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

Overview

Journal J Vet Intern Med

Specialties General Medicine
Veterinary Medicine

Date 2019 Jan 17

PMID 30648296

Citations 13

Authors

Maud De Lagarde

Caroline Larrieu

Karine Praud

Catherine Schouler

Benoit Doublet

Guillaume Salle

John M Fairbrother

Julie Arsenault

Affiliations

Soon will be listed here.

Abstract

Background: Although antimicrobial resistance is increasingly common in equine medicine, molecular and epidemiological data remains scarce.

Objectives: We estimated the prevalence of, and risk factors for, shedding of multidrug resistant (MDR), extended spectrum β-lactamase (ESBL)-producing, and AmpC β-lactamase-producing, or some combination of these in Escherichia coli in horses in France. We characterized ESBL/AmpC isolates for antimicrobial susceptibility and the presence of virulence and ESBL/AmpC-associated resistance genes.

Animals: Fecal samples from healthy adult horses at 41 premises were collected. A questionnaire was completed by each premises manager. A subset of these samples was tested to build 2 bacterial collections.

Methods: Indicator (without enrichment) and specific (enrichment with ceftriaxone) E. coli tested for antimicrobial susceptibility. Prevalence of isolates nonsusceptible to antimicrobials was estimated at the horse and the premises level. The ESBL/AmpC and virulence genes were identified by PCR. Multivariable logistic regression was used to investigate risk factors for MDR and ESBL/AmpC isolates at premises.

Results: Approximately 44% of horses shed MDR E. coli. Resistance most commonly was observed to ampicillin, streptomycin, and amoxicillin/clavulanic acid. Twenty-nine percent of premises housed horses shedding ESBL/AmpC-producing isolates. The ESBL/AmpC gene most commonly identified was bla . Virulence gene iutA was identified in 1 ESBL/AmpC-producing isolate. Medical treatment, staff numbers, and activity were identified as risk factors for housing horses shedding ESBL/AmpC-producing E. coli isolates.

Conclusions And Clinical Importance: Prevalence of healthy horses harboring ESBL/AmpC genes and MDR isolates in their intestinal microbiota is substantial. Risk factors could be used to elaborate guidelines to prevent their dissemination.

Citing Articles

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.

Eskola K, Aimo-Koivisto E, Heikinheimo A, Mykkanen A, Hautajarvi T, Gronthal T BMC Vet Res. 2024; 20(1):412.

PMID: 39272173 PMC: 11396584. DOI: 10.1186/s12917-024-04260-z.

The Effects of Antimicrobial Protocols and Other Perioperative Factors on Postoperative Complications in Horses Undergoing Celiotomy: A Retrospective Analysis, 2008-2021.

Rockow M, Griffenhagen G, Landolt G, Hendrickson D, Pezzanite L Animals (Basel). 2023; 13(22).

PMID: 38003189 PMC: 10668654. DOI: 10.3390/ani13223573.

Fecal shedding of extended-spectrum beta-lactamase-producing Enterobacterales in cats admitted to an animal shelter.

Weese J, OBrien T, Bateman S J Feline Med Surg. 2022; 24(12):1301-1304.

PMID: 35133182 PMC: 10812345. DOI: 10.1177/1098612X221075602.

Impact of Antibiotic Therapies on Resistance Genes Dynamic and Composition of the Animal Gut Microbiota.

Rochegue T, Haenni M, Mondot S, Astruc C, Cazeau G, Ferry T Animals (Basel). 2021; 11(11).

PMID: 34828011 PMC: 8614244. DOI: 10.3390/ani11113280.

Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Isolated From Specimens of Hospitalized Horses.

Kauter A, Epping L, Ghazisaeedi F, Lubke-Becker A, Wolf S, Kannapin D Front Microbiol. 2021; 12:671676.

PMID: 33936023 PMC: 8085565. DOI: 10.3389/fmicb.2021.671676.

References

Jahanbakhsh S, Letellier A, Fairbrother J . Circulating of CMY-2 β-lactamase gene in weaned pigs and their environment in a commercial farm and the effect of feed supplementation with a clay mineral. J Appl Microbiol. 2016; 121(1):136-48. DOI: 10.1111/jam.13166. View

Mataseje L, Bryce E, Roscoe D, Boyd D, Embree J, Gravel D . Carbapenem-resistant Gram-negative bacilli in Canada 2009-10: results from the Canadian Nosocomial Infection Surveillance Program (CNISP). J Antimicrob Chemother. 2012; 67(6):1359-67. DOI: 10.1093/jac/dks046. View

De Lagarde M, Larrieu C, Praud K, Schouler C, Doublet B, Salle G . 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; 33(2):902-911. PMC: 6430864. DOI: 10.1111/jvim.15415. View

Robert J, Cambau E, Grenet K, Trystram D, Pean Y, Fievet M . Trends in quinolone susceptibility of Enterobacteriaceae among inpatients of a large university hospital: 1992-98. Clin Microbiol Infect. 2001; 7(10):553-61. DOI: 10.1046/j.1198-743x.2001.00322.x. View

Martins M, Rivera I, Clark D, Stewart M, Wolfe R, Olson B . Distribution of uidA gene sequences in Escherichia coli isolates in water sources and comparison with the expression of beta-glucuronidase activity in 4-methylumbelliferyl-beta-D-glucuronide media. Appl Environ Microbiol. 1993; 59(7):2271-6. PMC: 182268. DOI: 10.1128/aem.59.7.2271-2276.1993. View

Salle G, Cortet J, Bois I, Dubes C, Guyot-Sionest Q, Larrieu C . Risk factor analysis of equine strongyle resistance to anthelmintics. Int J Parasitol Drugs Drug Resist. 2017; 7(3):407-415. PMC: 5727347. DOI: 10.1016/j.ijpddr.2017.10.007. View

Agerso Y, Aarestrup F, Pedersen K, Seyfarth A, Struve T, Hasman H . Prevalence of extended-spectrum cephalosporinase (ESC)-producing Escherichia coli in Danish slaughter pigs and retail meat identified by selective enrichment and association with cephalosporin usage. J Antimicrob Chemother. 2011; 67(3):582-8. DOI: 10.1093/jac/dkr507. View

DebRoy C, Roberts E, Jayarao B, Brooks J . Bronchopneumonia associated with extraintestinal pathogenic Escherichia coli in a horse. J Vet Diagn Invest. 2008; 20(5):661-4. DOI: 10.1177/104063870802000524. View

Huijbers P, De Kraker M, Graat E, van Hoek A, Van Santen M, de Jong M . Prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae in humans living in municipalities with high and low broiler density. Clin Microbiol Infect. 2013; 19(6):E256-9. DOI: 10.1111/1469-0691.12150. View

10.

Carattoli A . Plasmids in Gram negatives: molecular typing of resistance plasmids. Int J Med Microbiol. 2011; 301(8):654-8. DOI: 10.1016/j.ijmm.2011.09.003. View

11.

Jahanbakhsh S, Kabore K, Fravalo P, Letellier A, Fairbrother J . Impact of medicated feed along with clay mineral supplementation on Escherichia coli resistance to antimicrobial agents in pigs after weaning in field conditions. Res Vet Sci. 2015; 102:72-9. DOI: 10.1016/j.rvsc.2015.07.014. View

12.

Adams R, Kim S, Mollenkopf D, Mathys D, Schuenemann G, Daniels J . Antimicrobial-resistant Enterobacteriaceae recovered from companion animal and livestock environments. Zoonoses Public Health. 2018; 65(5):519-527. DOI: 10.1111/zph.12462. View

13.

Hammerum A, Larsen J, Andersen V, Lester C, Skovgaard Skytte T, Hansen F . Characterization of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli obtained from Danish pigs, pig farmers and their families from farms with high or no consumption of third- or fourth-generation cephalosporins. J Antimicrob Chemother. 2014; 69(10):2650-7. DOI: 10.1093/jac/dku180. View

14.

Andersson D, Hughes D . Antibiotic resistance and its cost: is it possible to reverse resistance?. Nat Rev Microbiol. 2010; 8(4):260-71. DOI: 10.1038/nrmicro2319. View

15.

Dolejska M, Duskova E, Rybarikova J, Janoszowska D, Roubalova E, Dibdakova K . Plasmids carrying blaCTX-M-1 and qnr genes in Escherichia coli isolates from an equine clinic and a horseback riding centre. J Antimicrob Chemother. 2011; 66(4):757-64. DOI: 10.1093/jac/dkq500. View

16.

Rubin J, Pitout J . Extended-spectrum β-lactamase, carbapenemase and AmpC producing Enterobacteriaceae in companion animals. Vet Microbiol. 2014; 170(1-2):10-8. DOI: 10.1016/j.vetmic.2014.01.017. View

17.

Damborg P, Marskar P, Baptiste K, Guardabassi L . Faecal shedding of CTX-M-producing Escherichia coli in horses receiving broad-spectrum antimicrobial prophylaxis after hospital admission. Vet Microbiol. 2011; 154(3-4):298-304. DOI: 10.1016/j.vetmic.2011.07.005. View

18.

Ewers C, Bethe A, Semmler T, Guenther S, Wieler L . Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin Microbiol Infect. 2012; 18(7):646-55. DOI: 10.1111/j.1469-0691.2012.03850.x. View

19.

Maddox T, Clegg P, Diggle P, Wedley A, Dawson S, Pinchbeck G . 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. 2011; 44(3):289-96. DOI: 10.1111/j.2042-3306.2011.00441.x. View

20.

Maddox T, Pinchbeck G, Clegg P, Wedley A, Dawson S, Williams N . 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. 2011; 44(3):297-303. DOI: 10.1111/j.2042-3306.2011.00440.x. View