A critical review of Salmonella Typhimurium infection in laying hens

Avian Pathology

Volumn 40, Issue 5, 2011, Pages 429-436

  Wales, A D ^a   Davies, R H ^a  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANIMAL SALMONELLOSIS; BIRD DISEASE; CHICKEN; COMPARATIVE STUDY; EGG; FEMALE; GENETICS; MICROBIOLOGY; OVARY; OVIDUCT; PATHOGENICITY; REVIEW; SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM; SPECIES DIFFERENCE;

ANIMALS; CHICKENS; EGGS; FEMALE; OVARY; OVIDUCTS; POULTRY DISEASES; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SPECIES SPECIFICITY;

SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM;

EID: 80053234265     PISSN: 03079457     EISSN: 14653338     Source Type: Journal    
DOI: 10.1080/03079457.2011.606799     Document Type: Review

References (73)

1. Baggesen, D.L., Olsen, J.E. & Bisgaard, M. (1992). Plasmid profiles and phage types of Salmonella typhimurium isolated from successive flocks of chickens on three parent stock farms. Avian Pathology, 21, 569-579.
2. Baker, R.C., Goff, J.P. & Mulnix, E.J. (1980). Salmonellae recovery following oral and intravenous inoculation of laying hens. Poultry Science, 59, 1067-1072.
3. Barnhart, H.M., Dreesen, D.W., Bastien, R. & Pancorbo, O.C. (1991). Prevalence of Salmonella enteritidis and other serovars in ovaries of layer hens at time of slaughter. Journal of Food Protection, 54, 488-491.
4. Baskerville, A., Humphrey, T.J., Fitzgeorge, R.B., Cook, R.W., Chart, H., Rowe, B. & Whitehead, A. (1992). Airborne infection of laying hens with Salmonella enteritidis phage type 4. Veterinary Record, 130, 395-398.
5. Berrang, M.E., Cox, N.A., Frank, J.F. & Buhr, R.J. (1999). Bacterial penetration of the eggshell and shell membranes of the chicken hatching egg: a review. Journal of Applied Poultry Research, 8, 499-504.
6. Brown, D.D. & Brand, T.F. (1978). Experimental infection of point-oflay and in-lay pullets with Salmonella typhimurium. British Veterinary Journal, 134, 92-100.
7. Calenge, F., Kaiser, P., Vignal, A. & Beaumont, C. (2010). Genetic control of resistance to salmonellosis and to Salmonella carrier-state in fowl: a review. Genetics Selection Evolution, 42, 11.
8. Carrique-Mas, J.J., Breslin, M., Snow, L., McLaren, I., Sayers, A.R. & Davies, R.H. (2009). Persistence and clearance of different Salmonella serovars in buildings housing laying hens. Epidemiology and Infection, 137, 837-846.
9. Clavijo, R.I., Loui, C., Andersen, G.L., Riley, L.W. & Lu, S.W. (2006). Identification of genes associated with survival of Salmonella enterica serovar Enteritidis in chicken egg albumen. Applied and Environmental Microbiology, 72, 1055-1064.
10. Clayton, D.J., Bowen, A.J., Hulme, S.D., Buckley, A.M., Deacon, V.L., Thomson, N.R., Barrow, P.A., Morgan, E., Jones, M.A., Watson, M. & Stevens, M.P. (2008). Analysis of the role of 13 major fimbrial subunits in colonisation of the chicken intestines by Salmonella enterica serovar Enteritidis reveals a role for a novel locus. BMC Microbiology, 8, 228.
11. Cogan, T.A., Jorgensen, F., Lappin-Scott, H.M., Benson, C.E., Woodward, M.J. & Humphrey, T.J. (2004). Flagella and curli fimbriae are important for the growth of Salmonella enterica serovars in hen eggs. Microbiology-SGM, 150, 1063-1071.
12. Cox, N.A., Berrang, M.E. & Cason, J.A. (2000). Salmonella penetration of egg shells and proliferation in broiler hatching eggs*a review. Poultry Science, 79, 1571-1574.
13. Cox, N.A., Davis, B.H., Watts, A.B. & Colmer, A.R. (1973). Salmonella in the laying hen. 1. Salmonella recovery from viscera, feces and eggs following oral inoculation. Poultry Science, 52, 661-666.
14. De Buck, J., Van Immerseel, F., Haesebrouck, F. & Ducatelle, R. (2004). Colonization of the chicken reproductive tract and egg contamination by Salmonella. Journal of Applied Microbiology, 97, 233-245.
15. EFSA. (2007). Report of the task force on zoonoses data collection on the analysis of the baseline study on the prevalence of Salmonella in holdings of laying hen flocks of Gallus gallus. EFSA Journal, 97, 1-84.
16. EFSA. (2009). The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and food-borne outbreaks in the European Union in 2007. EFSA Journal, 223, 1-310.
17. EFSA. (2010a). The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and food-borne outbreaks in the European Union in 2008. EFSA Journal, 8, 1496.
18. EFSA. (2010b). Scientific opinion on a quantitative estimate of the public health impact of setting a new target for the reduction of Salmonella in laying hens. EFSA Journal, 8, 1546.
19. Ekawa, T., Terai, S., Amano, F., Hanatani, Y. & Ohta, H. (2009). Diverse pathogenicity of Salmonella Enteritidis clones isolated from poultry farms in chicks and BALB/c mice. Journal of Poultry Science, 46, 370-376.
20. FSA. (2004). Report of the survey of Salmonella contamination of UK produced shell eggs on retail sale. UK Food Standards Agency. Available online at: http://www.food.gov.uk/science/surveillance/fsis2004branch/fsis5004eggs (accessed 11 April 2011).
21. FSA. (2007). UK wide survey of Salmonella in raw shell eggs used in catering premises. UK Food Standards Agency. Available online at: http://www.food.gov.uk/science/surveillance/fsisbranch2007/egg survey (accessed 11 April 2011).
22. Gantois, I., Ducatelle, R., Pasmans, F., Haesebrouck, F. & Van Immerseel, F. (2009). The Salmonella Enteritidis lipopolysaccharide biosynthesis gene rfbH is required for survival in egg albumen. Zoonoses and Public Health, 56, 145-149.
23. Gantois, I., Eeckhaut, V., Pasmans, F., Haesebrouck, F., Ducatelle, R. & Van Immerseel, F. (2008). A comparative study on the pathogenesis of egg contamination by different serotypes of Salmonella. Avian Pathology, 37, 399-406.
24. Garber, L., Smeltzer, M., Fedorka-Cray, P., Ladely, S. & Ferris, K. (2003). Salmonella enterica serotype Enteritidis in table egg layer house environments and in mice in US layer houses and associated risk factors. Avian Diseases, 47, 134-142.
25. Gast, R.K. (2007). Serotype-specific and serotype-independent strategies for preharvest control of food-borne Salmonella in poultry. Avian Diseases, 51, 817-828.
26. Gast, R.K. & Holt, P.S. (1998). Persistence of Salmonella enteritidis from one day of age until maturity in experimentally infected layer chickens. Poultry Science, 77, 1759-1762.
27. Gast, R.K., Guard-Petter, J. & Holt, P.S. (2002). Characteristics of Salmonella enteritidis contamination in eggs after oral, aerosol, and intravenous inoculation of laying hens. Avian Diseases, 46, 629-635.
28. Guan, J., Grenier, C. & Brooks, B.W. (2006). In vitro study of Salmonella enteritidis and Salmonella typhimurium definitive type 104: survival in egg albumen and penetration through the vitelline membrane. Poultry Science, 85, 1678-1681.
29. Guard-Petter, J. (2001). The chicken, the egg and Salmonella enteritidis. Environmental Microbiology, 3, 421-430.
30. Guard-Petter, J., Henzler, D.J., Rahman, M.M. & Carlson, R.W. (1997). On-farm monitoring of mouse-invasive Salmonella enterica serovar Enteritidis and a model for its association with the production of contaminated eggs. Applied and Environmental Microbiology, 63, 1588-1593.
31. Hassan, J.O. & Curtiss, R. (1997). Efficacy of a live avirulent Salmonella typhimurium vaccine in preventing colonization and invasion of laying hens by Salmonella typhimurium and Salmonella enteritidis. Avian Diseases, 41, 783-791.
32. Helmuth, R., Stephan, R., Bunge, C., Hoog, B., Steinbeck, A. & Bulling, E. (1985). Epidemiology of virulence-associated plasmids and outer membrane protein patterns within seven common Salmonella serotypes. Infection and Immunity, 48, 175-182.
33. Henzler, D.J. & Opitz, H.M. (1992). The role of mice in the epizootiology of Salmonella enteritidis infection on chicken layer farms. Avian Diseases, 36, 625-631.
34. Howard, Z.R., Moore, R.W., Zabala-Diaz, I.B., Landers, K.L., Byrd, J.A., Kubena, L.F., Nisbet, D.J., Birkhold, S.G. & Ricke, S.C. (2005). Ovarian laying hen follicular maturation and in vitro Salmonella internalization. Veterinary Microbiology, 108, 95-100.
35. HPA. (2010). Salmonella in humans (excluding S. typhi; S. Paratyphi). Faecal and lower gastrointestinal tract isolates reported to the Health Protection Agency Centre for Infections. England and Wales, 1990-2009. UK Health Protection Agency. Available online at: http://www. hpa.org.uk/Topics/InfectiousDiseases/InfectionsAZ/Salmonella/Epi demiologicalData/salmDataHuman/(accessed 29 June 2010).
36. Humphrey, T.J., Baskerville, A., Chart, H., Rowe, B. & Whitehead, A. (1991a). Salmonella enteritidis PT4 infection in specific pathogen free hens: influence of infecting dose. Veterinary Record, 129, 482-485.
37. Humphrey, T.J., Whitehead, A., Gawler, A.H., Henley, A. & Rowe, B. (1991b). Numbers of Salmonella enteritidis in the contents of naturally contaminated hens' eggs. Epidemiology and Infection, 106, 489-496.
38. Humphrey, T.J., Williams, A., McAlpine, K., Lever, M.S., Guard-Petter, J. & Cox, J.M. (1996). Isolates of Salmonella enterica Enteritidis PT4 with enhanced heat and acid tolerance are more virulent in mice and more invasive in chickens. Epidemiology and Infection, 117, 79-88.
39. Jørgensen, F., Leach, S., Wilde, S.J., Davies, A., Stewart, G.S. & Humphrey, T. (2000). Invasiveness in chickens, stress resistance and RpoS status of wild-type Salmonella enterica subsp. enterica serovar Typhimurium definitive type 104 and serovar Enteritidis phage type 4 strains. Microbiology, 146, 3227-3235.
40. Kang, H., Loui, C., Clavijo, R.I., Riley, L.W. & Lu, S. (2006). Survival characteristics of Salmonella enterica serovar Enteritidis in chicken egg albumen. Epidemiology and Infection, 134, 967-976.
41. Keller, L.H., Schifferli, D.M., Benson, C.E., Aslam, S. & Eckroade, R.J. (1997). Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella enteritidis. Avian Diseases, 41, 535-539.
42. Leach, S.A., Williams, A., Davies, A.C., Wilson, J., Marsh, P.D. & Humphrey, T.J. (1999). Aerosol route enhances the contamination of intact eggs and muscle of experimentally infected laying hens by Salmonella typhimurium DT104. FEMS Microbiology Letters, 171, 203-207.
43. Litrup, E., Christensen, H., Nordentoft, S., Nielsen, E.M., Davies, R.H., Helmuth, R. & Bisgaard, M. (2010). Use of multiple-locus variable-number tandem-repeats analysis (MLVA) typing to characterize Salmonella Typhimurium DT41 broiler breeder infections. Journal of Applied Microbiology, 109, 2032-2038.
44. Messens, W., Duboccage, L., Grijspeerdt, K., Heyndrickx, M. & Herman, L. (2004). Growth of Salmonella serovars in hens' egg albumen as affected by storage prior to inoculation. Food Microbiology, 21, 25-32.
45. Messens, W., Grijspeerdt, K. & Herman, L. (2005). Eggshell penetration by Salmonella: a review. World's Poultry Science Journal, 61, 71-85.
46. Miyamoto, T., Baba, E., Tanaka, T., Sasai, K., Fukata, T. & Arakawa, A. (1997). Salmonella enteritidis contamination of eggs from hens inoculated by vaginal, cloacal, and intravenous routes. Avian Diseases, 41, 296-303.
47. Miyamoto, T., Horie, T., Baba, E., Sasai, K., Fukata, T. & Arakawa, A. (1998). Salmonella penetration through eggshell associated with freshness of laid eggs and refrigeration. Journal of Food Protection, 61, 350-353.
48. Mizumoto, N., Sasai, K., Tani, H. & Baba, E. (2005). Specific adhesion and invasion of Salmonella Enteritidis in the vagina of laying hens. Veterinary Microbiology, 111, 99-105.
49. Ogunniyi, A.D., Kotlarski, I., Morona, R. & Manning, P.A. (1997). Role of SefA subunit protein of SEF14 fimbriae in the pathogenesis of Salmonella enterica serovar Enteritidis. Infection and Immunity, 65, 708-717.
50. Okamura, M., Kamijima, Y., Miyamoto, T., Tani, H., Sasai, K. & Baba, E. (2001a). Differences among six Salmonella serovars in abilities to colonize reproductive organs and to contaminate eggs in laying hens. Avian Diseases, 45, 61-69.
51. Okamura, M., Lillehoj, H.S., Raybourne, R.B., Babu, U.S., Heckert, R.A., Tani, H., Sasai, K., Baba, E. & Lillehoj, E.P. (2005). Differential responses of macrophages to Salmonella enterica serovars Enteritidis and Typhimurium. Veterinary Immunology and Immunopathology, 107, 327-335.
52. Okamura, M., Miyamoto, T., Kamijima, Y., Tani, H., Sasai, K. & Baba, E. (2001b). Differences in abilities to colonize reproductive organs and to contaminate eggs in intravaginally inoculated hens and in vitro adherences to vaginal explants between Salmonella enteritidis and other Salmonella serovars. Avian Diseases, 45, 962-971.
53. Okamura, M., Sonobe, M., Obara, S., Kubo, T., Nagai, T., Noguchi, M., Takehara, K. & Nakamura, M. (2010). Potential egg contamination by Salmonella enterica serovar Typhimurium definitive type 104 following experimental infection of pullets at the onset of lay. Poultry Science, 89, 1629-1634.
54. Östlund, K. (1971). Bacteriology of washed and unwashed eggs. II. Penetration of Salmonella bacteria through the eggshell. Acta Veterinaria Scandinavica, 12, 479-488.
55. OzFoodNet Working Group. (2009). Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of OzFoodNet Network, 2008. Communicable Diseases Intelligence, 33, 389-413.
56. Padron, M. (1990). Salmonella typhimurium penetration through the eggshell of hatching eggs. Avian Diseases, 34, 463-465.
57. Peralta, R.C., Yokoyama, H., Ikemori, Y., Kuroki, M. & Kodama, Y. (1994). Passive immunisation against experimental salmonellosis in mice by orally administered hen egg-yolk antibodies specific for 14-kDa fimbriae of Salmonella Enteritidis. Journal of Medical Microbiology, 41, 29-35.
58. Pires, S.M., Vigre, H., Makela, P. & Hald, T. (2010). Using outbreak data for source attribution of human salmonellosis and campylobacteriosis in Europe. Foodborne Pathogens and Disease, 7, 1351-1361.
59. Poppe, C., Demczuk, W., McFadden, K. & Johnson, R.P. (1993). Virulence of Salmonella enteritidis phagetypes 4, 8 and 13 and other Salmonella spp. for day-old chicks, hens and mice. Canadian Journal of Veterinary Research, 57, 281-287.
60. Rabsch, W., Andrews, H.L., Kingsley, R.A., Prager, R., Tschape, H., Adams, L.G. & Baumler, A.J. (2002). Salmonella enterica serotype Typhimurium and its host-adapted variants. Infection and Immunity, 70, 2249-2255.
61. Rajashekara, G., Munir, S., Alexeyev, M.F., Halvorson, D.A., Wells, C.L. & Nagaraja, K.V. (2000). Pathogenic role of SEF14, SEF17, and SEF21 fimbriae in Salmonella enterica serovar Enteritidis infection of chickens. Applied and Environmental Microbiology, 66, 1759-1763.
62. Rank, D.L., Saeed, M.A. & Muriana, P.M. (2009). Cloning of Salmonella enterica serovar Enteritidis fimbrial protein SefA as a surface protein in Escherichia coli confers the ability to attach to eukaryotic cell lines. Applied and Environmental Microbiology, 75, 6622-6625.
63. Refsum, T., Heir, E., Kapperud, G., Vardund, T. & Holstad, G. (2002). Molecular epidemiology of Salmonella enterica serovar Typhimurium isolates determined by pulsed-field gel electrophoresis: comparison of isolates from avian wildlife, domestic animals, and the environment in Norway. Applied and Environmental Microbiology, 68, 5600-5606.
64. Reiber, M.A., Conner, D.E., Bilgili, S.F. & Kotrola, J.S. (1991). Persistence of Salmonella Enteritidis and Salmonella Typhimurium in the oviducts of hens inseminated with contaminated semen. Poultry Science, 70(Suppl. 1), 98.
65. Sauter, E.A. & Petersen, C.F. (1974). The effect of egg shell quality on penetration by various salmonellae. Poultry Science, 53, 2159-2162.
66. Schoeni, J.L., Glass, K.A., McDermott, J.L. & Wong, A.C.L. (1995). Growth and penetration of Salmonella Enteritidis, Salmonella Heidelberg and Salmonella Typhimurium in eggs. International Journal of Food Microbiology, 24, 385-396.
67. Sesma, B., Alvarez, M.J., Aramendia, P., Goni, B., De Pablo, N. & Goni, P. (1987). Aislamiento extraintestinal de Salmonella en gallinas: estudio epidemiológico de dos brotes de salmonelosis por consumo de huevo crudo [Extraintestinal isolation of Salmonella in hens: epidemiological observations regarding two Salmonella outbreaks due to the ingestion of uncooked eggs]. Microbiologia (Madrid), 3, 209-212.
68. Snow, L.C., Davies, R.H., Christiansen, K.H., Carrique-Mas, J., Wales, A., O'Connor, J.L., Cook, A.J. & Evans, S.E. (2007). Survey of the prevalence of Salmonella species on commercial laying farms in the United Kingdom. Veterinary Record, 161, 471-476.
69. Thiagarajan, D., Saeed, M., Turek, J. & Asem, E. (1996). In vitro attachment and invasion of chicken ovarian granulosa cells by Salmonella enteritidis phage type 8. Infection and Immunity, 64, 5015-5021.
70. Wales, A., Breslin, M. & Davies, R. (2006). Semiquantitative assessment of the distribution of Salmonella in the environment of caged layer flocks. Journal of Applied Microbiology, 101, 309-318.
71. Wigley, P. (2004). Genetic resistance to Salmonella infection in domestic animals. Research in Veterinary Science, 76, 165-169.
72. Williams, A., Davies, A.C., Wilson, J., Marsh, P.D., Leach, S. & Humphrey, T.J. (1998). Contamination of the contents of intact eggs by Salmonella typhimurium DT104. The Veterinary Record, 143, 562-563.
73. Williams, J.E., Dillard, L.H. & Hall, G.O. (1968). Penetration patterns of Salmonella Typhimurium through outer structures of chicken eggs. Avian Diseases, 12, 445-466.