Richard K. Gast
United States Department of Agriculture, Agricultural Research Service, Egg Safety and Quality Research Unit, Russell Research Center, 950 College Station Road, Athens, Georgia 30605, USA
Rupa Guraya
United States Department of Agriculture, Agricultural Research Service, Egg Safety and Quality Research Unit, Russell Research Center, 950 College Station Road, Athens, Georgia 30605, USA
Jean Guard
United States Department of Agriculture, Agricultural Research Service, Egg Safety and Quality Research Unit, Russell Research Center, 950 College Station Road, Athens, Georgia 30605, USA
Peter S. Holt
United States Department of Agriculture, Agricultural Research Service, Egg Safety and Quality Research Unit, Russell Research Center, 950 College Station Road, Athens, Georgia 30605, USA
ABSTRACT
Contaminated eggs produced by infected laying hens continue to pose a significant public health concern as a leading source of transmission of Salmonella enteritidis infections to humans. A recently implemented national regulatory program for egg-producing poultry in the United States seeks to control egg-borne transmission of illness to consumers via a diverse program of mandatory risk reduction practices plus testing to detect infected flocks. However, many aspects of S. enteritidis infections in laying hens, including the precise relationship between the magnitude of oral exposure and infection parameters such as the numbers of bacteria that reach internal tissues, remain unresolved. In the present study, groups of laying hens were experimentally infected with oral doses of 104, 106, or 108 CFU of a phage type 13a strain of S. enteritidis and the number of S. enteritidis cells in the livers of infected hens was determined at 5 d and 20 d post-inoculation. The frequency of S. enteritidis recovery from livers ranged from 30% (104 CFU dose) to 90% (108 CFU dose) at 5d post-inoculation and from 0% (104 CFU dose) to 40% (108 CFU dose) at 20 d post-inoculation. Significantly (p<0.05) greater numbers of S. enteritidis were isolated from livers at both 5 d and 20 d post-inoculation following inoculation with 108 CFU than after administration of either of the two lower doses. These results demonstrate that the oral exposure dose significantly affects important parameters of S. enteritidis infection in laying hens and could thereby influence the outcome of testing efforts. Interpreting the potential implications of testing results and improving the effectiveness of testing protocols are both contingent on understanding how different levels of exposure are likely to be detected by particular sampling methods
PDF References
How to cite this article
Richard K. Gast, Rupa Guraya, Jean Guard and Peter S. Holt, 2011. Frequency and Magnitude of Internal Organ Colonization Following Exposure of Laying Hens to Different Oral Doses of Salmonella enteritidis. International Journal of Poultry Science, 10: 325-331.
DOI: 10.3923/ijps.2011.325.331
URL: https://scialert.net/abstract/?doi=ijps.2011.325.331
DOI: 10.3923/ijps.2011.325.331
URL: https://scialert.net/abstract/?doi=ijps.2011.325.331
REFERENCES
- Beaumont, C., H. Chapuis, J. Protais, N. Sellier, P. Menanteau, P. Fravalo and P. Velge, 2009. Resistance to Salmonella carrier state: Selection may be efficient but response depends on animali's age. Genet. Res. Camb., 91: 161-169.
PubMed - 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.
CrossRef - Braden, C.R., 2006. Salmonella enterica serotype Enteritidis and eggs: A national epidemic in the United States. Clin. Infect. Dis., 43: 512-517.
CrossRefPubMedDirect Link - Carrique-Mas, J.J., M. Breslin, L. Snow, I. McLaren, A.R. Sayers and R.H. Davies, 2009. Persistence and clearance of different Salmonella serovars in buildings housing laying hens. Epidemiol. Infect., 137: 837-846.
CrossRef - De Buck, J., F. Pasmans, F. van Immerseel, F. Haesebrouck and R. Ducatelle, 2004. Tubular glands of the isthmus are the predominant colonization site of Salmonella enteritidis in the upper oviduct of laying hens. Poult. Sci., 83: 352-358.
PubMed - Ebel, E. and W. Schlosser, 2000. Estimating the annual fraction of eggs contaminated with Salmonella enteritidis in the United States. Int. J. Food Microbiol., 61: 51-62.
CrossRef - 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.
CrossRefPubMedDirect Link - Gantois, I., R. Ducatelle, F. Pasmans, F. Haesebrouck and F. van Immerseel, 2008. Salmonella enterica serovar enteritidis genes induced during oviduct colonization and egg contamination in laying hens. Applied Environ. Microbiol., 74: 6616-6622.
PubMedDirect Link - Gast, R.K., 1993. Detection of Salmonella enteritidis in experimentally infected laying hens by culturing pools of egg contents. Poult. Sci., 72: 267-274.
PubMed - Gast, R.K., 2007. Serotype-specific and serotype-independent strategies for preharvest control of food-borne Salmonella in poultry. Avian Dis., 51: 817-828.
Direct Link - Gast, R.K. and C.W. Beard, 1990. Serological detection of experimental Salmonella enteritidis infections in laying hens. Avian Dis., 34: 721-728.
PubMed - Gast, R.K. and C.W. Beard, 1990. Production of Salmonella enteritidis-contaminated eggs by experimentally infected hens. Avian Dis., 34: 438-446.
CrossRefDirect Link - Gast, R.K. and C.W. Beard, 1990. Isolation of Salmonella enteritidis from internal organs of experimentally infected hens. Avian Dis., 34: 991-993.
Direct Link - Gast, R.K. and S.T. Benson, 1996. Intestinal colonization and organ invasion in chicks experimentally infected with Salmonella enteritidis phage type 4 and other phage types isolated from poultry in the United States. Avian Dis., 40: 853-857.
PubMed - Gast, R.K., J. Guard-Bouldin, R. Guraya and P.S. Holt, 2009. Effect of prior passage through laying hens on invasion of reproductive organs by Salmonella enteritidis. Int. J. Poult. Sci., 8: 116-121.
CrossRefDirect Link - Gast, R.K., J. Guard-Bouldin and P.S. Holt, 2004. Colonization of reproductive organs and internal contamination of eggs after experimental infection of laying hens with Salmonella heidelberg and Salmonella enteritidis. Avian Dis., 48: 863-869.
Direct Link - Gast, R.K., J. Guard-Bouldin and P.S. Holt, 2005. The relationship between the duration of fecal shedding and the production of contaminated eggs by laying hens infected with strains of Salmonella enteritidis and Salmonella heidelberg. Avian Dis., 49: 382-386.
Direct Link - Gast, R.K., J. Guard-Petter and P.S. Holt, 2002. Characteristics of Salmonella enteritidis contamination in eggs after oral, aerosol and intravenous inoculation of laying hens. Avian Dis., 46: 629-635.
Direct Link - Gast, R.K., M.S. Nasir, M.E. Jolley, P.S. Holt and H.D. Stone, 2002. Detection of experimental Salmonella enteritidis and S. typhimurium infections in laying hens by fluorescence polarization assay for egg yolk antibodies. Poult. Sci., 81: 1128-1131.
Direct Link - Gast, R.K., J. Guard-Petter and P.S. Holt, 2003. Effect of prior serial in vivo passage on the frequency of Salmonella enteritidis contamination in eggs from experimentally infected laying hens. Avian Dis., 47: 633-639.
Direct Link - 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.
Direct Link - Gast, R.K. and P.S. Holt, 1999. Experimental horizontal transmission of Salmonella enteritidis strains (phage types 4, 8 and 13a) in chicks. Avian Dis., 43: 774-778.
PubMed - Gast, R.K. and P.S. Holt, 2000. Deposition of phage type 4 and 13a Salmonella enteritidis strains in the yolk and albumen of eggs laid by experimentally infected hens. Avian Dis., 44: 706-710.
PubMed - Gast, R.K. and P.S. Holt, 2001. Assessing the frequency and consequences of Salmonella enteritidis deposition on the egg yolk membrane. Poult. Sci., 80: 997-1002.
Direct Link - Gast, R.K. and P.S. Holt, 2001. The relationship between the magnitude of the specific antibody response to experimental Salmonella enteritidis infection in laying hens and their production of contaminated eggs. Avian Dis., 45: 425-431.
PubMed - Gast, R.K., R.E. Porter Jr. and P.S. Holt, 1997. Assessing the sensitivity of egg yolk antibody testing for detecting Salmonella enteritidis infections in laying hens. Poult. Sci., 76: 798-801.
PubMed - Greig, J.D. and A. Ravel, 2009. Analysis of foodborne outbreak data reported internationally for source attribution. Int. J. Food Microbiol., 130: 77-87.
CrossRefPubMedDirect Link - Guard, J., R.K. Gast and R. Guraya, 2010. Colonization of avian reproductive-tract tissues by variant subpopulations of Salmonella enteritidis. Avian Dis., 54: 857-861.
CrossRef - Guard-Bouldin, J., R.K. Gast, T.J. Humphrey, D.J. Henzler, C. Morales and K. Coles, 2004. Subpopulation characteristics of egg-contaminating Salmonella enterica serovar enteritidis as defined by the lipopolysaccharide O chain. Applied Environ. Microbiol., 70: 2756-2763.
Direct Link - Guard-Petter, J., 1998. Variants of smooth Salmonella enterica serovar enteritidis that grow to higher cell density than the wild type are more virulent. Applied Environ. Microbiol., 64: 2166-2172.
Direct Link - Guard-Petter, J., 2001. The chicken, the egg and Salmonella enteritidis. Environ. Microbiol., 3: 421-430.
PubMed - Humphrey, T.J., A. Baskerville, H. Chart, B. Rowe and A. Whitehead, 1991. Salmonella enteritidis PT4 infection in specific pathogen free hens: Influence of infecting dose. Vet. Rec., 1: 482-485.
Direct Link - 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.
CrossRefPubMedDirect Link - 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.
Direct Link - Keller, L.H., D.M. Schifferli, C.E. Benson, S. Aslam and R.J. Eckroade, 1997. Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella enteritidis. Avian Dis., 41: 535-539.
Direct Link - McDermid, A.S., A.S. McKee, A.B. Dowsett and P.D. Marsh, 1996. The effect of environmental pH on the physiology and surface structures of Salmonella serotype Enteritidis phage type 4. J. Med. Microbiol., 45: 452-458.
CrossRefDirect Link - Methner, U., S. Al-Shabibi and H. Meyer, 1995. Experimental oral infection of specific pathogen-free laying hens and cocks with Salmonella enteritidis strains. J. Vet. Med. B, 42: 459-469.
PubMed - Morales, C.A., M. Musgrove, T.J. Humphrey, C. Cates, R. Gast and J. Guard-Bouldin, 2007. Pathotyping of Salmonella enterica by analysis of single-nucleotide polymorphisms in cyaA and flanking 23S ribosomal sequences. Environ. Microbiol., 9: 1047-1059.
PubMed - Mumma, G.A., P.M. Griffin, M.I. Meltzer, C.R. Braden and R.V. Tauxe, 2004. Egg quality assurance programs and egg-associated Salmonella enteritidis infections, United States. Emerg. Infect. Dis., 10: 1782-1789.
PubMed - Nakamura, M., N. Nagamine, T. Takahashi, S. Suzuki, M. Kijima, Y. Tamura and S. Sato, 1994. Horizontal transmission of Salmonella enteritidis and effect of stress on shedding in laying hens. Avian Dis., 38: 282-288.
CrossRefPubMedDirect Link - Okamura, M., M. Sonobe, S. Obara, T. Kubo and T. Nagai et al., 2010. Potential egg contamination by Salmonella enterica serovar typhimurium definitive type 104 following experimental infection of pullets at the onset of lay. Poult. Sci., 89: 1629-1634.
PubMed - Poirier, E., L. Watier, E. Espie, F.X. Weill, H. De Valk and J.C. Desenclos, 2008. Evaluation of the impact on human salmonellosis of control measures targeted to Salmonella enteritidis and Typhimurium in poultry breeding using time-series analysis and intervention models in France. Epidemiol. Infect., 136: 1217-1224.
PubMed - Snow, L.C., R.H. Davies, K.H. Christiansen, J.J. Carrique-Mas, A.J.C. Cook and S.J. Evans, 2010. Investigation of risk factors for Salmonella on commercial egg-laying farms in Great Britain, 2004-2005. Vet. Rec., 166: 579-586.
CrossRefPubMedDirect Link - Thomas, M.E., D. Klinkenberg, G. Ejeta, F. van Knapen, A.A. Bergwerff, J.A. Stegeman and A. Bouma, 2009. Quantification of horizontal transmission of Salmonella enterica serovar enteritidis bacteria in pair-housed groups of laying hens. Applied Environ. Microbiol., 75: 6361-6366.
CrossRef - U.S. Food and Drug Administration, 2009. Prevention of Salmonella enteritidis in shell eggs during production, storage and transportation: Final rule. Fed. Reg., 74: 33039-33101.
Direct Link - Van Immerseel, F., 2010. Stress-induced survival strategies enable Salmonella enteritidis to persistently colonize the chicken oviduct tissue and cope with antimicrobial factors in egg white: A hypothesis to explain a pandemic. Gut Pathogens, 2: 23-23.
CrossRef - Waltman, W.D. and R.K. Gast, 2008. Salmonellosis. In: A Laboratory Manual for the Isolation and Identification of Avian Pathogens, Dufour-Zavala, L., D.E. Swayne, J.R. Glisson, J.E. Pearson, W.M. Reed, M.W. Jackwood and P.R. Woolcock (Eds.). 5th Edn., American Association of Avian Pathologists, Athens, GA., USA., pp: 3-9.
- Walker, S.L., M. Sojka, M. Dibb-Fuller and M.J. Woodward, 1999. Effect of pH, temperature and surface contact on the elaboration of fimbriae and flagella by Salmonella serotype Enteritidis. J. Med. Microbiol., 48: 253-261.
CrossRefDirect Link - Schroeder, C.M., A.L. Naugle, W.D. Schlosser, A.T. Hogue and F.J. Angulo et al., 2005. Estimate of illnesses from Salmonella enteritidis in eggs, United States, 2000. Emerg. Infect. Dis., 11: 113-115.
PubMed