Mechanisms of egg contamination by Salmonella Enteritidis: Review article

FEMS Microbiology Reviews

Volumn 33, Issue 4, 2009, Pages 718-738

  Gantois, Inne ^a   Ducatelle, Richard ^a   Pasmans, Frank ^a   Haesebrouck, Freddy ^a   Gast, Richard ^b   Humphrey, Tom J ^c   Van Immerseel, Filip ^a  

^a GHENT UNIVERSITY   (Belgium)

^b RUSSELL RESEARCH CENTER   (United States)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Egg contamination; Eggshell penetration; Growth in eggs post lay; Reproductive tract colonization; Salmonella Enteritidis; Survival in the forming egg

Indexed keywords

ALBUMIN; EGG PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; VIRULENCE FACTOR;

BACTERIAL CELL WALL; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM CONTAMINATION; EGG; EGG LAYING; EGG SHELL; FOOD CONTAMINATION; GENETIC CODE; GENITAL SYSTEM; HOST PATHOGEN INTERACTION; HUMAN; MEMBRANE PERMEABILITY; NONHUMAN; OVARY; OVIDUCT; PREVALENCE; REVIEW; SALMONELLA ENTERITIDIS; SALMONELLOSIS; SEROTYPE; VAGINA; VITELLINE MEMBRANE;

ANIMALS; CHICKENS; EGGS; FEMALE; FOOD CONTAMINATION; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS, ANIMAL; VIRULENCE FACTORS;

SALMONELLA ENTERITIDIS;

EID: 66749124679     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2008.00161.x     Document Type: Review

References (142)

1. Abdel Mageed AM, Isobe N Yoshimura Y (2008) Expression of avian beta-defensins in the oviduct and effects of lipopolysaccharide on their expression in the vagina of hens. Poultry Sci 87 : 979 984.
2. Baron F, Gautier M Brulé G (1997) Factors involved in the inhibition of growth of Salmonella Enteritidis in liquid egg white. J Food Protect 60 : 1318 1323. (Pubitemid 27521888)
3. Barrow PA Lovell MA (1991) Experimental infection of egg-laying hens with Salmonella Enteritidis phage type 4. Avian Pathol 20 : 335 348.
4. Baskerville A, Humphrey TJ, Fitzgeorge RB, Cook RW, Chart H, Rowe B Whitehead A (1992) Airborne infection of laying hens with Salmonella Enteritidis phage type 4. Vet Rec 130 : 395 398.
5. Beaumont C, Protais J, Colin P, Guillot JF, Ballatif F, Mouline C, Lantier F, Lantier I, Girard O Pardon P (1994) Comparison of resistance of different poultry lines to intramuscular or oral inoculation by Salmonella Enteritidis. Vet Res 25 : 412.
6. Beaumont C, Protais J, Guillot JF, Colin P, Proux K, Millet N Pardon P (1999) Genetic resistance to mortality of day-old chicks and carrier-state of hens after inoculation with Salmonella Enteritidis. Avian Pathol 28 : 131 135. (Pubitemid 29235444)
7. Bellairs R, Harkness M Harkness RD (1963) The vitelline membrane of the hen's egg: a chemical and electron microscopial study. J Ultrastruct Res 8 : 339 359.
8. Berrang ME (1999) Bacterial penetration of the eggshell and shell membranes of the chicken hatching egg: a review. J Appl Poultry Res 8 : 499 504. (Pubitemid 129633357)
9. Bichler LA, Kabambi V, Nagaraja DVM Halvorson DA (1996) Salmonella Enteritidis in eggs, cloacal swab specimens, and internal organs of experimentally infected white leghorn chickens. Am J Vet Res 57 : 489 495. (Pubitemid 126575859)
10. Board RG (1966) Review: the course of microbial infection of the hen's egg. J Appl Bacteriol 29 : 319 341.
11. Bohez L, Gantois I, Ducatelle R, Pasmans F, Dewulf J, Haesebrouck F Van Immerseel F (2008) The Salmonella Pathogenicity Island 2 regulator SsrA promotes reproductive tract but not intestinal colonization in chickens. Vet Microbiol 126 : 216 224. (Pubitemid 350191743)
12. Bourret RB, Hess JF, Borkovich KA, Pakula AA Simon MI (1989) Protein phosphorylation in chemotaxis and two-component regulatory systems of bacteria. J Biol Chem 264 : 7085 7088. (Pubitemid 19119112)
13. Braden CR (2006) Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis 43 : 512 517. (Pubitemid 44157162)
14. Braun P Fehlhaber K (1995) Migration of Salmonella Enteritidis from the albumen into the egg yolk. Int J Food Microbiol 25 : 95 99.
15. Bruce J Drysdale EM (1994) Trans-shell transmission. Microbiology of the Avian Egg (Board RG Fuller R, eds), pp. 63 91. Chapman and Hall, London, UK.
16. Chen J, Clarke RC Griffiths MW (1996) Use of luminescent strains of Salmonella Enteritidis to monitor contamination and survival in eggs. J Food Protect 59 : 915 921. (Pubitemid 26380704)
17. Clavijo RI, Loui C, Andersen GL, Riley LW Lu S (2006) Identification of genes associated with survival of Salmonella entericaserovar Enteritidis in chicken egg albumen. Appl Environ Microb 72 : 1055 1064. (Pubitemid 43271210)
18. Cogan TA, Domingue G, Lappin-Scott HM, Benson CE, Woodward MJ Humphrey TJ (2001) Growth of Salmonella Enteritidis in artificially contaminated eggs: the effects of inoculum size and suspending media. Int J Food Microbiol 40 : 131 141. (Pubitemid 32979223)
19. Cogan TA, Jorgensen F, Lappin-Scott HM, Benson CE, Woodward MJ Humphrey TJ (2004) Flagella and curli fimbriae are important for the growth of Salmonella enterica serovars in hen eggs. Microbiology 150 : 1063 1071. (Pubitemid 38523296)
20. Collinson SK, Emody L, Muller KH, Trust TJ Kay WW (1991) Purification and characterization of thin, aggregative fimbriae from Salmonella Enteritidis. J Bacteriol 173 : 4773 4781.
21. De Buck J, Van Immerseel F, Meulemans G, Haesebrouck F Ducatelle R (2003) Adhesion of Salmonella enterica serotype Enteritidis isolates to chicken isthmal glandular secretions. Vet Microbiol 93 : 223 233. (Pubitemid 36412121)
22. De Buck J, Pasmans F, Van Immerseel F, Haesebrouck F Ducatelle R (2004a) Tubular glands of the isthmus are the predominant colonization site of Salmonella Enteritidis in the upper oviduct of laying hens. Poultry Sci 83 : 352 358. (Pubitemid 39197251)
23. De Buck J, Van Immerseel F, Haesebrouck F Ducatelle R (2004b) Effect of type-1 fimbriae of Salmonella enterica serotype Enteritidis on bacteremia and reproductive tract infection in laying hens. Avian Pathol 33 : 314 320. (Pubitemid 38940893)
24. De Buck J, Van Immerseel F, Haesebrouck F Ducatelle R (2004c) Colonization of the chicken reproductive tract and egg contamination by Salmonella. J Appl Microbiol 97 : 233 245. (Pubitemid 38998654)
25. De Reu K, Grijspeerdt K, Messens W, Heyndrickw M, Uyttendaele M, Debevere J Herman L (2006) Eggshell factors influencing eggshell penetration and whole egg contamination by different bacteria, including Salmonella Enteritidis. Int J Food Microbiol 112 : 253 260. (Pubitemid 44708379)
26. Desmidt M, Ducatelle R, Haesebrouck F, De Groot PA, Verlinden M, Wijffels R, Hinton M, Bale JA Allen VM (1996) Detection of antibodies to Salmonella Enteritidis in sera and yolks from experimentally and naturally infected chickens. Vet Rec 138 : 223 226. (Pubitemid 126614464)
27. Doran JL, Collinson SK, Burian J, Sarlos G, Todd EC, Munro CK, Kay CM, Banser PA, Peterkin PI Kay WW (1993) DNA-based diagnostic tests for Salmonella species targeting agfA, the structural gene for thin, aggregative fimbriae. J Clin Microbiol 31 : 2263 2273. (Pubitemid 23254185)
28. Duboccage L, Heyndrickx M, Grijpspeerdt K Herman L (2001) Growth of Salmonella in egg white. Meded Rijksuniv Gent Fak Landbouwkd Toegep Biol Wet 66 : 531 534.
29. EFSA (2007a) The community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2006. EFSA J 130 : 34 117.
30. EFSA (2007b) 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 J 97 : 1 84.
31. Elsbach P Weiss J (1998) Role of bactericidal/permeability-increasing protein in host defence. Curr Opin Immunol 10 : 45 49. (Pubitemid 28112078)
32. Fajardo TA, Anantheswaran RC, Puri VM Knabel SJ (1995) Penetration of Salmonella Enteritidis into eggs subjected to rapid cooling. J Food Protect 58 : 473 477.
33. Gantois I, Ducatelle R, Timbermont L, Boyen F, Bohez L, Haesebrouck F Van Immerseel F (2006) Oral immunisation of laying hens with live vaccine strains of TAD Salmonella vacE and TAD Salmonella vacT reduces internal egg contamination with Salmonella Enteritidis. Vaccine 24 : 6250 6255.
34. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F Van Immerseel F (2008a) The Salmonella Enteritidis lipopolysaccharide biosynthesis gene rfbH is required for survival in egg albumen. Zoonoses Public Health, DOI :.
35. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F Van Immerseel F (2008b) Salmonella Enteritidis genes induced during oviduct colonization and egg contamination in laying hens. Appl Environ Microb 74 : 6616 6622.
36. Gantois I, Eeckhaut V, Pasmans F, Haesebrouck F, Ducatelle R Van Immerseel F (2008c) A comparative study on the pathogenesis of egg contamination by different serotypes of Salmonella. Avian Pathol 37 : 399 406.
37. Gast RK Beard CW (1990) Production of Salmonella Enteritidis-contaminated eggs by experimentally infected hens. Avian Dis 34 : 438 446.
38. Gast RK Beard CW (1992) Detection and enumeration of Salmonella Enteritidis in fresh and stored eggs laid by experimentally infected hens. J Food Protect 55 : 152 156.
39. Gast RK Holt PS (1998) Persistence of Salmonella Enteritidis from one day of age until maturity in experimentally infected layer chickens. Poult Sci 77 : 1759 1762. (Pubitemid 128529098)
40. Gast RK Holt PS (2000a) Deposition of phage type 4 and 13a Salmonella Enteritidis strains in the yolk and albumen of eggs laid by experimentally infected hens. Avian Dis 44 : 706 710.
41. Gast RK Holt PS (2000b) Influence of the level and location of contamination on the multiplication of Salmonella Enteritidis at different storage temperatures in experimentally inoculated eggs. Poultry Sci 79 : 559 563.
42. Gast RK Holt PS (2001) Assessing the frequency and consequences of Salmonella Enteritidis deposition on the egg yolk membrane. Poultry Sci 80 : 997 1002. (Pubitemid 33659978)
43. Gast RK, Guard-Petter J Holt PS (2002) Characteristics of Salmonella Enteritidis contamination in eggs after oral, aerosol, and intravenous inoculation of laying hens. Avian Dis 46 : 629 635.
44. Gast RK, Guard-Petter J Holt PS (2003) Effect of prior serial in vivo passage on the frequency of Salmonella Enteritidis contamination in eggs from experimentally infected laying hens. Avian Dis 47 : 633 639. (Pubitemid 37156010)
45. Gast RK, Guard-Bouldin J Holt PS (2004) Colonization of reproductive organs and internal contamination of eggs after experimental infection of laying hens with Salmonella Heidelberg and Salmonella Enteritidis. Avian Dis 48 : 863 869. (Pubitemid 40059883)
46. Gast RK, Guard-Bouldin J Holt PS (2005a) The relationship between the duration of fecal shedding and the production of contaminated eggs by laying hens infected with strains of Salmonella Enteritidis and Salmonella Heidelberg. Avian Dis 49 : 382 386. (Pubitemid 41318896)
47. Gast RK, Holt PS Murase T (2005b) Penetration of Salmonella Enteritidis and Salmonella Heidelberg into egg yolks in an in vitro egg contamination model. Poultry Sci 84 : 621 625. (Pubitemid 40697359)
48. Gast RK, Guraya R, Guard-Bouldin J, Holt PS Moore RW (2007) Colonization of specific regions of the reproductive tract and deposition at different locations inside eggs laid by hens infected with Salmonella Enteritidis or Salmonella Heidelberg. Avian Dis 51 : 40 44. (Pubitemid 46481465)
49. Gast RK, Guraya R, Guard-Bouldin J Holt PS (2008a) Multiplication of Salmonella Enteritidis on the yolk membrane and penetration to the yolk contents at 30 degrees C in an in vitro contamination model.
50. Gautron J, Hincke MT, Panheleux M, Garcia-Ruiz JM, Boldicke T Nys Y (2001) Ovotransferrin is a matrix protein of the hen eggshell membranes and basal calcified layer. Connect Tissue Res 42 : 255 267. (Pubitemid 33138548)
51. Gautron J, Murayama E, Vignal A, Morisson M, McKee MD, Réhault S, Labas V, Belghazi M, Vidal M-L, Nys Y Hincke MT (2006) Cloning of ovocalyxin-36, a novel chicken eggshell protein related to lipopolysaccharide-binding proteins, bactericidal permeability-increasing proteins, and Plunc family proteins. J Biol Chem 282 : 5273 5286. (Pubitemid 47093753)
52. Griffin HD, Perry MM Gilbert AB (1984) Yolk formation. Physiology and Biochemistry of the Domestic Fowl (Freeman BM, ed), pp. 345 378. Academic Press, London.
53. Guan J, Grenier C Brooks BW (2006) In vitro study of Salmonella Enteritidis and Salmonella Typhimurium definitive type 104: survival in egg albumen and penetration through the vitelline membrane. Poultry Sci 85 : 1678 1681. (Pubitemid 44367851)
54. Guard-Bouldin J (2006) Comparative genome sequencing of Salmonella Enteritidis isolates that vary in virulence characteristics. Proceedings of the 110th US Animal Health Association, pp. 97 101. Minneapolis, MN.
55. Guard-Petter J (1998) Variants of smooth Salmonella enterica serovar Enteritidis that grow to higher cell density than the wild type are more virulent. Appl Environ Microb 64 : 2166 2172.
56. Guard-Petter J (2001) The chicken, the egg and Salmonella Enteritidis. Environ Microbiol 3 : 421 430. (Pubitemid 33136726)
57. Guard-Petter J, Henzler DJ, Rahman MM Carlson RW (1997) On-farm monitoring of mouse-invasive Salmonella enterica serovar Enteritidis and a model for its association with the production of contaminated eggs. Appl Environ Microb 63 : 1588 1593. (Pubitemid 27174872)
58. Guérin-Dubiard C, Pasco M, Mollé D, Désert C, Croguennec T Nau F (2006) Proteomic analysis of hen egg white. J Agr Food Chem 54 : 3901 3910. (Pubitemid 44030569)
59. Gürtler M Fehlhaber K (2004) Growth of Salmonella Enteritidis in yolk from eggs laid by immunized hens. Int J Food Microbiol 90 : 107 113. (Pubitemid 37522212)
60. Hammack TS, Sherrod PS, Bruce VR, June GA, Satchell FB Andrews WH (1993) Growth of Salmonella Enteritidis in grade A eggs during prolonged storage. Poultry Sci 71 : 373 377.
61. He H, Genovese KJ, Nisbet DJ Kogut MH (2006) Involvement of phosphatidylinositol-phospholipase C in immune response to Salmonella lipopolysaccharide in chicken macrophage cells (HD11). Int Immunopharmacol 6 : 1780 1787. (Pubitemid 44557185)
62. Higgs R, Lynn DJ, Gaines S, McMahon J, Tierney J, James T, Lloyd AT, Mulcahy G O'Farrelly C (2005) The synthetic form of a novel chicken beta-defensin identified in silico is predominantly active against intestinal pathogens. Immunogenetics 57 : 90 98. (Pubitemid 40591249)
63. Hincke MT Wellman-Labadie O (2007) XVIII European symposium on the quality of poultry meat and XII European symposium on the quality of eggs and egg products, Prague, September 2-5, pp. 39 41.
64. Hincke MT, Gautron J, Panheleux M, Garcia-Ruiz J, McKee MD Nys Y (2000) Identification and localization of lysozyme as a component of eggshell membranes and eggshell matrix. Matrix Biol 19 : 443 453.
65. Holt PS, Stone HD, Gast RK Porter Jr. RE (1996) Growth of Salmonella Enteritidis (SE) in egg contents from hens vaccinated with an SE bacterin. Food Microbiol 13 : 417 426. (Pubitemid 27052697)
66. Hoop RK Pospischil A (1993) Bacteriological, serological, histological and immunohistochemical findings in laying hens with naturally acquired Salmonella Enteritidis phage type 4 infection. Vet Microbiol 133 : 391 393.
67. Howard ZR, Moore RW, Zabala-Diaz IB, Landers KL, Byrd JA, Kubena LF, Nisbet DJ, Birkhold SG Ricke SC (2005) Ovarian laying hen follicular maturation and in vitro Salmonella internalization. Vet Microbiol 108 : 95 100. (Pubitemid 40726094)
68. Hughey VL Johnson EA (1987) Antimicrobial activity of lysozyme against bacteria involved in food spoilage and food-borne disease. Appl Environ Microb 53 : 2165 2170.
69. Humphrey TJ Whitehead A (1992) Techniques for the isolation of Salmonella from eggs. Brit Poultry Sci 33 : 761 768.
70. Humphrey TJ Whitehead A (1993) Egg age and the growth of Salmonella Enteritidis PT4 in egg contents. Epidemiol Infect 111 : 209 219. (Pubitemid 23297340)
71. Humphrey TJ, Baskerville A, Mawer S, Rowe B Hopper S (1989) Salmonella Enteritidis phage type 4 from contents of intact eggs: a study involving naturally infected eggs. Epidemiol Infect 103 : 415 423. (Pubitemid 20077279)
72. Humphrey TJ, Baskerville A, Chart H, Rowe B Whitehead A (1991a) Salmonella Enteritidis PT4 infection in specific pathogen free hens: influence of infecting dose. Vet Rec 129 : 482 485.
73. Humphrey TJ, Whitehead A, Gawer A, Henley A Rowe B (1991b) Numbers of Salmonella Enteritidis in the contents of naturally contaminated hen's eggs. Epidemiol Infect 106 : 489 496.
74. Ibrahim HR, Iwamori E, Sugimoto Y Aoki T (1998) Identification of a distinct antimicrobial domain within the N-lobe of ovotransferrin. Biochim Biophys Acta 1401 : 289 303. (Pubitemid 28122346)
75. Ibrahim HR, Sugimoto Y Aoki T (2000) Ovotransferrin antimicrobial peptide (OTAP-92) kills bacteria through a membrane damage mechanism. Biochim Biophys Acta 1523 : 196 205.
76. Jones DR, Anderson KE, Curtis PA Jones FT (2002) Microbial contamination in inoculated shell eggs: I. Effects of layer strain and hen age. Poultry Sci 81 : 715 720. (Pubitemid 39622770)
77. Jones MA, Wigley P, Page KL, Hulme SD Barrow PA (2001) Salmonella enterica serovar Gallinarum requires the Salmonella pathogenicity island 2 type III secretion system but not the Salmonella pathogenicity island 1 type III secretion system for virulence in chickens. Infect Immun 69 : 5471 5476. (Pubitemid 32786481)
78. Keller LH, Benson CE, Krotec K Eckroade RJ (1995) Salmonella Enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect Immun 63 : 2443 2449.
79. Keller LH, Schifferli DM, Benson CE, Aslam S Eckroade RJ (1997) Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella Enteritidis. Avian Dis 41 : 535 539. (Pubitemid 27426649)
80. Kim HS, Cho JH, Park HW, Yoon H, Kim MS Kim SC (2002) Endotoxin-neutralizing antimicrobial proteins of the human placenta. J Immunol 168 : 2356 2364. (Pubitemid 34171838)
81. Kinde H, Shivaprasad HL, Daft BM, Read DH, Ardans A, Breitmeyer R, Rajashekara G, Nagaraja KV Gardner IA (2000) Pathologic and bacteriologic findings in 27-week-old commercial laying hens experimentally infected with Salmonella Enteritidis, phage type 4. Avian Dis 44 : 239 248. (Pubitemid 30410883)
82. Leach SA, Williams A, Angela CD, Wilson J, Marsh PD Humphrey TJ (1999) Aerosol route enhances the contamination of intact eggs and muscle of experimentally infected laying hens by Salmonella Typhimurium DT104. FEMS Microbiol Lett 171 : 203 207.
83. Li S, Zhang Z, Pace L, Lillehoj H Zhang S (2009) Functions exerted by the virulence associated type three secretion system during Salmonella enterica serovar Enteritidis infection of chicken oviduct epithelial cells and macrophages. Avian Pathol, in press.
84. Li W, Watari S Kodama H (2003) Identification of glycosphingolipid binding sites for SEF21-fimbriated Salmonella enterica serovar Enteritidis in chicken oviductal mucosa. Vet Microbiol 93 : 73 78. (Pubitemid 36184678)
85. Lister SA (1988) Salmonella Enteritidis infection in broilers and broiler breeders. Vet Rec 123 : 350.
86. Lock JL Board RG (1992) Persistence of contamination of hens' egg albumen in vitro with Salmonella serotypes. Epidemiol Infect 108 : 389 396.
87. Lu S, Killoran PB Riley LW (2003) Association of Salmonella enterica serovar Enteritidis YafD with resistance to chicken egg albumen. Infect Immun 71 : 6734 6741. (Pubitemid 37475300)
88. Mann K (2007) The chicken egg white proteome. Proteomics 7 : 3558 3568. (Pubitemid 47597677)
89. Mann K (2008) Proteomic analysis of the chicken egg vitelline membrane. Proteomics 8 : 2322 2332.
90. Mariconda S, Wang Q Harshey RM (2006) A mechanical role for the chemotaxis system in swarming motility. Mol Microbiol 60 : 1590 1602. (Pubitemid 43801444)
91. Mayes FJ Takeballi MA (1983) Microbial contamination of the hen's egg: a review. J Food Protect 46 : 1092 1098.
92. 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 Microbiol 21 : 25 32. (Pubitemid 38047338)
93. Messens W, Grijspeerdt K Herman L (2005a) Eggshell penetration by Salmonella: a review. World Poultry Sci J 61 : 71 85.
94. Messens W, Grijspeerdt K Herman L (2005b) Eggshell characteristics and penetration by Salmonella enterica serovar Enteritidis through the production period of a layer flock. Brit Poultry Sci 46 : 694 700. (Pubitemid 43163241)
95. Messens W, Grijspeerdt K Herman L (2006) Eggshell penetration of hen's eggs by Salmonella enterica serovar Enteritidis upon various storage conditions. Brit Poultry Sci 47 : 554 560. (Pubitemid 44623219)
96. Messens W, Grijspeerdt K, De Reu K, De Ketelaere B, Mertens K, Bamelis F, Kemps B, De Baerdemaeker J, Decuypere E Herman L (2007) Eggshell penetration of various types of hens' eggs by Salmonella enterica serovar Enteritidis. J Food Protect 70 : 623 628. (Pubitemid 46446983)
97. Methner U, Al-Shabibi S Meyer H (1995) Experimental oral infection of specific pathogen-free laying hens and cocks with Salmonella Enteritidis strains. J Vet Med B 42 : 459 469.
98. Mine Y, Oberle C Kassaify Z (2003) Eggshell matrix proteins as a defense mechanism of avian eggs. J Agr Food Chem 51 : 249 253.
99. 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 Dis 41 : 296 303. (Pubitemid 27275116)
100. Miyamoto T, Horie T, Baba E, Sasai K, Fukata T Arakawa A (1998a) Salmonella penetration through eggshell associated with freshness of laid eggs and refrigeration. J Food Protect 61 : 350 353. (Pubitemid 28190263)
101. Miyamoto T, Horie T, Fukata T, Sasai K Baba E (1998b) Changes in microflora of the cloaca and oviduct of hens after intracloacal or intravaginal inoculation with Salmonella Enteritidis. Avian Dis 42 : 536 544.
102. Miyamoto T, Kitaoka D, Withanage GS, Fukata T, Sasai K Baba E (1999) Evaluation of the efficacy of Salmonella Enteritidis oil-emulsion bacterin in an intravaginal challenge model in hens. Avian Dis 43 : 497 505. (Pubitemid 29437626)
103. Mizumoto N, Sasai K, Tani H Baba E (2005) Specific adhesion and invasion of Salmonella Enteritidis in the vagina of laying hens. Vet Microbiol 111 : 99 105. (Pubitemid 41578946)
104. Morales CA, Porwollik S, Frye JG, Kinde H, McClelland M Guard-Bouldin J (2005) Correlation of phenotype with the genotype of egg-contaminating Salmonella enterica serovar Enteritidis. Appl Environ Microb 71 : 4388 4399. (Pubitemid 41129492)
105. Murase T, Fujimoto K, Nakayama R Otsuki K (2006) Multiplication and motility of Salmonella enterica serovars Enteritidis, Infantis, and Montevideo in in vitro contamination models of eggs. J Food Protect 69 : 1012 1016.
106. Nascimento VP, Cranstoun S Solomon SE (1992) Relationship between shell structure and movement of Salmonella Enteritidis across the eggshell wall. Brit Poultry Sci 33 : 37 48.
107. Ohashi H, Subedi M, Nishibori M, Isobe N Yoshimura Y (2005) Expressions of antimicrobial peptide gallinacin-1, -2 and -3 mRNAs in the oviduct of laying hens. J Poultry Sci 42 : 337 345.
108. 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 Dis 45 : 61 69. (Pubitemid 32285771)
109. 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 Dis 45 : 962 971. (Pubitemid 34067302)
110. Padron MN (1990) Salmonella Typhimurium penetration through the eggshell of hatching eggs. Avian Dis 34 : 463 465.
111. Parker CT, Harmon B Guard-Petter J (2002) Mitigation of avian reproductive tract function by Salmonella Enteritidis producing high-molecular-mass lipopolysaccharide. Environ Microbiol 4 : 538 545.
112. Patrick ME, Adcock PM, Gomez TM, Altekruse SF, Holland BH Tauxe RV (2004) Salmonella Enteritidis infections, United States, 1985-1999. Emerg Infect Dis 10 : 1 7. (Pubitemid 38040685)
113. Protais J, Colin P, Beaumont C, Guillot JF, Lantier F, Pardon P Bennejean G (1996) Line difference in resistance to Salmonella Enteritidis PT4 infection. Brit Poultry Sci 37 : 329 339. (Pubitemid 126460144)
114. Radkowski M (2002) Effect of moisture and temperature on survival of Salmonella Enteritidis on shell eggs. Archiv fur Geflügelkd 66 : 119 123.
115. Reiber MA, Conner DE Bilgili SF (1995) Salmonella colonization and shedding patterns of hens inoculated via semen. Avian Dis 39 : 317 322.
116. Ruiz J Lunam CA (2002) Ultrastructural analysis of the eggshell: contribution of the individual calcified layers and the cuticle to hatchability and egg viability in broiler breeders. Brit Poultry Sci 41 : 584 592.
117. Sauter EA Petersen CF (1969) The effect of eggshell quality on penetration by Pseudomonas fluorescens. Poultry Sci 45 : 825 829.
118. Sauter EA Petersen CF (1974) The effect of eggshell quality on penetration by various Salmonellae. Poultry Sci 53 : 2159 2162.
119. Schiemann DA Montgomery AL (1991) Immune response in chickens against Salmonella Typhimurium monitored with egg antibodies. Vet Microbiol 27 : 295 308.
120. Schoeni JL, Glass KA, McDermott JL Wang AC (1995) Growth and penetration of Salmonella Enteritidis, Salmonella Heidelberg and Salmonella Typhimurium in eggs. Int J Food Microbiol 24 : 385 393.
121. Sellier N, Vidal ML, Baron F, Michel J, Gautron J, Protais M, Beaumont C, Gautier M Nys Y (2007) Estimations of repeatability and heritability of egg albumen antimicrobial activity and of lysozyme and ovotransferrin concentrations. Brit Poultry Sci 48 : 559 566. (Pubitemid 47621331)
122. Shivaprasad HL, Timoney JF, Morales S, Lucio B Baker RC (1990) Pathogenesis of Salmonella Enteritidis infection in laying hens. I. Studies on egg transmission, clinical signs, fecal shedding, and serological responses. Avian Dis 34 : 548 557.
123. Silphaduang U, Hincke MT, Nys Y Mine Y (2006) Antimicrobial proteins in chicken reproductive system. Biochem Bioph Res Co 340 : 648 655. (Pubitemid 43021795)
124. Solomon SE (1997) Egg and eggshell quality. The Veterinary Press, pp. 11 36. Manson Publishing, Iowa State University Press, Ames.
125. Sourjik V (2004) Receptor clustering and signal processing in Escherichia coli chemotaxis. Trends Microbiol 12 : 569 576. (Pubitemid 39469906)
126. Sparks NHC Board RG (1985) Bacterial penetration of the recently developed oviposited shell of hens' eggs. Aust Vet J 62 : 169 170.
127. Stevens L (1991) Egg white proteins. Comp Biochem Phys B 100 : 1 9.
128. Subedi K, Isobe N, Nishibori M Yoshimura Y (2007) Changes in the expression of gallinacins, antimicrobial peptides in ovarian follicles during follicular growth and in response to lipopolysaccharide in laying hens (Gallus domesticus). Reproduction 133 : 127 133. (Pubitemid 46332162)
129. Sugiarto H Yu PL (2004) Avian antimicrobial peptides: the defense role of beta-defensins. Biochem Bioph Res Co 323 : 721 727. (Pubitemid 39243378)
130. Takase K, Nakayama T, Kawai T Fujikawan H (1999) Growth of Salmonella Typhimurium and Salmonella Enteritidis in egg yolks from highly immunized hens. J Vet Med Sci 61 : 959 960. (Pubitemid 129578200)
131. Thiagarajan D, Saeed AM Asem EK (1994) Mechanism of transovarian transmission of Salmonella Enteritidis in laying hens. Poultry Sci 73 : 89 98.
132. Thiagarajan D, Saeed AM, Turek J Asem EK (1996a) In vitro attachment and invasion of chicken ovarian granulosa cells by Salmonella Enteritidis phage type 8. Infect Immun 64 : 5015 5021. (Pubitemid 26403955)
133. Thiagarajan D, Thacker HL Saeed AM (1996b) Experimental infection of laying hens with Salmonella Enteritidis strains that express different types of fimbriae. Poultry Sci 75 : 1365 1372. (Pubitemid 126454713)
134. Thomson NR, Clayton DJ, Windhorst D et al 2008) Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res 18 : 1624 1637.
135. Timoney JF, Shivaprasad HL, Baker RC Rowe B (1989) Egg transmission after infection of hens with Salmonella Enteritidis phage type 4. Vet Rec 125 : 600 601.
136. Vazquez-Torres A, Jones-Carson J, Baumler AJ, Falkow S, Valdivia R, Brown W, Le M, Berggren R, Parks WT Fang FC (1999) Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401 : 804 808.
137. Wigley P, Berchieri A, Page KL, Smith AL Barrow PA (2001) Salmonella enterica serovar Pullorum persists in splenic macrophages and in the reproductive tract during persistent, disease-free carriage in chickens. Infect Immun 69 : 7873 7879. (Pubitemid 33086619)
138. Williams A, Davies AC, Wilson J, Marsh PD, Leach S Humphrey TJ (1998) Contamination of the contents of intact eggs by Salmonella Typhimurium DT104. Vet Rec 143 : 562 563. (Pubitemid 128489886)
139. Williams JE, Dillard LH Hall GO (1968) The penetration patterns of Salmonella Typhimurium through the outer structures of chickens eggs. Avian Dis 12 : 645 649.
140. Wong-Liong HW, Frank JF Bailey S (1997) Visualization of eggshell membranes and their interaction with Salmonella Enteriditis using confocal scanning laser microscopy. J Food Protect 60 : 1022 1028. (Pubitemid 27416046)
141. Yoshimura Y, Ohashi H, Subedi K, Nishibori M Isobe N (2006) Effects of age, egg-laying activity and Salmonella inoculation on the expression of gallinacin mRNA in the vagina of the hen oviduct. J Reprod Develop 52 : 211 218.
142. Zhou D, Mooseker MS Galan JE (1999) Role of the Salmonella Typhimurium actin-binding protein SipA in bacterial internalization. Science 283 : 2092 2095.