Longitudinal liquid biopsy predicts clinical benefit from immunotherapy in advanced non-small cell lung cancer.
Journal
NPJ precision oncology
ISSN: 2397-768X
Titre abrégé: NPJ Precis Oncol
Pays: England
ID NLM: 101708166
Informations de publication
Date de publication:
17 Oct 2024
17 Oct 2024
Historique:
received:
09
01
2024
accepted:
11
09
2024
medline:
18
10
2024
pubmed:
18
10
2024
entrez:
17
10
2024
Statut:
epublish
Résumé
High heterogeneity in clinical benefit characterizes the use of immune checkpoint inhibitors (ICIs) in non-small cell lung cancer (NSCLC). We prospectively enrolled 113 advanced NSCLC patients treated with ICIs and performed liquid biopsy at the time of ICI start (T1), after 3 weeks (T2) and at the time of radiological evaluation (T3). Molecular variables were associated with outcome endpoints: cfDNA quantification, its dynamic change (∆T2-T1), variant allele frequency (VAF) of the gene with the highest frequency detected at baseline with NGS (maxVAF) and its dynamic change (∆T2-T1). At multivariate analysis, PD-L1 negativity, T1 cfDNA, cfDNA increase (∆T2-T1), and T2 VAF were significantly associated with shorter progression-free survival (PFS); PD-L1 negativity, squamous histology, T1 cfDNA, cfDNA (∆T2-T1) increase, and T2 maxVAF affected overall survival (OS). Among high PD-L1 expressing patients treated in first-line, elevated T2 maxVAF and cfDNA increase (∆T2-T1) correlated with worse PFS; higher T2 maxVAF and cfDNA increase (∆T2-T1) with worse OS. Derived integrated models were used to build nomograms and categorize different risk groups.
Identifiants
pubmed: 39420036
doi: 10.1038/s41698-024-00704-9
pii: 10.1038/s41698-024-00704-9
doi:
Types de publication
Journal Article
Langues
eng
Pagination
234Informations de copyright
© 2024. The Author(s).
Références
Hendriks, L. E. et al. Non-oncogene-addicted metastatic non-small-cell lung cancer: ESMO clinical practice guideline for diagnosis, treatment and follow-up. Ann. Oncol. 34, 358–376 (2023).
doi: 10.1016/j.annonc.2022.12.013
pubmed: 36669645
Govindan, R. et al. Society for immunotherapy of cancer (SITC) clinical practice guideline on immunotherapy for the treatment of lung cancer and mesothelioma. J. Immunother. Cancer 10, e003956 (2022).
doi: 10.1136/jitc-2021-003956
pmcid: 9157337
pubmed: 35640927
Hendriks, L. E. et al. Oncogene-addicted metastatic non-small-cell lung cancer: ESMO clinical practice guideline for diagnosis, treatment and follow-up☆. Ann. Oncol. 34, 339–357 (2023).
doi: 10.1016/j.annonc.2022.12.009
pubmed: 36872130
Reck, M. et al. Five-year outcomes with pembrolizumab versus chemotherapy for metastatic non-small-cell lung cancer With PD-L1 tumor proportion score ≥ 50. J. Clin. Oncol. 39, 2339–2349 (2021).
doi: 10.1200/JCO.21.00174
pmcid: 8280089
pubmed: 33872070
Gandhi, L. et al. Pembrolizumab plus chemotherapy in metastatic non-small-cell lung cancer. N. Engl. J. Med. 378, 2078–2092 (2018).
doi: 10.1056/NEJMoa1801005
Mok, T. S. K. 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. Lancet Lond. Engl. 393, 1819–1830 (2019).
doi: 10.1016/S0140-6736(18)32409-7
Paz-Ares, L. 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. Lancet Oncol. 22, 198–211 (2021).
doi: 10.1016/S1470-2045(20)30641-0
pubmed: 33476593
Herbst, R. S. et al. Atezolizumab for first-line treatment of PD-L1-selected patients with NSCLC. N. Engl. J. Med. 383, 1328–1339 (2020).
doi: 10.1056/NEJMoa1917346
pubmed: 32997907
Sezer, A. et al. Cemiplimab monotherapy for first-line treatment of advanced non-small-cell lung cancer with PD-L1 of at least 50%: a multicentre, open-label, global, phase 3, randomised, controlled trial. Lancet Lond. Engl. 397, 592–604 (2021).
doi: 10.1016/S0140-6736(21)00228-2
Paz-Ares, L. et al. Pembrolizumab plus chemotherapy for squamous non-small-cell lung cancer. N. Engl. J. Med. 379, 2040–2051 (2018).
doi: 10.1056/NEJMoa1810865
pubmed: 30280635
Ferrara, R. et al. Hyperprogressive disease in patients with advanced non-small cell lung cancer treated With PD-1/PD-L1 inhibitors or with single-agent chemotherapy. JAMA Oncol. 4, 1543–1552 (2018).
doi: 10.1001/jamaoncol.2018.3676
pmcid: 6248085
pubmed: 30193240
Peters, S. et al. OA03.05 analysis of early survival in patients with advanced non-squamous NSCLC treated with nivolumab vs docetaxel in CheckMate 057. J. Thorac. Oncol. 12, S253 (2017).
doi: 10.1016/j.jtho.2016.11.241
Zulato, E. et al. Longitudinal liquid biopsy anticipates hyperprogression and early death in advanced non-small cell lung cancer patients treated with immune checkpoint inhibitors. Br. J. Cancer 127, 2034–2042 (2022).
doi: 10.1038/s41416-022-01978-1
pmcid: 9681746
pubmed: 36175621
Hegde, P. S., Karanikas, V. & Evers, S. The where, the when, and the how of immune monitoring for cancer immunotherapies in the era of checkpoint inhibition. Clin. Cancer Res. 22, 1865–1874 (2016).
doi: 10.1158/1078-0432.CCR-15-1507
pubmed: 27084740
Waldman, A. D., Fritz, J. M. & Lenardo, M. J. A guide to cancer immunotherapy: from T cell basic science to clinical practice. Nat. Rev. Immunol. 20, 651–668 (2020).
doi: 10.1038/s41577-020-0306-5
pmcid: 7238960
pubmed: 32433532
Zulato, E. et al. Early assessment of KRAS mutation in cfDNA correlates with risk of progression and death in advanced non-small-cell lung cancer. Br. J. Cancer 123, 81–91 (2020).
doi: 10.1038/s41416-020-0833-7
pmcid: 7341732
pubmed: 32376889
Bonanno, L. et al. Liquid biopsy and non-small cell lung cancer: Are we looking at the tip of the iceberg? Br. J. Cancer 127, 383–393 (2022).
doi: 10.1038/s41416-022-01777-8
pmcid: 9345955
pubmed: 35264788
Richards, S. et al. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet. Med. 17, 405–424 (2015).
doi: 10.1038/gim.2015.30
pmcid: 4544753
pubmed: 25741868
Eisenhauer, E. A. et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer 45, 228–247 (2009).
doi: 10.1016/j.ejca.2008.10.026
pubmed: 19097774
Champiat, S. et al. Hyperprogressive disease is a new pattern of progression in cancer patients treated by anti-PD-1/PD-L1. Clin. Cancer Res. 23, 1920–1928 (2017).
doi: 10.1158/1078-0432.CCR-16-1741
pubmed: 27827313
Merker, J. D. et al. Circulating tumor DNA analysis in patients with cancer: American Society of Clinical Oncology and College of American Pathologists Joint Review. J. Clin. Oncol. 36, 1631–1641 (2018).
doi: 10.1200/JCO.2017.76.8671
pubmed: 29504847
Siravegna, G., Marsoni, S., Siena, S. & Bardelli, A. Integrating liquid biopsies into the management of cancer. Nat. Rev. Clin. Oncol. 14, 531–548 (2017).
doi: 10.1038/nrclinonc.2017.14
pubmed: 28252003
Wan, J. C. M. et al. Liquid biopsies come of age: towards implementation of circulating tumour DNA. Nat. Rev. Cancer 17, 223–238 (2017).
doi: 10.1038/nrc.2017.7
pubmed: 28233803
Sivapalan, L. et al. Liquid biopsy approaches to capture tumor evolution and clinical outcomes during cancer immunotherapy. J. Immunother. Cancer 11, e005924 (2023).
doi: 10.1136/jitc-2022-005924
pmcid: 9853269
pubmed: 36657818
Cabel, L. et al. Circulating tumor DNA changes for early monitoring of anti-PD1 immunotherapy: a proof-of-concept study. Ann. Oncol. 28, 1996–2001 (2017).
doi: 10.1093/annonc/mdx212
pubmed: 28459943
Raja, R. et al. Early reduction in ctDNA predicts survival in patients with lung and bladder cancer treated with durvalumab. Clin. Cancer Res. 24, 6212–6222 (2018).
doi: 10.1158/1078-0432.CCR-18-0386
pubmed: 30093454
Hwang, M. et al. Peripheral blood immune cell dynamics reflect antitumor immune responses and predict clinical response to immunotherapy. J. Immunother. Cancer 10, e004688 (2022).
doi: 10.1136/jitc-2022-004688
pmcid: 9189831
pubmed: 35688557
Assaf, Z. J. F. et al. A longitudinal circulating tumor DNA-based model associated with survival in metastatic non-small-cell lung cancer. Nat. Med. 29, 859–868 (2023).
doi: 10.1038/s41591-023-02226-6
pmcid: 10115641
pubmed: 36928816
Vega, D. M. et al. Changes in circulating tumor DNA reflect clinical benefit across multiple studies of patients with non-small-cell lung cancer treated with immune checkpoint inhibitors. JCO Precis. Oncol. https://doi.org/10.1200/PO.21.00372 (2022).
Anagnostou, V. et al. ctDNA response after pembrolizumab in non-small cell lung cancer: phase 2 adaptive trial results. Nat. Med. 29, 2559–2569 (2023).
doi: 10.1038/s41591-023-02598-9
pmcid: 10579094
pubmed: 37814061
Pavan, A. et al. Role of next generation sequencing-based liquid biopsy in advanced non-small cell lung cancer patients treated with immune checkpoint inhibitors: impact of STK11, KRAS and TP53 mutations and co-mutations on outcome. Transl. Lung Cancer Res. 10, 202–220 (2021).
doi: 10.21037/tlcr-20-674
pmcid: 7867770
pubmed: 33569305
Lim, T. K. H. et al. KRAS G12C in advanced NSCLC: prevalence, co-mutations, and testing. Lung Cancer 184, 107293 (2023).
doi: 10.1016/j.lungcan.2023.107293
pubmed: 37683526
Skoulidis, F. et al. STK11/LKB1 mutations and PD-1 inhibitor resistance in KRAS-mutant lung adenocarcinoma. Cancer Discov. 8, 822–835 (2018).
doi: 10.1158/2159-8290.CD-18-0099
pmcid: 6030433
Ricciuti, B. et al. Diminished efficacy of programmed death-(Ligand)1 inhibition in STK11- and KEAP1-mutant lung adenocarcinoma is affected by KRAS mutation status. J. Thorac. Oncol. 17, 399–410 (2022).
doi: 10.1016/j.jtho.2021.10.013