Antimicrobial Resistance in Horses

A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Equids".

Deadline for manuscript submissions: closed (31 January 2020) | Viewed by 24650

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Koret School of Veterinary Medicine, the Hebrew University of Jerusalem, Rehovot 7610001, Israel
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Guest Editor
Molecular Biology Department, The Adelson School of Medicine, Ariel University, Ariel 40700, Israel
Interests: bacterial resistance and pathogenesis; molecular mechanisms of antibiotic resistance; novel antibacterial drug

Special Issue Information

Dear Colleagues,

Antimicrobial resistance (AMR) is a global problem with extremely complex epidemiology involving the direct and indirect transmission of antibiotic resistant pathogens and mobile genetic elements between humans, animals and the environment, and is therefore being recognized as a One Health concern. Data describing AMR prevalence and trends is required in order to enable the judicious and prudent use of antimicrobials in animals, which has implications both from the veterinary and animal welfare aspects, as well as from a zoonotic and public health perspective.   

Horses are one of the potential reservoirs of AMR that can be shared with humans, as was observed previously in several methicillin-resistant Staphylococcus aureus (MRSA) outbreaks in equine hospitals. Extended-spectrum beta-lactamases producing Enterobacteriaceae (ESBL-E), considered as the most clinically and economically important AMR burden in human and veterinary medicine, has been reported in both community and clinic equine populations. ESBL-E poses a major worldwide threat due to the geographical expansion of ESBL-producing clones, and the horizontal inter-species bacterial dissemination of ESBL-encoding plasmids and genes. In human medicine, ESBL-E infection is associated with increased morbidity, mortality, length of hospital stay, delay of targeted appropriate treatment and higher costs. These issues have not yet been demonstrated in horses.

We hereby invite authors to submit original high quality papers that provide a significant contribution to the understanding of AMR in horses. Topics of special interest are those describing the proper use of antibiotics for therapeutics and prophylaxis; the prevalence of multidrug resistant bacteria in different cohorts of horses and their effect on animal health and welfare; the emergence and dissemination of AMR patterns in various bacterial pathogens in different geographical areas and over time, as well as the associated risks.

Dr. Amir Steinman
Prof. Shiri Navon-Venezia
Guest Editors

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Keywords

  • horse
  • equine
  • antibiotic resistance
  • one health
  • multidrug resistance
  • zoonosis
  • risk factors
  • colonization
  • environmental shedding

Published Papers (9 papers)

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Editorial

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3 pages, 174 KiB  
Editorial
Antimicrobial Resistance in Horses
by Amir Steinman and Shiri Navon-Venezia
Animals 2020, 10(7), 1161; https://doi.org/10.3390/ani10071161 - 09 Jul 2020
Cited by 4 | Viewed by 1944
Abstract
Antimicrobial resistance (AMR) is an increasingly recognized global public health threat to the modern health-care system that could hamper the control and treatment of infectious diseases [...] Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Horses)

Research

Jump to: Editorial

11 pages, 658 KiB  
Article
Evolution of In Vitro Antimicrobial Susceptibility of Equine Clinical Isolates in France between 2016 and 2019
by Albertine Léon, Sophie Castagnet, Karine Maillard, Romain Paillot and Jean-Christophe Giard
Animals 2020, 10(5), 812; https://doi.org/10.3390/ani10050812 - 07 May 2020
Cited by 15 | Viewed by 2822
Abstract
The present study described the evolution of antimicrobial resistance in equine pathogens isolated from 2016 to 2019. A collection of 7806 bacterial isolates were analysed for their in vitro antimicrobial susceptibility using the disk diffusion method. The most frequently isolated pathogens were group [...] Read more.
The present study described the evolution of antimicrobial resistance in equine pathogens isolated from 2016 to 2019. A collection of 7806 bacterial isolates were analysed for their in vitro antimicrobial susceptibility using the disk diffusion method. The most frequently isolated pathogens were group C Streptococci (27.0%), Escherichia coli (18.0%), Staphylococcus aureus (6.2%), Pseudomonas aeruginosa (3.4%), Klebsiella pneumoniae (2.3%) and Enterobacter spp. (2.1%). The majority of these pathogens were isolated from the genital tract (45.1%, n = 3522). With the implementation of two French national plans (named ECOANTIBIO 1 and 2) in 2012–2016 and 2017–2021, respectively, and a reduction in animal exposure to veterinary antibiotics, our study showed decreases in the resistance of group C Streptococci, Klebsiella pneumoniae and Escherichia coli against five classes, four classes and one class of antimicrobials tested, respectively. However, Staphylococcus aureus, Escherichia coli and Enterobacter spp. presented an increased resistance against all the tested classes, excepted for two fifths of E. coli. Moreover, the percentages of multi-drug resistant strains of Staphylococcus aureus and Enterobacter spp. also increased from 24.5% to 37.4% and from 26.3% to 51.7%, respectively. The data reported here are relevant to equine practitioners and will help to improve knowledge related to antimicrobial resistance in common equine pathogens. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Horses)
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14 pages, 1392 KiB  
Article
Prevalence, Risk Factors, and Characterization of Multidrug Resistant and ESBL/AmpC Producing Escherichia coli in Healthy Horses in Quebec, Canada, in 2015–2016
by Maud de Lagarde, John M. Fairbrother and Julie Arsenault
Animals 2020, 10(3), 523; https://doi.org/10.3390/ani10030523 - 20 Mar 2020
Cited by 6 | Viewed by 2412
Abstract
Although antimicrobial resistance is an increasing threat in equine medicine, molecular and epidemiological data remain limited in North America. We assessed the prevalence of, and risk factors for, shedding multidrug-resistant (MDR) and extended-spectrum β-lactamase (ESBL) and/or AmpC β-lactamase-producing E. coli in healthy horses [...] Read more.
Although antimicrobial resistance is an increasing threat in equine medicine, molecular and epidemiological data remain limited in North America. We assessed the prevalence of, and risk factors for, shedding multidrug-resistant (MDR) and extended-spectrum β-lactamase (ESBL) and/or AmpC β-lactamase-producing E. coli in healthy horses in Quebec, Canada. We collected fecal samples in 225 healthy adult horses from 32 premises. A questionnaire on facility management and horse medical history was completed for each horse. Indicator (without enrichment) and specific (following enrichment with ceftriaxone) E. coli were isolated and tested for antimicrobial susceptibility. The presence of ESBL/AmpC genes was determined by PCR. The prevalence of isolates that were non-susceptible to antimicrobials and to antimicrobial classes were estimated at the horse and the premises level. Multivariable logistic regression was used to assess potential risk factors for MDR and ESBL/AmpC isolates. The shedding of MDR E. coli was detected in 46.3% of horses. Non-susceptibility was most commonly observed to ampicillin, amoxicillin/clavulanic acid or streptomycin. ESBL/AmpC producing isolates were detected in 7.3% of horses. The most commonly identified ESBL/AmpC gene was blaCTX-M-1, although we also identified blaCMY-2. The number of staff and equestrian event participation were identified as risk factors for shedding MDR isolates. The prevalence of healthy horses harboring MDR or ESBL/AmpC genes isolates in their intestinal microbiota is noteworthy. We identified risk factors which could help to develop guidelines to preclude their spread. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Horses)
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9 pages, 657 KiB  
Article
Multidrug-Resistant ESBL/AmpC-Producing Klebsiella pneumoniae Isolated from Healthy Thoroughbred Racehorses in Japan
by Eddy Sukmawinata, Ryoko Uemura, Wataru Sato, Myo Thu Htun and Masuo Sueyoshi
Animals 2020, 10(3), 369; https://doi.org/10.3390/ani10030369 - 25 Feb 2020
Cited by 11 | Viewed by 3644
Abstract
Extended-spectrum β-lactamase (ESBL)- and AmpC β-lactamase (AmpC)-producing Klebsiella spp. have become a major health problem, leading to treatment failure in humans and animals. This study aimed to evaluate the presence of ESBL/AmpC-producing Klebsiella spp. isolated from racehorses in Japan. Feces samples from 212 [...] Read more.
Extended-spectrum β-lactamase (ESBL)- and AmpC β-lactamase (AmpC)-producing Klebsiella spp. have become a major health problem, leading to treatment failure in humans and animals. This study aimed to evaluate the presence of ESBL/AmpC-producing Klebsiella spp. isolated from racehorses in Japan. Feces samples from 212 healthy Thoroughbred racehorses were collected from the Japan Racing Association Training Centers between March 2017 and August 2018. ESBL/AmpC-producing Klebsiella spp. were isolated using selective medium containing 1 µg/mL cefotaxime. All isolates were subjected to bacterial species identification (MALDI-TOF MS), antimicrobial susceptibility test (disk diffusion test), characterization of resistance genes (PCR), conjugation assay, and genetic relatedness (multilocus sequence typing/MLST). Twelve ESBL/AmpC-producing Klebsiella pneumoniae (ESBL/AmpC-KP) were isolated from 3.3% of horse samples. Antimicrobial resistance profiling for 17 antimicrobials showed all ESBL/AmpC-KP were multidrug-resistant (MDR). Only 1 isolate was confirmed as an ESBL producer (blaCTX-M-2-positive), whereas the other 11 isolates were plasmid-mediated AmpC (pAmpC) producers (blaCMY positive). On the basis of MLST analysis, the ESBL-KP isolate was identified as sequence type (ST)-133 and four different STs among AmpC-KP isolates, ST-145, ST-4830, ST-4831, and ST-4832, were found to share six of the seven loci constituting a single-locus variant. This is the first study to show K. pneumoniae carrying MDR pAmpC isolated from a racehorse. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Horses)
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10 pages, 238 KiB  
Article
Broad-Spectrum Cephalosporin-Resistant Klebsiella spp. Isolated from Diseased Horses in Austria
by Igor Loncaric, Adriana Cabal Rosel, Michael P. Szostak, Theresia Licka, Franz Allerberger, Werner Ruppitsch and Joachim Spergser
Animals 2020, 10(2), 332; https://doi.org/10.3390/ani10020332 - 20 Feb 2020
Cited by 16 | Viewed by 2814
Abstract
The aim of the present study was to investigate the diversity of broad-spectrum cephalosporin-resistant Klebsiella spp. isolated from horses in Austria that originated from diseased horses. A total of seven non-repetitive cefotaxime-resistant Klebsiella sp. isolates were obtained during diagnostic activities from autumn 2012 [...] Read more.
The aim of the present study was to investigate the diversity of broad-spectrum cephalosporin-resistant Klebsiella spp. isolated from horses in Austria that originated from diseased horses. A total of seven non-repetitive cefotaxime-resistant Klebsiella sp. isolates were obtained during diagnostic activities from autumn 2012 to October 2019. Antimicrobial susceptibility testing was performed. The isolates were genotyped by whole-genome sequencing (WGS). Four out of seven Klebsiella isolates were identified as K. pneumoniae, two as K. michiganensis and one as K. oxytoca. All isolates displayed a multi-drug resistant phenotype. The detection of resistance genes reflected well the phenotypic resistance profiles of the respective isolates. All but one isolate displayed the extended-spectrum β-lactamases (ESBL) phenotype and carried CTX-M cefotaximases, whereas one isolate displayed an ESBL and AmpC phenotype and carried cephamycinase (CMY)-2 and sulfhydryl variable (SHV)-type b and Temoniera (TEM) β-lactamases. Among Klebsiella pneumoniae isolates, for different sequence types (ST) could be detected (ST147, ST307, ST1228, and a new ST4848). Besides resistance genes, a variety of virulence genes, including genes coding for yersiniabactin were detected. Considering the high proximity between horses and humans, our results undoubtedly identified a public health issue. This deserves to be also monitored in the years to come. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Horses)
23 pages, 770 KiB  
Article
Extended-Spectrum β-lactamase-Producing Enterobacteriaceae Shedding in Farm Horses Versus Hospitalized Horses: Prevalence and Risk Factors
by Anat Shnaiderman-Torban, Shiri Navon-Venezia, Ziv Dor, Yossi Paitan, Haia Arielly, Wiessam Abu Ahmad, Gal Kelmer, Marcus Fulde and Amir Steinman
Animals 2020, 10(2), 282; https://doi.org/10.3390/ani10020282 - 11 Feb 2020
Cited by 10 | Viewed by 2631
Abstract
We aimed to investigate the prevalence, molecular characteristics and risk factors of extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae (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) [...] Read more.
We aimed to investigate the prevalence, molecular characteristics and risk factors of extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae (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 (p < 0.0001, odds ratio (OR) = 12.12). Shedding rate in farms was 20.8% (n = 40/192), significantly lower compared to hospitalized horses (p < 0.0001). The main ESBL-E species (n = 192 isolates) were E. coli (59.9%, 115/192), Enterobacter sp. (17.7%, 34/192) and Klebsiella pneumoniae (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. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Horses)
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14 pages, 308 KiB  
Article
The Occurrence and Characterization of Extended-Spectrum-Beta-Lactamase-Producing Escherichia coli Isolated from Clinical Diagnostic Specimens of Equine Origin
by Leta Elias, David C. Gillis, Tanya Gurrola-Rodriguez, Jeong Ho Jeon, Jung Hun Lee, Tae Yeong Kim, Sang Hee Lee, Sarah A. Murray, Naomi Ohta, Harvey Morgan Scott, Jing Wu and Artem S. Rogovskyy
Animals 2020, 10(1), 28; https://doi.org/10.3390/ani10010028 - 21 Dec 2019
Cited by 7 | Viewed by 2774
Abstract
Escherichia coli isolates were recovered from clinical specimens of equine patients admitted to the Texas A&M Veterinary Medical Teaching Hospital over a five-year period. Ceftiofur resistance was used as a marker for potential extended-spectrum beta-lactamase (ESBL)-activity, and of the 48 ceftiofur-resistant E. coli [...] Read more.
Escherichia coli isolates were recovered from clinical specimens of equine patients admitted to the Texas A&M Veterinary Medical Teaching Hospital over a five-year period. Ceftiofur resistance was used as a marker for potential extended-spectrum beta-lactamase (ESBL)-activity, and of the 48 ceftiofur-resistant E. coli isolates, 27.08% (n = 13) were phenotypically ESBL-positive. Conventional PCR analysis followed by the large-scalebla Finder multiplex PCR detected the ESBL genes, CTX-M-1 and SHV, in seven out of the 13 isolates. Moreover, beta-lactamase genes of TEM-1-type, BER-type (AmpC), and OXA-type were also identified. Sequencing of these genes resulted in identification of a novel TEM-1-type gene, called blaTEM-233, and a study is currently underway to determine if this gene confers the ESBL phenotype. Furthermore, this report is the first to have found E. coli ST1308 in horses. This subtype, which has been reported in other herbivores, harbored the SHV-type ESBL gene. Finally, one out of 13 E. coli isolates was PCR-positive for the carbapenemase gene, blaIMP-1 despite the lack of phenotypically proven resistance to imipenem. With the identification of novel ESBL gene variant and the demonstrated expansion of E. coli sequence types in equine patients, this study underscores the need for more investigation of equines as reservoirs for ESBL-producing pathogens. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Horses)
12 pages, 263 KiB  
Article
Antimicrobial Resistance, Virulence, and Genetic Lineages of Staphylococci from Horses Destined for Human Consumption: High Detection of S. aureus Isolates of Lineage ST1640 and Those Carrying the lukPQ Gene
by Olouwafemi Mistourath Mama, Paula Gómez, Laura Ruiz-Ripa, Elena Gómez-Sanz, Myriam Zarazaga and Carmen Torres
Animals 2019, 9(11), 900; https://doi.org/10.3390/ani9110900 - 01 Nov 2019
Cited by 17 | Viewed by 2515
Abstract
This work aimed to determine the frequency and diversity of Staphylococcus species carriage in horses intended for human consumption, as well as their resistance and virulence determinants. Eighty samples (30 nasal; 50 faecal) were recovered from 73 healthy horses in a Spanish slaughterhouse. [...] Read more.
This work aimed to determine the frequency and diversity of Staphylococcus species carriage in horses intended for human consumption, as well as their resistance and virulence determinants. Eighty samples (30 nasal; 50 faecal) were recovered from 73 healthy horses in a Spanish slaughterhouse. The samples were cultured for staphylococci and methicillin-resistant staphylococci (MRS) recovery. The phenotype/genotype of antimicrobial resistance was analysed for all isolates. The spa-type and sequence-type (ST) were determined in Staphylococcus aureus strains; moreover, the presence of virulence and host-adaptation genes (tst, eta, etb, pvl, lukPQ, scn-eq, and scn) was studied by PCR. Staphylococcus species were detected in 27/30 (90%) and 33/50 (66%) of nasal and faecal samples, respectively. Ninety isolates belonging to eight species were recovered, with predominance of S. aureus (n = 34), Staphylococcus delphini (n = 19), and Staphylococcus sciuri (n = 19). S. aureus strains were all methicillin-susceptible (MSSA), 28/34 were susceptible to all the antibiotics tested, and the remaining six showed resistance to (gene-detected) streptomycin (ant (6)-Ia), penicillin (blaZ), and trimetroprim/sulphametoxazole (SXT) (dfrA, dfrG). The lineage ST1640/t2559 was predominant (n = 21). The genes lukPQ and scn-eq were present in all but the ST1640 isolates. Three S. sciuri isolates were multidrug-resistant. Healthy horses in Spain seem to be a reservoir for virulent MSSA and the lineage ST1640, although the presence of the latter in horses is described for the first time in this study. Moreover, the equine-adapted leukocidin gene lukPQ is frequent among S. aureus strains. A large variety of staphylococcal species with low antibiotic resistance rate were also observed. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Horses)
13 pages, 790 KiB  
Article
Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae in Hospitalized Neonatal Foals: Prevalence, Risk Factors for Shedding and Association with Infection
by Anat Shnaiderman-Torban, Yossi Paitan, Haia Arielly, Kira Kondratyeva, Sharon Tirosh-Levy, Gila Abells-Sutton, Shiri Navon-Venezia and Amir Steinman
Animals 2019, 9(9), 600; https://doi.org/10.3390/ani9090600 - 23 Aug 2019
Cited by 15 | Viewed by 2482
Abstract
Extended-spectrum β-lactamase Enterobacteriaceae (ESBL-E) have been investigated in adult horses, but not in foals. We aimed to determine shedding and infection in neonatal foals and mares. Rectal swabs were sampled from mare and foal pairs on admission and on the 3rd day of [...] Read more.
Extended-spectrum β-lactamase Enterobacteriaceae (ESBL-E) have been investigated in adult horses, but not in foals. We aimed to determine shedding and infection in neonatal foals and mares. Rectal swabs were sampled from mare and foal pairs on admission and on the 3rd day of hospitalization; enriched, plated, and bacteria were verified for ESBL production. Identification and antibiotic susceptibility profiles were determined (Vitek2). Genotyping was performed by multilocus sequence typing (MLST). Genes were identified by PCR and Sanger sequencing. Medical data were analyzed for risk factors (SPSS). On admission, 55 pairs were sampled, of which 33 pairs were re-sampled. Shedding rates on admission in foals and mares were 33% (95% CI 21–47%) and 16% (95% CI 8–29%), respectively, and during hospitalization, these increased significantly to 85% (95% CI 70–94%) and 58% (95% CI 40–73%), respectively. Foal shedding was associated with umbilical infection on admission (P = 0.016) and with ampicillin treatment during hospitalization (p = 0.011), and was independent of the mare’s shedding. The most common ESBL-E was Escherichia coli. During hospitalization, species diversity increased. Four foals were infected with ESBL-E strains, including umbilical infections and wounds. This study substantiates an alarming prevalence of shedding in neonatal foals, which should be further investigated in order to reduce resistance rates. Full article
(This article belongs to the Special Issue Antimicrobial Resistance in Horses)
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