Functional preoperative and intraoperative mapping and monitoring: Increasing safety and efficacy in glioma surgery

Neurosurgical Focus

Volumn 38, Issue 1, 2015, Pages

  Ottenhausen, Malte ^a   Krieg, Sandro M ^a   Meyer, Bernhard ^a   Ringel, Florian ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cortical regions; Direct cortical stimulation; Eloquent; Glioma; Mapping; Monitoring

Indexed keywords

BRAIN NEOPLASMS; DIFFUSION TENSOR IMAGING; GLIOMA; HUMAN; NEURONAVIGATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATIENT MONITORING; PROCEDURES;

BRAIN NEOPLASMS; DIFFUSION TENSOR IMAGING; GLIOMA; HUMANS; MAGNETIC RESONANCE IMAGING; MONITORING, INTRAOPERATIVE; NEURONAVIGATION;

EID: 84937479812     PISSN: None     EISSN: 10920684     Source Type: Journal    
DOI: 10.3171/2014.10.FOCUS14611     Document Type: Article

References (128)

1. Barone DG, Lawrie TA, Hart MG: Image guided surgery for the resection of brain tumours. Cochrane Database Syst Rev 1:CD009685, 2014
2. Bauer MH, Barbieri S, Klein J, Egger J, Kuhnt D, Freisleben B, et al: Boundary estimation of fiber bundles derived from diffusion tensor images. Int J CARS 6:1-11, 2011
3. Beez T, Boge K, Wager M, Whittle I, Fontaine D, Spena G, et al: Tolerance of awake surgery for glioma: a prospective European Low Grade Glioma Network multicenter study. Acta Neurochir (Wien) 155:1301-1308, 2013
4. Bello L, Comi A, Riva M, Pessina F, Alfiero T, Raneri F, et al: Glioma surgery: tailoring intraoperative neurophysiological strategies to clinical conditions enhances resection, extends indications, and keeps patient functional integrity. Neuro Oncol 16 (Suppl 3):iii47, 2014 (Abstract)
5. Bello L, Gambini A, Castellano A, Carrabba G, Acerbi F, Fava E, et al: Motor and language DTI fiber tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 39:369-382, 2008
6. Bello L, Riva M, Fava E, Ferpozzi V, Castellano A, Raneri F, et al: Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving motor pathways. Neuro Oncol 16:1110-1128, 2014
7. Berger MS, Deliganis AV, Dobbins J, Keles GE: The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer 74:1784-1791, 1994
8. Berman JI, Berger MS, Chung SW, Nagarajan SS, Henry RG: Accuracy of diffusion tensor magnetic resonance imaging tractography assessed using intraoperative subcortical stimu- lation mapping and magnetic source imaging. J Neurosurg 107:488-494, 2007
9. Bizzi A, Blasi V, Falini A, Ferroli P, Cadioli M, Danesi U, et al: Presurgical functional MR imaging of language and motor functions: validation with intraoperative electrocortical mapping. Radiology 248:579-589, 2008
10. 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 118:1157-1168, 2013
11. Carrabba G, Fava E, Giussani C, Acerbi F, Portaluri F, Songa V, et al: Cortical and subcortical motor mapping in rolandic and perirolandic glioma surgery: impact on postoperative morbidity and extent of resection. J Neurosurg Sci 51:45-51, 2007
12. Castellano A, Bello L, Michelozzi C, Gallucci M, Fava E, Iadanza A, et al: Role of diffusion tensor magnetic resonance tractography in predicting the extent of resection in glioma surgery. Neuro Oncol 14:192-202, 2012
13. Cedzich C, Taniguchi M, Schäfer S, Schramm J: Somatosensory evoked potential phase reversal and direct motor cortex stimulation during surgery in and around the central region. Neurosurgery 38:962-970, 1996
14. Chang EF, Clark A, Smith JS, Polley MY, Chang SM, Barbaro NM, et al: Functional mapping-guided resection of low-grade gliomas in eloquent areas of the brain: improvement of long-term survival. Clinical article. J Neurosurg 114:566-573, 2011
15. Chen X, Weigel D, Ganslandt O, Fahlbusch R, Buchfelder M, Nimsky C: Diffusion tensor-based fiber tracking and intraoperative neuronavigation for the resection of a brainstem cavernous angioma. Surg Neurol 68:285-291, 2007
16. 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 103:1227-1233, 2005
17. De Benedictis A, Duffau H: Brain hodotopy: from esoteric concept to practical surgical applications. Neurosurgery 68:1709-1723, 2011
18. 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 30:2559-2565, 2012
19. DeAngelis LM: Brain tumors. N Engl J Med 344:114-123, 2001
20. Della Puppa A, De Pellegrin S, d'Avella E, Gioffrè G, Munari M, Saladini M, et al: Right parietal cortex and calculation processing: intraoperative functional mapping of multiplication and addition in patients affected by a brain tumor. J Neurosurg 119:1107-1111, 2013
21. Duffau H: Brain plasticity: from pathophysiological mechanisms to therapeutic applications. J Clin Neurosci 13:885- 897, 2006
22. Duffau H: Cognitive assessment in glioma patients. J Neurosurg 119:1348-1349, 2013 (Letter)
23. Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Taillandier L, 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 98:764-778, 2003
24. Duffau H, Herbet G, Moritz-Gasser S: Toward a pluri-component, multimodal, and dynamic organization of the ventral semantic stream in humans: lessons from stimulation mapping in awake patients. Front Syst Neurosci 7:44, 2013
25. Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, Van Effenterre R, et al: 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 76:845-851, 2005
26. Duffau H, Moritz-Gasser S, Mandonnet E: A re-examination of neural basis of language processing: proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang 131:1-10, 2014
27. Forster MT, Senft C, Hattingen E, Lorei M, Seifert V, Szelényi A: Motor cortex evaluation by nTMS after surgery of central region tumors: a feasibility study. Acta Neurochir (Wien) 154:1351-1359, 2012
28. Frey D, Schilt S, Strack V, Zdunczyk A, Rösler J, Niraula B, et al: Navigated transcranial magnetic stimulation improves the treatment outcome in patients with brain tumors in motor eloquent locations. Neuro Oncol 16:1365-1372, 2014
29. Frey D, Strack V, Wiener E, Jussen D, Vajkoczy P, Picht T: A new approach for corticospinal tract reconstruction based on navigated transcranial stimulation and standardized fractional anisotropy values. Neuroimage 62:1600-1609, 2012
30. Fujiwara N, Sakatani K, Katayama Y, Murata Y, Hoshino T, Fukaya C, et al: Evoked-cerebral blood oxygenation changes in false-negative activations in BOLD contrast functional MRI of patients with brain tumors. Neuroimage 21:1464- 1471, 2004
31. Ganslandt O, Buchfelder M, Hastreiter P, Grummich P, Fahlbusch R, Nimsky C: Magnetic source imaging supports clinical decision making in glioma patients. Clin Neurol Neurosurg 107:20-26, 2004
32. Giussani C, Roux FE, Ojemann J, Sganzerla EP, Pirillo D, Papagno C: Is preoperative functional magnetic resonance imaging reliable for language areas mapping in brain tumor surgery? Review of language functional magnetic resonance imaging and direct cortical stimulation correlation studies. Neurosurgery 66:113-120, 2010
33. Haglund MM, Berger MS, Shamseldin M, Lettich E, Ojemann GA: Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34:567-576, 1994
34. Henning Stieglitz L, Seidel K, Wiest R, Beck J, Raabe A: Localization of primary language areas by arcuate fascicle fiber tracking. Neurosurgery 70:56-65, 2012
35. Ius T, Angelini E, Thiebaut de Schotten M, Mandonnet E, Duffau H: Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a "minimal common brain." Neuroimage 56:992-1000, 2011
36. Jack CR Jr, Thompson RM, Butts RK, Sharbrough FW, Kelly PJ, Hanson DP, et al: Sensory motor cortex: correlation of presurgical mapping with functional MR imaging and invasive cortical mapping. Radiology 190:85-92, 1994
37. Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, Unsgård G, et al: Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in lowgrade gliomas. JAMA 308:1881-1888, 2012
38. Jakola AS, Unsgård G, Myrmel KS, Kloster R, Torp SH, Lindal S, et al: Low grade gliomas in eloquent locations - implications for surgical strategy, survival and long term quality of life. PLoS ONE 7:e51450, 2012
39. Kawashima A, Krieg SM, Faust K, Schneider H, Vajkoczy P, Picht T: Plastic reshaping of cortical language areas evaluated by navigated transcranial magnetic stimulation in a surgical case of glioblastoma multiforme. Clin Neurol Neurosurg 115:2226-2229, 2013
40. Keles GE, Lamborn KR, Berger MS: Low-grade hemispheric gliomas in adults: a critical review of extent of resection as a factor influencing outcome. J Neurosurg 95:735-745, 2001
41. Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS: 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 100:369-375, 2004
42. Kirsch HE, Zhu Z, Honma S, Findlay A, Berger MS, Nagarajan SS: Predicting the location of mouth motor cortex in patients with brain tumors by using somatosensory evoked field measurements. J Neurosurg 107:481-487, 2007
43. Kombos T, Picht T, Derdilopoulos A, Suess O: Impact of intraoperative neurophysiological monitoring on surgery of high-grade gliomas. J Clin Neurophysiol 26:422-425, 2009
44. Kombos T, Suess O, Ciklatekerlio O, Brock M: Monitoring of intraoperative motor evoked potentials to increase the safety of surgery in and around the motor cortex. J Neurosurg 95:608-614, 2001
45. Korvenoja A, Kirveskari E, Aronen HJ, Avikainen S, Brander A, Huttunen J, et al: Sensorimotor cortex localization: comparison of magnetoencephalography, functional MR imaging, and intraoperative cortical mapping. Radiology 241:213-222, 2006
46. Krieg SM, Buchmann NH, Gempt J, Shiban E, Meyer B, Ringel F: Diffusion tensor imaging fiber tracking using navigated brain stimulation-a feasibility study. Acta Neurochir (Wien) 154:555-563, 2012
47. Krieg SM, Sabih J, Bulubasova L, Obermueller T, Negwer C, Janssen I, et al: Preoperative motor mapping by navigated transcranial magnetic brain stimulation improves outcome for motor eloquent lesions. Neuro Oncol 16:1274-1282, 2014
48. Krieg SM, Schäffner M, Shiban E, Droese D, Obermüller T, Gempt J, et al: Reliability of intraoperative neurophysiological monitoring using motor evoked potentials during resection of metastases in motor-eloquent brain regions. Clinical article. J Neurosurg 118:1269-1278, 2013
49. Krieg SM, Schnurbus L, Shiban E, Droese D, Obermueller T, Buchmann N, et al: Surgery of highly eloquent gliomas primarily assessed as non-resectable: risks and benefits in a cohort study. BMC Cancer 13:51, 2013
50. Krieg SM, Shiban E, Buchmann N, Gempt J, Foerschler A, Meyer B, et al: Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. J Neurosurg 116:994-1001, 2012
51. Krieg SM, Shiban E, Buchmann N, Meyer B, Ringel F: Presurgical navigated transcranial magnetic brain stimulation for recurrent gliomas in motor eloquent areas. Clin Neurophysiol 124:522-527, 2013
52. Krieg SM, Shiban E, Droese D, Gempt J, Buchmann N, Pape H, et al: Predictive value and safety of intraoperative neurophysiological monitoring with motor evoked potentials in glioma surgery. Neurosurgery 70:1060-1071, 2012
53. Krieg SM, Sollmann N, Hauck T, Ille S, Foerschler A, Meyer B, et al: Functional language shift to the right hemisphere in patients with language-eloquent brain tumors. PLoS ONE 8:e75403, 2013
54. Krieg SM, Sollmann N, Hauck T, Ille S, Meyer B, Ringel F: Repeated mapping of cortical language sites by preoperative navigated transcranial magnetic stimulation compared to repeated intraoperative DCS mapping in awake craniotomy. BMC Neurosci 15:20, 2014
55. Krieg SM, Tarapore PE, Picht T, Tanigawa N, Houde J, Sollmann N, et al: Optimal timing of pulse onset for language mapping with navigated repetitive transcranial magnetic stimulation. Neuroimage 100:219-236, 2014
56. Krings T, Schreckenberger M, Rohde V, Spetzger U, Sabri O, Reinges MH, et al: Functional MRI and 18F FDG-positron emission tomography for presurgical planning: comparison with electrical cortical stimulation. Acta Neurochir (Wien) 144:889-899, 2002
57. Kuhnt D, Bauer MH, Becker A, Merhof D, Zolal A, Richter M, et al: Intraoperative visualization of fiber tracking based reconstruction of language pathways in glioma surgery. Neurosurgery 70:911-920, 2012
58. Leclercq D, Duffau H, Delmaire C, Capelle L, Gatignol P, Ducros M, et al: Comparison of diffusion tensor imaging tractography of language tracts and intraoperative subcortical stimulations. J Neurosurg 112:503-511, 2010
59. Lefaucheur JP: Transcranial magnetic stimulation in the management of pain. Suppl Clin Neurophysiol 57:737-748, 2004
60. Lefaucheur JP, Drouot X, Ménard-Lefaucheur I, Nguyen JP: Neuropathic pain controlled for more than a year by monthly sessions of repetitive transcranial magnetic stimulation of the motor cortex. Neurophysiol Clin 34:91-95, 2004
61. Liégeois F, Cross JH, Gadian DG, Connelly A: Role of fMRI in the decision-making process: epilepsy surgery for children. J Magn Reson Imaging 23:933-940, 2006
62. Lurito JT, Lowe MJ, Sartorius C, Mathews VP: Comparison of fMRI and intraoperative direct cortical stimulation in localization of receptive language areas. J Comput Assist Tomogr 24:99-105, 2000
63. Mäkelä JP, Forss N, Jääskeläinen J, Kirveskari E, Korvenoja A, Paetau R: Magnetoencephalography in neurosurgery. Neurosurgery 61 (1 Suppl):147-165, 2007
64. Mikuni N, Okada T, Enatsu R, Miki Y, Hanakawa T, Urayama S, et al: Clinical impact of integrated functional neuronavigation and subcortical electrical stimulation to preserve motor function during resection of brain tumors. J Neurosurg 106:593-598, 2007
65. Nagarajan S, Kirsch H, Lin P, Findlay A, Honma S, Berger MS: Preoperative localization of hand motor cortex by adaptive spatial filtering of magnetoencephalography data. J Neurosurg 109:228-237, 2008
66. Neuloh G, Bien CG, Clusmann H, von Lehe M, Schramm J: Continuous motor monitoring enhances functional preservation and seizure-free outcome in surgery for intractable focal epilepsy. Acta Neurochir (Wien) 152:1307-1314, 2010
67. Neuloh G, Pechstein U, Cedzich C, Schramm J: Motor evoked potential monitoring with supratentorial surgery. Neurosurgery 54:1061-1072, 2004
68. Neuloh G, Pechstein U, Cedzich C, Schramm J: Motor evoked potential monitoring with supratentorial surgery. Neurosurgery 61 (1 Suppl):337-348, 2007
69. Neuloh G, Pechstein U, Schramm J: Motor tract monitoring during insular glioma surgery. J Neurosurg 106:582-592, 2007
70. Neuloh G, Schramm J: Are there false-negative results of motor evoked potential monitoring in brain surgery? Cent Eur Neurosurg 70:171-175, 2009
71. Neuloh G, Schramm J: Motor evoked potential monitoring for the surgery of brain tumours and vascular malformations. Adv Tech Stand Neurosurg 29:171-228, 2004
72. Neuloh G, Simon M, Schramm J: Stroke prevention during surgery for deep-seated gliomas. Neurophysiol Clin 37:383- 389, 2007
73. Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, et al: Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 56:130-138, 2005
74. Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, et al: Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 61 (1 Suppl):178-186, 2007
75. Nimsky C, Ganslandt O, Merhof D, Sorensen AG, Fahlbusch R: Intraoperative visualization of the pyramidal tract by diffusion-tensor-imaging-based fiber tracking. Neuroimage 30:1219-1229, 2006
76. Nossek E, Korn A, Shahar T, Kanner AA, Yaffe H, Marcovici D, et al: Intraoperative mapping and monitoring of the corticospinal tracts with neurophysiological assessment and 3-dimensional ultrasonography-based navigation. Clinical article. J Neurosurg 114:738-746, 2011
77. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, et al: Intrinsic signal changes accompanying sen- sory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci U S A 89:5951- 5955, 1992
78. Ohue S, Kohno S, Inoue A, Yamashita D, Harada H, Kumon Y, et al: Accuracy of diffusion tensor magnetic resonance imaging-based tractography for surgery of gliomas near the pyramidal tract: a significant correlation between subcortical electrical stimulation and postoperative tractography. Neurosurgery 70:283-294, 2012
79. 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 71:316-326, 1989
80. Ojemann GA, Whitaker HA: Language localization and variability. Brain Lang 6:239-260, 1978
81. Ostrỳ S, Belšan T, Otáhal J, Beneš V, Netuka D: Is intraoperative diffusion tensor imaging at 3.0T comparable to subcortical corticospinal tract mapping? Neurosurgery 73:797-807, 2013
82. Ottenhausen M, Bodhinayake I, Banu M, Kesavabhotla K, Ray A, Boockvar JA: Industry progress report on neurooncology: Biotech update 2013. J Neurooncol 115:311-316, 2013
83. Ozawa N, Muragaki Y, Nakamura R, Hori T, Iseki H: Shift of the pyramidal tract during resection of the intraaxial brain tumors estimated by intraoperative diffusion-weighted imaging. Neurol Med Chir (Tokyo) 49:51-56, 2009
84. Papanicolaou AC, Simos PG, Breier JI, Zouridakis G, Willmore LJ, Wheless JW, et al: Magnetoencephalographic mapping of the language-specific cortex. J Neurosurg 90:85-93, 1999
85. Picht T, Krieg SM, Sollmann N, Rösler J, Niraula B, Neuvonen T, et al: A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery 72:808-819, 2013
86. Picht T, Schulz J, Hanna M, Schmidt S, Suess O, Vajkoczy P: Assessment of the influence of navigated transcranial magnetic stimulation on surgical planning for tumors in or near the motor cortex. Neurosurgery 70:1248-1257, 2012
87. Post A, Keck ME: Transcranial magnetic stimulation as a therapeutic tool in psychiatry: what do we know about the neurobiological mechanisms? J Psychiatr Res 35:193-215, 2001
88. Prabhu SS, Gasco J, Tummala S, Weinberg JS, Rao G: Intraoperative magnetic resonance imaging-guided tractography with integrated monopolar subcortical functional mapping for resection of brain tumors. Clinical article. J Neurosurg 114:719-726, 2011
89. 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 120:1015-1024, 2014
90. Robles SG, Gatignol P, Lehéricy S, Duffau H: Long-term brain plasticity allowing a multistage surgical approach to World Health Organization Grade II gliomas in eloquent areas. J Neurosurg 109:615-624, 2008
91. Rösler J, Niraula B, Strack V, Zdunczyk A, Schilt S, Savolainen P, et al: Language mapping in healthy volunteers and brain tumor patients with a novel navigated TMS system: evidence of tumor-induced plasticity. Clin Neurophysiol 125:526-536, 2014
92. Rossi S, Rossini PM: TMS in cognitive plasticity and the potential for rehabilitation. Trends Cogn Sci 8:273-279, 2004
93. Roux FE, Boulanouar K, Lotterie JA, Mejdoubi M, LeSage JP, Berry I: Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 52:1335- 1347, 2003
94. Roux FE, Boulanouar K, Ranjeva JP, Tremoulet M, Henry P, Manelfe C, et al: Usefulness of motor functional MRI correlated to cortical mapping in Rolandic low-grade astrocytomas. Acta Neurochir (Wien) 141:71-79, 1999
95. Sanai N, Berger MS: Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:753-764, 264-266, 2008
96. Sanai N, Berger MS: Intraoperative stimulation techniques for functional pathway preservation and glioma resection. Neurosurg Focus 28(2):E1, 2010
97. Sanai N, Mirzadeh Z, Berger MS: Functional outcome after language mapping for glioma resection. N Engl J Med 358:18-27, 2008
98. Satoer D, Vork J, Visch-Brink E, Smits M, Dirven C, Vincent A: Cognitive functioning early after surgery of gliomas in eloquent areas. J Neurosurg 117:831-838, 2012
99. Schiffbauer H, Berger MS, Ferrari P, Freudenstein D, Rowley HA, Roberts TP: Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. J Neurosurg 97:1333-1342, 2002
100. Schiffbauer H, Ferrari P, Rowley HA, Berger MS, Roberts TP: Functional activity within brain tumors: a magnetic source imaging study. Neurosurgery 49:1313-1321, 2001
101. Seidel K, Beck J, Stieglitz L, Schucht P, Raabe A: The warning-sign hierarchy between quantitative subcortical motor mapping and continuous motor evoked potential monitoring during resection of supratentorial brain tumors. J Neurosurg 118:287-296, 2013
102. Simos PG, Papanicolaou AC, Breier JI, Wheless JW, Constantinou JE, Gormley WB, et al: Localization of language- specific cortex by using magnetic source imaging and electrical stimulation mapping. J Neurosurg 91:787-796, 1999
103. 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 26:1338-1345, 2008
104. Sollmann N, Hauck T, Obermüller T, Hapfelmeier A, Meyer B, Ringel F, et al: Inter- and intraobserver variability in motor mapping of the hotspot for the abductor policis brevis muscle. BMC Neurosci 14:94, 2013
105. Stadlbauer A, Nimsky C, Buslei R, Salomonowitz E, Hammen T, Buchfelder M, et al: Diffusion tensor imaging and optimized fiber tracking in glioma patients: histopathologic evaluation of tumor-invaded white matter structures. Neuroimage 34:949-956, 2007
106. Stadlbauer A, Nimsky C, Gruber S, Moser E, Hammen T, Engelhorn T, et al: Changes in fiber integrity, diffusivity, and metabolism of the pyramidal tract adjacent to gliomas: a quantitative diffusion tensor fiber tracking and MR spectroscopic imaging study. AJNR Am J Neuroradiol 28:462-469, 2007
107. 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 62:564-576, 2008
108. Suess O, Suess S, Brock M, Kombos T: Intraoperative electrocortical stimulation of Brodman area 4: a 10-year analysis of 255 cases. Head Face Med 2:20, 2006
109. Szelényi A, Langer D, Beck J, Raabe A, Flamm ES, Seifert V, et al: Transcranial and direct cortical stimulation for motor evoked potential monitoring in intracerebral aneurysm surgery. Neurophysiol Clin 37:391-398, 2007
110. Szelényi A, Langer D, Kothbauer K, De Camargo AB, Flamm ES, Deletis V: Monitoring of muscle motor evoked potentials during cerebral aneurysm surgery: intraoperative changes and postoperative outcome. J Neurosurg 105:675- 681, 2006
111. Szelényi A, Senft C, Jardan M, Forster MT, Franz K, Seifert V, et al: Intra-operative subcortical electrical stimulation: a comparison of two methods. Clin Neurophysiol 122:1470- 1475, 2011
112. Takahashi S, Vajkoczy P, Picht T: Navigated transcranial magnetic stimulation for mapping the motor cortex in patients with rolandic brain tumors. Neurosurg Focus 34(4):E3, 2013
113. Talacchi A, Santini B, Casartelli M, Monti A, Capasso R, Miceli G: Awake surgery between art and science. Part II: language and cognitive mapping. Funct Neurol 28:223- 239, 2013
114. Talacchi A, Santini B, Savazzi S, Gerosa M: Cognitive effects of tumour and surgical treatment in glioma patients. J Neurooncol 103:541-549, 2011
115. Taniguchi M, Cedzich C, Schramm J: Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description. Neurosurgery 32:219- 226, 1993
116. 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 71:1012-1022, 2012
117. Tarapore PE, Tate MC, Findlay AM, Honma SM, Mizuiri D, Berger MS, et al: Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. J Neurosurg 117:354-362, 2012
118. Tassinari CA, Cincotta M, Zaccara G, Michelucci R: Transcranial magnetic stimulation and epilepsy. Clin Neurophysiol 114:777-798, 2003
119. Tergau F, Naumann U, Paulus W, Steinhoff BJ: Lowfrequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 353:2209, 1999
120. Tomczak RJ, Wunderlich AP, Wang Y, Braun V, Antoniadis G, Görich J, et al: fMRI for preoperative neurosurgical mapping of motor cortex and language in a clinical setting. J Comput Assist Tomogr 24:927-934, 2000
121. Ulmer JL, Hacein-Bey L, Mathews VP, Mueller WM, DeYoe EA, Prost RW, et al: Lesion-induced pseudodominance at functional magnetic resonance imaging: implications for preoperative assessments. Neurosurgery 55:569-581, 2004
122. Vigneau M, Beaucousin V, Hervé PY, Duffau H, Crivello F, Houdé O, et al: Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30:1414-1432, 2006
123. Wen PY, Kesari S: Malignant gliomas in adults. N Engl J Med 359:492-507, 2008
124. Wu AS, Witgert ME, Lang FF, Xiao L, Bekele BN, Meyers CA, et al: Neurocognitive function before and after surgery for insular gliomas. J Neurosurg 115:1115-1125, 2011
125. Wu JS, Zhou LF, Tang WJ, Mao Y, Hu J, Song YY, et al: Clinical evaluation and follow-up outcome of diffusion tensor imaging-based functional neuronavigation: a prospective, controlled study in patients with gliomas involving pyramidal tracts. Neurosurgery 61:935-949, 2007
126. Yetkin FZ, Mueller WM, Morris GL, McAuliffe TL, Ulmer JL, Cox RW, et al: Functional MR activation correlated with intraoperative cortical mapping. AJNR Am J Neuroradiol 18:1311-1315, 1997
127. Zhu FP, Wu JS, Song YY, Yao CJ, Zhuang DX, Xu G, et al: Clinical application of motor pathway mapping using diffusion tensor imaging tractography and intraoperative direct subcortical stimulation in cerebral glioma surgery: a prospective cohort study. Neurosurgery 71:1170-1184, 2012
128. Zolal A, Hejcl A, Vachata P, Bartoš R, Humhej I, Malucelli A, et al: The use of diffusion tensor images of the corticospinal tract in intrinsic brain tumor surgery: a comparison with direct subcortical stimulation. Neurosurgery 71:331- 340, 2012