Skip to main content

Advertisement

Log in

Changes in ocular biomechanics after treatment for active Graves’ orbitopathy

  • Original Article
  • Published:
Journal of Endocrinological Investigation Aims and scope Submit manuscript

Abstract

Purpose

To evaluate the changes in ocular biomechanical properties in active moderate-to-severe Graves’ orbitopathy (GO) after intravenous glucocorticoids (IVGCs), and to clarify correlations between clinical findings and ocular biomechanical properties.

Methods

A prospective study. A total of 20 consecutive GO patients and 20 age- and sex-matched healthy control subjects were included. GO was diagnosed on the basis of the recommendation by the European Group on Graves’ Orbitopathy (EUGOGO), and disease activity was assessed by the clinical activity score (CAS). Patients were assigned to receive once weekly IVGCs (0.5 g, then 0.25 g, 6 weeks each). All participants received a full ophthalmic examination and biomechanical evaluation was performed with dynamic Scheimpflug analyzer (Corvis ST) at baseline and 12th weeks after therapy.

Results

The biomechanically corrected intraocular pressure (bIOP) in GO patients was significantly higher than that in healthy subjects. In contrast, the whole eye movement (WEM) in GO patients was significantly lower than in healthy subjects after adjusting for bIOP. The CAS, NOSPECS score, and exophthalmos were significantly positively correlated with the bIOP and negatively correlated with the WEM after adjusting for bIOP, CCT and age. The WEM significantly increased, whereas bIOP significantly decreased after IVGCs (P < 0.001, P = 0.001 respectively). The overall response rate at the 12th week was 85% (17 of 20).

Conclusions

The changes of ocular biomechanical properties measured by Corvis ST were an objective indicator of inflammatory activity and severity of GO. Combining CAS and ocular biomechanical properties could better evaluate the therapeutic outcome of active moderate-to-severe GO.

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

Access this article

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. Bartalena L, Tanda ML (2009) Clinical practice. N Engl J Med 360(10):994–1001. https://doi.org/10.1056/NEJMcp0806317

    Article  CAS  PubMed  Google Scholar 

  2. Bahn RS (2010) Graves’ ophthalmopathy. N Engl J Med 362(8):726–738. https://doi.org/10.1056/NEJMra0905750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Wong LL, Lee NG, Amarnani D, Choi CJ, Bielenberg DR, Freitag SK, D'Amore PA, Kim LA (2016) Orbital angiogenesis and lymphangiogenesis in thyroid eye disease: an analysis of vascular growth factors with clinical correlation. Ophthalmology 123(9):2028–2036. https://doi.org/10.1016/j.ophtha.2016.05.052

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mourits MP, Prummel MF, Wiersinga WM, Koornneef L (1997) Clinical activity score as a guide in the management of patients with Graves’ ophthalmopathy. Clin Endocrinol (Oxf) 47(1):9–14. https://doi.org/10.1046/j.1365-2265.1997.2331047.x

    Article  CAS  Google Scholar 

  5. Prabhakar BS, Bahn RS, Smith TJ (2003) Current perspective on the pathogenesis of Graves' disease and ophthalmopathy. Endocr Rev 24(6):802–835. https://doi.org/10.1210/er.2002-0020

    Article  CAS  PubMed  Google Scholar 

  6. (1955) CORTISONE in exophthalmos: report on a therapeutic trial of cortisone and corticotrophin (A.C.T.H.) in exophthalmos and exophthalmic ophthalmoplegia by a panel appointed by the Medical Research Council. Lancet 268 (6853):6–9

  7. Wiersinga WM (2017) Advances in treatment of active, moderate-to-severe Graves’ ophthalmopathy. Lancet Diabetes Endocrinol 5(2):134–142. https://doi.org/10.1016/S2213-8587(16)30046-8

    Article  CAS  PubMed  Google Scholar 

  8. Strianese D (2017) Update on Graves disease: advances in treatment of mild, moderate and severe thyroid eye disease. Curr Opin Ophthalmol 28(5):505–513. https://doi.org/10.1097/ICU.0000000000000402

    Article  PubMed  Google Scholar 

  9. Bartalena L, Baldeschi L (2016) The 2016 European thyroid association/european group on Graves’ orbitopathy guidelines for the management of Graves’ orbitopathy. Eur Thyroid J 5(1):9–26. https://doi.org/10.1159/000443828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Hon Y, Lam AK (2013) Corneal deformation measurement using Scheimpflug noncontact tonometry. Optom Vis Sci 90(1):e1–8. https://doi.org/10.1097/OPX.0b013e318279eb87

    Article  PubMed  Google Scholar 

  11. Moghimi S, Safizadeh M, Mazloumi M, Hosseini H, Vahedian Z, Rajabi MT (2016) Evaluation of corneal biomechanical properties in patients with thyroid eye disease using ocular response analyzer. J Glaucoma 25(3):269–273. https://doi.org/10.1097/IJG.0000000000000254

    Article  PubMed  Google Scholar 

  12. Vellara HR, Hart R, Gokul A, McGhee CNJ, Patel DV (2017) In vivo ocular biomechanical compliance in thyroid eye disease. Br J Ophthalmol 101(8):1076–1079. https://doi.org/10.1136/bjophthalmol-2016-309532

    Article  PubMed  Google Scholar 

  13. Leszczynska A, Moehler K, Spoerl E, Ramm L, Herber R, Pillunat LE, Terai N (2018) Measurement of orbital biomechanical properties in patients with thyroid orbitopathy using the dynamic scheimpflug analyzer (Corvis ST). Curr Eye Res 43(3):289–292. https://doi.org/10.1080/02713683.2017.1405044

    Article  PubMed  Google Scholar 

  14. Profilo MA, Sisti E, Marcocci C, Vitti P, Pinchera A, Nardi M, Rocchi R, Latrofa F, Menconi F, Altea MA, Leo M, Rago T, Marino M (2013) Thyroid volume and severity of Graves’ orbitopathy. Thyroid 23(1):97–102. https://doi.org/10.1089/thy.2012.0379

    Article  PubMed  Google Scholar 

  15. Zhu W, Ye L, Shen L, Jiao Q, Huang F, Han R, Zhang X, Wang S, Wang W, Ning G (2014) A prospective, randomized trial of intravenous glucocorticoids therapy with different protocols for patients with Graves’ ophthalmopathy. J Clin Endocrinol Metab 99(6):1999–2007. https://doi.org/10.1210/jc.2013-3919

    Article  CAS  PubMed  Google Scholar 

  16. Fernandez J, Rodriguez-Vallejo M, Martinez J, Tauste A, Salvestrini P, Pinero DP (2017) New parameters for evaluating corneal biomechanics and intraocular pressure after small-incision lenticule extraction by Scheimpflug-based dynamic tonometry. J Cataract Refract Surg 43(6):803–811. https://doi.org/10.1016/j.jcrs.2017.03.035

    Article  PubMed  Google Scholar 

  17. Miki A, Maeda N, Ikuno Y, Asai T, Hara C, Nishida K (2017) Factors associated with corneal deformation responses measured with a dynamic scheimpflug analyzer. Invest Ophthalmol Vis Sci 58(1):538–544. https://doi.org/10.1167/iovs.16-21045

    Article  PubMed  Google Scholar 

  18. Yuksel N, Kars ME (2017) Evaluation of corneal biomechanical properties in patients with thyroid eye disease using an ocular response analyzer. J Glaucoma 26(2):e121. https://doi.org/10.1097/IJG.0000000000000476

    Article  PubMed  Google Scholar 

  19. Lee H, Roberts CJ, Kim TI, Ambrosio R Jr, Elsheikh A, Yong Kang DS (2017) Changes in biomechanically corrected intraocular pressure and dynamic corneal response parameters before and after transepithelial photorefractive keratectomy and femtosecond laser-assisted laser in situ keratomileusis. J Cataract Refract Surg 43(12):1495–1503. https://doi.org/10.1016/j.jcrs.2017.08.019

    Article  PubMed  Google Scholar 

  20. Danesh-Meyer HV, Savino PJ, Deramo V, Sergott RC, Smith AF (2001) Intraocular pressure changes after treatment for Graves’ orbitopathy. Ophthalmology 108(1):145–150. https://doi.org/10.1016/s0161-6420(00)00477-2

    Article  CAS  PubMed  Google Scholar 

  21. Onaran Z, Konuk O, Oktar SO, Yucel C, Unal M (2014) Intraocular pressure lowering effect of orbital decompression is related to increased venous outflow in Graves orbitopathy. Curr Eye Res 39(7):666–672. https://doi.org/10.3109/02713683.2013.867355

    Article  PubMed  Google Scholar 

  22. Sit AJ, McLaren JW (2011) Measurement of episcleral venous pressure. Exp Eye Res 93(3):291–298. https://doi.org/10.1016/j.exer.2011.05.003

    Article  CAS  PubMed  Google Scholar 

  23. Vinciguerra R, Elsheikh A, Roberts CJ, Ambrosio R Jr, Kang DS, Lopes BT, Morenghi E, Azzolini C, Vinciguerra P (2016) Influence of pachymetry and intraocular pressure on dynamic corneal response parameters in healthy patients. J Refract Surg 32(8):550–561. https://doi.org/10.3928/1081597X-20160524-01

    Article  PubMed  Google Scholar 

  24. Roberts CJ (2014) Concepts and misconceptions in corneal biomechanics. J Cataract Refract Surg 40(6):862–869. https://doi.org/10.1016/j.jcrs.2014.04.019

    Article  PubMed  Google Scholar 

  25. Kashkouli MB, Alemzadeh SA, Aghaei H, Pakdel F, Abdolalizadeh P, Ghazizadeh M, Moradpasandi F (2018) Subjective versus objective dry eye disease in patients with moderate-severe thyroid eye disease. Ocul Surf 16(4):458–462. https://doi.org/10.1016/j.jtos.2018.07.003

    Article  PubMed  Google Scholar 

  26. Clayton JA (2018) Dry eye. N Engl J Med 378(23):2212–2223. https://doi.org/10.1056/NEJMra1407936

    Article  CAS  PubMed  Google Scholar 

  27. Ma J, Wang Y, Wei P, Jhanji V (2018) Biomechanics and structure of the cornea: implications and association with corneal disorders. Surv Ophthalmol 63(6):851–861. https://doi.org/10.1016/j.survophthal.2018.05.004

    Article  PubMed  Google Scholar 

  28. Lombardo M, Lombardo G, Carbone G, De Santo MP, Barberi R, Serrao S (2012) Biomechanics of the anterior human corneal tissue investigated with atomic force microscopy. Invest Ophthalmol Vis Sci 53(2):1050–1057. https://doi.org/10.1167/iovs.11-8720

    Article  PubMed  Google Scholar 

  29. Villani E, Galimberti D, Viola F, Mapelli C, Ratiglia R (2007) The cornea in Sjogren’s syndrome: an in vivo confocal study. Invest Ophthalmol Vis Sci 48(5):2017–2022. https://doi.org/10.1167/iovs.06-1129

    Article  PubMed  Google Scholar 

  30. Ismailova DS, Fedorov AA, Grusha YO (2013) Ocular surface changes in thyroid eye disease. Orbit 32(2):87–90. https://doi.org/10.3109/01676830.2013.764440

    Article  PubMed  Google Scholar 

  31. Xu N, Cui Y, Fu D, Sun F (2020) Tear inflammatory cytokines and ocular surface changes in patients with active thyroid eye disease treated with high-dose intravenous glucocorticoids. J Endocrinol Invest. https://doi.org/10.1007/s40618-019-01174-8

    Article  PubMed  Google Scholar 

  32. Kahaly GJ, Pitz S, Hommel G, Dittmar M (2005) Randomized, single blind trial of intravenous versus oral steroid monotherapy in Graves’ orbitopathy. J Clin Endocrinol Metab 90(9):5234–5240. https://doi.org/10.1210/jc.2005-0148

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Wenjing Wu for her useful advice and critical review.

Funding

This work was supported by the National Natural Science Foundation of China (Grant numbers. 81670884).

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: HXL, YP, and XHZ; Methodology: HXL, HZ, and XHZ; Formal analysis and investigation: HXL, XHZ, and BKM; Writing-original draft preparation: HXL; Writing-review and editing: HXL, YS, XHZ, and YW; Funding acquisition: YW; Resources: HXL and YW; Supervision: YW.

Corresponding author

Correspondence to Y. Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of Tianjin Eye Hospital and Tianjin Medical University 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.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, H.X., Zhao, X.H., Song, Y. et al. Changes in ocular biomechanics after treatment for active Graves’ orbitopathy. J Endocrinol Invest 44, 453–458 (2021). https://doi.org/10.1007/s40618-020-01322-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40618-020-01322-5

Keywords

Navigation