Review of European Thyroid Association Guideline (2018) for the Management of Graves’ Hyperthyroidism
https://doi.org/10.14341/ket12474
Abstract
Graves’ disease (GD) is a systemic autoimmune disorder characterized by the infiltration of thyroid antigen-specific T-cells into thyroid-stimulating hormone receptor (TSH-R)-expressing tissues. Stimulatory autoantibodies (Ab) in GD activate the TSH-R leading to thyroid hyperplasia and unregulated thyroid hormone production and secretion. Diagnosis of GD is straightforward in a patient with biochemically confirmed thyrotoxicosis, positive TSH-R-Ab, a hypervascular and hypoechoic thyroid gland (ultrasound), and associated orbitopathy. In GD, measurement of TSH-R-Ab is recommended for an accurate diagnosis/differential diagnosis, prior to stopping antithyroid drug (ATD) treatment and during pregnancy. Graves’ hyperthyroidism is treated by decreasing thyroid hormone synthesis with the use of ATD, or by reducing the amount of thyroid tissue with radioactive iodine (RAI) treatment or total thyroidectomy. Patients with newly diagnosed Graves’ hyperthyroidism are usually medically treated for 12–18 months with methimazole (MMI) as the preferred drug. In children with GD, a 24- to 36-month course of MMI is recommended. Patients with persistently high TSH-R-Ab at 12–18 months can continue MMI treatment, repeating the TSH-R-Ab measurement after an additional 12 months, or opt for therapy with RAI or thyroidectomy. Women treated with MMI should be switched to propylthiouracil when planning pregnancy and during the first trimester of pregnancy. If a patient relapses after completing a course of ATD, definitive treatment is recommended; however, continued long-term low-dose MMI can be considered. Thyroidectomy should be performed by an experienced high-volume thyroid surgeon. RAI is contraindicated in Graves’ patients with active/severe orbitopathy, and steroid prophylaxis is warranted in Graves’ patients with mild/active orbitopathy receiving RAI.
About the Author
V. V. Fadeyev
http://www.vfadeyev.com/
I.M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation
I.M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation
Valentin V. Fadeyev, MD, PhD, Professor; eLibrary SPIN: 6825-8417.
1-1 Pogodinskaya street. 119992 Moscow, Russia
References
1. Bahn RS, Burch HB, Cooper DS, et al. Hyperthyroidism and other causes of thyrotoxicosis: management guidelines of the American Thyroid Association and American Association of Clinical Endocrinologists. Endocr Pract. 2011;17(3):456–520. Doi: 10.4158/ep.17.3.456.
2. Bartalena L. Diagnosis and management of Graves’ disease: a global overview. Nat Rev Endocrinol. 2013;9(12):724–734. Doi: 10.1038/nrendo.2013.193.
3. Kahaly GJ, Dillmann WH. Thyroid hormone action in the heart. Endocr Rev. 2005;26(5):704–728. Doi: 10.1210/er.2003-0033.
4. Biondi B, Kahaly GJ. Cardiovascular involvement in patients with different causes of hy-perthyroidism. Nat Rev Endocrinol. 2010;6(8):431–443. Doi: 10.1038/nrendo.2010.105.
5. Ross DS, Burch HB, Cooper DS, et al. 2016 American Thyroid Association guidelines for diagnosis and management of hyperthyroidism and other causes of thyrotoxicosis. Thyroid. 2016;26(10):1343–1421. Doi: 10.1089/thy.2016.0229.
6. Smith TJ, Hegedus L. Graves’ disease. N Engl J Med. 2016;375(16):1552–1565. Doi: 10.1056/NEJMra1510030.
7. Nystrom HF, Jansson S, Berg G. Incidence rate and clinical features of hyperthyroidism in a long-term iodine sufficient area of Sweden (Gothenburg) 2003–2005. Clin Endocrinol. 2013;78(5):768–776. Doi: 10.1111/cen.12060.
8. McLeod DS, Caturegli P, Cooper DS, et al. Variation in rates of autoimmune thyroid disease by race/ethnicity in US military personnel. JAMA. 2014;311(15):1563–1565. Doi: 10.1001/jama.2013.285606.
9. Rapoport B, Chazenbalk GD, Jaume JC, McLachlan SM. The thyrotropin (TSH) receptor: interaction with TSH and autoantibodies. Endocr Rev. 1998;19(6):673–716. Doi: 10.1210/edrv.19.6.0352.
10. Rapoport B, McLachlan SM. TSH receptor cleavage into subunits and shedding of the A-subunit; a molecular and clinical perspective. Endocr Rev. 2016;37(2):114–134. Doi: 10.1210/er.2015-1098.
11. Smith TJ, Hegedus L, Douglas RS. Role of insulin-like growth factor-1 (IGF-1) pathway in the pathogenesis of Graves’ orbitopathy. Best Pract Res Clin Endocrinol Metab. 2012;26(3):291–302. Doi: 10.1016/j.beem.2011.10.002.
12. Brix TH, Kyvik KO, Christensen K, Hegedus L. Evidence for a major role of heredity in Graves’ disease: a population-based study of two Danish twin cohorts. J Clin Endocrinol Metab. 2001;86(2):930–934. Doi: 10.1210/jcem.86.2.7242.
13. Inaba H, De Groot LJ, Akamizu T. Thyrotropin receptor epitope and human leukocyte anti-gen in Graves’ disease. Front Endocrinol (Lausanne). 2016;7:120. Doi: 10.3389/fendo.2016.00120.
14. Lee HJ, Li CW, Hammerstad SS, et al. Immunogenetics of autoimmune thyroid diseases: a comprehensive review. J Autoimmun. 2015;64:82–90. Doi: 10.1016/j.jaut.2015.07.009.
15. Strieder TG, Prummel MF, Tijssen JG, et al. Risk factors for and prevalence of thyroid dis-orders in a cross-sectional study among healthy female relatives of patients with autoim-mune thyroid disease. Clin Endocrinol (Oxf). 2003;59(3):396–401. Doi: 10.1046/j.1365-2265.2003.01862.x.
16. Laurberg P, Pedersen KM, Vestergaard H, Sigurdsson G. 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 thyrotox-icosis epidemiology in East-Jutland Denmark and Iceland. J Intern Med. 1991;229(5):415–420. Doi: 10.1111/j.1365-2796.1991.tb00368.x.
17. Brix TH, Hansen PS, Kyvik KO, Hegedus L. Cigarette smoking and risk of clinically overt thyroid disease: a population-based twin case-control study. Arch Intern Med. 2000;160(5):661–666. Doi: 10.1001/archinte.160.5.661.
18. Swiglo BA, Murad MH, Schunemann HJ, et al. A case for clarity, consistency, and helpful-ness: state-of-the-art clinical practice guidelines in endocrinology using the grading of rec-ommendations, assessment, development, and evaluation system. J Clin Endocrinol Metab. 2008;93(3):666–673. Doi: 10.1210/jc.2007-1907.
19. de los Santos ET, Starich GH, Mazzaferri EL. Sensitivity, specificity, and cost-effectiveness of the sensitive thyrotropin assay in the diagnosis of thyroid disease in ambulatory patients. Arch Intern Med. 1989;149(3):526–532. Doi: 10.1001/archinte.149.3.526.
20. Spencer CA, LoPresti JS, Patel A, et al. Applications of a new chemiluminometric thyrotro-pin assay to subnormal measurement. J Clin Endocrinol Metab. 1990;70(2):453–460. Doi: 10.1210/jcem-70-2-453.
21. Grebe SK, Kahaly GJ. Laboratory testing in hyperthyroidism. Am J Med. 2012;125(9):S2. Doi: 10.1016/j.amjmed.2012.05.013.
22. Bartalena L, Burch HB, Burman KD, Kahaly GJ. A 2013 European survey of clinical prac-tice patterns in the management of Graves’ disease. Clin Endocrinol. 2016;84(1):115–120. Doi: 10.1111/cen.12688.
23. Kahaly GJ, Olivo PD. Graves’ disease. N Engl J Med. 2017;376(2):184. Doi: 10.1056/NEJMc1614624.
24. Kahaly GJ, Diana T. TSH receptor antibody functionality and nomenclature. Front Endocrinol (Lausanne). 2017;8:28. Doi: 10.3389/fendo.2017.00028.
25. Tozzoli R, Bagnasco M, Giavarina D, Bizzaro N. TSH receptor autoantibody immunoassay in patients with Graves’ disease: improvement of diagnostic accuracy over different genera-tions of methods: systematic review and meta-analysis. Autoimmun Rev. 2012;12(2):107–113. Doi: 10.1016/j.autrev.2012.07.003.
26. Kahaly GJ. Bioassays for TSH receptor antibodies: quo vadis? Eur Thyroid J. 2015;4(1):3–5. Doi: 10.1159/000375445.
27. Araki N, Iida M, Amino N, et al. Rapid bioassay for detection of thyroid-stimulating anti-bodies using cyclic adenosine monophosphate-gated calcium channel and aequorin. Eur Thyroid J. 2015;4(1):14–19. Doi: 10.1159/000371740.
28. Lytton SD, Kahaly GJ. Bioassays for TSH-receptor autoantibodies: an update. Autoimmun Rev. 2010;10(2):116–122. Doi: 10.1016/j.autrev.2010.08.018.
29. Lytton SD, Li Y, Olivo PD, et al. Novel chimeric thyroid-stimulating hormone-receptor bio-assay for thyroid-stimulating immunoglobulins. Clin Exp Immunol. 2010;162(3):438–446. Doi: 10.1111/j.1365-2249.2010.04266.x.
30. Li Y, Kim J, Diana T, et al. A novel bioassay for anti-thyrotrophin receptor autoantibodies detects both thyroid-blocking and stimulating activity. Clin Exp Immunol. 2013;173(3):390–397. Doi: 10.1111/cei.12129.
31. Diana T, Kanitz M, Lehmann M, et al. Standardization of a bioassay for thyrotropin recep-tor stimulating autoantibodies. Thyroid. 2015;25(2):169–175. Doi: 10.1089/thy.2014.0346.
32. Diana T, Li Y, Olivo PD, et al. Analytical performance and validation of a bioassay for thy-roidblocking antibodies. Thyroid. 2016;26(5):734–740. Doi: 10.1089/thy.2015.0447.
33. Diana T, Krause J, Olivo PD, et al. Prevalence and clinical relevance of thyroid stimulating hormone receptor-blocking antibodies in autoimmune thyroid disease. Clin Exp Immunol. 2017;189(3):304–309. Doi: 10.1111/cei.12980.
34. Diana T, Wuster C, Kanitz M, Kahaly GJ. Highly variable sensitivity of five binding and two bio-assays for TSH-receptor antibodies. J Endocrinol Invest. 2016;39(10):1159–1165. Doi: 10.1007/s40618-016-0478-9.
35. Diana T, Wüster C, Olivo PD, et al. Performance and specificity of six immunoassays for TSH receptor antibodies: a multicenter study. Eur Thyroid J. 2017;6(5):243–249. Doi: 10.1159/000478522.
36. Lytton SD, Ponto KA, Kanitz M, et al. A novel thyroid stimulating immunoglobulin bioas-say is a functional indicator of activity and severity of Graves’ orbitopathy. J Clin Endocrinol Metab. 2010;95(5):2123–2131. Doi: 10.1210/jc.2009-2470.
37. Ponto KA, Kanitz M, Olivo PD, et al. Clinical relevance of thyroidstimulating immunoglob-ulins in graves’ ophthalmopathy. Ophthalmology. 2011;118(11):2279–2285. Doi: 10.1016/j.ophtha.2011.03.030.
38. Ponto KA, Diana T, Binder H, et al. Thyroid-stimulating immunoglobulins indicate the on-set of dysthyroid optic neuropathy. J Endocrinol Invest. 2015;38(7):769–777. Doi: 10.1007/s40618-015-0254-2.
39. Kahaly GJ, Diana T, Glang J, et al. Thyroid stimulating antibodies are highly prevalent in Hashimoto’s thyroiditis and associated orbitopathy. J Clin Endocrinol Metab. 2016;101(5):1998–2004. Doi: 10.1210/jc.2016-1220.
40. Diana T, Brown RS, Bossowski A, et al. Clinical relevance of thyroid-stimulating autoanti-bodies in pediatric Graves’ disease – a multicenter study. J Clin Endocrinol Metab. 2014;99(5):1648–1655. Doi: 10.1210/jc.2013-4026.
41. Kampmann E, Diana T, Kanitz M, et al. Thyroid stimulating but not blocking autoantibodies are highly prevalent in severe and active thyroid-associated orbitopathy: a prospective study. Int J Endocrinol. 2015;2015:678194. Doi: 10.1155/2015/678194.
42. Stozek K, Bossowski A, Ziora K, et al. Functional TSH receptor antibodies in children with autoimmune thyroid diseases. Autoimmunity. 2018;51(2):62–68. Doi: 10.1080/08916934.2018.1431776.
43. Kiefer FW, Klebermass-Schrehof K, Steiner M, et al. Fetal/neonatal thyrotoxicosis in a newborn from a hypothyroid woman with Hashimoto thyroiditis. J Clin Endocrinol Metab. 2017;102(1):6–9. Doi: 10.1210/jc.2016-2999.
44. Mestman JH. Fetal hyperthyroidism resulted from TSI in a mother with Hashimoto’s hypo-thyroidism. Clin Thyroidol. 2017;29(1):32–34. Doi: 10.1089/ct.2017;29.32-34.
45. McKee A, Peyerl F. TSI assay utilization: impact on costs of Graves’ hyperthyroidism diag-nosis. Am J Manag Care. 2012;18(1):e1–14.
46. Goichot B, Bouee S, Castello-Bridoux C, Caron P. Survey of clinical practice patterns in the management of 992 hyperthyroid patients in France. Eur Thyroid J. 2017;6(3):152–159. Doi: 10.1159/000453260.
47. Kahaly GJ, Bartalena L, Hegedus L. The American Thyroid Association/American Associa-tion of Clinical Endocrinologists guidelines for hyperthyroidism and other causes of thyro-toxicosis: a European perspective. Thyroid. 2011;21(6):585–591. Doi: 10.1089/thy.2011.2106.ed3.
48. Hegedus L. Thyroid ultrasound. Endocrinol Metab Clin North Am. 2001;30(2):339–360. Doi: 10.1016/s0889-8529(05)70190-0.
49. Vitti P, Rago T, Mancusi F, et al. Thyroid hypoechogenic pattern at ultrasonography as a tool for predicting recurrence of hyperthyroidism after medical treatment in patients with Graves’ disease. Acta Endocrinol (Copenh). 1992;126(2):128–131. Doi: 10.1530/acta.0.1260128.
50. Erdogan MF, Anil C, Cesur M, et al. Color flow Doppler sonography for the etiologic diag-nosis of hyperthyroidism. Thyroid. 2007;17(3):223–228. Doi: 10.1089/thy.2006.0104.
51. Ralls PW, Mayekawa DS, Lee KP, et al. Color-flow Doppler sonography in Graves’ disease: “thyroid inferno”. AJR Am J Roentgenol. 1988;150(4):781–784. Doi: 10.2214/ajr.150.4.781.
52. Kim TK, Lee EJ. The value of the mean peak systolic velocity of the superior thyroidal ar-tery in the differential diagnosis of thyrotoxicosis. Ultrasonography. 2015;34(4):292–296. Doi: 10.14366/usg.14059.
53. Emiliano AB, Governale L, Parks M, Cooper DS. Shifts in propylthiouracil and methima-zole prescribing practices: antithyroid drug use in the United States from 1991 to 2008. J Clin Endocrinol Metab. 2010;95(5):2227–2233. Doi: 10.1210/jc.2009-2752.
54. Brito JP, Schilz S, Singh Ospina N, et al. Antithyroid drugs – the most common treatment for Graves’ disease in the United States: a nationwide population-based study. Thyroid. 2016;26(8):1144–1145. Doi: 10.1089/thy.2016.0222.
55. Cooper DS. Antithyroid drugs in the management of patients with Graves’ disease: an evi-dence-based approach to therapeutic controversies. J Clin Endocrinol Metab. 2003;88(8):3474–3481. Doi: 10.1210/jc.2003-030185.
56. Cooper DS. Antithyroid drugs. N Engl J Med. 2005;352(9):905–917. Doi: 10.1056/NEJMra042972.
57. Abraham P, Avenell A, McGeoch SC, et al. Antithyroid drug regimen for treating Graves’ hyperthyroidism. Cochrane Database Syst Rev. 2010;2010:CD003420. Doi: 10.1002/14651858.CD003420.pub4.
58. Leschik JJ, Diana T, Olivo PD, et al. Analytical performance and clinical utility of a bioas-say for thyroid-stimulating immunoglobulins. Am J Clin Pathol. 2013;139(2):192–200. Doi: 10.1309/AJCPZUT7CNUEU7OP.
59. Giuliani C, Cerrone D, Harii N, et al. A TSHR-LH/CGR chimera that measures functional thyroid-stimulating autoantibodies (TSAb) can predict remission or recurrence in Graves’ patients undergoing antithyroid drug (ATD) treatment. J Clin Endocrinol Metab. 2012;97(7):E1080–E1087. Doi: 10.1210/jc.2011-2897.
60. Laurberg P, Berman DC, Andersen S, Bulow Pedersen I. Sustained control of Graves’ hy-perthyroidism during long-term low-dose antithyroid drug therapy of patients with severe Graves’ orbitopathy. Thyroid. 2011;21(9):951–956. Doi: 10.1089/thy.2011.0039.
61. Elbers L, Mourits M, Wiersinga W. Outcome of very long-term treatment with antithyroid drugs in Graves’ hyperthyroidism associated with Graves’ orbitopathy. Thyroid. 2011;21(3):279–283. Doi: 10.1089/thy.2010.0181.
62. Leger J, Carel JC. Management of endocrine disease: arguments for the prolonged use of antithyroid drugs in children with Graves’ disease. Eur J Endocrinol. 2017;177(2):R59-R67. Doi: 10.1530/EJE-16-0938.
63. Pearce SH. Spontaneous reporting of adverse reactions to carbimazole and propylthiouracil in the UK. Clin Endocrinol (Oxf). 2004;61(5):589–594. Doi: 10.1111/j.1365-2265.2004.02135.x.
64. Yang J, Zhu YJ, Zhong JJ, et al. Characteristics of antithyroid drug-induced agranulocytosis in patients with hyperthyroidism: a retrospective analysis of 114 cases in a single institution in China involving 9690 patients referred for radioiodine treatment over 15 years. Thyroid. 2016;26(5):627–633. Doi: 10.1089/thy.2015.0439.
65. Nakamura H, Miyauchi A, Miyawaki N, Imagawa J. Analysis of 754 cases of antithyroid drug-induced agranulocytosis over 30 years in Japan. J Clin Endocrinol Metab. 2013;98(12):4776–4783. Doi: 10.1210/jc.2013-2569.
66. Watanabe N, Narimatsu H, Noh JY, et al. Antithyroid drug-induced hematopoietic damage: a retrospective cohort study of agranulocytosis and pancytopenia involving 50,385 patients with Graves’ disease. J Clin Endocrinol Metab. 2012;97(1):E49–E53. Doi: 10.1210/jc.2011-2221.
67. Chen PL, Shih SR, Wang PW, et al. Genetic determinants of antithyroid drug-induced agranulocytosis by human leukocyte antigen genotyping and genome-wide association study. Nat Commun. 2015;6:7633. Doi: 10.1038/ncomms8633.
68. Hallberg P, Eriksson N, Ibanez L, et al. Genetic variants associated with antithyroid drug-induced agranulocytosis: a genome-wide association study in a European population. Lancet Diabetes Endocrinol. 2016;4(6):507–516. Doi: 10.1016/S2213-8587(16)00113-3.
69. Plantinga TS, Arts P, Knarren GH, et al. Rare NOX3 variants confer susceptibility to agranulocytosis during thyrostatic treatment of Graves’ disease. Clin Pharmacol Ther. 2017;102(6):1017–1024. Doi: 10.1002/cpt.733.
70. Rivkees SA, Mattison DR. Ending propylthiouracil-induced liver failure in children. N Engl J Med. 2009;360(15):1574–1575. Doi: 10.1056/NEJMc0809750.
71. Wang MT, Lee WJ, Huang TY, et al. Antithyroid drug-related hepatotoxicity in hyperthy-roidism patients: a population-based cohort study. Br J Clin Pharmacol. 2014;78(3):619–629. Doi: 10.1111/bcp.12336.
72. Castro MR, Espiritu RP, Bahn RS, et al. Predictors of malignancy in patients with cytologi-cally suspicious thyroid nodules. Thyroid. 2011;21(11):1191–1198. Doi: 10.1089/thy.2011.0146.
73. Sundaresh V, Brito JP, Wang Z, et al. Comparative effectiveness of therapies for Graves’ hyperthyroidism: a systematic review and network meta-analysis. J Clin Endocrinol Metab. 2013;98(9):3671–3677. Doi: 10.1210/jc.2013-1954.
74. Struja T, Fehlberg H, Kutz A, et al. Can we predict relapse in Graves’ disease? Results from a systematic review and meta-analysis. Eur J Endocrinol. 2017;176(1):87–97. Doi: 10.1530/EJE-16-0725.
75. Vos XG, Endert E, Zwinderman AH, et al. Predicting the risk of recurrence before the start of antithyroid drug therapy in patients with Graves’ hyperthyroidism. J Clin Endocrinol Metab. 2016;101(4):1381–1389. Doi: 10.1210/jc.2015-3644.
76. Villagelin D, Romaldini JH, Santos RB, et al. Outcomes in relapsed Graves’ disease patients following radioiodine or prolonged low dose of methimazole treatment. Thyroid. 2015;25(12):1282–1290. Doi: 10.1089/thy.2015.0195.
77. Azizi F, Ataie L, Hedayati M, et al. Effect of long-term continuous methimazole treatment of hyperthyroidism: comparison with radioiodine. Eur J Endocrinol. 2005;152(5):695–701. Doi: 10.1530/eje.1.01904.
78. Biondi B, Bartalena L, Cooper DS, et al. The 2015 European Thyroid Association guide-lines on diagnosis and treatment of endogenous subclinical hyperthyroidism. Eur Thyroid J. 2015;4(3):149–163. Doi: 10.1159/000438750.
79. Collet TH, Gussekloo J, Bauer DC, et al. Thyroid Studies Collaboration: Subclinical hyper-thyroidism and the risk of coronary heart disease and mortality. Arch Intern Med. 2012;172(10):799–809. Doi: 10.1001/archinternmed.2012.402.
80. Gencer B, Collet TH, Virgini V, et al. Subclinical thyroid dysfunction and the risk of heart failure events: an individual participant data analysis from 6 prospective cohorts. Circula-tion. 2012;126(9):1040–1049. Doi: 10.1161/CIRCULATIONAHA.112.096024.
81. Wirth CD, Blum MR, da Costa BR, et al. Subclinical thyroid dysfunction and the risk for fractures: a systematic review and meta-analysis. Ann Intern Med. 2014;161(3):189–199. Doi: 10.7326/M14-0125.
82. Blum MR, Bauer DC, Collet TH, et al. Subclinical thyroid dysfunction and fracture risk: a meta-analysis. JAMA. 2015;313(20):2055–2065. Doi: 10.1001/jama.2015.5161.
83. Zhyzhneuskaya S, Addison C, Tsatlidis V, et al. The natural history of subclinical hyperthy-roidism in Graves’ disease: the rule of thirds. Thyroid. 2016;26(6):765–769. Doi: 10.1089/thy.2015.0470.
84. Satoh T, Isozaki O, Suzuki A, et al. 2016 guidelines for the management of thyroid storm from the Japan Thyroid Association and Japan Endocrine Society. Endocr J. 2016;63(12):1025–1064. Doi: 10.1507/endocrj.EJ16-0336.
85. Akamizu T. Thyroid storm: a Japanese perspective. Thyroid. 2018;28(1):32–40. Doi: 10.1089/thy.2017.0243.
86. Burch HB, Wartofsky L. Life-threatening thyrotoxicosis: thyroid storm. Endocrinol Metab Clin North Am. 1993;22(2):263–277.
87. Akamizu T, Satoh T, Isozaki O, et al. Japan Thyroid Association: Diagnostic criteria, clini-cal features, and incidence of thyroid storm based on nationwide surveys. Thyroid. 2012;22(7):661–679. Doi: 10.1089/thy.2011.0334.
88. Isozaki O, Satoh T, Wakino S, et al. Treatment and management of thyroid storm: analysis of the nationwide surveys: the taskforce committee of the Japan Thyroid Association and Japan Endocrine Society for the establishment of diagnostic criteria and nationwide surveys for thyroid storm. Clin Endocrinol. 2016;84(6):912–918. Doi: 10.1111/cen.12949.
89. Bonnema SJ, Hegedus L. Radioiodine therapy in benign thyroid diseases: effects, side ef-fects, and factors affecting therapeutic outcome. Endocr Rev. 2012;33(6):920–980. Doi: 10.1210/er.2012-1030.
90. Torring O, Tallstedt L, Wallin G, et al. Graves’ hyperthyroidism: treatment with antithyroid drugs, surgery, or radioiodine – a prospective, randomized study. J Clin Endocrinol Metab. 1996;81(8):2986–2993. Doi: 10.1210/jcem.81.8.8768863.
91. In H, Pearce EN, Wong AK, et al. Treatment options for Graves’ disease: a cost-effectiveness analysis. J Am Coll Surg. 2009;209(2):170–179. Doi: 10.1016/j.jamcollsurg.2009.03.025.
92. Zanocco K, Heller M, Elaraj D, Sturgeon C. Is subtotal thyroidectomy a cost-effective treatment for Graves’ disease? A cost-effectiveness analysis of the medical and surgical treatment options. Surgery. 2012;152(2):164–172. Doi: 10.1016/j.surg.2012.02.020.
93. Patel NN, Abraham P, Buscombe J, Vanderpump MP. The cost effectiveness of treatment modalities for thyrotoxicosis in a UK center. Thyroid. 2006;16(6):593–598. Doi: 10.1089/thy.2006.16.593.
94. Donovan PJ, McLeod DS, Little R, Gordon L. Cost-utility analysis comparing radioactive iodine, anti-thyroid drugs and total thyroidectomy for primary treatment of Graves’ disease. Eur J Endocrinol. 2016;175(6):595–603. Doi: 10.1530/EJE-16-0527.
95. Cohen RZ, Felner EI, Heiss KF, et al. Outcomes analysis of radioactive iodine and total thy-roidectomy for pediatric Graves’ disease. J Pediatr Endocrinol Metab. 2016;29(3):319–325. Doi: 10.1515/jpem-2015-0333.
96. Sawka AM, Lakra DC, Lea J, et al. A systematic review examining the effects of therapeu-tic radioactive iodine on ovarian function and future pregnancy in female thyroid cancer survivors. Clin Endocrinol (Oxf). 2008;69(3):479–490. Doi: 10.1111/j.1365-2265.2008.03222.x.
97. Nygaard B, Hegedus L, Gervil M, et al. Influence of compensated radioiodine therapy on thyroid volume and incidence of hypothyroidism in Graves’ disease. J Intern Med. 1995;238(6):491–497. Doi: 10.1111/j.1365-2796.1995.tb01230.x.
98. Sridama V, McCormick M, Kaplan EL, et al. Long-term follow-up study of compensated low-dose 131I therapy for Graves’ disease. N Engl J Med. 1984;311(7):426–432. Doi: 10.1056/NEJM198408163110702.
99. Walter MA, Briel M, Christ-Crain M, et al. Effects of antithyroid drugs on radioiodine treatment: systematic review and meta-analysis of randomised controlled trials. BMJ. 2007;334(7592):514. Doi: 10.1136/bmj.39114.670150.BE.
100. Brandt F, Thvilum M, Almind D, et al. Graves’ disease and toxic nodular goiter are both associated with increased mortality but differ with respect to the cause of death: a Danish population-based register study. Thyroid. 2013;23(4):408–413. Doi: 10.1089/thy.2012.0500.
101. Schwensen CF, Brandt F, Hegedus L, Brix TH. Mortality in Graves’ orbitopathy is increased and influenced by gender, age and pre-existing morbidity: a nationwide Danish register study. Eur J Endocrinol. 2017;176(6):669–676. Doi: 10.1530/EJE-16-0954.
102. Lillevang-Johansen M, Abrahamsen B, Jorgensen HL, et al. Excess mortality in treated and untreated hyperthyroidism is related to cumulative periods of low serum TSH. J Clin Endocrinol Metab. 2017;102(7):2301–2309. Doi: 10.1210/jc.2017-00166.
103. Ron E, Doody MM, Becker DV, et al. Cancer mortality following treatment for adult hyperthyroidism. Cooperative Thyrotoxicosis Therapy Follow-up Study Group. JAMA. 1998;280(4):347–355. Doi: 10.1001/jama.280.4.347.
104. Bonnema SJ, Bennedbaek FN, Veje A, et al. Propylthiouracil before 131I therapy of hyperthyroid diseases: effect on cure rate evaluated by a randomized clinical trial. J Clin Endocrinol Metab. 2004;89(9):4439–4444. Doi: 10.1210/jc.2004-0247.
105. Bonnema SJ, Bennedbaek FN, Gram J, et al. Resumption of methimazole after 131I therapy of hyperthyroid diseases: effect on thyroid function and volume evaluated by a randomized clinical trial. Eur J Endocrinol. 2003;149(6):485–492. Doi: 10.1530/eje.0.1490485.
106. Bartalena L, Marcocci C, Bogazzi F, et al. Use of corticosteroids to prevent progres-sion of Graves’ ophthalmopathy after radioiodine therapy for hyperthyroidism. N Engl J Med. 1989;321(20):1349–1352. Doi: 10.1056/NEJM198911163212001.
107. Jensen BE, Bonnema SJ, Hegedus L. Glucocorticoids do not influence the effect of radioiodine therapy in Graves’ disease. Eur J Endocrinol. 2005;153(1):15–21. Doi: 10.1530/eje.1.01924.
108. Burch HB, Burman KD, Cooper DS. A 2011 survey of clinical practice patterns in the management of Graves’ disease. J Clin Endocrinol Metab. 2012;97(12):4549–4558. Doi: 10.1210/jc.2012-2802.
109. Bartalena L, Chiovato L, Vitti P. Management of hyperthyroidism due to Graves’ disease: frequently asked questions and answers (if any). J Endocrinol Invest. 2016;39(10):1105–1114. Doi: 10.1007/s40618-016-0505-x.
110. Genovese BM, Noureldine SI, Gleeson EM, et al. What is the best definitive treat-ment for Graves’ disease? A systematic review of the existing literature. Ann Surg Oncol. 2013;20(2):660–667. Doi: 10.1245/s10434-012-2606-x.
111. Guo Z, Yu P, Liu Z, et al. Total thyroidectomy vs bilateral subtotal thyroidectomy in patients with Graves’ diseases: a meta-analysis of randomized clinical trials. Clin Endocrinol (Oxf). 2013;79(5):739–746. Doi: 10.1111/cen.12209.
112. Sosa JA, Bowman HM, Tielsch JM, et al. The importance of surgeon experience for clinical and economic outcomes from thyroidectomy. Ann Surg. 2008;228(3):320–330. Doi: 10.1097/00000658-199809000-00005.
113. Erbil Y, Ozluk Y, Giris M, et al. Effect of lugol solution on thyroid gland blood flow and microvessel density in the patients with Graves’ disease. J Clin Endocrinol Metab. 2007;92(6):2182–2189. Doi: 10.1210/jc.2007-0229.
114. Edafe O, Antakia R, Laskar N, et al. Systematic review and meta-analysis of predic-tors of post-thyroidectomy hypocalcaemia. Br J Surg. 2014;101(4):307–320. Doi: 10.1002/bjs.9384.
115. Bartalena L, Baldeschi L, Boboridis K, et al. European Group on Graves Orbitopa-thy: The 2016 European Thyroid Association/European Group on Graves’ Orbitopathy guidelines for the management of Graves’ orbitopathy. Eur Thyroid J. 2016;5(1):9–26. Doi: 10.1159/000443828.
116. Bartalena L, Macchia PE, Marcocci C, et al. Effects of treatment modalities for Graves’ hyperthyroidism on Graves’ orbitopathy: a 2015 Italian Society of Endocrinology Consensus Statement. J Endocrinol Invest. 2015;38(4):481–487. Doi: 10.1007/s40618-015-0257-z.
117. Bartalena L. The dilemma of how to manage Graves’ hyperthyroidism in patients with associated orbitopathy. J Clin Endocrinol Metab. 2011;96(3):592–599. Doi: 10.1210/jc.2010-2329.
118. Laurberg P, Wallin G, Tallstedt L, et al. TSH-receptor autoimmunity in Graves’ dis-ease after therapy with anti-thyroid drugs, surgery, or radioiodine: a 5-year prospective ran-domized study. Eur J Endocrinol. 2008;158(1):69–75. Doi: 10.1530/EJE-07-0450.
119. Bartalena L, Marcocci C, Bogazzi F, et al. Relation between therapy for hyperthy-roidism and the course of Graves’ ophthalmopathy. N Engl J Med. 1998;338(2):73–78. Doi: 10.1056/NEJM199801083380201.
120. Karlsson F, Dahlberg P, Jansson R, et al. Importance of TSH receptor activation in the development of severe endocrine ophthalmopathy. Acta Endocrinol. 1989;121(suppl 2):132–141.
121. Bartalena L, Marcocci C, Bogazzi F, et al. Use of corticosteroids to prevent progres-sion of Graves’ ophthalmopathy after radioiodine therapy for hyperthyroidism. N Engl J Med. 1989;321(20):1349–1352. Doi: 10.1056/NEJM198911163212001.
122. Tallstedt L, Lundell G, Torring O, et al. Occurrence of ophthalmopathy after treat-ment for Graves’ hyperthyroidism. The Thyroid Study Group. N Engl J Med. 1992;326(26):1733–1738. Doi: 10.1056/NEJM199206253262603.
123. Traisk F, Tallstedt L, Abraham-Nordling M, et al. Thyroid-associated ophthalmopa-thy after treatment for Graves’ hyperthyroidism with antithyroid drugs or iodine-131. J Clin Endocrinol Metab. 2009;94:3700–3707.
124. Vannucchi G, Campi I, Covelli C, et al. Graves’ orbitopathy activation after radioac-tive iodine therapy with and without steroid prophylaxis. J Clin Endocrinol Metab. 2009;94(9):3381–3386. Doi: 10.1210/jc.2009-0506.
125. Tallstedt L, Lundell G, Blomgren H, Bring J. Does early administration of thyroxine reduce the development of Graves’ ophthalmopathy after radioiodine treatment? Eur J Endocrinol. 1994;130(5):494–497. Doi: 10.1530/eje.0.1300494.
126. Perros P, Kendall-Taylor P, Neoh C, et al. A prospective study of the effects of ra-dioiodine therapy for hyperthyroidism in patients with minimally active Graves’ ophthal-mopathy. J Clin Endocrinol Metab. 2005;90(9):5321–5323. Doi: 10.1210/jc.2005-0507.
127. Kung AW, Yau CC, Cheng A. The incidence of ophthalmopathy after radioiodine therapy for Graves’ disease: prognostic factors and the role of methimazole. J Clin Endocrinol Metab. 1994;79(2):542–546. Doi: 10.1210/jcem.79.2.7913934.
128. Lai A, Sassi L, Compri E, et al. Lower dose prednisone prevents radioiodine-associated exacerbation of initially mild or absent Graves’ orbitopathy: a retrospective co-hort study. J Clin Endocrinol Metab. 2010;95(3):1333–1337. Doi: 10.1210/jc.2009-2130.
129. Acharya SH, Avenell A, Philip S, et al. Radioiodine therapy (RAI) for Graves’ dis-ease (GD) and the effect on ophthalmopathy: a systematic review. Clin Endocrinol (Oxf). 2008;69(6):943–950. Doi: 10.1111/j.1365-2265.2008.03279.x.
130. Shiber S, Stiebel-Kalish H, Shimon I, et al. Glucocorticoid regimens for prevention of Graves’ ophthalmopathy progression following radioiodine treatment: systematic review and meta-analysis. Thyroid. 2014;24(10):1515–1523. Doi: 10.1089/thy.2014.0218.
131. Marcocci C, Bruno-Bossio G, Manetti L, et al. The course of Graves’ ophthalmopa-thy is not influenced by near-total thyroidectomy: a case-control study. Clin Endocrinol. 1999;51(4):503–508. Doi: 10.1046/j.1365-2265.1999.00843.x.
132. Marcocci C, Kahaly GJ, Krassas GE, et al. Selenium and the course of mild Graves’ orbitopathy. N Engl J Med. 2011;364(20):1920–1931. Doi: 10.1056/NEJMoa1012985.
133. Bartalena L, Tanda ML. Clinical practice: Graves’ ophthalmopathy. N Engl J Med. 2009;360(10):994–1001. Doi: 10.1056/NEJMcp0806317.
134. Krassas GE, Poppe K, Glinoer D. Thyroid function and human reproductive health. Endocr Rev. 2010;31(5):702–755. Doi: 10.1210/er.2009-0041.
135. Andersen SL, Olsen J, Carle A, Laurberg P. Hyperthyroidism incidence fluctuates widely in and around pregnancy and is at variance with some other autoimmune diseases: a Danish population-based study. J Clin Endocrinol Metab. 2015;100(3):1164–1171. Doi: 10.1210/jc.2014-3588.
136. Laurberg P, Bournaud C, Karmisholt J, Orgiazzi J. Management of Graves’ hyper-thyroidism in pregnancy: focus on both maternal and foetal thyroid function, and caution against surgical thyroidectomy in pregnancy. Eur J Endocrinol. 2009;160(1):1–8. Doi: 10.1530/EJE-08-0663.
137. Andersen SL, Olsen J, Laurberg P. Antithyroid drug side effects in the population and in pregnancy. J Clin Endocrinol Metab. 2016;101(4):1606–1614. Doi: 10.1210/jc.2015-4274.
138. Alexander EK, Larsen PR. High dose of 131I therapy for the treatment of hyperthy-roidism caused by Graves’ disease. J Clin Endocrinol Metab. 2002;87(3):1073–1077. Doi: 10.1210/jcem.87.3.8333.
139. Nicholas WC, Fischer RG, Stevenson RA, Bass JD. Single daily dose of methima-zole compared to every 8 hours propylthiouracil in the treatment of hyperthyroidism. South Med J. 1995;88(9):973–976. Doi: 10.1097/00007611-199509000-00018.
140. Nakamura H, Noh JY, Itoh K, et al. Comparison of methimazole and propylthioura-cil in patients with hyperthyroidism caused by Graves’ disease. J Clin Endocrinol Metab. 2007;92(6):2157–2162. Doi: 10.1210/jc.2006-2135.
141. Korelitz JJ, McNally DL, Masters MN, et al. Prevalence of thyrotoxicosis, antithy-roid medication use, and complications among pregnant women in the United States. Thyroid. 2013;23(6):758–765. Doi: 10.1089/thy.2012.0488.
142. Andersen SL, Olsen J, Wu CS, Laurberg P. Birth defects after early pregnancy use of antithyroid drugs: a Danish nationwide study. J Clin Endocrinol Metab. 2013;98(11):4373–4381. Doi: 10.1210/jc.2013-2831.
143. Rubin PC. Current concepts: beta-blockers in pregnancy. N Engl J Med. 1981;305(22):1323–1326. Doi: 10.1056/NEJM198111263052205.
144. Momotani N, Hisaoka T, Noh J, et al. Effects of iodine on thyroid status of fetus versus mother in treatment of Graves’ disease complicated by pregnancy. J Clin Endocrinol Metab. 1992;75(3):738–744. Doi: 10.1210/jcem.75.3.1517362.
145. Nedrebo BG, Holm PI, Uhlving S, et al. Predictors of outcome and comparison of different drug regimens for the prevention of relapse in patients with Graves’ disease. Eur J Endocrinol. 2002;147(5):583–589. Doi: 10.1530/eje.0.1470583.
146. Laurberg P, Andersen SL. Therapy of endocrine disease: antithyroid drug use in ear-ly pregnancy and birth defects: time windows of relative safety and high risk? Eur J Endo-crinol. 2014;171(1):R13–R20. Doi: 10.1530/EJE-14-0135.
147. Laurberg P. Remission of Graves’ disease during anti-thyroid drug therapy: time to reconsider the mechanism? Eur J Endocrinol. 2006;155(6):783–786. Doi: 10.1530/eje.1.02295.
148. Bliddal S, Rasmussen AK, Sundberg K, et al. Antithyroid drug-induced fetal goi-trous hypothyroidism. Nat Rev Endocrinol. 2011;7(7):396–406. Doi: 10.1038/nrendo.2011.34.
149. McKenzie JM, Zakarija M. Fetal and neonatal hyperthyroidism and hypothyroidism due to maternal TSH receptor antibodies. Thyroid. 1992;2(2):155–159. Doi: 10.1089/thy.1992.2.155.
150. Abeillon-du Payrat J, Chikh K, Bossard N, et al. Predictive value of maternal sec-ond-generation thyroid-binding inhibitory immunoglobulin assay for neonatal autoimmune hyperthyroidism. Eur J Endocrinol. 2014;171(4):451–460. Doi: 10.1530/EJE-14-0254.
151. Cove DH, Johnston P. Fetal hyperthyroidism: experience of treatment in four sib-lings. Lancet. 1985;1(8426):430–432. Doi: 10.1016/s0140-6736(85)91148-1.
152. Amino N, Tanizawa O, Mori H, et al. Aggravation of thyrotoxicosis in early preg-nancy and after delivery in Graves’ disease. J Clin Endocrinol Metab. 1982;55(1):108–112. Doi: 10.1210/jcem-55-1-108.
153. Alexander EK, Pearce EN, Brent GA, et al. 2017 guidelines of the American Thy-roid Association for the Diagnosis and Management of Thyroid Disease During Pregnancy and the Postpartum. Thyroid. 2017;27(3):315–389. Doi: 10.1089/thy.2016.0457.
154. Mandel SJ, Cooper DS. The use of antithyroid drugs in pregnancy and lactation. J Clin Endocrinol Metab. 2001;86(6):2354–2359. Doi: 10.1210/jcem.86.6.7573.
155. Pearce SH. Spontaneous reporting of adverse reactions to carbimazole and propylthiouracil in the UK. Clin Endocrinol (Oxf). 2004;61(5):589–594. Doi: 10.1111/j.1365-2265.2004.02135.x.
156. Perros P, Crombie AL, Matthews JN, Kendall-Taylor P. Age and gender influence the severity of thyroid-associated ophthalmopathy: a study of 101 patients attending a combined thyroid-eye clinic. Clin Endocrinol (Oxf). 1993;38(4):367–372. Doi: 10.1111/j.1365-2265.1993.tb00516.x.
157. Leger J, Gelwane G, Kaguelidou F, et al. French Childhood Graves’ Disease Study Group: Positive impact of long-term antithyroid drug treatment on the outcome of children with Graves’ disease: national long-term cohort study. J Clin Endocrinol Metab. 2012;97(1):110–119. Doi: 10.1210/jc.2011-1944.
158. Ohye H, Minagawa A, Noh JY, et al. Antithyroid drug treatment for graves’ disease in children: a long-term retrospective study at a single institution. Thyroid. 2014;24(2):200–207. Doi: 10.1089/thy.2012.0612.
159. Rivkees SA, Szarfman A. Dissimilar hepatotoxicity profiles of propylthiouracil and methimazole in children. J Clin Endocrinol Metab. 2010;95(7):3260–3267. Doi: 10.1210/jc.2009-2546.
160. Ma C, Kuang A, Xie J, Liu G. Radioiodine treatment for pediatric Graves’ disease. Cochrane Database Syst Rev. 2008;(3):CD006294. Doi: 10.1002/14651858.CD006294.pub2.
161. Coles AJ, Wing M, Smith S, et al. Pulsed monoclonal antibody treatment and auto-immune thyroid disease in multiple sclerosis. Lancet. 1999;354(9191):1691–1695. Doi: 10.1016/S0140-6736(99)02429-0.
162. Chen F, Day SL, Metcalfe RA, et al. Characteristics of autoimmune thyroid disease occurring as a late complication of immune reconstitution in patients with advanced human immunodeficiency virus (HIV) disease. Medicine (Baltimore). 2005;84(2):98–106. Doi: 10.1097/01.md.0000159082.45703.90.
163. Weetman AP. Graves’ disease following immune reconstitution or immunomodula-tory treatment: should we manage it any differently? Clin Endocrinol (Oxf). 2014;80(5):629–632. Doi: 10.1111/cen.12427.
164. Furmaniak J, Sanders J, Nunez Miguel R, Rees Smith B. Mechanisms of action of TSHR autoantibodies. Horm Metab Res. 2015;47(10):735–752. Doi: 10.1055/s-0035-1559648.
165. Gershengorn MC, Neumann S. Update in TSH receptor agonists and antagonists. J Clin Endocrinol Metab. 2012;97(12):4287–4292. Doi: 10.1210/jc.2012-3080.
166. El Fassi D, Nielsen CH, Hasselbalch HC, Hegedus L. The rationale for B lympho-cyte depletion in Graves’ disease: monoclonal anti-CD20 antibody therapy as a novel treatment option. Eur J Endocrinol. 2006;154(5):623–632. Doi: 10.1530/eje.1.02140.
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Fadeyev V.V. Review of European Thyroid Association Guideline (2018) for the Management of Graves’ Hyperthyroidism. Clinical and experimental thyroidology. 2020;16(1):4-20. (In Russ.) https://doi.org/10.14341/ket12474
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