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February 02, 2021; 96 (5) Article

Multi-shell Diffusion MRI Models for White Matter Characterization in Cerebral Small Vessel Disease

Marek J. Konieczny, Anna Dewenter, Annemieke ter Telgte, Benno Gesierich, Kim Wiegertjes, Sofia Finsterwalder, Anna Kopczak, Mathias Hübner, Rainer Malik, View ORCID ProfileAnil M. Tuladhar, José P. Marques, View ORCID ProfileDavid G. Norris, Alexandra Koch, View ORCID ProfileOlaf Dietrich, Michael Ewers, Reinhold Schmidt, Frank-Erik de Leeuw, View ORCID ProfileMarco Duering
First published November 16, 2020, DOI: https://doi.org/10.1212/WNL.0000000000011213
Marek J. Konieczny
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Anna Dewenter
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Annemieke ter Telgte
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Benno Gesierich
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Kim Wiegertjes
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Sofia Finsterwalder
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Anna Kopczak
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Mathias Hübner
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Rainer Malik
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Anil M. Tuladhar
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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José P. Marques
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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David G. Norris
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Alexandra Koch
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Olaf Dietrich
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Michael Ewers
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Reinhold Schmidt
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Frank-Erik de Leeuw
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Marco Duering
From the Institute for Stroke and Dementia Research (ISD) (M.J.K., A.D., B.G., S.F., A. Kopczak, M.H., R.M., M.E., M.D.) and the Department of Radiology (O.D.), University Hospital, LMU Munich, Germany; Department of Neurology (A.t.T., K.W., A.M.T., F.-E.d.L., M.D.) and Radboud University (J.P.M., D.G.N.), Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, the Netherlands;Population Health Sciences (A.K.), German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany;Department of Neurology (R.S.), Medical University of Graz, Austria; and Munich Cluster for Systems Neurology (SyNergy) (M.D.), Germany.
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Multi-shell Diffusion MRI Models for White Matter Characterization in Cerebral Small Vessel Disease
Marek J. Konieczny, Anna Dewenter, Annemieke ter Telgte, Benno Gesierich, Kim Wiegertjes, Sofia Finsterwalder, Anna Kopczak, Mathias Hübner, Rainer Malik, Anil M. Tuladhar, José P. Marques, David G. Norris, Alexandra Koch, Olaf Dietrich, Michael Ewers, Reinhold Schmidt, Frank-Erik de Leeuw, Marco Duering
Neurology Feb 2021, 96 (5) e698-e708; DOI: 10.1212/WNL.0000000000011213

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Abstract

Objective To test the hypothesis that multi-shell diffusion models improve the characterization of microstructural alterations in cerebral small vessel disease (SVD), we assessed associations with processing speed performance, longitudinal change, and reproducibility of diffusion metrics.

Methods We included 50 patients with sporadic and 59 patients with genetically defined SVD (cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy [CADASIL]) with cognitive testing and standardized 3T MRI, including multi-shell diffusion imaging. We applied the simple diffusion tensor imaging (DTI) model and 2 advanced models: diffusion kurtosis imaging (DKI) and neurite orientation dispersion and density imaging (NODDI). Linear regression and multivariable random forest regression (including conventional SVD markers) were used to determine associations between diffusion metrics and processing speed performance. The detection of short-term disease progression was assessed by linear mixed models in 49 patients with sporadic SVD with longitudinal high-frequency imaging (in total 459 MRIs). Intersite reproducibility was determined in 10 patients with CADASIL scanned back-to-back on 2 different 3T MRI scanners.

Results Metrics from DKI showed the strongest associations with processing speed performance (R2 up to 21%) and the largest added benefit on top of conventional SVD imaging markers in patients with sporadic SVD and patients with CADASIL with lower SVD burden. Several metrics from DTI and DKI performed similarly in detecting disease progression. Reproducibility was excellent (intraclass correlation coefficient >0.93) for DTI and DKI metrics. NODDI metrics were less reproducible.

Conclusion Multi-shell diffusion imaging and DKI improve the detection and characterization of cognitively relevant microstructural white matter alterations in SVD. Excellent reproducibility of diffusion metrics endorses their use as SVD markers in research and clinical care. Our publicly available intersite dataset facilitates future studies.

Classification of evidence This study provides Class I evidence that in patients with SVD, diffusion MRI metrics are associated with processing speed performance.

Glossary

CADASIL=
cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy;
CI=
confidence interval;
DKI=
diffusion kurtosis imaging;
DTI=
diffusion tensor imaging;
FSL=
Functional Magnetic Resonance Imaging of the Brain Software Library;
NODDI=
neurite orientation dispersion and density imaging;
RMSE=
root mean square error;
RUN DMC–inTENse study=
Radboud University Nijmegen Diffusion Tensor and Magnetic Resonance Imaging Cohort–Investigating the Origin and Evolution of Cerebral Small Vessel Disease;
SVD=
small vessel disease;
WMH=
white matter hyperintensities

Footnotes

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

  • ↵* These authors contributed equally to this work.

  • Class of Evidence: NPub.org/coe

  • Received December 19, 2019.
  • Accepted in final form September 21, 2020.
  • © 2020 American Academy of Neurology
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