Skip to main content Accessibility help
×
Home

Egg-borne infections of humans with salmonella: not only an S. enteritidis problem

  • E.J. THRELFALL (a1), J. WAIN (a1), T. PETERS (a1), C. LANE (a1), E. DE PINNA (a1), C.L. LITTLE (a1), A.D. WALES (a2) and R.H. DAVIES (a2)...

Abstract

The principal salmonella serovar associated with infections linked to eggs and egg products in the UK, most European countries and North America is Salmonella enteritidis. However, other serovars have also been implicated in a number of egg-associated outbreaks, most notably S. typhimurium exhibiting a range of phage types. The present article reviews human egg-associated salmonellosis associated with non-S. enteritidis serovars, predominantly in the European Union (EU) but also world-wide, using information from published literature and epidemiological databases. There are also brief reviews of S. enteritidis and of mechanisms leading to egg contamination by salmonella. The numbers of egg-associated infections caused by non-S. enteritidis serovars are fairly substantial (for example 22% of outbreaks and 11.5% of more than 20,000 cases in the EU in 2008), and such infections have resulted in hospitalisations and deaths. Furthermore, in parts of the world where S. enteritidis historically has not penetrated laying hen breeding flocks, egg-related salmonellosis is a problem associated specifically with non-S. enteritidis serovars. Control measures to limit the incidence of S. enteritidis and S. typhimurium in poultry flocks are vital. It is therefore important that close surveillance of salmonellosis incidence and serovars in laying flocks is used to establish suitable biosecurity and vaccination programmes throughout EU Member States and elsewhere.

Copyright

Corresponding author

Corresponding author: e.j.threlfall@btinternet.com

References

Hide All
ANON. (2002) Public health investigation of salmonella enteritidis in raw shell eggs. CDR Weekly 12: 3-5. http://www.hpa.org.uk/cdr/archives/back_issues_list.htm (accessed 23rd Aug 2010).
ANON. (2003) Commission Regulation (EC) No 2295 ⁄ 2003 of 23 December 2003 introducing detailed rules for implementing Council Regulation (EEC) No 1907 ⁄ 90 on certain marketing standards for eggs. Official Journal of the European Union L340: 16-34.
ARNEDO, A., BELLIDO, J.B., PAC, M.R., CRIADO, J., USERA, M.A., MESANZA, I., GONZALEZ, F., PEREZ, R. and CORTES, J.M. (1998) Brotes epidemicos de salmonelosis por consumo de huevos [Epidemic outbreaks of salmonellosis caused by eating eggs]. Enfermedades Infecciosas y Microbiologia Clinica 16: 408-412.
ASEFFA, A., MENGISTU, G. and TIRUNEH, M. (1994) salmonella newport: outbreak of food poisoning among college students due to contaminated undercooked eggs. Ethiopian Medical Journal 32: 1-6.
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: 488-491.
BAUMLER, A.J., HARGIS, B.M. and TSOLIS, R.M. (2000) Tracing the origins of salmonella outbreaks. Science 287: 50-52.
BRAUN, P., MAYER, K. and FEHLHABER, K. (2002) Breaking procedure as an important way of contamination of the liquid egg product with salmonella enteritidis. Archiv Für Lebensmittelhygiene 53: 124-126.
BROUGHTON, E.I., HEFFERNAN, H.M. and COLES, C.L. (2010) salmonella enterica serotypes and antibiotic susceptibility in New Zealand, 2002-2007. Epidemiology and Infection 138: 322-329.
CARRAMIÑANA, J.J., HUMBERT, F., ERMEL, G. and COLIN, P. (1997) Molecular epidemiological investigation of salmonella typhimurium strains related to an egg-borne outbreak. Research in Microbiology 148: 633-636.
CARRIQUE-MAS, J.J., BRESLIN, M., SNOW, L., ARNOLD, M.E., WALES, A., MCLAREN, I. and DAVIES, R.H. (2008) Observations related to the salmonella EU layer baseline survey in the United Kingdom: follow-up of positive flocks and sensitivity issues. Epidemiology and Infection 136: 1537-1546.
CARRIQUE-MAS, J.J., BRESLIN, M., SNOW, L., MCLAREN, I., SAYERS, A.R. and DAVIES, R.H. (2009) Persistence and clearance of different salmonella serovars in buildings housing laying hens. Epidemiology and Infection 137: 837-846.
CDC (2008) salmonella surveillance: annual summary, 2006. US Department of Health and Human Services Centers for Disease Control. (Atlanta, Georgia, USA). http://www.cdc.gov/ncidod/dbmd/phlisdata/Salmonella.htm.
CHAPMAN, P.A., RHODES, P. and RYLANDS, W. (1988) salmonella typhimurium phage type 141 infections in Sheffield during 1984 and 1985: association with hens' eggs. Epidemiology and Infection 101: 75-82.
CHEMALY, M., HUNEAU-SALAUN, A., LABBE, A., HOUDAYER, C., PETETIN, I. and FRAVALO, P. (2009) Isolation of salmonella enterica in laying-hen flocks and assessment of eggshell contamination in France. Journal of Food Protection 72: 2071-2077.
CHITTICK, P., SULKA, A., TAUXE, R.V. and FRY, A.M. (2006) A summary of national reports of foodborne outbreaks of salmonella Heidelberg infections in the United States: clues for disease prevention. Journal of Food Protection 69: 1150-1153.
CORKISH, J.D., DAVIES, R.H., WRAY, C. and NICHOLAS, R.A.J. (1994) Observations on a broiler breeder flock naturally infected with salmonella enteritidis phage type 4. Veterinary Record 134: 591-594.
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.
COX, N.A., BERRANG, M.E. and CASON, J.A. (2000) salmonella penetration of egg shells and proliferation in broiler hatching eggs - a review. Poultry Science 79: 1571-1574.
COYLE, E.F., PALMER, S.R., RIBEIRO, C.D., JONES, H.I., HOWARD, A.J., WARD, L. and ROWE, B. (1988) salmonella enteritidis phage type 4 infection: association with hen's eggs. Lancet 332: 1295-1297.
DAVIES, R. and BRESLIN, M. (2003) Observations on salmonella contamination of commercial laying farms before and after cleaning and disinfection. Veterinary Record 152: 283-287.
DAVIES, R. and BRESLIN, M. (2004) Observations on salmonella contamination of eggs from infected commercial laying flocks where vaccination for salmonella enterica serovar enteritidis had been used. Avian Pathology 33: 135-146.
DE BUCK, J., VAN IMMERSEEL, F., HAESEBROUCK, F. and DUCATELLE, R. (2004) Colonization of the chicken reproductive tract and egg contamination by Salmonella. Journal of Applied Microbiology 97: 233-245.
DEFRA (2010) Zoonoses report United Kingdom 2008. Department for Environment Food and Rural Affairs. (London, Defra). http://www.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/zoonoses/reports.htm (accessed 23rd Aug 2010).
DOORDUYN, Y., VAN DEN BRANDHOF, W.E., VAN DUYNHOVEN, Y., WANNET, W.J.B. and VAN PELT, W. (2006) Risk factors for salmonella enteritidis and typhimurium (DT104 and non-DT104) infections in The Netherlands: predominant roles for raw eggs in enteritidis and sandboxes in typhimurium infections. Epidemiology and Infection 134: 617-626.
DYDA, A., HUNDY, R., MOFFATT, C.R.M. and CAMERON, S. (2009) Outbreak of salmonella typhimurium 44 related to egg consumption. Communicable Diseases Intelligence 33: 414-418.
EFSA (2007a) The Community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2006. EFSA Journal 130.
EFSA (2007b) Report of the task force on zoonoses data collection on the analysis of the baseline study on the prevalence of salmonella in holdings of laying hen flocks of Gallus gallus. EFSA Journal 97.
EFSA (2009a) The Community Summary report on food-borne outbreaks in the European Union in 2007. EFSA Journal 271.
EFSA (2009b) Quantitative estimation of the impact of setting a new target for the reduction of salmonella in breeding hens of Gallus gallus. EFSA Journal 1036: 1-68.
EFSA (2010a) The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and food-borne outbreaks in the European Union in 2008. EFSA Journal 8: 1496.
EFSA (2010b) Scientific Opinion on a quantitative estimate of the public health impact of setting a new target for the reduction of salmonella in laying hens. EFSA Journal 8: 1546.
FOLEY, S.L., NAYAK, R., HANNING, I.B., JOHNSON, T.J., HAN, J. and RICKE, S.C. (2011) Population dynamics of salmonella enterica serotypes in commercial egg and poultry production. Applied and Environmental Microbiology 77: 4273-4279.
FSA (2004) Report of the survey of salmonella contamination of UK produced shell eggs on retail sale. U. Food Standards Agency. http://www.food.gov.uk/science/surveillance/fsis2004branch/fsis5004eggs (accessed 11th April 2011).
GANTOIS, I., EECKHAUT, V., PASMANS, F., HAESEBROUCK, F., DUCATELLE, R. and VAN IMMERSEEL, F. (2008) A comparative study on the pathogenesis of egg contamination by different serotypes of Salmonella. Avian Pathology 37: 399-406.
GARBER, L., SMELTZER, M., FEDORKA-CRAY, P., LADELY, S. and FERRIS, K. (2003) salmonella enterica serotype enteritidis in table egg layer house environments and in mice in US layer houses and associated risk factors. Avian Diseases 47: 134-142.
GAST, R.K., GUARD-PETTER, J. and HOLT, P.S. (2002) Characteristics of salmonella enteritidis contamination in eggs after oral, aerosol, and intravenous inoculation of laying hens. Avian Diseases 46: 629-635.
GREIG, J.D. and RAVEL, A. (2009) Analysis of foodborne outbreak data reported internationally for source attribution. International Journal of Food Microbiology 130: 77-87.
GUAN, J., GRENIER, C. and BROOKS, B.W. (2006) In vitro study of salmonella enteritidis and salmonella typhimurium definitive type 104: survival in egg albumen and penetration through the vitelline membrane. Poultry Science 85: 1678-1681.
HALL, R. (2002) Outbreak of gastroenteritis due to salmonella typhimurium phage type I 35a following consumption of raw egg. Communicable Diseases Intelligence 26: 285-287.
HATAKKA, M. (1992) salmonella outbreak among railway and airline passengers. Acta Veterinaria Scandinavica 33: 253-260.
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 principal risk factor for sporadic salmonella serotype Heidelberg infections: a case-control study in FoodNet sites. Clinical Infectious Diseases 38 Suppl 3: S237-243.
HERIKSTAD, H., MOTARJEMI, Y. and TAUXE, R.V. (2002) salmonella surveillance: a global survey of public health serotyping. Epidemiology and Infection 129: 1-8.
HOGUE, A., WHITE, P., GUARD-PETTER, J., SCHLOSSER, W., GAST, R., EBEL, E., FARRAR, J., GOMEZ, T., MADDEN, J., MADISON, M., MCNAMARA, A.M., MORALES, R., PARHAM, D., SPARLING, P., SUTHERLIN, W. and SWERDLOW, D. (1997) Epidemiology and control of egg-associated salmonella enteritidis in the United States of America. Revue Scientifique et Technique de l'Office International Des Epizooties 16: 542-553.
HOOP, R.K. and POSPISCHIL, A. (1993) Bacteriological, serological, histological and immunohistochemical findings in laying hens with naturally acquired salmonella enteritidis phage type 4 infection. Veterinary Record 133: 391-393.
HPA (2011) All human isolates reported to the Health Protection Agency Centre for Infections. England and Wales, 2000-2010. UK Health Protection Agency. http://www.hpa.org.uk/Topics/InfectiousDiseases/InfectionsAZ/Salmonella/EpidemiologicalData/salmDataHuman/ (accessed February 25th 2013).
HUMPHREY, T.J., WHITEHEAD, A., GAWLER, A.H., HENLEY, A. and ROWE, B. (1991) Numbers of salmonella enteritidis in the contents of naturally contaminated hens' eggs. Epidemiology and Infection 106: 489-496.
ISSACK, M.I., HENDRIKSEN, R.S., LUN, P.L., LUTCHUN, R.K. and AARESTRUP, F.M. (2009) salmonella enterica serovar typhimurium in Mauritius linked to consumption of marlin mousse. Foodborne Pathogens and Disease 6: 739-741.
KEENE, W.E., HEDBERG, K., CIESLAK, P., SCHAFER, S. and DECHET, A. (2004) salmonella serotype typhimurium outbreak associated with commercially processed egg salad - Oregon, 2003. Morbidity and Mortality Weekly Report 53: 1132-1134.
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.
KIST, M.J. and FREITAG, S. (2000) Serovar specific risk factors and clinical features of salmonella enterica ssp. enterica serovar enteritidis: a study in South-West Germany. Epidemiology and Infection 124: 383-392.
LACONCHA, I., BAGGESEN, D.L., REMENTERIA, A. and GARAIZAR, J. (2000) Genotypic characterisation by PFGE of salmonella enterica serotype enteritidis phage types 1, 4, 6, and 8 isolated from animal and human sources in three European countries. Veterinary Microbiology 75: 155-165.
LISTER, S.A. (1988) salmonella enteritidis infection in broilers and broiler breeders. Veterinary Record 123: 350.
LITTLE, C.L., SURMAN-LEE, S., GREENWOOD, M., BOLTON, F.J., ELSON, R., MITCHELL, R.T., NICHOLS, G.N., SAGOO, S.K., THRELFALL, E.J., WARD, L.R., GILLESPIE, I.A. and O'BRIEN, S. (2007a) Public health investigations of salmonella enteritidis in catering raw shell eggs, 2002-2004. Letters in Applied Microbiology 44: 595-601.
LITTLE, C.L., WALSH, S., HUCKLESBY, L., SURMAN-LEE, S., PATHAK, K., GATTY, Y., GREENWOOD, M., DE PINNA, E., THRELFALL, E.J., MAUND, A. and CHAN, C.H. (2007b) Survey of salmonella contamination of non-United Kingdom-produced raw shell eggs on retail sale in the northwest of England and London, 2005 to 2006. Journal of Food Protection 70: 2259-2265.
LITTLE, C.L., RHOADES, J.R., HUCKLESBY, L., GREENWOOD, M., SURMAN-LEE, S., BOLTON, F.J., MELDRUM, R., WILSON, I., MCDONALD, C., DE PINNA, E., THRELFALL, E.J. and CHAN, C.H. (2008) Survey of salmonella contamination of raw shell eggs used in food service premises in the United Kingdom, 2005 through 2006. Journal of Food Protection 71: 19-26.
MARCUS, R., RABATSKY-EHR, T., MOHLE-BOETANI, J.C., FARLEY, M., MEDUS, C., SHIFERAW, B., CARTER, M., ZANSKY, S., KENNEDY, M., VAN GILDER, T. and HADLER, J.L. (2004) Dramatic decrease in the incidence of salmonella serotype enteritidis infections in 5 FoodNet sites: 1996-1999. Clinical Infectious Diseases 38 Suppl 3: S135-S141.
MASON, B.W., WILLIAMS, N., SALMON, R.L., LEWIS, A., PRICE, J., JOHNSTON, K.M. and TROTT, R.M. (2001) Outbreak of salmonella indiana associated with egg mayonnaise sandwiches at an acute NHS hospital. Communicable Disease and Public Health 4: 300-304.
MESSENS, W., GRIJSPEERDT, K. and HERMAN, L. (2005) Eggshell penetration by Salmonella: a review. World's Poultry Science Journal 61: 71-85.
MITCHELL, E., OMAHONY, M., LYNCH, D., WARD, L.R., ROWE, B., UTTLEY, A., ROGERS, T., CUNNINGHAM, D.G. and WATSON, R. (1989) Large outbreak of food poisoning caused by salmonella typhimurium definitive type 49 in mayonnaise. British Medical Journal 298: 99-101.
MIYAMOTO, T., BABA, E., TANAKA, T., SASAI, K., FUKATA, T. and ARAKAWA, A. (1997) salmonella enteritidis contamination of eggs from hens inoculated by vaginal, cloacal, and intravenous routes. Avian Diseases 41: 296-303.
MUMMA, G.A., GRIFFIN, P.M., MELTZER, M.I., BRADEN, C.R. and TAUXE, R.V. (2004) Egg quality assurance programs and egg-associated salmonella enteritidis infections, United States. Emerging Infectious Diseases 10: 1782-1789.
MURRAY, C.J. (1994) salmonella serovars and phage types in humans and animals in Australia 1987-1992. Australian Veterinary Journal 71: 78-81.
NAKAMURA, M., NAGAMINE, N., NORIMATSU, M., SUZUKI, S., OHISHI, K., KIJIMA, M., TAMURA, Y. and SATO, S. (1993) The ability of salmonella enteritidis isolated from chicks imported from England to cause transovarian infection. Journal of Veterinary Medical Science 55: 135-136.
OKAMURA, M., KAMIJIMA, Y., MIYAMOTO, T., TANI, H., SASAI, K. and BABA, E. (2001a) Differences among six salmonella serovars in abilities to colonize reproductive organs and to contaminate eggs in laying hens. Avian Diseases 45: 61-69.
OKAMURA, M., MIYAMOTO, T., KAMIJIMA, Y., TANI, H., SASAI, K. and BABA, E. (2001b) 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.
ORTEGA-BENITO, J.M. and LANGRIDGE, P. (1992) Outbreak of food poisoning due to salmonella typhimurium DT4 in mayonnaise. Public Health 106: 203-208.
OTOMO, Y., ABE, K., ODAGIRI, K., SHIROTO, A., TAKATORI, K. and HARA-KUDO, Y. (2007) Detection of salmonella in spent hens and eggs associated with foodborne infections. Avian Diseases 51: 578-583.
OZFOODNET WORKING GROUP (2002) Enhancing foodborne disease surveillance across Australia in 2001: the OzFoodNet Working Group. Communicable Diseases Intelligence 26: 375-406.
OZFOODNET WORKING GROUP (2003) Foodborne disease in Australia: incidence, notifications and outbreaks. Annual report of the OzFoodNet network, 2002. Communicable Diseases Intelligence 27: 209-243.
OZFOODNET WORKING GROUP (2006) Burden and causes of foodborne disease in Australia: Annual report of the OzFoodNet network, 2005. Communicable Diseases Intelligence 30: 278-300.
OZFOODNET WORKING GROUP (2007) Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of OzFoodNet Network, 2006. Communicable Diseases Intelligence 31: 345-365.
OZFOODNET WORKING GROUP (2008) Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of OzFoodNet Network, 2007. Communicable Diseases Intelligence 32: 400-424.
OZFOODNET WORKING GROUP (2009) Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of OzFoodNet Network, 2008. Communicable Diseases Intelligence 33: 389-413.
PADRON, M. (1990) salmonella typhimurium penetration through the eggshell of hatching eggs. Avian Diseases 34: 463-465.
POPPE, C., JOHNSON, R.P., FORSBERG, C.M. and IRWIN, R.J. (1992) salmonella enteritidis and other salmonella in laying hens and eggs from flocks with salmonella in their environment. Canadian Journal of Veterinary Research 56: 226-232.
POPPE, C., DUNCAN, C.L. and MAZZOCCO, A. (1998) salmonella contamination of hatching and table eggs: a comparison. Canadian Journal of Veterinary Research 62: 191-198.
SARNA, M., DOWSE, G., EVANS, G. and GUEST, C. (2002) An outbreak of salmonella typhimurium PTI35 gastroenteritis associated with a minimally cooked dessert containing raw eggs. Communicable Diseases Intelligence 26: 32-37.
SLINKO, V.G., MCCALL, B.J., STAFFORD, R.J., BELL, R.J., HILEY, L.A., SANDBERG, S.M., WHITE, S.A. and BELL, K.M. (2009) Outbreaks of salmonella typhimurium phage type 197 of multiple genotypes linked to an egg producer. Communicable Diseases Intelligence 33: 419-425.
STEPHENS, N., SAULT, C., FIRESTONE, S.M., LIGHTFOOT, D. and BELL, C. (2007) Large outbreaks of salmonella typhimurium phage type 135 infections associated with the consumption of products containing raw egg in Tasmania. Communicable Diseases Intelligence 31: 118-124.
STEPHENS, N., COLEMAN, D. and SHAW, K. (2008) Recurring outbreaks of salmonella typhimurium phage type 135 associated with the consumption of products containing raw egg in Tasmania. Communicable Diseases Intelligence 32: 466-468.
TAYLOR, D.N., BOPP, C., BIRKNESS, K. and COHEN, M.L. (1984) An outbreak of salmonellosis associated with a fatality in a healthy child: a large dose and severe illness. American Journal of Epidemiology 119: 907-912.
THRELFALL, E.J., FROST, J.A., WARD, L.R. and ROWE, B. (1990) Plasmid profile typing can be used to subdivide phage-type 49 of salmonella typhimurium in outbreak investigations. Epidemiology and Infection 104: 243-251.
TRIBE, I.G., COWELL, D., CAMERON, P. and CAMERON, S. (2002) An outbreak of salmonella typhimurium phage type 135 infection linked to the consumption of raw shell eggs in an aged care facility. Communicable Diseases Intelligence 26: 38-39.
VAN DE GIESSEN, A.W., AMENT, A.J. and NOTERMANS, S.H. (1994) Intervention strategies for salmonella enteritidis in poultry flocks: a basic approach. International Journal of Food Microbiology 21: 145-154.
VELGE, P., CLOECKAERT, A. and BARROW, P. (2005) Emergence of salmonella epidemics: the problems related to salmonella enterica serotype enteritidis and multiple antibiotic resistance in other major serotypes. Veterinary Research 36: 267-288.
VIEIRA, A.R. (2009) WHO Global Foodborne Infections Network Country Databank – A resource to link human and non-human sources of Salmonella. ISVEE Conference. Durban, South Africa, 10-14 August 2009. http://www.who.int/gfn/activities/CDB_poster_Sept09.pdf.
WALES, A.D. and DAVIES, R.H. (2011) A critical review of salmonella typhimurium infection in laying hens. Avian Pathology 40: 429-436.
WARD, B., ANDREWS, R., GREGORY, J. and LIGHTFOOT, D. (2002) The use of sequential studies in a salmonellosis outbreak linked to continental custard cakes. Epidemiology and Infection 129: 287-293.
WEGENER, H.C., HALD, T., LO FO WONG, D., MADSEN, M., KORSGAARD, H., BAGER, F., GERNER-SMIDT, P. and MOLBAK, K. (2003) salmonella control programs in Denmark. Emerging Infectious Diseases 9: 774-780.
WHO (2010) Global Foodborne Infections Network (GFN) Country Databank. World Health Organisation. http://thor.dfvf.dk/gss (accessed 29th June 2010).

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed