Radiology
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Published online before print July 20, 2006, 10.1148/radiol.2403050916
This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
2403050916v1
240/3/849    most recent
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Okada, T.
Right arrow Articles by Togashi, K.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Okada, T.
Right arrow Articles by Togashi, K.
(Radiology 2006;240:849-857.)
© RSNA, 2006

Technical Developments

Corticospinal Tract Localization: Integration of Diffusion-Tensor Tractography at 3-T MR Imaging with Intraoperative White Matter Stimulation Mapping—Preliminary Results1

Tsutomu Okada, MD, Nobuhiro Mikuni, MD, PhD, Yukio Miki, MD, PhD, Ken-ichiro Kikuta, MD, PhD, Shin-ichi Urayama, PhD, Takashi Hanakawa, MD, PhD, Yasutaka Fushimi, MD, Akira Yamamoto, MD, Mitsunori Kanagaki, MD, PhD, Hidenao Fukuyama, MD, PhD, Nobuo Hashimoto, MD, PhD and Kaori Togashi, MD, PhD

1 From the Department of Diagnostic Imaging and Nuclear Medicine (T.O., Y.M., Y.F., A.Y., M.K., K.T.) and Department of Neurosurgery (N.M., K.K., N.H.), Graduate School of Medicine, Kyoto University, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan; and Human Brain Research Center, Kyoto University, Kyoto, Japan (S.U., T.H., H.F.). Received June 2, 2005; revision requested July 21; revision received August 27; accepted September 22; final version accepted October 19. Supported in part by a grant from the Ministry of Health, Labour, and Welfare of Japan (H15-003) and by a grant from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (15591270). Address correspondence to Y.M. (e-mail: mikiy{at}kuhp.kyoto-u.ac.jp).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Institutional review board approval and written informed consent were obtained. The purpose of this study was to prospectively validate usefulness of diffusion-tensor (DT) fiber tractography of the corticospinal tract at 3-T magnetic resonance imaging, in combination with the subcortical motor-evoked potential (MEP) technique, as a tool for tractography-guided neurosurgery. DT imaging and corticospinal tractography were performed at 3 T in eight patients (four men, four women; mean age, 41 years; age range, 23–58 years) with intracranial space-occupying lesions. Tractography data were transferred to a neuronavigation system, and tractography-guided neurosurgery was performed. During lesion resection, subcortical MEPs were recorded. Positive MEP response was observed in four patients. No patients developed new motor weakness postoperatively. Complementary use of tractography and MEP may be useful for intraoperative depiction of corticospinal tracts.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Image-guided neurosurgery is advancing rapidly with regard to the integration of functional and anatomic imaging data (1). Integration of functional and anatomic magnetic resonance (MR) imaging allows visualization of the functionality of gray matter and spatial relationships to tumors. This integrated information is not only applied to presurgical planning but also installed into the neuronavigation system to provide strategies to prevent intraoperative damage of eloquent cortical brain areas (2–5). Major white matter tracts, including the corticospinal tract, must also be preserved to avoid postoperative neurologic deficit.

Diffusion-tensor (DT) MR imaging and fiber tractography can be used to visualize three-dimensional macroscopic fiber tract architectures (6–9). These techniques offer information about eloquent white matter tracts in patients with intracranial space-occupying lesions (10,11) and postoperative reorganization of white matter (12). In addition, eloquent white matter tracts can be visualized intraoperatively by integrating DT fiber tractography and neuronavigation systems. Some reports have already presented the preliminary results of intraoperative corticospinal tract visualization (13–17).

Recording of motor-evoked potential (MEP) has been applied to the depiction of corticospinal tract location during neurosurgery (18,19). Some authors have reported the combination of cortical stimulation and corticospinal tractography (14,15). Intraoperative subcortical white matter stimulation has recently been applied in the evaluation of the subcortical corticospinal tract during brain tumor resection (20). To our knowledge, only one article so far has reported the combination of corticospinal tractography with neuronavigation systems and recording of subcortical MEP during neurosurgery (21), and none have applied 3-T MR imaging to tractography-guided surgery. Thus, the purpose of our study was to prospectively validate the usefulness of 3-T MR corticospinal tractography, in combination with subcortical MEP, as a tool for tractography-guided neurosurgery.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Patients
Between September 2004 and December 2004, 35 consecutive patients with intracranial space-occupying lesions underwent surgery. Among them, eight patients had lesions near the corticospinal tract, on the basis of conventional MR imaging findings, and these eight patients (four men, four women; mean age, 41 years; age range, 23–58 years) were included in our study. Institutional review board approval was obtained for this study. All patients provided written informed consent. All the patients were admitted to our institution for neurosurgery, and routine preoperative evaluations were performed, which included 1.5-T MR imaging. Underlying pathologic conditions included Spetzler-Martin grade 2 ruptured arteriovenous malformation in one patient, cavernous angioma in three patients, and anaplastic astrocytoma in four patients. Patient profiles are listed in Table 1. Three patients (patients 1, 3, and 4) displayed mild hemiparesis contralateral to the affected hemisphere. The remaining patients exhibited no motor weakness. All neurologic examinations were performed by the same neurosurgeon (N.M., with 15 years of clinical experience).


View this table:
[in this window]
[in a new window]

  		Table 1. Clinical Profiles of Patients

 
DT Imaging Data Acquisition
Between 2 and 7 days before surgery, DT imaging and anatomic T1-weighted volume imaging were performed by using a whole-body 3-T MR imager (Trio; Siemens, Erlangen, Germany) with a 40-mT/m gradient. DT imaging was performed by using a single-shot spin-echo echo-planar MR sequence with the following parameters: 5200/79 (repetition time msec/echo time msec), with a motion-probing gradient in 12 noncolinear directions; b value, 700 sec/mm2; matrix, 128 x 128; voxel size, 1.7 x 1.7 x 3 mm; no intersection gap; and four signals acquired. The generalized autocalibrating partial parallel acquisition algorithm was applied for parallel imaging, with a reduction factor of two, an additional 24 autocalibrating phase-encoding lines in the center of k-space, and a 75% partial Fourier technique in the phase-encoding direction. A total of 40 transverse sections were obtained to cover the whole brain. Imaging time was 7 minutes 20 seconds. A magnetization-prepared rapid acquisition gradient-echo sequence was applied for anatomic T1-weighted volume MR data acquisition by using the following parameters: 2000/4.4/990 (repetition time msec/echo time msec/inversion time msec); matrix, 256 x 240; voxel size, 0.9 x 0.9 x 1 mm; and two signals acquired. The generalized autocalibrating partial parallel acquisition algorithm was also applied with a reduction factor of two for the magnetization-prepared rapid acquisition gradient-echo sequence. A total of 208 transverse sections were obtained to cover the whole brain without intersection gaps. Field center was equivalent between the two sequences in each patient. DT imaging was performed by two authors (T.O. and Y.F.), both of whom had 8 years of experience as neuroradiologists and 2 years of experience with DT imaging.

DT Imaging Data Processing
DT imaging data sets were transferred, in Digital Imaging and Communications in Medicine (DICOM) format, to a personal computer workstation equipped with Windows (Microsoft, Redmond, Wash). DtiStudio version 2.02 software (H. Jiang, S. Mori, Department of Radiology, Johns Hopkins University, Baltimore, Md) was used for tensor calculations (7,9). All source images from DT imaging data sets were visually inspected by one author (T.O.), and images with visually apparent artifacts were removed. Because our DT imaging data set exhibited low eddy-current–related geometric distortion between images obtained in each motion-probing gradient direction (22), no postprocessing distortion correction was applied. After calculating the six independent elements of the 3 x 3 tensor and diagonalization, three eigenvalues and eigenvectors were obtained (23–25). The eigenvector associated with the largest eigenvalue was assumed to represent the intravoxel fiber orientation. Fractional anisotropy maps were synthesized from three eigenvalues in each voxel.

Reconstruction at Fiber Tractography
The DtiStudio software was also used to perform fiber tractography based on the fiber assignment by continuous tracking (FACT) method (7,9,26). Fiber tracking was performed from all the pixels inside the brain (ie, with the brute force approach) and was initiated in both retrograde and orthograde directions according to the direction of the principal eigenvector in each voxel. Results that penetrated the manually segmented regions of interest (ROIs) on the basis of known anatomic distributions of tracts were assigned to those specific tracts. Propagation in each fiber tract was terminated if a voxel with a fractional anisotropy of less than 0.2 was reached or if the inner product of two consecutive vectors was greater than 0.75, which prohibited the turning of angles larger than 41° during tracking (9).

To reconstruct the corticospinal tract at tractography, two ROIs were segmented on transverse non–diffusion-weighted MR images (b = 0 sec/mm2): The first ROI was placed in the cerebral peduncles bilaterally and the second was placed in the precentral gyri bilaterally (9,11,22,27). The sizes of ROIs were slightly different in each patient, depending on the shape of the cerebral peduncles and precentral gyri. The size range was 21–26 pixels for the first ROI and 143–173 pixels for the second. "Noise" fibers that were apparently tracing the error course were then removed, such as transcallosal fibers or transverse pontine fibers connecting the right and left corticospinal tracts. Some of these fibers may have represented real fiber connections but were removed because they did not comply with the definition of corticospinal tract. All ROI manipulation was performed by one author (T.O.) who had 2 years of experience with fiber tractography. Preoperative corticospinal tractography was performed successfully in all patients.

Fiber Tractography Data Processing
To convert tractography data into a DICOM-format data set, three processing steps were applied. The first step was to change tractography data to a voxel data set. An 8-bit voxel data set with binary contrast was created from the original tractography data by using the DtiStudio software, with the same matrix size as non–diffusion-weighted images (b = 0 sec/mm2). With this voxelized tractography data set, marked voxels (where fiber tracts penetrate) displayed the largest value, while other voxels displayed the smallest value (28).

The second step was to create merged tractographic images and non–diffusion-weighted images (b = 0 sec/mm2) with the same matrix size as that for magnetization-prepared rapid acquisition gradient-echo images. The three orthogonal coordinates of each voxel on magnetization-prepared rapid acquisition gradient-echo and non–diffusion-weighted images (b = 0 sec/mm2) were obtained from the DICOM header information. The same coordinates as those for non–diffusion-weighted images (b = 0 sec/mm2) were assigned to each corresponding voxel on voxelized tractographic images. The non–diffusion-weighted images and voxelized tractographic images were interpolated by assigning values to each voxel on magnetization-prepared rapid acquisition gradient-echo images. Trilinear interpolation was applied for voxel value calculation. Peak voxel values at voxelized tractography were adjusted to a 5% gain of the maximum value in the non–diffusion-weighted imaging volume data. Mask images were created from voxelized tractography data with a threshold adjusted to half maximum. Merged images were generated from mask images as explained; interpolated tractographic images were assigned to voxels of mask images higher than the threshold, and interpolated non–diffusion-weighted images (b = 0 sec/mm2) were assigned to voxels lower than the threshold.

The third step was to convert merged images into DICOM format according to the magnetization-prepared rapid acquisition gradient-echo header information. DICOM-format tractography studies consisting of 208 sections were obtained. The second and third steps were performed by using original software developed by one author (S.U.).

Preparation in the Navigation System
Magnetization-prepared rapid acquisition gradient-echo images and DICOM-format tractography studies were transferred to the navigation system (StealthStation TRIA plus with Cranial 4.0 software; Medtronic Sofamor-Danek, Memphis, Tenn). ImMerge software, a module in Cranial 4.0 software, was used for nonrigid image fusion based on a mutual information algorithm. Transverse whole-brain computed tomography (CT) scanning (Aquilion; Toshiba Medical Systems, Tokyo, Japan) with contiguous 1-mm-thick sections was performed the day before surgery by attaching six independent scalp point markers to the patient for anatomic registration. Images from CT, magnetization-prepared rapid acquisition gradient-echo MR imaging, and DICOM-format MR tractography were automatically registered in the navigation system by using nonrigid coregistration for distortion correction, and anatomic registration points were verified to minimize navigation errors (Fig 1).


Figure 1
View larger version (55K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1a: Schematic presentation of tractography processing and navigation display in illustrative case in patient 2. (a) Procedure for tractography: Transverse non–diffusion-weighted (b = 0 sec/mm2) MR image (5200/79) and ROIs (blue) segmented at bilateral precentral gyri (top left) and cerebral peduncles (bottom left). Resultant tractography image created with DtiStudio software is shown as a three-dimensional view (red) overlaid on a coronal reconstructed non–diffusion-weighted image (middle) and as a two-dimensional view (red) on a transverse non–diffusion-weighted image (right). (b) Tractography data processing: The first step was to change tractography data to a voxel data set. Bright voxels represent locations of fiber tracts in the volume data (top left). Overlay of voxelized tractography data on non–diffusion-weighted image (top right) reveals location of tracts penetrating both cerebral peduncles. The second step was to create merged images of tractography data and non–diffusion-weighted images. Merged tractographic image has the same matrix size as magnetization-prepared rapid gradient-echo MR images. The third step was to change merged images into DICOM format. Coronal view of DICOM-format tractographic image (bottom left), corresponding view of magnetization-prepared rapid acquisition gradient-echo image (2000/4.4/990; bottom middle), and overlay of DICOM-format tractography image with 50% transparency and magnetization-prepared rapid acquisition gradient-echo image (bottom right) are provided. (c) Operating view of neuronavigation system. Coregistered fusion image with transverse CT, transverse magnetization-prepared rapid acquisition gradient-echo, and DICOM-format tractography data were available in the neuronavigation system. Tractography data were assigned to the "HOTIRON" color scale that was prepared in the neuronavigation system.

 

Figure 1
View larger version (62K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1b: Schematic presentation of tractography processing and navigation display in illustrative case in patient 2. (a) Procedure for tractography: Transverse non–diffusion-weighted (b = 0 sec/mm2) MR image (5200/79) and ROIs (blue) segmented at bilateral precentral gyri (top left) and cerebral peduncles (bottom left). Resultant tractography image created with DtiStudio software is shown as a three-dimensional view (red) overlaid on a coronal reconstructed non–diffusion-weighted image (middle) and as a two-dimensional view (red) on a transverse non–diffusion-weighted image (right). (b) Tractography data processing: The first step was to change tractography data to a voxel data set. Bright voxels represent locations of fiber tracts in the volume data (top left). Overlay of voxelized tractography data on non–diffusion-weighted image (top right) reveals location of tracts penetrating both cerebral peduncles. The second step was to create merged images of tractography data and non–diffusion-weighted images. Merged tractographic image has the same matrix size as magnetization-prepared rapid gradient-echo MR images. The third step was to change merged images into DICOM format. Coronal view of DICOM-format tractographic image (bottom left), corresponding view of magnetization-prepared rapid acquisition gradient-echo image (2000/4.4/990; bottom middle), and overlay of DICOM-format tractography image with 50% transparency and magnetization-prepared rapid acquisition gradient-echo image (bottom right) are provided. (c) Operating view of neuronavigation system. Coregistered fusion image with transverse CT, transverse magnetization-prepared rapid acquisition gradient-echo, and DICOM-format tractography data were available in the neuronavigation system. Tractography data were assigned to the "HOTIRON" color scale that was prepared in the neuronavigation system.

 

Figure 1
View larger version (77K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1c: Schematic presentation of tractography processing and navigation display in illustrative case in patient 2. (a) Procedure for tractography: Transverse non–diffusion-weighted (b = 0 sec/mm2) MR image (5200/79) and ROIs (blue) segmented at bilateral precentral gyri (top left) and cerebral peduncles (bottom left). Resultant tractography image created with DtiStudio software is shown as a three-dimensional view (red) overlaid on a coronal reconstructed non–diffusion-weighted image (middle) and as a two-dimensional view (red) on a transverse non–diffusion-weighted image (right). (b) Tractography data processing: The first step was to change tractography data to a voxel data set. Bright voxels represent locations of fiber tracts in the volume data (top left). Overlay of voxelized tractography data on non–diffusion-weighted image (top right) reveals location of tracts penetrating both cerebral peduncles. The second step was to create merged images of tractography data and non–diffusion-weighted images. Merged tractographic image has the same matrix size as magnetization-prepared rapid gradient-echo MR images. The third step was to change merged images into DICOM format. Coronal view of DICOM-format tractographic image (bottom left), corresponding view of magnetization-prepared rapid acquisition gradient-echo image (2000/4.4/990; bottom middle), and overlay of DICOM-format tractography image with 50% transparency and magnetization-prepared rapid acquisition gradient-echo image (bottom right) are provided. (c) Operating view of neuronavigation system. Coregistered fusion image with transverse CT, transverse magnetization-prepared rapid acquisition gradient-echo, and DICOM-format tractography data were available in the neuronavigation system. Tractography data were assigned to the "HOTIRON" color scale that was prepared in the neuronavigation system.

 
Anesthesia and Subcortical White Matter Stimulation
Cervical epidural recordings were applied in patient 1. Bilateral abductor pollicis brevis, biceps, deltoid, gastrocnemius, quadriceps femoris, and tibialis anterior muscles were chosen for electromyographic recording in patients 2–8. Muscle relaxants were administered only for intubation and not during surgery. A peripheral nerve stimulator was used to confirm a train of four muscle contractions before stimulating the cortex. After craniotomy, cortical motor regions defined by using somatosensory-evoked potential were stimulated to identify positive control of MEP. Transcranial cortical stimulation was applied in patients 3 and 4, who had pontine cavernous angioma, and direct cortical stimulation was applied in the remaining patients for positive-control MEP. During removal of lesions, subcortical electric stimulations were applied repetitively around the area where the corticospinal tract was considered to be close according to tractography guidance visualized with the navigation system.

For patients who were administered general anesthetic (patients 1, 3, and 4), stimulation was performed by using a 2- or 7-mm-wide bipolar electrode that produced a biphasic square-wave pulse to depolarize subcortical fibers. A 2-mm-wide bipolar stimulator was used for the patients with pontine cavernous angioma (patients 3 and 4), and a 7-mm-wide bipolar stimulator was used for the patient with a ruptured right parietal arteriovenous malformation (patient 1). Five train stimuli with an amplitude of 10–30, a duration of 0.3 msec, and an interstimulus interval of 2 msec were applied.

For patients who underwent conscious surgery after administration of local anesthetic (patients 2 and 5–8), a 1-Hz electric current in square waves of alternating polarity with duration of 0.3 msec was delivered to a pair of strip subdural electrodes, 3 mm in diameter, with a center-to-center interelectrode distance of 1 cm. Current was increased in 1-mA increments from 5 mA to a maximum of 15 mA. Duration of stimulation was then increased to a maximum of 5 seconds. If afterdischarges were induced, the test was repeated at the same level of current or at a level of current that was 1 mA lower.

MEP recording was performed by one author (N.M.). In patients with positive MEP response, points of stimulus were confirmed on the navigation system. Distances between points of stimulus and center of the tract were measured on transverse navigation images and were graded as "adjacent" (≤1 cm), "close" (1–2 cm), and "distant" (>2 cm) (Table 2).


View this table:
[in this window]
[in a new window]

  		Table 2. Anesthetic and Stimulation Parameters

 
Postoperative Tractography
Postoperative DT imaging and corticospinal tractography were also performed in all patients. Mean duration between surgery and postoperative DT imaging was 29 days (range, 13–63 days). DT imaging sequence and methods for tractography were equivalent to those for preoperative tractography. Pre- and postoperative tractography images were compared in each patient. Distance between the center of the tract and the nearest portion of the removal margin were measured on transverse non–diffusion-weighted MR images (b = 0 sec/mm2) and were graded as for MEP grading.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Cortical MEP responses for positive control were observed in all patients except for patient 4. Subcortical MEP responses were positive in four patients (patients 1–3 and 8) and were negative in the remaining patients (patients 4–7).

The corticospinal tract at tractography was visualized "adjacent" to the points of stimulus in patients 1 and 3 and "close" to the points of stimulus in patients 2 and 8. At postoperative tractography, the tract was visualized as "adjacent" or "close" to the removal margin, as for points of stimulus. No tract in the affected hemisphere was disrupted or severely narrowed on images at postoperative tractography. Patients 1 and 3 (Fig 2) experienced preoperative motor weakness but improved during postoperative recovery. Patients 2 and 8 did not develop any postoperative neurologic deficit.


Figure 2
View larger version (91K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2a: Images for representative patients with positive MEP response. Images in (a) patient 1 and (b) patient 3 each show preoperative three-dimensional tractography data (red) on coronal reconstructed non–diffusion-weighted MR image (top left) and two-dimensional tractography data on transverse non–diffusion-weighted image (5200/79, top right), navigation image with red cross showing the point of stimulus (middle left) and recorded MEP wave (middle right), and postoperative three-dimensional tractography data on coronal reconstructed non–diffusion-weighted image (bottom left) and two-dimensional tractography data on transverse non–diffusion-weighted image (5200/79, bottom right). Navigation images are inverted from a superior-inferior view to an inferior-superior view, to be the same as other images. Arrow indicates location of cavernous angioma in patient 3. D-wave was recorded in patient 1 for positive epidural MEP response, and positive MEP response at electromyography was recorded in patient 3. Locations of electrodes are shown: RAPB = right abductor pollicis brevis muscle, RGC = right gastrocnemius muscle. The point of stimulus was graded "adjacent" to the center of the tract in both patients.

 

Figure 2
View larger version (86K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2b: Images for representative patients with positive MEP response. Images in (a) patient 1 and (b) patient 3 each show preoperative three-dimensional tractography data (red) on coronal reconstructed non–diffusion-weighted MR image (top left) and two-dimensional tractography data on transverse non–diffusion-weighted image (5200/79, top right), navigation image with red cross showing the point of stimulus (middle left) and recorded MEP wave (middle right), and postoperative three-dimensional tractography data on coronal reconstructed non–diffusion-weighted image (bottom left) and two-dimensional tractography data on transverse non–diffusion-weighted image (5200/79, bottom right). Navigation images are inverted from a superior-inferior view to an inferior-superior view, to be the same as other images. Arrow indicates location of cavernous angioma in patient 3. D-wave was recorded in patient 1 for positive epidural MEP response, and positive MEP response at electromyography was recorded in patient 3. Locations of electrodes are shown: RAPB = right abductor pollicis brevis muscle, RGC = right gastrocnemius muscle. The point of stimulus was graded "adjacent" to the center of the tract in both patients.

 
Among the four patients with negative MEP response, removal margin and tract at postoperative tractography were both "distant" in patient 5 (Fig 3, Table 3); in the remaining three patients, results were categorized as "close" for both. Patient 4 experienced preoperative motor weakness, and symptoms did not change during postoperative recovery. Patients 5–7 did not develop postoperative motor weakness.


Figure 3
View larger version (133K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3a: Images for representative patients with negative MEP response. Images in (a) patient 5 and (b) patient 6 each show preoperative three-dimensional tractography data (red) on coronal reconstructed non–diffusion-weighted MR image (top left) and two-dimensional tractography data on transverse non–diffusion-weighted image (5200/79; top right), and postoperative three-dimensional tractography data on coronal reconstructed non–diffusion-weighted image (bottom left) and two-dimensional tractography data on transverse non–diffusion-weighted image (bottom right). The center of the tract was graded "distant" to the nearest portion of the removal margin in patient 5 and "close" in patient 6.

 

Figure 3
View larger version (136K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3b: Images for representative patients with negative MEP response. Images in (a) patient 5 and (b) patient 6 each show preoperative three-dimensional tractography data (red) on coronal reconstructed non–diffusion-weighted MR image (top left) and two-dimensional tractography data on transverse non–diffusion-weighted image (5200/79; top right), and postoperative three-dimensional tractography data on coronal reconstructed non–diffusion-weighted image (bottom left) and two-dimensional tractography data on transverse non–diffusion-weighted image (bottom right). The center of the tract was graded "distant" to the nearest portion of the removal margin in patient 5 and "close" in patient 6.

 

View this table:
[in this window]
[in a new window]

  		Table 3. Subcortical MEP, Preoperative Motor Weakness, and Postoperative Course

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
Intracranial space-occupying lesions located in the eloquent brain area remain a challenge from the perspective of surgical removal with preservation of brain function. Image-guided neurosurgery is a tool that can help to prevent damage to the eloquent cortical and white matter areas. We have visualized corticospinal tracts by using 3-T DT MR imaging with the navigation system to provide tractography-guided neurosurgery. Although 1.5-T DT imaging and fiber tractography have already been reported for use with navigation systems (13–16,21), to our knowledge this is the first report to introduce 3-T DT imaging and fiber tractography in a navigation system. Although the advantages of 3-T MR fiber tractography over 1.5-T systems have not been fully established in patients with space-occupying lesions, the better depiction of DT fiber tracts at 3 T compared with 1.5 T in healthy subjects has already been demonstrated (29). High-spatial-resolution DT imaging and fiber tractography at 3 T MR imaging have been reported (30,31). The combination of subcortical MEP and tractography during neurosurgery has already been reported (21,32).

Kinoshita et al (32) did not apply tractography with the navigation system to compare points of stimulus and the tract. Kamada et al (21) visualized voxelized tractographic images with the navigation system, but they transformed tractography data together with non–diffusion-weighted (b = 0 sec/mm2) images into anatomic volume data and then merged tractography data with volume data. This means that two registration processes had to be applied from voxelized tractography data by means of anatomic volume data to volume CT data. Our merged images were based on non–diffusion-weighted (b = 0 sec/mm2) images. Magnetization-prepared rapid acquisition gradient-echo and merged MR images were registered to volume CT images in a single registration process, so misregistration would presumably be minimized.

In our study, the corticospinal tract at tractography was considered "adjacent" or "close" to the point of stimulus in all four patients with positive MEP responses. These results are compatible with those in previous reports (14,21). While two patients experienced preoperative motor weakness, symptoms improved during postoperative recovery. Of these four patients, three had noninfiltrating vascular lesions (cavernous angioma and arteriovenous malformation) and one had an infiltrating glioma. Among the four patients with negative MEP responses, the tract at postoperative tractography was "close" to the removal cavity in three patients (two patients with glioma and one patient with cavernous angioma) and was "distant" in one patient with glioma.

Although our experience is limited, corticospinal tractography in patients with noninfiltrating space-occupying lesions is more likely to represent a precise localization than infiltrating tumor. Mass displacement or vasogenic edema affects fiber depiction in patients with noninfiltrating space-occupying lesions (11). In addition, disruption and infiltration affect fiber depiction in patients with infiltrating tumor. The principal eigenvector and local anisotropy are distorted in the presence of infiltrating tumor. Future advances in tractography algorithms can be expected to depict topographic and pathologic changes in fibers surrounding infiltrating brain tumor.

Both successful results (10,15,16,21) and an unsuccessful result (32) have been reported in the combination of tractography and neurosurgery for brain tumors. No patient had deteriorating motor weakness during postoperative recovery in our study. On the basis of our results, although tractography in patients with infiltrating brain tumor is still being developed, assessment of tractography data in comparison with the known anatomic distribution of fiber tracts and careful interpretation of MEP results offers the possibility of preserving motor function during neurosurgery. Intraoperative electrophysiologic monitoring, including MEP, is relatively well established but remains an invasive and complicated procedure. Although validation of diagnostic accuracy is under way, tractography is supposed to be a noninvasive method with less technical error than electrophysiologic monitoring. Furthermore, tractographic images visualized with the navigation system provide interactive information on fiber tracts, which benefits neurosurgeons by depicting the course of eloquent fiber tracts during the surgery. Complementary use of tractography and MEP is recommended to preserve eloquent white matter.

While the use of DT imaging and tractography-guided neurosurgery is considered to be promising, our methods have some limitations. First, imaging distortion and the relatively lower signal-to-noise ratio of DT imaging represent major problems. We have already applied 3-T MR with parallel imaging as a solution, but 3-T MR imaging inevitably has a higher level of imaging distortion than does 1.5-T MR imaging, especially in the area near the skull base. We applied nonrigid coregistration between non–diffusion-weighted (b = 0 sec/mm2) MR imaging and CT for distortion correction. Nevertheless, some distortion may possibly remain. Further optimization and technical advances in 3-T MR imaging sequences may be required in the future to reduce the image distortion in DT imaging.

The second limitation is that tractographic image reconstruction is not a precise stepwise procedure with a reproducible outcome but is dependent on manipulation of ROIs. Combination with functional information derived from functional MR imaging (15,16) or magnetoencephalography will facilitate more objective ROI segmentation. Tractography results are also dependent on the tracking algorithm, threshold of fractional anisotropy, or angles between the two contiguous steps. It has been reported that fractional anisotropy has changed in infiltrating peritumoral white matter (33). Tracking results may change in regions with lower fractional anisotropy, such as tumor infiltration areas or crossing fiber areas where the corticospinal tract intersects with callosal fibers at the level of the centrum semiovale. We applied a two-ROI and brute force approach for the FACT algorithm to increase the validity of DT tractography rather than the single-ROI approach (34). Probabilistic tractography (35) and diffusion spectrum imaging (36) have been reported to help visualize detailed cortical connectivity, but they require increased calculation power and time. The FACT method does not require too much calculation power, and intraoperative recalculation is acceptable. Future advance in computation may bring new algorithms into clinical practice, but the FACT method remains clinically feasible.

Intraoperative brain shift represents the third limitation. Brain volume may change after craniotomy because of tumor reduction, brain perfusion, patient ventilation, and tissue damage. Deep brain structures can shift inward or outward, which results in misregistration between images at tractography and in vivo fiber tracts. Intraoperative DT imaging and tractography (16,17) or intraoperative ultrasonography (37) can be used to update the shifted fiber location and provide more reliable information. The DtiStudio software and our software for converting tractography data are installed on a single personal computer and are easy to use with the intraoperative environment.

In conclusion, we have attempted to establish the integration of tractography and intraoperative subcortical MEP. Complementary use of tractography and MEP may contribute to preventing intraoperative damage of the corticospinal tract during neurosurgical resection of intracranial space-occupying lesions.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
References
 


   ACKNOWLEDGMENTS
 
The authors thank Susumu Mori, PhD, Shigeki Aoki, MD, PhD, and Kei Yamada, MD, PhD, for their technical advice with regard to tractography and Namiko Nishida, MD, Junya Taki, MD, Rei Enatsu, MD, Akio Ikeda, MD, PhD, and Riki Matsumoto, MD, PhD, for their contribution in performing MEP procedures.


   FOOTNOTES
 

Abbreviations: DICOM = Digital Imaging and Communications in Medicine • DT = diffusion tensor • FACT = fiber assignment by continuous tracking • MEP = motor-evoked potential • ROI = region of interest

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, T.O., Y.M., K.T.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, Y.M., Y.F., M.K., K.T.; clinical studies, all authors; and manuscript editing, T.O., N.M., Y.M., K.K., S.U., T.H., Y.F., A.Y., M.K., H.F., K.T.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

  1. Schulder M, Maldjian JA, Liu WC, et al. Functional image-guided surgery of intracranial tumors located in or near the sensorimotor cortex. J Neurosurg 1998;89:412–418.[Medline]
  2. Nimsky C, Ganslandt O, Fahlbusch R. Functional neuronavigation and intraoperative MRI. Adv Tech Stand Neurosurg 2004;29:229–263.[Medline]
  3. Kober H, Nimsky C, Vieth J, Fahlbusch R, Ganslandt O. Co-registration of function and anatomy in frameless stereotaxy by contour fitting. Stereotact Funct Neurosurg 2002;79:272–283.[CrossRef][Medline]
  4. Nimsky C, Ganslandt O, Kober H, et al. Integration of functional magnetic resonance imaging supported by magnetoencephalography in functional neuronavigation. Neurosurgery 1999;44:1249–1255.[CrossRef][Medline]
  5. Bittar RG, Olivier A, Sadikot AF, et al. Localization of somatosensory function by using positron emission tomography scanning: a comparison with intraoperative cortical stimulation. J Neurosurg 1999;90:478–483.[Medline]
  6. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med 2000;44:625–632.[CrossRef][Medline]
  7. Mori S, van Zijl PC. Fiber tracking: principles and strategies—a technical review. NMR Biomed 2002;15:468–480.[CrossRef][Medline]
  8. Dong Q, Welsh RC, Chenevert TL, et al. Clinical applications of diffusion tensor imaging. J Magn Reson Imaging 2004;19:6–18.[CrossRef][Medline]
  9. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology 2004;230:77–87.[Abstract/Free Full Text]
  10. Clark CA, Barrick TR, Murphy MM, Bell BA. White matter fiber tracking in patients with space-occupying lesions of the brain: a new technique for neurosurgical planning? Neuroimage 2003;20:1601–1608.[CrossRef][Medline]
  11. Yamada K, Kizu O, Mori S, et al. Brain fiber tracking with clinically feasible diffusion-tensor MR imaging: initial experience. Radiology 2003;227:295–301.[Abstract/Free Full Text]
  12. Lazar M, Thottakara P, Field AS, et al. A white matter tractography study of white matter reorganization after surgical resection of brain neoplasms [abstract]. In: Proceedings of the 12th Meeting of the International Society for Magnetic Resonance in Medicine. Berkeley, Calif: International Society for Magnetic Resonance in Medicine, 2004; 1259.
  13. Coenen VA, Krings T, Mayfrank L, et al. Three-dimensional visualization of the pyramidal tract in a neuronavigation system during brain tumor surgery: first experiences and technical note. Neurosurgery 2001;49:86–92.[CrossRef][Medline]
  14. Coenen VA, Krings T, Axer H, et al. Intraoperative three-dimensional visualization of the pyramidal tract in a neuronavigation system (PTV) reliably predicts true position of principal motor pathways. Surg Neurol 2003;60:381–390.[CrossRef][Medline]
  15. Berman JI, Berger MS, Mukherjee P, Henry RG. 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.[Medline]
  16. Nimsky C, Ganslandt O, Hastreiter P, et al. Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 2005;56:130–137.[Medline]
  17. Nimsky C, Ganslandt O, Hastreiter P, et al. Intraoperative diffusion-tensor MR imaging: shifting of white matter tracts during neurosurgical procedures—initial experience. Radiology 2005;234:218–225.[Abstract/Free Full Text]
  18. Legatt AD, Emerson RG. Motor evoked potential monitoring: it's about time. J Clin Neurophysiol 2002;19:383–386.[Medline]
  19. Legatt AD. Current practice of motor evoked potential monitoring: results of a survey. J Clin Neurophysiol 2002;19:454–460.[Medline]
  20. 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;100:369–375.[Medline]
  21. Kamada K, Todo T, Masutani Y, et al. Combined use of tractography-integrated functional neuronavigation and direct fiber stimulation. J Neurosurg 2005;102:664–672.[Medline]
  22. Naganawa S, Koshikawa T, Kawai H, et al. Optimization of diffusion-tensor MR imaging data acquisition parameters for brain fiber tracking using parallel imaging at 3 T. Eur Radiol 2004;14:234–238.[CrossRef][Medline]
  23. Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J 1994;66:259–267.[Medline]
  24. Beaulieu C. The basis of anisotropic water diffusion in the nervous system: a technical review. NMR Biomed 2002;15:435–455.[CrossRef][Medline]
  25. Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology 1996;201:637–648.[Abstract/Free Full Text]
  26. Stieltjes B, Kaufmann WE, van Zijl PC, et al. Diffusion tensor imaging and axonal tracking in the human brainstem. Neuroimage 2001;14:723–735.[CrossRef][Medline]
  27. Kunimatsu A, Aoki S, Masutani Y, Abe O, Mori H, Ohtomo K. Three-dimensional white matter tractography by diffusion tensor imaging in ischaemic stroke involving the corticospinal tract. Neuroradiology 2003;45:532–535.[CrossRef][Medline]
  28. Masutani Y, Aoki S, Abe O, Hayashi N, Otomo K. MR diffusion tensor imaging: recent advance and new techniques for diffusion tensor visualization. Eur J Radiol 2003;46:53–66.[CrossRef][Medline]
  29. Okada T, Miki Y, Fushimi Y, et al. Diffusion-tensor fiber tractography: intraindividual comparison of 3.0-T and 1.5-T MR imaging. Radiology 2006;238(2):668–678.[Abstract/Free Full Text]
  30. Jaermann T, Crelier G, Pruessmann KP, et al. SENSE-DTI at 3 T. Magn Reson Med 2004;51:230–236.[CrossRef][Medline]
  31. Nagae-Poetscher LM, Jiang H, Wakana S, Golay X, van Zijl PC, Mori S. High-resolution diffusion tensor imaging of the brain stem at 3 T. AJNR Am J Neuroradiol 2004;25:1325–1330.[Abstract/Free Full Text]
  32. Kinoshita M, Yamada K, Hashimoto N, et al. Fiber-tracking does not accurately estimate size of fiber bundle in pathological condition: initial neurosurgical experience using neuronavigation and subcortical white matter stimulation. Neuroimage 2005;25:424–429.[CrossRef][Medline]
  33. Lu S, Ahn D, Johnson G, Law M, Zagzag D, Grossman RI. Diffusion-tensor MR imaging of intracranial neoplasia and associated peritumoral edema: introduction of the tumor infiltration index. Radiology 2004;232:221–228.[Abstract/Free Full Text]
  34. Huang H, Zhang J, van Zijl PC, Mori S. Analysis of noise effects on DTI-based tractography using the brute-force and multi-ROI approach. Magn Reson Med 2004;52:559–565.[CrossRef][Medline]
  35. Behrens TE, Woolrich MW, Jenkinson M, et al. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 2003;50:1077–1088.[CrossRef][Medline]
  36. Lin CP, Wedeen VJ, Chen JH, Yao C, Tseng WY. Validation of diffusion spectrum magnetic resonance imaging with manganese-enhanced rat optic tracts and ex vivo phantoms. Neuroimage 2003;19:482–495.[CrossRef][Medline]
  37. Coenen VA, Krings T, Weidemann J, et al. Sequential visualization of brain and fiber tract deformation during intracranial surgery with three-dimensional ultrasound: an approach to evaluate the effect of brain shift. Neurosurgery 2005;56:133–141.[CrossRef][Medline]



This article has been cited by other articles:


Home page
 Cereb CortexHome page
P.J. Wrigley, S.M. Gustin, P.M. Macey, P.G. Nash, S.C. Gandevia, V.G. Macefield, P.J. Siddall, and L.A. Henderson
Anatomical Changes in Human Motor Cortex and Motor Pathways following Complete Thoracic Spinal Cord Injury
Cereb Cortex, January 1, 2009; 19(1): 224 - 232.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Neuroradiol.Home page
T. Taoka, M. Sakamoto, H. Nakagawa, H. Nakase, S. Iwasaki, K. Takayama, K. Taoka, T. Hoshida, T. Sakaki, and K. Kichikawa
Diffusion Tensor Tractography of the Meyer Loop in Cases of Temporal Lobe Resection for Temporal Lobe Epilepsy: Correlation between Postsurgical Visual Field Defect and Anterior Limit of Meyer Loop on Tractography
AJNR Am. J. Neuroradiol., August 1, 2008; 29(7): 1329 - 1334.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
K. Fujiyoshi, M. Yamada, M. Nakamura, J. Yamane, H. Katoh, K. Kitamura, K. Kawai, S. Okada, S. Momoshima, Y. Toyama, et al.
In Vivo Tracing of Neural Tracts in the Intact and Injured Spinal Cord of Marmosets by Diffusion Tensor Tractography
J. Neurosci., October 31, 2007; 27(44): 11991 - 11998.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurol. Neurosurg. PsychiatryHome page
N. Mikuni, T. Okada, R. Enatsu, Y. Miki, S.-i. Urayama, J. A Takahashi, K. Nozaki, H. Fukuyama, and N. Hashimoto
Clinical significance of preoperative fibre-tracking to preserve the affected pyramidal tracts during resection of brain tumours in patients with preoperative motor weakness
J. Neurol. Neurosurg. Psychiatry, July 1, 2007; 78(7): 716 - 721.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Neuroradiol.Home page
T. Okada, Y. Miki, K. Kikuta, N. Mikuni, S. Urayama, Y. Fushimi, A. Yamamoto, N. Mori, H. Fukuyama, N. Hashimoto, et al.
Diffusion Tensor Fiber Tractography for Arteriovenous Malformations: Quantitative Analyses to Evaluate the Corticospinal Tract and Optic Radiation
AJNR Am. J. Neuroradiol., June 1, 2007; 28(6): 1107 - 1113.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
2403050916v1
240/3/849    most recent
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Okada, T.
Right arrow Articles by Togashi, K.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Okada, T.
Right arrow Articles by Togashi, K.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
RADIOLOGY RADIOGRAPHICS RSNA JOURNALS ONLINE