Many studies have established that a pregnant woman's smoking raises her child's risk of disruptive behavior disorders and of delinquency in the teen and young adult years, but its behavioral effects in early life have been been difficult to trace. Now, however, NIDA-funded researchers have revealed associations between a child's in utero exposure to smoking and specific patterns of aberrant behavior as a toddler, at school age, and as a teen. The researchers propose that these patterns form a continuum, united by an underlying theme of disrupted social information processing.
An Early Start to Disruptive Behavior
In an initial study, Dr. Lauren Wakschlag of the Institute for Juvenile Research at the University of Illinois at Chicago and her colleagues, Dr. Rolf Loeber of the University of Pittsburgh and Dr. Kate Pickett of The University of York in England, analyzed disruptive behavior patterns in first graders and subsequent problems that have been associated with later delinquency. Data were derived from the first-grade cohort of the Pittsburgh Youth Study (PYS), a community sample of boys at risk for delinquency who were followed over several decades under the direction of Dr. Loeber.
The researchers concentrated on 448 boys, who were roughly age 7 when the PYS study began. One hundred and sixty-six boys in this group had mothers who smoked during pregnancy. These boys developed the antisocial behavior pattern known as oppositional defiant disorder (ODD) at more than double the rate of the rest (see graph). Children with ODD demonstrate defiant, disobedient, and hostile behavior towards authority figures that persists for at least 6 months, and they are touchy, easily angered, and resentful. ODD is often considered a developmental precursor of conduct disorder (CD), a condition in older children and adolescents characterized by persistent antisocial behaviors such as lying, truancy, vandalism, and aggression.
Boys whose mothers smoked while pregnant did not have a higher incidence of attention deficit hyperactivity disorder (ADHD) without ODD than the nonexposed boys. However, the incidence of co-occurring ODD and ADHD—a combination that often results in chronic disruptive behavior problems—was nearly twice as high in the exposed group as in the nonexposed group. As the boys entered and traversed their teens, delinquent behavior began earlier and was more severe in the exposed group.
"All the children with ODD in the PYS study were diagnosed in first grade, meaning the disorder developed in the first 5 or 6 years of life. This provides evidence of a coherent developmental pathway from prenatal exposure to cigarettes to a subsequent sequence of conduct problems," Dr. Wakschlag says. "While previous research established a link between prenatal exposure to cigarettes and CD in older children, this study is the first to establish connections to ODD and to do so as early as first grade."
Toddlers With Troubles
To look for exposure-related behavioral abnormalities at even younger ages, Dr. Wakschlag's team conducted the Family Health and Development Project (FHDP), in collaboration with colleagues from the University of Illinois, The University of York, the National Institute of Mental Health, and the University of Massachusetts-Boston. The researchers recruited 96 expectant mothers, age 18 and older, at several clinics. The women were predominantly white and working class. Along with the women's self-reports, the researchers collected biological data, such as measurements of the nicotine metabolite cotinine in urine samples, to assess fetal exposure to maternal smoking. These measurements, taken three times during pregnancy, indicated that 47 percent of the women smoked throughout their pregnancies. Ninety-three infants and their mothers completed the study's developmental phase, which lasted until the babies were 24 months old.
The babies were evaluated every 6 months. At the 12-, 18-, and 24-month evaluations, each mother filled out the Infant-Toddler Social Emotional Assessment (ITSEA). During 20-minute laboratory observations of the toddlers and their mothers interacting at 24 months, the researchers rated specific components of the toddlers' behavior using codes from the Disruptive Behavior Diagnostic Observation Schedule.
The results indicated that toddlers whose mothers had smoked during pregnancy demonstrated a high and escalating pattern of disruptive behavior from 12 to 24 months, whereas nonexposed toddlers exhibited a relatively stable pattern. A mother's smoking during pregnancy increased the likelihood of the observed atypical trajectory of behavior independent of several associated risk factors, including parental antisocial behavior, quality of parenting, and postnatal exposure to tobacco smoke. At 24 months, toddlers whose mothers had smoked while pregnant were more than 11 times as likely as nonexposed peers to exhibit clinically significant patterns of disruptive behavior, shown on the ITSEA.
To more precisely determine the nature of the boys' behavior problems, the researchers examined four components of disruptive behavior, each of which is considered a precursor to disruptive behavior patterns seen at later ages:
- Aggressive/destructive behavior, including threatening, hitting, and throwing or smashing toys;
- Dysregulated negative affect, characterized by persistent, uncontrolled outbursts of anger with loud yelling, intense crying, and temper tantrums;
- Stubborn defiance, marked by obstructive behavior that persists after the mother has increased expressions of support for her child and has tried several strategies to change her child's behavior; and
- Low social competence, where the child misses social cues and exhibits low social interest or concern.
These four behaviors, while viewed as normal in toddlers, are considered precursors to clinical problems if they are severe or pervasive.
The children whose mothers had smoked during pregnancy displayed lower social competence than other children and significantly higher levels of aggressive/destructive behavior and stubborn defiance. They were not more likely to exhibit dysregulated negative affect.
"Dr. Wakschlag has teased out some components of disruptive behavior problems when they first emerge between 18 and 24 months of age," says Dr. Nicolette Borek of NIDA's Division of Clinical Neuroscience and Behavioral Research. "This gives us a way to identify at-risk children early and raises interesting questions about the role of brain development in later-stage behavioral issues."
On to Adolescence
Dr. Wakschlag and colleagues have hypothesized that the resistant, hostile, and unresponsive patterns of behavior demonstrated in FHDP, PYS, and similar studies may reflect disruptions in social-information processing that resulted from prenatal exposure to cigarette smoke. To test this hypothesis, the team is conducting the NIDA-funded East Boston Family Study (EBFS), which includes 272 adolescents and is a followup to the Maternal-Infant Smoking Study of East Boston (MISSEB). Dr. Wakschlag and her colleagues are also examining the influence of genetic makeup on exposure-related disruptive behavior among these young people. The researchers are using maternal exposure data originally collected by MISSEB but applying more sophisticated methods to measure prenatal exposure to cigarette smoke. These new techniques, which combine maternal self-report and biological data, were developed from FHDP-derived data by Dr. Vanja Dukic at the University of Chicago in collaboration with Dr. Neal Benowitz of the University of California, San Francisco and Dr. Wakschlag.
"Maternal self-reports are affected by memory lapses and social pressure not to smoke, and biological methods can be inaccurate because the smoke-derived chemicals have a short half-life and rates of metabolism differ among individuals," says Dr. Wakschlag. "In addition, we know that smoking levels fluctuate throughout a pregnancy. The new technique incorporates the unique information from both of these methods to provide a more precise estimate of prenatal exposure to cigarettes."
Wakschlag, L.S., et al. A developmental framework for distinguishing disruptive behavior from normative misbehavior in preschool children. Journal of Child Psychology and Psychiatry and Allied Disciplines 48 (10; Special Issue on Preschool Psychopathology):976-987, 2007. [Abstract]
Wakschlag, L.S., et al. Is prenatal smoking associated with a developmental pattern of conduct problems in young boys? Journal of the American Academy of Child and Adolescent Psychiatry 45(4):461-467, 2006. [Abstract]
Wakschlag, L.S., et al. Elucidating early mechanisms of developmental psychopathology: The case of prenatal smoking and disruptive behavior. Child Development 77(4):893-906, 2006. [Abstract]
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National Institute on Drug Abuse. Behavioral Problems Related to Maternal Smoking During Pregnancy Manifest Early in Childhood Retrieved from http://www.drugabuse.gov/news-events/nida-notes/2008/06/behavioral-problems-related-to-maternal-smoking-during-pregnancy-manifest-early-in-childhood