Summary
Refinement of neurosurgical technique has enabled safer operations with more aggressive outcomes. One cornerstone of modern-day practice is the utilization of intraoperative stimulation mapping. In addition to identifying critical motor pathways, this technique can be adapted to reliably identify language pathways. Given the individual variability of cortical language localization, such awake language mapping is essential to minimize language deficits following tumor resection. Our experience suggests that cortical language mapping is a safe and efficient adjunct to optimize tumor resection while preserving essential language sites, even in the setting of negative mapping data. However, the value of maximizing glioma resections remains surprisingly unclear, as there is no general consensus in the literature regarding the efficacy of extent of glioma resection in improving patient outcome. While the importance of resection in obtaining tissue diagnosis and alleviating symptoms is clear, a lack of Class I evidence prevents similar certainty in assessing the influence of extent of resection. Beyond an analysis of modern intraoperative mapping techniques, we examine every major clinical publication since 1990 on the role of extent of resection in glioma outcome. The mounting evidence suggests that, despite persistent limitations in the quality of available studies, a more extensive surgical resection is associated with longer life expectancy for both low-grade and high-grade gliomas.
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Foerster O. The cerebral cortex of man. Lancet 1931;2: 309–312.
Penfield W, Bolchey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937;60: 389–443.
Penfield W, Erickson TC. Epilepsy and cerebral localization. A study of the mechanism, treatment, and prevention of epileptic seizures. 1941.
Penfield W, Rasmussen T. Secondary sensory and motor representation. 1950.
Ranck JB, Jr. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 1975;98: 417–440.
Haglund MM, Ojemann GA, Blasdel GG. Optical imaging of bipolar cortical stimulation. J Neurosurg 1993;78: 785–793.
Haglund MM, Ojemann GA, Hochman DW. Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature 1992;358: 668–671.
Herholz K, Thiel A, Wienhard K, et al. Individual functional anatomy of verb generation. Neuroimage 1996;3: 185–194.
Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 1989;71: 316–326.
Ojemann GA, Whitaker HA. Language localization and variability. Brain Lang 1978;6: 239–260.
Ojemann GA. Individual variability in cortical localization of language. J Neurosurg 1979;50: 164–169.
Ojemann JG, Miller JW, Silbergeld DL. Reserved function in brain invaded by tumor. Neurosurgery 1996;39: 253–258.
Scitz RJ, Huang Y, Knorr U, et al. Large-scale plasticity of the human motor cortex. Neuroreport 1995;6: 742–744.
Wunderlich G, Knorr U, Herzog H, et al. Precentral glioma location determines the displacement of cortical hand representation. Neurosurgery 1998;42: 18–26.
Quinones-Hinojosa A, Ojemann SG, Sanai N, Dillon WP, Berger MS. Reoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. J Neurosurg 2003;99: 311–318.
Seghier ML, Lazeyras F, Pegna AJ, et al. Variability of fMRI activation during a phonological and semantic language task in healthy subjects. Hum Brain Mapp 2004;23: 140–155.
Tzourio-Mazoyer N, Josse G, Crivello F, Mazoyer B. Interindividual variability in the hemispheric organization for speech. Neuroimage 2004;21: 422–435.
Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA. Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 2002;16: 765–780.
Tzourio N, Crivello F, Mellet E, Nkanga-Ngila B, Mazoyer B. Functional anatomy of dominance for speech comprehension in left handers vs right handers. Neuroimage 1998;8: 1–16.
Dehaene S, Dupoux E, Mehler J, et al. Anatomical variability in the cortical representation of first and second language. Neuroreport 1997;8: 3809–3815.
Steinmetz H, Scitz RJ. Functional anatomy of language processing: neuroimaging and the problem of individual variability. Neuropsychologia 1991;29: 1149–1161.
Josse G, Herve PY, Crivello F, Mazoyer B, Tzourio-Mazoyer N. Hemispheric specialization for language: Brain volume matters. Brain Res 2006;1068: 184–193.
Davies KG, Maxwell RE, Jennum P, et al. Language function following subdural grid-directed temporal lobectomy. Acta Neurol Scand 1994;90: 201–206.
FitzGerald DB, Cosgrove GR, Ronner S, et al. Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. AJNR Am J Neuroradiol 1997;18: 1529–1539.
Skirboll SS, Ojemann GA, Berger MS, Lettich E, Winn HR. Functional cortex and subcortical white matter located within gliomas. Neurosurgery 1996;38: 678–684.
Ojemann GA. Models of the brain organization for higher integrative functions derived with electrical stimulation techniques. Hum Neurobiol 1982;1: 243–249.
Ojemann GA. Cortical organization of language. J Neurosci 1991;11: 2281–2287.
Ojemann GA, Creutzfeldt OD. Nervous System V, Part 2. 1987:675–700.
Ojemann GA. Organization of language cortex derived from investigations during neurosurgery. Seminars in Neuroscience 1990;2: 297–305.
Haglund MM, Berger MS, Shamseldin M, Lettich E, Ojemann GA. Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 1994;34: 567–576.
Taylor MD, Bernstein M. Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: a prospective trial of 200 cases. J Neurosurg 1999;90: 35–41.
Hochberg FH, Pruitt A. Assumptions in the radiotherapy of glioblastoma. Neurology 1980;30: 907–911.
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: 1405–1409.
Ebeling U, Steinmetz H, Huang YX, Kahn T. Topography and identification of the inferior precentral sulcus in MR imaging. AJR Am J Roentgenol 1989;153: 1051–1056.
Herholz K, Reulen HJ, von Stockhausen HM, et al. Preoperative activation and intraoperative stimulation of language-related areas in patients with glioma. Neurosurgery 1997;41: 1253–1260.
Carpentier A, Pugh KR, Westerveld M, et al. Functional MRI of language processing: dependence on input modality and temporal lobe epilepsy. Epilepsia 2001;42: 1241–1254.
Sartorius CJ, Berger MS. Rapid termination of intraoperative stimulation-evoked seizures with application of cold Ringer’s lactate to the cortex. Technical note. J Neurosurg 1998;88: 349–351.
Duffau H, Capelle L, Denvil D, et al. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 2003;98: 764–778.
Duffau H, Capelle L, Sichez N, et al. Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 2002;125: 199–214.
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: 190–198.
Sanai N, Berger MS. Mapping the horizon: techniques to optimize tumor resection before and during surgery. Clin Neurosurg 2008;55: 14–19.
Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med 2008;358: 18–27.
Berger MS. Lesions in functional (“eloquent”) cortex and sub-cortical white matter. Clin Neurosurg 1993;41: 443–463.
Chollet F, DiPiero V, Wise RJ, et al. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol 1991;29: 63–71.
Weder B, Scitz RJ. Deficient cerebral activation pattern in stroke recovery. Neuroreport 1994;5: 457–460.
Lewine JD, Astur RS, Davis LE, et al. Cortical organization in adulthood is modified by neonatal infarct: a case study. Radiology 1994;190: 93–96.
Maldjian J, Atlas SW, Howard RS, 2nd, et al. Functional magnetic resonance imaging of regional brain activity in patients with intracerebral arteriovenous malformations before surgical or endovascular therapy. J Neurosurg 1996;84: 477–483.
Grady MS, Jane JA, Steward O. Synaptic reorganization within the human central nervous system following injury. J Neurosurg 1989;71: 534–537.
Fandino J, Kollias SS, Wieser HG, Valavanis A, Yonekawa Y. Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg 1999;91: 238–250.
Duffau H, Capelle L, Denvil D, et al. Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 2003;74: 901–907.
Thiel A, Herholz K, Koyuncu A, et al. Plasticity of language networks in patients with brain tumors: a positron emission tomography activation study. Ann Neurol 2001;50: 620–629.
Duffau H, Bauchet L, Lehericy S, Capelle L. Functional compensation of the left dominant insula for language. Neuroreport 2001;12: 2159–2163.
Black P. Management of malignant glioma: role of surgery in relation to multimodality therapy. J Neurovirol 1998;4: 227–236.
Yasargil MG, Kadri PA, Yasargil DC. Microsurgery for malignant gliomas. J Neurooncol 2004;69: 67–81.
Guthrie BL, Laws ER, Jr. Supratentorial low-grade gliomas. Neurosurg Clin N Am 1990;1: 37–48.
Keles GE, Anderson B, Berger MS. The effect of extent of resection on time to tumor progression and survival in patients with glioblastoma multiforme of the cerebral hemisphere. Surg Neurol 1999;52: 371–379.
Proescholdt MA, Macher C, Woertgen C, Brawanski A. Level of evidence in the literature concerning brain tumor resection. Clin Neurol Neurosurg 2005;107: 95–98.
Sawaya R. Extent of resection in malignant gliomas: a critical summary. J Neurooncol 1999;42: 303–305.
Grant R. Biopsy versus resection for malignant glioma (review). Cochrane Database Syst Rev 2006.
Nazzaro JM, Neuwelt EA. The role of surgery in the management of supratentorial intermediate and high-grade astrocytomas in adults. J Neurosurg 1990;73: 331–344.
Pierga JY, Hoang-Xuan K, Feuvret L, et al. Treatment of malignant gliomas in the elderly. J Neurooncol 1999;43: 187–193.
Hess KR. Extent of resection as a prognostic variable in the treatment of gliomas. J Neurooncol 1999;42: 227–231.
Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery 2008;62: 753–764.
Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352: 997–1003.
Keles GE, Chang EF, Lamborn KR, et al. Volumetric extent of resection and residual contrast enhancement on initial surgery as predictors of outcome in adult patients with hemispheric anaplastic astrocytoma. J Neurosurg 2006;105: 34–40.
Leighton C, Fisher B, Bauman G, et al. Supratentorial low-grade glioma in adults: an analysis of prognostic factors and timing of radiation. J Clin Oncol 1997;15: 1294–1301.
Nakamura M, Konishi N, Tsunoda S, et al. Analysis of prognostic and survival factors related to treatment of low-grade astrocytomas in adults. Oncology 2000;58: 108–116.
Philippon JH, Clemenceau SH, Fauchon FH, Foncin JF. Supratentorial low-grade astrocytomas in adults. Neurosurgery 1993;32: 554–559.
Rajan B, Pickuth D, Ashley S, et al. The management of histologically unverified presumed cerebral gliomas with radiotherapy. Int J Radiat Oncol Biol Phys 1994;28: 405–413.
Shaw E, Arusell R, Scheithauer B, et al. Prospective randomized trial of lowversus 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: 2267–2276.
Yeh SA, Ho JT, Lui CC, et al. Treatment outcomes and prognostic factors in patients with supratentorial low-grade gliomas. Br J Radiol 2005;78: 230–235.
Shaw EG, Daumas-Duport C, Scheithauer BW, et al. Radiation therapy in the management of low-grade supratentorial astrocytomas. J Neurosurg 1989;70: 853–861.
Laws ER, Jr., Taylor WF, Clifton MB, Okazaki H. Neurosurgical management of low-grade astrocytoma of the cerebral hemispheres. J Neurosurg 1984;61: 665–673.
North CA, North RB, Epstein JA, Piantadosi S, Wharam MD. Low-grade cerebral astrocytomas. Survival and quality of life after radiation therapy. Cancer 1990;66: 6–14.
Ito S, Chandler KL, Prados MD, et al. Proliferative potential and prognostic evaluation of low-grade astrocytomas. J Neurooncol 1994;19: 1–9.
Nicolato A, Gerosa MA, Fina P, et al. Prognostic factors in low-grade supratentorial astrocytomas: a uni-multivariate statistical analysis in 76 surgically treated adult patients. Surg Neurol 1995;44: 208–221.
Whitton AC, Bloom HJ. Low grade glioma of the cerebral hemispheres in adults: a retrospective analysis of 88 cases. Int J Radiat Oncol Biol Phys 1990;18: 783–786.
Shibamoto Y, Kitakabu Y, Takahashi M, et al. Supratentorial low-grade astrocytoma. Correlation of computed tomography findings with effect of radiation therapy and prognostic variables. Cancer 1993;72: 190–195.
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) Study 22844. Int J Radiat Oncol Biol Phys 1996;36: 549–556.
Scerrati M, Roselli R, Iacoangeli M, Pompucci A, Rossi GF. Prognostic factors in low grade (WHO grade II) gliomas of the cerebral hemispheres: the role of surgery. J Neurol Neurosurg Psychiatry 1996;61: 291–296.
Lote K, Egeland T, Hager B, et al. Survival, prognostic factors, and therapeutic efficacy in low-grade glioma: a retrospective study in 379 patients. J Clin Oncol 1997;15: 3129–3140.
Peraud A, Ansari H, Bise K, Reulen HJ. Clinical outcome of supratentorial astrocytoma WHO grade II. Acta Neurochir (Wien) 1998;140: 1213–1222.
van Veelen ML, Avezaat CJ, Kros JM, van Putten W, Vecht C. Supratentorial low grade astrocytoma: prognostic factors, dedifferentiation, and the issue of early versus late surgery. J Neurol Neurosurg Psychiatry 1998;64: 581–587.
Bauman G, Pahapill P, Macdonald D, et al. Low grade glioma: a measuring radiographic response to radiotherapy. Can J Neurol Sci 1999;26: 18–22.
Johannesen TB, Langmark F, Lote K. Progress in long-term survival in adult patients with supratentorial low-grade gliomas: a population-based study of 993 patients in whom tumors were diagnosed between 1970 and 1993. J Neurosurg 2003;99: 854–862.
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: 1227–1233.
McGirt MJ, Chaichana KL, Attenello FJ, et al. Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 2008;63: 700–707.
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: 1338–1345.
Vecht CJ, Avezaat CJ, van Putten WL, Eijkenboom WM, Stefanko SZ. The influence of the extent of surgery on the neurological function and survival in malignant glioma. A retrospective analysis in 243 patients. J Neurol Neurosurg Psychiatry 1990;53: 466–471.
Shibamoto Y, Yamashita J, Takahashi M, et al. Supratentorial malignant glioma: an analysis of radiation therapy in 178 cases. Radiother Oncol 1990;18: 9–17.
Curran WJ, Jr., Scott CB, Horton J, et al. Does extent of surgery influence outcome for astrocytoma with atypical or anaplastic foci (AAF)? A report from three Radiation Therapy Oncology Group (RTOG) trials. J Neurooncol 1992;12: 219–227.
Simpson JR, Horton J, Scott C, et al. Influence of location and extent of surgical resection on survival of patients with glioblastoma multiforme: results of three consecutive Radiation Therapy Oncology Group (RTOG) clinical trials. Int J Radiat Oncol Biol Phys 1993;26: 239–244.
Dinapoli RP, Brown LD, Arusell RM, et al. Phase III comparative evaluation of PCNU and carmustine combined with radiation therapy for high-grade glioma. J Clin Oncol 1993;11: 1316–1321.
Jeremic B, Grujicic D, Antunovic V, et al. Influence of extent of surgery and tumor location on treatment outcome of patients with glioblastoma multiforme treated with combined modality approach. J Neurooncol 1994;21: 177–185.
Nitta T, Sato K. Prognostic implications of the extent of surgical resection in patients with intracranial malignant gliomas. Cancer 1995;75: 2727–2731.
Barker FG, 2nd, Prados MD, Chang SM, et al. Radiation response and survival time in patients with glioblastoma multiforme. J Neurosurg 1996;84: 442–448.
Brown PD, Maurer MJ, Rummans TA, et al. A prospective study of quality of life in adults with newly diagnosed high-grade gliomas: the impact of the extent of resection on quality of life and survival. Neurosurgery 2005;57: 495–504.
Buckner JC, Schomberg PJ, McGinnis WL, et al. A phase III study of radiation therapy plus carmustine with or without recombinant interferon-alpha in the treatment of patients with newly diagnosed high-grade glioma. 2001;92:420–433.
Lamborn KR, Chang SM, Prados MD. Prognostic factors for survival of patients with glioblastoma: recursive partitioning analysis. Neuro-oncol 2004;6: 227–235.
Stark AM, Nabavi A, Mehdorn HM, Blomer U. Glioblastoma multiforme-report of 267 cases treated at a single institution. Surg Neurol 2005;63: 162–169.
Ushio Y, Kochi M, Hamada J, Kai Y, Nakamura H. Effect of surgical removal on survival and quality of life in patients with supratentorial glioblastoma. Neurol Med Chir (Tokyo) 2005;45: 454–460.
Duncan GG, Goodman GB, Ludgate CM, Rheaume DE. The treatment of adult supratentorial high grade astrocytomas. J Neurooncol 1992;13: 63–72.
Hollerhage HG, Zumkeller M, Becker M, Dietz H. Influence of type and extent of surgery on early results and survival time in glioblastoma multiforme. Acta Neurochir (Wien) 1991;113: 31–37.
Huber A, Beran H, Becherer A, Prosenc N, Witzmann A. Supratentorial glioma: analysis of clinical and temporal parameters in 163 cases. Neurochirurgia (Stuttg) 1993;36: 189–193.
Kowalczuk A, Macdonald RL, Amidei C, et al. Quantitative imaging study of extent of surgical resection and prognosis of malignant astrocytomas. Neurosurgery 1997;41: 1028–1036.
Levin VA, Yung WK, Bruner J, et al. Phase II study of accelerated fractionation radiation therapy with carboplatin followed by PCV chemotherapy for the treatment of anaplastic gliomas. Int J Radiat Oncol Biol Phys 2002;53: 58–66.
Phillips TL, Levin VA, Ahn DK, et al. Evaluation of bromodeoxyuridine in glioblastoma multiforme: a Northern California Cancer Center Phase II study. Int J Radiat Oncol Biol Phys 1991;21: 709–714.
Pope WB, Sayre J, Perlina A, et al. MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol 2005;26: 2466–2474.
Prados MD, Gutin PH, Phillips TL, et al. Highly anaplastic astrocytoma: a review of 357 patients treated between 1977 and 1989. Int J Radiat Oncol Biol Phys 1992;23: 3–8.
Puduvalli VK, Hashmi M, McAllister LD, et al. Anaplastic oligodendrogliomas: prognostic factors for tumor recurrence and survival. Oncology 2003;65: 259–266.
Sandberg-Wollheim M, Malmstrom P, Stromblad LG, et al. A randomized study of chemotherapy with procarbazine, vincristine, and lomustine with and without radiation therapy for astrocytoma grades 3 and/or 4. Cancer 1991;68: 22–29.
Tortosa A, Vinolas N, Villa S, et al. Prognostic implication of clinical, radiologic, and pathologic features in patients with anaplastic gliomas. Cancer 2003;97: 1063–1071.
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: 156–162.
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.
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Sanai, N., Berger, M.S. Operative techniques for gliomas and the value of extent of resection. Neurotherapeutics 6, 478–486 (2009). https://doi.org/10.1016/j.nurt.2009.04.005
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DOI: https://doi.org/10.1016/j.nurt.2009.04.005