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Research ArticleULTRA-HIGH-FIELD MRI/IMAGING OF EPILEPSY/DEMYELINATING DISEASES/INFLAMMATION/INFECTION

Multiparametric Characterization and Spatial Distribution of Different MS Lesion Phenotypes

Francesco Tazza, Giacomo Boffa, Simona Schiavi, Caterina Lapucci, Gian Franco Piredda, Emilio Cipriano, Domenico Zacà, Luca Roccatagliata, Tom Hilbert, Tobias Kober, Matilde Inglese and Mauro Costagli
American Journal of Neuroradiology May 2024, DOI: https://doi.org/10.3174/ajnr.A8271
Francesco Tazza
aFrom the Departments of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (F.T., G.B., S.S., E.C., M.I., M.C.), University of Genoa, Genoa, Italy
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  • ORCID record for Francesco Tazza
Giacomo Boffa
aFrom the Departments of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (F.T., G.B., S.S., E.C., M.I., M.C.), University of Genoa, Genoa, Italy
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Simona Schiavi
aFrom the Departments of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (F.T., G.B., S.S., E.C., M.I., M.C.), University of Genoa, Genoa, Italy
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Caterina Lapucci
bIstituto di Ricovero e Cura a Carattere Scientifico (C.L., L.R., M.I., M.C.), Ospedale Policlinico San Martino, Genoa, Italy
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Gian Franco Piredda
cAdvanced Clinical Imaging Technology (G.F.P., T.H., T.K.), Siemens Healthineers International AG, Lausanne, Switzerland
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Emilio Cipriano
aFrom the Departments of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (F.T., G.B., S.S., E.C., M.I., M.C.), University of Genoa, Genoa, Italy
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Domenico Zacà
fSiemens Healthcare (D.Z.), Milan, Italy
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Luca Roccatagliata
bIstituto di Ricovero e Cura a Carattere Scientifico (C.L., L.R., M.I., M.C.), Ospedale Policlinico San Martino, Genoa, Italy
gDepartment of Health Sciences (L.R.), University of Genoa, Genoa, Italy
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Tom Hilbert
cAdvanced Clinical Imaging Technology (G.F.P., T.H., T.K.), Siemens Healthineers International AG, Lausanne, Switzerland
dDepartment of Radiology (T.H., T.K.), Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland
eLTS5 (T.H., T.K.), École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Tobias Kober
cAdvanced Clinical Imaging Technology (G.F.P., T.H., T.K.), Siemens Healthineers International AG, Lausanne, Switzerland
dDepartment of Radiology (T.H., T.K.), Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland
eLTS5 (T.H., T.K.), École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Matilde Inglese
aFrom the Departments of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (F.T., G.B., S.S., E.C., M.I., M.C.), University of Genoa, Genoa, Italy
bIstituto di Ricovero e Cura a Carattere Scientifico (C.L., L.R., M.I., M.C.), Ospedale Policlinico San Martino, Genoa, Italy
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Mauro Costagli
aFrom the Departments of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (F.T., G.B., S.S., E.C., M.I., M.C.), University of Genoa, Genoa, Italy
bIstituto di Ricovero e Cura a Carattere Scientifico (C.L., L.R., M.I., M.C.), Ospedale Policlinico San Martino, Genoa, Italy
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Figures

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  • FIG 1.
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    FIG 1.

    Flow chart of the MS lesions evaluation based on QSM and SMWI visualization.

  • FIG 2.
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    FIG 2.

    Examples of different MS lesion phenotypes. A, B, and C, MS lesions (black arrow) on FLAIR (upper image) and on QSM (lower image) classified, respectively, in HYPER, ISO-HYPO, and PRLs groups. D and E, MS lesions (white arrows) on FLAIR (left), QSM (center), and SMWI (right), which were relocated, respectively, from PRLs to HYPER and from HYPER to ISO-HYPO groups; particularly in D, the hyperintense rim on QSM was determined to be composed of 2 veins (visible as hypointense signal in SMWI). E, The hyperintensity on QSM located at the center of the lesion was a central vein, as shown on SMWI.

  • FIG 3.
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    FIG 3.

    Quantitative MR imaging metrics of myelin and axonal loss in different MS lesion phenotypes. Comparisons were performed using ANOVA with Bonferroni post hoc comparisons, controlling for age, sex, lesion volume, and subject identification as confounding factors. T1-relaxation times are expressed in milliseconds. **P ≤ .05; ****P < .001.

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    Table 1:

    Demographic and clinical features

    Patients with MS (n = 53)Healthy Controls (n = 24)P Value
    Female (No.) (%)34 (64.2%)16 (66.7%).830
    Mean age (yr)43.64 (SD, 12.58)38.12 (SD, 13.2).642
    RRMS (No.) (%)40 (75.5%)NANA
    Mean disease duration (yr)9.91 (SD, 10.56)NANA
    EDSS (median) (range)2.0 (0–7.0)NANA
    ARMSS (mean) (SD)3.99 (SD, 2.32)NANA
    Treatment
     No therapy (No.) (%)9 (17%)NANA
     Low-efficacy DMT (No.) (%)10 (19%)NANA
     High-efficacy DMT (No.) (%)34 (64%)NANA
    • Note:—RRMS indicates relapsing-remitting MS; NA, not applicable; DMT, disease-modifying therapy.

    • View popup
    Table 2:

    Comparison of lesion volume and quantitative MR imaging values of the 3 lesion phenotypes

    ISO-HYPO (Mean) (SD)HYPER (Mean) (SD)PRL (Mean) (SD)ISO-HYPO vs HYPER (P Value)ISO-HYPO vs PRL (P Value)HYPER vs PRL (P Value)
    Lesion volume (μL)311.44 (1069.32)820.93 (1733.99)955.35 (891.77)<.001a<.001a.455
    ICVF0.47 (0.09)0.42 (0.08)0.41 (0.08)<.001a<.001a.188
    ODI0.23 (0.07)0.21 (0.06)0.22 (0.05).060.506.703
    FWF0.03 (0.03)0.04 (0.05)0.07 (0.07).006a<.001a<.001a
    MWF0.075 (0.035)0.068 (0.031)0.062 (0.030).016a.022a.336
    T1-relaxometry (ms)1027.05 (131.35)1077.18 (157.63)1181.43 (157.01).001a<.001a<.001a
    QSM values (ppb)–9.10 (23.7)9.06 (25.1)7.75 (23.5)<.001a<.001a.567
    Distance from ventricular CSF (mm)14.6 (9.8)12.5 (9.7)10.5 (7.4).059.018a.177
    • Note:—ppb indicates parts per billion.

    • ↵a Statistically significant.

    • View popup
    Table 3:

    Pearson correlation among age, EDSS, and ARMSS with the volume of the different MS lesion phenotypes

    ISO-HYPOHYPERPRLHYPER + PRL
    rP ValuerP ValuerP ValuerP Value
    Age0.045.763−0.060.689−0.015.920−0.082.583
    EDSS−0.180.2320.282.057−0.160.2890.228.127
    ARMSS−0.268.0790.382.011a−0.167.2770.342.023a
    • ↵aStatistically significant.

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Francesco Tazza, Giacomo Boffa, Simona Schiavi, Caterina Lapucci, Gian Franco Piredda, Emilio Cipriano, Domenico Zacà, Luca Roccatagliata, Tom Hilbert, Tobias Kober, Matilde Inglese, Mauro Costagli
Multiparametric Characterization and Spatial Distribution of Different MS Lesion Phenotypes
American Journal of Neuroradiology May 2024, DOI: 10.3174/ajnr.A8271

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Multiparametric Characterization and Spatial Distribution of Different MS Lesion Phenotypes
Francesco Tazza, Giacomo Boffa, Simona Schiavi, Caterina Lapucci, Gian Franco Piredda, Emilio Cipriano, Domenico Zacà, Luca Roccatagliata, Tom Hilbert, Tobias Kober, Matilde Inglese, Mauro Costagli
American Journal of Neuroradiology May 2024, DOI: 10.3174/ajnr.A8271
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