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March 2022; 9 (2) ArticleOpen Access

Cortical and Subcortical Dysmetabolism Are Dynamic Markers of Clinical Disability and Course in Anti-LGI1 Encephalitis

View ORCID ProfileEero Rissanen, Kelsey Carter, View ORCID ProfileSteven Cicero, John Ficke, Marie Kijewski, Mi-Ae Park, Joseph Kijewski, Emily Stern, Tanuja Chitnis, David Silbersweig, Howard L. Weiner, Chun K. Kim, Jennifer Lyons, Joshua P. Klein, Shamik Bhattacharyya, Tarun Singhal
First published January 28, 2022, DOI: https://doi.org/10.1212/NXI.0000000000001136
Eero Rissanen
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
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Kelsey Carter
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
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Steven Cicero
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
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John Ficke
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
BA
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Marie Kijewski
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
DSc
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  • For correspondence: mkijewski@bwh.harvard.edu
Mi-Ae Park
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
PhD
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  • For correspondence: miaepark@gmail.com
Joseph Kijewski
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
BS
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Emily Stern
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
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Tanuja Chitnis
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
MD
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David Silbersweig
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
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Howard L. Weiner
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
MD
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Chun K. Kim
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
MD
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  • For correspondence: kimchun@gmail.com
Jennifer Lyons
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
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Joshua P. Klein
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
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Shamik Bhattacharyya
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
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Tarun Singhal
From the PET Imaging Program in Neurologic Diseases (E.R., K.C., S.C., J.F., T.S.) and Brigham Multiple Sclerosis Center (E.R., T.C., H.L.W., S.B., T.S.), Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women's Hospital and Harvard Medical School; Division of Nuclear Medicine and Molecular Imaging (M.K.), Department of Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Medical Physics Section (M.-A.P.), Radiology Department, University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (J.K.), Brigham and Women's Hospital, Boston, MA; Ceretype Neuromedicine (E.S.), Cambridge, MA; Functional Neuroimaging Laboratory (D.S.), Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; Nuclear Medicine (C.K.K.), Department of Medicine, College of Medicine, Hanyang University, Seoul, Republic of Korea; Biogen Inc. (J.L.), Cambridge, MA; and Department of Neurology (J.P.K.), Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
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Citation
Cortical and Subcortical Dysmetabolism Are Dynamic Markers of Clinical Disability and Course in Anti-LGI1 Encephalitis
Eero Rissanen, Kelsey Carter, Steven Cicero, John Ficke, Marie Kijewski, Mi-Ae Park, Joseph Kijewski, Emily Stern, Tanuja Chitnis, David Silbersweig, Howard L. Weiner, Chun K. Kim, Jennifer Lyons, Joshua P. Klein, Shamik Bhattacharyya, Tarun Singhal
Neurol Neuroimmunol Neuroinflamm Mar 2022, 9 (2) e1136; DOI: 10.1212/NXI.0000000000001136

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Abstract

Background and Objectives This [18F]fluorodeoxyglucose (FDG) PET study evaluates the accuracy of semiquantitative measurement of putaminal hypermetabolism in identifying anti–leucine-rich, glioma–inactivated-1 (LGI1) protein autoimmune encephalitis (AE). In addition, the extent of brain dysmetabolism, their association with clinical outcomes, and longitudinal metabolic changes after immunotherapy in LGI1-AE are examined.

Methods FDG-PET scans from 49 age-matched and sex-matched subjects (13 in LGI1-AE group, 15 in non–LGI1-AE group, 11 with Alzheimer disease [AD], and 10 negative controls [NCs]) and follow-up scans from 8 patients with LGI1 AE on a median 6 months after immunotherapy were analyzed. Putaminal standardized uptake value ratios (SUVRs) normalized to global brain (P-SUVRg), thalamus (P/Th), and midbrain (P/Mi) were evaluated for diagnostic accuracy. SUVRg was applied for all other analyses.

Results P-SUVRg, P/Th, and P/Mi were higher in LGI1-AE group than in non–LGI1-AE group, AD group, and NCs (all p < 0.05). P/Mi and P-SUVRg differentiated LGI1-AE group robustly from other groups (areas under the curve 0.84–0.99). Mediotemporal lobe (MTL) SUVRg was increased in both LGI1-AE and non–LGI1-AE groups when compared with NCs (both p < 0.05). SUVRg was decreased in several frontoparietal regions and increased in pallidum, caudate, pons, olfactory, and inferior occipital gyrus in LGI1-AE group when compared with that in NCs (all p < 0.05). In LGI1-AE group, both MTL and putaminal hypermetabolism were reduced after immunotherapy. Normalization of regional cortical dysmetabolism associated with clinical improvement at the 6- and 20-month follow-up.

Discussion Semiquantitative measurement of putaminal hypermetabolism with FDG-PET may be used to distinguish LGI1-AE from other pathologies. Metabolic abnormalities in LGI1-AE extend beyond putamen and MTL into other subcortical and cortical regions. FDG-PET may be used in evaluating disease evolution in LGI1-AE.

Classification of Evidence This study provides Class II evidence that semiquantitative measures of putaminal metabolism on PET can differentiate patients with LGI1-AE from patients without LGI1-AE, patients with AD, or NCs.

Glossary

[18F]FDG=
[18F]fluorodeoxyglucose;
AAL=
automated anatomical labeling;
AD=
Alzheimer disease;
AE=
autoimmune encephalitis;
AMPA=
α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid;
APS=
antiphospholipid syndrome;
AUC=
area under the curve;
BWH=
Brigham and Women's Hospital;
DMN=
default mode network;
FBDS=
facio-brachial dystonic seizures;
GABA=
gamma-aminobutyric acid;
HE=
Hashimoto encephalopathy;
IQR=
interquartile range;
LE=
limbic encephalitis;
LGI1=
leucine-rich, glioma–inactivated-1;
mRS=
modified Rankin scale;
MTL=
mediotemporal lobe;
NC=
negative controls;
P/Mi=
putamen-to-midbrain ratio;
P/Th=
putamen-to-thalamus ratio;
P-SUVRg=
putaminal global brain normalized SUV ratio;
ROC=
receiver operating characteristic;
ROI=
regions of interest;
SS=
Sjögren syndrome;
SUVR=
standardized uptake value ratio

Footnotes

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

  • The Article Processing Charge was funded by the authors.

  • Received June 29, 2021.
  • Accepted in final form December 14, 2021.
  • Copyright © 2022 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
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