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

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,...

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Main 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
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Language:English
Published: American Society for Microbiology 2025-05-01
Series:mBio
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Online Access:https://journals.asm.org/doi/10.1128/mbio.00651-25
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author 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
author_facet 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
author_sort Junxing Li
collection DOAJ
description 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.
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spelling doaj-art-a8cbe585d8ca4639a16a6ee8b38493bc2025-08-20T02:24:54ZengAmerican Society for MicrobiologymBio2150-75112025-05-0116510.1128/mbio.00651-25Genome-based assessment of antimicrobial resistance of Escherichia coli recovered from diseased swine in eastern China for a 12-year periodJunxing Li0Jiang Chang1Jiangang Ma2Wei Zhou3Yue Yang4Jing Wu5Chunjiu Guan6Xiufang Yuan7Lihua Xu8Bin Yu9Fei Su10Shiyi Ye11Yijie Chen12Guoping Zhao13Biao Tang14Institute of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, ChinaKey Laboratory of Systems Health Science of Zhejiang Province, School of Life Science, Hangzhou Institute for Advanced Study, University of the Chinese Academy of Sciences, Hangzhou, Zhejiang, ChinaXianghu Laboratory, Hangzhou, Zhejiang, ChinaZhejiang Provincial Center for Animal Disease Prevention and Control, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Agro-product Safety and Nutrition, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, ChinaKey Laboratory of Systems Health Science of Zhejiang Province, School of Life Science, Hangzhou Institute for Advanced Study, University of the Chinese Academy of Sciences, Hangzhou, Zhejiang, ChinaKey Laboratory of Systems Health Science of Zhejiang Province, School of Life Science, Hangzhou Institute for Advanced Study, University of the Chinese Academy of Sciences, Hangzhou, Zhejiang, ChinaInstitute of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, ChinaInstitute of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, ChinaInstitute of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, ChinaInstitute of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, ChinaInstitute of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, ChinaInstitute of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Agro-product Safety and Nutrition, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, ChinaKey Laboratory of Systems Health Science of Zhejiang Province, School of Life Science, Hangzhou Institute for Advanced Study, University of the Chinese Academy of Sciences, Hangzhou, Zhejiang, ChinaABSTRACT 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.https://journals.asm.org/doi/10.1128/mbio.00651-25Escherichia coliswineantimicrobial resistancemcrtet(X4)
spellingShingle 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
Genome-based assessment of antimicrobial resistance of Escherichia coli recovered from diseased swine in eastern China for a 12-year period
mBio
Escherichia coli
swine
antimicrobial resistance
mcr
tet(X4)
title Genome-based assessment of antimicrobial resistance of Escherichia coli recovered from diseased swine in eastern China for a 12-year period
title_full Genome-based assessment of antimicrobial resistance of Escherichia coli recovered from diseased swine in eastern China for a 12-year period
title_fullStr Genome-based assessment of antimicrobial resistance of Escherichia coli recovered from diseased swine in eastern China for a 12-year period
title_full_unstemmed Genome-based assessment of antimicrobial resistance of Escherichia coli recovered from diseased swine in eastern China for a 12-year period
title_short Genome-based assessment of antimicrobial resistance of Escherichia coli recovered from diseased swine in eastern China for a 12-year period
title_sort genome based assessment of antimicrobial resistance of escherichia coli recovered from diseased swine in eastern china for a 12 year period
topic Escherichia coli
swine
antimicrobial resistance
mcr
tet(X4)
url https://journals.asm.org/doi/10.1128/mbio.00651-25
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