Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
권호 표지
DOI QR코드

DOI QR Code

Effect of anti-rheumatic agents on periodontal parameters and biomarkers of inflammation: a systematic review and meta-analysis

  • Han, Ji-Young (Division of Periodontology, Department of Dentistry, Hanyang University College of Medicine) ;
  • Reynolds, Mark A. (Department of Periodontics, University of Maryland School of Dentistry)
  • Received : 2011.11.03
  • Accepted : 2012.01.05
  • Published : 2012.02.29
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: Anti-rheumatic agents target common molecular pathways of inflammation in rheumatoid arthritis (RA) and periodontitis. The purpose of this study was to determine the relative effect of anti-rheumatic agents on the levels of inflammatory biomarkers and periodontal inflammation in RA patients with periodontitis. Methods: A systematic review and meta-analysis were conducted of studies comparing periodontal parameters of inflammation, such as bleeding on probing, and biomarkers of inflammation in RA patients with periodontitis and healthy adults with and without periodontitis. The search included the electronic databases MEDLINE, Cochrane Database of Systematic Reviews, and Google Scholar, inclusive through October 2011, with no language restrictions. Hand searches were conducted of the bibliographies of related journals and systematic reviews. Observational and interventional studies assessing the effects of antirheumatic therapy qualified for inclusion. Two reviewers performed independent data extraction and risk-of-bias assessment. Of the 187 identified publications, 13 studies fulfilled the inclusion criteria. Results: When compared to healthy adults without periodontitis, RA subjects were found to have significantly higher levels of bleeding on probing and limited evidence of higher levels of interleukin-$1{\beta}$ and tumor necrosis factor-${\alpha}$ (TNF-${\alpha}$) in gingival crevicular fluid and saliva. No consistent differences were found in periodontal parameters and inflammatory biomarkers between RA subjects and adults with periodontitis. Studies evaluating the effect of anti-TNF-${\alpha}$ therapy in RA subjects with periodontitis have yielded inconsistent results. Conclusions: There are limited data, however, to suggest that anti-TNF-${\alpha}$ agents can reduce local production of inflammatory cytokines and periodontal inflammation in RA patients with periodontitis.

Keywords

References

  1. Symmons DP. Epidemiology of rheumatoid arthritis: determinants of onset, persistence and outcome. Best Pract Res Clin Rheumatol 2002;16:707-22. https://doi.org/10.1053/berh.2002.0257
  2. Bartold PM, Marshall RI, Haynes DR. Periodontitis and rheumatoid arthritis: a review. J Periodontol 2005;76(11 Suppl):2066-74. https://doi.org/10.1902/jop.2005.76.11-S.2066
  3. Pejcic A, Kesic LJ, Milasin J. C-reactive protein as a systemic marker of inflammation in periodontitis. Eur J Clin Microbiol Infect Dis 2011;30:407-14. https://doi.org/10.1007/s10096-010-1101-1
  4. Greenwald RA, Kirkwood K. Adult periodontitis as a model for rheumatoid arthritis (with emphasis on treatment strategies). J Rheumatol 1999;26:1650-3.
  5. Liao F, Li Z, Wang Y, Shi B, Gong Z, Cheng X. Porphyromonas gingivalis may play an important role in the pathogenesis of periodontitis-associated rheumatoid arthritis. Med Hypotheses 2009;72:732-5. https://doi.org/10.1016/j.mehy.2008.12.040
  6. Birkedal-Hansen H. Role of cytokines and inflammatory mediators in tissue destruction. J Periodontal Res 1993; 28(6 Pt 2):500-10. https://doi.org/10.1111/j.1600-0765.1993.tb02113.x
  7. Mercado F, Marshall RI, Klestov AC, Bartold PM. Is there a relationship between rheumatoid arthritis and periodontal disease? J Clin Periodontol 2000;27:267-72. https://doi.org/10.1034/j.1600-051x.2000.027004267.x
  8. Pischon N, Pischon T, Kröger J, Gulmez E, Kleber BM, Bernimoulin JP, et al. Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol 2008;79:979-86. https://doi.org/10.1902/jop.2008.070501
  9. Moen K, Brun JG, Valen M, Skartveit L, Eribe EK, Olsen I, et al. Synovial inflammation in active rheumatoid arthritis and psoriatic arthritis facilitates trapping of a variety of oral bacterial DNAs. Clin Exp Rheumatol 2006;24:656-63.
  10. Saal JG, Krimmel M, Steidle M, Gerneth F, Wagner S, Fritz P, et al. Synovial Epstein-Barr virus infection increases the risk of rheumatoid arthritis in individuals with the shared HLA-DR4 epitope. Arthritis Rheum 1999;42:1485-96. https://doi.org/10.1002/1529-0131(199907)42:7<1485::AID-ANR24>3.0.CO;2-7
  11. Slots J. Herpesviruses in periodontal diseases. Periodontol 2000 2005;38:33-62. https://doi.org/10.1111/j.1600-0757.2005.00109.x
  12. Vincent C, de Keyser F, Masson-Bessière C, Sebbag M, Veys EM, Serre G. Anti-perinuclear factor compared with the so called "antikeratin" antibodies and antibodies to human epidermis filaggrin, in the diagnosis of arthritides. Ann Rheum Dis 1999;58:42-8. https://doi.org/10.1136/ard.58.1.42
  13. van Venrooij WJ, Pruijn GJ. Citrullination: a small change for a protein with great consequences for rheumatoid arthritis. Arthritis Res 2000;2:249-51. https://doi.org/10.1186/ar95
  14. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097. https://doi.org/10.1371/journal.pmed.1000097
  15. Kobayashi T, Murasawa A, Komatsu Y, Yokoyama T, Ishida K, Abe A, et al. Serum cytokine and periodontal profiles in relation to disease activity of rheumatoid arthritis in Japanese adults. J Periodontol 2010;81:650-7. https://doi.org/10.1902/jop.2010.090688
  16. Mayer Y, Balbir-Gurman A, Machtei EE. Anti-tumor necrosis factor-alpha therapy and periodontal parameters in patients with rheumatoid arthritis. J Periodontol 2009;80:1414-20. https://doi.org/10.1902/jop.2009.090015
  17. Miranda LA, Islabao AG, Fischer RG, Figueredo CM, Oppermann RV, Gustafsson A. Decreased interleukin-1beta and elastase in the gingival crevicular fluid of individuals undergoing anti-inflammatory treatment for rheumatoid arthritis. J Periodontol 2007;78:1612-9. https://doi.org/10.1902/jop.2007.060520
  18. Nilsson M, Kopp S. Gingivitis and periodontitis are related to repeated high levels of circulating tumor necrosis factor-alpha in patients with rheumatoid arthritis. J Periodontol 2008;79:1689-96. https://doi.org/10.1902/jop.2008.070599
  19. Biyikoglu B, Buduneli N, Kardeşler L, Aksu K, Oder G, Kutukculer N. Evaluation of t-PA, PAI-2, IL-1beta and PGE(2) in gingival crevicular fluid of rheumatoid arthritis patients with periodontal disease. J Clin Periodontol 2006;33:605-11. https://doi.org/10.1111/j.1600-051X.2006.00961.x
  20. Biyikoglu B, Buduneli N, Kardesler L, Aksu K, Pitkala M, Sorsa T. Gingival crevicular fluid MMP-8 and -13 and TIMP-1 levels in patients with rheumatoid arthritis and inflammatory periodontal disease. J Periodontol 2009;80:1307-14. https://doi.org/10.1902/jop.2009.090130
  21. Bozkurt FY, Berker E, Akkus S, Bulut S. Relationship between interleukin-6 levels in gingival crevicular fluid and periodontal status in patients with rheumatoid arthritis and adult periodontitis. J Periodontol 2000;71:1756-60. https://doi.org/10.1902/jop.2000.71.11.1756
  22. Bozkurt FY, Yetkin Ay Z, Berker E, Tepe E, Akkus S. Anti-inflammatory cytokines in gingival crevicular fluid in patients with periodontitis and rheumatoid arthritis: a preliminary report. Cytokine 2006;35:180-5. https://doi.org/10.1016/j.cyto.2006.07.020
  23. Havemose-Poulsen A, Sorensen LK, Stoltze K, Bendtzen K, Holmstrup P. Cytokine profiles in peripheral blood and whole blood cell cultures associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol 2005;76:2276-85. https://doi.org/10.1902/jop.2005.76.12.2276
  24. Havemose-Poulsen A, Westergaard J, Stoltze K, Skjodt H, Danneskiold-Samsøe B, Locht H, et al. Periodontal and hematological characteristics associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol 2006;77:280-8. https://doi.org/10.1902/jop.2006.050051
  25. Mirrielees J, Crofford LJ, Lin Y, Kryscio RJ, Dawson DR 3rd, Ebersole JL, et al. Rheumatoid arthritis and salivary biomarkers of periodontal disease. J Clin Periodontol 2010;37:1068-74. https://doi.org/10.1111/j.1600-051X.2010.01625.x
  26. Ortiz P, Bissada NF, Palomo L, Han YW, Al-Zahrani MS, Panneerselvam A, et al. Periodontal therapy reduces the severity of active rheumatoid arthritis in patients treated with or without tumor necrosis factor inhibitors. J Periodontol 2009;80:535-40. https://doi.org/10.1902/jop.2009.080447
  27. Pers JO, Saraux A, Pierre R, Youinou P. Anti-TNF-alpha immunotherapy is associated with increased gingival inflammation without clinical attachment loss in subjects with rheumatoid arthritis. J Periodontol 2008;79:1645-51. https://doi.org/10.1902/jop.2008.070616
  28. Berthelot JM, Le Goff B. Rheumatoid arthritis and periodontal disease. Joint Bone Spine 2010;77:537-41. https://doi.org/10.1016/j.jbspin.2010.04.015
  29. Ramamurthy NS, Greenwald RA, Celiker MY, Shi EY. Experimental arthritis in rats induces biomarkers of periodontitis which are ameliorated by gene therapy with tissue inhibitor of matrix metalloproteinases. J Periodontol 2005;76:229-33. https://doi.org/10.1902/jop.2005.76.2.229
  30. Cantley MD, Haynes DR, Marino V, Bartold PM. Pre-existing periodontitis exacerbates experimental arthritis in a mouse model. J Clin Periodontol 2011;38:532-41. https://doi.org/10.1111/j.1600-051X.2011.01714.x
  31. Hart FD, Huskisson EC. Non-steroidal anti-inflammatory drugs. Current status and rational therapeutic use. Drugs 1984;27:232-55. https://doi.org/10.2165/00003495-198427030-00004
  32. Reddy MS, Geurs NC, Gunsolley JC. Periodontal host modulation with antiproteinase, anti-inflammatory, and bone-sparing agents. A systematic review. Ann Periodontol 2003;8:12-37. https://doi.org/10.1902/annals.2003.8.1.12
  33. Curtis JR, Singh JA. Use of biologics in rheumatoid arthritis: current and emerging paradigms of care. Clin Ther 2011;33:679-707. https://doi.org/10.1016/j.clinthera.2011.05.044
  34. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988;31:315-24. https://doi.org/10.1002/art.1780310302
  35. Culshaw S, McInnes IB, Liew FY. What can the periodontal community learn from the pathophysiology of rheumatoid arthritis? J Clin Periodontol 2011;38 Suppl 11:106-13. https://doi.org/10.1111/j.1600-051X.2010.01669.x
  36. Feldmann M, Maini RN. Lasker Clinical Medical Research Award. TNF defined as a therapeutic target for rheumatoid arthritis and other autoimmune diseases. Nat Med 2003;9:1245-50. https://doi.org/10.1038/nm939
  37. Bartold PM, Cantley MD, Haynes DR. Mechanisms and control of pathologic bone loss in periodontitis. Periodontol 2000 2010;53:55-69. https://doi.org/10.1111/j.1600-0757.2010.00347.x
  38. Bergström J. Tobacco smoking and chronic destructive periodontal disease. Odontology 2004;92:1-8. https://doi.org/10.1007/s10266-004-0043-4
  39. Sugiyama D, Nishimura K, Tamaki K, Tsuji G, Nakazawa T, Morinobu A, et al. Impact of smoking as a risk factor for developing rheumatoid arthritis: a meta-analysis of observational studies. Ann Rheum Dis 2010;69:70-81. https://doi.org/10.1136/ard.2008.096487
  40. Zambon JJ, Grossi SG, Machtei EE, Ho AW, Dunford R, Genco RJ. Cigarette smoking increases the risk for subgingival infection with periodontal pathogens. J Periodontol 1996;67(10 Suppl):1050-4. https://doi.org/10.1902/jop.1996.67.10s.1050

Cited by

  1. Inflammatory mediators in the pathogenesis of periodontitis vol.15, pp.None, 2012, https://doi.org/10.1017/erm.2013.8
  2. Future prospects of systemic host modulatory agents in periodontal therapy vol.214, pp.9, 2012, https://doi.org/10.1038/sj.bdj.2013.432
  3. Prevalence and Severity of Periodontitis in Indonesian Patients With Rheumatoid Arthritis vol.84, pp.8, 2012, https://doi.org/10.1902/jop.2012.110321
  4. Blocking Proinflammatory Cytokine Release Modulates Peripheral Blood Mononuclear Cell Response toPorphyromonas gingivalis vol.84, pp.9, 2012, https://doi.org/10.1902/jop.2012.120422
  5. Periodontal disease and rheumatoid arthritis: the evidence accumulates for complex pathobiologic interactions vol.25, pp.3, 2012, https://doi.org/10.1097/bor.0b013e32835fb8ec
  6. Rheumatoid arthritis in the elderly and its relationship with periodontitis: A review vol.14, pp.1, 2012, https://doi.org/10.1111/ggi.12062
  7. Modifiable risk factors in periodontitis: at the intersection of aging and disease vol.64, pp.1, 2012, https://doi.org/10.1111/prd.12047
  8. Tumor Necrosis Factor-α and Oral Inflammation in Patients With Crohn Disease vol.85, pp.10, 2012, https://doi.org/10.1902/jop.2014.130644
  9. Does a biological link exist between periodontitis and rheumatoid arthritis? vol.4, pp.3, 2012, https://doi.org/10.5499/wjr.v4.i3.80
  10. An Evaluation of Non-Surgical Periodontal Therapy in Patients with Rheumatoid Arthritis vol.9, pp.None, 2012, https://doi.org/10.2174/1874210601509010150
  11. Periodontal Disease in Individuals With a Genetic Risk of Developing Arthritis and Early Rheumatoid Arthritis: A Cross-Sectional Study vol.87, pp.4, 2012, https://doi.org/10.1902/jop.2015.150455
  12. Serum Immunoglobulin G Levels to Porphyromonas gingivalis Peptidylarginine Deiminase Affect Clinical Response to Biological Disease-Modifying Antirheumatic Drug in Rheumatoid Arthritis vol.11, pp.4, 2012, https://doi.org/10.1371/journal.pone.0154182
  13. Decision Making in the Treatment of Patients With Rheumatoid Arthritis and Periodontitis: Scientific Evidence and Clinical Experience vol.6, pp.4, 2012, https://doi.org/10.1902/cap.2016.160021
  14. Periodontitis in early and chronic rheumatoid arthritis: a prospective follow-up study in Finnish population vol.7, pp.1, 2012, https://doi.org/10.1136/bmjopen-2016-011916
  15. Salivary TNFα levels in groups of subjects with rheumatoid arthritis and chronic periodontitis vol.10, pp.None, 2017, https://doi.org/10.1186/s13104-016-2341-7
  16. Personalization of biologic therapy in patients with rheumatoid arthritis: less frequently accounted choice-driving variables vol.14, pp.None, 2012, https://doi.org/10.2147/tcrm.s175772
  17. Effects of Conventional Synthetic Disease-Modifying Antirheumatic Drugs on Response to Periodontal Treatment in Patients with Rheumatoid Arthritis vol.2018, pp.None, 2018, https://doi.org/10.1155/2018/1465402
  18. Linkage of Periodontitis and Rheumatoid Arthritis: Current Evidence and Potential Biological Interactions vol.20, pp.18, 2012, https://doi.org/10.3390/ijms20184541
  19. Predictive factors related to the progression of periodontal disease in patients with early rheumatoid arthritis: a cohort study vol.19, pp.1, 2012, https://doi.org/10.1186/s12903-019-0939-6
  20. Temporomandibular joint function, periodontal health, and oral microbiome in early rheumatoid arthritis and at-risk individuals: a prospective cohort study protocol vol.6, pp.None, 2012, https://doi.org/10.1038/s41405-020-0034-8
  21. Biosensor and Lab-on-a-chip Biomarker-identifying Technologies for Oral and Periodontal Diseases vol.11, pp.None, 2012, https://doi.org/10.3389/fphar.2020.588480
  22. Periodontitis and rheumatoid arthritis: An update 2012‐2017 vol.83, pp.1, 2012, https://doi.org/10.1111/prd.12300
  23. Current understanding of periodontal disease pathogenesis and targets for host‐modulation therapy vol.84, pp.1, 2012, https://doi.org/10.1111/prd.12331
  24. The periodontal inflamed surface area is associated with the clinical response to biological disease-modifying antirheumatic drugs in rheumatoid arthritis: a retrospective study vol.30, pp.6, 2012, https://doi.org/10.1080/14397595.2019.1680100
  25. Associations of periodontal status in periodontitis and rheumatoid arthritis patients vol.51, pp.2, 2012, https://doi.org/10.5051/jpis.2006060303
  26. Association among periodontitis severity, anti‐agalactosyl immunoglobulin G titer, and the disease activity of rheumatoid arthritis vol.56, pp.4, 2012, https://doi.org/10.1111/jre.12867
  27. Periodontitis and rheumatoid arthritis: What have we learned about their connection and their treatment? vol.87, pp.1, 2012, https://doi.org/10.1111/prd.12385
  28. Influence of anti‐rheumatic agents on the periodontal condition of patients with rheumatoid arthritis and periodontitis: A systematic review and meta‐analysis vol.56, pp.6, 2012, https://doi.org/10.1111/jre.12925