Infection of the Reproductive Tract and Eggs with Salmonella enterica Serovar Pullorum in the Chicken Is Associated with Suppression of Cellular Immunity at Sexual Maturity

Abstract

Salmonella enterica serovar Pullorum causes persistent infections in laying hens. Splenic macrophages are the main site of persistence. At sexual maturity, numbers of bacteria increase and spread to the reproductive tract, which may result in vertical transmission to eggs or chicks. In this study we demonstrate that both male and female chickens may develop a carrier state following infection but that the increases in bacterial numbers and spread to the reproductive tract are phenomena restricted to hens, indicating that such changes are likely to be related to the onset of egg laying. The immunological responses during the carrier state and through the onset of laying in hens were determined. These indicate that chickens produce both humoral and T-cell responses to infection, but at the onset of laying both the T-cell response to Salmonella and nonspecific responses to mitogenic stimulation fall sharply in both infected and noninfected birds. The fall in T-cell responsiveness coincided with the increase in numbers of Salmonella serovar Pullorum and its spread to the reproductive tract. Three weeks after the onset of egg laying, T-cell responsiveness began to increase and bacterial numbers declined. Specific antibody levels changed little at the onset of laying but increased following the rise in bacterial numbers in a manner reminiscent of a secondary antibody response to rechallenge. These findings indicate that a nonspecific suppression of cellular responses occurs at the onset of laying and plays a major role the ability of Salmonella serovar Pullorum to infect the reproductive tract, leading to transmission to eggs. The loss of T-cell activity at the point of laying also has implications for Salmonella enterica serovar Enteritidis infection and transmission to eggs, along with its control by vaccination offering a "window of opportunity" in which infection may occur.

Live and inactivated vaccine regimens against caecal Salmonella Typhimurium colonisation in laying hens

“…Hence, a vaccine must provide enduring protection at least until after the onset of sexual maturity, a physiological age at which cell‐mediated immunity may be compromised 21. The difficulty in producing an experimental challenge colonisation of adult hens, as seen here and in other studies that have evaluated long‐term protection,17, 25 suggests that caecal colonisation by serovar Typhimurium in older hens may be naturally limited.…”

“…An 80% positive colonisation in controls at 25 weeks of age was achieved, though at subsequent ages this rate declined sharply. It was more likely that this higher control colonisation at 25 weeks was related to the reduction in cell‐mediated immunity in hens around point of lay, which has been shown to allow a resurgence of previously suppressed Salmonella infection,21 rather than to the changes in the challenge methodology. This possible mechanism and its effect with serovar Typhimurium needs to be studied more closely in chickens.…”

“…The difficulty in producing an experimental challenge colonisation of adult hens, as seen here and in other studies that have evaluated long‐term protection,17, 25 suggests that caecal colonisation by serovar Typhimurium in older hens may be naturally limited. It would appear that protection in the peri‐maturity period, with its associated relaxation of cell‐mediated immunity,21 may be the most important point in time at which a vaccine may provide a reduction in colonisation of hens throughout their entire egg production period. Although cell‐mediated immunity may be suppressed at this time,21 adequate protection at this age may require the pre‐existence of an effective humoral antibody presence in the chicken.…”

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

“…Specific antibody levels changed little at the onset of lay but increased following the rise in bacterial numbers in a manner reminiscent of a secondary antibody response to re-challenge. These findings indicate that a non-specific suppression of cellular responses occurs at the onset of lay and plays a major role in the ability of Salmonella to infect the reproductive tract, leading to transmission to eggs (Wigley et al, 2005).…”

“…Cell-mediated immunity plays a more important role than the humoral response in protection and against Salmonella infection (Van Immerseel et al, 2005). Wigley et al (2005) have demonstrated that at the onset of laying both the T-cell response to Salmonella and non-specific responses to mitogenic stimulation fall sharply in both infected and noninfected birds. The fall in T-cell responsiveness coincides with the increase in numbers of S. Gallinarum biovar Pullorum and its spread to the reproductive tract.…”