Prevalence and Virulence Determinants of Staphylococcus aureus in Wholesale and Retail Pork in Wuhan, Central China

Zhihao Zhu; Xiaoying Liu; Xingyu Chen; Geng Zou; Qi Huang; Xianrong Meng; Xiaoying Pei; Zhou Chen; Rui Zhou; Dongliang Hu; Mei Liu; Shaowen Li

doi:10.3390/foods11244114

Prevalence and Virulence Determinants of Staphylococcus aureus in Wholesale and Retail Pork in Wuhan, Central China

Foods. 2022 Dec 19;11(24):4114. doi: 10.3390/foods11244114.

Authors

Zhihao Zhu¹, Xiaoying Liu¹, Xingyu Chen¹, Geng Zou¹, Qi Huang¹, Xianrong Meng¹, Xiaoying Pei², Zhou Chen², Rui Zhou¹, Dongliang Hu³, Mei Liu¹, Shaowen Li¹

Affiliations

¹ Key Laboratory of Preventive Veterinary Medicine in Hubei Province, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430070, China.
² Wuhan Agricultural Comprehensive Law Enforcement Inspector Corps, Wuhan 430010, China.
³ Department of Zoonoses, Kitasato University School of Veterinary Medicine, Towada 034-8628, Japan.

Abstract

Staphylococcus aureus is one of the major foodborne pathogens and can cause serious foodborne illness in humans by foods contaminated with S. aureus enterotoxins. In recent years, livestock-associated S. aureus has been a major public health concern for humans and has emerged in various countries globally. China is one of the largest producers of pigs and pork in the world. However, there are few studies on the detailed genotypic and pathogenic characterization of pork-associated S. aureus in China. In this study, the prevalence, antimicrobial resistance, and genotypic characteristics of S. aureus in raw pork in Wuhan, China, were investigated through multilocus sequence typing (MLST), staphylococcal protein A gene (spa) typing, and whole-genome sequencing analysis. A total of 518 S. aureus isolates (16.9%) were isolated from 3067 retail and wholesale pork samples. The prevalence of S. aureus in retail pork (22.7%) was significantly higher than in wholesale pork (15.1%), while the proportion of multidrug-resistant (MDR) isolates in wholesale pork (12.9%) was significantly higher than in retail pork (6.2%). Among the isolates, 10.8% were resistant to three or more antibiotics, with higher rates of resistance to penicillin (88.8%) and erythromycin (58.1%). A total of 28 sequence types (STs) were identified in the 518 isolates, and the predominant type was ST7 (57.5%), followed by ST5 (9.1%). In addition, based on the whole-genome sequences of 39 representative strains, 17 spa types were identified among the isolates, of which t899, t091, and t437 were the most common. Furthermore, 19 staphylococcal enterotoxin (SE) and SE-like (SEl) toxin genes were detected in the isolates, of which selw was the most common type (100%), followed by sei, sem, seo, seu, and selv (46.2%); sey (35.9%); and sea, seg, and sen (33.3%). This study found for the first time that ST7-t091-selw and ST9-t899-SCCmecXII-selw were the predominant genotypes of S. aureus in pork in China, which indicated the spreading of S. aureus with multiple virulence factors, especially with new SE/SEl types in pigs and pork, is a serious new challenge for food safety. Good hygiene and good production practices to prevent interspecies transmission and cross-contamination of S. aureus in the pig-pork chain are of great significance to public health.

Keywords: MRSA; Staphylococcus aureus; antimicrobial resistance; enterotoxin; food safety; pork; virulence factor.

Grants and funding

This work was financially supported by the National Key Research and Development Program of China (Grant Nos. 2022YFD1800400 and 2018YFD0500500) and the Joint Funds of the National Natural Science Foundation of China (NSFC) (Grant No. 8161101134).