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The Journal of antimicrobial chemotherapy2016; 71(6); 1497-1500; doi: 10.1093/jac/dkw006

High prevalence of international ESBL CTX-M-15-producing Enterobacter cloacae ST114 clone in animals.

Abstract: The objective of this study was to characterize ESBL-producing Enterobacter cloacae isolated from animals and to compare their clonal distribution with that of human-related isolates. Among 635 clinical E. cloacae from horses, dogs and cats collected in France between 2010 and 2013, 36 were resistant to ceftiofur as determined by disc diffusion. ESBL genes were identified by sequencing. Plasmids carrying ESBL-encoding genes were characterized by PCR-based replicon typing, S1-PFGE and Southern blotting. IncHI2 plasmids were subtyped using the plasmid double-locus sequence typing scheme and multiplex amplification of the hipA, smr0092 and smr0183 genes. All E. cloacae were typed by PFGE and MLST. ST clustering was analysed by eBURST. All 36 ceftiofur-resistant E. cloacae produced an ESBL. Their PFGE patterns formed 23 clusters of high similarity and 13 STs and were isolated from epidemiologically unrelated animals (14 horses, 11 dogs and 11 cats) distributed throughout France. ST114, the most prevalent clone in humans, was over-represented in animals (16/36) compared with other human-related clones detected here. The blaCTX-M-15 gene was dominant (66.7%) and mostly carried on IncHI2 plasmids (ST1 subtype). ST114 isolates always produced CTX-M-15. Most ESBL-producing E. cloacae from animals studied here (69.4%) belonged to potentially high-risk clones in humans, in particular ST114 (44.4%). These data raise questions and potential concerns about the transfer of E. cloacae between animals and humans.
© The Author 2016. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.
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Publication Date: 2016-02-04 PubMed ID: 26850718DOI: 10.1093/jac/dkw006Google Scholar: Lookup
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  • Comparative Study
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research analysed Extended-Spectrum B-Lactamases (ESBL)-producing Enterobacter cloacae bacteria in animals and found a high frequency of clones linked to human infections. It brings attention to the potential danger of bacteria transfer between animals and humans.

Objective

The primary aim of this research was to investigate the existence and distribution of ESBL-producing Enterobacter cloacae in animal clinical isolates and compare these to clones found in human infections.

Methodology

  • A total of 635 clinical isolates from dogs, cats, and horses were tested for resistance to ceftiofur, an antibiotic, through disc diffusion.
  • The required ESBL genes were recognized on sequenced genomes.
  • The genomes carrying ESBL-encoding genes were further analyzed using a variety of techniques, including PCR-based replicon typing, S1-PFGE, Southern blotting, and sequence typing scheme.
  • All the E. cloacae types were differentiated with different typing methods such as MLST and PFGE.
  • The clustering of different STs was analyzed using eBURST.

Findings

  • It was found that all 36 ceftiofur-resistant E. cloacae released an ESBL.
  • The 36 isolates exhibited various PFGE patterns, forming 23 distinctive clusters.
  • These isolates were found distributed across France, coming from different animals, including 14 horses, 11 dogs, and 11 cats.
  • The ST114 clone, which is prevalent in human infections, was abundantly found in animals.
  • The blaCTX-M-15 gene, frequently carried on IncHI2 plasmids, was the most dominant, especially in ST114 isolates.
  • Almost 70% of the ESBL-producing E. cloacae from the animals belonged to ST clones that are potentially high-risk for humans, especially ST114.

Conclusion

The study indicates a potentially high risk of transfer of E. cloacae bacteria from animals to humans, particularly concerning the ST114 clone. The findings may help in future studies and surveillance to prevent bacterial transfer and the potential emergence of antibiotic-resistant strains.

Cite This Article

APA
Haenni M, Saras E, Ponsin C, Dahmen S, Petitjean M, Hocquet D, Madec JY. (2016). High prevalence of international ESBL CTX-M-15-producing Enterobacter cloacae ST114 clone in animals. J Antimicrob Chemother, 71(6), 1497-1500. https://doi.org/10.1093/jac/dkw006

Publication

The Journal of antimicrobial chemotherapy
ISSN: 1460-2091
NlmUniqueID: 7513617
Country: England
Language: English
Volume: 71
Issue: 6
Pages: 1497-1500

Researcher Affiliations

Haenni, Marisa
  • Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail (ANSES), Unité Antibiorésistance et Virulence Bactériennes, Lyon, France marisa.haenni@anses.fr.
Saras, Estelle
  • Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail (ANSES), Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.
Ponsin, Cécile
  • Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail (ANSES), Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.
Dahmen, Safia
  • Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail (ANSES), Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.
Petitjean, Marie
  • Laboratoire d'Hygiène Hospitalière, Centre Hospitalier Universitaire, Laboratoire Chrono-environnement UMR CNRS 6249, Univ. Bourgogne Franche-Comté, F-25000 Besançon, France.
Hocquet, Didier
  • Laboratoire d'Hygiène Hospitalière, Centre Hospitalier Universitaire, Laboratoire Chrono-environnement UMR CNRS 6249, Univ. Bourgogne Franche-Comté, F-25000 Besançon, France.
Madec, Jean-Yves
  • Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail (ANSES), Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.

MeSH Terms

  • Animals
  • Blotting, Southern
  • Cats
  • Disk Diffusion Antimicrobial Tests
  • Dogs
  • Electrophoresis, Gel, Pulsed-Field
  • Enterobacter cloacae / classification
  • Enterobacter cloacae / enzymology
  • Enterobacter cloacae / genetics
  • Enterobacter cloacae / isolation & purification
  • Enterobacteriaceae Infections / epidemiology
  • Enterobacteriaceae Infections / microbiology
  • Enterobacteriaceae Infections / veterinary
  • France / epidemiology
  • Genotype
  • Molecular Epidemiology
  • Molecular Typing
  • Multilocus Sequence Typing
  • Plasmids / analysis
  • Plasmids / classification
  • Prevalence
  • Sequence Analysis, DNA
  • beta-Lactamases / analysis

Citations

This article has been cited 24 times.
  1. Marouf S, Li X, Salem HM, Ahmed ZS, Nader SM, Shaalan M, Awad FH, Zhou H, Cheang T. Molecular detection of multidrug-resistant Pseudomonas aeruginosa of different avian sources with pathogenicity testing and in vitro evaluation of antibacterial efficacy of silver nanoparticles against multidrug-resistant P. aeruginosa. Poult Sci 2023 Aug 2;102(10):102995.
    doi: 10.1016/j.psj.2023.102995pubmed: 37566970google scholar: lookup
  2. Merhi G, Amayri S, Bitar I, Araj GF, Tokajian S. Whole Genome-Based Characterization of Multidrug Resistant Enterobacter and Klebsiella aerogenes Isolates from Lebanon. Microbiol Spectr 2023 Feb 14;11(1):e0291722.
    doi: 10.1128/spectrum.02917-22pubmed: 36651778google scholar: lookup
  3. Pot M, Reynaud Y, Couvin D, Dereeper A, Ferdinand S, Bastian S, Foucan T, Pommier JD, Valette M, Talarmin A, Guyomard-Rabenirina S, Breurec S. Emergence of a Novel Lineage and Wide Spread of a bla(CTX-M-15)/IncHI2/ST1 Plasmid among Nosocomial Enterobacter in Guadeloupe. Antibiotics (Basel) 2022 Oct 20;11(10).
    doi: 10.3390/antibiotics11101443pubmed: 36290101google scholar: lookup
  4. He Z, Yang S, Ma Y, Zhang S, Cao Z. Detection of CTX-M-15 Extended-Spectrum β-Lactamases Producing Escherichia coli Isolates from Colostrum and Faeces of Newborn Dairy Calves in China. Pathogens 2021 Sep 9;10(9).
    doi: 10.3390/pathogens10091162pubmed: 34578194google scholar: lookup
  5. Shurina BA, Page RC. Structural Comparisons of Cefotaximase (CTX-M-ase) Sub Family 1. Front Microbiol 2021;12:688509.
    doi: 10.3389/fmicb.2021.688509pubmed: 34504475google scholar: lookup
  6. Pot M, Reynaud Y, Couvin D, Ducat C, Ferdinand S, Gravey F, Gruel G, Guérin F, Malpote E, Breurec S, Talarmin A, Guyomard-Rabenirina S. Wide Distribution and Specific Resistance Pattern to Third-Generation Cephalosporins of Enterobacter cloacae Complex Members in Humans and in the Environment in Guadeloupe (French West Indies). Front Microbiol 2021;12:628058.
    doi: 10.3389/fmicb.2021.628058pubmed: 34248862google scholar: lookup
  7. Nielsen SS, Bicout DJ, Calistri P, Canali E, Drewe JA, Garin-Bastuji B, Gonzales Rojas JL, Gortazar Schmidt C, Herskin M, Michel V, Miranda Chueca MA, Padalino B, Pasquali P, Roberts HC, Sihvonen LH, Spoolder H, Stahl K, Velarde A, Viltrop A, Winckler C, Guardabassi L, Hilbert F, Mader R, Aznar I, Baldinelli F, Alvarez J. Assessment of animal diseases caused by bacteria resistant to antimicrobials: Dogs and cats. EFSA J 2021 Jun;19(6):e06680.
    doi: 10.2903/j.efsa.2021.6680pubmed: 34194578google scholar: lookup
  8. Shnaiderman-Torban A, Marchaim D, Navon-Venezia S, Lubrani O, Paitan Y, Arielly H, Steinman A. Third Generation Cephalosporin Resistant Enterobacterales Infections in Hospitalized Horses and Donkeys: A Case-Case-Control Analysis. Antibiotics (Basel) 2021 Feb 4;10(2).
    doi: 10.3390/antibiotics10020155pubmed: 33557061google scholar: lookup
  9. Pot M, Guyomard-Rabenirina S, Couvin D, Ducat C, Enouf V, Ferdinand S, Gruel G, Malpote E, Talarmin A, Breurec S, Reynaud Y. Dissemination of Extended-Spectrum-β-Lactamase-Producing Enterobacter cloacae Complex from a Hospital to the Nearby Environment in Guadeloupe (French West Indies): ST114 Lineage Coding for a Successful IncHI2/ST1 Plasmid. Antimicrob Agents Chemother 2021 Feb 17;65(3).
    doi: 10.1128/AAC.02146-20pubmed: 33361294google scholar: lookup
  10. Loncaric I, Misic D, Szostak MP, Künzel F, Schäfer-Somi S, Spergser J. Broad-Spectrum Cephalosporin-Resistant and/or Fluoroquinolone-Resistant Enterobacterales Associated with Canine and Feline Urogenital Infections. Antibiotics (Basel) 2020 Jul 7;9(7).
    doi: 10.3390/antibiotics9070387pubmed: 32645942google scholar: lookup
  11. Wang S, Zhou K, Xiao S, Xie L, Gu F, Li X, Ni Y, Sun J, Han L. A Multidrug Resistance Plasmid pIMP26, Carrying bla(IMP-26), fosA5, bla(DHA-1), and qnrB4 in Enterobacter cloacae. Sci Rep 2019 Jul 15;9(1):10212.
    doi: 10.1038/s41598-019-46777-6pubmed: 31308469google scholar: lookup
  12. Gozi KS, Froes JR, Deus Ajude LPT, da Silva CR, Baptista RS, Peiró JR, Marinho M, Mendes LCN, Nogueira MCL, Casella T. Dissemination of Multidrug-Resistant Commensal Escherichia coli in Feedlot Lambs in Southeastern Brazil. Front Microbiol 2019;10:1394.
    doi: 10.3389/fmicb.2019.01394pubmed: 31293542google scholar: lookup
  13. Zeng H, Lei T, He W, Zhang J, Liang B, Li C, Ling N, Ding Y, Wu S, Wang J, Wu Q. Novel Multidrug-Resistant Cronobacter sakazakii Causing Meningitis in Neonate, China, 2015. Emerg Infect Dis 2018 Nov;24(11):2121-2124.
    doi: 10.3201/eid2411.180718pubmed: 30334728google scholar: lookup
  14. Dandachi I, Chabou S, Daoud Z, Rolain JM. Prevalence and Emergence of Extended-Spectrum Cephalosporin-, Carbapenem- and Colistin-Resistant Gram Negative Bacteria of Animal Origin in the Mediterranean Basin. Front Microbiol 2018;9:2299.
    doi: 10.3389/fmicb.2018.02299pubmed: 30323797google scholar: lookup
  15. Peirano G, Matsumura Y, Adams MD, Bradford P, Motyl M, Chen L, Kreiswirth BN, Pitout JDD. Genomic Epidemiology of Global Carbapenemase-Producing Enterobacter spp., 2008-2014. Emerg Infect Dis 2018 Jun;24(6):1010-1019.
    doi: 10.3201/eid2406.171648pubmed: 29774858google scholar: lookup
  16. Zogg AL, Simmen S, Zurfluh K, Stephan R, Schmitt SN, Nüesch-Inderbinen M. High Prevalence of Extended-Spectrum β-Lactamase Producing Enterobacteriaceae Among Clinical Isolates From Cats and Dogs Admitted to a Veterinary Hospital in Switzerland. Front Vet Sci 2018;5:62.
    doi: 10.3389/fvets.2018.00062pubmed: 29662886google scholar: lookup
  17. Dandachi I, Sokhn ES, Dahdouh EA, Azar E, El-Bazzal B, Rolain JM, Daoud Z. Prevalence and Characterization of Multi-Drug-Resistant Gram-Negative Bacilli Isolated From Lebanese Poultry: A Nationwide Study. Front Microbiol 2018;9:550.
    doi: 10.3389/fmicb.2018.00550pubmed: 29628921google scholar: lookup
  18. Wang S, Xiao SZ, Gu FF, Tang J, Guo XK, Ni YX, Qu JM, Han LZ. Antimicrobial susceptibility and molecular epidemiology of clinical Enterobacter cloacae bloodstream isolates in Shanghai, China. PLoS One 2017;12(12):e0189713.
    doi: 10.1371/journal.pone.0189713pubmed: 29244831google scholar: lookup
  19. Wang J, Ma ZB, Zeng ZL, Yang XW, Huang Y, Liu JH. The role of wildlife (wild birds) in the global transmission of antimicrobial resistance genes. Zool Res 2017 Mar 18;38(2):55-80.
    doi: 10.24272/j.issn.2095-8137.2017.003pubmed: 28409502google scholar: lookup
  20. Harada K, Shimizu T, Mukai Y, Kuwajima K, Sato T, Kajino A, Usui M, Tamura Y, Kimura Y, Miyamoto T, Tsuyuki Y, Ohki A, Kataoka Y. Phenotypic and molecular characterization of antimicrobial resistance in Enterobacter spp. isolates from companion animals in Japan. PLoS One 2017;12(3):e0174178.
    doi: 10.1371/journal.pone.0174178pubmed: 28328967google scholar: lookup
  21. Harel B, Sévin C, Le Hello S, Moreau P, Giard JC, Petry S, Gravey F. Genomic epidemiology of strains currently and formerly classified as Enterobacter spp. recovered from equine necropsy samples. PLoS One 2025;20(11):e0333701.
    doi: 10.1371/journal.pone.0333701pubmed: 41231827google scholar: lookup
  22. Scarpellini R, Assirelli G, Giunti M, Esposito E, Mondo E, Piva S. Monitoring the Prevalence of Antimicrobial Resistance in Companion Animals: Results from Clinical Isolates in an Italian University Veterinary Hospital. Transbound Emerg Dis 2023;2023:6695493.
    doi: 10.1155/2023/6695493pubmed: 40303797google scholar: lookup
  23. Haenni M, Châtre P, Drapeau A, Cazeau G, Troncy J, François P, Madec JY. 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 2025 Feb 3;80(2):567-575.
    doi: 10.1093/jac/dkae448pubmed: 39665267google scholar: lookup
  24. Genath A, Hackmann C, Denkel L, Weber A, Maechler F, Kola A, Schwarz S, Gastmeier P, Leistner R. The genetic relationship between human and pet isolates: a core genome multilocus sequence analysis of multidrug-resistant bacteria. Antimicrob Resist Infect Control 2024 Sep 20;13(1):107.
    doi: 10.1186/s13756-024-01457-7pubmed: 39304920google scholar: lookup
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