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ARS Home » Midwest Area » Ames, Iowa » National Animal Disease Center » Food Safety and Enteric Pathogens Research » Research » Publications at this Location » Publication #299239

Title: Gastrointestinal microbiota and porcine immunity: factors that influence salmonella shedding in swine

item Bearson, Shawn
item KNETTER, SUSAN - Iowa State University
item Allen, Heather
item Bearson, Bradley - Brad
item Brunelle, Brian
item HUANG, TING-HUA - Iowa State University
item Looft, Torey
item RAMER-TAIT, AMANDA - University Of Nebraska
item NETTLETON, DAN - Iowa State University
item Stanton, Thaddeus
item WANNEMUEHLER, MICHAEL - Iowa State University
item TUGGLE, CHRISTOPHER - Iowa State University

Submitted to: Meeting Abstract
Publication Type: Abstract Only
Publication Acceptance Date: 10/1/2013
Publication Date: 11/11/2013
Citation: Bearson, S.M., Knetter, S.M., Allen, H.K., Bearson, B.L., Brunelle, B.W., Huang, T., Looft, T.P., Ramer-Tait, A.E., Nettleton, D., Stanton, T.B., Wannemuehler, M.J., Tuggle, C.K. 2014. Gastrointestinal microbiota and porcine immunity: factors that influence salmonella shedding in swine [abstract]. In: Proceedings of Symposium on Gut Health in Production of Food Animals, Kansas City, Missouri, November 11-13, 2013. p. 12-13.

Interpretive Summary:

Technical Abstract: Pigs are often asymptomatically colonized with the human foodborne pathogen Salmonella and can exhibit notable variation in severity and duration of Salmonella fecal shedding. Multiple factors impact the dynamics of Salmonella in swine, including features of the microorganism, responses from the pig, and contributions from the gastrointestinal microbiota. To characterize the immune capacity and intestinal microbiota in swine before and after Salmonella challenge, 54 cohabitating, crossbred pigs from multiple litters were intranasally-inoculated with an equal dose of Salmonella enterica serovar Typhimurium (1 X 109 cfu); non-inoculated (NI) littermates were housed separately. Bacterial quantitation of Salmonella in swine feces over the 21-day study was performed, and the cumulative AULC was calculated to classify 8 low shedder (LS) and 8 persistent shedder (PS) pigs. Serum cytokine analysis and transcriptional profiling of blood RNA from the two shedding groups detected distinct immune responses within two days post-challenge: elevated serum IL-1b, TNF-a, and IFN-g was observed in the PS pigs compared to LS pigs, while LS pigs had greater serum CXCL8 than PS pigs. PS pigs up-regulated genes involved with STAT1, IFNB1 and IFNG networks, while up-regulation of genes involved in immune response regulation were detected only in LS pigs. Furthermore, an ex vivo endotoxin stimulation assay of whole blood from the PS and LS pigs revealed an attenuated inflammatory response in the LS pigs. To examine the influence of the gastrointestinal microbiota on Salmonella shedding, the microbial communities were evaluated using a smaller subset of the extreme shedding groups (n=5 pigs/group) as well as the NI control group. Total fecal DNA was isolated for 16S rRNA gene sequencing at 0, 2, 7 and 21 days post-challenge. Prior to inoculating the pigs with Salmonella, “will-be” LS pigs and “will-be” PS pigs had differences in their microbiotas, including a higher abundance of the Ruminococcaceae family in the “will-be” LS pigs. Following Salmonella challenge, PS pigs had dramatic changes in their microbial communities compared to LS pigs; no differences were detected between LS and NI pigs. However, by 21 days post-challenge, the microbiota communities of LS and PS pigs were no longer different from one another, but were both different from NI pigs, suggesting that introducing S. Typhimurium into the porcine gastrointestinal tract altered maturation of the microbiota regardless of shedding status. The data indicate significant correlations between Salmonella shedding in pigs with both the porcine immune response as well as shifts in the gastrointestinal microbiota, thereby broadening our appreciation of the complex host-microbe-microbiota relationship for this important food safety and public health issue.