The Neuro-Endo-Microbio-Ome Study: A Pilot Study of Neurobiological Alterations Pre- Versus Post-Bariatric Surgery

Author:

Agarwal Khushbu12,Maki Katherine A.3ORCID,Vizioli Carlotta12ORCID,Carnell Susan4,Goodman Ethan4,Hurley Matthew4,Harris Civonnia5,Colwell Rita678,Steele Kimberley59,Joseph Paule V.12

Affiliation:

1. National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, MD, USA

2. National Institute of Nursing Research, National Institutes of Health, Bethesda, MD, USA

3. Translational Biobehavioral and Health Disparities Branch, Clinical Center, National Institutes of Health, Bethesda, MD, USA

4. Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD, USA

5. Department of Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA

6. CosmosID Inc., Rockville, MD, USA

7. Center for Bioinformatics and Computational Biology, University of Maryland Institute for Advanced Computer Studies, University of Maryland, College Park, MD, USA

8. Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, USA

9. Department of Health, Behavior and Society, The Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA

Abstract

Background Plausible phenotype mechanisms following bariatric surgery include changes in neural and gastrointestinal physiology. This pilot study aims to investigate individual and combined neurologic, gut microbiome, and plasma hormone changes pre- versus post-vertical sleeve gastrectomy (VSG), Roux-en-Y gastric bypass (RYGB), and medical weight loss (MWL). We hypothesized post-weight loss phenotype would be associated with changes in central reward system brain connectivity, differences in postprandial gut hormone responses, and increased gut microbiome diversity. Methods Subjects included participants undergoing VSG, n = 7; RYGB, n = 9; and MWL, n = 6. Ghrelin, glucagon-like peptide-1, peptide-YY, gut microbiome, and resting state functional magnetic resonance imaging (rsfMRI; using fractional amplitude of low-frequency fluctuations [fALFF]) were measured pre- and post-intervention in fasting and fed states. We explored phenotype characterization using clustering on gut hormone, microbiome, and rsfMRI datasets and a combined analysis. Results We observed more widespread fALFF differences post-bariatric surgery versus post-MWL. Decreased post-prandial fALFF was seen in food reward regions post-RYGB. The highest number of microbial taxa that increased post-intervention occurred in the RYGB group, followed by VSG and MWL. The combined hormone, microbiome, and MRI dataset most accurately clustered samples into pre- versus post-VSG phenotypes followed by RYGB subjects. Conclusion The data suggest surgical weight loss (VSG and RYGB) has a bigger impact on brain and gut function versus MWL and leads to lesser post-prandial activation of food-related neural circuits. VSG subjects had the greatest phenotype differences in interactions of microbiome, rsfMRI, and gut hormone features, followed by RYGB and MWL. These results will inform future prospective research studying gut-brain changes post-bariatric surgery.

Funder

Intramural Research Training Awards, Clinical Center, National Institutes of Health

Intramural Research Training Awards, National Institute of Nursing Research

Division of Intramural Research National Institute on Alcohol Abuse and Alcoholism

The American Society of Metabolic and Bariatric Surgeons, Research Grant Award

Publisher

SAGE Publications

Subject

Research and Theory

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