Unidirectional animal-to-human transmission of methicillin-resistant Staphylococcus aureus ST398 in pig farming; evidence from a surveillance study in southern Italy

Abstract

BackgroundLivestock-associated methicillin-resistant Staphylococcus aureus (MRSA) belonging to clonal complex 398 is recognized as an occupational hazard for workers employed in intensive animal husbandry, especially in the swine-breeding chain. In this study, we compared the prevalence and epidemiological type of MRSA isolates from swine and farm workers in a large area of southern Italy.MethodsBetween January and March 2018, 88 workers from 32 farms where we had previously performed a survey for MRSA colonization of farmed pigs, were sampled by nasal swabbing. A follow-up investigation was conducted on seven workers 1 year after primary screening. MRSA isolates were characterized by MLST, spa and SCCmec typing, and tested for susceptibility to 15 antimicrobials. Epidemiological correlations between human and swine MRSA isolates were supported by Rep-MP3 and RAPD PCR fingerprinting, and whole-genome sequencing.ResultsThe overall colonization rate of MRSA in swine farm workers was 21.6%, being significantly higher in intensive farms and in workers with direct animal contact. All human MRSA isolates were multi-drug resistant, belonged to the ST398 livestock clade, and did not carry Panton-Valentine leukocidin and enterotoxin genes. Notably, 94.1% of human MRSA isolates belonged to the same epidemiological type as swine MRSA isolates from the corresponding farm. Persistent MRSA carriage was documented in some workers 1 year after primary sampling.ConclusionsWe report a high prevalence of MRSA among swine farm workers, with higher colonization rates associated with intensive breeding and animal exposure. Our findings suggest unidirectional animal-to-human transmission of LA-MRSA and denote the high zoonotic transmissibility of the ST398 livestock clade.

Assessment of the Antibiotic Resistance Profile, Genetic Heterogeneity and Biofilm Production of Methicillin-Resistant Staphylococcus aureus (MRSA) Isolated from The Italian Swine Production Chain

“…According to the EFSA report on antimicrobial monitoring on MRSA, the main route of transmission of LA-MRSA into the population is direct contact with animals, e.g., at abattoir level, and then dissemination [ 61 ]. In line with this, the study carried out by Pirolo et al [ 62 ] involving pig farm workers demonstrated that 21.6% of the workers were colonised by livestock-associated MRSA (LA-MRSA) and that this colonisation was significantly higher if direct animal–human contact occurred. Additionally, Cuny et al [ 63 ] detected a 30% antibiotic multiresistance to penicillins, tetracyclines and macrolides in ST398 MRSA isolated from humans in contact with farm animals, a fact that poses a therapeutic challenge if infection occurs.…”

Staphylococcus aureus in Intensive Pig Production in South Africa: Antibiotic Resistance, Virulence Determinants, and Clonality

“…A substantial number of isolates carried the PVL gene, corroborating a study conducted on S. aureus isolated from backyard-raised pigs and pig workers in Nigeria, with 27% of isolates harbouring PVL [ 65 ]. However, although PVL has been associated with necrotising pneumonia and joint infection in humans, its role in pigs is not thoroughly investigated; hence, the current findings should be interpreted with caution [ 66 ], as its presence does not necessarily imply diseased animals.…”

Antimicrobial use in food animals and human health: time to implement ‘One Health’ approach

“…Antimicrobial resistant bacteria originating in an animal can be transmitted to humans through the environment, food products, and/or by direct contact [ 8 ]. Similar strains of resistant bacteria are found in food animals and humans suggesting the bacterial transmission from animals to humans [ 21 ]. Plasmid-mediated resistance in E. coli , Salmonella and Klebsiella to colistin, a last line group of antimicrobial drug, is reported in both food animals and humans in countries from North America, Europe, Africa and Asia [ 17 ].…”