Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding

Samantha Scholtz; Alexander D. Miras; Navpreet Chhina; Christina G. Prechtl; Michelle L. Sleeth; Norlida M. Daud; Nurhafzan A. Ismail; Giuliana Durighel; Ahmed R. Ahmed; Torsten Olbers; Royce Vincent; Jamshid Alaghband-Zadeh; Mohammad A. Ghatei; Adam D. Waldman; Gary S. Frost; Jimmy D. Bell; Carel W. le Roux; Anthony P. Goldstone

doi:10.1136/gutjnl-2013-305008

Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding

Samantha Scholtz, Alexander D. Miras, Navpreet Chhina, Christina G. Prechtl, Michelle L. Sleeth, Norlida M. Daud, Nurhafzan A. Ismail, Giuliana Durighel, Ahmed R. Ahmed, Torsten Olbers, Royce Vincent, Jamshid Alaghband-Zadeh, Mohammad A. Ghatei, Adam D. Waldman, Gary S. Frost, Jimmy D. Bell, Carel W. le Roux, Anthony P. Goldstone^*

^*Corresponding author for this work

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

204 Citations (Scopus)

Abstract

Objectives: Roux-en-Y gastric bypass (RYGB) has greater efficacy for weight loss in obese patients than gastric banding (BAND) surgery. We hypothesise that this may result from different effects on food hedonics via physiological changes secondary to distinct gut anatomy manipulations.

Design: We used functional MRI, eating behaviour and hormonal phenotyping to compare body mass index (BMI)-matched unoperated controls and patients after RYGB and BAND surgery for obesity.

Results: Obese patients after RYGB had lower brain-hedonic responses to food than patients after BAND surgery. RYGB patients had lower activation than BAND patients in brain reward systems, particularly to high-calorie foods, including the orbitofrontal cortex, amygdala, caudate nucleus, nucleus accumbens and hippocampus. This was associated with lower palatability and appeal of high-calorie foods and healthier eating behaviour, including less fat intake, in RYGB compared with BAND patients and/or BMI-matched unoperated controls. These differences were not explicable by differences in hunger or psychological traits between the surgical groups, but anorexigenic plasma gut hormones (GLP-1 and PYY), plasma bile acids and symptoms of dumping syndrome were increased in RYGB patients.

Conclusions: The identification of these differences in food hedonic responses as a result of altered gut anatomy/physiology provides a novel explanation for the more favourable long-term weight loss seen after RYGB than after BAND surgery, highlighting the importance of the gut-brain axis in the control of reward-based eating behaviour.

Original language	English
Pages (from-to)	891-902
Number of pages	12
Journal	Gut
Volume	63
Issue number	6
DOIs	https://doi.org/10.1136/gutjnl-2013-305008
Publication status	Published - Jun 2014

Keywords

HIGH-CALORIE FOODS
BARIATRIC SURGERY
WEIGHT-LOSS
REWARD
ACTIVATION
SATIETY
HUMANS
BILE
MODULATION
STIMULUS

UN SDGs

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

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10.1136/gutjnl-2013-305008

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Scholtz, S., Miras, A. D., Chhina, N., Prechtl, C. G., Sleeth, M. L., Daud, N. M., Ismail, N. A., Durighel, G., Ahmed, A. R., Olbers, T., Vincent, R., Alaghband-Zadeh, J., Ghatei, M. A., Waldman, A. D., Frost, G. S., Bell, J. D., le Roux, C. W., & Goldstone, A. P. (2014). Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding. Gut, 63(6), 891-902. https://doi.org/10.1136/gutjnl-2013-305008

@article{dc078b6e7048402dbbce77be0f4f8646,

title = "Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding",

abstract = "Objectives: Roux-en-Y gastric bypass (RYGB) has greater efficacy for weight loss in obese patients than gastric banding (BAND) surgery. We hypothesise that this may result from different effects on food hedonics via physiological changes secondary to distinct gut anatomy manipulations.Design: We used functional MRI, eating behaviour and hormonal phenotyping to compare body mass index (BMI)-matched unoperated controls and patients after RYGB and BAND surgery for obesity.Results: Obese patients after RYGB had lower brain-hedonic responses to food than patients after BAND surgery. RYGB patients had lower activation than BAND patients in brain reward systems, particularly to high-calorie foods, including the orbitofrontal cortex, amygdala, caudate nucleus, nucleus accumbens and hippocampus. This was associated with lower palatability and appeal of high-calorie foods and healthier eating behaviour, including less fat intake, in RYGB compared with BAND patients and/or BMI-matched unoperated controls. These differences were not explicable by differences in hunger or psychological traits between the surgical groups, but anorexigenic plasma gut hormones (GLP-1 and PYY), plasma bile acids and symptoms of dumping syndrome were increased in RYGB patients.Conclusions: The identification of these differences in food hedonic responses as a result of altered gut anatomy/physiology provides a novel explanation for the more favourable long-term weight loss seen after RYGB than after BAND surgery, highlighting the importance of the gut-brain axis in the control of reward-based eating behaviour.",

keywords = "HIGH-CALORIE FOODS, BARIATRIC SURGERY, WEIGHT-LOSS, REWARD, ACTIVATION, SATIETY, HUMANS, BILE, MODULATION, STIMULUS",

author = "Samantha Scholtz and Miras, {Alexander D.} and Navpreet Chhina and Prechtl, {Christina G.} and Sleeth, {Michelle L.} and Daud, {Norlida M.} and Ismail, {Nurhafzan A.} and Giuliana Durighel and Ahmed, {Ahmed R.} and Torsten Olbers and Royce Vincent and Jamshid Alaghband-Zadeh and Ghatei, {Mohammad A.} and Waldman, {Adam D.} and Frost, {Gary S.} and Bell, {Jimmy D.} and {le Roux}, {Carel W.} and Goldstone, {Anthony P.}",

year = "2014",

month = jun,

doi = "10.1136/gutjnl-2013-305008",

language = "English",

volume = "63",

pages = "891--902",

journal = "Gut",

issn = "0017-5749",

publisher = "BMJ Publishing Group",

number = "6",

}

Scholtz, S, Miras, AD, Chhina, N, Prechtl, CG, Sleeth, ML, Daud, NM, Ismail, NA, Durighel, G, Ahmed, AR, Olbers, T, Vincent, R, Alaghband-Zadeh, J, Ghatei, MA, Waldman, AD, Frost, GS, Bell, JD, le Roux, CW & Goldstone, AP 2014, 'Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding', Gut, vol. 63, no. 6, pp. 891-902. https://doi.org/10.1136/gutjnl-2013-305008

TY - JOUR

T1 - Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding

AU - Scholtz, Samantha

AU - Miras, Alexander D.

AU - Chhina, Navpreet

AU - Prechtl, Christina G.

AU - Sleeth, Michelle L.

AU - Daud, Norlida M.

AU - Ismail, Nurhafzan A.

AU - Durighel, Giuliana

AU - Ahmed, Ahmed R.

AU - Olbers, Torsten

AU - Vincent, Royce

AU - Alaghband-Zadeh, Jamshid

AU - Ghatei, Mohammad A.

AU - Waldman, Adam D.

AU - Frost, Gary S.

AU - Bell, Jimmy D.

AU - le Roux, Carel W.

AU - Goldstone, Anthony P.

PY - 2014/6

Y1 - 2014/6

N2 - Objectives: Roux-en-Y gastric bypass (RYGB) has greater efficacy for weight loss in obese patients than gastric banding (BAND) surgery. We hypothesise that this may result from different effects on food hedonics via physiological changes secondary to distinct gut anatomy manipulations.Design: We used functional MRI, eating behaviour and hormonal phenotyping to compare body mass index (BMI)-matched unoperated controls and patients after RYGB and BAND surgery for obesity.Results: Obese patients after RYGB had lower brain-hedonic responses to food than patients after BAND surgery. RYGB patients had lower activation than BAND patients in brain reward systems, particularly to high-calorie foods, including the orbitofrontal cortex, amygdala, caudate nucleus, nucleus accumbens and hippocampus. This was associated with lower palatability and appeal of high-calorie foods and healthier eating behaviour, including less fat intake, in RYGB compared with BAND patients and/or BMI-matched unoperated controls. These differences were not explicable by differences in hunger or psychological traits between the surgical groups, but anorexigenic plasma gut hormones (GLP-1 and PYY), plasma bile acids and symptoms of dumping syndrome were increased in RYGB patients.Conclusions: The identification of these differences in food hedonic responses as a result of altered gut anatomy/physiology provides a novel explanation for the more favourable long-term weight loss seen after RYGB than after BAND surgery, highlighting the importance of the gut-brain axis in the control of reward-based eating behaviour.

AB - Objectives: Roux-en-Y gastric bypass (RYGB) has greater efficacy for weight loss in obese patients than gastric banding (BAND) surgery. We hypothesise that this may result from different effects on food hedonics via physiological changes secondary to distinct gut anatomy manipulations.Design: We used functional MRI, eating behaviour and hormonal phenotyping to compare body mass index (BMI)-matched unoperated controls and patients after RYGB and BAND surgery for obesity.Results: Obese patients after RYGB had lower brain-hedonic responses to food than patients after BAND surgery. RYGB patients had lower activation than BAND patients in brain reward systems, particularly to high-calorie foods, including the orbitofrontal cortex, amygdala, caudate nucleus, nucleus accumbens and hippocampus. This was associated with lower palatability and appeal of high-calorie foods and healthier eating behaviour, including less fat intake, in RYGB compared with BAND patients and/or BMI-matched unoperated controls. These differences were not explicable by differences in hunger or psychological traits between the surgical groups, but anorexigenic plasma gut hormones (GLP-1 and PYY), plasma bile acids and symptoms of dumping syndrome were increased in RYGB patients.Conclusions: The identification of these differences in food hedonic responses as a result of altered gut anatomy/physiology provides a novel explanation for the more favourable long-term weight loss seen after RYGB than after BAND surgery, highlighting the importance of the gut-brain axis in the control of reward-based eating behaviour.

KW - HIGH-CALORIE FOODS

KW - BARIATRIC SURGERY

KW - WEIGHT-LOSS

KW - REWARD

KW - ACTIVATION

KW - SATIETY

KW - HUMANS

KW - BILE

KW - MODULATION

KW - STIMULUS

U2 - 10.1136/gutjnl-2013-305008

DO - 10.1136/gutjnl-2013-305008

M3 - Article

SN - 0017-5749

VL - 63

SP - 891

EP - 902

JO - Gut

JF - Gut

IS - 6

ER -

Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding

Abstract

Keywords

UN SDGs

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