Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review.

OBJECTIVES Recent research suggests that in utero exposure to maternal smoking is a risk factor for conduct disorder and delinquency. We review evidence of causality, a controversial but important public health question. METHODS We analyzed studies of maternal prenatal smoking and offspring antisocial behavior within a causal framework. RESULTS The association is (1) independent of confounders, (2) present across diverse contexts, and (3) consistent with basic science. Methodological limitations of existing studies preclude causal conclusions. CONCLUSIONS Existing evidence provides consistent support for, but not proof of, an etiologic role for prenatal smoking in the onset of antisocial behavior. The possibility of identifying a preventable prenatal risk factor for a serious mental disorder makes further research on this topic important for public health.

[1]  P. Fried,et al.  Differential effects on cognitive functioning in 13- to 16-year-olds prenatally exposed to cigarettes and marihuana. , 1998, Neurotoxicology and teratology.

[2]  L. Wakschlag,et al.  Maternal smoking during pregnancy and conduct problems in high-risk youth: A developmental framework , 2002, Development and Psychopathology.

[3]  N. Benowitz,et al.  Accelerated metabolism of nicotine and cotinine in pregnant smokers. , 2002, The Journal of pharmacology and experimental therapeutics.

[4]  W. Velicer,et al.  Biochemical verification of tobacco use and cessation. , 2002, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[5]  B. Leventhal,et al.  Maternal smoking during pregnancy: Not a stable phenomenon , 2001 .

[6]  P. Eriksson,et al.  Neurobehavioural defects in adult mice neonatally exposed to nicotine: changes in nicotine-induced behaviour and maze learning performance , 2001, Behavioural Brain Research.

[7]  M. Ernst,et al.  Behavioral and neural consequences of prenatal exposure to nicotine. , 2001, Journal of the American Academy of Child and Adolescent Psychiatry.

[8]  H. Kraemer,et al.  How do risk factors work together? Mediators, moderators, and independent, overlapping, and proxy risk factors. , 2001, The American journal of psychiatry.

[9]  Lauren S. Wakschlag,et al.  Clinical Significance and Correlates of Disruptive Behavior in Environmentally At-Risk Preschoolers , 2001, Journal of clinical child psychology.

[10]  W. Slutske.  The genetics of antisocial behavior , 2001, Current psychiatry reports.

[11]  B. Zuckerman,et al.  Growth, development, and behavior in early childhood following prenatal cocaine exposure: a systematic review. , 2001, JAMA.

[12]  B. Leventhal,et al.  Smoking during pregnancy: Problematic health behavior or behavior problem? , 2001 .

[13]  S. Shawky,et al.  Cumulative impact of early maternal marital age during the childbearing period. , 2001, Paediatric and perinatal epidemiology.

[14]  D. Pine,et al.  Contribution of maternal smoking during pregnancy and lead exposure to early child behavior problems. , 2001, Neurotoxicology and teratology.

[15]  W. M. Kahler.  Tone abnormalities are associated with maternal cigarette smoking during pregnancy in in utero cocaine-exposed infants. , 2001, Pediatric physical therapy : the official publication of the Section on Pediatrics of the American Physical Therapy Association.

[16]  C. Orleans,et al.  Helping pregnant smokers quit: meeting the challenge in the next decade. , 2001, Tobacco control.

[17]  D P Farrington,et al.  Young children who commit crime: Epidemiology, developmental origins, risk factors, early interventions, and policy implications , 2000, Development and Psychopathology.

[18]  B. Leventhal,et al.  The association between maternal cigarette smoking and psychiatric diseases or criminal outcome in the offspring. , 2000, Reproductive toxicology.

[19]  B. Leventhal,et al.  Maternal Age at First Birth and Boys' Risk for Conduct Disorder , 2000 .

[20]  Chris L. Gibson,et al.  Assessing the relationship between maternal cigarette smoking during pregnancy and age at first police contact , 2000 .

[21]  C. Ehlers,et al.  Nicotine exposure during the neonatal brain growth spurt produces hyperactivity in preweanling rats. , 2000, Neurotoxicology and teratology.

[22]  D. Fergusson,et al.  Educational, psychosocial, and sexual outcomes of girls with conduct problems in early adolescence. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[23]  C. Nelson.  The Effects of Early Adversity on Neurobehavioral Development , 2000 .

[24]  D. Ferriero,et al.  Tone Abnormalities Are Associated With Maternal Cigarette Smoking During Pregnancy in In Utero Cocaine-Exposed Infants , 2000, Pediatrics.

[25]  M. Gillman,et al.  The fetal origins of adult disease: from sceptic to convert , 2000 .

[26]  G. Richardson,et al.  Effects of prenatal tobacco exposure on preschoolers' behavior. , 2000, Journal of developmental and behavioral pediatrics : JDBP.

[27]  C Osmond,et al.  Fetal, infant, and childhood growth are predictors of coronary heart disease, diabetes, and hypertension in adult men and women. , 2000, Environmental health perspectives.

[28]  E. J. van den Oord,et al.  Behavior problems among children from different family structures: the influence of genetic self-selection. , 2000, Child development.

[29]  U. Töllner,et al.  Parental Smoking and Neonatal Serum Levels of Polychlorinated Biphenyls and Hexachlorobenzene , 2000, Pediatric Research.

[30]  J. Brook,et al.  The influence of maternal smoking during pregnancy on the toddler's negativity. , 2000, Archives of pediatrics & adolescent medicine.

[31]  Chris L. Gibson,et al.  A Biosocial Interaction in Predicting Early Onset of Offending , 2000, Psychological reports.

[32]  J. A. Martin,et al.  Births: final data for 1998. , 2000, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[33]  Frank M. Scalzo,et al.  Can Adverse Neonatal Experiences Alter Brain Development and Subsequent Behavior? , 2000, Neonatology.

[34]  L. Wakschlag,et al.  More than the Terrible Twos: The Nature and Severity of Behavior Problems in Clinic-Referred Preschool Children , 2000, Journal of abnormal child psychology.

[35]  D. Holtzman,et al.  Trends in pregnancy-related smoking rates in the United States, 1987-1996. , 2000, JAMA.

[36]  K. Merikangas.  Familial and genetic factors and psychopathology. , 2000 .

[37]  B. Leventhal,et al.  Intergenerational health consequences of maternal smoking , 2000 .

[38]  J. Olsen.  Prenatal exposures and long-term health effects. , 2000, Epidemiologic reviews.

[39]  D. Glaser.  Child abuse and neglect and the brain--a review. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[40]  B. Eskenazi,et al.  Association of prenatal maternal or postnatal child environmental tobacco smoke exposure and neurodevelopmental and behavioral problems in children. , 1999, Environmental health perspectives.

[41]  G. Koren.  The association between maternal cigarette smoking and psychiatric diseases or criminal outcome in the offspring: a precautionary note about the assumption of causation. , 1999, Reproductive toxicology.

[42]  Tyrone D. Cannon,et al.  A prospective cohort study of neurodevelopmental processes in the genesis and epigenesis of schizophrenia , 1999, Development and Psychopathology.

[43]  S. Mednick,et al.  Prenatal teratogens and the development of adult mental illness , 1999, Development and Psychopathology.

[44]  Tyrone D. Cannon,et al.  Neurodevelopmental processes in the ontogenesis and epigenesis of psychopathology , 1999, Development and Psychopathology.

[45]  C. Nemeroff,et al.  The effects of neonatal stress on brain development: Implications for psychopathology , 1999, Development and Psychopathology.

[46]  E Susser,et al.  Prenatal exposure to wartime famine and development of antisocial personality disorder in early adulthood. , 1999, JAMA.

[47]  J. A. Martin,et al.  Births and deaths: preliminary data for July 1997-June 1998. , 1999, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[48]  M M Weissman,et al.  Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. , 1999, Journal of the American Academy of Child and Adolescent Psychiatry.

[49]  I. Waldman,et al.  Annotation: the development of antisocial behavior: an integrative causal model. , 1999, Journal of child psychology and psychiatry, and allied disciplines.

[50]  J. Tiihonen,et al.  Maternal smoking during pregnancy and risk of criminal behavior among adult male offspring in the Northern Finland 1966 Birth Cohort. , 1999, The American journal of psychiatry.

[51]  N. Benowitz,et al.  Biomarkers of environmental tobacco smoke exposure. , 1999, Environmental health perspectives.

[52]  S. Mednick,et al.  Maternal smoking during pregnancy and adult male criminal outcomes. , 1999, Archives of general psychiatry.

[53]  L. Wakschlag,et al.  Relation of maternal responsiveness during infancy to the development of behavior problems in high-risk youths. , 1999, Developmental psychology.

[54]  D. Fergusson.  Prenatal smoking and antisocial behavior. , 1999, Archives of general psychiatry.

[55]  A. Riley,et al.  Developmental Epidemiology of the Disruptive Behavior Disorders , 1999 .

[56]  J. Marshall,et al.  Mismeasurement and the resonance of strong confounders: correlated errors. , 1999, American journal of epidemiology.

[57]  Clark C. Presson,et al.  Maternal socialization of adolescent smoking: the intergenerational transmission of parenting and smoking. , 1998, Developmental psychology.

[58]  D. Capaldi,et al.  Prospective family predictors of aggression toward female partners for at-risk young men. , 1998, Developmental psychology.

[59]  S. Faraone,et al.  Further evidence of an association between maternal smoking during pregnancy and attention deficit hyperactivity disorder: findings from a high-risk sample of siblings. , 1998, Journal of clinical child psychology.

[60]  Chris L. Gibson,et al.  Interaction between Maternal Cigarette Smoking and Apgar Scores in Predicting Offending Behavior , 1998, Psychological reports.

[61]  B. Morse.  Fetal Alcohol Syndrome: A Guide for Families and Communities , 1998 .

[62]  D. Fergusson,et al.  Maternal smoking during pregnancy and psychiatric adjustment in late adolescence. , 1998, Archives of general psychiatry.

[63]  K. Pajer.  What happens to "bad" girls? A review of the adult outcomes of antisocial adolescent girls. , 1998, The American journal of psychiatry.

[64]  Gail M. Williams,et al.  Maternal Cigarette Smoking and Child Psychiatric Morbidity: A Longitudinal Study , 1998, Pediatrics.

[65]  T. Slotkin.  Fetal nicotine or cocaine exposure: which one is worse? , 1998, The Journal of pharmacology and experimental therapeutics.

[66]  J. Ajarem,et al.  Prenatal Nicotine Exposure Modifies Behavior of Mice Through Early Development , 1998, Pharmacology Biochemistry and Behavior.

[67]  Tobacco,et al.  Nicotine safety and toxicity , 1998 .

[68]  P. Fried,et al.  Differential effects on cognitive functioning in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. , 1998, Neurotoxicology and teratology.

[69]  F. Speizer,et al.  Maternal smoking during pregnancy, urine cotinine concentrations, and birth outcomes. A prospective cohort study. , 1997, International journal of epidemiology.

[70]  N. Grunberg,et al.  Hyperactivity Induced by Prenatal Nicotine Exposure Is Associated with an Increase in Cortical Nicotinic Receptors , 1997, Pharmacology Biochemistry and Behavior.

[71]  B. Leventhal,et al.  Maternal smoking during pregnancy and the risk of conduct disorder in boys. , 1997, Archives of general psychiatry.

[72]  M. Rutter,et al.  Nature–nurture integration: The example of antisocial behavior. , 1997 .

[73]  A. Kazdin,et al.  Practitioner review: psychosocial treatments for conduct disorder in children. , 1997, Journal of child psychology and psychiatry, and allied disciplines.

[74]  J. Mercy,et al.  Public health perspective on interpersonal violence among youths in the United States. , 1997 .

[75]  D. Olds.  Tobacco exposure and impaired development: A review of the evidence , 1997 .

[76]  D. Stoff,et al.  Handbook of antisocial behavior , 1997 .

[77]  Phil A. Silva,et al.  Adult mental health and social outcomes of adolescent girls with depression and conduct disorder , 1996, Development and Psychopathology.

[78]  S. Faraone,et al.  Is maternal smoking during pregnancy a risk factor for attention deficit hyperactivity disorder in children , 1996 .

[79]  B. Marcus,et al.  The impact of depression on smoking cessation in women. , 1996, American journal of preventive medicine.

[80]  J. R. Marshall,et al.  Mismeasurement and the resonance of strong confounders: uncorrelated errors. , 1996, American journal of epidemiology.

[81]  R. Tremblay,et al.  DSM-III-R and DSM-III criteria for conduct disorder in preadolescent girls: specific but insensitive. , 1996, Journal of the American Academy of Child and Adolescent Psychiatry.

[82]  Hans Sl.  Prenatal drug exposure: behavioral functioning in late childhood and adolescence. , 1996 .

[83]  S. Hans,et al.  Prenatal drug exposure: behavioral functioning in late childhood and adolescence. , 1996, NIDA research monograph.

[84]  D. Kandel,et al.  The Contributions of Mothers and Fathers to the Intergenerational Transmission of Cigarette Smoking in Adolescence , 1995 .

[85]  Walsh Ra,et al.  Effects of maternal smoking on adverse pregnancy outcomes: examination of the criteria of causation. , 1994 .

[86]  S A Mednick,et al.  Birth complications combined with early maternal rejection at age 1 year predispose to violent crime at age 18 years. , 1994, Archives of general psychiatry.

[87]  C. Pritchard,et al.  Depression and smoking in pregnancy in Scotland. , 1994, Journal of epidemiology and community health.

[88]  Yousef Tizabi,et al.  Hyperactivity in the offspring of nicotine-treated rats: Role of the mesolimbic and nigrostriatal dopaminergic pathways , 1994, Pharmacology Biochemistry and Behavior.

[89]  P. Cole,et al.  The development of emotion regulation and dysregulation: a clinical perspective. , 1994, Monographs of the Society for Research in Child Development.

[90]  Nathan A. Fox,et al.  The development of emotion regulation : biological and behavioral considerations , 1994 .

[91]  R. Walsh.  Effects of maternal smoking on adverse pregnancy outcomes: examination of the criteria of causation. , 1994, Human biology.

[92]  R. Windsor,et al.  The impact on infant birth weight and gestational age of cotinine-validated smoking reduction during pregnancy. , 1993, JAMA.

[93]  M. Zoccolillo.  Gender and the development of conduct disorder , 1993, Development and Psychopathology.

[94]  Terrie E. Moffitt,et al.  The neuropsychology of conduct disorder , 1993, Development and Psychopathology.

[95]  S. Hyman,et al.  The Molecular Foundations Of Psychiatry , 1993 .

[96]  M. Schlumpf,et al.  Prenatal nicotine exposure: biochemical and neuroendocrine bases of behavioral dysfunction , 1993 .

[97]  J. Groenewoud,et al.  Maternal smoking during pregnancy and delinquency of the offspring: an association without causation? , 1993, International journal of epidemiology.

[98]  N. Breslau,et al.  Nicotine dependence and major depression. New evidence from a prospective investigation. , 1993, Archives of general psychiatry.

[99]  E. Alberman,et al.  Effects of smoking on the fetus, neonate, and child , 1992 .

[100]  J. Samet.  Health benefits of smoking cessation. , 1991, Clinics in chest medicine.

[101]  M. Weissman,et al.  Family risk factors, parental depression, and psychopathology in offspring. , 1990 .

[102]  H. A. Navarro,et al.  Prenatal exposure to nicotine impairs nervous system development at a dose which does not affect viability or growth , 1989, Brain Research Bulletin.

[103]  M. Stitzer,et al.  Cigarette brand-switching: effects on smoke exposure and smoking behavior. , 1988, The Journal of pharmacology and experimental therapeutics.

[104]  R. Loeber,et al.  Family Factors as Correlates and Predictors of Juvenile Conduct Problems and Delinquency , 1986, Crime and Justice.

[105]  J. Valdés,et al.  Postnatal alterations in cerebellar GABA content, GABA uptake and morphology following exposure to carbon monoxide early in development. , 1986, Developmental neuroscience.

[106]  J. Singh.  Early behavioral alterations in mice following prenatal carbon monoxide exposure. , 1986, Neurotoxicology.

[107]  N. Morris,et al.  Crime and justice : an annual review of research , 1980 .

[108]  C. Buck.  Popper's philosophy for epidemiologists. , 1976, International journal of epidemiology.