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Temporal, Spatial, and Genomic Analyses of Enterobacteriaceae Clinical Antimicrobial Resistance in Companion Animals Reveals Phenotypes and Genotypes of One Health Concern

BACKGROUND: Antimicrobial resistance (AMR) is a globally important one health threat. The impact of resistant infections on companion animals, and the potential public health implications of such infections, has not been widely explored, largely due to an absence of structured population-level data....

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Autores principales: Singleton, David A., Pongchaikul, Pisut, Smith, Shirley, Bengtsson, Rebecca J., Baker, Kate, Timofte, Dorina, Steen, Stephen, Jones, Matthew, Roberts, Larry, Sánchez-Vizcaíno, Fernando, Dawson, Susan, Noble, P.-J. M., Radford, Alan D., Pinchbeck, Gina L., Williams, Nicola J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8362618/
https://www.ncbi.nlm.nih.gov/pubmed/34394045
http://dx.doi.org/10.3389/fmicb.2021.700698
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author Singleton, David A.
Pongchaikul, Pisut
Smith, Shirley
Bengtsson, Rebecca J.
Baker, Kate
Timofte, Dorina
Steen, Stephen
Jones, Matthew
Roberts, Larry
Sánchez-Vizcaíno, Fernando
Dawson, Susan
Noble, P.-J. M.
Radford, Alan D.
Pinchbeck, Gina L.
Williams, Nicola J.
author_facet Singleton, David A.
Pongchaikul, Pisut
Smith, Shirley
Bengtsson, Rebecca J.
Baker, Kate
Timofte, Dorina
Steen, Stephen
Jones, Matthew
Roberts, Larry
Sánchez-Vizcaíno, Fernando
Dawson, Susan
Noble, P.-J. M.
Radford, Alan D.
Pinchbeck, Gina L.
Williams, Nicola J.
author_sort Singleton, David A.
collection PubMed
description BACKGROUND: Antimicrobial resistance (AMR) is a globally important one health threat. The impact of resistant infections on companion animals, and the potential public health implications of such infections, has not been widely explored, largely due to an absence of structured population-level data. OBJECTIVES: We aimed to efficiently capture and repurpose antimicrobial susceptibility test (AST) results data from several veterinary diagnostic laboratories (VDLs) across the United Kingdom to facilitate national companion animal clinical AMR surveillance. We also sought to harness and genotypically characterize isolates of potential AMR importance from these laboratories. METHODS: We summarized AST results for 29,330 canine and 8,279 feline Enterobacteriaceae isolates originating from companion animal clinical practice, performed between April 2016 and July 2018 from four VDLs, with submissions from 2,237 United Kingdom veterinary practice sites. RESULTS: Escherichia coli (E. coli) was the most commonly isolated Enterobacteriaceae in dogs (69.4% of AST results, 95% confidence interval, CI, 68.7–70.0) and cats (90.5%, CI 89.8–91.3). Multi-drug resistance was reported in 14.1% (CI 13.5–14.8) of canine and 12.0% (CI 11.1–12.9) of feline E. coli isolates. Referral practices were associated with increased E. coli 3rd generation ≤ cephalosporin resistance odds (dogs: odds ratio 2.0, CI 1.2–3.4). We selected 95 E. coli isolates for whole genome analyses, of which seven belonged to sequence type 131, also carrying the plasmid-associated extended spectrum β-lactamase gene bla(CTX–M–)(15). The plasmid-mediated colistin resistance gene mcr-9 was also identified for the first time in companion animals. CONCLUSIONS: Linking clinical AMR data with genotypic characterization represents an efficient means of identifying important resistance trends in companion animals on a national scale.
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spelling pubmed-83626182021-08-14 Temporal, Spatial, and Genomic Analyses of Enterobacteriaceae Clinical Antimicrobial Resistance in Companion Animals Reveals Phenotypes and Genotypes of One Health Concern Singleton, David A. Pongchaikul, Pisut Smith, Shirley Bengtsson, Rebecca J. Baker, Kate Timofte, Dorina Steen, Stephen Jones, Matthew Roberts, Larry Sánchez-Vizcaíno, Fernando Dawson, Susan Noble, P.-J. M. Radford, Alan D. Pinchbeck, Gina L. Williams, Nicola J. Front Microbiol Microbiology BACKGROUND: Antimicrobial resistance (AMR) is a globally important one health threat. The impact of resistant infections on companion animals, and the potential public health implications of such infections, has not been widely explored, largely due to an absence of structured population-level data. OBJECTIVES: We aimed to efficiently capture and repurpose antimicrobial susceptibility test (AST) results data from several veterinary diagnostic laboratories (VDLs) across the United Kingdom to facilitate national companion animal clinical AMR surveillance. We also sought to harness and genotypically characterize isolates of potential AMR importance from these laboratories. METHODS: We summarized AST results for 29,330 canine and 8,279 feline Enterobacteriaceae isolates originating from companion animal clinical practice, performed between April 2016 and July 2018 from four VDLs, with submissions from 2,237 United Kingdom veterinary practice sites. RESULTS: Escherichia coli (E. coli) was the most commonly isolated Enterobacteriaceae in dogs (69.4% of AST results, 95% confidence interval, CI, 68.7–70.0) and cats (90.5%, CI 89.8–91.3). Multi-drug resistance was reported in 14.1% (CI 13.5–14.8) of canine and 12.0% (CI 11.1–12.9) of feline E. coli isolates. Referral practices were associated with increased E. coli 3rd generation ≤ cephalosporin resistance odds (dogs: odds ratio 2.0, CI 1.2–3.4). We selected 95 E. coli isolates for whole genome analyses, of which seven belonged to sequence type 131, also carrying the plasmid-associated extended spectrum β-lactamase gene bla(CTX–M–)(15). The plasmid-mediated colistin resistance gene mcr-9 was also identified for the first time in companion animals. CONCLUSIONS: Linking clinical AMR data with genotypic characterization represents an efficient means of identifying important resistance trends in companion animals on a national scale. Frontiers Media S.A. 2021-07-30 /pmc/articles/PMC8362618/ /pubmed/34394045 http://dx.doi.org/10.3389/fmicb.2021.700698 Text en Copyright © 2021 Singleton, Pongchaikul, Smith, Bengtsson, Baker, Timofte, Steen, Jones, Roberts, Sánchez-Vizcaíno, Dawson, Noble, Radford, Pinchbeck and Williams. 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
Singleton, David A.
Pongchaikul, Pisut
Smith, Shirley
Bengtsson, Rebecca J.
Baker, Kate
Timofte, Dorina
Steen, Stephen
Jones, Matthew
Roberts, Larry
Sánchez-Vizcaíno, Fernando
Dawson, Susan
Noble, P.-J. M.
Radford, Alan D.
Pinchbeck, Gina L.
Williams, Nicola J.
Temporal, Spatial, and Genomic Analyses of Enterobacteriaceae Clinical Antimicrobial Resistance in Companion Animals Reveals Phenotypes and Genotypes of One Health Concern
title Temporal, Spatial, and Genomic Analyses of Enterobacteriaceae Clinical Antimicrobial Resistance in Companion Animals Reveals Phenotypes and Genotypes of One Health Concern
title_full Temporal, Spatial, and Genomic Analyses of Enterobacteriaceae Clinical Antimicrobial Resistance in Companion Animals Reveals Phenotypes and Genotypes of One Health Concern
title_fullStr Temporal, Spatial, and Genomic Analyses of Enterobacteriaceae Clinical Antimicrobial Resistance in Companion Animals Reveals Phenotypes and Genotypes of One Health Concern
title_full_unstemmed Temporal, Spatial, and Genomic Analyses of Enterobacteriaceae Clinical Antimicrobial Resistance in Companion Animals Reveals Phenotypes and Genotypes of One Health Concern
title_short Temporal, Spatial, and Genomic Analyses of Enterobacteriaceae Clinical Antimicrobial Resistance in Companion Animals Reveals Phenotypes and Genotypes of One Health Concern
title_sort temporal, spatial, and genomic analyses of enterobacteriaceae clinical antimicrobial resistance in companion animals reveals phenotypes and genotypes of one health concern
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8362618/
https://www.ncbi.nlm.nih.gov/pubmed/34394045
http://dx.doi.org/10.3389/fmicb.2021.700698
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