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. 1995 Jul;63(7):2443–2449. doi: 10.1128/iai.63.7.2443-2449.1995

Salmonella enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens.

L H Keller 1, C E Benson 1, K Krotec 1, R J Eckroade 1
PMCID: PMC173326  PMID: 7790055

Abstract

Salmonella enteritidis colonizes the tissues of the chicken ovary and oviduct, presumably contaminating eggs and thereby contributing to human outbreaks of salmonellosis. In this study, commercial adult laying hens were given an oral inoculation of 10(8) S. enteritidis organisms. Tissues from various organs, the intestines, and the reproductive tract, including freshly laid eggs, were collected daily for up to 40 days postinoculation (p.i.). Within 2 days p.i. S. enteritidis was detected by culture in pools of the spleen, liver, heart, and gallbladder tissues, in intestinal tissues of all infected birds, and in various sections of the ovary and oviduct. Detection of organisms by immunohistochemical staining was rare for most tissues in spite of their culture-positive status, suggesting a low level of tissue colonization. However, S. enteritidis could be detected by immunohistochemical staining in oviduct tissues associated with four forming eggs, indicating the possibility of a heavier colonization in the egg during its development. In two subsequent experiments, forming eggs taken from the oviduct with their associated tissue, were found to be culture positive for S. enteritidis at a rate of 27.1 and 31.4%, while freshly laid eggs in these experiments were culture positive at the rate of 0 and 0.6%. These observations suggest that while forming eggs are significantly colonized in the reproductive tract, factors within the eggs may control the pathogen before the eggs are laid. The data show that prior to egg deposition, forming eggs are subject to descending infections from colonized ovarian tissue, ascending infections from colonized vaginal and cloacal tissues, and lateral infections from colonized upper oviduct tissues. The data are consistent with an ascending infection of freshly laid eggs from the cloaca, as the incidence of positive eggs in experiments 1 and 3 coincided with heavily contaminated cloacal tissues (50.7 and 80%, respectively), while no positive eggs were detected in experiment 2 when cloacal colonization was low (8.3%). The data do not support the possibility of egg invasion by bacterial translocation from the peritoneal cavity.

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Selected References

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  1. Fuller R., Jayne-Williams D. J. The origin of bacteria recovered from the peritoneum and yolk sac of healthy chickens. Br Poult Sci. 1968 Apr;9(2):159–163. doi: 10.1080/00071666808415705. [DOI] [PubMed] [Google Scholar]
  2. Gast R. K., Beard C. W. Isolation of Salmonella enteritidis from internal organs of experimentally infected hens. Avian Dis. 1990 Oct-Dec;34(4):991–993. [PubMed] [Google Scholar]
  3. Gast R. K., Beard C. W. Production of Salmonella enteritidis-contaminated eggs by experimentally infected hens. Avian Dis. 1990 Apr-Jun;34(2):438–446. [PubMed] [Google Scholar]
  4. Hedberg C. W., White K. E., Johnson J. A., Edmonson L. M., Soler J. T., Korlath J. A., Theurer L. S., MacDonald K. L., Osterholm M. T. An outbreak of Salmonella enteritidis infection at a fast-food restaurant: implications for foodhandler-associated transmission. J Infect Dis. 1991 Dec;164(6):1135–1140. doi: 10.1093/infdis/164.6.1135. [DOI] [PubMed] [Google Scholar]
  5. Humphrey T. J., Baskerville A., Chart H., Rowe B. Infection of egg-laying hens with Salmonella enteritidis PT4 by oral inoculation. Vet Rec. 1989 Nov 18;125(21):531–532. doi: 10.1136/vr.125.21.531. [DOI] [PubMed] [Google Scholar]
  6. Humphrey T. J., Chart H., Baskerville A., Rowe B. The influence of age on the response of SPF hens to infection with Salmonella enteritidis PT4. Epidemiol Infect. 1991 Feb;106(1):33–43. doi: 10.1017/s0950268800056429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Humphrey T. J., Whitehead A., Gawler A. H., Henley A., Rowe B. Numbers of Salmonella enteritidis in the contents of naturally contaminated hens' eggs. Epidemiol Infect. 1991 Jun;106(3):489–496. doi: 10.1017/s0950268800067546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Keller L. H., Benson C. E., Garcia V., Nocks E., Battenfelder P., Eckroade R. J. Monoclonal antibody-based detection system for Salmonella enteritidis. Avian Dis. 1993 Apr-Jun;37(2):501–507. [PubMed] [Google Scholar]
  9. Kim C. J., Emery D. A., Rinke H., Nagaraja K. V., Halvorson D. A. Effect of time and temperature on growth of Salmonella enteritidis in experimentally inoculated eggs. Avian Dis. 1989 Oct-Dec;33(4):735–742. [PubMed] [Google Scholar]
  10. Lindell K. A., Saeed A. M., McCabe G. P. Evaluation of resistance of four strains of commercial laying hens to experimental infection with Salmonella enteritidis phage type eight. Poult Sci. 1994 Jun;73(6):757–762. doi: 10.3382/ps.0730757. [DOI] [PubMed] [Google Scholar]
  11. Petter J. G. Detection of two smooth colony phenotypes in a Salmonella enteritidis isolate which vary in their ability to contaminate eggs. Appl Environ Microbiol. 1993 Sep;59(9):2884–2890. doi: 10.1128/aem.59.9.2884-2890.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Popiel I., Turnbull P. C. Passage of Salmonella enteritidis and Salmonella thompson through chick ileocecal mucosa. Infect Immun. 1985 Mar;47(3):786–792. doi: 10.1128/iai.47.3.786-792.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ryter A. Contribution of electron microscopy in the study of the interactions between pathogenic bacteria and their host cells. J Struct Biol. 1990 Jul-Sep;104(1-3):163–168. doi: 10.1016/1047-8477(90)90072-k. [DOI] [PubMed] [Google Scholar]
  14. Shivaprasad H. L., Timoney J. F., Morales S., Lucio B., Baker R. C. Pathogenesis of Salmonella enteritidis infection in laying chickens. I. Studies on egg transmission, clinical signs, fecal shedding, and serologic responses. Avian Dis. 1990 Jul-Sep;34(3):548–557. [PubMed] [Google Scholar]
  15. Snoeyenbos G. H., Smyser C. F., Van Roekel H. Salmonella infections of the ovary and peritoneum of chickens. Avian Dis. 1969 Aug;13(3):668–670. [PubMed] [Google Scholar]
  16. St Louis M. E., Morse D. L., Potter M. E., DeMelfi T. M., Guzewich J. J., Tauxe R. V., Blake P. A. The emergence of grade A eggs as a major source of Salmonella enteritidis infections. New implications for the control of salmonellosis. JAMA. 1988 Apr 8;259(14):2103–2107. [PubMed] [Google Scholar]
  17. Stephenson P., Satchell F. B., Allen G., Andrews W. H. Recovery of Salmonella from shell eggs. J Assoc Off Anal Chem. 1991 Sep-Oct;74(5):821–826. [PubMed] [Google Scholar]
  18. Turnbull P. C., Richmond J. E. A model of salmonella enteritis: the behaviour of Salmonella enteritidis in chick intestine studies by light and electron microscopy. Br J Exp Pathol. 1978 Feb;59(1):64–75. [PMC free article] [PubMed] [Google Scholar]
  19. Turnbull P. C., Snoeyenbos G. H. Experimental salmonellosis in the chicken. 1. Fate and host response in alimentary canal, liver, and spleen. Avian Dis. 1974 Apr-Jun;18(2):153–177. [PubMed] [Google Scholar]

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