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Alterations in retrobulbar haemodynamics in thyroid eye disease

Eye volume 37, pages 3682–3690 (2023)Cite this article

Subjects

Abstract

Purpose

To study the orbital perfusion parameters of ophthalmic artery (OA) and central retinal artery (CRA) in inactive TED and the changes following surgical decompression.

Methods

Non-randomised clinical trial. 24 inactive moderate-to-severe TED orbits of 24 euthyroid cases underwent surgical decompression and examined again at 3 months. The peak systolic velocity (PSV), end-diastolic velocity (EDV), and resistivity index (RI) of OA and CRA were evaluated using colour doppler imaging and normative database was established using 18 healthy controls.

Results

The mean age was 39.38 ± 12.56 years and male: female ratio was 1: 1.18. Intraocular pressure was higher, and CRA-PSV, CRA-RI, OA-PSV, and OA-EDV were lower in TED in comparison to heathy orbits. The CRA-PSV, CRA-EDV, OA-PSV, and OA-EDV negatively correlated with proptosis and duration of thyroid disease. The area under curve of OA-PSV (95% CI:0.964–1.000, p < 0.001) and OA-EDV (95% CI:0.699–0.905, p < 0.001) helped in differentiating TED orbits from HC, and in predicting the severity of disease. Post decompression, CRA-PSV, CRA-EDV, OA-PSV, and OA-EDV improved, with decrease in CRA-RI and OA-RI in both lipogenic and MO.

Conclusions

The orbital perfusion is reduced in inactive TED. The changes in OA flow velocities can help in differentiating inactive TED from healthy orbits and progression of TED. Sequential orbital CDI of OA and CRA can serve as an objective tool for case selection and monitoring response to surgical decompression.

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Fig. 1: ROC comparing doppler parameter changes.
Fig. 2: CDI showing gate placement and velocity waveform.

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Data availability

All data on the measured doppler variables indicating the perfusion in thyroid eye disease orbits that support the findings of this study are included within this paper and its Supplementary Information files.

References

  1. Rundle FF, Wilson CW. Development and course of exophthalmos and ophthalmoplegia in Graves’ disease with special reference to the effect of thyroidectomy. Clin Sci. 1945;5:177–94.

    CAS  PubMed  Google Scholar 

  2. Kashkouli MB, Heidari I, Pakdel F, Jam S, Honarbakhsh Y, Mirarmandehi B. Change in quality of life after medical and surgical treatment of graves’ ophthalmopathy. Middle East Afr J Ophthalmol. 2011;18:42–7.

    Article  PubMed Central  PubMed  Google Scholar 

  3. 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;33:375–80.

    Article  PubMed  Google Scholar 

  4. Nakase Y, Osanai T, Yoshikawa K, Inoue Y. Color Doppler imaging of orbital venous flow in dysthyroid optic neuropathy. Jpn J Ophthalmol. 1994;38:80–6.

    CAS  PubMed  Google Scholar 

  5. Jamshidian-Tehrani M, Nekoozadeh S, Alami E, Ghadimi H, Nabavi A, Ameli K, et al. Color Doppler imaging of orbital vasculature before and after orbital decompression in thyroid eye disease. Orbit. 2019;38:173–9.

    Article  PubMed  Google Scholar 

  6. Onaran Z, Konuk O, Oktar SO, Yucel C, Unal M. Intraocular pressure lowering effect of orbital decompression is related to increased venous outflow in Graves orbitopathy. Curr Eye Res. 2014;39:666–72.

    Article  PubMed  Google Scholar 

  7. Shah SS, Khanam S. Orbital color doppler imaging. Treasure Island (FL): StatPearls; 2021.

  8. Hayreh SS. The blood supply of the optic nerve head and the evaluation of it - myth and reality. Prog Retin Eye Res. 2001;20:563–93.

    Article  CAS  PubMed  Google Scholar 

  9. Alp MN, Ozgen A, Can I, Cakar P, Gunalp I. Colour Doppler imaging of the orbital vasculature in Graves’ disease with computed tomographic correlation. Br J Ophthalmol. 2000;84:1027–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Jamshidian-Tehrani M, Nabavi A, Kasaee A, Hasanpoor N, Elhami E, Sharif-Kashani S, et al. Color Doppler imaging in thyroid eye disease and its correlation to disease activity. Orbit. 2019;38:440–5.

    Article  PubMed  Google Scholar 

  11. Perez-Lopez M, Sales-Sanz M, Rebolleda G, Casas-Llera P, Gonzalez-Gordaliza C, Jarrin E, et al. Retrobulbar ocular blood flow changes after orbital decompression in Graves’ ophthalmopathy measured by color Doppler imaging. Invest Ophthalmol Vis Sci. 2011;52:5612–7.

    Article  PubMed  Google Scholar 

  12. Lesin M, Rogosic V, Vanjaka Rogosic L, Barisic I, Pelcic G. Flow changes in orbital vessels detected with color doppler ultrasound in patients with early dysthyroid optic neuropathy. Acta Clin Croat. 2018;57:301–6.

    PubMed Central  PubMed  Google Scholar 

  13. Nemeth J, Kovacs R, Harkanyi Z, Knezy K, Senyi K, Marsovszky I. Observer experience improves reproducibility of color Doppler sonography of orbital blood vessels. J Clin Ultrasound. 2002;30:332–5.

    Article  PubMed  Google Scholar 

  14. Bude RO, Rubin JM. Relationship between the resistive index and vascular compliance and resistance. Radiology. 1999;211:411–7.

    Article  CAS  PubMed  Google Scholar 

  15. Polska E, Kircher K, Ehrlich P, Vecsei PV, Schmetterer L. RI in central retinal artery as assessed by CDI does not correspond to retinal vascular resistance. Am J Physiol Heart Circ Physiol. 2001;280:H1442–7.

    Article  CAS  PubMed  Google Scholar 

  16. Ho AC, Lieb WE, Flaharty PM, Sergott RC, Brown GC, Bosley TM, et al. Color Doppler imaging of the ocular ischemic syndrome. Ophthalmology. 1992;99:1453–62.

    Article  CAS  PubMed  Google Scholar 

  17. Platt JF, Ellis JH, Rubin JM, DiPietro MA, Sedman AB. Intrarenal arterial Doppler sonography in patients with nonobstructive renal disease: correlation of resistive index with biopsy findings. AJR Am J Roentgenol. 1990;154:1223–7.

    Article  CAS  PubMed  Google Scholar 

  18. Bartalena L, Kahaly GJ, Baldeschi L, Dayan CM, Eckstein A, Marcocci C, et al. 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.

    Article  CAS  PubMed  Google Scholar 

  19. Monteiro ML, Moritz RB, Angotti Neto H, Benabou JE. Color Doppler imaging of the superior ophthalmic vein in patients with Graves’ orbitopathy before and after treatment of congestive disease. Clinics. 2011;66:1329–34.

    PubMed Central  PubMed  Google Scholar 

  20. Nunery WR, Martin RT, Heinz GW, Gavin TJ. The association of cigarette smoking with clinical subtypes of ophthalmic Graves’ disease. Ophthalmic Plast Reconstr Surg. 1993;9:77–82.

    Article  CAS  PubMed  Google Scholar 

  21. Mourits MP, Prummel MF, Wiersinga WM, Koornneef L. Clinical activity score as a guide in the management of patients with Graves’ ophthalmopathy. Clin Endocrinol. 1997;47:9–14.

    Article  CAS  Google Scholar 

  22. Dayan CM, Dayan MR. Dysthyroid optic neuropathy: a clinical diagnosis or a definable entity? Br J Ophthalmol. 2007;91:409–10.

    Article  PubMed Central  PubMed  Google Scholar 

  23. Barrett L, Glatt HJ, Burde RM, Gado MH. Optic nerve dysfunction in thyroid eye disease: CT. Radiology 1988;167:503–7.

    Article  CAS  PubMed  Google Scholar 

  24. Monteiro ML, Goncalves AC, Silva CT, Moura JP, Ribeiro CS, Gebrim EM. Diagnostic ability of Barrett’s index to detect dysthyroid optic neuropathy using multidetector computed tomography. Clinics. 2008;63:301–6.

    Article  PubMed Central  PubMed  Google Scholar 

  25. Muralidhar A, Das S, Tiple S. Clinical profile of thyroid eye disease and factors predictive of disease severity. Indian J Ophthalmol. 2020;68:1629–34.

    Article  PubMed Central  PubMed  Google Scholar 

  26. Naik MN, Vasanthapuram VH. Demographic and clinical profile of 1000 patients with thyroid eye disease presenting to a Tertiary Eye Care Institute in India. Int Ophthalmol. 2021;41:231–6.

    Article  PubMed  Google Scholar 

  27. 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  28. Nabi T, Rafiq N. Factors associated with severity of orbitopathy in patients with Graves’ disease. Taiwan J Ophthalmol. 2020;10:197–202.

    Article  PubMed Central  PubMed  Google Scholar 

  29. Kurioka Y, Inaba M, Kawagishi T, Emoto M, Kumeda Y, Inoue Y, et al. Increased retinal blood flow in patients with Graves’ disease: influence of thyroid function and ophthalmopathy. Eur J Endocrinol. 2001;144:99–107.

    Article  CAS  PubMed  Google Scholar 

  30. Meng N, Zhang P, Huang H, Ma J, Zhang Y, Li H, et al. Color Doppler imaging analysis of retrobulbar blood flow velocities in primary open-angle glaucomatous eyes: a meta-analysis. PLoS One. 2013;8:e62723.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Leydhecker W, Akiyama K, Neumann HG. Intraocular pressure in normal human eyes. Klin Monbl Augenheilkd Augenarzt Fortbild. 1958;133:662–70.

    CAS  Google Scholar 

  32. Ichiki T. Thyroid hormone and vascular remodeling. J Atheroscler Thromb. 2016;23:266–75.

    Article  CAS  PubMed  Google Scholar 

  33. Otto AJ, Koornneef L, Mourits MP. Deen-van Leeuwen L. Retrobulbar pressures measured during surgical decompression of the orbit. Br J Ophthalmol. 1996;80:1042–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Douglas RS, Kahaly GJ, Patel A, Sile S, Thompson EHZ, Perdok R, et al. Teprotumumab for the treatment of active thyroid eye disease. N Engl J Med. 2020;382:341–52.

    Article  CAS  PubMed  Google Scholar 

  35. Meyer P, Das T, Ghadiri N, Murthy R, Theodoropoulou S. Clinical pathophysiology of thyroid eye disease: the Cone Model. Eye. 2019;33:244–53.

    Article  PubMed Central  PubMed  Google Scholar 

  36. Rootman DB. Orbital decompression for thyroid eye disease. Surv Ophthalmol. 2018;63:86–104.

    Article  PubMed  Google Scholar 

  37. Danesh-Meyer HV, Savino PJ, Deramo V, Sergott RC, Smith AF. Intraocular pressure changes after treatment for Graves’ orbitopathy. Ophthalmology. 2001;108:145–50.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Ophthalmology, Maulana Azad Medical College, New Delhi, India

    Ruchi Goel, Shalin Shah, Sonam Singh, Mohit Chhabra, Samreen Khanam & Sumit Kumar

  2. Department of Radiology, Maulana Azad Medical College, New Delhi, India

    Swati Gupta & Tamanna Khullar

  3. Department of Prosthodontics, Maulana Azad Institute of Dental Sciences, New Delhi, India

    Pankaj Sharma

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Correspondence to Shalin Shah.

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Goel, R., Shah, S., Gupta, S. et al. Alterations in retrobulbar haemodynamics in thyroid eye disease. Eye 37, 3682–3690 (2023). https://doi.org/10.1038/s41433-023-02580-2

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