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

David A Singleton, Pisut Pongchaikul, Shirley Smith, Rebecca J Bengtsson, Kate Baker, Dorina Timofte, Stephen Steen, Matthew Jones , Larry Roberts , Fernando Sánchez-Vizcaíno, Susan Dawson , P-J.M Noble, Alan D Radford, Gina L Pinchbeck, Nicola J Williams

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Abstract

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.
Original languageEnglish
Article number700698
JournalFrontiers in Microbiology
Volume12
Issue number700698
DOIs
Publication statusPublished - 30 Jul 2021

Bibliographical note

Funding Information:
We wish to thank data providers both in veterinary practice (VetSolutions, Teleos, CVS, and other practitioners) and especially in veterinary diagnostic laboratories, without whose support and participation this research would not be possible. Finally, we are especially grateful for the help and support provided by SAVSNET team members Susan Bolan, Bethaney Brant, and Steven Smyth. Funding. This work was funded by The Veterinary Medicines Directorate (VM0520), the University of Liverpool and SAVSNET. We are extremely grateful for the support and major funding from BBSRC (BB/N019547/1) and BSAVA. KB was funded through a Wellcome Trust Clinical Research Career Development Award (106690/A/14/Z), and supported RB through a United Kingdom Research and Innovation Medical Research Council New Investigator Research Grant (MR/R020787/1).

Publisher Copyright:
© Copyright © 2021 Singleton, Pongchaikul, Smith, Bengtsson, Baker, Timofte, Steen, Jones, Roberts, Sánchez-Vizcaíno, Dawson, Noble, Radford, Pinchbeck and Williams.

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