The impact of temperature during the storage of table eggs on the viability of Salmonella enterica serovars enteritidis and virchow in the eggs

Poultry Science

Volumn 87, Issue 11, 2008, Pages 2208-2214

  Lublin, A ^a   Sela, S ^b  

^a KIMRON VETERINARY INSTITUTE   (Israel)

^b VOLCANI CENTER   (Israel)

Author keywords

Salmonella enterica serovar Enteritidis; Salmonella enterica serovar Virchow; Salmonellosis; Storage temperature; Table egg

Indexed keywords

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS;

EID: 55749097647     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2008-00153     Document Type: Article

References (39)

1. Alice, A. 1985. SAS User's Guide: Statistics. Version 5 ed. SAS Institute Inc., Cary, NC,
2. Baumler, A. J., B. M. Hargis, and R. M. Tsolis. 2000. Tracing the origins of Salmonella outbreaks. Science 287:50-52.
3. Bignardi, G. E., and T. Y. Khong. 1989. Immunohistological demonstration of Salmonella Virchow in infant death. J. Clin. Pathol. 42:329-330.
4. Braun, P., K. Fehlhaber, and A. Wicke. 1999. Salmonella Enteritidis invades the egg through the shell. World Poult. Spec. 11:23-24.
5. Chen, J., R. Clarke, and M. W. Griffiths. 1996. Penetration of Salmonella Enteritidis through whole-shell eggs and survival of the bacteria in whole-liquid egg during refrigeration storage. J. Food Prot. 59:915-921.
6. Chen, J., H. S. Thesmar, and W. L. Kerr. 2005. Outgrowth of Salmonellae and the physical property of albumen and vitelline membrane as influenced by egg storage conditions. J. Food Prot. 68:2553-2558.
7. Cogan, T. A., G. Domingue, H. M. Lappin-Scott, C. E. Benson, M. J. Woodward, and T. J. Humphrey. 2001. Growth of Salmonella Enteritidis in artificially contaminated eggs: The effects of inoculum size and suspending media. Int. J. Food Microbiol. 70:131-141.
8. Coughlin, L. B., J. McGuigan, N. G. Haddad, and P. Mannion. 2003. Salmonella sepsis and miscarriage. Clin. Microbiol. Infect. 9:866-868.
9. Durecko, R., D. Saladiova, P. Popelka, and I. Simanska. 2004. Epidemiological and epizootological aspects of salmonellosis. Bratisl. Lek Listy (Tlacene Vyd) 105:414-418.
10. Ebel, E., and W. Schlosser. 2002. Estimating the annual fraction of eggs contaminated with Salmonella Enteritidis in the United States. Int. J. Food Microbiol. 61:51-62.
11. Fierer, J., and M. Swancutt. 2000. Non-typhoid Salmonella: A review. Curr. Clin. Top. Infect. Dis. 20:134-157.
12. Gast, R. K., and P. S. Holt. 2000. 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.
13. Gast, R. K., and P. S. Holt. 2001. Multiplication in egg yolk and survival in egg albumen of Salmonella enterica serotype Enteritidis strains of phage types 4, 8, 13a, and 14b. J. Food Prot. 64:865-868.
14. Guard-Petter, J. 2001. The chicken, the egg and Salmonella Enteritidis. Environ. Res. 3:421-430.
15. Himathongkham, S., H. Riemann, and R. Ernst. 1999. Efficacy of disinfection of shell eggs externally contaminated with Salmonella Enteritidis. Implication for egg testing. Int. J. Food Microbiol. 49:161-167.
16. Howard, Z. R., R. W. Moore, I. B. Zabala Diaz, W. K. Kim, S. G. Birkhold, J. A. Byrd, L. F. Kubena, D. J. Nisbet, and S. C. Ricke. 2006. In vitro survival and growth of Salmonella Typhimurium inoculated on yolk membrane after long term refrigerated storage of shell eggs. J. Verbraucher. Lebensmittel. 1:28-32.
17. Humphrey, T. J., A. Whitehead, A. H. L. Gawler, A. Henley, and B. Rowe. 1991. Numbers of Salmonella Enteritidis in the contents of naturally contaminated hens' eggs. Epidemiol. Infect. 106:489-496.
18. Kinderlerer, J. L. 1994. Salmonella in eggs. Br. Nutr. Found. Nutr. Bull. 19:11-18.
19. Little, C. L., S. Surman-Lee, M. Greenwood, F. J. Bolton, R. Elson, R. T. Mitchell, G. N. Nichols, S. K. Sagoo, E. J. Threlfall, L. R. Ward, I. A. Gillespie, and S. O'Brien. 2007. Public health investigations of Salmonella Enteritidis in catering raw shell eggs, 2002-2004. Lett. Appl. Microbiol. 44:595-601.
20. Maris, D., D. Twillie, R. Johnson, R. L. Haberberger, S. R. Hinten, K. J. Giese, and R. Finnegan. 1998. An egg-associated outbreak of Salmonella Virchow among U.S. Army troops stationed in Dhahran, Saudi Arabia. New Mexicans for Science and Reasoning 1:15-18.
21. Martín, M., C. Gonzalez-Hevia, J. A. Alvarez-Riesgo, and M. C. Mendoza. 2001. Salmonella serovar Virchow causing salmonellosis in a Spanish region. Characterization and survey of clones by DNA fingerprinting, phage typing and antimicrobial resistance. Eur. J. Epidemiol. 17:31-40.
22. Messens, W., K. Grijspeerdt, and L. Herman. 2005. Eggshell penetration by Salmonella: A review. World's Poult. Sci. J. 61:71-85.
23. Miyamoto, T., T. Horie, E. Baba, K. Sasai, T. Fukata, and A. Arakawa. 1998. Salmonella penetration through eggshell associated with freshness of laid eggs and refrigeration. J. Food Prot. 61:350-353.
24. Mrden, M., M. Gagic, and M. Glavicic. 1988. Isolation of Salmonella Virchow from eggs and embryos. Peradarstvo 23:237-238.
25. Neill, S. D., J. N. Campbell, and J. J. O'Brien. 1985. Egg penetration of Campylobacter jejuni. Avian Pathol. 14:313-320.
26. Padron, M. 1990. Salmonella Typhimurium penetration through the eggshell of hatching eggs. Avian Dis. 34:463-465.
27. Patrick, M. E., P. M. Adcock, T. M. Gomez, S. F. Altekruse, B. H. Holland, R. V. Tauxe, and D. L. Swerdlow. 2004. Salmonella Enteritidis infections, United States, 1985-1999. Emerging Infectious Diseases. http://www.cdc.gov/ncidod/EID/vol10no1/02-0572.htm Accessed Jan. 2004.
28. Rabsch, W., H. Tschape, and A. J. Baumler. 2001. Non-typhoidal salmonellosis: Emerging problems. Microbes Infect. 3:237-247.
29. UDSA-FSIS. 2005. Risk Assessments for Salmonella Enteritidis in shell eggs and Salmonella spp. in egg products, 2005. Available from http://www.fsis.usda.gov/PDF/SE_Risk_Assess_ExecSumm_Oct2005.pdf Accessed Oct. 2005.
30. Saeed, A. M. 1998. The impact of Salmonella Enteritidis on public health and environmental quality. Pages 544-554 in Proc. 102nd Annu. Mtg. United States Anim. Health Assoc., Minneapolis, MN. USAHA Committee on Public Health and Environmental Quality, Minneapolis, MN.
31. Saeed, A. M., and C. W. Koons. 1993. Growth and heat resistance of Salmonella Enteritidis in refrigerated and abused eggs. J. Food Prot. 56:927-931.
32. Schoeni, J. L., K. A. Glass, J. L. McDermott, and A. C. Wong. 1995. Growth and penetration of Salmonella Enteritidis, Salmonella Heidelberg and Salmonella Typhimurium in eggs. Int. J. Food Microbiol. 24:385-396.
33. Schroeder, C. M., A. L. Naugle, W. D. Schlosser, A. T. Hogue, F. J. Angulo, J. S. Rose, E. D. Ebel, W. T. Disney, K. G. Holt, and D. P. Goldman. 2005. Estimate of illnesses from Salmonella Enteritidis in eggs, United States, 2000. Emerging Infectious Diseases. Online: http://www.cdc.gov/ncidod/ EID/vol11no01/04-0401.htm Accessed Jan. 2005.
34. Suryana, A., and I. F. Istiana. 1997. Bacteriological examinations of ducklings, duck's eggs, feed, and rice bran collected from Alabio market, South Kalimantan. J. IlmuTernak Veter. 2:208-211.
35. Usera, M. A., A. Echeita, A. Aladuena, M. C. Blanco, R. Reymundo, M. I. Prieto, O. Tello, R. Cano, D. Herrera, and F. Martinez-Navarro. 1996. Interregional foodborne salmonellosis outbreak due to powdered infant formula contaminated with lactose-fermenting Salmonella Virchow. Eur. J. Epidemiol. 12:377-381.
36. Usera, M. A., A. Rodriguez, A. Echeita, and R. Cano. 1998. Multiple analysis of a foodborne outbreak caused by infant formula contaminated by an atypical Salmonella Virchow strain. Eur. J. Clin. Microbiol. Infect. Dis. 17:551-555.
37. Weinberger, M., and N. Keller. 2005. Recent trends in the epidemiology of non-typhoid Salmonella and antimicrobial resistance: The Israeli experience and worldwide review. Curr. Opin. Infect. Dis. 18:513-521.
38. Weinberger, M., H. Solnik-Isaac, D. Shachar, A. Reisfeld, L. Valinsky, N. Andorn, V. Agmon, R. Yishai, R. Bassal, A. Fraser, S. Yaron, and D. Cohen. 2006. Salmonella enterica serovar Virchow: Epidemiology, resistance patterns and molecular characterization of an invasive Salmonella serovar in Israel. Clin. Microbiol. Infect. 12:999-1005.
39. Yang, S.-E., R.-C. Yu, and C.-C. Chou. 2001. Influence of holding temperature on the growth and survival of Salmonella spp. and Staphylococcus aureus and the production of staphylococcal enterotoxin in egg products. Int. J. Food Microbiol. 63:99-107.