Journal of Clinical Oncology, Vol 1, 710-719, Copyright © 1983 by American Society of Clinical Oncology

ARTICLES

Analysis of survival by tumor response

JR Anderson, KC Cain and RD Gelber

The common practice of comparing the survival of responders and nonresponders when reporting the results of cancer chemotherapy treatment is investigated. The usual method of comparing responders and nonresponders is biased in favor of responders, and these results are frequently misinterpreted as providing evidence that response prolongs survival, or that the treatment under study is effective. Two valid methods for comparing responders and nonresponders are discussed and recommendations are made concerning the analysis of survival by response. A comparison of survival by response category may be useful descriptively, but such a comparison should not be used for inference concerning treatment effectiveness.

Related Article

• Analysis of Survival by Tumor Response and Other Comparisons of Time-to-Event by Outcome Variables
  James R. Anderson, Kevin C. Cain, and Richard D. Gelber
  JCO 2008 26: 3913-3915 [Full Text]

This article has been cited by other articles:

				A. A. Tarhini, J. Stuckert, S. Lee, C. Sander, and J. M. Kirkwood Prognostic Significance of Serum S100B Protein in High-Risk Surgically Resected Melanoma Patients Participating in Intergroup Trial ECOG 1694 J. Clin. Oncol., January 1, 2009; 27(1): 38 - 44. [Abstract] [Full Text] [PDF]

				H. Wilke, R. Glynne-Jones, J. Thaler, A. Adenis, P. Preusser, E. A. Aguilar, M. S. Aapro, R. Esser, A. H. Loos, and S. Siena Cetuximab Plus Irinotecan in Heavily Pretreated Metastatic Colorectal Cancer Progressing on Irinotecan: MABEL Study J. Clin. Oncol., November 20, 2008; 26(33): 5335 - 5343. [Abstract] [Full Text] [PDF]

				D.-W. Park, S.-C. Yun, S.-W. Lee, Y.-H. Kim, C. W. Lee, M.-K. Hong, S.-S. Cheong, J.-J. Kim, S.-W. Park, and S.-J. Park Stent Thrombosis, Clinical Events, and Influence of Prolonged Clopidogrel Use After Placement of Drug-Eluting Stent: Data From an Observational Cohort Study of Drug-Eluting Versus Bare-Metal Stents J. Am. Coll. Cardiol. Intv., October 1, 2008; 1(5): 494 - 503. [Abstract] [Full Text] [PDF]

				J. K. Salama, K. M. Stenson, E. O. Kistner, B. B. Mittal, A. Argiris, M. E. Witt, F. Rosen, B. E. Brockstein, E. E. W. Cohen, D. J. Haraf, et al. Induction chemotherapy and concurrent chemoradiotherapy for locoregionally advanced head and neck cancer: a multi-institutional phase II trial investigating three radiotherapy dose levels Ann. Onc., October 1, 2008; 19(10): 1787 - 1794. [Abstract] [Full Text] [PDF]

				C. E. Buller, Y. Fu, K. W. Mahaffey, T. G. Todaro, P. Adams, C. M. Westerhout, H. D. White, A. W.J. van 't Hof, F. J. Van de Werf, G. S. Wagner, et al. ST-Segment Recovery and Outcome After Primary Percutaneous Coronary Intervention for ST-Elevation Myocardial Infarction: Insights From the Assessment of Pexelizumab in Acute Myocardial Infarction (APEX-AMI) Trial Circulation, September 23, 2008; 118(13): 1335 - 1346. [Abstract] [Full Text] [PDF]

				J. R. Anderson, K. C. Cain, and R. D. Gelber Analysis of Survival by Tumor Response and Other Comparisons of Time-to-Event by Outcome Variables J. Clin. Oncol., August 20, 2008; 26(24): 3913 - 3915. [Full Text] [PDF]

				M. Y. Chan, K. W. Mahaffey, L. J. Sun, K. S. Pieper, H. D. White, P. E. Aylward, J. J. Ferguson, R. M. Califf, and M. T. Roe Prevalence, Predictors, and Impact of Conservative Medical Management for Patients With Non-ST-Segment Elevation Acute Coronary Syndromes Who Have Angiographically Documented Significant Coronary Disease J. Am. Coll. Cardiol. Intv., August 1, 2008; 1(4): 369 - 378. [Abstract] [Full Text] [PDF]

				A. Cremonesi, C. Setacci, F. Castriota, and M. Valgimigli Carotid Stent Cell Design: Lack of Benefit or Lack of Evidence? Stroke, August 1, 2008; 39(8): e130 - e130. [Full Text] [PDF]

				E. M. Antman, S. D. Wiviott, S. A. Murphy, J. Voitk, Y. Hasin, P. Widimsky, H. Chandna, W. Macias, C. H. McCabe, and E. Braunwald Early and Late Benefits of Prasugrel in Patients With Acute Coronary Syndromes Undergoing Percutaneous Coronary Intervention: A TRITON-TIMI 38 (TRial to Assess Improvement in Therapeutic Outcomes by Optimizing Platelet InhibitioN with Prasugrel-Thrombolysis In Myocardial Infarction) Analysis J. Am. Coll. Cardiol., May 27, 2008; 51(21): 2028 - 2033. [Abstract] [Full Text] [PDF]

				D. R. Berthold, G. R. Pond, M. Roessner, R. de Wit, M. Eisenberger, a. I. F. Tannock, and on behalf of the TAX-327 investigators Treatment of Hormone-Refractory Prostate Cancer with Docetaxel or Mitoxantrone: Relationships between Prostate-Specific Antigen, Pain, and Quality of Life Response and Survival in the TAX-327 Study Clin. Cancer Res., May 1, 2008; 14(9): 2763 - 2767. [Abstract] [Full Text] [PDF]

				P. N. Lara Jr, M. W. Redman, K. Kelly, M. J. Edelman, S. K. Williamson, J. J. Crowley, and D. R. Gandara Disease Control Rate at 8 Weeks Predicts Clinical Benefit in Advanced Non-Small-Cell Lung Cancer: Results From Southwest Oncology Group Randomized Trials J. Clin. Oncol., January 20, 2008; 26(3): 463 - 467. [Abstract] [Full Text] [PDF]

				S.-L. T. Normand Evaluating the Optimal Timing of Angiography: Landmark or off the Mark? Circulation, December 4, 2007; 116(23): 2656 - 2657. [Full Text] [PDF]

				P. Tricoci, Y. Lokhnygina, L. G. Berdan, S. R. Steinhubl, D. C. Gulba, H. D. White, N. S. Kleiman, P. E. Aylward, A. Langer, R. M. Califf, et al. Time to Coronary Angiography and Outcomes Among Patients With High-Risk Non ST-Segment Elevation Acute Coronary Syndromes: Results From the SYNERGY Trial Circulation, December 4, 2007; 116(23): 2669 - 2677. [Abstract] [Full Text] [PDF]

				C. L. Slingluff Jr., G. R. Petroni, K. A. Chianese-Bullock, M. E. Smolkin, S. Hibbitts, C. Murphy, N. Johansen, W. W. Grosh, G. V. Yamshchikov, P. Y. Neese, et al. Immunologic and Clinical Outcomes of a Randomized Phase II Trial of Two Multipeptide Vaccines for Melanoma in the Adjuvant Setting Clin. Cancer Res., November 1, 2007; 13(21): 6386 - 6395. [Abstract] [Full Text] [PDF]

				L. H. Curtis, S. M. Al-Khatib, A. M. Shea, B. G. Hammill, A. F. Hernandez, and K. A. Schulman Sex Differences in the Use of Implantable Cardioverter-Defibrillators for Primary and Secondary Prevention of Sudden Cardiac Death JAMA, October 3, 2007; 298(13): 1517 - 1524. [Abstract] [Full Text] [PDF]

				A. Palumbo, M. T. Ambrosini, G. Benevolo, P. Pregno, N. Pescosta, V. Callea, C. Cangialosi, T. Caravita, F. Morabito, P. Musto, et al. Bortezomib, melphalan, prednisone, and thalidomide for relapsed multiple myeloma Blood, April 1, 2007; 109(7): 2767 - 2772. [Abstract] [Full Text] [PDF]

				B. Lagerqvist, S. K. James, U. Stenestrand, J. Lindback, T. Nilsson, L. Wallentin, and the SCAAR Study Group Long-Term Outcomes with Drug-Eluting Stents versus Bare-Metal Stents in Sweden N. Engl. J. Med., March 8, 2007; 356(10): 1009 - 1019. [Abstract] [Full Text] [PDF]

				E. L. Eisenstein, K. J. Anstrom, D. F. Kong, L. K. Shaw, R. H. Tuttle, D. B. Mark, J. M. Kramer, R. A. Harrington, D. B. Matchar, D. E. Kandzari, et al. Clopidogrel Use and Long-term Clinical Outcomes After Drug-Eluting Stent Implantation JAMA, January 10, 2007; 297(2): 159 - 168. [Abstract] [Full Text] [PDF]

				G. T. Budd, M. Cristofanilli, M. J. Ellis, A. Stopeck, E. Borden, M. C. Miller, J. Matera, M. Repollet, G. V. Doyle, L. W.M.M. Terstappen, et al. Circulating Tumor Cells versus Imaging--Predicting Overall Survival in Metastatic Breast Cancer. Clin. Cancer Res., November 1, 2006; 12(21): 6403 - 6409. [Abstract] [Full Text] [PDF]

				G. D. Shah, S. Kesari, R. Xu, T. T. Batchelor, A. M. O'Neill, F. H. Hochberg, B. Levy, J. Bradshaw, and P. Y. Wen Comparison of linear and volumetric criteria in assessing tumor response in adult high-grade gliomas Neuro-oncol, January 1, 2006; 8(1): 38 - 46. [Abstract] [Full Text] [PDF]

				J. L. Ramirez, R. Rosell, M. Taron, M. Sanchez-Ronco, V. Alberola, R. de las Penas, J. M. Sanchez, T. Moran, C. Camps, B. Massuti, et al. 14-3-3{sigma} Methylation in Pretreatment Serum Circulating DNA of Cisplatin-Plus-Gemcitabine-Treated Advanced Non-Small-Cell Lung Cancer Patients Predicts Survival: The Spanish Lung Cancer Group J. Clin. Oncol., December 20, 2005; 23(36): 9105 - 9112. [Abstract] [Full Text] [PDF]

				P. Rietschel, K. S. Panageas, C. Hanlon, A. Patel, D. H. Abramson, and P. B. Chapman Variates of Survival in Metastatic Uveal Melanoma J. Clin. Oncol., November 1, 2005; 23(31): 8076 - 8080. [Abstract] [Full Text] [PDF]

				J. R. Anderson and D. S. Neuberg Analysis of Outcome by Response Flawed J. Clin. Oncol., November 1, 2005; 23(31): 8122 - 8123. [Full Text] [PDF]

				K. Hotta, K. Matsuo, H. Ueoka, K. Kiura, M. Tabata, S. Harita, K. Gemba, T. Yonei, A. Bessho, and M. Tanimoto Continued gefitinib treatment after disease stabilisation prolongs survival of Japanese patients with non-small-cell lung cancer: Okayama Lung Cancer Study Group experience Ann. Onc., November 1, 2005; 16(11): 1817 - 1823. [Abstract] [Full Text] [PDF]

				P. Bruzzi, L. Del Mastro, M. P. Sormani, L. Bastholt, M. Danova, C. Focan, G. Fountzilas, J. Paul, R. Rosso, and M. Venturini Objective Response to Chemotherapy As a Potential Surrogate End Point of Survival in Metastatic Breast Cancer Patients J. Clin. Oncol., August 1, 2005; 23(22): 5117 - 5125. [Abstract] [Full Text] [PDF]

				P Kaul, L K Newby, Y Fu, D B Mark, S G Goodman, G S Wagner, R A Harrington, C B Granger, F Van de Werf, E M Ohman, et al. Relation between baseline risk and treatment decisions in non-ST elevation acute coronary syndromes: an examination of international practice patterns Heart, July 1, 2005; 91(7): 876 - 881. [Abstract] [Full Text] [PDF]

				G. Bonadonna, A. Moliterni, M. Zambetti, M. G. Daidone, S. Pilotti, L. Gianni, and P. Valagussa 30 years' follow up of randomised studies of adjuvant CMF in operable breast cancer: cohort study BMJ, January 29, 2005; 330(7485): 217. [Abstract] [Full Text] [PDF]

				B. Gronlund, C. Hogdall, J. Hilden, S. A. Engelholm, E. V.S. Hogdall, and H. H. Hansen Should CA-125 Response Criteria Be Preferred to Response Evaluation Criteria in Solid Tumors (RECIST) for Prognostication During Second-Line Chemotherapy of Ovarian Carcinoma? J. Clin. Oncol., October 15, 2004; 22(20): 4051 - 4058. [Abstract] [Full Text] [PDF]

				S. V. Rao, J. G. Jollis, R. A. Harrington, C. B. Granger, L. K. Newby, P. W. Armstrong, D. J. Moliterno, L. Lindblad, K. Pieper, E. J. Topol, et al. Relationship of Blood Transfusion and Clinical Outcomes in Patients With Acute Coronary Syndromes JAMA, October 6, 2004; 292(13): 1555 - 1562. [Abstract] [Full Text] [PDF]

				G. Molenberghs, T. Burzykowski, A. Alonso, and M. Buyse A perspective on surrogate endpoints in controlled clinical trials Statistical Methods in Medical Research, June 1, 2004; 13(3): 177 - 206. [Abstract] [PDF]

				B. G.M. Durie, J. Jacobson, B. Barlogie, and J. Crowley Magnitude of Response With Myeloma Frontline Therapy Does Not Predict Outcome: Importance of Time to Progression in Southwest Oncology Group Chemotherapy Trials J. Clin. Oncol., May 15, 2004; 22(10): 1857 - 1863. [Abstract] [Full Text] [PDF]

				C. M. van Herpen, M. Looman, M. Zonneveld, N. Scharenborg, P. C. de Wilde, L. van de Locht, M. A. W. Merkx, G. J. Adema, and P. H. De Mulder Intratumoral Administration of Recombinant Human Interleukin 12 in Head and Neck Squamous Cell Carcinoma Patients Elicits a T-Helper 1 Profile in the Locoregional Lymph Nodes Clin. Cancer Res., April 15, 2004; 10(8): 2626 - 2635. [Abstract] [Full Text] [PDF]

				E. J. Small, S. Halabi, N. A. Dawson, W. M. Stadler, B. I. Rini, J. Picus, P. Gable, F. M. Torti, E. Kaplan, and N. J. Vogelzang Antiandrogen Withdrawal Alone or in Combination With Ketoconazole in Androgen-Independent Prostate Cancer Patients: A Phase III Trial (CALGB 9583) J. Clin. Oncol., March 15, 2004; 22(6): 1025 - 1033. [Abstract] [Full Text] [PDF]

				V. A. Miller, M. G. Kris, N. Shah, J. Patel, C. Azzoli, J. Gomez, L. M. Krug, W. Pao, N. Rizvi, B. Pizzo, et al. Bronchioloalveolar Pathologic Subtype and Smoking History Predict Sensitivity to Gefitinib in Advanced Non-Small-Cell Lung Cancer J. Clin. Oncol., March 15, 2004; 22(6): 1103 - 1109. [Abstract] [Full Text] [PDF]

				K. Izutsu, Y. Kanda, H. Ohno, H. Sao, H. Ogawa, Y. Miyazaki, K. Kawa, Y. Kodera, S. Kato, Y. Morishima, et al. Unrelated bone marrow transplantation for non-Hodgkin lymphoma: a study from the Japan Marrow Donor Program Blood, March 1, 2004; 103(5): 1955 - 1960. [Abstract] [Full Text] [PDF]

				R. C. Kane, P. F. Bross, A. T. Farrell, and R. Pazdur Velcade(R): U.S. FDA Approval for the Treatment of Multiple Myeloma Progressing on Prior Therapy Oncologist, December 1, 2003; 8(6): 508 - 513. [Abstract] [Full Text] [PDF]

				M. Gupta, W.-C. Chang, F. Van de Werf, C. B. Granger, W. Midodzi, G. Barbash, K. Pehrson, A. Oto, P. Toutouzas, P. Jansky, et al. International differences in in-hospital revascularization and outcomes following acute myocardial infarction: A multilevel analysis of patients in ASSENT-2 Eur. Heart J., September 2, 2003; 24(18): 1640 - 1650. [Abstract] [Full Text] [PDF]

				W.-J. Hwu, S. E. Krown, J. H. Menell, K. S. Panageas, J. Merrell, L. A. Lamb, L. J. Williams, C. J. Quinn, T. Foster, P. B. Chapman, et al. Phase II Study of Temozolomide Plus Thalidomide for the Treatment of Metastatic Melanoma J. Clin. Oncol., September 1, 2003; 21(17): 3351 - 3356. [Abstract] [Full Text] [PDF]

				A. M. Tsimberidou, P. McLaughlin, A. Younes, M. A. Rodriguez, F. B. Hagemeister, A. Sarris, J. Romaguera, M. Hess, T. L. Smith, Y. Yang, et al. Fludarabine, mitoxantrone, dexamethasone (FND) compared with an alternating triple therapy (ATT) regimen in patients with stage IV indolent lymphoma Blood, December 15, 2002; 100(13): 4351 - 4357. [Abstract] [Full Text] [PDF]

				M. Mohty, M. Kuentz, M. Michallet, J.-H. Bourhis, N. Milpied, L. Sutton, J.-P. Jouet, M. Attal, P. Bordigoni, J.-Y. Cahn, et al. Chronic graft-versus-host disease after allogeneic blood stem cell transplantation: long-term results of a randomized study Blood, October 16, 2002; 100(9): 3128 - 3134. [Abstract] [Full Text] [PDF]

				M. Nottage and L. L. Siu Principles of Clinical Trial Design J. Clin. Oncol., September 15, 2002; 20(90001): 42s - 46. [Full Text] [PDF]

				E. J. Small, S. Halabi, M. J. Ratain, G. Rosner, W. Stadler, D. Palchak, E. Marshall, R. Rago, V. Hars, G. Wilding, et al. Randomized Study of Three Different Doses of Suramin Administered With a Fixed Dosing Schedule in Patients With Advanced Prostate Cancer: Results of Intergroup 0159, Cancer and Leukemia Group B 9480 J. Clin. Oncol., August 15, 2002; 20(16): 3369 - 3375. [Abstract] [Full Text] [PDF]

				C.-M. Wendtner, S. Abdel-Rahman, M. Krych, J. Baumert, L. H. Lindner, A. Baur, W. Hiddemann, and R. D. Issels Response to Neoadjuvant Chemotherapy Combined With Regional Hyperthermia Predicts Long-Term Survival for Adult Patients With Retroperitoneal and Visceral High-Risk Soft Tissue Sarcomas J. Clin. Oncol., July 15, 2002; 20(14): 3156 - 3164. [Abstract] [Full Text] [PDF]

				H. M. Kantarjian, S. O'Brien, J. E. Cortes, T. L. Smith, M. B. Rios, J. Shan, Y. Yang, F. J. Giles, D. A. Thomas, S. Faderl, et al. Treatment of Philadelphia Chromosome-positive, Accelerated-phase Chronic Myelogenous Leukemia with Imatinib Mesylate Clin. Cancer Res., July 1, 2002; 8(7): 2167 - 2176. [Abstract] [Full Text] [PDF]

				H. M. Kantarjian, M. Talpaz, S. O'Brien, T. L. Smith, F. J. Giles, S. Faderl, D. A. Thomas, G. Garcia-Manero, J.-P. J. Issa, M. Andreeff, et al. Imatinib Mesylate for Philadelphia Chromosome-positive, Chronic-Phase Myeloid Leukemia after Failure of Interferon-{alpha}: Follow-Up Results Clin. Cancer Res., July 1, 2002; 8(7): 2177 - 2187. [Abstract] [Full Text] [PDF]

				H. M. Kantarjian, J. Cortes, S. O'Brien, F. J. Giles, M. Albitar, M. B. Rios, J. Shan, S. Faderl, G. Garcia-Manero, D. A. Thomas, et al. Imatinib mesylate (STI571) therapy for Philadelphia chromosome-positive chronic myelogenous leukemia in blast phase Blood, May 15, 2002; 99(10): 3547 - 3553. [Abstract] [Full Text] [PDF]

				E. J. Small, A. McMillan, M. Meyer, L. Chen, W. J. Slichenmyer, P. F. Lenehan, and M. Eisenberger Serum Prostate-Specific Antigen Decline as a Marker of Clinical Outcome in Hormone-Refractory Prostate Cancer Patients: Association With Progression-Free Survival, Pain End Points, and Survival J. Clin. Oncol., March 1, 2001; 19(5): 1304 - 1311. [Abstract] [Full Text] [PDF]

				K. Takayasu, Y. Muramatsu, T. Maeda, R. Iwata, H. Furukawa, Y. Muramatsu, N. Moriyama, T. Okusaka, S. Okada, and H. Ueno Targeted Transarterial Oily Chemoembolization for Small Foci of Hepatocellular Carcinoma Using a Unified Helical CT and Angiography system: Analysis of Factors Affecting Local Recurrence and Survival rates Am. J. Roentgenol., March 1, 2001; 176(3): 681 - 688. [Abstract] [Full Text] [PDF]

				L. B. Silverman, R. D. Gelber, V. K. Dalton, B. L. Asselin, R. D. Barr, L. A. Clavell, C. A. Hurwitz, A. Moghrabi, Y. Samson, M. A. Schorin, et al. Improved outcome for children with acute lymphoblastic leukemia: results of Dana-Farber Consortium Protocol 91-01 Blood, March 1, 2001; 97(5): 1211 - 1218. [Abstract] [Full Text] [PDF]

				R. J. Packer, J. M. Boyett, A. J. Janss, T. Stavrou, L. Kun, J. Wisoff, C. Russo, R. Geyer, P. Phillips, M. Kieran, et al. Growth Hormone Replacement Therapy in Children With Medulloblastoma: Use and Effect on Tumor Control J. Clin. Oncol., January 15, 2001; 19(2): 480 - 487. [Abstract] [Full Text] [PDF]

				Pauline de La Salmonière, J.-J. Grob, B. Dreno, M. Delaunay, and C. Chastang White Blood Cell Count: A Prognostic Factor and Possible Subset Indicator of Optimal Treatment with Low-Dose Adjuvant Interferon in Primary Melanoma Clin. Cancer Res., December 1, 2000; 6(12): 4713 - 4718. [Abstract] [Full Text]

				A. Josting, U. Rueffer, J. Franklin, M. Sieber, V. Diehl, and A. Engert Prognostic factors and treatment outcome in primary progressive Hodgkin lymphoma: a report from the German Hodgkin Lymphoma Study Group Blood, August 15, 2000; 96(4): 1280 - 1286. [Abstract] [Full Text] [PDF]

				W. A. Peters III, P. Y. Liu, R. J. Barrett II, R. J. Stock, B. J. Monk, J. S. Berek, L. Souhami, P. Grigsby, W. Gordon Jr, and D. S. Alberts Concurrent Chemotherapy and Pelvic Radiation Therapy Compared With Pelvic Radiation Therapy Alone as Adjuvant Therapy After Radical Surgery in High-Risk Early-Stage Cancer of the Cervix J. Clin. Oncol., April 1, 2000; 18(8): 1606 - 1613. [Abstract] [Full Text] [PDF]

				R. M. Lemoli, G. Martinelli, E. Zamagni, M. R. Motta, S. Rizzi, C. Terragna, R. Rondelli, S. Ronconi, A. Curti, F. Bonifazi, et al. Engraftment, clinical, and molecular follow-up of patients with multiple myeloma who were reinfused with highly purified CD34+ cells to support single or tandem high-dose chemotherapy Blood, April 1, 2000; 95(7): 2234 - 2239. [Abstract] [Full Text] [PDF]

				D. Blaise, M. Kuentz, C. Fortanier, J. H. Bourhis, N. Milpied, L. Sutton, J.-P. Jouet, M. Attal, P. Bordigoni, J.-Y. Cahn, et al. Randomized Trial of Bone Marrow Versus Lenograstim-Primed Blood Cell Allogeneic Transplantation in Patients With Early-Stage Leukemia: A Report From the Societe Francaise de Greffe de Moelle J. Clin. Oncol., February 1, 2000; 18(3): 537 - 537. [Abstract] [Full Text] [PDF]