Long-term outcome of intracranial-intracranial side-to-side bypass for complex intracranial aneurysms

doi:10.3969/j.issn.1672-6731.2024.08.007

Abstract

Abstract:

Objective: To explore the long-term outcome of intracranial-intracranial side-to-side bypass for complex intracranial aneurysms. Methods: Five patients with complex intracranial aneurysms underwent intracranial-intracranial side-to-side bypass performed by the same surgeon at The First Hospital of China Medical University from January 2015 to December 2023 were included. Two cases involved the A2 segment of anterior cerebral artery (ACA) and 3 cases involved the M2 segment of middle cerebral artery (MCA). Indocyanine green angiography (ICGA) was used intraoperatively, and CTA or DSA was used postoperatively to evaluate aneurysm occlusion and blood flow reconstruction. The modified Rankin Scale (mRS) was used to evaluate the neurological prognosis at one week, 3 months and the last follow-up. CT/ MRI examination was completed on the first day, one week and 3 months after operation to evaluate whether hemorrhagic or ischemic complications occurred. Results: Five cases of complex intracranial aneurysms were all occluded accurately. Two cases underwent A3-A3 side-to-side anastomosis, and 3 cases underwent M2-M2 side-to-side anastomosis, among which one case added M1-radial artery (RA)-M2 intracranial-intracranial bypass with RA as graft on the basis of M2-M2 side-to-side anastomosis. During the operation, ICGA confirmed that the side-to-side anastomosis and M1-RA-M2 bypass were unobstructed in 5 cases. The postoperative follow-up time was 23 (14, 71) months. No aneurysm was found in cerebrovascular imaging examination one week and 3 months after operation in 5 patients, and 9 to 12 months after operation in 3 patients. Five side-to-side anastomosis stomas and one M1-RA-M2 graft were all unobstructed. At one week after operation, the mRS increased by 0-3 score compared with that before operation (4 score maintained unchanged before and after operation in one case, 2 score increased in one case, and 3 score increased in one case). In 2 unruptured cases, the mRS score was 1 score at one week after operation, and there was no change from that before operation. At 3 months after operation, the mRS scores of 5 cases were decreased (2 cases with 0 score, one case with 2 score, and 2 cases with 3 score); one case was lost at the last follow-up, and the mRS scores of other 4 cases decreased further (2 cases with 0 score, one case with 1 score, and one case with 2 score). No cerebral hemorrhage or cerebral ischemia occurred in the follow-up. Conclusions: Intracranial-intracranial side-to-side bypass has good short-term and long-term patency and stable long-term clinical effect. It is a reliable technique for surgical treatment of complex intracranial aneurysms.

Key words: Intracranial aneurysm, Anterior cerebral artery, Middle cerebral artery, Cerebral revascularization, Intracranial-intracranial (not in MeSH), Side-to-side anastomosis (not in MeSH)

摘要：

目的: 探讨颅内-颅内血管搭桥侧侧吻合术治疗复杂颅内动脉瘤的长期疗效。方法: 纳入2015年1月至2023年12月由中国医科大学附属第一医院神经外科同一术者实施颅内-颅内血管搭桥侧侧吻合术的5例复杂颅内动脉瘤患者，2例累及大脑前动脉A2段，3例累及大脑中动脉M2段。术中采用吲哚菁绿荧光血管造影术（ICGA）、术后采用CTA或DSA评估动脉瘤闭塞和血流重建情况；术后1周、3个月和末次随访时采用改良Rankin量表（mRS）评估神经功能预后；术后第1天、1周和3个月行头部CT和（或）MRI检查，评估是否发生出血性或缺血性并发症。结果: 本组5例复杂颅内动脉瘤均孤立确切，2例行A3-A3侧侧吻合术；3例行M2-M2侧侧吻合术，其中1例在M2-M2侧侧吻合术基础上获取桡动脉（RA）作为桥血管，联合M1-RA-M2嵌入桥接式血管搭桥术。术中经ICGA证实，5例侧侧吻合口和1例M1-RA-M2桥血管均通畅。术后随访时间为23（14，71）个月，5例术后1周和术后3个月CTA或DSA检查、3例术后9~12个月DSA检查均未见动脉瘤显影，5例侧侧吻合口和1例M1-RA-M2桥血管均通畅。术后1周mRS评分较术前升高0~3分（1例手术前后均为4分、1例增加2分、1例增加3分），2例未破裂患者术后1周mRS评分无变化（均为1分）；术后3个月mRS评分均下降（0分2例、2分1例、3分2例）；末次随访时1例失访，余4例mRS评分进一步下降（0分2例、1分1例、2分1例）。术后无脑出血或脑缺血事件发生。结论: 颅内-颅内血管搭桥侧侧吻合术的短期和长期通畅性良好，长期疗效稳定，是复杂颅内动脉瘤手术治疗的可靠技术。

关键词: 颅内动脉瘤, 大脑前动脉, 大脑中动脉, 脑血管重建术, 颅内-颅内（非MeSH词）, 侧侧吻合（非MeSH词）

Yuan LIU, Zhi-yong TONG, Guan-dong YU, Xu-dong ZHAO, Jin-gang CHU. Long-term outcome of intracranial-intracranial side-to-side bypass for complex intracranial aneurysms[J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(8): 632-643.

刘源, 佟志勇, 余冠东, 赵旭东, 初金刚. 颅内-颅内血管搭桥侧侧吻合术治疗复杂颅内动脉瘤长期疗效观察[J]. 中国现代神经疾病杂志, 2024, 24(8): 632-643.

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Figures/Tables 8

Table 1. Features, operative methods of 5 cases with complex intracranial aneurysms treated by intracranial⁃intracranial side⁃to⁃side bypass

序号	性别	年龄（岁）	动脉瘤出血时间	术前mRS(评分)	动脉瘤部位	动脉瘤性质	合并其他部位动脉瘤	手术日期	手术入路	搭桥方式
1	男性	57	1周	4	右ACA A2段	解离性	右ACA A2段近端及远端2个小动脉瘤	2015年5月	双额经纵裂	侧侧吻合术（A3-A3）
2	男性	52	6年	1	右ACA A2段	解离性	右ICA-PCoA交界处微小动脉瘤；右MCA M1段解离性动脉瘤	2018年8月	双额经纵裂+ 右侧翼点	侧侧吻合术$(A 3-A 3)$
3	女性	59	未破裂	1	左MCA M2段上干	动脉畸形	右ICA颈动脉窝动脉瘤	2022年7月	左侧扩大翼点	侧侧吻合术(M2-M2)
4	女性	16	未破裂	1	左MCA M2段上干	解离性	无	2023年4月	左侧额欺眶颧	侧侧吻合术(M2-M2)
5	女性	47	1周	1	右MCA M2段上干和下干	解离性	左MCA M2段微小动脉瘤	2023年11月	右侧扩大翼点	侧侧吻合术(M2-M2) + M1-RA-M2搭桥术

Figure 1 Imaging findings before and after surgery and intraoperative findings of Case 1 Preoperative axial CT showed longitudinal fissure hematoma (arrow indicates, Panel 1a). Bilateral anteroposterior DSA (Panel 1b) and DSA 3D volume reconstruction (Panel 1c) showed 3 aneurysms on the A2 segment to A3 segment of right ACA, the second of which was a dissociation aneurysm. Three aneurysms from proximal to distal ends of right ACA were revealed under microscope (Panel 1d-1f). The left side A3 and the right side A3 distal to the distal aneurysm were revealed, and both of them were more atherosclerotic (Panel 1g). Bilateral A3 side - to - side anastomosis was completed (Panel 1h). Right A2 dissociated aneurysm was occluded and distal aneurysm was clipped (Panel 1i). Bilateral anteroposterior DSA one week after operation (Panel 1j), anteroposterior CTA 3D volume reconstruction (Panel 1k) and left lateral CTA 3D volume reconstruction (Panel 1l) 3 months after operation showed the A3 - A3 side - to - side anastomotic stoma was unblocked, and the aneurysm was not shown.

Figure 2 Imaging findings before and after surgery and intraoperative findings of Case 2 Preoperative axial T₂WI showed local dilatation of the right ACA and MCA (arrows indicate, Panel 2a). Preoperative VW -HRMRI showed local dilatation of the right ACA and thickening of the vessel wall with enhancement (arrow indicates, Panel 2b). MIP (Panel 2c) and DSA 3D volume reconstruction (Panel 2d) showed the A2 segment of right ACA dilatation, one aneurysm in right MCA, and one microaneurysm in right ICA - PCoA (arrows indicate). Free adjacent parallel bilateral A3 (Panel 2e). After temporary blockade, bilateral A3 were incised and stained by methylene blue, and then the ventral side of the side - to - side anastomosis was continuously sutured (Panel 2f). Complete A3 - A3 side - to - side anastomosis and release temporary blockade (Panel 2g). Right lateral CTA 3D volume reconstruction one week after surgery (Panel 2h), DSA 3D volume reconstruction 3 months (Panel 2i) and 9 months (Panel 2j) after surgery showed the right A2 segment aneurysm disappeared, and the left A3 segment supplied blood to the proximal and distal ends of the right A3 segment through the side-to-side anastomosis.

Figure 3 Imaging findings before and after surgery and intraoperative findings of Case 3 Preoperative axial T₂WI showed aneurysmal dilatation of the left MCA (arrow indicates, Panel 3a). DSA (Panel 3b) and DSA 3D volume reconstruction (Panel 3c) showed tortuous dilatation of the arteries at the beginning of the superior trunk of left M2 segment of MCA (arrows indicate). Microscopically free adjacent distal branch of M2 segment superior trunk and distal segment of M2 segment inferior trunk (Panel 3d). Microscopic confirmation of the proximal and distal ends of the M2 segment arterial malformation (Panel 3e). The M2 segment superior trunk artery malformation was obstructed after M2-M2 side-to-side anastomosis (Panel 3f). Intraoperative ICGA showed that the arterial malformation disappeared, and the side-to-side anastomosis was unobstructed (Panel 3g). Anteroposterior DSA one week after surgery (Panel 3h) and DSA 3D volume reconstruction one year after surgery (Panel 3i) showed the arterial malformation did not recurrent, and the side-to-side anastomosis was unobstructed.

Figure 4 Imaging findings before and after surgery and intraoperative findings of Case 4 Preoperative CTA (Panel 4a), DSA (Panel 4b) and DSA 3D volume reconstruction (background was removed, Panel 4c) showed a dissociated aneurysm at the beginning of the superior trunk branch of M2 segment of left MCA (arrows indicate). A dissociated aneurysm was found at the beginning of the left superior trunk branch of M2 (Panel 4d). Microscopically free distal vessels of M2 segment superior trunk branch aneurysm and M2 segment inferior trunk branch vessels (Panel 4e). Intraoperative ICGA showed patency of side-to-side anastomotic stoma (Panel 4f), and the aneurysm was exactly obstructed (Panel 4g). CTA 3D volume reconstruction on one week (Panel 4h) and 9 months (Panel 4i) after surgery showed the side-to-side anastomosis was unobstructed, and no recurrence of aneurysm was observed.

Figure 5 Imaging findings before and after surgery and intraoperative findings of Case 5 Preoperative axial CT showed SAH in the right lateral fissure (arrow indicates) and old infarction in the right caudate nucleus head (Panel 5a). Anteroposterior DSA showed the M2 segment of right MCA aneurysm involving both superior and inferior trunks (arrow indicates, Panel 5b). The M2 segment aneurysm involved both superior and inferior trunks (Panel 5c). Distal vessels of M2 segment upper and lower trunks were free (Panel 5d). After temporary occlusion to upstream and downstream arteries of anastomosis and adjacent perforator arteries, longitudinal incision and staining with methylene blue were performed (Panel 5e). Intraoperative ICGA showed the side - to - side anastomosis stoma of the M2 superior trunk to the M2 inferior trunk was patent, and the adjacent perforating vessels were preserved (Panel 5f). A 4 cm autologous RA was taken, with which end-to-side anastomosis were performed respectively at the end of M1 and at the proximal end of the previous side-to-side anastomosis stoma, and then trapping of aneurysm was performed (Panel 5g, 5h). Intraoperative ICGA reconfirmed that the M1-RA-M2 superior trunk bypass and the M2 superior trunk-M2 inferior trunk side-to-side anastomosis were unobstructed, and the distal perforating artery of M1 was preserved (Panel 5i). CTA 3D volume reconstruction one week after surgery (Panel 5j), anteroposterior DSA 3 months after surgery (Panel 5k) showed the M1-RA-M2 superior trunk bypass and the M2 superior trunk-M2 inferior trunk side-to-side anastomosis were unobstructed, and the aneurysm was undeveloped.

Table 2. Follow-up of 5 cases with complex intracranial aneurysms treated by intracranial-intracranial side-to-side bypass

序号	末次随访时间	mRS（评分）			动脉瘤闭塞（评估方法）				侧侧吻合口（评估方法）
序号	末次随访时间	术后1周	术后3个月	末次随访	术中	术后1个月	术后3个月	末次影像	术中	术后1个月	术后3个月	末次影像
1	术后110个月	4	3	失访	无残留（切开）	无显影(DSA)	无显影(CTA)	-	通畅（充盈）	通畅（DSA）	通畅(CTA)	-
2	术后71个月	3	2	1	无残留（切开）	无显影(CTA)	无显影（DSA）	术后9个月，未显影（DSA）	(通畅	通畅(CTA)	通畅(DSA)	术后9个月, 通畅（DSA）
3	术后23个月	1	0	0	无残留(ICGA)	无显影(DSA)	无显影(DSA)	术后12个月，未显影（DSA）	通畅(ICGA)	通畅（DSA）	通畅(DSA)	术后12个月通畅（DSA）
4	术后14个月	1	0	0	无残留（ICGA）	无显影(CTA)	无显影（DSA）	术后9个月，未显影（DSA）	通畅(ICGA)	通畅(CTA)	通畅(DSA)	术后9个月, 通畅(DSA)
5	术后8个月	4	3	2	无残留(ICGA)	无显影(CTA)	无显影(DSA)	—	通畅(ICGA)	通畅(CTA)	通畅(DSA)	-

Figure 6 Brain CTP (basal ganglia level) findings 3 months after operation of Case 5 tMIP labelled the perfusion areas of brain tissue on both sides (Panel 6a). CBV showed no significant difference on both sides except for the right basal ganglia (3-R, Panel 6b). CBF showed no significant difference on both sides except for the right basal ganglia (3 - R, Panel 6c). MTT of the right frontal lobe (2-R) was 8 s, which was less than 3 s later than the contralateral lobe (Panel 6d). TTP was approximately 5 s longer in the right frontal lobe (2-R) than in the contralateral lobe (Panel 6e). The time for contrast agent to reach all tissues (Tmax) in the right frontal lobe (2-R) was longer than that in the left side, but still < 6 s (Panel 6f).

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