Skip to main content
Top
Published in: International Journal of Clinical Oncology 6/2020

01-06-2020 | Glioblastoma | Invited Review Article

Clinical impact of revisions to the WHO classification of diffuse gliomas and associated future problems

Author: Yukihiko Sonoda

Published in: International Journal of Clinical Oncology | Issue 6/2020

Login to get access

Abstract

The publication of the 2016 World Health Organization Classification of Tumors of the Central Nervous System (2016 WHO CNS) represented a major change in the classification of brain tumors. It is essential to determine the IDH and 1p/19q statuses of diffuse gliomas to ensure that the final diagnosis is accurate. The integrated diagnostic method outlined in the 2016 WHO CNS has enabled more precise prediction of the prognoses of diffuse gliomas. However, there are further two points that need to be addressed when planning future clinical trials. The first is the problems with the WHO grading system for diffuse gliomas. The second is that examinations for IDH mutations and 1p/19q co-deletion are not sufficient on their own to accurately predict the prognosis of diffuse glioma patients. Risk of an IDH-mut diffuse glioma should be evaluated based on a combination of clinical factors (age and the resection rate), molecular factors (the presence/absence of CDKN2A deletion), and histological factors (morphology and the mitotic index). Glioblastoma (GBM) have also been classified according to their IDH status; however, the frequency of IDH gene mutations is only 5–10% in GBM. Other molecular markers such as MGMT methylation, pTERT mutations and EGFR amplification could be more important to predict clinical outcome. Therefore, the next revision of the classification of diffuse gliomas will propose a detailed classification based on additional markers. In the near future, treatments for diffuse gliomas will be chosen according to the molecular profile of each tumor.
Literature
1.
go back to reference Louis DN, Ohgaki H, Wiestler OD, et al. (eds) (2016) WHO classification of tumours of the central nervous system (revised edition), 4th edn. International Agency for Research on Cancer, Lyon Louis DN, Ohgaki H, Wiestler OD, et al. (eds) (2016) WHO classification of tumours of the central nervous system (revised edition), 4th edn. International Agency for Research on Cancer, Lyon
2.
go back to reference Korshunov A, Meyer J, Capper D et al (2009) Combined molecular analysis of BRAF and IDH1 distinguishes pilocytic astrocytoma from diffuse astrocytoma. Acta Neuropathol 118:401–405PubMedCrossRef Korshunov A, Meyer J, Capper D et al (2009) Combined molecular analysis of BRAF and IDH1 distinguishes pilocytic astrocytoma from diffuse astrocytoma. Acta Neuropathol 118:401–405PubMedCrossRef
3.
go back to reference Louis DN, Wesseling P, Paulus W et al (2018) cIMPACT-NOW update 1: not otherwise specified (NOS) and not elsewhere classified (NEC). Acta Neuropathol 135:481–484PubMedCrossRef Louis DN, Wesseling P, Paulus W et al (2018) cIMPACT-NOW update 1: not otherwise specified (NOS) and not elsewhere classified (NEC). Acta Neuropathol 135:481–484PubMedCrossRef
4.
go back to reference Louis DN, Giannini C, Capper D et al (2018) cIMPACT-NOW update 2: diagnostic clarifications for diffuse midline glioma, H3 K27M-mutant and diffuse astrocytoma/anaplastic astrocytoma. IDH Mutant Acta Neuropathol 135:639–642PubMedCrossRef Louis DN, Giannini C, Capper D et al (2018) cIMPACT-NOW update 2: diagnostic clarifications for diffuse midline glioma, H3 K27M-mutant and diffuse astrocytoma/anaplastic astrocytoma. IDH Mutant Acta Neuropathol 135:639–642PubMedCrossRef
5.
go back to reference Brat DJ, Aldape K, Colman H et al (2018) cIMPACT-NOW update 3: recommended diagnostic criteria for "Diffuse astrocytic glioma, IDH-wildtype, with molecular features of glioblastoma, WHO grade IV". Acta Neuropathol 136:805–810PubMedPubMedCentralCrossRef Brat DJ, Aldape K, Colman H et al (2018) cIMPACT-NOW update 3: recommended diagnostic criteria for "Diffuse astrocytic glioma, IDH-wildtype, with molecular features of glioblastoma, WHO grade IV". Acta Neuropathol 136:805–810PubMedPubMedCentralCrossRef
6.
go back to reference Ellison DW, Hawkins C, Jones DTW et al (2019) cIMPACT-NOW update 4: diffuse gliomas characterized by MYB, MYBL1, or FGFR1 alterations or BRAFV600E mutation. Acta Neuropathol 137:683–687PubMedCrossRef Ellison DW, Hawkins C, Jones DTW et al (2019) cIMPACT-NOW update 4: diffuse gliomas characterized by MYB, MYBL1, or FGFR1 alterations or BRAFV600E mutation. Acta Neuropathol 137:683–687PubMedCrossRef
7.
go back to reference Louis DN, Ohgaki H, Wiestler OD, et al. (eds) (2007) WHO classification of tumours of the central nervous system, 4th edn. International Agency for Research on Cancer, Lyon Louis DN, Ohgaki H, Wiestler OD, et al. (eds) (2007) WHO classification of tumours of the central nervous system, 4th edn. International Agency for Research on Cancer, Lyon
8.
go back to reference Pignatti F, van den Bent M, Curran D et al (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20:2076–2084PubMedCrossRef Pignatti F, van den Bent M, Curran D et al (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20:2076–2084PubMedCrossRef
9.
go back to reference van den Bent MJ (2010) Interobserver variation of the histopathological diagnosis in clinical trials on glioma: a clinician’s perspective. Acta Neuropathol 120:297–304PubMedPubMedCentralCrossRef van den Bent MJ (2010) Interobserver variation of the histopathological diagnosis in clinical trials on glioma: a clinician’s perspective. Acta Neuropathol 120:297–304PubMedPubMedCentralCrossRef
10.
go back to reference Sahm F, Reuss D, Koelsche C et al (2014) Farewell to oligoastrocytoma: in situ molecular genetics favor classification as either oligodendroglioma or astrocytoma. Acta Neuropathol 128:551–559PubMedCrossRef Sahm F, Reuss D, Koelsche C et al (2014) Farewell to oligoastrocytoma: in situ molecular genetics favor classification as either oligodendroglioma or astrocytoma. Acta Neuropathol 128:551–559PubMedCrossRef
11.
go back to reference Suzuki H, Aoki K, Chiba K et al (2015) Mutational landscape and clonal architecture in grade II and III gliomas. Nat Genet 47:458–468PubMedCrossRef Suzuki H, Aoki K, Chiba K et al (2015) Mutational landscape and clonal architecture in grade II and III gliomas. Nat Genet 47:458–468PubMedCrossRef
12.
go back to reference Weller M, Weber RG, Willscher E et al (2015) Molecular classification of diffuse cerebral WHO grade II/III gliomas using genome- and transcriptome-wide profiling improves stratification of prognostically distinct patient groups. Acta Neuropathol 129:679–693PubMedCrossRef Weller M, Weber RG, Willscher E et al (2015) Molecular classification of diffuse cerebral WHO grade II/III gliomas using genome- and transcriptome-wide profiling improves stratification of prognostically distinct patient groups. Acta Neuropathol 129:679–693PubMedCrossRef
13.
go back to reference Tabouret E, Nguyen AT, Dehais C et al (2016) Prognostic impact of the 2016 WHO classification of diffuse gliomas in the French POLA cohort. Acta Neuropathol 132:625–634PubMedCrossRef Tabouret E, Nguyen AT, Dehais C et al (2016) Prognostic impact of the 2016 WHO classification of diffuse gliomas in the French POLA cohort. Acta Neuropathol 132:625–634PubMedCrossRef
14.
go back to reference van den Bent MJ, Baumert B, Erridge SC et al (2017) Interim results from the CATNON trial (EORTC study 26053–22054) of treatment with concurrent and adjuvant temozolomide for 1p/19q non-co-deleted anaplastic glioma: a phase 3, randomised, open-label intergroup study. Lancet 390:1645–1653PubMedPubMedCentralCrossRef van den Bent MJ, Baumert B, Erridge SC et al (2017) Interim results from the CATNON trial (EORTC study 26053–22054) of treatment with concurrent and adjuvant temozolomide for 1p/19q non-co-deleted anaplastic glioma: a phase 3, randomised, open-label intergroup study. Lancet 390:1645–1653PubMedPubMedCentralCrossRef
15.
go back to reference van den Bent MJ, Afra D, de Witte O et al (2005) Long-term efficacy of early versus delayed radiotherapy for low-grade astrocytoma and oligodendroglioma in adults: the EORTC 22845 randomised trial. Lancet 366:985–990PubMedCrossRef van den Bent MJ, Afra D, de Witte O et al (2005) Long-term efficacy of early versus delayed radiotherapy for low-grade astrocytoma and oligodendroglioma in adults: the EORTC 22845 randomised trial. Lancet 366:985–990PubMedCrossRef
16.
go back to reference Reuss DE, Mamatjan Y, Schrimpf D et al (2015) IDH mutant diffuse and anaplastic astrocytomas have similar age at presentation and little difference in survival: a grading problem for WHO. Acta Neuropathol 129:867–873PubMedPubMedCentralCrossRef Reuss DE, Mamatjan Y, Schrimpf D et al (2015) IDH mutant diffuse and anaplastic astrocytomas have similar age at presentation and little difference in survival: a grading problem for WHO. Acta Neuropathol 129:867–873PubMedPubMedCentralCrossRef
17.
go back to reference Appay R, Dehais C, Maurage CA et al (2019) CDKN2A homozygous deletion is a strong adverse prognosis factor in diffuse malignant IDH-mutant gliomas. Neuro Oncol Neuro Oncol 21:1519–1528PubMed Appay R, Dehais C, Maurage CA et al (2019) CDKN2A homozygous deletion is a strong adverse prognosis factor in diffuse malignant IDH-mutant gliomas. Neuro Oncol Neuro Oncol 21:1519–1528PubMed
18.
go back to reference Olar A, Wani KM, Alfaro-Munoz KD et al (2015) IDH mutation status and role of WHO grade and mitotic index in overall survival in grade II–III diffuse gliomas. Acta Neuropathol 129:585–596PubMedPubMedCentralCrossRef Olar A, Wani KM, Alfaro-Munoz KD et al (2015) IDH mutation status and role of WHO grade and mitotic index in overall survival in grade II–III diffuse gliomas. Acta Neuropathol 129:585–596PubMedPubMedCentralCrossRef
19.
go back to reference Shibahara I, Sonoda Y, Kanamori M et al (2012) IDH1/2 gene status defines the prognosis and molecular profiles in patients with grade III gliomas. Int J Clin Oncol 17:551–561PubMedCrossRef Shibahara I, Sonoda Y, Kanamori M et al (2012) IDH1/2 gene status defines the prognosis and molecular profiles in patients with grade III gliomas. Int J Clin Oncol 17:551–561PubMedCrossRef
20.
go back to reference Pratt D, Natarajan SK, Banda A et al (2018) Circumscribed/non-diffuse histology confers a better prognosis in H3K27M-mutant gliomas. Acta Neuropathol 135:299–301PubMedPubMedCentralCrossRef Pratt D, Natarajan SK, Banda A et al (2018) Circumscribed/non-diffuse histology confers a better prognosis in H3K27M-mutant gliomas. Acta Neuropathol 135:299–301PubMedPubMedCentralCrossRef
22.
go back to reference 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, Stupp BDD, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996CrossRef 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, Stupp BDD, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996CrossRef
23.
go back to reference Hegi ME, Diserens AC, Gorlia T et al (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003PubMedCrossRef Hegi ME, Diserens AC, Gorlia T et al (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003PubMedCrossRef
24.
go back to reference Esteller M, Hamilton SR, Burger PC et al (1999) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res 59:793–797PubMed Esteller M, Hamilton SR, Burger PC et al (1999) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res 59:793–797PubMed
27.
go back to reference Arita H, Narita Y, Fukushima S et al (2013) Upregulating mutations in the TERT promoter commonly occur in adult malignant gliomas and are strongly associated with total 1p19q loss. Acta Neuropathol 12:267–276CrossRef Arita H, Narita Y, Fukushima S et al (2013) Upregulating mutations in the TERT promoter commonly occur in adult malignant gliomas and are strongly associated with total 1p19q loss. Acta Neuropathol 12:267–276CrossRef
28.
go back to reference Eckel-Passow JE, Lachance DH, Molinaro AM et al (2015) Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 372:2499–2508PubMedPubMedCentralCrossRef Eckel-Passow JE, Lachance DH, Molinaro AM et al (2015) Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 372:2499–2508PubMedPubMedCentralCrossRef
29.
go back to reference Arita H, Yamasaki K, Matsushita Y et al (2016) A combination of TERT promoter mutation and MGMT methylation status predicts clinically relevant subgroups of newly diagnosed glioblastomas. Acta Neuropathol Commun 4(1):79PubMedPubMedCentralCrossRef Arita H, Yamasaki K, Matsushita Y et al (2016) A combination of TERT promoter mutation and MGMT methylation status predicts clinically relevant subgroups of newly diagnosed glioblastomas. Acta Neuropathol Commun 4(1):79PubMedPubMedCentralCrossRef
30.
go back to reference Nguyen HN, Lie A, Li T, Chowdhury R et al (2017) Human TERT promoter mutation enables survival advantage from MGMT promoter methylation in IDH1 wild-type primary glioblastoma treated by standard chemoradiotherapy. Neuro Oncol 19:394–404PubMed Nguyen HN, Lie A, Li T, Chowdhury R et al (2017) Human TERT promoter mutation enables survival advantage from MGMT promoter methylation in IDH1 wild-type primary glioblastoma treated by standard chemoradiotherapy. Neuro Oncol 19:394–404PubMed
31.
go back to reference Labussière MB, Boisselier K, Mokhtari AL et al (2014) Combined analysis of TERT, EGFR, and IDH status defines distinct prognostic glioblastoma classes. Neurology 83:1200–1206PubMedCrossRef Labussière MB, Boisselier K, Mokhtari AL et al (2014) Combined analysis of TERT, EGFR, and IDH status defines distinct prognostic glioblastoma classes. Neurology 83:1200–1206PubMedCrossRef
32.
go back to reference Keles GE, Chang EF, Lamborn KR et al (2006) Volumetric extent of resection and residual contrast enhancement on initial surgery as predictors of outcome in adult patients with hemispheric anaplastic astrocytoma. J Neurosurg 105:34–40PubMedCrossRef Keles GE, Chang EF, Lamborn KR et al (2006) Volumetric extent of resection and residual contrast enhancement on initial surgery as predictors of outcome in adult patients with hemispheric anaplastic astrocytoma. J Neurosurg 105:34–40PubMedCrossRef
33.
go back to reference Oppenlander ME, Wolf AB, Snyder LA et al (2014) An extent of resection threshold for recurrent glioblastoma and its risk for neurological morbidity. J Neurosurg 120:846–853PubMedCrossRef Oppenlander ME, Wolf AB, Snyder LA et al (2014) An extent of resection threshold for recurrent glioblastoma and its risk for neurological morbidity. J Neurosurg 120:846–853PubMedCrossRef
34.
go back to reference Pope WB, Sayre J, Perlina A, Villablanca JP et al (2005) MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol 26:2466–2474PubMedPubMedCentral Pope WB, Sayre J, Perlina A, Villablanca JP et al (2005) MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol 26:2466–2474PubMedPubMedCentral
35.
go back to reference Sanai N, Polley M-Y, McDermott MW et al (2011) An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115:3–8PubMedCrossRef Sanai N, Polley M-Y, McDermott MW et al (2011) An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115:3–8PubMedCrossRef
36.
go back to reference Kawaguchi T, Sonoda Y, Shibahara I et al (2016) Impact of gross total resection in patients with WHO grade III glioma harboring the IDH 1/2 mutation without the 1p/19q co-deletion. J Neurooncol 129:505–514PubMedCrossRef Kawaguchi T, Sonoda Y, Shibahara I et al (2016) Impact of gross total resection in patients with WHO grade III glioma harboring the IDH 1/2 mutation without the 1p/19q co-deletion. J Neurooncol 129:505–514PubMedCrossRef
37.
go back to reference van den Bent MJ, Smits M, Kros JM et al (2017) Diffuse infiltrating oligodendroglioma and astrocytoma. J Clin Oncol 35:2394–2401PubMedCrossRef van den Bent MJ, Smits M, Kros JM et al (2017) Diffuse infiltrating oligodendroglioma and astrocytoma. J Clin Oncol 35:2394–2401PubMedCrossRef
38.
go back to reference 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 90:1473–1479PubMedCrossRef 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 90:1473–1479PubMedCrossRef
39.
go back to reference Yung WK, Prados MD, Yaya-Tur R et al (1999) Multicenter phase II trial of temozolomide in patients with anaplastic astrocytoma or anaplastic oligoastrocytoma at first relapse. J Clin Oncol 17:2762–2771PubMedCrossRef Yung WK, Prados MD, Yaya-Tur R et al (1999) Multicenter phase II trial of temozolomide in patients with anaplastic astrocytoma or anaplastic oligoastrocytoma at first relapse. J Clin Oncol 17:2762–2771PubMedCrossRef
40.
go back to reference van den Bent MJ, Taphoorn MJ, Brandes AA et al (2003) (2003) Phase II study of first-line chemotherapy with temozolomide in recurrent oligodendroglial tumors: The European Organization for Research and Treatment of Cancer Brain Tumor Group Study 26971. J Clin Oncol 21:2525–2528PubMedCrossRef van den Bent MJ, Taphoorn MJ, Brandes AA et al (2003) (2003) Phase II study of first-line chemotherapy with temozolomide in recurrent oligodendroglial tumors: The European Organization for Research and Treatment of Cancer Brain Tumor Group Study 26971. J Clin Oncol 21:2525–2528PubMedCrossRef
41.
42.
go back to reference Cairncross G, Wang M, Shaw E et al (2013) Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J Clin Oncol 31:337–343PubMedCrossRef Cairncross G, Wang M, Shaw E et al (2013) Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J Clin Oncol 31:337–343PubMedCrossRef
43.
go back to reference van den Bent MJ, Brandes AA, Taphoorn MJ et al (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 31:344–350PubMedCrossRef van den Bent MJ, Brandes AA, Taphoorn MJ et al (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 31:344–350PubMedCrossRef
44.
go back to reference van den Bent MJ, Baumert B, Errridge S et al (2017) Concurrent and adjuvant temozolomide for 1p/19q non-co-deleted anaplastic glioma: interim results of the randomized intergroup CATNON trial (EORTC study 26053–22054). Lancet 390:1645PubMedPubMedCentralCrossRef van den Bent MJ, Baumert B, Errridge S et al (2017) Concurrent and adjuvant temozolomide for 1p/19q non-co-deleted anaplastic glioma: interim results of the randomized intergroup CATNON trial (EORTC study 26053–22054). Lancet 390:1645PubMedPubMedCentralCrossRef
45.
go back to reference Cairncross JG, Wang M, Jenkins RB et al (2014) Benefit from procarbazine, lomustine, and vincristine in oligodendroglial tumors is associated with mutation of IDH. J Clin Oncol 32:783–790PubMedPubMedCentralCrossRef Cairncross JG, Wang M, Jenkins RB et al (2014) Benefit from procarbazine, lomustine, and vincristine in oligodendroglial tumors is associated with mutation of IDH. J Clin Oncol 32:783–790PubMedPubMedCentralCrossRef
46.
go back to reference van den Bent MJ, Erdem-Eraslan L, Idbaih A et al (2013) MGMT-STP27methylation status as predictivemarker for response to PCV in anaplastic oligodendrogliomas and oligoastrocytomas: a report from EORTC study 26951. Clin Cancer Res 19:5513–5522PubMedCrossRef van den Bent MJ, Erdem-Eraslan L, Idbaih A et al (2013) MGMT-STP27methylation status as predictivemarker for response to PCV in anaplastic oligodendrogliomas and oligoastrocytomas: a report from EORTC study 26951. Clin Cancer Res 19:5513–5522PubMedCrossRef
47.
go back to reference Baumert BG, Hegi ME, van den Bent MJ et al (2016) Temozolomide chemotherapy versus radiotherapy in high-risk low-grade glioma (EORTC 22033–26033): a randomised, open-label, phase 3 intergroup study. Lancet Oncol 17:1521–1532PubMedPubMedCentralCrossRef Baumert BG, Hegi ME, van den Bent MJ et al (2016) Temozolomide chemotherapy versus radiotherapy in high-risk low-grade glioma (EORTC 22033–26033): a randomised, open-label, phase 3 intergroup study. Lancet Oncol 17:1521–1532PubMedPubMedCentralCrossRef
48.
go back to reference Wick W, Roth P, Hartmann C et al (2016) Long-term analysis of the NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with PCV or temozolomide. Neuro Oncol 18:1529–1537PubMedPubMedCentral Wick W, Roth P, Hartmann C et al (2016) Long-term analysis of the NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with PCV or temozolomide. Neuro Oncol 18:1529–1537PubMedPubMedCentral
49.
go back to reference Chinot OL, Wick W, Mason W et al (2014) Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 370:709–722PubMedCrossRef Chinot OL, Wick W, Mason W et al (2014) Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 370:709–722PubMedCrossRef
50.
51.
go back to reference Stupp R, Taillibert S, Kanner A et al (2017) Effect of tumor-treating fields plus maintenance temozolomide vs maintenance temozolomide alone on survival in patients with glioblastoma: a randomized clinical trial. JAMA 318:2306–2316PubMedPubMedCentralCrossRef Stupp R, Taillibert S, Kanner A et al (2017) Effect of tumor-treating fields plus maintenance temozolomide vs maintenance temozolomide alone on survival in patients with glioblastoma: a randomized clinical trial. JAMA 318:2306–2316PubMedPubMedCentralCrossRef
52.
go back to reference Kirson ED, Dbalý V, Tovarys F et al (2007) Alternating electric fields arrest cell proliferation in animal tumor models and human brain tumors. Proc Natl Acad Sci USA 104:10152–10157CrossRefPubMedPubMedCentral Kirson ED, Dbalý V, Tovarys F et al (2007) Alternating electric fields arrest cell proliferation in animal tumor models and human brain tumors. Proc Natl Acad Sci USA 104:10152–10157CrossRefPubMedPubMedCentral
53.
go back to reference Dang L, Yen K, Attar EC (2016) IDH mutations in cancer and progress toward development of targeted therapeutics. Ann Oncol 27:599–608PubMedCrossRef Dang L, Yen K, Attar EC (2016) IDH mutations in cancer and progress toward development of targeted therapeutics. Ann Oncol 27:599–608PubMedCrossRef
54.
go back to reference Lassman AB, van den Bent MJ, Gan HK et al (2019) Safety and efficacy of depatuxizumab mafodotin + temozolomide in patients with EGFR-amplified, recurrent glioblastoma: results from an international phase I multicenter trial. Neuro Oncol 21:106–114PubMedCrossRef Lassman AB, van den Bent MJ, Gan HK et al (2019) Safety and efficacy of depatuxizumab mafodotin + temozolomide in patients with EGFR-amplified, recurrent glioblastoma: results from an international phase I multicenter trial. Neuro Oncol 21:106–114PubMedCrossRef
55.
go back to reference Caccese M, Indraccolo S, Zagonel V et al (2019) (2019) PD-1/PD-L1 immune-checkpoint inhibitors in glioblastoma: a concise review. Crit Rev Oncol Hematol 135:128–134PubMedCrossRef Caccese M, Indraccolo S, Zagonel V et al (2019) (2019) PD-1/PD-L1 immune-checkpoint inhibitors in glioblastoma: a concise review. Crit Rev Oncol Hematol 135:128–134PubMedCrossRef
56.
go back to reference Jones DT, Kocialkowski S, Liu L et al (2009) Oncogenic RAF1 rearrangement and a novel BRAF mutation as alternatives to KIAA1549:BRAF fusion in activating the MAPK pathway in pilocytic astrocytoma. Oncogene 28:2119–2123PubMedPubMedCentralCrossRef Jones DT, Kocialkowski S, Liu L et al (2009) Oncogenic RAF1 rearrangement and a novel BRAF mutation as alternatives to KIAA1549:BRAF fusion in activating the MAPK pathway in pilocytic astrocytoma. Oncogene 28:2119–2123PubMedPubMedCentralCrossRef
Metadata
Title
Clinical impact of revisions to the WHO classification of diffuse gliomas and associated future problems
Author
Yukihiko Sonoda
Publication date
01-06-2020
Publisher
Springer Singapore
Published in
International Journal of Clinical Oncology / Issue 6/2020
Print ISSN: 1341-9625
Electronic ISSN: 1437-7772
DOI
https://doi.org/10.1007/s10147-020-01628-7

Other articles of this Issue 6/2020

International Journal of Clinical Oncology 6/2020 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine