DOI:

10.37988/1811-153X_2023_4_71

Filifactor alocis and its associations with anaerobic bacteria in patients with periodontitis and cardiovascular diseases

Authors

  • E.N. Nikolaeva 1, PhD in Medical Sciences, full professor of the Molecular biology research Laboratory, principal scientist
    ORCID ID: 0000-0002-7854-3262
  • O.O. Yanuchevich 1, Academician of the Russian Academy of Sciences, PhD in Medical Sciences, full professor of the Periodontology Department
    ORCID ID: 0000-0003-0059-4980
  • T.V. Tsareva 1, PhD in Medical Sciences, associate professor of the Microbiology, virology, immunology Department
    ORCID ID: 0000-0001-9571-0520
  • M.S. Podporin 1, PhD in Medical Sciences, researcher at the Molecular biology research Laboratory of the Medico-dental research Institute
    ORCID ID: 0000-0001-6785-0016
  • V.N. Tsarev 1, PhD in Medical Sciences, full professor of the Microbiology, virology, immunology Department
    ORCID ID: 0000-0002-3311-0367
  • 1 Moscow State University of Medicine and Dentistry, 127473, Moscow, Russia

Abstract

Microbial damage to periodontal tissues is closely associated with a number of systemic diseases and, possibly, plays an important role in the occurrence of comorbid pathology. The aim of the work is to identify the pathogen Filifactor alocis as a new diagnostic indicator of periodontal disease in patients with chronic periodontitis with coronary heart disease (CHD).
Materials and methods.
We examined 180 patients with chronic periodontitis (CP) and cardiovascular diseases (CVD), including: acute myocardial infarction (AMI), angina pectoris I—II FC classes (AP), coronary artery disease with postinfarction cardiosclerosis (CAD) and indications for myocardial revascularization. Control group — 60 patients with chronic periodontitis of moderate severity without CVD. Dental and cardiological status, endothelial dysfunction, DNA composition of the main types of periodontal pathogens, including a new marker of periodontitis F. alocis in the subgingival biofilm of patients, and a biochemical blood test were assessed.
Results.
Statistically significant relationship found between the colonization of the subgingival biofilm by periodontal pathogens F. alocis and P. gingivalis with the presence of CVD. In patients with coronary artery disease, the frequency of detection of F. alocis and P. gingivalis, including the joint, is higher than in people without CVD. The risk ratio for the presence of F. alocis and P. gingivalis in patients with AMI was 2.76 (95% CI 1.24—6.15; p<0.05); CAD patients — 2.25 (95% CI 1.00—5.03; p<0.05); angina pectoris — 1.95 (95% CI 0.86—4.38; p>0.05). Relationships of F. alocis and P. gingivalis with clinical manifestations of acute and chronic cardiovascular diseases were revealed, which may indicate their role as key pathogens of inflammatory periodontal diseases and auxiliary pathogens in CVD.
Conclusion.
The results of a prospective study confirm the important role of key periodontal pathogenic species in the pathology under consideration and indicate the practical need to identify F. alocis and P. gingivalis in patients with CP, including those with comorbid CVD.

Key words:

periodontal pathogens, subgingival biofilm, DNA, cardiovascular diseases

For Citation

[1]
Nikolaeva E.N., Yanuchevich O.O., Tsareva T.V., Podporin M.S., Tsarev V.N. Filifactor alocis and its associations with anaerobic bacteria in patients with periodontitis and cardiovascular diseases. Clinical Dentistry (Russia).  2024; 26 (4): 71—79. DOI: 10.37988/1811-153X_2023_4_71

References

  1. Kato-Kogoe N., Kamiya K., Sakaguchi S., Omori M., Komori E., Kudo A., Nakamura S., Nakano T., Ueno T., Tamaki J., Hoshiga M. Salivary microbiota associated with peripheral microvascular endothelial dysfunction. J Atheroscler Thromb. 2023; 30 (7): 820—833. PMID: 36130883
  2. Dietrich T., Webb I., Stenhouse L., Pattni A., Ready D., Wanyonyi K.L., White S., Gallagher J.E. Evidence summary: the relationship between oral and cardiovascular disease. Br Dent J. 2017; 222 (5): 381—385. PMID: 28281612
  3. Alshibaya M.M., Vitovich M.V., Nikolaeva E.N., Tsarev V.N. A parodontopathogenic microflora in atherosclerotic plaque in patient with cardiovascular disease. Journal of Atherosclerosis and Dyslipidemias. 2019; 4 (37): 64—68 (In Russian). eLIBRARY ID: 41357520
  4. Liccardo D., Cannavo A., Spagnuolo G., Ferrara N., Cittadini A., Rengo C., Rengo G. Periodontal disease: A risk factor for diabetes and cardiovascular disease. Int J Mol Sci. 2019; 20 (6): 1414. PMID: 30897827
  5. Tsarev V.N., Nikolaeva E.N., Vitovich M.V., Mitereva M.I., Podporin M.S. Biofilm-forming bacteria in atherosclerotic plaques in patients with cardiovascular diseases and chronic periodontitis. Clinical Dentistry (Russia). 2020; 2 (94): 40—45 (In Russian). eLIBRARY ID: 43125603
  6. Joshi C., Bapat R., Anderson W., Dawson D., Hijazi K., Cherukara G. Detection of periodontal microorganisms in coronary atheromatous plaque specimens of myocardial infarction patients: A systematic review and meta-analysis. Trends Cardiovasc Med. 2021; 31 (1): 69—82. PMID: 31983534
  7. Ziganshina E.E., Sharifullina D.M., Lozhkin A.P., Khayrullin R.N., Ignatyev I.M., Ziganshin A.M. Bacterial Communities Associated with Atherosclerotic Plaques from Russian Individuals with Atherosclerosis. PLoS One. 2016; 11 (10): e0164836. PMID: 27736997
  8. Hajishengallis G., Lamont R.J. Polymicrobial communities in periodontal disease: Their quasi-organismal nature and dialogue with the host. Periodontol 2000. 2021; 86 (1): 210—230. PMID: 33690950
  9. Balmasova I.P., Tsarev V.N., Yanushevich O.O., Maev I.V., Mkrtumyan A.M., Arutyunov S.D. Periodontal microecology. The relationship of local and systemic effects. Moscow: Practical medicine, 2021. 264 p. (In Russian).
  10. Edmisson J.S., Tian S., Armstrong C.L., Vashishta A., Klaes C.K., Miralda I., Jimenez-Flores E., Le J., Wang Q., Lamont R.J., Uriarte S.M. Filifactor alocis modulates human neutrophil antimicrobial functional responses. Cell Microbiol. 2018; 20 (6): e12829. PMID: 29377528
  11. Tonelli A., Lumngwena E.N., Ntusi N.A.B. The oral microbiome in the pathophysiology of cardiovascular disease. Nat Rev Cardiol. 2023; 20 (6): 386—403. PMID: 36624275
  12. Thygesen K., Alpert J.S., Jaffe A.S., Chaitman B.R., Bax J.J., Morrow D.A., White H.D., Executive Group on behalf of the Joint European Society of Cardiology (ESC)/American College of Cardiology (ACC)/American Heart Association (AHA)/World Heart Federation (WHF) Task Force for the Universal Definition of Myocardial Infarction Fourth Universal Definition of Myocardial Infarction (2018). J Am Coll Cardiol. 2018; 72 (18): 2231—2264. PMID: 30153967
  13. Kuzmina E.M., Yanushevich O.O., Kuzmina I.N. Dental morbidity in the Russian population. Epidemiological dental examination of the population of Russia. Moscow: Moscow State University of Medicine and Dentistry, 2019. 304 p. (In Russian).
  14. Corretti M.C., Anderson T.J., Benjamin E.J., Celermajer D., Charbonneau F., Creager M.A., Deanfield J., Drexler H., Gerhard-Herman M., Herrington D., Vallance P., Vita J., Vogel R., International Brachial Artery Reactivity Task Force Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol. 2002; 39 (2): 257—65. PMID: 11788217
  15. Shalnova S.A., Metelskaya V.A., Kutsenko V.A., Yarovaya E.B., Kapustina A.V., Muromtseva G.A., Svinin G.E., Balanova Yu.A., Imaeva A.E., Evstifeeva S.E., Vilkov V.G., Barbarash O.L., Belova O.A., Grinshtein Yu.I., Efanov A.Yu., Kalachikova O.N., Kulakova N.V., Rotar O.P., Trubacheva I.A., Duplyakov D.V., Libis R.A., Viktorova I.A., Redko A.N., Yakushin S.S., Boytsov S.A., Shlyakhto E.V., Drapkina O.M. Non-high density lipoprotein cholesterol: A modern benchmark for assessing lipid metabolism disorders. Rational Pharmacotherapy in Cardiology. 2022; 4: 366—375 (In Russian). eLIBRARY ID: 49382921
  16. Yanushevich O.O., Tsarev V.N., Balmasova I.P., Nikolaeva E.N., Tsareva T.V., Podporin M.S., Ippolitov E.V. The first experience of using a domestic diagnostic set of genetic primers to identify a new periodontal pathogen filifactor alocis and its association with porphyromonas gingivalis. Russian Clinical Laboratory Diagnostics. 2022; 12: 744—748 (In Russian). eLIBRARY ID: 49997611
  17. Rahman B., Al-Marzooq F., Saad H., Benzina D., Al Kawas S. Dysbiosis of the subgingival microbiome and relation to periodontal disease in association with obesity and overweight. Nutrients. 2023; 15 (4): 826. PMID: 36839184
  18. Koshy B.S., Mahendra J. The Association between periodontal status, serum lipid levels, lipoprotein associated phosholipase A2 (Lp-PLA2) in chronic periodontitis subjects and healthy controls. J Clin Diagn Res. 2017; 11 (9): ZC17—ZC21. PMID: 29207826
  19. Isola G., Polizzi A., Santonocito S., Alibrandi A., Ferlito S. Expression of salivary and serum malondialdehyde and lipid profile of patients with periodontitis and coronary heart disease. Int J Mol Sci. 2019; 20 (23): 6061. PMID: 31805680
  20. Fu Y.W., Li X.X., Xu H.Z., Gong Y.Q., Yang Y. Effects of periodontal therapy on serum lipid profile and proinflammatory cytokines in patients with hyperlipidemia: a randomized controlled trial. Clin Oral Investig. 2016; 20 (6): 1263—9. PMID: 26434651
  21. Choi Y.H., Kosaka T., Ojima M., Sekine S., Kokubo Y., Watanabe M., Miyamoto Y., Ono T., Amano A. Relationship between the burden of major periodontal bacteria and serum lipid profile in a cross-sectional Japanese study. BMC Oral Health. 2018; 18 (1): 77. PMID: 29728099
  22. Makkar H., Reynolds M.A., Wadhawan A., Dagdag A., Merchant A.T., Postolache T.T. Periodontal, metabolic, and cardiovascular disease: Exploring the role of inflammation and mental health. Pteridines. 2018; 29 (1): 124—163. PMID: 30705520
  23. Gao S., Tian J., Li Y., Liu T., Li R., Yang L., Xing Z. Periodontitis and number of teeth in the risk of coronary heart disease: An updated meta-analysis. Med Sci Monit. 2021; 27: e930112. PMID: 34421117
  24. Vedin O., Hagström E., Östlund O., Avezum A., Budaj A., Flather M.D., Harrington R.A., Koenig W., Soffer J., Siegbahn A., Steg P.G., Stewart R.A.H., Wallentin L., White H.D., Held C., STABILITY Investigators Associations between tooth loss and prognostic biomarkers and the risk for cardiovascular events in patients with stable coronary heart disease. Int J Cardiol. 2017; 245: 271—276. PMID: 28735759
  25. Shiloah J., Bland P.S., Scarbecz M., Patters M.R., Stein S.H., Tipton D.A. The effect of long-term aspirin intake on the outcome of non-surgical periodontal therapy in smokers: a double-blind, randomized pilot study. J Periodontal Res. 2014; 49 (1): 102—9. PMID: 23594239
  26. Felix J., Chaban P., Ouanounou A. Dental management of patients undergoing antithrombotic therapy. J Can Dent Assoc. 2020; 86: k17. PMID: 33326372
  27. Ruquet M., Maille G., Tavitian P., Tardivo D., Hüe O., Bonfil J.J. Alveolar bone loss and ageing: possible association with coronary heart diseases and/or severe vascular diseases. Gerodontology. 2016; 33 (3): 356—62. PMID: 25395062
  28. Saffi M.A., Furtado M.V., Polanczyk C.A., Montenegro M.M., Ribeiro I.W., Kampits C., Haas A.N., Rösing C.K., Rabelo-Silva E.R. Relationship between vascular endothelium and periodontal disease in atherosclerotic lesions: Review article. World J Cardiol. 2015; 7 (1): 26—30. PMID: 25632316
  29. Yanushevich O.O., Tsarev V.N., Nikolaeva E.N., Balmasova I.P., Ippolitov E.V., Tsareva T.V., Podporin M.S., Ponomareva A.G. The first domestic experience of detecting the association of anaerobic bacteria Filifactor alocis and Porphyromonas gingivalis by molecular biological methods in periodontal diseases and comorbid pathology (comparative research). Annals of the Russian Academy of Medical Sciences. 2022; 6: 437—446 (In Russian). eLIBRARY ID: 50359379
  30. Grudyanov A.I., Avraamova T.V. Studying the relationship between the periodontal status and cardiovascular system according to the clinical and laboratory data. Actual Problems of Medicine and Biology. 2019; 1: 9—12 (In Russian). eLIBRARY ID: 41412055
  31. Curia M.C., Pignatelli P., et al. Oral Porphyromonas gingivalis and Fusobacterium nucleatum abundance in subjects in primary and secondary cardiovascular prevention, with or without heterozygous familial hypercholesterolemia. Biomedicines. 2022; 10 (9): 2144. PMID: 36140246
  32. Wu Y., Wang Y., Du L., Wang K., Wang S., Li G. The link between different infection forms of Porphyromonas gingivalis and acute myocardial infarction: a cross-sectional study. BMC Oral Health. 2023; 23 (1): 63. PMID: 36732711
  33. Bui F.Q., Almeida-da-Silva C.L.C., Huynh B., Trinh A., Liu J., Woodward J., Asadi H., Ojcius D.M. Association between periodontal pathogens and systemic disease. Biomed J. 2019; 42 (1): 27—35. PMID: 30987702
  34. Piccioni A., Niccolai E., Rozzi G., Spaziani G., Zanza C., Candelli M., Covino M., Gasbarrini A., Franceschi F., Amedei A. Familial hypercholesterolemia and acute coronary syndromes: The microbiota-immunity axis in the new diagnostic and prognostic frontiers. Pathogens. 2023; 12 (4): 627. PMID: 37111513

Received

August 27, 2023

Accepted

November 21, 2023

Published on

January 16, 2024