The LUX-Lung clinical trial program of afatinib for non-small-cell lung cancer

References

• Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J. Clin.60(5), 277–300 (2010).
   PubMed Web of Science ®Google Scholar
• Ferlay J, Parkin DM, Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008. Eur. J. Cancer46(4), 765–781 (2010).
   PubMed Web of Science ®Google Scholar
• Ramalingam S, Belani C. Systemic chemotherapy for advanced non-small cell lung cancer: recent advances and future directions. Oncologist13(Suppl. 1), 5–13 (2008).
   PubMed Web of Science ®Google Scholar
• Sandler A, Gray R, Perry MC et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N. Engl. J. Med.355(24), 2542–2550 (2006).
   PubMed Web of Science ®Google Scholar
• Pirker R, Pereira JR, Szczesna A et al. Cetuximab plus chemotherapy in patients with advanced non-small-cell lung cancer (FLEX): an open-label randomised Phase III trial. Lancet373(9674), 1525–1531 (2009).
   PubMed Web of Science ®Google Scholar
• Metro G, Cappuzzo F. New targeted therapies for non-small-cell lung cancer. Therapy6(3), 335–350 (2009).
   Google Scholar
• Kwak EL, Bang YJ, Camidge DR et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N. Engl. J. Med.363(18), 1693–1703 (2010).
   PubMed Web of Science ®Google Scholar
• Mendelsohn J, Baselga J. Epidermal growth factor receptor targeting in cancer. Semin. Oncol.33(4), 369–385 (2006).
   PubMed Web of Science ®Google Scholar
• Sharma SV, Bell DW, Settleman J, Haber DA. Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer7(3), 169–181 (2007).
   PubMed Web of Science ®Google Scholar
• Paez JG, Jänne PA, Lee JC et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science304(5676), 1497–1500 (2004).
   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.350(21), 2129–2139 (2004).
   PubMed Web of Science ®Google Scholar
• Pao W, Miller V, Zakowski M et al. EGF receptor gene mutations are common in lung cancers from never smokers and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc. Natl Acad. Sci. USA101(36), 13306–13311 (2004).
   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.361(10), 947–957 (2009).
   PubMed Web of Science ®Google Scholar
• Lee JS, Park K, Kim SW et al. A randomized Phase III study of gefitinib (IRESSA™) versus standard chemotherapy (gemcitabine plus cisplatin) as a first-line treatment for never-smokers with advanced or metastatic adenocarcinoma of the lung J. Thor. Oncol.4(Suppl.), 4 (2009) (Abstract).
   Google Scholar
• Mitsudomi T, Morita S, Yatabe Y et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol.11(2), 121–128 (2010).
   PubMed Web of Science ®Google Scholar
• Maemondo M, Inoue A, Kobayashi K et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N. Engl. J. Med.362(25), 2380–2388 (2010).
   PubMed Web of Science ®Google Scholar
• Zhou C, Wu YL, Chen G et al. Efficacy results from the randomised Phase III OPTIMAL (CTONG 0802) study comparing first-line erlotinib versus carboplatin plus gemcitabine, in chinese advanced non-small-cell lung cancer patients with EGFR activating mutations. Ann. Oncol.21(Suppl. 8), LBA 13 (2010).
   Google Scholar
• Mitsudomi T, Kosaka T, Yatabe Y. Biological and clinical implications of EGFR mutations in lung cancer. Int. J. Clin. Oncol.11(3), 190–198 (2006).
   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.361(10), 958–967 (2009).
   PubMed Web of Science ®Google Scholar
• Murray S, Dahabreh IJ, Linardou H, Manoloukos M, Bafaloukos D, Kosmidis P. Somatic mutations of the tyrosine kinase domain of epidermal growth factor receptor and tyrosine kinase inhibitor response to TKIs in non-small cell lung cancer: an analytical database. J. Thorac. Oncol.3(8), 832–839 (2008).
   PubMed Web of Science ®Google Scholar
• Jackman DM, Yeap BY, Sequist LV et al. Exon 19 deletion mutations of epidermal growth factor receptor are associated with prolonged survival in non-small cell lung cancer patients treated with gefitinib or erlotinib. Clin. Cancer Res.12(13), 3908–3914 (2006).
   PubMed Web of Science ®Google Scholar
• Paz-Ares L, Soulières D, Melezínek I et al. Clinical outcomes in non-small-cell lung cancer patients with EGFR mutations: pooled analysis. J. Cell Mol. Med.14(1–2), 51–69 (2010).
   PubMed Web of Science ®Google Scholar
• Greulich H, Chen TH, Feng W et al. Oncogenic transformation by inhibitor-sensitive and – resistant EGFR mutants. PloS Med.2(11), e313 (2005).
   PubMed Web of Science ®Google Scholar
• Wu JY, Wu SG, Yang CH et al. Lung cancer with epidermal growth factor receptor exon 20 mutations is associated with poor gefitinib treatment response. Clin. Cancer Res.14(15), 4877–4882 (2008).
   PubMed Web of Science ®Google Scholar
• Kobayashi S, Boggon TJ, Dayaram T et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N. Engl. J. Med.352(8), 786–792 (2005).
   PubMed Web of Science ®Google Scholar
• Pao W, Miller VA, Politi KA et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PloS Med.2(3), e73 (2005).
   PubMed Web of Science ®Google Scholar
• Balak MN, Gong Y, Riely GJ et al. Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinomas with acquired resistance to kinase inhibitors. Clin. Cancer Res.12(21), 6494–6501 (2006).
   PubMed Web of Science ®Google Scholar
• Maheswaran S, Sequist LV, Nagrath S et al. Detection of mutations in EGFR in circulating lung-cancer cells. N. Engl. J. Med.359(4), 366–377 (2008).
   PubMed Web of Science ®Google Scholar
• Bean J, Riely GJ, Balak M et al. Acquired resistance to epidermal growth factor receptor kinase inhibitors associated with a novel T854A mutation in a patient with EGFR-mutant lung adenocarcinoma. Clin. Cancer Res.14(22), 7519–7525 (2008).
   PubMed Web of Science ®Google Scholar
• Engelman JA, Zejnullahu K, Mitsudomi T et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science316(5827), 1039–1043 (2007).
   PubMed Web of Science ®Google Scholar
• Bean J, Brennan C, Shih JY et al. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc. Natl Acad. Sci. USA104(52), 20932–20937 (2007).
   PubMed Web of Science ®Google Scholar
• Oxnard GR, Arcila ME, Sima C et al. Acquired resistance to EGFR tyrosine kinase inhibitors in EGFR mutant lung cancer: Distinct natural history of patients with tumors harboring the T790M mutation. Clin. Cancer Res.17(6), 1616–1622 (2011).
   PubMed Web of Science ®Google Scholar
• Li D, Ambrogio L, Shimamura T et al. BIBW2992, an irreversible EGFR/HER2 inhibitor highly effective in preclinical lung cancer models. Oncogene27(34), 4702–4711 (2008).
   PubMed Web of Science ®Google Scholar
• Yap TA, Vidal L, Adam J et al. Phase I trial of the irreversible EGFR and HER2 kinase inhibitor BIBW 2992 in patients with advanced solid tumors. J. Clin. Oncol.28(25), 3965–3972 (2010).
   PubMed Web of Science ®Google Scholar
• Lewis N, Marshall J, Amelsberg A et al. A Phase I dose escalation study of BIBW 2992, an irreversible dual EGFR/HER2 receptor tyrosine kinase inhibitor, in a 3 week on 1 week off schedule in patients with advanced solid tumors. Proc. Am. Soc. Clin. Oncol.24(Suppl. 18), 3091 (2006) (Abstract).
   Web of Science ®Google Scholar
• Agus DB, Terlizzi E, Stopfer P, Amelsberg A, Gordon MS. A Phase I dose escalation study of BIBW 2992, an irreversible dual EGFR/HER2 receptor tyrosine kinase inhibitor, in a continuous schedule in patients with advanced solid tumours. Proc. Am. Soc. Clin. Oncol.24(Suppl. 18), 2074 (2006) (Abstract).
   Web of Science ®Google Scholar
• Eskens FA, Mom CH, Planting AS et al. A Phase I dose escalation study of BIBW 2992, an irreversible dual inhibitor of epidermal growth factor receptor 1 (EGFR) and 2 (HER2) tyrosine kinase in a 2-week on, 2-week off schedule in patients with advanced solid tumours. Br. J. Cancer98(1), 80–85 (2008).
   PubMed Web of Science ®Google Scholar
• Miller VA, Hirsh V, Cadranei J et al. Phase IIB/III double-blind randomized trial of afatinib (BIBW 2992, an irreversible inhibitor of EGFR/HER1 and HER2) + best supportive care (BSC) versus placebo in patients with NSCLC failing 1–2 lines of chemotherapy and erlotinib or gefitinib (LUX-LUNG 1). Ann. Oncol.21(Suppl. 8), LBA 1 (2010) (Abstract).
   Google Scholar
• Miller VA, Hirsh V, Cadranei J et al. Subgroup analysis of LUX-Lung 1: a randomized Phase III trial of afatinib (BIBW 2992) + best supportive care (BSC) versus placebo + BSC in patients with NSCLC failing 1–2 lines of chemotherapy and erlotinib or gefitinib. Presented at: 2010 Chicago Multidisciplinary Symposium in Thoracic Oncology. Chicago, IL, USA, 9–11 December 2010.
   Google Scholar
• Yang CH, Shih JY, Su WC et al. A Phase II of afatinib (BIBW 2992) in patients with adenocarcinoma of the lung and activating EGFR mutations. Ann. Oncol.21(Suppl. 8), 367 (2010) (Abstract).
   Google Scholar
• Shih JY, Yu CJ, Su WC et al. Activity of afatinib (BIBW2992) an irreversible EGFR/HER1 and HER2 TKI, in lung adenocarcinoma patients harbouring less common EGFR/HER1 mutations. Ann. Oncol.21(Suppl. 8), 415 (2010) (Abstract).
   PubMedGoogle Scholar
• Jackman D, Pao W, Riely GJ et al. Clinical definition of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer. J. Clin. Oncol.28(2), 357–360 (2010).
   PubMed Web of Science ®Google Scholar
• Riely GJ, Kris MG, Zhao B et al. Prospective assessment of discontinuation and reinitiation of erlotinib or gefitinib in patients with acquired resistance to erlotinib or gefitinib followed by the addition of everolimus. Clin. Cancer Res.13(17), 5150–5155 (2007).
   PubMed Web of Science ®Google Scholar
• Costa DB, Nguyen KS, Cho BC, et al. Effects of erlotinib in EGFR mutated non-small cell lung cancers with resistance to gefitinib. Clin. Cancer Res.14(21), 7060–7067 (2008).
   PubMed Web of Science ®Google Scholar
• Broglio KR, Berry DA. Detecting an overall survival benefit that is derived from progression-free survival. J. Natl Cancer Inst.101(23), 1642–1649 (2009).
   PubMed Web of Science ®Google Scholar
• Kwak EL, Sordella R, Bell DW et al. Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib. Proc. Natl Acad. Sci. USA102(21), 7665–7670 (2005).
   PubMed Web of Science ®Google Scholar
• Asahina H, Yamazaki K, Kinoshita I et al. A Phase II trial of gefitinib as first-line therapy for advanced non-small cell lung cancer with epidermal growth factor receptor mutations. Br. J. Cancer95(8), 998–1004 (2006).
   PubMed Web of Science ®Google Scholar
• Inoue A, Kobayashi K, Usui K et al. First-line gefitinib for patients with advanced non-small-cell lung cancer harboring epidermal growth factor receptor mutations without indication for chemotherapy. J. Clin. Oncol.27(9), 1394–1400 (2009).
   PubMed Web of Science ®Google Scholar
• Inoue A, Suzuki T, Fukuhara T et al. Prospective Phase II study of gefitinib for chemotherapy-naive patients with advanced non-small-cell lung cancer with epidermal growth factor receptor gene mutations. J. Clin. Oncol.24(21), 3340–3346 (2006).
   PubMed Web of Science ®Google Scholar
• Rosell R, Perez-Roca L, Sanchez JJ et al. Customized treatment in non-small-cell lung cancer based on EGFR mutations and BRCA1 mRNA expression. PLoS One4(5), e5133 (2009).
   PubMed Web of Science ®Google Scholar
• Sequist LV, Martins RG, Spigel D et al. First-line gefitinib in patients with advanced non-small-cell lung cancer harboring somatic EGFR mutations. J. Clin. Oncol.26(15), 2442–2449 (2008).
   PubMed Web of Science ®Google Scholar
• Yang CH, Yu CJ, Shih JY et al. Specific EGFR mutations predict treatment outcome of stage IIIB/IV patients with chemotherapy-naive non-small-cell lung cancer receiving first-line gefitinib monotherapy. J. Clin. Oncol.26(16), 2745–2753 (2008).
   PubMed Web of Science ®Google Scholar
• Sugio K, Uramoto H, Onitsuka et al. Prospective Phase II study of gefitinib in non-small cell lung cancer with epidermal growth factor receptor gene mutations. Lung Cancer64(3), 314–318 (2009).
   PubMed Web of Science ®Google Scholar
• Sunaga N, Tomizawa Y, Yanagitani N et al. Phase II prospective study of the efficacy of gefitinib for the treatment of stage III/IV non-small cell lung cancer with EGFR mutations, irrespective of previous chemotherapy. Lung Cancer56(3), 383–389 (2007).
   PubMed Web of Science ®Google Scholar
• Sutani A, Nagai Y, Udagawa K et al. Gefitinib for non-small-cell lung cancer patients with epidermal growth factor receptor gene mutations screened by peptide nucleic acid-locked nucleic acid PCR clamp. Br. J. Cancer95(11), 1483–1489 (2006).
   PubMed Web of Science ®Google Scholar
• Yoshida K, Yatabe Y, Park J et al. Prospective validation for prediction of gefitinib sensitivity by epidermal growth factor receptor gene mutation in patients with non-small cell lung cancer. J. Thorac. Oncol.2(1), 22–28 (2007).
   PubMed Web of Science ®Google Scholar
• Han SW, Kim TY, Hwang PG et al. Predictive and prognostic impact of epidermal growth factor receptor mutation in non small-cell lung cancer patients treated with gefitinib. J. Clin. Oncol.23(11), 2493–2501 (2005).
   PubMed Web of Science ®Google Scholar
• Tamura K, Okamoto I, Kashii T et al. Multicentre prospective Phase II trial of gefitinib for advanced non-small cell lung cancer with epidermal growth factor receptor mutations: results of the West Japan Thoracic Oncology Group trial (WJTOG0403). Br. J. Cancer98(5), 907–914 (2008).
   PubMed Web of Science ®Google Scholar
• Regales L, Gong Y, Shen R et al. Dual targeting of EGFR can overcome a major drug resistance mutation in mouse models of EGFR mutant lung cancer. J. Clin. Invest.119(10), 3000–3010 (2009).
   PubMed Web of Science ®Google Scholar