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.
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References
Bartalena L, Tanda ML (2009) Clinical practice. N Engl J Med 360(10):994–1001. https://doi.org/10.1056/NEJMcp0806317
Bahn RS (2010) Graves’ ophthalmopathy. N Engl J Med 362(8):726–738. https://doi.org/10.1056/NEJMra0905750
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
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
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
(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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Clayton JA (2018) Dry eye. N Engl J Med 378(23):2212–2223. https://doi.org/10.1056/NEJMra1407936
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
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
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
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
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
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
Acknowledgements
We thank Wenjing Wu for her useful advice and critical review.
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This work was supported by the National Natural Science Foundation of China (Grant numbers. 81670884).
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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.
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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.
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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
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DOI: https://doi.org/10.1007/s40618-020-01322-5