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Prevalence and distribution of extended-spectrum β-lactamase and AmpC-producing Escherichia coli in two New Zealand dairy farm environments

Antimicrobial resistance (AMR) is a global threat to human and animal health, with the misuse and overuse of antimicrobials being suggested as the main driver of resistance. In a global context, New Zealand (NZ) is a relatively low user of antimicrobials in animal production. However, the role antim...

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Autores principales: Collis, Rose M., Biggs, Patrick J., Burgess, Sara A., Midwinter, Anne C., Brightwell, Gale, Cookson, Adrian L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9403332/
https://www.ncbi.nlm.nih.gov/pubmed/36033848
http://dx.doi.org/10.3389/fmicb.2022.960748
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author Collis, Rose M.
Biggs, Patrick J.
Burgess, Sara A.
Midwinter, Anne C.
Brightwell, Gale
Cookson, Adrian L.
author_facet Collis, Rose M.
Biggs, Patrick J.
Burgess, Sara A.
Midwinter, Anne C.
Brightwell, Gale
Cookson, Adrian L.
author_sort Collis, Rose M.
collection PubMed
description Antimicrobial resistance (AMR) is a global threat to human and animal health, with the misuse and overuse of antimicrobials being suggested as the main driver of resistance. In a global context, New Zealand (NZ) is a relatively low user of antimicrobials in animal production. However, the role antimicrobial usage on pasture-based dairy farms, such as those in NZ, plays in driving the spread of AMR within the dairy farm environment remains equivocal. Culture-based methods were used to determine the prevalence and distribution of extended-spectrum β-lactamase (ESBL)- and AmpC-producing Escherichia coli from farm environmental samples collected over a 15-month period from two NZ dairy farms with contrasting management practices. Whole genome sequencing was utilised to understand the genomic epidemiology and antimicrobial resistance gene repertoire of a subset of third-generation cephalosporin resistant E. coli isolated in this study. There was a low sample level prevalence of ESBL-producing E. coli (faeces 1.7%; farm dairy effluent, 6.7% from Dairy 4 and none from Dairy 1) but AmpC-producing E. coli were more frequently isolated across both farms (faeces 3.3% and 8.3%; farm dairy effluent 38.4%, 6.7% from Dairy 1 and Dairy 4, respectively). ESBL- and AmpC-producing E. coli were isolated from faeces and farm dairy effluent in spring and summer, during months with varying levels of antimicrobial use, but no ESBL- or AmpC-producing E. coli were isolated from bulk tank milk or soil from recently grazed paddocks. Hybrid assemblies using short- and long-read sequence data from a subset of ESBL- and AmpC-producing E. coli enabled the assembly and annotation of nine plasmids from six E. coli, including one plasmid co-harbouring 12 antimicrobial resistance genes. ESBL-producing E. coli were infrequently identified from faeces and farm dairy effluent on the two NZ dairy farms, suggesting they are present at a low prevalence on these farms. Plasmids harbouring several antimicrobial resistance genes were identified, and bacteria carrying such plasmids are a concern for both animal and public health. AMR is a burden for human, animal and environmental health and requires a holistic “One Health” approach to address.
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spelling pubmed-94033322022-08-26 Prevalence and distribution of extended-spectrum β-lactamase and AmpC-producing Escherichia coli in two New Zealand dairy farm environments Collis, Rose M. Biggs, Patrick J. Burgess, Sara A. Midwinter, Anne C. Brightwell, Gale Cookson, Adrian L. Front Microbiol Microbiology Antimicrobial resistance (AMR) is a global threat to human and animal health, with the misuse and overuse of antimicrobials being suggested as the main driver of resistance. In a global context, New Zealand (NZ) is a relatively low user of antimicrobials in animal production. However, the role antimicrobial usage on pasture-based dairy farms, such as those in NZ, plays in driving the spread of AMR within the dairy farm environment remains equivocal. Culture-based methods were used to determine the prevalence and distribution of extended-spectrum β-lactamase (ESBL)- and AmpC-producing Escherichia coli from farm environmental samples collected over a 15-month period from two NZ dairy farms with contrasting management practices. Whole genome sequencing was utilised to understand the genomic epidemiology and antimicrobial resistance gene repertoire of a subset of third-generation cephalosporin resistant E. coli isolated in this study. There was a low sample level prevalence of ESBL-producing E. coli (faeces 1.7%; farm dairy effluent, 6.7% from Dairy 4 and none from Dairy 1) but AmpC-producing E. coli were more frequently isolated across both farms (faeces 3.3% and 8.3%; farm dairy effluent 38.4%, 6.7% from Dairy 1 and Dairy 4, respectively). ESBL- and AmpC-producing E. coli were isolated from faeces and farm dairy effluent in spring and summer, during months with varying levels of antimicrobial use, but no ESBL- or AmpC-producing E. coli were isolated from bulk tank milk or soil from recently grazed paddocks. Hybrid assemblies using short- and long-read sequence data from a subset of ESBL- and AmpC-producing E. coli enabled the assembly and annotation of nine plasmids from six E. coli, including one plasmid co-harbouring 12 antimicrobial resistance genes. ESBL-producing E. coli were infrequently identified from faeces and farm dairy effluent on the two NZ dairy farms, suggesting they are present at a low prevalence on these farms. Plasmids harbouring several antimicrobial resistance genes were identified, and bacteria carrying such plasmids are a concern for both animal and public health. AMR is a burden for human, animal and environmental health and requires a holistic “One Health” approach to address. Frontiers Media S.A. 2022-08-11 /pmc/articles/PMC9403332/ /pubmed/36033848 http://dx.doi.org/10.3389/fmicb.2022.960748 Text en Copyright © 2022 Collis, Biggs, Burgess, Midwinter, Brightwell and Cookson. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Collis, Rose M.
Biggs, Patrick J.
Burgess, Sara A.
Midwinter, Anne C.
Brightwell, Gale
Cookson, Adrian L.
Prevalence and distribution of extended-spectrum β-lactamase and AmpC-producing Escherichia coli in two New Zealand dairy farm environments
title Prevalence and distribution of extended-spectrum β-lactamase and AmpC-producing Escherichia coli in two New Zealand dairy farm environments
title_full Prevalence and distribution of extended-spectrum β-lactamase and AmpC-producing Escherichia coli in two New Zealand dairy farm environments
title_fullStr Prevalence and distribution of extended-spectrum β-lactamase and AmpC-producing Escherichia coli in two New Zealand dairy farm environments
title_full_unstemmed Prevalence and distribution of extended-spectrum β-lactamase and AmpC-producing Escherichia coli in two New Zealand dairy farm environments
title_short Prevalence and distribution of extended-spectrum β-lactamase and AmpC-producing Escherichia coli in two New Zealand dairy farm environments
title_sort prevalence and distribution of extended-spectrum β-lactamase and ampc-producing escherichia coli in two new zealand dairy farm environments
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9403332/
https://www.ncbi.nlm.nih.gov/pubmed/36033848
http://dx.doi.org/10.3389/fmicb.2022.960748
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