Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T13:17:13.012Z Has data issue: false hasContentIssue false
  • English
  • Français

Prenatal smoking and childhood behavior problems: is the association mediated by birth weight?

Published online by Cambridge University Press:  16 February 2016

S. E. Parker ,
B. R. Collett ,
M. L. Speltz  and
M. M. Werler
S. E. Parker*
Affiliation:
Department of Epidemiology, Boston University School of Public Health, Boston, MA, USA
B. R. Collett
Affiliation:
Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, WA, USA
M. L. Speltz
Affiliation:
Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, WA, USA
M. M. Werler
Affiliation:
Department of Epidemiology, Boston University School of Public Health, Boston, MA, USA
*
*Address for correspondence: S. E. Parker, Department of Epidemiology, Boston University School of Public Health, 715 Albany Street, Boston, MA 02118, USA. (Email separker@bu.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Maternal smoking during pregnancy is associated with both reduced birth weight and adverse neurobehavioral outcomes. The aim of this study was to investigate longitudinal associations between maternal smoking during pregnancy and childhood behavioral outcomes, and to determine the role of birth weight in mediating such associations. The study included 489 mother–child pairs. Prenatal exposures were assessed via maternal interviews conducted on average 1 year after delivery and child behavior assessments were completed at 5–12 years of age using the Child Behavior Checklist (CBCL) and Teacher Report Form (TRF). Maternal smoking during pregnancy was associated with externalizing and total behavior problems according to both mother and teacher report. Maternal smoking was also associated with the following percentage increases in scores: 41% (CBCL) and 44% (TRF) for aggressive behavior and 65% (CBCL) and 47% (TRF) for attention problems. Associations with behavior problems were attenuated or no longer observed for mothers that quit smoking in early pregnancy. The proportion of the total effect of maternal smoking on behavioral outcomes explained by differences in birth weight was small and ranged from 6.6% for externalizing behavior on the CBCL to 20.1% for rule-breaking behavior on the CBCL. Our results suggest that birth weight differences explain only a small proportion of the magnitude of association between maternal smoking during pregnancy and selected behavioral outcomes.

Keywords

behavioral problemsbirth weightexternalizing behaviorpregnancysmoking
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 7 , Issue 3: Themed Issue: Ibero-American DOHaD Society , June 2016 , pp. 273 - 281
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Thapar, A, Fowler, T, Rice, F, et al. Maternal smoking during pregnancy and attention deficit hyperactivity disorder symptoms in offspring. Am J Psychiatry. 2003; 160, 1985–1989.CrossRefGoogle ScholarPubMed
2. Batstra, L, Hadders-Algra, M, Neeleman, J. Effect of antenatal exposure to maternal smoking on behavioural problems and academic achievement in childhood: prospective evidence from a Dutch birth cohort. Early Hum Dev. 2003; 75, 21–33.Google Scholar
3. Stene-Larsen, K, Borge, AI, Vollrath, ME. Maternal smoking in pregnancy and externalizing behavior in 18-month-old children: results from a population-based prospective study. J Am Acad Child Adolesc Psychiatry. 2009; 48, 283–289.CrossRefGoogle ScholarPubMed
4. Orlebeke, JF, Knol, DL, Verhulst, FC. Child behavior problems increased by maternal smoking during pregnancy. Arch Environ Health. 1999; 54, 15–19.Google Scholar
5. Kotimaa, AJ, Moilanen, I, Taanila, A, et al. Maternal smoking and hyperactivity in 8-year-old children. J Am Acad Child Adolesc Psychiatry. 2003; 42, 826–833.Google Scholar
6. Brook, DW, Zhang, C, Rosenberg, G, et al. Maternal cigarette smoking during pregnancy and child aggressive behavior. Am J Addict. 2006; 15, 450–456.CrossRefGoogle ScholarPubMed
7. Braun, JM, Froehlich, TE, Daniels, JL, et al. Association of environmental toxicants and conduct disorder in U.S. children: NHANES 2001–2004. Environ Health Perspect. 2008; 116, 956–962.Google Scholar
8. Paradis, AD, Fitzmaurice, GM, Koenen, KC, et al. Maternal smoking during pregnancy and criminal offending among adult offspring. J Epidemiol Community Health. 2011; 65, 1145–1150.Google Scholar
9. Rantakallio, P, Laara, E, Isohanni, M, et al. Maternal smoking during pregnancy and delinquency of the offspring: an association without causation? Int J Epidemiol. 1992; 21, 1106–1113.CrossRefGoogle ScholarPubMed
10. Cornelius, MD, De Genna, NM, Leech, SL, et al. Effects of prenatal cigarette smoke exposure on neurobehavioral outcomes in 10-year-old children of adolescent mothers. Neurotoxicol Teratol. 2011; 33, 137–144.CrossRefGoogle ScholarPubMed
11. Steyn, K, de Wet, T, Saloojee, Y, et al. The influence of maternal cigarette smoking, snuff use and passive smoking on pregnancy outcomes: the Birth To Ten Study. Paediatr Perinat Epidemiol. 2006; 20, 90–99.CrossRefGoogle ScholarPubMed
12. Bernstein, IM, Plociennik, K, Stahle, S, et al. Impact of maternal cigarette smoking on fetal growth and body composition. Am J Obstet Gynecol. 2000; 183, 883–886.Google Scholar
13. Dietz, PM, England, LJ, Shapiro-Mendoza, CK, et al. Infant morbidity and mortality attributable to prenatal smoking in the U.S. Am J Prev Med. 2010; 39, 45–52.CrossRefGoogle ScholarPubMed
14. Kelly, YJ, Nazroo, JY, McMunn, A, et al. Birthweight and behavioural problems in children: a modifiable effect? Int J Epidemiol. 2001; 30, 88–94.Google Scholar
15. Mick, E, Biederman, J, Prince, J, et al. Impact of low birth weight on attention-deficit hyperactivity disorder. J Dev Behav Pediatr. 2002; 23, 16–22.CrossRefGoogle ScholarPubMed
16. Weisglas-Kuperus, N, Koot, HM, Baerts, W, et al. Behaviour problems of very low-birthweight children. Dev Med Child Neurol. 1993; 35, 406–416.Google Scholar
17. Botting, N, Powls, A, Cooke, RW, et al. Attention deficit hyperactivity disorders and other psychiatric outcomes in very low birthweight children at 12 years. J Child Psychol Psychiatry. 1997; 38, 931–941.Google Scholar
18. Wadsby, M, Nelson, N, Ingemansson, F, et al. Behaviour problems and cortisol levels in very-low-birth-weight children. Nord J Psychiatry. 2014; 68, 626–632.CrossRefGoogle ScholarPubMed
19. Herrmann, M, King, K, Weitzman, M. Prenatal tobacco smoke and postnatal secondhand smoke exposure and child neurodevelopment. Curr Opin Pediatr. 2008; 20, 184–190.Google Scholar
20. Nigg, JT, Breslau, N. Prenatal smoking exposure, low birth weight, and disruptive behavior disorders. J Am Acad Child Adolesc Psychiatry. 2007; 46, 362–369.Google Scholar
21. Achenbach, T, Rescorla, L. Manual for the ASEBA School-Age Forms and Profiles, 2001. University of Vermont, Research Center for Children, Youth, and Families: Burlington, VT.Google Scholar
22. Talge, NM, Mudd, LM, Sikorskii, A, et al. United States birth weight reference corrected for implausible gestational age estimates. Pediatrics. 2014; 133, 844–853.Google Scholar
23. Valeri, L, Vanderweele, TJ. Mediation analysis allowing for exposure-mediator interactions and causal interpretation: theoretical assumptions and implementation with SAS and SPSS macros. Psychol Methods. 2013; 18, 137–150.Google Scholar
24. Anthopolos, R, Edwards, SE, Miranda, ML. Effects of maternal prenatal smoking and birth outcomes extending into the normal range on academic performance in fourth grade in North Carolina, USA. Paediatr Perinat Epidemiol. 2013; 27, 564–574.Google Scholar
25. Buschgens, CJ, Swinkels, SH, van Aken, MA, et al. Externalizing behaviors in preadolescents: familial risk to externalizing behaviors, prenatal and perinatal risks, and their interactions. Eur Child Adolesc Psychiatry. 2009; 18, 65–74.CrossRefGoogle ScholarPubMed
26. Slotkin, TA. Fetal nicotine or cocaine exposure: which one is worse? J Pharmacol Exp Ther. 1998; 285, 931–945.Google Scholar
27. Peterson, BS, Vohr, B, Staib, LH, et al. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA. 2000; 284, 1939–1947.CrossRefGoogle ScholarPubMed
28. Makrides, M, Anderson, A, Gibson, RA, et al. Improving the neurodevelopmental outcomes of low-birthweight infants. Nestle Nutr Inst Workshop Ser. 2013; 74, 211–221.Google Scholar
29. Smith, SE, Li, J, Garbett, K, et al. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci. 2007; 27, 10695–10702.CrossRefGoogle ScholarPubMed
30. Eskenazi, B, Trupin, LS. Passive and active maternal smoking during pregnancy, as measured by serum cotinine, and postnatal smoke exposure. II. Effects on neurodevelopment at age 5 years. Am J Epidemiol. 1995; 142(Suppl. 9), S19–S29.Google Scholar
31. Fergusson, DM, Horwood, LJ, Lynskey, MT. Maternal smoking before and after pregnancy: effects on behavioral outcomes in middle childhood. Pediatrics. 1993; 92, 815–822.CrossRefGoogle ScholarPubMed
32. Breslau, N, Chilcoat, HD. Psychiatric sequelae of low birth weight at 11 years of age. Biol Psychiatry. 2000; 47, 1005–1011.CrossRefGoogle Scholar
33. Knopik, VS. Maternal smoking during pregnancy and child outcomes: real or spurious effect? Dev Neuropsychol. 2009; 34, 1–36.Google Scholar
34. Maughan, B, Taylor, A, Caspi, A, et al. Prenatal smoking and early childhood conduct problems: testing genetic and environmental explanations of the association. Arch Gen Psychiatry. 2004; 61, 836–843.Google Scholar
35. Thapar, A, Rice, F, Hay, D, et al. Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biol Psychiatry. 2009; 66, 722–727.Google Scholar
36. Rahu, K, Rahu, M, Pullmann, H, et al. Effect of birth weight, maternal education and prenatal smoking on offspring intelligence at school age. Early Hum Dev. 2010; 86, 493–497.CrossRefGoogle ScholarPubMed
Supplementary material: File

Parker supplementary material

Figures 1-2

Download Parker supplementary material(File)
File 117.1 KB