Abstract
Introduction
Although approximately one in every 10 patients undergoing coil embolization of intracranial aneurysms requires retreatment, the factors that are associated with outcome following retreatment remain to be fully elucidated.
Methods
This is a single-center, retrospective review of 43 patients with 58 intracranial aneurysms that were retreated from 2004 to 2014. Aneurysms undergoing first time or microsurgical retreatment were excluded. Retreatment types were grouped into those without permanent parent vessel support (stand-alone and balloon-assisted coiling) versus those with permanent parent vessel support (stent-assisted coiling, stand-alone stenting, and flow diversion). The Modified Raymond Roy Classification was used to group aneurysms at all angiographic follow-up points either in the successful outcome group (Class I or II) or the unsuccessful outcome group (Class IIIa or IIIb).
Results
Of aneurysms with follow-up, 50% were in the successful group and 50% in the unsuccessful group. In univariate analysis, small aneurysm size (p < 0.001), previous treatment type (p = 0.022), retreatment type (p = 0.001), and initial occlusion class (p = 0.005) were all associated with angiographic outcome. In multivariate analysis, small aneurysm size (p = 0.005, odds ratio (OR) 24.56, confidence interval (CI) 2.68–225.4) and retreatment type with permanent parent vessel support, namely stent-assisted coiling (p = 0.017, OR 31.1, CI 1.89–517.7), were associated with retreatment success.
Conclusions
Small aneurysm size and retreatment with permanent parent vessel support, namely stent-assisted coiling, are predictors of success following endovascular retreatment of intracranial aneurysms. These findings could be useful in the effort to both prevent and predict treatment failure following endovascular retreatment.
Keywords: Intracranial aneurysm, endovascular retreatment
Introduction
Coil embolization has been used increasingly over the last two decades for the treatment of intracranial aneurysms. Incomplete occlusion, aneurysm recurrence, and the need for retreatment, however, continue to be disadvantages of this approach.1,2 A recent systematic review estimated that the overall recurrence and retreatment rate following coil embolization were 20.8% and 10.3%, respectively.3 There are limited data evaluating the factors that influence angiographic outcome following endovascular retreatment. The purpose of this study was to determine the patient, aneurysm, and procedural factors that are associated with successful or unsuccessful angiographic outcome following endovascular retreatment of intracranial aneurysms.
Methods
IRB approval was obtained for this study. We performed a retrospective analysis of 43 patients with 58 intracranial aneurysms that underwent endovascular retreatment at a single center from 2004 to 2014. All types of aneurysms and endovascular retreatments were included except endovascular parent vessel occlusion following surgical bypass. Patients undergoing first time treatment and those undergoing microsurgical retreatment were excluded.
Aneurysmal and subject characteristics were determined by review of both subject's medical chart and angiographic data. Aneurysm size was based on maximum diameter of the entire aneurysm (not just the filling portion): small (<10 mm), large (10–25 mm), and giant (>25 mm). Specific dome and neck measurements (and therefore packing density as well) were not included given that the geometry of residual aneurysm was frequently non-uniform. Aneurysm location was determined by angiographic review. Posterior communicating artery aneurysms were included in the anterior circulation.
Retreatment types included stand-alone coiling (n = 34), balloon-assisted coiling (n = 3), stent-assisted coiling (n = 16), stand-alone stenting (n = 3), and flow diversion (n = 2). Coil types included Galaxy (Codman), GDC (Stryker), Hydrocoil (Microvention), Orbit (Codman), Penumbra (Penumbra), Target (Stryker), and Trufill (Codman). Stent types included Enterprise (Codman), Liberty (Penumbra), and Neuroform (Stryker). Flow diverters included Pipeline Embolization Device (EV3). Retreatment types were grouped into those without permanent parent vessel support (stand-alone and balloon-assisted coiling) versus those with permanent parent vessel support (stent-assisted coiling, stand-alone stenting, and flow diversion).
All initial and follow-up angiograms were reviewed and graded using the Modified Raymond-Roy Occlusion Classification (MRRC),4 which is slightly different than the traditional Raymond Roy Occlusion Classification (RROC).5 In this system, Class IIIa designates contrast within the coil interstices and Class IIIb designates contrast outside the coil mass/along the aneurysm wall. Retreatment success was defined as complete aneurysm occlusion (Class I) or neck remnant (Class II) at all follow-ups (n = 22). Retreatment failure was defined as residual filling of the aneurysm dome (Class IIIa or IIIb) at any follow-up (n = 22). Class II aneurysms were grouped with the Class I aneurysms, as the experience at our institution is that Class II aneurysms behave more like Class I than Class III aneurysms and rarely require retreatment.6 A Class IIIa designation immediately after the procedure has been shown to be predictive of progression to thrombosis and is therefore considered an acceptable immediate result.4 A Class IIIa designation at follow-up, however, is considered to be a treatment failure because there is persistent dome filling.
Differences in pre-treatment variable distribution between groups were assessed using the Mann–Whitney test or chi-square test for continuous and categorical variables respectively. The significant results on univariate analysis were subsequently incorporated into a multivariable logistic regression model to measure their combined effect at follow-up angiography. Backward likelihood ratio testing was used to construct a final logit model. Fit lines were constructed utilizing least squares regression to investigate linear relationships between treatment variables and outcomes. All reported P values are two sided with a standard alpha set at 0.05. All ranges were reported as interquartile range (IQR), and plus-minus values are reported as mean ± one standard deviation (SD). All data management and analyses were conducted using SPSS 20.0 (IBM, Inc., Armonk, NY).
Results
Patient, aneurysm, and procedure characteristics
The majority of patients were female (89.6%) with an average age of 53.6 years. The majority of aneurysms were unruptured at the time of retreatment (94.8%), of which 40.0% were ruptured at the time of initial treatment (Table 1). The majority of aneurysms were located in the anterior circulation (87.9%) and were large (53.5%; Table 2). All patients underwent previous treatment, including stand-alone coiling (65.5%), stent-assisted coiling (23.1%), stand-alone stenting (5.2%), and surgical clipping (9.6%). Retreatment types included stand-alone coiling (58.6%), balloon-assisted coiling (5.2%), stent-assisted coiling (27.6%), stand-alone stenting (5.2%), and flow diversion (3.4%; Table 3). Almost all of the patients treated with coils were treated with bare platinum coils (98.1%). The most common stent used was the Enterprise Stent (79%). The majority of patients underwent only one retreatment (89.7%); the rest underwent two (5.2%), three (1.7%), and four (3.4%) retreatments.
Table 1.
Patient characteristics.
| Total (n = 58) | Successful (n = 22) | Unsuccessful (n = 22) | p Value | |
|---|---|---|---|---|
| Gender – n (%) | 0.294 | |||
| Female | 52 (89.6) | 21 (53) | 19 (47) | |
| Male | 6 (10.3) | 1 (25) | 3 (75) | |
| Age (yrs) | 53.6 | 50.9 | 55.0 | 0.152 |
| Presentation at retreatment – n (%) | 0.312 | |||
| SAH | 3 (5.2) | 0 (0) | 1 (100) | |
| Unruptureda | 55 (94.8) | 22 (51) | 21 (49) |
40.0% of the unruptured aneurysms were initially ruptured.
Table 2.
Aneurysm characteristics.
| Total (n = 58) | Successful (n = 22) | Unsuccessful (n = 22) | p Value | |
|---|---|---|---|---|
| Aneurysm location – n (%) | 0.374 | |||
| Anterior circulation | 51 (87.9) | 21 (53) | 19 (47) | |
| Petrous | 1 (1.7) | 0 (0) | 0 (0) | |
| Cavernous | 5 (8.6) | 1 (25) | 3 (75) | |
| Ophthalmic | 9 (15.5) | 3 (43) | 4 (57) | |
| Superior hypophyseal | 8 (13.8) | 3 (38) | 5 (62) | |
| Posterior communicating | 12 (20.7) | 3 (43) | 4 (57) | |
| Anterior choroidal | 1 (1.7) | 1 (100) | 0 (0) | |
| ICA dorsal wall | 5 (8.6) | 3 (75) | 1 (25) | |
| ICA bifurcation | 1 (1.7) | 1 (100) | 0 (0) | |
| ICA other | 1 (1.7) | 0 (0) | 1 (100) | |
| Anterior communicating | 3 (5.2) | 3 (100) | 0 (0) | |
| MCA | 5 (8.6) | 3 (75) | 1 (25) | |
| Posterior circulation | 7 (12.1) | 1 (25) | 3 (75) | |
| Vertebral–basilar junction | 1 (1.7) | 0 (0) | 0 (0) | |
| Basilar tip | 6 (10.3) | 1 (25) | 3 (75) | |
| Aneurysm size – n (%) | <0.001 | |||
| Small (<10 mm) | 23 (39.7) | 16 (89) | 2 (11) | |
| Large (10–25 mm) | 31 (53.5) | 5 (23) | 17 (77) | |
| Giant (>25 mm) | 4 (6.9) | 1 (25) | 3 (75) |
Table 3.
Procedure characteristics.
| Total (n = 58) | Successful (n = 22) | Unsuccessful (n = 22) | p Value | |
|---|---|---|---|---|
| Previous treatment – n (%) | 0.022 | |||
| Stand-alone coiling | 38 (65.5) | 15 (54) | 13 (46) | |
| Stent-assisted coiling or stand-alone stenting | 15 (28.3) | 4 (33) | 8 (67) | |
| Clipping | 5 (9.6) | 3 (75) | 1 (25) | |
| Type of recurrence/residual – n (%) | 0.111 | |||
| Coil compaction | 23 (39.7) | 8 (44) | 10 (56) | |
| Aneurysm regrowth | 7 (12.1) | 1 (20) | 4 (80) | |
| Stable residual | 15 (25.9) | 6 (50) | 6 (50) | |
| Re-rupture | 3 (5.2) | 0 (0) | 1 (100) | |
| Unknown | 10 (17.2) | 7 (88) | 1 (12) | |
| Retreatment type – n (%) | 0.001 | |||
| Without permanent parent vessel supporta | 37 (63.8) | 10 (33) | 20 (67) | |
| With permanent parent vessel supportb | 21 (36.3) | 12 (86) | 2 (14) |
Stand-alone and balloon-assisted coiling.
Stent-assisted coiling, stand-alone stenting, and flow diversion.
Angiographic outcome
Forty-four of 58 aneurysms (75.9%) had at least one angiographic follow-up following retreatment at an average of 8.0 months (Table 4). Additionally, 44.8% of aneurysms had a second angiographic follow-up at an average of 20.9 months and 27.6% had a third angiographic follow-up at an average of 47.6 months. Twenty-two of the 44 aneurysms with follow-up (50.0%) maintained a MRRC Class I or II designation throughout follow-up and were included in the “successful” group. Twenty-two of the 44 aneurysms with follow-up (50%) had a Class IIIa or IIIb designation at some point during follow-up and were included in the “unsuccessful” group. Approximately half of the patients had complete neck coverage with coils (50.9%).
Table 4.
Angiographic outcome.
| Total (n = 58) | Successful (n = 22) | Unsuccessful (n = 22) | p Value | |
|---|---|---|---|---|
| Initial occlusion class – n (%)a | 0.005 | |||
| Class I | 16 (27.6) | 6 (67) | 3 (33) | |
| Class II | 14 (24.1) | 10 (77) | 3 (23) | |
| Class IIIa | 9 (15.5) | 4 (57) | 3 (43) | |
| Class IIIb | 19 (32.8) | 2 (13) | 13 (87) | |
| Neck coverage with coils – n (%) | 0.155 | |||
| Complete | 27 (50.9) | 12 (57) | 9 (43) | |
| Incomplete | 25 (47.2) | 7 (35) | 13 (65) | |
| Not applicable | 6 (11.5) | 3 (100) | 0 (0) |
Initial occlusion class refers to the designation immediately following the retreatment (it does not refer to the occlusion class after the initial treatment).
Statistical analysis
In univariate analysis (Table 5), small aneurysm size (p < 0.001), previous treatment type (p = 0.022), retreatment type (p = 0.001), and initial occlusion class (p = 0.005) were all associated with angiographic outcome. The significance of previous treatment was driven by previous stent-assisted coiling or stand-alone stenting being associated with retreatment failure (p = 0.021). The significance of retreatment type was driven by stent-assisted coiling being associated with retreatment success. Initial occlusion class was driven by Class II status being associated with successful retreatment (p = 0.045) and Class IIIb status being associated with unsuccessful retreatment (p = 0.001). All other factors had no association with angiographic outcome (see non-significant p values in Tables 1 to 3).
Table 5.
Summary of univariate analyses.
| Total (n = 58) | Successful (n = 22) | Unsuccessful (n = 22) | p Value | |
|---|---|---|---|---|
| Aneurysm size – n (%) | ||||
| Small (<10 mm) | 23 (39.7) | 16 (89) | 2 (11) | <0.001 |
| Large (10–25 mm) | 31 (53.5) | 5 (23) | 17 (77) | <0.001 |
| Giant (>25 mm) | 4 (6.9) | 1 (25) | 3 (75) | |
| Previous treatment – n (%) | ||||
| Stand-alone coiling | 38 (65.5) | 15 (54) | 13 (46) | 0.022 |
| Stent-assisted coiling or stand-alone stenting | 15 (28.3) | 4 (33) | 8 (67) | 0.021 |
| Clipping | 5 (9.6) | 3 (75) | 1 (25) | |
| Retreatment type – n (%) | 0.001 | |||
| Without permanent parent vessel supporta | 37 (63.8) | 10 (33) | 20 (67) | |
| With permanent parent vessel supportb | 21 (36.2) | 12 (86) | 2 (14) | |
| Initial occlusion class – n (%)c | ||||
| Class I | 16 (27.6) | 6 (67) | 3 (33) | 0.005 |
| Class II | 14 (24.1) | 10 (77) | 3 (23) | 0.045 |
| Class IIIa | 9 (15.5) | 4 (57) | 3 (43) | 0.001 |
| Class IIIb | 19 (32.8) | 2 (13) | 13 (87) |
Stand-alone and balloon-assisted coiling.
Stent-assisted coiling, stand-alone stenting, and flow diversion.
Initial occlusion class refers to the designation immediately following the retreatment (it does not refer to the occlusion class after the initial treatment).
In multivariate analysis (Table 6), small aneurysm size (p = 0.005, odds ratio (OR) 24.56, confidence interval (CI) 2.68–225.4) and retreatment type with permanent parent vessel support, namely stent-assisted coiling (p = 0.017, OR 31.1, CI 1.89–517.7), were associated with retreatment success. Previous treatment type (p = 0.759) and initial occlusion class (p = 0.068) were not associated with angiographic outcome in multivariate analysis, although the latter approached statistical significance.
Table 6.
Multivariate model of successful retreatment.
| Patient characteristica | Multivariate p value | Odds ratio (multivariate 95% CI) |
|---|---|---|
| Previous treatment typeb | 0.759 | 0.69 (0.07–7.27) |
| Aneurysm sizec | 0.005 | 24.56 (2.68–225.4) |
| Retreatment typed | 0.017 | 31.1 (1.89–517.7) |
| Initial occlusion classe | 0.068 | 10.3 (0.84–127.04) |
Significant p values in bold. Model was built using logistic regression including all variables significant on univariate analysis. Due to the small sample size, variables were binarized prior to analysis.
Stand-alone coiling vs. others.
Small vs. large/giant.
With permanent parent vessel support (stent-assisted coiling, stand-alone stenting, and flow diversion) vs. without permanent parent vessel support (stand-alone and balloon-assisted coiling).
Class I, II, & IIIa vs. IIIb.
Clinical outcomes
As shown in Table 7, there was no difference in complications between the successful and unsuccessful cohorts (p = 0.393) and there was no difference in morbidity or mortality secondary to the complication (p = 0.488). There was no difference in Modified Rankin Score (mRS) at discharge (p = 0.724) or at follow-up (p = 0.766). There were more subsequent retreatments in the unsuccessful group (p < 0.001).
Table 7.
Clinical characteristics.
| Total (n = 58) | Successful (n = 22) | Unsuccessful (n = 22) | p Value | |
|---|---|---|---|---|
| Complications – n (%) | 5 (8.6) | 3 (75) | 1 (25) | 0.393 |
| Vessel compromise | 1 (1.7) | 1 (100) | 0 (0) | |
| Vessel dissection | 1 (1.7) | 0 (0) | 1 (100) | |
| Embolus | 1 (1.7) | 1 (100) | 0 (0) | |
| Inability to coil | 2 (3.5) | 1 (100) | 0 (0) | |
| Result of complication – n (%) | 0.488 | |||
| Morbidity | 1 (1.7) | 1 (100) | 0 (0) | |
| Mortality | 0 (0.0) | 0 (0) | 0 (0) | |
| Discharge mRS – n (%) | 0.724 | |||
| Good (0 – 2) | 36 (77.6) | 15 (48) | 16 (52) | |
| Poor (3 – 6) | 9 (20.0) | 2 (40) | 3 (60) | |
| Follow-up mRS – n (%) | 0.766 | |||
| Good (0–2) | 37 (90.2) | 16 (50) | 16 (50) | |
| Poor (3–6) | 4 (9.8) | 1 (25) | 3 (70) | |
| Further retreatment – n (%) | 11 (19.0) | 0 (0) | 11 (100) | <0.001 |
Discussion
Endovascular retreatment is not uncommon for incompletely occluded or recurrent intracranial aneurysms. Retreatment of these aneurysms is justified given that incomplete aneurysm occlusion has been associated with a higher, albeit small, risk of subsequent rupture.7 While many have investigated outcome following primary aneurysm treatment, there have been fewer studies that focus on outcome following aneurysm retreatment,8–18 and even fewer that aim to identify factors associated with successful or unsuccessful retreatment.12,13,15,16
Our study identified small aneurysm size and retreatment with permanent parent vessel support, namely stent-assisted coiling, to be associated with successful angiographic outcome. Although aneurysm regrowth (versus coil compaction) has previously been identified as a risk factor for retreatment failure,13 our study failed to reproduce this finding. It is not surprising that small aneurysm size is associated with successful retreatment. Many previous studies have demonstrated that larger aneurysm size is a significant risk factor for primary treatment failure.3,19–25 The relationship between aneurysm size and outcome after retreatment has not been described previously but is intuitive.
Stent assistance for primary treatment has also been studied in detail. While some studies have found only equivocal results compared to stand-alone coiling,26–29 more have found improved results.30–35 Lawson et al. found that stent assisted coiling not only led to fewer recurrences but also more aneurysms that progressed to occlusion.30 A systematic review published in 2013 demonstrated a recanalization rate of 13.2% for stent assisted coiling,34 an improvement compared to the 20.8% of stand-alone coiling.3 A meta-analysis published in 2014 demonstrated a significantly improved recurrence rate compared to stand-alone coiling (16.2% vs. 34.4%).35
Less attention has been paid to the angiographic results following stent-assisted coiling of recurrent aneurysms. Cho et al evaluated 162 patients with 197 recanalized intracranial aneurysms that were retreated at their institution. Stent assistance was utilized for 68 of these aneurysms. The procedural complication rate was 7.6% without permanent neurological sequelae. The major recanalization rate was 34.3%. In a multivariate logistic regression analysis, they demonstrated that stent assistance for retreatment reduced major recanalization at both 6 months (p = 0.012, OR 0.161, CI 0.038–0.067) and thereafter (p = 0.002, OR 0.226, CI 0.088–0.581).15
Over the last 5 years, flow diversion has been used increasingly for large/giant, difficult to treat, and recurrent aneurysms. Chalouhi et al. investigated the use of Pipeline for the treatment of recurrent aneurysms.16 They evaluated 15 patients with recurrent aneurysms that were treated with Pipeline. The major and minor complication rate was 6.7% and 26.7%, respectively. Favorable clinical outcome (mRS 0–2) was seen in 93.3% of patients. Complete and near complete occlusion at follow-up was achieved in 64.3% and 28.6% of patients, respectively. They found that there was a lower obliteration rate for aneurysms that had previously undergone stent assisted coiling. Unfortunately, there were too few flow diversion cases at our institution during this time period to lend to the analysis. Li et al. also demonstrated the successful use of the Willis covered stent in 8 recurrent aneurysms.12
This study has a number of limitations. It is retrospective in nature, which inherently introduces bias. The study spanned 2005–2013, during which much advancement in the endovascular field has occurred. The number of patients without angiographic follow-up is not insignificant and the generalization of our results may not be completely accurate. There were too few flow diversion cases to lend to the analysis. This treatment option has the potential to be very useful for recurrent aneurysms. The study did not include surgical clipping for recurrent aneurysms, which has been shown to be safe and effective for previously coiled aneurysms.36
Conclusions
Endovascular retreatment of intracranial aneurysms is not an uncommon practice. Our study demonstrates that small aneurysm size and retreatment with permanent parent vessel support, namely stent-assisted coiling, are associated with retreatment success. Although aneurysm size is not a modifiable factor, it should be noted that larger aneurysms require closer angiographic follow-up. Stent-assisted coiling should be considered for aneurysms requiring endovascular retreatment. These findings could be useful in the effort to both prevent and predict treatment failure following endovascular retreatment and should be validated in a prospective study.
Acknowledgments
All authors had integral participation in the study. JRM collected the data. JRM, JM, JF, SP, AP participated in the angiographic review. EO performed the statistical analysis and table creation. JRM performed the literature review and drafted the manuscript. All authors reviewed and edited the manuscript.
Conflict of interest
J Mocco is the national/international PI/Co-PI for the following trials: THERAPY (PI), FEAT (PI), AMERICA (PI), LARGE (Co-PI), POSITIVE (Co-PI). He is on the steering committee for the MAPS trial. He is a consultant to Lazarus Effect, Reverse, Pulsar, Edge Therapeutics, and Medina. He is an investor with Blockade Medical and Medina. Johanna Fifi is a consultant to Microvention. Srinivasan Paramasivam is a consultant to Microvention. Aman Patel is a consultant to Penumbra. These conflicts have no impact on this work. The other authors have no conflicts of interest.
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
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