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Cited by 121Bariatric Surgery and OutcomesRegulation of Appetite and ObesityPharmacology and Obesity Treatment

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Link Between Increased Satiety Gut Hormones and Reduced Food Reward After Gastric Bypass Surgery for Obesity

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Goldstone, Anthony P., Miras, Alexander D., Scholtz, Samantha, Jackson, Sabrina, Neff, Karl J., Pénicaud, Luc, Geoghegan, Justin, Chhina, Navpreet, Durighel, Giuliana, Bell, Jimmy D., Meillon, Sophie, le Roux, Carel W.·2016·The Journal of Clinical Endocrinology & Metabolism
DOI 10.1210/jc.2015-2665PMC PMC4880130
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Abstract

CONTEXT: Roux-en-Y gastric bypass (RYGB) surgery is an effective long-term intervention for weight loss maintenance, reducing appetite, and also food reward, via unclear mechanisms. OBJECTIVE: To investigate the role of elevated satiety gut hormones after RYGB, we examined food hedonic-reward responses after their acute post-prandial suppression. DESIGN: These were randomized, placebo-controlled, double-blind, crossover experimental medicine studies. PATIENTS: Two groups, more than 5 months after RYGB for obesity (n = 7-11), compared with nonobese controls (n = 10), or patients after gastric banding (BAND) surgery (n = 9) participated in the studies. INTERVENTION: Studies were performed after acute administration of the somatostatin analog octreotide or saline. In one study, patients after RYGB, and nonobese controls, performed a behavioral progressive ratio task for chocolate sweets. In another study, patients after RYGB, and controls after BAND surgery, performed a functional magnetic resonance imaging food picture evaluation task. MAIN OUTCOME MEASURES: Octreotide increased both appetitive food reward (breakpoint) in the progressive ratio task (n = 9), and food appeal (n = 9) and reward system blood oxygen level-dependent signal (n = 7) in the functional magnetic resonance imaging task, in the RYGB group, but not in the control groups. RESULTS: Octreotide suppressed postprandial plasma peptide YY, glucagon-like peptide-1, and fibroblast growth factor-19 after RYGB. The reduction in plasma peptide YY with octreotide positively correlated with the increase in brain reward system blood oxygen level-dependent signal in RYGB/BAND subjects, with a similar trend for glucagon-like peptide-1. CONCLUSIONS: Enhanced satiety gut hormone responses after RYGB may be a causative mechanism by which anatomical alterations of the gut in obesity surgery modify behavioral and brain reward responses to food.

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Figure 1. Study protocols. A, Progressive ratio task. B, Functional MRI food evaluation study. Note that the PRT lasted 10 minutes and all participants finished the task within this time period. The time interval between the end of the PRT and the +80-minute blood sample ranged from 9 to 13 minutes. AMV, auditory-motor-visual; BP, blood pressure; MRI, magnetic resonance imaging.
Figure 1. Study protocols. A, Progressive ratio task. B, Functional MRI food evaluation study. Note that the PRT lasted 10 minutes and all participants finished the task within this time period. The time interval between the end of the PRT and the +80-minute blood sample ranged from 9 to 13 minutes. AMV, auditory-motor-visual; BP, blood pressure; MRI, magnetic resonance imaging.CC BY · PubMed Central
Figure 2. Octreotide suppressed postprandial plasma gut hormones in progressive ratio task. A, Plasma glucose. Octreotide significantly increased plasma glucose in patients after RYGB (mean difference [95% CI] 0.6 [0.2, 1.1] mmol/L, F[1, 19] = 7.84, P = .011, Cohen's d = 0.84) but not in controls (0.3 [−0.2, 0.8] mmol/L, F[1, 19] = 1.25, P = .28, Cohen's d = 0.00). To convert millimoles per liter to milligrams per deciliter, multiply by 18.01. B, Serum insulin. Octreotide significantly decreased serum insulin in patients after RYGB (mean difference [95% CI] −22.3 [−27.7, −16.9] mU/L, F[1, 19] = 74.88, P < .001, Cohen's d = 2.05) but not in controls (−4.0 [−9.6, 1.7] mU/L, F[1, 19] = 2.15, P = .10, Cohen's d = 1.08). To convert milliunits per liter to picomoles per liter, multiply by 7.175. C, Plasma GLP-1. Octreotide significantly decreased plasma total GLP-1 both in patients after RYGB (mean difference [95% CI] −18.7 [−27.7, −9.6] pmol/L, F[1, 18] = 18.81, P < .001, Cohen's d = 0.98) and in controls (−11.0 [−20.0, −1.93] pmol/L, F[1, 8] = 6.50, P = .020, Cohen's d = 1.49). D, Plasma PYY. Octreotide significantly decreased plasma total PYY in patients after RYGB (mean difference [95% CI] −143.8 [−193.3, −94.4] pg/mL, F[1, 19] = 37.08, P < .001, Cohen's d = 1.48) but not in controls (−30.0 [−81.8, 21.9] pg/mL, F[1, 19] = 1.46, P = .24, Cohen's d = 0.62). To convert picograms per milliliter to picomoles per liter, multiply by 0.25. E, Plasma FGF19. Octreotide significantly decreased plasma FGF19 in patients after RYGB (mean difference [95% CI] −36.6 [−59.4, −13.7] pg/mL, F[1, 19] = 11.23, P = .003, Cohen's d = 0.91) but not in controls (−12.1 [−36.1, 11.9] pg/mL, F[1, 19] = 1.12, P = .30, Cohen's d = 0.47). Data represent mean ± SEM (n = 11 per group except RYGB group, GLP-1, n = 10). White bars, saline; black bars, octreotide. *, P < .05, ***, P < .001 with post hoc Fisher's LSD test. For statistics of repeated-measures ANOVA for effects of group, treatment, and group × treatment interaction, see Supplemental Table 2.
Figure 2. Octreotide suppressed postprandial plasma gut hormones in progressive ratio task. A, Plasma glucose. Octreotide significantly increased plasma glucose in patients after RYGB (mean difference [95% CI] 0.6 [0.2, 1.1] mmol/L, F[1, 19] = 7.84, P = .011, Cohen's d = 0.84) but not in controls (0.3 [−0.2, 0.8] mmol/L, F[1, 19] = 1.25, P = .28, Cohen's d = 0.00). To convert millimoles per liter to milligrams per deciliter, multiply by 18.01. B, Serum insulin. Octreotide significantly decreased serum insulin in patients after RYGB (mean difference [95% CI] −22.3 [−27.7, −16.9] mU/L, F[1, 19] = 74.88, P < .001, Cohen's d = 2.05) but not in controls (−4.0 [−9.6, 1.7] mU/L, F[1, 19] = 2.15, P = .10, Cohen's d = 1.08). To convert milliunits per liter to picomoles per liter, multiply by 7.175. C, Plasma GLP-1. Octreotide significantly decreased plasma total GLP-1 both in patients after RYGB (mean difference [95% CI] −18.7 [−27.7, −9.6] pmol/L, F[1, 18] = 18.81, P < .001, Cohen's d = 0.98) and in controls (−11.0 [−20.0, −1.93] pmol/L, F[1, 8] = 6.50, P = .020, Cohen's d = 1.49). D, Plasma PYY. Octreotide significantly decreased plasma total PYY in patients after RYGB (mean difference [95% CI] −143.8 [−193.3, −94.4] pg/mL, F[1, 19] = 37.08, P < .001, Cohen's d = 1.48) but not in controls (−30.0 [−81.8, 21.9] pg/mL, F[1, 19] = 1.46, P = .24, Cohen's d = 0.62). To convert picograms per milliliter to picomoles per liter, multiply by 0.25. E, Plasma FGF19. Octreotide significantly decreased plasma FGF19 in patients after RYGB (mean difference [95% CI] −36.6 [−59.4, −13.7] pg/mL, F[1, 19] = 11.23, P = .003, Cohen's d = 0.91) but not in controls (−12.1 [−36.1, 11.9] pg/mL, F[1, 19] = 1.12, P = .30, Cohen's d = 0.47). Data represent mean ± SEM (n = 11 per group except RYGB group, GLP-1, n = 10). White bars, saline; black bars, octreotide. *, P < .05, ***, P < .001 with post hoc Fisher's LSD test. For statistics of repeated-measures ANOVA for effects of group, treatment, and group × treatment interaction, see Supplemental Table 2.CC BY · PubMed Central
Figure 3. Octreotide increased food reward responses in progressive ratio task. Octreotide significantly increased the total number of clicks (breakpoint) in patients after RYGB (mean difference [95% CI] 503 [218, 788], F[1, 19] = 13.66, P = .002, Cohen's d = 0.62) but not in controls (effect size −1 [−300, 298], F[1, 19]=0.00, P = .99, Cohen's d = 0.00). Overall ANOVA: group (between subject), F(1, 19) = 1.53, P = .23; treatment (within subject), F(1, 19) = 6.47 P = .02; group × treatment interaction, F(1, 19) = 6.54, P = .02.
Figure 3. Octreotide increased food reward responses in progressive ratio task. Octreotide significantly increased the total number of clicks (breakpoint) in patients after RYGB (mean difference [95% CI] 503 [218, 788], F[1, 19] = 13.66, P = .002, Cohen's d = 0.62) but not in controls (effect size −1 [−300, 298], F[1, 19]=0.00, P = .99, Cohen's d = 0.00). Overall ANOVA: group (between subject), F(1, 19) = 1.53, P = .23; treatment (within subject), F(1, 19) = 6.47 P = .02; group × treatment interaction, F(1, 19) = 6.54, P = .02.CC BY · PubMed Central
Figure 4. Octreotide suppressed postprandial plasma gut hormones in fMRI food evaluation study. A, Plasma glucose. Octreotide significantly increased plasma glucose in patients after RYGB (mean difference [95% CI] 2.2 [0.9, 3.5] mmol/L, F[1, 16] = 12.78, P = .003, Cohen's d = 2.31) but not in patients after BAND (0.5 [−0.8, 1.8] mmol/L, F[1, 16] = 0.55, P = .47, Cohen's d = 0.48). To convert millimoles per liter to milligrams per deciliter, multiply by 18.01. B, Serum insulin. Octreotide did not have a significant effect on serum insulin in patients after RYGB (mean difference [95% CI] −1.6 [−5.1, 1.9] mU/L, F[1, 16] = 0.94, P = .35, Cohen's d = 0.26) or in patients after BAND (−0.2 [−3.7, 3.3] mU/L, F[1, 16] = 0.01, P = .92, Cohen's d = 0.11). To convert milliunits per liter to picomoles per liter, multiply by 7.175. C, Plasma GLP-1. Octreotide significantly decreased plasma total GLP-1 in patients after RYGB (mean difference [95% CI] −22.6 [−27.3, −17.8] pmol/L, F[1, 16] = 102.16, P < .001, Cohen's d = 1.80), with a significantly smaller decrease in patients after BAND (−10.4 [−15.1, −5.7] pmol/L, F[1, 16] = 21.74, P < .001, Cohen's d = 1.90). D, Plasma PYY. Octreotide significantly decreased plasma total PYY in patients after RYGB (mean difference [95% CI] −146.8 [−203.5, −90.1] pg/mL, F[1, 16] = 30.12, P < .001, Cohen's d = 0.95), with a significantly smaller decrease in patients after BAND (−57.6 [−114.3, −0.88] pg/mL, F[1, 16] = 4.63, P = .047, Cohen's d = 1.95). To convert picograms per milliliter to picomoles liter, multiply by 0.25. E, Plasma FGF19. Octreotide significantly decreased plasma FGF19 in patients after RYGB (mean difference [95% CI] −28.5 [−50.4, −6.5] pg/mL, F[1, 16] = 7.54, P = .014, Cohen's d = 0.40) but not in patients after BAND (−12.1 [−36.1, 11.9] pg/mL, F[1, 16] = 0.02, P = .90, Cohen's d = 0.08). Data represent mean ± SEM (n = 9 per group). White bars, saline; black bars, octreotide. *, P < .05, ***, P < .001 with post hoc Fisher's LSD test. For statistics of repeated-measures ANOVA for effects of group, treatment, and interaction, see Supplemental Table 4.
Figure 4. Octreotide suppressed postprandial plasma gut hormones in fMRI food evaluation study. A, Plasma glucose. Octreotide significantly increased plasma glucose in patients after RYGB (mean difference [95% CI] 2.2 [0.9, 3.5] mmol/L, F[1, 16] = 12.78, P = .003, Cohen's d = 2.31) but not in patients after BAND (0.5 [−0.8, 1.8] mmol/L, F[1, 16] = 0.55, P = .47, Cohen's d = 0.48). To convert millimoles per liter to milligrams per deciliter, multiply by 18.01. B, Serum insulin. Octreotide did not have a significant effect on serum insulin in patients after RYGB (mean difference [95% CI] −1.6 [−5.1, 1.9] mU/L, F[1, 16] = 0.94, P = .35, Cohen's d = 0.26) or in patients after BAND (−0.2 [−3.7, 3.3] mU/L, F[1, 16] = 0.01, P = .92, Cohen's d = 0.11). To convert milliunits per liter to picomoles per liter, multiply by 7.175. C, Plasma GLP-1. Octreotide significantly decreased plasma total GLP-1 in patients after RYGB (mean difference [95% CI] −22.6 [−27.3, −17.8] pmol/L, F[1, 16] = 102.16, P < .001, Cohen's d = 1.80), with a significantly smaller decrease in patients after BAND (−10.4 [−15.1, −5.7] pmol/L, F[1, 16] = 21.74, P < .001, Cohen's d = 1.90). D, Plasma PYY. Octreotide significantly decreased plasma total PYY in patients after RYGB (mean difference [95% CI] −146.8 [−203.5, −90.1] pg/mL, F[1, 16] = 30.12, P < .001, Cohen's d = 0.95), with a significantly smaller decrease in patients after BAND (−57.6 [−114.3, −0.88] pg/mL, F[1, 16] = 4.63, P = .047, Cohen's d = 1.95). To convert picograms per milliliter to picomoles liter, multiply by 0.25. E, Plasma FGF19. Octreotide significantly decreased plasma FGF19 in patients after RYGB (mean difference [95% CI] −28.5 [−50.4, −6.5] pg/mL, F[1, 16] = 7.54, P = .014, Cohen's d = 0.40) but not in patients after BAND (−12.1 [−36.1, 11.9] pg/mL, F[1, 16] = 0.02, P = .90, Cohen's d = 0.08). Data represent mean ± SEM (n = 9 per group). White bars, saline; black bars, octreotide. *, P < .05, ***, P < .001 with post hoc Fisher's LSD test. For statistics of repeated-measures ANOVA for effects of group, treatment, and interaction, see Supplemental Table 4.CC BY · PubMed Central
Figure 5. Effect of octreotide on hedonic and brain reward system responses in fMRI food evaluation task after RYGB and BAND. A and B, Octreotide increased food appeal ratings in patients after RYGB (mean difference [95% CI] 0.35 [0.01, 0.70], F[1, 8] = 5.48, P = .047, Cohen's d = 0.43) (A) but not BAND (mean difference [95% CI] 0.049 [−0.38, 0.48], F[1, 8] = 0.07, P = .80, Cohen's d = 0.07) (B). C and D, Octreotide significantly increased average BOLD signal (percentage) to any food picture averaged across all four fROIs (nucleus accumbens, caudate, anterior insula, amygdala) in patients after RYGB (mean difference [95% CI] 0.062 [0.003, 0.122], F[1, 6] = 6.54, P = .043, Cohen's d = 0.77) (C) but not BAND (mean difference [95% CI] 0.047 [−0.051, 0.146], F[1, 8] = 1.21, P = .30, Cohen's d = 0.68) (D). E and F, Octreotide significantly increased average BOLD signal (percentage) to any food picture in the nucleus accumbens alone in patients after RYGB (0.102 [0.023, 0.180], F[1, 6] = 10.11, P = .019, Cohen's d = 0.79) (E) but not BAND (mean difference [95% CI] 0.069 [−0.037, 0.174], F[1, 8] = 2.27, P = .17, Cohen's d = 0.82) (F). Analysis from repeated-measures ANOVA performed separately in each group, RYGB (n = 7, except food appeal rating, n = 9) or BAND (n = 9), with treatment (octreotide or saline) and energy density of food pictures (high or low) as within-subject factors. There was no significant effect of food picture energy density or energy density × treatment interaction for any fROI in either group. *, P < .05, octreotide vs saline with post hoc Fisher's LSD test. For statistics of repeated-measures ANOVA for effects of group, treatment, and interaction, see Supplemental Table 5.
Figure 5. Effect of octreotide on hedonic and brain reward system responses in fMRI food evaluation task after RYGB and BAND. A and B, Octreotide increased food appeal ratings in patients after RYGB (mean difference [95% CI] 0.35 [0.01, 0.70], F[1, 8] = 5.48, P = .047, Cohen's d = 0.43) (A) but not BAND (mean difference [95% CI] 0.049 [−0.38, 0.48], F[1, 8] = 0.07, P = .80, Cohen's d = 0.07) (B). C and D, Octreotide significantly increased average BOLD signal (percentage) to any food picture averaged across all four fROIs (nucleus accumbens, caudate, anterior insula, amygdala) in patients after RYGB (mean difference [95% CI] 0.062 [0.003, 0.122], F[1, 6] = 6.54, P = .043, Cohen's d = 0.77) (C) but not BAND (mean difference [95% CI] 0.047 [−0.051, 0.146], F[1, 8] = 1.21, P = .30, Cohen's d = 0.68) (D). E and F, Octreotide significantly increased average BOLD signal (percentage) to any food picture in the nucleus accumbens alone in patients after RYGB (0.102 [0.023, 0.180], F[1, 6] = 10.11, P = .019, Cohen's d = 0.79) (E) but not BAND (mean difference [95% CI] 0.069 [−0.037, 0.174], F[1, 8] = 2.27, P = .17, Cohen's d = 0.82) (F). Analysis from repeated-measures ANOVA performed separately in each group, RYGB (n = 7, except food appeal rating, n = 9) or BAND (n = 9), with treatment (octreotide or saline) and energy density of food pictures (high or low) as within-subject factors. There was no significant effect of food picture energy density or energy density × treatment interaction for any fROI in either group. *, P < .05, octreotide vs saline with post hoc Fisher's LSD test. For statistics of repeated-measures ANOVA for effects of group, treatment, and interaction, see Supplemental Table 5.CC BY · PubMed Central
Figure 6. Greater suppression of plasma PYY and GLP-1 with octreotide is associated with greater increase in brain reward system response in fMRI food evaluation task after bariatric surgery. The magnitude of the increase in BOLD signal (percentage) averaged across the four fROIs (nucleus accumbens, caudate, anterior insula, amygdala) to any food picture (high energy or low energy vs objects) with octreotide (delta octreotide-saline) was positively correlated with the decrease in plasma concentration of PYY with octreotide (delta saline-octreotide) (A), with a similar trend for plasma concentrations of GLP-1 (B), independent of the surgical group. r represents Pearson correlation coefficient. Open circles represent patients after BAND (n = 9) and filled circles patients after RYGB (n = 7). Results for PYY are displayed as log10 scale because data were not normally distributed. One RYGB subject with a decrease in plasma PYY after octreotide of 401.3 pg/mL was an outlier (> 2 SD) in these analyses. The relationship between delta BOLD signal and delta plasma PYY remained significant when excluding this subject (r[14] = +0.54, P = .036).
Figure 6. Greater suppression of plasma PYY and GLP-1 with octreotide is associated with greater increase in brain reward system response in fMRI food evaluation task after bariatric surgery. The magnitude of the increase in BOLD signal (percentage) averaged across the four fROIs (nucleus accumbens, caudate, anterior insula, amygdala) to any food picture (high energy or low energy vs objects) with octreotide (delta octreotide-saline) was positively correlated with the decrease in plasma concentration of PYY with octreotide (delta saline-octreotide) (A), with a similar trend for plasma concentrations of GLP-1 (B), independent of the surgical group. r represents Pearson correlation coefficient. Open circles represent patients after BAND (n = 9) and filled circles patients after RYGB (n = 7). Results for PYY are displayed as log10 scale because data were not normally distributed. One RYGB subject with a decrease in plasma PYY after octreotide of 401.3 pg/mL was an outlier (> 2 SD) in these analyses. The relationship between delta BOLD signal and delta plasma PYY remained significant when excluding this subject (r[14] = +0.54, P = .036).CC BY · PubMed Central

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Metadata

Authors
Goldstone, A. P., Miras, A. D., Scholtz, S., Jackson, S., Neff, K. J., Pénicaud, L., Geoghegan, J., Chhina, N., Durighel, G., Bell, J. D., Meillon, S., & le Roux, C. W.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • University College Dublin (IE)
Corresponding author
Goldstone, Anthony P.
ORCID
Venue
The Journal of Clinical Endocrinology & Metabolism
Publisher
The Endocrine Society
Published
2016-02
Volume
101
Issue
2
Pages
599-609
ISSN
  • 0021-972X (ISSN-L)
  • 1945-7197
DOI
10.1210/jc.2015-2665
PMC
PMC4880130
OpenAlex
W2177986650
Cited by
121
References
46
Citations by year
2026: 8 · 2025: 6 · 2024: 6 · 2023: 12 · 2022: 12 · 2021: 16 · 2020: 14 · 2019: 8 · 2018: 18 · 2017: 12 · 2016: 8
FWCI
13.10
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • The Journal of Clinical Endocrinology & Metabolism (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • WestminsterResearch (University of Westminster) (acceptedVersion)
  • WestminsterResearch (University of Westminster) (acceptedVersion, cc-by)
  • HAL (submittedVersion)
  • Spiral (Imperial College London) (submittedVersion, cc-by)
Funders
  • Wellcome Trust (087745/Z/08/Z)
  • Imperial College Healthcare Charity
  • National Institute for Health and Care Research
  • Imperial College London
  • Imperial College Healthcare NHS Trust
  • Science Foundation Ireland (12/YI/B2480)
  • Medical Research Council
  • NIHR Imperial Biomedical Research Centre
Topics
  • Health Sciences › Medicine › Surgery › Bariatric Surgery and Outcomes
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
  • Health Sciences › Medicine › Pharmacology (medical) › Pharmacology and Obesity Treatment
Keywords
Roux-en-Y gastric bypass, bariatric surgery, food reward, octreotide, somatostatin analogues, peptide YY, glucagon-like peptide-1, FGF19, brain reward system, gastric banding
MeSH terms
Adult, Appetite, Cacao, Double-Blind Method, Female, Food, Gastrointestinal Hormones, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Obesity, Oxygen, Photic Stimulation, Reward, Satiation, Octreotide, Gastric Bypass, Cross-Over Studies

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