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Home / Equine Research Bank / J Antimicrob Chemother / Distinct molecular epidemiology of resistances to extended-s...
The Journal of antimicrobial chemotherapy2024; 80(2); 567-575; doi: 10.1093/jac/dkae448

Distinct molecular epidemiology of resistances to extended-spectrum cephalosporins and carbapenems in Enterobacter hormaechei in cats and dogs versus horses in France.

Abstract: Enterobacter hormaechei is an important pathogen in humans and animals, which, in addition to its intrinsic AmpC, can acquire a wide variety of genes conferring resistances to extended-spectrum cephalosporins (ESCs) and carbapenems (CPs). In France, human clinical outbreaks of E. hormaechei resistant to ESC or carbapenem were reported. Objective: To study E. hormaechei isolates from cats and dogs (=59) as well as from horses (n = 55) presenting a non-susceptible phenotype to beta-lactams in order to determine which clones, resistance genes and plasmids are circulating in France. Methods: E. hormaechei isolates (n = 114) were short-read sequenced and five isolates were long-read sequenced to better characterize the plasmids carrying ESC- and CP-resistance determinants. Phenotypes were characterized by antibiograms using the disc diffusion method. Results: A clear divergence in the molecular epidemiology was observed depending on the host. In cats and dogs, most of the isolates presented an overexpressed ampC gene or the blaCTX-M-15 gene carried by an IncHI2 plasmid, and eight isolates (8/59, 13.6%) presented the blaOXA-48 carbapenemase gene. Thirty-two isolates (32/59, 54.2%) belonged to the human high-risk clones ST78, ST114 and ST171. Contrarily, in horses, ESC resistance was mostly due to the blaSHV-12 and blaCTX-M-15 genes carried by an IncHI2 plasmid, and high-risk clones were rarely identified (5/55, 9.0%). Conclusions: Potential selection by antibiotic use (which is on an increasing trend in France for cats, dogs and horses), the dissemination capacities of both conjugative IncHI2 plasmids and high-risk clones, and possible transfers of resistant bacteria between humans and animals strongly indicate that E. hormaechei should be closely monitored.
© The Author(s) 2024. Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy.
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Publication Date: 2024-12-12 PubMed ID: 39665267PubMed Central: PMC11787895DOI: 10.1093/jac/dkae448Google Scholar: Lookup
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Summary

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Overview

  • This research investigates the molecular characteristics of antibiotic resistance in Enterobacter hormaechei isolated from cats, dogs, and horses in France, focusing on differences in the strains and resistance genes found in these animals, particularly regarding resistance to extended-spectrum cephalosporins (ESCs) and carbapenems (CPs).

Introduction and Background

  • Enterobacter hormaechei is a bacterial pathogen affecting both humans and animals.
  • It naturally possesses an enzyme called AmpC beta-lactamase but can also acquire genes that provide resistance to important antibiotics such as ESCs and CPs.
  • Escalating antibiotic resistance in E. hormaechei has been reported in human clinical outbreaks in France.
  • The study focuses on identifying how these resistant bacteria differ between animal hosts — specifically, cats and dogs versus horses — and the implications for antibiotic resistance spread.

Objectives

  • To analyze E. hormaechei isolates from pets (cats and dogs) and horses with reduced susceptibility to beta-lactam antibiotics.
  • To characterize the bacterial clones, resistance genes, and plasmids circulating in France within these animals.

Methods

  • A total of 114 E. hormaechei isolates were collected: 59 from cats and dogs, and 55 from horses.
  • Short-read whole-genome sequencing was performed on all isolates to study their genetic makeup.
  • Five selected isolates underwent long-read sequencing to more precisely analyze plasmids carrying resistance genes.
  • Antibiotic susceptibility was assessed using antibiograms through the disc diffusion method.

Key Findings

  • Molecular differences by host animal:
    • In cats and dogs:
      • Most isolates showed either overexpression of the intrinsic ampC gene or carried the blaCTX-M-15 gene, which confers extended-spectrum cephalosporin resistance.
      • The blaCTX-M-15 gene was mostly located on IncHI2 plasmids, which are mobile genetic elements capable of transferring resistance between bacteria.
      • Eight isolates (13.6%) carried the blaOXA-48 gene encoding carbapenem resistance.
      • More than half of these isolates (54.2%) corresponded to known human high-risk clones (ST78, ST114, ST171), known for spreading resistance.
    • In horses:
      • Resistance to ESCs was predominantly due to blaSHV-12 and blaCTX-M-15 genes, mostly on IncHI2 plasmids.
      • High-risk human clones were rare, only detected in 9.0% of isolates.

Interpretation and Implications

  • The significant difference in molecular epidemiology between companion animals (cats and dogs) and horses indicates distinct reservoirs and transmission pathways of resistance genes.
  • High-risk human-associated bacterial clones being prevalent in cats and dogs suggests a potential for cross-species transmission between humans and pets.
  • The recurring presence of IncHI2 plasmids, known to spread resistance genes effectively, highlights a concerning mechanism for dissemination across bacterial populations.
  • Antibiotic use in animals, which is rising in France, may be selecting for resistant strains, raising the risk of further resistance development and spread.
  • Close monitoring and surveillance of E. hormaechei are advised to better control the spread of these resistant bacteria in both veterinary and human medicine settings.

Conclusions

  • The study reveals host-specific differences in the molecular epidemiology and resistance mechanisms of E. hormaechei in France.
  • The findings emphasize the importance of monitoring antibiotic resistance in animal pathogens due to their potential impact on human health.
  • Strategies to mitigate the spread should consider antibiotic stewardship in veterinary medicine and efforts to understand the epidemiology of plasmid-mediated and clonal dissemination of resistance.

Cite This Article

APA
Haenni M, Châtre P, Drapeau A, Cazeau G, Troncy J, François P, Madec JY. (2024). Distinct molecular epidemiology of resistances to extended-spectrum cephalosporins and carbapenems in Enterobacter hormaechei in cats and dogs versus horses in France. J Antimicrob Chemother, 80(2), 567-575. https://doi.org/10.1093/jac/dkae448

Publication

The Journal of antimicrobial chemotherapy
ISSN: 1460-2091
NlmUniqueID: 7513617
Country: England
Language: English
Volume: 80
Issue: 2
Pages: 567-575

Researcher Affiliations

Haenni, Marisa
  • ANSES-Université de Lyon, Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.
Châtre, Pierre
  • ANSES-Université de Lyon, Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.
Drapeau, Antoine
  • ANSES-Université de Lyon, Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.
Cazeau, Géraldine
  • ANSES-Université de Lyon, Unité Epidémiologie et Appui à la Surveillance, Lyon, France.
Troncy, Jonathan
  • ANSES-Université de Lyon, Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.
François, Pauline
  • ANSES-Université de Lyon, Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.
Madec, Jean-Yves
  • ANSES-Université de Lyon, Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.

MeSH Terms

  • Animals
  • Horses
  • France / epidemiology
  • Cats
  • Enterobacteriaceae Infections / veterinary
  • Enterobacteriaceae Infections / epidemiology
  • Enterobacteriaceae Infections / microbiology
  • Cephalosporins / pharmacology
  • Dogs
  • Anti-Bacterial Agents / pharmacology
  • Enterobacter / drug effects
  • Enterobacter / genetics
  • Enterobacter / isolation & purification
  • Carbapenems / pharmacology
  • Plasmids / analysis
  • Molecular Epidemiology
  • Microbial Sensitivity Tests
  • beta-Lactamases / genetics
  • Cat Diseases / microbiology
  • Cat Diseases / epidemiology
  • Sequence Analysis, DNA
  • Dog Diseases / microbiology
  • Dog Diseases / epidemiology
  • Horse Diseases / microbiology
  • Horse Diseases / epidemiology

Grant Funding

  • ANSES

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Citations

This article has been cited 1 times.
  1. De Maayer P, Green T, Jordan S, Smits THM, Coutinho TA. Pan-genome analysis of the Enterobacter hormaechei complex highlights its genomic flexibility and pertinence as a multidrug resistant pathogen.. BMC Genomics 2025 Apr 26;26(1):408.
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