Salmonella is a ubiquitous pathogen which, in addition to causing poultry diseases, has a growing zoonotic impact. It has demanded the implementation of diverse control strategies, in which vaccines play a major role. The understanding of the immune pathways elicited by the different vaccines is important, contributing for the establishment of strong immune correlates of protection, for instance. With the purpose of determining the dynamics of the humoral and cellular immune responses to vaccination, broiler breeders (Cobb Slow) were immunized with live or inactivated vaccines against Salmonella Enteritidis. Lymphocyte and macrophage subsets were analyzed in the peripheral blood by flow cytometry and antigen-specific circulating IgY and mucosal IgA were quantified. The markers analyzed by flow cytometry were CD8/CD28, CD4/TCRVβ1, Kul/ MHC II and Bu-1. Both live and inactivated vaccines induced an increase in the proportion of circulating monocytes (Kul + MHCII + ) in some time points compared to non-vaccinated controls. However, whereas the live vaccine leads to an increase in CD8 - CD28 + and Bu-1 + lymphocytescompared to the control group, the inactivated vaccine prompteda reduction in the percentage of severalleucocyte subsets (Kul - MHCII + , Bu-1 + , CD8 + CD28 + , CD8 - CD28 + , CD4 + TCRVβ1 - , CD4 + TCRVβ1 + , CD4 - TCRVβ1 + ) after the boost dose. Both vaccines induced specific serum IgY and mucosal IgA production; however, the inactivated vaccine stimulated higher titers in a shorter period. These results contribute to the understanding of mechanisms of action of live and inactivated Salmonella vaccines in chickens.
Keywords<i>Salmonella</i>EnteritidisHumoral and Cellular ImmunityLive VaccineBacterinBroiler Breeders
EFSA (2014) The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food- Borne Outbreaks in 2012. EFSA Journal, 12, 3547-3859.
Baú, A.C., Carvalhal, J.B. and Aleixo, J.A.G. (2001) Prevalência de Salmonella em produtos de frangos e ovos de galinha comercializados em Pelotas, RS, Brasil. Ciência Rural, 31, 303-307. http://dx.doi.org/10.1590/S0103-84782001000200018
Tessari, E.N.C., Cardoso, A.L.S.P., de Castro, A.G.M. and Zanatta, G.F. (2003) Prevalência de Salmonella enteritidis em carcaças de frango industrialmente processadas. Higiene Alimentar, 17, 52-55.
Santos, D.M.S., Berchieri Jr., A., Fernandes, S.A., Tavechio, A.T. and do Amaral, L.A. (2000) Salmonella em carcaças de frango congeladas. Pesquisa Veterinária Brasileira, 20, 39-42. http://dx.doi.org/10.1590/S0100-736X2000000100005
Vaz, C.S.L., Streck, A.F., Michael, G.B., Marks, F.S., Rodrigues, D.P., dos Reis, E.M.F., Cardoso, M.R.I. and Canal, C.W. (2010) Antimicrobial Resistance and Subtyping of Salmonella enterica Subspecies Enterica Serovar Enteritidis Isolated from Human Outbreaks and Poultry in Southern Brazil. Poultry Science, 89, 1530-1536. http://dx.doi.org/10.3382/ps.2009-00453
Kottwitz, L.B.M., de Oliveira, T.C.R.M., Alcocer, I., Farah, S., Abrahão, W.M. and dos Prazeres Rodrigues, D. (2009) Avaliação epidemiológica de surtos de salmonelose ocorridos no período de 1999 a 2008 no Estado do Paraná, Brasil. Acta Scientiarum, Health Science, 32, 9-15.
EFSA (2004) Opinion of the Scientific Panel on Biological Hazards on a Request from the Commission Related to the Use of Vaccines for the Control of Salmonella in Poultry. EFSA Journal, 114, 1-74.
Gantois, I., Ducatelle, R., Timbermont, L., Boyen, F., Bohez, L., Haesebrouck, F., Pasmans, F. and van Immerseel, F. (2006) Oral Immunisation of Laying Hens with the Live Vaccine Strains of TAD Salmonella vac E and TAD Salmonella vac T Reduces Internal Egg Contamination with Salmonella Enteritidis. Vaccine, 24, 6250-6255. http://dx.doi.org/10.1016/j.vaccine.2006.05.070
Chacana, P.A. and Terzolo, H.R. (2006) Protection Conferred by a Live Salmonella Enteritidis Vaccine against Fowl Typhoid in Laying Hens. Avian Diseases, 50, 280-283. http://dx.doi.org/10.1637/7463-102705R.1
Johnston, C.E., Hartley, C., Salisbury, A.-M. and Wigley, P. (2012) Immunological Changes at Point-of-Lay Increase Susceptibility to Salmonella enterica Serovar Enteritidis Infection in Vaccinated Chickens. PloS One, 7, e48195. http://dx.doi.org/10.1371/journal.pone.0048195
Wisner, A.L.S., Desin, T.S., Lam, P.K.S., Berberov, E., Mickael, C.S., Townsend, H.G., Potter, A.A. and Köster, W. (2011) Immunization of Chickens with Salmonella enterica Subspecies enterica Serovar Enteritidis Pathogenicity Island-2 Proteins. Veterinary Microbiology, 153, 274-284. http://dx.doi.org/10.1016/j.vetmic.2011.05.041
Zhang-Barber, L., Turner, A.K. and Barrow, P.A. (1999) Vaccination for Control of Salmonella in Poultry. Vaccine, 17, 2538-2545. http://dx.doi.org/10.1016/S0264-410X(99)00060-2
Crhanova, M., Hradecka, H., Faldynova, M., Matulova, M., Havlickova, H., Sisak, F. and Rychlik, I. (2011) Immune Response of Chicken Gut to Natural Colonization by Gut Microflora and to Salmonella enterica Serovar Enteritidis Infection. Infection and Immunity, 79, 2755-2763. http://dx.doi.org/10.1128/IAI.01375-10
Fernandes Filho, T., Fávaro Jr., C., Ingberman, M., Beirão, B.C.B., Zanata, S.M., Caron, L.F., Inoue, A. and Gomes, L. (2013) Effect of Spray E. coli Vaccine on the Immunity of Poultry. Avian Diseases, 57, 671-676. http://dx.doi.org/10.1637/10456-112612-ResNote.1
Engvall, E. and Perlmann, P. (1972) Enzyme-Linked Immunosorbent Assay, ELISA III. Quantitation of Specific Antibodies by Enzyme-Labeled Anti-Immunoglobulin in Antigen-Coated Tubes. The Journal of Immunology, 109, 129- 135.
Van Immerseel, F., De Buck, J., De Smet, I., Mast, J., Haesebrouck, F. and Ducatelle, R. (2002) Dynamics of Immune Cell Infiltration in the Caecal Lamina Propria of Chickens after Neonatal Infection with a Salmonella enteritidis Strain. Developmental & Comparative Immunology, 26, 355-364. http://dx.doi.org/10.1016/S0145-305X(01)00084-2
Marietto-Gonçalves, G.A., Curotto, S.M.R., Salgado, B.S., Milbradt, E.L. and Andreatti Filho, R.L. (2012) Leucometric Analysis of 1-Day-Old Chicks Inoculated with Salmonella typhimurium or lactobacilli. Comparative Clinical Pathology, 21, 1617-1621. http://dx.doi.org/10.1007/s00580-011-1336-y
Chappell, L., Kaiser, P., Barrow, P., Jones, M.A., Johnston, C. and Wigley, P. (2009) The Immunobiology of Avian Systemic Salmonellosis. Veterinary Immunology and Immunopathology, 128, 53-59. http://dx.doi.org/10.1016/j.vetimm.2008.10.295
Asheg, A.A., Levkut, M., Revajová, V., Evaíková, Z., Kolodzieyski, L. and Pistl, J. (2003) Dynamics of Lymphocyte Subpopulations in Immune Organs of Chickens Infected with Salmonella enteritidis. Acta Veterinaria Brunensis, 72, 359-364. http://dx.doi.org/10.2754/avb200372030359
Pawelec, G., Akbar, A., Caruso, C., Effros, R., Grubeck-Loebenstein, B. and Wikby, A. (2004) Is Immunosenescence Infectious? Trends in Immunology, 25, 406-410. http://dx.doi.org/10.1016/j.it.2004.05.006
Nabeshima, S., Murata, M., Kikuchi, K., Ikematsu, H., Kashiwagi, S. and Hayashi, J. (2002) A Reduction in the Number of Peripheral CD28+CD8+T Cells in the Acute Phase of Influenza. Clinical & Experimental Immunology, 128, 339- 346. http://dx.doi.org/10.1046/j.1365-2249.2002.01819.x
Olsson, J., Wikby, A., Johansson, B., Löfgren, S., Nilsson, B.-O. and Ferguson, F.G. (2001) Age-Related Change in Peripheral Blood T-Lymphocyte Subpopulations and Cytomegalovirus Infection in the Very Old: The Swedish Longitudinal OCTO Immune Study. Mechanisms of Ageing and Development, 121, 187-201. http://dx.doi.org/10.1016/S0047-6374(00)00210-4
Lundin, B.S., Johansson, C. and Svennerholm, A.-M. (2002) Oral Immunization with a Salmonella enterica Serovar Typhi Vaccine Induces Specific Circulating Mucosa-Homing CD4+ and CD8+ T Cells in Humans. Infection and Immunity, 70, 5622-5627. http://dx.doi.org/10.1128/IAI.70.10.5622-5627.2002
Carvajal, B.G., Methner, U., Pieper, J. and Berndt, A. (2008) Effects of Salmonella enterica Serovar Enteritidis on Cellular Recruitment and Cytokine Gene Expression in Caecum of Vaccinated Chickens. Vaccine, 26, 5423-5433. http://dx.doi.org/10.1016/j.vaccine.2008.07.088
Fukutome, K., Watarai, S., Mukamoto, M. and Kodama, H. (2001) Intestinal Mucosal Immune Response in Chickens Following Intraocular Immunization with Liposome-Associated Salmonella enterica Serovar Enteritidis Antigen. Developmental & Comparative Immunology, 25, 475-484. http://dx.doi.org/10.1016/S0145-305X(01)00014-3
Beal, R.K., Powers, C., Wigley, P., Barrow, P.A. and Smith, A.L. (2004) Temporal Dynamics of the Cellular, Humoral and Cytokine Responses in Chickens during Primary and Secondary Infection with Salmonella enterica Serovar Typhimurium. Avian Pathology, 33, 25-33. http://dx.doi.org/10.1080/03079450310001636282
Barrow, P.A. (2007) Salmonella Infections: Immune and Non-Immune Protection with Vaccines. Avian Pathology, 36, 1-13. http://dx.doi.org/10.1080/03079450601113167
Muir, W.I., Bryden, W.L. and Husband, A.J. (1998) Evaluation of the Efficacy of Intraperitoneal Immunization in Reducing Salmonella typhimurium Infection in Chickens. Poultry Science, 77, 1874-1883. http://dx.doi.org/10.1093/ps/77.12.1874
Beirão, B.C.B., Fávaro Jr., C., Nakao, L.S., Caron, L.F., Zanata, S.M. and Mercadante, A.F. (2012) Flow Cytometric Immune Profiling of Specific-Pathogen-Free Chickens before and after Infectious Challenges. Veterinary Immunology and Immunopathology, 145, 32-41. http://dx.doi.org/10.1016/j.vetimm.2011.10.004
Holt, P.S., Vaughn, L.E. and Gast, R.K. (2010) Flow Cytometric Characterization of Peyer’s Patch and Cecal Tonsil T Lymphocytes in Laying Hens Following Challenge with Salmonella enterica Serovar Enteritidis. Veterinary Immunology and Immunopathology, 133, 276-281. http://dx.doi.org/10.1016/j.vetimm.2009.08.001
Berndt, A., Pieper, J. and Methner, U. (2006) Circulating Gamma Delta T Cells in Response to Salmonella enterica Serovar Enteritidis Exposure in Chickens. Infection and Immunity, 74, 3967-3978. http://dx.doi.org/10.1128/IAI.01128-05
Tran, T.Q.L., Quessy, S., Letellier, A., Desrosiers, A. and Boulianne, M. (2010) Immune Response Following Vaccination against Salmonella Enteritidis Using 2 Commercial Bacterins in Laying Hens. Canadian Journal of Veterinary Research, 74, 185.