Toward better control of salmonella contamination by taking advantage of the egg's self-defense system: A review

Journal of Food Science

Volumn 76, Issue 3, 2011, Pages

  Zhang, Wei ^a   Zheng, Jiang Xia ^a   Xu, Gui Yun ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Egg safety; Egg's self protection mechanism; Salmonellacontrol; Salmonellatransmission

Indexed keywords

ANIMAL; ANIMAL HUSBANDRY; ARTICLE; CHICKEN; EGG; FEMALE; FOOD HANDLING; GROWTH, DEVELOPMENT AND AGING; HUMAN; MALE; METHODOLOGY; MICROBIOLOGY; PHYSIOLOGY; SALMONELLA; SALMONELLA FOOD POISONING;

ANIMAL HUSBANDRY; ANIMALS; CHICKENS; EGGS; FEMALE; FOOD HANDLING; HUMANS; MALE; SALMONELLA; SALMONELLA FOOD POISONING;

AVES; BACTERIA (MICROORGANISMS); COLEOPTERA; RODENTIA; SALMONELLA;

EID: 79955037337     PISSN: 00221147     EISSN: 17503841     Source Type: Journal    
DOI: 10.1111/j.1750-3841.2011.02053.x     Document Type: Article

References (89)

1. Ahlborn GJ, Clare DA, Sheldon BW, Kelly RW. 2006. Identification of eggshell membrane proteins and purification of ovotransferrin and β-NAGase from hen egg white. Protein J 25:71-81.
2. Back JF, Bain JM, Vadehra DV, Burley RW. 1982. Proteins of the outer layer of the vitelline membrane of hen's eggs. Biochim Biophys Acta 705(1):12-19.
3. Baker JR, Balch DA. 1962. A study of the organic material of hen's eggshell. Biochem J 82:352-61.
4. Ball HR, Meester FD, Schuman JD, inventors; Michael Foods, Inc., assignee. 2002 Sep 24. Treatment of food products using humidity controlled air. U.S. patent 6455094 B1.
5. Baron F, Gautier M, Brule G. 1997. Factors involved in the inhibition of growth ofSalmonellaEnteritidis in liquid egg white. J Food Prot 60:1318-23.
6. Barrow PA. 1992. Further observations on the serological response to experimentalSalmonellaTyphimurium in chicken measured by ELISA. Epidemiol Infect 108:231-41.
7. Bialka KL, Demirci A, Knabel SJ, Patterson PH, Puri VM. 2004. Processing and products efficacy of electrolyzed oxidizing water for the microbial safety and quality of eggs. Poult Sci 83:2071-8.
8. Cabeza MC, García ML, Hoz Ldl, Cambero I, Ordoñez JA. 2005. Destruction ofSalmonellaSenftenberg on the shells of intact eggs by thermoultrasonication. J Food Protect 68:841-4.
9. Cabeza MC, Ordóñez JA, Cambero I, Hoz Ldl, García ML. 2004. Effect of thermoultrasonication onSalmonella entericaserovar in distilled water and intact eggs to achieve its elimination from shell. J Food Protect 67:1886-91.
10. Carrique-Mas JJ, Breslin M, Sayers AR, Mclaren L, Arnold M, Davies R. 2008. Comparison of environmental sampling methods for detectingSalmonellain commercial laying flocks in the UK. Lett Appl Microbiol 47:514-9.
11. Carrique-Mas JJ, Breslin M, Snow L, McLaren I, Sayers AR. 2009. Persistence and clearance of differentSalmonellaserovars in buildings housing laying hens. Epidemiol Infect 137:837-46.
12. CDC. 2010. Investigation update: multistate outbreak of humanSalmonellaEnteritidis infections associated with shell eggs. Available from: Accessed Dec 2, 2010.
13. Chousalkar KK, Flynn P, Sutherland M, Roberts JR, Cheetham BF. 2010. Recovery ofSalmonellaandEscherichia colifrom commercial shell eggs and effect of translucency on bacterial penetration in eggs. Int J Food Microbial 142:207-213.
14. Clavijo RI, Loui C, Andersen GL, Riley LW, Lu S. 2006. Identification of genes associated with survival ofSalmonella entericaserovar in chicken egg albumen. Appl Environ Microbiol 72:1055-64.
15. Clay CE, Board RG. 1991. Growth ofSalmonellaEnteritidis in artificially contaminated hens' shell eggs. Epidemiol Infect 106:271-81.
16. Cogan TA, Jorgensen F, Lappin-Scott HM, Benson CE, Woodward MJ, Humphrey TJ. 2004. Flagella and curli fimbriae are important for the growth ofSalmonella entericaserovars in hen eggs. Microbiology 150:1063-71.
17. Commission of the European Communities. 2003. COM (2003) 479 final. Report from the commission to the council with regard to developments in consumption, washing and marking of eggs. Available from: Accessed Jun 8, 2003.
18. Davidson LJ, Wagner MA, inventors; Davidson Food Co., assignee. 2004 Jul 11. Pasteurized eggs. U.S. patent 20020090429 A1.
19. De Reu K, Messens W, Heyndrickx M, Rodenburg TB, Uyttendsele M, Herman L. 2008. Bacterial contamination of table eggs and the influence of housing systems. World's Poultry Sci J 64:5-19.
20. EFSA. 2004. Opinion of the scientific panel on biological hazards on the requests from the commission related to the use of vaccines for the control ofSalmonellain poultry. EFSA J 114:1-74.
21. EFSA. 2005. Opinion of the scientific panel on biological hazards on the request from the commission related to the microbiological risks on washing of table eggs. EFSA J 269:1-39.
22. EFSA. 2009. Scientific opinion of the panel on biological hazards on special measures to reduce the risk of consumers throughSalmonellain table eggs-e.g. cooling of table eggs. EFSA J 957:1-29.
23. FDA. 2010. New FDA regulations forSalmonellatesting in commercial layer. Available from: Accessed Jul 9, 2010.
24. FEHD. 2004. Salmonellain eggs and egg products. Hong Kong Food and Environmental Hygiene Dept. p 20. Available from: Accessed Dec 2004.
25. Fromm D. 1966. The influence of ambient PH on the moisture content and yolk index of the hens yolk. Poult Sci 45:234-41.
26. Fromm D. 1967. Some physical and chemical changes in the vitelline membrane of the hen's egg during storage. J Food Sci 32:52-6.
27. FSIS. 2005. Risk assessments ofSalmonellain shell eggs andSalmonellaspp. in egg products. Available from: Accessed Oct 2005.
28. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Gast R, Humphrey TJ, Immerseel FV. 2009. Mechanisms of egg contamination bySalmonella. FEMS Micobiol Rev 33:718-38.
29. Gast RK. 1994. UnderstandingSalmonellain laying chickens: the contributions of experimental infections. Int J Food Microbiol 21:107-16.
30. Gast RK, Holt PS. 1998. Persistence ofSalmonellaEnteritidis from one day of age until maturity in experimentally infected layer chickens. Poult Sci 77:1759-62.
31. Gast RK, Holt PS. 2000. Influence of the level and location of contamination on the multiplication ofSalmonellaEnteritidis at different storage temperatures in experimentally inoculated eggs. Poult Sci 79:559-63.
32. 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 ofSalmonellaandSalmonellaHeidelberg. Avian Dis 49:382-6.
33. Gast RK, Holt PS, Murase T. 2005b. Penetration ofSalmonellaEnteritidis andSalmonellaHeidelberg into egg yolks in a vitro contamination model. Poult Sci 84:621-5.
34. Gurtler JB, Conner DE. 2009. Survival and growth ofSalmonellaEnteritidis in liquid egg products varying by temperature, product composition and carbon dioxide concentration. Foodborne Pathog Dis 6:561-7.
35. Hasan MN, Ara N, Mamun SA, Rahman MM, Rahman MH. 2009. Prevalence ofSalmonellaspp. in chicken egg from Khulna city. J Innov Dev Strategy 3:1-6.
36. Hierro E, Manzano S, Ordóñez JA, Hoz Ldl, Fernández M. 2009. Inactivation ofSalmonella entericaserovar on shell eggs by pulsed light technology. Int J Food Microbiol 135:125-30.
37. Hou H, Singh RK, Muriana PM, Stadelman WJ. 1996. Pasteurization of intact shell eggs. Food Microbiol 13:93-101.
38. Humphrey TJ, Baskerville A, Mawer S, Rowe B, Hopper S. 1989. SalmonellaEnteritidis phage type 4 from the contents of intact eggs: a study involving naturally infected hens. Epidemiol Infect 103:415-23.
39. Humphrey TJ, Whitehead A. 1993. Egg age and the growth ofSalmonellaEnteritidis PT4 in egg contents. Epidemiol Infect 111:209-19.
40. Hutchison ML, Gittins J, Walker A, Sparks N, Humphrey TJ, Burton C, Moore A. 2004. An assessment of the microbiological risks involved with egg washing under commercial conditions. J Food Prot 67:4-11.
41. Jones DR, Musgrove MT. 2005. Effects of extended storage on egg quality factors. Poult Sci 84:1774-7.
42. Kang H, Loui C, Clsvijo RI, Riley LW, Lu S. 2006. Survival characteristics ofSalmonella entericaserovar in chicken egg albumen. Epidemiol Infect 134:967-76.
43. Kapperud G, Gustavsen S, Hellesnes I, Hansen AH, Lassen J, Him J, Jahkola M, Montenegro MA, Helmuth R. 1990. Outbreak ofSalmonellaTyphimurium infection trace to contaminated chocolate and caused by a strain lacking the 60-megadalton virulence plasmid. J Clin Microbiol 28:2597-601.
44. Keener KM, LaCrosse JD, Curtis PA, Anderson KE, Farkas BE. 2000a. Subsequent storage in air and carbon dioxide on shell egg quality. Poult Sci 79:1067-71.
45. Keener KM, Lacrosse JD, Farkas BE, Curtis PA, Anderson KE. 2000b. Gas exchange into shell eggs from cryogenic cooling. Poult Sci 79:275-80.
46. Keller LH, Benson CE, Krotec K, Eckroade RJ. 1995. Salmonellacolonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect Immun 63:2443-9.
47. Kido S, Janado M, Nunoura H. 1975. Macromolecular components of the vetelline membrane of hen's egg. I. Menbrane structure and its deterioration with age. J Biochem 78:261-8.
48. Kido S, Morimoto A, Kim F, Doi Y. 1992. Isolation of a novel protein from the outer layer of the vitelline membrane. Biochem J 286:17-22.
49. Kinderlerer JL. 1994. Salmonellain eggs. BNF Nutrition Bull 19:11-8.
50. Kirunda DFK, McKee SR. 2000. Relating quality characteristics of aged and fresh eggs to vitelline membrane strength as determined by a texture analyzer. Poult Sci 79:1189-93.
51. Knape KD, Carey JB, Ricke SC. 2001. Response of foodborneSalmonellaspp. marker strains inoculated on egg shell surfaces to disinfectants in a commercial egg washer. J Environ Sci Health 36:219-27.
52. Kraft AA, Mcnally EH, Brant AW. 1958. Shell quality and bacterial infection of shell eggs. Poult Sci 37:638-44.
53. Leleu S. 2009. Penetration ofSalmonellaEnteritidis through the vitelline membrane of hen's eggs as affected by its strength during the laying period. XIII European Symposium on the Quality of Eggs and Egg Products; 2009 June 21-25. Turku, Finland: WPSA.
54. Lin C-TJ, Morales RA, Ralston K. 1997. Raw and undercooked eggs: a danger of salmonellosis. Food Saf 20:27-32.
55. Little CL, Surman-Lee S, Greenwood M, Bolton FJ, Elson R, Mitchell RT, Nichols GN, Sagoo SK, Threlfall EJ, Ward LR, Gillespie IA, O'Brien S. 2007. Public health investigations ofSalmonellaEnteritidis in catering raw shell eggs, 2002-2004. Lett Appl Microbiol 44:595-601.
56. Liu X. 2008. Isolation and Identification ofSalmonellafrom eggs and biological characteristics. [MSc dissertation]. Mongolia Mongolia Agricultural Univ. 45 p.
57. Lu S, Killoran PB, Riley LW. 2003. Association ofSalmonella entericaserovar YafD with resistance to chicken egg albumen. Infect Immun 71:6734-41.
58. Lublin A, Sela S. 2008. The impact of temperature during the storage of table eggs on the viability ofSalmonella entericaserovars and Virchow in the eggs. Poult Sci 87:2208-14.
59. Lynch M, Painter J, Woodruff R, Braden C. 2006. Surveillance for foodborne-disease outbreaks-United States, 1998-2002. Surveill Summ 55(SS10):1-34.
60. Messens W. 2009. Effect of egg washing on the cuticle of table eggs. XIII European symposium on the quality of eggs and egg products; 2009 June 21-25. Turku, Finland: WPSA.
61. Messens W, Duboccage L, Grijspeerdt K, Heyndrickx M, Herman L. 2004. Growth ofSalmonellaserovars in hens' egg albumen as affected by storage prior to inoculation. Food Microbiol 21:25-32.
62. Messens W, Grijspeerdt K, Herman L. 2005a. Eggshell characteristics and penetration bySalmonella entericaserovar through the production period of a layer flock. Br Poult Sci 46:694-700.
63. Messens W, Grijspeerdt K, Herman L. 2005b. Eggshell penetration bySalmonella: a review. World's Poultry Sci J 61:71-82.
64. Messens W, Grijspeerdt K, Herman L. 2006. Eggshell penetration of hen's eggs bySalmonella entericaserovar upon various storage conditions. Br Poult Sci 47(5):554-60.
65. Mudau MS. 2007. Functional properties of microwave pasteurized and oil coated whole shell eggs. [MSc dissertation]. South Africa: Univ. of Pretoria. 111 p.
66. Murase T, Holt P, Gast RK. 2005. Growth ofSalmonella entericaserovar Enteritidis in albumn and yolk contents of eggs inoculated with this organism onto the vitelline membrane. J Food Protect 68:718-21.
67. Nakamura M, Nagamine N, Takahashi T, Suzuki S, Kijima M, Tamura Y, Sato S. 1994. Horizontal transmission ofSalmonellaand effect of stress on shedding in laying hens. Avian Dis 38:282-8.
68. Nascimento VP, Cranstoun S, Solomon SE. 1992. Relationship between shell structure and movement ofSalmonellaEnteritidis across the eggshell wall. Br Poult Sci 33:37-48.
69. Ngoka DA, Froning GW, Babji AS. 1983. Effect of temperature on egg yolk characteristics of eggs from young and old laying hens. Poult Sci 62:718-720.
70. Omwandho COA, Kubota T. 2010. Salmonella entericaserovar: a mini-review of contamination routes and limitations to effective control. Jpn Agr Res Quart 44:7-16.
71. Pasquali F. 2009. Hot air treatment for surface decontamination of table eggs. Food Control 21:431-5.
72. Peebles ED, Brake JT. 1986. The role of the cuticle in water vapor conductance by the eggshell of broiler breeders. Poult Sci 65:1034-9.
73. Piyasena P, Mohareb E, McKellar RC. 2003. Inactivation of microbes using ultrasound: a review. Int J Food Microbiol 87:207-16.
74. Radkowski M. 2002. Effect of moisture and temperature on survival ofSalmonellaon shell eggs. Arch Geflugelkd 66:119-23.
75. Ragni L, Berardinelli A, Vannini L, Montanari C, Sirri F, Guerzoni ME, Guarnieri A. 2010. Non-thermal atmospheric gas plasma device for surface decontamination of shell eggs. J Food Eng 100:125-32.
76. Rizk SS, Ayres JC, Kraft AA. 1996. Effect of holding condition on the development ofSalmonellain artificially inoculated hens' eggs. Poult Sci 45:825-9.
77. Rodríguez Romo LA. 2004. Control ofSalmonella entericaserovar in shell eggs by ozone, ultraviolet radiation, and heat. [DPhil dissertation]. Ohio Ohio State Univ. 185 p.
78. Russell SM. 2003. The effect of electrolyzed oxidative water applied using electrostatic spraying on pathogenic and indicator bacteria on the surface of eggs. Poult Sci 82:158-62.
79. Sabliov CM, Farkas BE, Keener KM, Curtis PA. 2002. Cooling of shell egg with cryogenic carbon dioxide: a finite element analysis of heat transfer. Lebensm-Wiss Technol 35:568-74.
80. Schade AL, Caroline L. 1944. Raw hen egg white and the role of iron in growth inhibition ofShigella dysenteriae, Staphylococcus aureus, Escherichia coliandSaccharomyces cerevisiae. Science 100(1944):14-5.
81. Schuman JD, Sheldon BW, Vandepopuliere JM, Ball Jr HR. 1997. Immersion heat treatments for inactivation ofSalmonellawith intact eggs. J Appl Microbiol 83:438-44.
82. Scott TA, Silversides FG. 2000. The effect of storage and strain of hen on egg quality. Poult Sci 79:1725-9.
83. Shivaprasad HL, Timoney JF, Morales S, Lucio B, Baker RC. 1990. Pathogenesis ofSalmonellaEnteritidis infection in laying chickens. I. Studies on egg transmission, clinical signs, fecal shedding, and serologic responses. Avian Dis 34:548-57.
84. Sivaramakrishnan SR. 2007. Microwave pasteurization of shell eggs-a preclude. [MSc dissertation]. Quebec McGill Univ. 88 p.
85. Thompson JF, Knutson J. 2000. Rapid cooling of shell eggs. J Appl Poultry Res 9:258-68.
86. USDA. 2010. USDA, AMS, Poultry market news and analysis weekly egg products report october 15, 2010. The "source" of poultry and egg market information. Available from: Accessed Oct 15, 2010.
87. Vought KJ, Tatini SR. 1998. SalmonellaEnteritidis contamination of ice cream associated with a 1994 multistate outbreak. J Food Prot 61:5-10.
88. Williams JE, Dillard LH, Hall GO. 1968. The penetration patterns ofSalmonellaTyphimurium through the outer structures of chicken eggs. Avian Dis 12:445-66.
89. Worley BS, Wheatley WB, Lauten SD, Williams DE, Mora EC, Worley SD. 1992. Inactivation ofSalmonellaon shell eggs by novel N-halamine biocidal compounds. J Ind Microbiol 11:37-42.