Predictive and prognostic value of early response assessment using 18FDG-PET in advanced non-small cell lung cancer patients treated with erlotinib

Shepherd FA, Rodriguez 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, Seymour L; National Cancer Institute of Canada Clinical Trials Group (2005) Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med 353:123–132CrossRefGoogle Scholar

Mok TS, Wu Y-L, 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 (2009) Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 361:947–957PubMedCrossRefGoogle Scholar

Rosell R, Carcereny E, Gervais R, Vergnenegre A, Massuti B, Felip E, Palmero R, Garcia-Gomez R, Pallares C, Sanchez JM, Porta R, Cobo M, Garrido P, Longo F, Moran T, Insa A, De Marinis F, Corre R, Bover I, Illiano A, Dansin E, de Castro J, Milella M, Reguart N, Altavilla G, Jimenez U, Provencio M, Moreno MA, Terrasa J, Muñoz-Langa J, Valdivia J, Isla D, Domine M, Molinier O, Mazieres J, Baize N, Garcia-Campelo R, Robinet G, Rodriguez-Abreu D, Lopez-Vivanco G, Gebbia V, Ferrera-Delgado L, Bombaron P, Bernabe R, Bearz A, Artal A, Cortesi E, Rolfo C, Sanchez-Ronco M, Drozdowskyj A, Queralt C, de Aguirre I, Ramirez JL, Sanchez JJ, Molina MA, Taron M, Paz-Ares L; Spanish Lung Cancer Group in collaboration with Groupe Français de Pneumo-Cancérologie and Associazione Italiana Oncologia Toracica (2012) 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 13:239–246CrossRefGoogle Scholar

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, Shepherd FA (2005) Erlotinib in lung cancer—molecular and clinical predictors of outcome. N Engl J Med 353:133–144PubMedCrossRefGoogle Scholar

Cappuzzo F, Ciuleanu T, Stelmakh L, Cicenas S, Szczésna A, Juhász E, Esteban E, Molinier O, Brugger W, Melezínek I, Klingelschmitt G, Klughammer B, Giaccone G (2010) SATURN investigators, Erlotinib as maintenance treatment in advanced non-small-cell lung cancer: a multicentre, randomised, placebo-controlled, phase III study. Lancet Oncol 11:521–529PubMedCrossRefGoogle Scholar

Therasse P, Arbuck SG, Esenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG (2000) New guidelines to evaluate the response to treatment in solid tumors. J Natl Cancer Inst 92:205–216PubMedCrossRefGoogle Scholar

Tuma R (2006) Sometimes size doesn’t matter: re-evaluating RECIST and tumor response rate endpoints. J Natl Cancer Inst 98:1272–1274PubMedCrossRefGoogle Scholar

Vansteenkiste J, Fischer BM, Dooms C, Mortensen J (2004) Positron-emission tomography in prognostic and therapeutic assessment of lung cancer: systematic review. Lancet Oncol 5:531–540PubMedCrossRefGoogle Scholar

Weber WA, Petersen V, Schmidt B, Tyndale-Hines L, Link T, Peschel C, Schwaiger M (2003) Positron emission tomography in non-small-cell lung cancer: prediction of response to chemotherapy by quantitative assessment of glucose use. J Clin Oncol 21:2651–2657PubMedCrossRefGoogle Scholar

Lee DH, Kim SK, Lee DH, Lee SY, Park SH, Kim HY, Kang KW, Han JY, Kim HT, Lee JS (2009) Early prediction of response to first-line therapy using integrated 18F-FDG PET/CT for patients with advanced/metastatic non-small cell lung cancer. J Thorac Oncol 4:816–821PubMedCrossRefGoogle Scholar

Stroobants S, Goeminne J, Seegers M, Dimitrijevic S, Dupont P, Nuyts J, Martens M, van den Borne B, Cole P, Sciot R, Dumez H, Silberman S, Mortelmans L, van Oosterom A (2003) 18FDG-Positron emission tomography for the early prediction of response in advanced soft tissue sarcoma treated with imatinib mesylate (Glivec). Eur J Cancer 39:2012–2020PubMedCrossRefGoogle Scholar

Prior JO, Montemurro M, Orcurto MV, Michielin O, Luthi F, Benhattar J, Guillou L, Elsig V, Stupp R, Delaloye AB, Leyvraz S (2009) Early prediction of response to sunitinib after imatinib failure by 18F-fluorodeoxyglucose positron emission tomography in patients with gastrointestinal stromal tumor. J Clin Oncol 27:439–445PubMedCrossRefGoogle Scholar

Walter MA, Benz MR, Hildebrandt IJ, Laing RE, Hartung V, Damoiseaux RD, Bockisch A, Phelps ME, Czernin J, Weber WA (2011) Metabolic imaging allows early prediction of response to vandetinib. J Nucl Med 52:231–240PubMedCrossRefGoogle Scholar

Whiteman EL, Cho H, Birnabaum MJ (2002) Role of Akt/protein kinase B in metabolism. Trends Endocrinol Metab 13:444–451PubMedCrossRefGoogle Scholar

Elstrom RL, Bauer DE, Buzzai M, Karnauskas R, Harris MH, Plas DR, Zhuang H, Cinalli RM, Alavi A, Rudin CM, Thompson CB (2004) Akt stimulates aerobic glycolysis in cancer cells. Cancer Res 64:3892–3899PubMedCrossRefGoogle Scholar

Su H, Bodenstein C, Dumont RA, Seimbille Y, Dubinett S, Phelps ME, Herschman H, Czernin J, Weber W (2006) Monitoring tumor glucose utilization by positron emission tomography for the prediction of treatment response to epidermal growth factor receptor kinase inhibitors. Clin Cancer Res 12:5659–5667PubMedCrossRefGoogle Scholar

Sunaga N, Oriuchi N, Kaira K, Yanagitani N, Tomizawa Y, Hisada T, Ishizuka T, Endo K, Mori M (2008) Usefulness of FDG-PET for early prediction of the response to gefitinib in non-small cell lung cancer. Lung Cancer 59:203–210PubMedCrossRefGoogle Scholar

Erlotinib. http://www.roche.com/products/productdetails.htm

Young H, Baum R, Cremerius U, Herholz K, Hoekstra O, Lammertsma AA, Pruim J, Price P (1999) Measurement of clinical and subclinical tumour response using [18F]-fluorodeoxyglucose and positron emission tomography: review and 1999 EORTC recommendations. European organization for research and treatment of cancer (EORTC) PET study group. Eur J Cancer 35:1773–1782PubMedCrossRefGoogle Scholar

Tiseo M, Rossi G, Capelletti M, Sartori G, Spiritelli E, Marchioni A, Bozzetti C, De Palma G, Lagrasta C, Campanini N, Camisa R, Boni L, Franciosi V, Rindi G, Ardizzoni A (2010) Predictors of gefitinib outcomes in advanced non-small cell lung cancer (NSCLC): study of comprehensive panel of molecular markers. Lung Cancer 67:355–360PubMedCrossRefGoogle Scholar

Cavazzoni A, Petronini PG, Galetti M, Roz L, Andriani F, Carbognani P, Rusca M, Fumarola C, Alfieri R, Sozzi G (2004) Dose-dependent effect of FHIT inducible expression in calu-1 lung cancer cell line. Oncogene 23:8439–8446PubMedCrossRefGoogle Scholar

Fumarola C, La Monica S, Alfieri RR, Borra E, Guidotti GG (2005) Cell size reduction induced by inhibition of the mTOR/S6 K-signaling pathway protects Jurkat cells from apoptosis. Cell Death Differ 12:1344–1357PubMedCrossRefGoogle Scholar

Cavazzoni A, Galetti M, Fumarola C, Alfieri RR, Roz L, Andriani F, Carbognani P, Rusca M, Sozzi G, Petronini PG (2007) Effect of inducible FHIT and p53 expression in the Calu-1 lung cancer cell line. Cancer Lett 246:69–81PubMedCrossRefGoogle Scholar

Younes M, Brown RW, Stephenson M, Gondo M, Cagle PT (1997) Overexpression of Glut1 and Glut3 in stage I nonsmall cell lung carcinoma is associated with poor survival. Cancer 80:1046–1051PubMedCrossRefGoogle Scholar

Herrmann K, Benz MR, Krause BJ, Pomykala KL, Buck AK, Czernin J (2011) (18)F-FDG-PET/CT in evaluating response to therapy in solid tumors: where we are and where we can go. Q J Nucl Med Mol Imaging 55:620–632PubMedGoogle Scholar

Zander T, Scheffler M, Nogova L, Kobe C, Engel-Riedel W, Hellmich M, Papachristou I, Toepelt K, Draube A, Heukamp L, Buettner R, Ko YD, Ullrich RT, Smit E, Boellaard R, Lammertsma AA, Hallek M, Jacobs AH, Schlesinger A, Schulte K, Querings S, Stoelben E, Neumaier B, Thomas RK, Dietlein M, Wolf J (2011) Early prediction of nonprogression in advanced non–small-cell lung cancer treated with erlotinib by using [18F]Fluorodeoxyglucose and [18F]Fluorothymidine positron emission tomography. J Clin Oncol 29:1701–1708PubMedCrossRefGoogle Scholar

Mileshkin L, Hicks RJ, Hughes BG, Mitchell PL, Charu V, Gitlitz BJ, Macfarlane D, Solomon B, Amler LC, Yu W, Pirzkall A, Fine BM (2011) Changes in FDG- and FLT-PET imaging in patients with non-small cell lung cancer treated with erlotinib. Clin Cancer Res 17:3304–3315PubMedCrossRefGoogle Scholar

Benz MR, Herrmann K, Walter F, Garon EB, Reckamp KL, Figlin R, Phelps ME, Weber WA, Czernin J, Allen-Auerbach MS (2011) [18]F-FDG PET/CT for monitoring treatment responses to the epidermal growth factor receptor inhibitor erlotinib. J Nucl Med 52:1684–1689PubMedCrossRefGoogle Scholar

Takahashi R, Hirata H, Tachibana I, Shimosegawa E, Inoue A, Nagatomo I, Takeda Y, Kida H, Goya S, Kijima T, Yoshida M, Kumagai T, Kumanogoh A, Okumura M, Hatazawa J, Kawase I (2012) Early [18F]fluorodeoxyglucose positron emission tomography at 2 days of gefitinib treatment predicts clinical outcome in patients with adenocarcinoma of the lung. Clin Cancer Res 18:220–228PubMedCrossRefGoogle Scholar

O’Brien ME, Myerson JS, Coward JI, Puglisi M, Trani L, Wotherspoon A, Sharma B, Cook G, Ashley S, Gunapala R, Chua S, Popat S (2012) A phase II study of 18F-fluorodeoxyglucose PET-CT in non-small cell lung cancer patients receiving erlotinib (Tarceva); objective and symptomatic responses at 6 and 12 weeks. Eur J Cancer 48:68–74PubMedCrossRefGoogle Scholar

Bengtsson T, Hicks RJ, Peterson A, Port RE (2012) 18F-FDG PET as a surrogate biomarker in non-small cell lung cancer treated with erlotinib: newly identified lesions are more informative than standardized uptake value. J Nucl Med 53:530–537PubMedCrossRefGoogle Scholar

Everitt S, Plumridge N, Herschtal A, Bressel M, Ball D, Callahan J, Kron T, Schneider-Kolsky M, Binns D, Hicks RJ, Mac Manus M (2013) The impact of time between staging PET/CT and definitive chemo-radiation on target volumes and survival in patients with non-small cell lung cancer. Radiother Oncol 106:288–291PubMedCrossRefGoogle Scholar

Chan CH, Li CF, Yang WL, Gao Y, Lee SW, Feng Z, Huang HY, Tsai KK, Flores LG, Shao Y, Hazle JD, Yu D, Wei W, Sarbassov D, Hung MC, Nakayama KI, Lin HK (2012) The Skp2-SCF E3 ligase regulates Akt ubiquitination, glycolysis, herceptin sensitivity, and tumorigenesis. Cell 149:1098–1111PubMedCentralPubMedCrossRefGoogle Scholar

Robey RB, Hay N (2009) Is Akt the “Warburg kinase”? Akt-energy metabolism interactions and oncogenesis. Semin Cancer Biol 19:25–31PubMedCentralPubMedCrossRefGoogle Scholar