Phenome-wide association of APOE alleles in the All of Us Research ProgramResearch in context

Summary: Background: Apolipoprotein E (APOE) variation is associated with altered lipid metabolism, as well as cardiovascular and neurodegenerative disease. Prior studies are largely limited to European ancestry populations and differential risk by sex and ancestry has not been widely evaluated. Me...

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Main Authors: Ehsan Khajouei, Valentina Ghisays, Ignazio S. Piras, Kiana L. Martinez, Anthony T. Vicenti, Marcus Naymik, Preston Ngo, Tam C. Tran, Joshua C. Denny, Travis J. Wheeler, Matthew J. Huentelman, Eric M. Reiman, Jason H. Karnes
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Language:English
Published: Elsevier 2025-07-01
Series:EBioMedicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352396425002129
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author Ehsan Khajouei
Valentina Ghisays
Ignazio S. Piras
Kiana L. Martinez
Anthony T. Vicenti
Marcus Naymik
Preston Ngo
Tam C. Tran
Joshua C. Denny
Travis J. Wheeler
Matthew J. Huentelman
Eric M. Reiman
Jason H. Karnes
author_facet Ehsan Khajouei
Valentina Ghisays
Ignazio S. Piras
Kiana L. Martinez
Anthony T. Vicenti
Marcus Naymik
Preston Ngo
Tam C. Tran
Joshua C. Denny
Travis J. Wheeler
Matthew J. Huentelman
Eric M. Reiman
Jason H. Karnes
author_sort Ehsan Khajouei
collection DOAJ
description Summary: Background: Apolipoprotein E (APOE) variation is associated with altered lipid metabolism, as well as cardiovascular and neurodegenerative disease. Prior studies are largely limited to European ancestry populations and differential risk by sex and ancestry has not been widely evaluated. Methods: We utilised a phenome-wide association study (PheWAS) to explore APOE-associated phenotypes in the All of Us Research Program. We determined APOE alleles for 181,880 participants, representing seven ancestry groups. We tested association of APOE variants, ordered based on Alzheimer’s disease risk hierarchy (ε2/ε2 < ε2/ε3 < ε3/ε3 < ε2/ε4 < ε3/ε4 < ε4/ε4), with 2318 phenotypes. Bonferroni-adjusted analyses were performed overall, by ancestry, by sex, and with adjustment for social determinants of health (SDOH). Findings: In the overall cohort, PheWAS identified 17 significant associations, including increased odds of hyperlipidaemia (OR 1.15 [1.14–1.16] per APOE genotype group; P = 1.8 × 10−129), dementia, and Alzheimer’s disease (OR 1.55 [1.40–1.70]; P = 5 × 10−19), and reduced odds of fatty liver disease and chronic liver disease. ORs were similar after SDOH adjustment and by sex, except for an increased number of cardiovascular associations in males, and decreased odds of noninflammatory disorders of vulva and perineum in females. Significant heterogeneity was observed for hyperlipidaemia and mild cognitive impairment across ancestry. Unique associations by ancestry included transient retinal arterial occlusion in the European ancestry group, and first-degree atrioventricular block in the American Admixed/Latino ancestry group. Interpretation: We replicate extensive phenotypic associations with APOE alleles in a large, diverse cohort. We provide a comprehensive catalogue of APOE-associated phenotypes and evidence of unique phenotypic associations by sex and ancestry, as well as heterogeneity in effect size across ancestry. Funding: Funding is listed in the Acknowledgements section.
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spelling doaj-art-32eae6da113e4e1bab94c2dbc9da1cff2025-08-20T03:55:22ZengElsevierEBioMedicine2352-39642025-07-0111710576810.1016/j.ebiom.2025.105768Phenome-wide association of APOE alleles in the All of Us Research ProgramResearch in contextEhsan Khajouei0Valentina Ghisays1Ignazio S. Piras2Kiana L. Martinez3Anthony T. Vicenti4Marcus Naymik5Preston Ngo6Tam C. Tran7Joshua C. Denny8Travis J. Wheeler9Matthew J. Huentelman10Eric M. Reiman11Jason H. Karnes12Department of Pharmacy Practice and Science, R. Ken Coit College of Pharmacy, University of Arizona, Tucson, AZ, USABanner Alzheimer’s Institute, Phoenix, AZ, USANeurogenomics Division, Translational Genomics Research Institute, Phoenix, AZ, USADepartment of Pharmacy Practice and Science, R. Ken Coit College of Pharmacy, University of Arizona, Tucson, AZ, USADepartment of Pharmacy Practice and Science, R. Ken Coit College of Pharmacy, University of Arizona, Tucson, AZ, USANeurogenomics Division, Translational Genomics Research Institute, Phoenix, AZ, USADepartment of Pharmacy Practice and Science, R. Ken Coit College of Pharmacy, University of Arizona, Tucson, AZ, USANational Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USANational Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA; All of Us Research Program, National Institutes of Health, Bethesda, MD, USADepartment of Pharmacy Practice and Science, R. Ken Coit College of Pharmacy, University of Arizona, Tucson, AZ, USANeurogenomics Division, Translational Genomics Research Institute, Phoenix, AZ, USABanner Alzheimer’s Institute, Phoenix, AZ, USADepartment of Pharmacy Practice and Science, R. Ken Coit College of Pharmacy, University of Arizona, Tucson, AZ, USA; Department of Biomedical Informatics, Vanderbilt University Medical Center, Nashville, TN, USA; Corresponding author. R. Ken Coit College of Pharmacy, University of Arizona, 1295 N Martin AVE, Tucson, AZ 85721, USA.Summary: Background: Apolipoprotein E (APOE) variation is associated with altered lipid metabolism, as well as cardiovascular and neurodegenerative disease. Prior studies are largely limited to European ancestry populations and differential risk by sex and ancestry has not been widely evaluated. Methods: We utilised a phenome-wide association study (PheWAS) to explore APOE-associated phenotypes in the All of Us Research Program. We determined APOE alleles for 181,880 participants, representing seven ancestry groups. We tested association of APOE variants, ordered based on Alzheimer’s disease risk hierarchy (ε2/ε2 < ε2/ε3 < ε3/ε3 < ε2/ε4 < ε3/ε4 < ε4/ε4), with 2318 phenotypes. Bonferroni-adjusted analyses were performed overall, by ancestry, by sex, and with adjustment for social determinants of health (SDOH). Findings: In the overall cohort, PheWAS identified 17 significant associations, including increased odds of hyperlipidaemia (OR 1.15 [1.14–1.16] per APOE genotype group; P = 1.8 × 10−129), dementia, and Alzheimer’s disease (OR 1.55 [1.40–1.70]; P = 5 × 10−19), and reduced odds of fatty liver disease and chronic liver disease. ORs were similar after SDOH adjustment and by sex, except for an increased number of cardiovascular associations in males, and decreased odds of noninflammatory disorders of vulva and perineum in females. Significant heterogeneity was observed for hyperlipidaemia and mild cognitive impairment across ancestry. Unique associations by ancestry included transient retinal arterial occlusion in the European ancestry group, and first-degree atrioventricular block in the American Admixed/Latino ancestry group. Interpretation: We replicate extensive phenotypic associations with APOE alleles in a large, diverse cohort. We provide a comprehensive catalogue of APOE-associated phenotypes and evidence of unique phenotypic associations by sex and ancestry, as well as heterogeneity in effect size across ancestry. Funding: Funding is listed in the Acknowledgements section.http://www.sciencedirect.com/science/article/pii/S2352396425002129Apolipoprotein EPhenome-wide association studyHealth disparitiesAlzheimer’s diseaseHypercholesterolaemia
spellingShingle Ehsan Khajouei
Valentina Ghisays
Ignazio S. Piras
Kiana L. Martinez
Anthony T. Vicenti
Marcus Naymik
Preston Ngo
Tam C. Tran
Joshua C. Denny
Travis J. Wheeler
Matthew J. Huentelman
Eric M. Reiman
Jason H. Karnes
Phenome-wide association of APOE alleles in the All of Us Research ProgramResearch in context
EBioMedicine
Apolipoprotein E
Phenome-wide association study
Health disparities
Alzheimer’s disease
Hypercholesterolaemia
title Phenome-wide association of APOE alleles in the All of Us Research ProgramResearch in context
title_full Phenome-wide association of APOE alleles in the All of Us Research ProgramResearch in context
title_fullStr Phenome-wide association of APOE alleles in the All of Us Research ProgramResearch in context
title_full_unstemmed Phenome-wide association of APOE alleles in the All of Us Research ProgramResearch in context
title_short Phenome-wide association of APOE alleles in the All of Us Research ProgramResearch in context
title_sort phenome wide association of apoe alleles in the all of us research programresearch in context
topic Apolipoprotein E
Phenome-wide association study
Health disparities
Alzheimer’s disease
Hypercholesterolaemia
url http://www.sciencedirect.com/science/article/pii/S2352396425002129
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