Meta-analysis of the Impact of Bariatric Surgery on Circulating TMAO Levels as a Predictor of Cardiovascular Disease Risk


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Abstract

Introduction:Trimethylamine N-oxide (TMAO) is a metabolite of the gut microbiota that is considered a cardiovascular risk factor. Because bariatric surgery (BS) produces changes in the composition of the gut microbiota, the production of TMAO can be compromised. Thus, the purpose of this meta-analysis was to determine the effect of BS on circulating TMAO levels.

Methods:A systematic search was carried on in Embase, PubMed, Web of Science, and Scopus databases. The meta-analysis was conducted using Comprehensive Meta-Analysis (CMA) V2 software. The overall effect size was determined by a random-effects metaanalysis and the leave-one-out approach.

Results:Random-effects meta-analysis of 5 studies consisting of 142 subjects demonstrated a significant increase in circulating TMAO levels after BS (SMD: 1.190, 95% CI: 0.521, 1.858, p(<0.001; I2:89.30%).

Conclusion:Considering that levels of TMAO are affected after BS due to gut microbial metabolism alteration, there has been a significant elevation in TMAO concentrations observed to occur after BS in obese subjects.

About the authors

Tannaz Jamialahmadi

Applied Biomedical Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences

Email: info@benthamscience.net

Luis Simental-Mendia

Biomedical Research Unit, Mexican Social Security Institute

Email: info@benthamscience.net

Gokhan Zengin

Department of Biology, Science Faculty, Selcuk University

Email: info@benthamscience.net

Wael Almahmeed

Heart and Vascular Institute, Cleveland Clinic Abu Dhabi

Email: info@benthamscience.net

Prashant Kesharwani

Department of Pharmaceutics, School of Pharmaceutical Education and Research, Jamia Hamdard

Email: info@benthamscience.net

Amirhossein Sahebkar

Applied Biomedical Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences,

Author for correspondence.
Email: info@benthamscience.net

References

  1. Ataey, A.; Jafarvand, E.; Adham, D.; Moradi-Asl, E. The relationship between obesity, overweight, and the human development index in world health organization Eastern Mediterranean region countries. J. Prev. Med. Public Health, 2020, 53(2), 98-105. doi: 10.3961/jpmph.19.100 PMID: 32268464
  2. Heymsfield, S.B.W.T.; Wadden, T.A. Mechanisms, pathophysiology, and management of obesity. N. Engl. J. Med., 2017, 376(15), 1492. PMID: 28402780
  3. Lahey, R.; Khan, S.S. Trends in obesity and risk of cardiovascular disease. Curr. Epidemiol. Rep., 2018, 5(3), 243-251. doi: 10.1007/s40471-018-0160-1 PMID: 30705802
  4. Ford, N.D.; Patel, S.A.; Narayan, K.M.V. Obesity in low- and middle-income countries: Burden, drivers, and emerging challenges. Annu. Rev. Public Health, 2017, 38(1), 145-164. doi: 10.1146/annurev-publhealth-031816-044604 PMID: 28068485
  5. Lee, C.M.Y.; Huxley, R.R.; Wildman, R.P.; Woodward, M. Indices of abdominal obesity are better discriminators of cardiovascular risk factors than BMI: A meta-analysis. J. Clin. Epidemiol., 2008, 61(7), 646-653. doi: 10.1016/j.jclinepi.2007.08.012 PMID: 18359190
  6. Khan, S.S.; Ning, H.; Wilkins, J.T.; Allen, N.; Carnethon, M.; Berry, J.D.; Sweis, R.N.; Lloyd-Jones, D.M. Association of body mass index with lifetime risk of cardiovascular disease and compression of morbidity. JAMA Cardiol., 2018, 3(4), 280-287. doi: 10.1001/jamacardio.2018.0022 PMID: 29490333
  7. Schauer, P.R.; Bhatt, D.L.; Kirwan, J.P.; Wolski, K.; Aminian, A.; Brethauer, S.A.; Navaneethan, S.D.; Singh, R.P.; Pothier, C.E.; Nissen, S.E.; Kashyap, S.R. Bariatric surgery versus intensive medical therapy for diabetes - 5-year outcomes. N. Engl. J. Med., 2017, 376(7), 641-651. doi: 10.1056/NEJMoa1600869 PMID: 28199805
  8. Sjöström, L.; Lindroos, A.K.; Peltonen, M.; Torgerson, J.; Bouchard, C.; Carlsson, B.; Dahlgren, S.; Larsson, B.; Narbro, K.; Sjöström, C.D.; Sullivan, M.; Wedel, H. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N. Engl. J. Med., 2004, 351(26), 2683-2693. doi: 10.1056/NEJMoa035622 PMID: 15616203
  9. Jamialahmadi, T. Reiner, Ž; Alidadi, M.; Kroh, M.; Simental-Mendia, L.E.; Pirro, M.; Sahebkar, A. Impact of bariatric surgery on pulse wave velocity as a measure of arterial stiffness: A systematic review and meta-analysis. Obes. Surg., 2021, 31(10), 4461-4469. doi: 10.1007/s11695-021-05611-7 PMID: 34319469
  10. Jamialahmadi, T.; Alidadi, M.; Atkin, S.L.; Kroh, M.; Almahmeed, W.; Moallem, S.A.; Al-Rasadi, K.; Rodriguez, J.H.; Santos, R.D.; Ruscica, M.; Sahebkar, A. Effect of bariatric surgery on flow-mediated vasodilation as a measure of endothelial function: A systematic review and meta-analysis. J. Clin. Med., 2022, 11(14), 4054. doi: 10.3390/jcm11144054 PMID: 35887817
  11. Jamialahmadi, T Reiner, Ž; Alidadi, M; Kroh, M; Cardenia, V; Xu, S The effect of bariatric surgery on circulating levels of oxidized low-density lipoproteins is apparently independent of changes in body mass index: A systematic review and meta-analysis. Oxid. Med. Cell. Longev., 2021, 2021 doi: 10.1155/2021/4136071
  12. Jamialahmadi, T. Reiner, Ž; Alidadi, M.; Almahmeed, W.; Kesharwani, P.; Al-Rasadi, K.; Eid, A.H.; Rizzo, M.; Sahebkar, A. Effect of bariatric surgery on intima media thickness: A systematic review and meta-analysis. J. Clin. Med., 2022, 11(20), 6056. doi: 10.3390/jcm11206056 PMID: 36294377
  13. Jamialahmadi, T. Reiner, Ž; Alidadi, M.; Kroh, M.; Almahmeed, W.; Ruscica, M. The effect of bariatric surgery on circulating levels of Lipoprotein (a): A meta-analysis. BioMed Res. Int., 2022, 2022, 8435133.
  14. Jamialahmadi, T.; Banach, M.; Almahmeed, W.; Kesharwani, P.; Sahebkar, A. Impact of bariatric surgery on circulating PCSK9 levels as marker of cardiovascular disease risk: A meta-analysis. Arch. Med. Sci., 2022, 18(5), 1372-1377. doi: 10.5114/aoms/152685 PMID: 36160336
  15. Kanitsoraphan, C.; Rattanawong, P.; Charoensri, S.; Senthong, V. Trimethylamine n-oxide and risk of cardiovascular disease and mortality. Curr. Nutr. Rep., 2018, 7(4), 207-213. doi: 10.1007/s13668-018-0252-z PMID: 30362023
  16. Schiattarella, G.G.; Sannino, A.; Toscano, E.; Giugliano, G.; Gargiulo, G.; Franzone, A.; Trimarco, B.; Esposito, G.; Perrino, C. Gut microbe-generated metabolite trimethylamine-N-oxide as cardiovascular risk biomarker: A systematic review and dose-response meta-analysis. Eur. Heart J., 2017, 38(39), 2948-2956. doi: 10.1093/eurheartj/ehx342 PMID: 29020409
  17. Wang, Z.; Klipfell, E.; Bennett, B.J.; Koeth, R.; Levison, B.S.; DuGar, B.; Feldstein, A.E.; Britt, E.B.; Fu, X.; Chung, Y.M.; Wu, Y.; Schauer, P.; Smith, J.D.; Allayee, H.; Tang, W.H.W.; DiDonato, J.A.; Lusis, A.J.; Hazen, S.L. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature, 2011, 472(7341), 57-63. doi: 10.1038/nature09922 PMID: 21475195
  18. Koeth, R.A.; Wang, Z.; Levison, B.S.; Buffa, J.A.; Org, E.; Sheehy, B.T.; Britt, E.B.; Fu, X.; Wu, Y.; Li, L.; Smith, J.D.; DiDonato, J.A.; Chen, J.; Li, H.; Wu, G.D.; Lewis, J.D.; Warrier, M.; Brown, J.M.; Krauss, R.M.; Tang, W.H.W.; Bushman, F.D.; Lusis, A.J.; Hazen, S.L. Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med., 2013, 19(5), 576-585. doi: 10.1038/nm.3145 PMID: 23563705
  19. Zhu, W.; Gregory, J.C.; Org, E.; Buffa, J.A.; Gupta, N.; Wang, Z.; Li, L.; Fu, X.; Wu, Y.; Mehrabian, M.; Sartor, R.B.; McIntyre, T.M.; Silverstein, R.L.; Tang, W.H.W.; DiDonato, J.A.; Brown, J.M.; Lusis, A.J.; Hazen, S.L. Gut microbial metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell, 2016, 165(1), 111-124. doi: 10.1016/j.cell.2016.02.011 PMID: 26972052
  20. Dehghan, P.; Farhangi, M.A.; Nikniaz, L.; Nikniaz, Z.; Asghari-Jafarabadi, M. Gut microbiota-derived metabolite trimethylamine N-oxide (TMAO) potentially increases the risk of obesity in adults: An exploratory systematic review and dose-response meta-analysis. Obes. Rev., 2020, 21(5), e12993. doi: 10.1111/obr.12993 PMID: 32017391
  21. Narath, S.H.; Mautner, S.I.; Svehlikova, E.; Schultes, B.; Pieber, T.R.; Sinner, F.M.; Gander, E.; Libiseller, G.; Schimek, M.G.; Sourij, H.; Magnes, C. An untargeted metabolomics approach to characterize short-term and long-term metabolic changes after bariatric surgery. PLoS One, 2016, 11(9), e0161425. doi: 10.1371/journal.pone.0161425 PMID: 27584017
  22. Trøseid, M.; Hov, J.R.; Nestvold, T.K.; Thoresen, H.; Berge, R.K.; Svardal, A.; Lappegård, K.T. Major increase in microbiota-dependent proatherogenic metabolite TMAO one year after bariatric surgery. Metab. Syndr. Relat. Disord., 2016, 14(4), 197-201. doi: 10.1089/met.2015.0120 PMID: 27081744
  23. Palmisano, S.; Campisciano, G.; Silvestri, M.; Guerra, M.; Giuricin, M.; Casagranda, B.; Comar, M.; de Manzini, N. Changes in gut microbiota composition after bariatric surgery: A new balance to decode. J. Gastrointest. Surg., 2020, 24(8), 1736-1746. doi: 10.1007/s11605-019-04321-x PMID: 31388884
  24. Higgins, J.P.T.; Green, S. Cochrane handbook for systematic reviews of interventions version 5.0.1. The Cochrane Collaboration. 2008. Available from: www.handbook. cochrane.org
  25. Wells, G.A.; Shea, B.; O’Connell, D.; Peterson, J.; Welch, V.; Losos, M. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in metaanalyses; Oxford, 2000.
  26. Borenstein, M.; Hedges, L.; Higgins, J.; Rothstein, H. Comprehensive meta-analysis, version 2 Biostat; Englewood NJ, 2005.
  27. Banach, M.; Serban, C.; Sahebkar, A.; Mikhailidis, D.P.; Ursoniu, S.; Ray, K.K.; Rysz, J.; Toth, P.P.; Muntner, P.; Mosteoru, S. García-García, H.M.; Hovingh, G.K.; Kastelein, J.J.P.; Serruys, P.W. Impact of statin therapy on coronary plaque composition: A systematic review and meta-analysis of virtual histology intravascular ultrasound studies. BMC Med., 2015, 13(1), 229. doi: 10.1186/s12916-015-0459-4 PMID: 26385210
  28. Huang, W.; Zhong, A.; Xu, H.; Xu, C.; Wang, A.; Wang, F.; Li, X.; Liu, Y.; Zou, J.; Zhu, H.; Zheng, X.; Yi, H.; Guan, J.; Yin, S. Metabolomics analysis on obesity-related obstructive sleep apnea after weight loss management: A preliminary study. Front. Endocrinol., 2022, 12, 761547. doi: 10.3389/fendo.2021.761547 PMID: 35046891
  29. Jomard, A.; Liberale, L.; Doytcheva, P.; Reiner, M.F.; Müller, D.; Visentin, M.; Bueter, M.; Lüscher, T.F.; Vettor, R.; Lutz, T.A.; Camici, G.G.; Osto, E. Effects of acute administration of trimethylamine N-oxide on endothelial function: A translational study. Sci. Rep., 2022, 12(1), 8664. doi: 10.1038/s41598-022-12720-5 PMID: 35606406
  30. Lee, S.J.; Park, Y.S.; Kim, Y.J.; Han, S.U.; Hwang, G.S.; Han, Y.; Heo, Y.; Ha, E.; Ha, T.K. 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). J. Clin. Med., 2021, 10(21), 5091. doi: 10.3390/jcm10215091 PMID: 34768610
  31. Shi, Q.; Wang, Q.; Zhong, H.; Li, D.; Yu, S.; Yang, H.; Wang, C.; Yin, Z. Roux-en-Y gastric bypass improved insulin resistance via alteration of the human gut microbiome and alleviation of endotoxemia. BioMed Res. Int., 2021, 2021, 1-14. doi: 10.1155/2021/5554991 PMID: 34337024
  32. Tremaroli, V.; Karlsson, F.; Werling, M. Ståhlman, M.; Kovatcheva-Datchary, P.; Olbers, T.; Fändriks, L.; le Roux, C.W.; Nielsen, J.; Bäckhed, F. Roux-en-Y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation. Cell Metab., 2015, 22(2), 228-238. doi: 10.1016/j.cmet.2015.07.009 PMID: 26244932
  33. Li, J.V.; Ashrafian, H.; Bueter, M.; Kinross, J.; Sands, C.; le Roux, C.W.; Bloom, S.R.; Darzi, A.; Athanasiou, T.; Marchesi, J.R.; Nicholson, J.K.; Holmes, E. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut, 2011, 60(9), 1214-1223. doi: 10.1136/gut.2010.234708 PMID: 21572120
  34. Dalla Via, A.; Gargari, G.; Taverniti, V.; Rondini, G.; Velardi, I.; Gambaro, V.; Visconti, G.L.; De Vitis, V.; Gardana, C.; Ragg, E.; Pinto, A.; Riso, P.; Guglielmetti, S. Urinary TMAO levels are associated with the taxonomic composition of the gut microbiota and with the choline TMA-lyase gene (cutC) harbored by enterobacteriaceae. Nutrients, 2019, 12(1), 62. doi: 10.3390/nu12010062 PMID: 31881690
  35. Juárez-Fernández, M.; Román-Sagüillo, S.; Porras, D.; García-Mediavilla, M.V.; Linares, P.; Ballesteros-Pomar, M.D.; Urioste-Fondo, A.; Álvarez-Cuenllas, B.; González-Gallego, J.; Sánchez-Campos, S.; Jorquera, F.; Nistal, E. Long-term effects of bariatric surgery on gut microbiota composition and faecal metabolome related to obesity remission. Nutrients, 2021, 13(8), 2519. doi: 10.3390/nu13082519 PMID: 34444679
  36. Sherry, B.H.; Zhang, R.; Garabedian, M.; Berger, J.S.; Heffron, S.P. Changes in tmao levels following bariatric surgery vary by procedure type. Circulation., 2022, 146(S1), A12480-A.

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