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Untargeted plasma metabolomic profiles associated with overall diet in women from the SU.VI.MAX cohort

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European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Dietary intakes are reflected in plasma by the presence of hundreds of exogenous metabolites and variations in endogenous metabolites. The exploration of diet-related plasma metabolic profiles could help to better understand the impact of overall diet on health. Our aim was to identify metabolomic signatures reflecting overall diet in women from the French general population.

Methods

This cross-sectional study included 160 women in the SU.VI.MAX cohort with detailed dietary data (≥ 10 24-h dietary records) selected according to their level of adherence to the French dietary recommendations, represented by the validated score mPNNS-GS; 80 women from the 10th decile of the score were matched with 80 women from the 1st decile. Plasma metabolomic profiles were acquired using untargeted UPLC-QToF mass spectrometry analysis. The associations between metabolomic profiles and the mPNNG-GS, its components and Principal Component Analyses-derived dietary patterns were investigated using multivariable conditional logistic regression models and partial correlations.

Results

Adherence to the dietary recommendations was positively associated with 3-indolepropionic acid and pipecolic acid (also positively associated with fruit and vegetable intake and a healthy diet)—2 metabolites linked to microbiota and inversely associated with lysophosphatidylcholine (LysoPC(17:1)), acylcarnitine C9:1 (also inversely associated with a healthy diet), acylcarnitine C11:1 and 2-deoxy-D-glucose. Increased plasma levels of piperine and Dihydro4mercapto-3(2H) furanone were observed in women who consumed a Western diet and a healthy diet, respectively. Ethyl-β-D-glucopyranoside was positively associated with alcohol intake. Plasma levels of LysoPC(17:1), cholic acid, phenylalanine-phenylalanine and phenylalanine and carnitine C9:1 decreased with the consumption of vegetable added fat, sweetened food, milk and dairy products and fruit and vegetable intakes, respectively.

Conclusion

This study highlighted several metabolites from both host and microbial metabolism reflecting the long-term impact of the overall diet.

Trial registration

SU.VI.MAX, clinicaltrials.gov NCT00272428. Registered 3 January 2006, https://clinicaltrials.gov/show/NCT00272428

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Abbreviations

SU.VI.MAX:

SUpplémentation en Vitamines et Minéraux AntioXydants

mPNNS-GS:

Modified Programme National Nutrition Santé- Guideline Score

UPLC:

Ultrahigh-performance liquid chromatography

LysoPC:

Lysophosphatidylcholine

FFQ:

Food frequency questionnaire

WHO:

World Health Organization

NMR:

Nuclear magnetic resonance

LC–MS:

Liquid chromatography mass spectrometry

PCA:

Principal component analysis

CVD:

Cardiovascular disease

BMI:

Body mass index

HCA:

Hierarchical clustering analysis

OR:

Odds ratios

SD:

Standard deviation

CI:

Confidence interval

FDR:

False discovery rate

BH:

Benjamini-Hochberg

PA:

Pipecolic acid

IPA:

3-Indolepropionic acid

2DG:

2-Deoxy-D-glucose

T2D:

Type 2 diabetes

HEI:

Healthy eating index

aMED:

Alternate mediterranean diet score

HDI:

Healthy diet indicator

BSD:

Baltic Sea diet

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Acknowledgements

The authors thank Younes Esseddik, Frédéric Coffinieres, Thi Hong Van Duong, Paul Flanzy, Régis Gatibelza, Jagatjit Mohinder and Maithyly Sivapalan (computer scientists), Rachida Mehroug and Frédérique Ferrat (logistic assistants), Nathalie Arnault, Véronique Gourlet, PhD, Fabien Szabo, PhD, Julien Allegre, and Laurent Bourhis (data-manager/statisticians) and Cédric Agaesse (dietitian) for their technical contribution to the SU.VI.MAX study. We also thank all participants of the SU.VI.MAX study. This work was conducted in the framework of the French network for Nutrition And Cancer Research (NACRe network), www.inra.fr/nacre and received the NACRe Partnership Label. Metabolomic analyses were performed within the metaboHUB French infrastructure (ANR-INBS-0010).

Funding

This work was supported by the French National Cancer Institute [Grant number INCa_8085 for the project, and PhD Grant number INCa_11323 for L. Lecuyer]; the Federative Institute for Biomedical Research IFRB Paris 13; and the Cancéropôle Ile-de-France/Région Ile-de-France [PhD Grant for M. Deschasaux]. The funders had no role in the design, analysis, or writing of this article.

Author information

Author notes

  1. Lucie Lécuyer and Céline Dalle share co-first-authorship

  2. Claudine Manach and Mathilde Touvier share co-last-authorship

Authors and Affiliations

  1. Sorbonne Paris Cité Epidemiology and Statistics Research Center (CRESS), French National Institute of Health and Medical Research (Inserm) U1153, French National Institute for Agricultural Research (Inra) U1125, French National Conservatory of Arts and Crafts (Cnam), Paris 13 University, Nutritional Epidemiology Research Team (EREN), 74 rue Marcel Cachin, 93017, Bobigny Cedex, France

    Lucie Lécuyer, Pilar Galan, Serge Hercberg, Valentin Partula, Mélanie Deschasaux, Bernard Srour, Paule Latino-Martel, Nathalie Druesne-Pecollo, Emmanuelle Kesse-Guyot & Mathilde Touvier

  2. Human Nutrition Unit, Université Clermont Auvergne, INRA, UMR 1019, 63000, Clermont-Ferrand, France

    Céline Dalle, Pierre Micheau & Claudine Manach

  3. Clermont Auvergne University, INRA, UNH, Plateforme d’Exploration du Métabolisme, MetaboHUB Clermont, 63000, Clermont-Ferrand, France

    Mélanie Pétéra, Delphine Centeno, Bernard Lyan, Stéphanie Durand & Estelle Pujos-Guillot

  4. Clermont Auvergne University, Institut de Chimie de Clermont-Ferrand, Plateforme d’Exploration du Métabolisme, MetaboHUB-Clermont, BP 80026, 63171, Aubière, France

    Marie Lagree

  5. Public Health Department, Avicenne Hospital, Bobigny, France

    Serge Hercberg

  6. Clermont Auvergne University, INRA, UMR 1019, Human Nutrition Unit (UNH), CRNH Auvergne, Cellular Micro-Environment, Immunomodulation and Nutrition (ECREIN), 63000, Clermont-Ferrand, France

    Adrien Rossary, Aicha Demidem & Marie-Paule Vasson

  7. Anticancer Center Jean-Perrin, CHU, Clermont-Ferrand, France

    Marie-Paule Vasson

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  1. Lucie Lécuyer
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  2. Céline Dalle
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Contributions

The author’s responsibilities were as follow CM and MT: designed the research and supervised data interpretation; LL and CD conducted the research; SH, PG, MT, EKG: conducted the SU.VI.MAX cohort and provided essential data and samples; DC, ML, SD, BL and EPG: performed metabolomic analyses; LL, CD and PM: performed statistical analysis; MT, CM, MP: supervised statistical analysis; LL, MT, CD, CM and EPG: wrote the paper; all authors provided critical intellectual input for data interpretation, read and approved the final manuscript; CM and MT had primary responsibility for final content.

Corresponding author

Correspondence to Lucie Lécuyer.

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Conflict of interest

The authors have no conflict of interest to disclose and the funders had no role in the design, analysis, or writing of this article.

Ethical approval

The study was conducted according to the guidelines laid down in the Declaration of Helsinki and approved by the Ethics Committee for Studies with Human Subjects of Paris-Cochin Hospital (CCPPRB 706/2364) and the ‘Commission Nationale de l’Informatique et des Libertés’ (CNIL 334641/907094). All subjects gave written informed consent to participate in the study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

394_2020_2177_MOESM1_ESM.docx

Supplementary file1 Loadings values of the a posteriori 3 dietary patterns derived by Principal Component Analysis (DOCX 27 kb)

Supplementary file2 Description and computation of mPNNS-GS (DOCX 31 kb)

Supplementary file3 Methods for MS metabolomic analysis (DOCX 103 kb)

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Supplementary file4 Identified metabolites associated with baseline clinical and biological parameters and nutrients intakes from Spearman correlation analyses (DOCX 58 kb)

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Supplementary file5 Associations between ions and the level of adherence to the French dietary recommendations, as measured by the a priori mPNNS-GS from multivariable conditional logistic regression (DOCX 50 kb)

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Supplementary file6 Associations between ions and components of the a priori mPNNS-GS from spearman correlation analyses (DOCX 363 kb)

394_2020_2177_MOESM7_ESM.docx

Supplementary file7 Associations between ions and a posteriori dietary patterns derived by principal component analysis from spearman correlation analyses (DOCX 96 kb)

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Lécuyer, L., Dalle, C., Micheau, P. et al. Untargeted plasma metabolomic profiles associated with overall diet in women from the SU.VI.MAX cohort. Eur J Nutr 59, 3425–3439 (2020). https://doi.org/10.1007/s00394-020-02177-5

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  • DOI: https://doi.org/10.1007/s00394-020-02177-5

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