Antimicrobial and biocide resistance in Staphylococcus aureus: genomic features, decontamination strategies, and the role of S. aureus complex-related species, with a focus on ready-to-eat food and food-contact surfaces

Abstract

Staphylococcus (S.) aureus can proliferate in a broad range of food and contact surfaces. The ability to grow as a biofilm enhances its resistance to cleaning agents and the chance to persist on food facility contact surfaces and enter the food chain. This presents a risk to the health of food workers and consumers, considering that this pathogen has been associated with a wide variety of local and systemic human infections, as well as with food poisoning caused by the production of enterotoxins. In particular, ready-to-eat (RTE) food, that does not undergo further processing capable of reducing bacterial contamination, may be of particular concern since its consumption poses a direct microbiological risk to consumers. To worsen this scenario, S. aureus harbors several biocide and antimicrobial resistance genes (BRGs and ARGs), which, respectively, reduce the efficacy of sanitizing agents during cleaning procedures and antimicrobial treatments when infections occur. Considering this, several novel methods have recently been investigated to control S. aureus contamination in food and contact surfaces in food facilities in order to overcome the limitations of traditional sanitizing protocols and improve the safety of the produced food products. In this review, we will provide an overview of S. aureus ARGs and BRGs and whole-genome sequence (WGS)-based methods recently implemented for their surveillance. Furthermore, we will describe the presence of antimicrobial-resistant S. aureus in RTE food and food-contact surfaces and present novel natural or chemical compounds, new food-contact materials, and innovative physical methods to control the contamination of this pathogen in the food sector. Finally, we will also discuss if S. aureus complex-related species are emerging as new antimicrobial-resistant pathogens of the food chain.