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Optimized Image-Based Surrogate Endpoints in Targeted Therapies for Glioblastoma: A Systematic Review and Meta-Analysis of Phase III Randomized Controlled Trials

  • Chong Hyun Suh (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Ho Sung Kim (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Seung Chai Jung (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Choong Gon Choi (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Sang Joon Kim (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Kyung Won Kim (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center)
  • 투고 : 2019.11.09
  • 심사 : 2019.12.19
  • 발행 : 2020.04.01

초록

Objective: We aimed to determine the optimized image-based surrogate endpoints (IBSEs) in targeted therapies for glioblastoma through a systematic review and meta-analysis of phase III randomized controlled trials (RCTs). Materials and Methods: A systematic search of OVID-MEDLINE and EMBASE for phase III RCTs on glioblastoma was performed in December 2017. Data on overall survival (OS) and IBSEs, including progression-free survival (PFS), 6-month PFS (6moPFS), 12-month PFS (12moPFS), median PFS, and objective response rate (ORR) were extracted. Weighted linear regression analysis for the hazard ratio for OS and the hazard ratios or odds ratios for IBSEs was performed. The associations between IBSEs and OS were evaluated. Subgroup analyses according to disease stage (newly diagnosed glioblastoma versus recurrent glioblastoma), types of test treatment, and types of response assessment criteria were performed. Results: Twenty-three phase III RCTs published between 2000 and 2017, including 8387 patients, met the inclusion criteria. OS showed strong correlations with PFS (standardized β coefficient [R] = 0.719), 6moPFS (R = 0.647), and 12moPFS (R = 0.638). OS showed no correlations with median PFS and ORR. In subgroup analysis according to types of therapies, PFS showed the highest correlations with OS in targeted therapies for cell cycle pathways (R = 0.913) and growth factor receptors and their downstream pathways (R = 0.962). 12moPFS showed the highest correlation with OS in antiangiogenic therapy (R = 0.821). The response assessment in neuro-oncology criteria provided higher correlation coefficients between OS and IBSEs than the Macdonald criteria. Conclusion: Overall, PFS is an optimized IBSE in targeted therapies for glioblastoma; however, 12moPFS is optimal in antiangiogenic therapy.

키워드

과제정보

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (grant number: NRF-2017R1A2A2A05001217).

참고문헌

  1. Barchana M, Margaliot M, Liphshitz I. Changes in brain glioma incidence and laterality correlates with use of mobile phones- -a nationwide population based study in Israel. Asian Pac J Cancer Prev 2012;13:5857-5863 https://doi.org/10.7314/APJCP.2012.13.11.5857
  2. Martell RE, Sermer D, Getz K, Kaitin KI. Oncology drug development and approval of systemic anticancer therapy by the U.S. Food and Drug Administration. Oncologist 2013;18:104-111 https://doi.org/10.1634/theoncologist.2012-0235
  3. Batchelor TT, Mulholland P, Neyns B, Nabors LB, Campone M, Wick A, et al. Phase III randomized trial comparing the efficacy of cediranib as monotherapy, and in combination with lomustine, versus lomustine alone in patients with recurrent glioblastoma. J Clin Oncol 2013;31:3212-3218 https://doi.org/10.1200/JCO.2012.47.2464
  4. Blumenthal DT, Rankin C, Stelzer KJ, Spence AM, Sloan AE, Moore DF Jr, et al. A Phase III study of radiation therapy (RT) and O6-benzylguanine + BCNU versus RT and BCNU alone and methylation status in newly diagnosed glioblastoma and gliosarcoma: Southwest Oncology Group (SWOG) study S0001. Int J Clin Oncol 2015;20:650-658 https://doi.org/10.1007/s10147-014-0769-0
  5. Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 2014;370:709-722 https://doi.org/10.1056/NEJMoa1308345
  6. Dresemann G, Weller M, Rosenthal MA, Wedding U, Wagner W, Engel E, et al. Imatinib in combination with hydroxyurea versus hydroxyurea alone as oral therapy in patients with progressive pretreated glioblastoma resistant to standard dose temozolomide. J Neurooncol 2010;96:393-402 https://doi.org/10.1007/s11060-009-9976-3
  7. Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med 2014;370:699-708 https://doi.org/10.1056/NEJMoa1308573
  8. Gilbert MR, Wang M, Aldape KD, Stupp R, Hegi ME, Jaeckle KA, et al. Dose-dense temozolomide for newly diagnosed glioblastoma: a randomized phase III clinical trial. J Clin Oncol 2013;31:4085-4091 https://doi.org/10.1200/JCO.2013.49.6968
  9. Kim IH, Park CK, Heo DS, Kim CY, Rhee CH, Nam DH, et al. Radiotherapy followed by adjuvant temozolomide with or without neoadjuvant ACNU-CDDP chemotherapy in newly diagnosed glioblastomas: a prospective randomized controlled multicenter phase III trial. J Neurooncol 2011;103:595-602 https://doi.org/10.1007/s11060-010-0427-y
  10. Kong DS, Nam DH, Kang SH, Lee JW, Chang JH, Kim JH, et al. Phase III randomized trial of autologous cytokine-induced killer cell immunotherapy for newly diagnosed glioblastoma in Korea. Oncotarget 2017;8:7003-7013 https://doi.org/10.18632/oncotarget.12273
  11. Levin VA, Uhm JH, Jaeckle KA, Choucair A, Flynn PJ, Yung WKA, et al. Phase III randomized study of postradiotherapy chemotherapy with alpha-difluoromethylornithine-procarbazine, N-(2-chloroethyl)-N'-cyclohexyl-N-nitrosurea, vincristine (DFMO-PCV) versus PCV for glioblastoma multiforme. Clin Cancer Res 2000;6:3878-3884
  12. Malmstrom A, Gronberg BH, Marosi C, Stupp R, Frappaz D, Schultz H, et al. Temozolomide versus standard 6-week radiotherapy versus hypofractionated radiotherapy in patients older than 60 years with glioblastoma: the Nordic randomised, phase 3 trial. Lancet Oncol 2012;13:916-926 https://doi.org/10.1016/S1470-2045(12)70265-6
  13. Perry JR, Laperriere N, O'Callaghan CJ, Brandes AA, Menten J, Phillips C, et al. Short-course radiation plus temozolomide in elderly patients with glioblastoma. N Engl J Med 2017;376:1027-1037 https://doi.org/10.1056/NEJMoa1611977
  14. Prados MD, Wara WM, Sneed PK, McDermott M, Chang SM, Rabbitt J, et al. Phase III trial of accelerated hyperfractionation with or without difluromethylornithine (DFMO) versus standard fractionated radiotherapy with or without DFMO for newly diagnosed patients with glioblastoma multiforme. Int J Radiat Oncol Biol Phys 2001;49:71-77 https://doi.org/10.1016/S0360-3016(00)01458-9
  15. Rainov NG. A phase III clinical evaluation of herpes simplex virus type 1 thymidine kinase and ganciclovir gene therapy as an adjuvant to surgical resection and radiation in adults with previously untreated glioblastoma multiforme. Hum Gene Ther 2000;11:2389-2401 https://doi.org/10.1089/104303400750038499
  16. Roa W, Kepka L, Kumar N, Sinaika V, Matiello J, Lomidze D, et al. International Atomic Energy Agency randomized phase III study of radiation therapy in elderly and/or frail patients with newly diagnosed glioblastoma multiforme. J Clin Oncol 2015;33:4145-4150 https://doi.org/10.1200/JCO.2015.62.6606
  17. Stupp R, Hegi ME, Gorlia T, Erridge SC, Perry J, Hong YK, et al. Cilengitide combined with standard treatment for patients with newly diagnosed glioblastoma with methylated MGMT promoter (CENTRIC EORTC 26071-22072 study): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol 2014;15:1100-1108 https://doi.org/10.1016/S1470-2045(14)70379-1
  18. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-996 https://doi.org/10.1056/NEJMoa043330
  19. Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA, et al. Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: a randomized clinical trial. JAMA 2015;314:2535-2543 https://doi.org/10.1001/jama.2015.16669
  20. Stupp R, Wong ET, Kanner AA, Steinberg D, Engelhard H, Heidecke V, et al. NovoTTF-100A versus physician's choice chemotherapy in recurrent glioblastoma: a randomised phase III trial of a novel treatment modality. Eur J Cancer 2012;48:2192-2202 https://doi.org/10.1016/j.ejca.2012.04.011
  21. Weller M, Butowski N, Tran DD, Recht LD, Lim M, Hirte H, et al. Rindopepimut with temozolomide for patients with newly diagnosed, EGFRvIII-expressing glioblastoma (ACT IV): a randomised, double-blind, international phase 3 trial. Lancet Oncol 2017;18:1373-1385 https://doi.org/10.1016/S1470-2045(17)30517-X
  22. Westphal M, Heese O, Steinbach JP, Schnell O, Schackert G, Mehdorn M, et al. A randomised, open label phase III trial with nimotuzumab, an anti-epidermal growth factor receptor monoclonal antibody in the treatment of newly diagnosed adult glioblastoma. Eur J Cancer 2015;51:522-532 https://doi.org/10.1016/j.ejca.2014.12.019
  23. Westphal M, Yla-Herttuala S, Martin J, Warnke P, Menei P, Eckland D, et al. Adenovirus-mediated gene therapy with sitimagene ceradenovec followed by intravenous ganciclovir for patients with operable high-grade glioma (ASPECT): a randomised, open-label, phase 3 trial. Lancet Oncol 2013;14:823-833 https://doi.org/10.1016/S1470-2045(13)70274-2
  24. Wick W, Gorlia T, Bendszus M, Taphoorn M, Sahm F, Harting I, et al. Lomustine and bevacizumab in progressive glioblastoma. N Engl J Med 2017;377:1954-1963 https://doi.org/10.1056/NEJMoa1707358
  25. Wick W, Puduvalli VK, Chamberlain MC, van den Bent MJ, Carpentier AF, Cher LM, et al. Phase III study of enzastaurin compared with lomustine in the treatment of recurrent intracranial glioblastoma. J Clin Oncol 2010;28:1168-1174 https://doi.org/10.1200/JCO.2009.23.2595
  26. Brandsma D, van den Bent MJ. Pseudoprogression and pseudoresponse in the treatment of gliomas. Curr Opin Neurol 2009;22:633-638 https://doi.org/10.1097/WCO.0b013e328332363e
  27. Wen PY, Chang SM, Van den Bent MJ, Vogelbaum MA, Macdonald DR, Lee EQ. Response assessment in neuro-oncology clinical trials. J Clin Oncol 2017;35:2439-2449 https://doi.org/10.1200/JCO.2017.72.7511
  28. Zhao F. Surrogate end points and their validation in oncology clinical trials. J Clin Oncol 2016;34:1436-1437 https://doi.org/10.1200/JCO.2016.66.4581
  29. Touat M, Idbaih A, Sanson M, Ligon KL. Glioblastoma targeted therapy: updated approaches from recent biological insights. Ann Oncol 2017;28:1457-1472 https://doi.org/10.1093/annonc/mdx106
  30. Burnand B, Kernan WN, Feinstein AR. Indexes and boundaries for "quantitative significance" in statistical decisions. J Clin Epidemiol 1990;43:1273-1284 https://doi.org/10.1016/0895-4356(90)90093-5
  31. Armstrong TS, Wefel JS, Wang M, Gilbert MR, Won M, Bottomley A, et al. Net clinical benefit analysis of radiation therapy oncology group 0525: a phase III trial comparing conventional adjuvant temozolomide with dose-intensive temozolomide in patients with newly diagnosed glioblastoma. J Clin Oncol 2013;31:4076-4084 https://doi.org/10.1200/JCO.2013.49.6067
  32. Mirimanoff RO, Gorlia T, Mason W, Van den Bent MJ, Kortmann RD, Fisher B, et al. Radiotherapy and temozolomide for newly diagnosed glioblastoma: recursive partitioning analysis of the EORTC 26981/22981-NCIC CE3 phase III randomized trial. J Clin Oncol 2006;24:2563-2569 https://doi.org/10.1200/JCO.2005.04.5963
  33. Taphoorn MJ, Henriksson R, Bottomley A, Cloughesy T, Wick W, Mason WP, et al. Health-related quality of life in a randomized phase III study of bevacizumab, temozolomide, and radiotherapy in newly diagnosed glioblastoma. J Clin Oncol 2015;33:2166-2175 https://doi.org/10.1200/JCO.2014.60.3217
  34. Kunwar S, Chang S, Westphal M, Vogelbaum M, Sampson J, Barnett G, et al. Phase III randomized trial of CED of IL13-PE38QQR vs Gliadel wafers for recurrent glioblastoma. Neuro Oncol 2010;12:871-881 https://doi.org/10.1093/neuonc/nop054
  35. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009;10:459-466 https://doi.org/10.1016/S1470-2045(09)70025-7
  36. Macdonald DR, Cascino TL, Schold SC Jr, Cairncross JG. Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 1990;8:1277-1280 https://doi.org/10.1200/JCO.1990.8.7.1277
  37. Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 2010;28:1963-1972 https://doi.org/10.1200/JCO.2009.26.3541
  38. Zer A, Prince RM, Amir E, Abdul Razak A. Evolution of randomized trials in advanced/metastatic soft tissue sarcoma: end point selection, surrogacy, and quality of reporting. J Clin Oncol 2016;34:1469-1475 https://doi.org/10.1200/JCO.2015.64.3437
  39. 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;26:5458-5464 https://doi.org/10.1200/JCO.2008.16.5456
  40. Foster NR, Renfro LA, Schild SE, Redman MW, Wang XF, Dahlberg SE, et al. Multitrial evaluation of progression-free survival as a surrogate end point for overall survival in first-line extensive-stage small-cell lung cancer. J Thorac Oncol 2015;10:1099-1106 https://doi.org/10.1097/JTO.0000000000000548
  41. Burzykowski T, Buyse M, Piccart-Gebhart MJ, Sledge G, Carmichael J, Luck HJ, et al. 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 2008;26:1987-1992 https://doi.org/10.1200/JCO.2007.10.8407
  42. Ballman KV, Buckner JC, Brown PD, Giannini C, Flynn PJ, LaPlant BR, et al. The relationship between six-month progression-free survival and 12-month overall survival end points for phase II trials in patients with glioblastoma multiforme. Neuro Oncol 2007;9:29-38 https://doi.org/10.1215/15228517-2006-025
  43. Lamborn KR, Yung WK, Chang SM, Wen PY, Cloughesy TF, DeAngelis LM, et al. Progression-free survival: an important end point in evaluating therapy for recurrent high-grade gliomas. Neuro Oncol 2008;10:162-170 https://doi.org/10.1215/15228517-2007-062
  44. Michiels S, Piedbois P, Burdett S, Syz N, Stewart L, Pignon JP. Meta-analysis when only the median survival times are known: a comparison with individual patient data results. Int J Technol Assess Health Care 2005;21:119-125 https://doi.org/10.1017/S0266462305050154
  45. Reardon DA, Galanis E, DeGroot JF, Cloughesy TF, Wefel JS, Lamborn KR, et al. Clinical trial end points for high-grade glioma: the evolving landscape. Neuro Oncol 2011;13:353-361 https://doi.org/10.1093/neuonc/noq203