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      The Effects of Intact Cereal Grain Fibers, Including Wheat Bran on the Gut Microbiota Composition of Healthy Adults: A Systematic Review

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          Abstract

          The human microbiota is increasingly recognized as a major factor influencing health and well-being, with potential benefits as diverse as improved immunity, reduced risk of obesity, Type 2 diabetes, and improved cognition and mood. Bacteria inhabiting the gut are dependent on the provision of fermentable dietary substrates making diet a major factor driving the composition of the human gut microbiota. Dietary fiber may modify microbiota abundance, diversity, and metabolism including short-chain fatty acid production. The majority of research to date has explored isolated fibers, and the influence of habitual fiber consumption is less well-established. The aim of the current article was to systematically review evidence from human intervention studies for the effects of intact cereal fibers, and their active sub-fractions, on gut microbiota composition in healthy adults. Studies published in the past 20 years were identified through the PubMed and Cochrane electronic databases. Inclusion criteria were: healthy adult participants (>18 years), inclusion of at least one intact cereal fiber, or its sub-fraction, and measurement of fecal microbiota related outcomes. As every individual has a unique microbiota many trials utilized a cross-over design where individuals acted as their own control. Outcome measures included change to the microbiota, species diversity, or species abundance, or metabolic indicators of microbiota fermentation such as short chain fatty acids or fecal nitrogen. Two hundred and twenty three publications were identified and 40 included in the final review. In discussing the findings, particular attention has been paid to the effects of wheat fiber, bran, and arabinoxylans (AXOS) as this is the dominant source of fiber in many Western countries. Thirty-nine of the forty-two studies demonstrated an increase in microbiota diversity and/or abundance following intact cereal fiber consumption, with effects apparent from 24 h to 52 weeks. Increases in wheat fiber as low as 6–8 g were sufficient to generate significant effects. Study duration ranged from 1 day to 12 weeks, with a single study over 1 year, and exploration of the stability of the microbiota following long-term dietary change is required. Increasing cereal fiber consumption should be encouraged for overall good health and for gut microbiota diversity.

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          Most cited references54

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          Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces.

          Weight loss diets for humans that are based on a high intake of protein but low intake of fermentable carbohydrate may alter microbial activity and bacterial populations in the large intestine and thus impact on gut health. In this study, 19 healthy, obese (body mass index range, 30 to 42) volunteers were given in succession three different diets: maintenance (M) for 3 days (399 g carbohydrate/day) and then high protein/medium (164 g/day) carbohydrate (HPMC) and high protein/low (24 g/day) carbohydrate (HPLC) each for 4 weeks. Stool samples were collected at the end of each dietary regimen. Total fecal short-chain fatty acids were 114 mM, 74 mM, and 56 mM (P < 0.001) for M, HPMC, and HPLC diets, respectively, and there was a disproportionate reduction in fecal butyrate (18 mM, 9 mM, and 4 mM, respectively; P < 0.001) with decreasing carbohydrate. Major groups of fecal bacteria were monitored using nine 16S rRNA-targeted fluorescence in situ hybridization probes, relative to counts obtained with the broad probe Eub338. No significant change was seen in the relative counts of the bacteroides (Bac303) (mean, 29.6%) or the clostridial cluster XIVa (Erec482, 23.3%), cluster IX (Prop853, 9.3%), or cluster IV (Fprau645, 11.6%; Rbro730 plus Rfla729, 9.3%) groups. In contrast, the Roseburia spp. and Eubacterium rectale subgroup of cluster XIVa (11%, 8%, and 3% for M, HPMC, and HPLC, respectively; P < 0.001) and bifidobacteria (4%, 2.1%, and 1.9%, respectively; P = 0.026) decreased as carbohydrate intake decreased. The abundance of butyrate-producing bacteria related to Roseburia spp. and E. rectale correlated well with the decline in fecal butyrate.
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            Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men.

            There is growing interest in understanding how diet affects the intestinal microbiota, including its possible associations with systemic diseases such as metabolic syndrome. Here we report a comprehensive and deep microbiota analysis of 14 obese males consuming fully controlled diets supplemented with resistant starch (RS) or non-starch polysaccharides (NSPs) and a weight-loss (WL) diet. We analyzed the composition, diversity and dynamics of the fecal microbiota on each dietary regime by phylogenetic microarray and quantitative PCR (qPCR) analysis. In addition, we analyzed fecal short chain fatty acids (SCFAs) as a proxy of colonic fermentation, and indices of insulin sensitivity from blood samples. The diet explained around 10% of the total variance in microbiota composition, which was substantially less than the inter-individual variance. Yet, each of the study diets induced clear and distinct changes in the microbiota. Multiple Ruminococcaceae phylotypes increased on the RS diet, whereas mostly Lachnospiraceae phylotypes increased on the NSP diet. Bifidobacteria decreased significantly on the WL diet. The RS diet decreased the diversity of the microbiota significantly. The total 16S ribosomal RNA gene signal estimated by qPCR correlated positively with the three major SCFAs, while the amount of propionate specifically correlated with the Bacteroidetes. The dietary responsiveness of the individual's microbiota varied substantially and associated inversely with its diversity, suggesting that individuals can be stratified into responders and non-responders based on the features of their intestinal microbiota.
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              Gut microbiome composition is linked to whole grain-induced immunological improvements.

              The involvement of the gut microbiota in metabolic disorders, and the ability of whole grains to affect both host metabolism and gut microbial ecology, suggest that some benefits of whole grains are mediated through their effects on the gut microbiome. Nutritional studies that assess the effect of whole grains on both the gut microbiome and human physiology are needed. We conducted a randomized cross-over trial with four-week treatments in which 28 healthy humans consumed a daily dose of 60 g of whole-grain barley (WGB), brown rice (BR), or an equal mixture of the two (BR+WGB), and characterized their impact on fecal microbial ecology and blood markers of inflammation, glucose and lipid metabolism. All treatments increased microbial diversity, the Firmicutes/Bacteroidetes ratio, and the abundance of the genus Blautia in fecal samples. The inclusion of WGB enriched the genera Roseburia, Bifidobacterium and Dialister, and the species Eubacterium rectale, Roseburia faecis and Roseburia intestinalis. Whole grains, and especially the BR+WGB treatment, reduced plasma interleukin-6 (IL-6) and peak postprandial glucose. Shifts in the abundance of Eubacterium rectale were associated with changes in the glucose and insulin postprandial response. Interestingly, subjects with greater improvements in IL-6 levels harbored significantly higher proportions of Dialister and lower abundance of Coriobacteriaceae. In conclusion, this study revealed that a short-term intake of whole grains induced compositional alterations of the gut microbiota that coincided with improvements in host physiological measures related to metabolic dysfunctions in humans.
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                Author and article information

                Contributors
                Journal
                Front Nutr
                Front Nutr
                Front. Nutr.
                Frontiers in Nutrition
                Frontiers Media S.A.
                2296-861X
                29 March 2019
                2019
                : 6
                : 33
                Affiliations
                [1] 1Independent Researcher , Bracknell, United Kingdom
                [2] 2The Kellogg Company , Manchester, United Kingdom
                Author notes

                Edited by: Jean-Pierre Guyot, Institut de Recherche pour le Développement (IRD), France

                Reviewed by: Philippe Gérard, Institut National de la Recherche Agronomique (INRA), France; Williams Turpin, University of Toronto, Canada

                *Correspondence: Angie Jefferson angie@ 123456angiejefferson.co.uk

                This article was submitted to Nutrition and Microbes, a section of the journal Frontiers in Nutrition

                Article
                10.3389/fnut.2019.00033
                6449473
                30984765
                c54717f3-2329-4105-b870-9f5136198f21
                Copyright © 2019 Jefferson and Adolphus.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 05 December 2018
                : 07 March 2019
                Page count
                Figures: 1, Tables: 3, Equations: 0, References: 75, Pages: 21, Words: 18435
                Categories
                Nutrition
                Systematic Review

                cereal fiber,dietary fiber,gut microbiome,gut microbiota,prebiotic,wheat fiber,wheat bran, systematic review

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