Biological and clinical features in predicting efficacy of epidermal growth factor receptor tyrosine kinase inhibitors: A systematic review and meta-analysis

Anticancer Research

Volumn 29, Issue 7, 2009, Pages 2691-2701

  Garassino, Marina Chiara ^a   Borgonovo, Karen ^a   Rossi, Antonio ^b   Mancuso, Andrea ^c   Martelli, Olga ^d   Tinazzi, Angelo ^e   Di Cosimo, Serena ^f   La Verde, Nicla ^a   Sburlati, Paola ^a   Bianchi, Celso ^a   Farina, Gabriella ^a   Torri, Valter ^g  

^a FATEBENEFRATELLI HOSPITAL   (Italy)

^b S G MOSCATI HOSPITAL   (Italy)

^c SAN CAMILLO FORLANINI HOSPITAL   (Italy)

^d MOLINETTE HOSPITAL   (Italy)

^e SENDO Foundation   (Italy)

^f HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^g MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

EGFR mutations; Erlotinib; Gefitinib; K ras mutations; Lung cancer; Predictive factors; Smoking habits

Indexed keywords

BIOLOGICAL FACTOR; CARBOPLATIN; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; K RAS PROTEIN; PACLITAXEL; PLACEBO;

CANCER CHEMOTHERAPY; CANCER SURVIVAL; CIGARETTE SMOKING; CLINICAL FEATURE; CLINICAL TRIAL; DATA ANALYSIS; DRUG EFFECT; DRUG EFFICACY; FLUORESCENCE IN SITU HYBRIDIZATION; HAZARD RATIO; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG NON SMALL CELL CANCER; META ANALYSIS; MODEL; PREDICTION; PRIORITY JOURNAL; QUALITY CONTROL; REVIEW; SEX DIFFERENCE; SMOKING; SYSTEMATIC REVIEW;

ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; HUMANS; LUNG NEOPLASMS; MUTATION; PROTEIN KINASE INHIBITORS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 69249161778     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (42)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T and Thun MJ: Cancer Statistics. CA Cancer J Clin 58: 71-96, 2008.
2. Schiller JH, Harrington D and Belani CP: Comparison of four chemotherapy regimens for advanced NSCLC. N Engl J Med 346: 92-98, 2002.
3. Shepherd FA, Dancey J, Ramlau R, Mattson K, Gralla R, O'Rourke M, Levitan N, Gressot L, Vincent M, Burkes R, Coughlin S, Kim Y and Berille J: 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 18: 2095-2103, 2000. (Pubitemid 30324363)
4. Hanna N, Shepherd F, Fossella F, Pereira JR, De Marinis F, von Pawel J, Gatzemeier U, Tsao TC, Pless M, Muller T, Lim HL, Desch C, Szondy K, Gervais R, Shaharyar, Manegold C, Paul S, Paoletti P, Einhorn L and Bunn PA Jr: Randomized phase III trial of pemetrexed versus docetaxel in pts with non-small cell lung cancer previously treated with chemotherapy. J Clin Oncol 122(9): 1589-1597, 2004. (Pubitemid 41079796)
5. Shepherd FA, Rodrigues Pereira J, Ciuleanu T, Tan EH, Hirsh V, Thongprasert S, Campos D, Maoleekoonpiroj S, Smylie M, Martins R, van Kooten M, Dediu M, Findlay B, Tu D, Johnston D, Bezjak A, Clark G, Santabárbara P and Seymour L: Erlotinib in previously treated non-small cell lung cancer. N Engl J Med 353(2): 123-132, 2005. (Pubitemid 41058344)
6. Thatcher N, Chang A, Parikh P, Rodrigues Pereira J, Ciuleanu T, von Pawel J, Thongprasert S, Tan EH, Pemberton K, Archer V and Carroll K: Gefitinib plus best supportive care in previously treated patients with refractory advanced non-small cell lung cancer: results from a randomized, placebo-controlled, multicentre study (Iressa™ Survival Evaluation in Lung Cancer). Lancet 366(9496): 1527-1537, 2005. (Pubitemid 41540110)
7. Kim ES, Hirsh V, Mok T, Socinski MA, Gervais R, Wu YL, Li LY, Watkins CL, Sellers MV, Lowe ES, Sun Y, Liao ML, Osterlind K, Reck M, Armour AA, Shepherd FA, Lippman SM and Douillard JY: Gefitinib versus docetaxel in previously treated non-small cell lung cancer (INTEREST): a randomised phase III trial. Lancet 22;372(9652): 1809-1818, 2008.
8. Maruyama R, Nishiwaki Y, Tamura T, Yamamoto N, Tsuboi M, Nakagawa K, Shinkai T, Negoro S, Imamura F, Eguchi K, Takeda K, Inoue A, Tomii K, Harada M, Masuda N, Jiang H, Itoh Y, Ichinose Y, Saijo N and Fukuoka M: Phase III study, V-15-32, of gefitinib versus docetaxel in previously treated Japanese patients with non-small cell lung cancer. J Clin Oncol 10;26(26): 4244-4252, 2008.
9. Gatzemeier U, Pluzanska A, Szczesna A, Kaukel E, Roubec J, De Rosa F, Milanowski J, Karnicka-Mlodkowski H, Pesek M, Serwatowski P, Ramlau R, Janaskova T, Vansteenkiste J, Strausz J, Manikhas GM and Von Pawel J: Phase III study of erlotinib in combination with cisplatin and gemcitabine in advanced non-small cell lung cancer: the Tarceva™ Lung Cancer Investigation Trial (TALENT). J Clin Oncol 25: 1545-1552, 2007. (Pubitemid 46733081)
10. Herbst RS, Preger D, Hermann R, Fehrenbacher L, Johnson BE, Sandler A, Kris MG, Tran HT, Klein P, Li X, Ramies D, Johnson DH, Miller VA: TRIBUTE Investigator Group et al: TRIBUTE: a phase III trial of erlotinib hydrochloride (OSI-774) combined with carboplatin and paclitaxel chemotherapy in advanced non-small cell lung cancer. J Clin Oncol 23: 5892-5899, 2005. (Pubitemid 46300205)
11. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG, Louis DN, Christiani DC, Settleman J and Haber DA: Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small cell lung cancer to gefitinib. N Engl J Med 350: 2129-2139, 2004. (Pubitemid 38637993)
12. Bell DW, Lynch TJ, Haserlat SM, Harris PL, Okimoto RA, Brannigan BW, Sgroi DC, Muir B, Riemenschneider MJ, Iacona RB, Krebs AD, Johnson DH, Giaccone G, Herbst RS, Manegold C, Fukuoka M, Kris MG, Baselga J, Ochs JS and Haber DA: Epidermal growth factor receptor mutations and gene amplification in non-small cell lung cancer: Molecular analysis of the IDEAL/INTACT gefitinib trials. J Clin Oncol 23: 8081-8092, 2005. (Pubitemid 46657411)
13. Janne PA, Engelman JA and Johnson BE: Epidermal growth factor receptor mutations in non-small cell lung cancer: Implications for treatment and tumor biology. J Clin Oncol 23: 3227-3234, 2005. (Pubitemid 46211347)
14. Kosaka T, Yatabe Y, Endoh H, Kuwano H, Takahashi T and Mitsudomi T: Mutations of the epidermal growth factor receptor gene in lung cancer: Biological and clinical implications. Cancer Res 64: 8919-8923, 2004. (Pubitemid 39665498)
15. Mitsudomi T, Kosaka T, Endoh H, Horio Y, Hida T, Mori S, Hatooka S, Shinoda M, Takahashi T and Yatabe Y: Mutations of the epidermal growth factor receptor gene predict prolonged survival after gefitinib treatment in patients with non-small cell lung cancer with postoperative recurrence. J Clin Oncol 23: 2513-2520, 2005. (Pubitemid 47050841)
16. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, Herman P, Kaye FJ, Lindeman N, Boggon TJ, Naoki K, Sasaki H, Fujii Y, Eck MJ, Sellers WR, Johnson BE and Meyerson M: EGFR mutations in lung cancer: Correlation with clinical response to gefitinib therapy. Science 304: 1497-1500, 2004. (Pubitemid 38720929)
17. Pao W, Miller V, Zakowski M, Doherty J, Politi K, Sarkaria I, Singh B, Heelan R, Rusch V, Fulton L, Mardis E, Kupfer D, Wilson R, Kris M and Varmus H: 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 USA 101: 13306-13311, 2004.
18. Riely GJ, Pao W, Pham D, Li AR, Rizvi N, Venkatraman ES, Zakowski MF, Kris MG, Ladanyi M and Miller VA: Clinical course of patients with non-small cell lung cancer and epidermal growth factor receptor exon 19 and exon 20 mutations treated with gefitinib or erlotinib. Clin Cancer Res 12: 839-844, 2006. (Pubitemid 43259866)
19. Sequist LV, Joshi VA, Janne PA, Muzikansky A, Fidias P, Meyerson M, Haber DA, Kucherlapati R, Johnson BE and Lynch TJ: Response to treatment and survival of patients with non-small cell lung cancer undergoing somatic EGFR mutation testing. Oncologist 12: 90-98, 2007. (Pubitemid 46143506)
20. Tokumo M, Toyooka S, Kiura K, Shigematsu H, Tomii K, Aoe M, Ichimura K, Tsuda T, Yano M, Tsukuda K, Tabata M, Ueoka H, Tanimoto M, Date H, Gazdar AF and Shimizu N: The relationship between epidermal growth factor receptor mutations and clinicopathologic features in non-small cell lung cancers. Clin Cancer Res 11: 1167-1173, 2005. (Pubitemid 40175767)
21. Chou TY, Chiu CH, Li LH, Hsiao CY, Tzen CY, Chang KT, Chen YM, Perng RP, Tsai SF and Tsai CM: Mutation in the tyrosine kinase domain of epidermal growth factor receptor is a predictive and prognostic factor for gefitinib treatment in patients with non-small cell lung cancer. Clin Cancer Res 11: 3750-3757, 2005. (Pubitemid 40685592)
22. Bailey R, Kris M, Wolf M, Kay A, Averbuch S, Askaa J and Janas M: Gefitinib (Iressa, ZD1839) monotherapy for pretreated advanced non-small cell lung cancer in IDEAL 1 and 2: Tumor response is not clinically predictable from tumor EGFR membrane staining alone. Lung Cancer 41: S71 (abstr O-242), 2004.
23. Cappuzzo F, Hirsch FR, Rossi E, Bartolini S, Ceresoli GL, Bemis L, Haney J, Witta S, Danenberg K, Domenichini I, Ludovini V, Magrini E, Gregore V, Doglioni C, Sidoni A, Tonato M, Franklin WA, Crino L, Bunn PA Jr and Varella-Garcia M: Epidermal growth factor receptor gene and protein and gefitinib sensitivity in non-small-cell lung cancer. J Natl Cancer Inst 97: 643-655, 2005. (Pubitemid 40812628)
24. Miller VA, Zakowski M, Riely GJ, Pao W, Ladanyi M, Tsao AS, Sandler A, Herbst R, Kris MG and Johnson DH: EGFR mutation and copy number, EGFR protein expression and KRAS mutation as predictors of outcome with erlotinib in bronchioloalveolar cell carcinoma (BAC): Results of a prospective phase II trial. J Clin Oncol 24: 364s, (abstr 7003), 2006.
25. Parra HS, Cavina R, Latteri F, Zucali PA, Campagnoli E, Morenghi E, Grimaldi GC, Roncalli M and Santoro A: Analysis of epidermal growth factor receptor expression as a predictive factor for response to gefitinib (Iressa, ZD1839) in non-small cell lung cancer. Br J Cancer 91: 208-212, 2004. (Pubitemid 39037060)
26. Perez-Soler R, Chachoua A, Hammond LA, Rowinsky EK, Huberman M, Karp D, Rigas J, Clark GM, Santabárbara P and Bonomi P: Determinants of tumor response and survival with erlotinib in patients with non-small cell lung cancer. J Clin Oncol 22: 3238-3247, 2004. (Pubitemid 41103678)
27. Toschi L, Metro G, Magrini E, Bartolini S, Ligorio C, Finocchiaro G, Pession A, Cancellieri A, Tallini G and Cappuzzo FI: EGFR, HER2, and phospho-Akt are not predictive factors for response to first-line chemotherapy in patients with advanced non-small cell lung cancer (NSCLC). J Clin Oncol 24: 391s (abstr 7111), 2006.
28. Tsao MS, Sakurada A, Cutz JC, Zhu CQ, Kamel-Reid S, Squire J, Lorimer I, Zhang T, Liu N, Daneshmand M, Marrano P, da Cunha Santos G, Lagarde A, Richardson F, Seymour L, Whitehead M, Ding K, Pater J and Shepherd FA: Erlotinib in lung cancer: Molecular and clinical predictors of outcome. N Engl J Med 353: 133-144, 2005. (Pubitemid 41058345)
29. Hirsch FR, Varella-Garcia M, Bunn P, Franklin WA, Dziadziuszko R, Thatcher N, Chang A, Parikh P, Pereira JR, Ciuleanu T, von Pawel J, Watkins C, Flannery A, Ellison G, Donald E, Knight L, Parums D, Botwood N and Holloway B: Molecular predictors of outcome with gefitinib in a phase III placebo-controlled study in advanced non-small cell lung cancer study. J Clin Oncol 31(24): 5034-5042, 2006. (Pubitemid 46631407)
30. Felip E, Rojo F, Reck M, Heller A, Klughammer B, Sala G, Cedres S, Peralta S, Maacke H, Foernzler D, Parera M, Mocks J, Saura C, Gatzemeier U and Baselga J: A phase II pharmacodynamic study of erlotinib in patients with advanced non-small cell lung cancer previously treated with platinum-based chemotherapy. Clin Cancer Res 14(12): 3867-3874, 2008.
31. Hirsch FR, Varella-Garcia M and Bunn PA: Fluorescence in situ hybridization (FISH) subgroup analysis of TRIBUTE, a phase III trial of erlotinib plus carboplatin and paclitaxel in NSCLC. J Clin Oncol 25: 18s (abstr 7570), 2007.
32. Eberhard DA, Johnson BE, Amler LC, Goddard AD, Heldens SL, Herbst RS, Ince WL, Jänne PA, Januario T, Johnson DH, Klein P, Miller VA, Ostland MA, Ramies DA, Sebisanovic D, Stinson JA, Zhang YR, Seshagiri S and Hillan KJ: Mutations in the epidermal growth factor receptor and in KRAS are predictive and prognostic indicators in patients with non-small cell lung cancer treated with chemotherapy alone and in combination with erlotinib. J Clin Oncol 23: 5900-5909, 2005. (Pubitemid 46300206)
33. Shepherd FA, Ding K, Sakurada A, Da Cunha Santos G, Zhu C, Seymour L, Whitehead M, Kamel-Reid S, Squire J and Tsao MSl: Updated molecular analyses of the epidermal growth factor receptor (EGFR) gene and codon 12 and 13 of the k-ras gene in non-small cell lung cancer patients treated with erlotinib in National Cancer Institute. J Clin Oncol 25: 18s (abstr 7571), 2007.
34. Feld R, Sridhar SS, Shepherd, Mackay JA, Evans WK and the Lung Cancer Disease Site Group: Use of the Epidermal Growth Factor Receptor Inhibitors, Gefitinib (Iressa®) and Erlotinib (Tarceva®), in the Treatment of Non-small Cell Lung Cancer: A Clinical Practice Guideline. A Quality Initiative of the Program in Evidence-based Care (PEBC), Cancer Care Ontario (CCO) Evidence-based Series #7-9: Section 1.
35. Begg C, Cho M, Eastwood S, Horton R, Moher D, Olkin I, Pitkin R, Rennie D, Schulz KF, Simel D and Stroup DF: Improving the quality of reporting of randomized controlled trials. The CONSORT statement. JAMA 276: 637-639, 1996.
36. Parmar MK, Torri V and Stewart L: Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med 17(24): 2815-2834, 1998. (Pubitemid 28562978)
37. Higgins JPT and Thompson SG: Quantifying heterogeneity in a meta-analysis. Stat Med 21: 1539-1558, 2002.
38. Tierney J and Tinazzi A: A demonstration and guide to SCHARP, a software application for the analysis and plotting of individual patient data (IPD) meta-analysis. Cochrane 2006 - Dublin, Workshop W43.
39. Sridhar SS, Seymour L and Shepherd FA: Inhibitors of epidermal growth factor receptors: a review of clinical research with a focus on non-small cell lung cancer. Lancet Oncol 4: 397-406, 2003. (Pubitemid 36833681)
40. Blackhall F, Ranson M and Thatcher N: Where next for gefitinib in patients with lung cancer? Lancet Oncol 7: 499-507, 2006.
41. Siegel-Lakhai WS, Beijnen JH and Schellens JHM: Current knowledge and future directions of the selective epidermal growth factor receptor inhibitors erlotinib (Tarceva™) and gefitinib (Iressa™). Oncologist 10: 579-589, 2005.
42. Crinò L, Cappuzzo F, Zatloukal P, Reck M, Pesek M, Thompson JC, Ford HE, Hirsch FR, Varella-Garcia M, Ghiorghiu S, Duffield EL, Armour AA, Speake G and Cullen M: Gefitinib versus vinorelbine in chemotherapy-naive elderly patients with advanced non-small cell lung cancer (INVITE): a randomized, phase II study. J Clin Oncol 26(26): 4253-4260, 2008.