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

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; CJ Reynolds; J. F. Roberts; R. J. Boynton; D. M. Altmann; J. A. K. McDonald; J. R. Marchesi; A. N. Akbar; N. E. Riddell; Gareth Wallis; G. Frost

doi: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

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, CJ Reynolds, J. F. Roberts, R. J. Boynton, D. M. Altmann, J. A. K. McDonald, J. R. Marchesi, A. N. Akbar, N. E. Riddell, Gareth Wallis, G. Frost

Sport, Exercise and Rehabilitation Sciences

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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.

Original language	English
Pages (from-to)	1430-1438
Number of pages	9
Journal	Gut
Volume	68
Issue number	8
Early online date	10 Apr 2019
DOIs	https://doi.org/10.1136/gutjnl-2019-318424
Publication status	Published - Aug 2019

Bibliographical 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/.

Keywords

colonic microflora
glucose metabolism
inflammation
short-chain fatty acids

ASJC Scopus subject areas

Gastroenterology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Chambers, E. S., Byrne, C. S., Morrison, D. J., Murphy, K. G., Preston, T., Catriona Tedford, M., Garcia-Perez, I., Fountana, S., Serran-Contreras, J. I., Holmes, E., Reynolds, CJ., Roberts, J. F., Boynton, R. J., Altmann, D. M., McDonald, J. A. K., Marchesi, J. R., Akbar, A. N., Riddell, N. E., Wallis, G., & 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, 68(8), 1430-1438. https://doi.org/10.1136/gutjnl-2019-318424

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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 crossover trial",

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.",

keywords = "colonic microflora, glucose metabolism, inflammation, short-chain fatty acids",

author = "Chambers, {E. S.} and Byrne, {C. S.} and Morrison, {D. J.} and Murphy, {K. G.} and T. Preston and {Catriona Tedford}, M and I. Garcia-Perez and S. Fountana and Serran-Contreras, {J. I.} and E. Holmes and CJ Reynolds and Roberts, {J. F.} and Boynton, {R. J.} and Altmann, {D. M.} and McDonald, {J. A. K.} and Marchesi, {J. R.} and Akbar, {A. N.} and Riddell, {N. E.} and Gareth Wallis and G. Frost",

note = "{\textcopyright} 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/.",

year = "2019",

month = aug,

doi = "10.1136/gutjnl-2019-318424",

language = "English",

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Chambers, ES, Byrne, CS, Morrison, DJ, Murphy, KG, Preston, T, Catriona Tedford, M, Garcia-Perez, I, Fountana, S, Serran-Contreras, JI, Holmes, E, Reynolds, CJ, Roberts, JF, Boynton, RJ, Altmann, DM, McDonald, JAK, Marchesi, JR, Akbar, AN, Riddell, NE, Wallis, G & 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, E. S.; Byrne, C. S.; Morrison, D. J. et al.
In: Gut, Vol. 68, No. 8, 08.2019, p. 1430-1438.

Research output: Contribution to journal › Article › peer-review

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, E. S.

AU - Byrne, C. S.

AU - Morrison, D. J.

AU - Murphy, K. G.

AU - Preston, T.

AU - Catriona Tedford, M

AU - Garcia-Perez, I.

AU - Fountana, S.

AU - Serran-Contreras, J. I.

AU - Holmes, E.

AU - Reynolds, CJ

AU - Roberts, J. F.

AU - Boynton, R. J.

AU - Altmann, D. M.

AU - McDonald, J. A. K.

AU - Marchesi, J. R.

AU - Akbar, A. N.

AU - Riddell, N. E.

AU - Wallis, Gareth

AU - Frost, G.

N1 - © 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/.

PY - 2019/8

Y1 - 2019/8

N2 - 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.

AB - 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.

KW - colonic microflora

KW - glucose metabolism

KW - inflammation

KW - short-chain fatty acids

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Chambers ES, Byrne CS, Morrison DJ, Murphy KG, Preston T, Catriona Tedford M et al. 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. 2019 Aug;68(8):1430-1438. Epub 2019 Apr 10. doi: 10.1136/gutjnl-2019-318424