Management of Low-Grade Gliomas
R. Soffietti
University Hospital San Giovanni Battista, Turin, Italy
Search for more papers by this authorB. Baumert
Maastricht University Medical Centre, Maastricht, The Netherlands
Search for more papers by this authorK. Hoang-Xuan
Groupe Hospitalier Pitié-Salpêtrière, Paris, France
Search for more papers by this authorM. Klein
VU University Medical Centre, Amsterdam, The Netherlands
Search for more papers by this authorJ. Rees
National Hospital for Neurology and Neurosurgery, London, United Kingdom
Search for more papers by this authorT. Siegal
Hadassah Hebrew University Hospital, Jerusalem, Israel
Search for more papers by this authorR. Stupp
University Hospital and University, Lausanne, Switzerland
Search for more papers by this authorR. Soffietti
University Hospital San Giovanni Battista, Turin, Italy
Search for more papers by this authorB. Baumert
Maastricht University Medical Centre, Maastricht, The Netherlands
Search for more papers by this authorK. Hoang-Xuan
Groupe Hospitalier Pitié-Salpêtrière, Paris, France
Search for more papers by this authorM. Klein
VU University Medical Centre, Amsterdam, The Netherlands
Search for more papers by this authorJ. Rees
National Hospital for Neurology and Neurosurgery, London, United Kingdom
Search for more papers by this authorT. Siegal
Hadassah Hebrew University Hospital, Jerusalem, Israel
Search for more papers by this authorR. Stupp
University Hospital and University, Lausanne, Switzerland
Search for more papers by this authorNils Erik Gilhus MD, PHD
Department of Clinical Medicine, University of Bergen, Norway
Department of Neurology, Haukeland University Hospital, Bergen, Norway
Search for more papers by this authorMichael P. Barnes MD, FRCP
University of Newcastle, Newcastle upon Tyne, UK
Hunters Moor Neurorehabilitation Ltd, Newcastle upon Tyne, UK
Search for more papers by this authorMichael Brainin MD
Department of Clinical Medicine and Prevention, Austria
Center for Clinical Neurosciences, Donau-Universität Krems, Austria
Department of Neurology, Landesklinikum Donauregion Tulln, Tulln, Austria
Search for more papers by this authorSummary
Background: Diffuse infiltrative low-grade gliomas (LGGs) of the cerebral hemispheres in the adult are a group of tumours with distinct clinical, histological and molecular characteristics, and there are still controversies in management.
Methods: The scientific evidence collected from the literature was evaluated and graded according to EFNS guidelines, and recommendations were made.
Results and conclusions: The WHO classification recognizes grade II astrocytomas, oligodendrogliomas and oligoastrocytomas. Conventional MRI is used for differential diagnosis, guiding surgery, planning radiotherapy and monitoring treatment response. Advanced imaging techniques can increase diagnostic accuracy. Younger age, normal neurological examination, oligodendroglial histology and 1p loss are favourable prognostic factors. Prophylactic antiepileptic drugs are not useful, and there is no evidence that one drug is better than any other7. Total or near-total resection can improve seizure control and progression-free and overall survival, while reducing the risk of malignant transformation. Early postoperative radiotherapy improves progression-free but not overall survival. Low doses of radiation are as effective as high doses and are better tolerated. Modern radiotherapy techniques reduce the risk of late cognitive deficits. Chemotherapy can be useful both at recurrence after radiotherapy and as initial treatment after surgery to delay the risk of late neurotoxicity from large-field radiotherapy. Neurocognitive deficits are frequent and can be caused by the tumour itself, tumour-related epilepsy, treatments and psychological distress.
References
- Duffau, L, Capelle, L. Preferential brain locations of low-grade gliomas. Cancer 2004; 100: 2622–6.
- Claus, EB, Black, PM. Survival rates and patterns of care for patients diagnosed with supratentorial low-grade gliomas: data from the SEER program, 1973–2001. Cancer 2006; 106: 1358–63.
- Mandonnet, E, Delattre, JY, Tanguy, ML, et al. Continuous growth of mean tumour diameter in a subset of grade II gliomas. Ann Neurol 2003; 53: 524–8.
- Rees, J, Watt, H, Jäger, HR, et al. Volumes and growth rates of untreated adult low-grade gliomas indicate risk of early malignant transformation. Eur J Radiol 2009; 72: 54–64.
- Schiff, D, Brown, PD, Giannini, C. Outcome in adult low- grade glioma: the impact of prognostic factors and treatment. Neurology 2007; 69: 1366–73.
- Brainin, M, Barnes, M, Baron, JC, et al. Guidance for the preparation of neurological management guidelines by EFNS scientific task forces–revised recommendation. 2004. Eur J Neurol 2004; 11: 577–81.
- D Louis, H Ohgaki, O Wiestler, W Cavenee (eds). World Health Organization Classification of Tumours of the Central Nervous System, 4th edn, 2007; IARC, Lyon.
- Okamoto, Y, Di Patre, PL, Burkhard, C, et al. Population-based study on incidence, survival rates, and genetic alterations of low-grade diffuse astrocytomas and oligodendrogliomas. Acta Neuropathol 2004; 108: 49–56.
- Balss, J, Meyer, J, Mueller, W, et al. Analysis of the IDH1 codon 132 mutation in brain tumours. Acta Neuropathol 2008; 116: 597–602.
- Kraus, JA, Koopmann, J, Kaskel, P, et al. Shared allelic losses on chromosomes 1p and 19q suggest a common origin of oligodendroglioma and oligoastrocytoma. J Neuropath Exp Neurol 1995; 54: 91–5.
-
Coons, SW, Johnson, PC, Scheithauer, BW, et al. Improving diagnostic accuracy and interobserver concordance in the classification and grading of primary gliomas. Cancer 1997; 79: 1381–93.
10.1002/(SICI)1097-0142(19970401)79:7<1381::AID-CNCR16>3.0.CO;2-W CAS PubMed Web of Science® Google Scholar
- Maintz, D, Fiedler, K, Koopmann, J, et al. Molecular genetic evidence for subtypes of oligoastrocytomas. J Neuropathol Exp Neurol 1997; 56: 1098–104.
- Lorente, A, Mueller, W, Urdangarín, E, et al. RASSF1A, BLU, NORE1A, PTEN and MGMT expression and promoter methylation in gliomas and glioma cell lines and evidence of deregulated expression of de novo DNMTs. Brain Pathol 2009; 19: 279–92.
- Chang, EF, Potts, MB, Keles, GE, et al. Seizure characteristics and control following resection in 332 patients with low-grade gliomas. J Neurosurg 2008; 108: 227–35.
- Sanders, WP, Chistoforidis, GA. Imaging of low-grade primary brain tumours, in The Practical Management of Low-Grade Primary Brain Tumours (eds JP Rock, ML Rosenblum, EG Shaw, JG Cairncross), 1999; Lippincott Williams & Wilkins, Philadelphia, pp. 5–32.
- Law, M, Yang, S, Wang, H, et al. Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging. AJNR Am J Neuroradiol 2003; 24: 1989–98.
- Zonari, P, Baraldi, P, Crisi, G. Multimodal MRI in the characterization of glial neoplasms: the combined role of single-voxel MR spectroscopy, diffusion imaging and echo-planar perfusion imaging. Neuroradiology 2007; 49: 795–803.
- Guillevin, R, Menuel, C, Duffau, H, et al. Proton magnetic resonance spectroscopy predicts proliferative activity in diffuse low-grade gliomas. J Neurooncol 2008; 87: 181–7.
- Reijneveld, JC, van der Grond, J, Ramos, LM, et al. Proton MRS imaging in the follow-up of patients with suspected low-grade gliomas. Neuroradiology 2005; 47: 887–91.
- Danchaivijitr, N, Waldman, AD, Tozer, DJ, et al. Low-grade gliomas: do changes in rCBV measurements at longitudinal perfusion-weighted MR imaging predict malignant transformation? Radiology 2008; 247: 170–8.
- Cha, S, Tihan, T, Crawfoed, F, et al. Differentiation of low-grade oligodendrogliomas from low-grade astrocytomas by using quantitative blood-volume measurements derived from dynamic susceptibility contrast-enhanced MR imaging. AJNR Am J Neuroradiol 2005; 26: 266–73.
- Law, M, Yang, S, Babb, JS, et al. Comparison of cerebral blood volume and vascular permeability from dynamic susceptibility contrast-enhanced perfusion MR imaging with glioma grade. AJNR Am J Neuroradiol 2004; 25: 746–55.
- Khayal, IS, McKnight, TR, McGue, C, et al. Apparent diffusion coefficient and fractional anisotropy of newly diagnosed grade II gliomas. NMR Biomed 2009; 22: 449–55.
- Khayal, IS, Crawford, FW, Saraswathy, S. Relationship between choline and apparent diffusion coefficient in patients with gliomas. J Magn Reson Imaging 2008; 27: 718–25.
- Jenkinson, MD, du Plessis, DG, Smith, TS, et al. Histological growth patterns and genotype in oligodendroglial tumours: correlation with MRI features. Brain 2006; 129: 1884–91.
- Brown, R, Zlatescu, M, Sijben, A, et al. The use of magnetic resonance imaging to noninvasively detect genetic signatures in oligodendroglioma. Clin Cancer Res 2008; 14: 2357–62.
- Di Chiro, G, Brooks, RA. PET -FDG of untreated and treated cerebral gliomas. J Nucl Med 1988; 29: 421–3.
- Minn, H. PET and SPECT in low-grade gliomas. Eur J Radiol 2005; 56: 171–8.
- Kaschten, B, Stevenaert, A, Sadzot, B, et al. Preoperative evaluation of 54 gliomas by PET with fluorine-18-fluorodeoxyglucose and/or carbon-11-methionine. J Nucl Med 1998; 39: 778–85.
- Herholz, K, Holzer, T, Bauer, B, et al. 11C-methionine PET for differential diagnosis of low-grade gliomas. Neurology 1998; 50: 1316–22.
- Pirotte, B, Goldman, S, Massager, N, et al. Comparison of 18F-FDG and 11C-methionine for PET-guided stereotactic brain biopsy of gliomas. J Nucl Med 2004; 45: 1293–8.
- Nuutinen, J, Sonninen, P, Lehikoinen, P. Radiotherapy treatment planning and long-term followup with [(11)C] methionine PET in patients with low-grade astrocytoma. Int J Radiat Oncol Biol Phys 2000; 48: 43–52.
- Jacobs, AH, Thomas, A, Kracht, LW, et al. 18F-fluoro -L-thymidine and 11C-methylmethionine as markers of increased transport and proliferation in brain tumours. J Nucl Med 2005; 46: 1948–58.
- Pignatti, F, van den Bent, MJ, Curran, D, et al. Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 2002; 20: 2076–84.
- Lebrun, C, Fontaine, D, Ramaioli, A, et al. Long-term outcome of oligodendrogliomas. Neurology 2004; 62: 1783–7.
- Pallud, J, Capelle, L, Taillandier, L, et al. Prognostic signifi-cance of imaging contrast enhancement for WHO grade II gliomas. Neuro Oncol 2009; 11: 176–82.
- Chaichana, KL, McGirt, MJ, Niranjan, A. Prognostic signifi-cance of contrast-enhancing low-grade gliomas in adults and a review of the literature. Neurol Res 2009; 31: 931–9.
- Law, M, Young, RJ, Babb, JS, et al. Gliomas: predicting time to progression or survival with cerebral blood volume measurements at dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology 2008; 247: 490–8.
-
Ribom, D, Eriksson, A, Hartman, M, et al. Positron emission tomography (11)C-methionine and survival in patients with low-grade gliomas. Cancer 2001; 92: 1541–9.
10.1002/1097-0142(20010915)92:6<1541::AID-CNCR1480>3.0.CO;2-D CAS PubMed Web of Science® Google Scholar
- Smith, JS, Perry, A, Borell, TJ, et al. Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 2000; 18: 636–45.
- Kujas, M, Lejeune, J, Benouaich-Amiel, A, et al Chromosome 1p loss: a favorable prognostic factor in low-grade gliomas. Ann Neurol 2005; 58: 322–6.
- Weller, M, Berger, H, Hartmann, C, et al. Combined 1p/19q loss in oligodendroglial tumours: predictive or prognostic biomarker? Clin Cancer Res 2007; 13: 6933–7.
- Komine, C, Watanabe, T, Katayama, Y, et al. Promoter hypermethylation of the DNA repair gene O6-methylguanine-DNA methyltransferase is an independent predictor of shortened progression free survival in patients with low-grade diffuse astrocytomas. Brain Pathol 2003; 13: 176–84.
- Everhard, S, Kaloshi, G, Crinière, E, et al. MGMT methylation: a marker of response to temozolomide in low-grade gliomas. Ann Neurol 2006; 60: 740–3.
- Sanson, M, Marie, Y, Paris, S, et al. Isocitrate dehydrogenase 1 codon 132 mutation is an important prognostic biomarker in gliomas. J Clin Oncol 2009; 27: 4150–4.
- Marson, A, Jacoby, A, Johnson, A, et al. Immediate versus deferred antiepileptic drug treatment for early epilepsy and single seizures: a randomised controlled trial. Lancet 2005; 365: 2007–13.
- Glantz, MJ, Cole, BF, Forsyth, PA, et al. Practice parameter: anticonvulsant prophylaxis in patients with newly diagnosed brain tumours. Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2000; 54: 1886–93.
- Perry, J, Zinman, L, Chambers, A, et al. The use of prophylactic anticonvulsants in patients with brain tumours–a systematic review. Curr Oncology 2006; 13: 222–9.
- Tremont-Lukas, IW, Ratilal, BO, Armstrong, T, et al. Anti-epileptic drugs for preventing seizures in patients with brain tumours (Review). Cochrane Database Syst Rev 2008; 2, Art No CD004424.
- ILAE Treatment Guidelines. Evidence -based analysis of antiepileptic drug efficacy and effectiveness as initial monotherapy for epileptic seizures and syndromes. Epilepsia 2006; 47: 1094–120.
- Wilby, J, Kainth, A, Hawkins, N, et al. Clinical effectiveness, tolerability and cost effectiveness of newer drugs for epilepsy in adults: a systematic review and economic evaluation. Health Technol Assess 2005; 9: 1–157.
-
Marson, AG, Appleton, R, Baker, GA, et al. A randomised controlled trial examining the longerterm outcomes of standard versus new antiepileptic drugs. The SANAD trial. Health Technol Assess 2007; 11: 1–134.
10.3310/hta11370 Google Scholar
- Bello, L, Gallucci, M, Fava, M, et al. Intraoperative subcortical language tract mapping guides surgical removal of gliomas involving speech areas. Neurosurgery 2007; 60: 67–80.
- Smith, JS, Chang, EF, Lamborn, KR, et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 2008; 26: 1338–45.
- Duffau, H. Surgery of low-grade gliomas: towards a functional neurooncology. Curr Opin Oncol 2009; 21: 543–9.
- Keles, GE, Lamborn, KR, Berger, MS. Low grade hemispheric gliomas in adults: a critical review of extent of resection as a factor influencing outcome. J Neurosurg 2001; 95: 735–45.
- Karim, AB, Afra, D, Cornu, P, et al. Randomized trial on the efficacy of radiotherapy for cerebral low-grade glioma in the adult: European Organization for Research and Treatment of Cancer Study 22845 with the Medical Research Council study BRO4: an interim analysis. Int J Radiat Oncol Biol Phys 2002; 52: 316–24.
-
Berger, MS, Deliganis, AV, Dobbins, J, Keles, GE. The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer 1994; 74: 1784–91.
10.1002/1097-0142(19940915)74:6<1784::AID-CNCR2820740622>3.0.CO;2-D CAS PubMed Web of Science® Google Scholar
- Claus, EB, Horlacher, A, Hsu, L, et al. Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer 2005; 103: 1227–33.
- Shaw, EG, Berkey, B, Coons, SW, et al. Recurrence following neurosurgeon-determined grosstotal resection of adult supratentorial low-grade glioma: results of a prospective clinical trial. J Neurosurg 2008; 109: 835–41.
- Recht, LD, Lew, R, Smith, TW. Suspected low-grade glioma: is deferring treatment safe? Ann Neurol 1992; 31: 431–6.
- Reijneveld, JC, Sitskoorn, MM, Klein, M, et al. Cognitive status and quality of life in patients with suspected versus proven low-grade gliomas. Neurology 2001; 56: 618–23.
- Olson, JD, Riedel, E, DeAngelis, LM. Long-term outcome of low-grade oligodendroglioma and mixed glioma. Neurology 2000; 54: 1442–8.
- van den Bent, MJ, Afra, D, de Witte, O, et al. EORTC Radiotherapy and Brain Tumour Groups and the UK Medical Research Council. Long-term efficacy of early versus delayed radiotherapy for low-grade astrocytoma and oligodendroglioma in adults: the EORTC 22845 randomised trial. Lancet 2005; 366: 985–90.
- Soffietti, R, Borgognone, M, Ducati, A, et al. Efficacy of radiation therapy on seizures in low-grade astrocytomas. Neuro-Oncol 2005; 7. 389. (suppl. World Congress of Neuro-Oncology, Ediburgh, 2005).
- Shaw, E, Arusell, R, Scheithauer, B, et al. Prospective randomized trial of low-versus high-dose radiation therapy in adults with supratentorial low-grade glioma: initial report of a North Central Cancer Treatment Group/Radiation Therapy Oncology Group/Eastern Cooperative Oncology Group study. J Clin Oncol 2002; 20: 2267–76.
- Karim, AB, Maat, B, Hatlevoll, R, et al. A randomized trial on dose-response in radiation therapy of low-grade cerebral glioma: European Organization for Research and Treatment of Cancer (EORTC) Stud. 22844. Int J Radiat Oncol Biol Phys 1996; 36: 549–56.
- Kiebert, GM, Curran, D, Aaronson, NK, et al. Quality of life after radiation therapy of cerebral low-grade gliomas of the adult: results of a randomised phase III trial on dose response (EORTC trial 22844). Eur J Cancer 1998; 34: 1902–9.
-
Shaw, EG, Wang, M, Coons, SW, et al. Final report of Radiation Therapy Oncology Group (RTOG) protocol 9802: radiation therapy (RT) versus RT + procarbazine, CCNU and vincristine (PCV) chemotherapy for adult low-grade gliomas (LGG). J Clin Oncol 2008; 26: 90s. 2006.
10.1200/jco.2008.26.15_suppl.2006 Google Scholar
- Surma-aho, O, Niemelä, M, Vilkki, J, et al. Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients. Neurology 2001; 56: 1285–90.
- Taphoorn, MJ, Schiphorst, AK, Snoek, FJ, et al. Cognitive functions and quality of life in patients with low-grade gliomas: the impact of radiotherapy. Ann Neurol 1994; 36: 48–54.
- Klein, M, Heimans, JJ, Aaronson, NK, et al. Effect of radiotherapy and other treatment-related factors on mid-term to long-term cognitive sequelae in low-grade gliomas: a comparative study. Lancet 2002; 360: 1361–8.
- Laack, NN, Brown, PD., Ivnik, RJ, et al. Cognitive function after radiotherapy for supratentorial low-grade glioma: a North Central Cancer Treatment Group prospective study. Int J Radiat Oncol Biol Phys 2005; 63: 1175–83.
- Douw, L, Klein, M, Fagel, SS, et al. Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term follow -up. Lancet Neurol 2009; 8: 810–18.
- Soffietti, R, Rudà, R., Bradac, GB, Schiffer, D. PCV chemotherapy for recurrent oligodendrogliomas and oligoastrocytomas. Neurosurgery 1998; 43: 1066–73.
- van den Bent, MJ, Kros, JM, Heimans, JJ, et al. Response rate and prognostic factors of recurrent oligodendroglioma treated with procarbazine, CCNU, and vincristine chemotherapy. Dutch Neuro-oncology Group. Neurology 1998; 51: 1140–5.
- van den Bent, MJ, Taphoorn, MJ, Brandes, AA, et al. Phase II study of first-line chemotherapy with temozolomide in recurrent oligodendroglial tumours: the European Organization for Research and Treatment of Cancer Brain Tumour Group Stud. 26971. J Clin Oncol 2003; 21: 2525–8.
- Pace, A, Vidiri, A, Galiè, E, et al. Temozolomide chemotherapy for progressive low-grade glioma: clinical benefits and radiological response. Ann Oncol 2003; 14: 1722–6.
- Quinn, JA, Reardon, DA, Friedman, AH, et al. Phase II trial of temozolomide in patients with progressive low-grade glioma. J Clin Oncol 2003; 21: 646–51.
- Brada, M, Viviers, L, Abson, C, et al. Phase II study of primary temozolomide chemotherapy in patients with WHO grade II gliomas. Ann Oncol 2003; 14: 1715–21.
- Buckner, JC, Gesme, D, Jr, O'Fallon, JR, et al. Phase II trial of procarbazine, lomustine, and vincristine as initial therapy for patients with low-grade oligodendroglioma or oligoastrocytoma: efficacy and associations with chromosomal abnormalities. J Clin Oncol 2003; 21: 251–5.
- Hoang-Xuan, K, Capelle, L, Kujas, M, et al. Temozolomide as initial treatment for adults with low-grade oligodendrogliomas or oligoastrocytomas and correlation with chromosome 1p deletions. J Clin Oncol 2004; 22: 3133–8.
- Kaloshi, G, Benouaich-Amiel, A, Diakite, F, et al. Temozolomide for low-grade gliomas: predictive impact of 1p/19q loss on response and outcome. Neurology 2007; 68: 1831–6.
- Frenay, MP, Fontaine, D, Vandenbos, F, et al. First-line nitrosourea-based chemotherapy in symptomatic non-resectable supratentorial pure low-grade astrocytomas. Eur J Neurol 2005; 12: 685–90.
- Kesari, S, Schiff, D, Drappatz, J, et al. Phase II study of protracted daily temozolomide for lowgrade gliomas in adults. Clin Cancer Res 2009; 15: 330–7.
- Tosoni, A, Franceschi, E, Ermani, M, et al. Temozolomide three weeks on and one week off as first-line therapy for patients with recurrent or progressive low-grade gliomas. J Neurooncol 2008; 89: 179–85.
- Duffau, H, Taillandier, L, Capelle, L. Radical surgery after chemotherapy: a new therapeutic strategy to envision in grade II glioma. J Neurooncol 2006; 80: 171–6.
- Tucha, O, Smely, C, Preier, M, Lange, KW. Cognitive deficits before treatment among patients with brain tumours. Neurosurgery 2000; 47: 324–33.
- Hahn, CA, Dunn, RH, Logue, PE, et al. Prospective study of neuropsychologic testing and quality-of-life assessment of adults with primary malignant brain tumours. Int J Radiat Oncol Biol Phys 2003; 55: 992–9.
- Yoshii, Y, Tominaga, D, Sugimoto, K, et al. Cognitive function of patients with brain tumour in pre-and postoperative stage. Surgical Neurol 2008; 69: 51–61.
- Meador, KJ. Cognitive outcomes and predictive factors in epilepsy. Neurology 2002; 58: 21–6.
- Meador, KJ. Cognitive and memory effects of the new antiepileptic drugs. Epilepsy Res 2006; 68: 63–7.
- Gehring, K, Sitskoorn, MM, Gundy, CM, et al. Cognitive rehabilitation in patients with gliomas: a randomized, controlled trial. J Clin Oncol 2009; 27: 3712–22.