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Neuroradiology |
1 From the Department of Neurosurgery, University Erlangen-Nürnberg, Schwabachanlage 6, 91054 Erlangen, Germany (C.N., O.G., P.H., R.F.); and Department of Radiology, Athinoula A. Martinos Center, Massachusetts General Hospital, Boston, Mass (R.W., T.B., A.G.S.). Received December 8, 2003; revision requested February 13, 2004; revision received February 27; accepted March 29. Supported in part by grants from the U.S. Public Health Service (P41-RR14075, M01-RR001066, NS-038477) and by the Deutsche Forschungsgemeinschaft. Address correspondence to C.N. (e-mail: nimsky@nch.imed.uni-erlangen.de).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Ethical committee approval and signed informed consent were obtained. A 1.5-T magnetic resonance imager with an adapted rotating surgical table that is placed in a radiofrequency-shielded operating theater was used for pre- and intraoperative imaging. DTI was performed by applying an echo-planar imaging sequence with six diffusion directions in 38 patients (20 female patients, 18 male patients; age range, 7–77 years; mean age, 45.6 years) who were undergoing surgery (35 craniotomy and three burr hole procedures). Color-encoded maps of fractional anisotropy were generated by depicting white matter tracts. A rigid registration algorithm was used to compare pre- and intraoperative images.
RESULTS: Intraoperative DTI was technically feasible in all patients, and no major image distortions occurred in the areas of interest. Pre- and intraoperative color-encoded maps of fractional anisotropy could be registered; these maps depicted marked and highly variable shifting of white matter tracts during neurosurgical procedures. In the 27 patients who underwent brain tumor resection, white matter tract shifting ranged from an inward shift of 8 mm to an outward shift of 15 mm (mean shift ± standard deviation, outward shift of 2.5 mm ± 5.8). In 16 (59%) of 27 patients, outward shifting was detected; in eight (30%), inward shifting was detected. In eight patients who underwent temporal lobe resections for drug-resistant epilepsy, shifting was only inward and ranged from 2 to 14 mm (9 mm ± 3.3). In two of the three patients who underwent burr hole procedures, outward shifting occurred.
CONCLUSION: Intraoperative DTI can depict shifting of major white matter tracts that is caused by surgical intervention.
© RSNA, 2004
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The integration of functional data obtained with magnetoencephalography and functional MR imaging into the navigational data sets for identification of eloquent brain areas allowed their preservation, which resulted in reduced postoperative neurologic deficits (7–9). These modalities, however, could be used only in the identification of the functional areas at the cortical surface. To avoid postoperative neurologic deficits, it is also necessary to preserve major white matter tracts, such as the pyramidal tract. Diffusion-weighted MR imaging was used to approximate the location of the pyramidal tract (10); these data were integrated into preoperative data sets, which were then used for navigation, so that the pyramidal tract could be identified during brain tumor resection (11,12).
Diffusion-tensor imaging (DTI) can assist resolution of the dominant fiber orientation in each voxel element by aiding in the measurement of the self-diffusion properties (eg, brownian motion of water molecules). Diffusion is anisotropic (eg, orientation dependent) in areas with a strong aligned microstructure. The direction of greatest diffusion measured with DTI parallels the dominant orientation of the tissue structure in each voxel, representing the mean longitudinal direction of axons in white matter tracts (13,14). DTI can be used in the identification of white matter tracts, such as the pyramidal tract, in patients with brain tumors. It may depict the normal course, displacement, or interruption of white matter tracts around a tumor and the widening of fiber bundles due to edema or tumor infiltration (15–23).
Advances in imager design, including those due to active magnetic shielding, have made it possible to adapt modern high-field-strength MR imagers to the surgical environment (1,5,24). In our setup, a rotating table that is adapted to the imager simultaneously serves as both the MR table and the surgical table. Surgery is performed with the head placed in the fringe field of the imager at the 0.5-mT line; for intraoperative imaging, the table is rotated into the imager (24,25). The successful integration of a high-field-strength imager into the operating room allowed us to consider the intraoperative application of DTI. Thus, the purpose of our study was to prospectively evaluate the localization of white matter tracts with DTI during neurosurgical procedures.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Operating Room Setup
The 1.5-T MR imager (Magnetom Sonata Maestro Class; Siemens Medical Solutions, Erlangen, Germany) is installed in an operating room with radiofrequency shielding. It is a high-field-strength MR imager, with a superconductive 1.5-T magnet that has a length of 160 cm and an inner bore diameter of 60 cm. This imager is equipped with a gradient system with a field strength of up to 40 mT/m (effective field strength, 69 mT/m) and a slew rate of up to 200 T/m/sec (effective slew rate, 346 T/m/sec). A surgical table (Trumpf, Saalfeld, Germany) that can be rotated is adapted to the imager to allow for a special surgical MR tabletop. This surgical table can be locked into various positions. The principal surgical position is 160°, with the head of the patient at the 0.5-mT line. For anesthesia, MR-compatible ventilation and monitoring equipment are used (26). An MR-compatible four-point head holder, which is made of fiberglass and reinforced with plastic, is integrated into the head coil for head fixation. The upper part of the head coil may be sterilized with plasma sterilization. Sterile adapters placed onto the lower part of the head coil assure the possibility of sterile draping (24,25).
Timing of intraoperative MR imaging was decided by the neurosurgeon (C.N. and R.F.). MR imaging was performed either when the surgeon had the impression that the goal of surgery was met (eg, complete tumor resection) or when a marked brain shift necessitated updating of the navigation system (27,28). Prior to imaging, the surgical resection cavity was covered with a piece of gelfoam, and sterile draping was placed over the coil after the sterile upper part of the head coil was locked.
MR Imaging and Data Processing
We used a single-shot spin-echo diffusion-weighted echo-planar imaging sequence (repetition time msec/echo time msec, 9200/86; matrix size, 128 x 128; field of view, 240 mm; section thickness, 1.9 mm; bandwidth, 1502 Hz/pixel). This sequence is based on a balanced diffusion gradient design that strongly minimizes eddy-current artifacts when compared with a single refocused design. Diffusion weighting of 1000 sec/mm2 (high b value) was used. One null image (low b value of 0 sec/mm2) and six diffusion-weighted images were obtained with the diffusion-encoding gradients directed along the (±1, 1, 0), (±1, 0, 1), and (1, ±1, 0) axes. The voxel size was 1.9 x 1.9 x 1.9 mm, and 60 sections with no intersection gap were measured. By applying five averages, total DTI measurement required 5 minutes 31 seconds.
DTI maps were calculated by using the DTI task card, version 1.60—which was developed at the Magnetic Resonance Center of Massachusetts General Hospital, Boston—and a 1.5-T MR imager with imaging software (MRease N4_VA21B under syngo VB10I; Siemens Medical Solutions). Diffusion-tensor information was then represented as color-encoded fractional anisotropy maps, apparent diffusion coefficient maps, and three maps of each eigenvalue of the diffusion tensor. Color-encoded fractional anisotropy maps were generated by mapping the principal eigenvector components into red, green, and blue color channels, which were weighted with fractional anisotropy. By assuming that the patient is lying in the supine position and his or her head is not tilted, color mapping depicts white matter tracts oriented in an anterior-to-posterior direction as green, in a left-to-right direction as red, and in a superior-to-inferior direction as blue (29–31). Furthermore, representations of the diffusion tensor as boxes or ellipsoids were possible, providing an intuitive interpretation of eigenvectors and eigenvalues. The eigenvector associated with the largest eigenvalue indicates the predominant orientation in a given voxel. The color-encoded fractional anisotropy maps of the principal eigenvector (eg, the eigenvector corresponding to the largest eigenvalue) were used for further evaluation.
Pre- and intraoperative images were registered with image fusion software (VectorVision2 Planning 1.3; BrainLab, Heimstetten, Germany), which is used to perform semiautomatic rigid registration. For example, after rough alignment by the user, images are registered with software by using a rigid registration algorithm that applies an intensity-based pyramidal approach and uses mutual information, with subpixel registration accuracy (32,33). After registration, the images could be displayed side by side or in an overlay mode, with adjustable weighting of the corresponding images. This allowed visual confirmation of the registration. Furthermore, Amira 3.0 software (Indeed Visual Concept, Berlin, Germany) was used to apply a grid scale, which allowed us to measure the displacement of white matter tracts after pre- and intraoperative images had been registered. For better visualization, the displaced major white matter tracts were segmented manually in consensus (C.N. and O.G., with 14 and 12 years of experience, respectively, with brain MR imaging); thereafter, pre- and intraoperative contours of white matter tracts were displayed with the grid scale.
In 24 patients (22 were undergoing tumor resections and two were undergoing a burr hole procedure), the pyramidal tract was evaluated; in six (five were undergoing tumor resections and one was undergoing a burr hole procedure), the corpus callosum was evaluated; and in eight patients undergoing temporal lobe resection for drug-resistant epilepsy, the optic tract was evaluated. The maximum intraoperative shift of white matter tracts was measured. Positive or negative values were assigned according to the direction of the shift, which was referred to the craniotomy opening. A positive value was assigned if movement was toward the surface (eg, swelling), and a negative value was assigned if movement was inward (27).
Data were summarized in three patient groups: those undergoing brain tumor resection, those undergoing burr hole procedures, and those undergoing temporal lobe resection for treatment of drug-resistant epilepsy. In a selected illustrative case, a DTI measurement was obtained at 3-month follow-up and compared with the preoperative image. By assuming that the brain hemisphere opposite the lesion is not much affected by the brain shift, the position of the pyramidal tract in the region of the internal capsule of the unaffected hemisphere was compared between the registered pre- and intraoperative images. The maximum distance was measured in each patient as an estimate for the registration accuracy.
The pre- and intraoperative color-encoded fractional anisotropy maps were displayed during surgery, so that the neurosurgeon could adapt his surgical strategy and account for the actual location of major white matter tracts. All procedures were analyzed for complications related directly to the imaging procedure. Furthermore, a follow-up neurologic examination was performed on the day after surgery and at discharge. Each patient’s postoperative status was compared with his or her preoperative status, and patient records were reviewed for late complications, such as wound infections. Recurrence of bleeding, neurologic deficits, any accidents due to the magnetic field, and all complications, such as wound infections, that necessitated additional surgery were considered major complications.
Technical Issues
All DTI measurements were technically feasible. Image distortion caused by the head fixation pins did not interfere with visualization of the pyramidal tract and other major fiber tract systems near the lesion in which surgery was performed. The open skull did not result in major image distortion. A challenge of intraoperative DTI is that the head is not always in a standard position. For example, if a lesion is located in the temporal lobe, a horizontal or tilted head position is necessary during surgery, so that the color encoding is not the same in pre- and intraoperative measurements. This problem could be solved either by measuring preoperative images obtained after induction of anesthesia and head fixation, so that pre- and intraoperative head positions were identical, or by changing the color encoding scheme in case of a well-defined head rotation (eg, 90° rotation).
A new version of the DTI task card software allows arbitrary section orientations and diffusion gradient direction to be taken into account. A calculation time of about 30 seconds for the color-encoded fractional anisotropy maps was needed so that all postprocessing could be performed intraoperatively. Image registration and calculation of maximum shifting added about 5 minutes.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In the 27 patients with brain tumor who were undergoing craniotomy, we observed an outward shift during surgery in 16 (59%) and an inward shift during surgery in eight (30%). In the three remaining patients (11%), no intraoperative displacement was detected. The shift ranged from an inward shift of 8 mm to an outward shift of 15 mm (mean ± standard deviation, outward shift of 2.5 ± 5.8 mm). In two of the three patients who underwent the burr hole procedure, marked outward shifting of 2 and 6 mm occurred. This shift was due to volume reduction of cystic lesions during the burr hole procedure; thus, displacement of white matter tracts resulted.
Figures 1–3 show images obtained in a 29-year-old man with a large grade III right temporoparietal oligoastrocytoma, which resulted in distinct displacement of the pyramidal tract to the midline. During tumor removal, repeated imaging was performed, which depicted outward shifting of the pyramidal tract (Fig 2). Comparison of the first and last intraoperative images showed an outward shift of 13 mm. Compared with the preoperative image, even an outward shift of 15 mm was detectable. In the postoperative period, the pyramidal tract nearly regained its normal position; thus, the comparison of preoperative data with data obtained at 3-month follow-up revealed a displacement of 20 mm. A patient with a glioma in the temporal lobe, which resembled the tumor seen in Figures 1–3 with a displacement of the pyramidal tract to the midline, demonstrates the opposite behavior, with a further 6-mm inward shift of the pyramidal tract after tumor removal (Fig 4). Figure 5 shows the displacement of the corpus callosum, which resolves nearly completely after tumor removal, in another patient. This figure also allows us to estimate the satisfying registration accuracy of pre- and intraoperative DTI data, since the segmented structures overlap well in the posterior portion of the corpus callosum. The corpus callosum is distant to the surgical site; thus, it is not influenced by brain shift.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MR imaging is implemented in a variety of neurosurgical operating theaters for intraoperative imaging with systems of various configurations and field strengths (1–6). Intraoperative MR imaging is used mainly to delineate the extent of a resection and monitor surgical complications; lesion localization is possible when MR imaging is used as a navigational device. To our knowledge, Mamata et al (34) were the first to report the possibility of using line-scan diffusion imaging and a 0.5-T interventional MR imaging system to detect intraoperative changes in fiber orientation that were caused by surgically induced brain deformation.
We applied pre- and intraoperative DTI in 38 patients by using a 1.5-T MR imaging system, which was adapted to the neurosurgical operating room environment (24,25). Despite the open skull, intraoperative DTI was possible. No major image distortion occurred in the areas of interest near the resection border. Only the head fixation pins, which are made of titanium, produced major susceptibility artifacts, which resulted in image distortion near the head fixation; however, registration of pre- and intraoperative images was not impaired. The application of alternative imaging methods for DTI may solve this problem (35–37).
Registration of pre- and intraoperative DTI data sets showed a marked individually unpredictable shifting of major white matter tracts; this shift was due to bulk removal of tumor or functionally abnormal brain tissue at surgery for drug-resistant epilepsy. Distinct intraoperative shifting may occur in patients who underwent craniotomy and burr hole procedures. In patients with nonlesional epilepsy who are undergoing tailored temporal lobe resections, the ventricular system is routinely opened; thus, the loss of cerebrospinal fluid results in inward shifting of the brain. Accordingly, in all patients, inward shift of the optic radiation was measured; however, the extent of the inward shift was quite variable and ranged from 2 to 14 mm. In patients undergoing brain tumor resection, the variability was much greater and ranged from an outward shift of 15 mm to an inward shift of 8 mm. In 59% of these patients, an outward movement occurred; in 30%, an inward movement occurred.
Regarding the accuracy of measurement of the extent of white matter shifting, there might be a certain bias toward overestimation of brain shift because of the manual segmentation process. It should be noted, however, that the overall extent of shifting of major white matter tracts, as depicted by DTI, and the unpredictable direction and interindividual variability of shifting (mean resection of brain tumors ± standard deviation, outward shift of 2.5 mm ± 5.8) corresponds well to previous data pertaining to outward brain shift of the deep tumor margin (27,38), which was reported to be approximately 4.4 mm ± 6.8 (27). These data were already used to emphasize the fact that navigation systems that rely on only preoperative data lose accuracy during ongoing surgery. Thus, at the critical steps of tumor resection (eg, reaching the deep margin, which may be close or even inside important white matter tracts), the navigation system cannot be used for reliable guidance.
Until now, integration of functional data from magnetoencephalography and functional MR imaging leading to functional neuronavigation were used only to identify eloquent brain areas at the cortical surface (8,9,39). Thus, integration of DTI data into neuronavigation systems that depict the location of the pyramidal tract is highly relevant. First attempts with diffusion-weighted MR images in a stereotactic setting were implemented to prevent damaging of deep-seated eloquent structures (11,12). As illustrated in our study, marked and unpredictable shifting of deep brain structures necessitates intraoperative updating of the navigation system if data obtained in white matter tracts is to be of use when integrated into navigation systems.
Despite increasingly sophisticated mathematic models used to describe the brain shift phenomenon, the most practical solution to compensate for brain shift is to update the navigation system with intraoperative image data. Until now, we believe this update was an anatomic update only (27,28,40). Functional data obtained with magnetoencephalography and functional MR imaging were integrated in the preoperative dataset for functional neuronavigation and were lost with the update procedure. Nonlinear elastic registration and techniques from pattern recognition analysis allowed matching of preoperative MR data sets that contained functional information with intraoperative MR image volumes; this transformed preoperative functional markers into intraoperative image data sets (41,42). Nonrigid registration of preoperative DTI data onto intraoperative MR volume data may be a solution to preserve preoperative information on the course of white matter tracts (43). However, all mathematic models that are used to describe and simulate the brain shift phenomenon and to warp preoperative data to an estimated intraoperative situation are not yet reliable enough to be used in a routine clinical setting. The comparison between model-predicted courses of fiber tracts with the real situation delineated with intraoperative DTI will offer a possibility to validate and refine the mathematic models.
A limitation of this study is that distortions of intraoperative images at the cortical surface that were caused by the open skull may have influenced the evaluation to a certain extent. Thus, the application of nonlinear registration algorithms, measurement of field maps that describe image distortions, and other sequence techniques that are not so distortion sensitive will be investigated in the future. Nonstandard head positioning at surgery caused different color encoding between images obtained with pre- and intraoperative DTI in some patients, and it complicated the comparison of images obtained with pre- and intraoperative DTI. Acquisition of preoperative data immediately after anesthesia induction and head fixation allowed us to avoid different color encoding. A semiautomatic segmentation of major white matter tracts on the basis of color thresholds may allow the prevention of errors that are due to a potentially biased manual segmentation procedure.
The use of intraoperative anatomic volume data and DTI measurements in the process of updating the navigation system will allow reliable compensation for brain shift of deep-seated eloquent brain structures, since intraoperative DTI data are used to visualize the actual course of major white matter tracts after surgically induced brain deformation. We hope that intraoperative knowledge of the actual position of white matter tracts will decrease the risk of new postoperative neurologic deficits that are caused by the removal of deep-seated tumor portions near eloquent brain areas, such as the pyramidal tract.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Authors stated no financial relationship to disclose.
Author contributions: Guarantors of integrity of entire study, C.N., R.F.; study concepts, C.N., A.G.S., R.F.; study design, C.N., O.G., A.G.S.; literature research, C.N., O.G., P.H.; clinical studies, C.N., O.G., P.H., R.F.; data acquisition, C.N., O.G., P.H.; data analysis/interpretation, C.N., O.G., R.W., T.B., A.G.S.; statistical analysis, C.N., P.H.; manuscript preparation, C.N.; manuscript definition of intellectual content, all authors; manuscript editing, C.N.; manuscript revision/review, C.N., O.G., R.W., T.B., A.G.S.; manuscript final version approval, all authors
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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