RESEARCH—HUMAN—CLINICAL STUDIES RESEARCH—HUMAN—CLINICAL STUDIES
Comparison of Stent-Assisted Coiling vs Coiling Alone in 563 Intracranial Aneurysms: Safety and Efficacy at a High-Volume Center Hongchao Yang, MD Yong Sun, MD Yuhua Jiang, MD Xianli Lv, MD Yang Zhao, MM Youxiang Li, MD, PhD Aihua Liu, MD Department of Interventional Neuroradiology, Beijing Neurosurgical Institute, Beijing Tiantan Hospital, Capital Medical University, Beijing, China Correspondence: Youxiang Li, MD, PhD, Department of Interventional Neuroradiology, Beijing Neurosurgical Institute, No. 6 Tiantan West Road, Dongcheng District, Beijing, China. E-mail: [email protected] Received, November 21, 2014. Accepted, February 25, 2015. Published Online, April 7, 2015. Copyright © 2015 by the Congress of Neurological Surgeons.
BACKGROUND: Stent-assisted coiling has been used in both unruptured and ruptured aneurysms, but the safety and efficacy still remain controversial. OBJECTIVE: To compare the safety and efficacy of stent-assisted coiling with coiling alone for intracranial aneurysms. METHODS: We retrospectively reviewed 512 patients treated by endovascular coiling or stent-assisted coiling over a 1-year period. The patients’ clinical and imaging information was recorded. Procedure-related complication rates, recurrence rates, and clinical outcomes were analyzed in both the total aneurysms and the subgroups of ruptured and unruptured aneurysms. RESULTS: A total of 243 patients were treated by coiling alone and 269 patients were treated by stent-assisted coiling. Procedure-related complications occurred in 6.2% of patients in the coiling-alone group compared with 6.3% in the stent-assisted coiling group. The procedural permanent morbidity and mortality rates were 1.6% (4/243) and 1.2% (3/243), respectively, in the coiling-alone group and 1.1% (3/269) and 1.5% (4/269), respectively, in the stent-assisted coiling group. A significantly lower recurrence rate was found in the stent-assisted coiling group compared with the coilingalone group (5.2% vs 16.5%, P = .002). In a comparison of subgroups of ruptured and unruptured aneurysms, the procedural complications rates were comparable in the 2 groups, with a lower recurrence rate in the stent-assisted coiling group. Multivariate analysis showed that larger aneurysm size and higher Hunt and Hess grade were predictors of procedural morbidity; larger aneurysm size, ruptured aneurysm, anterior circulation aneurysms, initial incomplete occlusion, and lack of stent assistance were predictors of recurrence. CONCLUSION: Compared with coiling alone, stent-assisted coiling may achieve lower recurrence rates, with comparable procedure-related complications and clinical outcomes in both ruptured and unruptured aneurysms. KEY WORDS: Cerebral aneurysm, Coil, Endovascular, Stent Neurosurgery 77:241–247, 2015
DOI: 10.1227/NEU.0000000000000765
E
ndovascular treatment has become an important technique for intracranial aneurysms. To increase packing density, improve neck coverage, and prevent coil protrusion, stents were invented and used to treat wide-necked and morphologically complex aneurysms. Additionally, stents have flow-diverting properties and provide a scaffold for endothelialization, which
ABBREVIATIONS: HH, Hunt and Hess; mRS, modified Rankin Scale
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may facilitate aneurysm thrombosis and eventual obliteration.1-3 Several studies have shown that stent-assisted coiling achieved favorable outcomes and decreased recanalization rates.4-7 However, literature review also showed that stent-assisted coiling had higher morbidity and mortality rates compared with coiling alone, especially in ruptured aneurysms.8-10 This study aimed to compare the safety and efficacy of treating ruptured and unruptured intracranial aneurysms by coiling alone and stent-assisted coiling.
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METHODS We retrospectively collected patients with intracranial aneurysms treated by endovascular embolization between February 2013 and February 2014 in our institution. Informed consent from all patients was obtained, and the protocol of this study was approved by our institution. The baseline data on age, sex, medical history, aneurysm size and location, subarachnoid hemorrhage, and Hunt and Hess (HH) grade were recorded. All ruptured aneurysms were confirmed by computed tomography (CT) scan. The procedure-related complications and immediate and follow-up angiographic results were reviewed. Embolization was complete when there was no contrast filling of the dome, body, or neck of the aneurysm. A neck remnant (or nearly complete occlusion) was defined by a residual neck (,2 mm) and incomplete embolization by a residual part of aneurysmal sac. An aneurysm that displayed a decreasing percentage of occlusion on follow-up angiography was considered a recurrence, eg, the occlusion grade decreasing from complete occlusion to a neck remnant or from a neck remnant to a residual aneurysm. We decided to use a stent if the aneurysm was wide necked (.4 mm or dome/neck ,2 mm) or morphologically complex and coiling alone could not obtain a satisfactory treatment result. However, in the setting of acute subarachnoid hemorrhage, coiling alone was preferred. A total of 512 patients with 563 aneurysms were treated with endovascular embolization. General anesthesia and systemic heparinization were used in all patients, and the activated clotting time was maintained at between 250 and 300 seconds during the procedure. For patients treated with stent-assisted coiling, dual-antiplatelet therapy (100 mg/d aspirin and 75 mg/d clopidogrel) was administered for unruptured aneurysms at least 3 to 5 days before the procedure, and a loading dose of 300 mg aspirin and 300 mg clopidogrel was given for ruptured aneurysms at least 2 hours before the procedure. After the procedure, patients were given clopidogrel (75 mg/d) for 4 to 6 weeks and aspirin (100 mg/d) for 6 months. The Enterprise stent (Cordis Neurovascular, Miami, Florida) and the Solitaire stent (Solitaire AB neurovascular remodeling device; eV3 Inc, Irvine, California) were used to treat wide-necked or complex aneurysms.
Statistical Analysis Normally distributed continuous data are presented as mean 6 SD and categorical data as frequency and percentage. Analysis was carried out with an independent-samples t test and the x2 and Fisher exact tests. Univariate logistic regression was used to analyze potential factors, and a covariate with a univariate P value of ,.05 was included in multivariate logistic regression to identify predictors of procedural complications and aneurysm recanalization. No adjustment for multiple comparisons was performed. The odds ratio, 95% confidence interval, and P value were determined for factors of the univariate and multivariate models. Statistical significance was defined as P , .05 and an odds ratio with 95% confidence interval not including 1.0. Statistical analysis was carried out with SPSS version 17.0 (SPSS Inc, Chicago, Illinois).
with stent-assisted coiling (Figure). Patient and aneurysm baseline characteristics are summarized in Table 1. There were no statistically significant differences in patient age, sex, medical history, or aneurysm location in the 2 groups. However, there was significantly higher rate of ruptured aneurysms in the coiling-alone group. Additionally, the aneurysm size was significantly larger in the stent-assisted coiling group. Descriptive Data and Main Results Complications and Outcomes Procedure-related complications occurred in 15 patients (6.2%, 15/243) in the coiling-alone group compared with 17 patients (6.3%, 17/269) in the stent-assisted coiling group. Thromboembolic complications occurred in 10 patients (4.1%, 10/243) in the coiling-alone group, and 13 patients (4.8%, 13/269) in the stentassisted coiling group, which caused permanent neurological deficit in 0.8% patients (2/243) in the coiling-alone group and 1.1% patients (3/269) in the stent-assisted coiling group, respectively. Additionally, 1 patient in the stent-assisted coiling group died of brainstem acute ischemic stroke. In the coiling-alone group, intraoperative rupture occurred 1 patient (modified Rankin Scale [mRS] score of 3 at discharge), and cerebral hemorrhage occurred in 4 patients after initial treatment (1 patient with an mRS score of 3, 3 patients died). In the stent-assisted coiling group, 3 patients died of rebleeding. Therefore, the procedure-related permanent morbidity and mortality rates were 1.6% (4/243) and 1.2% (3/243), respectively, in the coiling-alone group vs 1.1% (3/269) and 1.5% (4/269), respectively, in the stent-assisted coiling group. Clinical follow-up (range, 6-18 months; mean, 11.2 months) was available for 88.5% (215/243) of patients in the coiling-alone group vs 92.2% (248/269) of patients in the stent-assisted coiling group. According to final follow-up results, 181 patients (84.2%, 181/215) had favorable clinical outcomes (mRS scores of 0-2) in the coiling-alone group compared with 219 patients (88.3%, 219/ 248) in the stent-assisted coiling group (P = .19). Angiographic Results Initial complete occlusion was achieved in 64.2% (156/243) of patients in the coiling-alone group and in 53.9% (145/269) of
RESULTS Participants Baseline Characteristics Of the 512 patients, 243 with 266 aneurysms were treated with coiling alone and 269 with 297 aneurysms were treated
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FIGURE. Distribution of endovascular treatment of the 563 aneurysms in this study.
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STENT-ASSISTED COILING VS COILING ALONE
TABLE 1. Baseline Characteristics of Patientsa Coiling Alone Age, y, mean 6 SD Female Medical history Hypertension Diabetes Brain ischemia Coronary heart disease Ruptured aneurysmsb HH gradec 1-2 3-4 Aneurysm locationb Anterior circulation Posterior circulation Dome-to-neck ratiob Mean aneurysm diameter,b mm, mean 6 SD #5 5-15 .15
TABLE 2. Comparison of Coiling Alone and Stent-Assisted Coiling in Patients With Unruptured Aneurysmsa
Stent-Assisted P Coiling Value
54.3 6 12.9 151 (62.1)
54.4 6 11.1 173 (64.3)
.87 .85
87 (35.8) 23 (9.4) 25 (10.3) 14 (5.8) 115 (47.3)
115 (42.8) 28 (10.4) 22 (8.2) 17 (6.3) 58 (21.6)
.11 .72 .41 .79 ,.001 .001
35 (30.4) 80 (68.6)
33 (56.9) 25 (43.1)
198 (74.4) 68 (25.6) 2.5 6.7 6 3.6
232 (78.1) 65 (21.9) 1.6 8.8 6 7.1
107 (40.2) 150 (56.4) 9 (3.4)
102 (34.3) 154 (51.9) 41 (13.8)
Coiling Alone Age Female Mean aneurysm diameter,b mm, mean 6 SD Thromboembolic events Hemorrhagic complications Procedure-related mortality Initial complete occlusion Recanalization mRS score at follow-up 0-2
.31
Stent-Assisted P Coiling Value
53.1 6 13.5 53.9 6 11.6 87/128 (68.0) 136/211 (65.9) 7.4 6 4.2 8.7 6 7.2
.54 .51 .22
3/128 (2.3) 8/211 (3.8) 2/128 (1.6) 0 1/128 (0.8) 1/211 (0.5) 82/128 (64.1) 115/211 (54.5) 10/66 (15.2) 5/100 (5.0)
.54c .14c 1.0c .08 .03 .46
97/113 (85.8) 173/195 (88.7)
a
.08 .03 .001
SD, standard deviation; mRS, modified Rankin Scale. Data in parentheses are percentages. b Data are number of aneurysms (140 in coiling-alone group and 233 in stenting group) or number of patients (128 in coiling-alone group and 211 in stenting group). c Fisher exact test.
a
SD, standard deviation; HH, Hunt and Hess. Data in parentheses are percentages. There were 243 patients with 266 aneurysms treated by coiling alone compared with 269 patients with 297 aneurysms treated by stent-assisted coiling. b Data are number of aneurysms. c Data are number of patients with ruptured aneurysms (115 in coiling-alone group and 58 in stenting group) or number of patients.
patients in the stent-assisted coiling group (P = .02). Angiographic follow-up (range, 6-12 months; mean, 7.8 months) was performed by digital subtraction angiography or magnetic resonance angiography and available for 57.2% (139/243) of patients in the coiling-alone group and 56.9% (153/269) of patients in the stent-assisted coiling group. In the coiling-alone group, 21 of 139 (15.1%) patients showed progressive thrombosis occlusion during the follow-up period compared with 50 of 153 (32.7%) patients in the stent-assisted coiling group (P = .001). The recurrence rate was 16.5% (23/ 139) for the coiling-alone group and 5.2% (8/153) for the stentassisted coiling group (P = .002), including 16 patients (69.6%, 16/23) in the coiling-alone group and 2 patients (25.0%, 2/8) in the stent-assisted coiling group, who required retreatment because of growth shown on angiography and mass-effect symptoms (P = .04). Coiling Alone vs Stent-Assisted Coiling in Unruptured Aneurysms There were 128 patients with unruptured aneurysms in the coiling-alone group compared with 211 patients in the stentassisted coiling group. A comparison of the results in these 2 groups is summarized in Table 2; baseline characteristics showed no significant differences in these 2 groups.
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Although the rate of thromboembolic complications was higher in the stent-assisted coiling group (3.8%) than in the coiling-alone group (2.3%), this difference was not statistically significant (P = .54). Immediate complete occlusion was achieved in 64.1% of the coiling-alone group and 54.5% of the stent-assisted coiling group, which showed no statistically significant differences (P = .08). The recurrence rate was significantly higher in the coiling-alone group than in the stent-assisted coiling group (15.2% vs 5.0%, P = .03). Two cerebral hemorrhages occurred in the coiling-alone group (1 had an mRS score of 3 at discharge and 1 died 3 days after the initial treatment), but none were in the stent-assisted coiling group. As previously mentioned, 1 patient died of brainstem acute ischemia in the stent-assisted coiling group. There were 97 patients (85.8%, 97/113) with favorable outcomes in the coilingalone group and 173 patients (88.7%, 173/195) in the stentassisted coiling group (P = .46). Coiling Alone vs Stent-Assisted Coiling in Ruptured Aneurysms A total of 115 patients with ruptured aneurysms were treated by coiling alone and 58 patients by stent-assisted coiling. A comparison of the results in these 2 groups is shown in Table 3. Baseline characteristics were comparable except for the aneurysm size and initial HH grades, which showed larger aneurysm size in the stent-assisted coiling group than the coiling-alone group (5.5 6 2.0 mm vs 8.4 6 6.8 mm, respectively, P = .02) and a higher HH grade (grades 3-4) in the coiling-alone group (P = .001). The thromboembolic complication rate was 6.1% in the coiling-alone
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TABLE 3. Comparison of Coiling Alone and Stent-Assisted Coiling in Patients With Ruptured Aneurysmsa
Age Female Mean aneurysm diameter,b mm, mean 6 SD HH grade 3-4 Thromboembolic events Hemorrhagic complication Procedure-related mortality Initial complete occlusion Recanalization mRS score at last follow-up 0-2
Coiling Alone
Stent-Assisted Coiling
P Value
55.7 6 12.3 64/115 (55.7) 5.5 6 2.0
56.4 6 8.7 37/58 (63.8) 8.4 6 6.8
.71 .31 .02
80/115 (69.6) 7/115 (6.1)
25/58 (43.1) 5/58 (8.6)
.001 .54c
3/115 (2.6)
3/58 (5.2)
.41
c
c
2/115 (1.7)
3/58 (5.2)
.34
74/115 (64.3)
30/58 (51.7)
.11
13/73 (17.8)
3/53 (5.7)
.04 .48
84/102 (82.4)
46/102 (86.8)
a
SD, standard deviation; HH, Hunt and Hess; mRS, modified Rankin Scale. Data in parentheses are percentages. b Data are number of aneurysms (126 in coiling-alone group and 64 in stentassisted coiling group) or number of patients (115 in coiling-alone group and 58 in stent-assisted coiling group). c Fisher exact test.
group and 8.6% in the stent-assisted coiling group, but with no statistically significant difference (P = .54). The hemorrhagic complication rate was 2.6% in the coiling-alone group compared with 5.2% in the stent-assisted coiling group (P = .33). Immediate complete occlusion was achieved in 64.3% of the coiling-alone group and 51.7% of the stent-assisted coiling group, which showed no statistically significant difference (P = .11). The recurrence rate was significantly higher in the coiling-alone group than in the stent-assisted coiling group (17.8% vs 5.7%, respectively, P = .043). There were 82.4% patients (84/102) with favorable outcomes in the coiling-alone group (mRS scores of 0-2) and 86.8% (46/53) in the stent-assisted coiling group (P = .48). Predictors of Morbidity and Recurrence On univariate analysis, the following variables were tested as predictors of procedural morbidity: age (P = .52), sex (P = .46), aneurysm size (P = .002), anterior circulation aneurysm (P = .01), ruptured aneurysms (P = .02), HH grades (P = .001), type of endovascular technique (P = .22), type of stent (P = .68), and initial occlusion results (P = .47). Therefore, based on the univariate results, larger aneurysm size, anterior circulation aneurysm, ruptured aneurysm, and higher HH grade were associated with higher procedural morbidity. However, only larger aneurysm size (P = .01) and higher HH grade (P = .01) were predictors of procedural morbidity on multivariate analysis (Table 4).
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Regarding predictors of recurrence, the following factors were tested on univariate analysis: age (P = .44), sex (P = .93), aneurysm size (P , .001), anterior circulation aneurysm (P , .001), ruptured aneurysms (P , .001), HH grades (P = .16), stent treatment (P , .001), type of stent (P = .16), initial occlusion grade (P = .001), and follow-up time (P = .12). On multivariate analysis, larger aneurysm size, ruptured aneurysms, anterior circulation aneurysms, initial incomplete occlusion, and lack of stent assistance were associated with higher recurrence rates (Table 5).
DISCUSSION Key Results Endovascular coil embolization has been widely used to treat intracranial aneurysms.11-13 However, 1 major limitation of coil embolization is the relatively high recurrence rate, especially of wide-necked and complex aneurysms. Raymond et al14 reported a 33.6% recurrence rate of 501 aneurysms treated by coiling during a mean follow-up time of 12.3 6 11.33 months. Previous studies have reported aneurysm recurrence after coil embolization is associated with incomplete occlusion grade.15,16 Stents can serve as a scaffold for endothelialization and have an effect of flow diversion, which may induce changes in intra-aneurysmal hemodynamics and promote delayed thrombosis and obtain more complete occlusion in the long term.17,18 Several studies of stent-assisted coiling for aneurysms have shown that progressive thrombosis caused a more complete occlusion and decreased recurrence rate.19,20 Although the initial incomplete occlusion rate was higher in the stent-assisted coiling group in our study, the rates of recurrence and retreatment were significantly higher in the coiling-alone group than that in the stent-assisted coiling group, which might be associated with the significantly progressive thrombosis in the stent-assisted coiling group. In our study, procedure-related complications were comparable in the stent-assisted coiling group and the coiling-alone group, which were similar to the findings of Hong et al21 meta-analysis study. Thromboembolic events were the major complication, and the rate of this complication was comparable in the 2 groups. Previous studies showed a higher rate of thromboembolic complications in patients treated by stent-assisted coiling, which might be associated with thrombogenicity of stents.1,22,23 Dualantiplatelet therapy played an important role to prevent thromboembolic complications in our patients treated by stent-assisted coiling. Piotin et al19 reported a significantly higher permanent complication rate in the stent-assisted coiling group than that in the coiling-alone group, but dual-antiplatelet therapy was not used in the group of patients treated by stenting. Lee et al24 reported that 42.9% of their patients had a poor response to clopidogrel, and all thromboembolic events occurred in the poor-response group, which implied that a poor response to antiplatelet medication might induce thromboembolic complications. Platelet function test has been used to ascertain the effects of antiplatelet medication. The risk of thromboembolic
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STENT-ASSISTED COILING VS COILING ALONE
TABLE 4. Predictors of Procedural Morbidity Univariate Analysis Factors Age Sex Aneurysm size Anterior circulation aneurysm Ruptured aneurysm Hunt and Hess grade Type of treatment technique Type of stent Initial occlusion grade
Multivariate Analysis
Odds Ratio
95% Confidence Interval
P Value
Odds Ratio
95% Confidence Interval
P Value
1.008 0.893 0.716 0.598 2.183 0.568 1.086 0.958 0.725
0.985-1.031 0.428-1.394 0.572-0.964 0.332-0.879 1.102-3.562 0.273-0.914 0.835-1.412 0.626-1.323 0.458-1.020
.52 .46 .002 .005 .02 .001 .22 .68 .47
— — 0.671 — — 0.411 — — —
— — 0.498-0.904 — — 0.205-0.826 — — —
— — .01 — — .01 — — —
complications might be decreased by adjusting the protocol of antiplatelet therapy based on the results of the platelet function test.25 Previous studies demonstrated a higher risk of procedurerelated hemorrhagic complications in patients undergoing stentassisted coiling, especially in patients with acute subarachnoid hemorrhage.26,27 However, the rate of procedural hemorrhagic complications in our study was comparable in the coiling-alone group and the stent-assisted coiling group (2.1% vs 1.1%). Only 1 case of intraprocedural aneurysm rupture occurred in our series, which caused a permanent neurological deficit (mRS score of 3). In unruptured aneurysms, the baseline characteristics were not significantly different in the 2 groups. We found a significantly lower rate of recurrence (5.0% vs 15.2%) in the stent-assisted coiling group than in the coiling-alone group, with a comparable rate of thromboembolic complications (3.8% vs 2.3%) in these 2 types of endovascular treatment technique groups. Additionally, according to 6- to 18-month follow-up results, we obtained comparable good clinical outcomes in the 2 groups. However, for ruptured aneurysms, there still remains a debate on whether stenting might increase the risk of complications at the acute stage
and cause poor clinical outcomes. A systematic review reported that stent-assisted coiling treatment of aneurysms was associated with unfavorable clinical outcomes compared with data for coiling alone.9 However, Tähtinen et al28 showed more favorable clinical outcomes in patients treated with stent-assisted coiling, and recommended that stent-assisted coiling might be used to treat ruptured aneurysms with complex morphology. In this study, we demonstrated comparable complications and clinical outcomes in the two types of treatment technique, which implied that stentassisted coiling might be a safe technique in the treatment of ruptured aneurysms. In our study, we found that larger aneurysm size and higher HH grade were predictors of procedural morbidity, which were similar to the study of Starke et al.29 Our study also confirmed the previous findings that larger aneurysm size, subarachnoid hemorrhage, anterior circulation aneurysms, incomplete occlusion, and lack of stent assistance were predictors of aneurysm recurrence.14,17,19,30,31 Raymond et al14 reported that duration of follow-up was also an important predictor of aneurysm recurrence. In our study, duration of follow-up was not a predictor of recurrence, and the possible reason might be the short follow-up
TABLE 5. Predictors of Aneurysm Recurrence Univariate Analysis Factors Age Sex Aneurysm size Anterior circulation aneurysm Ruptured aneurysm Hunt and Hess grade Stent treatment Type of stent Initial occlusion grade Follow-up time
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Multivariate Analysis
Odds Ratio
95% Confidence Interval
P Value
Odds Ratio
95% Confidence Interval
P Value
1.008 0.968 0.914 0.425 3.891 0.739 3.957 1.134 0.587 0.827
0.982-1.043 0.462-1.527 0.862-0.983 0.218-0.793 1.865-7.801 0.413-1.162 1.963-8.312 0.801-1.754 0.391-0.824 0.584-1.105
.436 .931 ,.001 ,.001 ,.001 .164 ,.001 .163 .001 .12
— — 0.903 0.301 3.473 — 3.831 — 0.543 —
— — 0.843-0.966 0.149-0.609 1.694-7.123 — 1.795-8.176 — 0.373-0.792 —
— — .003 .001 .001 — .001 — .002 —
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YANG ET AL
period in our study. A study with longer follow-up is needed to verify the results. Interpretation We obtained a relatively low recurrence rate compared with other studies.14,21 One major reason might be the short follow-up period of our study. One confounder is that more ruptured aneurysms and higher HH grade patients were in the coilingalone group and larger aneurysm size in the stent-assisted coiling group, which might be associated with the comparable procedure-related complications and clinical outcome in the 2 types of endovascular treatment. Although we evaluated the ruptured and unruptured aneurysms separately, the selection bias was not addressed completely. Additionally, we did not treat patients aggressively in the setting of subarachnoid hemorrhage because of the potential bleeding complications induced by dualantiplatelet medication. Limitations and Generalizability This was a retrospective study with no randomization. There was selection bias in this study. There were more larger, widenecked, and complex aneurysms in the stent-assisted coiling group. Additionally, there were more ruptured aneurysms in the coiling-alone group. It is very difficult to randomize patients to stent-assisted coiling or to coiling alone without considering the morphological features and status of aneurysm. Another limitation is that this study did not have long-term follow-up results. Therefore, the recurrence rate may be underestimated. Previous studies demonstrated that the recurrence rate was lower in patients treated by stent-assisted coiling compared with coiling alone during long-term follow-up,14,19 which probably still needs a large prospective study to confirm.
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CONCLUSION In our study, we found that stent-assisted coiling for intracranial aneurysms achieved lower recurrence rates, with similar procedure-related complications and clinical outcomes compared with coiling alone. Comparing subgroups of ruptured and unruptured aneurysms, there was no significant difference in procedural events and clinical outcomes except for recurrence rate.
17.
Disclosures
20.
This work was supported by Capital Special Health Development Research Foundation Grant 2014-3-2044 founded by Beijing Municipal Health Bureau of China. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
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23.
24.
stent deployment and midterm follow-up. Neurosurgery. 2007;61(3):460-468; discussion 468-469. Higashida RT, Smith W, Gress D, et al. Intravascular stent and endovascular coil placement for a ruptured fusiform aneurysm of the basilar artery. Case report and review of the literature. J Neurosurg. 1997;87(6):944-949. Wiebers DO, Whisnant JP, Huston J III, et al. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362(9378):103-110. Gao B, Baharoglu MI, Cohen AD, Malek AM. Stent-assisted coiling of intracranial bifurcation aneurysms leads to immediate and delayed intracranial vascular angle remodeling. AJNR Am J Neuroradiol. 2012;33(4):649-654. Zhu YQ, Li MH, Fang C, et al. Application of the Willis covered stent in the treatment of aneurysm in the cisternal segment of the internal carotid artery: a pilot comparative study with midterm follow-up. J Endovasc Ther. 2010;17(1): 55-65. Raymond J, Darsaut TE, Bing F, et al. Stent-assisted coiling of bifurcation aneurysms may improve endovascular treatment: a critical evaluation in an experimental model. AJNR Am J Neuroradiol. 2013;34(3):570-576. Shapiro M, Becske T, Sahlein D, Babb J, Nelson PK. Stent-supported aneurysm coiling: a literature survey of treatment and follow-up. AJNR Am J Neuroradiol. 2012;33(1):159-163. Bodily KD, Cloft HJ, Lanzino G, Fiorella DJ, White PM, Kallmes DF. Stentassisted coiling in acutely ruptured intracranial aneurysms: a qualitative, systematic review of the literature. AJNR Am J Neuroradiol. 2011;32(7):1232-1236. Akpek S, Arat A, Morsi H, Klucznick RP, Strother CM, Mawad ME. Selfexpandable stent-assisted coiling of wide-necked intracranial aneurysms: a singlecenter experience. AJNR Am J Neuroradiol. 2005;26(5):1223-1231. Li H, Pan R, Wang H, et al. Clipping versus coiling for ruptured intracranial aneurysms: a systematic review and meta-analysis. Stroke. 2013;44(1):29-37. Zhang Z, Lv X, Wu Z, et al. Clinical and angiographic outcome of endovascular and conservative treatment for giant cavernous carotid artery aneurysms. Interv Neuroradiol. 2014;20(1):29-36. Qian Z, Peng T, Liu A, et al. Early timing of endovascular treatment for aneurysmal subarachnoid hemorrhage achieves improved outcomes. Curr Neurovasc Res. 2014;11(1):16-22. Raymond J, Guilbert F, Weill A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke. 2003; 34(6):1398-1403. Li MH, Gao BL, Fang C, et al. Angiographic follow-up of cerebral aneurysms treated with Guglielmi detachable coils: an analysis of 162 cases with 173 aneurysms. AJNR Am J Neuroradiol. 2006;27(5):1107-1112. 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. Colby GP, Paul AR, Radvany MG, et al. A single center comparison of coiling versus stent assisted coiling in 90 consecutive paraophthalmic region aneurysms. J Neurointerv Surg. 2012;4(2):116-120. Lawson MF, Newman WC, Chi YY, Mocco JD, Hoh BL. Stent-associated flow remodeling causes further occlusion of incompletely coiled aneurysms. Neurosurgery. 2011;69(3):598-603; discussion 603-594. 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. Jahshan S, Abla AA, Natarajan SK, et al. Results of stent-assisted vs Non-stentassisted endovascular therapies in 489 cerebral aneurysms: single-center experience. Neurosurgery. 2013;72(2):232-239. Hong Y, Wang YJ, Deng Z, Wu Q, Zhang JM. Stent- assisted coiling versus coiling in treatment of intracranial aneurysm: a systematic review and metaanalysis. PLoS One. 2014;9(1):e82311. Fiehler J, Ries T. Prevention and treatment of thromboembolism during endovascular aneurysm therapy. Klin Neuroradiol. 2009;19(1):73-81. Fiorella D, Albuquerque FC, Han P, McDougall CG. Preliminary experience using the Neuroform stent for the treatment of cerebral aneurysms. Neurosurgery. 2004;54(1):6-16; discussion 16-17. Lee DH, Arat A, Morsi H, Shaltoni H, Harris JR, Mawad ME. Dual antiplatelet therapy monitoring for neurointerventional procedures using a point-of-care platelet function test: a single-center experience. AJNR Am J Neuroradiol. 2008;29 (7):1389-1394.
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STENT-ASSISTED COILING VS COILING ALONE
25. McTaggart RA, Choudhri OA, Marcellus ML, et al. Use of thromboelastography to tailor dual-antiplatelet therapy in patients undergoing treatment of intracranial aneurysms with the Pipeline embolization device. J Neurointerv Surg. doi: 10. 1136/neurintsurg-2013-011089. Epub 2014 Apr 16. 26. Kim DJ, Suh SH, Kim BM, Kim DI, Huh SK, Lee JW. Hemorrhagic complications related to the stent-remodeled coil embolization of intracranial aneurysms. Neurosurgery. 2010;67(1):73-78; discussion 78-79. 27. Dumont AS, Evans AJ, Jensen ME. Hemorrhagic complications associated with stent-assisted coil embolization. J Neurosurg. 2008;108(6):1119-1121. 28. 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. 29. 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. 30. Murayama Y, Nien YL, Duckwiler G, et al. Guglielmi detachable coil embolization of cerebral aneurysms: 11 years’ experience. J Neurosurg. 2003;98 (5):959-966. 31. Sluzewski M, van Rooij WJ, Slob MJ, Bescós JO, Slump CH, Wijnalda D. Relation between aneurysm volume, packing, and compaction in 145 cerebral aneurysms treated with coils. Radiology. 2004;231(3):653-658.
COMMENT
T
he authors retrospectively review their experience with stent-assisted coiling and compared that with patients treated by coiling alone for the endovascular management of intracranial aneurysms. The study was not randomized nor should it have been. The intracranial aneurysms of patients treated with stent assistance are those that typically have a wider
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neck and therefore merit a stent to contain the coil. Interestingly, the authors had an almost equal split between their patients treated with coiling alone and those treated with stent assistance. Procedure-related complications were very similar in each group at 6.2% for those treated with coiling alone and 6.3% in the stent-assisted coiling group. The same was true for procedural permanent morbidity and mortality. In terms of recanalization, a significantly lower incidence of recanalization (retreatment) was found in those patients treated with stent assistance. This is in keeping with the findings of other groups and suggests that the stent adds an element of flow diversion to assist in stagnation of flow in the aneurysm and therefore thrombosis. Indeed, when a stent is deployed before coil deployment, this can be observed on the angiogram during a procedure. This was true for both ruptured and unruptured lesions. The authors’ findings raise some interesting questions about the endovascular treatment of aneurysms. Given the increasing safety of stent assistance, one wonders whether stents should be considered in a larger number of aneurysms to reduce the recurrence rate. One fear of using stent assistance for the acutely ruptured aneurysm has been that of having to give dual-antiplatelet therapy of aspirin and clopidogrel in the setting of subarachnoid hemorrhage. The authors’ data would suggest that this was not associated with an increase in hemorrhagic complications. The authors’ data support what many treating physicians are finding using endovascular techniques, namely, stent assistance does not significantly increase morbidity and mortality in the treatment of intracranial aneurysms. Christopher S. Ogilvy Boston, Massachusetts
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Comparison of Stent-Assisted Coiling vs Coiling Alone in 563 Intracranial Aneurysms: Safety and Efficacy at a High-Volume Center Hongchao Yang, MD Yong Sun, MD Yuhua Jiang, MD Xianli Lv, MD Yang Zhao, MM Youxiang Li, MD, PhD Aihua Liu, MD Department of Interventional Neuroradiology, Beijing Neurosurgical Institute, Beijing Tiantan Hospital, Capital Medical University, Beijing, China Correspondence: Youxiang Li, MD, PhD, Department of Interventional Neuroradiology, Beijing Neurosurgical Institute, No. 6 Tiantan West Road, Dongcheng District, Beijing, China. E-mail: [email protected] Received, November 21, 2014. Accepted, February 25, 2015. Published Online, April 7, 2015. Copyright © 2015 by the Congress of Neurological Surgeons.
BACKGROUND: Stent-assisted coiling has been used in both unruptured and ruptured aneurysms, but the safety and efficacy still remain controversial. OBJECTIVE: To compare the safety and efficacy of stent-assisted coiling with coiling alone for intracranial aneurysms. METHODS: We retrospectively reviewed 512 patients treated by endovascular coiling or stent-assisted coiling over a 1-year period. The patients’ clinical and imaging information was recorded. Procedure-related complication rates, recurrence rates, and clinical outcomes were analyzed in both the total aneurysms and the subgroups of ruptured and unruptured aneurysms. RESULTS: A total of 243 patients were treated by coiling alone and 269 patients were treated by stent-assisted coiling. Procedure-related complications occurred in 6.2% of patients in the coiling-alone group compared with 6.3% in the stent-assisted coiling group. The procedural permanent morbidity and mortality rates were 1.6% (4/243) and 1.2% (3/243), respectively, in the coiling-alone group and 1.1% (3/269) and 1.5% (4/269), respectively, in the stent-assisted coiling group. A significantly lower recurrence rate was found in the stent-assisted coiling group compared with the coilingalone group (5.2% vs 16.5%, P = .002). In a comparison of subgroups of ruptured and unruptured aneurysms, the procedural complications rates were comparable in the 2 groups, with a lower recurrence rate in the stent-assisted coiling group. Multivariate analysis showed that larger aneurysm size and higher Hunt and Hess grade were predictors of procedural morbidity; larger aneurysm size, ruptured aneurysm, anterior circulation aneurysms, initial incomplete occlusion, and lack of stent assistance were predictors of recurrence. CONCLUSION: Compared with coiling alone, stent-assisted coiling may achieve lower recurrence rates, with comparable procedure-related complications and clinical outcomes in both ruptured and unruptured aneurysms. KEY WORDS: Cerebral aneurysm, Coil, Endovascular, Stent Neurosurgery 77:241–247, 2015
DOI: 10.1227/NEU.0000000000000765
E
ndovascular treatment has become an important technique for intracranial aneurysms. To increase packing density, improve neck coverage, and prevent coil protrusion, stents were invented and used to treat wide-necked and morphologically complex aneurysms. Additionally, stents have flow-diverting properties and provide a scaffold for endothelialization, which
ABBREVIATIONS: HH, Hunt and Hess; mRS, modified Rankin Scale
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may facilitate aneurysm thrombosis and eventual obliteration.1-3 Several studies have shown that stent-assisted coiling achieved favorable outcomes and decreased recanalization rates.4-7 However, literature review also showed that stent-assisted coiling had higher morbidity and mortality rates compared with coiling alone, especially in ruptured aneurysms.8-10 This study aimed to compare the safety and efficacy of treating ruptured and unruptured intracranial aneurysms by coiling alone and stent-assisted coiling.
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YANG ET AL
METHODS We retrospectively collected patients with intracranial aneurysms treated by endovascular embolization between February 2013 and February 2014 in our institution. Informed consent from all patients was obtained, and the protocol of this study was approved by our institution. The baseline data on age, sex, medical history, aneurysm size and location, subarachnoid hemorrhage, and Hunt and Hess (HH) grade were recorded. All ruptured aneurysms were confirmed by computed tomography (CT) scan. The procedure-related complications and immediate and follow-up angiographic results were reviewed. Embolization was complete when there was no contrast filling of the dome, body, or neck of the aneurysm. A neck remnant (or nearly complete occlusion) was defined by a residual neck (,2 mm) and incomplete embolization by a residual part of aneurysmal sac. An aneurysm that displayed a decreasing percentage of occlusion on follow-up angiography was considered a recurrence, eg, the occlusion grade decreasing from complete occlusion to a neck remnant or from a neck remnant to a residual aneurysm. We decided to use a stent if the aneurysm was wide necked (.4 mm or dome/neck ,2 mm) or morphologically complex and coiling alone could not obtain a satisfactory treatment result. However, in the setting of acute subarachnoid hemorrhage, coiling alone was preferred. A total of 512 patients with 563 aneurysms were treated with endovascular embolization. General anesthesia and systemic heparinization were used in all patients, and the activated clotting time was maintained at between 250 and 300 seconds during the procedure. For patients treated with stent-assisted coiling, dual-antiplatelet therapy (100 mg/d aspirin and 75 mg/d clopidogrel) was administered for unruptured aneurysms at least 3 to 5 days before the procedure, and a loading dose of 300 mg aspirin and 300 mg clopidogrel was given for ruptured aneurysms at least 2 hours before the procedure. After the procedure, patients were given clopidogrel (75 mg/d) for 4 to 6 weeks and aspirin (100 mg/d) for 6 months. The Enterprise stent (Cordis Neurovascular, Miami, Florida) and the Solitaire stent (Solitaire AB neurovascular remodeling device; eV3 Inc, Irvine, California) were used to treat wide-necked or complex aneurysms.
Statistical Analysis Normally distributed continuous data are presented as mean 6 SD and categorical data as frequency and percentage. Analysis was carried out with an independent-samples t test and the x2 and Fisher exact tests. Univariate logistic regression was used to analyze potential factors, and a covariate with a univariate P value of ,.05 was included in multivariate logistic regression to identify predictors of procedural complications and aneurysm recanalization. No adjustment for multiple comparisons was performed. The odds ratio, 95% confidence interval, and P value were determined for factors of the univariate and multivariate models. Statistical significance was defined as P , .05 and an odds ratio with 95% confidence interval not including 1.0. Statistical analysis was carried out with SPSS version 17.0 (SPSS Inc, Chicago, Illinois).
with stent-assisted coiling (Figure). Patient and aneurysm baseline characteristics are summarized in Table 1. There were no statistically significant differences in patient age, sex, medical history, or aneurysm location in the 2 groups. However, there was significantly higher rate of ruptured aneurysms in the coiling-alone group. Additionally, the aneurysm size was significantly larger in the stent-assisted coiling group. Descriptive Data and Main Results Complications and Outcomes Procedure-related complications occurred in 15 patients (6.2%, 15/243) in the coiling-alone group compared with 17 patients (6.3%, 17/269) in the stent-assisted coiling group. Thromboembolic complications occurred in 10 patients (4.1%, 10/243) in the coiling-alone group, and 13 patients (4.8%, 13/269) in the stentassisted coiling group, which caused permanent neurological deficit in 0.8% patients (2/243) in the coiling-alone group and 1.1% patients (3/269) in the stent-assisted coiling group, respectively. Additionally, 1 patient in the stent-assisted coiling group died of brainstem acute ischemic stroke. In the coiling-alone group, intraoperative rupture occurred 1 patient (modified Rankin Scale [mRS] score of 3 at discharge), and cerebral hemorrhage occurred in 4 patients after initial treatment (1 patient with an mRS score of 3, 3 patients died). In the stent-assisted coiling group, 3 patients died of rebleeding. Therefore, the procedure-related permanent morbidity and mortality rates were 1.6% (4/243) and 1.2% (3/243), respectively, in the coiling-alone group vs 1.1% (3/269) and 1.5% (4/269), respectively, in the stent-assisted coiling group. Clinical follow-up (range, 6-18 months; mean, 11.2 months) was available for 88.5% (215/243) of patients in the coiling-alone group vs 92.2% (248/269) of patients in the stent-assisted coiling group. According to final follow-up results, 181 patients (84.2%, 181/215) had favorable clinical outcomes (mRS scores of 0-2) in the coiling-alone group compared with 219 patients (88.3%, 219/ 248) in the stent-assisted coiling group (P = .19). Angiographic Results Initial complete occlusion was achieved in 64.2% (156/243) of patients in the coiling-alone group and in 53.9% (145/269) of
RESULTS Participants Baseline Characteristics Of the 512 patients, 243 with 266 aneurysms were treated with coiling alone and 269 with 297 aneurysms were treated
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FIGURE. Distribution of endovascular treatment of the 563 aneurysms in this study.
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STENT-ASSISTED COILING VS COILING ALONE
TABLE 1. Baseline Characteristics of Patientsa Coiling Alone Age, y, mean 6 SD Female Medical history Hypertension Diabetes Brain ischemia Coronary heart disease Ruptured aneurysmsb HH gradec 1-2 3-4 Aneurysm locationb Anterior circulation Posterior circulation Dome-to-neck ratiob Mean aneurysm diameter,b mm, mean 6 SD #5 5-15 .15
TABLE 2. Comparison of Coiling Alone and Stent-Assisted Coiling in Patients With Unruptured Aneurysmsa
Stent-Assisted P Coiling Value
54.3 6 12.9 151 (62.1)
54.4 6 11.1 173 (64.3)
.87 .85
87 (35.8) 23 (9.4) 25 (10.3) 14 (5.8) 115 (47.3)
115 (42.8) 28 (10.4) 22 (8.2) 17 (6.3) 58 (21.6)
.11 .72 .41 .79 ,.001 .001
35 (30.4) 80 (68.6)
33 (56.9) 25 (43.1)
198 (74.4) 68 (25.6) 2.5 6.7 6 3.6
232 (78.1) 65 (21.9) 1.6 8.8 6 7.1
107 (40.2) 150 (56.4) 9 (3.4)
102 (34.3) 154 (51.9) 41 (13.8)
Coiling Alone Age Female Mean aneurysm diameter,b mm, mean 6 SD Thromboembolic events Hemorrhagic complications Procedure-related mortality Initial complete occlusion Recanalization mRS score at follow-up 0-2
.31
Stent-Assisted P Coiling Value
53.1 6 13.5 53.9 6 11.6 87/128 (68.0) 136/211 (65.9) 7.4 6 4.2 8.7 6 7.2
.54 .51 .22
3/128 (2.3) 8/211 (3.8) 2/128 (1.6) 0 1/128 (0.8) 1/211 (0.5) 82/128 (64.1) 115/211 (54.5) 10/66 (15.2) 5/100 (5.0)
.54c .14c 1.0c .08 .03 .46
97/113 (85.8) 173/195 (88.7)
a
.08 .03 .001
SD, standard deviation; mRS, modified Rankin Scale. Data in parentheses are percentages. b Data are number of aneurysms (140 in coiling-alone group and 233 in stenting group) or number of patients (128 in coiling-alone group and 211 in stenting group). c Fisher exact test.
a
SD, standard deviation; HH, Hunt and Hess. Data in parentheses are percentages. There were 243 patients with 266 aneurysms treated by coiling alone compared with 269 patients with 297 aneurysms treated by stent-assisted coiling. b Data are number of aneurysms. c Data are number of patients with ruptured aneurysms (115 in coiling-alone group and 58 in stenting group) or number of patients.
patients in the stent-assisted coiling group (P = .02). Angiographic follow-up (range, 6-12 months; mean, 7.8 months) was performed by digital subtraction angiography or magnetic resonance angiography and available for 57.2% (139/243) of patients in the coiling-alone group and 56.9% (153/269) of patients in the stent-assisted coiling group. In the coiling-alone group, 21 of 139 (15.1%) patients showed progressive thrombosis occlusion during the follow-up period compared with 50 of 153 (32.7%) patients in the stent-assisted coiling group (P = .001). The recurrence rate was 16.5% (23/ 139) for the coiling-alone group and 5.2% (8/153) for the stentassisted coiling group (P = .002), including 16 patients (69.6%, 16/23) in the coiling-alone group and 2 patients (25.0%, 2/8) in the stent-assisted coiling group, who required retreatment because of growth shown on angiography and mass-effect symptoms (P = .04). Coiling Alone vs Stent-Assisted Coiling in Unruptured Aneurysms There were 128 patients with unruptured aneurysms in the coiling-alone group compared with 211 patients in the stentassisted coiling group. A comparison of the results in these 2 groups is summarized in Table 2; baseline characteristics showed no significant differences in these 2 groups.
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Although the rate of thromboembolic complications was higher in the stent-assisted coiling group (3.8%) than in the coiling-alone group (2.3%), this difference was not statistically significant (P = .54). Immediate complete occlusion was achieved in 64.1% of the coiling-alone group and 54.5% of the stent-assisted coiling group, which showed no statistically significant differences (P = .08). The recurrence rate was significantly higher in the coiling-alone group than in the stent-assisted coiling group (15.2% vs 5.0%, P = .03). Two cerebral hemorrhages occurred in the coiling-alone group (1 had an mRS score of 3 at discharge and 1 died 3 days after the initial treatment), but none were in the stent-assisted coiling group. As previously mentioned, 1 patient died of brainstem acute ischemia in the stent-assisted coiling group. There were 97 patients (85.8%, 97/113) with favorable outcomes in the coilingalone group and 173 patients (88.7%, 173/195) in the stentassisted coiling group (P = .46). Coiling Alone vs Stent-Assisted Coiling in Ruptured Aneurysms A total of 115 patients with ruptured aneurysms were treated by coiling alone and 58 patients by stent-assisted coiling. A comparison of the results in these 2 groups is shown in Table 3. Baseline characteristics were comparable except for the aneurysm size and initial HH grades, which showed larger aneurysm size in the stent-assisted coiling group than the coiling-alone group (5.5 6 2.0 mm vs 8.4 6 6.8 mm, respectively, P = .02) and a higher HH grade (grades 3-4) in the coiling-alone group (P = .001). The thromboembolic complication rate was 6.1% in the coiling-alone
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TABLE 3. Comparison of Coiling Alone and Stent-Assisted Coiling in Patients With Ruptured Aneurysmsa
Age Female Mean aneurysm diameter,b mm, mean 6 SD HH grade 3-4 Thromboembolic events Hemorrhagic complication Procedure-related mortality Initial complete occlusion Recanalization mRS score at last follow-up 0-2
Coiling Alone
Stent-Assisted Coiling
P Value
55.7 6 12.3 64/115 (55.7) 5.5 6 2.0
56.4 6 8.7 37/58 (63.8) 8.4 6 6.8
.71 .31 .02
80/115 (69.6) 7/115 (6.1)
25/58 (43.1) 5/58 (8.6)
.001 .54c
3/115 (2.6)
3/58 (5.2)
.41
c
c
2/115 (1.7)
3/58 (5.2)
.34
74/115 (64.3)
30/58 (51.7)
.11
13/73 (17.8)
3/53 (5.7)
.04 .48
84/102 (82.4)
46/102 (86.8)
a
SD, standard deviation; HH, Hunt and Hess; mRS, modified Rankin Scale. Data in parentheses are percentages. b Data are number of aneurysms (126 in coiling-alone group and 64 in stentassisted coiling group) or number of patients (115 in coiling-alone group and 58 in stent-assisted coiling group). c Fisher exact test.
group and 8.6% in the stent-assisted coiling group, but with no statistically significant difference (P = .54). The hemorrhagic complication rate was 2.6% in the coiling-alone group compared with 5.2% in the stent-assisted coiling group (P = .33). Immediate complete occlusion was achieved in 64.3% of the coiling-alone group and 51.7% of the stent-assisted coiling group, which showed no statistically significant difference (P = .11). The recurrence rate was significantly higher in the coiling-alone group than in the stent-assisted coiling group (17.8% vs 5.7%, respectively, P = .043). There were 82.4% patients (84/102) with favorable outcomes in the coiling-alone group (mRS scores of 0-2) and 86.8% (46/53) in the stent-assisted coiling group (P = .48). Predictors of Morbidity and Recurrence On univariate analysis, the following variables were tested as predictors of procedural morbidity: age (P = .52), sex (P = .46), aneurysm size (P = .002), anterior circulation aneurysm (P = .01), ruptured aneurysms (P = .02), HH grades (P = .001), type of endovascular technique (P = .22), type of stent (P = .68), and initial occlusion results (P = .47). Therefore, based on the univariate results, larger aneurysm size, anterior circulation aneurysm, ruptured aneurysm, and higher HH grade were associated with higher procedural morbidity. However, only larger aneurysm size (P = .01) and higher HH grade (P = .01) were predictors of procedural morbidity on multivariate analysis (Table 4).
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Regarding predictors of recurrence, the following factors were tested on univariate analysis: age (P = .44), sex (P = .93), aneurysm size (P , .001), anterior circulation aneurysm (P , .001), ruptured aneurysms (P , .001), HH grades (P = .16), stent treatment (P , .001), type of stent (P = .16), initial occlusion grade (P = .001), and follow-up time (P = .12). On multivariate analysis, larger aneurysm size, ruptured aneurysms, anterior circulation aneurysms, initial incomplete occlusion, and lack of stent assistance were associated with higher recurrence rates (Table 5).
DISCUSSION Key Results Endovascular coil embolization has been widely used to treat intracranial aneurysms.11-13 However, 1 major limitation of coil embolization is the relatively high recurrence rate, especially of wide-necked and complex aneurysms. Raymond et al14 reported a 33.6% recurrence rate of 501 aneurysms treated by coiling during a mean follow-up time of 12.3 6 11.33 months. Previous studies have reported aneurysm recurrence after coil embolization is associated with incomplete occlusion grade.15,16 Stents can serve as a scaffold for endothelialization and have an effect of flow diversion, which may induce changes in intra-aneurysmal hemodynamics and promote delayed thrombosis and obtain more complete occlusion in the long term.17,18 Several studies of stent-assisted coiling for aneurysms have shown that progressive thrombosis caused a more complete occlusion and decreased recurrence rate.19,20 Although the initial incomplete occlusion rate was higher in the stent-assisted coiling group in our study, the rates of recurrence and retreatment were significantly higher in the coiling-alone group than that in the stent-assisted coiling group, which might be associated with the significantly progressive thrombosis in the stent-assisted coiling group. In our study, procedure-related complications were comparable in the stent-assisted coiling group and the coiling-alone group, which were similar to the findings of Hong et al21 meta-analysis study. Thromboembolic events were the major complication, and the rate of this complication was comparable in the 2 groups. Previous studies showed a higher rate of thromboembolic complications in patients treated by stent-assisted coiling, which might be associated with thrombogenicity of stents.1,22,23 Dualantiplatelet therapy played an important role to prevent thromboembolic complications in our patients treated by stent-assisted coiling. Piotin et al19 reported a significantly higher permanent complication rate in the stent-assisted coiling group than that in the coiling-alone group, but dual-antiplatelet therapy was not used in the group of patients treated by stenting. Lee et al24 reported that 42.9% of their patients had a poor response to clopidogrel, and all thromboembolic events occurred in the poor-response group, which implied that a poor response to antiplatelet medication might induce thromboembolic complications. Platelet function test has been used to ascertain the effects of antiplatelet medication. The risk of thromboembolic
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TABLE 4. Predictors of Procedural Morbidity Univariate Analysis Factors Age Sex Aneurysm size Anterior circulation aneurysm Ruptured aneurysm Hunt and Hess grade Type of treatment technique Type of stent Initial occlusion grade
Multivariate Analysis
Odds Ratio
95% Confidence Interval
P Value
Odds Ratio
95% Confidence Interval
P Value
1.008 0.893 0.716 0.598 2.183 0.568 1.086 0.958 0.725
0.985-1.031 0.428-1.394 0.572-0.964 0.332-0.879 1.102-3.562 0.273-0.914 0.835-1.412 0.626-1.323 0.458-1.020
.52 .46 .002 .005 .02 .001 .22 .68 .47
— — 0.671 — — 0.411 — — —
— — 0.498-0.904 — — 0.205-0.826 — — —
— — .01 — — .01 — — —
complications might be decreased by adjusting the protocol of antiplatelet therapy based on the results of the platelet function test.25 Previous studies demonstrated a higher risk of procedurerelated hemorrhagic complications in patients undergoing stentassisted coiling, especially in patients with acute subarachnoid hemorrhage.26,27 However, the rate of procedural hemorrhagic complications in our study was comparable in the coiling-alone group and the stent-assisted coiling group (2.1% vs 1.1%). Only 1 case of intraprocedural aneurysm rupture occurred in our series, which caused a permanent neurological deficit (mRS score of 3). In unruptured aneurysms, the baseline characteristics were not significantly different in the 2 groups. We found a significantly lower rate of recurrence (5.0% vs 15.2%) in the stent-assisted coiling group than in the coiling-alone group, with a comparable rate of thromboembolic complications (3.8% vs 2.3%) in these 2 types of endovascular treatment technique groups. Additionally, according to 6- to 18-month follow-up results, we obtained comparable good clinical outcomes in the 2 groups. However, for ruptured aneurysms, there still remains a debate on whether stenting might increase the risk of complications at the acute stage
and cause poor clinical outcomes. A systematic review reported that stent-assisted coiling treatment of aneurysms was associated with unfavorable clinical outcomes compared with data for coiling alone.9 However, Tähtinen et al28 showed more favorable clinical outcomes in patients treated with stent-assisted coiling, and recommended that stent-assisted coiling might be used to treat ruptured aneurysms with complex morphology. In this study, we demonstrated comparable complications and clinical outcomes in the two types of treatment technique, which implied that stentassisted coiling might be a safe technique in the treatment of ruptured aneurysms. In our study, we found that larger aneurysm size and higher HH grade were predictors of procedural morbidity, which were similar to the study of Starke et al.29 Our study also confirmed the previous findings that larger aneurysm size, subarachnoid hemorrhage, anterior circulation aneurysms, incomplete occlusion, and lack of stent assistance were predictors of aneurysm recurrence.14,17,19,30,31 Raymond et al14 reported that duration of follow-up was also an important predictor of aneurysm recurrence. In our study, duration of follow-up was not a predictor of recurrence, and the possible reason might be the short follow-up
TABLE 5. Predictors of Aneurysm Recurrence Univariate Analysis Factors Age Sex Aneurysm size Anterior circulation aneurysm Ruptured aneurysm Hunt and Hess grade Stent treatment Type of stent Initial occlusion grade Follow-up time
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Multivariate Analysis
Odds Ratio
95% Confidence Interval
P Value
Odds Ratio
95% Confidence Interval
P Value
1.008 0.968 0.914 0.425 3.891 0.739 3.957 1.134 0.587 0.827
0.982-1.043 0.462-1.527 0.862-0.983 0.218-0.793 1.865-7.801 0.413-1.162 1.963-8.312 0.801-1.754 0.391-0.824 0.584-1.105
.436 .931 ,.001 ,.001 ,.001 .164 ,.001 .163 .001 .12
— — 0.903 0.301 3.473 — 3.831 — 0.543 —
— — 0.843-0.966 0.149-0.609 1.694-7.123 — 1.795-8.176 — 0.373-0.792 —
— — .003 .001 .001 — .001 — .002 —
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YANG ET AL
period in our study. A study with longer follow-up is needed to verify the results. Interpretation We obtained a relatively low recurrence rate compared with other studies.14,21 One major reason might be the short follow-up period of our study. One confounder is that more ruptured aneurysms and higher HH grade patients were in the coilingalone group and larger aneurysm size in the stent-assisted coiling group, which might be associated with the comparable procedure-related complications and clinical outcome in the 2 types of endovascular treatment. Although we evaluated the ruptured and unruptured aneurysms separately, the selection bias was not addressed completely. Additionally, we did not treat patients aggressively in the setting of subarachnoid hemorrhage because of the potential bleeding complications induced by dualantiplatelet medication. Limitations and Generalizability This was a retrospective study with no randomization. There was selection bias in this study. There were more larger, widenecked, and complex aneurysms in the stent-assisted coiling group. Additionally, there were more ruptured aneurysms in the coiling-alone group. It is very difficult to randomize patients to stent-assisted coiling or to coiling alone without considering the morphological features and status of aneurysm. Another limitation is that this study did not have long-term follow-up results. Therefore, the recurrence rate may be underestimated. Previous studies demonstrated that the recurrence rate was lower in patients treated by stent-assisted coiling compared with coiling alone during long-term follow-up,14,19 which probably still needs a large prospective study to confirm.
3.
4.
5.
6.
7.
8.
9.
10.
11. 12.
13.
14.
15.
16.
CONCLUSION In our study, we found that stent-assisted coiling for intracranial aneurysms achieved lower recurrence rates, with similar procedure-related complications and clinical outcomes compared with coiling alone. Comparing subgroups of ruptured and unruptured aneurysms, there was no significant difference in procedural events and clinical outcomes except for recurrence rate.
17.
Disclosures
20.
This work was supported by Capital Special Health Development Research Foundation Grant 2014-3-2044 founded by Beijing Municipal Health Bureau of China. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
21.
18.
19.
22.
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STENT-ASSISTED COILING VS COILING ALONE
25. McTaggart RA, Choudhri OA, Marcellus ML, et al. Use of thromboelastography to tailor dual-antiplatelet therapy in patients undergoing treatment of intracranial aneurysms with the Pipeline embolization device. J Neurointerv Surg. doi: 10. 1136/neurintsurg-2013-011089. Epub 2014 Apr 16. 26. Kim DJ, Suh SH, Kim BM, Kim DI, Huh SK, Lee JW. Hemorrhagic complications related to the stent-remodeled coil embolization of intracranial aneurysms. Neurosurgery. 2010;67(1):73-78; discussion 78-79. 27. Dumont AS, Evans AJ, Jensen ME. Hemorrhagic complications associated with stent-assisted coil embolization. J Neurosurg. 2008;108(6):1119-1121. 28. 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. 29. 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. 30. Murayama Y, Nien YL, Duckwiler G, et al. Guglielmi detachable coil embolization of cerebral aneurysms: 11 years’ experience. J Neurosurg. 2003;98 (5):959-966. 31. Sluzewski M, van Rooij WJ, Slob MJ, Bescós JO, Slump CH, Wijnalda D. Relation between aneurysm volume, packing, and compaction in 145 cerebral aneurysms treated with coils. Radiology. 2004;231(3):653-658.
COMMENT
T
he authors retrospectively review their experience with stent-assisted coiling and compared that with patients treated by coiling alone for the endovascular management of intracranial aneurysms. The study was not randomized nor should it have been. The intracranial aneurysms of patients treated with stent assistance are those that typically have a wider
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neck and therefore merit a stent to contain the coil. Interestingly, the authors had an almost equal split between their patients treated with coiling alone and those treated with stent assistance. Procedure-related complications were very similar in each group at 6.2% for those treated with coiling alone and 6.3% in the stent-assisted coiling group. The same was true for procedural permanent morbidity and mortality. In terms of recanalization, a significantly lower incidence of recanalization (retreatment) was found in those patients treated with stent assistance. This is in keeping with the findings of other groups and suggests that the stent adds an element of flow diversion to assist in stagnation of flow in the aneurysm and therefore thrombosis. Indeed, when a stent is deployed before coil deployment, this can be observed on the angiogram during a procedure. This was true for both ruptured and unruptured lesions. The authors’ findings raise some interesting questions about the endovascular treatment of aneurysms. Given the increasing safety of stent assistance, one wonders whether stents should be considered in a larger number of aneurysms to reduce the recurrence rate. One fear of using stent assistance for the acutely ruptured aneurysm has been that of having to give dual-antiplatelet therapy of aspirin and clopidogrel in the setting of subarachnoid hemorrhage. The authors’ data would suggest that this was not associated with an increase in hemorrhagic complications. The authors’ data support what many treating physicians are finding using endovascular techniques, namely, stent assistance does not significantly increase morbidity and mortality in the treatment of intracranial aneurysms. Christopher S. Ogilvy Boston, Massachusetts
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