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November 2021; 8 (6) ArticleOpen Access

Infratentorial MRI Findings in Rasmussen Encephalitis Suggest Primary Cerebellar Involvement

View ORCID ProfileJohannes T. Reiter, View ORCID ProfileBastian David, Selma Enders, View ORCID ProfileConrad C. Prillwitz, View ORCID ProfileTobias Bauer, Deniz Atalay, View ORCID ProfileAnna Tietze, Angela M. Kaindl, View ORCID ProfileVera Keil, View ORCID ProfileAlexander Radbruch, View ORCID ProfileBernd Weber, View ORCID ProfileAlbert J. Becker, View ORCID ProfileChristian E. Elger, View ORCID ProfileRainer Surges, View ORCID ProfileTheodor Rüber
First published August 13, 2021, DOI: https://doi.org/10.1212/NXI.0000000000001058
Johannes T. Reiter
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Bastian David
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Selma Enders
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Conrad C. Prillwitz
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Tobias Bauer
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Deniz Atalay
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
MD
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Anna Tietze
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Angela M. Kaindl
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
MD, PhD
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Vera Keil
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Alexander Radbruch
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Bernd Weber
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Albert J. Becker
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Christian E. Elger
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Rainer Surges
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Theodor Rüber
From the Department of Epileptology (J.T.R., B.D., S.E., C.C.P., T.B., C.E.E., R.S., T.R.), University Hospital Bonn; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Department of Pediatric Neurology; Charité–Universitätsmedizin Berlin (D.A., A.M.K.), Center for Chronically Sick Children; Charité–Universitätsmedizin Berlin (A.T.), Institute of Neuroradiology; Charité–Universitätsmedizin Berlin (A.M.K.), Institute for Cell Biology and Neurobiology; Department of Neuroradiology (V.K., A.R.), University Hospital Bonn; Department of Radiology and Nuclear Medicine (V.K.), Vrije Universiteit Amsterdam Medisch Centrum, The Netherlands; Institute of Experimental Epileptology and Cognition Research (B.W.), University Hospital Bonn; and Section for Translational Epilepsy Research (A.J.B.), Department of Neuropathology, University Hospital Bonn, Germany.
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Full PDF
Citation
Infratentorial MRI Findings in Rasmussen Encephalitis Suggest Primary Cerebellar Involvement
Johannes T. Reiter, Bastian David, Selma Enders, Conrad C. Prillwitz, Tobias Bauer, Deniz Atalay, Anna Tietze, Angela M. Kaindl, Vera Keil, Alexander Radbruch, Bernd Weber, Albert J. Becker, Christian E. Elger, Rainer Surges, Theodor Rüber
Neurol Neuroimmunol Neuroinflamm Nov 2021, 8 (6) e1058; DOI: 10.1212/NXI.0000000000001058

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Abstract

Background and Objective Rasmussen encephalitis (RE) is characterized by its unilateral cerebral involvement. However, both ipsi- and contralesional cerebellar atrophy have been anecdotally reported raising questions about the nature and extent of infratentorial findings. Using MRI, we morphometrically investigated the cerebellum and hypothesized abnormalities beyond the effects of secondary atrophy, implicating a primary involvement of the cerebellum by RE.

Methods Voxel-based morphometry of the cerebellum and brainstem was conducted in 57 patients with RE and in 57 matched controls. Furthermore, patient-specific asymmetry indices (AIs) of cerebellar morphometry and fluid-attenuated inversion recovery (FLAIR) intensity were calculated. Using diffusion tensor imaging, the integrity of the cortico-ponto-cerebellar (CPC) tract was assessed. Finally, a spatial independent component analysis (ICA) was used to compare atrophy patterns between groups.

Results Patients with RE showed bilateral cerebellar and predominantly ipsilesional mesencephalic atrophy (p < 0.01). Morphometric AIs revealed ipsilesional < contralesional asymmetry in 27 and ipsilesional > contralesional asymmetry in 30 patients. In patients with predominant ipsilesional atrophy, morphometric AIs strongly correlated with FLAIR intensity AIs (r = 0.86, p < 0.0001). Fractional anisotropy was lower for ipsilesional-to-contralesional CPC tracts than opposite tracts (T = 2.30, p < 0.05). ICA revealed bilateral and strictly ipsi- and contralesional atrophy components in patients with RE (p < 0.05).

Discussion We demonstrated atrophy of the ipsilesional-to-contralesional CPC pathway and, consequently, interpret the loss of contralesional gray matter as secondary crossed cerebellar atrophy. The ipsilesional cerebellar atrophy, however, defies this explanation. Based on FLAIR hyperintensities, we interpret ipsilesional atrophy to be due to inflammation in the scope of a primary involvement of the cerebellum by RE.

Glossary

AI=
asymmetry index;
CON=
controls;
CPC=
cortico-ponto-cerebellar;
DTI=
diffusion tensor imaging;
FA=
fractional anisotropy;
FDR=
false discovery rate;
FLAIR=
fluid-attenuated inversion recovery;
FOD=
fiber orientation distribution;
FSL=
FMRIB Software Library 6.0;
FWE=
family-wise error;
GM=
gray matter;
ICA=
independent component analysis;
RE=
Rasmussen encephalitis;
SUIT=
spatially unbiased infratentorial atlas template;
VBM=
voxel-based morphometry;
WM=
white matter

Footnotes

  • Go to Neurology.org/NN for full disclosures. Funding information is provided at the end of the article.

  • ↵* These authors contributed equally to this work as co–first authors.

  • The Article Processing Charge was funded by the authors.

  • Received March 25, 2021.
  • Accepted in final form June 29, 2021.
  • Copyright © 2021 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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Neurology: Neuroimmunology & Neuroinflammation
Online ISSN: 2332-7812

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