Skip to main content

Advertisement

SpringerLink
Log in

A multimodal ophthalmic analysis in patients with systemic sclerosis using ocular response analyzer, corneal topography and specular microscopy

  • Original Paper
  • Published:
International Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

To conduct a multimodal ophthalmic evaluation of systemic sclerosis (SSc) in patients using ocular response analyzer (ORA), Pentacam, and specular microscopy (SM).

Methods

Thirty-one SSc patients and a group of age- and sex-matched controls were enrolled in this cross-sectional study. Corneal hysteresis (CH), corneal resistance factor (CRF), corneal-compensated intraocular pressure (IOPcc), and Goldmann-correlated IOP (IOPg) were measured with ORA. Anterior chamber depth (ACD), central corneal thickness (CCT), and corneal volume (CV) measurements were obtained using Pentacam. Corneal endothelial cell density (ECD) and CCT were evaluated by SM.

Results

SSc patients had significantly lower CH, ACD, and ECD values compared to the control group (p = 0.018; < 0.001; < 0.001, respectively). There was no significant difference regarding CRF, IOP, CV, or CCT measurements acquired by Pentacam and SM. Regarding CCT, SM and Pentacam showed relatively better agreement in SSc patients.

Conclusions

Multimodal imaging can provide more comprehensive and useful information regarding the ocular involvement of systemic diseases. The multimodal evaluation in our study demonstrated that the pathologic effects of SSc may manifest as reductions in ACD, corneal elasticity, and ECD before there are any detectable changes in corneal thickness or IOP.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Chifflot H, Fautrel B, Sordet C et al (2008) Incidence and prevalence of systemic sclerosis: a systematic literature review. Semin Arthritis Rheum 37:223–235. https://doi.org/10.1016/j.semarthrit.2007.05.003

    Article  PubMed  Google Scholar 

  2. Martin P, Teodoro WR, Velosa APP et al (2012) Abnormal collagen V deposition in dermis correlates with skin thickening and disease activity in systemic sclerosis. Autoimmun Rev 11:827–835. https://doi.org/10.1016/j.autrev.2012.02.017

    Article  CAS  PubMed  Google Scholar 

  3. Derk CT, Jimenez SA (2003) Systemic sclerosis: current views of its pathogenesis. Autoimmun Rev 2:181–191. https://doi.org/10.1016/S1568-9972(03)00005-3

    Article  CAS  PubMed  Google Scholar 

  4. Tailor R, Gupta A, Herrick A, Kwartz J (2009) Ocular manifestations of scleroderma. Surv Ophthalmol 54:292–304. https://doi.org/10.1016/j.survophthal.2008.12.007

    Article  PubMed  Google Scholar 

  5. Sii F, Lee GA, Sanfilippo P, Stephensen DC (2004) Pellucid marginal degeneration and scleroderma. Clin Exp Optom 87:180–184

    Article  Google Scholar 

  6. Shah S, Laiquzzaman M, Cunliffe I, Mantry S (2006) The use of the Reichert ocular response analyser to establish the relationship between ocular hysteresis, corneal resistance factor and central corneal thickness in normal eyes. Contact Lens Anterior Eye 29:257–262. https://doi.org/10.1016/j.clae.2006.09.006

    Article  PubMed  Google Scholar 

  7. Rio-Cristobal A, Martin R (2014) Corneal assessment technologies: current status. Surv Ophthalmol 59:599–614. https://doi.org/10.1016/j.survophthal.2014.05.001

    Article  PubMed  Google Scholar 

  8. Karaca I, Yilmaz SG, Palamar M, Ates H (2017) Comparison of central corneal thickness and endothelial cell measurements by Scheimpflug camera system and two noncontact specular microscopes. Int Ophthalmol. https://doi.org/10.1007/s10792-017-0630-3

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  10. Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310

    Article  CAS  Google Scholar 

  11. Ihanamäki T, Pelliniemi LJ, Vuorio E (2004) Collagens and collagen-related matrix components in the human and mouse eye. Prog Retin Eye Res 23:403–434. https://doi.org/10.1016/j.preteyeres.2004.04.002

    Article  CAS  PubMed  Google Scholar 

  12. Gezer A, Tuncer S, Canturk S et al (2005) Bilateral acquired brown syndrome in systemic scleroderma. J Am Assoc Pediatr Ophthalmol Strabismus 9:195–197. https://doi.org/10.1016/j.jaapos.2004.11.019

    Article  Google Scholar 

  13. Konuk O, Ozdek S, Onal B et al (2006) Ocular ischemic syndrome presenting as central retinal artery occlusion in scleroderma. Retina 26:102–104

    Article  Google Scholar 

  14. Ushiyama O, Ushiyama K, Yamada T et al (2003) Retinal findings in systemic sclerosis: a comparison with nailfold capillaroscopic patterns. Ann Rheum Dis 62:204–207. https://doi.org/10.1136/ARD.62.3.204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Allanore Y, Parc C, Monnet D et al (2004) Increased prevalence of ocular glaucomatous abnormalities in systemic sclerosis. Ann Rheum Dis 63:1276–1278. https://doi.org/10.1136/ard.2003.013540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Müller LJ, Pels E, Vrensen GF (2001) The specific architecture of the anterior stroma accounts for maintenance of corneal curvature. Br J Ophthalmol 85:437–443. https://doi.org/10.1136/BJO.85.4.437

    Article  PubMed  PubMed Central  Google Scholar 

  17. Dayanir V, Sakarya R, Ozcura F et al (2004) Effect of corneal drying on central corneal thickness. J Glaucoma 13:6–8

    Article  Google Scholar 

  18. Liu J, Roberts CJ (2005) Influence of corneal biomechanical properties on intraocular pressure measurement. J Cataract Refract Surg 31:146–155. https://doi.org/10.1016/j.jcrs.2004.09.031

    Article  PubMed  Google Scholar 

  19. Whitacre MM, Stein R (1993) Sources of error with use of Goldmann-type tonometers. Surv Ophthalmol 38:1–30

    Article  CAS  Google Scholar 

  20. Pepose JS, Feigenbaum SK, Qazi MA et al (2007) Changes in corneal biomechanics and intraocular pressure following LASIK using static, dynamic, and noncontact tonometry. Am J Ophthalmol 143:39–47. https://doi.org/10.1016/j.ajo.2006.09.036

    Article  PubMed  Google Scholar 

  21. Medeiros FA, Weinreb RN (2006) Evaluation of the influence of corneal biomechanical properties on intraocular pressure measurements using the ocular response analyzer. J Glaucoma 15:364–370. https://doi.org/10.1097/01.ijg.0000212268.42606.97

    Article  PubMed  Google Scholar 

  22. Deol M, Taylor DA, Radcliffe NM (2015) Corneal hysteresis and its relevance to glaucoma. Curr Opin Ophthalmol 26:96–102. https://doi.org/10.1097/ICU.0000000000000130

    Article  PubMed  PubMed Central  Google Scholar 

  23. Emre S, Kaykçoğlu Ö, Ateş H et al (2010) Corneal hysteresis, corneal resistance factor, and intraocular pressure measurement in patients with scleroderma using the reichert ocular response analyzer. Cornea 29:628–631. https://doi.org/10.1097/ICO.0b013e3181c3306a

    Article  PubMed  Google Scholar 

  24. Palamar M, Karatepe AS, Eğrilmez S, Yağcı A (2011) Evaluation of cornea and anterior chamber with pentacam in scleroderma cases. Turk J Ophthalmol 41:221–224. https://doi.org/10.4274/tjo.41.63825

    Article  Google Scholar 

  25. Sahin Atik S, Koc F, Akin Sari S et al (2016) Anterior segment parameters and eyelids in systemic sclerosis. Int Ophthalmol 36:577–583. https://doi.org/10.1007/s10792-015-0165-4

    Article  PubMed  Google Scholar 

  26. Yorio T, Krishnamoorthy R, Prasanna G (2002) Endothelin: is it a contributor to glaucoma pathophysiology? J Glaucoma 11:259–270

    Article  Google Scholar 

  27. Gaspar R, Pinto LA, Sousa DC (2017) Corneal properties and glaucoma: a review of the literature and meta-analysis. Arq Bras Oftalmol 80:202–206. https://doi.org/10.5935/0004-2749.20170050

    Article  PubMed  Google Scholar 

  28. Gomes BAF, Santhiago MR, Magalhães P et al (2011) Ocular findings in patients with systemic sclerosis. Clinics (Sao Paulo) 66:379–385. https://doi.org/10.1590/S1807-59322011000300003

    Article  Google Scholar 

  29. Yamamoto T, Maeda M, Sawada A et al (1999) Prevalence of normal-tension glaucoma and primary open-angle glaucoma in patients with collagen diseases. Jpn J Ophthalmol 43:539–542

    Article  CAS  Google Scholar 

  30. Kitsos G, Tsifetaki N, Gorezis S, Drosos AA (2007) Glaucomatous type abnormalities in patients with systemic sclerosis. Clin Exp Rheumatol 25:341

    CAS  PubMed  Google Scholar 

  31. Gomes BDAF, Santhiago MR, Kara-Junior N et al (2011) Central corneal thickness in patients with systemic sclerosis: a controlled study. Cornea 30:1125–1128. https://doi.org/10.1097/ICO.0b013e318206cac1

    Article  Google Scholar 

  32. Gomes BAF, Santhiago MR, Kara-Junior N et al (2016) Assessment of central corneal thickness in different subtypes of systemic sclerosis. Ocul Immunol Inflamm 24:693–698. https://doi.org/10.3109/09273948.2015.1076008

    Article  CAS  PubMed  Google Scholar 

  33. Gomes BF, Santhiago MR, Kara-Junior N, Moraes HV (2018) Evaluation of corneal parameters with dual Scheimpflug imaging in patients with systemic sclerosis. Curr Eye Res 43:451–454. https://doi.org/10.1080/02713683.2017.1414855

    Article  PubMed  Google Scholar 

  34. Serup L, Serup J, Hagdrup HK (1984) Increased central cornea thickness in systemic sclerosis. Acta Ophthalmol 62:69–74

    Article  CAS  Google Scholar 

  35. Nagy A, Rentka A, Nemeth G et al (2018) Corneal manifestations of systemic sclerosis. Ocul Immunol Inflamm 00:1–10. https://doi.org/10.1080/09273948.2018.1489556

    Article  Google Scholar 

  36. Şahin M, Yüksel H, Şahin A et al (2017) Evaluation of the anterior segment parameters of the patients with scleroderma. Ocul Immunol Inflamm 25:233–238. https://doi.org/10.3109/09273948.2015.1115079

    Article  PubMed  Google Scholar 

  37. Kim W-U, Min S-Y, Cho M-L et al (2005) Elevated matrix metalloproteinase-9 in patients with systemic sclerosis. Arthritis Res Ther 7:71–79. https://doi.org/10.1186/ar1454

    Article  CAS  Google Scholar 

  38. Chizzolini C, Parel Y, De Luca C et al (2003) Systemic sclerosis Th2 cells inhibit collagen production by dermal fibroblasts via membrane-associated tumor necrosis factor α. Arthritis Rheum 48:2593–2604. https://doi.org/10.1002/art.11129

    Article  CAS  PubMed  Google Scholar 

  39. Tai L, Khaw K, Ng C (2013) Central corneal thickness measurements with different imaging devices and ultrasound pachymetry. Cornea 32:766–771

    Article  Google Scholar 

  40. González-Pérez J, González-Méijome JM, Rodríguez Ares MT, Parafita MÁ (2011) Central corneal thickness measured with three optical devices and ultrasound pachometry. Eye Contact Lens Sci Clin Pract 37:66–70. https://doi.org/10.1097/ICL.0b013e31820c6ffc

    Article  Google Scholar 

  41. Fujioka M, Nakamura M, Tatsumi Y et al (2007) Comparison of Pentacam Scheimpflug camera with ultrasound pachymetry and noncontact specular microscopy in measuring central corneal thickness. Curr Eye Res 32:89–94. https://doi.org/10.1080/02713680601115010

    Article  PubMed  Google Scholar 

  42. Scotto R, Bagnis A, Papadia M et al (2017) Comparison of central corneal thickness measurements using ultrasonic pachymetry, anterior segment OCT and noncontact specular microscopy. J Glaucoma 26:860–865. https://doi.org/10.1097/IJG.0000000000000745

    Article  PubMed  Google Scholar 

  43. Módis L, Langenbucher A, Seitz B (2002) Corneal endothelial cell density and pachymetry measured by contact and noncontact specular microscopy. J Cataract Refract Surg 28:1763–1769. https://doi.org/10.1016/S0886-3350(02)01296-8

    Article  PubMed  Google Scholar 

  44. Gomes BF, Santhiago MR, Gomes SF et al (2016) Longitudinal evaluation of central corneal thickness in patients with systemic sclerosis. Cornea 35:1584–1588. https://doi.org/10.1097/ICO.0000000000000950

    Article  PubMed  Google Scholar 

  45. Waring GO, Bourne WM, Edelhauser HF, Kenyon KR (1982) The corneal endothelium. Normal and pathologic structure and function. Ophthalmology 89:531–590

    Article  Google Scholar 

Download references

Funding

No funding was secured for this study.

Author information

Authors and Affiliations

  1. Ophthalmology Department, Medical School, Manisa Celal Bayar University, Manisa, Turkey

    Huseyin Mayali, Muhammed Altinisik, Timur Pirildar & Emin Kurt

  2. Ophthalmology Department, Tinaztepe Hospital, Izmir, Turkey

    Secil Sencan

Authors
  1. Huseyin Mayali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muhammed Altinisik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Secil Sencan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Timur Pirildar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Emin Kurt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muhammed Altinisik.

Ethics declarations

Conflict of interest

None of the authors has any potential financial conflict of interest related to this manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mayali, H., Altinisik, M., Sencan, S. et al. A multimodal ophthalmic analysis in patients with systemic sclerosis using ocular response analyzer, corneal topography and specular microscopy. Int Ophthalmol 40, 287–296 (2020). https://doi.org/10.1007/s10792-019-01173-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10792-019-01173-x

Keywords

Search

Navigation