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European Radiology

, Volume 19, Issue 10, pp 2523–2534 | Cite as

Preoperative fMRI in tumour surgery

  • Ann TielemanEmail author
  • Karel Deblaere
  • Dirk Van Roost
  • Olivier Van Damme
  • Eric Achten
Neuro

Abstract

Minimally invasive resection of brain tumours aims at removing as much pathological tissue as possible while preserving essential brain functions. Therefore, the precise spatial relationship between the lesion and adjacent functionally essential brain parenchyma needs to be known. Functional magnetic resonance imaging (fMRI) is increasingly being used for this purpose because of its non-invasiveness, its relatively high spatial resolution and the preoperative availability of the results. In this review, the goals of fMRI at various key points during the management of patients with a brain tumour are discussed. Further, several practical aspects associated with fMRI for motor and language functioning are summarised, and the validation of the fMRI results with standard invasive mapping techniques is addressed. Next, several important pitfalls and limitations that warrant careful interpretations of the fMRI results are highlighted. Finally, two important future perspectives of presurgical fMRI are emphasised.

Keywords

Functional MRI Presurgical planning Motor cortex Language cortex 

References

  1. 1.
    Ojemann JG, Ojemann GA, Lettich E (2002) Cortical stimulation mapping of language cortex by using a verb generation task: effects of learning and comparison to mapping based on object naming. J Neurosurg 97:33–38PubMedCrossRefGoogle Scholar
  2. 2.
    Desmond JE, Sum JM, Wagner AD, Demb JB, Shear PK, Glover GH et al (1995) Functional MRI measurement of language lateralization in Wada-tested patients. Brain 118:1411–1419PubMedCrossRefGoogle Scholar
  3. 3.
    Hund-Georgiadis M, Lex U, Friederici AD, von Cramon DY (2002) Non-invasive regime for language lateralization in right- and left-handers by means of functional MRI and dichotic listening. Exp Brain Res 145:166–176PubMedCrossRefGoogle Scholar
  4. 4.
    Atlas SW, Howard RS 2nd, Maldjian J, Alsop D, Detre JA, Listerud J et al (1996) Functional magnetic resonance imaging of regional brain activity in patients with intracerebral gliomas: findings and implications for clinical management. Neurosurgery 38:329–338PubMedCrossRefGoogle Scholar
  5. 5.
    FitzGerald DB, Cosgrove GR, Ronner S, Jiang H, Buchbinder BR, Belliveau JW et al (1997) Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. AJNR 18:1529–1539PubMedGoogle Scholar
  6. 6.
    Lehericy S, Duffau H, Cornu P, Capelle L, Pidoux B, Carpentier A et al (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 92:589–598PubMedCrossRefGoogle Scholar
  7. 7.
    Jack CRJ, Thompson RM, Butts RK, Sharbrough FW, Kelly PJ, Hanson DP et al (1994) Sensory motor cortex: correlation of presurgical mapping with functional MR imaging and invasive cortical mapping. Radiology 190:85–92PubMedGoogle Scholar
  8. 8.
    Binder JR, Swanson SJ, Hammeke TA, Morris GL, Mueller WM, Fischer M et al (1996) Determination of language dominance using functional MRI: a comparison with the Wada test. Neurology 46:978–984PubMedGoogle Scholar
  9. 9.
    Deblaere K, Boon PA, Vandemaele P, Tieleman A, Vonck K, Vingerhoets G et al (2004) MRI language dominance assessment in epilepsy patients at 1.0 T: region of interest analysis and comparison with intracarotid amytal testing. Neuroradiology 46:413–420PubMedCrossRefGoogle Scholar
  10. 10.
    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. AJNR 21:1415–1422PubMedGoogle Scholar
  11. 11.
    Petrella JR, Shah LM, Harris KM, Friedman AH, George TM, Sampson JH et al (2006) Preoperative functional MR imaging localization of language and motor areas: effect on therapeutic decision making in patients with potentially resectable brain tumors. Radiology 240:793–802PubMedCrossRefGoogle Scholar
  12. 12.
    Ulmer JL, Krouwer HG, Mueller WM, Ugurel MS, Kocak M, Mark LP (2003) Pseudo-reorganization of language cortical function at fMR imaging: a consequence of tumor-induced neurovascular uncoupling. AJNR 24:213–217PubMedGoogle Scholar
  13. 13.
    Schreiber A, Hubbe U, Ziyeh S, Hennig J (2000) The influence of gliomas and nonglial space-occupying lesions on blood-oxygen-level-dependent contrast enhancement. AJNR 21:1055–1063PubMedGoogle Scholar
  14. 14.
    Lee CC, Ward HA, Sharbrough FW, Meyer FB, Marsh WR, Raffel C et al (1999) Assessment of functional MR imaging in neurosurgical planning. AJNR 20:1511–1519PubMedGoogle Scholar
  15. 15.
    Haberg A, Kvistad KA, Unsgard G, Haraldseth O (2004) Preoperative blood oxygen level-dependent functional magnetic resonance imaging in patients with primary brain tumors: clinical application and outcome. Neurosurgery 54:902–914, discussion 914–5PubMedCrossRefGoogle Scholar
  16. 16.
    Krishnan R, Raabe A, Hattingen E, Szelenyi A, Yahya H, Hermann E et al (2004) Functional magnetic resonance imaging-integrated neuronavigation: correlation between lesion-to-motor cortex distance and outcome. Neurosurgery 55:904–914, discussion 914–5PubMedCrossRefGoogle Scholar
  17. 17.
    Stippich C, Hofmann R, Kapfer D, Hempel E, Heiland S, Jansen O et al (1999) Somatotopic mapping of the human primary somatosensory cortex by fully automated tactile stimulation using functional magnetic resonance imaging. Neurosci Lett 277:25–28PubMedCrossRefGoogle Scholar
  18. 18.
    Desmond JE, Annabel Chen SH (2002) Ethical issues in the clinical application of fMRI: factors affecting the validity and interpretation of activations. Brain Cogn 50:482–497PubMedCrossRefGoogle Scholar
  19. 19.
    Nelson L, Lapsiwala S, Haughton VM, Noyes J, Sadrzadeh AH, Moritz CH et al (2002) Preoperative mapping of the supplementary motor area in patients harboring tumors in the medial frontal lobe. J Neurosurg 97:1108–1114PubMedCrossRefGoogle Scholar
  20. 20.
    Zentner J, Hufnagel A, Pechstein U, Wolf HK, Schramm J (1996) Functional results after resective procedures involving the supplementary motor area. J Neurosurg 85:542–549PubMedCrossRefGoogle Scholar
  21. 21.
    Krainik A, Lehericy S, Duffau H, Capelle L, Chainay H, Cornu P et al (2003) Postoperative speech disorder after medial frontal surgery: role of the supplementary motor area. Neurology 60:587–594PubMedGoogle Scholar
  22. 22.
    O’Shea JP, Whalen S, Branco DM, Petrovich NM, Knierim KE, Golby AJ (2006) Integrated image- and function-guided surgery in eloquent cortex: a technique report. Int J Med Robot 2:75–83PubMedGoogle Scholar
  23. 23.
    Jannin P, Fleig OJ, Seigneuret E, Grova C, Morandi X, Scarabin JM (2000) A data fusion environment for multimodal and multi-informational neuronavigation. Comput Aided Surg 5:1–10PubMedCrossRefGoogle Scholar
  24. 24.
    Rasmussen IAJ, Lindseth F, Rygh OM, Berntsen EM, Selbekk T, Xu J et al (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) 149:365–378CrossRefGoogle Scholar
  25. 25.
    Turner R, Le Bihan D, Moonen CT, Despres D, Frank J (1991) Echo-planar time course MRI of cat brain oxygenation changes. Magn Reson Med 22:159–166PubMedCrossRefGoogle Scholar
  26. 26.
    Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 87:9868–9872PubMedCrossRefGoogle Scholar
  27. 27.
    Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS (1992) Time course EPI of human brain function during task activation. Magn Reson Med 25:390–397PubMedCrossRefGoogle Scholar
  28. 28.
    Fujiwara N, Sakatani K, Katayama Y, Murata Y, Hoshino T, Fukaya C et al (2004) Evoked-cerebral blood oxygenation changes in false-negative activations in BOLD contrast functional MRI of patients with brain tumors. Neuroimage 21:1464–1471PubMedCrossRefGoogle Scholar
  29. 29.
    Leybaert L (2005) Neurobarrier coupling in the brain: a partner of neurovascular and neurometabolic coupling? J Cereb Blood Flow Metab 25:2–16PubMedCrossRefGoogle Scholar
  30. 30.
    Alkadhi H, Kollias SS, Crelier GR, Golay X, Hepp-Reymond MC, Valavanis A (2000) Plasticity of the human motor cortex in patients with arteriovenous malformations: a functional MR imaging study. AJNR 21:1423–1433PubMedGoogle Scholar
  31. 31.
    Rizzolatti G, Luppino G, Matelli M (1998) The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol 106:283–296PubMedCrossRefGoogle Scholar
  32. 32.
    Penfield W, Rasmussen T (1950) The cerebral cortex of man. MacMillan, New YorkGoogle Scholar
  33. 33.
    Tieleman A, Seurinck R, Deblaere K, Vandemaele P, Vingerhoets G, Achten E (2005) Stimulus pacing affects the activation of the medial temporal lobe during a semantic classification task: an fMRI study. Neuroimage 26:565–572PubMedCrossRefGoogle Scholar
  34. 34.
    Papke K, Reimer P, Renger B, Schuierer G, Knecht S, Schulz M et al (2000) Optimized activation of the primary sensorimotor cortex for clinical functional MR imaging. AJNR 21:395–401PubMedGoogle Scholar
  35. 35.
    Golaszewski SM, Siedentopf CM, Koppelstaetter F, Fend M, Ischebeck A, Gonzalez-Felipe V et al (2006) Human brain structures related to plantar vibrotactile stimulation: a functional magnetic resonance imaging study. Neuroimage 29:923–929PubMedCrossRefGoogle Scholar
  36. 36.
    Gasser TG, Sandalcioglu EI, Wiedemayer H, Hans V, Gizewski E, Forsting M et al (2004) A novel passive functional MRI paradigm for preoperative identification of the somatosensory cortex. Neurosurg Rev 27:106–112PubMedCrossRefGoogle Scholar
  37. 37.
    Stippich C, Ochmann H, Sartor K (2002) Somatotopic mapping of the human primary sensorimotor cortex during motor imagery and motor execution by functional magnetic resonance imaging. Neurosci Lett 331:50–54PubMedCrossRefGoogle Scholar
  38. 38.
    Yetkin FZ, Mueller WM, Morris GL, McAuliffe TL, Ulmer JL, Cox RW et al (1997) Functional MR activation correlated with intraoperative cortical mapping. AJNR 18:1311–1315PubMedGoogle Scholar
  39. 39.
    Dymarkowski S, Sunaert S, Van Oostende S, Van Hecke P, Wilms G, Demaerel P et al (1998) Functional MRI of the brain: localisation of eloquent cortex in focal brain lesion therapy. Eur Radiol 8:1573–1580PubMedCrossRefGoogle Scholar
  40. 40.
    Achten E, Jackson GD, Cameron JA, Abbott DF, Stella DL, Fabinyi GC (1999) Presurgical evaluation of the motor hand area with functional MR imaging in patients with tumors and dysplastic lesions. Radiology 210:529–538PubMedGoogle Scholar
  41. 41.
    Hirsch J, Ruge MI, Kim KH, Correa DD, Victor JD, Relkin NR et al (2000) An integrated functional magnetic resonance imaging procedure for preoperative mapping of cortical areas associated with tactile, motor, language, and visual functions. Neurosurgery 47:711–721, discussion 721–2PubMedCrossRefGoogle Scholar
  42. 42.
    Roessler K, Donat M, Lanzenberger R, Novak K, Geissler A, Gartus A et al (2005) Evaluation of preoperative high magnetic field motor functional MRI (3 Tesla) in glioma patients by navigated electrocortical stimulation and postoperative outcome. J Neurol Neurosurg Psychiatry 76:1152–1157PubMedCrossRefGoogle Scholar
  43. 43.
    Naidich TP, Hof PR, Gannon PJ, Yousry TA, Yousry (2001) Anatomic substrates of language: emphasizing speech. Neuroimaging Clin N Am 11:305–341PubMedGoogle Scholar
  44. 44.
    Noppeney U, Josephs O, Hocking J, Price CJ, Friston KJ (2008) The effect of prior visual information on recognition of speech and sounds. Cereb Cortex 18:598–609PubMedCrossRefGoogle Scholar
  45. 45.
    Lurito JT, Dzemidzic M (2001) Determination of cerebral hemisphere language dominance with functional magnetic resonance imaging. Neuroimaging Clin N Am 11:355–363PubMedGoogle Scholar
  46. 46.
    Rutten GJ, van Rijen PC, van Veelen CW, Ramsey NF (1999) Language area localization with three-dimensional functional magnetic resonance imaging matches intrasulcal electrostimulation in Broca’s area. Ann Neurol 46:405–408PubMedCrossRefGoogle Scholar
  47. 47.
    Majos A, Tybor K, Stefanczyk L, Goraj B (2005) Cortical mapping by functional magnetic resonance imaging in patients with brain tumors. Eur Radiol 15:1148–1158PubMedCrossRefGoogle Scholar
  48. 48.
    Deblaere K, Backes WH, Hofman P, Vandemaele P, Boon PA, Vonck K et al (2002) Developing a comprehensive presurgical functional MRI protocol for patients with intractable temporal lobe epilepsy: a pilot study. Neuroradiology 44:667–673PubMedCrossRefGoogle Scholar
  49. 49.
    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 52:1335–1345, discussion 1345–7PubMedCrossRefGoogle Scholar
  50. 50.
    Mueller WM, Yetkin FZ, Hammeke TA, Morris GL 3rd, Swanson SJ, Reichert K et al (1996) Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors. Neurosurgery 39:515–520, discussion 520–1PubMedCrossRefGoogle Scholar
  51. 51.
    Benson RR, FitzGerald DB, LeSueur LL, Kennedy DN, Kwong KK, Buchbinder BR et al (1999) Language dominance determined by whole brain functional MRI in patients with brain lesions. Neurology 52:798–809PubMedGoogle Scholar
  52. 52.
    Fernandez G, Specht K, Weis S, Tendolkar I, Reuber M, Fell J et al (2003) Intrasubject reproducibility of presurgical language lateralization and mapping using fMRI. Neurology 60:969–975PubMedGoogle Scholar
  53. 53.
    Amunts K, Schleicher A, Burgel U, Mohlberg H, Uylings HB, Zilles K (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412:319–341PubMedCrossRefGoogle Scholar
  54. 54.
    Amunts K, Weiss PH, Mohlberg H, Pieperhoff P, Eickhoff S, Gurd JM et al (2004) Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space–the roles of Brodmann areas 44 and 45. Neuroimage 22:42–56PubMedCrossRefGoogle Scholar
  55. 55.
    Price CJ (2000) The anatomy of language: contributions from functional neuroimaging. J Anat 197:335–359PubMedCrossRefGoogle Scholar
  56. 56.
    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 51:350–360PubMedCrossRefGoogle Scholar
  57. 57.
    Rutten GJ, Ramsey NF, van Rijen PC, van Veelen CW (2002) Reproducibility of fMRI-determined language lateralization in individual subjects. Brain Lang 80:421–437PubMedCrossRefGoogle Scholar
  58. 58.
    Abduljalil AM, Kangarlu A, Yu Y, Robitaille PM (1999) Macroscopic susceptibility in ultra high field MRI. II: Acquisition of spin echo images from the human head. J Comput Assist Tomogr 23:842–844PubMedCrossRefGoogle Scholar
  59. 59.
    Hou BL, Bradbury M, Peck KK, Petrovich NM, Gutin PH, Holodny AI (2006) Effect of brain tumor neovasculature defined by rCBV on BOLD fMRI activation volume in the primary motor cortex. Neuroimage 32:489–497PubMedCrossRefGoogle Scholar
  60. 60.
    Sunaert S (2006) Presurgical planning for tumor resectioning. J Magn Reson Imaging 23:887–905PubMedCrossRefGoogle Scholar
  61. 61.
    O’Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F, Kobal G et al (2000) Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. Neuroreport 11:893–897PubMedCrossRefGoogle Scholar
  62. 62.
    Hajnal JV, Myers R, Oatridge A, Schwieso JE, Young IR, Bydder GM (1994) Artifacts due to stimulus correlated motion in functional imaging of the brain. Magn Reson Med 31:283–291PubMedCrossRefGoogle Scholar
  63. 63.
    Krings T, Reinges MH, Erberich S, Kemeny S, Rohde V, Spetzger U et al (2001) Functional MRI for presurgical planning: problems, artefacts, and solution strategies. J Neurol Neurosurg Psychiatr 70:749–760PubMedCrossRefGoogle Scholar
  64. 64.
    Devlin JT, Russell RP, Davis MH, Price CJ, Wilson J, Moss HE et al (2000) Susceptibility-induced loss of signal: comparing PET and fMRI on a semantic task. Neuroimage 11:589–600PubMedCrossRefGoogle Scholar
  65. 65.
    Kim MJ, Holodny AI, Hou BL, Peck KK, Moskowitz CS, Bogomolny DL et al (2005) The effect of prior surgery on blood oxygen level-dependent functional MR imaging in the preoperative assessment of brain tumors. AJNR 26:1980–1985PubMedGoogle Scholar
  66. 66.
    Ugurbil K, Hu X, Chen W, Zhu XH, Kim SG, Georgopoulos (1999) A functional mapping in the human brain using high magnetic fields. Philos Trans R Soc Lond B Biol Sci 354:1195–1213PubMedCrossRefGoogle Scholar
  67. 67.
    Kruger G, Kastrup A, Glover GH (2001) Neuroimaging at 1.5 T and 3.0 T: comparison of oxygenation-sensitive magnetic resonance imaging. Magn Reson Med 45:595–604PubMedCrossRefGoogle Scholar
  68. 68.
    Krasnow B, Tamm L, Greicius MD, Yang TT, Glover GH, Reiss AL et al (2003) Comparison of fMRI activation at 3 and 1.5 T during perceptual, cognitive, and affective processing. Neuroimage 18:813–826PubMedCrossRefGoogle Scholar
  69. 69.
    Yang Y, Wen H, Mattay VS, Balaban RS, Frank JA, Duyn JH (1999) Comparison of 3D BOLD functional MRI with spiral acquisition at 1.5 and 4.0 T. Neuroimage 9:446–451PubMedCrossRefGoogle Scholar
  70. 70.
    Hoenig K, Kuhl CK, Scheef L (2005) Functional 3.0-T MR assessment of higher cognitive function: are there advantages over 1.5-T imaging? Radiology 234:860–868PubMedCrossRefGoogle Scholar
  71. 71.
    Tieleman A, Vandemaele P, Seurinck R, Deblaere K, Achten E (2007) Comparison between functional magnetic resonance imaging at 1.5 and 3 Tesla: effect of increased field strength on 4 paradigms used during presurgical work-up. Invest Radiol 42:130–138PubMedCrossRefGoogle Scholar
  72. 72.
    Jovicich J, Norris DG (1999) Functional MRI of the human brain with GRASE-based BOLD contrast. Magn Reson Med 41:871–876PubMedCrossRefGoogle Scholar
  73. 73.
    Pruessmann KP, Weiger M, Scheidegger MB, Boesiger P (1999) SENSE: sensitivity encoding for fast MRI. Magn Reson Med 42:952–962PubMedCrossRefGoogle Scholar
  74. 74.
    Weiger M, Pruessmann KP, Osterbauer R, Bornert P, Boesiger P, Jezzard P (2002) Sensitivity-encoded single-shot spiral imaging for reduced susceptibility artifacts in BOLD fMRI. Magn Reson Med 48:860–866PubMedCrossRefGoogle Scholar
  75. 75.
    Preston AR, Thomason ME, Ochsner KN, Cooper JC, Glover GH (2004) Comparison of spiral-in/out and spiral-out BOLD fMRI at 1.5 and 3 T. Neuroimage 21:291–301PubMedCrossRefGoogle Scholar
  76. 76.
    Nimsky C, Ganslandt O, Merhof D, Sorensen AG, Fahlbusch R (2006) Intraoperative visualization of the pyramidal tract by diffusion-tensor-imaging-based fiber tracking. Neuroimage 30:1219–1229PubMedCrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2009

Authors and Affiliations

  • Ann Tieleman
    • 1
    • 4
    Email author
  • Karel Deblaere
    • 1
  • Dirk Van Roost
    • 2
  • Olivier Van Damme
    • 3
  • Eric Achten
    • 1
  1. 1.Department of NeuroradiologyGhent University HospitalGhentBelgium
  2. 2.Department of NeurosurgeryGhent University HospitalGhentBelgium
  3. 3.Department of NeurosurgeryHeilig Hartziekenhuis, Roeselare-MenenRoeselareBelgium
  4. 4.Department of RadiologyGhent University HospitalGhentBelgium

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