Associations between Sleep and Physical Activity Behavior Clusters and Epigenetic Age Acceleration in Mexican Adolescents

Margaret Banker; Erica C. Jansen; Jaclyn M. Goodrich; Lindsey English; Dana C. Dolinoy; Peter X.K. Song; Jonathan A. Mitchell; Martha María Téllez-Rojo; Alejandra Cantoral; Karen E. Peterson

doi:10.1249/MSS.0000000000003498

Associations between Sleep and Physical Activity Behavior Clusters and Epigenetic Age Acceleration in Mexican Adolescents

Margaret Banker, Erica C. Jansen^*, Jaclyn M. Goodrich, Lindsey English, Dana C. Dolinoy, Peter X.K. Song, Jonathan A. Mitchell, Martha María Téllez-Rojo, Alejandra Cantoral, Karen E. Peterson

^*Corresponding author for this work

Preventive Medicine

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

1 Scopus citations

Abstract

Introduction Epigenetic aging, a marker of biological aging measured by DNA methylation, may be affected by behaviors, including sleep and physical activity. However, investigations of physical activity and sleep with epigenetic aging among pediatric populations are scant and have not accounted for correlated behaviors. Methods The study population included 472 Mexico City adolescents (52% female). Blood collection and 7-d wrist actigraphy (Actigraph GTX-BT) occurred during a follow-up visit when participants were 14.5 (2.09) yr. Leukocyte DNA methylation was measured with the Infinium MethylationEPIC array after bisulfite conversion, and nine epigenetic clocks were calculated. Sleep versus wake time was identified through a pruned dynamic programing algorithm, and physical activity was processed with Chandler cutoffs. Kmeans clustering was used to select actigraphy-assessed physical activity and sleep behavior clusters. Linear regression analyses were used to evaluate adjusted associations between the clusters and epigenetic aging. Results There were three unique clusters: "Short sleep/high sedentary behavior,""Adequate sleep duration and late sleep timing/low moderate or vigorous physical activity (MVPA),"and "Adequate sleep duration/high MVPA."Compared with the "Adequate duration/high MVPA,"adolescents with "Adequate duration and late sleep timing/low MVPA"had more accelerated aging for the GrimAge clock (β = 0.63; 95% confidence interval, 0.07-1.19). In pubertal-stratified analyses, more mature adolescents in the "Adequate sleep duration and late sleep timing/low MVPA group"had accelerated epigenetic aging. In contrast, females in the "Short sleep/high sedentary"group had decelerated epigenetic aging for the Wu pediatric clock. Conclusions Associations between behavior clusters and epigenetic aging varied by pubertal status and sex. Contrary results in the Wu clock suggest the need for future research on pediatric-specific clocks.

Original language	English (US)
Pages (from-to)	2173-2183
Number of pages	11
Journal	Medicine and science in sports and exercise
Volume	56
Issue number	11
DOIs	https://doi.org/10.1249/MSS.0000000000003498
State	Published - Nov 1 2024

Funding

This work was supported by US Environmental Protection Agency grants RD834800 and RD83543601 and National Institute for Environmental Health Sciences (NIEHS) grants P01 ES02284401, P30 ES017885 (Michigan Lifestage Environmental Exposures and Disease (M-LEEaD) NIEHS Core Center), R24 ES028502and R35 ES031686, and National Institute for Diabetes and Digestive and Kidney Disease P30 DK089503 (Michigan Nutrition Obesity Research Center). This study was also supported by National Heart, Lung, Blood Institute grant K01 HL151673. The authors of this work declare that the results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. The results of the present study do not constitute endorsement by the American College of Sports Medicine. This work was supported by US Environmental Protection Agency grants RD834800 and RD83543601 and National Institute for Environmental Health Sciences (NIEHS) grants P01 ES02284401, P30 ES017885 (Michigan Lifestage Environmental Exposures and Disease (M-LEEaD) NIEHS Core Center), R24 ES028502and R35 ES031686, and National Institute for Diabetes and Digestive and Kidney Disease P30 DK089503 (Michigan Nutrition Obesity Research Center). This study was also supported by National Heart, Lung, Blood Institute grant K01 HL151673. The authors of this work declare that the results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. The results of the present study do not constitute endorsement by the American College of Sports Medicine. Code from this analysis can be found here: https://github.com/mbanker719/EpiAge/tree/main . Data (certain epigenetic and demographic data) from the ELEMENT study are available through the National Institutes of Health Human Health Exposure Analysis Resource data repository (doi: 10.36043/1431_392 , 10.36043/1431_327 , 10.36043/1431_393 ). Other data can be requested via the ELEMENT study\u2019s online data-sharing platform: https://sph.umich.edu/cehc/element/index.html .

Keywords

EPIGENETIC CLOCKS
KMEANS CLUSTERING
SEX DIFFERENCES

ASJC Scopus subject areas

Orthopedics and Sports Medicine
Physical Therapy, Sports Therapy and Rehabilitation

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10.1249/MSS.0000000000003498

Cite this

Banker, M., Jansen, E. C., Goodrich, J. M., English, L., Dolinoy, D. C., Song, P. X. K., Mitchell, J. A., Téllez-Rojo, M. M., Cantoral, A., & Peterson, K. E. (2024). Associations between Sleep and Physical Activity Behavior Clusters and Epigenetic Age Acceleration in Mexican Adolescents. Medicine and science in sports and exercise, 56(11), 2173-2183. https://doi.org/10.1249/MSS.0000000000003498

@article{e012bd8bb0c9428a9ec23beddbedcb02,

title = "Associations between Sleep and Physical Activity Behavior Clusters and Epigenetic Age Acceleration in Mexican Adolescents",

abstract = "Introduction Epigenetic aging, a marker of biological aging measured by DNA methylation, may be affected by behaviors, including sleep and physical activity. However, investigations of physical activity and sleep with epigenetic aging among pediatric populations are scant and have not accounted for correlated behaviors. Methods The study population included 472 Mexico City adolescents (52% female). Blood collection and 7-d wrist actigraphy (Actigraph GTX-BT) occurred during a follow-up visit when participants were 14.5 (2.09) yr. Leukocyte DNA methylation was measured with the Infinium MethylationEPIC array after bisulfite conversion, and nine epigenetic clocks were calculated. Sleep versus wake time was identified through a pruned dynamic programing algorithm, and physical activity was processed with Chandler cutoffs. Kmeans clustering was used to select actigraphy-assessed physical activity and sleep behavior clusters. Linear regression analyses were used to evaluate adjusted associations between the clusters and epigenetic aging. Results There were three unique clusters: {"}Short sleep/high sedentary behavior,{"}{"}Adequate sleep duration and late sleep timing/low moderate or vigorous physical activity (MVPA),{"}and {"}Adequate sleep duration/high MVPA.{"}Compared with the {"}Adequate duration/high MVPA,{"}adolescents with {"}Adequate duration and late sleep timing/low MVPA{"}had more accelerated aging for the GrimAge clock (β = 0.63; 95% confidence interval, 0.07-1.19). In pubertal-stratified analyses, more mature adolescents in the {"}Adequate sleep duration and late sleep timing/low MVPA group{"}had accelerated epigenetic aging. In contrast, females in the {"}Short sleep/high sedentary{"}group had decelerated epigenetic aging for the Wu pediatric clock. Conclusions Associations between behavior clusters and epigenetic aging varied by pubertal status and sex. Contrary results in the Wu clock suggest the need for future research on pediatric-specific clocks.",

keywords = "EPIGENETIC CLOCKS, KMEANS CLUSTERING, SEX DIFFERENCES",

author = "Margaret Banker and Jansen, {Erica C.} and Goodrich, {Jaclyn M.} and Lindsey English and Dolinoy, {Dana C.} and Song, {Peter X.K.} and Mitchell, {Jonathan A.} and T{\'e}llez-Rojo, {Martha Mar{\'i}a} and Alejandra Cantoral and Peterson, {Karen E.}",

note = "Publisher Copyright: {\textcopyright} 2024 by the American College of Sports Medicine.",

year = "2024",

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doi = "10.1249/MSS.0000000000003498",

language = "English (US)",

volume = "56",

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Banker, M, Jansen, EC, Goodrich, JM, English, L, Dolinoy, DC, Song, PXK, Mitchell, JA, Téllez-Rojo, MM, Cantoral, A & Peterson, KE 2024, 'Associations between Sleep and Physical Activity Behavior Clusters and Epigenetic Age Acceleration in Mexican Adolescents', Medicine and science in sports and exercise, vol. 56, no. 11, pp. 2173-2183. https://doi.org/10.1249/MSS.0000000000003498

TY - JOUR

T1 - Associations between Sleep and Physical Activity Behavior Clusters and Epigenetic Age Acceleration in Mexican Adolescents

AU - Banker, Margaret

AU - Jansen, Erica C.

AU - Goodrich, Jaclyn M.

AU - English, Lindsey

AU - Dolinoy, Dana C.

AU - Song, Peter X.K.

AU - Mitchell, Jonathan A.

AU - Téllez-Rojo, Martha María

AU - Cantoral, Alejandra

AU - Peterson, Karen E.

PY - 2024/11/1

Y1 - 2024/11/1

N2 - Introduction Epigenetic aging, a marker of biological aging measured by DNA methylation, may be affected by behaviors, including sleep and physical activity. However, investigations of physical activity and sleep with epigenetic aging among pediatric populations are scant and have not accounted for correlated behaviors. Methods The study population included 472 Mexico City adolescents (52% female). Blood collection and 7-d wrist actigraphy (Actigraph GTX-BT) occurred during a follow-up visit when participants were 14.5 (2.09) yr. Leukocyte DNA methylation was measured with the Infinium MethylationEPIC array after bisulfite conversion, and nine epigenetic clocks were calculated. Sleep versus wake time was identified through a pruned dynamic programing algorithm, and physical activity was processed with Chandler cutoffs. Kmeans clustering was used to select actigraphy-assessed physical activity and sleep behavior clusters. Linear regression analyses were used to evaluate adjusted associations between the clusters and epigenetic aging. Results There were three unique clusters: "Short sleep/high sedentary behavior,""Adequate sleep duration and late sleep timing/low moderate or vigorous physical activity (MVPA),"and "Adequate sleep duration/high MVPA."Compared with the "Adequate duration/high MVPA,"adolescents with "Adequate duration and late sleep timing/low MVPA"had more accelerated aging for the GrimAge clock (β = 0.63; 95% confidence interval, 0.07-1.19). In pubertal-stratified analyses, more mature adolescents in the "Adequate sleep duration and late sleep timing/low MVPA group"had accelerated epigenetic aging. In contrast, females in the "Short sleep/high sedentary"group had decelerated epigenetic aging for the Wu pediatric clock. Conclusions Associations between behavior clusters and epigenetic aging varied by pubertal status and sex. Contrary results in the Wu clock suggest the need for future research on pediatric-specific clocks.

AB - Introduction Epigenetic aging, a marker of biological aging measured by DNA methylation, may be affected by behaviors, including sleep and physical activity. However, investigations of physical activity and sleep with epigenetic aging among pediatric populations are scant and have not accounted for correlated behaviors. Methods The study population included 472 Mexico City adolescents (52% female). Blood collection and 7-d wrist actigraphy (Actigraph GTX-BT) occurred during a follow-up visit when participants were 14.5 (2.09) yr. Leukocyte DNA methylation was measured with the Infinium MethylationEPIC array after bisulfite conversion, and nine epigenetic clocks were calculated. Sleep versus wake time was identified through a pruned dynamic programing algorithm, and physical activity was processed with Chandler cutoffs. Kmeans clustering was used to select actigraphy-assessed physical activity and sleep behavior clusters. Linear regression analyses were used to evaluate adjusted associations between the clusters and epigenetic aging. Results There were three unique clusters: "Short sleep/high sedentary behavior,""Adequate sleep duration and late sleep timing/low moderate or vigorous physical activity (MVPA),"and "Adequate sleep duration/high MVPA."Compared with the "Adequate duration/high MVPA,"adolescents with "Adequate duration and late sleep timing/low MVPA"had more accelerated aging for the GrimAge clock (β = 0.63; 95% confidence interval, 0.07-1.19). In pubertal-stratified analyses, more mature adolescents in the "Adequate sleep duration and late sleep timing/low MVPA group"had accelerated epigenetic aging. In contrast, females in the "Short sleep/high sedentary"group had decelerated epigenetic aging for the Wu pediatric clock. Conclusions Associations between behavior clusters and epigenetic aging varied by pubertal status and sex. Contrary results in the Wu clock suggest the need for future research on pediatric-specific clocks.

KW - EPIGENETIC CLOCKS

KW - KMEANS CLUSTERING

KW - SEX DIFFERENCES

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JF - Medicine and science in sports and exercise

IS - 11

ER -

Associations between Sleep and Physical Activity Behavior Clusters and Epigenetic Age Acceleration in Mexican Adolescents

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