Periodontal disease, but not edentulism, is independently associated with increased plasma fibrinogen levels

Christian Schwahn; Henry Völzke; Daniel M. Robinson; Jan Luedemann; Olaf Bernhardt; Dietmar Gesch; Ulrich John; Thomas Kocher

doi:10.1160/TH04-02-0092

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2004; 92(02): 244-252
DOI: 10.1160/TH04-02-0092

Theme Issue Article

Schattauer GmbH

Periodontal disease, but not edentulism, is independently associated with increased plasma fibrinogen levels

Results from a population-based study

Authors

Christian Schwahn

¹School of Dentistry, Ernst-Moritz-Arndt-University, Greifswald, Germany
Henry Völzke

²Institute of Epidemiology and Social Medicine, Ernst-Moritz-Arndt-University, Greifswald, Germany
Daniel M. Robinson

³Department of Internal Medicine B, Ernst-Moritz-Arndt-University, Greifswald, Germany
Jan Luedemann

⁴Institute of Clinical Chemistry and Laborartory Medicine, Ernst-Moritz-Arndt-University, Greifswald, Germany
Olaf Bernhardt

¹School of Dentistry, Ernst-Moritz-Arndt-University, Greifswald, Germany
Dietmar Gesch

¹School of Dentistry, Ernst-Moritz-Arndt-University, Greifswald, Germany
Ulrich John

²Institute of Epidemiology and Social Medicine, Ernst-Moritz-Arndt-University, Greifswald, Germany
Thomas Kocher

¹School of Dentistry, Ernst-Moritz-Arndt-University, Greifswald, Germany

Abstract

Summary

The systemic response to periodontal disease was analyzed in the cross-sectional Study of Health in Pomerania (SHIP). The completed data of 2,738 subjects aged 20 to 59 years were used for logistic regression analysis with an increased plasma fibrinogen level (≥3.25 g/L according to Clauss) as the dependent variable. Participants were divided into four groups according to the number of periodontal pockets ≥ 4mm (0, 1-7, 8-14, ≥15 pocketing). An additional group comprised the 52 edentulous subjects. The adjusted odds ratio (OR) of ≥15 periodontal pockets for increased plasma fibrinogen levels was 1.88 (95% CI: 1.25-2.83). Edentulism per se was not associated with increased plasma fibrinogen levels but was contained in a two-way interaction with the number of cigarettes/day in current smokers (p = 0.031). For edentulous nonsmokers the adjusted OR was 1.10 (95% CI: 0.51-2.39). Furthermore, body mass index, the interaction between gender and body mass index, serum LDL cholesterol, medication, the interaction between LDL cholesterol and medication, aspirin, smoking, school education, chronic bronchitis, and the interaction between alcohol consumption and chronic gastritis were associated with plasma fibrinogen levels. Our results show that periodontal disease but not edentulism per se is associated with an increased plasma fibrinogen level.

Keywords

Fibrinogen - periodontal disease - Study of Health in Pomerania - SHIP

Full Text

References

References
1 Kiechl S, Egger G, Mayr M. et al. Chronic infections and the risk of carotid atherosclerosis: prospective results from a large population study. Circulation 2001; 103: 1064-1070.
2 Espinola-Klein C, Rupprecht HJ, Blankenberg S. et al. Impact of infectious burden on progression of carotid atherosclerosis. Stroke 2002; 33: 2581-2586.
3 Mattila KJ, Valtonen VV, Nieminen MS. et al. Dental infection and the risk of new coronary events: prospective study of patients with documented coronary artery disease. Clin Infect Dis 1995; 20: 588-592.
4 Beck J, Garcia R, Heiss G. et al. Periodontal disease and cardiovascular disease. J Periodontol 1996; 67: 1123-1137.
5 Beck JD, Elter JR, Heiss G. et al. Relationship of periodontal disease to carotid artery intimamedia wall thickness: the atherosclerosis risk in communities (ARIC) study. Arterioscler Thromb Vasc Biol 2001; 21: 1816-1822.
6 Hujoel PP, Drangsholt M, Spiekerman C. et al. Periodontal disease and coronary heart disease risk. JAMA 2000; 284: 1406-1410.
7 Howell TH, Ridker PM, Ajani UA. et al. Periodontal disease and risk of subsequent cardiovascular disease in U.S. male physicians. J Am Coll Cardiol 2001; 37: 445-450.
8 Li L, Messas E, Batista EL Jr. et al. Porphyromonas gingivalis infection accelerrates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation 2002; 105: 861-867.
9 Wilhelmsen L, Svardsudd K, Korsan-Bengsten K. et al. Fibrinogen as a risk factor for stroke and myocardial infarction. New Engl J Med 1984; 311: 501-505.
10 Meade TW, Mellows S, Brozovic M. et al. Haemostatic function and ischaemic heart disease: principal results of the Northwick Park Heart Study. Lancet 1986; 02: 533-537.
11 Kannel WB, Wolf PA, Castelli WP. et al. Fibrinogen and risk of cardiovascular disease. J Am Med Assoc 1987; 258: 1183-1186.
12 Rosengren A, Wilhelmsen L. Fibrinogen, coronary heart disease and mortality from all causes in smokers and nonsmokers. The study of men born in 1933. J Intern Med 1996; 239: 499-507.
13 Danesh J, Collins R, Appleby P. et al. Association of fibrinogen, C-reactive protein, albumin, or leukocyte count with coronary heart disease. J Am Med Assoc 1998; 279: 1477-1482.
14 Danesh J, Whincup P, Walker M. et al. Low grade inflammation and coronary heart disease: prospective study and updated metaanalyses. Br Med J 2000; 321: 199-204.
15 Pearson TA, Mensah GA, Alexander RW. et al. Markers of inflammation and cardiovascular disease: application to clinical and public health practice: A statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 2003; 107: 499-511.
16 Ridker PM. Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation 2003; 107: 363-369.
17 Gabay C, Kushner MD. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 1999; 340: 448-454.
18 John U, Greiner B, Hensel E. et al. Study of Health in Pomerania (SHIP): a health examination survey in an east German region: objectives and design. Soz Präventivmed 2001; 46: 186-194.
19 Clauss A. Gerinnungsphysiologische Schnellmethode zur Bestimmung des Fibrinogens. Acta Haematol 1957; 17: 237-246.
20 Hensel E, Gesch D, Biffar R. et al. Study of Health in Pomerania (SHIP): A health survey in an East German Region – objectives and design of the Oral Health Section. Quintessence Int 2003; 34: 370-378.
21 Genco RJ. Risk factors for periodontal disease. In: Rose LF. ed. Periodontal medicine. Decker; 2000: 11-33.
22 Missov RM, Stolk RP, van-der-Bom JG. et al. Plasma fibrinogen in NIDDM: the Rotterdam study. Diab Care 1996; 19: 157-159.
23 Sun GW, Shook TL, Kay GL. Inappropriate use of bivariable analysis to screen risk factors for use in multivariable analysis. J Clin Epidemiol 1996; 49: 907-916.
24 Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic research. New York: Van Nostrand Reinhold; 1982
25 Hujoel PP, Drangsholt M, Spiekerman C. et al. Periodontitis-systemic disease associations in the presence of smoking causal or coincidental?. Periodontol 2000 2002; 30: 51-60.
26 Wu T, Trevisan M, Genco RJ. et al. Examination of the relation between periodontal health status and cardiovascular risk factors: serum total and high density lipoprotein cholesterol, C-reactive protein, and plasma fibrinogen. Am J Epidemiol 2000; 151: 273-282.
27 Slade GD, Offenbacher S, Beck JD. et al. Acute-phase inflammatory response to periodontal disease in the US population. J Dent Res 2000; 79: 49-57.
28 Kelsey JL, Whittemore AS, Evans AS. et al. Methods in observational epidemiology. Oxford University Press; 1996: 22-44.
29 DeStefano F, Anda RF, Kahn HS. et al. Dental disease and risk of coronary heart disease and mortality. Br Med J 1993; 306: 688-691.
30 Lopez R, Oyarzun M, Naranjo C. et al. Coronary heart disease and periodontitis – a case control study in Chilean adults. J Clin Periodontol 2002; 29: 468-473.
31 Mendall MA, Patel P, Ballam L. et al. C reactive protein and its relation to cardiovascular risk factors: a population based cross sectional study. Br Med J 1996; 312: 1061-1065.
32 Jousilahti P, Salomaa V, Rasi V. et al. Symptoms of chronic bronchitis, haemostatic factors, and coronary heart disease risk. Atherosclerosis 1999; 142: 403-407.
33 Parente F, Porro GB. The association between Helicobacter pylori infection and ischemic heart disease: facts or fancy?. Helicobacter 1997; 02: 67-72.
34 Torgano G, Cosentini R, Mandelli C. et al. Treatment of Helicobacter pylori and Chlamydia pneumoniae infections decreases fibrinogen plasma level in patients with ischemic heart disease. Circulation 1999; 99: 1555-1559.
35 Stone AF, Mendall MA, Kaski JC. et al. Effect of treatment for Chlamydia pneumoniae and Helicobacter pylori on markers of inflammation and cardiac events in patients with acute coronary syndromes: South Thames Trial of Antibiotics in Myocardial Infarction and Unstable Angina (STAMINA). Circulation 2002; 106: 1219-1223.
36 Zahn R, Schneider S, Frilling B. et al. Antibiotic therapy after acute myocardial infarction: a prospective randomized study. Working-Group-of-Leading-Hospital-Cardiologists. Circulation 2003; 107: 1253-1259.
37 Pitsavos C, Skoumas J, Dernellis J. et al. Influence of biological factors on lipid and fibrinogen measurements in young men: an epidemiological study in 2009 recruits. Eur Heart J 1998; 19: 1642-1647.
38 Mennen LI, Balkau B, Vol S. et al. Fibrinogen: a possible link between alcohol consumption and cardiovascular disease? DESIR Study Group. Arterioscler Thromb Vasc Biol 1999; 19: 887-892.
39 Stec JJ, Silbershatz H, Tofler GH. et al. Association of fibrinogen with cardiovascular risk factors and cardiovascular disease in the Framingham offspring population. Circulation 2000; 102: 1634-1638.
40 Nascetti S, Elosua R, Pena A. et al. REGICOR Investigators. Variables associated with fibrinogen in a population-based study: interaction between smoking and age on fibrinogen concentration. Eur J Epidemiol 2001; 17: 953-958.
41 Mukamal KJ, Jadhav PP, D’Agostino RB. et al. Alcohol consumption and hemostatic factors: analysis of the Framingham Offspring cohort. Circulation 2001; 104: 1367-1373.
42 Tuut M, Hense HW. Smoking, other risk factors and fibrinogen levels: evidence of effect modification. Ann Epidemiol 2001; 11: 232-238.
43 Church TS, Finley CE, Earnest CP. et al. Relative associations of fitness and fatness to fibrinogen, white blood cell count, uric acid and metabolic syndrome. Int J Obs Relat Metab Disord 2002; 26: 805-813.
44 Albert MA, Glynn RJ, Ridker PM. Alcohol consumption and plasma concentration of C-reactive protein. Circulation 2003; 107: 443-447.
45 Ridker PM, Cushman M, Stampfer MJ. et al. Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Engl J Med 1997; 336: 973-979.