Orbital US-based characteristics in Graves’ disease-associated autoimmune ophthalmopathy
Yu.V. Buldygina, G.M. Terekhova, Ie.A. Shelkovoy, T.V. Fed’ko
Komisarenko Institute for Endocrinology and Metabolism, NAMS of Ukraine; Kyiv (Ukraine)
TO CITE THIS ARTICLE: Buldygina YuV, Terekhova GM, Shelkovoy IeA, Fed’ko TV. Orbital US-based characteristics in Graves’ disease-associated autoimmune ophthalmopathy. J.ophthalmol.(Ukraine).2020;4:8-13.http://doi.org/10.31288/oftalmolzh20204813
Background: Autoimmune ophthalmopathy (AO) may develop in as much as 90% patients with Graves’ disease (GD), and may lead to visual disability. Adequate imaging of orbital structures allows planning adequate treatment in most cases, contributing to better treatment outcomes in patients with AO.
Purpose: To examine orbital ultrasound (US)-based characteristics in patients with GD-associated AO.
Material and Methods: One hundred patients with GD-associated AO underwent a comprehensive examination that included (1) determination of AO activity by clinical activity score (CAS), (2) measurements of thyrotropin (TSH), free thyroxine (FT4), free triiodothyronine (FT3), and TSH-R-Ab levels; and (3) US of the thyroid gland and orbital tissue. In addition, 31 of these patients underwent magnetic resonance imaging (MRI). The Student t test was used for statistical analyses. The level of significance p ≤ 0.05 was assumed. Data are presented as mean ± SEM.
Results: One hundred patients (73 women and 27 men; age, 18 to 79 years; mean age, 48.42 ± 13.56 years; mean disease duration, 3.1 ± 2.2 years) with GD-associated AO were included in this study. Of these, 65% were euthyroids, whereas 18% and 17% were found to have clinical hyperthyroidism and subclinical hyperthyroidism, respectively. As expected, the mean TSH-R-Ab level (11.07±1.03 U/mL) was higher than normal (<0.55 U/mL), confirming the presence of GD. Most patients had class III (36%) or class IV (34%) disease according to NO SPECS classification, 49 patients had a CAS score > 3 (active disease), and 51 had a CAS score < 3 (non-active disease). Orbital US found that, in all patients, the lens was normally located anatomically, and the chorioretinal complex and the subdural space of the optic nerve were of normal thickness. Retrobulbar adipose tissue (RAT) edema was found in 49 patients with active disease. Of these 49, four also exhibited eyelid edema. RAT fibrosis without muscle fibrosis was found in 21 patients, and with muscle fibrosis, in 30 patients. Although 49 patients had active AO, US-based thickness of the orbital rectus muscles was within reference intervals. In all patients, the rectus muscles were seen as hypoechogenic structures. There was a significant difference in orbital rectus muscle thickness measurements between orbital US and MRI. Thus, MRI-based thickness of medial, lateral, superior and inferior rectus muscles was significantly greater (р < 0.05) than US-based thickness of these muscles, with US demonstrating normal thickness.
Conclusion: First, orbital ultrasonography found RAT edema in 49%, and RAT fibrosis in 51% of patients with GD-associated AO. Second, in all patients with active AO, orbital US provided valuable data for assessing the status of RAT and determining whether RAT edema or fibrosis was present. Third, MRI-based thickness of orbital rectus muscles was significantly (p < 0.05) greater than US-based thickness of these muscles, with US demonstrating normal thickness. Finally, because orbital US does not provide reliable data for determining orbital rectus muscle thickness, especially in active AO, it is reasonable to use orbital MRI for this purpose.
Keywords: autoimmune ophthalmopathy, Graves’ disease, ultrasound examination, magnetic resonance imaging
1.Kahaly GJ, Bartalena L, Hegedüs L, Leenhardt L, Poppe K, Pearce SH. 2018 European Thyroid Association Guideline for the Management of Graves' Hyperthyroidism. Eur Thyroid J. 2018 Aug;7(4):167-86.
2.Smith TJ, Janssen JAMJL. Insulin-like Growth Factor-I Receptor and Thyroid-Associated Ophthalmopathy. Endocr Rev. 2019 Feb 1;40(1):236-67.
3.Bartalena L, Pinchera A, Marcocci C. Management of Graves' ophthalmopathy: reality and perspectives. Endocr Rev. 2000 Apr;21(2):168-99.
4.Mourits MP, Koornneef L, Wiersinga WM, Prummel MF, Berghout A, van der Gaag R. Clinical criteria for the assessment of disease activity in Graves' ophthalmopathy: a novel approach. Br J Ophthalmol. 1989 Aug;73(8):639-44.
5.Gerding MN, Prummel MF, Wiersinga WM. Assessment of disease activity in Graves' ophthalmopathy by orbital ultrasonography and clinical parameters. Clin Endocrinol (Oxf). 2000 May;52(5):641-6.
6.Stamato FJ, Maciel RM, Manso PG, Wolosker AM, Paiva ER, Lopes AC, Furlanetto RP. Colchicine in the treatment of the inflammatory phase of Graves' ophthalmopathy: a prospective and randomized trial with prednisone. Arq Bras Oftalmol. 2006 Nov-Dec;69(6):811-6.
7.Prummel MF. Graves' ophthalmopathy: diagnosis and management. Eur J Nucl Med. 2000 Apr;27(4):373-6.
8.Kahaly GJ. Imaging in thyroid-associated orbitopathy. Eur J Endocrinol. 2001 Aug;145(2):107-18.
9.Erickson BA, Harris GJ, Lewandowski MF, Murray KJ, Massaro BM. Echographic monitoring of response of extraocular muscles to irradiation in Graves' ophthalmopathy. Int J Radiat Oncol Biol Phys. 1995 Feb1;31(3):651-60.
10.Yanik B, Conkbayir I, Acaroglu G, Hekimoglu B. Graves' ophthalmopathy: comparison of the Doppler sonography parameters with the clinical activity score. J Clin Ultrasound. 2005 Oct;33(8):375-80.
11.Zubarev AV, editor. [A practical guide to diagnostic ultrasound in ophthalmology]. Moscow: Strom; 2002. Russian.
12.DiBernardo CW, Greenberg E. Ophthalmic Ultrasound: A Diagnostic Atlas. New York: Thieme Medical Publishers; 2007.
13.Nagy EV, Toth J, Kaldi I, Damjanovich J, Mezosi E, LenkeyA, et al. Graves’ ophthalmopathy: eye muscle involvement in patients with diplopia. Eur J Endocrinol. 2000 Jun;142 (6): 591–7
14.Gorman CA. The measurement of change in Graves' ophthalmopathy. Thyroid. 1998 Jun;8(6):539-43.
15.Werner SC. Classification of the eye changes of Graves' disease. Am J Ophthalmol. 1969;68(4):646–8.
16.Ozgen A, Aydingöz U. Normative measurements of orbital structures using MRI. J Comput Assist Tomogr. 2000 May-Jun;24(3):493-6.
17.Zhou Quan. Die Rolle der orbitalen MRT in der Differentialdiagnose von Erkrankungen der Augenmuskeln, des extrakonalen und subperiostalen Kompartimentes. Dissertation. 2003. Germany. 96 p. DOI: 10.18452/14831.
The authors certify that they have no conflicts of interest in the subject matter or materials discussed in this manuscript.