Abstract
Microbial contamination of eggs is a well-established phenomenon and has important economic implications to the poultry industry. In the case of table eggs spoilage may occur and if the organism is of public health significance the affected eggs may be the cause of spread of disease. Contamination of hatching eggs may reduce hatchability, be responsible for transmission of poultry pathogens and impair the quality of chicks produced.
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References
Alls, A.A., Cover, M.S., Benton, W.J. and Krauss, W.C. (1964) Treatment of hatching eggs for disease prevention — Factors affecting permeability and a visual detection of drug absorption. Avian Dis., 8, 245–56.
Amin, M.K. and Draughon, F.A. (1990) Infection of shell eggs with Yersinia enterocolitis. J. Food Protect., 53, 826–30.
Ar, A.M., Paganelli, C.V., Reeves, R.B. et al. (1974) The avian egg: water vapour conductance, shell thickness and functional pore area. The Condor, 76, 153–8.
Arhienbuwa, F.E., Adler, H.E. and Wiggins, A.D. (1980) A method of surveillance of bacteria on the shell of turkey eggs. Poult. Sci., 59, 28–33.
Attar, A.J. (1990) Formaldehyde in hatcheries: rules and monitoring explained. Poult. Digest, March 34, 36, 38–39.
Baker, J.R. and Balch, D. A. (1962) A study of the organic material of hen’s egg shell. Biochem. J. 82, 352–61.
Ball, R.F., Logan, V. and Hill, J.F. (1975) Factors affecting the cuticle of the egg as measured by intensity of staining. Poult. Sci., 54, 1479–84.
Baxter-Jones, C. (1991) Egg hygiene: microbial contamination, significance and control, in Avian Incubation, (Ed. S.G. Tullett). Poultry Science Symposium 22. Butterworth-Heinemann, Northants, pp. 269–76.
Baxter-Jones, C. (1983) The persistence and control of bacterial pathogens in turkey eggs. PhD Thesis, University of Liverpool.
Bean, K.C. and MacLaury, D.W. (1959) The bacterial contamination of hatching eggs and methods for its control. Poult. Sci., 38, 693–8.
Becirevic, M., Popovic, M. and Becirevic, N. (1988) Influence of iron and water on the growth of S.typhimurium and enteropathogenic E.coli in eggs and albumen. Vet. Yugoslav. 37, 41–9.
Blankenship, L.C., Hudspeth J.P. and Craven S.E. (1982) Microbiology of ova harvested from commercially slaughtered mature chickens. Poult. Sci., 57, 1550–3.
Board, R.G. (1964) The growth of Gram-ve bacteria in the hen’s egg. J. Appl. Bacteriol., 27, 350–64.
Board, R.G. (1965) Bacterial growth on and penetration of the shell membranes of the hen’s egg. J. Appl. Bacteriol., 28, 197–205.
Board, R.G. (1966) Review article: the course of microbial infection of the hen’s egg. J. Appl. Bacteriol., 29, 319–41.
Board, R.G. (1968) Microbiology of the egg: a review, in Egg Quality: A Study of the Hen’s Egg (ed. T.C. Carter), Oliver and Boyd, Edinburgh, pp. 133–62.
Board, R.G. (1969) The microbiology of the hen’s egg. Adv. Appl. Microbiol., 11, 245–81.
Board, R.G. (1975) The microstructure of the cuticle-less shell of the eggs of the domestic hen. Br. Poult. Sci., 16, 89–91.
Board, R.G. (1980) The avian eggshell: a resistance network. J. Appl. Bacteriol., 48, 303–13.
Board, R.G. (1982) Properties of avian eggshells and their adaptive value. Biol. Rev., 57, 1–28.
Board, P.A. and Board, R.G. (1967) A method of studying bacterial penetration of the shell of the hen’s egg. Lab. Pract., 16, 471–2, 482.
Board, R.G. and Fuller, R. (1974) Non-specific antimicrobial defences of the avian egg, embryo and neonate. Biol. Rev., 49, 15–49.
Board, R.G. and Halls, N.A. (1973) The cuticle: a barrier to liquid and particle penetration of the shell of the hen’s egg. Br. Poult. Sci., 14, 69–97.
Board, R.G., Ayres, J.C., Kraft, A.A. and Forsythe, R.H. (1964) The microbiological contamination of eggshells and egg-packing materials. Poult. Sci., 43, 584–95.
Board, P.A., Hendon, L.P. and Board, R.G. (1968) The influence of iron on the course of bacterial infection of the hen’s egg. Br. Poult. Sci., 9, 211–15.
Board, R.G., Loseby, S. and Miles, V.R. (1979). A note on microbial growth on hen eggshells. Br. Poult. Sci., 20, 413–20.
Board, R.G., Clay, C.E. and Lock, J.L. (1989) The behaviour of salmonella in egg contents and raw egg products. Abstracts Summer Meeting. Society for Applied Bacteriology. July 1989. Edinburgh, p. 19.
Brant, A.J. and Starr, P.B. (1962) Some physical factors related to egg spoilage. Poult. Sci., 41, 1468–73.
Brooks, J. and Taylor, D.I. (1955) Eggs and egg products. Report of the Food Investigation Board, No. 60. HMSO, London.
Brown, W.E., Baker, R.C. and Naylor, H.B. (1965) The role of the inner shell membrane in bacterial penetration of chicken eggs. Poult. Sci., 44, 1323–7.
Brown, W.E., Baker, R.C. and Naylor, H.B. (1966) The microbiology of cracked eggs. Poult. Sci., 45, 284–7.
Bruce, J. and Drysdale, E.M. (1983) The bacterial flora of candling reject and dead-in-shell turkey eggs. Br. Poult. Sci., 24, 391–5.
Bruce, J. and Drysdale E.M. (1991) Egg hygiene: routes of infection, in Avian Incubation (ed. S.G. Tullett), Poultry Science Symposium Number 22. Butterworth-Heinemann, Northants, Chapter 16.
Bruce, J. and Johnson, A.L. (1978) The bacterial flora of unhatched eggs. Br. Poult. Sci., 19, 681–9.
Burton, F. and Tullett, S.G. (1983) A comparison of the effects of eggshell porosity on the respiration and growth of domestic fowl, duck and turkey embryo. Comp. Biochem. Physiol., 75A, 167–74.
Carter, T.A., Gentry, R.F. and Bressler, G.O. (1973) Bacterial contamination of hatching eggs and chicks produced by broiler systems. Poult. Sci., 52, 2226–36.
Chander, H., Lata, K., Batish, V.K. and Bhatia, K.L. (1984) Antibacterial activity of lysozyme against some common food poisoning organisms. Arch. Lebensmittelhyg., 35, 73–96.
Clark, A.G. and Bueschkens, D.H. (1985) Laboratory infection of chicken eggs with Campylobacter jejuni by using temperature or pressure differentials. Appl. Environ. Microbiol., 49, 1467–71.
Coleman, J.R. and Terepka, A.R. (1972) Fine structural changes associated with the onset of calcium, sodium and water transport by the chick chorioallantoic membrane. J. Membr. Biol., 7, 111–27.
Cooke, A.S. and Balch, D.A. (1970) Studies on membrane, mammillary cores and cuticle of the hen egg shell. Br. Poult. Sci., 11, 345–52.
Cowden J.M. (1990) Salmonellosis and eggs; public health, food poisoning, and food hygiene. Curr. Opin. Infect. Dis., 3, 246–9.
Dawson, L.E. and Watts, J.P. (1952) Effect of nest-litter on cleanliness of eggs. Poult. Sci., 31, 31.
Doyle, M.P. (1984) Association of Campylobacter jejuni with laying hens and eggs. Appl. Environ. Microbiol., 47, 533–6.
Drysdale, E.M. (1985) Microbial penetration of the avian egg. MSc Thesis, University of Glasgow.
Finch, M.J. and Blake, P.A. (1985) Foodborne outbreaks of campylobacteriosis: The US experience 1980–82. Am. J. Epidemiol., 122, 262–8.
Forsythe, R.H., Ayres, J.C. and Radio, J.L. (1953) Factors affecting the microbiological populations of shell eggs. Food Technol., 7, 49–56.
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. Poult. Sci., 35, 61–2.
Gale, C. and Brown, K.I. (1966) The identification of bacteria contaminating collected semen and the use of antibiotics in their control. Poult. Sci., 45, 50–5.
Garibaldi, J. A. and Bayne, H.G. (1960) The effect of iron on Pseudomonas spoilage on experimentally infected eggs. Poult. Sci., 39, 1517–20.
Garibaldi, J. A. and Bayne, H.G. (1962) The effect of iron on the Pseudomonas spoilage on farm washed eggs. Poult. Sci., 41, 850–3.
Graves, R.C. and MacLaury, D.W. (1962) The effect of temperature, vapour pressure and absolute humidity on bacterial contamination of shell eggs. Poult. Sci., 41, 1219–25.
Haines, R.B. (1938) Bacterial flora of hen eggs with a description of a new species of proteus and Pseudomonas causing rots in eggs. J. Hyg., 38, 338–55.
Haines, R.B. and Moran, T. (1940) Porosity of, and bacterial invasion through the shell of hen’s egg. J. Hyg., 37, 453–61.
Harry, E.G. (1957) The effect on embryonic and chick mortality of yolk contamination with bacteria from the hen. Vet. Rec., 69, 1433–9.
Harry, E.G. (1963a) Some observations on the the bacterial content of the ovary and oviduct of the fowl. Br. Poult. Sci., 4, 63–70.
Harry, E.G. (1963b) The relationship between egg spoilage and the environment of the egg when laid. Br. Poult. Sci., 4, 91–100.
Hartung, T.E. and Stadelman, W.T. (1963) Pseudomonas fluorescens penetration of eggshell membranes as influenced by shell porosity, age of egg and degree of bacterial challenge. Poult. Sci., 42, 147–50.
Hodgetts, B. and Dance, G. (1974) Cleaner hatching eggs in the nest. Poult. World, Feb.
Holley, R.A. and Proulx, M. (1986). Use of egg washwater pH to prevent survival of salmonella at moderate temperatures. Poult. Sci., 65, 922–8.
Humphrey, T.J., Lanning, D.G. and Leeper, D. (1981) The effect of pH adjustment on the microbiology of chicken scald-tank water with particular reference to the death rate of salmonellas. J. Appl. Bacteriol., 51, 517–27.
International Association of Milk, Food and Environmental Sanitarians (IAMFES) (1976) Sanitary standards for shell egg washers. J. Milk Food Technol., 39, 654–6.
Jacobs, L.A., McDaniel, G.R. and Broughton, C.W. (1978) Microbial flora observed within sections of the oviduct in naturally mated, artificially inseminated and virgin hens. Poult. Sci., 57, 1550–3.
Jones, F.T., Axtell R.C., Rives D.V. et al. (1991) A survey of Campylobacter jejuni contamination in modern broiler production. J. Food Protect., 54, 259–62.
Joyce, D.A. and Chaplin, N.R.C. (1978) Hygiene and hatchability of duck eggs — a field study. Vet. Rec., 103, 9–12.
Kinner, J.A. and Moats, W.A. (1981) Effect of temperature, pH, and detergent on survival of bacteria associated with shell eggs. Poult. Sci., 60, 761–7.
Kollowa J. and Kollowa C. (1989) Occurrence and survival of Campylobacter jejuni on the shell surface of hen eggs. Monatsh. Vet., 44, 63–5.
Kraft, A.A. and Elliot, L.E. and Brant, A.W. (1958) The shell membranes as a barrier to penetration of eggs. Poult. Sci., 37, 238.
Laird, J.M., Bartlett, F.M. and McKellar, R.C. (1991) Survival of Listeria monocytogenes in egg washwater. Int. J. Food Microbiol., 12, 115–22.
Latala, A. and Dobrzanski, Z. (1989) Effect of ultraviolet radiation on the microbiological contamination of the shells of eggs for human consumption. Med. Wet., 45, 420–2.
Latala, A. and Wakula-Radzik, K. (1990) Effect of ultraviolet radiation of eggs on hatchability and microbial flora of the egg shell. Med. Wet., 46, 224–6.
Lifshitz, A., Baker, R.C. and Naylor, H.B. (1964) The relative importance of chicken egg exterior structure in resisting bacterial penetration. J. Food Sci., 29, 94–9.
Lifshitz, A., Baker, R.C. and Naylor, H.B. (1965) Exterior structures of the egg as nutrients for bacteria. J. Food Sci., 30, 516–19.
Lorenz, F.W. and Starr, P.B. (1952) Spoilage of washed eggs. Poult. Sci., 31, 204–14.
MacLaury, D.W. and Moran, A.B. (1959) Bacterial contamination of hatching eggs. Kentucky Agric. Exp. Sta. Bull., 665, 3–27.
Maesso, E.R., Vadehra, D.V. and Baker, R.C. (1970) Mechanism of bacterial penetration through the inner shell membrane of chicken eggs 2. Effect of charge and modification of structure. Poult. Sci., (abstract), 49, 1409.
March, B.E. (1969) Bacterial infection of washed and unwashed eggs with respect to salmonellae. Appl. Microbiol., 17, 98–101.
Marshall, W. and Cruickshank, D.B. (1938) The function of the cuticle in relation to the porosity of eggs. J. Agric. Sci., 28, 24–42.
Mayes, F.J. and Takeballi, M.A. (1983) Microbial contamination of the hen’s egg: A review. J. Food Protect., 46, 1092–8.
Metwally, M., Abd EL-R, Majeid, L.A. et al. (1984) Microbial contamination in relation to embryonic mortalities. Iraqi J. Agric. Sci., 2, 115–25.
Miller, W.A. and Crawford, L.B. (1953) Some factors influencing bacterial populations of eggs. Poult. Sci., 32, 303–9.
Moats, W.A. (1978) Egg washing: a review. J. Food Protect., 41, 919–25.
Moats, W.A. (1981) Factors affecting bacterial loads on shells of commercially washed eggs. Poult. Sci., 60, 2084–90.
Neill, S.D., Campbell, J.N. and O’Brien, J.J. (1985) Egg penetration by Campylobacter jejuni. Avian Pathol., 14, 313–20.
North, M.O. (1984) Maintaining hatching egg quality, in Commercial Chicken Production Manual, 3rd edn, The AVI Publication Company, Inc. Westport, CN., pp. 71–84.
Parsons, A.H. (1982) Structure of the eggshell. Poult. Sci., 61, 2013–21.
Quarles, C.L., Gentry, R.F. and Bressler, G.O. (1970) Bacterial contamination in poultry houses and its relationship to egg hatchability. Poult. Sci., 49, 60–6.
Rahn, H., Christensen, V.L. and Edens, F.W. (1981) Changes in shell conductance, pores and physical dimensions of egg and shell during the first breeding cycle of turkey hens. Poult. Sci., 60, 2536–41.
Romanoff, A.L. and Romanoff, A.J. (1949) The Avian Egg. John Wiley New York.
Rosser, F.T. (1942) Preservation of eggs. Surface contamination of egg shell in relation to spoilage. Can. J. Res., 20D, 291–6.
Sauter, E.A. and Peterson, C.F. (1974) The effect of egg shell quality on penetration by various salmonellae. Poult. Sci., 53, 2159–62.
Seviour, E.M. and Board, R.G. (1972) The behaviour of mixed bacterial infections in the shell membranes of the hen’s egg. Br. Poult. Sci., 13, 33–43.
Shane, S.M., Gifford, D.H. and Yogasundrum, K. (1986) Campylobacter jejuni contamination of eggs. Vet. Res. Commun., 10, 487–92.
Shanker, S., Lee, A. and Sorrell, T.C. (1986) Campylobacter jejuni in broilers: the role of vertical transmission. J. Hyg., 96, 153–9.
Sharp, P.F. and Stewart, G.F. (1936) Effect of relative humidity on growth of molds on eggs in storage. Mem. Cornell Univ. Agric. Exp. Sta., 91, 1–11.
Simkiss, K. (1961) Calcium metabolism and avian reproduction. Biol. Rev., 36, 321–67.
Simons, P.C.M. (1971) Ultrastructure of the Hen Eggshell and its Physiological Interpretation. Centre for Agricultural Publishing and Documentation, Wageningen.
Simons, P.C.M. and Wiertz, G. (1966) The ultrastructure of the surface of the cuticle of the hen’s egg in relation to egg cleaning. Poult. Sci., 45, 1153–62.
Smeltzer, T.I., Orange, K., Peel, B. and Runge, G.I. (1979) Bacterial penetration in floor and nest-box eggs from meat and layer birds. Aust. Vet. J., 55, 592–3.
Southam, G., Pearson, J. and Holley, R.A. (1987) Survival and growth of Yersinia enterocolitica in egg washwater. J. Food Protect., 50, 103–7.
Sparks, N.H.C. (1985) The hen eggshell: a resistance network. PhD Thesis, University of Bath.
Sparks, N.H.C. and Board, R.G. (1984) Cuticle, shell porosity and water uptake through hens’ eggshells. Br. Poult. Sci., 25, 267–76.
Sparks, N.H.C. and Board, R.G. (1985) Bacterial penetration of the recently oviposited shell of hens’ eggs. Aust. Vet. J., 6, 169–70.
Theodore, T.S. and Schade, A.L. (1965) Carbohydrate metabolism of iron rich and iron poor Staphylococcus aureus. J. Gen. Microbiol., 40, 385–96.
Tranter, H.C., Sparks, N.H.C. and Board, R.G. (1983) Br. Poult. Sci., 24, 123–30.
Tullett, S.G. (1976) The avian eggshell: a mediating boundary. PhD Thesis, University of Bath.
Tullett, S.G. (1981) Theoretical and practical aspects of eggshell porosity. Turkeys, 29, 24–8.
Tullett, S.G. (1990) Science and the art of incubation. Poult. Sci., 69, 1–15.
Tullett, S.G. and Board, R.G. (1976) Oxygen flux across the integument of the avian egg during incubation. Br. Poult. Sci., 17, 441–50.
Tullett, S.G., Lutz, P.L. and Board, R.G. (1975) The fine structure of the pores in the shell of the hen’s egg. Br. Poult. Sci., 16, 93–5.
Tyler, C. (1953) Studies on egg shells II. A method for marking and counting pores. J. Sci. Food Agric., 4, 266–72.
Tyler, C. (1955) Studies on eggshells VI. The distribution of pores in eggshells. J. Sci. Food Agric., 6, 170–6.
Tyler, C. (1958) Studies on eggshells X. A method for determining variations in characteristics in different parts of the same shell. J. Sci. Food Agric., 9, 584–90.
Vadhera, D.V., Baker, R.C. and Naylor, H.B. (1970a) Role of cuticle in spoilage of chicken eggs. J. Food Sci., 35, 5–6.
Vadhera, D.V., Baker, R.C. and Naylor, H.B. (1970b) Infection routes of bacteria into chicken eggs. J. Food Sci., 35, 61–2.
Vest, L.R. (1978) Floor eggs should not be kept for hatching. Poult. Digest, Nov.
Walden, C.C., Allen, I.V.F. and Trussell, P.C. (1956) The role of egg shell and shell membranes in restraining the entry of microorganisms. Poult. Sci., 35, 1190–6.
Whistler, P.E. and Sheldon, B.W. (1989) Biocidal activity of ozone versus formaldehyde against poultry pathogens inoculated in a prototype setter. Poult. Sci., 68, 1068–73.
Williams, J.E. (1970) Effect of high level formaldehyde fumigation on bacterial populations on the surface of chicken hatching eggs. Avian Dis., 14, 386–92.
Williams, J.E. and Whittemore, A.D. (1967) A method for studying microbial penetration through the structures of the avian egg. Avian Dis., 11, 467–90.
Williams, J.R., Dillard, L.H. and Hall, G.O. (1968) The penetration patterns of Salmonella typhimurium through the outer structures of chicken eggs. Avian Dis., 12, 69–97.
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Bruce, J., Drysdale, E.M. (1994). Trans-shell transmission. In: Board, R.G., Fuller, R. (eds) Microbiology of the Avian Egg. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3060-2_4
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