Salmonella enterica serovar Pullorum persists in splenic macrophages and in the reproductive tract during persistent, disease-free carriage in chickens - PubMed (original) (raw)

Salmonella enterica serovar Pullorum persists in splenic macrophages and in the reproductive tract during persistent, disease-free carriage in chickens

P Wigley et al. Infect Immun. 2001 Dec.

Abstract

Salmonella enterica serovar Pullorum is worldwide a poultry pathogen of considerable economic importance, particularly in those countries with a developing poultry industry. In addition to the characteristic high mortality rates among young chicks, one of the features of Salmonella serovar Pullorum infection is that it persists for long periods in convalescent chicks in the absence of clinical disease. This can lead to colonization of the reproductive tract of chickens and at sexual maturity can result in infected progeny through transovarian transmission to eggs. The sites of Salmonella serovar Pullorum persistence in convalescent birds are not known, and the mechanisms of persistence are not understood. Here we show that Salmonella serovar Pullorum can persist in both the spleen and the reproductive tract for over 40 weeks following experimental infection in chickens. During the period of sexual maturity, Salmonella serovar Pullorum colonized both the ovary and the oviduct of hens and led to 6% of laid eggs being infected by Salmonella serovar Pullorum. The colonization of several different sites of the reproductive tract suggests that Salmonella serovar Pullorum may employ more than one mechanism of egg infection. Persistence occurred despite a strong humoral response, suggesting an intracellular site of infection. By use of a Salmonella serovar Pullorum strain containing a plasmid stably expressing green fluorescent protein, we demonstrated that the main site of carriage in the spleen is within macrophages. This raises interesting questions about the biology of Salmonella serovar Pullorum, including why there is an increase in bacterial numbers when birds become sexually mature and in particular how Salmonella serovar Pullorum avoids clearance by macrophages and whether it modulates the immune system in other ways.

PubMed Disclaimer

Figures

FIG. 1

FIG. 1

Mean anti-Salmonella serovar Pullorum IgG titers in Salmonella serovar Pullorum-infected (n = 5) and uninfected (n = 3) commercial laying hens at postmortem (± standard errors of the means). Antibody titers were determined by ELISA using killed whole Salmonella serovar Pullorum sonicate as antigen. ○, IgG titer in Salmonella serovar Pullorum-infected birds; ●, IgG titer in uninfected controls. d, day; w, week.

FIG. 2

FIG. 2

Mean viable counts (± standard errors of the means) of Salmonella serovar Pullorum 449/87(pBRD940) bacteria per gram of tissue in spleen and splenic macrophages following experimental infection of commercial laying hens. At each time point, five birds were taken for postmortem analysis. ●, total viable counts of Salmonella serovar Pullorum bacteria per gram of splenic tissue; ○, viable counts of intracellular Salmonella serovar Pullorum bacteria in splenic macrophages.

FIG. 3

FIG. 3

Confocal laser micrograph of Salmonella serovar Pullorum 449/87(pBRD940) expressing GFP within splenic macrophages counterstained with wheat germ agglutinin–Texas Red-X. Macrophages were isolated from infected birds 21 days following infection. Bar = 10 μm.

References

    1. Abshire K Z, Neidhardt F C. Analysis of proteins synthesized by Salmonella typhimurium during growth within a host macrophage. J Bacteriol. 1993;175:3734–3743. - PMC - PubMed
    1. Anonymous. Salmonella in livestock 1998. London, United Kingdom: Veterinary Laboratory Agency/Ministry of Agriculture, Fisheries and Foods; 1999.
    1. Barrow P A, Lovell M A. Experimental infection of egg-laying hens with Salmonella enteritidis phage type 4. Avian Pathol. 1991;42:194–199. - PubMed
    1. Barrow P A, Berchieri A, Jr, Al-Haddad O. The serological response of chickens infected with Salmonella gallinarum-pullorum detected by ELISA. Avian Dis. 1992;36:227–236. - PubMed
    1. Barrow P A, Huggins M B, Lovell M A. Host specificity of Salmonella infections in chickens and mice is expressed in vivo primarily at the level of the reticuloendothelial system. Infect Immun. 1994;62:4602–4610. - PMC - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources