Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-19T12:18:28.930Z Has data issue: false hasContentIssue false
  • English
  • Français

Eggshell penetration by Salmonella: a review

Published online by Cambridge University Press:  18 September 2007

W. Messens ,
K. Grijspeerdt  and
L. Herman
W. Messens*
Affiliation:
Ministry of the Flemish Community, Agricultural Research Centre-Ghent, Department of Animal Product Quality and Transformation Technology, Brusselsesteenweg 370, B-9090 Melle, Belgium
K. Grijspeerdt
Affiliation:
Ministry of the Flemish Community, Agricultural Research Centre-Ghent, Department of Animal Product Quality and Transformation Technology, Brusselsesteenweg 370, B-9090 Melle, Belgium
L. Herman
Affiliation:
Ministry of the Flemish Community, Agricultural Research Centre-Ghent, Department of Animal Product Quality and Transformation Technology, Brusselsesteenweg 370, B-9090 Melle, Belgium
*
*Corresponding author: W.Messens@clo.fgov.be
Get access

Abstract

Intact eggs can become contaminated with Salmonella as a result of infections of the reproductive tissues of the laying hens but also by penetration through the shell. In this paper, the penetration of Salmonella through the shell of hen eggs is reviewed. A description is given of the advantages and disadvantages of the various methods used to study bacterial penetration through the shell and membranes. The possibility of Salmonella contamination of the shell after lay is included because shell contamination is the first requisite for penetration. Various factors affect the probability of bacterial penetration. Both the intrinsic and extrinsic factors are highlighted. For the extrinsic factors, the influence of bacterial strain and number of organisms, temperature, moisture and immersion and storage conditions on the probability of Salmonella penetration through the shell is described. With regard to intrinsic factors, the presence of cuticle, shell characteristics (shell quality, porosity, shell defects) and membrane properties are summarized.

Keywords

Salmonellapenetrationhen eggshellmembrane
Type
Reviews
Information
World's Poultry Science Journal , Volume 61 , Issue 1 , March 2005 , pp. 71 - 86
Copyright
Copyright © Cambridge University Press 2005

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

Allen, K.J. and Griffiths, M.W. (2001) Use of luminescent Campylobacter jejuni ATCC 33291 to assess eggshell colonization and penetration in fresh and retail eggs. Journal of Food Protection 64: 2058–2062.CrossRefGoogle ScholarPubMed
Anderson, K.E., Jones, F.T., Guo, L. and Curtis, P.A. (1995) Penetration and recovery of bacteria on inoculated shell eggs among different genetic strains. Poultry Science 74: 169.Google Scholar
Baker, R.C. (1990) Survival of Salmonella enteritidis on and in shelled eggs, liquid eggs and cooked egg products. Dairy, Food and Environmental Sanitation 10: 273–275.Google Scholar
Barrow, P.A. and Lovell, M.A. (1991) Experimental infection of egg-laying hens with Salmonella enteritidis phage type 4. Avian Pathology 20: 335–348.CrossRefGoogle ScholarPubMed
Berrang, M.E., Cox, N.A., Frank, J.F. and Buhr, R.J. (1999a) Bacterial penetration of the eggshell and shell membranes of the chicken hatching egg: a review. Journal of Applied Poultry Research 8: 499–504.CrossRefGoogle Scholar
Berrang, M.E., Frank, J.F., Buhr, R.J., Bailey, J.S. and Cox, N.A. (1999b) Eggshell membrane structure and penetration by Salmonella Typhimurium. Journal of Food Protection 62: 73–76.CrossRefGoogle ScholarPubMed
Berrang, M.E., Frank, J.F., Buhr, R.J., Bailey, J.S., Cox, N.A. and Mauldin, J. (1998) Eggshell characteristics and penetration by Salmonella through the productive life of a broiler breeder flock. Poultry Science 77: 1446–1450.CrossRefGoogle ScholarPubMed
Bichler, L.A., Nagaraja, K.V. and Halvorson, D.A. (1996) Salmonella enteritidis in eggs, cloacal swab specimens, and internal organs of experimentally infected White Leghorn chickens. American Journal of Veterinary Research 57: 489–495.CrossRefGoogle ScholarPubMed
Board, P.A. and Board, R.G. (1967) Amethod of studying bacterial penetration of the shell of the hen's egg. Laboratory Practice 16: 471–472, 482.Google Scholar
Board, R.G. (1980) The avian eggshell-a resistant network. Journal of Applied Bacteriology 48: 303–313.CrossRefGoogle Scholar
Board, R.G. and Halls, N.A. (1973) The cuticle: a barrier to liquid and particle penetration of the shell of hen's egg. British Poultry Science 14: 69–97.CrossRefGoogle Scholar
Board, R.G., Loseby, S. and Miles, V.R. (1979) A note on microbial growth on hen egg-shells. British Poultry Science 20: 413–420.CrossRefGoogle Scholar
Board, R.G. and Tranter, H.S. (1995) The microbiology of eggs. In: Stadelman, W.J. and Cotterill, O.J. (ed), Egg Science and Technology. The Haworth Press, London, pp. 81–104.Google Scholar
Braun, P., Fehlhaber, K. and Wicke, A. (1999) Salmonella enteritidis invades the egg through the shell. World Poultry Special: 23–24.Google Scholar
Bruce, J. and Drysdale, E.M. (1994b) Trans-shell transmission. In: Board, R.G. and Fuller, R. (ed), Microbiology of the Avian Egg. Chapman & Hall, London, pp. 63–91.CrossRefGoogle Scholar
Bryan, F.L. and Doyle, M.P. (1995) Health risks and consequences of Salmonella and Campylobacter jejuni in raw poultry. Journal of Food Protection 58: 326–344.CrossRefGoogle ScholarPubMed
Cavitte, J.C. (2003) Present and future control of food-borne pathogens in poultry; revision of the European Community legislation on zoonoses. In: Salvat, G. and Protais, J. (ed), Proceedings of the XVIth European Symposium on the Quality of Poultry Meat & Xth European Symposium on the Quality of Eggs and Egg Products. Saint-Brieuc, Proufragan, France, September 23–26, 2003, Volume 1, pp. 46–58.Google Scholar
Chen, H., Anantheswaran, R. and Knabel, S. (2002a) Effect of rapid cooling of shell eggs on microcrack development, penetration of Salmonella enteritidis, and eggshell strength. Journal of Food Processing and Preservation 26: 57–73.CrossRefGoogle Scholar
Chen, H., Anantheswaran, R.C. and Knabel, S.J. (2002b) Effect of rapid cooling on the growth and penetration of Salmonella enteritidis into egg contents. Journal of Food Safety 22: 255–271.CrossRefGoogle Scholar
Chen, J., Clarke, R.C. and Griffiths, M.W. (1996) Use of luminescent strains of Salmonella enteritidis to monitor contamination and survival in eggs. Journal of Food Protection 59: 915–921.CrossRefGoogle ScholarPubMed
Chen, J. and Griffiths, M.W. (1996) Luminescent Salmonella strains as real time reporters of growth and recovery from sublethal injury in food. International Journal of Food Microbiology 31: 27–43.CrossRefGoogle ScholarPubMed
Clay, C.E. and Board, R.G. (1991) Growth of Salmonella enteritidis in artificially contaminated hens shell eggs. Epidemiology and Infection 106: 271–281.CrossRefGoogle ScholarPubMed
Clay, C.E. and Board, R.G. (1992) Effect of faecal extract on the growth of Salmonella enteritidis in artificially contaminated hens'eggs. British Poultry Science 33: 755–760.CrossRefGoogle ScholarPubMed
Cogan, T.A. and Humphrey, T.J. (2003) The rise and fall of Salmonella enteritidis in the UK. Journal of Applied Microbiology 94 Suppl 1: 114–119.CrossRefGoogle ScholarPubMed
Cogan, T.A., Jorgensen, F., Lappin-Scott, H.M., Benson, C.E., Woodward, M.J. and Humphrey, T.J. (2004) Flagella and curli fimbriae are important for the growth of Salmonella enterica serovars in hen eggs. Microbiology 150: 1063–1071.CrossRefGoogle ScholarPubMed
Cox, N.A., Davis, B.H., Watts, A.B. and 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.CrossRefGoogle ScholarPubMed
Davies, R.H. and Breslin, M. (2003) Investigation of Salmonella contamination and disinfection in farm egg-packing plants. Journal of Applied Microbiology 94: 191–196.CrossRefGoogle ScholarPubMed
De Reu, K., Grijspeerdt, K., Messens, W., Heyndrickx, M., Uyttendaele, M. and Herman, L. (2004) Assessment of the eggshell penetration by different bacteria, including Salmonella enteritidis, isolated from the egg contents of consumption eggs. In: Proceedings of the XXIIth World's Poultry Congress. Istanbul, Turkey, pp. 367.Google Scholar
Ernst, R., Fuqua, L., Riemann, H.P. and Himathongkham, S. (1998) Effect of sweating on shell penetration of Salmonella enteritidis. Journal of Applied Poultry Research 7: 81–84.CrossRefGoogle Scholar
Fajardo, T.A., Anantheswaran, R.C., Puri, V.M. and Knabel, S.J. (1995) Penetration of Salmonella enteritidis into eggs subjected to rapid cooling. Journal of Food Protection 58: 473–477.CrossRefGoogle ScholarPubMed
Fromm, D. and Margolf, P.H. (1958) The influence of sweating and washing on weight loss, bacterial contamination and interior physical quality of 12-day old shell eggs. Poultry Science 37: 1273–1278.CrossRefGoogle Scholar
Gast, R.K. and Beard, C.W. (1990) Production of Salmonella enteritidis-contaminated eggs by experimentally infected hens. Avian Diseases 34: 438–446.CrossRefGoogle ScholarPubMed
Guard-Petter, J. (2001) The chicken, the egg and Salmonella enteritidis. Environmental Microbiology 3: 421–430.CrossRefGoogle ScholarPubMed
Haigh, T. and Betts, W.B. (1991) Microbial barrier properties of hen egg shells. Microbios 68: 137–146.Google ScholarPubMed
Hartung, T.E. and Stadelman, W.J. (1963) Pseudomonas fluorescens penetration of egg shell membranes as influenced by shell porosity, age of egg and degree of bacterial challenge. Poultry Science 42: 147–150.CrossRefGoogle Scholar
Himathongkham, S., Riemann, H. and Ernst, R. (1999) Efficacy of disinfection of shell eggs externally contaminated with Salmonella enteritidis. Implications for egg testing. International Journal of Food Microbiology 49: 161–167.CrossRefGoogle ScholarPubMed
Humphrey, T.J. (1994) Contamination of eggs with potential human pathogens. In: Board, R.G. and Fuller, R. (ed), Microbiology of the Avian Egg. Chapman & Hall, London, pp. 93–116.CrossRefGoogle Scholar
Imberechts, H. and Dierick, K. (2004) Report on zoonotic agents in Belgium in 2002, pp. 65. Veterinary and Agrochemical Research Centre – Scientific Institute of Public Health.Google Scholar
Jones, D.R., Anderson, K.E., Curtis, P.A. and Jones, F.T. (2002) Microbial contamination in inoculated shell eggs: I. Effects of layer strain and hen age. Poultry Science 81: 715–720.CrossRefGoogle ScholarPubMed
Jones, F.T., Rives, D.V. and Carey, J.B. (1995) Salmonella contamination in commercial eggs and an egg production facility. Poultry Science 74: 753–757.CrossRefGoogle Scholar
Kraft, A.A., Elliott, L.E. and Brant, A.W. (1958a) The shell membrane as a barrier to bacterial penetration of eggs. Poultry Science 37: 238–240.CrossRefGoogle Scholar
Kraft, A.A., Mcnally, E.H. and Brant, A.W. (1958b) Shell quality and bacterial infection of shell eggs. Poultry Science 37: 638–644.CrossRefGoogle Scholar
Lin, C.-T.J., Morales, R.A. and Ralston, K. (1997) Raw and undercooked eggs: a danger of salmonellosis. Food Safety 20: 27–32.Google Scholar
Lu, S., Killoran, P.B. and Riley, L.W. (2003) Association of Salmonella enterica serovar enteritidis yafD with resistance to chicken egg albumen. Infection and Immunity 71: 6734–6741.CrossRefGoogle ScholarPubMed
Mayes, F.J. and Takeballi, M.A. (1983) Microbial contamination of the hen's egg: a review. Journal of Food Protection 46: 1092–1098.CrossRefGoogle ScholarPubMed
Messens, W., Grijspeerdt, K. and Herman, L. (submitted) Eggshell characteristics, storage conditions and penetration of eggshells by Salmonella enterica serovar Enteritidis through the production period of a layer flock. British Poultry Science.Google Scholar
Miyamoto, T., Horie, T., Baba, E., Sasai, K., Fukata, T. and Arakawa, A. (1998) Salmonella penetration through eggshell associated with freshness of laid eggs and refrigeration. Journal of Food Protection 61: 350–353.CrossRefGoogle ScholarPubMed
Nascimento, V.P. (1992) The ease of translocation of Salmonella enteritidis through the eggshell wall: an immunocytochemical/ultrastructural study. Thesis University of Glasgow. Glasgow, pp. 266.Google Scholar
Nascimento, V.P., Cranstoun, S. and Solomon, S.E. (1992) Relationship between shell structure and movement of Salmonella enteritidis across the eggshell wall. British Poultry Science 33: 37–48.CrossRefGoogle ScholarPubMed
Nascimento, V.P. and Solomon, S.E. (1991) The transfer of bacteria (Salmonella enteritidis) across the eggshell wall of eggs classified as poor quality. Animal Technology 42: 157–165.Google Scholar
Orel, V. (1959) The Pseudomonas spoilage of eggs laid by individual hens. Poultry Science 38: 8–12.CrossRefGoogle Scholar
Padron, M. (1990) Salmonella typhimurium penetration through the eggshell of hatching eggs. Avian Diseases 34: 463–465.Google ScholarPubMed
Perales, I. and Audicana, A. (1989) The role of hens'eggs in outbreaks of salmonellosis in north Spain. International Journal of Food Microbiology 8: 175–180.CrossRefGoogle ScholarPubMed
Radkowski, M. (2002) Effect of moisture and temperature on survival of Salmonella enteritidis on shell eggs. Archiv für Geflügelkunde 66: 119–123.Google Scholar
Rizk, S.S., Ayres, J.C. and Kraft, A.A. (1966) Effect of holding condition on the development of Salmonellae in artificially inoculated hens'eggs. Poultry Science 45: 825–829.CrossRefGoogle ScholarPubMed
Roberts, J.R. and Brackpool, C.E. (1994) The ultrastructure of the avian egg shells. Poultry Science Reviews 5: 245–272.Google Scholar
Saeed, A.M. (1998) The impact of Salmonella enteritidis on public health and environmental quality. In: Proceedings of the United States Animal Health Association.Google Scholar
Sauter, E.A. and Petersen, C.F. (1974) The effect of egg shell quality on penetration by various salmonellae. Poultry Science 53: 2159–2162.CrossRefGoogle ScholarPubMed
Sauter, E.A., Petersen, C.F., Parkinson, J.F. and Steele, E.E. (1979) Effect of pH on eggshell penetration by Salmonellae. Poultry Science 58: 135–138.CrossRefGoogle ScholarPubMed
Schoeni, J.L., Glass, K.A., Mcdermott, J.L. and Wong, A.C. (1995) Growth and penetration of Salmonella enteritidis, Salmonella heidelberg and Salmonella typhimurium in eggs. International Journal of Food Microbiology 24: 385–396.CrossRefGoogle ScholarPubMed
Simmons, E.R., Ayres, J.C. and Kraft, A.A. (1970) Effect of moisture and temperature on ability of Salmonellae to infect shell eggs. Poultry Science 49: 761–768.CrossRefGoogle ScholarPubMed
Smeltzer, T.I., Orange, K., Peel, B. and Runge, G. (1979) Bacterial penetration in floor and nest box eggs from meat and layer birds. Australian Veterinary Journal 55: 592–593.CrossRefGoogle ScholarPubMed
Solomon, S.E. (1997) Egg & eggshell quality. Iowa State University Press. Iowa, USA, pp. 149.Google Scholar
Solomon, S.E. (1999) Gordon Memorial Lecture. An egg ist ein ei, es un huevo, est un oeuf. British Poultry Science 40: 5–11.CrossRefGoogle ScholarPubMed
Sooncharenying, S. and Edwards, H.M. (1989) Modelling the relationships of egg weight, specific gravity, shell calcium and shell thickness. British Poultry Science 30: 623–631.CrossRefGoogle ScholarPubMed
Sparks, N.H. and Board, R.G. (1985) Bacterial penetration of the recently oviposited shell of hens'eggs. Australian Veterinary Journal 62: 169–170.CrossRefGoogle ScholarPubMed
Thompson, J.F., Knutson, J., Ernst, R.A., Kuney, D., Riemann, H., Himathongkham, S. and Zeidler, G. (2000) Rapid cooling of shell eggs. Journal of Applied Poultry Research 9: 258–268.CrossRefGoogle Scholar
Wang, H. and Slavik, M.F. (1998) Bacterial penetration into eggs washed with various chemicals and stored at different temperatures and times. Journal of Food Protection 61: 276–279.CrossRefGoogle ScholarPubMed
WHO (2001) World Health Organisation surveillance programme for control of foodborne infections and intoxications in Europe. Seventh report, 1993–1998. In: Schmidt, K. and Tirado, C. (ed). Federal Institute for Health Protection of Consumers and Veterinary Medicine (BgVV), Berlin, Germany, pp. 415, 422–423.Google Scholar
Williams, J.E., Dillard, L.H. and Hall, G.O. (1968) The penetration patterns of Salmonella typhimurium through the outer structures of chicken eggs. Avian Diseases 12: 445–466.CrossRefGoogle ScholarPubMed
Wong Liong, J., Frank, J. and Bailey, S. (1997) Visualization of eggshell membranes and their interaction with Salmonella enteritidis using confocal scanning laser microscopy. Journal of Food Protection 60: 1022–1028.CrossRefGoogle ScholarPubMed