Response assessment in neuro-oncology (a report of the RANO group): Assessment of outcome in trials of diffuse low-grade gliomas

The Lancet Oncology

Volumn 12, Issue 6, 2011, Pages 583-593

  Van den Bent, M J ^a   Wefel, J S ^b   Schiff, D ^c   Taphoorn, M J B ^d,e   Jaeckle, K ^f   Junck, L ^g   Armstrong, T ^b,h   Choucair, A ⁱ   Waldman, A D ^j   Gorlia, T ^k   Chamberlain, M ^l   Baumert, B G ^m   Vogelbaum, M A ⁿ   Macdonald, D R ^o   Reardon, D A ^p   Wen, P Y ^q   Chang, S M ^r   Jacobs, A H ^s,t  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d MC Haaglanden The Hague ^*  (Netherlands)

^e VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^f MAYO CLINIC   (United States)

^g UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^h UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT HOUSTON   (United States)

ⁱ INTERMOUNTAIN HEALTHCARE   (United States)

^j IMPERIAL COLLEGE LONDON   (United Kingdom)

^k EORTC DATA CENTER   (Belgium)

^l UNIVERSITY OF WASHINGTON   (United States)

^m MAASTRICHT UNIVERSITY   (Netherlands)

ⁿ LERNER RESEARCH INSTITUTE   (United States)

^o UNIVERSITY OF WESTERN ONTARIO   (Canada)

^p DUKE UNIVERSITY MEDICAL CENTER   (United States)

^q BRIGHAM AND WOMEN S HOSPITAL   (United States)

^r UNIVERSITY OF CALIFORNIA   (United States)

^s UNIVERSITY OF MÜNSTER   (Germany)

^t MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

TEMOZOLOMIDE;

CANCER GRADING; CANCER SURVIVAL; CELL DENSITY; COGNITION; COMPUTER ASSISTED TOMOGRAPHY; DIFFUSION WEIGHTED IMAGING; DISEASE SEVERITY; GLIOMA; HUMAN; IMAGE ANALYSIS; LIFE EXPECTANCY; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; OVERALL SURVIVAL; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; QUALITY OF LIFE; REVIEW; SENSITIVITY AND SPECIFICITY; SYSTEMATIC REVIEW;

BRAIN NEOPLASMS; CLINICAL TRIALS AS TOPIC; DISEASE PROGRESSION; GLIOMA; HUMANS; MAGNETIC RESONANCE IMAGING; POSITRON-EMISSION TOMOGRAPHY; TREATMENT OUTCOME;

EID: 79957516708     PISSN: 14702045     EISSN: 14745488     Source Type: Journal    
DOI: 10.1016/S1470-2045(11)70057-2     Document Type: Review

References (91)

1. Karim ABMF, Maat B, Hatlevoll R, et al. A randomized trial on dose-response in radiation therapy of low grade cerebral glioma: European Organization for Research and Treatment of Cancer (EORTC) study 2284. Int J Radiat Oncol Biol Phys 1996, 36:549-556.
2. van den Bent MJ, Afra D, de Witte O, et al. Long-term efficacy of early versus delayed radiotherapy for low-grade astrocytoma and oligodendroglioma in adults: the EORTC 22845 randomised trial. Lancet 2005, 366:985-990. for the EORTC Radiotherapy and Brain Tumor Groups and the UK Medical Research Council.
3. Shaw E, Arusell RM, Scheithauer B, et al. A prospective randomized trial of low versus high dose radiation in adults with a supratentorial low grade glioma: initial report of a NCCTG-RTOG-ECOG study. J Clin Oncol 2002, 20:2267-2276.
4. Pignatti F, van den Bent MJ, Curran D, et al. Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 2002, 20:2076-2084.
5. Chang EF, Smith JS, Chang SM, et al. Preoperative prognostic classification system for hemispheric low-grade gliomas in adults. J Neurosurg 2008, 109:817-824.
6. Jenkins RB, Blair H, Ballman KV, et al. A t(1;19)(q10;p10) mediates the combined deletions of 1p and 19q and predicts a better prognosis of patients with oligodendroglioma. Cancer Res 2006, 66:9852-9861.
7. Brown PD, Buckner JC, O'Fallon JR, et al. Importance of baseline mini-mental state examination as a prognostic factor for patients with low-grade glioma. Int J Radiat Oncol Biol Phys 2004, 59:117-125.
8. Shaw EG, Berkey B, Coons SW, et al. Recurrence following neurosurgeon-determined gross-total resection of adult supratentorial low-grade glioma: results of a prospective clinical trial. J Neurosurg 2008, 109:835-841.
9. Smith JS, Chang EF, Lamborn KR, et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 2008, 26:1338-1345.
10. McBride SM, Perez DA, Polley MY, et al. Activation of PI3K/mTOR pathway occurs in most adult low-grade gliomas and predicts patient survival. J Neurooncol 2010, 97:33-40.
11. Dubbink HJ, Taal W, van Marion R, et al. IDH1 mutations in low-grade astrocytomas predict survival but not response to temozolomide. Neurology 2009, 73:1792-1795.
12. Kaloshi G, Benouaich-Amiel A, Diakite F, et al. Temozolomide for low-grade gliomas: predictive impact of 1p/19q loss on response and outcome. Neurology 2007, 68:1831-1836.
13. Wessels PH, Twijnstra A, Ummelen MIJ, Krijne-Kubat B, Ramaekers FSC, Hopman AHN Gain of chromosome 7 as detected by in situ hybridization correlates with shorter survival in astrocytoma grade II. Genes Chromosom Cancer 2002, 33:279-284.
14. Weller M, Berger H, Hartmann C, et al. Combined 1p/19q loss in oligodendroglial tumors: predictive or prognostic biomarker?. Clin Cancer Res 2007, 13:6933-6937.
15. Everhard S, Kaloshi G, Criniere E, et al. MGMT methylation: a marker of response to temozolomide in low-grade gliomas. Ann Neurol 2006, 60:740-743.
16. van den Bent MJ, Dubbink HJ, Marie Y, et al. IDH1 and IDH2 mutations are prognostic but not predictive for outcome in anaplastic oligodendroglial tumors: a report of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Clin Cancer Res 2010, 16:1597-1604.
17. Taphoorn MJB, Klein Schiphorst A, Snoek FJ, et al. Cognitive functions and quality of life in patients with low-grade gliomas: the impact of radiotherapy. Ann Neurol 1994, 36:48-54.
18. Reijneveld JC, Sitskoorn MM, Klein M, Nuyen J, Taphoorn MJB Cognitive status and quality of life in suspected versus proven low-grade gliomas. Neurology 2001, 56:618-623.
19. Surma-aho O, Niemelä M, Vilkki J, et al. Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients. Neurology 2001, 56:1285-1290.
20. Douw L, Klein M, Fagel SSAA, et al. Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term follow-up. Lancet Neurol 2009, 8:810-818.
21. Macdonald DR, Cascino TL, Schold SC, Cairncross JG Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 1990, 8:1277-1280.
22. Mason WP, Krol GS, DeAngelis LM Low-grade oligodendroglioma responds to chemotherapy. Neurology 1996, 46:203-207.
23. Pallud J, Capelle L, Taillandier L, et al. Prognostic significance of imaging contrast enhancement for WHO grade II gliomas. Neuro Oncol 2009, 11:176-182.
24. Mandonnet E, Delattre JY, Tanguy ML, et al. Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 2003, 53:524-528.
25. Rees J, Watt H, Jager HR, et al. Volumes and growth rates of untreated adult low-grade gliomas indicate risk of early malignant transformation. Eur J Radiol 2009, 72:54-64.
26. Danchaivijitr N, Waldman AD, Tozer DJ, et al. Low-grade gliomas: do changes in rCBV measurements at longitudinal perfusion-weighted MR imaging predict malignant transformation?. Radiology 2008, 247:170-178.
27. Biemond-ter Stege E, Kros JM, de Bruin HG, et al. Treatment of low grade oligodendroglial tumors with PCV chemotherapy. Cancer 2005, 103:802-809.
28. Brada M, Viviers L, Abson C, et al. Phase II study of primary temozolomide chemotherapy in patients with WHO grade II gliomas. Ann Oncol 2003, 14:1715-1721.
29. Hoang-Xuan K, Capelle L, Kujas M, et al. Temozolomide as initial treatment for adults with low-grade oligodendrogliomas or oligoastrocytomas and correlation with chromosome 1p deletions. J Clin Oncol 2004, 22:3133-3138.
30. Soffietti R, Baumert BG, Bello L, et al. Guidelines on management of low-grade gliomas: report of an EFNS-EANO* Task Force. Eur J Neurol 2010, 17:1124-1133.
31. Bynevelt M, Britton J, Seymour H, MacSweeney E, Thomas N, Sandhu K FLAIR imaging in the follow-up of low-grade gliomas: time to dispense with the dual-echo?. Neuroradiology 2001, 43:129-133.
32. Pallud J, Varlet P, Devaux B, et al. Diffuse low-grade oligodendrogliomas extend beyond MRI-defined abnormalities. Neurology 2010, 74:1724-1731.
33. Pallud J, Mandonnet E, Duffau H, et al. Prognostic value of initial magnetic resonance imaging growth rates for World Health Organization grade II gliomas. Ann Neurol 2006, 60:380-383.
34. Connor SE, Gunny R, Hampton T, O'gorman R Magnetic resonance image registration and subtraction in the assessment of minor changes in low grade glioma volume. Eur Radiol 2004, 14:2061-2066.
35. Ricard D, Kaloshi G, Amiel-Benouaich A, et al. Dynamic history of low-grade gliomas before and after temozolomide treatment. Ann Neurol 2007, 61:484-490.
36. Brasil CG, Ciccarelli O, Altmann DR, et al. Low-grade gliomas: six-month tumor growth predicts patient outcome better than admission tumor volume, relative cerebral blood volume, and apparent diffusion coefficient. Radiology 2009, 253:505-512.
37. Law M, Yang S, Babb JS, et al. Comparison of cerebral blood volume and vascular permeability from dynamic susceptibility contrast-enhanced perfusion MR imaging with glioma grade. AJNR Am J Neuroradiol 2004, 25:746-755.
38. Feinstein AR, Sosin DM, Wells CK The Will Rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med 1985, 312:1604-1608.
39. Murphy PS, Viviers L, Abson C, et al. Monitoring temozolomide treatment in low-grade glioma with proton magnetic resonance spectroscopy. Br J Cancer 2004, 90:781-786.
40. Moffat BA, Chenevert TL, Lawrence TS, et al. Functional diffusion map: a noninvasive MRI biomarker for early stratification of clinical brain tumor response. Proc Natl Acad Sci USA 2005, 102:5524-5529.
41. Jager PL, Vaalburg W, Pruim J, de Vries EG, Langen KJ, Piers DA Radiolabeled amino acids: basic aspects and clinical applications in oncology. J Nucl Med 2001, 42:432-445.
42. Yamada S, Kubota K, Kubota R, Ido T, Tamahashi N High accumulation of fluorine-18-fluorodeoxyglucose in turpentine-induced inflammatory tissue. J Nucl Med 1995, 36:1301-1306.
43. Herholz K, Holzer T, Bauer B, et al. 11C-methionine PET for differential diagnosis of low-grade gliomas. Neurology 1998, 50:1316-1322.
44. Kracht LW, Miletic H, Busch S, et al. Delineation of brain tumor extent with [11C]L-methionine positron emission tomography: local comparison with stereotactic histopathology. Clin Cancer Res 2004, 10:7163-7170.
45. Kracht LW, Friese M, Herholz K, et al. Methyl-[11C]-l-methionine uptake as measured by positron emission tomography correlates to microvessel density in patients with glioma. Eur J Nucl Med Mol Imaging 2003, 30:868-873.
46. Sato N, Suzuki M, Kuwata N, et al. Evaluation of the malignancy of glioma using 11C-methionine positron emission tomography and proliferating cell nuclear antigen staining. Neurosurg Rev 1999, 22:210-214.
47. Nuutinen J, Sonninen P, Lehikoinen P, et al. Radiotherapy treatment planning and long-term follow-up with [(11)C]methionine PET in patients with low-grade astrocytoma. Int J Radiat Oncol Biol Phys 2000, 48:43-52.
48. Terakawa Y, Tsuyuguchi N, Iwai Y, et al. Diagnostic accuracy of 11C-methionine PET for differentiation of recurrent brain tumors from radiation necrosis after radiotherapy. J Nucl Med 2008, 49:694-699.
49. Thiel A, Pietrzyk U, Sturm V, Herholz K, Hovels M, Schroder R Enhanced accuracy in differential diagnosis of radiation necrosis by positron emission tomography-magnetic resonance imaging coregistration: technical case report. Neurosurgery 2000, 46:232-234.
50. Pauleit D, Floeth F, Hamacher K, et al. O-(2-[18F]fluoroethyl)-L-tyrosine PET combined with MRI improves the diagnostic assessment of cerebral gliomas. Brain 2005, 128:678-687.
51. Floeth FW, Pauleit D, Sabel M, et al. Prognostic value of O-(2-18F-fluoroethyl)-L-tyrosine PET and MRI in low-grade glioma. J Nucl Med 2007, 48:519-527.
52. Ullrich RT, Kracht L, Brunn A, et al. Methyl-L-11C-methionine PET as a diagnostic marker for malignant progression in patients with glioma. J Nucl Med 2009, 50:1962-1968.
53. Popperl G, Goldbrunner R, Gildehaus FJ, et al. 5tO-(2-[18F]fluoroethyl)-L-tyrosine PET for monitoring the effects of convection-enhanced delivery of paclitaxel in patients with recurrent glioblastoma. Eur J Nucl Med Mol Imaging 2005, 32:1018-1025.
54. Galldiks N, Kracht LW, Burghaus L, et al. Use of 11C-methionine PET to monitor the effects of temozolomide chemotherapy in malignant gliomas. Eur J Nucl Med Mol Imaging 2006, 33:516-524.
55. Herholz K, Kracht LW, Heiss WD Monitoring the effect of chemotherapy in a mixed glioma by C-11-methionine PET. J Neuroimaging 2003, 13:269-271.
56. Tang BN, Sadeghi N, Branle F, De Witte O, Wikler D, Goldman S Semi-quantification of methionine uptake and flair signal for the evaluation of chemotherapy in low-grade oligodendroglioma. J Neurooncol 2005, 71:161-168.
57. Pallud J, Mandonnet E, Deroulers C, et al. Pregnancy increases the growth rates of World Health Organization grade II gliomas. Ann Neurol 2010, 67:398-404.
58. van den Bent MJ, Carpentier AF, Brandes AA, et al. Adjuvant PCV improves progression free survival but not overall survival in newly diagnosed anaplastic oligodendrogliomas and oligoastrocytomas: a randomized EORTC phase III trial. J Clin Oncol 2006, 24:2715-2722.
59. Barsevick AM, Cleeland CS, Manning DC, et al. ASCPRO recommendations for the assessment of fatigue as an outcome in clinical trials. J Pain Symptom Manage 2010, 39:1086-1099.
60. Gotay CC, Kawamoto CT, Bottomley A, Efficace F The prognostic significance of patient-reported outcomes in cancer clinical trials. J Clin Oncol 2008, 26:1355-1363.
61. Klein M Health-related quality of life aspects in patients with low-grade glioma. Adv Tech Stand Neurosurg 2010, 35:213-235.
62. Chang EF, Potts MB, Keles GE, et al. Seizure characteristics and control following resection in 332 patients with low-grade gliomas. J Neurosurg 2008, 108:227-235.
63. Wen PY, Macdonald DR, Reardon DA, et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 2010, 28:1963-1972.
64. Armstrong TS, Gilbert MR Net clinical benefit: functional endpoints in brain tumor clinical trials. Curr Oncol Rep 2007, 9:60-65.
65. Meyers CA, Kudelka AP, Conrad CA, Gelke CK, Grove W, Pazdur R Neurotoxicity of CI-980, a novel mitotic inhibitor. Clin Cancer Res 1997, 3:419-422.
66. Meyers CA, Wefel JS The use of the mini-mental state examination to assess cognitive functioning in cancer trials: no ifs, ands, buts, or sensitivity. J Clin Oncol 2003, 21:3557-3558.
67. Meyers CA, Brown PD Role and relevance of neurocognitive assessment in clinical trials of patients with CNS tumors. J Clin Oncol 2006, 24:1305-1309.
68. Brown PD, Buckner JC, O'Fallon JR, et al. Effects of radiotherapy on cognitive function in patients with low-grade glioma measured by Folstein Mini-Mental State Examination. J Clin Oncol 2003, 21:2519-2524.
69. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005, 352:987-996.
70. Duffau H, Capelle L Preferential brain locations of low-grade gliomas. Cancer 2004, 100:2622-2626.
71. Armstrong TS Symptoms experience: a concept analysis. Oncol Nurs Forum 2003, 30:601-606.
72. Clark JA, Talcott JA Symptom indexes to assess outcomes of treatment for early prostate cancer. Med Care 2001, 39:1118-1130.
73. Sarna L Effectiveness of structured nursing assessment of symptom distress in advanced lung cancer. Oncol Nurs Forum 1998, 25:1041-1048.
74. Litofsky NS, Farace E, Anderson F, Meyers CA, Huang W, Laws ER Depression in patients with high-grade glioma: results of the Glioma Outcomes Project. Neurosurgery 2004, 54:358-366.
75. Armstrong TS, Mendoza T, Gning I, et al. Validation of the M.D. Anderson Symptom Inventory Brain Tumor Module (MDASI-BT). J Neurooncol 2006, 80:27-35.
76. Weitzner MA, Meyers CA, Gelke CK, Byrne KS, Cella DF, Levin VA The Functional Assessment of Cancer Therapy (FACT) scale. Development of a brain subscale and revalidation of the general version (FACT-G) in patients with primary brain tumors. Cancer 1995, 75:1151-1161.
77. Aaronson NK, Ahmedzai S, Bergman B, et al. The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst 1993, 85:365-376.
78. Osoba D, Aaronson NK, Muller M, et al. The development and psychometric validation of a brain cancer quality-of-life questionnaire for use in combination with general cancer-specific questionnaires. Qual Life Res 1996, 5:139-150.
79. Osoba D, Brada M, Yung WKA, Prados M Health-related quality of life in patients treated with temozolomide versus procarbazine for recurrent glioblastoma multiforme. J Clin Oncol 2000, 18:1481-1491.
80. Taphoorn MJB, Stupp R, Coens C, et al. Health-related quality of life in patients with glioblastoma: a randomised controlled trial. Lancet Oncol 2005, 6:937-944.
81. Taphoorn MJ, van den Bent MJ, Mauer ME, et al. Health-related quality of life in patients treated for anaplastic oligodendroglioma with adjuvant chemotherapy: results of a European Organisation for Research and Treatment of Cancer randomized clinical trial. J Clin Oncol 2007, 25:5723-5730. for the European Organisation for Research and Treatment of Cancer (EORTC).
82. Efficace F, Bottomley A Health related quality of life assessment methodology and reported outcomes in randomised controlled trials of primary brain cancer patients. Eur J Cancer 2002, 38:1824-1831.
83. Taphoorn MJ, Claassens L, Aaronson NK, et al. An international validation study of the EORTC brain cancer module (EORTC QLQ-BN20) for assessing health-related quality of life and symptoms in brain cancer patients. Eur J Cancer 2010, 46:1033-1040.
84. Klein M, Engelberts NH, van der Ploeg HM, et al. Epilepsy in low-grade gliomas: the impact on cognitive function and quality of life. Ann Neurol 2003, 54:514-520.
85. Klein M, Heimans JJ, Aaronson NK, et al. Effect of radiotherapy and other treatment-related factors on mid-term to long-term cognitive sequelae in low grade gliomas: a comparative study. Lancet 2002, 360:1361-1368.
86. Gunnarsson T, Olafsson E, Sighvatsson V, Hannesson B Surgical treatment of patients with low-grade astrocytomas and medically intractable seizures. Acta Neurol Scand 2002, 105:289-292.
87. Ruda R, Trevisan E, Soffietti R Epilepsy and brain tumors. Curr Opin Oncol 2010, 22:611-620.
88. Engel J A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia 2001, 42:796-803.
89. Wieser HG, Blume WT, Fish D, et al. ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia 2001, 42:282-286.
90. Mohanraj R, Brodie MJ Measuring the efficacy of antiepileptic drugs. Seizure 2003, 12:413-443.
91. Perucca E Active control trials: endpoints beyond conventional efficacy and tolerability measures. Epilepsy Res 2006, 68:73-74.