Antimicrobial resistance of commensal Enterococcus faecalis and Enterococcus faecium from food-producing animals in Russia

Abstract

Background and aim: Although Enterococcus faecalis and Enterococcus faecium are common members of human and animal gut microbiota, their resistance to different antimicrobials makes them important pathogens. Multidrug-resistant enterococci often contaminate foods of animal origin at slaughterhouses. The World Health Organization and the World Organization for Animal Health recommend including animal-derived enterococci in antimicrobial resistance (AMR) monitoring programs. This study aimed to fill a literature gap by determining the current AMR prevalence of E. faecalis and E. faecium from different food-producing animals in Russia.

Materials and methods: Samples of biomaterial were taken from chickens (n=187), cattle (n=155), pigs (n=49), turkeys (n=34), sheep (n=31), and ducks (n=31) raised at 28 farms in 15 regions of Russia. Isolates of E. faecalis (n=277) and of E. faecium (n=210) (487 isolates in total; 1 isolate per sample) were tested for resistance to 12 antimicrobials from 11 classes using the broth microdilution method. Three criteria were used for the interpretation of minimum inhibitory concentration: Epidemiological cutoff values (ECOFFs) from the European Committee on Antimicrobial Susceptibility Testing (EUCAST) and Clinical and Laboratory Standards Institute (CLSI) clinical breakpoints. The AMR cloud online platform was used for data processing and statistical analysis.

Results: A difference of >10% was found between E. faecalis and E. faecium resistance to several antimicrobials (erythromycin, gentamycin, tetracycline, chloramphenicol, ciprofloxacin, and streptomycin). In total, resistance to most antimicrobials for enterococci isolates of both species taken from turkeys, chicken, and pigs was higher than cattle, sheep, and ducks. The highest levels were found for turkeys and the lowest for ducks. Among antimicrobials, resistance to bacitracin and virginiamycin was 88-100% in nearly all cases. High levels of clinical resistance were found for both bacteria species: Rifampicin (44-84%) from all animals, tetracycline (45-100%) from poultry and pigs, and erythromycin (60-100%), ciprofloxacin (23-100%), and trimethoprim-sulfamethoxazole (33-53%) from chickens, turkeys, and pigs. No vancomycin-resistant isolates were found. Most isolates were simultaneously resistant to one-three classes of antimicrobials, and they were rarely resistant to more than three antimicrobials or sensitive to all classes.

Conclusion: Differences in resistance between enterococci from different farm animals indicate that antimicrobial application is among the crucial factors determining the level of resistance. Conversely, resistance to rifampicin, erythromycin, tetracycline, and ciprofloxacin found in enterococci from farm animals in our study was notably also found in enterococci from wild animals and birds. Our results may be partly explained by the intrinsic resistance of E. faecium and E. faecalis to some antimicrobials, such as trimethoprim/sulfamethoxazole and bacitracin.

Keywords: Enterococcus faecalis; Enterococcus faecium; animals; antimicrobial resistance; enterococci; livestock.

Figure-1

Trimethoprim-sulfamethoxazole minimum inhibitory concentration distribution among Enterococcus faecalis isolates. Green columns – percent of susceptible isolates, red – resistant (EUCAST 2021 breakpoints), N – number of isolates.

Figure-2

Trimethoprim-sulfamethoxazole minimum inhibitory concentration distribution among Enterococcus faecium isolates. Green columns – percent of susceptible isolates, red – resistant (EUCAST 2021 breakpoints), N – number of isolates.

Figure-3

Rifampicin minimum inhibitory concentration distribution among Enterococcus faecalis isolates. Green columns – percent of susceptible isolates, yellow – intermediate resistant, red – resistant (CLSI 2021 breakpoints), N – number of isolates.

Figure-4

Rifampicin minimum inhibitory concentration distribution among Enterococcus faecium isolates. Green columns – percent of susceptible isolates, yellow – intermediate resistant, red – resistant (CLSI 2021 breakpoints), N – number of isolates.

Figure-5

Patterns of simultaneous resistance to different classes of antimicrobials. Sus (S+I) means the percent of isolates susceptible to all antimicrobials tested (susceptible + intermediate categories according to CLSI 2021). Res 1 means the percent of isolates resistant to at least 1 antimicrobial, Res 2 – to 2 antimicrobials, etc.