Depth of response and treatment outcomes of immune checkpoint inhibitor-based therapy in patients with advanced non-small cell lung cancer and high PD-L1 expression: An exploratory analysis of retrospective multicenter cohort.

Chemoimmunotherapy Depth of response Immune checkpoint inhibitor Non-small cell lung cancer Tumor shrinkage

Journal

Investigational new drugs
ISSN: 1573-0646
Titre abrégé: Invest New Drugs
Pays: United States
ID NLM: 8309330

Informations de publication

Date de publication:
21 Aug 2024
Historique:
received: 27 06 2024
accepted: 12 08 2024
medline: 22 8 2024
pubmed: 22 8 2024
entrez: 21 8 2024
Statut: aheadofprint

Résumé

The association between depth of response (DpR) and treatment outcomes has been documented across various types of cancer. Immune checkpoint inhibitor (ICI)-based treatment is globally used as first-line treatment for non-small cell lung cancer (NSCLC) with programmed death-ligand 1 (PD-L1) expression ≥ 50%. However, in this population, the significance of DpR is not elucidated. Patients with advanced NSCLC and PD-L1 expression ≥ 50% who received ICI-monotherapy or ICI plus chemotherapy were retrospectively enrolled into this study. Treatment responses were grouped into DpR 'quartiles' by percentage of maximal tumor reduction (Q1 = 1-25%, Q2 = 26-50%, Q3 = 51-75%, and Q4 =  ≥ 76%), and no tumor reduction (NTR). The association between DpR and survival rates were determined using hazard ratios (HR) generated by the Cox proportional hazards model. The Kaplan-Meier method was used to determine survival outcomes. A total of 349 patients were included, of which 214 and 135 patients received pembrolizumab monotherapy and ICI plus chemotherapy, respectively, as first-line treatments. The majority of the patients were male. All DpR quartiles, especially Q4, showed an association with progression-free survival (PFS)/overall survival (OS). In the Q4 cohort, patients who received pembrolizumab had a longer PFS than those who received ICI plus chemotherapy. High DpR was associated with longer PFS and OS, with a more pronounced effect observed with pembrolizumab monotherapy than with ICI plus chemotherapy.

Identifiants

pubmed: 39168900
doi: 10.1007/s10637-024-01467-7
pii: 10.1007/s10637-024-01467-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Kawachi H, Fujimoto D, Morimoto T et al (2019) Early depth of tumor shrinkage and treatment outcomes in non-small cell lung cancer treated using Nivolumab. Invest New Drugs 37:1257–1265. https://doi.org/10.1007/s10637-019-00770-y
doi: 10.1007/s10637-019-00770-y pubmed: 30937690
Ishida M, Morimoto K, Yamada T et al (2023) Early tumor shrinkage as a predictor of favorable treatment outcomes in patients with extensive-stage SCLC who received programmed cell death-ligand 1 inhibitor plus platinum-etoposide chemotherapy: a prospective observational study. JTO Clin Res Rep 4:100493. https://doi.org/10.1016/j.jtocrr.2023.100493
doi: 10.1016/j.jtocrr.2023.100493 pubmed: 37025120 pmcid: 10070895
McCoach CE, Blumenthal GM, Zhang L et al (2017) Exploratory analysis of the association of depth of response and survival in patients with metastatic non-small-cell lung cancer treated with a targeted therapy or immunotherapy. Ann Oncol 28:2707–2714. https://doi.org/10.1093/annonc/mdx414
doi: 10.1093/annonc/mdx414 pubmed: 29045514 pmcid: 6137816
Jo H, Yoshida T, Yagishita S et al (2023) Clinical characteristics and pharmacokinetics change of long-term responders to antiprogrammed cell death Protein 1 inhibitor among patients with advanced NSCLC. JTO Clin Res Rep 4:100474. https://doi.org/10.1016/j.jtocrr.2023.100474
doi: 10.1016/j.jtocrr.2023.100474 pubmed: 37007867 pmcid: 10050777
Xie X, Li X, Yao W (2021) A narrative review: depth of response as a predictor of the long-term outcomes for solid tumors. Transl Cancer Res 10:1119–1130. https://doi.org/10.21037/tcr-20-2547
Saijo K, Imai H, Ouchi K et al (2023) Depth of response may predict clinical outcome in patients with recurrent/metastatic head and neck cancer treated with pembrolizumab-containing regimens. Front Oncol 13:1230731. https://doi.org/10.3389/fonc.2023.1230731
doi: 10.3389/fonc.2023.1230731 pubmed: 37664016 pmcid: 10469278
Garon EB, Rizvi NA, Hui R et al (2015) Pembrolizumab for the treatment of non–small-cell lung cancer. N Engl J Med 372:2018–2028. https://doi.org/10.1056/NEJMoa1501824
doi: 10.1056/NEJMoa1501824 pubmed: 25891174
Borghaei H, Paz-Ares L, Horn L et al (2015) Nivolumab versus docetaxel in Advanced nonsquamous Non–Small-Cell Lung Cancer. N Engl J Med 373:1627–1639. https://doi.org/10.1056/NEJMoa1507643
doi: 10.1056/NEJMoa1507643 pubmed: 26412456 pmcid: 5705936
Brahmer J, Reckamp KL, Baas P et al (2015) Nivolumab versus docetaxel in advanced squamous-cell non–small-cell lung Cancer. N Engl J Med 373:123–135. https://doi.org/10.1056/NEJMoa1504627
doi: 10.1056/NEJMoa1504627 pubmed: 26028407 pmcid: 4681400
Rittmeyer A, Barlesi F, Waterkamp D et al (2017) Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet 389:255–265. https://doi.org/10.1016/S0140-6736(16)32517-X.Publishedonlinefirst:2016/12/17
doi: 10.1016/S0140-6736(16)32517-X.Publishedonlinefirst:2016/12/17 pubmed: 27979383
Herbst RS, Baas P, Kim DW et al (2016) Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet 387:1540–1550. https://doi.org/10.1016/S0140-6736(15)01281-7 . Published online first: 2015/12/30
Reck M, Rodríguez-Abreu D, Robinson AG et al (2016) Pembrolizumab versus chemotherapy for PD-L1–positive non–small-cell lung ancer. N Engl J Med 375:1823–1833. https://doi.org/10.1056/NEJMoa1606774
doi: 10.1056/NEJMoa1606774 pubmed: 27718847
Herbst RS, Giaccone G, de Marinis F et al (2020) Atezolizumab for first-line treatment of PD-L1-selected patients with NSCLC. N Engl J Med 383:1328–1339. https://doi.org/10.1056/NEJMoa1917346 . (Published online first: 2020/10/01)
doi: 10.1056/NEJMoa1917346 pubmed: 32997907
Mok TSK, Wu YL, Kudaba I et al (2019) 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 393:1819–1830. https://doi.org/10.1016/S0140-6736(18)32409-7
doi: 10.1016/S0140-6736(18)32409-7 pubmed: 30955977
Reck M, Rodríguez-Abreu D, Robinson AG et al (2021) 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. https://doi.org/10.1200/JCO.21.00174
doi: 10.1200/JCO.21.00174 pubmed: 33872070 pmcid: 8280089
Rodríguez-Abreu D, Powell SF, Hochmair MJ et al (2021) Pemetrexed plus platinum with or without pembrolizumab in patients with previously untreated metastatic nonsquamous NSCLC: protocol-specified final analysis from KEYNOTE-189. Ann Oncol 32:881–895. https://doi.org/10.1016/j.annonc.2021.04.008
doi: 10.1016/j.annonc.2021.04.008 pubmed: 33894335
Pons-Tostivint E, Hulo P, Guardiolle V et al (2023) Real-world multicentre cohort of first-line pembrolizumab alone or in combination with platinum-based chemotherapy in non-small cell lung cancer PD-L1 ≥ 50. Cancer Immunol Immunother 72:1881–1890. https://doi.org/10.1007/s00262-022-03359-2
doi: 10.1007/s00262-022-03359-2 pubmed: 36690799 pmcid: 10198917
Pérol M, Felip E, Dafni U et al (2022) Effectiveness of PD-(L)1 inhibitors alone or in combination with platinum-doublet chemotherapy in first-line (1L) non-squamous non-small-cell lung cancer (Nsq-NSCLC) with PD-L1-high expression using real-world data. Ann Oncol 33:511–521. https://doi.org/10.1016/j.annonc.2022.02.008
doi: 10.1016/j.annonc.2022.02.008 pubmed: 35218887
Eisenhauer EA, Therasse P, Bogaerts J et al (2009) New response evaluation criteria in solid tumours: revised RECIST guideline, version 1.1. Eur J Cancer, version 1.1 45:228–247. https://doi.org/10.1016/j.ejca.2008.10.026
Aguilar EJ, Ricciuti B, Gainor JF et al (2019) Outcomes to first-line pembrolizumab in patients with non-small-cell lung cancer and very high PD-L1 expression. Ann Oncol 30:1653–1659. https://doi.org/10.1093/annonc/mdz288
doi: 10.1093/annonc/mdz288 pubmed: 31435660
Kanda Y (2013) Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 48:452–458. https://doi.org/10.1038/bmt.2012.244
doi: 10.1038/bmt.2012.244 pubmed: 23208313
Bracci L, Schiavoni G, Sistigu A, Belardelli F (2014) Immune-based mechanisms of cytotoxic chemotherapy: implications for the design of novel and rationale-based combined treatments against cancer. Cell Death Differ 21:15–25. https://doi.org/10.1038/cdd.2013.67
doi: 10.1038/cdd.2013.67 pubmed: 23787994
Morimoto K, Uchino J, Yokoi T et al (2022) Early discontinuation of induction therapy in chemoimmunotherapy as an effective alternative to the standard regimen in patients with non-small cell lung cancer: a retrospective study. J Cancer Res Clin Oncol 148:2437–2446. https://doi.org/10.1007/s00432-021-03782-5
doi: 10.1007/s00432-021-03782-5 pubmed: 34510271
Wu T, Dai Y (2017) Tumor microenvironment and therapeutic response. Cancer Lett 387:61–68. https://doi.org/10.1016/j.canlet.2016.01.043
doi: 10.1016/j.canlet.2016.01.043 pubmed: 26845449
Li JY, Chen YP, Li YQ, Liu N, Ma J (2021) Chemotherapeutic and targeted agents can modulate the tumor microenvironment and increase the efficacy of immune checkpoint blockades. Mol Cancer 20:27. https://doi.org/10.1186/s12943-021-01317-7
doi: 10.1186/s12943-021-01317-7 pubmed: 33541368 pmcid: 7863268
DeNardo DG, Brennan DJ, Rexhepaj E et al (2011) Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 1:54–67. https://doi.org/10.1158/2159-8274.CD-10-0028
doi: 10.1158/2159-8274.CD-10-0028 pubmed: 22039576 pmcid: 3203524
Nakasone ES, Askautrud HA, Kees T et al (2012) Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 21:488–503. https://doi.org/10.1016/j.ccr.2012.02.017
doi: 10.1016/j.ccr.2012.02.017 pubmed: 22516258 pmcid: 3332002
Suzuki S, Haratani K, Hayashi H et al (2022) Association of tumour burden with the efficacy of programmed cell death-1/programmed cell death ligand-1 inhibitors for treatment-naïve advanced non-small-cell lung cancer. Eur J Cancer 161:44–54. https://doi.org/10.1016/j.ejca.2021.11.011
doi: 10.1016/j.ejca.2021.11.011 pubmed: 34922263
Miyawaki T, Naito T, Doshita K et al (2022) Predicting the efficacy of first-line immunotherapy by combining cancer cachexia and tumor burden in advanced non-small cell lung cancer. Thorac Cancer 13:2064–2074. https://doi.org/10.1111/1759-7714.14529
doi: 10.1111/1759-7714.14529 pubmed: 35698259 pmcid: 9284192

Auteurs

Yusuke Tachibana (Y)

Department of Pulmonary Medicine, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Kyoto, Japan.

Kenji Morimoto (K)

Department of Pulmonary Medicine, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Kyoto, Japan.

Tadaaki Yamada (T)

Department of Pulmonary Medicine, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Kyoto, Japan. tayamada@koto.kpu-m.ac.jp.

Hayato Kawachi (H)

Department of Pulmonary Medicine, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Kyoto, Japan.

Motohiro Tamiya (M)

Department of Thoracic Oncology, Osaka International Cancer Institute, Osaka, Osaka, Japan.

Yoshiki Negi (Y)

Department of Respiratory Medicine and Hematology, School of Medicine, Hyogo Medical University, Nishinomiya, Hyogo, Japan.

Yasuhiro Goto (Y)

Department of Respiratory Medicine, Fujita Health University School of Medicine, Toyoake, Aichi, Japan.

Akira Nakao (A)

Department of Respiratory Medicine, Fukuoka University Hospital, Fukuoka, Fukuoka, Japan.

Shinsuke Shiotsu (S)

Department of Respiratory Medicine, Japanese Red Cross Kyoto Daiichi Hospital, Kyoto, Kyoto, Japan.

Keiko Tanimura (K)

Department of Respiratory Medicine, Japanese Red Cross Kyoto Daini Hospital, Kyoto, Kyoto, Japan.

Takayuki Takeda (T)

Department of Respiratory Medicine, Japanese Red Cross Kyoto Daini Hospital, Kyoto, Kyoto, Japan.

Asuka Okada (A)

Department of Respiratory Medicine, Saiseikai Suita Hospital, Suita, Osaka, Japan.

Taishi Harada (T)

Department of Medical Oncology, Fukuchiyama City Hospital, Fukuchiyama, Kyoto, Japan.

Koji Date (K)

Department of Pulmonary Medicine, Kyoto Chubu Medical Center, Nantan, Kyoto, Japan.

Yusuke Chihara (Y)

Department of Respiratory Medicine, Uji-Tokushukai Medical Center, Uji, Kyoto, Japan.

Isao Hasegawa (I)

Department of Respiratory Medicine, Saiseikai Shigaken Hospital, Ritto, Shiga, Japan.

Nobuyo Tamiya (N)

Department of Respiratory Medicine, Rakuwakai Otowa Hospital, Kyoto, Kyoto, Japan.

Yuki Katayama (Y)

Department of Pulmonary Medicine, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Kyoto, Japan.

Naoya Nishioka (N)

Department of Pulmonary Medicine, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Kyoto, Japan.

Masahiro Iwasaku (M)

Department of Pulmonary Medicine, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Kyoto, Japan.

Shinsaku Tokuda (S)

Department of Pulmonary Medicine, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Kyoto, Japan.

Takashi Kijima (T)

Department of Respiratory Medicine and Hematology, School of Medicine, Hyogo Medical University, Nishinomiya, Hyogo, Japan.

Koichi Takayama (K)

Department of Pulmonary Medicine, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Kyoto, Japan.

Classifications MeSH