Molecular epidemiology of methicillin-resistant Staphylococcus aureus from dairy farms in North-eastern Italy

Transmission of Staphylococcus aureus along the dairy production chain is an emerging public health problem with human, veterinary, and food safety issues. The prevalence of multidrug-resistant, particularly methicillin-resistant S. aureus (MRSA), has steadily increased in several European countries. In this study, the prevalence of S. aureus in raw cow milk and farm workers was investigated, and the trajectories of MRSA transmission at the primary stage of the dairy chain were assessed. To this purpose, a longitudinal survey was conducted in 618 dairy farms in two contiguous regions with high livestock density in North-eastern Italy. S. aureus contamination of bulk tank milk (BTM) was observed in more than 80% of farms, while MRSA prevalence was 3.6% and 15.9% in BTM and farm workers, respectively. The majority of MRSA isolates from both BTM and farm workers were assigned to ST398, and showed a worrisome multidrug-resistant phenotype. Enterotoxin and Panton-Valentine leukocidin genes were detected in 11.5% and 4.9% of MRSA isolates from both sources. Nearly all MRSA isolates from workers belonged to the same epidemiological type as BTM isolates from the corresponding farm, denoting a bidirectional MRSA transmission pattern. A focus on the ST398 spa type t899 MRSA lineage in the Italian livestock system highlighted the presence of two major clusters whose dissemination was likely facilitated by the selective pressure imposed by antimicrobial use in animal farming. Our findings emphasize the need for continuous monitoring of MRSA along the dairy production chain, not only to avoid transmission between animals and exposed workers, but also to contain the risk of raw milk and dairy product contamination by multidrug resistant and toxigenic strain.