Salmonella Infantis, a Potential Human Pathogen has an Association with Table Eggs
DOI:
https://doi.org/10.3923/ijps.2013.185.191Keywords:
Factors, hen eggshell, salmonellosis, transmission routeAbstract
Food borne Salmonellosis in human is mainly caused by the consumption of contaminated eggs and other poultry products. Trans-shell route is considered the underlying phenomena leading to the production of Salmonella Infantis contaminated eggs. Salmonella Infantis comes in the top 10 human pathogenic Salmonella serovars, been isolated from human and poultry from diverse group of countries in patients linked to contaminated food. Majority of the Salmonella cases are sporadic, outbreaks occur frequently with a direct or indirect link to contaminated food especially poultry. This review has mainly highlighted the factors affecting Salmonella transmission with a special emphasis on hen eggshell quality.
References
Alakomi, H.L. and M. Saarela, 2009. Salmonella importance and current status of detection and surveillance methods. Qual. Assurance Saf. Crops Foods, 1: 142-152.
Barrow, P.A. and M.A. Lovell, 1991. Experimental infection of egg-laying hens with Salmonella enteritidis phage type 4. Avian Pathol., 20: 335-348.
Barrow, P.A., 1994. The Microflora of the Alimentary tract and Avian Pathogens: Translocation and Vertical Transmission. In: Microbiology of the Avian Egg, Board, R.G. and R. Fuller (Eds.). Chapman and Hall, London, UK., pp:117 138.
Berrang, M.E., N.A. Cox, J.F. Frank and R.J. Buhr, 1999. Bacterial penetration of the eggshell and shell membranes of the chicken hatching egg: A review. J. Appl. Poult. Res., 8: 499-504.
Berrang, M.E., J.F. Frank, R.J. Buhr, J.S. Bailey, N.A. Cox and J. Mauldin, 1998. Eggshell characteristics and penetration by Salmonella through the productive life of a broiler breeder flock. Poult. Sci., 77: 1446-1450.
Botteldoorn, N., E.V. Coillie, J. Goris, H. Werbrouck and V. Piessens et al., 2010. Limited genetic diversity and gene expression differences between egg and non-egg-related Salmonella enteritidis strains. Zoonoses Pub. Health, 57: 345-357.
Brown, W.E., R.C. Baker and H.B. Naylor, 1965. Comparative susceptibility of chicken, duck and turkey eggs to microbial invasion. J. Food Sci., 30: 886-892.
Bruce, J. and E.M. Drysdale, 1994. Trans-Shell Transmission. In: Microbiology of the Avian Egg, Board, R.G. and R. Fullar (Eds.). Chapman and Hall, London, UK., pp: 63-91.
Cogan, T.A., F. Jorgensen, H.M. Lappin-Scott, C.E. Benson, M.J. Woodward and T.J. Humphrey, 2004. Flagella and curli fimbriae are important for growth of Salmonella enteric serovars in hen eggs. Microbiology, 150: 1063-1071.
Cox, J.M., J.B. Woolcock and A.L. Sartor, 2002. The significance of Salmonella, particularly Salmonella Infantis, to the Australian egg industry. Report for the Rural Industries Research and Development Corporation Australia.
Cox, N.A., M.E. Berrang and J.A. Cason, 2000. Salmonella penetration of eggshells and proliferation in broiler hatching eggs: A review. Poult. Sci., 79: 1571-1574.
De Buck, J., F. Van Immerseel, F. Haesebrouck and R. Ducatelle, 2004. Colonization of the chicken reproductive tract and egg contamination by Salmonella. J. Applied Microbiol., 97: 233-245.
De Reu, K., K. Grijspeerdt, W. Messens, M. Heyndrickx, M. Uyttendaele, J. Debevere and L. Herman, 2006. Eggshell factors influencing eggshell penetration and whole egg contamination by different bacteria, including Salmonella enteritidis. Int. J. Food Microbiol., 112: 253-260.
De Reu, K., W. Messens, M. Heyndrickx, T.B. Rodenburg, M. Uyttendaele and L. Herman, 2008. Bacterial contamination of table eggs and the influence of housing systems. World Poult. Sci. J., 64: 5-19.
De Reu, K., K. Grijspeerdt, M. Heyndrickx, M. Uyttendaele, J. Debevere and L. Herman, 2006. Bacterial shell contamination in the egg collection chains of different housing systems for laying hens. Br. Poult. Sci., 47: 163-172.
De Vylder, J., J. Dewulf, S. van Hoorebeke, F. Pasmans, F. Haesebrouck, R. Ducatelle and F. van Immerseel, 2011. Horizontal transmission of Salmonella Enteritidis in groups of experimentally infected laying hens housed in different housing systems. Poult. Sci., 90: 1391-1396.
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 J., 269: 1-39.
Fluit, A.C., 2005. Mini review: Towards more virulent and antibiotic-resistant Salmonella? FEMS Immunol. Med. Microbiol., 43: 1-11.
Foley, S.L., R. Nayak, I.B. Hanning, T.J. Johnson, J. Han and S.C. Ricke, 2011. Population dynamics of Salmonella enterica serotypes in commercial egg and poultry production. Applied Environ. Microbiol., 77: 4273-4279.
Fonseca, E.L., O.L. Mykytczuk, M.D. Asensi, E.M.F. Reis and L.R. Ferraz et al., 2006. Clonality and antimicrobial resistance gene profiles of multidrug- resistant salmonella enterica serovar infantis isolates from four public hospitals in Rio de Janeiro, Brazil. J. Clin. Microbiol., 44: 2767-2772.
Gantois, I., R. Ducatelle, F. Pasmans, F. Haesebrouck, R. Gast, T.J. Humphrey and F. van Immerseel, 2009. Mechanisms of egg contamination by Salmonella enteritidis. FEMS Microbiol. Rev., 33: 718-738.
Gast, R.K. and C.W. Beard, 1990. Production of Salmonella enteritidis-contaminated eggs by experimentally infected hens. Avian Dis., 34: 438-446.
Gast, R.K., R. Guraya, J. Guard-Bouldin, P.S. Holt and R.W. Moore, 2007. Colonization of specific regions of the reproductive tract and deposition at different locations inside eggs by hens infected with Salmonella enteritidis or Salmonella heidelberg. Avian Dis., 51: 40-44.
Gentry, R.F. and C.L. Quarles, 1972. The measurement of bacterial contamination on egg shells. Poult. Sci., 51: 930-933.
Gillespie, I.A., S.J. OBrien, G.K. Adak, L.R. Ward and H.R. Smith, 2005. Foodborne generaloutbreaks of Salmonella Enteritidis phage type 4 infection, England and Wales, 1992-2002: Where are the risks? Epidemiol. Infect., 133: 795-801.
Graham, S.M., 2002. Salmonellosis in children in developing and developed countries and populations. Curr. Opin. Infect. Dis., 15: 507-512.
Graves, R.C. and D.W. Maclaury, 1962. The effects of temperature, vapor pressure and absolute humidity on bacterial contamination of shell eggs. Poult. Sci., 41: 1219-1225.
Gregory, D.W., 1948. Salmonella infections of turkey eggs. Poult. Sci., 27: 359-366.
Guan, J., C. Grenier and B.W. Brooks, 2006. In vitro study of Salmonella enteritidis and Salmonella typhimurium definitive type 104: Survival in egg albumen and penetration through the vitelline membrane. Poult. Sci., 85: 1678-1681.
Hara-Kudo, Y., Y. Sakakibara, H. Konuma, T. Sawada and S. Kumaga, 2001. Laying season and egg shell cracks on the growth of Salmonella Enteritidis in the egg albumen during storage. J. Food Prot., 64: 1134-1137.
Herikstad, H., Y. Motarjemi and R.V. Tauxe, 2002. Salmonella surveillance: A global survey of public health serotyping. Epidemiol. Infect., 219: 1-8.
Holt, P.S., R.H. Davies, J. Dewulf, R.K. Gast and J.K. Huwe et al., 2011. The impact of different housing systems on egg safety and quality. Poult. Sci., 90: 251-262.
Humphrey, T.J., A. Baskerville, S. Mawer, B. Rowe and S. Hopper, 1989. Salmonella enteritidis phage type 4 from the contents of intact eggs: A study involving naturally infected hens. Epidemiol. Infect., 103: 415-423.
Humphrey, T.J., A. Whitehead, A.H.L. Gawler, A. Henley and B. Rowe, 1991. Numbers of Salmonella enteritidis in the contents of naturally contaminated hens eggs. Epidemiol. Infect., 106: 489-496.
Humphrey, T.J., A. Baskerville, H. Chart, B. Rowe and A. Whitehead, 1992. Infection of laying hens with Salmonella Enteritidis PT4 by conjunctival challenge. Vet. Rec., 131: 386-388.
Humphrey, T.J., 1994. Contamination of egg shell and contents with Salmonella enteritidis: A review. Int. J. Food Microbiol., 21: 31-40.
Ibarra, J.A. and O. Steele-Mortimer, 2009. Salmonella-the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell. Microbiol., 11: 1579-1586.
Jones, D.R., M.T. Musgrove, K.E. Anderson and H.S. Thesmar, 2010. Physical quality and composition of retail shell eggs. Poult. Sci., 89: 582-587.
Jones, T.F., L.A. Ingram, P.R. Cieslak, D.J. Vugia and M. Tobin-D'Angelo et al., 2008. Salmonellosis outcomes differ substantially by serotype. J. Infect. Dis., 198: 109-114.
Keller, L.H., C.E. Benson, K. Krotec and R.J. Eckroade, 1995. Salmonella enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect. Immunity, 63: 2443-2449.
Kim, C.J., D.A. Emery, H. Rinke, K.V. Nagaraja and D.A. Halvorson, 1989. Effect of time and temperature on growth of Salmonella enteritidis in experimentally inoculated eggs. Avian Dis., 33: 735-745.
Kimura, A.C., V. Reddy, R. Marcus, P.R. Cieslak and J.C. Mohle-Boetani et al., 2004. Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype enteritidis infections in the United States: A case control study in food net sites. Clin. Infect. Dis., 38: S244-S252.
Kretzschmar-McCluskey, V., P.A. Curtis, K.E. Anderson, W.D. Berry and L.K. Derth, 2009. Influence of hen age and strain on eggshell exterior, eggshell interior with membranes, and egg contents of microflora and on Salmonella incidence during a single production cycle. J. Applied Poult. Res., 18: 665-670.
Kraft, A.A., E.H. McNally and A.W. Brant, 1958. Shell quality and bacterial infection of chicken eggs. Poult. Sci., 37: 638-644.
Lapuz, R.R., D.V. Umali, T. Suzuki, K. Shirota and H. Katoh, 2012. Comparison of the prevalence of Salmonella infection in layer hens from commercial layer farms with high and low rodent densities. Avian Dis., 56: 29-34.
Lock, J.L., J. Dolman and R. Board, 1992. Observations on the mode of bacterial infection of hens' eggs. FEMS Microbiol. Lett., 100: 71-73.
Majowicz, S.E., J. Musto, E. Scallan, F.J. Angulo and M. Kirk et al., 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis., 50: 882-889.
March, B.E., 1969. Bacterial infection of washed and unwashed eggs with reference to Salmonella. Applied Microbiol., 17: 98-101.
Marcus, S.L., J.H. Brumell, C.G. Pfeifer and B.B. Finlay, 2000. Salmonella pathogenicity islands: Big virulence in small packages. Microbes Infect., 2: 145-156.
Merino, L.A., M.C. Ronconi, M.M. Navia, J. Ruiz and J.M. Sierra et al., 2003. Analysis of the clonal relationship among clinical isolates of Salmonella enteric serovar Infantis by different typing methods. Rev. Inst. Med. Trop. Sao. Paulo., 45: 119-123.
Messens, W., K. Grijspeerdt and L. Herman, 2006. Eggshell penetration of hens eggs by Salmonella enteric serovar Enteritidis upon various storage conditions. Br. Poult. Sci., 47: 554-560.
Messens, W.I., K. Grijspeerdt and L. Herman, 2005. Eggshell characteristics and penetration by Salmonella enterica serovar Enteritidis through the production period of a layer flock. Br. Poult. Sci., 46: 694-700.
Miyamoto, T., E. Baba, T. Tanaka, K. Sasai, T. Fukata and A. Arakawa, 1997. Salmonella enteritidis contamination of eggs from hens inoculated by vaginal, cloacal and intravenous routes. Avian Dis., 41: 296-303.
Murase, T., K. Fujimoto, R. Nakayama and K. Otsuki, 2006. Multiplication and motility of Salmonella enterica serovars Enteritidis, Infantis and Mentervideo in In vitro contamination models of eggs. J. Food Prot., 69: 1012-1016.
Nascimento, V.P. and S.E. Solomon, 1991. The transfer of bacteria (Salmonella Enteritidis) across the eggshell wall of eggs classified as poor quality. Anim. Technol., 42: 157-166.
Okamura, M., Y. Kamijima, T. Miyamoto, H. Tani, K. Sasai and E. Baba, 2001. Differences among six Salmonella serovars in abilities to colonize reproductive organs and to contaminate eggs in laying hens. Avian Dis., 45: 61-69.
Pang, E., C. Tien-Lin, M. Selvaraj, J. Chang and K.J. Wang, 2011. Deletion of the aceE gene (encoding a component of pyruvate dehydrogenase) attenuates Salmonella enterica serovar Enteritidis. FEMS Immunol. Med. Microbiol., 63: 108-118.
Parry, S.M., S.R. Palmer, J. Slader, T. Humphrey and the South East Wales Infectious Disease Liaison Group, 2002. Risk factors for Salmonella food poisoning in the domestic kitchen-a case control study. Epidemiol. Infect., 129: 277-285.
Park, S.H., H.J. Kim, W.H. Cho, J.H. Kim and M.H. Oh et al., 2009. Identification of Salmonella enterica subspecies I, Salmonella enterica serovars typhimurium, enteritidis and typhi using multiplex PCR. FEMS Microbiol. Lett., 301: 137-146.
Patil, S.R., A.Y. Kshirsagar, M.V. Ghorpade and R.V. Shinde, 2012. Cellulitis due to Salmonella Infantis. Online J. Health Applied Sci., Vol. 11.
Patrick, M.E., P.M. Adcock, T.M. Gomez, S.F. Altekruse, B.H. Holland, R.V. Tauxe and D.L. Swerdlow, 2004. Salmonella Enteritidis infections, United states, 1985-1999. Emerg. Infect. Dis., 10: 1-7.
Pelkonen, S., E.L. Romppanen, A. Siitonen and J. Pelkonen, 1994. Differentiation of Salmonella serovar Infantis isolates from human and animal sources by fingerprinting IS200 and 16S rrn loci. J. Clin. Microbiol., 32: 2128-2133.
Forshell, L.P. and M. Wierup, 2006. Salmonella contamination: A significant challenge to the global marketing of animal food products. Rev. Sci. Tech. Office Int. Epizooties, 25: 541-554.
Poppe, C., R.P. Johnson, C.M. Forsberg and R.J. Irwin, 1992. Salmonella enteritidis and other Salmonella in laying hens and eggs from flocks with Salmonella in their environment. Can. J. Vet. Res., 56: 226-232.
Quarles, C.L., R.F. Gentry and G.O. Bressler, 1970. Bacterial contamination in poultry houses and its relationship to egg hatchability. Poult. Sci., 49: 60-66.
Radkowski, M., 2002. Effect of moisture and temperature on survival of Salmonella Enteritidis on shell eggs. Archiv Fur Geflugelkunde, 66: 119-123.
Reiber, M.A. and D.E. Conner, 1995. Effect of mating activity on the ability of Salmonella Enteritidis to persist in the ovary and oviduct of chickens. Avian Dis., 39: 323-327.
Roberts, J.R., 2004. Factors affecting egg internal quality and egg shell quality in laying hens. J. Poult. Sci., 41: 161-177.
Ross, I.L. and M.W. Heuzenroeder, 2008. A comparison of three molecular typing methods for the discrimination of Salmonella enterica serovar Infantis. FEMS Immunol. Med. Microbiol., 53: 375-384.
Sato, Y. and R. Kuwamoto, 1999. A case of canine Salmonellosis due to Salmonella Infantis. J. Vet. Med. Sci., 61: 71-72.
Sauter, E.A., C.F. Petersen, J.F. Parkinson and E.E. Steele, 1977. Effects of pH on eggshell penetration by Salmonellae. Poult. Sci., 56: 1754-1755.
Sauter, E.A. and C.F. Petersen, 1974. The effect of eggshell quality on penetration by various Salmonellae. Poult. Sci., 53: 2159-2162.
Schoeni, J.L., K.A. Glass, J.L. McDermott and A.C.L. Wong, 1995. Growth and penetration of Salmonella enteritidis, Salmonella heidelberg and Salmonella typhimurium in eggs. Int. J. Food Microbiol., 24: 385-396.
Shahada, F., T. Chuma, T. Tobata, K. Okamoto, M. Sueyoshi and K. Takase, 2006. Molecular epidemiology of antimicrobial resistance among Salmonella enterica serovar Infantis from poultry in Kagoshima, Japan. Int. J. Antimicrob. Agents, 28: 302-307.
Smith, H.W. and J.F. Tucker, 1980. The virulence of Salmonella strains for chickens: Their excretion by infected chickens. J. Hygiene, 84: 479-488.
Solomon, S.E., 1991. Egg and Shell Quality. Wolfe Publishing Ltd., England, Pages: 149.
Stadelman, W.J., 1994. Contaminants of Liquid Egg Products. In: Microbiology of the Avian Egg, Board, R.G. and R. Fuller (Eds.). Springer, London, UK., pp: 139-151.
Thomas, E., A. Bouma and D. Klinkenberg, 2011. A comparison of transmission characteristics of Salmonella enterica serovar Enteritidis between pair-housed and group-housed laying hens. Vet. Res., Vol. 42.
Tindall, B.J., P.A.D. Grimont, G.M. Garrity and J.P. Euzeby, 2005. Nomenclature and taxonomy of the genus Salmonella. Int. J. Syst. Evol. Microbiol., 55: 521-524.
Uzzau, S., D.J. Brown, T. Wallis, S. Rubino and G. Leori et al., 2000. Host adapted serotypes of Salmonella enterica. Epidemiol. Infect., 125: 229-255.
Vadehra, D.V., R.C. Baker and H.B. Naylor, 1970. Infection routes of bacteria into chicken eggs. J. Food Sci., 61: 61-62.
Vikari, A., 2011. Feed additives role in reducing Salmonella in poultry. World Poultry, Salmonella Special, pp: 10-11.
Walden, C.C., I.V.F. Allen and P.C. Trussell, 1956. The role of the eggshell and shell membranes in restraining the entry of microorganisms. Poult. Sci., 35: 1190-1196.
Weill, F.X. and P.A.D. Grimont, 2005. Les salmonelloses en France: Donnees 2001-2003 du Centre National de reference. http://www.invs.sante.fr/publications/2005/snmi/pdf/salmonelloses.pdf.
Williams, J.E., L.H. Dillard and G.O. Hall, 1968. The penetration patterns of Salmonella typhimurium through the outer structures of chicken eggs. Avian Dis., 12: 445-466.
Williams, J.E. and L.H. Dillard, 1973. The effect of external shell treatments on Salmonella penetration of chicken eggs. Poult. Sci., 52: 1084-1089.
Zhang, L., Z. Yan and E.T. Ryser, 2006. Comparison of the reveal test, the U.S. Food and Drug Administration culture method and selective media for recovery of Salmonella Enteritidis from commercial egg layer flock environment. J. Food Prot., 69: 2766-2769.
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