Improvement in Uncontrolled Eating Behavior after Laparoscopic Sleeve Gastrectomy Is Associated with Alterations in the Brain–Gut–Microbiome Axis in Obese Women

Abstract

Background: Bariatric surgery is proven to change eating behavior and cause sustained weight loss, yet the exact mechanisms underlying these changes are not clearly understood. We explore this in a novel way by examining how bariatric surgery affects the brain–gut–microbiome (BGM) axis. Methods: Patient demographics, serum, stool, eating behavior questionnaires, and brain magnetic resonance imaging (MRI) were collected before and 6 months after laparoscopic sleeve gastrectomy (LSG). Differences in eating behavior and brain morphology and resting-state functional connectivity in core reward regions were correlated with serum metabolite and 16S microbiome data. Results: LSG resulted in significant weight loss and improvement in maladaptive eating behaviors as measured by the Yale Food Addiction Scale (YFAS). Brain imaging showed a significant increase in brain volume of the putamen (p.adj < 0.05) and amygdala (p.adj < 0.05) after surgery. Resting-state connectivity between the precuneus and the putamen was significantly reduced after LSG (p.adj = 0.046). This change was associated with YFAS symptom count. Bacteroides, Ruminococcus, and Holdemanella were associated with reduced connectivity between these areas. Metabolomic profiles showed a positive correlation between this brain connection and a phosphatidylcholine metabolite. Conclusion: Bariatric surgery modulates brain networks that affect eating behavior, potentially through effects on the gut microbiota and its metabolites.

Early life adversity predicts brain-gut alterations associated with increased stress and mood

“…These have been previously described in great detail in recently published papers ( Dong et al, 2020a , 2020b bib_Dong_et_al_2020a bib_Dong_et_al_2020b ; Osadchiy et al, 2020 ). Participants were given “at home collection kits” which consisted of a standard laboratory supplies such as collection hat over the commode and a urine cup to pack the fresh stool.…”

Do Gut Microbes Taste?

“…This change in eating behavior was not associated with changes in taste sensitivity, however, suggesting other unknown mechanisms. Finally, changes in microbiome post bariatric surgery have been associated with brain connectivity between precuneus and putamen regions of the brain that are involved in addictive behavior [ 148 ]. Therefore, the dramatic shift in the gut microbiota composition due to bariatric surgery may contribute to changes in taste and food cues in core regions of the brain similar to those seen in addiction behavior; however, this hypothesis needs to be investigated.…”

Metabolic and Neural Mechanisms Underlying the Associations Between Gut Bacteroides and Cognition: A Large-Scale Functional Network Connectivity Study

“…There have been three resting-state fMRI precedents attempting to uncover the relationship between gut Bacteroides and brain functional connectivity ( Curtis et al, 2019 ; Strandwitz et al, 2019 ; Dong et al, 2020 ). In those earlier studies, however, functional connectivity was measured using a classical hypothesis-driven seed-based approach, which is limited in its ability to capture functional connectivity patterns globally since the seed regions must be selected ad hoc .…”

“…A resting-state functional magnetic resonance imaging (fMRI) study demonstrated that relative abundance of Bacteroides was negatively correlated with regional spontaneous neural activity of the cerebellum in patients with amnestic mild cognitive impairment ( Liu et al, 2021 ). By leveraging seed-based functional connectivity approaches, researchers have revealed associations of gut Bacteroides with reduced connectivity between core reward regions in patients with obesity after laparoscopic sleeve gastrectomy ( Dong et al, 2020 ) and lower connectivity between the dorsolateral prefrontal cortex and anterior medial frontal cortex in patients with major depressive disorder ( Strandwitz et al, 2019 ). While our previous work indicates significant effects of microbial diversity and enterotypes on functional connectivity between and within large-scale neural networks ( Cai et al, 2021 ), the exact relationship between gut Bacteroides and large-scale functional network connectivity has yet to be determined.…”