Molecular epidemiology of antibiotic-resistant Enterococcus spp. from the farm-to-fork continuum in intensive poultry production in KwaZulu-Natal, South Africa

Highlights: @@@ The poultry food production continuum is a reservoir of multidrug-resistant Enterococcus spp. @@@ High prevalence of resistance to antibiotics used as growth-promotors was observed. @@@ The tetM and ermB antibiotic resistance genes were most commonly detected. @@@ The adhesin virulence factor, efaAFm, was predominant among isolates. @@@ There was high genetic diversity among isolates along the farm-to-fork continuum. -- Abstract: The poultry industry is among the main protein suppliers worldwide. Thus, this study determined the antibiotic resistance and virulence profiles of Enterococcus spp. along the farm-to-fork production chain of an intensive poultry system in the uMgungundlovu District, Kwazulu-Natal, South Africa. Overall, 162 samples along the continuum (growth phase, transport and post-slaughter) were evaluated for the presence of Enterococcus spp. using selective media, biochemical tests and polymerase chain reaction (PCR). Resistance profiles were assessed by Kirby-Bauer disk diffusion method following the WHO-AGISAR recommended antibiotics panel for Enterococcus spp. Antibiotic resistance and virulence genes were detected using real-time PCR. Clonal relatedness was evaluated by REP-PCR. Overall, 131 isolates were recovered across the continuum, (34% E. faecalis, 32% E. faecium, 2% E. gallinarum and 32% other Enterococcus spp.). Resistance to tetracycline (79%), erythromycin (70%), nitrofurantoin (18%), ampicillin (15%), streptomycin (15%), chloramphenicol (10%), ciprofloxacin (4%), tigecycline (4%), gentamicin (4%), teicoplanin (3%) was observed among all Enterococcus spp.; no vancomycin resistance (0%) was recorded. Also, 24% of E. faecium were resistant to quinupristin-dalfopristin. Twenty-four multidrug resistance (MDR) antibiograms were observed across all species; E. faecium (43%) showed the highest frequency of MDR. The most frequently observed antibiotic resistomes were tetM (76%) and ermB (66%) while smaller percentages were noted for aph(3@@@)-IIIa (12%) and vanC1 (1%). Virulence genes efaAFs (100%), cpd (96%) and gelE (80%) were more prevalent in E. faecalis. Clonality revealed that isolates along the continuum were highly diverse with major REP-types consisting of isolates from the same sampling point. This study highlights the diversity of MDR Enterococcus in the food chain with isolates harbouring resistance and virulence genes. These could be reservoirs for the potential transfer of pathogenic enterococci carrying these genes from poultry to humans through the food chain continuum, thus, underscoring the need for routine antibiotic resistance surveillance in food animals.