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March 2019; 6 (2) ArticleOpen Access

MRI phenotypes in MS

Longitudinal changes and miRNA signatures

Christopher C. Hemond, Brian C. Healy, Shahamat Tauhid, Maria A. Mazzola, Francisco J. Quintana, Roopali Gandhi, Howard L. Weiner, Rohit Bakshi
First published February 15, 2019, DOI: https://doi.org/10.1212/NXI.0000000000000530
Christopher C. Hemond
From the Departments of Neurology (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.) and Department of Radiology (R.B.); Brigham and Women's Hospital (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Laboratory for Neuroimaging Research (C.C.H., S.T., R.H.); Partners Multiple Sclerosis Center (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Ann Romney Center for Neurologic Diseases (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); and Harvard Medical School (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W., R.B.), Boston, MA.
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Brian C. Healy
From the Departments of Neurology (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.) and Department of Radiology (R.B.); Brigham and Women's Hospital (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Laboratory for Neuroimaging Research (C.C.H., S.T., R.H.); Partners Multiple Sclerosis Center (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Ann Romney Center for Neurologic Diseases (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); and Harvard Medical School (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W., R.B.), Boston, MA.
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Shahamat Tauhid
From the Departments of Neurology (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.) and Department of Radiology (R.B.); Brigham and Women's Hospital (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Laboratory for Neuroimaging Research (C.C.H., S.T., R.H.); Partners Multiple Sclerosis Center (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Ann Romney Center for Neurologic Diseases (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); and Harvard Medical School (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W., R.B.), Boston, MA.
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Maria A. Mazzola
From the Departments of Neurology (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.) and Department of Radiology (R.B.); Brigham and Women's Hospital (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Laboratory for Neuroimaging Research (C.C.H., S.T., R.H.); Partners Multiple Sclerosis Center (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Ann Romney Center for Neurologic Diseases (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); and Harvard Medical School (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W., R.B.), Boston, MA.
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Francisco J. Quintana
From the Departments of Neurology (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.) and Department of Radiology (R.B.); Brigham and Women's Hospital (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Laboratory for Neuroimaging Research (C.C.H., S.T., R.H.); Partners Multiple Sclerosis Center (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Ann Romney Center for Neurologic Diseases (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); and Harvard Medical School (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W., R.B.), Boston, MA.
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Roopali Gandhi
From the Departments of Neurology (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.) and Department of Radiology (R.B.); Brigham and Women's Hospital (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Laboratory for Neuroimaging Research (C.C.H., S.T., R.H.); Partners Multiple Sclerosis Center (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Ann Romney Center for Neurologic Diseases (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); and Harvard Medical School (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W., R.B.), Boston, MA.
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Howard L. Weiner
From the Departments of Neurology (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.) and Department of Radiology (R.B.); Brigham and Women's Hospital (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Laboratory for Neuroimaging Research (C.C.H., S.T., R.H.); Partners Multiple Sclerosis Center (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Ann Romney Center for Neurologic Diseases (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); and Harvard Medical School (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W., R.B.), Boston, MA.
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Rohit Bakshi
From the Departments of Neurology (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.) and Department of Radiology (R.B.); Brigham and Women's Hospital (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Laboratory for Neuroimaging Research (C.C.H., S.T., R.H.); Partners Multiple Sclerosis Center (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); Ann Romney Center for Neurologic Diseases (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W, R.B.); and Harvard Medical School (C.C.H., B.C.H., S.T., M.A.M., F.J.Q., R.G., H.L.W., R.B.), Boston, MA.
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Citation
MRI phenotypes in MS
Longitudinal changes and miRNA signatures
Christopher C. Hemond, Brian C. Healy, Shahamat Tauhid, Maria A. Mazzola, Francisco J. Quintana, Roopali Gandhi, Howard L. Weiner, Rohit Bakshi
Neurol Neuroimmunol Neuroinflamm Mar 2019, 6 (2) e530; DOI: 10.1212/NXI.0000000000000530

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Abstract

Objective To classify and immunologically characterize persons with MS based on brain lesions and atrophy and their associated microRNA profiles.

Methods Cerebral T2-hyperintense lesion volume (T2LV) and brain parenchymal fraction (BPF) were quantified and used to define MRI phenotypes as follows: type I: low T2LV, low atrophy; type II: high T2LV, low atrophy; type III: low T2LV, high atrophy; type IV: high T2LV, high atrophy, in a large cross-sectional cohort (n = 1,088) and a subset with 5-year lngitudinal follow-up (n = 153). Serum miRNAs were assessed on a third MS cohort with 2-year MRI phenotype stability (n = 98).

Results One-third of the patients had lesion-atrophy dissociation (types II or III) in both the cross-sectional and longitudinal cohorts. At 5 years, all phenotypes had progressive atrophy (p < 0.001), disproportionally in type II (BPF −2.28%). Only type IV worsened in physical disability. Types I and II showed a 5-year MRI phenotype conversion rate of 33% and 46%, whereas III and IV had >90% stability. Type II switched primarily to IV (91%); type I switched primarily to II (47%) or III (37%). Baseline higher age (p = 0.006) and lower BPF (p < 0.001) predicted 5-year phenotype conversion. Each MRI phenotype demonstrated an miRNA signature whose underlying biology implicates blood-brain barrier pathology: hsa.miR.22.3p, hsa.miR.361.5p, and hsa.miR.345.5p were the most valid differentiators of MRI phenotypes.

Conclusions MRI-defined MS phenotypes show high conversion rates characterized by the continuation of either predominant neurodegeneration or inflammation and support the partial independence of these 2 measures. MicroRNA signatures of these phenotypes suggest a role for blood-brain barrier integrity.

Glossary

BPF=
brain parenchymal fraction;
Cq=
cycle quantification;
EDSS=
Expanded Disability Status Scale;
miRNA=
microRNA;
SP=
secondary progressive;
T2LV=
T2-hyperintense lesion volume

Footnotes

  • Funding information and disclosures are provided at the end of the article. Full disclosure form information provided by the authors is available with the full text of this article at Neurology.org/NN.

  • The Article Processing Charge was funded by the authors.

  • Received July 31, 2018.
  • Accepted in final form November 9, 2018.
  • Copyright © 2019 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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