Roux-En-Y Gastric Bypass (RYGB) Surgery during High Liquid Sucrose Diet Leads to Gut Microbiota-Related Systematic Alterations

Roux-en-Y gastric bypass (RYGB) surgery has been proven successful in weight loss and improvement of co-morbidities associated with obesity. Chronic complications such as malabsorption of micronutrients in up to 50% of patients underline the need for additional therapeutic approaches. We investigate...

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Main Authors: Laimdota Zizmare, Christina N. Boyle, Sabrina Buss, Sandrine Louis, Laura Kuebler, Ketki Mulay, Ralf Krüger, Lara Steinhauer, Isabelle Mack, Manuel Rodriguez Gomez, Kristina Herfert, Yvonne Ritze, Christoph Trautwein
Format: Article
Language:English
Published: MDPI AG 2022-01-01
Series:International Journal of Molecular Sciences
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Online Access:https://www.mdpi.com/1422-0067/23/3/1126
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author Laimdota Zizmare
Christina N. Boyle
Sabrina Buss
Sandrine Louis
Laura Kuebler
Ketki Mulay
Ralf Krüger
Lara Steinhauer
Isabelle Mack
Manuel Rodriguez Gomez
Kristina Herfert
Yvonne Ritze
Christoph Trautwein
author_facet Laimdota Zizmare
Christina N. Boyle
Sabrina Buss
Sandrine Louis
Laura Kuebler
Ketki Mulay
Ralf Krüger
Lara Steinhauer
Isabelle Mack
Manuel Rodriguez Gomez
Kristina Herfert
Yvonne Ritze
Christoph Trautwein
author_sort Laimdota Zizmare
collection DOAJ
description Roux-en-Y gastric bypass (RYGB) surgery has been proven successful in weight loss and improvement of co-morbidities associated with obesity. Chronic complications such as malabsorption of micronutrients in up to 50% of patients underline the need for additional therapeutic approaches. We investigated systemic RYGB surgery effects in a liquid sucrose diet-induced rat obesity model. After consuming a diet supplemented with high liquid sucrose for eight weeks, rats underwent RYGB or control sham surgery. RYGB, sham pair-fed, and sham ad libitum-fed groups further continued on the diet after recovery. Notable alterations were revealed in microbiota composition, inflammatory markers, feces, liver, and plasma metabolites, as well as in brain neuronal activity post-surgery. Higher fecal 4-aminobutyrate (GABA) correlated with higher Bacteroidota and <i>Enterococcus</i> abundances in RYGB animals, pointing towards the altered enteric nervous system (ENS) and gut signaling. Favorable C-reactive protein (CRP), serine, glycine, and 3-hydroxybutyrate plasma profiles in RYGB rats were suggestive of reverted obesity risk. The impact of liquid sucrose diet and caloric restriction mainly manifested in fatty acid changes in the liver. Our multi-modal approach reveals complex systemic changes after RYGB surgery and points towards potential therapeutic targets in the gut-brain system to mimic the surgery mode of action.
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spelling doaj.art-93b2dffb794f489f9b9c30b5e3328c102023-11-23T16:35:21ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-01-01233112610.3390/ijms23031126Roux-En-Y Gastric Bypass (RYGB) Surgery during High Liquid Sucrose Diet Leads to Gut Microbiota-Related Systematic AlterationsLaimdota Zizmare0Christina N. Boyle1Sabrina Buss2Sandrine Louis3Laura Kuebler4Ketki Mulay5Ralf Krüger6Lara Steinhauer7Isabelle Mack8Manuel Rodriguez Gomez9Kristina Herfert10Yvonne Ritze11Christoph Trautwein12Werner Siemens Imaging Center, Department of Preclinical Imaging and Radiopharmacy, University Hospital Tübingen, Eberhard Karls University of Tübingen, Röntgenweg 13, 72076 Tübingen, GermanyInstitute of Veterinary Physiology, University of Zurich, Winterthurerstraße 260, CH-8057 Zurich, SwitzerlandWerner Siemens Imaging Center, Department of Preclinical Imaging and Radiopharmacy, University Hospital Tübingen, Eberhard Karls University of Tübingen, Röntgenweg 13, 72076 Tübingen, GermanyDepartment of Physiology and Biochemistry of Nutrition, Max Rubner-Institut, Haid-und-Neu-Straße 9, 76131 Karlsruhe, GermanyWerner Siemens Imaging Center, Department of Preclinical Imaging and Radiopharmacy, University Hospital Tübingen, Eberhard Karls University of Tübingen, Röntgenweg 13, 72076 Tübingen, GermanyDepartment of Medical Psychology and Behavioral Neurobiology, Eberhard Karls University of Tübingen, Silcherstraße 5, 72076 Tübingen, GermanyDepartment of Physiology and Biochemistry of Nutrition, Max Rubner-Institut, Haid-und-Neu-Straße 9, 76131 Karlsruhe, GermanyDepartment of Physiology and Biochemistry of Nutrition, Max Rubner-Institut, Haid-und-Neu-Straße 9, 76131 Karlsruhe, GermanyDepartment of Psychosomatic Medicine and Psychotherapy, University Hospital Tübingen, Osianderstraße 5, 72076 Tübingen, GermanyDepartment of Physiology and Biochemistry of Nutrition, Max Rubner-Institut, Haid-und-Neu-Straße 9, 76131 Karlsruhe, GermanyWerner Siemens Imaging Center, Department of Preclinical Imaging and Radiopharmacy, University Hospital Tübingen, Eberhard Karls University of Tübingen, Röntgenweg 13, 72076 Tübingen, GermanyDepartment of Medical Psychology and Behavioral Neurobiology, Eberhard Karls University of Tübingen, Silcherstraße 5, 72076 Tübingen, GermanyWerner Siemens Imaging Center, Department of Preclinical Imaging and Radiopharmacy, University Hospital Tübingen, Eberhard Karls University of Tübingen, Röntgenweg 13, 72076 Tübingen, GermanyRoux-en-Y gastric bypass (RYGB) surgery has been proven successful in weight loss and improvement of co-morbidities associated with obesity. Chronic complications such as malabsorption of micronutrients in up to 50% of patients underline the need for additional therapeutic approaches. We investigated systemic RYGB surgery effects in a liquid sucrose diet-induced rat obesity model. After consuming a diet supplemented with high liquid sucrose for eight weeks, rats underwent RYGB or control sham surgery. RYGB, sham pair-fed, and sham ad libitum-fed groups further continued on the diet after recovery. Notable alterations were revealed in microbiota composition, inflammatory markers, feces, liver, and plasma metabolites, as well as in brain neuronal activity post-surgery. Higher fecal 4-aminobutyrate (GABA) correlated with higher Bacteroidota and <i>Enterococcus</i> abundances in RYGB animals, pointing towards the altered enteric nervous system (ENS) and gut signaling. Favorable C-reactive protein (CRP), serine, glycine, and 3-hydroxybutyrate plasma profiles in RYGB rats were suggestive of reverted obesity risk. The impact of liquid sucrose diet and caloric restriction mainly manifested in fatty acid changes in the liver. Our multi-modal approach reveals complex systemic changes after RYGB surgery and points towards potential therapeutic targets in the gut-brain system to mimic the surgery mode of action.https://www.mdpi.com/1422-0067/23/3/1126RYGBmetabolomicsmicrobiomeinflammationgut-brain axisGABA
spellingShingle Laimdota Zizmare
Christina N. Boyle
Sabrina Buss
Sandrine Louis
Laura Kuebler
Ketki Mulay
Ralf Krüger
Lara Steinhauer
Isabelle Mack
Manuel Rodriguez Gomez
Kristina Herfert
Yvonne Ritze
Christoph Trautwein
Roux-En-Y Gastric Bypass (RYGB) Surgery during High Liquid Sucrose Diet Leads to Gut Microbiota-Related Systematic Alterations
International Journal of Molecular Sciences
RYGB
metabolomics
microbiome
inflammation
gut-brain axis
GABA
title Roux-En-Y Gastric Bypass (RYGB) Surgery during High Liquid Sucrose Diet Leads to Gut Microbiota-Related Systematic Alterations
title_full Roux-En-Y Gastric Bypass (RYGB) Surgery during High Liquid Sucrose Diet Leads to Gut Microbiota-Related Systematic Alterations
title_fullStr Roux-En-Y Gastric Bypass (RYGB) Surgery during High Liquid Sucrose Diet Leads to Gut Microbiota-Related Systematic Alterations
title_full_unstemmed Roux-En-Y Gastric Bypass (RYGB) Surgery during High Liquid Sucrose Diet Leads to Gut Microbiota-Related Systematic Alterations
title_short Roux-En-Y Gastric Bypass (RYGB) Surgery during High Liquid Sucrose Diet Leads to Gut Microbiota-Related Systematic Alterations
title_sort roux en y gastric bypass rygb surgery during high liquid sucrose diet leads to gut microbiota related systematic alterations
topic RYGB
metabolomics
microbiome
inflammation
gut-brain axis
GABA
url https://www.mdpi.com/1422-0067/23/3/1126
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