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A longitudinal study reveals persistence of antimicrobial resistance on livestock farms is not due to antimicrobial usage alone

INTRODUCTION: There are concerns that antimicrobial usage (AMU) is driving an increase in multi-drug resistant (MDR) bacteria so treatment of microbial infections is becoming harder in humans and animals. The aim of this study was to evaluate factors, including usage, that affect antimicrobial resis...

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Autores principales: Smith, Richard P., May, Hannah E., AbuOun, Manal, Stubberfield, Emma, Gilson, Daniel, Chau, Kevin K., Crook, Derrick W., Shaw, Liam P., Read, Daniel S., Stoesser, Nicole, Vilar, Maria Jose, Anjum, Muna F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10043416/
https://www.ncbi.nlm.nih.gov/pubmed/36998408
http://dx.doi.org/10.3389/fmicb.2023.1070340
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author Smith, Richard P.
May, Hannah E.
AbuOun, Manal
Stubberfield, Emma
Gilson, Daniel
Chau, Kevin K.
Crook, Derrick W.
Shaw, Liam P.
Read, Daniel S.
Stoesser, Nicole
Vilar, Maria Jose
Anjum, Muna F.
author_facet Smith, Richard P.
May, Hannah E.
AbuOun, Manal
Stubberfield, Emma
Gilson, Daniel
Chau, Kevin K.
Crook, Derrick W.
Shaw, Liam P.
Read, Daniel S.
Stoesser, Nicole
Vilar, Maria Jose
Anjum, Muna F.
author_sort Smith, Richard P.
collection PubMed
description INTRODUCTION: There are concerns that antimicrobial usage (AMU) is driving an increase in multi-drug resistant (MDR) bacteria so treatment of microbial infections is becoming harder in humans and animals. The aim of this study was to evaluate factors, including usage, that affect antimicrobial resistance (AMR) on farm over time. METHODS: A population of 14 cattle, sheep and pig farms within a defined area of England were sampled three times over a year to collect data on AMR in faecal Enterobacterales flora; AMU; and husbandry or management practices. Ten pooled samples were collected at each visit, with each comprising of 10 pinches of fresh faeces. Up to 14 isolates per visit were whole genome sequenced to determine presence of AMR genes. RESULTS: Sheep farms had very low AMU in comparison to the other species and very few sheep isolates were genotypically resistant at any time point. AMR genes were detected persistently across pig farms at all visits, even on farms with low AMU, whereas AMR bacteria was consistently lower on cattle farms than pigs, even for those with comparably high AMU. MDR bacteria was also more commonly detected on pig farms than any other livestock species. DISCUSSION: The results may be explained by a complex combination of factors on pig farms including historic AMU; co-selection of AMR bacteria; variation in amounts of antimicrobials used between visits; potential persistence in environmental reservoirs of AMR bacteria; or importation of pigs with AMR microbiota from supplying farms. Pig farms may also be at increased risk of AMR due to the greater use of oral routes of group antimicrobial treatment, which were less targeted than cattle treatments; the latter mostly administered to individual animals. Also, farms which exhibited either increasing or decreasing trends of AMR across the study did not have corresponding trends in their AMU. Therefore, our results suggest that factors other than AMU on individual farms are important for persistence of AMR bacteria on farms, which may be operating at the farm and livestock species level.
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spelling pubmed-100434162023-03-29 A longitudinal study reveals persistence of antimicrobial resistance on livestock farms is not due to antimicrobial usage alone Smith, Richard P. May, Hannah E. AbuOun, Manal Stubberfield, Emma Gilson, Daniel Chau, Kevin K. Crook, Derrick W. Shaw, Liam P. Read, Daniel S. Stoesser, Nicole Vilar, Maria Jose Anjum, Muna F. Front Microbiol Microbiology INTRODUCTION: There are concerns that antimicrobial usage (AMU) is driving an increase in multi-drug resistant (MDR) bacteria so treatment of microbial infections is becoming harder in humans and animals. The aim of this study was to evaluate factors, including usage, that affect antimicrobial resistance (AMR) on farm over time. METHODS: A population of 14 cattle, sheep and pig farms within a defined area of England were sampled three times over a year to collect data on AMR in faecal Enterobacterales flora; AMU; and husbandry or management practices. Ten pooled samples were collected at each visit, with each comprising of 10 pinches of fresh faeces. Up to 14 isolates per visit were whole genome sequenced to determine presence of AMR genes. RESULTS: Sheep farms had very low AMU in comparison to the other species and very few sheep isolates were genotypically resistant at any time point. AMR genes were detected persistently across pig farms at all visits, even on farms with low AMU, whereas AMR bacteria was consistently lower on cattle farms than pigs, even for those with comparably high AMU. MDR bacteria was also more commonly detected on pig farms than any other livestock species. DISCUSSION: The results may be explained by a complex combination of factors on pig farms including historic AMU; co-selection of AMR bacteria; variation in amounts of antimicrobials used between visits; potential persistence in environmental reservoirs of AMR bacteria; or importation of pigs with AMR microbiota from supplying farms. Pig farms may also be at increased risk of AMR due to the greater use of oral routes of group antimicrobial treatment, which were less targeted than cattle treatments; the latter mostly administered to individual animals. Also, farms which exhibited either increasing or decreasing trends of AMR across the study did not have corresponding trends in their AMU. Therefore, our results suggest that factors other than AMU on individual farms are important for persistence of AMR bacteria on farms, which may be operating at the farm and livestock species level. Frontiers Media S.A. 2023-03-14 /pmc/articles/PMC10043416/ /pubmed/36998408 http://dx.doi.org/10.3389/fmicb.2023.1070340 Text en Copyright © 2023 Smith, May, AbuOun, Stubberfield, Gilson, Chau, Crook, Shaw, Read, Stoesser, Vilar and Anjum. 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
Smith, Richard P.
May, Hannah E.
AbuOun, Manal
Stubberfield, Emma
Gilson, Daniel
Chau, Kevin K.
Crook, Derrick W.
Shaw, Liam P.
Read, Daniel S.
Stoesser, Nicole
Vilar, Maria Jose
Anjum, Muna F.
A longitudinal study reveals persistence of antimicrobial resistance on livestock farms is not due to antimicrobial usage alone
title A longitudinal study reveals persistence of antimicrobial resistance on livestock farms is not due to antimicrobial usage alone
title_full A longitudinal study reveals persistence of antimicrobial resistance on livestock farms is not due to antimicrobial usage alone
title_fullStr A longitudinal study reveals persistence of antimicrobial resistance on livestock farms is not due to antimicrobial usage alone
title_full_unstemmed A longitudinal study reveals persistence of antimicrobial resistance on livestock farms is not due to antimicrobial usage alone
title_short A longitudinal study reveals persistence of antimicrobial resistance on livestock farms is not due to antimicrobial usage alone
title_sort longitudinal study reveals persistence of antimicrobial resistance on livestock farms is not due to antimicrobial usage alone
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10043416/
https://www.ncbi.nlm.nih.gov/pubmed/36998408
http://dx.doi.org/10.3389/fmicb.2023.1070340
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