EGFR Mutations, Gene Amplification, and Protein Expression and KRAS Mutations in Primary and Metastatic Tumors of Nonsmall Cell Lung Cancers and Their Clinical Implications: A Meta-Analysis

REFERENCES

• Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics 2009. CA Cancer J Clin 2009;59(4):225–249.
   PubMed Web of Science ®Google Scholar
• Marsit CJ, Hasegawa M, Hirao T, Kim DH, Aldape K, Hinds PW, Wiencke JK, Nelson HH, Kelsey KT. Loss of heterozygosity of chromosome 3p21 is associated with mutant TP53 and better patient survival in nonsmall-cell lung cancer. Cancer Res 2004;64(23):8702–8707.
   PubMed Web of Science ®Google Scholar
• Garnis C, Lockwood WW, Vucic E, Ge Y, Girard L, Minna JD, Gazdar AF, Lam S, MacAulay C, Lam WL. High resolution analysis of nonsmall cell lung cancer cell lines by whole genome tiling path array CGH. Int J Cancer 2006;118(6):1556–1564.
   PubMed Web of Science ®Google Scholar
• Mounawar M, Mukeria A, Le Calvez F, Hung RJ, Renard H, Cortot A, Bollart C, Zaridze D, Brennan P, Boffetta P, Brambilla E, Hainaut P. Patterns of EGFR, HER2, TP53, and KRAS mutations of p14arf expression in non-small cell lung cancers in relation to smoking history. Cancer Res 2007;67(12):5667–5672.
   PubMed Web of Science ®Google Scholar
• Mok TS, Wu YL, Thongprasert S, Yang CH, Chu DT, Saijo N, Sunpaweravong P, Han B, Margono B, Ichinose Y, Nishiwaki Y, Ohe Y, Yang JJ, Chewaskulyong B, Jiang H, Duffield EL, Watkins CL, Armour AA, Fukuoka M. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009;361(10):947–957.
   PubMed Web of Science ®Google Scholar
• 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, Douillard JY. Gefitinib versus docetaxel in previously treated non-small-cell lung cancer (INTEREST): a randomised phase III trial. Lancet 2008;372(9652):1809–1818.
   PubMed Web of Science ®Google Scholar
• Mok TS, Wu YL, Thongprasert S, Yang CH, Chu DT, Saijo N, Sunpaweravong P, Han B, Margono B, Ichinose Y, Nishiwaki Y, Ohe Y, Yang JJ, Chewaskulyong B, Jiang H, Duffield EL, Watkins CL, Armour AA, Fukuoka M. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009;361(10):947–957.
   PubMed Web of Science ®Google Scholar
• Maemondo M, Inoue A, Kobayashi K, Sugawara S, Oizumi S, Isobe H, Gemma A, Harada M, Yoshizawa H, Kinoshita I, Fujita Y, Okinaga S, Hirano H, Yoshimori K, Harada T, Ogura T, Ando M, Miyazawa H, Tanaka T, Saijo Y, Hagiwara K, Morita S, Nukiwa T; North-East Japan Study Group. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med 2010;362(25):2380–2388.
   PubMed Web of Science ®Google Scholar
• Hirsch FR, Varella-Garcia M, McCoy J, West H, Xavier AC, Gumerlock P, Bunn PA Jr, Franklin WA, Crowley J, Gandara DR. Increased epidermal growth factor receptor gene copy number detected by fluorescence in situ hybridization associates with increased sensitivity to gefitinib in patients with bronchioloalveolar carcinoma subtypes: a Southwest Oncology Group Study. J Clin Oncol 2005;23(28):6838–6845.
   PubMed Web of Science ®Google Scholar
• Dacic S, Flanagan M, Cieply K, Ramalingam S, Luketich J, Belani C, Yousem SA. Significance of EGFR protein expression and gene amplification in non-small cell lung carcinoma. Am J Clin Pathol 2006;125(6):860–865.
   PubMed Web of Science ®Google Scholar
• Dziadziuszko R, Witta SE, Cappuzzo F, Park S, Tanaka K, Danenberg PV, Baron AE, Crino L, Franklin WA, Bunn PA Jr, Varella-Garcia M, Danenberg KD, Hirsch FR. Epidermal growth factor receptor messenger RNA expression, gene dosage, and gefitinib sensitivity in nonsmall cell lung cancer. Clin Cancer Res 2006;12(10):3078–3084.
   PubMed Web of Science ®Google Scholar
• Pirker R, Pereira JR, Szczesna A, von Pawel J, Krzakowski M, Ramlau R, Vynnychenko I, Park K, Yu CT, Ganul V, Roh JK, Bajetta E, O'Byrne K, de Marinis F, Eberhardt W, Goddemeier T, Emig M, Gatzemeier U. Cetuximab plus chemotherapy in patients with advanced non-small-cell lung cancer (FLEX): an open-label randomised phase III trial. Lancet 2009;373(9674):1525–1531.
   PubMed Web of Science ®Google Scholar
• Khambata-Ford S, Harbison CT, Hart LL, Awad M, Xu LA, Horak CE, Dakhil S, Hermann RC, Lynch TJ, Weber MR. Analysis of potential predictive markers of cetuximab benefit in BMS099, a phase III study of cetuximab and first-line taxane/carboplatin in advanced non-small-cell lung cancer. J Clin Oncol 2010;28(6):918–927.
   PubMed Web of Science ®Google Scholar
• Riely GJ, Marks J, Pao W. KRAS mutations in non-small cell lung cancer. Proc Am Thorac Soc 2009;6(2):201–205.
   PubMedGoogle Scholar
• Uramoto H, Mitsudomi T. Which biomarker predicts benefit from EGFR-TKI treatment for patients with lung cancer? Br J Cancer 2007;96(6):857–863.
   PubMed Web of Science ®Google Scholar
• Massarelli E, Varella-Garcia M, Tang X, Xavier AC, Ozburn NC, Liu DD, Bekele BN, Herbst RS, Wistuba II. KRAS mutation is an important predictor of resistance to therapy with epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer. Clin Cancer Res 2007;13(10):2890–2896.
   PubMed Web of Science ®Google Scholar
• Linardou H, Dahabreh IJ, Kanaloupiti D, Siannis F, Bafaloukos D, Kosmidis P, Papadimitriou CA, Murray S. Assessment of somatic k-RAS mutations as a mechanism associated with resistance to EGFR-targeted agents: a systematic review and meta-analysis of studies in advanced non-small-cell lung cancer and metastatic colorectal cancer. Lancet Oncol 2008;9(10):962–972.
   PubMed Web of Science ®Google Scholar
• Paez JG, Jänne 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, Meyerson M. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004;304(5676):1497–1500.
   PubMed Web of Science ®Google Scholar
• Spremulli EN, Dexter DL. Human tumor cell heterogeneity and metastasis. J Clin Oncol 1983;1(8):496–509.
   PubMed Web of Science ®Google Scholar
• Daniele L, Cassoni P, Bacillo E, Cappia S, Righi L, Volante M, Tondat F, Inghirami G, Sapino A, Scagliotti GV, Papotti M, Novello S. Epidermal growth factor receptor gene in primary tumor and metastatic sites from non-small cell lung cancer. J Thorac Oncol 2009;4(6):684–688.
   PubMed Web of Science ®Google Scholar
• Gomez-Roca C, Raynaud CM, Penault-Llorca F, Mercier O, Commo F, Morat L, Sabatier L, Dartevelle P, Taranchon E, Besse B, Validire P, Italiano A, Soria JC. Differential expression of biomarkers in primary non-small cell lung cancer and metastatic sites. J Thorac Oncol 2009;4(10):1212–1220.
   PubMed Web of Science ®Google Scholar
• Cortot AB, Italiano A, Burel-Vandenbos F, Martel-Planche G, Hainaut P. KRAS mutation status in primary nonsmall cell lung cancer and matched metastases. Cancer 2010;116(11):2682–2687.
   PubMed Web of Science ®Google Scholar
• Gow CH, Chang YL, Hsu YC, Tsai MF, Wu CT, Yu CJ, Yang CH, Lee YC, Yang PC, Shih JY. Comparison of epidermal growth factor receptor mutations between primary and corresponding metastatic tumors in tyrosine kinase inhibitor-naive non-small-cell lung cancer. Ann Oncol 2009;20(4):696–702.
   PubMed Web of Science ®Google Scholar
• Kalikaki A, Koutsopoulos A, Trypaki M, Souglakos J, Stathopoulos E, Georgoulias V, Mavroudis D, Voutsina A. Comparison of EGFR and K-RAS gene status between primary tumours and corresponding metastases in NSCLC. Br J Cancer 2008;99(6):923–929.
   PubMed Web of Science ®Google Scholar
• Matsumoto S, Takahashi K, Iwakawa R, Matsuno Y, Nakanishi Y, Kohno T, Shimizu E, Yokota J. Frequent EGFR mutations in brain metastases of lung adenocarcinoma. Int J Cancer 2006;119(6):1491–1494.
   PubMed Web of Science ®Google Scholar
• Park S, Holmes-Tisch AJ, Cho EY, Shim YM, Kim J, Kim HS, Lee J, Park YH, Ahn JS, Park K, Jänne PA, Ahn MJ. Discordance of molecular biomarkers associated with epidermal growth factor receptor pathway between primary tumors and lymph node metastasis in non-small cell lung cancer. J Thorac Oncol 2009;4(7):809–815.
   PubMed Web of Science ®Google Scholar
• Schmid K, Oehl N, Wrba F, Pirker R, Pirker C, Filipits M. EGFR/KRAS/BRAF mutations in primary lung adenocarcinomas and corresponding locoregional lymph node metastases. Clin Cancer Res 2009;15(14):4554–4560.
   PubMed Web of Science ®Google Scholar
• Badalian G, Barbai T, Rásó E, Derecskei K, Szendrôi M, Tímár J. Phenotype of bone metastases of non-small cell lung cancer: epidermal growth factor receptor expression and K-RAS mutational status. Pathol Oncol Res 2007;13(2):99–104.
   PubMed Web of Science ®Google Scholar
• Monaco SE, Nikiforova MN, Cieply K, Teot LA, Khalbuss WE, Dacic S. A comparison of EGFR and KRAS status in primary lung carcinoma and matched metastases. Hum Pathol 2010;41(1):94–102.
   PubMed Web of Science ®Google Scholar
• Italiano A, Vandenbos FB, Otto J, Mouroux J, Fontaine D, Marcy PY, Cardot N, Thyss A, Pedeutour F. Comparison of the epidermal growth factor receptor gene and protein in primary non-small-cell-lung cancer and metastatic sites: implications for treatment with EGFR-inhibitors. Ann Oncol 2006;17(6):981–985.
   PubMed Web of Science ®Google Scholar
• Rao C, Hu Q, Ma J, Li J, Zhang C, Shen L, Wei Q. Comparison of the epidermal growth factor receptor protein expression between primary non-small cell lung cancer and paired lymph node metastases: implications for targeted nuclide radiotherapy. J Exp Clin Cancer Res 2010;29:1–7.
   PubMedGoogle Scholar
• Watzka SB, Rauscher-Pötsch I, Nierlich P, Setinek U, Köstler WJ, Pötschger U, Müller MR, Attems J. Concordance between epidermal growth factor receptor status in primary non-small-cell lung cancer and metastases: a post-mortem study. Eur J Cardiothorac Surg 2010;38(1):34–37.
   PubMed Web of Science ®Google Scholar
• Bozzetti C, Tiseo M, Lagrasta C, Nizzoli R, Guazzi A, Leonardi F, Gasparro D, Spiritelli E, Rusca M, Carbognani P, Majori M, Franciosi V, Rindi G, Ardizzoni A. Comparison between epidermal growth factor receptor (EGFR) gene expression in primary non-small cell lung cancer (NSCLC) and in fine-needle aspirates from distant metastatic sites. J Thorac Oncol 2008;3(1):18–22.
   PubMed Web of Science ®Google Scholar
• Li S, Rosell R, Urban A, Font A, Ariza A, Armengol P, Abad A, Navas JJ, Monzo M. K-ras gene point mutation: a stable tumor marker in non-small cell lung carcinoma. Lung Cancer 1994;11:19–27.
   PubMed Web of Science ®Google Scholar
• Gallegos Ruiz MI, van Cruijsen H, Smit EF, Grünberg K, Meijer GA, Rodriguez JA, Ylstra B, Giaccone G. Genetic heterogeneity in patients with multiple neoplastic lung lesions: a report of three cases. J Thorac Oncol 2007;2(1):12–21.
   PubMed Web of Science ®Google Scholar
• Rao UN, Jones MW, Finkelstein SD. Genotypic analysis of primary and metastatic cutaneous melanoma. Cancer Genet Cytogenet 2003;140:37–44.
   PubMed Web of Science ®Google Scholar
• Takahashi K, Kohno T, Matsumoto S, Nakanishi Y, Arai Y, Fujiwara T, Tanaka N, Yokota J. Clonality and heterogeneity of pulmonary blastoma from the viewpoint of genetic alterations: a case report. Lung Cancer 2007;57(1):103–108.
   PubMed Web of Science ®Google Scholar
• Kuukasjärvi T, Karhu R, Tanner M, Kähkönen M, Schäffer A, Nupponen N, Pennanen S, Kallioniemi A, Kallioniemi OP, Isola J. Genetic heterogeneity and clonal evolution underlying development of asynchronous metastasis in human breast cancer. Cancer Res 1997;57(8):1597–1604.
   PubMed Web of Science ®Google Scholar
• Tórtola S, Steinert R, Hantschick M, Peinado MA, Gastinger I, Stosiek P, Lippert H, Schlegel W, Reymond MA. Discordance between K-ras mutations in bone marrow micrometastases and the primary tumor in colorectal cancer. J Clin Oncol 2001;19(11):2837–2843.
   PubMed Web of Science ®Google Scholar
• Racila E, Euhus D, Weiss AJ, Rao C, McConnell J, Terstappen LW, Uhr JW. Detection and characterization of carcinoma cells in the blood. Proc Natl Acad Sci U S A 1998;95(8):4589–4594.
   PubMed Web of Science ®Google Scholar
• Hayes DF, Walker TM, Singh B, Vitetta ES, Uhr JW, Gross S, Rao C, Doyle GV, Terstappen LW. Monitoring expression of HER-2 on circulating epithelial cells in patients with advanced breast cancer. Int J Oncol 2002;21(5):1111–1117.
   PubMed Web of Science ®Google Scholar
• Cappuzzo F, Hirsch FR, Rossi E, Bartolini S, Ceresoli GL, Bemis L, Haney J, Witta S, Danenberg K, Domenichini I, Ludovini V, Magrini E, Gregorc V, Doglioni C, Sidoni A, Tonato M, Franklin WA, Crino L, Bunn PA Jr, Varella-Garcia M. Epidermal growth factor receptor gene and protein and gefitinib sensitivity in non-small-cell lung cancer. J Natl Cancer Inst 2005;97(9):643–655.
   PubMed Web of Science ®Google Scholar
• Takano T, Ohe Y, Sakamoto H, Tsuta K, Matsuno Y, Tateishi U, Yamamoto S, Nokihara H, Yamamoto N, Sekine I, Kunitoh H, Shibata T, Sakiyama T, Yoshida T, Tamura T. Epidermal growth factor receptor gene mutations and increased copy numbers predict gefitinib sensitivity in patients with recurrent non-small-cell lung cancer. J Clin Oncol 2005;23:6829–6837.
   PubMed Web of Science ®Google Scholar
• Pinter F, Papay J, Almasi A, Sapi Z, Szabo E, Kanya M, Tamasi A, Jori B, Varkondi E, Moldvay J, Szondy K, Keri G, Dominici M, Conte P, Eckhardt S, Kopper L, Schwab R, Petak I. Epidermal growth factor receptor (EGFR) high gene copy number and activating mutations in lung adenocarcinomas are not consistently accompanied by positivity for EGFR protein by standard immunohistochemistry. J Mol Diagn 2008;10:160–168.
   PubMed Web of Science ®Google Scholar
• Lee SY, Kim MJ, Jin G, Yoo SS, Park JY, Choi JE, Jeon HS, Cho S, Lee EB, Cha SI, Park TI, Kim CH, Jung TH, Park JY. Somatic mutations in epidermal growth factor receptor signaling pathway genes in non-small cell lung cancers. J Thorac Oncol 2010;5(11):1734–1740.
   PubMed Web of Science ®Google Scholar