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Periodontitis is associated with rheumatoid arthritis: a study with longstanding rheumatoid arthritis patients in Korea

  • Choi, In Ah (Department of Internal Medicine, Medical Research Center, Seoul National University College of Medicine) ;
  • Kim, Jin-Hee (Department of Periodontology, Seoul National University School of Dentistry) ;
  • Kim, Yong Mi (Department of Periodontology, Seoul National University School of Dentistry) ;
  • Lee, Joo Youn (Department of Molecular Medicine and Biopharmaceutical Sciences, Seoul National University) ;
  • Kim, Kyung Hwa (Department of Periodontology, Seoul National University School of Dentistry) ;
  • Lee, Eun Young (Department of Internal Medicine, Medical Research Center, Seoul National University College of Medicine) ;
  • Lee, Eun Bong (Department of Internal Medicine, Medical Research Center, Seoul National University College of Medicine) ;
  • Lee, Yong-Moo (Department of Periodontology, Seoul National University School of Dentistry) ;
  • Song, Yeong Wook (Department of Internal Medicine, Medical Research Center, Seoul National University College of Medicine)
  • Received : 2015.07.03
  • Accepted : 2015.09.02
  • Published : 2016.09.01

Abstract

Background/Aims: A cross-sectional study was undertaken to investigate the association between severity of periodontitis and clinical manifestation of rheumatoid arthritis (RA). Methods: Two hundred sixty-four RA patients and 88 age- and sex-matched controls underwent dental exam. Additionally, clinical manifestations including disease activity and anti-citrullinated protein antibodies were evaluated in RA patients. Results: The prevalence of moderate or severe periodontitis was higher in RA patients compared to controls (63.6% vs 34.1%, p < 0.001). In markers of periodontal inflammation, bleeding on probing was correlated with disease activity score 28 (r = 0.128, p = 0.041), RA disease duration (r = 0.211, p = 0.001), erythrocyte sedimentation rate (ESR; r = 0.141, p = 0.023), anti-cyclic citrullinated peptide antibody (r = 0.183, p = 0.009), and anti-citrullinated ${\alpha}$-enolase peptide-1 antibody (r = 0.143, p = 0.025). Gingival index was correlated with RA duration (r = 0.262, p < 0.001), ESR (r = 0.162, p = 0.009), anti-cyclic citrullinated peptide antibody (r = 0.203, p = 0.004) and anti-citrullinated ${\alpha}$-enolase peptide-1 antibody (r = 0.225, p < 0.001). Periodontal structural damage represented by probing pocket depth and clinical attachment level were less in RA patients with human leukocyte antigen (HLA)-DRB1 shared epitope compared than those without shared epitope (p = 0.005 and p =0.006, respectively). Conclusions: The prevalence of moderate or severe periodontitis was increased in RA patients compared to controls. Periodontal inflammation was correlated with RA disease duration, ESR, and anti-citrullinated protein antibodies. Periodontal structural damage was less in RA patients with HLA-DRB1 shared epitope.

Keywords

Acknowledgement

Supported by : Ministry of Science, ICT and Future Planning

References

  1. Cantaert T, De Rycke L, Bongartz T, et al. Citrullinated proteins in rheumatoid arthritis: crucial...but not sufficient! Arthritis Rheum 2006;54:3381-3389. https://doi.org/10.1002/art.22206
  2. Heliovaara M, Aho K, Aromaa A, Knekt P, Reunanen A. Smoking and risk of rheumatoid arthritis. J Rheumatol 1993;20:1830-1835.
  3. Silman AJ, Newman J, MacGregor AJ. Cigarette smoking increases the risk of rheumatoid arthritis: results from a nationwide study of disease-discordant twins. Arthritis Rheum 1996;39:732-735. https://doi.org/10.1002/art.1780390504
  4. Perry E, Kelly C, Eggleton P, De Soyza A, Hutchinson D. The lung in ACPA-positive rheumatoid arthritis: an initiating site of injury? Rheumatology (Oxford) 2014;53:1940-1950. https://doi.org/10.1093/rheumatology/keu195
  5. Pischon N, Pischon T, Kroger J, et al. Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol 2008;79:979-986. https://doi.org/10.1902/jop.2008.070501
  6. Mercado FB, Marshall RI, Klestov AC, Bartold PM. Relationship between rheumatoid arthritis and periodontitis. J Periodontol 2001;72:779-787. https://doi.org/10.1902/jop.2001.72.6.779
  7. Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G. Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation 2004;28:311-318. https://doi.org/10.1007/s10753-004-6641-z
  8. de Pablo P, Dietrich T, McAlindon TE. Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol 2008;35:70-76.
  9. Georgiou TO, Marshall RI, Bartold PM. Prevalence of systemic diseases in Brisbane general and periodontal practice patients. Aust Dent J 2004;49:177-184. https://doi.org/10.1111/j.1834-7819.2004.tb00070.x
  10. Arnett FC, Edworthy SM, Bloch DA, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988;31:315-324. https://doi.org/10.1002/art.1780310302
  11. Wegner N, Wait R, Sroka A, et al. Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and ${\alpha}$-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 2010;62:2662-2672. https://doi.org/10.1002/art.27552
  12. Arvikar SL, Collier DS, Fisher MC, et al. Clinical correlations with Porphyromonas gingivalis antibody responses in patients with early rheumatoid arthritis. Arthritis Res Ther 2013;15:R109. https://doi.org/10.1186/ar4289
  13. Lundberg K, Wegner N, Yucel-Lindberg T, Venables PJ. Periodontitis in RA-the citrullinated enolase connection. Nat Rev Rheumatol 2010;6:727-730. https://doi.org/10.1038/nrrheum.2010.139
  14. Dissick A, Redman RS, Jones M, et al. Association of periodontitis with rheumatoid arthritis: a pilot study. J Periodontol 2010;81:223-230. https://doi.org/10.1902/jop.2009.090309
  15. de Smit M, Westra J, Vissink A, et al. Periodontitis in established rheumatoid arthritis patients: a cross-sectional clinical, microbiological and serological study. Arthritis Res Ther 2012;14:R222. https://doi.org/10.1186/ar4061
  16. Mikuls TR, Payne JB, Yu F, et al. Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol 2014;66:1090-1100. https://doi.org/10.1002/art.38348
  17. Khantisopon N, Louthrenoo W, Kasitanon N, et al. Periodontal disease in Thai patients with rheumatoid arthritis. Int J Rheum Dis 2014;17:511-518.
  18. Joseph R, Rajappan S, Nath SG, Paul BJ. Association between chronic periodontitis and rheumatoid arthritis: a hospital-based case-control study. Rheumatol Int 2013;33:103-109. https://doi.org/10.1007/s00296-011-2284-1
  19. Vander Cruyssen B, Van Looy S, Wyns B, et al. DAS28 best reflects the physician's clinical judgment of response to infliximab therapy in rheumatoid arthritis patients: validation of the DAS28 score in patients under infliximab treatment. Arthritis Res Ther 2005;7:R1063-R1071. https://doi.org/10.1186/ar1787
  20. Lundberg K, Kinloch A, Fisher BA, et al. Antibodies to citrullinated alpha-enolase peptide 1 are specific for rheumatoid arthritis and cross-react with bacterial enolase. Arthritis Rheum 2008;58:3009-3019. https://doi.org/10.1002/art.23936
  21. Bannai M, Tokunaga K, Lin L, et al. Discrimination of human HLA-DRB1 alleles by PCR-SSCP (single-strand conformation polymorphism) method. Eur J Immunogenet 1994;21:1-9. https://doi.org/10.1111/j.1744-313X.1994.tb00170.x
  22. Im CH, Kang EH, Ryu HJ, et al. Anti-cyclic citrullinated peptide antibody is associated with radiographic erosion in rheumatoid arthritis independently of shared epitope status. Rheumatol Int 2009;29:251-256. https://doi.org/10.1007/s00296-008-0690-9
  23. Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condtion. Acta Odontol Scand 1964;22:121-135. https://doi.org/10.3109/00016356408993968
  24. Loe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 1963;21:533-551. https://doi.org/10.3109/00016356309011240
  25. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4:1-6. https://doi.org/10.1902/annals.1999.4.1.1
  26. Cantley MD, Haynes DR, Marino V, Bartold PM. Pre-existing periodontitis exacerbates experimental arthritis in a mouse model. J Clin Periodontol 2011;38:532-541. https://doi.org/10.1111/j.1600-051X.2011.01714.x
  27. Marchesan JT, Gerow EA, Schaff R, et al. Porphyromonas gingivalis oral infection exacerbates the development and severity of collagen-induced arthritis. Arthritis Res Ther 2013;15:R186. https://doi.org/10.1186/ar4376
  28. de Pablo P, Dietrich T, Chapple IL, et al. The autoantibody repertoire in periodontitis: a role in the induction of autoimmunity to citrullinated proteins in rheumatoid arthritis? Ann Rheum Dis 2014;73:580-586. https://doi.org/10.1136/annrheumdis-2012-202701
  29. American Dental Association Divison of Communications; Journal of the American Dental Association. For the dental patient: treating periodontal diseases. J Am Dent Assoc 2005;136:127. https://doi.org/10.14219/jada.archive.2005.0036
  30. Stastny P. Association of the B-cell alloantigen DRw4 with rheumatoid arthritis. N Engl J Med 1978;298:869-871. https://doi.org/10.1056/NEJM197804202981602
  31. Dougados M, Soubrier M, Antunez A, et al. Prevalence of comorbidities in rheumatoid arthritis and evaluation of their monitoring: results of an international, cross-sectional study (COMORA). Ann Rheum Dis 2014;73:62-68.

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