High Prevalence of Livestock-Associated Methicillin-Resistant Staphylococcus aureus in Hungarian Pig Farms and Genomic Evidence for the Spillover of the Pathogen to Humans

Abstract

Livestock-Associated Methicillin-ResistantStaphylococcus aureus (LA-MRSA) strains of clonal complex (CC) 398 are widely disseminated in pigs and are considered emerging pathogens in human medicine. To investigate the prevalence, genetic characteristics, and zoonotic potential of the pathogen in pig production settings, dust samples were collected from 40 pig operations in Hungary, along with nasal swabs of attending veterinarians and other swine professionals (n = 27) in 2019. MRSA isolates were further characterized by performing whole-genome sequencing and susceptibility testing. The whole-genome sequences of 14 human-derived LA-MRSA clinical isolates from the same year were also included in the study. The proportion of positive farms was 83% (33/40), and 70% (19/27) of the swine professionals carried the pathogen. All but one MRSA strain belonged to CC398, including the human clinical isolates. The core genome multilocus sequence typing (cgMLST) analysis revealed clusters of closely-related isolates of both environmental and human origin with a pairwise allelic distance of ≤24, and both cgMLST and single nucleotide polymorphism (SNP) analyses suggest recent transmission events between the farm environment and humans. Four human clinical isolates harboured the immune-evasion gene cluster, of which one was considered to be closely related to farm isolates. Half of the swine-related strains showed decreased susceptibility to eight or more antimicrobials, and along with human isolates, they carried eight different types of multidrug-resistance genes, including cfr. The results showed a dramatic increase in the occurrence of LA-MRSA in the swine industry in Hungary, compared with the 2% prevalence reported by the European Food Safety Authority baseline study in 2008. The wide range of antimicrobial resistance of the strains, accompanied by the emergence of the pathogen in humans — both asymptomatic carriers and diseased — call for revision of the risk posed by LA-MRSA to the public health.