Br J Nutr. 2017 Jan;117(1):83-92. doi: 10.1017/S0007114516004268.

Maternal short-chain fructo-oligosaccharide supplementation increases intestinal cytokine secretion, goblet cell number, butyrate concentration and Lawsonia intracellularis humoral vaccine response in weaned pigs.

Le Bourgot C1, Le Normand L1, Formal M1, Respondek F2, Blat S1, Apper E2, Ferret-Bernard S1, Le Huërou-Luron I1.
1French National Institute for Agricultural Research (INRA),UR1341 Food and Digestive, Nervous and Behavioural Adaptations (ADNC),Saint-Gilles,F-35590,France.
2Tereos,Marckolsheim,F-67390,France.

 

Abstract

Prebiotic supplementation modulates immune system development and function. However, less is known about the effects of maternal prebiotic consumption on offspring intestinal defences and immune system responsiveness. We investigated the effects of maternal short-chain fructo-oligosaccharide (scFOS) supplementation on mucin-secreting cells, ileal secretory IgA and cytokine secretion of weaned offspring and their humoral response to an oral vaccine against obligate intracellular Lawsonia intracellularis. Sows were fed a control diet (CTRL) or scFOS-supplemented diet during the last third of gestation and throughout lactation. At weaning, each litter was divided into two groups receiving a post-weaning CTRL or scFOS diet for a month. Pigs from the four groups were either non-vaccinated (n 16) or vaccinated (n 117) at day 33. Biomarkers related to intestinal defences and immune parameters were analysed 3 weeks later. SCFA production was assessed over time in suckling and weaned pigs. Maternal scFOS supplementation improved ileal cytokine secretions (interferon (IFN)-γ, P<0·05; IL-4, P=0·07) and tended to increase caecal goblet cell number (P=0·06). It increased IgA vaccine response in the serum (P<0·01) and ileal mucosa (P=0·08). Higher bacterial fermentative activity was observed during lactation (total faecal SCFA, P<0·001) and after weaning (colonic butyrate, P=0·10) in pigs from scFOS-supplemented mothers. No synergistic effect between maternal and post-weaning scFOS supplementation was observed. Therefore, maternal scFOS supplementation has long-lasting consequences by strengthening gut defences and immune response to a vaccine against an intestinal obligate intracellular pathogen. Prebiotic consumption by gestating and lactating mothers is decisive in modulating offspring intestinal immunity.

KEYWORDS:

IFN interferon; PND postnatal day; sIgA secretory IgA; scFOS short-chain fructo-oligosaccharides; Intestinal immune system; Maternal nutrition; Prebiotics; Short-chain fructo-oligosaccharides; Vaccination

PMID: 28115029

 

Supplement

Perinatal nutrition plays a decisive role in controlling gut bacterial primo-colonization and, thereby, is an important driver for the development and the maturation of intestinal immunity, particularly acquisition of mucosal immune tolerance as well as protection against pathogens. Since short-chain fructooligosaccharide (scFOS) prebiotic was known to positively modulate the microbiota composition and activity, it appeared as an interesting nutritional strategy during the perinatal life which is a critical window of development. We previously demonstrated, in a pig model, that scFOS supplementation of the maternal diet positively modulated the offspring gut microbiota and immune system maturation before weaning (Le Bourgot et al., 2014). Our recent study (Le Bourgot et al., 2017) showed that such improvement in intestinal immune system maturation induced beneficial effects on its functionality, later in life, by enhancing local defence mechanisms and responsiveness to a bacterial challenge. Interestingly, the maternal scFOS supplementation improved the immune response to a vaccine directed against the intestinal bacterium Lawsonia intracellularis, but not that to a vaccine directed against the Influenza respiratory virus (Le Bourgot et al., 2016). Yet, the direct scFOS supplementation of weaned piglets increased the response to Influenza virus challenge, but not that to Lawsonia intracellularis. No synergistic effect between maternal and post-weaning scFOS supplementation was observed for both types of vaccination. Thus, the window of nutritional exposure to scFOS (maternal versus post-weaning) conditioned the responses of the immune system.

Optimization of the maturation of intestinal immune system during the neonatal life, associated with a modulation of the intestinal microbiota by maternal scFOS supplementation, promoted the functionality of the mucosal immune system after weaning as evidenced by a local intestinal bacterial challenge. We speculate that such maternal supplementation programmed the mucosal immune system to respond appropriately to intestinal pathogens. Conversely, the direct intake of scFOS after weaning could have differently impacted the microbiota composition with different consequences on immunity. In fact, the abrupt process of weaning induces strong modifications of the composition and complexity of the intestinal microbiota and several weeks are needed to establish a stabilized bacterial balance. In this context, the consumption of prebiotic during post-weaning phase could have favoured the growth of specific bacteria species with consequences on humoral response.

Due to the complexity of the microbiota, it is difficult to pinpoint the exact bacterial determinants of the immune response to a vaccine challenge. Further studies are required to highlight the role of a specific microbiota composition to confer immuno-competence against different types of vaccination, depending on the timing of exposure to prebiotic supplementation. Our promising results confirm the role played by early prebiotic supplementation on the intestinal functionality.

 

 

Figure : Effects of scFOS supplementation on vaccine immune responses of the weaned pig.

 

References

Le Bourgot, C., Le Normand, L., Formal, M., Respondek, F., Blat, S., Apper, E., Ferret-Bernard, S., & Le Huërou-Luron, I. (2017). Maternal short-chain fructo-oligosaccharide supplementation increases intestinal cytokine secretion, goblet cell number, butyrate concentration and Lawsonia intracellularis humoral vaccine response in weaned pigs. Br. J. Nutr. 117(1):83-92.
Le Bourgot, C., Ferret-Bernard, S., Blat, S., Apper, E., & Le Huërou-Luron, I. (2016). Short-chain fructooligosaccharide supplementation during gestation and lactation or after weaning differentially impacts pig growth and IgA response to influenza vaccination. J.  Funct. Foods 24: 307-315.
Le Bourgot, C., Ferret-Bernard, S., Le Normand, L., Savary, G., Menendez-Aparicio, E., Blat, S., Apper-Bossard, E., Respondek, F., & Le Huërou-Luron, I. (2014). Maternal short-chain fructooligosaccharide supplementation influences intestinal immune system maturation in piglets. PloS one 9(9): e107508.