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Optical coherence tomography and shear wave elastography findings in Graves ophthalmopathy

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Abstract

Purpose

The main feature of Graves ophthalmopathy (GO) is revealed by determining the activity and severity of the disease. We aimed to evaluate the use of imaging methods can also provide additional information about the severity of this disease.

Methods

Optical coherence tomography (OCT) and shear wave elastography (SWE) findings were compared in 32 patients with mild GO group and in the healthy control group. Measuring for TSH receptor antibody (TRAb) serum level is used third-generation assay.

Results

In Graves group, optic nerve sheath diameter (ONSD) values were increased in both eyes (p < 0.001, p < 0.001). SWE measurements showed a significant increase both eye optic nerve (ON) and right eye soft tissue elasticity values in GO group (p < 0.001, p < 0.001, p < 0.001, respectively). There was a significant thinning in left temporal retinal nerve fiber layer (RNFL) thickness and left RNFL peripapillary thickness in GO group (p < 0.001, p < 0.025, respectively). There was a correlation between left eye OCT and SWE findings. Also, there was a significant difference between the median left eye ON and soft tissue elasticity results in the TRAb-positive GO group (p = 0.049, p = 0.048, respectively).

Conclusion

SWE measurements showed a significant increase both eyes ONSD, ON and right eye soft tissue elasticity values in GO group. GO group was significant thinning in some left eye regions in OCT measurements. There was a correlation between left eye OCT and SWE findings. In addition to clinical activity score and TRAb, SWE and OCT can be used to monitor in patients with GO.

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Data and materials availability

Authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. The data that support the findings of this study are available from the corresponding author and the principal investigator, Eren Gürkan, upon reasonable request.

References

  1. Kahaly GJ, Bartalena L, Hegedüs L, Leenhardt L, Poppe K, Pearce SH (2018) 2018 European thyroid association guideline for the management of graves hyperthyroidism. Eur Thyroid J 7(4):167–186. https://doi.org/10.1159/000490384

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Kahaly GJ (2020) Management of graves thyroidal and extrathyroidal disease: an update. J Clin Endocrinol Metab 105(12):3704–3720. https://doi.org/10.1210/clinem/dgaa646

    Article  PubMed  PubMed Central  Google Scholar 

  3. Perros P, Zarkovic M, Azzolini C, Ayvaz G, Baldeschi L, Bartalena L et al (2015) PREGO (presentation of graves orbitopathy) study: changes in referral patterns to European group on graves orbitopathy (EUGOGO) centers over the period from 2000 to 2012. Br J Ophthalmol 99:1531–1535. https://doi.org/10.1136/bjophthalmol-2015-306733

    Article  PubMed  Google Scholar 

  4. Bartalena L, Piantanida E, Gallo D, Lai A, Tanda ML (2020) Epidemiology, natural history, risk factors, and prevention of graves orbitopathy. Front Endocrinol 11:615993. https://doi.org/10.3389/fendo.2020.615993

    Article  Google Scholar 

  5. Ippolito S, Cusini C, Lasalvia P, Gianfagna F, Veronesi G, Gallo D et al (2021) Change in newly diagnosed graves disease phenotype between the twentieth and the twenty-first centuries: meta-analysis and meta-regression. J Endocrinol Invest 44:1707–1718. https://doi.org/10.1007/s40618-020-01479-z

    Article  PubMed  CAS  Google Scholar 

  6. Sakata LM, Deleon-Ortega J, Sakata V, Girkin CA (2009) Optical coherence tomography of the retina and optic nerve-a review. Clin Exp Ophthalmol 37(1):90–99. https://doi.org/10.1111/j.1442-9071

    Article  PubMed  Google Scholar 

  7. Ballantyne SA, O’Neill G, Hamilton R, Hollman AS (2002) Observer variation in the sonographic measurement of optic nerve sheath diameter in normal adults. Eur J Ultrasound 15(3):145–149. https://doi.org/10.1016/s0929-8266(02)00036-8

    Article  PubMed  CAS  Google Scholar 

  8. Çebi Olgun D, Korkmazer B, Kılıç F, Dikici AS, Velidedeoğlu M, Aydoğan F, Kantarcı F, Yılmaz MH (2014) Use of shear wave elastography to differentiate benign and malignant breast lesions. Diagn Interv Radiol 20(3):239–244. https://doi.org/10.5152/dir.2014.13306

    Article  PubMed  Google Scholar 

  9. Cetin EN, Yaylali V, Yildirim C (2011) Isolated optic neuropathy in a case of behçet’s disease. Int Ophthalmol 31(2):153–155. https://doi.org/10.1007/s10792-011-9416-1

    Article  PubMed  Google Scholar 

  10. Wiersinga WM, Perros P, Kahaly GJ, Mourits MP, Baldeschi L, Boboridis K, Boschi A, Dickinson AJ, Kendall-Taylor P, Krassas GE, Lane CM, Lazarus JH, Marcocci C, Marino M, Nardi M, Neoh C, Orgiazzi J, Pinchera A, Pitz S, Prummel MF, Sartini MS, Stahl M, von Arx G (2006) Clinical assessment of patients with graves’ orbitopathy: the European group on graves’ orbitopathy recommendations to generalists, specialists and clinical researchers. Eur J Endocrinol 155(3):387–389. https://doi.org/10.1530/eje.1.02230

    Article  PubMed  CAS  Google Scholar 

  11. Cakmak AI, Atalay E, Cankurtaran V, Yaşar E, Turgut FH (2020) Optical coherence tomography angiography analysis of fabry disease. Int Ophthalmol 40(11):3023–3032. https://doi.org/10.1007/s10792-020-01486-2

    Article  PubMed  Google Scholar 

  12. Spaide RF, Fujimoto JG, Waheed NK (2015) Optical coherence tomography angiography. Retina 35(11):2161–2162. https://doi.org/10.1097/IAE.0000000000000881

    Article  PubMed  PubMed Central  Google Scholar 

  13. Dubourg J, Javouhey E, Geeraerts T, Messerer M, Kassai B (2011) Ultrasonography of optic nerve sheath diameter for detection of raised intracranial pressure: a systematic review and meta-analysis. Intensive Care Med 37(7):1059–1068. https://doi.org/10.1007/s00134-011-2224-2

    Article  PubMed  Google Scholar 

  14. Kazim M, Trokel SL, Acaroglu G, Elliott A (2000) Reversal of dysthyroid optic neuropathy following orbital fat decompression. Br J Ophthalmol 84(6):600–605. https://doi.org/10.1136/bjo.84.6.600

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Jaggi GP, Miller NR, Flammer J, Weinreb RN, Remonda L, Killer HE (2012) Optic nerve sheath diameter in normal-tension glaucoma patients. Br J Ophthalmol 96(1):53–56. https://doi.org/10.1136/bjo.2010.199224

    Article  PubMed  Google Scholar 

  16. Lochner P, Cantello R, Brigo F, Coppo L, Nardone R, Tezzon F, Raymkulova O, Strigaro G, Comi C, Leone MA (2014) Transorbital sonography in acute optic neuritis: a case-control study. AJNR Am J Neuroradiol 35(12):2371–2375. https://doi.org/10.3174/ajnr.A4051

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Ji X, Xiao W, Ye H, Chen R, Wu J, Mao Y, Yang H (2021) Ultrasonographic measurement of the optic nerve sheath diameter in dysthyroid optic neuropathy. Eye 35(2):568–574. https://doi.org/10.1038/s41433-020-0904-2

    Article  PubMed  Google Scholar 

  18. Wu Y, Tu Y, Wu C, Bao L, Wang J, Lu F, Shen M, Chen Q (2020) Reduced macular inner retinal thickness and microvascular density in the early stage of patients with dysthyroid optic neuropathy. Eye Vis 10(7):16. https://doi.org/10.1186/s40662-020-00180-9

    Article  Google Scholar 

  19. Sen E, Berker D, Elgin U, Tutuncu Y, Ozturk F, Guler S (2012) Comparison of optic disc topography in the cases with graves disease and healthy controls. J Glaucoma 21(9):586–589. https://doi.org/10.1097/IJG.0b013e31822e8c4f

    Article  PubMed  Google Scholar 

  20. Blum Meirovitch S, Leibovitch I, Kesler A, Varssano D, Rosenblatt A, Neudorfer M (2017) Retina and nerve fiber layer thickness in eyes with thyroid-associated ophtha1mopathy. Isr Med Assoc J 19(5):277–281

    PubMed  Google Scholar 

  21. Zhang T, Xiao W, Ye H, Chen R, Mao Y, Yang H (2019) Peripapillary and macular vessel density in dysthyroid optic neuropathy: an optical coherence tomography angiography study. Invest Ophthalmol Vis Sci 60(6):1863–1869. https://doi.org/10.1167/iovs.18-25941

    Article  PubMed  Google Scholar 

  22. Zemanová M (2019) Usage of shear wave elastography for diagnosis of changes of oculomotor muscles in endocrine orbitopathy. Cesk Slov Oftalmol 75(1):14–24. https://doi.org/10.31348/2019/1/2

    Article  PubMed  Google Scholar 

  23. Özdemir A, Şahan MH, Asal N, İnal M, Güngüneş A (2020) Evaluation of the medial rectus muscle and optic nerve using strain and shear wave elastography in Graves’ patients. Jpn J Radiol 38(11):1028–1035. https://doi.org/10.1007/s11604-020-01014-3

    Article  PubMed  CAS  Google Scholar 

  24. Batur M, Batur A, Çilingir V, Seven E, Çinal A, Bora A, Yaşar T (2018) Ultrasonic elastography evaluation in optic neuritis. Semin Ophthalmol 33(2):237–241. https://doi.org/10.1080/08820538.2016.1208765

    Article  PubMed  Google Scholar 

  25. Inal M, Tan S, Demirkan S, Burulday V, Gündüz Ö, Örnek K (2017) Evaluation of optic nerve with strain and shear wave elastography in patients with behçet’s disease and healthy subjects. Ultrasound Med Biol 43(7):1348–1354. https://doi.org/10.1016/j.ultrasmedbio.2017.03.008

    Article  PubMed  Google Scholar 

  26. İnal M, Tan S, Yumusak EM, Şahan MH, Alpua M, Örnek K (2017) Evaluation of the optic nerve using strain and shear wave elastography in patients with multiple sclerosis and healthy subjects. Med Ultrason 19(1):39–44. https://doi.org/10.11152/mu-939

    Article  PubMed  Google Scholar 

  27. Wiersinga W, Žarković M, Bartalena L, Donati S, Perros P, Okosieme O, Morris D, Fichter N, Lareida J, von Arx G, Daumerie C, Burlacu MC, Kahaly G, Pitz S, Beleslin B, Ćirić J, Ayvaz G, Konuk O, Törüner FB, Salvi M, Covelli D, Curro N, Hegedüs L, Brix T (2018) Predictive score for the development or progression of Graves’ orbitopathy in patients with newly diagnosed Graves’ hyperthyroidism. Eur J Endocrinol 178(6):635–643. https://doi.org/10.1530/EJE-18-0039

    Article  PubMed  CAS  Google Scholar 

  28. Eckstein AK, Plicht M, Lax H, Neuhäuser M, Mann K, Lederbogen S, Heckmann C, Esser J, Morgenthaler NG (2006) Thyrotropin receptor autoantibodies are independent risk factors for Graves’ ophthalmopathy and help to predict severity and outcome of the disease. J Clin Endocrinol Metab 91(9):3464–3470. https://doi.org/10.1210/jc.2005-2813

    Article  PubMed  CAS  Google Scholar 

  29. McKeag D, Lane C, Lazarus JH, Baldeschi L, Boboridis K, Dickinson AJ, Hullo AI, Kahaly G, Krassas G, Marcocci C, Marinò M, Mourits MP, Nardi M, Neoh C, Orgiazzi J, Perros P, Pinchera A, Pitz S, Prummel MF, Sartini MS, Wiersinga WM (2007) Clinical features of dysthyroid optic neuropathy: a European group on graves’ orbitopathy (EUGOGO) survey. Br J Ophthalmol 91(4):455–458. https://doi.org/10.1136/bjo.2006.094607

    Article  PubMed  Google Scholar 

  30. Giaconi JA, Kazim M, Rho T, Pfaff C (2002) CT scan evidence of dysthyroid optic neuropathy. Ophthalmic Plast Reconstr Surg 18(3):177–182. https://doi.org/10.1097/00002341-200205000-00005

    Article  PubMed  Google Scholar 

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Acknowledgements

We dedicate this work to the memory of our co-author Ayşe İdil Çakmak, who we lost in the Hatay earthquake. In addition, we would like to thank Emre Dirican for helping us to prepare the statistics of our study.

Funding

None.

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Authors and Affiliations

Authors

Contributions

EG, AİÇ, GB helped in concept, analysis and/or interpretation and literature review; EG, AİÇ, GB, FÖK contributed to design, supervision, materials, critical review, data collection and/or processing; EG, AİÇ were involved in writing.

Corresponding author

Correspondence to Eren Gürkan.

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Authors declare no conflict of interests for this article.

Ethical approval

This study was initiated with the approval of the Hatay Mustafa Kemal University/School of Medicine Ethics Committee (01/08/2019–09). The principles of the Declaration of Helsinki were observed. Written informed consent was obtained from all participants.

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Gürkan, E., Çakmak, A.İ., Burakgazi, G. et al. Optical coherence tomography and shear wave elastography findings in Graves ophthalmopathy. Int Ophthalmol 44, 9 (2024). https://doi.org/10.1007/s10792-024-02931-2

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