Skip to main content Accessibility help
×
Home

Salmonella typhimurium in poultry: a review

  • M.A. DAR (a1) (a2), S.M. AHMAD (a2), S.A. BHAT (a3), R. AHMED (a2), U. URWAT (a2), P.T. MUMTAZ (a2), S.A. BHAT (a2), T.A. DAR (a1), R.A. SHAH (a2) and N.A. GANAI (a4)...

Abstract

Salmonellosis is a typical zoonotic disease that occurs frequently in poultry flocks. Many salmonella serovars have been found to be responsible for this disease. In this review besides, poultry as a carrier of Salmonella enterica serovar Typhimurium infection, various infectious routes, pathology, sources of infection are discussed as well as diagnostic measures and preventive strategies that aim at reducing the incidence of salmonellosis at the farm level. Among the different diseases occurring in poultry, those caused by the genus Salmonella is the most common, causing serious losses to the poultry industry in terms of mortality, reduced growth and loss of egg production. The diseases caused by S. enterica serovar Typhimurium have got public health significance, as well as being associated with food poisoning in humans. Salmonellosis in humans is mainly caused by S. typhimurium. The ability of this serovar to infect birds and contaminate eggs makes it a potent infection agent for humans. As S. typhimurium shows foodborne pathogenesis, it is important to comprehend how it can affect eggs and what strategies are needed to enhance control over infection.

Copyright

Corresponding author

Corresponding author: mudasirbio@gmail.com

References

Hide All
ANA, E., LEON, S. and JORG, V. (2012) The mammalian microRNA response to bacterial infections. RNA Biology 9 (6): 742-750.
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.
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.
BASTIAAN, G.M. and ALIZE, K. (2007) Role of rodents in transmission of Salmonella and Campylobacter. Journal of the Science of Food and Agriculture 87: 2774-2781.
BUCHER, O., HOLLEY, R.A., AHMED, R., TABOR, H., NADON, C., NG, L.K. and D'AOUST, J.Y. (2007) Occurrence and characterization of Salmonella from chicken nuggets, strips, and pelleted broiler feed. Journal of Food Protection 70: 2251-2258.
BUCK, D.F., 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.
CLAIRE, M., MIGUEL, M., USHASREE, S., MALVIKA, S., MAURO, G., KONRAD, U.F. and ANA, E. (2014) Functional high-throughput screening identifies the miR-15 microRNA family as cellular restriction factors for Salmonella infection. Nature Communications 5: 4718 DOI: 10.1038/ncomms5718.
CLAYTON, D.J., BOWEN, A.J., HULME, S.D., BUCKLEY, A.M., DEACON, V.L., THOMSON, N.R., BARROW, P.A., MORGAN, E., JONES, M.A., WATSON, M. and STEVENS, M.P. (2008) Analysis of the role of 13 major fimbrial subunits in colonisation of the chicken intestines by Salmonella enterica serovar Enteritidis reveals a role for a novel locus. BMC Microbiology 8: 228.
CORRY, J.E., ALLEN, V.M., HUDSON, W.R., BRESLIN, M.F. and DAVIES, R.H. (2002) Sources of Salmonella on broiler carcasses during transportation and processing: modes of contamination and methods of control. Journal of Applied Microbiology 93: 593-598.
COX, J.M. and PAVIC, A. (2010) Advances in enteropathogen control in poultry production. Journal of Applied Microbiology 108: 745-755.
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.
COX, N.A., RICHARDSON, L.J., BUHR, R.J., MUSGROVE, M.T., BERRANG, M.E. and BRIGHT, W. (2007) Bactericidal effect of several chemicals on hatching eggs inoculated with Salmonella serovar Typhimurium. Journal of Applied Poultry Research 16: 623-627.
CRAVEN, S.E., STERN, N.J., LINE, E., BAILEY, J.S., COX, N.A. and FEDORKA-CRAY, P. (2000) Determination of the incidence of Salmonella spp., Campylobacter jejuni, and Clostridium perfringens in wild birds near broiler houses by sampling intestinal droppings. Avian Diseases 44:715-720.
CRUMP, J.A., GRIFFIN, P.M. and ANGULO, F.J. (2002) Bacterial contamination of animal feed and its relationship to human foodborne illness. Clinical infection Diseases 35 (7): 859-865.
DAVIES, R.H. and WRAY, C. (1995) Mice as carriers of Salmonella Enteritidis on persistently infected poultry units. Veterinary Record 137: 337-341.
DE REU, K., GRIJSPEERDT, K., MESSENS, W., HEYNDRICKX, M., UYTTENDAELE, M., DEBEVERE, J. and HERMAN, L. (2006) Eggshell factors influencing eggshell penetration and whole egg contamination by different bacteria, including Salmonella Enteritidis. International Journal of Food Microbiology 112: 253-260.
DOYLE, M.P. and ERICKSON, M.C. (2006) Reducing the carriage of foodborne pathogens in livestock and poultry. Poultry Science 85: 960-973.
FRICKER, C.R. (1987) The isolation of salmonellas and campylobacters. Journal of Applied Bacteriology 63: 99-116.
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.
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.
GETACHEW, T. and TESFAYE, S.T. (2014) A meta-analysis of the prevalence of Salmonella in food animals in Ethiopia. BMC Microbiology 14: 270, doi: 10.1186/s12866-014-0270-y.
HAEGGBLOM, P. (1994) Monitoring and control of Salmonella in animal feed. In Report of the National Veterinary Institute (NVI) (Sweden)/World Health Organization (WHO) International Course on Salmonella control in animal production and products (S. Öijeberg-Bengtsson, ed.), Malmö, Sweden, 21-27 August 1993. WHO/CDS/VPH/ 93.126. NVI, Uppsala, Sweden, 127-137. Available at: www.sva.se (accessed on 13 July 2006).
HANNEMANN, S., GAO, B. and GALAN, J.E. (2013) Salmonella modulation of host cell gene expression promotes its intracellular growth. PLoS Pathogens 9 (10): e1003668. doi:10.1371/journal.ppat.1003668.
HASSAN, J.O. and CURTISS, R. (1997) Efficacy of a live avirulent Salmonella Typhimurium vaccine in preventing colonization and invasion of laying hens by Salmonella Typhimurium and Salmonella Enteritidis. Avian Diseases 41: 783-791.
HOWARD, Z.R., MOORE, R.W., ZABALA-DIAZ, I.B., LANDERS, K.L., BYRD, J.A., KUBENA, L.F., NISBET, D.J., BIRKHOLD, S.G. and RICKE, S.C. (2005) Ovarian laying hen follicular maturation and in vitro Salmonella internalization. Veterinary Microbiology 108: 95-100.
HPA (2010) Salmonella in humans (excluding S. Typhi; S. Paratyphi). Faecal and lower gastrointestinal tract isolates reported to the Health Protection Agency Centre for Infections. England and Wales, 1990 2009. UK Health Protection Agency. Available online at: http://www.hpa.org.uk/Topics/InfectiousDiseases/InfectionsAZ/Salmonella/EpidemiologicalData/salmDataHuman/ (accessed 29 June 2010).
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.
HURST, J.L. and WARD, W.R. (2001) Rats and mice and animal feed - a risk too far? The Veterinary Journal 162-3: 163-165.
JONES, F.T. and RICHARDSON, K.E. (2004) Salmonella in commercially manufactured feeds. Poultry Science 83: 384-391.
JORGENSEN, F., LEACH, S., WILDE, S.J., DAVIES, A., STEWART, G.S. and HUMPHREY, T. (2000) Invasiveness in chickens, stress resistance and RpoS status of wild-type Salmonella enterica subsp. enterica serovar Typhimurium definitive type 104 and serovar Enteritidis phage type 4 strains. Microbiology 146: 3227-3235.
KELLER, L.H., SCHIFFERLI, D.M., BENSON, C.E., ASLAM, S. and ECKROADE, R.J. (1997) Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella Enteritidis. Avian Diseases 41: 535-539.
KENT, T.H., FORMAL, S.B. and LABREC, E.H. (1966) Salmonella gastroenteritis in Rhesus monkeys. Archives of Pathology 82: 272-279.
KIM, T.L. and JAMES, E.C. (2007) Mechanisms of Salmonella entry into host cells. Cellular Microbiology 9: 2103-2111.
KOPANIC, R.J., SHELDON, B.W. and WRIGHT, C.G. (1994) Cockroaches as vectors of Salmonella: Laboratory and field trials . Journal of Food Protection 57: 125-132.
KUMAR, S., BALAKRISHNA, K. and BATRA, H.V. (2008) Enrichment-ELISA for detection of Salmonella typhi from food and water samples. Biomedical Environmental Sciences 21 (2): 137-143.
LEACH, S.A., WILLIAMS, A., DAVIES, A.C., WILSON, J., MARSH, P.D. and HUMPHREY, T.J. (1999) Aerosol route enhances the contamination of intact eggs and muscle of experimentally infected laying hens by Salmonella Typhimurium DT104. FEMS Microbiology Letters 171: 203-207.
LUTFUL, S.M. (2010) Avian colibacillosis and salmonellosis. A closer look at epidemiology, pathogenesis, diagnosis, control and public health concerns. International Journal of Environmental Research and Public Health 7 (1): 89-114.
MADDADI, M.S., HASSANZADEH, M., BOZOGMEHRIFARD, M. and SHOJAEI, H. (2010) Study on two inoculation routs of salmonella enteritidis in abilities to colonize in internal organs and to contaminate of eggs in broiler breeder hens. International Journal of Poultry Science 9 (3): 254-258.
MCALLISTER, J.C., STEELMAN, C.D. and SKEELES, J.K. (1994) Reservoir of the lesser worm (Coleoptera:Tenebrionidae) for Salmonella Typhimurium (Eubacteriales: Enterobacteriaceae). Journal of Medical Entomology 31: 369-372.
MESSENS, W., GRIJSPEERDT, K. and HERMAN, L.L. (2005) Eggshell penetration by Salmonella: a review. World Poultry Science Journal 61: 71-85.
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.
MOHEE, R., DRIVER, M.F. and SOBRATEE, N. (2008) Transformation of spent broiler litter from exogenous matter to compost in a sub-tropical context. Bioresource Technology 99: 128-136.
MUNIR, E.H., KHALIFA, K.A. and MOHAMMED, A.M. (2014) Status of food safety due to bacterial contaminants of poultry meat and poultry products in Khartoum State. Journal of Scientific Research & Reports 3 (14): 1897-1904.
OKAMURA, M., KAMIJIMA, Y., MIYAMOTO, T., TANI, H., SASAI, K. and BABA, E. (2001) Differences among six Salmonella serovars in abilities to colonize reproductive organs and to contaminate egg in laying hens. Avian Diseases 45: 61-69.
PANDE, V.V., DEVON, R.L., SHARMA, P., MCWHORTER, A.R. and CHOUSALKAR, K.K. (2016) Study of Salmonella Typhimurium infection in laying hens. Frontiers in Microbiology 7: 203.
PASCOPELLA, L., RAUPACH, B., GHORI, N., MONACK, D., FALKOW, S. and SMALL, P.L. (1995) Host restriction phenotypes of Salmonella typhi and Salmonella gallinarium. Infection and Immunity 63: 4329-4335.
PORWOLLIK, S., BOYD, E.F., CHOY, C., CHENG, P., FLOREA, L., PROCTOR, E. and MCCLELLAND, M. (2004) Characterization of Salmonella enterica Subspecies I Genovars by Use of Microarrays. Journal of Bacteriology 186: 5883-5898.
RABSCH, W., ANDREWS, H.L., KINGSLEY, R.A., PRAGER, R., TSCHAPE, H., ADAMS, L. and BAULMER, A. (2002) Salmonella enterica serotype Typhimurium and its host-adapted variants. Infection and Immunity 70: 2249-2255.
RANJBAR, R., NAGHONI, A., FARSHAD, S., LASHINI, H., NAJAFI, A., SADEGHIFARD, N. and MAMMINA, C. (2014) Use of TaqMan® real-time PCR for rapid detection of Salmonella enterica serovar Typhi. Acta Microbiologica et Immunologica Hungarica 61 (2): 121-130.
REFSUM, T., HEIR, E., KAPPERUD, G., VARDUND, T. and HOLSTAD, G. (2002) Molecular epidemiology of Salmonella enterica serovar Typhimurium isolates determined by pulsed-field gel electrophoresis: comparison of isolates from avian wildlife, domestic animals, and the environment in Norway. Applied and Environmental Microbiology 68: 5600-5606.
REIBER, M.A., CONNER, D.E., BILGILI, S.F. and KOTROLA, J.S. (1991) Persistence of Salmonella Enteritidis and Salmonella Typhimurium in the oviducts of hens inseminated with contaminated semen. Poultry Science 70 (Suppl. 1): 98.
RICHARD, K.G., GURAYA, R., JONES, R.D. and ANDERSON, K.E. (2014) Contamination of eggs by Salmonella Enteritidis in experimentally infected laying hens housed in conventional or enriched cages. Poultry Science 93: 728-733.
RICK, S.C. (2003) The gastrointestinal tract ecology of Salmonella Enteritidis colonization in molting hens. Poultry Science 82: 1003-1007.
RYCHLIK, I., ELSHEIMER-MATULOVA, M. and KYROVA, K. (2014) Gene expression in the chicken caecum in response to infections with non-typhoid Salmonella. Veterinary Research 45: 119.
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.
SHIVAPRASAD, H.L., TIMONEY, J.F., MORALES, S., LUCIO, B. and BAKER, R.C. (1990) Pathogenesis of Salmonella Enteritidis infection in laying hens. I. Studies on egg transmission, clinical signs, fecal shedding, and serological responses. Avian Diseases 34: 548-557.
SNOW, L.C., DAVIES, R.H., CHRISTIANSEN, K.H., CARRIQUE-MAS, J., WALES, A., O'CONNOR, J.L., COOK, A.J. and EVANS, S.E. (2007) Survey of the prevalence of Salmonella species on commercial laying farms in the United Kingdom. Veterinary Record 161: 471-476.
STERNBERG, S., BOQVIST, S., ENGSTROM, B. and HAGGBLOM, P. (2005) The effective control of hazards in Swedish poultry: the case for Sweden, in: MEAD, G.C. (Ed.) Food safety control in the poultry industry, pp. 195-215 (Woodhead Publishing, Cambridge, UK).
VANDEPLAS, S., DUBOIS, D.R., BECKERS, Y., THONART, P. and THÉWIS, A. (2010) Salmonella in chicken: current and developing strategies to reduce contamination at farm level. Journal of Food Protection 73: 774-785.
VEGAD, J.L. and KATIYAR, A.K. (2008) A Textbook of Veterinary Special Pathology. International Book Distributing Co. pp. 328-329.
WALES, A.M., BRESLIN, M. and DAVIES, R. (2006) Semiquantitative assessment of the distribution of Salmonella in the environment of caged layer flocks. Journal of Applied Microbiology 101: 309-318.
WALLACE, H.A., JUNE, G., SHERROD, P., HAMMACK, T.S. and AMAGUANA, R.M. (1999) Salmonella, in: TOMLISON, L.A. (Ed.) Food and Drug Administration bacteriological analytical manual, Hypertext source:http://vm.cfsan.fda.gov/~comm/bam5.html.
WALTMAN, W.D., HORNE, A.M. and PIRKEL, C. (1993) Influence of enrichment incubation time on the isolation of Salmonella. Avian Diseases 37: 884-887.
WILLIAMS, A., DAVIES, A.C., WILSON, J., MARSH, P.D., LEACH, S. and HUMPHREY, T.J. (1998) Contamination of the contents of intact eggs by Salmonella Typhimurium DT104. The Veterinary Record 143: 562-563.

Keywords

Salmonella typhimurium in poultry: a review

  • M.A. DAR (a1) (a2), S.M. AHMAD (a2), S.A. BHAT (a3), R. AHMED (a2), U. URWAT (a2), P.T. MUMTAZ (a2), S.A. BHAT (a2), T.A. DAR (a1), R.A. SHAH (a2) and N.A. GANAI (a4)...

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