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

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 shell 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.

Genetic Basis of Salmonella Enteritidis Pathogenesis in Chickens

“…It is now widely accepted that the primary route of egg contamination is via deposition of SE from the infected RT directly into the internal contents of eggs prior to oviposition (Arnold et al, 2014;Gast and Holt, 2000;Keller et al, 1995;Shivaprasad et al, 1990). It is also known that the hen egg presents a hostile environment for efficient propagation of SE.…”

Scientific Opinion on the public health risks of table eggs due to deterioration and development of pathogens

“…Other serovars (such as S. Enteritidis and S. Typhimurium) are more effective at spreading from the gastrointestinal tract to other organs, causing a systemic infection (Humphrey et al, 1989a;Keller et al, 1995;Okamura et al, 2001a;Okamura et al, 2010;Shivaprasad et al, 2013). In recent studies performing comparative genome analysis, it was concluded that S. Gallinarum and S. Enteritidis are highly related and that S. Gallinarum may be a direct descendant of S. Enteritidis, which has lost part of its genome and became host adapted.…”

“…Yolk contamination points to the ovary as the site of origin of the egg contamination . A systemic spread of Salmonella infection in the hen can lead to the colonization of the ovary (Keller et al, 1995) and Salmonella (in particular S. Enteritidis) is strongly believed to interact with the cellular components of the preovulatory follicles, which lead to the production of the egg yolk. Ovary contamination with Salmonella can result in colonization of the preovulatory follicles, but not necessarily in the production of yolk-contaminated eggs.…”

“…For example, Shivaprasad and colleagues (1990) observed that challenge with S. Enteritidis PT8 resulted in egg content contamination and that albumen contamination occurred (at frequencies as high as 2.9 %) more often than that of the yolk (≤ 0.7 %). Forming eggs have been shown to have a higher contamination rate than laid ones, as the egg albumen contains antibacterial compounds that reduce the bacterial load over time (Keller et al, 1995). Salmonella cannot replicate effectively in the albumen of fresh eggs, and therefore must gain access to the yolk contents in order to multiply (Gantois et al, 2008).…”

“…Humphrey and Whitehead (1993) and Gast and Holt (2000) observed that in artificially contaminated eggs, there is about 1 log of growth of S. Enteritidis during the first 24 hours postinoculation, probably as a result of the availability of bacterial intrinsic iron reserves. This may however also be an experimental artefact due to culture medium being transferred with the bacterial inoculum and contaminated forming eggs have been shown to have a higher contamination rate than eggs after lay due to the bactericidal effect of the albumen at the body temperature of the hen ( (Keller et al, 1995). After lay, cells enter a lag phase, where, in the majority of eggs, there is little or no change in the Salmonella counts until the yolk membrane begins to deteriorate, releasing nutrient into the albumen.…”