Skip to main content
Egyptian Rheumatology and Rehabilitation
Download PDF
  • Original article
  • Open access
  • Published:

Periodontal microbiota in a cohort of Egyptian patients with rheumatoid arthritis and their relation to serum and gingival anticitrullinated peptide protein antibodies and different disease parameters

Egyptian Rheumatology and Rehabilitation volume 45, pages 167–174 (2018)Cite this article

Abstract

Objective

The possibility of infectious trigger at the gingival site in rheumatoid arthritis (RA) was reported in previous studies. The aim of our study is to determine the organisms causing periodontitis (PD) in a cohort of Egyptian patients with RA and their relation to serum and gingival anticitrullinated peptide protein antibodies (ACPA) level and other disease parameters.

Patients and methods

A prospective cohort study was conducted on 100 consecutive Egyptian patients with RA. Disease activity was assessed by applying disease activity score-28, and functional status was measured using health assessment questionnaire. Dental examination, serum rheumatoid factor, ACPA in serum and gingival crevicular fluid (GCF), and radiograph of the hands were done for all patients. GCF culture was performed for all cases with PD for Porphyromonas gingivalis (Pg), Aggregatibacter actinomycetemcomitans (Aa), and Prevotella intermedia (Pi).

Results

Of the 100 patients, 66 patients had PD; of them, GCF culture was performed, and Pg, Aa, and Pi were found in 60.6, 15.2, and 30.3% of patients with RA with PD, respectively. Gingival ACPA showed significant higher level with Pg than Pi cases (P=0.047). No statistically significant difference was detected on comparing Pg with Aa or Aa with Pi. Aa-positive cases were associated with significantly higher level of C-reactive protein than Pi-positive cases (P=0.029), whereas no statistical significant difference was detected between Pg- and Aa-positive or Pi-positive cases.

Conclusion

Our findings support the relationship between PD and infectious trigger at the gingival site and RA. Pg is the most prevalent periodontal microbiota in our cohort of patients with RA with PD that is associated with significant higher level of gingival ACPA. None of the detected organisms correlated with the degree of RA activity or other disease parameters, apart from significantly higher C-reactive protein level with Aa.

References

  1. Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet 2010; 376:1094–1108.

    Article  Google Scholar 

  2. Ursell LK, Metcalf JL, Parfrey LW, Knight R. Defining the Human Microbiome. Nutr Rev 2012; 70 (Suppl 1):S38–S44.

    Article  Google Scholar 

  3. Brusca SB, Abramson SB, Scher JU. Microbiome and mucosal inflammation as extra-articular triggers for rheumatoid arthritis and autoimmunity. Curr Opin Rheumatol 2014; 26:101–107.

    Article  CAS  Google Scholar 

  4. Trosvik P, de Muinck EJ. Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa. Microbiome 2015; 3:44.

    Article  Google Scholar 

  5. Ogrendik M, Kokino S, Ozdemir F, Bird PS, Hamlet S. Serum antibodies to oral anaerobic bacteria in patients with rheumatoid arthritis. Med Gen Med 2005; 7:2.

    Google Scholar 

  6. Rosenstein ED, Weissmann G, Greenwald RA. Porphyromonas gingivalis, periodontitis and rheumatoid arthritis. Med Hypotheses 2009; 73:457–458.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Sandros J, Karlsson C, Lappin DF, Madianos PN, Kinane DF, Papapanou PN. Cytokine responses of oral epithelial cells to Porphyromonas gingivalis infection. J Dent Res 2000; 79:1808–1814.

    Article  CAS  Google Scholar 

  9. Eriksson K, Nise L, Kats A, Luttropp E, Catrina AI, Askling J, et al. Prevalence of periodontitis in patients with established rheumatoid arthritis: a Swedish population based case-control study. PLoS One 2016; 11:e 0155956.

  10. Payne JB, Golub LM, Thiele GM, Mikuls TR. The link between periodontitis and rheumatoid arthritis: a Periodontist’s perspective. Curr Oral Health Rep 2015; 2:20–29.

    Article  Google Scholar 

  11. Wegner N, Wait R, Sroka A, Eick S, Nguyen KA, Lundberg K, et al. Peptidylargininedeiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 2010; 62:2662–2672.

    Article  CAS  Google Scholar 

  12. Dye BA, Choudhary K, Shea S, Papapanou PN. Serum antibodies to periodontal pathogens and markers of systemic inflammation. J Clin Periodontol 2005; 32:1189–1199.

    Article  CAS  Google Scholar 

  13. Okada M, Kobayashi T, Ito S, Yokoyama T, Komatsu Y, Abe A, et al. Antibody responses to periodontopathic bacteria in relation to rheumatoid arthritis in Japanese adults. J Periodontol 2011; 82:1433–1441.

    Article  CAS  Google Scholar 

  14. Konig MF, Abusleme L, Reinholdt J, Palmer RJ, Teles RP, Sampson K, et al. Aggregatibacteractinomycetemcomitans-induced hypercitrullination links periodontal infection to autoimmunity in rheumatoid arthritis. Sci Transl Med 2016; 8:369ra176.

  15. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Ann Rheum Dis 2010; 69:1580–1588.

    Article  Google Scholar 

  16. Aletaha D, Landewe R, Karonitsch T, Bathon J, Boers M, Bombardier C, et al. Reporting disease activity in clinical trials of patients with rheumatoid arthritis: EULAR/ACR collaborative recommendations. Arthritis Rheum 2008; 59:137–147.

    Article  Google Scholar 

  17. DaMotaFalcao D, Ciconelli RM, Ferraz MB. Translation and cultural adaptation of quality of life questionnaires: an evaluation of methodology. J Rheumatol 2003; 30:379–385.

    PubMed  Google Scholar 

  18. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999; 4:1–6.

    Article  CAS  Google Scholar 

  19. Scott DL, Laasonen L, Priolo F, Houssien DA, Bacarini L, Cerase A, et al. The radiological assessment of rheumatoid arthritis. Clin Exp Rheumatol 1997; 15(Suppl 17):S53–S61.

  20. Rose HM, Peass E, Takayanagi H, Juji T. Differential agglutination of normal sensitized sheep erythrocyte sera of patients with rheumatoid arthritis. Pro Soc Exp Biol 1980; 68:1–5.

    Google Scholar 

  21. Swart A, Burlingame RW, Gürtler I, Mahler M. Third generation anti-citrullinated peptide antibody assay is a sensitive marker in rheumatoid factor negative rheumatoid arthritis. Clin Chim Acta 2012; 414:266–272.

    Article  CAS  Google Scholar 

  22. Goutoudi P, Diza E, Arvanitidou M. Effect of periodontal therapy on crevicular fluid interleukin-6 and interleukin-8 levels in chronic periodontitis. Int J Dent 2012; 36:290–295.

    Google Scholar 

  23. Ashimoto A, Chen C, Bakker I, Slots J. Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol 1996; 11:266–273.

    Article  CAS  Google Scholar 

  24. Kirkpatrick LA, Feeney BC. A simple guide to IBM SPSS statistics for version 20.0. Student ed. Belmont, CA: Wadsworth, Cengage Learning 2013.

  25. Mercado FB, Marshal RI, Klestov AC, Bartold PM. Is there a relationship between rheumatoid arthritis and periodontal disease? J Clin Periodontol 2000; 27:267–272.

    Article  CAS  Google Scholar 

  26. Mercado FB, Marshall RI, Klestov AC, Bartold PM. Relationship between rheumatoid arthritis and periodontitis. J Periodontol 2001; 72:779–787.

    Article  CAS  Google Scholar 

  27. Huang LG, Chen G, Chen DY, Chen HH. Factors associated with the risk of gingival disease in patients with rheumatoid arthritis. PLoS One 2017; 12:e0186346.

    Article  Google Scholar 

  28. Gargiulo AVJr, Toto PD, Robinson JA, et al. Latex slide agglutination vs. ELISA system. Rheumatoid factor detection in inflamed human gingiva. J Periodontal Res 1985; 20:31–34.

    PubMed  Google Scholar 

  29. 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.

    Article  Google Scholar 

  30. Scher JU, Ubeda C, Equinda M, Khanin R, Buischi Y, Viale A, et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum 2012; 64:3083–3094.

    Article  Google Scholar 

  31. Ziebolz D, Pabel SO, Lange K, Krohn-Grimberghe B, Hornecker E, Mausberg RF. Clinical periodontal and microbiologic parameters in patients with rheumatoid arthritis. J Periodontol 2011; 82:1424–1432.

    Article  CAS  Google Scholar 

  32. Mikuls TR, Payne JB, Reinhardt RA, Thiele GM, Maziarz E, Cannella AC, et al. Antibody responses to Porphyromonas gingivalis in subjects with rheumatoid arthritis and periodontitis. Int Immunopharmacol 2009; 9:38–42.

    Article  CAS  Google Scholar 

  33. Mikuls TR, Thiele GM, Deane KD, Payne JB, O’Dell JR, Yu F, et al. Porphyromonas gingivalis and disease-related autoantibodies in individuals at increased risk of rheumatoid arthritis. Arthritis Rheum 2012; 64:3522–3530.

    Article  CAS  Google Scholar 

  34. De Smit MD, Westra J, Vissink A, Doornbos-van der Meer B, Brouwer E, van Winkelhoff AJ. Periodontitis in established rheumatoid arthritis patients: a cross-sectional clinical, microbiological and serological study. Arthritis Res Ther 2012; 14:222.

    Article  Google Scholar 

  35. Harvey GP, Fitzsimmons TR, Dhamarpatni AA, Marchant C, Haynes DR, Bartold PM. J Expression of peptidylarginine deiminase-2 and -4, citrullinated proteins and anti-citrullinated protein antibodies in human gingiva. J Periodontal Res 2013; 48:252–261.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Internal Medicine, Faculty of Medicine, Alexandria University, Sidi Gaber Street, Alexandria, 21523, Egypt

    Eiman Soliman & Abeer Abdelati MD

  2. Departments of Oral Medicine and Periodontology, Faculty of Dentistry, Alexandria University, Alexandria, Egypt

    Rania Fahmy & Mona Helmy

Authors
  1. Eiman Soliman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abeer Abdelati MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rania Fahmy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mona Helmy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abeer Abdelati MD.

Additional information

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 License, which allows others to remix, tweak, and build upon the work noncommercially, as long as the author is credited and the new creations are licensed under the identical terms.

Rights and permissions

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soliman, E., Abdelati, A., Fahmy, R. et al. Periodontal microbiota in a cohort of Egyptian patients with rheumatoid arthritis and their relation to serum and gingival anticitrullinated peptide protein antibodies and different disease parameters. Egypt Rheumatol Rehabil 45, 167–174 (2018). https://doi.org/10.4103/err.err_29_18

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.4103/err.err_29_18

Keywords