Changes in Peyer's Patch and Cecal Tonsil B Lymphocytes in Laying Hens Following Challenge with Salmonella enterica Serovar Enteritidis


Authors

  • Peter S. Holt USDA/ARS Egg Safety and Quality Research Unit, 950 College Station Road, Athens, Georgia 30605, USA
  • Lara E. Vaughn USDA/ARS Egg Safety and Quality Research Unit, 950 College Station Road, Athens, Georgia 30605, USA
  • Richard K. Gast USDA/ARS Egg Safety and Quality Research Unit, 950 College Station Road, Athens, Georgia 30605, USA

DOI:

https://doi.org/10.3923/ijps.2011.231.237

Keywords:

Cecal tonsils, peyer`s patches, Salmonella enterica

Abstract

Two trials were conducted to determine B cell changes in Peyer’s Patches (PP) and Cecal Tonsils (CT) of specific-pathogen-free Single Comb White Leghorn hens challenged with Salmonella enterica Serovar Enteritidis (SE). Prior to challenge and then weekly post challenge, 4 or 3 hens in Trials 1 and 2, respectively, were sacrificed and their intestinal tracts excised. Cells were purified from proximal and distal PP along with both CT and then aliquots of cells were incubated with antibodies to chicken immunoglobulins IgM, IgG and IgA. The B cells expressing the different immunoglobulin isotopes were identified via flow cytometric analysis. B lymphocytes expressing IgM were most prevalent, representing 40-60% and 30-50% of CT and PP B cells, respectively, while 20-30% of CT and PP lymphocytes expressed IgA. Only a small percentage of CT and PP lymphocytes, <10%, expressed IgG. Significantly more IgM+ cells were detected in CT vs proximal and distal PP and proximal PP in trials 1 and 2, respectively. Significantly more IgA+ cells were observed in proximal PP vs distal PP and CT in trial 1 but not in trial 2. Following SE infection, these differences were no longer observed. For IgG+ cells, however, no significant differences between tissues were observed prior to challenge but significantly more IgG+ cells were observed in both PP vs CT at weeks 1 and 3 post challenge in trial 1 and week 1 post challenge in trial 2. These results indicate that B lymphocyte differences do occur in PP vs CT in adult chickens and these populations can change in response to stimuli such as intestinal infection.

References

Barrow, P.A., M.B. Huggins, M.A. Lovell and J.M. Simpson, 1987. Observations on the pathogenesis of experimental Salmonella typhimurium infection in chickens. Res. Vet. Sci., 42: 194-199.

Barrow, P.A., J.M. Simpson and M.A. Lovell, 1988. Intestinal colonization in the chicken by food-poisoning Salmonella serotypes: Microbial characteristics associated with faecal excretion. Avian Pathol., 17: 571-588.

Befus, A.D., N. Johnston, G.A. Leslie and J. Bienenstock, 1980. Gut-associated lymphoid tissue in the chicken. I. Morphology, ontogeny and some functional characteristics of Peyers patches. J. Immunol., 125: 2626-2632.

Berndt, A. and U. Methner, 2001. Gamma/delta T cell response of chickens after oral administration of attenuated and non-attenuated Salmonella typhimurium strains. Vet. Immunol. Immunopathol., 78: 143-161.

Berndt, A., A. Wilhelm, C. Jugert, J. Pieper, K. Sachse and U. Methner, 2007. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect. Immunity, 75: 5993-6007.

Braden, C.R., 2006. Salmonella enterica serotype Enteritidis and eggs: A national epidemic in the United States. Clin. Infect. Dis., 43: 512-517.

Burns, R.B., 1982. Histology and immunology of Peyer's patches in the domestic fowl (Gallus domesticus). Res. Vet. Sci., 32: 359-367.

Davison, F., K.E. Magor and B. Kaspers, 2008. Structure and Evolution of Avian Immunoglobulins. In: Avian Immunology, Davison, F., B. Kaspers, K.A. Schat and P. Kaiser (Eds.). Academic Press, London, UK., ISBN-13: 978-0123706348, pp: 117-118.

Densen, P. and G.L. Mandell, 1980. Phagocyte strategy vs. microbial tactics. Rev. Infect. Dis., 2: 817-838.

Gast, R.K., 2008. Paratyphoid Infections: Diseases of Poultry. Blackwell Publishing, Ames, Iowa, pp: 636-665.

Gast, R. and P. Holt, 1998. Persistence of Salmonella enteritidis from one day of age to maturity in experimentally infected layer chickens. Poult. Sci., 77: 1759-1762.

Hargis, B.M., D.J. Caldwell, R.L. Brewer, D.E. Corrier and J.R. DeLoach, 1995. Evaluation of the chicken crop as a source of Salmonella contamination for broiler carcasses. Poult. Sci., 74: 1548-1552.

Hassan, J.O., P.P.A. Mockett, D. Catty and P.A. Barrow, 1991. Infection and reinfection of chickens with Salmonella typhimurium: Bacteriology and immune responses. Avian Dis., 35: 809-819.

Holt, P.S., R.K. Gast, R.E. Jr. Porter and H.D. Stone, 1999. Hyporesponsiveness of the systemic and mucosal immune systems in chickens infected with Salmonella enterica serovar Enteritidis at one day of age. Poult. Sci., 78: 1510-1517.

Holt, P.S., L.E. Vaughn, R.K. Gast and H.D. Stone, 2002. Development of a lavage procedure to collect crop secretions from live chickens for studying crop immunity. Avian Pathol., 31: 589-592.

Holt, P.S., L.E. Vaughn and R.K. Gast, 2010. Flow cytometric characterization of Peyer's patch and cecal tonsil T lymphocytes in laying hens following challenge with Salmonella enterica serovar Enteritidis. Vet. Immuol. Immunopathol., 133: 276-281.

Keren, D.F., P.S. Holt, H.H. Collins, P. Gemski and S.B. Formal, 1978. The role of Peyer's patches in the local limmune response of rabbit ileum to live bacteria. J. Immunol., 120: 1892-1896.

Makala, L.H.C., N. Suzuki and H. Nagasawa, 2002. Peyer's patches: Organized lymphoid structures for the induction of mucosal immune responses in the intestine. Pathobiology, 70: 55-68.

Nencioni, L., L. Villa, D. Boraschi, B. Berti and A. Tagliabue, 1983. Natural and antibody-dependent cell-mediated activity against Salmonella typhimurium by peripheral and intestinal lymphoid cells in mice. J. Immunol., 130: 903-907.

O'Farrelly, C., D. Branton and C.A. Wanke, 1992. Oral ingestion of egg yolk immunoglobulin from hens immunized with an enterotoxigenic Escherichia coli strain prevents diarrhea in rabbits challenged with the same strain. Infect. Immun., 60: 2593-2597.

Rogers, H.J., 1973. Iron-binding catechols and virulence in Escherichia coli. Infect. Immun., 7: 445-456.

Rus, H., C. Cudrici and F. Niculescu, 2005. The role of the complement system in innate immunity. Immunol. Res., 33: 103-112.

Sasai, K., M. Aita, H.S. Lillehoj, T. Miyamoto, T. Fukata and E. Baba, 2000. Dynamics of lymphocyte subpopulation changes in the cecal tonsils of chickens infected with Salmonella enteritidis. Vet. Microbiol., 74: 345-351.

Sasai, K., K. Yoshimura, H.S. Lillehoj, G.S.K. Withanage, T. Fukata, E. Baba and A. Arakawa, 1997. Analysis of splenic and thymic lymphocyte subpopulations in chickens infected with Salmonella enteritidis. Vet. Immunol. Immunopathol., 59: 359-367.

Schroeder, C.M., A.L. Naugle, W.D. Schlosser, A.T. Hogue and F.J. Angulo et al., 2005. Estimate of illnesses from Salmonella Enteritidis in eggs, United States, 2000. Emerg. Infect. Dis., 11: 113-115.

Shikina, T., T. Hiroi, K. Iwatani, M.H. Jang and S. Fukuyama et al., 2004. IgA class switch occurs in the organized nasopharynx-and gut-associated lymphoid tissue but not in the diffuse lamina propria of airways and gut. J. Immunol., 172: 6259-6264.

Stavnezer, J. and C.T. Amemiya, 2004. Evolution of isotype switching. Seminars Immunol., 16: 257-275.

Swaggerty, C.L., P.J. Ferro, I.Y. Pevzner and M.H. Kogut, 2005. Heterophils are associated with resistance to systemic Salmonella enteritidis infections in genetically distinct chicken lines. FEMS Immunol. Med. Microbiol., 43: 149-154.

Van Hemert, S., A.J.W. Hoekman, M.A. Smits and J.M.J. Rebel, 2007. Immunological and gene expression responses to a Salmonella infection in the chicken intestine. Vet. Res., 38: 51-63.

Vaughn, L.E., P.S. Holt, R.W. Moore and R.K. Gast, 2006. Enhanced gross visualization of chicken Peyer's patch: Novel staining technique applied to fresh tissue specimens. Avian Dis., 50: 298-302.

Downloads

Published

2011-02-15

Issue

Section

Research Article

How to Cite

Holt, P. S., Vaughn, L. E., & Gast, R. K. (2011). Changes in Peyer’s Patch and Cecal Tonsil B Lymphocytes in Laying Hens Following Challenge with Salmonella enterica Serovar Enteritidis. International Journal of Poultry Science, 10(3), 231–237. https://doi.org/10.3923/ijps.2011.231.237