A universal method for seizure onset zone localization in focal epilepsy using standard deviation of spike amplitude

IF 2 4区 医学 Q3 CLINICAL NEUROLOGY
Xiang Ji , Yuanyuan Dang , Ming Song , Aijun Liu , Hulin Zhao , Tianzi Jiang
{"title":"A universal method for seizure onset zone localization in focal epilepsy using standard deviation of spike amplitude","authors":"Xiang Ji ,&nbsp;Yuanyuan Dang ,&nbsp;Ming Song ,&nbsp;Aijun Liu ,&nbsp;Hulin Zhao ,&nbsp;Tianzi Jiang","doi":"10.1016/j.eplepsyres.2024.107475","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><div>Precisely localizing the seizure onset zone (SOZ) is critical for focal epilepsy surgery. Existing methods mainly focus on high-frequency activities in stereo-electroencephalography, but often fail when seizures are not driven by high-frequency activities. Recognized as biomarkers of epileptic seizures, ictal spikes in SOZ induce epileptiform discharges in other brain regions. Based on this understanding, we aim to develop a universal algorithm to localize SOZ and investigate how ictal spikes within the SOZ induce seizures.</div></div><div><h3>Methods</h3><div>We proposed a novel metric called standard deviation of spike amplitude (SDSA) and utilized channel-averaged SDSA to describe seizure processes and detect seizures. By integrating SDSA values in specific intervals, the score for each channel located within SOZ was calculated. Channels with high SOZ scores were clustered as SOZ. The localization accuracy was asserted using area under the receiver operating characteristic (ROC) curve. Further, we analyzed early ictal signals from SOZ channels and investigated factors influencing their duration to reveal the seizure inducing conditions.</div></div><div><h3>Results</h3><div>We analyzed data from 15 patients with focal epilepsy. The channel-averaged SDSA successfully detected all 28 seizures without false alarms. Using SDSA integration, we achieved precise SOZ localization with an average area under ROC curve (AUC) of 0.96, significantly outperforming previous methods based on high-frequency activities. Further, we discovered that energy of ictal spikes in SOZ was concentrated at a specific frequency distributed in [6, 12 Hz]. Additionally, we found that the higher the energy per second in this frequency band, the faster ictal spikes could induce seizures.</div></div><div><h3>Conclusion</h3><div>The SDSA metric offered precise SOZ localization with robustness and low computational cost, making it suitable for clinical practice. By studying the propagation patterns of ictal spikes between the SOZ and non-SOZ, we suggest that ictal spikes from SOZ need to accumulate energy at a specific central frequency to induce epileptic spikes in non-SOZ, which may have significant implications for understanding the seizure onset pattern.</div></div>","PeriodicalId":11914,"journal":{"name":"Epilepsy Research","volume":"208 ","pages":"Article 107475"},"PeriodicalIF":2.0000,"publicationDate":"2024-11-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Epilepsy Research","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0920121124001906","RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Background

Precisely localizing the seizure onset zone (SOZ) is critical for focal epilepsy surgery. Existing methods mainly focus on high-frequency activities in stereo-electroencephalography, but often fail when seizures are not driven by high-frequency activities. Recognized as biomarkers of epileptic seizures, ictal spikes in SOZ induce epileptiform discharges in other brain regions. Based on this understanding, we aim to develop a universal algorithm to localize SOZ and investigate how ictal spikes within the SOZ induce seizures.

Methods

We proposed a novel metric called standard deviation of spike amplitude (SDSA) and utilized channel-averaged SDSA to describe seizure processes and detect seizures. By integrating SDSA values in specific intervals, the score for each channel located within SOZ was calculated. Channels with high SOZ scores were clustered as SOZ. The localization accuracy was asserted using area under the receiver operating characteristic (ROC) curve. Further, we analyzed early ictal signals from SOZ channels and investigated factors influencing their duration to reveal the seizure inducing conditions.

Results

We analyzed data from 15 patients with focal epilepsy. The channel-averaged SDSA successfully detected all 28 seizures without false alarms. Using SDSA integration, we achieved precise SOZ localization with an average area under ROC curve (AUC) of 0.96, significantly outperforming previous methods based on high-frequency activities. Further, we discovered that energy of ictal spikes in SOZ was concentrated at a specific frequency distributed in [6, 12 Hz]. Additionally, we found that the higher the energy per second in this frequency band, the faster ictal spikes could induce seizures.

Conclusion

The SDSA metric offered precise SOZ localization with robustness and low computational cost, making it suitable for clinical practice. By studying the propagation patterns of ictal spikes between the SOZ and non-SOZ, we suggest that ictal spikes from SOZ need to accumulate energy at a specific central frequency to induce epileptic spikes in non-SOZ, which may have significant implications for understanding the seizure onset pattern.
利用尖峰振幅标准偏差定位局灶性癫痫发作起始区的通用方法
背景精确定位癫痫发作区(SOZ)对局灶性癫痫手术至关重要。现有方法主要关注立体脑电图中的高频活动,但当癫痫发作并非由高频活动驱动时,这些方法往往会失败。作为癫痫发作的生物标志物,SOZ 中的发作性尖峰会诱发其他脑区的痫样放电。基于这一认识,我们旨在开发一种通用算法来定位 SOZ,并研究 SOZ 内的发作性尖峰如何诱发癫痫发作。方法 我们提出了一种名为尖峰振幅标准偏差(SDSA)的新指标,并利用通道平均 SDSA 来描述癫痫发作过程和检测癫痫发作。通过整合特定区间的 SDSA 值,计算出 SOZ 内各通道的得分。SOZ 分数高的通道被归类为 SOZ。利用接收者操作特征曲线(ROC)下的面积来判定定位的准确性。此外,我们还分析了 SOZ 通道的早期发作信号,并研究了影响其持续时间的因素,以揭示癫痫发作的诱发条件。通道平均 SDSA 成功检测到所有 28 次癫痫发作,且无误报。利用 SDSA 集成,我们实现了精确的 SOZ 定位,ROC 曲线下平均面积 (AUC) 为 0.96,明显优于之前基于高频活动的方法。此外,我们还发现 SOZ 中的发作性尖峰能量集中在一个特定的频率上,分布在 [6, 12 Hz]。此外,我们还发现,该频段的每秒能量越高,发作性尖峰诱发癫痫发作的速度就越快。通过研究发作性尖峰在 SOZ 和非 SOZ 之间的传播模式,我们认为来自 SOZ 的发作性尖峰需要在特定的中心频率积累能量才能诱发非 SOZ 的癫痫尖峰,这可能对理解癫痫发作的起始模式具有重要意义。
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
Epilepsy Research
Epilepsy Research 医学-临床神经学
CiteScore
0.10
自引率
4.50%
发文量
143
审稿时长
62 days
期刊介绍: Epilepsy Research provides for publication of high quality articles in both basic and clinical epilepsy research, with a special emphasis on translational research that ultimately relates to epilepsy as a human condition. The journal is intended to provide a forum for reporting the best and most rigorous epilepsy research from all disciplines ranging from biophysics and molecular biology to epidemiological and psychosocial research. As such the journal will publish original papers relevant to epilepsy from any scientific discipline and also studies of a multidisciplinary nature. Clinical and experimental research papers adopting fresh conceptual approaches to the study of epilepsy and its treatment are encouraged. The overriding criteria for publication are novelty, significant clinical or experimental relevance, and interest to a multidisciplinary audience in the broad arena of epilepsy. Review articles focused on any topic of epilepsy research will also be considered, but only if they present an exceptionally clear synthesis of current knowledge and future directions of a research area, based on a critical assessment of the available data or on hypotheses that are likely to stimulate more critical thinking and further advances in an area of epilepsy research.
×
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