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Is maternal smoking during pregnancy a causal environmental risk factor for adolescent antisocial behavior? Testing etiological theories and assumptions

Published online by Cambridge University Press:  16 November 2011

B. M. D'Onofrio*
Affiliation:
Indiana University, Bloomington, IN, USA
C. A. Van Hulle
Affiliation:
University of Wisconsin-Madison, Madison, WI, USA
J. A. Goodnight
Affiliation:
University of Dayton, Dayton, OH, USA
P. J. Rathouz
Affiliation:
University of Wisconsin-Madison, Madison, WI, USA
B. B. Lahey
Affiliation:
University of Chicago, Chicago, IL, USA
*
*Address for correspondence: B. M. D'Onofrio, Ph.D., Department of Psychological and Brain Sciences, Indiana University, 1101 East 10th Street, Bloomington, IN 47405, USA. (Email: bmdonofr@indiana.edu)

Abstract

Background

Although many studies indicate that maternal smoking during pregnancy (SDP) is correlated with later offspring antisocial behavior (ASB), recent quasi-experimental studies suggest that background familial factors confound the association. The present study sought to test alternative etiological hypotheses using multiple indices of adolescent ASB, comparing differentially exposed siblings, and testing assumptions in the sibling-comparison design.

Method

The study examined the association between maternal SDP and adolescent-reported ASB, criminal convictions and membership in a group of individuals with early-starting and chronic ASB among 6066 offspring of women from the National Longitudinal Survey of Youth, a representative sample of women in the USA. The analyses controlled for statistical covariates and examined associations while comparing differentially exposed siblings.

Results

At the population level, each additional pack of cigarettes per day predicted greater mean adolescent-reported ASB symptoms [ratio of means 1.15, 95% confidence interval (CI) 1.08–1.22], odds of being in the top 10% of ASB [odds ratio (OR) 1.34, 95% CI 1.10–1.65], hazard of a criminal conviction [hazard ratio (HR) 1.51, 95% CI 1.34–1.68] and odds of chronic ASB (OR 1.57, 95% CI 1.25–1.99). SDP robustly predicted most assessments of ASB while controlling for measured covariates. When siblings exposed to differing levels of SDP were compared, however, all of the associations were attenuated and were not statistically significant: adolescent-reported mean ASB (ratio of means 0.86, 95% CI 0.74–1.01), high ASB (OR 0.67, 95% CI 0.41–1.12), criminal conviction (HR 0.98, 95% CI 0.66–1.44) and chronic ASB (OR 0.80, 95% CI 0.46–1.38).

Conclusions

The results strongly suggest that familial factors account for the correlation between SDP and offspring adolescent ASB, rather than a putative causal environmental influence of SDP.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2011

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References

Achenbach, TM (1978). The Child Behavior Profile: I. Boys aged 6–11. Journal of Consulting and Clinical Psychology 46, 478488.CrossRefGoogle ScholarPubMed
Allison, PD (2009). Fixed Effects Regression Models. Sage: Washington, DC.CrossRefGoogle Scholar
Baker, P, Mott, FL (1989). NLSY Child Handbook. Center for Human Resource Research: Columbus, OH.Google Scholar
Barker, ED, Maughan, B (2009). Differentiating early-onset versus childhood-limited conduct problem youth. American Journal of Psychiatry 166, 900908.CrossRefGoogle ScholarPubMed
Batty, GD, Der, G, Deary, IJ (2006). Effect of maternal smoking during pregnancy on offspring's cognitive ability: empirical evidence for complete confounding in the US National Longitudinal Survey of Youth. Pediatrics 118, 943950.CrossRefGoogle ScholarPubMed
Boutwell, BB, Beaver, KM (2010). Maternal cigarette smoking during pregnancy and offspring externalizing behavioral problems: a propensity score matching analysis. International Journal of Environmental Research and Public Health 7, 146163.CrossRefGoogle ScholarPubMed
Brennan, PA, Grekin, ER, Mednick, SA (1999). Maternal smoking during pregnancy and adult male criminal outcomes. Archives of General Psychiatry 56, 215219.CrossRefGoogle ScholarPubMed
Brion, MJ, Victora, C, Matijasevich, A, Horta, B, Anselmi, L, Steer, C, Menezes, AMB, Lawlor, DA, Smith, GD (2010). Maternal smoking and child psychological problems: disentangling causal and noncausal effects. Pediatrics 126, e57e65.CrossRefGoogle ScholarPubMed
Chase-Lansdale, PL, Mott, FL, Brooks-Gunn, J, Phillips, DA (1991). Children of the National Longitudinal Survey of Youth: a unique research opportunity. Developmental Psychology 27, 918931.CrossRefGoogle Scholar
Cnattingius, S (2004). The epidemiology of smoking during pregnancy: smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine and Tobacco Research 6, S125S140.CrossRefGoogle ScholarPubMed
D'Onofrio, BM, Rathouz, PJ, Lahey, BB (2011). The importance of understanding gene–environment correlations in the development of antisocial behavior. In The Dynamic Genome and Mental Health: The Role of Genes and Environments in Youth Development (ed. Kendler, K. S., Jaffee, S. R. and Romer, D.), pp. 340364. Oxford University Press: NewYork.Google Scholar
D'Onofrio, BM, Singh, AL, Iliadou, A, Lambe, M, Hultman, C, Grann, M, Neiderhiser, JM, Långström, N, Lichtenstein, P (2010 a). Familial confounding of the association between maternal smoking during pregnancy and offspring criminality: a population-based study in Sweden. Archives of General Psychiatry 67, 529538.CrossRefGoogle ScholarPubMed
D'Onofrio, BM, Singh, AL, Iliadou, A, Lambe, M, Hultman, C, Neiderhiser, JM, Långström, N, Lichtenstein, P (2010 b). A quasi-experimental study of maternal smoking during pregnancy and offspring academic achievement. Child Development 81, 80–100.CrossRefGoogle ScholarPubMed
D'Onofrio, BM, Van Hulle, CA, Waldman, ID, Rodgers, JL, Harden, KP, Rathouz, PJ, Rathouz, PJ, Lahey, BB (2008). Smoking during pregnancy and offspring externalizing problems: an exploration of genetic and environmental confounds. Development and Psychopathology 20, 139164.CrossRefGoogle ScholarPubMed
D'Onofrio, BM, Van Hulle, CA, Waldman, ID, Rodgers, JL, Rathouz, PJ, Lahey, BB (2007). Causal inferences regarding prenatal alcohol exposure and childhood externalizing problems. Archives of General Psychiatry 64, 12961304.CrossRefGoogle ScholarPubMed
Day, NL, Goldschmid, L, Robles, N, Richardson, G, Cornelius, M, Taylor, P, Geva, D, Stoffer, D (1991). Prenatal alcohol exposure and offspring growth at 18 months of age: the predictive validity of two measures of drinking. Alcoholism, Clinical and Experimental Research 15, 914918.CrossRefGoogle ScholarPubMed
Derauf, C, Kekatpure, M, Neyzi, N, Lester, B, Kosofsky, B (2009). Neuroimaging of children following prenatal drug exposure. Seminars in Cell and Developmental Biology 20, 441454.CrossRefGoogle ScholarPubMed
Donovan, SJ, Susser, E (2011). Commentary: advent of sibling designs. International Journal of Epidemiology 40, 345349.CrossRefGoogle ScholarPubMed
Elliott, DS, Huizinga, D (1983). Social class and delinquent behavior in a national youth panel. Criminology: An Interdisciplinary Journal 21, 149177.CrossRefGoogle Scholar
Ernst, M, Moolchan, ET, Robinson, ML (2001). Behavioral and neural consequences of prenatal exposure to nicotine. Journal of the American Academy of Child and Adolescent Psychiatry 40, 630641.CrossRefGoogle ScholarPubMed
Federal Bureau of Investigation (FBI) (2011). Uniform Crime Reports as prepared by the National Archive of Criminal Justice Data (http://www.fbi.gov/about-us/cjis/ucr/). Accessed 12 August 2011.Google Scholar
Fergusson, DM, Horwood, LJ (2002). Male and female offending trajectories. Development and Psychopathology 14, 159177.CrossRefGoogle ScholarPubMed
George, L, Granath, F, Johansson, ALV, Cnattingius, S (2006). Self-reported nicotine exposure and plasma levels of cotinine in early and late pregnancy. Acta Obstetrica et Gynecologia Scandinavica 85, 13311337.CrossRefGoogle ScholarPubMed
Gilman, SE, Gardener, H, Buka, SL (2008). Maternal smoking during pregnancy and children's cognitive and physical development: a causal risk factor? American Journal of Epidemiology 168, 522531.CrossRefGoogle ScholarPubMed
Gold, AB, Keller, AB, Perry, DC (2009). Prenatal exposure of rats to nicotine causes persistent alterations of nicotinic cholinergic receptors. Brain Research 1250, 88–100.CrossRefGoogle ScholarPubMed
Heath, AC, Kessler, RC, Neale, MC, Hewitt, JK, Eaves, LJ, Kendler, KS (1993). Testing hypotheses about direction of causation using cross-sectional data. Behavior Genetics 23, 2950.CrossRefGoogle Scholar
Huizink, AC (2009). Moderate use of alcohol, tobacco and cannabis during pregnancy: new approaches and update on research findings. Reproductive Toxicology 28, 143151.CrossRefGoogle ScholarPubMed
Johansson, ALV, Dickman, PW, Kramer, MS, Cnattingius, S (2009). Maternal smoking and infant mortality: does quitting smoking reduce the risk of infant death? Epidemiology 20, 590597.CrossRefGoogle ScholarPubMed
Knopik, VS (2009). Maternal smoking during pregnancy and child outcomes: real or spurious effect? Developmental Neuropsychology 34, 136.CrossRefGoogle ScholarPubMed
Kuja-Halkola, R, D'Onofrio, BM, Iliadou, AN, Langstrom, N, Lichtenstein, P (2010). Prenatal smoking exposure and offspring stress coping in late adolescence: no causal link. International Journal of Epidemiology 39, 15311540.CrossRefGoogle ScholarPubMed
Lahey, BB, D'Onofrio, BM (2010). All in the family: comparing siblings to test causal hypotheses regarding environmental influences on behavior. Current Directions in Psychological Science 19, 319323.CrossRefGoogle ScholarPubMed
Lahey, BB, Van Hulle, CA, D'Onofrio, BM, Rodgers, JL, Waldman, ID (2008). Is parental knowledge of their adolescent offspring's whereabouts and peer associations spuriously associated with offspring delinquency? Journal of Abnormal Child Psychology 36, 807823.CrossRefGoogle ScholarPubMed
Lambe, M, Hultman, C, Torrang, A, MacCabe, J, Cnattingius, S (2006). Maternal smoking during pregnancy and school performance at age 15. Epidemiology 17, 524530.CrossRefGoogle ScholarPubMed
Lavigne, JV, Hopkins, J, Gouze, KR, Bryant, FB, LeBailly, SA, Binns, HJ, Lavigne, PM (2011). Is smoking during pregnancy a risk factor for psychopathology in young children? A methodological caveat and report on preschoolers. Journal of Pediatric Psychology 36, 1024.CrossRefGoogle ScholarPubMed
Leve, LD, Neiderhiser, JM, Scaramella, LV, Reiss, D (2010). The Early Growth and Development study: using the prospective adoption design to examine genotype–environment interplay. Behavior Genetics 40, 306314.CrossRefGoogle ScholarPubMed
Lindblad, F, Hjern, A (2010). ADHD after fetal exposure to maternal smoking. Nicotine and Tobacco Research 12, 408415.CrossRefGoogle ScholarPubMed
Loeber, R, Farrington, DP, Stouthamer-Loeber, M, Van Kammen, W (1998). Antisocial Behavior and Mental Health Problems: Explanatory Factors in Childhood and Adolescence. Lawrence Erlbaum: Mahwah, NJ.CrossRefGoogle Scholar
Long, JS (1997). Regression Models for Categorical and limited Dependent Variables. Sage: New York.Google Scholar
Lundberg, F, Cnattingius, S, D'Onofrio, B, Altman, D, Lambe, M, Hultman, C, Iliadou, A (2010). Maternal smoking during pregnancy and intellectual performance in young adult Swedish male offspring. Pediatric and Perinatal Epidemiology 24, 7987.CrossRefGoogle ScholarPubMed
Meyer, KA, Williams, P, Hernandez-Diaz, S, Cnattingius, S (2004). Smoking and risk of oral clefts: exploring the impact of study designs. Epidemiology 15, 671678.CrossRefGoogle ScholarPubMed
Mitchell, BF, Taggert, MJ (2009). Are animal models relevant to key aspects of human parturition? American Journal of Physiology Regulatory, Integrative and Comparative Physiology 297, R525R545.CrossRefGoogle ScholarPubMed
Moffitt, TE (2006). Life-course persistent and adolescence-limited antisocial behavior. In Developmental Psychopathology, 2nd edn (ed. Cicchetti, D. and Cohen, D.), pp. 570598. Wiley: New York.Google Scholar
Moffitt, TE, Caspi, A, Rutter, M, Silva, PA (2001). Sex Differences in Antisocial Behaviour: Conduct Disorder, Delinquency, and Violence in the Dunedin Longitudinal Study. Cambridge University Press: New York.CrossRefGoogle Scholar
Muthén, LK, Muthén, BO (1998–2010). Mplus User's Guide, 6th edn. Muthén and Muthén: Los Angeles.Google Scholar
Obel, C, Olsen, J, Henriksen, TB, Rodriguez, A, Järvelin, MR, Moilanen, I, Parner, E, Linnet, KM, Taanila, A, Ebeling, H, Heiervang, E, Gissler, M (2011). Is maternal smoking during pregnancy a risk factor for Hyperkinetic disorder? – findings from a sibling design. International Journal of Epidemiology 40, 338345.CrossRefGoogle ScholarPubMed
Odgers, CL, Moffitt, TE, Broadbent, JM, Dickson, N, Hancox, RJ, Harrington, HL, Poulton, R, Sears, MR, Thomson, WM, Caspi, A (2008). Female and male antisocial trajectories: from childhood origins to adult outcomes. Development and Psychopathology 20, 673716.CrossRefGoogle ScholarPubMed
Olds, D (1997). Tobacco exposure and impaired development: a review of the evidence. Mental Retardation and Developmental Disabilities Research Reviews 3, 257269.3.0.CO;2-M>CrossRefGoogle Scholar
Paradis, AD, Fitzmaurice, GM, Koenen, KC, Buka, SL (2010). Maternal smoking during pregnancy and criminal offending among adult offspring. Journal of Epidemiology and Community Health. Published online 15 November 2010. doi:2010;jech.2009.095802.Google ScholarPubMed
Post, A, Gilljam, H, Bremberg, S, Galanti, MR (2008). Maternal smoking during pregnancy: a comparison between concurrent and retrospective self-reports. Paediatric and Perinatal Epidemiology 22, 155161.CrossRefGoogle ScholarPubMed
Rice, F, Harold, GT, Boivin, J, Hay, DF, Van den Bree, M, Thapar, A (2009). Disentangling prenatal and inherited influences in humans with an experimental design. Proceedings of the National Academy of Sciences USA 106, 24642467.CrossRefGoogle ScholarPubMed
Rodgers, JL, Rowe, DC, Li, C (1994). Beyond nature vs. nurture: DF analyses of nonshared influences on problem behaviors. Developmental Psychology 30, 374384.CrossRefGoogle Scholar
Roza, SJ, Verhulst, FC, Jaddoe, VWV, Steegers, EAP, Mackenbach, JP, Hofman, A, Tiemeier, H (2009). Maternal smoking during pregnancy and child behaviour problems: the Generation R Study. International Journal of Epidemiology 38, 680689.CrossRefGoogle ScholarPubMed
Rubin, DB (2006). Matched Sampling for Causal Effects. Cambridge University Press: Cambridge.CrossRefGoogle Scholar
Rutter, M (2007). Proceeding from observed correlation to causal inference: the use of natural experiments. Perspectives on Psychological Science 2, 377395.CrossRefGoogle ScholarPubMed
Rutter, M, Pickles, A, Murray, R, Eaves, LJ (2001). Testing hypotheses on specific environmental causal effects on behavior. Psychological Bulletin 127, 291324.CrossRefGoogle ScholarPubMed
Shadish, WR, Cook, TD, Campbell, DT (2002). Experimental and Quasi-Experimental Designs for Generalized Causal Inference. Houghton Mifflin: New York.Google Scholar
Talati, A, Weissman, MM (2010). In utero smoking exposure warrants further investigation. Archives of General Psychiatry 67, 1094.CrossRefGoogle ScholarPubMed
Thapar, A, Harold, G, Rice, F, Ge, X, Boivin, J, Hay, D, van den Bree, M, Lewis, A (2007). Do intrauterine or genetic influences explain the foetal origins of chronic disease? A novel experimental method for disentangling effects. BMC Medical Research Methodology 7, 25.CrossRefGoogle ScholarPubMed
Thapar, A, Rice, F, Hay, D, Boivin, J, Langley, K, Van den Bree, M, Rutter, M, Harold, G (2009). Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biological Psychiatry 66, 722727.CrossRefGoogle Scholar
Wakschlag, LS, Pickett, KE, Cook, E, Benowitz, NL, Leventhal, BL (2002). Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review. American Journal of Public Health 92, 966974.CrossRefGoogle ScholarPubMed