An update on pathogenesis and control of Salmonella infections in pigs

In order to be able to come up with efficient control measures to combat Salmonella infections in pigs, for example by means of vaccination, detailed knowledge of the pathogenesis should be the starting point. Transmission of Salmonella between pigs is thought to occur mainly via the faecal–oral route. Depending on the inoculation dose and the used strain, experimental oral infection of pigs with Salmonella Typhimurium may result in clinical signs and faecal excretion of high numbers of bacteriaLoynachan and Harris, 2005 A.T. Loynachan and D.L. Harris, Dose determination for acute Salmonella infection in pigs, Appl. Environ. Microbiol. 71 (2005), pp. 2753–2755. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (5). During ingestion, Salmonella enters the tonsils in the soft palate and persists in the tonsillar crypts. The palatine tonsils are often heavily infected in pigs and should, therefore, not be underestimated as a source of Salmonella contamination during slaughter. Surprisingly little information has been gathered on how Salmonella interacts with and persists in the porcine tonsillar tissue. Persistence of Salmonella on the superficial epithelium of the tonsillar crypts has been reported (Van Parys et al., 2010). The mode of colonization of the tonsils is probably very different from the mechanism of colonization of the intestines (Boyen et al., 2006). Very recently, various genes that are expressed in the porcine tonsils during persistent infection have been identified using the in vivo expression technology (Van Parys et al., submitted). Bacteria that are swallowed and survive passage through the stomach, reach the gut. In the distal parts of the intestine, adherence to the intestinal mucosa is generally accepted to be the first step in the pathogenesis of Salmonella infections in pigs. It has recently been shown that in epithelial cells, reversible adhesion of Salmonella Typhimurium is mediated by type 1 fimbriae and irreversible adhesion (docking) is Salmonella Pathogenicity Island 1 (SPI-1) mediated (Misselwitz et al., 2011). Both type 1 fimbriae and SPI-1 have been shown to contribute to the colonization of the porcine intestinal tract. Following adhesion, Salmonella invades the intestinal epithelium. Salmonella Typhimurium can be found within the porcine enterocytes and mesenteric lymph nodes at 2 h after oral inoculation. Recently, it has been shown that the virulence genes encoded in the SPI-1 mediate this invasion step and that these genes are crucial for the colonization of the porcine gut and GALT. The rapid growth of Salmonella Typhimurium in the porcine gut and subsequent induction of pro-inflammatory responses may explain why pigs in most cases confine Salmonella Typhimurium infection to the intestines, whereas slow replication of Salmonella Choleraesuis may enable it to evade host immunity and subsequently spread beyond the intestinal boundariesPaulin et al., 2007 S.M. Paulin, A. Jagannathan, J. Campbell, T.S. Wallis and M.P. Stevens, Net replication of Salmonella enterica serovars Typhimurium and Choleraesuis in porcine intestinal mucosa and nodes is associated with their differential virulence, Infect. Immun. 75 (2007), pp. 3950–3960. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (15). The systemic part of a Salmonella Typhimurium infection in pigs is not well-documented. It is generally accepted that Salmonella can spread throughout an organism using the blood stream or the lymphatic fluids and infect internal organs, although this has not yet been studied in detail in swine. The colonization of the gut associated lymphoid tissue (GALT), spleen and liver can result in prominent systemic and local immune responses. Macrophages are the cells of interest for Salmonella to disseminate to internal organs of different host species. The bacteria replicate rapidly intracellularly and cause the systemic phase of the infection, while interfering with the antibacterial mechanisms of the macrophages and inducing cell deathWaterman and Holden, 2003 S.R. Waterman and D.W. Holden, Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system, Cell. Microbiol. 5 (2003), pp. 501–511. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (157). In pigs, non-typhoidal serotypes such as Salmonella Typhimurium, can reach liver and spleen shortly after experimental inoculation, but are cleared from these organs a few days after inoculation. At this time, the bacteria are still found in the gut, gut-associated lymph nodes and tonsils. These infections may result in long-term asymptomatic carriage of the bacterium. Since this carrier state in pigs is difficult to detect in live animals, either by bacteriological or serological methods, these pigs can bias monitoring programmes. Very few researchers have made an attempt to unravel the mechanism of the concealed, but prolonged infection in carrier pigs. Recent evidence suggests that Salmonella Typhimurium interferes with seroconversion in pigs, and that this phenomenon might be related to strain-dependent persistency capacities (Van Parys et al., 2011). Stress-induced excretion of Salmonella Typhimurium by carrier pigs transported to the slaughterhouse may cause contamination of shipping equipment and holding areas, resulting in preslaughter transmission of Salmonella to non-infected pigs. Although the mechanism of this stress-induced excretion is not known, there are some indications that catecholamines and/or cortisol may play a role. It has been shown that Salmonella Typhimurium can “sense” catecholamines and as a result increase its growth rate. It has very recently been shown that the presence of cortisol has marked effects on the intracellular fate of Salmonella Typhimurium in porcine macrophages (Verbrugghe et al., 2011). The mechanism and the bacterial factors playing a role in this phenomenon are currently under investigation.