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May 18, 2021; 96 (20) Article

Association of Neighborhood Context, Cognitive Decline, and Cortical Change in an Unimpaired Cohort

View ORCID ProfileJack F.V. Hunt, Nicholas M. Vogt, Erin M. Jonaitis, William R. Buckingham, Rebecca L. Koscik, Megan Zuelsdorff, Lindsay R. Clark, Carey E. Gleason, Menggang Yu, Ozioma Okonkwo, Sterling C. Johnson, Sanjay Asthana, Barbara B. Bendlin, Amy J.H. Kind
First published April 14, 2021, DOI: https://doi.org/10.1212/WNL.0000000000011918
Jack F.V. Hunt
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Nicholas M. Vogt
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Erin M. Jonaitis
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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William R. Buckingham
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Rebecca L. Koscik
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Megan Zuelsdorff
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Lindsay R. Clark
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Carey E. Gleason
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Menggang Yu
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Ozioma Okonkwo
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Sterling C. Johnson
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Sanjay Asthana
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Barbara B. Bendlin
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Amy J.H. Kind
From the Wisconsin Alzheimer's Disease Research Center (J.F.V.H., N.M.V., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Wisconsin Alzheimer's Institute (E.M.J., R.L.K., O.O., S.C.J., S.A., B.B.B.), Department of Medicine, Geriatrics Division (W.R.B., M.Z., L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), Health Services and Care Research Program (W.R.B., A.J.H.K.), and Department of Biostatistics & Medical Informatics (M.Y.), University of Wisconsin School of Medicine and Public Health; University of Wisconsin School of Nursing (M.Z.); and Geriatric Research Education and Clinical Center (GRECC) (L.R.C., C.E.G., O.O., S.C.J., S.A., B.B.B., A.J.H.K.), William S. Middleton Hospital, United States Department of Veterans Affairs, Madison, WI.
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Association of Neighborhood Context, Cognitive Decline, and Cortical Change in an Unimpaired Cohort
Jack F.V. Hunt, Nicholas M. Vogt, Erin M. Jonaitis, William R. Buckingham, Rebecca L. Koscik, Megan Zuelsdorff, Lindsay R. Clark, Carey E. Gleason, Menggang Yu, Ozioma Okonkwo, Sterling C. Johnson, Sanjay Asthana, Barbara B. Bendlin, Amy J.H. Kind
Neurology May 2021, 96 (20) e2500-e2512; DOI: 10.1212/WNL.0000000000011918

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Abstract

Objective To test the hypothesis that neighborhood-level disadvantage is associated with longitudinal measures of neurodegeneration and cognitive decline in an unimpaired cohort.

Methods Longitudinal MRI and cognitive testing data were collected from 601 cognitively unimpaired participants in the Wisconsin Registry for Alzheimer's Prevention Study and the Wisconsin Alzheimer's Disease Research Center clinical cohort. Area Deprivation Index was geospatially determined based on participant residence geocode and ranked relative to state of residence. Linear regression models were fitted to test associations between neighborhood-level disadvantage and longitudinal change in cortical thickness and cognitive test performance. Mediation tests were used to assess whether neurodegeneration and cognitive decline were associated with neighborhood-level disadvantage along the same theoretical causal path.

Results In our middle- to older-aged study population (mean baseline age 59 years), living in the 20% most disadvantaged neighborhoods (n = 19) relative to state of residence was associated with cortical thinning in Alzheimer signature regions (p = 0.002) and decline in the Preclinical Alzheimer's Disease Cognitive Composite (p = 0.04), particularly the Trail-Making Test, part B (p < 0.001), but not Rey Auditory Verbal Learning Test (p = 0.77) or Story Memory Delayed Recall (p = 0.49) subtests. Associations were attenuated but remained significant after controlling for racial and demographic differences between neighborhood-level disadvantage groups. Cortical thinning partially mediated the association between neighborhood-level disadvantage and cognitive decline.

Conclusions In this longitudinal study of cognitively unimpaired adults, living in the most highly disadvantaged neighborhoods was associated with accelerated degeneration in Alzheimer signature regions and cognitive decline. This study provides further evidence for neighborhood-level disadvantage as a risk factor for preclinical neurodegeneration and cognitive decline in certain populations. Limitations of the present study, including a small number of participants from highly disadvantaged neighborhoods and a circumscribed geographic setting, should be explored in larger and more diverse study cohorts.

Glossary

ACS=
American Community Survey;
AD=
Alzheimer disease;
ADI=
Area Deprivation Index;
ADRD=
Alzheimer disease and related dementia;
CAT=
Computational Anatomy Toolbox;
CI=
confidence interval;
LME=
linear mixed effects;
OLS=
ordinary least squares;
PACC-R=
Preclinical Alzheimer's Cognitive Composite–Revised;
RAVLT-L=
Rey Auditory Verbal Learning Test, total trials 1–5;
ROI=
region of interest;
SDOH=
social determinants of health;
SM-D=
Story Memory Delayed Recall;
TMT-B=
Trail-Making Test, part B;
WADRC=
Wisconsin Alzheimer's Disease Research Center;
WRAP=
Wisconsin Registry for Alzheimer's Prevention

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.

  • Received July 9, 2020.
  • Accepted in final form February 24, 2021.
  • © 2021 American Academy of Neurology
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