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Decrease in the prevalence of antimicrobial resistance in Escherichia coli isolates of Canadian turkey flocks driven by the implementation of an antimicrobial stewardship program

The emergence of antimicrobial-resistant organisms at the human-animal-environment interface has raised global concern prompting governments and various stakeholders to take action. As a part of the stewardship initiative, Canadian turkey producers have implemented an antimicrobial use (AMU) strateg...

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Autores principales: Shrestha, Rima D., Agunos, Agnes, Gow, Sheryl P., Deckert, Anne E., Varga, Csaba
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10365295/
https://www.ncbi.nlm.nih.gov/pubmed/37486902
http://dx.doi.org/10.1371/journal.pone.0282897
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author Shrestha, Rima D.
Agunos, Agnes
Gow, Sheryl P.
Deckert, Anne E.
Varga, Csaba
author_facet Shrestha, Rima D.
Agunos, Agnes
Gow, Sheryl P.
Deckert, Anne E.
Varga, Csaba
author_sort Shrestha, Rima D.
collection PubMed
description The emergence of antimicrobial-resistant organisms at the human-animal-environment interface has raised global concern prompting governments and various stakeholders to take action. As a part of the stewardship initiative, Canadian turkey producers have implemented an antimicrobial use (AMU) strategy to manage antimicrobial resistance (AMR) in their sector. This study evaluated farm-level AMU and AMR data collected between 2016 and 2021 in major turkey-producing provinces/regions through the Canadian Integrated Program for Antimicrobial Resistance Surveillance to assess the progress of the strategy by characterizing the prevalence of homologous and multidrug resistance (MDR) in Escherichia coli isolated from turkeys. Multivariable mixed-effect logistic regression models assessed temporal and provincial/regional variations in AMR and MDR. Negative binomial regression models examined the temporal and regional variations in the total AMU. The total AMU (measured in mg/kg turkey biomass) significantly decreased in all provinces/regions in 2020 and 2021. Escherichia coli isolates from turkey flocks showed a significant decrease in resistance to gentamicin, sulfisoxazole, and tetracyclines during the six-year study period, consistent with the timing of the AMU reduction strategy. The prevalence of MDR isolates was significantly lower in 2020 and 2021 compared to 2016. Higher prevalence was observed in the Western region compared to Québec and Ontario. Two common AMR patterns were identified: ampicillin-streptomycin-tetracyclines and streptomycin-sulfisoxazole-tetracyclines. These AMR patterns indicate possible cross-resistances (same class), co-selection (unrelated classes) for resistance, or potential carryover of resistance determinants from previous production cycles. The decreasing prevalence of resistance to homologous antimicrobials, MDR, and AMU quantity are suggestive that the turkey sector’s AMU strategy is achieving its desired impact. However, antimicrobials previously eliminated for preventive use in turkey flocks and the use of highly important antimicrobials in human medicine suggest that the AMU reduction strategy should be monitored and re-evaluated periodically to mitigate the emergence of MDR bacteria and safeguard animal and public health.
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spelling pubmed-103652952023-07-25 Decrease in the prevalence of antimicrobial resistance in Escherichia coli isolates of Canadian turkey flocks driven by the implementation of an antimicrobial stewardship program Shrestha, Rima D. Agunos, Agnes Gow, Sheryl P. Deckert, Anne E. Varga, Csaba PLoS One Research Article The emergence of antimicrobial-resistant organisms at the human-animal-environment interface has raised global concern prompting governments and various stakeholders to take action. As a part of the stewardship initiative, Canadian turkey producers have implemented an antimicrobial use (AMU) strategy to manage antimicrobial resistance (AMR) in their sector. This study evaluated farm-level AMU and AMR data collected between 2016 and 2021 in major turkey-producing provinces/regions through the Canadian Integrated Program for Antimicrobial Resistance Surveillance to assess the progress of the strategy by characterizing the prevalence of homologous and multidrug resistance (MDR) in Escherichia coli isolated from turkeys. Multivariable mixed-effect logistic regression models assessed temporal and provincial/regional variations in AMR and MDR. Negative binomial regression models examined the temporal and regional variations in the total AMU. The total AMU (measured in mg/kg turkey biomass) significantly decreased in all provinces/regions in 2020 and 2021. Escherichia coli isolates from turkey flocks showed a significant decrease in resistance to gentamicin, sulfisoxazole, and tetracyclines during the six-year study period, consistent with the timing of the AMU reduction strategy. The prevalence of MDR isolates was significantly lower in 2020 and 2021 compared to 2016. Higher prevalence was observed in the Western region compared to Québec and Ontario. Two common AMR patterns were identified: ampicillin-streptomycin-tetracyclines and streptomycin-sulfisoxazole-tetracyclines. These AMR patterns indicate possible cross-resistances (same class), co-selection (unrelated classes) for resistance, or potential carryover of resistance determinants from previous production cycles. The decreasing prevalence of resistance to homologous antimicrobials, MDR, and AMU quantity are suggestive that the turkey sector’s AMU strategy is achieving its desired impact. However, antimicrobials previously eliminated for preventive use in turkey flocks and the use of highly important antimicrobials in human medicine suggest that the AMU reduction strategy should be monitored and re-evaluated periodically to mitigate the emergence of MDR bacteria and safeguard animal and public health. Public Library of Science 2023-07-24 /pmc/articles/PMC10365295/ /pubmed/37486902 http://dx.doi.org/10.1371/journal.pone.0282897 Text en © 2023 Shrestha et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Shrestha, Rima D.
Agunos, Agnes
Gow, Sheryl P.
Deckert, Anne E.
Varga, Csaba
Decrease in the prevalence of antimicrobial resistance in Escherichia coli isolates of Canadian turkey flocks driven by the implementation of an antimicrobial stewardship program
title Decrease in the prevalence of antimicrobial resistance in Escherichia coli isolates of Canadian turkey flocks driven by the implementation of an antimicrobial stewardship program
title_full Decrease in the prevalence of antimicrobial resistance in Escherichia coli isolates of Canadian turkey flocks driven by the implementation of an antimicrobial stewardship program
title_fullStr Decrease in the prevalence of antimicrobial resistance in Escherichia coli isolates of Canadian turkey flocks driven by the implementation of an antimicrobial stewardship program
title_full_unstemmed Decrease in the prevalence of antimicrobial resistance in Escherichia coli isolates of Canadian turkey flocks driven by the implementation of an antimicrobial stewardship program
title_short Decrease in the prevalence of antimicrobial resistance in Escherichia coli isolates of Canadian turkey flocks driven by the implementation of an antimicrobial stewardship program
title_sort decrease in the prevalence of antimicrobial resistance in escherichia coli isolates of canadian turkey flocks driven by the implementation of an antimicrobial stewardship program
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10365295/
https://www.ncbi.nlm.nih.gov/pubmed/37486902
http://dx.doi.org/10.1371/journal.pone.0282897
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