Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-05T13:11:31.177Z Has data issue: false hasContentIssue false
  • English
  • Français

Disentangling the relationships between maternal smoking during pregnancy and co-occurring risk factors

Published online by Cambridge University Press:  25 November 2011

J. M. Ellingson ,
M. E. Rickert ,
P. Lichtenstein ,
N. Långström  and
B. M. D'Onofrio
J. M. Ellingson
Affiliation:
Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, USA Department of Psychological Sciences, University of Missouri, Columbia, MO, USA
M. E. Rickert
Affiliation:
Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, USA
P. Lichtenstein
Affiliation:
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Sweden
N. Långström
Affiliation:
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Sweden
B. M. D'Onofrio*
Affiliation:
Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, USA
*
*Address for correspondence: Dr B. M. D'Onofrio, Department of Psychological and Brain Sciences, Indiana University, 1101 East 10th St, Bloomington, IN 47405, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Maternal smoking during pregnancy (SDP) has been studied extensively as a risk factor for adverse offspring outcomes and is known to co-occur with other familial risk factors. Accounting for general familial risk factors has attenuated associations between SDP and adverse offspring outcomes, and identifying these confounds will be crucial to elucidating the relationship between SDP and its psychological correlates.

Method

The current study aimed to disentangle the relationship between maternal SDP and co-occurring risk factors (maternal criminal activity, drug problems, teen pregnancy, educational attainment, and cohabitation at childbirth) using a population-based sample of full- (n=206 313) and half-sister pairs (n=19 363) from Sweden. Logistic regression models estimated the strength of association between SDP and co-occurring risk factors. Bivariate behavioral genetic models estimated the degree to which associations between SDP and co-occurring risk factors are attributable to genetic and environmental factors.

Results

Maternal SDP was associated with an increase in all co-occurring risk factors. Of the variance associated with SDP, 45% was attributed to genetic factors and 53% was attributed to unshared environmental factors. In bivariate models, genetic factors accounted for 21% (non-drug-, non-violence-related crimes) to 35% (drug-related crimes) of the covariance between SDP and co-occurring risk factors. Unshared environmental factors accounted for the remaining covariance.

Conclusions

The genetic factors that influence a woman's criminal behavior, substance abuse and her offspring's rearing environment all influence SDP. Therefore, the intergenerational transmission of genes conferring risk for antisocial behavior and substance misuse may influence the associations between maternal SDP and adverse offspring outcomes.

Keywords

Antisocialbehavior geneticscriminaldrugpregnancysmoking
Type
Original Articles
Information
Psychological Medicine , Volume 42 , Issue 7 , July 2012 , pp. 1547 - 1557
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agrawal, A, Knopik, VS, Pergadia, ML, Waldron, M, Bucholz, KK, Martin, NG, Heath, AC, Madden, PAF (2008). Correlates of cigarette smoking during pregnancy and its genetic and environmental overlap with nicotine dependence. Nicotine and Tobacco Research 10, 567–578.CrossRefGoogle ScholarPubMed
Barkley, RA (1997). Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychological Bulletin 121, 65–94.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, 943–950.CrossRefGoogle ScholarPubMed
Brennan, PA, Grekin, ER, Mortensen, EL, Mednick, SA (2002). Relationship of maternal smoking during pregnancy with criminal arrest and hospitalization for substance abuse in male and female adult offspring. American Journal of Psychiatry 159, 48–54.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, e57–e65.CrossRefGoogle ScholarPubMed
Centre for Epidemiology (2003). The Swedish Medical Birth Register: A Summary of Content and Quality. Sweden: Centre for Epidemiology.Google Scholar
Centre for Epidemiology (2005). The Swedish Hospital Discharge Register. Sweden: Centre for Epidemiology.Google Scholar
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, 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, 529–538.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
Ekblad, M, Gissler, M, Lehtonen, L, Korkeila, J (2010). Prenatal smoking exposure and the risk of psychiatric morbidity into young adulthood. Archives of General Psychiatry 67, 841–849.CrossRefGoogle ScholarPubMed
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, 630–642.CrossRefGoogle ScholarPubMed
Espy, KA, Fang, H, Johnson, C, Stopp, C, Wiebe, SA, Respass, J (2010). Prenatal tobacco exposure: developmental outcomes in the neonatal period. Developmental Psychology 47, 153–169.CrossRefGoogle Scholar
Frisell, T, Lichtenstein, LN, Långström, N (2011). Violent crime runs in families: a total population study of 12.5 million individuals. Psychological Medicine 41, 97–106.CrossRefGoogle ScholarPubMed
Gilman, SE, Breslau, J, Subramanian, SV, Hitsman, B, Koenen, KC (2008 a). Social factors, psychopathology, and maternal smoking during pregnancy. American Journal of Public Health 98, 448–453.CrossRefGoogle ScholarPubMed
Gilman, SE, Gardener, H, Buka, SL (2008 b). Maternal smoking during pregnancy and children's cognitive and physical development: a causal risk factor? American Journal of Epidemiology 168, 522–531.CrossRefGoogle ScholarPubMed
Ginther, DK, Pollak, RA (2004). Family structure and children's educational outcomes: blended families, stylized facts, and descriptive regressions. Demography 41, 671–696.CrossRefGoogle ScholarPubMed
Han, C, McGue, MK, Iacono, WG (1999). Lifetime tobacco, alcohol and other substance use in adolescent Minnesota twins: univariate and multivariate behavioral genetic analyses. Addiction 94, 981–993.CrossRefGoogle ScholarPubMed
Hicks, BM, Blonigen, DM, Kramer, MD, Krueger, RF, Patrick, CJ, Iacono, WG, McGue, M (2007). Gender differences and developmental change in externalizing disorders from late adolescence to early adulthood: a longitudinal twin study. Journal of Abnormal Psychology 116, 433–447.CrossRefGoogle ScholarPubMed
Higuchi, S, Matsushita, S, Imazeki, H, Kinoshita, T, Takagi, S, Kono, H (1994). Aldehyde dehydrogenase genotypes in Japanese alcoholics. Lancet 343, 741–742.CrossRefGoogle ScholarPubMed
Huijbregts, SCJ, Warren, AJ, de Sonneville, LMJ, Swaab-Barneveld, H (2008). Hot and cool forms of inhibitory control and externalizing behavior in children of mothers who smoked during pregnancy: an exploratory study. Journal of Abnormal Child Psychology 36, 323–333.CrossRefGoogle ScholarPubMed
Jacobson, SW, Chiodo, LM, Sokol, RJ, Jacobson, JL (2002). Validity of maternal report of prenatal alcohol, cocaine, and smoking in relation to neurobehavioral outcome. Pediatrics 109, 815–825.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, 590–597.CrossRefGoogle ScholarPubMed
Kandel, DB, Wu, P, Davies, M (1994). Maternal smoking during pregnancy and smoking by adolescent daughters. American Journal of Public Health 84, 1407–1413.CrossRefGoogle ScholarPubMed
Knopik, VS (2009). Maternal smoking during pregnancy and child outcomes: real or spurious effect? Developmental Neuropsychology 34, 1–36.CrossRefGoogle ScholarPubMed
Krueger, RF, Hicks, BM, Patrick, CJ, Carlson, SR, Iacono, WG, McGue, M (2002). Etiologic connections among substance dependence, antisocial behavior and personality: modeling the externalizing spectrum. Journal of Abnormal Psychology 111, 411–424.CrossRefGoogle ScholarPubMed
Krueger, RF, Markon, KE (2006). Reinterpreting comorbidity: a model-based approach to understanding and classifying psychopathology. Annual Review of Clinical Psychology 2, 111–133.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, 1531–1540.CrossRefGoogle ScholarPubMed
Lahey, BB, D'Onofrio, BM, Waldman, ID (2009). Using epidemiologic methods to test hypotheses regarding causal influences on child and adolescent mental disorders. Journal of Child Psychology and Psychiatry 50, 53–62.CrossRefGoogle ScholarPubMed
Lambe, M, Hultman, C, Torrång, A, MacCabe, J, Cnattingius, S (2006). Maternal smoking during pregnancy and school performance at age 15. Epidemiology 17, 524–530.CrossRefGoogle ScholarPubMed
Langley, K, Holmans, PA, van den Bree, M, Thapar, A (2007). Effects of low birth weight, maternal smoking in pregnancy and social class on the phenotypic manifestation of Attention Deficit Hyperactivity Disorder and associated antisocial behaviour: investigation in a clinical sample. BMC Psychiatry 7, 26.CrossRefGoogle Scholar
Lau, MA, Pihl, RO, Peterson, JB (1995). Provocation, acute alcohol intoxication, cognitive performance, and aggression. Journal of Abnormal Psychology 104, 150–155.CrossRefGoogle ScholarPubMed
Lindblad, F, Hjern, A (2010). ADHD after fetal exposure to maternal smoking. Nicotine and Tobacco Research 12, 408–415.CrossRefGoogle ScholarPubMed
Lindqvist, R, Lendahls, L, Tollbom, ÖR, Åberg, H, Håkansson, A (2002). Smoking during pregnancy: comparison of self reports and cotinine levels in 496 women. Acta Obstetricia et Gynecologica Scandinavica 81, 240–244.CrossRefGoogle ScholarPubMed
Loehlin, JC (1996). The Cholesky approach: a cautionary note. Behavior Genetics 26, 65–69.CrossRefGoogle Scholar
Lotfipour, S, Ferguson, E, Leonard, G, Perron, M, Pike, B, Richer, L, Seguin, JR, Toro, R, Veillette, S, Pausova, Z (2009). Orbitofrontal cortex and drug use during adolescence: role of prenatal exposure to maternal smoking and BDNF genotype. Archives of General Psychiatry 66, 1244–1252.CrossRefGoogle ScholarPubMed
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. Paediatric and Perinatal Epidemiology 24, 79–87.CrossRefGoogle ScholarPubMed
Maughan, B, Taylor, A, Caspi, A, Moffitt, TE (2004). Prenatal smoking and early childhood conduct problems: testing genetic and environmental explanations of the association. Archives of General Psychiatry 61, 836–843.CrossRefGoogle ScholarPubMed
Metcalfe, J, Mischel, W (1999). A hot/cool-system analysis of delay of gratification: dynamics of willpower. Psychological Review 106, 3–19.CrossRefGoogle ScholarPubMed
Monuteaux, MC, Blacker, D, Biederman, J, Fitzmaurice, G, Buka, SL (2006). Maternal smoking during pregnancy and offspring overt and covert conduct problems: a longitudinal study. Journal of Child Psychology and Psychiatry 47, 883–890.CrossRefGoogle ScholarPubMed
Muthén, LK, Muthén, BO (2010). Mplus User's Guide, 6th edition. Muthén & Muthén: Los Angeles, CA.Google Scholar
Neale, MC, Cardon, LRD (1992). Methodology for Genetic Studies of Twins and Families. Kluwer Academic Press: Dordrecht, The Netherlands.CrossRefGoogle Scholar
Neuman, RJ, Lobos, E, Reich, W, Henderson, CA, Sun, LW, Todd, RD (2007). Prenatal smoking exposure and dopaminergic genotypes interact to cause a severe ADHD subtype. Biological Psychiatry 61, 1320–1328.CrossRefGoogle Scholar
Office of Applied Studies (2007). Cigarette Use Among Pregnant Women and Recent Mothers. The National Survey of Drug Use and Health (NSDUH) Report. Mental Health Services Administration: Rockville, MD.Google 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:10.1136/jech.2009.095802.Google ScholarPubMed
Payton, JW, Wardlaw, DM, Graczyk, PA, Bloodworth, MR, Tompsett, CJ, Weissberg, RP (2000). Social and emotional learning: a framework for promoting mental health and reducing risk behavior in children and youth. Journal of School Health 70, 179–185.CrossRefGoogle ScholarPubMed
Pickett, KE, Kasza, K, Biesecker, G, Wright, RJ, Wakschlag, LS (2009). Women who remember, women who do not: a methodological study of maternal recall of smoking in pregnancy. Nicotine and Tobacco Research 11, 1166–1174.CrossRefGoogle Scholar
Plomin, R, DeFries, JC, Loehlin, JC (1977). Genotype-environment interaction and correlation in the analysis of human behavior. Psychological Bulletin 84, 309–322.CrossRefGoogle ScholarPubMed
Prescott, CA (2004). Using the Mplus computer program to estimate models for continuous and categorical data from twins. Behavior Genetics 34, 17–40.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, 2464–2467.CrossRefGoogle ScholarPubMed
Rutter, M, Pickles, A, Murray, R, Eaves, LJ (2001). Testing hypotheses on specific environmental causal effects on behavior. Psychological Bulletin 127, 291–324.CrossRefGoogle ScholarPubMed
Silberg, JL, Parr, T, Neale, MC, Rutter, M, Angold, A, Eaves, LJ (2003). Maternal smoking during pregnancy and risk to boys' conduct disturbance: an examination of the causal hypothesis. Biological Psychiatry 53, 130–135.CrossRefGoogle ScholarPubMed
Slotkin, TA (1998). Fetal nicotine or cocaine exposure: which one is worse? Journal of Pharmacology and Experimental Therapeutics 285, 931–945.Google ScholarPubMed
Solanto, MV, Abikoff, H, Sonuga-Barke, E, Schachar, R, Logan, GD, Wigal, T, Hechtman, L, Hinshaw, S, Turkel, E (2001). The ecological validity of delay aversion and response inhibition as measures of impulsivity in AD/HD: a supplement to the NIMH multimodal treatment study of AD/HD. Journal of Abnormal Child Psychology 29, 215–228.CrossRefGoogle Scholar
Statistics Sweden Educational attainment of the population 2001. Official statistics of Sweden UF 37 SM 0101, 2001: (http://www.scb.se/templates/Publikation__44633.asp).Google Scholar
Statistics Sweden (2006). Multi-Generation Register 2005 – A Description of Contents and Quality. Statistics Sweden: Örebro.Google Scholar
Thapar, A, Fowler, T, Rice, F, Scourfield, J, van den Bree, M, Thomas, H, Harold, G, Hay, D (2003). Maternal smoking during pregnancy and attention deficit hyperactivity disorder symptoms in offspring. American Journal of Psychiatry 160, 1985–1989.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, 722–727.CrossRefGoogle Scholar
Wakschlag, LS, Kistner, EO, Pine, DS, Biesecker, G, Pickett, KE, Skol, AD, Dukic, V, Blaire, RJR, Leventhal, BL, Cox, NJ, Burns, JL, Kasza, KE, Wright, RJ, Cook, EHJ (2010). Interaction of prenatal exposure to cigarettes and MAOA genotype in pathways to youth antisocial behavior. Molecular Psychiatry 15, 928–937.CrossRefGoogle ScholarPubMed
Wakschlag, LS, Leventhal, BL, Pine, DS, Pickett, KE, Carter, AS (2006). Elucidating early mechanisms of developmental psychopathology: the case of prenatal smoking and disruptive behavior. Child Development 77, 893–906.CrossRefGoogle ScholarPubMed
Weissman, MM, Warner, V, Wickramaratne, PJ, Kandel, DB (1999). Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. Journal of the American Academy of Child and Adolescent Psychiatry 38, 892–899.CrossRefGoogle ScholarPubMed
WHO (1992). The ICD-10 Classification of Mental and Behavioural Disorders: Clinical Descriptions and Diagnostic Guidelines. World Health Organization: Geneva.Google Scholar
Widiger, TA, Sankis, LM (2000). Adult psychopathology: issues and controversies. Annual Review of Psychology 51, 377–404.CrossRefGoogle ScholarPubMed
Wiebe, SA, Espy, KA, Stopp, C, Respass, J, Stewart, P, Jameson, TR, Gilbert, DG, Huggenvik, JI (2009). Gene-environment interactions across development: exploring DRD2 genotype and prenatal smoking effects on self-regulation. Developmental Psychology 45, 31–44.CrossRefGoogle ScholarPubMed