Clinical Rheumatology

, Volume 33, Issue 4, pp 505–509 | Cite as

Periodontitis treatment improves systemic lupus erythematosus response to immunosuppressive therapy

  • Cristiana Fabbri
  • Ricardo Fuller
  • Eloisa Bonfá
  • Lissiane K. N. Guedes
  • Paulo Sergio R. D’Alleva
  • Eduardo F. Borba
Original Article


Periodontal disease (POD) may affect rheumatic diseases severity, but there are no data regarding the effect of its treatment on disease activity in SLE patients under immunosuppressive therapy. Forty-nine consecutive SLE patients (SLEDAI ≥ 2) with POD and under corticosteroid and cyclophosphamide pulse therapy (IVCYC) were selected. Periodontal assessment included bleeding gingival index (BGI), probing depth (PD), and probing attachment level (PAL). At entry, POD was defined as BGI > 1 and patients were assigned to groups according to the availability of odontological intervention in TREATED (n = 32) and NOT TREATED (n = 17). SLEDAI and POD parameters were determined at entry and after 3 months. Age, female gender, and race were alike among TREATED and NOT TREATED (p > 0.05). Both groups had also comparable disease duration (10.7 ± 6.8 vs. 11.0 ± 6.6, p = 0.83), IVCYC number (5.8 ± 4.8 vs. 4.5 ± 4.8, p = 0.17), and SLEDAI (5.9 ± 4.2 vs. 6.3 ± 4.3, p = 0.73) as well as POD parameters [BGI (40.8 ± 31.0 vs. 40.7 ± 36.2 %, p = 0.89), PD (1.7 ± 1.8 vs. 1.5 ± 0.60 mm, p = 0.80), and PAL (2.5 ± 1.9 vs. 1.9 ± 1.1 mm, p = 0.18)]. At the end of the study, TREATED group had a significant improvement in SLEDAI (5.9 ± 4.2 vs. 3.4 ± 3.3, p = 0.04) with a paralleled reduction in BGI (40.8 ± 31.0 vs. 15.2 ± 17.2 %, p < 0.01), PD (1.7 ± 1.8 vs. 1.1 ± 0.3 mm, p < 0.01), and PAL (2.5 ± 1.9 vs. 1.7 ± 0.9 mm, p < 0.01). In contrast, SLEDAI (6.3 ± 4.3 vs. 6.0 ± 5.5, p = 0.40) and POD parameters [BGI (p = 0.33), PD (p = 0.91), and PAL (p = 0.39)] remained largely unchanged in NOT TREATED group. Periodontal disease treatment seems to have a beneficial effect in controlling disease activity in SLE patients under immunosuppressive therapy. Therefore, management of this modifiable risk factor is recommended.


Inflammation Periodontitis Systemic lupus erythematosus Treatment 


  1. 1.
    Flemmig TF (1999) Periodontitis. Ann Periodontol 4(1):32–88PubMedCrossRefGoogle Scholar
  2. 2.
    Mercado F, Marshall R, Klestov A, Bartold P (2000) Is there a relationship between rheumatoid arthritis and periodontal disease? J Clin Periodontol 27:267–272PubMedCrossRefGoogle Scholar
  3. 3.
    Mercado F, Marshall RI, Klestov A, Bartold PM (2001) Relationship between rheumatoid arthritis and periodontitis. J Periodontol 72:779–787PubMedCrossRefGoogle Scholar
  4. 4.
    Marotte H, Farge P, Gaudin P, Alexandre C, Mougin B, Miossec P (2006) The association between periodontal disease and joint destruction in rheumatoid arthritis extends the link between the HLA-Dr shared epitope and severity of bone destruction. Ann Rheum Dis 65:905–909PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Abou-raya S, Abou-Raya A, Naim A, Abuelkheir H (2008) Rheumatoid arthritis, periodontal disease and coronary artery disease. Clin Rheumatol 27:421–427PubMedCrossRefGoogle Scholar
  6. 6.
    Pischon N, Pischon T, Kröger J, Gülmez E, Kleber BM, Bernimoulin JP, Landau H, Brinkmann PG, Schlattmann P, Zernicke J, Buttgereit F, Detert J (2008) Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol 79(6):979–986PubMedCrossRefGoogle Scholar
  7. 7.
    de Pablo P, Dietrich T, McAlindon TE (2008) Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol 35:70–76PubMedGoogle Scholar
  8. 8.
    Mutlu S, Richards A, Maddison P, Scully C (1993) Gingival and periodontal health in systemic lupus erythematosus. Community Dent Oral Epidemiol 21(3):158–161PubMedCrossRefGoogle Scholar
  9. 9.
    Rhodus NL, Johnson DK (1990) The prevalence of oral manifestations of systemic lupus erythematosus. Quintessence Int 21(6):461–465PubMedGoogle Scholar
  10. 10.
    Novo E, García-Mac Gregor E, Nava S, Perini L (1997) A possible defective estimation of antineutrophil cytoplasmic antibodies in systemic lupus erythematosus due to the coexistence of periodontitis: preliminary observations. P R Health Sci J 16(4):369–373PubMedGoogle Scholar
  11. 11.
    Meyer U, Kleinheinz J, Gaubitz M, Schulz M, Weingart D, Joos U (1997) Oral manifestations in patients with systemic lupus erythematosus. Mund Kiefer Gesichtschir 1(2):90–94PubMedCrossRefGoogle Scholar
  12. 12.
    Novo E, Garcia-MacGregor E, Viera N, Chaparro N, Crozzoli Y (1999) Periodontitis and anti-neutrophil cytoplasmic antibodies in systemic lupus erythematosus and rheumatoid arthritis: a comparative study. J Periodontol 70(2):185–188PubMedCrossRefGoogle Scholar
  13. 13.
    Kobayashi T, Ito S, Yamamoto K, Hasegawa H, Sugita N, Kuroda T, Kaneko S, Narita I, Yasuda K, Nakano M, Gejyo F, Yoshie H (2003) Risk of periodontitis in systemic lupus erythematosus is associated with Fcgamma receptor polymorphisms. J Periodontol 74(3):378–384PubMedCrossRefGoogle Scholar
  14. 14.
    Fernandes EG, Savioli C, Siqueira JT, Silva CA (2007) Oral health and the masticatory system in juvenile systemic lupus erythematosus. Lupus 16(9):713–719PubMedCrossRefGoogle Scholar
  15. 15.
    Riberio J, Leao A, Novaes AB (2005) Periodontal infection as a possible severity factor for rheumatoid arthritis. J Clin Periodontol 32:412–416CrossRefGoogle Scholar
  16. 16.
    Al-Katma MK, Bissada NF, Bordeaux JM, Sue J, Askari AD (2007) Control of periodontal infection reduces the severity of active rheumatoid arthritis. J Clin Rheumatol 13(3):134–137PubMedCrossRefGoogle Scholar
  17. 17.
    Ortiz P, Bissada NF, Palomo L, Han YW, Al-Zahrani MS, Panneerselvam A, Askari A (2009) Periodontal therapy reduces the severity of active rheumatoid arthritis in patients treated with or without tumor necrosis factor inhibitors. J Periodontol 80(4):535–540PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277PubMedCrossRefGoogle Scholar
  19. 19.
    Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH, the committee on prognosis studies in SLE (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. Arthritis Rheum 35:630–640PubMedCrossRefGoogle Scholar
  20. 20.
    Ainamo J, Bay I (1975) Problems and proposals for recording gingivitis and plaque. Int Dent J 25:229–235PubMedGoogle Scholar
  21. 21.
    Silness J, Löe H (1964) Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22:121–135PubMedCrossRefGoogle Scholar
  22. 22.
    Löe H (1967) The gingival index, the plaque index and the retention index systems. J Periodontol 38(6 Suppl):610–616PubMedCrossRefGoogle Scholar
  23. 23.
    Grossi SG, Zambon JJ, Ho AW, Koch G, Dunford RG, Machtei EE, Norderyd OM, Genco RJ (1994) Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol 65(3):260–267PubMedCrossRefGoogle Scholar
  24. 24.
    Grossi SG, Genco RJ, Machtei EE, Ho AW, Koch G, Dunford R, Zambon JJ, Hausmann E (1995) Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J Periodontol 66(1):23–29PubMedCrossRefGoogle Scholar
  25. 25.
    Vaudo G, Bocci EB, Shoenfeld Y, Schillaci G, Wu R, Del Papa N, Vitali C, Delle Monache F, Marchesi S, Mannarino E, Gerli R (2005) Precocious intima-media thickening in patients with primary Sjögren’s syndrome. Arthritis Rheum 52(12):3890–3897PubMedCrossRefGoogle Scholar
  26. 26.
    Najera MP, al-Hashimi I, Plemons JM, Rivera-Hidalgo F, Rees TD, Haghighat N, Wright JM (1997) Prevalence of periodontal disease in patients with Sjögren’s syndrome. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 83(4):453–457PubMedCrossRefGoogle Scholar
  27. 27.
    Boutsi EA, Paikos S, Dafni UG, Moutsopoulos HM, Skopouli FN (2000) Dental and periodontal status of Sjögren's syndrome. J Clin Periodontol 27(4):231–235PubMedCrossRefGoogle Scholar
  28. 28.
    Ciancio SG (2004) Medications’ impact on oral health. J Am Dent Assoc 135(10):1440–1448PubMedCrossRefGoogle Scholar
  29. 29.
    Ciancio SG (2005) Medications: a risk factor for periodontal disease diagnosis and treatment. J Periodontol 76(11 Suppl):2061–2065PubMedCrossRefGoogle Scholar
  30. 30.
    Abdellatif HM, Burt BA (1987) An epidemiological investigation into the relative importance of age and oral hygiene status as determinants of periodontitis. J Periodontal Res 66(13):1987Google Scholar
  31. 31.
    Sooriyamoorthy M, Gower DB (1989) Hormonal influences in gingival tissue: relationship to periodontal disease. J Clin Periodontol 16:201–208PubMedCrossRefGoogle Scholar
  32. 32.
    Safkan B, Knnutila M (1984) Corticosteroid therapy and periodontal disease. J Clin Periodontol 11:515–522PubMedCrossRefGoogle Scholar
  33. 33.
    Been V, Engel D (1984) The effects of immunosuppressive drugs on periodontal inflammation in human renal allograft patients. J Periodontol 53:245–248CrossRefGoogle Scholar
  34. 34.
    Lehman TJA (1995) A practical guide to systemic lupus erythematosus. Pediatr Clin N Am 42:1223–1227Google Scholar
  35. 35.
    Rezaieyazdi Z, Sahebari M, Hatef MR, Abbasi B, Rafatpanah H, Tavakol Afshari J, Esmaily H (2011) Is there any correlation between high sensitive CRP and disease activity in systemic lupus erythematosus? Lupus 20:1494PubMedCrossRefGoogle Scholar
  36. 36.
    Szalai AJ (2004) C-Reactive protein (CRP) and autoimmune disease:facts and conjectures. Clin Dev Immunol 11:221–226PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Rose NR (2010) Autoimmunity, infection and adjuvants. Lupus 19(4):354–358PubMedCrossRefGoogle Scholar
  38. 38.
    Rogers MA, Levine DA, Blumberg N, Fisher GG, Kabeto M, Langa KM (2012) Antigenic challenge in the etiology of autoimmune disease in women. J Autoimmun 38(2–3):J97–J102PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Navarra SV, Leynes MSN (2010) Infections in systemic lupus erythematosus. Lupus 19(12):1419–1424PubMedCrossRefGoogle Scholar
  40. 40.
    Sebastiani GD, Galeazzi M (2009) Infection—genetics relationship in systemic lupus erythematosus. Lupus 18(13):1169–1175PubMedCrossRefGoogle Scholar
  41. 41.
    Pessoa L, Galvão V, Santos-Neto L (2011) Periodontal disease as a risk factor for cardiovascular disease: suggestion of a further link in systemic lupus erythematosus. Med Hypotheses 77(2):286–289PubMedCrossRefGoogle Scholar
  42. 42.
    Li X, Tse HF, Yiu KH, Li LS, Jin L (2011) Effect of periodontal treatment on circulating CD34(+) cells and peripheral vascular endothelial function: a randomized controlled trial. J Clin Periodontol 38(2):148–156PubMedCrossRefGoogle Scholar
  43. 43.
    Pisetsky DS, Vrabie IA (2009) Antibodies to DNA: infection or genetics? Lupus 18(13):1176–1180PubMedCrossRefGoogle Scholar
  44. 44.
    Chai L, Song YQ, Leung WK (2012) Genetic polymorphism studies in periodontitis and Fcγ receptors. Periodontal Res 47(3):273–285CrossRefGoogle Scholar

Copyright information

© Clinical Rheumatology 2014

Authors and Affiliations

  • Cristiana Fabbri
    • 2
  • Ricardo Fuller
    • 1
    • 3
  • Eloisa Bonfá
    • 1
  • Lissiane K. N. Guedes
    • 1
  • Paulo Sergio R. D’Alleva
    • 2
  • Eduardo F. Borba
    • 1
  1. 1.Rheumatology Division of São Paulo UniversityFaculdade de Medicina da Universidade de São PauloSão PauloBrazil
  2. 2.Odontology Division of São Paulo UniversityFaculdade de Medicina da Universidade de São PauloSão PauloBrazil
  3. 3.Rheumatology Division of São Paulo UniversityFaculdade de Medicina da Universidade de São PauloSão PauloBrazil

Personalised recommendations