Antimicrobial resistance of endometrial bacterial isolates collected from UK Thoroughbred mares between 2014 and 2020

Abstract

Background: Antimicrobial resistance (AMR) is important in equine reproduction, as antimicrobials have historically been widely used in the management of breeding mares. However, evidence of the characteristics of AMR in uterine isolates is limited in the UK. The objective of this retrospective study was therefore to describe temporal changes in AMR patterns of bacteria isolated from the endometrium of Thoroughbred broodmares in south-east England between 2014 and 2020. Method: Endometrial swabs were processed for microbiology and antimicrobial susceptibility testing (AST). For frequently isolated bacteria, changes in AMR patterns over time were assessed using a logistic regression model. Results: From 18,996 endometrial swabs, 30.5% were positive for microbial culture. AST was performed on 2091 isolates, representing 1924 swabs collected from 1370 mares located at 132 premises. Beta-haemolytic Streptococcus (BHS, 52.5%) and Escherichia coli (25.8%) were most frequently isolated. In BHS, resistance to enrofloxacin (p = 0.02), nitrofurazone (p < 0.001) and oxytetracycline (p < 0.01) increased significantly between 2014 and 2020, while resistance to trimethoprim-sulfamethoxazole (p < 0.001) decreased. In E. coli, resistance to nitrofurazone increased (p = 0.04) and resistance to gentamycin (p = 0.02) and trimethoprim-sulfamethoxazole (p < 0.001) decreased. Limitations: Variations in the specimen collection protocols might have affected the frequency of isolates detected. Conclusion: Between 2014 and 2020, AMR changed in this bacterial population. However, there was no significant increase in resistance to penicillin (99.6% BHS susceptible), gentamycin (81.7% E. coli susceptible) or ceftiofur.

Prevalence of Microbial Isolates Cultured from Endometrial Swab Samples Collected from United Kingdom Thoroughbred Mares from 2014 to 2020

“…In summary, this study has, for the first time, estimated the population-level prevalence of isolates in over 18,000 endometrial-swab samples collected over a 7-year period from Thoroughbred broodmares in the UK, and has evaluated the variation in overall prevalence and the prevalence of the most common isolates according to year of sampling, mare age and cytology findings. These results provide much-needed population-level benchmarking of key bacterial species in a UK setting and compliment the findings from our larger body of work [ 18 , 19 ], which aims to highlight important limitations in current practices in terms of the use of unguarded endometrial swabs and the routine pre-breeding swabbing of clinically normal mares. Our findings also highlight knowledge gaps in the understanding of uterine “health” and “disease” in Thoroughbred broodmares and can inform future research to improve both antimicrobial stewardship and Thoroughbred reproductive health and productivity.…”

“…The overall prevalence of all types of isolates reported in the present study (35%) is in keeping with isolate frequencies reported from a study of 2311 uterine swab samples submitted to a laboratory in Ithaca, USA between 2007 and 2017 (39%) [ 17 ]. It is also similar to those from 8269 pre-breeding or diagnostic uterine samples from 7655 mares (swabs (95%), flushes or biopsies) submitted to a laboratory in Florida, USA between 2003 and 2008 (31%) [ 18 ], and from 394 routine pre-breeding samples (315 swabs, 79 flushes) submitted to a laboratory in Italy between 2014 and 2018 (33%) [ 19 ]. It is, however, much higher than frequencies reported from studies exclusively using guarded swabs for 2660 routine pre-breeding samples collected from 1621 mares on 17 Thoroughbred studs in Australia (7%) [ 10 ] and 2123 pre-breeding and diagnostic samples collected from 970 mares in the USA between 2001 and 2004 (11%) [ 11 ].…”

“…There is growing concern over the risk of antimicrobial resistance (AMR) in the reproductive tract of broodmares, due to the widespread usage of antibiotics both in intra-uterine treatments and semen extenders [23]. As such, the AMR patterns of present isolates have also been reported [19], where it can be observed that, particularly for E. coli isolates but perhaps also for β-hemolytic Streptococcus isolates, the patterns of temporal variation in prevalence reported here appear to follow patterns of temporal variation in AMR [19].…”

“…This study forms part of a larger body of work that has also described antimicrobial resistance patterns in a subset of these isolates [ 19 ] and evaluated current diagnostic strategies [ 18 ].…”

Clinical Aspects of Bacterial Distribution and Antibiotic Resistance in the Reproductive System of Equids

“…Antibiotic resistance of bacteria isolated from equine reproductive organs has been reported for animals with fertility problems, as shown in studies performed in various countries in Europe (France [ 10 , 130 ], Germany [ 136 ], Italy [ 42 , 137 ], Slovakia [ 43 ], Sweden [ 20 ], Turkey [ 138 ], United Kingdom [ 139 ]) and elsewhere (Brazil [ 140 ], Canada [ 141 ], India [ 142 ], United States of America [ 143 ]). Antimicrobials are commonly used to treat empirically reproductive disorders.…”