Frequency and characteristics of immune-related thyroid adverse events in patients with resected stage III/IV melanoma treated with adjuvant PD-1 inhibitors: a national cohort study.

Adjuvant Immune checkpoint inhibitors Immune-related adverse events Immune-related thyroiditis Melanoma PD-1 inhibitor

Journal

Supportive care in cancer : official journal of the Multinational Association of Supportive Care in Cancer
ISSN: 1433-7339
Titre abrégé: Support Care Cancer
Pays: Germany
ID NLM: 9302957

Informations de publication

Date de publication:
10 Apr 2024
Historique:
received: 19 11 2023
accepted: 18 03 2024
medline: 10 4 2024
pubmed: 10 4 2024
entrez: 10 4 2024
Statut: epublish

Résumé

Immune-related thyroid adverse events (irTAEs) occur frequently following immune checkpoint inhibitor (ICI) therapy. The purpose of this study is to provide knowledge about the incidence, clinical timeline characteristics, associated factors of irTAEs, and potential impact on treatment efficacy in patients with melanoma receiving adjuvant ICI therapy. A national multicenter retrospective cohort study of patients with resected stage III/IV melanoma treated with adjuvant PD-1 inhibitors between November 2018 and December 2020. Data were extracted from the Danish Metastatic Melanoma Database. The irTAEs were defined as two consecutive abnormal TSH values and subdivided into transient or persistent. Of 454 patients, 99 developed an irTAE (21.8%), of these were 46 transient (46.5%) and 53 persistent (53.5%). Median time to transient and persistent irTAE was 55 and 44 days, respectively (p = 0.57). A hyperthyroid phase followed by hypothyroidism was seen in 73.6% of persistent irTAEs, whereas 87% of transient irTAEs developed an isolated hypo- or hyperthyroid phase. Multiple variable analysis demonstrated an association between irTAE and female sex (HR 2.45; 95% CI 1.63-3.70; p < 0.001), but no association with recurrence-free survival (HR 0.86; 95% CI 0.50-1.48; p = 0.587) or overall survival (HR 1.05; 95% CI 0.52-2.12, p = 0.891). IrTAE is a common side effect to PD-1 inhibitors primarily occurring within the first 3 months, with a high risk of persistency. Female sex is a strong predictive factor. IrTAE was not associated with improved clinical outcome.

Identifiants

pubmed: 38598052
doi: 10.1007/s00520-024-08445-y
pii: 10.1007/s00520-024-08445-y
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

281

Informations de copyright

© 2024. The Author(s).

Références

Sun Q, Sun H, Wu N et al (2022) Patients with melanoma treated with immune checkpoint inhibitors who had non-thyroid endocrine and skin immune-related adverse events have better prognosis: a systematic review and meta-analysis. Front Oncol 12:976224. https://doi.org/10.3389/fonc.2022.976224
doi: 10.3389/fonc.2022.976224 pubmed: 36185176 pmcid: 9515964
Iyer PC, Cabanillas ME, Waguespack SG et al (2018) Immune-related thyroiditis with immune checkpoint inhibitors. Thyroid 28:1243–1251. https://doi.org/10.1089/thy.2018.0116
doi: 10.1089/thy.2018.0116 pubmed: 30132401 pmcid: 6157359
Kennedy LB, Salama AKS (2019) A review of immune-mediated adverse events in melanoma. Oncol Ther 7:101–120. https://doi.org/10.1007/s40487-019-0096-8
doi: 10.1007/s40487-019-0096-8 pubmed: 32699983 pmcid: 7359990
Sznol M, Postow MA, Davies MJ et al (2017) Endocrine-related adverse events associated with immune checkpoint blockade and expert insights on their management. Cancer Treat Rev 58:70–76. https://doi.org/10.1016/j.ctrv.2017.06.002
doi: 10.1016/j.ctrv.2017.06.002 pubmed: 28689073
Fan Y, Xie W, Huang H et al (2021) Association of immune related adverse events with efficacy of immune checkpoint inhibitors and overall survival in cancers: a systemic review and meta-analysis. Front Oncol 11:633032. https://doi.org/10.3389/fonc.2021.633032
doi: 10.3389/fonc.2021.633032 pubmed: 33912454 pmcid: 8072154
Ramos-Casals M, Brahmer JR, Callahan MK et al (2020) Immune-related adverse events of checkpoint inhibitors. Nat Rev Dis Primers 6:38. https://doi.org/10.1038/s41572-020-0160-6
doi: 10.1038/s41572-020-0160-6 pubmed: 32382051 pmcid: 9728094
Liu X, Shi Y, Zhang D et al (2021) Risk factors for immune-related adverse events: what have we learned and what lies ahead? Biomark Res 9:79. https://doi.org/10.1186/s40364-021-00314-8
doi: 10.1186/s40364-021-00314-8 pubmed: 34732257 pmcid: 8565046
Wong SK, Nebhan CA, Johnson DB (2021) Impact of patient age on clinical efficacy and toxicity of checkpoint inhibitor therapy. Front Immunol 12:786046. https://doi.org/10.3389/fimmu.2021.786046
doi: 10.3389/fimmu.2021.786046 pubmed: 34868071 pmcid: 8635107
Socinski MA, Jotte RM, Cappuzzo F et al (2023) Association of immune-related adverse events with efficacy of atezolizumab in patients with non-small cell lung cancer: pooled analyses of the phase 3 IMpower130, IMpower132, and IMpower150 randomized clinical trials. JAMA Oncol 9:527–535. https://doi.org/10.1001/jamaoncol.2022.7711
doi: 10.1001/jamaoncol.2022.7711 pubmed: 36795388 pmcid: 9936386
de Filette J, Andreescu CE, Cools F, Bravenboer B, Velkeniers B (2019) A systematic review and meta-analysis of endocrine-related adverse events associated with immune checkpoint inhibitors. Horm Metab Res 51:145–156. https://doi.org/10.1055/a-0843-3366
doi: 10.1055/a-0843-3366 pubmed: 30861560
Khoja L, Day D, Wei-Wu Chen T, Siu LL, Hansen AR (2017) Tumour- and class-specific patterns of immune-related adverse events of immune checkpoint inhibitors: a systematic review. Ann Oncol 28:2377–2385. https://doi.org/10.1093/annonc/mdx286
doi: 10.1093/annonc/mdx286 pubmed: 28945858
Muir CA, Menzies AM, Clifton-Bligh R, Tsang VHM (2020) Thyroid toxicity following immune checkpoint inhibitor treatment in advanced cancer. Thyroid 30:1458–1469. https://doi.org/10.1089/thy.2020.0032
doi: 10.1089/thy.2020.0032 pubmed: 32264785
Dawidowska A, Jagodzinska-Mucha P, Koseła-Paterczyk H et al (2022) Immune-related thyroid adverse events predict response to PD-1 blockade in patients with melanoma Cancers (Basel) 14. https://doi.org/10.3390/cancers14051248
Lima Ferreira J, Costa C, Marques B et al (2021) Improved survival in patients with thyroid function test abnormalities secondary to immune-checkpoint inhibitors. Cancer Immunol Immunother 70:299–309. https://doi.org/10.1007/s00262-020-02664-y
doi: 10.1007/s00262-020-02664-y pubmed: 32712715
Muir CA, Clifton-Bligh RJ, Long GV et al (2021) Thyroid immune-related adverse events following immune checkpoint inhibitor treatment. J Clin Endocrinol Metab 106:e3704–e3713. https://doi.org/10.1210/clinem/dgab263
doi: 10.1210/clinem/dgab263 pubmed: 33878162
von Itzstein MS, Gonugunta AS, Wang Y et al (2022) Divergent prognostic effects of pre-existing and treatment-emergent thyroid dysfunction in patients treated with immune checkpoint inhibitors. Cancer Immunol Immunother 71:2169–2181. https://doi.org/10.1007/s00262-022-03151-2
doi: 10.1007/s00262-022-03151-2
Ellebaek E, Svane IM, Schmidt H et al (2021) The Danish metastatic melanoma database (DAMMED): a nation-wide platform for quality assurance and research in real-world data on medical therapy in Danish melanoma patients. Cancer Epidemiol 73:101943. https://doi.org/10.1016/j.canep.2021.101943
doi: 10.1016/j.canep.2021.101943 pubmed: 33962356
Kotwal A, Kottschade L, Ryder M (2020) PD-L1 inhibitor-induced thyroiditis is associated with better overall survival in cancer patients. Thyroid 30:177–184. https://doi.org/10.1089/thy.2019.0250
doi: 10.1089/thy.2019.0250 pubmed: 31813343 pmcid: 7047075
Zhang X, Wu Y, Lv J et al (2019) Nivolumab-induced thyroid dysfunctions in patients with previously treated non-small cell lung cancer. Interdiscip Sci 11:287–291. https://doi.org/10.1007/s12539-019-00337-8
doi: 10.1007/s12539-019-00337-8 pubmed: 31187431
Al Mushref M, Guido PA, Collichio FA, Moore DT, Clemmons DR (2020) Thyroid dysfunction, recovery, and prognosis in melanoma patients treated with immune checkpoint inhibitors: a retrospective review. Endocr Pract 26:36–42. https://doi.org/10.4158/ep-2019-0244
doi: 10.4158/ep-2019-0244 pubmed: 31461358
Schwartz LH, Litière S, de Vries E et al (2016) RECIST 1.1-update and clarification: from the RECIST committee. Eur J Cancer 62:132–137. https://doi.org/10.1016/j.ejca.2016.03.081
doi: 10.1016/j.ejca.2016.03.081 pubmed: 27189322 pmcid: 5737828
Lévesque LE, Hanley JA, Kezouh A, Suissa S (2010) Problem of immortal time bias in cohort studies: example using statins for preventing progression of diabetes. Bmj 340:b5087. https://doi.org/10.1136/bmj.b5087
doi: 10.1136/bmj.b5087 pubmed: 20228141
Yamauchi I, Yasoda A, Matsumoto S et al (2019) Incidence, features, and prognosis of immune-related adverse events involving the thyroid gland induced by nivolumab. PLoS One 14:e0216954. https://doi.org/10.1371/journal.pone.0216954
doi: 10.1371/journal.pone.0216954 pubmed: 31086392 pmcid: 6516638
Eggermont AMM, Kicinski M, Blank CU et al (2020) Association between immune-related adverse events and recurrence-free survival among patients with stage III melanoma randomized to receive pembrolizumab or placebo: a secondary analysis of a randomized clinical trial. JAMA Oncol 6:519–527. https://doi.org/10.1001/jamaoncol.2019.5570
doi: 10.1001/jamaoncol.2019.5570 pubmed: 31895407 pmcid: 6990933
Mangan BL, McAlister RK, Balko JM et al (2020) Evolving insights into the mechanisms of toxicity associated with immune checkpoint inhibitor therapy. Br J Clin Pharmacol 86:1778–1789. https://doi.org/10.1111/bcp.14433
doi: 10.1111/bcp.14433 pubmed: 32543711 pmcid: 7444794

Auteurs

Stine K Christensen (SK)

Department of Clinical Research, University of Southern Denmark, Odense, Denmark.

Mette L Winther (ML)

North Denmark Region, Aalborg, Denmark.

Ida J Laursen (IJ)

Department of Clinical Research, University of Southern Denmark, Odense, Denmark.

Freja S Madsen (FS)

Region of Southern Denmark, Odense, Denmark.

Carsten Brink (C)

Laboratory of Radiation Physics, Department of Oncology, Odense University Hospital, Odense, Denmark.

Thomas H Brix (TH)

Department of Endocrinology, Odense University Hospital, Odense, Denmark.

Eva Ellebaek (E)

Department of Oncology, National Center for Cancer Immune Therapy (CCIT-DK), Copenhagen University Hospital, Herlev, Denmark.

Inge Marie Svane (IM)

Department of Oncology, National Center for Cancer Immune Therapy (CCIT-DK), Copenhagen University Hospital, Herlev, Denmark.

Frederikke S Hansen (FS)

Department of Oncology, National Center for Cancer Immune Therapy (CCIT-DK), Copenhagen University Hospital, Herlev, Denmark.

Charlotte Haslund (C)

Department of Oncology, Aalborg University Hospital, Aalborg, Denmark.

Olivia K Laursen (OK)

Department of Oncology, Aalborg University Hospital, Aalborg, Denmark.

Henrik Schmidt (H)

Department of Oncology, Aarhus University Hospital, Aarhus, Denmark.

Ida D Larsen (ID)

Department of Oncology, Aarhus University Hospital, Aarhus, Denmark.

Lars Bastholt (L)

Department of Oncology, Odense University Hospital, Odense, Denmark.

Christina H Ruhlmann (CH)

Department of Clinical Research, University of Southern Denmark, Odense, Denmark. christina.ruhlmann@rsyd.dk.
Department of Oncology, Odense University Hospital, Odense, Denmark. christina.ruhlmann@rsyd.dk.

Classifications MeSH