Porcine response to a multidrug-resistant Salmonella enterica serovar I 4,[5],12:i:- outbreak isolate

Authors: Shippy, Daniel; Bearson, Bradley - Brad; HOLMAN, DEVIN - Orise Fellow; Brunelle, Brian; Allen, Heather; Bearson, Shawn

Submitted to: Foodborne Pathogens and Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/3/2018
Publication Date: 5/1/2018
Citation: Shippy, D.C., Bearson, B.L., Holman, D.B., Brunelle, B.W., Allen, H.K., Bearson, S.M. 2018. Porcine response to a multidrug-resistant Salmonella enterica serovar I 4,[5],12:i:- outbreak isolate. Foodborne Pathogens and Disease. 15(5):253-261. https://doi.org/10.1089/fpd.2017.2378.
DOI: https://doi.org/10.1089/fpd.2017.2378

Interpretive Summary: Salmonella is a human and animal health concern. In recent years, many of the human foodborne outbreaks associated with Salmonella contamination of pork products have been caused by monophasic Salmonella strains (Salmonella strains that only express one flagellar gene instead of switching between two). In order to further understand the Salmonella strains associated with these outbreaks, we inoculated pigs with a monophasic Salmonella strain isolated from a 2015 outbreak in pork products. Pigs inoculated with the monophasic Salmonella isolate exhibited transient clinical disease as shown by increased body temperature, diarrhea, and interferon-gamma levels. Furthermore, monophasic Salmonella was able to colonize porcine intestinal tissues, was shed in the feces, and disrupted the normal microbial community that reside in the porcine intestinal tract (microbiota). Collectively, these data suggest monophasic Salmonella strains induce similar clinical symptoms in swine to other Salmonella strains, suggesting that increased virulence in the natural porcine host is not a likely reason for the increased prevalence of monophasic Salmonella contamination of pork products.

Technical Abstract: Salmonella enterica serovar I 4,[5],12:i:- has emerged as a common nontyphoidal Salmonella serovar to cause human foodborne illness. An interesting trait of serovar I 4,[5],12:i:- is it only expresses the fliC gene for bacterial motility (i.e. monophasic), while most Salmonella strains alternately express two flagellin genes (fliC and fljB). The goal of this study was to characterize the porcine response following inoculation with a multidrug-resistant (MDR) serovar I 4,[5],12:i:- isolate associated with a multistate pork outbreak to determine if the increased prevalence of serovar I 4,[5],12:i:- in swine is due to enhanced pathogenicity. Pigs were inoculated and subsequently evaluated for the ability of the isolate to cause disease, induce an immune response, and alter the fecal microbiota over a 7-day period. Pigs exhibited a significant increase in rectal temperature (fever) [P less than 0.01] and fecal moisture content (diarrhea) [P less than 0.05] at 2 days post-inoculation (d.p.i.) compared to pre-inoculation (day 0). Serum analyses revealed significantly increased IFN-gamma levels at 2 [P less than or equal to 0.0001] and 3 [P less than 0.01] d.p.i. compared to day 0, and antibodies against Salmonella LPS were present in all pigs by 7 d.p.i. Serovar I 4,[5],12:i:- colonized porcine intestinal tissues and was shed in the feces throughout the 7-day study. Analysis of the 16S rRNA gene sequences demonstrated that the fecal microbiota was significantly altered following MDR serovar I 4,[5],12:i:- inoculation, with the largest shift observed between 0 and 7 d.p.i. Our data indicate that the pork outbreak-associated MDR serovar I 4,[5],12:i:- isolate induced transient clinical disease in swine and perturbed the gastrointestinal microbial community. The porcine response to MDR serovar I 4,[5],12:i:- is similar to previous studies with virulent biphasic S. Typhimurium, suggesting that the absence of fljB does not substantially alter acute colonization or pathogenesis in pigs.