Skip to main content
SpringerLink
Log in

Clinical characteristics and the treatment modalities of Graves’ orbitopathy in a tertiary referral center in Turkey: changes over two decades

  • Original Paper
  • Published:
International Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

To evaluate the changes in demographics, clinical findings, and treatment modalities in Graves’ orbitopathy (GO) patients at a tertiary referral center in Turkey over the last two decades.

Methods

The clinical data of 752 GO patients were evaluated retrospectively. Patients were divided into 2 groups according to the first ophthalmic examination date; Group 1(n:344) between January 1998 and December 2007 and Group 2(n:408) between January 2008 and December 2017.

Results

The number of nonsmokers was significantly higher in Group 2 (44.0 vs. 26.5%, p < 0.001). The time from the diagnosis of thyroid dysfunction and referral to our center was 32.4 months in Group 1 and 34.8 months in Group 2, (p = 0.166). The most common treatment of hyperthyroidism was antithyroid medications. Radioiodine ablation treatment rate was significantly lower in Group 2 (14.8 vs. 9.1%, p < 0.001). The time between the diagnosis of thyroid disease and orbital involvement was 22.0 vs. 26.6 months in Groups 1 and 2, respectively (p = 0.009). The time elapsed between the diagnosis of orbital disease and referral to our clinic was 21.0 months vs. 22.4 months in Group 1 and 2, respectively (p = 0.068). Orbital disease was most commonly mild, and inactive. Mild and moderate to severe GO and the mean Clinical Activity Score significantly increased, and the rate of sight-threatening disease and orbital decompression surgery significantly decreased in Group 2 (p = 0.042; p < 0.001, respectively).

Conclusions

Mild and inactive orbital disease was the most common form of GO. The severity of GO is declining over the last two decades in Turkey.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

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

    Article  PubMed  Google Scholar 

  2. Perros P, Neoh C, Dickinson J (2009) Thyroid eye disease. BMJ 338:b560. https://doi.org/10.1136/bmj.b560

    Article  PubMed  Google Scholar 

  3. Kahaly GJ (2020) Management of graves thyroidal and extrathyroidal disease: an update. J Clin Endocrinol Metab. https://doi.org/10.1210/clinem/dgaa646

    Article  PubMed  PubMed Central  Google Scholar 

  4. European Group of Graves O, Perros P, Baldeschi L, Boboridis K, Dickinson AJ, Hullo A, Kahaly GJ, Kendall-Taylor P, Krassas GE, Lane CM, Lazarus JH, Marcocci C, Marino M, Mourits MP, Nardi M, Orgiazzi J, Pinchera A, Pitz S, Prummel MF, Wiersinga WM (2006) A questionnaire survey on the management of Graves’ orbitopathy in Europe. Eur J Endocrinol 155(2):207–211. https://doi.org/10.1530/eje.1.02201

    Article  CAS  Google Scholar 

  5. Ippolito S, Cusini C, Lasalvia P, Gianfagna F, Veronesi G, Gallo D, Masiello E, Premoli P, Sabatino J, Mercuriali A, Lai A, Piantanida E, Tanda ML, Bartalena L (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(8):1707–1718. https://doi.org/10.1007/s40618-020-01479-z

    Article  CAS  PubMed  Google Scholar 

  6. Tanda ML, Piantanida E, Liparulo L, Veronesi G, Lai A, Sassi L, Pariani N, Gallo D, Azzolini C, Ferrario M, Bartalena L (2013) Prevalence and natural history of Graves’ orbitopathy in a large series of patients with newly diagnosed graves’ hyperthyroidism seen at a single center. J Clin Endocrinol Metab 98(4):1443–1449. https://doi.org/10.1210/jc.2012-3873

    Article  CAS  PubMed  Google Scholar 

  7. Perros P, Zarkovic M, Azzolini C, Ayvaz G, Baldeschi L, Bartalena L, Boschi A, Bournaud C, Brix TH, Covelli D, Ciric S, Daumerie C, Eckstein A, Fichter N, Fuhrer D, Hegedus L, Kahaly GJ, Konuk O, Lareida J, Lazarus J, Leo M, Mathiopoulou L, Menconi F, Morris D, Okosieme O, Orgiazzi J, Pitz S, Salvi M, Vardanian-Vartin C, Wiersinga W, Bernard M, Clarke L, Curro N, Dayan C, Dickinson J, Knezevic M, Lane C, Marcocci C, Marino M, Moller L, Nardi M, Neoh C, Pearce S, von Arx G, Toruner FB (2015) PREGO (presentation of Graves’ orbitopathy) study: changes in referral patterns to European group on graves’ orbitopathy (EUGOGO) centres over the period from 2000 to 2012. Br J Ophthalmol 99(11):1531–1535. https://doi.org/10.1136/bjophthalmol-2015-306733

    Article  PubMed  Google Scholar 

  8. European Group on Graves O, 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  CAS  Google Scholar 

  9. Mourits MP, Koornneef L, Wiersinga WM, Prummel MF, Berghout A, van der Gaag R (1989) Clinical criteria for the assessment of disease activity in Graves’ ophthalmopathy: a novel approach. Br J Ophthalmol 73(8):639–644. https://doi.org/10.1136/bjo.73.8.639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Bartalena L, Kahaly GJ, Baldeschi L, Dayan CM, Eckstein A, Marcocci C, Marino M, Vaidya B, Wiersinga WM, dagger E, (2021) The 2021 European group on graves’ orbitopathy (EUGOGO) clinical practice guidelines for the medical management of Graves’ orbitopathy. Eur J Endocrinol 185(4):G43–G67. https://doi.org/10.1530/EJE-21-0479

    Article  CAS  PubMed  Google Scholar 

  11. Laurberg P, Pedersen KM, Vestergaard H, Sigurdsson G (1991) High incidence of multinodular toxic goitre in the elderly population in a low iodine intake area vs. high incidence of Graves' disease in the young in a high iodine intake area: comparative surveys of thyrotoxicosis epidemiology in East-Jutland Denmark and Iceland. J Intern Med, 229 (5): 415–420. https://doi.org/10.1111/j.1365-2796.1991.tb00368.x

  12. Todd CH, Allain T, Gomo ZA, Hasler JA, Ndiweni M, Oken E (1995) Increase in thyrotoxicosis associated with iodine supplements in Zimbabwe. Lancet 346(8989):1563–1564. https://doi.org/10.1016/s0140-6736(95)92095-1

    Article  CAS  PubMed  Google Scholar 

  13. Taylor PN, Albrecht D, Scholz A, Gutierrez-Buey G, Lazarus JH, Dayan CM, Okosieme OE (2018) Global epidemiology of hyperthyroidism and hypothyroidism. Nat Rev Endocrinol 14(5):301–316. https://doi.org/10.1038/nrendo.2018.18

    Article  PubMed  Google Scholar 

  14. Wiersinga WM (2013) Smoking and thyroid. Clin Endocrinol (Oxf) 79(2):145–151. https://doi.org/10.1111/cen.12222

    Article  CAS  PubMed  Google Scholar 

  15. Eckstein A, Quadbeck B, Mueller G, Rettenmeier AW, Hoermann R, Mann K, Steuhl P, Esser J (2003) Impact of smoking on the response to treatment of thyroid associated ophthalmopathy. Br J Ophthalmol 87(6):773–776. https://doi.org/10.1136/bjo.87.6.773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Bartley GB, Fatourechi V, Kadrmas EF, Jacobsen SJ, Ilstrup DM, Garrity JA, Gorman CA (1996) Clinical features of Graves’ ophthalmopathy in an incidence cohort. Am J Ophthalmol 121(3):284–290. https://doi.org/10.1016/s0002-9394(14)70276-4

    Article  CAS  PubMed  Google Scholar 

  17. Khoo DH, Eng PH, Ho SC, Tai ES, Morgenthaler NG, Seah LL, Fong KS, Chee SP, Choo CT, Aw SE (2000) Graves’ ophthalmopathy in the absence of elevated free thyroxine and triiodothyronine levels: prevalence, natural history, and thyrotropin receptor antibody levels. Thyroid 10(12):1093–1100. https://doi.org/10.1089/thy.2000.10.1093

    Article  CAS  PubMed  Google Scholar 

  18. Marcocci C, Bartalena L, Bogazzi F, Panicucci M, Pinchera A (1989) Studies on the occurrence of ophthalmopathy in Graves’ disease. Acta Endocrinol (Copenh) 120(4):473–478. https://doi.org/10.1530/acta.0.1200473

    Article  CAS  PubMed  Google Scholar 

  19. Eckstein AK, Losch C, Glowacka D, Schott M, Mann K, Esser J, Morgenthaler NG (2009) Euthyroid and primarily hypothyroid patients develop milder and significantly more asymmetrical Graves ophthalmopathy. Br J Ophthalmol 93(8):1052–1056. https://doi.org/10.1136/bjo.2007.137265

    Article  CAS  PubMed  Google Scholar 

  20. Bartalena L, Burch HB, Burman KD, Kahaly GJ (2016) A 2013 European survey of clinical practice patterns in the management of Graves’ disease. Clin Endocrinol (Oxf) 84(1):115–120. https://doi.org/10.1111/cen.12688

    Article  CAS  PubMed  Google Scholar 

  21. Brito JP, Schilz S, Singh Ospina N, Rodriguez-Gutierrez R, Maraka S, Sangaralingham LR, Montori VM (2016) Antithyroid drugs-the most common treatment for graves’ disease in the United States: a nationwide population-based study. Thyroid 26(8):1144–1145. https://doi.org/10.1089/thy.2016.0222

    Article  PubMed  Google Scholar 

  22. Bartalena L, Baldeschi L, Boboridis K, Eckstein A, Kahaly GJ, Marcocci C, Perros P, Salvi M, Wiersinga WM, European Group on Graves O (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. https://doi.org/10.1159/000443828

    Article  CAS  Google Scholar 

  23. Ma C, Xie J, Wang H, Li J, Chen S (2016) Radioiodine therapy versus antithyroid medications for Graves' disease. Cochrane Database Syst Rev 2: CD010094. https://doi.org/10.1002/14651858.CD010094.pub2

  24. Tallstedt L, Lundell G, Torring O, Wallin G, Ljunggren JG, Blomgren H, Taube A (1992) Occurrence of ophthalmopathy after treatment for Graves’ hyperthyroidism. The thyroid study group. N Engl J Med 326(26):1733–1738. https://doi.org/10.1056/NEJM199206253262603

    Article  CAS  PubMed  Google Scholar 

  25. Li HX, Xiang N, Hu WK, Jiao XL (2016) Relation between therapy options for Graves’ disease and the course of Graves’ ophthalmopathy: a systematic review and meta-analysis. J Endocrinol Invest 39(11):1225–1233. https://doi.org/10.1007/s40618-016-0484-y

    Article  CAS  PubMed  Google Scholar 

  26. Daumerie C, Duprez T, Boschi A (2008) Long-term multidisciplinary follow-up of unilateral thyroid-associated orbitopathy. Eur J Intern Med 19(7):531–536. https://doi.org/10.1016/j.ejim.2008.01.013

    Article  PubMed  Google Scholar 

  27. Bartley GB (1994) The epidemiologic characteristics and clinical course of ophthalmopathy associated with autoimmune thyroid disease in Olmsted County, Minnesota. Trans Am Ophthalmol Soc 92:477–588

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Wiersinga WM, Bleumink M, Saeed P, Baldeschi L, Prummel MF (2008) Is sleeping position related to asymmetry in bilateral Graves’ ophthalmopathy? Thyroid 18(5):541–544. https://doi.org/10.1089/thy.2007.0302

    Article  PubMed  Google Scholar 

  29. Prummel MF, Bakker A, Wiersinga WM, Baldeschi L, Mourits MP, Kendall-Taylor P, Perros P, Neoh C, Dickinson AJ, Lazarus JH, Lane CM, Heufelder AE, Kahaly GJ, Pitz S, Orgiazzi J, Hullo A, Pinchera A, Marcocci C, Sartini MS, Rocchi R, Nardi M, Krassas GE, Halkias A (2003) Multi-center study on the characteristics and treatment strategies of patients with Graves’ orbitopathy: the first European Group on Graves’ Orbitopathy experience. Eur J Endocrinol 148(5):491–495. https://doi.org/10.1530/eje.0.1480491

    Article  CAS  PubMed  Google Scholar 

  30. Naik MN, Vasanthapuram VH (2021) Demographic and clinical profile of 1000 patients with thyroid eye disease presenting to a Tertiary Eye Care Institute in India. Int Ophthalmol 41(1):231–236. https://doi.org/10.1007/s10792-020-01571-6

    Article  PubMed  Google Scholar 

  31. Kahaly GJ (2017) Management of Moderately Severe Graves orbitopathy. In: Wiersinga WM Kahaly GJ eds. A Multidisciplinary Approach: Questions and Answers. 3rd edition (revised and expanded) . Karger, Basel, pp 140–176

Download references

Funding

This study was funded by the authors and did not receive any grant from finance agencies in the public or commercial sectors.

Author information

Authors and Affiliations

  1. Department of Ophthalmology, Haseki Training and Research Hospital, University of Health Sciences, Millet Street, 34096, Istanbul, Turkey

    Mine Ozturk

  2. Department of Ophthalmology, Faculty of Medicine, Gazi University, Ankara, Turkey

    Onur Konuk & Bercin Tarlan

  3. Department of Endocrinology and Metabolism, Faculty of Medicine, Gazi University, Ankara, Turkey

    Mehmet Muhittin Yalcın & Fusun Balos Toruner

  4. Department of Ophthalmology, Gaziantep Abdulkadir Yuksel State Hospital, Gaziantep, Turkey

    Yavuz Kemal Arıbas

  5. Ophthalmology, Private Practice, Ankara, Turkey

    Mehmet Unal

  6. Endocrinology and Metabolism, Private Practice, Ankara, Turkey

    Goksun Ayvaz

Authors
  1. Mine Ozturk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Onur Konuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bercin Tarlan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mehmet Muhittin Yalcın
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yavuz Kemal Arıbas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fusun Balos Toruner
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mehmet Unal
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Goksun Ayvaz
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Involved in design and conduct of the study (MO, OK, BT, MMY, YKA, FBT, MU, GA); preparation and review of the study (MO, OK, BT, MMY, YKA, FBT, MU, GA); data collection (MO, YKA); and statistical analysis (MO, YKA).

Corresponding author

Correspondence to Mine Ozturk.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The study was approved by the Institutional Review Board of Gazi University Faculty of Medicine and was conducted in accordance with the tenets of the Helsinki Declaration.

Informed consent

Informed consent was waived due to the retrospective nature of this study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ozturk, M., Konuk, O., Tarlan, B. et al. Clinical characteristics and the treatment modalities of Graves’ orbitopathy in a tertiary referral center in Turkey: changes over two decades. Int Ophthalmol 43, 643–653 (2023). https://doi.org/10.1007/s10792-022-02468-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10792-022-02468-2

Keywords

Search

Navigation