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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*
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: bmdonofr@indiana.edu.

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
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, 478488.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google 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, 703731.Google Scholar
Cnattingius, S. (2004). The epidemiology of smoking during pregnancy: Smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine and Tobacco Research, 6, S125S140.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Elliott, D. S., & Huizinga, D. (1983). Social class and delinquent behavior in a national youth panel. Criminology, 21, 149177.Google Scholar
Ernst, M. (2001). Behavioral and neural consequences of prental exposure to nicotine. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 630642.Google 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, 223224.Google Scholar
Fergusson, D. M., & Horwood, L. J. (2002). Male and female offending trajectories. Development and Psychopathology, 14, 159177.Google Scholar
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.Google Scholar
Geronimus, A. T., & Korenman, S. (1992). The socioeconomic consequences of teen childbearing reconsidered. The Quarterly Journal of Economics, 107, 11871214.Google 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, 519542.Google Scholar
Gottesman, I. I., & Bertelsen, A. (1989). Confirming unexpressed genotypes for schizophrenia. Archives of General Psychiatry, 46, 867872.Google Scholar
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, 159185.Google 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, 667683.Google Scholar
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.Google Scholar
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.Google Scholar
Kim, J., & Ferree, G. D. (1981). Standardization in causal analysis. Sociological Methods and Research, 10, 187210.Google Scholar
Kim, J., & Mueller, C. W. (1976). Standardized and unstandardized coefficients in causal analysis: An expository note. Sociological Methods and Research, 4, 423438.Google 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, 14611471.Google Scholar
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.Google 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. 431446). New York: Plenum Press.Google 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, 34893514.Google Scholar
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.Google Scholar
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.Google 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, 190198.Google Scholar
Matthews, T. J. (2001). Smoking during pregnancy in the 1990s. National Vital Statistics Reports, 49, 114.Google Scholar
Maughan, B., Taylor, A., Caspi, A., & Moffitt, T. E. (2004). Prenatal smoking and early childhood conduct problems. Archives of General Psychiatry, 61, 836843.Google Scholar
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.Google Scholar
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.Google Scholar
Mehta, P. D., & Neale, M. C. (2005). People are variables too: Multilevel structuralequations modeling. Psychological Methods, 10, 259284.Google 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, 535542.Google 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, 378385.Google Scholar
Miles, D. R., & Carey, G. (1997). Genetic and environmental architecture of human aggression. Journal of Personality and Social Psychology, 72, 207217.Google Scholar
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.Google Scholar
Moffitt, T. E. (1990). Juvenile delinquency and attention deficit disorder: Boys' developmental trajectories from age 3 to 15. Child Development, 61, 893910.Google Scholar
Moffitt, T. E. (2005). The new look of behavioral genetics in developmental psychopathology: Gene–environment interplay in antisocial behaviors. Psychological Bulletin, 131, 533554.Google Scholar
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.Google Scholar
Muthén, L. K., & Muthén, B. O. (19982005). 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.Google 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, 259275.Google Scholar
Peterson, J. L., & Zill, N. (1986). Marital disruption, parent–child relationships, and behavior problems in children. Journal of Marriage and the Family, 48, 295307.Google 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, 308311.Google Scholar
Purcell, S., & Koenen, K. C. (2005). Environmental mediation and the twin design. Behavior Genetics, 35, 491498.Google Scholar
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.Google Scholar
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, 599612.Google Scholar
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, 145168.Google 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, 2941.Google Scholar
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.Google Scholar
Rodgers, J. L., Rowe, D. C., & May, K. (1994). DF analysis of NLSY IQ/achievement data: Nonshared environmental influences. Intelligence, 19, 157177.Google 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, 246254.Google Scholar
Rutter, M., Pickles, A., Murray, R., & Eaves, L. J. (2001). Testing hypotheses on specific environmental causal effects on behavior. Psychological Bulletin, 127, 291324.Google Scholar
Scarr, S., & McCartney, K. (1983). How people make their own environments: A theory of genotype–environment effects. Child Development, 54, 424435.Google Scholar
Schafer, J. L. (1997). Analysis of incomplete multivariate data. London: Chapman & Hall.Google 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, 130135.Google Scholar
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.Google 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, 19851989.Google Scholar
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.Google Scholar
Turley, R. N. L. (2003). Are children of young mothers disadvantaged because of their mother's age or family background? Child Development, 74, 465474.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google 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, 395426.Google Scholar
Zimmer, M. H., & Zimmer, M. (1998). Socioeconomic determinants of smoking behavior during pregnancy. The Social Science Journal, 35, 133142.Google Scholar