Large-Scale Studies on Antimicrobial Resistance and Molecular Characterization of Escherichia coli from Food Animals in Developed Areas of Eastern China

Jiangang Ma; Wei Zhou; Jing Wu; Xiaofeng Liu; Jiahui Lin; Xiaofeng Ji; Hui Lin; Jianmei Wang; Han Jiang; Qianjin Zhou; Guoping Zhao; Hua Yang; Biao Tang

doi:10.1128/spectrum.02015-22

Microbiology Spectrum (Aug 2022)

Large-Scale Studies on Antimicrobial Resistance and Molecular Characterization of Escherichia coli from Food Animals in Developed Areas of Eastern China

Jiangang Ma,
Wei Zhou,
Jing Wu,
Xiaofeng Liu,
Jiahui Lin,
Xiaofeng Ji,
Hui Lin,
Jianmei Wang,
Han Jiang,
Qianjin Zhou,
Guoping Zhao,
Hua Yang,
Biao Tang

Affiliations

Jiangang Ma: State 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, China
Wei Zhou: Zhejiang Provincial Center for Animal Disease Prevention and Control, Hangzhou Zhejiang, China
Jing Wu: State 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, China
Xiaofeng Liu: College of Food Science and Technology, Zhejiang University of Technology, Hangzhou, Zhejiang, China
Jiahui Lin: State 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, China
Xiaofeng Ji: State 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, China
Hui Lin: State 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, China
Jianmei Wang: State 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, China
Han Jiang: Key Laboratory of Marine Food Quality and Hazard Controlling Technology of Zhejiang Province, China Jiliang University, Hangzhou, Zhejiang, China
Qianjin Zhou: School of Marine Science, Ningbo University, Ningbo, Zhejiang, China
Guoping Zhao: CAS Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
Hua Yang: State 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, China
Biao Tang: State 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, China

DOI: https://doi.org/10.1128/spectrum.02015-22
Journal volume & issue: Vol. 10, no. 4

Abstract

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ABSTRACT Widely distributed multidrug-resistant (MDR) bacteria threaten animals and human health. Nevertheless, few antimicrobial resistance (AMR) surveys of large-scale animal-derived bacteria have been explored. Here, 1,468 (97.54%) Escherichia coli strains were isolated from 1,505 pig (1,060) and chicken (445) anal swab samples from 11 cities in Zhejiang Province, China, in 2020. These isolates had a high resistance to tetracycline (92.92%), sulfisoxazole (93.05%), florfenicol (83.11%), and ampicillin (78.27%). More than 88.68% of the strains were MDR bacteria. A low AMR ratio to the “last-resort” antimicrobials tigecycline (0.75%), colistin (1.36%), and meropenem (0.75%) were found. The AMR of E. coli from pigs was higher than that of chickens. Eighteen strains among 31 MDR strains that were resistant to “last-resort” antimicrobials could transfer the AMR genes (mcr-1, tet(X), and blaNDM) to the recipient strain J53, which confer colistin, tigecycline, and carbapenem resistance, respectively. The homology among mcr-1-carrying isolates was relatively high, and the sequence types were mainly ST5529, ST101, and ST354, while the homology of isolates harboring tet(X4) and blaNDM-5 genes were different. The mcr-1, blaNDM-5, and tet(X4) genes in strains LS45, JH51, and TZ118 were identified on the Incl2, IncHI2, and IncX1 plasmids, respectively. Moreover, tet(A), sul2, floR, and blaTEM-1B were the most common ARGs in 31 strains. Additionally, the heavy metals copper and zinc had a significant correlation with amoxicillin/clavulanate and tetracycline resistance. Controlling the movement of animals between cities and reducing the use of antimicrobials are effective methods to reduce the threat of AMR bacteria. IMPORTANCE Pigs and chickens are the most common food animals that are the important vectors for spreading antimicrobial-resistant pathogens among animals and humans. Limited systematic AMR monitoring of these food animal origin bacteria had been reported, especially in developed areas of China. Our study provides a comprehensive and systematic study of AMR in Escherichia coli from eastern China. The AMR of E. coli strains among the animals or cities has statistically significant differences. Moreover, the mcr-1, tet(X4), and blaNDM-5 genes, considered resistant to the last line of AMR, were identified in part of farms. The transferability and the prevalence of these AMR strains were intensively studied. Our monitoring is comparable to human clinical research and has an essential reference for public health safety. These findings will provide early warning for AMR strains and guide the clinical use of antibiotics to control the spread of antibiotic resistance.

Published in Microbiology Spectrum

ISSN: 2165-0497 (Online)
Publisher: American Society for Microbiology
Country of publisher: United States
LCC subjects: Science: Microbiology
Website: https://journals.asm.org/journal/spectrum

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