Oral infection with a periodontal pathogen accelerates early atherosclerosis in apolipoprotein E-null mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 23, Issue 8, 2003, Pages 1405-1411

  Lalla, Evanthia ^a,c   Lamster, Ira B ^a   Hofmann, Marion A ^b   Bucciarelli, Loredana ^b   Jerud, Adrienne P ^a   Tucker, Sid ^a   Lu, Yan ^b   Papapanou, Panos N ^a   Schmidt, Ann Marie ^b  

^a Columbia University ^*  (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

^c NONE   (United States)

Author keywords

ApoE null mouse; Atherosclerosis; Infection; Periodontitis; Porphyromonas gingivalis

Indexed keywords

APOLIPOPROTEIN E; BACTERIAL DNA; IMMUNOGLOBULIN G; INTERLEUKIN 6; THROMBOPLASTIN; VASCULAR CELL ADHESION MOLECULE 1;

ALVEOLAR BONE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; BONE MASS; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE MODEL; HYPERLIPOPROTEINEMIA TYPE 3; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; NULL ALLELE; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; RISK FACTOR; SIGNAL TRANSDUCTION;

ALVEOLAR BONE LOSS; ANIMALS; APOLIPOPROTEINS E; ARTERIOSCLEROSIS; BACTEROIDACEAE INFECTIONS; CHOLESTEROL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; TRIGLYCERIDES;

EID: 0042490523     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000082462.26258.FE     Document Type: Article

References (37)

1. Papapanou PN. Periodontal diseases: epidemiology. Ann Periodontol. 1996;1:1-36.
2. Mattila KJ, Nieminen MS, Valtonen VV, Rasi VP, Kesaniemi YA, Syrjala SL, Jungell PS, Isoluoma M, Hietaniemi K, Jokinen MJ. Association between dental health and acute myocardial infarction. BMJ. 1989;298:779-781.
3. Paunio K, Impivaara O, Tiekso J, Maki J. Missing teeth and ischaemic heart disease in men aged 45-64 years. Eur Heart J. 1993;14(suppl K):54-56.
4. Beck J, Garcia R, Heiss G, Vokonas P, Offenbacher S. Periodontal disease and cardiovascular disease. J Periodontol. 1996;67:1123-1137.
5. Grau AJ, Buggle F, Ziegler C, Schwarz W, Meuser J, Tasman AJ, Buhler A, Benesch C, Becher H, Hacke W. Association between acute cerebrovascular ischemia and chronic and recurrent infection. Stroke. 1997;28:1724-1729.
6. Park L, Raman KG, Lee KJ, Lu Y, Ferran LJ Jr, Chow WS, Stem D, Schmidt AM. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med. 1998;4:1025-1031.
7. Eikelboom JW, Lonn E, Genest J Jr, Hankey G, Yusuf S. Homocyst(e)ine and cardiovascular disease: a critical review of the epidemiologic evidence. Ann Intern Med. 1999;131:363-375.
8. Assmann G, Cullen P, Jossa F, Lewis B, Mancini M. Coronary heart disease: reducing the risk: the scientific background to primary and secondary prevention of coronarv heart disease. A worldwide view. International Task Force for the Prevention of Coronary Heart Disease. Arterioscler Thromb Vasc Biol. 1999;19:1819-1824.
9. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
10. Grayston JT, Kuo CC, Campbell LA, Wang SP, Jackson LA. Chlamydia pneumoniae and cardiovascular disease. Cardiologia. 1997;42:1145-1151.
11. Elkind MS, Lin IF, Grayston JT, Sacco RL. Chlamydia pneumoniae and the risk of first ischemic stroke: the Northern Manhattan Stroke Study. Stroke. 2000;31:1521-1525.
12. Li L, Messas E, Batista EL Jr, Levine RA, Amar S. Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation. 2002;105:861-867.
13. Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 1992;258:468-471.
14. Paigen B, Morrow A, Holmes PA, Mitchell D, Williams RA. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis. 1987;68:231-240.
15. Lalla E, Lamster IB, Feit M, Huang L, Schmidt AM. A murine model of accelerated periodontal disease in diabetes. J Periodontal Res. 1998;33:387-399.
16. Sakellari D, Socransky SS, Dibart S, Eftimiadi C, Taubman MA. Estimation of serum antibody to subgingival species using checkerboard immunoblotting. Oral Microbiol Immunol. 1997;12:303-310.
17. Ashimoto A, Chen C, Bakker I, Slots J. Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol. 1996;11:266-273.
18. Socransky SS, Haffajee AD. Evidence of bacterial etiology: a historical perspective. Periodontol 2000. 1994;5:7-25.
19. Sandros J, Papapanou PN, Nannmark U, Dahlen G. Porphyromonas gingivalis invades human pocket epithelium in vitro. J Periodontal Res. 1994;29:62-69.
20. Seymour GJ, Gemmell E, Reinhardt RA, Eastcott J, Taubman MA. Immunopathogenesis of chronic inflammatory periodontal disease: cellular and molecular mechanisms. J Periodont Res. 1993;28:478-486.
21. Madianos PN, Papapanou PN, Sandros J. Porphyromonas gingivalis infection of oral epithelium inhibits neutrophil transepithelial migration. Infect Immunol. 1997;65:3983-3990.
22. Lofthus JE, Waki MY, Jolkovsky DL, Otomo-Corgel J, Newman MG. Flemmig T, Nachnani S. Bacteremia following subgingival irrigation and scaling and root planing. J Periodontol. 1991;62:602-607.
23. Ebersole JL, Holt SC. Immunological procedures for diagnosis and risk assessment in periodontal diseases. In: Johnson NW, ed. Risk Markers for Oral Diseases. Cambridge: Cambridge University Press; 1991.
24. Papapanou PN, Neiderud AM, Sandros J, Dahlen G. Checkerboard assessments of serum antibodies to oral microbiota as surrogate markers of clinical periodontal status. J Clin Periodontol. 2001;28:103-106.
25. Mayr M, Metzler B, Kiechl S, Willeit J, Schett G, Xu Q, Wick G. Endothelial cytotoxicity mediated by serum antibodies to heat shock proteins of Escherichia coli and Chlamydia pneumoniae: immune reactions to heat shock proteins as a possible link between infection and atherosclerosis. Circulation. 1999;99:1560-1566.
26. Kweider M, Lowe GD, Murray GD, Kinane DF, McGowan DA. Dental disease, fibrinogen and white cell count: links with myocardial infarction? Scott Med J. 1993;38:73-74.
27. Ebersole JL, Machen RL, Steffen MJ, Willmann DE. Systemic acute-phase reactants, C-reactive protein and haptoglobin, in adult periodontitis. Clin Exp Immunol. 1997;107:347-352.
28. Loos BG, Craandijk J, Hoek FJ, Wertheim-van Dillen PM, van der Velden U. Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol. 2000;71:1528-1534.
29. Wu T, Trevisan M, Genco RJ, Falkner KL, Dorn JP, Sempos CT. 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.
30. Salvi GE, Brown CE, Fujihashi K, Kiyono H, Smith FW, Beck JD, Offenbacher S. Inflammatory mediators of the terminal dentition in adult and early onset periodontitis. J Periodontal Res. 1998;33:212-225.
31. Kornman KS, Pankow J, Offenbacher S, Beck J, di Giovine F, Duff GW. Interleukin-1 genotypes and the association between periodontitis and cardiovascular disease. J Periodontal Res. 1999;34:353-357.
32. Chiu B. Multiple infections in carotid atherosclerotic plaques. Am Heart J. 1999;138:S534-S536.
33. Haraszthy VI, Zambon JJ, Trevisan M, Zeid M, Genco RJ. Identification of periodontal pathogens in atheromatous plaques. J Periodontol. 2000;71:1554-1560.
34. Deshpande RG, Khan M, Genco CA. Invasion strategies of the oral pathogen Porphyromonas gingivalis: implications for cardiovascular disease. Invasion Metastasis. 1998;18:57-69.
35. Dorn BR, Dunn WA Jr, Progulske-Fox A. Invasion of human coronary artery cells by periodontal pathogens. Infect Immunol. 1999;67:5792-5798.
36. Kuramitsu HK, Qi M, Kang IC, Chen W. Role for periodontal bacteria in cardiovascular diseases. Ann Periodontol. 2001;6:41-47.
37. Giacona MB, Papapanou PN, Lamster IB, Schmidt AM, Lalla E. Determinants of foam cell formation by human monocyte-derived macrophages infected with Porphyromonas gingivalis. J Dent Res. 2003;82:B-27. Abstract.