Altered structural network in temporal lobe epilepsy with focal to bilateral tonic–clonic seizures

IF 4.4 2区 医学 Q1 CLINICAL NEUROLOGY
Yi Ge, Cong Chen, Hong Li, Ruyi Wang, Yuyu Yang, Lingqi Ye, Chenmin He, Ruotong Chen, Zijian Wang, Xiaotong Shao, Yuting Gong, Linglin Yang, Shan Wang, Jiping Zhou, Xunyi Wu, Shuang Wang, Yao Ding
{"title":"Altered structural network in temporal lobe epilepsy with focal to bilateral tonic–clonic seizures","authors":"Yi Ge,&nbsp;Cong Chen,&nbsp;Hong Li,&nbsp;Ruyi Wang,&nbsp;Yuyu Yang,&nbsp;Lingqi Ye,&nbsp;Chenmin He,&nbsp;Ruotong Chen,&nbsp;Zijian Wang,&nbsp;Xiaotong Shao,&nbsp;Yuting Gong,&nbsp;Linglin Yang,&nbsp;Shan Wang,&nbsp;Jiping Zhou,&nbsp;Xunyi Wu,&nbsp;Shuang Wang,&nbsp;Yao Ding","doi":"10.1002/acn3.52135","DOIUrl":null,"url":null,"abstract":"<div>\n \n \n <section>\n \n <h3> Objectives</h3>\n \n <p>This study aims to investigate whether alterations in white matter topological networks are associated with focal to bilateral tonic–clonic seizures (FBTCS) in temporal lobe epilepsy (TLE). Additionally, we investigated the variables contributing to memory impairment in TLE.</p>\n </section>\n \n <section>\n \n <h3> Methods</h3>\n \n <p>This cross-sectional study included 88 unilateral people with TLE (45 left/43 right), and 42 healthy controls. Graph theory analysis was employed to compare the FBTCS (+) group (<i>n</i> = 51) with the FBTCS (−) group (<i>n</i> = 37). The FBTCS (+) group was subcategorized into current-FBTCS (<i>n</i> = 31) and remote-FBTCS (<i>n</i> = 20), based on the history of FBTCS within 1 year or longer than 1 year before scanning, respectively. We evaluated the discriminatory power of topological network properties by receiver operating characteristic (ROC) analysis. Generalized linear models (GLMs) were employed to investigate variables associated with memory impairment in TLE.</p>\n </section>\n \n <section>\n \n <h3> Results</h3>\n \n <p>Global efficiency (Eg) was significantly reduced in the FBTCS (+) group, especially in the current-FBTCS subgroup. Greater disruption of regional properties in the ipsilateral occipital and temporal association cortices was observed in the FBTCS (+) group. ROC analysis revealed that Eg, normalized characteristic shortest path length, and nodal efficiency of the ipsilateral middle temporal gyrus could distinguish between FBTCS (+) and FBTCS (−) groups. Additionally, GLMs linked the occurrence of current FBTCS with poorer verbal memory outcomes in TLE.</p>\n </section>\n \n <section>\n \n <h3> Interpretation</h3>\n \n <p>Our study suggests that abnormal networks could be the structural basis of seizure propagation in FBTCS. Strategies aimed at reducing the occurrence of FBTCS could potentially improve the memory outcomes in people with TLE.</p>\n </section>\n </div>","PeriodicalId":126,"journal":{"name":"Annals of Clinical and Translational Neurology","volume":null,"pages":null},"PeriodicalIF":4.4000,"publicationDate":"2024-08-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/acn3.52135","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Annals of Clinical and Translational Neurology","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/acn3.52135","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

Objectives

This study aims to investigate whether alterations in white matter topological networks are associated with focal to bilateral tonic–clonic seizures (FBTCS) in temporal lobe epilepsy (TLE). Additionally, we investigated the variables contributing to memory impairment in TLE.

Methods

This cross-sectional study included 88 unilateral people with TLE (45 left/43 right), and 42 healthy controls. Graph theory analysis was employed to compare the FBTCS (+) group (n = 51) with the FBTCS (−) group (n = 37). The FBTCS (+) group was subcategorized into current-FBTCS (n = 31) and remote-FBTCS (n = 20), based on the history of FBTCS within 1 year or longer than 1 year before scanning, respectively. We evaluated the discriminatory power of topological network properties by receiver operating characteristic (ROC) analysis. Generalized linear models (GLMs) were employed to investigate variables associated with memory impairment in TLE.

Results

Global efficiency (Eg) was significantly reduced in the FBTCS (+) group, especially in the current-FBTCS subgroup. Greater disruption of regional properties in the ipsilateral occipital and temporal association cortices was observed in the FBTCS (+) group. ROC analysis revealed that Eg, normalized characteristic shortest path length, and nodal efficiency of the ipsilateral middle temporal gyrus could distinguish between FBTCS (+) and FBTCS (−) groups. Additionally, GLMs linked the occurrence of current FBTCS with poorer verbal memory outcomes in TLE.

Interpretation

Our study suggests that abnormal networks could be the structural basis of seizure propagation in FBTCS. Strategies aimed at reducing the occurrence of FBTCS could potentially improve the memory outcomes in people with TLE.

Abstract Image

颞叶癫痫伴局灶至双侧强直阵挛发作的结构网络改变。
研究目的本研究旨在探讨白质拓扑网络的改变是否与颞叶癫痫(TLE)的局灶至双侧强直阵挛发作(FBTCS)有关。此外,我们还调查了导致颞叶癫痫患者记忆障碍的变量:这项横断面研究包括88名单侧TLE患者(45名左侧/43名右侧)和42名健康对照者。采用图论分析法对FBTCS(+)组(n = 51)和FBTCS(-)组(n = 37)进行比较。根据扫描前 1 年内或超过 1 年的 FBTCS 病史,FBTCS(+)组又分为当前 FBTCS 组(n = 31)和远程 FBTCS 组(n = 20)。我们通过接收器操作特征(ROC)分析评估了拓扑网络特性的判别能力。我们采用了广义线性模型(GLM)来研究与TLE记忆损伤相关的变量:结果:FBTCS(+)组的全局效率(Eg)明显降低,尤其是在当前-FBTCS亚组中。在FBTCS(+)组中,同侧枕叶和颞叶联想皮层的区域特性受到了更大的破坏。ROC分析显示,同侧颞中回的Eg、归一化特征最短路径长度和结节效率可以区分FBTCS(+)组和FBTCS(-)组。此外,GLMs将当前FBTCS的发生与TLE患者较差的言语记忆结果联系起来:我们的研究表明,异常网络可能是 FBTCS 中癫痫发作传播的结构基础。旨在减少FBTCS发生的策略有可能改善TLE患者的记忆效果。
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
Annals of Clinical and Translational Neurology
Annals of Clinical and Translational Neurology Medicine-Neurology (clinical)
CiteScore
9.10
自引率
1.90%
发文量
218
审稿时长
8 weeks
期刊介绍: Annals of Clinical and Translational Neurology is a peer-reviewed journal for rapid dissemination of high-quality research related to all areas of neurology. The journal publishes original research and scholarly reviews focused on the mechanisms and treatments of diseases of the nervous system; high-impact topics in neurologic education; and other topics of interest to the clinical neuroscience community.
×
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