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Metabolic signature of 13C-labeled wheat bran consumption related to gut fermentation in humans: a pilot study

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Abstract

Purpose

The aim of this pilot study was to analyze concomitantly the kinetics of production of 13C-labeled gut-derived metabolites from 13C-labeled wheat bran in three biological matrices (breath, plasma, stools), in order to assess differential fermentation profiles among subjects.

Methods

Six healthy women consumed a controlled breakfast containing 13C-labeled wheat bran biscuits. H2, CH4 and 13CO2, 13CH4 24 h-concentrations in breath were measured, respectively, by gas chromatography (GC) and GC-isotope ratio mass spectrometry (GC-IRMS). Plasma and fecal concentrations of 13C-short-chain fatty acids (linear SCFAs: acetate, propionate, butyrate, valerate; branched SCFAs: isobutyrate, isovalerate) were quantified using GC-combustion-IRMS. Gut microbiota composition was assessed by16S rRNA gene sequencing analysis.

Results

H2 and CH4 24 h-kinetics distinguished two groups in terms of fermentation-related gas excretion: high-CH4 producers vs low-CH4 producers (fasting concentrations: 45.3 ± 13.6 ppm vs 6.5 ± 3.6 ppm). Expired 13CH4 was enhanced and prolonged in high-CH4 producers compared to low-CH4 producers. The proportion of plasma and stool 13C-butyrate tended to be higher in low-CH4 producers, and inversely for 13C-acetate. Plasma branched SCFAs revealed different kinetics of apparition compared to linear SCFAs.

Conclusion

This pilot study allowed to consider novel procedures for the development of biomarkers revealing dietary fiber-gut microbiota interactions. The non-invasive assessment of exhaled gas following 13C-labeled fibers ingestion enabled to decipher distinct fermentation profiles: high-CH4 producers vs low-CH4 producers. The isotope labeling permits a specific in vivo characterisation of the dietary fiber impact consumption on microbiota metabolite production.

Clinical trial registration

The study has been registered under the number NCT03717311 at ClinicalTrials.gov on October 24, 2018.

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Data availability

Data will be available from the corresponding author on reasonable request.

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Acknowledgements

We thank all the staff of the Centre de Recherche en Nutrition Humaine Rhône-Alpes and more particularly N. Feugier, S. Lambert-Porcheron, L. Van Den Berghe, M. Sothier, E. Brossa, A. Samperiz, C. Louche-Pélissier and A. Cestre for their excellent technical assistance in subject recruitment, sample collection and analysis, and dietary surveys. We thank the six subjects who participated in this study. 13C-Wheat bran biscuits were designed and made by the Nutrition Department of Mondelēz International, Saclay, France. 13CH4 measurements were performed by Sam Barker and Rob Berstan from Elementar UK Ltd (data presented). The Stable Isotope Facility at UC Davis performed the analysis of duplicate samples (identical results not shown). NMD is a recipient of grants from the Fonds de la Recherche Scientifique (FRS-FNRS) [PINT-MULTI R.8013.19 (NEURONERANET, call 2019) and PDR T.0068.19].

Funding

FiberTAG project was initiated from a European Joint Programming Initiative ‘A Healthy Diet for a Healthy Life’ (JPI HDHL). Funding for this article is provided by the Agence Nationale de la Recherche (ANR, France).

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Author notes

  1. Laure Meiller and Valérie Sauvinet have contributed equally to this work.

Authors and Affiliations

  1. Centre de Recherche en Nutrition Humaine Rhône-Alpes, Univ-Lyon, INSERM, INRAe, Claude Bernard Lyon1 University, Centre Hospitalier Lyon Sud, Hospices Civils de Lyon, Pierre Bénite, France

    Laure Meiller, Valérie Sauvinet, Anne-Esther Breyton, Harimalala Ranaivo, Martine Laville & Julie-Anne Nazare

  2. CarMeN Laboratory, INSERM, INRAe, Claude Bernard Lyon1 University, Pierre Bénite, France

    Anne-Esther Breyton, Harimalala Ranaivo, Martine Laville & Julie-Anne Nazare

  3. Service de Biochimie et Biologie Moléculaire, Hospices Civils de Lyon, Pierre Bénite, France

    Christelle Machon & Anne Mialon

  4. Nutrition Research, Mondelez International, Saclay, France

    Alexandra Meynier & Sophie Vinoy

  5. Institute of Nutritional Medicine, University of Hohenheim, Stuttgart, Germany

    Stephan C. Bischoff

  6. Department of Medicine, School of Microbiology, APC Microbiome Ireland, University College Cork, Cork, Ireland

    Jens Walter

  7. Metabolism and Nutrition Research Group, UCLouvain, Brussels, Belgium

    Audrey M. Neyrinck & Nathalie M. Delzenne

  8. Service d’Endocrinologie Diabète Nutrition, Hospices Civils de Lyon, Pierre Bénite, France

    Martine Laville

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Contributions

LM, VS, AEB, AM, SCB, JW, AMN, ML, NMD, SV and JAN contributed to the study design. AEB contributed to data collection. LM, VS, CM and AM performed the analysis. LM, VS, HR and JAN wrote the manuscript. All authors reviewed the manuscript.

Corresponding author

Correspondence to Julie-Anne Nazare.

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Conflict of interest

A Meynier and S Vinoy are Mondelez International employees. No potential conflict of interest was reported by the other author(s).

Informed consent

The study protocol was in line with the Declaration of Helsinki and was approved by the Ethics Committee (Comité de Protection des Personnes Nord-Ouest IV, France, Registration Number: 2018 A00949 46). All participants signed written informed consent.

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Meiller, L., Sauvinet, V., Breyton, AE. et al. Metabolic signature of 13C-labeled wheat bran consumption related to gut fermentation in humans: a pilot study. Eur J Nutr 62, 2633–2648 (2023). https://doi.org/10.1007/s00394-023-03161-5

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