Abstract
Persistent colonization of the avian reproductive tract by Salmonella enterica serovar Enteritidis (SE) negatively affects egg production and contaminates the egg. The immune function of the ovary and oviduct is essential for protection from infection and for the production of wholesome eggs. However, the immune response of laying ducks during SE infection is not well-understood. In this study, ducks (Anas platyrhynchos) were infected with SE and were systematically monitored for fecal shedding during a 13-week period. We also assessed bacterial distribution in the reproductive tract and classified infected ducks as resistant or susceptible based on the presence of tissue lesions and on SE isolation from fecal samples. We found that infected animals had persistent, but intermittent, bacterial shedding that resulted in the induction of carrier ducks. Laying rate and egg quality were also decreased after SE infection (P < 0.05). SE readily colonized the stroma, small follicle, isthmus, and vagina in the reproductive tracts of susceptible ducks. Immunoglobulin (IgA, IgG, IgM) levels were higher in susceptible ducks compared with resistant birds (P < 0.05); T-lymphocyte subpopulations (CD3+, CD4+, CD8+) displayed the opposite trend. qRT-PCR analysis was used to examine expression profiles of immune response genes in the reproductive tract of infected ducks. The analysis revealed that immune genes, including toll-like receptors (TLR2, TLR4-5, TLR15, TLR21), NOD-like receptors (NOD1, NLRX1, NLRP12), avian β-defensins (AvβD4-5, AvβD7, AvβD12), cytokines (IL-6, IL-1β, IFN-γ), and MyD88 were markedly upregulated in the reproductive tracts of SE-infected ducks (all P < 0.05); TLR3, TLR7, NLRC3, NLRC5, and TNF-α were significantly downregulated. These results revealed that SE infection promoted lower egg production and quality, and altered the expression of TLRs, NLRs, AvβDs, and cytokine family genes. These findings provide a basis for further investigation of the physiological and immune mechanisms of SE infection in laying ducks.
Highlights
Food-borne salmonellosis outbreaks in humans are, in large part, caused by the consumption of contaminated poultry meat or eggs, and usually result from infection with Salmonella enterica serovar Enteritidis (SE) (Harker et al, 2014; Martelli & Davies, 2012)
These data revealed that overall, the percentage of SE(+) ducks displaying fecal shedding decreased over time; an increasing percentage of SE(+) shedding was observed during sexual maturity (20–21 week; 24–25 week) (Fig. 2, Table S1)
We focused on the additional immune factors Toll-like receptors (TLRs), NODlike receptors (NLRs), avian β-defensins (AvβDs), and cytokines, and investigated the expression of these four families of proteins in the follicle, ovary stroma, isthmus, and vagina during SE infection
Summary
Food-borne salmonellosis outbreaks in humans are, in large part, caused by the consumption of contaminated poultry meat or eggs, and usually result from infection with Salmonella enterica serovar Enteritidis (SE) (Harker et al, 2014; Martelli & Davies, 2012). SE infection frequently results in the production of contaminated eggs, and vertical transmission and serious environmental pollution frequently occur because of infection of the reproductive organs and shedding in fecal matter. SE is deposited in the yolk or albumen, or both, of developing eggs (Gantois et al, 2009), which suggests that egg contamination in any part of the reproductive tract is possible. A better understanding of SE infection in the various segments of the duck reproductive tract and how immune response dynamics contribute to the mechanism of SE invasion during egg formation is critical for the development of effective control measures
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