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.

Antibiotic resistance in Italian poultry meat production chain: a one-health perspective comparing antibiotic free and conventional systems from the farming to the slaughterhouse

“…In enterococci the resistance for tetracycline, and streptomycin were mostly detected, while other studies, involving enterococci isolates recovered from broilers, revealed the resistance also for vancomycin, gentamicin and quinupristin-dalfopristin in Portugal (Novais et al, 2005), Turkey (Ünal et al, 2020) and, more recently, in Bangladesh (Roy et al, 2022) and Russia (Makarov et al, 2022). This evidence represents an important public health concern, considering that resistant enterococci of animal origin could be Frontiers in Food Science and Technology frontiersin.org 10 drivers of resistance patterns for human strains responsible of various nosocomial infections (Hammerum et al, 2010).…”

Comparing antibiotic resistance and virulence profiles of Enterococcus faecium, Klebsiella pneumoniae, and Pseudomonas aeruginosa from environmental and clinical settings

“…In clinical settings, E. faecium HA outbreaks [e.g., urinary tract infections (UTIs), amongst others] are associated with highly resistant and virulent strains of this species [ [17] , [18] , [19] ]. Resistant E. faecium isolates exhibit intrinsic resistance to cephalosporins, beta (β)-lactams, clindamycin (lincosamide), quinupristin and dalfopristin (streptogramins), and trimethoprim-sulfamethoxazole or acquired resistance to β-lactams, aminoglycosides, glycopeptides, streptogramins, linezolid, daptomycin, and tigecycline [ 20 , 21 ]. Resistance has been attributed to the acquisition of antimicrobial resistance gene (ARG) variants [e.g., van (vancomycin resistance), tet (tetracycline resistance)], expression of β-lactamases, point mutations in antibiotic binding regions, and modifications of antibiotic precursors, amongst others [ [22] , [23] , [24] ].…”

Exploring the causes of the prevalence of vancomycin-resistant Enterococcus faecalis

“…Additionally, Ali Liaqat et al explicated the influence of environmental factors, such as eutrophication, on the resistance profiles of enterococci, illustrating the environmental dimension of antimicrobial resistance [32]. The work of Makarov Dmitry A et al further explored the impact of antibiotic utilization practices on the resistance levels among enterococci from farm animals, shedding light on the interconnectedness of antibiotic use and resistance emergence [33]. The emergence of antibiotic resistance in E. faecalis strains presents a formidable challenge to global public health, encompassing a broad spectrum of contexts from clinical settings to agricultural domains and aquatic environments.…”