Accelerated biological aging six decades after prenatal famine exposure

Mengling Cheng; Dalton Conley; Tom Kuipers; Chihua Li; Calen P. Ryan; M. Jazmin Taeubert; Shuang Wang; Tian Wang; Jiayi Zhou; Lauren L. Schmitz; Elmar W. Tobi; Bas Heijmans; L. H. Lumey; Daniel W. Belsky

doi:10.1073/pnas.2319179121

Accelerated biological aging six decades after prenatal famine exposure

Mengling Cheng, Dalton Conley, Tom Kuipers, Chihua Li, Calen P. Ryan, M. Jazmin Taeubert, Shuang Wang, Tian Wang, Jiayi Zhou, Lauren L. Schmitz, Elmar W. Tobi, Bas Heijmans, L. H. Lumey, Daniel W. Belsky

Sociology

Research output: Contribution to journal › Article › peer-review

2 Scopus citations

Abstract

To test the hypothesis that early-life adversity accelerates the pace of biological aging, we analyzed data from the Dutch Hunger Winter Families Study (DHWFS, N = 951). DHWFS is a natural-experiment birth-cohort study of survivors of in-utero exposure to famine conditions caused by the German occupation of the Western Netherlands in Winter 1944 to 1945, matched controls, and their siblings. We conducted DNA methylation analysis of blood samples collected when the survivors were aged 58 to quantify biological aging using the DunedinPACE, GrimAge, and PhenoAge epigenetic clocks. Famine survivors had faster DunedinPACE, as compared with controls. This effect was strongest among women. Results were similar for GrimAge, although effect-sizes were smaller. We observed no differences in PhenoAge between survivors and controls. Famine effects were not accounted for by blood-cell composition and were similar for individuals exposed early and later in gestation. Findings suggest in-utero undernutrition may accelerate biological aging in later life.

Original language	English (US)
Article number	e2319179121
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	121
Issue number	24
DOIs	https://doi.org/10.1073/pnas.2319179121
State	Published - Jun 11 2024

All Science Journal Classification (ASJC) codes

General

Keywords

Dutch famine
biological aging
epigenetic clock
fetal origins
natural experiment

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10.1073/pnas.2319179121

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Cheng, M., Conley, D., Kuipers, T., Li, C., Ryan, C. P., Taeubert, M. J., Wang, S., Wang, T., Zhou, J., Schmitz, L. L., Tobi, E. W., Heijmans, B., Lumey, L. H., & Belsky, D. W. (2024). Accelerated biological aging six decades after prenatal famine exposure. Proceedings of the National Academy of Sciences of the United States of America, 121(24), Article e2319179121. https://doi.org/10.1073/pnas.2319179121

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title = "Accelerated biological aging six decades after prenatal famine exposure",

abstract = "To test the hypothesis that early-life adversity accelerates the pace of biological aging, we analyzed data from the Dutch Hunger Winter Families Study (DHWFS, N = 951). DHWFS is a natural-experiment birth-cohort study of survivors of in-utero exposure to famine conditions caused by the German occupation of the Western Netherlands in Winter 1944 to 1945, matched controls, and their siblings. We conducted DNA methylation analysis of blood samples collected when the survivors were aged 58 to quantify biological aging using the DunedinPACE, GrimAge, and PhenoAge epigenetic clocks. Famine survivors had faster DunedinPACE, as compared with controls. This effect was strongest among women. Results were similar for GrimAge, although effect-sizes were smaller. We observed no differences in PhenoAge between survivors and controls. Famine effects were not accounted for by blood-cell composition and were similar for individuals exposed early and later in gestation. Findings suggest in-utero undernutrition may accelerate biological aging in later life.",

keywords = "Dutch famine, biological aging, epigenetic clock, fetal origins, natural experiment",

author = "Mengling Cheng and Dalton Conley and Tom Kuipers and Chihua Li and Ryan, {Calen P.} and Taeubert, {M. Jazmin} and Shuang Wang and Tian Wang and Jiayi Zhou and Schmitz, {Lauren L.} and Tobi, {Elmar W.} and Bas Heijmans and Lumey, {L. H.} and Belsky, {Daniel W.}",

note = "Publisher Copyright: {\textcopyright} 2024 the Author(s). Published by PNAS.",

year = "2024",

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doi = "10.1073/pnas.2319179121",

language = "English (US)",

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Cheng, M, Conley, D, Kuipers, T, Li, C, Ryan, CP, Taeubert, MJ, Wang, S, Wang, T, Zhou, J, Schmitz, LL, Tobi, EW, Heijmans, B, Lumey, LH & Belsky, DW 2024, 'Accelerated biological aging six decades after prenatal famine exposure', Proceedings of the National Academy of Sciences of the United States of America, vol. 121, no. 24, e2319179121. https://doi.org/10.1073/pnas.2319179121

TY - JOUR

T1 - Accelerated biological aging six decades after prenatal famine exposure

AU - Cheng, Mengling

AU - Conley, Dalton

AU - Kuipers, Tom

AU - Li, Chihua

AU - Ryan, Calen P.

AU - Taeubert, M. Jazmin

AU - Wang, Shuang

AU - Wang, Tian

AU - Zhou, Jiayi

AU - Schmitz, Lauren L.

AU - Tobi, Elmar W.

AU - Heijmans, Bas

AU - Lumey, L. H.

AU - Belsky, Daniel W.

PY - 2024/6/11

Y1 - 2024/6/11

N2 - To test the hypothesis that early-life adversity accelerates the pace of biological aging, we analyzed data from the Dutch Hunger Winter Families Study (DHWFS, N = 951). DHWFS is a natural-experiment birth-cohort study of survivors of in-utero exposure to famine conditions caused by the German occupation of the Western Netherlands in Winter 1944 to 1945, matched controls, and their siblings. We conducted DNA methylation analysis of blood samples collected when the survivors were aged 58 to quantify biological aging using the DunedinPACE, GrimAge, and PhenoAge epigenetic clocks. Famine survivors had faster DunedinPACE, as compared with controls. This effect was strongest among women. Results were similar for GrimAge, although effect-sizes were smaller. We observed no differences in PhenoAge between survivors and controls. Famine effects were not accounted for by blood-cell composition and were similar for individuals exposed early and later in gestation. Findings suggest in-utero undernutrition may accelerate biological aging in later life.

AB - To test the hypothesis that early-life adversity accelerates the pace of biological aging, we analyzed data from the Dutch Hunger Winter Families Study (DHWFS, N = 951). DHWFS is a natural-experiment birth-cohort study of survivors of in-utero exposure to famine conditions caused by the German occupation of the Western Netherlands in Winter 1944 to 1945, matched controls, and their siblings. We conducted DNA methylation analysis of blood samples collected when the survivors were aged 58 to quantify biological aging using the DunedinPACE, GrimAge, and PhenoAge epigenetic clocks. Famine survivors had faster DunedinPACE, as compared with controls. This effect was strongest among women. Results were similar for GrimAge, although effect-sizes were smaller. We observed no differences in PhenoAge between survivors and controls. Famine effects were not accounted for by blood-cell composition and were similar for individuals exposed early and later in gestation. Findings suggest in-utero undernutrition may accelerate biological aging in later life.

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KW - biological aging

KW - epigenetic clock

KW - fetal origins

KW - natural experiment

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IS - 24

M1 - e2319179121

ER -

Accelerated biological aging six decades after prenatal famine exposure

Abstract

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