The treatment of glioblastomas: A systematic update on clinical Phase III trials

Critical Reviews in Oncology/Hematology

Volumn 87, Issue 3, 2013, Pages 265-282

  Yin, An an ^a   Cheng, Jin xiang ^a   Zhang, Xiang ^a   Liu, Bo lin ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Elderly patients; Glioblastoma; Phase III trials; Prognostic factors; Recurrent glioblastomas

Indexed keywords

AMINOLEVULINIC ACID; BEVACIZUMAB; CARMUSTINE; CEDIRANIB; CILENGITIDE; CINTREDEKIN BESUDOTOX; CISPLATIN; EDOTECARIN; ENZASTAURIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYDROXYUREA; IMATINIB; LEFLUNOMIDE; LOMUSTINE; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; NIMOTUZUMAB; NIMUSTINE; PLACEBO; PROCARBAZINE; RINDOPEPIMUT; SITIMAGENE CERADENOVEC; TEMOZOLOMIDE; TRABEDERSEN; VINCRISTINE;

ADULT; AGED; BLOOD BRAIN BARRIER; BLOOD TOXICITY; CANCER RADIOTHERAPY; CANCER SURVIVAL; CONTROLLED STUDY; DOSAGE SCHEDULE COMPARISON; DRUG DELIVERY SYSTEM; DRUG WITHDRAWAL; FEMALE; GLIOBLASTOMA; HUMAN; INTENSITY MODULATED RADIATION THERAPY; LIFE EXPECTANCY; MAJOR CLINICAL STUDY; MALE; META ANALYSIS; MICROSURGERY; MULTIPLE CYCLE TREATMENT; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PHASE 3 CLINICAL TRIAL; PHOTODYNAMIC THERAPY; PROGNOSIS; PROGRESSION FREE SURVIVAL; QUALITY OF LIFE; RADIATION DOSE; RADIATION DOSE FRACTIONATION; REVIEW; SALVAGE THERAPY; SYSTEMATIC REVIEW; TUMOR RECURRENCE;

ELDERLY PATIENTS; GLIOBLASTOMA; PHASE III TRIALS; PROGNOSTIC FACTORS; RECURRENT GLIOBLASTOMAS;

AGE FACTORS; BRAIN NEOPLASMS; CLINICAL TRIALS, PHASE III AS TOPIC; COMBINED MODALITY THERAPY; GLIOBLASTOMA; HUMANS; RECURRENCE; TREATMENT OUTCOME;

EID: 84881661380     PISSN: 10408428     EISSN: 18790461     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2013.01.007     Document Type: Review

References (97)

1. Central Brain Tumor Registry (CBTRUS). Primary brain and central nervous system tumors diagnosed in the United States in 2004-2008; 2012. http://www.cbtrus.org/reports/reports.html.
2. Brem S.S., Bierman P.J., Brem H., et al. Central nervous system cancers: clinical practice guidelines in oncology. Journal of the National Comprehensive Cancer Network 2011, 4:352-400.
3. Wen P.Y., Kesari S. Malignant gliomas in adults. New England Journal of Medicine 2008, 359:492-507.
4. Nicholas M.K. Glioblastoma multiforme: evidence-based approach to therapy. Expert Review of Anticancer Therapy 2007, 7:S23-S27.
5. Stupp R., Mason W.P., van den Bent M.J., et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. New England Journal of Medicine 2005, 352:987-996.
6. Anderson E., Grant R., Lewis S.C., Whittle I.R. Randomized Phase III controlled trials of therapy in malignant glioma: where are we after 40 years?. British Journal of Neurosurgery 2008, 22:339-349.
7. Adamson C., Kanu O.O., Mehta A.I., et al. Glioblastoma multiforme: a review of where we have been and where we are going. Expert Opinion on Investigational Drugs 2009, 18:1061-1083.
8. You B., Gan H.K., Pond G., Chen E.X. Consistency in the analysis and reporting of primary end points in oncology randomized controlled trials from registration to publication: a systematic review. Journal of Clinical Oncology 2012, 30:210-216.
9. Stummer W., Pichlmeier U., Meinel T., Wiestler O.D., Zanella F., Reulen H.J. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre Phase III trial. Lancet Oncology 2006, 7:392-401.
10. Buckner J.C., Ballman K.V., Michalak J.C., et al. Phase III trial of carmustine and cisplatin compared with carmustine alone and standard radiation therapy or accelerated radiation therapy in patients with glioblastoma multiforme: North Central Cancer Treatment Group 93-72-52 and Southwest Oncology Group 9503 Trials. Journal of Clinical Oncology 2006, 24:3871-3879.
11. Gilbert M.R., Wang M., Aldape K.D., et al. RTOG 0525: a randomized Phase III trial comparing standard adjuvant temozolomide (TMZ) with a dose-dense (dd) schedule in newly diagnosed glioblastoma (GBM). Journal of Clinical Oncology 2011, 29(suppl). abstract 2006.
12. Kim I.H., Park C.K., Heo D.S., 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. Journal of Neuro-Oncology 2011, 103:595-602.
13. Shibui S., Narita Y., Mizusawa J., et al. Randomized trial of chemoradiotherapy and adjuvant chemotherapy with nimustine (ACNU) versus nimustine plus procarbazine for newly diagnosed anaplastic astrocytoma and glioblastoma (JCOG0305). Cancer Chemotherapy and Pharmacology 2012.
14. Chinot O., Wick W., Mason W., et al. Phase III trial of bevacizumab added to standard radiotherapy and temozolomide for newly-diagnosed glioblastoma: mature progression-free survival and preliminary overall survival results in avaglio. Neuro-Oncology 2012, 14. iv101 OT-3.
15. Westphal M., Bach F. Final results of a randomized Phase III trial of nimotuzumab for the treatment of newly diagnosed glioblastoma in addition to standard radiation and chemotherapy with temozolomide versus standard radiation and temoziolamide. Journal of Clinical Oncology 2012, (Suppl.). [abstr 2033].
16. Brada M., Stenning S., Gabe R., et al. Temozolomide versus procarbazine, lomustine, and vincristine in recurrent high-grade glioma. Journal of Clinical Oncology 2010, 28:4601-4608.
17. Kunwar S., Chang S., Westphal M., et al. Phase III randomized trial of CED of IL13-PE38QQR vs Gliadel wafers for recurrent glioblastoma. Neuro-Oncology 2010, 12:871-881.
18. Batchelor T., Mulholland P., Neyns B., et al. A phase 3 randomized study comparing the efficacy of Cediranib as monotherapy, and in combination with lomustine, with lomustine alone in recurrent glioblastoma patients. Annals of Oncology 2010, 8(Suppl.):LBA7.
19. Wick W., Puduvalli V.K., Chamberlain M.C., et al. Phase III study of enzastaurin compared with lomustine in the treatment of recurrent intracranial glioblastoma. Journal of Clinical Oncology 2010, 28:1168-1174.
20. Dresemann G., Weller M., Rosenthal M.A., et al. Imatinib in combination with hydroxyurea versus hydroxyurea alone as oral therapy in patients with progressive pretreated glioblastoma resistant to standard dose temozolomide. Journal of Neuro-Oncology 2010, 96:393-402.
21. Stupp R., Wong E.T., Kanner A.A., et al. NovoTTF-100A versus physician's choice chemotherapy in recurrent glioblastoma: a randomised Phase III trial of a novel treatment modality. European Journal of Cancer 2012, 48:2192-2202.
22. Malmstrom A., Gronberg B.H., Marosi C., 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 Oncology 2012, 13:916-926.
23. Keime-Guibert F., Chinot O., Taillandier L., et al. Radiotherapy for glioblastoma in the elderly. New England Journal of Medicine 2007, 356:1527-1535.
24. Wick W., Platten M., Meisner C., et al. Temozolomide chemotherapy alone versus radiotherapy alone for malignant astrocytoma in the elderly: the NOA-08 randomised, phase 3 trial. Lancet Oncology 2012, 13:707-715.
25. Sanai N., Berger M.S. Glioma extent of resection and its impact on patient outcome. Neurosurgery 2008, 62:753-764. discussion 264-6.
26. Stummer W., Reulen H.J., Meinel T., et al. Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 2008, 62:564-576. discussion 564-76.
27. Van den Bent M.J., Stupp R., Mason W. Impact of the extent of resection on overall survival in newly diagnosed glioblastoma after chemo-irradiation with temozolamide: further analysis of EORTC study 26981. European Journal of Cancer 2005, 3. abstract.
28. Stummer W., Kamp M.A. The importance of surgical resection in malignant glioma. Current Opinion in Neurology 2009, 22:645-649.
29. Vuorinen V., Hinkka S., Farkkila M., Jaaskelainen J. Debulking or biopsy of malignant glioma in elderly people - a randomised study. Acta Neurochirurgica 2003, 145:5-10.
30. Kubben P.L., ter Meulen K.J., Schijns O.E., ter Laak-Poort M.P., van Overbeeke J.J., van Santbrink H. Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncology 2011, 12:1062-1070.
31. Tsitlakidis A., Foroglou N., Venetis C.A., Patsalas I., Hatzisotiriou A., Selviaridis P. Biopsy versus resection in the management of malignant gliomas: a systematic review and meta-analysis. Journal of Neurosurgery 2010, 112:1020-1032.
32. Stepp H., Beck T., Pongratz T., et al. ALA and malignant glioma: fluorescence-guided resection and photodynamic treatment. Journal of Environmental Pathology, Toxicology and Oncology 2007, 26:157-164.
33. Stummer W., Tonn J.C., Mehdorn H.M., et al. Counterbalancing risks and gains from extended resections in malignant glioma surgery: a supplemental analysis from the randomized 5-aminolevulinic acid glioma resection study. Clinical article. Journal of Neurosurgery 2011, 114:613-623.
34. Cheng J.X., Zhang X., Liu B.L. Health-related quality of life in patients with high-grade glioma. Neuro-Oncology 2009, 11:41-50.
35. Stupp R., Hegi M.E., Mason W.P., 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 Oncology 2009, 10:459-466.
36. Westphal M., Hilt D.C., Bortey E., et al. A phase 3 trial of local chemotherapy with biodegradable carmustine (BCNU) wafers (Gliadel wafers) in patients with primary malignant glioma. Neuro-Oncology 2003, 5:79-88.
37. Westphal M., Ram Z., Riddle V., Hilt D., Bortey E. Gliadel wafer in initial surgery for malignant glioma: long-term follow-up of a multicenter controlled trial. Acta Neurochirurgica 2006, 148:269-275. discussion 275.
38. Valtonen S., Timonen U., Toivanen P., et al. Interstitial chemotherapy with carmustine-loaded polymers for high-grade gliomas: a randomized double-blind study. Neurosurgery 1997, 41:44-48. discussion 48-9.
39. Weller M., Stupp R., Reifenberger G., et al. MGMT promoter methylation in malignant gliomas: ready for personalized medicine?. Nature Reviews Neurology 2010, 6:39-51.
40. Hegi M.E., Diserens A.C., Gorlia T., et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. New England Journal of Medicine 2005, 352:997-1003.
41. Villano J.L., Seery T.E., Bressler L.R. Temozolomide in malignant gliomas: current use and future targets. Cancer Chemotherapy and Pharmacology 2009, 64:647-655.
42. Grossman S.A., Wharam M., Sheidler V., et al. Phase II study of continuous infusion carmustine and cisplatin followed by cranial irradiation in adults with newly diagnosed high-grade astrocytoma. Journal of Clinical Oncology 1997, 15:2596-2603.
43. Grossman S.A., O'Neill A., Grunnet M., et al. Phase III study comparing three cycles of infusional carmustine and cisplatin followed by radiation therapy with radiation therapy and concurrent carmustine in patients with newly diagnosed supratentorial glioblastoma multiforme: Eastern Cooperative Oncology Group Trial 2394. Journal of Clinical Oncology 2003, 21:1485-1491.
44. Glass J., Silverman C.L., Axelrod R., Corn B.W., Andrews D.W. Fractionated stereotactic radiotherapy with cis-platinum radiosensitization in the treatment of recurrent, progressive, or persistent malignant astrocytoma. American Journal of Clinical Oncology 1997, 20:226-229.
45. Candelaria M., Garcia-Arias A., Cetina L., Duenas-Gonzalez A. Radiosensitizers in cervical cancer. Cisplatin and beyond. Radiation Oncology 2006, 1:15.
46. Charest G., Paquette B., Fortin D., Mathieu D., Sanche L. Concomitant treatment of F98 glioma cells with new liposomal platinum compounds and ionizing radiation. Journal of Neuro-Oncology 2010, 97:187-193.
47. Marshall N.E., Ballman K.V., Michalak J.C., et al. Ototoxicity of cisplatin plus standard radiation therapy vs. accelerated radiation therapy in glioblastoma patients. Journal of Neuro-Oncology 2006, 77:315-320.
48. Prados M.D., Yung W.K., Fine H.A., et al. Phase 2 study of BCNU and temozolomide for recurrent glioblastoma multiforme: North American Brain Tumor Consortium study. Neuro-Oncology 2004, 6:33-37.
49. Chang S.M., Prados M.D., Yung W.K., et al. Phase II study of neoadjuvant 1, 3-bis (2-chloroethyl)-1-nitrosourea and temozolomide for newly diagnosed anaplastic glioma: a North American Brain Tumor Consortium Trial. Cancer 2004, 100:1712-1716.
50. Kanu O.O., Hughes B., Di C., et al. Glioblastoma multiforme oncogenomics and signaling pathways. Clinical Medicine: Oncology 2009, 3:39-52.
51. Vredenburgh J.J., Desjardins A., Herndon J.N., et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. Journal of Clinical Oncology 2007, 25:4722-4729.
52. Friedman H.S., Prados M.D., Wen P.Y., et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. Journal of Clinical Oncology 2009, 27:4733-4740.
53. Heimberger A.B., Suki D., Yang D., Shi W., Aldape K. The natural history of EGFR and EGFRvIII in glioblastoma patients. Journal of Translational Medicine 2005, 3:38.
54. Franceschi E., Tosoni A., Bartolini S., Mazzocchi V., Fioravanti A., Brandes A.A. Treatment options for recurrent glioblastoma: pitfalls and future trends. Expert Review of Anticancer Therapy 2009, 9:613-619.
55. Clarke J.L., Ennis M.M., Yung W.K., et al. Is surgery at progression a prognostic marker for improved 6-month progression-free survival or overall survival for patients with recurrent glioblastoma?. Neuro-Oncology 2011, 13:1118-1124.
56. Amelio D., Amichetti M. Radiation therapy for the treatment of recurrent glioblastoma: an overview. Cancers 2012, 4:257-280.
57. Bidros D.S., Vogelbaum M.A. Novel drug delivery strategies in neuro-oncology. Neurotherapeutics 2009, 6:539-546.
58. Buonerba C., Di Lorenzo G., Marinelli A., et al. A comprehensive outlook on intracerebral therapy of malignant gliomas. Critical Reviews in Oncology/Hematology 2011, 80:54-68.
59. Kawakami M., Kawakami K., Puri R.K. Intratumor administration of interleukin 13 receptor-targeted cytotoxin induces apoptotic cell death in human malignant glioma tumor xenografts. Molecular Cancer Therapeutics 2002, 1:999-1007.
60. Kawakami M., Kawakami K., Puri R.K. Tumor regression mechanisms by IL-13 receptor-targeted cancer therapy involve apoptotic pathways. International Journal of Cancer 2003, 103:45-52.
61. Kunwar S., Chang S.M., Prados M.D., et al. Safety of intraparenchymal convection-enhanced delivery of cintredekin besudotox in early-phase studies. Neurosurgical Focus 2006, 20:E15.
62. Mueller S., Polley M.Y., Lee B., et al. Effect of imaging and catheter characteristics on clinical outcome for patients in the PRECISE study. Journal of Neuro-Oncology 2011, 101:267-277.
63. Reardon D.A., Turner S., Peters K.B., et al. A review of VEGF/VEGFR-targeted therapeutics for recurrent glioblastoma. Journal of the National Comprehensive Cancer Network 2011, 9:414-427.
64. Graff J.R., McNulty A.M., Hanna K.R., et al. The protein kinase Cbeta-selective inhibitor, Enzastaurin (LY317615.HCl), suppresses signaling through the AKT pathway, induces apoptosis, and suppresses growth of human colon cancer and glioblastoma xenografts. Cancer Research 2005, 65:7462-7469.
65. Dresemann G. Imatinib and hydroxyurea in pretreated progressive glioblastoma multiforme: a patient series. Annals of Oncology 2005, 16:1702-1708.
66. Reardon D.A., Egorin M.J., Quinn J.A., et al. Phase II study of imatinib mesylate plus hydroxyurea in adults with recurrent glioblastoma multiforme. Journal of Clinical Oncology 2005, 23:9359-9368.
67. Wen P.Y., Yung W.K., Lamborn K.R., et al. Phase I/II study of imatinib mesylate for recurrent malignant gliomas: North American Brain Tumor Consortium Study 99-08. Clinical Cancer Research 2006, 12:4899-4907.
68. Holdhoff M., Kreuzer K.A., Appelt C., et al. Imatinib mesylate radiosensitizes human glioblastoma cells through inhibition of platelet-derived growth factor receptor. Blood Cells, Molecules, and Diseases 2005, 34:181-185.
69. Arora A., Scholar E.M. Role of tyrosine kinase inhibitors in cancer therapy. Journal of Pharmacology and Experimental Therapeutics 2005, 315:971-979.
70. Yin D., Wang X., Konda B.M., et al. Increase in brain tumor permeability in glioma-bearing rats with nitric oxide donors. Clinical Cancer Research 2008, 14:4002-4009.
71. Reardon D.A., Egorin M.J., Desjardins A., et al. Phase I pharmacokinetic study of the vascular endothelial growth factor receptor tyrosine kinase inhibitor vatalanib (PTK787) plus imatinib and hydroxyurea for malignant glioma. Cancer 2009, 115:2188-2198.
72. Kirson E.D., Gurvich Z., Schneiderman R., et al. Disruption of cancer cell replication by alternating electric fields. Cancer Research 2004, 64:3288-3295.
73. Yovino S., Grossman S.A. Treatment of glioblastoma in "elderly" patients. Current Treatment Options in Oncology 2011, 12:253-262.
74. Iwamoto F.M., Reiner A.S., Panageas K.S., Elkin E.B., Abrey L.E. Patterns of care in elderly glioblastoma patients. Annals of Neurology 2008, 64:628-634.
75. Kita D., Ciernik I.F., Vaccarella S., et al. Age as a predictive factor in glioblastomas: population-based study. Neuroepidemiology 2009, 33:17-22.
76. Scott J.G., Suh J.H., Elson P., et al. Aggressive treatment is appropriate for glioblastoma multiforme patients 70 years old or older: a retrospective review of 206 cases. Neuro-Oncology 2011, 13:428-436.
77. Laperriere N., Weller M., Stupp R., et al. Optimal management of elderly patients with glioblastoma. Cancer Treatment Reviews 2012.
78. Scherer R.W., Langenberg P., von Elm E. Full publication of results initially presented in abstracts. Cochrane Database of Systematic Reviews 2007, MR000005.
79. Glioblastoma Multiforme (GBM). Locoregional agent survival study - anti-tenascin radiolabeled antibody therapy (Glass-Art). http://clinicaltrials.gov/ct2/show/NCT00615186.
80. Efficacy and Safety of AP. 12009 in patients with recurrent or refractory anaplastic astrocytoma or secondary glioblastoma (SAPPHIRE). http://clinicaltrials.gov/ct2/show/NCT00761280.
81. Lacroix M., Abi-Said D., Fourney D.R., et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. Journal of Neurosurgery 2001, 95:190-198.
82. Stummer W., Novotny A., Stepp H., Goetz C., Bise K., Reulen H.J. Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. Journal of Neurosurgery 2000, 93:1003-1013.
83. Tortosa A., Vinolas N., Villa S., et al. Prognostic implication of clinical, radiologic, and pathologic features in patients with anaplastic gliomas. Cancer 2003, 97:1063-1071.
84. Pope W.B., Sayre J., Perlina A., Villablanca J.P., Mischel P.S., Cloughesy T.F. MR imaging correlates of survival in patients with high-grade gliomas. American Journal of Neuroradiology 2005, 26:2466-2474.
85. Kowalczuk A., Macdonald R.L., Amidei C., et al. Quantitative imaging study of extent of surgical resection and prognosis of malignant astrocytomas. Neurosurgery 1997, 41:1028-1036. discussion 1036-8.
86. Macdonald D.R., Cascino T.L., Schold S.J., Cairncross J.G. Response criteria for Phase II studies of supratentorial malignant glioma. Journal of Clinical Oncology 1990, 8:1277-1280.
87. Chamberlain M.C., Glantz M.J., Chalmers L., Van Horn A., Sloan A.E. Early necrosis following concurrent Temodar and radiotherapy in patients with glioblastoma. Journal of Neuro-Oncology 2007, 82:81-83.
88. Taal W., Brandsma D., de Bruin H.G., et al. Incidence of early pseudo-progression in a cohort of malignant glioma patients treated with chemoirradiation with temozolomide. Cancer 2008, 113:405-410.
89. Norden A.D., Drappatz J., Wen P.Y. Antiangiogenic therapies for high-grade glioma. Nature Reviews Neurology 2009, 5:610-620.
90. Clarke J.L., Chang S.M. Neuroimaging: diagnosis and response assessment in glioblastoma. Cancer Journal 2012, 18:26-31.
91. Lutz K., Radbruch A., Wiestler B., Baumer P., Wick W., Bendszus M. Neuroradiological response criteria for high-grade gliomas. Clinical Neuroradiology 2011, 21:199-205.
92. Chang S.M., Clarke J., Wen P.Y. Novel imaging response assessment for drug therapies in recurrent malignant glioma 2009, American Society of Clinical Oncology, p. 107-11 [Educational Book].
93. Korn E.L., Freidlin B., Abrams J.S. Overall survival as the outcome for randomized clinical trials with effective subsequent therapies. Journal of Clinical Oncology 2011, 29:2439-2442.
94. Ballman K.V., Buckner J.C., Brown P.D., 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-Oncology 2007, 9:29-38.
95. Buyse M., Sargent D.J., Saad E.D. Survival is not a good outcome for randomized trials with effective subsequent therapies. Journal of Clinical Oncology 2011, 29:4719-4720. author reply 4720-1.
96. Lewis J.H., Kilgore M.L., Goldman D.P., et al. Participation of patients 65 years of age or older in cancer clinical trials. Journal of Clinical Oncology 2003, 21:1383-1389.
97. Siu L.L. Clinical trials in the elderly - a concept comes of age. New England Journal of Medicine 2007, 356:1575-1576.