Salmonella vaccines used in poultry in the EU are based on attenuated strains of either Salmonella serovar Enteritidis or Typhimurium which results in a decrease in S. Enteritidis and S. Typhimurium but may allow other Salmonella serovars to fill an empty ecological niche. In this study we were therefore interested in the early interactions of chicken immune system with S. Infantis compared to S. Enteritidis and S. Typhimurium, and a role of O-antigen in these interactions. To reach this aim, we orally infected newly hatched chickens with 7 wild type strains of Salmonella serovars Enteritidis, Typhimurium and Infantis as well as with their rfaL mutants and characterized the early Salmonella-chicken interactions. Inflammation was characterized in the cecum 4 days post-infection by measuring expression of 43 different genes. All wild type strains stimulated a greater inflammatory response than any of the rfaL mutants. However, there were large differences in chicken responses to different wild type strains not reflecting their serovar classification. The initial interaction between newly-hatched chickens and Salmonella was found to be dependent on the presence of O-antigen but not on its structure, i.e. not on serovar classification. In addition, we observed that the expression of calbindin or aquaporin 8 in the cecum did not change if inflammatory gene expression remained within a 10 fold fluctuation, indicating the buffering capacity of the cecum, preserving normal gut functions even in the presence of minor inflammatory stimuli.

Veterinary Research Institute Brno Czech Republic

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Lahuerta A, Westrell T, Takkinen J, Boelaert F, Rizzi V, et al. (2011) Zoonoses in the European Union: origin, distribution and dynamics - the EFSA-ECDC summary report 2009. Euro Surveill 16: 19832. PubMed

Kohl KS, Farley TA (2000) Initially unrecognized distribution of a commercially cooked meat product contaminated over several months with Salmonella serotype Infantis. Epidemiol Infect 125: 491–8. PubMed PMC

Najjar Z, Furlong C, Stephens N, Shadbolt C, Maywood P, et al. (2012) An outbreak of Salmonella Infantis gastroenteritis in a residential aged care facility associated with thickened fluids. Epidemiol Infect 140: 2264–72. PubMed PMC

Berndt A, Wilhelm A, Jugert C, Pieper J, Sachse K, et al. (2007) Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect Immun 75: 5993–6007. PubMed PMC

Matulova M, Havlickova H, Sisak F, Rychlik I (2012) Vaccination of chickens with Salmonella Pathogenicity Island (SPI) 1 and SPI2 defective mutants of Salmonella enterica serovar Enteritidis. Vaccine 30: 2090–7. PubMed

Setta AM, Barrow PA, Kaiser P, Jones MA (2012) Early immune dynamics following infection with Salmonella enterica serovars Enteritidis, Infantis, Pullorum and Gallinarum: cytokine and chemokine gene expression profile and cellular changes of chicken cecal tonsils. Comp Immunol Microbiol Infect Dis 35: 397–410. PubMed

Matulova M, Varmuzova K, Sisak F, Havlickova H, Babak V, et al. (2013) Chicken innate immune response to oral infection with Salmonella enterica serovar Enteritidis. Vet Res 44: 37. PubMed PMC

Matulova M, Rajova J, Vlasatikova L, Volf J, Stepanova H, et al. (2012) Characterization of chicken spleen transcriptome after infection with Salmonella enterica serovar Enteritidis. PLoS One 7: e48101. PubMed PMC

Guard-Petter J, Keller LH, Rahman MM, Carlson RW, Silvers S (1996) A novel relationship between O-antigen variation, matrix formation, and invasiveness of Salmonella enteritidis . Epidemiol Infect 117: 219–31. PubMed PMC

Crhanova M, Malcova M, Mazgajova M, Karasova D, Sebkova A, et al. (2011) LPS structure influences protein secretion in Salmonella enterica . Vet Microbiol 152: 131–7. PubMed

Coward C, Sait L, Cogan T, Humphrey TJ, Maskell DJ (2013) O-antigen repeat number in Salmonella enterica serovar Enteritidis is important for egg contamination, colonisation of the chicken reproductive tract and survival in egg albumen. FEMS Microbiol Lett 343: 169–76. PubMed

Zhang S, Adams LG, Nunes J, Khare S, Tsolis RM, et al. (2003) Secreted effector proteins of Salmonella enterica serotype typhimurium elicit host-specific chemokine profiles in animal models of typhoid fever and enterocolitis. Infect Immun 71: 4795–803. PubMed PMC

Komoriya K, Shibano N, Higano T, Azuma N, Yamaguchi S, et al. (1999) Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium . Mol Microbiol 34: 767–79. PubMed

Setta A, Barrow PA, Kaiser P, Jones MA (2012) Immune dynamics following infection of avian macrophages and epithelial cells with typhoidal and non-typhoidal Salmonella enterica serovars; bacterial invasion and persistence, nitric oxide and oxygen production, differential host gene expression, NF-kappaB signalling and cell cytotoxicity. Vet Immunol Immunopathol 146: 212–24. PubMed

Aabo S, Christensen JP, Chadfield MS, Carstensen B, Olsen JE, et al. (2002) Quantitative comparison of intestinal invasion of zoonotic serotypes of Salmonella enterica in poultry. Avian Pathol 31: 41–7. PubMed

Andrews-Polymenis HL, Rabsch W, Porwollik S, McClelland M, Rosetti C, et al. (2004) Host restriction of Salmonella enterica serotype Typhimurium pigeon isolates does not correlate with loss of discrete genes. J Bacteriol 186: 2619–28. PubMed PMC

Swords WE, Cannon BM, Benjamin WH Jr (1997) Avirulence of LT2 strains of Salmonella typhimurium results from a defective rpoS gene. Infect Immun 65: 2451–3. PubMed PMC

Wilmes-Riesenberg MR, Foster JW, Curtiss R III (1997) An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect Immun 65: 203–10. PubMed PMC

Spector MP (1998) The starvation-stress response (SSR) of Salmonella . Adv Microb Physiol 40: 233–79. PubMed

Karasova D, Sebkova A, Vrbas V, Havlickova H, Sisak F, et al. (2009) Comparative analysis of Salmonella enterica serovar Enteritidis mutants with a vaccine potential. Vaccine 27: 5265–70. PubMed

Trebichavsky I, Dlabac V, Rehakova Z, Zahradnickova M, Splichal I (1997) Cellular changes and cytokine expression in the ilea of gnotobiotic piglets resulting from peroral Salmonella typhimurium challenge. Infect Immun 65: 5244–9. PubMed PMC

Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640–5. PubMed PMC

Li YP, Bang DD, Handberg KJ, Jorgensen PH, Zhang MF (2005) Evaluation of the suitability of six host genes as internal control in real-time RT-PCR assays in chicken embryo cell cultures infected with infectious bursal disease virus. Vet Microbiol 110: 155–65. PubMed

De Boever S, Vangestel C, De Backer P, Croubels S, Sys SU (2008) Identification and validation of housekeeping genes as internal control for gene expression in an intravenous LPS inflammation model in chickens. Vet Immunol Immunopathol 122: 312–7. PubMed

Gene expression in the chicken caecum in response to infections with non-typhoid Salmonella