International Ophthalmology

, Volume 39, Issue 10, pp 2187–2194 | Cite as

An assessment of ocular elasticity using real time ultrasound and ocular response analyzer in active or remission rheumatoid arthritis

  • Mehmet Erol CanEmail author
  • Özlem Unal
  • Meltem Ece Kars
  • Sukran Erten
  • Gamze Dereli Can
  • Necati Duru
  • Nurullah Cagil
Original Paper



To investigate the elasticity of ocular structures in patients with rheumatoid arthritis (RA) without ocular involvement.


The study included 56 RA patients (study group) and 24 healthy volunteers as the control group. The rheumatoid arthritis patients were divided into two subgroups as those in active phase (Group 1, n = 25) or in remission phase (Group 2, n = 31) according to the disease activity index (DAS 28) score. The elastography values of the ratio of orbital fat-sclera (ROF/S) were measured with real-time US elastography, and corneal mechanical values were measured with the Reichert Ocular Response Analyzer in each eye.


The mean ROF/S value was 5.2 ± 1.8 in Group 1, 0.7 ± 0.4 Group 2, and 0.6 ± 0.1 in the control group. There was a significant difference between the Group 1 and control group with regard to ROF/S (p < 0.001), but no significant difference was determined between Group 2 and control group (p > 0.05). The mean ROF/S value was a significant difference between the Group 1 and 2 (p < 0.001). ROF/S was significantly correlated with DAS-28 and C-reactive protein (CRP) (r = 0.816, p < 0.001 and r = 0.259, p = 0.006).


ROF/S was significantly increased in patients in the active phase of RA. Findings revealed that ocular tissue structural changes may occur in the active phase and these could be related to ocular complications as a prognostic factor.


Rheumatoid arthritis Ocular elasticity Ultrasound elastography DAS 28 


Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. 1.
    Grassi W, De Angelis R, Lamanna G, Cervini C (1998) The clinical features of rheumatoid arthritis. Eur J Radiol 27:18–24CrossRefGoogle Scholar
  2. 2.
    Scutellari PN, Orzincolo C (1998) Rheumatoid arthritis: sequences. Eur J Radiol 27:31–38CrossRefGoogle Scholar
  3. 3.
    Alamanos Y, Voulgari PV, Drosos AA (2006) Incidence and prevalence of rheumatoid arthritis, based on the 1987 American College of Rheumatology criteria: a systematic review. Semin Arthritis Rheum 36:182–188CrossRefGoogle Scholar
  4. 4.
    Huizinga TWJ, Pincus T (2010) In the clinic. Rheumatoid arthritis. Ann Intern Med 153:ITC1-1-ITC1-15; quiz ITC1-16CrossRefGoogle Scholar
  5. 5.
    Scott DL, Wolfe F, Huizinga TW (2010) Rheumatoid arthritis. Lancet 376:1094–1108CrossRefGoogle Scholar
  6. 6.
    Silman AJ, Pearson JE (2002) Epidemiology and genetics of rheumatoid arthritis. Arthritis Res 4:265–272CrossRefGoogle Scholar
  7. 7.
    Turesson C (2013) Extra-articular rheumatoid arthritis. Curr Opin Rheumatol 25:360–366CrossRefGoogle Scholar
  8. 8.
    Harper SL, Foster CS (1998) The ocular manifestations of rheumatoid disease. Int Ophthalmol Clin 38:1–19CrossRefGoogle Scholar
  9. 9.
    Vignesh APP, Srinivasan R (2015) Ocular manifestations of rheumatoid arthritis and their correlation with anti-cyclic citrullinated peptide antibodies. Clin Ophthalmol 9:393–397PubMedPubMedCentralGoogle Scholar
  10. 10.
    Lemp MA (2005) Dry eye (keratoconjunctivitis sicca), rheumatoid arthritis, and Sjögren’s syndrome. Am J Ophthalmol 140:898–899CrossRefGoogle Scholar
  11. 11.
    Artifoni M, Rothschild P-R, Brézin A et al (2014) Ocular inflammatory diseases associated with rheumatoid arthritis. Nat Rev Rheumatol 10:108–116CrossRefGoogle Scholar
  12. 12.
    Sigrist RMS, Liau J, El Kaffas A et al (2017) Ultrasound elastography: review of techniques and clinical applications. Theranostics 7:1303–1329CrossRefGoogle Scholar
  13. 13.
    Dewall RJ (2013) Ultrasound elastography: principles, techniques, and clinical applications. Crit Rev Biomed Eng 41:1–19CrossRefGoogle Scholar
  14. 14.
    Goekoop-Ruiterman YPM, de Vries-Bouwstra JK, Kerstens PJSM et al (2010) DAS-driven therapy versus routine care in patients with recent-onset active rheumatoid arthritis. Ann Rheum Dis 69:65–69CrossRefGoogle Scholar
  15. 15.
    Nayak BK, Hazra A (2011) How to choose the right statistical test? Indian J Ophthalmol 59:85–86CrossRefGoogle Scholar
  16. 16.
    Bacons PA, Kitas GD (1994) The significance of vascular inflammation in rheumatoid arthritis. Ann Rheum Dis 53:621–623CrossRefGoogle Scholar
  17. 17.
    Genta MS, Genta RM, Gabay C (2006) Systemic rheumatoid vasculitis: a review. Semin Arthritis Rheum 36:88–98CrossRefGoogle Scholar
  18. 18.
    Voskuyl AE, Zwinderman AH, Westedt ML et al (1996) Factors associated with the development of vasculitis in rheumatoid arthritis: results of a case-control study. Ann Rheum Dis 55:190–192CrossRefGoogle Scholar
  19. 19.
    Smolen JS, Steiner G (2003) Therapeutic strategies for rheumatoid arthritis. Nat Rev Drug Discov 2:473–488CrossRefGoogle Scholar
  20. 20.
    Smolen JS, Aletaha D, Koeller M et al (2007) New therapies for treatment of rheumatoid arthritis. Lancet (London) 370:1861–1874CrossRefGoogle Scholar
  21. 21.
    Choy E (2012) Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford) 51:3–11CrossRefGoogle Scholar
  22. 22.
    Cojocaru M, Cojocaru IM, Silosi I et al (2010) Extra-articular manifestations in rheumatoid arthritis. Maedica (Buchar) 5:286–291Google Scholar
  23. 23.
    Scott DG, Bacon PA, Tribe CR (1981) Systemic rheumatoid vasculitis: a clinical and laboratory study of 50 cases. Medicine (Baltimore) 60:288–297CrossRefGoogle Scholar
  24. 24.
    Rao NA, Marak GE, Hidayat AA (1985) Necrotizing scleritis. A clinico-pathologic study of 41 cases. Ophthalmology 92:1542–1549CrossRefGoogle Scholar
  25. 25.
    Androudi S, Dastiridou A, Symeonidis C et al (2013) Retinal vasculitis in rheumatic diseases: an unseen burden. Clin Rheumatol 32:7–13CrossRefGoogle Scholar
  26. 26.
    Duru N, Altinkaynak H, Erten Ş et al (2016) Thinning of choroidal thickness in patients with rheumatoid arthritis unrelated to disease activity. Ocul Immunol Inflamm 24:246–253CrossRefGoogle Scholar
  27. 27.
    Sims J (2012) Scleritis: presentations, disease associations and management. Postgrad Med J 88:713–718CrossRefGoogle Scholar
  28. 28.
    Jayson MI, Jones DE (1971) Scleritis and rheumatoid arthritis. Ann Rheum Dis 30:343–347CrossRefGoogle Scholar
  29. 29.
    Garra BS (2007) Imaging and estimation of tissue elasticity by ultrasound. Ultrasound Q 23:255–268CrossRefGoogle Scholar
  30. 30.
    Frey H (2003) Realtime elastography. A new ultrasound procedure for the reconstruction of tissue elasticity. Radiologe 43:850–855CrossRefGoogle Scholar
  31. 31.
    Luce DA (2005) Determining in vivo biomechanical properties of the cornea with an ocular response analyzer. J Cataract Refract Surg 31:156–162CrossRefGoogle Scholar
  32. 32.
    Taş M, Öner V, Özkaya E, Durmuş M (2014) Evaluation of corneal biomechanical properties in patients with rheumatoid arthritis: a study by ocular response analyzer. Ocul Immunol Inflamm 22:224–227CrossRefGoogle Scholar
  33. 33.
    Prata TS, Sousa AK, Garcia Filho CAA et al (2009) Assessment of corneal biomechanical properties and intraocular pressure in patients with rheumatoid arthritis. Can J Ophthalmol/J Can d’Ophtalmologie 44:602CrossRefGoogle Scholar
  34. 34.
    Can ME, Erten S, Can GD et al (2015) Corneal biomechanical properties in rheumatoid arthritis. Eye Contact Lens 41:382–385CrossRefGoogle Scholar
  35. 35.
    Detorakis ET, Drakonaki EE, Tsilimbaris MK et al (2010) Real-time ultrasound elastographic imaging of ocular and periocular tissues: a feasibility study. Ophthalmic Surg Lasers Imaging 41:135–141CrossRefGoogle Scholar
  36. 36.
    Pekel G, Ağladıoğlu K, Acer S et al (2015) Evaluation of ocular and periocular elasticity after panretinal photocoagulation: an ultrasonic elastography study. Curr Eye Res 40:332–337CrossRefGoogle Scholar
  37. 37.
    Unal O, Cay N, Yulek F et al (2016) Real-time ultrasound elastographic features of primary open angle glaucoma. Ultrasound Q 32:333–337CrossRefGoogle Scholar
  38. 38.
    Agladioglu K, Pekel G, Altintas Kasikci S et al (2016) An evaluation of ocular elasticity using real-time ultrasound elastography in primary open-angle glaucoma. Br J Radiol 89:20150429CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of OphthalmologyYuksek Ihtisas Training and Research HospitalBursaTurkey
  2. 2.Department of Radiology, Yildirim Beyazit University Faculty of MedicineAnkara Ataturk Training and Research HospitalAnkaraTurkey
  3. 3.Department of Ophthalmology, Yildirim Beyazit University Faculty of MedicineAnkara Ataturk Training and Research HospitalAnkaraTurkey
  4. 4.Department of Rheumatology, Yildirim Beyazit University Faculty of MedicineAnkara Ataturk Training and Research HospitalAnkaraTurkey
  5. 5.Department of OphthalmologyKayseri Training and Research HospitalKayseriTurkey

Personalised recommendations