Immunotherapy-chemotherapy combinations for non-small cell lung cancer: current trends and future perspectives

References

• Buchbinder EI, Desai A. CTLA-4 and PD-1 pathways: similarities, differences, and implications of their inhibition. Am J Clin Oncol. 2016;39(1):98–106. Papers of special note have been highlighted as either of interest (•) or of considerable interest (••) to readers
   PubMed Web of Science ®Google Scholar
• Li X, Yan S, Yang J, et al. Efficacy and safety of PD-1/PD-L1 inhibitors plus chemotherapy versus PD-1/PD-L1 inhibitors in advanced non-small cell lung cancer: a network analysis of randomized controlled trials. Front Oncol. 2021;10:574752.
   PubMed Web of Science ®Google Scholar
• Bailly C, Thuru X, Quesnel B, et al. Combined cytotoxic chemotherapy and immunotherapy of cancer: modern times. NAR Cancer. 2020;2(1):002.
   Google Scholar
• Tuminello S, Sikavi D, Veluswamy R, et al. PD-L1 as a prognostic biomarker in surgically resectable non-small cell lung cancer: a meta-analysis. Transl Lung Cancer Res. 2020;4(4):1343–1360.
   Google Scholar
• Qin S, Linping X, Ming Y, et al. Novel immune checkpoint targets: moving beyond PD-1 and CTLA-4. Mol Cancer. 2019;18(1):155.
   PubMed Web of Science ®Google Scholar
• Puri S, Shafique M. Combination checkpoint inhibitors for treatment of non-small-cell lung cancer: an update on dual antiCTLA-4 and anti-PD-1/PD-L1 therapies. Drugs Context. 2020;9:2019.
   PubMedGoogle Scholar
• Funaki S, Shintani Y, Kawamura T, et al. Chemotherapy enhances programmed cell death 1/ligand 1 expression via TGF-β induced epithelial mesenchymal transition in non-small cell lung cancer. Oncol Rep. 2017;38(4):2277–2284.
   PubMed Web of Science ®Google Scholar
• Cavazzoni A, Digiacomo G, Alfieri R, et al. Pemetrexed enhances membrane PD-L1 expression and potentiates T cell-mediated cytotoxicity by anti-PD-L1 antibody therapy in non-small-cell lung cancer. Cancers (Basel). 2020;12(3):666.
   PubMed Web of Science ®Google Scholar
• Genova C, Dellepiane C, Carrega P, et al. Therapeutic implications of tumor microenvironment in lung cancer: focus on immune checkpoint blockade. Front Immunol. 2022;12:799455.
   PubMed Web of Science ®Google Scholar
• Veglia F, Sanseviero E, Gabrilovich DI, et al. Myeloid-derived suppressor cells in the era of increasing myeloid cell diversity. Nat Rev Immunol. 2021;8(8):485–498.
   Google Scholar
• Lee CR, Lee W, Cho SK, et al. Characterization of multiple cytokine combinations and TGF-β on differentiation and functions of myeloid-derived suppressor cells. Int J Mol Sci. 2018;19(3):869.
   PubMed Web of Science ®Google Scholar
• Su YL, Banerjee S, White SV, et al. STAT3 in Tumor-associated myeloid cells: multitasking to disrupt immunity. Int J Mol Sci. 2018;19(6):1803.
   PubMed Web of Science ®Google Scholar
• Yang Z, Guo J, Weng L, et al. Myeloid-derived suppressor cells-new and exciting players in lung cancer. J Hematol Oncol. 2020;13(1):10.
   PubMed Web of Science ®Google Scholar
• Marvel D, Gabrilovich DI. Myeloid-derived suppressor cells in the tumor microenvironment: expect the unexpected. J Clin Invest. 2015;125(9):3356–3364.
   PubMed Web of Science ®Google Scholar
• Pircher A, Gamerith G, Amann A, et al. Neoadjuvant chemo-immunotherapy modifies CD4(+)CD25(+) regulatory T cells (Treg) in non-small cell lung cancer (NSCLC) patients. Lung Cancer. 2014;85(1):81–87.
   PubMed Web of Science ®Google Scholar
• Larionova I, Cherdyntseva N, Liu T, et al. Interaction of tumor-associated macrophages and cancer chemotherapy. Oncoimmunology. 2019;8(7):1596004.
   PubMed Web of Science ®Google Scholar
• Fumet JD, Limagne E, Thibaudin M, et al. Immunogenic cell death and elimination of immunosuppressive cells: a double-edged sword of chemotherapy. Cancers (Basel). 2020 Sep 16;12(9):2637.
   PubMed Web of Science ®Google Scholar
• Kroemer G, Galluzzi Lkepp O, Kepp O, et al. Immunogenic cell death in cancer therapy. Annu Rev Immunol. 2013;31(1):51–72.
   PubMed Web of Science ®Google Scholar
• Simons M, Gordon E, Claesson-Welsh L, et al. Mechanisms and regulation of endothelial VEGF receptor signalling. Nat Rev Mol Cell Biol. 2016;17(10):611–625.
   PubMed Web of Science ®Google Scholar
• Tao L, Huang G, Shi S, et al. Bevacizumab improves the antitumor efficacy of adoptive cytokine-induced killer cells therapy in non-small cell lung cancer models. Med Oncol. 2014;31(1):777.
   PubMed Web of Science ®Google Scholar
• Heist RS, Duda DG, Sahani DV, et al. Improved tumor vascularization after anti-VEGF therapy with carboplatin and nab-paclitaxel associates with survival in lung cancer. Proc National Acad Sci USA 2015;112:1547–1552.
   PubMed Web of Science ®Google Scholar
• Fukumura D, Kloepper J, Amoozgar Z, et al. Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges. Nat Rev Clin Oncol. 2018;15(5):325–340.
   PubMed Web of Science ®Google Scholar
• Khan KA, Kerbel RS. Improving immunotherapy outcomes with antiangiogenic treatments and vice versa. Nat Rev Clin Oncol. 2018;15(5):310–324.
   PubMed Web of Science ®Google Scholar
• Horn L, Spigel DR, Vokes EE, et al. Nivolumab Versus Docetaxel in Previously Treated Patients With Advanced Non-Small-Cell Lung Cancer: Two-Year Outcomes From Two Randomized, Open-Label, Phase III Trials (CheckMate 017 and CheckMate 057). J Clin Oncol. 2017;35(35):3924–3923.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Baas P, Kim DW, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet. 2016;387(10027):1540–1550.
   PubMed Web of Science ®Google Scholar
• Reck M, Rodríguez-Abreu D, Robinson AG, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell Lung cancer. N Engl J Med. 2016;375(19):1823–1833.
   PubMed Web of Science ®Google Scholar
• Langer CJ, Gadgeel SM, Borghaei H, et al. Carboplatin and pemetrexed with or without pembrolizumab for advanced, non-squamous non-small-cell lung cancer: a randomised, phase 2 cohort of the open-label KEYNOTE-021 study. Lancet Oncol. 2016;11(11):1497–1508.
   Google Scholar
• Gandhi L, Rodríguez-Abreu D, Gadgeel S, et al., Pembrolizumab plus chemotherapy in metastatic non-small-cell lung cancer. N Engl J Med. 2018;378(22):2078–2092.
   PubMed Web of Science ®Google Scholar
• Gadgeel S, Rodríguez-Abreu D, Speranza G, et al. Pembrolizumab or placebo plus pemetrexed and platinum for previously untreated metastatic nonsquamous non-small-cell lung cancer. J Clin Oncol. 2020;38(14):1505–1517.
   PubMed Web of Science ®Google Scholar
• Paz-Ares L, Luft A, Vicente D, et al., Pembrolizumab plus chemotherapy for squamous non-small-cell lung cancer. N Engl J Med. 2018;379(21):2040–2051.
   PubMed Web of Science ®Google Scholar
• Borghaei H, Langer CJ, Paz-Ares L, et al. Pembrolizumab plus chemotherapy versus chemotherapy alone in patients with advanced non-small cell lung cancer without tumor PD-L1 expression: a pooled analysis of 3 randomized controlled trials. Cancer. 2020;126(22):4867–4877.
   PubMed Web of Science ®Google Scholar
• Paz-Ares L, Ciuleanu TE, Yu X, et al. LBA3 Nivolumab (NIVO) þ platinum-doublet chemotherapy (chemo) vs chemo as first-line (1L) treatment (tx) for advanced non-small cell lung cancer (aNSCLC): checkMate 227 - part 2 final analysis. Ann Oncol. 2019;30:xi67–xi68.
   Web of Science ®Google Scholar
• Paz-Ares L, Ciuleanu TE, Lee JS, et al. Nivolumab (NIVO) plus ipilimumab (IPI) versus chemotherapy (chemo) as first-line (1L) treatment for advanced non-small cell lung cancer (NSCLC): 4-year update from CheckMate 227. J Clin Oncol. 2021;39(15_suppl):9016.
   Google Scholar
• Sezer A, Kilickap S, Gumus M, 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. 2021;397(10274):592–604.
   PubMed Web of Science ®Google Scholar
• Gogishvili M, Melkadze T, Makharadze T, et al. EMPOWER-lung 3: cemiplimab in combination with platinum doublet chemotherapy (Chemo) for First-Line (1L) treatment of advanced non-small cell lung cancer (NSCLC). ESMO. 2021;32:S1283–S1346.
   Web of Science ®Google Scholar
• Zhou C, Wu L, Fan Y, et al. Sintilimab plus platinum and gemcitabine as first-line treatment for advanced or metastatic squamous NSCLC: results from a randomized, double-blind, phase 3 trial (ORIENT-12). J Thorac Oncol. 2021;16(9):1501–1511.
   PubMed Web of Science ®Google Scholar
• Yang Y, Sun J, Wang Z, et al. Updated overall survival data and predictive biomarkers of sintilimab plus pemetrexed and platinum as first-line treatment for locally advanced or metastatic nonsquamous NSCLC in the phase 3 ORIENT-11 study. J Thorac Oncol. 2021;16(12):2109–2120.
   PubMed Web of Science ®Google Scholar
• Wu J, Wuang C, Fan Y, et al. JCSE01.09 A phase ii umbrella study of camrelizumab in different PD-L1 expression cohorts in pre-treated advanced/metastatic non-small cell lung cancer. J Thorac Oncol. 2019;14(10):s128.
   Google Scholar
• Zhou C, Chen G, Huang Y, et al. Camrelizumab plus carboplatin and pemetrexed versus chemotherapy alone in chemotherapy-naive patients with advanced non-squamous non-small-cell lung cancer (CameL): a randomised, open-label, multicentre, phase 3 trial. Lancet Respir Med. 2021;9(3):305–314.
   PubMed Web of Science ®Google Scholar
• Shengxiang R, Ren S, Chen J, et al. Camrelizumab plus carboplatin and paclitaxel as first-line treatment for advanced squamous NSCLC (CameL-Sq): a phase 3 trial. J Thorac Oncol. 2021;16(4):s748–s802.
   Web of Science ®Google Scholar
• West H, McCleod M, Hussein M, et al. Atezolizumab in combination with carboplatin plus nab-paclitaxel chemotherapy compared with chemotherapy alone as first-line treatment for metastatic non-squamous non-small-cell lung cancer (IMpower130): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol. 2019;20(7):924–937.
   PubMed Web of Science ®Google Scholar
• Nishio M, Barlesi F, West H, et al. Atezolizumab plus chemotherapy for first-line treatment of nonsquamous NSCLC: results from the randomized phase 3 IMpower132 trial. J Thorac Oncol. 2021;16(4):653–664.
   PubMed Web of Science ®Google Scholar
• Jotte R, Cappuzzo F, Vynnychenko I, et al. Atezolizumab in combination with carboplatin and Nab-paclitaxel in advanced squamous NSCLC (IMpower131): results from a randomized phase III trial. J Thorac Oncol. 2020;15(8):1351–1360.
   PubMed Web of Science ®Google Scholar
• Socinski MA, Jotte RM, Cappuzzo F, et al. Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC. N Engl J Med. 2018 14;378(24):2288–2301.
   PubMed Web of Science ®Google Scholar
• Johnson ML, Cho BC, Luft A, et al. Durvalumab± tremelimumab + chemotherapy as first-line treatmente for mNSCLC results from the phase 3 POSEIDON study. World Conference on Lung Cancer (WCLC). 2021.
   Google Scholar
• Hodi FS, Chiarion-Sileni V, Gonzalez R, et al. Nivolumab plus ipilimumab or nivolumab alone versus ipilimumab alone in advanced melanoma (CheckMate 067): 4-year outcomes of a multicentre, randomised, phase 3 trial. Lancet Oncol. 2018;19(11):1480–1492.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Escudier B, McDermott DF, et al. Survival outcomes and independent response assessment with nivolumab plus ipilimumab versus sunitinib in patients with advanced renal cell carcinoma: 42-month follow-up of a randomized phase 3 clinical trial. J Immunother Cancer. 2020;8(2):e000891. Erratum in: J Immunother Cancer 2021;9(5).
   PubMed Web of Science ®Google Scholar
• Baas P, Scherpereel A, Nowak AK, et al. First-line nivolumab plus ipilimumab in unresectable malignant pleural mesothelioma (CheckMate 743): a multicentre, randomised, open-label, phase 3 trial. Lancet. 2021 30;397(10272):375–386.
   PubMed Web of Science ®Google Scholar
• Govindan R, Szczesna A, Ahn M, et al. Phase III trial of ipilimumab combined with paclitaxel and carboplatin in advanced squamous non-small-cell lung cancer. J Clin Oncol. 2017 20;35(30):3449–3457.
   PubMed Web of Science ®Google Scholar
• Lynch TJ, Bondarenko I, Luft A, et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J Clin Oncol. 2012;30(17):2046–2054.
   PubMed Web of Science ®Google Scholar
• Paz-Ares L, Ciuleanu TE, Cobo M, 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. 2021;22(2):198–211.
   PubMed Web of Science ®Google Scholar
• Reck M, Ciuleanu TE, Cobo M, et al. First-line nivolumab plus ipilimumab with two cycles of chemotherapy versus chemotherapy alone (four cycles) in advanced non-small-cell lung cancer: checkMate 9LA 2-year update. ESMO Open. 2021;6(5):100273.
   PubMed Web of Science ®Google Scholar
• Carbone DP, Ciuleanu T, Cobo M, et al. First-line nivolumab + ipilimumab + chemotherapy in patients with advanced NSCLC and brain metastases: results from CheckMate 9LA. World Conference of Lung Cancer (WCLC). 2021.
   Google Scholar
• Phase III POSEIDON trial shows positive results for patients taking chemotherapy plus durvalumab and tremelimumab | IASLC ( consulted on 15/07/2022)
   Google Scholar
• Liu L, Bai H, Wang C, et al. Efficacy and safety of first-line immunotherapy combinations for advanced NSCLC: a systematic review and network meta-analysis. J Thorac Oncol. 2021;16(7):1099–1117.
   PubMed Web of Science ®Google Scholar
• Wang X, Niu X, An N, et al. Comparative efficacy and safety of immunotherapy alone and in combination with chemotherapy for advanced non-small cell lung cancer. Front Oncol. 2021;11:611012.
   PubMed Web of Science ®Google Scholar
• Paz-Ares LG, Ramalingam SS, Ciuleanu TE, et al. First-line nivolumab plus ipilimumab in advanced NSCLC: 4-year outcomes from the randomized, open-label, phase 3 CheckMate 227 part 1 trial. J Thorac Oncol. 2022;17(2):289–308.
   PubMed Web of Science ®Google Scholar
• Bai R, Li L, Chen X, et al. Neoadjuvant and adjuvant immunotherapy: opening new horizons for patients with early-stage non-small cell lung cancer. Front Oncol. 2020;10:575472.
   PubMed Web of Science ®Google Scholar
• Provencio M, Nadal E, Insa A, 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. 2020;21(11):1413–1422.
   PubMed Web of Science ®Google Scholar
• The IASLC Lung cancer staging project: external validation of the revision of the TNM stage groupings in the eighth edition of the TNM classification of lung cancer. J Thorac Oncol. n.d. [cited 25 August 2022]. Available from: WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340], WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340WWW Documenthttps://www.jto.org/article/S1556-0864(17)30340
   Web of Science ®Google Scholar
• Forde PM, Spicer J, Lu S, et al. Abstract CT003: nivolumab (NIVO) + platinum-doublet chemotherapy (chemo) vs chemo as neoadjuvant treatment (tx) for resectable (IB-IIIA) non-small cell lung cancer (NSCLC) in the phase 3 CheckMate 816 trial. Cancer Res. 2021;81:CT003.
   Google Scholar
• Spicer J, Wang C, Tanaka F, et al. Surgical outcomes from the phase 3 CheckMate 816 trial: nivolumab (NIVO) + platinum-doublet chemotherapy (chemo) vs chemo alone as neoadjuvant treatment for patients with resectable non-small cell lung cancer (NSCLC). | ASCO 2021. J clin oncol. n.d.; [WWW Document]. https://ascopubs.org/do/abs/10.1200/JCO.2021.39.15_suppl.8503
   Google Scholar
• [cited 25 August 2022]. Available from: https://www.fda.gov/drugs/resources-information-approved-drugs/fda-approves-neoadjuvant-nivolumab-and-platinum-doublet-chemotherapy-early-stage-non-small-cell-lung
   Google Scholar
• Cascone T, Provencio M, Sepesi B, et al. Checkmate 77T: a phase III trial of neoadjuvant nivolumab (NIVO) plus chemotherapy (chemo) followed by adjuvant nivo in resectable early-stage NSCLC. J Clin Oncol. 2020;38: TPS9076-TPS9076.
   Google Scholar
• Peters S, Kim AW, Solomon B, et al. IMpower030: phase III study evaluating neoadjuvant treatment of resectable stage II-IIIB non-small cell lung cancer (NSCLC) with atezolizumab (atezo) + chemotherapy. Ann Oncol. 2019;30:ii30.
   Google Scholar
• Rothschild SI, Zippelius A, Eboulet EI, 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. 2021;39:2872–2880.
   PubMed Web of Science ®Google Scholar
• Felip E, Altorki N, Zhou C, et al. Adjuvant atezolizumab after adjuvant chemotherapy in resected stage IB–IIIA non-small-cell lung cancer (IMpower010): a randomised, multicentre, open-label, phase 3 trial. Lancet. 2021;398(10308):1344–1357.
   PubMed Web of Science ®Google Scholar
• Adjuvant Immunotherapy Approved for Lung Cancer - National Cancer Institute [WWW Document], 2021. [cited 2021 Dec 23]. Available from: https://www.cancer.gov/news-events/cancer-currents-blog/2021/fda-adjuvant-atezolizumab-lung-cancer
   Google Scholar
• Paz-Ares L, M.r.e O, Mauer M, 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. Published online March 17, 2022 (ESMO Virtual Plenary)
   Google Scholar
• Rossi G, Russo A, Tagliamento M, et al. Precision medicine for NSCLC in the era of immunotherapy: new biomarkers to select the most suitable treatment or the most suitable patient. Cancers (Basel). 2020;12(5):1125.
   PubMed Web of Science ®Google Scholar
• Sun R, Limkin EJ, Vakalopoulou M, et al. A radiomics approach to assess tumour-infiltrating CD8 cells and response to anti-PD-1 or anti-PD-L1 immunotherapy: an imaging biomarker, retrospective multicohort study. Lancet Oncol. 2019;19(9):1180–1191.
   Web of Science ®Google Scholar
• Cascone T, William WN, Weissferdt A, et al. Neoadjuvant nivolumab or nivolumab plus ipilimumab in operable non-small cell lung cancer: the phase 2 randomized NEOSTAR trial. Nat Med. 2021;27(3):504–514.
   PubMed Web of Science ®Google Scholar