The Indoor-Air Microbiota of Pig Farms Drives the Composition of the Pig Farmers’ Nasal Microbiota in a Season-Dependent and Farm-Specific Manner

Abstract

Prior studies have demonstrated an influence of the built environment on the human nasal microbiota. However, very little is known about the influences of working on a pig farm on the human nasal microbiota. We longitudinally collected samples from 30 pig farms (air and nasal swabs from humans and pigs) in Switzerland from 2014 to 2015. As controls, nasal swabs from cow farmers and individuals with no contact with farm animals were included. An analysis of the microbiota for all samples (n = 609) was performed based on 16S rRNA gene sequencing (MiSeq) and included the investigations of source-sink dynamics. The numbers of indoor airborne particles and bacterial loads in pig farms were also investigated and were highest in winter. Similarly, the microbiota analyses revealed that the alpha diversity values of the nares of pig farmers were increased in winter in contrast to those of samples from the nonexposed controls, which displayed low alpha diversity values throughout the seasons. Source-sink analyses revealed that bacteria from the noses of pigs are more commonly coidentified within the pig farmers' microbiota in winter but to a less extent in summer. In addition, in winter, there was a stronger intrasimilarity for samples that originated from the same farm than for samples from different farms, and this farm specificity was partially or completely lost in spring, summer, and fall. In conclusion, in contrast to nonexposed controls, a pig farmer’s nasal microbiota is dynamic, as the indoor-air microbiota of pig farms drives the composition of the pig farmer’s nasal microbiota in a season-dependent manner. IMPORTANCE The airborne microbiota of pig farms poses a potential health hazard and impacts both livestock and humans working in this environment. Therefore, a more thorough understanding of the microbiota composition and dynamics in this setting is needed. This study was of a prospective design (12 months) and used samples from different sites. This means that the microbiota of air, animals (pigs), and humans was simultaneously investigated. Our findings highlight that the potential health hazard might be particularly high in winter compared to that in summer.

Relationships among Fecal, Air, Oral, and Tracheal Microbial Communities in Pigs in a Respiratory Infection Disease Model

“…Despite great heterogeneity, the air microbial community was more closely related to that of the trachea, hence, the estimated proportion for air as a source was greater than that inferred for feces and oral fluids. However, the distribution of the proportions was different from that observed in previous research [ 31 ], in which the inferred contribution of air as a source of the nasal microbiome in pigs and workers was higher than 40% throughout the year. Those differences could stem from the fact that Kraemer, Aebi, Oppliger, and Hilty [ 31 ] sampled the upper respiratory tract of pigs instead of the lower respiratory tract, as in this study.…”

“…Recently, researchers strived to characterize the microbiome of the environment of swine facilities [ 31 , 32 , 33 , 34 ]. The air microbiome is of special interest as it may serve as an epidemiological vehicle for the transmission of microorganisms between different environments.…”

Investigation of the human nasal microbiome in persons with long- and short-term exposure to methicillin-resistant Staphylococcus aureus and other bacteria from the pig farm environment

“…In addition, there were no statistically significant associations between nasal bacterial community composition at the CST level and the MRSA status in the 64 nasal swabs (P > 0.05 by Fisher's exact test) ( Table 4). The former finding is in line with previous studies showing that exposure to the pig farm environment affects the nasal microbiome of pig farm workers at work [38,39]. Interestingly, CST2 was present in some pig farm workers (e.g., subjects 1, 6, 14, and 16) up to four days after their last workday (S1 Fig), supporting that they may carry these bacteria for long periods and thus serve as a hub for the spread of pathogens from the pig farm environment to other animals and farms as well as to their households and the general population.…”

“…Interestingly, CST1 and CST2 had low proportions of S. aureus (<0.5% of each community). The widespread distribution and abundance of Pseudomonas and Acinetobacter, which both belong to the order Pseudomonadales, as well as the low abundance of S. aureus, is reminiscent of previously published studies of the microbial diversity in the pig nose [34][35][36][37][38][39]. In contrast, CST3, CST4, and CST5 were dominated by the genera Moraxella (44% of the community), Corynebacterium (30% of the community), and Staphylococcus (40% of the community), respectively, which are known members of nasal bacterial communities present in the general human population [5,[40][41][42].…”

Turning the Lungs Inside Out: The Intersecting Microbiomes of the Lungs and the Built Environment

“…These environmental microbiomes are influenced by geography, season, outside air, building ventilation, and the animals and humans that inhabit the space ( 12 , 13 ). The environmental microbiome contributes to the skin, nasal, and oral microbiota of its occupants ( 14 , 15 ) and has been correlated with differences in health outcomes, including respiratory disease ( 16 ). Surprisingly, these fields have not yet intersected.…”