Prevalence and Characterization of Methicillin-Resistant Staphylococcus aureus from Animals, Retail Meats and Market Shopping Vehicles in Shandong, China

<i>Staphylococcus aureus</i> has been recognized as an important foodborne pathogen and methicillin-resistant <i>S. aureus</i> (MRSA) can cause fatal infections worldwide. Of great concern is that MRSA have been found in animals and non-healthcare settings; however, knowledge about the prevalence and genetic characteristics of <i>S. aureus</i>, especially MRSA from animals, retail meats and market shared shopping vehicles in the same district, is limited. In this study, we collected 423 samples including handrail swabs (<i>n</i> = 226) of shopping trolleys and baskets from 18 supermarkets, retail meats (<i>n</i> = 137) and swine nasal swabs (<i>n</i> = 60) between 2018 and 2020 in China. <i>S. aureus</i> isolates were isolated and identified by PCR, and then the <i>mecA</i> was used to confirm the MRSA. The antibiotic resistance and virulence genes among <i>S. aureus</i> were also analyzed, followed by whole genome sequencing (WGS). <i>S. aureus</i> isolates were widely distributed in shared shopping vehicles (8.0%, 18/226), retail meats (14.6%, 20/137) and swine (18.3%, 11/60). In total, 49 <i>S. aureus</i> were obtained and 20 of the 49 isolates were MRSA. We firstly reported a high prevalence of MRSA in shared shopping vehicles (7.5%, 17/226), followed by raw meats (2.2%, 3/137), and 44.4% (8/18) of the 18 supermarkets possessed MRSA-positive shopping vehicles. All 20 MRSA isolates were SCC<i>mec</i> IVa MRSA clones. Enterotoxin genes (<i>sea</i>/<i>seb</i>) associated with <i>S. aureus</i> food poisoning were present in 45.0% of the 20 <i>S. aureus</i> isolates from retail meats and 25.0% of the 20 MRSA isolates carried enterotoxin genes. Retail meats in this study carried ST6-MRSA, a common ST type of <i>S. aureus</i> from food-poisoning outbreaks in China. WGS showed that the MRSA from meats harbored enterotoxin gene <i>sea</i> and immune evasion genes (<i>sak</i> and <i>scn</i>) associated with human infections, and were clustered with previously reported MRSA isolates from animals and humans. The MRSA isolates carrying multiple virulence genes from shopping vehicles were also clustered with previously reported MRSA isolates from humans and animals, suggesting that the exchange of MRSA isolates might occur among different niches. Our results highlighted the risk of retail meats and shared shopping vehicles in spreading antimicrobial-resistant pathogens including MRSA. To our knowledge, this is the first report of the wide spread of MRSA in shared shopping vehicles in China.