Design of phase I combination trials: Recommendations of the Clinical Trial Design Task Force of the NCI Investigational Drug Steering Committee

Clinical Cancer Research

Volumn 20, Issue 16, 2014, Pages 4210-4217

  Paller, Channing J ^a   Bradbury, Penelope A ^k   Ivy, S Percy ^b   Seymour, Lesley ^k   LoRusso, Patricia M ^c   Baker, Laurence ^d   Rubinstein, Larry ^b   Huang, Erich ^b   Collyar, Deborah ^e   Groshen, Susan ^f   Reeves, Steven ^b   Ellis, Lee M ^g   Sargent, Daniel J ^h   Rosner, Gary L ^a   LeBlanc, Michael L ⁱ   Ratain, Mark J ^j  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c KARMANOS CANCER INSTITUTE   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

^e Patient Advocates in Research   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^g UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^h MAYO CLINIC   (United States)

ⁱ USA   (United States)

^j UNIVERSITY OF CHICAGO   (United States)

^k Clinical Trials Group   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BEVACIZUMAB; BEXAROTENE; DASATINIB; ERLOTINIB; GEFITINIB; IMATINIB; KETOCONAZOLE; LENALIDOMIDE; LEVOTHYROXINE; NILOTINIB; SORAFENIB; SUNITINIB; TEMSIROLIMUS; VERAPAMIL; NEW DRUG; TUMOR MARKER;

ADVERSE OUTCOME; AREA UNDER THE CURVE; CANCER COMBINATION CHEMOTHERAPY; CANCER RESEARCH; CLINICAL STUDY; DRUG ABSORPTION; DRUG ANTAGONISM; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG EXCRETION; DRUG MECHANISM; DRUG METABOLISM; DRUG SAFETY; HUMAN; MAXIMUM PLASMA CONCENTRATION; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEINURIA; REVIEW; STUDY DESIGN; THROMBOCYTOPENIA; BIOASSAY; CLINICAL PROTOCOL; METHODOLOGY; NATIONAL HEALTH ORGANIZATION; NEOPLASMS; PATIENT SELECTION; PHASE 2 CLINICAL TRIAL (TOPIC); PRACTICE GUIDELINE; PROCEDURES; STANDARDS; UNITED STATES;

BIOMARKERS, TUMOR; CLINICAL PROTOCOLS; CLINICAL TRIALS, PHASE II AS TOPIC; DRUGS, INVESTIGATIONAL; ENDPOINT DETERMINATION; HUMANS; NATIONAL CANCER INSTITUTE (U.S.); NEOPLASMS; PATIENT SELECTION; PRACTICE GUIDELINES AS TOPIC; RESEARCH DESIGN; UNITED STATES;

EID: 84905983305     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-0521     Document Type: Review

References (67)

1. Demetri GD, von Mehren M, Blanke CD, Van den Abbeele AD, Eisenberg B, Roberts PJ, et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 2002;347: 472-80.
2. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001;344:1031-7. (Pubitemid 32267972)
3. Mok TS, Wu YL, Thongprasert S, Yang CH, Chu DT, Saijo N, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009;361:947-57.
4. Sosman JA, Kim KB, Schuchter L, Gonzalez R, Pavlick AC, Weber JS, et al. Survival in BRAF V600-mutant advanced melanoma treated with vemurafenib. N Engl J Med 2012;366:707-14.
5. Kwak EL, Bang YJ, Camidge DR, Shaw AT, Solomon B, Maki RG, et al. Anaplastic lymphoma kinase inhibition in non-small cell lung cancer. N Engl J Med 2010;363:1693-703.
6. Kantarjian HM, Talpaz M, O'Brien S, Giles F, Garcia-Manero G, Faderl S, et al. Dose escalation of imatinib mesylate can overcome resistance to standard-dose therapy in patients with chronic myelogenous leukemia. Blood 2003;101:473-5. (Pubitemid 36077567)
7. Kobayashi S, Boggon TJ, Dayaram T, Janne PA, Kocher O, Meyerson M, et al. EGFR mutation and resistance of non-small cell lung cancer to gefitinib. N Engl J Med 2005;352:786-92. (Pubitemid 40271173)
8. Kosaka T, Yatabe Y, Endoh H, Yoshida K, Hida T, Tsuboi M, et al. Analysis of epidermal growth factor receptor gene mutation in patients with non-small cell lung cancer and acquired resistance to gefitinib. Clin Cancer Res 2006;12:5764-9. (Pubitemid 44629607)
9. Mehra R, Camidge DR, Sharma S, Felip E, Tan DS, Vansteenkiste JF, et al. First-in-human phase I study of the ALK inhibitor LDK378 in advanced solid tumors. J Clin Oncol 2012;30 Suppl:174s, abstr 3007.
10. Soverini S, Martinelli G, Rosti G, Bassi S, Amabile M, Poerio A, et al. ABL mutations in late chronic phase chronic myeloid leukemia patients with up-front cytogenetic resistance to imatinib are associated with a greater likelihood of progression to blast crisis and shorter survival: a study by the GIMEMA Working Party on Chronic Myeloid Leukemia. J Clin Oncol 2005;23:4100-9. (Pubitemid 46211315)
11. Chee KG, Longmate J, Quinn DI, Chatta G, Pinski J, Twardowski P, et al. The AKT inhibitor perifosine in biochemically recurrent prostate cancer: a phase II California/Pittsburgh Cancer Consortium trial. Clin Genitourin Cancer 2007;5:433-7. (Pubitemid 351219696)
12. Jonker DJ, O'Callaghan CJ, Karapetis CS, Zalcberg JR, Tu D, Au HJ, et al. Cetuximab for the treatment of colorectal cancer. N Engl J Med 2007;357:2040-8. (Pubitemid 350106711)
13. Karapetis CS, Khambata-Ford S, Jonker DJ, O'Callaghan CJ, Tu D, Tebbutt NC, et al. K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med 2008;359:1757-65.
14. Krug LM, Kindler H, Calvert H, Manegold C, Tsao AS, Fennell D, et al. Vorinostat in patients with advanced malignant pleural mesothelioma who have failed prior pemetrexed and either cisplatin or carboplatin therapy: a phase III, randomized, double-blind, placebo-controlled trial. Eur J Cancer 2011; 47 Suppl 2:2-3.
15. Miller VA, Hirsh V, Cadranel J, Chen YM, Park K, Kim SW, 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 2012;13:528-38.
16. Shepherd FA, Rodrigues Pereira J, Ciuleanu T, Tan EH, Hirsh V, Thongprasert S, et al. Erlotinib in previously treated non-small cell lung cancer. N Engl J Med 2005;353:123-32. (Pubitemid 41058344)
17. Lorusso PM, Eder JP. Therapeutic potential of novel selective-spectrum kinase inhibitors in oncology. Expert Opin Investig Drugs 2008;17:1013-28.
18. LoRusso PM, Boerner SA, Seymour L. An overview of the optimal planning, design, and conduct of phase I studies of new therapeutics. Clin Cancer Res 2010;16:1710-8.
19. Seymour L, Ivy SP, Sargent D, Spriggs D, Baker L, Rubinstein L, et al. The design of phase II clinical trials testing cancer therapeutics: consensus recommendations from the clinical trial design task force of the national cancer institute investigational drug steering committee. Clin Cancer Res 2010;16:1764-9.
20. National Cancer Institute: Transforming the NCI Clinical Trials Enterprise. Roster of Investigational Drug Steering Committee members. [Accessed 2012 March 25]. Available from: http://www.cancer.gov/aboutnci/organization/ ccct/steering-committees/investigational-drug.
21. Hamberg P, Ratain MJ, Lesaffre E, Verweij J. Dose-escalation models for combination phase I trials in oncology. Eur J Cancer 2010;46:2870-8.
22. Dancey JE, Chen HX. Strategies for optimizing combinations of molecularly targeted anticancer agents. Nat Rev Drug Discov 2006;5:649-59. (Pubitemid 44151603)
23. Johnson JI, Decker S, Zaharevitz D, Rubinstein LV, Venditti JM, Schepartz S, et al. Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br J Cancer 2001;84:1424-31. (Pubitemid 32522115)
24. Voskoglou-Nomikos T, Pater JL, Seymour L. Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin Cancer Res 2003;9:4227-39. (Pubitemid 37204044)
25. Holbeck S, Collins JM, Doroshow JH. NCI-60 combination screening matrix of approved anticancer drugs. Eur J Cancer 2012;48:11.
26. Ocana A, Amir E, Yeung C, Seruga B, Tannock IF. How valid are claims for synergy in published clinical studies? Ann Oncol 2012;23:2161-6.
27. Park SR, Davis M, Doroshow JH, Kummar S. Safety and feasibility of targeted agent combinations in solid tumours. Nat Rev Clin Oncol 2013;10:154-68.
28. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006;58:621-81.
29. Gatzemeier U, Pluzanska A, Szczesna A, Kaukel E, Roubec J, De Rosa F, et al. Phase III study of erlotinib in combination with cisplatin and gemcitabine in advanced non-small cell lung cancer: the Tarceva Lung Cancer Investigation Trial. J Clin Oncol 2007;25:1545-52. (Pubitemid 46733081)
30. Giaccone G, Herbst RS, Manegold C, Scagliotti G, Rosell R, Miller V, et al. Gefitinib in combination with gemcitabine and cisplatin in advanced non-small cell lung cancer: a phase III trial-INTACT 1. J Clin Oncol 2004;22:777-84. (Pubitemid 41103588)
31. Mok TW, Wu YL, Thongprasert S, Yu CJ, Zhang L, Ladreran GE, et al. A randomized placebo-controlled phase III study of intercalated erlotinib with gemcitabine/platinum in first-line advanced non-small cell lung cancer (NSCLC): FASTACT-II. J Clin Oncol 30, 2012 (suppl; abstr 7519).
32. Begley CG, Ellis LM. Drug development: raise standards for preclinical cancer research. Nature 2012;483:531-3.
33. Journal of Negative Results in BioMedicine. [Accessed 2014 Feb 10]. Available from: www.jnrbm.com.
34. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, Sosman J, et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 2012;367:1694-703.
35. Azad NS, Posadas EM, Kwitkowski VE, Steinberg SM, Jain L, Annunziata CM, et al. Combination targeted therapy with sorafenib and bevacizumab results in enhanced toxicity and antitumor activity. J Clin Oncol 2008;26:3709-14.
36. Kummar S, Ji J, Morgan R, Lenz HJ, Puhalla SL, Belani CP, et al. A phase I study of veliparib in combination with metronomic cyclophosphamide in adults with refractory solid tumors and lymphomas. Clin Cancer Res 2012;18:1726-34.
37. Gangadhar TC, Cohen EE, Wu K, Janisch L, Geary D, Kocherginsky M, et al. Two drug interaction studies of sirolimus in combination with sorafenib or sunitinib in patients with advanced malignancies. Clin Cancer Res 2011;17:1956-63.
38. Lee JM, Sarosy GA, Annunziata CM, Azad N, Minasian L, Kotz H, et al. Combination therapy: intermittent sorafenib with bevacizumab yields activity and decreased toxicity. Br J Cancer 2010;102:495-9.
39. Rini BI, Garcia JA, Cooney MM, Elson P, Tyler A, Beatty K, et al. A phase I study of sunitinib plus bevacizumab in advanced solid tumors. Clin Cancer Res 2009;15:6277-83.
40. Wu K, House L, Ramirez J, Seminerio MJ, Ratain MJ. Evaluation of utility of pharmacokinetic studies in phase I trials of two oncology drugs. Clin Cancer Res 2013;19:6039-4.
41. Connolly RM, Rudek MA, Garrett-Mayer E, Jeter SC, Donehower MG, Wright LA, et al. Docetaxel metabolism is not altered by imatinib: findings from an early phase study in metastatic breast cancer. Breast Cancer Res Treat 2011;127:153-62.
42. Zhang X, Huang Y, Navarro MT, Hisoire G, Caulfield JP. A proof-ofconcept and drug-drug interaction study of pamapimod, a novel p38 MAP kinase inhibitor, with methotrexate in patients with rheumatoid arthritis. J Clin Pharmacol 2010;50:1031-8.
43. Hofmeister CC, Yang X, Pichiorri F, Chen P, Rozewski DM, Johnson AJ, et al. Phase I trial of lenalidomide and CCI-779 in patients with relapsed multiple myeloma: evidence for lenalidomide-CCI-779 interaction via P-glycoprotein. J Clin Oncol 2011;29:3427-34.
44. Ribas A, Hodi FS, Callahan M, Konto C, Wolchok J. Hepatotoxicity with combination of vemurafenib and ipilimumab. N Engl J Med 2013;368:1365-6.
45. Le Tourneau C, Lee JJ, Siu LL. Dose escalation methods in phase I cancer clinical trials. J Natl Cancer Inst 2009;101:708-20.
46. Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 2010;376:687-97.
47. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 2004;350:2335-42. (Pubitemid 38702844)
48. Pirker R, Pereira JR, Szczesna A, von Pawel J, Krzakowski M, Ramlau R, et al. Cetuximab plus chemotherapy in patients with advanced non- small cell lung cancer (FLEX): an open-label randomised phase III trial. Lancet 2009;373:1525-31.
49. Scagliotti GV, Novello S, Schiller JH, Hirsh V, Sequist LV, Soria JC, et al. Rationale and design of MARQUEE: a phase III, randomized, doubleblind study of tivantinib plus erlotinib versus placebo plus erlotinib in previously treated patients with locally advanced or metastatic, nonsquamous, non-small cell lung cancer. Clin Lung Cancer 2012;13:391-5.
50. Mita AC, Takimoto CH, Mita M, Tolcher A, Sankhala K, Sarantopoulos J, et al. Phase 1 study of AMG 386, a selective angiopoietin 1/2- neutralizing peptibody, in combination with chemotherapy in adults with advanced solid tumors. Clin Cancer Res 2010;16:3044-56.
51. Goss G, Shepherd FA, Laurie S, Gauthier I, Leighl N, Chen E, et al. A phase I and pharmacokinetic study of daily oral cediranib, an inhibitor of vascular endothelial growth factor tyrosine kinases, in combination with cisplatin and gemcitabine in patients with advanced non-small cell lung cancer: a study of the National Cancer Institute of Canada Clinical Trials Group. Eur J Cancer 2009;45:782-8.
52. Laurie SA, Gauthier I, Arnold A, Shepherd FA, Ellis PM, Chen E, et al. Phase I and pharmacokinetic study of daily oral AZD2171, an inhibitor of vascular endothelial growth factor tyrosine kinases, in combination with carboplatin and paclitaxel in patients with advanced non-small cell lung cancer: the National Cancer Institute of Canada clinical trials group. J Clin Oncol 2008;26:1871-8.
53. Harrington JA, Wheeler GM, Sweeting MJ, Mander AP, Jodrell DI. Adaptive designs for dual-agent phase I dose-escalation studies. Nat Rev Clin Oncol 2013;10:277-88.
54. Mandrekar SJ, Cui Y, Sargent DJ. An adaptive phase I design for identifying a biologically optimal dose for dual agent drug combinations. Stat Med 2007;26:2317-30. (Pubitemid 46730251)
55. Thall PF, Cook JD. Dose-finding based on efficacy-toxicity trade-offs. Biometrics 2004;60:684-93. (Pubitemid 39181113)
56. Reardon DA, Vredenburgh JJ, Desjardins A, Peters KB, Sathornsumetee S, Threatt S, et al. Phase 1 trial of dasatinib plus erlotinib in adults with recurrent malignant glioma. J Neurooncol 2012;108:499-506.
57. Rudin CM. Vismodegib. Clin Cancer Res 2012;18:3218-22.
58. Lewis LD. Drug-drug interactions: is there an optimal way to study them? Br J Clin Pharmacol 2010;70:781-3.
59. Reardon DA, Groves MD, Wen PY, Nabors L, Mikkelsen T, Rosenfeld S, et al. A Phase I/II Trial of pazopanib in combination with lapatinib in adult patients with relapsed malignant glioma. Clin Cancer Res 2013;19:900-8.
60. Sandler A, Gray R, Perry MC, Brahmer J, Schiller JH, Dowlati A, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small cell lung cancer. N Engl J Med 2006;355:2542-50. (Pubitemid 44917502)
61. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013;369:122-33.
62. Boulay A, Rudloff J, Ye J, Zumstein-Mecker S, O'Reilly T, Evans DB, et al. Dual inhibition of mTOR and estrogen receptor signaling in vitro induces cell death in models of breast cancer. Clin Cancer Res 2005;11:5319-28. (Pubitemid 41003721)
63. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, et al. MET amplification leads to ge fitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007;316:1039-43. (Pubitemid 46799492)
64. Li J, Zhao M, He P, Hidalgo M, Baker SD. Differential metabolism of gefitinib and erlotinib by human cytochrome P450 enzymes. Clin Cancer Res 2007;13:3731-7. (Pubitemid 46955138)
65. Padda SK, Chhatwani L, Zhou L, Jacobs CD, Lopez-Anaya A, Wakelee HA. Phase I and pharmacokinetic study of bexarotene in combination with gefitinib in the third-line treatment of non-small cell lung cancer: brief report. Anticancer Drugs 2013;24:731-5.
66. Nilotinib: Highlights of Prescribing Information, 2008. [2013 March 26]. Available from: http://dailymed.nlm.nih.gov/dailymed/archives/fdaDrugInfo.cfm? archiveid=6775.
67. Haouala A, Widmer N, Duchosal MA, Montemurro M, Buclin T, Decosterd LA. Drug interactions with the tyrosine kinase inhibitors imatinib, dasatinib, and nilotinib. Blood 2011;117:e75-87.