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Abstract
Short-chain fatty acids (SCFA), formed by microbial fermentation, are believed to be involved in the aetiology of obesity and diabetes. This study investigated the effects of colonic administration of physiologically relevant SCFA mixtures on human substrate and energy metabolism. In this randomized, double-blind, crossover study, twelve normoglycaemic men (BMI 25–35 kg/m2) underwent four investigational days, during which SCFA mixtures (200 mmol/L) high in either acetate (HA), propionate (HP), butyrate (HB) or placebo (PLA) were rectally administered during fasting and postprandial conditions (oral glucose load). Before and for two hours after colonic infusions, indirect calorimetry was performed and blood samples were collected. All three SCFA mixtures increased fasting fat oxidation (P < 0.01), whilst resting energy expenditure increased after HA and HP compared with PLA (P < 0.05). In addition, all three SCFA mixtures increased fasting and postprandial plasma peptide YY (PYY) concentrations, and attenuated fasting free glycerol concentrations versus PLA (P < 0.05). Colonic infusions of SCFA mixtures, in concentrations and ratios reached after fibre intake, increased fat oxidation, energy expenditure and PYY, and decreased lipolysis in overweight/obese men. Human intervention studies are warranted to investigate whether these effects translate into long-term benefits for body weight control and insulin sensitivity in the obese insulin resistant state.
Highlights
A growing body of evidence suggests that the gut microbiota has a crucial role in the regulation of energy and substrate metabolism and, as such, in the aetiology of cardiometabolic disease[1]
The included volunteers had an average age of 36 ± 3 years, a body mass index (BMI) of 30.3 ± 0.8 kg/m2 and were normoglycaemic
Energy expenditure increased following a colonic infusion of Short-chain fatty acids (SCFA) mixture high in acetate (HA) and a SCFA mixture high in propionate (HP) as compared to placebo (PLA) (P < 0.05, Fig. 1A and B)
Summary
A growing body of evidence suggests that the gut microbiota has a crucial role in the regulation of energy and substrate metabolism and, as such, in the aetiology of cardiometabolic disease[1]. Increasing evidence supports an important role of SCFA, including acetate, propionate and butyrate, in control of body weight and insulin sensitivity[2] These SCFA might have pronounced effects on host metabolism through the secretion of gut-derived signalling hormones[4,5,6] or by entering the systemic circulation[7], thereby affecting peripheral energy and substrate metabolism. Oral administration of acetate, propionate and butyrate to high-fat diet-fed mice all prevented gains in body weight and improved insulin sensitivity without changing energy intake and the amount of physical activity[8, 14, 15] Based on these rodent data, it is tempting to speculate that colonic administration of SCFA may have beneficial effects on human substrate and energy metabolism. Secondary outcomes were effects of SCFA mixtures on carbohydrate oxidation, circulating metabolites (triacylglycerol (TAG), free fatty acids (FFA), free glycerol, glucose, lactate) and hormones (insulin, PYY, glucagon-like peptide 1 (GLP-1), angiopoietin-like protein 4 (ANGPTL4)), plasma SCFA, inflammatory markers (tumour necrosis factor-alpha (TNF-α), interleukin-1-beta (IL-1β), interleukin-6 (IL-6), interleukin-8 (IL-8)) and Visual Analogue Scale (VAS)-scores for hunger and satiety during fasting and postprandial conditions
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