Skip to main content
Top
Published in: Journal of Neuro-Oncology 3/2014

01-12-2014 | Clinical Study

1p/19q-driven prognostic molecular classification for high-grade oligodendroglial tumors

Authors: Haihui Jiang, Zhe Zhang, Xiaohui Ren, Wei Zeng, Wenqing Jia, Junmei Wang, Song Lin

Published in: Journal of Neuro-Oncology | Issue 3/2014

Login to get access

Abstract

The subjectivity in pathological diagnosis of anaplastic oligoastrocytoma (AOA) and uncertainty in designation of glioblastoma with oligodendroglioma component (GBMO) were two major dilemmas which puzzled neuro-pathologists and neurosurgeons. The present study was designed to project a molecular classification scheme based on the status of chromosome 1p and 19q. Patients (n = 117) with histological diagnosis of primary high-grade oligodendroglial tumors (HGOs) enrolled in the study. Fluorescence in situ hybridization (FISH) for chromosomes 1p and 19q was performed. Univariate analysis showed that higher tumor grade, 1p/19q maintenance and 1q/19p co polysomy were confirmed as risk factors in HGOs (P < 0.01). Accordingly, patients with HGOs were divided into four subtypes which conferred remarkably distinct prognosis based on the number of risk factors (0 risk factor: HGOs-1, 1 risk factor: HGOs-2, 2 risk factors: HGOs-3, 3 risk factors: HGOs-4). Cox regression model revealed that the tumor grade was no longer independently associated with survival, while the molecular classification scheme showed a marked prognostic significance (HR = 0.359, 95 % CI 0.261–0.494, P < 0.001 for progression-free survival (PFS); HR = 0.393, 95 % CI 0.283–0.546, P < 0.001 for overall survival (OS)). The classification scheme incorporating traditional pathology with molecular information can be served as a supplement of the current WHO classification system and contribute to the personalized treatment decision-making.
Appendix
Available only for authorised users
Literature
1.
2.
go back to reference Fuller CE, Schmidt RE, Roth KA et al (2003) Clinical utility of fluorescence in situ hybridization (FISH) in morphologically ambiguous gliomas with hybrid oligodendroglial/astrocytic features. J Neuropathol Exp Neurol 62:1118–1128PubMed Fuller CE, Schmidt RE, Roth KA et al (2003) Clinical utility of fluorescence in situ hybridization (FISH) in morphologically ambiguous gliomas with hybrid oligodendroglial/astrocytic features. J Neuropathol Exp Neurol 62:1118–1128PubMed
3.
go back to reference Kros JM, Gorlia T, Kouwenhoven MC et al (2007) 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 66:545–551PubMedCrossRef Kros JM, Gorlia T, Kouwenhoven MC et al (2007) 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 66:545–551PubMedCrossRef
4.
go back to reference Smith JS, Perry A, Borell TJ, Lee HK et al (2000) Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18:636–645PubMed Smith JS, Perry A, Borell TJ, Lee HK et al (2000) Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18:636–645PubMed
5.
go back to reference Jiang H, Ren X, Cui X et al (2013) 1p/19q codeletion and IDH1/2 mutation identified a subtype of anaplastic oligoastrocytomas with prognosis as favorable as anaplastic oligodendrogliomas. Neuro Oncol 15:775–782PubMedCentralPubMedCrossRef Jiang H, Ren X, Cui X et al (2013) 1p/19q codeletion and IDH1/2 mutation identified a subtype of anaplastic oligoastrocytomas with prognosis as favorable as anaplastic oligodendrogliomas. Neuro Oncol 15:775–782PubMedCentralPubMedCrossRef
6.
go back to reference Klink B, Schlingelhof B, Klink M et al (2010) Glioblastomas with oligodendroglial component—common origin of the different histological parts and genetic subclassification. Anal Cell Pathol (Amst) 33:37–54 Klink B, Schlingelhof B, Klink M et al (2010) Glioblastomas with oligodendroglial component—common origin of the different histological parts and genetic subclassification. Anal Cell Pathol (Amst) 33:37–54
7.
go back to reference Pinto LW, Araujo MB, Vettore AL et al (2008) Glioblastomas: correlation between oligodendroglial components, genetic abnormalities, and prognosis. Virchows Arch 452:481–490PubMedCrossRef Pinto LW, Araujo MB, Vettore AL et al (2008) Glioblastomas: correlation between oligodendroglial components, genetic abnormalities, and prognosis. Virchows Arch 452:481–490PubMedCrossRef
8.
go back to reference Noushmehr H, Weisenberger DJ, Diefes K et al (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17:510–522PubMedCentralPubMedCrossRef Noushmehr H, Weisenberger DJ, Diefes K et al (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17:510–522PubMedCentralPubMedCrossRef
9.
go back to reference Sturm D, Witt H, Hovestadt V et al (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22:425–437PubMedCrossRef Sturm D, Witt H, Hovestadt V et al (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22:425–437PubMedCrossRef
10.
go back to reference Verhaak RG, Hoadley KA, Purdom E et al (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17:98–110PubMedCentralPubMedCrossRef Verhaak RG, Hoadley KA, Purdom E et al (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17:98–110PubMedCentralPubMedCrossRef
11.
go back to reference McLendon R, Friedman A, Bigner D et al (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061–1068CrossRef McLendon R, Friedman A, Bigner D et al (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061–1068CrossRef
12.
go back to reference Wick W, Hartmann C, Engel C et al (2009) NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol 27:5874–5880PubMedCrossRef Wick W, Hartmann C, Engel C et al (2009) NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol 27:5874–5880PubMedCrossRef
13.
go back to reference Ambros PF, Ambros IM (2001) Pathology and biology guidelines for resectable and unresectable neuroblastic tumors and bone marrow examination guidelines. Med Pediatr Oncol 37:492–504PubMedCrossRef Ambros PF, Ambros IM (2001) Pathology and biology guidelines for resectable and unresectable neuroblastic tumors and bone marrow examination guidelines. Med Pediatr Oncol 37:492–504PubMedCrossRef
14.
go back to reference Snuderl M, Eichler AF, Ligon KL et al (2009) Polysomy for chromosomes 1 and 19 predicts earlier recurrence in anaplastic oligodendrogliomas with concurrent 1p/19q loss. Clin Cancer Res 15:6430–6437PubMedCentralPubMedCrossRef Snuderl M, Eichler AF, Ligon KL et al (2009) Polysomy for chromosomes 1 and 19 predicts earlier recurrence in anaplastic oligodendrogliomas with concurrent 1p/19q loss. Clin Cancer Res 15:6430–6437PubMedCentralPubMedCrossRef
15.
go back to reference Tortosa A, Vinolas N, Villa S et al (2003) Prognostic implication of clinical, radiologic, and pathologic features in patients with anaplastic gliomas. Cancer 97:1063–1071PubMedCrossRef Tortosa A, Vinolas N, Villa S et al (2003) Prognostic implication of clinical, radiologic, and pathologic features in patients with anaplastic gliomas. Cancer 97:1063–1071PubMedCrossRef
16.
go back to reference Miller CR, Dunham CP, Scheithauer BW et al (2006) a clinicopathologic and genetic study of newly diagnosed high-grade gliomas. J Clin Oncol 24:5419–5426PubMedCrossRef Miller CR, Dunham CP, Scheithauer BW et al (2006) a clinicopathologic and genetic study of newly diagnosed high-grade gliomas. J Clin Oncol 24:5419–5426PubMedCrossRef
17.
go back to reference Park CK, Lee SH, Han JH et al (2009) Recursive partitioning analysis of prognostic factors in WHO grade III glioma patients treated with radiotherapy or radiotherapy plus chemotherapy. BMC Cancer 9:450PubMedCentralPubMedCrossRef Park CK, Lee SH, Han JH et al (2009) Recursive partitioning analysis of prognostic factors in WHO grade III glioma patients treated with radiotherapy or radiotherapy plus chemotherapy. BMC Cancer 9:450PubMedCentralPubMedCrossRef
18.
go back to reference Hegi ME, Janzer RC, Lambiv WL et al (2012) Presence of an oligodendroglioma-like component in newly diagnosed glioblastoma identifies a pathogenetically heterogeneous subgroup and lacks prognostic value: central pathology review of the EORTC_26981/NCIC_CE.3 trial. Acta Neuropathol 123:841–852PubMedCrossRef Hegi ME, Janzer RC, Lambiv WL et al (2012) Presence of an oligodendroglioma-like component in newly diagnosed glioblastoma identifies a pathogenetically heterogeneous subgroup and lacks prognostic value: central pathology review of the EORTC_26981/NCIC_CE.3 trial. Acta Neuropathol 123:841–852PubMedCrossRef
19.
go back to reference 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 9:157–173PubMedCrossRef 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 9:157–173PubMedCrossRef
21.
go back to reference Hartmann C, Hentschel B, Wick W et al (2010) Patients with IDH1 wild type anaplastic astrocytomas exhibit worse prognosis than IDH1-mutated glioblastomas, and IDH1 mutation status accounts for the unfavorable prognostic effect of higher age: implications for classification of gliomas. Acta Neuropathol 120:707–718PubMedCrossRef Hartmann C, Hentschel B, Wick W et al (2010) Patients with IDH1 wild type anaplastic astrocytomas exhibit worse prognosis than IDH1-mutated glioblastomas, and IDH1 mutation status accounts for the unfavorable prognostic effect of higher age: implications for classification of gliomas. Acta Neuropathol 120:707–718PubMedCrossRef
22.
go back to reference 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 14:842–853PubMedCrossRef 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 14:842–853PubMedCrossRef
23.
go back to reference Ren X, Jiang H, Cui X et al (2013) Co-polysomy of chromosome 1q and 19p predicts worse prognosis in 1p/19q codeleted oligodendroglial tumors: fISH analysis of 148 consecutive cases. Neuro Oncol 15:1244–1250PubMedCentralPubMedCrossRef Ren X, Jiang H, Cui X et al (2013) Co-polysomy of chromosome 1q and 19p predicts worse prognosis in 1p/19q codeleted oligodendroglial tumors: fISH analysis of 148 consecutive cases. Neuro Oncol 15:1244–1250PubMedCentralPubMedCrossRef
24.
go back to reference Jiang H, Ren X, Wang J et al (2014) Short-term survivors in glioblastomas with oligodendroglioma component: a clinical study of 186 Chinese patients from a single institution. J Neurooncol 116:395–404PubMedCentralPubMedCrossRef Jiang H, Ren X, Wang J et al (2014) Short-term survivors in glioblastomas with oligodendroglioma component: a clinical study of 186 Chinese patients from a single institution. J Neurooncol 116:395–404PubMedCentralPubMedCrossRef
25.
go back to reference Jiang H, Ren X, Zhang Z, et al. (2014) Polysomy of chromosomes 1 and 19: an underestimated prognostic factor in oligodendroglial tumors. J Neurooncol. doi:10.1007/s11060-014-1526-y Jiang H, Ren X, Zhang Z, et al. (2014) Polysomy of chromosomes 1 and 19: an underestimated prognostic factor in oligodendroglial tumors. J Neurooncol. doi:10.​1007/​s11060-014-1526-y
26.
go back to reference Cowell JK, Barnett GH, Nowak NJ et al (2004) Characterization of the 1p/19q chromosomal loss in oligodendrogliomas using comparative genomic hybridization arrays (CGHa). J Neuropathol Exp Neurol 63:151–158PubMed Cowell JK, Barnett GH, Nowak NJ et al (2004) Characterization of the 1p/19q chromosomal loss in oligodendrogliomas using comparative genomic hybridization arrays (CGHa). J Neuropathol Exp Neurol 63:151–158PubMed
Metadata
Title
1p/19q-driven prognostic molecular classification for high-grade oligodendroglial tumors
Authors
Haihui Jiang
Zhe Zhang
Xiaohui Ren
Wei Zeng
Wenqing Jia
Junmei Wang
Song Lin
Publication date
01-12-2014
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 3/2014
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-014-1593-0

Other articles of this Issue 3/2014

Journal of Neuro-Oncology 3/2014 Go to the issue