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May 30, 2017; 88 (22) Article

BDNF Val66Met predicts cognitive decline in the Wisconsin Registry for Alzheimer's Prevention

Elizabeth A. Boots, Stephanie A. Schultz, Lindsay R. Clark, Annie M. Racine, Burcu F. Darst, Rebecca L. Koscik, Cynthia M. Carlsson, Catherine L. Gallagher, Kirk J. Hogan, Barbara B. Bendlin, Sanjay Asthana, Mark A. Sager, Bruce P. Hermann, Bradley T. Christian, Dena B. Dubal, Corinne D. Engelman, Sterling C. Johnson, Ozioma C. Okonkwo
First published May 3, 2017, DOI: https://doi.org/10.1212/WNL.0000000000003980
Elizabeth A. Boots
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Stephanie A. Schultz
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Lindsay R. Clark
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Annie M. Racine
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Burcu F. Darst
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Rebecca L. Koscik
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Cynthia M. Carlsson
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Catherine L. Gallagher
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Kirk J. Hogan
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Barbara B. Bendlin
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Sanjay Asthana
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Mark A. Sager
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Bruce P. Hermann
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Bradley T. Christian
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Dena B. Dubal
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Corinne D. Engelman
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Sterling C. Johnson
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Ozioma C. Okonkwo
From the Geriatric Research Education and Clinical Center (E.A.B., S.A.S., L.R.C., C.M.C., C.L.G., B.B.B., S.A., S.C.J., O.C.C.), William S. Middleton Memorial Veterans Hospital; Wisconsin Alzheimer's Disease Research Center (E.A.B., S.A.S., L.R.C., A.M.R., C.M.C., C.L.G., B.B.B., S.A., M.A.S., B.P.H., B.T.C., S.C.J., O.C.O.), Wisconsin Alzheimer's Institute (L.R.C., R.L.K., C.M.C., K.J.H., B.B.B., S.A., M.A.S., B.P.H., C.D.E., S.C.J., O.C.O.), Department of Population Health Sciences (B.F.D., C.D.E.), Department of Neurology (C.L.G., B.P.H.), Department of Anesthesiology (K.J.H.), Department of Radiology (M.A.S.), and Department of Medical Physics (B.T.C.), University of Wisconsin School of Medicine and Public Health, Madison; and Department of Neurology (D.B.D.), University of California, San Francisco.
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Full PDF
Citation
BDNF Val66Met predicts cognitive decline in the Wisconsin Registry for Alzheimer's Prevention
Elizabeth A. Boots, Stephanie A. Schultz, Lindsay R. Clark, Annie M. Racine, Burcu F. Darst, Rebecca L. Koscik, Cynthia M. Carlsson, Catherine L. Gallagher, Kirk J. Hogan, Barbara B. Bendlin, Sanjay Asthana, Mark A. Sager, Bruce P. Hermann, Bradley T. Christian, Dena B. Dubal, Corinne D. Engelman, Sterling C. Johnson, Ozioma C. Okonkwo
Neurology May 2017, 88 (22) 2098-2106; DOI: 10.1212/WNL.0000000000003980

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Abstract

Objective: To examine the influence of the brain-derived neurotrophic factor (BDNF) Val66Met polymorphism on longitudinal cognitive trajectories in a large, cognitively healthy cohort enriched for Alzheimer disease (AD) risk and to understand whether β-amyloid (Aβ) burden plays a moderating role in this relationship.

Methods: One thousand twenty-three adults (baseline age 54.94 ± 6.41 years) enrolled in the Wisconsin Registry for Alzheimer's Prevention underwent BDNF genotyping and cognitive assessment at up to 5 time points (average follow-up 6.92 ± 3.22 years). A subset (n = 140) underwent 11C-Pittsburgh compound B (PiB) scanning. Covariate-adjusted mixed-effects regression models were used to elucidate the effect of BDNF on cognitive trajectories in 4 cognitive domains, including verbal learning and memory, speed and flexibility, working memory, and immediate memory. Secondary mixed-effects regression models were conducted to examine whether Aβ burden, indexed by composite PiB load, modified any observed BDNF-related cognitive trajectories.

Results: Compared to BDNF Val/Val homozygotes, Met carriers showed steeper decline in verbal learning and memory (p = 0.002) and speed and flexibility (p = 0.017). In addition, Aβ burden moderated the relationship between BDNF and verbal learning and memory such that Met carriers with greater Aβ burden showed even steeper cognitive decline (p = 0.033).

Conclusions: In a middle-aged cohort with AD risk, carriage of the BDNF Met allele was associated with steeper decline in episodic memory and executive function. This decline was exacerbated by greater Aβ burden. These results suggest that the BDNF Val66Met polymorphism may play an important role in cognitive decline and could be considered as a target for novel AD therapeutics.

GLOSSARY

Aβ=
β-amyloid;
AD=
Alzheimer disease;
BDNF=
brain-derived neurotrophic factor;
DVR=
distribution volume ratio;
Met=
methionine;
PiB=
11C-Pittsburgh compound B;
RAVLT=
Rey Auditory Verbal Learning Test;
SNP=
single nucleotide polymorphism;
Val=
valine;
WRAP=
Wisconsin Registry for Alzheimer's Prevention

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 July 19, 2016.
  • Accepted in final form March 13, 2017.
  • © 2017 American Academy of Neurology
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