Perforating artery injury as a critical factor besides cortical dysfunction in motor deficit after peri-rolandic epilepsy surgery.

IF 3.5 2区 医学 Q1 CLINICAL NEUROLOGY
Atsuhiko Ninomiya, Shin-Ichiro Osawa, Kyoko Suzuki, Kazuo Kakinuma, Kazushi Ukishiro, Yoshiteru Shimoda, Kazutaka Jin, Mitsugu Uematsu, Shiho Sato, Shunji Mugikura, Hiroyoshi Suzuki, Hajime Miyata, Shingo Kayano, Nobukazu Nakasato, Hidenori Endo
{"title":"Perforating artery injury as a critical factor besides cortical dysfunction in motor deficit after peri-rolandic epilepsy surgery.","authors":"Atsuhiko Ninomiya, Shin-Ichiro Osawa, Kyoko Suzuki, Kazuo Kakinuma, Kazushi Ukishiro, Yoshiteru Shimoda, Kazutaka Jin, Mitsugu Uematsu, Shiho Sato, Shunji Mugikura, Hiroyoshi Suzuki, Hajime Miyata, Shingo Kayano, Nobukazu Nakasato, Hidenori Endo","doi":"10.3171/2024.10.JNS24878","DOIUrl":null,"url":null,"abstract":"<p><strong>Objective: </strong>Surgery for peri-rolandic epilepsy requires appropriate consideration to balance the functional risk of postoperative motor deficit and seizure outcome. Based on voxel-based morphometric analysis, the authors hypothesized that cortical damage and ischemic subcortical damage related to surgery could affect postoperative motor deterioration.</p><p><strong>Methods: </strong>Sixteen patients with peri-rolandic epilepsy who underwent resective surgery at a single institution were retrospectively investigated. Their imaging findings, postoperative seizure outcomes, and postoperative neurological deteriorations in motor function, as well as duration, were analyzed. Using the standardized MRI data of each case, the authors examined the surgically resected area on high-resolution 3D MR images and the high-intensity area on diffusion-weighted images, which were converted to voxel data. These voxel data were superimposed on a standard brain image for neuroimaging assessment. Postoperative motor deterioration of the orofacial region, upper limb, or lower limb was noted as no, transient, or permanent deterioration and analyzed in relation to the surgically resected area and subcortical damage. Univariate analysis of the clinical factors was conducted between cases with permanent upper- and/or lower-limb motor deterioration and those with no or transient deterioration.</p><p><strong>Results: </strong>The mean follow-up period was 28 months. Ten patients (62.5%) achieved Engel class I. Fourteen patients (87.5%) experienced postoperative motor deteriorations in the following areas (no/transient/permanent): orofacial (11/5/0), upper limb (9/5/2), and lower limb (9/3/4). All cases with orofacial motor deterioration underwent cortical resection of the inferior third of the peri-rolandic cortex. Cortical resection of the precentral gyrus only, in contrast to both the precentral and postcentral gyri, was not associated with permanent upper- and/or lower-limb motor deterioration. Cortical resection involving the postcentral gyrus was significantly associated with permanent upper- and/or lower-limb motor deterioration in 4 cases (25.0%). Surgically related perforating artery injury caused ischemic subcortical damage, which was significantly associated with postoperative transient or permanent motor deterioration by extending to the corticospinal tract (CST).</p><p><strong>Conclusions: </strong>Postoperative motor deterioration for peri-rolandic epilepsy was related to both the resected cortex and ischemic subcortical damage. In peri-rolandic epilepsy, cortical resection of the precentral gyrus might not necessarily cause permanent upper- and/or lower-limb motor deterioration because of the functional reserve in other peri-rolandic areas outside the epileptic focus. On the other hand, cortical resection of the postcentral gyrus could cause permanent upper- and/or lower-limb motor deterioration because of injury to the vasculature, which is crucial for the descending motor pathway in the CST.</p>","PeriodicalId":16505,"journal":{"name":"Journal of neurosurgery","volume":" ","pages":"1-13"},"PeriodicalIF":3.5000,"publicationDate":"2025-02-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of neurosurgery","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.3171/2024.10.JNS24878","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Objective: Surgery for peri-rolandic epilepsy requires appropriate consideration to balance the functional risk of postoperative motor deficit and seizure outcome. Based on voxel-based morphometric analysis, the authors hypothesized that cortical damage and ischemic subcortical damage related to surgery could affect postoperative motor deterioration.

Methods: Sixteen patients with peri-rolandic epilepsy who underwent resective surgery at a single institution were retrospectively investigated. Their imaging findings, postoperative seizure outcomes, and postoperative neurological deteriorations in motor function, as well as duration, were analyzed. Using the standardized MRI data of each case, the authors examined the surgically resected area on high-resolution 3D MR images and the high-intensity area on diffusion-weighted images, which were converted to voxel data. These voxel data were superimposed on a standard brain image for neuroimaging assessment. Postoperative motor deterioration of the orofacial region, upper limb, or lower limb was noted as no, transient, or permanent deterioration and analyzed in relation to the surgically resected area and subcortical damage. Univariate analysis of the clinical factors was conducted between cases with permanent upper- and/or lower-limb motor deterioration and those with no or transient deterioration.

Results: The mean follow-up period was 28 months. Ten patients (62.5%) achieved Engel class I. Fourteen patients (87.5%) experienced postoperative motor deteriorations in the following areas (no/transient/permanent): orofacial (11/5/0), upper limb (9/5/2), and lower limb (9/3/4). All cases with orofacial motor deterioration underwent cortical resection of the inferior third of the peri-rolandic cortex. Cortical resection of the precentral gyrus only, in contrast to both the precentral and postcentral gyri, was not associated with permanent upper- and/or lower-limb motor deterioration. Cortical resection involving the postcentral gyrus was significantly associated with permanent upper- and/or lower-limb motor deterioration in 4 cases (25.0%). Surgically related perforating artery injury caused ischemic subcortical damage, which was significantly associated with postoperative transient or permanent motor deterioration by extending to the corticospinal tract (CST).

Conclusions: Postoperative motor deterioration for peri-rolandic epilepsy was related to both the resected cortex and ischemic subcortical damage. In peri-rolandic epilepsy, cortical resection of the precentral gyrus might not necessarily cause permanent upper- and/or lower-limb motor deterioration because of the functional reserve in other peri-rolandic areas outside the epileptic focus. On the other hand, cortical resection of the postcentral gyrus could cause permanent upper- and/or lower-limb motor deterioration because of injury to the vasculature, which is crucial for the descending motor pathway in the CST.

除皮质功能障碍外,穿动脉损伤是罗兰周围癫痫术后运动障碍的关键因素。
目的:罗兰周围癫痫手术需要适当考虑平衡术后运动缺陷和癫痫发作结果的功能风险。基于体素的形态学分析,作者假设手术相关的皮质损伤和缺血性皮质下损伤可能影响术后运动恶化。方法:对在同一医院行切除手术的16例罗兰周围癫痫患者进行回顾性研究。我们分析了他们的影像学表现、术后癫痫发作结果、术后运动功能的神经功能恶化以及持续时间。利用每个病例的标准化MRI数据,作者在高分辨率3D MR图像上检查手术切除区域,在弥散加权图像上检查高强度区域,并将其转换为体素数据。这些体素数据被叠加在标准脑图像上用于神经成像评估。术后口面区、上肢或下肢的运动恶化分为无、短暂或永久性恶化,并分析与手术切除区域和皮质下损伤的关系。对永久性上肢和/或下肢运动恶化的病例和无或短暂性恶化的病例进行临床因素的单因素分析。结果:平均随访28个月。10例患者(62.5%)达到Engel i级。术后14例患者(87.5%)出现以下部位的运动恶化(无/短暂/永久性):口面部(11/5/0)、上肢(9/5/2)和下肢(9/3/4)。所有出现口面部运动恶化的病例均行下三分之一的罗兰周围皮质皮质切除术。与中央前回和中央后回相比,仅皮质切除中央前回与永久性上肢和/或下肢运动恶化无关。在4例(25.0%)患者中,累及中央后回的皮质切除术与永久性上肢和/或下肢运动恶化显著相关。手术相关穿通动脉损伤引起缺血性皮质下损伤,其与术后短暂或永久性运动功能恶化显著相关,并延伸至皮质脊髓束(CST)。结论:罗兰周癫痫术后运动功能恶化与切除的皮质和皮质下缺血性损伤有关。在罗兰周围癫痫中,皮质切除中央前回不一定会导致永久性的上肢和/或下肢运动恶化,因为癫痫病灶外的其他罗兰周围区域有功能储备。另一方面,由于脉管系统损伤,皮质切除中央后回可能导致永久性上肢和/或下肢运动恶化,而脉管系统损伤对CST的下行运动通路至关重要。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Journal of neurosurgery
Journal of neurosurgery 医学-临床神经学
CiteScore
7.20
自引率
7.30%
发文量
1003
审稿时长
1 months
期刊介绍: The Journal of Neurosurgery, Journal of Neurosurgery: Spine, Journal of Neurosurgery: Pediatrics, and Neurosurgical Focus are devoted to the publication of original works relating primarily to neurosurgery, including studies in clinical neurophysiology, organic neurology, ophthalmology, radiology, pathology, and molecular biology. The Editors and Editorial Boards encourage submission of clinical and laboratory studies. Other manuscripts accepted for review include technical notes on instruments or equipment that are innovative or useful to clinicians and researchers in the field of neuroscience; papers describing unusual cases; manuscripts on historical persons or events related to neurosurgery; and in Neurosurgical Focus, occasional reviews. Letters to the Editor commenting on articles recently published in the Journal of Neurosurgery, Journal of Neurosurgery: Spine, and Journal of Neurosurgery: Pediatrics are welcome.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信