Prevalence and Occupational Risk of Methicillin- Resistant Staphylococcus aureus Carriage in Commercially Produced Food Animals

Xiaoyu Ma

doi:10.60867/00000181

Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) has emerged as an important public health concern within intensive food animal production systems due to the potential for antimicrobial resistance dissemination and occupational exposure at the animal–human–environment interface. Despite increasing reports of LA-MRSA in livestock production environments, integrated investigations comparing different commercial livestock production systems and linking animal, human, and environmental populations remain limited. This thesis investigated the molecular epidemiology, antimicrobial resistance characteristics, phylogenetic relationships, and occupational exposure associated with LA-MRSA across commercial pig, cattle, and chicken production systems in a major livestock-producing region of China. Samples were collected from animals, farm workers, and farm-associated environments within commercial production systems. MRSA isolates were characterised using antimicrobial susceptibility testing and whole genome sequencing to determine clonal complexes (CCs), sequence types (STs), staphylococcal cassette chromosome mec (SCCmec) types, antimicrobial resistance genes, virulence genes, and phylogenetic relationships. A total of 64 MRSA isolates were identified from pig production systems, of which 59 were included in further analyses. In cattle and chicken production systems, 16 and 221 MRSA isolates were identified, respectively, with 16 cattle-associated isolates and 147 chicken-associated isolates included. Distinct livestock production systems were associated with different dominant LA-MRSA lineage structures. CC398-ST398 predominated in pig and layer chicken production systems. CC9-ST9 was the predominant lineage identified in cattle and broiler production systems. A localized CC5 lineage was additionally identified in broiler production systems. Phylogenetic analyses showed isolates from animals, farm workers, and environmental sources were interspersed throughout the phylogenetic trees within livestock production systems, with no evident clustering according to source. Similar patterns were observed in lineage-specific analyses of CC5, CC9 and CC398, in which isolates from different livestock production systems did not form distinct phylogenetic clusters. Multidrug resistance (MDR) was widely identified among LA-MRSA isolates recovered from animal, worker, and environmental sources across all livestock sectors. Resistance to chloramphenicol, clindamycin, erythromycin, gentamicin and tetracycline was observed phenotypically and corresponded with the presence of resistance genes including aac(6′)- aph(2″), erm(C), fexA, lnu(B), lsa(E) and tet(L). A broad range of virulence genes was also identified across isolates from all source types, including genes associated with adhesion, biofilm formation, immune evasion, haemolysis, capsule synthesis and iron acquisition. Occupational LA-MRSA carriage was identified among farm workers with direct animal contact across pig, cattle, and chicken production systems. MRSA carriage was identified exclusively among feeding workers and was associated with several occupational and individual exposure factors, including hospitalisation within the previous year, skin breakdown or inflammation, household animal exposure, longer employment duration, and current farm animal contact. Occupational risk patterns varied between livestock production systems, with prolonged occupational exposure more prominent in pig production systems, skin breakdown or inflammation more evident among cattle workers, and household animal exposure contributing more substantially within chicken-associated occupational settings. This thesis provides an integrated investigation of LA-MRSA across commercial livestock production systems by linking animal, farm worker, and environmental populations within intensive food animal production environments. The findings improve understanding of the molecular epidemiology, antimicrobial resistance characteristics, and potential dissemination patterns of LA-MRSA within livestock production systems and highlight the importance of integrated One Health surveillance approaches targeting interconnected farm-associated populations.

Prevalence and Occupational Risk of Methicillin- Resistant Staphylococcus aureus Carriage in Commercially Produced Food Animals

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