Immune-checkpoint inhibition for resectable non-small-cell lung cancer - opportunities and challenges.
Journal
Nature reviews. Clinical oncology
ISSN: 1759-4782
Titre abrégé: Nat Rev Clin Oncol
Pays: England
ID NLM: 101500077
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
accepted:
19
06
2023
medline:
22
9
2023
pubmed:
25
7
2023
entrez:
24
7
2023
Statut:
ppublish
Résumé
Therapeutic strategies harnessing the immune system to eliminate tumour cells have been successfully used for several cancer types, including in patients with advanced-stage non-small-cell lung cancer (NSCLC). In these patients, immune-checkpoint inhibitors (ICIs) can provide durable responses and improve overall survival either as monotherapy, or combined with chemotherapy or other immunotherapeutic agents. However, the implementation of ICIs in early stage NSCLC has been hampered by the continuous struggle to develop robust end points to assess their efficacy in this setting, especially those enabling a fast and reproducible evaluation of the clinical activity of neoadjuvant strategies. Several trials are testing ICIs, alone or in combination with chemotherapy, in early stage NSCLC as an adjuvant, neoadjuvant or perioperative approach. As a novelty, most trials in the neoadjuvant setting have adopted pathological response as a primary end point. ICIs have been approved for use in the neoadjuvant and adjuvant settings on the basis of event-free survival and disease-free survival benefit, respectively; however, the correlation of these end points with overall survival remains unclear in these settings. Unresolved challenges for the optimal use of ICIs with curative intent include concerns about their applicability in daily clinical practice and about improving patient selection based on predictive biomarkers or assessment of pathological response and minimal residual disease. In this Review, we discuss the rationale, available strategies and current trial landscape for the implementation of ICIs in patients with resectable NSCLC, and we further elaborate on future approaches to optimize their clinical benefit.
Identifiants
pubmed: 37488229
doi: 10.1038/s41571-023-00794-7
pii: 10.1038/s41571-023-00794-7
doi:
Substances chimiques
Immune Checkpoint Inhibitors
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
664-677Informations de copyright
© 2023. Springer Nature Limited.
Références
Reck, M., Remon, J. & Hellmann, M. D. First-line immunotherapy for non-small-cell lung cancer. J. Clin. Oncol. 40, 586–597 (2022).
pubmed: 34985920
doi: 10.1200/JCO.21.01497
Spigel, D. R. et al. Five-year survival outcomes from the PACIFIC trial: durvalumab after chemoradiotherapy in stage III non-small-cell lung cancer. J. Clin. Oncol. 40, 1301–1311 (2022).
pubmed: 35108059
pmcid: 9015199
doi: 10.1200/JCO.21.01308
Schmid, P. et al. Pembrolizumab for early triple-negative breast cancer. N. Engl. J. Med. 382, 810–821 (2020).
pubmed: 32101663
doi: 10.1056/NEJMoa1910549
Kelly, R. J. et al. Adjuvant nivolumab in resected esophageal or gastroesophageal junction cancer. N. Engl. J. Med. 384, 1191–1203 (2021).
pubmed: 33789008
doi: 10.1056/NEJMoa2032125
Choueiri, T. K. et al. Adjuvant pembrolizumab after nephrectomy in renal-cell carcinoma. N. Engl. J. Med. 385, 683–694 (2021).
pubmed: 34407342
doi: 10.1056/NEJMoa2106391
Bajorin, D. F. et al. Adjuvant nivolumab versus placebo in muscle-invasive urothelial carcinoma. N. Engl. J. Med. 384, 2102–2114 (2021).
pubmed: 34077643
pmcid: 8215888
doi: 10.1056/NEJMoa2034442
Weber, J. et al. Adjuvant nivolumab versus ipilimumab in resected stage III or IV melanoma. N. Engl. J. Med. 377, 1824–1835 (2017).
pubmed: 28891423
doi: 10.1056/NEJMoa1709030
Eggermont, A. M. M. et al. Adjuvant pembrolizumab versus placebo in resected stage III melanoma. N. Engl. J. Med. 378, 1789–1801 (2018).
pubmed: 29658430
doi: 10.1056/NEJMoa1802357
Patel, S. P. et al. Neoadjuvant–adjuvant or adjuvant-only pembrolizumab in advanced melanoma. N. Engl. J. Med. 388, 813–823 (2023).
pubmed: 36856617
pmcid: 10410527
doi: 10.1056/NEJMoa2211437
Cascone, T. et al. Superior efficacy of neoadjuvant compared to adjuvant immune checkpoint blockade in non-small cell lung cancer [abstract]. Cancer Res. 78 (Suppl. 13), 1719 (2018).
doi: 10.1158/1538-7445.AM2018-1719
Vansteenkiste, J. F. et al. Efficacy of the MAGE-A3 cancer immunotherapeutic as adjuvant therapy in patients with resected MAGE-A3-positive non-small-cell lung cancer (MAGRIT): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 17, 822–835 (2016).
pubmed: 27132212
doi: 10.1016/S1470-2045(16)00099-1
Vansteenkiste, J. et al. Current status of immune checkpoint inhibition in early-stage NSCLC. Ann. Oncol. 30, 1244–1253 (2019).
pubmed: 31143921
doi: 10.1093/annonc/mdz175
Pignon, J. P. et al. Lung adjuvant cisplatin evaluation: a pooled analysis by the LACE Collaborative Group. J. Clin. Oncol. 26, 3552–3559 (2006).
doi: 10.1200/JCO.2007.13.9030
Bakos, O. et al. Combining surgery and immunotherapy: turning an immunosuppressive effect into a therapeutic opportunity. J. Immunother. Cancer 6, 86 (2018).
pubmed: 30176921
pmcid: 6122574
doi: 10.1186/s40425-018-0398-7
Matzner, P. et al. Harnessing cancer immunotherapy during the unexploited immediate perioperative period. Nat. Rev. Clin. Oncol. 17, 313–326 (2020).
pubmed: 32066936
doi: 10.1038/s41571-019-0319-9
Chaft, J. E. et al. Evolution of systemic therapy for stages I-III non-metastatic non-small-cell lung cancer. Nat. Rev. Clin. Oncol. 18, 547–557 (2021).
pubmed: 33911215
pmcid: 9447511
doi: 10.1038/s41571-021-00501-4
Sharma, S. et al. Tumor cyclooxygenase-2/prostaglandin E-2-dependent promotion of FOXP3 expression and CD4
pubmed: 15958566
doi: 10.1158/0008-5472.CAN-05-0141
Topalian, S. L., Taube, J. M. & Pardoll, D. M. Neoadjuvant checkpoint blockade for cancer immunotherapy. Science 367, eaax0182 (2020).
pubmed: 32001626
pmcid: 7789854
doi: 10.1126/science.aax0182
McGranahan, N. et al. Clonal neoantigens elIicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science 351, 1463–1469 (2016).
pubmed: 26940869
pmcid: 4984254
doi: 10.1126/science.aaf1490
Liu, J. et al. Improved efficacy of neoadjuvant compared to adjuvant immunotherapy to eradicate metastatic disease. Cancer Discov. 6, 1382–1399 (2016).
pubmed: 27663893
doi: 10.1158/2159-8290.CD-16-0577
Martín-Ruiz, A. et al. Effects of anti-PD-1 immunotherapy on tumor regression: insights from a patient-derived xenograft model. Sci. Rep. 10, 7078 (2020).
pubmed: 32341383
pmcid: 7184589
doi: 10.1038/s41598-020-63796-w
Forde, P. M. et al. Neoadjuvant PD-1 blockade in resectable lung cancer. N. Engl. J. Med. 378, 1976–1986 (2018).
pubmed: 29658848
pmcid: 6223617
doi: 10.1056/NEJMoa1716078
Rosner, S. et al. Neoadjuvant nivolumab in early-stage non-small cell lung cancer (NSCLC): five-year outcomes [abstract]. J. Clin. Oncol. 40 (Suppl. 16), 8537 (2022).
doi: 10.1200/JCO.2022.40.16_suppl.8537
Hellmann, M. D. et al. Pathological response after neoadjuvant chemotherapy in resectable non-small-cell lung cancers: proposal for the use of major pathological response as a surrogate endpoint. Lancet Oncol. 15, e42–e50 (2014).
pubmed: 24384493
pmcid: 4734624
doi: 10.1016/S1470-2045(13)70334-6
Cascone, T. et al. Neoadjuvant chemotherapy plus nivolumab with or without ipilimumab in operable non-small cell lung cancer: the phase 2 platform NEOSTAR trial. Nat. Med. 29, 593–604 (2023).
pubmed: 36928818
pmcid: 10033402
doi: 10.1038/s41591-022-02189-0
Chaft, J. E. et al. Neoadjuvant atezolizumab for resectable non-small cell lung cancer: an open-label, single-arm phase II trial. Nat. Med. 28, 2155–2161 (2022).
pubmed: 36097216
pmcid: 9556329
doi: 10.1038/s41591-022-01962-5
Besse, B. et al. Neoadjuvant atezolizumab (A) for resectable non-small cell lung cancer (NSCLC): results from the phase II PRINCEPS trial [abstract 1215O - SC]. Ann. Oncol. 31(S4), S794–S795 (2020).
doi: 10.1016/j.annonc.2020.08.1417
Wislez, M. et al. Neoadjuvant durvalumab for resectable non- small-cell lung cancer (NSCLC): results from a multicenter study (IFCT-1601 IONESCO). J. Immunother. Cancer 10, e005636 (2022).
pubmed: 36270733
pmcid: 9594538
doi: 10.1136/jitc-2022-005636
Zhang, F. et al. Three-year follow-up of neoadjuvant programmed cell death protein-1 inhibitor (sintilimab) in NSCLC. J. Thorac. Oncol. 17, 909–920 (2022).
pubmed: 35550174
doi: 10.1016/j.jtho.2022.04.012
Rusch, W. et al. Surgical results of the Lung Cancer Mutation Consortium 3 trial: a phase II multicenter single-arm study to investigate the efficacy and safety of atezolizumab as neoadjuvant therapy in patients with stages IB-select IIIB resectable non-small cell lung cancer. J. Thorac. Cardiovasc. Surg. 165, 828–839.e6 (2023).
doi: 10.1016/j.jtcvs.2022.10.007
Cascone, T. et al. Neoadjuvant nivolumab or nivolumab plus ipilimumab in operable non-small cell lung cancer: the phase 2 randomized NEOSTAR trial. Nat. Med. 27, 504–514 (2021).
pubmed: 33603241
pmcid: 8818318
doi: 10.1038/s41591-020-01224-2
Aigner, C. et al. Surgical outcomes of patients with resectable non-small-cell lung cancer receiving neoadjuvant immunotherapy with nivolumab plus relatlimab or nivolumab: findings from the prospective, randomized, multicentric phase II study NEOpredict-Lung [abstract]. J. Clin. Oncol. 41 (Suppl. 16), 8500 (2023).
doi: 10.1200/JCO.2023.41.16_suppl.8500
Reuss, J. E. et al. Neoadjuvant nivolumab plus ipilimumab in resectable non-small cell lung cancer. J. Immunother. Cancer 8, e001282 (2020).
pubmed: 32929052
pmcid: 7488786
doi: 10.1136/jitc-2020-001282
Mok, T. S. K. et al. CANOPY-N: A phase II trial of canakinumab (CAN) or pembrolizumab (PEM), alone or in combination, as neoadjuvant therapy in patients (pts) with resectable stage Ib–IIIa non-small-cell lung cancer [abstract LBA4]. Ann. Oncol. 33 (Suppl. 9), S1547–S1548 (2022).
doi: 10.1016/j.annonc.2022.10.322
Reckamp, K. L. et al. Phase II randomized study of ramucirumab and pembrolizumab versus standard of care in advanced non-small-cell lung cancer previously treated with immunotherapy – Lung-MAP S1800A. J. Clin. Oncol. 40, 2295–2306 (2022).
pubmed: 35658002
pmcid: 9287284
doi: 10.1200/JCO.22.00912
Aokage, K. et al. Pembrolizumab and ramucirumab neoadjuvant therapy for PD-L1-positive stage IB-IIIA lung cancer (EAST ENERGY) [abstract]. J. Clin. Oncol. 41 (Suppl. 16), 8509 (2023).
doi: 10.1200/JCO.2023.41.16_suppl.8509
Rothschild, S. I. et al. SAKK 16/14: durvalumab in addition to neoadjuvant chemotherapy in patients with stage IIIA(N2) non-small-cell lung cancer – a multicenter single-arm phase II trial. J. Clin. Oncol. 39, 2872–2880 (2021).
pubmed: 34251873
doi: 10.1200/JCO.21.00276
Zhang, P. et al. Neoadjuvant sintilimab and chemotherapy for resectable stage IIIA non-small cell lung cancer. Ann. Thorac. Surg. 22, 949–958 (2022).
doi: 10.1016/j.athoracsur.2022.01.039
Shu, C. A. et al. Neoadjuvant atezolizumab and chemotherapy in patients with resectable non-small-cell lung cancer: an open-label, multicentre, single-arm, phase 2 trial. Lancet Oncol. 21, 786–795 (2020).
pubmed: 32386568
doi: 10.1016/S1470-2045(20)30140-6
Provencio, M. et al. Neoadjuvant chemotherapy and nivolumab in resectable non-small-cell lung cancer (NADIM): an open-label, multicentre, single-arm, phase 2 trial. Lancet Oncol. 21, 1413–1422 (2020).
pubmed: 32979984
doi: 10.1016/S1470-2045(20)30453-8
Provencio, M. et al. Overall survival and biomarker analysis of neoadjuvant nivolumab plus chemotherapy in operable stage IIIA non-small-cell lung cancer (NADIM phase II trial). J. Clin. Oncol. 40, 2924–2933 (2022).
pubmed: 35576508
pmcid: 9426809
doi: 10.1200/JCO.21.02660
Provencio, M. et al. Perioperative nivolumab and chemotherapy in stage III non-small-cell lung cancer. New. Engl. J. Med., https://doi.org/10.1056/NEJMoa2215530 (2023).
doi: 10.1056/NEJMoa2215530
pubmed: 37379158
Forde, P. M. et al. Neoadjuvant nivolumab plus chemotherapy in resectable lung cancer. N. Engl. J. Med. 386, 1973–1985 (2022).
pubmed: 35403841
pmcid: 9844511
doi: 10.1056/NEJMoa2202170
Heymach, J. et al. AEGEAN: a phase 3 trial of neoadjuvant durvalumab + chemotherapy followed by adjuvant durvalumab in patients with resectable NSCLC [abstract]. Cancer Res. 83 (Suppl. 8), CT005 (2023).
doi: 10.1158/1538-7445.AM2023-CT005
Lu, S. et al. Perioperative toripalimab + platinum-doublet chemotherapy vs chemotherapy in resectable stage II/III non-small cell lung cancer (NSCLC): interim event-free survival (EFS) analysis of the phase III Neotorch study [abstract]. J. Clin. Oncol. 41 (Suppl. 36), 425126 (2023).
doi: 10.1200/JCO.2023.41.36_suppl.425126
Wakelee, H. et al. Perioperative pembrolizumab for early-stage non-small-cell lung cancer. N. Engl. J. Med. https://doi.org/10.1056/NEJMoa2302983 (2023).
doi: 10.1056/NEJMoa2302983
pubmed: 37272513
US Food and Drug Administration. FDA approves neoadjuvant nivolumab and platinum-doublet chemotherapy for early-stage non-small cell lung cancer. FDA https://www.fda.gov/drugs/resources-information-approved-drugs/fda-approves-neoadjuvant-nivolumab-and-platinum-doublet-chemotherapy-early-stage-non-small-cell-lung (2022).
Forde, P. M. et al. Neoadjuvant nivolumab (N) + platinum-doublet chemotherapy (C) for resectable NSCLC: 3-y update from CheckMate 816 [abstract 84O]. J. Thorac. Oncol. 18 (Suppl. 4), S89–S90 (2023).
doi: 10.1016/S1556-0864(23)00338-6
Spicer, J. et al. Clinical outcomes with neoadjuvant nivolumab (N) + chemotherapy (C) vs C by definitive surgery in patients (pts) with resectable NSCLC: 3-y results from the phase 3 CheckMate 816 trial. J. Clin. Oncol. 41, 8521 (2023).
doi: 10.1200/JCO.2023.41.16_suppl.8521
Qiu, F. et al. Two cycles versus three cycles of neoadjuvant sintilimab plus platinum-doublet chemotherapy in patients with resectable non-small-cell lung cancer (neoSCORE): a randomized, single center, two-arm phase II trial [abstract]. J. Clin. Oncol. 40 (Suppl. 16), 8500 (2022).
doi: 10.1200/JCO.2022.40.16_suppl.8500
Altorki, N. K. et al. Neoadjuvant durvalumab with or without stereotactic body radiotherapy in patients with early-stage non-small-cell lung cancer: a single-centre, randomised phase 2 trial. Lancet Oncol. 22, 824–835 (2021).
pubmed: 34015311
doi: 10.1016/S1470-2045(21)00149-2
US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT03924869 (2023).
Felip, E. et al. Adjuvant atezolizumab after adjuvant chemotherapy in resected stage IB-IIIA non-small-cell lung cancer (IMpower 010): a randomised, multicentre, open-label, phase 3 trial. Lancet 398, 1344–1357 (2021).
pubmed: 34555333
doi: 10.1016/S0140-6736(21)02098-5
Paz-Ares, L. et al. Pembrolizumab (pembro) versus placebo for early-stage non-small cell lung cancer (NSCLC) following complete resection and adjuvant chemotherapy (chemo) when indicated: randomized, triple-blind, phase III EORTC-1416-LCG/ETOP 8-15 – PEARLS/KEYNOTE-091 study [abstract VP3-2022]. Ann. Oncol. 33, 451–453 (2022).
doi: 10.1016/j.annonc.2022.02.224
US Food and Drug Administration. FDA approves atezolizumab as adjuvant treatment for non-small cell lung cancer. FDA https://www.fda.gov/drugs/resources-information-approved-drugs/fda-approves-atezolizumab-adjuvant-treatment-non-small-cell-lung-cancer (2023).
Felip, E. et al. IMpower010: Sites of relapse and subsequent therapy from a phase III study of atezolizumab vs best supportive care after adjuvant chemotherapy in stage IB-IIIA NSCLC [abstract LBA9]. Ann. Oncol. 32 (Suppl. 5), S1319 (2021).
doi: 10.1016/j.annonc.2021.08.2120
European Medicines Agency. Tecentriq: atezolizumab. European Medicines Agency https://www.ema.europa.eu/en/documents/smop/chmp-post-authorisation-summary-opinion-tecentriq-ii-64_en.pdf (2022).
Wakelee, H. et al. IMpower010: Overall survival interim analysis of a phase III study of atezolizumab vs best supportive care in resected NSCLC [abstract PL03.09]. J. Thorac. Oncol. 17 (Suppl. 9), S2 (2022).
doi: 10.1016/j.jtho.2022.07.013
O’Brien, M. et al. EORTC-1416-LCG/ETOP 8-15 – PEARLS/KEYNOTE-091 study of pembrolizumab versus placebo for completely resected early-stage non-small cell lung cancer (NSCLC): outcomes in subgroups related to surgery, disease burden, and adjuvant chemotherapy use [abstract]. J. Clin. Oncol. 40 (Suppl. 16), 8512 (2022).
doi: 10.1200/JCO.2022.40.16_suppl.8512
US National Library of Medicine.ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT04385368 (2023).
US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT04642469 (2023).
Garon, E. et al. CANOPY-A: A phase III study of canakinumab (CAN) as adjuvant therapy in patients (pts) with surgically resected non-small cell lung cancer (NSCLC) [abstract LBA49]. Ann. Oncol. 33 (Suppl. 7), S1414–S1415 (2022).
doi: 10.1016/j.annonc.2022.08.049
Rami-Porta, R., Wittekind, C. & Goldstraw, P. International Association for the Study of Lung Cancer Staging Committee Complete resection in lung cancer surgery: proposed definition. Lung Cancer 49, 25–33 (2005).
pubmed: 15949587
doi: 10.1016/j.lungcan.2005.01.001
Allaeys, T., Berzenji, L. & Schil, Van P. E. Surgery after induction targeted therapy and immunotherapy for lung cancer. Cancers 13, 2603 (2021).
pubmed: 34073302
pmcid: 8199385
doi: 10.3390/cancers13112603
Bott, M. J. et al. Initial results of pulmonary resection after neoadjuvant nivolumab in patients with resectable non-small cell lung cancer. J. Thorac. Cardiovasc. Surg. 158, 269–276 (2019).
pubmed: 30718052
doi: 10.1016/j.jtcvs.2018.11.124
Provencio, M., Calvo, V., Romero, A., Spicer, J. D. & Cruz-Bermudez, A. Treatment sequencing in resectable lung cancer: the good and the bad of adjuvant versus neoadjuvant therapy. Am. Soc. Clin. Oncol. Educ. Book 42, 1–18 (2022).
pubmed: 35561296
Felip, E. et al. Preoperative chemotherapy plus surgery versus surgery plus adjuvant chemotherapy versus surgery alone in early-stage non-small-cell lung cancer. J. Clin. Oncol. 28, 3138–3145 (2010).
pubmed: 20516435
doi: 10.1200/JCO.2009.27.6204
Kehl, K. L. et al. Rates of guideline-concordant surgery and adjuvant chemotherapy among patients with early-stage lung cancer in the US Alchemist study. JAMA Oncol. 8, 717–728 (2022).
pubmed: 35297944
pmcid: 8931674
doi: 10.1001/jamaoncol.2022.0039
Carbone et al. Updated survival, efficacy and safety of adjuvant (adj) atezolizumab (atezo) after neoadjuvant (neoadj) atezo in the phase II LCMC3 study [abstract 145MO]. J. Thorac. Oncol. 18 (Suppl. 4), S90–S91 (2023).
doi: 10.1016/S1556-0864(23)00339-8
Mazieres, J. et al. Immune checkpoint inhibitors for patients with advanced lung cancer and oncogenic driver alterations: results from the IMMUNOTARGET registry. Ann. Oncol. 30, 1321–1328 (2019).
pubmed: 31125062
pmcid: 7389252
doi: 10.1093/annonc/mdz167
Ghamati, M. R. et al. Surgery without preoperative histological confirmation of lung cancer: what is the current clinical practice? J. Thorac. Dis. 13, 5765–5775 (2021).
pubmed: 34795925
pmcid: 8575862
doi: 10.21037/jtd-21-617
Moding, E. J. et al. Circulating tumor DNA dynamics predict benefit from consolidation immunotherapy in locally advanced non-small cell lung cancer. Nat. Cancer 1, 176–183 (2020).
pubmed: 34505064
pmcid: 8425388
doi: 10.1038/s43018-019-0011-0
Anagnostou, V. et al. Dynamics of tumor and immune responses during immune checkpoint blockade in non-small cell lung cancer. Cancer Res. 79, 1214–1225 (2019).
pubmed: 30541742
doi: 10.1158/0008-5472.CAN-18-1127
Goldberg, S. B. et al. Early assessment of lung cancer immunotherapy response via circulating tumor DNA. Clin. Cancer Res. 24, 1872–1880 (2018).
pubmed: 29330207
pmcid: 5899677
doi: 10.1158/1078-0432.CCR-17-1341
Nabet, B. Y. et al. Noninvasive early identification of therapeutic benefit from immune checkpoint inhibition. Cell 183, 363–376 (2020).
pubmed: 33007267
pmcid: 7572899
doi: 10.1016/j.cell.2020.09.001
Abbosh, C. et al. Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution. Nature 545, 446–451 (2017).
pubmed: 28445469
pmcid: 5812436
doi: 10.1038/nature22364
Xia, L. et al. Perioperative ctDNA-based molecular residual disease detection for non-small cell lung cancer: a prospective multicenter cohort study (LUNGCA-1). Clin. Cancer Res. 28, 3308–3317 (2022).
pubmed: 34844976
doi: 10.1158/1078-0432.CCR-21-3044
Zhang, J. T. et al. Longitudinal undetectable molecular residual disease defines potentially cured population in localized non-small cell lung cancer. Cancer Discov. 12, 1690–1701 (2022).
pubmed: 35543554
pmcid: 9394392
doi: 10.1158/2159-8290.CD-21-1486
Tie, J. et al. Circulating tumor DNA analysis guiding adjuvant therapy in stage II colon cancer. N. Engl. J. Med. 386, 2261–2272 (2022).
pubmed: 35657320
pmcid: 9701133
doi: 10.1056/NEJMoa2200075
Kim, E. S. et al. Blood-based tumor mutational burden as a biomarker for atezolizumab in non-small cell lung cancer: the phase 2 B-F1RST trial. Nat. Med. 28, 939–945 (2022).
pubmed: 35422531
pmcid: 9117143
doi: 10.1038/s41591-022-01754-x
Kris, M. G. et al. Dynamic circulating tumour DNA (ctDNA) response to neoadjuvant atezolizumab and surgery and association with outcomes in patients with NSCLC. Ann. Oncol. 32, S1373–S1391 (2021).
doi: 10.1016/j.annonc.2021.10.017
Chen, K. et al. Perioperative dynamic changes in circulating tumor DNA in patients with lung cancer (DYNAMIC). Clin. Cancer Res. 25, 7058–7067 (2019).
pubmed: 31439586
doi: 10.1158/1078-0432.CCR-19-1213
Zhou, C. et al. IMpower010: Biomarkers of disease-free survival (DFS) in a phase 3 study of atezolizumab (atezo) vs best supportive care (BSC) after adjuvant chemotherapy in stage IB-IIIA NSCLC [abstract 2O]. Ann. Oncol. 32 (Suppl. 7), S1374 (2021).
doi: 10.1016/j.annonc.2021.10.018
West, H. J. et al. Clinical efficacy of atezolizumab plus bevacizumab and chemotherapy in KRAS-mutated non-small cell lung cancer with STK11, KEAP1, or TP53 comutations: subgroup results from the phase III IMpower150 trial. J. Immunother. Cancer 10, e003027 (2022).
pubmed: 35190375
pmcid: 8862451
doi: 10.1136/jitc-2021-003027
Herbst, R. S. et al. Adjuvant osimertinib for resected EGFR-mutated stage IB-IIIA non-small-cell lung cancer: updated results from the phase III randomized ADAURA trial. J. Clin. Oncol. 41, 1830–1840 (2023).
pubmed: 36720083
pmcid: 10082285
doi: 10.1200/JCO.22.02186
Tsuboi, M. et al. Overall survival with osimertinib in resected EGFR-mutated NSCLC. N. Engl. J. Med. https://doi.org/10.1056/NEJMoa2304594 (2023).
doi: 10.1056/NEJMoa2304594
pubmed: 37272535
Wu, Y.-L. et al. Osimertinib in resected EGFR-mutated non-small-cell lung cancer. N. Engl. J. Med. 383, 1711–1723 (2020).
pubmed: 32955177
doi: 10.1056/NEJMoa2027071
Liu, S. Y. et al. Perioperative targeted therapy for oncogene-driven NSCLC. Lung Cancer 172, 160–169 (2022).
pubmed: 35644704
doi: 10.1016/j.lungcan.2022.05.007
Mielgo-Rubio, X. et al. Targeted therapy moves to earlier stages of non-small-cell lung cancer: emerging evidence, controversies and future challenges. Future Oncol. 17, 4011–4025 (2021).
pubmed: 34337973
doi: 10.2217/fon-2020-1255
Waterhouse, D. M. et al. Continuous versus 1-year fixed-duration nivolumab in previously treated advanced non-small-cell lung cancer: CheckMate 153. J. Clin. Oncol. 38, 3863–3873 (2020).
pubmed: 32910710
pmcid: 7676888
doi: 10.1200/JCO.20.00131
Zalcman, G. et al. Nivolumab (Nivo) plus ipilimumab (Ipi) 6-months treatment versus continuation in patients with advanced non-small cell lung cancer (aNSCLC): results of the randomized IFCT-1701 phase III trial [abstract 972O]. Ann. Oncol. 33 (Suppl. 7), S992 (2022).
doi: 10.1016/j.annonc.2022.07.1100
Brahmer, J. R. et al. Five-year survival outcomes with nivolumab plus ipilimumab versus chemotherapy as first-line treatment for metastatic non-small cell lung cancer in CheckMate 227. J. Clin. Oncol. 41, 1200–1212 (2023).
pubmed: 36223558
doi: 10.1200/JCO.22.01503
Betticher, D. C. et al. Cisplatin neoadjuvant chemotherapy is prognostic of survival in patients with stage IIIA pN2 non-small-cell lung cancer: a multicenter phase II trial. J. Clin. Oncol. 21, 1752–1759 (2003).
pubmed: 12721251
doi: 10.1200/JCO.2003.11.040
Depierre, A. et al. Preoperative chemotherapy followed by surgery compared with primary surgery in resectable stage I (except T1N0), II, and IIIa non-small-cell lung cancer. J. Clin. Oncol. 20, 247–253 (2002).
pubmed: 11773176
Betticher, D. C. et al. Prognostic factors affecting long-term outcomes in patients with resected stage IIIA pN2 non-small-cell lung cancer: 5-year follow-up of a phase II study. Br. J. Cancer 94, 1099–1106 (2006).
pubmed: 16622435
pmcid: 2361244
doi: 10.1038/sj.bjc.6603075
Mouillet, G. et al. Pathologic complete response to preoperative chemotherapy predicts cure in early-stage non-small-cell lung cancer: combined analysis of two IFCT randomized trials. J. Thorac. Oncol. 7, 841–849 (2012).
pubmed: 22722786
doi: 10.1097/JTO.0b013e31824c7d92
Liao, W.-Y. et al. Neoadjuvant chemotherapy with docetaxel-cisplatin in patients with stage III N2 non-small-cell lung cancer. Clin. Lung Cancer 14, 418–424 (2013).
pubmed: 23291258
doi: 10.1016/j.cllc.2012.10.003
Dacic, S. et al. Artificial intelligence (AI)-powered pathologic response (PathR) assessment of resection specimens after neoadjuvant atezolizumab in patients with non-small cell lung cancer: results from the LCMC3 study [abstract]. J. Clin. Oncol. 39 (Suppl. 15), 106 (2021).
doi: 10.1200/JCO.2021.39.15_suppl.106
Sheth, S. et al. Durvalumab activity in previously treated patients who stopped durvalumab without disease progression. J. Immunother. Cancer 8, e000650 (2020).
pubmed: 32847985
pmcid: 7451272
doi: 10.1136/jitc-2020-000650
Rodriguez-Abreu, D. et al. Pooled analysis of outcomes with second-course pembrolizumab across 5 phase 3 studies of non-small-cell lung cancer. J. Thorac. Oncol. 17, S42–S43 (2022).
doi: 10.1016/j.jtho.2022.07.075
Akamatsu, H. et al. Nivolumab re-treatment in non-small cell lung cancer patients who responded to prior immune-checkpoint inhibitors and had ICI-free intervals (WJOG9616L). Clin. Cancer Res. https://doi.org/10.1158/1078-0432.CCR-22-0602 (2022).
doi: 10.1158/1078-0432.CCR-22-0602
pubmed: 35762926
pmcid: 9662947
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 multicenter, open-label, global, phase 3, randomised, controlled trial. Lancet 397, 592–604 (2021).
pubmed: 33581821
doi: 10.1016/S0140-6736(21)00228-2
Muthusamy, B. et al. Quantifying the value of multigene testing in resected early-stage lung adenocarcinoma. J. Thorac. Oncol. 18, 476–486 (2023).
pubmed: 36494074
doi: 10.1016/j.jtho.2022.11.027
Gao, S. et al. Neoadjuvant PD-1 inhibitor (sintilimab) in NSCLC. J. Thor. Oncol. 15, 816–826 (2020).
doi: 10.1016/j.jtho.2020.01.017