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January 04, 2022; 98 (1) Research Article

Association Between Antemortem FLAIR White Matter Hyperintensities and Neuropathology in Brain Donors Exposed to Repetitive Head Impacts

Madeline Uretsky, Sylvain Bouix, Ronald J. Killiany, Yorghos Tripodis, Brett Martin, Joseph Palmisano, Asim Z. Mian, Karen Buch, View ORCID ProfileChad Farris, Daniel H. Daneshvar, Brigid Dwyer, Lee Goldstein, Douglas Katz, View ORCID ProfileChristopher Nowinski, Robert Cantu, Neil Kowall, Bertrand Russell Huber, View ORCID ProfileRobert A. Stern, Victor E. Alvarez, View ORCID ProfileThor D. Stein, Ann McKee, Jesse Mez, Michael L. Alosco
First published November 24, 2021, DOI: https://doi.org/10.1212/WNL.0000000000013012
Madeline Uretsky
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Sylvain Bouix
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Ronald J. Killiany
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Yorghos Tripodis
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Brett Martin
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Joseph Palmisano
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Asim Z. Mian
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Karen Buch
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Chad Farris
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Daniel H. Daneshvar
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Brigid Dwyer
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Lee Goldstein
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Douglas Katz
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Christopher Nowinski
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Robert Cantu
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Neil Kowall
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Bertrand Russell Huber
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Robert A. Stern
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Victor E. Alvarez
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Thor D. Stein
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Ann McKee
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Jesse Mez
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Michael L. Alosco
From the Boston University Alzheimer's Disease Research Center and CTE Center, Department of Neurology (M.U., R.J.K., Y.T., D.H.D., B.D., L.G., D.K., C.N., R.C., N.K., B.R.H., R.A.S., V.E.A., T.D.S., A.M., J.M., M.L.A.), Department of Anatomy and Neurobiology (R.J.K., R.A.S.), Center for Biomedical Imaging (R.J.K.), Department of Radiology (A.Z.M., C.F.), Framingham Heart Study (C.F., T.D.S., A.M., J.M.), Department of Pathology and Laboratory Medicine (L.G., N.K., T.D.S., A.M.), Department of Psychiatry (L.G.), Department of Ophthalmology (L.G.), and Department of Neurosurgery (R.C., R.A.S.), Boston University School of Medicine; Department of Psychiatry, Psychiatry Neuroimaging Laboratory (S.B.), Brigham and Women's Hospital, Harvard Medical School; Department of Biostatistics (Y.T.) and Biostatistics and Epidemiology Data Analytics Center (B.M., J.P.), Boston University School of Public Health; Departments of Radiology (K.B.) and Physical Medicine & Rehabilitation (D.H.D.), Massachusetts General Hospital, Boston; Braintree Rehabilitation Hospital (B.D., D.K.); Department of Biomedical, Electrical & Computer Engineering (L.G.), Boston University College of Engineering; Concussion Legacy Foundation (C.N., R.C.), Boston; Department of Neurosurgery (R.C.), Emerson Hospital, Concord; VA Boston Healthcare System (B.R.H., V.E.A., T.D.S., A.M.), US Department of Veterans Affairs, Jamaica Plain; National Center for PTSD (B.R.H., V.E.A.), VA Boston Healthcare, Jamaica Plain; and Department of Veterans Affairs Medical Center (V.E.A., T.D.S., A.M.), Bedford, MA.
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Association Between Antemortem FLAIR White Matter Hyperintensities and Neuropathology in Brain Donors Exposed to Repetitive Head Impacts
Madeline Uretsky, Sylvain Bouix, Ronald J. Killiany, Yorghos Tripodis, Brett Martin, Joseph Palmisano, Asim Z. Mian, Karen Buch, Chad Farris, Daniel H. Daneshvar, Brigid Dwyer, Lee Goldstein, Douglas Katz, Christopher Nowinski, Robert Cantu, Neil Kowall, Bertrand Russell Huber, Robert A. Stern, Victor E. Alvarez, Thor D. Stein, Ann McKee, Jesse Mez, Michael L. Alosco
Neurology Jan 2022, 98 (1) e27-e39; DOI: 10.1212/WNL.0000000000013012

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Abstract

Background and Objectives Late neuropathologies of repetitive head impacts from contact sports can include chronic traumatic encephalopathy (CTE) and white matter degeneration. White matter hyperintensities (WMH) on fluid-attenuated inversion recovery (FLAIR) MRI scans are often viewed as microvascular disease from vascular risk, but might have unique underlying pathologies and risk factors in the setting of repetitive head impacts. We investigated the neuropathologic correlates of antemortem WMH in brain donors exposed to repetitive head impacts. The association between WMH and repetitive head impact exposure and informant-reported cognitive and daily function were tested.

Methods This imaging–pathologic correlation study included symptomatic male decedents exposed to repetitive head impacts. Donors had antemortem FLAIR scans from medical records and were without evidence of CNS neoplasm, large vessel infarcts, hemorrhage, or encephalomalacia. WMH were quantified using log-transformed values for total lesion volume (TLV), calculated using the lesion prediction algorithm from the Lesion Segmentation Toolbox. Neuropathologic assessments included semiquantitative ratings of white matter rarefaction, cerebrovascular disease, hyperphosphorylated tau (p-tau) severity (CTE stage, dorsolateral frontal cortex), and β-amyloid (Aβ). Among football players, years of play was a proxy for repetitive head impact exposure. Retrospective informant-reported cognitive and daily function were assessed using the Cognitive Difficulties Scale (CDS) and Functional Activities Questionnaire (FAQ). Regression models controlled for demographics, diabetes, hypertension, and MRI resolution. Statistical significance was defined as p ≤ 0.05.

Results The sample included 75 donors: 67 football players and 8 nonfootball contact sport athletes or military veterans. Dementia was the most common MRI indication (64%). Fifty-three (70.7%) had CTE at autopsy. Log TLV was associated with white matter rarefaction (odds ratio [OR] 2.32, 95% confidence interval [CI] 1.03, 5.24; p = 0.04), arteriolosclerosis (OR 2.38, 95% CI 1.02, 5.52; p = 0.04), CTE stage (OR 2.58, 95% CI 1.17, 5.71; p = 0.02), and dorsolateral frontal p-tau severity (OR 3.03, 95% CI 1.32, 6.97; p = 0.01). There was no association with Aβ. More years of football play was associated with log TLV (unstandardized β 0.04, 95% CI 0.01, 0.06; p = 0.01). Greater log TLV correlated with higher FAQ (unstandardized β 4.94, 95% CI 0.42, 8.57; p = 0.03) and CDS scores (unstandardized β 15.35, 95% CI −0.27, 30.97; p = 0.05).

Discussion WMH might capture long-term white matter pathologies from repetitive head impacts, including those from white matter rarefaction and p-tau, in addition to microvascular disease. Prospective imaging–pathologic correlation studies are needed.

Classification of Evidence This study provides Class IV evidence of associations between FLAIR white matter hyperintensities and neuropathologic changes (white matter rarefaction, arteriolosclerosis, p-tau accumulation), years of American football play, and reported cognitive symptoms in symptomatic brain donors exposed to repetitive head impacts.

Glossary

Aβ=
β-amyloid;
AD=
Alzheimer disease;
BU=
Boston University;
bvFTD=
behavioral variant frontotemporal dementia;
CAA=
cerebral amyloid angiopathy;
CDS=
Cognitive Difficulties Scale;
CERAD=
Consortium to Establish a Registry for Alzheimer's Disease;
CI=
confidence interval;
CTE=
chronic traumatic encephalopathy;
FAQ=
Functional Activities Questionnaire;
FLAIR=
fluid-attenuated inversion recovery;
LPA=
lesion prediction algorithm;
LST=
Lesion Segmentation Toolbox;
NFL=
National Football League;
NINDS/NIBIB=
National Institutes of Neurological Disease and Stroke/National Institute of Brain Imaging and Behavior;
p-tau=
hyperphosphorylated tau;
TBI=
traumatic brain injury;
TLN=
total lesion number;
TLV=
total lesion volume;
UNITE=
Understanding Neurologic Injury in Traumatic Encephalopathy;
VRF=
vascular risk factor;
WMH=
white matter hyperintensities

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Class of Evidence: NPub.org/coe

  • Podcast: NPub.org/Podcast9801

  • Received February 4, 2021.
  • Accepted in final form September 29, 2021.
  • © 2021 American Academy of Neurology
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  • Reader Response: Association Between Antemortem FLAIR White Matter Hyperintensities and Neuropathology in Brain Donors Exposed to Repetitive Head Impacts
    • Nitin K. Sethi, Associate Professor of Neurology, New York-Presbyterian Hospital, Weill Cornell Medical Center, New York, NY 10065
    Submitted January 09, 2022
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Neurology | Print ISSN:0028-3878
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