Grading of gliomas: The road from eminence to evidence

Journal of Neuropathology and Experimental Neurology

Volumn 70, Issue 2, 2011, Pages 101-109

  Kros, Johan M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Astrocytoma; Glioblastoma; Glioma; Grading; Histopathology; Oligodendroglioma

Indexed keywords

LOMUSTINE; PROCARBAZINE; VINCRISTINE;

ASTROCYTOMA; BRAIN TUMOR; CANCER COMBINATION CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER SURVIVAL; CELL PROLIFERATION; CLINICAL TRIAL (TOPIC); DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE SEVERITY; EPENDYMOMA; GLIOBLASTOMA; GLIOMA; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; INTERRATER RELIABILITY; NEUROIMAGING; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; OLIGODENDROGLIOMA; OVERALL SURVIVAL; PERFUSION WEIGHTED IMAGING; PILOCYTIC ASTROCYTOMA; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROGNOSIS; PROSPECTIVE STUDY; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SUBEPENDYMOMA; TUMOR LOCALIZATION; WORLD HEALTH ORGANIZATION;

ASTROCYTOMA; BRAIN NEOPLASMS; DIAGNOSTIC IMAGING; EPENDYMOMA; EVIDENCE-BASED MEDICINE; GLIOMA; HUMANS; OBSERVER VARIATION; OLIGODENDROGLIA;

EID: 79251599407     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31820681aa     Document Type: Review

References (97)

1. Maintz D, Fiedler K, Koopmann J, et al. Molecular genetic evidence for subtypes of oligoastrocytomas. J Neuropathol Exp Neurol 1997;56: 1098-104
2. Mueller W, Hartmann C, Hoffmann A, et al. Genetic signature of oligo-astrocytomas correlates with tumor location and denotes distinct molecular subsets. Am J Pathol 2002;161:313-19
3. Ohgaki H, Kleihues P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol 2005;64:479-89
4. Rasheed BK, Wiltshire RN, Bigner SH, et al. Molecular pathogenesis of malignant gliomas. Curr Opin Oncol 1999;11:162-67
5. Reifenberger J, Reifenberger G, Liu L, et al. Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol 1994;145:1175-90
6. Van Den Bent MJ, Looijenga LH, Langenberg K, et al. Chromosomal anomalies in oligodendroglial tumors are correlated with clinical features. Cancer 2003;97:1276-84
7. Weller M, Berger H, Hartmann C, et al. Combined 1p/19q loss in oli-godendroglial tumors: Predictive or prognostic biomarker? Clin Cancer Res 2007;13:6933-37
8. Felsberg J, Erkwoh A, Sabel MC, et al. Oligodendroglial tumors: Refinement of candidate regions on chromosome arm 1p and correlation of 1p/19q status with survival. Brain Pathol 2004;14:121-30
9. Kujas M, Lejeune J, Benouaich-Amiel A, et al. Chromosome 1p loss: A favorable prognostic factor in low-grade gliomas. Ann Neurol 2005;58: 322-26
10. Smith JS, Perry A, Borell TJ, et al. Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 2000;18:636-45
11. Van Den Bent MJ, Carpentier AF, Brandes AA, et al. Adjuvant pro-carbazine, lomustine, and vincristine improves progression-free survival but not overall survival in newly diagnosed anaplastic oligodendro-gliomas and oligoastrocytomas: A randomized European Organisation for Research and Treatment of Cancer phase III trial. J Clin Oncol 2006; 24:2715-22
12. Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003
13. Gilles FH, Sobel EL, Leviton A, et al. Clusters of histologic characteristics in children with infratentorial neuroglial tumors. The Childhood Brain Tumor Consortium. J Neurooncol 1998;39:51-63
14. Kouwenhoven MC, Gorlia T, Kros JM, et al. Molecular analysis of anaplastic oligodendroglial tumors in a prospective randomized study: A report from EORTC study 26951. Neuro Oncol 2009;11:737-46
15. Weller M, Felsberg J, Hartmann C, et al. Molecular predictors of progression-free and overall survival in patients with newly diagnosed glioblastoma: A prospective translational study of the German Glioma Network. J Clin Oncol 2009;27:5743-50
16. Fuller GN, Hess KR, Rhee CH, et al. Molecular classification of human diffuse gliomas by multidimensional scaling analysis of gene expression profiles parallels morphology-based classification, correlates with survival, and reveals clinically-relevant novel glioma subsets. Brain Pathol 2002;12:108-16
17. Nutt CL, Mani DR, Betensky RA, et al. Gene expression-based classification of malignant gliomas correlates better with survival than histo-logical classification. Cancer Res 2003;63:1602-7
18. Beetz C, Bergner S, Brodoehl S, et al. Outcome-based profiling of astrocytic tumors identifies prognostic gene expression signatures which link molecular and morphology-based pathology. Int J Oncol 2006;29: 1183-91
19. Van Den Boom J, Wolter M, Kuick R, et al. Characterization of gene expression profiles associated with glioma progression using oligonucleotide-based microarray analysis and real-time reverse transcription-polymerase chain reaction. Am J Pathol 2003;163:1033-43
20. Shirahata M, Iwao-Koizumi K, Saito S, et al. Gene expression-based molecular diagnostic system for malignant gliomas is superior to histo-logical diagnosis. Clin Cancer Res 2007;13:7341-56
21. Gravendeel LA, Kouwenhoven MC, Gevaert O, et al. Intrinsic gene expression profiles of gliomas are a better predictor of survival than histology. Cancer Res 2009;69:9065-72
22. Colman H, Zhang L, Sulman EP, et al. A multigene predictor of outcome in glioblastoma. Neuro Oncol 2009;12:49-57
23. Law M, Yang S, Wang H, et al. Glioma grading: Sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectro-scopic imaging compared with conventional MR imaging. AJNR Am J Neuroradiol 2003;24:1989-98
24. Callot V, Galanaud D, Figarella-Branger D, et al. Correlations between MR and endothelial hyperplasia in low-grade gliomas. J Magn Reson Imaging 2007;26:52-60
25. Kim JH, Chang KH, Na DG, et al. 3T 1H-MR spectroscopy in grading of cerebral gliomas: Comparison of short and intermediate echo time sequences. AJNR Am J Neuroradiol 2006;27:1412-18
26. Spampinato MV, Smith JK, Kwock L, et al. Cerebral blood volume measurements and proton MR spectroscopy in grading of oligoden-droglial tumors. AJR Am J Roentgenol 2007;188:204-12
27. Daumas-Duport C, Tucker ML, Kolles H, et al. Oligodendrogliomas. Part II: A new grading system based on morphological and imaging criteria. J Neurooncol 1997;34:61-78
28. Hamlat A, Saikali S, Chaperon J, et al. Proposal of a scoring scale as a survival predictor in intracranial oligodendrogliomas. J Neurooncol 2006; 79:159-68
29. Ribbert H. Beitrage zur Enstehung der Geschwulste. Bonn, Germany: Cohen, 1907
30. Bailey PC, Cushing H. A Classification of the Tumors of the Glioma Group on a Histogenesis Basis, with a Correlated Study of Prognosis. Philadelphia, PA: J.B. Lippincott, 1926
31. Broders A. Carcinoma: Grading and practical application. Arch Pathol Lab Med 1926;2:376-81
32. Kernohan JW, Mabon RF, et al. A simplified classification of the glio-mas. Mayo Clin Proc 1949;24:71-75
33. Zulch K. Atlas of the Histology of Brain Tumors. Berlin, Germany: Springer-Verlag, 1971
34. Kleihues P, Burger PC, Aldape KD, et al. WHO Classification of Tumours of the Central Nervous System. 4th ed. Lyon, France: International Agency for Research on Cancer, 2007
35. Kleihues P, Burger PC, Scheithauer BW. Histological Typing of Tumours of the Central Nervous System. Berlin, Germany: Springer-Verlag, 1993
36. Kleihues P, Burger PC, Plate KH, Ohgaki H, Cavenee WK. Pathology and Genetics of Tumours of the Nervous System. Lyon, France: International Agency for Research on Cancer, 1997
37. Kleihues P, Burger PC, Collins VP, et al. Pathology and Genetics of Tumours of the Nervous System. WHO edition. Lyon, France: International Agency for Research on Cancer, 2000
38. Zulch KJ. Histological Typing of Tumours of the Central Nervous System. Geneva, Switzerland: World Health Organization, 1979
39. Bruner JM, Inouye L, Fuller GN, et al. Diagnostic discrepancies and their clinical impact in a neuropathology referral practice. Cancer 1997;79: 796-803
40. Aldape K, Simmons ML, Davis RL, et al. Discrepancies in diagnoses of neuroepithelial neoplasms: The San Francisco Bay Area Adult Glioma Study. Cancer 2000;88:2342-49
41. Coons SW, Johnson PC, Scheithauer BW, et al. Improving diagnostic accuracy and interobserver concordance in the classification and grading of primary gliomas. Cancer 1997;79:1381-93
42. Giannini C, Scheithauer BW, Weaver AL, et al. Oligodendrogliomas: Reproducibility and prognostic value of histologic diagnosis and grading. J Neuropathol Exp Neurol 2001;60:248-62
43. Fuller CE, Schmidt RE, Roth KA, et al. Clinical utility of fluorescence in situ hybridization (FISH) in morphologically ambiguous gliomas with hybrid oligodendroglial/astrocytic features. J Neuropathol Exp Neurol 2003;62:1118-28
44. Prayson RA, Agamanolis DP, Cohen ML, et al. Interobserver reprodu-cibility among neuropathologists and surgical pathologists in fibrillary astrocytoma grading. J Neurol Sci 2000;175:33-39
45. Barry M, Sinha SK, Leader MB, et al. Poor agreement in recognition of abnormal mitoses: Requirement for standardized and robust definitions. Histopathology 2001;38:68-72
46. Edwards JL, Donalson JT. The time of fixation and the mitotic index. Am J Clin Pathol 1964;41:158-62
47. Giannini C, Scheithauer BW, Burger PC, et al. Cellular proliferation in pilocytic and diffuse astrocytomas. J Neuropathol Exp Neurol 1999;58: 46-53
48. Hsu DW, Louis DN, Efird JT, et al. Use of MIB-1 (Ki-67) immuno-reactivity in differentiating grade II and grade III gliomas. J Neuropathol Exp Neurol 1997;56:857-65
49. Weidl G, Iglesias-Rozas JR, Roehrl N. Causal probabilistic modeling for malignancy grading in pathology with explanations of dependency to the related histological features. Histol Histopathol 2007;22: 947-62
50. Sallinen PK, Sallinen SL, Helen PT, et al. Grading of diffusely infiltrating astrocytomas by quantitative histopathology, cell proliferation and image cytometric DNA analysis. Comparison of 133 tumors in the context of the WHO 1979 and WHO 1993 grading schemes. Neuropathol Appl Neurobiol 2000;26:319-31
51. Gilles FH, Sobel EL, Leviton A, et al. Quantitative histologic factors for grouping childhood supratentorial neuroglial tumors. Pediatr Pathol Lab Med 1997;17:729-54
52. Rohrl N, Iglesias-Rozas JR, Weidl G. A modern reproducible method for the histologic grading of astrocytomas with statistical classification tools. Anal Quant Cytol Histol 2008;30:33-38
53. Schmitt HP, Oberwittler C. Computer-aided classification of malignancy in astrocytomas. II. The value of categorically evaluated histologic and non-histologic features for a numerical classifier. Anal Cell Pathol 1992; 4:409-19
54. Schmitt HP, Oberwittler C, Schad LR. Computer-aided classification of malignancy in astrocytomas. I. The value of nuclear parameters obtained by automated black and white image analysis. Anal Cell Pathol 1992;4: 397-407
55. Sharma S, Karak AK, Sarkar C, et al. A grading study of gliomas using computer aided malignancy classification and histologic morphometry. J Neurooncol 1996;27:75-85
56. McDonald JM, See SJ, Tremont IW, et al. The prognostic impact of histology and 1p/19q status in anaplastic oligodendroglial tumors. Cancer 2005;104:1468-77
57. Ringertz J. Grading of gliomas. Acta Pathol Microbiol Scand 1950;27: 51-64
58. Fulling KH, Garcia DM. Anaplastic astrocytoma of the adult cerebrum. Prognostic value of histologic features. Cancer 1985;55:928-31
59. Burger PC, Vogel FS, Green SB, et al. Glioblastoma multiforme and anaplastic astrocytoma. Pathologic criteria and prognostic implications. Cancer 1985;56:1106-11
60. Nelson JS, Tsukada Y, Schoenfeld D, et al. Necrosis as a prognostic criterion in malignant supratentorial, astrocytic gliomas. Cancer 1983;52: 550-54
61. Rubinstein L. Tumors of the Central Nervous System. Washington, DC: Armed Forced Institute of Pathology, 1972
62. Daumas-Duport C, Scheithauer B, O'Fallon J, et al. Grading of astrocy-tomas. A simple and reproducible method. Cancer 1988;62:2152-65
63. Kros JM, Gorlia T, Kouwenhoven MC, et al. Panel review of anaplastic oligodendroglioma from European Organization for Research and Treatment of Cancer Trial 26951: Assessment of consensus in diagnosis, influence of 1p/19q loss, and correlations with outcome. J Neuropathol Exp Neurol 2007;66:545-51
64. Kleihues P, Burger PC, Scheithauer BW. Histological Typing of Tumours of the Central Nervous System. Berlin, Germany: Springer-Verlag, 1993
65. Greenfield JG, Roberston EG. Cystic oligodendrogliomas of the cerebral hemispheres and ventricular oligodendrogliomas. Brain 1933;56:247-64
66. Ravens JR, Adamkiewicz LL, Groff R. Cytology and cellular pathology of the oligodendrogliomas of the brain. J Neuropathol Exp Neurol 1955; 14:142-84
67. Earnest F III, Kernohan JW, Craig WM. Oligodendrogliomas: A review of 200 cases. Arch Neurol Psychiatry 1950;63:964-76
68. Smith MT, Ludwig CL, Godfrey AD, et al. Grading of oligodendro-gliomas. Cancer 1983;52:2107-14
69. Kernohan JW. Tumors of the CNS. Proc Staff Meet Mayo Clin 1938;24: 71-75
70. Muller W, Afra D, Schroder R. Supratentorial recurrences of gliomas. Morphological studies in relation to time intervals with oligodendro-gliomas. Acta Neurochir (Wien) 1977;39:15-25 (Pubitemid 8188641)
71. Roberts M, German WJ. A long term study of patients with oligoden-drogliomas. Follow-up of 50 cases, including Dr. Harvey Cushing's series. J Neurosurg 1966;24:697-700
72. Afra D, Muller W, Benoist G, et al. Supratentorial recurrences of gliomas. Results of reoperations on astrocytomas and oligodendro-gliomas. Acta Neurochir (Wien) 1978;43:217-27
73. Horrax G, Wu WQ. Postoperative survival of patients with intracranial oligodendroglioma with special reference to radical tumor removal; a study of 26 patients. J Neurosurg 1951;8:473-79
74. McCann WP, Weir BK, Elvidge AR. Long-term survival after removal of metastatic malignant melanoma of the brain. Report of two cases. J Neurosurg 1968;28:483-87
75. Kros JM, Troost D, Van Eden CG, et al. Oligodendroglioma. A comparison of two grading systems. Cancer 1988;61:2251-59
76. Burger PC, Rawlings CE, Cox EB, et al. Clinicopathologic correlations in the oligodendroglioma. Cancer 1987;59:1345-52
77. Kros JM, Hop WC, Godschalk JJ, et al. Prognostic value of the proliferation-related antigen Ki-67 in oligodendrogliomas. Cancer 1996; 78:1107-13
78. Daumas-Duport C, Varlet P, Tucker ML, et al. Oligodendrogliomas. Part I: Patterns of growth, histological diagnosis, clinical and imaging correlations: A study of 153 cases. J Neurooncol 1997;34:37-59
79. Mork SJ, Halvorsen TB, Lindegaard KF, et al. Oligodendroglioma. Histologic evaluation and prognosis. J Neuropathol Exp Neurol 1986;45: 65-78
80. Schiffer D, Bosone I, Dutto A, et al. The prognostic role of vessel productive changes and vessel density in oligodendroglioma. J Neurooncol 1999;44:99-107
81. Daumas-Duport C, Koziak M, Miquel C, et al. [Reappraisal of the Sainte-Anne Hospital classification of oligodendrogliomas in view of retrospective studies]. Neurochirurgie 2005;51:247-53
82. Giannini C, Burger PC, Berkey BA, et al. Anaplastic oligodendroglial tumors: Refining the correlation among histopathology, 1p 19q deletion and clinical outcome in Intergroup Radiation Therapy Oncology Group Trial 9402. Brain Pathol 2008;18:360-69
83. Miller CR, Dunham CP, Scheithauer BW, Significance of necrosis in grading of oligodendroglial neoplasms: A clinicopathologic and genetic study of newly diagnosed high-grade gliomas. J Clin Oncol 2006;24: 5419-26
84. Smith SF, Simpson JM, Brewer JA, et al. The presence of necrosis and/or microvascular proliferation does not influence survival of patients with anaplastic oligodendroglial tumors: Review of 98 patients. J Neurooncol 2006;80:75-82
85. Scheithauer BW, Fuller GN, VandenBerg SR. The 2007 WHO classification of tumors of the nervous system: Controversies in surgical neuropathology. Brain Pathol 2008;18:307-16
86. Guyotat J, Signorelli F, Desme S, et al. Intracranial ependymomas in adult patients: Analyses of prognostic factors. J Neurooncol 2002;60:255-68
87. Ho DM, Hsu CY, Wong TT, et al. A clinicopathologic study of 81 patients with ependymomas and proposal of diagnostic criteria for anaplastic ependymoma. J Neurooncol 2001;54:77-85
88. Korshunov A, Golanov A, Sycheva R, et al. The histologic grade is a main prognostic factor for patients with intracranial ependymomas treated in the microneurosurgical era: An analysis of 258 patients. Cancer 2004; 100:1230-37
89. Reni M, Brandes AA, Vavassori V, et al. A multicenter study of the prognosis and treatment of adult brain ependymal tumors. Cancer 2004; 100:1221-29
90. Tihan T, Zhou T, Holmes E, et al. The prognostic value of histological grading of posterior fossa ependymomas in children: A Children's Oncology Group study and a review of prognostic factors. Mod Pathol 2008;21:165-77
91. Figarella-Branger D, Civatte M, Bouvier-Labit C, et al. Prognostic factors in intracranial ependymomas in children. J Neurosurg 2000;93:605-13
92. Kurt E, Zheng PP, Hop WC, et al. Identification of relevant prognostic histopathologic features in 69 intracranial ependymomas, excluding myxopapillary ependymomas and subependymomas. Cancer 2006;106: 388-95
93. Rushing EJ, Brown DF, Hladik CL, et al. Correlation of bcl-2, p53, and MIB-1 expression with ependymoma grade and subtype. Mod Pathol 1998;11:464-70
94. Verstegen MJ, Leenstra DT, Ijlst-Keizers H, et al. Proliferation- and apoptosis-related proteins in intracranial ependymomas: An immunohis-tochemical analysis. J Neurooncol 2002;56:21-28
95. Prayson RA. Clinicopathologic study of 61 patients with ependymoma including MIB-1 immunohistochemistry. Ann Diagn Pathol 1999;3:11-18
96. Scott CB, Nelson JS, Farnan NC, et al. Central pathology review in clinical trials for patients with malignant glioma. A Report of Radiation Therapy Oncology Group 83-02. Cancer 1995;76:307-13
97. Hildebrand J, Gorlia T, Kros JM, et al. Adjuvant dibromodulcitol and BCNU chemotherapy in anaplastic astrocytoma: Results of a randomised European Organisation for Research and Treatment of Cancer phase III study (EORTC study 26882). Eur J Cancer 2008;44:1210-16