Progress in the clinical application of immune checkpoint inhibitors in small cell lung cancer

Small cell lung cancer (SCLC) is a refractory cancer with poor prognosis due to its aggressive malignancy and high rates of metastasis, recurrence and drug resistance. These characteristics have also greatly impeded the identification of new treatment methods and drugs. The traditional model of SCLC...

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Published inFrontiers in immunology Vol. 14; p. 1126582
Main Authors He, Jiahui, Hu, Qinyong
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 29.03.2023
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Abstract Small cell lung cancer (SCLC) is a refractory cancer with poor prognosis due to its aggressive malignancy and high rates of metastasis, recurrence and drug resistance. These characteristics have also greatly impeded the identification of new treatment methods and drugs. The traditional model of SCLC treatment that has been reliant on platinum combined with etoposide for decades has been superseded by the emergence of immune checkpoint inhibitors (ICIs), which have shown significant therapeutic effects and broad application prospects as a monotherapy. This has led to the evaluation of ICIs with different mechanisms of action and their use in combination with radiotherapy or a variety of molecular targeted drugs to achieve synergy, complementary advantages, and reduce adverse reactions. Here, we review the progress in the use of ICIs as a monotherapy or in combination therapy for SCLC and consider the current limitations of these approaches as well as prospects for future developments.
AbstractList Small cell lung cancer (SCLC) is a refractory cancer with poor prognosis due to its aggressive malignancy and high rates of metastasis, recurrence and drug resistance. These characteristics have also greatly impeded the identification of new treatment methods and drugs. The traditional model of SCLC treatment that has been reliant on platinum combined with etoposide for decades has been superseded by the emergence of immune checkpoint inhibitors (ICIs), which have shown significant therapeutic effects and broad application prospects as a monotherapy. This has led to the evaluation of ICIs with different mechanisms of action and their use in combination with radiotherapy or a variety of molecular targeted drugs to achieve synergy, complementary advantages, and reduce adverse reactions. Here, we review the progress in the use of ICIs as a monotherapy or in combination therapy for SCLC and consider the current limitations of these approaches as well as prospects for future developments.
Author Hu, Qinyong
He, Jiahui
AuthorAffiliation Department of Oncology, Renmin Hospital of Wuhan University , Wuhan, Hubei , China
AuthorAffiliation_xml – name: Department of Oncology, Renmin Hospital of Wuhan University , Wuhan, Hubei , China
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  givenname: Jiahui
  surname: He
  fullname: He, Jiahui
  organization: Department of Oncology, Renmin Hospital of Wuhan University, Wuhan, Hubei, China
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  givenname: Qinyong
  surname: Hu
  fullname: Hu, Qinyong
  organization: Department of Oncology, Renmin Hospital of Wuhan University, Wuhan, Hubei, China
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Cites_doi 10.1056/NEJMoa1809064
10.1038/nature14664
10.1016/j.soncn.2019.08.013
10.3390/ijms18102134
10.1158/2326-6066.CIR-19-0744
10.1001/jama.2017.14155
10.1007/s12325-020-01538-0
10.1200/JCO.20.02212
10.21037/tlcr-21-52
10.1016/S1470-2045(22)00224-8
10.1002/ijc.33453
10.1634/theoncologist.2015-0498
10.6004/jnccn.2018.0079
10.1172/JCI67313
10.1158/2326-6066.CIR-14-0191
10.1158/1078-0432.CCR-08-2424
10.1073/pnas.0915174107
10.1016/j.ccell.2018.04.001
10.1093/annonc/mdz278
10.1016/S0140-6736(11)60165-7
10.1016/S1470-2045(20)30539-8
10.1200/JCO.2016.67.6601
10.1016/j.jtho.2018.10.003
10.1093/jjco/hyy068
10.1016/S1470-2045(16)30098-5
10.1038/nrd3877
10.1016/S0140-6736(14)61085-0
10.1177/17588359211018018
10.1093/annonc/mds213
10.1200/JCO.2022.40.17_suppl.LBA8507
10.1007/s00262-011-0975-9
10.1200/JCO.20.00793
10.1016/j.jtho.2016.05.028
10.1200/JCO.2018.36.15_suppl.8506
10.1158/2159-8290.CD-18-0367
10.1016/S0140-6736(19)32222-6
10.1016/j.jtho.2019.10.001
10.21037/tlcr.2017.03.04
10.4161/onci.28499
10.1200/JCO.20.01055
10.1016/j.annonc.2021.01.071
10.1136/jitc-2020-001302
10.1093/annonc/mdz264
10.1200/JCO.2017.72.5069
10.1158/1078-0432.CCR-05-0627
10.1016/j.annonc.2019.10.021
10.1016/j.jtho.2019.12.109
10.14423/SMJ.0000000000001166
10.1038/nm730
10.18632/oncotarget.14759
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Keywords clinical trials
immune checkpoint inhibitors
small cell lung cancer
PD1,PD-L1
combined immunotherapy
CTLA- 4
Language English
License Copyright © 2023 He and Hu.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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Reviewed by: Valerio Gristina, University of Palermo, Italy; Agnieszka Graczyk-Jarzynka, Polish Academy of Sciences, Poland
Edited by: Malgorzata Firczuk, Medical University of Warsaw, Poland
This article was submitted to Cancer Immunity and Immunotherapy, a section of the journal Frontiers in Immunology
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References B22
B24
B25
B26
Gristina (B55) 2021; 13
B27
Goldman (B56) 2021; 22
Reck (B7) 2013; 24
Arriola (B34) 2016; 11
Chung (B38) 2020; 15
Topalian (B32) 2017; 318
Ready (B49) 2019; 14
van Meerbeeck (B1) 2011; 378
Hart (B31) 2021; 38
Owonikoko (B17) 2021; 39
Ott (B9) 2017; 35
Weiss (B30) 2019; 30
George (B2) 2015; 524
Stewart (B52) 2015; 3
Antonia (B15) 2016; 17
Chen D (B42) 2017; 8
Rudin (B20) 2022; 40
Spigel (B16) 2021; 32
Patel (B46) 2017; 6
Dong (B35) 2002; 8
Saito (B57) 2018; 48
Liu (B18) 2020; 39
Passiglia (B54) 2021; 10
Yao (B4) 2013; 12
Paz-Ares (B21) 2019; 394
Blanquicett (B43) 2005; 11
Curran (B53) 2010; 107
Bukamur (B6) 2020; 113
Wang (B28) 2022; 23
Reck (B8) 2016; 34
Deng (B44) 2014; 124
Kalemkerian (B48) 2018; 16
Kareva (B40) 2017; 18
B12
Hellmann (B5) 2018; 33
Chung (B10) 2018; 36
B14
Rudin (B11) 2020; 38
Reck (B58) 2019; 30
B59
Kim (B36) 2011; 60
Kottschade (B3) 2019; 35
Chen (B41) 2020; 8
Welsh (B13) 2020; 15
Sul (B37) 2016; 21
Daniel (B29) 2020; 148
Deng (B45) 2014; 3
(B39) 2019
Horn (B19) 2018; 379
Wei (B50) 2018; 8
Slotman (B47) 2015; 385
Klein (B33) 2009; 15
Mansfield (B51) 2020; 31
Pakkala (B23) 2020; 8
References_xml – ident: B12
– volume: 379
  year: 2018
  ident: B19
  article-title: First-line atezolizumab plus chemotherapy in extensive-stage small-cell lung cancer
  publication-title: N Engl J Med
  doi: 10.1056/NEJMoa1809064
  contributor:
    fullname: Horn
– volume: 524
  start-page: 47
  year: 2015
  ident: B2
  article-title: Comprehensive genomic profiles of small cell lung cancer
  publication-title: Nature
  doi: 10.1038/nature14664
  contributor:
    fullname: George
– volume: 35
  start-page: 150934
  year: 2019
  ident: B3
  article-title: The future of immunotherapy in the treatment of cancer
  publication-title: Semin Oncol Nurs
  doi: 10.1016/j.soncn.2019.08.013
  contributor:
    fullname: Kottschade
– volume: 18
  start-page: 2134
  year: 2017
  ident: B40
  article-title: A combination of immune checkpoint inhibition with metronomic chemotherapy as a way of targeting therapy-resistant cancer cells, international journal of molecular sciences 18(10)
  publication-title: Int J Mol Sci
  doi: 10.3390/ijms18102134
  contributor:
    fullname: Kareva
– volume: 8
  year: 2020
  ident: B41
  article-title: SHP-2 and PD-L1 inhibition combined with radiotherapy enhances systemic antitumor effects in an anti-PD-1-Resistant model of non-small cell lung cancer
  publication-title: Cancer Immunol Res
  doi: 10.1158/2326-6066.CIR-19-0744
  contributor:
    fullname: Chen
– volume: 318
  year: 2017
  ident: B32
  article-title: Targeting immune checkpoints in cancer therapy
  publication-title: JAMA
  doi: 10.1001/jama.2017.14155
  contributor:
    fullname: Topalian
– volume-title: KEYTRUDA® (pembrolizumab) full prescribing information
  year: 2019
  ident: B39
– volume: 38
  year: 2021
  ident: B31
  article-title: Myelopreservation with trilaciclib in patients receiving topotecan for small cell lung cancer: Results from a randomized, double-blind, placebo-controlled phase II study
  publication-title: Adv Ther
  doi: 10.1007/s12325-020-01538-0
  contributor:
    fullname: Hart
– volume: 39
  year: 2021
  ident: B17
  article-title: Nivolumab and ipilimumab as maintenance therapy in extensive-disease small-cell lung cancer: CheckMate
  publication-title: J Clin Oncol
  doi: 10.1200/JCO.20.02212
  contributor:
    fullname: Owonikoko
– volume: 10
  year: 2021
  ident: B54
  article-title: Is there any place for PD-1/CTLA-4 inhibitors combination in the first-line treatment of advanced NSCLC?–a trial-level meta-analysis in PD-L1 selected subgroups
  publication-title: Trans Lung Cancer Res
  doi: 10.21037/tlcr-21-52
  contributor:
    fullname: Passiglia
– ident: B25
– volume: 23
  year: 2022
  ident: B28
  article-title: Adebrelimab or placebo plus carboplatin and etoposide as first-line treatment for extensive-stage small-cell lung cancer (CAPSTONE-1): a multicentre, randomised, double-blind, placebo-controlled, phase 3 trial
  publication-title: Lancet Oncol
  doi: 10.1016/S1470-2045(22)00224-8
  contributor:
    fullname: Wang
– volume: 148
  year: 2020
  ident: B29
  article-title: Trilaciclib prior to chemotherapy and atezolizumab in patients with newly diagnosed extensive-stage small cell lung cancer: A multicentre, randomised, double-blind, placebo-controlled phase II trial
  publication-title: Int J Cancer
  doi: 10.1002/ijc.33453
  contributor:
    fullname: Daniel
– volume: 21
  year: 2016
  ident: B37
  article-title: FDA Approval summary: Pembrolizumab for the treatment of patients with metastatic non-small cell lung cancer whose tumors express programmed death-ligand 1
  publication-title: Oncologist
  doi: 10.1634/theoncologist.2015-0498
  contributor:
    fullname: Sul
– volume: 16
  year: 2018
  ident: B48
  article-title: NCCN guidelines insights: Small cell lung cancer, version 2.2018
  publication-title: J Natl Compr Canc Netw
  doi: 10.6004/jnccn.2018.0079
  contributor:
    fullname: Kalemkerian
– volume: 124
  year: 2014
  ident: B44
  article-title: Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice
  publication-title: J Clin Invest
  doi: 10.1172/JCI67313
  contributor:
    fullname: Deng
– ident: B59
– volume: 3
  year: 2015
  ident: B52
  article-title: Identification and characterization of MEDI4736, an antagonistic anti-PD-L1 monoclonal antibody
  publication-title: Cancer Immunol Res
  doi: 10.1158/2326-6066.CIR-14-0191
  contributor:
    fullname: Stewart
– volume: 15
  year: 2009
  ident: B33
  article-title: Melan-a-specific cytotoxic T cells are associated with tumor regression and autoimmunity following treatment with anti-CTLA-4
  publication-title: Clin Cancer Res
  doi: 10.1158/1078-0432.CCR-08-2424
  contributor:
    fullname: Klein
– ident: B24
– volume: 107
  year: 2010
  ident: B53
  article-title: PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors
  publication-title: Proc Natl Acad Sci U.S.A.
  doi: 10.1073/pnas.0915174107
  contributor:
    fullname: Curran
– volume: 33
  start-page: 853
  year: 2018
  ident: B5
  article-title: Tumor mutational burden and efficacy of nivolumab monotherapy and in combination with ipilimumab in small-cell lung cancer
  publication-title: Cancer Cell
  doi: 10.1016/j.ccell.2018.04.001
  contributor:
    fullname: Hellmann
– volume: 30
  year: 2019
  ident: B30
  article-title: Myelopreservation with the CDK4/6 inhibitor trilaciclib in patients with small-cell lung cancer receiving first-line chemotherapy: a phase ib/randomized phase II trial
  publication-title: Ann Oncol
  doi: 10.1093/annonc/mdz278
  contributor:
    fullname: Weiss
– volume: 378
  year: 2011
  ident: B1
  article-title: Small-cell lung cancer
  publication-title: Lancet
  doi: 10.1016/S0140-6736(11)60165-7
  contributor:
    fullname: van Meerbeeck
– volume: 22
  start-page: 51
  year: 2021
  ident: B56
  article-title: Durvalumab, with or without tremelimumab, plus platinum–etoposide versus platinum–etoposide alone in first-line treatment of extensive-stage small-cell lung cancer (CASPIAN): updated results from a randomised, controlled, open-label, phase 3 trial
  publication-title: Lancet Oncol
  doi: 10.1016/S1470-2045(20)30539-8
  contributor:
    fullname: Goldman
– volume: 34
  year: 2016
  ident: B8
  article-title: Phase III randomized trial of ipilimumab plus etoposide and platinum versus placebo plus etoposide and platinum in extensive-stage small-cell lung cancer
  publication-title: J Clin Oncol
  doi: 10.1200/JCO.2016.67.6601
  contributor:
    fullname: Reck
– volume: 14
  year: 2019
  ident: B49
  article-title: Third-line nivolumab monotherapy in recurrent SCLC: CheckMate 032
  publication-title: J Thorac Oncol
  doi: 10.1016/j.jtho.2018.10.003
  contributor:
    fullname: Ready
– volume: 48
  year: 2018
  ident: B57
  article-title: Development of targeted therapy and immunotherapy for treatment of small cell lung cancer
  publication-title: Jpn J Clin Oncol
  doi: 10.1093/jjco/hyy068
  contributor:
    fullname: Saito
– volume: 17
  year: 2016
  ident: B15
  article-title: Nivolumab alone and nivolumab plus ipilimumab in recurrent small-cell lung cancer (CheckMate 032): a multicentre, open-label, phase 1/2 trial
  publication-title: Lancet Oncol
  doi: 10.1016/S1470-2045(16)30098-5
  contributor:
    fullname: Antonia
– volume: 12
  year: 2013
  ident: B4
  article-title: Advances in targeting cell surface signalling molecules for immune modulation, nature reviews
  publication-title: Drug Discovery
  doi: 10.1038/nrd3877
  contributor:
    fullname: Yao
– volume: 385
  start-page: 36
  year: 2015
  ident: B47
  article-title: Use of thoracic radiotherapy for extensive stage small-cell lung cancer: a phase 3 randomised controlled trial
  publication-title: Lancet
  doi: 10.1016/S0140-6736(14)61085-0
  contributor:
    fullname: Slotman
– volume: 13
  start-page: 17588359211018018
  year: 2021
  ident: B55
  article-title: Is there any room for PD-1 inhibitors in combination with platinum-based chemotherapy as frontline treatment of extensive-stage small cell lung cancer? a systematic review and meta-analysis with indirect comparisons among subgroups and landmark survival analyses
  publication-title: Ther Adv Med Oncol
  doi: 10.1177/17588359211018018
  contributor:
    fullname: Gristina
– volume: 24
  start-page: 75
  year: 2013
  ident: B7
  article-title: Ipilimumab in combination with paclitaxel and carboplatin as first-line therapy in extensive-disease-small-cell lung cancer: results from a randomized, double-blind, multicenter phase 2 trial
  publication-title: Ann Oncol
  doi: 10.1093/annonc/mds213
  contributor:
    fullname: Reck
– ident: B14
– volume: 40
  year: 2022
  ident: B20
  article-title: SKYSCRAPER-02: primary results of a phase III, randomized, double-blind, placebo controlled study of atezolizumab (atezo) + carboplatin + etoposide (CE) with or without tiragolumab (tira) in patients (pts) with untreated extensive-stage small cell lung cancer (ES-SCLC)
  publication-title: J Clin Oncol
  doi: 10.1200/JCO.2022.40.17_suppl.LBA8507
  contributor:
    fullname: Rudin
– ident: B27
– volume: 60
  year: 2011
  ident: B36
  article-title: Impact of minimal tumor burden on antibody response to vaccination
  publication-title: Cancer Immunology Immunotherapy
  doi: 10.1007/s00262-011-0975-9
  contributor:
    fullname: Kim
– volume: 38
  year: 2020
  ident: B11
  article-title: Pembrolizumab or placebo plus etoposide and platinum as first-line therapy for extensive-stage small-cell lung cancer: Randomized, double-blind
  publication-title: Phase III KEYNOTE-604 Study
  doi: 10.1200/JCO.20.00793
  contributor:
    fullname: Rudin
– volume: 11
  year: 2016
  ident: B34
  article-title: Outcome and biomarker analysis from a multicenter phase 2 study of ipilimumab in combination with carboplatin and etoposide as first-line therapy for extensive-stage SCLC
  publication-title: J Thorac Oncol
  doi: 10.1016/j.jtho.2016.05.028
  contributor:
    fullname: Arriola
– volume: 36
  start-page: 8506
  year: 2018
  ident: B10
  article-title: Phase 2 study of pembrolizumab in advanced small-cell lung cancer (SCLC): KEYNOTE-158
  publication-title: J Clin Oncol
  doi: 10.1200/JCO.2018.36.15_suppl.8506
  contributor:
    fullname: Chung
– volume: 8
  year: 2018
  ident: B50
  article-title: Fundamental mechanisms of immune checkpoint blockade therapy
  publication-title: Cancer Discovery
  doi: 10.1158/2159-8290.CD-18-0367
  contributor:
    fullname: Wei
– volume: 394
  year: 2019
  ident: B21
  article-title: 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
  publication-title: Lancet
  doi: 10.1016/S0140-6736(19)32222-6
  contributor:
    fullname: Paz-Ares
– volume: 15
  year: 2020
  ident: B13
  article-title: Phase I trial of pembrolizumab and radiation therapy after induction chemotherapy for extensive-stage small cell lung cancer
  publication-title: J Thorac Oncol
  doi: 10.1016/j.jtho.2019.10.001
  contributor:
    fullname: Welsh
– volume: 6
  year: 2017
  ident: B46
  article-title: Combining immunotherapy and radiation therapy for small cell lung cancer and thymic tumors
  publication-title: Transl Lung Cancer Res
  doi: 10.21037/tlcr.2017.03.04
  contributor:
    fullname: Patel
– volume: 3
  year: 2014
  ident: B45
  article-title: Radiation and anti-PD-L1 antibody combinatorial therapy induces T cell-mediated depletion of myeloid-derived suppressor cells and tumor regression
  publication-title: Oncoimmunology
  doi: 10.4161/onci.28499
  contributor:
    fullname: Deng
– volume: 39
  year: 2020
  ident: B18
  article-title: Updated overall survival and PD-L1 subgroup analysis of patients with extensive-stage small-cell lung cancer treated with atezolizumab, carboplatin, and etoposide (IMpower133)
  publication-title: J Clin Oncol
  doi: 10.1200/JCO.20.01055
  contributor:
    fullname: Liu
– volume: 32
  year: 2021
  ident: B16
  article-title: Second-line nivolumab in relapsed small-cell lung cancer: CheckMate 331()
  publication-title: Ann Oncol
  doi: 10.1016/j.annonc.2021.01.071
  contributor:
    fullname: Spigel
– volume: 8
  year: 2020
  ident: B23
  article-title: Durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer: a randomized phase II study
  publication-title: J Immunother Cancer
  doi: 10.1136/jitc-2020-001302
  contributor:
    fullname: Pakkala
– volume: 30
  year: 2019
  ident: B58
  article-title: IMpower133: Updated overall survival (OS) analysis of first-line (1L) atezolizumab (atezo) + carboplatin + etoposide in extensive-stage SCLC (ES-SCLC)
  publication-title: Ann Oncol
  doi: 10.1093/annonc/mdz264
  contributor:
    fullname: Reck
– volume: 35
  year: 2017
  ident: B9
  article-title: Pembrolizumab in patients with extensive-stage small-cell lung cancer: Results from the phase ib KEYNOTE-028 study
  publication-title: J Clin Oncol
  doi: 10.1200/JCO.2017.72.5069
  contributor:
    fullname: Ott
– ident: B26
– volume: 11
  year: 2005
  ident: B43
  article-title: Antitumor efficacy of capecitabine and celecoxib in irradiated and lead-shielded, contralateral human BxPC-3 pancreatic cancer xenografts: clinical implications of abscopal effects
  publication-title: Clin Cancer Res
  doi: 10.1158/1078-0432.CCR-05-0627
  contributor:
    fullname: Blanquicett
– ident: B22
– volume: 31
  year: 2020
  ident: B51
  article-title: Safety and patient-reported outcomes of atezolizumab, carboplatin, and etoposide in extensive-stage small-cell lung cancer (IMpower133): a randomized phase I/III trial
  publication-title: Ann Oncol
  doi: 10.1016/j.annonc.2019.10.021
  contributor:
    fullname: Mansfield
– volume: 15
  year: 2020
  ident: B38
  article-title: Pembrolizumab after two or more lines of previous therapy in patients with recurrent or metastatic SCLC: Results from the KEYNOTE-028 and KEYNOTE-158 studies
  publication-title: J Thorac Oncol
  doi: 10.1016/j.jtho.2019.12.109
  contributor:
    fullname: Chung
– volume: 113
  year: 2020
  ident: B6
  article-title: Immune checkpoint inhibitor-related pulmonary toxicity: Focus on nivolumab
  publication-title: South Med J
  doi: 10.14423/SMJ.0000000000001166
  contributor:
    fullname: Bukamur
– volume: 8
  start-page: 793
  year: 2002
  ident: B35
  article-title: Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion
  publication-title: Nat Med
  doi: 10.1038/nm730
  contributor:
    fullname: Dong
– volume: 8
  year: 2017
  ident: B42
  article-title: Consolidative thoracic radiotherapy for extensive stage small cell lung cancer
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.14759
  contributor:
    fullname: Chen D
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Snippet Small cell lung cancer (SCLC) is a refractory cancer with poor prognosis due to its aggressive malignancy and high rates of metastasis, recurrence and drug...
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SubjectTerms clinical trials
combined immunotherapy
Combined Modality Therapy
CTLA- 4
Humans
immune checkpoint inhibitors
Immune Checkpoint Inhibitors - therapeutic use
Immunology
Immunotherapy - methods
Lung Neoplasms
PD1,PD-L1
small cell lung cancer
Small Cell Lung Carcinoma
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Title Progress in the clinical application of immune checkpoint inhibitors in small cell lung cancer
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