Effect of 1-year lifestyle intervention with energy-reduced Mediterranean diet and physical activity promotion on the gut metabolome and microbiota: a randomized clinical trial.

Mediterranean diet cardiovascular disease risk factor fecal metabolome fecal microbiota lifestyle intervention metabolic syndrome

Journal

The American journal of clinical nutrition
ISSN: 1938-3207
Titre abrégé: Am J Clin Nutr
Pays: United States
ID NLM: 0376027

Informations de publication

Date de publication:
29 Feb 2024
Historique:
received: 30 11 2023
revised: 23 02 2024
accepted: 26 02 2024
pubmed: 2 3 2024
medline: 2 3 2024
entrez: 1 3 2024
Statut: aheadofprint

Résumé

The health benefits of the Mediterranean diet (MedDiet) have been linked to the presence of beneficial gut microbes and related metabolites. However, its impact on the fecal metabolome remains poorly understood. Our goal was to investigate the weight-loss effects of a 1-y lifestyle intervention based on an energy-reduced MedDiet coupled with physical activity (intervention group), compared with an ad libitum MedDiet (control group), on fecal metabolites, fecal microbiota, and their potential association with cardiovascular disease risk factors. A total of 400 participants (200 from each study group), aged 55-75 y, and at high cardiovascular disease risk, were included. Dietary and lifestyle information, anthropometric measurements, blood biochemical parameters, and stool samples were collected at baseline and after 1 y of follow-up. Liquid chromatography-tandem mass spectrometry was used to profile endogenous fecal metabolites, and 16S amplicon sequencing was employed to profile the fecal microbiota. Compared with the control group, the intervention group exhibited greater weight loss and improvement in various cardiovascular disease risk factors. We identified intervention effects on 4 stool metabolites and subnetworks primarily composed of bile acids, ceramides, and sphingosines, fatty acids, carnitines, nucleotides, and metabolites of purine and the Krebs cycle. Some of these were associated with changes in several cardiovascular disease risk factors. In addition, we observed a reduction in the abundance of the genera Eubacterium hallii group and Dorea, and an increase in alpha diversity in the intervention group after 1 y of follow-up. Changes in the intervention-related microbiota profiles were also associated with alterations in different fecal metabolite subnetworks and some cardiovascular disease risk factors. An intervention based on an energy-reduced MedDiet and physical activity promotion, compared with an ad libitum MedDiet, was associated with improvements in cardiometabolic risk factors, potentially through modulation of the fecal microbiota and metabolome. This trial was registered at https://www.isrctn.com/ as ISRCTN89898870 (https://doi.org/10.1186/ISRCTN89898870).

Sections du résumé

BACKGROUND BACKGROUND
The health benefits of the Mediterranean diet (MedDiet) have been linked to the presence of beneficial gut microbes and related metabolites. However, its impact on the fecal metabolome remains poorly understood.
OBJECTIVES OBJECTIVE
Our goal was to investigate the weight-loss effects of a 1-y lifestyle intervention based on an energy-reduced MedDiet coupled with physical activity (intervention group), compared with an ad libitum MedDiet (control group), on fecal metabolites, fecal microbiota, and their potential association with cardiovascular disease risk factors.
METHODS METHODS
A total of 400 participants (200 from each study group), aged 55-75 y, and at high cardiovascular disease risk, were included. Dietary and lifestyle information, anthropometric measurements, blood biochemical parameters, and stool samples were collected at baseline and after 1 y of follow-up. Liquid chromatography-tandem mass spectrometry was used to profile endogenous fecal metabolites, and 16S amplicon sequencing was employed to profile the fecal microbiota.
RESULTS RESULTS
Compared with the control group, the intervention group exhibited greater weight loss and improvement in various cardiovascular disease risk factors. We identified intervention effects on 4 stool metabolites and subnetworks primarily composed of bile acids, ceramides, and sphingosines, fatty acids, carnitines, nucleotides, and metabolites of purine and the Krebs cycle. Some of these were associated with changes in several cardiovascular disease risk factors. In addition, we observed a reduction in the abundance of the genera Eubacterium hallii group and Dorea, and an increase in alpha diversity in the intervention group after 1 y of follow-up. Changes in the intervention-related microbiota profiles were also associated with alterations in different fecal metabolite subnetworks and some cardiovascular disease risk factors.
CONCLUSIONS CONCLUSIONS
An intervention based on an energy-reduced MedDiet and physical activity promotion, compared with an ad libitum MedDiet, was associated with improvements in cardiometabolic risk factors, potentially through modulation of the fecal microbiota and metabolome. This trial was registered at https://www.isrctn.com/ as ISRCTN89898870 (https://doi.org/10.1186/ISRCTN89898870).

Identifiants

DOI: 10.1016/j.ajcnut.2024.02.021 PMID: 38428742
pubmed: 38428742
pii: S0002-9165(24)00167-9
doi: 10.1016/j.ajcnut.2024.02.021
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.

Auteurs

Jesús F García-Gavilán (JF)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Departament de Bioquímica i Biotecnologia, Alimentaciò, Nutrició, Desenvolupament i Salut Mental (ANUT-DSM), Universitat Rovira i Virgili, Reus, Spain; Institut d'Investigació Sanitària Pere Virgili (IISPV), Reus, Spain.

Alessandro Atzeni (A)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Departament de Bioquímica i Biotecnologia, Alimentaciò, Nutrició, Desenvolupament i Salut Mental (ANUT-DSM), Universitat Rovira i Virgili, Reus, Spain; Institut d'Investigació Sanitària Pere Virgili (IISPV), Reus, Spain. Electronic address: alessandro.atzeni@urv.cat.

Nancy Babio (N)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Departament de Bioquímica i Biotecnologia, Alimentaciò, Nutrició, Desenvolupament i Salut Mental (ANUT-DSM), Universitat Rovira i Virgili, Reus, Spain; Institut d'Investigació Sanitària Pere Virgili (IISPV), Reus, Spain.

Liming Liang (L)

Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, United States; Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, United States.

Clara Belzer (C)

Laboratory of Microbiology, Wageningen University, Wageningen, The Netherlands.

Jesús Vioque (J)

CIBER de Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III, Madrid, Spain; Instituto de Investigación Sanitaria y Biomédica de Alicante, Universidad Miguel Hernández (ISABIAL-UMH), Alicante, Spain.

Dolores Corella (D)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Department of Preventive Medicine, University of Valencia, Valencia, Spain.

Montserrat Fitó (M)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Unit of Cardiovascular Risk and Nutrition, Institut Hospital del Mar de Investigaciones Médicas Municipal d'Investigació Médica (IMIM), Barcelona, Spain.

Josep Vidal (J)

CIBER Diabetes y Enfermedades Metabólicas (CIBERDEM), Instituto de Salud Carlos III (ISCIII), Madrid, Spain; Department of Endocrinology, Institut d'Investigacions Biomédiques August Pi Sunyer (IDIBAPS), Hospital Clinic, University of Barcelona, Barcelona, Spain.

Isabel Moreno-Indias (I)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Department of Endocrinology and Nutrition, Instituto de Investigación Biomédica de Málaga (IBIMA), Hospital Universitario Virgen de la Victoria, Málaga, Spain.

Laura Torres-Collado (L)

CIBER de Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III, Madrid, Spain; Instituto de Investigación Sanitaria y Biomédica de Alicante, Universidad Miguel Hernández (ISABIAL-UMH), Alicante, Spain.

Oscar Coltell (O)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Department of Computer Languages and Systems, Jaume I University, Castellón, Spain.

Estefanía Toledo (E)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Department of Preventive Medicine and Public Health, University of Navarra, Pamplona, Spain; Epidemiología y Salud Pública, Instituto de Investigación Sanitaria de Navarra (IdiSNA), Pamplona, Spain.

Clary Clish (C)

Metabolomics Platform, The Broad Institute of MIT and Harvard, Boston, MA, United States.

Javier Hernando (J)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Unit of Cardiovascular Risk and Nutrition, Institut Hospital del Mar de Investigaciones Médicas Municipal d'Investigació Médica (IMIM), Barcelona, Spain.

Huan Yun (H)

Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, United States; Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, United States.

Adrián Hernández-Cacho (A)

Departament de Bioquímica i Biotecnologia, Alimentaciò, Nutrició, Desenvolupament i Salut Mental (ANUT-DSM), Universitat Rovira i Virgili, Reus, Spain; Institut d'Investigació Sanitària Pere Virgili (IISPV), Reus, Spain.

Sarah Jeanfavre (S)

Metabolomics Platform, The Broad Institute of MIT and Harvard, Boston, MA, United States.

Courtney Dennis (C)

Metabolomics Platform, The Broad Institute of MIT and Harvard, Boston, MA, United States.

Ana M Gómez-Pérez (AM)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Department of Endocrinology and Nutrition, Instituto de Investigación Biomédica de Málaga (IBIMA), Hospital Universitario Virgen de la Victoria, Málaga, Spain.

Maria Angeles Martínez (MA)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Departament de Bioquímica i Biotecnologia, Alimentaciò, Nutrició, Desenvolupament i Salut Mental (ANUT-DSM), Universitat Rovira i Virgili, Reus, Spain; Institut d'Investigació Sanitària Pere Virgili (IISPV), Reus, Spain.

Miguel Ruiz-Canela (M)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Department of Preventive Medicine and Public Health, University of Navarra, Pamplona, Spain; Epidemiología y Salud Pública, Instituto de Investigación Sanitaria de Navarra (IdiSNA), Pamplona, Spain.

Francisco J Tinahones (FJ)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Department of Endocrinology and Nutrition, Instituto de Investigación Biomédica de Málaga (IBIMA), Hospital Universitario Virgen de la Victoria, Málaga, Spain.

Frank B Hu (FB)

Department of Nutrition, Harvard T. H. Chan School of Public Health, Boston, MA, United States; Channing Division for Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, United States.

Jordi Salas-Salvadó (J)

CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain; Departament de Bioquímica i Biotecnologia, Alimentaciò, Nutrició, Desenvolupament i Salut Mental (ANUT-DSM), Universitat Rovira i Virgili, Reus, Spain; Institut d'Investigació Sanitària Pere Virgili (IISPV), Reus, Spain. Electronic address: jordi.salas@urv.cat.

Classifications MeSH