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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.

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Information & Authors

Information

Published In

Neurology®
Volume 99Number 19November 8, 2022
Pages: e2114-e2124
PubMed: 36038275

Publication History

Received: November 29, 2021
Accepted: June 13, 2022
Published online: August 29, 2022
Published in print: November 8, 2022

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Disclosure

The authors report no relevant disclosures. Go to Neurology.org/N for full disclosures.

Study Funding

The HRS (Health and Retirement Study) is sponsored by the National Institute on Aging (grant number NIA U01AG009740) and is conducted by the University of Michigan. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. Dr. Avila-Rieger is in part supported by P30AG059303.

Authors

Affiliations & Disclosures

Justina Avila-Rieger, PhD
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.
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
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1.
NONE
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NONE
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Indira C. Turney, PhD
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.
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:
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Jet M.J. Vonk, PhD
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.
Disclosure
Scientific Advisory Boards:
1.
None
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
None
Editorial Boards:
1.
(1) Guest Editor Special Issue Frontiers in Psychology Jan 2021-present (2) Review Editor Frontiers in Neurology: Dementia and Neurodegenerative Diseases Jul 2020-present (3) Associate Editor Journal of Alzheimer's Disease Jan 2020-Dec 2020 (4) Editorial board member Journal of Speech Language Hearing Research Jan 2019-Jan 2021
Patents:
1.
NONE
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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.
Research grants:- NIH NIA K99/R00 Award (1K99AG066934-01) ($1,008,539) "Preclinical markers of Alzheimer's disease using psycholinguistic semantic measures" 2020 - NWO ZonMw Veni Grant (project 09150161810017) (e250,000) "Towards a cognitive marker of preclinical Alzheimer's disease: A psycholinguistic approach of semantic decline" 2019
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
Alzheimer Nederland Fellowship (WE.15-2018-05) (e65,000) - - "Early detection of semantic loss in preclinical Alzheimer's disease" 2018
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1.
NONE
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1.
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Precious Esie, MPH
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.
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
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1.
NONE
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1.
NONE
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Dominika Seblova, PhD
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.
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.
(1) NIH/NIA, 1P30AG066462, Investigator, 05/01/2021-04/30/2023 (2) Ministry of Health of the Czech Republic, NU22J-09-00064, Principal Investigator, 05/01/2022-12/31/2025
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
(1) Alzheimer's Association, AARF-21-848200, 02/01/2022-01/31/2025
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NONE
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Vanessa R. Weir, BA
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.
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.
(1) Columbia University - NIA T35 Grant
Research Support, Foundations and Societies:
1.
None
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
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1.
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1.
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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.
Disclosure
Scientific Advisory Boards:
1.
BroadRiver Asset Management SAB
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
None
Editorial Boards:
1.
Journals of Gerontology Series A, Editorial Board Member, 2017-present
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.
Daniel Belsky is named as an inventor on the Pace of Aging (mPoA) Measure licensed by Duke University to TruDiagnostic, an Epigenetics/Health and Aging company.
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NIA, R01AG066887, MPI, 5/15/2020-present NIA, R01AG061378, PI, 7/1/2019-present NIA, R01AG057800, Co-I, 9/15/2017-present NIA, R01AG054070, Co-I, 9/1/2021-present NIA, R01AG058683, Co-I, 9/30/2018-present NIA, R01AG071717, Consultant, 9/01/2021-present CIFAR, CF-0249 - CP22-034, PI, 1/5/2022-present CIFAR, CU19-2322, Fellow, 7/1/2019-present
Research Support, Academic Entities:
1.
Columbia University Population Research Center University of Oslo PROMENTA Center Universidad Mayor, SocioMed Research Nucleus
Research Support, Foundations and Societies:
1.
Russel Sage Foundation Jacobs Foundation
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NONE
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Legal Proceedings:
1.
NONE
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.
Disclosure
Scientific Advisory Boards:
1.
Reimbursement of AAIC registration and ISTAART membership associated with serving on the Alzheimer's Association International Grants Program Review Group
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.
National Academy of Sciences, 2018 - present University of Mississippi, 2019 - present
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. NIA RF1/R01AG054070, MPI, 09/01/2016-08/31/2026 2. NIA RF1AG056164, PI, 09/15/2016-06/30/2021 3. NIA RF1AG058067, MPI, 09/01/2018 – 03/31/2023 4. NIA R01AG049810, Co-investigator, 03/15/2016- 02/28/2021 5. NIA RF1AG054023, Co-investigator, 09/01/2016- 06/30/2021 6. NIA P30AG059303, MPI, 04/01/2018 - 03/31/2023 7. NIA U01AG009740, Subcontract PI; co-investigator, 01/01/2018 - 12/31/2023 8. NIA U01AG058499, Subcontract PI; co-investigator, 01/01/2018 - 12/31/2023 9.NINDS U01NS041588, MPI, 12/01/2017-11/30/2022 10. NIA T35AG044303, MPI, 05/01/2018-04/30/2023 11. NIA U2CAG057441, Subcontract PI; co-investigator, 09/01/2017-04/30/2022 12. NIA R01AG058683, Subcontract PI; co-investigator, 09/01/2018-5/31/2023 13. NIA R01AG058719, Subcontract PI; co-investigator, 05/15/2019-02/29/2024 14. NIA R01AG051142, Subcontract PI; co-investigator, 09/01/2019 - 07/31/2024 15. NINDS R01NS102715, Co-investigator, 07/01/2017- 06/30/2022 16. NIA R01AG066134, Co-investigator, 09/15/2019 – 11/30/2024 17. NIA R01AG058767, Co-investigator, 09/01/2018- 5/31/2023 18. NIA R01AG071024, Co-investigator, 04/01/2021- 03/31/2026 19. NIA R01AG074359, Co-investigator, 07/01/2021 – 06/30/2026 20. NIA K99 AG066932, Mentor, 05/01/2020-04/30/2022 21. NIA K99 AG066934, Mentor, 05/01/2020-04/30/2022 22.NIA K99 AG065506, Mentor, 09/1/2019- 08/31/2024
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

Notes

Correspondence Dr. Manly [email protected]
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.

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