Decreased frequency and duration of tooth brushing is a risk factor for endothelial dysfunction



      Periodontal disease is associated with endothelial dysfunction, leading to cardiovascular disease. The effect of detailed tooth brushing behavior, not only frequency but also duration of tooth brushing, on endothelial function is unclear. The purpose of this study was to evaluate the relationships of detailed methods of tooth brushing with vascular function.


      We evaluated flow-mediated vasodilation (FMD), nitroglycerine-induced vasodilation, and frequency and duration of tooth brushing in 896 subjects. We divided the subjects into three groups according to the frequency and duration of tooth brushing: low frequency and short duration group (<twice/day and <2 min/procedure), low frequency or short duration group (<twice/day or <2 min/procedure), non-low frequency and non-short duration group (≥twice/day and ≥2 min/procedure).


      FMD in the low frequency and short duration group was significantly lower than FMD in the low frequency or short duration group and FMD in the non-low frequency and non-short duration group [3.1 (2.7)% vs. 4.2 (3.1)% and 4.7 (3.1)%, P = 0.001 and <0.001, respectively]. Nitroglycerine-induced vasodilation was similar in the three groups. Using the non-low frequency and non-short duration group as the reference, the low frequency and short duration of tooth brushing group was significantly associated with an increased odds ratio of a low FMD tertile after adjustment for conventional risk factors (OR: 2.25, 95% CI: 1.39–3.59; P < 0.001).


      These findings suggest that low frequency and short duration of tooth brushing are associated with endothelial dysfunction.
      Clinical trial registration information: URL for clinical trial: http://UMIN; registration number for clinical trial: UMIN000003409.


      To read this article in full you will need to make a payment


      Subscribe to International Journal of Cardiology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Mattila K.J.
        • Nieminen M.S.
        • Valtonen V.V.
        • et al.
        Association between dental health and acute myocardial infarction.
        BMJ. 1989; 298: 779-781
        • 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: 688-691
        • Spahr A.
        • Klein E.
        • Khuseyinova N.
        • et al.
        Periodontal infections and coronary heart disease: role of periodontal bacteria and importance of total pathogen burden in the Coronary Event and Periodontal Disease (CORODONT) study.
        Arch. Intern. Med. 2006; 166: 554-559
        • Wu T.
        • Trevisan M.
        • Genco R.J.
        • Dorn J.P.
        • Falkner K.L.
        • Sempos C.T.
        Periodontal disease and risk of cerebrovascular disease: the first national health and nutrition examination survey and its follow-up study.
        Arch. Intern. Med. 2000; 160: 2749-2755
        • Reyes L.
        • Herrera D.
        • Kozarov E.
        • Rolda S.
        • Progulske-Fox A.
        Periodontal bacterial invasion and infection: contribution to atherosclerotic pathology.
        J. Periodontol. 2013; 84: S30-S50
        • Schenkein H.A.
        • Loos B.G.
        Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases.
        J. Periodontol. 2013; 84: S51-S69
        • De Oliveira C.
        • Watt R.
        • Hamer M.
        Toothbrushing, inflammation, and risk of cardiovascular disease: results from Scottish Health Survey.
        BMJ. 2010; 340: c2451
        • Ross R.
        Atherosclerosis: an inflammatory disease.
        N. Engl. J. Med. 1999; 340: 115-126
        • Higashi Y.
        • Noma K.
        • Yoshizumi M.
        • Kihara Y.
        Oxidative stress and endothelial function in cardiovascular diseases (review).
        Circ. J. 2009; 73: 411-418
        • Celermajer D.S.
        • Sorensen K.E.
        • Gooch V.M.
        • et al.
        Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis.
        Lancet. 1992; 340: 1111-1115
        • Celermajer D.S.
        • Sorensen K.E.
        • Bull C.
        • Robinson J.
        • Deanfield J.E.
        Endothelium-dependent dilation in the systemic arteries of asymptomatic subjects relates to coronary risk factors and their interaction.
        J. Am. Coll. Cardiol. 1994; 24: 1468-1474
        • Benjamin E.J.
        • Larson M.G.
        • Keyes M.J.
        • et al.
        Clinical correlates and heritability of flow-mediated dilation in the community: the Framingham Heart Study.
        Circulation. 2004; 109: 613-619
        • Idei N.
        • Nishioka K.
        • Soga J.
        • et al.
        Vascular function and circulating progenitor cells in thromboangiitis obliterans (Buerger's disease) and atherosclerosis obliterans.
        Hypertension. 2011; 57: 70-78
        • Soga J.
        • Noma K.
        • Hata T.
        • ROCK Study Group
        • et al.
        Rho-associated kinase activity, endothelial function, and cardiovascular risk factors.
        Arterioscler. Thromb. Vasc. Biol. 2011; 31: 2353-2359
        • Modena M.G.
        • Bonetti L.
        • Coppi F.
        • Bursi F.
        • Rossi R.
        Prognostic role of reversible endothelial dysfunction in hypertensive postmenopausal women.
        J. Am. Coll. Cardiol. 2002; 40: 505-510
        • Gokce N.
        • Keaney Jr., J.F.
        • Hunter L.M.
        • Watkins M.T.
        • Menzoian J.O.
        • Vita J.A.
        Risk stratification for postoperative cardiovascular events via noninvasive assessment of endothelial function: a prospective study.
        Circulation. 2002; 105: 1567-1572
        • Brevetti G.
        • Silvestro A.
        • Schiano V.
        • Chiariello M.
        Endothelial dysfunction and cardiovascular risk prediction in peripheral arterial disease: additive value of flow-mediated dilation to ankle-brachial pressure index.
        Circulation. 2003; 108: 2093-2098
        • Lerman A.
        • Zeiher A.M.
        Endothelial function: cardiac events.
        Circulation. 2005; 111: 363-368
        • Yeboah J.
        • Folsom A.R.
        • Burke G.L.
        • et al.
        Predictive value of brachial flow-mediated dilation for incident cardiovascular events in a population-based study: the multi-ethnic study of atherosclerosis.
        Circulation. 2009; 120: 502-509
        • Amar S.
        • Gokce N.
        • Morgan S.
        • Loukideli M.
        • Van Dyke T.E.
        • Vita J.A.
        Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation.
        Arterioscler. Thromb. Vasc. Biol. 2003; 23: 1245-1249
        • Blum A.
        • Kryuger K.
        • Mashiach Eizenberg M.
        • et al.
        Periodontal care may improve endothelial function.
        Eur. J. Intern. Med. 2007; 18: 295-298
        • Tonetti M.S.
        • D'Aiuto F.
        • Nibali L.
        • et al.
        Treatment of periodontitis and endothelial function.
        N. Engl. J. Med. 2007; 356: 911-920
        • Higashi Y.
        • Goto C.
        • Jitsuiki D.
        • et al.
        Periodontal infection is associated with endothelial dysfunction in healthy subjects and hypertensive patients.
        Hypertension. 2008; 51: 446-453
        • Higashi Y.
        • Goto C.
        • Hidaka T.
        • et al.
        Oral infection-inflammatory pathway, periodontitis, is a risk factor for endothelial dysfunction in patients with coronary artery disease.
        Atherosclerosis. 2009; 206: 604-610
        • Seinost G.
        • Wimmer G.
        • Skerget M.
        • et al.
        Periodontal treatment improves endothelial dysfunction in patients with severe periodontitis.
        Am. Heart J. 2005; 149: 1050-1054
        • Ghiadoni L.
        • Virdis A.
        • Magagna A.
        • Taddei S.
        • Salvetti A.
        Effect of the angiotensin II type 1 receptor blocker candesartan on endothelial function in patients with essential hypertension.
        Hypertension. 2000; 35: 501-506
        • Wolfrum S.
        • Jensen K.S.
        • Liao J.K.
        Endothelium-dependent effects of statins.
        Arterioscler. Thromb. Vasc. Biol. 2003; 23: 729-736
        • Martens F.M.
        • Rabelink T.J.
        • op 't Roodt J.
        • de Koning E.J.
        • Visseren F.L.
        TNF-alpha induces endothelial dysfunction in diabetic adults, an effect reversible by the PPAR-gamma agonist pioglitazone.
        Eur. Heart J. 2006; 27: 1605-1609
        • Higashi Y.
        • Oshima T.
        • Ozono R.
        • Watanabe M.
        • Matsuura H.
        • Kajiyama G.
        Effects of l-arginine infusion on renal hemodynamics in patients with mild essential hypertension.
        Hypertension. 1995; 25: 898-902
        • Sanada M.
        • Higashi Y.
        • Sasaki S.
        • et al.
        Relationship between the angiotensin-converting enzyme genotype and forearm vasodilator response to estrogen replacement therapy in postmenopausal women.
        J. Am. Coll. Cardiol. 2001; 37: 1529-1535
        • Goto C.
        • Higashi Y.
        • Kimura M.
        • et al.
        The effect of different intensities of exercise on endothelium-dependent vasodilation in humans: role of endothelium-dependent nitric oxide and oxidative stress.
        Circulation. 2003; 108: 530-535
        • Kajikawa M.
        • Nakashima A.
        • Maruhashi T.
        • et al.
        Poor oral health, that is, decreased frequency of tooth brushing, is associated with endothelial dysfunction.
        Circ. J. 2014; 78: 950-954
        • American Diabetes Association
        Clinical practice recommendations 1999.
        Diabetes Care. 1999; 22: S1-S114
        • Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults
        Executive summary of the third report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III).
        JAMA. 2001; 285: 2486-2497
        • Sjölander A.
        • Greenland S.
        Ignoring the matching variables in cohort studies — when is it valid and why?.
        Stat. Med. 2013; 32: 4696-4708
        • Bhagat K.
        • Vallance P.
        Inflammatory cytokines impair endothelium-dependent dilatation in human veins in vivo.
        Circulation. 1997; 96: 3042-3047
        • Libby P.
        • Ridker P.M.
        • Maseri A.
        Inflammation and atherosclerosis.
        Circulation. 2002; 105: 1135-1143
        • Yoshizumi M.
        • Perrella M.A.
        • Burnett Jr., J.C.
        • Lee M.E.
        Tumor necrosis factor downregulates an endothelial nitric oxide synthase mRNA by shortening its half-life.
        Circ. Res. 1993; 73: 205-209
        • Verma S.
        • Wang C.H.
        • Li S.H.
        • et al.
        A self-fulfilling prophecy: C-reactive protein attenuates nitric oxide production and inhibits angiogenesis.
        Circulation. 2002; 106: 913-919
        • Kofler S.
        • Nickel T.
        • Weis M.
        Role of cytokines in cardiovascular diseases: a focus on endothelial responses to inflammation.
        Clin. Sci. 2005; 108: 205-213
        • Wang P.
        • Ba Z.F.
        • Chaudry I.H.
        Administration of tumor necrosis factor-alpha in vivo depresses endothelium-dependent relaxation.
        Am. J. Phys. 1994; 266: 2535-2541
        • Venugopal S.K.
        • Devaraj S.
        • Yuhanna I.
        • Shaul P.
        • Jialal I.
        Demonstration that C-reactive protein decreases eNOS expression and bioactivity in human aortic endothelial cells.
        Circulation. 2002; 106: 1439-1441
        • Bokhari S.A.
        • Khan A.A.
        • Butt A.K.
        • et al.
        Non-surgical periodontal therapy reduces coronary heart disease risk markers: a randomized controlled trial.
        J. Clin. Periodontol. 2012; 39: 1065-1074
        • D'Aiuto F.
        • Parkar M.
        • Nibali L.
        • Suvan J.
        • Lessem J.
        • Tonetti M.S.
        Periodontal infections cause changes in traditional and novel cardiovascular risk factors: results from a randomized controlled clinical trial.
        Am. Heart J. 2006; 151: 977-984
        • Wainwright J.
        • Sheiham A.
        An analysis of methods of toothbrushing recommended by dental associations, toothpaste and toothbrush companies and in dental texts.
        Br. Dent. J. 2014; 217E5