Genentech. Dr Turner is a consultant for Covidien, Microvention, Codman Neurovascular, Stryker, Penumbra, and Blockade Medical and has received grant support from Covidien, Codman Neurovascular, and Microvention. The other authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.
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The authors report the results of a multicenter retrospective series of 45 patients from 7 high-volume centers in the United States. All aneurysms were treated with a Y-configuration construct; the majority of aneurysms were located at the basilar apex. Half of the patients were treated with a combination of an open and closed cell stent, 29% with 2 open-cell stents, and 16% with 2 closed-cell stents. On follow-up angiography, > 90% of patients had a Raymond I or II score. Interestingly, patients with initial suboptimal result (Raymond III) showed significant improvement (P = .04) in the aneurysm occlusion at follow-up. No difference in the degree of aneurysm occlusion was found between different stent combinations, but the number of patients in each stent group was limited. At our institution, we prefer the use of 2 closed-cell design stents because this combination may provide superior flow-diversion effects.1,2 Further investigation is needed. Balloon-assisted coiling is also a good alternative for wide-necked aneurysms, although in our experience stent-assisted coiling yields lower rates of retreatment and higher rates of aneurysm obliteration and progression of occlusion at follow-up with a similar morbidity rate.3,4 Another alternative for wide-necked basilar apex aneurysms is the deployment of a horizontal stent from 1 posterior cerebral artery to the other posterior cerebral artery through the posterior communication artery (transcirculation approach). This procedure is technically demanding, however, and does not offer the same flow-remodeling effects as the Y-construct configuration.5 Finally, the authors should be commended for conducting a multicenter study that sheds light on important issues in endovascular neurosurgery for which numbers are low in individual centers. This should encourage others to follow.
L. Fernando Gonzalez
1. Cekirge HS, Yavuz K, Geyik S, Saatci I. A novel “Y” stent flow diversion technique for the endovascular treatment of bifurcation aneurysms without endosaccular coiling. AJNR Am J Neuroradiol. 2011;32(7):1262–1268. PubMed | CrossRef Cited Here... |
2. 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. View Full Text | PubMed | CrossRef Cited Here... |
3. Chalouhi N, Starke RM, Koltz MT, et al.. Stent-assisted coiling versus balloon remodeling of wide-neck aneurysms: comparison of angiographic outcomes [published online ahead of print May 2, 2013]. AJNR Am J Neuroradiol. Cited Here...
4. 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. View Full Text | PubMed | CrossRef Cited Here... |
5. Babiker MH, Gonzalez LF, Ryan J, et al.. Influence of stent configuration on cerebral aneurysm fluid dynamics. J Biomech. 2012;45(3):440–447. PubMed | CrossRef Cited Here... |
The endovascular contribution to management of basilar apex aneurysms has been one of improved access with a resulting decrease in morbidity. As with most pathology at the basilar apex, there is always a caveat. Although surgeons should be wary of basilar aneurysms with a posterior projection and elevated height above the posterior clinoid process, the endovascular practitioner should be wary of the wide-necked basilar lesion.
Although multiple possibilities exist to address this endovascular problem, the authors present an experience using Y stenting to treat wide-necked basilar apex aneurysms. By involving 7 different centers, the authors could evaluate 45 such cases with respect to morbidity and radiographic obliteration at follow-up. The procedural morbidity of 11.1% belies the complexity of the procedure and this pathology. Various stenting combinations yielded similar rates of obliteration. The presence of a stent construct at the aneurysm neck seemed to contribute to improving obliteration rates at the time of follow-up imaging.
The takeaway from this article is that Y stenting is within the standard of care for this level of pathology and may be applied using various combinations of current stent technologies. I would also suggest that the reported cumulative morbidity should make the reader wonder at what point a surgical solution should be considered. I would like to express my appreciation to the authors for their thoughtful contribution to the literature.
Babu G. Welch
Cerebral aneurysm; Coiling; Endovascular; Stent; Y stent
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