Increasing plant protein in the diet induces changes in the plasma metabolome that may be beneficial for metabolic health. A randomized crossover study in males

Dietary shifts replacing animal protein (AP) with plant protein (PP) sources have been associated with lowering cardiometabolic risk (CMR), but underlying mechanisms are poorly characterized. This nutritional intervention aims to characterize the metabolic changes induced by diets containing differe...

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Veröffentlicht in:Clinical nutrition (Edinburgh, Scotland) Scotland), 2024-12, Vol.43 (12), p.146-157
Hauptverfasser: Lépine, Gaïa, Mariotti, François, Tremblay-Franco, Marie, Courrent, Marion, Verny, Marie-Anne, David, Jérémie, Mathé, Véronique, Jame, Patrick, Anchisi, Anthony, Lefranc-Millot, Catherine, Perreau, Caroline, Guérin-Deremaux, Laetitia, Chollet, Céline, Castelli, Florence, Chu-Van, Emeline, Huneau, Jean-François, Rémond, Didier, Pickering, Gisèle, Fouillet, Hélène, Polakof, Sergio
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container_issue 12
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container_title Clinical nutrition (Edinburgh, Scotland)
container_volume 43
creator Lépine, Gaïa
Mariotti, François
Tremblay-Franco, Marie
Courrent, Marion
Verny, Marie-Anne
David, Jérémie
Mathé, Véronique
Jame, Patrick
Anchisi, Anthony
Lefranc-Millot, Catherine
Perreau, Caroline
Guérin-Deremaux, Laetitia
Chollet, Céline
Castelli, Florence
Chu-Van, Emeline
Huneau, Jean-François
Rémond, Didier
Pickering, Gisèle
Fouillet, Hélène
Polakof, Sergio
description Dietary shifts replacing animal protein (AP) with plant protein (PP) sources have been associated with lowering cardiometabolic risk (CMR), but underlying mechanisms are poorly characterized. This nutritional intervention aims to characterize the metabolic changes induced by diets containing different proportions of AP and PP sources in males at CMR. This study is a 4-week, crossover, randomized, controlled-feeding trial in which 19 males with CMR followed two diets providing either 36 % for the control diet (CON-D) or 64 % for the flexitarian diet (FLEX-D) of total protein intake from PP sources. Plasma nontargeted metabolomes (LC-MS method) were measured in the fasted state and after a high-fat challenge meal at the end of each intervention arm. Lipogenesis and protein synthesis fluxes, flow-mediated dilatation (FMD) and gluco-lipidic responses were assessed after the challenge meal. Data were analyzed with mixed models, and univariate and multivariate models for metabolomics data. In both arms CMR improved with time, with decreased body weight (−0.9 %), insulin resistant (−34 %, HOMA-IR, Homeostatic Model Assessment for Insulin Resistance) and low-density lipoproteins (LDL)-cholesterol (−11 %). Diet had no effect on FMD or metabolic fluxes, but a trend (0.05
doi_str_mv 10.1016/j.clnu.2024.10.009
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This nutritional intervention aims to characterize the metabolic changes induced by diets containing different proportions of AP and PP sources in males at CMR. This study is a 4-week, crossover, randomized, controlled-feeding trial in which 19 males with CMR followed two diets providing either 36 % for the control diet (CON-D) or 64 % for the flexitarian diet (FLEX-D) of total protein intake from PP sources. Plasma nontargeted metabolomes (LC-MS method) were measured in the fasted state and after a high-fat challenge meal at the end of each intervention arm. Lipogenesis and protein synthesis fluxes, flow-mediated dilatation (FMD) and gluco-lipidic responses were assessed after the challenge meal. Data were analyzed with mixed models, and univariate and multivariate models for metabolomics data. In both arms CMR improved with time, with decreased body weight (−0.9 %), insulin resistant (−34 %, HOMA-IR, Homeostatic Model Assessment for Insulin Resistance) and low-density lipoproteins (LDL)-cholesterol (−11 %). Diet had no effect on FMD or metabolic fluxes, but a trend (0.05 &lt;p ≤ 0.1) was observed for a stronger decrease in HOMA-IR and lower postprandial glucose after FLEX-D vs CON-D. The abundance of 21 and 37 metabolites differed between diets at fasted and fed states, respectively, including food intake biomarkers of AP (methylhistidine, eicosapentaenoic acid, hydroxyprolines) and PP sources (trigonelline, N-acetyl-ornithine). In fasted or fed states, indole acrylic acid and indole propionic acid, both products of tryptophan catabolism, were higher after FLEX-D vs CON-D, while the indispensable amino acids-related metabolites alpha-aminoadipic acid, hydroxymethylbutyric acids and propionylcarnitine were lower. In the postprandial state only, the ω-oxidation products dodecanedioic, tetradecanedioic and hexadecanedioic acids were higher after FLEX-D vs CON-D. Despite little changes in risk factors after 4 wk, this study evidenced subtle metabolic adaptations in amino acids and lipid metabolism and gut microbiota activity occurring after higher PP source intake that may be beneficial to CMR. NCT04236518. 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A randomized crossover study in males</title><title>Clinical nutrition (Edinburgh, Scotland)</title><addtitle>Clin Nutr</addtitle><description>Dietary shifts replacing animal protein (AP) with plant protein (PP) sources have been associated with lowering cardiometabolic risk (CMR), but underlying mechanisms are poorly characterized. This nutritional intervention aims to characterize the metabolic changes induced by diets containing different proportions of AP and PP sources in males at CMR. This study is a 4-week, crossover, randomized, controlled-feeding trial in which 19 males with CMR followed two diets providing either 36 % for the control diet (CON-D) or 64 % for the flexitarian diet (FLEX-D) of total protein intake from PP sources. Plasma nontargeted metabolomes (LC-MS method) were measured in the fasted state and after a high-fat challenge meal at the end of each intervention arm. Lipogenesis and protein synthesis fluxes, flow-mediated dilatation (FMD) and gluco-lipidic responses were assessed after the challenge meal. Data were analyzed with mixed models, and univariate and multivariate models for metabolomics data. In both arms CMR improved with time, with decreased body weight (−0.9 %), insulin resistant (−34 %, HOMA-IR, Homeostatic Model Assessment for Insulin Resistance) and low-density lipoproteins (LDL)-cholesterol (−11 %). Diet had no effect on FMD or metabolic fluxes, but a trend (0.05 &lt;p ≤ 0.1) was observed for a stronger decrease in HOMA-IR and lower postprandial glucose after FLEX-D vs CON-D. The abundance of 21 and 37 metabolites differed between diets at fasted and fed states, respectively, including food intake biomarkers of AP (methylhistidine, eicosapentaenoic acid, hydroxyprolines) and PP sources (trigonelline, N-acetyl-ornithine). In fasted or fed states, indole acrylic acid and indole propionic acid, both products of tryptophan catabolism, were higher after FLEX-D vs CON-D, while the indispensable amino acids-related metabolites alpha-aminoadipic acid, hydroxymethylbutyric acids and propionylcarnitine were lower. In the postprandial state only, the ω-oxidation products dodecanedioic, tetradecanedioic and hexadecanedioic acids were higher after FLEX-D vs CON-D. Despite little changes in risk factors after 4 wk, this study evidenced subtle metabolic adaptations in amino acids and lipid metabolism and gut microbiota activity occurring after higher PP source intake that may be beneficial to CMR. NCT04236518. 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Plasma nontargeted metabolomes (LC-MS method) were measured in the fasted state and after a high-fat challenge meal at the end of each intervention arm. Lipogenesis and protein synthesis fluxes, flow-mediated dilatation (FMD) and gluco-lipidic responses were assessed after the challenge meal. Data were analyzed with mixed models, and univariate and multivariate models for metabolomics data. In both arms CMR improved with time, with decreased body weight (−0.9 %), insulin resistant (−34 %, HOMA-IR, Homeostatic Model Assessment for Insulin Resistance) and low-density lipoproteins (LDL)-cholesterol (−11 %). Diet had no effect on FMD or metabolic fluxes, but a trend (0.05 &lt;p ≤ 0.1) was observed for a stronger decrease in HOMA-IR and lower postprandial glucose after FLEX-D vs CON-D. The abundance of 21 and 37 metabolites differed between diets at fasted and fed states, respectively, including food intake biomarkers of AP (methylhistidine, eicosapentaenoic acid, hydroxyprolines) and PP sources (trigonelline, N-acetyl-ornithine). In fasted or fed states, indole acrylic acid and indole propionic acid, both products of tryptophan catabolism, were higher after FLEX-D vs CON-D, while the indispensable amino acids-related metabolites alpha-aminoadipic acid, hydroxymethylbutyric acids and propionylcarnitine were lower. In the postprandial state only, the ω-oxidation products dodecanedioic, tetradecanedioic and hexadecanedioic acids were higher after FLEX-D vs CON-D. Despite little changes in risk factors after 4 wk, this study evidenced subtle metabolic adaptations in amino acids and lipid metabolism and gut microbiota activity occurring after higher PP source intake that may be beneficial to CMR. NCT04236518. 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identifier ISSN: 0261-5614
ispartof Clinical nutrition (Edinburgh, Scotland), 2024-12, Vol.43 (12), p.146-157
issn 0261-5614
1532-1983
1532-1983
language eng
recordid cdi_hal_primary_oai_HAL_hal_04769512v1
source MEDLINE; Access via ScienceDirect (Elsevier)
subjects Adult
Blood Glucose - metabolism
Branched-chain amino acids
Cardiometabolic Risk Factors
Cross-Over Studies
Diet - methods
Fasting - blood
Food and Nutrition
Humans
Hypertriglyceridemic waist phenotype
Insulin Resistance
Life Sciences
Male
Metabolome - physiology
Middle Aged
Plant Proteins
Plant-based diet
Postprandial Period - physiology
Postprandial response
Trimethylamine-oxide
Young Adult
title Increasing plant protein in the diet induces changes in the plasma metabolome that may be beneficial for metabolic health. A randomized crossover study in males
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