Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults

E.S. Chambers, A. Viardot, A. Psichas, D.J. Morrison, K.G. Murphy, S.E.K. Zac-Varghese, K. Macdougall, T. Preston, Catriona Tedford, Graham S. Finlayson, J.E. Blundell, Jimmy D. Bell, E. Louise Thomas, Shahrul Mt-Isa, Deborah Ashby, Glen R. Gibson, Sofia Kolida, Waljit S. Dhillo, S.R. Bloom, Wayne Morley & 2 others Stuart Clegg, G.S. Frost

Research output: Contribution to journalArticle

Abstract

The colonic microbiota ferment dietary fibres, producing short chain fatty acids. Recent evidence suggests that the short chain fatty acid propionate may play an important role in appetite regulation. We hypothesised that colonic delivery of propionate would increase peptide YY (PYY) and glucagon like peptide-1 (GLP-1) secretion in humans, and reduce energy intake and weight gain in overweight adults.
To investigate whether propionate promotes PYY and GLP-1 secretion, a primary cultured human colonic cell model was developed. To deliver propionate specifically to the colon, we developed a novel inulin-propionate ester. An acute randomised, controlled cross-over study was used to assess the effects of this inulin-propionate ester on energy intake and plasma PYY and GLP-1 concentrations. The long-term effects of inulin-propionate ester on weight gain were subsequently assessed in a randomised, controlled 24-week study involving 60 overweight adults.
Propionate significantly stimulated the release of PYY and GLP-1 from human colonic cells. Acute ingestion of 10 g inulin-propionate ester significantly increased postprandial plasma PYY and GLP-1 and reduced energy intake. Over 24 weeks, 10 g/day inulin-propionate ester supplementation significantly reduced weight gain, intra-abdominal adipose tissue distribution, intrahepatocellular lipid content and prevented the deterioration in insulin sensitivity observed in the inulin-control group.
These data demonstrate for the first time that increasing colonic propionate prevents weight gain in overweight adult humans.
Original languageEnglish
JournalGut
Volume64
Issue number11
DOIs
Publication statusPublished - Dec 2014

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Appetite Regulation
Propionates
Adiposity
Colon
Inulin
Peptide YY
Glucagon-Like Peptide 1
Esters
Weight Gain
Energy Intake
Volatile Fatty Acids
Body Weight Maintenance
Intra-Abdominal Fat
Microbiota
Dietary Fiber
Tissue Distribution
Cross-Over Studies
Insulin Resistance
Eating

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Chambers, E. S., Viardot, A., Psichas, A., Morrison, D. J., Murphy, K. G., Zac-Varghese, S. E. K., ... Frost, G. S. (2014). Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut, 64(11). https://doi.org/10.1136/gutjnl-2014-307913
Chambers, E.S. ; Viardot, A. ; Psichas, A. ; Morrison, D.J. ; Murphy, K.G. ; Zac-Varghese, S.E.K. ; Macdougall, K. ; Preston, T. ; Tedford, Catriona ; Finlayson, Graham S. ; Blundell, J.E. ; Bell, Jimmy D. ; Thomas, E. Louise ; Mt-Isa, Shahrul ; Ashby, Deborah ; Gibson, Glen R. ; Kolida, Sofia ; S. Dhillo, Waljit ; Bloom, S.R. ; Morley, Wayne ; Clegg, Stuart ; Frost, G.S. / Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. In: Gut. 2014 ; Vol. 64, No. 11.
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abstract = "The colonic microbiota ferment dietary fibres, producing short chain fatty acids. Recent evidence suggests that the short chain fatty acid propionate may play an important role in appetite regulation. We hypothesised that colonic delivery of propionate would increase peptide YY (PYY) and glucagon like peptide-1 (GLP-1) secretion in humans, and reduce energy intake and weight gain in overweight adults.To investigate whether propionate promotes PYY and GLP-1 secretion, a primary cultured human colonic cell model was developed. To deliver propionate specifically to the colon, we developed a novel inulin-propionate ester. An acute randomised, controlled cross-over study was used to assess the effects of this inulin-propionate ester on energy intake and plasma PYY and GLP-1 concentrations. The long-term effects of inulin-propionate ester on weight gain were subsequently assessed in a randomised, controlled 24-week study involving 60 overweight adults.Propionate significantly stimulated the release of PYY and GLP-1 from human colonic cells. Acute ingestion of 10 g inulin-propionate ester significantly increased postprandial plasma PYY and GLP-1 and reduced energy intake. Over 24 weeks, 10 g/day inulin-propionate ester supplementation significantly reduced weight gain, intra-abdominal adipose tissue distribution, intrahepatocellular lipid content and prevented the deterioration in insulin sensitivity observed in the inulin-control group.These data demonstrate for the first time that increasing colonic propionate prevents weight gain in overweight adult humans.",
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Chambers, ES, Viardot, A, Psichas, A, Morrison, DJ, Murphy, KG, Zac-Varghese, SEK, Macdougall, K, Preston, T, Tedford, C, Finlayson, GS, Blundell, JE, Bell, JD, Thomas, EL, Mt-Isa, S, Ashby, D, Gibson, GR, Kolida, S, S. Dhillo, W, Bloom, SR, Morley, W, Clegg, S & Frost, GS 2014, 'Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults' Gut, vol. 64, no. 11. https://doi.org/10.1136/gutjnl-2014-307913

Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. / Chambers, E.S.; Viardot, A.; Psichas, A.; Morrison, D.J.; Murphy, K.G.; Zac-Varghese, S.E.K.; Macdougall, K.; Preston, T.; Tedford, Catriona; Finlayson, Graham S. ; Blundell, J.E.; Bell, Jimmy D. ; Thomas, E. Louise ; Mt-Isa, Shahrul; Ashby, Deborah; Gibson, Glen R. ; Kolida, Sofia; S. Dhillo, Waljit; Bloom, S.R.; Morley, Wayne; Clegg, Stuart; Frost, G.S.

In: Gut, Vol. 64, No. 11, 12.2014.

Research output: Contribution to journalArticle

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T1 - Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults

AU - Chambers, E.S.

AU - Viardot, A.

AU - Psichas, A.

AU - Morrison, D.J.

AU - Murphy, K.G.

AU - Zac-Varghese, S.E.K.

AU - Macdougall, K.

AU - Preston, T.

AU - Tedford, Catriona

AU - Finlayson, Graham S.

AU - Blundell, J.E.

AU - Bell, Jimmy D.

AU - Thomas, E. Louise

AU - Mt-Isa, Shahrul

AU - Ashby, Deborah

AU - Gibson, Glen R.

AU - Kolida, Sofia

AU - S. Dhillo, Waljit

AU - Bloom, S.R.

AU - Morley, Wayne

AU - Clegg, Stuart

AU - Frost, G.S.

PY - 2014/12

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N2 - The colonic microbiota ferment dietary fibres, producing short chain fatty acids. Recent evidence suggests that the short chain fatty acid propionate may play an important role in appetite regulation. We hypothesised that colonic delivery of propionate would increase peptide YY (PYY) and glucagon like peptide-1 (GLP-1) secretion in humans, and reduce energy intake and weight gain in overweight adults.To investigate whether propionate promotes PYY and GLP-1 secretion, a primary cultured human colonic cell model was developed. To deliver propionate specifically to the colon, we developed a novel inulin-propionate ester. An acute randomised, controlled cross-over study was used to assess the effects of this inulin-propionate ester on energy intake and plasma PYY and GLP-1 concentrations. The long-term effects of inulin-propionate ester on weight gain were subsequently assessed in a randomised, controlled 24-week study involving 60 overweight adults.Propionate significantly stimulated the release of PYY and GLP-1 from human colonic cells. Acute ingestion of 10 g inulin-propionate ester significantly increased postprandial plasma PYY and GLP-1 and reduced energy intake. Over 24 weeks, 10 g/day inulin-propionate ester supplementation significantly reduced weight gain, intra-abdominal adipose tissue distribution, intrahepatocellular lipid content and prevented the deterioration in insulin sensitivity observed in the inulin-control group.These data demonstrate for the first time that increasing colonic propionate prevents weight gain in overweight adult humans.

AB - The colonic microbiota ferment dietary fibres, producing short chain fatty acids. Recent evidence suggests that the short chain fatty acid propionate may play an important role in appetite regulation. We hypothesised that colonic delivery of propionate would increase peptide YY (PYY) and glucagon like peptide-1 (GLP-1) secretion in humans, and reduce energy intake and weight gain in overweight adults.To investigate whether propionate promotes PYY and GLP-1 secretion, a primary cultured human colonic cell model was developed. To deliver propionate specifically to the colon, we developed a novel inulin-propionate ester. An acute randomised, controlled cross-over study was used to assess the effects of this inulin-propionate ester on energy intake and plasma PYY and GLP-1 concentrations. The long-term effects of inulin-propionate ester on weight gain were subsequently assessed in a randomised, controlled 24-week study involving 60 overweight adults.Propionate significantly stimulated the release of PYY and GLP-1 from human colonic cells. Acute ingestion of 10 g inulin-propionate ester significantly increased postprandial plasma PYY and GLP-1 and reduced energy intake. Over 24 weeks, 10 g/day inulin-propionate ester supplementation significantly reduced weight gain, intra-abdominal adipose tissue distribution, intrahepatocellular lipid content and prevented the deterioration in insulin sensitivity observed in the inulin-control group.These data demonstrate for the first time that increasing colonic propionate prevents weight gain in overweight adult humans.

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DO - 10.1136/gutjnl-2014-307913

M3 - Article

VL - 64

JO - Gut

JF - Gut

SN - 0017-5749

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