B R I T I S H J O U R N A L O F P S YC H I AT RY ( 2 0 0 5 ) , 1 8 7, 1 5 5 ^ 1 6 0
Relationship between antisocial behaviour,
attention-deficit hyperactivity disorder
and maternal prenatal smoking
T. M. M. BUT TON, A. THAPAR and P. McGUFFIN
Background There is substantial
evidence that maternal smoking during
pregnancy is associated with both
antisocial behaviour and symptoms of
attention-deficit hyperactivity disorder
(ADHD) in offspring.However, it is not
clear whether maternal smoking during
pregnancy is independently associated
with antisocial behaviour or whether the
association arises because antisocial
behaviour and ADHD covary.
Aims To examine the relationship
between maternal smoking during
pregnancy, antisocial behaviour and
ADHD in offspring.
Method Questionnaires concerning
behaviour and environmental factors
were sentto twins from the CaStANET
study and data analysed using a number of
bivariate structural equation models.
Results Maternal prenatal smoking
contributed small but significant amounts
to the variance of ADHD and of antisocial
behaviour.The best fitting bivariate model
was one in which maternal prenatal
smoking had a specific influence on each
phenotype, independent of the effect on
the other phenotype.
Conclusions Both antisocial behaviour
and ADHD symptoms in offspring are
independently influenced by maternal
prenatal smoking during pregnancy.
Declaration of interest None.
Funding detailed in Acknowledgement.
Maternal prenatal smoking has been
consistently associated with conduct disorder and delinquency (Fergusson et al,
al,
1998; Maughan et al,
al, 2001) and
attention-deficit hyperactivity disorder
(ADHD) (Mick et al,
al, 2002; Thapar et al,
al,
2003) in children and adolescents. Associations remain after controlling for confounding variables such as socio-economic status,
maternal age, birth weight and maternal
psychopathology (Fergusson et al,
al, 1998;
Brennan et al,
al, 1999) and have been
described for both males and females
(Fergusson et al,
al, 1998; Maughan et al,
al,
2001). Several reasons for this association
have been suggested, including direct
effects of nicotine on the developing foetus
(Cornelius & Day, 2000) and even genetic
mediation (Fergusson et al,
al, 1998; Brennan
et al,
al, 1999). Antisocial behaviour and
ADHD commonly covary, with evidence
that ADHD behaves as a risk factor for
subsequent antisocial behaviour (Fergusson
& Horwood, 1995; Taylor et al,
al, 1996).
Thus, it has been suggested that the association between antisocial behaviour and
maternal prenatal smoking may arise
indirectly, mediated by the influence of
prenatal smoking on ADHD, and the comorbidity between antisocial behaviour
and ADHD (Thapar et al,
al, 2003). Comorbidity between ADHD and antisocial
behaviour appears to be largely due to the
influence of the same genes on the two
phenotypes (Silberg et al,
al, 1996; Thapar et
al,
al, 2003), although there is some evidence
that environmental risk factors may also
contribute (Burt et al,
al, 2001).
The aim of the present study was to
investigate whether maternal prenatal
smoking contributes to the comorbidity
between antisocial behaviour and ADHD,
or whether the association between
maternal prenatal smoking and antisocial
behaviour is mediated by ADHD, given
the evidence that ADHD may increase the
risk of antisocial behaviour (Schachar &
Tannock, 2002).
METHOD
Participants
The participants were a part of CaStaNET
(Cardiff Study of All Wales and North West
England Twins), a population-based twin
register. The twins in this study were a
sample of school age born between 1980
and 1991 in Greater Manchester (Thapar
et al,
al, 2000). At the time of the study these
twins were aged 5–18 years. Of the 2846
families who were sent questionnaires,
2082 (73%) returned completed forms.
Zygosity was determined using parental
responses to a twin similarity questionnaire, with an accuracy of 95% (Cohen et
al,
al, 1975). Owing to ambiguous responses
162 twins were not assigned zygosity; 731
monozygotic twin pairs (383 female and
348 male) and 1189 dizygotic twin pairs
(313 female, 276 male, and 600 opposite
gender) were identified. However, 8 monozygotic and 16 dizygotic twin pairs whose
mothers did not provide data regarding
their prenatal smoking were eliminated
from the analysis, resulting in a final
sample of 723 monozygotic and 1173
dizygotic twin pairs. The age distribution
of the twins in this analysis was: 5–9 years,
34.4%; 10–14 years, 47.4%; and 15+
years, 18.2%.
Measures
Parents were asked to complete the Rutter
A scale (Rutter, 1970), an extensively used,
parent report questionnaire with good
validity, retest reliability and interrater
reliability. Antisocial behaviour in the
twins was measured using antisocial items
from the scale, which were: ‘does he ever
steal things?’, ‘often destroys own or
other’s belongings’, ‘is often disobedient’,
‘often tells lies’, and ‘bullies other children’.
Item scores were summed for each twin.
The presence of ADHD was assessed using
a modified version of the DuPaul ADHD
rating scale (DuPaul, 1981), which contained 14 DSM–III–R ADHD symptoms
(American Psychiatric Association, 1987),
and was augmented with four additional
items to cover ICD–10 symptoms of hyperkinetic disorder (World Health Organization, 1993; Thapar et al,
al, 2001). Scores
were regressed for age and gender, and
standardised values were calculated prior
to genetic analysis to eliminate any inflation of common environment effects across
same-gender twins (McGue & Bouchard,
1984).
15 5
B U T TON E T A L
As a measure of maternal prenatal
smoking, mothers were asked to retrospectively report how many cigarettes they
smoked daily during their pregnancy
according to four categories: non-smokers
(0 cigarettes), light smokers (1–10), moderate smokers (11–20) and heavy smokers
(over 20).
Statistical analysis
Initial statistical analyses were performed
using the Statistical Package for the Social
Sciences, version 10 for Windows (Kinnear
& Gray, 2000). Data were double-entered
to avoid any bias owing to birth order,
and twin order was then selected randomly.
The structural equation modelling package
Mx (Neale, 1997) was used to test a univariate model that enables us to estimate
the proportion of the phenotypic variance
attributable to additive genetic effects,
non-additive genetic effects, and nonshared environmental effects and maternal
prenatal smoking (Fig. 1).
To examine the relationship between
maternal prenatal smoking, antisocial
behaviour and ADHD two further models
were used. The first of these was a
Cholesky model, which enabled us to look
at the extent to which genes and the environment contribute to both the individual
phenotypic variation and the phenotypic
covariation between the two. This model
also incorporated the measure of maternal
prenatal smoking to investigate whether
smoking independently contributed to each
phenotype (Fig. 2).
The final model tested was one in
which the relationship between maternal
smoking in pregnancy and antisocial behaviour is mediated by ADHD, with maternal
prenatal smoking increasing the risk of
ADHD, and ADHD in turn increasing the
risk of antisocial behaviour. This ‘causal’
model is shown in Fig. 3.
The fit of all models was tested using w2
and Akaike’s information criterion (AIC),
which is calculated as w2 minus twice the
degrees of freedom, and provides an index
both of parsimony and goodness of fit.
The fit of nested models is also tested and
compared with the full model by comparisons of the goodness of fit and also AIC
values. The best fitting model was selected
as that in which pathways could be
dropped without a significant reduction in
the fit of the model, and also with the
lowest AIC value.
15 6
Fig. 1 A univariate ADE model which includes maternal smoking effects on the twins’ phenotypes (attentiondeficit hyperactivity disorder and antisocial behaviour). A, additive genetic influences; D, non-additive genetic
influences; E, non-shared environmental influences; S, latent variable of maternal smoking which contributes to
the twins’ antisocial phenotype as well as being the sole source of variance for the maternal prenatal smoking
score (‘smoke’); MZ, monozygotic; DZ, dizygotic.
Fig. 2
A Cholesky decomposition. A1, additive genetic effects with influence on both attention-deficit hyper-
activity disorder (ADHD) (a1) and antisocial behaviour (a2 ); A2, additive genetic effects specific to antisocial
behaviour (a2 ); A2, additive genetic effects specific to antisocial behaviour (a3); D1, non-additive genetic effects
with influence on ADHD (d1); E1, non-shared environmental effects with influence on both ADHD (e1) and antisocial behaviour (e2 ); E2, non-shared environmental effects specific to antisocial behaviour (e3); S, prenatal
smoking effects; s1, proportion of the variance of ADHD attributable to S; s2, proportion of the variance of
antisocial behaviour attributable to S; v, the influence of the latent prenatal smoking variable on the prenatal
smoking score.
RESULTS
Males scored higher than females for both
antisocial behaviour and ADHD symptoms, with means of 1.46 (s.d.¼1.87)
(s.d. 1.87) for
antisocial
behaviour
and
14.47
(s.d.¼11.97)
(s.d. 11.97) for ADHD for males and
0.92 (s.d.¼1.47)
(s.d. 1.47) and 9.30 (s.d.¼9.48)
(s.d. 9.48) for
females. The mean scores remained
constant across age. A Mann–Whitney Utest confirmed these differences to be significant (ADHD: Z¼7
710.80, P50.001;
antisocial behaviour: Z¼7
77.61, P50.001).
Of the 29.1% (552) of mothers who
reported smoking during pregnancy,
38.6% (213) smoked 1–10 cigarettes/day,
P R E N ATA L S M OK IIN
N G , A N T I S O C I A L B E H AV I OU R A ND
ND A D
DH
HD
Fig. 3
A causal model. A1, additive genetic effects influencing attention-deficit hyperactivity disorder (ADHD)
(a1); A2, additive genetic effects influencing antisocial behaviour (a3); D1, non-additive genetic effects influencing
behaviour, the best fitting Cholesky decomposition model is one in which path a3 was
dropped, thus setting the genetic correlation at 1.0. Thus there are no genetic
effects specific to antisocial behaviour.
Non-shared environment also appears to
influence the correlation between the two
phenotypes. Moreover, it is not possible
to drop the two paths from smoking to
antisocial behaviour or ADHD, indicating
that smoking is significantly associated
with both phenotypes, contributing
approximately 2% of the variance for
ADHD and 3% for antisocial behaviour.
Although it is not possible to directly
compare the ‘causal’ model with the
Cholesky model, the model in which the
relationship between maternal prenatal
smoking and antisocial behaviour was
mediated by ADHD did not fit the observed
data, judging by the large and significant w2
fit, whereas the Cholesky model does
appear to satisfactorily explain our data
statistically.
ADHD (d1); E1, non-shared environmental effects influencing ADHD (e1); E2, non-shared environmental effects
influencing antisocial behaviour (e3); S, prenatal smoking effects; s, proportion of the variance of ADHD attributable to S; v, the influence of the latent prenatal smoking variable on the prenatal smoking score; b, the causal
Causes of covariation
relationship between ADHD and antisocial behaviour.
55.1% (304) smoked 11–20/day and 6.3%
(35) smoked more than 20/day. The mean
scores for both antisocial behaviour and
ADHD increased with the number of cigarettes smoked. Means of 70.11 and 70.09
for antisocial behaviour and ADHD respectively were calculated for the non-smoking
category, 0.15 and 0.11 were calculated
for those smoking fewer than 10 cigarettes
per day. Means were 0.35 and 0.24 for
those smoking 11–20/day, and 0.24 and
0.30 for those smoking 20 or more cigarettes per day. Both antisocial behaviour
and ADHD correlated significantly with
amount of maternal prenatal smoking
(antisocial behaviour: r¼0.17,
0.17, P50.001;
ADHD: r¼0.14,
0.14, P50.001).
A gender limitation model was used to
identify whether the parameter estimates
differed significantly across gender; for
ADHD no such difference was found
(Dw¼2.823
2.823(4), P¼0.588),
0.588), although for antisocial behaviour there was a small but significant difference (D
(Dw¼24.206
24.206(4), P50.001.)
However, as we were not aiming to examine gender differences in these analyses we
regressed out both gender and age differences and included males, females and
opposite-gender twin pairs in our analyses.
DISCUSSION
Univariate models
The monozygotic and dizygotic correlations for ADHD were 0.74 and 0.45 respectively, and the respective correlations for
antisocial behaviour were 0.68 and 0.44,
suggesting a genetic contribution to both.
The univariate analyses showed ADHD to
be moderately heritable, with both an additive and non-additive genetic component.
Neither of these parameters could be
dropped from the univariate analysis without significantly reducing the fit of the
model. The broad heritability of this phenotype is thus approximately 74%. However,
dropping non-additive genetic influences
(D) from the antisocial behaviour model
did not result in a worse fit, although dropping additive genetic influences (A) did.
The AE model is thus the best fit, and the
heritability is 66% (Table 1).
Bivariate models
A substantial correlation of 0.62
(P50.001) between antisocial behaviour
and ADHD was demonstrated, and the
results of bivariate model fitting are presented in Table 2. As it was possible to drop
additive genetic effects specific to antisocial
Both ADHD and antisocial behaviour have
a substantial genetic and moderate nonshared environmental influence, although
there is evidence of both additive and
non-additive genetic influences on ADHD
and only additive genetic influences on antisocial behaviour. As shown previously in
other studies (Silberg et al,
al, 1996) and for this
data-set using categorical definitions (Thapar
et al,
al, 2001), additive genetic influences account for most of the covariation between
the two, with a non-shared environmental
effect also contributing to a small extent.
Contribution of maternal prenatal
smoking to the phenotype
Consistent with previous studies, we found
that maternal smoking during pregnancy
was associated with antisocial behaviour
as well as ADHD, contributing 3% to the
variance of antisocial behaviour and 2%
to the variance of ADHD.
Relationship between maternal
prenatal smoking, ADHD
and antisocial behaviour
We investigated whether the relationship of
maternal prenatal smoking with antisocial
behaviour was attributable to the association of maternal smoking in pregnancy
and ADHD and the covariation of the
157
Phenotype
ADHD2
A
C
D
E
S
w2
d.f.
P
AIC
(95% CI)
(95% CI)
(95% CI)
(95% CI)
(95% CI)
(difference)1
(difference)1
(difference)1
(difference)1
Model
78.012
ADES4
0.37 (0.17^0.57)
[0]
0.37 (0.17^0.58)
0.24 (0.21^0.26)
0.02 (0.01^0.03)
5.988
7
0.541
ACES
0.74 (0.70^0.77)
0.00 (0.00^0.02)
[0]
0.25 (0.22^0.28)
0.02 (0.01^0.03)
20.137
7
0.005
6.137
AES
0.74 (0.71^0.77)
[0]
[0]
0.25 (0.22^0.28)
0.02 (0.01^0.03)
20.137 (14.149)
8 (1)
0.010 (5
(50.001)
4.137 (12.149)
DES
[0]
[0]
0.75 (0.72^0.77)
0.23 (0.21^0.26)
0.02 (0.01^0.03)
18.316 (12.328)
8 (1)
0.020 (5
(50.001)
4.137 (12.149)
CES
[0]
0.45 (0.41^0.48)
[0]
0.53 (0.50^0.57)
0.02 (0.01^0.03)
27.751 (237.614)
8 (1)
50.001 (5
(50.001)
241.751 (235.614)
50.001 (5
(50.001)
37.801 (45.813)
ADE
0.43 (0.22^0.63)
[0]
0.33 (0.13^0.54)
0.24 (0.21^0.26)
[0]
53.801 (47.813)
8 (1)
Antisocial
ADES
0.59 (0.40^0.69)
[0]
0.07 (0.00^0.27)
0.30 (0.27^0.34)
0.03 (0.02^0.04)
8.796
7
0.268
behaviour3
ACES
0.66 (0.58^0.70)
0.00 (0.00^0.07)
[0]
0.31 (0.28^0.34)
0.03 (0.02^0.04)
9.336
7
0.229
AES4
0.66 (0.63^0.70)
[0]
[0]
0.31 (0.28^0.34)
0.03 (0.02^0.04)
9.336 (0.540)
8 (1)
DES
[0]
[0]
0.68 (0.64^0.71)
0.29 (0.26^0.33)
0.03 (0.02^0.04)
42.180 (33.384)
8 (1)
50.001 (5
(50.001)
CES
[0]
0.43 (0.40^0.47)
[0]
0.54 (0.50^0.57)
0.03 (0.02^0.04)
138.408 (129.068)
8 (1)
50.001 (5
(50.001) 122.408 (127.068)
ADE
0.68 (0.49^0.73)
[0]
0.01 (0.00^0.21)
0.30 (0.27^0.34)
[0]
89.483 (80.687)
8 (1)
50.001 (5
(50.001)
0.315
(0.462)
75.204
74.664
76.664 (7
(71.460)
26.180 (31.384)
73.483 (78.687)
A, additive genetic influences; C, common environmental influences; D, non-additive genetic influences; E, non-shared environmental influences; S, influence of maternal smoking; AIC, Akaike’s information criterion; [0], variable fixed at zero.
1. Differences between the nested models and the full saturated ADES model, except for the CES model, which is compared with the saturated ACES model.
2. No gender differences (difference between free and equated models: w 2¼2.823,
2.823, d.f.¼4,
d.f. 4, P¼0.588).
0.588).
3. Gender differences evident (difference between free and equated models: w 2¼24.206,
24.206, d.f.¼4,
d.f. 4, P50.001).
4. Best-fitting model for each phenotype.
Table 2
Results of bivariate model fitting
Model
ADHD
a1
d1
e1
Correlation
s1
a2
e2
ASB
a3
e3
Fit
s2
w2
d.f.
P
AIC
(difference)1
(difference)1
(difference)1
(difference)1
Cholesky
0.42
0.33
0.23
0.02
0.50
0.03
0.16
0.27
0.03
22.303
20
Drop s1
0.46
0.31
0.23
[0]
0.49
0.03
0.19
0.28
0.01
69.515 (47.211)
21 (1)
50.001 (5
(50.001)
0.324
717.697
27.515 (45.211)
Drop s2
0.43
0.33
0.24
0.00
0.53
0.03
0.17
0.27
[0]
101.556 (79.252)
21 (1)
50.001 (5
(50.001)
59.556 (77.252)
Drop a2
0.20
0.23
0.55
0.02
[0]
0.34
0.31
0.32
0.03
505.181 (482.877)
21 (1)
50.001 (5
(50.001)
463.181 (480.877)
Drop a32
0.32
0.43
0.23
0.02
0.663
0.04
[0]
0.27
0.03
24.267 (1.944)
21 (1)
ADHD mediating
0.37
0.38
0.23
0.02
^
0.58
0.42
[0]
97.121
22
^
0.281
(0.163)
50.001
717.753 (7
(70.056)
53.121
a1, influence of the common genetic component on ADHD; a2, influence of the common genetic component on antisocial behaviour; a3, influence of the genetic component specific to antisocial behaviour on the variance of antisocial behaviour; d1,
influence of the non-additive genetic component on ADHD; e1, influence of the non-shared environmental component common to both phenotypes on ADHD; e2, influence of the non-shared environmental component common to both phenotypes on antisocial behaviour; e3, influence of the non-shared environmental component specific to antisocial behaviour on the variance of antisocial behaviour; s1, contribution of maternal smoking to the variance of ADHD; s2, contribution of
maternal smoking to the variance of antisocial behaviour; AIC, Akaike’s information criterion; [0], variable fixed at zero.
1. Differences between the nested models and the full saturated model.
2. Best-fitting model.
3. Genetic correlation in the best-fitting model¼1.0,
model 1.0, environment correlation¼0.34.
correlation 0.34.
B U T TON E T A L
15 8
Table 1 Univariate ADE models for attention-deficit hyperactivity disorder (ADHD) and antisocial behaviour
P R E N ATA L S M OK IIN
N G , A N T I S O C I A L B E H AV I OU R A ND
ND A D
DH
HD
two childhood phenotypes. However, the
‘causal’ model did not fit the data at all
whereas the Cholesky model did, suggesting that smoking in pregnancy has a specific influence on each, accounting for some
of the covariance between them, rather
than resulting from this covariance. These
findings suggest that the association of
smoking in pregnancy with antisocial behaviour is not attributable to its association
with ADHD.
CLINICAL IMPLICATIONS
& Maternal prenatal smoking is associated with both antisocial behaviour and
attention-deficit hyperactivity disorder (ADHD) in offspring.
The association of smoking in pregnancy with antisocial behaviour in offspring
appears to operate independently; it does not appear to be mediated through the
covariation with ADHD.
&
We cannot conclude with confidence that smoking during pregnancy is not a direct
risk factor for both ADHD symptoms and conduct disorder in offspring.Therefore,
the safest clinical message is that smoking in pregnancy should be avoided.
&
Limitations
There are a number of limitations to this
study. First, the age range of the twins
was large and the sample contained male,
female and opposite-gender twins. A larger
twin data-set might allow more thorough
investigation of the relationships, controlling for differences in both age and gender.
However, according to this study and
previous research, these differences may
not be so important. Second, all measures
used in this study were rated by a single
individual, with mothers accounting for a
large proportion of the raters. Consequently shared rater effects may account
for some of the covariance between phenotypes. This is an especially important factor
given that maternal prenatal smoking may
index antisocial behaviour in the mother
(Silberg et al,
al, 2003), which may be
associated with reporter bias. Using different raters’ accounts of the child’s behaviour, such as the child him- or herself,
may help to overcome this problem.
Finally, the data-set is cross-sectional; the
mother’s report of her smoking during
pregnancy is retrospective and a memory
of both smoking and the amount smoked
between 5 and 18 years previously was required. Consequently memory recall may
have an effect on the outcomes of the study.
Another limitation of this study is that
it fails to account for the fact that maternal
prenatal smoking may be an index of other
latent risk variables transmitted from the
mother to the children. For example, it
has been suggested that maternal prenatal
smoking may index a broader antisocial
phenotype in the mother (Silberg et al,
al,
2003). Consequently, antisocial behaviour
of the offspring may partly or entirely result
from genetic transmission of the propensity
to antisocial behaviour from the mother to
child (Fergusson et al,
al, 1998; Brennan et al,
al,
1999). Although it was not possible to test
this hypothesis in the present study, lack
of a significant contribution of shared
LIMITATIONS
& The data-set is cross-sectional, covers a large age range and both males and
females.
The measures used in this study were all parent-rated, and the majority of raters
were the mothers; consequently if smoking behaviour is, as has been suggested, an
index of maternal antisocial behaviour, there may be some bias from shared rater
effects in the maternal responses.
&
The report of maternal smoking in pregnancy is retrospective. Problems with such
long-term memory recall may influence the results.
&
T. M. M. BUTTON, PhD, Social,Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Denmark
Hill, London SE5 8AF; A. THAPAR, MRCPsych, Section of Child and Adolescent Psychiatry, Department of
Psychological Medicine, University of Wales College of Medicine, Cardiff; P. McGUFFIN, FRCPsych, Social,
Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Denmark Hill, London
Correspondence: DrT.M.M.Button,Institute for Behavioral Genetics, 447
4 47 UCB,Boulder,CO8
UCB,Boulder,CO80309-4
0309-447,
47,
USA. E-mail: tanya.button@
tanya.button @colorado.edu
(First received 15 June 2004, final revision 5 November 2004, accepted 16 November 2004)
environmental influences along with a
significant influence of maternal prenatal
smoking suggests an underlying genetic
rather than environmental mediation,
consistent with other studies (Maughan
et al,
al, 2004). Finally, maternal prenatal
smoking may be indicative of other
environmental risk factors for antisocial
behaviour, such as poor family relationships (van den Bree et al,
al, 2004) and low
socio-economic status (Wakschlag et al,
al,
2002). Longitudinal studies and children
of twins studies may be more useful in
differentiating these causal relationships.
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