Epigenetic age acceleration in offspring linked to paternal smoking initiation and overweight in puberty: Evidence from a two-generation study

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Background Father’s adolescent smoking and overweight contribute to shape future offsprings’ respiratory health. We examined whether biological aging in offspring was associated with parents’ smoking or overweight in puberty. Methods We estimated Horvath, GrimAge, PhenoAge and DunedinPACE epigenetic clocks from blood DNA methylation, in 892 RHINESSA cohort participants (mean age 27 years) with data on parental smoking and body shape in the RHINE/ECRHS surveys. Linear regressions assessed associations of parental smoking initiation ≤15 versus >15 years, and overweight body shapes in childhood/puberty versus age 30, with offspring epigenetic age acceleration, adjusting for offspring sex, age, and parental childhood socioeconomic status. Sensitivity analyses accounted for offspring smoking and BMI. Results Daughters of fathers who started smoking ≤15 years showed accelerated PCHorvath (β coefficient=1.53; 95% confidence interval=0.2-2.9) and PCGrimAge (1.21; 0.3-2.1), and suggestive trends in similar direction for DunedinPACE and PCPhenoAge. No corresponding associations were observed in sons. Father’s overweight in childhood/ puberty was associated with higher PCHorvath and PCPhenoAge acceleration in daughters, and higher acceleration across all clocks in sons. In analyses of sons and daughters together, paternal overweight in childhood/ puberty was associated with higher PCHorvath (2.25; 1.2-3.3), DunedinPACE (0.07; 0.01-0.1) and PCPhenoAge (3.11; 1.9- 4.4). These findings remained consistent in sensitivity analyses. Mothers’s puberty exposures showed no consistent associations with offsprings’ age acceleration. Conclusions We find that smoking as well as overweight around puberty in future fathers associate with higher epigenetic age acceleration in their offspring, suggesting father’s puberty might be a susceptible period regarding offsprings’ biological aging.

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