Meta-analysis for the evaluation of surrogate endpoints in cancer clinical trials

International Journal of Clinical Oncology

Volumn 14, Issue 2, 2009, Pages 102-111

  Shi, Qian ^a   Sargent, Daniel J ^a  

^a MAYO CLINIC   (United States)

Author keywords

Cancer clinical trial; Disease free survival; Evaluation of surrogate endpoint; Meta analysis; Progression free survival

Indexed keywords

ALEMTUZUMAB; ALTRETAMINE; AMIFOSTINE; ANASTROZOLE; ARSENIC TRIOXIDE; BORTEZOMIB; BUSULFAN; CAPECITABINE; CARCINOEMBRYONIC ANTIGEN; CLADRIBINE; CYTARABINE; DENILEUKIN DIFTITOX; DOCETAXEL; DOXORUBICIN; EXEMESTANE; FULVESTRANT; GEFITINIB; GEMTUZUMAB OZOGAMICIN; IBRITUMOMAB TIUXETAN; IMATINIB; IRINOTECAN; LETROZOLE; OXALIPLATIN; PACLITAXEL; PENTOSTATIN; PROSTATE SPECIFIC ANTIGEN; RETINOIC ACID; TOPOTECAN; TOREMIFENE; UNINDEXED DRUG;

ADVANCED CANCER; ANALYTIC METHOD; BREAST CANCER; CANCER RESEARCH; CANCER SURVIVAL; CLINICAL EVALUATION; CLINICAL TRIAL; COLON CANCER; COLORECTAL CANCER; DISEASE FREE SURVIVAL; DISEASE MARKER; DRUG APPROVAL; FOOD AND DRUG ADMINISTRATION; HUMAN; KAPOSI SARCOMA; LEUKEMIA; LUNG CANCER; LYMPHOMA; META ANALYSIS; MYELOMA; ONCOLOGY; OUTCOME ASSESSMENT; OVARY CANCER; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REVIEW; THERAPY EFFECT;

BIOLOGICAL MARKERS; CLINICAL TRIALS AS TOPIC; HUMANS; META-ANALYSIS AS TOPIC; NEOPLASMS;

EID: 65349191398     PISSN: 13419625     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10147-009-0885-4     Document Type: Review

References (105)

1. J.R. Johnson R. Temple 1985 Food and Drug Administration requirements for approval of new anticancer drugs Cancer Treat Rep 69 1155 1159 (Pubitemid 16239319)
2. T.R. Fleming D.L. DeMets 1996 Surrogate end points in clinical trials: are we being misled? Ann Intern Med 125 605 613 (Pubitemid 126450094)
3. A. Schatzkin 2000 Intermediate markers as surrogate endpoints in cancer research Hematol Oncol Clin North Am 14 887 905 (Pubitemid 30636692)
4. T.R. Fleming 2005 Surrogate endpoints and FDA's accelerated approval process Health Aff (Millwood) 24 67 78 (Pubitemid 40173935)
5. L. Collette T. Burzykowski F.H. Schroder 2006 Prostate-specific antigen (PSA) alone is not an appropriate surrogate marker of long-term therapeutic benefit in prostate cancer trials Eur J Cancer 42 1344 1350 (Pubitemid 43922404)
6. S. Ellenberg J.M. Hamilton 1989 Surrogate endpoints in clinical trials: cancer Stat Med 8 405 413 (Pubitemid 19105888)
7. J. Herson 1989 The use of surrogate endpoints in clinical trials (an introduction to a series of four papers) Stat Med 8 403 404 (Pubitemid 19105887)
8. A. Hillis D. Seigel 1989 Surrogate endpoints in clinical trials: ophthalmologic disorders Stat Med 8 427 430 (Pubitemid 19105890)
9. R.L. Prentice 1989 Surrogate endpoints in clinical trials: definition and operational criteria Stat Med 8 431 440 (Pubitemid 19105891)
10. J. Wittes E. Lakatos J. Probstfield 1989 Surrogate endpoints in clinical trials: cardiovascular diseases Stat Med 8 415 425 (Pubitemid 19105889)
11. J.P. Boissel J.P. Collet P. Moleur 1992 Surrogate endpoints: a basis for a rational approach Eur J Clin Pharmacol 43 235 244
12. M.R. Kosorok 1993 Using surrogate failure time data to increase cost effectiveness in clinical trials Biometrika 80 823 833
13. T.R. Fleming 1994 Surrogate markers in AIDS and cancer trials Stat Med 13 1423 1435 (Pubitemid 24236194)
14. Temple RJ (1995) A regulatory authority's opinion about surrogate endpoints. In: Nimmo WS, Tucker GT (eds) Clinical measurement in drug evaluation. John Wiley and Sons, New York, pp 1-22
15. V. De Gruttola T. Fleming D.Y. Lin 1997 Perspective: validating surrogate markers-are we being naive? J Infect Dis 175 237 246 (Pubitemid 27052228)
16. M.N. Lassere K.R. Johnson M. Boers 2007 Definitions and validation criteria for biomarkers and surrogate endpoints: development and testing of a quantitative hierarchical levels of evidence schema J Rheumatol 34 607 615 (Pubitemid 46364019)
17. R.B. D'Agostino Jr 2000 Debate: the slippery slope of surrogate outcomes Curr Control Trials Cardiovasc Med 1 76 78 (Pubitemid 32219882)
18. Biomarkers Definitions Working Group 2001 Biomarkers and surrogate endpoints: preferred definitions and conceptual framework Clin Pharmacol Ther 69 89 95 (Pubitemid 32225406)
19. B. Manns W.F. Owen Jr W.C. Winkelmayer 2006 Surrogate markers in clinical studies: problems solved or created? Am J Kidney Dis 48 159 166 (Pubitemid 43912941)
20. C. Gluud J. Brok Y. Gong 2007 Hepatology may have problems with putative surrogate outcome measures J Hepatol 46 734 742 (Pubitemid 46420383)
21. US Department of Health and Human Services (2004) FDA: the nation's premier consumer health protection agency. In: US Food and Drug Administration Washington, DC
22. US Department of Health and Human Services (2004) Guidance for industry: fast track drug development programs-designation, development, and application review. In: US Food and Drug Administration, Washington, DC
23. R. Katz 2004 Biomarkers and surrogate markers: an FDA perspective NeuroRx®: J Am Soc Exp NeuroTher 1 189 195 (Pubitemid 46604746)
24. Note for guidance on general considerations for clinical trials (CPMP/ICH/291/95). ICH Topic E 8: general considerations for clinical trials (2006)
25. S. Freud 1910 The origin and development of psychoanalysis Am J Psychol 21 181 218
26. P.H. Wood 1983 Where are we now with radiographic assessment of rheumatoid arthritis? Br J Rheumatol 22 24 33
27. R.B. D'Agostino M.J. Campbell J.B. Greenhouse 2006 Surrogate markers: back to the future Stat Med 25 181 182
28. K. Ray P.K. Sarkar 1999 Surrogate endpoints: do they really contribute in therapeutic decision making? J Assoc Physicians India 47 894 896
29. K. Johnston 1999 What are surrogate outcome measures and why do they fail in clinical research? Neuroepidemiology 18 167 173 (Pubitemid 29284077)
30. B.M. Psaty N.S. Weiss C.D. Furberg 1999 Surrogate end points, health outcomes, and the drug-approval process for the treatment of risk factors for cardiovascular disease JAMA 282 786 790 (Pubitemid 29404389)
31. D.A. Grimes K.F. Schulz 2005 Surrogate end points in clinical research: hazardous to your health Obstet Gynecol 105 1114 1118 (Pubitemid 40571032)
32. H. Hemila 2007 Small trials focusing on surrogate end points may be uninformative Eur J Appl Physiol 99 707 708 (Pubitemid 46404029)
33. J.G. Hardman I.K. Moppett R.P. Mahajan 2008 Validity, credibility, and applicability: the rise and rise of the surrogate Br J Anaesth 101 595 596
34. V.G. De Gruttola P. Clax D.L. DeMets 2001 Considerations in the evaluation of surrogate endpoints in clinical trials: summary of a National Institutes of Health Workshop Control Clin Trials 22 485 502 (Pubitemid 32907433)
35. S.G. Baker B.S. Kramer 2003 A perfect correlate does not a surrogate make BMC Med Res Methodol 3 16 (Pubitemid 38789564)
36. R.J. Lipicky M. Packer 1993 Role of surrogate end points in the evaluation of drugs for heart failure J Am Coll Cardiol 22 179A 184A (Pubitemid 23285821)
37. D.G. Altman 1994 The scandal of poor medical research BMJ 308 283 284 (Pubitemid 24159143)
38. B.E. Sobel C.D. Furberg 1997 Surrogates, semantics, and sensible public policy Circulation 95 1661 1663 (Pubitemid 27142830)
39. P.M. Ridker J. Torres 2006 Reported outcomes in major cardiovascular clinical trials funded by for-profit and not-for-profit organizations: 2000-2005 JAMA 295 2270 2274 (Pubitemid 43736577)
40. P.R. Mansfield J. Lexchin L.S. Wen 2006 Educating health professionals about drug and device promotion: advocates' recommendations PLoS Med 3 e451
41. The Cardiac Arrhythmia Suppression Trial 1989 Preliminary report: effect of encainide and flecainide on mortality in a randomized trial of arrhythmia suppression after myocardial infarction N Engl J Med 321 406 412 (Pubitemid 19190455)
42. C.J. Weir R.J. Walley 2006 Statistical evaluation of biomarkers as surrogate endpoints: a literature review Stat Med 25 183 203 (Pubitemid 43141502)
43. L.S. Freedman B.I. Graubard A. Schatzkin 1992 Statistical validation of intermediate endpoints for chronic diseases Stat Med 11 167 178
44. M.N. Lassere 2008 The Biomarker-Surrogacy Evaluation Schema: a review of the biomarker-surrogate literature and a proposal for a criterion-based, quantitative, multidimensional hierarchical levels of evidence schema for evaluating the status of biomarkers as surrogate endpoints Stat Methods Med Res 17 303 340
45. Burzykowski T, Molenberghs G, Buyse M (eds) (2005) The evaluation of surrogate endpoints (statistics for biology and health). Springer, Berlin Heidelberg New York
46. D.Y. Lin T.R. Fleming V. De Gruttola 1997 Estimating the proportion of treatment effect explained by a surrogate marker Stat Med 16 1515 1527 (Pubitemid 27322655)
47. M. Buyse G. Molenberghs 1998 Criteria for the validation of surrogate endpoints in randomized experiments Biometrics 54 1014 1029 (Pubitemid 28429294)
48. G. Molenberghs M. Buyse H. Geys 2002 Statistical challenges in the evaluation of surrogate endpoints in randomized trials Control Clin Trials 23 607 625 (Pubitemid 36005472)
49. P.W. Bycott J.M. Taylor 1998 An evaluation of a measure of the proportion of the treatment effect explained by a surrogate marker Control Clin Trials 19 555 568 (Pubitemid 29057721)
50. P. Flandre Y. Saidi 1999 Estimating the proportion of treatment effect explained by a surrogate marker Stat Med 18 107 109 (Pubitemid 29015335)
51. M. Buyse G. Molenberghs T. Burzykowski 2000 Statistical validation of surrogate endpoints: problems and proposals Drug Inf J 34 447 454 (Pubitemid 30350997)
52. G. Molenberghs T. Burzykowski A. Alonso 2004 A perspective on surrogate endpoints in controlled clinical trials Stat Methods Med Res 13 177 206 (Pubitemid 38744603)
53. M. Lassere K. Johnson M. Hughes 2007 Simulation studies of surrogate endpoint validation using single trial and multitrial statistical approaches J Rheumatol 34 616 619 (Pubitemid 46364020)
54. M. Buyse G. Molenberghs T. Burzykowski 2000 The validation of surrogate endpoints in meta-analyses of randomized experiments Biostatistics 1 49 67 (Pubitemid 33213521)
55. A. Alonso G. Molenberghs T. Burzykowski 2004 Prentice's approach and the meta-analytic paradigm: a reflection on the role of statistics in the evaluation of surrogate endpoints Biometrics 60 724 728 (Pubitemid 39181117)
56. M.D. Hughes 2002 Evaluating surrogate endpoints Control Clin Trials 23 703 707 (Pubitemid 36005479)
57. M.D. Hughes V. DeGruttola S.L. Welles 1995 Evaluating surrogate markers J Acquir Immune Defic Syndr Hum Retrovirol 10 Suppl2 S1 8
58. M.J. Daniels M.D. Hughes 1997 Meta-analysis for the evaluation of potential surrogate markers Stat Med 16 1965 1982 (Pubitemid 27397267)
59. M.H. Gail R. Pfeiffer H.C. Van Houwelingen 2000 On meta-analytic assessment of surrogate outcomes Biostatistics 1 231 246 (Pubitemid 33213533)
60. H.C. van Houwelingen L.R. Arends T. Stijnen 2002 Advanced methods in meta-analysis: multivariate approach and metaregression Stat Med 21 589 624 (Pubitemid 34141379)
61. A. Alonso G. Molenberghs 2007 Surrogate marker evaluation from an information theory perspective Biometrics 63 180 186 (Pubitemid 46622694)
62. A. Tilahun A. Pryseley A. Alonso 2008 Information theory-based surrogate marker evaluation from several randomized clinical trials with binary endpoints, using SAS J Biopharm Stat 18 326 341
63. A. Alonso G. Molenberghs 2008 Evaluating time to cancer recurrence as a surrogate marker for survival from an information theory perspective Stat Methods Med Res 17 497 504
64. A. Pryseley A. Tilahun A. Alonso 2007 Information-theory based surrogate marker evaluation from several randomized clinical trials with continuous true and binary surrogate endpoints Clin Trials 4 587 597
65. D.J. Sargent H.S. Wieand D.G. Haller 2005 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 23 8664 8670 (Pubitemid 46211509)
66. D.J. Sargent S. Patiyil G. Yothers 2007 End points for colon cancer adjuvant trials: observations and recommendations based on individual patient data from 20 898 patients enrolled onto 18 randomized trials from the ACCENT Group J Clin Oncol 25 4569 4574 (Pubitemid 350035314)
67. S.G. Baker 2006 A simple meta-analytic approach for using a binary surrogate endpoint to predict the effect of intervention on true endpoint Biostatistics 7 58 70 (Pubitemid 43007181)
68. S.G. Baker 2008 Two simple approaches for validating a binary surrogate endpoint using data from multiple trials Stat Methods Med Res 17 505 514
69. E.L. Korn P.S. Albert L.M. McShane 2005 Assessing surrogates as trial endpoints using mixed models Stat Med 24 163 182 (Pubitemid 40124164)
70. J.C. Abrahantes Z. Shkedy G. Molenberghs 2008 Alternative methods to evaluate trial level surrogacy Clin Trials 5 194 208
71. T. Burzykowski M. Buyse 2006 Surrogate threshold effect: an alternative measure for meta-analytic surrogate endpoint validation Pharm Stat 5 173 186 (Pubitemid 44400217)
72. J.R. Johnson G. Williams R. Pazdur 2003 End points and United States Food and Drug Administration approval of oncology drugs J Clin Oncol 21 1404 1411 (Pubitemid 46606423)
73. R. Dagher J. Johnson G. Williams 2004 Accelerated approval of oncology products: a decade of experience J Natl Cancer Inst 96 1500 1509 (Pubitemid 39445531)
74. M. Buyse P. Thirion R.W. Carlson 2000 Relation between tumour response to first-line chemotherapy and survival in advanced colorectal cancer: a meta-analysis Lancet 356 373 378 (Pubitemid 30487493)
75. P.A. Tang S.M. Bentzen E.X. Chen 2007 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 25 4562 4568 (Pubitemid 350035313)
76. A. Hackshaw A. Knight P. Barrett-Lee 2005 Surrogate markers and survival in women receiving first-line combination anthracycline chemotherapy for advanced breast cancer Br J Cancer 93 1215 1221 (Pubitemid 41679406)
77. T. Burzykowski M. Buyse M.J. Piccart-Gebhart 2008 Evaluation of tumor response, disease control, progression-free survival, and time to progression as potential surrogate end points in metastatic breast cancer J Clin Oncol 26 1987 1992
78. T. Burzykowski M. Buyse G. Yothers 2008 Exploring and validating surrogate endpoints in colorectal cancer Lifetime Data Anal 14 54 64
79. M. Buyse T. Burzykowski K. Carroll 2007 Progression-free survival is a surrogate for survival in advanced colorectal cancer J Clin Oncol 25 5218 5224 (Pubitemid 350232253)
80. R.A. Miksad V. Zietemann R. Gothe 2008 Progression-free survival as a surrogate endpoint in advanced breast cancer Int J Technol Assess Health Care 24 371 383
81. M. Roessner R. De Wit I.F. Tannock 2005 Prostate-specific antigen (PSA) response as surrogate endpoint for overall survival (OS): analysis of the TAX 327 Study comparing docetaxel plus prednisone to mitoxantrone plus prednisone in advanced prostate cancer (abstract) J Clin Oncol 23 391s
82. A. Chakravarty R. Sridhara 2008 Use of progression-free survival as a surrogate marker in oncology trials: some regulatory issues Stat Methods Med Res 17 515 518
83. M.D. Hughes 2008 Practical issues arising in an exploratory analysis evaluating progression-free survival as a surrogate endpoint for overall survival in advanced colorectal cancer Stat Methods Med Res 17 487 495
84. J.H. Powers 2005 Microbiologic surrogate end points in clinical trials of infectious diseases: example of acute otitis media trials Pharmacotherapy 25 109S 123S (Pubitemid 41790084)
85. C.J. Punt M. Buyse C.H. Kohne 2007 Endpoints in adjuvant treatment trials: a systematic review of the literature in colon cancer and proposed definitions for future trials J Natl Cancer Inst 99 998 1003 (Pubitemid 47232601)
86. L.A. Stewart M.J. Clarke 1995 Practical methodology of meta-analyses (overviews) using updated individual patient data Cochrane Working Group. Stat Med 14 2057 2079
87. M. Packer J.R. Carver R.J. Rodeheffer 1991 Effect of oral milrinone on mortality in severe chronic heart failure. The PROMISE Study Research Group N Engl J Med 325 1468 1475
88. M. Packers J. Rouleau K. Swedberg 1993 Effect of Flosequinan on survival in chronic heart failure: Preliminary results of the PROFILE study (abstract) Circulation 88 I 301
89. R.M. Califf K.F. Adams W.J. McKenna 1997 A randomized controlled trial of epoprostenol therapy for severe congestive heart failure: The Flolan International Randomized Survival Trial (FIRST) Am Heart J 134 44 54 (Pubitemid 27329022)
90. S. Hulley D. Grady T. Bush 1998 Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/ progestin Replacement Study (HERS) Research Group JAMA 280 605 613
91. J.E. Rossouw G.L. Anderson R.L. Prentice 2002 Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial JAMA 288 321 333 (Pubitemid 34761611)
92. The Writing Group for the PEPI Trial 1995 Effects of estrogen or estrogen/progestin regimens on heart disease risk factors in postmenopausal women. The Postmenopausal Estrogen/Progestin Interventions (PEPI) Trial JAMA 273 199 208
93. Report of the Committee of Principal Investigators 1980 W.H.O. cooperative trial on primary prevention of ischaemic heart disease using clofibrate to lower serum cholesterol: mortality follow-up Lancet 2 379 385 (Pubitemid 14038716)
94. Gordon DJ (1994) Cholesterol lowering and total mortality. In: Contemporary issues in cholesterol lowering: clinical and population aspects. Marcel Dekker, New York
95. B.L. Riggs S.F. Hodgson W.M. O'Fallon 1990 Effect of fluoride treatment on the fracture rate in postmenopausal women with osteoporosis N Engl J Med 322 802 8029 (Pubitemid 20094143)
96. J.P. Aboulker A.M. Swart C.C. Committee 1993 Preliminary analysis of the Concorde trial Lancet 341 889 890 (Pubitemid 23094533)
97. S.G. Baker G. Izmirlian V. Kipnis 2005 Resolving paradoxes involving surrogate end points J R Stat Soc Ser A Stat Soc 168 753 762 (Pubitemid 41452731)
98. D. Renard H. Geys G. Molenberghs 2002 Validation of surrogate endpoints in multiple randomized clinical trials with discrete outcomes Biom J 44 921 935 (Pubitemid 36046930)
99. G. Molenberghs H. Geys M. Buyse 2001 Evaluation of surrogate endpoints in randomized experiments with mixed discrete and continuous outcomes Stat Med 20 3023 3038 (Pubitemid 32982526)
100. T. Burzykowski G. Molenberghs M. Buyse 2004 The validation of surrogate end points by using data from randomized clinical trials: a case-study in advanced colorectal cancer J R Stat Soc Ser A Stat Soc 167 103 124 (Pubitemid 38341448)
101. T. Burzykowski G. Molenberghs M. Buyse 2001 Validation of surrogate end points in multiple randomized clinical trials with failure time end points J Appl Stat 50 405 422 (Pubitemid 33348800)
102. D. Renard H. Geys G. Molenberghs 2002 Validation of longitudinally measured surrogate marker for a time-to-event endpoint J Appl Stat 30 235 247
103. Buyse M, Vangeneugden T, Bijnens L, et al. (2003) Validation of biomarkers as surrogates for clinical endpoints. Marcel Dekker, New York
104. D. Newling K. Carroll T. Morris 2004 Is prostate-specific antigen progression a surrogate for objective clinical progression in early prostate cancer? (abstract) J Clin Oncol 22 4652
105. L. Collette T. Burzykowski K.J. Carroll 2005 Is prostate-specific antigen a valid surrogate end point for survival in hormonally treated patients with metastatic prostate cancer? Joint research of the European Organisation for Research and Treatment of Cancer, the Limburgs Universitair Centrum, and AstraZeneca Pharmaceuticals J Clin Oncol 23 6139 6148 (Pubitemid 46300232)