Skip to main content Accesibility Help

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

  • Brian M. D'Onofrio (a1), Carol A. van Hulle (a2), Irwin D. Waldman (a3), Joseph Lee Rodgers (a4), K. Paige Harden (a5), Paul J. Rathouz (a2) and Benjamin B. Lahey (a2)...

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.

Corresponding author
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:
Hide All

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.

Hide All
Achenbach, T. M. (1978). The Child Behavior Profile: I. Boys aged 6–11. Journal of Consulting and Clinical Psychology, 46, 478488.
Brennan, P. A., Grekin, E. R., & Mednick, S. A. (1999). Maternal smoking during pregnancy and adult male criminal outcomes. Archives of General Psychiatry, 56, 215219.
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, 941946.
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, 381385.
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, 155160.
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, 918931.
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, 703731.
Cnattingius, S. (2004). The epidemiology of smoking during pregnancy: Smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine and Tobacco Research, 6, S125S140.
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, 11301144.
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, 570586.
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, 486499.
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, 180188.
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, 283290.
Elliott, D. S., & Huizinga, D. (1983). Social class and delinquent behavior in a national youth panel. Criminology, 21, 149177.
Ernst, M. (2001). Behavioral and neural consequences of prental exposure to nicotine. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 630642.
Falconer, D. S. (1981). Introduction to quantitative genetics. New York: Longman.
Fergusson, D. M. (1999). Prenatal smoking and antisocial behavior. Archives of General Psychiatry, 56, 223224.
Fergusson, D. M., & Horwood, L. J. (2002). Male and female offending trajectories. Development and Psychopathology, 14, 159177.
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, 721727.
Geronimus, A. T., & Korenman, S. (1992). The socioeconomic consequences of teen childbearing reconsidered. The Quarterly Journal of Economics, 107, 11871214.
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, 519542.
Gottesman, I. I., & Bertelsen, A. (1989). Confirming unexpressed genotypes for schizophrenia. Archives of General Psychiatry, 46, 867872.
Greene, W. H. (2003). Econometric analysis. (5th ed.). Upper Saddle River, NJ: Prentice–Hall.
Griesler, P., Kandel, D., & Davies, M. (1998). Maternal smoking in pregnancy, child behavior problems, and adolescent smoking. Journal of Research on Adolescence, 8, 159185.
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, 667683.
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, 439465.
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, 2441.
Kim, J., & Ferree, G. D. (1981). Standardization in causal analysis. Sociological Methods and Research, 10, 187210.
Kim, J., & Mueller, C. W. (1976). Standardized and unstandardized coefficients in causal analysis: An expository note. Sociological Methods and Research, 4, 423438.
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, 14611471.
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, 625635.
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. 431446). New York: Plenum Press.
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, 34893514.
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, 10281040.
Little, R. J. A., & Rubin, D. B. (1987). Statistical analysis with missing data. New York: Wiley.
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.
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, 190198.
Matthews, T. J. (2001). Smoking during pregnancy in the 1990s. National Vital Statistics Reports, 49, 114.
Maughan, B., Taylor, A., Caspi, A., & Moffitt, T. E. (2004). Prenatal smoking and early childhood conduct problems. Archives of General Psychiatry, 61, 836843.
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, 10211028.
McDonald, S. D., Perkins, S. L., & Walker, M. C. (2005). Correlation between self-reported smoking status and serum cotinie during pregnancy. Addictive Behaviors, 30, 853857.
Mehta, P. D., & Neale, M. C. (2005). People are variables too: Multilevel structuralequations modeling. Psychological Methods, 10, 259284.
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, 535542.
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, 378385.
Miles, D. R., & Carey, G. (1997). Genetic and environmental architecture of human aggression. Journal of Personality and Social Psychology, 72, 207217.
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, 4354.
Moffitt, T. E. (1990). Juvenile delinquency and attention deficit disorder: Boys' developmental trajectories from age 3 to 15. Child Development, 61, 893910.
Moffitt, T. E. (2005). The new look of behavioral genetics in developmental psychopathology: Gene–environment interplay in antisocial behaviors. Psychological Bulletin, 131, 533554.
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, 399424.
Muthén, L. K., & Muthén, B. O. (19982005). Mplus user's guide (3rd ed.) Los Angeles, CA: Author.
Neale, M. C., & Cardon, L. R. D. (1992). Methodology for genetic studies of twins and families. Dordrecht: Kluwer.
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, 259275.
Peterson, J. L., & Zill, N. (1986). Marital disruption, parent–child relationships, and behavior problems in children. Journal of Marriage and the Family, 48, 295307.
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, 308311.
Purcell, S., & Koenen, K. C. (2005). Environmental mediation and the twin design. Behavior Genetics, 35, 491498.
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, 857862.
Raudenbush, S. W., & Bryk, A. S. (2002). Hierarchical linear models: Applications and data analysis methods (2nd ed.) Thousand Oaks, CA: Sage.
Rodgers, J., Cleveland, H., van den Oord, E., & Rowe, D. (2000). Resolving the debate over birth order, family size, and intelligence. American Psychologist, 55, 599612.
Rodgers, J. L. (1996). NLSY youth linking algorithm. Unpublished manuscript.
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, 145168.
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, 2941.
Rodgers, J. L., Rowe, D. C., & Li, C. (1994). Beyond nature vs. nurture: DF analyses of nonshared influences on problem behaviors. Developmental Psychology, 30, 374384.
Rodgers, J. L., Rowe, D. C., & May, K. (1994). DF analysis of NLSY IQ/achievement data: Nonshared environmental influences. Intelligence, 19, 157177.
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, 246254.
Rutter, M., Pickles, A., Murray, R., & Eaves, L. J. (2001). Testing hypotheses on specific environmental causal effects on behavior. Psychological Bulletin, 127, 291324.
Scarr, S., & McCartney, K. (1983). How people make their own environments: A theory of genotype–environment effects. Child Development, 54, 424435.
Schafer, J. L. (1997). Analysis of incomplete multivariate data. London: Chapman & Hall.
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, 130135.
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, 505522.
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, 19851989.
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, 12171233.
Turley, R. N. L. (2003). Are children of young mothers disadvantaged because of their mother's age or family background? Child Development, 74, 465474.
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, 351369.
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, 262275.
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, 670676.
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, 966974.
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, 892899.
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, 117127.
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, 395426.
Zimmer, M. H., & Zimmer, M. (1998). Socioeconomic determinants of smoking behavior during pregnancy. The Social Science Journal, 35, 133142.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Development and Psychopathology
  • ISSN: 0954-5794
  • EISSN: 1469-2198
  • URL: /core/journals/development-and-psychopathology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed