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Smoking during pregnancy and offspring externalizing problems: An exploration of genetic and environmental confounds

Published online by Cambridge University Press:  23 January 2008

Brian M. D'Onofrio ,
Carol A. van Hulle ,
Irwin D. Waldman ,
Joseph Lee Rodgers ,
K. Paige Harden ,
Paul J. Rathouz  and
Benjamin B. Lahey
Brian M. D'Onofrio*
Affiliation:
Indiana University;
Carol A. van Hulle
Affiliation:
University of Chicago;
Irwin D. Waldman
Affiliation:
Emory University;
Joseph Lee Rodgers
Affiliation:
University of Oklahoma
K. Paige Harden
Affiliation:
University of Virginia
Paul J. Rathouz
Affiliation:
University of Chicago;
Benjamin B. Lahey
Affiliation:
University of Chicago;
*
Address correspondence and reprint requests to: Brian D'Onofrio, Department of Psychological and Brain Sciences, Indiana University, 1101 E. 10th Street, Bloomington, IN 47405; E-mail: [email protected].
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Abstract

Previous studies have documented that smoking during pregnancy (SDP) is associated with offspring externalizing problems, even when measured covariates were used to control for possible confounds. However, the association may be because of nonmeasured environmental and genetic factors that increase risk for offspring externalizing problems. The current project used the National Longitudinal Survey of Youth and their children, ages 4–10 years, to explore the relations between SDP and offspring conduct problems (CPs), oppositional defiant problems (ODPs), and attention-deficit/hyperactivity problems (ADHPs) using methodological and statistical controls for confounds. When offspring were compared to their own siblings who differed in their exposure to prenatal nicotine, there was no effect of SDP on offspring CP and ODP. This suggests that SDP does not have a causal effect on offspring CP and ODP. There was a small association between SDP and ADHP, consistent with a causal effect of SDP, but the magnitude of the association was greatly reduced by methodological and statistical controls. Genetically informed analyses suggest that unmeasured environmental variables influencing both SDP and offspring externalizing behaviors account for the previously observed associations. That is, the current analyses imply that important unidentified environmental factors account for the association between SDP and offspring externalizing problems, not teratogenic effects of SDP.

Type
Research Article
Information
Development and Psychopathology , Volume 20 , Issue 1 , Winter 2008 , pp. 139 - 164
Copyright
Copyright © Cambridge University Press 2008

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Footnotes

This research was supported by Grant R01-MH070025 to Benjamin B. Lahey. We thank Valerie Knopik for her helpful comments on an earlier version of the manuscript.

References

Achenbach, T. M. (1978). The Child Behavior Profile: I. Boys aged 6–11. Journal of Consulting and Clinical Psychology, 46, 478–488.CrossRefGoogle ScholarPubMed
Brennan, P. A., Grekin, E. R., & Mednick, S. A. (1999). Maternal smoking during pregnancy and adult male criminal outcomes. Archives of General Psychiatry, 56, 215–219.CrossRefGoogle ScholarPubMed
Breslau, N., Kilbey, M., & Andreski, P. (1993). Vulnerability to psychopathology in nicotine-dependent smokers: An epidemiologic study of young adults. American Journal of Psychiatry, 150, 941–946.Google ScholarPubMed
Brook, J. S., Brook, D. W., & Whiteman, M. (2000). The influence of maternal smoking during pregnancy on the toddler's negativity. Archives of Pediatric and Adolescent Medicine, 154, 381–385.CrossRefGoogle ScholarPubMed
Button, T. M. M., Thapar, A., & McGuffin, P. (2005). Relationship between antisocial behaviour, attention-deficit hyperactivity disorder and maternal prenatal smoking. British Journal of Psychiatry, 187, 155–160.CrossRefGoogle ScholarPubMed
Chase-Lansdale, P. L., Mott, F. L., Brooks-Gunn, J., & Phillips, D. A. (1991). Children of the National Longitudinal Survey of Youth: A unique research opportunity. Developmental Psychology, 27, 918–931.CrossRefGoogle Scholar
Chatterji, P., & Markowitz, S. (2001). The impact of maternal alcohol and illicit drug use on children's behavior problems: Evidence from the children of the National Longitudinal Survey of Youth. Journal of Health Economics, 20, 703–731.CrossRefGoogle ScholarPubMed
Cnattingius, S. (2004). The epidemiology of smoking during pregnancy: Smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine and Tobacco Research, 6, S125–S140.CrossRefGoogle ScholarPubMed
D'Onofrio, B. M., Turkheimer, E., Eaves, L. J., Corey, L. A., Berg, K., Solaas, M. H., et al. (2003). The role of the Children of Twins design in elucidating causal relations between parent characteristics and child outcomes. Journal of Child Psychology and Psychiatry, 44, 1130–1144.CrossRefGoogle ScholarPubMed
D'Onofrio, B. M., Turkheimer, E. N., Emery, R. E., Slutske, W., Heath, A., Madden, P. A. F., et al. (2005). A genetically informed study of marital instability and its association with offspring psychopathology. Journal of Abnormal Psychology, 114, 570–586.CrossRefGoogle ScholarPubMed
D'Onofrio, B. M., Turkheimer, E. N., Emery, R. E., Slutske, W., Heath, A., Madden, P. A. F., et al. (2006). A genetically informed study of the processes underlying the association between parental marital instability and offspring adjustment. Developmental Psychology, 42, 486–499.CrossRefGoogle ScholarPubMed
Day, N. L., Richardson, G. A., Goldschmidt, L., & Cornelius, M. D. (2000). Effects of prenatal tobacco exposure on preschoolers' behavior. Journal of Developmental and Behavioral Pediatrics, 21, 180–188.Google ScholarPubMed
Eaves, L. J., Silberg, J. L., & Maes, H. H. (2005). Revisiting the children of twins: Can they be used to resolve the environmental effects of dyadic parental treatment on child behavior? Twin Research, 8, 283–290.Google ScholarPubMed
Elliott, D. S., & Huizinga, D. (1983). Social class and delinquent behavior in a national youth panel. Criminology, 21, 149–177.CrossRefGoogle Scholar
Ernst, M. (2001). Behavioral and neural consequences of prental exposure to nicotine. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 630–642.CrossRefGoogle Scholar
Falconer, D. S. (1981). Introduction to quantitative genetics. New York: Longman.Google Scholar
Fergusson, D. M. (1999). Prenatal smoking and antisocial behavior. Archives of General Psychiatry, 56, 223–224.CrossRefGoogle ScholarPubMed
Fergusson, D. M., & Horwood, L. J. (2002). Male and female offending trajectories. Development and Psychopathology, 14, 159–177.CrossRefGoogle ScholarPubMed
Fergusson, D. M., Woodward, L. J., & Horwood, L. J. (1998). Maternal smoking during pregnancy and psychiatric adjustment in late adolescence. Archives of General Psychiatry, 55, 721–727.CrossRefGoogle ScholarPubMed
Geronimus, A. T., & Korenman, S. (1992). The socioeconomic consequences of teen childbearing reconsidered. The Quarterly Journal of Economics, 107, 1187–1214.CrossRefGoogle Scholar
Gibson, C., Piquero, A., & Tibbets, S. (2000). Assessing the relationship between maternal cigarette smoking during pregnancy and age at first police contact. Justice Quarterly, 17, 519–542.CrossRefGoogle Scholar
Gottesman, I. I., & Bertelsen, A. (1989). Confirming unexpressed genotypes for schizophrenia. Archives of General Psychiatry, 46, 867–872.CrossRefGoogle ScholarPubMed
Greene, W. H. (2003). Econometric analysis. (5th ed.). Upper Saddle River, NJ: Prentice–Hall.Google Scholar
Griesler, P., Kandel, D., & Davies, M. (1998). Maternal smoking in pregnancy, child behavior problems, and adolescent smoking. Journal of Research on Adolescence, 8, 159–185.CrossRefGoogle Scholar
Harden, K. P., Lynch, S. K., Turkheimer, E., Emery, R. E., D'Onofrio, B. M., Slutske, W. S., et al. . (2007). A behavior genetic investigation of adolescent motherhood and offspring mental health problems. Journal of Abnormal Psychology, 116, 667–683.CrossRefGoogle ScholarPubMed
Heath, A. C., Kendler, K. S., Eaves, L. J., & Markell, D. (1985). The resolution of cultural and biological inheritance: Informativeness of different relationships. Behavior Genetics, 15, 439–465.CrossRefGoogle ScholarPubMed
Huizink, A. C., & Mulder, E. J. H. (2006). Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neuroscience and Biobehavioral Reviews, 30, 24–41.CrossRefGoogle ScholarPubMed
Kim, J., & Ferree, G. D. (1981). Standardization in causal analysis. Sociological Methods and Research, 10, 187–210.CrossRefGoogle Scholar
Kim, J., & Mueller, C. W. (1976). Standardized and unstandardized coefficients in causal analysis: An expository note. Sociological Methods and Research, 4, 423–438.CrossRefGoogle Scholar
Knopik, V. S., Heath, A. C., Jacob, T., Slutske, W. S., Bucholz, K. K., Madden, P. A. F., et al. (2006). Maternal alcoholism and offspring ADHD: Disentangling genetic and environmental effects using a children-of-twins design. Psychological Medicine, 36, 1461–1471.CrossRefGoogle ScholarPubMed
Knopik, V. S., Sparrow, E. P., Madden, P. A. F., Bucholz, K. K., Hudziak, J. J., Reich, W., et al. (2005). Contributions of parental alcoholism, prenatal substance exposure, and genetic transmission to child ADHD risk: A female twin study. Psychological Medicine, 35, 625–635.CrossRefGoogle Scholar
Lahey, B. B., McBurnett, K., & Loeber, R. (2000). Are attention-deficit hyperactivity disorder and oppositional defiant disorder developmental precursors to conduct disorder? In Sameroff, A., Lewis, M. & Miller, S. (Eds.), Handbook of developmental psychopathology (2nd ed., pp. 431–446). New York: Plenum Press.CrossRefGoogle Scholar
Li, K., & Poirier, D. J. (2003). The roles of inputs and outputs in predicting health, behaviour and test scores in early childhood. Statistics in Medicine, 22, 3489–3514.CrossRefGoogle ScholarPubMed
Linnet, K. M., Dalsgaard, S., Obel, C., Wisborg, K., Henriksen, T. B., Rodriguez, A., et al. (2003). Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. American Journal of Psychiatry, 160, 1028–1040.CrossRefGoogle ScholarPubMed
Little, R. J. A., & Rubin, D. B. (1987). Statistical analysis with missing data. New York: Wiley.Google Scholar
Loeber, R., Farrington, D. P., Stouthamer-Loeber, M., & Van Kammen, W. (1998). Antisocial behavior and mental health problems: Explanatory factors in childhood and adolescence. Mahwah, NJ: Erlbaum.CrossRefGoogle Scholar
Lynch, S. K., Turkheimer, E., Emery, R. E., D'Onofrio, B. M., Mendle, J., Slutske, W., et al. (2006). A genetically informed study of the association between harsh punishment and offspring behavioral problems. Journal of Family Psychology, 20, 190–198.CrossRefGoogle ScholarPubMed
Matthews, T. J. (2001). Smoking during pregnancy in the 1990s. National Vital Statistics Reports, 49, 1–14.Google Scholar
Maughan, B., Taylor, A., Caspi, A., & Moffitt, T. E. (2004). Prenatal smoking and early childhood conduct problems. Archives of General Psychiatry, 61, 836–843.CrossRefGoogle ScholarPubMed
Maughan, B., Taylor, C., Taylor, A., Butler, N., & Bynner, J. (2001). Pregnancy smoking and childhood conduct problems: A causal association? Journal of Child Psychology and Psychiatry, 42, 1021–1028.CrossRefGoogle ScholarPubMed
McDonald, S. D., Perkins, S. L., & Walker, M. C. (2005). Correlation between self-reported smoking status and serum cotinie during pregnancy. Addictive Behaviors, 30, 853–857.CrossRefGoogle ScholarPubMed
Mehta, P. D., & Neale, M. C. (2005). People are variables too: Multilevel structuralequations modeling. Psychological Methods, 10, 259–284.CrossRefGoogle Scholar
Mendle, J., Turkheimer, E., D'Onofrio, B. M., Lynch, S. K., Emery, R. E., Slutske, W., et al. (2006). Familiy structure and age at menarche: A children of twins approach. Developmental Psychology, 42, 535–542.CrossRefGoogle Scholar
Mick, E., Biederman, J., Faraone, S. V., Sayer, J., & Kleinman, S. (2002). Case control study of attention deficit hyperactivity disorder and maternal smoking, alcohol use, and drug use during pregnancy. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 378–385.CrossRefGoogle ScholarPubMed
Miles, D. R., & Carey, G. (1997). Genetic and environmental architecture of human aggression. Journal of Personality and Social Psychology, 72, 207–217.CrossRefGoogle ScholarPubMed
Miller, W. B., Pasta, D. J., MacMurray, J., Chiu, C., Wu, H., & Comings, D. E. (1999). Dopamine receptors are associated with age at first sexual intercourse. Journal of Biosocial Science, 31, 43–54.CrossRefGoogle ScholarPubMed
Moffitt, T. E. (1990). Juvenile delinquency and attention deficit disorder: Boys' developmental trajectories from age 3 to 15. Child Development, 61, 893–910.CrossRefGoogle Scholar
Moffitt, T. E. (2005). The new look of behavioral genetics in developmental psychopathology: Gene–environment interplay in antisocial behaviors. Psychological Bulletin, 131, 533–554.CrossRefGoogle ScholarPubMed
Moffitt, T. E., Caspi, A., Dickson, N., Silva, P. A., & Stanton, W. (1996). Childhood-onset versus adolescent-onset antisocial conduct in males: Natural history from age 3 to 18. Development and Psychopathology, 8, 399–424.CrossRefGoogle Scholar
Muthén, L. K., & Muthén, B. O. (1998–2005). Mplus user's guide (3rd ed.) Los Angeles, CA: Author.Google Scholar
Neale, M. C., & Cardon, L. R. D. (1992). Methodology for genetic studies of twins and families. Dordrecht: Kluwer.CrossRefGoogle Scholar
Neiss, M., Rowe, D. C., & Rodgers, J. L. (2002). Does education mediate the relationship between IQ and age of first birth? A behavioural genetic analysis. Journal of Biosocial Science, 34, 259–275.CrossRefGoogle ScholarPubMed
Peterson, J. L., & Zill, N. (1986). Marital disruption, parent–child relationships, and behavior problems in children. Journal of Marriage and the Family, 48, 295–307.CrossRefGoogle Scholar
Petitti, D. B., Friedman, G. D., & Kahn, W. (1981). Accuracy of information on smoking habits provided on self-administered research questionnaires. American Journal of Public Health, 71, 308–311.CrossRefGoogle ScholarPubMed
Purcell, S., & Koenen, K. C. (2005). Environmental mediation and the twin design. Behavior Genetics, 35, 491–498.CrossRefGoogle ScholarPubMed
Rasanen, P., Hakko, H., Isohanni, M., Hodgins, S., Jarvelin, J., & Tiihonen, J. (1999). Maternal smoking during pregnancy and risk of criminal behavior among adult male offspring in the Northern Finland 1966 birth cohort. American Journal of Psychiatry, 156, 857–862.CrossRefGoogle ScholarPubMed
Raudenbush, S. W., & Bryk, A. S. (2002). Hierarchical linear models: Applications and data analysis methods (2nd ed.) Thousand Oaks, CA: Sage.Google Scholar
Rodgers, J., Cleveland, H., van den Oord, E., & Rowe, D. (2000). Resolving the debate over birth order, family size, and intelligence. American Psychologist, 55, 599–612.CrossRefGoogle ScholarPubMed
Rodgers, J. L. (1996). NLSY youth linking algorithm. Unpublished manuscript.Google Scholar
Rodgers, J. L., Buster, M., & Rowe, D. C. (2001). Genetic and environmental influences on delinquency: DF analysis of NLSY kinship data. Journal of Quantitative Criminology, 17, 145–168.CrossRefGoogle Scholar
Rodgers, J. L., Rowe, D. C., & Buster, M. (1999). Nature, nurture and first sexual intercourse in the USA: Fitting behavioural genetic models to NLSY kinship data. Journal of Biosocial Science, 31, 29–41.CrossRefGoogle ScholarPubMed
Rodgers, J. L., Rowe, D. C., & Li, C. (1994). Beyond nature vs. nurture: DF analyses of nonshared influences on problem behaviors. Developmental Psychology, 30, 374–384.CrossRefGoogle Scholar
Rodgers, J. L., Rowe, D. C., & May, K. (1994). DF analysis of NLSY IQ/achievement data: Nonshared environmental influences. Intelligence, 19, 157–177.CrossRefGoogle Scholar
Rodriguez, A., & Bohlin, G. (2005). Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? Journal of Child Psychology and Psychiatry, 46, 246–254.CrossRefGoogle ScholarPubMed
Rutter, M., Pickles, A., Murray, R., & Eaves, L. J. (2001). Testing hypotheses on specific environmental causal effects on behavior. Psychological Bulletin, 127, 291– 324.CrossRefGoogle ScholarPubMed
Scarr, S., & McCartney, K. (1983). How people make their own environments: A theory of genotype–environment effects. Child Development, 54, 424–435.Google Scholar
Schafer, J. L. (1997). Analysis of incomplete multivariate data. London: Chapman & Hall.CrossRefGoogle Scholar
Silberg, J. L., Parr, T., Neale, M. C., Rutter, M., Angold, A., & Eaves, L. J. (2003). Maternal smoking during pregnancy and risk to boys' conduct disturbance: An examination of the causal hypothesis. Biological Psychiatry, 53, 130–135.CrossRefGoogle ScholarPubMed
Tambs, K., Sundet, J. M., Magnus, P., & Berg, K. (1989). Genetic and environmental contributions to the covariance between occupational status, educational attainment, and IQ: A study of twins. Behavior Genetics, 19, 505–522.CrossRefGoogle Scholar
Thapar, A., Fowler, T., Rice, F., Scourfield, J., van den Bree, M., Thomas, H., et al. (2003). Maternal smoking during pregnancy and attention deficit hyperactivity disorder symptoms in offspring. American Journal of Psychiatry, 160, 1985–1989.CrossRefGoogle ScholarPubMed
Turkheimer, E., D'Onofrio, B. M., Maes, H. H., & Eaves, L. J. (2005). Analysis and interpretation of twin studies with measured environments. Child Development, 76, 1217–1233.CrossRefGoogle Scholar
Turley, R. N. L. (2003). Are children of young mothers disadvantaged because of their mother's age or family background? Child Development, 74, 465–474.CrossRefGoogle ScholarPubMed
Wakschlag, L. S., & Hans, S. L. (2002). Maternal smoking during pregnancy and conduct problems in high-risk youth: A developmental framework. Development and Psychopathology, 14, 351–369.CrossRefGoogle ScholarPubMed
Wakschlag, L. S., & Keenan, K. (2001). Clinical significance and correlates of disruptive behavior symptoms in environmentally at-risk preschoolers. Journal of Clinical Child Psychology, 30, 262–275.CrossRefGoogle ScholarPubMed
Wakschlag, L. S., Lahey, B. B., Loeber, R., Green, S. M., Gordon, R. A., & Leventhal, B. L. (1997). Maternal smoking during pregnancy and the risk of conduct disorder in boys. Archives of General Psychiatry, 54, 670–676.CrossRefGoogle ScholarPubMed
Wakschlag, L. S., Pickett, K. E., Cook, E., Benowitz, N. L., & Leventhal, B. L. (2002). Maternal smoking during pregnancy and severe antisocial behavior in offspring: A review. American Journal of Public Health, 92, 966–974.CrossRefGoogle ScholarPubMed
Weissman, M. M., Warner, V., Wickramaratne, P. J., & Kandel, D. B. (1999). Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. Journal of the American Academy of Child & Adolescent Psychiatry, 38, 892–899.CrossRefGoogle ScholarPubMed
Wichman, A. L., Rodgers, J. L., & MacCallum, R. C. (2006). A multilevel approach to the relationship between birth order and intelligence. Personality and Social Psychology Bulletin, 32, 117–127.CrossRefGoogle Scholar
Willett, J. B., Singer, J. D., & Martin, N. C. (1998). The design and analysis of longitudinal studies of development and psychopathology in context: Statistical models and methodological recommendations. Development and Psychopathology, 10, 395–426.CrossRefGoogle ScholarPubMed
Zimmer, M. H., & Zimmer, M. (1998). Socioeconomic determinants of smoking behavior during pregnancy. The Social Science Journal, 35, 133–142.CrossRefGoogle Scholar