Interplay between grain digestion and fibre in relation to gastro-small-intestinal passage rate and feed intake in a pig model: physiological manipulation of satiety

Abstract

Whole grain foods with a low digestibility are considered healthy in human nutrition. This includes effects of passage rate or transit time in the gastrointestinal tract (GIT) combined with intrinsic grain digestibility. Fibre is considered to affect the passage rate, and may affect passage rates differently when combined with grains of low and high digestibility. Undigested nutrients from partially digested grains reaching the ileum, the last section of the small intestine (SI), may trigger the ileal brake, and fibre fermentation in the large intestine (LI) triggers the colonic brake. Both ileal and colonic brakes act through secretion of gut peptides, and decrease gastric emptying rate and intestinal passage rate. Thus, a faster passage rate may result from grains with high digestibility and low fibre. Physiologically, fibre affects gastric emptying rate and intestinal passage rate by increasing bulk and water retention of the digesta. Establishing the effects of grain digestibility on the passage rate as influenced by fibre is a novel approach to mechanistically understand digestive processes, which control energy intake in humans and pigs.The close resemblance of the pig digestive system to humans, and prevalence of cereal grains in their diets provides a research platform to investigate: 1) the individual and combined effects of grain digestibility and fibre on GIT passage rate; and 2) the combined effects of grain digestibility, fibre and GIT passage rate on feed intake (FI). The interventional, invasive and non-invasive, studies underlying this investigation were designed to manipulate three presumed physiological mechanisms controlling the GIT passage rate: 1) gastric emptying rate; 2) interplay of digestion rate and passage rate in the SI – slow digestion rate may trigger ileal brake when undigested nutrients reach the ileum; and 3) colonic brake triggered by fermentation in the LI.The research methodology: 1) characterised intrinsic grain digestibility by determining enzyme diffusion rate (EDR) in milled grain particles and then associated the EDR with ileal digesiblity in pigs. 2) established the effects of partially fermentable and soluble (wheat bran) and largely unfermentable and insoluble (oat hulls) fibres offered with highly digestible starch-based diets on FI and LI fermentation in pigs. Furthermore, hydration capacity of starchy feeds, a measure of swellability, was determined. 3) determinedporcine intake of nutritionally balanced diets based on grains (milled wheat and sorghum; steam-flaked wheat and sorghum) with widely different EDR at 5% insoluble fibre level, and their effects on LI fermentation. 4) identified the effects of the four grain-based diets, as influenced by insoluble fibre level (0, 5 and 20%), on the GIT passage rate, expressed as cumulative mean retention time (MRT) in the stomach and SI, determined with indigestible markers. The key findings were -EDR of grains mainly differed based on grain type, physical structure affected by environmental stressors, maturity level and treatment process used before milling of the grain.Partially fermentable fibre, wheat bran, lowered intake of the highly digestible starch-based diet. The effect could partially have resulted from activation of the colonic brake.Feed hydration capacity correlated tightly with intake of starch-based diets, mixed with different fibre levels, possibly by affecting gastric emptying rate.Steam-flaking approximately doubled the EDR of both wheat and sorghum. Sorghum because of its low digestibility in the SI fermented more than wheat in the LI. EDR of milled grains is negatively correlated to faecal short chain fatty acids (SCFA) concentration and positively to faecal pH respectively. There is an inverse association between the relative extents of SI digestion and LI fermentation.Fibre level affected MRT in the stomach and SI, which reduced the intake of grain-based diets.MRT decreased with increasing grain digestibility. Grain digestibility affected passage rate as shown by one hour shorter MRT of steam-flaked wheat compared with milled wheat and sorghum. Lower ileal digestibility, higher faecal SCFA concentration and longer MRT of milled sorghum compared with steam-flaked wheat all point towards the ileal brake mechanism being activated to reduce the passage rate for maximum nutrient utilisation.The interaction of grain digestibility and fibre amount affected MRT differently depending on the fibre level.FI appeared to be positively associated with passage rate. Passage rate increased with increasing grain digestibility. Grains digestibility had no effect on FI. This evidence suggests that passage rate may largely be controlled locally by the entericnervous system, whereas FI is controlled by both the enteric nervous system and the satiety centres in the brain.These findings provide novel insights into how the interplay of grain digestibility and fibre can be manipulated to induce satiety by influencing passage rate and feed/food intake, controlled by three underlying physiological mechanisms (gastric residence, enzyme digestion rate, microbial fermentation extent). This foundational understanding may inform nutritional strategies to maximise feed utilisation in pigs, and control food intake in humans.