Dietary supplementation with inulin-propionate ester or inulin improves insulin sensitivity in adults with overweight and obesity with distinct effects on the gut microbiota, plasma metabolome and systemic inflammatory responses: a randomised cross-over trial

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Title: Dietary supplementation with inulin-propionate ester or inulin improves insulin sensitivity in adults with overweight and obesity with distinct effects on the gut microbiota, plasma metabolome and systemic inflammatory responses: a randomised cross-over trial
Authors: Chambers, E
Byrne, C
Morrison, D
Murphy, K
Preston, T
Tedford, MC
Garcia Perez, I
Fountana, S
Serrano Contreras, J
Holmes, E
Roberts, J
Reynolds, C
Boyton, R
Altmann, D
McDonald, J
Marchesi, J
Akbar, A
Riddell, N
Wallis, G
Frost, G
Item Type: Journal Article
Abstract: Objective: To investigate the underlying mechanisms behind changes in glucose homeostasis with delivery of propionate to the human colon by comprehensive and coordinated analysis of gut bacterial composition, plasma metabolome and immune responses. Design: Twelve non-diabetic adults with overweight and obesity received 20g/day of inulin-propionate ester (IPE), designed to selectively deliver propionate to the colon, a high-fermentable fibre control (inulin) and a low-fermentable fibre control (cellulose) in a randomised, double-blind, placebo controlled, crossover design. Outcome measurements of metabolic responses, inflammatory markers and gut bacterial composition were analysed at the end of each 42-day supplementation period. Results: Both IPE and inulin supplementation improved insulin resistance compared to cellulose supplementation, measured by homeostatic model assessment (HOMA) 2 (Mean±SEM 1.23±0.17 IPE vs. 1.59±0.17 cellulose, P=0.001; 1.17±0.15 inulin vs. 1.59±0.17 cellulose, P=0.009), with no differences between IPE and inulin (P=0.272). Fasting insulin was only associated positively with plasma tyrosine and negatively with plasma glycine following inulin supplementation. IPE supplementation decreased pro-inflammatory IL-8 levels compared to cellulose, whilst inulin had no impact on the systemic inflammatory markers studied. Inulin promoted changes in gut bacterial populations at the class level (increased Actinobacteria and decreased Clostridia) and order level (decreased Clostridales) compared to cellulose, with small differences at the species level observed between IPE and cellulose. Conclusion: These data demonstrate a distinctive physiological impact of raising colonic propionate delivery in humans, as improvements in insulin sensitivity promoted by IPE and inulin were accompanied with different effects on the plasma metabolome, gut bacterial populations and markers of systemic inflammation.
Issue Date: 5-Jul-2019
Date of Acceptance: 24-Feb-2019
URI: http://hdl.handle.net/10044/1/66974
DOI: https://doi.org/10.1136/gutjnl-2019-318424
ISSN: 0017-5749
Publisher: BMJ Publishing Group
Start Page: 1430
End Page: 1438
Journal / Book Title: Gut
Volume: 68
Issue: 8
Copyright Statement: © Author(s) (or their employer(s)) 2019. Re-use permitted under CC BY. Published by BMJ. This is an open access article distributed in accordance with the Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits others to copy, redistribute, remix, transform and build upon this work for any purpose, provided the original work is properly cited, a link to the licence is given, and indication of whether changes were made. See: https://creativecommons.org/licenses/by/4.0/.
Sponsor/Funder: Biotechnology and Biological Sciences Research Council (BBSRC)
Welton Foundation
Imperial College Healthcare NHS Trust- BRC Funding
Versus Arthritis
Biotechnology and Biological Sciences Research Council (BBSRC)
Imperial Health Charity
Imperial College Healthcare NHS Trust- BRC Funding
Funder's Grant Number: BB/L004259/1
N/A
RDF01 79560
21135
BB/H004971/1
80108
RDA27
Keywords: Science & Technology
Life Sciences & Biomedicine
Gastroenterology & Hepatology
CHAIN FATTY-ACIDS
TARGETED DELIVERY
BODY-WEIGHT
PROTEIN
GLUCOSE
FIBER
RISK
BIFIDOBACTERIA
RESISTANCE
DISEASE
colonic microflora
glucose metabolism
inflammation
short-chain fatty acids
Adult
Body Mass Index
Cross-Over Studies
Dietary Supplements
Double-Blind Method
Feces
Female
Gastrointestinal Microbiome
Humans
Inflammation
Insulin
Insulin Resistance
Inulin
Male
Metabolome
Middle Aged
Obesity
Overweight
Propionates
Treatment Outcome
Feces
Humans
Insulin Resistance
Obesity
Inflammation
Propionates
Inulin
Insulin
Body Mass Index
Treatment Outcome
Cross-Over Studies
Double-Blind Method
Dietary Supplements
Adult
Middle Aged
Female
Male
Overweight
Metabolome
Gastrointestinal Microbiome
1103 Clinical Sciences
1114 Paediatrics and Reproductive Medicine
Gastroenterology & Hepatology
Publication Status: Published online
Online Publication Date: 2019-04-10
Appears in Collections:Faculty of Medicine



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