Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-26T12:55:48.512Z Has data issue: false hasContentIssue false

The eggshell cuticle of the laying hen

Published online by Cambridge University Press:  13 November 2014

S. SAMIULLAH
Affiliation:
Animal Science, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia
J.R. ROBERTS*
Affiliation:
Animal Science, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia
*
Corresponding author: [email protected]
Get access

Abstract

The cuticle is the outermost layer, deposited on the palisade layer of the eggshell during the last 1.5-2 hr of eggshell formation in utero. It is a non-calcified, thin, water-insoluble layer composed mainly of glycoproteins with some carbohydrate and fat constituents. The cuticle functions as a protective layer which regulates gaseous exchange across the shell, acts as a first line of defence against microbial penetration across the eggshell and is associated with termination of calcite crystal growth during shell formation. The extent of cuticle deposition is influenced by hen age and strain. The physiological and microbiological characteristics of the hen eggshell cuticle are reviewed in relation to its protective functions.

Type
Review Article
Copyright
Copyright © World's Poultry Science Association 2014 

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

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 inspection of drug absorption. Avian Diseases 8: 245-256.Google Scholar
BAIN, M.M., RODRIGUEZ-NAVARRO, A., McDADE, K., SCHMUTZ, M., PREISINGER, R., WADDINGTON, D. and DUNN, I.C. (2009) The potential of eggshell crystal size and cuticle coverage for genetic selection in laying hens. Abstract from 60th Annual Meeting of the European Association for Animal Production, Barcelona, Spain, pp. 169.Google Scholar
BAKER, J.R. and BALCH, D.A. (1962) A study of the organic material of hen's eggshell. Biochemical Journal 82: 352-350.Google Scholar
BALL, R.F., LOGAN, V. and HILL, J.F. (1975) Factors affecting the cuticle of the egg as measured by intensity of staining. Poultry Science 54: 1479-1484.Google Scholar
BARON, F., GAUTIER, M. and BRUL, G. (1999) Rapid Growth of Salmonella Enteritidis in egg white reconstituted from industrial egg white powder. Journal of Food Protection 62: 585-591.Google Scholar
BECKETT, M., BEGOTT, G.K. and GRAEME-COOK, K. (2003) Bacterial degradation of the eggshell cuticle of the mandarin duck (Aix galerculata). Avian and Poultry Biology Reviews 14: 196-197.Google Scholar
BECKING, J.H. (1975) The ultrastructure of the avian eggshell. Ibis 117: 143-151.Google Scholar
BELYAVIN, C.G. and BOORMAN, K.N. (1980) The influence of the cuticle on egg-shell strength. British Poultry Science 21: 295-298.Google Scholar
BERA, A., BERBERT, S., JAKOB, A., VOLLMER, W. and GOTZ, F. (2005) Why are pathogenic Staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase oatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Molecular Microbiology 55: 778-787.Google Scholar
BERRANG, M.E., COX, N.A., FRANK, J.F. and BUHR, R.J. (1999) Bacterial penetration of the eggshell and shell membranes of the chicken hatching egg: a review. Journal of Applied Poultry Research 8: 499-504.Google Scholar
BIALKA, K.L., DEMIRCI, A., KNABEL, S.J., PATTERSON, P.H. and PURI, V.M. (2004) Efficacy of electrolyzed oxidizing water for the microbial safety and quality of eggs. Poultry Science 83: 2071-2078.Google Scholar
BOARD, R.G. (1974) Microstructure, water resistance and water repellence of the pigeon eggshell. British Poultry Science 15: 415-419.Google Scholar
BOARD, R.G. (1975) The microstructure of the cuticle-less shell of the eggs of the domestic hen. British Poultry Science 16: 89-91.Google Scholar
BOARD, R.G. (1980) The avian eggshell-a resistance network. Journal of Applied Microbiology 48: 303-313.Google Scholar
BOARD, R.G. (1982) Properties of avian eggshells and their adaptive value. Biological Reviews 57: 1-28.Google Scholar
BOARD, R.G. and FULLER, R. (1974) Non-specific antimicrobial defences of the avian egg, embryo and neonate. Biological Reviews 49: 15-49.Google Scholar
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. British Poultry Science 14: 69-97.Google Scholar
BOARD, R.G. and LOVE, G. (1980) Magnesium distribution in avian eggshells. Comparative Biochemistry and Physiology Part A: Physiology 66: 667-672.Google Scholar
BOARD, R.G. and SCOTT, V.D. (1980) Porosity of the Avian Eggshell. American Zoologist 20: 339-349.Google Scholar
BOARD, R.G., LOSEBY, S. and MILES, V.R. (1979) A note on microbial growth on hen eggshells. British Poultry Science 20: 413-420.Google Scholar
BOARD, R.G., TULLETT, S.G. and PERROTT, H.R. (1977) An arbitrary classification of the pore systems in avian eggshells. Journal of Zoology 182: 251-265.Google Scholar
BRUCE, J. and DRYSDALE, E.M. (1994) Trans-shell transmission, in: BOARD R.G. & FULLER R. (Ed) Microbiology of the Avian Egg, pp. 63-91 (Chapman & Hall, London).Google Scholar
BURLEY, R.W. and VADEHRA, D.V. (1989) The Avian Egg. Chemistry and Biology. Wiley Interscience. New York.Google Scholar
BUTCHER, G.D. and MILES, R.D. (2003) Factors causing poor pigmentation of brown shelled eggs. University of Florida. Online retrieved from: http://edis.ifas.ufl.edu/pdffiles/ VM/VM04700.pdf.Google Scholar
CAIN, C.J. and HEYN, A.N. (1964) X-RAY diffraction studies of the crystalline structure of the avian eggshell. Biophysical Journal 4: 23-39.Google Scholar
CAVERO, D., SCHMUTZ, M., ICKEN, W. and PREISINGER, R. (2012) Attractive eggshell colour as a breeding goal. Lohmann Information 47: 15-21.Google Scholar
COLELLA, R., SAKAGUCHI, Y., NAGASE, H. and BIRD, J.W. (1989) Chicken egg white cystatin. Molecular cloning, nucleotide sequence, and tissue distribution. Journal of Biological Chemistry 264: 17164-17169.Google Scholar
COOK, M.I., BEISSINGER, S.R., TORANZOS, G.A., RODRIGUEZ, R.A. and ARENDT, W.J. (2003) Trans–shell infection by pathogenic microorganisms reduces the shelf life of non–incubated bird's eggs: a constraint on the onset of incubation? Proceedings of the Royal Society B 270: 2233-2240.Google Scholar
COOKE, A.S. and BALCH, D.A. (1970) Studies of membranes, mammillary core and cuticle of the hen eggshell. British Poultry Science 11: 345-352.Google Scholar
CURTIS, P.A., GARDNER, F.A. and MELLOR, D.B. (1985) A comparison of selected quality and compositional characteristics of brown and white shell eggs. II. Interior quality. Poultry Science 64: 302-306.Google Scholar
DENNIS, J.E., XIAO, S.Q., AGARWAL, M., FINK, D.J., HEUER, A.H. and CAPLAN, A.I. (1996) Microstructure of matrix and mineral components of eggshell from white leghorn chickens (Gallus gallus). Journal of Morphology 228: 287-306.Google Scholar
DE REU, K., GRIJSPEERDT, K., MESSENS, W., HEYNDRICKX, M., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2006a) Eggshell factors influencing eggshell penetration and whole egg contamination by different bacteria, including Salmonella Enteritidis. International Journal of Food Microbiology 112: 253-260.Google Scholar
DE REU, K., GRIJSPEERDT, K., HEYNDRICKX, M., MESSENS, W., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2006b) Influence of eggshell condensation on eggshell penetration and whole egg contamination with Salmonella enterica serovar Enteritidis. Journal of Food Protection 69: 1539-1545.Google Scholar
DE REU, K., MESSENS, W., GRIJSPEERDT, K., HEYNDRICKX, M., UYTTENDAELE, M. and HERMAN, L. (2010) Eggshell factors influencing eggshell penetration and whole egg contamination by different bacteria, including Salmonella Enteritidis. Proceedings of the Australian Poultry Science Symposium 21: 126-129.Google Scholar
DU, J. (2013) Chicken eggshell membrane and cuticle: insight from bioinformatics and proteomics. M.Sc thesis. University of Ottawa, Canada. Online retrieved from: http://www.ruor.uottawa.ca/en//handle/10393/23631.Google Scholar
EKPERIGIN, H.E. and McCAPES, R.H. (1977) Pre-incubation dipping of turkey hatching eggs I. effect of shell treatment on amount and variability of fluid intake. Avian Diseases 21: 596-604.Google Scholar
EUROPEAN COMMISSION REGULATION (2008) Laying down detailed rules for implementing Council Regulation (EC) No 1234/2007 as regards marketing standards for eggs. Online Retrieved from: http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32008R0589&from=en.Google Scholar
EUROPEAN FOOD SAFETY AUTHORITY (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 Journal 269: 1-39.Google Scholar
FASENKO, G.M., O'DEA CHRISTOPHER, E.E. and MCMULLEN, L.M. (2009) Spraying hatching eggs with electrolyzed oxidizing water reduces eggshell microbial load without compromising broiler production parameters. Poultry Science 88: 1121-1127.Google Scholar
FERNANDEZ, M.S., ESCOBAR, C., LAVELIN, I., PINES, M. and ARIAS, J.L. (2003) Localisation of osteopontin in oviduct tissue and eggshell during different stages of the avian egg laying cycle. Journal of Structural Biology 143: 171-180.CrossRefGoogle ScholarPubMed
FERNANDEZ, M.S., MOYA, A., LOPEZ, L. and ARIAS, J.L. (2001) Secretion pattern, ultrastructural localisation and function of extracellular matrix molecules involved in eggshell formation. Matrix Biology 19: 793-803.Google Scholar
FRASER, A.C., BAIN, M.M. and SOLOMON, S.E. (1999) Transmission electron microscopy of the vertical crystal layer and cuticle of the eggshell of the domestic fowl. British Poultry Science 40: 626-631.Google Scholar
GAUTRON, J., HINCKE, M.T., PANHÉLEUX, M., GARCIA-RUIZ, J.M., BOLDICKE, T. and NYS, Y. (2001) Ovotransferrin is a matrix protein of the hen eggshell membranes and basal calcified layer. Connective Tissue Research 42: 255-267.Google Scholar
GAUTRON, J., HINCKE, M.T. and NYS, Y. (1997) Precursor matrix proteins in the uterine fluid change with stages of eggshell formation in hens. Connective Tissue Research 36 (3): 195-210.Google Scholar
GILBERT, A.B. (1971) The egg: Its physical and chemical aspects. In D.J. Bell and B.M. Freeman (Eds.). Physiology and Biochemistry of the domestic fowl 3: 1379-1399.Google Scholar
HAIGH, T. and BETTS, W.B. (1991) Microbial barrier properties of hen eggshells. Microbios 68: 137-146.Google Scholar
HAINES, R.B. and MORAN, T. (1940) Porosity of, and bacterial invasion through, the shell of the hen egg. The Journal of Hygiene 40: 453-461.Google Scholar
HINCKE, M.T., GAUTRON, J., NYS, Y., RODRIGUEZ-NAVARRO, A.B. and McKEE, M.D. (2011) The eggshell: structure and productive function, in: NYS, Y., BAIN, M. & IMMERSEEL, F.V. (Eds) Improving the safety and quality of eggs and egg products, Vol. 1, pp. 151-182 (Woodhead Publishing Limited).Google Scholar
HINCKE, M.T., NYS, Y. and GAUTRON, J. (2010) The role of matrix protein in eggshell formation (Review). Journal of Poultry Science 47: 208-219.Google Scholar
HINCKE, M.T., GAUTRON, J., MANN, K., PANHELEUX, M., McKEE, M.A., BAIN, M., SOLOMON, S.E. and NYS, Y. (2003) Purification of ovocalyxin-32, a novel chicken eggshell matrix protein. Connective Tissue Research 44: 16-19.Google Scholar
HINCKE, M.T., GAUTRON, J., PANHELEUX, M., GARCIA-RUIZ, J., MCKEE, M.D. and NYS, Y. (2000) Identification and localisation of lysozyme as a component of eggshell membranes and eggshell matrix. Matrix Biology 19: 443-453.Google Scholar
HODGES, R.D. (1974) The Histology of the Fowl. Academic Press Inc. London.Google Scholar
HUGHEY, V.L. and JOHNSON, E.A. (1987) Antimicrobial activity of lysozyme against bacteria involved in food spoilage and food-borne disease. Applied and Environmental Microbiology 53: 2165-2170.Google Scholar
HUMPHREY, T.J. (1994) Contamination of eggshell and contents with Salmonella Enteritidis: A review. International Journal of Food Microbiology 21: 31-40.Google Scholar
HUTCHISON, M.L., GITTINS, J., WALKER, A., SPARK, N., HUMPHREY, T.J., BURTON, C. and MOORE, A. (2004) An assessment of the microbiological risks involved with egg washing under commercial conditions. Journal of Food Protection 67 (1): 4-11.Google Scholar
IBRAHIM, H.R., SUGIMOTO, Y. and AOKI, T. (2000) Ovotransferrin antimicrobial peptide (OTAP-92) kills bacteria through a membrane damage mechanism. Biochimica et Biophysica Acta (BBA) - General Subjects 1523: 196-205.Google Scholar
ISHIKAWA, S., SUZUKI, K., FUKUDA, E., ARIHARA, K., YAMAMOTO, Y., MUKAI, T. and ITOH, M. (2010) Photodynamic antimicrobial activity of avian eggshell pigments. FEBS Letters 584: 770-774.Google Scholar
JOHNSON, A.L. (2000) Reproduction in the female, in: WHITTOW, G.C. (Ed) Sturkie Avian Physiology, 5th Edition, pp. 569-596 (Academic Press, USA).Google Scholar
JONCHERE, V., REHAULT-GODBERT, S., HENNEQUET-ANTIER, C., CABAU, C., SIBUT, V., COGBURN, L.A., NYS, Y. and GAUTRON, J. (2010) Gene expression profiling to identify eggshell proteins involved in physical defence of the chicken egg. BMC Genomics, 11: 57.Google Scholar
JONES, D.R., MUSGROVE, M.T., ANDERSON, K.E. and THESMAR, H.S. (2010) Physical quality and composition of retail shell eggs. Poultry Science 89: 582-587.Google Scholar
JUNG, J.G., LIM, W., PARK, T.S., KIM, J.N., HAN, B.K., SONG G. and HAN, J.Y. (2011) Structural and histological characterisation of oviductal magnum and lectin-binding patterns in Gallus domesticus. Reproductive Biology and Endocrinology 9: 62.Google Scholar
KAMILA, K. (2005) Antimicrobial activity of chicken egg white cystatin. World Journal of Microbiology and Biotechnology 21: 59-64.Google Scholar
KELLER, L.H., BENSON, C.E., KROTEC, K. and ECKROADE, R.J. (1995) Salmonella Enteritidis colonisation of the reproductive tract and forming and freshly laid eggs of chickens. Infection and Immunity 63: 2443-2449.Google Scholar
KENNEDY, G.Y. and VEVERS, H.G. (1973) Eggshell pigments of the Araucano fowl. Comparative Biochemistry and Physiology 44B: 11-25.Google Scholar
KENNEDY, G.Y. and VEVERS, H.G. (1976) A survey of avian eggshell pigments. Comparative Biochemistry and Physiology 55B: 117-123.Google Scholar
KIM, J.W. and SLAVIK, M.F. (1996a) Changes in eggshell surface microstructure after washing with cetylpyridinium chloride or trisodium phosphate. Journal of Food Protection 59 (8): 859-863.Google Scholar
KIM, J.W. and SLAVIK, M.F. (1996b) Use of blue lake as an indicator of bacterial penetration into eggs. Journal of Rapid Methods and Automation in Microbiology 4: 183-190.Google Scholar
KRAMPITZ, G. and WITT, W. (1979) Biochemical aspects of biomineralisation. Biochemistry: Springer Berlin Heidelberg. pp. 57-144.Google Scholar
KUHL, H.J. (2005) The economic and hygienic benefits of egg washing. Proceedings of the XIth European Symposium on the Quality of Eggs and Egg Products, Doorwerth, The Netherlands, pp. 233-236.Google Scholar
KUSUDA, S., IWASAWA, A., DOI, O., OHYA, Y. and YOSHIZAKI, N. (2011) Diversity of the cuticle layer of avian eggshells. Journal of Poultry Science 48: 119-124.Google Scholar
LAMMIE, D., BAIN, M.M. and WESS, T.J. (2005) Microfocus X-ray scattering investigations of eggshell nanotexture. Journal of Synchrotron Radiation 12: 721-726.Google Scholar
LANG, M.R. and WELLS, J.W. (1987) A review of eggshell pigmentation. World's Poultry Science Journal 43 (3): 238-246.Google Scholar
LAVELIN, I., MEIRI, N. and PINES, M. (2000) New insight in eggshell formation. Poultry Science 79: 1014-1017.Google Scholar
LELEU, S., MESSENS, W., DE REU, K., DE PRETER, S., HERMAN, S., HEYNDRICKX, M., DE BAERDEMAEKER, J., MICHIELS, C.W. and BAIN, M. (2011a) Effect of egg washing on the cuticle quality of brown and white table eggs. Journal of Food Protection 74 (10): 1649-1654.Google Scholar
LELEU, S., BAIN, M., HERMAN, L., HEYNDRICKX, M., DE BAERDEMAEKER, J., MICHIELS, C.W., PERIANU, C. and MESSENS, W. (2011b) The effect of microcracks and the presence of the cuticle on trans-shell penetration of table eggs by Salmonella Enteritidis. Proceedings of the European Symposium on the Quality of Eggs and Egg Products, Leipzig, Germany, 2011.Google Scholar
MACLEOD, N., BAIN, M. and HANCOCK, J. (2006) The mechanics and mechanisms of failure of hens’ eggs. International Journal of Fracture 142: 29-41.Google Scholar
MARTINEZ-DE LA PUENTE, J., MERINO, S., MORENO, J., TOMAS, G., MORALES, J., LOBATO, E., GARCIA-FRAILE, S. and MARTINEZ, J. (2007) Are eggshell spottiness and colour indicators of health and condition in blue tits Cyanistes caeruleus? Journal of Avian Biology 38: 377-384.Google Scholar
MAYES, F.J. and TAKEBALLI, M.A. (1983) Microbial contamination of the hen egg: a review. Journal of Food Protection 46: 1092-1098.Google Scholar
MEGAN, L., ROSE, H. and HINCKE, M.T. (2009) Protein constituents of the eggshell: eggshell-specific matrix proteins. Cellular and Molecular Life Sciences 66: 2707-2719.Google Scholar
MERTENS, K., VAESEN, I., LOFFEL, J., KEMPS, B., KAMERS, B., PERIANU, C., ZOONS, J., DARIUS, P., DECUYPERE, E., DE BAERDEMAEKER, J. and DE KETELAERE, B. (2010) The transmission colour value: A novel egg quality measure for recording shell colour used for monitoring the stress and health status of a brown layer flock. Poultry Science 89: 609-617.Google Scholar
MESSENS, W., GRIJSPEERDT, K., DE REU, K., DE KETELAERE, B., MERTENS, K., BAMELIS, F., KEMPS, B., DE BAERDEMAEKER, J., DECUYPERE, E. and HERMAN, L. (2007) Eggshell penetration of various types of hen's eggs by Salmonella enterica serovar Enteritidis. Journal of Food Protection 70: 623-628.Google Scholar
MESSENS, W., GRIJSPEERDT, K. and HERMAN, L. (2005) Eggshell characteristics and penetration by Salmonella enterica serovar Enteritidis through the production period of a layer flock. British Poultry Science 46: 694-700.Google Scholar
MIKSIK, I., CHARVATOVA, J., ECKHARDT, A. and DEYL, Z. (2003) Insoluble eggshell matrix proteins--their peptide mapping and partial characterisation by capillary electrophoresis and high-performance liquid chromatography. Electrophoresis 24 (5): 843-852.Google Scholar
MIKSIK, I., ECKHARDT, A., SEDLAKOVA, P. and MIKULIKOVA, K. (2007) Proteins of insoluble matrix of avian (Gallus gallus) eggshell. Connective Tissue Research 48: 1-8.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.Google Scholar
MORENO, J. and OSORNO, J.L. (2003) Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecology Letters 6: 803-806.Google Scholar
NASCIMENTO, V.P., CRANSTOUN, S. and SOLOMON, S.E. (1992) Relationship between shell structure and moment of Salmonella Enteritidis across the eggshell wall. British Poultry Science 33: 37-48.Google Scholar
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
NYS, Y. and GAUTRON, J. (2007) Structure and Formation of the Eggshell, in: HUOPALAHTI, R., LOPEZ-FANDINO, R., ANTON, M. & SCHADE, R. (Eds) Bioactive Egg Compounds, pp. 99-102 (Springer Berlin Heidelberg).Google Scholar
NYS, Y. and GUYOT, N. (2011) Egg formation and chemistry, in: NYS, Y., BAIN, M. & IMMERSEEL, F.V. (Eds) Improving the safety and quality of eggs and egg products, Vol. 1, pp. 83-132 (Woodhead Publishing Limited).Google Scholar
NYS, Y., GAUTRON, J., GARCIA-RUIZ, J.M. and HINCKE, M.T. (2004) Avian eggshell mineralisation: biochemical and functional characterisation of matrix proteins. Comptes Rendus Palevol 3: 549-562.Google Scholar
NYS, Y., HINCKE, M., ARIAS, J.L. GARCIA-RUIZ, J.M. and SOLOMON, S.E. (1999) Avian eggshell mineralisation. Poultry and Avian Biology Reviews 10: 143-166.Google Scholar
NYS, Y., ZAWADZKI, J., GAUTRON, J. and MILLS, A.D. (1991) Whitening of brown-shelled eggs: mineral composition of uterine fluid and rate of protoporphyrin deposition. Poultry Science 70: 1236-1245.Google Scholar
PARK, C.M., HUNG, Y.C., LIN, C.S. and BRACKETT, R.E. (2005) Efficacy of electrolyzed water in inactivating Salmonella Enteritidis and Listeria monocytogenes on shell eggs. Journal of Food Protection 68 (5): 986-990.Google Scholar
PARSONS, A.H. (1982) Structure of the eggshell. Poultry Science 61: 2013-2021.Google Scholar
PEEBLES, E.D. and BRAKE, J. (1986) The role of the cuticle in water vapor conductance by the eggshell of broiler breeders. Poultry Science 65: 1034-1039.Google Scholar
PELLEGRINI, A., HULSMEIER, A.J., HUNZIKER, P. and THOMAS, U. (2004) Proteolytic fragments of ovalbumin display antimicrobial activity. Biochimica et Biophysica Acta 1672: 76-85.Google Scholar
RAHMAN, M.A., MORIYAMA, A., IWASAWA, A. and YOSHIZAKI, N. (2009) Cuticle formation in quail eggs. Zoological Science Japan 26: 496-499.Google Scholar
RICHARDS, P.D.G. and DEEMING, D.C. (2001) Correlation between shell colour and ultrastructure in pheasant eggs. British Poultry Science 42: 338-343.Google Scholar
ROBERTS, J.R., CHOUSALKAR, K. and SAMIULLAH (2013) Egg quality and age of laying hens: implications for product safety. Animal Production Science 53: 1291-1297.Google Scholar
RODRIGUEZ-NAVARRO, A., KALIN, O., NYS, Y. and GARCIA-RUIZ, J.M. (2002) Influence of the microstructure on the shell strength of eggs laid by hens of different ages. British Poultry Science 43: 395-403.Google Scholar
ROSE, M.L.H. and HINCKE, M.T. (2009) Protein constituents of the eggshell: eggshell-specific matrix proteins. Cellular and Molecular Life Sciences 66: 2707-2719.Google Scholar
ROSE-MARTEL, M., DU, J. and HINCKE, M.T. (2012) Proteomic analysis provides new insight into the chicken eggshell cuticle. Journal of Proteomics 75 (9): 2697-2706.Google Scholar
RUIZ, J. and LUNAM, C.A. (2000) Ultrastructural analysis of the eggshell: contribution of the individual calcified layers and the cuticle to hatchability and egg viability in broiler breeders. British Poultry Science 41: 584-592.Google Scholar
SAMIULLAH (2012) The eggshell quality of table eggs and how this affects food safety. Master of Rural Science Degree Thesis, University of New England Armidale NSW Australia.Google Scholar
SAMIULLAH, CHOUSALKAR, K.K., ROBERTS, J.R., SEXTON, M., MAY, D. and KIERMEIER, A. (2013) Effects of eggshell quality and washing on Salmonella Infantis penetration. International Journal of Food Microbiology 165: 77-83.Google Scholar
SAMIULLAH and ROBERTS, J.R. (2013) The location of protoporphyrin in the eggshell of brown shelled eggs. Poultry Science 92: 2783-2788.Google Scholar
SHEPHERD, J.H., MULVIHILL, E.R., THOMAS, P.S. and PALMITER, R.D. (1980) Commitment of chick oviduct tubular gland cells to produce ovalbumin mRNA during hormonal withdrawal and restimulation. Journal of Cell Biology 87: 142-151.Google Scholar
SILPHADUANG, U., HINCKE, M.T., NYS, Y. and MINE, Y. (2006) Antimicrobial proteins in chicken reproductive system. Biochemical and Biophysical Research Communications 340: 648-655.Google Scholar
SIMONS, P.C.M. (1971) Ultrastructure of the hen eggshell and its physiological interpretation. Online retrieved from: http://edepot.wur.nl/194052.Google Scholar
SIMONS, P.C.M. and WIERTZ, G. (1963) Notes on the structure of membranes and shell in the hen egg: an electron microscopical study. Zeitschrift fur Zellforschung 59: 555-567.Google Scholar
SOLOMON, S.E. (1991) Egg and shell quality. Published by Wolfe publishing ltd. England. P. 149.Google Scholar
SOLOMON, S.E. (1992) Eggshell quality and microbial penetration. Poultry International, May, 1992, pp. 20-22.Google Scholar
SOLOMON, S.E., BAIN, M.M., CRANSTOUN, S. and NASCIMENTO, V. (1994) Hen's eggshell structure and function, in: BOARD, R.G. & FULLER, R. (Eds) Microbiology of the Avian Egg, pp. 1-24 (Springer US).Google Scholar
SPARKS, N.H.C. (1994) Shell accessory materials: structure and function, in: BOARD, R.G. & FULLER, R. (Eds) Microbiology of the Avian Egg, pp. 25-42 (Chapman and Hall London).Google Scholar
SPARKS, N.H.C. and BOARD, R.G. (1984) Cuticle, shell porosity and water intake through hen eggshells. British Poultry Science 25: 267-276.Google Scholar
SPARKS, N.H. and BOARD, R.G. (1985) Bacterial penetration of the recently oviposited shell of hens’ eggs. Australian Veterinary Journal 62: 169-170.Google Scholar
THOMPSON, M.B. and GOLDIE, K.N. (1990) Conductance and structure of eggs of Adelie penguins, Pygoscelis adeliae, and its implications for incubation. The Condor 92 (2): 304-312.Google Scholar
TULLETT, S.G. (1975) Regulation of avian eggshell porosity. Journal of Zoology 177: 339-348.Google Scholar
TULLETT, S.G. and BOARD, R.G. (1977) Determinants of avian eggshell porosity. Journal of Zoology 183: 203-211.Google Scholar
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. British Poultry Science 16: 93-95.Google Scholar
TUNG, M.A., GARLAND, M.R. and GILL, P.K. (1979) A scanning electron microscope study of bacterial invasion in hen's eggshell. Canadian Institute of Food Science and Technology Journal 12: 16-22.Google Scholar
VADEHRA, D.V., BAKER, R.C. and NAYLOR, H.B. (1970) Role of cuticle in spoilage of chicken eggs. Journal of Food Science 35: 5-6.Google Scholar
VALENTI, P., ANTONINI, G., VON HUNOLSTEIN, C., VISCA, P., ORSI, N. and ANTONINI, E. (1983) Studies of the antimicrobial activity of ovotransferrin. International Journal of Tissue Reactions 5: 97-105.Google Scholar
WALKER, A.W. and HUGHES, B.O. (1998) Eggshell colour is affected by laying cage design. British Poultry Science 39: 696-699.Google 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 (3): 276-279.Google Scholar
WANGENSTEEN, O.D., WILSON, D. and RAHN, H. (1970) Diffusion of gases across the shell of the hen's egg. Respiration Physiology 11: 16-30.Google Scholar
WEDRAL, E.M., VADEHRA, D.U. and BAKER, R.C. (1974) Chemical composition of the cuticle and inner and outer membranes from eggs of Gallus gallus. Comparative Biochemistry and Physiology 47B: 231-240.Google Scholar
WELLMAN-LABADIE, O., LEMAIRE, S., MANN, K., PICMAN, J. and HINCKE, M.T. (2010) Antimicrobial activity of lipophilic avian eggshell surface extracts. Journal of Agricultural and Food Chemistry 58: 10156-10161.Google Scholar
WELLMAN-LABADIE, O., PICMAN, J. and HINCKE, M.T. (2008a) Antimicrobial activity of cuticle and outer eggshell protein extracts from three species of domestic birds. British Poultry Science 49 (2): 133-143.Google Scholar
WELLMAN-LABADIE, O., PICMAN, J. and HINCKE, M.T. (2008b) Antimicrobial activity of the anseriform outer eggshell and cuticle. Comparative Biochemistry and Physiology, Part B 149: 640-649.Google Scholar
WESIERSKA, E., SALEH, Y., TRZISZKA, T., KOPEC, W. and SIEWINSKI, M. (2005) Antimicrobial activity of chicken egg white cystatin. World Journal of Biotechnology & Microbiology 22: 59-64.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 (3): 445-466.Google Scholar
WILLIAMS, J.E. and WHITTEMORE, A.D. (1967) A method for studying microbial penetration through the outer structures of the avian egg. Avian Diseases 11: 467-490.Google Scholar
WYBURN, G.M., JOHNSTON, H.S., DRAPER, M.H. and DAVIDSON, M.F. (1973) The ultrastructure of the shell forming region of the oviduct and the development of the shell of Gallus domesticus. Quarterly Journal of Experimental Physiology 58: 143-151.Google Scholar
XING, J., WELLMAN-LABADIE, O., GAUTRON, J. and HINCKE, M.T. (2007) Recombinant eggshell ovocalyxin-32: Expression, purification and biological activity of the glutathione S-transferase fusion protein. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 147: 172-177Google Scholar