Y-Configuration Stenting for Coil Embolization of Complex Intracranial Aneurysms: Distinguishing Between Use of Crossing-Y and Kissing-Y

Y-Configuration Stenting for Coil Embolization of Complex Intracranial Aneurysms: Distinguishing Between Use of Crossing-Y and Kissing-Y

Journal Pre-proof Y-configuration stenting for coil embolization of complex intracranial aneurysms: distinguishing to use between “crossing-Y” and “ki...

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Journal Pre-proof Y-configuration stenting for coil embolization of complex intracranial aneurysms: distinguishing to use between “crossing-Y” and “kissing-Y” Kenichi Sato, M.D., Ph.D., Yasushi Matsumoto, M.D., Atsushi Kanoke, M.D., Ph.D., Akira Ito, M.D., Ph.D., Miki Fujimura, M.D., Ph.D., Teiji Tominaga, M.D., Ph.D. PII:

S1878-8750(20)32467-0

DOI:

https://doi.org/10.1016/j.wneu.2020.11.092

Reference:

WNEU 16363

To appear in:

World Neurosurgery

Received Date: 3 September 2020 Revised Date:

15 November 2020

Accepted Date: 16 November 2020

Please cite this article as: Sato K, Matsumoto Y, Kanoke A, Ito A, Fujimura M, Tominaga T, Yconfiguration stenting for coil embolization of complex intracranial aneurysms: distinguishing to use between “crossing-Y” and “kissing-Y”, World Neurosurgery (2020), doi: https://doi.org/10.1016/ j.wneu.2020.11.092. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Inc. All rights reserved.

CRediT author statement Conceptualization: Kenichi Sato, Yasushi Matsumoto Methodology: Kenichi Sato Software: None Validation: Kenichi Sato, Atsushi Kanoke, Akira Ito Formal analysis: Kenichi Sato Investigation: Kenichi Sato, Yasushi Matsumoto, Atsushi Kanoke, Akira Ito

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Data Curation: Kenichi Sato, Yasushi Matsumoto

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Visualization: Kenichi Sato

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Writing- Original Draft: Kenichi Sato Writing- Review & Editing: all authors

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Resources: Yasushi Matsumoto, Miki Fujimura, Teiji Tominaga

Supervision: Miki Fujimura, Teiji Tominaga

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Funding acquisition: None

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Project administration: Kenichi Sato, Miki Fujimura, Teiji Tominaga

Y-configuration stenting for coil embolization of complex intracranial aneurysms: distinguishing to use between “crossing-Y” and “kissing-Y”

Kenichi Sato, M.D., Ph.D.,a, b Yasushi Matsumoto, M.D.,a Atsushi Kanoke, M.D., Ph.D.,a, c Akira Ito, M.D., Ph.D.,a, c Miki Fujimura, M.D., Ph.D.,d Teiji Tominaga, M.D., Ph.D.c

Department of Neuroendovascular Therapy, Kohnan Hospital, Sendai, Japan

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Department of Neurosurgery, Tohoku Medical and Pharmaceutical University, Sendai,

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Japan

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Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai,

Department of Neurosurgery, Kohnan Hospital, Sendai, Japan

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d

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Japan

Corresponding Author:

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Kenichi Sato, M.D., Ph.D.

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Department of Neurosurgery, Tohoku Medical and Pharmaceutical University 1-15-1, Hukumuro, Miyagino-Ku, Sendai, Japan, 983-8536 Telephone: +81-22-290-8500 Fax: +81-22-290-8860 E-mail: [email protected]

Other author’s contact information Yasushi Matsumoto, M.D.,a Email: [email protected] Phone: +81-22-248-2131

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Atsushi Kanoke, M.D., Ph.D.,a,c Email: [email protected] Phone: +81-22-248-2131

Akira Ito, M.D., Ph.D.,a,c Email: [email protected]

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Phone: +81-22-717-7230

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Miki Fujimura, M.D., Ph.D.,d

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Email: [email protected]

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Teiji Tominaga, M.D., Ph.D. c

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Phone: +81-22-248-2131

Email: [email protected]

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Phone: +81-22-717-7230

Keywords: bifurcation, cerebral aneurysm, endovascular treatment, stent-assisted coiling, Y configuration

Short title: Y-configuration stenting

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Y-configuration stenting for coil embolization of complex intracranial aneurysms: distinguishing to use between “crossing-Y” and “kissing-Y”

Kenichi Sato, M.D., Ph.D.,a, b Yasushi Matsumoto, M.D.,a Atsushi Kanoke, M.D., Ph.D.,a, c Akira Ito, M.D., Ph.D.,a, c Miki Fujimura, M.D., Ph.D.,d Teiji Tominaga, M.D., Ph.D.c

Department of Neuroendovascular Therapy, Kohnan Hospital, Sendai, Japan

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Department of Neurosurgery, Tohoku Medical and Pharmaceutical University, Sendai,

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Japan

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Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai,

Department of Neurosurgery, Kohnan Hospital, Sendai, Japan

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d

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Japan

Corresponding Author:

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Kenichi Sato, M.D., Ph.D.

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Department of Neurosurgery, Tohoku Medical and Pharmaceutical University 1-15-1, Hukumuro, Miyagino-Ku, Sendai, Japan, 983-8536 Telephone: +81-22-290-8500 Fax: +81-22-290-8860 E-mail: [email protected]

Other author’s contact information Yasushi Matsumoto, M.D.,a Email: [email protected] Phone: +81-22-248-2131

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Atsushi Kanoke, M.D., Ph.D.,a,c Email: [email protected] Phone: +81-22-248-2131

Akira Ito, M.D., Ph.D.,a,c Email: [email protected]

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Phone: +81-22-717-7230

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Miki Fujimura, M.D., Ph.D.,d

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Email: [email protected]

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Teiji Tominaga, M.D., Ph.D. c

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Phone: +81-22-248-2131

Email: [email protected]

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Phone: +81-22-717-7230

Keywords: bifurcation, cerebral aneurysm, endovascular treatment, stent-assisted coiling, Y configuration

Short title: Y-configuration stenting

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Abbreviations: AcomA, anterior communicating artery AN, aneurysm BA, basilar artery ICA, internal carotid artery MCA, middle cerebral artery

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mRR, modified Raymond-Roy

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SAH, subarachnoid hemorrhage

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PcomA, posterior communicating artery

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mRS, modified Rankin scale

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Abstract Objective: Coil embolization with Y-stenting is recognized as a suitable treatment for complex wide-necked aneurysms. Y-stenting comprises crossing-Y stenting, in which a stent is passed through the interstices of another stent, and kissing-Y stenting, in which two stents are arranged parallelly. The purpose of this study was to elucidate how to distinguish to use between the two Y-stenting techniques.

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Methods: Clinical and angiographic data of patients who underwent coil embolization with

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Y-stenting at our department from 2015 to 2019, were retrospectively analyzed. Basic

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characteristics, endovascular procedure, complications, and outcomes were compared

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between kissing-Y and crossing-Y stenting groups.

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Results: Thirty-eight intracranial aneurysms in 38 consecutive patients were included in this

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study. Nineteen (50%) patients were treated with coil embolization with kissing-Y stenting and 19 (50%) with crossing-Y. Endovascular procedures were successfully performed in all

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but one patient, in the kissing-Y group, who had stent migration. One (2.6%) hemorrhage

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recurred 12 months after coiling with kissing-Y stenting. Angiographic follow-up (mean, 15.8 months) was available in 35 patients. Adequate occlusion was demonstrated in 14 (77.8%) and 13 (76.5%) patients in the kissing-Y and crossing-Y groups, respectively. Larger, wider-necked, and more proximal aneurysms were treated with kissing-Y stenting than with crossing-Y stenting, although there were no significant differences between the groups in complication rates or clinical outcomes. Conclusions: Kissing-Y and crossing-Y stenting of intracranial aneurysms were both feasible and yielded reasonable angiographic and clinical results. The choice between the kissing-Y or crossing-Y stenting technique should be decided according to the angioarchitecture of targeted aneurysms.

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Introduction Despite improvements in endovascular techniques, wide-necked aneurysms located at an arterial bifurcation pose formidable challenges for intra-aneurysmal coil embolization, particularly when the branches originate from the aneurysm base. New devices, such as the Woven EndoBridge system (MicroVention-Terumo, Tustin, CA, USA)1 or PulseRider (CERENOVUS, Miami Lakes, FL, USA),2 which both detain embolic materials in the aneurysmal sac, also do not resolve those difficulties. Use of flow-diverting stents in such

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situations is not ideal, because these would jail one of the daughter branches.3-5 To address

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these difficulties, intra-aneurysmal coil embolization with double stent deployment in

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various configurations has been introduced to attempt to preserve the branches, to avoid

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coil prolapse to the parent artery, and to modify intra-aneurysmal flow.6-15

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Y-configuration stenting, which is the most widespread among these complex stent

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deployment techniques, comprises two different constructions: crossing-Y stenting, in which a stent is passed through the interstices of another stent, and kissing-Y stenting, in which

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two stents are arranged in parallel.9, 10, 12, 15-17 Although a recent meta-analysis showed that

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crossing-Y stenting was more common than kissing-Y stenting,10 no study to date has compared the safety and efficacy between the two constructions in detail. Here, we retrospectively reviewed our experience of the treatment of complex, wide-necked intracranial aneurysms using coil embolization with Y-stenting techniques, to compare the safety and efficacy between crossing-Y and kissing-Y stenting. This study sought to elucidate how to distinguish to use between the two Y-stenting techniques for endovascular treatment of aneurysms that are not amenable to conventional approaches.

Materials and Methods Patients We retrospectively reviewed medical records from a prospectively maintained database to 6

identify all patients with complex, wide-necked intracranial aneurysms treated with coil embolization, using Y-stenting, at our institute from January 2015 to December 2019. Patients’ perioperative outcomes were analyzed. Long-term clinical follow-up was attempted through chart review, patient telephone interview, or both. The institutional review board approved this retrospective study, which was performed according to the principles of the Declaration of Helsinki. An opt-out consent was posted on a Web homepage of our hospital prior to inclusion in this study, instead of obtaining

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informed consent from all study subjects.

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Aneurysms

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Aneurysms were diagnosed by catheter angiography using an Innova IGC630 (GE

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Healthcare, Chicago, IL, USA). We used 3-dimensional reformatted images derived from

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rotational angiograms using the Advantage Workstation Share 5 (version 4.6, GE

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Healthcare) to evaluate aneurysm shape, size, and relationship to arterial branches, perforators, and parent arteries.

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The location of aneurysms were divided into proximal and distal. Proximal aneurysms

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located the basilar artery (BA) bifurcation, the origin of the fetal-type posterior communicating artery (PcomA), and the internal carotid artery (ICA) bifurcation, while distal aneurysms included anterior communicating artery (AcomA) and the middle cerebral artery (MCA) bifurcation. Endovascular treatment A multidisciplinary team made joint aneurysm treatment decisions for each patient. Preoperative surgical planning, including stent configuration, was based on angiographic findings. Kissing-Y stenting (Figure 1A) was employed for large, wide-necked proximal aneurysms arising from a parent artery large enough for parallel placement of two stents, with daughter arteries taking-off at an angle that made it difficult to navigate a microcatheter (i.e., horizontal or arrow angle), and where it was necessary to obtain both 7

vessel-angle remodeling and flow-diversion in order to stabilize aneurysmal hemodynamics. Crossing-Y stenting (Figure 1B) was selected for wide-necked distal aneurysms with a moderately complex angioarchitecture where there was a risk of thrombogenic complications if kissing-Y stenting was applied. Patients with unruptured aneurysms were prescribed 100 mg aspirin and 75 mg clopidogrel 4 days before the endovascular procedure. All procedures were performed via a unilateral or bilateral transfemoral approach with systemic heparinization. The activated

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coagulation time was monitored from the beginning of the endovascular procedure and was

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maintained at a target value between 250 and 300 seconds.

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An 8-F guiding catheter was advanced to the ICA for the anterior circulation aneurysms.

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For posterior circulation aneurysms, a 6-F guiding catheter was advanced to both of the

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vertebral arteries, or an 8-F guiding catheter was advanced to the dominant side. In

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kissing-Y stenting, three microcatheters were navigated through the guiding catheters: two microcatheters were placed into each daughter branch for delivery of the stent and one was

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placed into the aneurysm sac for delivery of coils. Two stents were simultaneously

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deployed in a synchronized fashion from the proximal portion of both daughter branches to the distal portion of parent artery. In crossing-Y stenting, a microcatheter was first advanced within the more challenging daughter branch and the aneurysm was catheterized with a second microcatheter. After deployment of the first stent, the other daughter branch was catheterized, crossing the interstices of the stent. The second stent was deployed to form a Y-shaped construct. Stent configuration, apposition to the vessel, and coverage on the aneurysmal neck were routinely checked using cone-beam computed tomography (CT) angiograms. Then, intra-aneurysmal coil embolization was performed using a jailing technique. For aneurysms where the artery was not large enough for more than two microcatheters to travel in parallel, a stent-deploying microcatheter was inserted into the aneurysmal sac through the interstices of the stent, and the coils were delivered (trans-cell 8

technique). Several large aneurysms were embolized by coils via both the jailing and the trans-cell technique (combined technique). Postoperatively, dual antiplatelet therapy (75 mg/day clopidogrel and 100 mg/day aspirin) was maintained for 6 months, and was then reduced to lifelong clopidogrel monotherapy. Outcomes Angiographic findings were evaluated according to the modified Raymond-Roy (mRR) scales.18 Adequate occlusion was defined as classes

(complete obliteration) and

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(residual neck). Angiographic follow-up was performed at 6, 12, and 24 months, and then as

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needed. Angiographic recurrence was defined as any worsening of the mRR grade or

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enlargement of the residual aneurysm. When angiographic recurrence was considered

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progressive or large enough for embolization, retreatment was planned.

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Clinical outcomes were assessed using the modified Rankin Scale (mRS) score.

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Procedure-related complications were defined as any new neurological deficits or death occurring within 30 days posttreatment. Complications that developed more than 30 days

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after the endovascular procedure were considered delayed complications. Clinical

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follow-up was performed at 6 months and annually thereafter. Each patient was evaluated using the mRS score at follow-up, and any worsening was recorded. The latest mRS scores were dichotomized into favorable (mRS 0-2) or poor (mRS 3-6) for statistical analysis. Statistical analysis Statistical analyses were performed using JMP software (version 12; SAS Institute, Cary, NC, USA). Numerical data are expressed as mean ± SD. Group comparisons of mean and categorical data were performed using Student’s t-test and Pearson’s chi-square test as appropriate. P < 0.05 was considered statistically significant.

Results Patients’ and aneurysms’ characteristics 9

Table 1 shows a summary of characteristics of the patients and aneurysms. During the study period, 38 intracranial aneurysms in 38 consecutive patients (11 men and 27 women; mean age, 68.4 years) were treated with coil embolization with Y-configuration stenting, including 19 aneurysms that were treated with kissing-Y stenting (Figure 2) and 19 treated with crossing-Y (Figure 3). Clinical presentations included subarachnoid hemorrhage (SAH), headache, hydrocephalus, visual disturbance, and oculomotor palsy, while some patients were asymptomatic. The location of the aneurysms included the BA bifurcation in

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17 (44.7%) patients, the origin of the fetal-type PcomA in 8 (21.1%), ICA bifurcation in 5

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(13.2%), AcomA in 5 (13.2%), and the MCA bifurcation in 3 (7.9%). The mean size of the

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with or without stents, or with clipping.

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aneurysms was 11.5mm. Ten aneurysms had been previously treated elsewhere with coiling,

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There was no significant difference between the crossing-Y and kissing-Y stenting groups

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in terms of patients’ characteristics, However, aneurysms treated with kissing-Y stent-assisted coiling were located more proximally (100% versus 57.9%, P = 0.002), were

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larger (13.0 ± 4.6 mm versus 10.0 ± 3.5 mm, P = 0.027), had wider necks (8.2 ± 2.7 mm

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versus 6.6 ± 2.0 mm, P=0.049), and had larger parent arteries (4.3 ± 0.5 mm versus 3.5 ± 0.6 mm, P < 0.001) than those treated with crossing-Y stenting. Endovascular treatment Table 2 summarizes the endovascular procedures and angiographic results. Y-stenting was successfully performed in all but one patient in the kissing-Y group (37/38 patients, 97.4%). This patient had a large, wide-necked PcomA aneurysm that was to be treated with coil embolization using kissing-Y stenting. During stent deployment, the distal edge of an open-cell type stent in the PcomA migrated into the aneurysmal sac. A stent in the ICA was still available and intra-aneurysmal coil embolization was subsequently performed safely. Twenty-six aneurysms (68.4%) were treated using Y-configuration stenting technique using identical stents of the same size, while 12 were treated with stents of different sizes 10

(asymmetrical Y-stenting), because the daughter arteries had different diameters (e.g., PcomA aneurysms). Three stent types (closed-cell type stents: Enterprise2, Codman, Miami Lakes, FL; braded type stents: Lvis, MicroVention-Terumo, Tustin, CA; open-cell type stents: Neuroform Atlas, Stryker, Kalamazoo, MI) were employed equally in the kissing-Y group, while open-cell type stents were preferentially used in the crossing-Y group. Coil-delivery microcatheters were advanced into the aneurysmal sac by a jailing method in all except one of the patients in the kissing-Y group, while crossing-Y stenting enabled

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coil-delivery microcatheters to cross the interstices of the stent to the aneurysmal sac, or to

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combine the trans-cell and jailing techniques in nine and three patients, respectively. For

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four large aneurysms in the kissing-Y stenting group, partial coil embolization was

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performed before deploying stents to prevent migration of the deployed stents into the

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aneurysmal sac.

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Acute in-stent thrombus formation was encountered in two patients of each group and was resolved by intra-arterial fibrinolysis with antithrombotic drugs. Neurological sequelae

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persisted in one of these patients, resulting in the left thalamic infarction (mRS 3). No

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delayed ischemic complications were encountered during this study period. In three patients, post-procedure brain CT revealed convexity SAH, which disappeared without symptoms. A ruptured large PcomA aneurysm re-ruptured lethally 12-months post-coiling with asymmetric kissing-Y stenting using open-cell type stents. Two re-treatments were performed in required. A patient with a symptomatic large PcomA aneurysm, treated with coil embolization with kissing-Y stenting using braded type stents underwent additional coil embolization 12 months after the initial treatment. Another patient with a growing large BA bifurcation aneurysm was treated by coil embolization with crossing-Y stenting using open-cell type stents, but required additional coil embolization 12 months after the initial treatment. Angiographic outcomes 11

Angiograms obtained immediately after the procedures revealed complete aneurysm obliteration (mRR class

) in 18.4%, a residual neck (mRR class Ⅱ) in 36.8%. Most

patients (92.1%) underwent follow-up catheter angiography at least once. During a mean period of 15.8 months, follow-up angiograms demonstrated further thrombosis of the aneurysmal sac in 17.1%. The final results included adequate occlusion in 27 (77.1%) patients and a residual aneurysm in 8 (22.9%). There were no significant differences in angiographic results and the rate of procedure-related complications between kissing-Y and

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crossing-Y stenting groups (Table 2).

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Clinical outcomes

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The mean length of postoperative follow-up was 22.9 ± 4.6 months. Overall, a good

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outcome (mRS 0-2) was observed in 31 patients (81.6%), and a poor outcome (mRS 3-6)

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was 7 (18.4%). Overall, the morbidity and mortality rates of this study were 7.9% and

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10.5%, respectively. There were no significant differences between the two groups in terms

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Discussion

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of clinical outcomes (Table 3).

In this study, we compared the efficacy and safety of coil embolization for treating complex wide-necked bifurcation aneurysms between the kissing-Y and crossing-Y technique to elucidate how to distinguish to use between the two Y-stenting technique. The kissing-Y stenting approach was employed for large, wide-necked proximal aneurysms arising from a parent artery large (at least more than 4 mm in diameter) enough for placing two parallel stents, with daughter arteries taking-off at an angle that hampers microcatheter navigation, and where both vessel-angle remodeling and flow-diversion are required to stabilize aneurysmal hemodynamics. Crossing-Y stenting was selected for wide-necked, distal aneurysms with a moderate complex angioarchitecture and where application of kissing-Y would pose a thrombogenic complication risk. Overall, Y-stenting procedures were 12

successful in 97.4% of patients, and complications occurred in 23.7%. Over the 22.9-months follow-up period, 77.1% of treated aneurysms retained adequate occlusion, and morbidity and mortality rates were 7.9% and 10.5%, respectively. Although our study involved complex aneurysms in difficult situations (relatively high rate of ruptured aneurysms and high-age patients), these results were similar to those reported previously.6, 8, 10, 11, 13-15

The double stenting technique in a Y-configuration was originally described for treating

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peripheral bifurcation vasculature20 and has since been widely applied for treating cerebral

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wide-necked bifurcation aneurysms, to provide support for the coil mass and to preserve the

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daughter arteries.11, 13-15, 19 Several experimental and clinical studies have evaluated changes

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in hemodynamic forces in a bifurcation aneurysm model and have shown that, after

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Y-stenting, the velocity and wall shear stress are markedly reduced inside the treated

Crossing-Y stenting

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aneurysms.16, 17, 21, 22

However, this procedure sometimes includes potential risks, such as migration and

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Crossing-Y stenting has been widely performed as a standard Y-stenting technique.6, 8, 10,

breakage of the first stent when advancing a microcatheter for delivering the second stent through the interstices of the first stent. Additionally, it is difficult to catheterize the second arterial branch through the interstices of the stent due to the acute bifurcation angle.8 The individual cells of the deployed stent cannot be recognized during the procedure, and a microguidewire does not always select an ideal cell for second stent deployment.8 Consequently, stents with an open-cell design are preferred for use in crossing-Y stenting, even though its flow-diverting effect is less.6, 8, 11, 14 When using closed-cell or braded stents, undesirable tubular collapse of the second deployed stent can occur because of its constrained interstices.13 The captured floating struts of the second stent may not be apposite to the underlying vessel wall. Creation of orphaned space and inadequately expanded stent 13

struts remain a potential source of thrombus formation as well as aneurysmal recurrence. Kissing-Y stenting Kissing-Y stenting has also been reported to involve a considerable risk, mainly because the second stent, which is sequentially deployed between the first stent and the vessel wall, may open insufficiently, resulting in acute in-stent thrombosis.9, 10, 15 Thus, we introduced a modified method for kissing-Y stenting, in which two stents are simultaneously deployed from each daughter branch to the parent artery in order to prevent intersection between the

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be due to the following advantages of this technique:

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stents. The satisfactory procedural success rate and angiographic results in this series may

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First, the type of stent (i.e., closed-cell, open-cell, or braded type) can be selected

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according to aneurysmal location, shape, and the relationship to the surrounding vascular

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anatomy, as long as compatible microcatheters are advanced into both daughter vessels. The

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importance of selecting the stent type with respect to the vessel apposition or the flow-diverting effect has been recognized.17, 22, 23 The same type of stents should be selected

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to prevent failure of stent-expansion due to differences in the radial force of stents in the

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parent artery where double stents are arranged in parallel.24 When a bifurcation aneurysm with daughter vessels with diameters differing markedly from that of parent artery is encountered, this technique has advantages in selecting the type of stents in reference to the daughter artery diameter. No patients developed ischemic complications due to the thrombosis of the parent artery or perforating arteries arising from the parent artery during the follow-up period. Second, kissing-Y stenting can make the aneurysmal neck so robust that complete intra-aneurysmal coiling can be achieved.9, 14 A flow-diverting effect or vessel straightening effect, produced by double stents arranged in parallel in the parent artery and diverging to each daughter artery, is also likely when using closed-cell or braided types of stents.12, 16, 17, 22, 23

Consequently, our case series in the kissing-Y stenting group demonstrated satisfactory 14

aneurysmal obliteration rates and durability, despite involving more complex and larger aneurysms than those treated in the crossing-Y stenting group in this study. The kissing-Y technique had some shortcomings. A large-bore guiding catheter or double guiding catheters are required, because at least three microcatheters, including two stent-delivery catheters and one coil-delivery catheter, have to be used simultaneously. Additional coil embolization via a trans-cell approach or parallel usage of a balloon catheter should be avoided, because a microcatheter can hardly pass through the interstices

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of stents in the kissing -Y configuration. A coil-delivery catheter should be inserted to the

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desired position of the aneurysmal sac before deploying stents. Lastly strict application of

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antithrombotic therapy is mandatory to prevent ischemic complications.

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Limitations

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Our study was limited by its small sample size that was derived from a single institution. It

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was retrospective and consecutive and was thus vulnerable to confounding factors and inherent bias. Selection bias in regard with the aneurysmal characteristics was likely caused

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by our treatment strategy. Our hypothesis was that kissing-Y configured by robust stents

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might be more effective but also has a higher risk of complications compared with crossing-Y stenting. Thus kissing-Y stenting was preferentially indicated for larger, wider-necked proximal aneurysms. On the other hands, in distal bifurcation aneurysms or proximal aneurysms of which parent artery was less than 4 mm in diameter, crossing-Y stenting was selected due to prioritizing safety. As a result, it is nigh impossible to simply determine the superiority or inferiority of the two stenting techniques. Rather, the importance of using two techniques properly should be emphasized in this study. Further studies and larger case series are required to assess the efficacy and safety of these techniques.

Conclusions 15

In conclusion, coil embolization with Y-stenting could be a feasible option for the treatment of complex, wide-necked, bifurcation aneurysms. The long-term angiographic and clinical results are similarly good for both kissing-Y and crossing-Y stenting techniques. The choice between the kissing-Y or crossing-Y stenting technique should be decided according to the angioarchitecture of targeted aneurysms.

Declarations of interest

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None.

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Funding

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commercial, or not-for-profit sectors.

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This research did not receive any specific grant from funding agencies in the public,

Ethical Approval

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All procedures performed in the studies involving human participants were in accordance

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with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Author Contributions All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Kenichi Sato, Yasushi Matsumoto, Akira Ito, and Atsushi Kanoke. The first draft of the manuscript was written by Kenichi Sato and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Aydin K, Balci S, Sencer S, Barburoglu M, Umutlu MR, Arat A. Y-stent-assisted coiling with low-profile Neuroform atlas stents for endovascular treatment of wide-necked complex intracranial bifurcation aneurysms. Neurosurgery. 2019:nyz516 https://doi.org/10.1093/neuros/nyz516. 17

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Aydin K, Stracke P, Barburoglu M, Yamac E, Berdikhojaayev M, Sencer S, Chapot R. Long-term outcomes of wide-necked intracranial bifurcation aneurysms treated with T-stent-assisted coiling. J Neurosurg. 2019:1-10. https://doi.org/10.3171/2019.9.JNS1911733.

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Bartolini B, Blanc R, Pistocchi S, Redjem H, Piotin M. “Y” and “X” stent-assisted coiling of complex and wide-neck intracranial bifurcation aneurysms. AJNR Am J Neuroradiol. 2015;35:2153-2158. https://doi.org/10.3174/ajnr.A4060. Brassel F, Melber K, Schlunz-Hendann M, Meila D. Kissing-Y stenting for

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endovascular treatment of complex wide necked bifurcation aneurysms using Acandis

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Acclino stents: results and literature review. J Neurointerv Surg. 2016;8:386-395.

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10. Cagnazzo F, Limbucci N, Nappini S, Renieri L, Rosi A, Laiso A, Tiziano di Carlo D,

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Perrini P, Mangiafico S. Y-stent-assisted coiling of wide-neck bifurcation intracranial aneurysms: a meta-analysis. AJNR Am J Neuroradiol. 2019;40:122-128.

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11. Fargen KM, Mocco J, Neal D, Dewan MC, Reavey-Cantwell J, Woo HH, Fiorella DJ, Mokin M, Siddiqui AH, Turk AS, Turner RD, Chaudry I, Kalani MY, Albuquerque F, Hoh BL. A multicenter study of stent-assisted coiling of cerebral aneurysms with a Y configuration. Neurosurgery. 2013;73:466-472. https://doi.org/10.1227/NEU.0000000000000015. 12. Jankowitz BT, Thomas A, Jovin T, Horowitz M. Y stenting using kissing stents for the treatment of bifurcation aneurysms. J Neurointerv Surg. 2012;4:16-21. https://doi.org/10.1136/jnis.2010.004275. 13. Spiotta AM, Gupta R, Fiorella D, Gonugunta V, Lobo B, Rasmussen PA, Moskowitz SI. Mid-term results of endovascular coiling of wide-necked aneurysms using double stents in a Y configuration. Neurosurgery. 2011;69:421-429. 18

https://doi.org/10.1227/NEU.0b013e318214abbd. 14. Yavuz K, Geyik S, Cekirge S, Saatci I. Double stent-assisted coil embolization treatment for bifurcation aneurysms: immediate treatment results and long-term angiographic outcome. AJNR Am J Neuroradiol. 2013;34:1778-1784. https://doi.org/10.3174/ajnr.A3464 15. Zhao KJ, Yang PF, Huang QH, Li Q, Zhao WY, Liu JM, Hong B. Y-configuration stent placement (crossing and kissing) for endovascular treatment of wide-neck cerebral

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aneurysms located at 4 different bifurcation sites. AJNR Am J Neuroradiol.

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17. Melber K, Meila D, Draheim P, Grieb D, Greling B, Schlunz-Hendann M, Brassel F. Vascular angular remodeling by kissing-Y stenting in wide necked intracranial

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bifurcation aneurysms. J Neurointerv Surg. 2017;9:1233-1237.

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https://doi.org/10.1136/neurointsurg-2016-012858. 18. Mascitelli JR, Moyle H, Oermann EK, Polykarpou MF, Patel AA, Doshi AH, Gologorsky Y, Bederson JB, Patel AB. An update to the Raymond-Roy occlusion classification of intracranial aneurysms treated with coil embolization. J Neurointerv Surg. 2015;7:496-502. https://doi.org/10.1136/neurointsurg-2014-011258. 19. Chow MM, Woo HH, Masaryk TJ, Rasmussen PA. A novel endovascular treatment of a wide-necked basilar apex aneurysm by using a Y-configuration, double-stent technique. AJNR Am J Neuroradiol 2004;25:509-512. 20. Sze DY, Razavi MK, Mitri RK, Regala AC, Dake MD. The “Y” stent: a technique using nitinol stents to treat bifurcations. J Endovasc Ther. 2003;10:780-787. https://doi.org/10.1177//152660280301000415. 19

21. Canton G, Levy DI, Lasheras JC. Hemodynamic changes due to stent placement in bifurcating intracranial aneurysms. J Neurosurg. 2005;103:146-155. https://doi.org/10.3171/jns.2005.103.1.0146. 22. Gao B, Baharoglu MI, Cohen AD, Malek AM. Y-stent coiling of basilar bifurcation aneurysms induces a dynamic angular vascular remodeling with alteration of the apical wall shear stress pattern. Neurosurgery. 2013;72:617-629. https://doi.org/10.1227//NEU.0b013e3182846d9f.

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24. Bain M, Hussain MS, Spiotta A, Gonugunta V, Moskowitz S, Gupta R. “Double-Barrel”

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Figure legends Figure 1. Experimental model of kissing-Y (A) and crossing-Y (B) configuration stentings.

Figure 2. A and B, Initial three-dimensional (3D) reconstructed images show the left, wide-necked, large internal carotid artery (ICA) bifurcation aneurysm. 3D image (C) and cross-sectional image (D) of the cone-beam computed tomography angiogram demonstrate the kissing-Y configuration of two stents, the coil delivery microcatheter, and the lumens of

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two stents in the ICA. E and F, Angiograms obtained immediately after intra-aneurysmal

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coil embolization. Arrowheads in E indicate edge markers of each stent. G and H, Digital

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subtraction angiograms obtained 12 months after the procedure demonstrate complete

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occlusion of the aneurysm and patency of the stents.

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Figure 3. A and B, Initial digital subtraction angiograms (DSAs) show the right, wide-necked, large middle cerebral artery bifurcation aneurysm with a bleb. C, Cone-beam

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computed tomography angiogram showing crossing-Y configuration of two stents, two coil

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delivery microcatheters via a trans-cell (white arrowhead) and jailing technique (white arrow). D, Angiograms obtained immediately after intra-aneurysmal coil embolization with the double catheter technique. Arrowheads indicate edge markers of each stent. E and F, The final DSAs demonstrate adequate occlusion of the aneurysm.

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Table 3. Clinical Outcomes Total

Kissing-Y

Crossing-Y

38

19

19

Good (0-2)

31 (81.6%)

15 (78.9%)

16 (84.2%)

Poor (3-6)

7 (18.4%)

4 (21.1%)

3 (15.8%)

n

P value

Clinical Outcomes (Modified Rankin Scale)

Reasons of Poor Outcome 1

Rerupture of treated aneurysm

1

Brainstem compression by treated aneurysm

1

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Procedure-related cerebral infarction

Primary brain damage due to SAH

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Medical complications

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Abbreviations: SAH, subarachnoid hemorrhage

1

1 1 1

0.677

Table 1. Baseline Characteristics Total

Kissing-Y

38

n

19

Crossing-Y

P value

19

Patient 68.4±11.2

69.1±11. 2

67.7±11.5

0.703

Symptom

15 (39.5%)

8 (42.1%)

7 (36.8%)

0.740

Subarachnoid hemorrhage

8 (21.1%)

3 (15.8%)

5 (26.3%)

Headache

4 (10.5%)

2 (10.5%)

2 (10.5%)

Hydrocephalus

2 (5.3%)

1 (5.3%)

1 (5.3%)

Visual disturbance

1 (2.6%)

1 (5.3%)

0

Oculomotor palsy

1 (2.6%)

1 (5.3%)

0

Asymptomatic

23(60.5%)

11 (57.9%)

12 (63.2%)

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Age (mean±S.D., years)

Aneurysm

11 (28.9%)

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Ruptured

27 (71.1%)

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Unruptured Location

16 (84.2%)

8 (42.1%) 11 (57.9%)

0.074

17 (44.7%)

7 (36.8%)

10 (52.6%)

8 (21.1%)

8 (42.1%)

0

5 (13.2%)

4 (21.1%)

1 (5.3%)

5 (13.2%)

0

5 (26.3%)

MCA bifurcation

3 (7.9%)

0

3 (15.8%)

Max. diameter (mean±S.D., mm)

11.5±4.3

13.0±4.6

10.0±3.5

0.027*

Neck size

7.4±2.5

8.2±2.7

6.6±2.0

0.049*

Dome-to-neck ratio

1.6±0.3

1.6±0.3

1.5±0.3

0.364

Parent diameter (mean±S.D., mm)

3.9±0.7

4.3±0.5

3.5±0.6

<.001*

Daughter diameter (mean±S.D., mm)

2.6±0.5

2.7±0.5

2.4±0.5

0.08

Preceding AN treatment

10 (26.3%)

4 (21.1%)

6 (31.6%)

Coiling

4 (10.5%)

2 (10.5%)

2 (10.5%)

Stent-assisted coiling

3 (7.9%)

0

3 (15.8%)

Clipping

3 (7.9%)

2 (10.5%)

1 (5.3%)

PcomA

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ICA bifurcation

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BA bifurcation

3 (15.8%)

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AcomA

*statistically significant Abbreviations: BA, basilar artery; PcomA, posterior communicating artery; ICA, internal carotid artery; AcomA, anterior communicating artery; MCA, middle cerebral artery; Max.diameter, maximum diameter; AN, 1

0.002*

0.461

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aneurysm

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Table 2. Endovascular Treatment and Angiographic Results Total

Kissing-Y

Crossing-Y

P value

38

19

19

Emergent

7 (18.4%)

3 (15.8%)

4 (23.5%)

0.675

Local Anesthesia

5 (13.2%)

3 (15.8%)

2 (10.5%)

0.631

Asymmetrical Y-stenting

12 (31.6%)

7 (36.8%)

5 (26.3%)

0.485

Stent (n)

76

38

38

Closed-cell

16 (21.1%)

15 (39.5%)

1 (2.6%)

Open-cell

50 (65.8%)

15 (39.5%)

35 (92.1%)

8 (21.1%)

2 (5.3%)

18 (94.7%)

6 (31.6%)

1 (5.3%)

10 (52.6%)

3 (7.9%)

0

3 (15.8%)

9 (23.7%)

6 (31.6%)

3 (15.8%)

4 (7.9%)

2 (10.5%)

2 (10.5%)

Convexity SAH

3 (7.9%)

2 (10.5%)

1 (5.3%)

Stent migration

1 (2.6%)

1 (5.3%)

0

Re-rupture

1 (2.6%)

1 (5.3%)

0

Retreatment

2 (5.3%)

1 (5.3%)

1 (5.3%)

Class Ⅰ

7 (18.4%)

4 (21.1%)

3 (15.8%)

Class Ⅱ

14 (36.8%)

7 (36.8%)

7 (36.8%)

Class Ⅲa

12 (31.6%)

4 (21.1%)

8 (42.1%)

Class Ⅲb

5 (13.2%)

4 (21.1%)

1 (5.3%)

Adequate occlusion

21

11

10 (52.6%)

n

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10

Braded

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Procedure

(13.2%)

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Coil-delivery Microcatheter

24 (63.2%)

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Jailing

11

Complications

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In-stent thrombosis

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Combined

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Trans-cell

(28.9%)

0.002*

0.003*

0.249

Angiographic Results (Modified Raymond-Roy Scale) Immediately after endovascular procedure

1

0.732

(55.3%)

(57.9%)

Adequate occlusion

27 (77.1%)

14 (77.8%)

13 (76.5%)

Body filling

8 (22.9%)

4 (22.2%)

4 (23.5%)

Follow-up (mean 15.8 months)

*statistically significant Modified Raymond-Roy classification Class Ⅰ: complete obliteration Class Ⅱ: residual neck Class Ⅲa: residual aneurysm with contrast within coil interstices

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Class Ⅲb: residual aneurysm with contrast along aneurysm wall Abbreviations: SAH, subarachnoid hemorrhage

2

0.927

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Abbreviations: AcomA, anterior communicating artery AN, aneurysm BA, basilar artery ICA, internal carotid artery MCA, middle cerebral artery mRR, modified Raymond-Roy

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mRS, modified Rankin scale

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PcomA, posterior communicating artery

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SAH, subarachnoid hemorrhage

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Declaration of interests ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: