Front. Neurol. Frontiers in Neurology Front. Neurol. 1664-2295 Frontiers Media S.A. 10.3389/fneur.2022.869880 Neurology Systematic Review Risk Factors for Recurrence of Intracranial Aneurysm After Coil Embolization: A Meta-Analysis Jin Ji 1 † Guo Geng 2 * † Ren Yeqing 2 † Yang Biao 2 Wu Yongqiang 2 Wang Shule 2 Sun Yanqi 2 Wang Xiaogang 2 Wang Yuxiao 1 Zheng Jianzhong 1 1School of Public Health, Shanxi Medical University, Taiyuan, China 2Department of Neurosurgery, The First Hospital, Shanxi Medical University, Taiyuan, China

Edited by: Gustavo J. Rodriguez, Texas Tech University Health Sciences Center El Paso, United States

Reviewed by: Faheem G. Sheriff, Texas Tech University Health Science Center, United States; Basil Erwin Grüter, Aarau Cantonal Hospital, Switzerland

 *Correspondence: Geng Guo guogeng973@163.com

This article was submitted to Endovascular and Interventional Neurology, a section of the journal Frontiers in Neurology

†These authors have contributed equally to this work

 22 07 2022 2022 13 869880 11 02 2022 23 05 2022 Copyright © 2022 Jin, Guo, Ren, Yang, Wu, Wang, Sun, Wang, Wang and Zheng. 2022 Jin, Guo, Ren, Yang, Wu, Wang, Sun, Wang, Wang and Zheng

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Intracranial aneurysm is a severe cerebral disorder involving complicated risk factors and endovascular coiling is a common therapeutic selection for intracranial aneurysm. The recurrence is a clinical challenge in intracranial aneurysms after coil embolization. With this study, we provided a meta-analysis of the risk factors for the recurrence of intracranial aneurysm after coil embolization. Nine studies were included with a total of 1,270 studies that were retrieved from the database. The sample size of patients with intracranial aneurysms ranged from 241 to 3,530, and a total of 9,532 patients were included in the present meta-analysis. The intracranial aneurysms that occurred in middle cerebral artery (MCA) (OR = 1.09, 95% CI: 1.03–1.16, P = 0.0045) and posterior circulation (OR = 2.01, 95% CI: 1.55–2.60, P = 0.000) presented the significantly higher risk of recurrence after coil embolization. Meanwhile, intracranial aneurysms of size > 7 mm (OR = 5.38, 95%CI: 3.76–7.70, P = 0.000) had a significantly higher risk of recurrence after coil embolization. Moreover, ruptured aneurysm (OR = 2.86, 95% CI: 2.02–4.04, P = 0.000) and subarachnoid hemorrhage (SAH) (OR = 1.57, 95% CI: 1.20–2.06, P = 0.001) was positively correlated with the risk of recurrence after coil embolization. In conclusion, this meta-analysis identified the characteristics of intracranial aneurysms with MCA, posterior circulation, size > 7 mm, ruptured aneurysm, and SAH as the risk factors of recurrence after coil embolization for intracranial aneurysms.

 intracranial aneurysm coil embolization recurrence meta-analysis risk factors Introduction

The cerebral arterial aneurysm is a severe and prevalent disorder, which is a leading cause of sudden neurological disability secondary to rupture (1, 2). Intracranial aneurysms are among the most popular non-traumatic risk factors of subarachnoid hemorrhage (SAH) with an increasing incidence, resulting in a heavy economic and social burden globally (3, 4). Even though the patients accept therapy, many cases will ultimately die or suffer from a cognitive disability or severe neurological (5, 6). The treatment of intracranial aneurysms is associated with multiple unexpected risk factors (7, 8). Endovascular coiling has become a prevalent therapeutic selection for intracranial aneurysm patients in many hospitals (9, 10). Nevertheless, the recurrence of the intracranial aneurysm treated by endovascular coiling is still a crucial problem in the clinic (11). Numerous risk factors are involved in the events of recurrence and rebleeding (12, 13), which are poorly understood.

In this study, we were interested in the exploration of the correlation of risk factors, such as gender, smoking, posterior circulation, anterior cerebral artery (ACA), interior carotid artery (ICA), middle cerebral artery (MCA), aneurysms of size, aneurysms of the neck, ruptured aneurysm, and SAH, with the recurrence of intracranial aneurysms after coil embolization.

 Materials and Methods Literature Inclusion and Exclusion Criteria

The inclusion criteria were as follows: the study type is a retrospective study; the language is limited to English.

Exclusion criteria: duplicate publication; research without full text, research without the needed information of this study, incomplete information, or inability to conduct data extraction; animal experiments; reviews and systematic reviews.

 Search Strategy

In this meta-analysis, we searched Pubmed, Embase, and Cochrane Library from the establishment of the database to December 2020. The search terms are mainly: “Intracranial Aneurysm” “Brain Aneurysm” “Anterior Communicating Artery Aneurysm” “Basilar Artery Aneurysm” “Cerebral Aneurysm” and “Coil embolization” “recurrence”. Keywords were combined with Boolean operators to increase search sensitivity and specificity.

 Literature Screening and Data Extraction

The literature search, screening, and information extraction were all independently completed by two researchers. When there were doubts or disagreements, the decision was made after discussion or consultation with a third party. The data extraction included the author, year, study area, research type, number of cases, and the OR and 95%CI of age, smoking, posterior circulation, ACA (anterior cerebral artery), ICA (interior carotid artery), MCA (middle cerebral artery), Ruptured aneurysm, SHA (subarachnoid hemorrhage), aneurysm size > 7mm and aneurysm neck > 4mm for the prediction of recurrence after coil embolization for intracranial aneurysms. Aneurysm recurrence was defined as inflow into a previously completely occluded aneurysm or growth of an incompletely occluded aneurysm (aneurysm recanalization) (14).

 Literature Quality Assessment

Two authors (GENG GUO and JIANZHONG ZHENG) independently conducted literature quality evaluations using the NOS (Newcastle-Ottawa Scale) for the retrospective study. When the opinions are inconsistent, it is decided through discussion or consultation with a third person. The meta-analysis was performed based on the related items of the Preferred Reporting Items for Systematic Reviews and Meta-analysis statement (PRISMA statement).

 Data Synthesis and Statistical Analysis

Following eligibility verification, data about the risk factors, such as gender, smoking, posterior circulation, ACA, ICA, MCA, aneurysms of size, aneurysms of the neck, ruptured aneurysm, and SAH, were extracted from the manuscript text, patient demographic tables, and on-line tables and figures. STATA 15.1 was used to analyze the data. Odds ratio (OR; 95% Cl) was used to analyze the risk factors of no-reflow/slow-flow. Higgins index (I2) is used to evaluate heterogeneity. If the heterogeneity test is P ≥ 0.1 and I2 ≤ 50%, it indicates that there is homogeneity between studies, and the fixed effects model is used for combined analysis; if P < 0.1, I2 > 50%, it indicates that the study is heterogeneous, and we use sensitivity analysis to find the source of heterogeneity. If the heterogeneity is still large, we use the random-effects model or give up the combination of results and use descriptive analysis. A funnel plot was used to analyze publication bias.

 Results The Results of the Literature Search

In this study, a total of 1,270 studies were retrieved from the database. After eliminating duplicate studies, 638 were obtained. After browsing titles and abstracts, 385 studies were obtained. Finally, nine studies were meta-analyzed through full-text reading (Figure 1).

Flow diagram for the selection of studies.

 Baseline Characteristics and Quality Assessment of the Included Studies

A total of nine retrospective studies were included in this meta-analysis. The sample size of patients with intracranial aneurysms ranged from 241 to 3,530, and a total of 9,532 patients were included in the present meta-analysis. Patients in four studies were from China, patients in two studies were from Korea, and the others were from Europe and America. The NOS score used for quality assessment is all above seven and meets the requirements. The baseline characteristics quality assessment of the included studies is shown in Table 1.

Baseline characteristics and quality assessment of the included studies.

References Research type Study area Number of cases Gender Age Follow-Up time NOS score
(Male/Female) (Year) (Month)
Tian et al. (12) Retrospective China 504 219/285 52.5 ± 10.7 13.6 ± 4.5 7
Choi et al. (7) Retrospective Korea 3,530 948/2,094 57.8 ± 10.9 21.4 ± 16.8 8
Futchko et al. (14) Retrospective USA 296 64/232 56.4 / 8
Mortimer (15) Retrospective UK 241 166/75 49.9 ± 12.5 31 7
Jeon (16) Retrospective Korea 870 275/595 57.9 ± 11.0 30.8 ± 8.3 7
Li (17) Retrospective China 1,335 467/868 54.0 ± 9.8 / 8
Zhang (18) Retrospective China 283 205/78 51.7 ± 8.9 / 7
Nishido (19) Retrospective France 1,815 986/829 50.5 ± 12.9 / 7
Huang (20) Retrospective China 658 243/415 / / 8
Results of Meta-Analysis

We first explored the correlation between gender (female) and recurrence after coil embolization for intracranial aneurysms. There are 4 studies, including 4,558 patients, that reported the association between gender (female) and recurrence after coil embolization for intracranial aneurysms. Since there is no significant heterogeneity (I2 = 0.0%, P = 0.793 > 0.1), a meta-analysis was conducted through a fixed-effects model. The pooled results show that there is no significant association between gender (female) and recurrence after coil embolization for intracranial aneurysms (OR = 0.96, 95% CI: 0.77–1.19, P = 0.707 > 0.05; Figure 2A). We also pooled the results through a random-effects model (I2 = 62.5%, P = 0.103 > 0.1), thus we found that there is no significant association between smoking and recurrence after coil embolization for intracranial aneurysms (OR = 1.61, 95% CI: 0.59–4.34, P = 0.351 > 0.05; enrolling 579 patients; Figure 2B).

(A) The correlation between gender and recurrence after coil embolization for intracranial aneurysms. (B) The correlation between smoking and recurrence after coil embolization for intracranial aneurysms. (C) The correlation between posterior circulation and recurrence after coil embolization for intracranial aneurysms. (D) The correlation between ACA and recurrence after coil embolization for intracranial aneurysms. (E) The correlation between ICA and recurrence after coil embolization for intracranial aneurysms. (F) The correlation between MCA and recurrence after coil embolization for intracranial aneurysms.

We continue to explore the correlation between the location of the aneurysm and the recurrence of intracranial aneurysms after coil embolization. There are four studies, including 5,145 patients, that reported the association between posterior circulation and recurrence after coil embolization for intracranial aneurysms. Since there is no significant heterogeneity (I2 = 45.4%, P = 0.139 > 0.1), a meta-analysis was conducted through a fixed-effects model. The pooled results indicate that intracranial aneurysms that occur in posterior circulation have a significantly higher risk of recurrence after coil embolization (OR = 2.01, 95% CI: 1.55–2.60, P = 0.000 < 0.05; Figure 2C). There are two studies, including 899 patients, that reported the association between ACA and its recurrence after coil embolization for intracranial aneurysms. Since there is significant heterogeneity (I2 = 83.4%, P = 0.014 < 0.1), a meta-analysis was conducted through a random-effects model. The polled results indicate that there is no significant association between ACA and recurrence after coil embolization for intracranial aneurysms (OR = 0.42, 95% CI: 44–4.66, P = 0.483.05; Figure 2D). Additionally, pooled results also show that there is no significant association between ICA and recurrence after coil embolization for intracranial aneurysms (OR = 1.33, 95% CI: 0.42–4.18, P = 0.627 > 0.05; enrolling 2,056 patients) from a random-effects model (I2 = 75.0%, P = 0.045 < 0.1; Figure 2E). However, pooled results show that intracranial aneurysms that occur in MCA have a significantly higher risk of recurrence after coil embolization (OR = 1.09, 95% CI: 1.03–1.16, P = 0.004 < 0.05; enrolling 2,714 patients) from a fixed-effects model (I2 = 0.0%, P = 0.806 > 0.1; Figure 2F).

In addition, we explored the correlation between disease characteristics and recurrence after coil embolization. There are four studies, including 2,065 patients, that reported the association between aneurysms of size > 7 mm and their recurrence after coil embolization for intracranial aneurysms. Since there is no significant heterogeneity (I2 = 0.0%, P = 0.866 > 0.1), a meta-analysis was conducted through a fixed-effects model. The pooled results indicate that intracranial aneurysms of size > 7 mm have a significantly higher risk of recurrence after coil embolization. (OR = 5.38, 95% CI: 3.76–7.70, P = 0.000 < 0.05; Figure 3A). There are two studies, including 3,771 patients, that reported the association between aneurysms of neck > 4 mm and recurrence after coil embolization for intracranial aneurysms. Since there is significant heterogeneity (I2 = 72.2%, P = 0.058 < 0.1), a meta-analysis was conducted through a random-effects model. The pooled results indicate that there is no significant association between aneurysms of neck > 4 mm and recurrence after coil embolization for intracranial aneurysms (OR = 2.08, 95% CI: 0.50–8.70, P = 0.315 > 0.05; Figure 3B).

(A) The correlation between aneurysms of size > 7 mm and recurrence after coil embolization for intracranial aneurysms. (B) The correlation between aneurysms of neck > 4 mm and recurrence after coil embolization for intracranial aneurysms. (C) The correlation between ruptured aneurysm and recurrence after coil embolization for intracranial aneurysms. (D) The correlation between SAH and recurrence after coil embolization for intracranial aneurysms.

Lastly, pooled results show that ruptured aneurysm (OR = 2.86, 95% CI: 2.02–4.04, P = 0.000 < 0.05; enrolling 4,975 patients) and SAH (OR = 1.57, 95% CI: 1.20–2.06, P = 0.001 < 0.05; enrolling 4,020 patients) can all significantly increase the risk of recurrence after coil embolization with random effects models (I2 = 56.1%, P = 0.077 < 0.1; I2 = 52.5%, P = 0.122 > 0.1; Figures 3C,D).

 Publication Bias

The funnel plot of this study is shown in Supplementary Figure S1. The funnel plot is basically symmetrical, indicating that there is no obvious publication bias in this study.

 Sensitivity Analysis

Sensitivity analysis eliminates each included study one by one and performs a summary analysis on the remaining studies to assess whether a single included study has an excessive impact on the results of the entire meta-analysis. The results showed that none of the studies had an excessive impact on the results of the meta-analysis, indicating that the results of the remaining studies are stable and reliable.

 Discussion

Intracranial aneurysm is a prevalent cerebral disorder with severe injury and coil embolization has been identified as a prevalent therapeutic method in the intracranial aneurysm. In the present study, we identified the risk factors of recurrence of intracranial aneurysm after coil embolization using a meta-analysis based on nine studies.

In our meta-analysis, we found that there is no significant association between gender and smoking with recurrence after coil embolization for intracranial aneurysms. However, it has been reported that smoking is harmful to the clinical outcomes of intracranial aneurysm patients using coil embolization, and aneurysms are more prevalent in women than men (21). The influence of gender and smoking on the recurrence after coil embolization for intracranial aneurysms may be complicated and are affected by other factors. It has been identified that ACA, ICA, and MCA are close factors of intracranial aneurysms (22–27). Previous investigation has shown that posterior circulation is a risk factor for coil embolization of unruptured aneurysms (28). The behavior of posterior circulation has been proved to associate with PcoA aneurysms recanalization (29). Our analysis showed that MCA bifurcation and posterior circulation aneurysms presented a higher recurrence risk. It has been reported that endovascular treatment of wide-neck MCA and basilar apex aneurysms resulted in a core lab adjudicated Raymond Roy (14) occlusion rate of 30.6% and self-reported results at follow-up favor better angiographic outcomes (30). It suggests the necessity and significance of novel endovascular devices specifically designed to treat complex intracranial aneurysms.

Our data also revealed that ruptured aneurysm and SAH were positively correlated with the risk of recurrence after coil embolization. Recently, a study of the comparison between outcomes of endovascular and surgical treatments of ruptured anterior communicating artery aneurysms show that aneurysms with the first presentation of SAH secondary to a ruptured anterior communicating artery aneurysm treated by endovascular coiling have an increased risk of recurrence vs. those treated with clipping (31). These findings may provide some reference for treatment decisions of a multi-disciplinary team. It has been identified that the size of intracranial aneurysms significantly affects the selection and treatment effectiveness of intracranial aneurysms (32–35). Consistently, our analysis showed that intracranial aneurysms of size > 7 mm have a significantly higher risk of recurrence after coil embolization.

There are still some limitations in the current study. In this work, we provided a meta-analysis of the risk factors for recurrence of intracranial aneurysms after coil embolization. Despite the crucial risk of rebleeding or symptomatic recurrences needing retreatment in the model, we did not describe them in our analysis because there was no such detailed data in the literature. Meanwhile, the aspect of time and the aneurysms recurrence were not considered in the current study because there was no such detailed data in the literature, which is crucial for treatment decisions. In this study, we only included retrospective studies. Other types of studies should be considered in future investigations.

 Conclusions

This meta-analysis identified the characteristics of intracranial aneurysms with MCA, posterior circulation, size > 7 mm, ruptured aneurysm, and SAH as the risk factors of recurrence after coil embolization for intracranial aneurysms. Our finding enriches the understanding of the recurrence of intracranial aneurysms after coil embolization in patients, providing the theoretical reference for the clinical application of coil embolization for intracranial aneurysms. Meanwhile, it is crucial to design novel and specific endovascular devices for the treatment of these complex intracranial aneurysms and attenuate their recurrence.

 Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

 Author Contributions

GG, JJ, YR, and JZ designed the study and wrote the manuscript. GG, YR, BY, YWu, SW, YS, XW, and YWa performed the analysis. All authors contributed to the article and approved the submitted version.

 Funding

This study was supported by the Scientific Research Foundation of Shanxi Intelligence Institute of Big Data Technology and Innovation (SIBD-2020-YL0052).

 Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

 Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

 Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fneur.2022.869880/full#supplementary-material

Funnel plot for evaluating the publication bias of this meta-analysis.

 References Brown RD Jr Broderick JP. Unruptured intracranial aneurysms: epidemiology, natural history, management options, and familial screening. Lancet Neurol. (2014) 13:393–404. 10.1016/S1474-4422(14)70015-824646873 Etminan N Rinkel GJ. Unruptured intracranial aneurysms: development, rupture and preventive management. Nat Rev Neurol. (2016) 12:699–713. 10.1038/nrneurol.2016.15028145447 Matsushige T Sakamoto S Ishii D Shinagawa K Shimonaga K Hosogai M . Safety and efficacy of a new outreach distal access catheter, TACTICS, for coil embolization of unruptured intracranial aneurysms. Interv Neuroradiol. (2018) 24:482–8. 10.1177/159101991877488829783870 Ihn YK Shin SH Baik SK Choi IS. Complications of endovascular treatment for intracranial aneurysms: management and prevention. Interv Neuroradiol. (2018) 24:237–45. 10.1177/159101991875849329466903 Nevzati E Rey J Coluccia D Gruter BE Wanderer S. vonGunten M . Aneurysm wall cellularity affects healing after coil embolization: assessment in a rat saccular aneurysm model. J Neurointerv Surg. (2020) 12:621–5. 10.1136/neurintsurg-2019-01533531871070 Cai ZQ Chai SH Wei XL You KZ Li J Zhang DM. Comparison of postsurgical clinical sequences between completely embolized and incompletely embolized patients with wide nicked intracranial aneurysms treated with stent assisted coil embolization technique: a STROBE-compliant study. Medicine. (2018) 97:e10987. 10.1097/MD.000000000001098729879055 Choi HH Lee SH Yeon EK Yoo DH Cho YD Cho WS . Determination of aneurysm volume critical for stability after coil embolization: a retrospective study of 3530 aneurysms. World Neurosurg. (2019) 132:e766–74. 10.1016/j.wneu.2019.08.02031415892 Kim SS Park H Lee KH Jung S Yoon CH Kim SK . Utility of low-profile visualized intraluminal support junior stent as a rescue therapy for treating ruptured intracranial aneurysms during complicated coil embolization. World Neurosurg. (2020) 135:e710–e5. 10.1016/j.wneu.2019.12.11031887464 Haffaf I Clarencon F Shotar E Rolla-Bigliani C Vande Perre S Mathon B . Medina embolization device for the treatment of intracranial aneurysms: 18 months' angiographic results. J Neurointerv Surg. (2019) 11:516–22. 10.1136/neurintsurg-2018-01411030472677 Yamagami K Hatano T Nakahara I Ishii A Ando M Chihara H . Long-term outcomes after intraprocedural aneurysm rupture during coil embolization of unruptured intracranial aneurysms. World Neurosurg. (2020) 134:e289–97. 10.1016/j.wneu.2019.10.03831629140 Suzuki T Genkai N Nomura T Abe H. Assessing the hemodynamics in residual cavities of intracranial aneurysm after coil embolization with combined computational flow dynamics and silent magnetic resonance angiography. J Stroke Cerebrovasc Dis. (2020) 29:105290. 10.1016/j.jstrokecerebrovasdis.2020.10529032992205 Tian Z Liu J Zhang Y Zhang Y Zhang X Zhang H . Risk factors of angiographic recurrence after endovascular coil embolization of intracranial saccular aneurysms: a retrospective study using a multicenter database. Front Neurol. (2020) 11:1026. 10.3389/fneur.2020.0102633041975 Son W Kang DH. Risk factor analysis of delayed intracerebral hemorrhage after coil embolization of unruptured cerebral aneurysms. Front Neurol. (2020) 11:584596. 10.3389/fneur.2020.58459633193045 Futchko J Starr J Lau D Leach MR Roark C Pandey AS . Influence of smoking on aneurysm recurrence after endovascular treatment of cerebrovascular aneurysms. J Neurosurg. (2018) 128:992–8. 10.3171/2016.12.JNS16162528644100 Mortimer AM Marsh H Klimczak K Joshi D Barton H Nelson RJ . Is long-term follow-up of adequately coil-occluded ruptured cerebral aneurysms always necessary? A single-center study of recurrences after endovascular treatment. J Neurointerv Surg. (2015) 7:373–9. 10.1136/neurintsurg-2014-01115224721754 Jeon JP Cho YD Yoo DH Moon J Lee J Cho WS . Risk factor analysis of recanalization timing in coiled aneurysms: Early versus late recanalization. AJNR Am J Neuroradiol. (2017) 38:1765–70. 10.3174/ajnr.A526728619836 Li H Gao BL Li CH Wang JW Liu JF Yang ST. Endovascular retreatment of cerebral aneurysms previously treated with endovascular embolization. J Neurol Surg A Cent Eur Neurosurg. (2020) 81:207–12. 10.1055/s-0039-168551331746449 Zhang Q Jing L Liu J Wang K Zhang Y Paliwal N . Predisposing factors for recanalization of cerebral aneurysms after endovascular embolization: a multivariate study. J Neurointerv Surg. (2018) 10:252–7. 10.1136/neurintsurg-2017-01304128377443 Nishido H Piotin M Bartolini B Pistocchi S Redjem H Blanc R. Analysis of complications and recurrences of aneurysm coiling with special emphasis on the stent-assisted technique. AJNR Am J Neuroradiol. (2014) 35:339–44. 10.3174/ajnr.A365823907240 Huang DZ Jiang B He W Wang YH Wang ZG. Risk factors for the recurrence of an intracranial saccular aneurysm following endovascular treatment. Oncotarget. (2017) 8:33676–82. 10.18632/oncotarget.1689728430600 Ahmad S. Clinical outcome of endovascular coil embolization for cerebral aneurysms in Asian population in relation to risk factors: a 3-year retrospective analysis. BMC Surg. (2020) 20:104. 10.1186/s12893-020-00756-132408864 King RM Chueh JY van der Bom IM Silva CF Carniato SL Spilberg G . The effect of intracranial stent implantation on the curvature of the cerebrovasculature. Am J Neuroradiol. (2012) 33:1657–62. 10.3174/ajnr.A306222538075 Yamada S Ishikawa M Yamamoto K Ino T Kimura T Kobayashi S . Aneurysm location and clipping vs. coiling for development of secondary normal-pressure hydrocephalus after aneurysmal subarachnoid hemorrhage: Japanese stroke databank. J Neurosurg. (2015) 123:1555–61. 10.3171/2015.1.JNS14276126230474 Poncyljusz W Kubiak K. Initial experience with LVIS EVO stents for the treatment of intracranial aneurysms. J Clin Med. (2020) 9:3966. 10.3390/jcm912396633297449 Twitchell S Abou-Al-Shaar H Reese J Karsy M Eli IM Guan J . Analysis of cerebrovascular aneurysm treatment cost: retrospective cohort comparison of clipping, coiling, and flow diversion. Neurosurg Focus. (2018) 44:E3. 10.3171/2018.1.FOCUS1777529712525 Koyanagi M Ishii A Imamura H Satow T Yoshida K Hasegawa H . Long-term outcomes of coil embolization of unruptured intracranial aneurysms. J Neurosurg. (2018) 129:1492–8. 10.3171/2017.6.JNS1717431629140 Takeshima Y Kaku Y Nishi T Mukasa A Yamashiro S. Multiple cerebral aneurysms associated with neurofibromatosis type 1. J Stroke Cerebrovasc Dis. (2019) 28:e83–91. 10.1016/j.jstrokecerebrovasdis.2019.04.01931080139 Son W Kang DH. Is vertebral artery and posterior inferior cerebellar artery dominance a risk factor for thromboembolism during coil embolization of unruptured posterior circulation aneurysms? World Neurosurg. (2020) 138:e743–8. 10.1016/j.wneu.2020.03.06532200010 Choi HH Cho YD Yoo DH Lee SH Yeon EK Kang HS . Comparative analysis of coil embolization in posterior and anterior communicating artery aneurysms. J Neurointerv Surg. (2019) 11:790–5. 10.1136/neurintsurg-2018-01449030655359 De Leacy RA Fargen KM Mascitelli JR Fifi J Turkheimer L Zhang X . Wide-neck bifurcation aneurysms of the middle cerebral artery and basilar apex treated by endovascular techniques: a multicentre, core lab adjudicated study evaluating safety and durability of occlusion (BRANCH). J Neurointerv Surg. (2019) 11:31–6. 10.1136/neurintsurg-2018-01377129858397 Harris L Hill CS Elliot M Fitzpatrick T Ghosh A Vindlacheruvu R. Comparison between outcomes of endovascular and surgical treatments of ruptured anterior communicating artery aneurysms. Br J Neurosurg. (2021) 35:313–8. 10.1080/02688697.2020.181251732852231 Lee J Cho YD Yoo DH Kang HS Cho WS Kim JE . Does stent type impact coil embolization outcomes in extended follow-up of small-sized aneurysms (<10 mm)? Neuroradiology. (2018) 60:747–56. 10.1007/s00234-018-2022-429737413 Damiano RJ Tutino VM Paliwal N Patel TR Waqas M Levy EI . Aneurysm characteristics, coil packing, and post-coiling hemodynamics affect long-term treatment outcome. J Neurointerv Surg. (2020) 12:706–13. 10.1136/neurintsurg-2019-01542231848217 Burkhardt JK Srinivasan V Srivatsan A Albuquerque F Ducruet AF Hendricks B . Multicenter postmarket analysis of the neuroform atlas stent for stent-assisted coil embolization of intracranial aneurysms. Am J Neuroradiol. (2020) 41:1037–42. 10.3174/ajnr.A658132467183 Yu LB Yang XJ Zhang Q Zhang SS Zhang Y Wang R . Management of recurrent intracranial aneurysms after coil embolization: a novel classification scheme based on angiography. J Neurosurg. (2018) 131:1455–61. 10.3171/2018.6.JNS18104630497155