Skip to main content

Advertisement

SpringerLink
Log in

Risk association between scleroderma disease characteristics, periodontitis, and tooth loss

  • Original Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Systemic sclerosis (SSc) is a multi-system disorder that can have significant adverse effects on the health of the mouth. The aim of this study was to investigate the associations between the disease characteristics of SSc, periodontal disease (PD), and tooth loss. Fifty-four patients affected by SSc and 55 non-diseased controls were matched for age and gender. SSc was characterized in subtypes and with the mean duration of disease and the Modified Rodnan Skin Score [mRSS]. Patients were surveyed and examined through the evaluation of the periodontal parameters and the number of teeth. A logistic regression analysis showed that patients with SSc presented a higher number of missing teeth (p = 0.001) and a significant median increased odds 2.95 (95% CI 1.26 to 6.84) of PD (defined as clinical attachment loss, CAL) compared to nondiseased controls (6.83, 95% CI 1.94 to 24.36). Moreover, the fewer values of PD was correlated with mRSS in the total SSc group and with the mean duration of disease in patients with limited SSc (p = 0.007), even after adjusting this correlation with the presence of the major organ involvement. This study showed that patients with SSc presented increased odds of PD and tooth loss compared to non-diseased controls. In SSc patients, the magnitude of PD was strongly associated with the mRSS and with the mean duration of the disease. The clinicians should be aware of the potential systemic health problems related to PD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Derk CT, Jimenez SA (2003) Systemic sclerosis: current views of its pathogenesis. Autoimmun Rev 2:181–191

    Article  CAS  PubMed  Google Scholar 

  2. Mayes MD, Lacey JV Jr, Beebe-Dimmer J et al (2003) Prevalence, incidence, survival, and disease characteristics of systemic sclerosis in a large US population. Arthritis Rheum 48:2246–2255

    Article  PubMed  Google Scholar 

  3. Amin K, Clarke A, Sivakumar B et al (2011) The psychological impact of facial changes in scleroderma. Psychol Health Med 16:304–312

    Article  PubMed  Google Scholar 

  4. Matarese G, Isola G, Alibrandi A et al (2016) Occlusal and MRI characterizations in systemic sclerosis patients: A prospective study from Southern Italian cohort. Joint Bone Spine 83:57–62

    Article  PubMed  Google Scholar 

  5. Albilia JB, Lam DK, Blanas N, Clokie CM, Sándor GK (2007) Small mouths. . . big problems? A review of scleroderma and its oral health implications. J Can Dent Assoc 73:831–836

    PubMed  Google Scholar 

  6. Baron M, Hudson M, Tatibouet S et al (2014) The Canadian systemic sclerosis oral health study: orofacial manifestations and oral health-related quality of life in systemic sclerosis compared with the general population. Rheumatology 53:1386–1394

    Article  PubMed  PubMed Central  Google Scholar 

  7. Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS (1997) Advances in the pathogenesis of periodontitis: Summary of developments, clinical implications and future directions. Periodontol 14:216–248

    Article  CAS  Google Scholar 

  8. Matarese G, Isola G, Anastasi GP et al (2012) Immunohistochemical analysis of TGF-β1 and VEGF in gingival and periodontal tissues: a role of these biomarkers in the pathogenesis of scleroderma and periodontal disease. Int J Mol Med 30:502–508

    Article  PubMed  Google Scholar 

  9. Leung WK, Chu CH, Mok MY, Yeung KW, Ng SK (2011) Periodontal status of adults with systemic sclerosis: Case control study. J Periodontol 82:1140–1145

    Article  PubMed  Google Scholar 

  10. Matarese G, Isola G, Anastasi GP et al (2013) Effects of the Transforming Growth Factor Beta 1 and Vascular Endothelial Growth Factor expressions in the pathogenesis of periodontal disease. Eur J Inflamm 11:479–488

    Article  CAS  Google Scholar 

  11. Baron M, Hudson M, Dagenais M et al (2016) Relationship Between Disease Characteristics and Oral Radiologic Findings in Systemic Sclerosis: Results From a Canadian Oral Health Study. Arthritis Care Res [Hoboken] 68:673–680

    Article  Google Scholar 

  12. Pischon N, Hoedke D, Kurth S et al (2016) Increased Periodontal Attachment Loss in Patients With Systemic Sclerosis. J Periodontol 87:763–771

    Article  PubMed  Google Scholar 

  13. Hollan I, 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 13:134–137

    Article  Google Scholar 

  14. Masi AT (1980) Subcommittee for Scleroderma Criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. Preliminary criteria for the classification of systemic sclerosis [scleroderma]. Arthritis Rheum 23:581–590

    Article  Google Scholar 

  15. White B, Bauer EA, Goldsmith LA et al (1995) Guidelines for clinical trials in systemic sclerosis [scleroderma]. I. Disease-modifying interventions. The American College of Rheumatology Committee on Design and Outcomes in Clinical Trials in Systemic Sclerosis. Arthritis Rheum 38:351–360

    Article  CAS  PubMed  Google Scholar 

  16. Matarese G, Currò M, Isola G et al (2015) Transglutaminase 2 up-regulation is associated with RANKL/OPG pathway in cultured HPDL cells and THP-1-differentiated macrophages. Amino Acids 47:2447–2455

    Article  CAS  PubMed  Google Scholar 

  17. Silness J, Loe H (1964) Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22:121–135

    Article  CAS  PubMed  Google Scholar 

  18. Furst DE, Clements PJ, Steen VD et al (1998) The modified Rodnan skin score is an accurate reflection of skin biopsy thickness in systemic sclerosis. J Rheumatol 25:84–88

    CAS  PubMed  Google Scholar 

  19. Clements PJ, Furst DE (2003) Systemic Sclerosis, 2nd edn. Lippincott Williams & Wilkins, Los Angeles, pp 129–137

    Google Scholar 

  20. Dagenais M, MacDonald D, Baron M et al (2015) The Canadian Systemic Sclerosis Oral Health Study IV: oral radiographic manifestations in systemic sclerosis compared with the general population. Oral Surg Oral Med Oral Pathol Oral Radiol 120:104–111

    Article  PubMed  PubMed Central  Google Scholar 

  21. Isola G, Matarese G, Williams RC, et al (2017) The effects of a desiccant agent in the treatment of chronic periodontitis: a randomized, controlled clinical trial. Clin Oral Investig In press. https://doi.org/10.1007/s00784-017-2154-7

  22. Baron M, Hudson M, Tatibouet S et al (2015) Relationship between disease characteristics and orofacial manifestations in systemic sclerosis: Canadian Systemic Sclerosis Oral Health Study III. Arthritis Care Res [Hoboken] 67:681–690

    Article  Google Scholar 

  23. White SC, Frey NW, Blaschke DD et al (1977) Oral radiographic changes in patients with progressive systemic sclerosis [scleroderma]. J Am Dent Assoc 46:178–182

    Google Scholar 

  24. Isola G, Matarese G, Cordasco G, Rotondo F, Crupi A, Ramaglia L (2015) Anticoagulant therapy in patients undergoing dental interventions: a critical review of the literature and current perspectives. Minerva Stomatol 64:21–46

    CAS  PubMed  Google Scholar 

  25. Bender P, Bürgin WB, Sculean A, Eick S (2017) Serum antibody levels against Porphyromonas gingivalis in patients with and without rheumatoid arthritis - a systematic review and meta-analysis. Clin Oral Investig 21:33–42

    Article  PubMed  Google Scholar 

  26. Laugisch O, Wong A, Sroka A et al (2016) Citrullination in the periodontium--a possible link between periodontitis and rheumatoid arthritis. Clin Oral Investig 20:675–683

    Article  PubMed  Google Scholar 

  27. Ursini F, D'Angelo S, Padula A, et al (2017) Vitamin D deficiency in systemic sclerosis: a possible role of subclinical liver fibrosis? Retrospective analysis from an Italian cohort Clin Rheumatol. https://doi.org/10.1007/s10067-017-3709-3

  28. Scardina GA, Pizzigatti ME, Messina P (2005) Periodontal microcirculatory abnormalities in patients with systemic sclerosis. J Periodontol 76:1991–1995

    Article  CAS  PubMed  Google Scholar 

  29. Ozcelik O, Haytac MC, Ergin M, Antmen B, Seydaoglu G (2008) The immunohistochemical analysis of vascular endothelial growth factors A and C and microvessel density in gingival tissues of systemic sclerosis patients: Their possible effects on gingival inflammation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 105:481–485

    Article  PubMed  Google Scholar 

  30. Calderaro DC, Ferreira GA, Corrêa JD et al (2017) Is chronic periodontitis premature in systemic lupus erythematosus patients? Clin Rheumatol 36:713–718

    Article  PubMed  Google Scholar 

  31. Lo Giudice G, Lo Giudice R, Matarese G et al (2015) Evaluation of magnification systems in restorative dentistry. An in-vitro study. Dent Cadmos 83:296–305

    Article  Google Scholar 

  32. Pugliese C, van der Vinne RT, Campos LM et al (2016) Juvenile idiopathic arthritis activity and function ability: deleterious effects in periodontal disease? Clin Rheumatol 35:81–91

    Article  PubMed  Google Scholar 

  33. Becker MO, Riemekasten G (2016) Risk factors for severity and manifestations in systemic sclerosis and prediction of disease course. Expert Rev Clin Immunol 12:115–135

    Article  CAS  PubMed  Google Scholar 

  34. Cavuoti S, Matarese G, Isola G, Abdolreza J, Femiano F, Perillo L (2016) Combined orthodontic-surgical management of a transmigrated mandibular canine: a case report. Angle Orthod 86:681–691

    Article  PubMed  Google Scholar 

  35. Domsic RT, Rodriguez-Reyna T, Lucas M, Fertig N, Medsger TA Jr (2011) Skin thickness progression rate: a predictor of mortality and early internal organ involvement in diffuse scleroderma. Ann Rheum Dis 70:104–109

    Article  PubMed  Google Scholar 

  36. Arana-Ruiz JC, Silveira LH, Castillo-Martínez D, Amezcua-Guerra LM (2016) Assessment of nailfold capillaries with a handheld dermatoscope may discriminate the extent of organ involvement in patients with systemic sclerosis. Clin Rheumatol 35:479–482

    Article  PubMed  Google Scholar 

  37. Matarese G, Isola G, Anastasi GP et al (2017) Immunohistochemical analysis of TGF-β1 and VEGF in gingival and periodontal tissues: a role of these biomarkers in the pathogenesis of scleroderma and periodontal disease. Int J Mol Med 30:502–8. https:/doi.org/10.3892/ijmm.2012.1024

  38. Tzach-Nahman R, Nashef R, Fleissig O, Palmon A, Shapira L, Wilensky A, Nussbaum G (2017) Oral fibroblasts modulate the macrophage response to bacterial challenge. Scientific Reports 7:11516

Download references

Acknowledgements

This work was carried out with funding from Department of Biomedical, Odontostomatological Sciences and Morphological and Functional Images, University of Messina. The authors declare that they have no competing interest or other benefits from commercial sources for the work reported in the manuscript.

All authors were involved in drafting the article. G. Isola and G. Matarese have full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of data analysis.

Study conception and design: G. Isola, G. Matarese, L. Ramaglia.

Acquisition of data: G. Isola, C. Cosio.

Analysis and interpretation of data: G. Isola, M. Matarese, L. Ramaglia.

Critical revision and interpretation of data: G. Isola, A. Lo Gullo.

Author information

Authors and Affiliations

  1. Department of Biomedical, Odontostomatological Sciences and of Morphological and Functional Images, School of Dentistry, University of Messina, AOU Policlinico “G. Martino”, via C. Valeria, 98125, Messina, Italy

    Gaetano Isola, Marco Matarese, Claudio Cosio & Giovanni Matarese

  2. Department of Periodontology, UNC School of Dentistry, Campus Box #7450, Chapel Hill, NC, 27599-7450, USA

    Ray C. Williams

  3. Department of Clinical and Experimental Medicine, Section of internal medicine and rheumatology, University of Messina, AOU Policlinico “G. Martino”, via C. Valeria, 98125, Messina, Italy

    Alberto Lo Gullo

  4. Department of Neurosciences, Reproductive and Odontostomatological Sciences, School of Medicine, University of Naples “Federico II”, Via C. Pansini 5, 80100, Naples, Naples, Italy

    Luca Ramaglia & Vincenzo Iorio-Siciliano

Authors
  1. Gaetano Isola
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ray C. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alberto Lo Gullo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luca Ramaglia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marco Matarese
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vincenzo Iorio-Siciliano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Claudio Cosio
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Giovanni Matarese
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marco Matarese.

Ethics declarations

The study protocol was approved by the Ethical Committee of the University of Messina, Italy (#918-10), and a written informed consent was acquired by all patients who were informed about the characteristics of the study, by the Declaration of the World Medical Association 1975 in Helsinki, revised in 2000.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Isola, G., Williams, R.C., Lo Gullo, A. et al. Risk association between scleroderma disease characteristics, periodontitis, and tooth loss. Clin Rheumatol 36, 2733–2741 (2017). https://doi.org/10.1007/s10067-017-3861-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-017-3861-9

Keywords

Search

Navigation