Directional Diffusion in Relapsing-Remitting Multiple Sclerosis: A Possible In Vivo Signature of Wallerian Degeneration

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1 JOURNAL OF MAGNETIC RESONANCE IMAGING 18: (2003) Original Research Directional Diffusion in Relapsing-Remitting Multiple Sclerosis: A Possible In Vivo Signature of Wallerian Degeneration Roland G. Henry, PhD, 1 * Joonmi Oh, PhD, 1 Sarah J. Nelson, PhD, 1 and Daniel Pelletier, MD 2 Purpose: To examine the role of directional dependence of the apparent diffusion coefficients in the evaluation of normal-appearing brain regions of patients with relapsingremitting multiple sclerosis. Materials and Methods: The role of diffusion tensor eigenvalues was investigated in the normal-appearing brain regions for 18 patients with relapsing-remitting multiple sclerosis and 15 age-matched normal controls. Results: The isotropic apparent diffusion was increased in all regions. However, reduced anisotropy was significant only in regions with high anisotropy, including the corpus callosum and the internal capsule, and was due to increased diffusion tensor eigenvalues corresponding to diffusion transverse to the fibers without significant increase along the fibers. This characteristic pattern of changes in diffusion tensor eigenvalues has been observed previously in cases of Wallerian degeneration. Low-anisotropy regions corresponded to gray matter and gray/white interface regions. Since fiber tract orientations are not determined for regions of low anisotropy, this characteristic pattern of diffusion change is not detectable in these regions. Conclusion: Examination of diffusion tensor eigenvectors may provide insight into the changes observed in diffusion and a signature of Wallerian degeneration in the normal-appearing white matter of relapsing-remitting multiple sclerosis patients. Key Words: diffusion tensor imaging; normal-appearing white matter; multiple sclerosis; fiber tracts; Wallerian degeneration J. Magn. Reson. Imaging 2003;18: Wiley-Liss, Inc. 1 Magnetic Resonance Science Center, Department of Radiology, University of California, San Francisco, California. 2 UCSF Multiple Sclerosis Center, Department of Neurology, University of California, San Francisco, California. Contract grant sponsor: National Multiple Sclerosis Society; Contract grant number: RG2655B6/1; Contract grant sponsor: NIH; Contract grant number: R01 NS *Address reprint requests to: R.G.H., Magnetic Resonance Science Center, Box 1290, Department of Radiology, University of California, San Francisco, San Francisco, CA Roland.Henry@mrsc.ucsf.edu Received July 8, 2002; Accepted June 20, DOI /jmri Published online in Wiley InterScience ( THE GOAL OF THIS STUDY was to investigate the role of diffusion tensor eigenvalues in understanding changes in the normal-appearing brain tissue of patients with relapsing-remitting multiple sclerosis (RRMS). RRMS is a disease affecting the central nervous system that is characterized by acute neurological symptoms, followed by significant clinical recovery, with stability between acute attacks. Understanding changes in the normal-appearing brain is an important issue because recent histopathological findings have indicated that normal-appearing white matter (NAWM) is abnormal in patients with multiple sclerosis, and perhaps very early in the disease process (1 6). The origin of the NAWM changes is unknown; contrary to conventional wisdom, a recent study has suggested that Wallerian degeneration due to insults caused by lesions may be responsible at the earliest stages of the disease (6). Recently, MRI techniques like diffusion tensor imaging (DTI) (7), which probe different physiological aspects of the brain, have been used to measure features of regions that appear normal on anatomical MR images. These reports have indicated increased isotropic diffusion and reduced diffusion anisotropy in the NAWM (8 16). Although they are interesting, these results do not indicate any specific pathology or which structural changes may be reflected. To gain further insight into these changes, we propose to study the changes in the diffusion tensor eigenvalues that determine the observed increase in isotropic diffusion and the decrease in diffusion anisotropy. Furthermore, we hypothesize that the study of the diffusion tensor eigenvalues may lead to improved sensitivity to and provide more specific markers of the pathological changes in the normal-appearing brain of multiple sclerosis (MS) patients. In particular, the diffusion tensor eigenvalues may reflect a signature of Wallerian degeneration in the high-anisotropy NAWM of relapsing-remitting MS patients. Diffusion tensor eigenvalues are the magnitudes of the principal vectors (eigenvectors) that describe the diffusion in a region and are obtained by diagonalization of the measured diffusion tensor for that region. Although a voxel may contain many fibers in different 2003 Wiley-Liss, Inc. 420

2 Directional Diffusion in Multiple Sclerosis 421 directions, the apparent diffusion in this complicated architecture may be approximated by such a tensor (7). These three diffusion directions are labeled as approximately along the direction of maximum diffusion, along the direction of minimum diffusion, and along the third direction, which is orthogonal to the other two directions. The isotropic apparent diffusion coefficient (ADC), characterizing the isotropic diffusion, is the average of the three eigenvalues. The diffusion relative anisotropy (RA), a scalar invariant defined by Basser et al (7), is a function reflecting the variance of the diffusion tensor eigenvalues. When the magnitude of RA is large, then diffusion is preferred in one direction compared to the other two orthogonal directions. This is the result expected from a homogeneous cylindrical fiber bundle in which all fibers are oriented parallel to each other. Anisotropy (i.e., RA) is low when all directions have apparent diffusion of similar magnitudes and is the case in regions without structure or where tissue fibers intersect at various angles and there is no preferred fiber bundle direction dominating in a voxel. Fluid attenuation inversion recovery (FLAIR) sequences are used to attenuate cerebrospinal fluid (CSF) in the brain based on the T1 relaxation rate. This sequence also attenuates the MR signal from other tissue depending on the closeness in value to the T1 of the CSF. FLAIR imaging sequences are used in MS in order to improve delineation of periventricular lesions compared to CSF, which are both bright on T2-weighted images. When combined with diffusion imaging, FLAIR acts to attenuate the contribution of CSF to the measured diffusion. Because of the relatively poor resolution of echo-planar sequences used for diffusion tensor imaging, there are significant partial volume effects of CSF with brain tissue that increase the net measured apparent diffusion. The FLAIR diffusion sequence reduces this effect and thereby allows a truer measurement of brain diffusion (17 21). When evaluating the mean diffusion from large regions of the brain, the effect of increased rate of diffusion due to CSF is difficult to control and will especially increase the rate of diffusion transverse to fibers because of the contribution of the ADC of greater magnitude due to the CSF within the voxel. With the FLAIR diffusion sequence, variation in the measured brain diffusion is lower, is assumed to be more accurate (due to the reasons mentioned above), and changes in the smaller directional ADCs representing transverse diffusion may be better determined. This study looks at the diffusion tensor eigenvalues in the normal-appearing brain tissue of RRMS patients using a FLAIR-DTI technique to better understand the origin of increased isotropic diffusion and the reduced anisotropy observed for these patients. MATERIALS AND METHODS A FLAIR-diffusion tensor sequence (GE, Milwaukee, WI), modified in our laboratory, was used to study 18 RRMS patients as defined by Poser et al (22) (mean age 40.3 years, SD 8.6 years, range years) and 15 normal controls (mean age 43.1 years, SD 9.3 years, range years). The mean disease duration for the RRMS patients was 9.1 years (range 4 24 years) and expanded disability status score (EDSS) 2.0 (range 0 to 3.5). All patients and controls gave consent and the studies were approved by our institution s committee on human research. All RRMS patients were treated with standard approved diseasemodifying therapy. The imaging protocol included a research echo-planar FLAIR-diffusion pulse sequence with TR/TE/TI 10 seconds/90 msec/2.2 seconds; diffusion weighting parameter b 1000 seconds/mm 2 ; six diffusion gradient directions; 3 mm thick slices; matrix size ; and FOV 36 cm 18 cm; typically 28 slices with interleaved acquisition. T1-weighted spoiled gradient recalled echo (SPGR) volumes, T2-weighted images, and oblique fast-spin-echo (FSE) images were also obtained. The inversion time used in this sequence was set to suppress the signal from cerebrospinal fluid. The isotropic apparent diffusion coefficient, eigenvalues, and relative anisotropy were calculated on a pixel by pixel basis. Figure 1 shows FLAIR T2-weighted images acquired without diffusion gradients, and the isotropic diffusion and eigenvalue maps for a RRMS patient. The periventricular hyperintense lesions are clearly visible and are easily differentiated from CSF in the ventricles on the FLAIR T2-weighted images. The oblique FSE data were prescribed similarly in all patients, with slices chosen parallel to the body of the corpus callosum. The T1-weighted SPGR volume was aligned to the FSE oblique images and these alignment parameters were used to align the diffusion data to the oblique orientation. Central brain regions of 15 mm were subsampled from the aligned diffusion data and centered about the body of the corpus callosum. The centers of the corpus callosum were determined from sagittal-like views of the aligned FLAIR-DTI data. The normal-appearing brain was segmented from CSF and lesions based on the intensity of the FLAIR-DTI images without diffusion weighting (and only these brain regions) were used for analysis. The normal-appearing brain was further segmented into three regions based on the diffusion anisotropy properties. Voxels corresponding to the 75th to 100th percentile of the anisotropy distribution were classified as high-anisotropy regions, those with a 50th to 75th percentile were classified as mid-anisotropy regions, and those voxels with a 0 to50th percentile were classified as low-anisotropy regions. First, Histograms of diffusion parameters for the central brain and anisotropy-based regions were calculated and normalized to the total number of counts. The histogram means and standard deviations were calculated for each diffusion parameter and compared between those of patients and normal controls. The F-test was used to compare means and standard deviations between the groups for the entire central brain. Second, F-tests were performed on the means from the anisotropy-segmented regions between RRMS patients and normal controls. Both sets of F-tests were aged adjusted. RESULTS Results from the analysis of the central brain are shown in Table 1. The mean isotropic diffusion was signifi-

3 422 Henry et al. Figure 1. FLAIR T2-weighted echo-planar images 3 mm thick in a RRMS patient (a). Also shown are isotropic diffusion (b), maximum (c), middle (d), and minimum (e) eigenvalue maps. cantly elevated and the anisotropy tended to decrease for the RRMS patients compared to the normal controls. The maximum eigenvalue was not significantly different in RRMS patients compared to controls, while both middle and minimum eigenvalues were significantly elevated. Histogram standard deviations were significantly increased for isotropic diffusion, decreased for anisotropic diffusion, but were not significantly different from normal for eigenvalues. The anisotropy-based segmented regions corresponded to distinct regions of the brain and an example for an RRMS patient is shown in Figure 2. The highanisotropy region included highly-ordered white matter tracts such as the corpus callosum, internal capsule, and corona radiata. The low-anisotropy regions corresponded primarily with cortical and deep gray matter and some gray/white junction tissue. The mid-anisotropy regions corresponded to white matter tissue not included in the other regions and are believed to correspond to regions of crossing white matter fibers. Anisotropy and eigenvalues were extremely different between these regions for each group and are shown in Table 2. Isotropic ADC was significantly lower in the medium and high anisotropy regions compared to the low anisotropy regions. In the high-anisotropy regions, the maximum eigenvalue was higher and the minor eigenvalues lower compared to the central brain. The reverse was true in the low-anisotropy region, with the maximum eigenvalues lower and the minor eigenvalues higher than the entire central brain. The mid-anisotropy values were similar to those of the entire central brain. Table 1 Histogram Parameters in Normal Appearing Central Brain Region Means SD NC RRMS P value NC RRMS P value IADC RA Max ev Mid ev Min ev IADC isotropic ADC in units of m 2 /ms, RA relative anisotropy, Max ev maximum eigenvalue, Mid ev midian eigenvalue, Min ev minimum eigenvalues, RRMS relapsing-remitting patients, NC normal controls. *Significant P values (.05) are shown in bold.

4 Directional Diffusion in Multiple Sclerosis 423 Figure 2. Example of anisotropy-based segmentation of the normal-appearing brain for the RRMS patient from Fig. 1. Shown are the relative anisotropy map of the normal-appearing brain (a); and segmented regions of high anisotropy (b), medium anisotropy (c), and low anisotropy (d). These complex patterns of change in the central brain can be best understood by looking at changes in the anisotropy-segmented regions. In Table 2, the mean values for the different regions are shown with F-test results from comparisons between normal controls and relapsing-remitting patients. The weak tendency of reduced anisotropy seen in the central brain arises from significantly reduced anisotropy in the high-anisotropy region and no significant change in the other regions. In turn, the reduced anisotropy in the high-anisotropy region arises from increased medium and minimum eigenvalues; no significant change is noted in the maximum eigenvalue, as is evident in Figure 3. The reduction in the standard deviation of the anisotropy distribution for the central brain is also consistent with the reduction in the highest anisotropy values. These values make a tail on the high end of the anisotropy distribution in the central brain of normal controls and reduction of these tailing values leads to a tighter distribution in the RRMS patients. The higher isotropic ADC in the central brain arises from an increase in all regions. The low and mid-anisotropy regions show significantly increased isotropic diffusion but no change in anisotropy, while the highanisotropy region shows smaller increases in isotropic ADC and significantly reduced anisotropy (see Figs. 4 and 5). DISCUSSION In this work we have investigated the role of directional apparent diffusion coefficients in the normal-appearing brain tissue of patients with RRMS. We used a FLAIRdiffusion sequence that enabled good segmentation of normal-appearing brain from CSF and lesions and that also reduced the effects of partial volume averaging on Table 2 Mean Values in Anisotropy-Segmented Regions Low anisotropy Mid anisotropy High anisotropy NC RRMS P value NC RRMS P value NC RRMS P value IADC < RA Max ev Mid ev Min ev < <.001 IADC isotropic ADC in units of m 2 /ms, RA relative anisotropy, Max ev maximum eigenvalue, Mid ev midium eigenvalue, Min ev minimum eigenvalue, RRMS relapsing-remitting patients, NC normal controls. *Significant P values (.05) are shown in bold.

5 424 Henry et al. Figure 3. Maximum (Ev1) (a), medium (Ev2) (b), and minimum (Ev3) (c) diffusion tensor eigenvalues in high-anisotropy regions for normal controls (NC) and RRMS patients (RR). The diffusion is increased transverse to the fibers (minimum and medium eigenvalues) but not along the fibers (maximum eigenvalue). Bars denote 95% confidence interval for the means. the diffusion parameters. Our analysis of central brain regions suggested that the decreased anisotropy for these patients arises from changes detectable only in regions with normally high anisotropy, and this was confirmed by segmentation of normal-appearing brain into regions of low, medium, and high anisotropy. Furthermore, the observed decrease in anisotropy arose from increased diffusion transverse to the fibers; there was no significant change along the fibers. This may provide a distinct diffusion signature of demyelination and/or axonal damage associated with MS pathology. The FLAIR-diffusion sequence used here enabled relatively easy segmentation of normal-appearing brain from cerebral-spinal fluid and lesions. The somewhat poor resolution associated with the echo-planar images usually makes it difficult to identify all regions with partial volume effects due to cerebral spinal fluid. However use of the FLAIR-diffusion sequence allows suppression of partial voxel contributions of CSF to the measured diffusion coefficient. While the FLAIR images do improve CSF elimination, preliminary results from our studies suggest that the same results can be obtained without the use of FLAIR diffusion-weighted imaging, provided that adequate segmentation of normalappearing brain is possible. This is not surprising, because the segmented region of high-anisotropy is less likely to contain appreciable CSF contribution. These issues are under further examination. Because the same pulse sequence parameters were used to image both patients and controls, there is no a priori reason to suspect differences in the signal-tonoise ratio (SNR). Furthermore, the observed changes Figure 4. Isotropic ADC (a) and relative anisotropy (b) in highanisotropy regions for normal controls (NC) and RRMS patients (RR). The anisotropy is reduced and the isotropic diffusion is increased. Bars denote 95% confidence interval for the means. Figure 5. Isotropic diffusion (a) and relative anisotropy (b) in low-anisotropy regions for normal controls (NC) and RRMS patients (RR). The isotropic ADC is increased for RR patients but no change is observed in the anisotropy. Bars denote 95% confidence interval for the means.

6 Directional Diffusion in Multiple Sclerosis 425 were not large enough to appreciably affect SNR and are reflected in the small differences in the acquired images. Increased signal-to-noise leads to larger maximum eigenvalues and smaller minimum eigenvalues, which results in increased anisotropy (28). Therefore, poorer SNR in patients would give the opposite effect than that observed here. With regards to sorting bias, the region exhibiting increased transverse diffusion has high anisotropy with a large separation between maximum and smaller eigenvalues and therefore is not prone to sorting biases or other errors of this type when averaging over larger regions of interest (28). Also, the effect of sorting bias on the middle eigenvalue tends to be small (28) and it is this parameter that reflects the changes discussed here. Averaging the two smaller eigenvalues gives the same result, therefore sorting bias between these two eigenvalues does not affect the comparison. Although there have been many diffusion studies in MS (8 16,26), most if not all of these studies have reported only the directionally-averaged diffusion or anisotropy and have, as in the present study, found increased isotropic ADC and reduced diffusion anisotropy. We have found that the origin of these differences can be better understood by evaluation of the diffusion tensor eigenvalues and by segmentation of the normalappearing brain tissues according to their unique structural properties. In particular, the anisotropic changes are limited to regions of high-anisotropy that correspond to highly-ordered white matter tissue like corpus callosum, internal capsule, and corona radiata. Furthermore, the diffusion in these highly-ordered regions of NAWM in RRMS patients increases only transverse to the fiber tracts. On the other hand, low-anisotropy regions that correspond primarily to cortical and deep gray matter and to some gray/white junction areas also exhibit increased isotropic diffusion. Since the diffusion tensor eigenvalues are not well defined for these low-anisotropy regions, it is not surprising that no direction of preferential diffusion change is observed there. The mid-anisotropy regions correspond to complex white matter structures that include crossing fibers from different tissue tracts. Here again the complexity of the fiber orientations may disguise the preference for diffusion changes transverse to fiber tracts. Our findings may indicate that diffusion changes in normal-appearing tissue of relapsing-remitting patients is best accomplished by focusing on the transverse diffusion in highly-ordered white matter tracts and looking at the isotropic diffusion in low-anisotropy regions including gray matter regions. A recent study of RRMS patients has also indicated increased diffusion and decreased anisotropy in NAWM but increased anisotropy in the basal ganglia (13). We did not observe changes in gray matter anisotropy. However, our anisotropy-based segmentation included both cortical and deep gray matter and we qualitatively ascertained between 50% and 75% of this region to be gray matter tissue. Since the transverse diffusion eigenvalues reflect changes in the most restricted spins, other techniques that may give similar advantages are those techniques using high b information like q-space diffusion and multiexponential fits to diffusion data. Recent neuropathological studies (1 6) provide evidence of axonal damage in NAWM. The etiology of the NAWM damage may be due to Wallerian degeneration distal to damaged axons (2,3,6) and/or microscopic lesions to which anatomical MR images are not sensitive. Recent studies have attempted to better delineate the changes associated with diffusion in Wallerian degeneration in animal (23,24) and human studies (6,25). Pierpaoli et al (25) studied retrograde Wallerian degeneration in the cortical spinal tract of patients who had internal capsule lesions a year after stroke. The results from their study indicated reduced diffusion along the fibers and increased diffusion transverse to the fibers. Beaulieu et al (23) studied crush- and tie-induced injuries in frog sciatic nerves and found decreased longitudinal diffusion and increased transverse diffusion associated with Wallerian degeneration of the nerves. Stanisz et al (24) evaluated degeneration and regeneration of rat sciatic nerves after cutting and crushing, respectively, and determined the same diffusion signature of increased diffusion only transverse to the nerve fibers, with pathological confirmation of demyelination and Wallerian degeneration associated with the degenerating nerves. In distal regions of crushed but regenerating nerves, this study indicated a return to normal anisotropy values. Similarly to the study of Stanisz et al (24), the same mechanism of nerve degeneration and regeneration may occur in the NAWM of RRMS patients, with the lesions playing the role of the insult. Credence may have been given to this mechanism; in studies using proton MR spectroscopy (26) and diffusion (27), changes in the contralateral homologous normal-appearing tissue correlated with the appearance and remittance of MS lesions. In a study of patients with large MS lesions superior to the internal capsule, Simon et al (6) demonstrated delayed T2-hyperintensity along the internal capsule distal from the lesions and interpreted this change in terms of Wallerian degeneration. In general, lesions may be acting as insult to relatively smaller bundles of axons that undergo Wallerian degeneration but remain below the threshold detectable by anatomic MR images. Combined, this evidence and the present study suggest that Wallerian degeneration may be detected in the high-anisotropy NAWM of MS patients by the signature of increased diffusion transverse to the fibers and relatively unchanged or even reduced diffusion along the fibers. Nonetheless, the characteristic change of transverse eigenvalues may not be unique to Wallerian degeneration and further studies with clear histopathology are needed. In conclusion, diffusion changes noted in relapsingremitting MS patients arise from a combination of changes related to the structural properties of the tissue. Anisotropic reductions in the normal-appearing brain regions for RRMS patients compared to normal controls were appreciated only in highly-ordered NAWM regions and arise from increased diffusion transverse to, but not along the white matter tracts. Isotropic diffusion is increased in all regions of the brain including ordered white matter, complex white matter structures, and gray matter. Evaluation of diffusion tensor eigen-

7 426 Henry et al. values and the consideration of the distinct diffusion anisotropy characteristics of different brain regions increase our understanding of and sensitivity to diffusion changes in the normal-appearing brain of RRMS patients. In particular, these results may represent the first in vivo delineation of Wallerian degeneration in the NAWM of RRMS patients by DTI and suggests that the distinct directional diffusion changes may serve as a signature of this process. ACKNOWLEDGMENT Dr. Daniel Pelletier is a National Multiple Sclerosis Society Physician Fellowship Awardee. REFERENCES 1. Allen I, McKeown S. A histological, histochemical and biochemical study of the macroscopically normal white matter in multiple sclerosis. J Neurol Sci 1979;41: Ferguson B, Matyszak MK, Esiri MM, Perry VH. Axonal damage in acute multiple sclerosis lesions. Brain 1997;120: Trapp BD, Peterson J, Ransohoff RM, et al. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998;338: Bitsch A, Schuchardt J, Bunkowski S, Kuhlmann T, Bruck W. Acute axonal injury in multiple sclerosis: correlation with demyelination and inflammation. Brain 2000;123: Evangelou N, Esiri MM, Smith S, Palace J, Matthews PM. Quantitative pathological evidence for axonal loss in normal appearing white matter in multiple sclerosis. Ann Neurol 2000;47: Simon JH, Kinkel RP, Jacobs L, Bub L, Simonian N. A Wallerian degeneration pattern in patients at risk for MS. Neurology 2000;54: Basser PJ, Matiello J, Le Bihan D. Estimation of the effective selfdiffusion tensor from the NMR spin-echo. J Magn Reson B 1994; 103: Werring DJ, Clark CA, Barker GJ, Thompson AJ, Miller DH. Diffusion tensor imaging of lesions and normal appearing white matter in multiple sclerosis. Neurology 1999;52: Bammer R, Augustin M, Strasser-Fuchs S, et al. Magnetic resonance diffusion tensor imaging for characterizing diffuse and focal white matter abnormalities in multiple sclerosis. Magn Reson Med 2000;44: Cercignani M, Iannucci G, Rocca MA, et al. Pathologic damage in MS assessed by diffusion-weighted and magnetization transfer MRI. Neurology 2000;54: Nusbaum AO, Tang CY, Wei T-C, Buchsbaum MS, Atlas SW. Whole-brain diffusion MR histograms differ between MS subtypes. Neurology 2000;54: Ciccarelli O, Werring DJ, Wheeler-Kingshott CAM, et al. Investigation of MS normal-appearing brain using diffusion tensor MRI with clinical correlations. Neurology 2001;56: Cergiani M, Bozzali M, Iannucci G, Comi G, Filippi M. Magnetization transfer ratio and mean diffusivity of normal appearing white and gray matter from patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 2001;70: Iannucci G, Rovaris M, Giacomotti L, Comi G, Filippin M. Correlation of multiple sclerosis measures derived from T2-weighted, magnetization transfer, and diffusion tensor imaging. AJNR Am J Neuroradiol 2001;22: Marinero C, DeStefano N, Iannucci G, et al. Correlates of MS disability assessed in vivo using aggregates of MR quantities. Neurology 2001;56: Christiansen P, Gideon P, Thomsen C, et al. Increased water selfdiffusion in chronic plaques and in apparently normal white matter in patients with multiple sclerosis. Acta Neurol Scand 1993;87: Falconer JC, Ponnada AN. Cerebrospinal fluid-suppressed highresolution diffusion imaging of human brain. Magn Reson Med 1997;37: Kwong KK, McKinstry RC, Chien D, Crawley AP, Pearlman JD, Rosen BR. CSF-suppressed quantitative single-shot diffusion imaging. Magn Reson Med 1991;21: Liu G, van Gelderen P, Duyn J, Moonen CTW. Single-shot diffusion MRI of human brain on a conventional clinical instrument. Magn Reson Med 1996;35: Zacharopoulos NG, Narayana PA. Selective measurement of white matter and gray matter diffusion trace values in normal human brain. Med Phys 1998;25: Normandeau M, Schricker A, Henry RG. Importance of CSF suppression in diffusion tensor measurements. In: Proceedings of ISMRM Workshop on White Matter Disease, Bordeaux, France, Poser CM, Paty DW, Scheinberg L, et al. New diagnostic criteria for multiple sclerosis: guidelines for research protocols. Ann Neurol 1983;13: Beaulieu C, Does MD, Snyder RE, Allen PS. Changes in water diffusion due to Wallerian degeneration in peripheral nerve. Magn Res Med 1996;36: Stanisz GJ, Midha R, Munro CA, Henkelman RM. MR properties of rat sciatic nerve following trauma. Magn Reson Med 2001;45: Pierpaoli C, Barnett A, Sinisia P, et al. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 2001;13: Werring DJ, Brassat D, Droogan AG, et al. The pathogenesis of lesions and normal-appearing white matter changes in multiple sclerosis a serial diffusion study. Brain 2000;123: De Stefano N, Narayanan S, Matthews PM, et al. In vivo evidence for axonal dysfunction remote from focal cerebral demyelination of the type seen in multiple sclerosis. Brain 1999;122: Basser PJ, Pajeevic S. Statistical artifacts in diffusion tensor MRI (DT-MRI) caused by background noise. Magn Res Med 2000;44:41 50.

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