Understanding the clinical and molecular basis of thyroid orbitopathy: a review of recent evidence.
Biomarkers
EUGOGO guidelines
Graves’ disease
TED
TED review
Thyroid eye disease
Thyroid orbitopathy
VISA grading
Journal
Hormones (Athens, Greece)
ISSN: 2520-8721
Titre abrégé: Hormones (Athens)
Pays: Switzerland
ID NLM: 101142469
Informations de publication
Date de publication:
Mar 2024
Mar 2024
Historique:
received:
13
07
2023
accepted:
10
10
2023
medline:
8
2
2024
pubmed:
1
11
2023
entrez:
1
11
2023
Statut:
ppublish
Résumé
Thyroid eye disease (TED) is an autoimmune orbital inflammatory disease which ranges from mild to severe. Tissue remodeling, fibrosis and fat proliferation cause changes in the orbital tissues which can affect esthetics and visual function. In its severe form, it is sight threatening, debilitating, and disfiguring and may lead to social stigma, the embarrassment about which has an impact on the quality of life of those affected and the family members. The pathogenesis of TED, which is influenced by genetic, immunological, and environmental factors, is complex and not fully elucidated. However, it remains unknown what factors determine the severity of the disease. Recent research has revealed a number of diagnostic and prognostic biomarkers of this disease. In this overview of TED, we focus on new insights and perspectives regarding biological agents that may provide a basis for new treatment modalities.
Identifiants
pubmed: 37910311
doi: 10.1007/s42000-023-00498-8
pii: 10.1007/s42000-023-00498-8
pmc: PMC10847210
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
25-34Informations de copyright
© 2023. The Author(s).
Références
Simmonds MJ, Gough SC (2004) Unravelling the genetic complexity of autoimmune thyroid disease: HLA, CTLA-4 and beyond. Clin Exp Immunol 136(1):1–10
pubmed: 15030506
pmcid: 1808990
doi: 10.1111/j.1365-2249.2004.02424.x
Dayan CM, Daniels GH (1996) Chronic autoimmune thyroiditis. N Engl J Med 335(2):99–107
pubmed: 8649497
doi: 10.1056/NEJM199607113350206
Anaya JM, Castiblanco J, Rojas-Villarraga A, Pineda-Tamayo R, Levy RA, Gómez-Puerta J et al (2012) The multiple autoimmune syndromes. A clue for the autoimmune tautology. Clin Rev Allergy Immunol 43(3):256–264
Kumari R, Chandra SB (2018) Advances in the management of thyroid eye diseases: an overview. Int Ophthalmol 5:2247–2255
doi: 10.1007/s10792-017-0694-0
Bartley GB (2011) Rundle and his curve. Arch Ophthalmol 129(3):356–358
pubmed: 21402995
doi: 10.1001/archophthalmol.2011.29
Tanda ML, Piantanida E, Liparulo L, Veronesi G, Lai A, Sassi L et al (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
pubmed: 23408569
doi: 10.1210/jc.2012-3873
Bartley GB, Gorman CA (1995) Diagnostic criteria for Graves’ ophthalmopathy. Am J Ophthalmol 119(6):792–795
pubmed: 7785696
doi: 10.1016/S0002-9394(14)72787-4
Frueh BR (1984) Graves’ eye disease: orbital compliance and other physical measurements. Trans Am Ophthalmol Soc 82:492–598
pubmed: 6398935
pmcid: 1298676
Kendler DL, Lippa J, Rootman J (1993) The initial clinical characteristics of Graves’ orbitopathy vary with age and sex. Arch Ophthalmol 111(2):197–201
pubmed: 8431156
doi: 10.1001/archopht.1993.01090020051022
Tellez M, Cooper J, Edmonds C (1992) Graves’ ophthalmopathy in relation to cigarette smoking and ethnic origin. Clin Endocrinol 36(3):291–294
doi: 10.1111/j.1365-2265.1992.tb01445.x
Chin YH, Ng CH, Lee MH, Koh JWH, Kiew J, Yang SP et al (2020) Prevalence of thyroid eye disease in Graves’ disease: a meta-analysis and systematic review. Clin Endocrinol (Oxf) 93(4):363–374
pubmed: 32691849
doi: 10.1111/cen.14296
Muñoz-Ortiz J, Sierra-Cote MC, Zapata-Bravo E, Valenzuela-Vallejo L, Marin-Noriega MA, Uribe-Reina P et al (2020) Prevalence of hyperthyroidism, hypothyroidism, and euthyroidism in thyroid eye disease: a systematic review of the literature. Syst Rev 9(1):201
pubmed: 32873324
pmcid: 7465839
doi: 10.1186/s13643-020-01459-7
Douglas RS, Tsirbas A, Gordon M, Lee D, Khadavi N, Garneau HC et al (2009) Development of criteria for evaluating clinical response in thyroid eye disease using a modified Delphi technique. Arch Ophthalmol 127(9):1155–1160
pubmed: 19752424
pmcid: 4005726
doi: 10.1001/archophthalmol.2009.232
Mourits MP, Prummel MF, Wiersinga WM, Koornneef L (1997) Clinical activity score as a guide in the management of patients with Graves’ ophthalmopathy. Clin Endocrinol (Oxf) 47(1):9–14
pubmed: 9302365
doi: 10.1046/j.1365-2265.1997.2331047.x
Barrio-Barrio J, Sabater AL, Bonet-Farriol E, Velázquez-Villoria Á, Galofré JC (2015) Graves’ ophthalmopathy: VISA versus EUGOGO classification, assessment, and management. J Ophthalmol. https://doi.org/10.1155/2015/249125
Bartalena L, Kahaly GJ, Baldeschi L, Dayan CM, Eckstein A, Marcocci C et al (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
pubmed: 34297684
doi: 10.1530/EJE-21-0479
Terwee CB, Gerding MN, Dekker FW, Prummel MF, Wiersinga WM (1998) Development of a disease specific quality of life questionnaire for patients with Graves’ ophthalmopathy: the GO-QOL. BMJ Publishing Group, pp 773–779
Park JJ, Sullivan TJ, Mortimer RH, Wagenaar M, Perry-Keene DA (2004) Assessing quality of life in Australian patients with Graves’ ophthalmopathy. Br J Ophthalmol 88(1):75–78
pubmed: 14693779
pmcid: 1771927
doi: 10.1136/bjo.88.1.75
Delampady K, Reddy SVB, Yadav SB (2020) Assessing the quality of life in Indian Graves’ orbitopathy patients and validation of Hindi version of GO-QOL questionnaire. Indian J Ophthalmol 68(8):1617–1621
pubmed: 32709791
pmcid: 7640857
doi: 10.4103/ijo.IJO_2183_19
Lee TH, Sundar G (2020) Quality of life in thyroid eye disease: a systematic review. Ophthalmic Plast Reconstr Surg 36(2):118–126
pubmed: 31567783
doi: 10.1097/IOP.0000000000001446
Estcourt S, Quinn AG, Vaidya B (2011) Quality of life in thyroid eye disease: impact of quality of care. Eur J Endocrinol 164(5):649–655
pubmed: 21367964
doi: 10.1530/EJE-11-0055
Watt T, Cramon P, Hegedüs L, Bjorner JB, Bonnema SJ, Rasmussen ÅK et al (2014) The thyroid-related quality of life measure ThyPRO has good responsiveness and ability to detect relevant treatment effects. J Clin Endocrinol Metab 99(10):3708–3717
pubmed: 25004246
doi: 10.1210/jc.2014-1322
Effraimidis G, Badenhoop K, Tijssen JG, Wiersinga WM (2012) Vitamin D deficiency is not associated with early stages of thyroid autoimmunity. Eur J Endocrinol 167(1):43–48
pubmed: 22518050
doi: 10.1530/EJE-12-0048
Furmaniak J, Sanders J, Rees SB (2013) Blocking type TSH receptor antibodies. Auto Immun Highlights 4(1):11–26
pubmed: 26000138
doi: 10.1007/s13317-012-0028-1
Orgiazzi J (2012) Thyroid autoimmunity. La Presse Médicale 41(12, Part 2):e611–ee25
pubmed: 23164679
doi: 10.1016/j.lpm.2012.10.002
Tsui S, Naik V, Hoa N, Hwang CJ, Afifiyan NF, Sinha Hikim A, Gianoukakis AG, Douglas RS, Smith TJ et al (2008) Evidence for an association between thyroid-stimulating hormone and insulin-like growth factor 1 receptors: a tale of two antigens implicated in Graves’ disease. J Immunol:4397–4405
Rotondo Dottore G, Bucci I, Lanzolla G, Dallan I, Sframeli A, Torregrossa L et al (2021) Genetic profiling of orbital fibroblasts from patients with Graves’ orbitopathy. J Clin Endocrinol Metab 106(5):e2176–e2e90
pubmed: 33484567
doi: 10.1210/clinem/dgab035
Janssen J, Smith TJ (2021) Lessons learned from targeting IGF-I receptor in thyroid-associated ophthalmopathy. Cells 10(2):383
pubmed: 33673340
pmcid: 7917650
doi: 10.3390/cells10020383
Douglas RS, Kahaly GJ, Patel A, Sile S, Thompson EHZ, Perdok R et al (2020) Teprotumumab for the treatment of active thyroid eye disease. N Engl J Med 382(4):341–352
pubmed: 31971679
doi: 10.1056/NEJMoa1910434
Yamada T, Mishima T, Sakamoto M, Sugiyama M, Matsunaga S, Wada M (2006) Oxidation of myosin heavy chain and reduction in force production in hyperthyroid rat soleus. J Appl Physiol 100(5):1520–1526
pubmed: 16397059
doi: 10.1152/japplphysiol.01456.2005
Song Y, Driessens N, Costa M, De Deken X, Detours V, Corvilain B et al (2007) Roles of hydrogen peroxide in thyroid physiology and disease. J Clin Endocrinol Metab 92(10):3764–3773
pubmed: 17666482
doi: 10.1210/jc.2007-0660
Khandji J, Campbell AA, Callahan AB, Sirinek P, Kazim M (2018) IgG4-related orbital disease masquerading as thyroid eye disease, vice versa, or both? Orbit 37(4):239–242
pubmed: 29053038
doi: 10.1080/01676830.2017.1383478
Yin X, Latif R, Bahn R, Tomer Y, Davies TF (2008) Influence of the TSH receptor gene on susceptibility to Graves’ disease and Graves’ ophthalmopathy. Thyroid 18(11):1201–1206
pubmed: 18925838
pmcid: 2857451
doi: 10.1089/thy.2008.0098
Ting W-H, Chien M-N, Lo F-S, Wang C-H, Huang C-Y, Lin C-L et al (2016) Association of cytotoxic T-lymphocyte-associated protein 4 (CTLA4) gene polymorphisms with autoimmune thyroid disease in children and adults: case-control study. PLoS One 11(4):e0154394
pubmed: 27111218
pmcid: 4844099
doi: 10.1371/journal.pone.0154394
Zou H, Xu W, Wang Y, Wang Z (2021) A data-driven approach for the discovery of biomarkers associated with thyroid eye disease. BMC Ophthalmol 21(1):166
pubmed: 33832456
pmcid: 8034124
doi: 10.1186/s12886-021-01903-9
Wang Y, Ma X-M, Wang X, Sun X, Wang L-J, Li X-Q et al (2022) Emerging insights into the role of epigenetics and gut microbiome in the pathogenesis of Graves’ ophthalmopathy. Front Endocrinol 12:788535
doi: 10.3389/fendo.2021.788535
Stein JD, Childers D, Gupta S, Talwar N, Nan B, Lee BJ et al (2015) Risk factors for developing thyroid-associated ophthalmopathy among individuals with Graves’ disease. JAMA Ophthalmol 133(3):290–296
Wiersinga WM (2013) Smoking and thyroid 79(2):145–511
R J, J S. (2006) Serum TSH levels in smokers and non-smokers. The 5th Tromsø study. Exp Clin Endocrinol Diabetes 114(7):343–347
doi: 10.1055/s-2006-924264
Sawicka-Gutaj N, Gutaj P, Sowiński J, Wender-Ożegowska E, Czarnywojtek A, Brązert J et al (2014) Influence of cigarette smoking on thyroid gland--an update. Endokrynol Pol 65(1):54–62
pubmed: 24549603
doi: 10.5603/EP.2014.0008
Strieder TG, Prummel MF, Tijssen JG, Endert E, Wiersinga WM (2003) Risk factors for and prevalence of thyroid disorders in a cross-sectional study among healthy female relatives of patients with autoimmune thyroid disease. Clin Endocrinol (Oxf) 59(3):396–401
pubmed: 12919165
doi: 10.1046/j.1365-2265.2003.01862.x
Sadeghi-Tari A, Jamshidian-Tehrani M, Nabavi A, Sharif-Kashani S, Elhami E, Hassanpour N et al (2016) Effect of smoking on retrobulbar blood flow in thyroid eye disease. Eye (Lond) 30(12):1573–1578
pubmed: 27540833
doi: 10.1038/eye.2016.184
Pedersen IB, Knudsen N, Carlé A, Vejbjerg P, Jørgensen T, Perrild H et al (2011) A cautious iodization programme bringing iodine intake to a low recommended level is associated with an increase in the prevalence of thyroid autoantibodies in the population. Clin Endocrinol (Oxf) 75(1):120–126
pubmed: 21521277
doi: 10.1111/j.1365-2265.2011.04008.x
Sadaka A, Nguyen K, Malik A, Brito R, Berry S, Lee AG (2019) Vitamin D and selenium in a thyroid eye disease population in Texas. Neuroophthalmology 43(5):291–294
pubmed: 31741672
pmcid: 6844498
doi: 10.1080/01658107.2019.1566382
Mackawy AM, Al-Ayed BM, Al-Rashidi BM (2013) Vitamin D deficiency and its association with thyroid disease. Int J Health Sci (Qassim) 7(3):267–275
Lanzolla G, Marinò M, Marcocci C (2021) Selenium in the treatment of Graves’ hyperthyroidism and eye disease. Front Endocrinol 26(11):608428
Khong JJ, Goldstein RF, Sanders KM, Schneider H, Pope J, Burdon KP et al (2014) Serum selenium status in Graves’ disease with and without orbitopathy: a case-control study. Clin Endocrinol (Oxf) 80(6):905–910
Bullen J, Griffiths E, Rogers H, Ward G (2021) Sepsis: the critical role of iron. Microbes Infect 2(4):409–415
doi: 10.1016/S1286-4579(00)00326-9
Knezevic J, Starchl C, Tmava Berisha A, Amrein K (2020) Thyroid-gut-axis: how does the microbiota influence thyroid function? Nutrients 12(6):1769
pubmed: 32545596
pmcid: 7353203
doi: 10.3390/nu12061769
Caturegli P, De Remigis A, Rose NR (2014) Hashimoto thyroiditis: clinical and diagnostic criteria. Autoimmun Rev 13(4–5):391–397
Covelli D, Ludgate M (2017) The thyroid, the eyes and the gut: a possible connection. J Endocrinol Invest 40(6):567–576
pubmed: 28063079
doi: 10.1007/s40618-016-0594-6
Betsy A, Binitha M, Sarita S (2013) Zinc deficiency associated with hypothyroidism: an overlooked cause of severe alopecia. Int J Trichology 5(1):40–42
pubmed: 23960398
pmcid: 3746228
doi: 10.4103/0974-7753.114714
Khanam S (2018) Impact of zinc on thyroid metabolism. J Diabetes Metab Disord Control 5:27–28
doi: 10.15406/jdmdc.2018.05.00134
Sabini E, Mazzi B, Profilo MA, Mautone T, Casini G, Rocchi R et al (2018) High serum cholesterol is a novel risk factor for Graves’ orbitopathy: results of a cross-sectional study. Thyroid 28(3):386–394
pubmed: 29336220
doi: 10.1089/thy.2017.0430
Nilsson A, Tsoumani K, Planck T (2021) Statins decrease the risk of orbitopathy in newly diagnosed patients with Graves’ disease. J Clin Endocrinol Metab 106(5):1325–1332
pubmed: 33560351
doi: 10.1210/clinem/dgab070
Ahmadieh H, Salti I (2013) Tyrosine kinase inhibitors induced thyroid dysfunction: a review of its incidence, pathophysiology, clinical relevance, and treatment. Biomed Res Int 725410. https://doi.org/10.1155/2013/725410
Hamada Y, Sato A, Motojima S (2017) Pulmonary tuberculosis and tuberculous pleurisy complicated with rifampicin-induced hypothyroidism: a case report. Kekkaku:[Tuberculosis] 92(1):41–45
pubmed: 30646472
Loh KC (2000) Amiodarone-induced thyroid disorders: a clinical review. Postgrad Med J 76(893):133–140
pubmed: 10684321
pmcid: 1741517
doi: 10.1136/pmj.76.893.133
Ross DS, Burch HB, Cooper DS, Greenlee MC, Laurberg P, Maia AL et al (2016) 2016 American thyroid association guidelines for diagnosis and management of hyperthyroidism and other causes of thyrotoxicosis. Thyroid 26(10):1343–1421
pubmed: 27521067
doi: 10.1089/thy.2016.0229
Burch HB, Cooper DS (2018) Anniversary review: Antithyroid drug therapy: 70 years later. Eur J Endocrinol 179(5):R261–Rr74
pubmed: 30320502
doi: 10.1530/EJE-18-0678
Nirmalan A, Blecher N, Hyder S, Couch SM, Godfrey KJ, Stan MN et al (2023) Alemtuzumab-induced thyroid eye disease: a comprehensive case series and review of the literature. Ophthalmic Plast Reconstr Surg 39(5):470–474
pubmed: 36893061
doi: 10.1097/IOP.0000000000002367
Ashkar C, Sztal-Mazer S, Topliss DJ (2023) How to manage Graves’ disease in women of childbearing potential. Clin Endocrinol (Oxf) 98(5):643–648
pubmed: 35192205
doi: 10.1111/cen.14705
Hoang TD, Stocker DJ, Chou EL, Burch HB (2022) Update on clinical management of Graves’ disease and thyroid eye disease. Endocrinol Metab Clin North Am 51(2):287–304
pubmed: 35662442
pmcid: 9174594
doi: 10.1016/j.ecl.2021.12.004
Wong Y, Dickinson J, Perros P, Dayan C, Veeramani P, Morris D et al (2018) A British Ophthalmological Surveillance Unit (BOSU) study into dysthyroid optic neuropathy in the United Kingdom. Eye (Lond) 32(10):1555–1562
pubmed: 29915191
doi: 10.1038/s41433-018-0144-x
Bagheri A, Abbaszadeh M, Yazdani S (2020) Intraorbital steroid injection for active thyroid ophthalmopathy. J Ophthalmic Vis Res 15(1):69–77
pubmed: 32095211
pmcid: 7001014
Goldberg RA (2004) Orbital steroid injections. Br J Ophthalmol 88(11):1359–1360
pubmed: 15489472
pmcid: 1772387
doi: 10.1136/bjo.2004.051755
Ginter A, Migliori ME (2016) The role of biological agents and immunomodulators in treatment strategies for thyroid eye disease: an evidence-based review. R I Med J 99(6):26–29
Ostrowski RA, Bussey MR, Shayesteh Y, Jay WM (2015) Rituximab in the treatment of thyroid eye disease: a review. Neuroophthalmology 39(3):109–115
pubmed: 27928343
pmcid: 5123122
doi: 10.3109/01658107.2015.1039140
Stan MN, Garrity JA, Carranza Leon BG, Prabin T, Bradley EA, Bahn RS (2015) Randomized controlled trial of rituximab in patients with Graves’ orbitopathy. J Clin Endocrinol Metab 100(2):432–441
pubmed: 25343233
doi: 10.1210/jc.2014-2572
Salvi M, Vannucchi G, Currò N, Campi I, Covelli D, Dazzi D et al (2015) Efficacy of B-cell targeted therapy with rituximab in patients with active moderate to severe Graves’ orbitopathy: a randomized controlled study. J Clin Endocrinol Metab 100(2):422–431
pubmed: 25494967
doi: 10.1210/jc.2014-3014
Shen WC, Lee CH, Loh EW, Hsieh AT, Chen L, Tam KW (2018) Efficacy and safety of rituximab for the treatment of Graves’ orbitopathy: a meta-analysis of randomized controlled trials. Pharmacotherapy 38(5):503–510
pubmed: 29601105
doi: 10.1002/phar.2111
Smith TJ, Janssen J (2019) Insulin-like growth factor-I receptor and thyroid-associated ophthalmopathy. Endocr Rev 40(1):236–267
pubmed: 30215690
doi: 10.1210/er.2018-00066
Smith TJ, Kahaly GJ, Ezra DG, Fleming JC, Dailey RA, Tang RA et al (2017) Teprotumumab for thyroid-associated ophthalmopathy. N Engl J Med 376(18):1748–1761
pubmed: 28467880
pmcid: 5718164
doi: 10.1056/NEJMoa1614949
Hoang TD, Nguyen NT, Chou E, Shakir MK (2021) Rapidly progressive cognitive decline associated with teprotumumab in thyroid eye disease. BMJ Case Rep 10;14(5):e242153
Paridaens D, van den Bosch WA, van der Loos TL, Krenning EP, van Hagen PM (2005) The effect of etanercept on Graves’ ophthalmopathy: a pilot study. Eye (Lond) 19(12):1286–1289
pubmed: 15550932
doi: 10.1038/sj.eye.6701768
Ayabe R, Rootman D, Hwang C, Artzi A, Goldberg R (2014) Adalimumab as steroid-sparing treatment of inflammatory-stage thyroid eye disease. Ophthalmic Plast Reconstr Surg 30(5):415–419
pubmed: 24978425
doi: 10.1097/IOP.0000000000000211
Karim AF, Bansie RD, Rombach SM, Paridaens D, Verdijk RM, van Hagen PM et al (2018) The treatment outcomes in IgG4-related disease. Neth J Med 76(6):275–285
pubmed: 30152392
Virakul S, Dalm VA, Paridaens D, van den Bosch WA, Hirankarn N, van Hagen PM et al (2014) The tyrosine kinase inhibitor dasatinib effectively blocks PDGF-induced orbital fibroblast activation. Graefes Arch Clin Exp Ophthalmol 252(7):1101–1109
pubmed: 24874745
doi: 10.1007/s00417-014-2674-7
Boboridis KG, Bunce C (2011) Surgical orbital decompression for thyroid eye disease. Cochr Database Syst Rev 7(12):CD007630. https://doi.org/10.1002/14651858.CD007630