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Dynamic antimicrobial resistant patterns of Escherichia coli from healthy poultry and swine over 10 years in Chongming Island, Shanghai

BACKGROUND: Antimicrobial resistance (AMR) is one of the greatest threats to animal and public health. Here, we conducted a dynamic surveillance of Escherichia coli on Chongming Island in Shanghai during 2009–2021 to identify the characteristics and trends of Chongming’s AMR pandemic. METHODS: Recta...

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Autores principales: Lv, Chao, Shang, Jun, Zhang, Wengang, Sun, Bingqing, Li, Min, Guo, Chaoyi, Zhou, Nan, Guo, Xiaokui, Huang, Shixin, Zhu, Yongzhang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9482194/
https://www.ncbi.nlm.nih.gov/pubmed/36114584
http://dx.doi.org/10.1186/s40249-022-01025-4
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author Lv, Chao
Shang, Jun
Zhang, Wengang
Sun, Bingqing
Li, Min
Guo, Chaoyi
Zhou, Nan
Guo, Xiaokui
Huang, Shixin
Zhu, Yongzhang
author_facet Lv, Chao
Shang, Jun
Zhang, Wengang
Sun, Bingqing
Li, Min
Guo, Chaoyi
Zhou, Nan
Guo, Xiaokui
Huang, Shixin
Zhu, Yongzhang
author_sort Lv, Chao
collection PubMed
description BACKGROUND: Antimicrobial resistance (AMR) is one of the greatest threats to animal and public health. Here, we conducted a dynamic surveillance of Escherichia coli on Chongming Island in Shanghai during 2009–2021 to identify the characteristics and trends of Chongming’s AMR pandemic. METHODS: Rectal (cloaca) swabs from four poultry and nine swine farms (Chongming Island, 2009–2021) were collected for E. coli strains acquisition. The micro-broth dilution method was used to test antimicrobial susceptibility of E. coli isolates against 10 antimicrobial classes including 15 antimicrobials. Utilizing generalized linear mixed models (GLMMs) and co-occurrence analyses, we further explored the multiple-drug-resistance (MDR) combinations and dynamic patterns of E. coli over 10 years in two food animals. RESULTS: Total of 863 MDR isolates were found among 945 collected E. coli isolates, 337 from poultry and 608 from swine. Both isolates exhibited high resistant rates (> 70%) to tetracyclines, phenicols, sulfonamides, penicillins, and aminoglycosides (only in swine). The resistant rates of swine isolates to penicillins, aminoglycosides, tetracyclines, phenicols, and polymyxins were significantly higher than those of poultry isolates, whereas resistance to fluoroquinolones was reversed. Resistance to polymyxins decreased similarly in swine (42.4% in 2009 to 0.0% in 2021) and poultry isolates (from 16.5% to 0.0%). However, resistance to other seven antimicrobial classes (excluding carbapenems and penicillins) declined dramatically in swine isolates, particularly fluoroquinolones (from 80.5% to 14.4%), and tendencies of resistance to the seven classes showed markedly divergent patterns in poultry isolates. Using Poisson GLMMs, the AMR carriage since 2016 was significantly lower than that of 2009 (odds ratio < 1), indicating a decline in the risk of MDR emergence. Furthermore, despite the highly diverse MDR profiles, co-occurrence analysis identified two prominent MDR clusters of penicillins-phenicols-fluoroquinolones in poultry and aminoglycosides-tetracyclines-sulfonamides-phenicols in swine. CONCLUSIONS: Our study uncovered vastly distinct AMR patterns and dynamic tendencies of poultry and swine E. coli isolates from Chongming. Meanwhile, Chongming’s AMR status has ameliorated, as indicated by the decline in antimicrobials prevalence (particularly in swine), lower likelihood of MDR emergence and low carbapenem-, cephalosporin-, and polymyxin resistance. Importantly, this surveillance results are the vital basis for future policy development in Chongming and Shanghai. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-022-01025-4.
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spelling pubmed-94821942022-09-18 Dynamic antimicrobial resistant patterns of Escherichia coli from healthy poultry and swine over 10 years in Chongming Island, Shanghai Lv, Chao Shang, Jun Zhang, Wengang Sun, Bingqing Li, Min Guo, Chaoyi Zhou, Nan Guo, Xiaokui Huang, Shixin Zhu, Yongzhang Infect Dis Poverty Research Article BACKGROUND: Antimicrobial resistance (AMR) is one of the greatest threats to animal and public health. Here, we conducted a dynamic surveillance of Escherichia coli on Chongming Island in Shanghai during 2009–2021 to identify the characteristics and trends of Chongming’s AMR pandemic. METHODS: Rectal (cloaca) swabs from four poultry and nine swine farms (Chongming Island, 2009–2021) were collected for E. coli strains acquisition. The micro-broth dilution method was used to test antimicrobial susceptibility of E. coli isolates against 10 antimicrobial classes including 15 antimicrobials. Utilizing generalized linear mixed models (GLMMs) and co-occurrence analyses, we further explored the multiple-drug-resistance (MDR) combinations and dynamic patterns of E. coli over 10 years in two food animals. RESULTS: Total of 863 MDR isolates were found among 945 collected E. coli isolates, 337 from poultry and 608 from swine. Both isolates exhibited high resistant rates (> 70%) to tetracyclines, phenicols, sulfonamides, penicillins, and aminoglycosides (only in swine). The resistant rates of swine isolates to penicillins, aminoglycosides, tetracyclines, phenicols, and polymyxins were significantly higher than those of poultry isolates, whereas resistance to fluoroquinolones was reversed. Resistance to polymyxins decreased similarly in swine (42.4% in 2009 to 0.0% in 2021) and poultry isolates (from 16.5% to 0.0%). However, resistance to other seven antimicrobial classes (excluding carbapenems and penicillins) declined dramatically in swine isolates, particularly fluoroquinolones (from 80.5% to 14.4%), and tendencies of resistance to the seven classes showed markedly divergent patterns in poultry isolates. Using Poisson GLMMs, the AMR carriage since 2016 was significantly lower than that of 2009 (odds ratio < 1), indicating a decline in the risk of MDR emergence. Furthermore, despite the highly diverse MDR profiles, co-occurrence analysis identified two prominent MDR clusters of penicillins-phenicols-fluoroquinolones in poultry and aminoglycosides-tetracyclines-sulfonamides-phenicols in swine. CONCLUSIONS: Our study uncovered vastly distinct AMR patterns and dynamic tendencies of poultry and swine E. coli isolates from Chongming. Meanwhile, Chongming’s AMR status has ameliorated, as indicated by the decline in antimicrobials prevalence (particularly in swine), lower likelihood of MDR emergence and low carbapenem-, cephalosporin-, and polymyxin resistance. Importantly, this surveillance results are the vital basis for future policy development in Chongming and Shanghai. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-022-01025-4. BioMed Central 2022-09-16 /pmc/articles/PMC9482194/ /pubmed/36114584 http://dx.doi.org/10.1186/s40249-022-01025-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Lv, Chao
Shang, Jun
Zhang, Wengang
Sun, Bingqing
Li, Min
Guo, Chaoyi
Zhou, Nan
Guo, Xiaokui
Huang, Shixin
Zhu, Yongzhang
Dynamic antimicrobial resistant patterns of Escherichia coli from healthy poultry and swine over 10 years in Chongming Island, Shanghai
title Dynamic antimicrobial resistant patterns of Escherichia coli from healthy poultry and swine over 10 years in Chongming Island, Shanghai
title_full Dynamic antimicrobial resistant patterns of Escherichia coli from healthy poultry and swine over 10 years in Chongming Island, Shanghai
title_fullStr Dynamic antimicrobial resistant patterns of Escherichia coli from healthy poultry and swine over 10 years in Chongming Island, Shanghai
title_full_unstemmed Dynamic antimicrobial resistant patterns of Escherichia coli from healthy poultry and swine over 10 years in Chongming Island, Shanghai
title_short Dynamic antimicrobial resistant patterns of Escherichia coli from healthy poultry and swine over 10 years in Chongming Island, Shanghai
title_sort dynamic antimicrobial resistant patterns of escherichia coli from healthy poultry and swine over 10 years in chongming island, shanghai
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9482194/
https://www.ncbi.nlm.nih.gov/pubmed/36114584
http://dx.doi.org/10.1186/s40249-022-01025-4
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