The Effect of Selected Synbiotics on Microbial Composition and Short-Chain Fatty Acid Production in a Model System of the Human Colon

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Abstract

Background

Prebiotics, probiotics and synbiotics can be used to modulate both the composition and activity of the gut microbiota and thereby potentially affecting host health beneficially. The aim of this study was to investigate the effects of eight synbiotic combinations on the composition and activity of human fecal microbiota using a four-stage semicontinuous model system of the human colon.

Methods and Findings

Carbohydrates were selected by their ability to enhance growth of the probiotic bacteria Lactobacillus acidophilus NCFM (NCFM) and Bifidobacterium animalis subsp. lactis Bl-04 (Bl-04) under laboratory conditions. The most effective carbohydrates for each probiotic were further investigated, using the colonic model, for the ability to support growth of the probiotic bacteria, influence the composition of the microbiota and stimulate formation of short-chain fatty acids (SCFA).The following combinations were studied: NCFM with isomaltulose, cellobiose, raffinose and an oat β-glucan hydrolysate (OBGH) and Bl-04 with melibiose, xylobiose, raffinose and maltotriose. All carbohydrates showed capable of increasing levels of NCFM and Bl-04 during fermentations in the colonic model by 10 ³–10 ⁴ fold and 10–10 ² fold, respectively. Also the synbiotic combinations decreased the modified ratio of Bacteroidetes/Firmicutes (calculated using qPCR results for Bacteroides-Prevotella-Porphyromonas group, Clostridium perfringens cluster I, Clostridium coccoides - Eubacterium rectale group and Clostridial cluster XIV) as well as significantly increasing SCFA levels, especially acetic and butyric acid, by three to eight fold, as compared to the controls. The decreases in the modified ratio of Bacteroidetes/ Firmicutes were found to be correlated to increases in acetic and butyric acid (p = 0.04 and p = 0.03, respectively).

Conclusions

The results of this study show that all synbiotic combinations investigated are able to shift the predominant bacteria and the production of SCFA of fecal microbiota in a model system of the human colon, thereby potentially being able to manipulate the microbiota in a way connected to human health.

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Most cited references 34

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Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease.

Sofia Tedelind, Fredrik Westberg, Martin Kjerrulf … (2007)

To compare the anti-inflammatory properties of butyrate with two other SCFAs, namely acetate and propionate, which have less well-documented effects on inflammation. The effect of SCFAs on cytokine release from human neutrophils was studied with ELISA. SCFA-dependent modulation of NF-kappaB reporter activity was assessed in the human colon adenocarcinoma cell line, Colo320DM. Finally, the effect of SCFAs on gene expression and cytokine release, measured with RT-PCR and ELISA, respectively, was studied in mouse colon organ cultures established from colitic mice. Acetate, propionate and butyrate at 30 mmol/L decreased LPS-stimulated TNFalpha release from neutrophils, without affecting IL-8 protein release. All SCFAs dose dependently inhibited NF-kappaB reporter activity in Colo320DM cells. Propionate dose-dependently suppressed IL-6 mRNA and protein release from colon organ cultures and comparative studies revealed that propionate and butyrate at 30 mmol/L caused a strong inhibition of immune-related gene expression, whereas acetate was less effective. A similar inhibition was achieved with the proteasome inhibitor MG-132, but not the p38 MAPK inhibitor SB203580. All SCFAs decreased IL-6 protein release from organ cultures. In the present study propionate and butyrate were equipotent, whereas acetate was less effective, at suppressing NF-kappaB reporter activity, immune-related gene expression and cytokine release in vitro. Our findings suggest that propionate and acetate, in addition to butyrate, could be useful in the treatment of inflammatory disorders, including IBD.

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Clinical trial: the effects of a trans-galactooligosaccharide prebiotic on faecal microbiota and symptoms in irritable bowel syndrome.

G Tzortzis, Glenn R. Gibson, Alain Silk … (2009)

Gut microflora-mucosal interactions may be involved in the pathogenesis of irritable bowel syndrome (IBS). To investigate the efficacy of a novel prebiotic trans-galactooligosaccharide in changing the colonic microflora and improve the symptoms in IBS sufferers. In all, 44 patients with Rome II positive IBS completed a 12-week single centre parallel crossover controlled clinical trial. Patients were randomized to receive either 3.5 g/d prebiotic, 7 g/d prebiotic or 7 g/d placebo. IBS symptoms were monitored weekly and scored according to a 7-point Likert scale. Changes in faecal microflora, stool frequency and form (Bristol stool scale) subjective global assessment (SGA), anxiety and depression and QOL scores were also monitored. The prebiotic significantly enhanced faecal bifidobacteria (3.5 g/d P < 0.005; 7 g/d P < 0.001). Placebo was without effect on the clinical parameters monitored, while the prebiotic at 3.5 g/d significantly changed stool consistency (P < 0.05), improved flatulence (P < 0.05) bloating (P < 0.05), composite score of symptoms (P < 0.05) and SGA (P < 0.05). The prebiotic at 7 g/d significantly improved SGA (P < 0.05) and anxiety scores (P < 0.05). The galactooligosaccharide acted as a prebiotic in specifically stimulating gut bifidobacteria in IBS patients and is effective in alleviating symptoms. These findings suggest that the prebiotic has potential as a therapeutic agent in IBS.

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Randomised, double-blind, placebo-controlled trial of fructo-oligosaccharides in active Crohn's disease.

Jane L Benjamin, Charlotte Hedin, Andreas L Koutsoumpas … (2011)

The commensal intestinal microbiota drive the inflammation associated with Crohn's disease. However, bacteria such as bifidobacteria and Faecalibacterium prausnitzii appear to be immunoregulatory. In healthy subjects the intestinal microbiota are influenced by prebiotic carbohydrates such as fructo-oligosaccharides (FOS). Preliminary data suggest that FOS increase faecal bifidobacteria, induce immunoregulatory dendritic cell (DC) responses and reduce disease activity in patients with Crohn's disease. To assess the impact of FOS in patients with active Crohn's disease using an adequately powered randomised double-blind placebo-controlled trial with predefined clinical, microbiological and immunological end points. Patients with active Crohn's disease were randomised to 15 g/day FOS or non-prebiotic placebo for 4 weeks. The primary end point was clinical response at week 4 (fall in Crohn's Disease Activity Index of ≥ 70 points) in the intention-to-treat (ITT) population. 103 patients were randomised to receive FOS (n = 54) or placebo (n = 49). More patients receiving FOS (14 (26%) vs 4 (8%); p = 0.018) withdrew before the 4-week end point. There was no significant difference in the number of patients achieving a clinical response between the FOS and placebo groups in the ITT analysis (12 (22%) vs 19 (39%), p = 0.067). Patients receiving FOS had reduced proportions of interleukin (IL)-6-positive lamina propria DC and increased DC staining of IL-10 (p < 0.05) but no change in IL-12p40 production. There were no significant differences in the faecal concentration of bifidobacteria and F prausnitzii between the groups at baseline or after the 4-week intervention. An adequately powered placebo-controlled trial of FOS showed no clinical benefit in patients with active Crohn's disease, despite impacting on DC function. ISRCTN50422530.

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Author and article information

Contributors

Stefan Bereswill: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2012

Publication date (Electronic): 17 October 2012

Volume: 7

Issue: 10

Electronic Location Identifier: e47212

Affiliations

[1 ]Department of Food Science, Faculty of Life Sciences, University of Copenhagen, Frederiksberg, Denmark

[2 ]Enzyme and Protein Chemistry, Department of Systems Biology, Technical University of Denmark, Kgs. Lyngby, Denmark

[3 ]Department of Plant Biology and Biotechnology, Faculty of Life Sciences, University of Copenhagen Frederiksberg, Denmark

[4 ]DuPont Nutrition and Health, Kantvik, Finland

[5 ]Biovelop A/S, Kvistgård, Denmark

Charité-University Medicine Berlin, Germany

Author notes

* E-mail: gcz@ 123456life.ku.dk

Competing Interests: Henna Röytiö, Sofia Forssten and Sampo J. Lahtinen are employed by DuPont Nutrition & Health, a manufacturer of the probiotics used in this study. Mark Lawther is employed by Biovelop A/S, the manufacturer of the β-glucan used in this study. Other authors declare no conflict of interest. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

Contributed reagents/materials/analysis tools: SJL SF HR. Conceived and designed the experiments, preparation of carbohydrates: AB. Conceived and designed the experiments, colonic model: SJL MJ BS LJ. Performed the experiments, preparation of carbohydrates: AK helped by AB and ML. Performed the experiments, colonic model: GCVZ helped by HR and SF. Analyzed the data: GCVZ helped by HR SF and SJL. Wrote the manuscript: GCVZ helped by MJ. Manuscript revised by: AB SF SJL BS LJ. All authors read and approved its final version.

Article

Publisher ID: PONE-D-12-16122

DOI: 10.1371/journal.pone.0047212

PMC ID: 3474826

PubMed ID: 23082149

SO-VID: e5a8c8d1-9020-486b-87e4-c0d5e43bee28

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 26 April 2012

Date accepted : 10 September 2012

Page count

Pages: 11

Funding

This project was funded by the Danish Strategic Research Council’s Program Committee on Health, Food and Welfare (FøSu). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

The Effect of Selected Synbiotics on Microbial Composition and Short-Chain Fatty Acid Production in a Model System of the Human Colon

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Abstract

Background

Methods and Findings

Conclusions

Related collections

PLOS Climate

Most cited references 34

Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease.

Clinical trial: the effects of a trans-galactooligosaccharide prebiotic on faecal microbiota and symptoms in irritable bowel syndrome.

Randomised, double-blind, placebo-controlled trial of fructo-oligosaccharides in active Crohn's disease.

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