Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-28T17:59:47.625Z Has data issue: false hasContentIssue false

Microbiological challenges of poultry egg production in the US

Published online by Cambridge University Press:  25 June 2007

P. CURTIS
Affiliation:
Poultry Products Safety & Quality Peaks of Excellence Program, Department of Poultry Science, 201 Poultry Science Building, 260 Lem Morrison Drive, Auburn University, Auburn, Alabama, 36849, USA E-mail: Pat_Curtis@auburn.edu
Get access

Abstract

Over the past 40 years there have been many changes in egg production and processing, as well as, the egg itself. Many of these changes have contributed to the microbial challenges of the egg that we face today. Salmonella enterica serovar Enteritidis (SE) and more recently Salmonella enterica serovar Heidelberg (SH) are the two organisms of most concern associated with eggs. Most U. S. egg producers utilize some type of control programme to ensure egg safety. Many use the United Egg Producers' “5-Start” Food Safety Programme. Commercial egg washing significantly reduced concentrations of aerobic bacteria, yeasts and moulds, Enterobacteriaceae, and E. coli on shell egg surfaces. However, refrigeration of eggs is often identified as one the most critical issues in minimizing the risks associated with Salmonella contamination in eggs. The condensation question always arises any time egg refrigeration is discussed. Moisture often condenses on the shell surface when cold eggs are moved from the cool storage into hot and/or humid conditions. Research has shown that the ability of any microbes present on the shell to penetrate the shell was not increased with egg sweating. Also, heat sensitivity of SE can be induced by exposure to low temperatures. Although low numbers of SE and SH can contaminate eggs via the transovarian or shell penetration route, these small numbers cannot be ignored. Storage at temperatures as low 4°C combined with natural defences does not completely prevent growth. Furthermore, rapid growth occurs at 25°C, so minimal temperature abuse could result in high levels of contamination within eggs. The need for proper management during production, properly controlled storage, cooking and serving is critical.

Type
Review Article
Copyright
Copyright © World's Poultry Science Association 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

ANDERSON, K. E., JONES, F. T. and CURTIS, P. A. (1992) Heat loss from commercially packed eggs in postprocessing coolers. North Carolina State Cooperative Extension Service Report Vol. I, ER-1, Raleigh, NC, pp. 3.Google Scholar
BARNHART, H. M., DREESEN, D. W., BASTIEN, R. and 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: 488491.CrossRefGoogle ScholarPubMed
BARON, F. M., GAUTIER, M. and BRULE, G. (1997) Factors involved in the inhibition of growth of Salmonella enteritidis in liquid egg white. Journal of Food Protection 60: 13181323.CrossRefGoogle ScholarPubMed
BRANT, A. W. and STARR, P. B. (1962) Some physical factors related to egg spoilage. Poultry Science 41: 14681473.CrossRefGoogle Scholar
BRAUN, P. and FEHLHABER, K. (1995) Migration of Salmonella enteritidis from the albumen into the egg yolk. International Journal of Food Microbiology 25: 9599.CrossRefGoogle ScholarPubMed
CHEN, H., ANANTHESWARAN, R. C. and KNABEL, S. J. (2002) Effect of rapid cooling on the growth and penetration of Salmonella enteritidis into egg contents. Journal of Food Safety 22: 255271.CrossRefGoogle Scholar
CHITTICK, P., SULKA, A., TAUXE, R. V. and FRY, A. M. (2004) Outbreaks of Salmonella heidelberg infections in the United States: Are eggs a common source? Proceedings of the International Conference on Emerging Infectious Diseases, Atlanta, GA. 179.Google Scholar
CLAY, C. E. and BOARD, R. G. (1991) Growth of Salmonella enteritidis in artificially contaminated hens’ shell eggs. Epidemiology of Infection 106: 271281.CrossRefGoogle ScholarPubMed
COGAN, T. A., JORGENSEN, F., LAPPIN-SCOTT, H. M., BENSON, C. E., WOODWARD, M. J. and HUMPHREY, T. J. (2001) Growth of Salmonella enteritidis in artificially contaminated eggs: The effect of inoculum size and suspending media. International Journal of Food Microbiology 70: 131141.CrossRefGoogle ScholarPubMed
CORRY, J. E. L. and BARNES, E. M. (1968) The heat resistance of salmonellae in egg albumen. British Poultry Science 9: 253260.CrossRefGoogle ScholarPubMed
CURTIS, P. A., ANDERSON, K. E. and JONES, F. T. (1995) Cryogenic gas for rapid cooling of commercially processed shell eggs before packaging. Journal of Food Protection 58(4): 389394.CrossRefGoogle ScholarPubMed
CURTIS, PA., ANDERSON, K. E., JONES, F. T., THARRINGTON, J. B. and JONES, D. R. (2003) How much has the table egg changed over last 40 years? Xth European Symposium on the Quality of Eggs and Egg Products Proceedings, Saint-Brieuc, France.Google Scholar
DABBAH, R., MOATS, W. A. and EDWARDS, V. M. (1971) Survivor curves of selected Salmonella enteritidis serotypes in liquid whole egg homogenates at 60°C. Poultry Science 50: 17721776.CrossRefGoogle Scholar
DOYLE, M. P. and CLIVER, D. O. (1990) Salmonella. In. Cliver, D. O. (editor) Food Diseases. Academic Press, San Diego, CA, pp. 185204.Google Scholar
ERNST, R. A., FUQUA, L., RIEMANN, H. P. and HIMATHONGKHAM, S. (1998) Effect of sweating on shell penetration of Salmonella enteritidis. Journal of Applied Poultry Research 7: 8184.CrossRefGoogle Scholar
FUNK, E. M. (1935) The cooling of eggs. Missouri Agricultural Experiment Station Bulletin, No. 350.Google Scholar
GAST, R. K. and BEARD, C. W. (1990) Production of Salmonella enteritidis-contaminated eggs by experimentally infected hens. Avian Disease 34: 438446.CrossRefGoogle ScholarPubMed
GAST, R. K. and BEARD, C. W. (1992) Detection and enumeration of Salmonella enteritidis in fresh and stored eggs laid by experimentally infected hens. Journal of Food Protection 55: 152156.CrossRefGoogle ScholarPubMed
GAST, R. K., GUARD-BOULDIN, J. and HOLT, P. S. (2004) Colonization of reproductive organs and internal contamination of eggs after experimental infection of laying hens with Salmonella heidelberg and Salmonella enteritidis. Avian Disease 48: 863869.CrossRefGoogle ScholarPubMed
GAST, R. K. and HOLT, P. S. (2000a) The relationship between the magnitude of the specific antibody response to experimental Salmonella enteritidis strains in the yolk and albumen of eggs laid by experimentally infected hens. Avian Disease 44: 706710.CrossRefGoogle Scholar
GAST, R. K. and HOLT, P. S. (2000b) Influence of the level and location of contamination on the multiplication of Salmonella enteritidis at different storage temperatures in experimentally inoculated eggs. Poultry Science 79: 559563.CrossRefGoogle ScholarPubMed
GAST, R. K., HOLT, P. S. and MURASE, T. (2005) Penetration of Salmonella enteritidis and Salmonella heidelberg into egg yolks in an in vitro contamination model. Poultry Science 84: 621625.CrossRefGoogle Scholar
GIRIBALDI, J. A. and STOKES, J. L. (1958) Protective Role of Shell Membranes in Bacterial Spoilage of Eggs. Food Research 23(1): 283290.CrossRefGoogle Scholar
HENNESSY, T. W., CHENG, L. H., KASSENBORG, H., AHUJA, S. D., MOHLE-BOETANI, J., MARCUS, R., SHIFERAW, B. and ANGULO, F. J. (2004) Egg consumption is the principle risk factor for sporadic Salmonella serotype Heidelberg infections: Acase control study in FoodNet sites. Clinical Infectious Diseases 38(Supplement 3): S237S243.CrossRefGoogle Scholar
HUGHES, L. A., CONNER, D. E., CURTIS, P. A. and KEENER, K. M. (1999) Effects of cryogenic cooling and traditional cooling on Salmonella enteritidis population in table eggs. International Association of Milk, Food, and Environmental Sanitarians Association Annual Meeting Proceedings. Abstract No. T41, IAMFES, Dearborne, MI.Google Scholar
HUMPHREY, T. J. (1990a) Growth of salmonellas in intact shell eggs: influence of storage temperature. Veterinary Record 126: 292.Google ScholarPubMed
HUMPHREY, T. J. (1990b) Heat resistance in Salmonella enteritidis phage type 4: The influence of storage temperatures before heating. Journal of Applied Bacteriology 69: 493497.CrossRefGoogle ScholarPubMed
HUMPREY, T. J., BASKERVILLE, A., MAWER, S., ROWE, B. and HOPPER, S. (1989a) Salmonella enteritidis phage type 4 from the contents of intact eggs: A study involving naturally infected hens. Epidemiology of Infection 103: 415423.CrossRefGoogle Scholar
HUMPREY, T. J., GREENWOOD, M., GILBERT, R. J., ROWE, B. and CHAPMAN, P. A. (1989b) The survival of salmonellas in shell eggs cooked under simulated domestic conditions. Epidemiology of Infection 102: 3545.CrossRefGoogle Scholar
HUMPHREY, T. J., RICHARDSON, N. P., GAWLER, A. H. L. and ALLEN, M. A. (1991) Heat resistance in Salmonella enteritidis PT4 and the influence of prior exposure to alkaline conditions. Letters in Applied Microbiology 12: 258260.CrossRefGoogle Scholar
HUMPHREY, T. J., RICHARDSON, N. P., STATTON, K. M. and ROWBURY, R. J. (1993) Effects of temperature shift on acid and heat tolerance in Salmonella enteritidis phage type 4. Applied Environmental Microbiology 59: 31203122.CrossRefGoogle ScholarPubMed
HUMPHREY, T. J. and WHITEHEAD, A. (1993) Egg age and the growth of Salmonella enteritidis in egg contents. Epidemiology of Infection 111: 209291.CrossRefGoogle ScholarPubMed
HUMPHREY, T. J., WHITEHEAD, A., GAWLER, A. H. L., HENLEY, A. and ROWE, B. (1991) Numbers of Salmonella enteritidis in the contents of naturally contaminated hens’ eggs. Epidemiology of Infection 106: 489496.CrossRefGoogle ScholarPubMed
JENKINS, D. E., SCHULTZ, J. E. and MATIN, A. (1998) Starvation induced cross protection against head and H2O2 challenge in Escherichia coli. Journal of Bacteriology 170: 39103914.Google Scholar
JONES, D. R., CURTIS, P. A., ANDERSON, K. E. and JONES, F. T. (2004) Microbial contamination in inoculated shell eggs: II. Effects of layer strain and egg storage. Poultry Science 83: 95100.CrossRefGoogle ScholarPubMed
JONES, D. R., THARRINGTON, J. B., CURTIS, P. A., ANDERSON, K. E., KEENER, K. M. and JONES, F. T. (2002) Effects of cryogenic cooling on shell eggs on egg quality. Poultry Science 81: 727733.CrossRefGoogle ScholarPubMed
KEENER, K. M., ANDERSON, K. E., CURTIS, P. A and FOEGEDING, J. B. (2004) Determination of cooling rates and carbon dioxide uptake in commercially processed shell eggs using cryogenic carbon dioxide gas. Poultry Science 83(1): 8994.CrossRefGoogle ScholarPubMed
KELLER, L. H., BENSON, C. E., KROTEC, K. and ECKROADE, R. J. (1995) salmonella enteritidis colonization of the reproductive tract and forming and freshly laid eggs in chickens. Infection and Immunity 63(7): 24432449.CrossRefGoogle ScholarPubMed
KIM, C. J., EMERY, D. A., RINKE, H., NAGARAJA, K. V. and HALVORSON, D. A. (1989) Effect of time and temperature n growth of Salmonella enteritidis in experimentally inoculated eggs. Avian Diseases 33: 735742.CrossRefGoogle Scholar
LIN, F. Y. C., MORRIS, J. G. JR., TRUMP, D., TILHGMAN, D., WOOD, P. K., JACKMAN, N., ISRAEL, E. and LIBONATI, J. P. (1988) Investigation of an outbreak of Salmonella enteritidis gastroenteritis associated will consumption of eggs in a restaurant chain in Maryland. American Journal of Epidemiology 128: 839844.CrossRefGoogle Scholar
LORENZ, F. W. and STARR, P. B. (1952) Spoilage of washed eggs: Effect of sprayed versus static water under different washing temperatures. Poultry Science 31:204213.CrossRefGoogle Scholar
LUCORE, L. A., JONES, F. T., ANDERSON, K. E. and CURTIS, P. A. (1997) Internal and external bacterial counts from shells of eggs washed in a commercial type processor at various wash water temperatures. Journal of Food Protection 60(11): 13241328.CrossRefGoogle Scholar
MACKEY, B. M. and DERRICK, C. M. (1986) Elevation of the heat resistance of Salmonella typhimurium by sublethal heat shock. Journal of Applied Bacteriology 61: 389393.CrossRefGoogle ScholarPubMed
MESSENS, W., DUBOCCAGE, L., GRIJSPEERDT, K., HEYNDRICKX, M. and HERMAN, L. (2004) Growth of Salmonella serovars in hens’ egg albumen as affected by storage prior to inoculation. Food Microbiology 21: 2532.CrossRefGoogle Scholar
MUSGOVE, M. T., JONES, D. R., NORTHCUTT, J. K., HARRISON, M. A. and COX, N. A. (2005) Impact of commercial processing on the microbiology of shell eggs. Journal of Food Protection 68(11): 23672375.CrossRefGoogle Scholar
PRESIDENT'S COUNCIL ON FOOD SAFETY (1999) Egg safety from production to consumption: An action plan to eliminate Salmonella Enteritidis illness due to eggs. National Academy of Science, Washington, D. C.Google Scholar
SAEED, A. M. and KOONS, C. W. (1993) Growth and heat resistance of Salmonella enteritidis in refrigerated and abused eggs. Journal of Food Protection 56(11): 927931.CrossRefGoogle ScholarPubMed
SCHOENI, J. L., GLASS, K. A., MCDERMOTT, J. L. and WONG, A. C. L. (1995) Growth and penetration of Salmonella enteritidis, Salmonella heidelberg and Salmonella typhimurium in eggs. International Journal of Food Microbiology 24: 385396.CrossRefGoogle ScholarPubMed
ST.LOUIS, M. F., MORSE, D. I., POTTER, M. F., DEMELFI, T. M., GUZEWICH, J. J., TAUXE, R. V. and BLAKE, P. A. (1988) The emergence of grade A eggs as a major source of Salmonella enteritidis infections. New implications for the control of salmonellosis. Journal of American Medical Association 259: 21032107.CrossRefGoogle Scholar
STADELMAN, W. J. and RHORER, A. R. (1987) Egg quality: Which is best— in-line or off-line production? Egg Industry 93: 810.Google Scholar
TRUSSELL, P. C. and FULTON, C. O. (1955) Bacterial Spoilage of Shell Eggs. II. Incidence of Spoilage in Eggs from Ninety-four Farms. Food Technology January: 130134.Google Scholar
U. S. DEPARTMENT OF AGRICULTURE (1998) Refrigeration and labelling requirements for shell eggs (Final Rule). Federal Register 63: 4566345675.Google Scholar
UNITED EGG PRODUCERS (2004) Food Safety: 5 Star Programme. United Egg Producers website. http://www.unitedegg.org/food_safety.aspx.Google Scholar