Prenatal glucocorticoids and maternal smoking during pregnancy independently program adult nicotine dependence in daughters: A 40-year prospective study

Laura R. Stroud, George D. Papandonatos, Edmond Shenassa, Daniel Rodriguez, Raymond Niaura, Kaja Z. Lewinn, Lewis P. Lipsitt, Stephen L. Buka

Research output: Contribution to journalArticle

Abstract

Background Maternal smoking during pregnancy (MSDP) is an independent risk factor for offspring nicotine dependence (ND), but mechanisms remain unknown. We investigated prenatal glucocorticoid (cortisol) and androgen (testosterone) associations with offspring ND over 40 years and the possibility that prenatal glucocorticoids and androgens would mediate links between MSDP and offspring ND. Methods Participants were 1086 mother-adult offspring pairs (59% female) from the New England Family Study, a 40-year longitudinal follow-up of the Collaborative Perinatal Project. MSDP was assessed prospectively at each prenatal visit. Maternal cortisol, testosterone, and cotinine (nicotine metabolite) were assayed from third trimester maternal sera. Offspring lifetime ND was assessed via structured interview. Results Significant bivariate associations emerged for: 1) MSDP/cotinine and lifetime ND; and 2) maternal cortisol and lifetime ND, for daughters only. In multivariate models, maternal cortisol and MSDP/cotinine remained significantly and independently associated with increased odds of lifetime ND of daughters. However, cortisol did not mediate the MSDP-lifetime ND relation. No associations emerged between maternal testosterone and offspring ND. Conclusions Results provide the first evidence in support of prenatal glucocorticoid programming of adult ND over 40 years in daughters only. Our study highlights two independent prenatal pathways leading to increased risk for ND in daughters: elevated prenatal glucocorticoids and MSDP/nicotine exposure. Daughter-specific effects of glucocorticoid and MSDP programming over 40 years highlight the breadth and persistence of sexually dimorphic programming effects in humans. Results do not support androgen programming of offspring ND.

Original languageEnglish (US)
Pages (from-to)47-55
Number of pages9
JournalBiological Psychiatry
Volume75
Issue number1
DOIs
StatePublished - Jan 1 2014

Fingerprint

Tobacco Use Disorder
Glucocorticoids
Smoking
Mothers
Prospective Studies
Pregnancy
Hydrocortisone
Cotinine
Androgens
Testosterone
Nicotine
Embryonic and Fetal Development
New England
Third Pregnancy Trimester

Keywords

  • Androgen
  • cortisol
  • cotinine
  • glucocorticoid
  • maternal smoking during pregnancy
  • nicotine dependence
  • programming
  • testosterone

ASJC Scopus subject areas

  • Biological Psychiatry

Cite this

Prenatal glucocorticoids and maternal smoking during pregnancy independently program adult nicotine dependence in daughters : A 40-year prospective study. / Stroud, Laura R.; Papandonatos, George D.; Shenassa, Edmond; Rodriguez, Daniel; Niaura, Raymond; Lewinn, Kaja Z.; Lipsitt, Lewis P.; Buka, Stephen L.

In: Biological Psychiatry, Vol. 75, No. 1, 01.01.2014, p. 47-55.

Research output: Contribution to journalArticle

Stroud, Laura R. ; Papandonatos, George D. ; Shenassa, Edmond ; Rodriguez, Daniel ; Niaura, Raymond ; Lewinn, Kaja Z. ; Lipsitt, Lewis P. ; Buka, Stephen L. / Prenatal glucocorticoids and maternal smoking during pregnancy independently program adult nicotine dependence in daughters : A 40-year prospective study. In: Biological Psychiatry. 2014 ; Vol. 75, No. 1. pp. 47-55.
@article{bd3209c677a14a469d37c0140ab0a4fe,
title = "Prenatal glucocorticoids and maternal smoking during pregnancy independently program adult nicotine dependence in daughters: A 40-year prospective study",
abstract = "Background Maternal smoking during pregnancy (MSDP) is an independent risk factor for offspring nicotine dependence (ND), but mechanisms remain unknown. We investigated prenatal glucocorticoid (cortisol) and androgen (testosterone) associations with offspring ND over 40 years and the possibility that prenatal glucocorticoids and androgens would mediate links between MSDP and offspring ND. Methods Participants were 1086 mother-adult offspring pairs (59{\%} female) from the New England Family Study, a 40-year longitudinal follow-up of the Collaborative Perinatal Project. MSDP was assessed prospectively at each prenatal visit. Maternal cortisol, testosterone, and cotinine (nicotine metabolite) were assayed from third trimester maternal sera. Offspring lifetime ND was assessed via structured interview. Results Significant bivariate associations emerged for: 1) MSDP/cotinine and lifetime ND; and 2) maternal cortisol and lifetime ND, for daughters only. In multivariate models, maternal cortisol and MSDP/cotinine remained significantly and independently associated with increased odds of lifetime ND of daughters. However, cortisol did not mediate the MSDP-lifetime ND relation. No associations emerged between maternal testosterone and offspring ND. Conclusions Results provide the first evidence in support of prenatal glucocorticoid programming of adult ND over 40 years in daughters only. Our study highlights two independent prenatal pathways leading to increased risk for ND in daughters: elevated prenatal glucocorticoids and MSDP/nicotine exposure. Daughter-specific effects of glucocorticoid and MSDP programming over 40 years highlight the breadth and persistence of sexually dimorphic programming effects in humans. Results do not support androgen programming of offspring ND.",
keywords = "Androgen, cortisol, cotinine, glucocorticoid, maternal smoking during pregnancy, nicotine dependence, programming, testosterone",
author = "Stroud, {Laura R.} and Papandonatos, {George D.} and Edmond Shenassa and Daniel Rodriguez and Raymond Niaura and Lewinn, {Kaja Z.} and Lipsitt, {Lewis P.} and Buka, {Stephen L.}",
year = "2014",
month = "1",
day = "1",
doi = "10.1016/j.biopsych.2013.07.024",
language = "English (US)",
volume = "75",
pages = "47--55",
journal = "Biological Psychiatry",
issn = "0006-3223",
publisher = "Elsevier USA",
number = "1",

}

TY - JOUR

T1 - Prenatal glucocorticoids and maternal smoking during pregnancy independently program adult nicotine dependence in daughters

T2 - A 40-year prospective study

AU - Stroud, Laura R.

AU - Papandonatos, George D.

AU - Shenassa, Edmond

AU - Rodriguez, Daniel

AU - Niaura, Raymond

AU - Lewinn, Kaja Z.

AU - Lipsitt, Lewis P.

AU - Buka, Stephen L.

PY - 2014/1/1

Y1 - 2014/1/1

N2 - Background Maternal smoking during pregnancy (MSDP) is an independent risk factor for offspring nicotine dependence (ND), but mechanisms remain unknown. We investigated prenatal glucocorticoid (cortisol) and androgen (testosterone) associations with offspring ND over 40 years and the possibility that prenatal glucocorticoids and androgens would mediate links between MSDP and offspring ND. Methods Participants were 1086 mother-adult offspring pairs (59% female) from the New England Family Study, a 40-year longitudinal follow-up of the Collaborative Perinatal Project. MSDP was assessed prospectively at each prenatal visit. Maternal cortisol, testosterone, and cotinine (nicotine metabolite) were assayed from third trimester maternal sera. Offspring lifetime ND was assessed via structured interview. Results Significant bivariate associations emerged for: 1) MSDP/cotinine and lifetime ND; and 2) maternal cortisol and lifetime ND, for daughters only. In multivariate models, maternal cortisol and MSDP/cotinine remained significantly and independently associated with increased odds of lifetime ND of daughters. However, cortisol did not mediate the MSDP-lifetime ND relation. No associations emerged between maternal testosterone and offspring ND. Conclusions Results provide the first evidence in support of prenatal glucocorticoid programming of adult ND over 40 years in daughters only. Our study highlights two independent prenatal pathways leading to increased risk for ND in daughters: elevated prenatal glucocorticoids and MSDP/nicotine exposure. Daughter-specific effects of glucocorticoid and MSDP programming over 40 years highlight the breadth and persistence of sexually dimorphic programming effects in humans. Results do not support androgen programming of offspring ND.

AB - Background Maternal smoking during pregnancy (MSDP) is an independent risk factor for offspring nicotine dependence (ND), but mechanisms remain unknown. We investigated prenatal glucocorticoid (cortisol) and androgen (testosterone) associations with offspring ND over 40 years and the possibility that prenatal glucocorticoids and androgens would mediate links between MSDP and offspring ND. Methods Participants were 1086 mother-adult offspring pairs (59% female) from the New England Family Study, a 40-year longitudinal follow-up of the Collaborative Perinatal Project. MSDP was assessed prospectively at each prenatal visit. Maternal cortisol, testosterone, and cotinine (nicotine metabolite) were assayed from third trimester maternal sera. Offspring lifetime ND was assessed via structured interview. Results Significant bivariate associations emerged for: 1) MSDP/cotinine and lifetime ND; and 2) maternal cortisol and lifetime ND, for daughters only. In multivariate models, maternal cortisol and MSDP/cotinine remained significantly and independently associated with increased odds of lifetime ND of daughters. However, cortisol did not mediate the MSDP-lifetime ND relation. No associations emerged between maternal testosterone and offspring ND. Conclusions Results provide the first evidence in support of prenatal glucocorticoid programming of adult ND over 40 years in daughters only. Our study highlights two independent prenatal pathways leading to increased risk for ND in daughters: elevated prenatal glucocorticoids and MSDP/nicotine exposure. Daughter-specific effects of glucocorticoid and MSDP programming over 40 years highlight the breadth and persistence of sexually dimorphic programming effects in humans. Results do not support androgen programming of offspring ND.

KW - Androgen

KW - cortisol

KW - cotinine

KW - glucocorticoid

KW - maternal smoking during pregnancy

KW - nicotine dependence

KW - programming

KW - testosterone

UR - http://www.scopus.com/inward/record.url?scp=84889562306&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84889562306&partnerID=8YFLogxK

U2 - 10.1016/j.biopsych.2013.07.024

DO - 10.1016/j.biopsych.2013.07.024

M3 - Article

C2 - 24034414

AN - SCOPUS:84889562306

VL - 75

SP - 47

EP - 55

JO - Biological Psychiatry

JF - Biological Psychiatry

SN - 0006-3223

IS - 1

ER -