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Increase of Central Foveal and Temporal Choroidal Thickness in Patients with Inactive Thyroid Eye Disease Joohyun Kim, Sumin Yoon and Sehyun Baek*

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Increase of Central Foveal and Temporal Choroidal Thickness in Patients with Inactive Thyroid Eye Disease Joohyun Kim, Sumin Yoon and Sehyun Baek* Kim et al. BMC Ophthalmology (2021) 21:32 https://doi.org/10.1186/s12886-021-01804-x RESEARCH ARTICLE Open Access Increase of central foveal and temporal choroidal thickness in patients with inactive thyroid eye disease Joohyun Kim, Sumin Yoon and Sehyun Baek* Abstract Background: In this study, we aimed to compare the choroidal thickness between a group of Korean patients with inactive thyroid eye disease (TED) and a control group of Korean patients and to analyze the variables affecting choroidal thickness. Methods: Patients diagnosed with inactive TED and without TED who underwent optical coherence tomography and axial length measurements were included and classified into the TED group and control group. Choroidal thickness was measured using images acquired in enhanced depth imaging (EDI) mode by cirrus HD-OCT (Carl Zeiss Meditec Inc., Dublin, CA, UAS) at the central fovea and points 1.5 mm nasal and 1.5 mm temporal from the central fovea using a caliper tool provided by OCT software. Results: The mean central foveal choroidal thickness was 294.2 ± 71.4 µm and 261.1 ± 47.4 µm in the TED and control groups, respectively, while the mean temporal choroidal thickness was 267.6 ± 67.5 µm and 235.7 ± 41.3 µm in the TED and control groups, respectively, showing significant differences between the two groups (P = 0.011, P = 0.008). The mean nasal choroidal thickness was 232.1 ± 71.7 µm and 221.1 ± 59.9 µm in the TED and control groups, respectively, showing no significant difference between the two groups (P = 0.421). Multivariate regression analysis showed the factors affecting central foveal choroidal thickness were age, axial length, and degree of exophthalmos, and factors affecting temporal choroidal thickness were age and degree of exophthalmos. Conclusions: Central foveal and temporal choroidal thickness were significantly thicker in patients with inactive TED than in control subjects, while age, axial length, and degree of exophthalmos were identified as major factors affecting choroidal thickness. Keywords: Choroidal thickness, Optical coherence tomography, Thyroid eye disease Background TED present with mild symptoms, the condition may Thyroid eye disease (TED) is an autoimmune disorder progress into a more severe form in approximately 3–5% characterized by proliferation of the orbital fat tissue of the patients. TED involves proliferation of orbital and inflammation of the orbital connective tissue and fibro-adipose tissues and infiltration of inflammatory extraocular muscles. TED is observed in approximately cells, causing an increase in orbital tissue volume. Clin- 25–50% of patients with Graves’ disease and 2% of ical signs of TED include dry eyes, exposure keratopathy, patients with thyroiditis [1]. Although most patients with exophthalmos, diplopia, and decreased visual acuity [2]. The choroid supplies 70% or more of the total blood * Correspondence: [email protected] volume involved in ocular circulation, and provides Department of Ophthalmology, Korea University College of Medicine, 148 oxygen and nutrients to the outer retinal layer. It has Gurodong-ro, Guro-gu, 08308 Seoul, Korea © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Kim et al. BMC Ophthalmology (2021) 21:32 Page 2 of 6 been reported that central serous chorioretinopathy, eyelid swelling, eyelid erythema, conjunctival injection, age-related macular degeneration, ocular inflammatory chemosis, and swollen caruncle [12]. disease, diabetes mellitus, and glaucoma may affect Choroidal thickness was measured using images ac- choroidal circulation, leading to changes in choroidal quired in enhanced depth imaging (EDI) mode by cirrus thickness [3–9]. HD-OCT (Carl Zeiss Meditec Inc., Dublin, CA, UAS). Recently, there have been a few studies on changes in For choroidal thickness, the vertical distance between choroidal thickness in patients with TED and it has been the outermost border of retinal pigment epithelium reported that patients with higher clinical activity scores appearing as high-reflection line in OCT images and (CAS) tend to show increased choroidal thickness [10, 11]. inner border of the sclera was measured at the central However, the exact cause of choroidal thickening has not fovea and points 1.5 mm nasal and 1.5 mm temporal yet been identified, and there is no clinical study that from the central fovea using a caliper tool provided by included only patients with TED who have low CAS. OCT software (Fig. 1). Accordingly, the authors of the present study aimed to SPSS version 20.0 (IBM corp., Armonk, NY, USA) was compare the choroidal thickness between patients with in- used for statistical analysis and the measured values active TED (TED group) and control group and analyze from the right eye of TED and control groups were used the variables affecting choroidal thickness to understand in the statistical analysis. The choroidal thickness be- the pathophysiology of changes in choroidal thickness in tween the two groups was compared by independent patients with TED. sample t-test with a statistical significance level of < 0.05. In addition, for variables with a P value of ≤ 0.15 in Methods univariate regression analysis, multivariate regression Among 58 patients who visited the Department of analysis was performed to examine the factors that affect Ophthalmology in Korea University Guro Hospital be- choroidal thickness. tween March 2017 and June 2018 and were subsequently diagnosed with TED, the medical records of 49 patients Results (15 males and 34 females) with inactive TED and CAS < The present study included 49 eyes each from the TED 3 were analyzed retrospectively. For the control group, and control groups. The mean age of the target patients we included 49 consecutive patients (15 male and 34 fe- was 51.1 ± 13.2 and 50.2 ± 14.4 years in the TED and male) without TED who underwent optical coherence control groups, respectively, showing no significant dif- tomography and axial length measurements since March ference between the two groups (P = 0.656). The mean 2017 in the Department of Ophthalmology. The patients spherical equivalent was − 1.3 ± 2.4 D and − 0.8 ± 1.7 D provided informed consent. The study was conducted in the TED and control groups, respectively, showing no following the tenets of the Helsinki Declaration and was significant difference between the two groups (P = 0.112) approved by the Institutional Review Board of Korea (Table 1). The mean CAS was 1.4 ± 1.3 in the TED University Medical Center. group with 81.6%, 8.2%, and 10.2% showing hyperthy- Diagnosis of TED was defined as meeting two or more roidism, hypothyroidism, and normal thyroid function, of the following criteria: (1) abnormal findings in thyroid respectively (Table 2). function tests, (2) having degree of exophthalmos ≥ The mean central foveal choroidal thickness was 17 mm or difference of ≥ 2 mm between the two eyes as 294.2 ± 71.4 µm and 261.1 ± 47.4 µm in the TED and measured using an exophthalmometer; presenting with control groups, respectively, while the mean temporal other symptoms, including lid retraction or lid lag, and choroidal thickness was 267.6 ± 67.5 µm and 235.7 ± (3) enlarged extraocular muscles confirmed by orbital 41.3 µm in the TED and control groups, respectively, computed tomography. Patients diagnosed with glau- showing significant differences between the two groups coma, pachychroid disease spectrum, choroidal disease, (P = 0.011 and P = 0.008, respectively). Meanwhile, the or retinopathy; patients with refractive power < -6 or mean nasal choroidal thickness was 232.1 ± 71.7 µm and ≥ + 6 diopter; and patients who underwent previous 221.1 ± 59.9 µm in the TED and control groups, respect- refractive surgery were excluded. ively, showing no significant difference between the two The patient characteristics investigated included age, groups (P = 0.421)(Table 3). gender, intraocular pressure, degree of exophthalmos, In the TED group, factors affecting central foveal chor- CAS, spherical equivalent, axial length, blood free T4, oidal thickness were analyzed using univariate regression T3, thyroid-stimulating hormone(TSH), and thyroid- analysis, and variables P value of ≤ 0.15, including age, stimulating immunoglobulin(TSI) concentrations, and axial length, degree of exophthalmos, and CAS were in- choroidal thickness. To assess the disease activity, CAS cluded in the multivariate regression analysis (Table 4). was calculated by adding 1 point each for the following The multivariate simple regression analysis results showed
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