Presence of Tannerella forsythia in patients with chronic periodontal disease and atherosclerosis

  • Danijela Staletović University of Priština Kosovska Mitrovica, Faculty of Medicine, Clinic for Dentistry, Kosovska Mitrovica, Serbia
  • Ibrachim Kannosh University of Belgrade, Faculty of Dental Medicine, Department of Human Genetics, Belgrade, Serbia
  • Meliha Šehalić University of Priština Kosovska Mitrovica, Faculty of Medicine, Clinic for Dentistry, Kosovska Mitrovica, Serbia
  • Vladanka Vukićević University of Priština Kosovska Mitrovica, Faculty of Medicine, Clinic for Dentistry, Kosovska Mitrovica, Serbia
  • Zoraida Milojković University of Priština Kosovska Mitrovica, Faculty of Medicine, Clinic for Dentistry, Kosovska Mitrovica, Serbia
  • Aleksandra Ilić University of Priština Kosovska Mitrovica, Faculty of Medicine, Institute for Preventive Medicine, Kosovska Mitrovica, Serbia
  • Verica Pavlić Institute for Dentistry, Banja Luka, Bosnia and Herzegovina
  • Zlata Brkić University of Defence, Faculty of Medicine of the Military Medical Academy, Belgarde Serbia
Keywords: periapical periodontitits, tannerella forsythia, atherosclerosis, risk factors, comorbidity

Abstract


Background/Aim. Periodontal disease is an inflammatory disease that occur in the tissues surrounding the teeth in response to bacterial biofilm accumulation (dental plaque). Among others, Tannerela forsythia (Tf) was recognized as one of the most significant and specific bacterial species in periodontal pocket („red complex“ bacteria). Atherosclerosis is a progressive narrowing of arteries that may lead to occlusion, as a consequence of lipid deposition. It underlies coronary heart disease (80%), as well as myocardial and cerebral infarctions. Increasing evidence over the past decade suggests a link between periodontal disease and atherosclerosis, where Tf can enter the systemic circulation directly or indirectly, and be present in atherosclerotic blood vessels. Therefore, the aim of this study was to detect the presence of Tf in atheromatous plaques obtained from different blood vessels in patients with chronic periodontitis. Methods. Ninety patients (male 61, female 29) with periodontal disease and atherosclerosis [recruited for either carotid artery stenosis requiring endartectomy or percutaneous transluminal coronary angioplasty (PTCA)] were included in this study. Clinical periodontal examinations consisted of plaque index (PI) (according to Silness Lӧu), gingival index (GI) (according to Lӧe Silnes), sulcus bleeding index (according to Mühleman-Son) and periodontal probing depth (PPD). Presence of Tf in periodontal pockets and atherosclerotic vessels was detected using polymerase chain reaction (PCR) method with positive control Tf ATCC 43037. Results. Tf was present in subgingival plaques of 68 (75.6%) of the patients, while its presence in atheromatous plaques were registered in 42 (53.3%) of the patients. It was significantly present in coronary blood vessels (41.7%), followed by carotid arteries (35.4%) and a. abdominalis aneurism (12.5%), a. mamaria (8.5%) and a. femoralis (2.1%) while in a. iliaca Tf was not detected at all. Conclusion. The present study suggests strong relationship between periodontal inflammation and atherogenesis; therefore, it should be considered as potential risk factor for atherosclerosis. Accordingly, it would be necessary to control periodontal disease in order to reduce mortality and morbidity associated with atherosclerosis.

References

Schützhold S, Kocher T, Biffar R, Hoffmann T, Schmidt CO, Micheelis W, et al. Changes in prevalence of periodontitis in two German population-based studies. J Clin Periodontol 2015; 42(2): 121–30.

Pucar A, Milasin J, Lekovic V, Vukadinovic M, Ristic M, Putnik S, Keet al. Correlation between atherosclerosis and periodontal putative pathogenic bacterial infections in coronary and inter-nal mammary arteries. J Periodontol 2007; 78(4): 677–82.

Koshi E, Rajesh S, Koshi P, Arunima PR. Risk assessment for periodontal disease. J Indian Soc Periodontol. 2012; 16(3): 324–8.

Kanjuh V, Ostojić M, Bojić M, Đurić D, Gojković-Bukarica Lj, Tasić N, et al. Atherosclerosis at the threshold of the III mil-lennium (Morphological clinical correlation of atherosclerotic lesions of relevant clinical syndromes). In: Nedeljković IS, Kanjuh IV, Vukotić RM, editors. Cardiology. 3rd ed. Begrade: D.P za izdavačko trgovinsku delatnost, 2000; p. 2393–423. (Serbian)

Beck JD, Garsia R, Heiss G, Vokonas P, Ofenbacher S. Periodon-tal disease and cardiovascular disease. J Periodontol 1996; 67(10 Suppl): 1123–37.

De Stefano F, Anda RF, Kahn HS, Williamson DF, Russell CM. Dental disease and risk of coronary heart disease and mortali-ty. BMJ 1993; 306 (6879): 688–91.

Chhibber-Goel J, Singhal V, Bhowmik D, Vivek R, Parakh N, Bhargava B, et al. Linkages between oral commensal bacteria and atherosclerotic plaques in coronary artery disease patients. NPJ Biofilms Microbiomes 2016; 2: 7.

Libby P. The vascular biology of aterosclerosos. In: Libby P, Bonow RO, Mann DL, Zipes D, Braunwald E, editors. Braun-wald’s Heart disease. 8ht ed. Philadelphia, PA: Sounders Else-vier, 2008; p. 985–1002.

Friedrich V, Pubingers S, Chen T, Messner P, Dewhirst FE, Schäffer C. Draft genome sequence of Tannerella forsythia type strain ATCC 43037. Genome Announc 2015; 3(3): pii: e00660-15.

Cairo F, Castellani S, Gori AM, Nieri M, Baldelli G, Abbate R, et al. Severe periodontitis in young adults is associated with sub-clinical atherosclerosis. J Clin Periodontol 2008; 35(6): 465–72.

Armitage GC. Development of a classification system for peri-odontal diseases and conditions. Ann Periodontol. 1999; 4(1): 1–6.

Papapanou PN. Systemic effects of periodontitis: lessons learned from research on atherosclerotic vascular disease and adverse pregnancy outcomes. Int Dent J 2015; 65(6): 283–91.

Mahalakshmi K, Krishnan P, Arumugam SB. Association of peri-odontopathic anaerobic bacterial co-occurrence to atheroscle-rosis-a cross-sectional study. Anaerobe 2017; 44: 66–72.

Ohki T, Itabashi Y, Kohno T, Yoshizawa A, Nishikubo S, Watanabe S, et al. Detection of periodontal bacteria in throm-bi of patients with acute myocardial infarction by polymerase chain reaction. Am Heart J 2012; 163(2): 164–7.

Perunovic ND, Rakic MM, Nikolic LI, Jankovic SM, Aleksic ZM, Plecas DV, et al. The Association Between Periodontal In-flammation and Labor Triggers (Elevated Cytokine Levels) in Preterm Birth: A Cross-Sectional Study. J Periodontol 2016; 87(3): 248–56.

Mattila KJ, Valle MS, Neiminen MS, Valtonen W, Hietanierni KL. Dental infections and coronary atherosclerosis. Athero-sclerosis. 1993; 103(2): 205–11.

Mattila KJ, Asikanen S, Wolf J, Jousimies-Somer H, Valtonen V, Nieminen M. Age, dental infections,and coronary heart disease. J Dent Res 2000; 79(2): 756–60.

Chistiakov DA, Orekhov AN, Bobryshev YV. Links between ath-erosclerotic and periodontal disease. Exp Mol Pathol 2016; 100(1): 220–35.

Szulc M, Kustrzycki W, Janczak D, Michalowska D, Baczynska D, Radwan-Oczko M. Presence of Periodontopathic Bacteria DNA in Atheromatous Plaques from Coronary and Carotid Arteries. Biomed Res Int 2015; 2015: 825397.

Velsko IM, Chukkapalli SS, Rivera MF, Lee JY, Chen H, Zheng D, et al. Active invasion of oral and aortic tissues by Porphy-romonas gingivalis in mice causally links periodontitis and ath-erosclerosis. PLoS One 2014; 9(5): e97811.

Hussain M, Stover CM, Dupont AP. Gingivalis in periodontal disease and atherosclerosis – scenes of action for antimicrobial peptides and complement. Front Immunol 2015; 6: 45.

Kholy KE, Genco RJ, Van Dyke TE. Oral infections and cardio-vascular disease. Trends Endocrinol Metab 2015; 26(6): 315–21.

Rangé H, Labreuche J, Louedec L, Rondeau P, Planesse C, Sebbag U, et al. Periodontal bacteria in human carotid atherothrom-bosis as a potential trigger for neutrophil activation. Athero-sclerosis 2014; 236(2): 448–55.

Haraszthy VI, Zambon JJ, Trevisan M, Zeid M, Genco RJ. Identi-fication of periodontal pathogens in atheromatous plaques. J Periodontol 2000; 71(10): 1554–60.

Figuero Е, Sánchez-Beltrán М, Cuesta-Frechoso S, Tejerina MJ, Castro JA, Gutiérrez JM, et al. Detection of periodontal bacte-ria in atheromatous plaque by nested polymerase chain. J Peri-odontol 2011; 82(10): 1469–77.

Kurihara N, Inoue Y, Iwai T, Umeda M, Huang Y, Ishikawa I. De-tection and localization of periodontopathic bacteria in ab-dominal aortic aneurysms. Eur J Vasc Endovasc Surg 2004; 28(5): 553–8.

Published
2021/04/19
Section
Original Paper