Vaccination and early protection against non-host-specific Salmonella serotypes in poultry: Exploitation of innate immunity and microbial activity

Epidemiology and Infection

Volumn 133, Issue 6, 2005, Pages 959-978

  van Immerseel, F ^a   Methner, U ^b   Rychlik, I ^c   Nagy, B ^d   Velge, P ^e   Martin, G ^b   Foster, N ^f   Ducatelle, R ^a   Barrow, Paul A ^f  

^a GHENT UNIVERSITY   (Belgium)

^b FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^c VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^e CEMAGREF   (France)

^f INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; BACTERIUM LIPOPOLYSACCHARIDE; CD4 ANTIGEN; CD8 ANTIGEN; COMPLEMENT COMPONENT C3B; DNA VACCINE; GAMMA INTERFERON RECEPTOR; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G2A; INACTIVATED VACCINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 4; INTERLEUKIN 6; LIVE VACCINE; LYMPHOKINE; MESSENGER RNA; PHOP PROTEIN; RECA PROTEIN; SALMONELLA ENTERITIDIS IMMUNE LYMPHOKINE DERIVATIVE; SALMONELLA GALLINARUM VACCINE; SALMONELLA TYPHIMURIUM VACCINE; SALMONELLOSIS VACCINE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; YERSINIA OUTER PROTEIN E;

ACTIVE IMMUNIZATION; ADOPTIVE IMMUNOTHERAPY; B LYMPHOCYTE; BACTERIAL COLONIZATION; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL IMMUNITY; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIRD DISEASE; BREEDING; CELL INFILTRATION; CELLULAR IMMUNITY; CITROBACTER; CLOSTRIDIUM DIFFICILE; COST EFFECTIVENESS ANALYSIS; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG SYNTHESIS; ESCHERICHIA COLI; GRANULOCYTE FUNCTION; GROWTH INHIBITION; HATCHING; HEALTH PROGRAM; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOSTIMULATION; INFECTION CONTROL; INFECTION PREVENTION; INFECTION SENSITIVITY; INNATE IMMUNITY; INTESTINE WALL; KLEBSIELLA PNEUMONIAE; LETHAL DOSE; MICROBIAL ACTIVITY; NONHUMAN; POLYMORPHONUCLEAR CELL; POULTRY; PREVENTIVE HEALTH SERVICE; REVIEW; SALMONELLA ENTERITIDIS; SALMONELLOSIS; SEROTYPING; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, BACTERIAL; CHICKENS; POULTRY; POULTRY DISEASES; SALMONELLA; SALMONELLA INFECTIONS; SALMONELLA VACCINES; VACCINATION;

EID: 28244438781     PISSN: 09502688     EISSN: 14694409     Source Type: Journal    
DOI: 10.1017/S0950268805004711     Document Type: Review

References (187)

1. Rodrigue DL, Tauxe RV, Rowe B. International increase in Salmonella enteritidis: A new pandemic? Epidemiology and Infection 1990 105: 21-27.
2. Oldfield EC. Emerging foodborne pathogens: Keeping your patients and your families safe. Reviews in Gastroenterological Disorders 2001; 1: 177-186.
3. Rabsch W, Tschape H, Baumler AJ. Non-typhoidal salmonellosis: Emerging problems. Microbes and Infection 2001; 3: 237-247.
4. World Health Organisation. WHO Surveillance Programme for Control of Foodborne Infections and Intoxications in Europe. 7th Report 1993-1998. FAO/WHO Collaborating Centre for Research and Training in Food Hygiene and Zoonoses, Berlin, Germany, 2001.
5. Ejidokun OO, Killalea D, Cooper M, Holmyard S, Cross A, Kemp C. Four linked outbreaks of Salmonella enteritidis phage type 4 infection: The continuing egg threat. Communicable Diseases Public Health 2000; 3: 95-100.
6. Parry SM, Palmer SR, Slader J, Humphrey T. Risk factors for Salmonella food poisoning in the domestic kitchen: A case control study. Epidemiology and Infection 2002; 129: 277-285.
7. Mohle-Boetani JC, Werner SB, Abbott S, et al. Salmonella enteritidis infections from shell eggs: Outbreaks in California. West Journal of Medicine 1998; 169: 299-303.
8. Hayes S, Nylen G, Smith R, Salmon RL, Palmer SR. Undercooked hens eggs remain a risk factor for sporadic Salmonella enteritidis infection. Communicable Diseases Public Health 1999; 2: 66-67.
9. Kimura AC, Reddy V, Marcus R, et al. Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype Enteritidis infections in the United States: A case-control study in FoodNet sites. Clinical Infectious Diseases 2004; 38: 244-252.
10. Heyndrickx M, Vanderkerckhove D, Herman L, Rollier I, Grijspeerdt K, De Zutter L. Routes for Salmonella contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiology and Infection 2002; 129: 253-265.
11. Wilson IG. Salmonella and campylobacter contamination of raw retail chickens from different producers: A six year survey. Epidemiology and Infection 2002; 129: 635-645.
12. Van Duijkeren E, Wannet WJ, Houwers DJ, Van Pelt W. Serotype and phage type distribution of Salmonella strains isolated from humans, cattle, pigs, and chickens in the Netherlands from 1984 to 2001. Journal of Clinical Microbiology 2002; 40: 3980-3985.
13. Capita R, Alvarez-Astorga M, Alonso-Calleja C, Moreno B, del Camino Garcia-Fernandez M. Occurrence of Salmonellae in retail chicken carcasses and their products in Spain. International Journal of Food Microbiology 2003; 81: 169-173.
14. Van Immerseel F, Cauwerts K, Devriese L, Haesebrouck F, Ducatelle R. Feed additives to control Salmonella in poultry World's Poultry Science Journal 2002; 58: 501-513.
15. Cooper GL, Venables LM, Nicholas RAJ, Cullen GA, Hormaeche CE. Vaccination of chickens with chicken-derived Salmonella Enteritidis phage type 4 aroA live oral Salmonella vaccines. Vaccine 1992; 10: 247-254.
16. Cooper GL, Venables LM, Woodward MJ, Hormaeche CE. Vaccination of chickens with strain CVL30, a genetically defined Salmonella Enteritidis aroA live oral vaccine candidate. Infection and Immunity 1994; 62: 4747-4754.
17. Vielitz E, Conrad C, Voss M, Löhren U, Bachmeier J, Hahn I. Immunization against Salmonella-infections using live and inactivated vaccine preparations. Deutsche Tierärztliche Wochenschrift 1992; 99: 483-485.
18. Gast RK, Stone HD, Holt PS. Evaluation of the efficacy of oil-emulsion bacterins for reducing faecal shedding of Salmonella Enteritidis by laying hens. Avian Diseases 1993; 37: 1085-1091.
19. Gast RK, Stone HD, Holt PS, Beard CW. Evaluation of the efficacy of an oil-emulsion bacterin for protecting chickens against Salmonella Enteritidis. Avian Diseases 1992; 36: 992-999.
20. Hassan JO, Curtiss R. Development and evaluation of an experimental vaccination program using a live avirulent Salmonella Typhimurium strain to protect immunized chickens against challenge with homologous and heterologous Salmonella serotypes. Infection and Immunity 1994; 62: 5519-5527.
21. Nakamura M, Nagamine N, Takahashi T, Suzuki S, Sato S. Evaluation of the efficacy of a bacterin against Salmonella enteritidis infection and the effect of stress after vaccination. Avian Diseases 1994; 38: 717-724.
22. Curtiss R, Hassan JO. Nonrecombinant and recombinant avirulent Salmonella vaccines for poultry. Veterinary Immunology and Immunopathology 1996; 54: 365-372.
23. Hahn I. A contribution to consumer protection: TAD Salmonella vac® E - a new live vaccine for chickens against Salmonella Enteritidis. Lohmann Information 2000, 23: 29-32.
24. Springer S, Lehmann J, Lindner Th, Thielebein J, Alber G, Selbitz HJ. A new live Salmonella Enteritidis vaccine for chicken - experimental evidence of its safety and efficacy. Berliner und Münchner Tierärztliche Wochenschrift 2000, 113: 246-252.
25. Timms LM, Marshall RN, Breslin MF. Laboratory and field trial assessment of protection given by a Salmonella Enteritidis PT4 inactivated, adjuvant vaccine. British Veterinary Journal 1994; 150: 93-102.
26. Feberwee A, deVries TS, Elbers AR, de Jong WA. Results of a Salmonella enteritidis vaccination field trial in broiler-breeder flocks in The Netherlands. Avian Diseases 2000;, 44: 249-255.
27. 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 Diseases 2001; 45: 83-91.
28. Clifton-Hadley FA, Breslin M, Venables LM, et al. A laboratory study of an inactivated bivalent iron restricted Salmonella enterica serovars Enteritidis and Typhimurium dual vaccine against Typhimurium challenge in chickens. Veterinary Microbiology 2002; 89: 167-179.
29. Woodward MJ, Gettinby G, Breslin MF, Corkish JD, Houghton S. The efficacy of Salenvac, a Salmonella enterica subsp. Enterica serotype Enteritidis iron-restricted bacterin vaccine, in laying chickens. Avian Pathology 2002; 31: 383-392.
30. Davies R, Breslin M. Effects of vaccination and other preventive methods for Salmonella enteritidis on commercial laying chicken farms. Veterinary Record 2003, 153: 673-677.
31. Lister A. Salmonella enteritidis infection in broilers and broiler breeders. Veterinary Record 1988; 123: 350.
32. Gast RK, Holt PS. Experimental horizontal transmission of Salmonella Enteritidis strains (phage types 4, 8 and 13a) in chicks. Avian Diseases 1999; 43: 774-778.
33. Cox NA, Berrang ME, Cason JA. Salmonella penetration of egg shells and proliferation in broiler hatching eggs - a review. Poultry Science 2000; 79: 1571-1574.
34. Van Immerseel F, Meulemans L, De Buck J, et al. Bacteria-host interactions of Salmonella Paratyphi B dT+ in poultry. Epidemiology and Infection 2004; 132: 239-243.
35. Byrd JA, DeLoach JR, Corrier DE, Nisbet DJ, Stanker LH. Evaluation of Salmonella serotype distributions from commercial broiler hatcheries and grower houses. Avian Diseases 1999; 43: 774-778.
36. Bailey JS, Cox NA, Craven SE, Cosby DE. Serotype tracking of Salmonella through integrated broiler chicken operations. Journal of Food Protection 2002; 65: 742-745.
37. Methner U, Steinbach G, Meyer H. Investigations on the efficacy of Salmonella immunization of broiler breeder birds to Salmonella colonization of these birds and their progeny following experimental oral infection. Berliner und Münchner Tierärztliche Wochenschrift 1994; 107: 192-198.
38. Methner U, Steinbach G. Efficacy of maternal Salmonella antibodies against oral infection of chicks with Salmonella Enteritidis. Berliner und Münchner Tierärztliche Wochenschrift 1997; 110: 373-377.
39. Methner U, Keiling S, Kreutzer B, Schweinitz P. Impact of maternal antibodies on the efficacy of immunisation of chicks with live Salmonella vaccines. Deutsche Tierärztliche Wochenschrift 2002; 109: 149-153.
40. Vainio O, Imhof BA (eds). Immunology and developmental biology of the chicken, Springer, Berlin: Germany, 1996.
41. Friedman A, Bar-Shira E, Sklan D. Ontogeny of gut associated immune competence in the chick. World Poultry Science Journal 2003; 59: 209-220.
42. Collins FM. Vaccines and cell-mediated immunity. Bacteriological Reviews 1974; 38: 371-374.
43. Mastroeni P, Villareal-Ramos B, Demarco de Hormaeche D, Hormaeche CE. Delayed (footpad) hypersensitivity and Arthus reactivity using protein-rich antigens and LPS in mice immunized with live attenuated aroA Salmonella vaccines. Microbial Pathogenesis 1993; 14: 369-379.
44. Raupach B, Kaufmann SHE. Bacterial virulence, proinflammatory cytokines and host immunity: How to choose the appropriate Salmonella vaccine strain? Microbes and Infection 2001; 3: 1261-1269.
45. Eckmann L, Kagnoff MF. Cytokines in host defense against Salmonella. Microbes and Infection 2001; 3: 1191-1200.
46. + TCR-alpha beta cells and IFN-gamma in bacterial clearance independent of intracellular location. Journal of Immunology 1996; 156: 3321-3326.
47. Sinha K, Mastroeni P, Harrison J, de Hormaeche RD, Hormaeche CE. Salmonella Typhimurium aroA, htrA, and aroD htrA mutants cause progressive infections in athymic (nu/nu) BALB/c mice. Infection and Immunity 1997; 65: 1566-1569.
48. Mastroeni P, Harrison JA, Robinson JH, et al. Interleukin-12 is required for control of the growth of attenuated aromatic-compound-dependent Salmonellae in BALB/c mice: Role of gamma interferon and macrophage activation. Infection and Immunity 1998; 66: 4467-4476.
49. McSorley SJ, Jenkins MK. Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar Typhimurium. Infection and Immunity 2000; 68: 3344-3348.
50. Mastroeni P, Simmons C, Fowle, R, Hormaeche CE, Dougan G. Igh-6-/- (B-cell-deficient) mice fail to mount solid acquired resistance to oral challenge with virulent Salmonella enterica serovar Typhimurium and show impaired Th1 T-cell responses to Salmonella antigens. Infection and Immunity 2000; 68: 46-53.
51. Mittrücker H, Raupach B, Köhler A, Kaufmann S. Cutting edge: Role of B-lymphocytes in protective immunity against Salmonella Typhimurium infection. Journal of Immunology 2000; 164: 1648-1652.
52. Mastroeni P, Ménager N. Development of acquired immunity to Salmonella. Journal of Medical Microbiology 2003; 52: 453-459.
53. Thatte J, Rath S, Bal V. Analysis of immunization route-related variation in the immune response to heat-killed Salmonella typhimurium in mice. Infection and Immunity 1995; 63: 99-103.
54. Thatte J, Rath S, Bal V. Immunisation with live versus killed Salmonella typhimurium leads to the generation of an interferon-γ-dominant versus an IL-4 dominant immune response. International Immunology 1993; 5: 1431-1436.
55. Foster N, Hulme SD, Barrow PA. Induction of antimicrobial pathways during early phase immune response to Salmonella in murine macrophages; Interferon gamma (IFN-γ) and up-regulation of interferon gamma receptor alpha (IFNγRα) expression are required for NADPH gp 91 phox stimulated oxidative burst and control of virulent Salmonella. Infection and Immunity 2003; 71: 4733-4741.
56. Berndt A, Methner U. Gamma/delta T cell response of chickens after oral administration of attenuated and non-attenuated Salmonella typhimurium strains. Veterinary Immunology and Immunopathology 2001; 78: 143-161.
57. Nagaraja KV, Rajashekara G. Vaccination against Salmonella enterica serovar Enteritidis infection: Dilemma and realities. In: Saeed AM, ed. Salmonella enterica serovar Enteritidis in humans and animals. Iowa State University Press, Ames, USA, 1999: 397-404.
58. Barrow PA, Wallis TS. Vaccination against Salmonella infections in food animals: Rationale, theoretical basis and practical application. In: Wray A, Wray C, eds. Salmonella in domestic animals. CAB International, Oxford, England, 2000: 323-339.
59. Lee GM, Jackson GDF, Cooper GN. The role of serum and biliary antibodies and cell-mediated immunity in the clearance of S. Typhimurium from chickens. Veterinary Immunology and Immunopathology 1981; 2: 233-252.
60. Lee GM, Jackson GDF, Cooper GN. Infection and Immune responses in chickens exposed to Salmonella Typhimurium. Avian Diseases 1983; 27: 577-583.
61. Desmidt M, Ducatelle R, Mast J, Goddeeris BM, Kaspers B, Haesebrouck F. Role of the humoral immune system in Salmonella Enteritidis phage type four infection in chickens. Veterinary Immunology and Immunopathology 1998; 63: 355-367.
62. Farnell MB, El Halawani M, You S, McElroy AP, Hargis BM, Caldwell DJ. In vivo biologic effects of recombinant-turkey interferon-gamma in neonatal leg-horn chicks: Protection against Salmonella enteritidis organ invasion. Avian Diseases 2001; 45: 473-478.
63. Fierer J. Polymorphonuclear leukocytes and innate immunity to Salmonella infections in mice. Microbes and Infection 2001; 3: 1233-1237.
64. Hargis BM, Caldwell DJ, Kogut MH. Immunoprophylaxis of chicks against Salmonella enterica serovar Enteritidis. In: Salmonella enterica serovar Enteritidis in humans and animals. Iowa State University Press, Ames, USA, 1999: 413-418.
65. Van Immerseel F, De Buck J, De Smet I, Haesebrouck F, Ducatelle R. The effect of vaccination with a Salmonella Enteritidis aroA mutant on early cellular responses in caecal lamina propria of newly-hatched chickens. Vaccine 2002; 20: 3034-3041.
66. Withanage GSK, Kaiser P, Wigley P, et al. Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar Typhimurium. Infection and Immunity 2004; 72: 2152-2159.
67. Kogut MH, Rothwell L, Kaiser P. Differential regulation of cytokine gene expression by avian heterophils during receptor-mediated phagocytosis of opsonized and nonopsonized Salmonella enteritidis. Journal of Interferon Cytokine Research 2003; 23: 319-327.
68. Wood MW, Jones MA, Watson PR, et al. The secreted effector protein of Salmonella Dublin, SopA, is translocated into eukaryotic cells and influences the induction of enteritis. Cellular Microbiology 2000; 2: 293-303.
69. Lee CA, Silva M, Siber AM, Kelly AJ, Galyov E, McCormick BA. A secreted Salmonella protein induces a pro-inflammatory response in epithelial cells, which promotes neutrophil migration. Proceedings of the National Academy of Sciences USA. 2000; 97: 12283-12288.
70. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL. Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. Journal of Immunology 2001; 167: 1882-1885.
71. Hayashi F, Smith KD, Ozinsky A, et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001; 410: 1099-1103.
72. Reed KA, Hobert ME, Kolenda CE, et al. The Salmonella typhimurium flagellar basal body protein FliE is required for flagellin production and to induce a pro-inflammatory response in epithelial cells. Journal of Biological Chemistry 2002; 227: 13346-13353.
73. Kaiser P, Rothwell L, Galyov EE, Barrow PA, Burnside J, Wigley P. Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum. Microbiology 2000; 146: 3217-3226.
74. Foster N, Lovell MA, Marston KL, et al. Rapid protection of gnotobiotic pigs against experimental salmonellosis following induction of ploymorphonuclear leukocytes by avirulent Salmonella enterica. Infection and Immunity 2003; 71: 2182-2191.
75. Kogut MH, Tellez GI, Hargis BM, Corrier DE, DeLoach JR. The effect of 5-fluorouracil treatment of chicks: A cell depletion model for the study of avian polymorphonuclear leukocytes and natural host defenses. Poultry Science 1993; 72: 1873-1880.
76. Kogut MH, Tellez GI, McGruder ED, et al. Heterophils are decisive components in the early responses of chickens to Salmonella Enteritidis infections. Microbial Pathogenesis 1994; 16: 141-151.
77. Tellez GI, Kogut MH, Hargis BM. Immunoprophylaxis of Salmonella Enteritidis infection by lymphocines in leghorn chicks. Avian Diseases 1993; 37: 1062-1070.
78. Kogut MH, McGruder ED, Hargis BM, Corrier DE, DeLoach JR. Characterization of the pattern of inflammatory cell influx in chicks following the intraperitoneal administration of live Salmonella Enteritidis and Salmonella Enteritidis - immune lymphokines. Poultry Science 1995; 74: 8-17.
79. Kogut MH, McGruder ED, Hargis BM, Corrier DE, DeLoach JR. In vivo activation of heterophil function in chickens following injection with Salmonella Enteritidis-immune lymphokines. Journal of Leukocyte Biology 1995; 57: 56-62.
80. Smith HW. The use of live vaccines in experimental Salmonella Gallinarum infection in chickens with observations on their interference effect. Journal of Hygiene 1956; 54: 419-432.
81. 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. Infection and Immunity 1994; 62: 4602-4610.
82. Uzzau S, Brown DJ, Wallis T, et al. Host adapted serotypes of Salmonella enterica. Epidemiology and Infection 2000; 125: 229-255.
83. Meyer H, Barrow PA, Pardon P. Salmonella immunization in animals. Proceedings of the International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. 1992: 345-374.
84. Barrow PA. Immunological control of Salmonella in poultry. In: Blankenship LC, ed. Colonization control of human bacterial enteropathogens in poultry. Academic Press, San Diego, USA, 1991: 199-217.
85. Zhang-Barber L, Turner AK, Barrow PA. Vaccination for control of Salmonella in poultry. Vaccine 1999; 17: 2538-2545.
86. Liu W, Yang Y, Chung N, Kwang J. Induction of humoral immune responses and protective immunity in chickens against Salmonella Enteritidis after a single dose of killed bacterium-loaded microspheres. Avian Diseases 2001; 45: 797-806.
87. McCapes RH, Coffland RT, Christie LE. Challenge of turkey poults originating from hens vaccinated with Salmonella Typhimurium bacterins. Avian Diseases 1967; 11: 15-24.
88. Truscott RB, Friars GW. The transfer of endotoxin induced immunity from hens to poults. Canadian Journal of Comparative Medical and Veterinary Science 1972; 36: 64-68.
89. Miyamoto T, Kitaoka D, Withanage GSK, Fukata T, Sasai K, Baba E. Evaluation of the efficacy of Salmonella Enteritidis oil-emulsion bacterin in an intravaginal challenge model in hens. Avian Diseases 1999; 43: 487-505.
90. Davison S, Benson CE, Henzler DJ, Eckroade RJ. Field observations with Salmonella Enteritidis bacterins. Avian Diseases 1999; 43: 664-669.
91. Woodward MJ, Gettinby G, Breslin MF, Corkish JD, Houghton S. The efficacy of Salenvac, a Salmonella enterica subsp. Enterica serotype Enteritidis iron-restricted bacterin vaccine, in laying chickens. Avian Pathology 2002; 31: 383-392.
92. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Molecular Microbiology 2003; 47: 103-118.
93. Meenakshi M, Bakshi CS, Butchaiah G, Bansal MP, Siddiqui MZ, Singh VP. Adjuvanted outer membrane protein vaccine protects against infection with Salmonella Enteritidis. Veterinary Research Communications 1999; 23: 81-90.
94. Khan MI, Fadl AA, Venkitanarayanan KS. Reducing colonization of Salmonella Enteritidis in chicken by targeting outer membrane proteins. Journal of Applied Microbiology 2003; 95: 142-145.
95. Fadl AA, Venkitanarayanan K, Khan MI. Identification of Salmonella Enteritidis outer membrane proteins expressed during attachment to human intestinal epithelial cells. Journal of Applied Microbiology 2002; 92: 180-186.
96. Meyer H, Koch H, Methner U, Steinbach G. Vaccines in salmonellosis control in animals. Zentralblatt Bakteriologie 1993; 278: 407-415.
97. Linde K, Hahn I, Vielitz E. Development of live Salmonella vaccines optimally attenuated for chickens. Lohmann Information 1997; 20: 23-31.
98. Schwarz S, Liebisch B. Use of ribotyping, IS200 typing and plasmid analysis for the identification of Salmonella enterica subsp. Enterica serovar Typhimurium vacccine strain Zoosaloral H and its differentiation from wild-type strains of the same serovar. Zentralblatt Bakteriologie 1994; 281: 442-450.
99. Barrow PA, Lovell MA, Berchieri Jr. A. The use of two live attenuated vaccines to immunize egg-laying hens against Salmonella enteritidis phage type 4. Avian Pathology 1991; 20: 681-692.
100. Feberwee A, Hartman EG, De Wit JJ, De Vries TS. The spread of Salmonella Gallinarum 9R vaccine strain under field conditions. Avian Diseases 2001; 45: 1024-1029.
101. Cerquetti MC, Gherardi MM. Orally administered attenuated Salmonella Enteritidis reduces chicken cecal carriage of virulent Salmonella challenge organisms. Veterinary Microbiology 2000; 76: 185-192.
102. Cerquetti MC, Gherardi MM. Vaccination of chickens with a temperature-sensitive mutant of Salmonella Enteritidis. Vaccine 2000; 18: 1140-1145.
103. Maskell DJ, Hormaeche CE, Harrington KA, Joycey HS, Liew FY. The initial suppression of bacterial growth in a Salmonella infection is mediated by a localized rather than a systemic response. Microbial Pathogenesis 1987; 2: 295-305.
104. Klose KE, Mekalanos JJ. Simultaneous prevention of glutamine synthesis and high-affinity transport attenuates Salmonella typhimurium virulence. Infection and Immunity 1997; 65: 587-596.
105. Tacket CO, Sztein MB, Losonsky GA, et al. Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans. Infection and Immunity 1997; 65: 452-456.
106. Methner U, Barrow PA, Gregorova D, Rychlik I. Intestinal colonisation-inhibition and virulence of Salmonella phoP, rpoS and ompC deletion mutants in chickens. Veterinary Microbiology 2004; 98: 37-43.
107. Mastroeni P, Chabalgoity JA, Dunstan SJ, Maskell DJ, Dougan G. Salmonella: Immune responses and vaccines. Veterinary Journal 2000; 161: 132-164.
108. Wick MJ, Harding CV, Twesten NJ, Normark SJ, Pfeifer JD. The phoP locus influences processing and presentation of Salmonella typhimurium antigens by activated macrophages. Molecular Microbiology 1995; 16: 465-476.
109. Miller SI, Mekalanos JJ. Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. Journal of Bacteriology 1990; 172: 2485-2460.
110. Hopkins S, Kraehenbuhl JP, Schodel F, et al. A recombinant Salmonella typhimurium vaccine induces local immunity by four different routes of immunization. Infection and Immunity 1995; 63: 3279-3286.
111. Niedergang F, Sirard JC, Blanc CT, Kraehenbuhl JP. Entry and survival of Salmonella typhimurium in dendritic cells and presentation of recombinant antigens do not require macrophage-specific virulence factors. Proceedings of the National Academy of Sciences USA 2000; 97: 14650-14655.
112. Barrow PA, Hassan JO, Berchieri Jr. A. Reduction in faecal excretion by chickens of Salmonella typhimurium by immunization with avirulent mutants of S. typhimurium. Epidemiology and Infection 1990; 104: 413-426.
113. Cooper GL, Nicholas RA, Cullen GA, Hormaeche CE. Vaccination of chickens with a Salmonella enteritidis aroA live oral Salmonella vaccine. Microbial Pathogenesis 1990; 9: 255-265.
114. Parker C, Asokan K, Guard-Petter J. Egg contamination by Salmonella serovar Enteritidis following vaccination with delta-aroA Salmonella serovar Typhimurium. FEMS Microbiology Letters 2001; 195: 73-78.
115. Barrow PA, Page K, Lovell MA. The virulence for gnotobiotic pigs of live attenuated vaccine strains of Salmonella enterica serovar Typhimurium and Enteritidis. Vaccine 2001; 19: 3432-3436.
116. Dueger EL, House JK, Heithoff DM, Mahan MJ. Salmonella DNA adenine methylase mutants prevent colonization of newly hatched chickens by homologous and heterologous serovars. International Journal of Food Microbiology 2003; 80: 153-159.
117. Wallis TS, Galyov EE. Molecular basis of Salmonella-induced enteritis. Molecular Microbiology 2000; 36: 997-1005.
118. Roland K, Curtiss III R, Sizemore D. Construction and evaluation of a delta cya delta crp Salmonella typhimurium strain expressing avian pathogenic Escherichia coli O78 LPS as a vaccine to prevent air sacculitis in chickens. Avian Diseases 1999; 43: 429-441.
119. Pogonka T, Klotz C, Kovacs F, Lucius R. A single dose of recombinant Salmonella typhimurium induces specific humoral immune responses against heterologous Eimeria tenella antigens in chicken. International Journal of Parasitology 2003; 33: 81-88.
120. Drabner B, Guzmann CA. Elicitation of predictable immune responses by using live bacterial vectors. Biomolecular Engineering 2001; 17: 75-82.
121. Dietrich G, Spreng S, Favre D, Viret JF, Guzman CA. Live attenuated bacteria as vectors to deliver plasmid DNA vaccines. Current Opinions in Molecular Therapeutics 2003; 5: 10-19.
122. Kang BY, Curtiss III R. Immune responses dependent on antigen location in recombinant attenuated Salmonella typhimurium vaccines following oral immunization. FEMS Immunology Medical Microbiology 2003; 15: 99-104.
123. Dunstan SJ, Ramsay AJ, Strugnell RA. Studies of immunity and bacterial invasiveness in mice given recombinant salmonella vector encoding murine interleukin-6. Infection and Immunity 1996; 64: 2730-2736.
124. Igwe EI, Geginat G, Russmann H. Concomitant cytosolic delivery of two immunodominant listeria antigens by Salmonella enterica serovar typhimurium conferring superior protection against murine listeriosis. Infection and Immunity 2002; 70: 7114-7119.
125. Russmann H. Inverted pathogenicity: The use of pathogen-specific molecular mechanisms for prevention or therapy of disease. International Journal of Medical Microbiology 2004; 293: 565-569.
126. Darji A, Guzman CG, Gerstel B, et al. Oral somatic trangene vaccination using attenuated S. typhimurium. Cell 1997; 91: 765-775.
127. Ianaro A, Xu D, O'Donnell CA, Di Rosa M, Liew FY. Expression of TGF-beta in attenuated Salmonella typhimurium oral administration leads to the reduction of inflammation, IL-2 and IFN-gamma, but enlargement of IL-10, in carrageenin-induced oedema in mice. Immunology 1995; 84: 8-15.
128. Babu U, Scott M, Myers MJ, et al. Effects of live attenuated and killed vaccine on T-lymphocyte mediated immunity in laying hens. Veterinary Immunology and Immunopathology 2003; 91: 39-44.
129. Pritchard DG, Nivas SC, York MD, Pomeroy BS. Effect of galE mutant Salmonella Typhimurium on experimental salmonellosis in chickens. Avian Diseases 1978; 22: 562-575.
130. Desmidt M, Ducatelle R, Haesebrouck F. Serological and bacteriological observations on experimental infection with Salmonella Hadar in chickens. Veterinary Microbiology 1998; 60: 259-269.
131. Van der Wielen PW, Biesterveld S, Notermans S, Hofstra H, Urlings BA, van Knapen F. Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Applied and Environmental Microbiology 2000; 66: 2536-2540.
132. Nurmi E, Rantala M. New aspects of Salmonella infection in broiler production. Nature 1973; 241: 210-211.
133. Mead GC. Prospects for 'competitive exclusion' treatment to control salmonellosis and other foodborne pathogens in poultry. Veterinary Journal 2000; 159: 111-123.
134. Barrow PA, Tucker JF. Inhibition of colonization of the chicken caecum with Salmonella typhimurium by pre-treatment with strains of Escherichia coli. Journal of Hygiene 1986, 96: 161-169.
135. Barrow PA, Tucker JF, Simpson JM. Inhibition of colonization of the chicken alimentary tract with Salmonella Typhimurium gram-negative facultatively anaerobic bacteria. Epidemiology and Infection 1987; 98: 311-322.
136. Berchieri A, Barrow PA. In vitro characterization of intra-generic inhibition of growth in Salmonella typhimurium. Journal of General Microbiology 1991; 137: 2147-2153.
137. Martin G, Methner U, Rychlik I, Barrow PA. Zur Spezifitat von Hemmwirkungen zwischen Salmonella-Stämmen. Deutsche Tierärztliche Wochenschrift 2002; 109: 154-157.
138. Barrow PA, Lovell MA, Murphy CK, Page K. Salmonella infection in a commercial line of ducks; experimental studies on virulence, intestinal colonisation and immune protection. Epidemiology and Infection 1999; 123: 121-132.
139. Iba AM, Berchieri Jr. A, Barrow PA. Interference between Salmonella serotypes in intestinal colonization of chickens: Correlation with in vitro behaviour. FEMS Microbiology Letters 1995; 131: 153-159.
140. Nógrady N, Imre A, Rychlik I, Barrow PA, Nagy B. Growth and colonization suppression of Salmonella enterica serovar Hadar in vitro and in vivo. FEMS Microbiology Letters 2003; 218: 127-133.
141. Berchieri Jr. A, Barrow PA. Further studies on the inhibition of colonization of the chicken alimentary tract with Salmonella Typhimurium by pre-colonization with an avirulent mutant. Epidemiology and Infection 1990; 104: 427-441.
142. Barrow PA, Simpson JM, Lovell MA. Intestinal colonization in the chicken of food-poisoning Salmonella serotypes; microbial characteristics associated with faecal excretion. Avian Pathology 1988; 17: 571-588.
143. Cooper GL, Venables LM, Woodward MJ, Hormaeche CE. Invasiveness and persistence of Salmonella Typhimurium, and a genetically defined S. Enteritidis aroA strain in young chickens. Infection and Immunity 1994; 62: 4739-4746.
144. Methner U, Berndt A, Steinbach G. Combination of competitive exclusion and immunization with an attenuated live Salmonella vaccine strain in chickens. Avian Diseases 2001; 45: 631-638.
145. Curtiss R, Kelly SM. Salmonella Typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infection and Immunity 1987; 55: 3035-3043.
146. Methner U, Barrow PA, Martin G, Meyer H. Comparative study of the protective effect against Salmonella colonisation in newly hatched chickens using live, attenuated Salmonella vaccine strains, wildtype Salmonella strains or a competitive exclusion product. International Journal of Food Microbiology 1997; 35: 223-330.
147. Lovell MA, Barrow PA. Intestinal colonisation of gnotobiotic pigs by Salmonella organisms; interaction between isogenic and unrelated strains. Journal of Medical Microbiology 1999; 48: 1-10.
148. Duval-Iflah Y, Chappuis JP, Ducluzeau R, Raibaud P. Intra-specific interactions between Escherichia coli in human newborns and in gnotobiotic mice and piglets. Progress in Food and Nutrition Science 1983; 7: 107-116.
149. Davidson JN, Hirsch DC. Bacterial competition as a means of reventing neonatal diarrhoea in pigs. Infection and Immunity 1976; 13: 1773-1774.
150. Shinefield HR, Ribble JC, Boris M, Eichenwald HF. Bacterial interference: Its effect on nursery acquired infections with Staphylococcus aureus. I. II. III. IV. Am J Dis Child 1963; 105: 646-682.
151. Selwyn S, Marsh PD, Setna TN. In vitro and in vivo studies on antibiotics from skin micrococcaceae. Chemotherapy 1975; 5: 391-396.
152. Noble W, Willie JA. Infections between antibiotic-producing and non-producing staphylococci in skin surface and sub-surface models. British Journal of Experimental Pathology 1980; 61: 339-343.
153. Sprunt K, Leidy G. The use of bacterial interference to prevent infection. Canadian Journal of Microbiology 1988; 34: 332-338.
154. Borriello SP, Barclay FE. Protection of hamster against Clostridium difficile ileocaecitis by prior colonization with non-pathogenic strains. Journal of Medical Microbiology 1985; 19: 339-350.
155. Barrow PA, Page K. Inhibition of colonisation of the alimentary tract in young chickens with Campylobacter jejuni by pre-colonisation with strains of C. jejuni. FEMS Microbiology Letters 2000; 182: 87-91.
156. s. Journal of Bacteriology 1996; 178: 3072-3076.
157. Rychlik I, Martin G, Methner U, et al. Identification of Salmonella enterica serovar Typhimurium genes associated with growth suppression in stationary-phase nutrient broth cultures and in the chicken intestine. Archives in Microbiology 2002; 178: 411-420.
158. Volf J, Sevcik M, Havlickova H, Sisak F, Damborsky J, Rychlik I. Role of SdiA in Salmonella enterica serovar Typhimurium physiology and virulence. Arch Microbiol 2002; 178: 94-101.
159. Zhang-Barber L, Turner AK, Martin G, Frankel G, Dougan G, Barrow PA. Influence of genes encoding proton-translocating enzymes on suppression of Salmonella Typhimurium growth and colonization. Journal of Bacteriology 1997; 179: 7186-7190.
160. Nógrády N, Imre A, Rychlik I, Barrow PA, Nagy N. Genes responsible for anaerobic fumarate and arginine metabolism are involved in growth suppression in Salmonella enterica serovar Typhimurium in vitro, without influencing colonization inhibition in the chicken in vivo. Veterinary Microbiology 2003; 97: 191-199.
161. Surette MG, Miller MB, Bassler B. Quorum sensing in Escherichia coli, Salmonella Typhimurium, and Vibrio harveyi: A new family of genes responsible for auto-inducer production. Proceedings of the National Academy of Sciences USA 1999; 96: 1639-1644.
162. Sperandio V, Mellies JL, Nguyen W, Shin S, Kaper JB. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proceedings of the National Academy of Sciences USA 1999; 96: 15196-15201.
163. Wang XD, de Boer PA, Rothfield LI. A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division
164. Ahmer BMM, Vanreeuwijk J, Timmers CD, Valentine PJ, Heffron F. Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on he virulence plasmid. Journal of Bacteriology 1998; 180: 1185-1193.
165. Takeuchi K. Electron microscope studies of experimental Salmonella infection. 1. Penetration into intestinal epithelium by Salmonella typhimurium. Journal of Food Protection 1967; 50: 928-932.
166. Chauviere G, Coconnier MH, Kerneis S, Darfeuille-Michaud A, Joly B, Servin AL. Competitive exclusion of diarrheagenic Escherichia coli (ETEC) from human enterocyte-like Caco-2 cells by heat-killed Lactobacillus. FEMS Microbiology Letters 1992; 70: 213-217.
167. Servin AL, Coconnier MH. Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Practice Research Clinical Gastroenterology 2003; 17: 741-754.
168. Horie M, Ishiyama A, Fujihira-Ueki Y, Sillanpaa J, Korhonen TK, Toba T. Inhibition of the adherence of Escherichia coli strains to basement membrane by Lactobacillus crispatus expressing an S-layer. Journal of Applied Microbiology 2002; 92: 396-403.
169. Coconnier MH, Klaenhammer TR, Kerneis S, Bernet MF, Servin AL. Protein-mediated adhesion of Lactobacillus acidophilus BG2FO4 on human enterocyte and mucus-secreting cell lines in culture. Applied Environmental Microbiology 1992; 58: 2034-2039.
170. Lee YK, Puong KY, Ouwehand AC, Salminen S. Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. Journal Medical Microbiology 2003; 52: 925-930.
171. Soerjadi AS, Rufner R, Snoeyenbos GH, Weinack OM. Adherence of salmonellae and native gut microflora to the gastrointestinal mucosa of chicks. Avian Diseases 1982; 26: 576-584.
172. Soerjadi AS, Stehman SM, Snoeyenbos GH, Weinack OM, Smyser CF. The influence of lactobacilli on the competitive exclusion of paratyphoid salmonellae in chickens. Avian Diseases 1981; 25: 1027-1033.
173. Seuna E, Nurmi E. Therapeutical trials with antimicrobial agents and cultured cecal microflora in Salmonella infantis infections in chickens. Poultry Science 1979; 58: 1171-1174.
174. Mack DR, Michail S, Wei S, McDougall L, Hollingsworth MA. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. American Journal Physiology 1999; 276: 941-950.
175. Van Immerseel F, De Buck J, De Smet I, Haesebrouck F, Ducatelle R. Dynamics of immune cell infiltration in the caecal lamina propria of chickens after neonatal infection with a Salmonella Enteritidis strain. Developmental and Comparative Immunology 2002; 26: 355-364.
176. Desmidt M, Ducatelle R, Haesebrouck F. Pathogenesis of Salmonella Enteritidis phage type four after experimental infection of young chickens. Veterinary Microbiology 1997; 56: 99-109.
177. Desmidt M, Ducatelle R, Haesebrouck F. Research notes: immunohistochemical observations in the ceca of chickens infected with Salmonella Enteritidis phage type four. Poultry Science 1998; 77: 73-74.
178. Van Immerseel F, Meulemans L, De Buck J, Pasmans F, Haesebrouck F, Ducatelle R. Early protection against Salmonella Enteritidis after vaccination with a live strain is abolished by depletion of the heterophilic granulocytes. 2003. XIIIth Congress of the World Veterinary Poultry Association, Denver, Colorado, USA.
179. Field TE, Howard JG, Whitby JL. Studies on the rapid production of a non-specific type of immunity to Salmonella typhi infection in mice. Journal of the Royal Army Medical Corps 1955; 101: 324-444.
180. Wilson GS, Miles AA. Topley and Wilson's principles of bacteriology, virology and immunity, 5th edn. London: Edward Arnold, 1964.
181. Kodama H, Sato G, Mikami T. Age-dependent resistance of chickens to Salmonella in vitro: Phagocytic and bactericidal activities of splenic phagocytes. American Journal of Veterinary Research 1976; 37: 1091-1094.
182. Barrow PA, Lovell MA, Frost AJ, Bland P. Prevention of salmonellosis in gnotobiotic pigs by pre-colonization with avirulent Salmonella strains. Proceedings of the International Symposium on Salmonella and Salmonellosis, 20-22 May, Ploufragan, France. Zoopole development, Institut Superieur des Productions Animales et des Industries Agro-alimentaires, 1997; 519-520.
183. Roch-Arveiller M, el Abbouyi A, Paul JL, Smets P, Raichvarg D, Giroud JP. Effects exerted by RU 41740 on oxidative metabolism and migration of rat polymorphonuclear leukocytes collected after induction of one acute non specific inflammatory reaction. International Journal of Immunopharmacology 1987; 9: 417-424.
184. Capsoni F, Minonzio F, Ongari AM, Bonara P, Guidi G, Zanussi C. Increased expression of C3b and C3bi receptors on human neutrophils and monocytes induced by a glycoprotein extract from Klebsiella pneumoniae (RU41740). International Journal of Immunopharmacology 1991; 13: 227-233.
185. Minonzio F, Ongari AM, Palmieri R, Bochicchio D, Guidi G, Capsoni F. Immunostimulation of neutrophil phagocytic function by RU41740 (Biostim) in elderly subjects. Allergology and Immunopathology (Madrid) 1991; 19: 58-62.
186. Idohou N, Couderc R, Roch-Arveiller M, Tallet F, Giroud JP, Raichvarg D. The immunomodulating agent RU 41740 complexed with very-low-density lipoproteins enhances human polymorphonuclear neutrophil oxidative metabolism in vitro. Pharmacology 1993; 46: 341-345.
187. Turner AK, Lovell MA, Hulme SD, Zhang-Barber L, Barrow PA. Identification of Salmonella typhimurium genes required for colonization of the alimentary tract and for virulence in newly hatched chickens. Infection and Immunity 1998; 66: 2099-2106.