J Abnorm Child Psychol (2007) 35:203–215
DOI 10.1007/s10802-006-9073-4
ORIGINAL PAPER
Associations of Maternal Prenatal Smoking with Early Childhood
Physical Aggression, Hyperactivity-Impulsivity,
and Their Co-Occurrence
Stephan C. J. Huijbregts · Jean R. Séguin ·
Mark Zoccolillo · Michel Boivin · Richard E. Tremblay
Published online: 10 February 2007
C Springer Science+Business Media, LLC 2007
Abstract This study investigated associations between
maternal prenatal smoking and physical aggression (PA),
hyperactivity-impulsivity (HI) and co-occurring PA and HI
between ages 17 and 42 months in a population sample of
children born in Québec (Canada) in 1997/1998 (N = 1745).
Trajectory model estimation showed three distinct developmental patterns for PA and four for HI. Multinomial regression analyses showed that prenatal smoking significantly predicted children’s likelihood to follow different PA trajectories
beyond the effects of other perinatal factors, parental psychopathology, family functioning and parenting, and socioeconomic factors. However, prenatal smoking was not a significant predictor of HI in a model with the same control
variables. Further multinomial regression analyses showed
that, together with gender, presence of siblings and maternal
S. C. J. Huijbregts ()
Department of Clinical Child and Adolescent Studies, Section
Neurodevelopmental Disorders, Faculty of Social Sciences,
Leiden University,
P.O. Box 9555, 2300 RB Leiden, The Netherlands
e-mail: SHuijbregts@fsw.leidenuniv.nl
J. R. Séguin
Department of Psychiatry, University of Montreal,
Montreal, Canada
M. Zoccolillo
Department of Psychiatry, McGill University,
Montreal, Canada
M. Boivin
Department of Psychology, Laval University,
Quebec City, Canada
R. E. Tremblay
Departments of Psychiatry, Pediatrics, and Psychology,
University of Montreal,
Montreal, Canada
hostile reactive parenting, prenatal smoking independently
predicted co-occurring high PA and high HI compared to
low levels of both behaviors, to high PA alone, and to high
HI alone. These results show that maternal prenatal smoking predicts multiple behavior regulation problems in early
childhood.
Keywords Prenatal smoking . Physical aggression .
Hyperactivity . Impulsivity . Comorbidity
The literature on maternal prenatal smoking and externalizing behavior problems is clearly separated in two developmental periods. The bulk of the current literature on maternal
prenatal smoking and externalizing behavior problems covers either childhood and adolescence or the preschool years.
However, the rates of common childhood psychiatric disorders such as conduct disorder (CD) and attention deficit hyperactivity disorder (ADHD) and the patterns of comorbidity
among them in early childhood are similar to those seen in
later childhood (Egger & Angold, 2006). Limitations in current diagnostic criteria for early childhood psychopathology
have resulted in a research focus on specific behaviors such
as physical aggression (PA) and hyperactivity-impulsivity
(HI) rather than clinical disorders in this age group. Both
physical aggression and hyperactivity during early childhood appear to be typical precursors of full-blown CD and
ADHD during the school years and beyond (Séguin, Nagin,
Assaad, & Tremblay, 2004). A substantial number of studies
show continuity between early and late childhood externalizing behavior problems (e.g. Campbell, Breaux, Ewing, &
Szumowski, 1986; Keenan & Wakschlag, 2000) or have identified consistent developmental trajectories for PA and HI
that start as early as age 1 1/2 years (e.g. Côté, Vaillancourt,
LeBlanc, Nagin, & Tremblay, 2006; NICHD Early Child
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Care Research Network, 2004; Romano, Tremblay, Farhat,
& Côté, 2006; Shaw, Lacourse, & Nagin, 2005).
In reviewing childhood and adolescence studies, maternal prenatal smoking has consistently been associated with
CD- and ADHD- symptoms (for reviews, see Linnet et al.,
2003; Wakschlag, Pickett, Cook, Benowitz, & Leventhal,
2002). The associations have been observed in clinical samples (e.g. Mick, Biederman, Faraone, Sayer, & Kleinman,
2002; Milberger, Biederman, Faraone, Chen, & Jones, 1996),
‘at-risk’ samples (e.g. Wakschlag & Hans, 2002) and large
population-based samples (e.g. Braun, Kahn, Froehlich,
Auinger, & Lanphaer, 2006; Kotimaa et al., 2003). Whereas
these studies generally controlled for familial psychopathology and numerous environmental risk factors, there are also
indications from studies using (large) twin samples that maternal prenatal smoking predicts children’s CD- and ADHDsymptoms beyond the effects of heritable risk (e.g. Button,
Thapar, & McGuffin, 2005; Maughan, Taylor, Caspi, &
Moffitt, 2004; Silberg et al., 2003; Thapar et al., 2003). Studies showing associations between maternal prenatal smoking
and CD-symptoms and delinquency during adolescence and
adulthood (Brennan, Grekin, Mortensen, & Mednick, 2002;
Fergusson, Woodward, & Horwood, 1998; Räsänen et al.,
1999) and studies showing behavior problems in children
of mothers who smoked during pregnancy at different time
points (e.g. Maughan et al., 2004; Wakschlag & Hans, 2002;
Wakschlag, Pickett, Kasza, & Loeber, 2006) suggest longlasting effects.
Although there are indications that maternal prenatal
smoking is more strongly or even exclusively related to
CD symptoms (Wakschlag & Hans, 2002; Wakschlag,
Leventhal, Pine, Pickett, & Carter, 2006; Wakschlag,
Pickett et al., 2006), only few studies tested for specificity
of the relations between maternal prenatal smoking and CDor ADHD-symptoms (Button et al., 2005; Mick et al., 2002;
Thapar et al., 2003). This is an important matter considering the high comorbidity of these behavior problems (e.g.
Jensen, Martin, & Cantwell, 1997). Mick et al. (2002) found
a robust link with ADHD-symptoms after controlling for
CD-symptoms in a clinical population. In that study, children aged 6 to 17 years with ADHD and non-ADHD controls
were compared after statistical control for CD. In contrast,
Thapar et al.’s (2003) and Button et al.’s (2005) populationbased twin study using the Greater Manchester Twin Register
did not select on either CD- or ADHD-symptoms. Whereas
Thapar et al. showed that prenatal maternal smoking predicted a unique proportion of the variance in ADHDsymptoms after control for CD-symptoms in children between 5 and 16 years, Button et al. (2005) tested a
more complex model showing unique variance for both
CD- and ADHD-symptoms in children 5 to 18 years
of age. Although the aforementioned studies used some
form of statistical control for the symptoms associated
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J Abnorm Child Psychol (2007) 35:203–215
with the ‘other’ disorder, only one study to date examined a relation between prenatal maternal smoking
and co-occurring behavior problems (Wakschlag, Pickett
et al., 2006). In that study maternal prenatal smoking predicted the co-occurrence of Oppositional Defiant Disorder
(ODD) and ADHD when high levels of both were contrasted
with absence of both. This suggests that maternal prenatal
smoking, to the extent that it is a causal factor, may affect
behavior much more seriously than initially shown in specificity studies. However, such a conclusion may be premature
because that analysis did not inform us if maternal prenatal
smoking was related specifically to the co-occurrence of both
behavior problems or whether it was driven by its association
with either behavior problem because we do not know if the
combined group differed from the ODD-only or ADHD-only
groups. Thus whether maternal prenatal smoking is related
to the co-occurrence of behavior problems remains an open
question in this literature.
In contrast to childhood and adolescence studies, there is
a more limited number of early childhood studies and they
tend to focus on symptoms rather than diagnoses. Tremblay
et al. (2004) reported an association with early childhood
trajectories of PA across time, and Romano et al. (2006)
found an association between maternal prenatal smoking
and hyperactive symptoms from age 2 to 7, but both studies focused on one externalizing behavior problem. Other
studies focused on multiple behaviors. Orlebeke, Knol, and
Verhulst (1997) and Williams et al. (1998), using the Child
Behavior Checklist (CBCL) in large cohort studies of 3year-old and 4 to 6-year old children, respectively, found
associations with externalizing behavior problems (aggressive, overactive, oppositional) but not with internalizing
behavior problems (withdrawn, anxious, depressed). Day,
Richardson, Goldschmidt, and Cornelius (2000) reported
significant associations of third trimester exposure with
scores on each of the subscales of the Toddler Behavior Checklist (Physical Aggression, Oppositional Behavior,
Immaturity, and Emotionality) and Activity level assessed
with the Routh Activity Scale. Wakschlag, Leventhal et al.
(2006) noted a persistent association between maternal prenatal smoking and disruptive behaviors during early childhood. None of these multiple behavior studies examined
co-occurrence. Thus there also remains a need in the early
childhood literature to examine whether maternal prenatal
smoking is specifically associated with the co-occurrence of
problem behaviors.
From a developmental perspective, early onset of externalizing behavior has been associated with the poorest outcomes
(Brame, Nagin, & Tremblay, 2001; Lacourse et al., 2006;
Moffitt, 1993; Woodward, Fergusson, & Horwood, 2002).
In addition, co-occurring externalizing behaviors during
middle childhood have been associated with the poorest behavioral outcomes during adolescence and adulthood
J Abnorm Child Psychol (2007) 35:203–215
(Lacourse et al., 2006; Lahey, McBurnett, & Loeber, 2000;
Séguin et al., 2004). However, co-occurring behavior problems may be etiologically different from individual behavior
problems, with their own social, sociodemographic and biological precursors (Waschbusch, 2002). Yet, we know very
little about the prenatal markers of co-occurring behavior
problems in general. Given that maternal prenatal smoking
has been clearly associated with several single externalizing
problems across development, in the present study, we test
the hypothesis that maternal prenatal smoking is associated
with co-occurring externalizing problems. Specifically we
predict that maternal prenatal smoking will be associated to
the co-occurrence of PA and HI in contrast with the absence
of both, PA-only, and HI-only in a large early childhood
sample.
Methods
Participants
The children of this study were born in 1997/1998 in the
province of Québec, Canada and participate in the Québec
Longitudinal Study of Children’s Development. This sample excluded very remote regions of the province populated mainly by aboriginal people (2.1% of live births),
babies for whom gestational age could not be computed
(1.3%), babies born in a different territory but whose parents reside in Québec (4.5%), and very premature babies
(<24 weeks) and babies for whom there were delays
in filing the birth records in the Master Birth Registry
on time for the first assessment, i.e. babies born after
42 weeks gestation (0.1%; for full details, see Jetté & Des
Groseilliers, 2000). A total of 2940 infants met inclusion
criteria and were selected through a region-based stratification procedure (Jetté & Des Groseilliers, 2000). Of this
original selection, a number of families could not be included in the initial 5 month-assessment for the following
reasons: (1) Families not found on time (incorrect address/
tel no.) (n = 172, 5.9%); (2) Families excluded (total n = 93,
3.2%) because of death of the baby (n = 5), because of
participation in other longitudinal studies (n = 5), because
they had no command of either English or French language (n = 81), or because the instruments of the study
were not designed to adequately measure development of
children with severe physical or mental handicaps (n = 2);
(3) Families that could not be reached (n = 14, 0.5%); (4)
Families who declined participating (n = 438, 16.4%). 2223
Families (75.6%) took part in the first assessment, which
took place when the infants were 5 months old. Demographic characteristics of this Québec sample were comparable to those of a large Canadian sample consisting
of 13,439 households which contains sufficient samples
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Table 1
Demographic characteristics of families enrolled in the
Québec Longitudinal Study of Children’s Development (QLSCD 1)
(n max = 2223) and families included in the present study (QLSCD 2:
n = 1745)
QLSCD 1
n
%
Sex of child
Male
Female
Age of mother at birth of first child
21 years or less
Older than 21 years
Mother graduated from high school
Yes
No
Family status
Two parents
One parent
Number of siblings in the home
None
One or more
Family income
Less than 30,000$
30,000$–50,000$
50,000$–80,000$
More than 80,000$
QLSCD 2
n
%
1,123
1,069
51.2
48.8
884
861
50.7
49.3
471
1648
22.2
77.8
372
1373
21.3
78.7
1865
355
84.0
16.0
1504
241
86.2
13.8
1617
424
79.2
20.8
1407
338
80.6
19.4
830
1215
40.6
59.4
713
1032
40.9
59.1
639
625
611
307
29.3
28.7
28.0
14.1
468
527
499
251
26.8
30.2
28.6
14.4
Data courtesy of the Institut de la Statistique du Québec.
from each of the 10 Canadian provinces (Human Resources
Development Canada, 1996: National Longitudinal Survey
of Children and Youth, 1994–1995). Assessments relevant
to this study took place at 17, 30 and 42 months. Parental
informed consent was obtained before every assessment. 478
participants had either dropped out since the initial assessment at 5 months or had missing values for PA, HI or one
or more predictor variables. Thus, the final study sample
consisted of 1745 children (78.5% of families enrolled at
5 months). Table 1 indicates that, despite the fact there was
a slight tendency for less advantaged families to drop out or
have missing values on relevant variables, demographic characteristics were largely similar for in- and excluded families.
Measurements
Maternal prenatal smoking
When the child was 5 months of age, mothers filled out
a number of questionnaires. One set of questions concerned substance use (alcohol, tobacco, and illegal drugs)
during pregnancy. The questions assessing smoking behavior during pregnancy were straightforward, ‘Did you
smoke during pregnancy?’ and ‘How many cigarettes/day
did you smoke whilst pregnant?’ We also asked when during pregnancy the mother had smoked, i.e. (only) in the
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first, second or third trimester or throughout pregnancy.
These questions are similar to those found in most other assessment instruments (e.g., the Centers for Disease Control
and Prevention (CDC) Pregnancy Risk Assessment Monitoring System (PRAMS) Questionnaire, see Beck et al.,
2002) and like those found in most other studies (particularly those assessing large samples, e.g. Button et al., 2005;
Fergusson et al., 1998; Maughan et al., 2004; Thapar et al.,
2003; Wakschlag et al., 1997; Wakschlag & Hans, 2002).
Because amount of cigarettes reportedly smoked tends to be
a ‘rounded’ number, e.g. 5, 10, 15, etc, mothers were classified into 1 of 4 groups (0, 1–9, 10–19, or ≥20 cigarettes/day).
This or similar classifications have been used in most other
studies investigating smoking during pregnancy (e.g. Button
et al., 2005; Fergusson et al., 1998; Maughan et al., 2004;
Thapar et al., 2003; Wakschlag et al., 1997; Wakschlag &
Hans, 2002). Although there is a risk for a social desirability
bias, several studies have indicated a relatively strong association between retrospective self-report and blood/urine
cotinine-levels (i.e. the main nicotine metabolite) (e.g. Law
et al., 2003; Pickett, Rathouz, Kasza, Wakschlag, & Wright,
2005). Further reliance on self-report measures may be inferred from the strong relation between the amount reportedly smoked during pregnancy and birth weight (e.g.
Huijbregts et al., 2006; Kramer et al., 2001). Other studies have shown that whereas for some prenatal exposures
(e.g. alcohol, drugs) higher levels were reported postnatally
than antenatally, this was not the case for tobacco exposure,
which might indicate that smoking is considered a more habitual behavior that is more reliably recalled (e.g. Jacobsen,
Chiodo, Sokol, & Jacobson, 2002). For the current analyses,
1307 (74.9%) mothers reported not to have smoked during pregnancy, 202 (11.6%) reported to have smoked 1–9
cigarettes/day, 174 (10%) between 10 and 19, and 62 (3.6%)
reported to have smoked 20 or more cigarettes/day during
pregnancy.
Physical aggression and hyperactivity-impulsivity
Maternal ratings of child behavior were obtained with the
use of an early childhood behavior scale from the Canadian
National Longitudinal Study of Children and Youth (Statistics Canada, 1995), which incorporates items from the Child
Behavior Checklist for Ages 2–3 (Achenbach, Edelbrock,
& Howell, 1987), the Ontario Child Health Study Scales
(Offord, Boyle, & Racine, 1989), and the Preschool Behavior Questionnaire (Tremblay, Desmarais-Gervais, Gagnon,
& Charlebois, 1987). In order to assess PA mothers were
asked at 17, 30 and 42 months to indicate whether the child:
(1) hits, bites, kicks; (2) fights; and (3) bullies others. The
items for HI were: (1) can’t sit still, is restless (or hyperactive), (2) fidgets, (3) cannot settle down to do anything
for more than a few moments, (4) is impulsive, acts without
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thinking, and (5) has difficulty waiting for turn in games.
The first three representing hyperactivity, and the latter two
representing impulsivity. The items were scored as follows:
never or not true (score = 0), sometimes or somewhat
true (score = 1), or often or very true (score = 2). The
items were summed to obtain PA (range = 0 to 6) and HI
scores (range = 0 to 10). The internal consistency values
(Cronbach’s α) for PA were 0.80 at 17 months, 0.82 at 30
months, and 0.72 at 42 months. For HI they were 0.75, 0.75,
and 0.71, respectively. The scales were shown to have good
discriminant validity in the prediction of different types of
adolescent criminal behaviors (Broidy et al., 2003; Nagin
& Tremblay, 1999), and although correlated, the PA and HI
scales were related in predictable ways with mother and child
reports of CD and ADHD, respectively (Séguin et al., 2004).
Their validity in early childhood is also well established
(Tremblay et al., 2004; Romano et al., 2006).
Control variables
Potential confounders of associations between maternal prenatal smoking and early behavior problems were selected
from four key domains: demographic factors (age at birth of
first child, family status (separation/divorce: yes/no), presence of siblings, family income, maternal education); perinatal factors (alcohol and drug exposure during pregnancy,
birth weight); family functioning and parenting (hostile reactive parenting, responsiveness, involvement), and parental
background and mental health (mother’s and father’s history of antisocial behavior, maternal depression). Mothers
provided information on most of these factors when their
child was 5 months of age and again when their child was
17 months of age.
Family income was indicated on a 7-point scale (1 = less
than $10,000 (Canadian) to 8 = more than $80,000, as was
maternal education (1 = no high school diploma to 7 =
university degree). The poverty line in Canada is situated at
around $15,000 per capita (Statistics Canada, 2006).
Perinatal factors included exposure to illegal drugs
(yes/no) and alcohol (7-point scale ranging from ‘never’ to
‘daily’) during pregnancy and birth weight. Birth weight
and gestational age were derived from birth records. Birth
weight for gestational age was standardized within gender
for each week of gestation using Canadian norms (Kramer
et al., 2001).
Parenting measures were obtained by observing the
mother-child dyad during home visits at 5 and 17 months
using the Home Observation for Measurement of the Environment (HOME)-Infant version (Caldwell & Bradley,
1984). The observations were carried out by trained observers who spent about 3 hours in the home to complete a
battery of questionnaires and tests. These observers received
a one-week training session and were closely supervised
J Abnorm Child Psychol (2007) 35:203–215
during the data collection. Three scales were obtained: hostile reactive parenting (e.g. “talks negatively about her child,”
“shouts at her child,” “hits or physically punishes her child”;
α = 0.43 at 5 months and 0.73 at 17 months), responsiveness
(e.g. “responds verbally to child’s vocalizations or verbalizations,” “tells child name of object or person during the visit,”
“spontaneously praises the child at least twice”; α = 0.85 at
5 months and 0.83 at 17 months), and involvement (e.g.
“provides toys that challenge child to develop new skills,”
“structures child’s play periods”; α = 0.85 at 5 months and
0.88 at 17 months). Scores for each item on each scale ranged
from 1 (never) to 5 (all the time). Only the scale score for
hostile reactive parenting at 17 months was used because of
the low internal reliability of this scale at 5 months. Mean
scores across the 5 and 17 months assessments were used for
the responsiveness and involvement scales.
Family functioning (at 5 and 17 months) was assessed
with a scale containing 12 items measuring communication,
problem resolution, control of disruptive behavior, and showing and receiving affection (Statistics Canada, 1995). Scores
per item could be 0 (‘never’), 1 (‘sometimes’), or 2 (‘often’),
thus ranging from 0 to 36 on the scale. The Cronbach α’s
were 0.86 (5 months) and 0.98 (17 months).
In order to assess history of antisocial behavior, both
parents completed a questionnaire at the 5-month assessment. The questionnaire included items related to childhood/adolescence (i.e. the period before the end of high
school) and items related to adulthood (Zoccolillo, 2000;
see also Tremblay et al., 2004), and was largely derived from
the NIMH-Diagnostic Interview Schedule (Robins, Helzer,
Croughan, & Radcliff, 1981). Childhood/adolescence items
included ‘starting fights,’ theft, involvement with youth protection or police, expulsion or suspension from school, truancy, and running away from home. Adult items included
arrests (other than for traffic violations), being fired from a
job (excluding layoffs for lack of work), trouble at work,
with family, or with the police due to drug or alcohol abuse,
‘starting fights’ (fathers), and ‘hitting or throwing things at
the spouse or partner’ (mothers). Adolescent and adult scores
(0 = no, 1 = yes) were summed for mothers and for fathers.
Internal reliability for mother’s items was 0.54 (Cronbach’s
α) and 0.59 for father’s items. Latent class analysis identified 3-class models for both mothers ((1) not antisocial, (2)
moderately antisocial, (3) antisocial) and fathers ((1) not antisocial, (2) antisocial as an adolescent but not as an adult,
(3) moderately antisocial as an adolescent, antisocial as an
adult). The Center for Epidemiological Studies-Depression
Scale (CES-D; Radloff, 1977) was used for report of symptoms associated with depression (at 5 and 17 months).
Studies have shown that all these factors are associated with increased risk for physical aggression, hyperactivity, CD- and ADHD-symptoms and with prenatal maternal smoking (e.g. Biederman, Milberger, & Faraone, 1995;
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Campbell, Shaw, & Gilliom, 2000; Huijbregts et al., 2006;
Linnet et al., 2003; Maughan et al., 2004; NICHD ECCRN, 2004; Tremblay et al., 2004; Nagin & Tremblay, 2001;
Romano et al., 2006; Shaw et al., 2005). Apart from the dichotomous variables (i.e. gender, presence of siblings, drug
use during pregnancy, family status), all scores were standardized for statistical analyses.
Data analyses
Assignment to trajectories
Scores from the three assessment points were analyzed
to identify distinctive behavioral trajectories across time
(Nagin, 1999, 2005; Nagin & Tremblay, 2001). Rather than
to assume that all children follow the same developmental
pattern, this methodology identifies different groups of individuals who tend follow similar patterns over time. For
example, some children may never show a given problem
behavior (intercept model or zero order polynomial), others may show constant high levels (also intercept model),
and others may increase or decrease over time (e.g., linear –
1st, quadratic – 2nd, or cubic – 3rd order polynomials). The
methodology can also be adapted to accommodate various
data distributions (i.e., binary, censored normal, zero-inflated
Poisson, and count data). The trajectory methodology uses
all available developmental data points and assigns individuals to trajectories on the basis of a posterior probability
rule. Resulting groups are meant to represent approximations of an underlying continuous process. In order to identify the model that best represents development of a specific
behavior during a given time frame, models with a varying number of trajectories are estimated. Model selection is
dependent on a combination of statistical and investigatorguided concerns. Besides a need to determine the best model
for the data distribution, key decisions are also based on
Bayesian fit indices for model selection in accordance to
procedures described by Nagin (2005), e.g. the higher the
Bayesian Information Criterion (BIC), the better. The optimal model is thus also determined by adding trajectories to
the model until the BIC ceases to improve. The investigator
would then have enough information to determine the best
model.
A key output of model estimation is the posterior probability of group membership. For each trajectory group this
probability measures the likelihood of an individual of belonging to that trajectory group based on observations across
assessments. In other words, 100% accuracy in classification
is not assumed nor required. For example, in the case of an
individual who scores high on hyperactivity at all assessment periods, the posterior probability of membership to
the chronic group would be high whereas the probability
of membership to the low trajectory group would be near 0.
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Participants can be assigned to the trajectory group for which
they show the highest probability of belonging. Ideally, the
posterior membership probability should be near 1 for this
trajectory group. Further, when trajectories are joined, conditional and joint probabilities can be used to further describe
the relationship between the joint factors. Posterior probabilities will then be applied to weight PA, HI and their
combination when they enter further analyses (see Séguin
et al., 2004).
Prediction of physical aggression, hyperactivity/impulsivity,
and their co-occurrence
Weighted multinomial regressions were conducted with
PROC CATMOD in SAS v.8.2. (SAS Institute Inc., 2001).
First, weighted multinomial regressions were conducted separately on PA and HI between ages 17 and 42 months for descriptive purposes. The influence of maternal prenatal smoking on these behaviors was investigated in analyses with and
without control variables.
For the second set of analyses predicting PA and HI between ages 17 and 42 months, we contrasted, in weighted
multinomial regression, those children who were high on
both PA and HI (combined group), to those who were only
high on PA (PA only group), to those only high on HI (HI
only group) and to the remainder of the sample.
Results
Assignment to trajectories
Models with between 2 to 5 trajectories and varied shapes for
each trajectory were compared using BIC for both PA and
HI. Three trajectories were modeled for PA between ages 17
and 42 months using a zero-inflated Poisson distribution: a
consistently low, a moderate and rising, and a high and rising
trajectory, each representing respectively 25, 50, and 25% of
the sample, all of these were best modeled using a linear
trend except for the low group which was best represented
by a constant term (Fig. 1, left panel). The shape and level of
the PA trajectories were very similar to those we identified
in Tremblay et al., 2004, in a smaller sample using the same
measures. It reveals that most of the children show an increase of physical aggression over time, which is consistent
with other longitudinal and cross sectional studies of early
childhood.
Four trajectories were modeled for HI using a censored
normal distribution: consistently low, low to moderate, moderate to high and chronic HI, representing respectively, 12,
45, 37, and 6% of the sample. All were best modeled by a
constant term except for the low to moderate group that was
best modeled with a quadratic trend (Fig. 1, right panel).
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J Abnorm Child Psychol (2007) 35:203–215
Thus in contrast to PA, HI in early childhood appears to be
more stable in level across time, with very few children being
atypically high.
In the current models for PA and HI the average posterior probability for the assigned trajectory group ranged
between .75 and .83, thereby indicating good fit (Nagin,
1999, 2005). Further, a close match of predicted and observed means shown in Fig. 1 also illustrates this good fit.
Models with three trajectories for PA and four trajectories for
HI have also produced the best fit in studies using other samples that included children in early childhood (e.g. Tremblay
et al., 2004; Côté et al., 2006; Romano et al., 2006; Shaw
et al., 2005).
Physical aggression
A first multinomial regression revealed that maternal prenatal smoking significantly predicted PA. In an analysis without control variables, both the odds ratio (OR) contrasts between high and low PA [OR = 1.49 (95% CI: 1.25 to 1.75),
2
= 21.0, p < .001] and between high and moderate PA
χ(1)
2
[OR = 1.27 (95% CI: 1.11 to 1.45), χ(1)
= 12.8, p < .001]
were significantly predicted by maternal prenatal smoking
2
= 23.6, p < .001; see also Table 2). The ORs represent
(χ(2)
one categorical increase in maternal prenatal smoking, i.e.
from ‘0 cigarettes/day’ to ‘1–9,’ ‘1–9’ to ‘10–19,’ and from
‘10–19’ to ≥20 cigarettes/day.
Maternal prenatal smoking was also a significant predictor of PA in a multinomial regression with control factors
2
= 8.4, p = .015]. The ORs were reduced to 1.33 (95%
[χ(2)
2
CI: 1.10 to 1.61) [χ(1)
= 8.1, p = .004] for the contrast between high and low PA, and to 1.16 (95% CI: 0.99 to 1.35)
2
= 3.3, p = .057] for the contrast between high and mod[χ(1)
erate PA. Other significant predictors of PA between ages 17
2
= 22.0, p < .001], presand 42 months were gender [χ(2)
2
ence of siblings [χ(2) = 86.2, p < .001], and hostile reactive
2
parenting (by the mother) [χ(2)
= 23.6, p < .001].
Hyperactivity-impulsivity
A first multinomial regression predicting HI without control
variables revealed significant contrasts between high and
2
= 15.1,
low HI [OR = 1.75 (95% CI: 1.32 to 2.33), χ(1)
p < .001], between high and low-moderate HI [OR = 1.49
2
= 13.1, p < .001] and high
(95% CI: 1.20 to 1.85), χ(1)
and moderate-high HI [OR = 1.25 (95% CI: 1.01 to 1.56),
2
= 4.1, p = .043], resulting in an overall significant efχ(1)
2
fect (χ(3)
= 22.8, p < .001). In a second multinomial regression with control variables the association of maternal prenatal smoking with HI was strongly attenuated, although
the overall effect was still not too far from significance
2
= 5.8, p = .12] (see also Table 2). This attenuation
[χ(3)
J Abnorm Child Psychol (2007) 35:203–215
209
Physical Aggression
Hyperactivity-Impulsivity
3
9
8
2.5
H-C pred
H-C obs
M-H pred
M-H obs
L-M pred
L-M obs
C-L pred
C-L obs
7
PA-score
2
1.5
1
6
HI-score
H-R pred
H-R obs
M-R pred
M-R obs
C-L pred
C-L obs
5
4
3
2
0.5
1
0
0
17
30
42
17
Age in Months
30
42
Age in Months
Fig. 1 Observed and predicted means for developmental trajectories of
physical aggression (PA) and Hyperactivity-impulsivity (HI) between
ages 17 and 42 months. ∗ Physical aggression: H-R = high-rising;
M-R = moderate-rising; C-L = consistently low; Hyperactivity-
Impulsivity: H-C = high-chronic; M-H = moderate-high; L-M =
low-moderate; C-L = consistently low.
Data courtesy of the Institut de la Statistique du Québec.
can also be seen in the contrasts between high and low HI
2
[OR = 1.38 (95% CI: 0.99 to 1.91), χ(1)
= 3.8, p = .052], between high and low-moderate HI [OR = 1.27 (95% CI: 0.98
2
= 3.3, p = .070] and high and moderate-high
to 1.63),χ(1)
2
HI [OR = 1.13 (95% CI: 0.88 to 1.46), χ(1)
= 1.0, p = .327].
The remaining significant predictors of HI between ages 17
2
= 31.1, p < .001], hostile
and 42 months were gender [χ(3)
2
= 42.6, p < .001],
reactive parenting (by the mother) [χ(3)
2
maternal depression [χ(3) = 12.4, p = .006], and age of the
2
mother when she had her first child [χ(3)
= 11.0, p = .012].
Spearman r = .245, p < .001). The conditional probabilities
for PA and HI in Table 3 show that, with higher PA or HI,
there is also a higher probability of HI and PA, respectively.
The conditional probabilities further reveal an asymmetry
in the association in that most high HI children were
likely to be high PA, but that most high PA children are
not likely to be high HI. Table 3 also shows the joint
probabilities of displaying particular levels of PA and HI
simultaneously. There are 12 cells (3 PA × 4 HI). In order
to test the contrasts relevant to our research question, i.e.
that maternal prenatal smoking might specifically predict
co-occurring PA and HI as opposed to PA only or HI
only, these 12 groups were collapsed into 4 groups representing the combined group (PA3HI4), the high PA only
group (PA3HI1 + PA3HI2 + PA3HI3), the high HI only
group (PA1HI4 + PA2HI4), and the remainder of the sample
(PA1HI1 + PA1HI2 + PA1HI3 + PA2HI1 + PA2HI2 +
Combining physical aggression
and hyperactivity-impulsivity
Although distinct, the trajectories of PA and HI were
2
moderately but significantly related (χ(6)
= 114.5, p < .001;
Table 2 Maternal prenatal smoking and physical aggression (PA), hyperactivity-impulsivity (HI) and joint PA + HI trajectories between ages
17 and 42 months
Physical aggression
Physical aggression adjusted for control variables
Hyperactivity
Hyperactivity adjusted for control variables
Physical aggression and hyperactivity
Physical aggression and hyperactivity adjusted for control variables
MLE 1 (SE)
MLE 2 (SE)
MLE 3 (SE)
χ2
P
− .40 (.09)
− .29 (.10)
− .56 (.15)
− .32 (.17)
− .65 (.14)
− .46 (.16)
− .24 (.07)
− .15 (.08)
− .41 (.11)
− .24 (.13)
− .57 (.22)
− .55 (.25)
NA
NA
− .22 (.11)
− .13 (.13)
− .41 (.14)
− .33 (.17)
23.6
8.4
22.8
5.8
31.2
10.5
< .001
.015
< .001
.121
< .001
.015
Note. MLE = Maximum Likelihood Estimate, Reference categories for PA, HI and PA + HI are high PA, high HI and high PA + high HI,
respectively. NA = Not Applicable. (MLE) 1 = consistently-low PA; consistently-low HI; and low PA + low HI; (MLE) 2 = moderate-rising
PA; low-moderate HI; and low PA + high HI; (MLE) 3 = moderate-high HI; and high PA + low HI. DF = 2 for PA, DF = 3 for HI and for
PA + HI.
Data courtesy of the Institut de la Statistique du Québec.
Springer
210
J Abnorm Child Psychol (2007) 35:203–215
Table 3 Co-occurrence of
physical aggression (PA) and
hyperactivity-impulsivity (HI)
Probability of PA conditional on HI
Low HI
Low-Moderate (L-M) HI
Moderate-High (M-H) HI
Chronic-High (C-H) HI
Low PA
.40
.28
.18
.12
Probability of HI conditional on PA
Low HI
Low PA
.19
Moderate PA
.12
High PA
.05
Sum
Moderate PA
.49
.54
.49
.39
High PA
.11
.18
.33
.49
1.0
1.0
1.0
1.0
L-M HI
.51
.48
.34
M-H HI
.27
.36
.50
C-H HI
.03
1.0
.04
1.0
.11
1.0
L-M HI
.13
.24
.08
.45
M-H HI
.07
.18
.12
.37
C-H HI Sum/PA
.01
.25
.02
.51
.03
.24
.06
1.0
Joint probability of PA and HI
Low PA
Moderate PA
High PA
Sum/HI
Data courtesy of the Institut de
la Statistique du Québec.
PA2HI3) (Table 4). For the next analysis, these four groups
will constitute our dependent variable.
In order to be able to conclude that prenatal smoking
specifically predicts co-occurring PA and HI the a priori
contrasts of all groups to the combined group should be significant. A multinomial regression with the control variables
that had featured in the previous separate analyses of PA and
HI showed that this was indeed the case. The overall effect
2
= 10.5, p = .015], and
of maternal prenatal smoking [χ(3)
the predictions by prenatal smoking of the contrasts of the
combined group with the PA only group [OR = 1.39, 95%
2
= 4.0, p = .047], with HI only group
CI to 1.01 to 1.92, χ(1)
2
= 4.8, p = .029], and
[OR = 1.72, 95% CI 1.06 to 2.86, χ(1)
with the remainder of the sample [OR = 1.59, 95% CI 1.16
2
= 8.4, p = .004], were all significant (see also
to 2.17, χ(1)
Table 4 Co-occurrence of physical aggression (PA) (2 levels) and
hyperactivity-impulsivity (HI) (2 levels)
Probability of PA conditional on HI
Low PA
Low HI
.77
High HI
.51
High PA
.23
.49
Sum
1.0
1.0
Probability of HI conditional on PA
Low HI
Low PA
.96
High PA
.89
High HI
.04
.11
1.0
1.0
Joint probability of PA and HI
Low HI
Low PA
.73
High PA
.22
Sum/HI
.95
High HI
.03
.03
.05
Sum/PA
.76
.24
1.0
Data courtesy of the Institut de la Statistique du Québec.
Springer
Low HI
.05
.06
.01
.12
Table 2). Although additional contrasts were not significant,
the contrast between the PA-only group and ‘the remainder
2
= 3.0,
of the sample’- group approached significance [χ(1)
p = .08]. Other significant and independent predictors of the
2
= 18.0, p < .001], prescombined group were gender [χ(3)
2
ence of siblings [χ(3) = 59.3, p < .001], and hostile reactive
2
= 22.5, p < .001].
parenting (by the mother) [χ(3)
Discussion
The results of this study of early childhood show that maternal prenatal smoking was associated with PA but not with
HI in covariate regression analyses when PA and HI were
examined separately. When PA and HI were combined, a
contrast between the PA-only group and the remainder of
the sample, which was neither high on PA or HI, fell short of
significance. However, maternal prenatal smoking predicted
co-occurring elevated levels of PA and HI. Therefore the key
finding of this study is that maternal prenatal smoking predicted high PA, but largely when it is co-occurring with high
HI. Had we just examined PA and HI separately, as has often
been done in studies of specificity, we would have missed the
fact that HI is also sensitive to maternal prenatal smoking,
even after controlling for several confounding variables, but
only when it is combined with PA.
The first implication of these findings is that maternal prenatal smoking may be associated with the most severe forms
of PA and HI, i.e. their combination, in early childhood.
Second, the fact that maternal prenatal smoking predicts cooccurring PA and HI may be considered an important finding
in light of evidence indicating that multiple co-occurring behavior problems at an early age are associated with a higher
J Abnorm Child Psychol (2007) 35:203–215
risk of persistent antisocial problems (Brame et al., 2001;
Broidy et al., 2003; Nagin & Tremblay, 1999; Lacourse
et al., 2006; Lahey et al., 2000; Moffitt, 1993; Moffitt, Caspi,
Dickson, Silva, & Stanton, 1996), as well as with several
other functional impairments (Waschbusch, 2002; Séguin
et al., 2004). Finally, the risk factors identified for these
combined behavior problems, are largely modifiable.
Our study replicates the reports from Orlebeke et al.
(1997), Williams et al. (1998), Day et al. (2000), and
Tremblay et al. (2004), based largely on early childhood behavior problems. However, we extend these findings because
none of those early childhood studies had tested for the prediction of specific behavior problems or for the specificity of
their combination. Tremblay et al. (2004) covered the same
developmental period and used the exact same PA scale as
we did here on another sample. We both found that the association between maternal prenatal smoking and PA was not
explained by control variables. However, our results for HI
appear to contrast slightly with those of Romano et al. (2006)
who reported that the association between maternal prenatal smoking and hyperactivity was not explained by control
variables. There are a number of key differences between the
current study and Romano et al. (2006). Besides using a different sample, we included impulsivity along with hyperactivity items, and focused exclusively on behavior during early
childhood. Thus, in the current study the effects of maternal
prenatal smoking on HI were largely explained by control
variables. It is possible that control variables have a greater
effect on the impulsivity component of HI than on the hyperactivity component. We note that our results appear to be
consistent with those of Wakschlag, Leventhal et al. (2006),
who also failed to find a relation of maternal prenatal smoking but with ADHD, which includes impulsivity. Because of
our goal for a strict test for specificity of effects on PA, it
was more conservative to have a combination of impulsivity
and hyperactivity items in our scale. Alternately, by having
information extending beyond the early childhood period to
estimate trajectories Romano et al. (2006) may have more
accurately identified children for whom maternal prenatal
smoking matters beyond the effects of control variables. Despite this limitation to early childhood, and despite the fact
that we cannot claim to have accounted for all possible control variables (examples include exposure to environmental
smoking postnatally and forms of parental psychopathology
other than maternal depression and parental history of antisocial behavior such as parental ADHD), this study replicates
and extends all previous studies by providing an empirical
basis for how the association of prenatal smoking to both PA
and HI may manifest itself. It is now much more clear that
studies need to examine co-occurrence of behavior problems.
There is a leap in drawing parallels between early childhood symptoms to DSM-based disorder, i.e., from PA to CD
and from HI to ADHD. CD is characterized by aggression
211
to people and/or animals, deceitfulness or theft, vandalism
and serious rule violations whereas ADHD is characterized
by hyperactivity, behavior disinhibition (or impulsivity), and
inattention and distractibility (American Psychiatric Association, 1994). It is not yet clear to what extent behavior problems during the early childhood years map onto ADHD and
CD symptoms during later childhood and (antisocial) behavior problems during adolescence and adulthood, although we
have shown that childhood PA trajectories and hyperactivity
trajectories were respectively related to CD and ADHD measured in adolescence (Séguin et al., 2004). But manifestation
of PA and HI symptoms are often not sufficient to warrant
diagnoses. We also note that behavior problems during the
early childhood years tend to be more common and typically
decline over time (Côté et al., 2006; Romano et al., 2006;
Bongers, Koot, Van Der Ende, & Verhulst, 2003).
A number of pioneering studies showed that behavior
problems later in life (ranging from school-age to adulthood) could already be identified during early childhood
(e.g. Campbell et al., 1986; Keenan & Wakschlag, 2000),
but only recently a number of studies have started to show,
particularly with respect to HI, a significant consistency in
the likelihood to display (very) high levels from age 1 1/2
years onwards (e.g. Romano et al., 2006; Shaw et al., 2005).
With respect to PA, there is a larger group of very young
children showing rather high levels, but most of them will
use less PA from early school age onwards (e.g. Côté et al.,
2006; NICHD Early Child Care Research Network, 2004;
Shaw et al., 2005). Such general trends might also underlie differences in number of groups identified by the trajectory methodology in samples with different age ranges.
Whereas our three PA-groups were consistent with the three
groups identified by some authors (e.g. Côté et al., 2006)
covering early and middle childhood, other authors identified
more than three groups for this period (NICHD Early Child
Care Research Network, 2004; Shaw et al., 2005). However,
most children will not yet have finished learning alternative
strategies (i.e. have undergone ‘socialization of aggression,’
Tremblay, 2003) between 17 and 42 months, so the expected
‘desisting’ patterns of PA will not yet be evident. One thing
the abovementioned studies have in common is that they
show a degree of consistency between early and middle childhood conduct problems, i.e. children with chronic PA during
middle childhood generally had high PA levels during early
childhood as well. This, in turn, emphasizes the importance
of searching for predictors of co-occurring early childhood
behavior problems: children most at risk of subsequent behavior problems might be those who display both high PA
and high HI at this stage.
The combination of conduct problems and hyperactivityimpulsivity-attention problems has been distinguished from
their pure forms at a number of levels (Waschbusch, 2002).
Although research has again mainly focused on older
Springer
212
children with diagnosed disorders rather than the combination of behaviors such as PA and HI (but see Séguin,
Arseneault, Boulerice, Harden, & Tremblay, 2002; Séguin
et al., 2004), evidence has been provided for a number
of etiological and developmental differences between the
comorbid and individual conditions. For example, greater
behavioral and autonomic nervous system reactivity in response to provocation has been shown in the comorbid
compared to the separate conditions (Waschbusch, 2002).
Children with CD + ADHD were also shown to have lower
baseline sympathetic arousal than children with the separate disorders (specifically those with ADHD only; Herpertz
et al., 2001). There is also evidence for differences in patterns of brain activity between CD + ADHD and the separate conditions (Banaschewski et al., 2003) and for specific heritable risk of CD + ADHD (Dick, Viken, Kaprio,
Pulkkinen, & Rose, 2005; Thapar, Harrington, & McGuffin,
2001). Several studies have shown that specific family psychosocial characteristics (e.g. parent-child conflict; parental
psychopathology) specifically predict CD + ADHD or predict CD + ADHD more strongly than the separate conditions (e.g. Burt, Krueger, McGue, & Iacono, 2003; Pfiffner,
McBurnett, Rathouz, & Judice, 2005). Thus, although extrapolation to CD and ADHD must be done with caution,
the results of the present study support an etiological basis
for the combined behavior problems in an early childhood
sample.
Finally, in addition to prenatal maternal smoking, we
found that maternal hostile- reactive parenting was also associated with co-occurring PA and HI beyond its effects on
the separate behaviors. Hostile-reactive parenting and similar ‘negative’ parenting behaviors have been associated with
children’s PA and HI levels in earlier studies (e.g. Côté et al.,
2006; Romano et al., 2006; Shaw et al., 2005; Tremblay
et al., 2004), Negative parenting has also been related to the
failure of training programs aimed at improving child conduct problems (Webster-Stratton, Reid, & Hammond, 2001).
This association could be seen as resulting from the impact
of maternal behavior on their child’s behavior. However,
they may also reflect, at least in part, parent’s reactions to
their child’s behavior. For instance, when faced with conduct problems, mothers of preschoolers at risk for ADHD
and Oppositional Defiant Disorder tend to resort to more
negative parenting strategies (Cunningham & Boyle, 2002).
Furthermore, mothers hostile-reactive parenting toward their
5 month-old infants has been found to be partly driven by
their infant’s difficult temperament (Boivin et al., 2005).
Our finding that maternal hostile-reactive parenting is associated with an increased risk of co-occurring PA and HI
may thus reflect the increased challenge of parenting when
a child displays multiple behavior problems (cf. Seipp &
Johnston, 2005). This pattern could lead to the establishment of a family coercive process and the further learning
Springer
J Abnorm Child Psychol (2007) 35:203–215
of anti-social behaviors by the child. However, the state of
evidence precludes any definite conclusions at this point, and
there is a clear need to better document the early dynamics
of negative parenting and externalizing problems in early
childhood.
To the extent that they may be involved in causation, the
good news is that prenatal maternal smoking and hostilereactive parenting could be significantly attenuated in prevention and intervention programs. The fact that the effects of smoking during pregnancy on both PA and PA + HI
were robust, added to the evidence that PA + HI increases
the risk for continued serious behavior problems, emphasizes the importance of smoking cessation during pregnancy
(for a review on effectiveness of cessation programs, see
Lumley, Oliver, Chamberlain, & Oakley, 2004). Considering the high prevalence of prenatal smoking (around 25%
in Western countries), it will be important to further refine
the identification of families most at risk of having children
with a prepotency to develop co-occurring PA and HI. Our
results further confirm that hostile-reactive parenting should
be targeted in preventive intervention aimed at children with
early multiple behavior problems. However, because parenting interventions often are the least effective in multiple-risk
families (for a review, see Hutchings & Lane, 2005), including those characterized by prenatal smoking (Vuijk, van Lier,
Huizink, Verhulst, & Crijnen, 2006), cessation programs targeting the most vulnerable families should be emphasized,
intensified, and given appropriate means to succeed.
Acknowledgements We are grateful to the children and their families
for their participation in the study, to l’Institut de la Statistique du
Québec, direction Santé Québec, and its partners for data collection
and preparation, to Charles Édouard Giguère and Qian Xu for data
management, and to Danielle Forest for statistical analyses.
References
Achenbach, T. M., Edelbrock, C. S., & Howell, C. T. (1987). Empirically based assessment of the behavioral/emotional problems of 2and 3- year-old children. Journal of Abnormal Child Psychology,
15, 629–650.
American Psychiatric Association. (1994). Diagnostic and statistical
manual of mental disorders (4th ed., pp. 78–85). Washington, DC:
American Psychiatric Association.
Banaschewski, T., Brandeis, D., Heinrich, H., Albrecht, B., Brunner,
E., & Rothenberger, A. (2003). Association of ADHD and conduct
disorder – brain electrical evidence for the existence of a distinct
subtype. Journal of Child Psychology and Psychiatry, 44, 356–
376.
Beck, L. F., Morrow, B., Lipscomb, L. E., Johnson, C. H., Gaffield, M.
E., Rogers, M. et al. (2002). Prevalence of selected maternal behaviors and experiences: Pregnancy Risk Assessment Monitoring
System (PRAMS) 1999. CDC Surveillance Summaries, 51, 1–27.
Biederman, J., Milberger, S., & Faraone, S. V. (1995). Familyenvironment risk factors for attention-deficit hyperactivity disorder: A test of Rutter’s indicators of adversity. Archives of General
Psychiatry, 52, 464–470.
J Abnorm Child Psychol (2007) 35:203–215
Boivin, M., Pérusse, D., Dionne, G., Saysset, V., Zoccolillo, M.,
Tarabulsy, G. et al. (2005). Parent’s perceptions and self-assessed
behaviors toward their 5-month-old infants in a large twin and
singleton sample. Journal of Child Psychology and Psychiatry,
46, 612–630.
Bongers, I. L., Koot, H. M., van der Ende, J., & Verhulst, F. C. (2003).
The normative development of child and adolescent problem behavior. Journal of Abnormal Psychology, 112, 179–192.
Brame, B., Nagin, D. S., & Tremblay, R. E. (2001). Developmental trajectories of physical aggression from school entry to late adolescence. Journal of Child Psychology and Psychiatry, 58, 389–394.
Braun, J., Kahn, R. S., Froehlich, T., Auinger, P., & Lanphaer, B. P.
(2006). Exposures to environmental toxicants and attention deficit
hyperactivity disorder in US children. Environmental Health Perspectives, ehp. 9478 (available at http://dx.doi.org/).
Brennan, P., Grekin, E., & Mednick, S. (1999). Maternal smoking
during pregnancy and adult male criminal outcomes. Archives of
General Psychiatry, 56, 215–219.
Broidy, L. M., Nagin, D. S., Tremblay, R. E., Bates, J. E., Brame, B.,
Dodge, K. A. et al. (2003). Developmental trajectories of childhood disruptive behaviors and adolescent delinquency: A sixsite, cross-national study. Developmental Psychology, 39, 222–
245.
Burt, S. A., Krueger, R. F., McGue, M., & Iacono, W. (2003). Parentchild conflict and the comorbidity among childhood externalizing
disorders. Archives of General Psychiatry, 60, 505–513.
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, 155–160.
Campbell, S. B., Breaux, A. M., Ewing, L. J., & Szumowski, E. K.
(1986). Correlates and predictors of hyperactivity and aggression: A longitudinal study of parent-referred problem preschoolers. Journal of Abnormal Child Psychology, 14, 217–234.
Campbell, S. B., Shaw, D. S., & Gilliom, M. (2000). Early externalizing behavior problems: Toddlers and preschoolers at risk for
later maladjustment. Development and Psychopathology, 12, 467–
488.
Côté, S., Vaillancourt, T., LeBlanc, J. C., Nagin, D. S., & Tremblay, R. E.
(2006). The development of physical aggression from toddlerhood
to pre-adolescence: A nation-wide longitudinal study of Canadian
children. Journal of Abnormal Child Psychology, 34, 68–82.
Cunningham, C. E., & Boyle, M. H. (2002). Preschoolers at risk for
attention-deficit hyperactivity disorder and oppositional defiant
disorder: Family, parenting and behavioral correlates. Journal of
Abnormal Child Psychology, 30, 555–569.
Day, N. L., Richardson, G. A., Goldschmidt, L., & Cornelius, M. D.
(2000). Effects of prenatal tobacco exposure on preschoolers’ behavior. Journal of Developmental & Behavioral Pediatrics, 21,
180–188.
Dick, D. M., Viken, R. J., Kaprio, J., Pulkkinen, L., & Rose, R. J.
(2005). Understanding the covariation among childhood externalizing symptoms: Genetic and environmental influences on conduct
disorder, attention deficit hyperactivity disorder, and oppositional
defiant disorder symptoms. Journal of Abnormal Child Psychology, 33, 219–229.
Egger, H. L., & Angold, A. (2006). Common emotional and behavioral disorders in preschool children: Presentation, nosology, and
epidemiology. Journal of Child Psychology and Psychiatry, 47,
313–337.
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, 721–727.
Herpertz, S. C., Wenning, B., Mueller, B., Qunaibi, M., Sass, H., &
Herpertz-Dahlmann, B. (2001). Psychophysiological responses in
213
ADHD boys with and without conduct disorder: Implications for
adult antisocial behavior. Journal of the American Academy of
Child and Adolescent Psychiatry, 40, 1222–1230.
Huijbregts, S. C. J., Séguin, J. R., Zelazo, P. D., Parent, S., Japel,
C., & Tremblay, R. E. (2006). Interrelations between maternal
smoking during pregnancy, birth weight and sociodemographic
factors in the prediction of early cognitive abilities. Infant and
Child Development, 15, 593–607.
Human Resources Development Canada and Statistics Canada. (1996).
Growing up in Canada: National Longitudinal Survey of Children and Youth. Ottawa: Statistics Canada. http://www.statcan.ca/
english/Dli/Data/Ftp/nlscy.htm.
Hutchings, J., & Lane, E. (2005). Parenting and the development and
prevention of child mental health problems. Current Opinion in
Psychiatry, 18, 386–391.
Jacobsen, S. W., Chiodo, L. M., Sokol, R. J., & Jaconson, J. L. (2002).
Validity of maternal report of prenatal alcohol, cocaine, and smoking in relation to neurobehavioral outcome. Pediatrics, 109, 815–
825.
Jensen, P. S., Martin, D., & Cantwell, D. P. (1997). Comorbidity in
ADHD: Implications for research, practice, and DSM-V. Journal
of the American Academy of Child and Adolescent Psychiatry, 40,
147–158.
Jetté, M., & Des Groseilliers, L. (2000). Survey Description and
Methodology. In Longitudinal Study of Child Development in
Québec (ELDEQ 1998–2002) (Vol. 1, No. 1). Québec: Institut de la Statistique du Québec. http://www.jesuisjeserai.stat.
gouv.qc.ca/doc tech an.htm.
Keenan, K., & Wakschlag, L. S. (2000). More than the terrible twos:
The nature and severity of behavior problems in clinic-referred
preschool children. Journal of Abnormal Child Psychology, 28,
33–46.
Kotimaa, A. J., Moilanen, I., Taanila, A., Ebeling, H., Smalley, S. L.,
McGough, J. J. et al. (2003). Maternal smoking and hyperactivity
in 8-year-old children. Journal of the American Academy of Child
and Adolescent Psychiatry, 42, 826–833.
Kramer, M. S., Platt, R. W., Wen, S. W., Joseph, K. S., Allen, A.,
Abrahamowicz, M., Blondel, B., & Breart, G.; Fetal/Infant Health
Study Group of the Canadian Perinatal Surveillance System.
(2001). A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics, 108,
e35.
Lacourse, E., Nagin, D. S., Vitaro, F., Côté, S., Arseneault, L., &
Tremblay, R. E. (2006). Prediction of early-onset deviant peer
group affiliation: A 12-year longitudinal study. Archives of General Psychiatry, 63, 562–568.
Lahey, B. B., McBurnett, K., & Loeber, R. (2000). Are attentiondeficit/hyperactivity disorder and oppositional defiant disorder developmental precursors to conduct disorder? In A. J. Sameroff,
M. Lewis, & S. M. Miller (Eds.), Handbook of developmental
psychopathology (2nd ed., pp. 431–446). New York: Kluwer Academic.
Law, K. L., Stroud, L. R., LaGasse, L. L., Niaura, R., Liu, J., & Lester,
B. M. (2003). Smoking during pregnancy and newborn neurobehaviour. Pediatrics, 111, 1318–1323.
Linnet, K. M., Dalsgaard, S., Obel, C., Wisborg, K., Hendriksen,
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, 1028–1040.
Lumley, J., Oliver, S. S., Chamberlain, C., & Oakley, L. (2004). Interventions for promoting smoking cessation during pregnancy.
Cochrane Database Systematic Reviews, 4, CD001055.
Maughan, B., Taylor, A., Caspi, A., & Moffitt, T. E. (2004). Prenatal
smoking and early childhood conduct problems: Testing genetic
Springer
214
and environmental explanations of the association. Archives of
General Psychiatry, 61, 836–843.
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 and Adolescent Psychiatry, 41, 378–385.
Milberger, S., Biederman, J., Faraone, S. V., Chen, L., & Jones, J.
(1996). Is maternal smoking during pregnancy a risk factor for attention deficit hyperactivity disorder in children? American Journal of Psychiatry, 153, 1138–1142.
Moffitt, T. E. (1993). Adolescence-limited and life-course persistent
antisocial behavior: A developmental taxonomy. Psychological
Review, 100, 674–701.
Moffitt, T. E., Caspi, A., Dickson, N., Silva, P., & Stanton, W. (1996).
Childhood-onset versus adolescent-onset antisocial conduct problems in males: Natural history from ages 3 to 18 years. Development and Psychopathology, 8, 399–424.
Nagin, D. S. (1999). Analyzing developmental trajectories: A semiparametric, group-based approach. Psychological Methods, 4,
139–177.
Nagin, D. S. (2005). Group-based modeling of development.
Cambridge, MA: Harvard University Press.
Nagin, D. S., & Tremblay, R. E. (1999). Trajectories of boys’ physical
aggression, opposition, and hyperactivity on the path to physically
violent and nonviolent juvenile delinquency. Child Development,
70, 1181–1196.
Nagin, D. S., & Tremblay, R. E. (2001). Analyzing developmental trajectories of distinct but related behaviors: A group-based method.
Psychological Methods, 6, 18–34.
NICHD Early Child Care Research Network. (2004). Trajectories of
physical aggression from toddlerhood to middle childhood. Monographs of the Society for Research in Child Development. Serial
No. 278, Vol. 69, 4.
Offord, D. R., Boyle, M. H., & Racine, Y. (1989). Ontario child health
study: Correlates of disorder. Journal of the American Academy
of Child and Adolescent Psychiatry, 28, 856–860.
Orlebeke, J. F., Knol, D. L., & Verhulst, F. C. (1997). Increase in
child behavior problems resulting from maternal smoking during
pregnancy. Archives of Environmental Health, 52, 317–321.
Pfiffner, L. J., McBurnett, K., Rathouz, P. J., & Judice, S. (2005). Family
correlates of oppositional and conduct disorders in children with
attention deficit/hyperactivity disorder. Journal of Abnormal Child
Psychology, 33, 551–563.
Pickett, K. E., Rathouz, P. J., Kasza, K., Wakschlag, L. S., & Wright,
R. (2005). Self-reported smoking, cotinine levels, and patterns of
smoking in pregnancy. Paediatric and Perinatal Epidemiology, 19,
368–376.
Radloff, L. (1977). The CES-D scale: A self-report depression scale for
research in the general population. Applied Psychological Measurement, 1, 385–401.
Räsänen, P., Hakko, H., Isohanni, M., Hodgins, S., Järvelin, M. 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,
857–862.
Robins, L. N., Helzer, J. E., Croughan, J., & Ratcliff, K. S. (1981).
National Institute of Mental Health Diagnostic Interview Schedule. Its history, characteristics, and validity. Archives of General
Psychiatry, 38, 381–389.
Romano, E., Tremblay, R. E., Farhat, A., & Côté, S. (2006). Development and prediction of hyperactive symptoms from 2 to 7 years in
a population-based sample. Pediatrics, 117, 2101–2110.
SAS Institute Inc. (2001). The SAS System for Windows, v.8.2. Cary,
NC: Author.
Springer
J Abnorm Child Psychol (2007) 35:203–215
Seipp, C. M., & Johnston, C. (2005). Mother-son interactions in families of boys with Attention-Deficit/Hyperactivity Disorder with
and without oppositional behavior. Journal of Abnormal Child
Psychology, 33, 87–98.
Séguin, J. R., Arseneault, L., Boulerice, B., Harden, P. W., &
Tremblay, R. E. (2002). Response perseveration in adolescent
boys with stable and unstable histories of physical aggression:
The role of underlying processes. Journal of Child Psychology
and Psychiatry, 43, 481–494.
Séguin, J. R., Nagin, D., Assaad, J.-M., & Tremblay, R. E. (2004).
Cognitive-neuropsychological function in chronic physical
aggression and hyperactivity. Journal of Abnormal Psychology,
113, 603–613.
Shaw, D. S., Lacourse, E., & Nagin, D. S. (2005). Developmental
trajectories of conduct problems and hyperactivity from ages 2
to 10. Journal of Child Psychology and Psychiatry, 46, 931–
942.
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, 130–135.
Statistics Canada. (1995). Overview of Survey Instruments for 1994–95
Data Collection, Cycle 1. Ottawa, ON: Statistics Canada.
Statistics Canada. (2006). Income trends in Canada: 1980–2004.
Ottawa, ON: Statistics Canada.
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, 1985–1989.
Thapar, A., Harrington, R., & McGuffin, P. (2001). Examining the
comorbidity of ADHD-related behaviours and conduct problems
using a twin study design. British Journal of Psychiatry, 179,
224–229.
Tremblay, R. E. (2003). Why socialization fails?: The case of chronic
physical aggression. In B. B. Lahey, T. E. Moffitt, & A. Caspi
(Eds.), Causes of conduct disorder and juvenile delinquency
(pp. 182–224). New York: Guilford Publications.
Tremblay, R. E., Desmarais-Gervais, L., Gagnon, C., & Charlebois,
P. (1987). The Preschool Behaviour Questionnaire: Stability of
its factor structure between cultures, sexes, ages and socioeconomic classes. International Journal of Behavioral Development,
10, 467–484.
Tremblay, R., Nagin, D., Séguin, J., Zoccolillo, M., Zelazo, P. D.,
Boivin, M. et al. (2004). Physical aggression during early childhood: Trajectories and predictors. Pediatrics, 114, e43–e50.
Vuijk, P., van Lier, P. A., Huizink, A. C., Verhulst, F. C., & Crijnen,
A. A. (2006). Prenatal smoking predicts non-responsiveness to
an intervention targeting attention-deficit/hyperactivity symptoms
in elementary schoolchildren. Journal of Child Psychology and
Psychiatry, 47, 891–901.
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, 351–369.
Wakschlag, L. S., Leventhal, B. L., Pine, D. S., Pickett, K. E., & Carter,
A. S. (2006). Elucidating early mechanisms of developmental psychopathology: The case of prenatal smoking and disruptive behavior. Child Development, 77, 893–906.
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, 966–974.
Wakschlag, L. S., Pickett, K. E., Kasza, K. E., & Loeber, R. (2006). 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, 461–467.
J Abnorm Child Psychol (2007) 35:203–215
Waschbusch, D. A. (2002). A meta-analytic examination of comorbid hyperactive/impulsive/inattention problems and conduct problems. Psychological Bulletin, 128, 118–150.
Webster-Stratton, C., Reid, J., & Hammond, M. (2001). Social skills
and problem-solving training of children with early-onset conduct problems: Who benefits? Journal of Child Psychology and
Psychiatry, 42, 943–952.
Williams, G. M., O’Callaghan, M., Najman, J. M., Bor, W., Andersen,
M., & Richards, D. U. C. (1998). Maternal cigarette smoking and
215
child psychiatric morbidity: A longitudinal study. Pediatrics, 102,
e11.
Woodward, L. J., Fergusson, D. M., & Horwood, L. J. (2002). Romantic relationships of young people with childhood and adolescent
onset antisocial behavior problems. Journal of Abnormal Child
Psychology, 30, 231–243.
Zoccolillo, M. (2000). Parents’ health and social adjustment: Part II,
social adjustment. In Longitudinal Study of Child Development in
Québec (ELDEQ 1998–2002) (pp. 37–45). Québec (Qc), Canada:
Institut de la Statistique du Québec.
Springer