Evaluation of Henle Nerve Fiber Layer by Optical Coherence Tomography in Thyroid Eye Disease

Öz

Aim: The aim of this study was to evaluate the Henle's nerve fiber layer (HNFL) consisting of photoreceptors and Müller cells in individuals with Thyroid Eye Disease (TED) using optical coherence tomography (OCT) and to compare it with healthy individuals. Material and Methods: Twenty eyes of 20 patients with inactive mild TED (Group-1) and 20 eyes of 20 age- and gender-matched healthy participants (Group-2) were retrospectively included in the study. Detailed ocular examination findings of all participants were recorded. Retinal thickness obtained by OCT and central 500 and 1000 μm wide HNFL area, measured by ImageJ software, were recorded. The findings were statistically compared between the two groups. Results: There was no significant difference in mean age and gender distribution between the groups (p>0.05). Mean best corrected visual acuity, intraocular pressure, spherical equivalent, axial length and anterior chamber depth were similar between the two groups (p>0.05 for all). Retinal thickness and choroidal thickness were not significantly different between the two groups (p>0.05). The mean HNFL area in the central 500 μm region was significantly higher in group-1 than in group-2 (Group-1: 25678,4 ± 5372,0 μm2 vs. group-2: 23375,0 ± 3974,5 μm2, p=0.010). In the central 1000 μm region, the mean HSLT areas were similar between the two groups (Group-1: 99859,9 ± 9936,4 μm2 vs group-2: 97563,0 ± 8478,4 μm2, p=0.090). Conclusion: The findings of our study show an increased HNFL area consisting of photoreceptors and Müller cells in the central foveal region in eyes with mild and inactive TED. Evaluation of HNFL may be promising for early detection and follow-up of TED

Anahtar Kelimeler

• Henle
• Müller cell
• photoreceptor cell
• thyroid eye disease

Tiroid Göz Hastalığında Henle Sinir Lifi Tabakasının Optik Koherens Tomografi ile Değerlendirilmesi

Öz

Amaç: Tiroid Göz Hastalığı (TGH) olan bireylerde, fotoreseptör ve Müller hücrelerinden oluşan Henle sinir lifi tabakasının (HSLT) optik koherens tomografi (OKT) ile değerlendirilerek sağlıklı bireylerde kıyaslanması amaçlanmıştır. Gereç ve Yöntemler: İnaktif hafif seviyede TGH olan 20 hastanın 20 gözü (Grup-1) ile yaş ve cinsiyet uyumlu 20 sağlıklı katılımcının 20 gözü (Grup-2) retrospektif olarak çalışmaya dahil edildi. Tüm katılımcıların detaylı göz muayene bulguları kaydedildi. OKT ile elde edilen retinal kalınlıkları ve ImageJ programı yardımıyla ölçülen santral 500 ve 1000 μm genişlikteki HSLT alanı ölçülerek kaydedildi. Bulgular iki grup arasında istatistiksel olarak kıyaslandı. Bulgular: Gruplar arasında ortalama yaş ve cinsiyet dağılımı açısından anlamlı fark saptanmadı (p>0,05). En iyi düzeltilmiş görme keskinliği, göz içi basıncı, sferik eşdeğer, aksiyel uzunluk ve ön kamara derinliği ortalamaları iki grup arasında benzerdi (tümü için p>0,05). Retinal kalınlık ve koroid kalınlığı açısından da iki grup arasında istatistiksel anlamlı fark görülmedi (p>0,05). Ortalama HSLT alanı santral 500 μm’lik bölgede Grup-1’de anlamlı olarak daha yüksekti (Grup-1: 25678,4 ± 5372,0 μm2 vs. Grup-2: 23375,0 ± 3974,5 μm2, p=0,010). Santral 1000 μm’lik bölgede ise iki grup arasında ortalama HSLT alanları benzerdi (Grup-1: 99859,9 ± 9936,4 μm2 vs Grup-2: 97563 ± 8478,4 μm2, p=0,090). Sonuç: Çalışmamızın bulguları, hafif dereceli ve inaktif dönemdeki TGH olan gözlerde santral foveal bölgede fotoreseptör ve Müller hücrelerinden oluşan HSLT alanında artış olduğunu göstermektedir. HSLT’nin değerlendirilmesi TGH’nin erken tanınması ve takibi için ümit vericidir.

Anahtar Kelimeler

• Fotoreseptör hücre
• Henle sinir lifi tabakası
• Müller hücresi
• tiroid göz hastalığı

Kaynakça

1. 1. Bahn RS. Graves’ ophthalmopathy. N Engl J Med 2010;362:726- 38.
2. 2. Bartalena L, Baldeschi L, Boboridis K, Eckstein A, Kahaly GJ, Marcocci C, Perros P, Salvi M, Wiersinga WM. The 2016 european thyroid association/european group on graves’ orbitopathy guidelines for the management of graves’ orbitopathy. Eur Thyroid J 2016;5:9-26.
3. 3. Bartalena L, Kahaly GJ, Baldeschi L, Dayan CM, Eckstein A, Marcocci C, Marinò M, Vaidya B, Wiersinga WM. The 2021 european group on graves’ orbitopathy (eugogo) clinical practice guidelines for the medical management of graves’ orbitopathy. Eur J Endocrinol 2021;185:G43-g67.
4. 4. Boulakh L, Nygaard B, Bek T, Faber J, Heegaard S, Toft PB, Poulsen HE, Toft-Petersen AP, Hesgaard HB, Ellervik C. Nationwide incidence of thyroid eye disease cumulative incidence of strabismus and surgical interventions in denmark. JAMA Ophthalmol 2022;140:667-673.
5. 5. Bartalena L, Piantanida E, Gallo D, Lai A, Tanda ML. Epidemiology, natural history, risk factors, and prevention of graves’ orbitopathy. Front Endocrinol (Lausanne) 2020;11:615993.
6. 6. Gianoukakis AG, Khadavi N, Smith TJ. Cytokines, graves’ disease, and thyroid-associated ophthalmopathy. Thyroid 2008;18:953-8.
7. 7. Moledina M, Damato EM, Lee V. The changing landscape of thyroid eye disease: Current clinical advances and future outlook. Eye (Lond) 2024;38:1425-1437.
8. 8. Lee H, Lee YH, Suh SI, Jeong EK, Baek S, Seo HS. Characterizing intraorbital optic nerve changes on diffusion tensor imaging in thyroid eye disease before dysthyroid optic neuropathy. J Comput Assist Tomogr 2018;42:293-298.

9. 9. Lujan BJ, Roorda A, Croskrey JA, Dubis AM, Cooper RF, Bayabo JK, Duncan JL, Antony BJ, Carroll J. Directional optical coherence tomography provides accurate outer nuclear layer and henle fiber layer measurements. Retina 2015;35:1511-20.
10. 10. Lujan BJ, Roorda A, Knighton RW, Carroll J. Revealing henle’s fiber layer using spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52:1486-92.
11. 11. Sabermoghaddam A, Shoeibi N, Jafarzadeh H, Bakhtiari E, Salahi Z, Saeidi Rezvani T, Heidarzadeh HR, Abrishami M. Optic nerve head optical coherence tomography angiography findings in patients with thyroid eye disease: A case-control study. Thyroid Res 2022;15:17.
12. 12. Xu B, Wang S, Chen L, Tan J. The early diagnostic value of optical coherence tomography (oct) and oct angiography in thyroid-associated ophthalmopathy. Ther Adv Chronic Dis 2023;14:20406223231166802.
13. 13. Aggarwal D, Tan O, Huang D, Sadun AA. Patterns of ganglion cell complex and nerve fiber layer loss in nonarteritic ischemic optic neuropathy by fourier-domain optical coherence tomography. Invest Ophthalmol Vis Sci 2012;53:4539-45.
14. 14. Dotan G, Goldstein M, Kesler A, Skarf B. Long-term retinal nerve fiber layer changes following nonarteritic anterior ischemic optic neuropathy. Clin Ophthalmol 2013;7:735-40.
15. 15. Wollstein G, Schuman JS, Price LL, Aydin A, Stark PC, Hertzmark E, Lai E, Ishikawa H, Mattox C, Fujimoto JG, Paunescu LA. Optical coherence tomography longitudinal evaluation of retinal nerve fiber layer thickness in glaucoma. Arch Ophthalmol 2005;123:464-70.
16. 16. Ackermann P, Brachert M, Albrecht P, Ringelstein M, Finis D, Geerling G, Aktas O, Guthoff R. Alterations of the outer retina in non-arteritic anterior ischaemic optic neuropathy detected using spectral-domain optical coherence tomography. Clin Exp Ophthalmol 2017;45:496-508.
17. 17. Grading diabetic retinopathy from stereoscopic color fundus photographs--an extension of the modified airlie house classification. Etdrs report number 10. Early treatment diabetic retinopathy study research group. Ophthalmology 1991;98:786-806.
18. 18. Hee MR, Puliafito CA, Duker JS, Reichel E, Coker JG, Wilkins JR, Schuman JS, Swanson EA, Fujimoto JG. Topography of diabetic macular edema with optical coherence tomography. Ophthalmology 1998;105:360-70.
19. 19. Lazarus JH. Epidemiology of graves’ orbitopathy (go) and relationship with thyroid disease. Best Pract Res Clin Endocrinol Metab 2012;26:273-9.
20. 20. Rashad R, Pinto R, Li E, Sohrab M, Distefano AG. Thyroid eye disease. Life (Basel) 2022;12:
21. 21. Kurt MM, Akpolat C, Evliyaoglu F, Yilmaz M, Ordulu F. Evaluation of retinal neurodegeneration and choroidal thickness in patients with inactive graves’ ophthalmopathy. Klin Monbl Augenheilkd 2021;238:797-802.
22. 22. Forte R, Bonavolontà P, Vassallo P. Evaluation of retinal nerve fiber layer with optic nerve tracking optical coherence tomography in thyroid-associated orbitopathy. Ophthalmologica 2010;224:116-21.
23. 23. Eslami F, Borzouei S, Khanlarzadeh E, Seif S. Prevalence of increased intraocular pressure in patients with graves’ ophthalmopathy and association with ophthalmic signs and symptoms in the north-west of iran. Clin Ophthalmol 2019;13:1353-1359.
24. 24. Gumińska M, Kłysik A, Siejka A, Jurowski P. Latanoprost is effective in reducing high intraocular pressure associated with graves’ ophthalmopathy. Klin Oczna 2014;116:89-93.
25. 25. Bilici S, Gültekin Erol T, Bilici E, Cantürk Uğurbaş S, Uğurbaş SH. Evaluating the Effect of Childhood Obesity on Choroidal Structures. Turk J Diab Obes. 2024;8:6–12.
26. 26. Tenlik A, Kulak AE, Güler E, Totan Y, Gürağaç FB, Boyraz M. Evaluation of Ganglion Cell-Inner Plexiform and Retinal Nerve Fiber Layer Thicknesses in Obese Children and Their Associations with Obesity Severity and Duration. Turk J Diab Obes. 2018;2:29–34.
27. 27. Çalışkan S, Acar M, Gürdal C. Choroidal thickness in patients with graves’ ophthalmopathy. Curr Eye Res 2017;42:484-490.
28. 28. Gul A, Basural E, Ozturk HE. Comparison of choroidal thickness in patients with active and stable thyroid eye disease. Arq Bras Oftalmol 2019;82:124-128.
29. 29. Casini G, Marinò M, Rubino M, Licari S, Covello G, Mazzi B, Ionni I, Rocchi R, Sframeli AT, Figus M, Loiudice P. Retinal, choroidal and optic disc analysis in patients with graves’ disease with or without orbitopathy. Int Ophthalmol 2020;40:2129- 2137.
30. 30. Del Noce C, Vagge A, Nicolò M, Traverso CE. Evaluation of choroidal thickness and choroidal vascular blood flow in patients with thyroid-associated orbitopathy (tao) using sd-oct and angio-oct. Graefes Arch Clin Exp Ophthalmol 2020;258:1103- 1107.
31. 31. Zhong S, He F, Fang S, Sun J, Li Y, Shuo Z, Liu X, Song X, Wang Y, Huang Y, Zhou H, Fan X. Choroidal thickness in patients with thyroid-associated ophthalmopathy, as determined by swept-source optical coherence tomography. Br J Ophthalmol 2023;
32. 32. Ersoz MG, Kırık F, Isik B, Ozdemir H. Henle fiber layer thickness and area measurement in type 2 diabetes mellitus with and without retinopathy using a modified directional optical coherence tomography strategy. Retina 2023;43:1097-1106.
33. 33. Motschi AR, Schwarzhans F, Desissaire S, Steiner S, Bogunović H, Roberts PK, Vass C, Hitzenberger CK, Pircher M. Characteristics of henle’s fiber layer in healthy and glaucoma eyes assessed by polarization-sensitive optical coherence tomography. Biomed Opt Express 2023;14:2709-2725.
34. 34. Kennerdell JS, Rosenbaum AE, El-Hoshy MH. Apical optic nerve compression of dysthyroid optic neuropathy on computed tomography. Arch Ophthalmol 1981;99:807-9.
35. 35. Luo L, Li D, Gao L, Wang W. Retinal nerve fiber layer and ganglion cell complex thickness as a diagnostic tool in early stage dysthyroid optic neuropathy. Eur J Ophthalmol 2022;32:3082- 3091.
36. 36. Ooto S, Akagi T, Kageyama R, Akita J, Mandai M, Honda Y, Takahashi M. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci U S A 2004;101:13654-9.
37. 37. Wan J, Zheng H, Chen ZL, Xiao HL, Shen ZJ, Zhou GM. Preferential regeneration of photoreceptor from müller glia after retinal degeneration in adult rat. Vision Res 2008;48:223-34.
38. 38. Iao TWU, Rong SS, Ling AN, Brelén ME, Young AL, Chong KKL. Electrophysiological studies in thyroid associated orbitopathy: A systematic review. Sci Rep 2017;7:12108.
39. 39. Pérez-Rico C, Rodríguez-González N, Arévalo-Serrano J, Blanco R. Evaluation of multifocal visual evoked potentials in patients with graves’ orbitopathy and subclinical optic nerve involvement. Doc Ophthalmol 2012;125:11-9.