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Nutrients
Volume 12
Issue 10
10.3390/nu12102924
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Article

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

by
Tien S. Dong
1,2,3,
Arpana Gupta
1,2,4,5,
Jonathan P. Jacobs
1,2,3,4,5,
Venu Lagishetty
1,2,3,
Elizabeth Gallagher
4,
Ravi R. Bhatt
4,6,
Priten Vora
4,
Vadim Osadchiy
4,7,
Jean Stains
4,
Anna Balioukova
8,
Yijun Chen
5,8,
Erik Dutson
5,8,
Emeran A. Mayer
1,2,4,5 and
Claudia Sanmiguel
1,2,3,4,5,*
1
The Vatche and Tamar Manoukian Division of Digestive Diseases, Department of Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095, USA
2
UCLA Microbiome Center, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095, USA
3
Division of Gastroenterology, Hepatology and Parenteral Nutrition, VA Greater Los Angeles Healthcare System, Los Angeles, CA 90025, USA
4
G. Oppenheimer Center for Neurobiology of Stress and Resilience, University of California, Los Angeles, CA 90095, USA
5
David Geffen School of Medicine, University of California, Los Angeles, CA 90095, USA
6
Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine at USC, University of Southern California, Los Angeles, CA 90033, USA
7
Department of Urology, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095, USA
8
UCLA Center for Obesity and METabolic Health (COMET), Los Angeles, CA 90024, USA
*
Author to whom correspondence should be addressed.
Nutrients 2020, 12(10), 2924; https://doi.org/10.3390/nu12102924
Received: 28 August 2020 / Revised: 17 September 2020 / Accepted: 21 September 2020 / Published: 24 September 2020
(This article belongs to the Special Issue Brain-Gut Microbiota Interactions in Obesity)
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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. View Full-Text
Keywords: bariatric surgery; brain–gut–microbiome axis; metabolite; obesity; brain bariatric surgery; brain–gut–microbiome axis; metabolite; obesity; brain
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MDPI and ACS Style

Dong, T.S.; Gupta, A.; Jacobs, J.P.; Lagishetty, V.; Gallagher, E.; Bhatt, R.R.; Vora, P.; Osadchiy, V.; Stains, J.; Balioukova, A.; Chen, Y.; Dutson, E.; Mayer, E.A.; Sanmiguel, C. Improvement in Uncontrolled Eating Behavior after Laparoscopic Sleeve Gastrectomy Is Associated with Alterations in the Brain–Gut–Microbiome Axis in Obese Women. Nutrients 2020, 12, 2924. https://doi.org/10.3390/nu12102924

AMA Style

Dong TS, Gupta A, Jacobs JP, Lagishetty V, Gallagher E, Bhatt RR, Vora P, Osadchiy V, Stains J, Balioukova A, Chen Y, Dutson E, Mayer EA, Sanmiguel C. Improvement in Uncontrolled Eating Behavior after Laparoscopic Sleeve Gastrectomy Is Associated with Alterations in the Brain–Gut–Microbiome Axis in Obese Women. Nutrients. 2020; 12(10):2924. https://doi.org/10.3390/nu12102924

Chicago/Turabian Style

Dong, Tien S., Arpana Gupta, Jonathan P. Jacobs, Venu Lagishetty, Elizabeth Gallagher, Ravi R. Bhatt, Priten Vora, Vadim Osadchiy, Jean Stains, Anna Balioukova, Yijun Chen, Erik Dutson, Emeran A. Mayer, and Claudia Sanmiguel. 2020. "Improvement in Uncontrolled Eating Behavior after Laparoscopic Sleeve Gastrectomy Is Associated with Alterations in the Brain–Gut–Microbiome Axis in Obese Women" Nutrients 12, no. 10: 2924. https://doi.org/10.3390/nu12102924

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