Changes in gut microbiome can be associated with abrupt seizure exacerbation in epilepsy patients

IF 1.8 4区 医学 Q3 CLINICAL NEUROLOGY
Dong Won Kwack , Sunghee Lee , Dong-Hoon Lee , Dong Wook Kim
{"title":"Changes in gut microbiome can be associated with abrupt seizure exacerbation in epilepsy patients","authors":"Dong Won Kwack ,&nbsp;Sunghee Lee ,&nbsp;Dong-Hoon Lee ,&nbsp;Dong Wook Kim","doi":"10.1016/j.clineuro.2024.108556","DOIUrl":null,"url":null,"abstract":"<div><h3>Objective</h3><p>Seizures can be triggered by a variety of endogenous or exogenous factors. We hypothesized that alterations in the gut microbiome may be a seizure precipitant and analyzed the composition and characteristics of the gut microbiome in epilepsy patients who experienced an abrupt seizure exacerbation without a clear seizure precipitant.</p></div><div><h3>Methods</h3><p>We prospectively enrolled 25 adult patients with epilepsy and collected fecal samples on the admission and after seizure recovery for next-generation sequencing analysis. We performed nonparametric paired t-test analysis to evaluate changes in the gut microbiota as seizures worsened and when it recovered and also estimated alpha and beta diversities in each category.</p></div><div><h3>Results</h3><p>A total of 19 patients (13 males) aged between 19 and 78 years (mean 45.2 years) were included in the study. The composition of the gut microbiota underwent a significant change following an abrupt seizure exacerbation. At the phylum level, the relative abundance of <em>Fusobacteria</em> and <em>Synergistetes</em> was decreased in the seizure recovery state compared to the acute seizure exacerbation. A similar trend was observed at the lower hierarchical levels, with a decrease in the relative abundance of <em>Fusobacteria</em>, <em>Tissierellia</em>, and <em>Synergistia</em> at the class level, and that of <em>Synergistales</em>, <em>Tissierellales</em>, and <em>Fusobacteriales</em> at the order level. At the family level, the relative abundance of <em>Fusobacteriaceae</em> and <em>Staphylococcaceae</em> was decreased, whereas that of <em>Leuconostocaceae</em> was increased. No statistical differences were observed in alpha and beta diversity between the pre- and post-acute seizure exacerbation periods.</p></div><div><h3>Significance</h3><p>Our study suggests that the changes in <em>Fusobacteriaceae</em> and <em>Lecuonostocaceae</em> may be associated with acute seizure exacerbation in epilepsy patients. Given that <em>Fusobacteriaceae</em> are associated with various systemic diseases due to their invasive properties and that <em>Leuconostocaceae</em> are known to produce GABA, our results may suggest a gut microbiome-based treatment option for epilepsy patients.</p></div>","PeriodicalId":10385,"journal":{"name":"Clinical Neurology and Neurosurgery","volume":null,"pages":null},"PeriodicalIF":1.8000,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Clinical Neurology and Neurosurgery","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0303846724004438","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

Objective

Seizures can be triggered by a variety of endogenous or exogenous factors. We hypothesized that alterations in the gut microbiome may be a seizure precipitant and analyzed the composition and characteristics of the gut microbiome in epilepsy patients who experienced an abrupt seizure exacerbation without a clear seizure precipitant.

Methods

We prospectively enrolled 25 adult patients with epilepsy and collected fecal samples on the admission and after seizure recovery for next-generation sequencing analysis. We performed nonparametric paired t-test analysis to evaluate changes in the gut microbiota as seizures worsened and when it recovered and also estimated alpha and beta diversities in each category.

Results

A total of 19 patients (13 males) aged between 19 and 78 years (mean 45.2 years) were included in the study. The composition of the gut microbiota underwent a significant change following an abrupt seizure exacerbation. At the phylum level, the relative abundance of Fusobacteria and Synergistetes was decreased in the seizure recovery state compared to the acute seizure exacerbation. A similar trend was observed at the lower hierarchical levels, with a decrease in the relative abundance of Fusobacteria, Tissierellia, and Synergistia at the class level, and that of Synergistales, Tissierellales, and Fusobacteriales at the order level. At the family level, the relative abundance of Fusobacteriaceae and Staphylococcaceae was decreased, whereas that of Leuconostocaceae was increased. No statistical differences were observed in alpha and beta diversity between the pre- and post-acute seizure exacerbation periods.

Significance

Our study suggests that the changes in Fusobacteriaceae and Lecuonostocaceae may be associated with acute seizure exacerbation in epilepsy patients. Given that Fusobacteriaceae are associated with various systemic diseases due to their invasive properties and that Leuconostocaceae are known to produce GABA, our results may suggest a gut microbiome-based treatment option for epilepsy patients.

肠道微生物组的变化可能与癫痫患者突然发作加重有关
目的癫痫发作可由多种内源性或外源性因素诱发。我们假设肠道微生物群的改变可能是癫痫发作的诱因,并分析了在没有明确癫痫发作诱因的情况下突然发作加重的癫痫患者的肠道微生物群的组成和特征。方法我们前瞻性地招募了 25 名成年癫痫患者,并在入院时和发作恢复后收集粪便样本进行新一代测序分析。我们进行了非参数配对 t 检验分析,以评估癫痫发作恶化时和恢复时肠道微生物群的变化,并估计了每个类别中的α和β多样性。在癫痫突然加重后,肠道微生物群的组成发生了显著变化。在门一级,与急性发作加重时相比,发作恢复状态下的镰刀菌和协同菌的相对丰度有所下降。在较低的层次上也观察到类似的趋势,在类的层次上,Fusobacteria、Tissierellia 和 Synergistia 的相对丰度下降,在目的层次上,Synergistales、Tissierellales 和 Fusobacteriales 的相对丰度下降。在科一级,Fusobacteriaceae 和 Staphylococcaceae 的相对丰度下降,而 Leuconostocaceae 的相对丰度上升。我们的研究表明,镰刀菌科和白色念珠菌科的变化可能与癫痫患者的急性发作加重有关。鉴于镰刀菌科细菌因其侵袭性而与各种系统性疾病相关,而且已知亮绿菌科细菌能产生 GABA,我们的研究结果可能为癫痫患者提供了一种基于肠道微生物的治疗方案。
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
Clinical Neurology and Neurosurgery
Clinical Neurology and Neurosurgery 医学-临床神经学
CiteScore
3.70
自引率
5.30%
发文量
358
审稿时长
46 days
期刊介绍: Clinical Neurology and Neurosurgery is devoted to publishing papers and reports on the clinical aspects of neurology and neurosurgery. It is an international forum for papers of high scientific standard that are of interest to Neurologists and Neurosurgeons world-wide.
×
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