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DOI: 10.1055/s-2005-836606
© Georg Thieme Verlag Stuttgart · New York
Visualization of the Pyramidal Tract in Glioma Surgery by Integrating Diffusion Tensor Imaging in Functional Neuronavigation
Intraoperative Darstellung der Pyramidenbahn in der Gliomchirurgie durch Integration der Diffusions-Tensor-Bildgebung in funktionelle NeuronavigationPublication History
Publication Date:
22 August 2005 (online)
Abstract
Object: The aim of this study was to investigate whether diffusion tensor imaging (DTI) can be integrated into functional navigation for the intraoperative visualization of the pyramidal tract. Methods: A single-shot spin-echo diffusion-weighted echo planar imaging sequence on a 1.5 T magnetic resonance (MR) scanner was used for DTI. One null image and six diffusion-weighted images (high B value 1 000 mm/s2) were obtained. Color-encoded fractional anisotropy maps of the principal eigenvector rendered as a boxoid within each voxel were used for segmentation of the pyramidal tract. The segmented images were rigidly registered with a T1-weighted gradient echo 3D dataset for navigation in 16 patients with gliomas. In tumors adjacent to the motor cortex (n = 6) data from functional MR imaging were co-registered. Results: The whole DTI processing lasted about 25-30 minutes in each case. In all cases DTI could be integrated into the navigational dataset resulting in an intraoperative visualization of the pyramidal tract by microscope-based navigation. Navigational accuracy measured as the target registration error was 1.2 ± 0.46 mm. Registration of fractional anisotropy maps with the 3D navigational dataset was possible with an error of less than 2 mm. Co-registration with fMRI was consistent with DTI data. A neurological deterioration was observed only in one patient. Conclusions: DTI can be reliably integrated into navigational datasets. Thus, microscope-based neuronavigation can be used for an intraoperative visualization of the course of the pyramidal tract. However, a possible shifting of the pyramidal tract has to be taken into account after major tumor parts are removed.
Zusammenfassung
Einleitung: Ziel war es, zu untersuchen, ob die Diffusions-Tensor-Bildgebung (DTI) in die funktionelle Neuronavigation zur intraoperativen Darstellung der Pyramidenbahn eingebunden werden kann. Material und Methoden: Die DTI-Daten wurden mit einer single-shot diffusions-gewichteten echo-planar-imaging-Sequenz an einem 1,5 Tesla Magnetresonanz-Scanner gemessen. Je Schicht wurden eine Messung ohne Diffusionsgradienten (B0-Bild) sowie Messungen mit Diffusionsgradienten (b-Wert 1 000 s/mm2) in 6 verschiedenen Richtungen akquiriert. In farbkodierten Schichten der fraktionellen Anisotropie (FA), in denen in jedem Voxel der Hauteigenvektor als kleiner Quader dargestellt ist, wurde die Pyramidenbahn segmentiert. Bei insgesamt 16 Patienten mit Gliomen wurden diese segmentierten Bilddaten dann starr mit einem 3D T1-gewichteten Navigationsdatensatz registriert. Bei Tumoren in der Nähe des motorischen Kortex (n = 6) wurden zusätzlich funktionelle MR-Messungen ko-registriert. Ergebnisse: Die gesamte Verarbeitung der DTI-Daten dauerte bei jedem Patienten zwischen 25 und 30 Minuten. In allen Fällen konnten die DTI-Daten in die Navigation integriert und so konnte die Pyramidenbahn mit Hilfe der mikroskop-gestützten Navigation während der Operation dargestellt werden. Die Navigationsgenauigkeit, gemessen als „Target Registration Error” betrug 1,2 ± 0,46 mm. Der Fehler der Registrierung der FA-Schichten mit den anatomischen Bilddaten war kleiner als 2 mm. Die Ko-Registrierung mit funktionellem MR war mit den DTI-Messungen konsistent. Bei nur einem Patienten kam es zu einer neurologischen Verschlechterung. Schlussfolgerung: DTI-Daten können zuverlässig in die Navigation eingebunden werden. Damit kann die mikroskop-gestützte Navigation zur intraoperativen Visualisierung der Pyramidenbahn eingesetzt werden. Jedoch muss eine mögliche Verlagerung der Pyramidenbahn, nachdem wesentliche Tumoranteile entfernt worden sind, berücksichtigt werden.
Key words
diffusion tensor imaging - functional neuronavigation - functional magnetic resonance imaging - white matter tracts
Schlüsselwörter
Bahnsysteme - Diffusions-Tensor-Bildgebung - funktionelle Neuronavigation - funktionelle Magnetresonanztomographie
References
- 1 Basser P J, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J. 1994; 66 259-267
- 2 Basser P J, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med. 2000; 44 625-632
- 3 Beppu T, Inoue T, Shibata Y, Kurose A, Arai H, Ogasawara K, Ogawa A, Nakamura S, Kabasawa H. Measurement of fractional anisotropy using diffusion tensor MRI in supratentorial astrocytic tumors. J Neurooncol. 2003; 63 109-116
- 4 Berman J I, Berger M S, Mukherjee P, Henry R G. Diffusion-tensor imaging-guided tracking of fibers of the pyramidal tract combined with intraoperative cortical stimulation mapping in patients with gliomas. J Neurosurg. 2004; 101 66-72
- 5 Black P M, Jaaskelainen J. Visualization of the eloquent motor system by integration of MEG, functional, and anisotropic diffusion-weighted MRI in functional neuronavigation [comment]. Surg Neurol. 2003; 59 362
- 6 Clark C A, Barrick T R, Murphy M M, Bell B A. White matter fiber tracking in patients with space-occupying lesions of the brain: a new technique for neurosurgical planning?. Neuroimage. 2003; 20 1601-1608
- 7 Coenen V A, Krings T, Mayfrank L, Polin R S, Reinges M H, Thron A, Gilsbach J M. Three-dimensional visualization of the pyramidal tract in a neuronavigation system during brain tumor surgery: first experiences and technical note. Neurosurgery. 2001; 49 86-93
- 8 Coenen V A, Krings T, Weidemann J, Spangenberg P, Gilsbach J M, Rohde V. [Diffusion weighted imaging combined with intraoperative 3D-ultrasound and fMRI for the resection of an optic radiation cavernoma]. Zentralbl Neurochir. 2003; 64 133-137
- 9 Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Taillandier L, Lopes M, Mitchell M C, Roche S, Muller J C, Bitar A, Sichez J P, Effenterre R van. 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. 2003; 98 764-778
- 10 Ferrant M, Nabavi A, Macq B, Black P M, Jolesz F A, Kikinis R, Warfield S K. Serial registration of intraoperative MR images of the brain. Med Image Anal. 2002; 6 337-359
- 11 Ganslandt O, Fahlbusch R, Nimsky C, Kober H, Möller M, Steinmeier R, Romstöck J, Vieth J. Functional neuronavigation with magnetoencephalography: outcome in 50 patients with lesions around the motor cortex. J Neurosurg. 1999; 91 73-79
- 12 Guye M, Parker G J, Symms M, Boulby P, Wheeler-Kingshott C A, Salek-Haddadi A, Barker G J, Duncan J S. Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo. Neuroimage. 2003; 19 1349-1360
- 13 Hendler T, Pianka P, Sigal M, Kafri M, Ben-Bashat D, Constantini S, Graif M, Fried I, Assaf Y. Delineating gray and white matter involvement in brain lesions: three-dimensional alignment of functional magnetic resonance and diffusion-tensor imaging. J Neurosurg. 2003; 99 1018-1027
- 14 Inoue T, Shimizu H, Yoshimoto T. Imaging the pyramidal tract in patients with brain tumors. Clin Neurol Neurosurg. 1999; 101 4-10
- 15 Kamada K, Houkin K, Takeuchi F, Ishii N, Ikeda J, Sawamura Y, Kuriki S, Kawaguchi H, Iwasaki Y. Visualization of the eloquent motor system by integration of MEG, functional, and anisotropic diffusion-weighted MRI in functional neuronavigation. Surg Neurol. 2003; 59 352-362
- 16 Keles G E, Lamborn K R, Berger M S. Coregistration accuracy and detection of brain shift using intraoperative sononavigation during resection of hemispheric tumors. Neurosurgery. 2003; 53 556-564
- 17 Keles G E, Lundin D A, Lamborn K R, Chang E F, Ojemann G, Berger M 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; 100 369-375
- 18 Kober H, Nimsky C, Möller M, Hastreiter P, Fahlbusch R, Ganslandt O. Correlation of sensorimotor activation with functional magnetic resonance imaging and magnetoencephalography in presurgical functional imaging: a spatial analysis. Neuroimage. 2001; 14 1214-1228
- 19 Krings T, Reinges M H, Thiex R, Gilsbach J M, Thron A. Functional and diffusion-weighted magnetic resonance images of space-occupying lesions affecting the motor system: imaging the motor cortex and pyramidal tracts. J Neurosurg. 2001; 95 816-824
- 20 Le Bihan D, Zijl P Van. From the diffusion coefficient to the diffusion tensor. NMR Biomed. 2002; 15 431-434
- 21 Lu S, Ahn D, Johnson G, Cha S. Peritumoral diffusion tensor imaging of high-grade gliomas and metastatic brain tumors. AJNR Am J Neuroradiol. 2003; 24 937-941
- 22 Mamata Y, Mamata H, Nabavi A, Kacher D F, Pergolizzi R S, Schwartz R B, Kikinis R, Jolesz F A, Maier S E. Intraoperative diffusion imaging on a 0.5 Tesla interventional scanner. J Magn Reson Imaging. 2001; 13 115-119
- 23 Merhof D, Hastreiter P, Soza G, Stamminger M, Nimsky C. Non-linear integration of DTI-based fiber tracts into standard 3D MR data. In: Girod B, Magnor M, Seidel H (eds). Vision Modeling and Visualization 2004. Akademische Verlagsgesellschaft Aka, Berlin 2004; 371-377
- 24 Mori S, Zijl P C Van. Fiber tracking: principles and strategies - a technical review. NMR Biomed. 2002; 15 468-480
- 25 Nabavi A, Black P M, Gering D T, Westin C F, Mehta V, Pergolizzi R S, Ferrant M, Warfield S K, Hata N, Schwartz R B, Wells W M, Kikinis R, Jolesz F A. Serial intraoperative magnetic resonance imaging of brain shift. Neurosurgery. 2001; 48 787-798
- 26 Nimsky C, Ganslandt O, Cerny S, Hastreiter P, Greiner G, Fahlbusch R. Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging. Neurosurgery. 2000; 47 1070-1080
- 27 Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen A G, Fahlbusch R. Intraoperative diffusion tensor imaging: shifting of white matter tracts during neurosurgical procedures - initial experience. Radiology. 2005; 234 218-225
- 28 Nimsky C, Ganslandt O, Kober H, Möller M, Ulmer S, Tomandl B, Fahlbusch R. Integration of functional magnetic resonance imaging supported by magnetoencephalography in functional neuronavigation. Neurosurgery. 1999; 44 1249-1256
- 29 Pajevic S, Pierpaoli C. Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn Reson Med. 1999; 42 526-540
- 30 Price S, Burnet N, Donovan T, Green H, Pena A, Antoun N, Pickard J, Carpenter T, Gillard J. Diffusion tensor imaging of brain tumours at 3 T: a potential tool for assessing white matter tract invasion?. Clin Radiol. 2003; 58 455-462
- 31 Romstöck J, Fahlbusch R, Ganslandt O, Nimsky C, Strauss C. Localisation of the sensorimotor cortex during surgery for brain tumors: feasibility and waveform patterns of somatosensory evoked potentials. J Neurol Neurosurg Psychiatry. 2002; 72 221-229
- 32 Talos I, O’Donnell L, Westin C F, Warfield S K, Wells W M, Yoo S, Panych L, Golby A, Mamata H, Maier S, Ratiu P, Guttmann C, Black P M, Jolesz F, Kikinis R. Diffusion tensor and functional MRI fusion with anatomical MRI for image-guided neurosurgery. In: Ellis R, Peters T (eds). MICCAI 2003. Springer-Verlag, Berlin, Heidelberg 2003; 407-415
- 33 Tummala R P, Chu R M, Liu H, Truwit C L, Hall W A. Application of diffusion tensor imaging to magnetic-resonance-guided brain tumor resection. Pediatr Neurosurg. 2003; 39 39-43
- 34 Wieshmann U C, Clark C A, Symms M R, Franconi F, Barker G J, Shorvon S D. Reduced anisotropy of water diffusion in structural cerebral abnormalities demonstrated with diffusion tensor imaging. Magn Reson Imaging. 1999; 17 1269-1274
- 35 Witwer B P, Moftakhar R, Hasan K M, Deshmukh P, Haughton V, Field A, Arfanakis K, Noyes J, Moritz C H, Meyerand M E, Rowley H A, Alexander A L, Badie B. Diffusion-tensor imaging of white matter tracts in patients with cerebral neoplasm. J Neurosurg. 2002; 97 568-575
- 36 Wu J S, Zhou L F, Hong X N, Mao Y, Du G H. [Role of diffusion tensor imaging in neuronavigation surgery of brain tumors involving pyramidal tracts]. Zhonghua Wai Ke Za Zhi [Chinese]. 2003; 41 662-666
- 37 Yamada K, Kizu O, Mori S, Ito H, Nakamura H, Yuen S, Kubota T, Tanaka O, Akada W, Sasajima H, Mineura K, Nishimura T. Brain fiber tracking with clinically feasible diffusion-tensor MR imaging: initial experience. Radiology. 2003; 227 295-301
- 38 Yingling C D, Ojemann S, Dodson B, Harrington M J, Berger M S. Identification of motor pathways during tumor surgery facilitated by multichannel electromyographic recording. J Neurosurg. 1999; 91 922-927
- 39 Yoo S S, Talos I F, Golby A J, Black P M, Panych L P. Evaluating requirements for spatial resolution of fMRI for neurosurgical planning. Hum Brain Mapp. 2004; 21 34-43
C. NimskyMD
Department of Neurosurgery · University Erlangen-Nürnberg
Schwabachanlage 6
91054 Erlangen
Germany
Phone: +49/9131/8 53 45 70
Fax: +49/9131/8 53 45 51
Email: nimsky@nch.imed.uni-erlangen.de