Smoking remains associated with education after controlling for social background and genetic factors in a study of 18 twin cohorts

Karri Silventoinen; Maarit Piirtola; Aline Jelenkovic; Reijo Sund; Adam D. Tarnoki; David L. Tarnoki; Emanuela Medda; Lorenza Nisticò; Virgilia Toccaceli; Chika Honda; Fujio Inui; Rie Tomizawa; Mikio Watanabe; Norio Sakai; Margaret Gatz; David A. Butler; Jooyeon Lee; Soo Ji Lee; Joohon Sung; Carol E. Franz; William S. Kremen; Michael J. Lyons; Catherine A. Derom; Robert F. Vlietinck; Ruth J.F. Loos; Per Tynelius; Finn Rasmussen; Nicholas G. Martin; Sarah E. Medland; Grant W. Montgomery; Ingunn Brandt; Thomas S. Nilsen; Jennifer R. Harris; Jessica Tyler; John L. Hopper; Patrik K.E. Magnusson; Nancy L. Pedersen; Anna K. Dahl Aslan; Juan R. Ordoñana; Juan F. Sánchez-Romera; Lucia Colodro-Conde; Esther Rebato; Dongfeng Zhang; Zengchang Pang; Qihua Tan; Judy L. Silberg; Hermine H. Maes; Dorret I. Boomsma; Thorkild I.A. Sørensen; Tellervo Korhonen; Jaakko Kaprio

doi:10.1038/s41598-022-17536-x

Smoking remains associated with education after controlling for social background and genetic factors in a study of 18 twin cohorts

Karri Silventoinen^*, Maarit Piirtola, Aline Jelenkovic, Reijo Sund, Adam D. Tarnoki, David L. Tarnoki, Emanuela Medda, Lorenza Nisticò, Virgilia Toccaceli, Chika Honda, Fujio Inui, Rie Tomizawa, Mikio Watanabe, Norio Sakai, Margaret Gatz, David A. Butler, Jooyeon Lee, Soo Ji Lee, Joohon Sung, Carol E. FranzWilliam S. Kremen, Michael J. Lyons, Catherine A. Derom, Robert F. Vlietinck, Ruth J.F. Loos, Per Tynelius, Finn Rasmussen, Nicholas G. Martin, Sarah E. Medland, Grant W. Montgomery, Ingunn Brandt, Thomas S. Nilsen, Jennifer R. Harris, Jessica Tyler, John L. Hopper, Patrik K.E. Magnusson, Nancy L. Pedersen, Anna K. Dahl Aslan, Juan R. Ordoñana, Juan F. Sánchez-Romera, Lucia Colodro-Conde, Esther Rebato, Dongfeng Zhang, Zengchang Pang, Qihua Tan, Judy L. Silberg, Hermine H. Maes, Dorret I. Boomsma, Thorkild I.A. Sørensen, Tellervo Korhonen, Jaakko Kaprio

^*Corresponding author for this work

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

Abstract

We tested the causality between education and smoking using the natural experiment of discordant twin pairs allowing to optimally control for background genetic and childhood social factors. Data from 18 cohorts including 10,527 monozygotic (MZ) and same-sex dizygotic (DZ) twin pairs discordant for education and smoking were analyzed by linear fixed effects regression models. Within twin pairs, education levels were lower among the currently smoking than among the never smoking co-twins and this education difference was larger within DZ than MZ pairs. Similarly, education levels were higher among former smoking than among currently smoking co-twins, and this difference was larger within DZ pairs. Our results support the hypothesis of a causal effect of education on both current smoking status and smoking cessation. However, the even greater intra-pair differences within DZ pairs, who share only 50% of their segregating genes, provide evidence that shared genetic factors also contribute to these associations.

Original language	English
Article number	13148
Pages (from-to)	1-9
Number of pages	9
Journal	Scientific Reports
Volume	12
DOIs	https://doi.org/10.1038/s41598-022-17536-x
Publication status	Published - 31 Jul 2022

Bibliographical note

Funding Information:
This study was conducted within the CODATwins project. Open access funded by Helsinki University Library. Support for collaborators: This research was facilitated through access to Twins Research Australia, a national resource supported by a Centre of Research Excellence Grant (ID: 1079102), from the National Health and Medical Research Council. Data collection and analyses in Finnish twin cohorts have been supported by ENGAGE – European Network for Genetic and Genomic Epidemiology, FP7-HEALTH-F4-2007, Grant Agreement Number 201413, National Institute of Alcohol Abuse and Alcoholism (Grants AA-12502, AA-00145, and AA-09203 to R J Rose, the Academy of Finland Center of Excellence in Complex Disease Genetics (Grant Numbers: 213506, 129680), and the Academy of Finland (Grants 100499, 205585, 118555, 141054, 265240, 263278 and 264146 to J Kaprio). Since its origin the East Flanders Prospective Survey has been partly supported by Grants from the Fund of Scientific Research, Flanders and Twins, a non-profit Association for Scientific Research in Multiple Births (Belgium). Anthropometric measurements of the Hungarian twins were supported by Medexpert Ltd., Budapest, Hungary. Korean Twin-Family Register was supported by the Global Research Network Program of the National Research Foundation (NRF 2011-220-E00006). The Murcia Twin Registry is supported by Fundación Séneca, Regional Agency for Science and Technology, Murcia, Spain (19479/PI/14) and Ministry of Science and Innovation, Spain (RTI2018-095185-B-I00, co-funded by European Regional Development Fund (FEDER)). Osaka University Aged Twin Registry is supported by Grants from JSPS KAKENHI JP (23593419, 24792601, 26671010, 24590695, 26293128, 16K15385, 16K15978, 16K15989, 16H03261). The Swedish Twin Registry is managed by Karolinska Institutet and receives funding through the Swedish Research Council under the Grant No. 2017-00641. Vietnam Era Twin Study of Aging was supported by National Institute of Health Grants NIA R01 AG018384, R01 AG018386, R01 AG022381, and R01 AG022982. The Cooperative Studies Program of the Office of Research & Development of the United States Department of Veterans Affairs has provided financial support for the development and maintenance of the Vietnam Era Twin (VET) Registry. The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the NIA/NIH, or the VA. The NAS-NRC Twin Registry acknowledges financial support from the National Institutes of Health Grant Number R21 AG039572.

Publisher Copyright:
© 2022, The Author(s).

Funding

This study was conducted within the CODATwins project. Open access funded by Helsinki University Library. Support for collaborators: This research was facilitated through access to Twins Research Australia, a national resource supported by a Centre of Research Excellence Grant (ID: 1079102), from the National Health and Medical Research Council. Data collection and analyses in Finnish twin cohorts have been supported by ENGAGE – European Network for Genetic and Genomic Epidemiology, FP7-HEALTH-F4-2007, Grant Agreement Number 201413, National Institute of Alcohol Abuse and Alcoholism (Grants AA-12502, AA-00145, and AA-09203 to R J Rose, the Academy of Finland Center of Excellence in Complex Disease Genetics (Grant Numbers: 213506, 129680), and the Academy of Finland (Grants 100499, 205585, 118555, 141054, 265240, 263278 and 264146 to J Kaprio). Since its origin the East Flanders Prospective Survey has been partly supported by Grants from the Fund of Scientific Research, Flanders and Twins, a non-profit Association for Scientific Research in Multiple Births (Belgium). Anthropometric measurements of the Hungarian twins were supported by Medexpert Ltd., Budapest, Hungary. Korean Twin-Family Register was supported by the Global Research Network Program of the National Research Foundation (NRF 2011-220-E00006). The Murcia Twin Registry is supported by Fundación Séneca, Regional Agency for Science and Technology, Murcia, Spain (19479/PI/14) and Ministry of Science and Innovation, Spain (RTI2018-095185-B-I00, co-funded by European Regional Development Fund (FEDER)). Osaka University Aged Twin Registry is supported by Grants from JSPS KAKENHI JP (23593419, 24792601, 26671010, 24590695, 26293128, 16K15385, 16K15978, 16K15989, 16H03261). The Swedish Twin Registry is managed by Karolinska Institutet and receives funding through the Swedish Research Council under the Grant No. 2017-00641. Vietnam Era Twin Study of Aging was supported by National Institute of Health Grants NIA R01 AG018384, R01 AG018386, R01 AG022381, and R01 AG022982. The Cooperative Studies Program of the Office of Research & Development of the United States Department of Veterans Affairs has provided financial support for the development and maintenance of the Vietnam Era Twin (VET) Registry. The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the NIA/NIH, or the VA. The NAS-NRC Twin Registry acknowledges financial support from the National Institutes of Health Grant Number R21 AG039572.

Funders	Funder number
Academy of Finland Center of Excellence in Complex Disease Genetics	213506, 129680
FP7-HEALTH-F4-2007	201413
Fund of Scientific Research, Flanders and Twins
Helsinki University Library	1079102
Medexpert Ltd.
Regional Agency for Science and Technology, Murcia, Spain	19479/PI/14
National Institutes of Health	R21 AG039572
National Institute on Alcohol Abuse and Alcoholism	AA-09203, K05AA000145, AA-12502
National Institute on Aging	R01 AG022381, R01 AG018384, R01 AG022982, R01 AG018386
U.S. Department of Veterans Affairs
Office of Research and Development
Fundación Séneca
National Health and Medical Research Council
Japan Society for the Promotion of Science	16K15978, 16K15989, 24590695, 16H03261, 16K15385, 26293128, 23593419, 26671010, 24792601
Academy of Finland	141054, 264146, 205585, 118555, 263278, 265240, 100499
National Research Foundation of Korea	2011-220-E00006
Karolinska Institutet
Vetenskapsrådet	2017-00641
Ministerio de Ciencia e Innovación	RTI2018-095185-B-I00
European Regional Development Fund

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/s41598-022-17536-x

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Silventoinen, K., Piirtola, M., Jelenkovic, A., Sund, R., Tarnoki, A. D., Tarnoki, D. L., Medda, E., Nisticò, L., Toccaceli, V., Honda, C., Inui, F., Tomizawa, R., Watanabe, M., Sakai, N., Gatz, M., Butler, D. A., Lee, J., Lee, S. J., Sung, J., ... Kaprio, J. (2022). Smoking remains associated with education after controlling for social background and genetic factors in a study of 18 twin cohorts. Scientific Reports, 12, 1-9. Article 13148. https://doi.org/10.1038/s41598-022-17536-x

@article{a269c5fd7373400398dc364f10468db9,

title = "Smoking remains associated with education after controlling for social background and genetic factors in a study of 18 twin cohorts",

abstract = "We tested the causality between education and smoking using the natural experiment of discordant twin pairs allowing to optimally control for background genetic and childhood social factors. Data from 18 cohorts including 10,527 monozygotic (MZ) and same-sex dizygotic (DZ) twin pairs discordant for education and smoking were analyzed by linear fixed effects regression models. Within twin pairs, education levels were lower among the currently smoking than among the never smoking co-twins and this education difference was larger within DZ than MZ pairs. Similarly, education levels were higher among former smoking than among currently smoking co-twins, and this difference was larger within DZ pairs. Our results support the hypothesis of a causal effect of education on both current smoking status and smoking cessation. However, the even greater intra-pair differences within DZ pairs, who share only 50% of their segregating genes, provide evidence that shared genetic factors also contribute to these associations.",

author = "Karri Silventoinen and Maarit Piirtola and Aline Jelenkovic and Reijo Sund and Tarnoki, {Adam D.} and Tarnoki, {David L.} and Emanuela Medda and Lorenza Nistic{\`o} and Virgilia Toccaceli and Chika Honda and Fujio Inui and Rie Tomizawa and Mikio Watanabe and Norio Sakai and Margaret Gatz and Butler, {David A.} and Jooyeon Lee and Lee, {Soo Ji} and Joohon Sung and Franz, {Carol E.} and Kremen, {William S.} and Lyons, {Michael J.} and Derom, {Catherine A.} and Vlietinck, {Robert F.} and Loos, {Ruth J.F.} and Per Tynelius and Finn Rasmussen and Martin, {Nicholas G.} and Medland, {Sarah E.} and Montgomery, {Grant W.} and Ingunn Brandt and Nilsen, {Thomas S.} and Harris, {Jennifer R.} and Jessica Tyler and Hopper, {John L.} and Magnusson, {Patrik K.E.} and Pedersen, {Nancy L.} and {Dahl Aslan}, {Anna K.} and Ordo{\~n}ana, {Juan R.} and S{\'a}nchez-Romera, {Juan F.} and Lucia Colodro-Conde and Esther Rebato and Dongfeng Zhang and Zengchang Pang and Qihua Tan and Silberg, {Judy L.} and Maes, {Hermine H.} and Boomsma, {Dorret I.} and S{\o}rensen, {Thorkild I.A.} and Tellervo Korhonen and Jaakko Kaprio",

note = "Funding Information: This study was conducted within the CODATwins project. Open access funded by Helsinki University Library. Support for collaborators: This research was facilitated through access to Twins Research Australia, a national resource supported by a Centre of Research Excellence Grant (ID: 1079102), from the National Health and Medical Research Council. Data collection and analyses in Finnish twin cohorts have been supported by ENGAGE – European Network for Genetic and Genomic Epidemiology, FP7-HEALTH-F4-2007, Grant Agreement Number 201413, National Institute of Alcohol Abuse and Alcoholism (Grants AA-12502, AA-00145, and AA-09203 to R J Rose, the Academy of Finland Center of Excellence in Complex Disease Genetics (Grant Numbers: 213506, 129680), and the Academy of Finland (Grants 100499, 205585, 118555, 141054, 265240, 263278 and 264146 to J Kaprio). Since its origin the East Flanders Prospective Survey has been partly supported by Grants from the Fund of Scientific Research, Flanders and Twins, a non-profit Association for Scientific Research in Multiple Births (Belgium). Anthropometric measurements of the Hungarian twins were supported by Medexpert Ltd., Budapest, Hungary. Korean Twin-Family Register was supported by the Global Research Network Program of the National Research Foundation (NRF 2011-220-E00006). The Murcia Twin Registry is supported by Fundaci{\'o}n S{\'e}neca, Regional Agency for Science and Technology, Murcia, Spain (19479/PI/14) and Ministry of Science and Innovation, Spain (RTI2018-095185-B-I00, co-funded by European Regional Development Fund (FEDER)). Osaka University Aged Twin Registry is supported by Grants from JSPS KAKENHI JP (23593419, 24792601, 26671010, 24590695, 26293128, 16K15385, 16K15978, 16K15989, 16H03261). The Swedish Twin Registry is managed by Karolinska Institutet and receives funding through the Swedish Research Council under the Grant No. 2017-00641. Vietnam Era Twin Study of Aging was supported by National Institute of Health Grants NIA R01 AG018384, R01 AG018386, R01 AG022381, and R01 AG022982. The Cooperative Studies Program of the Office of Research & Development of the United States Department of Veterans Affairs has provided financial support for the development and maintenance of the Vietnam Era Twin (VET) Registry. The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the NIA/NIH, or the VA. The NAS-NRC Twin Registry acknowledges financial support from the National Institutes of Health Grant Number R21 AG039572. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = jul,

day = "31",

doi = "10.1038/s41598-022-17536-x",

language = "English",

volume = "12",

pages = "1--9",

journal = "Scientific Reports",

issn = "2045-2322",

publisher = "Nature Publishing Group",

}

Silventoinen, K, Piirtola, M, Jelenkovic, A, Sund, R, Tarnoki, AD, Tarnoki, DL, Medda, E, Nisticò, L, Toccaceli, V, Honda, C, Inui, F, Tomizawa, R, Watanabe, M, Sakai, N, Gatz, M, Butler, DA, Lee, J, Lee, SJ, Sung, J, Franz, CE, Kremen, WS, Lyons, MJ, Derom, CA, Vlietinck, RF, Loos, RJF, Tynelius, P, Rasmussen, F, Martin, NG, Medland, SE, Montgomery, GW, Brandt, I, Nilsen, TS, Harris, JR, Tyler, J, Hopper, JL, Magnusson, PKE, Pedersen, NL, Dahl Aslan, AK, Ordoñana, JR, Sánchez-Romera, JF, Colodro-Conde, L, Rebato, E, Zhang, D, Pang, Z, Tan, Q, Silberg, JL, Maes, HH, Boomsma, DI, Sørensen, TIA, Korhonen, T & Kaprio, J 2022, 'Smoking remains associated with education after controlling for social background and genetic factors in a study of 18 twin cohorts', Scientific Reports, vol. 12, 13148, pp. 1-9. https://doi.org/10.1038/s41598-022-17536-x

TY - JOUR

T1 - Smoking remains associated with education after controlling for social background and genetic factors in a study of 18 twin cohorts

AU - Silventoinen, Karri

AU - Piirtola, Maarit

AU - Jelenkovic, Aline

AU - Sund, Reijo

AU - Tarnoki, Adam D.

AU - Tarnoki, David L.

AU - Medda, Emanuela

AU - Nisticò, Lorenza

AU - Toccaceli, Virgilia

AU - Honda, Chika

AU - Inui, Fujio

AU - Tomizawa, Rie

AU - Watanabe, Mikio

AU - Sakai, Norio

AU - Gatz, Margaret

AU - Butler, David A.

AU - Lee, Jooyeon

AU - Lee, Soo Ji

AU - Sung, Joohon

AU - Franz, Carol E.

AU - Kremen, William S.

AU - Lyons, Michael J.

AU - Derom, Catherine A.

AU - Vlietinck, Robert F.

AU - Loos, Ruth J.F.

AU - Tynelius, Per

AU - Rasmussen, Finn

AU - Martin, Nicholas G.

AU - Medland, Sarah E.

AU - Montgomery, Grant W.

AU - Brandt, Ingunn

AU - Nilsen, Thomas S.

AU - Harris, Jennifer R.

AU - Tyler, Jessica

AU - Hopper, John L.

AU - Magnusson, Patrik K.E.

AU - Pedersen, Nancy L.

AU - Dahl Aslan, Anna K.

AU - Ordoñana, Juan R.

AU - Sánchez-Romera, Juan F.

AU - Colodro-Conde, Lucia

AU - Rebato, Esther

AU - Zhang, Dongfeng

AU - Pang, Zengchang

AU - Tan, Qihua

AU - Silberg, Judy L.

AU - Maes, Hermine H.

AU - Boomsma, Dorret I.

AU - Sørensen, Thorkild I.A.

AU - Korhonen, Tellervo

AU - Kaprio, Jaakko

N1 - Funding Information: This study was conducted within the CODATwins project. Open access funded by Helsinki University Library. Support for collaborators: This research was facilitated through access to Twins Research Australia, a national resource supported by a Centre of Research Excellence Grant (ID: 1079102), from the National Health and Medical Research Council. Data collection and analyses in Finnish twin cohorts have been supported by ENGAGE – European Network for Genetic and Genomic Epidemiology, FP7-HEALTH-F4-2007, Grant Agreement Number 201413, National Institute of Alcohol Abuse and Alcoholism (Grants AA-12502, AA-00145, and AA-09203 to R J Rose, the Academy of Finland Center of Excellence in Complex Disease Genetics (Grant Numbers: 213506, 129680), and the Academy of Finland (Grants 100499, 205585, 118555, 141054, 265240, 263278 and 264146 to J Kaprio). Since its origin the East Flanders Prospective Survey has been partly supported by Grants from the Fund of Scientific Research, Flanders and Twins, a non-profit Association for Scientific Research in Multiple Births (Belgium). Anthropometric measurements of the Hungarian twins were supported by Medexpert Ltd., Budapest, Hungary. Korean Twin-Family Register was supported by the Global Research Network Program of the National Research Foundation (NRF 2011-220-E00006). The Murcia Twin Registry is supported by Fundación Séneca, Regional Agency for Science and Technology, Murcia, Spain (19479/PI/14) and Ministry of Science and Innovation, Spain (RTI2018-095185-B-I00, co-funded by European Regional Development Fund (FEDER)). Osaka University Aged Twin Registry is supported by Grants from JSPS KAKENHI JP (23593419, 24792601, 26671010, 24590695, 26293128, 16K15385, 16K15978, 16K15989, 16H03261). The Swedish Twin Registry is managed by Karolinska Institutet and receives funding through the Swedish Research Council under the Grant No. 2017-00641. Vietnam Era Twin Study of Aging was supported by National Institute of Health Grants NIA R01 AG018384, R01 AG018386, R01 AG022381, and R01 AG022982. The Cooperative Studies Program of the Office of Research & Development of the United States Department of Veterans Affairs has provided financial support for the development and maintenance of the Vietnam Era Twin (VET) Registry. The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the NIA/NIH, or the VA. The NAS-NRC Twin Registry acknowledges financial support from the National Institutes of Health Grant Number R21 AG039572. Publisher Copyright: © 2022, The Author(s).

PY - 2022/7/31

Y1 - 2022/7/31

N2 - We tested the causality between education and smoking using the natural experiment of discordant twin pairs allowing to optimally control for background genetic and childhood social factors. Data from 18 cohorts including 10,527 monozygotic (MZ) and same-sex dizygotic (DZ) twin pairs discordant for education and smoking were analyzed by linear fixed effects regression models. Within twin pairs, education levels were lower among the currently smoking than among the never smoking co-twins and this education difference was larger within DZ than MZ pairs. Similarly, education levels were higher among former smoking than among currently smoking co-twins, and this difference was larger within DZ pairs. Our results support the hypothesis of a causal effect of education on both current smoking status and smoking cessation. However, the even greater intra-pair differences within DZ pairs, who share only 50% of their segregating genes, provide evidence that shared genetic factors also contribute to these associations.

AB - We tested the causality between education and smoking using the natural experiment of discordant twin pairs allowing to optimally control for background genetic and childhood social factors. Data from 18 cohorts including 10,527 monozygotic (MZ) and same-sex dizygotic (DZ) twin pairs discordant for education and smoking were analyzed by linear fixed effects regression models. Within twin pairs, education levels were lower among the currently smoking than among the never smoking co-twins and this education difference was larger within DZ than MZ pairs. Similarly, education levels were higher among former smoking than among currently smoking co-twins, and this difference was larger within DZ pairs. Our results support the hypothesis of a causal effect of education on both current smoking status and smoking cessation. However, the even greater intra-pair differences within DZ pairs, who share only 50% of their segregating genes, provide evidence that shared genetic factors also contribute to these associations.

UR - http://www.scopus.com/inward/record.url?scp=85135182674&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85135182674&partnerID=8YFLogxK

U2 - 10.1038/s41598-022-17536-x

DO - 10.1038/s41598-022-17536-x

M3 - Article

C2 - 35909142

AN - SCOPUS:85135182674

SN - 2045-2322

VL - 12

SP - 1

EP - 9

JO - Scientific Reports

JF - Scientific Reports

M1 - 13148

ER -

Smoking remains associated with education after controlling for social background and genetic factors in a study of 18 twin cohorts

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