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Abstract

Objective:

To investigate the association between periventricular white mater hyperintensities (PVWMH) and biomarkers of elevated cerebral β-amyloid (Aβ) in the Alzheimer's Disease Neuroimaging Initiative, a large prospective multicenter observational study.

Methods:

The burden of frontal, parietal, and occipital PVWMH on 3T fluid-attenuated inversion recovery MRI was evaluated in 698 cognitively normal participants and participants with mild cognitive impairment (MCI) using a novel semiquantitative visual rating scale. Results were correlated with CSF-Aβ, florbetapir-PET, and fluorodeoxyglucose (FDG)–PET.

Results:

Increased burden of parietal, occipital, and frontal PVWMH was associated with elevated cerebral amyloid evidenced by high florbetapir-PET signal (p < 0.01) and low CSF-Aβ (p < 0.01). In logistic regression models, including PVWMH, age, sex, APOE status, vascular risk factors, pulse pressure, vascular secondary prevention medications, education, ethnicity, and race, parietal, occipital, and frontal PVWMH burden was independently associated with high florbetapir-PET uptake (p < 0.05). In a similar logistic regression model, parietal and occipital (p < 0.05) but not frontal (p = 0.05) PVWMH were independently associated with CSF-Aβ. Weaker associations were found between parieto-occipital PVWMH and elevated CSF-tau (p < 0.05) and occipital PVWMH and elevated CSF-phospho-tau (p < 0.05). PVWMH were associated with cerebral hypometabolism on FDG-PET independent of CSF-Aβ levels (p < 0.05). Absolute and consistency of agreement intraclass correlation coefficients were, respectively, 0.83 and 0.83 for frontal, 0.78 and 0.8 for parietal, and 0.45 and 0.75 for occipital PVWMH measurements.

Conclusions:

Increased PVWMH were associated with elevated cerebral amyloid independent of potential confounders such as age, APOE genotype, and vascular risk factors. The mechanisms underlying the association between PVWMH and cerebral amyloid remain to be clarified.

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Supplementary Material

File (appendix_e-1.pdf)
File (coinvestigators.pdf)
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File (tables.pdf)

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Information & Authors

Information

Published In

Neurology®
Volume 86Number 6February 9, 2016
Pages: 535-543
PubMed: 26747881

Publication History

Received: June 1, 2015
Accepted: October 19, 2015
Published online: January 8, 2016
Published in print: February 9, 2016

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Disclosure

M. Marnane, O. Al-Jawadi, S. Mortazavi, K. Pogorzelec, and B. Wang report no disclosures relevant to the manuscript. H. Feldman reports having been the UBC site principal investigator for ADNI through 2008. He is currently UBC site co-Investigator for ADNI. He has no other disclosures related to this study. G. Hsiung reports being the UBC site principal investigator for ADNI since 2008. He has no other disclosures related to this study. Go to Neurology.org for full disclosures.

Study Funding

Dr. Hsiung acknowledges funding support from the Ralph Fisher Professorship in Alzheimer's Research (Alzheimer Society of British Columbia, Canada) and the CIHR Clinical Genetics Investigatorship award. Dr. Marnane's salary was funded by an unrestricted research fellowship award from the Heart and Stroke Foundation of Canada. Data collection and sharing for this project was funded by ADNI (National Institutes of Health grant U01 AG024904) and DOD ADNI (Department of Defense award number W81XWH-12-2-0012). ADNI is funded by the National Institute on Aging, the National Institute of Biomedical Imaging and Bioengineering, and through contributions from the following: AbbVie; Alzheimer's Association; Alzheimer's Drug Discovery Foundation; Araclon Biotech; BioClinica, Inc.; Biogen; Bristol-Myers Squibb Company; CereSpir, Inc.; Eisai Inc.; Elan Pharmaceuticals, Inc.; Eli Lilly and Company; EuroImmun; F. Hoffmann-La Roche Ltd. and its affiliated company Genentech, Inc.; Fujirebio; GE Healthcare; IXICO Ltd.; Janssen Alzheimer Immunotherapy Research & Development, LLC; Johnson & Johnson Pharmaceutical Research & Development LLC; Lumosity; Lundbeck; Merck & Co., Inc.; Meso Scale Diagnostics, LLC; NeuroRx Research; Neurotrack Technologies; Novartis Pharmaceuticals Corporation; Pfizer Inc.; Piramal Imaging; Servier; Takeda Pharmaceutical Company; and Transition Therapeutics. The Canadian Institutes of Health Research provides funds to support ADNI clinical sites in Canada. Private sector contributions are facilitated by the Foundation for the NIH (www.fnih.org). The grantee organization is the Northern California Institute for Research and Education, and the study is coordinated by the Alzheimer's Disease Cooperative Study at the University of California, San Diego. ADNI data are disseminated by the Laboratory for Neuroimaging at the University of Southern California.

Authors

Affiliations & Disclosures

Michael Marnane, MD, PhD
From the Clinic for Alzheimer Disease and Related Disorders, Djavad Mowafaghian Center for Brain Health (M.M., O.O.A.-J., S.M., K.J.P., B.W.W., H.H.F., G.-Y.R.H.), and Department of Medicine, Division of Neurology (M.M., H.H.F., G.-Y.R.H.), University of British Columbia, Vancouver, Canada.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
(1) American Academy of Neurology fellow travel award (2) Alzheimer Association International Conference fellow travel award
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
Heart and Stroke Foundation of Canada (fellowship salary award)
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Osama O. Al-Jawadi
From the Clinic for Alzheimer Disease and Related Disorders, Djavad Mowafaghian Center for Brain Health (M.M., O.O.A.-J., S.M., K.J.P., B.W.W., H.H.F., G.-Y.R.H.), and Department of Medicine, Division of Neurology (M.M., H.H.F., G.-Y.R.H.), University of British Columbia, Vancouver, Canada.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Shervin Mortazavi
From the Clinic for Alzheimer Disease and Related Disorders, Djavad Mowafaghian Center for Brain Health (M.M., O.O.A.-J., S.M., K.J.P., B.W.W., H.H.F., G.-Y.R.H.), and Department of Medicine, Division of Neurology (M.M., H.H.F., G.-Y.R.H.), University of British Columbia, Vancouver, Canada.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Kathleen J. Pogorzelec, BSc
From the Clinic for Alzheimer Disease and Related Disorders, Djavad Mowafaghian Center for Brain Health (M.M., O.O.A.-J., S.M., K.J.P., B.W.W., H.H.F., G.-Y.R.H.), and Department of Medicine, Division of Neurology (M.M., H.H.F., G.-Y.R.H.), University of British Columbia, Vancouver, Canada.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Bing Wei Wang, MD
From the Clinic for Alzheimer Disease and Related Disorders, Djavad Mowafaghian Center for Brain Health (M.M., O.O.A.-J., S.M., K.J.P., B.W.W., H.H.F., G.-Y.R.H.), and Department of Medicine, Division of Neurology (M.M., H.H.F., G.-Y.R.H.), University of British Columbia, Vancouver, Canada.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Howard H. Feldman, MD
From the Clinic for Alzheimer Disease and Related Disorders, Djavad Mowafaghian Center for Brain Health (M.M., O.O.A.-J., S.M., K.J.P., B.W.W., H.H.F., G.-Y.R.H.), and Department of Medicine, Division of Neurology (M.M., H.H.F., G.-Y.R.H.), University of British Columbia, Vancouver, Canada.
Disclosure
Scientific Advisory Boards:
1.
1. Commercial; Eli Lilly and Co: SAB 2. Commercial; Biogen Idec: SAB 3. Commercial Genentech: DMC 4. Commercial Eisai LTD: DSMB 5. Commercial ISIS Pharmaceuticals: Advisory Board 6. Commercial Arena Pharmaceuticals: Advisory Board Payments from Commercial Organizations to UBC 6. Not for Profit: Tau Consortium: SAB honoraria
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
1. Not for Profit: Tau Consortium Investigator Meetings 2015 2. Not for Profit: New York Academy of Sciences and US Against Alzheimer's Disease 2013 and 2014 (travel expenses) 3. Not for Profit: Alzheimer Society of Canada 2015 (travel expenses) 4. Not for Profit: US Alzheimer Association 2015 4. Not for Profit: Brain Canada 2014 (travel expenses)
Editorial Boards:
1.
NONE
Patents:
1.
US Serial Number PCT/2007/070008 Detecting and Treating Dementia
Publishing Royalties:
1.
Royalties from the book Atlas of Alzheimer?s Disease (2007) Informa Health London
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
1. Commercial Arena Pharmaceuticals LTD: 2014
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
1. Canadian Institutes of Health Research CIHR # 287674 (2013-18)role co Principal Investigator, 2. CIHR Consortium for Neurodegeneration and Aging co Principal Investigator (2014-19), 3. CIHR Canadian Pipeline for AD Therapeutics 2015 Principal Investigator (2015-16)
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Ging-Yuek R. Hsiung, MD, MHSc
From the Clinic for Alzheimer Disease and Related Disorders, Djavad Mowafaghian Center for Brain Health (M.M., O.O.A.-J., S.M., K.J.P., B.W.W., H.H.F., G.-Y.R.H.), and Department of Medicine, Division of Neurology (M.M., H.H.F., G.-Y.R.H.), University of British Columbia, Vancouver, Canada.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
Dr. Hsiung has received research support as a clinical trials site investigator from Eli Lilly, Hoffman-La Roche, and TauRx, and has received honorarium for participation in expert review committee with Merck and Eli Lilly.
Research Support, Government Entities:
1.
Dr. Hsiung has provided investigator's report to the British Columbia Ministry of Health on the Alzheimer Disease Therapeutic Initiative.
Research Support, Academic Entities:
1.
Dr. Hsiung is supported by a Clinical Genetics Investigatorship award from the CIHR, and has received research funding from the CIHR, Alzheimer Society of Canada, and NIH.
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
For the Alzheimer's Disease Neuroimaging Initiative
From the Clinic for Alzheimer Disease and Related Disorders, Djavad Mowafaghian Center for Brain Health (M.M., O.O.A.-J., S.M., K.J.P., B.W.W., H.H.F., G.-Y.R.H.), and Department of Medicine, Division of Neurology (M.M., H.H.F., G.-Y.R.H.), University of British Columbia, Vancouver, Canada.

Notes

Correspondence to Dr. Marnane: [email protected]
Data used in preparation of this article were obtained from the Alzheimer's Disease Neuroimaging Initiative (ADNI) database (adni.loni.usc.edu). As such, the investigators within the ADNI contributed to the design and implementation of ADNI and/or provided data but did not participate in analysis or writing of this report. A complete listing of ADNI investigators can be found at Neurology.org.
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.

Author Contributions

Dr. Michael Marnane contributed to design and conceptualization of the study, analysis and interpretation of the data, developing the image analysis paradigm, and drafting and revising the manuscript for intellectual content. Osama O. Al-Jawadi contributed by analyzing the data, developing the image analysis paradigm, and drafting the manuscript. Shervin Mortazavi contributed by analyzing the data and developing the image analysis paradigm. Kathleen Pogorzelec contributed by analyzing the data and developing the image analysis paradigm. Dr. Bing Wei Wang contributed by analyzing the data and developing the image analysis paradigm. Dr. Howard H. Feldman contributed by revising the manuscript for intellectual content. Dr. Ging-Yuek R. Hsiung contributed to conceptualization of the study, supervision of the analysis, and revising the manuscript for intellectual content.

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