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(Hypertension. 2003;41:488.)
© 2003 American Heart Association, Inc.
Scientific Contributions |
From Dipartimento Malattie Cardiovascolari, Università degli Studi di Perugia and Ospedale R. Silvestrini (F.A., P.V., L.P., M.B.), Perugia; and Università degli Studi di Perugia, Corso di Laurea in Odontoiatria e Protesi Dentaria (C.P., R.G.P., G.P., C.G., S.C.), Perugia, Italy.
Correspondence to Fabio Angeli, MD, Via Eugubina n. 68 A/8, 06100 Perugia, Italy. E-mail fangeli{at}cardionet.it
| Abstract |
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6 mm) (overall F 51.2; P<0.0001). Body surface area (P=0.04), systolic (P<0.0001) and diastolic (P<0.01) blood pressure, and left ventricular mass (P<0.0001) were determinants of a composite of CPITN 3 and 4. In a multivariate logistic analysis, left ventricular mass was the sole determinant (P<0.0001) of CPITN stages 3 and 4. Our findings suggest a direct association between severity of periodontitis and left ventricular mass in subjects with essential hypertension. Periodontal evaluation might contribute to refine cardiovascular risk assessment in hypertensive subjects.
Key Words: hypertension, essential left ventricular hypertrophy periodontal disease left ventricular mass echocardiography
| Introduction |
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Prevalence of periodontal disease approaches 14% over a wide age span, including younger and elderly people.1 Periodontitis begins with a loss of alveolar bone and subsequent formation of a pocked around the tooth, the final stage being tooth mobility and loss.2 Periodontal pocket can be detected with a periodontal probe and estimated through measurement of distance from gingival margin to the base of the periodontal pocket.3 In a healthy periodontium, there is no loss of epithelial attachment or pocket formation, and the gingival crevice is <2 mm deep.3 Established risk factors for periodontal disease are dental plaque, calculus, age, genetics, smoking, and diabetes.4
At least 9 cohort studies513 examined the association between periodontal disease and coronary heart disease (CHD), with conflicting results. An overview of these studies14 showed a 15% excess risk of CHD in association with periodontal disease, with 95% confidence intervals ranging from 8% to 122%. To define the underlying mechanisms of such association, several studies, reviewed in depth by Armitage,15 examined the potential link between periodontal disease and cardiovascular risk factors, including diabetes, smoking, hyperlipidemia, and hypertension. Surprisingly, despite the high prevalence of hypertension in the general population and its leading prognostic importance, few data are available on the relation between elevated blood pressure (BP), hypertensive organ damage, and periodontal disease. Castelli et al16 found a proliferation of the intima and elastic layers with lumen reduction of vessels feeding the periodontal membrane in hypertensive subjects.16 In another study, tooth position and movements were affected by the force of BP transmitted through periodontal vessels.17 Interestingly, periodontal pulsation reflected changes in pulse pressure rather than in mean BP.17
Left ventricular (LV) mass is abnormally increased in about one third of people with hypertension,18 and LV hypertrophy is associated with an excess risk of cardiovascular complications independently of BP and other risk factors.18 There is also growing evidence that serial changes in LV hypertrophy are independent predictor of outcome.19,20
In view of the high prevalence and the potential interrelationship among elevated BP, cardiac organ damage, and periodontal disease as determinants of cardiovascular risk, we conducted the present study to examine the relation of periodontal disease to BP and LV mass (LVM) in a cohort of subjects with essential hypertension. To eliminate any interference by previous treatment on LVM,21 only never-treated subjects were included.
| Methods |
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140 mm Hg and/or diastolic BP
90 mm Hg in 3 different visits over 1 month. None of the subjects had been previously treated or screened for hypertension. We used the average of 3 consecutive BP readings taken at distance of
1 minute. None of the subjects had secondary hypertension, important concomitant disease, or heart failure on the base of clinic visit, medical histories, physical examinations, 12-lead ECG, laboratory test, and echocardiographic study. To exclude a possible misleading factor, another inclusion criteria was a history of good oral hygiene. Each subject used to brush the tooth at least twice daily, generally with fluoride toothpaste. Subjects made also regular use of flossing in order to achieve a more effective interdental, and most of them were examined by a dentist at every 6 to 12 months, following accurate preventive instructions for low intake of hypercaloric food and limiting the use of cigarettes.
Echocardiography
The M-mode echocardiographic study of LV was performed according to the American Society of Echocardiography recommendations.22 The mean value from at least 5 measurements was computed. Relative wall thickness was calculated as twice the end-diastolic posterior wall thickness divided by end-diastolic diameter. LVM was calculated according to Devereux et al23 and normalized by height elevated to 2.7 (LVM/h2.7) according to De Simone et al.24
Dental Examination
To assess periodontal condition we used the World Health Organization (WHO) community periodontal index of treatment needs (CPITN) and the specially designed WHO periodontal probe with a sensing force of not >20 g.25 Briefly, the mouth of each patient was divided into sextants (see Figure 1 for details), and each sextant was examined only if there were
2 teeth present and not indicated for extraction; the teeth examined were 17, 16, 11, 26, 27, 47, 46, 31, 36, and 37; for each sextant we recorded the highest index found according to the following score: 0, periodontal health; 1, gingival bleeding; 2, calculus detected during probing; 3, pocket 4- to 5-mm depth; and 4, pocket
6-mm depth. Periodontal condition of every patient is reported as the worst sextant CPITN condition.
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Data Analysis
We used SPSS, lease 9.0 (SPSS Inc) for statistical analysis. Data are presented as mean (±SD) or frequency in percentage. Differences between groups were performed by 1-way ANOVA or
2 analysis when appropriate. Univariate and multiple logistic regression analyses were used to test the relationship of clinical and echocardiographic parameters to moderate-to-severe periodontitis and to determine the probability of a composite of moderate-to-severe periodontitis expressed by a CPITN 3 or 4. Thus, CPITN stage 3 or 4 was coded as 1, and CPITN stage 0, 1, or 2 was coded as 0 in the logistic regression analysis. In 2-tailed tests, P<0.05 were considered significant.
| Results |
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In a logistic regression analysis (Table 2), we tested the univariate association between each single clinical and echocardiographic variable with moderate-to-severe periodontal disease as indicated by a composite of CPITN 3 to 4. Body surface area, systolic and diastolic BP, interventricular septum, LV posterior wall, LV internal diameter, relative wall thickness, and LVM showed an association (all, P<0.05) with moderate-to-severe periodontal disease. In a multivariate logistic regression analysis, only LVM (Table 3) maintained an independent association (P<0.0001) with periodontal disease CPITN 3 to 4. Body surface area, systolic BP, and diastolic BP did not achieve significance to enter the model. In an additional model that included interventricular septum (P=0.076), LV internal diameter (P=0.168), posterior wall thickness (P=0.303), and LVM (P=0.028), only LVM achieved significance.
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The progressive increase in LVM with periodontal status and the prevalence of moderate-to-severe periodontitis in the 4 quartiles of LVM (<39.0, 39.0 to 41.9, 42.0 to 53.9,
54.0) are depicted in Figure 2. Subjects in the fourth quartile of LVM/height2.7 showed the highest probability (85%) of moderate-to-severe periodontitis.
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| Discussion |
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Periodontitis and Cardiovascular Disease
Over the past few years, several epidemiologic studies examined the potential association between periodontal and cardiovascular disease.513 Infections of periodontal structure could accelerate atherosclerosis by promoting a systemic inflammatory status through release of endotoxins, heat-shock proteins, or acute-phase reactants.26,27
Periodontitis and cardiovascular disease might also share some explanatory risk factors such as diabetes mellitus, smoking, and dyslipidemia.15 Poor glycemic control is an established risk factor for periodontitis, and patients with diabetes mellitus are at increased risk of edentulia.28 A possible basic mechanism could be the thickening of basement membranes of small vessels in diabetics, leading to reduced transport of oxygen and nutritional substances across the vessels walls.28 Cigarette smoking is also associated with periodontitis,29,30 and the underlying mechanisms include an inhibited neutrophil function in saliva and connective tissue, as well as a defective Ig2 antibody response.29,30 Part of the association between periodontitis and CHD has been attributed to cigarette smoking as a confounding factor.31 The association between elevated LDL cholesterol and periodontal disease seems to hold mostly in the male sex.31
Periodontitis and Hypertension
Despite the high prevalence of hypertension in the general population and its leading prognostic importance, only a few studies addressed the relation between BP and periodontal disease.16,17 In the present study, systolic BP progressively increased with severity of periodontal disease, whereas diastolic BP did not show any significant changes. LVM showed also a progressive increase with the severity of periodontal disease. Because of the likelihood of residual confounding, we tested whether the association between LVM and periodontal disease was independent of BP. Indeed, the multivariate logistic regression analysis showed that LVM was an independent predictor of moderate-to-severe periodontitis.
The potential mechanisms underlying the association between LVM and periodontitis remain speculative. In hypertensive subjects, hypertrophic heart and periodontium may share microcirculatory dysfunction and arteriolar and capillary rarefaction.32,33 Pressure overload could be involved at a time in inducing development of LV hypertrophy and generalized narrowing of the luminal diameter of microvessels. The resulting vascular rarefaction may lead to ischemia at cardiac and periodontal level. Because office BP determined by conventional sphygmomanometry is subject to important intrasubject and intersubject variability, increased LVM and periodontal disease may represent more stable biological assays, reflecting chronically elevated BP levels. Insulin resistance might be another potential mechanism involved in the pathogenesis of LV hypertrophy in subjects with periodontitis, but further research is needed to verify such hypothesis.34 In a previous study from our laboratory, insulin and insulin growth factor I were independent determinants of LVM and geometry in subjects with essential hypertension, and such relation was independent of office and ambulatory BP.35 Unfortunately, insulin resistance was not assessed in the present study.
Some limitations of this study deserve mention. Ambulatory BP, which is more accurate than office BP to predict the degree of LV hypertrophy,36 was not measured. Use of ambulatory BP might provide a more restrictive assessment of the association between LVM and periodontal disease. Furthermore, because all subjects were white, caution is needed in extrapolating results to different ethnic groups.
Clinical Implications
Our findings have clinical implications. It is widely established that LVM is associated with an increased risk of a variety of adverse cardiovascular events independently of BP levels.18,37,38 Our data suggest that periodontal disease can provide an easily accessible biological assay for a more accurate definition of cardiovascular risk profile in individual subjects. Thus, a simple periodontal evaluation might be useful to refine cardiovascular risk assessment in hypertensive subjects.
Perspectives
We found an association between periodontal disease, expressed by the CPITN and LVM in untreated subjects with essential hypertension. Such association was independent of BP and other determinants of LVM. Although the present study was not designed to investigate the potential mechanisms underlying the association between periodontal disease and LVM, it is tempting to speculate that pressure overload might accelerate microcirculatory changes leading to capillary rarefaction and subsequent ischemia at both periodontal and cardiac level. Periodontal disease could provide an easily accessible biological assay for a more accurate definition of cardiovascular risk profile in individual subjects.
Received September 26, 2002; first decision October 22, 2002; accepted January 3, 2003.
| References |
|---|
|
|
|---|
2. Chapple IL. Periodontal disease diagnosis: current status and future developments. J Dent. 1997; 25: 315.[CrossRef][Medline] [Order article via Infotrieve]
3. McLeod DE. A practical approach to the diagnosis and treatment of periodontal disease. J Am Dent Assoc. 2000; 131: 483491.
4. Page RC, Krall EA, Martin J, Mancl L, Garcia RI. Validity and accuracy of a risk calculator in predicting periodontal disease. J Am Dent Assoc. 2002; 133: 569576.
5. Genco R, Offenbacher S, Beck J. Periodontal disease and cardiovascular disease: epidemiology and possible mechanisms. J Am Dent Assoc. 2002; 133: 14S22S.
6. Hujoel PP, Drangsholt M, Spiekerman C, DeRouen TA. Pre-existing cardiovascular disease and periodontitis: a follow-up study. J Dent Res. 2002; 81: 186191.
7. Mattila KJ, Valtonen VV, Nieminen M, Huttunen JK. Dental infection and the risk of new coronary events: prospective study of patients with documented coronary artery disease. Clin Infect Dis. 1995; 20: 588592.[Medline] [Order article via Infotrieve]
8. Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S. Periodontal disease and cardiovascular disease. J Periodont. 1996; 67: 11231137.[Medline] [Order article via Infotrieve]
9. Morrison HI, Ellison LF, Taylor GW. Periodontal disease and risk of fatal coronary heart and cerebrovascular diseases. J Cardiovasc Risk. 1999; 6: 711.[Medline] [Order article via Infotrieve]
10. Hujoel PP, Drangsholt M, Spiekerman C, DeRouen TA. Periodontal disease and coronary heart disease risk. JAMA. 2000; 284: 14061410.
11. DeStefano F, Anda RFH, Kahn S, Williamson DF, Russell CM. Dental disease and risk of coronary heart disease and mortality. BMJ. 1993; 306: 668691.
12. Joshipura KJ, Rimm EB, Douglass CW, Trichopoulos D, Ascherio A, Willet WC. Poor oral health and coronary heart disease. J Dent Res. 1996; 75: 16311636.
13. Howell TH, Ridker PM, Ajani UA, hennekens CH, Christen WG. Periodontal disease and risk of subsequent cardiovascular disease in US male physicians. J Am Coll Cardiol. 2001; 37: 445450.
14. Hujoel PP. Does chronic periodontitis cause coronary heart disease? J Am Dent Assoc. 2002; 133: 31S36S.
15. Armitage GC. Periodontal infections and cardiovascular disease-how strong is the association? Oral Disease. 2000; 6: 335350.
16. Castelli WA, Diaz-Perez R, Nasjleti CE, Caffesse RG. Effect of renovascular hypertension of the morphology of oral blood vessels. Oral Surg Oral Med Oral Pathol. 1978; 46: 576582.[CrossRef][Medline] [Order article via Infotrieve]
17. Ioi H, Nakata S, Nakasima A, Counts AL, Nanda RS. Changes in tooth position in humans in relation to arterial blood pressure. Arch Oral Biol. 2002; 47: 219226.[CrossRef][Medline] [Order article via Infotrieve]
18. Devereux RB, Roman MJ. Hypertensive cardiac hypertrophy: pathophysiologic and clinical characteristics. In: Laragh JH, Brenner BM, eds. Hypertension: Pathophysiology, Diagnosis and Management. 2nd ed. New York, NY: Raven Press; 1995: 409424.
19. Muiesan ML, Salvetti M, Rizzoni D, Castellano M, Donato F, Agabiti-Rosei E. Association of change in left ventricular mass with prognosis during long-term antihypertensive treatment. J Hypertens. 1995; 13: 10911095.[CrossRef][Medline] [Order article via Infotrieve]
20. Verdecchia P, Schillaci G, Borgioni C, Ciucci A, Gattobigio R, Zampi I, Reboldi G, Porcellani C. Prognostic significance of serial changes in left ventricular mass in essential hypertension. Circulation. 1998; 97: 4854.
21. Schmieder RE, Schlaich MP, Klingbeil AU, Martus P. Update on reversal of left ventricular hypertrophy in essential hypertension: a meta-analysis of all randomized double-blind studies until December 1996. Nephrol Dial Transplant. 1998; 13: 564569.
22. Sahn D, DeMaria A, Kisslo J, Weyman A. The committee on M-mode standardization of the American Society of Echocardiography: recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation. 1978; 58: 10721083.
23. Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N. Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol. 1986; 57: 450458.[CrossRef][Medline] [Order article via Infotrieve]
24. De Simone G, Devereux RB, Daniels SR, Koren MJ, Meyer RA, Laragh JH. Effect of growth on variability of left ventricular mass: assessment of allometric signals in adults and children and their capacity to predict cardiovascular risk. J Am Coll Cardiol. 1995; 25: 10561062.[Abstract]
25. Ainamo J, Barmes D, Beagrie G, Cutress T, Martin J, Sardo-Infirri J. Development of the World Health Organization (WHO) community periodontal index of treatment needs (CPITN). Int Dent J. 1982; 32: 281291.[Medline] [Order article via Infotrieve]
26. Offenbacher S, Madianos PN, Champagne CM, Southerland JH, Paquette DW, Williams RC, Slade G, Beck JD. Periodontitisatherosclerosis syndrome: an expanded model of pathogenesis. J Periodont Res. 1990; 34: 346352.
27. Scannapieco FA, Genco RJ. Association of periodontal infections with atherosclerotic and pulmonary diseases. J Periodont Res. 1999; 34: 340345.[CrossRef][Medline] [Order article via Infotrieve]
28. Noack B, Jachmann I, Roscher S, Sieber L, Kopprasch S, Luck C, Hanefeld M, Hoffmann T. Metabolic diseases and their possible link to risk indicators of periodontitis. J Periodont. 2000; 71: 898903.[Medline] [Order article via Infotrieve]
29. Bennet KR, Reade PC. Salivary immunoglobulin A levels in normal subjects, tobacco smokers, and patients with minor aphthous ulcerations. Oral Surg Oral Med Oral Pathol. 1982; 53: 461465.[CrossRef][Medline] [Order article via Infotrieve]
30. Payne JB, Johnson GK, Reinhardt RA, Dyer JK, Maze CA, Dunning DG. Nicotine effects on PGE2 and IL-1-ß release by LPS-treated human monocytes. J Periodontal Res. 1996; 31: 99104.[CrossRef][Medline] [Order article via Infotrieve]
31. Katz J, Flugelman Y, Goldberg A, Heft M. Association between periodontal pockets and elevated cholesterol and low-density lipoprotein cholesterol levels. J Periodontol. 2002; 73: 494500.[CrossRef][Medline] [Order article via Infotrieve]
32. Sernè EH, Gans R OB, Maaten JC, Tangelder G, Donker JM, Stehouwer C. Impaired skin capillary recruitment in essential hypertension is caused by both functional and structural capillary rarefaction. Hypertension. 2001; 38: 238242.
33. Chapple CC, Kumar RK, Hunter N. Vascular remodelling in chronic inflammatory periodontal disease. J Oral Pathol Med. 2000; 29: 500506.[CrossRef][Medline] [Order article via Infotrieve]
34. Donahue RP, Wu T. Insulin resistance and periodontal disease: an epidemiologic overview of research and future directions. Ann Periodontol. 2001; 6: 119124.[CrossRef][Medline] [Order article via Infotrieve]
35. Verdecchia P, Reboldi G, Schillaci G, Borgioni C, Ciucci A, Telera MP, Santeusanio F, Porcellani C, Brunetti P. Circulating insulin and insulin-growth-factor-1 are independent determinants of left ventricular mass and geometry in essential hypertension. Circulation. 1999; 100: 18021807.
36. Verdecchia P. Prognostic value of ambulatory blood pressure: current evidence and clinical implications. Hypertension. 2000; 35: 844851.
37. Koren MJ, Devereux RB, Casale PN, Savage DD, Laragh JH. Role of left ventricular mass and geometry to morbidity and mortality in uncomplicated essential hypertension. Ann Intern Med. 1991; 114: 345352.
38. Levy D, Garrison RJ, Savage DD, Kannel WB, Castelli WP. Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N Engl J Med. 1990; 322: 15611566.[Abstract]
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