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Published in: Journal of Neuro-Oncology 2/2014

Open Access 01-01-2014 | Clinical Study

Short-term survivors in glioblastomas with oligodendroglioma component: a clinical study of 186 Chinese patients from a single institution

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

Published in: Journal of Neuro-Oncology | Issue 2/2014

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Abstract

This study was designed to display the molecular genetic features of short-term survivors in glioblastomas with oligodendroglioma component (GBMO). A total of 186 patients with histological diagnosis of primary gliomas, including 11 GBMO-STS (short-term survivors, survival ≤12 months), 29 GBMO-LTS (relatively long-term survivors, survival >12 months), 36 anaplastic oligoastrocytoma (AOA) and 110 glioblastoma multiforme (GBM), enrolled in the study. An evaluation form was developed and used to document molecular pathological, clinical and treatment-associated parameters between subgroups. Kaplan–Meier plots for survival showed that the median progression-free survival (PFS) and overall survival (OS) of GBMO-STS were 5.0 and 10.0 months, respectively. Intergroup comparison revealed that the GBMO-STS harbored the most dismal prognosis than those with AOA, GBMO-LTS or GBM (P < 0.001 for PFS, P < 0.001 for OS, respectively). Cox regression analyses revealed that 1p/19q co-deletion and 19p polysomy were independent prognostic factors (P < 0.05). Pearson’s Chi square test demonstrated GBMO-STS exhibited lower 1p/19q co-deletion, IDH1 mutation rates than AOA or GBMO-LTS (P = 0.032, P = 0.045 for 1p/19q co-deletion; P = 0.034, P = 0.005 for IDH1 mutation, respectively) but higher chromosome 1q, 19p polysomy rates compared with AOA or GBM (P = 0.037, P = 0.030 for 1q polysomy; P = 0.017, P = 0.011 for 19p polysomy, respectively). Patients with glioblastomas with oligodendroglioma component concurrent with polysomy for chromosomes 1 and 19 always confers an unfavorable prognosis which needs our extra attention in clinic.
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Literature
1.
go back to reference Vordermark D, Ruprecht K, Rieckmann P, Roggendorf W, Vince GH, Warmuth-Metz M, Kolbl O, Flentje M (2006) Glioblastoma multiforme with oligodendroglial component (GBMO): favorable outcome after post-operative radiotherapy and chemotherapy with nimustine (ACNU) and teniposide (VM26). BMC Cancer 6:247PubMedCentralPubMedCrossRef Vordermark D, Ruprecht K, Rieckmann P, Roggendorf W, Vince GH, Warmuth-Metz M, Kolbl O, Flentje M (2006) Glioblastoma multiforme with oligodendroglial component (GBMO): favorable outcome after post-operative radiotherapy and chemotherapy with nimustine (ACNU) and teniposide (VM26). BMC Cancer 6:247PubMedCentralPubMedCrossRef
2.
go back to reference Miller CR, Dunham CP, Scheithauer BW, Perry A (2006) Significance of necrosis in grading of oligodendroglial neoplasms: a clinicopathologic and genetic study of newly diagnosed high-grade gliomas. J Clin Oncol 24:5419–5426PubMedCrossRef Miller CR, Dunham CP, Scheithauer BW, Perry A (2006) Significance of necrosis in grading of oligodendroglial neoplasms: a clinicopathologic and genetic study of newly diagnosed high-grade gliomas. J Clin Oncol 24:5419–5426PubMedCrossRef
3.
go back to reference Kanno H, Nishihara H, Narita T, Yamaguchi S, Kobayashi H, Tanino M, Kimura T, Terasaka S, Tanaka S (2012) Prognostic implication of histological oligodendroglial tumor component: clinicopathological analysis of 111 cases of malignant gliomas. PLoS One 7:e41669PubMedCentralPubMedCrossRef Kanno H, Nishihara H, Narita T, Yamaguchi S, Kobayashi H, Tanino M, Kimura T, Terasaka S, Tanaka S (2012) Prognostic implication of histological oligodendroglial tumor component: clinicopathological analysis of 111 cases of malignant gliomas. PLoS One 7:e41669PubMedCentralPubMedCrossRef
4.
go back to reference Pinto LW, Araujo MB, Vettore AL, Wernersbach L, Leite AC, Chimelli LM, Soares FA (2008) Glioblastomas: correlation between oligodendroglial components, genetic abnormalities, and prognosis. Virchows Arch 452:481–490PubMedCrossRef Pinto LW, Araujo MB, Vettore AL, Wernersbach L, Leite AC, Chimelli LM, Soares FA (2008) Glioblastomas: correlation between oligodendroglial components, genetic abnormalities, and prognosis. Virchows Arch 452:481–490PubMedCrossRef
5.
go back to reference Hegi ME, Janzer RC, Lambiv WL, Gorlia T, Kouwenhoven MC, Hartmann C, von Deimling A, Martinet D, Besuchet SN, Diserens AC, Hamou MF, Bady P, Weller M, van den Bent MJ, Mason WP, Mirimanoff RO, Stupp R, Mokhtari K, Wesseling P (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, Gorlia T, Kouwenhoven MC, Hartmann C, von Deimling A, Martinet D, Besuchet SN, Diserens AC, Hamou MF, Bady P, Weller M, van den Bent MJ, Mason WP, Mirimanoff RO, Stupp R, Mokhtari K, Wesseling P (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
6.
go back to reference Nakamura H, Makino K, Kuratsu J (2011) Molecular and clinical analysis of glioblastoma with an oligodendroglial component (GBMO). Brain Tumor Pathol 28:185–190PubMedCrossRef Nakamura H, Makino K, Kuratsu J (2011) Molecular and clinical analysis of glioblastoma with an oligodendroglial component (GBMO). Brain Tumor Pathol 28:185–190PubMedCrossRef
7.
go back to reference Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109PubMedCentralPubMedCrossRef Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109PubMedCentralPubMedCrossRef
8.
go back to reference Ren X, Cui X, Lin S, Wang J, Jiang Z, Sui D, Li J, Wang Z (2012) Co-deletion of chromosome 1p/19q and IDH1/2 mutation in glioma subsets of brain tumors in Chinese patients. PLoS One 7:e32764PubMedCentralPubMedCrossRef Ren X, Cui X, Lin S, Wang J, Jiang Z, Sui D, Li J, Wang Z (2012) Co-deletion of chromosome 1p/19q and IDH1/2 mutation in glioma subsets of brain tumors in Chinese patients. PLoS One 7:e32764PubMedCentralPubMedCrossRef
9.
go back to reference Jiang H, Ren X, Zhang W, Ma J, Sui D, Jiang Z, Cui X, Lin S (2013) A new prognostic scoring scale for patients with primary WHO grade III gliomas based on molecular predictors. J Neurooncol 111:367–375PubMedCrossRef Jiang H, Ren X, Zhang W, Ma J, Sui D, Jiang Z, Cui X, Lin S (2013) A new prognostic scoring scale for patients with primary WHO grade III gliomas based on molecular predictors. J Neurooncol 111:367–375PubMedCrossRef
10.
go back to reference Wang Y, Li S, Chen L, You G, Bao Z, Yan W, Shi Z, Chen Y, Yao K, Zhang W, Kang C, Jiang T (2012) Glioblastoma with an oligodendroglioma component: distinct clinical behavior, genetic alterations, and outcome. Neuro Oncol 14:518–525PubMedCentralPubMedCrossRef Wang Y, Li S, Chen L, You G, Bao Z, Yan W, Shi Z, Chen Y, Yao K, Zhang W, Kang C, Jiang T (2012) Glioblastoma with an oligodendroglioma component: distinct clinical behavior, genetic alterations, and outcome. Neuro Oncol 14:518–525PubMedCentralPubMedCrossRef
11.
go back to reference Jeuken JW, von Deimling A, Wesseling P (2004) Molecular pathogenesis of oligodendroglial tumors. J Neurooncol 70:161–181PubMedCrossRef Jeuken JW, von Deimling A, Wesseling P (2004) Molecular pathogenesis of oligodendroglial tumors. J Neurooncol 70:161–181PubMedCrossRef
12.
go back to reference Cairncross G, Jenkins R (2008) Gliomas with 1p/19q codeletion: a.k.a. oligodendroglioma. Cancer J 14:352–357PubMedCrossRef Cairncross G, Jenkins R (2008) Gliomas with 1p/19q codeletion: a.k.a. oligodendroglioma. Cancer J 14:352–357PubMedCrossRef
13.
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 90:1473–1479PubMedCrossRef 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 90:1473–1479PubMedCrossRef
14.
go back to reference Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, Brachman D, Buckner J, Fink K, Souhami L, Laperierre N, Mehta M, Curran W (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 24:2707–2714PubMedCrossRef Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, Brachman D, Buckner J, Fink K, Souhami L, Laperierre N, Mehta M, Curran W (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 24:2707–2714PubMedCrossRef
15.
go back to reference Wick W, Hartmann C, Engel C, Stoffels M, Felsberg J, Stockhammer F, Sabel MC, Koeppen S, Ketter R, Meyermann R, Rapp M, Meisner C, Kortmann RD, Pietsch T, Wiestler OD, Ernemann U, Bamberg M, Reifenberger G, von Deimling A, Weller M (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, Stoffels M, Felsberg J, Stockhammer F, Sabel MC, Koeppen S, Ketter R, Meyermann R, Rapp M, Meisner C, Kortmann RD, Pietsch T, Wiestler OD, Ernemann U, Bamberg M, Reifenberger G, von Deimling A, Weller M (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
16.
go back to reference Bauman GS, Ino Y, Ueki K, Zlatescu MC, Fisher BJ, Macdonald DR, Stitt L, Louis DN, Cairncross JG (2000) Allelic loss of chromosome 1p and radiotherapy plus chemotherapy in patients with oligodendrogliomas. Int J Radiat Oncol Biol Phys 48:825–830PubMedCrossRef Bauman GS, Ino Y, Ueki K, Zlatescu MC, Fisher BJ, Macdonald DR, Stitt L, Louis DN, Cairncross JG (2000) Allelic loss of chromosome 1p and radiotherapy plus chemotherapy in patients with oligodendrogliomas. Int J Radiat Oncol Biol Phys 48:825–830PubMedCrossRef
17.
go back to reference Brandes AA, Tosoni A, Cavallo G, Reni M, Franceschi E, Bonaldi L, Bertorelle R, Gardiman M, Ghimenton C, Iuzzolino P, Pession A, Blatt V, Ermani M (2006) Correlations between O6-methylguanine DNA methyltransferase promoter methylation status, 1p and 19q deletions, and response to temozolomide in anaplastic and recurrent oligodendroglioma: a prospective GICNO study. J Clin Oncol 24:4746–4753PubMedCrossRef Brandes AA, Tosoni A, Cavallo G, Reni M, Franceschi E, Bonaldi L, Bertorelle R, Gardiman M, Ghimenton C, Iuzzolino P, Pession A, Blatt V, Ermani M (2006) Correlations between O6-methylguanine DNA methyltransferase promoter methylation status, 1p and 19q deletions, and response to temozolomide in anaplastic and recurrent oligodendroglioma: a prospective GICNO study. J Clin Oncol 24:4746–4753PubMedCrossRef
18.
go back to reference Kouwenhoven MC, Kros JM, French PJ, Biemond-ter SE, Graveland WJ, Taphoorn MJ, Brandes AA, van den Bent MJ (2006) 1p/19q loss within oligodendroglioma is predictive for response to first line temozolomide but not to salvage treatment. Eur J Cancer 42:2499–2503PubMedCrossRef Kouwenhoven MC, Kros JM, French PJ, Biemond-ter SE, Graveland WJ, Taphoorn MJ, Brandes AA, van den Bent MJ (2006) 1p/19q loss within oligodendroglioma is predictive for response to first line temozolomide but not to salvage treatment. Eur J Cancer 42:2499–2503PubMedCrossRef
19.
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. N Engl J Med 360:765–773PubMedCentralPubMedCrossRef 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. N Engl J Med 360:765–773PubMedCentralPubMedCrossRef
20.
go back to reference Sanson M, Marie Y, Paris S, Idbaih A, Laffaire J, Ducray F, El HS, 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 27:4150–4154PubMedCrossRef Sanson M, Marie Y, Paris S, Idbaih A, Laffaire J, Ducray F, El HS, 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 27:4150–4154PubMedCrossRef
22.
go back to reference Zhao S, Lin Y, Xu W, Jiang W, Zha Z, Wang P, Yu W, Li Z, Gong L, Peng Y, Ding J, Lei Q, Guan KL, Xiong Y (2009) Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science 324:261–265PubMedCentralPubMedCrossRef Zhao S, Lin Y, Xu W, Jiang W, Zha Z, Wang P, Yu W, Li Z, Gong L, Peng Y, Ding J, Lei Q, Guan KL, Xiong Y (2009) Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science 324:261–265PubMedCentralPubMedCrossRef
23.
go back to reference Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, Fantin VR, Jang HG, Jin S, Keenan MC, Marks KM, Prins RM, Ward PS, Yen KE, Liau LM, Rabinowitz JD, Cantley LC, Thompson CB, Vander HM, Su SM (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462:739–744PubMedCentralPubMedCrossRef Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, Fantin VR, Jang HG, Jin S, Keenan MC, Marks KM, Prins RM, Ward PS, Yen KE, Liau LM, Rabinowitz JD, Cantley LC, Thompson CB, Vander HM, Su SM (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462:739–744PubMedCentralPubMedCrossRef
24.
go back to reference Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, Brachman D, Buckner J, Fink K, Souhami L, Laperierre N, Mehta M, Curran W (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 24:2707–2714PubMedCrossRef Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, Brachman D, Buckner J, Fink K, Souhami L, Laperierre N, Mehta M, Curran W (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 24:2707–2714PubMedCrossRef
25.
go back to reference Li S, Yan C, Huang L, Qiu X, Wang Z, Jiang T (2012) Molecular prognostic factors of anaplastic oligodendroglial tumors and its relationship: a single institutional review of 77 patients from China. Neuro Oncol 14:109–116PubMedCentralPubMedCrossRef Li S, Yan C, Huang L, Qiu X, Wang Z, Jiang T (2012) Molecular prognostic factors of anaplastic oligodendroglial tumors and its relationship: a single institutional review of 77 patients from China. Neuro Oncol 14:109–116PubMedCentralPubMedCrossRef
26.
go back to reference Watanabe T, Nobusawa S, Kleihues P, Ohgaki H (2009) IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas. Am J Pathol 174:1149–1153PubMedCrossRef Watanabe T, Nobusawa S, Kleihues P, Ohgaki H (2009) IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas. Am J Pathol 174:1149–1153PubMedCrossRef
27.
go back to reference Snuderl M, Eichler AF, Ligon KL, Vu QU, Silver M, Betensky RA, Ligon AH, Wen PY, Louis DN, Iafrate AJ (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, Vu QU, Silver M, Betensky RA, Ligon AH, Wen PY, Louis DN, Iafrate AJ (2009) Polysomy for chromosomes 1 and 19 predicts earlier recurrence in anaplastic oligodendrogliomas with concurrent 1p/19q loss. Clin Cancer Res 15:6430–6437PubMedCentralPubMedCrossRef
28.
go back to reference Wiens AL, Cheng L, Bertsch EC, Johnson KA, Zhang S, Hattab EM (2012) Polysomy of chromosomes 1 and/or 19 is common and associated with less favorable clinical outcome in oligodendrogliomas: fluorescent in situ hybridization analysis of 84 consecutive cases. J Neuropathol Exp Neurol 71:618–624PubMedCrossRef Wiens AL, Cheng L, Bertsch EC, Johnson KA, Zhang S, Hattab EM (2012) Polysomy of chromosomes 1 and/or 19 is common and associated with less favorable clinical outcome in oligodendrogliomas: fluorescent in situ hybridization analysis of 84 consecutive cases. J Neuropathol Exp Neurol 71:618–624PubMedCrossRef
Metadata
Title
Short-term survivors in glioblastomas with oligodendroglioma component: a clinical study of 186 Chinese patients from a single institution
Authors
Haihui Jiang
Xiaohui Ren
Junmei Wang
Zhe Zhang
Wenqing Jia
Song Lin
Publication date
01-01-2014
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 2/2014
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-013-1311-3

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