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Association between periodontitis and pulse wave velocity: a systematic review and meta-analysis

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Abstract

Objectives

Severe periodontitis has been associated with endothelial dysfunction and arterial stiffness. The present study aimed to provide a critical appraisal and a meta-analysis of the literature investigating pulse wave velocity (PWV) in patients with and without severe periodontitis and to assess whether treatments influence PWV.

Materials and methods

English literature was searched on multiple databases up to April 2020 by two independent reviewers. Studies comparing PWV between patients with and without severe periodontitis or assessing the impact of periodontal treatments on PWV were searched and retrieved. Pool data analyses with random effect models were performed. The risk of bias was assessed using Newcastle–Ottawa Scale and RoB2 tools.

Results

Seventeen studies were selected. Of these, 10 were used for the meta-analysis. Twelve were cross-sectional studies and 5 interventional studies, including 3176 patients, of whom 1894 had severe periodontitis and 1282 were considered as the controls (without severe periodontitis). Based on carotid–femoral PWV measurement, patients with severe periodontitis (n = 309) have a significantly higher PVW than patients with non-severe periodontitis (n = 213), with a mean difference of 0.84 m/s (95% CI 0.50–1.18; p < 0.0001; I2 = 5%). Similarly, carotid–radial or brachial–ankle PWV values were significantly higher in patients with severe periodontitis. Results concerning the effect of non-surgical periodontal therapy were not conclusive. Overall, 9 studies (53%) were classified at a low risk of bias.

Conclusions

The present study demonstrates that patients with severe periodontitis have higher PWV compared to patients with non-severe periodontitis.

Clinical significance

Severe periodontitis is associated with arterial stiffness, supporting the mutual involvement of dentists and physicians.

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References

  1. Darnaud C, Thomas F, Pannier B, Danchin N, Bouchard P (2015) Oral health and blood pressure: the IPC cohort. Am J Hypertens 28:1257–1261. https://doi.org/10.1093/ajh/hpv025

    Article  PubMed  Google Scholar 

  2. Sen S, Giamberardino LD, Moss K, Morelli T, Rosamond WD, Gottesman RF, Beck J, Offenbacher S (2018) Periodontal disease, regular dental care use, and incident ischemic stroke. Stroke 49:355–362. https://doi.org/10.1161/STROKEAHA.117.018990

    Article  PubMed  PubMed Central  Google Scholar 

  3. Adolph M, Darnaud C, Thomas F, Pannier B, Danchin N, Batty GD, Bouchard P (2017) Oral health in relation to all-cause mortality: the IPC cohort study. Sci Rep 7:44604. https://doi.org/10.1038/srep44604

    Article  PubMed  PubMed Central  Google Scholar 

  4. Orlandi M, Suvan J, Petrie A, Donos N, Masi S, Hingorani A, Deanfield J, D'Aiuto F (2014) Association between periodontal disease and its treatment, flow-mediated dilatation and carotid intima-media thickness: a systematic review and meta-analysis. Atherosclerosis 236:39–46. https://doi.org/10.1016/j.atherosclerosis.2014.06.002

    Article  PubMed  Google Scholar 

  5. Czesnikiewicz-Guzik M, Osmenda G, Siedlinski M, Nosalski R, Pelka P, Nowakowski D, Wilk G, Mikolajczyk TP, Schramm-Luc A, Furtak A, Matusik P, Koziol J, Drozdz M, Munoz-Aguilera E, Tomaszewski M, Evangelou E, Caulfield M, Grodzicki T, D'Aiuto F, Guzik TJ (2019) Causal association between periodontitis and hypertension: evidence from Mendelian randomization and a randomized controlled trial of non-surgical periodontal therapy. Eur Heart J 40:3459–3470. https://doi.org/10.1093/eurheartj/ehz646

    Article  PubMed  PubMed Central  Google Scholar 

  6. Munoz Aguilera E, Suvan J, Buti J, Czesnikiewicz-Guzik M, Barbosa Ribeiro A, Orlandi M, Guzik TJ, Hingorani AD, Nart J, D'Aiuto F (2020) Periodontitis is associated with hypertension: a systematic review and meta-analysis. Cardiovasc Res 116:28–39. https://doi.org/10.1093/cvr/cvz201

    Article  PubMed  Google Scholar 

  7. Sanz M, Marco Del Castillo A, Jepsen S, Gonzalez-Juanatey JR, D'Aiuto F, Bouchard P, Chapple I, Dietrich T, Gotsman I, Graziani F, Herrera D, Loos B, Madianos P, Michel JB, Perel P, Pieske B, Shapira L, Shechter M, Tonetti M, Vlachopoulos C, Wimmer G (2020) Periodontitis and cardiovascular diseases: consensus report. J Clin Periodontol 47:268–288. https://doi.org/10.1111/jcpe.13189

    Article  PubMed  PubMed Central  Google Scholar 

  8. Vlachopoulos C, Aznaouridis K, Stefanadis C (2010) Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol 55:1318–1327. https://doi.org/10.1016/j.jacc.2009.10.061

    Article  PubMed  Google Scholar 

  9. Laurent S, Boutouyrie P, Cunha PG, Lacolley P, Nilsson PM (2019) Concept of extremes in vascular aging. Hypertension 74:218–228. https://doi.org/10.1161/HYPERTENSIONAHA.119.12655

    Article  PubMed  Google Scholar 

  10. Laurent S, Cockcroft J, Van Bortel L, Boutouyrie P, Giannattasio C, Hayoz D, Pannier B, Vlachopoulos C, Wilkinson I, Struijker-Boudier H, European Network for Non-invasive Investigation of Large Arteries (2006) Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 27:2588–2605. https://doi.org/10.1093/eurheartj/ehl254

    Article  PubMed  Google Scholar 

  11. Van Bortel LM, Laurent S, Boutouyrie P, Chowienczyk P, Cruickshank JK, De Backer T, Filipovsky J, Huybrechts S, Mattace-Raso FU, Protogerou AD, Schillaci G, Segers P, Vermeersch S, Weber T, Artery S, European Society of Hypertension Working Group on Vascular Structure and Function and European Network for Noninvasive Investigation of Large Arteries (2012) Expert consensus document on the measurement of aortic stiffness in daily practice using carotid-femoral pulse wave velocity. J Hypertens 30:445–448. https://doi.org/10.1097/HJH.0b013e32834fa8b0

    Article  PubMed  Google Scholar 

  12. Sun Z (2015) Aging, arterial stiffness, and hypertension. Hypertension 65:252–256. https://doi.org/10.1161/HYPERTENSIONAHA.114.03617

    Article  PubMed  Google Scholar 

  13. Schmitt A, Carra MC, Boutouyrie P, Bouchard P (2015) Periodontitis and arterial stiffness: a systematic review and meta-analysis. J Clin Periodontol 42:977–987. https://doi.org/10.1111/jcpe.12467

    Article  PubMed  Google Scholar 

  14. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605. https://doi.org/10.1007/s10654-010-9491-z

    Article  PubMed  Google Scholar 

  15. Sterne JAC, Savovic J, Page MJ, Elbers RG, Blencowe NS, Boutron I, Cates CJ, Cheng HY, Corbett MS, Eldridge SM, Emberson JR, Hernan MA, Hopewell S, Hrobjartsson A, Junqueira DR, Juni P, Kirkham JJ, Lasserson T, Li T, McAleenan A, Reeves BC, Shepperd S, Shrier I, Stewart LA, Tilling K, White IR, Whiting PF, Higgins JPT (2019) RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ 366:l4898. https://doi.org/10.1136/bmj.l4898

    Article  PubMed  Google Scholar 

  16. Ren J, Chen YB, Zhang YY, Zhou QB, Chen S, Yang JY, Tao J (2016) Decreased circulating neopterin is associated with increased arterial elasticity: a beneficial role of periodontal treatment. Aust Dent J 61:76–83. https://doi.org/10.1111/adj.12303

    Article  PubMed  Google Scholar 

  17. Sanz-Miralles EC, Li R, Momen-Heravi F, Mendieta C, Konofagou EE, Papapanou PN (2017) Assessment of arterial stiffness in periodontitis using a novel pulse wave imaging methodology. J Clin Periodontol 44:502–510. https://doi.org/10.1111/jcpe.12717

    Article  PubMed  Google Scholar 

  18. Jockel-Schneider Y, Harks I, Haubitz I, Fickl S, Eigenthaler M, Schlagenhauf U, Baulmann J (2014) Arterial stiffness and pulse wave reflection are increased in patients suffering from severe periodontitis. PLoS One 9:e103449. https://doi.org/10.1371/journal.pone.0103449

    Article  PubMed  PubMed Central  Google Scholar 

  19. Khumaedi AI, Purnamasari D, Wijaya IP, Soeroso Y, Marhamah S (2018) Association of Periodontitis and Arterial Stiffness in Type 2 Diabetic Patients. Acta Med Indones 50:320–327

    PubMed  Google Scholar 

  20. Miyaki K, Masaki K, Naito M, Naito T, Hoshi K, Hara A, Tohyama S, Nakayama T (2006) Periodontal disease and atherosclerosis from the viewpoint of the relationship between community periodontal index of treatment needs and brachial-ankle pulse wave velocity. BMC Public Health 6:131. https://doi.org/10.1186/1471-2458-6-131

    Article  PubMed  PubMed Central  Google Scholar 

  21. Franek E, Klamczynska E, Ganowicz E, Blach A, Budlewski T, Gorska R (2009) Association of chronic periodontitis with left ventricular mass and central blood pressure in treated patients with essential hypertension. Am J Hypertens 22:203–207. https://doi.org/10.1038/ajh.2008.330

    Article  PubMed  Google Scholar 

  22. Vieira CL, Cury PR, Miname MH, Martinez LR, Bortolotto LA, Giuliano IB, Santos RD, Caramelli B (2011) Severe periodontitis is associated with diastolic blood pressure elevation in individuals with heterozygous familial hypercholesterolemia: a pilot study. J Periodontol 82:683–688. https://doi.org/10.1902/jop.2010.100496

    Article  PubMed  Google Scholar 

  23. Franek E, Januszkiewicz-Caulier J, Blach A, Napora M, Jedynasty K, Budlewski T, Gozdowski D, Gorska R (2012) Intima-media thickness and other markers of atherosclerosis in patients with type 2 diabetes and periodontal disease. Kardiol Pol 70:7–13

    PubMed  Google Scholar 

  24. Hanaoka Y, Soejima H, Yasuda O, Nakayama H, Nagata M, Matsuo K, Shinohara M, Izumi Y, Ogawa H (2013) Level of serum antibody against a periodontal pathogen is associated with atherosclerosis and hypertension. Hypertens Res 36:829–833. https://doi.org/10.1038/hr.2013.46

    Article  PubMed  Google Scholar 

  25. Shanker J, Setty P, Arvind P, Nair J, Bhasker D, Balakrishna G, Kakkar VV (2013) Relationship between periodontal disease, Porphyromonas gingivalis, peripheral vascular resistance markers and coronary artery disease in Asian Indians. Thromb Res 132:e8–e14. https://doi.org/10.1016/j.thromres.2013.04.023

    Article  PubMed  Google Scholar 

  26. Kapellas K, Jamieson LM, Do LG, Bartold PM, Wang H, Maple-Brown LJ, Sullivan D, O'Dea K, Brown A, Celermajer DS, Slade GD, Skilton MR (2014) Associations between periodontal disease and cardiovascular surrogate measures among Indigenous Australians. Int J Cardiol 173:190–196. https://doi.org/10.1016/j.ijcard.2014.02.015

    Article  PubMed  Google Scholar 

  27. Houcken W, Teeuw WJ, Bizzarro S, Alvarez Rodriguez E, Mulders TA, van den Born BJ, Loos BG (2016) Arterial stiffness in periodontitis patients and controls. A case-control and pilot intervention study. J Hum Hypertens 30:24–29. https://doi.org/10.1038/jhh.2015.41

    Article  PubMed  Google Scholar 

  28. Nibali L, Donos N, Terranova V, Di Pino A, Di Marca S, Ferrara V, Pisano M, Scicali R, Rabuazzo AM, Purrello F, Malatino L (2019) Left ventricular geometry and periodontitis in patients with the metabolic syndrome. Clin Oral Investig 23:2695–2703. https://doi.org/10.1007/s00784-018-2667-8

    Article  PubMed  Google Scholar 

  29. Jockel-Schneider Y, Bechtold M, Haubitz I, Stork S, Fickl S, Harks I, Eigenthaler M, Vollrath O, Baulmann J, Schlagenhauf U (2018) Impact of anti-infective periodontal therapy on parameters of vascular health. J Clin Periodontol 45:354–363. https://doi.org/10.1111/jcpe.12849

    Article  PubMed  Google Scholar 

  30. Vidal F, Cordovil I, Figueredo CM, Fischer RG (2013) Non-surgical periodontal treatment reduces cardiovascular risk in refractory hypertensive patients: a pilot study. J Clin Periodontol 40:681–687. https://doi.org/10.1111/jcpe.12110

    Article  PubMed  Google Scholar 

  31. Kapellas K, Maple-Brown LJ, Jamieson LM, Do LG, O'Dea K, Brown A, Cai TY, Anstey NM, Sullivan DR, Wang H, Celermajer DS, Slade GD, Skilton MR (2014) Effect of periodontal therapy on arterial structure and function among aboriginal australians: a randomized, controlled trial. Hypertension 64:702–708. https://doi.org/10.1161/hypertensionaha.114.03359

    Article  PubMed  Google Scholar 

  32. Armitage GC (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4:1–6. https://doi.org/10.1902/annals.1999.4.1.1

    Article  PubMed  Google Scholar 

  33. Caton JG, Armitage G, Berglundh T, Chapple ILC, Jepsen S, Kornman KS, Mealey BL, Papapanou PN, Sanz M, Tonetti MS (2018) A new classification scheme for periodontal and peri-implant diseases and conditions - introduction and key changes from the 1999 classification. J Periodontol 89(Suppl 1):S1–S8. https://doi.org/10.1002/JPER.18-0157

    Article  PubMed  Google Scholar 

  34. Solowiej-Wedderburn J, Ide M, Pennington M (2017) Cost-effectiveness of non-surgical periodontal therapy for patients with type 2 diabetes in the UK. J Clin Periodontol 44:700–707. https://doi.org/10.1111/jcpe.12746

    Article  PubMed  Google Scholar 

  35. D'Aiuto F, Orlandi M, Gunsolley JC (2013) Evidence that periodontal treatment improves biomarkers and CVD outcomes. J Periodontol 84:S85–S105. https://doi.org/10.1902/jop.2013.134007

    Article  PubMed  Google Scholar 

  36. Ohkuma T, Ninomiya T, Tomiyama H, Kario K, Hoshide S, Kita Y, Inoguchi T, Maeda Y, Kohara K, Tabara Y, Nakamura M, Ohkubo T, Watada H, Munakata M, Ohishi M, Ito N, Nakamura M, Shoji T, Vlachopoulos C, Yamashina A, Collaborative Group for J-BAVEL (Japan Brachial-Ankle Pulse Wave Velocity Individual Participant Data Meta-Analysis of Prospective Studies) (2017) Brachial-ankle pulse wave velocity and the risk prediction of cardiovascular disease: an individual participant data meta-analysis. Hypertension 69:1045–1052. https://doi.org/10.1161/HYPERTENSIONAHA.117.09097

    Article  PubMed  Google Scholar 

  37. Tanaka H, Munakata M, Kawano Y, Ohishi M, Shoji T, Sugawara J, Tomiyama H, Yamashina A, Yasuda H, Sawayama T, Ozawa T (2009) Comparison between carotid-femoral and brachial-ankle pulse wave velocity as measures of arterial stiffness. J Hypertens 27:2022–2027. https://doi.org/10.1097/HJH.0b013e32832e94e7

    Article  PubMed  Google Scholar 

  38. Tonetti MS, D'Aiuto F, Nibali L, Donald A, Storry C, Parkar M, Suvan J, Hingorani AD, Vallance P, Deanfield J (2007) Treatment of periodontitis and endothelial function. N Engl J Med 356:911–920. https://doi.org/10.1056/NEJMoa063186

    Article  PubMed  Google Scholar 

  39. Reyes L, Herrera D, Kozarov E, Rolda S, Progulske-Fox A (2013) Periodontal bacterial invasion and infection: contribution to atherosclerotic pathology. J Periodontol 84:S30–S50. https://doi.org/10.1902/jop.2013.1340012

    Article  PubMed  Google Scholar 

  40. Schenkein HA, Loos BG (2013) Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases. J Periodontol 84:S51–S69. https://doi.org/10.1902/jop.2013.134006

    Article  PubMed  Google Scholar 

  41. Teeuw WJ, Slot DE, Susanto H, Gerdes VE, Abbas F, D'Aiuto F, Kastelein JJ, Loos BG (2014) Treatment of periodontitis improves the atherosclerotic profile: a systematic review and meta-analysis. J Clin Periodontol 41:70–79. https://doi.org/10.1111/jcpe.12171

    Article  PubMed  Google Scholar 

  42. Gurav AN (2014) The implication of periodontitis in vascular endothelial dysfunction. Eur J Clin Investig 44:1000–1009. https://doi.org/10.1111/eci.12322

    Article  Google Scholar 

  43. D'Aiuto F, Nibali L, Parkar M, Patel K, Suvan J, Donos N (2010) Oxidative stress, systemic inflammation, and severe periodontitis. J Dent Res 89:1241–1246. https://doi.org/10.1177/0022034510375830

    Article  PubMed  PubMed Central  Google Scholar 

  44. Schenkein HA, Papapanou PN, Genco R, Sanz M (2020) Mechanisms underlying the association between periodontitis and atherosclerotic disease. Periodontol 2000 83:90–106. https://doi.org/10.1111/prd.12304

    Article  PubMed  Google Scholar 

  45. Mancia G, Fagard R, Narkiewicz K, Redon J, Zanchetti A, Bohm M, Christiaens T, Cifkova R, De Backer G, Dominiczak A, Galderisi M, Grobbee DE, Jaarsma T, Kirchhof P, Kjeldsen SE, Laurent S, Manolis AJ, Nilsson PM, Ruilope LM, Schmieder RE, Sirnes PA, Sleight P, Viigimaa M, Waeber B, Zannad F, Redon J, Dominiczak A, Narkiewicz K, Nilsson PM, Burnier M, Viigimaa M, Ambrosioni E, Caufield M, Coca A, Olsen MH, Schmieder RE, Tsioufis C, van de Borne P, Zamorano JL, Achenbach S, Baumgartner H, Bax JJ, Bueno H, Dean V, Deaton C, Erol C, Fagard R, Ferrari R, Hasdai D, Hoes AW, Kirchhof P, Knuuti J, Kolh P, Lancellotti P, Linhart A, Nihoyannopoulos P, Piepoli MF, Ponikowski P, Sirnes PA, Tamargo JL, Tendera M, Torbicki A, Wijns W, Windecker S, Clement DL, Coca A, Gillebert TC, Tendera M, Rosei EA, Ambrosioni E, Anker SD, Bauersachs J, Hitij JB, Caulfield M, De Buyzere M, De Geest S, Derumeaux GA, Erdine S, Farsang C, Funck-Brentano C, Gerc V, Germano G, Gielen S, Haller H, Hoes AW, Jordan J, Kahan T, Komajda M, Lovic D, Mahrholdt H, Olsen MH, Ostergren J, Parati G, Perk J, Polonia J, Popescu BA, Reiner Z, Ryden L, Sirenko Y, Stanton A, Struijker-Boudier H, Tsioufis C, van de Borne P, Vlachopoulos C, Volpe M, Wood DA (2013) 2013 ESH/ESC guidelines for the management of arterial hypertension: the Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Eur Heart J 34:2159–2219. https://doi.org/10.1093/eurheartj/eht151

    Article  PubMed  Google Scholar 

  46. Stewart J, Manmathan G, Wilkinson P (2017) Primary prevention of cardiovascular disease: a review of contemporary guidance and literature. JRSM Cardiovasc Dis 6:2048004016687211. https://doi.org/10.1177/2048004016687211

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We contacted several authors by email to clarify points of their already published respective studies. We would like to warmly thank both Dr. Yvonne Jockel-Schneider for her response to our requests and Dr. Anandhara Indriani, Dr. Purnamasari’s assistant, for the response and additional data that were provided to us.

Funding

No external funding, apart from the support of the authors’ institutions, was received for this study.

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Author notes

  1. Christelle Darnaud and Alexandre Courtet contributed equally to this work.

Authors and Affiliations

  1. Department of Periodontology, Service of Odontology, Rothschild Hospital, AP-HP, Paris 7 - UFR Odontologie-Garancière, University of Paris, 5, rue Garancière, 75006, Paris, France

    Christelle Darnaud, Alexandre Courtet, Audrey Schmitt, Philippe Bouchard & Maria Clotilde Carra

  2. UMR-S970, Department of Epidemiology, Paris Cardiovascular Research Center, Paris, France

    Christelle Darnaud & Pierre Boutouyrie

  3. Medicine Faculty, Paris Descartes - Sorbonne Paris Cité University, Paris, France

    Pierre Boutouyrie

  4. AP-HP, Georges Pompidou European Hospital, INSERM U970, Paris 5 - Descartes University, Paris, France

    Pierre Boutouyrie

  5. EA 2496, U.F.R. of Odontology, Paris 5 - Descartes University, Paris, France

    Philippe Bouchard

  6. Population-based Epidemiologic Cohorts Unit, Inserm, UMS 011, Villejuif, France

    Maria Clotilde Carra

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  1. Christelle Darnaud
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Correspondence to Maria Clotilde Carra.

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Darnaud, C., Courtet, A., Schmitt, A. et al. Association between periodontitis and pulse wave velocity: a systematic review and meta-analysis. Clin Oral Invest 25, 393–405 (2021). https://doi.org/10.1007/s00784-020-03718-2

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