Functional Magnetic Resonance Imaging and Cortical Mapping in Motor Cortex Tumor Surgery: Complementary Methods

 

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Abstract

Functional magnetic resonance imaging (fMRI) and direct electrocortical stimulation (DES) are the most commonly used means of analyzing the functional brain topography prior to surgery in the vicinity of Brodmann area 4. No consensus has been established in the literature about the significance of both procedures in reducing operative morbidity. The study presented here was conducted in 30 patients with tumors in the area of the primary motor cortex. Blood oxygen level dependent (BOLD) sequences were preoperatively established with a standardized paradigm. Intraoperatively motor mapping was performed with DES. The results of both methods were digitally matched with a frameless image-guidance system. Correlations between the results of fMRI and of DES were analyzed. Furthermore, the potential influences of the size, position, and histology of the lesions on the mapping results were analyzed and the motor outcome was evaluated. The mean deviation between the results of fMRI and of DES was 13.8 mm (range: 7-28 mm). This deviation was independent of the histology, size, or location of the corresponding lesion. The individual variability of the analysis threshold value for the evaluation of the BOLD sequences led to a considerable topographical inaccuracy. As complementary methods, fMRI contributes to estimating the operational risk, while DES is performed when the results of MRI and fMRI suggest an immediate proximity of the tumor to motor areas.

Zusammenfassung

Funktionelle Magnetresonanztomographie (fMRT) und direkte elektrische Kortexstimulation (DES) sind die am häufigsten eingesetzten Methoden zur Analyse der funktionellen Topographie bei Eingriffen im Bereich der Zentralregion. In der Literatur besteht kein Konsens über die Wertigkeit der beiden Methoden zur Reduktion der operativen Morbidität. Die Studie umfasst 30 Patienten mit Tumoren im Bereich des primär motorischen Kortex. Präoperativ wurden mit einem standardisiertem Paradigma kernspintomographisch BOLD (blood oxygen level dependent) Sequenzen erstellt. Intraoperativ erfolgte ein motorisches Mapping mit DES. Die Ergebnisse beider Methoden wurden in den Datensatz eines rahmenlosen Stereotaxiegerätes übertragen. Analysiert wurde die Korrelation zwischen den Ergebnissen von fMRT und DES, der mögliche Einfluss von Größe, Lokalisation und Histologie der Tumoren auf die Mapping-Ergebnisse sowie der motorische Status. Die mittlere Abweichung zwischen den Ergebnissen von fMRT und DES betrug 13,8 mm (Spanne: 7-28 mm). Die Abweichung war unabhängig von Größe, Lokalisation und Histologie der Tumoren. Die individuelle Variabilität des Analyseschwellenwertes für die Auswertung der BOLD Sequenzen führte zu einer deutlichen topographischen Unschärfe. Als komplementäre Methoden dient die fMRT der Abschätzung des operativen Risikos, wohingegen die DES eingesetzt wird, wenn MRT und fMRT eine unmittelbare Nachbarschaft von Tumor und primär motorischen Kortex erwarten lassen.

References

• 1 Atlas SW, Howard 2nd RS, Maldjian J, Alsop D, Detre JA, Listerud J, D’Esposito M, Judy KD, Zager E, Stecker M. Functional magnetic resonance imaging of regional brain activity in patients with intracerebral gliomas: findings and implications for clinical management.  Neurosurgery. 1996;  38 ((2)) 329-338
  CrossrefPubMedGoogle Scholar
• 2 Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, Effenterre R Van, Capelle L. 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. 2005;  76 ((6)) 845-851 , [Review]
  CrossrefPubMedGoogle Scholar
• 3 Gati JS, Menon RS, Ugurbil K, Rutt BK. Experimental determination of the BOLD field strength dependence in vessels and tissue.  Magn Reson Med. 1997;  38 ((2)) 296-302
  CrossrefPubMedGoogle Scholar
• 4 Hill DL, Smith AD, Simmons A, Maurer Jr CR, Cox TC, Elwes R, Brammer M, Hawkes DJ, Polkey CE. Sources of error in comparing functional magnetic resonance imaging and invasive electrophysiological recordings.  J Neurosurg. 2000;  93 ((2)) 214-223
  PubMedGoogle Scholar
• 5 Hirsch J, Ruge MI, Kim KH, Correa DD, Victor JD, Relkin NR, Labar DR, Krol G, Bilsky MH, Souweidane MM, Angelis LM De, Gutin PH. An integrated functional magnetic resonance imaging procedure for preoperative mapping of cortical areas associated with tactile, motor, language, and visual functions.  Neurosurgery. 2000;  47 ((3)) 711-721 , , discussion 721-722
  PubMedGoogle Scholar
• 6 Holodny AI, Schulder M, Liu WC, Wolko J, Maldjian JA, Kalnin AJ. The effect of brain tumors on BOLD functional MR imaging activation in the adjacent motor cortex: implications for image-guided neurosurgery.  AJNR Am J Neuroradiol. 2000;  21 ((8)) 1415-1422
  PubMedGoogle Scholar
• 7 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. 2004;  100 ((3)) 369-375
  CrossrefPubMedGoogle Scholar
• 8 Kim SG, Hendrich K, Hu X, Merkle H, Ugurbil K. Potential pitfalls of functional MRI using conventional gradient-recalled echo techniques.  NMR Biomed. 1994;  7 ((1-2)) 69-74
  CrossrefPubMedGoogle Scholar
• 9 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. 2001;  95 ((4)) 608-614
  CrossrefPubMedGoogle Scholar
• 10 Korvenoja A, Kirveskari E, Aronen HJ, Avikainen S, Brander A, Huttunen J, Ilmoniemi RJ, Jaaskelainen JE, Kovala T, Makela JP, Salli E, Seppa M. Sensorimotor cortex localization: comparison of magnetoencephalography, functional MR imaging, and intraoperative cortical mapping.  Radiology. 2006;  241 ((1)) 213-222 , . Epub 2006 Aug 14
  CrossrefPubMedGoogle Scholar
• 11 Krings T, Schreckenberger M. et al . Metabolic and electrophysiological validation of fuctional MRI.  J Neurol Neurosurg Psychiatry. 2001;  71 762-771
  CrossrefPubMedGoogle Scholar
• 12 Krings T, Reinges MH, Erberich S, Kemeny S, Rohde V, Spetzger U, Korinth M, Willmes K, Gilsbach JM, Thron A. Functional MRI for presurgical planning: problems, artefacts, and solution strategies.  J Neurol Neurosurg Psychiatry. 2001;  70 ((6)) 749-760
  CrossrefPubMedGoogle Scholar
• 13 Krishnan R, Raabe A, Hattingen E, Szelenyi A, Yahya H, Hermann E, Zimmermann M, Seifert V. Functional magnetic resonance imaging-integrated neuronavigation: correlation between lesion-to-motor cortex distance and outcome.  Neurosurgery. 2004;  55 ((4)) 904-914 , ; discussion 914-915
  PubMedGoogle Scholar
• 14 Lehericy S, Duffau H. et al . Correspondance 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;  92 589-598
  PubMedGoogle Scholar
• 15 Majos A, Tybor K, Stefanczyk L, Goraj B. Cortical mapping by functional magnetic resonance imaging in patients with brain tumors.  Eur Radiol. 2005;  15 ((6)) 1148-1158 , Epub 2004 Dec 31
  CrossrefPubMedGoogle Scholar
• 16 Mueller WM, Yetkin FZ, Hammeke TA, Morris 3rd GL, Swanson SJ, Reichert K, Cox R, Haughton VM. Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors.  Neurosurgery. 1996;  39 ((3)) 515-520 , ; discussion 520-521
  PubMedGoogle Scholar
• 17 Neuloh G, Pechstein U, Cedzich C, Schramm J. Motor evoked potential monitoring with supratentorial surgery.  Neurosurgery. 2004;  54 ((5)) 1061-1070 , ; discussion 1070-1072
  CrossrefPubMedGoogle Scholar
• 18 Nimsky C, Grummich P, Sorensen AG, Fahlbusch R, Ganslandt O. Visualization of the pyramidal tract in glioma surgery by integrating diffusion tensor imaging in functional neuronavigation.  Zentralbl Neurochir. 2005;  66 ((3)) 133-141
  Article in Thieme ConnectPubMedGoogle Scholar
• 19 Nimsky C, Ganslandt O. et al . Integration of functional magnetic resonance imaging supported by magnetencephalography in functional neuronavigation.  Neurosurgery. 1999;  44 1249-1256
  PubMedGoogle Scholar
• 20 Pujol J, Conesa G, Deus J, Lopez-Obarrio L, Isamat F, Capdevila A. Clinical application of functional magnetic resonance imaging in presurgical identification of the central sulcus.  J Neurosurg. 1998;  88 ((5)) 863-869
  PubMedGoogle Scholar
• 21 Reinges MH, Krings T, Meyer PT, Schreckenberger M, Rohde V, Weidemann J, Sabri O, Mulders EJ, Buell U, Thron A, Gilsbach JM. Preoperative mapping of cortical motor function: prospective comparison of functional magnetic resonance imaging and [15O]-H₂O-positron emission tomography in the same co-ordinate system.  Nucl Med Commun. 2004;  25 ((10)) 987-997
  CrossrefPubMedGoogle Scholar
• 22 Reithmeier T, Krammer M, Gumprecht H, Gerstner W, Lumenta CB. 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. 2003;  46 ((2)) 65-71
  Article in Thieme ConnectPubMedGoogle Scholar
• 23 Riem T, Vignes JR, San-Galli F, Guerin J, Allard M. Functional neuronavigation. Fusion of functional MRI data in a neuronavigation system.  Neurochirurgie. 2004;  50 ((2-3 Pt 1)) 111-1116 , [in French]
  PubMedGoogle Scholar
• 24 Roux FE, Ibarrola D, Tremoulet M, Lazorthes Y, Henry P, Sol JC, Berry I. Methodological and technical issues for integrating functional magnetic resonance imaging data in a neuronavigational system.  Neurosurgery. 2001;  49 ((5)) 1145-1156 , ; discussion 1156-1157
  CrossrefPubMedGoogle Scholar
• 25 Schreckenberger M, Spetzger U, Sabri O, Meyer PT, Zeggel T, Zimny M, Gilsbach J, Buell U. Localisation of motor areas in brain tumour patients: a comparison of preoperative [18F] FDG-PET and intraoperative cortical electrostimulation.  Eur J Nucl Med. 2001;  28 ((9)) 1394-1403
  CrossrefPubMedGoogle Scholar
• 26 Schulder M, Maldjian JA, Liu WC, Holodny AI, Kalnin AT, Mun IK, Carmel PW. Functional image-guided surgery of intracranial tumors located in or near the sensorimotor cortex.  J Neurosurg. 1998;  89 ((3)) 412-418
  CrossrefPubMedGoogle Scholar
• 27 Stippich C, Kress B, Ochmann H, Tronnier V, Sartor K. Preoperative functional magnetic resonance tomography (FMRI) in patients with rolandic brain tumors: indication, investigation strategy, possibilities and limitations of clinical application.  Rofo. 2003;  175 ((8)) 1042-1050 , . Review [German]
  PubMedGoogle Scholar
• 28 Suess O, Suess S, Brock M, Kombos T. Intraoperative electrocortical stimulation of Brodmann area 4: a 10-year analysis of 255 cases.  Head Face Med. 2006;  ((2)) 20
  CrossrefPubMedGoogle Scholar
• 29 Tomczak RJ, Wunderlich AP, Wang Y, Braun V, Antoniadis G, Gorich J, Richter HP, Brambs HJ. fMRI for preoperative neurosurgical mapping of motor cortex and language in a clinical setting.  J Comput Assist Tomogr. 2000;  24 ((6)) 927-934
  CrossrefPubMedGoogle Scholar
• 30 Yetkin FZ, Mueller WM, Morris GL, MacAuliffe TL, Ulmer JL, Cox RW, Daniels DL, Haughton VM. Functional MR activation correlated with intraoperative cortical mapping.  AJNR Am J Neuroradiol. 1997;  18 ((7)) 1311-1315
  PubMedGoogle Scholar
• 31 Yousry TA, Schmid UD, Jassoy AG, Schmidt D, Eisner WE, Reulen HJ, Reiser MF, Lissner J. Topography of the cortical motor hand area: prospective study with functional MR imaging and direct motor mapping at surgery.  Radiology. 1995;  195 ((1)) 23-29
  CrossrefPubMedGoogle Scholar

Correspondence

Dr. T. Picht

Neurochirurgische Klinik

Charité - Universitaetsmedizin Berlin

Hindenburgdamm 30

12200 Berlin

Germany

Phone: +30/8445/31 91

Fax: +30/8445/35 69

Email: thomas.picht@charite.de