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Separating Family-Level and Direct Exposure Effects of Smoking During Pregnancy on Offspring Externalizing Symptoms: Bridging the Behavior Genetic and Behavior Teratologic Divide

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Abstract

Maternal smoking during pregnancy (MSDP) has been robustly associated with externalizing problems and their developmental precursors in offspring in studies using behavioral teratologic designs (Wakschlag et al., Am J Public Health 92(6):966–974, 2002; Espy et al., Dev Psychol 47(1):153–169, 2011). In contrast, the use of behavior genetic approaches has shown that the effects commonly attributed to MSDP can be explained by family-level variables (D’Onofrio et al., Dev Psychopathol 20(01):139–164, 2008). Reconciling these conflicting findings requires integration of these study designs. We utilize longitudinal data on a preschool proband and his/her sibling from the Midwest Infant Development Study-Preschool (MIDS-P) to test for teratologic and family level effects of MSDP. We find considerable variation in prenatal smoking patterns both within and across pregnancies within families, indicating that binary smoking measures are not sufficiently capturing exposure. Structural equation models indicate that both conduct disorder and oppositional defiant disorder symptoms showed unique effects of MSDP over and above family level effects. Blending high quality exposure measurement with a within-family design suggests that it is premature to foreclose the possibility of a teratologic effect of MSDP on externalizing problems. Implications and recommendations for future studies are discussed.

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References

  • Baron H (1996) Strengths and limitations of ipsative measurement. J Occup Organ Psychol 69(1):49–56

    Article  Google Scholar 

  • Brigham J, Lessov-Schlaggar CN, Javitz HS, McElroy M, Krasnow R, Swan GE (2008) Reliability of adult retrospective recall of lifetime tobacco use. Nicotine Tob Res 10(2):287–299. doi:10.1080/14622200701825718

    Article  PubMed  Google Scholar 

  • Brown RA, Burgess ES, Sales SD, Whiteley JA, Evans DM, Miller IW (1998) Reliability and validity of a smoking timeline follow-back interview. Psychol Addit Behav 12(2):101–112

    Article  Google Scholar 

  • Chassin L, Presson CC, Pitts SC, Sherman SJ (2000) The natural history of cigarette smoking from adolescence to adulthood in a midwestern community sample: multiple trajectories and their psychosocial correlates. Health Psychol 19(3):223

    Article  PubMed  Google Scholar 

  • Clark CAC, Sheffield T, Johnson C, Espy KA, Wakschlag LS (2009) Timeline follow-back interview for the assessment of maternal smoking during pregnancy for multiple siblings. Unpublished instrument, available upon request

  • D’Onofrio BM, Lahey BB, Turkheimer E, Lichtenstein P (2013) Critical need for family-based, quasi-experimental designs in integrating genetic and social science research. Am J Public Health 103(S1):S46–S55

    Article  PubMed  PubMed Central  Google Scholar 

  • Dick DM, Johnson JK, Viken RJ, Rose RJ (2000) Testing between-family associations in within-family comparisons. Psychol Sci 11(5):409–413

    Article  PubMed  Google Scholar 

  • D’Onofrio BM, Hulle CAV, Waldman ID, Rodgers JL, Harden KP, Rathouz PJ, Lahey BB (2008) Smoking during pregnancy and offspring externalizing problems: an exploration of genetic and environmental confounds. Dev Psychopathol 20(01):139–164

    PubMed  PubMed Central  Google Scholar 

  • D’Onofrio BM, Singh AL, Iliadou A, Lambe M, Hultman CM, Grann M et al (2010) Familial confounding of the association between maternal smoking during pregnancy and offspring criminality: a population-based study in Sweden. Arch Gen Psychiatry 67(5):529–538

    Article  PubMed  PubMed Central  Google Scholar 

  • Dukic VM, Niessner M, Benowitz N, Hans S, Wakschlag L (2007) Modeling the relationship of cotinine and self-reported measures of maternal smoking during pregnancy: a deterministic approach. Nicotine Tob Res 9(4):453–465

    Article  PubMed  Google Scholar 

  • Eiden RD, Homish GG, Colder CR, Schuetze P, Gray TR, Huestis MA (2013) Changes in smoking patterns during pregnancy. Subst Use Misuse 48(7):513–522

    Article  PubMed  PubMed Central  Google Scholar 

  • Eisenhower D, Mathiowetz NA, Moganstein D (1991) Recall error: sources and bias reduction techniques. In: Biemer P, Groves RM, Lyberg LE, Mathiowetz NA, Sudman S (eds) Measurement errors in surveys. John Wiley & Sons, New York. doi:10.1002/9781118150382.ch8

  • Ellingson JM, Goodnight JA, Van Hulle CA, Waldman ID, D’Onofrio BM (2014) A sibling-comparison study of smoking during pregnancy and childhood psychological traits. Behav Genet 44(1):25–35

    Article  PubMed  PubMed Central  Google Scholar 

  • England LJ, Grauman A, Quian C, Wilkins DG, Schisterman EF, Yu KF et al (2007) Misclassification of maternal smoking status and its effects on an epidemiologic study of pregnancy outcomes. Nicotine Tob Res 9:1005–1013

    Article  PubMed  Google Scholar 

  • Ernst M, Moolchan ET, Robinson ML (2001) Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psychiatry 40(6):630–641

    Article  PubMed  Google Scholar 

  • Espy KA, Fang H, Johnson C, Stopp C, Wiebe SA, Respass J (2011) Prenatal tobacco exposure: developmental outcomes in the neonatal period. Dev Psychol 47(1):153–169

    Article  PubMed  PubMed Central  Google Scholar 

  • Gadow KD, Sprafkin J (1994) Child Symptom Inventories manual. Checkmate Plus, Stony Brook

    Google Scholar 

  • Gadow KD, Sprafkin J (1998) Adolescent Symptom Inventory-4 norms manual. Checkmate Plus, Stony Brook

    Google Scholar 

  • Gadow KD, Sprafkin J (2000) Early Childhood Inventory-4 screening manual. Checkmate Plus, Stony Brook

    Google Scholar 

  • Glasner T, van der Vaart W (2009) Applications of calendar instruments in social surveys: a review. Qual Quant 43:333–349

    Article  PubMed  PubMed Central  Google Scholar 

  • Harrod SB, Lacy RT, Morgan AJ (2012) Offspring of prenatal IV nicotine exposure exhibit increased sensitivity to the reinforcing effects of methamphetamine. Front Pharmacol 3:116. doi:10.3389/fphar.2012.00116

    Article  PubMed  PubMed Central  Google Scholar 

  • Horn JL (1965) A rationale and test for the number of factors in factor analysis. Psychometrika 30:179–185

    Article  PubMed  Google Scholar 

  • Huijbregts SC, Séguin JR, Zoccolillo M, Boivin M, Tremblay RE (2007) Associations of maternal prenatal smoking with early childhood physical aggression, hyperactivity-impulsivity, and their co-occurrence. J Abnorm Child Psychol 35(2):203–215

    Article  PubMed  PubMed Central  Google Scholar 

  • Huizink AC, Mulder EJ (2006) Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neurosci Biobehav Rev 30:24–41

    Article  PubMed  Google Scholar 

  • Jackson DJ, Alwin DF (1980) The factor analysis of ipsative measures. Sociol Methods Res 9(2):218–238

    Article  Google Scholar 

  • Kim-Cohen J, Caspi A, Taylor A, Williams B, Newcombe R, Craig IW, Moffitt TE (2006) MAOA, maltreatment, and gene–environment interaction predicting children’s mental health: new evidence and a meta-analysis. Mol Psychiatry 11(10):903–913

    Article  PubMed  Google Scholar 

  • Knopik VS (2009) Maternal smoking during pregnancy and child outcomes: real or spurious effect? Dev Neuropsychol 34(1):1–36. doi:10.1080/87565640802564366

    Article  PubMed  PubMed Central  Google Scholar 

  • Kodl MM, Wakschlag LS (2004) Does a childhood history of externalizing problems predict smoking during pregnancy? Addict Behav 29:273–279

    Article  PubMed  Google Scholar 

  • Kuja-Halkola R, D’Onofrio BM, Iliadou AN, Långström N, Lichtenstein P (2010) Prenatal smoking exposure and offspring stress coping in late adolescence: no causal link. Int J Epidemiol 39(6):1531–1540

    Article  PubMed  PubMed Central  Google Scholar 

  • Lacy RT, Hord LL, Morgan AJ, Harrod SB (2012) Intravenous gestational nicotine exposure results in increased motivation for sucrose reward in adult rat offspring. Drug Alcohol Depend 124:299–306. doi:10.1016/j.drugalcdep.2012.01.025

    Article  PubMed  PubMed Central  Google Scholar 

  • LeSage MG, Gustaf E, Dufek MB, Pentel PR (2006) Effects of maternal intravenous nicotine administration on locomotor behavior in pre-weanling rats. Pharmacol Biochem Behav 85:575–583. doi:10.1016/j.pbb.2006.10.012

    Article  PubMed  PubMed Central  Google Scholar 

  • Leve LD, Neiderhiser JM, Shaw DS, Ganiban J, Natsuaki MN, Reiss D (2013) The early growth and development study: a prospective adoption study from birth through middle childhood. Twin Res Hum Genet 16(01):412–423

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewis-Esquerre JM, Colby SM, Tevyaw TOL, Eaton CA, Kahler CW, Monti PM (2005) Validation of the timeline follow-back in the assessment of adolescent smoking. Drug Alcohol Depend 79(1):33–43

    Article  PubMed  Google Scholar 

  • Lotfipour S, Ferguson E, Leonard G, Perron M, Pike B, Richer L et al (2009) Orbitofrontal cortex and drug use during adolescence: role of prenatal exposure to maternal smoking and BDNF genotype. Arch Gen Psychiatry 66(11):1244–1252

    Article  PubMed  Google Scholar 

  • Marceau K, Hajal N, Leve LD, Reiss D, Shaw DS, Ganiban JM, Mayes LC, Neiderhiser JM (2013) Measurement and associations of pregnancy risk factors with genetic influences, postnatal environmental influences, and toddler behavior. Int J Behav Dev 37(4):366–375

    Article  PubMed  PubMed Central  Google Scholar 

  • Massey SH, Compton MT (2013) Psychological differences between smokers who quit during pregnancy and those who do not: a review of observational studies and directions for future research. Nicotine Tob Res 15(2):307–319

    Article  PubMed  Google Scholar 

  • Massey SH, Bublitz MH, Magee SR, Salisbury A, Niaura RS, Wakschlag LS, Stroud LR (2015a) Maternal-fetal attachment differentiates patterns of prenatal smoking and exposure. Addict Behav 45:51–56

    Article  PubMed  Google Scholar 

  • Massey SH, Estabrook C, O’Brien TC, Burns JL, Pine DS, Jacob S, Cook EC, Wakschlag LS (2015b) Preliminary evidence for the interaction of the oxytocin receptor gene and face processing in differentiating prenatal smoking patterns. Neurosci Lett 584:259–264

    Article  PubMed  Google Scholar 

  • McGrath LM, Mustanski B, Metzger A, Pine DS, Kistner-Griffin E, Cook E, Wakschlag LS (2012) A latent modeling approach to genotype–phenotype relationships: maternal problem behavior clusters, prenatal smoking, and MAOA genotype. Arch Women Mental Health 15(4):269–282

    Article  Google Scholar 

  • Neale MC, Hunter MD, Pritikin JN, Zahery M, Brick TR, Kirkpatrick RM, Estabrook R, Bates TC, Maes HH, Boker SM (2015) OpenMx 2.0: extended structural equation and statistical modeling. Manuscript accepted at Psychometrika

  • Nigg JT, Breslau N (2007) Prenatal smoking exposure, low birth weight, and disruptive behavior disorders. J Am Acad Child Adolesc Psychiatry 46(3):362–369

    Article  PubMed  Google Scholar 

  • Pickett KE, Wakschlag LS, Dai L, Leventhal BL (2003) Fluctuations of maternal smoking during pregnancy. Obstet Gynecol 101(1):140–147

    PubMed  Google Scholar 

  • Pickett KE, Rathouz PJ, Kasza K, Wakschlag LS, Wright R (2005) Self-reported smoking, cotinine levels, and patterns of smoking in pregnancy. Paediatr Perinat Epidemiol 19(5):368–376

    Article  PubMed  Google Scholar 

  • Pickett KE, Wilkinson RG, Wakschlag LS (2009a) The psychosocial context of pregnancy smoking and quitting in the Millennium Cohort Study. J Epidemiol Community Health 63:474–480. doi:10.1136/jech.2008.082594

    Article  PubMed  Google Scholar 

  • Pickett KE, Kasza K, Biesecker G, Wright RJ, Wakschlag LS (2009b) Women who remember, women who do not: a methodological study of maternal recall of smoking in pregnancy. Nicotine Tob Res 11(10):1166–1174

    Article  PubMed  PubMed Central  Google Scholar 

  • Schneider T, Bizarro L, Asherson PJ, Stolerman IP (2010) Gestational exposure to nicotine in drinking water: teratogenic effects and methodological issues. Behav Pharmacol 21:206–216. doi:10.1097/FBP.0b013e32833a5bb5

    Article  PubMed  PubMed Central  Google Scholar 

  • Skoglund C, Chen Q, D’Onofrio BM, Lichtenstein P, Larsson H (2014) Familial confounding of the association between maternal smoking during pregnancy and ADHD in offspring. J Child Psychol Psychiatry 55(1):61–68

    Article  PubMed  PubMed Central  Google Scholar 

  • Sobell LC, Sobell MB (1996) Timeline Follow-Back user’s guide: a calendar method assessing alcohol and drug abuse. Addiction Research Foundation, Toronto

    Google Scholar 

  • U.S. Department of Health and Human Services (U.S. DHHS) (2014) The health consequences of smoking—50 years of progress. A Report of the Surgeon General. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health, Atlanta

  • Wakschlag LS, Hans SL (2002) Maternal smoking during pregnancy and conduct problems in high-risk youth: a developmental framework. Dev Psychopathol 14(2):351–369

    Article  PubMed  Google Scholar 

  • Wakschlag L, Kistner E, Pine D, Biesecker G, Pickett K, Skol A et al (2010) Interaction of prenatal exposure to cigarettes and MAOA genotype in pathways to youth antisocial behavior. Mol Psychiatry 15:928–937. doi:10.1038/mp.2009.22

    Article  PubMed  PubMed Central  Google Scholar 

  • Wakschlag L, Pickett K, Cook E, Benowitz N, Leventhal B (2002) Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review. Am J Public Health 92(6):966–974

    Article  PubMed  PubMed Central  Google Scholar 

  • Wakschlag LS, Pickett KE, Middlecamp MK, Walton LL, Tenzer P, Leventhal BL (2003) Pregnant smokers who quit, pregnant smokers who don’t: does history of problem behavior make a difference? Soc Sci Med 56(12):2449–2460

    Article  PubMed  Google Scholar 

  • Wakschlag LS, Briggs-Gowan M, Choi S, Nichols S, Kestler J, Burns J et al (2014) Advancing a multidimensional, developmental spectrum approach to preschool disruptive behavior. J Am Acad Child Adolesc Psychiatry 53:82–96

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiebe S, Clark C, de Jong D, Chevalier N, Espy K, Wakschlag L (2015) Prenatal tobacco exposure and self-regulation in early childhood: Implications for developmental psychopathology. Dev Psychopathol 27(2):397–409

    Article  PubMed  Google Scholar 

  • Zoccolillo M (2000) Parents’ health and social adjustment: Part II, social adjustment. Longitudinal Study of Child Development in Québec (ELDEQ 1998–2002). Institut de la Statistique du Québec, Québec, pp 37–45

    Google Scholar 

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Acknowledgments

We gratefully acknowledge the members of the Developmental Cognitive Neuroscience Laboratory for assistance with data collection and coding and the families who made this research possible. Ryne Estabrook, Carrie Clark, Brian Mustanski, Edwin Cook, Kimberly Espy and Lauren Wakschlag were all supported by R01 DA023653 (PIs: Wakschlag and Espy). Suena Massey was supported by K23 DA037913 (PI: Massey), Kimberly Espy was also supported by R01 DA014661 (PI: Espy) and Lauren Wakschlag was also supported by the Walden & Jean Young Shaw Foundation.

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Authors and Affiliations

  1. Department of Medical Social Sciences, Northwestern University Feinberg School of Medicine, 633 N. St. Clair Street, 19th Floor, Chicago, IL, 60611, USA

    Ryne Estabrook, Suena H. Massey, James L. Burns, Brian S. Mustanski, Beth Makowski & Lauren S. Wakschlag

  2. Department of Psychiatry & Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

    Suena H. Massey

  3. Department of Psychology, University of Arizona, Tucson, AZ, USA

    Caron A. C. Clark

  4. Institute for Juvenile Research, Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA

    Edwin H. Cook

  5. Department of Psychology, Illinois College, Jacksonville, IL, USA

    T. Caitlin O’Brien

  6. Departments of Psychology and Psychiatry, University of Arizona, Tucson, AZ, USA

    Kimberly A. Espy

  7. Office for Research & Economic Development, University of Nebraska-Lincoln, Lincoln, NE, USA

    Kimberly A. Espy

  8. Institute for Policy Research, Northwestern University, Evanston, IL, USA

    Lauren S. Wakschlag

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  1. Ryne Estabrook
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  2. Suena H. Massey
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  3. Caron A. C. Clark
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  7. T. Caitlin O’Brien
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  9. Kimberly A. Espy
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Correspondence to Ryne Estabrook.

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Conflict of Interest

Ryne Estabrook, Suena H. Massey, Caron A. C. Clark, James L. Burns, Brian S. Mustanski, Edwin H. Cook, T. Caitlin O’Brien, Beth Makowski, Kimberly A. Espy and Lauren S. Wakschlag declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This research was completed with appropriate review by the institutional review boards of the authors’ universities. All data collection and data manipulation was compliant with rules regarding ethical treatment of human subjects and informed consent.

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Appendix

Appendix

Appendix 1

See Table 5.

Table 5 Correlations between prospective and retrospective measures
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Appendix 2: Power simulation

To test our assertion that our longitudinal assessment increases power over a single assessment of SDP, we created a small Monte Carlo simulation. Data were generated using either a single continuous SDP indicator or three indicators correlated 0.8. We varied the sample size (values of 250, 500, 750 and 1000) and the size of the individual level effect from our model in Fig. 2 (Bdirect of 0.1, 0.2, 0.3 and 0.4). The direct effect was held constant at 0.1, while the within-family correlations of both SDP and externalizing were held constant at 0.5. These values are reasonably close to those found in our empirical data, but with a much wider range of sample sizes to inform future studies. We created 250 datasets for each condition, generated an empirical power estimate as the proportion of studies within a cell that find the effect, and presented all results in Fig. 4.

Fig. 4
figure 4

Power of one- and three-occasion designs

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We found three occasion exposure models with power of .8 have their power reduced to .602 when reduced to a single measure. Three occasions with power of .9 have power of .735 with a single measure.

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Estabrook, R., Massey, S.H., Clark, C.A.C. et al. Separating Family-Level and Direct Exposure Effects of Smoking During Pregnancy on Offspring Externalizing Symptoms: Bridging the Behavior Genetic and Behavior Teratologic Divide. Behav Genet 46, 389–402 (2016). https://doi.org/10.1007/s10519-015-9762-2

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