References
Burger PC, Scheithauer BW, Lee RR et al (1997) An interdisciplinary approach to avoid the overtreatment of patients with central nervous system lesions. Cancer 80:2040–2046
Burger PC, Nelson JS, Boyko OB (1998) Diagnostic synergy in radiology and surgical neuropathology: neuroimaging techniques and general interpretive guidelines. Arch Pathol Lab Med 122:609–619
Burger PC, Nelson JS, Boyko OB (1998) Diagnostic synergy in radiology and surgical neuropathology: radiographic findings of specific pathologic entities. Arch Pathol Lab Med 122:620–632
Burger PC, Scheithauer BW, Vogel FS (2002) Surgical pathology of the nervous system and its coverings. Churchill Livingstone, New York
Kleihues P, Cavenee WK (2000) Pathology and genetics of tumours of the nervous system. IARC Press, Lyon
Greenfield JG, Graham DI, Lantos PL (2002) Greenfield’s neuropathology. Arnold, London
Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (2007) WHO classification of tumours of the central nervous system. International Agency for Research, Lyon
McLendon RE, Rosenblum MK, Bigner DD (2006) Russel & Rubinstein’s pathology of tumors of the nervous system. Hodder Arnold, London
McShane LM, Altman DG, Sauerbrei W et al (2005) Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst 97:1180–1184
Riley RD, Ridley G, Williams K et al (2007) Prognosis research: toward evidence-based results and a Cochrane methods group. J Clin Epidemiol 60:863–865, author reply 865–866
Altman DG, Riley RD (2005) Primer: an evidence-based approach to prognostic markers. Nat Clin Pract Oncol 2:466–472
Walters BC (1998) Clinical practice parameter development in neurosurgery. In: Bean J (ed) Neurosurgery in transition: the socioeconomic transformation of neurological surgery. Williams and Wilkins, Baltimore, pp 99–111
Lai R, Chu R, Fraumeni M et al (2006) Quality of randomized controlled trials reporting in the primary treatment of brain tumors. J Clin Oncol 24:1136–1144
Moher D, Schulz KF, Altman DG (2001) The CONSORT statement: revised recommendations for improving the quality of reports of parallel-group randomised trials. Lancet 357:1191–1194
Bullock R, Chesnut RM, Clifton G et al (1996) Guidelines for the management of severe head injury. Brain Trauma Foundation. Eur J Emerg Med 3:109–127
Bigner DD, McLendon RE, Bruner JM (1998) Russell & Rubinstein’s pathology of tumors of the nervous system. Arnold, London
Burger PC, Scheithauer BW (1994) Tumors of the central nervous system. Armed Forces Institute of Pathology, Washington, DC
Ringertz N (1950) Grading of gliomas. Acta Pathol Microbiol Scand 27:51–64
Kernohan JW, Sayre GP, Armed Forces Institute of Pathology (U.S.) (1952) Tumors of the central nervous system. Armed Forces Institute of Pathology; sold by American Registry of Pathology, Washington, DC
Zülch KJ, Organization WorldHealth (1979) Histological typing of tumours of the central nervous system. World Health Organization, Geneva
Daumas-Duport C, Scheithauer B, O’Fallon J et al (1988) Grading of astrocytomas. A simple and reproducible method. Cancer 62:2152–2165
Revesz T, Scaravilli F, Coutinho L et al (1993) Reliability of histological diagnosis including grading in gliomas biopsied by image-guided stereotactic technique. Brain 116(Pt 4):781–793
Gupta M, Djalilvand A, Brat DJ (2005) Clarifying the diffuse gliomas: an update on the morphologic features and markers that discriminate oligodendroglioma from astrocytoma. Am J Clin Pathol 124:755–768
Giannini C, Scheithauer BW, Burger PC et al (1999) Cellular proliferation in pilocytic and diffuse astrocytomas. J Neuropathol Exp Neurol 58:46–53
Ashby LS, Shapiro WR (2004) Low-grade glioma: supratentorial astrocytoma, oligodendroglioma, and oligoastrocytoma in adults. Curr Neurol Neurosci Rep 4:211–217
Coons SW, Pearl DK (1998) Mitosis identification in diffuse gliomas: implications for tumor grading. Cancer 82:1550–1555
Brat DJ, Mapstone TB (2003) Malignant glioma physiology: cellular response to hypoxia and its role in tumor progression. Ann Intern Med 138:659–668
Barker FG 2nd, Davis RL, Chang SM et al (1996) Necrosis as a prognostic factor in glioblastoma multiforme. Cancer 77:1161–1166
Giannini C, Scheithauer BW, Weaver AL et al (2001) Oligodendrogliomas: reproducibility and prognostic value of histologic diagnosis and grading. J Neuropathol Exp Neurol 60:248–262
Mork SJ, Halvorsen TB, Lindegaard KF et al (1986) Oligodendroglioma. Histologic evaluation and prognosis. J Neuropathol Exp Neurol 45:65–78
Burger PC, Rawlings CE, Cox EB et al (1987) Clinicopathologic correlations in the oligodendroglioma. Cancer 59:1345–1352
Miller CR, Dunham CP, Scheithauer BW et al (2006) Significance of necrosis in grading of oligodendroglial neoplasms: a clinicopathologic and genetic study of newly diagnosed high-grade gliomas. J Clin Oncol 24:5419–5426
Smith SF, Simpson JM, Brewer JA et al (2006) The presence of necrosis and/or microvascular proliferation does not influence survival of patients with anaplastic oligodendroglial tumours: review of 98 patients. J Neurooncol 80:75–82
Shaw EG, Scheithauer BW, O’Fallon JR (1997) Supratentorial gliomas: a comparative study by grade and histologic type. J Neurooncol 31:273–278
Shaw EG, Scheithauer BW, O’Fallon JR et al (1994) Mixed oligoastrocytomas: a survival and prognostic factor analysis. Neurosurgery 34:577–582, discussion 582
Donahue B, Scott CB, Nelson JS et al (1997) Influence of an oligodendroglial component on the survival of patients with anaplastic astrocytomas: a report of Radiation Therapy Oncology Group 83–02. Int J Radiat Oncol Biol Phys 38:911–914
Coons SW, Johnson PC, Scheithauer BW et al (1997) Improving diagnostic accuracy and interobserver concordance in the classification and grading of primary gliomas. Cancer 79:1381–1393
Mittler MA, Walters BC, Stopa EG (1996) Observer reliability in histological grading of astrocytoma stereotactic biopsies. J Neurosurg 85:1091–1094
Prayson RA, Agamanolis DP, Cohen ML et al (2000) Interobserver reproducibility among neuropathologists and surgical pathologists in fibrillary astrocytoma grading. J Neurol Sci 175:33–39
Burger PC, Nelson JS (1997) Stereotactic brain biopsies: specimen preparation and evaluation. Arch Pathol Lab Med 121:477–480
Burger PC, Vogel FS (1978) Frozen section interpretation in surgical neuropathology. II. Intraspinal lesions. Am J Surg Pathol 2:81–95
Martinez AJ, Pollack I, Hall WA et al (1988) Touch preparations in the rapid intraoperative diagnosis of central nervous system lesions. A comparison with frozen sections and paraffin-embedded sections. Mod Pathol 1:378–384
Reyes MG, Homsi MF, McDonald LW et al (1991) Imprints, smears, and frozen sections of brain tumors. Neurosurgery 29:575–579
Colbassani HJ, Nishio S, Sweeney KM et al (1988) CT-assisted stereotactic brain biopsy: value of intraoperative frozen section diagnosis. J Neurol Neurosurg Psychiatry 51:332–341
Brainard JA, Prayson RA, Barnett GH (1997) Frozen section evaluation of stereotactic brain biopsies: diagnostic yield at the stereotactic target position in 188 cases. Arch Pathol Lab Med 121:481–484
Burger PC (1985) Use of cytological preparations in the frozen section diagnosis of central nervous system neoplasia. Am J Surg Pathol 9:344–354
Ironside JW (1994) Update on central nervous system cytopathology. II. Brain smear technique. J Clin Pathol 47:683–688
Gaudin PB, Sherman ME, Brat DJ et al (1997) Accuracy of grading gliomas on CT-guided stereotactic biopsies: a survival analysis. Diagn Cytopathol 17:461–466
Roessler K, Dietrich W, Kitz K (2002) High diagnostic accuracy of cytologic smears of central nervous system tumors. A 15-year experience based on 4, 172 patients. Acta Cytol 46:667–674
Firlik KS, Martinez AJ, Lunsford LD (1999) Use of cytological preparations for the intraoperative diagnosis of stereotactically obtained brain biopsies: a 19-year experience and survey of neuropathologists. J Neurosurg 91:454–458
Bleggi-Torres LF, de Noronha L, Schneider Gugelmin E et al (2001) Accuracy of the smear technique in the cytological diagnosis of 650 lesions of the central nervous system. Diagn Cytopathol 24:293–295
Shah AB, Muzumdar GA, Chitale AR et al (1998) Squash preparation and frozen section in intraoperative diagnosis of central nervous system tumors. Acta Cytol 42:1149–1154
Cosgrove M, Fitzgibbons PL, Sherrod A et al (1989) Intermediate filament expression in astrocytic neoplasms. Am J Surg Pathol 13:141–145
Oh D, Prayson RA (1999) Evaluation of epithelial and keratin markers in glioblastoma multiforme: an immunohistochemical study. Arch Pathol Lab Med 123:917–920
Kros JM, Van Eden CG, Stefanko SZ et al (1990) Prognostic implications of glial fibrillary acidic protein containing cell types in oligodendrogliomas. Cancer 66:1204–1212
Herpers MJ, Budka H (1984) Glial fibrillary acidic protein (GFAP) in oligodendroglial tumors: gliofibrillary oligodendroglioma and transitional oligoastrocytoma as subtypes of oligodendroglioma. Acta Neuropathol (Berl) 64:265–272
Dehghani F, Schachenmayr W, Laun A et al (1998) Prognostic implication of histopathological, immunohistochemical and clinical features of oligodendrogliomas: a study of 89 cases. Acta Neuropathol (Berl) 95:493–504
Kriho VK, Yang HY, Moskal JR et al (1997) Keratin expression in astrocytomas: an immunofluorescent and biochemical reassessment. Virchows Arch 431:139–147
Cosgrove MM, Rich KA, Kunin SA et al (1993) Keratin intermediate filament expression in astrocytic neoplasms: analysis by immunocytochemistry, western blot, and northern hybridization. Mod Pathol 6:342–347
Nakopoulou L, Kerezoudi E, Thomaides T et al (1990) An immunocytochemical comparison of glial fibrillary acidic protein, S-100p and vimentin in human glial tumors. J Neurooncol 8:33–40
de Wit NJ, van Muijen GN, Ruiter DJ (2004) Immunohistochemistry in melanocytic proliferative lesions. Histopathology 44:517–541
Prayson RA (2002) Cell proliferation and tumors of the central nervous system, part II: radiolabeling, cytometric, and immunohistochemical techniques. J Neuropathol Exp Neurol 61:663–672
McKeever PE, Ross DA, Strawderman MS et al (1997) A comparison of the predictive power for survival in gliomas provided by MIB-1, bromodeoxyuridine and proliferating cell nuclear antigen with histopathologic and clinical parameters. J Neuropathol Exp Neurol 56:798–805
Hsu DW, Louis DN, Efird JT et al (1997) Use of MIB-1 (Ki-67) immunoreactivity in differentiating grade II and grade III gliomas. J Neuropathol Exp Neurol 56:857–865
Wakimoto H, Aoyagi M, Nakayama T et al (1996) Prognostic significance of Ki-67 labeling indices obtained using MIB-1 monoclonal antibody in patients with supratentorial astrocytomas. Cancer 77:373–380
Moskowitz SI, Jin T, Prayson RA (2006) Role of MIB1 in predicting survival in patients with glioblastomas. J Neurooncol 76:193–200
Coons SW, Johnson PC, Pearl DK (1997) The prognostic significance of Ki-67 labeling indices for oligodendrogliomas. Neurosurgery 41:878–884 discussion 884–875
Marie D, Liu Y, Moore SA et al (2001) Interobserver variability associated with the MIB-1 labeling index: high levels suggest limited prognostic usefulness for patients with primary brain tumors. Cancer 92:2720–2726
Hunter SB, Brat DJ, Olson JJ et al (2003) Alterations in molecular pathways of diffusely infiltrating glial neoplasms: application to tumor classification and anti-tumor therapy (Review). Int J Oncol 23:857–869
Ohgaki H, Kleihues P (2005) Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol 64:479–489
Collins VP (2007) Mechanisms of disease: genetic predictors of response to treatment in brain tumors. Nat Clin Pract Oncol 4:362–374
Smith JS, Perry A, Borell TJ et al (2000) Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18:636–645
Perry A, Fuller CE, Banerjee R et al (2003) Ancillary FISH analysis for 1p and 19q status: preliminary observations in 287 gliomas and oligodendroglioma mimics. Front Biosci 8:a1–9
Cairncross JG, Ueki K, Zlatescu MC et al (1998) Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst 90:1473–1479
Smith JS, Alderete B, Minn Y et al (1999) Localization of common deletion regions on 1p and 19q in human gliomas and their association with histological subtype. Oncogene 18:4144–4152
Aldape K, Burger PC, Perry A (2007) Clinicopathologic aspects of 1p/19q loss and the diagnosis of oligodendroglioma. Arch Pathol Lab Med 131:242–251
Reifenberger J, Reifenberger G, Liu L et al (1994) Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol 145:1175–1190
McDonald JM, See SJ, Tremont IW et al (2005) The prognostic impact of histology and 1p/19q status in anaplastic oligodendroglial tumors. Cancer 104:1468–1477
Burger PC, Minn AY, Smith JS et al (2001) Losses of chromosomal arms 1p and 19q in the diagnosis of oligodendroglioma. A study of paraffin-embedded sections. Mod Pathol 14:842–853
Ueki K, Nishikawa R, Nakazato Y et al (2002) Correlation of histology and molecular genetic analysis of 1p, 19q, 10q, TP53, EGFR, CDK4, and CDKN2A in 91 astrocytic and oligodendroglial tumors. Clin Cancer Res 8:196–201
Nigro JM, Takahashi MA, Ginzinger DG et al (2001) Detection of 1p and 19q loss in oligodendroglioma by quantitative microsatellite analysis, a real-time quantitative polymerase chain reaction assay. Am J Pathol 158:1253–1262
Chahlavi A, Kanner A, Peereboom D et al (2003) Impact of chromosome 1p status in response of oligodendroglioma to temozolomide: preliminary results. J Neurooncol 61:267–273
Cairncross G, Berkey B, Shaw E et al (2006) Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: Intergroup Radiation Therapy Oncology Group Trial 9402. J Clin Oncol 24:2707–2714
Brat DJ, Seiferheld WF, Perry A et al (2004) Analysis of 1p, 19q, 9p, and 10q as prognostic markers for high-grade astrocytomas using fluorescence in situ hybridization on tissue microarrays from Radiation Therapy Oncology Group trials. Neuro-oncol 6:96–103
Schmidt MC, Antweiler S, Urban N et al (2002) Impact of genotype and morphology on the prognosis of glioblastoma. J Neuropathol Exp Neurol 61:321–328
Smith JS, Tachibana I, Passe SM et al (2001) PTEN mutation, EGFR amplification, and outcome in patients with anaplastic astrocytoma and glioblastoma multiforme. J Natl Cancer Inst 93:1246–1256
Liu L, Backlund LM, Nilsson BR et al (2005) Clinical significance of EGFR amplification and the aberrant EGFRvIII transcript in conventionally treated astrocytic gliomas. J Mol Med 83:917–926
Frederick L, Wang XY, Eley G et al (2000) Diversity and frequency of epidermal growth factor receptor mutations in human glioblastomas. Cancer Res 60:1383–1387
Wong AJ, Ruppert JM, Bigner SH et al (1992) Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc Natl Acad Sci U S A 89:2965–2969
Olson JJ, Barnett D, Yang J et al (1998) Gene amplification as a prognostic factor in primary brain tumors. Clin Cancer Res 4:215–222
Huncharek M, Kupelnick B (2000) Epidermal growth factor receptor gene amplification as a prognostic marker in glioblastoma multiforme: results of a meta-analysis. Oncol Res 12:107–112
Simmons ML, Lamborn KR, Takahashi M et al (2001) Analysis of complex relationships between age, p53, epidermal growth factor receptor, and survival in glioblastoma patients. Cancer Res 61:1122–1128
Aldape KD, Ballman K, Furth A et al (2004) Immunohistochemical detection of EGFRvIII in high malignancy grade astrocytomas and evaluation of prognostic significance. J Neuropathol Exp Neurol 63:700–707
Heimberger AB, Hlatky R, Suki D et al (2005) Prognostic effect of epidermal growth factor receptor and EGFRvIII in glioblastoma multiforme patients. Clin Cancer Res 11:1462–1466
Perry A, Aldape KD, George DH et al (2004) Small cell astrocytoma: an aggressive variant that is clinicopathologically and genetically distinct from anaplastic oligodendroglioma. Cancer 101:2318–2326
Burger PC, Pearl DK, Aldape K et al (2001) Small cell architecture–a histological equivalent of EGFR amplification in glioblastoma multiforme? J Neuropathol Exp Neurol 60:1099–1104
Mellinghoff IK, Wang MY, Vivanco I et al (2005) Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 353:2012–2024
Rich JN, Reardon DA, Peery T et al (2004) Phase II trial of gefitinib in recurrent glioblastoma. J Clin Oncol 22:133–142
Ciardiello F, Tortora G (2001) A novel approach in the treatment of cancer: targeting the epidermal growth factor receptor. Clin Cancer Res 7:2958–2970
Haas-Kogan DA, Prados MD, Tihan T et al (2005) Epidermal growth factor receptor, protein kinase B/Akt, and glioma response to erlotinib. J Natl Cancer Inst 97:880–887
Stommel JM, Kimmelman AC, Ying H et al (2007) Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 318:287–290
Esteller M, Garcia-Foncillas J, Andion E et al (2000) Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 343:1350–1354
Stupp R, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996
Hegi ME, Diserens AC, Gorlia T et al (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003
Mikeska T, Bock C, El-Maarri O et al (2007) Optimization of Quantitative MGMT Promoter Methylation Analysis Using Pyrosequencing and Combined Bisulfite Restriction Analysis. J Mol Diagn 9:368–381
Pollack IF, Hamilton RL, Sobol RW et al (2006) O6-methylguanine-DNA methyltransferase expression strongly correlates with outcome in childhood malignant gliomas: results from the CCG–945 Cohort. J Clin Oncol 24:3431–3437
Fruehauf JP, Brem H, Brem S et al (2006) In vitro drug response and molecular markers associated with drug resistance in malignant gliomas. Clin Cancer Res 12:4523–4532
Grasbon-Frodl EM, Kreth FW, Ruiter M et al (2007) Intratumoral homogeneity of MGMT promoter hypermethylation as demonstrated in serial stereotactic specimens from anaplastic astrocytomas and glioblastomas. Int J Cancer 121:2458–2464
Bao S, Wu Q, McLendon RE et al (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760
Singh SK, Hawkins C, Clarke ID et al (2004) Identification of human brain tumour initiating cells. Nature 432:396–401
Khwaja FW, Duke-Cohan JS, Brat DJ et al (2006) Attractin is elevated in the cerebrospinal fluid of patients with malignant astrocytoma and mediates glioma cell migration. Clin Cancer Res 12:6331–6336
Khwaja FW, Nolen JD, Mendrinos SE et al (2006) Proteomic analysis of cerebrospinal fluid discriminates malignant and nonmalignant disease of the central nervous system and identifies specific protein markers. Proteomics 6:6277–6287
Phillips HS, Kharbanda S, Chen R et al (2006) Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9:157–173
Nutt CL, Mani DR, Betensky RA et al (2003) Gene expression-based classification of malignant gliomas correlates better with survival than histological classification. Cancer Res 63:1602–1607
Pomeroy SL, Tamayo P, Gaasenbeek M et al (2002) Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 415:436–442
Acknowledgements
We wish to acknowledge Beverly Murphy for her assistance in creating a coherent series of literature searches. Additionally we wish to thank Stephen Haines, MD, Jack Rock, MD, Tom Mikkelson, MD for their review and consultations regarding on this work. The members of the committees express appreciation to the AANS/CNS Joint Guidelines Committee for their review, comments and suggestions. We also thank Linda Phillips for meeting organization and collection of materials and Emily Feinstein for her assistance in editing the material for publication. Additionally we want to acknowledge the unrestricted financial grants provided by Aesculap, Inc., Codman, A Johnson and Johnson, Company., NeoPharm, Inc., Stryker/Leibinger Inc., Schering-Plough, and Guilford Pharmaceuticals for support of the venues in which the experts gathered for development and review of the guidelines.
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Brat, D.J., Prayson, R.A., Ryken, T.C. et al. Diagnosis of malignant glioma: role of neuropathology. J Neurooncol 89, 287–311 (2008). https://doi.org/10.1007/s11060-008-9618-1
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DOI: https://doi.org/10.1007/s11060-008-9618-1