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J Neurol Surg A Cent Eur Neurosurg 2021; 82(01): 075-086
DOI: 10.1055/s-0040-1701635
Review Article

Importance and Evidence of Extent of Resection in Glioblastoma

Victoria Wykes
1   Institute of Cancer and Genomic Sciences, University of Birmingham College of Medical and Dental Sciences, Birmingham, United Kingdom of Great Britain and Northern Ireland
2   Department of Neurosurgery, University Hospitals Birmingham NHS Foundation Trust, Birmingham, United Kingdom of Great Britain and Northern Ireland
,
Athanasios Zisakis
2   Department of Neurosurgery, University Hospitals Birmingham NHS Foundation Trust, Birmingham, United Kingdom of Great Britain and Northern Ireland
,
Mihaela Irimia
2   Department of Neurosurgery, University Hospitals Birmingham NHS Foundation Trust, Birmingham, United Kingdom of Great Britain and Northern Ireland
,
Ismail Ughratdar
2   Department of Neurosurgery, University Hospitals Birmingham NHS Foundation Trust, Birmingham, United Kingdom of Great Britain and Northern Ireland
,
Vijay Sawlani
3   Department of Radiology, University Hospitals Birmingham NHS Foundation Trust, Birmingham, United Kingdom of Great Britain and Northern Ireland
,
Colin Watts
1   Institute of Cancer and Genomic Sciences, University of Birmingham College of Medical and Dental Sciences, Birmingham, United Kingdom of Great Britain and Northern Ireland
2   Department of Neurosurgery, University Hospitals Birmingham NHS Foundation Trust, Birmingham, United Kingdom of Great Britain and Northern Ireland
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Abstract

Maximal safe resection is an essential part of the multidisciplinary care of patients with glioblastoma. A growing body of data shows that gross total resection is an independent prognostic factor associated with improved clinical outcome. The relationship between extent of glioblastoma (GB) resection and clinical benefit depends critically on the balance between cytoreduction and avoiding neurologic morbidity. The definition of the extent of tumor resection, how this is best measured pre- and postoperatively, and its relation to volume of residual tumor is still discussed. We review the literature supporting extent of resection in GB, highlighting the importance of a standardized definition and measurement of extent of resection to allow greater collaboration in research projects and trials. Recent developments in neurosurgical techniques and technologies focused on maximizing extent of resection and safety are discussed.

Keywords

glioblastoma - extent of resection - survival - gross total resection - supramaximal resection


Publication History

Received: 30 June 2019

Accepted: 22 October 2019

Article published online:
13 October 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Ostrom QT, Gittleman H, Fulop J. et al. CBTRUS Statistical Report: primary brain and central nervous system tumours diagnosed in the United States in 2008–2012. Neuro Oncol 2015; 17 (Suppl. 04) iv1-iv62
    CrossrefPubMedGoogle Scholar
  • 2 Cancer Research UK. Brain, other CNS and intracranial tumours statistics. Available at: https://www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/brain-other-cns-and-intracranial-tumours
    PubMedGoogle Scholar
  • 3 Louis DN, Ohgaki H, Wiestler OD. et al. WHO Classification of Tumours of the Central Nervous System. Rev. 4th ed. Lyon, France: International Agency for Research on Cancer; 2016: 10-122
    Google Scholar
  • 4 Stupp R, Mason WP, van den Bent MJ. et al; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352 (10) 987-996
    CrossrefPubMedGoogle Scholar
  • 5 Hegi ME, Diserens AC, Gorlia T. et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005; 352 (10) 997-1003
    CrossrefPubMedGoogle Scholar
  • 6 Rouse C, Gittleman H, Ostrom QT, Kruchko C, Barnholtz-Sloan JS. Years of potential life lost for brain and CNS tumors relative to other cancers in adults in the United States, 2010. Neuro Oncol 2016; 18 (01) 70-77
    CrossrefPubMedGoogle Scholar
  • 7 Rachet B, Mitry E, Quinn MJ, Cooper N, Coleman MP. Survival from brain tumours in England and Wales up to 2001. Br J Cancer 2008; 99 (Suppl. 01) S98-S101
    CrossrefPubMedGoogle Scholar
  • 8 Yamahara T, Numa Y, Oishi T. et al. Morphological and flow cytometric analysis of cell infiltration in glioblastoma: a comparison of autopsy brain and neuroimaging. Brain Tumor Pathol 2010; 27 (02) 81-87
    CrossrefPubMedGoogle Scholar
  • 9 Nagashima G, Suzuki R, Hokaku H. et al. Graphic analysis of microscopic tumor cell infiltration, proliferative potential, and vascular endothelial growth factor expression in an autopsy brain with glioblastoma. Surg Neurol 1999; 51 (03) 292-299
    CrossrefPubMedGoogle Scholar
  • 10 Maxwell HP. The incidence of interhemispheric extension of glioblastoma multiforme through the corpus callosum. J Neurosurg 1946; 3: 54-57
    CrossrefPubMedGoogle Scholar
  • 11 Brown TJ, Brennan MC, Li M. et al. Association of the extent of resection with survival in glioblastoma: a systematic review and meta-analysis. JAMA Oncol 2016; 2 (11) 1460-1469
    CrossrefPubMedGoogle Scholar
  • 12 Nitta T, Sato K. Prognostic implications of the extent of surgical resection in patients with intracranial malignant gliomas. Cancer 1995; 75 (11) 2727-2731
    CrossrefPubMedGoogle Scholar
  • 13 McGirt MJ, Chaichana KL, Gathinji M. et al. Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg 2009; 110 (01) 156-162
    CrossrefPubMedGoogle Scholar
  • 14 Kuhnt D, Becker A, Ganslandt O, Bauer M, Buchfelder M, Nimsky C. Correlation of the extent of tumor volume resection and patient survival in surgery of glioblastoma multiforme with high-field intraoperative MRI guidance. Neuro Oncol 2011; 13 (12) 1339-1348
    CrossrefPubMedGoogle Scholar
  • 15 Grabowski MM, Recinos PF, Nowacki AS. et al. Residual tumor volume versus extent of resection: predictors of survival after surgery for glioblastoma. J Neurosurg 2014; 121 (05) 1115-1123
    CrossrefPubMedGoogle Scholar
  • 16 Wen PY, Macdonald DR, Reardon DA. et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 2010; 28 (11) 1963-1972
    CrossrefPubMedGoogle Scholar
  • 17 Wen PY, Cloughesy TF, Ellingson BM. et al. Report of the Jumpstarting Brain Tumor Drug Development Coalition and FDA clinical trials neuroimaging endpoint workshop (January 30, 2014, Bethesda MD). Neuro Oncol 2014; 16 (Suppl. 07) vii36-vii47
    CrossrefPubMedGoogle Scholar
  • 18 Ellingson BM, Bendszus M, Boxerman J. et al; Jumpstarting Brain Tumor Drug Development Coalition Imaging Standardization Steering Committee. Consensus recommendations for a standardized Brain Tumor Imaging Protocol in clinical trials. Neuro Oncol 2015; 17 (09) 1188-1198
    CrossrefPubMedGoogle Scholar
  • 19 Sorensen AG, Patel S, Harmath C. et al. Comparison of diameter and perimeter methods for tumor volume calculation. J Clin Oncol 2001; 19 (02) 551-557
    CrossrefPubMedGoogle Scholar
  • 20 Marten K, Auer F, Schmidt S, Kohl G, Rummeny EJ, Engelke C. Inadequacy of manual measurements compared to automated CT volumetry in assessment of treatment response of pulmonary metastases using RECIST criteria. Eur Radiol 2006; 16 (04) 781-790
    CrossrefPubMedGoogle Scholar
  • 21 Kanaly CW, Mehta AI, Ding D. et al. A novel, reproducible, and objective method for volumetric magnetic resonance imaging assessment of enhancing glioblastoma. J Neurosurg 2014; 121 (03) 536-542
    CrossrefPubMedGoogle Scholar
  • 22 Reuter M, Gerstner ER, Rapalino O, Batchelor TT, Rosen B, Fischl B. Impact of MRI head placement on glioma response assessment. J Neurooncol 2014; 118 (01) 123-129
    CrossrefPubMedGoogle Scholar
  • 23 Weltens C, Menten J, Feron M. et al. Interobserver variations in gross tumor volume delineation of brain tumors on computed tomography and impact of magnetic resonance imaging. Radiother Oncol 2001; 60 (01) 49-59
    CrossrefPubMedGoogle Scholar
  • 24 Egger J, Kapur T, Fedorov A. et al. GBM volumetry using the 3D Slicer medical image computing platform. Sci Rep 2013; 3: 1364
    CrossrefPubMedGoogle Scholar
  • 25 Menze BH, Jakab A, Bauer S. et al. The multimodal brain tumor image segmentation benchmark (BRATS). IEEE Trans Med Imaging 2015; 34 (10) 1993-2024
    CrossrefPubMedGoogle Scholar
  • 26 Zhang X, Yan LF, Hu YC. et al. Optimizing a machine learning based glioma grading system using multi-parametric MRI histogram and texture features. Oncotarget 2017; 8 (29) 47816-47830
    CrossrefPubMedGoogle Scholar
  • 27 Naceur MB, Saouli R, Akil M, Kachouri R. Fully automatic brain tumor segmentation using end-to-end incremental deep neural networks in MRI images. Comput Methods Programs Biomed 2018; 166: 39-49
    CrossrefPubMedGoogle Scholar
  • 28 Mohan G, Subashini MM. MRI based medical image analysis: survey on brain tumor grade classification. Biomed Signal Processing 2018; 39: 139-161
    CrossrefPubMedGoogle Scholar
  • 29 Bakas S, Reyes M, Jakab A. et al. Identifying the best machine learning algorithms for brain tumor segmentation, progression assessment, and overall survival prediction in the BRATS challenge 2018. Available at: https://arxiv.org/abs/1811.02629
    PubMedGoogle Scholar
  • 30 Shin HC, Roth HR, Gao M. et al. Deep convolutional neural networks for computer-aided detection: CNN architectures, dataset characteristics and transfer learning. IEEE Trans Med Imaging 2016; 35 (05) 1285-1298
    CrossrefPubMedGoogle Scholar
  • 31 Vallatos A, Al-Mubarak HF, Birch JL. et al. Quantitative histopathologic assessment of perfusion MRI as a marker of glioblastoma cell infiltration in and beyond the peritumoral edema region. J Magn Reson Imaging 2019; 50: 529-540
    CrossrefPubMedGoogle Scholar
  • 32 Zeng Q, Ling C, Shi F, Dong F, Jiang B, Zhang J. Glioma infiltration sign on high b-value diffusion-weighted imaging in gliomas and its prognostic value. J Magn Reson Imaging 2018; 48: 643-651
    CrossrefPubMedGoogle Scholar
  • 33 Langen KJ, Galldiks N, Hattingen E, Shah NJ. Advances in neuro-oncology imaging. Nat Rev Neurol 2017; 13 (05) 279-289
    CrossrefPubMedGoogle Scholar
  • 34 Grabner G, Kiesel B, Wöhrer A. et al. Local image variance of 7 Tesla SWI is a new technique for preoperative characterization of diffusely infiltrating gliomas: correlation with tumour grade and IDH1 mutational status. Eur Radiol 2017; 27 (04) 1556-1567
    CrossrefPubMedGoogle Scholar
  • 35 Horská A, Barker PB. Imaging of brain tumors: MR spectroscopy and metabolic imaging. Neuroimaging Clin N Am 2010; 20 (03) 293-310
    CrossrefPubMedGoogle Scholar
  • 36 Hangel G, Jain S, Springer E. et al. High-resolution metabolic mapping of gliomas via patch-based super-resolution magnetic resonance spectroscopic imaging at 7T. Neuroimage 2019; 191: 587-595
    CrossrefPubMedGoogle Scholar
  • 37 Mauer M, Stupp R, Taphoorn MJ. et al. The prognostic value of health-related quality-of-life data in predicting survival in glioblastoma cancer patients: results from an international randomised phase III EORTC Brain Tumour and Radiation Oncology Groups, and NCIC Clinical Trials Group study. Br J Cancer 2007; 97 (03) 302-307
    CrossrefPubMedGoogle Scholar
  • 38 Gulati S, Jakola AS, Nerland US, Weber C, Solheim O. The risk of getting worse: surgically acquired deficits, perioperative complications, and functional outcomes after primary resection of glioblastoma. World Neurosurg 2011; 76 (06) 572-579
    CrossrefPubMedGoogle Scholar
  • 39 Rahman M, Abbatematteo J, De Leo EK. et al. The effects of new or worsened postoperative neurological deficits on survival of patients with glioblastoma. J Neurosurg 2017; 127 (01) 123-131
    CrossrefPubMedGoogle Scholar
  • 40 Ma R, Chari A, Brennan PM. et al; British Neurosurgical Trainee Research Collaborative. Residual enhancing disease after surgery for glioblastoma: evaluation of practice in the United Kingdom. Neurooncol Pract 2018; 5 (02) 74-81
    PubMedGoogle Scholar
  • 41 Stupp R, Brada M, van den Bent MJ, Tonn JC, Pentheroudakis G. ESMO Guidelines Working Group. High-grade glioma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2014; 25 (Suppl. 03) iii93-iii101
    CrossrefPubMedGoogle Scholar
  • 42 Weller M, van den Bent M, Hopkins K. et al; European Association for Neuro-Oncology (EANO) Task Force on Malignant Glioma. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol 2014; 15 (09) e395-e403
    CrossrefPubMedGoogle Scholar
  • 43 Lacroix M, Abi-Said D, Fourney DR. et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 2001; 95 (02) 190-198
    CrossrefPubMedGoogle Scholar
  • 44 Orringer D, Lau D, Khatri S. et al. Extent of resection in patients with glioblastoma: limiting factors, perception of resectability, and effect on survival. J Neurosurg 2012; 117 (05) 851-859
    CrossrefPubMedGoogle Scholar
  • 45 Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS. An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 2011; 115 (01) 3-8
    CrossrefPubMedGoogle Scholar
  • 46 Chaichana KL, Cabrera-Aldana EE, Jusue-Torres I. et al. When gross total resection of a glioblastoma is possible, how much resection should be achieved?. World Neurosurg 2014; 82 (1-2): e257-e265
    CrossrefPubMedGoogle Scholar
  • 47 Chaichana KL, Jusue-Torres I, Navarro-Ramirez R. et al. Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro Oncol 2014; 16 (01) 113-122
    CrossrefPubMedGoogle Scholar
  • 48 Coburger J, Segovia J, Ganslandt O, Ringel F, Wirtz CR, Renovanz M. Counseling patients with a glioblastoma amenable only for subtotal resection: results of a multicenter retrospective assessment of survival and neurologic outcome. World Neurosurg 2018; 114: e1180-e1185
    CrossrefPubMedGoogle Scholar
  • 49 Awad AW, Karsy M, Sanai N. et al. Impact of removed tumor volume and location on patient outcome in glioblastoma. J Neurooncol 2017; 135 (01) 161-171
    CrossrefPubMedGoogle Scholar
  • 50 Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ. ALA-Glioma Study Group. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 2006; 7 (05) 392-401
    CrossrefPubMedGoogle Scholar
  • 51 Stummer W, Tonn JC, Mehdorn HM. et al; ALA-Glioma Study Group. Counterbalancing risks and gains from extended resections in malignant glioma surgery: a supplemental analysis from the randomized 5-aminolevulinic acid glioma resection study. Clinical article. J Neurosurg 2011; 114 (03) 613-623
    CrossrefPubMedGoogle Scholar
  • 52 Pichlmeier U, Bink A, Schackert G, Stummer W. ALA Glioma Study Group. Resection and survival in glioblastoma multiforme: an RTOG recursive partitioning analysis of ALA study patients. Neuro Oncol 2008; 10 (06) 1025-1034
    CrossrefPubMedGoogle Scholar
  • 53 Stummer W, Meinel T, Ewelt C. et al. Prospective cohort study of radiotherapy with concomitant and adjuvant temozolomide chemotherapy for glioblastoma patients with no or minimal residual enhancing tumor load after surgery. J Neurooncol 2012; 108 (01) 89-97
    CrossrefPubMedGoogle Scholar
  • 54 Senft C, Bink A, Franz K, Vatter H, Gasser T, Seifert V. Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 2011; 12 (11) 997-1003
    CrossrefPubMedGoogle Scholar
  • 55 Kim YJ, Lee DJ, Park CK, Kim IA. Optimal extent of resection for glioblastoma according to site, extension, and size: a population-based study in the temozolomide era. Neurosurg Rev 2019; 42: 937-950
    CrossrefPubMedGoogle Scholar
  • 56 Duffau H. Long-term outcomes after supratotal resection of diffuse low-grade gliomas: a consecutive series with 11-year follow-up. Acta Neurochir (Wien) 2016; 158 (01) 51-58
    CrossrefPubMedGoogle Scholar
  • 57 Duffau H. Is supratotal resection of glioblastoma in noneloquent areas possible?. World Neurosurg 2014; 82 (1–2): e101-e103
    CrossrefPubMedGoogle Scholar
  • 58 Li YM, Suki D, Hess K, Sawaya R. The influence of maximum safe resection of glioblastoma on survival in 1229 patients: can we do better than gross-total resection?. J Neurosurg 2016; 124 (04) 977-988
    CrossrefPubMedGoogle Scholar
  • 59 Pessina F, Navarria P, Cozzi L. et al. Maximize surgical resection beyond contrast-enhancing boundaries in newly diagnosed glioblastoma multiforme: is it useful and safe? A single institution retrospective experience. J Neurooncol 2017; 135 (01) 129-139
    CrossrefPubMedGoogle Scholar
  • 60 Glenn CA, Baker CM, Conner AK. et al. An examination of the role of supramaximal resection of temporal lobe glioblastoma multiforme. World Neurosurg 2018; 114: e747-e755
    CrossrefPubMedGoogle Scholar
  • 61 Yan JL, van der Hoorn A, Larkin TJ, Boonzaier NR, Matys T, Price SJ. Extent of resection of peritumoral diffusion tensor imaging-detected abnormality as a predictor of survival in adult glioblastoma patients. J Neurosurg 2017; 126 (01) 234-241
    CrossrefPubMedGoogle Scholar
  • 62 Al-Holou WN, Hodges TR, Everson RG. et al. Perilesional resection of glioblastoma is independently associated with improved outcomes. Neurosurgery 2019; February 25 (Epub ahead of print)
    PubMedGoogle Scholar
  • 63 Roh TH, Kang SG, Moon JH. et al. Survival benefit of lobectomy over gross-total resection without lobectomy in cases of glioblastoma in the non-eloquent area: a retrospective study. J Neurosurg 2019; March 1 (Epub ahead of print)
    PubMedGoogle Scholar
  • 64 Schucht P, Murek M, Jilch A. et al. Early re-do surgery for glioblastoma is a feasible and safe strategy to achieve complete resection of enhancing tumor. PLOS One 2013; 8 (11) e79846
    CrossrefPubMedGoogle Scholar
  • 65 Bloch O, Han SJ, Cha S. et al. Impact of extent of resection for recurrent glioblastoma on overall survival: clinical article. J Neurosurg 2012; 117 (06) 1032-1038
    CrossrefPubMedGoogle Scholar
  • 66 Chaichana KL, Zadnik P, Weingart JD. et al. Multiple resections for patients with glioblastoma: prolonging survival. J Neurosurg 2013; 118 (04) 812-820
    CrossrefPubMedGoogle Scholar
  • 67 Suchorska B, Weller M, Tabatabai G. et al. Complete resection of contrast-enhancing tumor volume is associated with improved survival in recurrent glioblastoma-results from the DIRECTOR trial. Neuro Oncol 2016; 18 (04) 549-556
    CrossrefPubMedGoogle Scholar
  • 68 Ringel F, Pape H, Sabel M. et al; SN1 study group. Clinical benefit from resection of recurrent glioblastomas: results of a multicenter study including 503 patients with recurrent glioblastomas undergoing surgical resection. Neuro Oncol 2016; 18 (01) 96-104
    CrossrefPubMedGoogle Scholar
  • 69 Pessina F, Navarria P, Cozzi L. et al. Role of surgical resection in recurrent glioblastoma: prognostic factors and outcome evaluation in an observational study. J Neurooncol 2017; 131 (02) 377-384
    CrossrefPubMedGoogle Scholar
  • 70 Oppenlander ME, Wolf AB, Snyder LA. et al. An extent of resection threshold for recurrent glioblastoma and its risk for neurological morbidity. J Neurosurg 2014; 120 (04) 846-853
    CrossrefPubMedGoogle Scholar
  • 71 Yong RL, Wu T, Mihatov N. et al. Residual tumor volume and patient survival following reoperation for recurrent glioblastoma. J Neurosurg 2014; 121 (04) 802-809
    CrossrefPubMedGoogle Scholar
  • 72 Eckel-Passow JE, Lachance DH, Molinaro AM. et al. Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 2015; 372 (26) 2499-2508
    CrossrefPubMedGoogle Scholar
  • 73 Weller M, Weber RG, Willscher E. et al. 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 2015; 129 (05) 679-693
    CrossrefPubMedGoogle Scholar
  • 74 Brat DJ, Verhaak RG, Aldape KD. et al; Cancer Genome Atlas Research Network. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 2015; 372 (26) 2481-2498
    CrossrefPubMedGoogle Scholar
  • 75 Wijnenga MMJ, Dubbink HJ, French PJ. et al. Molecular and clinical heterogeneity of adult diffuse low-grade IDH wild-type gliomas: assessment of TERT promoter mutation and chromosome 7 and 10 copy number status allows superior prognostic stratification. Acta Neuropathol 2017; 134 (06) 957-959
    CrossrefPubMedGoogle Scholar
  • 76 Wijnenga MMJ, French PJ, Dubbink HJ. et al. Prognostic relevance of mutations and copy number alterations assessed with targeted next generation sequencing in IDH mutant grade II glioma. J Neurooncol 2018; 139 (02) 349-357
    CrossrefPubMedGoogle Scholar
  • 77 Shankar GM, Francis JM, Rinne ML. et al. Rapid intraoperative molecular characterization of glioma. JAMA Oncol 2015; 1 (05) 662-667
    CrossrefPubMedGoogle Scholar
  • 78 Hollon T, Stummer W, Orringer D, Suero Molina E. Surgical adjuncts to increase the extent of resection: intraoperative MRI, fluorescence, and Raman histology. Neurosurg Clin N Am 2019; 30 (01) 65-74
    CrossrefPubMedGoogle Scholar
  • 79 Laperriere N, Weller M, Stupp R. et al. Optimal management of elderly patients with glioblastoma. Cancer Treat Rev 2013; 39 (04) 350-357
    CrossrefPubMedGoogle Scholar
  • 80 Perry JR, Laperriere N, O'Callaghan CJ. et al; Trial Investigators. Short-course radiation plus temozolomide in elderly patients with glioblastoma. N Engl J Med 2017; 376 (11) 1027-1037
    CrossrefPubMedGoogle Scholar
  • 81 Barnholtz-Sloan JS, Williams VL, Maldonado JL. et al. Patterns of care and outcomes among elderly individuals with primary malignant astrocytoma. J Neurosurg 2008; 108 (04) 642-648
    CrossrefPubMedGoogle Scholar
  • 82 Iwamoto FM, Reiner AS, Panageas KS, Elkin EB, Abrey LE. Patterns of care in elderly glioblastoma patients. Ann Neurol 2008; 64 (06) 628-634
    CrossrefPubMedGoogle Scholar
  • 83 Pessina F, Navarria P, Cozzi L. et al. Is surgical resection useful in elderly newly diagnosed glioblastoma patients? Outcome evaluation and prognostic factors assessment. Acta Neurochir (Wien) 2018; 160 (09) 1779-1787
    CrossrefPubMedGoogle Scholar
  • 84 Babu R, Komisarow JM, Agarwal VJ. et al. Glioblastoma in the elderly: the effect of aggressive and modern therapies on survival. J Neurosurg 2016; 124 (04) 998-1007
    CrossrefPubMedGoogle Scholar
  • 85 Hoffermann M, Bruckmann L, Kariem Mahdy A, Asslaber M, Payer F, von Campe G. Treatment results and outcome in elderly patients with glioblastoma multiforme—a retrospective single institution analysis. Clin Neurol Neurosurg 2015; 128: 60-69
    CrossrefPubMedGoogle Scholar
  • 86 Vuorinen V, Hinkka S, Färkkilä M, Jääskeläinen J. Debulking or biopsy of malignant glioma in elderly people—a randomised study. Acta Neurochir (Wien) 2003; 145 (01) 5-10
    CrossrefPubMedGoogle Scholar
  • 87 Stark AM, Hedderich J, Held-Feindt J, Mehdorn HM. Glioblastoma—the consequences of advanced patient age on treatment and survival. Neurosurg Rev 2007; 30 (01) 56-61 ; discussion 61–62
    CrossrefPubMedGoogle Scholar
  • 88 Ewelt C, Goeppert M, Rapp M, Steiger HJ, Stummer W, Sabel M. Glioblastoma multiforme of the elderly: the prognostic effect of resection on survival. J Neurooncol 2011; 103 (03) 611-618
    CrossrefPubMedGoogle Scholar
  • 89 Chaichana KL, Garzon-Muvdi T, Parker S. et al. Supratentorial glioblastoma multiforme: the role of surgical resection versus biopsy among older patients. Ann Surg Oncol 2011; 18 (01) 239-245
    CrossrefPubMedGoogle Scholar
  • 90 Jordan JT, Gerstner ER, Batchelor TT, Cahill DP, Plotkin SR. Glioblastoma care in the elderly. Cancer 2016; 122 (02) 189-197
    CrossrefPubMedGoogle Scholar
  • 91 Zanello M, Roux A, Ursu R. et al; Club de Neuro-Oncologie of the Société Française de Neurochirurgie. Recurrent glioblastomas in the elderly after maximal first-line treatment: does preserved overall condition warrant a maximal second-line treatment?. J Neurooncol 2017; 135 (02) 285-297
    CrossrefPubMedGoogle Scholar
  • 92 Díez Valle R, Hadjipanayis CG, Stummer W. Established and emerging uses of 5-ALA in the brain: an overview. J Neurooncol 2019; 141 (03) 487-494
    CrossrefPubMedGoogle Scholar
  • 93 Coburger J, Wirtz CR. Fluorescence guided surgery by 5-ALA and intraoperative MRI in high grade glioma: a systematic review. J Neurooncol 2019; 141 (03) 533-546
    CrossrefPubMedGoogle Scholar
  • 94 Chohan MO, Berger MS. 5-Aminolevulinic acid fluorescence guided surgery for recurrent high-grade gliomas. J Neurooncol 2019; 141 (03) 517-522
    CrossrefPubMedGoogle Scholar
  • 95 Xie Y, Thom M, Ebner M. et al. Wide-field spectrally resolved quantitative fluorescence imaging system: toward neurosurgical guidance in glioma resection. J Biomed Opt 2017; 22 (11) 1-14
    CrossrefPubMedGoogle Scholar
  • 96 Szelényi A, Bello L, Duffau H. et al; Workgroup for Intraoperative Management in Low-Grade Glioma Surgery within the European Low-Grade Glioma Network. Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 2010; 28 (02) E7
    CrossrefPubMedGoogle Scholar
  • 97 Sanai N, Berger MS. Surgical oncology for gliomas: the state of the art. Nat Rev Clin Oncol 2018; 15 (02) 112-125
    CrossrefPubMedGoogle Scholar
  • 98 Spena G, Nava A, Cassini F. et al. Preoperative and intraoperative brain mapping for the resection of eloquent-area tumors. A prospective analysis of methodology, correlation, and usefulness based on clinical outcomes. Acta Neurochir (Wien) 2010; 152 (11) 1835-1846
    CrossrefPubMedGoogle Scholar
  • 99 Pujol S, Wells W, Pierpaoli C. et al. The DTI challenge: toward standardized evaluation of diffusion tensor imaging tractography for neurosurgery. J Neuroimaging 2015; 25 (06) 875-882
    CrossrefPubMedGoogle Scholar
  • 100 De Witte E, Satoer D, Robert E. et al. The Dutch Linguistic Intraoperative Protocol: a valid linguistic approach to awake brain surgery. Brain Lang 2015; 140: 35-48
    CrossrefPubMedGoogle Scholar
  • 101 Raabe A, Beck J, Schucht P, Seidel K. Continuous dynamic mapping of the corticospinal tract during surgery of motor eloquent brain tumors: evaluation of a new method. J Neurosurg 2014; 120 (05) 1015-1024
    CrossrefPubMedGoogle Scholar
  • 102 De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS. Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 2012; 30 (20) 2559-2565
    CrossrefPubMedGoogle Scholar
  • 103 Schucht P, Beck J, Abu-Isa J. et al. Gross total resection rates in contemporary glioblastoma surgery: results of an institutional protocol combining 5-aminolevulinic acid intraoperative fluorescence imaging and brain mapping. Neurosurgery 2012; 71 (05) 927-935 ; discussion 935–936
    CrossrefPubMedGoogle Scholar
  • 104 Schucht P, Seidel K, Beck J. et al. Intraoperative monopolar mapping during 5-ALA-guided resections of glioblastomas adjacent to motor eloquent areas: evaluation of resection rates and neurological outcome. Neurosurg Focus 2014; 37 (06) E16
    CrossrefPubMedGoogle Scholar
  • 105 Bello L, Gambini A, Castellano A. et al. Motor and language DTI fiber tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 2008; 39 (01) 369-382
    CrossrefPubMedGoogle Scholar
  • 106 Schneider JP, Trantakis C, Rubach M. et al. Intraoperative MRI to guide the resection of primary supratentorial glioblastoma multiforme—a quantitative radiological analysis. Neuroradiology 2005; 47 (07) 489-500
    CrossrefPubMedGoogle Scholar
  • 107 Senft C, Franz K, Blasel S. et al. Influence of iMRI-guidance on the extent of resection and survival of patients with glioblastoma multiforme. Technol Cancer Res Treat 2010; 9 (04) 339-346
    CrossrefPubMedGoogle Scholar
  • 108 Leroy HA, Delmaire C, Le Rhun E. et al. High-field intraoperative MRI and glioma surgery: results after the first 100 consecutive patients. Acta Neurochir (Wein) 2019; 161: 1467-1474
    CrossrefPubMedGoogle Scholar
  • 109 Solheim O, Selbekk T, Jakola AS, Unsgård G. Ultrasound-guided operations in unselected high-grade gliomas—overall results, impact of image quality and patient selection. Acta Neurochir (Wien) 2010; 152 (11) 1873-1886
    CrossrefPubMedGoogle Scholar
  • 110 Moiyadi AV, Shetty P. Direct navigated 3D ultrasound for resection of brain tumors: a useful tool for intraoperative image guidance. Neurosurg Focus 2016; 40 (03) E5
    CrossrefPubMedGoogle Scholar
  • 111 Jenkinson MD, Barone DG, Bryant A. et al. Intraoperative imaging technology to maximise extent of resection for glioma. Cochrane Database Syst Rev 2018; 1: CD012788
    PubMedGoogle Scholar
  • 112 Berntsen EM, Gulati S, Solheim O. et al. Functional magnetic resonance imaging and diffusion tensor tractography incorporated into an intraoperative 3-dimensional ultrasound-based neuronavigation system: impact on therapeutic strategies, extent of resection, and clinical outcome. Neurosurgery 2010; 67 (02) 251-264
    CrossrefPubMedGoogle Scholar
  • 113 Picht T, Frey D, Thieme S, Kliesch S, Vajkoczy P. Presurgical navigated TMS motor cortex mapping improves outcome in glioblastoma surgery: a controlled observational study. J Neurooncol 2016; 126 (03) 535-543
    CrossrefPubMedGoogle Scholar
  • 114 Raffa G, Scibilia A, Conti A. et al. The role of navigated transcranial magnetic stimulation for surgery of motor-eloquent brain tumors: a systematic review and meta-analysis. Clin Neurol Neurosurg 2019; 180: 7-17
    CrossrefPubMedGoogle Scholar
  • 115 Stummer W, Reulen HJ, Meinel T. et al. Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 2008; 62: 564-576
    CrossrefPubMedGoogle Scholar