From the Farms to the Dining Table: The Distribution and Molecular Characteristics of Antibiotic-Resistant Enterococcus spp. in Intensive Pig Farming in South Africa

Abstract

Foodborne pathogens, including antibiotic-resistant species, constitute a severe menace to food safety globally, especially food animals. Identifying points of concern that need immediate mitigation measures to prevent these bacteria from reaching households requires a broad understanding of these pathogens’ spread along the food production chain. We investigated the distribution, antibiotic susceptibility, molecular characterization and clonality of Enterococcus spp. in an intensive pig production continuum in South Africa, using the farm-to-fork approach. Enterococcus spp. were isolated from 452 samples obtained along the pig farm-to-fork continuum (farm, transport, abattoir, and retail meat) using the IDEXX Enterolert®/Quanti-Tray® 2000 system. Pure colonies were obtained on selective media and confirmed by real-time PCR, targeting genus- and species-specific genes. The susceptibility to antibiotics was determined by the Kirby–Bauer disk diffusion method against 16 antibiotics recommended by the WHO-AGISAR using EUCAST guidelines. Selected antibiotic resistance and virulence genes were detected by real-time PCR. Clonal relatedness between isolates across the continuum was evaluated by REP-PCR. A total of 284 isolates, consisting of 79.2% E. faecalis, 6.7% E. faecium, 2.5% E. casseliflavus, 0.4% E. gallinarum, and 11.2% other Enterococcus spp., were collected along the farm-to-fork continuum. The isolates were most resistant to sulfamethoxazole-trimethoprim (78.8%) and least resistant to levofloxacin (5.6%). No resistance was observed to vancomycin, teicoplanin, tigecycline and linezolid. E. faecium displayed 44.4% resistance to quinupristin-dalfopristin. Also, 78% of the isolates were multidrug-resistant. Phenotypic resistance to tetracycline, aminoglycosides, and macrolides was corroborated by the presence of the tetM, aph(3′)-IIIa, and ermB genes in 99.1%, 96.1%, and 88.3% of the isolates, respectively. The most detected virulence gene was gelE. Clonality revealed that E. faecalis isolates belonged to diverse clones along the continuum with major REP-types, mainly isolates from the same sampling source but different sampling rounds (on the farm). E. faecium isolates revealed a less diverse profile. The results suggest that intensive pig farming could serve as a reservoir of antibiotic-resistant bacteria that could be transmitted to occupationally exposed workers via direct contact with animals or consumers through animal products/food. This highlights the need for more robust guidelines for antibiotic use in intensive farming practices and the necessity of including Enterococcus spp. as an indicator in antibiotic resistance surveillance systems in food animals.

Molecular characterization and antimicrobial resistance of Enterococcus faecalis isolated from seafood samples

“…Badul et al. (2021) displayed that E. faecalis resistance rate against ciprofloxacin, gentamicin, streptomycin, teicoplanin, quinupristin‐dalfopristin, nitrofurantoin, sulphamethoxazole‐trimethoprim, erythromycin, tetracycline, chloramphenicol, and levofloxacin antimicrobials was 9.3%, 15.1%, 69.8%, 0.0%, 3.1%, 77.8%, 71.6%, 79.6%, 25.3%, and 4.4%, respectively. E. faecalis strains isolated from food samples in Brazil (Riboldi et al., 2009) harbored the boost resistance rate towards ampicillin (11.1%), vancomycin (3.7%), erythromycin (11.1%), tetracycline (33.3%), ciprofloxacin (7.4%), norfloxacin (0.0%), nitrofurantoin (0.0%), chloramphenicol (7.4%), gentamicin (22.2%), and lincomycin (51.9%) antimicrobials.…”

Antimicrobial resistance in the Spanish swine production: Impact of the production system and the antimicrobial use = Resistencias antimicrobianas en la producción porcina española: impacto del sistema de producción y del uso de antibióticos

“…Genotypic characterization of the collection of isolates evidenced a differential distribution of ARDs, not only by taxon, but also within taxon by species. The most prevalent ARDs harbored by these taxa conferred resistance to antimicrobial classes not included in the AMEG Category B, such as aminoglycosides, tetracyclines, macrolideslincosamides-streptogramins-pleuromutilins (MLSP) and beta-lactams, in agreement with previous studies (AbuOun et al, 2020;Arredondo-Alonso et al, 2020;Badul et al, 2021;Rivera-Mendoza et al, 2020). In fact, isolates harboring transferable ARGs to last resort antimicrobials forbidden in food-producing animals were residual on the investigated farms, highlighting that no ESBL or vancomycin ARGs were detected.…”

Prevalence and Characterisation of Multiresistant Bacterial Strains Isolated in Pigs from the Island of Tenerife

“…The presence of vancomycin-resistant Enterococcus (VRE), as well as carbapenemaseproducing and colistin-resistant Enterobacteriaceae (CRE), was not found, despite various studies describing the presence of these multiresistant strains in pig livestock [44,45].…”