A systematic review and meta-analyses on C-reactive protein in relation to periodontitis

Journal of Clinical Periodontology

Volumn 35, Issue 4, 2008, Pages 277-290

  Paraskevas, Spiros ^a   Huizinga, John D ^a   Loos, Bruno G ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

C reactive protein (CRP); Cardiovascular diseases; Meta analysis; Periodontitis; Systematic review

Indexed keywords

ANTIINFECTIVE AGENT; C REACTIVE PROTEIN;

ARTICLE; BLOOD; CASE CONTROL STUDY; CROSS-SECTIONAL STUDY; HUMAN; META ANALYSIS; PERIODONTITIS; PREVENTIVE DENTISTRY;

ANTI-BACTERIAL AGENTS; C-REACTIVE PROTEIN; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; DENTAL SCALING; HUMANS; PERIODONTITIS;

EID: 40849088226     PISSN: 03036979     EISSN: 1600051X     Source Type: Journal    
DOI: 10.1111/j.1600-051X.2007.01173.x     Document Type: Article

References (88)

1. Ajwani, S., Mattila, K. J., Narhi, T. O., Tilvis, R. S. Ainamo, A. (2003) Oral health status, C-reactive protein and mortality - a 10 year follow-up study. Gerodontology 20, 32 40.
2. Amar, S., Gokce, N., Morgan, S., Loukideli, M., Van Dyke, T. E. Vita, J. A. (2003) Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation. Arteriosclerosis, Thrombosis, and Vascular Biology 23, 1245 1249.
3. Beck, J. D. Offenbacher, S. (2002) Relationships among clinical measures of periodontal disease and their associations with systemic markers. Annals of Periodontology 7, 79 89.
4. Beck, J. D., Slade, G. Offenbacher, S. (2000) Oral disease, cardiovascular disease and systemic inflammation. Periodontology 2000 23, 110 120.
5. Bizzarro, S., van der Velden, U., Ten Heggeler, J. M., Leivadaros, E., Hoek, F. J., Gerdes, V. E., Bakker, S. J., Gans, R. O., Ten Cate, H. Loos, B. G. (2007) Periodontitis is characterized by elevated PAI-1 activity. Journal of Clinical Periodontology 34, 574 580.
6. Blake, G. J. Ridker, P. M. (2001) High sensitivity C-reactive protein for predicting cardiovascular disease: an inflammatory hypothesis. European Heart Journal 22, 349 352.
7. Blake, G. J. Ridker, P. M. (2002) Inflammatory bio-markers and cardiovascular risk prediction. Journal of Internal Medicine 252, 283 294.
8. Blake, G. J. Ridker, P. M. (2003) C-reactive protein: a surrogate risk marker or mediator of atherothrombosis? American Journal of Physiology - Regulatory Integrative and Comparitive Physiology 285, R1250 R1252.
9. Blake, G. J., Rifai, N., Buring, J. E. Ridker, P. M. (2003) Blood pressure, C-reactive protein, and risk of future cardiovascular events. Circulation 108, 2993 2999.
10. Bloemenkamp, D. G., van den Bosch, M. A., Mali, W. P., Tanis, B. C., Rosendaal, F. R., Kemmeren, J. M., Algra, A., Visseren, F. L. van der Graaf, Y. (2002) Novel risk factors for peripheral arterial disease in young women. American Journal of Medicine 113, 462 467.
11. Borrell, L. N., Burt, B. A. Taylor, G. W. (2005) Prevalence and trends in periodontitis in the USA: the [corrected] NHANES, 1988 to 2000. Journal of Dental Research 84, 924 930.
12. Boucher, N. E. Jr., Hanrahan, J. J. Kihara, F. Y. (1967) Occurrence of C-reactive protein in oral disease. Journal of Dental Research 46, 624.
13. Bretz, W. A., Weyant, R. J., Corby, P. M., Ren, D., Weissfeld, L., Kritchevsky, S. B., Harris, T., Kurella, M., Satterfield, S., Visser, M. Newman, A. B. (2005) Systemic inflammatory markers, periodontal diseases, and periodontal infections in an elderly population. Journal of the American Geriatrics Society 53, 1532 1537.
14. Brown, L. J., Oliver, R. C. Loe, H. (1990) Evaluating periodontal status of US employed adults. Journal of the American Dental Association 121, 226 232.
15. Buhlin, K., Gustafsson, A., Pockley, A. G., Frostegard, J. Klinge, B. (2003) Risk factors for cardiovascular disease in patients with periodontitis. European Heart Journal 24, 2099 2107.
16. Cochrane 2005) Cochrane Methods Group on Systematic Review of Screening and Diagnostic Tests Recommended methods, updated 6 June 1996.
17. Craig, R. G., Yip, J. K., So, M. K., Boylan, R. J., Socransky, S. S. Haffajee, A. D. (2003) Relationship of destructive periodontal disease to the acute-phase response. Journal of Periodontology 74, 1007 1016.
18. D'Aiuto, F., Nibali, L., Mohamed-Ali, V., Vallance, P. Tonetti, M. S. (2004a) Periodontal therapy: a novel non-drug-induced experimental model to study human inflammation. Journal of Periodontal Research 39, 294 299.
19. D'Aiuto, F., Nibali, L., Parkar, M., Suvan, J. Tonetti, M. S. (2005a) Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. Journal of Dental Research 84, 269 273.
20. D'Aiuto, F., Parkar, M., Andreou, G., Suvan, J., Brett, P. M., Ready, D. Tonetti, M. S. (2004b) Periodontitis and systemic inflammation: control of the local infection is associated with a reduction in serum inflammatory markers. Journal of Dental Research 83, 156 160.
21. D'Aiuto, F., Parkar, M., Nibali, L., Suvan, J., Lessem, J. Tonetti, M. S. (2006) Periodontal infections cause changes in traditional and novel cardiovascular risk factors: results from a randomized controlled clinical trial. American Heart Journal 151, 977 984.
22. D'Aiuto, F., Parkar, M. Tonetti, M. S. (2005b) Periodontal therapy: a novel acute inflammatory model. Inflammation Research 54, 412 414.
23. D'Aiuto, F., Ready, D. Tonetti, M. S. (2004c) Periodontal disease and C-reactive protein-associated cardiovascular risk. Journal of Periodontal Research 39, 236 241.
24. Danesh, J., Collins, R., Appleby, P. Peto, R. (1998) Association of fibrinogen, C-reactive protein, albumin, or leukocyte count with coronary heart disease: meta-analyses of prospective studies. Journal of the American Medical Association 279, 1477 1482.
25. Desvarieux, M., Demmer, R. T., Rundek, T., Boden-Albala, B., Jacobs, D. R. Jr., Sacco, R. L. Papapanou, P. N. (2005) Periodontal microbiota and carotid intima-media thickness: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Circulation 111, 576 582.
26. Deville, W. L., Buntinx, F., Bouter, L. M., Montori, V. M., de Vet, H. C., van der Windt, D. A. Bezemer, P. D. (2002) Conducting systematic reviews of diagnostic studies: didactic guidelines. BioMed Central - Medical Research Methodology 2, 9.
27. Dye, B. A., Choudhary, K., Shea, S. Papapanou, P. N. (2005) Serum antibodies to periodontal pathogens and markers of systemic inflammation. Journal of Clinical Periodontology 32, 1189 1199.
28. Ebersole, J., Machen, R. L., Steffen, M. Willman, D. (1997) Systemic acute-phase reactants, C-reactive protein and haptoglobin, in adult periodontitis. Clinical and Experimental Immunology 107, 347 352.
29. Ebersole, J. L. Cappelli, D. (2000) Acute-phase reactants in infections and inflammatory diseases. Periodontology 2000 23, 19 49.
30. Ebersole, J. L., Cappelli, D., Mathys, E. C., Steffen, M. J., Singer, R. E., Montgomery, M., Mott, G. E. Novak, M. J. (2002) Periodontitis in humans and non-human primates: oral-systemic linkage inducing acute phase proteins. Annals of Periodontology 7, 102 111.
31. Elter, J. R., Hinderliter, A. L., Offenbacher, S., Beck, J. D., Caughey, M., Brodala, N. Madianos, P. N. (2006) The effects of periodontal therapy on vascular endothelial function: a pilot trial. American Heart Journal 151, 47.
32. Florez, H., Castillo-Florez, S., Mendez, A., Casanova-Romero, P., Larreal-Urdaneta, C., Lee, D. Goldberg, R. (2006) C-reactive protein is elevated in obese patients with the metabolic syndrome. Diabetes Research and Clinical Practice 71, 92 100.
33. Forner, L., Larsen, T., Kilian, M. Holmstrup, P. (2006) Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. Journal of Clinical Periodontology 33, 401 407.
34. Fredriksson, M., Bergstrom, K. Asman, B. (2002) IL-8 and TNF-alpha from peripheral neutrophils and acute-phase proteins in periodontitis. Journal of Clinical Periodontology 29, 123 128.
35. Fredriksson, M., Gustafsson, A., Asman, B. Bergstrom, K. (1998) Hyper-reactive peripheral neutrophils in adult periodontitis: generation of chemiluminescence and intracellular hydrogen peroxide after in vitro priming and FcgammaR-stimulation. Journal of Clinical Periodontology 25, 394 398.
36. Fredriksson, M. I., Figueredo, C. M., Gustafsson, A., Bergstrom, K. G. Asman, B. E. (1999) Effect of periodontitis and smoking on blood leukocytes and acute-phase proteins. Journal of Periodontology 70, 1355 1360.
37. Fredriksson, M. I., Gustafsson, A. K., Bergstrom, K. G. Asman, B. E. (2003) Constitutionally hyperreactive neutrophils in periodontitis. Journal of Periodontology 74, 219 224.
38. Furuichi, Y., Shimotsu, A., Ito, H., Namariyama, Y., Yotsumoto, Y., Hino, Y., Mishige, Y., Inoue, M. Izumi, Y. (2003) Associations of periodontal status with general health conditions and serum antibody titers for Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans. Journal of Periodontology 74, 1491 1497.
39. Geerts, S. O., Nys, M., De, M. P., Charpentier, J., Albert, A., Legrand, V. Rompen, E. H. (2002) Systemic release of endotoxins induced by gentle mastication: association with periodontitis severity. Journal of Periodontology 73, 73 78.
40. Gjermo, P. (1998) Epidemiology of periodontal diseases in Europe. Journal de Parodontologie et d'Implantologie Orale 17, 111 121.
41. Glurich, I., Grossi, S., Albini, B., Ho, A., Shah, R., Zeid, M., Baumann, H., Genco, R. J. De Nardin, E. (2002) Systemic inflammation in cardiovascular and periodontal disease: comparative study. Clinical and Diagnostic Laboratory Immunology 9, 425 432.
42. Greenwell, H. (2000) Periodontitis as a risk factor for cardiovascular disease. Journal of Contempary Dental Practice 1, 106.
43. Havemose-Poulsen, A., Westergaard, J., Stoltze, K., Skjodt, H., Danneskiold-Samsoe, B., Locht, H., Bendtzen, K. Holmstrup, P. (2006) Periodontal and hematological characteristics associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. Journal of Periodontology 77, 280 288.
44. Haynes, W. G. Stanford, C. (2003) Periodontal disease and atherosclerosis: from dental to arterial plaque. Arteriosclerosis, Thrombosis, and Vascular Biology 23, 1309 1311.
45. Higgins, J. P. Thompson, S. G. (2002) Quantifying heterogeneity in a meta-analysis. Statistics in Medicine 21, 1539 1558.
46. Ide, M., Jagdev, D., Coward, P. Y., Crook, M., Barclay, G. R. Wilson, R. F. (2004) The short-term effects of treatment of chronic periodontitis on circulating levels of endotoxin, C-reactive protein, tumor necrosis factor-alpha, and interleukin-6. Journal of Periodontology 75, 420 428.
47. Ide, M., McPartlin, D., Coward, P. Y., Crook, M., Lumb, P. Wilson, R. F. (2003) Effect of treatment of chronic periodontitis on levels of serum markers of acute-phase inflammatory and vascular responses. Journal of Clinical Periodontology 30, 334 340.
48. Ioannidou, E., Kao, D., Chang, N., Burleson, J. Dongari-Bagtzoglou, A. (2006) Elevated serum interleukin-6 (IL-6) in solid-organ transplant recipients is positively associated with tissue destruction and IL-6 gene expression in the periodontium. Journal of Periodontology 77, 1871 1878.
49. Iwamoto, Y., Nishimura, F., Soga, Y., Takeuchi, K., Kurihara, M., Takashiba, S. Murayama, Y. (2003) Antimicrobial periodontal treatment decreases serum C-reactive protein, tumor necrosis factor-alpha, but not adiponectin levels in patients with chronic periodontitis. Journal of Periodontology 74, 1231 1236.
50. Janket, S. J., Baird, A. E., Chuang, S. K. Jones, J. A. (2003) Meta-analysis of periodontal disease and risk of coronary heart disease and stroke. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 95, 559 569.
51. Joshipura, K. J., Wand, H. C., Merchant, A. T. Rimm, E. B. (2004) Periodontal disease and biomarkers related to cardiovascular disease. Journal of Dental Research 83, 151 155.
52. Jousilahti, P., Salomaa, V., Rasi, V., Vahtera, E. Palosuo, T. (2003) Association of markers of systemic inflammation, C reactive protein, serum amyloid A, and fibrinogen, with socioeconomic status. Journal of Epidemiology Community Health. 57, 730 733.
53. Kinane, D. F., Riggio, M. P., Walker, K. F., MacKenzie, D. Shearer, B. (2005) Bacteraemia following periodontal procedures. Journal of Clinical Periodontology 32, 708 713.
54. Lakoski, S. G., Cushman, M., Criqui, M., Rundek, T., Blumenthal, R. S., D'Agostino, R. B. Herrington, D. M. (2006) Gender and C-reactive protein: data from the Multiethnic Study of Atherosclerosis(MESA) cohort. American Heart Journal 152, 593 598.
55. Leivadaros, E., van der Velden, U., Bizzarro, S., ten Heggeler, J. M., Gerdes, V. E., Hoek, F. J., Nagy, T. O., Scholma, J., Bakker, S. J., Gans, R. O., ten Cate, H. Loos, B. G. (2005) A pilot study into measurements of markers of atherosclerosis in periodontitis. Journal of Periodontology 76, 121 128.
56. Libby, P., Ridker, P. M. Maseri, A. (2002) Inflammation and atherosclerosis. Circulation 105, 1135 1143.
57. Loos, B. G. (2005) Systemic markers of inflammation in periodontitis. Journal of Periodontology 76, 2106 2115.
58. Loos, B. G., Craandijk, J., Hoek, F. J., Wertheim-van Dillen, P. M. van der Velden, U. (2000) Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. Journal of Periodontology 71, 1528 1534.
59. Lusis, A. J. (2000) Atherosclerosis. Nature 407, 233 241.
60. Mattila, K., Vesanen, M., Valtonen, V., Nieminen, M., Palosuo, T., Rasi, V. Asikainen, S. (2002) Effect of treating periodontitis on C-reactive protein levels: a pilot study. BioMed Central - Infectious Diseases 2, 30.
61. McCarty, M. F. (1999) Interleukin-6 as a central mediator of cardiovascular risk associated with chronic inflammation, smoking, diabetes, and visceral obesity: downregulation with essential fatty acids, ethanol and pentoxifylline. Medical Hypotheses 52, 465 477.
62. Meurman, J. H., Sanz, M. Janket, S. J. (2004) Oral health, atherosclerosis, and cardiovascular disease. Critical Reviews in Oral Biology and Medicine 15, 403 413.
63. Midgette, A. S., Stukel, T. A. Littenberg, B. (1993) A meta-analytic method for summarizing diagnostic test performances: receiver-operating- characteristic-summary point estimates. Medical Decision Making 13, 253 257.
64. Moher, D., Pham, B., Klassen, T. P., Schulz, K. F., Berlin, J. A., Jadad, A. R. Liberati, A. (2000) What contributions do languages other than English make on the results of meta-analyses? Journal of Clinical Epidemiology 53, 964 972.
65. Noack, B., Genco, R. J., Trevisan, M., Grossi, S., Zambon, J. J. De Nardin, E. (2001) Periodontal infections contribute to elevated systemic C-reactive protein level. Journal of Periodontology 72, 1221 1227.
66. Persson, G. R., Pettersson, T., Ohlsson, O. Renvert, S. (2005) High-sensitivity serum C-reactive protein levels in subjects with or without myocardial infarction or periodontitis. Journal of Clinical Periodontology 32, 219 224.
67. Pihlstrom, B. L., Michalowicz, B. S. Johnson, N. W. (2005) Periodontal diseases. Lancet 366, 1809 1820.
68. Pollitt, R. A., Kaufman, J. S., Rose, K. M., Diez-Roux, A. V., Zeng, D. Heiss, G. (2007) Early-life and adult socioeconomic status and inflammatory risk markers in adulthood. European Journal of Epidemiology 22, 55 66.
69. Rahman, A. U., Rashid, S., Noon, R., Samuel, Z. S., Lu, B., Borgnakke, W. S. Williams, R. C. (2005) Prospective evaluation of the systemic inflammatory marker C-reactive protein in patients with end-stage periodontitis getting teeth replaced with dental implants: a pilot investigation. Clinical Oral Implants Research 16, 128 131.
70. RevMan.
71. Ridker, P. M., Brown, N. J., Vaughan, D. E., Harrison, D. G. Mehta, J. L. (2004) Established and emerging plasma biomarkers in the prediction of first atherothrombotic events. Circulation 109, IV6 IV19.
72. Ridker, P. M., Cushman, M., Stampfer, M. J., Tracy, R. P. Hennekens, C. H. (1997) Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. New England Journal of Medicine 336, 973 979.
73. Ridker, P. M., Rifai, N., Rose, L., Buring, J. E. Cook, N. R. (2002) Comparison of C-Reactive Protein and Low-Density Lipoprotein Cholesterol Levels in the Prediction of First Cardiovascular Events. New England Journal of Medicine 347, 1557 1565.
74. Rosner, B. (2000) Fundamentals of Biostatistics, 5th edition, pp. 135 138. Pacific Grove, CA : Duxbury Press.
75. Saito, T., Murakami, M., Shimazaki, Y., Oobayashi, K., Matsumoto, S. Koga, T. (2003) Association between alveolar bone loss and elevated serum C-reactive protein in Japanese men. Journal of Periodontology 74, 1741 1746.
76. Salzberg, T. N., Overstreet, B. T., Rogers, J. D., Califano, J. V., Best, A. M. Schenkein, H. A. (2006) C-reactive protein levels in patients with aggressive periodontitis. Journal of Periodontology 77, 933 939.
77. Seinost, G., Wimmer, G., Skerget, M., Thaller, E., Brodmann, M., Gasser, R., Bratschko, R. O. Pilger, E. (2005) Periodontal treatment improves endothelial dysfunction in patients with severe periodontitis. American Heart Journal 149, 1050 1054.
78. Shklair, I. L., Loving, R. H., Leberman, O. F. Rau, C. F. (1968) C-Reactive protein and periodontal disease. Journal of Periodontology 39, 93 95.
79. Slade, G. D., Ghezzi, E. M., Heiss, G., Beck, J. D., Riche, E. Offenbacher, S. (2003) Relationship between periodontal disease and C-reactive protein among adults in the Atherosclerosis Risk in Communities study. Archives of Internal Medicine 163, 1172 1179.
80. Slade, G. D., Offenbacher, S., Beck, J. D., Heiss, G. Pankow, J. S. (2000) Acute-phase inflammatory response to periodontal disease in the US population. Journal of Dental Research 79, 49 57.
81. Socransky, S. S., Haffajee, A. D., Cugini, M. A., Smith, C. Kent, R. L. Jr. (1998) Microbial complexes in subgingival plaque. Journal of Clinical Periodontology 25, 134 144.
82. Söder, P. O., Söder, B., Nowak, J. Jogestrand, T. (2005) Early carotid atherosclerosis in subjects with periodontal diseases. Stroke 36, 1195 1200.
83. Taylor, B. A., Tofler, G. H., Carey, H. M. R., Morel-Kopp, M. C., Philcox, S., Carter, T. R., Elliott, M. J., Kull, A. D., Ward, C. Schenck, K. (2006) Full-mouth tooth extraction lowers systemic inflammatory and thrombotic markers of cardiovascular risk. Journal of Dental Research 85, 74 78.
84. Tonetti, M. S., D'Aiuto, F., Nibali, L., Donald, A., Storry, C., Parkar, M., Suvan, J., Hingorani, A. D., Vallance, P. Deanfield, J. (2007) Treatment of periodontitis and endothelial function. The New England Journal of Medicine 356, 911 920.
85. Tousoulis, D., Davies, G., Stefanadis, C., Toutouzas, P. Ambrose, J. A. (2003) Inflammatory and thrombotic mechanisms in coronary atherosclerosis. Heart 89, 993 997.
86. Wakai, K., Kawamura, T., Umemura, O., Hara, Y., Machida, J., Anno, T., Ichihara, Y., Mizuno, Y., Tamakoshi, A., lin, Y., Nakayama, T. Ohno, Y. (1999) Associations of medical status and physical fitness with periodontal disease. Journal of Clinical Periodontology 26, 664 672.
87. Wu, T., Trevisan, M., Genco, R. J., Falkner, K. L., Dorn, J. P. Sempos, C. T. (2000) 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. American Journal of Epidemiology 151, 273 282.
88. Yamazaki, K., Honda, T., Oda, T., Ueki-Maruyama, K., Nakajima, T., Yoshie, H. Seymour, G. J. (2005) Effect of periodontal treatment on the C-reactive protein and proinflammatory cytokine levels in Japanese periodontitis patients. Journal of Periodontal Research 40, 53 58.