Is Smoking During Pregnancy a Risk Factor for Psychopathology
in Young Children? A Methodological Caveat and Report on
John V. Lavigne,1PHD, Joyce Hopkins,2PHD, Karen R. Gouze,1PHD, Fred B. Bryant,3PHD,
Susan A. LeBailly,1PHD, Helen J. Binns,4PHD, and Paul M. Lavigne,5MD
1Department of Child and Adolescent Psychiatry, Children’s Memorial Hospital, Feinberg School of Medicine,
Northwestern University, Mary Ann and J. Milburn Smith, Child Health Research Program, Children’s
Memorial Research Center,2Institute of Psychology, Illinois Institute of Technology,3Department of
Psychology, Loyola University Chicago,4Department of Pediatrics, Children’s Memorial Hospital, Feinberg
School of Medicine, Northwestern University, Mary Ann and J. Milburn Smith, Child Health Research Program,
Children’s Memorial Research Center, and5Tufts New England Medical Center
All correspondence concerning this article should be addressed to John V. Lavigne, Department of Child and
Adolescent Psychiatry (#10), Children’s Memorial Hospital, 2300 Children’s Plaza, Chicago, IL, 60614,
USA. E-mail: email@example.com
Received September 14, 2009; revisions received and accepted April 22, 2010
relationships, most studies (1) failed to control for a range of correlates of maternal smoking that could affect
children’s behavior; (2) have been conducted with school-age rather than younger children, so it is not clear
when such problems emerge; and (3) have not examined the effects on internalizing problems.
This study examined the effects of prenatal smoke exposure on behaviors associated with externalizing and
internalizing behavior problems and negative temperament in a diverse community sample of 679 4-year-olds.
ResultsAfter controlling for correlates that include socioeconomic status, life stress, family conflict, mater-
nal depression, maternal scaffolding skills, mother–child attachment, child negative affect and effortful
control, smoking during pregnancy was no longer associated with child behavior or emotional problems.
ConclusionsFuture studies need to control for a wide range of covariates of maternal smoking.
While studies of the effects of prenatal smoking on child psychopathology have found positive
Key wordsadjustment; mental health; parenting; risk; smoking.
Cigarette smoking has harmful effects on the fetus, leading
to premature differentiation of developing neural tissue,
altered noradrenergic and dopaminergic central nervous
system pathways (van IJzendoorn, Vereijken, Bakermans-
Kranenburg, & Riksen-Walraven, 2004), and intrauterine
growth retardation (Lassen & Oei, 1998). Many studies
suggest that smoking during pregnancy is a risk factor
affecting the development of externalizing behavior prob-
lems via the neurological or physiological changes that
smoking produces in utero. The resulting externalizing
problems may include oppositional or antisocial behavior
(Wakschlag, Pickett, Cook, Benowitz, & Leventhal, 2002),
Attention Deficit Hyperactivity Disorder (Linnett et al.,
2003), or both.
Demonstrating a direct association between smoking
during pregnancy and behavior problems is complicated by
the presence of confounding risk factors that provide
alternative explanations for any smoking/behavior problem
relationship (Wakschlag et al., 2002). Because mothers
who smoke during pregnancy differ on important variables
from those who do not (Button, Maughan, & McGuffin,
2007; Wakschlag et al., 2002) and random assignment to
prenatal smoking conditions is not possible, statistical
Journal of Pediatric Psychology 36(1) pp. 10–24, 2011
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Journal of Pediatric Psychology vol. 36 no. 1 ? The Author 2010. Published by Oxford University Press on behalf of the Society of Pediatric Psychology.
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procedures must control for demographic, physical and
psychosocial factors during pregnancy or early childhood
that co-vary with smoking during pregnancy and that could
be associated with child behavior problems. Nevertheless,
residual effects of covariates may still remain after statistical
controls are applied (Wakschlag et al., 2002). Eliminating
any residual effects after applying statistical controls and
controlling for every conceivable correlate of maternal
smoking may be impossible, but confidence in the findings
of such studies will increase if the range of covariates ex-
amined is reasonably comprehensive.
Viewed from another perspective, failure to include
critical psychosocial variables when studying the effects
of smoking during pregnancy may result in an ‘‘omitted
variables’’ problem, in which the effect of a particular risk
variable is over-estimated when constructs playing a role in
the causal structure of the outcome variable are omitted
from analysis. The ‘‘omitted variables’’ problem is consid-
erable in studies of the etiology of psychopathology
(Tomarken & Waller, 2003), biasing estimates of causal
parameters in the model or leading to inaccurate standard
errors affecting significance levels of relationships. It is
even possible for an omitted variable to completely account
for the effects of a variable included in the model
(Tomarken & Waller, 2003). While an emphasis on ‘‘con-
trolling for’’ certain variables might lead researchers to be
satisfied with including variables known to correlate with
smoking during pregnancy, attending to omitted variables
emphasizes inclusion of a wider range of variables associ-
ated with the outcome measure in order to obtain a more
accurate estimate of the magnitude of the effects of smok-
ing during pregnancy on child psychopathology.
Psychosocial Correlates of Smoking During
Wakschlag et al. (2002) noted that pregnant women who
smoke differ from nonsmokers in several ways, including
contextual factors, presence of psychiatric disorder, and
parenting behavior. Variables studied along with smoking
during pregnancy vary widely across studies in the litera-
ture; these may include contextual factors (i.e., demo-
graphics, such as maternal education, socioeconomic
status) parental psychological problems (e.g., conduct
disorder, depression), parenting variables (e.g., warmth,
hostility), family climate factors (e.g., stressors, conflict in
the home) and child health factors (e.g., birth weight, other
illnesses). Few studies, however, include covariates from
each of these categories. Controlling for demographic fac-
tors usually occurs (Ashford, van Lier, Timmermans,
Cuijpers, & Koot, 2008; Batstra, Hadders-Algra, &
Neeleman, 2003; D’Onofrio et al., 2008) but not always
(Brennan, Grekin, & Mednick, 1999; Silberg et al., 2003),
while pre- and perinatal factors, including birth weight, are
often (Cornelius, Ryan, Day, Goldschmidt, & Willford,
2001; Weitzman, Gortmaker, & Sobol, 1992), but not
always (Brook, Brook, & Whiteman, 2000; Linnett et al.,
2003), included as covariates. Similarly, attention to psy-
chosocial factors is inconsistent. Controlling for parental
psychopathology is relatively common, but few studies
have assessed family conflict and life stress, or attempted
to assess parenting attitudes, behavior, and the family en-
vironment. Although several studies have found a relation-
ship between smoking during pregnancy and behavior
problems after controlling for maternal hostility and sup-
portive home environment, other important aspects of par-
enting and the parent–child relationship (e.g., attachment
security) have been overlooked. D’Onofrio et al. (2008)
argue that important, as yet unidentified, environmental
factors may account for the relationship between smoking
during pregnancy and externalizing behaviors, including
Identifying and examining the effects of such variables is
important if an unbiased estimate of the effects of smoking
during pregnancy is to be obtained.
Recently, the possibility of genetic factors confounding the
study of the effects of smoking during pregnancy on child
behavior outcomes has been raised (Knopik, 2009).
Genetic confounding can occur, for example, if mothers
with ADHD who are more likely to smoke also transmit
genes that predispose the child to developing ADHD. To
address genetic confounds, genetically-sensitive designs are
needed to estimate the relative contributions of genetic
factors and smoking during pregnancy. Such studies are
still uncommon. D’Onofrio et al. (2008) used a genetically
informed design to study the effects of smoking during preg-
nancy on externalizing disorders This study included
mothers and their children, ages 4–10 years, from the
National Longitudinal Survey of Youth. The study is
‘‘genetically informed’’ because data on various kinship
pairs, including twins, full siblings, half-siblings, and cous-
ins, among others, were collected and used to estimate the
genetic effects contributing to the relationship between
smoking during pregnancy and child problems. The
authors concluded that: (1) smoking during pregnancy
was not associated with conduct or oppositional behavior
problems; (2) there was a small relationship between
smoking during pregnancy and attention deficit symptoms,
with the relationship reduced by methodological and sta-
tistical controls; and (3) the confounds were less likely to
be genetic than environmental. However, the maternal
Prenatal Smoking Effects
‘‘environmental’’ characteristics examined only included
intellectual ability, education, income, delinquency, and
age at delivery, which have not been shown to be signifi-
cant psychosocial confounds in the extant literature on the
relationship between prenatal smoking and behavior prob-
lems. Knopik et al. (2006) used a children-of-twins design
to study genetic factors associated with ADHD and prena-
tal alcohol use and smoking on ADHD. In such a design,
the children vary in prenatal exposure to alcohol and smok-
ing depending on maternal use, and also on genetic risk.
The Knopik et al. study was primarily concerned with al-
cohol use during pregnancy, but smoking during pregnan-
cy was highly correlated with prenatal alcohol use. The
results suggest that genetic transmission plays an impor-
tant role in the association between maternal alcohol use
and offspring ADHD, with prenatal exposure to smoking
increasing the risk for ADHD. This children-of-twins design
and other promising genetic approaches may improve our
ability to obtain an unbiased estimate of the effect of smok-
ing during pregnancy on behavior problems in future stud-
ies (Knopik, 2009). Such designs include molecular genetic
approaches examining specific target genes; co-twin con-
trol designs that include twin pairs differing on the out-
come of interest, or some other environmental factor
(Knopik, 2009); or even prenatal cross-fostering designs
comparing mothers who are either biologically related or
unrelated to the child after undergoing in vitro fertilization
(Rice et al., 2009).
Studying Causal Mechanisms versus Reducing
In the field of developmental psychopathology, increasing
attention is being devoted to studying the causal mecha-
nisms underlying the relationships between purported risk
factors and outcomes. Many researchers are interested
in the process of mediation, in which an independent
variable is thought to affect a dependent variable through
some intervening variable known as a mediator (Iacobucci,
2008). With the exception of the Nigg and Breslau (2007)
study discussed later, researchers have not posited that
psychosocial variables serve as mediators of the relation-
ship between smoking during pregnancy and child behav-
ior problems. Causal modeling must begin with a strong,
coherent theoretical rationale, and thus far no researchers
have posited that smoking during pregnancy leads to a
parent having lower socioeconomic status (SES), more con-
flict at home, or poor parenting. Thus, such psychosocial
factors are viewed as smoking correlates, possibly related
to an underlying ‘‘third variable,’’ rather than as media-
tors of the prenatal smoking/child behavior relationship.
As a result, these studies have not typically examined
mediation; rather, statistical procedures attempt to control
for the effects of these correlates so that the specific effect
of smoking during pregnancy on behavior problems can be
Studies of Young Children
A second problem in the literature on smoking during
pregnancy is the absence of studies of young children
that address the omitted variables problem and, thereby,
rule out alternative explanations of the data by including a
wide range of risk variables in the causal model. Studies of
young children are important: identifying a relationship
between smoking during pregnancy and psychopathology
in preschoolers can point to the early onset of the relation-
ship between this prenatal risk factor and problem behav-
iors, while the absence of such a relationship may suggest a
mediating role for environmental risk factors or child char-
acteristics that become important as children enter school
or transition to adolescence. Studies of preschoolers can
help further our understanding of the developmental pro-
gression of the linkage between smoking during pregnancy
Among studies of smoking during pregnancy and
ADHD in young children, only one attempted to control
concurrently for demographic factors, family environment,
parental psychopathology, parenting, and prenatal factors.
Romano Tremblay, Farhat, & Cote (2008) found that
smoking during pregnancy was associated with ADHD
symptoms in 2- to 7-year-olds, while controlling for SES,
maternal depression, family dysfunction and maternally
reported parental warmth and hostility. That study, how-
ever, was limited by its use of a three-item ADHD scale
with unreported psychometric properties. Other investiga-
tors studying the relationship between smoking during
pregnancy and ADHD symptoms in predominantly pre-
school samples have failed to control for parenting and
family environmental effects (Streissguth, Martin, Barr, &
Sandman, 1984), parental psychopathology (Huijbregts
et al., 2007; McGee & Stanton, 1994) or family climate,
including stress or conflict (Huijbregts et al., 2007).
Among studies of the effects of smoking during preg-
nancy on externalizing disorders in young children, only
two studies controlled for at least one covariate in each area
of demographic, parental psychopathology, parenting, en-
vironment, family stress, and pre-or perinatal factors.
Results from one of these studies (Day, Richardson,
Goldschmidt, & Cornelius, 2000) suggest a relationship
between smoking during pregnancy and inattention,
and results from the other (Wakschlag, Leventhal, Pine,
Pickett, & Carter, 2006) suggest a relationship between
smoking during pregnancy and externalizing problems at
Lavigne et al.
24 months. The latter study was limited by a lack of racial/
ethnic diversity in the sample. Other studies finding a
relationship between smoking during pregnancy and exter-
nalizing problems in preschoolers failed to control for
family climate and parenting factors such as parental
warmth (Williams et al., 1998), perinatal factors or paren-
tal psychopathology (Huijbregts et al., 2007), or multiple
types of parenting or psychosocial factors (O’Callaghan,
Williams, Andersen, Bor, & Nahman, 1997; Orlebeke,
Knol, & Verhulst, 1997; Stene-Larsen & Borge, 2009;
Wakschlag & Keenan, 2001).
Furthermore, Nigg and Breslau (2007) posit an impor-
tantrolefor temperamentinyoungchildrenasamediator of
the relationship between smoking during pregnancy
and subsequent externalizing problems. Nigg and Breslau
proposed a model in which: (1) prenatal smoke exposure
‘‘amplifies’’ irritable temperament in children; and (2) this
‘‘lays the foundation for negative parent–child inter-
changes’’ that can generate oppositional defiant disorder
(ODD) symptoms. The model implies certain testable hy-
potheses, including: (a) preschool children exposed to
smoking in utero are more likely to have a difficult or ‘‘irri-
table’’ temperament; (b) the effects of smoking during preg-
nancy on the development of ODD symptoms are mediated
by negative temperament. A study by Brook et al. (2000), in
which smoking during pregnancy was associated with tem-
peramental negative affect (NA) in 2-year-olds, is relevant to
this model. Unfortunately, the measurement of NA was
based on a scale devised by the authors with unreported
psychometric characteristics, and assessed ‘‘impulsivity,
risk taking, and rebelliousness,’’ a construct more associat-
ed with externalizing disorders than temperamental NA.
Another limitation in the literature on smoking during
pregnancy is the lack of attention to internalizing disorders.
Since nicotine exposure affects the norepinephrine and se-
rotonin neurotransmitter systems associated with anxiety
and depression (Ashford et al., 2008), the impact of smok-
ing during pregnancy on internalizing problems merits fur-
ther study. We have identified only three studies of the
effects of smoking during pregnancy on internalizing prob-
lems (Ashford et al., 2008; Orlebeke et al., 1997; Williams
et al., 1998). While none of these studies identified a clear
relationship between smoking during pregnancy and child-
hood internalizing problems, the number of studies is quite
limited and further research is warranted.
The Present Study
The present study examines whether there is a direct effect
of smoking during pregnancy on child psychopathology,
addressing several of the methodological limitations in
the literature in several ways. First, this study extends
the limited range of studies of smoking during pregnancy
and children’s behavior problems in preschool children by
examining its effects in 4-year-olds. Second, we examined
the effects of smoking during pregnancy on internalizing,
as well as externalizing and attentional, problems.
Third, we included a wider range of psychosocial co-
variates than has previously been examined. The present
report is based upon data collected during the first wave of
a longitudinal study of the risk factors and correlates of the
development of oppositional behavior, anxiety, and depres-
sion in young children. We selected the risk factors to be
studied based on Bronfenbrenner’s (1979) bioecological
model, Cicchetti and Toth’s (1998) transactional model
of childhood depression, and Campbell’s (1990) model
of the development of externalizing behaviors. We also re-
viewed the literature associated with the development of
these disorders to identify additional, specific risk factors
that had been studied but not noted in the general models.
As Smeekens, Riksen-Walrave, and van Bakel (2007) have
noted, there are four domains of variables that have gener-
ally been proposed to be related to the development of
child externalizing problems; given the relative absence of
studies of specificity of risk factors (Shanahan, Copeland,
Costello, & Angold, 2008) and prior literature, the do-
mains appear to be relevant to internalizing disorders, as
well. These domains include: (1) contextual characteristics
(e.g., SES, stress); (2) parental characteristics (e.g., person-
ality, psychopathology); (3) parenting (e.g., support, scaf-
folding, hostility); and (4) child characteristics (e.g.,
attachment, temperament). We included risk factors from
each of these domains as possible psychosocial covariates
of smoking during pregnancy.
Fourth, the present study used multiple outcome mea-
sures rather than relying on single measures, as in most
prior studies. Finally, the present study examined the role
that NA may play as a preschool-age precursor to the
development of later problem behaviors as proposed by
Nigg and Breslau (2007).
Although the present study offers some methodologi-
cal advantages over prior studies, noted above, it is limited
by its use of retrospective report of smoking. As Knopick
(2009) has noted, there are times when a retrospective
report on smoking during pregnancy is necessary, even
though prospective reports, particularly those accompa-
nied by obtaining serum cotinine levels from the mother,
are ideal. Since the present study was initiated when the
children were 4 years old, retrospective reports were nec-
essary. The use of retrospective reports in the literature on
smoking during pregnancy, however, is not uncommon
Prenatal Smoking Effects
and collecting serum cotinine levels is still quite unusual.
In addition, while studying 4-year-olds means that behav-
ior problems that emerge early in the child’s life could be
studied, problems that might emerge later in life could not
be examined in the present report.
Participants were part of the first wave of the longitudinal
study described above. Children were recruited from 23 pri-
mary care pediatric practices throughout Cook County,
Illinois, and at 13 Chicago Public Schools with preschool
At the time of initial contact at the schools and prac-
tices, 1738 families expressed an interest in learning more
about the study. Subsequently, these families were con-
tacted by telephone to provide them with additional infor-
mation, and 831 (47.8%) families then completed the
Wave 1 evaluation. That participation rate was similar to
that in one prior preschoolers’ study (Lavigne et al., 1993);
it could not be compared to those of other large commu-
nity studies of children in this age group (Egger & Angold,
2006) because the recruitment rates were not described in
those reports. There were 35 children who did not meet
the following inclusion criteria: (1) child did not exhibit an
autistic spectrum disorder; (2) child and parent spoke
Spanish or English; (3) child had lived with the same pri-
mary caretaker for the prior 6 months (because otherwise
the caretaker may not have had sufficient experience to
report on the child’s functioning); (4) child obtained a
standard score on a language screen above 70 at baseline,
was not enrolled in a classroom for the mentally retarded,
or did not have a school IQ test below 70, because he/she
would not be able to participate in certain study tasks. Data
on smoking during pregnancy were not provided for an
additional 117 families, including 30 families in which fa-
thers completed study questionnaires. Because smoking
during pregnancy may be related to race or ethnicity, we
restricted the sample to the three largest race/ethnicity
groups in the sample (non-Hispanic whites, n¼421,
62.0%; African Americans, n¼113, 16.6%; Hispanic
Whites, n¼145, 21.4%). Thus, the final sample for anal-
ysis of the effects of smoking during pregnancy consisted of
679 children and families. The sample included 338 boys
(49.8%) and 341 girls (50.2%). The mean age was 4.43
years (range 3.87–5.14 years) at the time of assessment.
While all SES groups were represented, the sample was
skewed in the direction of the higher two Hollingshead
SES groups (74.4% higher in two SES groups). Smoking
during pregnancy occurred in 7.5% (n¼51) of the sample.
Mothers completed a demographic questionnaire that pro-
vided information concerning education and employment
to be coded into the Hollingshead Four-Factor Index of
Social Status (Hollingshead, 1975).
Smoking during Pregnancy
The measure of smoking during pregnancy from the
Smoke-Free Families clinical trials (Melvin, Tucker, &
Group, 2000) was used and information on smoking ob-
tained at the first wave visit with the family. Women were
asked: (a) if they had never smoked; (b) if they stopped
smoking before becoming pregnant and no longer smoke;
(c) stopped before pregnancy and resumed after the preg-
nancy; (d) if they continued to smoke after they became
pregnant and no longer smoke; (e) if they continued to
smoke after they became pregnant and were still smoking.
Women were considered to have smoked during pregnancy
if they reported they continued to smoke after they became
pregnant (category d and e) regardless of current smoking
status. Children were classified as exposed versus not ex-
posed to smoke prenatally.
As noted above, prospective reports on smoking are
preferable but, since prospective reports cannot always be
obtained (Knopik, 2009), it is important to determine the
accuracy of retrospective reports. Pregnancy is a time of
high importance to most women, and recall of events
during that time may differ from that for other periods.
Indeed, studies suggest that long-term recall of events
during pregnancy is generally quite good. In one report
(Tomeo et al., 1999), women were contacted 30 years,
on average, after their pregnancy and asked about specific
pregnancy- related events. Their responses were compared
to those obtained during their pregnancy as part of the
National Collaborative Perinatal Project. Sensitivity of
their recall of smoking was .86; specificity was .94. In
a second study (Heath et al., 2003), the reliability of
retrospective recall was assessed by comparing reports
of women about smoking during pregnancy with those of
their twin sisters. There was good agreement for self-report
and informant (sister)-report of smoking during pregnancy.
While retrospective reports are never preferred, these
data provide adequate support for the use of retrospective
reports of the presence/absence of smoking during
Composite Measures of Risk Factors
As part of the longitudinal study design, multiple measures
were used for several risk factors. To reduce the number of
predictors and avoid multicollinearity in the present study,
Lavigne et al.
composite measures of life stress, family conflict, maternal
depression, and support/scaffolding were created by con-
verting each measure to standard scores and calculating the
sum of the standard scores to create composite measures.
A composite life stress measure was created from: (1) the
total stress score of Abidin’s (1995) Parenting Stress Index
Short Form, a measure with acceptable internal consisten-
cy (i.e., a values >0.9) and test–retest reliability coeffi-
cients between .65 and .96 (Lessenberry & Rehfeldt,
2004); (2) the Perceived Stress Scale (Cohen, Kamarck,
& Mermelstein, 1983), a measure with high internal con-
sistency (a¼.84) and test–retest reliability (.86), which
correlates well with other measures of life stress; and (3)
(McCubbin, Thompson, & McCubbin, 1996), a¼.79.
A composite family conflict scale was created from: (1) the
Family Environment Scale conflict scale (Moos & Moos,
1981); (2) the McCubbin Family Distress Index, a measure
of family pressures and lack of social support (a¼.87)
(McCubbin et al., 1996); and (3) the McCubbin Family
Problem Solving/Communication scales (McCubbin et al.,
1996), which assesses conflict-related family communica-
tion (a¼.89; test–retest reliability¼.86).
A composite measure of maternal depression was created
from: (a) the Beck Depression Inventory (Beck & Steer,
1987; Beck, Ward, Mendelson, Mock, & Erbaugh,
1961), with an average internal consistency (a¼.86) in
clinical samples (Beck, Steer, & Garbin, 1988); (b) the
(Radloff, 1977), (a>.85), moderate reliability (.45–.70
across several weeks), and validity as reflected in correla-
tions with other depression scales (Radloff, 1977).
Maternal Support and Hostility
Maternal support and hostility were assessed with the
Parent Behavior Inventory (Lovejoy, Weis, O’Hare, &
Rubin, 1999). The two factor-analytically derived sub-
scales, Support/Engagement and Hostility/Coercion have
internal consistencies of .90 and .87 for the Support/
Engagement and Hostility/Coercion scales, respectively.
Test–retest reliabilities are .74 and .69, respectively.
A composite measure of parental support/scaffolding was
created from the NICHD Three Boxes task (NICHD Early
Childhood Research Network, 1999). This task consists
of two activities that are designed to be too difficult for
the child to accomplish without parental assistance, and
a free-play, parent–child activity. Maternal behavior during
the 15-min interaction is videotaped and rated on support/
scaffolding ability, i.e., skills and affect suited for assisting a
child in dealing with demanding tasks. Ratings are made on
seven-point Likert scales on the following dimensions: sup-
portive presence, quality of assistance, cognitive stimula-
tion, respect for autonomy, maternal confidence, and
hostility. Coders were trained to 80% reliability with two
master coders, and a random sample of 20% of the tapes
was double-coded to assess inter-rater reliability. Reliability
ranged from .69 for maternal hostility to .80 for quality of
assistance, with a mean reliability of .74. There was a low
base rate of maternal hostility during the videotaped ses-
sions which may have affected the intraclass correlations
for this variable. The composite measure of scaffolding
skills was calculated by summing the standard scores for
supportive presence, respect for autonomy, cognitive stim-
ulation, quality of assistance and confidence, and hostility
The Attachment Q-Sort (AQS) is a measure of attachment
security suitable for use with preschoolers that utilizes
Q-sort methodology to provide a continuous measure of
attachment security (Waters, 1987). After the 2-h home
visit that included a 45-min free interaction period as
well as interaction during the mother–child interaction
tasks, observers sorted 90 behavioral descriptions into
nine piles according to similarity with the target child’s
behavior. A security score was calculated by correlating
the child’s sort with that of a prototypically secure child.
A recent meta-analysis indicates that the AQS is a valid,
reliable measure when using observer ratings (van
IJzendoorn et al., 2004). Inter-rater reliability was assessed
by randomly selecting (in blocks of 10) 20% of the home
visits to be double-coded by two graduate research assis-
tants. Interrater reliability was .77. Observers were blind
to results for all other measures of child and family
Child Temperament: Negative Affect
The Children’s Behavior Questionnaire (CBQ) negative af-
fectivity (NA) scale of the was used to assess NA (Rothbart,
Ahadi, Hershy, & Fisher, 2001). Rothbart et al. (2001)
define temperament as ‘‘constitutionally based individual
differences in reactivity and self-regulation’’ (p. 1395). The
NA scale combines parent ratings of the child’s discomfort,
fear, anger/frustration, and sadness, with soothability (neg-
atively loaded). Item-total correlations for the CBQ range
Prenatal Smoking Effects
from .64 to .92 for 4 year olds, and 2-year stability is .69
(Rothbart et al., 2001).
Measures of Internalizing and Externalizing
Three measures assessed symptoms of ADHD (Diagnostic
Interview Schedule for Children-Parent Scale-Young Child:
DISC-YC; Child Symptom Inventory (CSI) ADHD scales;
DuPaul ADHD Rating Scales), ODD (DISC-YC ODD scale,
CSI ODD scale, Eyberg Scale), anxiety symptoms (DISC-YC
generalized anxiety scale, CSI generalized anxiety scale and
CSI separation anxiety scale) and depressive symptoms
(DISC-YC major depression scale; CSI major depression
scale, CSI dysthymia scale). For ADHD, the inattentive
(ADHD-I), and hyperactive (ADHD-H) subtypes were
examined separately, as well as the combined type
(ADHD-C), because recent factor analysis suggests the
two subtypes are well-differentiated in preschoolers
(Sterba, Egger, & Angold, 2007).
Diagnostic Interview Schedule for Children-Parent
Scale—Young Child Version
The young children’s Diagnostic Interview Schedule for
Children-Parent Scale—Young Child Version (DISC-YC)
(Fisher & Lucas, 2006) is a developmentally appropriate
adaptation of the DISC-P, a DSM-IV-based structured
parent interview. Because the rates of disorder were ex-
pected to be low in this sample, the symptom counts for
each disorder were used rather than the presence versus
absence of disorder. High levels of agreement are obtained
for concrete, observable symptoms, and test–retest reliabil-
ities for the DISC-YC are high. Overall reliability of symp-
tom scales (C. Lucas, personal communication, 2006) is
acceptable to high (test–retest reliability for ADHD
scales¼.67; for ODD, test–retest reliability¼.88; for anx-
iety and depression scales¼.57–.81). Ratings were ob-
tained for ADHD symptoms (combined, inattentive and
hyperactive/impulsive), ODD, anxiety and depression.
The parent form of the CSI (Gadow & Sprafkin, 1997,
2000) is a problem behavior checklist with items derived
from DSM-IV diagnostic criteria. Each scale was treated as
a continuous measure yielding T-scores. Overall reliability
of symptom scales is acceptable to high for ADHD scales
(a¼.91; test–retestreliability ¼.67); ODD (a¼.70;
(a¼.70–.83; test–retestreliability ¼.65–.77). As with
the DISC-YC, scales used included those for ADHD
symptoms (combined, inattentive and hyperactive/impul-
sive), ODD, anxiety and depression.
DuPaul ADHD Rating Scale
The ADHD Rating Scale (DuPaul et al., 1998) provided a
third measure of ADHD symptoms. This measure has
well-developed norms, an a of .92 overall, with test–
retest reliability of .85, and shows high levels of criterion
and discriminatory validity.
Eyberg Child Behavior Inventory
The Eyberg Child Behavior Inventory (ECBI) (Eyberg &
Pincus, 1999) is designed to assess parental report of
ODD symptoms. Criterion validity for the ECBI has been
assessed and found to be acceptable (test–retest reliability
ranges .86–.88; inter-rater reliability, .79–.86; and internal
consistency for the subscales ranges from .88 to .95
(Eyberg & Pincus, 1999).
Recruitment occurred in pediatric practices and schools
with preschool programs, during the first wave of data col-
lection when the children were 4 years old. Parents who
expressed interest were subsequently contacted by tele-
phone. A home visit was scheduled, and questionnaires
were mailed to the family. The home visit included a
45-min observation period followed by the structured
parent–child interaction paradigm. A research assistant
then conducted the DISC-YC interview, either in English
or Spanish, and parents subsequently completed the re-
mainder of the questionnaires. The total duration of the
home visit was about 2.5h. Procedures were approved
by the Institutional Review Boards of the authors’
For measures of psychopathology, multivariate analyses of
variance were conducted with the three measures of emo-
tional or behavior problems entered as dependent variables
and smoking during pregnancy, risk factors described
above, and the child’s gender entered as predictors. If
the overall effects on the measure of psychopathology
were significant, then the results for each individual mea-
sure of psychopathology were examined. For the analysis of
NA, linear regression was used because there was only one
measure of NA. The interaction of gender with smoking
during pregnancy was also examined. If the prenatal smok-
ing x gender interaction was significant, then gender effects
were examined in all subsequent analyses. Given the large
number of comparisons, a Bonferroni-type sequential Sidak
correction for multiple comparisons (Sidak, 1967) was
Lavigne et al.
used for hypothesis testing, while noting all findings for
which the traditional p value of .05 was achieved. With that
correction, a value of p<.00365 was adopted. SPSS 17.0
was used in data analysis.
Descriptive Statistics for Outcome Measures
As expected in a community sample, scores on each of the
outcome measures varied widely. If the sample included
children with high level of behavior or emotional disorders,
?10% of the sample should obtain scores that exceed the
cutoff score for the 90th percentile in the standardization
sample. Cutoff scores for the 90th percentile are available
for the CSI, and the percent above the 90th percentile
cutoff approximated 10% for ADHD-I (10.0%, n¼68),
ADHD-H (10.2%, n¼69), ADHD-C (9.5%, n¼65),
ODD (9.4%, n¼64). The rates for internalizing disorders
were slightly lower (GAD, 6.2%, n¼42; SAD, 6.6%,
n¼60), but the full range of scores were obtained on the
internalizing disorders scales. The mean, standard devia-
tion, and range for each CSI scales were: ADHD-I,
M¼5.87, SD¼4.18, R¼0–25; ADHD-H, M¼7.32,
SD¼5.1, R¼0–27; ADHD-C, M¼13.2, SD¼8.42,
R¼0–27; ODD, M¼5.13, SD¼3.63, R¼0–24; GAD,
R¼0–13; Dysthymia, M¼.76, SD¼1.23, R¼0–9.
MDD, 2.5%,n¼17;Dysthymia, 8.8%,
Relationship Between Smoking During
Pregnancy and Behavior Problems Without
When covariates were not included (Table I), the effects
of smoking during pregnancy were significant overall for
ADHD-I at the traditional p < .05 level, but not after cor-
recting for multiple comparisons. Smoking effects were not
significant for ADHD-H or ADHD-C. The results for each of
the individual measures of ADHD-I were also significant for
smoking during pregnancy. In the multivariate analyses,
gender effects were significant for each type of ADHD,
with boys showing more ADHD symptoms than girls for
all three types. The prenatal smoking x gender interaction,
however, was not significant for any type of ADHD
The relationship between smoking during pregnancy
and symptoms of ODD were not significant, nor were there
significant gender or prenatal smoking?gender interac-
tions for ODD.
The relationships between smoking during pregnancy and
symptoms of both anxiety and depression were not signif-
icant in the multivariate analyses. Gender effects were sig-
nificant and higher for boys, but prenatal smoking x gender
interaction effects were not significant.
The effect of smoking during pregnancy on NA approached
significance (?¼.098, t¼2.55, p¼.011) when corrected
for multiple comparisons, while the gender (?¼.04,
t¼1.04, p ¼.30) and prenatal smoking x gender interac-
tions (?¼–.112, t¼.91, p¼.36) were not significant.
Correlates of Smoking During Pregnancy
The relationship between smoking during pregnancy and
demographic and psychosocial variables related to a variety
of child psychiatric disorders were then examined. Among
demographic correlates, smoking during pregnancy was
Table I. Prenatal Smoking Effects, Without Covariates
Type of emotional/behavioral
Multivariate test results
Du Paul symptoms
Multivariate test results
Du Paul symptoms
Multivariate test results
Du Paul symptoms
Oppositional defiant symptoms
Multivariate test results
Multivariate test results
CSI symptoms (generalized anxiety)
CSI symptoms (separation anxiety)
Multivariate test results
CSI symptoms (depression)
CSI symptoms (dysthymia)
Note. *p<.05; **p<.01; ***p<.005; ****p<.001.
Prenatal Smoking Effects
related to lower levels of SES, t(677)¼4.47, p¼.001.
Therewere also race
p¼.001, with a higher percentage of smoking among
African American mothers (n¼18, 15.9%) than among
non-Hispanic Whites (n¼22, 5.2%), or Hispanic white
mothers (n¼10, 6.9%). Birth weight, t(677)¼.98,
p¼.33, was not related to smoking during pregnancy.
Among family climate variables, family stress, t(677)¼
3.19, p¼.002 and maternal depression, t(677)¼2.86,
p¼.006 were associated with smoking during pregnancy.
There was no relationship, however, between family con-
flict and smoking during pregnancy, t(677)¼.40, p¼.69.
Smoking during pregnancy was not associated with paren-
tal support/engagement, t(677) ¼.02, p¼.98. Hostility
and smoking during pregnancy were significantly related,
t(677)¼2.38, p¼.035 at the traditional p-value level but
not when corrected for multiple comparisons. Smoking
during pregnancy was not associated with support/scaf-
folding skills, t(677)¼1.94, p¼.053. There was a signifi-
cant relationship between smoking during pregnancy and
less secure attachment, t(677)¼3.41, p¼.001.
Models of Prenatal Smoking Effects
on Emotional/Behavioral Problems,
Including other Demographic and Psychosocial
Prior to examining models that included other demograph-
ic and psychosocial variables with smoking during
pregnancy, we examined the correlations between psycho-
social risk factors (Table II). All but one of the correlations
was low to moderate even when significant, suggesting that
the risk factors were largely independent of one another.
The correlation between life stress and maternal depression
however was moderate in size (r¼.62). In addition, t-test
results described above indicated that both life stress and
maternal depression were significantly associated with
smoking duringpregnancy.The moderately strong
relationships between these variables raised the possibility
that suppression effects could occur in regression analyses
if both stress and maternal depression were entered simul-
taneously along with prenatal smoking. Suppression occurs
when the relationship of one predictor variable to the cri-
terion variable is altered when it is corrected for its corre-
lation with another variable. When suppression is present,
the magnitude of the relationship between the predictor
and criterion variable may be reduced or can even reverse
the direction of the relationship. Suppression can be exam-
ined by removing one of the predictor variables from the
regression equation (Kline, 1998). We tested for this
possibility in models where the effects of smoking during
pregnancy were significant. We examined the effects of
smoking during pregnancy in regression models that
included demographic (SES, race dummy coded), family
climate (family conflict, stress), maternal depression, par-
enting (maternal support/engagement, maternal hostility,
maternal support/scaffolding skills, child attachment),
and child birth weight. Models were tested only for
ADHD-I, for which smoking during pregnancy showed a
significant relationship when covariates were not included,
and for NA, because the effects of smoking during preg-
nancy on NA approached the significance level for multiple
comparisons, we elected to conduct the analysis of NA
when psychosocial covariates were added.
As Table III indicates, the effect of smoking during preg-
nancy on ADHD-I was significant (p¼.048) at the tradi-
tional p-value level, when demographic, family climate,
maternal depression, parent–child interaction, and child
factors were included in the model, but was not significant
at the p¼.01 level for multiple comparisons. To examine
the possibility that suppression effects were present, the
analysis was repeated with life stress eliminated and
Table II. Correlates Between Psychosocial Risk Variables
1. Life stress
2. Family Conflict:
3. Maternal depression
5. Maternal hostility
6. Maternal Support/scaffolding skills
7. Attachment security
8. Birth weight (g)
Note. *p<.05; **p<.01; ***p<.001.
Lavigne et al.
the effects of smoking during pregnancy still were not
Other psychosocial variables were significantly associ-
ated with ADHD-I symptoms, including race (African
Americans higher than non-Hispanic whites), lower SES,
higher family conflict, maternal depression, higher mater-
nal hostility, lower support/engagement, poorer maternal
support-scaffolding, and less secure attachment.
Smoking during pregnancy was not significantly associated
with NA when the psychosocial covariates were included,
among those psychosocial risk factors, race (being Hispanic
rather than non-Hispanic white), family conflict, less ma-
ternal support/engagement, and more maternal hostility
were significantly associated with NA.
The present study examined the relationship between
smoking during pregnancy and behavior and emotional
problems in a community sample of 4-year-old children.
This study differed from most prior research in the use of a
large, diverse sample, the age of the children participating
in the study, the range of psychosocial factors studied, and
the use of multiple measures of child psychopathology.
The findings having implications for our understanding
of the relationship between smoking during pregnancy
and child psychopathology, as well as implications for
the design of future studies in this area.
First, in the present study, the relationship between
smoking during pregnancy and symptoms of ODD in pre-
schoolers was not significant, even without including other
risk factors and correlates of smoking during pregnancy.
While a small number of other studies of preschool chil-
dren have reported a significant relationship between
smoking during pregnancy and externalizing problems,
all (Day et al., 2000; Huijbregts et al., 2007; O’Callaghan
et al., 1997; Orlebeke et al., 1997; Wakschlag & Keenan,
2001) but one (Wakschlag et al., 2006) failed to control for
at least one covariate in each area of demographic, parental
psychopathology, parenting, family stress, and pre-/perina-
tal factors, and the latter study was limited by a lack of
racial/ethnic diversity in the sample. Thus, overall, there is
little evidence for a main effect of smoking during pregnan-
cy on oppositional behavior in preschool children.
Second, the present study failed to find a significant
relationship between smoking during pregnancy and either
ADHD-H or ADHD-C, and the relationship between smok-
ing during pregnancy and ADHD-I was not significant after
including a wide range of covariates. While these results
differ from prior studies (Huijbregts et al., 2007; McGee &
Stanton, 1994; Romano et al., 2008; Streissguth et al.,
1984), those studies failed to include the range of variables
included in the present study.
Third, consistent with three prior studies, the present
study failed to find a relationship between smoking during
pregnancy and internalizing disorders. Collectively, these
studied provide little evidence for an association of smok-
ing during pregnancy with these types of disorder.
Fourth, the present study does not support the devel-
opmental model proposed by Nigg and Breslau (2007).
That model posited that smoking during pregnancy con-
tributes to temperamentally-based NA in young children
which, combined with problems in parent–child relation-
ships, mediates the relationship between smoking during
pregnancy and the later development of ODD symptoms.
If NA serves as a mediator, then the relationship between
the independent variable (smoking during pregnancy) and
the mediator (NA) should be statistically significant (Baron
& Kenny, 1986). The results of the present study do not
support this model because there was a nonsignificant
effect for smoking during pregnancy on NA in young chil-
dren when controlling for theoretically and empirically
However, while the results of the present study do not
support a relationship between smoking during pregnancy
and behavior problems in preschool children, it is possible
that direct effects of smoking during pregnancy on behav-
ior and emotional problems do not emerge until children
are school age or older. While ODD in preschoolers
Table III. Multivariate Analyses of Prenatal Smoking Effects
Race (Dummy 1) African American
versus non-Hispanic White
Race (Dummy 2) Hispanic versus
Maternal support-scaffolding skills
Birth weight (grams)
Note.aLife stress variable removed to test for suppression effects.
*p<.05; **p<.01; ***p<.001.
Prenatal Smoking Effects
is reasonably stable, ODD symptoms do decline in some
children at about age 5 years (Lavigne et al., 1998), and the
direct effects of smoking during pregnancy on ODD and
other externalizing problems and ADHD might only
become apparent among those children with ODD persist-
ing into, or beginning in, the school years.
Finally, the present study demonstrates the impor-
tance of including a wide range of variables that are asso-
ciated with the development of child psychopathology in
order to estimate the effects of smoking during pregnancy.
While prior studies typically included demographic and
child health variables, and often assessed maternal psycho-
pathology and some aspects of family climate, important
aspects of mother–child interaction patterns, particularly
those required to promote secure attachment, have been
ignored. When the full range of variables was included in
the present study, reducing the effects of omitted variables,
the effects of smoking during pregnancy for ADHD-I that
had appeared significant no longer were. This is not entire-
ly surprising. Wakschlag et al. (2002) had raised concerns
about confounding variables in studying the effects of pre-
natal smoke exposure, concerns about the effects of omit-
ted variables in study psychopathology have been noted
before (Tomarken & Waller, 2003), and the results of
the present study are consistent with those predicted by
D’Onofrio et al. (2008), who argued that the relationship
between smoking during pregnancy and measures of child
psychopathology would be associated with environmental
risk factors other than those which had been studied pre-
viously. The results of the present study suggest a wide
range of correlates of prenatal smoke exposure, including
child attachment, should be included when studying the
effects of smoking during pregnancy.
The two main limitations of the present study involve
the use of retrospective reports of smoking and the inability
to assess dose effects of exposure to smoking during preg-
nancy. The present study used the retrospective report of
smoking during pregnancy from the Smoke-Free Families
clinical trial (Melvin et al., 2000) and classified the children
as exposed versus not exposed. We followed this proce-
dure because our confidence was greater that mothers
would more accurately recall whether or not they had
smoked during pregnancy than the number of cigarettes
they typically smoked at that time, and studies have indi-
cated that maternal recall for smoking during pregnancy is
good even over long periods of time. In addition, if the
measure used in the present study was not at all valid,
then significant correlations between many of the known
psychosocial correlates of smoking and prenatal smoke ex-
posure obtained with the measure used in the present
study wouldnot have been significant.However,
contemporaneous reports of smoking during pregnancy
are still to be preferred to retrospective reports. The
‘‘caveat’’ to be taken from this report is that a wide range
of psychosocial correlates needs to be included in future
studies on the effects of smoking during pregnancy when
contemporaneous or retrospective measures of smoking
A second major limitation concerns the possibility of
dose effects. Most studies of compared exposed to unex-
posed children, other studies have identified a dose effect,
with behavior problems emerging if mothers were relatively
heavier smokers. Since the present study did not examine
dose effects, it is possible that there is a dose effect for
smoking during pregnancy not detected in the present
study. The most important finding of the present study is
that, since the inclusion of the wide range of psychosocial
variables, particularly parenting variables and attachment,
examined in the present study showed no effect of prenatal
smoke exposure versus non-exposure, future studies of
dose effects for prenatal smoke exposure need to examine
these same critical variables to be definitive. Thus far, stud-
ies (Ashford et al., 2008; Button, Thapar, & McGuffin,
2005; D’Onofrio et al., 2008; Day et al., 2000;
Fergusson, Horwood, & Lynskey, 1993; Fergusson,
Woodward, & Horwood, 1998; Maughan, Taylor, Caspi,
& Moffitt, 2004; Silberg et al., 2003; Streissguth et al.,
1984; Thapar, Fowler, Rice, & al., 2003; Wakschlag
et al., 2006; Weitzman et al., 1992; Williams et al.,
1998) showing a dose-effect relationship with stronger
effects for heavier prenatal smoke exposure have failed to
do this, so the problem of ‘‘omitted variables’’ in
dose-effect studies remains. Future studies of dose-effect
relationships need to include a sufficiently broad represen-
tation of psychosocial factors associated either with smok-
ing or the development of behavior problems to assess the
strength of the relationship between smoking during preg-
nancy and child psychopathology.
A third limitation involves the use of a single parent
informant for many of the risk factors. The use of a single
informant increases the possibility that significant results
are inflated due to common method variance. However,
this was certainly not the case in the present study because
the main findings involved an absence of significant
relationships between the variables, so it is unlikely that
inflated effects sizes due to common method variance sig-
nificantly impacted the results. Also, in addition to
maternal-report, we used direct observation to examine
several of the risk variables included in this study (i.e.,
parent scaffolding, child attachment).
The strengths of this study include attention to pre-
schoolers, the wide range of covariates studied, the
Lavigne et al.
assessment of both externalizing and internalizing disor-
ders in young children, the use of multiple measures of
outcome rather than reliance upon a single measure, and
the inclusion of a large, diverse community sample. These
results highlight the importance of carefully selecting the-
oretically relevant, empirically tested variables that may
serve as mediators in the relationship between smoking
during pregnancy and child internalizing and externalizing
problems. This is consistent with current approaches in
developmental psychopathology, in which researchers are
turning their attention to the interaction between biological
and psychosocial variables as causal factors in child disor-
ders, rather than focusing on only one of these aspects of
human functioning (Cicchetti & Curtis, 2007) .
The authors wish to thank the Chicago Public Schools
Department of Early Childhood Education, school princi-
pals, lead teachers and participating pediatricians in the
Pediatric Practice Research Group who participated in
National Institute of Mental Health RO1 MH 063665,
Principal Investigator, John V. Lavigne.
Conflicts of interest: None declared.
Abidin, R. R. (1995). Manual for the Parenting Stress
Index. Odessa, FL: Psychological Assessment
Ashford, J., van Lier, P. A. C., Timmermans, M.,
Cuijpers, P., & Koot, H. M. (2008). Prenatal
smoking and internalizing and externalizing problems
in children studied from childhood to late adoles-
cence. Journal of the American Academy of Child and
Adolescent Psychiatry, 47(7), 779–787.
Baron, R. M., & Kenny, D. A. (1986). The moderator-
mediator variable distinction in social psychological
research: Conceptual, strategic, and statistical
considerations. Journal of Personality and Social
Psychology, 51, 1173–1182.
Batstra, L., Hadders-Algra, M., & Neeleman, J. (2003).
Effect of antenatal exposure to maternal smoking on
behavioural problems and academic achievement in
childhood: Prospective evidence from a Dutch birth
cohort. Early Human Development, 75(102), 21–33.
Beck, A. T., & Steer, R. A. (1987). Beck Depression
Inventory Manual. San Antonio: Psychological
Beck, A. T., Steer, R. A., & Garbin, M. G. (1988).
Psychometric properties of the Beck Depression
Inventory: Twenty-five years of evaluation. Clinical
Psychology Review, 8, 77–100.
Beck, A. T., Ward, C. H., Mendelson, M., Mock, J.,
& Erbaugh, J. (1961). An inventory for measuring
depression. Archives of General Psychiatry, 4,
Brennan, P. A., Grekin, E. R., & Mednick, S. A. (1999).
Maternal smoking during pregnancy and adult male
criminal outcomes. Archives of General Psychiatry,
Bronfenbrenner, U. (1979). The ecology of human develop-
ment: Experiments by nature and design. Cambridge,
MA: Harvard University Press.
Brook, J. S., Brook, D. W., & Whiteman, M. (2000).
The influence of maternal smoking during pregnancy
on the toddler’s negativity. Archives of Pediatric and
Adolescent Medicine, 154(4), 381–385.
Button, T. M. M., Maughan, B., & McGuffin, P. (2007).
The relationship of maternal smoking to psychologi-
cal problems in offspring. Early Human Development,
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. (1990). Behavior problems in preschool
children: Clinical and developmental issues. New York:
Cicchetti, D., & Curtis, W. J. (2007). Multilevel
perspectives on pathways to resilient functioning.
Development & Psychopathology, 19, 627–629.
Cicchetti, D., & Toth, S. L. (1998). The development of
depression in children and adolescents. American
Psychologist, 53, 221–241.
Cohen, S., Kamarck, T., & Mermelstein, R. (1983). A
global measure of perceived stress. Journal of Health
and Social Behavior, 24, 385–396.
Cornelius, M. D., Ryan, C. M., Day, N. L.,
Goldschmidt, L., & Willford, J. (2001). Prenatal
tobacco effects on neuropsychological outcomes
among preadolescents. Journal of Developmental and
Behavioral Pediatrics, 22(4), 217–225.
D’Onofrio, B. M., Van Hulle, C. A., Waldman, I. D.,
Rodgers, J. L., Harden, K. P., Rathouz, P. H.,
& Lahey, B. B. (2008). Smoking during pregnancy
and offspring externalizing problems: An exploration
Prenatal Smoking Effects
of genetic and environmental confounds.
Development and Psychopathology, 20, 139–164.
Day, N. L., Richardson, G. A., Goldschmidt, L.,
& Cornelius, M. D. (2000). Effects of prenatal
tobacco exposure on preschoolers’ behavior. Journal
of Developmental and Behavioral Pediatrics, 21(3),
DuPaul, G. H., Anastopoulos, A. D., Power, T. J.,
Reid, R., Ikeda, M. J., & McGoey, K. E. (1998).
Parent ratings of attention-deficit/hyperactivity
disorder symptoms: Factor structure and normative
data. Psychopathology and Behavioral Assessment, 20,
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(3/4), 313–337.
Eyberg, S., & Pincus, D. (1999). Eyberg Child Behavior
Inventory Manual. Lutz, Fl: Psychological Assessment
Fergusson, D. M., Horwood, J., & Lynskey, M. T.
(1993). Maternal smoking before and after
pregnancy: Effects on behavioral outcomes in middle
childhood. Pediatrics, 92, 815–822.
Fergusson, D. M., Woodward, L. J., & Horwood, J.
(1998). Maternal smoking during pregnancy and
psychiatric adjustment in late adolescence. Archives
of General Psychiatry, 55, 721–727.
Fisher, P., & Lucas, C. (2006). Diagnostic Interview
Schedule for Children (DISC-IV)-Young Child.
New York: Columbia University.
Gadow, K. D., & Sprafkin, J. (1997). Early Childhood
Inventory 4 Norms Manual. Stonybrook, NY:
Gadow, K. D., & Sprafkin, J. (2000). Early Childhood
Inventory 4 Screening Manual. Stonybrook, NY:
Heath, A. C., Knopik, V. S., Madden, P. A., Neuman, R.
J., Lynskey, M. J., Slutske, W. S., ... Martin, N. G.
(2003). Accuracy of mothers’ retrospective reports of
smoking during pregnancy: Comparison with twin
sister informant reports. Twin Research, 6(4),
Hollingshead, A. B. (1975). Four-factor Index of Social
Position. Yale University Department of Sociology.
Huijbregts, S. C., Seguin, J. R., Zoccolillo, M., Boivin, M.,
& Tremblay, R. E. (2007). Associations of maternal
prenatal smoking with early childhood physical
aggression, hyperactivity-impulsivity, and their co-
occurrence. [erratum appears in Journal of Abnormal
Child Psychology 2007, 35(4), 683]. [Research
Support, Non-U.S. Gov’t]. Journal of Abnormal Child
Psychology, 35(2), 203–215 .
Iacobucci, D. (2008). Mediation analysis. Thousand Oaks,
Kline, R. B. (1998). Principles and practice of structural
equation modeling. NY: Guilford.
Knopik, V. S. (2009). Maternal smoking during preg-
nancy and child outcomes: Real or spurious effect?
Developmental Neuropsychology, 34(1), 1–36.
Knopik, V. S., Heath, A. C., Jacob, T., Slutske, W. S.,
Bucholz, K. K., Madden, P. A. F., ... Martin, N. G.
(2006). Maternal alcohol use disorder and offspring
ADHD: Disentangling genetic and environmental
effects using a children-of-twins design. Psychological
Medicine, 36, 1461–1471.
Lassen, K., & Oei, T. P. S. (1998). Effects of maternal
cigarette smoking during pregnancy on long-term
physical and cognitive parameters of child develop-
ment. Addictive Behaviors, 23(5), 635–653.
Lavigne, J. V., Arend, R., Rosenbaum, D., Binns, H. J.,
Christoffel, K. K., & Gibbons, R. D. (1998).
Psychiatric disorders with onset in the preschool
years: I. Stability of diagnosis. Journal of the American
Academy of Child and Adolescent Psychiatry, 37(12),
Lavigne, J. V., Binns, H. J., Christoffel, K. K.,
Rosenbaum, D., Arend, R., Smith, K., ... The
Pediatric Practice Research Group. (1993). Behavioral
and emotional problems among preschool children
in pediatric primary care: Prevalence and pediatri-
cians’ recognition. Pediatrics, 91, 649–655.
Lessenberry, B., & Rehfeldt, R. (2004). Evaluating stress
levels of parents of children with disabilities.
Exceptional Children, 70, 231–244.
Linnett, K. M., Dalsgaard, S., Obel, C., Wisborg, K.,
Henriksen, T. B., Rodriguez, A., ... Jarvelin, M. -R.
(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.
Lovejoy, C. M., Weis, R., O’Hare, E., & Rubin, E. C.
(1999). Development and initial validation of the
Parent Behavior Inventory. Psychological Assessment,
Maughan, B., Taylor, A., Caspi, A., & Moffitt, T. E.
(2004). Prenatal smoking and early childhood
conduct problems. Archives of General Psychiatry, 61,
McCubbin, H. I., Thompson, A. I., & McCubbin, M. A.
(1996). Family assessment: Resiliency, coping and
Lavigne et al.
adaptation: Inventories for research and practice.
Madison, WI: University of Wisconsin Publishers.
McGee, R., & Stanton, W. R. (1994). Smoking in
pregnancy and child development to age 9 years.
Journal of Paediatric Child Health, 30, 263–268.
Melvin, C. L., Tucker, P., & Group, S. F. F. C. E. M. W.
(2000). Measurement and definition for smoking
cessation intervention research: The Smoke-Free
Families experience. Tobacco Control, 9 (Suppl III),
Moos, R. H., & Moos, B. S. (1981). Family Environment
Scale Manual. Palo Alto, CA: Consulting
NICHD Early Childhood Research Network (1999). Child
care and mother-child interaction in the first three
years of life. Developmental Psychology, 35,
Nigg, J. T., & Breslau, N. (2007). Prenatal smoking
exposure, low birth weight, and disruptive behavior
disorders. Journal of the American Academy of Child
and Adolescent Psychiatry, 46(3), 362–369.
O’Callaghan, M. J., Williams, G. M., Andersen, M. J.,
Bor, W., & Nahman, J. M. (1997). Obstetric and
perinatal factors as predictors of child behaviour at
5 years. Journal of Paediatric Child Health, 33,
Orlebeke, J. F., Knol, F. C., & Verhulst, F. C. (1997).
Increase in child behavior problems resulting from
maternal smoking during pregnancy. Archives of
Environmental Health, 52, 317–321.
Radloff, L. A. (1977). The CES-D Scale: A self-report
depression scale for research in the general
population. Applied Psychological Measurement, 1,
Rice, F., Harold, G. T., Boivin, J., Hay, D. F., van den
Bree, M., & Thapar, A. (2009). Disentangling
prenatal and inherited influences in humans with an
experimental design. Proceedings of the National
Academy of Sciences of the United States of America,
Romano, E., Tremblay, R. E., Farhat, A., & Cote, S.
(2008). Development and prediction of hyperactive
symptoms form 2 to 7 years in a population-based
sample. Pediatrics, 117, 2101–2110.
Rothbart, M. K., Ahadi, S. A., Hershy, K. L., & Fisher, P.
(2001). Investigations of temperament at three to
seven years: The Children’s Behavior Questionnaire.
Child Development, 72(5), 1394–1408.
Shanahan, L., Copeland, W., Costello, E. J.,
& Angold, A. (2008). Specificity of putative psycho-
social risk factors for psychiatric disorders in children
and adolescents. Journal of Child Psychology and
Psychiatry, 49(1), 34–42.
Sidak, Z. (1967). Rectangular confidence regions for the
means of multivariate normal distributions. Journal of
the American Statistical Association, 63, 626–633.
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 distur-
bance: An examination of the causal hypothesis.
Biological Psychiatry, 53, 130–135.
Smeekens, S., Riksen-Walraven, J. M., & van Bakel, H. J.
A. (2007). Multiple determinants of externalizing
behavior in 5-year-olds: A longitudinal model. Journal
of Abnormal Child Psychology, 35, 347–361.
Stene-Larsen, K., & Borge, A. I. H. (2009). Maternal
smoking in pregnancy and externalizing behavior in
18-month-old children: Results from a population-
based prospective study. Journal of the American
Academy of Child and Adolescent Psychiatry, 48(3),
Sterba, S. K., Egger, H. E., & Angold, A. (2007).
Diagnostic specificity and nonspecificity in the
dimensions of preschool psychopathology. Journal of
Child Psychology and Psychiatry, 48(10), 1005–1013.
Streissguth, A. P., Martin, D. C., Barr, H. M.,
& Sandman, B. M. (1984). Intrauterine alcohol and
nicotine exposure: Attention and reaction time in
4-year-old children. Developmental Psychology, 20(4),
Thapar, A., Fowler, T., Rice, F., Scourfield, J., van den
Bree, M., Thomas, H., ... Hay, D. (2003).
Maternal smoking during pregnancy and attention
deficit hyperactivity disorder symptoms in offspring.
American Journal of Psychiatry, 160(11), 1985–1989.
Tomarken, A. J., & Waller, N. G. (2003). Potential
problems with ‘‘well fitting’’ models. Journal of
Abnormal Psychology, 112(4), 578–598.
Tomeo, C. A., Rich-Edwards, J. W., Michels, K. B.,
Berkey, C. S., Hunter, D. J., Frazier, L., ... Buka, S.
L. (1999). Reproducibility and validity of maternal
recall of pregnancy-related events. Epidemiology,
van IJzendoorn, M., Vereijken, C., Bakermans-
Kranenburg, M., & Riksen-Walraven, J. (2004).
Assessing attachment security with the Attachment
Q-sort: Meta-analytic evidence for the validity of the
observer AQS. Child Development, 75, 1188–1213.
Wakschlag, L. S., & Keenan, K. (2001). Clinical
significance and correlates of disruptive behavior
symptoms in environmentally at-risk preschoolers.
Journal of Clinical Child Psychology, 30, 262–275.
Prenatal Smoking Effects
Wakschlag, L. S., Leventhal, B. L., Pine, D. S., Pickett, K. Download full-text
E., & Carter, A. S. (2006). Elucidating early
mechanisms of developmental psychopathology: The
case of prenatal smoking and disruptive behavior.
Child Development, 77(4), 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,
Waters, E. (1987). Attachment Q-set (version 3.0). Stony
Brook, NY: State University of New York at Stony
Weitzman, M., Gortmaker, S., & Sobol, A. (1992).
Maternal smoking and behavior problems of
children. Pediatrics in Review, 90(3), 342–348.
Williams, G. M., O’Callaghan, M., Najman, J. M., Bor, W.,
Andersen,M. J.,Richardson, D., & Chinlyn, N.(1998).
Maternal cigarette smoking and child psychiatric mor-
bidity: A longitudinal study. Pediatrics, 102, e11.
Lavigne et al.