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November 05, 2013; 81 (19) Article

MRI and pathology of REM sleep behavior disorder in dementia with Lewy bodies

Melissa E. Murray, Tanis J. Ferman, Bradley F. Boeve, Scott A. Przybelski, Timothy G. Lesnick, Amanda M. Liesinger, Matthew L. Senjem, Jeffrey L. Gunter, Gregory M. Preboske, Val J. Lowe, Prashanthi Vemuri, Brittany N. Dugger, David S. Knopman, Glenn E. Smith, Joseph E. Parisi, Michael H. Silber, Neill R. Graff-Radford, Ronald C. Petersen, Clifford R. Jack, Dennis W. Dickson, Kejal Kantarci
First published October 9, 2013, DOI: https://doi.org/10.1212/01.wnl.0000435299.57153.f0
Melissa E. Murray
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Tanis J. Ferman
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Bradley F. Boeve
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Scott A. Przybelski
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Timothy G. Lesnick
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Amanda M. Liesinger
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Matthew L. Senjem
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Jeffrey L. Gunter
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Gregory M. Preboske
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Val J. Lowe
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Prashanthi Vemuri
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Brittany N. Dugger
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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David S. Knopman
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Glenn E. Smith
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Joseph E. Parisi
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Michael H. Silber
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Neill R. Graff-Radford
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Ronald C. Petersen
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Clifford R. Jack Jr
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Dennis W. Dickson
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Kejal Kantarci
From the Department of Neuroscience (M.E.M., A.M.L., B.N.D., D.W.D.), Psychiatry and Psychology (T.J.F.), and Neurology (N.R.G.-R.), Mayo Clinic, Jacksonville, FL; and Department of Neurology (B.F.B., D.S.K., M.H.S., R.C.P.), Biomedical Statistics (S.A.P., T.G.L.), Radiology (M.L.S., J.L.G., G.M.P., P.V., C.R.J., K.K.), Nuclear Medicine (V.J.L.), Psychology (G.E.S.), Laboratory Medicine and Pathology (J.E.P.), and Center for Sleep Medicine (M.H.S.), Mayo Clinic, Rochester, MN.
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Full PDF
Citation
MRI and pathology of REM sleep behavior disorder in dementia with Lewy bodies
Melissa E. Murray, Tanis J. Ferman, Bradley F. Boeve, Scott A. Przybelski, Timothy G. Lesnick, Amanda M. Liesinger, Matthew L. Senjem, Jeffrey L. Gunter, Gregory M. Preboske, Val J. Lowe, Prashanthi Vemuri, Brittany N. Dugger, David S. Knopman, Glenn E. Smith, Joseph E. Parisi, Michael H. Silber, Neill R. Graff-Radford, Ronald C. Petersen, Clifford R. Jack, Dennis W. Dickson, Kejal Kantarci
Neurology Nov 2013, 81 (19) 1681-1689; DOI: 10.1212/01.wnl.0000435299.57153.f0

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Abstract

Objective: To determine structural MRI and digital microscopic characteristics of REM sleep behavior disorder in individuals with low-, intermediate-, and high-likelihood dementia with Lewy bodies (DLB) at autopsy.

Methods: Patients with autopsy-confirmed low-, intermediate-, and high-likelihood DLB, according to the probability statement recommended by the third report of the DLB Consortium, and antemortem MRI, were identified (n = 75). The clinical history was assessed for presence (n = 35) and absence (n = 40) of probable REM sleep behavior disorder (pRBD), and patients' antemortem MRIs were compared using voxel-based morphometry. Pathologic burdens of phospho-tau, β-amyloid, and α-synuclein were measured in regions associated with early neuropathologic involvement, the hippocampus and amygdala.

Results: pRBD was present in 21 patients (60%) with high-likelihood, 12 patients (34%) with intermediate-likelihood, and 2 patients (6%) with low-likelihood DLB. Patients with pRBD were younger, more likely to be male (p ≤ 0.001), and had a more frequent neuropathologic diagnosis of diffuse (neocortical) Lewy body disease. In the hippocampus and amygdala, phospho-tau and β-amyloid burden were lower in patients with pRBD compared with those without pRBD (p < 0.01). α-Synuclein burden did not differ in the hippocampus, but trended in the amygdala. Patients without pRBD had greater atrophy of temporoparietal cortices, hippocampus, and amygdala (p < 0.001) than those with pRBD; atrophy of the hippocampus (p = 0.005) and amygdala (p = 0.02) were associated with greater phospho-tau burdens in these regions.

Conclusion: Presence of pRBD is associated with a higher likelihood of DLB and less severe Alzheimer-related pathology in the medial temporal lobes, whereas absence of pRBD is characterized by Alzheimer-like atrophy patterns on MRI and increased phospho-tau burden.

GLOSSARY

AD=
Alzheimer disease;
DLB=
dementia with Lewy bodies;
DSM-III-R=
Diagnostic and Statistical Manual of Mental Disorders, 3rd edition, revised;
MCI=
mild cognitive impairment;
NFT=
neurofibrillary tangle;
pRBD=
probable REM sleep behavior disorder;
RBD=
REM sleep behavior disorder;
VBM=
voxel-based morphometry

Footnotes

  • 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.

  • Supplemental data at www.neurology.org

  • Received April 7, 2013.
  • Accepted in final form August 9, 2013.
  • © 2013 American Academy of Neurology
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