Skip to main content

C-reactive protein as a systemic marker of inflammation in periodontitis

European Journal of Clinical Microbiology & Infectious Diseases volume 30, pages 407–414 (2011)Cite this article

Abstract

Periodontitis has been identified as a potential risk factor for systemic pathologies such as cardiovascular disease (CVD). The aims of this investigation were to assess the relationship between periodontitis and systemic inflammatory factor, as well as to discover whether there is a relation to the severity of periodontitis and to the periodontopathogens. Periodontal examinations and serum C-reactive protein (CRP) level measurements were performed in 50 patients with periodontitis. Periodontal health indicators included the gingival bleeding on probing index and periodontal disease status. The patients with moderate periodontitis had low attachment loss and pocket depth <4 mm. The patients with severe periodontitis had high attachment loss and pocket depth >5 mm. The control group comprised 25 volunteers with healthy gingiva, gingival sulcus <2 mm and no attachment loss. The presence of Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans in subgingival plaque samples was analysed by the polymerase chain reaction (PCR) method. The periodontal parameters and CRP levels were significantly higher in the patients with periodontitis. Patients who had severe periodontitis, with high levels of mean clinical attachment loss, and subjects with moderate periodontitis had higher mean CRP levels. The percentage of subjects with elevated levels of CRP >5 mg/l was greater in the higher clinical attachment loss group compared to the group with lower attachment loss. The presence of P. gingivalis and A. actinomycetemcomitans were also associated with elevated CRP levels and poor periodontal status. Periodontitis and the presence of P. gingivalis are associated with an enhanced inflammatory response expressed by higher CRP levels. The association of periodontitis with CRP levels appears to be a contributing factor for CVD and might be a possible intermediate pathway in this association.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  1. Van de Veire NR, Philippé J, De Winter O, Langlois M, Bernard D, De Sutter J (2006) Neurohumoral and inflammatory activation in patients with coronary artery disease treated with statins. Heart 92:1858–1859

    Article  PubMed  Google Scholar 

  2. Libby P, Ridker PM (2006) Inflammation and atherothrombosis: from population biology and bench research to clinical practice. J Am Coll Cardiol 48:A33–A46

    CAS  Article  Google Scholar 

  3. Ji SR, Wu Y, Zhu L, Potempa LA, Sheng FL, Lu W, Zhao J (2007) Cell membranes and liposomes dissociate C-reactive protein (CRP) to form a new, biologically active structural intermediate: mCRPm. FASEB J 21:284–294

    CAS  Article  PubMed  Google Scholar 

  4. Ridker PM, Rifai N, Rose L, Buring JE, Cook NR (2002) Comparison of C-reactive protein and low-density lipoprotein cholesterol levels in the prediction of first cardiovascular events. N Engl J Med 347:1557–1565

    CAS  Article  PubMed  Google Scholar 

  5. Tamakoshi K, Yatsuya H, Kondo T, Hori Y, Ishikawa M, Zhang H, Murata C, Otsuka R, Zhu S, Toyoshima H (2003) The metabolic syndrome is associated with elevated circulating C-reactive protein in healthy reference range, a systemic low-grade inflammatory state. Obesity 27:443–449

    CAS  Article  Google Scholar 

  6. Pitiphat W, Joshipura KJ, Rich-Edwards JW, Williams PL, Douglass CW, Gillman MW (2006) Periodontitis and plasma C-reactive protein during pregnancy. J Periodontol 77:821–825

    CAS  Article  PubMed  Google Scholar 

  7. Geerts SO, Nys M, De Mol P, Charpentier J, Albert A, Legrand V, Rompen EH (2002) Systemic release of endotoxins induced by gentle mastication: association with periodontitis severity. J Periodontol 73(1):73–78

    CAS  Article  PubMed  Google Scholar 

  8. Beck JD, Garcia R, Heiss G, Vokonas PS, Offenbacher S (1996) Periodontal disease and cardiovascular disease. J Periodontol 67(10):1123–1137

    CAS  Article  PubMed  Google Scholar 

  9. Loos BG (2005) Systemic markers of inflammation in periodontitis. J Periodontol 76:2106–2115

    Article  PubMed  Google Scholar 

  10. Buhlin K, Gustafsson A, Pockley AG, Frostegård J, Klinge B (2003) Risk factors for cardiovascular disease in patients with periodontitis. Eur Heart J 24:2099–2107

    Article  PubMed  Google Scholar 

  11. Craig RG, Yip JK, So MK, Boylan RJ, Socransky SS, Haffajee AD (2003) Relationship of destructive periodontal disease to the acute-phase response. J Periodontol 74:1007–1016

    Article  PubMed  Google Scholar 

  12. Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ, De Nardin E (2001) Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol 72(9):1221–1227

    CAS  Article  PubMed  Google Scholar 

  13. Lu Q, Jin L (2010) Human gingiva is another site of C-reactive protein formation. J Clin Periodontol 37:789–796

    CAS  Article  PubMed  Google Scholar 

  14. Megson E, Fitzsimmons T, Dharmapatni K, Mark Bartold P (2010) C-reactive protein in gingival crevicular fluid may be indicative of systemic inflammation. J Clin Periodontol 37:797–804

    CAS  Article  PubMed  Google Scholar 

  15. Pearson TA, Mensah GA, Alexander RW, Anderson JL, Cannon RO 3rd, Criqui M, Fadl YY, Fortmann SP, Hong Y, Myers GL, Rifai N, Smith SC Jr, Taubert K, Tracy RP, Vinicor F (2003) 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 107:499–511

    Article  PubMed  Google Scholar 

  16. Ebersole JL, Machen RL, Steffen MJ, Willmann DE (1997) Systemic acute-phase reactants, C-reactive protein and haptoglobin, in adult periodontitis. Clin Exp Immunol 107:347–352

    CAS  Article  PubMed  Google Scholar 

  17. Loos BG, Craandijk J, Hoek FJ, Wertheim-van Dillen PM, van der Velden U (2000) Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol 71:1528–1534

    CAS  Article  PubMed  Google Scholar 

  18. Amar S, Gokce N, Morgan S, Loukideli M, Van Dyke TE, Vita JA (2003) Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation. Arterioscler Thromb Vasc Biol 23:1245–1249

    CAS  Article  PubMed  Google Scholar 

  19. Morrison HI, Ellison LF, Taylor GW (1999) Periodontal disease and risk of fatal coronary heart and cerebrovascular diseases. J Cardiovasc Risk 6(1):7–11

    CAS  PubMed  Google Scholar 

  20. Newman MG, Takei H, Carranza FA (2002) Carranza’s clinical periodontology, 9th edn. W.B. Saunders Company, Philadelphia

    Google Scholar 

  21. Milićević R, Brajović G, Nikolić-Jakoba N, Popović B, Pavlica D, Leković V, Milasin J (2008) Identification of periodontopathogen microorganisms by PCR technique. Srp Arh Celok Lek 136:476–480

    Article  PubMed  Google Scholar 

  22. Wu T, Trevisan M, Genco RJ, Falkner KL, Dorn JP, Sempos CT (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. Am J Epidemiol 151:273–282

    CAS  PubMed  Google Scholar 

  23. Mattila KJ, Valle MS, Nieminen MS, Valtonen VV, Hietaniemi KL (1993) Dental infections and coronary atherosclerosis. Atherosclerosis 103:205–211

    CAS  Article  PubMed  Google Scholar 

  24. Emingil G, Buduneli E, Aliyev A, Akilli A, Atilla G (2000) Association between periodontal disease and acute myocardial infarction. J Periodontol 71:1882–1886

    CAS  Article  PubMed  Google Scholar 

  25. López R, Oyarzún M, Naranjo C, Cumsille F, Ortiz M, Baelum V (2002) Coronary heart disease and periodontitis—a case control study in Chilean adults. J Clin Periodontol 29:468–473

    Article  PubMed  Google Scholar 

  26. Genco RJ, Wu TJ, Grossi S, Falkner K, Zambon JJ, Trevisan M (1999) Periodontal microflora related to the risk for myocardial infarction: a case control study. J Dent Res 78:457

    Google Scholar 

  27. Reife RA, Shapiro RA, Bamber BA, Berry KK, Mick GE, Darveau RP (1995) Porphyromonas gingivalis lipopolysaccharide is poorly recognized by molecular components of innate host defense in a mouse model of early inflammation. Infect Immun 63:4686–4694

    CAS  PubMed  Google Scholar 

  28. Chung SW, Kang HS, Park HR, Kim SJ, Kim SJ, Choi JI (2003) Immune responses to heat shock protein in Porphyromonas gingivalis-infected periodontitis and atherosclerosis patients. J Periodontal Res 38:388–393

    CAS  Article  PubMed  Google Scholar 

  29. Mattila KJ, Nieminen MS, Valtonen VV, Rasi VP, Kesäniemi YA, Syrjälä SL, Jungell PS, Isoluoma M, Hietaniemi K, Jokinen MJ (1989) Association between dental health and acute myocardial infarction. BMJ 298:779–781

    CAS  Article  PubMed  Google Scholar 

  30. Kweider M, Lowe GDO, Murray GD, Kinane DF, McGowan DA (1993) Dental disease, fibrinogen and white cell count; links with myocardial infarction? Scott Med J 38:73–74

    CAS  PubMed  Google Scholar 

  31. Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH (1997) Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Engl J Med 336:973–979

    CAS  Article  PubMed  Google Scholar 

  32. Tsimikas S, Willerson JT, Ridker PM (2006) C-reactive protein and other emerging blood biomarkers to optimize risk stratification of vulnerable patients. J Am Coll Cardiol 47:C19–C31

    CAS  Article  PubMed  Google Scholar 

  33. Beck JD, Eke P, Heiss G, Madianos P, Couper D, Lin D, Moss K, Elter J, Offenbacher S (2005) Periodontal disease and coronary heart disease: a reappraisal of the exposure. Circulation 112:19–24

    Article  PubMed  Google Scholar 

  34. Garcia RI, Henshaw MM, Krall EA (2001) Relationship between periodontal disease and systemic health. Periodontol 2000 25:21–36

    CAS  Article  PubMed  Google Scholar 

  35. Jeffcoat MK, Geurs NC, Reddy MS, Cliver SP, Goldenberg RL, Hauth JC (2001) Periodontal infection and preterm birth: results of a prospective study. J Am Dent Assoc 132:875–880

    CAS  PubMed  Google Scholar 

  36. López NJ, Smith PC, Gutierrez J (2002) Higher risk of preterm birth and low birth weight in women with periodontal disease. J Dent Res 81:58–63

    Article  PubMed  Google Scholar 

  37. Slade GD, Ghezzi EM, Heiss G, Beck JD, Riche E, Offenbacher S (2003) Relationship between periodontal disease and C-reactive protein among adults in the Atherosclerosis Risk in Communities study. Arch Intern Med 163:1172–1179

    Article  PubMed  Google Scholar 

  38. Lowe GDO, Woodward M, Rumley A, Morrison C, Tunstall-Pedoe H, Stephen K (2003) Total tooth loss and prevalent cardiovascular disease in men and women: possible roles of citrus fruit consumption, vitamin C, and inflammatory and thrombotic variables. J Clin Epidemiol 56:694–700

    Article  PubMed  Google Scholar 

  39. Bos MJ, Schipper CM, Koudstaal PJ, Witteman JCM, Hofman A, Breteler MMB (2006) High serum C-reactive protein level is not an independent predictor for stroke: the Rotterdam Study. Circulation 114:1591–1598

    CAS  Article  PubMed  Google Scholar 

  40. Papapanou PN, Neiderud AM, Sandros J, Dahlén G (2001) Checkerboard assessments of serum antibodies to oral microbiota as surrogate markers of clinical periodontal status. J Clin Periodontol 28:103–106

    CAS  Article  PubMed  Google Scholar 

  41. Papapanou PN, Neiderud AM, Disick E, Lalla E, Miller GC, Dahlén G (2004) Longitudinal stability of serum immunoglobulin G responses to periodontal bacteria. J Clin Periodontol 31:985–990

    CAS  Article  PubMed  Google Scholar 

  42. Pussinen PJ, Vilkuna-Rautiainen T, Alfthan G, Mattila K, Asikainen S (2002) Multiserotype enzyme-linked immunosorbent assay as a diagnostic aid for periodontitis in large-scale studies. J Clin Microbiol 40:512–518

    CAS  Article  PubMed  Google Scholar 

  43. Hyman JJ, Albandar JM, Rams TE, Adesanya MR, Winn DM, Ebersole JL (2002) Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans serum antibodies and periodontal disease severity in the United States adults. J Dent Res (special issue) 81: abstract #0795, A–121

  44. Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366:1809–1820

    Article  PubMed  Google Scholar 

  45. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144

    CAS  Article  PubMed  Google Scholar 

  46. Haraszthy VI, Zambon JJ, Trevisan M, Zeid M, Genco RJ (2000) Identification of periodontal pathogens in atheromatous plaques. J Periodontol 71:1554–1560

    CAS  Article  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

  1. Department of Periodontology and Oral Medicine, Medical Faculty, University of Nis, Nade Tomic 3/5, 18000, Nis, Serbia

    A. Pejcic & L. J. Kesic

  2. Institute of Biology and Human Genetics, Dental Faculty, University of Belgrade, Belgrade, Serbia

    J. Milasin

Authors
  1. A. Pejcic
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. J. Kesic
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Milasin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Pejcic.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pejcic, A., Kesic, L.J. & Milasin, J. C-reactive protein as a systemic marker of inflammation in periodontitis. Eur J Clin Microbiol Infect Dis 30, 407–414 (2011). https://doi.org/10.1007/s10096-010-1101-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-010-1101-1

Keywords

  • Periodontitis
  • Periodontal Pocket
  • Pocket Depth
  • Periodontal Pathogen
  • Periodontal Status