The influence the oral microbiome on the risk of cardiovascular diseases
https://doi.org/10.30629/0023-2149-2025-103-8-9-596-605
Abstract
Justification. The occurrence of cardiovascular diseases (CVD) is influenced by many modifiable and unmodifiable risk factors, the number of which is constantly growing. One of these factors can be a violation of the composition of the oral microbiome. Its structure is quite variable. The predominance of certain microorganisms can not only cause local pathology, such as the development of caries or periodontitis, but also lead to systemic changes. The most pathogenic bacteria living in the oral cavity are Porphyromonas gingivalis, Streptococcus mutans, and bacteria of the genus Eikenella, the colonization of which is a risk factor for infectious endocarditis (IE), as well as coronary heart disease (CHD). Prevention of CVD should be aimed not only at the already known risk factors for cardiovascular pathology (obesity, emotional stress, metabolic syndrome, smoking, etc.), but also at the oral microbiome.
Goal. To prove the existence of a relationship between the pathology of the oral cavity and the development of CVD.
Material and methods. The analysis of publications was carried out using the following databases: PubMed, RSCI, Science Direct, CyberLeninka, Web of Science. The literature review includes 94 sources over the past 10 years.
Conclusion. The composition of the oral microbiome plays a significant role in the pathogenesis of CVD. Bacteria synthesize substances that mediate immune and inflammatory reactions, and can also migrate into the bloodstream, contributing to the development of atherosclerosis, CHD and IE, contributing to the development and progression of hypertension and chronic heart failure. It is necessary to pay attention to the prevention of oral dysbiosis as a risk factor for the development and progression of somatic pathology.
About the Authors
E. V. ReznikРоссия
Elena V. Reznik — Doctor of Medical Sciences, Doctor of the Highest category, Head of the Department of Propaedeutics of Internal Diseases №2 of the Institute of Clinical Medicine
Researcher ID N-6856-2016
Moscow
I. S. Kopetskiy
Россия
Igor S. Kopetskiy — Doctor of Medical Sciences, Professor of Therapeutic Dentistry, Head of the Department of Therapeutic Dentistry
Moscow
L. V. Pobozhieva
Россия
Ludmila V. Pobozhieva — Candidate of Medical Sciences, Associate Professor of Therapeutic Dentistry,
Moscow
M. D. Iarovoi
Россия
Maksim D. Iarovoi — 6th year student of the Federal State Autonomous Educational Institution of Higher Education
Moscow
L. I. Kafarskaya
Россия
Ludmila I. Kafarskaya — Doctor of Medical Sciences, Professor, Head of the Department of Microbiology and Virology, Institute of Microbiology and Virology
Moscow
References
1. Ivanov D.O., Orel V.I., Alexandrovich Yu.S. and others. Diseases of the cardiovascular system as a cause of mortality in the Russian Federation: ways to solve the problem. Medicine and healthcare organization. 2019;2:4–12. (In Russian). URL: https://cyberleninka.ru/article/n/zabolevaniya-serdechno-sosudistoy-sistemy-kak-prichina-smertnosti-v-rossiyskoy-federatsii-puti-resheniya-problemy (date access: 13.12.2024).
2. Clinical recommendations of the Ministry of Health of the Russian Federation. Stable coronary artery disease, 2024. Healthcare. Federal State Statistics Service. (In Russian). URL: https://rosstat.gov.ru/folder/13721# (date access: 13.12.2024).
3. Boytsov S.A.., Shalnova S.A.., Deev A.D. Mortality from cardiovascular diseases in the Russian Federation and possible mechanisms of its change. Journal of Neurology and Psychiatry. 2018;8:98–103. (In Russian).
4. Li X., Liu Y., Yang X., Li C., Song Z. The oral microbiota: community composition, influencing factors, pathogenesis, and interventions. Front Microbiol. 2022;13:895537. DOI: 10.3389/fmicb.2022.895537
5. Pobozhyeva L.V., Skvortsov-Iglov G.A., Bocharova Yu.A., Kopetsky I.S., Chebotar I.V. The relationship between Nanosynbacter lyticus epibiont bacteria and inflammatory periodontal diseases. Bulletin of the Russian State Medical University. 2024;6:139–143. (In Russian). DOI: 10.24075/vrgmu.2024.050
6. Roth C.E., Craveiro R.B., Niederau C., Malyaran H., Neuss S., Jankowski J., et al. Mechanical compression by simulating orthodontic tooth movement in an in vitro model modulates phosphorylation of AKT and MAPKS via TLR4 in human periodontal ligament cells. Int. J. Mol. Sci. 2022;23(15):8062. DOI: https://doi.org/10.3390/ijms23158062
7. Popova C., Dosseva-Panova V., Panov V. Microbiology of periodontal diseases. A review.Biotechnol. Biotechnol. Equip. 2013;27(3):3754–9. DOI: 10.5504/bbeq.2013.0027
8. Neal TW., Schlieve T. Complications of Severe Odontogenic Infections: A Review. Biology (Basel). 2022;11(12):1784. DOI: 10.3390/biology11121784. PMID: 36552293
9. Jafarzadeh S.R., Thomas B.S., Warren D.K., Gill J., Fraser V.J. Longitudinal study of the effects of bacteremia and sepsis on 5-year risk of cardiovascular events. Clin. Infect. Dis. 2016;63(4):495–500. DOI: 10.1093/cid/ciw320
10. Clinical recommendations of the Ministry of Health of the Russian Federation. Infectious endocarditis. 2021. (In Russian). URL: https://cr.minzdrav.gov.ru/recomend/54?ysclid=m4rju8mpb2228587281 (date access: 17.12.2024)
11. Lindholm M., Metsäniitty M., Granström E., Oscarsson J. Outer membrane vesicle-mediated serum protection in Aggregatibacter actinomycetemcomitans. J. Oral Microbiol. 2020;12(1):1747857. DOI: 10.1080/20002297.2020.1747857
12. Ozuna H., Snider I., Belibasakis G.N., Oscarsson J., Johansson A., Uriarte S.M. Aggregatibacter actinomycetemcomitans and filifactor alocis: Two exotoxin- producing oral pathogens. Front Oral Health. 2022;3:981343. DOI: 10.3389/froh.2022.981343
13. Kobsar A., Wiebecke S., Weber K., Koessler A., Kuhn S., Boeck M. et al. Effect of toxins from different periodontitis-associated bacteria on human platelet function. Mol. Oral Microbiol. 2024;39(6):468–476. DOI: 10.1111/omi.12480
14. Oscarsson J., Claesson R., Bao K., Brundin M., Belibasakis G.N. Phylogenetic analysis of filifactor alocis strains isolated from several oral infections identified a novel RTX toxin., FtxA. Toxins (Basel). 2020;12(11):687. DOI: 10.3390/toxins12110687
15. Talapko J., Juzbašić M., Meštrović T., Matijević T., Mesarić D., Katalinić D.et al. Aggregatibacter actinomycetemcomitans: from the oral cavity to the heart valves. Microorganisms. 2024;12(7):1451. DOI: 10.3390/microorganisms12071451
16. Wang C.Y., Wang H.C., Li J.M., Wang J.Y., Yang K.C., Ho Y.K. et al. Invasive infections of Aggregatibacter (Actinobacillus) actinomycetemcomitans. J Microbiol. Immunol. Infect. 2010;43(6):491–7. DOI: 10.1016/S1684-1182(10)60076-X
17. Borcan A.M., Olariu M.C., Costea E.L., Radu G., Simoiu M. Aggregatibacter actinomycetemcomitansendocarditis in an adult patient with patent ductus arteriosus. Germs. 2024;14(2):210–215. DOI: 10.18683/germs.2024.1433
18. Oliveira F.A.F., Forte C.P.F., Silva P.G.B., Lopes C.B., Montenegro R.C., Santos Â.K.C.R.D. et al. Molecular analysis of oral bacteria in heart valve of patients with cardiovascular disease by real-time polymerase chain reaction. Medicine (Baltimore). 2015;94(47):e2067. DOI: 10.1097/MD.0000000000002067
19. Del Giudice C., Vaia E., Liccardo D., Marzano F., Valletta A., Spagnuolo G. et al. Infective endocarditis: a focus on oral microbiota. Microorganisms. 2021;9(6):1218. DOI: 10.3390/microorganisms9061218
20. Liesenborghs L., Meyers S., Lox M., Criel M., Claes J., Peetermans M. et al. Staphylococcus aureus endocarditis: distinct mechanisms of bacterial adhesion to damaged and inflamed heart valves. Eur. Heart J. 2019;40(39):3248–3259. DOI: 10.1093/eurheartj/ehz175
21. Yasir A., Ghaidaa Gihadi Mohammed. (2024). THE importance of microRNAs in Endocarditis Associated with Staphylococcus aureus. University of Thi-Qar Journal of Science. 2024;11(2):34–39. DOI: 10.32792/utq/utjsci/v11i2.1226
22. Martini A.M., Moricz B.S., Ripperger A.K., Tran P.M., Sharp M.E., Forsythe A.N. et al. Association of Novel Streptococcus sanguinis virulence factors with pathogenesis in a native valve infective endocarditis model. Front Microbiol. 2020;11:10. DOI: 10.3389/fmicb.2020.00010
23. Souto R., Colombo AP. Prevalence of Enterococcus faecalis in subgingival biofilm and saliva of subjects with chronic periodontal infection. Arch. Oral Biol. 2008;53(2):155–60. DOI: 10.1016/j.archoralbio.2007.08.004
24. Dahl A., Iversen K., Tonder N., Hoest N., Arpi M., Dalsgaard M.et al. Prevalence of infective endocarditis in enterococcus faecalis bacteremia. J. Am. Coll. Cardiol. 2019;74(2):193–201. DOI: 10.1016/j.jacc.2019.04.059
25. Lockhart P.B., Brennan M.T., Sasser H.C., Fox P.C., Paster B.J., Bahrani-Mougeot F.K. Bacteremia associated with toothbrushing and dental extraction. Circulation. 2008;117(24):3118–25. DOI: 10.1161/CIRCULATIONAHA.107.758524
26. Mougeot F.K., Saunders S.E., Brennan M.T., Lockhart P.B. Associations between bacteremia from oral sources and distant-site infections: tooth brushing versus single tooth extraction. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2015;119(4):430–5. DOI: 10.1016/j.oooo.2015.01.009
27. Tubiana S., Blotière P.O., Hoen B., Lesclous P., Millot S., Rudant J. et al. Dental procedures, antibiotic prophylaxis, and endocarditis among people with prosthetic heart valves: nationwide population based cohort and a case crossover study. BMJ. 2017;358:j3776. DOI: 10.1136/bmj.j3776
28. Infectious endocarditis and intracardiac device infections. Clinical recommendations of the Ministry of Health of the Russian Federation., 2021. (In Russian). URL: https://scardio.ru/content/Guidelines/KP_Inf_Endokardit.pdf?ysclid=m6xxk987o7797865458 (date access 09.02.2025).
29. Del Giudice C., Vaia E., Liccardo D., Marzano F., Valletta A., Spagnuolo G. et al. Infective endocarditis: a focus on oral microbiota. Microorganisms. 2021;9(6):1218. DOI: 10.3390/microorganisms9061218
30. DeStefano F., Anda R.F., Kahn H.S., Williamson D.F., Russell C.M. Dental disease and risk of coronary heart disease and mortality. BMJ. 1993;306(6879):688–91. DOI: 10.1136/bmj.306.6879.688
31. Humphrey L.L., Fu R., Buckley D.I., Freeman M., Helfand M. Periodontal disease and coronary heart disease incidence: a systematic review and meta-analysis. J. Gen. Intern. Med. 2008;23(12):2079– 86. DOI: 10.1007/s11606-008-0787-6
32. Bouzid F., Gtif I., Alfadhli S., Charfeddine S., Ghorbel W., Abdelhédi R. et al. A potential oral microbiome signature associated with coronary artery disease in Tunisia. Biosci. Rep. 2022;42(7):BSR20220583. DOI: 10.1042/BSR20220583
33. Yumoto H., Nakae H., Fujinaka K., Ebisu S., Matsuo T. Interleukin-6 (IL-6) and IL-8 are induced in human oral epithelial cells in response to exposure to periodontopathic Eikenella corrodens. Infect. Immun. 1999;67(1):384–94. DOI: 10.1128/IAI.67.1.384-394.1999
34. Viafara-Garcia S.M., Gualtero DF., Avila-Ceballos D., Lafaurie G.I. Eikenella corrodens lipopolysaccharide stimulates the pro-atherosclerotic response in human coronary artery endothelial cells and monocyte adhesion. Eur. J. Oral Sci. 2018;126(6):476–484. DOI: 10.1111/eos.12580
35. Chhibber-Goel J., Singhal V., Bhowmik D., Vivek R., Parakh N., Bhargava B., Sharma A. Linkages between oral commensal bacteria and atherosclerotic plaques in coronary artery disease patients. NPJ Biofilms Microbiomes. 2016;2:7. DOI: 10.1038/s41522-016-0009-7
36. Schenkein H.A., Loos B.G. Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases. J. Clin. Periodontol. 2013;40 Suppl 14(0 14):S51–69. DOI: 10.1111/jcpe.12060
37. Liljestrand J.M., Paju S., Pietiäinen M., Buhlin K., Persson G.R., Nieminen M.S. et al. Immunologic burden links periodontitis to acute coronary syndrome. Atherosclerosis. 2018;268:177–184. DOI: 10.1016/j.atherosclerosis.2017.12.007
38. Kesavalu L., Lucas A.R., Verma RK., Liu L., Dai E., Sampson E., Progulske-Fox A. Increased atherogenesis during Streptococcus mutans infection in ApoE-null mice. J. Dent. Res. 2012;91(3):255–60. DOI: 10.1177/0022034511435101
39. Pietiäinen M., Liljestrand J.M., Kopra E., Pussinen P.J. Mediators between oral dysbiosis and cardiovascular diseases. Eur. J. Oral Sci. 2018;126(1):26–36. DOI: 10.1111/eos.12423. PMID: 30178551
40. Sen S., Logue L., Logue M., Otersen E.A.L., Mason E., Moss K. et al. Dental caries, race and incident ischemic stroke, coronary heart disease and death. Stroke. 2024;55(1):40–49. DOI: 10.1161/STROKEAHA.123.042528
41. Kaburova A.N., Drapkina O.M., Yudin S.M., Yafarova A.A., Koretsky S.N., Pokrovskaya M.S. et al. The relationship between gut microbiota., chronic systemic inflammation., and endotoxemia in patients with heart failure with preserved ejection fraction. Cardiovascular Therapy and Prevention. 2022;21(9):3315. (In Russian) DOI: 10.15829/1728-8800-2022-3315
42. Matacchione G., Piacenza F., Pimpini L., Rosati Y., Marcozzi S. The role of the gut microbiota in the onset and progression of heart failure: insights into epigenetic mechanisms and aging. Clin. Epigenetics. 2024;16(1):175. DOI: 10.1186/s13148-024-01786-9
43. Levine B., Kalman J., Mayer L., Fillit H.M., Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. N. Engl. J. Med. 1990;323(4):236–41. DOI: 10.1056/NEJM199007263230405
44. Mann D.L. Innate immunity and the failing heart: the cytokine hypothesis revisited. Circ. Res. 2015;116(7):1254–68. DOI: 10.1161/CIRCRESAHA.116.302317
45. Liu L., Wang Y., Cao Z.Y., Wang M.M., Liu X.M., Gao T. et al. Up-regulated TLR4 in cardiomyocytes exacerbates heart failure after longterm myocardial infarction. J. Cell. Mol. Med. 2015;19(12):2728–40. DOI: 10.1111/jcmm.12659
46. Francisqueti-Ferron F.V., Nakandakare-Maia E.T., Siqueira J.S., Ferron A.J.T., Vieira T.A., Bazan S.G.Z., Corrêa C.R. The role of gut dysbiosis-associated inflammation in heart failure. Rev. Assoc. Med. Bras. 2022;68(8):1120–1124. DOI: 10.1590/1806-9282.20220197
47. Mills KT., Stefanescu A., He J. The global epidemiology of hypertension. Nat. Rev. Nephrol. 2020;16(4):223–237. DOI: 10.1038/s41581-019-0244-2
48. Balanova Yu.A., Drapkina O.M., Kutsenko V.A., Imaeva A.E., Kontseva M.V., Maksimov S.A. et al. Arterial hypertension in the Russian population during the COVID-19 pandemic: gender differences in prevalence, treatment and its effectiveness. The ESSAY research data is RF3. Cardiovascular therapy and prevention. 2023;22(8S):3785. (in Russian). DOI: 10.15829/1728-8800-2023-3785. EDN: YRUNUX
49. d’El-Rei J., Cunha AR., Trindade M., Neves MF. Beneficial effects of dietary nitrate on endothelial function and blood pressure levels. Int. J. Hypertens. 2016;2016:6791519. DOI: 10.1155/2016/6791519
50. Velmurugan S., Gan J.M., Rathod K.S., Khambata R.S., Ghosh S.M., Hartley A.et al. Dietary nitrate improves vascular function in patients with hypercholesterolemia: a randomized., double-blind., placebo-controlled study. Am. J. Clin. Nutr. 2016;103(1):25–38. DOI: 10.3945/ajcn.115.116244. Erratum in: Am. J. Clin. Nutr. 2018;107(4):676. DOI: 10.1093/ajcn/nqx052
51. Lidder S., Webb A.J. Vascular effects of dietary nitrate (as found in green leafy vegetables and beetroot) via the nitrate-nitrite-nitric oxide pathway. Br. J. Clin. Pharmacol. 2013;75(3):677–96. DOI: 10.1111/j.1365-2125.2012.04420.x
52. Bondonno C.P., Liu A.H., Croft K.D., Considine M.J., Puddey I.B., Woodman R.J., Hodgson J.M. Antibacterial mouthwash blunts oral nitrate reduction and increases blood pressure in treated hypertensive men and women. Am. J. Hypertens. 2015;28(5):572–5. DOI: 10.1093/ajh/hpu192. Epub 2014 Oct 30. PMID: 25359409
53. Mitsui T., Harasawa R. The effects of essential oil., povidone-iodine., and chlorhexidine mouthwash on salivary nitrate/nitrite and nitrate-reducing bacteria. J. Oral Sci. 2017;59(4):597–601. DOI: 10.2334/josnusd.16-0593
54. Ostalska-Nowicka D., Paszyńska E., Dmitrzak-Węglarz M., Neyman-Bartkowiak A., Rabiega A., Zachwieja J., Nowicki M. Dental caries-related primary hypertension in children and adolescents: Cross-sectional study. Oral Dis. 2021;27(7):1822–1833. DOI: 10.1111/odi.13700
55. Kolesnikova LR., Dolgikh VV., Kolesnikova LI., Vlasov BYa., Natyaganova LV. The impact of arterial hypertension in children on dental decay activity. Stomatology. 2016;95(2):26–29. (In Russian). DOI: 10.17116/stomat201695226-29
56. Deehan EC., Yang C., Perez-Muñoz M.E., Nguyen N.K., Cheng C.C., Triador L.et al. Precision microbiome modulation with discrete dietary fiber structures directs short-chain fatty acid production. Cell. Host Microbe. 2020;27(3):389–404.e6. DOI: 10.1016/j.chom.2020.01.006
57. Zhang S.M., Huang S.L. The commensal anaerobe veillonella dispar reprograms its lactate metabolism and short-chain fatty acid production during the stationary phase. Microbiol. Spectr. 2023;11(2):e0355822. DOI: 10.1128/spectrum.03558-22
58. Perry R.J., Peng L., Barry N.A., Cline G.W., Zhang D., Cardone R.L. et al. Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature. 2016;534(7606):213–7. DOI: 10.1038/nature18309
59. Li J., Zhao F., Wang Y., Chen J., Tao J., Tian G. et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017;5(1):14. DOI: 10.1186/s40168-016-0222-x
60. Yakovleva M.V., Chervinets V.M., Chervinets Yu.V., Smirnova L.E. Gut and oral microbiota in patients with arterial hypertension and metabolic syndrome. Patologicheskaya Fiziologiya i Eksperimental`naya terapiya. (Pathological Physiology and Experimental Therapy., Russian Journal). 2020;64(4):101–105. (In Russian). DOI: 10.25557/0031-2991.2020.04.101-105
61. Sintim H.O., Gürsoy U.K. Biofilms as “Connectors” for Oral and Systems Medicine: A New Opportunity for Biomarkers., Molecular Targets., and Bacterial Eradication. OMICS. 2016;20(1):3–11. DOI: 10.1089/omi.2015.0146
62. Olsen I., Hajishengallis G. Major neutrophil functions subverted by Porphyromonas gingivalis. J. Oral Microbiol. 2016;8:30936. DOI: 10.3402/jom.v8.30936
63. Darveau RP. Periodontitis: a polymicrobial disruption of host homeostasis. Nat. Rev. Microbiol. 2010;8(7):481–90. DOI: 10.1038/nrmicro2337
64. Hajishengallis E., Hajishengallis G. Neutrophil homeostasis and periodontal health in children and adults. J. Dent. Res. 2014;93(3):231-7. DOI: 10.1177/0022034513507956
65. Hajishengallis G., Harokopakis E. Porphyromonas gingivalis interactions with complement receptor 3 (CR3): innate immunity or immune evasion? Front Biosci. 2007;12:4547–57. DOI: 10.2741/2409
66. Hajishengallis G., Shakhatreh MA., Wang M., Liang S. Complement receptor 3 blockade promotes IL-12-mediated clearance of Porphyromonas gingivalis and negates its virulence in vivo. J. Immunol. 2007;179(4):2359–67. DOI: 10.4049/jimmunol.179.4.2359
67. Imamura T., Potempa J., Tanase S., Travis J. Activation of blood coagulation factor X by arginine-specific cysteine proteinases (gingipain-Rs) from Porphyromonas gingivalis. J. Biol. Chem. 1997;272(25):16062–7. DOI: 10.1074/jbc.272.25.16062
68. Tonelli A., Lumngwena EN., Ntusi NAB. The oral microbiome in the pathophysiology of cardiovascular disease. Nat. Rev. Cardiol. 2023;20(6):386–403. DOI: 10.1038/s41569-022-00825-3
69. Neves A.L., Coelho J., Couto L., Leite-Moreira A., Roncon-Albuquerque R.Jr. Metabolic endotoxemia: a molecular link between obesity and cardiovascular risk. J. Mol. Endocrinol. 2013;51(2):R51–64. DOI: 10.1530/JME-13-0079
70. Liljestrand J.M., Paju S., Pietiäinen M., Buhlin K., Persson G.R., Nieminen M.S.et al. Immunologic burden links periodontitis to acute coronary syndrome. Atherosclerosis. 2018;268:177–184. DOI: 10.1016/j.atherosclerosis.2017.12.007
71. Jia R., Kurita-Ochiai T., Oguchi S., Yamamoto M. Periodontal pathogen accelerates lipid peroxidation and atherosclerosis. J. Dent. Res. 2013;92(3):247–52. DOI: 10.1177/0022034513475625
72. Tuomainen AM., Jauhiainen M., Kovanen PT., Metso J., Paju S., Pussinen PJ. Aggregatibacter actinomycetemcomitans induces MMP-9 expression and proatherogenic lipoprotein profile in apoE-deficient mice. Microb. Pathog. 2008;44(2):111–7. DOI: 10.1016/j.micpath.2007.08.011
73. Tonetti M.S., D’Aiuto F., Nibali L., Donald A., Storry C., Parkar M. et al. Treatment of periodontitis and endothelial function. N. Engl. J. Med. 2007;356(9):911–20. DOI: 10.1056/NEJMoa063186. Erratum in: N. Engl. J. Med. 2018;378(25):2450. DOI: 10.1056/NEJMx180022
74. Mollenhauer J., Schulmeister A. The humoral immune response to heat shock proteins. Experientia. 1992;48(7):644–9. DOI: 10.1007/BF02118310
75. Suárez LJ., Garzón H., Arboleda S., Rodríguez A. Oral Dysbiosis and autoimmunity: from local periodontal responses to an imbalanced systemic immunity. A Review. Front Immunol. 2020;11:591255. DOI: 10.3389/fimmu.2020.591255
76. Wick G., Perschinka H., Xu Q. Autoimmunity and atherosclerosiS. am. Heart J. 1999;138(5 Pt 2):S444–9. DOI: 10.1016/s0002-8703(99)70272-3
77. Wick G., Jakic B., Buszko M., Wick MC., Grundtman C. The role of heat shock proteins in atherosclerosis. Nat. Rev. Cardiol. 2014;11(9):516–29. DOI: 10.1038/nrcardio.2014.91
78. Kilian M. The oral microbiome - friend or foe? Eur. J. Oral Sci. 2018;126(1):5–12. DOI: 10.1111/eos.12527
79. Sälzer S., Graetz C., Dörfer C.E., Slot D.E., Van der Weijden F.A. Contemporary practices for mechanical oral hygiene to prevent periodontal disease. Periodontol. 2000. 2020;84(1):35–44. DOI: 10.1111/prd.12332
80. Chapple I.L., Van der Weijden F., Doerfer C., Herrera D., Shapira L., Polak D. et al. Primary prevention of periodontitis: managing gingivitis. J. Clin. Periodontol. 2015;42(16):S71–6. DOI: 10.1111/jcpe.12366
81. Arnett D.K., Blumenthal R.S., Albert M.A., Buroker A.B., Goldberger Z.D., Hahn E.J. et al. 2019 ACC/AHA guideline on the primary prevention of cardiovascular disease: executive summary: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. Circulation. 2019;140(11):e563–e595. DOI: 10.1161/CIR.0000000000000677. Erratum in: Circulation. 2019;140(11):e647–e648. Erratum in: Circulation. 2020 Jan 28;141(4):e59. Erratum in: Circulation. 2020;141(16):e773
82. Jia YJ., Liao Y., He Y.Q., Zheng M.Q., Tong X.T., Xue W.Q. et al. Association between oral microbiota and cigarette smoking in the chinese population. Front. Cell Infect. Microbiol. 2021;11:658203. DOI: 10.3389/fcimb.2021.658203
83. Beklen A., Sali N., Yavuz M.B. The impact of smoking on periodontal status and dental caries. Tob. Induc. Dis. 2022;20:72. DOI: 10.18332/tid/152112
84. Bergström J. Tobacco smoking and chronic destructive periodontal disease. Odontology. 2004;92(1):1–8. DOI: 10.1007/s10266-004-0043-4
85. Tobacco: Preventing Uptake, Promoting Quitting and Treating Dependence. 2023.
86. Benowitz N.L., Barua R.S., Rigotti N.A. et al. 2018 ACC expert consensus decision pathway on tobacco cessation treatment: a report of the American College of Cardiology task force on clinical expert consensus documents J. Am. Coll. Cardiol. 2018;72(25): 3332–3365. DOI: https://doi.org/10.1016/j.jacc.2018.10.027
87. Royal College of Physicians. E-Cigarettes and Harm Reduction: An Evidence Review. RCP, 2024.
88. Visseren F.L.J., Mach F., Smulders Y.M., Carballo D. et al. 2021 ESC guidelines on cardiovascular disease prevention in clinical practice. Eur. Heart J. 2021; 42(34): 3227–3337. DOI: https://doi.org/10.1093/eurheartj/ehab484 Erratum in: Eur. Heart J. 2022; 43(42): 4468.
89. Mostaza J.M., Pintó X., Armario P., Masana L. et al. SEA 2024 standards for global control of vascular risk. Clin. Investig. Arterioscler. 2024; 36(3);133–194. DOI: https://doi.org/10.1016/j.arteri.2024.02.001 (in English, Spanish).
90. Abellán Alemán J., Sabaris R.C., Pardo D.E., García Donaire J.A. et al. En representación de la Sociedad Española de Hipertensión y las Sociedades Autonómicas de Hipertensión y Riesgo Vascular de España. Documento de consenso sobre tabaquismo y riesgo vascular. Hipertens. Riesgo Vasc. 2024; 41(suppl. 1);S1–S85. DOI: https://doi.org/10.1016/S1889-1837(24)00075-8 (in Spanish).
91. Crean A.M., Adler A., Arbour L., Chan J. et al. Canadian Cardiovascular Society clinical practice update on contemporary management of the patient with hypertrophic cardiomyopathy. Can. J. Cardiol. 2024. Vol. 40, N 9. P. 1503–1523. DOI: https://doi.org/10.1016/j.cjca.2024.06.007
92. Virani S.S., Newby L.K., Arnold S.V., Bittner V. et al. 2023 AHA/ ACC/ACCP/ ASPC/NLA/PCNA guideline for the management of patients with chronic coronary disease: a report of the American Heart Association/American College of Cardiology Joint Committee on Clinical Practice Guidelines. Circulation. 2023; 148(9); e9–e119. DOI: https://doi.org/10.1161/CIR.0000000000001168 Erratum in: Circulation. 2023;148(13); e148. DOI: https://doi.org/10.1161/CIR.0000000000001183 Erratum in:Circulation.2023;148(23);e186. DOI: https://doi.org/10.1161/CIR.0000000000001195
93. Consensus on tobacco control in patients with metabolic syndrome. Endocrinology: news, opinions, training. 2025;14(3);74-91 (In Russian). DOI: https://doi.org/10.33029/2304-9529-2025-14-3-74-91
94. Tishchenko O.V., Krivenko L.S., Gargina V.V. The effect of smoking., heating tobacco products and electronic cigarettes on the plaque microbiota. Pol. Merkur. Lekarski. 2022;50(295):16–20. (In Russian). PMID: 35278292
95. Benowitz N.L., Barua R.S., Rigotti N.A. et al. 2018 ACC expert consensus decision pathway on tobacco cessation treatment: a report of the American College of Cardiology Task Force on Clinical Expert Consensus Documents. J. Am. Coll. Cardiol. 2018; 72(25);3332– 3365. DOI: https://doi.org/10.1016/j.jacc.2018.10.027
96. Lindson N., Butler A.R., McRobbie H., Bullen C., Hajek P., Wu A.D. et al. Electronic cigarettes for smoking cessation. Cochrane Database Syst. Rev. 2025;1. CD010216. DOI: https://doi.org/10.1002/14651858.CD010216.pub9
97. Hartmann-Boyce J., Lindson N., Butler A.R., McRobbie H., Bullen C., Hajek P. et al. Electronic cigarettes for smoking cessation. Cochrane Database Syst. Rev. 2024;1. CD010216. DOI: https://doi.org/10.1002/14651858.CD010216.pub8
98. Choi S., Lee K., Park S.M. Combined associations of changes in noncombustible nicotine or tobacco product and combustible cigarette use habits with subsequent short-term cardiovascular disease risk among South Korean men: a nationwide cohort study. Circulation. 2021; 144(19);1528–1538. DOI: https://doi.org/10.1161/CIRCULATIONAHA.121.054967 Erratum in: Circulation. 2021;144(19);e306. PMID: 34601948
99. Wong J.M., Esfahani A., Singh N., Villa C.R., Mirrahimi A., Jenkins D.J., Kendall C.W. Gut microbiota., diet., and heart disease. J. AOAC Int. 2012;95(1):24–30. DOI: 10.5740/jaoacint.sge_wong
100. Hara H., Haga S., Aoyama Y., Kiriyama S. Short-chain fatty acids suppress cholesterol synthesis in rat liver and intestine. J. Nutr. 1999;129(5):942–8. DOI: 10.1093/jn/129.5.942
101. Agnello M., Cen L., Tran NC., Shi W., McLean J.S., He X. Arginine improves pH homeostasis via metabolism and microbiome modulation. J. Dent Res. 2017;96(8):924–930. DOI: 10.1177/0022034517707512
102. Agnello M., Cen L., Tran N.C., Shi W., McLean JS., He X. Arginine improves pH homeostasis via metabolism and microbiome modulation. J. Dent Res. 2017;96(8):924–930. DOI: 10.1177/0022034517707512
103. Nguyen T., Brody H., Lin GH., Rangé H., Kuraji R., Ye C., Kamarajan P., Radaic A., Gao L., Kapila Y. Probiotics., including nisin-based probiotics., improve clinical and microbial outcomes relevant to oral and systemic diseases. Periodontol. 2020;82(1):173– 185. DOI: 10.1111/prd.12324
104. Vivekananda M.R., Vandana K.L., Bhat K.G. Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: a preliminary randomized clinical trial. J. Oral Microbiol. 2010;2. DOI: 10.3402/jom.v2i0.5344
105. Zhen W., Wang Z., Wang Q., Sun W., Wang R., Zhang W. et al. Cardiovascular disease therapeutics via engineered oral microbiota: Applications and perspective. Imeta. 2024;3(3):e197. DOI: 10.1002/imt2.197
106. Wang X.L., Chen W.J., Jin R., Xu X., Wei J., Huang H. et al. Engineered probiotics Clostridium butyricum-pMTL007-GLP-1 improves blood pressure via producing GLP-1 and modulating gut microbiota in spontaneous hypertension rat models. Microb. Biotechnol. 2023;16(4):799–812. DOI: 10.1111/1751-7915.14196
107. Lee M.F., Chiang C.H., Lin S.J., Song P.P., Liu H.C., Wu T.J., Lin W.W. Recombinant lactococcus lactis expressing ling zhi 8 protein ameliorates nonalcoholic fatty liver and early atherogenesis in cholesterol-fed rabbits. Biomed. Res. Int. 2020;2020:3495682. DOI: 10.1155/2020/3495682
Review
For citations:
Reznik E.V., Kopetskiy I.S., Pobozhieva L.V., Iarovoi M.D., Kafarskaya L.I. The influence the oral microbiome on the risk of cardiovascular diseases. Clinical Medicine (Russian Journal). 2025;103(8-9):596-605. (In Russ.) https://doi.org/10.30629/0023-2149-2025-103-8-9-596-605
JATS XML
































