Analyze Diet
BMC veterinary research2020; 16(1); 479; doi: 10.1186/s12917-020-02701-z

Extended spectrum β lactamase-producing Enterobacteriaceae shedding by race horses in Ontario, Canada.

Abstract: We aimed to investigate the prevalence, molecular epidemiology and prevalence factors for Extended Spectrum β-Lactamase-producing Enterobacteriaceae (ESBL-E) shedding by race horses. A cross-sectional study was performed involving fecal samples collected from 169 Thoroughbred horses that were housed at a large racing facility in Ontario, Canada. Samples were enriched, plated on selective plates, sub-cultured to obtain pure cultures and ESBL production was confirmed. Bacterial species were identified and antibiotic susceptibility profiles were assessed. E. coli sequence types (ST) and ESBL genes were determined using multilocus sequence type (MLST) and sequencing. Whole genome sequencing was performed to isolates harboring CTX-M-1 gene. Medical records were reviewed and associations were investigated. Results: Adult horses (n = 169), originating from 16 different barns, were sampled. ESBL-E shedding rate was 12% (n = 21/169, 95% CI 8-18%); 22 ESBL-E isolates were molecularly studied (one horse had two isolates). The main species was E. coli (91%) and the major ESBL gene was CTX-M-1 (54.5%). Ten different E. coli STs were identified. Sixty-four percent of total isolates were defined as multi-drug resistant. ESBL-E shedding horses originated from 8/16 different barns; whereas 48% (10/21) of them originated from one specific barn. Overall, antibiotic treatment in the previous month was found as a prevalence factor for ESBL-E shedding (p = 0.016, prevalence OR = 27.72, 95% CI 1.845-416.555). Conclusions: Our findings demonstrate the potential diverse reservoir of ESBL-E in Thoroughbred race horses. Multi-drug resistant bacteria should be further investigated to improve antibiotic treatment regimens and equine welfare.
Publication Date: 2020-12-09 PubMed ID: 33298039PubMed Central: PMC7726890DOI: 10.1186/s12917-020-02701-zGoogle 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

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.

The research was focused on studying the extent, molecular characteristics, and factors related to the shedding of antibiotic-resistant bacteria, specifically Extended Spectrum β-Lactamase-producing Enterobacteriaceae, by race horses in Ontario, Canada.

Study Design

  • The study was of cross-sectional nature, using fecal samples from 169 Thoroughbred race horses based in a large racing facility in Ontario, Canada. This study aims to provide valuable insights into the prevalence of antibiotic-resistant bacteria in commonly shared spaces like horse racing facilities.
  • The samples were run through various tests including enrichment, placement on selective plates, sub-culturing for pure cultures and confirmation of ESBL production.
  • Procedures like multilocus sequence type (MLST) and sequencing were used to specify bacterial species, analyze their antibiotic susceptibility profiles, and identify the specific E. coli sequence types and ESBL genes. Whole genome sequencing was provided for isolates carrying the CTX-M-1 gene.

Results

  • The results revealed that 12% (21 out of 169 horses) were shedding ESBL-producing Enterobacteriaceae. One of the horses had two isolates, hence 22 isolates were studied molecularly in total.
  • The majority of the bacteria were identified as E. coli (91%), with the prominent ESBL gene being CTX-M-1 (54.5%). Ten different E. coli Sequence Types were identified within the samples.
  • A considerable percentage of the isolates (64%) were defined as multi-drug resistant, underlying the potential risks and challenges these bacteria may impose on equine health and antibiotic therapy.
  • The study also examined the physical location and factors associated with these outcomes. The horses that were shedding ESBL-producing Enterobacteriaceae originated from half of the different barns studied; however, 10 out of 21 of these horses originated from one specific barn. This could be a valuable pointer towards understanding environmental and management factors facilitating such bacterial prevalence.
  • Importantly, the research found a significant link between antibiotic treatment in the month prior to the investigation and ESBL-E shedding, indicating that recent antibiotic use can be a factor in promoting the proliferation of antibiotic-resistant bacteria.

Conclusion

  • This study emphasizes the potential wide reservoir of antibiotic-resistant bacteria, especially ESBL-producing Enterobacteriaceae, within the population of race horses.
  • Further extensive studies are warranted to provide a deeper understanding of these multi-drug resistant bacteria, which would help in improving antibiotic treatment regimens, enhancing equine health and welfare, and reducing the risk of transmission of such bacteria to other animals and humans.

Cite This Article

APA
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. (2020). Extended spectrum β lactamase-producing Enterobacteriaceae shedding by race horses in Ontario, Canada. BMC Vet Res, 16(1), 479. https://doi.org/10.1186/s12917-020-02701-z

Publication

ISSN: 1746-6148
NlmUniqueID: 101249759
Country: England
Language: English
Volume: 16
Issue: 1
Pages: 479
PII: 479

Researcher Affiliations

Shnaiderman-Torban, Anat
  • The Robert H. Smith Faculty of Agriculture, Food and Environment, Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, PO Box 12, 7610001, Rehovot, Israel.
Navon-Venezia, Shiri
  • Department of Molecular Biology, Faculty of Natural Science, Ariel University, Ariel, Israel.
Paitan, Yossi
  • Sackler Faculty of Medicine, Department of Clinical Microbiology and Immunology, Tel Aviv University, Tel Aviv, Israel.
  • Clinical Microbiology Lab, Meir Medical Center, Kfar Saba, Israel.
Archer, Holly
  • Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Canada.
Abu Ahmad, Wiessam
  • Hadassah Braun School of Public Health and Community Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel.
Bonder, Darryl
  • Ontario Equine Hospital, Mississauga, Ontario, Canada.
Hanael, Erez
  • The Robert H. Smith Faculty of Agriculture, Food and Environment, Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, PO Box 12, 7610001, Rehovot, Israel.
Nissan, Israel
  • Ministry of Health, National Public Health Laboratory, Tel Aviv, Israel.
Zizelski Valenci, Gal
  • Ministry of Health, National Public Health Laboratory, Tel Aviv, Israel.
Weese, Scott J
  • Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Canada.
Steinman, Amir
  • The Robert H. Smith Faculty of Agriculture, Food and Environment, Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, PO Box 12, 7610001, Rehovot, Israel. amirst@savion.huji.ac.il.

MeSH Terms

  • Animals
  • Anti-Bacterial Agents / administration & dosage
  • Cross-Sectional Studies
  • Drug Resistance, Multiple / genetics
  • Enterobacteriaceae / genetics
  • Enterobacteriaceae / isolation & purification
  • Enterobacteriaceae Infections / epidemiology
  • Enterobacteriaceae Infections / microbiology
  • Enterobacteriaceae Infections / veterinary
  • Escherichia coli / genetics
  • Escherichia coli / isolation & purification
  • Escherichia coli Infections / epidemiology
  • Escherichia coli Infections / microbiology
  • Escherichia coli Infections / veterinary
  • Feces / microbiology
  • Female
  • Horse Diseases / epidemiology
  • Horse Diseases / microbiology
  • Horses
  • Male
  • Microbial Sensitivity Tests / veterinary
  • Multilocus Sequence Typing / veterinary
  • Ontario / epidemiology
  • Prevalence
  • beta-Lactamases / genetics

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 42 references
  1. Maddox TW, Clegg PD, Diggle PJ, Wedley AL, Dawson S, Pinchbeck GL, Williams NJ. Cross-sectional study of antimicrobial-resistant bacteria in horses. Part 1: Prevalence of antimicrobial-resistant Escherichia coli and methicillin-resistant Staphylococcus aureus.. Equine Vet J 2012 May;44(3):289-96.
  2. Maddox TW, Pinchbeck GL, Clegg PD, Wedley AL, Dawson S, Williams NJ. Cross-sectional study of antimicrobial-resistant bacteria in horses. Part 2: Risk factors for faecal carriage of antimicrobial-resistant Escherichia coli in horses.. Equine Vet J 2012 May;44(3):297-303.
  3. Lee JH, Bae IK, Lee SH. New definitions of extended-spectrum β-lactamase conferring worldwide emerging antibiotic resistance.. Med Res Rev 2012 Jan;32(1):216-32.
    doi: 10.1002/med.20210pubmed: 20577973google scholar: lookup
  4. Liu X, Thungrat K, Boothe DM. Occurrence of OXA-48 Carbapenemase and Other β-Lactamase Genes in ESBL-Producing Multidrug Resistant Escherichia coli from Dogs and Cats in the United States, 2009-2013.. Front Microbiol 2016;7:1057.
    pmc: PMC4939299pubmed: 27462301doi: 10.3389/fmicb.2016.01057google scholar: lookup
  5. Schwaber MJ, Navon-Venezia S, Kaye KS, Ben-Ami R, Schwartz D, Carmeli Y. Clinical and economic impact of bacteremia with extended- spectrum-beta-lactamase-producing Enterobacteriaceae.. Antimicrob Agents Chemother 2006 Apr;50(4):1257-62.
  6. Rubin JE, Pitout JD. Extended-spectrum β-lactamase, carbapenemase and AmpC producing Enterobacteriaceae in companion animals.. Vet Microbiol 2014 May 14;170(1-2):10-8.
    doi: 10.1016/j.vetmic.2014.01.017pubmed: 24576841google scholar: lookup
  7. Isgren CM, Edwards T, Pinchbeck GL, Winward E, Adams ER, Norton P, Timofte D, Maddox TW, Clegg PD, Williams NJ. Emergence of carriage of CTX-M-15 in faecal Escherichia coli in horses at an equine hospital in the UK; increasing prevalence over a decade (2008-2017).. BMC Vet Res 2019 Jul 29;15(1):268.
    pmc: PMC6664770pubmed: 31357996doi: 10.1186/s12917-019-2011-9google scholar: lookup
  8. Dierikx CM, van Duijkeren E, Schoormans AH, van Essen-Zandbergen A, Veldman K, Kant A, Huijsdens XW, van der Zwaluw K, Wagenaar JA, Mevius DJ. Occurrence and characteristics of extended-spectrum-β-lactamase- and AmpC-producing clinical isolates derived from companion animals and horses.. J Antimicrob Chemother 2012 Jun;67(6):1368-74.
    doi: 10.1093/jac/dks049pubmed: 22382469google scholar: lookup
  9. Walther B, Klein KS, Barton AK, Semmler T, Huber C, Wolf SA, Tedin K, Merle R, Mitrach F, Guenther S, Lübke-Becker A, Gehlen H. Extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli and Acinetobacter baumannii among horses entering a veterinary teaching hospital: The contemporary "Trojan Horse".. PLoS One 2018;13(1):e0191873.
  10. Shnaiderman-Torban A, Paitan Y, Arielly H, Kondratyeva K, Tirosh-Levy S, Abells-Sutton G, Navon-Venezia S, Steinman A. Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae in Hospitalized Neonatal Foals: Prevalence, Risk Factors for Shedding and Association with Infection.. Animals (Basel) 2019 Aug 23;9(9).
    doi: 10.3390/ani9090600pmc: PMC6770135pubmed: 31450865google scholar: lookup
  11. de la Rua-Domenech R, Reid SW, González-Zariquiey AE, Wood JL, Gettinby G. Modelling the spread of a viral infection in equine populations managed in Thoroughbred racehorse training yards.. Prev Vet Med 1999 Oct 19;47(1-2):61-77.
    doi: 10.1016/S0167-5877(00)00161-6pubmed: 11018735google scholar: lookup
  12. Weese JS, Sabino C. Scrutiny of antimicrobial use in racing horses with allergic small airway inflammatory disease.. Can Vet J 2005 May;46(5):438-9.
    pmc: PMC1090451pubmed: 16018565
  13. Kim DH, Chung YS, Park YK, Yang SJ, Lim SK, Park YH, Park KT. Antimicrobial resistance and virulence profiles of Enterococcus spp. isolated from horses in korea.. Comp Immunol Microbiol Infect Dis 2016 Oct;48:6-13.
    doi: 10.1016/j.cimid.2016.07.001pubmed: 27638114google scholar: lookup
  14. Mallardo K, Nizza S, Fiorito F, Pagnini U, De Martino L. A comparative evaluation of methicillin-resistant staphylococci isolated from harness racing-horses, breeding mares and riding-horses in Italy.. Asian Pac J Trop Biomed 2013 Mar;3(3):169-73.
  15. Chung YS, Song JW, Kim DH, Shin S, Park YK, Yang SJ, Lim SK, Park KT, Park YH. Isolation and characterization of antimicrobial-resistant Escherichia coli from national horse racetracks and private horse-riding courses in Korea.. J Vet Sci 2016 Jun 30;17(2):199-206.
    doi: 10.4142/jvs.2016.17.2.199pmc: PMC4921668pubmed: 26645344google scholar: lookup
  16. Sukmawinata E, Sato W, Mitoma S, Kanda T, Kusano K, Kambayashi Y, Sato T, Ishikawa Y, Goto Y, Uemura R, Sueyoshi M. Extended-spectrum β-lactamase-producing Escherichia coli isolated from healthy Thoroughbred racehorses in Japan.. J Equine Sci 2019 Sep;30(3):47-53.
    doi: 10.1294/jes.30.47pmc: PMC6773619pubmed: 31592106google scholar: lookup
  17. Katz MH. Multivariable analysis: a primer for readers of medical research.. Ann Intern Med 2003 Apr 15;138(8):644-50.
  18. Wolny-Koładka K, Lenart-Boroń A. Antimicrobial resistance and the presence of extended-spectrum beta-lactamase genes in Escherichia coli isolated from the environment of horse riding centers.. Environ Sci Pollut Res Int 2018 Aug;25(22):21789-21800.
    doi: 10.1007/s11356-018-2274-xpmc: PMC6063325pubmed: 29796881google scholar: lookup
  19. de Lagarde M, Larrieu C, Praud K, Schouler C, Doublet B, Sallé G, Fairbrother JM, Arsenault J. Prevalence, risk factors, and characterization of multidrug resistant and extended spectrum β-lactamase/AmpC β-lactamase producing Escherichia coli in healthy horses in France in 2015.. J Vet Intern Med 2019 Mar;33(2):902-911.
    doi: 10.1111/jvim.15415pmc: PMC6430864pubmed: 30648296google scholar: lookup
  20. Huijbers PM, de Kraker M, Graat EA, van Hoek AH, van Santen MG, de Jong MC, van Duijkeren E, de Greeff SC. Prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae in humans living in municipalities with high and low broiler density.. Clin Microbiol Infect 2013 Jun;19(6):E256-9.
    doi: 10.1111/1469-0691.12150pubmed: 23397953google scholar: lookup
  21. Sadikalay S, Reynaud Y, Guyomard-Rabenirina S, Falord M, Ducat C, Fabre L, Le Hello S, Talarmin A, Ferdinand S. High genetic diversity of extended-spectrum β-lactamases producing Escherichia coli in feces of horses.. Vet Microbiol 2018 Jun;219:117-122.
    doi: 10.1016/j.vetmic.2018.04.016pubmed: 29778183google scholar: lookup
  22. Manges AR, Harel J, Masson L, Edens TJ, Portt A, Reid-Smith RJ, Zhanel GG, Kropinski AM, Boerlin P. Multilocus sequence typing and virulence gene profiles associated with Escherichia coli from human and animal sources.. Foodborne Pathog Dis 2015 Apr;12(4):302-10.
    doi: 10.1089/fpd.2014.1860pubmed: 25774654google scholar: lookup
  23. Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, Platteel T, Fluit AC, van de Sande-Bruinsma N, Scharinga J, Bonten MJ, Mevius DJ. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains.. Clin Microbiol Infect 2011 Jun;17(6):873-80.
  24. Yamaji R, Friedman CR, Rubin J, Suh J, Thys E, McDermott P, Hung-Fan M, Riley LW. A Population-Based Surveillance Study of Shared Genotypes of Escherichia coli Isolates from Retail Meat and Suspected Cases of Urinary Tract Infections.. mSphere 2018 Aug 15;3(4).
    doi: 10.1128/mSphere.00179-18pmc: PMC6094058pubmed: 30111626google scholar: lookup
  25. Guiral E, Pons MJ, Vubil D, Marí-Almirall M, Sigaúque B, Soto SM, Alonso PL, Ruiz J, Vila J, Mandomando I. Epidemiology and molecular characterization of multidrug-resistant Escherichia coli isolates harboring bla(CTX-M) group 1 extended-spectrum β-lactamases causing bacteremia and urinary tract infection in Manhiça, Mozambique.. Infect Drug Resist 2018;11:927-936.
    doi: 10.2147/IDR.S153601pmc: PMC6037150pubmed: 30013375google scholar: lookup
  26. Kim JS, Kim J, Kim SJ, Jeon SE, Oh KH, Cho SH, Kang YH, Han SY, Chung GT. Characterization of CTX-M-type extended-spectrum beta-lactamase-producing diarrheagenic Escherichia coli isolates in the Republic of Korea during 2008-2011.. J Microbiol Biotechnol 2014 Mar 28;24(3):421-6.
    doi: 10.4014/jmb.1401.01023pubmed: 24509253google scholar: lookup
  27. Apostolakos I, Franz E, van Hoek AHAM, Florijn A, Veenman C, Sloet-van Oldruitenborgh-Oosterbaan MM, Dierikx C, van Duijkeren E. Occurrence and molecular characteristics of ESBL/AmpC-producing Escherichia coli in faecal samples from horses in an equine clinic.. J Antimicrob Chemother 2017 Jul 1;72(7):1915-1921.
    doi: 10.1093/jac/dkx072pubmed: 28333298google scholar: lookup
  28. Lupo A, Haenni M, Saras E, Gradin J, Madec JY, Börjesson S. Is bla(CTX-M-1) Riding the Same Plasmid Among Horses in Sweden and France?. Microb Drug Resist 2018 May 24;.
    doi: 10.1089/mdr.2017.0412pubmed: 29792781google scholar: lookup
  29. Livermore DM, Canton R, Gniadkowski M, Nordmann P, Rossolini GM, Arlet G, Ayala J, Coque TM, Kern-Zdanowicz I, Luzzaro F, Poirel L, Woodford N. CTX-M: changing the face of ESBLs in Europe.. J Antimicrob Chemother 2007 Feb;59(2):165-74.
    doi: 10.1093/jac/dkl483pubmed: 17158117google scholar: lookup
  30. Moodley A, Guardabassi L. Transmission of IncN plasmids carrying blaCTX-M-1 between commensal Escherichia coli in pigs and farm workers.. Antimicrob Agents Chemother 2009 Apr;53(4):1709-11.
    doi: 10.1128/AAC.01014-08pmc: PMC2663060pubmed: 19188380google scholar: lookup
  31. Belas A, Salazar AS, Gama LT, Couto N, Pomba C. Risk factors for faecal colonisation with Escherichia coli producing extended-spectrum and plasmid-mediated AmpC β-lactamases in dogs.. Vet Rec 2014 Aug 30;175(8):202.
    doi: 10.1136/vr.101978pubmed: 24943100google scholar: lookup
  32. Ben-Ami R, Rodríguez-Baño J, Arslan H, Pitout JD, Quentin C, Calbo ES, Azap OK, Arpin C, Pascual A, Livermore DM, Garau J, Carmeli Y. A multinational survey of risk factors for infection with extended-spectrum beta-lactamase-producing enterobacteriaceae in nonhospitalized patients.. Clin Infect Dis 2009 Sep 1;49(5):682-90.
    doi: 10.1086/604713pubmed: 19622043google scholar: lookup
  33. Bert F, Larroque B, Paugam-Burtz C, Dondero F, Durand F, Marcon E, Belghiti J, Moreau R, Nicolas-Chanoine MH. Pretransplant fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae and infection after liver transplant, France.. Emerg Infect Dis 2012 Jun;18(6):908-16.
    doi: 10.3201/eid1806.110139pmc: PMC3358139pubmed: 22607885google scholar: lookup
  34. Raidal SL. Antimicrobial stewardship in equine practice.. Aust Vet J 2019 Jul;97(7):238-242.
    doi: 10.1111/avj.12833pubmed: 31236925google scholar: lookup
  35. Jazmati N, Hein R, Hamprecht A. Use of an Enrichment Broth Improves Detection of Extended-Spectrum-Beta-Lactamase-Producing Enterobacteriaceae in Clinical Stool Samples.. J Clin Microbiol 2016 Feb;54(2):467-70.
    doi: 10.1128/JCM.02926-15pmc: PMC4733169pubmed: 26607984google scholar: lookup
  36. CLSI. Performance Standards for Antimicrobial Susceptibility Testing. 27th ed. CLSI supplement M100. Wayne: Clinical and Laboratory Standards Institute; 2017.
  37. Falagas ME, Karageorgopoulos DE. Pandrug resistance (PDR), extensive drug resistance (XDR), and multidrug resistance (MDR) among Gram-negative bacilli: need for international harmonization in terminology.. Clin Infect Dis 2008 Apr 1;46(7):1121-2; author reply 1122.
    doi: 10.1086/528867pubmed: 18444833google scholar: lookup
  38. Lin SP, Liu MF, Lin CF, Shi ZY. Phenotypic detection and polymerase chain reaction screening of extended-spectrum β-lactamases produced by Pseudomonas aeruginosa isolates.. J Microbiol Immunol Infect 2012 Jun;45(3):200-7.
    doi: 10.1016/j.jmii.2011.11.015pubmed: 22209695google scholar: lookup
  39. Tofteland S, Haldorsen B, Dahl KH, Simonsen GS, Steinbakk M, Walsh TR, Sundsfjord A. Effects of phenotype and genotype on methods for detection of extended-spectrum-beta-lactamase-producing clinical isolates of Escherichia coli and Klebsiella pneumoniae in Norway.. J Clin Microbiol 2007 Jan;45(1):199-205.
    doi: 10.1128/JCM.01319-06pmc: PMC1828980pubmed: 17079502google scholar: lookup
  40. Versalovic J, Koeuth T, Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes.. Nucleic Acids Res 1991 Dec 25;19(24):6823-31.
    doi: 10.1093/nar/19.24.6823pmc: PMC329316pubmed: 1762913google scholar: lookup
  41. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M. Sex and virulence in Escherichia coli: an evolutionary perspective.. Mol Microbiol 2006 Jun;60(5):1136-51.
  42. Woodford N, Fagan EJ, Ellington MJ. Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum (beta)-lactamases.. J Antimicrob Chemother 2006 Jan;57(1):154-5.
    doi: 10.1093/jac/dki412pubmed: 16284100google scholar: lookup

Citations

This article has been cited 2 times.
  1. Khalid E, Tartor YH, Ammar AM, Abdelaziz R, Mahmmod Y, Abdelkhalek A. Controlling drug-resistant bacteria in Arabian horses: bacteriophage cocktails for treating wound infections. Front Vet Sci 2025;12:1609955.
    doi: 10.3389/fvets.2025.1609955pubmed: 41169678google scholar: lookup
  2. Polo MC, Huby FD, Uehlinger FD, Rubin JE. Survey of the antimicrobial susceptibility of Escherichia coli isolated from horses admitted to the Western College of Veterinary Medicine, Saskatoon, Saskatchewan. Can Vet J 2025 Apr;66(4):435-439.
    pubmed: 40170942