This Article Abstract Full Text (PDF) All Versions of this Article: 35/2/496    most recent 01.STR.0000110789.20526.9Dv1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Grau, A. J. Articles by Dörfer, C. E. Search for Related Content PubMed PubMed Citation Articles by Grau, A. J. Articles by Dörfer, C. E. Related Collections Risk Factors for Stroke

(Stroke. 2004;35:496.)
© 2004 American Heart Association, Inc.

Original Contributions

Periodontal Disease as a Risk Factor for Ischemic Stroke

Armin J. Grau, MD; Heiko Becher, PhD; Christoph M. Ziegler, MD, DDS; Christoph Lichy, MD; Florian Buggle, MD; Claudia Kaiser; Rainer Lutz, MD; Stefan Bültmann, MD; Michael Preusch, Cand Med Christof E. Dörfer, DDS

From the Department of Neurology (A.J.G., C.L., F.B., S.B., M.P.), Department of Tropical Hygiene and Public Health (H.B.), Clinic and Policlinic for Maxillofacial Surgery (C.M.Z.), and Policlinic for Conservative Dentistry and Periodontology (C.K., R.L., C.E.D.), University of Heidelberg, Heidelberg, Germany.

Correspondence to Armin J. Grau, MD, Department of Neurology, Klinikum der Stadt Ludwigshafen a Rh, Bremserstr 79, 67063 Ludwigshafen a Rh, Federal Republic of Germany. E-mail graua{at}klilu.de

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose— Chronic infectious diseases may increase the risk of stroke. We investigated whether periodontal disease, including periodontitis and gingivitis, is a risk factor for cerebral ischemia.

Methods— We performed a case-control study with 303 patients examined within 7 days after acute ischemic stroke or transient ischemic attack, 300 population controls, and 168 hospital controls with nonvascular and noninflammatory neurological diseases. All subjects received a complete clinical and radiographic dental examination. The individual mean clinical attachment loss measured at 4 sites per tooth served as the main indicator for periodontitis.

Results— Patients had higher clinical attachment loss than population (P<0.001) and hospital (P=0.010) controls. After adjustment for age, sex, number of teeth, vascular risk factors and diseases, childhood and adult socioeconomic conditions, and lifestyle factors, the risk of cerebral ischemia increased with more severe periodontitis. Subjects with severe periodontitis (mean clinical attachment loss >6 mm) had a 4.3-times-higher (95% confidence interval, 1.85 to 10.2) risk of cerebral ischemia than subjects with mild or without periodontitis (3 mm). Severe periodontitis was a risk factor in men but not women and in younger (<60 years) but not older subjects. Periodontitis increased the risk of cerebral ischemia caused by large-artery atherosclerosis, cardioembolism, and cryptogenic etiology. Gingivitis and severe radiologic bone loss were also independently associated with the risk of cerebral ischemia, whereas caries was not.

Conclusions— Our study indicates that periodontal disease, a treatable condition, is an independent risk factor for cerebral ischemia in men and younger subjects.

Key Words: infection • inflammation • risk factors • stroke

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The established risk factors do not fully account for the risk of stroke.¹ Recently, chronic infectious diseases, including periodontal disease, were also linked to stroke risk. Gingivitis and periodontitis are among the most common human infections. Gingivitis can develop within days and includes inflammatory changes of the gingiva most commonly induced by accumulation of dental plaque. Periodontitis results from a complex interplay between chronic bacterial infection and the inflammatory host response, leading to irreversible destruction of tooth-supporting tissues, with tooth loss as a common end point.² Periodontitis is associated with elevated markers of inflammation³ that are themselves indicators of stroke risk. Bacteria from periodontal pockets can enter the bloodstream during activities such as chewing or tooth brushing,⁴ and periodontal pathogens were identified in carotid plaques,⁵ but their role in atherogenesis is not yet understood.

Seven studies have investigated the association between stroke and periodontal disease and/or tooth loss: 2 small case-control studies^6,7 and 5 cohort studies, of which 2 relied on self-reported periodontal disease^8,9 and 3 represented posthoc analyses.^10–12 Five of these studies found significant associations between stroke and periodontal disease.^6,7,9,10,12 Evidence on the role of periodontal disease in stroke is still limited because of small sample size, retrospective data analyses, or potential residual confounding. We performed a case-control study, including a complete clinical and radiographic examination of oral hard and soft tissues, to investigate whether periodontal disease is independently associated with acute ischemic stroke or transient ischemic attack in general and with its etiologic subtypes.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
We investigated 303 hospitalized patients with acute cerebral ischemia from one university hospital, 300 population controls, and 168 hospital controls. Subjects had to be native German speakers between 18 and 75 years of age living in a defined area around the university hospital. Exclusion criteria included pregnancy, inability to give informed consent or to cooperate in the dental examination within 1 week after ischemia (patients) or admission (hospital controls), and known conditions requiring prophylactic antibiotic treatment before dental examination.

Patients with acute cerebral ischemia had ischemic stroke (acute ischemic lesion on brain imaging and/or neurological deficits lasting >24 hours; n=208) or transient ischemic attack (neurological deficit of <24 hours without new ischemic lesions; n=95). Cerebral hemorrhages were excluded by neuroimaging in all patients. Among 497 consecutive patients (August 1998 through January 2000), 367 were eligible, and 303 (82.8%) agreed to participate. Patients were examined within 3.3±2.2 days (mean±SD) after ischemia. We used established criteria for etiologic stroke subtype analysis¹³ (atherothrombosis: atherosclerotic stenosis 50% in ipsilateral brain-supplying artery without alternative etiology; cardioembolism: high- or medium-risk source of cardiac embolism¹³ without alternative etiology; microangiopathy: presence of 1 of 5 lacunar syndromes and infarction <1.5 cm of diameter without alternative etiology; cryptogenic: absence of stroke etiology despite complete workup).

We received a 2% random sample of all inhabitants 18 to 75 years of age from the official population registry of the study area. Population controls were randomly selected from this sample, frequency matched to patients by age and sex, and examined parallel to patient recruitment. Among 497 controls contacted, 435 were eligible, and 300 (69.0%) participated. Hospital controls were selected from patients consecutively hospitalized at the neurology and neurosurgery departments of the same hospital and investigated parallel to patients with ischemia. Subjects with vascular, inflammatory, or alcohol or drug-derived neurological diseases or with brain metastases were excluded. Among 259 eligible patients, 168 (64.9%) participated. Patients had diseases of the vertebral column (n=89), primary central nervous system tumors (n=54), and neurodegenerative (n=14) and other neurological (n=11) diseases. All participating individuals gave informed consent for study participation and separately for radiography. The study protocol was approved by the local ethics committee.

Interview and Dental Examination
Trained interviewers used a standardized questionnaire that focused on previous diseases and vascular and periodontal risk factors, including a detailed assessment of smoking and drinking habits,¹⁴ nutrition,¹⁵ childhood and adult social history,¹⁶ past and present medication use, and dental care (eg, frequency and duration of tooth brushing, frequency of dentist visits, previous dental treatments). Risk factors—eg, hypertension and diabetes mellitus—were diagnosed if the patient reported that a physician had previously diagnosed the condition or if the patient was on treatment. All individuals were examined in a standardized way in a dental unit under optimum conditions with illumination by a standard dental light, compressed air, and a mouth mirror. Dental examinations were performed by a trained dentist (C.K.; 89.6%) or by a calibrated substitute (R.L.; 10.4%). Radiographs were analyzed in a blinded manner (all by R.L.).

For assessment of periodontitis, the clinical attachment loss (CAL; distance between probed base of the pocket and cementoenamel junction) was selected as the primary variable. Measurements were performed in all teeth at 4 sites to the nearest millimeter with a North Carolina periodontal probe.¹⁷ Individual mean values were calculated. Attachment levels were analyzed as a continuous variable and after stratification into absence of periodontitis or mild periodontitis (defined as mean CAL 3 mm) and steps of 1.5 mm (mean CAL, 3 to 4.5, 4.5 to 6, and >6 mm), with mean CAL >6 mm defined as severe periodontitis. Gingivitis severity was assessed with the Löe and Silness Gingival Index that is based on gingival bleeding after skimming a periodontal probe 1 mm into the crevicular sulcus to irritate the gingiva. Higher index numbers represent more severe gingivitis. Severe gingivitis was defined as index values >1.2. Dental plaque was graded according to the Silness and Löe Plaque Index.¹⁸ Plaque and gingivitis were scored at 4 sites per tooth (buccal, mesiolingual, lingual, and distolingual) and averaged for each subject. At least 1 remaining tooth was required for these analyses. For assessment of caries, teeth were slightly air dried and visually inspected with a dental mirror. Only teeth with visible cavitation were taken as decayed. The number of decayed (D), missing (M), and restored teeth (FT) was calculated according to the DMFT Index system.¹⁹ Panoramic radiographs were taken in 261 stroke cases (86%), 152 hospital controls (89%), and 285 population controls (95%). Radiographic bone loss was measured as the distance from the cementoenamel junction to the most apical extension of the bony defect at 2 sites per tooth (mesial and distal), expressed as absolute values (in millimeters) and relative to the overall root length (in percent), and averaged in each individual.

Statistical Analysis
Conditional logistic regression analysis stratified by age (5-year age groups) and sex, as described recently,²⁰ was used to analyze the association of factors with cerebral ischemia. All factors of interest were first analyzed separately and adjusted for number of teeth in dental parameters. In the multivariate model, the CAL was included, plus those factors considered important a priori (hypertension, diabetes mellitus, smoking, alcohol consumption, atrial fibrillation, previous cerebral ischemia, other ischemic vascular diseases, family history of stroke, school education, profession) or significant (P<0.05) in univariate analysis. Individuals with no teeth left (28 teeth missing) were assigned an additional category. Subgroup analyses by number of teeth were also performed. Linear tests for trend were performed with scored variables. Odds ratios (ORs) and 95% confidence intervals (CIs) are given for all factors. Both control groups were combined in multivariate analyses on the basis of mostly similar results in univariate analysis of dental variables.²¹ The SAS software package PROC PHREG was used for the analyses.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Tables 1 and 2 depict demographic data, risk factors, and results from dental examinations. The mean CAL was higher, indicating more severe periodontitis, in patients than in both control groups. Similar results were found for number of teeth, gingivitis, radiological bone loss, and plaque index (Table 2). After adjustment for age, sex, number of teeth, and other covariables, increasing severity of periodontitis was associated with an increasing risk of cerebral ischemia. Severe periodontitis increased the risk by a factor of 4.3 (Table 3). In contrast, missing teeth, plaque index, and caries were not independent risk factors. Similar results were obtained when patients with first-ever stroke or transient ischemic attack were analyzed separately (Table 4). Periodontitis represented a risk factor in men and younger subjects but not in women or older individuals (>60 years). Regarding etiologic subgroups, severe periodontitis was an independent risk factor for atherothrombotic, cryptogenic, and cardioembolic origins (Table 4). Subgroup analyses by number of teeth showed an increased risk by severe periodontitis in subjects with <10 teeth missing (OR, 9.02; 95% CI, 1.03 to 79.4; model as in Table 3) but not in those with 10 to 27 teeth missing (OR, 1.47; 95% CI, 0.39 to 5.6). In subjects with >5 remaining teeth, severe periodontitis was still associated with increased risk (OR, 6.7; 95% CI, 2.39 to 19.0).

View this table: [in this window] [in a new window]   TABLE 1. Demographic Variables and Risk Factors

View this table: [in this window] [in a new window]   TABLE 2. Intraoral Variables Among the 3 Groups

View this table: [in this window] [in a new window]   TABLE 3. ORs for Clinical Attachment Loss and Other Risk Factors*

View this table: [in this window] [in a new window]   TABLE 4. ORs for Clinical Attachment Loss in Subgroups*

In multivariate analysis, severe radiological bone loss and severity of gingivitis were significantly associated with cerebral ischemia. Similar results were found if patients with transient ischemic attack were excluded from the analyses (Table 5). Severity of gingivitis was not correlated with the time period between ischemia and dental examination (R=0.037; P=NS). When gingivitis is added to the multivariate model in Table 4, the role of severe periodontitis is attenuated (OR, 2.09; 95% CI, 0.84 to 5.2), whereas severe gingivitis remains an independent risk factor (OR, 7.27; 95% CI, 2.94 to 18.0).

View this table: [in this window] [in a new window]   TABLE 5. ORs for Radiographic Bone Loss and Gingivitis*

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Our results support the hypothesis that periodontal disease is an independent stroke risk factor. This is the first case-control study that performed a meticulous clinical and radiographic evaluation of orodental conditions and etiologic subgroup analyses of stroke as a heterogeneous disease. Our patient group is representative of stroke patients in the age segment studied because our hospital is the main stroke center in the area and stroke patients <75 years of age are commonly admitted to our wards. The role of periodontal disease as a risk factor could be explained by residual confounding, mainly by smoking, a health-neglecting lifestyle, and socioeconomic variables. We separately evaluated every smoking period using a standardized approach¹⁴ and adjusted for adult and childhood socioeconomic variables and specific periodontal risk factors, such as dental plaque and frequency of dentist visits, that are indicators of dental care and general health awareness. These factors did not modify the role of periodontitis. Furthermore, caries that also results from oral neglect was not an independent risk factor. This result is similar to that in a previous study⁷ and supports the hypothesis of a specific link between periodontal disease and stroke risk. Nevertheless, a causal relationship cannot be inferred from our data, and large intervention studies are required to test for causality.

Limitations of our study include a possible selection bias toward controls with higher health awareness, although the participation rate in our control groups was comparably good. For obvious reasons, the examiner could not be blinded to patient status, potentially leading to an ascertainment bias. However, radiologic assessment was blinded, and its results confirmed clinical periodontal findings. Stroke patients are older and more often male than other neurological inpatients. This limited age and sex matching with hospital controls, but all comparisons were adjusted for age and sex, allowing full comparability. We had to restrict our study to patients with transient ischemic attack and mild to moderately severe stroke. Therefore, results cannot be transferred to severe and fatal stroke. Residual confounding by factors not adjusted for in the multivariate analysis (eg, physical activity) may be a further limitation.

Periodontitis was an independent risk factor only in younger patients and men. This may be caused by a decreasing role of periodontitis as a risk factor in increasing age and by differences in health awareness between sexes. Periodontitis was associated with cerebral ischemia caused by large-artery atherosclerosis, supporting the hypothesis of a possible link between periodontitis and atherogenesis or complications of atherosclerosis.⁵ There was also a strong association with cryptogenic stroke and, to a lesser degree, with cardioembolism. Active periodontal inflammation may contribute to a prothrombotic state via recurrent bacteremia, platelet activation, and elevated clotting factors, thereby increasing the risk of cardioembolism and cryptogenic stroke.²²

Two lines of evidence further support the hypothesis that active periodontal inflammation increases stroke risk. First, edentulousness in which periodontal inflammation is usually absent was not an independent risk factor; in contrast, severe periodontitis was a more important risk factor in those with several teeth left. Second, gingivitis was strongly and independently associated with cerebral ischemia. When tested together with periodontitis, severe gingivitis even appeared as the more important risk factor. Gingivitis is an indicator for the actual status of periodontal inflammation. As shown recently, acute infection is a trigger for ischemic stroke.²³ Bone loss and attachment loss require longer periods to develop² and therefore undoubtedly preceded cerebral ischemia. Because of its fast development, gingivitis could partly be a sequel of poor health care after stroke. However, we rapidly examined our patients and found no correlation between gingivitis and time elapsed after ischemia. This may support the hypothesis that gingivitis preceded cerebral ischemia. Gingivitis was not a significant risk factor for stroke in a recent cohort study,¹² a finding that is not surprising given the discontinuous presence and variable strength of the disease over time. Periodontal disease is a chronic inflammatory disease with acute exacerbations and periods of quiescence, and periodontal conditions at the time of acute ischemia may be of major interest.

In conclusion, our study indicates that periodontal disease is significantly associated with cerebral ischemia. Gingivitis and periodontitis are treatable and preventable conditions. Therefore, their identification as stroke risk factors that require further studies would have a major impact on stroke prevention.

	Acknowledgments

 
This study was supported by the Deutsche Forschungsgemeinschaft (grant Gr 1102/3-1). We wish to thank Gabriele Stieglbauer for her help with statistical analyses and Daniela Jörß and Marc Gierich for their assistance in interviews with the subjects.

Received June 25, 2003; revision received September 26, 2003; accepted October 13, 2003.

	References

Top Abstract Introduction Subjects and Methods Results Discussion References

 

1. Gorelick PB. Stroke prevention therapy beyond antithrombotics: unifying mechanisms in ischemic stroke pathogenesis and implications for therapy: an invited review. Stroke. 2002; 33: 862–875.[Abstract/Free Full Text]
2. Kinane DF. Causation and pathogenesis of periodontal disease. Periodontol 2000. 2001; 25: 8–20.[CrossRef]
3. Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ, De Nardin E. Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol. 2001; 72: 1221–1227.[CrossRef][Medline] [Order article via Infotrieve]
4. Lockhart PB. The risk for endocarditis in dental practice. Periodontol 2000. 2000; 23: 127–135.[CrossRef]
5. Chiu B. Multiple infections in carotid atherosclerotic plaques. Am Heart J. 1999; 138: S534–S536.[CrossRef][Medline] [Order article via Infotrieve]
6. Syrjänen J, Peltola J, Valtonen V, Iivanainen M, Kaste M, Huttunen JK. Dental infections in association with cerebral infarction in young and middle-aged men. J Intern Med. 1989; 225: 179–184.[Medline] [Order article via Infotrieve]
7. Grau AJ, Buggle F, Ziegler C, Schwarz W, Meuser J, Tasman A-J, Bühler A, Benesch C, Becher H, Hacke W. Association between acute cerebrovascular ischemia and chronic and recurrent infection. Stroke. 1997; 28: 1724–1729.[Abstract/Free Full Text]
8. Howell TH, Ridker PM, Ajani UA, Hennekens CH, Christen WG. Periodontal disease and risk of subsequent cardiovascular disease in U.S. male physicians. J Am Coll Cardiol. 2001; 37: 445–450.[Abstract/Free Full Text]
9. Joshipura KJ, Hung HC, Rimm EB, Willett WC, Ascherio A. Periodontal disease, tooth loss, and incidence of ischemic stroke. Stroke. 2003; 34: 47–52.[Abstract/Free Full Text]
10. Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S. Periodontal disease and cardiovascular disease. J Periodontol. 1996; 67: 1123–1137.[Medline] [Order article via Infotrieve]
11. Morrison HI, Ellison LF, Taylor GW. Periodontal disease and risk of fatal coronary heart and cerebrovascular diseases. J Cardiovasc Risk. 1999; 6: 7–11.[Medline] [Order article via Infotrieve]
12. Wu T, Trevisan M, Genco RJ, Dorn JP, Falkner KL, Sempos CT. 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.[Abstract/Free Full Text]
13. Adams HP, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE. Classification of subtype of acute stroke: definitions for use in a multicenter clinical trial. Stroke. 1993; 24: 35–41.[Abstract/Free Full Text]
14. Becher H, Jockel KH, Timm J, Wichmann HE, Drescher K. Smoking cessation and nonsmoking intervals: effect of different smoking patterns on lung cancer risk. Cancer Causes Control. 1991; 2: 381–387.[CrossRef][Medline] [Order article via Infotrieve]
15. Brandstetter BR, Korfmann A, Kroke A, Becker N, Schulze MB, Boeing H. Dietary habits in the german epic cohorts: food group intake estimated with the food frequency questionnaire: European investigation into cancer and nutrition. Ann Nutr Metab. 1999; 43: 246–257.[CrossRef][Medline] [Order article via Infotrieve]
16. Mendall MA, Goggin PM, Molineaux N, Levy J, Toosy T, Strachan D, Northfield TC. Childhood living conditions and Helicobacter pylori seropositivity in adult life. Lancet. 1992; 339: 896–897.[CrossRef][Medline] [Order article via Infotrieve]
17. Carranza FA. Clinical diagnosis. In: Carranza FA, ed. Glickman’s Clinical Periodontology. Philadelphia, Pa: WB Saunders; 1990: 476–501.
18. Löe H. The gingival index, the plaque index and the retention index systems. J Periodontol. 1967; 38: 610–616.[Medline] [Order article via Infotrieve]
19. Klein H. The family and dental disease, IV: dental disease (DMF) experience in parents and offspring. JAMA. 1946; 33: 735–737.
20. Neuhäuser M, Becher H. Improved odds ratio estimation by post-hoc stratification of case-control data. Stat Med. 1997; 16: 993–1004.[CrossRef][Medline] [Order article via Infotrieve]
21. Hosmer DW, Lemeshow S. Applied Logistic Regression. New York, NY: Wiley & Sons; 2000.
22. Lourbakos A, Yuan YP, Jenkins AL, Travis J, Andrade-Gordon P, Santulli R, Potemba J, Pike RN. Activation of protease-activated receptors by gingipains from Porphyromonas gingivalis leads to platelet aggregation: a new trait in microbial pathogenicity. Blood. 2001; 97: 3790–3797.[Abstract/Free Full Text]
23. Grau AJ, Buggle F, Becher H, Zimmermann E, Spiel M, Fent T, Maiwald M, Werle E, Zorn M, Hengel H, Hacke W. Recent bacterial and viral infection is a risk factor for cerebrovascular ischemia: clinical and biochemical studies. Neurology. 1998; 50: 196–203.[Abstract/Free Full Text]

This article has been cited by other articles:

				T. Dietrich, M. Jimenez, E. A. Krall Kaye, P. S. Vokonas, and R. I. Garcia Age-Dependent Associations Between Chronic Periodontitis/Edentulism and Risk of Coronary Heart Disease Circulation, April 1, 2008; 117(13): 1668 - 1674. [Abstract] [Full Text] [PDF]

				P. S. Stein, M. Desrosiers, S. J. Donegan, J. F. Yepes, and R. J. Kryscio Tooth loss, dementia and neuropathology in the Nun Study J Am Dent Assoc, October 1, 2007; 138(10): 1314 - 1322. [Abstract] [Full Text] [PDF]

				T. K. Boehm and F. A. Scannapieco The Epidemiology, Consequences and Management of Periodontal Disease in Older Adults J Am Dent Assoc, September 1, 2007; 138(suppl_1): 26S - 33S. [Abstract] [Full Text] [PDF]

				D.J. Caplan, J.B. Chasen, E.A. Krall, J. Cai, S. Kang, R.I. Garcia, S. Offenbacher, and J.D. Beck Lesions of endodontic origin and risk of coronary heart disease. J. Dent. Res., November 1, 2006; 85(11): 996 - 1000. [Abstract] [Full Text] [PDF]

				E. Vanterpool, F. Roy, W. Zhan, S. M. Sheets, L. Sangberg, and H. M. Fletcher VimA is part of the maturation pathway for the major gingipains of Porphyromonas gingivalis W83. Microbiology, November 1, 2006; 152(Pt 11): 3383 - 3389. [Abstract] [Full Text] [PDF]

				R. T. Demmer and M. Desvarieux Periodontal infections and cardiovascular disease: The heart of the matter J Am Dent Assoc, October 1, 2006; 137(suppl_2): 14S - 20S. [Abstract] [Full Text] [PDF]

				G Sanna, L Preda, R Bruschini, M Cossu Rocca, S Ferretti, L Adamoli, E Verri, L Franceschelli, A Goldhirsch, and F Nole Bisphosphonates and jaw osteonecrosis in patients with advanced breast cancer Ann. Onc., October 1, 2006; 17(10): 1512 - 1516. [Abstract] [Full Text] [PDF]

				T. Schillinger, W. Kluger, M. Exner, W. Mlekusch, S. Sabeti, J. Amighi, O. Wagner, E. Minar, and M. Schillinger Dental and Periodontal Status and Risk for Progression of Carotid Atherosclerosis: The Inflammation and Carotid Artery Risk for Atherosclerosis Study Dental Substudy Stroke, September 1, 2006; 37(9): 2271 - 2276. [Abstract] [Full Text] [PDF]

				M. L. Rufail, H. A. Schenkein, S. E. Barbour, J. G. Tew, and R. van Antwerpen Altered lipoprotein subclass distribution and PAF-AH activity in subjects with generalized aggressive periodontitis J. Lipid Res., December 1, 2005; 46(12): 2752 - 2760. [Abstract] [Full Text] [PDF]

				N. Brodala, E. P. Merricks, D. A. Bellinger, D. Damrongsri, S. Offenbacher, J. Beck, P. Madianos, D. Sotres, Y.-L. Chang, G. Koch, et al. Porphyromonas gingivalis Bacteremia Induces Coronary and Aortic Atherosclerosis in Normocholesterolemic and Hypercholesterolemic Pigs Arterioscler. Thromb. Vasc. Biol., July 1, 2005; 25(7): 1446 - 1451. [Abstract] [Full Text] [PDF]

				P.-O. Soder, B. Soder, J. Nowak, and T. Jogestrand Early Carotid Atherosclerosis in Subjects With Periodontal Diseases Stroke, June 1, 2005; 36(6): 1195 - 1200. [Abstract] [Full Text] [PDF]

				S. P. Engebretson, I. B. Lamster, M. S.V. Elkind, T. Rundek, N. J. Serman, R. T. Demmer, R. L. Sacco, P. N. Papapanou, and M. Desvarieux Radiographic Measures of Chronic Periodontitis and Carotid Artery Plaque Stroke, March 1, 2005; 36(3): 561 - 566. [Abstract] [Full Text] [PDF]

				M. Desvarieux, R. T. Demmer, T. Rundek, B. Boden-Albala, D. R. Jacobs Jr, R. L. Sacco, and P. N. Papapanou Periodontal Microbiota and Carotid Intima-Media Thickness: The Oral Infections and Vascular Disease Epidemiology Study (INVEST) Circulation, February 8, 2005; 111(5): 576 - 582. [Abstract] [Full Text] [PDF]

				P. J. Pussinen, G. Alfthan, H. Rissanen, A. Reunanen, S. Asikainen, and P. Knekt Antibodies to Periodontal Pathogens and Stroke Risk Stroke, September 1, 2004; 35(9): 2020 - 2023. [Abstract] [Full Text] [PDF]

				M. Desvarieux, C. Schwahn, H. Volzke, R. T. Demmer, J. Ludemann, C. Kessler, D. R. Jacobs Jr, U. John, and T. Kocher Gender Differences in the Relationship Between Periodontal Disease, Tooth Loss, and Atherosclerosis Stroke, September 1, 2004; 35(9): 2029 - 2035. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) All Versions of this Article: 35/2/496    most recent 01.STR.0000110789.20526.9Dv1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Grau, A. J. Articles by Dörfer, C. E. Search for Related Content PubMed PubMed Citation Articles by Grau, A. J. Articles by Dörfer, C. E. Related Collections Risk Factors for Stroke