Biomarker enrichment strategies: Matching trial design to biomarker credentials

Nature Reviews Clinical Oncology

Volumn 11, Issue 2, 2014, Pages 81-90

  Freidlin, Boris ^a   Korn, Edward L ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENTS; ENDPOINT DETERMINATION; HUMANS; NEOPLASMS; RESEARCH DESIGN; TUMOR MARKERS, BIOLOGICAL;

EID: 84895905845     PISSN: 17594774     EISSN: 17594782     Source Type: Journal    
DOI: 10.1038/nrclinonc.2013.218     Document Type: Review

References (53)

1. U.S. Department of Health and Human Services. Enrichment strategies for clinical trials to support approval of human drugs and biological products [online], http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInforma tion/Guidances/UCM332181.pdf%20 (2012).
2. Temple, R. Enrichment of clinical study populations. Clin. Pharmacol. Ther. 88, 774-778 (2010).
3. Van Cutsem, E. et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N. Engl. J. Med. 360, 1408-1417 (2009).
4. Jimeno, A., Messersmith, W. A., Hirsch, F. R., Franklin, W. A. & Eckhardt, S. G. KRAS mutations and sensitivity to epidermal growth factor receptor inhibitors in colorectal cancer: Practical application of patient selection. J. Clin. Oncol. 27, 1130-1136 (2009).
5. Van Custem, E. et al. Cetuximab plus irinotecan, fluorouracil, and leucovorin as first-line treatment for metastatic colorectal cancer: Updated analysis of overall survival according to tumour KRAS and BRAF mutation status. J. Clin. Oncol. 29, 2011-2019 (2011).
6. Leaf, C. Do clinical trials work New York Times [online], http://www.nytimes.com/2013/07/14/opinion/sunday/do-clinical-trials-work. htmlpagewanted=all&-r=0 (13 July 2013).
7. Williams, P. M., Lively, T. G., Jessup, J. M. & Conley, B. A. Bridging the gap: Moving predictive and prognostic assays from research to clinical use. Clin. Cancer Res. 18, 1531-1539 (2012).
8. Simon, R. M., Paik, S. & Hayes, D. F. Use of archived specimens in evaluation of prognostic and predictive biomarkers. J. Natl Cancer. Inst. 101, 1446-1452 (2009).
9. Polley, M. Y. et al. Statistical and practical considerations for clinical evaluation of predictive biomarkers. J. Natl Cancer Inst. http://dx.doi.org/10.1093/jnci/djt282.
10. Simon, R. & Maitournam, A. Evaluating the efficiency of targeted designs for randomized clinical trials. Clin. Cancer Res. 10, 6759-6763 (2004).
11. Chapman, P. B. et al. Improved survival with vemurafenib in melanoma with BRAFV600E mutation. N. Engl. J. Med. 364, 2507-16 (2011).
12. Romond, E. H. et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N. Engl. J. Med. 353, 1673-1684 (2005).
13. Mandrekar, S. J. & Sargent, D. J. Clinical trial designs for predictive biomarker validation: Theoretical considerations and practical challenges. J. Clin. Oncol. 27, 4027-4034 (2009).
14. Paik, S., Kim, C. & Wolmark, N. HER2 status and benefit from adjuvant trastuzumab in breast cancer. N. Engl. J. Med. 358, 1409-1411 (2008).
15. Perez, E. A. et al. HER2 and chromosome 17 effect on patient outcome in the N9831 adjuvant trastuzumab trial. J. Clin. Oncol. 28, 4307-4315 (2010).
16. Freidlin, B., McShane, L. M. & Korn, E. L. Randomized clinical trials with biomarkers: Design issues. J. Natl Cancer Inst. 102, 152-160 (2010).
17. Douillard, J. Y. et al. Randomized, phase III trial of panitumumab with infusional fluorouracil leucovorin, and oxaliplatin (FOLFOX4) versus FOLFOX4 alone as first-line treatment in patients with previously untreated metastatic colorectal cancer: The PRIME study. J. Clin. Oncol. 28, 4697-4705 (2010).
18. Johnston, S. et al. Lapatinib combined with letrozole versus letrozole and placebo as first-line therapy for postmenopausal hormone receptor-positive metastatic breast cancer. J. Clin. Oncol. 27, 5538-5546 (2009).
19. Cappuzzo, F. et al. Erlotinib as maintenance treatment in advanced non-small-cell lung cancer: A multicentre, randomised, placebo-controlled phase study. Lancet Oncol. 11, 521-529 (2010).
20. Rothmann, M. D., Zhang, J. J., Lu, L. & Fleming, T. R. Testing in a prespecified subgroup and the intent-to-treat population. Drug Inf. J. 46, 175-179 (2012).
21. Karuri, S. W. & Simon, R. A two-stage Bayesian design for co-development of new drugs and companion diagnostics. Stat. Med. 31, 901-914 (2012).
22. Freidlin, B., Korn, E. L. & Gray, R. Marker sequential test (MaST) design. Clin. Trials. http://dx.doi.org/10.1177/1740774513503739.
23. Freidlin, B., Sun, Z., Gray, R. & Korn , E. L. Phase III clinical trials that integrate treatment and biomarker evaluation. J. Clin. Oncol. 31, 3158-3161 (2013).
24. Simon, R. The use of genomics in clinical trial design. Clin. Cancer Res. 14, 5984-5993 (2008).
25. Jiang, W., Freidlin, B. & Simon, R. Biomarker-adaptive threshold design: A procedure for evaluating treatment with possible biomarker-defined subset effect. J. Natl Cancer Inst. 99, 1036-1043 (2007).
26. Freidlin, B. & Simon, R. Adaptive signature design: An adaptive clinical trial design for generating and prospectively testing a gene expression signature for sensitive patients. Clin. Cancer Res. 11, 7 872-7878 (2005).
27. McShane, L. M. et al. Criteria for the use of omics-based predictors in clinical trials: Explanation and elaborations. BMC Med. 11, 220 (2013).
28. Green, S., Benedetti, J., Smith, A. & Crowley, J. Clinical Trials in Oncology 2nd edn 97-122 (Chapman & Hall/CRC Press, 2002).
29. Korn, E. L. & Freidlin, B. in Oncology Clinical Trials Ch. 19 (eds Kelly, W. K. & Halabi, S.) 163-177 (Demos Medical Publishing, 2010).
30. Liu, A., Liu, C., Li, Q., Yu, K. F. & Yuan, V. W. A threshold sample-enrichment approach in a clinical trial with h eterogeneous subpopulations. Clin. Trials 7, 537-545 (2010).
31. Rubinstein, L. V. et al. Design issues of randomized phase II trials and a proposal for phase II screening trials. J. Clin. Oncol. 23, 7199-7206 (2005).
32. Amatu, A. et al. Promoter CpG island hypermethylation of the DNA repair enzyme MGMT predicts clinical response to dacarbazine in a phase II study for metastatic colorectal cancer. Clin. Cancer Res. 19, 2265-2272 (2013).
33. Edelman, M. J. et al. Randomized phase II study of ixabepilone or paclitaxel plus carboplatin in patients with non-small-cell lung cancer prospectively stratif ied by -3 tubulin status. J. Clin. Oncol. 31, 1990-1996 (2013).
34. Flaherty, K. T. et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N. Engl. J. Med. 363, 809-819 (2010).
35. Spigel, D. R. et al. Treatment rationale study design for the MetLung trial: A randomized, double-blind phase III study of onartuzumab (MetMAb) in combination with erlotinib versus erlotinib alone in patients who have received standard chemotherapy for stage IIIB or IV Met-positive non-small-cell lung cancer. Clin. Lung Cancer 13, 500-504 (2012).
36. Jones, C. L. & Holmgren, E. An adaptive Simon two-stage design for phase studies of targeted therapies. Contemp. Clin. Trials 28, 654-661 (2007).
37. Freidlin, B., McShane, L. M., Polley, M. Y. & Korn, E. L. Randomized phase II trial designs with biomarkers. J. Clin. Oncol. 30, 3304-3309 (2012).
38. Hayes, D. F. Targeting adjuvant chemotherapy: A good idea that needs to be proven! J. Clin. Oncol. 30, 1264-1267 (2012).
39. Paik, S. et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351, 2817-2826 (2004).
40. Paik, S. et al. Gene expression and benefit of chemotherapy in women with node-negative, oestrogen receptor-positive breast cancer. J. Clin. Oncol. 24, 3726-3734 (2006).
41. Sparano, J. A. TAILORx: Trial assigning individualized options for treatment (Rx). Clin. Breast Cancer 7, 347-350 (2006).
42. Ramsey, S. D. et al. Integrating comp arative effectiveness design elements and endpoints into a phase III, randomized clinical trial (SWOG S1007) evaluating Oncotype DX-guided management for women with breast cancer involving lymph nodes. Contemp. Clin. Trials 34, 1-9 (2013).
43. Rosell, R. et al. 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 trial. Lancet Oncol. 13, 239-246 (2012).
44. Baselga, J. et al. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N. Engl. J. Med. 366, 109-119 (2012).
45. Shaw, A. T. et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N. Engl. J. Med. 368, 2385-2394 (2013).
46. S equist, L. V. et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J. Clin. Oncol. 31, 3327-3334 (2013).
47. Peeters, M. et al. Randomized phase III study of panitumumab with fluorouracil, leucovorin, and irinotecan (FOLFIRI) compared with FOLFIRI alone as second-line treatment in patients with metastatic colorectal cancer. J. Clin. Oncol. 28, 4706-4713 (2010).
48. Sargent, D. J. & Mandrekar, S. J. Statistical issues in the validation of prognostic, predictive, and surrogate biomarkers. Clin. Trials 10, 647-652 (2013).
49. Herbst, R. S. et al. Vandetanib plus docetaxel versus docetaxel as second-line treatment for patients with advanced non-small-cell lung cancer (ZODIAC): A double-blind, randomized, phase trial. Lancet Oncol. 11, 619-626 (2010).
50. Scagliotti, G. V. et al. International, randomized, placebo-controlled, double-blind phase III study of motesanib plus carboplatin/paclitaxel in patients with advanced nonsquamous non-small-cell lung cancer: MONET1. J. Clin. On col. 30, 2829-2836 (2012).
51. Redman, M. W. et al. Design of a phase III clinical trial with prospective biomarker validation: SWOG S0819. Clin. Cancer Res. 18, 4004-4012 (2012).
52. Boyer, M. et al. Rationale and study design for ARCHER: A randomized, double-blind, phase III study of dacomitinib versus erlotinib for advanced non-small-cell lung cancer. Clin. Invest. 3, 29-35 (2013).
53. Miles, D. et al. MERiDiAN: A phase III, randomized, double-blind study of efficacy, safety, and associated biomarker of bevacizumab plus paclitaxel compared with paclitaxel plus placebo, as first-line therapy of pati ents with HER2-negative breast cancer [abstract]. J. Clin. Oncol. 31 (Suppl.), TPS1142 (2013).