Salmonella enterica Serovar Pullorum Persists in Splenic Macrophages and in the Reproductive Tract during Persistent, Disease-Free Carriage in Chickens

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.

Antimicrobial susceptibility of Salmonella Gallinarum and Salmonella Pullorum isolated from ill poultry in Brazil

“…Many studies report an increasing resistance to β-lactams in paratyphoid Salmonella enterica and E. coli isolated from humans and animals (MARANO et al 2000;CLEMENTE et al 2013;LIEBANA et al 2013;FERREIRA et al 2014). S. Gallinarum and S. Pullorum are hostspecific biovars that invade quickly through the intestinal mucosa colonizing the internal organs, such as spleen and liver, the elected sites for bacterial survival and replication (WIGLEY et al 2001). This characteristic differentiates the typhoid biovars from the paratyphoid and other non-invasive enterobacteria.…”

“…Both biovars can persist in the host, with no signs of the disease in surviving birds or genetically resistant chickens and also survive in the environment for long periods. Thus, these bacteria are able to cause recurrent infections in flocks, even after therapy (SHIVAPRASAD 2000;WIGLEY et al 2001;LEE et al 2005).…”

Salmonella infections: immune and non-immune protection with vaccines

“…Using an infection model established by Berchieri ), Wigley and his colleagues showed that S. Pullorum persists within macrophages in the spleen (Wigley et al , 2001). However, the reason for the absence of clearance has not been fully elucidated.…”

Identification by PCR signature-tagged mutagenesis of attenuated Salmonella Pullorum mutants and corresponding genes in a chicken embryo model

“…S. Pullorum has been experimentally shown to persist in convalescent birds after infection in 2-4-day-old-chickens [7], and at the onset of the lay surge in sex hormones, it is believed to suppress T cell responsiveness [8], leading to its extensive spread to the reproductive tract, resulting in uninfected eggs, a large proportion of which will result in infected live chickens at hatch. The persistent infection is thought to result largely from a Th2-type immune response directed by the pathogen in contrast to the characteristic Th1-type response induced by S. Enteritidis [9].…”