Zoonotic linkage and environmental contamination of Methicillin-resistant Staphylococcus aureus (MRSA) in dairy farms: A one health perspective

Abstract

Methicillin-Resistant Staphylococcus aureus (MRSA) is a ubiquitous public health challenge, with its prevalence in human, animal, and environmental interfaces posing significant concerns. This study aimed to characterize and detect the zoonotic linkages of MRSA within the cow-environment-human interfaces in dairy farms to address the One Health perspective. A comprehensive investigation, involving 636 samples (an equal number of raw milk and cow nasal swab samples, along with varying numbers of human nasal swab and environmental samples), revealed an overall MRSA prevalence of 13.4% (n = 271/636). Notably, environmental samples exhibited the highest prevalence (19.3%), emphasizing the potential role of farm surroundings in MRSA transmission, while the lowest prevalence was found in raw milk at 11.8% (n = 31/263). The prevalence in cow nasal swabs and human nasal swabs was 13.3% (n = 35/263) and 15.1% (n = 8/53), respectively. Multiplex PCR analysis revealed the presence of different Staphylococcal enterotoxin (SEa, SEb, SEc, and SEd), and exfoliative toxin-producing genes (Eta, Etb) within the MRSA isolates underlining their potential to induce public health threats. All MRSA isolates exhibited complete resistance to Oxacillin (100%) and Amoxicillin (100%), while the highest sensitivity was observed for Vancomycin (85.8%). Furthermore, these MRSA strains demonstrated varying degrees of resistance to other commonly used antimicrobial drugs, including Cefoxitin (75.3%), Ceftarolin (71.2%), Sulfamethoxazole-Trimethoprim (63.5%), Ciprofloxacin (60%), and Gentamicin (49.5%). Detection of MRSA in cow, human, and environmental samples within the same farm vicinity highlights the risk of zoonotic transmission of MRSA from cows to humans through environmental interfaces. Phylogenetic analysis of the mecA gene in MRSA isolates from all sources within the same farm revealed a high similarity index (>84%) among them suggesting a shared evolutionary origin. Moreover, the MRSA isolates from milk samples showed a close evolutionary relationship with isolates from Kenya and Brazil, while the isolates from humans and the environment displayed noticeable resemblance to isolates from several Asian countries. The findings emphasize the importance of collaborative efforts under the One Health framework to address this multifaceted issue and ensure the safety of our food supply and public health.