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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 August 2024, 45 (8) 1166-1174; 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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  • ORCID record for Giacomo Boffa
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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  • ORCID record for Caterina Lapucci
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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Abstract

BACKGROUND AND PURPOSE: MS lesions exhibit varying degrees of axonal and myelin damage. A comprehensive description of lesion phenotypes could contribute to an improved radiologic evaluation of smoldering inflammation and remyelination processes. This study aimed to identify in vivo distinct MS lesion types using quantitative susceptibility mapping and susceptibility mapping–weighted imaging and to characterize them through T1-relaxometry, myelin mapping, and diffusion MR imaging. The spatial distribution of lesion phenotypes in relation to ventricular CSF was investigated.

MATERIALS AND METHODS: MS lesions of 53 individuals were categorized into iso- or hypointense lesions, hyperintense lesions, and paramagnetic rim lesions, on the basis of their appearance on quantitative susceptibility mapping alone, according to published criteria, and with the additional support of susceptibility mapping–weighted imaging. Susceptibility values, T1-relaxation times, myelin and free water fractions, intracellular volume fraction, and the orientation dispersion index were compared among lesion phenotypes. The distance of the geometric center of each lesion from the ventricular CSF was calculated.

RESULTS: Eight hundred ninety-six MS lesions underwent the categorization process using quantitative susceptibility mapping and susceptibility mapping–weighted imaging. The novel use of susceptibility mapping–weighted images, which revealed additional microvasculature details, led us to re-allocate several lesions to different categories, resulting in a 35.6% decrease in the number of paramagnetic rim lesions, a 22.5% decrease in hyperintense lesions, and a 17.2% increase in iso- or hypointense lesions, with respect to the categorization based on quantitative susceptibility mapping only. The outcome of the categorization based on the joint use of quantitative susceptibility mapping and susceptibility mapping–weighted imaging was that 44.4% of lesions were iso- or hypointense lesions, 47.9% were hyperintense lesions, and 7.7% were paramagnetic rim lesions. A worsening gradient was observed from iso- or hypointense lesions to hyperintense lesions to paramagnetic rim lesions in T1-relaxation times, myelin water fraction, free water fraction, and intracellular volume fraction. Paramagnetic rim lesions were located closer to ventricular CSF than iso- or hypointense lesions. The volume of hyperintense lesions was associated with a more severe disease course.

CONCLUSIONS: Quantitative susceptibility mapping and susceptibility mapping–weighted imaging allow in vivo classification of MS lesions into different phenotypes, characterized by different levels of axonal and myelin loss and spatial distribution. Hyperintense lesions and paramagnetic rim lesions, which have the most severe microstructural damage, were more often observed in the periventricular WM and were associated with a more severe disease course.

ABBREVIATIONS:

ARMSS
Age-Related MS Severity Score
EDSS
Expanded Disability Status Scale
FWF
free water fraction
HC
healthy control
HYPER
hyperintense lesions
ISO-HYPO
iso- or hypointense lesions
ICVF
intracellular volume fraction
MWF
myelin water fraction
ODI
orientation dispersion index
PRL
paramagnetic rim lesion
QSM
quantitative susceptibility mapping
SMWI
susceptibility mapping–weighted imaging
  • © 2024 by American Journal of Neuroradiology
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American Journal of Neuroradiology: 45 (8)
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Vol. 45, Issue 8
1 Aug 2024
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Cite this article
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 Aug 2024, 45 (8) 1166-1174; DOI: 10.3174/ajnr.A8271

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Multiparametric 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 Aug 2024, 45 (8) 1166-1174; DOI: 10.3174/ajnr.A8271
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