Stent-assisted Coil Placement for the Treatment of 211 Acutely Ruptured Wide-necked Intracranial Aneurysms: A Single-Center 11-Year Experience 1

Note: This copy is for your personal non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at www.rsna.org/rsnarights. Stent-assisted Coil Placement for the Treatment of 211 Acutely Ruptured Wide-necked Intracranial Aneurysms: A Single-Center 11-Year Experience 1 Original Research n Neuroradiology Pengfei Yang, MD Kaijun Zhao, MD Yu Zhou, MD Rui Zhao, MD Lei Zhang, MD Wenyuan Zhao, MD Bo Hong, MD Yi Xu, MD Qinghai Huang, MD Timo Krings, MD Jianmin Liu, MD An earlier incorrect version of this article appeared online. This article was corrected on June 30, 2015. 1 From the Department of Neurosurgery, Changhai Hospital, Second Military Medical University, 168 Changhai Rd, Shanghai 200433, People s Republic of China (P.Y., K.Z., Y.Z., R.Z., L.Z., W.Z., B.H., Y.X., Q.H., J.L.); and Division of Neuroradiology, Departments of Medical Imaging and Surgery, Toronto Western Hospital, University of Toronto, Toronto, Ontario, Canada (T.K.). Received April 24, 2014; revision requested June 6, 2014; revision received October 30; accepted December 11; final version accepted January 15, 2015. Supported in part by the National Natural Science Foundation of China (grant 81471189) and Shanghai Municipal Education Commission (grant 11CG043). Address correspondence to J.L. (e-mail: liu118@vip.163.com). q RSNA, 2015 Purpose: Materials and Methods: Results: Conclusion: To evaluate the safety and angiographic and clinical outcome of stent-assisted coil placement (SACP) for acutely ruptured wide-necked intracranial aneurysms treated in a single center during an 11-year period. According to an institutional review board approved protocol, the angiographic and clinical data of 211 patients (52 men, 159 women; median age, 56 years; age range, 31 83 years) with acutely ruptured wide-necked intracranial aneurysms (neck. 4 mm and/or dome-to-neck ratio 2) treated with SACP from September 2000 to December 2011 were reviewed retrospectively. Baseline characteristics, procedure-related complications, angiographic follow-up results, and clinical outcome were analyzed statistically. A Mann-Whitney U test was performed for non normally distributed continuous variables. A Pearson x 2 or Fisher exact test was performed for categorical variables. Univariate analysis and logistic regression analysis were performed to determine the association of procedure-related complications and clinical outcome with potential risk factors. Procedure-related complications occurred in 30 patients (14.2%). They were more common in the anterior communicating artery (26.7%, 12 of 45) and middle cerebral artery bifurcation (40%, four of 10) aneurysms than in aneurysms at other locations (9.0%, 14 of 156). Clinical outcome (median, 33 months) was good in 175 patients (82.9%) with a modified Rankin Scale score of up to 2. Older age (P =.013, odds ratio = 1.054) and higher Hunt and Hess grade (P,.001, odds ratio = 15.876) were independent risk factors for unfavorable outcome. One hundred fifty-two of 190 patients who survived (80%) underwent angiographic follow-up at least once (median, 12 months). The complete occlusion rate improved from an immediate 45.5% to 75.7% at follow-up (115 of 152 patients). Angiographic and clinical outcomes in our series were comparable to those reported by using coil placement alone or balloon-assisted coil placement techniques. SACP for the treatment of acutely ruptured middle cerebral artery bifurcation and anterior communicating artery aneurysms was associated with a significantly higher incidence of complications than was the case for treatment of aneurysms at other locations. q RSNA, 2015 Radiology: Volume 276: Number 2 August 2015 n radiology.rsna.org 545

Acutely ruptured wide-necked intracranial aneurysms pose technical challenges to the treating physician; thus, multiple endovascular techniques have been described to treat these lesions, including balloon-assisted coil placement (1), double microcatheter technique (2), and microcatheterassisted coil placement (3). However, the use of these techniques can sometimes be limited, owing to the lack of permanent support for the coil mass inside the aneurysm sac, which may lead to coil prolapse or migration after the procedure, especially for wide-necked aneurysms (dome-to-neck ratio, 1) or tiny aneurysms (,3 mm). Therefore, surgical clipping is preferred for acutely ruptured wide-necked intracranial aneurysms in most institutions. Surgery, however, may also be challenging in some of these lesions, since clips may slip, and surgical access may be limited because of the swelling of the brain in the acute setting of a subarachnoid hemorrhage. Since the description by Higashida et al regarding stent placement to treat Advances in Knowledge nn The rates of favorable outcomes (82.9%) and procedural complications (14.2%) after stentassisted coil placement (SACP) in acutely ruptured wide-necked intracranial aneurysms are comparable to those reported with simple coil placement and balloon-assisted coil placement of similar aneurysms. nn Complete occlusion of the aneurysm sac is crucial to prevent postprocedural early repeat bleeding, because the incidence of early repeat bleeding was closely correlated (P =.035) with the degree of occlusion immediately after treatment. nn The incidence of procedurerelated complications was significantly higher in patients with middle cerebral artery (MCA) bifurcation and anterior communicating artery aneurysms than in those with aneurysms at other locations (P =.003). an acutely ruptured fusiform posterior fossa aneurysm in 1997 (4), stent-assisted coil placement (SACP) has been increasingly used and extensively reported as an effective means to treat widenecked intracranial aneurysms, especially after the advent of self-expandable intracranial stents. However, most investigators have reported the experience of this type of treatment in unruptured wide-necked intracranial aneurysms. Only a few investigators have described SACP in acutely ruptured wide-necked intracranial aneurysms. Owing to limitations in the number of reported cases and the varied inclusion criteria, the safety and effectiveness of SACP in acutely ruptured wide-necked intracranial aneurysms are not known (5 11). In this report, we present a retrospective analysis of the procedure-related complications, clinical outcomes, immediate postangiographic outcomes, and shortterm angiographic outcomes achieved in a single-center series during an 11-year period by using SACP for the treatment of acutely ruptured wide-necked intracranial aneurysms. Materials and Methods According to an institutional review board approved protocol, three experienced endovascular surgeons (P.Y., Y.Z., and L.Z.) retrospectively reviewed the angiographic and clinical data of 211 patients treated with SACP for an acutely ruptured wide-necked intracranial aneurysm during an 11-year period between September 2000 and December 2011. Patient Selection and Population Inclusion criteria for this study were (a) ruptured saccular aneurysm with a wide neck (neck. 4 mm and/or dometo-neck ratio 2) and (b) acutely ruptured aneurysm, which was defined Implication for Patient Care nn SACP is an alternative for the treatment of acutely ruptured wide-necked intracranial aneurysms in locations other than the MCA bifurcation or the anterior communicating artery. as an aneurysm treated no more than 28 days after the initial rupture. The exclusion criteria for this study were (a) aneurysms other than saccular that is, fusiform, traumatic, and blood blister like; (b) aneurysms treated with special treatment strategies that is, staged stent placement and stent placement alone; and (c) patients with multiple aneurysms, where there was doubt about which aneurysm had ruptured. From September 2000 to November 2011, we treated 805 patients with stents at our institution. According to our criteria, a total of 211 consecutive patients (52 men, 159 women) were included in this analysis (Fig 1). Patient age ranged between 31 and 83 years (median, 56 years). The interval between aneurysm rupture and treatment with SACP was up to 3 days for 91 patients (43.1%), 3 14 days for 90 patients (42.6%), and 14 28 days for 30 patients (14.2%). According to the Hunt and Hess scale, 194 patients (91.9%) were classified as grade I III, and 17 (8.0%) were classified as grade IV V. Aneurysm Characteristics Of the 211 ruptured wide-necked intracranial aneurysms, 203 (96.2%) were in the anterior circulation, and eight (3.8%) were in the posterior circulation. Published online before print 10.1148/radiol.2015140974 Content code: Radiology 2015; 276:545 552 Abbreviations: MCA = middle cerebral artery MRS = modified Rankin Scale SACP = stent-assisted coil placement Author contributions: Guarantors of integrity of entire study, P.Y., K.Z., L.Z., Y.X., Q.H., J.L.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; agrees to ensure any questions related to the work are appropriately resolved, all authors; literature research, P.Y., K.Z., Y.Z., R.Z., W.Z., Q.H., T.K.; clinical studies, P.Y., K.Z., Y.Z., R.Z., L.Z., W.Z., B.H., Y.X., Q.H., J.L.; experimental studies, R.Z., W.Z.; statistical analysis, P.Y., K.Z., R.Z., W.Z., T.K.; and manuscript editing, P.Y., R.Z., W.Z., Q.H., T.K., J.L. Conflicts of interest are listed at the end of this article. 546 radiology.rsna.org n Radiology: Volume 276: Number 2 August 2015

Figure 1 Figure 1: Flowchart shows the process of patient selection according to the inclusion and exclusion criteria. SAH = subarachnoid hemorrhage. The aneurysm size (maximal aneurysm diameter) ranged from 1.0 to 28.1 mm (median, 6.4 mm). It was up to 3 mm in 40 aneurysms (19.0%), 3 10 mm in 151 aneurysms (71.6%), 10 25 mm in 19 aneurysms (9.0%), and more than 25 mm in one aneurysm (0.5%). There were 44 patients with multiple aneurysms, including 33 patients with two aneurysms, 10 patients with three aneurysms, and one patient with four aneurysms. Procedure Technique Five endovascular neurosurgeons (J.L., Y.X., B.H., Y.Z., and Q.H.), all with more than 10 years of experience, treated these patients. All patients were treated within 3 days after admission, although some were transferred to our institution with a substantial delay. All procedures were performed by using general anesthesia with a transfemoral approach and systemic heparinization, aiming for increase of the activated clotting time to a level of 2 3 over baseline. A loading dose of clopidogrel and aspirin (300 mg each) was administered orally or rectally immediately after a decision was made to perform SACP. A 6-F guiding catheter was inserted into the distal internal carotid artery or vertebral artery, as appropriate. All microcatheters, stents, and coils were delivered through this catheter. Stents were deployed according to standard procedure, as recommended by the manufacturer. Two different stent placement strategies were used in this series: (a) Stent placement was achieved before coil placement, which means that the stent was implanted first to bridge the wide aneurysm neck, followed by coil placement; and (b) stent placement was achieved after coil placement, which means that some or part of the coils were introduced into the aneurysm sac before implanting the stent. If acute thrombosis occurred during the procedure, glycoprotein IIb/ IIIa inhibitor (Tirofiban; Grand Pharma, Wuhan, China) was used (Fig 2). The immediate angiographic results were evaluated by two authors independently (P.Y. and R.Z., all with 7 years of experience) using Raymond classification. Postprocedural Anticoagulation and Antiplatelet Management Until 2010, we often administered low molecular-weight heparin to the patients immediately after the procedure (40 mg every 12 hours for 3 days by means of subcutaneous injection). Because of what seemed to be an increase in the incidence of repeat bleeding in patients in which this regimen was used, which was noted when we performed a retrospective review of our data in February 2010, we discontinued the use of postprocedural anticoagulation therapy. All patients were maintained by means of aspirin (300 mg daily) and clopidogrel (75 mg daily) for 6 weeks, followed by aspirin alone (100 mg daily), which was continued indefinitely. Since 2010, thromboelastograms became available in our institution, and we found that 100 mg of aspirin alone effectively inhibited platelet aggregation. Since June 2010, the postprocedural antiplatelet regimen has been aspirin 100 mg daily and clopidogrel 75 mg daily for 6 weeks, followed by a 100-mg dose of aspirin daily, for an indefinite length of time. Clinical and Angiographic Follow-up All surviving patients were advised to undergo both clinical and angiographic follow-up 3, 6, and 12 months after the treatment and annually thereafter. Radiology: Volume 276: Number 2 August 2015 n radiology.rsna.org 547

Figure 2 Statistical Analysis Statistical analysis was performed by using SPSS version 17.0 software (SPSS, Chicago, Ill) by one author (K.Z.). Potential risk factors related to the complications and unfavorable outcome (patient age and sex, Hunt and Hess score, aneurysm location and size, interval from subarachnoid hemorrhage to treatment, stent placement strategy, type of stent used, immediate embolization degree, use of low molecularweight heparin after the procedure, and treatment experience) were categorized and analyzed in Tables 1 and 2. Mann-Whitney U tests were used for non normally distributed but continuous variables. Pearson x 2 or Fisher exact tests were used for categorical variables. Univariate analysis was performed to determine the association of procedurerelated complications and unfavorable outcome with potential risk factors. Logistic regression analysis was performed to determine the independent association of unfavorable outcome with these factors. The univariate analysis cutoff for inclusion in the logistic regression analysis was P,.20. The level of statistical significance was set at.05. Results Figure 2: Working angiographic projection images show, A, a ruptured anterior communicating artery aneurysm. Coil placement alone was attempted to treat this aneurysm. B, However, coil protrusion into the right A2 segment (arrow) occurred during the procedure, which required salvaging stent placement. C, Intrastent thrombosis (arrow) was noted immediately after stent placement, which, D, resolved 40 minutes after using Tirofiban (Grand Pharma) intravenously. The clinical outcome evaluations were based on the modified Rankin Scale (MRS). Good outcomes were defined as an MRS score of 0 2; poor outcomes were defined as an MRS score of 3 6. The angiographic follow-up results obtained with digital subtraction angiography were classified into four categories when compared with the immediate embolization degree: (a) occluded, defined as no contrast material filling into the aneurysm sac; (b) improved, defined as decreased contrast material filling into the aneurysm sac; (c) stable, defined as unchanged contrast material filling into the aneurysm sac; or (d) recanalized, defined as increased contrast material filling into the aneurysm sac. The same two physicians who evaluated the immediate posttreatment angiographic results also evaluated the angiographic follow-up studies. Immediate Embolization Results A total of 230 stents were implanted. These included 14 (6.1%) balloon expandable stents, 74 (32.2%) Neuroform (Stryker, Kalamazoo, Mich) stents, nine (3.9%) LEO (Balt) stents, 124 (53.9%) Enterprise (Codman, Johnson & Johnson, Miami, Fla) stents, and nine (3.9%) Solitaire (ev3/coviden, Irvine, Calif) stents. Sixty-six of 211 aneurysms (31.3%) were treated by using the stent placement before coil placement technique, while the other 145 aneurysms (68.7%, 145 of 211) were treated by using the stent placement after coil placement technique. Ninetysix of the 211 aneurysms (45.5%) were completely occluded immediately (Raymond class I), 35 (16.6%, 35 of 211) had a residual neck (Raymond class II), and 80 (37.9%, 80 of 211) had a residual sac (Raymond class III). 548 radiology.rsna.org n Radiology: Volume 276: Number 2 August 2015

Complications Procedure-related complications occurred in 30 patients (14.2%, 30 of 211). Twenty of these (9.5%, 20 of 211) resulted in either death (4.7%, 10 of 211) or permanent neurologic deficits (4.7%, 10 of 211). The other 10 (4.7%, 10 of 211) caused no permanent morbidity. Seventeen (8.1%, 17 of 211) of the complications were due to ischemic events (eight acute in-stent thrombus formations, five thromboembolic events, three branch occlusions, and one carotid dissection), and 13 (6.2%, 13 of 211) were due to hemorrhagic events (nine intraoperative aneurysm ruptures and four cases of early repeat bleeding). Statistical analysis demonstrated that procedure-related ischemic events were correlated with the location of the aneurysms (P =.030). Intraoperative aneurysm rupture was also correlated with the location of the aneurysms (P =.014), as well as the immediate embolization degree (P =.027). Early repeat bleeding was correlated with both the immediate embolization degree (P =.035) and the postoperative use of heparin (P =.021). Patients with MCA bifurcation and anterior communicating artery aneurysms were more likely to have experienced a higher incidence of complications than those with aneurysms in the other locations (P =.003) (Table 1). Angiographic Follow-up One hundred ninety patients survived the initial subarachnoid hemorrhage. Of those, 152 patients with 152 aneurysms (80.0%) underwent angiographic follow-up at least once, ranging from 3 to 77 months (median, 12 months). Follow-up angiograms showed that 115 aneurysms (75.6%, 115 of 152 aneurysms) were occluded, 13 (8.6%, 13 of 152 aneurysms) were improved, 16 (10.5%, 16 of 152 aneurysms) were stable, and eight (5.3%, eight of 152) were recanalized. All parent arteries were patent without clinically significant in-stent stenosis. Clinical Outcome Twenty-one patients died. Two of these resulted from postoperative early repeat Figure 3 Figure 3: A, Working angiographic projection image shows a ruptured wide-necked multilobular posterior communicating artery aneurysm. The aneurysm was treated by using SACP (LEO; Balt, Montmorency, France). B, Angiogram of the immediate result shows the residual neck of the sac. C, D, Follow-up angiograms obtained at 7 months and 42 months show complete occlusion of the aneurysm. bleeding, four resulted from perioperative aneurysm perforation, four resulted from large cerebral infarction, and 11 resulted from initial subarachnoid hemorrhage. Clinical evaluation was performed for the other 190 patients at discharge by using MRS, 147 (69.7%, 147 of 211 patients) of whom were independent (MRS scores of 0 2), while the other 43 were dependent (MRS scores of 3 5). All 190 surviving patients underwent clinical follow-up after discharge at intervals between 6 and 77 months (median, 33 months). These evaluations showed that 175 patients (82.9%, 175 of 211) had a good outcome (MRS scores of 0 2). During the follow-up period, six patients died of unrelated causes. Statistical analysis demonstrated that older age (P =.013; odds ratio, 1.054) and higher Hunt and Hess grade (P,.001; odds ratio, 15.876) were independent risk factors for poor clinical outcome (Table 2). Discussion In this single-center series of 211 consecutive cases, the procedure-related complication rate was modest at approximately 14%. The immediate rate of complete angiographic occlusion approached 50% and increased to 75% during follow-up. A good clinical outcome was achieved in more than 80% of patients. These results suggest that SACP for the treatment of acutely ruptured wide-necked intracranial aneurysms has good durability, with reasonable complication rates. The procedure-related complication rate in our current study is in line with those reported previously in several similar studies, which have ranged from 10% to 30% (5,6,9 13). Although these complication rates for SACP in ruptured aneurysms are higher than those reported for SACP in unruptured aneurysms (14 16), they are similar to those of balloon-assisted coil placement (17) and, according to some prior literature, even Radiology: Volume 276: Number 2 August 2015 n radiology.rsna.org 549

Table 1 Potential Risk Factors Related to Procedure-related Complications Ischemic Events (n = 17) Intraoperative Rupture (n = 9) Early Repeat Bleeding (n = 4) Cumulative Adverse Events (n = 30) Variable Yes No P Value Yes No P Value Yes No P Value Yes No P Value Median age (y) 62 56.846* 54 56.506* 62 56.396* 58 56.922* Sex.855..99.569.857 Men 5 (10) 47 (90) 2 (4) 50 (96) 0 (0) 52 (100) 7 (13) 45 (87) Women 12 (8) 147 (92) 7 (4) 152 (96) 4 (3) 155 (97) 23 (14) 136 (86) Hunt and Hess grade..99..99..99.507 Grade I III 16 (8) 178 (92) 9 (5) 185 (95) 4 (2) 190 (98) 29 (15) 165 (85) Grade IV V 1 (6) 16 (94) 0 (0) 17 (0) 0 (0) 17 (100) 1 (6) 16 (94) Location.030.014.675.003 Anterior communicating artery 8 (18) 37 (82) 4 (9) 41 (91) 0 (0) 45 (100) 12 (27) 33 (73) Middle cerebral artery (MCA) bifurcation 2 (20) 8 (80) 2 (20) 8 (80) 0 (0) 10 (100) 4 (40) 6 (60) Posterior communicating artery 3 (3) 85 (97) 2 (2) 86 (98) 2 (2) 86 (98) 7 (8) 81 (92) Other 4 (6) 64 (94) 1 (1) 67 (99) 2 (3) 66 (97) 7 (10) 61 (90) Aneurysm size.967.803.436.863 Tiny (,3 mm) 3 (8) 37 (92) 2 (5) 38 (95) 2 (5) 38 (95) 7 (18) 33 (82) Small (3 10 mm) 12 (8) 139 (92) 7 (5) 144 (95) 2 (1) 149 (99) 21 (14) 130 (86) Large (10 25 mm) 2 (11) 17 (89) 0 (0) 19 (100) 0 (0) 19 (100) 2 (11) 17 (89) Giant ( 25 mm) 0 (0) 1 (100) 0 (0) 1 (100) 0 (0) 1 (100) 0 (0) 1 (100) Treatment interval.098.245.399.762 3 d 8 (9) 83 (91) 3 (3) 88 (97) 3 (3) 88 (97) 14 (15) 77 (85) 3 14 d 4 (4) 86 (96) 6 (7) 84 (93) 1 (1) 89 (99) 11 (12) 79 (88) 15 28 d 5 (17) 25 (83) 0 (0) 30 (100) 0 (0) 30 (100) 5 (17) 25 (83) Stent placement strategy.710..99..99.793 Stent placement before coiling 6 (9) 60 (91) 3 (5) 63 (95) 1 (2) 65 (98) 10 (15) 56 (85) Stent placement after coiling 11 (8) 134 (92) 6 (4) 139 (96) 3 (2) 142 (98) 20 (14) 125 (86) Type of stent..99..99..99.698 Balloon-expanding stents 1 (7) 13 (93) 0 (0) 14 (100) 0 (0) 14 (100) 1 (7) 13 (93) Self-expanding stents 16 (8) 181 (92) 9 (5) 188 (95) 4 (2) 193 (98) 29 (15) 168 (85) Immediate embolization degree.972.027.035.211 Complete occlusion 8 (8) 88 (92) 8 (8) 88 (92) 0 (0) 96 (100) 16 (17) 80 (83) Residual neck 3 (9) 32 (91) 0 (0) 35 (100) 0 (0) 35 (100) 3 (9) 32 (91) Residual aneurysm 6 (8) 74 (92) 1 (1) 79 (99) 4 (5) 76 (95) 11 (14) 69 (86) Use of low molecular-weight heparin after procedure.503.347.021.864 Yes 7 (10) 65 (90) 5 (7) 67 (93) 4 (6) 68 (94) 16 (22) 56 (78) No 10 (7) 129 (93) 4 (3) 135 (97) 0 (0) 139 (100) 14 (10) 125 (90) Treatment experience.363.769..99.607 Early phase (first 50 cases) 2 (4) 48 (96) 3 (6) 47 (94) 1 (2) 49 (98) 6 (12) 44 (88) Late phase (the other cases) 15 (9) 146 (91) 6 (4) 155 (96) 3 (2) 158 (98) 24 (15) 137 (85) Note. Unless indicated otherwise, data are number of cases, with percentages in parentheses. * According to the Mann-Whitney U test. According to the Pearson x 2 or Fisher exact test. 550 radiology.rsna.org n Radiology: Volume 276: Number 2 August 2015

Table 2 Potential Risk Factors Related to Unfavorable Outcomes Variable Favorable Outcome (n = 175) unassisted coil placement in ruptured aneurysms (18). Although the immediate rate of complete angiographic occlusion in our series seems to be slightly lower than that reported by using balloonassisted coil placement techniques (17), Unfavorable Outcome (n = 36) Total (n = 211) P Value Logistic Regression P Value Median age (y) 55 64 56,.001*.002 (1.061) [1.022, 1.101] Patient sex.100 Men 47 (90) 5 (10) 52 Women 128 (81) 31 (19) 159 Hunt and Hess grade,.001,.001 (13.389) [4.291, 41.779] Grade I III 169 (87) 25 (13) 194 Grade IV V 6 (35) 11 (65) 17 Location.895 Anterior communicating artery 37 (82) 8 (18) 45 MCA bifurcation 8 (80) 2 (20) 10 Posterior communicating artery 75 (85) 13 (15) 88 Other 55 (81) 13 (19) 68 Aneurysm size.060 Tiny (,3 mm) 36 (90) 4 (10) 40 Small (3 10 mm) 125 (83) 26 (17) 151 Large (10 25 mm) 14 (74) 5 (26) 19 Giant ( 25 mm) 0 (0) 1 (100) 1 Treatment interval,.001 3 d 64 (70) 27 (30) 91 3 14 d 83 (92) 7 (8) 90 15 28 d 28 (93) 2 (7) 30 Stent placement strategy Stent placement before coil 54 (82) 12 (18) 66.806 placement Stent placement after coil 121 (83) 24 (17) 145 placement Type of stent..99 Balloon-expanding stents 12 (86) 2 (14) 14 Self-expanding stents 163 (83) 34 (17) 197 Immediate embolization degree.132 Complete occlusion 77 (80) 19 (20) 96 Residual neck 33 (94) 2 (6) 35 Residual aneurysm 65 (80) 15 (20) 80 Treatment experience Early phase (first 50 cases) 40 (80) 10 (20) 50.907 Late phase (the other cases) 130 (81) 31 (19) 161 Note. Unless indicated otherwise, data are number of cases, with percentages in parentheses. * According to the Mann-Whitney U test. Numbers in parentheses are the odds ratio. Numbers in brackets are the 95% confidence interval. P values were obtained with binary logistic regression. According to the Pearson x 2 or Fisher exact test. it is noteworthy that at short-term follow-up, SACP has shown good durability, with a high complete occlusion rate (Fig 3). This is consistent with the study of Jahshan et al, which showed a higher rate of complete occlusion during follow-up by using SACP as compared with simple coil placement (16). Although truly longterm follow-up data are not available in our study, the follow-up data that are available show a comparable rate of complete angiographic occlusion than that reported for these other techniques. If this durability of occlusion is documented in studies with angiographic follow-up of longer duration, this would add further reasons to consider SACP as a treatment option for these difficult aneurysms. The rate of good clinical outcome is comparable to the 1-year clinical outcome for patients with ruptured aneurysms in the randomized International Subarachnoid Aneurysm Trial (76%) (19) and the Barrow Ruptured Aneurysm Trial (80%) (20), as well as the meta-analysis (77%) conducted by Li et al (18). These results seem to indicate that, for aneurysms such as those in our study, SACP may achieve clinical outcomes similar to those reported in the treatment of aneurysms that can usually be treated without the need for adjunctive techniques and are also most likely not as morphologically complex as those in our series. Therefore, in our series of 211 patients with acutely ruptured widenecked aneurysms, the results achieved by using SACP were comparable to those reported by using simple coil placement or balloon-assisted coil placement. In our series, the incidence of repeat bleeding was 1.9%, which was significantlyy related to posttreatment anticoagulation therapy and incomplete aneurysm occlusion immediately. This is comparable to the incidence reported in other series, where dual antiplatelet therapy was either not used or could not be correlated with repeat bleeding (21 23). These observations may indicate that the use of dual antiplatelet therapy in patients treated with SACP may not put them at undue risk of repeat bleeding. Although in our series, the use of dual antiplatelet therapy was not associated with bleeding in patients who underwent placement of a ventricular drain, the study of Kung et al showed that this risk is approximately three times higher than that without dual antiplatelet medication (24). Only six patients in our series underwent ventricular drainage. This is because we prefer Radiology: Volume 276: Number 2 August 2015 n radiology.rsna.org 551

to treat patients with an acutely ruptured wide-necked aneurysm who are likely to require open surgical procedures as a part of their care by using either surgical clipping or staged SACP with initial dome protection and then stent placement and final coil placement delayed for 1 month after hemorrhage. This study has two major limitations. First, selection bias derived from our exclusion criteria precluded the ability to generalize our results to ruptured widenecked aneurysms in general. Second, our study was also limited in this regard because of the long time period over which our series was performed, as well as the variety of stents that were used during this interval. In conclusion, our experience demonstrates that SACP for the treatment of selected acutely ruptured wide-necked intracranial aneurysms can achieve results comparable to those reported by using traditional coil placement or balloonassisted coil placement techniques. Our angiographic follow-up data, although not long term, showed an improved rate of aneurysm occlusion than has been reported by using other techniques. The higher incidence of procedural complications observed in the treatment of MCA bifurcation and the anterior communicating artery aneurysms has made us adopt a conservative approach for choosing SACP as a technique for the treatment of these aneurysms. Acknowledgments: The authors thank Charles Strother, MD (neuroradiologist), and Alejandro Munoz del Rio, PhD (biostatistician), at the Department of Radiology of University of Wisconsin Madison for pertinent revisions. Disclosures of Conflicts of Interest: P.Y. disclosed no relevant relationships. K.Z. disclosed no relevant relationships. Y.Z. disclosed no relevant relationships. R.Z. disclosed no relevant relationships. L.Z. disclosed no relevant relationships. W.Z. disclosed no relevant relationships. B.H. disclosed no relevant relationships. Y.X. disclosed no relevant relationships. Q.H. disclosed no relevant relationships. T.K. disclosed no relevant relationships. J.L. disclosed no relevant relationships. References 1. Moret J, Cognard C, Weill A, Castaings L, Rey A. The remodelling technique in the treatment of wide neck intracranial aneurysms. Angiographic results and clinical follow-up in 56 cases. Interv Neuroradiol 1997;3(1):21 35. 2. Baxter BW, Rosso D, Lownie SP. Double microcatheter technique for detachable coil treatment of large, wide-necked intracranial aneurysms. AJNR Am J Neuroradiol 1998;19(6):1176 1178. 3. Ihn YK, Kim DI, Kim BS, Lee JM. Utility of catheter-assisted Guglielmi detachable coiling in the treatment of wide-necked aneurysms. Acta Neurochir (Wien) 2006; 148(10):1045 1052; discussion 1052. 4. 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. 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Kung DK, Policeni BA, Capuano AW, et al. Risk of ventriculostomy-related hemorrhage in patients with acutely ruptured aneurysms treated using stent-assisted coiling. J Neurosurg 2011;114(4):1021 1027. 552 radiology.rsna.org n Radiology: Volume 276: Number 2 August 2015

Note: This copy is for your personal non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at www.rsna.org/rsnarights. LETTERS TO THE EDITOR 5. Nyanta SJ, Sherman ME, Pfeiffer RM, et al. Prognostic significance of mammographic density change after initiation of tamoxifen for ER-positive breast cancer. J Natl Cancer Inst doi: 10.1093/jnci/dju425. Published online February 6, 2015. Accessed March 13, 2015. 6. Daniels J, Harkness E, Lim Y, et al. How does volumetric breast density change with time? Breast Cancer Res 2014;16(Suppl 1):P38. Errata Originally published in: Radiology 2015;276(2):536 544 DOI: 10.1148/radiol.15141251 Prognostic Value of Cervical Nodal Necrosis in Nasopharyngeal Carcinoma: Analysis of 1800 Patients with Positive Cervical Nodal Metastasis at MR Imaging Mei Lan, Ying Huang, Chun-Yan Chen, Fei Han, Shao-Xiong Wu, Li Tian, Lie Zheng, Tai-Xiang Lu Erratum in: Radiology 2015;276(2):619 DOI:10.1148/radiol.15154020 In the Abstract, the fourth sentence of the Results section should read as follows: Subgroup analysis revealed similar survival outcomes between stage N1 disease with CNN and stage N2 disease without CNN, stage N2 disease with CNN, and stage N3 disease regardless of CNN. This correction applies only to an early online version of the article; final print and online versions of the article are correct. Originally published in: Radiology 2015;276(2):545 552 DOI:10.1148/radiol.2015140974 Stent-assisted Coil Placement for the Treatment of 211 Acutely Ruptured Wide-necked Intracranial Aneurysms: A Single-Center 11-Year Experience Pengfei Yang, Kaijun Zhao, Yu Zhou, Rui Zhao, Lei Zhang, Wenyuan Zhao, Bo Hong, Yi Xu, Qinghai Huang, Timo Krings, and Jianmin Liu Erratum in: Radiology 2015;276(2):619 DOI:10.1148/radiol.2015154025 An early online version of the article was incorrect. Page 548, Figure 2 caption should read as follows: Figure 2: Working angiographic projection images show, A, a ruptured anterior communicating artery aneurysm. Coil placement alone was attempted to treat this aneurysm. B, However, coil protrusion into the right A2 segment (arrow) occurred during the procedure, which required salvaging stent placement. C, Intrastent thrombosis (arrow) was noted immediately after stent placement, which, D, resolved 40 minutes after using Tirofiban (Grand Pharma) intravenously. Page 549, Figure 3 caption should read as follows: Figure 3: A, Working angiographic projection image shows a ruptured wide-necked multilobular posterior communicating artery aneurysm. The aneurysm was treated by using SACP (LEO; Balt, Montmorency, France). B, Angiogram of the immediate result shows the residual neck of the sac. C, D, Follow-up angiograms obtained at 7 months and 42 months show complete occlusion of the aneurysm. Radiology: Volume 276: Number 2 August 2015 n radiology.rsna.org 619