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May 26, 2015; 84 (21) Article

Odor identification and Alzheimer disease biomarkers in clinically normal elderly

Matthew E. Growdon, Aaron P. Schultz, Alexander S. Dagley, Rebecca E. Amariglio, Trey Hedden, Dorene M. Rentz, Keith A. Johnson, Reisa A. Sperling, Mark W. Albers, Gad A. Marshall
First published May 1, 2015, DOI: https://doi.org/10.1212/WNL.0000000000001614
Matthew E. Growdon
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Aaron P. Schultz
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Alexander S. Dagley
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Rebecca E. Amariglio
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Trey Hedden
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Dorene M. Rentz
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Keith A. Johnson
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Reisa A. Sperling
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Mark W. Albers
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Gad A. Marshall
From Harvard Medical School (M.E.G., R.E.A., T.H., D.M.R., K.A.J., R.A.S., M.W.A., G.A.M.) and Harvard T.H. Chan School of Public Health (M.E.G.), Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging (A.P.S., A.S.D., T.H., R.A.S., M.W.A.), Massachusetts General Hospital, Charlestown; Departments of Neurology (A.P.S., A.S.D., R.E.A., D.M.R., R.A.S., M.W.A., G.A.M.), Psychiatry (A.P.S., A.S.D.), and Radiology (T.H., K.A.J.), MassGeneral Institute of Neurodegenerative Disease (M.W.A.), Massachusetts General Hospital, Boston; and Center for Alzheimer Research and Treatment (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.) and Department of Neurology (R.E.A., D.M.R., K.A.J., R.A.S., G.A.M.), Brigham and Women's Hospital, Boston, MA.
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Citation
Odor identification and Alzheimer disease biomarkers in clinically normal elderly
Matthew E. Growdon, Aaron P. Schultz, Alexander S. Dagley, Rebecca E. Amariglio, Trey Hedden, Dorene M. Rentz, Keith A. Johnson, Reisa A. Sperling, Mark W. Albers, Gad A. Marshall
Neurology May 2015, 84 (21) 2153-2160; DOI: 10.1212/WNL.0000000000001614

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Abstract

Objectives: Our objective was to investigate cross-sectional associations between odor identification ability and imaging biomarkers of neurodegeneration and amyloid deposition in clinically normal (CN) elderly individuals, specifically testing the hypothesis that there may be an interaction between amyloid deposition and neurodegeneration in predicting odor identification dysfunction.

Methods: Data were collected on 215 CN participants from the Harvard Aging Brain Study. Measurements included the 40-item University of Pennsylvania Smell Identification Test and neuropsychological testing, hippocampal volume (HV) and entorhinal cortex (EC) thickness from MRI, and amyloid burden using Pittsburgh compound B (PiB) PET. A linear regression model with backward elimination (p < 0.05 retention) evaluated the cross-sectional association between the University of Pennsylvania Smell Identification Test and amyloid burden, HV, and EC thickness, assessing for effect modification by PiB status. Covariates included age, sex, premorbid intelligence, APOE ε4 carrier status, and Boston Naming Test.

Results: In unadjusted univariate analyses, worse olfaction was associated with decreased HV (p < 0.001), thinner EC (p = 0.003), worse episodic memory (p = 0.03), and marginally associated with greater amyloid burden (binary PiB status, p = 0.06). In the multivariate model, thinner EC in PiB-positive individuals (interaction term) was associated with worse olfaction (p = 0.02).

Conclusions: In CN elderly, worse odor identification was associated with markers of neurodegeneration. Furthermore, individuals with elevated cortical amyloid and thinner EC exhibited worse odor identification, elucidating the potential contribution of olfactory testing to detect preclinical AD in CN individuals.

GLOSSARY

Aβ=
β-amyloid;
AD=
Alzheimer disease;
AmNART=
American National Adult Reading Test;
CN=
clinically normal;
DVR=
distribution volume ratio;
EC=
entorhinal cortex;
HV=
hippocampal volume;
MCI=
mild cognitive impairment;
NFT=
neurofibrillary tangle;
PiB=
Pittsburgh compound B;
UPSIT-40=
40-item University of Pennsylvania Smell Identification Test

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 Neurology.org

  • Received November 12, 2014.
  • Accepted in final form February 12, 2015.
  • © 2015 American Academy of Neurology
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