The strength of association between surrogate end points and survival in oncology: A systematic review of trial-level meta-analyses

JAMA Internal Medicine

Volumn 175, Issue 8, 2015, Pages 1389-1398

  Prasad, Vinay ^a   Kim, Chul ^a   Burotto, Mauricio ^a   Vandross, Andrae ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED CANCER; ARTICLE; CANCER ADJUVANT THERAPY; CORRELATION ANALYSIS; HUMAN; METASTASIS; MULTICENTER STUDY; ONCOLOGICAL PARAMETERS; OVERALL SURVIVAL; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); SURROGATE END POINT; SYSTEMATIC REVIEW; META ANALYSIS; MORTALITY; NEOPLASMS; SURVIVAL RATE; TREATMENT OUTCOME;

BIOLOGICAL MARKER;

BIOLOGICAL MARKERS; HUMANS; NEOPLASMS; SURVIVAL RATE; TREATMENT OUTCOME;

EID: 84939825159     PISSN: 21686106     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamainternmed.2015.2829     Document Type: Article

References (101)

1. Svensson S, Menkes DB, Lexchin J. Surrogate outcomes in clinical trials: a cautionary tale. JAMA Intern Med. 2013;173(8):611-612.
2. Prasad V, Vandross A. Cardiovascular primary prevention: how high should we set the bar? Arch Intern Med. 2012;172(8):656-659.
3. Fleming TR, DeMets DL. Surrogate end points in clinical trials: are we being misled? Ann Intern Med. 1996;125(7):605-613.
4. Messerli FH, Bangalore S. ALTITUDE trial and dual RAS blockade: the alluring but soft science of the surrogate end point. Am J Med. 2013;126(3):e1-e3.
5. Yudkin JS, Lipska KJ, Montori VM. The idolatry of the surrogate. BMJ. 2011;343:d7995.
6. Ciani O, Buyse M, Garside R, et al. Comparison of treatment effect sizes associated with surrogate and final patient relevant outcomes in randomised controlled trials:meta-epidemiological study. http://www.bmj.com/content/346/bmj.f457. Accessed May 12, 2015.
7. Shi Q, Sargent DJ. Meta-analysis for the evaluation of surrogate endpoints in cancer clinical trials. Int J Clin Oncol. 2009;14(2):102-111.
8. Fauber JCE. FDA approves cancer drugs without proof they're extending lives. http://www.jsonline.com/watchdog/watchdogreports/fda-approves-cancer-drugs-without-proof-theyre-extending-lives-b99348000z1-280437692.html. Accessed December 14, 2014.
9. Korde N, Zingone A, Kwok M, et al Phase II clinical and correlative study of carfilzomib, lenalidomide, and dexamethasone (CRd) in newly diagnosed multiplemyeloma (MM) patients. J Clin Oncol. 2012(suppl);abstr e18568.
10. Jakubowiak AJ, Dytfeld D, Griffith KA, et al. A phase 1/2 study of carfilzomib in combination with lenalidomide and low-dose dexamethasone as a frontline treatment for multiplemyeloma. Blood. 2012;120(9):1801-1809.
11. National Comprehensive Cancer Network. Myeloma NgM [registration required]. http://www.nccn.org/professionals/physician-gls/pdf/myeloma.pdf. Accessed May 12, 2015.
12. Tillman K, Burton B, Jacques LB, Phurrough SE. Compendia and anticancer therapy under Medicare. Ann Intern Med. 2009;150(5):348-350.
13. McGivneyWT. Medicare recognizes NCCN compendium. J Natl Compr Canc Netw. 2008;6(7):635.
14. McGivneyWT. NCCN guidelines and their impact on coverage policy. J Natl Compr Canc Netw. 2010;8(6):625.
15. Miller K,WangM, Gralow J, et al. Paclitaxel plus bevacizumab versus paclitaxel alone formetastatic breast cancer. N Engl J Med. 2007;357(26):2666-2676.
16. Carpenter D, Kesselheim AS, Joffe S. Reputation and precedent in the bevacizumab decision. N Engl J Med. 2011;365(2):e3.
17. Torri V, Simon R, Russek-Cohen E, Midthune D, Friedman M. Statistical model to determine the relationship of response and survival in patients with advanced ovarian cancer treated with chemotherapy. J Natl Cancer Inst. 1992;84(6):407-414.
18. Freedman LS, Graubard BI, Schatzkin A. Statistical validation of intermediate endpoints for chronic diseases. Stat Med. 1992;11(2):167-178.
19. Buyse M, Molenberghs G, Burzykowski T, Renard D, Geys H. The validation of surrogate endpoints inmeta-analyses of randomized experiments. Biostatistics. 2000;1(1):49-67.
20. Weir CJ,Walley RJ. Statistical evaluation of biomarkers as surrogate endpoints: a literature review. Stat Med. 2006;25(2):183-203.
21. Elston J, Taylor RS. Use of surrogate outcomes in cost-effectiveness models: a review of United Kingdom health technology assessment reports. Int J Technol Assess Health Care. 2009;25(1):6-13.
22. BuyseM, Burzykowski T, Michiels S, Carroll K. Individual- and trial-level surrogacy in colorectal cancer. Stat Methods Med Res. 2008;17(5):467-475.
23. Prentice RL. Surrogate endpoints in clinical trials: definition and operational criteria. Stat Med. 1989;8(4):431-440.
24. Sargent DJ,Wieand HS, Haller DG, et al. Disease-free survival versus overall survival as a primary end point for adjuvant colon cancer studies: individual patient data from 20,898 patients on 18 randomized trials. J Clin Oncol. 2005;23(34):8664-8670.
25. Pratt CM, Moyé LA. The cardiac arrhythmia suppression trial: casting suppression in a different light. Circulation. 1995;91(1):245-247.
26. Echt DS, Liebson PR,Mitchell LB, et al. Mortality and morbidity in patients receiving encainide, flecainide, or placebo: the Cardiac Arrhythmia Suppression Trial. N Engl J Med. 1991;324(12):781-788.
27. Laporte S, Squifflet P, Baroux N, et al. Prediction of survival benefits from progression-free survival benefits in advanced non-small-cell lung cancer: evidence from a meta-analysis of 2334 patients from 5 randomised trials. BMJ Open. 2013;3(3):e001802.
28. Burzykowski T, BuyseM. Surrogate threshold effect: an alternative measure for meta-analytic surrogate endpoint validation. Pharm Stat. 2006;5(3):173-186.
29. Buyse M. Use of meta-analysis for the validation of surrogate endpoints and biomarkers in cancer trials. Cancer J. 2009;15(5):421-425.
30. Sherrill B, Kaye JA, Sandin R, Cappelleri JC, Chen C. Review of meta-analyses evaluating surrogate endpoints for overall survival in oncology. Onco Targets Ther. 2012;5:287-296.
31. Davis S, Tappenden P, Cantrell A. A review of studies examining the relationship between progression-free survival and overall survival in advanced or metastatic cancer. http://www.nicedsu.org.uk/PFSOS%20Report.FINAL.06.08.12.pdf. Accessed May 12, 2015.
32. Ciani O, Davis S, Tappenden P, et al. Validation of surrogate endpoints in advanced solid tumors: systematic review of statistical methods, results, and implications for policy makers. Int J Technol Assess Health Care. 2014;30(3):312-324.
33. Institute for Quality and Efficiency in Health Care [Institut für Qualität und Wirtschaftlichkeit im Gesundheitswesen] (IQWiG). Validity of surrogate endpoints in oncology: executive summary. http://www.iqwig.de/download/A10-05-Executive-Summary-v1-1-Surrogate-endpoints-in-oncology.pdf. Accessed December 20, 2014.
34. Cortazar P, Zhang L, Untch M, et al. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet. 2014;384(9938):164-172.
35. Berruti A, Amoroso V, Gallo F, et al. Pathologic complete response as a potential surrogate for the clinical outcome in patients with breast cancer after neoadjuvant therapy: ameta-regression of 29 randomized prospective studies. J Clin Oncol. 2014;32(34):3883-3891.
36. Ng R, Pond GR, Tang PA, MacIntosh PW, Siu LL, Chen EX. Correlation of changes between 2-year disease-free survival and 5-year overall survival in adjuvant breast cancer trials from 1966 to 2006. Ann Oncol. 2008;19(3):481-486.
37. Burzykowski T, Buyse M, Yothers G, Sakamoto J, Sargent D. Exploring and validating surrogate endpoints in colorectal cancer. Lifetime Data Anal. 2008;14(1):54-64.
38. Oba K, Paoletti X, Alberts S, et al; GASTRIC group. Disease-free survival as a surrogate for overall survival in adjuvant trials of gastric cancer: ameta-analysis. J Natl Cancer Inst. 2013;105(21):1600-1607.
39. Michiels S, Le Maître A, Buyse M, et al MARCH and MACH-NC Collaborative Groups. Surrogate endpoints for overall survival in locally advanced head and neck cancer:meta-analyses of individual patient data. Lancet Oncol. 2009;10(4):341-350.
40. Mauguen A, Pignon JP, Burdett S, et al Surrogate Lung Project Collaborative Group. Surrogate endpoints for overall survival in chemotherapy and radiotherapy trials in operable and locally advanced lung cancer: a re-analysis of meta-analyses of individual patients' data. Lancet Oncol. 2013;14(7):619-626.
41. Bruzzi P, Del Mastro L, Sormani MP, et al. Objective response to chemotherapy as a potential surrogate end point of survival inmetastatic breast cancer patients. J Clin Oncol. 2005;23(22):5117-5125.
42. Hackshaw A, Knight A, Barrett-Lee P, Leonard R. Surrogate markers and survival in women receiving first-line combination anthracycline chemotherapy for advanced breast cancer. Br J Cancer. 2005;93(11):1215-1221.
43. Burzykowski T, Buyse M, Piccart-Gebhart MJ, et al. Evaluation of tumor response, disease control, progression-free survival, and time to progression as potential surrogate end points inmetastatic breast cancer. J Clin Oncol. 2008;26(12):1987-1992.
44. Miksad RA, Zietemann V, Gothe R, et al. Progression-free survival as a surrogate endpoint in advanced breast cancer. Int J Technol Assess Health Care. 2008;24(4):371-383.
45. Sherrill B, Amonkar M, Wu Y, et al. Relationship between effects on time-to-disease progression and overall survival in studies of metastatic breast cancer. Br J Cancer. 2008;99(10):1572-1578.
46. Wilkerson J, Fojo T. Progression-free survival is simply a measure of a drug's effect while administered and is not a surrogate for overall survival. Cancer J. 2009;15(5):379-385.
47. Beauchemin C, Cooper D, Lapierre ME, Yelle L, Lachaine J. Progression-free survival as a potential surrogate for overall survival inmetastatic breast cancer. Onco Targets Ther. 2014;7:1101-1110.
48. Petrelli F, Barni S. Surrogate endpoints in metastatic breast cancer treated with targeted therapies: an analysis of the first-line phase III trials. Med Oncol. 2014;31(1):776.
49. Johnson KR, Ringland C, Stokes BJ, et al. Response rate or time to progression as predictors of survival in trials of metastatic colorectal cancer or non-small-cell lung cancer: ameta-analysis. Lancet Oncol. 2006;7(9):741-746.
50. Chirila C, Odom D, Devercelli G, et al. Meta-analysis of the association between progression-free survival and overall survival in metastatic colorectal cancer. Int J Colorectal Dis. 2012;27(5):623-634.
51. Sidhu R, Rong A, Dahlberg S. Evaluation of progression-free survival as a surrogate endpoint for survival in chemotherapy and targeted agent metastatic colorectal cancer trials. Clin Cancer Res. 2013;19(5):969-976.
52. Buyse M, Thirion P, Carlson RW, Burzykowski T, Molenberghs G, Piedbois P; Meta-Analysis Group in Cancer. Relation between tumour response to first-line chemotherapy and survival in advanced colorectal cancer: ameta-analysis. Lancet. 2000;356(9227):373-378.
53. Tang PA, Bentzen SM, Chen EX, Siu LL. Surrogate end points for median overall survival in metastatic colorectal cancer: literature-based analysis from 39 randomized controlled trials of first-line chemotherapy. J Clin Oncol. 2007;25(29):4562-4568.
54. Giessen C, Laubender RP, Ankerst DP, et al. Progression-free survival as a surrogate endpoint for median overall survival inmetastatic colorectal cancer: literature-based analysis from 50 randomized first-line trials. Clin Cancer Res. 2013;19(1):225-235.
55. Shi Q, de Gramont A, Grothey A, et al. Individual patient data analysis of progression-free survival versus overall survival as a first-line end point formetastatic colorectal cancer in modern randomized trials: findings from the analysis and research in cancers of the digestive system database. J Clin Oncol. 2015;33(1):22-28.
56. Giessen C, Laubender RP, Ankerst DP, et al. Surrogate end points in second-line treatment for mCRC: a systematic literature-based analysis from 23 randomised trials. Acta Oncol. 2015;54(2):187-193.
57. Buyse M, Burzykowski T, Carroll K, et al. Progression-free survival is a surrogate for survival in advanced colorectal cancer. J Clin Oncol. 2007;25(33):5218-5224.
58. Amir E, Seruga B, Kwong R, Tannock IF, Ocaña A. Poor correlation between progression-free and overall survival in modern clinical trials: are composite endpoints the answer? Eur J Cancer. 2012;48(3):385-388.
59. Paoletti X, Oba K, Bang YJ, et al; GASTRIC group. Progression-free survival as a surrogate for overall survival in advanced/recurrent gastric cancer trials: ameta-analysis. J Natl Cancer Inst. 2013;105(21):1667-1670.
60. Shitara K, Matsuo K, Muro K, Doi T, Ohtsu A. Correlation between overall survival and other endpoints in clinical trials of second-line chemotherapy for patients with advanced gastric cancer. Gastric Cancer. 2014;17(2):362-370.
61. Flaherty KT, HennigM, Lee SJ, et al. Surrogate endpoints for overall survival inmetastatic melanoma: ameta-analysis of randomised controlled trials. Lancet Oncol. 2014;15(3):297-304.
62. Lee L,Wang L, Crump M. Identification of potential surrogate end points in randomized clinical trials of aggressive and indolent non-Hodgkin's lymphoma: correlation of complete response, time-to-event and overall survival end points. Ann Oncol. 2011;22(6):1392-1403.
63. Hayashi H, Okamoto I, Taguri M, Morita S, Nakagawa K. Postprogression survival in patients with advanced non-small-cell lung cancer who receive second-line or third-line chemotherapy. Clin Lung Cancer. 2013;14(3):261-266.
64. Delea TE, Khuu A, Heng DY, Haas T, Soulières D. Association between treatment effects on disease progression end points and overall survival in clinical studies of patients with metastatic renal cell carcinoma. Br J Cancer. 2012;107(7):1059-1068.
65. Johnson KR, Liauw W, Lassere MN. Evaluating surrogacy metrics and investigating approval decisions of progression-free survival (PFS) in metastatic renal cell cancer: a systematic review. Ann Oncol. 2015;26(3):485-496.
66. Foster NR, Qi Y, Shi Q, et al. Tumor response and progression-free survival as potential surrogate endpoints for overall survival in extensive stage small-cell lung cancer: findings on the basis of North Central Cancer Treatment Group trials. Cancer. 2011;117(6):1262-1271.
67. Hotta K, Fujiwara Y, Matsuo K, et al. Time to progression as a surrogate marker for overall survival in patients with advanced non-small cell lung cancer. J Thorac Oncol. 2009;4(3):311-317.
68. Non-small Cell Lung Cancer Collaborative Group. Chemotherapy in non-small cell lung cancer: ameta-analysis using updated data on individual patients from 52 randomised clinical trials. BMJ. 1995;311(7010):899-909.
69. Aupérin A, Le Péchoux C, Rolland E, et al. Meta-analysis of concomitant versus sequential radiochemotherapy in locally advanced non-small-cell lung cancer. J Clin Oncol. 2010;28(13):2181-2190.
70. Arriagada R, Auperin A, Burdett S, et al NSCLC Meta-analyses Collaborative Group. Adjuvant chemotherapy, with or without postoperative radiotherapy, in operable non-small-cell lung cancer: two meta-analyses of individual patient data. Lancet. 2010;375(9722):1267-1277.
71. NSCLC Meta-Analyses Collaborative Group. Chemotherapy in addition to supportive care improves survival in advanced non-small-cell lung cancer: a systematic review and meta-analysis of individual patient data from 16 randomized controlled trials. J Clin Oncol. 2008;26(28):4617-4625.
72. Mauguen A, Le Péchoux C, Saunders MI, et al. Hyperfractionated or accelerated radiotherapy in lung cancer: an individual patient data meta-analysis. J Clin Oncol. 2012;30(22):2788-2797.
73. Paoletti X, Oba K, Burzykowski T, et al GASTRIC (Global Advanced/Adjuvant Stomach Tumor Research International Collaboration) Group. Benefit of adjuvant chemotherapy for resectable gastric cancer: ameta-analysis. JAMA. 2010;303(17):1729-1737.
74. Buyse M, Sargent DJ, Grothey A, Matheson A, de Gramont A. Biomarkers and surrogate end points: the challenge of statistical validation. Nat Rev Clin Oncol. 2010;7(6):309-317.
75. Booth CM, Eisenhauer EA. Progression-free survival: meaningful or simply measurable? J Clin Oncol. 2012;30(10):1030-1033.
76. Booth CM, Cescon DW,Wang L, Tannock IF, Krzyzanowska MK. Evolution of the randomized controlled trial in oncology over three decades. J Clin Oncol. 2008;26(33):5458-5464.
77. Kay A, Higgins J, Day AG,Meyer RM, Booth CM. Randomized controlled trials in the era of molecular oncology: methodology, biomarkers, and end points. Ann Oncol. 2012;23(6):1646-1651.
78. Prasad V, Cifu A, Ioannidis JP. Reversals of established medical practices: evidence to abandon ship. JAMA. 2012;307(1):37-38.
79. Prasad V, Vandross A, Toomey C, et al. A decade of reversal: an analysis of 146 contradicted medical practices. Mayo Clin Proc. 2013;88(8):790-798.
80. US Food and Drug Administration. FDA approves Afinitor for advanced breast cancer. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm312965.htm. Accessed January 4, 2014.
81. Piccart M, Hortobagyi GN, Campone M, et al. Everolimus plus exemestane for hormone-receptorpositive, human epidermal growth factor receptor-2-negative advanced breast cancer: overall survival results from BOLERO-2. Ann Oncol. 2014;25(12):2357-2362.
82. Finn RS, Crown JP, Lang I, et al. The cyclin-dependent kinase 4/6 inhibitor palbociclib in combination with letrozole versus letrozole alone as first-line treatment of oestrogen receptor-positive, HER2-negative, advanced breast cancer (PALOMA-1/TRIO-18): a randomised phase 2 study. Lancet Oncol. 2015;16(1):25-35.
83. Ning YM, He K, Dagher R, et al. Liposomal doxorubicin in combination with bortezomib for relapsed or refractory multiplemyeloma. Oncology (Williston Park). 2007;21(12):1503-1508.
84. Orlowski RZ, Nagler A, Sonneveld P, et al. Final overall survival results of a randomized trial comparing bortezomib plus pegylated liposomal doxorubicin with bortezomib alone in subjects with relapsed or refractory multiplemyeloma. Blood. 2014;124(21):3448.
85. Ioannidis JP. Effect of the statistical significance of results on the time to completion and publication of randomized efficacy trials. JAMA. 1998;279(4):281-286.
86. Krzyzanowska MK, Pintilie M, Tannock IF. Factors associated with failure to publish large randomized trials presented at an oncology meeting. JAMA. 2003;290(4):495-501.
87. Misakian AL, Bero LA. Publication bias and research on passive smoking: comparison of published and unpublished studies. JAMA. 1998;280(3):250-253.
88. Dickersin K, Min YI, Meinert CL. Factors influencing publication of research results. Follow-up of applications submitted to two institutional review boards. JAMA. 1992;267(3):374-378.
89. Dwan K, Altman DG, Arnaiz JA, et al. Systematic review of the empirical evidence of study publication bias and outcome reporting bias. PLoS One. 2008;3(8):e3081.
90. Rising K, Bacchetti P, Bero L. Reporting bias in drug trials submitted to the Food and Drug Administration: review of publication and presentation. PLoS Med. 2008;5(11):e217.
91. Jefferson T, JonesM, Doshi P, Spencer EA, Onakpoya I, Heneghan CJ. Oseltamivir for influenza in adults and children: systematic review of clinical study reports and summary of regulatory comments. BMJ. 2014;348:g2545.
92. Kirsch I, Deacon BJ, Huedo-Medina TB, Scoboria A, Moore TJ, Johnson BT. Initial severity and antidepressant benefits: ameta-analysis of data submitted to the Food and Drug Administration. PLoS Med. 2008;5(2):e45.
93. Chapman PB, Hauschild A, Robert C, et al; BRIM-3 Study Group. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med. 2011;364(26):2507-2516.
94. Raymond E, Dahan L, Raoul J-L, et al. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med. 2011;364(6):501-513.
95. Kantoff PW, Higano CS, Shore ND, et al IMPACT Study Investigators. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363(5):411-422.
96. Baselga J, Campone M, Piccart M, et al. Everolimus in postmenopausal hormone-receptor-positive advanced breast cancer. N Engl J Med. 2012;366(6):520-529.
97. Burstein HJ. Bevacizumab for advanced breast cancer: all tied up with a RIBBON? J Clin Oncol. 2011;29(10):1232-1235.
98. Prasad V. Double-crossed: why crossover in clinical trials may be distorting medical science. J Natl Compr Canc Netw. 2013;11(5):625-627.
99. Prasad V, Grady C. Themisguided ethics of crossover trials. Contemp Clin Trials. 2014;37(2):167-169.
100. Lakdawalla DN, Chou JW, Linthicum MT, MacEwan JP, Zhang J, Goldman DP. Evaluating expected costs and benefits of granting access to new treatments on the basis of progression-free survival in non-small-cell lung cancer [published online March 19, 2015]. JAMA Oncol. doi:10.1001/jamaoncol.2015.0203.
101. Fojo T, Mailankody S, Lo A. Unintended consequences of expensive cancer therapeutics - the pursuit of marginal indications and a me-too mentality that stifles innovation and creativity: the John Conley Lecture. JAMA Otolaryngol Head Neck Surg. 2014;140(12):1225-1236.