Staphylococcus aureus nasal and intestinal carriage by free-ranging red deer: evidence of human, domestic and wild animal lineages

Abstract

Purpose: Habitat loss and fragmentation, caused by human activities, can trigger interactions among humans, domestic and wild animals, creating opportunities for the transmission of infectious agents. In Stelvio National Park (SNP, Central Italian Alps, Lombardy sector), the increase of the red deer population, associated with an intense browsing impact and cross transmission of pathogens with livestock, imposed the activation of a culling plan. Moreover, culled deer from SNP entered the human food chain with 37.3 tons of meat in 2011-16. This study evaluates the prevalence and genetic characteristics of Staphylococcus aureus isolates from nasal cavities and rectal tracts in red deer culled in SNP in January and February 2017. Methods & Materials: Both nasal swabs and feces or rectal swabs, collected from 75 red deer, were incubated in Mueller-Hinton broth with 6.5% NaCl and seeded on Baird-Parker with rabbit plasma fibrinogen. S. aureus was confirmed by amplification of the nuc gene. One isolate per collection site from simultaneous nasal and intestinal carriers was characterized using a S. aureus-specific DNA microarray, which detects over 333 genes and alleles. Results: A S. aureus prevalence of 90.67% (95% CI: 81.97–95.41) and 26.67% (95% CI:17.98–37.63) was detected in nasal and intestinal site respectively. All intestinal carriers (n = 20) had also a nasal colonization. Clonal complex (CC) 425, known to be widespread in ruminants, was the most prevalent lineage (68.29%). Notably, 67.86% of CC425 strains carried the leukocidin genes lukM/lukF-P83, which are not typical of this lineage. Further lineages identified included some that are also known to infect humans and/or livestock (CC7, CC9, CC350, CC707) and some (CC2328, CC2671) that are so rare that no epidemiological information is available. All isolates were negative for methicillin resistance genes, but human lineages harbored penicillin resistance genes and one isolate also ermA gene. Conclusion: A high prevalence of S. aureus carriers has been observed among free-ranging red deer during the cold season in the Alps. Red deer S. aureus population mainly comprised lineages known to occur in domestic and wild ruminants. Sporadic overlaps with human and other animal lineages were observed.