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Bariatric Surgery Modulates Circulating and Cardiac Metabolites

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Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, SW11 2PH London, U.K.
*T.A. Mailing address: Professor of Cardiothoracic Surgery and Cardiovascular Sciences, Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, Praed Street, W2 1NY, London, U.K. E-mail: [email protected]
*E.H. Mailing address: Head of the Section of Computational and Systems Medicine, Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, SW7 2AZ, London, U.K. Tel: +44(0)20 75943220. Fax: +44(0)20 75943226. E-mail: [email protected]
Cite this: J. Proteome Res. 2014, 13, 2, 570–580
Publication Date (Web):October 13, 2013
Copyright © 2013 American Chemical Society

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    Bariatric procedures such as the Roux-en-Y gastric bypass (RYGB) operation offer profound metabolic enhancement in addition to their well-recognized weight loss effects. They are associated with significant reduction in cardiovascular disease risk and mortality, which suggests a surgical modification on cardiac metabolism. Metabolic phenotyping of the cardiac tissue and plasma postsurgery may give insight into cardioprotective mechanisms. The aim of the study was to compare the metabolic profiles of plasma and heart tissue extracts from RYGB- and sham-operated Wistar rats to identify the systemic and cardiac signature of metabolic surgery. A total of 27 male Wistar rats were housed individually for a week and subsequently underwent RYGB (n = 13) or sham (n = 14) operation. At week 8 postoperation, a total of 27 plasma samples and 16 heart tissue samples (8 RYGB; 8 Sham) were collected from animals and analyzed using 1H nuclear magnetic resonance (NMR) spectroscopy and ultra performance liquid chromatography (UPLC-MS) to characterize the global metabolite perturbation induced by RYGB operation. Plasma bile acids, phosphocholines, amino acids, energy-related metabolites, nucleosides and amine metabolites, and cardiac glycogen and amino acids were found to be altered in the RYGB operated group. Correlation networks were used to identify metabolite association. The metabolic phenotype of this bariatric surgical model inferred systematic change in both myocardial and systemic activity post surgery. The altered metabolic profile following bariatric surgery reflects an enhancement of cardiac energy metabolism through TCA cycle intermediates, cardiorenal protective activity, and biochemical caloric restriction. These surgically induced metabolic shifts identify some of the potential mechanisms that contribute toward bariatric cardioprotection through gut microbiota ecological fluxes and an enterocardiac axis to shield against metabolic syndrome of cardiac dysfunction.

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    3. Laura A. Filla, Wei Yuan, Eva L. Feldman, Shuwei Li, and James L. Edwards . Global Metabolomic and Isobaric Tagging Capillary Liquid Chromatography–Tandem Mass Spectrometry Approaches for Uncovering Pathway Dysfunction in Diabetic Mouse Aorta. Journal of Proteome Research 2014, 13 (12) , 6121-6134.
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    5. Mingjing Chen, Guanhong Miao, Zhiguang Huo, Hao Peng, Xiaoxiao Wen, Stephen Anton, Dachuan Zhang, Gang Hu, Ricky Brock, Phillip J. Brantley, Jinying Zhao. Longitudinal Profiling of Fasting Plasma Metabolome in Response to Weight-Loss Interventions in Patients with Morbid Obesity. Metabolites 2024, 14 (2) , 116.
    6. Davide Masi, Mickael Massicard, Karine Clément. Obésité et risque cardiovasculaire : le rôle de la chirurgie bariatrique dans la modulation du microbiote intestinal. Nutrition Clinique et Métabolisme 2023, 37 (2) , 2S8-2S15.
    7. Shanya Huang, Yi Lan, Chunlan Zhang, Jingjing Zhang, Zhiguang Zhou. The Early Effects of Bariatric Surgery on Cardiac Structure and Function: a Systematic Review and Meta-Analysis. Obesity Surgery 2023, 33 (2) , 453-468.
    8. Yogesh Garg, Navjot Kanwar, Shruti Chopra, Murtaza M. Tambuwala, Hemraj Dodiya, Amit Bhatia, Abhinav Kanwal. Microbiome Medicine: Microbiota in Development and Management of Cardiovascular Diseases. Endocrine, Metabolic & Immune Disorders - Drug Targets 2022, 22 (14) , 1344-1356.
    9. Khalid Mehmood, Afrasim Moin, Talib Hussain, Syed Mohd Danish Rizvi, DV Gowda, Shazi Shakil, MA Kamal. Can manipulation of gut microbiota really be transformed into an intervention strategy for cardiovascular disease management?. Folia Microbiologica 2021, 66 (6) , 897-916.
    10. Soo Jin Lee, Young Suk Park, Yong-Jin Kim, Sang-Uk Han, Geum-Sook Hwang, Yeyoung Han, Yoonseok Heo, Eunyoung Ha, Tae Kyung Ha. Changes in Trimethylamine-N-oxide Levels in Obese Patients following Laparoscopic Roux-en-Y Gastric Bypass or Sleeve Gastrectomy in a Korean Obesity Surgical Treatment Study (KOBESS). Journal of Clinical Medicine 2021, 10 (21) , 5091.
    11. Dimitrios E. Magouliotis, Maria P. Fergadi, Dimitris Zacharoulis. The Significant Hormonal Traits of Laparoscopic Sleeve Gastrectomy Are Further Supported Using Three-Dimensional MDCT Gastrography. Obesity Surgery 2021, 31 (5) , 2291-2292.
    12. Hany A. Balamoun, Mohamed Y. Ibrahim, Ahmed M. Hassan, Khaled M. Torfa, Mohamed S. El Hawary, Sahar A. Sharaf. Glycemic Control Changes After Sleeve Gastrectomy. Bariatric Surgical Practice and Patient Care 2020, 15 (1) , 27-32.
    13. Ali Aminian. Bariatric procedure selection in patients with type 2 diabetes: choice between Roux-en-Y gastric bypass or sleeve gastrectomy. Surgery for Obesity and Related Diseases 2020, 16 (2) , 332-339.
    14. Mihai V. Podgoreanu. Metabolomics and Other “-Omic” Approaches to Characterize Perioperative Trajectories. 2020, 67-91.
    15. Victoria Ceperuelo-Mallafré, Gemma Llauradó, Noelia Keiran, Ester Benaiges, Brenno Astiarraga, Laia Martínez, Silvia Pellitero, Jose Miguel González-Clemente, Amaia Rodríguez, José Manuel Fernández-Real, Albert Lecube, Ana Megía, Nuria Vilarrasa, Joan Vendrell, Sonia Fernández-Veledo. Preoperative Circulating Succinate Levels as a Biomarker for Diabetes Remission After Bariatric Surgery. Diabetes Care 2019, 42 (10) , 1956-1965.
    16. Parisa Savedoroudi, Tue Bjerg Bennike, Kenneth Kastaniegaard, Mohammad Talebpour, Alireza Ghassempour, Allan Stensballe. Serum proteome changes and accelerated reduction of fat mass after laparoscopic gastric plication in morbidly obese patients. Journal of Proteomics 2019, 203 , 103373.
    17. Esther Forkosh, Yaron Ilan. The heart-gut axis: new target for atherosclerosis and congestive heart failure therapy. Open Heart 2019, 6 (1) , e000993.
    18. Kemin Yan, Weijie Chen, Huijuan Zhu, Guole Lin, Wei Sun, Xiaoyan Liu, Hui Pan, Linjie Wang, Hongbo Yang, Meijuan Liu, Fengying Gong. The Changes of Serum Metabolites in Diabetic GK Rats after Ileal Transposition Surgery. Obesity Surgery 2019, 29 (3) , 882-890.
    19. Nadeeja N. Wijayatunga, Valerie G. Sams, John A. Dawson, Matthew L. Mancini, Gregory J. Mancini, Naima Moustaid‐Moussa. Roux‐en‐Y gastric bypass surgery alters serum metabolites and fatty acids in patients with morbid obesity. Diabetes/Metabolism Research and Reviews 2018, 34 (8)
    20. Zeena Eblimit, Sundararajah Thevananther, Saul J. Karpen, Heinrich Taegtmeyer, David D. Moore, Luciano Adorini, Daniel J. Penny, Moreshwar S. Desai. TGR 5 activation induces cytoprotective changes in the heart and improves myocardial adaptability to physiologic, inotropic, and pressure‐induced stress in mice. Cardiovascular Therapeutics 2018, 36 (5)
    21. Ali Aminian. Sleeve Gastrectomy: Metabolic Surgical Procedure of Choice?. Trends in Endocrinology & Metabolism 2018, 29 (8) , 531-534.
    22. Paulina Samczuk, Magdalena Luba, Joanna Godzien, Annalaura Mastrangelo, Hady Razak Hady, Jacek Dadan, Coral Barbas, Maria Gorska, Adam Kretowski, Michal Ciborowski. “Gear mechanism” of bariatric interventions revealed by untargeted metabolomics. Journal of Pharmaceutical and Biomedical Analysis 2018, 151 , 219-226.
    23. Hector C. Keun. NMR Spectroscopy of Serum and Plasma. 2018, 85-132.
    24. Panagiotis A. Vorkas, M. R. Abellona U, Jia V. Li. Tissue Multiplatform-Based Metabolomics/Metabonomics for Enhanced Metabolome Coverage. 2018, 239-260.
    25. Paulina Samczuk, Michal Ciborowski, Adam Kretowski. Application of Metabolomics to Study Effects of Bariatric Surgery. Journal of Diabetes Research 2018, 2018 , 1-13.
    26. Himel Mallick, Siyuan Ma, Eric A. Franzosa, Tommi Vatanen, Xochitl C. Morgan, Curtis Huttenhower. Experimental design and quantitative analysis of microbial community multiomics. Genome Biology 2017, 18 (1)
    27. Bernd Schultes. Increased Trimethylamine-N-Oxide (TMAO) Levels After Roux-en Y Gastric Bypass Surgery—Should We Worry About It?. Obesity Surgery 2017, 27 (8) , 2170-2173.
    28. Dimitrios E. Magouliotis, Vasiliki S. Tasiopoulou, Eleni Sioka, Christina Chatedaki, Dimitrios Zacharoulis. Impact of Bariatric Surgery on Metabolic and Gut Microbiota Profile: a Systematic Review and Meta-analysis. Obesity Surgery 2017, 27 (5) , 1345-1357.
    29. Mohsen Mazidi, Pedro Paulo P. de Caravatto, John R. Speakman, Ricardo V. Cohen. Mechanisms of Action of Surgical Interventions on Weight-Related Diseases: the Potential Role of Bile Acids. Obesity Surgery 2017, 27 (3) , 826-836.
    30. N. Floch. The Influence of Microbiota on Mechanisms of Bariatric Surgery. 2017, 267-281.
    31. Meimei Chen, Fafu Yang, Jie Kang, Huijuan Gan, Xinmei Lai, Yuxing Gao. Metabolomic investigation into molecular mechanisms of a clinical herb prescription against metabolic syndrome by a systematic approach. RSC Advances 2017, 7 (87) , 55389-55399.
    32. Mohsen Mazidi, Peyman Rezaie, Ali Jangjoo, Alireza Tavassoli, Mohammad Taghi Rajabi, Andre Pascal Kengne, Mohsen Nematy. Effect of bariatric surgery on adiposity and metabolic profiles: A prospective cohort study in Middle-Eastern patients. World Journal of Diabetes 2017, 8 (7) , 374.
    33. Farnaz Fouladi, James E. Mitchell, Joseph A. Wonderlich, Kristine J. Steffen. The Contributing Role of Bile Acids to Metabolic Improvements After Obesity and Metabolic Surgery. Obesity Surgery 2016, 26 (10) , 2492-2502.
    34. Sophie H. Narath, Selma I. Mautner, Eva Svehlikova, Bernd Schultes, Thomas R. Pieber, Frank M. Sinner, Edgar Gander, Gunnar Libiseller, Michael G. Schimek, Harald Sourij, Christoph Magnes, . An Untargeted Metabolomics Approach to Characterize Short-Term and Long-Term Metabolic Changes after Bariatric Surgery. PLOS ONE 2016, 11 (9) , e0161425.
    35. J. David Mosinski, John P. Kirwan. Longer-Term Physiological and Metabolic Effects of Gastric Bypass Surgery. Current Diabetes Reports 2016, 16 (6)
    36. Ravi Aggarwal, Leanne Harling, Evangelos Efthimiou, Ara Darzi, Thanos Athanasiou, Hutan Ashrafian. The Effects of Bariatric Surgery on Cardiac Structure and Function: a Systematic Review of Cardiac Imaging Outcomes. Obesity Surgery 2016, 26 (5) , 1030-1040.
    37. Marius Trøseid, Johannes R. Hov, Torunn Kristin Nestvold, Hanne Thoresen, Rolf K. Berge, Asbjørn Svardal, Knut Tore Lappegård. Major Increase in Microbiota-Dependent Proatherogenic Metabolite TMAO One Year After Bariatric Surgery. Metabolic Syndrome and Related Disorders 2016, 14 (4) , 197-201.
    38. Elaine Holmes, Jeremy K. Nicholson, Jia Li, Ara W. Darzi. Phenotyping the Patient Journey. 2016, 49-74.
    39. Ewa Gralka, Claudio Luchinat, Leonardo Tenori, Barbara Ernst, Martin Thurnheer, Bernd Schultes. Metabolomic fingerprint of severe obesity is dynamically affected by bariatric surgery in a procedure-dependent manner ,. The American Journal of Clinical Nutrition 2015, 102 (6) , 1313-1322.
    40. N C Penney, J Kinross, R C Newton, S Purkayastha. The role of bile acids in reducing the metabolic complications of obesity after bariatric surgery: a systematic review. International Journal of Obesity 2015, 39 (11) , 1565-1574.
    41. Hina Y Bhutta, Neetu Rajpal, Wendy White, Johannes M. Freudenberg, Yaping Liu, James Way, Deepak Rajpal, David C. Cooper, Andrew Young, Ali Tavakkoli, Lihong Chen, . Effect of Roux-en-Y Gastric Bypass Surgery on Bile Acid Metabolism in Normal and Obese Diabetic Rats. PLOS ONE 2015, 10 (3) , e0122273.
    42. Julian L. Griffin, Xinzhu Wang, Elizabeth Stanley. Does Our Gut Microbiome Predict Cardiovascular Risk?. Circulation: Cardiovascular Genetics 2015, 8 (1) , 187-191.
    43. Timothy E. Sweeney, John M. Morton. Metabolic surgery: Action via hormonal milieu changes, changes in bile acids or gut microbiota? A summary of the literature. Best Practice & Research Clinical Gastroenterology 2014, 28 (4) , 727-740.
    44. Carmine Finelli. Could the improvement of obesity-related co-morbidities depend on modified gut hormones secretion?. World Journal of Gastroenterology 2014, 20 (44) , 16649.

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