Spread of multidrug-resistant IncHI1 plasmids carrying ESBL gene blaCTX-M-1 and metabolism operon of prebiotic oligosaccharides in commensal Escherichia coli from healthy horses, France

Maud de Lagarde; Caroline Larrieu; Karine Praud; Nathalie Lallier; Angélina Trotereau; Guillaume Sallé; John M Fairbrother; Catherine Schouler; Benoît Doublet

doi:10.1016/j.ijantimicag.2020.105936

Spread of multidrug-resistant IncHI1 plasmids carrying ESBL gene bla_CTX-M-1 and metabolism operon of prebiotic oligosaccharides in commensal Escherichia coli from healthy horses, France

Int J Antimicrob Agents. 2020 Jun;55(6):105936. doi: 10.1016/j.ijantimicag.2020.105936. Epub 2020 Mar 7.

Authors

Maud de Lagarde¹, Caroline Larrieu², Karine Praud², Nathalie Lallier², Angélina Trotereau², Guillaume Sallé², John M Fairbrother¹, Catherine Schouler², Benoît Doublet³

Affiliations

¹ OIE Reference Laboratory for Escherichia coli, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, Canada.
² INRAE, Université de Tours, ISP, Nouzilly, France.
³ INRAE, Université de Tours, ISP, Nouzilly, France. Electronic address: benoit.doublet@inrae.fr.

PMID: 32156619
DOI: 10.1016/j.ijantimicag.2020.105936

Abstract

The objective of the study was to identify the genetic determinants and characteristics of expanded-spectrum cephalosporin (ESC) resistance in commensal Escherichia coli from healthy horses in France in 2015. Faecal samples from 744 adult horses were screened for ESC-resistant E. coli isolates. The extended-spectrum beta-lactamase (ESBL)/AmpC resistance genes were identified using polymerase chain reaction (PCR) and sequencing. ESC phenotypes were horizontally transferred by conjugation or transformation. Plasmids carrying ESBL/AmpC genes were typed by PCR-based replicon typing, restriction fragment length polymorphism (RFLP), and plasmid multilocus sequence typing (pMLST). The ESC-resistant E. coli isolates were typed by XbaI macrorestriction analysis. Sixteen of 41 stables harboured at least one horse carrying ESC-resistant E. coli. The proportion of individually tested horses carrying ESC-resistant E. coli was 8.5% (28/328). Fifty non-redundant ESC-resistant E. coli isolates showing a great diversity of XbaI macrorestriction profiles belonged mainly to phylogroup B1, and were negative for major E. coli virulence genes, indicating they are commensal isolates. ESBL bla_CTX-M genes were dominant (bla_CTX-M-1, n=34; bla_CTX-M-2, n=8; bla_CTX-M-14, n=2) and located on conjugative plasmids belonging to various incompatibility groups (IncHI1, IncI1, IncN, IncY, or non-typeable). Among these, the multidrug-resistant IncHI1-pST9 plasmids were dominant and simultaneously harboured the bla_CTX-M-1/2 genes and an operon enabling the metabolism of short-chain fructo-oligosaccharides (scFOS). In conclusion, commensal E. coli of French horses displayed a significant distribution of IncHI1-pST9 plasmids carrying both the bla_CTX-M-1/2 gene and the fos metabolism operon. This finding highlights the risk of co-selection of multidrug-resistant IncHI1 plasmids carrying ESBL genes possibly mediated by the use of scFOS as prebiotic in horses.

Keywords: Companion animals; ESBL; Short-chain fructo-oligosaccharides.

MeSH terms

Animals
Anti-Bacterial Agents / pharmacology
Bacterial Proteins / genetics*
Cephalosporins / pharmacology
Conjugation, Genetic
Drug Resistance, Multiple, Bacterial / genetics
Escherichia coli / drug effects
Escherichia coli / genetics*
Escherichia coli / metabolism
Feces / microbiology
France / epidemiology
Horses / microbiology*
Multilocus Sequence Typing
Oligosaccharides / metabolism*
Operon
Phylogeny
Plasmids / genetics*
Prebiotics / microbiology
beta-Lactamases / genetics*

Substances

Anti-Bacterial Agents
Bacterial Proteins
Cephalosporins
Oligosaccharides
Prebiotics
AmpC beta-lactamases
beta-Lactamases