Critical evaluation of disease stabilization as a measure of activity of systemic therapy: Lessons from trials with arms in which patients do not receive active treatment

Journal of Clinical Oncology

Volumn 32, Issue 3, 2014, Pages 260-263

  Le Tourneau, Christophe ^a   Paoletti, Xavier ^a   Coquan, Elodie ^b   Sablin, Marie Paule ^b   Zoubir, Mustapha ^b   Tannock, Ian F ^c  

^a INSERM   (France)

^b INSTITUT CURIE   (France)

^c PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; PLACEBO;

CANCER CHEMOTHERAPY; CANCER CONTROL; CANCER GROWTH; CANCER SIZE; CANCER SURVIVAL; CLINICAL EVALUATION; CLINICAL EXAMINATION; COMPUTER ASSISTED TOMOGRAPHY; DISEASE COURSE; GROWTH RATE; HUMAN; LETTER; MEASUREMENT ERROR; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RANDOM ERROR; RANDOMIZED CONTROLLED TRIAL (TOPIC); SOLID TUMOR; SYSTEMIC THERAPY; TIME TO TREATMENT; UNCERTAINTY; CLINICAL TRIAL (TOPIC); DISEASE FREE SURVIVAL; EPIDEMIOLOGY; METHODOLOGY; NEOPLASM; TREATMENT OUTCOME;

ANTINEOPLASTIC AGENTS; CLINICAL TRIALS AS TOPIC; CONFOUNDING FACTORS (EPIDEMIOLOGY); DISEASE PROGRESSION; DISEASE-FREE SURVIVAL; HUMANS; NEOPLASMS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RESEARCH DESIGN; TREATMENT OUTCOME;

EID: 84897018980     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2013.53.5518     Document Type: Letter

References (75)

1. Italiano A, Massard C, Bahleda R, et al: Treatment outcome and survival in participants of phase I oncology trials carried out from 2003 to 2006 at Institut Gustave Roussy. Ann Oncol 19:787-792, 2008 (Pubitemid 351467383)
2. Reference deleted
3. Tannock I, Hill R, Bristow R, et al: The Basic Science of Oncology (ed 4). New York, NY, McGraw-Hill Professional, 2004, pp 181-189
4. Thiesse P, Ollivier L, Di Stefano-Louineau D, et al: Response rate accuracy in oncology trials: Reasons for interobserver variability - Groupe Francais d'Immunothérapie of the Fédération Nationale des Centres de Lutte Contre le Cancer. J Clin Oncol 15:3507-3514, 1997
5. Schwartz LH, Mazumdar M, Brown W, et al: Variability in response assessment in solid tumors: Effect of number of lesions chosen for measurement. Clin Cancer Res 9:4318-1323, 2003
6. Bedikian AY, Millward M, Pehamberger H, et al: Bcl-2 antisense (oblimersen sodium) plus dacarbazine in patients with advanced melanoma: The Oblimersen Melanoma Study Group. J Clin Oncol 24:4738-4745, 2006 (Pubitemid 46630937)
7. Kay R, Wu J, Wittes J: On assessing the presence of evaluation-time bias in progression-free survival in randomized trials. Pharm Stat 10:213-217, 2011
8. Selawry O, Krant M, Scotto J, et al: Methotrexate compared with placebo in lung cancer. Cancer 40:4-8, 1977 (Pubitemid 8160494)
9. Ganz PA, Figlin RA, Haskell CM, et al: Supportive care versus supportive care and combination chemotherapy in metastatic non-small cell lung cancer: Does chemotherapy make a difference? Cancer 63:1271-1278, 1989 (Pubitemid 19084544)
10. Woods RL, Williams CJ, Levi J, et al: A randomised trial of cisplatin and vindesine versus supportive care only in advanced non-small cell lung cancer. Br J Cancer 61:608-611, 1990 (Pubitemid 20126344)
11. Cellerino R, Tummarello D, Guidi F, et al: A randomized trial of alternating chemotherapy versus best supportive care in advanced non-small-cell lung cancer. J Clin Oncol 9:1453-1461, 1991
12. Cullen MH, Billingham LJ, Woodroffe CM, et al: Mitomycin, ifosfamide, and cisplatin in unresectable non-small-cell lung cancer: Effects on survival and quality of life. J Clin Oncol 17:3188-3194, 1999 (Pubitemid 29470650)
13. Helsing M, Bergman B, Thaning L, et al: Quality of life and survival in patients with advanced non-small cell lung cancer receiving supportive care plus chemotherapy with carboplatin and etoposide or supportive care only: A multicentre randomised phase III trial - Joint Lung Cancer Study Group. Eur J Cancer 34:1036-1044, 1998 (Pubitemid 28308344)
14. Anderson H, Hopwood P, Stephens RJ, et al: Gemcitabine plus best supportive care (BSC) vs BSC in inoperable non-small cell lung cancer: a randomized trial with quality of life as the primary outcome - UK NSCLC Gemcitabine Group: Non-Small Cell Lung Cancer. Br J Cancer 83:447-453, 2000 (Pubitemid 30487855)
15. Shepherd FA, Dancey J, Ramlau R, et al: 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)
16. Ranson M, Davidson N, Nicolson M, et al: Randomized trial of paclitaxel plus supportive care versus supportive care for patients with advanced non-small-cell lung cancer. J Natl Cancer Inst 92:1074-1080, 2000 (Pubitemid 30616481)
17. Roszkowski K, Pluzanska A, Krzakowski M, et al: A multicenter, randomized, phase III study of docetaxel plus best supportive care versus best supportive care in chemotherapy-naive patients with metastatic or non-resectable localized non-small cell lung cancer (NSCLC). Lung Cancer 27:145-157, 2000 (Pubitemid 30105654)
18. The Elderly Lung Cancer Vinorelbine Italian Study Group: Effects of vinorelbine on quality of life and survival of elderly patients with advanced non-small-cell lung cancer: The Elderly Lung Cancer Vinorelbine Italian Study Group. J Natl Cancer Inst 91:66-72, 1999
19. Shepherd FA, Rodrigues Pereira J, Ciuleanu T, et al: Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med 353:123-132, 2005 (Pubitemid 41058344)
20. Thatcher N, Chang A, Parikh P, et al: Gefitinib plus best supportive care in previously treated patients with refractory advanced non-small-cell lung cancer: Results from a randomised, placebo-controlled, multicentre study (Iressa Survival Evaluation in Lung Cancer). Lancet 366:1527-1537, 2005 (Pubitemid 41540110)
21. Parikh PM, Vaid A, Advani SH, et al: Randomized, double-blind, placebo-controlled phase II study of single-agent oral talactoferrin in patients with locally advanced or metastatic non-small-cell lung cancer that progressed after chemotherapy. J Clin Oncol 29:4129-4136, 2011
22. Goss G, Ferry D, Wierzbicki R, et al: Randomized phase II study of gefitinib compared with placebo in chemotherapy-naive patients with advanced non-small-cell lung cancer and poor performance status. J Clin Oncol 27:2253-2260, 2009
23. Lee SM, Khan I, Upadhyay S, et al: First-line erlotinib in patients with advanced non-small-cell lung cancer unsuitable for chemotherapy (TOPICAL): A double-blind, placebo-controlled, phase 3 trial. Lancet Oncol 13:1161-1170, 2012
24. Lee JS, Hirsh V, Park K, et al: Vandetanib Versus placebo in patients with advanced non-small-cell lung cancer after prior therapy with an epidermal growth factor receptor tyrosine kinase inhibitor: A randomized, double-blind phase III trial (ZEPHYR). J Clin Oncol 30:1114-1121, 2012
25. Miller VA, Hirsh V, Cadranel J, et al: Afatinib versus placebo for patients with advanced, metastatic non-small-cell lung cancer after failure of erlotinib, gefitinib, or both, and one or two lines of chemotherapy (LUX-Lung 1): A phase 2b/3 randomised trial. Lancet Oncol 13:528-538, 2012
26. Iversen P, Rasmussen F, Asmussen C, et al: Estramustine phosphate versus placebo as second line treatment after orchiectomy in patients with metastatic prostate cancer: DAPROCA study 9002. Danish Prostatic Cancer Group. J Urol 157:929-934, 1997 (Pubitemid 27066281)
27. Carducci MA, Padley RJ, Breul J, et al: Effect of endothelin-A receptor blockade with atrasentan on tumor progression in men with hormone-refractory prostate cancer: A randomized, phase II, placebo-controlled trial. J Clin Oncol 21:679-689, 2003 (Pubitemid 46621903)
28. Small EJ, Schellhammer PF, Higano CS, et al: Placebo-controlled phase III trial of immunologic therapy with sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer. J Clin Oncol 24:3089-3094, 2006 (Pubitemid 46638945)
29. Kantoff PW, Higano CS, Shore ND, et al: Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 363:411-422, 2010
30. Pili R, Häggman M, Stadler WM, et al: Phase II randomized, double-blind, placebo-controlled study of tasquinimod in men with minimally symptomatic metastatic castrate-resistant prostate cancer. J Clin Oncol 29:4022-4028, 2011
31. de Bono JS, Logothetis CJ, Molina A, et al: Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med 364:1995-2005, 2011
32. Ryan CJ, Smith MR, de Bono JS, et al: Abiraterone in metastatic prostate cancer without previous chemotherapy. N Engl J Med 368:138-148, 2013
33. Scher HI, Fizazi K, Saad F, et al: Increased survival with enzalutamide in prostate cancer after chemotherapy. N Engl J Med 367:1187-1197, 2012
34. Gleave ME, Elhilali M, Fradet Y, et al: Interferon gamma-1b compared with placebo in metastatic renal-cell carcinoma: Canadian Urologic Oncology Group. N Engl J Med 338:1265-1271, 1998 (Pubitemid 28216580)
35. Yang JC, Haworth L, Sherry RM, et al: A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 349:427-434, 2003 (Pubitemid 36910021)
36. Escudier B, Eisen T, Stadler WM, et al: Sorafenib for treatment of renal cell carcinoma: Final efficacy and safety results of the phase III treatment approaches in renal cancer global evaluation trial. J Clin Oncol 27:3312-3318, 2009
37. Motzer RJ, Escudier B, Oudard S, et al: Efficacy of everolimus in advanced renal cell carcinoma: A double-blind, randomised, placebo-controlled phase III trial. Lancet 372:449-456, 2008
38. Sternberg CN, Davis ID, Mardiak J, et al: Pazopanib in locally advanced or metastatic renal cell carcinoma: Results of a randomized phase III trial. J Clin Oncol 28:1061-1068, 2010
39. Mulders P, Hawkins R, Nathan P, et al: Cediranib monotherapy in patients with advanced renal cell carcinoma: Results of a randomised phase II study. Eur J Cancer 48:527-537, 2012
40. Scheithauer W, Rosen H, Kornek GV, et al: Randomised comparison of combination chemotherapy plus supportive care with supportive care alone in patients with metastatic colorectal cancer. BMJ 306:752-755, 1993 (Pubitemid 23080053)
41. Goldberg RM, Moertel CG, Wieand HS, et al: A phase III evaluation of a somatostatin analogue (octreotide) in the treatment of patients with asymptomatic advanced colon carcinoma. North Central Cancer Treatment Group and the Mayo Clinic. Cancer 76:961-966, 1995
42. Loprinzi CL, Kuross SA, O'Fallon JR, et al: Randomized placebo-controlled evaluation of hydrazine sulfate in patients with advanced colorectal cancer. J Clin Oncol 12:1121-1125, 1994 (Pubitemid 24173923)
43. Rao S, Cunningham D, de Gramont A, et al: Phase III double-blind placebo-controlled study of farnesyl transferase inhibitor R115777 in patients with refractory advanced colorectal cancer. J Clin Oncol 22:3950-3957, 2004 (Pubitemid 41079877)
44. Jonker DJ, O'Callaghan CJ, Karapetis CS, et al: Cetuximab for the treatment of colorectal cancer. N Engl J Med 357:2040-2048, 2007 (Pubitemid 350106711)
45. Van Cutsem E, Peeters M, Siena S, et al: Open-label phase III trial of panitumumab plus best supportive care compared with best supportive care alone in patients with chemotherapy-refractory metastatic colorectal cancer. J Clin Oncol 25:1658-1664, 2007 (Pubitemid 46797944)
46. Yoshino T, Mizunuma N, Yamazaki K, et al: TAS-102 monotherapy for pretreated metastatic colorectal cancer: A double-blind, randomised, placebo-controlled phase 2 trial. Lancet Oncol 13:993-1001, 2012
47. Grothey A, Van Cutsem E, Sobrero A, et al: Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): An international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet 381:303-312, 2013
48. Grimaldi C, Bleiberg H, Gay F, et al: Evaluation of antiandrogen therapy in unresectable hepatocellular carcinoma: Results of a European Organization for Research and Treatment of Cancer multicentric double-blind trial. J Clin Oncol 16:411-417, 1998 (Pubitemid 28135581)
49. Manesis EK, Giannoulis G, Zoumboulis P, et al: Treatment of hepatocellular carcinoma with combined suppression and inhibition of sex hormones: A randomized, controlled trial. Hepatology 21:1535-1542, 1995
50. Castells A, Bruix J, Brú C, et al: Treatment of hepatocellular carcinoma with tamoxifen: A double-blind placebo-controlled trial in 120 patients. Gastroenterology 109:917-922, 1995
51. Barbare JC, Bouché O, Bonnetain F, et al: Treatment of advanced hepatocellular carcinoma with long-acting octreotide: A phase III multicentre, randomised, double blind placebo-controlled study. Eur J Cancer 45:1788-1797, 2009
52. Llovet JM, Ricci S, Mazzaferro V, et al: Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359:378-390, 2008
53. Cheng AL, Kang YK, Chen Z, et al: Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: A phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 10:25-34, 2009
54. Santoro A, Rimassa L, Borbath I, et al: Tivantinib for second-line treatment of advanced hepatocellular carcinoma: A randomised, placebo-controlled phase 2 study. Lancet Oncol 14:55-63, 2013
55. Pyrhonen S, Kuitunen T, Nyandoto P, et al: Randomised comparison of fluorouracil, epidoxorubicin and methotrexate (FEMTX) plus supportive care with supportive care alone in patients with non-resectable gastric cancer. Br J Cancer 71:587-591, 1995
56. Glimelius B, Ekstrom K, Hoffman K, et al: Randomized comparison between chemotherapy plus best supportive care with best supportive care in advanced gastric cancer. Ann Oncol 8:163-168, 1997 (Pubitemid 27112884)
57. Thuss-Patience PC, Kretzschmar A, Bichev D, et al: Survival advantage for irinotecan versus best supportive care as second-line chemotherapy in gastric cancer: A randomised phase III study of the Arbeitsgemeinschaft Internistische Onkologie (AIO). Eur J Cancer 47:2306-2314, 2011
58. Kang JH, Lee SI, Lim do H, et al: Salvage chemotherapy for pretreated gastric cancer: A randomized phase III trial comparing chemotherapy plus best supportive care with best supportive care alone. J Clin Oncol 30:1513-1518, 2012
59. Mallinson CN, Rake MO, Cocking JB, et al: Chemotherapy in pancreatic cancer: Results of a controlled, prospective, randomised, multicentre trial. BMJ 281:1589-1591, 1980 (Pubitemid 11253138)
60. Pelzer U, Schwaner I, Stieler J, et al: Best supportive care (BSC) versus oxaliplatin, folinic acid and 5-fluorouracil (OFF) plus BSC in patients for second-line advanced pancreatic cancer: A phase III-study from the German CONKO-study group. Eur J Cancer 47:1676-1681, 2011
61. Ciuleanu TE, Pavlovsky AV, Bodoky G, et al: A randomised phase III trial of glufosfamide compared with best supportive care in metastatic pancreatic adenocarcinoma previously treated with gemcitabine. Eur J Cancer 45:1589-1596, 2009
62. Rinke A, Müller HH, Schade-Brittinger C, et al: Placebo-controlled, double-blind, prospective, randomized study on the effect of octreotide LAR in the control of tumor growth in patients with metastatic neuroendocrine midgut tumors: A report from the PROMID Study Group. J Clin Oncol 27:4656-4663, 2009
63. Raymond E, Dahan L, Raoul JL, et al: Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med 364:501-513, 2011
64. Yao JC, Shah MH, Ito T, et al: Everolimus for advanced pancreatic neuroendocrine tumors. N Engl J Med 364:514-523, 2011
65. Jassem J, Ramlau R, Santoro A, et al: Phase III trial of pemetrexed plus best supportive care compared with best supportive care in previously treated patients with advanced malignant pleural mesothelioma. J Clin Oncol 26:1698-1704, 2008
66. Muers MF, Stephens RJ, Fisher P, et al: Active symptom control with or without chemotherapy in the treatment of patients with malignant pleural mesothelioma (MS01): A multicentre randomised trial. Lancet 371:1685-1694, 2008 (Pubitemid 351671885)
67. Wells SA Jr, Robinson BG, Gagel RF, et al: Vandetanib in patients with locally advanced or metastatic medullary thyroid cancer: A randomized, double-blind phase III trial. J Clin Oncol 30:134-141, 2012
68. Machiels JP, Subramanian S, Ruzsa A, et al: Zalutumumab plus best supportive care versus best supportive care alone in patients with recurrent or metastatic squamous-cell carcinoma of the head and neck after failure of platinum-based chemotherapy: An open-label, randomised phase 3 trial. Lancet Oncol 12:333-343, 2011
69. van der Graaf WT, Blay JY, Chawla SP, et al: Pazopanib for metastatic soft-tissue sarcoma (PALETTE): A randomised, double-blind, placebo-controlled phase 3 trial. Lancet 379:1879-1886, 2012
70. Bellmunt J, Théodore C, Demkov T, et al: Phase III trial of vinflunine plus best supportive care compared with best supportive care alone after a platinum-containing regimen in patients with advanced transitional cell carcinoma of the urothelial tract. J Clin Oncol 27:4454-4461, 2009
71. Demetri GD, van Oosterom AT, Garrett CR, et al: Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: A randomised controlled trial. Lancet 368:1329-1338, 2006 (Pubitemid 44528723)
72. Demetri GD, Reichardt P, Kang YK, et al: Efficacy and safety of regorafenib for advanced gastrointestinal stromal tumours after failure of imatinib and sunitinib (GRID): An international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet 381:295-302, 2013
73. O'Brien ME, Ciuleanu TE, Tsekov H, et al: Phase III trial comparing supportive care alone with supportive care with oral topotecan in patients with relapsed small-cell lung cancer. J Clin Oncol 24:5441-5447, 2006 (Pubitemid 46623178)
74. Sharma A, Dwary AD, Mohanti BK, et al: Best supportive care compared with chemotherapy for unresectable gall bladder cancer: A randomized controlled study. J Clin Oncol 28:4581-4586, 2010
75. Kopec JA, Abrahamowicz M, Esdaile JM: Randomized discontinuation trials: Utility and efficiency. J Clin Epidemiol 46:959-971, 1993 (Pubitemid 23258894)