Abstract
Purpose
To compare the macular choroidal thickness in patients with thyroid-associated ophthalmopathy (TAO) with those with normal tension glaucoma (NTG).
Methods
A total of 70 normal eyes, 74 eyes with TAO and 60 eyes with NTG were enrolled in this study. All patients underwent spectral-domain optical coherence tomography (SD-OCT) (Cirrus HD-OCT, Carl Zeiss Meditec Inc., Dublin, CA, USA). Macular choroidal thickness was assessed using enhanced depth imaging. The average macular choroidal thickness was defined as the average value of three measurements: at the fovea and at the points located 1.5 mm in the nasal and temporal directions from the fovea. Generalized estimating equations were used to uncover factors affecting the average macular choroidal thickness.
Results
The average, superior and inferior quadrant retinal nerve fiber layer thicknesses were significantly thinner in the NTG group compared with the TAO and control groups (p < 0.001). The average macular choroidal thickness of the TAO group, NTG group and controls was 281.01 ± 60.06 μ m, 241.66 ± 55.00 μ m and 252.07 ± 55.05 μ m, respectively, which were significantly dif-ferent (p = 0.013). The subfoveal, nasal and temporal side choroidal thicknesses were significantly thinner in the NTG group compared with the TAO group (p = 0.014, 0.012 and 0.034, respectively). Subjects with TAO were associated with a thicker aver-age macular choroidal thickness compared with the NTG group after adjusting for age, sex, spherical equivalent and intraocular pressure (β = 32.61, p = 0.017).
References
1. Stein JD, Childers D, Gupta S. . Risk factors for developing thyroid-associated ophthalmopathy among individuals with Graves disease. JAMA Ophthalmol. 2015; 133:290–6.
2. Çalış kan S, Acar M, Gürdal C. Choroidal thickness in patients with Graves' ophthalmopathy. Curr Eye Res. 2017; 42:484–90.
3. Asman P. Ophthalmological evaluation in thyroid-associated ophthalmopathy. Acta Ophthalmol Scand. 2003; 81:437–48.
4. Bartley GB. The epidemiologic characteristics and clinical course of ophthalmopathy associated with autoimmune thyroid disease in Olmsted County, Minnesota. Trans Am Ophthalmol Soc. 1994; 92:477–588.
5. Eckstein AK, Plicht M, Lax H. . Thyrotropin receptor autoanti-bodies are independent risk factors for Graves' ophthalmopathy and help to predict severity and outcome of the disease. J Clin Endocrinol Metab. 2006; 91:3464–70.
6. Bahn RS, Dutton CM, Natt N. . Thyrotropin receptor ex-pression in Graves' orbital adipose/connective tissues: potential autoantigen in Graves' ophthalmopathy. J Clin Endocrinol Metab. 1998; 83:998–1002.
7. Tripathy D, Rao A, Banerjee A, Padhy D. Aqueous misdirection in thyroid eye disease. BMJ Case Rep. 2014; 2014:pii: bcr2014205824.
9. Kim M, Kim TW, Park KH, Kim JM. Risk factors for primary open-angle glaucoma in South Korea: the Namil study. Jpn J Ophthalmol. 2012; 56:324–9.
10. Kalmann R, Mourits MP. Prevalence and management of elevated intraocular pressure in patients with Graves' orbitopathy. Br J Ophthalmol. 1998; 82:754–7.
11. Cockerham KP, Pal C, Jani B. . The prevalence and implications of ocular hypertension and glaucoma in thyroid-associated orbitopathy. Ophthalmology. 1997; 104:914–7.
12. Özkan B, Koçer ÇA, Altintaş Ö. . Choroidal changes observed with enhanced depth imaging optical coherence tomography in patients with mild Graves orbitopathy. Eye (Lond). 2016; 30:917–24.
13. Duijm HF, van den Berg TJ, Greve EL. Choroidal haemodynamics in glaucoma. Br J Ophthalmol. 1997; 81:735–42.
14. Hayreh SS. Blood supply of the optic nerve head and its role in op-tic atrophy, glaucoma, and oedema of the optic disc. Br J Ophthalmol. 1969; 53:721–48.
15. Yin ZQ, Vaegan Millar TJ. . Widespread choroidal in-sufficiency in primary open-angle glaucoma. J Glaucoma. 1997; 6:23–32.
16. Suh W, Cho HK, Kee C. Evaluation of peripapillary choroidal thickness in unilateral normal-tension glaucoma. Jpn J Ophthalmol. 2014; 58:62–7.
17. Ho J, Branchini L, Regatieri C. . Analysis of normal peripapil-lary choroidal thickness via spectral domain optical coherence tomography. Ophthalmology. 2011; 118:2001–7.
18. Jang SY, Lee SY, Lee EJ, Yoon JS. Clinical features of thy-roid-associated ophthalmopathy in clinically euthyroid Korean patients. Eye (Lond). 2012; 26:1263–9.
19. Kazuo K, Fujikado T, Ohmi G. . Value of thyroid stimulating antibody in the diagnosis of thyroid associated ophthalmopathy of euthyroid patients. Br J Ophthalmol. 1997; 81:1080–3.
20. Esporcatte BL, Tavares IM. Normal-tension glaucoma: an update. Arq Bras Oftalmol. 2016; 79:270–6.
21. Shields MB. Normal-tension glaucoma: is it different from pri-mary open-angle glaucoma? Curr Opin Ophthalmol. 2008; 19:85–8.
22. Mourits MP, Prummel MF, Wiersinga WM, Koornneef L. Clinical activity score as a guide in the management of patients with Graves' ophthalmopathy. Clin Endocrinol (Oxf). 1997; 47:9–14.
23. Kim JW, Woo YJ, Yoon JS. Is modified clinical activity score an accurate indicator of diplopia progression in Graves' orbitopathy patients? Endocr J. 2016; 63:1133–40.
24. Mwanza JC, Durbin MK, Budenz DL. . Profile and predictors of normal ganglion cell-inner plexiform layer thickness measured with frequency-domain optical coherence tomography. Invest Ophthalmol Vis Sci. 2011; 52:7872–9.
25. Spaide RF, Koizumi H, Pozzoni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol. 2008; 146:496–500.
26. Selbach JM, Posielek K, Steuhl KP, Kremmer S. Episcleral venous pressure in untreated primary open-angle and normal-tension glaucoma. Ophthalmologica. 2005; 219:357–61.
27. Shiau T, Armogan N, Yan DB. . The role of episcleral venous pressure in glaucoma associated with Sturge-Weber syndrome. J AAPOS. 2012; 16:61–4.
28. da Silva FL, de Lourdes Veronese Rodrigues M, Akaishi PM, Cruz AA. Graves' orbitopathy: frequency of ocular hypertension and glaucoma. Eye (Lond). 2009; 23:957–9.
29. Mrejen S, Spaide RF. Optical coherence tomography: imaging of the choroid and beyond. Surv Ophthalmol. 2013; 58:387–429.
30. Maul EA, Friedman DS, Chang DS. . Choroidal thickness measured by spectral domain optical coherence tomography: fac-tors affecting thickness in glaucoma patients. Ophthalmology. 2011; 118:1571–9.
31. Ersoz MG, Mart DK, Ayintap E. . The factors influencing peri-papillary choroidal thickness in primary open-angle glaucoma. Int Ophthalmol. 2016; Sep 12.:[Epub ahead of print].
32. Mwanza JC, Hochberg JT, Banitt MR. . Lack of association be-tween glaucoma and macular choroidal thickness measured with enhanced depth-imaging optical coherence tomography. Invest Ophthalmol Vis Sci. 2011; 52:3430–5.
33. Kanamori A, Nakamura M, Escano MF. . Evaluation of the glaucomatous damage on retinal nerve fiber layer thickness meas-ured by optical coherence tomography. Am J Ophthalmol. 2003; 135:513–20.
34. Mugdha K, Kaur A, Sinha N, Saxena S. Evaluation of retinal nerve fiber layer thickness profile in thyroid ophthalmopathy without op-tic nerve dysfunction. Int J Ophthalmol. 2016; 9:1634–7. eCollection 2016..
35. Sen E, Berker D, Elgin U. . Comparison of optic disc top-ography in the cases with graves disease and healthy controls. J Glaucoma. 2012; 21:586–9.
36. Park SC, Brumm J, Furlanetto RL. . Lamina cribrosa depth in different stages of glaucoma. Invest Ophthalmol Vis Sci. 2015; 56:2059–64.
37. Usui S, Ikuno Y, Miki A. . Evaluation of the choroidal thick-ness using high-penetration optical coherence tomography with long wavelength in highly myopic normal-tension glaucoma. Am J Ophthalmol. 2012; 153:10–6.e1.
38. Kim CS, Seong GJ, Lee NH. . Prevalence of primary open-angle glaucoma in central South Korea the Namil study. Ophthalmology. 2011; 118:1024–30.
Table 1.
Normal | TAO | NTG | p-value* | Post-hoc test | |
---|---|---|---|---|---|
Number of eyes (n) | 70 | 74 | 60 | ||
Age (years) | 51.4 ± 12.9 | 40.5 ± 18.6 | 54.7 ± 16.3 | <0.001* | <0.001‡/0.767§/<0.001Π |
SE (diopters) | -1.3 ± 2.8 | -1.7 ± 1.9 | -1.8 ± 4.2 | 0.686* | |
Phakic eye (n, %) | 100.0 | 97.3 | 100.0 | 0.119† | |
Baseline IOP (mmHg) | 14.9 ± 3.8 | 17.6 ± 4.5 | 16.2 ± 2.5 | <0.001* | <0.001‡/0.019§/0.113Π |
Treated IOP (mmHg) | 14.9 ± 3.8 | 16.1 ± 4.3 | 12.4 ± 2.6 | <0.001* | 0.009‡/0.004§/<0.001Π |
Number of anti-glaucoma medications (n) | 0.0 ± 0.0 | 0.5 ± 0.6 | 1.3 ± 0.5 | <0.001* | <0.001‡/<0.001§/<0.001Π |
History of diabetes (%) | 20.7 | 11.5 | 24.0 | 0.244† | |
History of hypertension (%) | 26.9 | 20.0 | 24.0 | 0.712† |
Table 2.
Location | Normal | TAO | NTG | p-value* | Post-hoc test |
---|---|---|---|---|---|
Average RNFL thickness (μ m) | 94.4 ± 9.9 | 94.1 ± 13.0 | 80.3 ± 11.3 | <0.001 | 0.900†/<0.001‡/<0.001§ |
Superior quadrant (μ m) | 115.7 ± 15.1 | 115.9 ± 21.6 | 100.2 ± 18.2 | <0.001 | 0.900†/<0.001‡/<0.001§ |
Inferior quadrant (μ m) | 120.9 ± 15.1 | 119.8 ± 21.5 | 90.0 ± 24.7 | <0.001 | 0.900†/<0.001‡/<0.001§ |
Temporal quadrant (μ m) | 74.9 ± 14.2 | 73.3 ± 12.2 | 67.7 ± 12.0 | 0.006 | 0.900†/<0.001‡/0.007§ |
Nasal quadrant (μ m) | 66.2 ± 11.9 | 67.5 ± 12.0 | 63.4 ± 10.1 | 0.124 | 0.900†/<0.001‡/0.498§ |
Table 3.
Location | Normal | TAO | NTG | p-value |
---|---|---|---|---|
Average macular choroidal thickness (μ m) | 252.07 ± 55.05 | 281.01 ± 60.06 | 241.66 ± 55.00 | 0.013*/0.022†/0.426‡/0.004§ |
Nasal side macular choroidal thickness (μ m) | 244.56 ± 61.30 | 269.50 ± 65.93 | 233.40 ± 50.37 | 0.040*/0.068†/0.381‡/0.012§ |
Subfoveal choroidal thickness (μ m) | 257.01 ± 60.38 | 288.25 ± 64.93 | 245.94 ± 65.17 | 0.014*/0.076†/0.900‡/0.014§ |
Temporal side macular choroidal thickness (μ m) | 253.44 ± 58.72 | 285.29 ± 59.34 | 245.61 ± 68.28 | 0.028*/0.083†/0.900‡/0.034§ |
Table 4.
Univariate | Multivariate | |||||
---|---|---|---|---|---|---|
Regression coefficient (95% CI) | Standard error | p-value | Regression coefficient (95% CI) | Standard error | p-value | |
Group* | ||||||
TAO | 38.72 (11.38, 66.05) | 13.94 | 0.006 | 32.61 (5.93, 59.29) | 13.61 | 0.017 |
Normal | 9.50 (-13.72, 32.72) | 11.84 | 0.423 | 7.56 (-16.21, 31.32) | 12.13 | 0.533 |
NTG | 1 | |||||
Age | -0.78 (-1.55, -0.02) | -0.39 | 0.046 | -0.57 (-1.28, 0.15) | 0.37 | 0.123 |
Sex | -9.57 (-32.00, 12.85) | 1.44 | 0.403 | |||
SE | -0.20 (-3.500, -3.11) | 1.67 | 0.908 | |||
Treated IOP | -0.253 (-2.75, 2.24) | 1.28 | 0.843 |