Effects of Arabinoxylan and Resistant Starch on Intestinal Microbiota and Short-Chain Fatty Acids in Subjects with Metabolic Syndrome: A Randomised Crossover Study.

Stine Hald,Kjeld Hermansen,Anne Grethe Schioldan,Mary E Moore,Jørgen Agnholt,Anders Dige,Maria L Marco,Knud Erik Bach Knudsen,Helle Nygaard Lærke,Søren Gregersen,Jens F Dahlerup

doi:10.1371/journal.pone.0159223

Stine Hald, Kjeld Hermansen + Show 9 more

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https://doi.org/10.1371/journal.pone.0159223

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Abstract

Recently, the intestinal microbiota has been emphasised as an important contributor to the development of metabolic syndrome. Dietary fibre may exert beneficial effects through modulation of the intestinal microbiota and metabolic end products. We investigated the effects of a diet enriched with two different dietary fibres, arabinoxylan and resistant starch type 2, on the gut microbiome and faecal short-chain fatty acids. Nineteen adults with metabolic syndrome completed this randomised crossover study with two 4-week interventions of a diet enriched with arabinoxylan and resistant starch and a low-fibre Western-style diet. Faecal samples were collected before and at the end of the interventions for fermentative end-product analysis and 16S ribosomal RNA bacterial gene amplification for identification of bacterial taxa. Faecal carbohydrate residues were used to verify compliance. The diet enriched with arabinoxylan and resistant starch resulted in significant reductions in the total species diversity of the faecal-associated intestinal microbiota but also increased the heterogeneity of bacterial communities both between and within subjects. The proportion of Bifidobacterium was increased by arabinoxylan and resistant starch consumption (P<0.001), whereas the proportions of certain bacterial genera associated with dysbiotic intestinal communities were reduced. Furthermore, the total short-chain fatty acids (P<0.01), acetate (P<0.01) and butyrate concentrations (P<0.01) were higher by the end of the diet enriched with arabinoxylan and resistant starch compared with those resulting from the Western-style diet. The concentrations of isobutyrate (P = 0.05) and isovalerate (P = 0.03) decreased in response to the arabinoxylan and resistant starch enriched diet, indicating reduced protein fermentation. In conclusion, arabinoxylan and resistant starch intake changes the microbiome and short-chain fatty acid compositions, with potential beneficial effects on colonic health and metabolic syndrome.Trial RegistrationClinicalTrials.gov NCT01618526

Highlights

Increased consumption of dietary fibre (DF) has been shown to improve components of metabolic syndrome (MetS), including dyslipidaemia, insulin sensitivity and abdominal obesity,[1,2,3] which are well-known risk factors for cardiovascular disease and type 2 diabetes. These beneficial effects are most likely modulated through the actions of DF on certain bacteria in the colon[4] and the capabilities of these bacteria to produce an array of small organic molecules, including short-chain fatty acids (SCFAs).[5]
The concentrations of formic acid, valeric acid, heptanoic acid and succinic acid concentrations remained unchanged, and those of sorbic acid, benzoic acid and hippuric acid were all below the detection levels. In this 4-week, randomised, crossover, dietary intervention study of individuals with MetS, we found that a diet rich in Resistant starch (RS) and AX modified the gut microbiome and increased the concentration of faecal SCFAs in general and those of butyrate and acetate in particular compared with a low-fibre diet
This finding corroborates that of a previous study reporting that a diet high in RS is associated with decreased bacterial diversity relative to other diets.[52]

Summary

Introduction

Increased consumption of dietary fibre (DF) has been shown to improve components of metabolic syndrome (MetS), including dyslipidaemia, insulin sensitivity and abdominal obesity,[1,2,3] which are well-known risk factors for cardiovascular disease and type 2 diabetes. These beneficial effects are most likely modulated through the actions of DF on certain bacteria in the colon[4] and the capabilities of these bacteria to produce an array of small organic molecules, including short-chain fatty acids (SCFAs).[5] Increased production of SCFAs in general and of butyrate in particular may protect against diet-induced obesity and improve insulin sensitivity. RS type 2 has been shown to augment butyrate production[12, 13] and to modify the composition of the intestinal microbiota[5, 14,15,16] typically by increasing the proportions of Bifidobacterium species, Ruminococcus bromii[14, 17] and Eubacterium rectale. [14] Studies on RS type 3 have been conducted and shown enhancement of Ruminococcus bromii and Eubacterium rectale,[18, 19] whereas RS type 4 apparently demonstrate different functional effects on the microbiota by augmentation of Bifidobacterium adolescentis and Parabacteroides distasonis.[14]

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