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Published in: Journal of Neuro-Oncology 3/2015

01-12-2015 | Topic Review & Clinical Guidelines

The role of neuropathology in the management of patients with diffuse low grade glioma

A systematic review and evidence-based clinical practice guideline

Authors: Daniel P. Cahill, Andrew E. Sloan, Brian V. Nahed, Kenneth D. Aldape, David N. Louis, Timothy C. Ryken, Steven N. Kalkanis, Jeffrey J. Olson

Published in: Journal of Neuro-Oncology | Issue 3/2015

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Abstract

Target population

Adult patients (age ≥18 years) who have suspected low-grade diffuse glioma.

Question

What are the optimal neuropathological techniques to diagnose low-grade diffuse glioma in the adult?

Recommendation

Level I

Histopathological analysis of a representative surgical sample of the lesion should be used to provide the diagnosis of low-grade diffuse glioma.

Level III

Both frozen section and cytopathologic/smear evaluation should be used to aid the intra-operative assessment of low-grade diffuse glioma diagnosis. A resection specimen is preferred over a biopsy specimen, to minimize the potential for sampling error issues.

Target population

Patients with histologically-proven WHO grade II diffuse glioma.

Question

In adult patients (age ≥18 years) with histologically-proven WHO grade II diffuse glioma, is testing for IDH1 mutation (R132H and/or others) warranted? If so, is there a preferred method?

Recommendation

Level II

IDH gene mutation assessment, via IDH1 R132H antibody and/or IDH1/2 mutation hotspot sequencing, is highly-specific for low-grade diffuse glioma, and is recommended as an additional test for classification and prognosis.

Target population

Patients with histologically-proven WHO grade II diffuse glioma.

Question

In adult patients (age ≥18 years) with histologically-proven WHO grade II diffuse glioma, is testing for 1p/19q loss warranted? If so, is there a preferred method?

Recommendation

Level III

1p/19q loss-of-heterozygosity testing, by FISH, array-CGH or PCR, is recommended as an additional test in oligodendroglial cases for prognosis and potential treatment planning.

Target population

Patients with histologically-proven WHO grade II diffuse glioma.

Question

In adult patients (age ≥18 years) with histologically-proven WHO grade II diffuse glioma, is MGMT promoter methylation testing warranted? If so, is there a preferred method?

Recommendation

There is insufficient evidence to recommend methyl-guanine methyl-transferase (MGMT) promoter methylation testing as a routine for low-grade diffuse gliomas. It is recommended that patients be enrolled in properly designed clinical trials to assess the value of this and related markers for this target population.

Target population

Patients with histologically-proven WHO grade II diffuse glioma.

Question

In adult patients (age ≥18 years) with histologically-proven WHO grade II diffuse glioma, is Ki-67/MIB1 immunohistochemistry warranted? If so, is there a preferred method to quantitate results?

Recommendation

Level III

Ki67/MIB1 immunohistochemistry is recommended as an option for prognostic assessment.
Literature
1.
3.
go back to reference Wilden JN, Kelly PJ (1987) CT computerised stereotactic biopsy for low density CT lesions presenting with epilepsy. J Neurol Neurosurg Psychiatry 50:1302–1305PubMedCentralCrossRefPubMed Wilden JN, Kelly PJ (1987) CT computerised stereotactic biopsy for low density CT lesions presenting with epilepsy. J Neurol Neurosurg Psychiatry 50:1302–1305PubMedCentralCrossRefPubMed
6.
go back to reference Burger PC, Nelson JS, Boyko OB (1998) Diagnostic synergy in radiology and surgical neuropathology: neuroimaging techniques and general interpretive guidelines. Arch Pathol Lab Med 122:609–619PubMed Burger PC, Nelson JS, Boyko OB (1998) Diagnostic synergy in radiology and surgical neuropathology: neuroimaging techniques and general interpretive guidelines. Arch Pathol Lab Med 122:609–619PubMed
7.
go back to reference Burger PC, Nelson JS, Boyko OB (1998) Diagnostic synergy in radiology and surgical neuropathology: radiographic findings of specific pathologic entities. Arch Pathol Lab Med 122:620–632PubMed Burger PC, Nelson JS, Boyko OB (1998) Diagnostic synergy in radiology and surgical neuropathology: radiographic findings of specific pathologic entities. Arch Pathol Lab Med 122:620–632PubMed
8.
go back to reference Colbassani HJ, Nishio S, Sweeney KM, Bakay RA, Takei Y (1988) CT-assisted stereotactic brain biopsy: value of intraoperative frozen section diagnosis. J Neurol Neurosurg Psychiatry 51:332–341PubMedCentralCrossRefPubMed Colbassani HJ, Nishio S, Sweeney KM, Bakay RA, Takei Y (1988) CT-assisted stereotactic brain biopsy: value of intraoperative frozen section diagnosis. J Neurol Neurosurg Psychiatry 51:332–341PubMedCentralCrossRefPubMed
9.
go back to reference Revesz T, Scaravilli F, Coutinho L, Cockburn H, Sacares P, Thomas DG (1993) Reliability of histological diagnosis including grading in gliomas biopsied by image-guided stereotactic technique. Brain 116(Pt 4):781–793CrossRefPubMed Revesz T, Scaravilli F, Coutinho L, Cockburn H, Sacares P, Thomas DG (1993) Reliability of histological diagnosis including grading in gliomas biopsied by image-guided stereotactic technique. Brain 116(Pt 4):781–793CrossRefPubMed
10.
go back to reference 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 121:481–484PubMed 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 121:481–484PubMed
12.
go back to reference Burger PC, Vogel FS, Green SB, Strike TA (1985) Glioblastoma multiforme and anaplastic astrocytoma. Pathologic criteria and prognostic implications. Cancer 56:1106–1111PubMed Burger PC, Vogel FS, Green SB, Strike TA (1985) Glioblastoma multiforme and anaplastic astrocytoma. Pathologic criteria and prognostic implications. Cancer 56:1106–1111PubMed
14.
go back to reference Daumas-Duport C, Scheithauer B, O’Fallon J, Kelly P (1988) Grading of astrocytomas. A simple and reproducible method. Cancer 62:2152–2165PubMed Daumas-Duport C, Scheithauer B, O’Fallon J, Kelly P (1988) Grading of astrocytomas. A simple and reproducible method. Cancer 62:2152–2165PubMed
15.
go back to reference Shaw EG, Scheithauer BW, O’Fallon JR (1997) Supratentorial gliomas: a comparative study by grade and histologic type. J Neurooncol 31:273–278CrossRefPubMed Shaw EG, Scheithauer BW, O’Fallon JR (1997) Supratentorial gliomas: a comparative study by grade and histologic type. J Neurooncol 31:273–278CrossRefPubMed
16.
go back to reference (2007) World Health Organization Histological Classification of Tumours of the Central Nervous System International Agency for Research on Cancer, Lyon (2007) World Health Organization Histological Classification of Tumours of the Central Nervous System International Agency for Research on Cancer, Lyon
17.
go back to reference Burger PC (1985) Use of cytological preparations in the frozen section diagnosis of central nervous system neoplasia. Am J Surg Pathol 9:344–354CrossRefPubMed Burger PC (1985) Use of cytological preparations in the frozen section diagnosis of central nervous system neoplasia. Am J Surg Pathol 9:344–354CrossRefPubMed
18.
go back to reference Burger PC, Nelson JS (1997) Stereotactic brain biopsies: specimen preparation and evaluation. Arch Pathol Lab Med 121:477–480PubMed Burger PC, Nelson JS (1997) Stereotactic brain biopsies: specimen preparation and evaluation. Arch Pathol Lab Med 121:477–480PubMed
19.
go back to reference Shah AB, Muzumdar GA, Chitale AR, Bhagwati SN (1998) Squash preparation and frozen section in intraoperative diagnosis of central nervous system tumors. Acta Cytol 42:1149–1154CrossRefPubMed Shah AB, Muzumdar GA, Chitale AR, Bhagwati SN (1998) Squash preparation and frozen section in intraoperative diagnosis of central nervous system tumors. Acta Cytol 42:1149–1154CrossRefPubMed
20.
go back to reference Reyes MG, Homsi MF, McDonald LW, Glick RP (1991) Imprints, smears, and frozen sections of brain tumors. Neurosurgery 29:575–579CrossRefPubMed Reyes MG, Homsi MF, McDonald LW, Glick RP (1991) Imprints, smears, and frozen sections of brain tumors. Neurosurgery 29:575–579CrossRefPubMed
21.
go back to reference Ironside JW (1994) Update on central nervous system cytopathology. II. Brain smear technique. J Clin Pathol 47:683–688PubMed Ironside JW (1994) Update on central nervous system cytopathology. II. Brain smear technique. J Clin Pathol 47:683–688PubMed
22.
go back to reference Bleggi-Torres LF, de Noronha L, Schneider Gugelmin E, Martins Sebastiao AP, Werner B, Marques Maggio E, Queiroz Telles JE, Martins Collaco L (2001) Accuracy of the smear technique in the cytological diagnosis of 650 lesions of the central nervous system. Diagn Cytopathol 24:293–295. doi:10.1002/dc.1062 CrossRefPubMed Bleggi-Torres LF, de Noronha L, Schneider Gugelmin E, Martins Sebastiao AP, Werner B, Marques Maggio E, Queiroz Telles JE, Martins Collaco L (2001) Accuracy of the smear technique in the cytological diagnosis of 650 lesions of the central nervous system. Diagn Cytopathol 24:293–295. doi:10.​1002/​dc.​1062 CrossRefPubMed
23.
go back to reference 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 46:667–674CrossRefPubMed 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 46:667–674CrossRefPubMed
24.
go back to reference Giannini C, Scheithauer BW, Weaver AL, Burger PC, Kros JM, Mork S, Graeber MB, Bauserman S, Buckner JC, Burton J, Riepe R, Tazelaar HD, Nascimento AG, Crotty T, Keeney GL, Pernicone P, Altermatt H (2001) Oligodendrogliomas: reproducibility and prognostic value of histologic diagnosis and grading. J Neuropathol Exp Neurol 60:248–262PubMed Giannini C, Scheithauer BW, Weaver AL, Burger PC, Kros JM, Mork S, Graeber MB, Bauserman S, Buckner JC, Burton J, Riepe R, Tazelaar HD, Nascimento AG, Crotty T, Keeney GL, Pernicone P, Altermatt H (2001) Oligodendrogliomas: reproducibility and prognostic value of histologic diagnosis and grading. J Neuropathol Exp Neurol 60:248–262PubMed
25.
go back to reference McDonald JM, See SJ, Tremont IW, Colman H, Gilbert MR, Groves M, Burger PC, Louis DN, Giannini C, Fuller G, Passe S, Blair H, Jenkins RB, Yang H, Ledoux A, Aaron J, Tipnis U, Zhang W, Hess K, Aldape K (2005) The prognostic impact of histology and 1p/19q status in anaplastic oligodendroglial tumors. Cancer 104:1468–1477. doi:10.1002/cncr.21338 CrossRefPubMed McDonald JM, See SJ, Tremont IW, Colman H, Gilbert MR, Groves M, Burger PC, Louis DN, Giannini C, Fuller G, Passe S, Blair H, Jenkins RB, Yang H, Ledoux A, Aaron J, Tipnis U, Zhang W, Hess K, Aldape K (2005) The prognostic impact of histology and 1p/19q status in anaplastic oligodendroglial tumors. Cancer 104:1468–1477. doi:10.​1002/​cncr.​21338 CrossRefPubMed
26.
27.
go back to reference Prayson RA, Agamanolis DP, Cohen ML, Estes ML, Kleinschmidt-DeMasters BK, Abdul-Karim F, McClure SP, Sebek BA, Vinay R (2000) Interobserver reproducibility among neuropathologists and surgical pathologists in fibrillary astrocytoma grading. J Neurol Sci 175:33–39CrossRefPubMed Prayson RA, Agamanolis DP, Cohen ML, Estes ML, Kleinschmidt-DeMasters BK, Abdul-Karim F, McClure SP, Sebek BA, Vinay R (2000) Interobserver reproducibility among neuropathologists and surgical pathologists in fibrillary astrocytoma grading. J Neurol Sci 175:33–39CrossRefPubMed
29.
go back to reference Kim YH, Nobusawa S, Mittelbronn M, Paulus W, Brokinkel B, Keyvani K, Sure U, Wrede K, Nakazato Y, Tanaka Y, Vital A, Mariani L, Stawski R, Watanabe T, De Girolami U, Kleihues P, Ohgaki H (2010) Molecular classification of low-grade diffuse gliomas. Am J Pathol 177:2708–2714. doi:10.2353/ajpath.2010.100680 PubMedCentralCrossRefPubMed Kim YH, Nobusawa S, Mittelbronn M, Paulus W, Brokinkel B, Keyvani K, Sure U, Wrede K, Nakazato Y, Tanaka Y, Vital A, Mariani L, Stawski R, Watanabe T, De Girolami U, Kleihues P, Ohgaki H (2010) Molecular classification of low-grade diffuse gliomas. Am J Pathol 177:2708–2714. doi:10.​2353/​ajpath.​2010.​100680 PubMedCentralCrossRefPubMed
31.
go back to reference Giannini C, Scheithauer BW, Burger PC, Christensen MR, Wollan PC, Sebo TJ, Forsyth PA, Hayostek CJ (1999) Cellular proliferation in pilocytic and diffuse astrocytomas. J Neuropathol Exp Neurol 58:46–53CrossRefPubMed Giannini C, Scheithauer BW, Burger PC, Christensen MR, Wollan PC, Sebo TJ, Forsyth PA, Hayostek CJ (1999) Cellular proliferation in pilocytic and diffuse astrocytomas. J Neuropathol Exp Neurol 58:46–53CrossRefPubMed
32.
go back to reference Muller MB, Schmidt MC, Schmidt O, Hayashi Y, Rollbrocker B, Waha A, Fimmers R, Volk B, Warnke P, Ostertag CB, Wiestler OD, von Deimling A (1999) Molecular genetic analysis as a tool for evaluating stereotactic biopsies of glioma specimens. J Neuropathol Exp Neurol 58:40–45CrossRefPubMed Muller MB, Schmidt MC, Schmidt O, Hayashi Y, Rollbrocker B, Waha A, Fimmers R, Volk B, Warnke P, Ostertag CB, Wiestler OD, von Deimling A (1999) Molecular genetic analysis as a tool for evaluating stereotactic biopsies of glioma specimens. J Neuropathol Exp Neurol 58:40–45CrossRefPubMed
33.
go back to reference Jackson RJ, Fuller GN, Abi-Said D, Lang FF, Gokaslan ZL, Shi WM, Wildrick DM, Sawaya R (2001) Limitations of stereotactic biopsy in the initial management of gliomas. Neuro Oncol 3:193–200PubMedCentralPubMed Jackson RJ, Fuller GN, Abi-Said D, Lang FF, Gokaslan ZL, Shi WM, Wildrick DM, Sawaya R (2001) Limitations of stereotactic biopsy in the initial management of gliomas. Neuro Oncol 3:193–200PubMedCentralPubMed
34.
go back to reference Thon N, Eigenbrod S, Grasbon-Frodl EM, Ruiter M, Mehrkens JH, Kreth S, Tonn JC, Kretzschmar HA, Kreth FW (2009) Novel molecular stereotactic biopsy procedures reveal intratumoral homogeneity of loss of heterozygosity of 1p/19q and TP53 mutations in World Health Organization grade II gliomas. J Neuropathol Exp Neurol 68:1219–1228. doi:10.1097/NEN.0b013e3181bee1f1 CrossRefPubMed Thon N, Eigenbrod S, Grasbon-Frodl EM, Ruiter M, Mehrkens JH, Kreth S, Tonn JC, Kretzschmar HA, Kreth FW (2009) Novel molecular stereotactic biopsy procedures reveal intratumoral homogeneity of loss of heterozygosity of 1p/19q and TP53 mutations in World Health Organization grade II gliomas. J Neuropathol Exp Neurol 68:1219–1228. doi:10.​1097/​NEN.​0b013e3181bee1f1​ CrossRefPubMed
35.
go back to reference Olson JJ, Barnett D, Yang J, Assietti R, Cotsonis G, James CD (1998) Gene amplification as a prognostic factor in primary brain tumors. Clin Cancer Res 4:215–222PubMed Olson JJ, Barnett D, Yang J, Assietti R, Cotsonis G, James CD (1998) Gene amplification as a prognostic factor in primary brain tumors. Clin Cancer Res 4:215–222PubMed
37.
go back to reference Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LA Jr, Hartigan J, Smith DR, Strausberg RL, Marie SK, Shinjo SM, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807–1812. doi:10.1126/science.1164382 PubMedCentralCrossRefPubMed Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LA Jr, Hartigan J, Smith DR, Strausberg RL, Marie SK, Shinjo SM, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807–1812. doi:10.​1126/​science.​1164382 PubMedCentralCrossRefPubMed
39.
go back to reference Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, Reardon D, Herndon J, Kinzler KW, Velculescu VE, Vogelstein B, Bigner DD (2009) IDH1 and IDH2 mutations in gliomas. The New England journal of medicine 360:765–773. doi:10.1056/NEJMoa0808710 PubMedCentralCrossRefPubMed Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, Reardon D, Herndon J, Kinzler KW, Velculescu VE, Vogelstein B, Bigner DD (2009) IDH1 and IDH2 mutations in gliomas. The New England journal of medicine 360:765–773. doi:10.​1056/​NEJMoa0808710 PubMedCentralCrossRefPubMed
40.
go back to reference Hartmann C, Meyer J, Balss J, Capper D, Mueller W, Christians A, Felsberg J, Wolter M, Mawrin C, Wick W, Weller M, Herold-Mende C, Unterberg A, Jeuken JW, Wesseling P, Reifenberger G, von Deimling A (2009) Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: a study of 1,010 diffuse gliomas. Acta Neuropathol 118:469–474. doi:10.1007/s00401-009-0561-9 CrossRefPubMed Hartmann C, Meyer J, Balss J, Capper D, Mueller W, Christians A, Felsberg J, Wolter M, Mawrin C, Wick W, Weller M, Herold-Mende C, Unterberg A, Jeuken JW, Wesseling P, Reifenberger G, von Deimling A (2009) Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: a study of 1,010 diffuse gliomas. Acta Neuropathol 118:469–474. doi:10.​1007/​s00401-009-0561-9 CrossRefPubMed
42.
go back to reference van den Bent MJ, Hartmann C, Preusser M, Strobel T, Dubbink HJ, Kros JM, von Deimling A, Boisselier B, Sanson M, Halling KC, Diefes KL, Aldape K, Giannini C (2013) Interlaboratory comparison of IDH mutation detection. J Neurooncol 112:173–178. doi:10.1007/s11060-013-1056-z CrossRefPubMed van den Bent MJ, Hartmann C, Preusser M, Strobel T, Dubbink HJ, Kros JM, von Deimling A, Boisselier B, Sanson M, Halling KC, Diefes KL, Aldape K, Giannini C (2013) Interlaboratory comparison of IDH mutation detection. J Neurooncol 112:173–178. doi:10.​1007/​s11060-013-1056-z CrossRefPubMed
43.
go back to reference Thon N, Eigenbrod S, Kreth S, Lutz J, Tonn JC, Kretzschmar H, Peraud A, Kreth FW (2012) IDH1 mutations in grade II astrocytomas are associated with unfavorable progression-free survival and prolonged postrecurrence survival. Cancer 118:452–460. doi:10.1002/cncr.26298 CrossRefPubMed Thon N, Eigenbrod S, Kreth S, Lutz J, Tonn JC, Kretzschmar H, Peraud A, Kreth FW (2012) IDH1 mutations in grade II astrocytomas are associated with unfavorable progression-free survival and prolonged postrecurrence survival. Cancer 118:452–460. doi:10.​1002/​cncr.​26298 CrossRefPubMed
44.
go back to reference Dubbink HJ, Taal W, van Marion R, Kros JM, van Heuvel I, Bromberg JE, Zonnenberg BA, Zonnenberg CB, Postma TJ, Gijtenbeek JM, Boogerd W, Groenendijk FH, Smitt PA, Dinjens WN, van den Bent MJ (2009) IDH1 mutations in low-grade astrocytomas predict survival but not response to temozolomide. Neurology 73:1792–1795. doi:10.1212/WNL.0b013e3181c34ace CrossRefPubMed Dubbink HJ, Taal W, van Marion R, Kros JM, van Heuvel I, Bromberg JE, Zonnenberg BA, Zonnenberg CB, Postma TJ, Gijtenbeek JM, Boogerd W, Groenendijk FH, Smitt PA, Dinjens WN, van den Bent MJ (2009) IDH1 mutations in low-grade astrocytomas predict survival but not response to temozolomide. Neurology 73:1792–1795. doi:10.​1212/​WNL.​0b013e3181c34ace​ CrossRefPubMed
45.
go back to reference Hartmann C, Hentschel B, Tatagiba M, Schramm J, Schnell O, Seidel C, Stein R, Reifenberger G, Pietsch T, von Deimling A, Loeffler M, Weller M, German Glioma N (2011) Molecular markers in low-grade gliomas: predictive or prognostic? Clin Cancer Res 17:4588–4599. doi:10.1158/1078-0432.CCR-10-3194 CrossRefPubMed Hartmann C, Hentschel B, Tatagiba M, Schramm J, Schnell O, Seidel C, Stein R, Reifenberger G, Pietsch T, von Deimling A, Loeffler M, Weller M, German Glioma N (2011) Molecular markers in low-grade gliomas: predictive or prognostic? Clin Cancer Res 17:4588–4599. doi:10.​1158/​1078-0432.​CCR-10-3194 CrossRefPubMed
46.
go back to reference Metellus P, Coulibaly B, Colin C, de Paula AM, Vasiljevic A, Taieb D, Barlier A, Boisselier B, Mokhtari K, Wang XW, Loundou A, Chapon F, Pineau S, Ouafik L, Chinot O, Figarella-Branger D (2010) Absence of IDH mutation identifies a novel radiologic and molecular subtype of WHO grade II gliomas with dismal prognosis. Acta Neuropathol 120:719–729. doi:10.1007/s00401-010-0777-8 CrossRefPubMed Metellus P, Coulibaly B, Colin C, de Paula AM, Vasiljevic A, Taieb D, Barlier A, Boisselier B, Mokhtari K, Wang XW, Loundou A, Chapon F, Pineau S, Ouafik L, Chinot O, Figarella-Branger D (2010) Absence of IDH mutation identifies a novel radiologic and molecular subtype of WHO grade II gliomas with dismal prognosis. Acta Neuropathol 120:719–729. doi:10.​1007/​s00401-010-0777-8 CrossRefPubMed
47.
go back to reference Sanson M, Marie Y, Paris S, Idbaih A, Laffaire J, Ducray F, El Hallani S, Boisselier B, Mokhtari K, Hoang-Xuan K, Delattre JY (2009) Isocitrate dehydrogenase 1 codon 132 mutation is an important prognostic biomarker in gliomas. J Clin Oncol 27:4150–4154. doi:10.1200/JCO.2009.21.9832 CrossRefPubMed Sanson M, Marie Y, Paris S, Idbaih A, Laffaire J, Ducray F, El Hallani S, Boisselier B, Mokhtari K, Hoang-Xuan K, Delattre JY (2009) Isocitrate dehydrogenase 1 codon 132 mutation is an important prognostic biomarker in gliomas. J Clin Oncol 27:4150–4154. doi:10.​1200/​JCO.​2009.​21.​9832 CrossRefPubMed
48.
go back to reference Ahmadi R, Stockhammer F, Becker N, Hohlen K, Misch M, Christians A, Dictus C, Herold-Mende C, Capper D, Unterberg A, von Deimling A, Wick W, Hartmann C (2012) No prognostic value of IDH1 mutations in a series of 100 WHO grade II astrocytomas. J Neurooncol 109:15–22. doi:10.1007/s11060-012-0863-y CrossRefPubMed Ahmadi R, Stockhammer F, Becker N, Hohlen K, Misch M, Christians A, Dictus C, Herold-Mende C, Capper D, Unterberg A, von Deimling A, Wick W, Hartmann C (2012) No prognostic value of IDH1 mutations in a series of 100 WHO grade II astrocytomas. J Neurooncol 109:15–22. doi:10.​1007/​s11060-012-0863-y CrossRefPubMed
49.
go back to reference Korshunov A, Meyer J, Capper D, Christians A, Remke M, Witt H, Pfister S, von Deimling A, Hartmann C (2009) Combined molecular analysis of BRAF and IDH1 distinguishes pilocytic astrocytoma from diffuse astrocytoma. Acta Neuropathol 118:401–405. doi:10.1007/s00401-009-0550-z CrossRefPubMed Korshunov A, Meyer J, Capper D, Christians A, Remke M, Witt H, Pfister S, von Deimling A, Hartmann C (2009) Combined molecular analysis of BRAF and IDH1 distinguishes pilocytic astrocytoma from diffuse astrocytoma. Acta Neuropathol 118:401–405. doi:10.​1007/​s00401-009-0550-z CrossRefPubMed
50.
go back to reference Capper D, Sahm F, Hartmann C, Meyermann R, von Deimling A, Schittenhelm J (2010) Application of mutant IDH1 antibody to differentiate diffuse glioma from nonneoplastic central nervous system lesions and therapy-induced changes. Am J Surg Pathol 34:1199–1204. doi:10.1097/PAS.0b013e3181e7740d CrossRefPubMed Capper D, Sahm F, Hartmann C, Meyermann R, von Deimling A, Schittenhelm J (2010) Application of mutant IDH1 antibody to differentiate diffuse glioma from nonneoplastic central nervous system lesions and therapy-induced changes. Am J Surg Pathol 34:1199–1204. doi:10.​1097/​PAS.​0b013e3181e7740d​ CrossRefPubMed
51.
go back to reference Capper D, Reuss D, Schittenhelm J, Hartmann C, Bremer J, Sahm F, Harter PN, Jeibmann A, von Deimling A (2011) Mutation-specific IDH1 antibody differentiates oligodendrogliomas and oligoastrocytomas from other brain tumors with oligodendroglioma-like morphology. Acta Neuropathol 121:241–252. doi:10.1007/s00401-010-0770-2 CrossRefPubMed Capper D, Reuss D, Schittenhelm J, Hartmann C, Bremer J, Sahm F, Harter PN, Jeibmann A, von Deimling A (2011) Mutation-specific IDH1 antibody differentiates oligodendrogliomas and oligoastrocytomas from other brain tumors with oligodendroglioma-like morphology. Acta Neuropathol 121:241–252. doi:10.​1007/​s00401-010-0770-2 CrossRefPubMed
52.
53.
go back to reference Pope WB, Prins RM, Albert Thomas M, Nagarajan R, Yen KE, Bittinger MA, Salamon N, Chou AP, Yong WH, Soto H, Wilson N, Driggers E, Jang HG, Su SM, Schenkein DP, Lai A, Cloughesy TF, Kornblum HI, Wu H, Fantin VR, Liau LM (2012) Non-invasive detection of 2-hydroxyglutarate and other metabolites in IDH1 mutant glioma patients using magnetic resonance spectroscopy. J Neurooncol 107:197–205. doi:10.1007/s11060-011-0737-8 PubMedCentralCrossRefPubMed Pope WB, Prins RM, Albert Thomas M, Nagarajan R, Yen KE, Bittinger MA, Salamon N, Chou AP, Yong WH, Soto H, Wilson N, Driggers E, Jang HG, Su SM, Schenkein DP, Lai A, Cloughesy TF, Kornblum HI, Wu H, Fantin VR, Liau LM (2012) Non-invasive detection of 2-hydroxyglutarate and other metabolites in IDH1 mutant glioma patients using magnetic resonance spectroscopy. J Neurooncol 107:197–205. doi:10.​1007/​s11060-011-0737-8 PubMedCentralCrossRefPubMed
54.
go back to reference Andronesi OC, Kim GS, Gerstner E, Batchelor T, Tzika AA, Fantin VR, Vander Heiden MG, Sorensen AG (2012) Detection of 2-hydroxyglutarate in IDH-mutated glioma patients by in vivo spectral-editing and 2D correlation magnetic resonance spectroscopy. Science translational medicine 4: 116ra-114 doi:10.1126/scitranslmed.3002693 Andronesi OC, Kim GS, Gerstner E, Batchelor T, Tzika AA, Fantin VR, Vander Heiden MG, Sorensen AG (2012) Detection of 2-hydroxyglutarate in IDH-mutated glioma patients by in vivo spectral-editing and 2D correlation magnetic resonance spectroscopy. Science translational medicine 4: 116ra-114 doi:10.​1126/​scitranslmed.​3002693
55.
go back to reference Choi C, Ganji SK, DeBerardinis RJ, Hatanpaa KJ, Rakheja D, Kovacs Z, Yang XL, Mashimo T, Raisanen JM, Marin-Valencia I, Pascual JM, Madden CJ, Mickey BE, Malloy CR, Bachoo RM, Maher EA (2012) 2-hydroxyglutarate detection by magnetic resonance spectroscopy in IDH-mutated patients with gliomas. Nat Med 18:624–629. doi:10.1038/nm.2682 PubMedCentralCrossRefPubMed Choi C, Ganji SK, DeBerardinis RJ, Hatanpaa KJ, Rakheja D, Kovacs Z, Yang XL, Mashimo T, Raisanen JM, Marin-Valencia I, Pascual JM, Madden CJ, Mickey BE, Malloy CR, Bachoo RM, Maher EA (2012) 2-hydroxyglutarate detection by magnetic resonance spectroscopy in IDH-mutated patients with gliomas. Nat Med 18:624–629. doi:10.​1038/​nm.​2682 PubMedCentralCrossRefPubMed
56.
go back to reference Elkhaled A, Jalbert LE, Phillips JJ, Yoshihara HA, Parvataneni R, Srinivasan R, Bourne G, Berger MS, Chang SM, Cha S, Nelson SJ (2012) Magnetic resonance of 2-hydroxyglutarate in IDH1-mutated low-grade gliomas. Science translational medicine 4: 116ra115 doi:10.1126/scitranslmed.3002796 Elkhaled A, Jalbert LE, Phillips JJ, Yoshihara HA, Parvataneni R, Srinivasan R, Bourne G, Berger MS, Chang SM, Cha S, Nelson SJ (2012) Magnetic resonance of 2-hydroxyglutarate in IDH1-mutated low-grade gliomas. Science translational medicine 4: 116ra115 doi:10.​1126/​scitranslmed.​3002796
57.
go back to reference Kalinina J, Carroll A, Wang L, Yu Q, Mancheno DE, Wu S, Liu F, Ahn J, He M, Mao H, Van Meir EG (2012) Detection of “oncometabolite” 2-hydroxyglutarate by magnetic resonance analysis as a biomarker of IDH1/2 mutations in glioma. J Mol Med 90:1161–1171. doi:10.1007/s00109-012-0888-x PubMedCentralCrossRefPubMed Kalinina J, Carroll A, Wang L, Yu Q, Mancheno DE, Wu S, Liu F, Ahn J, He M, Mao H, Van Meir EG (2012) Detection of “oncometabolite” 2-hydroxyglutarate by magnetic resonance analysis as a biomarker of IDH1/2 mutations in glioma. J Mol Med 90:1161–1171. doi:10.​1007/​s00109-012-0888-x PubMedCentralCrossRefPubMed
58.
go back to reference Smith JS, Alderete B, Minn Y, Borell TJ, Perry A, Mohapatra G, Hosek SM, Kimmel D, O’Fallon J, Yates A, Feuerstein BG, Burger PC, Scheithauer BW, Jenkins RB (1999) Localization of common deletion regions on 1p and 19q in human gliomas and their association with histological subtype. Oncogene 18:4144–4152. doi:10.1038/sj.onc.1202759 CrossRefPubMed Smith JS, Alderete B, Minn Y, Borell TJ, Perry A, Mohapatra G, Hosek SM, Kimmel D, O’Fallon J, Yates A, Feuerstein BG, Burger PC, Scheithauer BW, Jenkins RB (1999) Localization of common deletion regions on 1p and 19q in human gliomas and their association with histological subtype. Oncogene 18:4144–4152. doi:10.​1038/​sj.​onc.​1202759 CrossRefPubMed
59.
go back to reference Smith JS, Perry A, Borell TJ, Lee HK, O’Fallon J, Hosek SM, Kimmel D, Yates A, Burger PC, Scheithauer BW, Jenkins RB (2000) Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18:636–645PubMed Smith JS, Perry A, Borell TJ, Lee HK, O’Fallon J, Hosek SM, Kimmel D, Yates A, Burger PC, Scheithauer BW, Jenkins RB (2000) Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18:636–645PubMed
60.
go back to reference Reifenberger J, Reifenberger G, Liu L, James CD, Wechsler W, Collins VP (1994) Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol 145:1175–1190PubMedCentralPubMed Reifenberger J, Reifenberger G, Liu L, James CD, Wechsler W, Collins VP (1994) Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol 145:1175–1190PubMedCentralPubMed
61.
62.
go back to reference Iuchi T, Namba H, Iwadate Y, Shishikura T, Kageyama H, Nakamura Y, Ohira M, Yamaura A, Osato K, Sakiyama S, Nakagawara A (2002) Identification of the small interstitial deletion at chromosome band 1p34-p35 and its association with poor outcome in oligodendroglial tumors. Genes Chromosom Cancer 35:170–175. doi:10.1002/gcc.10080 CrossRefPubMed Iuchi T, Namba H, Iwadate Y, Shishikura T, Kageyama H, Nakamura Y, Ohira M, Yamaura A, Osato K, Sakiyama S, Nakagawara A (2002) Identification of the small interstitial deletion at chromosome band 1p34-p35 and its association with poor outcome in oligodendroglial tumors. Genes Chromosom Cancer 35:170–175. doi:10.​1002/​gcc.​10080 CrossRefPubMed
63.
go back to reference Cairncross JG, Ueki K, Zlatescu MC, Lisle DK, Finkelstein DM, Hammond RR, Silver JS, Stark PC, Macdonald DR, Ino Y, Ramsay DA, Louis DN (1998) Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst 90:1473–1479CrossRefPubMed Cairncross JG, Ueki K, Zlatescu MC, Lisle DK, Finkelstein DM, Hammond RR, Silver JS, Stark PC, Macdonald DR, Ino Y, Ramsay DA, Louis DN (1998) Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst 90:1473–1479CrossRefPubMed
65.
go back to reference van den Bent MJ, Brandes AA, Taphoorn MJ, Kros JM, Kouwenhoven MC, Delattre JY, Bernsen HJ, Frenay M, Tijssen CC, Grisold W, Sipos L, Enting RH, French PJ, Dinjens WN, Vecht CJ, Allgeier A, Lacombe D, Gorlia T, Hoang-Xuan K (2013) Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin Oncol 31:344–350. doi:10.1200/JCO.2012.43.2229 CrossRefPubMed van den Bent MJ, Brandes AA, Taphoorn MJ, Kros JM, Kouwenhoven MC, Delattre JY, Bernsen HJ, Frenay M, Tijssen CC, Grisold W, Sipos L, Enting RH, French PJ, Dinjens WN, Vecht CJ, Allgeier A, Lacombe D, Gorlia T, Hoang-Xuan K (2013) Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin Oncol 31:344–350. doi:10.​1200/​JCO.​2012.​43.​2229 CrossRefPubMed
66.
go back to reference Ochsenbein AF, Schubert AD, Vassella E, Mariani L (2011) Quantitative analysis of O6-methylguanine DNA methyltransferase (MGMT) promoter methylation in patients with low-grade gliomas. J Neurooncol 103:343–351. doi:10.1007/s11060-010-0395-2 CrossRefPubMed Ochsenbein AF, Schubert AD, Vassella E, Mariani L (2011) Quantitative analysis of O6-methylguanine DNA methyltransferase (MGMT) promoter methylation in patients with low-grade gliomas. J Neurooncol 103:343–351. doi:10.​1007/​s11060-010-0395-2 CrossRefPubMed
67.
go back to reference Jenkins RB, Blair H, Ballman KV, Giannini C, Arusell RM, Law M, Flynn H, Passe S, Felten S, Brown PD, Shaw EG, Buckner JC (2006) 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 66:9852–9861. doi:10.1158/0008-5472.CAN-06-1796 CrossRefPubMed Jenkins RB, Blair H, Ballman KV, Giannini C, Arusell RM, Law M, Flynn H, Passe S, Felten S, Brown PD, Shaw EG, Buckner JC (2006) 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 66:9852–9861. doi:10.​1158/​0008-5472.​CAN-06-1796 CrossRefPubMed
69.
go back to reference Bettegowda C, Agrawal N, Jiao Y, Sausen M, Wood LD, Hruban RH, Rodriguez FJ, Cahill DP, McLendon R, Riggins G, Velculescu VE, Oba-Shinjo SM, Marie SK, Vogelstein B, Bigner D, Yan H, Papadopoulos N, Kinzler KW (2011) Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 333:1453–1455. doi:10.1126/science.1210557 PubMedCentralCrossRefPubMed Bettegowda C, Agrawal N, Jiao Y, Sausen M, Wood LD, Hruban RH, Rodriguez FJ, Cahill DP, McLendon R, Riggins G, Velculescu VE, Oba-Shinjo SM, Marie SK, Vogelstein B, Bigner D, Yan H, Papadopoulos N, Kinzler KW (2011) Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 333:1453–1455. doi:10.​1126/​science.​1210557 PubMedCentralCrossRefPubMed
70.
go back to reference Yip S, Butterfield YS, Morozova O, Chittaranjan S, Blough MD, An J, Birol I, Chesnelong C, Chiu R, Chuah E, Corbett R, Docking R, Firme M, Hirst M, Jackman S, Karsan A, Li H, Louis DN, Maslova A, Moore R, Moradian A, Mungall KL, Perizzolo M, Qian J, Roldan G, Smith EE, Tamura-Wells J, Thiessen N, Varhol R, Weiss S, Wu W, Young S, Zhao Y, Mungall AJ, Jones SJ, Morin GB, Chan JA, Cairncross JG, Marra MA (2012) Concurrent CIC mutations, IDH mutations, and 1p/19q loss distinguish oligodendrogliomas from other cancers. J Pathol 226:7–16. doi:10.1002/path.2995 PubMedCentralCrossRefPubMed Yip S, Butterfield YS, Morozova O, Chittaranjan S, Blough MD, An J, Birol I, Chesnelong C, Chiu R, Chuah E, Corbett R, Docking R, Firme M, Hirst M, Jackman S, Karsan A, Li H, Louis DN, Maslova A, Moore R, Moradian A, Mungall KL, Perizzolo M, Qian J, Roldan G, Smith EE, Tamura-Wells J, Thiessen N, Varhol R, Weiss S, Wu W, Young S, Zhao Y, Mungall AJ, Jones SJ, Morin GB, Chan JA, Cairncross JG, Marra MA (2012) Concurrent CIC mutations, IDH mutations, and 1p/19q loss distinguish oligodendrogliomas from other cancers. J Pathol 226:7–16. doi:10.​1002/​path.​2995 PubMedCentralCrossRefPubMed
71.
go back to reference Labussiere M, Idbaih A, Wang XW, Marie Y, Boisselier B, Falet C, Paris S, Laffaire J, Carpentier C, Criniere E, Ducray F, El Hallani S, Mokhtari K, Hoang-Xuan K, Delattre JY, Sanson M (2010) All the 1p19q codeleted gliomas are mutated on IDH1 or IDH2. Neurology 74:1886–1890. doi:10.1212/WNL.0b013e3181e1cf3a CrossRefPubMed Labussiere M, Idbaih A, Wang XW, Marie Y, Boisselier B, Falet C, Paris S, Laffaire J, Carpentier C, Criniere E, Ducray F, El Hallani S, Mokhtari K, Hoang-Xuan K, Delattre JY, Sanson M (2010) All the 1p19q codeleted gliomas are mutated on IDH1 or IDH2. Neurology 74:1886–1890. doi:10.​1212/​WNL.​0b013e3181e1cf3a​ CrossRefPubMed
72.
go back to reference Killela PJ, Reitman ZJ, Jiao Y, Bettegowda C, Agrawal N, Diaz LA Jr, Friedman AH, Friedman H, Gallia GL, Giovanella BC, Grollman AP, He TC, He Y, Hruban RH, Jallo GI, Mandahl N, Meeker AK, Mertens F, Netto GJ, Rasheed BA, Riggins GJ, Rosenquist TA, Schiffman M, Shih Ie M, Theodorescu D, Torbenson MS, Velculescu VE, Wang TL, Wentzensen N, Wood LD, Zhang M, McLendon RE, Bigner DD, Kinzler KW, Vogelstein B, Papadopoulos N, Yan H (2013) TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc Nat Acad Sci United States of Am 110:6021–6026. doi:10.1073/pnas.1303607110 CrossRef Killela PJ, Reitman ZJ, Jiao Y, Bettegowda C, Agrawal N, Diaz LA Jr, Friedman AH, Friedman H, Gallia GL, Giovanella BC, Grollman AP, He TC, He Y, Hruban RH, Jallo GI, Mandahl N, Meeker AK, Mertens F, Netto GJ, Rasheed BA, Riggins GJ, Rosenquist TA, Schiffman M, Shih Ie M, Theodorescu D, Torbenson MS, Velculescu VE, Wang TL, Wentzensen N, Wood LD, Zhang M, McLendon RE, Bigner DD, Kinzler KW, Vogelstein B, Papadopoulos N, Yan H (2013) TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc Nat Acad Sci United States of Am 110:6021–6026. doi:10.​1073/​pnas.​1303607110 CrossRef
73.
go back to reference Jiao Y, Killela PJ, Reitman ZJ, Rasheed AB, Heaphy CM, de Wilde RF, Rodriguez FJ, Rosemberg S, Oba-Shinjo SM, Nagahashi Marie SK, Bettegowda C, Agrawal N, Lipp E, Pirozzi C, Lopez G, He Y, Friedman H, Friedman AH, Riggins GJ, Holdhoff M, Burger P, McLendon R, Bigner DD, Vogelstein B, Meeker AK, Kinzler KW, Papadopoulos N, Diaz LA, Yan H (2012) Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas. Oncotarget 3:709–722PubMedCentralCrossRefPubMed Jiao Y, Killela PJ, Reitman ZJ, Rasheed AB, Heaphy CM, de Wilde RF, Rodriguez FJ, Rosemberg S, Oba-Shinjo SM, Nagahashi Marie SK, Bettegowda C, Agrawal N, Lipp E, Pirozzi C, Lopez G, He Y, Friedman H, Friedman AH, Riggins GJ, Holdhoff M, Burger P, McLendon R, Bigner DD, Vogelstein B, Meeker AK, Kinzler KW, Papadopoulos N, Diaz LA, Yan H (2012) Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas. Oncotarget 3:709–722PubMedCentralCrossRefPubMed
74.
go back to reference Louis DN, Perry A, Burger P, Ellison DW, Reifenberger G, von Deimling A, Aldape K, Brat D, Collins VP, Eberhart C, Figarella-Branger D, Fuller GN, Giangaspero F, Giannini C, Hawkins C, Kleihues P, Korshunov A, Kros JM, Lopes MB, Ng HK, Ohgaki H, Paulus W, Pietsch T, Rosenblum M, Rushing E, Soylemezoglu F, Wiestler O, Wesseling P (2014) International Society of Neuropathology-Haarlem Consensus Guidelines, for Nervous System Tumor Classification and Grading. Brain Pathol. doi:10.1111/bpa.12171 Louis DN, Perry A, Burger P, Ellison DW, Reifenberger G, von Deimling A, Aldape K, Brat D, Collins VP, Eberhart C, Figarella-Branger D, Fuller GN, Giangaspero F, Giannini C, Hawkins C, Kleihues P, Korshunov A, Kros JM, Lopes MB, Ng HK, Ohgaki H, Paulus W, Pietsch T, Rosenblum M, Rushing E, Soylemezoglu F, Wiestler O, Wesseling P (2014) International Society of Neuropathology-Haarlem Consensus Guidelines, for Nervous System Tumor Classification and Grading. Brain Pathol. doi:10.​1111/​bpa.​12171
75.
go back to reference Nakamura M, Watanabe T, Yonekawa Y, Kleihues P, Ohgaki H (2001) Promoter methylation of the DNA repair gene MGMT in astrocytomas is frequently associated with G: C – > A: T mutations of the TP53 tumor suppressor gene. Carcinogenesis 22:1715–1719CrossRefPubMed Nakamura M, Watanabe T, Yonekawa Y, Kleihues P, Ohgaki H (2001) Promoter methylation of the DNA repair gene MGMT in astrocytomas is frequently associated with G: C – > A: T mutations of the TP53 tumor suppressor gene. Carcinogenesis 22:1715–1719CrossRefPubMed
76.
go back to reference Groenendijk FH, Taal W, Dubbink HJ, Haarloo CR, Kouwenhoven MC, van den Bent MJ, Kros JM, Dinjens WN (2011) MGMT promoter hypermethylation is a frequent, early, and consistent event in astrocytoma progression, and not correlated with TP53 mutation. J Neurooncol 101:405–417. doi:10.1007/s11060-010-0274-x PubMedCentralCrossRefPubMed Groenendijk FH, Taal W, Dubbink HJ, Haarloo CR, Kouwenhoven MC, van den Bent MJ, Kros JM, Dinjens WN (2011) MGMT promoter hypermethylation is a frequent, early, and consistent event in astrocytoma progression, and not correlated with TP53 mutation. J Neurooncol 101:405–417. doi:10.​1007/​s11060-010-0274-x PubMedCentralCrossRefPubMed
77.
go back to reference Taal W, Dubbink HJ, Zonnenberg CB, Zonnenberg BA, Postma TJ, Gijtenbeek JM, Boogerd W, Groenendijk FH, Kros JM, Kouwenhoven MC, van Marion R, van Heuvel I, van der Holt B, Bromberg JE, Sillevis Smitt PA, Dinjens WN, van den Bent MJ, Dutch Society for N-O (2011) First-line temozolomide chemotherapy in progressive low-grade astrocytomas after radiotherapy: molecular characteristics in relation to response. Neuro Oncol 13:235–241. doi:10.1093/neuonc/noq177 PubMedCentralCrossRefPubMed Taal W, Dubbink HJ, Zonnenberg CB, Zonnenberg BA, Postma TJ, Gijtenbeek JM, Boogerd W, Groenendijk FH, Kros JM, Kouwenhoven MC, van Marion R, van Heuvel I, van der Holt B, Bromberg JE, Sillevis Smitt PA, Dinjens WN, van den Bent MJ, Dutch Society for N-O (2011) First-line temozolomide chemotherapy in progressive low-grade astrocytomas after radiotherapy: molecular characteristics in relation to response. Neuro Oncol 13:235–241. doi:10.​1093/​neuonc/​noq177 PubMedCentralCrossRefPubMed
78.
go back to reference Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, Verhaak RG, Hoadley KA, Hayes DN, Perou CM, Schmidt HK, Ding L, Wilson RK, Van Den Berg D, Shen H, Bengtsson H, Neuvial P, Cope LM, Buckley J, Herman JG, Baylin SB, Laird PW, Aldape K, Cancer Genome Atlas Research N (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17:510–522. doi:10.1016/j.ccr.2010.03.017 PubMedCentralCrossRefPubMed Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, Verhaak RG, Hoadley KA, Hayes DN, Perou CM, Schmidt HK, Ding L, Wilson RK, Van Den Berg D, Shen H, Bengtsson H, Neuvial P, Cope LM, Buckley J, Herman JG, Baylin SB, Laird PW, Aldape K, Cancer Genome Atlas Research N (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17:510–522. doi:10.​1016/​j.​ccr.​2010.​03.​017 PubMedCentralCrossRefPubMed
79.
go back to reference Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, Baylin SB, Herman JG (2000) Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 343:1350–1354. doi:10.1056/NEJM200011093431901 CrossRefPubMed Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, Baylin SB, Herman JG (2000) Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 343:1350–1354. doi:10.​1056/​NEJM200011093431​901 CrossRefPubMed
80.
go back to reference Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003. doi:10.1056/NEJMoa043331 CrossRefPubMed Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003. doi:10.​1056/​NEJMoa043331 CrossRefPubMed
81.
go back to reference McKeever PE, Ross DA, Strawderman MS, Brunberg JA, Greenberg HS, Junck L (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 56:798–805CrossRefPubMed McKeever PE, Ross DA, Strawderman MS, Brunberg JA, Greenberg HS, Junck L (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 56:798–805CrossRefPubMed
82.
go back to reference Mork SJ, Halvorsen TB, Lindegaard KF, Eide GE (1986) Oligodendroglioma. Histologic evaluation and prognosis. J Neuropathol Exp Neurol 45:65–78CrossRefPubMed Mork SJ, Halvorsen TB, Lindegaard KF, Eide GE (1986) Oligodendroglioma. Histologic evaluation and prognosis. J Neuropathol Exp Neurol 45:65–78CrossRefPubMed
83.
go back to reference Burger PC, Rawlings CE, Cox EB, McLendon RE, Schold SC Jr, Bullard DE (1987) Clinicopathologic correlations in the oligodendroglioma. Cancer 59:1345–1352CrossRefPubMed Burger PC, Rawlings CE, Cox EB, McLendon RE, Schold SC Jr, Bullard DE (1987) Clinicopathologic correlations in the oligodendroglioma. Cancer 59:1345–1352CrossRefPubMed
84.
go back to reference Coons SW, Johnson PC, Pearl DK (1997) The prognostic significance of Ki-67 labeling indices for oligodendrogliomas. Neurosurgery 41: 878–884; discussion 884–875 Coons SW, Johnson PC, Pearl DK (1997) The prognostic significance of Ki-67 labeling indices for oligodendrogliomas. Neurosurgery 41: 878–884; discussion 884–875
85.
go back to reference Dehghani F, Schachenmayr W, Laun A, Korf HW (1998) Prognostic implication of histopathological, immunohistochemical and clinical features of oligodendrogliomas: a study of 89 cases. Acta Neuropathol 95:493–504CrossRefPubMed Dehghani F, Schachenmayr W, Laun A, Korf HW (1998) Prognostic implication of histopathological, immunohistochemical and clinical features of oligodendrogliomas: a study of 89 cases. Acta Neuropathol 95:493–504CrossRefPubMed
87.
go back to reference Hsu DW, Louis DN, Efird JT, Hedley-Whyte ET (1997) Use of MIB-1 (Ki-67) immunoreactivity in differentiating grade II and grade III gliomas. J Neuropathol Exp Neurol 56:857–865CrossRefPubMed Hsu DW, Louis DN, Efird JT, Hedley-Whyte ET (1997) Use of MIB-1 (Ki-67) immunoreactivity in differentiating grade II and grade III gliomas. J Neuropathol Exp Neurol 56:857–865CrossRefPubMed
88.
go back to reference Nakamura M, Konishi N, Tsunoda S, Nakase H, Tsuzuki T, Aoki H, Sakitani H, Inui T, Sakaki T (2000) Analysis of prognostic and survival factors related to treatment of low-grade astrocytomas in adults. Oncology 58:108–116CrossRefPubMed Nakamura M, Konishi N, Tsunoda S, Nakase H, Tsuzuki T, Aoki H, Sakitani H, Inui T, Sakaki T (2000) Analysis of prognostic and survival factors related to treatment of low-grade astrocytomas in adults. Oncology 58:108–116CrossRefPubMed
89.
go back to reference Ralte AM, Sharma MC, Karak AK, Mehta VS, Sarkar C (2001) Clinicopathological features, MIB-1 labeling index and apoptotic index in recurrent astrocytic tumors. Pathol Oncol Res 7:267–278CrossRefPubMed Ralte AM, Sharma MC, Karak AK, Mehta VS, Sarkar C (2001) Clinicopathological features, MIB-1 labeling index and apoptotic index in recurrent astrocytic tumors. Pathol Oncol Res 7:267–278CrossRefPubMed
90.
go back to reference Hilton DA, Love S, Barber R, Ellison D, Sandeman DR (1998) Accumulation of p53 and Ki-67 expression do not predict survival in patients with fibrillary astrocytomas or the response of these tumors to radiotherapy. Neurosurgery 42:724–729CrossRefPubMed Hilton DA, Love S, Barber R, Ellison D, Sandeman DR (1998) Accumulation of p53 and Ki-67 expression do not predict survival in patients with fibrillary astrocytomas or the response of these tumors to radiotherapy. Neurosurgery 42:724–729CrossRefPubMed
92.
go back to reference Colman H, Giannini C, Huang L, Gonzalez J, Hess K, Bruner J, Fuller G, Langford L, Pelloski C, Aaron J, Burger P, Aldape K (2006) Assessment and prognostic significance of mitotic index using the mitosis marker phospho-histone H3 in low and intermediate-grade infiltrating astrocytomas. Am J Surg Pathol 30:657–664. doi:10.1097/01.pas.0000202048.28203.25 CrossRefPubMed Colman H, Giannini C, Huang L, Gonzalez J, Hess K, Bruner J, Fuller G, Langford L, Pelloski C, Aaron J, Burger P, Aldape K (2006) Assessment and prognostic significance of mitotic index using the mitosis marker phospho-histone H3 in low and intermediate-grade infiltrating astrocytomas. Am J Surg Pathol 30:657–664. doi:10.​1097/​01.​pas.​0000202048.​28203.​25 CrossRefPubMed
94.
go back to reference Torp SH (2002) Diagnostic and prognostic role of Ki67 immunostaining in human astrocytomas using four different antibodies. Clin Neuropathol 21:252–257PubMed Torp SH (2002) Diagnostic and prognostic role of Ki67 immunostaining in human astrocytomas using four different antibodies. Clin Neuropathol 21:252–257PubMed
95.
go back to reference Torp SH, Alsaker M (2002) Ki-67 immunoreactivity, basic fibroblastic growth factor (bFGF) expression, and microvessel density as supplementary prognostic tools in low-grade astrocytomas. An immunohistochemical study with special reference to the reliability of different Ki-67 antibodies. Pathol Res Pract 198:261–265. doi:10.1078/0344-0338-00252 PubMed Torp SH, Alsaker M (2002) Ki-67 immunoreactivity, basic fibroblastic growth factor (bFGF) expression, and microvessel density as supplementary prognostic tools in low-grade astrocytomas. An immunohistochemical study with special reference to the reliability of different Ki-67 antibodies. Pathol Res Pract 198:261–265. doi:10.​1078/​0344-0338-00252 PubMed
96.
go back to reference Cancer Genome Atlas Research N, Brat DJ, Verhaak RG, Aldape KD, Yung WK, Salama SR, Cooper LA, Rheinbay E, Miller CR, Vitucci M, Morozova O, Robertson AG, Noushmehr H, Laird PW, Cherniack AD, Akbani R, Huse JT, Ciriello G, Poisson LM, Barnholtz-Sloan JS, Berger MS, Brennan C, Colen RR, Colman H, Flanders AE, Giannini C, Grifford M, Iavarone A, Jain R, Joseph I, Kim J, Kasaian K, Mikkelsen T, Murray BA, O’Neill BP, Pachter L, Parsons DW, Sougnez C, Sulman EP, Vandenberg SR, Van Meir EG, von Deimling A, Zhang H, Crain D, Lau K, Mallery D, Morris S, Paulauskis J, Penny R, Shelton T, Sherman M, Yena P, Black A, Bowen J, Dicostanzo K, Gastier-Foster J, Leraas KM, Lichtenberg TM, Pierson CR, Ramirez NC, Taylor C, Weaver S, Wise L, Zmuda E, Davidsen T, Demchok JA, Eley G, Ferguson ML, Hutter CM, Mills Shaw KR, Ozenberger BA, Sheth M, Sofia HJ, Tarnuzzer R, Wang Z, Yang L, Zenklusen JC, Ayala B, Baboud J, Chudamani S, Jensen MA, Liu J, Pihl T, Raman R, Wan Y, Wu Y, Ally A, Auman JT, Balasundaram M, Balu S, Baylin SB, Beroukhim R, Bootwalla MS, Bowlby R, Bristow CA, Brooks D, Butterfield Y, Carlsen R, Carter S, Chin L, Chu A, Chuah E, Cibulskis K, Clarke A, Coetzee SG, Dhalla N, Fennell T, Fisher S, Gabriel S, Getz G, Gibbs R, Guin R, Hadjipanayis A, Hayes DN, Hinoue T, Hoadley K, Holt RA, Hoyle AP, Jefferys SR, Jones S, Jones CD, Kucherlapati R, Lai PH, Lander E, Lee S, Lichtenstein L, Ma Y, Maglinte DT, Mahadeshwar HS, Marra MA, Mayo M, Meng S, Meyerson ML, Mieczkowski PA, Moore RA, Mose LE, Mungall AJ, Pantazi A, Parfenov M, Park PJ, Parker JS, Perou CM, Protopopov A, Ren X, Roach J, Sabedot TS, Schein J, Schumacher SE, Seidman JG, Seth S, Shen H, Simons JV, Sipahimalani P, Soloway MG, Song X, Sun H, Tabak B, Tam A, Tan D, Tang J, Thiessen N, Triche T, Jr., Van Den Berg DJ, Veluvolu U, Waring S, Weisenberger DJ, Wilkerson MD, Wong T, Wu J, Xi L, Xu AW, Yang L, Zack TI, Zhang J, Aksoy BA, Arachchi H, Benz C, Bernard B, Carlin D, Cho J, DiCara D, Frazer S, Fuller GN, Gao J, Gehlenborg N, Haussler D, Heiman DI, Iype L, Jacobsen A, Ju Z, Katzman S, Kim H, Knijnenburg T, Kreisberg RB, Lawrence MS, Lee W, Leinonen K, Lin P, Ling S, Liu W, Liu Y, Liu Y, Lu Y, Mills G, Ng S, Noble MS, Paull E, Rao A, Reynolds S, Saksena G, Sanborn Z, Sander C, Schultz N, Senbabaoglu Y, Shen R, Shmulevich I, Sinha R, Stuart J, Sumer SO, Sun Y, Tasman N, Taylor BS, Voet D, Weinhold N, Weinstein JN, Yang D, Yoshihara K, Zheng S, Zhang W, Zou L, Abel T, Sadeghi S, Cohen ML, Eschbacher J, Hattab EM, Raghunathan A, Schniederjan MJ, Aziz D, Barnett G, Barrett W, Bigner DD, Boice L, Brewer C, Calatozzolo C, Campos B, Carlotti CG, Jr., Chan TA, Cuppini L, Curley E, Cuzzubbo S, Devine K, DiMeco F, Duell R, Elder JB, Fehrenbach A, Finocchiaro G, Friedman W, Fulop J, Gardner J, Hermes B, Herold-Mende C, Jungk C, Kendler A, Lehman NL, Lipp E, Liu O, Mandt R, McGraw M, McLendon R, McPherson C, Neder L, Nguyen P, Noss A, Nunziata R, Ostrom QT, Palmer C, Perin A, Pollo B, Potapov A, Potapova O, Rathmell WK, Rotin D, Scarpace L, Schilero C, Senecal K, Shimmel K, Shurkhay V, Sifri S, Singh R, Sloan AE, Smolenski K, Staugaitis SM, Steele R, Thorne L, Tirapelli DP, Unterberg A, Vallurupalli M, Wang Y, Warnick R, Williams F, Wolinsky Y, Bell S, Rosenberg M, Stewart C, Huang F, Grimsby JL, Radenbaugh AJ, Zhang J (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 372: 2481–2498. doi:10.1056/NEJMoa1402121 Cancer Genome Atlas Research N, Brat DJ, Verhaak RG, Aldape KD, Yung WK, Salama SR, Cooper LA, Rheinbay E, Miller CR, Vitucci M, Morozova O, Robertson AG, Noushmehr H, Laird PW, Cherniack AD, Akbani R, Huse JT, Ciriello G, Poisson LM, Barnholtz-Sloan JS, Berger MS, Brennan C, Colen RR, Colman H, Flanders AE, Giannini C, Grifford M, Iavarone A, Jain R, Joseph I, Kim J, Kasaian K, Mikkelsen T, Murray BA, O’Neill BP, Pachter L, Parsons DW, Sougnez C, Sulman EP, Vandenberg SR, Van Meir EG, von Deimling A, Zhang H, Crain D, Lau K, Mallery D, Morris S, Paulauskis J, Penny R, Shelton T, Sherman M, Yena P, Black A, Bowen J, Dicostanzo K, Gastier-Foster J, Leraas KM, Lichtenberg TM, Pierson CR, Ramirez NC, Taylor C, Weaver S, Wise L, Zmuda E, Davidsen T, Demchok JA, Eley G, Ferguson ML, Hutter CM, Mills Shaw KR, Ozenberger BA, Sheth M, Sofia HJ, Tarnuzzer R, Wang Z, Yang L, Zenklusen JC, Ayala B, Baboud J, Chudamani S, Jensen MA, Liu J, Pihl T, Raman R, Wan Y, Wu Y, Ally A, Auman JT, Balasundaram M, Balu S, Baylin SB, Beroukhim R, Bootwalla MS, Bowlby R, Bristow CA, Brooks D, Butterfield Y, Carlsen R, Carter S, Chin L, Chu A, Chuah E, Cibulskis K, Clarke A, Coetzee SG, Dhalla N, Fennell T, Fisher S, Gabriel S, Getz G, Gibbs R, Guin R, Hadjipanayis A, Hayes DN, Hinoue T, Hoadley K, Holt RA, Hoyle AP, Jefferys SR, Jones S, Jones CD, Kucherlapati R, Lai PH, Lander E, Lee S, Lichtenstein L, Ma Y, Maglinte DT, Mahadeshwar HS, Marra MA, Mayo M, Meng S, Meyerson ML, Mieczkowski PA, Moore RA, Mose LE, Mungall AJ, Pantazi A, Parfenov M, Park PJ, Parker JS, Perou CM, Protopopov A, Ren X, Roach J, Sabedot TS, Schein J, Schumacher SE, Seidman JG, Seth S, Shen H, Simons JV, Sipahimalani P, Soloway MG, Song X, Sun H, Tabak B, Tam A, Tan D, Tang J, Thiessen N, Triche T, Jr., Van Den Berg DJ, Veluvolu U, Waring S, Weisenberger DJ, Wilkerson MD, Wong T, Wu J, Xi L, Xu AW, Yang L, Zack TI, Zhang J, Aksoy BA, Arachchi H, Benz C, Bernard B, Carlin D, Cho J, DiCara D, Frazer S, Fuller GN, Gao J, Gehlenborg N, Haussler D, Heiman DI, Iype L, Jacobsen A, Ju Z, Katzman S, Kim H, Knijnenburg T, Kreisberg RB, Lawrence MS, Lee W, Leinonen K, Lin P, Ling S, Liu W, Liu Y, Liu Y, Lu Y, Mills G, Ng S, Noble MS, Paull E, Rao A, Reynolds S, Saksena G, Sanborn Z, Sander C, Schultz N, Senbabaoglu Y, Shen R, Shmulevich I, Sinha R, Stuart J, Sumer SO, Sun Y, Tasman N, Taylor BS, Voet D, Weinhold N, Weinstein JN, Yang D, Yoshihara K, Zheng S, Zhang W, Zou L, Abel T, Sadeghi S, Cohen ML, Eschbacher J, Hattab EM, Raghunathan A, Schniederjan MJ, Aziz D, Barnett G, Barrett W, Bigner DD, Boice L, Brewer C, Calatozzolo C, Campos B, Carlotti CG, Jr., Chan TA, Cuppini L, Curley E, Cuzzubbo S, Devine K, DiMeco F, Duell R, Elder JB, Fehrenbach A, Finocchiaro G, Friedman W, Fulop J, Gardner J, Hermes B, Herold-Mende C, Jungk C, Kendler A, Lehman NL, Lipp E, Liu O, Mandt R, McGraw M, McLendon R, McPherson C, Neder L, Nguyen P, Noss A, Nunziata R, Ostrom QT, Palmer C, Perin A, Pollo B, Potapov A, Potapova O, Rathmell WK, Rotin D, Scarpace L, Schilero C, Senecal K, Shimmel K, Shurkhay V, Sifri S, Singh R, Sloan AE, Smolenski K, Staugaitis SM, Steele R, Thorne L, Tirapelli DP, Unterberg A, Vallurupalli M, Wang Y, Warnick R, Williams F, Wolinsky Y, Bell S, Rosenberg M, Stewart C, Huang F, Grimsby JL, Radenbaugh AJ, Zhang J (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 372: 2481–2498. doi:10.​1056/​NEJMoa1402121
97.
go back to reference Gonda DD, Cheung VJ, Muller KA, Goyal A, Carter BS, Chen CC (2014) The cancer genome atlas expression profiles of low-grade gliomas. Neurosurg Focus 36:E23CrossRefPubMed Gonda DD, Cheung VJ, Muller KA, Goyal A, Carter BS, Chen CC (2014) The cancer genome atlas expression profiles of low-grade gliomas. Neurosurg Focus 36:E23CrossRefPubMed
98.
Metadata
Title
The role of neuropathology in the management of patients with diffuse low grade glioma
A systematic review and evidence-based clinical practice guideline
Authors
Daniel P. Cahill
Andrew E. Sloan
Brian V. Nahed
Kenneth D. Aldape
David N. Louis
Timothy C. Ryken
Steven N. Kalkanis
Jeffrey J. Olson
Publication date
01-12-2015
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 3/2015
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-015-1909-8

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