The dissemination of Staphylococcus aureus in the pork production chain is a major food safety concern. Abattoirs can serve both as disruptor and transmitter for S. aureus. In this study, we conducted a systematic genomic epidemiology research on the prevalence, heterogeneity, and transmission of S. aureus in 3,638 samples collected from four pig abattoirs in Hubei province, China. Our findings revealed substantial heterogeneity between S. aureus recovered from samples collected at upstream (from stunning step to head-removal step) and downstream (from splitting step to chilling step) locations within the slaughter process. Overall, 966 (26.6%) samples were positive for S. aureus, with significantly higher overall prevalence for upstream samples (29.0%, 488/1,681) compared to downstream samples (24.4%, 478/1,957). Antimicrobial susceptibility testing demonstrated that the isolates from the upstream exhibited significantly higher resistance proportions to different antimicrobials than those from the downstream. Whole-genome sequencing of 126 isolates revealed that ST398 (32.9%, 23/70) and ST9 (22.9%, 16/70) were more common among upstream isolates, while ST7 (35.7%, 20/56) and ST97 (28.6%, 16/56) were most frequently observed among downstream isolates. Additionally, molecular characterization analysis demonstrated that upstream isolates possessed significantly higher enterotoxigenic potential, more antimicrobial resistance genes, and S. aureus pathogenicity islands than downstream isolates. Notably, we discovered that enterotoxigenic S. aureus could be transmitted across different slaughter stages, with knives, water, and air serving as vectors. Although slaughtering processes had a substantial effect on reducing the food safety risk posed by enterotoxigenic S. aureus, the possibility of its widespread transmission should not be disregarded. IMPORTANCE Staphylococcus aureus (S. aureus) is one of the most important foodborne pathogens, and can cause foodborne poisoning by producing enterotoxins. Pork is a preferable reservoir and its contamination often occurs during the slaughter process. Our findings revealed significant differences in the prevalence, antimicrobial resistance, and enterotoxigenic potential between the upstream and downstream isolates within the slaughter process. Also, it is imperative not to overlook enterotoxigenic S. aureus transmitted across all stages of the slaughter process, with notable vectors being knives, water, and air. These findings hold significant implications for policy-makers to reassess their surveillance projects, and underscore the importance of implementing effective control measures to minimize the risk of S. aureus contamination in pork production. Moreover, we provide a more compelling method of characterizing pathogen transmission based on core-SNPs of bacterial genomes.
Keywords: Staphylococcus aureus; food safety; genomic epidemiology; heterogeneity; transmission.