Effects of Salmonella enterica serovar Enteritidis infection on egg production and the immune response of the laying duck Anas platyrhynchos

Yu Zhang; Yang Chen; Tiantian Gu; Qi Xu; Guoqiang Zhu; Guohong Chen

doi:10.7717/peerj.6359

Effects of Salmonella enterica serovar Enteritidis infection on egg production and the immune response of the laying duck Anas platyrhynchos

PeerJ. 2019 Jan 25:7:e6359. doi: 10.7717/peerj.6359. eCollection 2019.

Authors

Yu Zhang¹, Yang Chen¹, Tiantian Gu¹, Qi Xu¹, Guoqiang Zhu², Guohong Chen¹

Affiliations

¹ Joint International Research Laboratory of Agriculture & Agri-Product Safety of the Ministry of Education, Yangzhou University, Yangzhou, China.
² College of Veterinary Medicine, Yangzhou University, Yangzhou, China.

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.

Keywords: Bacterial distribution; Duck; Immune gene; Reproductive tract; Salmonella enterica serovar enteritidis.

Associated data

figshare/10.6084/m9.figshare.6916271.v1

Grants and funding

This work was supported by the Natural Science Foundation of China (31702107) and Earmarked Fund for Modern Agro-industry Technology Research System (CARS-43-3). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.