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. 2005 Aug;76(8):1152–1157. doi: 10.1136/jnnp.2004.050286

Evaluation of preoperative high magnetic field motor functional MRI (3 Tesla) in glioma patients by navigated electrocortical stimulation and postoperative outcome

K Roessler 1, M Donat 1, R Lanzenberger 1, K Novak 1, A Geissler 1, A Gartus 1, A Tahamtan 1, D Milakara 1, T Czech 1, M Barth 1, E Knosp 1, R Beisteiner 1
PMCID: PMC1739751  PMID: 16024896

Abstract

Objectives: The validity of 3 Tesla motor functional magnetic resonance imaging (fMRI) in patients with gliomas involving the primary motor cortex was investigated by intraoperative navigated motor cortex stimulation (MCS).

Methods: Twenty two patients (10 males, 12 females, mean age 39 years, range 10–65 years) underwent preoperative fMRI studies, performing motor tasks including hand, foot, and mouth movements. A recently developed high field clinical fMRI technique was used to generate pre-surgical maps of functional high risk areas defining a motor focus. Motor foci were tested for validity by intraoperative motor cortex stimulation (MCS) employing image fusion and neuronavigation. Clinical outcome was assessed using the Modified Rankin Scale.

Results: FMRI motor foci were successfully detected in all patients preoperatively. In 17 of 22 patients (77.3%), a successful stimulation of the primary motor cortex was possible. All 17 correlated patients showed 100% agreement on MCS and fMRI motor focus within 10 mm. Technical problems during stimulation occurred in three patients (13.6%), no motor response was elicited in two (9.1%), and MCS induced seizures occurred in three (13.6%). Combined fMRI and MCS mapping results allowed large resections in 20 patients (91%) (gross total in nine (41%), subtotal in 11 (50%)) and biopsy in two patients (9%). Pathology revealed seven low grade and 15 high grade gliomas. Mild to moderate transient neurological deterioration occurred in six patients, and a severe hemiparesis in one. All patients recovered within 3 months (31.8% transient, 0% permanent morbidity).

Conclusions: The validation of clinically optimised high magnetic field motor fMRI confirms high reliability as a preoperative and intraoperative adjunct in glioma patients selected for surgery within or adjacent to the motor cortex.

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Selected References

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  1. Ammirati M., Vick N., Liao Y. L., Ciric I., Mikhael M. Effect of the extent of surgical resection on survival and quality of life in patients with supratentorial glioblastomas and anaplastic astrocytomas. Neurosurgery. 1987 Aug;21(2):201–206. doi: 10.1227/00006123-198708000-00012. [DOI] [PubMed] [Google Scholar]
  2. Beisteiner R., Lanzenberger R., Novak K., Edward V., Windischberger C., Erdler M., Cunnington R., Gartus A., Streibl B., Moser E. Improvement of presurgical patient evaluation by generation of functional magnetic resonance risk maps. Neurosci Lett. 2000 Aug 18;290(1):13–16. doi: 10.1016/s0304-3940(00)01303-3. [DOI] [PubMed] [Google Scholar]
  3. Beisteiner R., Windischberger C., Lanzenberger R., Edward V., Cunnington R., Erdler M., Gartus A., Streibl B., Moser E., Deecke L. Finger somatotopy in human motor cortex. Neuroimage. 2001 Jun;13(6 Pt 1):1016–1026. doi: 10.1006/nimg.2000.0737. [DOI] [PubMed] [Google Scholar]
  4. Beisteiner Roland, Gartus Andreas, Erdler Marcus, Mayer Dagmar, Lanzenberger Rupert, Deecke Lüder. Magnetoencephalography indicates finger motor somatotopy. Eur J Neurosci. 2004 Jan;19(2):465–472. doi: 10.1111/j.1460-9568.2004.03115.x. [DOI] [PubMed] [Google Scholar]
  5. Berger M. S., Deliganis A. V., Dobbins J., Keles G. E. The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer. 1994 Sep 15;74(6):1784–1791. doi: 10.1002/1097-0142(19940915)74:6<1784::aid-cncr2820740622>3.0.co;2-d. [DOI] [PubMed] [Google Scholar]
  6. Berger M. S., Kincaid J., Ojemann G. A., Lettich E. Brain mapping techniques to maximize resection, safety, and seizure control in children with brain tumors. Neurosurgery. 1989 Nov;25(5):786–792. doi: 10.1097/00006123-198911000-00015. [DOI] [PubMed] [Google Scholar]
  7. Berger M. S., Ojemann G. A. Intraoperative brain mapping techniques in neuro-oncology. Stereotact Funct Neurosurg. 1992;58(1-4):153–161. doi: 10.1159/000098989. [DOI] [PubMed] [Google Scholar]
  8. Bonita R., Beaglehole R. Recovery of motor function after stroke. Stroke. 1988 Dec;19(12):1497–1500. doi: 10.1161/01.str.19.12.1497. [DOI] [PubMed] [Google Scholar]
  9. Cosgrove G. R., Buchbinder B. R., Jiang H. Functional magnetic resonance imaging for intracranial navigation. Neurosurg Clin N Am. 1996 Apr;7(2):313–322. [PubMed] [Google Scholar]
  10. Daneyemez M., Gezen F., Canakçi Z., Kahraman S. Radical surgery and reoperation in supratentorial malignant glial tumors. Minim Invasive Neurosurg. 1998 Dec;41(4):209–213. doi: 10.1055/s-2008-1052044. [DOI] [PubMed] [Google Scholar]
  11. Duffau H., Capelle L., Sichez J., Faillot T., Abdennour L., Law Koune J. D., Dadoun S., Bitar A., Arthuis F., Van Effenterre R. Intra-operative direct electrical stimulations of the central nervous system: the Salpêtrière experience with 60 patients. Acta Neurochir (Wien) 1999;141(11):1157–1167. doi: 10.1007/s007010050413. [DOI] [PubMed] [Google Scholar]
  12. Duffau Hugues, Denvil Dominique, Capelle Laurent. Absence of movement disorders after surgical resection of glioma invading the right striatum. J Neurosurg. 2002 Aug;97(2):363–369. doi: 10.3171/jns.2002.97.2.0363. [DOI] [PubMed] [Google Scholar]
  13. Edward V., Windischberger C., Cunnington R., Erdler M., Lanzenberger R., Mayer D., Endl W., Beisteiner R. Quantification of fMRI artifact reduction by a novel plaster cast head holder. Hum Brain Mapp. 2000 Nov;11(3):207–213. doi: 10.1002/1097-0193(200011)11:3&#x0003c;207::AID-HBM60&#x0003e;3.0.CO;2-J. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eisner W., Burtscher J., Bale R., Sweeney R., Koppelstätter F., Golaszewski S., Kolbitsch C., Twerdy K. Use of neuronavigation and electrophysiology in surgery of subcortically located lesions in the sensorimotor strip. J Neurol Neurosurg Psychiatry. 2002 Mar;72(3):378–381. doi: 10.1136/jnnp.72.3.378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fandino J., Kollias S. S., Wieser H. G., Valavanis A., Yonekawa Y. Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg. 1999 Aug;91(2):238–250. doi: 10.3171/jns.1999.91.2.0238. [DOI] [PubMed] [Google Scholar]
  16. Fransson Peter, Merboldt Klaus-Dietmar, Petersson Karl Magnus, Ingvar Martin, Frahm Jens. On the effects of spatial filtering--a comparative fMRI study of episodic memory encoding at high and low resolution. Neuroimage. 2002 Aug;16(4):977–984. doi: 10.1006/nimg.2002.1079. [DOI] [PubMed] [Google Scholar]
  17. Gallen C. C., Sobel D. F., Waltz T., Aung M., Copeland B., Schwartz B. J., Hirschkoff E. C., Bloom F. E. Noninvasive presurgical neuromagnetic mapping of somatosensory cortex. Neurosurgery. 1993 Aug;33(2):260–268. [PubMed] [Google Scholar]
  18. Geissler Alexander, Lanzenberger Rupert, Barth Markus, Tahamtan Amir Reza, Milakara Denny, Gartus Andreas, Beisteiner Roland. Influence of fMRI smoothing procedures on replicability of fine scale motor localization. Neuroimage. 2004 Dec 10;24(2):323–331. doi: 10.1016/j.neuroimage.2004.08.042. [DOI] [PubMed] [Google Scholar]
  19. Hentschel Stephen J., Lang Frederick F. Current surgical management of glioblastoma. Cancer J. 2003 Mar-Apr;9(2):113–125. doi: 10.1097/00130404-200303000-00007. [DOI] [PubMed] [Google Scholar]
  20. Hulshof M. C., Koot R. W., Schimmel E. C., Dekker F., Bosch D. A., González González D. Prognostic factors in glioblastoma multiforme. 10 years experience of a single institution. Strahlenther Onkol. 2001 Jun;177(6):283–290. doi: 10.1007/pl00002409. [DOI] [PubMed] [Google Scholar]
  21. Jack C. R., Jr, Thompson R. M., Butts R. K., Sharbrough F. W., Kelly P. J., Hanson D. P., Riederer S. J., Ehman R. L., Hangiandreou N. J., Cascino G. D. Sensory motor cortex: correlation of presurgical mapping with functional MR imaging and invasive cortical mapping. Radiology. 1994 Jan;190(1):85–92. doi: 10.1148/radiology.190.1.8259434. [DOI] [PubMed] [Google Scholar]
  22. Keles G. E., Lamborn K. R., Berger M. S. Low-grade hemispheric gliomas in adults: a critical review of extent of resection as a factor influencing outcome. J Neurosurg. 2001 Nov;95(5):735–745. doi: 10.3171/jns.2001.95.5.0735. [DOI] [PubMed] [Google Scholar]
  23. Keles G. Evren, Lamborn Kathleen R., Chang Susan M., Prados Michael D., Berger Mitchel S. Volume of residual disease as a predictor of outcome in adult patients with recurrent supratentorial glioblastomas multiforme who are undergoing chemotherapy. J Neurosurg. 2004 Jan;100(1):41–46. doi: 10.3171/jns.2004.100.1.0041. [DOI] [PubMed] [Google Scholar]
  24. Keles G. Evren, Lundin David A., Lamborn Kathleen R., Chang Edward F., Ojemann George, Berger Mitchel S. 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. 2004 Mar;100(3):369–375. doi: 10.3171/jns.2004.100.3.0369. [DOI] [PubMed] [Google Scholar]
  25. Kleihues P., Burger P. C., Scheithauer B. W. The new WHO classification of brain tumours. Brain Pathol. 1993 Jul;3(3):255–268. doi: 10.1111/j.1750-3639.1993.tb00752.x. [DOI] [PubMed] [Google Scholar]
  26. Krings T., Reinges M. H., Erberich S., Kemeny S., Rohde V., Spetzger U., Korinth M., Willmes K., Gilsbach J. M., Thron A. Functional MRI for presurgical planning: problems, artefacts, and solution strategies. J Neurol Neurosurg Psychiatry. 2001 Jun;70(6):749–760. doi: 10.1136/jnnp.70.6.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Krings T., Reul J., Spetzger U., Klusmann A., Roessler F., Gilsbach J. M., Thron A. Functional magnetic resonance mapping of sensory motor cortex for image-guided neurosurgical intervention. Acta Neurochir (Wien) 1998;140(3):215–222. doi: 10.1007/s007010050088. [DOI] [PubMed] [Google Scholar]
  28. Krüger G., Kastrup A., Glover G. H. Neuroimaging at 1.5 T and 3.0 T: comparison of oxygenation-sensitive magnetic resonance imaging. Magn Reson Med. 2001 Apr;45(4):595–604. doi: 10.1002/mrm.1081. [DOI] [PubMed] [Google Scholar]
  29. Lehéricy S., Duffau H., Cornu P., Capelle L., Pidoux B., Carpentier A., Auliac S., Clemenceau S., Sichez J. P., Bitar A. 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. 2000 Apr;92(4):589–598. doi: 10.3171/jns.2000.92.4.0589. [DOI] [PubMed] [Google Scholar]
  30. Matz P. G., Cobbs C., Berger M. S. Intraoperative cortical mapping as a guide to the surgical resection of gliomas. J Neurooncol. 1999 May;42(3):233–245. doi: 10.1023/a:1006122122404. [DOI] [PubMed] [Google Scholar]
  31. Mohan D. S., Suh J. H., Phan J. L., Kupelian P. A., Cohen B. H., Barnett G. H. Outcome in elderly patients undergoing definitive surgery and radiation therapy for supratentorial glioblastoma multiforme at a tertiary care institution. Int J Radiat Oncol Biol Phys. 1998 Dec 1;42(5):981–987. doi: 10.1016/s0360-3016(98)00296-x. [DOI] [PubMed] [Google Scholar]
  32. Moser Ewald, Trattnig Siegfried. 3.0 Tesla MR systems. Invest Radiol. 2003 Jul;38(7):375–376. doi: 10.1097/01.RLI.0000068411.72031.72. [DOI] [PubMed] [Google Scholar]
  33. Mueller W. M., Yetkin F. Z., Hammeke T. A., Morris G. L., 3rd, Swanson S. J., Reichert K., Cox R., Haughton V. M. Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors. Neurosurgery. 1996 Sep;39(3):515–521. doi: 10.1097/00006123-199609000-00015. [DOI] [PubMed] [Google Scholar]
  34. 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 Sep;71(3):316–326. doi: 10.3171/jns.1989.71.3.0316. [DOI] [PubMed] [Google Scholar]
  35. Piepmeier J., Christopher S., Spencer D., Byrne T., Kim J., Knisel J. P., Lacy J., Tsukerman L., Makuch R. Variations in the natural history and survival of patients with supratentorial low-grade astrocytomas. Neurosurgery. 1996 May;38(5):872–879. doi: 10.1097/00006123-199605000-00002. [DOI] [PubMed] [Google Scholar]
  36. Reijneveld J. C., Sitskoorn M. M., Klein M., Nuyen J., Taphoorn M. J. Cognitive status and quality of life in patients with suspected versus proven low-grade gliomas. Neurology. 2001 Mar 13;56(5):618–623. doi: 10.1212/wnl.56.5.618. [DOI] [PubMed] [Google Scholar]
  37. Roberts D. W., Strohbehn J. W., Hatch J. F., Murray W., Kettenberger H. A frameless stereotaxic integration of computerized tomographic imaging and the operating microscope. J Neurosurg. 1986 Oct;65(4):545–549. doi: 10.3171/jns.1986.65.4.0545. [DOI] [PubMed] [Google Scholar]
  38. Roessler K., Ungersboeck K., Aichholzer M., Dietrich W., Goerzer H., Matula C., Czech T., Koos W. T. Frameless stereotactic lesion contour-guided surgery using a computer-navigated microscope. Surg Neurol. 1998 Mar;49(3):282–289. doi: 10.1016/s0090-3019(97)00421-7. [DOI] [PubMed] [Google Scholar]
  39. Roessler K., Ungersboeck K., Dietrich W., Aichholzer M., Hittmeir K., Matula C., Czech T., Koos W. T. Frameless stereotactic guided neurosurgery: clinical experience with an infrared based pointer device navigation system. Acta Neurochir (Wien) 1997;139(6):551–559. doi: 10.1007/BF02750999. [DOI] [PubMed] [Google Scholar]
  40. Sartorius C. J., Berger M. S. Rapid termination of intraoperative stimulation-evoked seizures with application of cold Ringer's lactate to the cortex. Technical note. J Neurosurg. 1998 Feb;88(2):349–351. doi: 10.3171/jns.1998.88.2.0349. [DOI] [PubMed] [Google Scholar]
  41. Schiffbauer Hagen, Berger Mitchel S., Ferrari Paul, Freudenstein Dirk, Rowley Howard A., Roberts Timothy P. L. Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. J Neurosurg. 2002 Dec;97(6):1333–1342. doi: 10.3171/jns.2002.97.6.1333. [DOI] [PubMed] [Google Scholar]
  42. Schulder M., Maldjian J. A., Liu W. C., Holodny A. I., Kalnin A. T., Mun I. K., Carmel P. W. Functional image-guided surgery of intracranial tumors located in or near the sensorimotor cortex. J Neurosurg. 1998 Sep;89(3):412–418. doi: 10.3171/jns.1998.89.3.0412. [DOI] [PubMed] [Google Scholar]
  43. Scott J. N., Rewcastle N. B., Brasher P. M., Fulton D., MacKinnon J. A., Hamilton M., Cairncross J. G., Forsyth P. Which glioblastoma multiforme patient will become a long-term survivor? A population-based study. Ann Neurol. 1999 Aug;46(2):183–188. [PubMed] [Google Scholar]
  44. Watanabe E., Watanabe T., Manaka S., Mayanagi Y., Takakura K. Three-dimensional digitizer (neuronavigator): new equipment for computed tomography-guided stereotaxic surgery. Surg Neurol. 1987 Jun;27(6):543–547. doi: 10.1016/0090-3019(87)90152-2. [DOI] [PubMed] [Google Scholar]
  45. Wilkinson I. D., Romanowski C. A. J., Jellinek D. A., Morris J., Griffiths P. D. Motor functional MRI for pre-operative and intraoperative neurosurgical guidance. Br J Radiol. 2003 Feb;76(902):98–103. doi: 10.1259/bjr/66817309. [DOI] [PubMed] [Google Scholar]
  46. Yetkin F. Z., Papke R. A., Mark L. P., Daniels D. L., Mueller W. M., Haughton V. M. Location of the sensorimotor cortex: functional and conventional MR compared. AJNR Am J Neuroradiol. 1995 Nov-Dec;16(10):2109–2113. [PMC free article] [PubMed] [Google Scholar]
  47. Yousry T. A., Schmid U. D., Jassoy A. G., Schmidt D., Eisner W. E., Reulen H. J., Reiser M. F., Lissner J. Topography of the cortical motor hand area: prospective study with functional MR imaging and direct motor mapping at surgery. Radiology. 1995 Apr;195(1):23–29. doi: 10.1148/radiology.195.1.7892475. [DOI] [PubMed] [Google Scholar]

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