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July 07, 2015; 85 (1) Article

Gadolinium-based MRI characterization of leptomeningeal inflammation in multiple sclerosis

Martina Absinta, Luisa Vuolo, Anuradha Rao, Govind Nair, Pascal Sati, Irene C.M. Cortese, Joan Ohayon, Kaylan Fenton, María I. Reyes-Mantilla, Dragan Maric, Peter A. Calabresi, John A. Butman, Carlos A. Pardo, Daniel S. Reich
First published April 17, 2015, DOI: https://doi.org/10.1212/WNL.0000000000001587
Martina Absinta
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Luisa Vuolo
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Anuradha Rao
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Govind Nair
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Pascal Sati
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Irene C.M. Cortese
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Joan Ohayon
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Kaylan Fenton
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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María I. Reyes-Mantilla
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Dragan Maric
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Peter A. Calabresi
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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John A. Butman
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Carlos A. Pardo
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Daniel S. Reich
From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy; Department of Neurology (M.I.R.-M., P.A.C., C.A.P.), Johns Hopkins School of Medicine, Baltimore; and Diagnostic Radiology Department (J.A.B., D.S.R.), Clinical Center, NIH, Bethesda, MD.
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Citation
Gadolinium-based MRI characterization of leptomeningeal inflammation in multiple sclerosis
Martina Absinta, Luisa Vuolo, Anuradha Rao, Govind Nair, Pascal Sati, Irene C.M. Cortese, Joan Ohayon, Kaylan Fenton, María I. Reyes-Mantilla, Dragan Maric, Peter A. Calabresi, John A. Butman, Carlos A. Pardo, Daniel S. Reich
Neurology Jul 2015, 85 (1) 18-28; DOI: 10.1212/WNL.0000000000001587

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Abstract

Objective: To determine the frequency and nature of leptomeningeal contrast enhancement in multiple sclerosis (MS) via in vivo 3-tesla postcontrast T2-weighted, fluid-attenuated inversion recovery (FLAIR) MRI and 7-tesla postmortem MRI–pathology correlation.

Methods: Brain MRI, using the postcontrast T2-weighted, FLAIR technique, was prospectively collected in 299 MS cases and 37 age-matched neurologically healthy controls. Expert raters evaluated focal gadolinium enhancement in the leptomeningeal compartment. Two progressive MS cases came to autopsy after in vivo MRI characterization. Pathologic and immunohistochemical examination assessed the association of enhancement with leptomeningeal inflammation and adjacent cortical demyelination.

Results: Focal contrast enhancement was detected in the leptomeningeal compartment in 74 of 299 MS cases (25%) vs 1 of 37 neurologically healthy controls (2.7%; p = 0.001). Enhancement was nearly twice as frequent (p = 0.009) in progressive MS (39/118 cases, 33%) as in relapsing-remitting MS (35/181, 19%). Enhancing foci generally remained stable throughout the evaluation period (up to 5.5 years). Pathology showed perivascular lymphocytic and mononuclear infiltration in the enhancing areas in association with flanking subpial cortical demyelination.

Conclusion: Leptomeningeal contrast enhancement occurs frequently in MS and is a noninvasive, in vivo marker of inflammation and associated subpial demyelination. It might therefore enable testing of new treatments aimed at eliminating this inflammation and potentially arresting progressive MS.

GLOSSARY

MS=
multiple sclerosis;
T2-FLAIR=
T2-weighted, fluid-attenuated inversion recovery

Footnotes

  • ↵* These authors contributed equally to this work.

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Editorial, page 12

  • Supplemental data at Neurology.org

  • Received September 18, 2014.
  • Accepted in final form January 15, 2015.
  • © 2015 American Academy of Neurology
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