Occurrence of Staphylococcus aureus in swine and swine workplace environments on industrial and antibiotic-free hog operations in North Carolina, USA: A One Health pilot study

Abstract

Occupational exposure to swine has been associated with increased Staphylococcus aureus carriage, including antimicrobial-resistant strains, and increased risk of infections. To characterize animal and environmental routes of worker exposure, we optimized methods to identify S. aureus on operations that raise swine in confinement with antibiotics (industrial hog operation: IHO) versus on pasture without antibiotics (antibiotic-free hog operation: AFHO). We associated findings from tested swine and environmental samples with those from personal inhalable air samplers on worker surrogates at one IHO and three AFHOs in North Carolina using a new One Health approach. We determined swine S. aureus carriage status by collecting swab samples from multiple anatomical sites, and we determined environmental positivity for airborne bioaerosols with inhalable and impinger samplers and a single-stage impactor (ambient air) cross-sectionally. All samples were analyzed for S. aureus, and isolates were tested for antimicrobial susceptibility, absence of scn (livestock marker), and spa type. Seventeen of twenty (85%) swine sampled at the one IHO carried S. aureus at >1 anatomical sites compared to none of 30 (0%) swine sampled at the three AFHOs. All S. aureus isolates recovered from IHO swine and air samples were scn negative and spa type t337; almost all isolates (62/63) were multidrug resistant. S. aureus was recovered from eight of 14 (67%) ambient air and two (100%) worker surrogate personal air samples at the one IHO, whereas no S. aureus isolates were recovered from 19 ambient and six personal air samples at the three AFHOs. Personal worker surrogate inhalable sample findings were consistent with both swine and ambient air data, indicating the potential for workplace exposure. IHO swine and the one IHO environment could be a source of potential pathogen exposure to workers, as supported by the detection of multidrug-resistant S. aureus (MDRSA) with livestock-associated spa type t337 among swine, worker surrogate personal air samplers and environmental air samples at the one IHO but none of the three AFHOs sampled in this study. Concurrent sampling of swine, personal swine worker surrogate air, and ambient airborne dust demonstrated that IHO workers may be exposed through both direct (animal contact) and indirect (airborne) routes of transmission. Investigation of the effectiveness of contact and respiratory protections is warranted to prevent IHO worker exposure to multidrug-resistant livestock-associated S. aureus and other pathogens.

Face Mask Use and Persistence of Livestock-associated Staphylococcus aureus Nasal Carriage among Industrial Hog Operation Workers and Household Contacts, USA

“…Surprisingly, household members who were persistent carriers of S. aureus putatively associated with CC398 or CC9 appeared to have similar numbers of S. aureus CFU in their noses, on average, as workers who persistently carried these outcomes. These findings were unexpected given that household members in this study had no direct contact with the IHO environment, the likely source of livestock-associated S. aureus (Davis et al. 2018).…”

“…Participants in this study lived in a region characterized by the highest density of industrial hog production in the United States and rapidly growing poultry production (National Agricultural Statistics Service 2012; Webb 2014). By venting animal barns and spraying animal waste on proximal fields, industrial food animal production facilities regularly emit S. aureus and other bioaerosols that could contaminate neighboring households (Davis et al. 2018; Gibbs et al.…”

Association Between agr Type, Virulence Factors, Biofilm Formation and Antibiotic Resistance of Staphylococcus aureus Isolates From Pork Production

“…The “One Health” concept recognizes that human health or livestock or wildlife health are interconnected and bound to the animal-human-ecosystems in which they (co)exist. Occupational exposure to swine has been associated with increased Staphylococcus aureus carriage, and increased risk of colonization and infections of different hosts ( Witte et al, 2007 ; Graveland et al, 2011 ; Price et al, 2012 ; Kock et al, 2013 ; Ge et al, 2017 ; Davis et al, 2018 ). The risk of zoonotic transmission to humans demands our deep understanding of S. aureus contamination and ecology in the swine production.…”

Quantifying resilience of humans and other animals

“…Industrial livestock production is associated with concerns regarding animal welfare ( 6 ) as well as worries about risks to human health arising from antibiotic-resistant bacteria ( 7 , 8 ) and disease outbreaks ( 9 – 11 ). This has led to the global One Health movement focusing on the collaborative effort of multiple disciplines to attain optimal health for people, animals, and our environment ( 12 – 15 ). One problem is that the conditions that facilitate highly efficient production of meat, milk, and eggs tend to come at a cost in the animals’ resilience ( 16 – 19 ).…”