Second-line therapy of squamous non-small cell lung cancer: an evolving landscape

References

• Torre LA, Siegel RL, Ward EM, et al. Global cancer incidence and mortality rates and trends–an update. Cancer Epidemiol Biomarkers Prev. 2016;25(1):16–27.
   PubMed Web of Science ®Google Scholar
• Kwak EL, Bang YJ, Camidge DR, et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med. 2010;363(18):1693–1703.
   PubMed Web of Science ®Google Scholar
• Santarpia M, Altavilla G, Salazar MF, et al. Tyrosine kinase inhibitors for non-small-cell lung cancer: finding patients who will be responsive. Expert Rev Respir Med. 2011;5(3):413–424.
   PubMed Web of Science ®Google Scholar
• Rosell R, Carcereny E, Gervais R, et al. Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol. 2012;13(3):239–246.
   PubMed Web of Science ®Google Scholar
• Lazzari C, Spitaleri G, Catania C, et al. Targeting ALK in patients with advanced non small cell lung cancer: biology, diagnostic and therapeutic options. Crit Rev Oncol Hematol. 2014;89(3):358–365.
   PubMed Web of Science ®Google Scholar
• Santarpia M, Altavilla G, Rosell R. Alectinib: a selective, next-generation ALK inhibitor for treatment of ALK-rearranged non-small-cell lung cancer. Expert Rev Respir Med. 2015;9(3):255–268.
   PubMed Web of Science ®Google Scholar
• Santarpia M, Gil N, Rosell R. Strategies to overcome resistance to tyrosine kinase inhibitors in non-small-cell lung cancer. Expert Rev Clin Pharmacol. 2015;8(4):461–477.
   PubMed Web of Science ®Google Scholar
• Rosell R, Karachaliou N. Large-scale screening for somatic mutations in lung cancer. Lancet. 2016;387(10026):1354–1356.
   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(21):3543–3551.
   PubMed Web of Science ®Google Scholar
• Reck M, von Pawel J, Zatloukal P, et al. Phase III trial of cisplatin plus gemcitabine with either placebo or bevacizumab as first-line therapy for nonsquamous non-small-cell lung cancer: aVAil. J Clin Oncol. 2009;27(8):1227–1234.
   PubMed Web of Science ®Google Scholar
• Scagliotti G, Hanna N, Fossella F, et al. The differential efficacy of pemetrexed according to NSCLC histology: a review of two Phase III studies. Oncologist. 2009;14(3):253–263.
   PubMed Web of Science ®Google Scholar
• Lortet-Tieulent J, Soerjomataram I, Ferlay J, et al. International trends in lung cancer incidence by histological subtype: adenocarcinoma stabilizing in men but still increasing in women. Lung Cancer. 2014;84(1):13–22.
   PubMed Web of Science ®Google Scholar
• Schaal C, Chellappan SP. Nicotine-mediated cell proliferation and tumor progression in smoking-related cancers. Mol Cancer Res. 2014;12(1):14–23.
   PubMed Web of Science ®Google Scholar
• Hecht SS. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat Rev Cancer. 2003;3(10):733–744.
   PubMed Web of Science ®Google Scholar
• Cheng H, Shcherba M, Kandavelou K, et al. Emerging drugs for squamous cell lung cancer. Expert Opin Emerg Drugs. 2015;20(1):149–160.
   PubMed Web of Science ®Google Scholar
• Besse B, Adjei A, Baas P, et al. 2nd ESMO consensus conference on lung cancer: non-small-cell lung cancer first-line/second and further lines of treatment in advanced disease. Ann Oncol. 2014;25(8):1475–1484.
   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(2):123–135.
   PubMed Web of Science ®Google Scholar
• Karachaliou N, Sosa AE, Barron FB, et al. Pharmacological management of relapsed/refractory NSCLC with chemical drugs. Expert Opin Pharmacother. 2017;18:295–304.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research N. Comprehensive genomic characterization of squamous cell lung cancers. Nature. 2012;489(7417):519–525.
   PubMed Web of Science ®Google Scholar
• Kris MG, Johnson BE, Berry LD, et al. Using multiplexed assays of oncogenic drivers in lung cancers to select targeted drugs. JAMA. 2014;311(19):1998–2006.
   PubMed Web of Science ®Google Scholar
• Thatcher N, Hirsch FR, Luft AV, et al. Necitumumab plus gemcitabine and cisplatin versus gemcitabine and cisplatin alone as first-line therapy in patients with stage IV squamous non-small-cell lung cancer (SQUIRE): an open-label, randomised, controlled phase 3 trial. Lancet Oncol. 2015;16(7):763–774.
   PubMed Web of Science ®Google Scholar
• Paz-Ares L, Socinski MA, Shahidi J, et al. Correlation of EGFR-expression with safety and efficacy outcomes in SQUIRE: a randomized, multicenter, open-label, phase III study of gemcitabine-cisplatin plus necitumumab versus gemcitabine-cisplatin alone in the first-line treatment of patients with stage IV squamous non-small-cell lung cancer. Ann Oncol. 2016;27(8):1573–1579.
   PubMed Web of Science ®Google Scholar
• Novello S, Barlesi F, Califano R, et al. Metastatic non-small-cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016;27(suppl 5):v1–v27.
   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.
   PubMed Web of Science ®Google Scholar
• Wilkerson MD, Yin X, Hoadley KA, et al. Lung squamous cell carcinoma mRNA expression subtypes are reproducible, clinically important, and correspond to normal cell types. Clin Cancer Res. 2010;16(19):4864–4875.
   PubMed Web of Science ®Google Scholar
• Campbell JD, Alexandrov A, Kim J, et al. Distinct patterns of somatic genome alterations in lung adenocarcinomas and squamous cell carcinomas. Nat Genet. 2016;48(6):607–616.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhao W, Zhou X. Integration of genomic data analysis for demonstrating potential targets in the subgroup populations of squamous cell lung cancer patients. Oncotarget. 2016 Jun 15. doi:10.18632/oncotarget.10072. [Epub ahead of print].
   Google Scholar
• Shepherd FA, Dancey J, Ramlau R, et al. Prospective randomized trial of docetaxel versus best supportive care in patients with non-small-cell lung cancer previously treated with platinum-based chemotherapy. J Clin Oncol. 2000;18(10):2095–2103.
   PubMed Web of Science ®Google Scholar
• Fossella FV, DeVore R, Kerr RN, et al. Randomized phase III trial of docetaxel versus vinorelbine or ifosfamide in patients with advanced non-small-cell lung cancer previously treated with platinum-containing chemotherapy regimens. J Clin Oncol. 2000;18(12):2354–2362.
   PubMed Web of Science ®Google Scholar
• Gridelli C, Gallo C, Di Maio M, et al. A randomised clinical trial of two docetaxel regimens (weekly vs 3 week) in the second-line treatment of non-small-cell lung cancer. The DISTAL 01 study. Br J Cancer. 2004;91(12):1996–2004.
   PubMed Web of Science ®Google Scholar
• Di Maio M, Perrone F, Chiodini P, et al. Individual patient data meta-analysis of docetaxel administered once every 3 weeks compared with once every week second-line treatment of advanced non-small-cell lung cancer. J Clin Oncol. 2007;25(11):1377–1382.
   PubMed Web of Science ®Google Scholar
• Adjei AA. Pemetrexed (ALIMTA), a novel multitargeted antineoplastic agent. Clin Cancer Res. 2004;10(12 Pt 2):4276s–80s.
   PubMed Web of Science ®Google Scholar
• Shepherd FA, Rodrigues Pereira J, Ciuleanu T, et al. Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med. 2005;353(2):123–132.
   PubMed Web of Science ®Google Scholar
• Kawaguchi T, Ando M, Asami K, et al. Randomized phase III trial of erlotinib versus docetaxel as second- or third-line therapy in patients with advanced non-small-cell lung cancer: docetaxel and Erlotinib Lung Cancer Trial (DELTA). J Clin Oncol. 2014;32(18):1902–1908.
   PubMed Web of Science ®Google Scholar
• Karampeazis A, Voutsina A, Souglakos J, et al. Pemetrexed versus erlotinib in pretreated patients with advanced non-small cell lung cancer: a Hellenic Oncology Research Group (HORG) randomized phase 3 study. Cancer. 2013;119(15):2754–2764.
   PubMed Web of Science ®Google Scholar
• Garassino MC, Martelli O, Broggini M, et al. Erlotinib versus docetaxel as second-line treatment of patients with advanced non-small-cell lung cancer and wild-type EGFR tumours (TAILOR): a randomised controlled trial. Lancet Oncol. 2013;14(10):981–988.
   PubMed Web of Science ®Google Scholar
• Taguchi F, Solomon B, Gregorc V, et al. Mass spectrometry to classify non-small-cell lung cancer patients for clinical outcome after treatment with epidermal growth factor receptor tyrosine kinase inhibitors: a multicohort cross-institutional study. J Natl Cancer Inst. 2007;99(11):838–846.
   PubMedGoogle Scholar
• Gregorc V, Novello S, Lazzari C, et al. Predictive value of a proteomic signature in patients with non-small-cell lung cancer treated with second-line erlotinib or chemotherapy (PROSE): a biomarker-stratified, randomised phase 3 trial. Lancet Oncol. 2014;15(7):713–721.
   PubMed Web of Science ®Google Scholar
• Peters S, Stahel RA, Dafni U, et al. Randomized phase III trial of erlotinib versus docetaxel in patients with advanced squamous cell non-small cell lung cancer failing first line platinum-based doublet chemotherapy stratified by Veristrat good versus Veristrat poor. The European Thoracic Oncology Platform (ETOP) EMPHASIS-lung trial. J Thorac Oncol. 2017 Apr;12(4):752-762. doi:10.1016/j.jtho.2016.12.017. Epub 2016 Dec 23.
   Web of Science ®Google Scholar
• Soria JC, Felip E, Cobo M, et al. Afatinib versus erlotinib as second-line treatment of patients with advanced squamous cell carcinoma of the lung (LUX-Lung 8): an open-label randomised controlled phase 3 trial. Lancet Oncol. 2015;16(8):897–907.
   PubMed Web of Science ®Google Scholar
• Garon EB, Ciuleanu TE, Arrieta O, et al. Ramucirumab plus docetaxel versus placebo plus docetaxel for second-line treatment of stage IV non-small-cell lung cancer after disease progression on platinum-based therapy (REVEL): a multicentre, double-blind, randomised phase 3 trial. Lancet. 2014;384(9944):665–673.
   PubMed Web of Science ®Google Scholar
• Reck M, Kaiser R, Mellemgaard A, et al. Docetaxel plus nintedanib versus docetaxel plus placebo in patients with previously treated non-small-cell lung cancer (LUME-Lung 1): a phase 3, double-blind, randomised controlled trial. Lancet Oncol. 2014;15(2):143–155.
   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
• 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(10030):1837–1846.
   PubMed Web of Science ®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
• Hanna N, Shepherd FA, Fossella FV, et al. Randomized phase III trial of pemetrexed versus docetaxel in patients with non-small-cell lung cancer previously treated with chemotherapy. J Clin Oncol. 2004;22(9):1589–1597.
   PubMed Web of Science ®Google Scholar
• Lynch TJ, Bell DW, Sordella R, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med. 2004;350(21):2129–2139.
   PubMed Web of Science ®Google Scholar
• Paez JG, Janne PA, Lee JC, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science. 2004;304(5676):1497–1500.
   PubMed Web of Science ®Google Scholar
• Mok TS, Wu YL, Thongprasert S, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med. 2009;361(10):947–957.
   PubMed Web of Science ®Google Scholar
• Rosell R, Moran T, Queralt C, et al. Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med. 2009;361(10):958–967.
   PubMed Web of Science ®Google Scholar
• Li N, Yang L, Ou W, et al. Meta-analysis of EGFR tyrosine kinase inhibitors compared with chemotherapy as second-line treatment in pretreated advanced non-small cell lung cancer. PLoS One. 2014;9(7):e102777.
   PubMed Web of Science ®Google Scholar
• Goss GD, Lee KH, Felip E. Evaluation of VeriStrat, a serum proteomic test, in the randomized, open-label, phase 3 LUX Lung 8 (LL8) trial of afatinib (A) versus erlotinib (E) for the second-line treatment of advanced squamous cell carcinoma (SCC) of the lung. J Clin Oncol. 34, 2016 (suppl; abstr e20510).
   Google Scholar
• Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1):57–70.
   PubMed Web of Science ®Google Scholar
• Sheng J, Yang Y, Ma Y, et al. The efficacy of combining antiangiogenic agents with chemotherapy for patients with advanced non-small cell lung cancer who failed first-line chemotherapy: a systematic review and meta-analysis. PLoS One. 2015;10(6):e0127306.
   PubMed Web of Science ®Google Scholar
• Spratlin JL, Cohen RB, Eadens M, et al. Phase I pharmacologic and biologic study of ramucirumab (IMC-1121B), a fully human immunoglobulin G1 monoclonal antibody targeting the vascular endothelial growth factor receptor-2. J Clin Oncol. 2010;28(5):780–787.
   PubMed Web of Science ®Google Scholar
• Yamamoto H, Shigematsu H, Nomura M, et al. PIK3CA mutations and copy number gains in human lung cancers. Cancer Res. 2008;68(17):6913–6921.
   PubMed Web of Science ®Google Scholar
• Weiss J, Sos ML, Seidel D, et al. Frequent and focal FGFR1 amplification associates with therapeutically tractable FGFR1 dependency in squamous cell lung cancer. Sci Transl Med. 2010;2(62):62ra93.
   PubMed Web of Science ®Google Scholar
• Hammerman PS, Sos ML, Ramos AH, et al. Mutations in the DDR2 kinase gene identify a novel therapeutic target in squamous cell lung cancer. Cancer Discov. 2011;1(1):78–89.
   PubMed Web of Science ®Google Scholar
• Miao L, Wang Y, Zhu S, et al. Identification of novel driver mutations of the discoidin domain receptor 2 (DDR2) gene in squamous cell lung cancer of Chinese patients. BMC Cancer. 2014;14:369.
   PubMed Web of Science ®Google Scholar
• Pan Y, Wang R, Ye T, et al. Comprehensive analysis of oncogenic mutations in lung squamous cell carcinoma with minor glandular component. Chest. 2014;145(3):473–479.
   PubMed Web of Science ®Google Scholar
• Langer CJ, Obasaju C, Bunn P, et al. Incremental innovation and progress in advanced squamous cell lung cancer: current status and future impact of treatment. J Thorac Oncol. 2016;11(12):2066–2081.
   PubMed Web of Science ®Google Scholar
• Brunner AM, Costa DB, Heist RS, et al. Treatment-related toxicities in a phase II trial of dasatinib in patients with squamous cell carcinoma of the lung. J Thorac Oncol. 2013;8(11):1434–1437.
   PubMed Web of Science ®Google Scholar
• Justilien V, Walsh MP, Ali SA, et al. The PRKCI and SOX2 oncogenes are coamplified and cooperate to activate Hedgehog signaling in lung squamous cell carcinoma. Cancer Cell. 2014;25(2):139–151.
   PubMed Web of Science ®Google Scholar
• Lum L, Beachy PA. The Hedgehog response network: sensors, switches, and routers. Science. 2004;304(5678):1755–1759.
   PubMed Web of Science ®Google Scholar
• Huang L, Walter V, Hayes DN, et al. Hedgehog-GLI signaling inhibition suppresses tumor growth in squamous lung cancer. Clin Cancer Res. 2014;20(6):1566–1575.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674.
   PubMed Web of Science ®Google Scholar
• Pardoll DM. Immunology beats cancer: a blueprint for successful translation. Nat Immunol. 2012;13(12):1129–1132.
   PubMed Web of Science ®Google Scholar
• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252–264.
   PubMed Web of Science ®Google Scholar
• Karachaliou N, Sosa AE, Rosell R. Unraveling the genomic complexity of small cell lung cancer. Transl Lung Cancer Res. 2016;5(4):363–366.
   PubMed Web of Science ®Google Scholar
• Bustamante Alvarez JG, Gonzalez-Cao M, Karachaliou N, et al. Advances in immunotherapy for treatment of lung cancer. Cancer Biol Med. 2015;12(3):209–222.
   PubMed Web of Science ®Google Scholar
• Santarpia M, Giovannetti E, Rolfo C, et al. Recent developments in the use of immunotherapy in non-small cell lung cancer. Expert Rev Respir Med. 2016;10(7):781–798.
   PubMed Web of Science ®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(3):257–265.
   PubMed Web of Science ®Google Scholar
• Goldberg SB, Gettinger SN, Mahajan A, et al. Pembrolizumab for patients with melanoma or non-small-cell lung cancer and untreated brain metastases: early analysis of a non-randomised, open-label, phase 2 trial. Lancet Oncol. 2016;17(7):976–983.
   PubMed Web of Science ®Google Scholar
• Rosell R, Karachaliou N. Trends in immunotherapy for brain metastases. Lancet Oncol. 2016;17(7):859–860.
   PubMed Web of Science ®Google Scholar
• Michot JM, Bigenwald C, Champiat S, et al. Immune-related adverse events with immune checkpoint blockade: a comprehensive review. Eur J Cancer. 2016;54:139–148.
   PubMed Web of Science ®Google Scholar
• Johnson DB, Balko JM, Compton ML, et al. Fulminant myocarditis with combination immune checkpoint blockade. N Engl J Med. 2016;375(18):1749–1755.
   PubMed Web of Science ®Google Scholar
• Weber JS, Yang JC, Atkins MB, et al. Toxicities of immunotherapy for the practitioner. J Clin Oncol. 2015;33(18):2092–2099.
   PubMed Web of Science ®Google Scholar
• Okano Y, Satoh T, Horiguchi K, et al. Nivolumab-induced hypophysitis in a patient with advanced malignant melanoma. Endocr J. 2016;63(10):905–912.
   PubMed Web of Science ®Google Scholar
• Nishino M, Ramaiya NH, Awad MM, et al. PD-1 inhibitor-related pneumonitis in advanced cancer patients: radiographic patterns and clinical course. Clin Cancer Res. 2016;22(24):6051–6060.
   PubMed Web of Science ®Google Scholar
• Nishino M, Sholl LM, Hodi FS, et al. Anti-PD-1-related pneumonitis during cancer immunotherapy. N Engl J Med. 2015;373(3):288–290.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Cao M, Boada A, Teixido C, et al. Fatal gastrointestinal toxicity with ipilimumab after BRAF/MEK inhibitor combination in a melanoma patient achieving pathological complete response. Oncotarget. 2016;7(35):56619–56627.
   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(7528):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(2):208-222. Epub 2016 Nov 29.
   Web of Science ®Google Scholar
• Nicolazzo C, Raimondi C, Mancini M, et al. Monitoring PD-L1 positive circulating tumor cells in non-small cell lung cancer patients treated with the PD-1 inhibitor Nivolumab. Sci Rep. 2016;6:31726.
   PubMed Web of Science ®Google Scholar
• Brown SD, Warren RL, Gibb EA, et al. Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res. 2014;24(5):743–750.
   PubMed Web of Science ®Google Scholar
• Le DT, Uram JN, Wang H, et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med. 2015;372(26):2509–2520.
   PubMed Web of Science ®Google Scholar
• Rizvi NA, Hellmann MD, Snyder A, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015;348(6230):124–128.
   PubMed Web of Science ®Google Scholar
• Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348(6230):69–74.
   PubMed Web of Science ®Google Scholar
• Ock CY, Keam B, Kim S, et al. Pan-cancer immunogenomic perspective on the tumor microenvironment based on PD-L1 and CD8 T-cell infiltration. Clin Cancer Res. 2016;22(9):2261–2270.
   PubMed Web of Science ®Google Scholar
• Gros A, Parkhurst MR, Tran E, et al. Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat Med. 2016;22(4):433–438.
   PubMed Web of Science ®Google Scholar
• Schumacher TN, Scheper W. A liquid biopsy for cancer immunotherapy. Nat Med. 2016;22(4):340–341.
   PubMed Web of Science ®Google Scholar