A brief review and update on radioactive iodine-131 treatment for differentiated thyroid cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

ZHANG Teng ¹ , LI Jiao ² ,  LIN Yansong ³

1. Department of Nuclear Medicine, Beijing Chaoyang Hospital, Capital Medical University, Beijing 100020, P. R. China;
2. Department of Nuclear Medicine, the Affiliated Hospital of Qingdao University, Qingdao 266003, P. R. China;
3. Department of Nuclear Medicine, Peking Union Medical College (PUMC) Hospital, Chinese Academy of Medical Sciences & PUMC, Beijing 100730, P. R. China;

Corresponding author：

LIN Yansong, Email: linys@pumch.cn

Keywords：

differentiated thyroid cancer; ¹³¹I therapy; theranostic; indicator of response to radioactive iodine therapy; overall management

DOI：

10.7507/1007-9424.202405028

Video：

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The administration of radioactive iodine-131 (¹³¹I) is one of the representative traditional targeted therapy for post-surgical differentiated thyroid carcinoma (DTC). As DTC tumor cells largely preserve the capability of thyroid follicular epithelial cells, including the expression of the sodium iodide symporter (NIS), ¹³¹I can be selectively internalized by these cells once introduced into the body. The simultaneous emitting of both γ-ray and β-ray from ¹³¹I featured its unique theranostic value in managing DTC, through γ-ray to detect the residual thyroid tissue and DTC lesions via nuclear medical imaging, while through β-ray to yield the precise tumoricidal effect as well as remnant thyroid ablation. This theranostic potential of ¹³¹I significantly enhances progression-free survival, disease-specific survival, and overall survival in DTC patients with residual/recurrent/metastatic lesions as long as they are capable of iodine uptake. Nevertheless, the clinical application of ¹³¹I, despite its “precise” treatment philosophy, remains far from precision medicine while clinical practice, which urges further refinement in pre-treatment assessment, dosage tailoring, and post-treatment efficacy evaluation to fully capitalize on its theranostic benefits. Recently, with the accumulation of evidence-based medical data, ¹³¹I treatment has evolved with respect to treatment principles, pre-treatment risk stratification, post-treatment dynamic assessment, and comprehensive patient management, with an aim to optimize the diagnostic and therapeutic precision of ¹³¹I. Here we briefly review and update the recent advance on ¹³¹I management on DTC.

Citation： ZHANG Teng, LI Jiao, LIN Yansong. A brief review and update on radioactive iodine-131 treatment for differentiated thyroid cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2024, 31(11): 1300-1306. doi: 10.7507/1007-9424.202405028 Copy

1.	中华医学会核医学分会. ¹³¹I治疗分化型甲状腺癌指南 (2021版). 中华核医学与分子影像杂志, 2021, 41(4): 218-241.
2.	中国抗癌协会甲状腺癌专业委员会. 中国抗癌协会甲状腺癌整合诊治指南 (2022精简版). 中国肿瘤临床, 2023, 50(7): 325-330.
3.	Haugen BR, Alexander EK, Bible KC, et al. 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer: The American Thyroid Association Guidelines Task Force on Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid, 2016, 26(1): 1-133.
4.	中国临床肿瘤学会指南工作委员会甲状腺癌专家委员会. 中国临床肿瘤学会 (CSCO) 持续/复发及转移性分化型甲状腺癌诊疗指南-2019. 肿瘤预防与治疗, 2019, 32(12): 1051-1079.
5.	中国临床肿瘤学会甲状腺癌专业委员会, 中国研究型医院学会分子诊断专业委员会甲状腺癌学组, 医促会甲状腺疾病专业委员会核医学组, 等. 分化型甲状腺癌术后¹³¹I治疗前评估专家共识. 中国癌症杂志, 2019, 29(10): 832-840.
6.	Durante C, Puxeddu E, Ferretti E, et al. BRAF mutations in papillary thyroid carcinomas inhibit genes involved in iodine metabolism. J Clin Endocrinol Metab, 2007, 92(7): 2840-2843.
7.	Soares P, Lima J, Preto A, et al. Genetic alterations in poorly differentiated and undifferentiated thyroid carcinomas. Curr Genomics, 2011, 12(8): 609-617.
8.	Riesco-Eizaguirre G, Rodríguez I, De la Vieja A, et al. The BRAFV600E oncogene induces transforming growth factor beta secretion leading to sodium iodide symporter repression and increased malignancy in thyroid cancer. Cancer Res, 2009, 69(21): 8317-8325.
9.	Yang K, Wang H, Liang Z, et al. BRAFV600E mutation associated with non-radioiodine-avid status in distant metastatic papillary thyroid carcinoma. Clin Nucl Med, 2014, 39(8): 675-679.
10.	Yang X, Li J, Li X, et al. TERT promoter mutation predicts radioiodine-refractory character in distant metastatic differentiated thyroid cancer. J Nucl Med, 2017, 58(2): 258-265.
11.	Mu Z, Zhang X, Sun D, et al. Characterizing genetic alterations related to radioiodine avidity in metastatic thyroid cancer. J Clin Endocrinol Metab, 2024, 109(5): 1231-1240.
12.	Cancer Genome Atlas Research Network. Integrated genomic characterization of papillary thyroid carcinoma. Cell, 2014, 159(3): 676-690.
13.	Landa I, Ibrahimpasic T, Boucai L, et al. Genomic and transcriptomic hallmarks of poorly differentiated and anaplastic thyroid cancers. J Clin Invest, 2016, 126(3): 1052-1066.
14.	Latteyer S, Tiedje V, König K, et al. Targeted next-generation sequencing for TP53, RAS, BRAF, ALK and NF1 mutations in anaplastic thyroid cancer. Endocrine, 2016, 54(3): 733-741.
15.	Bikas A, Ahmadi S, Pappa T, et al. Additional oncogenic alterations in RAS-driven differentiated thyroid cancers associate with worse clinicopathologic outcomes. Clin Cancer Res, 2023, 29(14): 2678-2685.
16.	Avram AM, Giovanella L, Greenspan B, et al. SNMMI Procedure Standard/EANM Practice Guideline for Nuclear Medicine Evaluation and Therapy of Differentiated Thyroid Cancer: Abbreviated Version. J Nucl Med, 2022, 63(6): 15N-35N.
17.	Filetti S, Durante C, Hartl D, et al. Thyroid cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol, 2019, 30(12): 1856-1883.
18.	Tuttle RM, Ahuja S, Avram AM, et al. Controversies, consensus, and collaboration in the use of ¹³¹I therapy in differentiated thyroid cancer: a joint statement from the American Thyroid Association, the European Association of Nuclear Medicine, the Society of Nuclear Medicine and Molecular Imaging, and the European Thyroid Association. Thyroid, 2019, 29(4): 461-470.
19.	Zhang X, Liu JR, Mu ZZ, et al. Response to surgery assessments for sparing radioiodine remnant ablation in intermediate-risk papillary thyroid cancer. J Clin Endocrinol Metab, 2023, 108(6): 1330-1337.
20.	Sabra MM, Grewal RK, Tala H, et al. Clinical outcomes following empiric radioiodine therapy in patients with structurally identifiable metastatic follicular cell-derived thyroid carcinoma with negative diagnostic but positive post-therapy ¹³¹I whole-body scans. Thyroid, 2012, 22(9): 877-883.
21.	Haddad RI, Bischoff L, Ball D, et al. Thyroid Carcinoma, Version 2. 2022, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw, 2022, 20(8): 925-951.
22.	Muratet JP, Giraud P, Daver A, et al. Predicting the efficacy of first iodine-131 treatment in differentiated thyroid carcinoma. J Nucl Med, 1997, 38(9): 1362-1368.
23.	Fatourechi V, Hay ID, Mullan BP, et al. Are posttherapy radioiodine scans informative and do they influence subsequent therapy of patients with differentiated thyroid cancer? Thyroid, 2000, 10(7): 573-577.
24.	Sherman SI, Tielens ET, Sostre S, et al. Clinical utility of posttreatment radioiodine scans in the management of patients with thyroid carcinoma. J Clin Endocrinol Metab, 1994, 78(3): 629-634.
25.	Petrich T, Quintanilla-Martinez L, Korkmaz Z, et al. Effective cancer therapy with the alpha-particle emitter [ ²¹¹At]astatine in a mouse model of genetically modified sodium/iodide symporter-expressing tumors. Clin Cancer Res, 2006, 12(4): 1342-1348.
26.	Watabe T, Kaneda-Nakashima K, Liu Y, et al. Enhancement of ²¹¹At uptake via the sodium iodide symporter by the addition of ascorbic acid in targeted α-therapy of thyroid cancer. J Nucl Med, 2019, 60(9): 1301-1307.
27.	Watabe T, Liu Y, Kaneda-Nakashima K, et al. Comparison of the therapeutic effects of [²¹¹At]NaAt and [¹³¹I]NaI in an NIS-expressing thyroid cancer mouse model. Int J Mol Sci, 2022, 23(16): 9434. doi: 10.3390/ijms23169434.
28.	Oh JM, Ahn BC. Molecular mechanisms of radioactive iodine refractoriness in differentiated thyroid cancer: impaired sodium iodide symporter (NIS) expression owing to altered signaling pathway activity and intracellular localization of NIS. Theranostics, 2021, 11(13): 6251-6277.
29.	Groussin L, Theodon H, Bessiene L, et al. Redifferentiating effect of larotrectinib in NTRK-rearranged advanced radioactive-iodine refractory thyroid cancer. Thyroid, 2022, 32(5): 594-598.
30.	Rothenberg SM, Daniels GH, Wirth LJ. Redifferentiation of iodine-refractory BRAF V600E-mutant metastatic papillary thyroid cancer with dabrafenib-response. Clin Cancer Res, 2015, 21(24): 5640-5641.
31.	Iravani A, Solomon B, Pattison DA, et al. Mitogen-activated protein kinase pathway inhibition for redifferentiation of radioiodine refractory differentiated thyroid cancer: an evolving protocol. Thyroid, 2019, 29(11): 1634-1645.
32.	Falchook GS, Millward M, Hong D, et al. BRAF inhibitor dabrafenib in patients with metastatic BRAF-mutant thyroid cancer. Thyroid, 2015, 25(1): 71-77.

1. 中华医学会核医学分会. ¹³¹I治疗分化型甲状腺癌指南 (2021版). 中华核医学与分子影像杂志, 2021, 41(4): 218-241.
2. 中国抗癌协会甲状腺癌专业委员会. 中国抗癌协会甲状腺癌整合诊治指南 (2022精简版). 中国肿瘤临床, 2023, 50(7): 325-330.
3. Haugen BR, Alexander EK, Bible KC, et al. 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer: The American Thyroid Association Guidelines Task Force on Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid, 2016, 26(1): 1-133.
4. 中国临床肿瘤学会指南工作委员会甲状腺癌专家委员会. 中国临床肿瘤学会 (CSCO) 持续/复发及转移性分化型甲状腺癌诊疗指南-2019. 肿瘤预防与治疗, 2019, 32(12): 1051-1079.
5. 中国临床肿瘤学会甲状腺癌专业委员会, 中国研究型医院学会分子诊断专业委员会甲状腺癌学组, 医促会甲状腺疾病专业委员会核医学组, 等. 分化型甲状腺癌术后¹³¹I治疗前评估专家共识. 中国癌症杂志, 2019, 29(10): 832-840.
6. Durante C, Puxeddu E, Ferretti E, et al. BRAF mutations in papillary thyroid carcinomas inhibit genes involved in iodine metabolism. J Clin Endocrinol Metab, 2007, 92(7): 2840-2843.
7. Soares P, Lima J, Preto A, et al. Genetic alterations in poorly differentiated and undifferentiated thyroid carcinomas. Curr Genomics, 2011, 12(8): 609-617.
8. Riesco-Eizaguirre G, Rodríguez I, De la Vieja A, et al. The BRAFV600E oncogene induces transforming growth factor beta secretion leading to sodium iodide symporter repression and increased malignancy in thyroid cancer. Cancer Res, 2009, 69(21): 8317-8325.
9. Yang K, Wang H, Liang Z, et al. BRAFV600E mutation associated with non-radioiodine-avid status in distant metastatic papillary thyroid carcinoma. Clin Nucl Med, 2014, 39(8): 675-679.
10. Yang X, Li J, Li X, et al. TERT promoter mutation predicts radioiodine-refractory character in distant metastatic differentiated thyroid cancer. J Nucl Med, 2017, 58(2): 258-265.
11. Mu Z, Zhang X, Sun D, et al. Characterizing genetic alterations related to radioiodine avidity in metastatic thyroid cancer. J Clin Endocrinol Metab, 2024, 109(5): 1231-1240.
12. Cancer Genome Atlas Research Network. Integrated genomic characterization of papillary thyroid carcinoma. Cell, 2014, 159(3): 676-690.
13. Landa I, Ibrahimpasic T, Boucai L, et al. Genomic and transcriptomic hallmarks of poorly differentiated and anaplastic thyroid cancers. J Clin Invest, 2016, 126(3): 1052-1066.
14. Latteyer S, Tiedje V, König K, et al. Targeted next-generation sequencing for TP53, RAS, BRAF, ALK and NF1 mutations in anaplastic thyroid cancer. Endocrine, 2016, 54(3): 733-741.
15. Bikas A, Ahmadi S, Pappa T, et al. Additional oncogenic alterations in RAS-driven differentiated thyroid cancers associate with worse clinicopathologic outcomes. Clin Cancer Res, 2023, 29(14): 2678-2685.
16. Avram AM, Giovanella L, Greenspan B, et al. SNMMI Procedure Standard/EANM Practice Guideline for Nuclear Medicine Evaluation and Therapy of Differentiated Thyroid Cancer: Abbreviated Version. J Nucl Med, 2022, 63(6): 15N-35N.
17. Filetti S, Durante C, Hartl D, et al. Thyroid cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol, 2019, 30(12): 1856-1883.
18. Tuttle RM, Ahuja S, Avram AM, et al. Controversies, consensus, and collaboration in the use of ¹³¹I therapy in differentiated thyroid cancer: a joint statement from the American Thyroid Association, the European Association of Nuclear Medicine, the Society of Nuclear Medicine and Molecular Imaging, and the European Thyroid Association. Thyroid, 2019, 29(4): 461-470.
19. Zhang X, Liu JR, Mu ZZ, et al. Response to surgery assessments for sparing radioiodine remnant ablation in intermediate-risk papillary thyroid cancer. J Clin Endocrinol Metab, 2023, 108(6): 1330-1337.
20. Sabra MM, Grewal RK, Tala H, et al. Clinical outcomes following empiric radioiodine therapy in patients with structurally identifiable metastatic follicular cell-derived thyroid carcinoma with negative diagnostic but positive post-therapy ¹³¹I whole-body scans. Thyroid, 2012, 22(9): 877-883.
21. Haddad RI, Bischoff L, Ball D, et al. Thyroid Carcinoma, Version 2. 2022, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw, 2022, 20(8): 925-951.
22. Muratet JP, Giraud P, Daver A, et al. Predicting the efficacy of first iodine-131 treatment in differentiated thyroid carcinoma. J Nucl Med, 1997, 38(9): 1362-1368.
23. Fatourechi V, Hay ID, Mullan BP, et al. Are posttherapy radioiodine scans informative and do they influence subsequent therapy of patients with differentiated thyroid cancer? Thyroid, 2000, 10(7): 573-577.
24. Sherman SI, Tielens ET, Sostre S, et al. Clinical utility of posttreatment radioiodine scans in the management of patients with thyroid carcinoma. J Clin Endocrinol Metab, 1994, 78(3): 629-634.
25. Petrich T, Quintanilla-Martinez L, Korkmaz Z, et al. Effective cancer therapy with the alpha-particle emitter [ ²¹¹At]astatine in a mouse model of genetically modified sodium/iodide symporter-expressing tumors. Clin Cancer Res, 2006, 12(4): 1342-1348.
26. Watabe T, Kaneda-Nakashima K, Liu Y, et al. Enhancement of ²¹¹At uptake via the sodium iodide symporter by the addition of ascorbic acid in targeted α-therapy of thyroid cancer. J Nucl Med, 2019, 60(9): 1301-1307.
27. Watabe T, Liu Y, Kaneda-Nakashima K, et al. Comparison of the therapeutic effects of [²¹¹At]NaAt and [¹³¹I]NaI in an NIS-expressing thyroid cancer mouse model. Int J Mol Sci, 2022, 23(16): 9434. doi: 10.3390/ijms23169434.
28. Oh JM, Ahn BC. Molecular mechanisms of radioactive iodine refractoriness in differentiated thyroid cancer: impaired sodium iodide symporter (NIS) expression owing to altered signaling pathway activity and intracellular localization of NIS. Theranostics, 2021, 11(13): 6251-6277.
29. Groussin L, Theodon H, Bessiene L, et al. Redifferentiating effect of larotrectinib in NTRK-rearranged advanced radioactive-iodine refractory thyroid cancer. Thyroid, 2022, 32(5): 594-598.
30. Rothenberg SM, Daniels GH, Wirth LJ. Redifferentiation of iodine-refractory BRAF V600E-mutant metastatic papillary thyroid cancer with dabrafenib-response. Clin Cancer Res, 2015, 21(24): 5640-5641.
31. Iravani A, Solomon B, Pattison DA, et al. Mitogen-activated protein kinase pathway inhibition for redifferentiation of radioiodine refractory differentiated thyroid cancer: an evolving protocol. Thyroid, 2019, 29(11): 1634-1645.
32. Falchook GS, Millward M, Hong D, et al. BRAF inhibitor dabrafenib in patients with metastatic BRAF-mutant thyroid cancer. Thyroid, 2015, 25(1): 71-77.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

A brief review and update on radioactive iodine-131 treatment for differentiated thyroid cancer

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