Extended-Spectrum β-lactamase-Producing Enterobacteriaceae Shedding in Farm Horses Versus Hospitalized Horses: Prevalence and Risk Factors.
Abstract: We aimed to investigate the prevalence, molecular characteristics and risk factors of extended-spectrum β-lactamase (ESBL)-producing (ESBL-E) shedding in horses. A prospective study included three cohorts: (i) farm horses (13 farms, n = 192); (ii) on hospital admission (n = 168) and; (iii) horses hospitalized for ≥72 h re-sampled from cohort (ii) (n = 86). Enriched rectal swabs were plated, ESBL-production was confirmed (Clinical and Laboratory Standards Institute (CLSI)) and genes were identified (polymerase chain reaction (PCR)). Identification and antibiotic susceptibility were determined (Vitek-2). Medical records and owners' questionnaires were analyzed. Shedding rates increased from 19.6% (n = 33/168) on admission to 77.9% (n = 67/86) during hospitalization ( < 0.0001, odds ratio (OR) = 12.12). Shedding rate in farms was 20.8% (n = 40/192), significantly lower compared to hospitalized horses ( < 0.0001). The main ESBL-E species (n = 192 isolates) were (59.9%, 115/192), sp. (17.7%, 34/192) and (13.0%, 25/192). The main gene group was CTX-M-1 (56.8%). A significant increase in resistance rates to chloramphenicol, enrofloxacin, gentamicin, nitrofurantoin, and trimethoprim-sulpha was identified during hospitalization. Risk factors for shedding in farms included breed (Arabian, OR = 3.9), sex (stallion, OR = 3.4), and antibiotic treatment (OR = 9.8). Older age was identified as a protective factor (OR = 0.88). We demonstrated an ESBL-E reservoir in equine cohorts, with a significant ESBL-E acquisition, which increases the necessity to implement active surveillance and antibiotic stewardship programs.
Publication Date: 2020-02-11 PubMed ID: 32054111PubMed Central: PMC7070874DOI: 10.3390/ani10020282Google 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.
This research focuses on the prevalence, characteristics, and risk factors of a bacteria (extended-spectrum β-lactamase-producing Enterobacteriaceae or ESBL-E) present in horses, showing a substantial increase in this bacteria in horses during hospitalization compared to horses on farms, and highlights some contributing factors.
Research Methodology
- The study used a prospective design, involving three different groups of horses: farm horses (from 13 different farms, total 192 horses), horses upon hospital admission (168 horses), and horses who had been hospitalized for at least 72 hours, re-sampled from the previous cohort (86 horses).
- To test for the bacteria, rectal swabs from the horses were enriched and plated. ESBL-production was confirmed using standards from the Clinical and Laboratory Standards Institute. The specific genes involved were identified using polymerase chain reaction (PCR), a widely-used method for making multiple copies of a specific segment of DNA.
- The researchers determined the type of bacteria and their susceptibility to antibiotics using an automated microbial system called Vitek-2.
- Medical records from each horse, as well as questionnaires completed by their owners, were also analyzed as part of the data collection process.
Key Findings
- The study found a significant increase in the rates of ESBL-E shedding from point of admission (19.6%) to during hospitalization at 72 hours or more (77.9%), indicating that prolonged hospital stays may be associated with an increased risk of bacterial shedding.
- The rate of shedding in farm horses was found to be 20.8%, which was significantly lower than in hospitalized horses.
- Of the 192 bacterial isolates identified, the majority were Escherichia coli (59.9%), followed by Klebsiella species (17.7%), and Proteus (13.0%).
- The study identified the main gene group responsible as CTX-M-1 (56.8%), which is a major type of ESBL gene group.
- Bacteria’s resistance rates to various antibiotics (chloramphenicol, enrofloxacin, gentamicin, nitrofurantoin, and trimethoprim-sulpha) were shown to increase significantly during hospitalization.
Risk Factors and Protective Measures
- In terms of risk factors, certain breeds (Arabian), sex (stallions), and antibiotic treatment were found to be associated with higher rates of shedding in farm horses.
- Older age was identified as a protective factor, with its odds ratio suggesting that for each year increase in age, the risk of ESBL-E shedding decreased by around 12%.
- The study concludes by signalling the importance of active surveillance and antibiotic stewardship programs in managing the risk and spread of ESBL-E shedding in equine cohorts.
Cite This Article
APA
Shnaiderman-Torban A, Navon-Venezia S, Dor Z, Paitan Y, Arielly H, Ahmad WA, Kelmer G, Fulde M, Steinman A.
(2020).
Extended-Spectrum β-lactamase-Producing Enterobacteriaceae Shedding in Farm Horses Versus Hospitalized Horses: Prevalence and Risk Factors.
Animals (Basel), 10(2), 282.
https://doi.org/10.3390/ani10020282 Publication
Researcher Affiliations
- Koret School of Veterinary Medicine (KSVM), The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7610001, Israel.
- Department of Molecular Biology, Faculty of Natural Sciences, Ariel University, Ariel 40700, Israel.
- The Miriam and Sheldon Adelson School of Medicine, Ariel University, Ariel 40700, Israel.
- Department of Molecular Biology, Faculty of Natural Sciences, Ariel University, Ariel 40700, Israel.
- Department of Clinical Microbiology and Immunology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 6997801, Israel.
- Clinical Microbiology Lab, Meir Medical Center, Kfar Saba 4428164, Israel.
- Clinical Microbiology Lab, Meir Medical Center, Kfar Saba 4428164, Israel.
- Braun School of Public Health and Community Medicine, Hebrew University, Jerusalem 9112102, Israel.
- Koret School of Veterinary Medicine (KSVM), The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7610001, Israel.
- Institute of Microbiology and Epizootics, Department of Veterinary Medicine at the Freie Universität Berlin, Berlin 14163, Germany.
- Koret School of Veterinary Medicine (KSVM), The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7610001, Israel.
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 41 references
- Vo AT, van Duijkeren E, Fluit AC, Gaastra W. Characteristics of extended-spectrum cephalosporin-resistant Escherichia coli and Klebsiella pneumoniae isolates from horses.. Vet Microbiol 2007 Oct 6;124(3-4):248-55.
- Paterson DL, Bonomo RA. Extended-spectrum beta-lactamases: a clinical update.. Clin Microbiol Rev 2005 Oct;18(4):657-86.
- Denkel LA, Schwab F, Kola A, Leistner R, Garten L, von Weizsäcker K, Geffers C, Gastmeier P, Piening B. The mother as most important risk factor for colonization of very low birth weight (VLBW) infants with extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-E).. J Antimicrob Chemother 2014 Aug;69(8):2230-7.
- 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.
- Ewers C, Stamm I, Pfeifer Y, Wieler LH, Kopp PA, Schønning K, Prenger-Berninghoff E, Scheufen S, Stolle I, Günther S, Bethe A. Clonal spread of highly successful ST15-CTX-M-15 Klebsiella pneumoniae in companion animals and horses.. J Antimicrob Chemother 2014 Oct;69(10):2676-80.
- Ewers C, Bethe A, Stamm I, Grobbel M, Kopp PA, Guerra B, Stubbe M, Doi Y, Zong Z, Kola A, Schaufler K, Semmler T, Fruth A, Wieler LH, Guenther S. CTX-M-15-D-ST648 Escherichia coli from companion animals and horses: another pandemic clone combining multiresistance and extraintestinal virulence?. J Antimicrob Chemother 2014 May;69(5):1224-30.
- Shnaiderman-Torban A, Navon-Venezia S, Dahan R, Dor Z, Taulescu M, Paitan Y, Edery N, Steinman A. CTX-M-15 Producing Escherichia coli Sequence Type 361 and Sequence Type 38 Causing Bacteremia and Umbilical Infection in a Neonate Foal.. J Equine Vet Sci 2020 Feb;85:102881.
- 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).
- Johns I, Verheyen K, Good L, Rycroft A. Antimicrobial resistance in faecal Escherichia coli isolates from horses treated with antimicrobials: a longitudinal study in hospitalised and non-hospitalised horses.. Vet Microbiol 2012 Oct 12;159(3-4):381-9.
- Dolejska M, Duskova E, Rybarikova J, Janoszowska D, Roubalova E, Dibdakova K, Maceckova G, Kohoutova L, Literak I, Smola J, Cizek A. 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 Apr;66(4):757-64.
- 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.
- Kaspar U, von Lützau K, Schlattmann A, Rösler U, Köck R, Becker K. Zoonotic multidrug-resistant microorganisms among non-hospitalized horses from Germany.. One Health 2019 Jun;7:100091.
- 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.
- 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.
- Murk JL, Heddema ER, Hess DL, Bogaards JA, Vandenbroucke-Grauls CM, Debets-Ossenkopp YJ. Enrichment broth improved detection of extended-spectrum-beta-lactamase-producing bacteria in throat and rectal surveillance cultures of samples from patients in intensive care units.. J Clin Microbiol 2009 Jun;47(6):1885-7.
- Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. Clinical and Laboratory Standards Institute 26th ed.; Wayne, PA, USA: 2016.
- 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.
- 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.
- 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.
- 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.
- Johnson JR, Clermont O, Johnston B, Clabots C, Tchesnokova V, Sokurenko E, Junka AF, Maczynska B, Denamur E. Rapid and specific detection, molecular epidemiology, and experimental virulence of the O16 subgroup within Escherichia coli sequence type 131.. J Clin Microbiol 2014 May;52(5):1358-65.
- Ahmed MO, Clegg PD, Williams NJ, Baptiste KE, Bennett M. Antimicrobial resistance in equine faecal Escherichia coli isolates from North West England.. Ann Clin Microbiol Antimicrob 2010 Apr 7;9:12.
- Bilavsky E, Temkin E, Lerman Y, Rabinovich A, Salomon J, Lawrence C, Rossini A, Salvia A, Samso JV, Fierro J, Paul M, Hart J, Gniadkowski M, Hochman M, Kazma M, Klein A, Adler A, Schwaber MJ, Carmeli Y. Risk factors for colonization with extended-spectrum beta-lactamase-producing enterobacteriaceae on admission to rehabilitation centres.. Clin Microbiol Infect 2014 Nov;20(11):O804-10.
- Shitrit P, Reisfeld S, Paitan Y, Gottesman BS, Katzir M, Paul M, Chowers M. Extended-spectrum beta-lactamase-producing Enterobacteriaceae carriage upon hospital admission: prevalence and risk factors.. J Hosp Infect 2013 Nov;85(3):230-2.
- Ewers C, Grobbel M, Stamm I, Kopp PA, Diehl I, Semmler T, Fruth A, Beutlich J, Guerra B, Wieler LH, Guenther S. Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-beta-lactamase-producing Escherichia coli among companion animals.. J Antimicrob Chemother 2010 Apr;65(4):651-60.
- 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.
- Maddox TW, Williams NJ, Clegg PD, O'Donnell AJ, Dawson S, Pinchbeck GL. Longitudinal study of antimicrobial-resistant commensal Escherichia coli in the faeces of horses in an equine hospital.. Prev Vet Med 2011 Jun 15;100(2):134-45.
- European Medicines Agency [(accessed on 15 January 2015)]; Available online: https://www.ema.europa.eu/en/documents/scientific-guideline/reflection-paper-risk-antimicrobial-resistance-transfer-companion-animals_en.pdf.
- Dunkel B, Johns IC. Antimicrobial use in critically ill horses.. J Vet Emerg Crit Care (San Antonio) 2015 Jan-Feb;25(1):89-100.
- Norris JM, Zhuo A, Govendir M, Rowbotham SJ, Labbate M, Degeling C, Gilbert GL, Dominey-Howes D, Ward MP. Factors influencing the behaviour and perceptions of Australian veterinarians towards antibiotic use and antimicrobial resistance.. PLoS One 2019;14(10):e0223534.
- Van Spijk JN, Schmitt S, Schoster A. Infections caused by multidrug-resistant bacteria in an equine hospital (2012–2015). Equine Vet. Educ. 2019;31:653–658.
- Johns IC, Adams EL. Trends in antimicrobial resistance in equine bacterial isolates: 1999-2012.. Vet Rec 2015 Mar 28;176(13):334.
- Colodner R, Rock W, Chazan B, Keller N, Guy N, Sakran W, Raz R. Risk factors for the development of extended-spectrum beta-lactamase-producing bacteria in nonhospitalized patients.. Eur J Clin Microbiol Infect Dis 2004 Mar;23(3):163-7.
- Vázquez-Martínez ER, García-Gómez E, Camacho-Arroyo I, González-Pedrajo B. Sexual dimorphism in bacterial infections.. Biol Sex Differ 2018 Jun 20;9(1):27.
- Adler A, Sturlesi N, Fallach N, Zilberman-Barzilai D, Hussein O, Blum SE, Klement E, Schwaber MJ, Carmeli Y. Prevalence, Risk Factors, and Transmission Dynamics of Extended-Spectrum-β-Lactamase-Producing Enterobacteriaceae: a National Survey of Cattle Farms in Israel in 2013.. J Clin Microbiol 2015 Nov;53(11):3515-21.
- McGowan C. Welfare of Aged Horses.. Animals (Basel) 2011 Oct 31;1(4):366-76.
- Monroe M, Whitworth JD, Wharton T, Turner J. Effects of an Equine-Assisted Therapy Program for Military Veterans with Self-Reported PTSD. Soc. Amp Anim. 2019;1:1–14.
- Borgi M, Loliva D, Cerino S, Chiarotti F, Venerosi A, Bramini M, Nonnis E, Marcelli M, Vinti C, De Santis C, Bisacco F, Fagerlie M, Frascarelli M, Cirulli F. Effectiveness of a Standardized Equine-Assisted Therapy Program for Children with Autism Spectrum Disorder.. J Autism Dev Disord 2016 Jan;46(1):1-9.
- White-Lewis S, Johnson R, Ye S, Russell C. An equine-assisted therapy intervention to improve pain, range of motion, and quality of life in adults and older adults with arthritis: A randomized controlled trial.. Appl Nurs Res 2019 Oct;49:5-12.
- Linder DE, Mueller MK, Gibbs DM, Siebens HC, Freeman LM. The Role of Veterinary Education in Safety Policies for Animal-Assisted Therapy and Activities in Hospitals and Nursing Homes.. J Vet Med Educ 2017 Summer;44(2):229-233.
- Royden A, Ormandy E, Pinchbeck G, Pascoe B, Hitchings MD, Sheppard SK, Williams NJ. Prevalence of faecal carriage of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli in veterinary hospital staff and students.. Vet Rec Open 2019;6(1):e000307.
Citations
This article has been cited 8 times.- Pimenta J, Pinto AR, Saavedra MJ, Cotovio M. Equine Gram-Negative Oral Microbiota: An Antimicrobial Resistances Watcher?. Antibiotics (Basel) 2023 Apr 21;12(4).
- Shnaiderman-Torban A, Navon-Venezia S, Baron H, Abu-Ahmad W, Arielly H, Zizelski Valenci G, Nissan I, Paitan Y, Steinman A. Prevalence and Molecular Characterization of Extended-Spectrum β-Lactamase Producing Enterobacterales in Healthy Community Dogs in Israel.. Antibiotics (Basel) 2022 Aug 7;11(8).
- 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.
- Kauter A, Epping L, Ghazisaeedi F, Lübke-Becker A, Wolf SA, Kannapin D, Stoeckle SD, Semmler T, Günther S, Gehlen H, Walther B. Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses.. Front Microbiol 2021;12:671676.
- 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).
- Dor Z, Shnaiderman-Torban A, Kondratyeva K, Davidovich-Cohen M, Rokney A, Steinman A, Navon-Venezia S. Emergence and Spread of Different ESBL-Producing Salmonella enterica Serovars in Hospitalized Horses Sharing a Highly Transferable IncM2 CTX-M-3-Encoding Plasmid.. Front Microbiol 2020;11:616032.
- Shnaiderman-Torban A, Navon-Venezia S, Kelmer E, Cohen A, Paitan Y, Arielly H, Steinman A. Extended-Spectrum β-Lactamase-Producing Enterobacterales Shedding by Dogs and Cats Hospitalized in an Emergency and Critical Care Department of a Veterinary Teaching Hospital.. Antibiotics (Basel) 2020 Aug 27;9(9).
- Steinman A, Navon-Venezia S. Antimicrobial Resistance in Horses.. Animals (Basel) 2020 Jul 9;10(7).
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists