Research progress on thyroid dysfunction induced by immunotherapy for lung cancer

doi:10.19401/j.cnki.1007-3639.2023.07.008

Abstract

Abstract:

Immune checkpoint inhibitors [mainly programmed death-1/programmed death ligand-1 (PD-1/PD-L1) inhibitors] have emerged as the most promising therapy in lung cancer treatment. However, clinicians still lack sufficient knowledge about immune-related adverse events. Immune-related thyroid dysfunction (irTD), one of the common immune-related adverse events, can be life-threatening in severe cases. This article discussed the thyroid dysfunction induced by PD-1/PD-L1 inhibitors in the treatment of lung cancer from the aspects of the incidence, pathogenesis, predictive biomarkers and treatment of irTD.

Key words: Immune-related thyroid dysfunction, Immune checkpoint inhibitors, Programmed death-1/programmed death ligand-1 inhibitors, Lung cancer

CLC Number:

R734.2

ZHANG Haoting, ZHENG Jing, FU Mengjiao, ZHOU Jianying. Research progress on thyroid dysfunction induced by immunotherapy for lung cancer[J]. China Oncology, 2023, 33(7): 701-706.

Figures/Tables 1

Tab. 1

References 45

[1]	SUNG H, FERLAY J, SIEGEL R L, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries[J]. CA Cancer J Clin, 2021, 71(3): 209-249. doi: 10.3322/caac.v71.3
[2]	周彩存, 王洁, 王宝成, 等. 中国非小细胞肺癌免疫检查点抑制剂治疗专家共识(2020年版)[J]. 中国肺癌杂志, 2021, 24(4): 217-235.
	ZHOU C C, WANG J, WANG B C, et al. Chinese experts consensus on immune checkpoint inhibitors for non-small cell lung cancer (2020 version)[J]. Chin J Lung Cancer, 2021, 24(4): 217-235.
[3]	BORGHAEI H, PAZ-ARES L, HORN L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small cell lung cancer[J]. N Engl J Med, 2015, 373(17): 1627-1639. doi: 10.1056/NEJMoa1507643
[4]	BRAHMER J, RECKAMP K L, BAAS P, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer[J]. N Engl J Med, 2015, 373(2): 123-135. doi: 10.1056/NEJMoa1504627
[5]	MOK T S K, WU Y L, KUDABA I, et al. Pembrolizumab versus chemotherapy for previously untreated, PD-L1-expressing, locally advanced or metastatic non-small cell lung cancer (KEYNOTE-042): a randomised, open-label, controlled, phase 3 trial[J]. Lancet, 2019, 393(10183): 1819-1830. doi: 10.1016/S0140-6736(18)32409-7
[6]	READY N E, OTT P A, HELLMANN M D, et al. Nivolumab monotherapy and nivolumab plus ipilimumab in recurrent small cell lung cancer: results from the CheckMate 032 randomized cohort[J]. J Thorac Oncol, 2020, 15(3): 426-435. doi: S1556-0864(19)33531-2 pmid: 31629915
[7]	HELLMANN M D, PAZ-ARES L, BERNABE CARO R, et al. Nivolumab plus ipilimumab in advanced non-small-cell lung cancer[J]. N Engl J Med, 2019, 381(21): 2020-2031. doi: 10.1056/NEJMoa1910231
[8]	CARBONE D P. First-line nivolumab in stage Ⅳ or recurrent non-small cell lung cancer[J]. Oncol Times, 2017, 39(17): 28-29.
[9]	RECK M, RODRÍGUEZ-ABREU D, ROBINSON A G, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small cell lung cancer[J]. N Engl J Med, 2016, 375(19): 1823-1833. doi: 10.1056/NEJMoa1606774
[10]	WU Y L, LU S, CHENG Y, et al. Nivolumab versus docetaxel in a predominantly Chinese patient population with previously treated advanced NSCLC: CheckMate 078 randomized phase Ⅲ clinical trial[J]. J Thorac Oncol, 2019, 14(5): 867-875. doi: 10.1016/j.jtho.2019.01.006
[11]	WU Y L, ZHANG L, FAN Y, et al. Randomized clinical trial of pembrolizumab vs chemotherapy for previously untreated Chinese patients with PD-L1-positive locally advanced or metastatic non-small cell lung cancer: KEYNOTE-042 China study[J]. Int J Cancer, 2021, 148(9): 2313-2320. doi: 10.1002/ijc.v148.9
[12]	ANTONIA S J, VILLEGAS A, DANIEL D, et al. Durvalumab after chemoradiotherapy in stage Ⅲ non-small cell lung cancer[J]. N Engl J Med, 2017, 377(20): 1919-1929. doi: 10.1056/NEJMoa1709937
[13]	BARLESI F, VANSTEENKISTE J, SPIGEL D, et al. Avelumab versus docetaxel in patients with platinum-treated advanced non-small cell lung cancer (JAVELIN Lung 200): an open-label, randomised, phase 3 study[J]. Lancet Oncol, 2018, 19(11): 1468-1479. doi: 10.1016/S1470-2045(18)30673-9
[14]	GANDHI L, RODRÍGUEZ-ABREU D, GADGEEL S, et al. Pembrolizumab plus chemotherapy in metastatic non-small cell lung cancer[J]. N Engl J Med, 2018, 378(22): 2078-2092. doi: 10.1056/NEJMoa1801005
[15]	NISHIO M, BARLESI F, WEST H, et al. Atezolizumab plus chemotherapy for first-line treatment of nonsquamous NSCLC: results from the randomized phase 3 IMpower132 trial[J]. J Thorac Oncol, 2021, 16(4): 653-664. doi: 10.1016/j.jtho.2020.11.025
[16]	PAZ-ARES L, DVORKIN M, CHEN Y B, et al. Durvalumab plus platinum-etoposide versus platinum-etoposide in first-line treatment of extensive-stage small cell lung cancer (CASPIAN): a randomised, controlled, open-label, phase 3 trial[J]. Lancet, 2019, 394(10212): 1929-1939. doi: 10.1016/S0140-6736(19)32222-6
[17]	PAZ-ARES L, LUFT A, VICENTE D, et al. Pembrolizumab plus chemotherapy for squamous non-small cell lung cancer[J]. N Engl J Med, 2018, 379(21): 2040-2051. doi: 10.1056/NEJMoa1810865
[18]	WEST H, MCCLEOD M, HUSSEIN M, et al. Atezolizumab in combination with carboplatin plus nab-paclitaxel chemotherapy compared with chemotherapy alone as first-line treatment for metastatic non-squamous non-small cell lung cancer (IMpower130): a multicentre, randomised, open-label, phase 3 trial[J]. Lancet Oncol, 2019, 20(7): 924-937. doi: 10.1016/S1470-2045(19)30167-6
[19]	BOYER M, ŞENDUR M A N, RODRÍGUEZ-ABREU D, et al. Pembrolizumab plus ipilimumab or placebo for metastatic non-small cell lung cancer with PD-L1 tumor proportion score ≥ 50%: randomized, double-blind phase Ⅲ KEYNOTE-598 study[J]. J Clin Oncol, 2021, 39(21): 2327-2338. doi: 10.1200/JCO.20.03579
[20]	HORN L, MANSFIELD A S, SZCZĘSNA A, et al. First-line atezolizumab plus chemotherapy in extensive-stage small cell lung cancer[J]. N Engl J Med, 2018, 379(23): 2220-2229. doi: 10.1056/NEJMoa1809064
[21]	PROF, LUIS, PAZ-ARES, et al. First-line nivolumab plus ipilimumab combined with two cycles of chemotherapy in patients with non-small cell lung cancer (CheckMate 9LA): an international, randomised, open-label, phase 3 trial[J]. Lancet Oncol, 2021, 22(2): 198-211. doi: 10.1016/S1470-2045(20)30641-0
[22]	National Cancer Institute. Protocol development cancer therapy evaluation program[EB/OL]. (2017-11-27)[2023-04-28]. https://ctep.cancer.gov/protocolDevelopment/electronic_applications/ctc.htm.
[23]	KHAN U, RIZVI H, SANO D, et al. Nivolumab induced myxedema crisis[J]. J Immunother Cancer, 2017, 5: 13. doi: 10.1186/s40425-017-0213-x pmid: 28239466
[24]	ZHOU N, VELEZ M A, BACHRACH B, et al. Immune checkpoint inhibitor induced thyroid dysfunction is a frequent event post-treatment in NSCLC[J]. Lung Cancer, 2021, 161: 34-41. doi: 10.1016/j.lungcan.2021.08.009 pmid: 34507111
[25]	YAMAZAKI H, IWASAKI H, YAMASHITA T, et al. Potential risk factors for nivolumab-induced thyroid dysfunction[J]. In Vivo, 2017, 31(6): 1225-1228. pmid: 29102951
[26]	OSORIO J C, NI A, CHAFT J E, et al. Antibody-mediated thyroid dysfunction during T-cell checkpoint blockade in patients with non-small cell lung cancer[J]. Ann Oncol, 2017, 28(3): 583-589. doi: 10.1093/annonc/mdw640
[27]	KOTWAL A, GUSTAFSON M P, BORNSCHLEGL S, et al. Immune checkpoint inhibitor-induced thyroiditis is associated with increased intrathyroidal T lymphocyte subpopulations[J]. Thyroid, 2020, 30(10): 1440-1450. doi: 10.1089/thy.2020.0075
[28]	TORIMOTO K, OKADA Y, NAKAYAMADA S, et al. Anti-PD-1 antibody therapy induces Hashimoto’s disease with an increase in peripheral blood follicular helper T cells[J]. Thyroid, 2017, 27(10): 1335-1336. doi: 10.1089/thy.2017.0062
[29]	KIMBARA S, FUJIWARA Y, IWAMA S, et al. Association of antithyroglobulin antibodies with the development of thyroid dysfunction induced by nivolumab[J]. Cancer Sci, 2018, 109(11): 3583-3590. doi: 10.1111/cas.2018.109.issue-11
[30]	YAMAUCHI I, YASODA A, MATSUMOTO S, et al. Incidence, features, and prognosis of immune-related adverse events involving the thyroid gland induced by nivolumab[J]. PLoS One, 2019, 14(5): e0216954. doi: 10.1371/journal.pone.0216954
[31]	SABINI E, SFRAMELI A, MARINÒ M. A case of drug-induced Graves’ orbitopathy after combination therapy with tremelimumab and durvalumab[J]. J Endocrinol Invest, 2018, 41(7): 877-878. doi: 10.1007/s40618-018-0906-0
[32]	ZHAN L, FENG H F, LIU H Q, et al. Immune checkpoint inhibitors-related thyroid dysfunction: epidemiology, clinical presentation, possible pathogenesis, and management[J]. Front Endocrinol (Lausanne), 2021, 12: 649863. doi: 10.3389/fendo.2021.649863
[33]	MAZARICO I, CAPEL I, GIMÉNEZ-PALOP O, et al. Low frequency of positive antithyroid antibodies is observed in patients with thyroid dysfunction related to immune check point inhibitors[J]. J Endocrinol Invest, 2019, 42(12): 1443-1450. doi: 10.1007/s40618-019-01058-x pmid: 31093955
[34]	YAMAUCHI I, SAKANE Y, FUKUDA Y, et al. Clinical features of nivolumab-induced thyroiditis: a case series study[J]. Thyroid, 2017, 27(7): 894-901. doi: 10.1089/thy.2016.0562 pmid: 28537531
[35]	DELIVANIS D A, GUSTAFSON M P, BORNSCHLEGL S, et al. Pembrolizumab-induced thyroiditis: comprehensive clinical review and insights into underlying involved mechanisms[J]. J Clin Endocrinol Metab, 2017, 102(8): 2770-2780. doi: 10.1210/jc.2017-00448 pmid: 28609832
[36]	KURIMOTO C, INABA H, ARIYASU H, et al. Predictive and sensitive biomarkers for thyroid dysfunctions during treatment with immune-checkpoint inhibitors[J]. Cancer Sci, 2020, 111(5): 1468-1477. doi: 10.1111/cas.v111.5
[37]	KRIEG C, NOWICKA M, GUGLIETTA S, et al. High-dimensional single-cell analysis predicts response to anti-PD-1 immunotherapy[J]. Nat Med, 2018, 24(2): 144-153. doi: 10.1038/nm.4466 pmid: 29309059
[38]	MAEKURA T, NAITO M, TAHARA M, et al. Predictive factors of nivolumab-induced hypothyroidism in patients with non-small cell lung cancer[J]. In Vivo, 2017, 31(5): 1035-1039. pmid: 28882978
[39]	YOON J H, HONG A R, KIM H K, et al. Characteristics of immune-related thyroid adverse events in patients treated with PD-1/PD-L1 inhibitors[J]. Endocrinol Metab (Seoul), 2021, 36(2): 413-423. doi: 10.3803/EnM.2020.906 pmid: 33820396
[40]	DE FILETTE J, ANDREESCU C E, COOLS F, et al. A systematic review and meta-analysis of endocrine-related adverse events associated with immune checkpoint inhibitors[J]. Horm Metab, 2019, 51(3): 145-156.
[41]	KOTWAL A, KOTTSCHADE L, RYDER M. PD-L1 inhibitor-induced thyroiditis is associated with better overall survival in cancer patients[J]. Thyroid, 2020, 30(2): 177-184. doi: 10.1089/thy.2019.0250 pmid: 31813343
[42]	CAMPREDON P, MOULY C, LUSQUE A, et al. Incidence of thyroid dysfunctions during treatment with nivolumab for non-small cell lung cancer: retrospective study of 105 patients[J]. Presse Med, 2019, 48(4): e199-e207. doi: 10.1016/j.lpm.2018.10.019
[43]	POLLACK R, ASHASH A, CAHN A, et al. Immune checkpoint inhibitor-induced thyroid dysfunction is associated with higher body mass index[J]. J Clin Endocrinol Metab, 2020, 105(10): dgaa458.
[44]	D'AIELLO A, LIN J, GUCALP R, et al. Thyroid dysfunction in lung cancer patients treated with immune checkpoint inhibitors (ICIs): outcomes in a multiethnic urban cohort[J]. Cancers (Basel), 2021, 13(6): 1464. doi: 10.3390/cancers13061464
[45]	彭智, 袁家佳, 王正航, 等. ASCO/NCCN免疫治疗毒性管理指南解读[J]. 肿瘤综合治疗电子杂志, 2018, 4(2): 38-47.
	PENG Z, YUAN J J, WANG Z H, et al. Comments on ASCO/NCCN management guidelines of toxicities from immunotherapy[J]. J Multidiscip Cancer Manag Electron Version, 2018, 4(2): 38-47.