Breath volatile metabolome reveals the impact of dietary fibres on the gut microbiota: Proof of concept in healthy volunteers

Audrey M Neyrinck, Julie Rodriguez, Zhengxiao Zhang, Julie-Anne Nazare, Laure B Bindels, Patrice D Cani, Véronique Maquet, Martine Laville, Stephan C Bischoff, Jens Walter, Nathalie M Delzenne, Audrey M Neyrinck, Julie Rodriguez, Zhengxiao Zhang, Julie-Anne Nazare, Laure B Bindels, Patrice D Cani, Véronique Maquet, Martine Laville, Stephan C Bischoff, Jens Walter, Nathalie M Delzenne

Abstract

Background: Current data suggest that dietary fibre (DF) interaction with the gut microbiota largely contributes to their physiological effects. The bacterial fermentation of DF leads to the production of metabolites, most of them are volatile. This study analyzed the breath volatile metabolites (BVM) profile in healthy individuals (n=15) prior and after a 3-week intervention with chitin-glucan (CG, 4.5 g/day), an insoluble fermentable DF.

Methods: The present exploratory study presents the original data related to the secondary outcomes, notably the analysis of BVM. BVM were analyzed throughout the test days -in fasting state and after standardized meals - using selected ion flow tube mass spectrometry (SIFT-MS). BVM production was correlated to the gut microbiota composition (Illumina sequencing, primary outcome), analyzed before and after the intervention.

Findings: The data reveal that the post-prandial state versus fasting state is a key determinant of BVM fingerprint. Correlation analyses with fecal microbiota spotlighted butyrate-producing bacteria, notably Faecalibacterium, as dominant bacteria involved in butyrate and other BVM expiration. CG intervention promotes interindividual variations of fasting BVM, and decreases or delays the expiration of most exhaled BVM in favor of H2 expiration, without any consequence on gastrointestinal tolerance.

Interpretation: Assessing BVM is a non-invasive methodology allowing to analyze the influence of DF intervention on the gut microbiota.

Funding: FiberTAG project was initiated from a European Joint Programming Initiative "A Healthy Diet for a Healthy Life" (JPI HDHL) and was supported by the Service Public de Wallonie (SPW-EER, convention 1610365, Belgium).

Keywords: Breath volatile metabolome; Chitin-glucan; Fermentation; Fibre; Gut microbiota; Short-chain fatty acids.

Conflict of interest statement

P.D.C. is cofounder of A-Mansia Biotech SA and owner of patents on Akkermansia muciniphila, gut microbes and metabolic diseases. The other authors declare no conflict of interest.

Copyright © 2022 The Author(s). Published by Elsevier B.V. All rights reserved.

Figures

Figure 1
Figure 1
Overview of the study design during the test days.
Figure 2
Figure 2
Hydrogen exhaled in the breath of healthy subjects (n=15) in response to a standardized breakfast intake prior (day 0) and after (day 21) chitin-glucan intake. Data present absolute values (a) and changes from baseline (b). Data are medians ± interquartile ranges (*p < 0.05; matched-pairs Wilcoxon signed-rank test).
Figure 3
Figure 3
Targeted BVM concentrations (changes from baseline) exhaled in breath of healthy subjects (n=15) in response to a standardized breakfast intake prior (day 0) and after (day 21) chitin-glucan intake (and significantly affected by the chitin-glucan intake during 3 weeks). Data are medians ± interquartile ranges (*p < 0.05; matched-pairs Wilcoxon signed-rank test on net area under the curve).
Figure 4
Figure 4
Correlation analysis between breath volatile metabolites (ppm, exhaled at time 8h) and gut microbiota composition of 15 healthy subjects (n=15) prior chitin-glucan intervention (day 0). Barplots of relative abundance of genus levels accounting for more than 1% for each subject (a). Heatmap of correlations between genera accounting for more than 1% for each subject and BVM (at time 8h, in ppm, corrected by the baseline value at fasted state) (b). The presence of a circle indicates that the correlation is significant, p < 0.05 (Spearman's correlation test).

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