Some putative prebiotics increase the severity of Salmonella entericaserovar Typhimurium infection in mice

Abstract

BackgroundPrebiotics are non-digestible food ingredients believed to beneficially affect host health by selectively stimulating the growth of the beneficial bacteria residing in the gut. Such beneficial bacteria have been reported to protect against pathogenic infections. However, contradicting results on prevention of Salmonella infections with prebiotics have been published. The aim of the present study was to examine whether S. Typhimurium SL1344 infection in mice could be prevented by administration of dietary carbohydrates with different structures and digestibility profiles. BALB/c mice were fed a diet containing 10% of either of the following carbohydrates: inulin, fructo-oligosaccharide, xylo-oligosaccharide, galacto-oligosaccharide, apple pectin, polydextrose or beta-glucan for three weeks prior to oral Salmonella challenge (107 CFU) and compared to mice fed a cornstarch-based control diet.ResultsThe mice fed with diets containing fructo-oligosaccharide (FOS) or xylo-oligosaccharide (XOS) had significantly higher (P < 0.01 and P < 0.05) numbers of S. Typhimurium SL1344 in liver, spleen and mesenteric lymph nodes when compared to the mice fed with the cornstarch-based control diet. Significantly increased amounts (P < 0.01) of Salmonella were detected in ileal and fecal contents of mice fed with diets supplemented with apple pectin, however these mice did not show significantly higher numbers of S. Typhimyrium in liver, spleen and lymph nodes than animals from the control group (P < 0.20).The acute-phase protein haptoglobin was a good marker for translocation of S. Typhimurium in mice. In accordance with the increased counts of Salmonella in the organs, serum concentrations of haptoglobin were significantly increased in the mice fed with FOS or XOS (P < 0.001). Caecum weight was increased in the mice fed with FOS (P < 0.01), XOS (P < 0.01), or polydextrose (P < 0.001), and caecal pH was reduced in the mice fed with polydextrose (P < 0.001). In vitro fermentation in monocultures revealed that S. Typhimurium SL1344 is capable of fermenting FOS, beta-glucan and GOS with a corresponding decline in pH.ConclusionSupplementing a cornstarch-based rodent diet with 10% FOS or XOS was found to increase the translocation of S. Typhimurium SL1344 to internal organs in mice, while 10% apple pectin was found to increase the numbers of S. Typhimurium in intestinal content and feces.

Bifidogenic effect of whole-grain wheat during a 12-week energy-restricted dietary intervention in postmenopausal women

“…One example of this is a study showing that an increase in Bifidobacterium in ob/ob mice due to prebiotic treatment resulted in a decrease in gut permeability. 32 However, several studies [15][16][17][18]33,34 also observe increased Salmonella translocation and/or infection in rodents in vivo following intake of bifidogenic oligosaccharides, which could be caused by a reduction in epithelial integrity in the gut, as shown by Ten Bruggencate et al 17 We speculate that any negative correlation between Bifidobacterium and TER may be connected to metabolic cross-feeding between different bacterial groups, resulting in changed abundances of other bacteria that may influence TER. Such effects will not be revealed in in vitro fermentation models based on bifidobacterial monocultures.…”

Carbohydrates and the human gut microbiota

“…A recent study comparing the gut microbiome of adults from different continents (Africa, North and South America) confirmed large variations among Americans, Europeans and Africans. Prebiotics are generally recognized to enhance the barrier effect of the gut microbiota toward enteropathogens, but few studies with animal models have shown that prebiotics, especially inulin and FOSs, could promote Salmonella growth, translocation or virulence [40][41][42][43]. Carbohydrates in the diet could, therefore, contribute to the large variation observed for gut microbiota composition [1 && ].…”

Enteric pathogen exploitation of the microbiota-generated nutrient environment of the gut

“…However, prebiotic supplementation with nutrients thought to promote in vivo growth of Bifidobacteria and Lactobacilli did not inhibit S . Typhimurium colonization in vivo , but instead increased pathogen colonization when compared to mice fed a standard diet [10]. These studies indicate that identification of beneficial microbiota communities, and the nutrients that shape their composition, may be incomplete or not specific enough.…”