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Differential effects of two fermentable carbohydrates on central appetite regulation and body composition

Differential effects of two fermentable carbohydrates on central appetite regulation and body composition
Differential effects of two fermentable carbohydrates on central appetite regulation and body composition

BACKGROUND: Obesity is rising at an alarming rate globally. Different fermentable carbohydrates have been shown to reduce obesity. The aim of the present study was to investigate if two different fermentable carbohydrates (inulin and β-glucan) exert similar effects on body composition and central appetite regulation in high fat fed mice.

METHODOLOGY/PRINCIPAL FINDINGS: Thirty six C57BL/6 male mice were randomized and maintained for 8 weeks on a high fat diet containing 0% (w/w) fermentable carbohydrate, 10% (w/w) inulin or 10% (w/w) β-glucan individually. Fecal and cecal microbial changes were measured using fluorescent in situ hybridization, fecal metabolic profiling was obtained by proton nuclear magnetic resonance ((1)H NMR), colonic short chain fatty acids were measured by gas chromatography, body composition and hypothalamic neuronal activation were measured using magnetic resonance imaging (MRI) and manganese enhanced MRI (MEMRI), respectively, PYY (peptide YY) concentration was determined by radioimmunoassay, adipocyte cell size and number were also measured. Both inulin and β-glucan fed groups revealed significantly lower cumulative body weight gain compared with high fat controls. Energy intake was significantly lower in β-glucan than inulin fed mice, with the latter having the greatest effect on total adipose tissue content. Both groups also showed an increase in the numbers of Bifidobacterium and Lactobacillus-Enterococcus in cecal contents as well as feces. β-Glucan appeared to have marked effects on suppressing MEMRI associated neuronal signals in the arcuate nucleus, ventromedial hypothalamus, paraventricular nucleus, periventricular nucleus and the nucleus of the tractus solitarius, suggesting a satiated state.

CONCLUSIONS/SIGNIFICANCE: Although both fermentable carbohydrates are protective against increased body weight gain, the lower body fat content induced by inulin may be metabolically advantageous. β-Glucan appears to suppress neuronal activity in the hypothalamic appetite centers. Differential effects of fermentable carbohydrates open new possibilities for nutritionally targeting appetite regulation and body composition.

Adipocytes/cytology, Animals, Appetite Regulation, Bifidobacterium/metabolism, Body Composition, Brain Mapping/methods, Carbohydrates/chemistry, Chromatography, Gas/methods, Enterococcus/metabolism, Fermentation, In Situ Hybridization, Fluorescence, Inulin/metabolism, Lactobacillus/metabolism, Magnetic Resonance Imaging/methods, Magnetic Resonance Spectroscopy/methods, Male, Mice, Mice, Inbred C57BL, Obesity/physiopathology, Peptide YY/metabolism, Radioimmunoassay/methods, beta-Glucans/metabolism
1932-6203
1-10
Arora, Tulika
a61f372e-fb97-47ec-84a1-299193ad5653
Loo, Ruey Leng
7177cc94-909e-4385-942d-536dbf2a84cc
Anastasovska, Jelena
229cc944-5a2e-457c-9297-d020ff9cf682
Gibson, Glenn R
24ac4753-4f78-475f-9766-5da179e2ab92
Tuohy, Kieran M
33a7a5da-4abd-4759-b992-2cd45fc65831
Sharma, Raj Kumar
3e3ec480-912b-4f52-9b9d-f28ec5721278
Swann, Jonathan R
7c11a66b-f4b8-4dbf-aa17-ad8b0561b85c
Deaville, Eddie R
b88fc5d7-6eb3-46c4-8201-28ece6708687
Sleeth, Michele L
b281bdca-6ecb-42fd-a294-8880e07d24b5
Thomas, E Louise
5048b967-1f22-4f03-b1f3-41662f0f9a4a
Holmes, Elaine
d3b92a6b-1c3f-4758-b653-ba35afd3f57d
Bell, Jimmy D
7f913309-c2f4-42ba-bcfb-701cd0662e64
Frost, Gary
1be0554f-cb33-4754-a8e7-01015ec03c4b
Arora, Tulika
a61f372e-fb97-47ec-84a1-299193ad5653
Loo, Ruey Leng
7177cc94-909e-4385-942d-536dbf2a84cc
Anastasovska, Jelena
229cc944-5a2e-457c-9297-d020ff9cf682
Gibson, Glenn R
24ac4753-4f78-475f-9766-5da179e2ab92
Tuohy, Kieran M
33a7a5da-4abd-4759-b992-2cd45fc65831
Sharma, Raj Kumar
3e3ec480-912b-4f52-9b9d-f28ec5721278
Swann, Jonathan R
7c11a66b-f4b8-4dbf-aa17-ad8b0561b85c
Deaville, Eddie R
b88fc5d7-6eb3-46c4-8201-28ece6708687
Sleeth, Michele L
b281bdca-6ecb-42fd-a294-8880e07d24b5
Thomas, E Louise
5048b967-1f22-4f03-b1f3-41662f0f9a4a
Holmes, Elaine
d3b92a6b-1c3f-4758-b653-ba35afd3f57d
Bell, Jimmy D
7f913309-c2f4-42ba-bcfb-701cd0662e64
Frost, Gary
1be0554f-cb33-4754-a8e7-01015ec03c4b

Arora, Tulika, Loo, Ruey Leng, Anastasovska, Jelena, Gibson, Glenn R, Tuohy, Kieran M, Sharma, Raj Kumar, Swann, Jonathan R, Deaville, Eddie R, Sleeth, Michele L, Thomas, E Louise, Holmes, Elaine, Bell, Jimmy D and Frost, Gary (2012) Differential effects of two fermentable carbohydrates on central appetite regulation and body composition. PLoS ONE, 7 (8), 1-10, [e43263]. (doi:10.1371/journal.pone.0043263).

Record type: Article

Abstract

BACKGROUND: Obesity is rising at an alarming rate globally. Different fermentable carbohydrates have been shown to reduce obesity. The aim of the present study was to investigate if two different fermentable carbohydrates (inulin and β-glucan) exert similar effects on body composition and central appetite regulation in high fat fed mice.

METHODOLOGY/PRINCIPAL FINDINGS: Thirty six C57BL/6 male mice were randomized and maintained for 8 weeks on a high fat diet containing 0% (w/w) fermentable carbohydrate, 10% (w/w) inulin or 10% (w/w) β-glucan individually. Fecal and cecal microbial changes were measured using fluorescent in situ hybridization, fecal metabolic profiling was obtained by proton nuclear magnetic resonance ((1)H NMR), colonic short chain fatty acids were measured by gas chromatography, body composition and hypothalamic neuronal activation were measured using magnetic resonance imaging (MRI) and manganese enhanced MRI (MEMRI), respectively, PYY (peptide YY) concentration was determined by radioimmunoassay, adipocyte cell size and number were also measured. Both inulin and β-glucan fed groups revealed significantly lower cumulative body weight gain compared with high fat controls. Energy intake was significantly lower in β-glucan than inulin fed mice, with the latter having the greatest effect on total adipose tissue content. Both groups also showed an increase in the numbers of Bifidobacterium and Lactobacillus-Enterococcus in cecal contents as well as feces. β-Glucan appeared to have marked effects on suppressing MEMRI associated neuronal signals in the arcuate nucleus, ventromedial hypothalamus, paraventricular nucleus, periventricular nucleus and the nucleus of the tractus solitarius, suggesting a satiated state.

CONCLUSIONS/SIGNIFICANCE: Although both fermentable carbohydrates are protective against increased body weight gain, the lower body fat content induced by inulin may be metabolically advantageous. β-Glucan appears to suppress neuronal activity in the hypothalamic appetite centers. Differential effects of fermentable carbohydrates open new possibilities for nutritionally targeting appetite regulation and body composition.

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Accepted/In Press date: 18 July 2012
Published date: 29 August 2012
Keywords: Adipocytes/cytology, Animals, Appetite Regulation, Bifidobacterium/metabolism, Body Composition, Brain Mapping/methods, Carbohydrates/chemistry, Chromatography, Gas/methods, Enterococcus/metabolism, Fermentation, In Situ Hybridization, Fluorescence, Inulin/metabolism, Lactobacillus/metabolism, Magnetic Resonance Imaging/methods, Magnetic Resonance Spectroscopy/methods, Male, Mice, Mice, Inbred C57BL, Obesity/physiopathology, Peptide YY/metabolism, Radioimmunoassay/methods, beta-Glucans/metabolism

Identifiers

Local EPrints ID: 439397
URI: http://eprints.soton.ac.uk/id/eprint/439397
ISSN: 1932-6203
PURE UUID: d2ad1c15-def8-4652-a77a-08db07f0d05d
ORCID for Jonathan R Swann: ORCID iD orcid.org/0000-0002-6485-4529

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Date deposited: 21 Apr 2020 16:36
Last modified: 17 Mar 2024 04:00

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Contributors

Author: Tulika Arora
Author: Ruey Leng Loo
Author: Jelena Anastasovska
Author: Glenn R Gibson
Author: Kieran M Tuohy
Author: Raj Kumar Sharma
Author: Eddie R Deaville
Author: Michele L Sleeth
Author: E Louise Thomas
Author: Elaine Holmes
Author: Jimmy D Bell
Author: Gary Frost

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