Intraoperative Diffusion Imaging on a 0.5 Tesla Interventional Scanner

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1 JOURNAL OF MAGNETIC RESONANCE IMAGING 13: (2001) Original Research Intraoperative Diffusion Imaging on a 0.5 Tesla Interventional Scanner Yoshiaki Mamata, MD, PhD, Hatsuho Mamata, MD, Arya Nabavi, MD, Daniel F. Kacher, MSc, Richard S. Pergolizzi Jr., MD, Richard B. Schwartz, MD, PhD, Ron Kikinis, MD, Ferenc A. Jolesz, MD, and Stephan E. Maier, MD, PhD* Intraoperative line scan diffusion imaging (LSDI) on a 0.5 Tesla interventional MRI was performed during neurosurgery in three patients. Diffusion trace images were obtained in acute ischemic cases. Scan time per slice was 46 seconds and 94 seconds, respectively, for diffusion tensor images. Diagnosis of acutely developed vascular occlusion was confirmed with follow-up scans. White matter tracts were displayed with the principal eigenvectors and provided guidance for the tumor surgery. In all cases, the diagnostic utility of LSDI was established. J. Magn. Reson. Imaging 2001;13: Wiley-Liss, Inc. Index terms: line scan diffusion imaging; diffusion-weighted images; interventional MRI; brain tumor; cerebral ischemia DIFFUSION-WEIGHTED IMAGING (DWI) has become a diagnostically accepted MRI tissue characterization method for assessing brain pathology, such as ischemic stroke (1 3), brain tumor (4,5), and multiple sclerosis (6). Diffusion tensor imaging has demonstrated the ability of MRI to reveal the structure of white matter fiber tracts (7 9). The potential of this method for monitoring therapy and providing image guidance is obvious, but its current use is limited. Diffusion-weighted imaging for monitoring of brain ischemia after stent placement following neurovascular intervention has been reported (10). Sunshine et al. (3) recommended obtaining diffusion-weighted images and perfusion images before interventional therapy in hyperacute stroke patients. Diffusion imaging is usually obtained with single-shot echo-planar imaging (EPI) using scanners at high field strength with relatively strong and fast gradients. Lovblad et al. (11) introduced echo-planar diffusion-weighted images performed on a mediumfield (1.0 Tesla) scanner in stroke patients. Maier et al. (1) demonstrated the utility of line scan diffusion imaging (LSDI) in stroke diagnosis on a 0.5 Tesla magnet. It Department of Radiology, Brigham and Women s Hospital, Harvard Medical School, Boston, Massachusetts. Contract grant sponsor: NIH; Contract grant number: PO1; Contract grant sponsor: NAC; Contract grant number: P41 RR13218; Contract grant sponsor: The Whitaker Foundation. *Address reprint requests to: S.E.M., Department of Radiology, Brigham and Women s Hospital, Harvard Medical School, 75 Francis Street, Boston, MA stephan@bwh.harvard.edu Received April 19, 2000; Accepted July 27, has been demonstrated repeatedly that intraoperative magnetic resonance (IMR) imaging at low- to mid-field ( Tesla) is of great benefit in guiding various surgical interventions (12 15). There is always the possibility of accidental ischemic events during surgery, in which case intraoperative diffusion imaging may permit immediate diagnosis. Our goal was to investigate the feasibility of LSDI during surgical procedures on a 0.5 Tesla intraoperative MRI. We also explored the utility of white matter fiber mapping with diffusion tensor imaging during brain tumor surgery. SUBJECTS AND METHODS Line scan diffusion-weighted images (16) were obtained in three brain tumor cases during neurosurgical procedures in a vertical gap open-configuration 0.5 Tesla MRI system (SIGNA SP, General Electric Medical System, Milwaukee, WI) (17). All studies were obtained within the guidelines of the institutional internal review board (IRB). Informed consent was obtained from all subjects or their authorized representatives. Diffusion imaging protocols were tested in normal volunteers, prior to intraoperative application in patients. Imaging was performed with a flexible double-loop surface coil. In cases of suspected ischemia, line scan diffusion trace images were obtained with the following scan parameters: TR/TR Eff /TE 225/3825/158 msec; rectangular FOV mm; effective slice thickness 7mm (16); slice gap 3 mm; matrix size (frequency column); bandwidth 2.02 khz; and excitation 1. To measure the apparent diffusion coefficient (ADC), images were scanned at two different diffusion weightings (b-factors: 5 and 500 sec/mm 2 ; 57 msec; 77 msec). For the low b-factor, diffusion weighting was only applied along one direction, whereas for the high b-factor diffusion weighting was applied along three directions (16). For diffusion tensor imaging, the high b-factor diffusion weighting was applied along six directions. The following parameters were also different for diffusion tensor scans: TR/TR Eff / TE 230/3910/163 msec; rectangular FOV mm; slice gap 1 mm; 60 msec; and 80 msec. The scan time per slice was 94 seconds for diffusion tensor imaging and 46 seconds for diffusion trace 2001 Wiley-Liss, Inc. 115

2 116 Mamata et al. imaging. In order to minimize the gradient heating limited repetition time, only 50% (4.25 mt/m) of the maximal permissible gradient amplitude was used. Diffusion-weighted images and ADC maps were computed and displayed on the scanner console. Diffusion tensor data, however, was processed and displayed off-line using dedicated software written by one of the authors. For better visualization, diffusion-weighted images were reconstructed on the basis of the measured apparent diffusion coefficient and of an assumed b-factor of 1000 sec/mm 2. All calculated images, including maps of the principal eigenvector, were displayed within minutes after the acquisition on a monitor installed in the operation area. RESULTS The first and second cases demonstrate the use of diffusion MRI for the early detection of intraoperatively developed hyperacute cerebral ischemia. The first case was a 67-year-old male with an anaplastic astrocytoma who underwent tumor resection in the right temporal lobe (Fig. 1a and b) under general anesthesia. On T 2 - weighted images, obtained during the third hour of operation after the coagulation of a tumor-feeding vessel, the right temporal sulci above the lesion appeared narrower than they did on earlier images. Moreover, the subcortical white matter close to the sulci showed slightly increased MR signal. A right temporal lobe infarction was suspected and diffusion imaging was performed. The line-scan T 2 -weighted image (low diffusion weighting) shows the narrowing of right temporal sulci and the signal increase within subcortical white matter (Fig. 1c). On the corresponding ADC map (Fig. 1d), the same area demonstrates markedly decreased diffusion of 0.42 m 2 /msec vs m 2 /msec on the contralateral normal side. On diffusion-weighted images (Fig. 1e and f), a well defined lesion with increased signal intensity can be identified within the temporo-posterior distribution of the right middle cerebral artery (MCA). Postoperatively, the patient had mild left-side weakness in his upper extremity and extinction of left sensory stimuli. On follow-up MR images, infarction of the right MCA temporal distribution was confirmed (Fig. 1g and h). Interestingly, the lesion appears considerably smaller on the follow-up T 2 -weighted images. The second case was a 43-year-old female with an oligodendroglioma in the left fronto-temporal region, who underwent craniotomy awake. During the procedure, she suddenly developed motor weakness in her upper extremity and consciousness disturbance. Conventional T 1 - and T 2 -weighted images did not indicate any abnormality. Consequently, diffusion-weighted images were obtained. An area of increased signal on the diffusion-weighted images revealed a hyperacute ischemic lesion involving the left basal ganglia and internal capsule. Follow-up imaging confirmed this early finding. The third case demonstrates the use of diffusion MRI as an integral part of image-guided tumor resection. A 21-year-old female with a temporo-parietal oligodendroglioma underwent tumor resection while awake using computer-assisted neuronavigation based on intraoperative data. After the craniotomy, diffusion tensor imaging was performed. Post-processing demonstrated the anatomy of white matter fiber tracts adjacent to the lesion. On the preoperative T 1 -weighted (Fig. 2a) and T 2 -weighted images, the tumor shows homogeneous signal intensity with clear margin and no signs of peritumoral edema. On the intraoperative ADC map (Fig. 2b) the diffusion in the tumor area is markedly increased (1.76 vs m 2 / msec on the contralateral normal side). The same area shows high signal on the diffusion-weighted image (Fig. 2c). The tumor exerted a mass effect against the left lateral ventricle and the adjacent white matter fiber tracts were displaced. On the eigenvector map (Fig. 2d), the course of fiber tracts is well demonstrated. A part of the arcuate faciculus is remarkably displaced and curved along the medial tumor margin without obvious disruption. In addition, the right corona radiata is slightly displaced medially. The space between the right arcuate faciculus and corona radiata appeared to be narrowed due to mass effect. Total tumor resection was done successfully without any postoperative neurological deficit. DISCUSSION Intraoperative MRI is now widely used in neurosurgery with systems of various configurations and field strengths (12 15,18 22). MRI guidance is particularly helpful in localizing tumor margins (target definition), selecting the best surgical approaches (trajectory optimization), achieving complete resection of intracerebral lesions (tumor control), and monitoring potential intraoperative complications (13,14,19). On diagnostic MR systems it has been demonstrated that the earliest detection of ischemic brain damage is possible with diffusion weighted imaging (2). More recently, the anisotropic diffusion of white matter tracts has been utilized to demonstrate the course of white matter fiber tracts Figure 1. A 67-year-old man with recurrent anaplastic astrocytoma. Preoperative contrast-enhanced (Gd-DTPA) T 1 -weighted (a) and T 2 -weighted (b) images demonstrate the tumor lesion and the adjacent focal edema in the right medial temporal lobe. c: Line scan T 2 -weighted image, obtained during the procedure, demonstrates slightly increased intensity within right temporal lobe. d: The LSDI ADC map demonstrates the corresponding region with markedly decreased signal intensity. e and f: On the diffusion-weighted images obtained at two different levels, increased signal intensity is observed at the temporo-posterior distribution of the right middle cerebral artery (MCA). g and h: Follow-up T 2 -weighted images demonstrate right temporal ischemic lesion at comparable slice levels. The motion artifacts are due to the restless state of the patient after the stroke. The high signal intensity area on follow-up T 2 -weighted images is clearly smaller than the lesion on the diffusion-weighted images obtained during operation.

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4 118 Mamata et al. Figure 2. A 21-year-old woman with oligodendroglioma. T 1 -weighted image reveals a well-defined mass lesion located in the left temporo-parietal brain (a). LSDI ADC map (b) and diffusion-weighted image (c) demonstrate marked changes within the tumor. The eigenvector map of the tumor area (d) demonstrates that a part of the arcuate faciculus is considerably shifted and curved along the medial tumor margin (arrows). The right corona radiata (through-plane eigenvectors represented with dots) is slightly shifted medially (arrow heads). (7,8). Intraoperative MRI can utilize both of these features. Some applications of diffusion-weighted imaging for neurovascular intervention have been reported (3,10). These applications have been limited to EPIcapable MRI systems. We implemented the line scan diffusion sequence (16) on a 0.5 Tesla open-configuration scanner. In all three cases, diffusion imaging provided clinically important, intraoperatively relevant information about the pathologic state of brain tissue and/or the structure of white matter. As shown in the two presented cases of hyperacute ischemia, diffusionweighted imaging is extremely helpful for the immediate detection of intraoperative ischemic complications. It permits the surgeon to perform alternative procedures, such as recanalizing the occlusion that leads to the ischemia or administering brain-protective agents (e.g., steroids or mannitol) to reduce damage and prevent further enlargement of the lesion. However, our experience at this time is limited. Further scans of intraoperative ischemic events are necessary to determine the correlation between the initial ADC changes and the extent of damages on the postoperative follow-up scan. It is also unclear whether perfusion imaging would be more useful than diffusion imaging in monitoring tissue at risk.

5 Intraoperative Diffusion Imaging 119 Diffusion tensor data may demonstrate the normal course, displacement, or interruption of white matter fiber tracts around a tumor. In addition, the widening of white matter fiber bundles due to edema or tumor infiltration can be detected. The lack of anisotropy can demonstrate the presence of tumor within normal, anisotropic white matter (8). Intraoperative changes in fiber orientation due to surgically induced brain deformation can be detected. This intraoperative mapping of white matter anatomy may help to avoid injury to critical white matter tracts. Although functional MRI (fmri) may localize cortical function, determining the course and integrity of white matter tracts is essential to avoid postoperative neurologic deficit. Unlike EPI-based diffusion imaging, LSDI is applicable in lower-field magnets without fast gradients (1). We also prefer LSDI because of its insensitivity to susceptibility and chemical shift. It is particularly helpful if the surgical target is close to bone structures. Also, air pockets are often present during surgery and may cause degradation of the images. The images obtained with LSDI are essentially free of distortion in such situations. Currently, multislice imaging is limited due to long scan times. In acute ischemic cases monodirectional diffusion-encoded images, which can be obtained in 21 seconds per slice, may be sufficient. Improvement in the gradient performance of future intraoperative systems may also permit shorter scan times. Moreover, the reduced echo time that results from higher gradient amplitudes would improve the relatively low signal-tonoise ratio of the diffusion-weighted images. CONCLUSIONS A line scan diffusion sequence was successfully installed on a 0.5 Tesla open configuration interventional MRI scanner. Diffusion tensor imaging was used to display the displaced white matter tracts around the tumor and to detect ischemic complications. The feasibility and potential of this technique in MRI-guided neurosurgery has been demonstrated. ACKNOWLEDGMENTS We thank Dr. Peter M. Black, Dr. Eben Alexander III, and Dr. Liangee Hsu for their cooperation and advice. We thank the MRT staff for making the research run smoothly. This investigation was aided by grants from the NIH (PO1) and NAC (P41 RR13218) to F.A.J, and from the Whitaker Foundation to S.E.M. REFERENCES 1. Maier SE, Gudbjartsson H, Patz S, et al. Line scan diffusion imaging: characterization in healthy subjects and stroke patients. Am J Roentgenol 1998;171: Warach S, Chien D, Li W, Ronthal M, Edelman RR. Fast magnetic resonance diffusion-weighted imaging of acute human stroke. Neurology 1992;42: Sunshine JL, Tarr RW, Lanzieri CF, Landis DM, Selman WR, Lewin JS. Hyperacute stroke: ultrafast MR imaging to triage patients prior to therapy. Radiology 1999;212: Desprechins B, Stadnik T, Koerts G, Shabana W, Breucq C, Osteaux M. 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