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Published in: BMC Medicine 1/2022

01-12-2022 | Affective Disorder | Research article

Impact of prenatal tobacco smoking on infant telomere length trajectory and ADHD symptoms at 18 months: a longitudinal cohort study

Authors: Meghan P. Howell, Christopher W. Jones, Cade A. Herman, Celia V. Mayne, Camilo Fernandez, Katherine P. Theall, Kyle C. Esteves, Stacy S. Drury

Published in: BMC Medicine | Issue 1/2022

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Abstract

Background

Prenatal maternal tobacco smoking is a predictor of child attention-deficit/hyperactivity disorder (ADHD) and is associated with offspring telomere length (TL). In this study, we examine the relationship between maternal prenatal smoking, infant TL, and maternal report of early childhood symptoms of ADHD.

Methods

One-hundred and eighty-one mother-infant dyads were followed prospectively for the infant’s first 18 months of life. Prenatal smoking was assessed from maternal report and medical records. TL was measured from infant buccal swab DNA obtained across the first 18 months of life. ADHD symptoms were obtained from maternal report on the Child Behavior Check List. Multiple regression models tested the relation between prenatal smoking and both ADHD symptoms and infant TL. Additional analyses tested whether the change in infant TL influenced the relation between prenatal smoking and ADHD symptoms.

Results

Sixteen percent of mothers reported prenatal smoking. Infant TL at 4, 12, and 18 months of age were correlated. Consistent with previous cross-sectional studies linking shorter offspring TL to maternal prenatal smoking, maternal prenatal smoking predicted greater telomere shortening from four to 18 months of infant age (β = − 5.797, 95% CI [-10.207, -1.386]; p = 0.010). Maternal depression was positively associated with both prenatal smoking (odds ratio (OR): 4.614, 95% CI [1.733, 12.282]; p = 0.002) and child ADHD symptoms (β = 4.713, 95% CI [2.073, 7.354]; p = 0.0006). To prevent confounding, analyses examined the relation between TL, ADHD symptoms, and prenatal smoking only in non-depressed mothers. In non-depressed mothers, infant TL attrition across the first 18 months moderated the relation between smoking and child ADHD.

Conclusions

The findings extend previous studies linking prenatal smoking to shorter infant TL by providing data demonstrating the effect on TL trajectory. The relation between prenatal smoking and early infant ADHD symptoms was moderated by the change in TL. The findings provide novel initial evidence suggesting that TL dynamics are one mechanistic pathway influencing the relation between maternal prenatal smoking and ADHD.
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Literature
1.
go back to reference Drake P, Driscoll AK, Mathews TJ. Cigarette smoking during pregnancy: United States, 2016. NCHS Data Brief. 2018;305:1–8. PMID: 29528282. Drake P, Driscoll AK, Mathews TJ. Cigarette smoking during pregnancy: United States, 2016. NCHS Data Brief. 2018;305:1–8. PMID: 29528282.
5.
go back to reference Burke H, Leonardi-Bee J, Hashim A, Pine-Abata H, Chen Y, Cook DG, et al. Prenatal and passive smoke exposure and incidence of asthma and wheeze: systematic review and meta-analysis. Pediatrics. 2012;129(4):735–44.CrossRef Burke H, Leonardi-Bee J, Hashim A, Pine-Abata H, Chen Y, Cook DG, et al. Prenatal and passive smoke exposure and incidence of asthma and wheeze: systematic review and meta-analysis. Pediatrics. 2012;129(4):735–44.CrossRef
7.
go back to reference Durmuş B, Heppe DH, Taal HR, Manniesing R, Raat H, Hofman A, Steegers EA, Gaillard R, Jaddoe VW. Parental smoking during pregnancy and total and abdominal fat distribution in school-age children: the Generation R Study. Int J Obes (Lond). 2014;38(7):966-72. https://doi.org/10.1038/ijo.2014.9. Durmuş B, Heppe DH, Taal HR, Manniesing R, Raat H, Hofman A, Steegers EA, Gaillard R, Jaddoe VW. Parental smoking during pregnancy and total and abdominal fat distribution in school-age children: the Generation R Study. Int J Obes (Lond). 2014;38(7):966-72. https://​doi.​org/​10.​1038/​ijo.​2014.​9.
8.
go back to reference Dong T, Hu W, Zhou X, Lin H, Lan L, Hang B, et al. Prenatal exposure to maternal smoking during pregnancy and attention-deficit/hyperactivity disorder in offspring: A meta-analysis. Reprod Toxicol. 2018;76:63–70.CrossRef Dong T, Hu W, Zhou X, Lin H, Lan L, Hang B, et al. Prenatal exposure to maternal smoking during pregnancy and attention-deficit/hyperactivity disorder in offspring: A meta-analysis. Reprod Toxicol. 2018;76:63–70.CrossRef
9.
go back to reference Huang L, Wang Y, Zhang L, Zheng Z, Zhu T, Qu Y, et al. Maternal smoking and attention-deficit/hyperactivity disorder in offspring: a meta-analysis. Pediatrics. 2018;141(1):e20172465.CrossRef Huang L, Wang Y, Zhang L, Zheng Z, Zhu T, Qu Y, et al. Maternal smoking and attention-deficit/hyperactivity disorder in offspring: a meta-analysis. Pediatrics. 2018;141(1):e20172465.CrossRef
10.
go back to reference Makadia LD, Roper PJ, Andrews JO, Tingen MS. Tobacco Use and smoke exposure in children: new trends, harm, and strategies to improve health outcomes. Curr Allergy Asthma Rep. 2017;17(8):55.CrossRef Makadia LD, Roper PJ, Andrews JO, Tingen MS. Tobacco Use and smoke exposure in children: new trends, harm, and strategies to improve health outcomes. Curr Allergy Asthma Rep. 2017;17(8):55.CrossRef
11.
go back to reference Health CfDCaPNCfCDPaHPOoSa. How tobacco smoke causes disease: the biology and behavioral basis for smoking-attributable disease: a report of the surgeon general: Centers for Disease Control and Prevention (US); 2010. Health CfDCaPNCfCDPaHPOoSa. How tobacco smoke causes disease: the biology and behavioral basis for smoking-attributable disease: a report of the surgeon general: Centers for Disease Control and Prevention (US); 2010.
12.
go back to reference Garrabou G, Hernandez AS, Catalan Garcia M, Moren C, Tobias E, Cordoba S, et al. Molecular basis of reduced birth weight in smoking pregnant women: mitochondrial dysfunction and apoptosis. Addict Biol. 2016;21(1):159–70.CrossRef Garrabou G, Hernandez AS, Catalan Garcia M, Moren C, Tobias E, Cordoba S, et al. Molecular basis of reduced birth weight in smoking pregnant women: mitochondrial dysfunction and apoptosis. Addict Biol. 2016;21(1):159–70.CrossRef
13.
go back to reference Astuti Y, Wardhana A, Watkins J, Wulaningsih W. Cigarette smoking and telomere length: a systematic review of 84 studies and meta-analysis. Environ Res. 2017;158:480–9.CrossRef Astuti Y, Wardhana A, Watkins J, Wulaningsih W. Cigarette smoking and telomere length: a systematic review of 84 studies and meta-analysis. Environ Res. 2017;158:480–9.CrossRef
14.
go back to reference Savage SA, Bertuch AA. The genetics and clinical manifestations of telomere biology disorders. Genet Med. 2010;12(12):753–64.CrossRef Savage SA, Bertuch AA. The genetics and clinical manifestations of telomere biology disorders. Genet Med. 2010;12(12):753–64.CrossRef
15.
go back to reference Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas LF, et al. Obesity, cigarette smoking, and telomere length in women. Lancet. 2005;366(9486):662–4.CrossRef Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas LF, et al. Obesity, cigarette smoking, and telomere length in women. Lancet. 2005;366(9486):662–4.CrossRef
16.
go back to reference Khan RJ, Gebreab SY, Gaye A, Crespo PR, Xu R, Davis SK. Associations of smoking indicators and cotinine levels with telomere length: National Health and Nutrition Examination Survey. Prev Med Rep. 2019;15:100895.CrossRef Khan RJ, Gebreab SY, Gaye A, Crespo PR, Xu R, Davis SK. Associations of smoking indicators and cotinine levels with telomere length: National Health and Nutrition Examination Survey. Prev Med Rep. 2019;15:100895.CrossRef
17.
go back to reference Bateson M, Aviv A, Bendix L, Benetos A, Ben-Shlomo Y, Bojesen SE, et al. Smoking does not accelerate leucocyte telomere attrition: a meta-analysis of 18 longitudinal cohorts. R Soc Open Sci. 2019;6(6):190420.CrossRef Bateson M, Aviv A, Bendix L, Benetos A, Ben-Shlomo Y, Bojesen SE, et al. Smoking does not accelerate leucocyte telomere attrition: a meta-analysis of 18 longitudinal cohorts. R Soc Open Sci. 2019;6(6):190420.CrossRef
18.
go back to reference Factor-Litvak P, Susser E, Kezios K, McKeague I, Kark JD, Hoffman M, et al. Leukocyte telomere length in newborns: implications for the role of telomeres in human disease. Pediatrics. 2016;137(4). Factor-Litvak P, Susser E, Kezios K, McKeague I, Kark JD, Hoffman M, et al. Leukocyte telomere length in newborns: implications for the role of telomeres in human disease. Pediatrics. 2016;137(4).
19.
go back to reference Benetos A, Kark JD, Susser E, Kimura M, Sinnreich R, Chen W, et al. Tracking and fixed ranking of leukocyte telomere length across the adult life course. Aging Cell. 2013;12(4):615–21.CrossRef Benetos A, Kark JD, Susser E, Kimura M, Sinnreich R, Chen W, et al. Tracking and fixed ranking of leukocyte telomere length across the adult life course. Aging Cell. 2013;12(4):615–21.CrossRef
20.
go back to reference Ip P, Chung BHY, Ho FKW, Chan GCF, Deng W, Wong WHS, et al. Prenatal tobacco exposure shortens telomere length in children. Nicotine Tob Res. 2016;19(1):111–8.CrossRef Ip P, Chung BHY, Ho FKW, Chan GCF, Deng W, Wong WHS, et al. Prenatal tobacco exposure shortens telomere length in children. Nicotine Tob Res. 2016;19(1):111–8.CrossRef
21.
go back to reference Liu B, Song L, Zhang L, Wu M, Wang L, Cao Z, et al. Prenatal second-hand smoke exposure and newborn telomere length. Pediatr Res. 2019. Liu B, Song L, Zhang L, Wu M, Wang L, Cao Z, et al. Prenatal second-hand smoke exposure and newborn telomere length. Pediatr Res. 2019.
22.
go back to reference Osorio-Yáñez C, Clemente DBP, Maitre L, Vives-Usano M, Bustamante M, Martinez D, et al. Early life tobacco exposure and children's telomere length: the HELIX project. (1879-1026 (Electronic)). Osorio-Yáñez C, Clemente DBP, Maitre L, Vives-Usano M, Bustamante M, Martinez D, et al. Early life tobacco exposure and children's telomere length: the HELIX project. (1879-1026 (Electronic)).
23.
go back to reference Mirzakhani H, De Vivo I, Leeder JS, Gaedigk R, Vyhlidal CA, Weiss ST, et al. Early pregnancy intrauterine fetal exposure to maternal smoking and impact on fetal telomere length. Eur J Obstet Gynecol Reprod Biol. 2017;218:27–32.CrossRef Mirzakhani H, De Vivo I, Leeder JS, Gaedigk R, Vyhlidal CA, Weiss ST, et al. Early pregnancy intrauterine fetal exposure to maternal smoking and impact on fetal telomere length. Eur J Obstet Gynecol Reprod Biol. 2017;218:27–32.CrossRef
24.
go back to reference Salihu HM, Pradhan A, King L, Paothong A, Nwoga C, Marty PJ, et al. Impact of intrauterine tobacco exposure on fetal telomere length. Am J Obstet Gynecol. 2015;212(2):205. e1–8.CrossRef Salihu HM, Pradhan A, King L, Paothong A, Nwoga C, Marty PJ, et al. Impact of intrauterine tobacco exposure on fetal telomere length. Am J Obstet Gynecol. 2015;212(2):205. e1–8.CrossRef
25.
go back to reference Theall KP, McKasson S, Mabile E, Dunaway LF, Drury SS. Early hits and long-term consequences: tracking the lasting impact of prenatal smoke exposure on telomere length in children. Am J Public Health. 2013;103(S1):S133–S5.CrossRef Theall KP, McKasson S, Mabile E, Dunaway LF, Drury SS. Early hits and long-term consequences: tracking the lasting impact of prenatal smoke exposure on telomere length in children. Am J Public Health. 2013;103(S1):S133–S5.CrossRef
26.
go back to reference Almanzar G, Eberle G, Lassacher A, Specht C, Koppelstaetter C, Heinz-Erian P, et al. Maternal cigarette smoking and its effect on neonatal lymphocyte subpopulations and replication. BMC Pediatr. 2013;13:57.CrossRef Almanzar G, Eberle G, Lassacher A, Specht C, Koppelstaetter C, Heinz-Erian P, et al. Maternal cigarette smoking and its effect on neonatal lymphocyte subpopulations and replication. BMC Pediatr. 2013;13:57.CrossRef
27.
go back to reference Zhang L, Song L, Liu B, Wu M, Wang L, Zhang B, et al. Prenatal cadmium exposure is associated with shorter leukocyte telomere length in Chinese newborns. Zhang L, Song L, Liu B, Wu M, Wang L, Zhang B, et al. Prenatal cadmium exposure is associated with shorter leukocyte telomere length in Chinese newborns.
28.
go back to reference Yeh JK, Wang CY. Telomeres and telomerase in cardiovascular diseases. Genes (Basel). 2016;7(9). Yeh JK, Wang CY. Telomeres and telomerase in cardiovascular diseases. Genes (Basel). 2016;7(9).
29.
go back to reference Clemente DBP, Maitre L, Bustamante M, Chatzi L, Roumeliotaki T, Fossati S, et al. Obesity is associated with shorter telomeres in 8 year-old children. Sci Rep. 2019;9(1):18739.CrossRef Clemente DBP, Maitre L, Bustamante M, Chatzi L, Roumeliotaki T, Fossati S, et al. Obesity is associated with shorter telomeres in 8 year-old children. Sci Rep. 2019;9(1):18739.CrossRef
30.
go back to reference Wang J, Dong X, Cao L, Sun Y, Qiu Y, Zhang Y, et al. Association between telomere length and diabetes mellitus: a meta-analysis. J Int Med Res. 2016;44. Wang J, Dong X, Cao L, Sun Y, Qiu Y, Zhang Y, et al. Association between telomere length and diabetes mellitus: a meta-analysis. J Int Med Res. 2016;44.
31.
go back to reference Barnes RP, Fouquerel E, Opresko PL. The impact of oxidative DNA damage and stress on telomere homeostasis. Mech Ageing Dev. 2019;177:37–45.CrossRef Barnes RP, Fouquerel E, Opresko PL. The impact of oxidative DNA damage and stress on telomere homeostasis. Mech Ageing Dev. 2019;177:37–45.CrossRef
32.
go back to reference Di Micco R, Krizhanovsky V, Baker D, d'Adda di Fagagna F. Cellular senescence in ageing: from mechanisms to therapeutic opportunities. Nat Rev Mol Cell Biol. 2021;22(2):75–95.CrossRef Di Micco R, Krizhanovsky V, Baker D, d'Adda di Fagagna F. Cellular senescence in ageing: from mechanisms to therapeutic opportunities. Nat Rev Mol Cell Biol. 2021;22(2):75–95.CrossRef
33.
go back to reference Costa Dde S, Rosa DV, Barros AG, Romano-Silva MA, Malloy-Diniz LF, Mattos P, et al. Telomere length is highly inherited and associated with hyperactivity-impulsivity in children with attention deficit/hyperactivity disorder. Front Mol Neurosci. 2015;8:28.PubMed Costa Dde S, Rosa DV, Barros AG, Romano-Silva MA, Malloy-Diniz LF, Mattos P, et al. Telomere length is highly inherited and associated with hyperactivity-impulsivity in children with attention deficit/hyperactivity disorder. Front Mol Neurosci. 2015;8:28.PubMed
34.
go back to reference Momany AM, Lussier S, Nikolas MA, Stevens H. Telomere length and ADHD symptoms in young adults. J Atten Disord. 2019;1087054719865776. Momany AM, Lussier S, Nikolas MA, Stevens H. Telomere length and ADHD symptoms in young adults. J Atten Disord. 2019;1087054719865776.
35.
go back to reference Krieger N, Chen Jt, Waterman PD, Soobader MJ, Subramanian SV, Carson R. Choosing area based socioeconomic measures to monitor social inequalities in low birth weight and childhood lead poisoning: The Public Health Disparities Geocoding Project (US). (0143-005X (Print)). Krieger N, Chen Jt, Waterman PD, Soobader MJ, Subramanian SV, Carson R. Choosing area based socioeconomic measures to monitor social inequalities in low birth weight and childhood lead poisoning: The Public Health Disparities Geocoding Project (US). (0143-005X (Print)).
36.
go back to reference Jones CW, Gambala C, Esteves KC, Wallace M, Schlesinger R, O’Quinn M, et al. Differences in placental telomere length suggest a link between racial disparities in birth outcomes and cellular aging. Am J Obstet Gynecol. 2017;216(3):294. e1–8.CrossRef Jones CW, Gambala C, Esteves KC, Wallace M, Schlesinger R, O’Quinn M, et al. Differences in placental telomere length suggest a link between racial disparities in birth outcomes and cellular aging. Am J Obstet Gynecol. 2017;216(3):294. e1–8.CrossRef
37.
go back to reference Beck AT, Steer RA, Brown GK. Beck depression inventory-II. San Antonio; 1996. p. 78204–2498. Beck AT, Steer RA, Brown GK. Beck depression inventory-II. San Antonio; 1996. p. 78204–2498.
38.
go back to reference Achenbach TM, Edelbrock CS. Manual for the child behavior checklist: and revised child behavior profile: University of Vermont, Department of Psychiatry; 1983. Achenbach TM, Edelbrock CS. Manual for the child behavior checklist: and revised child behavior profile: University of Vermont, Department of Psychiatry; 1983.
39.
go back to reference Cawthon RM. Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res. 2009;37(3):e21-e.CrossRef Cawthon RM. Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res. 2009;37(3):e21-e.CrossRef
40.
go back to reference Esteves KC, Jones CW, Wade M, Callerame K, Smith AK, Theall KP, et al. Adverse childhood experiences: implications for offspring telomere length and psychopathology. Am J Psychiatry. 2020;177(1):47–57.CrossRef Esteves KC, Jones CW, Wade M, Callerame K, Smith AK, Theall KP, et al. Adverse childhood experiences: implications for offspring telomere length and psychopathology. Am J Psychiatry. 2020;177(1):47–57.CrossRef
41.
go back to reference Lindrose AR, McLester-Davis LWY, Tristano RI, Kataria L, Gadalla SM, Eisenberg DTA, et al. Method comparison studies of telomere length measurement using qPCR approaches: a critical appraisal of the literature. bioRxiv. 2020:2020.09.04.282632. Lindrose AR, McLester-Davis LWY, Tristano RI, Kataria L, Gadalla SM, Eisenberg DTA, et al. Method comparison studies of telomere length measurement using qPCR approaches: a critical appraisal of the literature. bioRxiv. 2020:2020.09.04.282632.
42.
go back to reference Graham JW. Missing data analysis: making it work in the real world. Annu Rev Psychol. 2009;60:549–76.CrossRef Graham JW. Missing data analysis: making it work in the real world. Annu Rev Psychol. 2009;60:549–76.CrossRef
43.
go back to reference Whiteman VE, Goswami A, Salihu HM. Telomere length and fetal programming: a review of recent scientific advances. Am J Reprod Immunol (New York, NY : 1989). 2017;77(5). Whiteman VE, Goswami A, Salihu HM. Telomere length and fetal programming: a review of recent scientific advances. Am J Reprod Immunol (New York, NY : 1989). 2017;77(5).
44.
go back to reference Caporaso GL, Chao MV. Telomerase and oligodendrocyte differentiation. J Neurobiol. 2001;49(3):224–34.CrossRef Caporaso GL, Chao MV. Telomerase and oligodendrocyte differentiation. J Neurobiol. 2001;49(3):224–34.CrossRef
45.
go back to reference Uzun Cicek AA-O, Mercan Isik CA-O, Bakir SA-O, Ulger DA-OX, Sari SA-O, Bakir DA-O, et al. Evidence supporting the role of telomerase, MMP-9, and SIRT1 in attention-deficit/hyperactivity disorder (ADHD). (1435-1463 (Electronic)). Uzun Cicek AA-O, Mercan Isik CA-O, Bakir SA-O, Ulger DA-OX, Sari SA-O, Bakir DA-O, et al. Evidence supporting the role of telomerase, MMP-9, and SIRT1 in attention-deficit/hyperactivity disorder (ADHD). (1435-1463 (Electronic)).
46.
go back to reference Eisenberg DTA. Telomere length measurement validity: the coefficient of variation is invalid and cannot be used to compare quantitative polymerase chain reaction and Southern blot telomere length measurement techniques. Int J Epidemiol. 2016;45(4):1295–8.PubMed Eisenberg DTA. Telomere length measurement validity: the coefficient of variation is invalid and cannot be used to compare quantitative polymerase chain reaction and Southern blot telomere length measurement techniques. Int J Epidemiol. 2016;45(4):1295–8.PubMed
47.
go back to reference McEvoy CT, Spindel ER. Pulmonary effects of maternal smoking on the fetus and child: effects on lung development, respiratory morbidities, and life long lung health. Paediatr Respir Rev. 2017;21:27–33.PubMed McEvoy CT, Spindel ER. Pulmonary effects of maternal smoking on the fetus and child: effects on lung development, respiratory morbidities, and life long lung health. Paediatr Respir Rev. 2017;21:27–33.PubMed
48.
go back to reference Neuman A, Hohmann C, Orsini N, Pershagen G, Eller E, Kjaer HF, et al. Maternal smoking in pregnancy and asthma in preschool children: a pooled analysis of eight birth cohorts. Am J Respir Crit Care Med. 2012;186(10):1037–43.CrossRef Neuman A, Hohmann C, Orsini N, Pershagen G, Eller E, Kjaer HF, et al. Maternal smoking in pregnancy and asthma in preschool children: a pooled analysis of eight birth cohorts. Am J Respir Crit Care Med. 2012;186(10):1037–43.CrossRef
49.
go back to reference Cui M, Kimura T, Ikehara S, Dong JY, Ueda K, Kawanishi Y, et al. Prenatal tobacco smoking is associated with postpartum depression in Japanese pregnant women: the Japan Environment and Children’s Study. (1573-2517 (Electronic)). Cui M, Kimura T, Ikehara S, Dong JY, Ueda K, Kawanishi Y, et al. Prenatal tobacco smoking is associated with postpartum depression in Japanese pregnant women: the Japan Environment and Children’s Study. (1573-2517 (Electronic)).
50.
go back to reference Smedberg J, Lupattelli A, Mårdby A-C, Øverland S, Nordeng H. The relationship between maternal depression and smoking cessation during pregnancy—a cross-sectional study of pregnant women from 15 European countries. Arch Womens Ment Health. 2015;18(1):73–84.CrossRef Smedberg J, Lupattelli A, Mårdby A-C, Øverland S, Nordeng H. The relationship between maternal depression and smoking cessation during pregnancy—a cross-sectional study of pregnant women from 15 European countries. Arch Womens Ment Health. 2015;18(1):73–84.CrossRef
51.
go back to reference Cheung K, Aberdeen K, Ward MA, Theule J. Maternal depression in families of children with ADHD: a meta-analysis. J Child Fam Stud. 2018;27(4):1015–28.CrossRef Cheung K, Aberdeen K, Ward MA, Theule J. Maternal depression in families of children with ADHD: a meta-analysis. J Child Fam Stud. 2018;27(4):1015–28.CrossRef
52.
go back to reference Loukola A, Hällfors J, Korhonen T, Kaprio J. Genetics and smoking. Curr Addict Rep. 2014;1(1):75–82.CrossRef Loukola A, Hällfors J, Korhonen T, Kaprio J. Genetics and smoking. Curr Addict Rep. 2014;1(1):75–82.CrossRef
53.
go back to reference Broer L, Codd V, Nyholt DR, Deelen J, Mangino M, Willemsen G, et al. Meta-analysis of telomere length in 19,713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur J Hum Genet. 2013;21(10):1163–8.CrossRef Broer L, Codd V, Nyholt DR, Deelen J, Mangino M, Willemsen G, et al. Meta-analysis of telomere length in 19,713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur J Hum Genet. 2013;21(10):1163–8.CrossRef
54.
go back to reference Jaddoe VW, Troe EJW, Hofman A, Mackenbach JP, Moll HA, Steegers EA, et al. Active and passive maternal smoking during pregnancy and the risks of low birthweight and preterm birth: the Generation R Study. Paediatr Perinat Epidemiol. 2008;22(2):162–71.CrossRef Jaddoe VW, Troe EJW, Hofman A, Mackenbach JP, Moll HA, Steegers EA, et al. Active and passive maternal smoking during pregnancy and the risks of low birthweight and preterm birth: the Generation R Study. Paediatr Perinat Epidemiol. 2008;22(2):162–71.CrossRef
Metadata
Title
Impact of prenatal tobacco smoking on infant telomere length trajectory and ADHD symptoms at 18 months: a longitudinal cohort study
Authors
Meghan P. Howell
Christopher W. Jones
Cade A. Herman
Celia V. Mayne
Camilo Fernandez
Katherine P. Theall
Kyle C. Esteves
Stacy S. Drury
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2022
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-022-02340-1

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