Impact of Dietary Manganese on Intestinal Barrier and Inflammatory Response in Broilers Challenged with Salmonella Typhimurium

Abstract

Growing concern for public health and food safety has prompted a special interest in developing nutritional strategies for removing waterborne and foodborne pathogens, including Salmonella. Strong links between manganese (Mn) and intestinal barrier or immune function hint that dietary Mn supplementation is likely to be a promising approach to limit the loads of pathogens in broilers. Here, we provide evidence that Salmonella Typhimurium (S. Typhimurium, 4 × 108 CFUs) challenge-induced intestinal injury along with systemic Mn redistribution in broilers. Further examining of the effect of dietary Mn treatments (a basal diet plus additional 0, 40, or 100 mg Mn/kg for corresponding to Mn-deficient, control, or Mn-surfeit diet, respectively) on intestinal barrier and inflammation status of broilers infected with S. Typhimurium revealed that birds fed the control and Mn-surfeit diets exhibited improved intestinal tight junctions and microbiota composition. Even without Salmonella infection, dietary Mn deficiency alone increased intestinal permeability by impairing intestinal tight junctions. In addition, when fed the control and Mn-surfeit diets, birds showed decreased Salmonella burdens in cecal content and spleen, with a concomitant increase in inflammatory cytokine levels in spleen. Furthermore, the dietary Mn-supplementation-mediated induction of cytokine production was probably associated with the nuclear factor kappa-B (NF-κB)/hydrogen peroxide (H2O2) pathway, as judged by the enhanced manganese superoxide dismutase activity and the increased H2O2 level in mitochondria, together with the increased mRNA level of NF-κB in spleen. Ingenuity-pathway analysis indicated that acute-phase response pathways, T helper type 1 pathway, and dendritic cell maturation were significantly activated by the dietary Mn supplementation. Our data suggest that dietary Mn supplementation could enhance intestinal barrier and splenic inflammatory response to fight against Salmonella infection in broilers.

Recent Advances in Understanding the Influence of Zinc, Copper, and Manganese on the Gastrointestinal Environment of Pigs and Poultry

“…The higher Mn group also had higher percentages of CD4+ and CD8+ T-cells in peripheral blood and modulated cytokine gene expression in spleen, caecal tonsils, and bursa of Fabricius. In another Salmonella Typhimurium broiler chicken challenge study, greater duodenal villus height, increased jejunal Lactobacillus and Bifidobacterium and decreased Salmonella and E. coli , higher tight junction gene expression and reduced gut permeability, reduced numbers of Salmonella in both caecal content and spleen, greater splenic proinflammatory gene expression and mitochondrial MnSOD activity, and activation of acute-phase response, T helper type 1, and dendritic cell maturation pathways were associated with higher Mn supplementation (basal diet + 100 mg Mn/kg) in comparison to a Mn adequate (basal diet + 40 mg Mn/kg) and/or deficient (basal diet + 0 mg Mn/kg) diets [ 64 ]. Interestingly, there were also differences in specific broiler chicken peripheral blood T and innate cell proportions following Salmonella Enteritidis vaccination between birds fed diets providing 80 mg Mn/kg via MnSO 4 supplementation alone or a 50:50 mix of MnSO 4 and Mn amino acid complex [ 65 ], again indicating the importance of Mn source(s) for the biological response.…”

Characterization of Salmonella Phage LPST153 That Effectively Targets Most Prevalent Salmonella Serovars

“…The most prevalent Salmonella serovars are including S. Typhimurium, S. Enteritidis, S . Pullorum and S. Gallinarum, among them, S. Typhimurium and S. Enteritidis have been described as worldwide spread [ 1 , 2 , 3 ]. Some of these prevalent serovars could lead to serious zoonotic diseases [ 4 ].…”

Copper/Zinc-Modified Palygorskite Protects Against Salmonella Typhimurium Infection and Modulates the Intestinal Microbiota in Chickens

“…Tight junction proteins (e.g., claudin-1, occludin, and ZO-1) are crucial molecules for the maintenance of intestinal epithelial barrier integrity ( Pei et al, 2019 ; Konieczka et al, 2020 ). Previous studies reported that S. Typhimurium could disrupt the tight junction structure in broilers and T84 intestinal epithelial cells ( Zhang H. et al, 2020 ). Our results showed that the expression levels of tight junction proteins were significantly downregulated with S. Typhimurium challenge relative to the CON group, which was consistent with previous reports ( Zhang H. et al, 2020 ).…”

“…A large body of evidence suggests that Salmonella challenge decreases productivity and increases the Salmonella colonization of organs ( Symonds et al, 2012 ; Zhang H. et al, 2020 ). In our study, compared with the uninfected control (CON) group, the body weight of chickens infected with Salmonella was significantly decreased, and the S. Typhimurium load was dramatically increased in the feces and organs, which was consistent with a previous report ( Zhang H. et al, 2020 ).…”

“…A large body of evidence suggests that Salmonella challenge decreases productivity and increases the Salmonella colonization of organs ( Symonds et al, 2012 ; Zhang H. et al, 2020 ). In our study, compared with the uninfected control (CON) group, the body weight of chickens infected with Salmonella was significantly decreased, and the S. Typhimurium load was dramatically increased in the feces and organs, which was consistent with a previous report ( Zhang H. et al, 2020 ). However, compared with the group infected with Salmonella (SAL), Cu/Zn-Pal-1 supplementation in the CZPS group enhanced weight gain in the infected chickens and significantly attenuated the S. Typhimurium load in feces and tissues.…”