Role of Surgical Resection in Low- and High-Grade Gliomas

  • Shawn L. Hervey-Jumper
  • Mitchel S. BergerEmail author
Part of the following topical collections:
  1. Topical Collection on Neuro-oncology

Opinion statement

Central nervous system tumors are a major cause of morbidity and mortality in the United States. Outside of brain metastasis, low- and high-grade gliomas are the most common intrinsic brain tumors. Low-grade gliomas have a 5- and 10-year survival rate of 97 % and 91 %, respectively, when extent of resection is greater than 90 %. High-grade gliomas are extremely aggressive with the vast majority of patients experiencing recurrence and a median survival of 1 to 3 years. Survival of patients with both low- and high-grade gliomas is enhanced with maximal tumor resection. The pursuit of more aggressive extent of resection must be balanced with preservation of functional pathways. Several innovations in neurosurgical oncology have expanded our understanding of individualized patient neuroanatomy, physiology, and function. Emerging imaging technologies as well as intraoperative techniques have expanded our ability to resect maximal amounts of tumor while preserving essential function. Stimulation mapping of language and motor pathways is well-established for the safe resection of intrinsic brain lesions. Additional techniques including neuro-navigation, fluorescence-guided microsurgery using 5-aminolevulinic acid, intraoperative magnetic resonance imaging, and high-frequency ultrasonography can all be used to improve extent of resection in glioma patients.


Extent of resection Glioma Oncology Glioblastoma 5-ALA High-grade glioma Low-grade glioma Intraoperative MRI Cortical stimulation mapping Surgical resection∙Treatment iMRI Neuro-navigation Ultrasound 


Compliance with Ethics Guidelines

Conflict of Interest

Shawn L. Hervey-Jumper and Mitchel S. Berger declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References and Recommended Reading

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Barnholtz-Sloan JS, Sloan AE, Schwartz AG. Chapter 25: Cancer of the brain and other central nervous system. In: SEER Survival Monograph: Cancer Survival Among Adults: U.S. SEER Program, 1988–2001, Patient and Tumor Characteristics. Bethesda: National Cancer Institute, 2007. Available at: Accessed September 3, 2013.
  2. 2.
    Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):997–1003.PubMedGoogle Scholar
  3. 3.
    Keles GE, Chang EF, Lamborn KR, Tihan T, Chang CJ, Chang SM, 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(1):34–40.PubMedGoogle Scholar
  4. 4.
    Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol. 2008;26(8):1338–45.PubMedGoogle Scholar
  5. 5.
    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(2):190–8.PubMedGoogle Scholar
  6. 6.
    Lote K, Egeland T, Hager B, Stenwig B, Skullerud K, Berg-Johnsen J, et al. Survival, prognostic factors, and therapeutic efficacy in low-grade glioma: a retrospective study in 379 patients. J Clin Oncol. 1997;15(9):3129–40.PubMedGoogle Scholar
  7. 7.
    Nakamura M, Konishi N, Tsunoda S, Nakase H, Tsuzuki T, Aoki H, et al. Analysis of prognostic and survival factors related to treatment of low-grade astrocytomas in adults. Oncology. 2000;58(2):108–16.PubMedGoogle Scholar
  8. 8.
    Nicolato A, Gerosa MA, Fina P, Iuzzolino P, Giorgiutti F, Bricolo A. Prognostic factors in low-grade supratentorial astrocytomas: a uni-multivariate statistical analysis in 76 surgically treated adult patients. Surg Neurol. 1995;44(3):208–21.PubMedGoogle Scholar
  9. 9.
    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(3):291–6.PubMedCentralPubMedGoogle Scholar
  10. 10.
    Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009;360(8):765–73.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Bauman G, Pahapill P, Macdonald D, Fisher B, Leighton C, Cairncross G. Low grade glioma: a measuring radiographic response to radiotherapy. Can J Neurol Sci. 1999;26(1):18–22.PubMedGoogle Scholar
  12. 12.
    Claus EB, Horlacher A, Hsu L, Schwartz RB, Dello-Iacono D, Talos F, et al. Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer. 2005;103(6):1227–33.PubMedGoogle Scholar
  13. 13.
    Ito S, Chandler KL, Prados MD, Lamborn K, Wynne J, Malec MK, et al. Proliferative potential and prognostic evaluation of low-grade astrocytomas. J Neurooncol. 1994;19(1):1–9.PubMedGoogle Scholar
  14. 14.
    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(5):854–62.PubMedGoogle Scholar
  15. 15.
    Karim AB, Maat B, Hatlevoll R, Menten J, Rutten EH, Thomas DG, 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(3):549–56.PubMedGoogle Scholar
  16. 16.
    Leighton C, Fisher B, Bauman G, Depiero S, Stitt L, MacDonald D, et al. Supratentorial low-grade glioma in adults: an analysis of prognostic factors and timing of radiation. J Clin Oncol. 1997;15(4):1294–301.PubMedGoogle Scholar
  17. 17.
    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(1):6–14.PubMedGoogle Scholar
  18. 18.
    Peraud A, Ansari H, Bise K, Reulen HJ. Clinical outcome of supratentorial astrocytoma WHO grade II. Acta Neurochir. 1998;140(12):1213–22.PubMedGoogle Scholar
  19. 19.
    Philippon JH, Clemenceau SH, Fauchon FH, Foncin JF. Supratentorial low-grade astrocytomas in adults. Neurosurgery. 1993;32(4):554–9.PubMedGoogle Scholar
  20. 20.
    Rajan B, Pickuth D, Ashley S, Traish D, Monro P, Elyan S, et al. The management of histologically unverified presumed cerebral gliomas with radiotherapy. Int J Radiat Oncol Biol Phys. 1994;28(2):405–13.PubMedGoogle Scholar
  21. 21.
    Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery. 2008;62(4):753–64.PubMedGoogle Scholar
  22. 22.
    Shaw E, Arusell R, Scheithauer B, O'Fallon J, O'Neill B, Dinapoli R, 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(9):2267–76.PubMedGoogle Scholar
  23. 23.
    Shibamoto Y, Kitakabu Y, Takahashi M, Yamashita J, Oda Y, Kikuchi H, et al. Supratentorial low-grade astrocytoma. Correlation of computed tomography findings with effect of radiation therapy and prognostic variables. Cancer. 1993;72(1):190–5.PubMedGoogle Scholar
  24. 24.
    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(5):581–7.PubMedCentralPubMedGoogle Scholar
  25. 25.
    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(4):783–6.PubMedGoogle Scholar
  26. 26.
    Yeh SA, Ho JT, Lui CC, Huang YJ, Hsiung CY, Huang EY. Treatment outcomes and prognostic factors in patients with supratentorial low-grade gliomas. Br J Radiol. 2005;78(927):230–5.PubMedGoogle Scholar
  27. 27.
    McGirt MJ, Chaichana KL, Gathinji M, Attenello FJ, Than K, Olivi A, et al. Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg. 2009;110(1):156–62.PubMedGoogle Scholar
  28. 28.
    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(4):371–9.PubMedGoogle Scholar
  29. 29.
    Pope WB, Sayre J, Perlina A, Villablanca JP, Mischel PS, Cloughesy TF. MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol. 2005;26(10):2466–74.PubMedGoogle Scholar
  30. 30.•
    Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS. An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg. 2011;115(1):3–8. A retrospective study using volumetric analysis and long-term patient outcomes to determine an extent of resection threshold for patients with glioblastoma.Google Scholar
  31. 31.••
    Capelle L, Fontaine D, Mandonnet E, Taillandier L, Golmard JL, Bauchet L, et al. Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases: clinical article. J Neurosurg. 2013;118(6):1157–68. A retrospective study showing 15 year survival for patients with low-grade glioma.Google Scholar
  32. 32.
    Schomas DA, Laack NN, Rao RD, Meyer FB, Shaw EG, O'Neill BP, et al. Intracranial low-grade gliomas in adults: 30-year experience with long-term follow-up at Mayo Clinic. Neuro Oncol. 2009;11(4):437–45.PubMedCentralPubMedGoogle Scholar
  33. 33.••
    Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, Unsgard G, et al. Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA. 2012;308(18):1881–8. A retrospective analysis showing the survival benefit of surgical resection over biopsy with watchful waiting for patients with low-grade glioma.Google Scholar
  34. 34.
    Duffau H, Moritz-Gasser S, Gatignol P. Functional outcome after language mapping for insular World Health Organization Grade II gliomas in the dominant hemisphere: experience with 24 patients. Neurosurg Focus. 2009;27(2):E7. doi: 10.3171/2009.5.FOCUS0938.PubMedGoogle Scholar
  35. 35.
    Soffietti R, Baumert BG, Bello L, von Deimling A, Duffau H, Frenay M, et al. Guidelines on management of low-grade gliomas: report of an EFNS-EANO Task Force. Eur J Neurol. 2010;17(9):1124–33.PubMedGoogle Scholar
  36. 36.
    Frazier JL, Johnson MW, Burger PC, Weingart JD, Quinones-Hinojosa A. Rapid malignant transformation of low-grade astrocytomas: report of 2 cases and review of the literature. World Neurosurg. 2010;73(1):53–62.PubMedGoogle Scholar
  37. 37.
    Recht LD, Lew R, Smith TW. Suspected low-grade glioma: is deferring treatment safe? Ann Neurol. 1992;31(4):431–6.PubMedGoogle Scholar
  38. 38.
    Piepmeier J, Christopher S, Spencer D, Byrne T, Kim J, Knisel JP, et al. Variations in the natural history and survival of patients with supratentorial low-grade astrocytomas. Neurosurgery. 1996;38(5):872–8.PubMedGoogle Scholar
  39. 39.
    Ruda R, Bello L, Duffau H, Soffietti R. Seizures in low-grade gliomas: natural history, pathogenesis, and outcome after treatments. Neuro Oncol. 2012;14 Suppl 4:iv55–64.PubMedCentralPubMedGoogle Scholar
  40. 40.
    Englot DJ, Han SJ, Berger MS, Barbaro NM, Chang EF. Extent of surgical resection predicts seizure freedom in low-grade temporal lobe brain tumors. Neurosurgery. 2012;70(4):921–8.PubMedGoogle Scholar
  41. 41.
    Barker 2nd FG, Prados MD, Chang SM, Gutin PH, Lamborn KR, Larson DA, et al. Radiation response and survival time in patients with glioblastoma multiforme. J Neurosurg. 1996;84(3):442–8.PubMedGoogle Scholar
  42. 42.•
    Bloch O, Han SJ, Cha S, Sun MZ, Aghi MK, McDermott MW, et al. Impact of extent of resection for recurrent glioblastoma on overall survival: clinical article. J Neurosurg. 2012;117(6):1032–8. A retrospective analysis showing the value of extent of re-operation with maximal extent of resection for patients with recurrent glioblastoma.Google Scholar
  43. 43.
    Brown PD, Ballman KV, Rummans TA, Maurer MJ, Sloan JA, Boeve BF, et al. Prospective study of quality of life in adults with newly diagnosed high-grade gliomas. J Neurooncol. 2006;76(3):283–91.PubMedGoogle Scholar
  44. 44.
    Buckner JC, Schomberg PJ, McGinnis WL, Cascino TL, Scheithauer BW, O'Fallon JR, 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. Cancer. 2001;92(2):420–33.PubMedGoogle Scholar
  45. 45.
    Curran WJJ, Scott CB, Horton J, Nelson JS, Weinstein AS, Nelson DF, 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(3):219–27.PubMedGoogle Scholar
  46. 46.
    Dinapoli RP, Brown LD, Arusell RM, Earle JD, O'Fallon JR, Buckner JC, et al. Phase III comparative evaluation of PCNU and carmustine combined with radiation therapy for high-grade glioma. J Clin Oncol. 1993;11(7):1316–21.PubMedGoogle Scholar
  47. 47.
    Duncan GG, Goodman GB, Ludgate CM, Rheaume DE. The treatment of adult supratentorial high grade astrocytomas. J Neurooncol. 1992;13(1):63–72.PubMedGoogle Scholar
  48. 48.
    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. 1991;113(1–2):31–7.PubMedGoogle Scholar
  49. 49.
    Huber A, Beran H, Becherer A, Prosenc N, Witzmann A. [Supratentorial glioma: analysis of clinical and temporal parameters in 163 cases]. Neurochirurgia. 1993;36(6):189–93.PubMedGoogle Scholar
  50. 50.
    Jeremic B, Grujicic D, Antunovic V, Djuric L, Stojanovic M, Shibamoto Y. 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(2):177–85.PubMedGoogle Scholar
  51. 51.
    Kowalczuk A, Macdonald RL, Amidei C, Dohrmann III G, Erickson RK, Hekmatpanah J, et al. Quantitative imaging study of extent of surgical resection and prognosis of malignant astrocytomas. Neurosurgery. 1997;41(5):1028–36.PubMedGoogle Scholar
  52. 52.
    Lamborn KR, Chang SM, Prados MD. Prognostic factors for survival of patients with glioblastoma: recursive partitioning analysis. Neuro Oncol. 2004;6(3):227–35.PubMedCentralPubMedGoogle Scholar
  53. 53.
    Levin VA, Yung WK, Bruner J, Kyritsis A, Leeds N, Gleason MJ, 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(1):58–66.PubMedGoogle Scholar
  54. 54.
    Nitta T, Sato K. Prognostic implications of the extent of surgical resection in patients with intracranial malignant gliomas. Cancer. 1995;75(11):2727–31.PubMedGoogle Scholar
  55. 55.
    Nomiya T, Nemoto K, Kumabe T, Takai Y, Yamada S. Prognostic significance of surgery and radiation therapy in cases of anaplastic astrocytoma: retrospective analysis of 170 cases. J Neurosurg. 2007;106(4):575–81.PubMedGoogle Scholar
  56. 56.
    Oszvald A, Guresir E, Setzer M, Vatter H, Senft C, Seifert V, et al. Glioblastoma therapy in the elderly and the importance of the extent of resection regardless of age. J Neurosurg. 2012;116(2):357–64.PubMedGoogle Scholar
  57. 57.
    Phillips TL, Levin VA, Ahn DK, Gutin PH, Davis RL, Wilson CB, et al. Evaluation of bromodeoxyuridine in glioblastoma multiforme: a Northern California Cancer Center Phase II study. Int J Radiat Oncol Biol Phys. 1991;21(3):709–14.PubMedGoogle Scholar
  58. 58.
    Prados MD, Gutin PH, Phillips TL, Wara WM, Larson DA, Sneed PK, et al. Highly anaplastic astrocytoma: a review of 357 patients treated between 1977 and 1989. Int J Radiat Oncol Biol Phys. 1992;23(1):3–8.PubMedGoogle Scholar
  59. 59.
    Puduvalli VK, Hashmi M, McAllister LD, Levin VA, Hess KR, Prados M, et al. Anaplastic oligodendrogliomas: prognostic factors for tumor recurrence and survival. Oncology. 2003;65(3):259–66.PubMedGoogle Scholar
  60. 60.
    Sandberg-Wollheim M, Malmstrom P, Stromblad LG, Anderson H, Borgstrom S, Brun A, 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(1):22–9.PubMedGoogle Scholar
  61. 61.
    Shibamoto Y, Yamashita J, Takahashi M, Yamasaki T, Kikuchi H, Abe M. Supratentorial malignant glioma: an analysis of radiation therapy in 178 cases. Radiother Oncol. 1990;18(1):9–17.PubMedGoogle Scholar
  62. 62.
    Simpson JR, Horton J, Scott C, Curran WJ, Rubin P, Fischbach J, 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(2):239–44.PubMedGoogle Scholar
  63. 63.
    Stark AM, Nabavi A, Mehdorn HM, Blomer U. Glioblastoma multiforme-report of 267 cases treated at a single institution. Surg Neurol. 2005;63(2):162–9.PubMedGoogle Scholar
  64. 64.
    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. 2005;45(9):454–60.Google Scholar
  65. 65.
    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(6):466–71.PubMedCentralPubMedGoogle Scholar
  66. 66.
    Penfield W, Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain. 1937;60(4):389–443. doi: 10.1093/brain/60.4.389.Google Scholar
  67. 67.
    Herholz K, Thiel A, Wienhard K, Pietrzyk U, von Stockhausen HM, Karbe H, et al. Individual functional anatomy of verb generation. Neuroimage. 1996;3(3 Pt 1):185–94.PubMedGoogle Scholar
  68. 68.
    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(3):316–26.PubMedGoogle Scholar
  69. 69.
    Ojemann GA. Individual variability in cortical localization of language. J Neurosurg. 1979;50(2):164–9.PubMedGoogle Scholar
  70. 70.
    Ojemann GA. Cortical organization of language. J Neurosci. 1991;11(8):2281–7.PubMedGoogle Scholar
  71. 71.
    Ojemann GA, Whitaker HA. Language localization and variability. Brain Lang. 1978;6(2):239–60.PubMedGoogle Scholar
  72. 72.
    Ojemann JG, Miller JW, Silbergeld DL. Preserved function in brain invaded by tumor. Neurosurgery. 1996;39(2):253–8.PubMedGoogle Scholar
  73. 73.
    Seitz RJ, Huang Y, Knorr U, Tellmann L, Herzog H, Freund HJ. Large-scale plasticity of the human motor cortex. Neuroreport. 1995;6(5):742–4.PubMedGoogle Scholar
  74. 74.
    Wunderlich G, Knorr U, Herzog H, Kiwit JC, Freund HJ, Seitz RJ. Precentral glioma location determines the displacement of cortical hand representation. Neurosurgery. 1998;42(1):18–26.PubMedGoogle Scholar
  75. 75.
    Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med. 2008;358(1):18–27.PubMedGoogle Scholar
  76. 76.
    Davies KG, Maxwell RE, Jennum P, Dhuna A, Beniak TE, Destafney E, et al. Language function following subdural grid-directed temporal lobectomy. Acta Neurol Scand. 1994;90(3):201–6.PubMedGoogle Scholar
  77. 77.
    FitzGerald DB, Cosgrove GR, Ronner S, Jiang H, Buchbinder BR, Belliveau JW, et al. Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. AJNR Am J Neuroradiol. 1997;18(8):1529–39.PubMedGoogle Scholar
  78. 78.
    Quinones-Hinojosa A, Ojemann SG, Sanai N, Dillon WP, Berger MS. Preoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. J Neurosurg. 2003;99(2):311–8.PubMedGoogle Scholar
  79. 79.
    Seghier ML, Lazeyras F, Pegna AJ, Annoni JM, Zimine I, Mayer E, et al. Variability of fMRI activation during a phonological and semantic language task in healthy subjects. Hum Brain Mapp. 2004;23(3):140–55.PubMedGoogle Scholar
  80. 80.
    Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA. Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage. 2002;16(3 Pt 1):765–80.PubMedGoogle Scholar
  81. 81.
    Tzourio-Mazoyer N, Josse G, Crivello F, Mazoyer B. Interindividual variability in the hemispheric organization for speech. Neuroimage. 2004;21(1):422–35.PubMedGoogle Scholar
  82. 82.
    Ranck Jr JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 1975;98(3):417–40.PubMedGoogle Scholar
  83. 83.
    Haglund MM, Berger MS, Shamseldin M, Lettich E, Ojemann GA. Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery. 1994;34(4):567–76.PubMedGoogle Scholar
  84. 84.
    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(1):35–41.PubMedGoogle Scholar
  85. 85.
    Skirboll SS, Ojemann GA, Berger MS, Lettich E, Winn HR. Functional cortex and subcortical white matter located within gliomas. Neurosurgery. 1996;38(4):678–84.PubMedGoogle Scholar
  86. 86.
    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(2):349–51.PubMedGoogle Scholar
  87. 87.
    Sanai N, Berger MS. Mapping the horizon: techniques to optimize tumor resection before and during surgery. Clin Neurosurg. 2008;55:14–9.PubMedGoogle Scholar
  88. 88.
    Albert FK, Forsting M, Sartor K, Adams HP, Kunze S. Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery. 1994;34(1):45–60.PubMedGoogle Scholar
  89. 89.
    Orringer D, Lau D, Khatri S, Zamora-Berridi GJ, Zhang K, Wu C, et al. Extent of resection in patients with glioblastoma: limiting factors, perception of resectability, and effect on survival. J Neurosurg. 2012;117(5):851–9.PubMedGoogle Scholar
  90. 90.
    Kennedy JC, Pottier RH. Endogenous protoporphyrin IX, a clinically useful photosensitizer for photodynamic therapy. J Photochem Photobiol B. 1992;14(4):275–92.PubMedGoogle Scholar
  91. 91.
    el-Sharabasy MM, el-Waseef AM, Hafez MM, Salim SA. Porphyrin metabolism in some malignant diseases. Br J Cancer. 1992;65(3):409–12.PubMedCentralPubMedGoogle Scholar
  92. 92.
    Pottier RH, Chow YF, LaPlante JP, Truscott TG, Kennedy JC, Beiner LA. Noninvasive technique for obtaining fluorescence excitation and emission spectra in vivo. Photochem Photobiol. 1986;44(5):679–87.PubMedGoogle Scholar
  93. 93.
    Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ. Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg. 2000;93(6):1003–13.PubMedGoogle Scholar
  94. 94.
    Stummer W, Stocker S, Wagner S, Stepp H, Fritsch C, Goetz C, et al. Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery. 1998;42(3):518–25.PubMedGoogle Scholar
  95. 95.
    Lilge L, Olivo MC, Schatz SW, MaGuire JA, Patterson MS, Wilson BC. The sensitivity of normal brain and intracranially implanted VX2 tumour to interstitial photodynamic therapy. Br J Cancer. 1996;73(3):332–43.PubMedCentralPubMedGoogle Scholar
  96. 96.
    Diez Valle R, Slof J, Galvan J, Arza C, Romariz C, Vidal C. Observational, retrospective study of the effectiveness of 5-aminolevulinic acid in malignant glioma surgery in Spain (The VISIONA study). Neurologia. 2013. doi: 10.1016/j.nrl.2013.05.004.PubMedGoogle Scholar
  97. 97.
    Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 2006;7(5):392–401.PubMedGoogle Scholar
  98. 98.
    Stummer W, Reulen HJ, Meinel T, Pichlmeier U, Schumacher W, Tonn JC, et al. Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery. 2008;62(3):564–76.PubMedGoogle Scholar
  99. 99.
    Roberts TP, Zusman E, McDermott M, Barbaro N, Rowley HA. Correlation of functional magnetic source imaging with intraoperative cortical stimulation in neurosurgical patients. J Image Guid Surg. 1995;1(6):339–47.PubMedGoogle Scholar
  100. 100.
    Schucht P, Beck J, Abu-Isa J, Andereggen L, Murek M, Seidel K, 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(5):927–35.PubMedGoogle Scholar
  101. 101.
    Tsugu A, Ishizaka H, Mizokami Y, Osada T, Baba T, Yoshiyama M, et al. Impact of the combination of 5-aminolevulinic acid-induced fluorescence with intraoperative magnetic resonance imaging-guided surgery for glioma. World Neurosurg. 2011;76(1–2):120–7.PubMedGoogle Scholar
  102. 102.
    Bogomolny DL, Petrovich NM, Hou BL, Peck KK, Kim MJ, Holodny AI. Functional MRI in the brain tumor patient. Top Magn Reson Imaging. 2004;15(5):325–35.PubMedGoogle Scholar
  103. 103.
    Guggisberg AG, Honma SM, Findlay AM, Dalal SS, Kirsch HE, Berger MS, et al. Mapping functional connectivity in patients with brain lesions. Ann Neurol. 2008;63(2):193–203.PubMedCentralPubMedGoogle Scholar
  104. 104.
    Hirsch J, Ruge MI, Kim KH, Correa DD, Victor JD, Relkin NR, et al. An integrated functional magnetic resonance imaging procedure for preoperative mapping of cortical areas associated with tactile, motor, language, and visual functions. Neurosurgery. 2000;47(3):711–21.PubMedGoogle Scholar
  105. 105.
    Meyer PT, Sturz L, Schreckenberger M, Spetzger U, Meyer GF, Setani KS, et al. Preoperative mapping of cortical language areas in adult brain tumour patients using PET and individual non-normalised SPM analyses. Eur J Nucl Med Mol Imaging. 2003;30(7):951–60.PubMedGoogle Scholar
  106. 106.
    Mueller WM, Yetkin FZ, Hammeke TA, Morris III GL, Swanson SJ, Reichert K, et al. Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors. Neurosurgery. 1996;39(3):515–20.PubMedGoogle Scholar
  107. 107.
    Schreckenberger M, Spetzger U, Sabri O, Meyer PT, Zeggel T, Zimny M, et al. Localisation of motor areas in brain tumour patients: a comparison of preoperative [18F]FDG-PET and intraoperative cortical electrostimulation. Eur J Nucl Med. 2001;28(9):1394–403.PubMedGoogle Scholar
  108. 108.
    Tarapore PE, Martino J, Guggisberg AG, Owen J, Honma SM, Findlay A, et al. Magnetoencephalographic imaging of resting-state functional connectivity predicts postsurgical neurological outcome in brain gliomas. Neurosurgery. 2012;71(5):1012–22.PubMedCentralPubMedGoogle Scholar
  109. 109.
    Vlieger EJ, Majoie CB, Leenstra S, Den Heeten GJ. Functional magnetic resonance imaging for neurosurgical planning in neurooncology. Eur Radiol. 2004;14(7):1143–53.PubMedGoogle Scholar
  110. 110.
    Black PM, Alexander 3rd E, Martin C, Moriarty T, Nabavi A, Wong TZ, et al. Craniotomy for tumor treatment in an intraoperative magnetic resonance imaging unit. Neurosurgery. 1999;45(3):423–31.PubMedGoogle Scholar
  111. 111.
    Knauth M, Wirtz CR, Tronnier VM, Aras N, Kunze S, Sartor K. Intraoperative MR imaging increases the extent of tumor resection in patients with high-grade gliomas. AJNR Am J Neuroradiol. 1999;20(9):1642–6.PubMedGoogle Scholar
  112. 112.
    Kowalik K, Truwit C, Hall W, Kucharczyk J. Initial assessment of costs and benefits of MRI-guided brain tumor resection. Eur Radiol. 2000;10(3):S366–7.PubMedGoogle Scholar
  113. 113.
    Kubben PL, ter Meulen KJ, Schijns OE, ter Laak-Poort MP, van Overbeeke JJ, van Santbrink H. Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncol. 2011;12(11):1062–70.PubMedGoogle Scholar
  114. 114.
    Lu J, Wu J, Yao C, Zhuang D, Qiu T, Hu X, et al. Awake language mapping and 3-Tesla intraoperative MRI-guided volumetric resection for gliomas in language areas. J Clin Neurosci. 2013;20(9):1280–7.PubMedGoogle Scholar
  115. 115.
    Nimsky C, Fujita A, Ganslandt O, Von Keller B, Fahlbusch R. Volumetric assessment of glioma removal by intraoperative high-field magnetic resonance imaging. Neurosurgery. 2004;55(2):358–70.PubMedGoogle Scholar
  116. 116.
    Nimsky C, Ganslandt O, Tomandl B, Buchfelder M, Fahlbusch R. Low-field magnetic resonance imaging for intraoperative use in neurosurgery: a 5-year experience. Eur Radiol. 2002;12(11):2690–703.PubMedGoogle Scholar
  117. 117.
    Nimsky C, Ganslandt O, Von Keller B, Romstock J, Fahlbusch R. Intraoperative high-field-strength MR imaging: implementation and experience in 200 patients. Radiology. 2004;233(1):67–78.PubMedGoogle Scholar
  118. 118.
    Ntoukas V, Krishnan R, Seifert V. The new generation polestar n20 for conventional neurosurgical operating rooms: a preliminary report. Neurosurgery. 2008;62(3 Suppl 1):82–9.PubMedGoogle Scholar
  119. 119.
    Schneider JP, Schulz T, Schmidt F, Dietrich J, Lieberenz S, Trantakis C, et al. Gross-total surgery of supratentorial low-grade gliomas under intraoperative MR guidance. AJNR Am J Neuroradiol. 2001;22(1):89–98.PubMedGoogle Scholar
  120. 120.
    Schneider JP, Trantakis C, Rubach M, Schulz T, Dietrich J, Winkler D, et al. Intraoperative MRI to guide the resection of primary supratentorial glioblastoma multiforme–a quantitative radiological analysis. Neuroradiology. 2005;47(7):489–500.PubMedGoogle Scholar
  121. 121.
    Shaikhouni A, Chiocca EA. Editorial: Intraoperative magnetic resonance spectroscopy and gliomas. J Neurosurg. 2013;118(6):1188–9.PubMedGoogle Scholar
  122. 122.
    Senft C, Franz K, Ulrich CT, Bink A, Szelenyi A, Gasser T, et al. Low field intraoperative MRI-guided surgery of gliomas: a single center experience. Clin Neurol Neurosurg. 2010;112(3):237–43.PubMedGoogle Scholar
  123. 123.
    Wirtz CR, Knauth M, Staubert A, Bonsanto MM, Sartor K, Kunze S, et al. Clinical evaluation and follow-up results for intraoperative magnetic resonance imaging in neurosurgery. Neurosurgery. 2000;46(5):1112–20.PubMedGoogle Scholar
  124. 124.
    Enchev Y, Bozinov O, Miller D, Tirakotai W, Heinze S, Benes L, et al. Image-guided ultrasonography for recurrent cystic gliomas. Acta Neurochir. 2006;148(10):1053–63.PubMedGoogle Scholar
  125. 125.
    Erdogan N, Tucer B, Mavili E, Menku A, Kurtsoy A. Ultrasound guidance in intracranial tumor resection: correlation with postoperative magnetic resonance findings. Acta Radiol. 2005;46(7):743–9.PubMedGoogle Scholar
  126. 126.
    Le Roux PD, Berger MS, Wang K, Mack LA, Ojemann GA. Low grade gliomas: comparison of intraoperative ultrasound characteristics with preoperative imaging studies. J Neurooncol. 1992;13(2):189–98.PubMedGoogle Scholar
  127. 127.
    Serra C, Stauffer A, Actor B, Burkhardt JK, Ulrich NH, Bernays RL, et al. Intraoperative high frequency ultrasound in intracerebral high-grade tumors. Ultraschall Med. 2012;33(7):E306–12.PubMedGoogle Scholar
  128. 128.
    Tortosa A, Vinolas N, Villa S, Verger E, Gil JM, Brell M, et al. Prognostic implication of clinical, radiologic, and pathologic features in patients with anaplastic gliomas. Cancer. 2003;97(4):1063–71.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Neurological SurgeryUniversity of CaliforniaSan FranciscoUSA

Personalised recommendations