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

Gut Microbes. 2021 Jan-Dec;13(1):1-16. doi: 10.1080/19490976.2020.1862028.

Abstract

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.

Keywords: Gut microbiota; SCFA; breath volatile metabolites; chitin-glucan; fermentation; insoluble dietary fibre.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Breath Tests
  • Chitin / metabolism
  • Dietary Fiber / metabolism*
  • Fatty Acids, Volatile / analysis*
  • Fatty Acids, Volatile / metabolism
  • Feces / chemistry
  • Feces / microbiology
  • Fermentation
  • Gastrointestinal Microbiome
  • Glucans / metabolism
  • Healthy Volunteers
  • Humans
  • Polysaccharides / metabolism
  • RNA, Ribosomal, 16S / genetics
  • Respiratory Aerosols and Droplets / chemistry*
  • Young Adult

Substances

  • Dietary Fiber
  • Fatty Acids, Volatile
  • Glucans
  • Polysaccharides
  • RNA, Ribosomal, 16S
  • Chitin
  • maltodextrin

Associated data

  • ClinicalTrials.gov/NCT03494491

Grants and funding

FiberTAG project was initiated from a European Joint Programming Initiative “A Healthy Diet for a Healthy Life” (JPI HDHL). This work was supported by the Service Public de Wallonie (SPW-EER, convention 1610365, Belgium). NMD is a recipient of grants from Fond de la Recherche Scientifique (FRS-FNRS, convention PINT-MULTI R.8013.19 (NEURON, call 2019) and convention PDR T.0068.19) and from UCLouvain (Action de Recherche Concertée ARC18-23/092). SCB is a recipient of a grant from the German Federal Ministry for Education and Research (BMBF, Germany, ID: 01EA1701). PDC is supported by the Fonds Baillet Latour (Grant for Medical Research 2015), the Fonds de la Recherche Scientifique (FNRS, FRFS-WELBIO: WELBIO-CR-2019C-02R, and EOS program no. 30770923).