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Towards an understanding of Salmonella enterica serovar Typhimurium persistence in swine

Published online by Cambridge University Press:  03 February 2017

Sheila K. Patterson ,
Hyeun Bum Kim ,
Klaudyna Borewicz  and
Richard E. Isaacson
Sheila K. Patterson
Affiliation:
Department of Pathobiology, University of Illinois, Urbana, IL 61801, USA
Hyeun Bum Kim
Affiliation:
Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN 55108, USA
Klaudyna Borewicz
Affiliation:
Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN 55108, USA
Richard E. Isaacson*
Affiliation:
Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN 55108, USA
*
*Corresponding author. E-mail: [email protected]
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Abstract

Salmonella enterica is an important food borne pathogen that is frequently carried by swine. Carrier animals pose a food safety risk because they can transmit S. enterica to finished food products in the processing plant or by contamination of the environment. Environmental contamination has become increasingly important as non-animal foods (plant-based) have been implicated as sources of S. enterica. The prevalence of S. enterica in swine is high and yet carrier animals remain healthy. S. enterica has developed a highly sophisticated set of virulence factors that allow it to adapt to host environments and to cause disease. It is assumed that S. enterica also has developed unique ways to maintain itself in animals and yet not cause disease. Here we describe our research to understand persistence. Specifically, data are presented that demonstrates that detection of most carrier animals requires specific stresses that cause S. enterica to be shed from pigs. As well, we describe a phenotypic phase variation process that appears to be linked to the carrier state and a complex set of factors that control phenotypic phase variation. Finally, we describe how the composition of the gut bacterial microbiome may contribute to persistence and at the least how S. enterica might alter the composition of the gut bacterial microbiome.

Keywords

Salmonellacarrierphase variationtransportation stressvirulencemicrobiomeLawsoniaswine
Type
Review Article
Information
Animal Health Research Reviews , Volume 17 , Issue 2 , December 2016 , pp. 159 - 168
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

† Current Address: HBK, Department of Animal Resources, Dankook University, Dandae-ro 119 Cheonan 330-714, South Korea.
‡ Current Address: KB, Stippeneng 4, 6708 WE, Wageningen, The Netherlands.

References

Althouse, C, Patterson, S, Fedorka-Cray, P and Isaacson, RE (2003). Type 1 Fimbriae of Salmonella enterica Serovar Typhimurium bind to enterocytes and contribute to colonization of swine in vivo. Infection and Immunity 71: 6446–6452.CrossRefGoogle ScholarPubMed
Anonymous (2009). Salmonella on U.S. Swine Site – Prevalence and Antimicrobial Susceptibility. USDA, APHIS, Veterinary Services, Center for Epidemiology and Animal Health, Fort Collins, CO.Google Scholar
Bahnson, PB, Damman, DJ, Isaacson, RE, Miller, GY, Weigel, RM and Troutt, HF (2006a). Prevalence and serovars of Salmonella enterica isolated from ileocolic lymph nodes of market pigs reared in selected Midwest US swine herds. Journal of Swine Health and Production 14: 182–188.Google Scholar
Bahnson, PB, Fedorka-Cray, PJ, Ladely, SR and Mateus-Pinilla, NE (2006b). Herd-level risk factors for Salmonella enterica subsp. enterica in U.S. market pigs. Preventive Veterinary Medicine 76: 249–262.Google Scholar
Batz, MB, Hoffmann, S and Morris, JG Jr (2011). Ranking the risks: the 10 pathogen-food combinations with the greatest burden on public health. In Emerging Pathogens Institute. Gainesville, FL: University of Florida, pages 1–68.Google Scholar
Bean, NH and Griffin, PM (1990). Foodborne disease outbreaks in the United States, 1973–1987: pathogens, vehicles, and trends. Journal of Food Protection 53: 804–817.CrossRefGoogle ScholarPubMed
Beloeil, PA, Fravalo, P, Fablet, C, Jolly, JP, Eveno, E, Hascoet, Y, Chauvin, C, Salvat, G and Madec, F (2004). Risk factors for Salmonella enterica subsp. enterica shedding by market-age pigs in French farrow-to-finish herds. Preventive Veterinary Medicine 63: 103–120.Google Scholar
Borewicz, KA, Kim, HB, Singer, RS, Gebhart, CJ, Sreevatsan, S, Johnson, T and Isaacson, RE (2015). Changes in the porcine intestinal microbiome in response to infection with Salmonella enterica and Lawsonia intracellularis . PLoS ONE 10: e0139106.Google Scholar
Brendan, RJ, Patricia, MG, Dana, C, Kelly, AW and Shua, JC (2013). Outbreak-associated Salmonella enterica serotypes and food commodities, United States, 1998–2008. Emerging Infectious Disease Journal 19: 1239.Google Scholar
Brinton, CC (1959). Non-flagellar appendages of bacteria. Nature 183: 782–786.Google Scholar
Brown, L and Elliott, T (1996). Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. Journal of Bacteriology 178: 3763–3770.CrossRefGoogle ScholarPubMed
Broz, P, Ohlson, MB and Monack, DM (2012). Innate immune response to Salmonella typhimurium, a model enteric pathogen. Gut Microbes 3: 62–70.CrossRefGoogle ScholarPubMed
Bryan, FL (1988). Risk of practices, procedures and processes that lead to outbreaks of foodborne disease. Journal of Food Protection 51: 663–667.Google Scholar
Carter, PB and Collins, FM (1974). The route of enteric infection in normal mice. Journal of Experimental Medicine 139: 1189–1203.CrossRefGoogle ScholarPubMed
(CDC) CFDCaP (2013). An Atlas of Salmonella in the United States, 1968–2011: Laboratory-based Enteric Disease Surveillance. Atlanta, GA: US Department of Health and Human Services, CDC.Google Scholar
Coburn, B, Sekirov, I and Finlay, BB (2007). Type III secretion systems and disease. Clinical Microbiology Reviews 20: 535–549.CrossRefGoogle ScholarPubMed
Cunning, C and Elliott, T (1999). RpoS synthesis is growth rate regulated in Salmonella typhimurium, but its turnover is not dependent on acetyl phosphate synthesis or PTS function. Journal of Bacteriology 181: 4853–4862.Google Scholar
Efsa (2012). Scientific opinion on an estimation of the public health impact of setting a new target for the reduction of Salmonella in turkeys. EFSA Journal 10: 2616.Google Scholar
Eisenstein, BI (1981). Phase variation of type 1 fimbriae in Escherichia coli is under transcriptional control. Science 214: 337–339.CrossRefGoogle ScholarPubMed
Elliott, T and Roth, JR (1988). Characterization of Tn10d-Cam: a transposition-defective Tn10 specifying chloramphenicol resistance. Molecular and General Genetics 213: 332–338.CrossRefGoogle ScholarPubMed
Fedorka-Cray, PJ, Kelley, LC, Stabel, TJ, Gray, JT and Laufer, JA (1995). Alternate routes of invasion may affect pathogenesis of Salmonella typhimurium in swine. Infection and Immunity 63: 2658–2664.CrossRefGoogle ScholarPubMed
Ganesh, BP, Klopfleisch, R, Loh, G and Blaut, M (2013). Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella typhimurium-infected gnotobiotic mice. PLoS ONE 8: e74963.CrossRefGoogle ScholarPubMed
Garcia-Quintanilla, M and Casadesus, J (2011). Virulence plasmid interchange between strains ATCC 14028, LT2, and SL1344 of Salmonella enterica serovar Typhimurium. Plasmid 65: 169–175.CrossRefGoogle ScholarPubMed
Henderson, IR, Owen, P and Nataro, JP (1999). Molecular switches – the ON and OFF of bacterial phase variation. Molecular Microbiology 33: 919–932.Google Scholar
Hensel, M (2000). Salmonella pathogenicity island 2. Molecular Microbiology 36: 1015–1023.Google Scholar
Hohmann, AW, Schmidt, G and Rowley, D (1978). Intestinal colonization and virulence of Salmonella in mice. Infection and Immunity 22: 763–770.Google Scholar
Hoiseth, SK and Stocker, BA (1981). Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238–239.Google Scholar
Huang, TH, Uthe, JJ, Bearson, SM, Demirkale, CY, Nettleton, D, Knetter, S, Christian, C, Ramer-Tait, AE, Wannemuehler, MJ and Tuggle, CK (2011). Distinct peripheral blood RNA responses to Salmonella in pigs differing in Salmonella shedding levels: intersection of IFNγ, TLR and miRNA pathways. PloS ONE 6: e28768.Google Scholar
Hurd, HS, Mckean, JD, Griffith, RW, Wesley, IV and Rostagno, MH (2002). Salmonella enterica infections in market swine with and without transport and holding. Applied and Environmental Microbiology 68: 2376–2381.Google Scholar
Isaacson, RE and Kinsel, M (1992). Adhesion of Salmonella typhimurium to porcine intestinal epithelial surfaces: identification and characterization of two phenotypes. Infection and Immunity 60: 3193–3200.CrossRefGoogle ScholarPubMed
Isaacson, RE, Argyilan, C, Kwan, L, Patterson, S and Yoshinaga, K (1999a). Phase variable switching of in vivo and environmental phenotypes of Salmonella typhimurium . Advances in Experimental Biology 473: 281–289.Google Scholar
Isaacson, RE, Firkins, LD, Weigel, RM, Zuckermann, FA and Dipietro, JA (1999b). Effect of transportation and feed withdrawal on shedding of Salmonella typhimurium among experimentally infected pigs. American Journal of Veterinary Research 60: 1155–1158.Google Scholar
Jones, BD, Ghori, N and Falkow, S (1994). Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. Journal of Experimental Biology 180: 15–23.CrossRefGoogle ScholarPubMed
Klumpp, J and Fuchs, TM (2007). Identification of novel genes in genomic islands that contribute to Salmonella typhimurium replication in macrophages. Microbiology 153: 1207–1220.Google Scholar
Kwan, LY and Isaacson, RE (1998). Identification and characterization of a phase-variable nonfimbrial Salmonella typhimurium gene that alters o-antigen production. Infection and Immunity 66: 5725–5730.Google Scholar
Lostroh, CP and Lee, CA (2001). The Salmonella pathogenicity island-1 type III secretion system. Microbes and Infection 3: 1281–1291.CrossRefGoogle ScholarPubMed
Matthews, L, Low, JC, Gally, DL, Pearce, MC, Mellor, DJ, Heesterbeek, JAP, Chase-Topping, M, Naylor, SW, Shaw, DJ, Reid, SWJ, Gunn, GJ and Woolhouse, MEJ (2006). Heterogeneous shedding of Escherichia coli O157 in cattle and its implications for control. Proceedings of the National Academy of Sciences of the United States of America 103: 547–552.Google Scholar
Patterson, SK, Borewicz, K, Johnson, T, Xu, W and Isaacson, RE (2012). Characterization and differential gene expression between two phenotypic phase variants in Salmonella enterica Serovar Typhimurium. PLoS ONE 7: e43592.CrossRefGoogle ScholarPubMed
Penheiter, KL, Mathur, N, Giles, D, Fahlen, T and Jones, BD (1997). Non-invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroy M cells of ileal peyer's patches. Molecular Microbiology 24: 697–709.Google Scholar
Scallan, E, Hoekstra, RM, Angulo, FJ, Tauxe, RV, Widdowson, MA, Roy, SL, Jones, JL and Griffin, PM (2011). Foodborne illness acquired in the United States – major pathogens. Emerging Infectious Diseases 17: 7–15.CrossRefGoogle ScholarPubMed
Stecher, BR, Robbiani, R, Walker, AW, Westendorf, AM, Barthel, M, Kremer, M, Chaffron, S, Macpherson, AJ, Buer, J, Parkhill, J, Dougan, G, Von Mering, C and Hardt, W-D (2007). Serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5: e244.Google Scholar
Takeuchi, A (1967). Electron microscopic studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium . American Journal of Pathology 50: 109–136.Google Scholar
Troisfontaines, P and Cornelis, GR (2005). Type III secretion: more systems than you think. Physiology (Bethesda) 20: 326–339.Google Scholar
Wallis, TS and Galyov, EE (2000). Molecular basis of Salmonella-induced enteritis. Molecular Microbiology 36: 997–1005.CrossRefGoogle ScholarPubMed
Williams, LP and Newell, KW (1970). Salmonella excretion in joy-riding pigs. American Journal of Public Health 60: 926–929.Google Scholar
Winter, SE, Thiennimitr, P, Winter, MG, Butler, BP, Huseby, DL, Crawford, RW, Russell, JM, Bevins, CL, Adams, LG, Tsolis, RM, Roth, JR and Baumler, AJ (2010). Gut inflammation provides a respiratory electron acceptor for Salmonella . Nature 467: 426–429.Google Scholar
Wood, RL, Pospischil, A and Rose, R (1989). Distribution of persistent Salmonella typhimurium infection in internal organs of swine. American Journal of Veterinary Research 50: 1015–1021.Google Scholar