Beyond EGFR TKI in EGFR-mutant Non-Small Cell Lung Cancer patients: Main challenges still to be overcome

Cancer Treatment Reviews

Volumn 40, Issue 6, 2014, Pages 723-729

  Remon, J ^a   Moran T ^b   Reguart, N ^c   Majem, M ^d   Carcereny, E ^b   Lianes, P ^a  

^a HOSPITAL DE MATARÓ   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c HOSPITAL CLÍNIC   (Spain)

^d HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

Author keywords

EGFR mutant tumors; Non Small Cell Lung Cancer; Sequence of treatment; Tyrosine kinase inhibitors

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR;

CANCER CHEMOTHERAPY; CANCER PATIENT; CLINICAL FEATURE; HUMAN; LUNG NON SMALL CELL CANCER; MUTAGENIC ACTIVITY; PHASE 3 CLINICAL TRIAL (TOPIC); REVIEW; TREATMENT RESPONSE;

EGFR-MUTANT TUMORS; NON-SMALL CELL LUNG CANCER; SEQUENCE OF TREATMENT; TYROSINE KINASE INHIBITORS;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CARCINOMA, NON-SMALL-CELL LUNG; CLINICAL TRIALS, PHASE III AS TOPIC; DISEASE-FREE SURVIVAL; DRUG ADMINISTRATION SCHEDULE; HUMANS; LUNG NEOPLASMS; MOLECULAR TARGETED THERAPY; MUTATION; PROTEIN-TYROSINE KINASES; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84899957391     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2014.03.006     Document Type: Review

References (87)

1. Barlesi F., Blons H., Beau-Faller M., et al. Biomarkers France: results of routine EGFR, HER2, KRAS, BRAF, PI3KCA mutation detection and EML4-ALK gene fusion assessment on the first 10,000 non-small cell lung cancer patients. J Clin Oncol 2013, 31. (Suppl.; abstract 8000).
2. Gahr S., Stoehr R., Geissinger E., et al. EGFR mutational status in a large series of Caucasian European NSCLC patients: data from daily practice. Br J Cancer 2013, 109:1821-1828.
3. Nowak F., Calvo F., Soria J.C. Europe does it better: molecular testing across a National Health Care System - The French Example. Educational Book. Am Soc Clin Oncol Educ Book 2013, 33:332-337.
4. Kris M., Johnson B., Berry L., et al. Treatment with therapies matched to oncogenic drivers improves survival in patients with lung cancers: results from the lung cancer mutation consortium. J Thorac Oncol 2013, 8(Suppl. 2):S3. (PL 03.06).
5. Fukoka M., Wu Y.L., Thongprasert S., et al. Biomarker analyses and final overall survival results from a phase III, randomized, open-label, first-line study of gefitinib versus carboplatin/paclitaxel in clinically selected patients with advanced non-small-cell lung cancer in Asia (IPASS). J Clin Oncol 2011, 29:2866-2874.
6. Han J.Y., Par K., Sim S.W., et al. First-SIGNAL: first-line single-agent iressa versus gemcitabine and cisplatin trial in never-smokers with adenocarcinoma of the lung. J Clin Oncol 2012, 30:1122-1128.
7. Mitsudomi T., Morita S., Yatabe Y., et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harboring mutations of epidermal growth factor receptor (WJTOG 3405): an open label, randomized phase 3 trial. Lancet Oncol 2010, 11:121-128.
8. Mitsudomi T., Morita S., Yatabe Y., et al. Up-dated overall survival results of WJTOG 3405, a randomized phase III trial comparing gefitinib with cisplatin plus docetaxel as the first-line treatment for patients with advanced non-small-cell lung cancer harboring mutations of the epidermal growth factor receptor. J Clin Oncol 2012, 30. (Suppl.; abstract 7521).
9. Inoue A., Kobayashi K., Maemondo M., et al. Updated overall survival results from a randomized phase III trial comparing gefitinib with carboplatin-paclitaxel for chemo-naïve lung cancer with sensitive EGFR gene mutation (NEJ002). Ann Oncol 2013, 24:54-59.
10. Zhou C., Wu Y.L., Chen G., et al. Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicenter, open-label, randomized, phase 3 study. Lancet Oncol 2011, 12:735-742.
11. 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 multicenter, open-label, randomized phase 3 trial. Lancet Oncol 2012, 13:239-246.
12. Solca F., Dahl G., Zoephel A., et al. Target binding properties and cellular activity of afatinib (BIBW2992), an irreversible ErbB family blocker. J Pharmacol Exp Ther 2012, 343:342-350.
13. Sequist L.V., Yang J.C., Yamamoto N., et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutation. J Clin Oncol 2013, 31:3327-3334.
14. Wu Y.L., Zhou C., Hu C.P., et al. Afatinib versus cisplatin plus gemcitabine for first-line treatment of Asian patients with advanced non-small cell lung cancer harboring EGFR mutation (LUX-Lung 6): an open-label, randomized phase 3 trial. Lancet Oncol 2014, 15:213-222.
15. Gao G., Ren S., Li A., et al. Epidermal growth factor receptor-tyrosine kinase inhibitor therapy is effective as first-line treatment of advanced non-small-cell lung cancer with mutated EGFR: a meta-analysis from six phase III randomized controlled trials. Int J Cancer 2012, 131:E822-E829.
16. Lee C.K., Brown C., Gralla R.J., et al. Impact on EGFR inhibitor in non-small cell lung cancer on progression-free and overall survival: a meta-analysis. J Natl Cancer Inst 2013, 105:595-605.
17. Paz-Ares L., Soulières D., Klughammer B., et al. Pooled analysis of clinical outcomes for patients with EGFR mutations in non-small cell lung cancer: an update. Ann Oncol 2012, 23. (Suppl. 9, abstract 1254P).
18. Petrelli F., Borgonovo K., Cabiddu M., et al. Efficacy of EGFR tyrosine kinase inhibitors in patients with EGFR-mutated non-small-cell lung cancer: a meta-analysis of 13 randomized trials. Clin Lung Cancer 2012, 13:107-114.
19. Liang W., Wu X., Fang W., et al. Network meta-analysis of erlotinib, gefitinib, afatinib and icotinib in patients with advanced non-small-cell lung cancer harboring EGFR mutations. PLoS One 2014, 9(2):e85245.
20. Kris M., Mok T., Ignatius S.H., et al. First-line dacomitinib (PF-00299804), an irreversible pan-HER tyrosine kinase inhibitor, for patients with EGFR-mutation lung cancer. J Clin Oncol 2012, 30. (Suppl.; abstract 7530).
21. Yun C.H., Mengwasser K.E., Toms A.V., et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci USA 2008, 105:2070-2075.
22. Su K.Y., Chen H.Y., Li K.-C.H., et al. Pretreatment epidermal growth factor receptor T790M mutation predicts shorter EGFR tyrosine kinase inhibitor response duration in patients with non-small-cell lung cancer. J Clin Oncol 2012, 30:433-440.
23. Riely G.J., Yu H.A., Arcila M.E., et al. Response to erlotinib and prognosis for patients with the novo epidermal growth factor receptor T790M mutations. J Clin Oncol 2013, 31. (Suppl.; abstr. 8018).
24. Yang J.C., Schuler M., Massey D., et al. Activity of afatinib in uncommon epidermal growth factor receptor mutations: findings from three trials of afatinib in EGFR mutation-positive lung cancer. J Thorac Oncol 2013, 8(Suppl. 2):S 141. (O03.05).
25. Rosell R., Molina M.A., Costa C., et al. Pretreatment EGFR T790M mutation and BRCA1 mRNA expression in erlotinib-treated advanced non-small cell lung cancer patients with EGFR mutation. Clin Cancer Res 2011, 17:1160-1168.
26. Costa C., Molina-Vila M.A., Drozdowskyi A., et al. The impact of EGFR T790M mutations and BIM mRNA expression on outcome in patients with EGFR-mutant NSCLC treated with erlotinib or chemotherapy in the randomized phase III EURTAC trial. Clin Cancer Res 2014, (Epub ahead of print).
27. Soria J.C., Sequist L.V., Gadgeel S., et al. First in-human evaluation of CO-1686, an irreversible, highly selective tyrosine kinase inhibitor of mutations of EGFR (activating and T790M). J Thorac Oncol 2013, 8(Suppl. 2):S141-S142. (O03.06).
28. Ranson M., Pao W., Kim D.W., et al. AZD9291: an irreversible, potent and selective tyrosine kinase inhibitor of activating EGFR and resistance T790M mutations in advanced NSCLC. J Thorac Oncol 2013, 8(Suppl. 2):S389. (P1.11-034).
29. Li L., Wang H., Yang E.S., et al. Erlotinib attenuates homologous recombinational repair of chromosomal breaks in human breast cancer cells. Cancer Res 2008, 68:941-946.
30. Garcia-Campelo R., Felip E., Massuti B., et al. Phase IB study of olaparib (AZD2281) plus gefitinib in EGFR-mutant patients with advanced non-small cell lung cancer. J Clin Oncol 2013, 31. (Suppl.; abstract 2581).
31. Gong Y., Somwar R., Politi K., et al. Induction of BIM is essential for apoptosis triggered by EGFR kinase inhibitors in mutant EGFR-dependent lung adenocarcinomas. PLoS Med 2007, 4:e294.
32. Faber A.C., Corcoran R.B., Ebi H., et al. BIM expression in treatment-naïve cancers predicts responsiveness to kinase inhibitors. Cancer Discov 2011, 1:352-365.
33. Ng K.P., Hillmer A.M., Chuah C.T., et al. A common BIM deletion polymorphism mediates intrinsic resistance and inferior response to tyrosine kinase inhibitors in cancer. Nat Med 2012, 18:521-528.
34. Isobe K., Hata Y., Kaburaki K., et al. Clinical significance of BIM deletion polymorphisms in non-small cell lung cancer with epidermal growth factor receptor mutation. J Clin Oncol 2013, 31. (Suppl.; abstract 11052).
35. Lee J.K., Shin J.Y., Kim S., et al. Primary resistance to epidermal growth factor receptor tyrosine kinase inhibitors in patients with non-small-cell lung cancer harboring TKI-sensitive EGFR mutations: an exploratory study. Ann Oncol 2013, 24:2080-2087.
36. Nakagawa T., Takeuchi S., Yamada T., et al. EGFR TKI resistance due to BIM polymorphisms can be circumvented in combination with HDAC inhibition. Cancer Res 2013, 73:2428-2434.
37. Rosell R., Moran T., Queralt C., et al. Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med 2009, 361:958-967.
38. Maemondo M., Inoue A., Kobayashi K., et al. Gefitinib or chemotherapy for non-small cell lung cancer with mutated EGFR. N Engl J Med 2010, 362:2380-2388.
39. Hirsch F.R., Varella-Garcia M., Bunn P.A., et al. Molecular predictors of outcome with gefitinib in a phase III placebo-controlled study in advanced non-small cell lung cancer. J Clin Oncol 2006, 25:5034-5042.
40. Douillard J.Y., Shepherd F.A., Hirsh V., et al. Molecular predictors of outcome with gefitinib and docetaxel in previously treated non-small cell lung cancer: data from the randomized phase III INTEREST trial. J Clin Oncol 2010, 28:744-752.
41. Zhu Ch.-Q., Santos G., Ding K., et al. Role of KRAS and EGFR as biomarker of response to erlotinib in National Cancer Institute of Canada Clinical Trials Group Study BR.21. J Clin Oncol 2008, 10:4268-4275.
42. Sugio K., Uramoto H., Onitsuka T., et al. Prospective phase II study of gefitinib in non-small cell lung cancer with epidermal growth factor receptor gene mutation. Lung Cancer 2009, 64:314-318.
43. Gandara D.R., Grimminger P., Mack P.C., et al. Association of epidermal growth factor receptor activating mutations with low ERCC1 gene expression in non-small cell lung cancer. J Thorac Oncol 2010, 5:1933-1938.
44. Mok T., Wu Y.L., Thongprasert S., et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009, 361:947-957.
45. Chin T.M., Quinlan M.P., Singh A., et al. Reduced erlotinib sensitivity of epidermal growth factor receptor-mutant non-small cell lung cancer following cisplatin exposure: a cell culture model of second-line erlotinib treatment. Clin Cancer Res 2008, 14:6867-6876.
46. Chen Z.Y., Zhong W.Z., Zhang X.C., et al. EGFR mutation heterogeneity and the mixed response to EGFR tyrosine kinase inhibitors of lung adenocarcinoma. Oncologist 2012, 17:978-985.
47. Bai H., Wang Z., Chen K., et al. Influence of chemotherapy on EGFR mutation status among patients with non-small-cell lung cancer. J Clin Oncol 2012, 30:3077-3083.
48. Zhang Y., Sun Y., Wang L., et al. Sequential treatment of tyrosine kinase inhibitors and chemotherapy for EGFR mutated non-small cell lung cancer: a meta-analysis of phase III trials. Oncol Target Ther 2013, 29:1771-1777.
49. Gridelli C., Ciardiello F., Gallo C., et al. First-line erlotinib followed by second-line cisplatin-gemcitabine chemotherapy in advanced non-small-cell lung cancer: the TORCH randomized trial. J Clin Oncol 2012, 30:3002-3011.
50. Morita S., Okamoto I., Kobayashi K., et al. Combined survival analysis of prospective trials of gefitinib for non-small cell lung cancer with EGFR mutations. Clin Cancer Res 2009, 15:4493-4498.
51. Wu Y.L., Fukuoka N., Mok T.S., et al. Tumor response and health-related quality of life in clinically selected patients from Asia with advanced non-small-cell lung cancer treated with first-line gefitinib: post-hoc analyses from the IPASS study. Lung Cancer 2013, 8:280-287.
52. Chen G., Feng J., Zhou C., et al. Quality of life analyses from OPTIMAL (CTONG-0802), a phase III, randomized, open-label study of first-line erlotinib versus chemotherapy in patients with advanced EGFR mutation-positive non-small-cell lung cancer. Ann Oncol 2013, 24:1615-1622.
53. Han J.Y., Park K., Kim S.W., et al. First-SIGNAL? First line single-agent iressa versus gemcitabine and cisplatin trial in never-smokers with adenocarcinoma of the lung. J Clin Oncol 2012, 30:122-128.
54. Oizumi S., Kobayashi K., Inoue A., et al. Quality of life with gefitinib in patients with EGFR-mutated non-small cell lung cancer: quality of life analysis of North East Japan Study Group 002 trial. Oncologist 2012, 17:863-870.
55. Yang J.C., Hirsh V., Schuler M., et al. Symptom control and quality of life in LUX-Lung 3: a phase III study of afatinib or cisplatin/pemetrexed in patients with advanced lung adenocarcinoma with EGFR mutation. J Clin Oncol 2013, 31:3342-3350.
56. Geater S.L., Zhou C., Hu C.H.-P., et al. LUX-Lung 6: patient reported outcome from a randomized open-label, phase III study in first-line advanced NSCLC patients harboring epidermal growth factor receptor mutations. J Clin Oncol 2013, 31. (Suppl.; abstract 8061).
57. 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 mutation without indication for chemotherapy. J Clin Oncol 2009, 27:1394-1400.
58. Hayat M.J., Howlader N., Reichamn M.E., et al. Cancer statistics trends, and multiple primary cancer analyses from the Surveillance, Epidemiology and End Results (SEER) program. Oncologist 2007, 12:20-37.
59. Alam M., Shepherd F.A., Winton T., et al. Compliance with post-operative adjuvant chemotherapy in non-small-cell lung cancer. An analysis of National Cancer Institute of Canada and Intergroup Study JBR.10 and review of the literature. Lung Cancer 2005, 47:385-394.
60. Lüchtenborg M., Jakobsen E., Krasnik M., et al. The effect of comorbidity on stage-specific survival in resected non-small cell lung cancer patients. Eur J Cancer 2012, 48:3386-3395.
61. Maemondo M., Minegishi Y., Inoue A., et al. First-line gefitinib in patients aged 75 or older with advanced non-small cell lung cancer harboring epidermal growth factor receptor mutations: NEJ 003 study. J Thorac Oncol 2012, 7:1417-1422.
62. Hendriks L.E., Smit E.F., Vosse B.A., et al. EGFR mutated non-small cell lung cancer patients: more prone to development of bone and brain metastases?. Lung Cancer 2014, 84:86-91.
63. Heon S., Yeap B.Y., Lindeman N.I., et al. The impact of initial gefitinib or erlotinib versus chemotherapy on central nervous system progression in advanced non-small cell lung cancer with EGFR mutations. Clin Cancer Res 2012, 18:4406-4414.
64. Weber B., Winterdahl M., Memon A., et al. Erlotinib accumulation in brain metastases from non-small cell lung cancer: visualization by positron emission tomography in a patient harboring a mutation in epidermal growth factor receptor. J Thorac Oncol 2011, 6:1287-1289.
65. Park S.J., Kim H.T., Lee D.H., et al. Efficacy of epidermal growth factor receptor tyrosine kinase inhibitors for brain metastasis in non-small cell lung cancer patients harboring either exon 19 or 21 mutation. Lung Cancer 2012, 77:556-560.
66. Porta R., Sánchez-Torres J.M., Paz-Ares L., et al. Brain metastases from lung cancer responding to erlotinib: the importance of EGFR mutation. Eur Respir J 2011, 37:624-631.
67. Moran T., Sequist L.V. Timing of epidermal growth factor receptor tyrosine kinase inhibitor therapy in patients with lung cancer with EGFR mutation. J Clin Oncol 2012, 30:3330-3336.
68. Takeda K., Hida T., Sato T., et al. Randomized phase III trial of platinum-doublet chemotherapy followed by gefitinib compared with continued platinum doublet chemotherapy in Japanese patients with advanced non-small cell lung cancer: results of a West Japan Thoracic Oncology Group Trial (WJTOG0203). J Clin Oncol 2010, 28:753-760.
69. Gaafar R.M., Surmont V.F., Scagliotti G.V., et al. A double blind, randomized, placebo controlled phase III intergroup of gefitinib in patients with advanced NSCLC, non-progressing after first line platinum-based chemotherapy (EORTC 08021/ILCP 01/03). Eur J Cancer 2011, 47:2331-2340.
70. Zhang L., Ma S., Song X., et al. Gefitinib versus placebo as maintenance therapy in patients with locally advanced or metastatic non-small cell lung cancer (INORM; C-TONG 0804): a multicenter, double-blind randomized phase 3 trial. Lancet Oncol 2012, 13:466-475.
71. Brugger W., Triller N., Blasniska-Morawiec M., et al. Prospective molecular marker analysis of EGFR and KRAS from a randomized, placebo-controlled study of erlotinib as maintenance therapy in advanced non-small cell lung cancer. J Clin Oncol 2011, 1:4113-4203.
72. Johnson B.E., Kabbinavar F., Fehrenbacher L., et al. ATLAS: randomized, double-blind, placebo-controlled, phase IIIB trial comparing bevacizumab therapy with or without erlotinib, after completion of chemotherapy, with bevacizumab for first-line treatment of advanced non-small cell lung cancer. J Clin Oncol 2013, 31:3926-3934.
73. Pennell N.A. Integration of EGFR inhibitors and conventional chemotherapy in the treatment of non-small cell lung cancer. Clin Lung Cancer 2011, 12:350-359.
74. Jänne P., Wang X., Socinscki M.A., et al. Randomized phase II trial of erlotinib alone or with carboplatin and paclitaxel in patients who were never or light former smokers with advanced lung adenocarcinoma: CALGB 30406 trial. J Clin Oncol 2012, 30:2063-2069.
75. Davies A.M., Ho Ch., Lara P.N., et al. Pharmacodynamic separation of epidermal growth factor receptor tyrosine kinase inhibitors and chemotherapy in non-small cell lung cancer. Clinical Lung Cancer 2006; 6: 385-8. Gefitinib induces apoptosis in the EGFR-L858 non-small cell lung cancer cell line H3255. Cancer Res 2004, 64:7241-7244.
76. Solit D.B., She Y., Lobo J., et al. Pulsatile administration of the epidermal growth factor receptor inhibitor gefitinib is significantly more effective than continuous dosing for sensitizing tumors to paclitaxel. Clin Cancer Res 2005, 11:1983-1989.
77. Tsai C.M., Chen J.T., Chiu C.H., et al. Combined epidermal growth factor receptor (EGFR)-tyrosine kinase inhibitor and chemotherapy in non-small cell lung cancer: chemo-refractoriness of cells harboring sensitizing-EGFR mutations in the presence of gefitinib. Lung Cancer 2013, 82:305-312.
78. Goldberg S.B., Oxnard G.R., Diugmarthy S., et al. Chemotherapy with erlotinib or chemotherapy alone in advanced non-small cell lung cancer with acquired resistance to EGFR tyrosine kinase inhibitors. Oncologist 2013, 18:1214-1220.
79. Riely G., Rizvi N.A., Kris M.G., et al. Randomized phase II study of pulse erlotinib before or after carboplatin and paclitaxel in current or former smokers with advanced non-small cell lung cancer. J Clin Oncol 2009, 27:264-270.
80. Li T., Ling Y.H., Goldman D., et al. Schedule-dependent cytotoxic synergism of pemetrexed and erlotinib in human non-small cell lung cancer. Clin Cancer Res 2007, 13:3413-3422.
81. Giovanetti E., Lemos C., Tekle C., et al. Molecular mechanisms underlying the synergistic interaction of erlotinib, an epidermal growth factor receptor tyrosine kinase inhibitor, with the multi-targeted antifolate pemetrexed in non-small cell lung cancer. Mol Pharmacol 2008, 73:1290-1300.
82. Lee D.H., Lee J.S., Kim S.W., et al. Three-arm randomized controlled phase 2 study comparing pemetrexed and erlotinib to either pemetrexed or erlotinib alone as second-line treatment for never-smokers with non-squamous non-small cell lung cancer. Eur J Cancer 2013, 49:3111-3121.
83. Li T., Piperdi B., Walsh W.V., et al. Randomized phase II study of pharmacodynamic separation of pemetrexed and erlotinib versus pemetrexed alone in patients with advanced non-small cell lung cancer. J Clin Oncol 2013, 31. (Suppl.; abstract 8097).
84. Aerts J.G., Codrington H., Lankheet N.A.G., et al. A randomized phase II study comparing erlotinib versus erlotinib with alternating chemotherapy in relapsed non-small cell lung cancer patients: the NVALT-10 study. Ann Oncol 2013, 24:2860-2865.
85. Wu Y.L., Lee J.S., Thongprasert S., et al. Intercalated combination of chemotherapy and erlotinib for patients with advanced stage non-small cell lung cancer (FASTACT-2): a randomized, double blind trial. Lancet Oncol 2013, 14:777-786.
86. Hirsch F., Kabbinavar F., Eisen T., et al. A randomized, phase II, biomarker-selected study comparing erlotinib to erlotinib intercalated with chemotherapy in first-line therapy for advanced non-small cell lung cancer. J Clin Oncol 2011, 29:3567-3573.
87. Ouyang P.Y., Su Z., Mao Y.P., et al. Combination of EGFR-TKIs and chemotherapy as first-line therapy for advanced NSCLC: a meta-analysis. PLoS One 2013, 8:e79000.