Perinatal short‐chain fructooligosaccharides program intestinal microbiota and improve enteroinsular axis function and inflammatory status in high‐fat diet‐fed adult pigs

Abstract

Perinatal nutrition programs physiologic and metabolic functions, with consequences on the susceptibility to develop metabolic diseases in adulthood. The microbiota represents a key factor of such programming. We investigated whether perinatal prebiotic [short-chain fructooligosaccharides (scFOS)] supplementation improved adult metabolic health in association with microbiota changes in pigs used as human model. Sows were supplemented with scFOS or not during the end of gestation and the entire lactation, and offspring received scFOS accordingly during 1 mo after weaning. Pigs were then fed a standard diet for 5 mo, followed by a high-fat diet for 3 mo once adults. Perinatal scFOS supplementation induced a persistent modulation of the composition of the fecal microbiota in adulthood, notably by increasing the Prevotella genus. Meanwhile, scFOS animals displayed improved capacity to secrete glucagon-like peptide-1 and improved pancreas sensitivity to glucose without any changes in peripheral insulin sensitivity. Perinatal scFOS supplementation also increased ileal secretory IgA secretion and alkaline phosphatase activity and decreased TNF-α expression in adipose tissue. In conclusion, perinatal scFOS supplementation induced long-lasting modulation of intestinal microbiota and had beneficial consequences on the host physiology in adulthood. Our results highlight the key role of perinatal nutrition on later microbiota and host metabolic adaptation to an unbalanced diet.-Le Bourgot, C., Ferret-Bernard, S., Apper, E., Taminiau, B., Cahu, A., Le Normand, L., Respondek, F., Le Huërou-Luron, I., Blat, S. Perinatal short-chain fructooligosaccharides program intestinal microbiota and improve enteroinsular axis function and inflammatory status in high-fat diet-fed adult pigs.

Maternal Supplementation of Food Ingredient (Prebiotic) or Food Contaminant (Mycotoxin) Influences Mucosal Immune System in Piglets

“…The impact of prebiotic (CTRL- vs. PREB) was analyzed on mononuclear immune cells extracted from jej-PP at PND49 and PND90 and from il-PP at PND10, PND21, PND49 and PND90. We used immune cells from il-PP and jej-PP at PND90, as we recognized the effects of perinatal maternal scFOS on offspring immune system, long after his birth [ 8 , 10 ]. Previous studies have demonstrated that the intestinal absorption of DON takes mainly place in the jejunum directly from the intestinal lumen to the apical side of the intestinal epithelium [ 29 ].…”

“…Maternal diet supplementation with prebiotics during pregnancy improves the offspring immune defenses by supporting the structural development of the gut mucosa [ 4 , 5 , 6 , 7 ]. Herein, we selected short-chain fructooligosaccharides (scFOS), a highly interesting prebiotic fiber, since we obtained previously very interesting results after maternal and/or direct FOS supplementation on mucosal immune system development and functionality [ 5 , 8 , 9 , 10 ]. Direct dietary FOS supplementation also promotes intestinal IgA secretion [ 11 , 12 ].…”

“…However, only a few studies have reported the impact of prebiotic supplementation on the number and functionality of APC in Peyer’s patches [ 14 , 15 , 16 ]. Moreover, modification in the microbiota composition and fermentative activity was observed in the offspring when the sow diet was supplemented with prebiotics [ 5 , 8 ].…”

Physiological, antimicrobial, intestine morphological, and immunological effects of fructooligosaccharides in pigs

“…FOS can also stimulate immune responses directly, through GALT (Peshev and Van den Ende, 2014). Molecules of fructans or polysaccharides may enhance the activation of specific cells of the immune system, as macrophages, dendritic cells, lymphocytes, or neutrophils, because pathogen-associated molecular patterns (PAMPs) are bonded with toll-like receptors (TLRs), which result in immunostimulation (Liu et al, 2011). For example, a yacón (which contains FOS) treatment increased TLR-4 expression in baby mice (Delgado et al, 2012;Velez et al, 2013).…”

Le Dréan et al Neonatal consumption of oligosaccharides deeply increases L-cells density without any significant consequence on adult eating behavior

“…Indeed, in our experimental protocols, prebiotic supplementation was applied during a short postnatal period and completed before the start of solid food consumption, whereas the studies reporting programming effects of early supplementation with OS on the subsequent composition of the microbiota were based on longer-term supplements extending from the prenatal period (i.e. supplementation of gestating mothers) to complete weaning or even further [Fugiwara et al 2010;Le Bourgot et al 2019]. Whether the supplementation we applied was insufficiently early, insufficiently late or insufficiently sustained is difficult to establish on the sole basis of this comparison.…”