Behavioural and neuroimaging studies of food reward after bariatric surgery for obesity

Abstract

BACKGROUND Roux-en-Y gastric bypass (RYGB) surgery is the most effective treatment for obesity and has greater efficacy for weight loss than gastric banding (BAND) surgery. The superior weight loss seen after RYGB may result from profoundly different effects on food hedonics and reward brought about by physiological changes secondary to the distinct manipulations of gut anatomy. AIMS To compare body mass index (BMI) matched patients after RYGB or BAND surgery and unoperated controls using comprehensive phenotyping of brain structure and function, eating behaviour and metabolism. METHODS In these cross-sectional studies, un-operated controls and patients after RYGB and BAND surgery had functional and anatomical neuroimaging of food reward systems. Reward responses to food were assessed with a functional magnetic resonance imaging (fMRI) food picture evaluation task. Anatomical differences in grey and white matter were assessed using voxel-based morphometry (VBM) and diffusion tensor imaging (DTI). Eating behaviour, food appeal and palatability, potential mediators, and post-ingestive effects were compared between groups using questionnaires, test meals, food diaries and assay of plasma hormones and metabolites. Surgical patients were compared in both the fasted and fed state, and after administration of the somatostatin analogue, Octreotide, to suppress anorexigenic gut hormone responses after RYGB.

RESULTS Obese patients after RYGB had healthier gut-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 to BAND patients and/or BMI-matched unoperated controls. These differences were not explicable by differences in hunger or psychological traits between the surgical groups, or by differences in brain structure as measured by VBM and DTI. However anorexigenic plasma gut hormones (GLP-1 and PYY), plasma bile acids and symptoms of dumping syndrome were increased in RYGB patients. Octreotide increased nucleus accumbens activation to food pictures, increased food appeal and decreased post-meal satiety in patients after RYGB, but not BAND surgery. The preliminary nature of this small study precludes extensive interpretation especially of the difference between surgical groups. Patients in the operated groups (RYGB and BAND) had lower grey matter density in areas involved in reward processing, including the amygdala, nucleus accumbens and hippocampus compared to BMI-matched controls. There was no difference between the groups in white matter tract integrity. CONCLUSIONS Identification of these differences in the gut-brain axis and hence food hedonic responses as a result of altered gut anatomy/physiology provides a novel explanation for the more favorable long-term weight loss seen after RYGB than BAND surgery. This supports targeting of gut-brain reward systems for future treatments of obesity.