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Research ArticleUltra-High-Field MRI/Imaging of Epilepsy/Demyelinating Diseases/Inflammation/Infection

Diffusion- and Tractography-Based Characterization of Tissue Damage Within and Surrounding Paramagnetic Rim Lesions in Multiple Sclerosis

Maryam Mohebbi, Jack A. Reeves, Dejan Jakimovski, Alexander Bartnik, Niels Bergsland, Fahad Salman, Ferdinand Schweser, Bianca Weinstock-Guttman, Robert Zivadinov and Michael G. Dwyer
American Journal of Neuroradiology March 2025, 46 (3) 611-619; DOI: https://doi.org/10.3174/ajnr.A8524
Maryam Mohebbi
aFrom the Buffalo Neuroimaging Analysis Center (M.M., J.A.R., D.J., A.B., N.B., F.Salman, F.Schweser, R.Z., M.G.D.), Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York
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Jack A. Reeves
aFrom the Buffalo Neuroimaging Analysis Center (M.M., J.A.R., D.J., A.B., N.B., F.Salman, F.Schweser, R.Z., M.G.D.), Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York
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Dejan Jakimovski
aFrom the Buffalo Neuroimaging Analysis Center (M.M., J.A.R., D.J., A.B., N.B., F.Salman, F.Schweser, R.Z., M.G.D.), Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York
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Alexander Bartnik
aFrom the Buffalo Neuroimaging Analysis Center (M.M., J.A.R., D.J., A.B., N.B., F.Salman, F.Schweser, R.Z., M.G.D.), Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York
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Niels Bergsland
aFrom the Buffalo Neuroimaging Analysis Center (M.M., J.A.R., D.J., A.B., N.B., F.Salman, F.Schweser, R.Z., M.G.D.), Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York
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Fahad Salman
aFrom the Buffalo Neuroimaging Analysis Center (M.M., J.A.R., D.J., A.B., N.B., F.Salman, F.Schweser, R.Z., M.G.D.), Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York
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Ferdinand Schweser
aFrom the Buffalo Neuroimaging Analysis Center (M.M., J.A.R., D.J., A.B., N.B., F.Salman, F.Schweser, R.Z., M.G.D.), Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York
bCenter for Biomedical Imaging at the Clinical Translational Science Institute (F.Schweser, R.Z.), University at Buffalo, State University of New York, Buffalo, New York
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Bianca Weinstock-Guttman
cJacobs Neurological Institute (B.W.-G.), Buffalo, New York
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Robert Zivadinov
aFrom the Buffalo Neuroimaging Analysis Center (M.M., J.A.R., D.J., A.B., N.B., F.Salman, F.Schweser, R.Z., M.G.D.), Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York
bCenter for Biomedical Imaging at the Clinical Translational Science Institute (F.Schweser, R.Z.), University at Buffalo, State University of New York, Buffalo, New York
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Michael G. Dwyer
aFrom the Buffalo Neuroimaging Analysis Center (M.M., J.A.R., D.J., A.B., N.B., F.Salman, F.Schweser, R.Z., M.G.D.), Department of Neurology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York
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  • FIG 1.
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    FIG 1.

    Examples of PRL (pink) and non-PRL T2 (light green) lesions on QSM and FLAIR images from 2 different pwMS.

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    FIG 2.

    Diffusion-based fiber tractography, specifically highlighting the tracts located within a 10-mm radius of the lesions (A and B are PRL tracts and C is non-PRL tracts). A, Colors represent the direction of diffusion—blue for superior-inferior, green for anterior-posterior, and red for left-right. B, Notably, tracts closer to the lesions correspond to lower FA values, as indicated by the accompanying color bar.

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    FIG 3.

    The result of tractography of PRL-connected tracts versus PRL-nonconnected tracts through the selection of different region types as presented in the Supplemental Data. A, PRL-nonconnected tracts along with ROIs and without the ROIs (a), which clearly shows a holelike area of the ROIs that are terminative regions, restricting the tracts from entering the regions. B, The PRL-connected tracts with and without ROIs (b). C, The same tracts from the coronal view. The color bar shows the FA value.

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    Table 1:

    Demographic and clinical characteristics of the study population

    AllPRL−PRL +
    Overall (n = 115)Overall (n = 66)Overall (n = 49)
    PRL number, mean ± SD0.65 ± 1.90–1.52 ± 2.92
    T2 LN, mean ± SD19.5 ± 11.1218.32 ± 12.620.85 ± 9.05
    T2 LVa, mean ± SD, mL10.94 ± 13.648.35 ± 10.5913.92 ± 16.06
    Sex
     Female88 (76.5%)55 (83.3%)33 (67.3%)
     Male27 (23.5%)11 (16.7%)16 (32.6%)
    Age (yrs)
     Mean ± SD52.9 ± 11.854.4 ± 11.150.5 ± 12.6
     Median [min, max]53.2 [23.2, 75.2]53.6 [23.2, 73.4]52.2 [24.2, 75.2]
    Disease (type of MS)
     RRMS78 (67.8%)46 (69.7%)33 (67.3%)
     PMS37 (32.1%)20 (30.3%)16 (32.6%)
    Disease duration in years
     Mean ± SD19.5 ± 10.120.2 ± 9.8118.5 ± 10.6
     Median [min, max]17.0 [5.00, 47.0]18.0 [5.00, 47.0]17.0 [5.00, 40.0]
    EDSS
     Mean ± SD3.44 ± 2.053.19 ± 1.843.71 ± 2.27
     Median [min, max]3.00 [0, 9.00]2.50 [0, 7.00]3.00 [0, 9.00]
     Missing3 (2.6%)2 (3.0%)1 (2.1%)
    • ↵a Overall T2 LVs before excluding non-PRLs within close vicinity of PRLs by using double-threshold.

    • Note:—LN indicates lesion number; EDSS = Expanded Disability Status Scale; PMS = progressive MS.

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    Table 2:

    Comparison of the diffusion parameters within the nearby tracts connected to all lesions (PRLs and non-PRLs) versus within the lesions themselvesa

    MetricsTractsWithin-LesionCohen dP Valueq-Value
    FA, mean ± SD0.383 ± 0.0540.296 ± 0.0521.38<.0010.001
    QA, mean ± SD0.326 ± 0.0620.290 ± 0.0580.76<.0010.001
    MD, mean ± SD1.092 ± 0.1471.232 ± 0.218−0.70<.0010.001
    AD, mean ± SD1.539 ± 0.1841.572 ± 0.206−0.24.020.02
    RD, mean ± SD0.869 ± 0.1401.018 ± 0.195−0.89<.0010.001
    Iso, mean ± SD0.789 ± 0.2260.836 ± 0.255−0.77<.0010.001
    RDI, mean ± SD0.519 ± 0.0940.535 ± 0.111−0.41<.0010.001
    • ↵a Paired t-tests and effect sizes were calculated within subjects who had at least 1 PRL (n = 49), P < .05 considered statistically significant. q-value represents the Benjamini-Hochberg FDR corrected P value at the table level.

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    Table 3:

    Comparison of diffusion parameters between PRLs versus non-PRLs, within the lesionsa

    MetricsPRLsNon-PRLsCohen dP Valueq-Value
    Total LV,b mean ± SD, mL0.459 ± 1.258.33 ± 11.03–<.0010.008
    FA, mean ± SD0.279 ± 0.0470.302 ± 0.056−0.30.040.16
    QA, mean ± SD0.283 ± 0.0670.219 ± 0.056−0.13.380.43
    MD, mean ± SD1.232 ± 0.2181.186 ± 0.1120.16.260.35
    AD, mean ± SD1.581 ± 0.2651.560 ± 0.1350.07.630.63
    RD, mean ± SD1.058 ± 0.2000.999 ± 0.1150.20.150.26
    Iso, mean ± SD0.855 ± 0.2570.818 ± 0.2200.28.090.24
    RDI, mean ± SD0.542 ± 0.1120.529 ± 0.0860.22.160.26
    • ↵a Paired t-test was calculated within subjects who had at least 1 PRL (n = 49), P < .05 considered statistically significant. q-value represents the Benjamini-Hochberg FDR corrected P value at the table level.

    • ↵b Non-PRL T2 LVs after excluding non-PRL T2 lesions overlapping or confluent with PRLs.

    • View popup
    Table 4:

    Comparison of diffusion metrics between PRL-connected and non-PRL T2-lesion connected tracts near lesionsa

    MetricsPRL ConnectedNon-PRL T2 Lesion ConnectedCohen dP Valueq-Value
    Total LV,b mean ± SD, mL0.459 ± 1.258.33 ± 11.03–< .0010.004
    FA, mean ± SD0.354 ± 0.0470.391 ± 0.056–0.56< .0010.004
    QA, mean ± SD0.315 ± 0.0670.328 ± 0.056–0.17.270.36
    MD, mean ± SD1.092 ± 0.2181.101 ± 0.112–0.04.750.75
    AD, mean ± SD1.496 ± 0.2651.562 ± 0.135–0.23.100.16
    RD, mean ± SD0.890 ± 0.2000.871 ± 0.1150.09.510.58
    Iso, mean ± SD0.814 ± 0.2570.766 ± 0.2200.43.0070.02
    RDI, mean ± SD0.534 ± 0.1120.508 ± 0.0860.37.020.04
    • ↵a Paired t-test was calculated within subjects who had at least 1 PRL (n = 49), P < .05 considered statistically significant. q-value represents the Benjamini-Hochberg FDR corrected P value at the table level.

    • ↵b Non-PRL T2 LVs after excluding non-PRL T2 lesions adjacent to PRLs.

    • View popup
    Table 5:

    Comparison of diffusion metrics in PRL-connected versus PRL-nonconnected tracts (surrounding white matter)a

    MetricsPRL ConnectedPRL Nonconnected Surrounding TractsCohen dP Valueq-Value
    FA, mean ± SD0.354 ± 0.0470.354 ± 0.0480.00.980.98
    QA, mean ± SD0.315 ± 0.0670.298 ± 0.0620.44.0030.02
    MD, mean ± SD1.092 ± 0.2181.077 ± 0.2250.11.450.63
    AD, mean ± SD1.496 ± 0.2651.467 ± 0.2560.19.210.46
    RD, mean ± SD0.890 ± 0.2000.881 ± 0.2130.06.680.79
    Iso, mean ± SD0.814 ± 0.2570.799 ± 0.2480.39.260.46
    RDI, mean ± SD0.534 ± 0.1120.523 ± 0.1070.41.210.46
    • ↵a Paired t-test was calculated within subjects who had at least 1 PRL (n = 49), P < .05 considered statistically significant. q-value represents the Benjamini-Hochberg FDR corrected P value at the table level.

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Maryam Mohebbi, Jack A. Reeves, Dejan Jakimovski, Alexander Bartnik, Niels Bergsland, Fahad Salman, Ferdinand Schweser, Bianca Weinstock-Guttman, Robert Zivadinov, Michael G. Dwyer
Diffusion- and Tractography-Based Characterization of Tissue Damage Within and Surrounding Paramagnetic Rim Lesions in Multiple Sclerosis
American Journal of Neuroradiology Mar 2025, 46 (3) 611-619; DOI: 10.3174/ajnr.A8524

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Tissue Damage Characterization in MS Using DWI
Maryam Mohebbi, Jack A. Reeves, Dejan Jakimovski, Alexander Bartnik, Niels Bergsland, Fahad Salman, Ferdinand Schweser, Bianca Weinstock-Guttman, Robert Zivadinov, Michael G. Dwyer
American Journal of Neuroradiology Mar 2025, 46 (3) 611-619; DOI: 10.3174/ajnr.A8524
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