Associations of socioeconomic disparities with buccal DNA-methylation measures of biological aging

Abstract Background Individuals who are socioeconomically disadvantaged are at increased risk for aging-related diseases and perform less well on tests of cognitive function. The weathering hypothesis proposes that these disparities in physical and cognitive health arise from an acceleration of biol...

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Main Authors: L. Raffington, T. Schwaba, M. Aikins, D. Richter, G. G. Wagner, K. P. Harden, D. W. Belsky, E. M. Tucker-Drob
Format: Article
Language:English
Published: BMC 2023-04-01
Series:Clinical Epigenetics
Subjects:
Online Access:https://doi.org/10.1186/s13148-023-01489-7
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author L. Raffington
T. Schwaba
M. Aikins
D. Richter
G. G. Wagner
K. P. Harden
D. W. Belsky
E. M. Tucker-Drob
author_facet L. Raffington
T. Schwaba
M. Aikins
D. Richter
G. G. Wagner
K. P. Harden
D. W. Belsky
E. M. Tucker-Drob
author_sort L. Raffington
collection DOAJ
description Abstract Background Individuals who are socioeconomically disadvantaged are at increased risk for aging-related diseases and perform less well on tests of cognitive function. The weathering hypothesis proposes that these disparities in physical and cognitive health arise from an acceleration of biological processes of aging. Theories of how life adversity is biologically embedded identify epigenetic alterations, including DNA methylation (DNAm), as a mechanistic interface between the environment and health. Consistent with the weathering hypothesis and theories of biological embedding, recently developed DNAm algorithms have revealed profiles reflective of more advanced aging and lower cognitive function among socioeconomically-at-risk groups. These DNAm algorithms were developed using blood-DNA, but social and behavioral science research commonly collect saliva or cheek-swab DNA. This discrepancy is a potential barrier to research to elucidate mechanisms through which socioeconomic disadvantage affects aging and cognition. We therefore tested if social gradients observed in blood DNAm measures could be reproduced using buccal-cell DNA obtained from cheek swabs. Results We analyzed three DNAm measures of biological aging and one DNAm measure of cognitive performance, all of which showed socioeconomic gradients in previous studies: the PhenoAge and GrimAge DNAm clocks, DunedinPACE, and Epigenetic-g. We first computed blood-buccal cross-tissue correlations in n = 21 adults (GEO111165). Cross-tissue correlations were low-to-moderate (r = .25 to r = .48). We next conducted analyses of socioeconomic gradients using buccal DNAm data from SOEP-G (n = 1128, 57% female; age mean = 42 yrs, SD = 21.56, range 0–72). Associations of socioeconomic status with DNAm measures of aging were in the expected direction, but were smaller as compared to reports from blood DNAm datasets (r = − .08 to r = − .13). Conclusions Our findings are consistent with the hypothesis that socioeconomic disadvantage is associated with DNAm indicators of worse physical health. However, relatively low cross-tissue correlations and attenuated effect sizes for socioeconomic gradients in buccal DNAm compared with reports from analysis of blood DNAm suggest that in order to take full advantage of buccal DNA samples, DNAm algorithms customized to buccal DNAm are needed.
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spelling doaj.art-110060a6ea914109a78f228df881bd682023-04-30T11:19:16ZengBMCClinical Epigenetics1868-70832023-04-011511910.1186/s13148-023-01489-7Associations of socioeconomic disparities with buccal DNA-methylation measures of biological agingL. Raffington0T. Schwaba1M. Aikins2D. Richter3G. G. Wagner4K. P. Harden5D. W. Belsky6E. M. Tucker-Drob7Max Planck Research Group Biosocial – Biology, Social Disparities, and Development, Max Planck Institute for Human DevelopmentDepartment of Psychology, The University of Texas at AustinMax Planck Research Group Biosocial – Biology, Social Disparities, and Development, Max Planck Institute for Human DevelopmentSHARE Berlin InstituteMax Planck Institute for Human DevelopmentDepartment of Psychology, The University of Texas at AustinDepartment of Epidemiology, Columbia University Mailman School of Public HealthDepartment of Psychology, The University of Texas at AustinAbstract Background Individuals who are socioeconomically disadvantaged are at increased risk for aging-related diseases and perform less well on tests of cognitive function. The weathering hypothesis proposes that these disparities in physical and cognitive health arise from an acceleration of biological processes of aging. Theories of how life adversity is biologically embedded identify epigenetic alterations, including DNA methylation (DNAm), as a mechanistic interface between the environment and health. Consistent with the weathering hypothesis and theories of biological embedding, recently developed DNAm algorithms have revealed profiles reflective of more advanced aging and lower cognitive function among socioeconomically-at-risk groups. These DNAm algorithms were developed using blood-DNA, but social and behavioral science research commonly collect saliva or cheek-swab DNA. This discrepancy is a potential barrier to research to elucidate mechanisms through which socioeconomic disadvantage affects aging and cognition. We therefore tested if social gradients observed in blood DNAm measures could be reproduced using buccal-cell DNA obtained from cheek swabs. Results We analyzed three DNAm measures of biological aging and one DNAm measure of cognitive performance, all of which showed socioeconomic gradients in previous studies: the PhenoAge and GrimAge DNAm clocks, DunedinPACE, and Epigenetic-g. We first computed blood-buccal cross-tissue correlations in n = 21 adults (GEO111165). Cross-tissue correlations were low-to-moderate (r = .25 to r = .48). We next conducted analyses of socioeconomic gradients using buccal DNAm data from SOEP-G (n = 1128, 57% female; age mean = 42 yrs, SD = 21.56, range 0–72). Associations of socioeconomic status with DNAm measures of aging were in the expected direction, but were smaller as compared to reports from blood DNAm datasets (r = − .08 to r = − .13). Conclusions Our findings are consistent with the hypothesis that socioeconomic disadvantage is associated with DNAm indicators of worse physical health. However, relatively low cross-tissue correlations and attenuated effect sizes for socioeconomic gradients in buccal DNAm compared with reports from analysis of blood DNAm suggest that in order to take full advantage of buccal DNA samples, DNAm algorithms customized to buccal DNAm are needed.https://doi.org/10.1186/s13148-023-01489-7AgingDNA methylationBiological agingPace of agingCognitionBiomarker
spellingShingle L. Raffington
T. Schwaba
M. Aikins
D. Richter
G. G. Wagner
K. P. Harden
D. W. Belsky
E. M. Tucker-Drob
Associations of socioeconomic disparities with buccal DNA-methylation measures of biological aging
Clinical Epigenetics
Aging
DNA methylation
Biological aging
Pace of aging
Cognition
Biomarker
title Associations of socioeconomic disparities with buccal DNA-methylation measures of biological aging
title_full Associations of socioeconomic disparities with buccal DNA-methylation measures of biological aging
title_fullStr Associations of socioeconomic disparities with buccal DNA-methylation measures of biological aging
title_full_unstemmed Associations of socioeconomic disparities with buccal DNA-methylation measures of biological aging
title_short Associations of socioeconomic disparities with buccal DNA-methylation measures of biological aging
title_sort associations of socioeconomic disparities with buccal dna methylation measures of biological aging
topic Aging
DNA methylation
Biological aging
Pace of aging
Cognition
Biomarker
url https://doi.org/10.1186/s13148-023-01489-7
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