Advertisement

Clinical and Translational Oncology

, Volume 20, Issue 8, pp 989–1003 | Cite as

From imaging to biology of glioblastoma: new clinical oncology perspectives to the problem of local recurrence

  • A. Zygogianni
  • M. Protopapa
  • A. Kougioumtzopoulou
  • F. Simopoulou
  • S. Nikoloudi
  • V. Kouloulias
Review Article

Abstract

GBM is one of the most common and aggressive brain tumors. Surgery and adjuvant chemoradiation have succeeded in providing a survival benefit. Although most patients will eventually experience local recurrence, the means to fight recurrence are limited and prognosis remains poor. In a disease where local control remains the major challenge, few trials have addressed the efficacy of local treatments, either surgery or radiation therapy. The present article reviews recent advances in the biology, imaging and biomarker science of GBM as well as the current treatment status of GBM, providing new perspectives to the problem of local recurrence.

Keywords

Glioblastoma multiforme Radiotherapy Recurrence Re-irradiation Review 

Notes

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical statements

This is a review article and for this type of study formal consent is not required. Moreover, this manuscript does not involve human participants and/or animals.

References

  1. 1.
    McNeill KA. Epidemiology of brain tumors. Neurol Clin. 2016;34:981–98.PubMedCrossRefGoogle Scholar
  2. 2.
    Stupp R, Brada M, van den Bent MJ, Tonn J-C, Pentheroudakis G, ESMO Guidelines Working Group. High-grade glioma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2014;25:iii93–101.PubMedCrossRefGoogle Scholar
  3. 3.
    Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C, et al. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neuro-oncology. 2015;17(Suppl 4):iv1–62.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Kelly PJ. Computed tomography and histologic limits in glial neoplasms: tumor types and selection for volumetric resection. Surg Neurol. 1993;39:458–65.PubMedCrossRefGoogle Scholar
  5. 5.
    Müller C, Holtschmidt J, Auer M, Heitzer E, Lamszus K, Schulte A, et al. Hematogenous dissemination of glioblastoma multiforme. Sci Transl Med. 2014;6:247ra101-1 (American Association for the Advancement of Science).CrossRefGoogle Scholar
  6. 6.
    Gil-Salú JL, Román P, Benítez E, Maestro E, Pérez-Requena J, López-Escobar M. Survival analysis following the addition of temozolomide to surgery and radiotherapy in patients with glioblastoma multiforme. Neurocirugia (Asturias). 2004;15:144–50.CrossRefGoogle Scholar
  7. 7.
    Keime-Guibert F, Chinot O, Taillandier L, Cartalat-Carel S, Frenay M, Kantor G, et al. Radiotherapy for glioblastoma in the elderly. N Engl J Med. 2007;356:1527–35 (Massachusetts Medical Society).PubMedCrossRefGoogle Scholar
  8. 8.
    Farah P, Blanda R, Kromer C, Ostrom QT, Kruchko C, Barnholtz-Sloan JS. Conditional survival after diagnosis with malignant brain and central nervous system tumor in the United States, 1995–2012. J Neurooncol. 2016;128:419–29.PubMedCrossRefGoogle Scholar
  9. 9.
    Nicholas MK, Lukas RV, Chmura S, Yamini B, Lesniak M, Pytel P. Molecular heterogeneity in glioblastoma: therapeutic opportunities and challenges. Semin Oncol. 2011;38:243–53.PubMedCrossRefGoogle Scholar
  10. 10.
    Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131:803–20 (Springer Berlin Heidelberg).PubMedCrossRefGoogle Scholar
  11. 11.
    Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007;114:97–109 (Springer-Verlag).PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Parsons DW, Jones S, Zhang X, Lin JC-H, Leary RJ, Angenendt P, et al. An integrated genomic analysis of human glioblastoma multiforme. Science. 2008;321:1807–12 (American Association for the Advancement of Science).PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455:1061–8.CrossRefGoogle Scholar
  14. 14.
    Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17:98–110.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Hervey-Jumper SL, Berger MS. Maximizing safe resection of low- and high-grade glioma. J Neurooncol. 2016;130:269–82 (Springer US).PubMedCrossRefGoogle Scholar
  16. 16.
    Brown TJ, Brennan MC, Li M, Church EW, Brandmeir NJ, Rakszawski KL, et al. Association of the extent of resection with survival in glioblastoma: a systematic review and meta-analysis. JAMA Oncol. 2016;2:1460–9 (American Medical Association).PubMedCrossRefGoogle Scholar
  17. 17.
    Delgado-López PD, Corrales-García EM. Survival in glioblastoma: a review on the impact of treatment modalities. Clin Transl Oncol. 2016;18:1062–71.PubMedCrossRefGoogle Scholar
  18. 18.
    Li J, Wang M, Won M, Shaw EG, Coughlin C, Curran WJ, et al. Validation and simplification of the Radiation Therapy Oncology Group recursive partitioning analysis classification for glioblastoma. Int J Radiat Oncol Biol Phys. 2011;81:623–30.PubMedCrossRefGoogle Scholar
  19. 19.
    Scott JG, Bauchet L, Fraum TJ, Nayak L, Cooper AR, Chao ST, et al. Recursive partitioning analysis of prognostic factors for glioblastoma patients aged 70 years or older. Cancer. 2012;118:5595–600 (Wiley Subscription Services, Inc., A Wiley Company).PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Curran WJ, Scott CB, Horton J, Nelson JS, Weinstein AS, Fischbach AJ, et al. Recursive partitioning analysis of prognostic factors in three Radiation Therapy Oncology Group malignant glioma trials. J Natl Cancer Inst. 1993;85:704–10.PubMedCrossRefGoogle Scholar
  21. 21.
    Hegi ME, Diserens A-C, Gorlia T, Hamou M-F, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352:997–1003 (Massachusetts Medical Society).PubMedCrossRefGoogle Scholar
  22. 22.
    Hegi ME, Liu L, Herman JG, Stupp R, Wick W, Weller M, et al. Correlation of O6-methylguanine methyltransferase (MGMT) promoter methylation with clinical outcomes in glioblastoma and clinical strategies to modulate MGMT activity. J Clin Oncol. 2008;26:4189–99.PubMedCrossRefGoogle Scholar
  23. 23.
    Brandes AA, Franceschi E, Tosoni A, Benevento F, Scopece L, Mazzocchi V, et al. Temozolomide concomitant and adjuvant to radiotherapy in elderly patients with glioblastoma: correlation with MGMT promoter methylation status. Cancer. 2009;115:3512–8 (Wiley Subscription Services, Inc., A Wiley Company).PubMedCrossRefGoogle Scholar
  24. 24.
    Lee SM, Koh H-J, Park D-C, Song BJ, Huh T-L, Park J-W. Cytosolic NADP(+)-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radic Biol Med. 2002;32:1185–96.PubMedCrossRefGoogle Scholar
  25. 25.
    Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E, et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature. 2012;483:479–83.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Cohen AL, Holmen SL, Colman H. IDH1 and IDH2 mutations in gliomas. Curr Neurol Neurosci Rep. 2013;13:345 (Current Science Inc).PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Chen R, Smith-Cohn M, Cohen AL, Colman H. Glioma subclassifications and their clinical significance. Neurotherapeutics. 2017;14:284–97.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Sathyan P, Zinn PO, Marisetty AL, Liu B, Kamal MM, Singh SK, et al. Mir-21–Sox2 axis delineates glioblastoma subtypes with prognostic impact. J Neurosci. 2015;35:15097–112 (Society for Neuroscience).PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Karsy M, Guan J, Cohen AL, Jensen RL, Colman H. New molecular considerations for glioma: IDH, ATRX, BRAF, TERT, H3 K27 M. Curr Neurol Neurosci Rep. 2017;17:19 (Springer US).PubMedCrossRefGoogle Scholar
  30. 30.
    Eckel-Passow JE, Lachance DH, Molinaro AM, Walsh KM, Decker PA, Sicotte H, et al. Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med. 2015;372:2499–508 (Massachusetts Medical Society).PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Arita H, Yamasaki K, Matsushita Y, Nakamura T, Shimokawa A, Takami H, et al. A combination of TERT promoter mutation and MGMT methylation status predicts clinically relevant subgroups of newly diagnosed glioblastomas. Acta Neuropathol Commun. 2016;4:79 (BioMed Central).PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Nguyen HN, Lie A, Li T, Chowdhury R, Liu F, Ozer B, et al. Human TERT promoter mutation enables survival advantage from MGMT promoter methylation in IDH1 wild-type primary glioblastoma treated by standard chemoradiotherapy. Neuro-oncology. 2017;19:394–404.PubMedGoogle Scholar
  33. 33.
    Fink JR, Muzi M, Peck M, Krohn KA. Multimodality brain tumor imaging: MR imaging, PET, and PET/MR imaging. J Nucl Med. 2015;56:1554–61 (Society of Nuclear Medicine).PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Young RM, Jamshidi A, Davis G, Sherman JH. Current trends in the surgical management and treatment of adult glioblastoma. Ann Transl Med. 2015;3:121.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Herneth AM, Guccione S, Bednarski M. Apparent diffusion coefficient: a quantitative parameter for in vivo tumor characterization. Eur J Radiol. 2003;45:208–13.PubMedCrossRefGoogle Scholar
  36. 36.
    Essayed WI, Zhang F, Unadkat P, Cosgrove GR, Golby AJ, O’Donnell LJ. White matter tractography for neurosurgical planning: a topography-based review of the current state of the art. Neuroimage Clin. 2017;15:659–72.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Martín Noguerol T, Sánchez-González J, Martínez Barbero JP, García-Figueiras R, Baleato-González S, Luna A. Clinical imaging of tumor metabolism with 1H magnetic resonance spectroscopy. Magn Reson Imaging Clin N Am. 2016;24:57–86.PubMedCrossRefGoogle Scholar
  38. 38.
    Sawlani V, Taylor R, Rowley K, Redfern R, Martin J, Poptani H. Magnetic resonance spectroscopy for differentiating pseudo-progression from true progression in GBM on concurrent chemoradiotherapy. Neuroradiol J. 2012;25:575–86 (SAGE Publications, Sage UK: London, England).PubMedCrossRefGoogle Scholar
  39. 39.
    Nguyen ML, Willows B, Khan R, Chi A, Kim L, Nour SG, et al. The potential role of magnetic resonance spectroscopy in image-guided radiotherapy. Front Oncol. 2014;4:91.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Mabray MC, Barajas RF, Cha S. Modern brain tumor imaging. Brain Tumor Res Treat. 2015;3:8–23.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Zinn PO, Mahmood Z, Elbanan MG, Colen RR. Imaging Genomics in Gliomas. Cancer J. 2015;21:225–34.PubMedCrossRefGoogle Scholar
  42. 42.
    Pope WB. Genomics of brain tumor imaging. Neuroimaging Clin N Am. 2015;25:105–19.PubMedCrossRefGoogle Scholar
  43. 43.
    Anil R, Colen RR. Imaging genomics in glioblastoma multiforme: a predictive tool for patients prognosis, survival, and outcome. Magn Reson Imaging Clin N Am. 2016;24:731–40.PubMedCrossRefGoogle Scholar
  44. 44.
    Tolia M, Verganelakis D, Tsoukalas N, Kyrgias G, Papathanasiou M, Mosa E, et al. Prognostic value of MRS metabolites in postoperative irradiated high grade gliomas. Biomed Res Int Hindawi. 2015;2015:341042–6.Google Scholar
  45. 45.
    Tran DKT, Jensen RL. Treatment-related brain tumor imaging changes: so-called “pseudoprogression” vs. tumor progression: Review and future research opportunities. Surg Neurol Int. 2013;4:S129–35.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Brandsma D, Stalpers L, Taal W, Sminia P, van den Bent MJ. Clinical features, mechanisms, and management of pseudoprogression in malignant gliomas. Lancet Oncol. 2008;9:453–61.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Chinot OL, Macdonald DR, Abrey LE, Zahlmann G, Kerloëguen Y, Cloughesy TF. Response assessment criteria for glioblastoma: practical adaptation and implementation in clinical trials of antiangiogenic therapy. Curr Neurol Neurosci Rep. 2013;13:347 (Current Science Inc).PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol. 2010;28:1963–72.PubMedCrossRefGoogle Scholar
  49. 49.
    Protopapa M, Zygogianni A, Stamatakos GS, Antypas C, Armpilia C, Uzunoglu NK, et al. Clinical implications of in silico mathematical modeling for glioblastoma: a critical review. J Neurooncol. 2017;25:93-11 (Springer US).Google Scholar
  50. 50.
    Weller M, van den Bent M, Hopkins K, Tonn JC, Stupp R, Falini A, et al. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol. 2014;15:e395–403.PubMedCrossRefGoogle Scholar
  51. 51.
    Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg. 2001;95:190–8.PubMedCrossRefGoogle Scholar
  52. 52.
    Sanai N, Polley M-Y, McDermott MW, Parsa AT, Berger MS. An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg. 2011;115:3–8 (American Association of Neurological Surgeons).PubMedCrossRefGoogle Scholar
  53. 53.
    Chaichana KL, Jusue-Torres I, Navarro-Ramirez R, Raza SM, Pascual-Gallego M, Ibrahim A, et al. Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro-oncology. 2014;16:113–22.PubMedCrossRefGoogle Scholar
  54. 54.
    Yogarajah M, Focke NK, Bonelli SB, Thompson P, Vollmar C, McEvoy AW, et al. The structural plasticity of white matter networks following anterior temporal lobe resection. Brain. 2010;133:2348–64.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Eyüpoglu IY, Hore N, Savaskan NE, Grummich P, Roessler K, Buchfelder M, et al. Improving the extent of malignant glioma resection by dual intraoperative visualization approach. Berger M, editor. PLoS One. 2012;7:e44885 (Public Library of Science).PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Hadjipanayis CG, Widhalm G, Stummer W. What is the surgical benefit of utilizing 5-aminolevulinic acid for fluorescence-guided surgery of malignant gliomas? Neurosurgery. 2015;77:663–73.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Hauser SB, Kockro RA, Actor B, Sarnthein J, Bernays R-L. Combining 5-aminolevulinic acid fluorescence and intraoperative magnetic resonance imaging in glioblastoma surgery: a histology-based evaluation. Neurosurgery. 2016;78:475–83.PubMedCrossRefGoogle Scholar
  58. 58.
    Walker MD, Alexander E, Hunt WE, MacCarty CS, Mahaley MS, Mealey J, et al. Evaluation of BCNU and/or radiotherapy in the treatment of anaplastic gliomas. A cooperative clinical trial. J Neurosurg. 1978;49:333–43.PubMedCrossRefGoogle Scholar
  59. 59.
    Corso CD, Bindra RS, Mehta MP. The role of radiation in treating glioblastoma: here to stay. J Neurooncol. 2017;134:479–85 (Springer US).PubMedCrossRefGoogle Scholar
  60. 60.
    Walker MD, Strike TA, Sheline GE. An analysis of dose–effect relationship in the radiotherapy of malignant gliomas. Int J Radiat Oncol Biol Phys. 1979;5:1725–31.PubMedCrossRefGoogle Scholar
  61. 61.
    Wallner KE, Galicich JH, Krol G, Arbit E, Malkin MG. Patterns of failure following treatment for glioblastoma multiforme and anaplastic astrocytoma. Int J Radiat Oncol Biol Phys. 1989;16:1405–9.PubMedCrossRefGoogle Scholar
  62. 62.
    Shapiro WR, Green SB, Burger PC, Mahaley MS, Selker RG, VanGilder JC, et al. Randomized trial of three chemotherapy regimens and two radiotherapy regimens and two radiotherapy regimens in postoperative treatment of malignant glioma. Brain Tumor Cooperative Group Trial 8001. J Neurosurg. 1989;71:1–9.PubMedCrossRefGoogle Scholar
  63. 63.
    Chan JL, Lee SW, Fraass BA, Normolle DP, Greenberg HS, Junck LR, et al. Survival and failure patterns of high-grade gliomas after three-dimensional conformal radiotherapy. J Clin Oncol. 2002;20:1635–42.PubMedCrossRefGoogle Scholar
  64. 64.
    Nelson DF, Diener-West M, Horton J, Chang CH, Schoenfeld D, Nelson JS. Combined modality approach to treatment of malignant gliomas—re-evaluation of RTOG 7401/ECOG 1374 with long-term follow-up: a joint study of the Radiation Therapy Oncology Group and the Eastern Cooperative Oncology Group. NCI Monogr. 1988;6:279–84.Google Scholar
  65. 65.
    Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–96.PubMedCrossRefGoogle Scholar
  66. 66.
    Niyazi M, Brada M, Chalmers AJ, Combs SE, Erridge SC, Fiorentino A, et al. ESTRO-ACROP guideline “target delineation of glioblastomas”. Radiother Oncol. 2016;118:35–42.PubMedCrossRefGoogle Scholar
  67. 67.
    Sulman EP, Ismaila N, Chang SM. Radiation therapy for glioblastoma: American Society of Clinical Oncology Clinical Practice Guideline Endorsement of the American Society for Radiation Oncology Guideline. J Oncol Pract. 2017;13:123–7.PubMedCrossRefGoogle Scholar
  68. 68.
    Ataman F, Poortmans P, Stupp R, Fisher B, Mirimanoff R-O. Quality assurance of the EORTC 26981/22981; NCIC CE3 intergroup trial on radiotherapy with or without temozolomide for newly-diagnosed glioblastoma multiforme: the individual case review. Eur J Cancer. 2004;40:1724–30.PubMedCrossRefGoogle Scholar
  69. 69.
    Malmström A, Grønberg BH, Marosi C, Stupp R, Frappaz D, Schultz H, et al. Temozolomide versus standard 6-week radiotherapy versus hypofractionated radiotherapy in patients older than 60 years with glioblastoma: the Nordic randomised, phase 3 trial. Lancet Oncol. 2012;13:916–26.PubMedCrossRefGoogle Scholar
  70. 70.
    Wick W, Platten M, Meisner C, Felsberg J, Tabatabai G, Simon M, et al. Temozolomide chemotherapy alone versus radiotherapy alone for malignant astrocytoma in the elderly: the NOA-08 randomised, phase 3 trial. Lancet Oncol. 2012;13:707–15.PubMedCrossRefGoogle Scholar
  71. 71.
    Roa W, Kepka L, Kumar N, Sinaika V, Matiello J, Lomidze D, et al. International atomic energy agency randomized phase III study of radiation therapy in elderly and/or frail patients with newly diagnosed glioblastoma multiforme. J Clin Oncol. 2015;33:4145–50.PubMedCrossRefGoogle Scholar
  72. 72.
    Cao JQ, Fisher BJ, Bauman GS, Megyesi JF, Watling CJ, Macdonald DR. Hypofractionated radiotherapy with or without concurrent temozolomide in elderly patients with glioblastoma multiforme: a review of ten-year single institutional experience. J Neurooncol. 2012;107:395–405 (7 ed., Springer US).PubMedCrossRefGoogle Scholar
  73. 73.
    Azoulay M, Santos F, Souhami L, Panet-Raymond V, Petrecca K, Owen S, et al. Comparison of radiation regimens in the treatment of Glioblastoma multiforme: results from a single institution. Radiat Oncol. 2015;10:106 (BioMed Central).PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Kouloulias V, Zygogianni A, Kouvaris J, Platoni K, Georgakopoulos J, Boviatsis E, et al. Hypofractionated irradiation for gliomas with 45.5 Gy in 13 fractions: a retrospective study. J Neurosurg Sci. 2015;59:447–53.PubMedGoogle Scholar
  75. 75.
    Kaul D, Florange J, Badakhshi H, Grün A, Ghadjar P, Exner S, et al. Accelerated hyperfractionation plus temozolomide in glioblastoma. Radiat Oncol. 2016;11:70 (BioMed Central).PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Badiyan SN, Markovina S, Simpson JR, Robinson CG, DeWees T, Tran DD, et al. Radiation therapy dose escalation for glioblastoma multiforme in the era of temozolomide. Int J Radiat Oncol Biol Phys. 2014;90:877–85.PubMedCrossRefGoogle Scholar
  77. 77.
    Iuchi T, Hatano K, Narita Y, Kodama T, Yamaki T, Osato K. Hypofractionated high-dose irradiation for the treatment of malignant astrocytomas using simultaneous integrated boost technique by IMRT. Int J Radiat Oncol Biol Phys. 2006;64:1317–24.PubMedCrossRefGoogle Scholar
  78. 78.
    Tsien CI, Brown D, Normolle D, Schipper M, Piert M, Junck L, et al. Concurrent temozolomide and dose-escalated intensity-modulated radiation therapy in newly diagnosed glioblastoma. Clin Cancer Res. 2012;18:273–9.PubMedCrossRefGoogle Scholar
  79. 79.
    Giordano FA, Brehmer S, Abo-Madyan Y, Welzel G, Sperk E, Keller A, et al. INTRAGO: intraoperative radiotherapy in glioblastoma multiforme—a phase I/II dose escalation study. BMC Cancer. 2014;14:992 (BioMed Central).PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Miyatake S-I, Kawabata S, Hiramatsu R, Kuroiwa T, Suzuki M, Kondo N, et al. Boron neutron capture therapy for malignant brain tumors. Neurol. Med Chir (Tokyo). 2016;56:361–71 (The Japan Neurosurgical Society).CrossRefGoogle Scholar
  81. 81.
    Kageji T, Nagahiro S, Mizobuchi Y, Matsuzaki K, Nakagawa Y, Kumada H. Boron neutron capture therapy (BNCT) for newly-diagnosed glioblastoma: comparison of clinical results obtained with BNCT and conventional treatment. J Med Investig. 2014;61:254–63.CrossRefGoogle Scholar
  82. 82.
    Mizumoto M, Yamamoto T, Ishikawa E, Matsuda M, Takano S, Ishikawa H, et al. Proton beam therapy with concurrent chemotherapy for glioblastoma multiforme: comparison of nimustine hydrochloride and temozolomide. J Neurooncol. 2016;130:165–70 (Springer US).PubMedCrossRefGoogle Scholar
  83. 83.
    Fitzek MM, Thornton AF, Rabinov JD, Lev MH, Pardo FS, Munzenrider JE, et al. Accelerated fractionated proton/photon irradiation to 90 cobalt gray equivalent for glioblastoma multiforme: results of a phase II prospective trial. J Neurosurg. 1999;91:251–60.PubMedCrossRefGoogle Scholar
  84. 84.
    Combs SE, Kieser M, Rieken S, Habermehl D, Jäkel O, Haberer T, et al. Randomized phase II study evaluating a carbon ion boost applied after combined radiochemotherapy with temozolomide versus a proton boost after radiochemotherapy with temozolomide in patients with primary glioblastoma: the CLEOPATRA trial. BMC Cancer. 2010;10:478 (BioMed Central).PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Mizoe J-E, Tsujii H, Hasegawa A, Yanagi T, Takagi R, Kamada T, et al. Phase I/II clinical trial of carbon ion radiotherapy for malignant gliomas: combined X-ray radiotherapy, chemotherapy, and carbon ion radiotherapy. Int J Radiat Oncol Biol Phys. 2007;69:390–6.PubMedCrossRefGoogle Scholar
  86. 86.
    Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA, et al. Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: a randomized clinical trial. JAMA. 2015;314:2535–43.PubMedCrossRefGoogle Scholar
  87. 87.
    Stupp R, Wong ET, Kanner AA, Steinberg D, Engelhard H, Heidecke V, et al. NovoTTF-100A versus physician’s choice chemotherapy in recurrent glioblastoma: a randomised phase III trial of a novel treatment modality. Eur J Cancer. 2012;48:2192–202.PubMedCrossRefGoogle Scholar
  88. 88.
    Kirson ED, Schneiderman RS, Dbalý V, Tovarys F, Vymazal J, Itzhaki A, et al. Chemotherapeutic treatment efficacy and sensitivity are increased by adjuvant alternating electric fields (TTFields). BMC Med Phys. 2009;9:1 (3rd ed., BioMed Central).PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Giladi M, Schneiderman RS, Voloshin T, Porat Y, Munster M, Blat R, et al. Mitotic spindle disruption by alternating electric fields leads to improper chromosome segregation and mitotic catastrophe in cancer cells. Sci Rep. 2015;5:18046 (Nature Publishing Group).PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Kirson ED, Dbalý V, Tovarys F, Vymazal J, Soustiel JF, Itzhaki A, et al. Alternating electric fields arrest cell proliferation in animal tumor models and human brain tumors. Proc Natl Acad Sci USA. 2007;104:10152–7.PubMedCrossRefGoogle Scholar
  91. 91.
    Kirson ED, Gurvich Z, Schneiderman R, Dekel E, Itzhaki A, Wasserman Y, et al. Disruption of cancer cell replication by alternating electric fields. Cancer Res. 2004;64:3288–95.PubMedCrossRefGoogle Scholar
  92. 92.
    Mrugala MM, Engelhard HH, Dinh Tran D, Kew Y, Cavaliere R, Villano JL, et al. Clinical practice experience with NovoTTF-100A™ system for glioblastoma: the Patient Registry Dataset (PRiDe). Semin Oncol. 2014;41(Suppl 6):S4–13.PubMedCrossRefGoogle Scholar
  93. 93.
    Kanner AA, Wong ET, Villano JL, Ram Z. EF-11 Investigators. Post Hoc analyses of intention-to-treat population in phase III comparison of NovoTTF-100A™ system versus best physician’s choice chemotherapy. Semin Oncol. 2014;41(Suppl 6):S25–34.PubMedCrossRefGoogle Scholar
  94. 94.
    Oberoi RK, Parrish KE, Sio TT, Mittapalli RK, Elmquist WF, Sarkaria JN. Strategies to improve delivery of anticancer drugs across the blood-brain barrier to treat glioblastoma. Neuro-oncology. 2016;18:27–36.PubMedCrossRefGoogle Scholar
  95. 95.
    Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJB, Janzer RC, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10:459–66.PubMedCrossRefGoogle Scholar
  96. 96.
    Gilbert MR, Wang M, Aldape KD, Stupp R, Hegi ME, Jaeckle KA, et al. Dose-dense temozolomide for newly diagnosed glioblastoma: a randomized phase III clinical trial. J Clin Oncol. 2013;31:4085–91.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Buglione M, Triggiani L, Borghetti P, Pedretti S, Pasinetti N, Magrini SM. The “radioresistance” of glioblastoma in the clinical setting, and the present therapeutic options Radiobiology of glioblastoma. Cham: Springer International Publishing; 2016. p. 15–27.Google Scholar
  98. 98.
    Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med. 2014;370:709–22 (Massachusetts Medical Society).PubMedCrossRefGoogle Scholar
  99. 99.
    Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 2014;370:699–708 (Massachusetts Medical Society).PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Brem H, Piantadosi S, Burger PC, Walker M, Selker R, Vick NA, et al. Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. The polymer-brain tumor treatment group. Lancet. 1995;345:1008–12.PubMedCrossRefGoogle Scholar
  101. 101.
    Westphal M, Hilt DC, Bortey E, Delavault P, Olivares R, Warnke PC, et al. A phase 3 trial of local chemotherapy with biodegradable carmustine (BCNU) wafers (Gliadel wafers) in patients with primary malignant glioma. Neuro-oncology. 2003;5:79–88.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Valtonen S, Timonen U, Toivanen P, Kalimo H, Kivipelto L, Heiskanen O, et al. Interstitial chemotherapy with carmustine-loaded polymers for high-grade gliomas: a randomized double-blind study. Neurosurgery. 1997;41:44–8 (discussion48–9).PubMedCrossRefGoogle Scholar
  103. 103.
    Ashby LS, Smith KA, Stea B. Gliadel wafer implantation combined with standard radiotherapy and concurrent followed by adjuvant temozolomide for treatment of newly diagnosed high-grade glioma: a systematic literature review. World J Surg Oncol. 2016;14:225 (BioMed Central).PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Gorlia T, Stupp R, Brandes AA, Rampling RR, Fumoleau P, Dittrich C, et al. New prognostic factors and calculators for outcome prediction in patients with recurrent glioblastoma: a pooled analysis of EORTC brain tumour group phase I and II clinical trials. Eur J Cancer. 2012;48:1176–84.PubMedCrossRefGoogle Scholar
  105. 105.
    Wu W, Lamborn KR, Buckner JC, Novotny PJ, Chang SM, O’Fallon JR, et al. Joint NCCTG and NABTC prognostic factors analysis for high-grade recurrent glioma. Neuro-oncology. 2010;12:164–72.PubMedCrossRefGoogle Scholar
  106. 106.
    Carson KA, Grossman SA, Fisher JD, Shaw EG. Prognostic factors for survival in adult patients with recurrent glioma enrolled onto the new approaches to brain tumor therapy CNS consortium phase I and II clinical trials. J Clin Oncol. 2007;25:2601–6.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Tosoni A, Franceschi E, Poggi R, Brandes AA. Relapsed glioblastoma: treatment strategies for initial and subsequent recurrences. Curr Treat Options Oncol. 2016;17:49 (Springer US).PubMedCrossRefGoogle Scholar
  108. 108.
    Cohen MH, Shen YL, Keegan P, Pazdur R. FDA drug approval summary: bevacizumab (Avastin) as treatment of recurrent glioblastoma multiforme. Oncologist. 2009;14:1131–8 (AlphaMed Press).PubMedCrossRefGoogle Scholar
  109. 109.
    Zhu P, Du XL, Lu G, Zhu J-J. Survival benefit of glioblastoma patients after FDA approval of temozolomide concomitant with radiation and bevacizumab: a population-based study. Oncotarget Impact J. 2017;8:44015–31.Google Scholar
  110. 110.
    Taal W, Oosterkamp HM, Walenkamp AME, Dubbink HJ, Beerepoot LV, Hanse MCJ, et al. Single-agent bevacizumab or lomustine versus a combination of bevacizumab plus lomustine in patients with recurrent glioblastoma (BELOB trial): a randomised controlled phase 2 trial. Lancet Oncol. 2014;15:943–53.PubMedCrossRefGoogle Scholar
  111. 111.
    Brandes AA, Finocchiaro G, Zagonel V, Reni M, Caserta C, Fabi A, et al. AVAREG: a phase II, randomized, noncomparative study of fotemustine or bevacizumab for patients with recurrent glioblastoma. Neuro-oncology. 2016;18:1304–12.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Weller M, Tabatabai G, Kästner B, Felsberg J, Steinbach JP, Wick A, et al. MGMT promoter methylation is a strong prognostic biomarker for benefit from dose-intensified temozolomide rechallenge in progressive glioblastoma: the DIRECTOR trial. Clin Cancer Res. 2015;21:2057–64.PubMedCrossRefGoogle Scholar
  113. 113.
    Elsamadicy AA, Chongsathidkiet P, Desai R, Woroniecka K, Farber SH, Fecci PE, et al. Prospect of rindopepimut in the treatment of glioblastoma. Expert Opin Biol Ther. 2017;17:507–13.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Chistiakov DA, Chekhonin IV, Chekhonin VP. The EGFR variant III mutant as a target for immunotherapy of glioblastoma multiforme. Eur J Pharmacol. 2017;810:70–82.PubMedCrossRefGoogle Scholar
  115. 115.
    Neagu MR, Reardon DA. An update on the role of immunotherapy and vaccine strategies for primary brain tumors. Curr Treat Options Oncol. 2015;16:54.PubMedCrossRefGoogle Scholar
  116. 116.
    Robin AM, Lee I, Kalkanis SN. Reoperation for recurrent glioblastoma multiforme. Neurosurg Clin N Am. 2017;28:407–28.PubMedCrossRefGoogle Scholar
  117. 117.
    Suchorska B, Weller M, Tabatabai G, Senft C, Hau P, Sabel MC, et al. Complete resection of contrast-enhancing tumor volume is associated with improved survival in recurrent glioblastoma-results from the DIRECTOR trial. Neuro-oncology. 2016;18:549–56.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Chang SM, Parney IF, McDermott M, Barker FG, Schmidt MH, Huang W, et al. Perioperative complications and neurological outcomes of first and second craniotomies among patients enrolled in the Glioma Outcome Project. J Neurosurg. 2003;98:1175–81.PubMedCrossRefGoogle Scholar
  119. 119.
    Mayer R, Sminia P. Reirradiation tolerance of the human brain. Int J Radiat Oncol Biol Phys. 2008;70:1350–60.PubMedCrossRefGoogle Scholar
  120. 120.
    Dong Y, Fu C, Guan H, Zhang T, Zhang Z, Zhou T, et al. Re-irradiation alternatives for recurrent high-grade glioma. Oncol Lett. 2016;12:2261–70.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Cho KH, Hall WA, Gerbi BJ, Higgins PD, McGuire WA, Clark HB. Single dose versus fractionated stereotactic radiotherapy for recurrent high-grade gliomas. Int J Radiat Oncol Biol Phys. 1999;45:1133–41.PubMedCrossRefGoogle Scholar
  122. 122.
    Flieger M, Ganswindt U, Schwarz SB, Kreth F-W, Tonn J-C, la Fougère C, et al. Re-irradiation and bevacizumab in recurrent high-grade glioma: an effective treatment option. J Neurooncol. 2014;117:337–45 (Springer US).PubMedCrossRefGoogle Scholar
  123. 123.
    Hundsberger T, Brügge D, Putora PM, Weder P, Weber J, Plasswilm L. Re-irradiation with and without bevacizumab as salvage therapy for recurrent or progressive high-grade gliomas. J Neurooncol. 2013;112:133–9 (Springer US).PubMedCrossRefGoogle Scholar
  124. 124.
    Maier-Hauff K, Ulrich F, Nestler D, Niehoff H, Wust P, Thiesen B, et al. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J Neurooncol. 2011;103:317–24 (Springer US).PubMedCrossRefGoogle Scholar
  125. 125.
    Combs SE, Bischof M, Welzel T, Hof H, Oertel S, Debus J, et al. Radiochemotherapy with temozolomide as re-irradiation using high precision fractionated stereotactic radiotherapy (FSRT) in patients with recurrent gliomas. J Neurooncol. 2008;89:205–10.PubMedCrossRefGoogle Scholar
  126. 126.
    Combs SE, Thilmann C, Edler L, Debus J, Schulz-Ertner D. Efficacy of fractionated stereotactic reirradiation in recurrent gliomas: long-term results in 172 patients treated in a single institution. J Clin Oncol. 2005;23:8863–9.PubMedCrossRefGoogle Scholar
  127. 127.
    Minniti G, Armosini V, Salvati M, Lanzetta G, Caporello P, Mei M, et al. Fractionated stereotactic reirradiation and concurrent temozolomide in patients with recurrent glioblastoma. J Neurooncol. 2011;103:683–91 (Springer US).PubMedCrossRefGoogle Scholar
  128. 128.
    Vordermark D, Kölbl O, Ruprecht K, Vince GH, Bratengeier K, Flentje M. Hypofractionated stereotactic re-irradiation: treatment option in recurrent malignant glioma. BMC Cancer. 2005;5:55 (BioMed Central).PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Fogh SE, Andrews DW, Glass J, Curran W, Glass C, Champ C, et al. Hypofractionated stereotactic radiation therapy: an effective therapy for recurrent high-grade gliomas. J Clin Oncol. 2010;28:3048–53.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Den RB, Kamrava M, Sheng Z, Werner-Wasik M, Dougherty E, Marinucchi M, et al. A phase I study of the combination of sorafenib with temozolomide and radiation therapy for the treatment of primary and recurrent high-grade gliomas. Int J Radiat Oncol Biol Phys. 2013;85:321–8.PubMedCrossRefGoogle Scholar
  131. 131.
    Archavlis E, Tselis N, Birn G, Ulrich P, Baltas D, Zamboglou N. Survival analysis of HDR brachytherapy versus reoperation versus temozolomide alone: a retrospective cohort analysis of recurrent glioblastoma multiforme. BMJ Open. 2013;3:e002262.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Barbarite E, Sick JT, Berchmans E, Bregy A, Shah AH, Elsayyad N, et al. The role of brachytherapy in the treatment of glioblastoma multiforme. Neurosurg Rev. 2017;40:195–211 (Springer Berlin Heidelberg).PubMedCrossRefGoogle Scholar
  133. 133.
    Adkison JB, Tomé W, Seo S, Richards GM, Robins HI, Rassmussen K, et al. Reirradiation of large-volume recurrent glioma with pulsed reduced-dose-rate radiotherapy. Int J Radiat Oncol Biol Phys. 2011;79:835–41.PubMedCrossRefGoogle Scholar
  134. 134.
    Pellettieri L. H-Stenstam B, Rezaei A, Giusti V, Sköld K. An investigation of boron neutron capture therapy for recurrent glioblastoma multiforme. Acta Neurol Scand. 2008;117:191–7.PubMedCrossRefGoogle Scholar
  135. 135.
    Cihoric N, Tsikkinis A, Minniti G, Lagerwaard FJ, Herrlinger U, Mathier E, et al. Current status and perspectives of interventional clinical trials for glioblastoma—analysis of ClinicalTrials.gov. Radiat Oncol. 2017;12:1 (19 ed., BioMed Central).PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Federación de Sociedades Españolas de Oncología (FESEO) 2018

Authors and Affiliations

  1. 1.Radiotherapy Unit, 1st Department of Radiology, Medical School, Aretaieion University HospitalNational and Kapodistrian University of AthensAthensGreece
  2. 2.Radiotherapy Unit, 2nd Department of Radiology, Medical School, ATTIKON University HospitalNational and Kapodistrian University of AthensChaidariGreece

Personalised recommendations