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 crossover trial

Research output: Contribution to journalArticle

Authors

  • E. S. Chambers
  • C. S. Byrne
  • D. J. Morrison
  • K. G. Murphy
  • T. Preston
  • M Catriona Tedford
  • I. Garcia-Perez
  • S. Fountana
  • J. I. Serran-Contreras
  • E. Holmes
  • J. F. Roberts
  • CJ Reynolds
  • R. J. Boynton
  • D. M. Altmann
  • J. A. K. McDonald
  • J. R. Marchesi
  • A. N. Akbar
  • N. E. Riddell
  • G. Frost

Colleges, School and Institutes

External organisations

  • University of Glasgow
  • University of the West of Scotland
  • Imperial College London
  • University College London
  • University of Surrey

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 20 g/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, cross-over 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 with cellulose supplementation, measured by homeostatic model assessment 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 proinflammatory interleukin-8 levels compared with cellulose, while 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 Clostridiales) compared with 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.

Bibliographic note

© 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/.

Details

Original languageEnglish
Pages (from-to)1430-1438
Number of pages9
JournalGut
Volume68
Issue number8
Early online date10 Apr 2019
Publication statusPublished - Aug 2019

Keywords

  • colonic microflora, glucose metabolism, inflammation, short-chain fatty acids

ASJC Scopus subject areas