J . ChildPs~chnl.P>vr.hwr. Vol. 42, No 8. pp. 10?1-10?8.

2001
Cambrldge Unwersty Press
C 2001 Association for Chdd Psychology and Psychlatry
Prlnted In Greet Brltain All rights reserved
o n 2 1 - 9 m / o 1$1s.oo+o.nn

Pregnancy Smoking and Childhood Conduct Problems :

A Causal Association?
Barbara Maughan, Colin Taylor, and Alan Taylor
Institute of Psychiatry, London, U.K.

Neville Butler John Bynnerl

International Centre for Child Studies, Bristol, U.K. Institute of Education, London, U.K.

Recent investigations have highlighted associations between maternal smoking in pregnancy

and antisocial behaviour in offspring, and suggested
the possibility of a causal effect. We used
data from the 1970 British birth cohort study (BCS70) to examine these links in a large,
population-based sample studied prospectively from birth to age 16. We found a strong
dose-response relationship between the extent of pregnancy smoking and childhood-onset
conductproblems, but no links with adolescent-onsetantisocial behaviours. Effects on
childhood-onset conduct problems were as marked for girls as for boys, and were robust to
controls for a variety of social backgroundfactors and maternal characteristics. Controls for
mothers subsequent smoking history modified this picture, however, suggesting that the
prime risks for early-onset conduct problems maybe associated with persistent maternal
smoking-or correlates of persistent smoking-rather than with pregnancy smoking per se.

Keywords: Conduct disorder, delinquency, longitudinal studies, prenatal smoking.

Abbreviations: BCS70: 1970 British birth cohort study.

Introduction of plausible confounds, including aspectsof social back-

ground, styles of parenting, and paternal psychopath-
Maternal smoking in pregnancy is a well-established ology; (3) that controlled forbackgroundconfounds,
risk for adverse pregnancy outcomes and reduced infant risks are specific to disruptive, antisocial behaviours; and
birthweight(Royal College of Physicians,1992); in (4) that effects may be specific to boys. Although the
addition, follow-up studiessuggest some small continuing mechanisms involved are unknown, theoverall pattern of
effects on childrens physical development, and possibly the findings hasled to speculation that these associations
on their cognitive skills, inthe first few years of life may reflect causal influences of prenatalsmokingon
(Lassen & Oei, 1998). More recently, reports have also foetal brain development in ways that affect vulnerability
highlighted
links between prenatal
smoking and to antisocial behaviour.
childrens behavioural development. A series of studies, Existing studies have used a variety of measures of
in both clinical and epidemiological samples, have docu- child behaviouraloutcomes,taken at different ages.
mentedassociations between prenatalsmokingand Currentliterature suggests, however, that disruptive
increased risks of disruptive behaviour problems, conduct behaviour problems are almost certainly heterogeneous,
disorder,delinquency, andadult crimein offspring and that one key marker for that heterogeneity is age at
(Fergusson,Horwood, & Lynskey, 1993; Fergusson, onset (see, e.g.,Moffitt, 1993). Persistentantisocial
Woodward, & Horwood, 1998; Orlebeke, Knol, & behaviours that begin early in childhood are associated
Verhulst,
1997;
Rantakallio, Laara,
Isohanni, & with a range of individualandenvironmental risks
Moilanen,1992;Wakschlagetal.,1997;Weissman, (including adverse temperamental features, compromised
Warner, Wickramaratne, & Kandell, 1999; Williams et neuropsychological functioning, hyperactivity, and poor
al., 1998). Taken together, these studies suggest (1) a social and familycircumstances), and oftencarry an
dose-response relationship between the extentof prenatal extremely poor long-term prognosis. Delinquency that
smoking and risk for antisocial behaviour in offspring; begins in adolescence,by contrast, shows fewer links with
(2) that the associationis robust to controls for a variety individual or social adversities, and is markedly less
ominous for later development. Although associations
between prenatalsmokingand disruptivebehaviours
have been examined in children of different ages, few
Requests for reprints to: Barbara Maughan, Department of studieshave as yet explicitly testedforvariations ac-
Child & Adolescent Psychiatry, Institute of Psychiatry, 16 De
Crespigny Park, London SE5 SAF, U.K. cording to age at onset, though some suggestive findings
Barbara Maughan andAlan Taylor are attached to the MRC haveemerged. In a small high-risk sample,maternal
Social, Genetic & Developmental Psychiatry Research Centre smoking was found to be associated with prepubertal but
at the Institute of Psychiatry. John Bynner is affiliated to the not with later-onset conduct disorder in boys (Weissman
Centre for Longitudinal Studies. et al., 1999), and results from twolarge-scale population-

1021
1022 al. et B. MAUGHAN
based studies of criminality in adult males suggest that
prenatal smoking maybe especially associated with more
severe, persistent offending. In a large Danish cohort,
prenatalsmoking was morestrongly associatedwith
persistent than with adolescence-limited criminality
(Brennan,Grekin, & Mednick, 1999). InaFinnish
cohort, maternal smoking in pregnancy was associated
withviolentoffending upto age 28, butnot with
nonviolent crimes (Rasanen et al., 1999).
Our first aim in the present study was to explore this
issue further, testing associations between prenatal smok-
ing and age at onset of behaviour problems in a large-
scale childhood sample. We hypothesized that if preg-
nancy smoking is indeed directly implicated in risk for
serious or persistent conduct problems, this should be
moreevidentinchildhoodthaninadolescent-onset
difficulties. The 1970 British birth cohort study (BCS70,
Butler & Golding, 1986) offered the opportunity to test
this out. BCS70 has tracked a national sample of children
from birth; mothers were questioned about smoking in
pregnancy shortly
after
the
childs
birth,
and the
childrens behaviour was subsequently assessed in both
childhood and adolescence. The sample is large enough
to test the postulatedspecificity of effects to boys, and the
data-set includesmeasures of other childoutcomes
known tobe associated with prenatal smoking; indicators
of hyperactivity and depressive symptoms (allowing for
tests of the specificity of any associations to antisocial
behaviours); and measures of a wide range of potential
environmentalconfounds.Ina recent review of the
consequences of prenatalexposure to nicotine, Ernst,
Moolchan, and Robinson (2001) stressed the likelihood
of both environmental andgenetic confounds of prenatal
smoking, and the difficulties these raise in interpreting
much current evidence from human studies. Oursecond
aimwas toexaminethe effects of theenvironmental
confounds assessedinBCS70in moredetail.Inpar-
ticular, we set out to assess how far any associations
between prenatalsmokingand childrensbehaviour
problems were robust to theextensiverangeofsocial
backgroundmeasuresrecorded inBCS70, andinde-
pendent of reports of later maternal smoking, after the
childs birth. If prenatal smoking retained associations
with behaviour problems after controls for these various
confounds, the presumption of a direct causal influence
on developmentalprocesses associated with vulnerability
to antisocial behaviour would clearly be strengthened.
Methods
Samples
BCS70 is a prospective studyof all children born in England,
Scotland, and Wales in the first week of April 1970 (Butler &
Golding, 1986). Survivors a t l month ( N = 16,151) were
followed up atages 5, 10, and 16 years. Response rates (one or
more follow-up questionnaires completed)were 8 1 % at age 5,
92% at age 10, and 71 YOat age 16. In addition to the usual
factors affecting attrition inlarge-scale longitudinal surveys, the
lower response rateat age16 was influencedby industrial action
by teachers, which affected tracing via schools.
Measures
Data were collected from medical examinations and parental
interviews, and from cognitive tests and questionnaires com-
pleted by the study children. The following measures were used
in the analyses:
(1) Gestational age, birthweight, and maternal age: recorded
at the birth sweep.
(2) Maternal smoking: a number of questions on cigarette
smoking were included at the birth sweep. These were
combined to produce a five-category indicator of the
extent of any smokingin pregnancy: (a)never smoked;
(b) smoked previously, but stopped smoking in preg-
nancy; (c) smoked 1 4 cigarettes a dayin pregnancy; (d)
smoked 5-14 cigarettes a day in pregnancy:(e) smoked
15 or morecigarettes a dayin pregnancy. Self-reports of
subsequent maternal smoking were also available from
the 5, 10, and 16 year contacts.
(3) Maternal drinking in pregnancy: reports were collected
retrospectively, attheage 10 sweep. Motherswho
reported drinking on two or more days per week were
contrasted with all others.
(4) Social andfamily background: extensive data on family
and social background werecollected throughinter-
views with parentsat each study contact. Measures used
in the present analyses include: (a) parental education
(no academic or vocational qualifications vs. any); (b)a
composite social adversity index combining measures of
family social class, housing tenure, overcrowding, and
availability of carsand telephones: families in the lowest
quintile of the range on this index were contrasted with
all others; (c) family structure (two biological parents
vs. all other types) at each study contact: (d) instability
in family structure (i.e., changes in parentfigures) across
three age-ranges: (i) birth-age 5 ; (ii) age 5-age 10; (iii)
age 10-age 16; (e) ordinal position of the study child
(middle child vs. all other positions) at age 10; and (f)
major family disruption, resultinginthe study child
being placed in Local Authority care before age 16.
(5) Maternal depressed mood: mothers completed the Mal-
aise Inventory(Rutteret al., 1970), a24-item self-
completionmeasure of affective symptomatology, at
eachchildhoodstudy sweep. TheMalaiseInventory
shows good psychometric properties, and high scores
(of 6 or more) have been shown to provide an index of
risk for case-level depression (Rodgers,Power,
Collishaw,Pickles, & Maughan, 1999). Binaryindi-
cators of high/low scores at this cut-pointwere used in
the analyses.
( 6 ) Abilityandattainnzents: thechildrencompletedthe
EnglishPictureVocabularyTest (EPVT; Brimer &
Dunn, 1962) at age 5, and a shortened version of the
Edinburgh Reading Testdevised specially for the study
(GodfreyThomsonUnitforEducationalResearch,
1977) at age 10.
(7) Conduct problems and hyperactivity at uges 5 and 10
years: parentscompleted the Rutter A2 behaviour rating
scales (Rutter, Tizard,& Whitmore, 1970) at each of the
S and 10 yearcontacts.0-2ratings (no problem,
somewhat, and definite) are made on3 1 items reflecting
emotional and behavioural difficulties. The scales have
been widely used in studies of childrensemotional and
behaviouralproblems,andshowgoodpsychometric
properties(Elander & Rutter, 1996). Factoranalyses
identified two main factors of interest for the present
study:conductproblems(loading on lying,stealing,
bullying,fighting,destructiveness, and disobedience)
and hyperactivity (loading on restlessness, fidgetiness,
and lack of concentration). Scores on these items were
summed to create subscales, and subscale scores at or
above the 90th percentile were used to identify children
with high levels of problems at ages S and 10 years.
(8) Conduct problems at age 16 years: parents also com-
pleted modified Rutter A(2) scales at the age 16 sweep.
Inaddition,theadolescent self-completionquestion-
nairesincludedavarietyofindicatorsofconduct
problems.Itemsfromboth ofthesesourceswere
combined usinga n O Rrule (i.e., the item was treatedas
present if reported eitherby parent or adolescent) to rate
the presence of seven conduct problems (stealing with-
 PREGNANCY
SMOKING
CHILD
CONDUCT
ANDPROBLEMS 1023

outconfrontation, fighting,breaking intoproperty, outcomesknownfrompreviousstudiestoshowlinks

destroying others property, stealing with confrontation, with maternalsmokingalsovariedinexpected ways
lying, and bullying). Scores of 2 or higher on this scale (Table 2): babies born to motherswhosmoked in
were takento reflect adolescentconductproblems/ pregnancy were of lower birthweight than those of non-
delinquency;12.0%oftheadolescents(16.0%boys
and 7.8 % girls) scored above this cut-point.
smokers, had significantly lower standardized vocabulary
Age at onset and persistence of conduct problems: the scores at age 5, lower standardized reading scoresat age
measures of childhood and adolescent conduct problems10, and were themselves more likely to report that they
were combined to classify children into three mutually smoked at age 16. Controllingforthe possible con-
exclusive age at onset groupings in relation to conduct founding effects of the childs sex and gestationalage, and
problems: (a) no marked conduct problems at any age for maternal age, maternal education, social disadvan-
(Le,, scores below the selected cut-points at ages S, 10, tage, and maternal drinking in pregnancy, smoking in
and 16 years);(b)childhood-onsetproblems(high pregnancy remained significantly associated with eachof
scores at either S or 10 years); and (c) adolescent-onset these outcomes. As Table 2 shows, links with parent-
problems (high scoresat age 16 in the absence of earlier rated hyperactivity and with adolescent depressed mood
difficulties). Children who had high scores at ages 5 or 10
years and also inadolescence were classified as showing
were less clear.Prenatalsmokingwasunrelatedto
persistent conduct problems. hyperactivity ingirls; in boys, although tests of the
Depressed mood at age 16: adolescents also completed overall association fell short of conventional significance
the Malaise Inventory (Rodgers et al., 1999; Rutter et levels, sons of motherswhosmokedmost heavily in
al., 1970) at the age16 sweep. Items reflecting depressive pregnancy were more likely thansons of complete
symptomatology were combined(againusing an OR nonsmokersto be ratedas showing high levels of
rule)withrelateditems from the parent Rutter A(2) hyperactive behaviours at both 5 and 10 years. Rates of
scales, to rate the presence of a number of depressive adolescentdepressed mood were alsoelevated among
symptoms. We focus hereon the indicator of depressed girls whose mothers had smoked most heavily in preg-
mood/misery which, as expected, was reported more nancy; again, however, tests of across the full range of
commonly in girls (15.6 YO)than boys (7.5 YO).
maternal prenatal smoking fell short of significance.

Statistical Methods Smoking in Pregnancy and Childhood Conduct

Completedataon keyvariablesfortheanalyses were Problems
available on 5770 cases (2969 boys and 2801 girls).Weights Againstthisbackground, we went onto examine
derived from predictorsof responseat each wave were included associations with conductproblems in childhoodand
in all analyses to reduce the effects of any bias associated with
adolescence. As expected, conduct problems were more
sample attrition andmissing data. A range of social and family
common among boys than girls at each study contact:
background factors (includingfamily social adversity, region of
24.1 Y O of boys and 13.0 YOof girls were rated as showing
birth, and parental education)emerged as significant predictors
of response; in addition, both maternal smoking in pregnancy high levels of childhood-onsetconduct problems
and child conductproblemsatage (reported for the first time at 5 or 10 years). The great
10 yearscontributedto
responseprediction,and so wereincludedin majority of these difficulties had remitted by age 16: only
the weighting
system. Preliminary analyses confirmed that weighted distri- 5.5% of boys and2.2% of girls showedpersistent
butions on key variables closely paralleled the composition of
conductproblemsspanningbothchildhoodandado-
the sample at thebirth sweep. The analyseswere undertaken in lescence. In addition, a further 10.5 YOof boys and 5.6%
STATA (StataCorp, 1999), with robust variance estimates to of girls showed adolescent-onset antisocial behaviours,
give correct inferences for weighted models. Linear regression
with problems reported for the first time at age 16.
modelswereusedforcontinuousvariablesand logistic re-
gression models for binary outcomes. Overall model Figures 1 and show
results are 2 rates of childhood and
adolescent-onset conduct problems for boys and girls in
reported in terms of F-ratios for continuous variables and Wald
each of the pregnancy smoking categories.As they show,
xs for logistic regression models. Specific contrasts between
there was a strong dose-response relationship
categories tested in logistic regression models are reported in between
terms of odds ratios (OR) and 95 YOconfidence intervals. levels of maternal smoking in pregnancy and rates of
childhood-onset conduct problems in both girls and boys;
rates of adolescent-onset problems, however, were un-
Results related to prenatal smoking in eithersex. Compared with
Rates and Correlates of Maternal Smoking in nonsmokers, the
odds
of
childhood-onset
conduct
Pregnancy problems among children whose mothers smoked 5-14
cigarettes per day in pregnancy were 1.47 (95 YOC1 =
Justover 40% of mothersreportedsome level of 1.16-1.86) for boys, and 2.17 ( 9 5 % C1 = 1.59-2.97) for
smoking in pregnancy : 7.0 YOsmoked l 4 cigarettes per girls. In the heaviest pregnancy smoking category (15 or
day, 21.4% smoked 5-14 cigarettes per day, and 13.2 YO more cigarettes per day), odds ratios were 2.07 (95 YOC1
smoked 15 cigarettes per day or more. The majority of the = 1.56-2.76) for boys and 3.04 (95 YOC1 = 2.134.35) for
remainder were complete nonsmokers, but a small group girls.
(4.7%) reported that they had smoked previously, but Childhood-onset conduct problems were also signifi-
had given up while they were pregnant. As Table 1 shows, cantly associated with a wide spectrum of other factors:
smoking in pregnancy was stronglyassociatedwitha male sex, family social disadvantage,youngmaternal
variety of othermaternal characteristics and social age, family instability, the child having been received in
background indicators : poor maternal education, early Local Authority care, maternal depressive symptoms, the
childbearing, drinking in pregnancy, subsequent family childs ordinal position in the family, childhood hyper-
instability and social disadvantage, maternal depressive activity, andpoorer vocabulary andreading skills. A
affect, andsubsequentmaternalsmoking allshowed logistic regression model including all these significant
strong links with prenatal smoking. In addition, child predictorscontinued toshowan effect ofprenatal
1024 et B. MAUGHAN al.

Table 1
Correlates of' Maternal Cigarette Smoking in Pregnancy
Number of cigarettes smoked per day in pregnancy

None 1 4 5-1 4 > 15

Never Gave up in
smoked pregnancy
( N = 3099)' ( N = 270) ( N = 402) ( N = 1237) ( N = 762) ,f (4) p
YOMothers no educational qualifications 26.7 28.5 29.5 40.0* 46.0* 115.1 < .001
% Mothers teenager at first/index birth 19.9 32.2* 24.8* 30.1* 34.0* 75.8 < ,001
Yo Mothers lone parent at index birth 2.9 6.9* 5.6* 6.1* 6.4* 19.8 < ,001
'/O Mothers drank 2-7 days per week 3.3 5.2 6.5* 7.0* 8.4* 35.5 < ,001
in pregnancy
YOFamilies socially disadvantaged 18.9 21.8 29.6* 33.6* 44.7* 186.0 < ,001
YOFamily instability birth-age 16 17.7 29.S* 26.7* 26.2* 3 1.9* 75.9 < ,001
9'0 High maternal depression score
Age 5 sweep 7.3 9.6 10.5* 11.6* 15.3* 38.1 < ,001
Age 10 sweep 7.2 8.0 8.1 10.8* 17.S* 52.2 < ,001
Age 16 sweep 8.5 8.5 9.7 10.2 16.6* 29.6 < ,001
%O Maternal smoking
Age 5 sweep 9.0 47.8* 66.3* 85.4* 91.1* 1902.4 < ,001
Age 10 sweep 9.8 51.2* 64.2* 79.4* 89.3* 1763.7 < ,001
Age 16 sweev 8.9 37.7* 47.9* 72.8* 83.2* 1437.7 < ,001
*Weighted Ns, rounded to nearest whole number.
* Significantly different from never smoked at p < .05.

Table 2
Maternal Smoking in Pregnancy and Selected Child Outcomes
Numbers of cigarettes smoked per day in pregnancy

None 1 4 5-1 4 > 15

Never Gave up in
smoked pregnancy
( N = 3099) ( N = 270) ( N = 402) ( N = 1237) ( N = 762) X' (4) p
Mean birthweight (grammes) 3344 3283 3279* 3 149* 3102* 40.9" < ,001
YOHyperactive age S
Girls 6.8 8.2 7.7 6.9 8.4 1.2 n.s.
Boys 9.4 11.2 10.2 8.6 15.0* 8.9 .06
Yo Hyperactive age 10
Girls 7.1 9.5 8.8 7.3 8.6 1.6 n.s.
Boys 12.0 15.0 12.7 12.8 16.6" 4.3 n.s.
Mean standardized EPVT score age S 0.17 0.09 0.10 - 0.05* -0.12* 15.8" < ,001
Mean standardized Edinburgh 103.5 101.4* 102.5 99.3* 97.2" 28.3" < ,001
reading score age 10
O/O Smoking age 16 11.8 18.6* 21.8* 23.1* 28.9* 72.7 < ,001
YODepressed mood age 16
Girls 13.7 17.2 16.0 17.5 20.0* 8.8 ,084
Boys 7.1 6.6 4.1 8.1 10.4 5.5 n.s.
~~

B F test with 4, 5670 &(birthweight); 4, S424 df'(EPVT); 4, 5070 @(Edinburgh reading test).
* Significantly different from never smoked at p < .OS.

smoking on risk for childhood-onset conduct problems.
Compared withmotherswhohad never smoked,the
adjustedoddsofchildhood-onsetconductproblems
among children whose mothers smoked 5-14 cigarettes a
day in pregnancy was 1.48 (95 YOC1 = 1.18-1.85, p =
.OOl). For children of the heaviest smoking mothers (15
or more cigarettes per day) the adjusted odds ratio was
1.53 (95 Yo C1 = 1.17-2.00, JJ .002).1
Heavy smoking in pregnancy was also associated with
persistence of conductproblemsfromchildhood to
adolescence. Thirtypercent of boyswithchildhood-
onsetproblemswhosemotherssmoked 15 or more
cigarettes perday in pregnancy showed persistentconduct
problems at age 16 bycomparison with 21.5 YOof sons of
nonsmokers. Contrasts for girls were if anything more
striking: 29.2 % persistence amongdaughters of the
heaviest smokers,13.2 YO amongdaughters of non-
smokers. Other predictors of persistence were male sex,
young maternal age, and family instability between ages
10 and 16 years;for girls only, persistence was also
associated with family change in middle childhood (ages
5-10 years). Once again, prenatal smoking continued to
show significant associationswithpersistentconduct
problems in alogistic regression model takingthese other
factors into account. Compared with mothers who had
never smoked, the adjusted odds of persisting conduct
 PREGNANCY SMOKING A N D CHILD CONDUCT PROBLEMS I025

Nonsmoker Gave up in pregnancy l+

per day 5* per day p
e
l$+r day
Maternal smokfng in pregnancy

Childhood (ages 5 10 years) Adolescent (age 16 years) Figwe 3. Childhood-onset conduct problems, maternal
Age at onset of conduct probfems
smoking in pregnancy, and subsequent maternal smoking.
..__.
.............................................................................................................
;4 0Nonsmoker Stopped in pregnancy l + per day i year study contacts-the period over which childhood-
onset conduct problems had been assessed. Controlling
i 5+ per day 15+ per day
for all other significant predictors, this index, treatedas a
scale, was significantly associated with increased risk for
Figure 1. Conduct problems and maternal smoking in childhood conduct problems (adjustedOR = l . 17, 95 %
pregnancy: boys.
C1 = 1.04-1.32,~ = -011 ) ; with this indicator included in
themodel, effects of smoking in pregnancy became
nonsignificant ( p = ,238). Exploring contrasts between
25 l categories of the postnatal smoking index, it was clear
that these effects were primarily associated with persistent
smoking. Risks for children of mothers who smoked at
only one of the 5 or 10 year sweeps werenot significantly
elevated by contrast with those who reported ne postnatal
smoking (adjusted OR = 1.20, 9 5 % C1 = 0.88-1.62);
for children of persistent smokers, however, risks were
significantly increased (adjusted OR = 1.37, 95% C1 =
1.07-1.74).
Thesefindingssuggestedthatmotherssubsequent
smoking was associatedwith some additional effects,
over and above those apparentfor smoking in pregnancy.
Childhood (ages 5-10 years) Adolescent (age 16 years)
To explore this further, we plotted rates of childhood-
onsetconductproblems for children in each of the
Age at onset of conduct problems pregnancy smoking categories, subdivided according to
the mothers reports of subsequent smoking. Figure 3
i Nonsmoker Stopped in pregnancy I+ per day I illustrates the results, contrasting rates for children of
mothers who reportedsmoking at boththe 5 and 10
i 5+ per day 15+ per day contacts(persistentsmokers) with those forchildren
...................................................................................................................... whose mothersreportedsmoking at neitherpostnatal
Figure 2. Conduct problems and maternal smoking in contact, oratonly one. Two featuresare especially
pregnancy: girls. striking. First, children whose mothers had not smoked
in pregnancy but who did report smoking at both later
study contactsseemed at someincreased risk ofchildhood
problemsamongchildren of mothers in theheaviest conduct problems; tests confirmed that this was indeed
pregnancysmokingcategory was 1.69 (95 YO C1 = the case (OR = 1.43, 95 Yo C1 = 0.95-2.14, p = 48).
1.08-2.63, p = .021). Second, at the opposite endof the spectrum,effects were
more marked, and significantly higher ( p = .03 on a one-
S~bseguenrMaternal Smoking tailed test).Outcomes for childrenofmothers who
smoked most heavily in pregnancy (15or more cigarettes
Theseanalysessuggestedthatassociationsbetween per day) variedmarkedlydepending on themothers
prenatal smoking and both early onset and persistent subsequentsmokinghistory. Where motherssmoked
childhood conduct problems could notbe accounted for persistently, rates of childhood conduct problems were
by the strong overlaps between maternal smoking and a the highest in the sample as a whole (31.5 %); if women
range of social, family, and maternal characteristics. The who smoked heavily in pregnancy subsequently gave up
final stage in the analyses was designedto explore how far smoking for a t least some period, problem levels were
these effects were specific toprenaralsmoking. To do this, little elevated above those of the children of nonsmokers
we repeated the logistic regressionanalysespredicting (14.2 % vs. 14.3 % among complete nonsmokers). Given
childhood-onset conduct probIems, but included as an the strong continuity in maternal smoking across study
additional predictor a 3-point cumulative indexof post- contacts (see Table l), the numbersin this last group were
natal smoking, reflecting on how many occasions (none, inevitably relatively small: only 15.2% of mothers who
one, or two) mothers reported smoking at the 5 and 10 smoked heavily in pregnancy (100/657) did not report
1026 B. MAUGHAN et a1

persistentsmokingaftertheirchildwas born.None- and in some senses tookthemfurther. Like other

theless, testsconfirmed that differences between these investigators, we found a clear dose-response relationship
groups inrisk forchildhoodconductproblems were between the extent of prenatal smoking and childrens
statisticallyreliable (OR = 2.79, C1 = 1.54-5.05, p = conduct problems, but little to suggest consistent links
.OOl). In addition,these variationswere robust to controls with either parent-rated hyperactivity in childhood, or
for other predictors of childhood-onset conduct problemswith depressed affect in adolescence. Our findings were
within the group of heavy prenatal smokers. Male sex, novelinshowing thatthe associations with conduct
hyperactivity, middle child ordinal position, social dis- problems were as marked for girls as for boys; that they
advantage, and the child having been received into care were specific to early-onset disruptive behaviours; and
were all significantly associatedwithrisk for conduct that prenatal smoking was also a significant predictor of
problems within the heaviest prenatal smokers. Taking the persistence of early childhood behaviour problems
these additional factors into account, continued maternal into the teenage years. Although maternal smoking was
smoking after the childs birth continued to predict risk associated with a wide spectrum of maternal and social
for childhood conduct problems (adjusted OR = 2.12, risks, and with other adverse outcomes for children, links
95 Yo C1 = 1.194.02, p = .021). with conduct problems remained when the effects of all
Thissuggested that persistentsmoking, both before these other factors were controlled.
and after childs birth, was of particular importance.To In epidemiologicalterms,a specific dose-response
clarify the influences involved here, we examined other relationship of this kind, robust to controls for a number
correlates of persistent smoking vs. partial or complete of plausibleconfounds,would generally be takento
quitting up to age 10 within the group of women who suggest at least the possibility of a causal role for the risk
reported smoking mostheavily in pregnancy (1 5 or more factor involved. In this instance, however, controls for
cigarettes per day). Mothers who were persistent post- onefurther set of confounds-mothers subsequent
natal smokers did not differ systematically from other smoking histories4ast some doubtonthis view. If
heavy pregnancy smokers in rates of drinking in preg- previously nonsmoking mothers took up smoking after
nancy, lone parent status at the study childs birth, family their childs birth,their childrens risk for early-onset
changeoversubsequentstudy sweeps, or risks of the conduct problems was somewhat increased. If mothers
study child having been admittedtocare.Group who had smoked heavily in pregnancy gave up smoking
differences were apparent, however,intermsofthe for at least some time, their childrens risk of conduct
mothers age at the birth of her first child, educational problems was little elevated above that of nonsmokers.
qualifications, rates of family social disadvantage, and Despite the relatively small numbers in this last group,
maternal Malaise scores. In each case, mothers whowere thesecomparisons seemed statistically reliable, and
persistent smokers were more disadvantaged than those remained apparent when otherpredictors of conduct
who smoked heavily in pregnancy, but who subsequently problems within this subgroup of children had been taken
quitforat leastsomeperiod. In termsofageat into account.
motherhood, 36.0 % of persistent smokers had their first Before discussing possible implications of these
child in their teens,by contrast with 22.9 % of those who findings we should underline both the strengths and the
subsequently quit(OR = 1.SS, 95 YOC1 = 1.09-3.29, p = limitations of ourstudy. BCS70 hadanumber of
.024). In terms of educational qualifications, 48.8% of important advantages for a study of this kind: it has
persistentsmokers by contrast with 30.7% of later tracked the development of a nationally representative
quitters had no educational or vocational qualifications sample of children (large enough to provide statistical
(OR = 2.14, C1 = 1.32-3.49, p = .002). On the social power for quite complex multivariate analyses) over an
disadvantageindex,47.7%of persistentsmokers vs. extended developmental period, and included measures
27.8 YOof later quitters fell into the most disadvantaged of a wide range of individual and family factors relevant
quintile (OR = 2.37, C1 = 1.43-3.94,~ = .OOl). In terms to ourhypotheses. The measures of maternal smoking in
of Malaisescores,persistentsmokersshowedelevated pregnancy were quantifiedinenoughdetail to allow
rates of depressed mood at bothchildhood study sweeps assessments
dose-response
of relationships with
by contrast withwomen whosubsequently gave up childrens outcomes, and associations between prenatal
smoking: age 5: 17.2 % vs. 4.9 % (OR = 4.00, C1 = smokingandboth birthweight andother aspects of
1.65-9.74, p = .002);age 10: 19.3% vs. 7.3% (OR = childrensdevelopmentreplicated effects reportedin
3.02, C1 = 1.33-6.85,~= .008). numerous previous investigations.
Set against these advantages, three main limitations
Discussion must be borne in mind in interpreting the findings. First,
likeall large-scale longitudinalstudies, BCS70 faced
A number of recentinvestigationshavehighlighted problems of sampleattritionand missing data.Our
links between maternal smoking in pregnancy and risk requirements for measures from all four main childhood
forantisocialbehaviour in offspring; the specificity, data collection waves, and froma varietyof different data
replicability, and apparent robustnessof these effects lead sources within waves, were especially demanding here.
to speculations thata causal influence might be involved. Our preliminary analyses identified a range of predictors
We set out toclarify this picturefurther, testing effects of of nonresponse; amongst a range of other factors, these
prenatal smoking in a large-scale, representative sample included both smoking in pregnancy and conduct
of children studied prospectively from birth. We were problems at age 10 years. We developed weights to take
especially interested in assessing how far any effects that account of these effects so far aspossible, but we recognise
emerged would be specific-as might be hypothesized- that our estimates may still be affected by some element of
toearly-onsetconductproblems,andhowfar, ina bias. Because key variables in our substantive analyses
samplewithgoodpower to test for sex differences, were alsoimportant predictors of response, we were
associations would be specific to males. especially sensitive to the implications of this problem.
Our initial findings confirmed those of previous studies, We thus repeated all of the key analyses unweighted, to
 PREGNANCY
SMOKING
CHILD
CONDUCT
ANDPROBLEMS
check howfarthefindings were affected. All key
conclusionsrelated to pregnancysmokingremained
essentially unchanged.
A second potential limitation lay in the fact that our
measures of maternal smoking in pregnancy were based
on self-reports, and did not include indicatorsof the stage
inpregnancy at whichthemotherssmoked.We were
fortunate that these reports were collected shortly after
thestudy childs birth, minimising the risk ofrecall/
retrospective reporting bias. Nonetheless, studies com-
paring self-reports of smoking with serum cotininelevels
have foundless than perfect agreement. Oneinvestigation
of pregnancy smoking, for example, found that pregnant
women reportedreasonablyaccuratelywhetherthey
smoked or not (kappa = .83), but that the correlation
between self-reports of number of cigarettes smoked and
cotinineconcentration was quitemodest (Y = .44)
(Klebanoff, Levine, Clemens, DerSimonian, & Wilkins,
1998). In that study, infant birthweight correlated more
strongly with measured cotinine concentrations than with
self-reports. We have no way of assessing how any error
in self-reports may have affected the associations reported
here; it would undoubtedly be desirable to replicate our
findings in data-sets with more direct measures of the
tobacco dose received.
Finally, our measures of childhood conduct problems
were based on parentratings ratherthandiagnostic
assessments of disorder or official reports of delinquency.
The cutoffs we used to define the presence of conduct
problems were inevitably arbitrary, and our definitions of
childhood-onset difficulties were quite broad. Rates of
persistent conduct problems (5.5 ?4 in boys and 2.2 % in
girls) were, however, much closer to the ratesof clinically
significant disorder reported in epidemiological studies
(Angold, Erkanli, & Costello, 2001). As we have seen,
associationswith heavy prenatalsmoking applied as
much to these more stringent indicators as to the wider
problem categories. Once again, however, it would clearly
be desirable to replicate our results in groups defined in
diagnostic terms.
Given these caveats, our finding that later maternal
smoking moderated associationsbetween prenatal smok-
ing and risk for childhood conduct problems must cast
some doubt on the likelihood of any directly causal role
for prenatal smokingin thegenesis of childhood conduct
problems. In this sample, the highest risks for childhood-
onset conduct problemswere for children whose mothers
not onlysmoked heavily inpregnancy, butwhoalso
continued to smoke after theirchildren were born. If
heavy smoking mothers
subsequently quit,
their
childrens risk was barely elevated above that of non-
smokers.The key risk thus seemed associatedwith
persistent maternal smoking,rather thanwith smoking in
pregnancy per se.
Two interpretations flow from these findings. First, it
remains possible that prenatal cigarettesmokingdoes
indeed contribute to vulnerability for antisocial behav-
iour, but that vulnerability requires continued postnatal
exposure tobe converted into risk. We knowof no studies
whereby a cumulative exposure modelof this kindhas yet
been explicatedinrelation to behaviouraloutcomes.
Second,rather than reflecting anycausal influence of
smoking, our findingsmaypoint totheimpact of
correlatedsocial,familial, or maternalfactorsnotin-
cluded in our analyses (Ernst et al., 2001). Our measures
of social adversitywere quite extensive, and tapped many
of the domainstypically reported in studies of childhood
1027
conductproblems;althoughitremainsplausiblethat
other social factors strongly correlated with persistent
smoking could account for the pattern of thefindings, it
is not immediately obvious whatthese would be. We were
not, however,able tocontrol fortwoother types of
potentially important confounds : aspects of parenting,
and of maternal personality characteristics, that might
show links with both persistent maternal smoking and
withchildhooddisruptivebehaviours.Oneprevious
epidemiological study has reported effects of maternal
smoking controlled for adverse parenting (Fergusson et
al., 1998). The role of maternal personality characteristics
or othergenetically mediated influences has not, so far as
we are aware, been tested at this stage. Our findings that
maternalMalaisescores were consistently elevated
among persistent smokers, even by contrast with women
who quit after smoking heavily in pregnancy, hintsat the
likely importance of factors of this kind. As Fergusson
(1999) stressed in his discussion of recent findings in this
area, other aspects of mothers personality functioning
may be especially important avenues to pursue in this
regard.
Acknowledgements-The BCS70 data at birth (British Births
Survey) was collected by the National Birthday Trust Fund, at
5 and 10 years(Child Health and Education Study) by the
Department of Child Health, University of Bristol, and at 16
years (Youthscan) by the International Centre for
Child Studies.
The present study was supported by a grant from the Nuffield
Foundation to NB, JB, and BM. We are indebted to Alison
Goodman for her workinderiving many of the composite
variables used in the analyses.
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