Establishment of a live vaccine strain against fowl typhoid and paratyphoid

  • Received : 2015.11.07
  • Accepted : 2015.12.24
  • Published : 2015.12.31


To develop a live vaccine strain against fowl typhoid and paratyphoid caused by Salmonella serovar Gallinarum biovar Gallinarum (Salmonella Gallinarum) and Salmonella serovar Enteritidis (Salmonella Enteritidis), respectively, several nalidixic acid resistant mutants were selected from lipopolysaccharide (LPS) rough strains of Salmonella Gallinarum that escaped from fatal infection of a LPS-binding lytic bacteriophage. A non-virulent and immunogenic vaccine strain of Salmonella Gallinarum, SR2-N6, was established through in vivo pathogenicity and protection efficacy tests. SR2-N6 was highly protective against Salmonella Gallinarum and Salmonella Enteritidis and safer than Salmonella Gallinarum vaccine strain SG 9R in the condition of protein-energy malnutrition. Thus, SR2-N6 may be a safe and efficacious vaccine strain to prevent both fowl typhoid and paratyphoid.


Supported by : Ministry of Food, Agriculture, Forestry and Fisheries


  1. Barrow PA, Huggins MB, Lovell MA. Host specificity of Salmonella infection in chickens and mice is expressed in vivo primarily at the level of the reticuloendothelial system. Infect Immun 1994, 62, 4602-4610.
  2. Bouzoubaa K, Nagaraja KV, Kabbaj FZ, Newman JA, Pomeroy BS. Feasibility of using proteins from Salmonella gallinarum vs. 9R live vaccine for the prevention of fowl typhoid in chickens. Avian Dis 1989, 33, 385-391.
  3. Chandra RK. Lymphocyte subpopulations in human malnutrition: cytotoxic and suppressor cells. Pediatrics 1977, 59, 423-427.
  4. Chandra RK. Numerical and functional deficiency in T helper cells in protein energy malnutrition. Clin Exp Immunol 1983, 51, 126-132.
  5. Chappell L, Kaiser P, Barrow P, Jones MA, Johnston C, Wigley P. The immunobiology of avian systemic salmonellosis. Vet Immunol Immunopathol 2009, 128, 53-59.
  6. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard Nineth edition. CLSI document M02-A9, Clinical and Laboratory Standards Institute, Wayne, 2006.
  7. Feberwee A, de Vries TS, Hartman EG, de Wit JJ, Elbers ARW, de Jong WA. Vaccination against Salmonella enteritidis in Dutch commercial layer flocks with a vaccine based on a live Salmonella gallinarum 9R strain: evaluation of efficacy, safety, and performance of serologic Salmonella tests. Avian Dis 2001, 45, 83-91.
  8. Grimont PAD, Weill FX. Antigenic formulae of the Salmonella serovars. WHO Collaborating Centre for Reference and Research on Salmonella. 9th ed. Institut Pasteur, Paris, 2007.
  9. Gulig PA. Virulence plasmids of Salmonella typhimurium and other salmonellae. Microb Pathog 1990, 8, 3-11.
  10. Hoffman-Goetz L, Keir R, Young C. Modulation of cellular immunity in malnutrition: effect of interleukin 1 on suppressor T cell activity. Clin Exp Immunol 1986, 65, 381-386.
  11. Kang MS, Kwon YK, Kim HR, Oh JY, Kim MJ, An BK, Shin EG, Kwon JH, Park CK. Comparative proteome and transcriptome analyses of wild-type and live vaccine strains of Salmonella enterica serovar Gallinarum. Vaccine 2012, 30, 6368-6375.
  12. Kim KS, Lee HS, Mo IP, Kim SJ. Outbreak of fowl typhoid from chickens in Korea. RDA J Agri Sci 1995, 37, 544-549.
  13. Kwon HJ, Cho SH. Pathogenicity of SG 9R, a rough vaccine strain against fowl typhoid. Vaccine 2011, 29, 1311-1318.
  14. Kwon HJ, Cho SH, Kim TE, Won YJ, Jeong J, Park SC, Kim JH, Yoo HS, Park YH, Kim SJ. Characterization of a T7-like lytic bacteriophage ($\varphi$SG-JL2) of Salmonella enterica serovar Gallinarum biovar Gallinarum. Appl Environ Microbiol 2008, 74, 6970-6979.
  15. Lee YJ, Mo IP, Kang MS. Safety and efficacy of Salmonella gallinarum 9R vaccine in young laying chickens. Avian Pathol 2005, 34, 362-366.
  16. Lyman MB, Steward JP, Roantree RJ. Characterization of the virulence and antigenic structure of Salmonella typhimurium strains with lipopolysaccharide core defects. Infect Immun 1976, 13, 1539-1542.
  17. Masoud H. LPS-based conjugate vaccines composed of saccharide antigens of smooth-type Salmonella enteritidis and rough-type S. gallinarum 9R bound to bovine serum albumin. Scand J Infect Dis 2007, 39, 315-322.
  18. Matsuda K, Chaudhari AA, Kim SW, Lee KM, Lee JH. Physiology, pathogenicity and immunogenicity of lon and/or cpxR deleted mutants of Salmonella Gallinarum as vaccine candidates for fowl typhoid. Vet Res 2010, 41, 59.
  19. Matsui H, Bacot CM, Garlington WA, Doyle TJ, Roberts S, Gulig PA. Virulence plasmid-borne spvB and spvC genes can replace the 90-kilobase plasmid in conferring virulence to Salmonella enterica serovar Typhimurium in subcutaneously inoculated mice. J Bacteriol 2001, 183, 4652-4658.
  20. McCarter MD, Naama HA, Shou J, Kwi LX, Evoy DA, Calvano SE, Daly JM. Altered macrophage intracellular signaling induced by protein-calorie malnutrition. Cell Immunol 1998, 183, 131-136.
  21. McMurray DN. Cell-mediated immunity in nutritional deficiency. Prog Food Nutr Sci 1984, 8, 193-228.
  22. Nicholas RA, Cullen GA. Development and application of an ELISA for detecting antibodies to Salmonella enteritidis in chicken flocks. Vet Rec 1991, 128, 74-76.
  23. Park KY, Lee SU, Yoo HS, Yeh JK. Epidemiological studies of Salmonella gallinarum infection in Korea: infection routes, biochemical characteristics, antimicrobial drug susceptibility pattern and plasmid profile. Infect Chemother 1996, 28, 413-421.
  24. Penha Filho RA, de Paiva JB, Arguello YM, da Silva MD, Gardin Y, Resende F, Berchieri Junior AB, Sesti L. Efficacy of several vaccination programmes in commercial layer and broiler breeder hens against experimental challenge with Salmonella enterica serovar Enteritidis. Avian Pathol 2009, 38, 367-375.
  25. Purchase C, Picard J, McDonald R, Bisschop SP. A comparison of the oral application and injection routes using the onderstepoort biological products fowl typhoid vaccine, its safety, efficacy and duration of protection in commercial laying hens. J S Afr Vet Assoc 2008, 79, 39-43.
  26. Rivadeneira DE, Grobmyer SR, Naama HA, Mackrell PJ, Mestre JR, Stapleton PP, Daly JM. Malnutritioninduced macrophage apoptosis. Surgery 2001, 129, 617-625.
  27. Rodrigue DC, Tauxe RV, Rowe B. International increase in Salmonella enteritidis: a new pandemic? Epidemiol Infect 1990, 105, 21-27.
  28. Shivaprasad HC, Barrow PA. Pullorum disease and fowl typhoid. In: Swayne DE, Glisson JR, McDougald LR, Nolan LK, Suarez DL, Nair V (eds.). Diseases of Poultry. 13th ed. pp. 678-692, Wiley-Blackwell, Ames, 2013.
  29. Silva EN, Snoeyenbos GH, Weinack OM, Smyser CF. Studies on the use of 9R strain of Salmonella gallinarum as a vaccine in chickens. Avian Dis 1981, 25, 38-52.
  30. Wigley P, Hulme S, Rothwell L, Bumstead N, Kaiser P, Barrow P. Macrophages isolated from chickens genetically resistant or susceptible to systemic salmonellosis show magnitudinal and temporal differential expression of cytokines and chemokines following Salmonella enterica challenge. Infect Immun 2006, 74, 1425-1430.
  31. Wigley P, Hulme SD, Bumstead N, Barrow PA. In vivo and in vitro studies of genetic resistance to systemic salmonellosis in the chicken encoded by the SAL1 locus. Microbes Infect 2002, 4, 1111-1120.
  32. Yi EC, Hackett M. Rapid isolation method for lipopolysaccharide and lipid A from gram-negative bacteria. Analyst 2000, 125, 651-656.