Antioxidant effect of gut microbiota on cardiovascular system

Close metadata

Recommended articles:

Major risk factors of cardiovascular complications at all stages of surgical treatment of elderly and senile patients with colorectal cancer and concomitant cardiovascular diseases. Russian Journal of Cardiology and Cardiovascular Surgery. 2023;(2):199-204

The influence of uric acid on the course of amyotrophic lateral sclerosis. S.S. Korsakov Journal of Neurology and Psychiatry. 2023;(5):177-180

Risk factors and pathogenetic mechanisms of genitourinary menopausal syndrome. Russian Bulletin of Obstetrician-Gynecologist. 2023;(4):44-49

Cerium oxide nanoparticles for surgery, plastic surgery and aesthetic medicine. Plastic Surgery and Aesthetic Medicine. 2023;(3):120-129

Changes in the intestinal microbiota and their relationship with some indicators of the cytokine profile in patients with external genital endometriosis. Russian Journal of Human Reproduction. 2023;(6):87-94

Colorectal cancer and gut microbiota. P.A. Herzen Journal of Oncology. 2024;(2):60-66

Over the past decade, significant attention has been paid to the studies devoted to the role of gut microbiota composition and its metabolites (short-chain fatty acids, trimethylamine, gaseous metabolites, etc.) in pathogenesis of various non-infectious diseases caused by oxidative stress including cardiovascular diseases. Research of interaction of environmental factors (components of diet, medications, etc.), gut microbiota and host metabolism can lead to emergence of a new therapeutic target in the treatment of arterial hypertension, heart failure, atherosclerosis and other cardiovascular diseases.

Keywords:

antioxidant

molecular hydrogen

gut microbiota

Authors:

A.Yu. Ivanova

Lomonosov Moscow State University

ORCID: 0000-0002-0497-7666

E.Yu. Rysenkova

National Medical Research Center of Cardiology

M.D. Smirnova

National Medical Research Center of Cardiology

T.V. Fofanova

National Medical Research Center of Cardiology

O.S. Medvedev

Lomonosov Moscow State University;
National Medical Research Center of Cardiology

Received:

28.03.2021

Accepted:

08.04.2021

List of references:

World Health Organization. Global Action Plan for the Prevention and Control of NCDs 2013—2030. Geneva: World Health Organization, 2013. Accessed May 31, 2021. https://www.who.int/nmh/publications/ncd-action-plan/en/
World Health Organization. Cardiovascular Diseases (CVDs) Fact Sheet. Accessed May 31, 2021. https://www.who.int/news-room/fact-sheets/detail/cardiovascular-diseases-(cvds)
DiBaise JK, Zhang H, Crowell M D, Krajmalnik-Brown R, Decker GA, Rittmann BE. Gut microbiota and its possible relationship with obesity. Mayo Clinic Proceedings. 2008;83(4):460-469. https://doi.org/10.4065/83.4.460
Tang WHW, Kitai T, Hazen SL. Gut microbiota in cardiovascular health and disease. Circulation Research. 2017;120(7):1183-1196. https://doi.org/10.1161/circresaha.117.309715
Komaroff AL. The Microbiome and Risk for Atherosclerosis. JAMA. 2018;319(23):2381. https://doi.org/10.1001/jama.2018.5240
Gopalakrishnan V, Helmink BA, Spencer C N, Reuben A, Wargo JA. The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy. Cancer Cell. 2018;33(4):570-580. https://doi.org/10.1016/j.ccell.2018.03.015
Marques FZ, Nelson E, Chu P-Y, Horlock D, Fiedler A, Ziemann M, Jian K Tan, Kuruppu S, Rajapakse NW, El-Osta A, Mackay CR, Kaye DM. High-Fiber Diet and Acetate Supplementation Change the Gut Microbiota and Prevent the Development of Hypertension and Heart Failure in Hypertensive Mice. Clinical Perspective. Circulation. 2016;135(10):964-977. https://doi.org/10.1161/circulationaha.116.024545
Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, Zadeh M, Gong M, Qi Y, Zubcevic J, Sahay B, Pepine CJ, Raizada MK, Mohamadzadeh M. Gut Dysbiosis Is Linked to Hypertension Novelty and Significance. Hypertension. 2015;65(6):1331-1340. https://doi.org/10.1161/hypertensionaha.115.05315
Li J, Zhao F, Wang Y, Chen J, Tao J, Tian G, Wu S, Liu W, Cui Q, Geng B, Zhang W, Weldon R, Auguste K, Yang L, Liu X, Chen L, Yang X, Zhu B, Cai J. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017;5(1):1-19. https://doi.org/10.1186/s40168-016-0222-x
Verhaar BJH, Collard D, Prodan A, Levels JHM, Zwinderman AH, Bäckhed F, Vogt L, Peters MJL, Muller M, Nieuwdorp M, van den Born BH. Associations between gut microbiota, faecal short-chain fatty acids, and blood pressure across ethnic groups: the HELIUS study. European Heart Journal. 2020;41(44):4259-4267. https://doi.org/10.1093/eurheartj/ehaa704
Seungbum K, Rigatto K, Gazzana MB, Knorst MM, Richards EM, Pepine CJ, Raizada MK. Altered Gut Microbiome Profile in Patients with Pulmonary Arterial Hypertension. Hypertension. 2020;75(4):1063-1071. https://doi.org/10.1161/HYPERTENSIONAHA.119.14294
Pasini E, Aquilani R, Testa C, Baiardi P, Angioletti S, Boschi F, Verri M, Dioguardi F. Pathogenic Gut Flora in Patients With Chronic Heart Failure. JACC: Heart Failure. 2016;4(3):220-227. https://doi.org/10.1016/j.jchf.2015.10.009
Cui X, Ye L, Li J, Jin L, Wang W, Li S, Bao M, Wu S, Li L, Geng B, Zhou X, Zhang J, Cai J. Metagenomic and metabolomic analyses unveil dysbiosis of gut microbiota in chronic heart failure patients. Scientific Reports. 2018;8(1):635. https://doi.org/10.1038/s41598-017-18756-2
Lanter BB, Sauer K, Davies DG. Bacteria Present in Carotid Arterial Plaques are Found as Biofilm Deposits which May Contribute to Enhanced Risk of Plaque Rupture. mBio. 2014;5(3):e01206-14. https://doi.org/10.1128/mbio.01206-14
Jonsson LA, Hallenius FF, Akrami R, Johansson E, Wester P, Arnerlöv C, Backhed F, Bergström G. Bacterial profile in human atherosclerotic plaques. Atherosclerosis. 2017;263:177-183. https://doi.org/10.1016/j.atherosclerosis.2017.06.016
Liu H, Chen X, Hu X, Niu H, Tian R, Wang H, Pang H, Jiang L, Qiu B, Chen X, Zhang Y, Ma Y, Tang S, Li H, Feng S, Zhang S, Zhang C. Alterations in the gut microbiome and metabolism with coronary artery disease severity. Microbiome. 2019;7(1):68. https://doi.org/10.1186/s40168-019-0683-9
Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, Britt EB, Fu X, Wu Y, Li L, Smith JD, DiDonato JA, Chen J, Li H, Wu GD, Lewis JD, Warrier M, Brown JM, Krauss RM, Tang WHW, Bushman FD, Lusis AJ, Hazen SL. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nature Medicine. 2013;19(5):576-585. https://doi.org/10.1038/nm.3145
Wang Z, Klipfell E, Bennett BJ, Koeth RS, Levison B, DuGar B, Feldstein A E, Britt E B, Fu X, Chung Y-M, Wu Y, Schauer Ph, Smith JD, Allayee H, Wilson Tang WH, DiDonato JA, Lusis A J, Hazen SL. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472(7341):57-63. https://doi.org/10.1038/nature09922
Chen K, Zheng X, Feng M, Li D, Zhang H. Gut Microbiota-Dependent Metabolite Trimethylamine N-Oxide Contributes to Cardiac Dysfunction in Western Diet-Induced Obese Mice. Frontiers in Physiology. 2017;8:139. https://doi.org/10.3389/fphys.2017.00139
Raetz CRH, Whitfield C. Lipopolysaccharide Endotoxins. Annual Review of Biochemistry. 2002;71:635-700. https://doi.org/10.1146/annurev.biochem.71.110601.135414
Masson GS, Nair AR, Dange RB, Silva-Soares PP, Michelini LC, Francis J. Toll-Like Receptor 4 Promotes Autonomic Dysfunction, Inflammation and Microglia Activation in the Hypothalamic Paraventricular Nucleus: Role of Endoplasmic Reticulum Stress. PLoS ONE. 2015;10(3):e0122850. https://doi.org/10.1371/journal.pone.0122850
Santisteban MM, Qi YF, Zubcevic J, Kim S, Yang T, Shenoy V, Cole-Jeffrey CT, Lobaton G, Stewart DC, Rubiano A, Simmons CS, Garcia-Pereira F, Johnson RD, Pepine CJ, Raizada MK. Hypertension-Linked Pathophysiological Alterations in the Gut. Circulation Research. 2017;120(2):312-323. https://doi.org/10.1161/CIRCRESAHA.116.309006
Morrison DJ, Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes. 2016;7(3):189-200. https://doi.org/10.1080/19490976.2015.1134082
Le Poul E, Loison C, Struyf S, Springael J-Y, Lannoy V, Decobecq M-E, Brézillon S, Dupriez V, Vassart G, Van Damme J, Parmentier M, Detheux M. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. The Journal of Biological Chemistry. 2003;278(28):25481-25489. https://doi.org/10.1074/jbc.M301403200
Busnelli M, Manzini S, Chiesa G. The Gut Microbiota Affects Host Pathophysiology as an Endocrine Organ: A Focus on Cardiovascular Disease. Nutrients. 2019;27:12(1):79. https://doi.org/10.3390/nu12010079
Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, Katsura K, Katayama Y, Asoh S, Ohta S. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nature Medicine. 2007;13(6):688-694. https://doi.org/10.1038/nm1577
Ohsawa I, Nishimaki K, Yamagata K, Ishikawa M, Ohta S. Consumption of hydrogen water prevents atherosclerosis in apolipoprotein E knockout mice. Biochemical and Biophysical Research Communications. 2008;377(4):1195-1198. https://doi.org/10.1016/j.bbrc.2008.10.156
Iketani M, Sekimoto K, Igarashi T, Takahashi M, Komatsu M, Sakane I, Takahashi H, Kawaguchi H, Ohtani-Kaneko R, Ohsawa I. Administration of hydrogen-rich water prevents vascular aging of the aorta in LDL receptor-deficient mice. Scientific Reports. 2018;8(1):16822. https://doi.org/10.1038/s41598-018-35239-0
Chi J, Li Z, Hong X, Zhao T, Bie Y, Zhang W, Yang J, Feng Z, Yu Z, Xu Q, Zhao L, Liu W, Gao Y, Yang H, Yang J, Liu J, Yang W. Inhalation of Hydrogen Attenuates Progression of Chronic Heart Failure via Suppression of Oxidative Stress and P53 Related to Apoptosis Pathway in Rats. Frontiers in Physiology. 2018;9:1026. https://doi.org/10.3389/fphys.2018.01026
Li X, Li L, Liu X, Wu J, Sun X, Li Z, Geng YJ, Liu F, Zhou Y. Attenuation of Cardiac Ischaemia-reperfusion Injury by Treatment with Hydrogen-rich Water. Current Molecular Medicine. 2019;19(4):294-302. https://doi.org/10.2174/1566524019666190321113544
Gao Q, Song H, Wang XT, Liang Y, Xi YJ, Gao Y, Guo QJ, LeBaron T, Luo YX, Li SC, Yin X, Shi HS, Ma YX. Molecular hydrogen increases resilience to stress in mice. Scientific Reports. 2017;7(1):9625. https://doi.org/10.1038/s41598-017-10362-6
Sakai T, Sato B, Hara K, Hara Y, Naritomi Y, Koyanagi S, Hara H, Nagao T, Ishibashi T. Consumption of water containing over 3.5 mg of dissolved hydrogen could improve vascular endothelial function. Vascular Health and Risk Management. 2014;10:591-597. https://doi.org/10.2147/VHRM.S68844
Ishibashi T, Kawamoto K, Matsuno K, Ishihara G, Baba T, Komori N. Peripheralendothelial function can be improved by daily consumption of water containing over 7 ppm of dissolved hydrogen: A randomized controlled trial. PLoS ONE. 2020;15(5):e0233484. https://doi.org/10.1371/journal.pone.0233484
Kawamura T, Wakabayashi N, Shigemura N, Huang CS, Masutani K, Tanaka Y, Noda K, Peng X, Takahashi T, Billiar TR, Okumura M, Toyoda Y, Kensler TW, Nakao A. Hydrogen gas reduces hyperoxic lung injury via the Nrf2 pathway in vivo. American Journal of Physiology. Lung Cellular and Molecular Physiology. 2013;304(10):L646-656. https://doi.org/10.1152/ajplung.00164.2012
Duncan SH, Aminov RI, Scott KP, Louis P, Stanton TB, Flint HJ. Proposal of Roseburia faecis sp. nov., Roseburia hominis sp. nov. and Roseburia inulinivorans sp. nov., based on isolates from human faeces. International Journal of Systematic and Evolutionary Microbiology. 2006;56(Pt 10):2437-2441. https://doi.org/10.1099/ijs.0.64098-0
Calusinska M, Happe T, Joris B, Wilmotte The surprising diversity of clostridial hydrogenases: a comparative genomic perspective. Microbiology (Reading). 2010;156(Pt 6):1575-1588. https://doi.org/10.1099/mic.0.032771-0
Simmering R, Taras D, Schwiertz A, Le Blay G, Gruhl B, Lawson PA, Collins MD, Blaut M. Ruminococcus luti sp. nov., isolated from a human faecal sample. Systematic and Applied Microbiology. 2002;25(2):189-193. https://doi.org/10.1078/0723-2020-00112
Suzuki A, Ito M, Hamaguchi T, Mori H, Takeda Y, Baba R, Watanabe T, Kurokawa K, Asakawa S, Hirayama M, Ohno K. Quantification of hydrogen production by intestinal bacteria that are specifically dysregulated in Parkinson’s disease. PLoS One. 2018;13(12):e0208313. https://doi.org/10.1371/journal.pone.0208313
Duncan SH, Flint HJ. Proposal of a neotype strain (A1-86) for Eubacterium rectale. Request for an opinion. International Journal of Systematic and Evolutionary Microbiology. 2008;58(Pt 7):1735-1736. https://doi.org/10.1099/ijs.0.2008/004580-0
Steer T, Collins MD, Gibson GR, Hippe H, Lawson PA. Clostridium hathewayi sp. nov., from human faeces. Systematic and Applied Microbiology. 2001;24(3):353-357. https://doi.org/10.1078/0723-2020-00044
Chassard C, Delmas E, Lawson PA, Bernalier-Donadille A. Bacteroides xylanisolvens sp. nov., a xylan-degrading bacterium isolated from human faeces. International Journal of Systematic and Evolutionary Microbiology. 2008;58(Pt 4):1008-1013. https://doi.org/10.1099/ijs.0.65504-0
Carbonero F, Benefiel AC, Gaskins HR. Contributions of the microbial hydrogen economy to colonic homeostasis. Nature Reviews. Gastroenterology and Hepatology. 2012;9(9):504-518. https://doi.org/10.1038/nrgastro.2012.85
Levitt MD. Volume and Composition of Human Intestinal Gas Determined by Means of an Intestinal Washout Technic. New England Journal of Medicine. 1971;284(25):1394-1398. https://doi.org/10.1056/nejm197106242842502
Flourié B, Etanchaud F, Florent C, Pellier P, Bouhnik Y, Rambaud JC. Comparative study of hydrogen and methane production in the human colon using caecal and faecal homogenates. Gut. 1990;31(6):684-685. https://doi.org/10.1136/gut.31.6.684
Strocchi A, Levitt MD. Factors affecting hydrogen production and consumption by human fecal flora. The critical roles of hydrogen tension and methanogenesis. The Journal of Clinical Investigation. 1992;89(4):1304-1311. https://doi.org/10.1172/JCI115716
Berean KJ, Ha N, Ou JZ, Chrimes AF, Grando D, Yao CK, Muir JG, Ward SA, Burgell RE, Gibson PR, Kalantar-Zadeh K. The safety and sensitivity of a telemetric capsule to monitor gastrointestinal hydrogen production in vivo in healthy subjects: a pilot trial comparison to concurrent breath analysis. Alimentary Pharmacology and Therapeutics. 2018;48(6):646-654. https://doi.org/10.1111/apt.14923
Levitt MD. Production and Excretion of Hydrogen Gas in Man. New England Journal of Medicine. 1969;281(3):122-127. https://doi.org/10.1056/nejm196907172810303
Cummings JH, Englyst HN. Measurement of starch fermentation in the human large intestine. Canadian Journal of Physiology and Pharmacology. 1991;69(1):121-129. https://doi.org/10.1139/y91-018
Sheflin AM, Borresen EC, Kirkwood JS, Boot CM, Whitney AK, Lu S, Brown RJ, Broeckling CD, Ryan EP, Weir TL. Dietary supplementation with rice bran or navy bean alters gut bacterial metabolism in colorectal cancer survivors. Molecular Nutrition & Food Research. 2017;61(1):10.1002/mnfr.201500905. https://doi.org/10.1002/mnfr.201500905
de Lorgeril M, Salen P, Martin JL, Monjaud I, Delaye J, Mamelle N. Mediterranean diet, traditional risk factors, and the rate of cardiovascular complications after myocardial infarction: final report of the Lyon Diet Heart Study. Circulation. 1999;99(6):779-785. https://doi.org/10.1161/01.cir.99.6.779
Ivanova AJu, Trunov SS, Shirokov IV, Belousova MA, Medvedeva NA, Medvedev OS. Changes in the functional activity of the rat gut microbiota against the background of a diet with an increased content of fat products with different fatty acid composition. Tehnologii zhivyh sistem. 2020;17(4):29-41. (In Russ.).
Suzuki Y, Sano M, Hayashida K, Ohsawa I, Ohta S, Fukuda K. Are the effects of alpha-glucosidase inhibitors on cardiovascular events related to elevated levels of hydrogen gas in the gastrointestinal tract? FEBS Letters. 2009;583(13):2157-2159. https://doi.org/10.1016/j.febslet.2009.05.052
Hanefeld M, Cagatay M, Petrowitsch T, Neuser D, Petzinna D, Rupp M. Acarbose reduces the risk for myocardial infarction in type 2 diabetic patients: meta-analysis of seven long-term studies. European Heart Journal. 2004;25(1):10-16. https://doi.org/10.1016/s0195-668x(03)00468-8
Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Microbiology: diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635-1638. https://doi.org/10.1126/science.1110591
Nava GM, Carbonero F, Croix JA, Greenberg E, Gaskins HR. Abundance and diversity of mucosa-associated hydrogenotrophic microbes in the healthy human colon. The ISME Journal. 2012;6(1):57-70. https://doi.org/10.1038/ismej.2011.90
Gottlieb K, Wacher V, Sliman J, Pimentel M. Review article: inhibition of methanogenic archaea by statins as a targeted management strategy for constipation and related disorders. Alimentary Pharmacology and Therapeutics. 2016;43(2):197-212. https://doi.org/10.1111/apt.13469

Close metadata