Modulating a prebiotic food source influences inflammation and immune-regulating gut microbes and metabolites: insights from the BE GONE trial.

Colorectal cancer Dry beans Gut microbiota Inflammation Metabolites Obesity Prebiotic Proteomic biomarkers

Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
20 Nov 2023
Historique:
received: 20 08 2023
revised: 06 10 2023
accepted: 31 10 2023
medline: 2 12 2023
pubmed: 2 12 2023
entrez: 1 12 2023
Statut: aheadofprint

Résumé

Accessible prebiotic foods hold strong potential to jointly target gut health and metabolic health in high-risk patients. The BE GONE trial targeted the gut microbiota of obese surveillance patients with a history of colorectal neoplasia through a straightforward bean intervention. This low-risk, non-invasive dietary intervention trial was conducted at MD Anderson Cancer Center (Houston, TX, USA). Following a 4-week equilibration, patients were randomized to continue their usual diet without beans (control) or to add a daily cup of study beans to their usual diet (intervention) with immediate crossover at 8-weeks. Stool and fasting blood were collected every 4 weeks to assess the primary outcome of intra and inter-individual changes in the gut microbiome and in circulating markers and metabolites within 8 weeks. This study was registered on ClinicalTrials.gov as NCT02843425, recruitment is complete and long-term follow-up continues. Of the 55 patients randomized by intervention sequence, 87% completed the 16-week trial, demonstrating an increase on-intervention in diversity [n = 48; linear mixed effect and 95% CI for inverse Simpson index: 0.16 (0.02, 0.30); p = 0.02] and shifts in multiple bacteria indicative of prebiotic efficacy, including increased Faecalibacterium, Eubacterium and Bifidobacterium (all p < 0.05). The circulating metabolome showed parallel shifts in nutrient and microbiome-derived metabolites, including increased pipecolic acid and decreased indole (all p < 0.002) that regressed upon returning to the usual diet. No significant changes were observed in circulating lipoproteins within 8 weeks; however, proteomic biomarkers of intestinal and systemic inflammatory response, fibroblast-growth factor-19 increased, and interleukin-10 receptor-α decreased (p = 0.01). These findings underscore the prebiotic and potential therapeutic role of beans to enhance the gut microbiome and to regulate host markers associated with metabolic obesity and colorectal cancer, while further emphasizing the need for consistent and sustainable dietary adjustments in high-risk patients. This study was funded by the American Cancer Society.

Sections du résumé

BACKGROUND BACKGROUND
Accessible prebiotic foods hold strong potential to jointly target gut health and metabolic health in high-risk patients. The BE GONE trial targeted the gut microbiota of obese surveillance patients with a history of colorectal neoplasia through a straightforward bean intervention.
METHODS METHODS
This low-risk, non-invasive dietary intervention trial was conducted at MD Anderson Cancer Center (Houston, TX, USA). Following a 4-week equilibration, patients were randomized to continue their usual diet without beans (control) or to add a daily cup of study beans to their usual diet (intervention) with immediate crossover at 8-weeks. Stool and fasting blood were collected every 4 weeks to assess the primary outcome of intra and inter-individual changes in the gut microbiome and in circulating markers and metabolites within 8 weeks. This study was registered on ClinicalTrials.gov as NCT02843425, recruitment is complete and long-term follow-up continues.
FINDINGS RESULTS
Of the 55 patients randomized by intervention sequence, 87% completed the 16-week trial, demonstrating an increase on-intervention in diversity [n = 48; linear mixed effect and 95% CI for inverse Simpson index: 0.16 (0.02, 0.30); p = 0.02] and shifts in multiple bacteria indicative of prebiotic efficacy, including increased Faecalibacterium, Eubacterium and Bifidobacterium (all p < 0.05). The circulating metabolome showed parallel shifts in nutrient and microbiome-derived metabolites, including increased pipecolic acid and decreased indole (all p < 0.002) that regressed upon returning to the usual diet. No significant changes were observed in circulating lipoproteins within 8 weeks; however, proteomic biomarkers of intestinal and systemic inflammatory response, fibroblast-growth factor-19 increased, and interleukin-10 receptor-α decreased (p = 0.01).
INTERPRETATION CONCLUSIONS
These findings underscore the prebiotic and potential therapeutic role of beans to enhance the gut microbiome and to regulate host markers associated with metabolic obesity and colorectal cancer, while further emphasizing the need for consistent and sustainable dietary adjustments in high-risk patients.
FUNDING BACKGROUND
This study was funded by the American Cancer Society.

Identifiants

pubmed: 38040541
pii: S2352-3964(23)00439-5
doi: 10.1016/j.ebiom.2023.104873
pii:
doi:

Banques de données

ClinicalTrials.gov
['NCT02843425']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104873

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests Study beans were independently purchased with funds from the Dry Bean Health Research Program, a peer-reviewed incentive award (to CRD) created by the Northarvest Bean Growers Association, Communique Inc. to identify and encourage researchers that apply for NIH-funding to support studies on beans and human health.

Auteurs

Xiaotao Zhang (X)

Division of Cancer Prevention and Population Sciences, Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; Institute for Translational Epidemiology & Division of Liver Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Ehsan Irajizad (E)

Division of Basic Sciences, Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Kristi L Hoffman (KL)

Alkek Center for Metagenomics and Microbiome Research, Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX, USA.

Johannes F Fahrmann (JF)

Red & Charline McCombs Institute for the Early Detection and Treatment of Cancer, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; Division of Cancer Prevention and Population Sciences, Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Fangyu Li (F)

Division of Cancer Prevention and Population Sciences, Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Yongwoo David Seo (YD)

Division of Surgery, Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Gladys J Browman (GJ)

Division of Cancer Prevention and Population Sciences, Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Jennifer B Dennison (JB)

Red & Charline McCombs Institute for the Early Detection and Treatment of Cancer, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Jody Vykoukal (J)

Red & Charline McCombs Institute for the Early Detection and Treatment of Cancer, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Pamela N Luna (PN)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA.

Wesley Siu (W)

Division of Cancer Prevention and Population Sciences, Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Ranran Wu (R)

Red & Charline McCombs Institute for the Early Detection and Treatment of Cancer, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Eunice Murage (E)

Red & Charline McCombs Institute for the Early Detection and Treatment of Cancer, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Nadim J Ajami (NJ)

Platform for Innovative Microbiome and Translational Research, Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Jennifer L McQuade (JL)

Division of Cancer Medicine, Department of Melanoma Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Jennifer A Wargo (JA)

Division of Surgery, Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; Platform for Innovative Microbiome and Translational Research, Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

James P Long (JP)

Division of Basic Sciences, Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Kim-Anh Do (KA)

Division of Basic Sciences, Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Johanna W Lampe (JW)

Public Health Sciences Division, Fred Hutchinson Cancer Center, Seattle, WA, USA.

Karen M Basen-Engquist (KM)

Division of Cancer Prevention and Population Sciences, Department of Heath Disparities Research, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Pablo C Okhuysen (PC)

Department of Infectious Diseases, Infection Control, and Employee Health, Division of Internal Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Scott Kopetz (S)

Department of Gastrointestinal Medical Oncology, Division of Cancer Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Samir M Hanash (SM)

Red & Charline McCombs Institute for the Early Detection and Treatment of Cancer, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; Division of Cancer Prevention and Population Sciences, Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Joseph F Petrosino (JF)

Alkek Center for Metagenomics and Microbiome Research, Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX, USA.

Paul Scheet (P)

Division of Cancer Prevention and Population Sciences, Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Carrie R Daniel (CR)

Division of Cancer Prevention and Population Sciences, Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA. Electronic address: cdaniel@mdanderson.org.

Classifications MeSH