Abstract
Chicken eggs are the main source of human Salmonella enterica serovar Enteritidis infection. S. Enteritidis infects the oviduct and ovary of the chicken leading to infection of developing eggs. Therefore, control in poultry production is a major public health priority. Vaccination of hens has proved successful in control strategies in United Kingdom leading to a 70% drop in human cases since introduced. However, as hens reach sexual maturity they become immunosuppressed and it has been postulated this leads to increased susceptibility to Salmonella infection. In this study we define the changes to the systemic and reproductive tract-associated immune system of hens throughout sexual development by flow cytometry and histology and determine changes in susceptibility to experimental S. Enteritidis challenge in naive and vaccinated hens. Changes to both systemic and local immune systems occur in chickens at sexual development around 140 days of age. The population of several leukocyte classes drop, with the greatest fall in CD4+ lymphocyte numbers. Within the developing reproductive tract there an organised structure of lymphocytic aggregates with γδ-T lymphocytes associated with the mucosa. At point-of-lay, this organised structure disappears and only scattered lymphocytes remain. Protection against Salmonella challenge is significantly reduced in vaccinated birds at point-of-lay, coinciding with the drop in CD4+ lymphocytes. Susceptibility to reproductive tract infection by Salmonella increased in vaccinated and naïve animals at 140 and 148 days of age. We hypothesise that the drop in γδ-T lymphocytes in the tract leads to decreased innate protection of the mucosa to infection. These findings indicate that systemic and local changes to the immune system increase the susceptibility of hens to S. Enteritidis infection. The loss of protective immunity in vaccinated birds demonstrates that Salmonella control should not rely on vaccination alone, but as part of an integrated control strategy including biosecurity and improved animal welfare.
Highlights
Salmonella enterica serovar Enteritidis is the most common cause of human non-typhoidal salmonellosis in Europe and North America and is frequently associated with consumption of infected eggs
Changes in leucocyte populations at point-of-lay As birds move towards sexual maturity at 130 to 140 days of age there is a decline in T lymphocyte populations in the spleen (Fig. 1a, 1b, 1c, whereas there is no consistent change in macrophage or B lymphocyte populations (Figure 1d, 1e)
The B lymphocyte population was considerably variable from bird-to-bird and between time points though there was no discernable change in population
Summary
Salmonella enterica serovar Enteritidis is the most common cause of human non-typhoidal salmonellosis in Europe and North America and is frequently associated with consumption of infected eggs. Enteritidis is a consequence of its ability to colonise the chicken reproductive tract leading to transovarian vertical transmission to both eggs and chicks [2,3,4,5]. Tropism for the reproductive tract in S. enterica is largely confined to S. Enteritidis and the genetically similar avian-adapted serovar S. Pullorum and as such transovarian transmission is largely confined to these serovars [4,5,7]. Pullorum is characterised by a persistent systemic carrier state with reproductive tract infection occurring as part of a recrudescent infection at point-of-lay [7]. It has been postulated that immunosuppression in production hens may lead to reproductive tract infection with Salmonella carried systemically or in the gastrointestinal tract, or that Salmonella bacteria within the environment of the poultry house may utilise this immunosuppressive event as a ‘window of opportunity’ to infect hens
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