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Automated evaluation of parapapillary choroidal microvasculature in thyroid eye disease

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Abstract

Purpose

The purpose of the study was to investigate the parapapillary choroidal microvasculature in thyroid eye disease (TED) using optical coherence tomography angiography (OCTA).

Methods

Only one eye of each subject was included in the study. Patients with TED and controls were included in the study. Participants were divided into three groups: control, inactive TED (ITED) and active TED (ATED). OCTA scans of the optic discs were obtained in a 4.5 × 4.5-mm rectangular area. Radial peripapillary capillary (RPC) density and peripapillary retinal nerve fibre layer (pRNFL) thickness were automatically calculated by the device software. Parapapillary choroidal microvasculature (PPCMv) density was automatically calculated using MATLAB software.

Results

Forty-one patients with TED and 40 controls were included in the study. RPC density was significantly decreased in the ATED and dysthyroid optic neuropathy (DON) group compared to the controls and ITED group. There was significant increase in pRNFL in the ATED group. PPCMv density increased in the ATED group compared to the controls in whole ring area. The RPC density was significantly correlated with the TSHr Ab level (r < − 0.396, p < 0.001). Clinical activity score correlated positively with PPCMv density (r = 0.349, p = 0.001) but negatively with RPC density (r = − 0.321, p = 0.004).

Conclusion

Changes in peripapillary microvascular perfusion may play a role in the development of DON. As the severity of TED increases with clinical activity, so do the changes observed in peripapillary parameters. The decrease in RPC density may be due to compression caused by optic disc oedema, which may result in reduced blood flow. The increase in PPCMv density may be related to factors such as orbital congestion.

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Data availability

The data sets generated and/or analysed in the current study are available from the corresponding author upon reasonable request.

References

  1. Weiler DL (2017) Thyroid eye disease: a review. Clin Exp Optom 100(1):20–25

    Article  PubMed  Google Scholar 

  2. Gupta S, Douglas R (2011) The pathophysiology of thyroid eye disease (TED): implications for immunotherapy. Curr Opin Ophthalmol 22(5):385

    Article  PubMed  PubMed Central  Google Scholar 

  3. Shan SJ, Douglas RS (2014) The pathophysiology of thyroid eye disease. J Neuroophthalmol 34(2):177–185

    Article  PubMed  Google Scholar 

  4. Scott IU, Siatkowski RM (1999) Thyroid eye disease. Semin Ophthalmol 4(2):52–61

    Article  Google Scholar 

  5. Mourits M, Koornneef L, Wiersinga W et al (1989) Clinical criteria for the assessment of disease activity in Graves’ ophthalmopathy: a novel approach. Br J Ophthalmol 73(8):639–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Bartalena L, Baldeschi L, Boboridis K et al (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Jia Y, Wei E, Wang X et al (2016) Optical coherence tomography angiography of optic disc perfusion in glaucoma. Ophthalmology 121(7):1322–1332

    Article  Google Scholar 

  8. Fard MA, Safizadeh M, Shaabani A et al (2021) Automated evaluation of parapapillary choroidal microvasculature in pseudoexfoliation syndrome and pseudoexfoliation glaucoma. Am J Ophthalmol 224:178–184

    Article  Google Scholar 

  9. Konuk O, Onaran Z, Ozhan Oktar S et al (2009) Intraocular pressure and superior ophthalmic vein blood flow velocity in Graves’ orbitopathy: relation with the clinical features. Graefe’s Arch Clin Exp Ophthalmol 247:1555–1559

    Article  Google Scholar 

  10. Özkan B, Koçer ÇA, Altintaş Ö et al (2016) Choroidal changes observed with enhanced depth imaging optical coherence tomography in patients with mild graves orbitopathy. Eye 30(7):917–924

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hayreh SS (2001) The blood supply of the optic nerve head and the evaluation of it—Myth and reality. Prog Ret Eye Res 20(5):563–593

    Article  CAS  Google Scholar 

  12. Hojati S, Kafieh R, Fardafshari P et al (2020) A MATLAB package for automatic extraction of flow index in OCT-A images by intelligent vessel manipulation. SoftwareX 12:100510

    Article  Google Scholar 

  13. Fard MA, Salabati M, Mahmoudzadeh R et al (2020) Automated evaluation of parapapillary choroidal microvasculature in ischemic optic neuropathy and open angle glaucoma. Invest Ophthalmol Vis Sci 61(3):35

    Article  Google Scholar 

  14. Delaey C, Van de Voorde J (2000) Regulatory mechanisms in the retinal and choroidal circulation. Ophthalmic Res 32(6):249–256

    Article  CAS  PubMed  Google Scholar 

  15. Alm A, Bill A (1973) Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): a study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Exp Eye Res 15(1):15–29

    Article  CAS  PubMed  Google Scholar 

  16. Coskun E, Gurler B, Pehlivan Y et al (2013) Enhanced depth imaging optical coherence tomography findings in Behcet disease. Ocul Immunol Inflamm 21(6):440–445

    Article  PubMed  Google Scholar 

  17. Çalışkan S, Acar M, Gürdal C (2017) Choroidal thickness in patients with Graves’ ophthalmopathy. Curr Eye Res 42(3):484–490

    Article  PubMed  Google Scholar 

  18. Agrawal R, Gupta P, Tan K-A et al (2016) Choroidal vascularity index as a measure of vascular status of the choroid: measurements in healthy eyes from a population-based study. Sci Rep 6(1):1–9

    Article  CAS  Google Scholar 

  19. Loiudice P, Pellegrini M, Marinò M et al (2021) Choroidal vascularity index in thyroid-associated ophthalmopathy: a cross-sectional study. Eye Vis 8(1):1–8

    Article  Google Scholar 

  20. Dave TV, Jonnadula GB, Lanka P et al (2022) Choroidal vascularity index in thyroid eye disease: comparison with controls and application in diagnosing non-inflammatory active disease. Orbit 41(1):89–96

    Article  PubMed  Google Scholar 

  21. Zhang T, Xiao W, Ye H et al (2019) Peripapillary and macular vessel density in dysthyroid optic neuropathy: an optical coherence tomography angiography study. Invest Ophthalmol Vis Sci 60(6):1863–1869

    Article  PubMed  Google Scholar 

  22. Jian H, Wang Y, Ou L et al (2022) Altered peripapillary vessel density and nerve fiber layer thickness in thyroid-associated ophthalmopathy using optical coherence tomography angiography. Int Ophthalmol 42(3):855–862

    Article  PubMed  Google Scholar 

  23. Jamshidian Tehrani M, Mahdizad Z, Kasaei A et al (2019) Early macular and peripapillary vasculature dropout in active thyroid eye disease. Graefe’s Arch Clin Exp Ophthalmol 257:2533–2540

    Article  Google Scholar 

  24. Diana T, Kahaly GJ (2018) Thyroid stimulating hormone receptor antibodies in thyroid eye disease—Methodology and clinical applications. Ophthalmic Plast Reconst Surg 34(4S):S13–S19

    Article  Google Scholar 

  25. Balzan S, Del Carratore R, Nicolini G et al (2012) Proangiogenic effect of TSH in human microvascular endothelial cells through its membrane receptor. J Clin Endocrinol 97(5):1763–1770

    Article  CAS  Google Scholar 

  26. Dolman P (2021) Dysthyroid optic neuropathy: evaluation and management. J Endocrinol Invest 44(3):421–429

    Article  CAS  PubMed  Google Scholar 

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Funding

The authors declare that no funding, grants or other support were received during the preparation of this manuscript. The authors have no relevant financial interests to disclose.

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Authors and Affiliations

  1. Department of Ophthalmology, Erciyes University School of Medicine, Kayseri, Turkey

    Hidayet Sener, Furkan Ozer, Metin Unlu & Duygu Gulmez Sevim

Authors
  1. Hidayet Sener
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  2. Furkan Ozer
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  3. Metin Unlu
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  4. Duygu Gulmez Sevim
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Contributions

HS contributed to methodology, data curation, formal analysis, statistical and image processing software and writing—original draft. FO helped in conceptualisation, data curation, investigation, validation and writing—revision and editing. MU helped in methodology, project management, visualisation and writing—revision and editing. DGS helped in validation, visualisation and writing—revision and editing.

Corresponding author

Correspondence to Metin Unlu.

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Conflict of interest

The authors report no potential conflicts of interest.

Ethics approval and informed consent

The study protocol was approved by the local ethics committee of Erciyes University (No.: 2021/356). Written informed consent was obtained from all individual participants.

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This paper has not been published elsewhere. It is not currently under consideration for publication elsewhere.

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Sener, H., Ozer, F., Unlu, M. et al. Automated evaluation of parapapillary choroidal microvasculature in thyroid eye disease. Int Ophthalmol 43, 4323–4331 (2023). https://doi.org/10.1007/s10792-023-02844-6

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  • DOI: https://doi.org/10.1007/s10792-023-02844-6

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