Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T10:04:57.558Z Has data issue: false hasContentIssue false
  • English
  • Français

Bacterial contamination of table eggs and the influence of housing systems

Published online by Cambridge University Press:  07 May 2008

K. DE REU ,
W. MESSENS ,
M. HEYNDRICKX ,
T.B. RODENBURG ,
M. UYTTENDAELE  and
L. HERMAN
K. DE REU*
Affiliation:
Institute for Agricultural and Fisheries Research, Technology and Food Unit, Brusselsesteenweg 370, 9090 Melle, Belgium
W. MESSENS
Affiliation:
Institute for Agricultural and Fisheries Research, Technology and Food Unit, Brusselsesteenweg 370, 9090 Melle, Belgium
M. HEYNDRICKX
Affiliation:
Institute for Agricultural and Fisheries Research, Technology and Food Unit, Brusselsesteenweg 370, 9090 Melle, Belgium
T.B. RODENBURG
Affiliation:
Animal Breeding and Genomics Centre, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands
M. UYTTENDAELE
Affiliation:
Department of Food Safety and Food Quality, Laboratory of Food Microbiology and Food Preservation, University of Ghent, Coupure Links 653, 9000 Ghent, Belgium
L. HERMAN
Affiliation:
Institute for Agricultural and Fisheries Research, Technology and Food Unit, Brusselsesteenweg 370, 9090 Melle, Belgium
*
Corresponding author: [email protected]
Get access

Abstract

With the introduction of alternative housing systems for laying hens in the EU, recent research has focussed on the bacterial contamination of table eggs, e.g. eggshell and egg content contamination. Contamination of eggshells with aerobic bacteria is generally higher for nest eggs from non-cage systems compared to nest eggs from furnished cages or eggs from conventional cages. Studies indicate limited or no systematic differences in eggshell contamination with aerobic bacteria between eggs laid in the nest boxes of furnished cages and eggs laid in conventional cages. The major differences found in experimental studies between cage- and non-cage systems are less pronounced under commercial conditions. The effect of housing system on eggshell contamination with specific groups of bacteria is variable. Limited information is available on the influence of housing system on egg content contamination. Recent research does not indicate large differences in egg content contamination between eggs from cage- and non-cage systems (ignoring outside nest and floor eggs). The microflora of the eggshell is dominated by Gram-positive bacteria, whereas Gram-negative bacteria are best equipped to overcome the antimicrobial defences of the egg content. Much of the research on eggshell and egg content contamination focuses on Salmonella, since infection with Salmonella enteritidis, resulting from the consumption of contaminated eggs or egg products, is still a major health problem. Observed Salmonella prevalence on the eggshell and in the egg content vary, depending on the fact whether investigations were based on randomly sampled table eggs or on eggs from naturally infected hens. The limited information available on other pathogens shows that they are exclusively isolated from the eggshell and not from the internal contents.

Keywords

bacterial eggshell contaminationegg content contaminationhousing systems laying henstable eggsfood safety
Type
Review Article
Information
World's Poultry Science Journal , Volume 64 , Issue 1 , March 2008 , pp. 5 - 19
Copyright
Copyright © World's Poultry Science Association 2008

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

ABRAHAMSSON, P. and TAUSON, R. (1995) Aviary systems and conventional cages for laying hens. Acta agriculturae scandinavica, section A, Animal Science 45: 191-203.Google Scholar
ANON, (1999) Council Directive 1999/74/EC of 19 July 1999 laying down minimum standards for the protection of laying hens. Official Journal of the European Communities L203: 53-57.Google Scholar
ANON, (2004a) Final report of EggDefence project QLRT-2001-01606: Improving quality and safety of hen eggs in new production system by reinforcing the antimicrobial natural defence and by developing tools for grading eggs. Nouzilly, France, European Commission: 127-131, 366 p.Google Scholar
ANON, (2004b) Report of the survey of Salmonella contamination of UK produced shell eggs on retail sale. London, Food Standard Agency: 124 p.Google Scholar
BAKER, R.C., QURESHI, R.A., SANDHU, T.S. and TIMONEY, J.F. (1985) The frequency of salmonellae on duck eggs. Poultry Science 64: 646-652.CrossRefGoogle ScholarPubMed
BOARD, R.G., AYRES, J.C., KRAFT, A.A. and FORSYTHE, R.H. (1964) The microbiological contamination of egg shells and egg packaging materials. Poultry Science 43: 584-594.CrossRefGoogle Scholar
BOARD, R.G. and TRANTER, H.S. (1995) The microbiology of eggs. Egg science and technology. W.J. Stadelman, Cotterill, O.J. (Eds.). New York, Food Products Press - The Haworth Press, Inc.: 81-104.Google Scholar
BRACKETT, R.E. and BEUCHAT, L.R. (1992) Survival of Listeria monocytogenes on the surface of egg shells and during frying of whole and scrambled eggs. Journal of Food Protection 55: 862-865.CrossRefGoogle ScholarPubMed
BRUCE, J. and DRYSDALE, E.M. (1994) Trans-shell transmission. Microbiology of the avian egg. R.G. Board and R. Fuller (Eds.). London, Chapman & Hall: 63-91.Google Scholar
BRUCE, J. and JOHNSON, A.L. (1978) The bacterial flora of unhatched eggs. British Poultry Science 19: 681-689.Google Scholar
CEPERO, R., MARIA, G. and HERNANDIS, A. (2001) Calidad del huevo en jaulas enriquecidas: Resultados en la fase final de puesta. XXXVIII Symposium Sec. Esp. WPSA, I Congreso Internacional de Sanidad y Producción Animal, Noviembre 2001 - Conference proceedings, Córdoba, Spain.Google Scholar
CEPERO, R., YANGÜELA, J., LIDÓN, M.D. and HERNANDIS, A. (2000) Calidad del huevo en jaulas enriquecidas. XXXVII Symposium Sec. Esp. WPSA, I Congreso Internacional de Sanidad y Producción Animal, Noviembre 2000 - Conference proceedings, Barcelona, Spain: 61-80.Google Scholar
DE BOER, E. and WIT, B. (2000) Salmonella in eieren. Tijdschrift voor Diergeneeskunde 125: 126-127.Google Scholar
DE REU, K. (2006) Bacteriological contamination and infection of shell eggs in the production chain. PhD Thesis. Faculty of Bioscience Engineering. University of Ghent. Ghent.Google Scholar
DE REU, K., GRIJSPEEDT, K., HEYNDRICKX, M., UYTTENDAELE, M. and HERMAN, L. (2005a) The use of total aerobic and Gram-negative flora for quality assurance in the production chain of consumption eggs. Food Control 16: 147-155.CrossRefGoogle Scholar
DE REU, K., GRIJSPEERDT, K., HERMAN, L., HEYNDRICKX, M., UYTTENDAELE, M., DEBEVERE, J., PUTIRULAN, F.F. and BOLDER, N.M. (2006a) The effect of a commercial UV disinfection system on the bacterial load of shell eggs. Letters in Applied Microbiology 42: 144-148.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
DE REU, K., GRIJSPEERDT, K., HEYNDRICKX, M., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2006c) Bacterial eggshell contamination in the egg collection chains of different housing systems for laying hens. British Poultry Science 47: 163-172.CrossRefGoogle ScholarPubMed
DE REU, K., GRIJSPEERDT, K., HEYNDRICKX, M., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2006d) Bacterial shell contamination in the egg handling chains of different housing systems for laying hens. XIIth European Poultry Conference - Conference proceedings, Verona, Italy: Abstracts & Proceedings CD, 6p.CrossRefGoogle Scholar
DE REU, K., GRIJSPEERDT, K., HEYNDRICKX, M., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2006e) Bacterial shell contamination in the egg handling chains of different housing systems for laying hens. World's Poultry Science Journal 62 (supplement): 562-563.Google Scholar
DE REU, K., GRIJSPEERDT, K., HEYNDRICKX, M., ZOONS, J., DE BAERE, K., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2005b) Bacterial eggshell contamination in conventional cages, furnished cages and aviary housing systems for laying hens. British Poultry Science 46: 149-155.CrossRefGoogle ScholarPubMed
DE REU, K., GRIJSPEERDT, K., MESSENS, W., HEYNDRICKX, M., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2006f) Eggshell factors influencing eggshell penetration and whole egg contamination by different bacteria, including Salmonella Enteritidis. International Journal of Food Microbiology 112: 253-260.CrossRefGoogle ScholarPubMed
DE REU, K., HEYNDRICKX, M., GRIJSPEERDT, K., RODENBURG, B., TUYTTENS, F., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2006g) Assessment of the vertical and horizontal aerobic bacterial infection of shell eggs. World's Poultry Science Journal 62 (supplement): 564.Google Scholar
DE REU, K., HEYNDRICKX, M., GRIJSPREEDT, K., RODENBURG, B., TUYTTENS, F., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2007a) Estimation of the vertical and horizontal bacterial infection of hen's table eggs. XVIII European symposium on the quality of poultry meat & XII European symposium on the quality of eggs and egg products - Conference proceedings, Prague, Czech Republic: 55-56.Google Scholar
DE REU, K., RODENBURG, B., GRIJSPEERDT, K., HEYNDRICKX, M., TUYTTENS, F., ZOONS, J. and HERMAN, L. (2007b) Bacteriological contamination of eggs and eggshell quality in furnished cages and non-cage systems for laying hens: an international on-farm comparison. XVIII European symposium on the quality of poultry meat & XII European symposium on the quality of eggs and egg products - Conference proceedings, Prague, Czech Republic: 46-47.Google Scholar
DOYLE, M.P. (1984) Association of Campylobacter jejuni with laying hens and eggs. Applied Environmental Microbiology 47: 533-536.CrossRefGoogle ScholarPubMed
EBEL, E. and SCHLOSSER, W.D. (2001) Estimating the annual fraction of eggs contaminated with Salmonella Enteritidis in the United States. International Journal of Food Microbiology 61: 51-62.Google Scholar
ELLEN, H.H., BOTTCHER, R.W., VON WACHENFELT, E. and TAKAI, H. (2000) Dust levels and control methods in poultry houses. Journal of Agricultural Safety and Health 6: 275-282.CrossRefGoogle ScholarPubMed
FAVIER, G.I., ESCUDERO, M.E. and GUZMÁN, A.M.S. (2005) Genotypic and phenotypic characteristics of Yersinia enterocolitica isolated from the surface of chicken eggshells obtained in Argentina. Journal of Food Protection 68: 1812-1815.Google Scholar
FAVIER, G.I., ESCUDERO, M.E., MATTAR, M.A. and GUZMAN, A.M.S. (2000) Survival of Yersinia enterocolitica and mesophilic aerobic bacteria on eggshell after washing with hypochlorite and organic acid solutions. Journal of Food Protection 63: 1053-1057.CrossRefGoogle ScholarPubMed
GAST, R.K. and BEARD, C.W. (1990) Production of Salmonella enteritidis-contaminated eggs by experimentally infected hens. Avian Diseases 34: 438-446.Google Scholar
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: 152-156.CrossRefGoogle ScholarPubMed
GENTRY, R.F. and QUARLES, C.L. (1972) The measurement of bacterial contamination on eggshells. Poultry Science 51: 930-933.Google Scholar
HAINES, R.H. (1938) Observation on the bacterial flora of the hen's egg with a description of new species of Proteus and Pseudomonas causing rot in eggs. Journal of Hygiene Cambridge 38: 338-355.Google Scholar
HARRY, E.G. (1963) The relationship between egg spoilage and the environment of the egg when laid. British Poultry Science 4: 91-100.Google Scholar
HUMPHREY, T.J. (1989) Salmonella Enteritidis phage type 4 and hens' eggs. Lancet I: 281.Google Scholar
HUMPHREY, T.J. (1994a) Contamination of egg shell and contents with Salmonella enteritidis: a review. International Journal of Food Microbiology 21: 31-40.CrossRefGoogle ScholarPubMed
HUMPHREY, T.J. (1994b) Contamination of eggs with potential pathogens. Microbiology of the avian egg. R.G. Board and R. Fuller (Eds.). London, Chapman & Hall: 93-116.Google Scholar
HUMPHREY, T.J., BASKERVILLE, A., MAWER, S., ROWE, B. and HOPPER, S. (1989) Salmonella enteritidis phage type 4 from the contents of intact eggs: A study involving naturally infected eggs. Epidemiology and Infection 103: 415-423.CrossRefGoogle Scholar
HUMPHREY, T.J., CHART, H., BASKERVILLE, A. and ROWE, B. (1991a) The influence of age on the response of SPF hens to infection with S. enteritidis PT4. Epidemiology and Infection 106: 33-43.Google Scholar
HUMPHREY, T.J., WHITEHEAD, A., GAWER, A.H.L., HENLEY, A. and ROWE, B. (1991b) Numbers of Salmonella enteritidis in the contents of naturally contaminated hen's eggs. Epidemiology and Infection 106: 489-496.CrossRefGoogle Scholar
JONES, D.R., MUSGROVE, M.T. and NORTHCUTT, J.K. (2004) Variations in external and internal microbial populations in shell eggs during extended storage. Journal of Food Protection 67: 2657-2660.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
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 of chickens. Infection and Immunity 63: 2443-2449.CrossRefGoogle ScholarPubMed
KINDE, H., READ, R.P., CHIN, R.P., BICKFORD, A.A., WALKER, R.L., ARDANS, A., BREITMEYER, R.E., WILLOUGHBY, D., LITTLE, H.E., KERR, D. and GARDNER, I.A. (1996) Salmonella enteritidis, phage type 4 infection in a commercial layer flock in southern California: bacteriologic and epidemiologic findings. Avian Diseases 40: 665-671.CrossRefGoogle Scholar
KNAPE, K.D., CAREY, J.B., BURGESS, R.P., KWON, Y.M. and RICKE, S.C. (1999) Comparison of chlorine with an iodine-based compound on eggshell surface microbial populations in a commercial egg washer. Journal of Food Safety 19: 185-194.CrossRefGoogle Scholar
KNAPE, K.D., CHAVEZ, C., BURGESS, R.P., COUFAL, C.D. and CAREY, J.B. (2002) Comparison of eggshell surface microbial populations for in-line and off-line commercial egg processing facilities. Poultry Science 81: 695-698.CrossRefGoogle ScholarPubMed
LARSSON, B.-M., LARSSON, K., MALMBERG, P., MARTENSSON, L. and PALMBERG, L. (1999) Airway responses in naive subjects to exposure in poultry houses: Comparison between cage rearing system and alternative rearing system for laying hens. American Journal of Industrial Medicine 35: 142-149.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
LUCORE, L.A., JONES, F.T., KENNETH, E.A. 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: 1324-1328.CrossRefGoogle Scholar
MALLET, S., GUESDON, V., AHMED, A.M.H. and NYS, Y. (2006) Comparison of eggshell hygiene in two housing systems: Standard and furnished cages. British Poultry Science 47: 30-35.CrossRefGoogle ScholarPubMed
MALLET, S., GUESDON, V. and NYS, Y. (2004) Hygienic properties of eggs laid at different locations in two furnished cage models. XXII thWorld's Poultry Congress, Full paper CD - category N1 - Nutrition and management aspects of quality and safety of eggs - Conference proceedings, Istanbul, Turkey: 6 p.Google Scholar
MAWER, S.L., SPAIN, G.E. and ROWE, B. (1989) Salmonella enteritidis phage type 4 and hens' eggs. Lancet I: 280-281.CrossRefGoogle Scholar
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., 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
MESSENS, W., GRIJSPEERDT, K. and HERMAN, L. (2006) Eggshell penetration of hen's eggs by Salmonella enterica serovar Enteritidis upon various storage conditions. British Poultry Science 47: 554-560.CrossRefGoogle ScholarPubMed
MICHEL, V. and HUONNIC, D. (2003) A comparison of welfare, health and production performance of laying hens reared in cages or aviaries. British Poultry Science 43: 775-776.CrossRefGoogle Scholar
MITCHELL, R., LITTLE, C., WARD, L. and SURMAN, S. (2002) Public health investigations of Salmonella Enteritidis in raw shell eggs in England and Wales. Eurosurveillance weekly p. 50.CrossRefGoogle Scholar
MUSGROVE, M. (2004) Effects of processing on the microbiology of commercial shell eggs. PhD Thesis. U.S. Department of Agriculture. University of Georgia. Athens.Google Scholar
MUSGROVE, M.T., JONES, D.R., NORTHCUTT, J.K., COX, N.A. and HARRISON, M.A. (2005) Identification of Enterobacteriaceae from washed and unwashed commercial shell eggs. Journal of Food Protection 67: 2613-2616.CrossRefGoogle Scholar
NITCHEVA, L., YONKOVA, V., POPOV, V. and MANEV, C. (1990) Listeria isolation from foods of animal origin. Acta Veterinaria Hungaria 37: 223-225.Google ScholarPubMed
OKAMURA, M., MIYAMOTO, T., KAMIJIMA, Y., TANI, H., SASAI, K. and BABA, E. (2001) Differences in abilities to colonize reproductive organs and to contaminate eggs in intravaginally inoculated hens and in vitro adherences to vaginal explants between Salmonella Enteritidis and other Salmonella serovars. Avian Diseases 45: 962-971.CrossRefGoogle 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.Google Scholar
PETERSEN, S., NONNENMANN, M., RAUTIAINEN, M., DEMMERS, T.G., BANHAZI, T. and LYNGBYE, M. (2000) Dust in pig buildings. Journal of Agricultural Safety and Health 6: 261-274.CrossRefGoogle Scholar
PETRAK, K., PETRAK, T., JELIC, A., NEDJELI, S. and HRASTE, A. (1999) Correlation between initial bacteriological egg contamination and the technological preservation process. VIII thEuropean Symposium on the Quality of Eggs and Egg Products. - Conference proceedings, Bologna, Italy: 561-567.Google Scholar
POPPE, C., DUNCAN, C. and MAZZOCCO, A. (1998) Salmonella contamination of hatching and table eggs: a comparison. Canadian Journal of Veterinary Research 62: 191-198.Google ScholarPubMed
PROTAIS, J., QUEGUINER, S., BOSCHER, E., PIQUET, J.-C., NAGARD, B. and SALVAT, G. (2003a) Effect of housing system on the bacterial flora in the air and on egg shells. X thEuropean Symposium on the Quality of Eggs and Egg Products - Conference proceedings, Saint-Brieuc, Ploufragan, France: 142-149.Google Scholar
PROTAIS, J., QUEGUINER, S., BOSCHER, E., PIQUET, J.-C., NAGARD, B. and SALVAT, G. (2003b) Effect of housing system on the bacterial flora of the air. British Poultry Science 44: 778-779.CrossRefGoogle ScholarPubMed
PROTAIS, J., QUEGUINER, S., BOSCHER, E., PIQUET, J.-C., NAGARD, B. and SALVAT, G. (2003c) Effects of housing system on the bacterial flora of egg shells. British Poultry Science 44: 788-789.CrossRefGoogle ScholarPubMed
QUARLES, C.L., GENTRY, R.F. and BRESSLER, G.O. (1970) Bacterial contamination in poultry houses and its relationship to egg hatchability. Poultry Science 49: 60-66.CrossRefGoogle Scholar
RODENBURG, B., TUYTTENS, F., DE REU, K., HERMAN, L., ZOONS, J. and SONCK, B. (2005) Welfare, health and hygiene of laying hens housed in furnished cages and in alternative housing systems. Journal of Applied Animal Welfare Science 8: 211-226.CrossRefGoogle ScholarPubMed
RODENBURG, B., TUYTTENS, F., DE REU, K., HERMAN, L., ZOONS, J. and SONCK, B. (2006) Welfare of laying hens in furnished cages and in non-cage systems. 40th International Congress of the ISAE - Conference proceedings, Bristol, United Kingdom p.102.Google Scholar
SAHIN, O., KOBALKA, P. and ZHANG, Q. (2003) Detection and survival of Campylobacter in chicken eggs. Journal of Applied Microbiology 95: 1070-1079.CrossRefGoogle ScholarPubMed
SALVAT, G., PROTAIS, J., LAHELLEC, C. and COLIN, P. (1991) Excretionate of Salmonella enteritidis in laying hens following a production of Salm. enteritidis contaminated eggs responsible for foodborne disease. Quality of Poultry Products III, Safety and Marketing Aspects. R.W.A.W. Mulder and A.W. de Vries (Eds.). Beekbergen, Spelderholt Centre for Poultry Research and Information Services: 35-42.Google Scholar
SCHLOSSER, W.D., HENZLER, D.J., MASON, D., KRADEL, L., SHIPMAN, S., TROCK, S., HURD, S.H., HOGUE, A.T., SISCHO, W. and EBEL, E. (1999) The Salmonella enterica serovar Enteritidis pilot project. Salmonella enterica serovar Enteritidis in humans and animals. A.M. Saeed, K. Gast, M.E. Potter and P.G. Wall (Eds.). Ames, Iowa, Iowa State University Press: 353-365.Google Scholar
SCHOENI, J.L. and DOYLE, M.P. (1994) Variable colonization of chickens perorally inoculated with Escherichia coli O157:H7 and subsequent contamination of eggs. Applied and Environmental Microbiology 60: 2958-2962.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: 385-396.CrossRefGoogle ScholarPubMed
SEVIOUR, E.M. and BOARD, R.G. (1972) The behaviour of mixed bacterial infections in the shell membranes of the hen's egg. British Poultry Science 13: 33-43.CrossRefGoogle ScholarPubMed
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. Australian Veterinary Journal 55: 592-3.CrossRefGoogle ScholarPubMed
SMITH, A., ROSE, S.P., WELLS, R.G. and PIRGOZLIEV, V. (2000) The effect of changing the excreta moisture of caged hens on the excreta and microbial contamination. British Poultry Science 41: 168-173.CrossRefGoogle ScholarPubMed
TAUSON, R. (2002) Furnished cages and aviaries: production and health. World's Poultry Science Journal 58: 49-63.CrossRefGoogle Scholar
TAUSON, R., WAHLSTRÖM, A. and ABRAHAMSSON, P. (1999) Effect of two floor housing systems and cages on health, production and fear response in layers. Journal of Applied Poultry Research 8: 152-159.Google Scholar
WALL, H., TAUSON, R. and ELWINGER, K. (2002) Effects of nest design, passages and hybrid on use of nest and production performance of layers in furnished cages. Poultry Science 81: 333-339.CrossRefGoogle ScholarPubMed
ZOONS, J., SMEYERS, K., CALDERS, R., DE REU, K. and THIJS, J. (2005) Evaluatie van de werkomstandigheden in volière en verrijkte kooien voor leghennen. Pluimvee Januari 2005: 14-15.Google Scholar