Body mass index is negatively associated with telomere length: a collaborative cross-sectional meta-analysis of 87 observational studies

Marij Gielen; Geja J. Hageman; Evangelia E. Antoniou; Katarina Nordfjall; Massimo Mangino; Muthuswamy Balasubramanyam; Tim de Meyer; Audrey E. Hendricks; Erik J. Giltay; Steven C. Hunt; Jennifer A. Nettleton; Klelia D. Salpea; Vanessa A. Diaz; Ramin Farzaneh-Far; Gil Atzmon; Sarah E. Harris; Lifang Hou; David Gilley; Iiris Hovatta; Jeremy D. Kark; Hisham Nassar; David J. Kurz; Karen A. Mather; Peter Willeit; Yun-Ling Zheng; Sofia Pavanello; Ellen W. Demerath; Line Rode; Daniel Bunout; Andrew Steptoe; Lisa Boardman; Amelia Marti; Belinda Needham; Wei Zheng; Rosalind Ramsey-Goldman; Andrew J. Pellatt; Jaakko Kaprio; Jonathan N. Hofmann; Christian Gieger; Giuseppe Paolisso; Jacob B. H. Hjelmborg; Lisa Mirabello; Teresa Seeman; Jason Wong; Pim van der Harst; Linda Broer; Florian Kronenberg; Barbara Kollerits; Timo Strandberg; Dan TA Eisenberg; Catherine Duggan; Josine E. Verhoeven; Roxanne Schaakxs; Raffaela Zannolli; Rosana MR dos Reis; Fadi J. Charchar; Maciej Tomaszewski; U. Mons; Ilja Demuth; Andrea Elena  Iglesias Molli; Guo Cheng; Dmytro Krasnienkov; Bianca D'Antono; Marek Kasielski; Barry J McDonnell; Richard P. Ebstein; Kristina Sundquist; Maurice P. Zeegers; TELOMAAS Group

doi:10.1093/ajcn/nqy107

Body mass index is negatively associated with telomere length: a collaborative cross-sectional meta-analysis of 87 observational studies

Marij Gielen^*, Geja J. Hageman, Evangelia E. Antoniou, Katarina Nordfjall, Massimo Mangino, Muthuswamy Balasubramanyam, Tim de Meyer, Audrey E. Hendricks, Erik J. Giltay, Steven C. Hunt, Jennifer A. Nettleton, Klelia D. Salpea, Vanessa A. Diaz, Ramin Farzaneh-Far, Gil Atzmon, Sarah E. Harris, Lifang Hou, David Gilley, Iiris Hovatta, Jeremy D. KarkHisham Nassar, David J. Kurz, Karen A. Mather, Peter Willeit, Yun-Ling Zheng, Sofia Pavanello, Ellen W. Demerath, Line Rode, Daniel Bunout, Andrew Steptoe, Lisa Boardman, Amelia Marti, Belinda Needham, Wei Zheng, Rosalind Ramsey-Goldman, Andrew J. Pellatt, Jaakko Kaprio, Jonathan N. Hofmann, Christian Gieger, Giuseppe Paolisso, Jacob B. H. Hjelmborg, Lisa Mirabello, Teresa Seeman, Jason Wong, Pim van der Harst, Linda Broer, Florian Kronenberg, Barbara Kollerits, Timo Strandberg, Dan TA Eisenberg, Catherine Duggan, Josine E. Verhoeven, Roxanne Schaakxs, Raffaela Zannolli, Rosana MR dos Reis, Fadi J. Charchar, Maciej Tomaszewski, U. Mons, Ilja Demuth, Andrea Elena Iglesias Molli, Guo Cheng, Dmytro Krasnienkov, Bianca D'Antono, Marek Kasielski, Barry J McDonnell, Richard P. Ebstein, Kristina Sundquist, Maurice P. Zeegers, TELOMAAS Group

^*Corresponding author for this work

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

63 Downloads (Pure)

Abstract

Background: Even before the onset of age-related diseases, obesity might be a contributing factor to the cumulative burden of oxidative stress and chronic inflammation throughout the life course. Obesity may therefore contribute to accelerated shortening of telomeres. Consequently, obese persons are more likely to have shorter telomeres, but the association between body mass index (BMI) and leukocyte telomere length (TL) might differ across the life span and between ethnicities and sexes.

Objective: A collaborative cross-sectionalmeta-analysis of observational studies was conducted to investigate the associations between BMI and TL across the life span.

Design: Eighty-seven distinct study samples were included in the meta-analysis capturing data from 146,114 individuals. Study-specific age-and sex-adjusted regression coefficients were combined by using a random-effects model in which absolute [base pairs (bp)] and relative telomere to single-copy gene ratio (T/S ratio) TLs were regressed against BMI. Stratified analysis was performed by 3 age categories ("young": 18-60 y; "middle": 61-75 y; and "old": > 75 y), sex, and ethnicity.

Results: Each unit increase in BMI corresponded to a-3.99 bp (95% CI: -5.17, -2.81 bp) difference in TL in the total pooled sample; among young adults, each unit increase in BMI corresponded to a -7.67 bp (95% CI:-10.03,-5.31 bp) difference. Each unit increase in BMI corresponded to a -1.58 x 10(-3) unit T/S ratio (0.16% decrease; 95% CI: -2.14 x 10(-3), -1.01 x 10(-3)) difference in ageand sex-adjusted relative TL in the total pooled sample; among young adults, each unit increase in BMI corresponded to a -2.58 x 10(-3) unit T/S ratio (0.26% decrease; 95% CI: -3.92 x 10(-3), -1.25 x 10(-3)). The associations were predominantly for the white pooled population. No sex differences were observed.

Conclusions: A higher BMI is associated with shorter telomeres, especially in younger individuals. The presently observed difference is not negligible. Meta-analyses of longitudinal studies evaluating change in body weight alongside change in TL are warranted.

Original language	English
Pages (from-to)	453-475
Number of pages	23
Journal	American Journal of Clinical Nutrition
Volume	108
Issue number	3
DOIs	https://doi.org/10.1093/ajcn/nqy107
Publication status	Published - Sept 2018

Keywords

BMI
telomere length
obesity
low-grade inflammation
meta-analysis
observational studies
STRONG HEART FAMILY
HELSINKI BIRTH COHORT
CORONARY-ARTERY CALCIFICATION
OXIDATIVE DNA-DAMAGE
PULSE-WAVE VELOCITY
II BASE-II
CARDIOVASCULAR-DISEASE
AMERICAN-INDIANS
CANCER RISK
INSULIN-RESISTANCE

Access to Document

10.1093/ajcn/nqy107Licence: Free access - publisher

Full text Final published version, 612 KBLicence: Taverne

Cite this

Gielen, M., Hageman, G. J., Antoniou, E. E., Nordfjall, K., Mangino, M., Balasubramanyam, M., de Meyer, T., Hendricks, A. E., Giltay, E. J., Hunt, S. C., Nettleton, J. A., Salpea, K. D., Diaz, V. A., Farzaneh-Far, R., Atzmon, G., Harris, S. E., Hou, L., Gilley, D., Hovatta, I., ... TELOMAAS Group (2018). Body mass index is negatively associated with telomere length: a collaborative cross-sectional meta-analysis of 87 observational studies. American Journal of Clinical Nutrition, 108(3), 453-475. https://doi.org/10.1093/ajcn/nqy107

@article{c0c6569184ef44439938aaf84f2ed881,

title = "Body mass index is negatively associated with telomere length: a collaborative cross-sectional meta-analysis of 87 observational studies",

abstract = "Background: Even before the onset of age-related diseases, obesity might be a contributing factor to the cumulative burden of oxidative stress and chronic inflammation throughout the life course. Obesity may therefore contribute to accelerated shortening of telomeres. Consequently, obese persons are more likely to have shorter telomeres, but the association between body mass index (BMI) and leukocyte telomere length (TL) might differ across the life span and between ethnicities and sexes.Objective: A collaborative cross-sectionalmeta-analysis of observational studies was conducted to investigate the associations between BMI and TL across the life span.Design: Eighty-seven distinct study samples were included in the meta-analysis capturing data from 146,114 individuals. Study-specific age-and sex-adjusted regression coefficients were combined by using a random-effects model in which absolute [base pairs (bp)] and relative telomere to single-copy gene ratio (T/S ratio) TLs were regressed against BMI. Stratified analysis was performed by 3 age categories ({"}young{"}: 18-60 y; {"}middle{"}: 61-75 y; and {"}old{"}: > 75 y), sex, and ethnicity.Results: Each unit increase in BMI corresponded to a-3.99 bp (95% CI: -5.17, -2.81 bp) difference in TL in the total pooled sample; among young adults, each unit increase in BMI corresponded to a -7.67 bp (95% CI:-10.03,-5.31 bp) difference. Each unit increase in BMI corresponded to a -1.58 x 10(-3) unit T/S ratio (0.16% decrease; 95% CI: -2.14 x 10(-3), -1.01 x 10(-3)) difference in ageand sex-adjusted relative TL in the total pooled sample; among young adults, each unit increase in BMI corresponded to a -2.58 x 10(-3) unit T/S ratio (0.26% decrease; 95% CI: -3.92 x 10(-3), -1.25 x 10(-3)). The associations were predominantly for the white pooled population. No sex differences were observed.Conclusions: A higher BMI is associated with shorter telomeres, especially in younger individuals. The presently observed difference is not negligible. Meta-analyses of longitudinal studies evaluating change in body weight alongside change in TL are warranted.",

keywords = "BMI, telomere length, obesity, low-grade inflammation, meta-analysis, observational studies, STRONG HEART FAMILY, HELSINKI BIRTH COHORT, CORONARY-ARTERY CALCIFICATION, OXIDATIVE DNA-DAMAGE, PULSE-WAVE VELOCITY, II BASE-II, CARDIOVASCULAR-DISEASE, AMERICAN-INDIANS, CANCER RISK, INSULIN-RESISTANCE",

author = "Marij Gielen and Hageman, {Geja J.} and Antoniou, {Evangelia E.} and Katarina Nordfjall and Massimo Mangino and Muthuswamy Balasubramanyam and {de Meyer}, Tim and Hendricks, {Audrey E.} and Giltay, {Erik J.} and Hunt, {Steven C.} and Nettleton, {Jennifer A.} and Salpea, {Klelia D.} and Diaz, {Vanessa A.} and Ramin Farzaneh-Far and Gil Atzmon and Harris, {Sarah E.} and Lifang Hou and David Gilley and Iiris Hovatta and Kark, {Jeremy D.} and Hisham Nassar and Kurz, {David J.} and Mather, {Karen A.} and Peter Willeit and Yun-Ling Zheng and Sofia Pavanello and Demerath, {Ellen W.} and Line Rode and Daniel Bunout and Andrew Steptoe and Lisa Boardman and Amelia Marti and Belinda Needham and Wei Zheng and Rosalind Ramsey-Goldman and Pellatt, {Andrew J.} and Jaakko Kaprio and Hofmann, {Jonathan N.} and Christian Gieger and Giuseppe Paolisso and Hjelmborg, {Jacob B. H.} and Lisa Mirabello and Teresa Seeman and Jason Wong and {van der Harst}, Pim and Linda Broer and Florian Kronenberg and Barbara Kollerits and Timo Strandberg and Eisenberg, {Dan TA} and Catherine Duggan and Verhoeven, {Josine E.} and Roxanne Schaakxs and Raffaela Zannolli and {dos Reis}, {Rosana MR} and Charchar, {Fadi J.} and Maciej Tomaszewski and U. Mons and Ilja Demuth and {Iglesias Molli}, {Andrea Elena} and Guo Cheng and Dmytro Krasnienkov and Bianca D'Antono and Marek Kasielski and McDonnell, {Barry J} and Ebstein, {Richard P.} and Kristina Sundquist and Zeegers, {Maurice P.} and {TELOMAAS Group}",

year = "2018",

month = sep,

doi = "10.1093/ajcn/nqy107",

language = "English",

volume = "108",

pages = "453--475",

journal = "American Journal of Clinical Nutrition",

issn = "0002-9165",

publisher = "Elsevier Inc.",

number = "3",

}

Gielen, M , Hageman, GJ, Antoniou, EE, Nordfjall, K, Mangino, M, Balasubramanyam, M, de Meyer, T, Hendricks, AE, Giltay, EJ, Hunt, SC, Nettleton, JA, Salpea, KD, Diaz, VA, Farzaneh-Far, R, Atzmon, G, Harris, SE, Hou, L, Gilley, D, Hovatta, I, Kark, JD, Nassar, H, Kurz, DJ, Mather, KA, Willeit, P, Zheng, Y-L, Pavanello, S, Demerath, EW, Rode, L, Bunout, D, Steptoe, A, Boardman, L, Marti, A, Needham, B, Zheng, W, Ramsey-Goldman, R, Pellatt, AJ, Kaprio, J, Hofmann, JN, Gieger, C, Paolisso, G, Hjelmborg, JBH, Mirabello, L, Seeman, T, Wong, J, van der Harst, P, Broer, L, Kronenberg, F, Kollerits, B, Strandberg, T, Eisenberg, DTA, Duggan, C, Verhoeven, JE, Schaakxs, R, Zannolli, R, dos Reis, RMR, Charchar, FJ, Tomaszewski, M, Mons, U, Demuth, I, Iglesias Molli, AE, Cheng, G, Krasnienkov, D, D'Antono, B, Kasielski, M, McDonnell, BJ, Ebstein, RP, Sundquist, K, Zeegers, MP & TELOMAAS Group 2018, 'Body mass index is negatively associated with telomere length: a collaborative cross-sectional meta-analysis of 87 observational studies', American Journal of Clinical Nutrition, vol. 108, no. 3, pp. 453-475. https://doi.org/10.1093/ajcn/nqy107

TY - JOUR

T1 - Body mass index is negatively associated with telomere length

T2 - a collaborative cross-sectional meta-analysis of 87 observational studies

AU - Gielen, Marij

AU - Hageman, Geja J.

AU - Antoniou, Evangelia E.

AU - Nordfjall, Katarina

AU - Mangino, Massimo

AU - Balasubramanyam, Muthuswamy

AU - de Meyer, Tim

AU - Hendricks, Audrey E.

AU - Giltay, Erik J.

AU - Hunt, Steven C.

AU - Nettleton, Jennifer A.

AU - Salpea, Klelia D.

AU - Diaz, Vanessa A.

AU - Farzaneh-Far, Ramin

AU - Atzmon, Gil

AU - Harris, Sarah E.

AU - Hou, Lifang

AU - Gilley, David

AU - Hovatta, Iiris

AU - Kark, Jeremy D.

AU - Nassar, Hisham

AU - Kurz, David J.

AU - Mather, Karen A.

AU - Willeit, Peter

AU - Zheng, Yun-Ling

AU - Pavanello, Sofia

AU - Demerath, Ellen W.

AU - Rode, Line

AU - Bunout, Daniel

AU - Steptoe, Andrew

AU - Boardman, Lisa

AU - Marti, Amelia

AU - Needham, Belinda

AU - Zheng, Wei

AU - Ramsey-Goldman, Rosalind

AU - Pellatt, Andrew J.

AU - Kaprio, Jaakko

AU - Hofmann, Jonathan N.

AU - Gieger, Christian

AU - Paolisso, Giuseppe

AU - Hjelmborg, Jacob B. H.

AU - Mirabello, Lisa

AU - Seeman, Teresa

AU - Wong, Jason

AU - van der Harst, Pim

AU - Broer, Linda

AU - Kronenberg, Florian

AU - Kollerits, Barbara

AU - Strandberg, Timo

AU - Eisenberg, Dan TA

AU - Duggan, Catherine

AU - Verhoeven, Josine E.

AU - Schaakxs, Roxanne

AU - Zannolli, Raffaela

AU - dos Reis, Rosana MR

AU - Charchar, Fadi J.

AU - Tomaszewski, Maciej

AU - Mons, U.

AU - Demuth, Ilja

AU - Iglesias Molli, Andrea Elena

AU - Cheng, Guo

AU - Krasnienkov, Dmytro

AU - D'Antono, Bianca

AU - Kasielski, Marek

AU - McDonnell, Barry J

AU - Ebstein, Richard P.

AU - Sundquist, Kristina

AU - Zeegers, Maurice P.

AU - TELOMAAS Group

PY - 2018/9

Y1 - 2018/9

N2 - Background: Even before the onset of age-related diseases, obesity might be a contributing factor to the cumulative burden of oxidative stress and chronic inflammation throughout the life course. Obesity may therefore contribute to accelerated shortening of telomeres. Consequently, obese persons are more likely to have shorter telomeres, but the association between body mass index (BMI) and leukocyte telomere length (TL) might differ across the life span and between ethnicities and sexes.Objective: A collaborative cross-sectionalmeta-analysis of observational studies was conducted to investigate the associations between BMI and TL across the life span.Design: Eighty-seven distinct study samples were included in the meta-analysis capturing data from 146,114 individuals. Study-specific age-and sex-adjusted regression coefficients were combined by using a random-effects model in which absolute [base pairs (bp)] and relative telomere to single-copy gene ratio (T/S ratio) TLs were regressed against BMI. Stratified analysis was performed by 3 age categories ("young": 18-60 y; "middle": 61-75 y; and "old": > 75 y), sex, and ethnicity.Results: Each unit increase in BMI corresponded to a-3.99 bp (95% CI: -5.17, -2.81 bp) difference in TL in the total pooled sample; among young adults, each unit increase in BMI corresponded to a -7.67 bp (95% CI:-10.03,-5.31 bp) difference. Each unit increase in BMI corresponded to a -1.58 x 10(-3) unit T/S ratio (0.16% decrease; 95% CI: -2.14 x 10(-3), -1.01 x 10(-3)) difference in ageand sex-adjusted relative TL in the total pooled sample; among young adults, each unit increase in BMI corresponded to a -2.58 x 10(-3) unit T/S ratio (0.26% decrease; 95% CI: -3.92 x 10(-3), -1.25 x 10(-3)). The associations were predominantly for the white pooled population. No sex differences were observed.Conclusions: A higher BMI is associated with shorter telomeres, especially in younger individuals. The presently observed difference is not negligible. Meta-analyses of longitudinal studies evaluating change in body weight alongside change in TL are warranted.

AB - Background: Even before the onset of age-related diseases, obesity might be a contributing factor to the cumulative burden of oxidative stress and chronic inflammation throughout the life course. Obesity may therefore contribute to accelerated shortening of telomeres. Consequently, obese persons are more likely to have shorter telomeres, but the association between body mass index (BMI) and leukocyte telomere length (TL) might differ across the life span and between ethnicities and sexes.Objective: A collaborative cross-sectionalmeta-analysis of observational studies was conducted to investigate the associations between BMI and TL across the life span.Design: Eighty-seven distinct study samples were included in the meta-analysis capturing data from 146,114 individuals. Study-specific age-and sex-adjusted regression coefficients were combined by using a random-effects model in which absolute [base pairs (bp)] and relative telomere to single-copy gene ratio (T/S ratio) TLs were regressed against BMI. Stratified analysis was performed by 3 age categories ("young": 18-60 y; "middle": 61-75 y; and "old": > 75 y), sex, and ethnicity.Results: Each unit increase in BMI corresponded to a-3.99 bp (95% CI: -5.17, -2.81 bp) difference in TL in the total pooled sample; among young adults, each unit increase in BMI corresponded to a -7.67 bp (95% CI:-10.03,-5.31 bp) difference. Each unit increase in BMI corresponded to a -1.58 x 10(-3) unit T/S ratio (0.16% decrease; 95% CI: -2.14 x 10(-3), -1.01 x 10(-3)) difference in ageand sex-adjusted relative TL in the total pooled sample; among young adults, each unit increase in BMI corresponded to a -2.58 x 10(-3) unit T/S ratio (0.26% decrease; 95% CI: -3.92 x 10(-3), -1.25 x 10(-3)). The associations were predominantly for the white pooled population. No sex differences were observed.Conclusions: A higher BMI is associated with shorter telomeres, especially in younger individuals. The presently observed difference is not negligible. Meta-analyses of longitudinal studies evaluating change in body weight alongside change in TL are warranted.

KW - BMI

KW - telomere length

KW - obesity

KW - low-grade inflammation

KW - meta-analysis

KW - observational studies

KW - STRONG HEART FAMILY

KW - HELSINKI BIRTH COHORT

KW - CORONARY-ARTERY CALCIFICATION

KW - OXIDATIVE DNA-DAMAGE

KW - PULSE-WAVE VELOCITY

KW - II BASE-II

KW - CARDIOVASCULAR-DISEASE

KW - AMERICAN-INDIANS

KW - CANCER RISK

KW - INSULIN-RESISTANCE

U2 - 10.1093/ajcn/nqy107

DO - 10.1093/ajcn/nqy107

M3 - Article

C2 - 30535086

SN - 0002-9165

VL - 108

SP - 453

EP - 475

JO - American Journal of Clinical Nutrition

JF - American Journal of Clinical Nutrition

IS - 3

ER -