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November 08, 2022; 99 (19) Research Article

Socioeconomic Status, Biological Aging, and Memory in a Diverse National Sample of Older US Men and Women

Justina Avila-Rieger, Indira C. Turney, Jet M.J. Vonk, Precious Esie, Dominika Seblova, Vanessa R. Weir, View ORCID ProfileDaniel W. Belsky, View ORCID ProfileJennifer J. Manly
First published August 29, 2022, DOI: https://doi.org/10.1212/WNL.0000000000201032
Justina Avila-Rieger
From the Taub Institute for Research on Alzheimer's Disease and the Aging Brain (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Gertrude H. Sergievsky Center (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Department of Neurology (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Julius Center for Health Sciences and Primary Care (J.M.J.V.), Department of Epidemiology, University Medical Center Utrecht and Utrecht University, Utrecht, The Netherlands; Department of Epidemiology (P.E., D.W.B.), Columbia University Mailman School of Public Health, New York; and Butler Columbia Aging Center (D.W.B.), Columbia University Mailman School of Public Health, New York, NY.
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Indira C. Turney
From the Taub Institute for Research on Alzheimer's Disease and the Aging Brain (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Gertrude H. Sergievsky Center (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Department of Neurology (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Julius Center for Health Sciences and Primary Care (J.M.J.V.), Department of Epidemiology, University Medical Center Utrecht and Utrecht University, Utrecht, The Netherlands; Department of Epidemiology (P.E., D.W.B.), Columbia University Mailman School of Public Health, New York; and Butler Columbia Aging Center (D.W.B.), Columbia University Mailman School of Public Health, New York, NY.
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Jet M.J. Vonk
From the Taub Institute for Research on Alzheimer's Disease and the Aging Brain (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Gertrude H. Sergievsky Center (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Department of Neurology (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Julius Center for Health Sciences and Primary Care (J.M.J.V.), Department of Epidemiology, University Medical Center Utrecht and Utrecht University, Utrecht, The Netherlands; Department of Epidemiology (P.E., D.W.B.), Columbia University Mailman School of Public Health, New York; and Butler Columbia Aging Center (D.W.B.), Columbia University Mailman School of Public Health, New York, NY.
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Precious Esie
From the Taub Institute for Research on Alzheimer's Disease and the Aging Brain (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Gertrude H. Sergievsky Center (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Department of Neurology (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Julius Center for Health Sciences and Primary Care (J.M.J.V.), Department of Epidemiology, University Medical Center Utrecht and Utrecht University, Utrecht, The Netherlands; Department of Epidemiology (P.E., D.W.B.), Columbia University Mailman School of Public Health, New York; and Butler Columbia Aging Center (D.W.B.), Columbia University Mailman School of Public Health, New York, NY.
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Dominika Seblova
From the Taub Institute for Research on Alzheimer's Disease and the Aging Brain (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Gertrude H. Sergievsky Center (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Department of Neurology (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Julius Center for Health Sciences and Primary Care (J.M.J.V.), Department of Epidemiology, University Medical Center Utrecht and Utrecht University, Utrecht, The Netherlands; Department of Epidemiology (P.E., D.W.B.), Columbia University Mailman School of Public Health, New York; and Butler Columbia Aging Center (D.W.B.), Columbia University Mailman School of Public Health, New York, NY.
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Vanessa R. Weir
From the Taub Institute for Research on Alzheimer's Disease and the Aging Brain (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Gertrude H. Sergievsky Center (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Department of Neurology (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Julius Center for Health Sciences and Primary Care (J.M.J.V.), Department of Epidemiology, University Medical Center Utrecht and Utrecht University, Utrecht, The Netherlands; Department of Epidemiology (P.E., D.W.B.), Columbia University Mailman School of Public Health, New York; and Butler Columbia Aging Center (D.W.B.), Columbia University Mailman School of Public Health, New York, NY.
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Daniel W. Belsky
From the Taub Institute for Research on Alzheimer's Disease and the Aging Brain (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Gertrude H. Sergievsky Center (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Department of Neurology (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Julius Center for Health Sciences and Primary Care (J.M.J.V.), Department of Epidemiology, University Medical Center Utrecht and Utrecht University, Utrecht, The Netherlands; Department of Epidemiology (P.E., D.W.B.), Columbia University Mailman School of Public Health, New York; and Butler Columbia Aging Center (D.W.B.), Columbia University Mailman School of Public Health, New York, NY.
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Jennifer J. Manly
From the Taub Institute for Research on Alzheimer's Disease and the Aging Brain (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Gertrude H. Sergievsky Center (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Department of Neurology (J.A.-R., I.C.T., J.M.J.V., D.S., V.R.W., J.J.M.), College of Physicians and Surgeons, Columbia University, New York; Julius Center for Health Sciences and Primary Care (J.M.J.V.), Department of Epidemiology, University Medical Center Utrecht and Utrecht University, Utrecht, The Netherlands; Department of Epidemiology (P.E., D.W.B.), Columbia University Mailman School of Public Health, New York; and Butler Columbia Aging Center (D.W.B.), Columbia University Mailman School of Public Health, New York, NY.
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  • ORCID record for Jennifer J. Manly
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Socioeconomic Status, Biological Aging, and Memory in a Diverse National Sample of Older US Men and Women
Justina Avila-Rieger, Indira C. Turney, Jet M.J. Vonk, Precious Esie, Dominika Seblova, Vanessa R. Weir, Daniel W. Belsky, Jennifer J. Manly
Neurology Nov 2022, 99 (19) e2114-e2124; DOI: 10.1212/WNL.0000000000201032

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Abstract

Background and Objectives Exposure to socioeconomic disadvantage is associated with early-onset cognitive aging. Biological aging, the progressive loss of system integrity that occurs as we age, is proposed as a modifiable process mediating this health inequality. We examined whether socioeconomic disparities in cognitive aging in mid-to late-life adults is explained by accelerated biological aging similarly across race, ethnicity, and sex/gender.

Methods Data were from a prospective cohort study of the US Health and Retirement Study DNA methylation substudy. Socioeconomic status (SES) was measured from years of education and household wealth at baseline. The extent and pace of biological aging were quantified using 3 DNA methylation measures: PhenoAge, GrimAge, and DunedinPoAm. Cognitive aging was measured from repeated longitudinal assessments of immediate and delayed word recall. Latent growth curve modeling estimated participants' level of memory performance and rate of decline over 2–11 follow-up assessments spanning 2–20 years. Multiple-group models were estimated to assess whether the relationship between SES and memory trajectories was mediated by biological aging across racial-ethnic by sex/gender subgroups.

Results Data from a total of 3,997 adults aged 50–100 years were analyzed. Participants with lower SES had a lower memory performance, had a faster decline, and exhibited accelerated biological aging (SES effect size associations [β] ranged from 0.08 to 0.41). Accelerated biological aging was associated with decreased memory performance and faster memory decline (effect size range 0.03–0.23). SES-biological aging associations were the strongest for White men and women and weakest for Latinx women. The relationship between biological aging measures and memory was weaker for Black participants compared with that for White and Latinx people. In mediation analysis, biological aging accounted for 4%–27% of the SES-memory gradient in White participants. There was little evidence of mediation in Black or Latinx participants.

Discussion Among a national sample of mid-to late-life adults, DNA methylation measures of biological aging were variably associated with memory trajectories and SES across White, Black, and Latinx mid-to late-life adults. These results challenge the assumption that DNA methylation biomarkers of aging that were developed in primarily White people can equivalently quantify aging processes affecting cognition in Black and Latinx mid-to late-life adults.

Glossary

DNAm=
DNA methylation;
HRS=
Health and Retirement Study;
PM=
proportion mediated;
SES=
socioeconomic status

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.

  • Previously published at medRxiv, https://doi.org/10.1101/2021.06.04.21258370.

  • Submitted and externally peer reviewed. The handling editor was Linda Hershey, MD, PhD, FAAN.

  • Received November 29, 2021.
  • Accepted in final form June 13, 2022.
  • © 2022 American Academy of Neurology
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