Present day’s standards in microsurgery of low-grade gliomas

  • L. Bello
  • E. Fava
  • G. Carrabba
  • C. Papagno
  • S. M. Gaini
Part of the Advances and Technical Standards in Neurosurgery book series (NEUROSURGERY, volume 35)


Low-grade gliomas are slow growing intrinsic lesions that induces a progressive functional reshaping of the brain. Surgical removal of these lesions requires the combined efforts of a multidisclipinary team of neurosurgeon, neuroradiologist, neuropsychologist, neurophysiologist, and neurooncologists that all together contribute in the definition of the location, extension, and extent of functional involvement that a specific lesion has induced in a particular patient. Each tumor has induced particular and specific changes of the functional network, that varies among patients. This requires that each treatment plan should be tailored to the tumor and to the patient. When this is reached, surgery should be accomplished according to functional and anatomical boundaries, and has to aim to the maximal resection with the maximal patient functional preservation. This can be reached at the time of the initial surgery, depending on the functional organization of the brain, or may require additional surgeries, eventually intermingled with adjuvant treatments. The use of so called brain mapping techniques extend surgical indications, improve extent of resection with greater oncological impact, minimization of morbidity and increase in quality of life. To achieve the goal of a satisfactory tumor resection associated with the full preservation of the patients abilities, a series of neuropsychological, neurophysiological, neuroradiological and intraoperative investigations have to be performed. In this chapter, we will describe the rationale, the indications and the modality for performing a safe and rewarding surgical removal of low-grade gliomas by using these techniques, as well as the functional and oncological results.


Low-grade gliomas brain mapping fMRI fiber tracking neuropsychology 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Andrewes DG, Kaye A, Murphy M, Harris B, Aitken S, Parr C, Bates L (2003) Emotional and social dysfunction in patients following surgical treatment for brain tumor. J Clin Neurosci 10: 428–33PubMedGoogle Scholar
  2. 2.
    Andrewes DG, Kaye A, Aitken S, Parr C, Bates L, Murphy M (2003) The ESDQ: a new method of assessing emotional and social dysfunction in patients following brain surgery. J Clin Exp Neuropsychol 25: 173–89PubMedGoogle Scholar
  3. 3.
    Archip N, Clatz O, Whalen S, Kacher D, Fedorov A, Kot A, Chrisochoides N, Jolesz F, Golby A, Black PM, Warfield SK (2007) Non-rigid alignment of pre-operative MRI, fMRI, and DT-MRI with intra-operative MRI for enhanced visualization and navigation in imageguided neurosurgery. Neuroimage 35(2): 609–24PubMedGoogle Scholar
  4. 4.
    Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine/Society of Magnetic Resonance in Medicine 44(4): 625–32Google Scholar
  5. 5.
    Bello L, Acerbi F, Giussani C, Baratta P, Taccone P, Songa V, Fava M, Stocchetti N, Papagno C, Gaini SM (2006) Intraoperative language localization in multilingual patients with gliomas. Neurosurgery 59(1): 115–25; discussion 115–25PubMedGoogle Scholar
  6. 6.
    Bello L, Gallucci M, Fava M, Carrabba G, Giussani C, Acerbi F, Baratta P, Songa V, Conte V, Branca V, Stocchetti N, Papagno C, Gaini SM (2007) Intraoperative subcortical language tract mapping guides surgical removal of gliomas involving speech areas. Neurosurgery 60(1): 67–80; discussion 80–82PubMedGoogle Scholar
  7. 7.
    Bello L, Gambini A, Castellano A, Carrabba G, Acerbi F, Fava E, Giussani C, Cadioli M, Blasi V, Casarotti A, Papagno C, Gupta AK, Gaini S, Scotti G, Falini A (2008) Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 39(1): 369–82 (Epub 2007 Aug 29)PubMedGoogle Scholar
  8. 8.
    Benard F, Romsa J, Hustinx R (2003) Imaging gliomas with positron emission tomography and single-photon emission computed tomography. Semin Nucl Med 33: 148–62PubMedGoogle Scholar
  9. 9.
    Berger MS, Ojemann G A, Lettich E (1990) Neurophysiological monitoring during astrocytoma surgery. Neurosurg Clin N Am 1: 65–70PubMedGoogle Scholar
  10. 10.
    Berger MS, Deliganis AV, Dobbins J, et al. (1994) The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer 74: 1784–91PubMedGoogle Scholar
  11. 11.
    Berger MS (1995) Functional mapping-guided resection of low-grade gliomas. Clin-Neurosurg 42: 437–52PubMedGoogle Scholar
  12. 12.
    Berger MS, Rostomily RC (1997) Low-grade gliomas: Functional mapping resection strategies, extent of resection, and outcome. J Neurooncol 34: 85–101PubMedGoogle Scholar
  13. 13.
    Berman JI, Berger MS, Mukherjee P, Henry RG (2004) Diffusion-tensor imaging-guided tracking of fibers of the pyramidal tract combined with intraoperative cortical stimulation mapping in patients with gliomas. J Neurosurg 101(1): 66–72PubMedGoogle Scholar
  14. 14.
    Black PM, Ronner SF (1987) Cortical mapping for defining the limits of tumor resection. Neurosurgery 25: 786–92Google Scholar
  15. 15.
    Bogomolny DL, Petrovich NM, Hou BL, Peck KK, Kim MJ, Holodny AI (2004) Functional MRI in the brain tumor patient. Top Magn Reson Imaging 15: 325–35PubMedGoogle Scholar
  16. 16.
    Branco DM, Coelho TM, Branco BM, Schmidt L, Calcagnotto ME, Portuguez M, Neto EP, Paglioli E, Palmini A, Lima JV, Da Costa JC (2003) Functional variability of the human cortical motor map: electrical stimulation findings in perirolandic epilepsy surgery. J Clin Neurophysiol 20: 17–25PubMedGoogle Scholar
  17. 17.
    Brown PD, Buckner J C, O’Neill BP, Brown CA, Scheithauer BW, Dinapoli RP, Arusell RM, Curran WJ, Abrams R, Shaw EG (2004) North Central Cancer Treatment Group; Mayo Clinic: Importance of baseline mini-mental state examination as a prognostic factor for patients with low-grade glioma. Int J Radiat Oncol Biol Phys 59: 117–25PubMedGoogle Scholar
  18. 18.
    Capelle L, Duffau H, Lopes M, Sichez JP, Bitar A, Faillot T, Arthuis F, Cornu P, Van Effenterre R, Keime-Guibert F, Carpentier A, Hong-Xuan K, Sanson M, Delattre JY, Kujas M, Mokhtari K, Poirier J, Sahel M, Zouaoui A, Lehericy S, Guillevin R, Guerin G, Mitchell MC, Roche S, Abdennour L, Puybasset L (2002) Who grade 2 gliomas in adults: a study of prognostic factors with special emphasis on the role of surgery. J Neurooncol 4: S17–69Google Scholar
  19. 19.
    Carrabba G, Fava E, Giussani C, Acerbi F, Portaluri F, Songa V, Stocchetti N, Branca V, Gaini SM, Bello L (2007) Cortical and subcortical motor mapping in rolandic and perirolandic glioma surgery: impact on postoperative morbidity and extent of resection. J Neurosurg Sci 51(2): 45–51PubMedGoogle Scholar
  20. 20.
    Carrabba G, Fava E, Mandonnet E, Capelle L, Duffau H, Bello L (2008) Transient axonal inhibition induced by CUSA during brain mapping: a case report with motor EMG evidence. Neurosurgery 63(1): E178–79; discussion E179PubMedGoogle Scholar
  21. 21.
    Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17: 77–94PubMedGoogle Scholar
  22. 22.
    Cavaliere R, Lopes MB, Schiff D (2005) Low-grade gliomas: An update on pathology and therapy. Lancet Neurol 4: 760–70PubMedGoogle Scholar
  23. 23.
    Cha S, Tihan T, Crawford F, Fischbein NJ, Chang S, Bollen A, Nelson SJ, Prados M, Berger MS, Dillon WP (2005) Differentiation of low-grade oligodendrogliomas from lowgrade astrocytomas by using quantitative blood-volume measurements derived from dynamic susceptibility contrast-enhanced MR imaging. Am J Neuroradiol 26(2): 266–73PubMedGoogle Scholar
  24. 24.
    Chahlavi A, Kanner A, Peereboom D, Staugaitis SM, Elson P, Barnett G (2003) Impact of chromosome 1p status in response of oligodendroglioma to temozolomide: preliminary results. J Neurooncol 61: 267–73PubMedGoogle Scholar
  25. 25.
    Chang EF, Potts MB, Keles GE, Lamborn KR, Chang SM, Barbaro NM, Berger MS (2008) Seizure characteristics and control following resection in 332 patients with low-grade gliomas. J Neurosurg 108(2): 227–35PubMedGoogle Scholar
  26. 26.
    Claus EB, Horlacher A, Hsu L, et al. (2005) Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer 103: 1227–33PubMedGoogle Scholar
  27. 27.
    Clark CA, Barrick TR, Murphy MM, Bell BA (2003) White matter fiber tracking in patients with space-occupying lesions of the brain: a new technique for neurosurgical planning? NeuroImage 20(3): 1601–08PubMedGoogle Scholar
  28. 28.
    Cedzich C, Taniguchi M, Schaffer S, Schramm J (1996) Somatosensory evoked potential phase reversal and direct motor cortex stimulation during surgery in and around the central region. Technical application. Neurosurgery 38: 962–71PubMedGoogle Scholar
  29. 29.
    Danks RA, Rogers M, Aglio LS, Gugino LD, Black PM (1998) Patient tolerance of craniotomy performed with the patient under local anesthesia and monitored conscious sedation. Neurosurgery 42: 28–36PubMedGoogle Scholar
  30. 30.
    Danks RA, Aglio LS, Gugino LD, Black PM (2000) Craniotomy under local anesthesia and monitored conscious sedation for the resection of tumors involving eloquent cortex. J Neurooncol 49: 131–39PubMedGoogle Scholar
  31. 31.
    Desmurget M, Bonnetblanc F, Duffau H (2007) Contrasting acute and slow-growing lesions: a new door to brain plasticity. Brain 130(Pt 4): 898–14PubMedGoogle Scholar
  32. 32.
    De Witte O, Levivier M, Violon P, Salmon I, Damhaut P, Wikler D Jr, Hildebrand J, Brotchi J, Goldman S (1996) Prognostic value positron emission tomography with [18F]fluoro-2-deoxy-D-glucose in the low-grade glioma. Neurosurgery 39: 470–76PubMedGoogle Scholar
  33. 33.
    Duffau H, Capelle L, Sichez J, Faillot T, Abdennour L, Law Koune JD, Dadoun S, Bitar A, Arthuis F, Van Effenterre R, Fohanno D (1999) Intraoperative direct electrical stimulations of the central nervous system: the Salpêtrière experience with 60 patients. Acta Neurochir (Wien) 141: 1157–67Google Scholar
  34. 34.
    Duffau H, Sichez JP, Lehéricy S (2000) Intraoperative unmasking of brain redundant motor sites during resection of a precentral angioma: evidence using direct cortical stimulation. Ann Neurol 47: 132–35PubMedGoogle Scholar
  35. 35.
    Duffau H, Denvil D, Lopes M, Gasparini F, Cohen L, Capelle L, Van Effenterre R (2002) Intraoperative mapping of the cortical areas involved in multiplication and subtraction: an electrostimulation study in a patient with a left parietal glioma. J Neurol Neurosurg Psychiatry 73: 733–38PubMedGoogle Scholar
  36. 36.
    Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, Bitar A, Fohanno D (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomofunctional study. Brain 125: 199–214PubMedGoogle Scholar
  37. 37.
    Duffau H, Denvil D, Capelle L (2002) Long term reshaping of language, sensory, and motor maps after glioma resection: a new parameter to integrate in the surgical strategy. J Neurol Neurosurg Psychiatry 72: 511–16PubMedGoogle Scholar
  38. 38.
    Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Lopes M, Mitchell MC, Sichez JP, Van Effenterre R (2003) Functional recovery after surgical resection of low-grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 74: 901–07PubMedGoogle Scholar
  39. 39.
    Duffau L, Capelle L (2004) Preferential brain locations of low-grade gliomas. Cancer 100: 2622–26PubMedGoogle Scholar
  40. 40.
    Duffau H, Khalil I, Gatignol P, Denvil D, Capelle L (2004) Surgical removal of corpus callosum infiltrated by low-grade glioma: functional outcome and oncological considerations. J Neurosurg 100: 431–37PubMedGoogle Scholar
  41. 41.
    Duffau H, Lopes M, Arthuis F, et al. (2005) Contribution of intraoperative electrical stimulations in surgery of low-grade gliomas: a comparative study between two series without (1985–96) and with (1996–2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 76: 845–51PubMedGoogle Scholar
  42. 42.
    Duffau H (2005) Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 4: 476–86PubMedGoogle Scholar
  43. 43.
    Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128: 797–810PubMedGoogle Scholar
  44. 44.
    Duffau H, Taillandier L, Capelle L (2006) Radical surgery after chemotherapy: a new therapeutic strategy to envision in grade II glioma. J Neurooncol 80(2): 171–76PubMedGoogle Scholar
  45. 45.
    Duffau H (2006) New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity — a review. J Neurooncol 79(1): 77–115PubMedGoogle Scholar
  46. 46.
    Ebel H, Ebel M, Schillinger G, Klimek M, Sobesky J, Klug N (2000) Surgery of intrinsic cerebral neoplasms in eloquent areas under local anesthesia. Minim Invasive Neurosurg 43: 192–96PubMedGoogle Scholar
  47. 47.
    Ebeling U, Schmid UD, Ying H, Reulen HJ (1992) Safe surgery of lesions near the motor cortex using intraoperative mapping techniques: a report on 50 patients. Acta Neurochir (Wien) 119: 23–28Google Scholar
  48. 48.
    Everhard S, Kaloshi G, Crinière E, Benouaich-Amiel A, Lejeune J, Marie Y, Sanson M, Kujas M, Mokhtari K, Hoang-Xuan K, Delattre JY, Thillet J (2006) MGMT methylation: a marker of response to temozolomide in low-grade gliomas. Ann Neurol 60(6): 740–43PubMedGoogle Scholar
  49. 49.
    Fukaya C, Katayama Y, Yoshino A, Kobayashi K, Kasai M, Yamamoto T (2001) Intraoperative wake-up procedure with propofol and laryngeal mask for optimal excision of brain tumor in eloquent areas. J Clin Neurosci 8: 253–55PubMedGoogle Scholar
  50. 50.
    Galanaud D, Chinot O, Nicoli F, Confort-Gouny S, Le Fur Y, Barrie-Attarian M, Ranjeva JP, Fuentes S, Viout P, Figarella-Branger D, Cozzone PJ (2003) Use of proton magnetic resonance spectroscopy of the brain to differentiate gliomatosis cerebri from low-grade glioma. J Neurosurg 98: 269–276PubMedGoogle Scholar
  51. 51.
    Gasparini FM, Cohen L, Lopes M, Denvil D, Capelle L, Duffau H, Van Effenterre R (2005) A clinical study of the number processing system: decimal size effects on reading numbers in patients with left parieto-occipital gliomas. Rev Neurol (Paris) 161: 427–35Google Scholar
  52. 52.
    Giussani C, Roux FE, Lubrano V, Gaini SM, Bello L (2007) Review of language organisation in bilingual patients: what can we learn from direct brain mapping? Acta Neurochir (Wien) 149(11): 1109–16; discussion 1116 [Epub 2007 Aug 23. Review]Google Scholar
  53. 53.
    Goldstein B, Obrzut JE, John C, Ledakis G, Armstrong CL (2004) The impact of frontal and non-frontal brain tumor lesions on Wisconsin Card Sorting Test performance. Brain Cogn 54: 110–16PubMedGoogle Scholar
  54. 54.
    Goldstein B, Obrzut JE, John C, Hunter JV, Armstrong CL (2004) The impact of low-grade brain tumors on verbal fluency performance. J Clin Exp Neuropsychol 26: 750–58PubMedGoogle Scholar
  55. 55.
    Goldstein B, Armstrong CL, Modestino E, Ledakis G, John C, Hunter JV (2004) The impact of left and right intracranial tumors on picture and word recognition memory. Brain Cogn 54: 1–6PubMedGoogle Scholar
  56. 56.
    Gossl C, Fahrmeir L, Putz B, Auer LM, Auer DP (2002) Fiber tracking from DTI using linear state space models: detectability of the pyramidal tract. Neuroimage 16: 378–88PubMedGoogle Scholar
  57. 57.
    Guillevin R, Menuel C, Duffau H, Kujas M, Capelle L, Aubert A, Taillibert S, Idbaih A, Pallud J, Demarco G, Costalat R, Hoang-Xuan K, Chiras J, Vallée JN (2008) Proton magnetic resonance spectroscopy predicts proliferative activity in diffuse low-grade gliomas. J Neurooncol 87(2): 181–87PubMedGoogle Scholar
  58. 58.
    Haglund MM, Berger M (1996) Functional mapping of motor, sensory and language pathways during low-grade glioma removal. Tech Neurosurg 2: 141–49Google Scholar
  59. 59.
    Heimans JJ, Taphoorn MJ (2002) Impact of brain tumour treatment on quality of life. J Neurol 249: 955–60PubMedGoogle Scholar
  60. 60.
    Hildebrand J, Lecaille C, Perennes J, Delattre JY (2005) Epileptic seizures during follow-up of patients treated for primary brain tumors. Neurology 65(2): 212–15PubMedGoogle Scholar
  61. 61.
    Hoang-Xuan K, Capelle L, Kujas M, Taillibert S, Duffau H, Lejeune J, Polivka M, Criniere E, Marie Y, Mokhtari K, Carpentier AF, Laigle F, Simon JM, Cornu P, Broet P, Sanson M, Delattre JY (2004) Temozolomide as initial treatment for adults with low-grade oligodendrogliomas or oligoastrocytomas and correlation with chromosome 1p deletions. J Clin Oncol 22: 3133–38PubMedGoogle Scholar
  62. 62.
    Holodny AI, Schulder M, Liu WC, Wolko J, Maldjian JA, Kalnin AJ (2000) The effect of brain tumors on BOLD functional MR Imaging activation in the adjacent motor cortex: implications for image-guided neurosurgery. Am J Neuroradiol 21: 1415–22PubMedGoogle Scholar
  63. 63.
    Jbabdi S, Mandonnet E, Duffau H, Capelle L, Swanson KR, Pelegrini-Issac M, Guillevin R, Benali H (2005) Diffusion tensor imaging allows anisotropic growth simulations of low-grade gliomas. Mag Reson Med 54: 616–24Google Scholar
  64. 64.
    Johannesen TB, Langmark F, Lote K (2003) 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 99: 854–62PubMedGoogle Scholar
  65. 65.
    Kaloshi G, Benouaich-Amiel A, Diakite F, Taillibert S, Lejeune J, Laigle-Donadey F, Renard MA, Iraqi W, Idbaih A, Paris S, Capelle L, Duffau H, Cornu P, Simon JM, Mokhtari K, Polivka M, Omuro A, Carpentier A, Sanson M, Delattre JY, Hoang-Xuan K (2007) Temozolomide for low-grade gliomas: predictive impact of 1p/19q loss on response and outcome. Neurology 68(21): 1831–36PubMedGoogle Scholar
  66. 66.
    Kamada K, Todo T, Masutani Y, Aoki S, Ino K, Takano T, Kirino T, Kawahara N, Morita A (2005) Combined use of tractography-integrated functional neuronavigation and direct fiber stimulation. J Neurosurg 102(4): 664–72PubMedGoogle Scholar
  67. 67.
    Keles GE, Lamborn KR, Berger MS (2001) Low-grade hemispheric gliomas in adults: a critical review of extent of resection as a factor influencing outcome. J Neurosurg 95: 735–45PubMedGoogle Scholar
  68. 68.
    Keles GE, Lamborn KR, Berger MS (2003) Coregistration accuracy and detection of brain shift using intraoperative sononavigation during resection of hemispheric tumors. Neurosurgery 53: 556–64PubMedGoogle Scholar
  69. 69.
    Keles GE (2004) Intracranial neuronavigation with intraoperative magnetic resonance imaging. Curr Opin Neurol 17: 497–500PubMedGoogle Scholar
  70. 70.
    Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS (2004) Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. J Neurosurg 100: 369–75PubMedGoogle Scholar
  71. 71.
    Keles GE, Chang EF, Lamborn KR, Tihan T, Chang CJ, Chang SM, Berger MS (2006) Volumetric extent of resection and residual contrast enhancement on initial surgery as predictors of outcome in adult patients with hemispheric anaplastic astrocytoma. J Neurosurg 105(1): 34–40PubMedGoogle Scholar
  72. 72.
    Kleihues P, Cavenee W (2000) Pathology and genetics of tumours of the nervous system. In: Kleihues P, Cavenee W (eds) International Agency for Research on Cancer Press, Lyon, FranceGoogle Scholar
  73. 73.
    Kleihues P, Louis DN, Scheithauer BW, et al. (2002) The WHO classification of tumors of the nervous system. J Neuropathol Exp Neurol 61: 215–29PubMedGoogle Scholar
  74. 74.
    Klein M, Engelberts NH, van der Ploeg HM, Kasteleijn-Nolst Trenite DG, Aaronson NK, Taphoorn MJ, Baaijen H, Vandertop WP, Muller M, Postma TJ, Heimans JJ (2003) Epilepsy in low-grade gliomas: the impact on cognitive function and quality of life. Ann Neurol 54: 514–20PubMedGoogle Scholar
  75. 75.
    Klein M, Heimans JJ (2004) The measurement of cognitive functioning in low-grade glioma patients after radiotherapy. J Clin Oncol 22: 966–67PubMedGoogle Scholar
  76. 76.
    Klein M, Heimans JJ, Aaronson NK, Postma TJ, Muller M, van der Ploeg HM, Taphoorn MJ (2004) Impaired cognitive functioning in low-grade glioma patients: relationship to tumor localisation, radiotherapy and the use of anticonvulsants. Ned Tijdschr Geneeskd 148: 2175–80PubMedGoogle Scholar
  77. 77.
    Kombos T, Suess O, Ciklatekerlio O, Brock M (2001) Monitoring of intraoperative motor evoked potentials to increase the safety of surgery in and around the motor cortex. J Neurosurg 95: 608–14PubMedGoogle Scholar
  78. 78.
    Krainik A, Duffau H, Capelle L, Cornu P, Boch AL, Mangin JF, Le Bihan D, Marsault C, Chiras J, Lehericy S (2004) Role of the healthy hemisphere in recovery after resection of the supple-mentary motor area. Neurology 62: 1323–32PubMedGoogle Scholar
  79. 79.
    Kuznetsov YE, Caramanos Z, Antel SB, Preul MC, Leblanc R, Villemure JG, Pokrupa R, Olivier A, Sadikot A, Arnold DL (2003) Proton magnetic resonance spectroscopic imaging can predict length of survival in patients with supratentorial gliomas. Neurosurgery 53: 565–76PubMedGoogle Scholar
  80. 80.
    Lang FF, Gilbert MR (2006) Diffusely infiltrative low-grade gliomas in adults. J Clin Oncol 24: 1236–45PubMedGoogle Scholar
  81. 81.
    Laws ER, Shaffrey ME, Morris A, Anderson FA Jr (2003) Surgical management of intracranial gliomas-does radical resection improve outcome?. Acta Neurochir Suppl 85: 47–53PubMedGoogle Scholar
  82. 82.
    Lehericy S, Duffau H, Cornu P, Capelle L, Pidoux B, Carpentier A, Auliac S, Clemenceau S, Sichez JP, Bitar A, Valery CA, Van Effenterre R, Faillot T, Srour A, Fohanno D, Philippon J, Le Bihan D, Marsault C (2000) Correspondence between functional magnetic resonance imaging somatotopy and individual brain anatomy of the central region: comparison with intraoperative stimulation in patients with brain tumors. J Neurosurg 92: 589–98PubMedGoogle Scholar
  83. 83.
    Leighton C, Fisher B, Bauman G, et al. (1997) Supratentorial low-grade glioma in adults: an analysis of prognostic factors and timing of radiation. J Clin Oncol 15: 1294–301PubMedGoogle Scholar
  84. 84.
    Lote K, Egeland T, Hager B, Stenwig B, Skullerud K, Berg-Johnsen J, Storm-Mathisen I, Hirschberg H (1997) Survival, prognostic factors, and therapeutic efficacy in low-grade glioma: a retrospective study in 379 patients. J Clin Oncol 15: 3129–40PubMedGoogle Scholar
  85. 85.
    Lucas TH, McKhann GM, Ojemann GA (2004) Functional separation of languages in the bilingual brain: a comparison of electrical stimulation language mapping in 25 bilingual patients and 117 monolingual control patients. J Neurosurg 101: 449–57PubMedGoogle Scholar
  86. 86.
    Mandonnet E, Delattre JY, Tanguy ML, Swanson KR, Carpentier AF, Duffau H, Cornu P, Van Effenterre R, Alvord EC Jr, Capelle L (2003) Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 53: 524–28PubMedGoogle Scholar
  87. 87.
    Mandonnet E, Jbabdi S, Taillandier L, Galanaud D, Benali H, Capelle L, Duffau H (2007) Preoperative estimation of residual volume for WHO grade II glioma resected with intraoperative functional mapping. Neuro Oncol 9(1): 63–69PubMedGoogle Scholar
  88. 88.
    Manninen PH, Tan TK (2002) Postoperative nausea and vomiting after craniotomy for tumor surgery: a comparison between awake craniotomy and general anesthesia. J Clin Anesth 14: 279–83PubMedGoogle Scholar
  89. 89.
    Mariani L, Siegenthaler P, Guzman R, et al. (2004) The impact of tumour volume and surgery on the outcome of adults with supratentorial WHO grade II astrocytomas and oligoastrocytomas. Acta Neurochir (Wien) 146: 441–48Google Scholar
  90. 90.
    Martin C, Alexander E 3rd, Wong T, Schwartz R, Jolesz F, Black PM (1998) Surgical treatment of low-grade gliomas in the intraoperative magnetic resonance imager. Neurosurg Focus 4(4): e8PubMedGoogle Scholar
  91. 91.
    McClain CD, Soriano SG, Goumnerova LC, Black PM, Rockoff MA (2007) Detection of unanticipated intracranial hemorrhage during intraoperative magnetic resonance imageguided neurosurgery. Report of two cases. J Neurosurg 106 (5 Suppl): 398–400PubMedGoogle Scholar
  92. 92.
    Meyer PT, Sturz L, Schreckenberger M, Spetzger U, Meyer GF, Setani KS, Sabri O, Buell U (2003) Preoperative mapping of cortical language areas in adult brain tumor patients using PET and individual non-normalised SPManalyses. Eur J NuclMedMol Imaging 30: 951–60Google Scholar
  93. 93.
    Minn H (2005) PET and SPECT in low-grade glioma. Eur J Radiol 56: 171–78PubMedGoogle Scholar
  94. 94.
    Mittal S, Black PM (2006) Intraoperative magnetic resonance imaging in neurosurgery: the Brigham concept. Acta Neurochir Suppl 98: 77–86PubMedGoogle Scholar
  95. 95.
    Nakamura M, Konishi N, Tsunoda S, Nakase H, Tsuzuki T, Aoki H, Sakitani H, Inui T, Sakaki T (2000) Analysis of prognostic and survival factors related to treatment of lowgrade astrocytomas in adults. Oncology 58: 108–16PubMedGoogle Scholar
  96. 96.
    Neuloh G, Schramm J (2004) Motor evoked potential monitoring for the surgery of brain tumours and vascular malformations. Adv Tech Stand Neurosurg 29: 171–228PubMedGoogle Scholar
  97. 97.
    Nikas DC, Bello L, Zamani AA, Black PM (1998) Neurosurgical considerations in supratentorial low-grade gliomas: experience with 175 patients. Neurosurg Focus 4(4): e4PubMedGoogle Scholar
  98. 98.
    Nimsky C, Ganslandt O, Fahlbusch R (2004) Functional neuronavigation and intraoperative MRI. Adv Tech Stand Neurosurg 29: 229–63PubMedGoogle Scholar
  99. 99.
    Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2005) Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 56(1): 130–37; discussion 138PubMedGoogle Scholar
  100. 100.
    Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2005) Intraoperative diffusion-tensor MR imaging: shifting of white matter tracts during neurosurgical procedures — initial experience. Radiology 234(1): 218–25PubMedGoogle Scholar
  101. 101.
    Nimsky C, Ganslandt O, von Keller B, Fahlbusch R (2006) Intraoperative high-field MRI: anatomical and functional imaging. Acta Neurochir Suppl 98: 87–95PubMedGoogle Scholar
  102. 102.
    Nimsky C, Ganslandt O, Fahlbusch R (2006) Implementation of fiber tract navigation. Neurosurgery 58 (4 Suppl 2): ONS-292-303; discussion ONS-303-04Google Scholar
  103. 103.
    Ojemann G, Ojemann G, Lettich E, Berger M (1989) Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 71: 316–26PubMedGoogle Scholar
  104. 104.
    Pace A, Vidiri A, Galie E, Carosi M, Telera S, Cianciulli AM, Canalini P, Giannarelli D, Jandolo B, Carapella CM (2003) Temozolomide chemotherapy for progressive low-grade glioma: clinical benefits and radiological response. Ann Oncol 14: 1722–26PubMedGoogle Scholar
  105. 105.
    Pallud J, Mandonnet E, Duffau H, Kujas M, Guillevin R, Galanaud D, Taillandier L, Capelle L (2006) Prognostic value of initial magnetic resonance imaging growth rates for World Health Organization grade II gliomas. Ann Neurol 60(3): 380–83PubMedGoogle Scholar
  106. 106.
    Papagikos MA, Shaw EG, Stiebert VW (2005) Lessons learned from randomised clinical trials in adult low-grade glioma. Lancet Oncol 6: 240–44PubMedGoogle Scholar
  107. 107.
    Peraud A, Ansari H, Bise K, Reulen HJ (1998) Clinical outcome of supratentorial astrocytoma WHO grade II. Acta Neurochir (Wien) 140: 1213–22Google Scholar
  108. 108.
    Petrovich N, Holodny AI, Tabar V, Correa DD, Hirsch J, Gutin PH, Brennan CW (2005) Discordance between functional magnetic resonance imaging during silent speech tasks and intraoperative speech arrest. J Neurosurg 103: 267–74PubMedGoogle Scholar
  109. 109.
    Piepmeier J, Baehring JM (2004) Surgical resection for patients with benign primary brain tumors and low-grade gliomas. J Neurooncol 69: 55–65PubMedGoogle Scholar
  110. 110.
    Pignatti F, van den Bent M, Curran D, Debruyne C, Sylvester R, Therasse P, Afra D, Cornu P, Bolla M, Vecht C, Karim AB (2002) European Organization for Research and Treatment of Cancer Brain Tumor Cooperative Group; European Organization for Research and Treatment of Cancer Radiotherapy Cooperative Group: Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20: 2076–84PubMedGoogle Scholar
  111. 111.
    Quinn JA, Reardon DA, Friedman AH, Rich JN, Sampson JH, Provenzale JM, McLendon RE, Gururangan S, Bigner DD, Herndon JE 2nd, Avgeropoulos N, Finlay J, Tourt-Uhlig S, Affronti ML, Evans B, Stafford-Fox V, Zaknoen S, Friedman HS (2003) Phase II trial of temozolomide in patients with progressive low-grade glioma. J Clin Oncol 21: 646–51PubMedGoogle Scholar
  112. 112.
    Rasmussen IA Jr, Lindseth F, Rygh OM, Berntsen EM, Selbekk T, Xu J, Nagelhus Hernes TA, Harg E, Håberg A, Unsgaard G (2007) Functional neuronavigation combined with intra-operative 3D ultrasound: initial experiences during surgical resections close to eloquent brain areas and future directions in automatic brain shift compensation of preoperative data. Acta Neurochir (Wien) 149(4): 365–78Google Scholar
  113. 113.
    Reinges MH, Nguyen HH, Krings T, Hutter BO, Rohde V, Gilsbach JM (2004) Course of brain shift during microsurgical resection of supratentorial cerebral lesions: limits of conventional neuronavigation. Acta Neurochir (Wien) 146: 369–77Google Scholar
  114. 114.
    Reijneveld JC, Sitskoorn MM, Klein M, Nuyen J, Taphoorn MJ (2001) Cognitive status and quality of life in patients with suspected versus proven low-grade gliomas. Neurology 56: 618–23PubMedGoogle Scholar
  115. 115.
    Reithmeier T, Krammer M, Gumprecht H, Gerstner W, Lumenta CB (2003) Neuronavigation combined with electrophysiological monitoring for surgery of lesions in eloquent brain areas in 42 cases: a retrospective comparison of the neurological outcome and the quality of resection with a control group with similar lesions. Minim Invasive Neurosurg 46: 65–71PubMedGoogle Scholar
  116. 116.
    Ricard D, Kaloshi G, Amiel-Benouaich A, Lejeune J, Marie Y, Mandonnet E, Kujas M, Mokhtari K, Taillibert S, Laigle-Donadey F, Carpentier AF, Omuro A, Capelle L, Duffau H, Cornu P, Guillevin R, Sanson M, Hoang-Xuan K, Delattre JY (2007) Dynamic history of low-grade gliomas before and after temozolomide treatment. Ann Neurol 61(5): 484–90PubMedGoogle Scholar
  117. 117.
    Romstock J, Fahlbusch R, Ganslandt O, Nimsky C, Strauss C (2002) Localisation of the sensorimotor cortex during surgery for brain tumours: feasibility and waveform patterns of somatosensory evoked potentials. J Neurol Neurosurg Psychiatry 72: 221–29PubMedGoogle Scholar
  118. 118.
    Rostomily RC, Keles GE, Berger MS (1996) Radical surgery in the management of lowgrade and high-grade gliomas. Baillieres Clin Neurol 5: 345–69PubMedGoogle Scholar
  119. 119.
    Roux FE, Boulanouar K, Ibarrola D, Tremoulet M, Chollet F, Berry I (2000) Functional MRI and intraoperative brain mapping to evaluate brain plasticity in patients with brain tumours and hemiparesis. J Neurol Neurosurg Psychiatry 69: 453–63PubMedGoogle Scholar
  120. 120.
    Roux FE, Tremoulet M (2002) Organization of language areas in bilingual patients: a cortical stimulation study. J Neurosurg 97: 857–64PubMedGoogle Scholar
  121. 121.
    Roux FE, Boulanouar K, Lotterie JA, Mejdoubi M, LeSage JP, Berry I (2003) Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 52: 1335–45PubMedGoogle Scholar
  122. 122.
    Roux FE, Boetto S, Sacko O, Chollet F, Tremoulet M (2003) Writing, calculating, and finger recognition in the region of the angular gyrus: a cortical stimulation study of Gerstmann syndrome. J Neurosurg 99: 716–27PubMedGoogle Scholar
  123. 123.
    Roux FE, Lubrano V, Lauwers-Cances V, Tremoulet M, Mascott CR, Demonet JF (2004) Intra-operative mapping of cortical areas involved in reading in mono-and bilingual patients. Brain 127: 1796–1810PubMedGoogle Scholar
  124. 124.
    Rutten GJ, Ramsey NF, van Rijen PC, Noordmans HJ, van Veelen CW (2002) Development of a functional magnetic resonance imaging protocol for intraoperative localization of critical temporoparietal language areas. Ann Neurol 51: 350–60PubMedGoogle Scholar
  125. 125.
    Rutten GJ, Ramsey N, Noordmans HJ, Willems P, van Rijen P, van der Berkelbach Sprenkel JW, Viergever M, van Veelen C (2003) Toward functional neuronavigation: implementation of functional magnetic resonance imaging data in a surgical guidance system for intraoperative identification of motor and language cortices. Technical note and illustrative case. Neurosurg Focus 15: E6Google Scholar
  126. 126.
    Sanai N, Berger MS (2008) Glioma extent of resection and its impact on patient outcome. Neurosurgery 62(4): 753–64; discussion 264–66 (Review)PubMedGoogle Scholar
  127. 127.
    Sarang A, Dinsmore J (2003) Anesthesia for awake craniotomy — evolution of a technique that facilitates awake neurological testing. Br J Anaesth 90: 161–65PubMedGoogle Scholar
  128. 128.
    Schmidt MH, Berger MS, Lamborn KR, Aldape K, McDermott MW, Prados MD, Chang SM (2003) Repeated operations for infiltrative low-grade gliomas without intervening therapy. Neurosurg 98(6): 1165–69Google Scholar
  129. 129.
    Smith JS, Perry A, Borell TJ, Lee HK, O’Fallon J, Hosek SM, Kimmel D, Yates A, Burger PC, Scheithauer BW, Jenkins RB (2000) Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18: 636–45PubMedGoogle Scholar
  130. 130.
    Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, Tihan T, Vandenberg S, McDermott MW, Berger MS (2008) Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26(8): 1338–45PubMedGoogle Scholar
  131. 131.
    Stupp R, Janzer RC, Hegi ME, Villemure JG, Mirimanoff RO (2003) Prognostic factors for low-grade gliomas. Semin Oncol 30: 23–28PubMedGoogle Scholar
  132. 132.
    Talos IF, Zou KH, Ohno-Machado L, Bhagwat JG, Kikinis R, Black PM, Jolesz FA (2006) Supratentorial low-grade glioma resectability: statistical predictive analysis based on anatomic MR features and tumor characteristics. Radiology 239(2): 506–13PubMedGoogle Scholar
  133. 133.
    Taphoorn MJ (2003) Neurocognitive sequelae in the treatment of low-grade gliomas. Semin Oncol 30: 45–48PubMedGoogle Scholar
  134. 134.
    Van den Bent MJ, Looijenga LH, Langenberg K, Dinjens W, Graveland W, Uytdewilligen L, Sillevis Smitt PA, Jenkins RB, Kros JM (2003) Chromosomal anomalies in oligodendroglial tumors are correlated with clinical features. Cancer 97: 1276–84PubMedGoogle Scholar
  135. 135.
    van Veelen ML, Avezaat CJ, Kros JM, et al. (1998) Supratentorial low grade astrocytoma: prognostic factors, dedifferentiation, and the issue of early versus late surgery. J Neurol Neurosurg Psychiatry 64: 581–87PubMedGoogle Scholar
  136. 136.
    Vlieger EJ, Majoie CB, Leenstra S, den Heeten GJ (2004) Functional magnetic resonance imaging for neurosurgical planning in neurooncology. Eur Radiol 14: 1143–53PubMedGoogle Scholar
  137. 137.
    Whittle IR, Midgley S, Georges H, Pringle AM, Taylor R (2005) Patient perceptions of “awake” brain tumour surgery. Acta Neurochir (Wien) 147: 275–277Google Scholar
  138. 138.
    Yingling CD, Ojemann S, Dodson B, Harrington MJ, Berger MS (1999) Identification of motor pathways during tumor surgery facilitated by multichannel electromyographic recording. J Neurosurg 91: 922–27PubMedGoogle Scholar

Copyright information

© Springer-Verlag/Wien 2010

Authors and Affiliations

  • L. Bello
    • 1
  • E. Fava
    • 1
  • G. Carrabba
    • 1
  • C. Papagno
    • 1
  • S. M. Gaini
    • 1
  1. 1.Neurosurgery, Department of Neurological SciencesUniversità degli Studi di MilanoMilanoItaly

Personalised recommendations