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High genetic diversity of extended-spectrum β-lactamases producing Escherichia coli in feces of horses.
Abstract: Extended-spectrum beta-lactamases (ESBLs), especially those of the CTX-M type, represent a major public health problem throughout the world. Although the carriage of ESBL-producing Enterobacteriaceae (EPE) in feces of horses is now well recognized, little is known about the diversity of EPE after treatment of horses with antibiotics. We undertook this study to assess and follow the diversity of EP Escherichia coli isolated from horses after antibiotic treatment for an infection. Fecal samples from two horses treated and two that were untreated were tested for the presence of EPE on different days. All isolated E. coli strains were evaluated for antimicrobial resistance (AMR) and by whole-genome sequencing. Multi locus sequence typing, phylogrouping, resistance genes and plasmid content were extracted from genomic data. A phylogenetic analysis based on single nucleotide polymorphism (SNP) divergence was also performed on the core genome. We isolated 35 strains belonging to the A, B1 and C phylo-groups. All but one expressed SHV-12 enzymes and one expressed CTX-M-1. Intra- and inter-horse genetic diversity of E. coli strains was identified in the genome analysis and 10 AMR profiles. Two distinct EP E. coli-resistant populations (phylo-group B1: ST4164-AMR3 and ST155-AMR2) were found in one horse, and five other resistant populations were found in the second horse (phylo-group A: ST1250-AMR1; phylo-group B1: ST1250-AMR1, ST6981-AMR1 and phylo-group C: ST10-AMR4). Some persistent EP E. coli strains were detected at least 1 month after treatment. These results indicate that EP E. coli strains isolated from horse feces show intra- and inter-host genetic diversity, even in a region with low ESBL prevalence and in horses that are rarely treated with third-generation cephalosporins. These results also suggest that horizontal gene transfer and/or selection of resistance genes probably occurs in vivo within the horse gut microbiome. Follow-up of EP E. coli resistance profiles for at least 1 month after treatment is warranted to prevent persistence of EP E. coli.
Copyright © 2018 Elsevier B.V. All rights reserved.
Publication Date: 2018-04-15 PubMed ID: 29778183DOI: 10.1016/j.vetmic.2018.04.016Google Scholar: Lookup The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
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The researchers undertook a study to investigate the diversity of bacteria known as ESBL-producing Escherichia coli in the feces of horses especially after antibiotic treatment. The study identified a high genetic diversity in both treated and untreated horses, also discovered that some strains of the bacteria persisted a month after treatment.
Research Methodology
- The researchers collected fecal samples from two pairs of horses: those treated with antibiotics and those who were not.
- The samples were tested for the presence of ESBL-producing Escherichia coli (EPE) at different points in time.
- All E. coli strains that were isolated underwent tests for antimicrobial resistance and genome sequencing.
- The researchers extracted multi locus sequence typing, phylogrouping, resistance genes, and plasmid content from the genomic data to analyze the diversity of the bacteria.
- A phylogenetic analysis based on single nucleotide polymorphism divergence was performed on the core genome of the isolates.
Findings
- The researchers isolated 35 strains of E. coli, all of which were part of the A, B1 and C phylo-groups.
- Almost all the strains expressed SHV-12 enzymes (a type of ESBLs), and one expressed CTX-M-1.
- Different E. coli strains were found in the same horse, showing intra-host diversity. Further, the strains found were different between the two horses, demonstrating inter-host diversity.
- Some strains of EPE were found to be persistent, remaining detectable at least a month after antibiotic treatment.
Significance of Results
- The results show that E. coli isolated from horse feces show a high degree of genetic diversity, even in horses from regions with low prevalence of ESBLs and not frequently treated with antibiotics like third-generation cephalosporins.
- The persistence of some strains after treatment suggests that both horizontal gene transfer and selection of resistance genes probably occur within the horse gut microbiome.
- The findings hint at the necessity for follow-up of E. coli resistance profiles for at least a month after treatment to prevent the persistence of these bacteria.
Cite This Article
APA
Sadikalay S, Reynaud Y, Guyomard-Rabenirina S, Falord M, Ducat C, Fabre L, Le Hello S, Talarmin A, Ferdinand S.
(2018).
High genetic diversity of extended-spectrum β-lactamases producing Escherichia coli in feces of horses.
Vet Microbiol, 219, 117-122.
https://doi.org/10.1016/j.vetmic.2018.04.016 Publication
Researcher Affiliations
- Unité Environnement Santé, Institut Pasteur de Guadeloupe, Les Abymes, Guadeloupe, France.
- Unité Environnement Santé, Institut Pasteur de Guadeloupe, Les Abymes, Guadeloupe, France.
- Unité Environnement Santé, Institut Pasteur de Guadeloupe, Les Abymes, Guadeloupe, France.
- Unité Environnement Santé, Institut Pasteur de Guadeloupe, Les Abymes, Guadeloupe, France.
- Unité Environnement Santé, Institut Pasteur de Guadeloupe, Les Abymes, Guadeloupe, France.
- Institut Pasteur, Unité des Bactéries Pathogènes Entériques, Centre National de Réfé.rence des Escherichia coli, Shigella et Salmonella, Paris, France.
- Institut Pasteur, Unité des Bactéries Pathogènes Entériques, Centre National de Réfé.rence des Escherichia coli, Shigella et Salmonella, Paris, France.
- Unité Environnement Santé, Institut Pasteur de Guadeloupe, Les Abymes, Guadeloupe, France.
- Unité Environnement Santé, Institut Pasteur de Guadeloupe, Les Abymes, Guadeloupe, France. Electronic address: sferdinand@pasteur-guadeloupe.fr.
MeSH Terms
- Animals
- Anti-Bacterial Agents / pharmacology
- Drug Resistance, Multiple, Bacterial / genetics
- Escherichia coli / classification
- Escherichia coli / drug effects
- Escherichia coli / enzymology
- Escherichia coli / genetics
- Escherichia coli Infections / microbiology
- Escherichia coli Infections / veterinary
- Escherichia coli Proteins / biosynthesis
- Escherichia coli Proteins / drug effects
- Escherichia coli Proteins / genetics
- Feces / microbiology
- Gastrointestinal Microbiome
- Gene Transfer, Horizontal
- Genetic Variation
- Horses / microbiology
- Microbial Sensitivity Tests
- Phylogeny
- Plasmids
- Whole Genome Sequencing
- beta-Lactamases / biosynthesis
- beta-Lactamases / drug effects
- beta-Lactamases / genetics
Citations
This article has been cited 11 times.- Wongtawan T, Narinthorn R, Sontigun N, Sansamur C, Petcharat Y, Fungwithaya P, Saengsawang P, Blackall PJ, Thomrongsuwannakij T. Characterizing the antimicrobial resistance profile of Escherichia coli found in sport animals (fighting cocks, fighting bulls, and sport horses) and soils from their environment. Vet World 2022 Nov;15(11):2673-2680.
- Gruel G, Couvin D, Guyomard-Rabenirina S, Arlet G, Bambou JC, Pot M, Roy X, Talarmin A, Tressieres B, Ferdinand S, Breurec S. High Prevalence of bla (CTXM-1)/IncI1-Iγ/ST3 Plasmids in Extended-Spectrum β-Lactamase-Producing Escherichia coli Isolates Collected From Domestic Animals in Guadeloupe (French West Indies). Front Microbiol 2022;13:882422.
- Thomson K, Eskola K, Eklund M, Suominen K, Määttä M, Junnila J, Nykäsenoja S, Niinistö K, Grönthal T, Rantala M. Characterisation of and risk factors for extended-spectrum β-lactamase producing Enterobacterales (ESBL-E) in an equine hospital with a special reference to an outbreak caused by Klebsiella pneumoniae ST307:CTX-M-1. Acta Vet Scand 2022 Feb 9;64(1):4.
- Gruel G, Sellin A, Riveiro H, Pot M, Breurec S, Guyomard-Rabenirina S, Talarmin A, Ferdinand S. Antimicrobial use and resistance in Escherichia coli from healthy food-producing animals in Guadeloupe. BMC Vet Res 2021 Mar 8;17(1):116.
- Valcek A, Sismova P, Nesporova K, Overballe-Petersen S, Bitar I, Jamborova I, Kant A, Hrabak J, Wagenaar JA, Madec JY, Damborg P, van Duijkeren E, Ewers C, Hordijk J, Hasman H, Brouwer MSM, Dolejska M. Horsing around: Escherichia coli ST1250 of equine origin harbouring epidemic IncHI1/ST9 plasmid with bla (CTX-M-1) and an operon for short-chain fructooligosaccharides metabolism. Antimicrob Agents Chemother 2023 May 1;65(5).
- Shnaiderman-Torban A, Navon-Venezia S, Paitan Y, Archer H, Abu Ahmad W, Bonder D, Hanael E, Nissan I, Zizelski Valenci G, Weese SJ, Steinman A. Extended spectrum β lactamase-producing Enterobacteriaceae shedding by race horses in Ontario, Canada. BMC Vet Res 2020 Dec 9;16(1):479.
- Hordijk J, Farmakioti E, Smit LAM, Duim B, Graveland H, Theelen MJP, Wagenaar JA. Fecal Carriage of Extended-Spectrum-β-Lactamase/AmpC-Producing Escherichia coli in Horses. Appl Environ Microbiol 2020 Apr 1;86(8).
- Sadikalay S, Cavé L, Ducat C, Mauriello G, Berchel M, Boismoreau D, Guyomard S, Nazaret S, Talarmin A, Ferdinand S. Tracking Enterobacteria, microbiomes, and antibiotic resistance genes from waste to soil with repeated compost applications. PLoS One 2025;20(8):e0329200.
- Caderhoussin A, Couvin D, Gruel G, Quétel I, Pot M, Arquet R, Dereeper A, Bambou JC, Talarmin A, Ferdinand S. The fly route of extended-spectrum-β-lactamase-producing Enterobacteriaceae dissemination in a cattle farm: from the ecosystem to the molecular scale. Front Antibiot 2024;3:1367936.
- Eskola K, Aimo-Koivisto E, Heikinheimo A, Mykkänen A, Hautajärvi T, Grönthal T. Prevalence, risk factors, and characterisation of extended-spectrum β-lactamase -producing Enterobacterales (ESBL-E) in horses entering an equine hospital and description of longitudinal excretion. BMC Vet Res 2024 Sep 13;20(1):412.
- Batantou Mabandza D, Colletin E, Dagot C, Quétel I, Breurec S, Guyomard-Rabenirina S. Do Microorganisms in Bathing Water in Guadeloupe (French West Indies) Have Resistance Genes?. Antibiotics (Basel) 2024 Jan 16;13(1).
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