The effects of low to moderate alcohol consumption and binge in early pregnancy on selective and sustained attention in 5-year-old children

Department of Public Health, Section of Epidemiology, Aarhus University, Aarhus, Denmark.
BJOG An International Journal of Obstetrics & Gynaecology (Impact Factor: 3.45). 06/2012; 119(10):1211-21. DOI: 10.1111/j.1471-0528.2012.03396.x
Source: PubMed
ABSTRACT
The aim was to examine the effects of low to moderate maternal alcohol consumption and binge drinking in early pregnancy on children's attention at 5 years of age.
Prospective follow-up study.
Neuropsychological testing in four Danish cities 2003-2008.
A cohort of 1628 women and their children sampled from the Danish National Birth Cohort.
Participants were sampled based on maternal alcohol consumption during pregnancy. At 5 years of age, the children were tested with the recently developed Test of Everyday Attention for Children at Five (TEACh-5). Parental education, maternal IQ, maternal smoking in pregnancy, the child's age at testing, gender, and tester were considered core confounding factors, whereas the full model also controlled the following potential confounding factors: maternal binge drinking or low to moderate alcohol consumption, age, body mass index (BMI), parity, home environment, postnatal smoking in the home, child's health status, and indicators for hearing and vision impairments.
TEACh-5 attention scores.
There were no significant effects on test performance in children of mothers drinking up to 8 drinks per week compared with children of mothers who abstained, but there was a significant association between maternal consumption of 9 or more drinks per week and risk of a low overall attention score (OR 3.50, 95% CI 1.15-10.68). No consistent or significant associations were observed between binge drinking and attention test scores.
The findings suggest an effect of maternal consumption of 9 or more drinks per week on attention functions in children, but the study detected no effects of lower levels of maternal consumption and no consistent effects of maternal binge drinking.

Full-text

Available from: Ulrik Schiøler Kesmodel, Oct 04, 2014
The effects of low to moderate alcohol
consumption and binge drinking in early
pregnancy on selective and sustained attention
in 5-year-old children
M Underbjerg,
a,b
US Kesmodel,
a,c
NI Landrø,
d
L Bakketeig,
e
J Grove,
a,f
T Wimberley,
g
TR Kilburn,
a
C Sværke,
a
P Thorsen,
h
EL Mortensen
i
a
Department of Public Health, Section of Epidemiology, Aarhus University, Aarhus, Denmark
b
Children’s Neurocenter at Vejlefjord
Rehabilitation Center, Stouby, Denmark
c
Department of Obstetrics and Gynaecology, Aarhus University Hospital, Aarhus, Denmark
d
Department of Psychology, Centre for the Study of Human Cognition, University of Oslo, Oslo, Norway
e
National Institute of Public
Health, University of Oslo, Oslo, Norway
f
Department of Biomedicine, Faculty of Health Sciences and Bioinformatics Research Centre
(BiRC), Aarhus University, Aarhus, Denmark
g
Section of Biostatistics, Department of Public Health, Aarhus University, Aarhus, Denmark
h
Department of Obstetrics and Gynaecology, Lillebaelt Hospital, Kolding, Denmark
i
Institute of Public Health and Center for Healthy Aging,
University of Copenhagen, Copenhagen, Denmark
Correspondence: Prof EL Mortensen, Medical Psychology Unit, Institute of Public Health, University of Copenhagen, Øster Farimagsgade A,
DK-1353, Copenhagen K, Denmark. Email elme@sund.ku.dk
Accepted 10 April 2012. Published Online 20 June 2012.
Objective The aim was to examine the effects of low to moderate
maternal alcohol consumption and binge drinking in early
pregnancy on children’s attention at 5 years of age.
Design Prospective follow-up study.
Setting Neuropsychological testing in four Danish cities 2003–
2008.
Population A cohort of 1628 women and their children sampled
from the Danish National Birth Cohort.
Methods Participants were sampled based on maternal alcohol
consumption during pregnancy. At 5 years of age, the children
were tested with the recently developed Test of Everyday
Attention for Children at Five (TEACh-5). Parental education,
maternal IQ, maternal smoking in pregnancy, the child’s age at
testing, gender, and tester were considered core confounding
factors, whereas the full model also controlled the following
potential confounding factors: maternal binge drinking or low to
moderate alcohol consumption, age, body mass index (BMI),
parity, home environment, postnatal smoking in the home,
child’s health status, and indicators for hearing and vision
impairments.
Main outcome measures TEACh-5 attention scores.
Results There were no significant effects on test performance in
children of mothers drinking up to 8 drinks per week compared
with children of mothers who abstained, but there was a
significant association between maternal consumption of 9 or
more drinks per week and risk of a low overall attention score
(OR 3.50, 95% CI 1.15–10.68). No consistent or significant
associations were observed between binge drinking and attention
test scores.
Conclusions The findings suggest an effect of maternal
consumption of 9 or more drinks per week on attention functions
in children, but the study detected no effects of lower levels of
maternal consumption and no consistent effects of maternal binge
drinking.
Keywords Attention, attention deficits, binge drinking, maternal
alcohol consumption, prenatal alcohol exposure, selective atten-
tion, sustained attention, TEACh-5.
Please cite this paper as: Underbjerg M, Kesmodel U, Landrø N, Bakketeig L, Grove J, Wimberley T, Kilburn T, Sværke C, Thorsen P, Mortensen E. The
effects of low to moderate alcohol consumption and binge drinking in early pregnancy on selective and sustained attention in 5-year-old children. BJOG
2012;119:1211–1221.
ª 2012 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2012 RCOG 1211
DOI: 10.1111/j.1471-0528.2012.03396.x
www.bjog.org
Epidemiology
Page 1
Introduction
Attention deficits and dysfunctions in children are among
the most commonly reported effects of drinking during
pregnancy,
1–5
and prenatal alcohol exposure has been sug-
gested to constitute a key element in the development of a
subtype of Attention Deficit Hyperactivity Disorder
(ADHD).
6,7
However, other studies have failed to observe a
relationship between prenatal alcohol exposure and atten-
tion problems.
8–11
Cerebral structural changes after prenatal alcohol expo-
sure have been observed in several areas considered to be
involved in attention processes, such as the parietal and or-
bitofrontal regions, cerebellum, and the basal ganglia.
12,13
To date, most studies have looked at the impact of rela-
tively high doses of prenatal alcohol exposure (i.e. an
intake of about one drink per day or more), but there is a
growing concern that prenatal exposure to more moderate
quantities of alcohol may also be damaging to cognitive
and behavioural functions in the offspring.
14,15
It remains
unclear whether there is a safe level of drinking during
pregnancy,
16
and in spite of animal studies suggesting that
the brain may be particularly susceptible to high peak
blood alcohol concentrations,
17
only very few human stud-
ies have investigated the effect of exposure to binge drink-
ing during pregnancy on neurocognitive and behavioural
outcomes in offspring.
18
Results are inconsistent, and
whether binge drinking, independent of the average alcohol
intake, is harmful to the cognitive development of offspring
remains an open question.
Attention is a multidimensional construct related to
memory and executive functions.
19
In an influential review,
Posner and Petersen
20
argued, from adult neuropsychologi-
cal and functional imaging evidence, that distinct attention
networks are vulnerable to selective damage, and that sys-
tems involved in selective attention (e.g. finding a visual
target among distractors) diverge from those involved in
sustained attention or alertness (e.g. maintaining a readi-
ness to respond over a long interval). The proposed separa-
tion does not necessarily imply that these functions share
no common processes, but rather that they have distinct
features and are susceptible to being differentially damaged.
Several studies have investigated the effects of prenatal
alcohol exposure on sustained attention (visual vigilance)
using variants of the Continuous Performance Task,
21
whereas fewer studies have examined selective atten-
tion,
5,22,23
and overall it remains unclear whether some
aspects of attention are more vulnerable to prenatal alcohol
exposure than others. The aim of the current study was to
examine the effects of low to moderate maternal alcohol
consumption and binge drinking during pregnancy on
attention functions at 5 years of age, using a recently devel-
oped, theoretically founded, and comprehensive test bat-
tery, the Test of Everyday Attention for Children at Five
(TEACh-5),
24
designed to conduct differential assessment
of selective and sustained attention.
Methods
Sample
The design of the Lifestyle During Pregnancy Study (LDPS)
has been described in detail elsewhere.
25
Briefly, the study
is a prospective follow-up, based on a sample from the
Danish National Birth Cohort (DNBC),
26
with oversam-
pling of moderate to high alcohol exposure categories,
including binge drinking.
25
The DNBC consists of 101 042
women and their offspring, recruited from 1997 to 2003 at
their first antenatal visit to a general practitioner, who rou-
tinely is the first health practitioner to see a pregnant
woman. The participating women represent 60% of those
invited and approximately 30% of all pregnant women in
Denmark in the enrolment period. Based on their alcohol-
drinking pattern before and during pregnancy, a total of
3478 women with singleton pregnancies were sampled from
the DNBC and invited to participate in the LDPS between
2003 and 2008.
25
Of the invited women, 3189 were sam-
pled on the basis of their alcohol intake during pregnancy.
Of these women, 1628 mothers and their children partici-
pated in a 5-year follow-up, and only these mother and
child pairs were included in the analyses. Information on
binge drinking was invalid for 11 of the 1628 mothers, and
consequently the binge drinking analyses were conducted
on 1617 mothers and their children.
Exclusion criteria for the LDPS were an inability to
speak Danish, an inability to complete the cognitive tests
because of impaired hearing or vision, multiple pregnan-
cies, and congenital diseases likely to cause mental retarda-
tion (e.g. trisomy 21).
The 5-year follow-up
The follow-up study was designed to assess attention func-
tions, and also included assessment of intelligence with
three verbal and three performance subtests from the
Wechsler Primary and Preschool Scales of Intelligence
Revised (WPPSI-R).
27
The cognitive test battery was
administered to children aged from 5 years to 5 years and
4 months. Testing took place in four major cities in Den-
mark (Copenhagen, Odense, Aalborg, and Aarhus). Test
procedures were standardised in detail and carried out by
ten trained psychologists blinded to the children’s exposure
status. Tester differences were taken into account by the
inclusion of indicator variables in the statistical analyses.
Exposure information
Information on alcohol intake during pregnancy was derived
from the first prenatal DNBC interview,
26
conducted at a
Underbjerg et al.
1212 ª 2012 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2012 RCOG
Page 2
median gestational age of 17 weeks (range: 7–39 weeks).
During the interview the women were asked about the aver-
age number of beers, glasses of wine, and glasses of spirits
they currently consumed during a week, and based on this
information, the total number of weekly drinks was calcu-
lated. Information on binge drinking during pregnancy
included data on the number of binge episodes (defined as
an intake of 5 or more drinks on a single occasion) and the
timing (gestational week) of these episodes. Some women
reported one or more binge episodes during the early weeks
of pregnancy, although their average number of drinks per
week at the time of interview was zero. These women were
classified accordingly as consuming 0 drinks at the time of
interview, but with one or more previous binge episodes.
Our definition of a drink followed that of the Danish
National Board of Health, with one standard drink being
equal to 12 g of pure alcohol. For this study low drinking
was defined as consuming between one and 4 drinks per
week, and moderate drinking was defined as consuming
between five and 8 drinks per week.
All mothers were sampled in strata defined by their aver-
age alcohol intake (0, 1–4, 5–8, 9 drinks/week), and by
the timing and number of binge episodes (gestational
weeks 1–2, 3–4, 5–8, 9, or later).
25
The higher exposure
categories were oversampled in an effort to ensure that all
exposure categories included enough children to attain suf-
ficient statistical power. For each sample stratum the sam-
pling probability was computed as the ratio between the
number of sampled women and the total number of
women available in the corresponding DNBC stratum.
Outcome measures
Attention was assessed by TEACh-5,
24
which is the most
recent development in a series of comprehensive attention
test batteries.
28
Briefly, TEACh-5 takes the form of a children’s story-
book, with puzzles and games to complete with the charac-
ters. To obtain pure measures of attention, demands on
task comprehension, memory, reasoning, language, and
motor skills have been minimised. For all subtests, practise
trials formally checking the comprehension of instructions
and basic visual and auditory skills were included. Auditory
stimuli consist of animal noises that are relatively universal
and usually recognisable at an earlier developmental stage
than complicated language, and verbal responses are few
and kept to simple yes/no answers.
Several subtest scores can be derived from TEACh-5.
24
For the present analyses two subtests assessing selective
attention and two subtests assessing sustained attention
were selected. Subtests with an approximate normal distri-
bution of test scores (or transformed test scores) and with
a pattern of positive intercorrelations were selected. An
overall composite mean attention score was derived from
the four selected subtests, and in addition means were
derived for selective attention and for sustained attention.
Selective attention
The Great Balloon Hunt. The children were given 15 sec-
onds to mark as many as possible of 48 balloon targets on
a greyscale A4 sheet, first on a sheet with nothing but bal-
loons, and second on a sheet with the target balloons dis-
tributed among visual distractors. The sum of the scores
on the two tasks was used in the present analyses.
Hide and Seek II. The task was to listen to a total of 14
sound clips of 10-seconds duration, and then to report
whether the target element (a bark from the dog) was
absent or present. The level of performance was measured
by a compound score reflecting both accuracy and speed
by weighing the mean reaction time when the bark was
present based on the proportionate accuracy of the items.
Only the log-transformed compound score was used in the
present study.
Sustained attention
Barking. The children were told to listen to ten CD tracks
of a single, repeated dog bark, and to keep a count of how
many barks occurred on each item. The longest tone string
was six, the shortest was two, and intervals between the
stimuli varied between 2 and 10 seconds, with a total of
four ‘fast presented items’ and six ‘slowly presented items’.
The number of correct slowly presented items had an
approximately symmetric distribution, and was used in the
present analyses.
Draw-a-Line. The children were asked to use a pen to
trace a line as slowly as possible without stopping and
without lifting the pen from the page. To ensure that left-
handed children were not disadvantaged, the pages were
presented in opposite orientations (i.e. the practise went
from left to right and the test item from right to left, or
vice versa). The time taken in seconds to complete the task
was noted, and for data analysis this time measure was log
transformed.
The total number correct (Barking and Great Balloon
Hunt) and the log-transformed scores (Hide and Seek II
and Draw-a-Line) were first standardised to a mean of 0
and an SD of 1 (for Hide and Seek II the standardised score
was reversed to ensure that higher scores reflected a better
performance). Then, the mean of the four standardised
scores was calculated and re-standardised to a mean of 0
and an SD of 1 for use in the statistical analyses. Similarly,
mean scores were derived for selective attention (Great
Balloon Hunt and Hide and Seek II), and for sustained
attention (Barking and Draw-a-Line). The calculation of
the mean score of overall attention was corroborated by a
principal component analysis, showing that all four subtests
The effects of early prenatal alcohol consumption
ª 2012 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2012 RCOG 1213
Page 3
loaded on the first principal component. The overall atten-
tion mean has also been analysed together with measures
of intelligence and executive functioning, but this is
reported in a separate article.
29
Covariates
The following covariates were obtained in the prenatal
interview, and were subsequently coded as follows: parity
(0, 1, 2+); prenatal maternal smoking (yes/no); and
maternal pre-pregnancy BMI [weight in kg/(height in
m
2
)]. At the time of the 5-year follow-up, the following
variables were recorded: length of parental education in
years (the average educational length for the two parents
or the length of maternal education if information on
the father was unavailable); marital status (single either
at the prenatal interview or at the follow-up/married or
cohabitating at both); postnatal parental smoking (yes, if
at least one of the parents smoked in the home/no if
otherwise); child health status, i.e. the presence of any
medical conditions (epilepsy, or syndromes such as Mor-
pheus syndrome, von Recklinghausen’s neurofibromatosis,
congenital toxoplasmosis, or myxoedema) or regular
medications (such as medicines for asthma and allergies,
methylphenidate for ADHD, and medicines for epilepsy
and respiratory conditions) that might influence test per-
formance; dichotomised family/home environment index
(presence of two or more of the following seven adverse
conditions: living with only one biological parent;
changes in primary caregiver; daycare for more than 8
hours a day before the age of 3 years; 14 days of
separation from parents; breakfast irregularity; maternal
depression; and parental alcohol use above the maximum
recommended level by the Danish National Board of
Health of 14 drinks/week for non-pregnant women or
21 drinks/week for men); the child’s hearing ability mea-
sured on the day of the test (impaired/not impaired);
and the child’s vision ability measured on the day of the
test (impaired/not impaired).
Maternal IQ was assessed at the follow-up examination:
two verbal subtests (information and vocabulary) from the
Wechsler Adult Intelligence Scale
30
(WAIS) were used to
assess verbal IQ, and the Raven’s Standard Progressive
Matrices provided non-verbal IQ.
31
Raw scores of each test
were standardised based on the results from the full sample
and weighted equally in a combined score that was restan-
dardised to an IQ scale with a mean of 100 and an SD
of 15.
Maternal age was obtained directly from the unique
Danish personal identification number, as was the child’s
gender and age at testing. Birthweight (g) and gestational
age (days) were obtained from the Danish Medical Birth
Registry.
Data analysis
All statistical analyses were conducted in stata 11 (Stata-
Corp LP, College Station, TX, USA) and weighted by sam-
pling probabilities with robust variance estimation. All
statistical tests were two-sided and declared significant at a
level of 5%.
The number of missing values for the covariates ranged
from two to 33, but the number of missing values on the
overall attention, selective attention, and sustained attention
means were 249, 136, and 162, respectively. Missing values
were imputed based on two strategies: a dedicated model
for imputation with missing values modelled from the other
variables considered to be most predictive of each variable
(specific equations are available upon request), and a black-
box strategy with all outcomes, exposures, and covariates
used to predict missing values. For both strategies 100 com-
pleted data sets were generated. Regardless of imputation
strategy, the main conclusions were unaffected, and the
point estimates of the exposure parameters never differed
by more than 18% relative to their standard error. Essen-
tially the same results were obtained when the strategy of
complete case analysis was used, and only results based on
the dedicated imputation strategy will be reported. All
imputations were implemented with the ice add-on com-
mand and the built-in mi estimate command in stata 11.
The primary analyses used the three composite attention
scores as outcomes in multiple linear regression. In supple-
mentary analyses, the three attention outcomes were
dichotomised, using the sample mean minus 1 SD as the
cut-off for subnormal scores on overall, selective, and
sustained attention. Logistic regression was used in these
analyses, and odds ratios were calculated using the category
of attention scores above the cut-off as the reference group.
Parental education, maternal IQ, prenatal maternal
smoking, the child’s age at testing, the child’s gender, and
tester were considered to be core confounding factors,
whereas the full model also controlled for maternal age,
pre-pregnancy body mass index (BMI), parity, marital sta-
tus, home environment, postnatal parental smoking, child’s
health status, and indicators for hearing and vision impair-
ment. In the analyses of maternal average alcohol con-
sumption, binge drinking (coded yes/no) was included as a
potential confounding factor, whereas the average number
of drinks per week consumed by the mother during preg-
nancy was included as a potential confounding factor in
the analyses of effects of binge drinking (coded as 0, 1–4,
5–8, 9 drinks/week).
Birthweight, gestational age, and the child’s IQ were con-
sidered potential mediators of the effects of alcohol expo-
sure on attention. Consequently, these variables were not
included in the main analyses, but were included in sepa-
rate models evaluating potential mediation.
Underbjerg et al.
1214 ª 2012 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2012 RCOG
Page 4
In supplementary analyses, we analysed potential interac-
tions between average alcohol consumption and binge
drinking, as well as interactions of the alcohol exposure
variables with gender of the child, parental education, pre-
natal maternal binge drinking, and maternal smoking dur-
ing pregnancy. Furthermore, raw scores of each of the four
individual TEACh-5 subtests were analysed with regression
models adjusting for core and all confounding factors.
Results
Sample characteristics are presented elsewhere.
32,33
Nota-
bly, women reporting no alcohol consumption during a
typical week were significantly younger, and were also
significantly more likely to be primiparous and less likely
to be smokers or have suboptimal family/home condi-
tions. Smoking and suboptimal family/home conditions
were more frequent among women who reported con-
suming 5 or more drinks per week.
32
Women without
binge drinking episodes were significantly older, less
likely to be primiparous, had significantly higher BMI,
were less likely to be smokers, had a lower average alco-
hol intake, and had significantly lower IQs, compared
with bingers.
33
No substantial differences were seen
between participants and non-participants.
Results for low to moderate alcohol intake
Overall attention mean
Both the crude and adjusted analyses showed the same
pattern (
Table 1). The overall mean scores for the children
of mothers who drank 1–4 and 5–8 drinks per week drinks
per week were almost identical to the mean of the offspring
of the reference group of mothers who did not drink alco-
hol during a typical week. By contrast, the mean attention
scores associated with consuming 9 drinks per week were
substantially lower than that observed for the reference
group, but because of the small number of children in this
category the confidence intervals were wide, and the
adjusted differences from the reference group were not sta-
tistically significant. However,
Table 2 shows that when the
Table 1. Associations between maternal average alcohol intake in pregnancy and offspring mean TEACh-5 mean scores, Denmark, 2003–2007
Average no. drinks/week in pregnancy Crude Adjusted for core
confounding factors*
Adjusted for p otential
confounding factors**
Mean
score
Mean
difference
95% CI Mean
difference
95% CI Mean
difference
95% CI
Overall attention mean***
0 )0.03 Reference
Reference Reference
1–4 )0.02 0.02 )0.14; 0.17 0.01 )0.14; 0.16 0.03 )0.12; 0.18
5–8 )0.02 0.01 )0.27; 0.30 0.00 )0.27; 0.28 0.03 )0.26; 0.32
9 )0.56 )0.52 )1.17; 0.12 )0.56 )1.20; 0.07 )0.45 )1.08; 0.18
P**** 0.44 0.37 0.50
Selective attention mean
0 )0.04 Reference Reference Reference
1–4 )0.02 0.02 )0.14; 0.18 0.04 )0.12; 0.19 0.07 )0.09; 0.22
5–8 0.07 0.12 )0.15; 0.39 0.10 )0.15; 0.36 0.16 )0.10; 0.42
9 )0.63 )0.58 )1.11; )0.06 )0.64 )1.17;–0.10 )0.48 )1.00; 0.03
P**** 0.12 0.08 0.11
Sustained attention mean
0 )0.01 Reference Reference Reference
1–4 )0.00 0.01 )0.15; 0.16 )0.02 )0.17; 0.13 )0.02 )0.17; 0.14
5–8 )0.10 )0.09 )0.38; 0.20
)0.09 )0.38; 0.19 )0.10 )0.40; 0.20
9 )0.24 )0.24 )0.88; 0.41 )0.25 )0.89; 0.40 )0.22 )0.89; 0.45
P**** 0.82 0.82 0.85
*Parental education, maternal IQ, prenatal maternal smoking, the child’s gender and age, and tester.
**Parental education, maternal IQ, prenatal maternal smoking and binge drinking, maternal age, parity, prenatal and postnatal marital status,
postnatal parental smoking, maternal pre-pregnancy BMI, the child’s gender and age, health status, hearing and vision on the day of testing,
family/home environment, and tester.
***The number of children in each exposure category was 758, 675, 175, and 20 for the 0, 1–4, 5–8 and 9 drinks/week categories,
respectively.
****P value for the hypothesis of no difference in attention scores across levels of average alcohol intake.
The effects of early prenatal alcohol consumption
ª 2012 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2012 RCOG 1215
Page 5
overall attention mean was dichotomised and analysed by
logistic regression models, the odds ratios associated with
consuming 9 drinks per week were significant, with
adjustment for both core confounding factors (OR 3.61,
95% CI 1.22–10.71) and all potential confounding factors
(OR 3.20, 95% CI 1.08–9.53).
Selective attention
For the mean selective attention scores, a similar pattern
was observed (Table 1). The mean scores of offspring of
mothers who drank 1–4 and 5–8 drinks per week were
similar to the mean scores observed for children whose
mothers did not drink alcohol. However, the children of
mothers who consumed 9 drinks per week performed
about 0.5 SD below the reference group, and the difference
was significant for both the crude and the core confounding
factor-adjusted analyses. Table 2 shows that results were
corroborated when the dichotomised selective attention
score was analysed with significant odds ratios for the crude
and the core confounding factor-adjusted logistic regression
models (OR 3.32, 95% CI 1.23–9.00, and OR 4.42, 95% CI
1.38–14.22, respectively). However, when adjusted for all
potential confounding factors, the mean difference and the
adjusted odds ratio were insignificant (OR 3.22, 95% CI
0.94–11.05), albeit of a comparable magnitude.
Sustained attention
Corresponding to the pattern for selective attention, the
mean sustained attention scores of the children whose
mothers drank 1–4 and 5–8 drinks per week were similar
to the means of the reference group (Table 1). The mean
of the children whose mothers drank 9 drinks per week
was only 0.24 SD below the mean of the reference group,
but analysis of the dichotomised variable with adjustment
for all potential confounding factors showed a significantly
increased risk of low sustained attention performance for
the 9 group (OR 4.19, 95% CI 1.17–14.96).
The supplementary analyses showed no consistent effects
of alcohol exposure on raw scores for individual TEACh-5
subtests. The dichotomised ‘barking’ score showed a signifi-
cantly increased OR associated with consuming 9 drinks
per week during pregnancy, with adjustment for core
Table 2. Associations between maternal average alcohol intake in pregnancy and below-average offspring TEACh-5 scores (<1 SD below the
mean), Denmark, 2003–2007
Average no. drinks/week in pregnancy Crude Adjusted for core con-
founding factors*
Adjusted for potential
confounding factors**
Odds ratio 95% CI Odds ratio 95% CI Odds ratio 95% CI
Overall attention mean***
0 Reference Reference Reference
1–4 1.20 0.81; 1.79 1.22 0.80; 1.84 1.17 0.75; 1.81
5–8 1.27 0.66; 2.47 1.41 0.69; 2.90 1.37 0.63; 2.97
9 2.73 1.02;7.31 3.61 1.22; 10.71 3.20 1.08; 9.53
P**** 0.23 0.13 0.22
Selective attention mean
0 Reference Reference Reference
1–4 1.08 0.72; 1.61 1.03 0.66; 1.59 0.97 0.62; 1.54
5–8 0.95 0.49; 1.82 1.09 0.57; 2.11 0.94 0.45; 1.95
9 3.32 1.23; 9.00 4.42 1.38; 14.22 3.22 0.94; 11.05
P**** 0.12 0.09 0.26
Sustained attention mean
0 Reference Reference Reference
1–4 1.03 0.69; 1.54 1.11 0.73; 1.69 1.15 0.74; 1.78
5–8 1.63 0.82; 3.23 1.78 0.84; 3.77 2.05 0.95; 4.41
9 2.12 0.71; 6.32 2.66 0.84; 8.38 4.19 1.17; 14.96
P**** 0.31 0.20 0.06
*Parental education, maternal IQ, prenatal maternal smoking, the child’s gender and age, and tester.
**Parental education, maternal IQ, prenatal maternal smoking and binge drinking, maternal age, parity, prenatal and postnatal marital status,
postnatal parental smoking, maternal pre-pregnancy BMI, the child’s gender and age, health status, hearing and vision on the day of testing, fam-
ily/home environment, and tester.
***The number of children in each exposure category was 758, 675, 175, and 20 for the 0, 1–4, 5–8 and 9 drinks/week categories, respec-
tively.
****P value for the hypothesis of no difference in OR for attention score below the sample mean )1 SD across levels of average alcohol intake.
Underbjerg et al.
1216 ª 2012 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2012 RCOG
Page 6
confounding factors (OR 3.31, 95% CI 1.03–10.62), but the
increase in OR was not statistically significant when
adjusted for all potential confounding factors.
Tests of interactions with gender, parental education,
and prenatal maternal binge drinking were not statistically
significant. A test of the interaction with prenatal smoking
was marginally significant for the mean selective attention
score, and stratified analysis showed a trend towards stron-
ger effects of maternal consumption of 9 drinks per week
among the children of mothers who also smoked.
Adjustment for gestational age and birthweight did not
change the results for any of the analyses, whereas adjust-
ment for the child’s WPPSI-R full-scale IQ was associated
with smaller effect estimates for the 9 drinks per week
consumption category.
Results for binge drinking
No significant differences were observed for the dichoto-
mous binge variable, for the number of binge drinking
episodes during pregnancy, or for the timing of binge
drinking. For the overall attention mean, unadjusted ana-
lyses showed a small, but significant, increase in attention
score associated with binge drinking during gestational
weeks 5–8 (Table 3). However, when adjusting for core
and potential confounding factors, no significant or clini-
cally relevant differences were observed (Table 3). These
results were corroborated by linear regression analyses of
the selective and sustained attention scores, which
showed no significant or clinically relevant effects for the
dichotomous binge variable, for the number of binge
drinking episodes during pregnancy, or for the timing of
binge episodes in the unadjusted or the adjusted analyses
(data not shown). The number of binge episodes
reported in early pregnancy did not vary with time of
interview.
Corroborating these findings, supplementary analyses of
the dichotomised overall attention mean score, and the di-
chotomised selective and sustained attention scores, showed
no significant associations with any binge variable (data
not shown). Supplementary analyses also showed no con-
Table 3. Associations between maternal binge drinking in pregnancy and TEACh-5 offspring overall attention mean, Denmark, 2003–2008
Crude Adjusted for core
confounding factors*
Adjusted for potential
confounding factors**
Mean
score
Mean
difference
95% CI Mean
difference
95% CI Mean
difference
95% CI
Binge drinking in pregnancy***
No )0.04 Reference Reference Reference
Yes 0.01 0.05 )0.07; 0.17 )0.01 )0.13; 0.11 )0.02 )0.14; 0.10
P**** 0.45 0.86 0.80
Number of binge drinking episodes in pregnancy***
0 )0.04 Reference Reference Reference
1 )0.01 0.03 )0.10; 0.16 )0.01 )0.14; 0.11 )0.02 )0.15; 0.10
2 0.03 0.07 )0.11;.0.25 )0.02 )0.19; 0.16 )0.02 )0.20; 0.16
3+ 0.05 0.09 )0.15; 0.32 0.02 )0.21; 0.25 0.04 )0.19; 0.27
P**** 0.81 0.99 0.95
Timing of binge drinking episodes in pregnancy (gestational week)***
No binge drinking ) 0.04 Reference Reference Reference
1–2 0.05 0.09 )0.08; 0.25 0.01 )0.15; 0.17 0.00 )0.16; 0.16
3–4 )0.07 )0.03 )0.19; 0.13 )0.09 )0.25; 0.07 )0.11 )0.27; 0.06
5–8 0.15 0.19 0.03; 0.35 0.13 )0.02; 0.28 0.13
)0.02; 0.28
9 0.01 0.05 )0.12; 0.21 0.04 )0.12; 0.20 0.04 )0.13; 0.22
Multiple episodes 0.02 0.06 )0.13; 0.25 0.01 )0.17; 0.20 0.02 )0.17; 0.21
P**** 0.20 0.27 0.21
*Parental education, maternal IQ, prenatal maternal smoking, age at testing, gender of child, and tester.
**Parental education, maternal IQ, prenatal maternal smoking, prenatal maternal average alcohol intake, maternal age, parity, prenatal and post-
natal marital status, postnatal parental smoking, maternal pre-pregnancy BMI, gender of child, age at testing, health status, hearing and vision on
the day of testing, and family/home environment and tester.
***Of the 1617 mothers, 1122 reported binge drinking on one or more occasions (range: 3–12 episodes). The number of children in each cate-
gory was 495, 783, 225, and 114 for 0, 1, 2, and 3+ episodes, respectively. The number of children in each timing category was 495, 237, 261,
216, 234, and 174.
****P value for the hypothesis of no difference in mean attention scores across levels of average alcohol intake.
The effects of early prenatal alcohol consumption
ª 2012 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2012 RCOG 1217
Page 7
sistent effects of binge drinking on raw scores from indivi-
dual TEACh-5 subtests.
For the overall attention mean score, the interaction
between parental education and the dichotomous binge
variable was significant (P = 0.05) in the model adjusting
for core confounding factors, and was marginally signifi-
cant in the model adjusting for all potential confounding
factors (P = 0.06). Stratified analyses showed a non-signifi-
cant negative effect of binge drinking among offspring of
parents with high education, and a non-significant positive
effect of binge drinking among offspring of parents with
low education.
Discussion
In this study maternal binge drinking was not associated
with consistent effects, but a consistent pattern was
observed for the effects of maternal low to moderate con-
sumption on the three attention composite means: the
consumption of 1–4 and 5–8 drinks per week during preg-
nancy was not associated with adverse effects, whereas con-
suming 9 drinks per week during pregnancy was
associated with significant or marginally significant negative
effects. For the overall attention mean score no significant
effects were observed in the linear models, whereas the
logistic models showed significant unadjusted and adjusted
odds ratios. The effects on the selective attention mean
score were significant in both crude and core confounding
factor-adjusted linear and logistic analyses, but when the
analyses included adjustment for all potential confounding
factors, the effects became smaller and non-significant.
Finally, the only significant association observed for the
sustained attention mean score was significantly increased
odds for performing below the dichotomised cut-off level
when adjusted for all potential confounding factors. Signifi-
cant effects were only observed for offspring of mothers
who drank 9 drinks per week, and because of the small
sample size in this category, all confidence intervals were
wide.
This is one of very few studies to specifically address the
effects of low to moderate prenatal alcohol exposure on
offspring attention functions. The finding of no significant
effects associated with consuming <9 drinks per week dur-
ing pregnancy seems to be consistent with results from a
longitudinal study reporting no association between low to
moderate (or high) prenatal alcohol exposure and various
attention measures,
10
with studies reporting no association
between low to moderate consumption and a questionnaire
on reported attention problems,
34
and with null findings in
studies using computerised measures of (sustained) atten-
tion.
9,11
Furthermore, it can be argued that the apparent
effects associated women consuming 9 or more drinks per
week during pregnancy are in line with the findings of sev-
eral studies based on the The Seattle Longitudinal Prospec-
tive Study on Alcohol and Pregnancy, reporting adverse
effects of prenatal alcohol exposure on attention functions,
in particular on vigilance/sustained attention.
4,5,34,35
It is well established that prenatal alcohol exposure may
affect offspring intelligence,
2
and as correlations have been
observed between intelligence and attention measures,
24
effects on intelligence may mediate effects on attention
functions. Consequently, we conducted separate analyses
including the child’s IQ as a covariate to evaluate the spe-
cific effects of prenatal low to moderate alcohol exposure
on attention, independent of effects on global cognitive
function. Including the IQ of offspring as a covariate atten-
uated the effect estimates associated with consuming 9
drinks per week during pregnancy, and it is possible that
the effects of prenatal alcohol exposure on general intelli-
gence to some extent mediate effects on attention.
Overall, no systematic associations between binge drink-
ing during early pregnancy and offspring attention scores
were observed in this study. The evidence of improved per-
formance associated with binge drinking in gestational
weeks 5–8 was only significant in the unadjusted analyses,
and indeed the results presented in Table 3 are consistent
in showing no significant effects and effect estimates that
were close to zero. The analyses of the dichotomised atten-
tion composite means corroborated these findings, which
were also supported when the overall attention mean score
was analysed together with measures of intelligence and
executive functioning.
29
Thus, this large-scale study sug-
gests no or clinically insignificant effects of a few binge
drinking episodes during early pregnancy on the attention
measure used in this study.
Only few studies have investigated associations between
binge drinking and cognitive outcomes. Of the two studies
including attention measures, one study used a vigilance
paradigm and reported poorer performance in 7-year-old
children of binge drinkers than in children whose mothers
did not binge drink during pregnancy.
36
The other study
used questionnaires and reported no statistically significant
association between the attention scores of the children
and the mothers’ binge drinking during pregnancy.
37
Only
one study specifically addressed the issue of the timing of
the binge episodes during pregnancy, using trimesters as a
rough differentiation of time periods, but that study did
not include attention measures.
38
The general inconsistency in results regarding the effects
of low to moderate prenatal alcohol exposure and maternal
binge drinking on attention functions may be the result of
methodological differences reflecting different study
designs, different exposure and/or outcome measures, and
different conceptualisation of attention. Our study was
based on prospectively collected information on alcohol
consumption during pregnancy, obtained through tele-
Underbjerg et al.
1218 ª 2012 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2012 RCOG
Page 8
phone interviews asking beverage-specific questions about
weekly alcohol consumption: a method that has proven
reliable in a Danish pregnant population.
39
However, the
distributions within the 1–4 and 5–8 drinks per week cate-
gories were skewed: on average, the observed exposure rep-
resents the lower tail of the distribution for these
consumption categories, suggesting that the findings are
more in line with occasional weekly drinking (1 or 2 drinks
per week for the 1–4 drinks/week group) or, at most, levels
of less than one drink per day. The study may not have
had sufficient statistical power to detect small effects associ-
ated with such low levels of consumption, although the
detected mean differences were very small. On the other
hand, potential problems with under-reporting and subse-
quent misclassification may not be negligible, and should
be considered, particularly when attempting to identify a
safe lower limit for alcohol consumption during pregnancy.
Interpretation of results regarding binge drinking must
take into account that blood alcohol concentration is not
only determined by the actual dose of alcohol consumed by
the women, but also by several other important factors such
as the time perspective, body size, and individual metabo-
lism.
40
Binge drinking is commonly defined as the intake of
5 or more drinks on a single occasion, but this definition
does not distinguish between women who consumed 5
drinks or more within one or a few hours, versus women
who spread their intake over several hours. Similarly, the
definition of binge drinking does not incorporate whether
the woman consumed 5 or 10 drinks on a single occasion.
Our study was based on prospectively collected information
obtained through telephone interviews asking the number of
times the woman consumed 5 drinks or more on a single
occasion, and during what week(s) of gestation these epi-
sodes took place: a method that has proven reliable in a Dan-
ish pregnant population.
39,41
The participants generally had
a low to moderate average alcohol intake, and the reported
number of drinks per week was included in the binge analy-
ses, adjusting for all potential confounding factors.
The availability of data on potential confounding factors
is crucial, and our study took advantage of the prospec-
tively collected and detailed information in the DNBC.
29
This information was supplemented with the assessment of
other important covariates at follow-up. In particular,
efforts were made to obtain reliable measures of parental
education, and of maternal general intellectual abilities.
Measures of maternal and paternal IQ are rarely available,
and among the studies mentioned, only one seems to have
assessed maternal intelligence.
10
Our study lacked informa-
tion on some potentially important confounding factors
such as prenatal maternal medication, and alcohol con-
sumption in late pregnancy, and even for the included
covariates there may be residual confounding as a result of
gross categorisation/dichotomisation.
Using the recently developed TEACh-5 battery has both
strengths and weaknesses. Along with the child-friendly
appearance and the relatively short time needed to admin-
ister the test battery, the most obvious advantage was the
theoretical foundation of the battery that makes it possible
to derive measures of both selective and sustained atten-
tion. However, although the psychometric properties of the
TEACh-5 have been described in detail,
24
the test battery
still needs to prove its validity as a measure of attention
that can detect relatively small effects of prenatal exposures
on offspring cognitive development.
Finally, it is also important to consider the relatively
large number of statistical tests when evaluating the signifi-
cant effects of maternal average consumption. The large
number of statistical tests may of course be associated with
spurious significant results, but we decided against adjust-
ment for multiple tests because of the risk of masking true
associations, and because, from a public health perspective,
overlooking indications of possibly harmful effects of low
to moderate and binge doses of a known teratogen may be
considered more serious than spurious significance. Fur-
thermore, we believe that the observed pattern of no effects
with maternal consumption below 9 drinks per week, and
the indications of effects from the consumption of 9
drinks per week during pregnancy, is both biologically
meaningful and consistent. In addition, we believe that the
observed pattern of effects in the TEACh-5 attention com-
posite mean scores is corroborated by other studies sug-
gesting effects of moderate maternal alcohol consumption
on offspring attention. However, the small sample of
women who consumed 9 drinks per week implies a lack
of statistical power, and experience with the TEACh-5 as a
measure of attention is still limited. For these reasons, and
because of the few and contradictory previous studies,
there is an obvious need for more studies focusing on the
effects of low to moderate prenatal alcohol exposure on
specific attention functions in offspring. Similarly, the
strengths and weaknesses of our study should be consid-
ered when interpreting the lack of consistent associations
between binge drinking during early pregnancy and off-
spring attention, even after the adjustment for maternal
intelligence and a wide set of other potential confounding
factors.
Disclosure of interests
None to declare.
Contribution to authorship
MU developed the TEACh-5 attention test. MU, USK, NIL,
LB, TRK, PT, and ELM contributed to the design of the
Lifestyle During Pregnancy Study. MU wrote the first draft
of the article, and JG, TW, and CS were responsible for the
statistical analyses. All authors contributed to the interpre-
The effects of early prenatal alcohol consumption
ª 2012 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2012 RCOG 1219
Page 9
tation of the results, and provided critical comments and
revisions of the article.
Details of ethics approval
The study was approved by the DNBC Board of Directors,
the DNBC Steering Committee, the Regional Ethics Com-
mittee, the Danish Data Protection Agency, and the Institu-
tional Review Board at the Centers for Disease Control and
Prevention. Signed informed consent was obtained for the
LDPS.
Funding
This study was primarily supported by the Centers for Disease
Control and Prevention (CDC),Atlanta,Georgia,USA.
Acknowledgement
The Danish National Research Foundation established the
Danish Epidemiology Science Centre that initiated and cre-
ated the Danish National Birth Cohort. The cohort was fur-
thermore a result of a major grant from this Foundation.
Additional support for the Danish National Birth Cohort
was obtained from the Pharmacy Foundation, the Egmont
Foundation, the March of Dimes Birth Defects Foundation,
the Augustinus Foundation, and the Health Foundation.
The authors would like to thank all the participants for
their time, as well as Dr Tom Manly for his contribution
to the development of the TEACh-5 test.
j
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The effects of early prenatal alcohol consumption
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  • Source
    • "We also analyzed potential interactions between average alcohol consumption and binge drinking and interactions of these factors with smoking, sex of child, and parental education. As in previous analysis of the LDPS-data [8,30] parental education, maternal IQ, prenatal maternal smoking, the child's age at testing, child's sex, and tester were considered core confounders , while the full model also controlled for maternal age, pre-pregnancy BMI, parity, marital status, home environment, postnatal parental smoking, child's health status, and indicators for hearing and vision impairment. In the full models prenatal maternal binge drinking (coded yes/no) was included as potential confounder in analyses of average number of drinks per weeks, while maternal average number of drinks per week during pregnancy (coded 0, 1–4, 5–8, 9 drinks per week) was included as in the analyses of effects of binge drinking. "
    [Show abstract] [Hide abstract] ABSTRACT: Background: Deficits in information processing may be a core deficit after fetal alcohol exposure. This study was designed to investigate the possible effects of weekly low to moderate maternal alcohol consumption and binge drinking episodes in early pregnancy on choice reaction time (CRT) and information processing time (IPT) in young children. Method: Participants were sampled based on maternal alcohol consumption during pregnancy. At the age of 60-64 months, 1,333 children were administered a modified version of the Sternberg paradigm to assess CRT and IPT. In addition, a test of general intelligence (WPPSI-R) was administered. Results: Adjusted for a wide range of potential confounders, this study showed no significant effects of average weekly maternal alcohol consumption during pregnancy on CRT or IPT. There was, however, an indication of slower CRT associated with binge drinking episodes in gestational weeks 1-4. Conclusion: This study observed no significant effects of average weekly maternal alcohol consumption during pregnancy on CRT or IPT as assessed by the Sternberg paradigm. However, there were some indications of CRT being associated with binge drinking during very early pregnancy. Further large-scale studies are needed to investigate effects of different patterns of maternal alcohol consumption on basic cognitive processes in offspring.
    Full-text · Article · Sep 2015 · PLoS ONE
  • Source
    • "Preschool and Primary Scale of Intelligence, Wechsler or Wide Range Achievement Test or subscales of these tests [6,11,13,15,19,33343536 . For the evaluation of child behavior the authors used The Child Behavior Checklist [5,29] or Test of Everyday Attention for Children [28,36]. "
    [Show abstract] [Hide abstract] ABSTRACT: Maternal active and passive smoking and low or moderate alcohol drinking during pregnancy, taking into account the level of exposure and developmental or behavioral outcomes, are recognized as a significant issue from both a clinical and a public health perspective. The article aims at evaluating the impact of prenatal exposure to tobacco smoke constituents and low or moderate alcohol drinking during pregnancy on children neurodevelopment by reviewing the most recently published literature. Relevant studies were identified by searching the Pubmed, Medline and Ebsco literature databases. This review is restricted to 29 human studies published in English in peer reviewed journals since 2006. The studies published recently continued to show some relationship between tobacco smoke exposure, from active and passive maternal smoking during pregnancy, and children's psychomotor development independent of other variables, but this relationship is not straightforward. The association is mostly consistent for measures of academic achievements and behavioral problems which require further attention. The results of the studies on low or moderate exposure to alcohol are not fully conclusive, but some of them suggest that consumption of alcohol during pregnancy may adversely affect children's intelligence quotient (IQ), mental health, memory and verbal or visual performance. As the reviewed studies indicate, maternal lifestyle during pregnancy like alcohol drinking or smoking may affect children neurodevelopment. All effort should be taken to eliminate such exposure to ensure appropriate children's development. This work is available in Open Access model and licensed under a CC BY-NC 3.0 PL license.
    Full-text · Article · Jul 2015 · International Journal of Occupational Medicine and Environmental Health
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    • "The results of the studies on low or moderate exposure to alcohol are inconsistent. In some of the studies maternal alcohol intake during pregnancy was associated with a reduced child psychomotor development and behavioural problems343536, whereas other indicated no effect37383940414243. The crucial aspect, which needs to be considered, is valid exposure assessment. "
    [Show abstract] [Hide abstract] ABSTRACT: Nowadays special attention is paid to prenatal exposures to maternal lifestyle factors and their impact on a child development. The objective of this study was to evaluate the impact of modifiable maternal lifestyle factors on child neurodevelopment based on the Polish Mother and Child Cohort study. The current analysis included 538 mother-child pairs. The following factors related to maternal lifestyle were considered: smoking and environmental tobacco smoke (ETS) exposure (based on the cotinine level in maternal saliva measured using LC-ESI+MS/MS method), alcohol consumption and leisure-time physical activity (LTPA) in pregnancy, pre-pregnancy BMI, and folic acid supplementations before and during pregnancy based on questionnaire data. Psychomotor development was assessed in children at the ages of one and two by the Bayley Scales of Infant and Toddler Development. Significant association was observed between prenatal exposure to tobacco constituents and a decreased child motor development in assessments performed at both ages (β=-0.8, p=0.01; β=-1.4, p<0.001). Maternal pre-pregnancy underweight was associated with decreased language abilities at 12months of age (β=-5.2, p=0.01) and cognitive and motor development at 24months of age, for which the associations were of borderline significance (p=0.06). The recommended level of LTPA during pregnancy was beneficial for child language development at two years of age (β=4.8, p=0.02). For alcohol and folic acid consumption there were no significant associations with any of the analyzed domains of child neurodevelopment. Children prenatally exposed to tobacco compounds and those of underweight mothers had a decreased psychomotor development. The recommended level of LTPA during pregnancy had positive impact on child development. These results underscore the importance of policies and public health interventions promoting healthy lifestyle among women in reproductive age and during pregnancy. Copyright © 2015 Elsevier Ireland Ltd. All rights reserved.
    Full-text · Article · Apr 2015 · Early human development
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