Genome-based assessment of antimicrobial resistance of Escherichia coli recovered from diseased swine in eastern China for a 12-year period.

IF 5.1 1区 生物学 Q1 MICROBIOLOGY
mBio Pub Date : 2025-05-14 Epub Date: 2025-04-17 DOI:10.1128/mbio.00651-25
Junxing Li, Jiang Chang, Jiangang Ma, Wei Zhou, Yue Yang, Jing Wu, Chunjiu Guan, Xiufang Yuan, Lihua Xu, Bin Yu, Fei Su, Shiyi Ye, Yijie Chen, Guoping Zhao, Biao Tang
{"title":"Genome-based assessment of antimicrobial resistance of <i>Escherichia coli</i> recovered from diseased swine in eastern China for a 12-year period.","authors":"Junxing Li, Jiang Chang, Jiangang Ma, Wei Zhou, Yue Yang, Jing Wu, Chunjiu Guan, Xiufang Yuan, Lihua Xu, Bin Yu, Fei Su, Shiyi Ye, Yijie Chen, Guoping Zhao, Biao Tang","doi":"10.1128/mbio.00651-25","DOIUrl":null,"url":null,"abstract":"<p><p>The global rise of antimicrobial resistance (AMR), driven by antibiotic use in healthcare and agriculture, poses a major public health threat. While AMR in clinical settings is well studied, there is a gap in understanding the resistance profiles of <i>Escherichia coli</i> from diseased livestock, particularly regarding zoonotic transmission. This study analyzes 114 <i>E. coli</i> isolates from diseased swine over 12 years, revealing that 99.12% were multidrug-resistant. Resistance was highest for ampicillin and amoxicillin/clavulanic acid (100%), followed by ciprofloxacin (96.49%) and tetracycline (94.74%). Furthermore, 21.05% of isolates were resistant to colistin, and 1.75% to tigecycline. A total of 76 antimicrobial resistance genes (ARGs) were identified, with <i>mcr-1</i> found in 18.42%, <i>mcr-3</i> in 4.39%, and <i>tet</i>(X4) in 1.75%. Significant co-occurrence of ARGs and plasmids suggests potential for co-selective dissemination. This study is the first to report enterotoxigenic <i>E. coli</i> (ETEC) strains carrying both <i>mcr-1</i> and <i>mcr-3</i> genes. After the 2017 colistin ban in China, <i>mcr-1</i> detection rates significantly decreased, while florfenicol resistance rates increased in 2018-2021 (94.29%) compared to 2010-2017 (79.55%). This work provides valuable insights into the AMR profiles of <i>E. coli</i> from diseased swine and highlights trends that can inform strategies for monitoring and controlling public health risks associated with zoonotic <i>E. coli</i> transmission.IMPORTANCEThis study highlights the critical role of diseased and deceased swine in the spread of antimicrobial resistance (AMR), providing new insights into the transmission of resistance genes in zoonotic contexts. By analyzing <i>E. coli</i> from diseased swine, we identify key resistance genes such as <i>mcr-1</i>, <i>mcr-3</i>, and <i>tet</i>(X4), which pose significant public health risks, especially regarding last-resort antibiotics like colistin. Moreover, the study identifies novel transmission patterns of <i>mcr</i> genes, including ETEC strains carrying the <i>mcr-3</i> gene and strains harboring both <i>mcr-1</i> and <i>mcr-3</i> genes. The role of plasmids in horizontal gene transfer is also revealed, facilitating rapid AMR spread across species. The long-term persistence of resistant strains highlights the challenges in controlling AMR in livestock. These findings underscore the need for enhanced surveillance and a One Health approach to mitigate AMR risks across animal, human, and environmental health.</p>","PeriodicalId":18315,"journal":{"name":"mBio","volume":"16 5","pages":"e0065125"},"PeriodicalIF":5.1000,"publicationDate":"2025-05-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12077178/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"mBio","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/mbio.00651-25","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/4/17 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

The global rise of antimicrobial resistance (AMR), driven by antibiotic use in healthcare and agriculture, poses a major public health threat. While AMR in clinical settings is well studied, there is a gap in understanding the resistance profiles of Escherichia coli from diseased livestock, particularly regarding zoonotic transmission. This study analyzes 114 E. coli isolates from diseased swine over 12 years, revealing that 99.12% were multidrug-resistant. Resistance was highest for ampicillin and amoxicillin/clavulanic acid (100%), followed by ciprofloxacin (96.49%) and tetracycline (94.74%). Furthermore, 21.05% of isolates were resistant to colistin, and 1.75% to tigecycline. A total of 76 antimicrobial resistance genes (ARGs) were identified, with mcr-1 found in 18.42%, mcr-3 in 4.39%, and tet(X4) in 1.75%. Significant co-occurrence of ARGs and plasmids suggests potential for co-selective dissemination. This study is the first to report enterotoxigenic E. coli (ETEC) strains carrying both mcr-1 and mcr-3 genes. After the 2017 colistin ban in China, mcr-1 detection rates significantly decreased, while florfenicol resistance rates increased in 2018-2021 (94.29%) compared to 2010-2017 (79.55%). This work provides valuable insights into the AMR profiles of E. coli from diseased swine and highlights trends that can inform strategies for monitoring and controlling public health risks associated with zoonotic E. coli transmission.IMPORTANCEThis study highlights the critical role of diseased and deceased swine in the spread of antimicrobial resistance (AMR), providing new insights into the transmission of resistance genes in zoonotic contexts. By analyzing E. coli from diseased swine, we identify key resistance genes such as mcr-1, mcr-3, and tet(X4), which pose significant public health risks, especially regarding last-resort antibiotics like colistin. Moreover, the study identifies novel transmission patterns of mcr genes, including ETEC strains carrying the mcr-3 gene and strains harboring both mcr-1 and mcr-3 genes. The role of plasmids in horizontal gene transfer is also revealed, facilitating rapid AMR spread across species. The long-term persistence of resistant strains highlights the challenges in controlling AMR in livestock. These findings underscore the need for enhanced surveillance and a One Health approach to mitigate AMR risks across animal, human, and environmental health.

中国东部12年病猪大肠杆菌耐药性基因组分析
由于在卫生保健和农业中使用抗生素,全球抗菌素耐药性(AMR)上升,对公共卫生构成重大威胁。虽然对临床环境中的抗菌素耐药性进行了很好的研究,但在了解来自病畜的大肠杆菌的耐药概况方面存在差距,特别是在人畜共患传播方面。本研究对12年来从病猪分离的114株大肠杆菌进行了分析,发现99.12%的菌株具有多重耐药性。耐药最高的是氨苄西林和阿莫西林/克拉维酸(100%),其次是环丙沙星(96.49%)和四环素(94.74%)。21.05%的菌株对粘菌素耐药,1.75%的菌株对替加环素耐药。共鉴定出76个耐药基因(ARGs),其中mcr-1占18.42%,mcr-3占4.39%,tet(X4)占1.75%。ARGs和质粒的显著共存提示可能存在共选择传播。这项研究首次报道了携带mcr-1和mcr-3基因的产肠毒素大肠杆菌(ETEC)菌株。2017年中国禁用粘菌素后,mcr-1检出率明显下降,而氟苯尼考耐药率在2018-2021年(94.29%)较2010-2017年(79.55%)上升。这项工作为病猪大肠杆菌的AMR概况提供了有价值的见解,并突出了可以为监测和控制与人畜共患大肠杆菌传播相关的公共卫生风险的战略提供信息的趋势。本研究强调了病猪和死猪在抗菌素耐药性(AMR)传播中的关键作用,为人畜共患环境下耐药基因的传播提供了新的见解。通过分析来自病猪的大肠杆菌,我们确定了关键的耐药基因,如mcr-1、mcr-3和tet(X4),它们构成重大的公共卫生风险,特别是对于最后的抗生素,如粘菌素。此外,该研究还发现了mcr基因的新传播模式,包括携带mcr-3基因的ETEC菌株和同时携带mcr-1和mcr-3基因的菌株。质粒在水平基因转移中的作用也被揭示,促进了抗菌素耐药性在物种间的快速传播。耐药菌株的长期存在凸显了控制牲畜抗菌素耐药性的挑战。这些发现强调需要加强监测和“同一个健康”方针,以减轻动物、人类和环境健康方面的抗菌素耐药性风险。
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
mBio
mBio MICROBIOLOGY-
CiteScore
10.50
自引率
3.10%
发文量
762
审稿时长
1 months
期刊介绍: mBio® is ASM''s first broad-scope, online-only, open access journal. mBio offers streamlined review and publication of the best research in microbiology and allied fields.
×
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