MAGNETIC RESONANCE I N MEDICINE 19,316-320 ( 199 I )
Diffusion-Weighted MR Imaging of Extraaxial Tumors * JAYs. TSURUDA, WIL M. CHEW, MICHAELE. MOSELEY,AND DAVIDNORMAN Department of Radiology, Diagnostic and Interventional Neuroradiology Section, University of Cal[fornia, San Francisco, California 94143-0628 Received February I, 1991 The clinical usefulness of the application of spin-echo diffusion-weightedimaging in the evaluation of extraaxial cysts and epidermoid tumors is demonstrated in a series of 15 patients. Apparent diffusion coefficient ( ADC) images based on intravoxel incoherent motion (IVIM) were obtained with a maximum gradient b value = 100 s/mmz. Lesion ADC was qualitatively compared to external phantoms. In all cases, epidermoid tumors revealed reduced ADC values similar to that of normal brain tissue. On the other hand, all cysts had ADC similar to the stationary water phantom. Lesion delineation was improved due to the replacement of normal pulsatile (very high ADC) cisternal CSF. Direct quantitative measurements of ADC using this technique may not be possible due to unavoidable motion artifact. o 1991 Academic Press, Inc. INTRODUCTION
The application of strong magnetic field gradients during proton magnetic resonance (MR) imaging has been shown to be a method in which differences in molecular selfdiffusion can be observed which may differ depending upon the tissue type. Because of macroscopic CSF motion which occurs in vzvo, the diffusion value of CSF is increased when compared to stationary fluid ( 1 ) . This phenomenon may assist in accentuating image contrast between normal CSF and extraaxial tumors on a diffusion-weighted image. Additionally, further characterization of a mass lesion based on intrinsic diffusion values should be possible. The purpose of this article is to report the results of apparent diffusion coefficient ( ADC) imaging on a large series of patients with extraaxial tumors. ADC images were analyzed for lesion conspicuity and specificity in both surgically and nonsurgically proven cases and its impact on therapeutic management. MATERIAL AND METHODS
A 1.5-T system (General Electric Signa, Milwaukee, WI) equipped with a selfshielded RF gradient coil system and a maximum gradient strength of 10 m T / m was utilized. The patient’s head was immobilized with a vacuum-assisted device (size 20, Olympic Medical, Seattle, WA ) . An external phantom filled with mineral oil and water was simultaneously imaged. Multislice ADC images (2) were obtained using a
* Presented at SMRM Workshop on Future Directions in MRI of Diffusion and Microcirculation,Bethesda, MD, June 7 and 8, 1990. 0740-3 l94/9 1 $3.00 Copyright O 199 I by Academic Press, Inc. All rights of reproduction in any form resewed.
316
DIFFUSION MRI EXTRAAXIAL TUMORS
317
cardiac-gated spin-echo sequence TR 900- 1000 ms (effective TR range ), TE 100 ms, NEX 2 or 4 with a maximum gradient b value of 100 s/mm2 ( 3 ) .Further details of this technique have been published recently ( 4 ) . RESULTS
The study group consisted of 15 symptomatic patients who were referred for ADC imaging after an initial screening spin-echo MR demonstrated a possible extraaxial mass lesion. Nine of the patients had surgical confirmation which included six epidermoid tumors, two arachnoid cysts, and one neuroepithelial cyst. Representative examples are shown in Figs. 1 and 2. In all cases, the ADC images confirmed the findings of a possible mass lesion as shown on the initial spin-echo MRI and provided additional information on the location and extent of the lesion thus assisting surgical planning. In addition, in all nine patients the ADC study was able to prospectively determine if the lesion was either cystic or solid by qualitatively comparing the ADC of the lesion with the external phantoms and normal brain parenchyma. Using this comparison, all of the epidermoid tumors were noted to have decreased ADC similar to normal brain parenchyma (Fig. 1 ), whereas all cysts had nearly the same ADC as the stationary water phantom (Fig. 2 ) . The information gained from the surgically proven group was used to analyze the results in six patients without a surgical diagnosis. Based on the imaging findings, the diagnoses consisted of one epidermoid tumor, two arachnoid cysts, one third ventricular ependymal cyst, and two developmental variants consisting of a dilated fourth ventricle
FIG. I . Surgically proven epidermoid tumor of the right cerebellopontine angle. ( a ) The SE 600/20 axial image demonstrates asymmetric widening of the cistern with mass effect on the adjacent brain stem at the level of the right internal auditory canal. This displacing lesion shows slightly heterogeneous CSF signal intensity. The SE 2800/30/80 study (not shown) also showed similar findings. Portions of the oil (0)and water ( W ) phantoms are visualized. The spin-echo findings were not able to determine the exact margins or lesion type. ( b ) ADC axial section at the same level depicts a well-defined mass surrounded by normal hyperintense (very long ADC) CSF. Note that the mass has similar ADC as compared to the brain stem and shorter ADC when compared to the stationary water phantom. From these imaging findings, a solid extraaxial mass, most likely an epidermoid tumor, was diagnosed.
318
TSURUDA ET AL.
FIG.2. ( a ) SE 600/20 axial section through the pontomedullary junction demonstrates a multilobulated extraaxial mass ( m ) with intensity similar to the adjacent brain stem ( b ) . The SE 2800/30/80 study (not shown) showed that this lesion was nonspecific and slightly hyperintense when compared to CSF on the first echo and isointense on the second echo. Based on this spin-echo study, an epidermoid tumor was suspected. Portions of the oil (0)and water ( W ) phantoms are visualized. (b) ADC image through the same level shows that the ADC of the lesion is greater when compared to the adjacent brain stem and is closer to the intensity ofthe water phantom. The actual average intensity values obtained by drawing region of interests on the image were: 255 (lesion), 235 (water phantom), 120 (brain stem), and 105 (cerebellar hemispheres). The slight differences in intensity of the right versus left cerebellar hemispheres was uncertain but probably due to minimal subject motion. Due to the lesion’s high ADC value, a fluid-filled cyst and not a solid epidermoid tumor was suspected. This lesion was confirmed to be a cyst during surgical exploration and the final pathologic diagnosis was neuroepithelial cyst.
in one case and asymmetrical widening of the perimedullary cistern in another. The ADC images were thought to be very helpful in the diagnosis of epidermoid tumor since the imaging findings were very similar to those in Fig. 1. ADC imaging was also helpful in confirming the fluid-like nature of the ependymal cyst. The diagnosis of developmental variants was primarily based on the finding of normal CSF ADC noted in the questionable areas. Because of these normal findings, no further work up, such as a CT contrast cisternogram, was performed. Due to the characteristic spin-echo findings of arachnoid cysts, the ADC images did not contribute any additional specificity in these two cases. DISCUSSION
Intravoxel incoherent motion (IVIM) imaging ( 3 )is a method of obtaining images sensitive to microscopic translational motions which occur in each MR imaging voxel. For the purpose of this study, we have found that viewing the ADC image is preferred since image contrast is independent of either spin density, T1, or T2 differences. On the ADC image, signal intensity is proportional to diffusion and perfusion (if present). The application of spin-echo ADC imaging in vivo has been met with limited success due to motion artifacts ( 5 ) . An attempt was made to reduce unwanted motion by patient immobilization with a vacuum device (6) and by the application of cardiac
DIFFUSION MRI EXTRAAXIAL TUMORS
319
gating. Sufficient image artifact was still present in our clinical cases resulting in degradation of parenchymal detail with associated nonuniformity of signal intensity as shown in Fig. 2. This observation is consistent with the known physiologic pulsation (up to 5 mm/s) of the brain parenchyma as a function of the cardiac cycle ( 7) which is several orders of magnitude greater than diffusion of water in the brain. Sensitivity to pulsatile motion is unavoidable due to the relatively long diffusion gradient duration resulting in a TE of 100 ms in order to have a sufficiently high b value. These macroscopic motions are significant enough that quantitative diffusion measurements of brain parenchyma may not be very accurate ( 5 ) . Despite these limitations, we have noted that the ADC images have yielded consistently good results in delineating normal cisternal CSF due to three factors: ( 1 ) the high diffusion associated with water (2.5 X cm2/s)( 8 ) ;(2) restricted diffusion associated with biological soft tissue ( 9 ) ;and ( 3 ) the macroscopic flow associated with pulsatile cisternal CSF which further elevates its ADC over stationary water by up to 400% (1, 8). As a result, the differences in the ADC between brain parenchyma and CSF are significant by several orders of magnitude. This potential for high dynamic range can be qualitatively seen on the ADC images as very high image contrast. In addition, any lesion within the cistern which inhibits bulk CSF flow will be easily detected. Determining tissue specificity based on spin-echo images as well as calculated T1, T2, and proton density values have been shown to be unreliable (10-12). In some cases complicated cysts may mimic solid neoplasms if there is alteration in protein content (13). An example of a complex cyst is shown in Fig. 2. Arachnoid cysts are typically isointense to CSF on all pulsing sequences (14-16) and are usually not a diagnostic challenge. Epidermoid tumors on the other hand may have variable signal intensity which is typically slightly hyperintense compared to CSF on both T1- and TZweighted MR images (17-20). Unfortunately in some cases, the MR signal intensity of epidermoids may closely approach that of CSF which may lead to diagnostic uncertainty and poor definition of the surgical anatomy. The patient in Fig. 1 demonstrated these difficulties.CT cisternographymay still be indicated in problematic cases. In conclusion, in our patient population ADC imaging can yield additional specificity in distinguishing between the cystic and solid nature of these extraaxial tumors. This distinction can be obtained by simultaneously imaging external phantoms which can provide an objective comparison. Improved delineation between the lesion interface with the adjacent CSF can be made due to the replacement of normally pulsatile cisternal CSF. In one sense, ADC imaging depicts a physiologic MR “cisternogram.” Diagnostic confidence is enhanced. Motion artifact using spin-echo ADC imaging cannot be entirely avoided; therefore, direct quantitative measurements are not possible. Some of these problems may be alleviated with the use of echo planar techniques (21, 22). REFERENCES 1. D. CHIEN,R. BUXTON,B. ROSEN,AND K. JOHNSON. irz “Abstracts, 6th Annual Meeting, Society of Magnetic Resonance in Medicine, August 1987,” p. 887.
2. D. LE BIHAN,E. BRETON,D. LALLEMAND, M.-L. AUBIN, J. VIGNAUD, AND M. LAVAL-JEANTET, Radiology 168, 497 (1988).
320
TSURUDA ET AL.
3. D. LE BIHAN,E. BRETON, D. LALLEMAND, P. GRENIER, E. CABANIS,AND M. LAVAL-JEANTET, Radiology 161,401 ( 1986). 4. J. TSURUDA, W. CHEW,M. MOSELEY,AND D. NORMAN, AJNR 11,925 (1990). 5. K.-D. MERBOLDT, H. BRUHN,J. FRAHM, M. GYNGELL,W. HANICKE,AND M. DEIMLING, Magn. Reson. Med. 9,423 (1989). 6. C. THOMSEN, 0. HENRIKSEN, AND P. RING,Acta Radiol. 28, 353 (1987). 7. D. FEINBERG AND A. MARK,Radiology 163,793 ( 1987). 8. D. LE BIHAN,E. BRETON,M. BARTH,M. AUBIN,D. LALLEMAND, AND J. VIGNAUD, in “Abstracts, 6th Annual Meeting, Society of Magnetic Resonance in Medicine, August 1987,” p. 313. 9. D. LE BIHAN,E. BRETON,D. LALLEMAND, P. BRUGIERES, AND M. GUERON, in “Abstracts, 8th Annual Meeting, Society of Magnetic in Resonance in Medicine, August 1989,” p. 306. 10. M. KOMIYAMA, H. YAGURA,T. YASUI,A. HAKUBEA, S. NISHIMURA, AND Y. INOUE,AJNR 8, 65 (1987). 11. M . JUSTA N D M. THELEN, Radiology 169, 779 ( 1988). 12. D. HACKNEY. R. GROSSMAN, P. JOSEPH,H. GOLDBERG, L. BILANIUK, AND M. SPAGNOLI. AJNR 8, I003 (1987). 13. A. HAIMES,R. ZIMMERMAN, S. MORGELLO, K. WEINGARTEN, R. BECKER.R. JENNIS, A N D M. DECK, AJNR 10,279 (1989). 14. G. HARSIi, M. EDWARDS, AND c . WILSON,J. Neurosurg. 64,835 (1986). 15. S. WIENER,A. PEARLSTEIN, AND A. EIBER,J . Comput. Assist. Tomogr. 11, 236 (1987). 16. M. GARCIA-BACH, F. ISMAT, AND F. VILA,Acta Neurochir. Suppl. (Wein) 42, 205 ( 1988). 17. J. VION-DURY, F. VINCENTELLI, M. JIDDANE,Y. VAN BUNNEN, C. RUMEAU,F. GRISCOLI, A N D G. SALAMON, Neuroradiology 29, 333 (1987). 18. J. OLSON,D. BECK,S. CRAWFORD, AND A. MENEZES, Neurosurgery 21, 357 (1987). 19. D. STEFFEY,G. DEE FILIPP,T. SPERA,AND T. GABRIELSEN, J. Compul. Assisl. Tomugr. 12, 438 (1988). 20. D. TAMPERI, D. MELANSON, AND R. ETHIER,AJNR 10, 351 (1989). 21. R. TURNER, D. LE BIHAN,J. DELANNOY, AND .I.PEKAR,in “Abstracts, 8th Annual Meeting, Society of Magnetic Resonance in Medicine, August 1989,” p. 139. 22. R. TURNER,D. LE BIHAN,J. MAIER,R. VAVREK,L. KYLEHEDGES,AND J. PEKAR,Radiology 177, 407 (1990).
Diffusion-Weighted MR Imaging of Extraaxial Tumors * JAYs. TSURUDA, WIL M. CHEW, MICHAELE. MOSELEY,AND DAVIDNORMAN Department of Radiology, Diagnostic and Interventional Neuroradiology Section, University of Cal[fornia, San Francisco, California 94143-0628 Received February I, 1991 The clinical usefulness of the application of spin-echo diffusion-weightedimaging in the evaluation of extraaxial cysts and epidermoid tumors is demonstrated in a series of 15 patients. Apparent diffusion coefficient ( ADC) images based on intravoxel incoherent motion (IVIM) were obtained with a maximum gradient b value = 100 s/mmz. Lesion ADC was qualitatively compared to external phantoms. In all cases, epidermoid tumors revealed reduced ADC values similar to that of normal brain tissue. On the other hand, all cysts had ADC similar to the stationary water phantom. Lesion delineation was improved due to the replacement of normal pulsatile (very high ADC) cisternal CSF. Direct quantitative measurements of ADC using this technique may not be possible due to unavoidable motion artifact. o 1991 Academic Press, Inc. INTRODUCTION
The application of strong magnetic field gradients during proton magnetic resonance (MR) imaging has been shown to be a method in which differences in molecular selfdiffusion can be observed which may differ depending upon the tissue type. Because of macroscopic CSF motion which occurs in vzvo, the diffusion value of CSF is increased when compared to stationary fluid ( 1 ) . This phenomenon may assist in accentuating image contrast between normal CSF and extraaxial tumors on a diffusion-weighted image. Additionally, further characterization of a mass lesion based on intrinsic diffusion values should be possible. The purpose of this article is to report the results of apparent diffusion coefficient ( ADC) imaging on a large series of patients with extraaxial tumors. ADC images were analyzed for lesion conspicuity and specificity in both surgically and nonsurgically proven cases and its impact on therapeutic management. MATERIAL AND METHODS
A 1.5-T system (General Electric Signa, Milwaukee, WI) equipped with a selfshielded RF gradient coil system and a maximum gradient strength of 10 m T / m was utilized. The patient’s head was immobilized with a vacuum-assisted device (size 20, Olympic Medical, Seattle, WA ) . An external phantom filled with mineral oil and water was simultaneously imaged. Multislice ADC images (2) were obtained using a
* Presented at SMRM Workshop on Future Directions in MRI of Diffusion and Microcirculation,Bethesda, MD, June 7 and 8, 1990. 0740-3 l94/9 1 $3.00 Copyright O 199 I by Academic Press, Inc. All rights of reproduction in any form resewed.
316
DIFFUSION MRI EXTRAAXIAL TUMORS
317
cardiac-gated spin-echo sequence TR 900- 1000 ms (effective TR range ), TE 100 ms, NEX 2 or 4 with a maximum gradient b value of 100 s/mm2 ( 3 ) .Further details of this technique have been published recently ( 4 ) . RESULTS
The study group consisted of 15 symptomatic patients who were referred for ADC imaging after an initial screening spin-echo MR demonstrated a possible extraaxial mass lesion. Nine of the patients had surgical confirmation which included six epidermoid tumors, two arachnoid cysts, and one neuroepithelial cyst. Representative examples are shown in Figs. 1 and 2. In all cases, the ADC images confirmed the findings of a possible mass lesion as shown on the initial spin-echo MRI and provided additional information on the location and extent of the lesion thus assisting surgical planning. In addition, in all nine patients the ADC study was able to prospectively determine if the lesion was either cystic or solid by qualitatively comparing the ADC of the lesion with the external phantoms and normal brain parenchyma. Using this comparison, all of the epidermoid tumors were noted to have decreased ADC similar to normal brain parenchyma (Fig. 1 ), whereas all cysts had nearly the same ADC as the stationary water phantom (Fig. 2 ) . The information gained from the surgically proven group was used to analyze the results in six patients without a surgical diagnosis. Based on the imaging findings, the diagnoses consisted of one epidermoid tumor, two arachnoid cysts, one third ventricular ependymal cyst, and two developmental variants consisting of a dilated fourth ventricle
FIG. I . Surgically proven epidermoid tumor of the right cerebellopontine angle. ( a ) The SE 600/20 axial image demonstrates asymmetric widening of the cistern with mass effect on the adjacent brain stem at the level of the right internal auditory canal. This displacing lesion shows slightly heterogeneous CSF signal intensity. The SE 2800/30/80 study (not shown) also showed similar findings. Portions of the oil (0)and water ( W ) phantoms are visualized. The spin-echo findings were not able to determine the exact margins or lesion type. ( b ) ADC axial section at the same level depicts a well-defined mass surrounded by normal hyperintense (very long ADC) CSF. Note that the mass has similar ADC as compared to the brain stem and shorter ADC when compared to the stationary water phantom. From these imaging findings, a solid extraaxial mass, most likely an epidermoid tumor, was diagnosed.
318
TSURUDA ET AL.
FIG.2. ( a ) SE 600/20 axial section through the pontomedullary junction demonstrates a multilobulated extraaxial mass ( m ) with intensity similar to the adjacent brain stem ( b ) . The SE 2800/30/80 study (not shown) showed that this lesion was nonspecific and slightly hyperintense when compared to CSF on the first echo and isointense on the second echo. Based on this spin-echo study, an epidermoid tumor was suspected. Portions of the oil (0)and water ( W ) phantoms are visualized. (b) ADC image through the same level shows that the ADC of the lesion is greater when compared to the adjacent brain stem and is closer to the intensity ofthe water phantom. The actual average intensity values obtained by drawing region of interests on the image were: 255 (lesion), 235 (water phantom), 120 (brain stem), and 105 (cerebellar hemispheres). The slight differences in intensity of the right versus left cerebellar hemispheres was uncertain but probably due to minimal subject motion. Due to the lesion’s high ADC value, a fluid-filled cyst and not a solid epidermoid tumor was suspected. This lesion was confirmed to be a cyst during surgical exploration and the final pathologic diagnosis was neuroepithelial cyst.
in one case and asymmetrical widening of the perimedullary cistern in another. The ADC images were thought to be very helpful in the diagnosis of epidermoid tumor since the imaging findings were very similar to those in Fig. 1. ADC imaging was also helpful in confirming the fluid-like nature of the ependymal cyst. The diagnosis of developmental variants was primarily based on the finding of normal CSF ADC noted in the questionable areas. Because of these normal findings, no further work up, such as a CT contrast cisternogram, was performed. Due to the characteristic spin-echo findings of arachnoid cysts, the ADC images did not contribute any additional specificity in these two cases. DISCUSSION
Intravoxel incoherent motion (IVIM) imaging ( 3 )is a method of obtaining images sensitive to microscopic translational motions which occur in each MR imaging voxel. For the purpose of this study, we have found that viewing the ADC image is preferred since image contrast is independent of either spin density, T1, or T2 differences. On the ADC image, signal intensity is proportional to diffusion and perfusion (if present). The application of spin-echo ADC imaging in vivo has been met with limited success due to motion artifacts ( 5 ) . An attempt was made to reduce unwanted motion by patient immobilization with a vacuum device (6) and by the application of cardiac
DIFFUSION MRI EXTRAAXIAL TUMORS
319
gating. Sufficient image artifact was still present in our clinical cases resulting in degradation of parenchymal detail with associated nonuniformity of signal intensity as shown in Fig. 2. This observation is consistent with the known physiologic pulsation (up to 5 mm/s) of the brain parenchyma as a function of the cardiac cycle ( 7) which is several orders of magnitude greater than diffusion of water in the brain. Sensitivity to pulsatile motion is unavoidable due to the relatively long diffusion gradient duration resulting in a TE of 100 ms in order to have a sufficiently high b value. These macroscopic motions are significant enough that quantitative diffusion measurements of brain parenchyma may not be very accurate ( 5 ) . Despite these limitations, we have noted that the ADC images have yielded consistently good results in delineating normal cisternal CSF due to three factors: ( 1 ) the high diffusion associated with water (2.5 X cm2/s)( 8 ) ;(2) restricted diffusion associated with biological soft tissue ( 9 ) ;and ( 3 ) the macroscopic flow associated with pulsatile cisternal CSF which further elevates its ADC over stationary water by up to 400% (1, 8). As a result, the differences in the ADC between brain parenchyma and CSF are significant by several orders of magnitude. This potential for high dynamic range can be qualitatively seen on the ADC images as very high image contrast. In addition, any lesion within the cistern which inhibits bulk CSF flow will be easily detected. Determining tissue specificity based on spin-echo images as well as calculated T1, T2, and proton density values have been shown to be unreliable (10-12). In some cases complicated cysts may mimic solid neoplasms if there is alteration in protein content (13). An example of a complex cyst is shown in Fig. 2. Arachnoid cysts are typically isointense to CSF on all pulsing sequences (14-16) and are usually not a diagnostic challenge. Epidermoid tumors on the other hand may have variable signal intensity which is typically slightly hyperintense compared to CSF on both T1- and TZweighted MR images (17-20). Unfortunately in some cases, the MR signal intensity of epidermoids may closely approach that of CSF which may lead to diagnostic uncertainty and poor definition of the surgical anatomy. The patient in Fig. 1 demonstrated these difficulties.CT cisternographymay still be indicated in problematic cases. In conclusion, in our patient population ADC imaging can yield additional specificity in distinguishing between the cystic and solid nature of these extraaxial tumors. This distinction can be obtained by simultaneously imaging external phantoms which can provide an objective comparison. Improved delineation between the lesion interface with the adjacent CSF can be made due to the replacement of normally pulsatile cisternal CSF. In one sense, ADC imaging depicts a physiologic MR “cisternogram.” Diagnostic confidence is enhanced. Motion artifact using spin-echo ADC imaging cannot be entirely avoided; therefore, direct quantitative measurements are not possible. Some of these problems may be alleviated with the use of echo planar techniques (21, 22). REFERENCES 1. D. CHIEN,R. BUXTON,B. ROSEN,AND K. JOHNSON. irz “Abstracts, 6th Annual Meeting, Society of Magnetic Resonance in Medicine, August 1987,” p. 887.
2. D. LE BIHAN,E. BRETON,D. LALLEMAND, M.-L. AUBIN, J. VIGNAUD, AND M. LAVAL-JEANTET, Radiology 168, 497 (1988).
320
TSURUDA ET AL.
3. D. LE BIHAN,E. BRETON, D. LALLEMAND, P. GRENIER, E. CABANIS,AND M. LAVAL-JEANTET, Radiology 161,401 ( 1986). 4. J. TSURUDA, W. CHEW,M. MOSELEY,AND D. NORMAN, AJNR 11,925 (1990). 5. K.-D. MERBOLDT, H. BRUHN,J. FRAHM, M. GYNGELL,W. HANICKE,AND M. DEIMLING, Magn. Reson. Med. 9,423 (1989). 6. C. THOMSEN, 0. HENRIKSEN, AND P. RING,Acta Radiol. 28, 353 (1987). 7. D. FEINBERG AND A. MARK,Radiology 163,793 ( 1987). 8. D. LE BIHAN,E. BRETON,M. BARTH,M. AUBIN,D. LALLEMAND, AND J. VIGNAUD, in “Abstracts, 6th Annual Meeting, Society of Magnetic Resonance in Medicine, August 1987,” p. 313. 9. D. LE BIHAN,E. BRETON,D. LALLEMAND, P. BRUGIERES, AND M. GUERON, in “Abstracts, 8th Annual Meeting, Society of Magnetic in Resonance in Medicine, August 1989,” p. 306. 10. M. KOMIYAMA, H. YAGURA,T. YASUI,A. HAKUBEA, S. NISHIMURA, AND Y. INOUE,AJNR 8, 65 (1987). 11. M . JUSTA N D M. THELEN, Radiology 169, 779 ( 1988). 12. D. HACKNEY. R. GROSSMAN, P. JOSEPH,H. GOLDBERG, L. BILANIUK, AND M. SPAGNOLI. AJNR 8, I003 (1987). 13. A. HAIMES,R. ZIMMERMAN, S. MORGELLO, K. WEINGARTEN, R. BECKER.R. JENNIS, A N D M. DECK, AJNR 10,279 (1989). 14. G. HARSIi, M. EDWARDS, AND c . WILSON,J. Neurosurg. 64,835 (1986). 15. S. WIENER,A. PEARLSTEIN, AND A. EIBER,J . Comput. Assist. Tomogr. 11, 236 (1987). 16. M. GARCIA-BACH, F. ISMAT, AND F. VILA,Acta Neurochir. Suppl. (Wein) 42, 205 ( 1988). 17. J. VION-DURY, F. VINCENTELLI, M. JIDDANE,Y. VAN BUNNEN, C. RUMEAU,F. GRISCOLI, A N D G. SALAMON, Neuroradiology 29, 333 (1987). 18. J. OLSON,D. BECK,S. CRAWFORD, AND A. MENEZES, Neurosurgery 21, 357 (1987). 19. D. STEFFEY,G. DEE FILIPP,T. SPERA,AND T. GABRIELSEN, J. Compul. Assisl. Tomugr. 12, 438 (1988). 20. D. TAMPERI, D. MELANSON, AND R. ETHIER,AJNR 10, 351 (1989). 21. R. TURNER, D. LE BIHAN,J. DELANNOY, AND .I.PEKAR,in “Abstracts, 8th Annual Meeting, Society of Magnetic Resonance in Medicine, August 1989,” p. 139. 22. R. TURNER,D. LE BIHAN,J. MAIER,R. VAVREK,L. KYLEHEDGES,AND J. PEKAR,Radiology 177, 407 (1990).
