Noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the FiberTAG intervention study

The fermentation of dietary fibre (DF) leads to the production of bioactive metabolites, the most volatile ones being excreted in the breath. The aim of this study was to analyze the profile of exhaled breath volatile metabolites (BVM) and gastrointestinal symptoms in healthy volunteers after a sing...

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Main Authors: Audrey M. Neyrinck, Julie Rodriguez, Zhengxiao Zhang, Benjamin Seethaler, Florence Mailleux, Joeri Vercammen, Laure B. Bindels, Patrice D. Cani, Julie-Anne Nazare, Véronique Maquet, Martine Laville, Stephan C. Bischoff, Jens Walter, Nathalie M. Delzenne
Format: Article
Language:English
Published: Taylor & Francis Group 2021-01-01
Series:Gut Microbes
Subjects:
Online Access:http://dx.doi.org/10.1080/19490976.2020.1862028
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spelling doaj-6cfb6301c90c4f62bfabfb14375922852021-07-26T12:59:35ZengTaylor & Francis GroupGut Microbes1949-09761949-09842021-01-0113110.1080/19490976.2020.18620281862028Noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the FiberTAG intervention studyAudrey M. Neyrinck0Julie Rodriguez1Zhengxiao Zhang2Benjamin Seethaler3Florence Mailleux4Joeri Vercammen5Laure B. Bindels6Patrice D. Cani7Julie-Anne Nazare8Véronique Maquet9Martine Laville10Stephan C. Bischoff11Jens Walter12Nathalie M. Delzenne13UCLouvain, Université catholique de LouvainUCLouvain, Université catholique de LouvainUniversity of AlbertaUniversity of HohenheimUCLouvain, Université catholique de LouvainInterscienceUCLouvain, Université catholique de LouvainUCLouvain, Université catholique de LouvainUniversité Claude Bernard Lyon1, Hospices Civils de Lyon, CENS, FCRIN/FORCE NetworkKitoZymeUniversité Claude Bernard Lyon1, Hospices Civils de Lyon, CENS, FCRIN/FORCE NetworkUniversity of HohenheimUniversity of AlbertaUCLouvain, Université catholique de LouvainThe fermentation of dietary fibre (DF) leads to the production of bioactive metabolites, the most volatile ones being excreted in the breath. The aim of this study was to analyze the profile of exhaled breath volatile metabolites (BVM) and gastrointestinal symptoms in healthy volunteers after a single ingestion of maltodextrin (placebo) versus chitin-glucan (CG), an insoluble DF previously shown to be fermented into short-chain fatty acids (SCFA) by the human microbiota in vitro. Maltodextrin (4.5 g at day 0) or CG (4.5 g at day 2) were added to a standardized breakfast in fasting healthy volunteers (n = 15). BVM were measured using selected ion flow tube mass spectrometry (SIFT-MS) throughout the day. A single ingestion of 4.5 g CG did not induce significant gastrointestinal discomfort. Untargeted metabolomics analysis of breath highlighted that 13 MS-fragments (among 408 obtained from ionizations of breath) discriminated CG versus maltodextrin acute intake in the posprandial state. The targeted analysis revealed that CG increased exhaled butyrate and 5 other BVM – including the microbial metabolites 2,3-butanedione and 3-hydroxybutanone – with a peak observed 6 h after CG intake. Correlation analyses with fecal microbiota (Illumina 16S rRNA sequencing) spotlighted Mitsuokella as a potential genus responsible for the presence of butyric acid, triethylamine and 3-hydroxybutanone in the breath. In conclusion, measuring BMV in the breath reveals the microbial signature of the fermentation of DF after a single ingestion. This protocol allows to analyze the time-course of released bioactive metabolites that could be proposed as new biomarkers of DF fermentation, potentially linked to their biological properties. Trial registration: Clinical Trials NCT03494491. Registered 11 April 2018 – Retrospectively registered, https://clinicaltrials.gov/ct2/show/NCT03494491http://dx.doi.org/10.1080/19490976.2020.1862028gut microbiotachitin-glucanfermentationbreath volatile metabolitesscfainsoluble dietary fibre
collection DOAJ
language English
format Article
sources DOAJ
author Audrey M. Neyrinck
Julie Rodriguez
Zhengxiao Zhang
Benjamin Seethaler
Florence Mailleux
Joeri Vercammen
Laure B. Bindels
Patrice D. Cani
Julie-Anne Nazare
Véronique Maquet
Martine Laville
Stephan C. Bischoff
Jens Walter
Nathalie M. Delzenne
spellingShingle Audrey M. Neyrinck
Julie Rodriguez
Zhengxiao Zhang
Benjamin Seethaler
Florence Mailleux
Joeri Vercammen
Laure B. Bindels
Patrice D. Cani
Julie-Anne Nazare
Véronique Maquet
Martine Laville
Stephan C. Bischoff
Jens Walter
Nathalie M. Delzenne
Noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the FiberTAG intervention study
Gut Microbes
gut microbiota
chitin-glucan
fermentation
breath volatile metabolites
scfa
insoluble dietary fibre
author_facet Audrey M. Neyrinck
Julie Rodriguez
Zhengxiao Zhang
Benjamin Seethaler
Florence Mailleux
Joeri Vercammen
Laure B. Bindels
Patrice D. Cani
Julie-Anne Nazare
Véronique Maquet
Martine Laville
Stephan C. Bischoff
Jens Walter
Nathalie M. Delzenne
author_sort Audrey M. Neyrinck
title Noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the FiberTAG intervention study
title_short Noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the FiberTAG intervention study
title_full Noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the FiberTAG intervention study
title_fullStr Noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the FiberTAG intervention study
title_full_unstemmed Noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the FiberTAG intervention study
title_sort noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the fibertag intervention study
publisher Taylor & Francis Group
series Gut Microbes
issn 1949-0976
1949-0984
publishDate 2021-01-01
description The fermentation of dietary fibre (DF) leads to the production of bioactive metabolites, the most volatile ones being excreted in the breath. The aim of this study was to analyze the profile of exhaled breath volatile metabolites (BVM) and gastrointestinal symptoms in healthy volunteers after a single ingestion of maltodextrin (placebo) versus chitin-glucan (CG), an insoluble DF previously shown to be fermented into short-chain fatty acids (SCFA) by the human microbiota in vitro. Maltodextrin (4.5 g at day 0) or CG (4.5 g at day 2) were added to a standardized breakfast in fasting healthy volunteers (n = 15). BVM were measured using selected ion flow tube mass spectrometry (SIFT-MS) throughout the day. A single ingestion of 4.5 g CG did not induce significant gastrointestinal discomfort. Untargeted metabolomics analysis of breath highlighted that 13 MS-fragments (among 408 obtained from ionizations of breath) discriminated CG versus maltodextrin acute intake in the posprandial state. The targeted analysis revealed that CG increased exhaled butyrate and 5 other BVM – including the microbial metabolites 2,3-butanedione and 3-hydroxybutanone – with a peak observed 6 h after CG intake. Correlation analyses with fecal microbiota (Illumina 16S rRNA sequencing) spotlighted Mitsuokella as a potential genus responsible for the presence of butyric acid, triethylamine and 3-hydroxybutanone in the breath. In conclusion, measuring BMV in the breath reveals the microbial signature of the fermentation of DF after a single ingestion. This protocol allows to analyze the time-course of released bioactive metabolites that could be proposed as new biomarkers of DF fermentation, potentially linked to their biological properties. Trial registration: Clinical Trials NCT03494491. Registered 11 April 2018 – Retrospectively registered, https://clinicaltrials.gov/ct2/show/NCT03494491
topic gut microbiota
chitin-glucan
fermentation
breath volatile metabolites
scfa
insoluble dietary fibre
url http://dx.doi.org/10.1080/19490976.2020.1862028
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