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

Edward S. Chambers, Claire S. Byrne, Douglas J. Morrison, Kevin G. Murphy, Tom Preston, M. Catriona Tedford, Isabel Garcia-Perez, Sofia Fountana, Jose I. Serrano-Contreras, Elaine Holmes, Jordie F. Roberts, Catherine J. Reynolds, Rosemary J. Boyton, Daniel M. Altmann, Julie A.K. McDonald, Julian R. Marchesi, Arne N. Akbar, Natalie E. Riddell, Gareth A. Wallis, Gary Frost

Research output: Contribution to journalArticle

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.
Original languageEnglish
Pages (from-to)1430-1438
Number of pages9
JournalGut
Volume68
Issue number8
Early online date10 Apr 2019
DOIs
Publication statusE-pub ahead of print - 10 Apr 2019

Fingerprint

Inulin
Metabolome
Propionates
Dietary Supplements
Cross-Over Studies
Insulin Resistance
Esters
Obesity
Cellulose
Gastrointestinal Microbiome
Colon
Clostridium
Actinobacteria
Interleukin-8
Glycine
Population

Keywords

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

Cite this

Chambers, Edward S. ; Byrne, Claire S. ; Morrison, Douglas J. ; Murphy, Kevin G. ; Preston, Tom ; Tedford, M. Catriona ; Garcia-Perez, Isabel ; Fountana, Sofia ; Serrano-Contreras, Jose I. ; Holmes, Elaine ; Roberts, Jordie F. ; Reynolds, Catherine J. ; Boyton, Rosemary J. ; Altmann, Daniel M. ; McDonald, Julie A.K. ; Marchesi, Julian R. ; Akbar, Arne N. ; Riddell, Natalie E. ; Wallis, Gareth A. ; Frost, Gary. / 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. In: Gut. 2019 ; Vol. 68, No. 8. pp. 1430-1438.
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abstract = "ObjectiveTo 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.DesignTwelve 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.ResultsBoth 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.ConclusionThese 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.",
keywords = "short chain fatty acids, glucose metabolism, colonic microflora, inflammation",
author = "Chambers, {Edward S.} and Byrne, {Claire S.} and Morrison, {Douglas J.} and Murphy, {Kevin G.} and Tom Preston and Tedford, {M. Catriona} and Isabel Garcia-Perez and Sofia Fountana and Serrano-Contreras, {Jose I.} and Elaine Holmes and Roberts, {Jordie F.} and Reynolds, {Catherine J.} and Boyton, {Rosemary J.} and Altmann, {Daniel M.} and McDonald, {Julie A.K.} and Marchesi, {Julian R.} and Akbar, {Arne N.} and Riddell, {Natalie E.} and Wallis, {Gareth A.} and Gary Frost",
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Chambers, ES, Byrne, CS, Morrison, DJ, Murphy, KG, Preston, T, Tedford, MC, Garcia-Perez, I, Fountana, S, Serrano-Contreras, JI, Holmes, E, Roberts, JF, Reynolds, CJ, Boyton, RJ, Altmann, DM, McDonald, JAK, Marchesi, JR, Akbar, AN, Riddell, NE, Wallis, GA & Frost, G 2019, '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' Gut, vol. 68, no. 8, pp. 1430-1438. https://doi.org/10.1136/gutjnl-2019-318424

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. / Chambers, Edward S.; Byrne, Claire S.; Morrison, Douglas J.; Murphy, Kevin G.; Preston, Tom; Tedford, M. Catriona; Garcia-Perez, Isabel; Fountana, Sofia; Serrano-Contreras, Jose I.; Holmes, Elaine; Roberts, Jordie F.; Reynolds, Catherine J.; Boyton, Rosemary J.; Altmann, Daniel M.; McDonald, Julie A.K.; Marchesi, Julian R.; Akbar, Arne N.; Riddell, Natalie E.; Wallis, Gareth A.; Frost, Gary.

In: Gut, Vol. 68, No. 8, 10.04.2019, p. 1430-1438.

Research output: Contribution to journalArticle

TY - JOUR

T1 - 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

T2 - a randomised crossover trial

AU - Chambers, Edward S.

AU - Byrne, Claire S.

AU - Morrison, Douglas J.

AU - Murphy, Kevin G.

AU - Preston, Tom

AU - Tedford, M. Catriona

AU - Garcia-Perez, Isabel

AU - Fountana, Sofia

AU - Serrano-Contreras, Jose I.

AU - Holmes, Elaine

AU - Roberts, Jordie F.

AU - Reynolds, Catherine J.

AU - Boyton, Rosemary J.

AU - Altmann, Daniel M.

AU - McDonald, Julie A.K.

AU - Marchesi, Julian R.

AU - Akbar, Arne N.

AU - Riddell, Natalie E.

AU - Wallis, Gareth A.

AU - Frost, Gary

PY - 2019/4/10

Y1 - 2019/4/10

N2 - ObjectiveTo 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.DesignTwelve 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.ResultsBoth 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.ConclusionThese 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.

AB - ObjectiveTo 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.DesignTwelve 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.ResultsBoth 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.ConclusionThese 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.

KW - short chain fatty acids

KW - glucose metabolism

KW - colonic microflora

KW - inflammation

U2 - 10.1136/gutjnl-2019-318424

DO - 10.1136/gutjnl-2019-318424

M3 - Article

VL - 68

SP - 1430

EP - 1438

JO - Gut

JF - Gut

SN - 0017-5749

IS - 8

ER -