The role of immune checkpoint inhibitors in advanced non-small cell lung cancer

References

• Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–86.
   PubMed Web of Science ®Google Scholar
• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68:7–30.
   PubMed Web of Science ®Google Scholar
• Hashim D, Boffetta P, La Vecchia C, et al. The global decrease in cancer mortality: trends and disparities. Ann Oncol. 2016;27:926–933.
   PubMed Web of Science ®Google Scholar
• Sandler AB, Nemunaitis J, Denham C, et al. Phase III trial of gemcitabine plus cisplatin versus cisplatin alone in patients with locally advanced or metastatic non-small-cell lung cancer. J Clin Oncol. 2000;18:122–130.
   PubMed Web of Science ®Google Scholar
• Wozniak AJ, Crowley JJ, Balcerzak SP, et al. Randomized trial comparing cisplatin with cisplatin plus vinorelbine in the treatment of advanced non-small-cell lung cancer: a Southwest oncology group study. J Clin Oncol. 1998;16:2459–2465.
   PubMed Web of Science ®Google Scholar
• Scagliotti GV, Parikh P, von Pawel J, et al. Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol. 2008;26:3543–3551.
   PubMed Web of Science ®Google Scholar
• Reck M, von Pawel J, Zatloukal P, et al. Overall survival with cisplatin-gemcitabine and bevacizumab or placebo as first-line therapy for nonsquamous non-small-cell lung cancer: results from a randomised phase III trial (AVAiL). Ann Oncol. 2010;21:1804–1809.
   PubMed Web of Science ®Google Scholar
• Masters GA, Temin S, Azzoli CG, et al. Systemic therapy for stage IV non-small-cell lung cancer: American Society of clinical oncology clinical practice guideline update. J Clin Oncol. 2015;33:3488–3515.
   PubMed Web of Science ®Google Scholar
• Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348:56–61.
   PubMed Web of Science ®Google Scholar
• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–264.
   PubMed Web of Science ®Google Scholar
• Schneider H, Downey J, Smith A, et al. Reversal of the TCR stop signal by CTLA-4. Science. 2006;313:1972–1975.
   PubMed Web of Science ®Google Scholar
• Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39:1–10.
   PubMed Web of Science ®Google Scholar
• Fecher LA, Agarwala SS, Hodi FS, et al. Ipilimumab and its toxicities: a multidisciplinary approach. Oncologist. 2013;18:733–743.
   PubMed Web of Science ®Google Scholar
• Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J Clin Oncol. 2015;33:1974–1982.
   PubMed Web of Science ®Google Scholar
• Butte MJ, Keir ME, Phamduy TB, et al. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity. 2007;27:111–122.
   PubMed Web of Science ®Google Scholar
• Chen DS, Irving BA, Hodi FS. Molecular pathways: next-generation immunotherapy–inhibiting programmed death-ligand 1 and programmed death-1. Clin Cancer Res off J Am Assoc Cancer Res. 2012;18:6580–6587.
   PubMed Web of Science ®Google Scholar
• Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366:2443–2454.
   PubMed Web of Science ®Google Scholar
• Ribas A. Tumor immunotherapy directed at PD-1. N Engl J Med. 2012;366:2517–2519.
   PubMed Web of Science ®Google Scholar
• Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012;366:2455–2465.
   PubMed Web of Science ®Google Scholar
• Brahmer J, Horn L, Jackman D, et al. Five-year follow-up from the CA209-003 study of nivolumab in previously treated advanced non-small cell lung cancer (NSCLC): clinical characteristics of long-term survivors. Cancer Res. 2017;77(13 Supplement):CT077.
   Google Scholar
• Rizvi NA, Mazieres J, Planchard D, et al. Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): a phase 2, single-arm trial. Lancet Oncol. 2015;16:257–265.
   PubMed Web of Science ®Google Scholar
• Brahmer J, Reckamp KL, Baas P, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373:123–135.
   PubMed Web of Science ®Google Scholar
• Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373:1627–1639.
   PubMed Web of Science ®Google Scholar
• Vokes EE, Ready N, Felip E, et al. Nivolumab versus docetaxel in previously treated advanced non-small-cell lung cancer (CheckMate 017 and CheckMate 057): 3-year update and outcomes in patients with liver metastases. Ann Oncol. 2018;29:959–965.
   PubMed Web of Science ®Google Scholar
• Garon EB, Rizvi NA, Hui R, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015;372:2018–2028.
   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;387:1540–1550.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Garon EB, Kim D-W, et al. Long-term survival in patients (pts) with advanced NSCLC in the KEYNOTE-010 study overall and in pts who completed two years of pembrolizumab. Ann Oncol. 2018;29(8):LBA63.
   Google Scholar
• Fehrenbacher L, Spira A, Ballinger M, et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial. Lancet. 2016;387:1837–1846.
   PubMed Web of Science ®Google Scholar
• Mazières J, Park K, Lewanski C, et al. 136PD_PR 3-year survival and duration of response in randomized phase II study of atezolizumab (atezo) vs docetaxel (doc) in 2L+ NSCLC (POPLAR). J Thoracic Oncol. 2018 Apr;13(4S):S79.
   Google Scholar
• Rittmeyer A, Barlesi F, Waterkamp D, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet. 2017;389:255–265.
   PubMed Web of Science ®Google Scholar
• Aguiar PN Jr., De Mello RA, Barreto CMN, et al. Immune checkpoint inhibitors for advanced non-small cell lung cancer: emerging sequencing for new treatment targets. ESMO Open. 2017;2:e000200.
   PubMed Web of Science ®Google Scholar
• Gulley JL, Rajan A, Spigel DR, et al. Avelumab for patients with previously treated metastatic or recurrent non-small-cell lung cancer (JAVELIN solid tumor): dose-expansion cohort of a multicentre, open-label, phase 1b trial. Lancet Oncol. 2017;18:599–610.
   PubMed Web of Science ®Google Scholar
• Rajan A, Gulley JL, Spigel DR, et al. Avelumab (anti–PD-L1) in patients with platinum-treated advanced NSCLC: 2.5-year follow-up from the JAVELIN solid tumor trial. J Clin Oncol. 2018;36(15_suppl):9090.
   Google Scholar
• Barlesi F, Vansteenkiste J, Spigel D, et al. Avelumab versus docetaxel in patients with platinum-treated advanced non-small-cell lung cancer (JAVELIN Lung 200): an open-label, randomised, phase 3 study. Lancet Oncol. 2018;19:1468–1479.
   PubMed Web of Science ®Google Scholar
• Antonia SJ, Brahmer JR, Khleif S, et al. Phase 1/2 study of the safety and clinical activity of durvalumab in patients with non-small cell lung cancer (NSCLC). Ann Oncol. 2016;27:1216PD.
   Web of Science ®Google Scholar
• Garassino MC, Cho BC, Kim JH, et al. Durvalumab as third-line or later treatment for advanced non-small-cell lung cancer (ATLANTIC): an open-label, single-arm, phase 2 study. Lancet Oncol. 2018;19:521–536.
   PubMed Web of Science ®Google Scholar
• Gettinger S, Rizvi NA, Chow LQ, et al. Nivolumab monotherapy for first-line treatment of advanced non-small-cell lung cancer. J Clin Oncol. 2016;34:2980–2987.
   PubMed Web of Science ®Google Scholar
• Carbone DP, Reck M, Paz-Ares L, et al. First-line Nivolumab in Stage IV or recurrent non-small-cell lung cancer. N Engl J Med. 2017;376:2415–2426.
   PubMed Web of Science ®Google Scholar
• Reck M, Rodriguez-Abreu D, Robinson AG, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375:1823–1833.
   PubMed Web of Science ®Google Scholar
• Brahmer JR, Rodríguez-Abreu D, Robinson AG, et al. Updated analysis of KEYNOTE-024: pembrolizumab vs platinum-based chemotherapy for advanced NSCLC with PD-L1≥50%. J Thoracic Oncol. 2017;12(11):S1793–S1794.
   Web of Science ®Google Scholar
• Lopes G, Wu YL, Kudaba I, et al. Pembrolizumab (pembro) versus platinum-based chemotherapy (chemo) as first-line therapy for advanced/metastatic NSCLC with a PD-L1 tumor proportion score (TPS) ≥ 1%: open-label, phase 3 KEYNOTE-042 study. J clin oncol. 2018;36(18_suppl):LBA4–LBA4.
   Web of Science ®Google Scholar
• Peters S, Gettinger S, Johnson ML, et al. Phase II trial of atezolizumab as first-line or subsequent therapy for patients with programmed death-ligand 1-selected advanced non-small-cell lung cancer (BIRCH). J Clin Oncol. 2017;35:2781–2789.
   PubMed Web of Science ®Google Scholar
• Reck M, Kf R. Precision diagnosis and treatment for advanced non-small-cell lung cancer. N Engl J Med. 2017;377:849–861.
   PubMed Web of Science ®Google Scholar
• Boussiotis VA. Molecular and Biochemical Aspects of the PD-1 Checkpoint Pathway. N Engl J Med. 2016;375:1767–1778.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Soria JC, Kowanetz M, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014;515:563–567.
   PubMed Web of Science ®Google Scholar
• Hirsch FR, McElhinny A, Stanforth D, et al. PD-L1 Immunohistochemistry Assays for Lung Cancer: results from Phase 1 of the Blueprint PD-L1 IHC Assay Comparison Project. J Thorac Oncol. 2017;12:208–222.
   PubMed Web of Science ®Google Scholar
• Rimm D, Han G, Taube JM, et al. ORAL01.01: A Prospective, Multi-Institutional Assessment of Four Assays for PD-L1 Expression in NSCLC by Immunohistochemistry: topic: pathology. J Thorac Oncol. 2016;11:S249.
   PubMed Web of Science ®Google Scholar
• McGranahan N, Furness AJ, Rosenthal R, et al. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science. 2016;351:1463–1469.
   PubMed Web of Science ®Google Scholar
• Rizvi NA, Hellmann MD, Snyder A, et al. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015;348:124–128. Cancer immunology.
   PubMed Web of Science ®Google Scholar
• Hellmann MD, Rizvi NA, Goldman JW, et al. Nivolumab plus ipilimumab as first-line treatment for advanced non-small-cell lung cancer (CheckMate 012): results of an open-label, phase 1, multicohort study. Lancet Oncol. 2017;18:31–41.
   PubMed Web of Science ®Google Scholar
• Yarchoan M, Hopkins A, Jaffee EM. Tumor Mutational Burden and Response Rate to PD-1 Inhibition. N Engl J Med. 2017;377:2500–2501.
   PubMed Web of Science ®Google Scholar
• Hanna N, Johnson D, Temin S, et al. Systemic therapy for stage iv non-small-cell lung cancer: American Society of clinical oncology clinical practice guideline update summary. J Oncol Pract. 2017;13:832–837.
   PubMed Web of Science ®Google Scholar
• Planchard D, Popat S, Kerr K, et al. Metastatic non-small cell lung cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018;29:iv192–iv237.
   PubMed Web of Science ®Google Scholar
• Wang Z, Till B, Gao Q. Chemotherapeutic agent-mediated elimination of myeloid-derived suppressor cells. Oncoimmunology. 2017;6:e1331807.
   PubMed Web of Science ®Google Scholar
• Roselli M, Cereda V, Di Bari MG, et al. Effects of conventional therapeutic interventions on the number and function of regulatory T cells. Oncoimmunology. 2013;2:e27025.
   PubMed Web of Science ®Google Scholar
• Kroemer G, Galluzzi L, Kepp O, et al. Immunogenic cell death in cancer therapy. Annu Rev Immunol. 2013;31:51–72.
   PubMed Web of Science ®Google Scholar
• Peng J, Hamanishi J, Matsumura N, et al. Chemotherapy induces programmed cell death-ligand 1 overexpression via the nuclear factor-kappaB to Foster an immunosuppressive tumor microenvironment in ovarian cancer. Cancer Res. 2015;75:5034–5045.
   PubMed Web of Science ®Google Scholar
• Gadgeel SM, Stevenson J, Langer CJ, et al. Pembrolizumab (pembro) plus chemotherapy as front-line therapy for advanced NSCLC: KEYNOTE-021 cohorts A-C. J clin oncol. 2017;4(15_suppl):9016.
   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;17:1497–1508.
   PubMed Web of Science ®Google Scholar
• Borghaei H, Langer CJ, Gadgeel S, et al. Updated results from KEYNOTE-021 cohort G: a randomized, phase II study of pemetrexed and carboplatin with or without pembrolizumab as first-line therapy for advanced nonsquamous non-small-cell lung cancer. Ann Oncol. 2017;28:636-637.
   Web of Science ®Google Scholar
• Rizvi NA, Hellmann MD, Brahmer JR, et al. Nivolumab in combination with platinum-based doublet chemotherapy for first-line treatment of advanced non-small-cell lung cancer. J Clin Oncol. 2016;34:2969–2979.
   PubMed Web of Science ®Google Scholar
• Liu SV, Camidge DR, Gettinger SN, et al. Atezolizumab (atezo) plus platinum-based chemotherapy (chemo) in non-small cell lung cancer (NSCLC): update from a phase Ib study. J clin oncol. 2017;35(15_suppl):9092.
   Google Scholar
• Gandhi L, Rodriguez-Abreu D, Gadgeel S, et al. Pembrolizumab plus Chemotherapy in Metastatic Non-Small-Cell Lung Cancer. N Engl J Med. 2018;378:2078–2092.
   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;379:2040–51.
   PubMed Web of Science ®Google Scholar
• Schiller JH. A new standard of care for advanced lung cancer. N Engl J Med. 2018;378:2135–2137.
   PubMed Web of Science ®Google Scholar
• Jotte RM, Cappuzzo F, Vynnychenko I, et al. IMpower131: primary PFS and safety analysis of a randomized phase III study of atezolizumab + carboplatin + paclitaxel or nab-paclitaxel vs carboplatin + nab-paclitaxel as 1L therapy in advanced squamous NSCLC. J clin oncol. 2018;36(18_suppl):LBA9000–LBA9000.
   Web of Science ®Google Scholar
• Papadimitrakopoulou V, Cobo M, Bordoni R, et al. OA05.07 IMpower132: PFS and safety results with 1L Atezolizumab + Carboplatin/Cisplatin + Pemetrexed in Stage IV non-squamous NSCLC. J Thorac Oncol. 2018;13:S332–S3.
   Web of Science ®Google Scholar
• Cappuzzo F, McCleod M, Hussein M, et al. IMpower 130: progression-free survival and safety analysis from a randomised phase III study of carboplatin+ nab-paclitaxel with or without atezolizumab as first-line therapy in advanced non-squamous NSCLC. Ann Oncol. 2018;29:viii742–3.
   Web of Science ®Google Scholar
• Borghaei H, Hellmann MD, Paz-Ares LG, et al. Nivolumab (Nivo) + platinum-doublet chemotherapy (Chemo) vs chemo as first-line (1L) treatment (Tx) for advanced non-small cell lung cancer (NSCLC) with <1% tumor PD-L1 expression: results from CheckMate 227. J clin oncol. 2018;36(15_suppl):9001.
   Web of Science ®Google Scholar
• Yoon SM, Shaikh T, Hallman M. Therapeutic management options for stage III non-small cell lung cancer. World J Clin Oncol. 2017;8:1–20.
   PubMed Web of Science ®Google Scholar
• Dovedi SJ, Adlard AL, Lipowska-Bhalla G, et al. Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade. Cancer Res. 2014;74:5458–5468.
   PubMed Web of Science ®Google Scholar
• Deng L, Liang H, Burnette B, et al. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest. 2014;124:687–695.
   PubMed Web of Science ®Google Scholar
• Antonia SJ, Villegas A, Daniel D, et al. Durvalumab after chemoradiotherapy in Stage III non-small-cell lung cancer. N Engl J Med. 2017; 377:1919–1929.
   PubMed Web of Science ®Google Scholar
• Antonia SJ, Villegas A, Daniel D, et al. Overall survival with durvalumab after chemoradiotherapy in Stage III NSCLC. N Engl J Med. 2018;379:2342–2450.
   PubMed Web of Science ®Google Scholar
• Rizvi NA, Peters S. Immunotherapy for unresectable Stage III non-small-cell lung cancer. N Engl J Med. 2017;377:1986–8.
   PubMed Web of Science ®Google Scholar
• Peters S, Dafni U, Boyer M, et al. Position of a panel of international lung cancer experts on the approval decision for use of durvalumab in stage III non-small-cell lung cancer (NSCLC) by the Committee for Medicinal Products for Human Use (CHMP). Ann Oncol. 2019;30:161–165.
   PubMed Web of Science ®Google Scholar
• Rodionov EO, Miller SV, Tuzikov SA, et al. The results of treatment of non-small cell lung cancer stage III with a preoperative vinorelbine/carboplatin and personalized adjuvant chemotherapy. Ann Oncol. 2018;29:viii488–viii92.
   Web of Science ®Google Scholar
• Allen E, Jabouille A, Rivera LB, et al. Combined antiangiogenic and anti-PD-L1 therapy stimulates tumor immunity through HEV formation. Sci Transl Med. 2017;9.
   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; 378:2288–2301.
   PubMed Web of Science ®Google Scholar
• Socinski MA, Jotte RM, Cappuzzo F, et al. Overall survival (OS) analysis of IMpower150, a randomized Ph 3 study of atezolizumab (atezo) + chemotherapy (chemo) ± bevacizumab (bev) vs chemo + bev in 1L nonsquamous (NSQ) NSCLC. J clin oncol. 2018;36(15_suppl):9002.
   Web of Science ®Google Scholar
• Reck M, Karagiannis T, Wehler T, et al. Patient-reported outcomes (PROs) in the randomized, phase III IMpower150 study of atezolizumab (atezo) + chemotherapy (chemo) ± bevacizumab (bev) vs chemo + bev in 1L nonsquamous metastatic NSCLC (mNSCLC). J clin oncol. 2018;36(15_suppl):9047.
   Web of Science ®Google Scholar
• Ramalingam SS, Hellmann MD, Awad MM et al. Tumor mutational burden (TMB) as a biomarker for clinical benefit from dual immune checkpoint blockade with nivolumab (nivo) + ipilimumab (ipi) in first-line (1L) non-small cell lung cancer (NSCLC): identification of TMB cutoff from CheckMate 568. Presented at the American Association for Cancer Research 2018 Annual Meeting; 2018 April 16; Chicago.
   Google Scholar
• Hellmann MD, Ciuleanu TE, Pluzanski A, et al. Nivolumab plus Ipilimumab in lung cancer with a high tumor mutational burden. N Engl J Med. 2018; 378:2093–2104).
   PubMed Web of Science ®Google Scholar
• Bristol-Myers Squibb [ Published 2018 October 19; cited 2018 Feb 14]. https://bit.ly/2ySdgoC
   Google Scholar
• Hellmann MD, Nathanson T, Rizvi H, et al. Genomic features of response to combination immunotherapy in patients with advanced non-small-cell lung cancer. Cancer Cell. 2018;33:843–852, e4.
   PubMed Web of Science ®Google Scholar
• Rizvi H, Sanchez-Vega F, La K, et al. Molecular determinants of response to anti-programmed cell death (PD)-1 and anti-programmed death-ligand 1 (PD-L1) blockade in patients with non-small-cell lung cancer profiled with targeted next-generation sequencing. J Clin Oncol. 2018;36:633–641.
   PubMed Web of Science ®Google Scholar
• Gandara DR, Paul SM, Kowanetz M, et al. Blood-based tumor mutational burden as a predictor of clinical benefit in non-small-cell lung cancer patients treated with atezolizumab. Nat Med. 2018;24:1441–1448.
   PubMed Web of Science ®Google Scholar
• Velcheti V, Kim ES, Mekhail T, et al. Prospective clinical evaluation of blood-based tumor mutational burden (bTMB) as a predictive biomarker for atezolizumab (atezo) in 1L non-small cell lung cancer (NSCLC): interim B-F1RST results. J clin oncol. 2018;36:12001.
   Web of Science ®Google Scholar
• Le DT, Durham JN, Smith KN, et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science. 2017;357:409–413.
   PubMed Web of Science ®Google Scholar
• Gettinger SN, Wurtz A, Goldberg SB, et al. Clinical features and management of acquired resistance to PD-1 axis inhibitors in 26 patients with advanced non-small cell lung cancer. J Thorac Oncol. 2018;13:831–839.
   PubMed Web of Science ®Google Scholar