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Evidence is conflicting regarding the relationship between low maternal alcohol consumption and birth outcomes. This paper aimed to investigate the association between alcohol intake before and during pregnancy with birth weight and gestational age and to examine the effect of timing of exposure. A prospective cohort in Leeds, UK, of 1303 pregnant women aged 18-45 years. Questionnaires assessed alcohol consumption before pregnancy and for the three trimesters separately. Categories of alcohol consumption were divided into ≤2 units/week and >2 units/week with a non-drinking category as referent. This was related to size at birth and preterm delivery, adjusting for confounders including salivary cotinine as a biomarker of smoking status. Nearly two-thirds of women before pregnancy and over half in the first trimester reported alcohol intakes above the Department of Health (UK) guidelines of ≤2 units/week. Associations with birth outcomes were strongest for intakes >2 units/week before pregnancy and in trimesters 1 and 2 compared to non-drinkers. Even women adhering to the guidelines in the first trimester were at significantly higher risk of having babies with lower birth weight, lower birth centile and preterm birth compared to non-drinkers, after adjusting for confounders (p<0.05). We found the first trimester to be the period most sensitive to the effect of alcohol on the developing fetus. Women adhering to guidelines in this period were still at increased risk of adverse birth outcomes. Our findings suggest that women should be advised to abstain from alcohol when planning to conceive and throughout pregnancy.
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Maternal alcohol intake prior to and during
pregnancy and risk of adverse birth outcomes:
evidence from a British cohort
Camilla Nykjaer,
1
Nisreen A Alwan,
1
Darren C Greenwood,
2
Nigel A B Simpson,
3
Alastair W M Hay,
4
Kay L M White,
4
Janet E Cade
1
1
Nutritional Epidemiology
Group, School of Food Science
and Nutrition, University of
Leeds, Leeds, UK
2
Division of Biostatistics,
Centre for Epidemiology and
Biostatistics, University of
Leeds, Leeds, UK
3
Department of Obstetrics and
Gynaecology, University of
Leeds, Leeds, UK
4
Epidemiology, LIGHT Institute,
University of Leeds, Leeds, UK
Correspondence to
Camilla Nykjaer,
Nutritional Epidemiology
Group, School of Food Science
and Nutrition, University of
Leeds, Leeds LS2 9JT, UK;
c.nykjaer@leeds.ac.uk
Received 4 June 2013
Revised 10 December 2013
Accepted 23 December 2013
To cite: Nykjaer C,
Alwan NA, Greenwood DC,
et al.J Epidemiol
Community Health Published
Online First: [please include
Day Month Year]
doi:10.1136/jech-2013-
202934
ABSTRACT
Background Evidence is conicting regarding the
relationship between low maternal alcohol
consumption and birth outcomes. This paper aimed to
investigate the association between alcohol intake
before and during pregnancy with birth weight and
gestational age and to examine the effect of timing
of exposure.
Methods A prospective cohort in Leeds, UK, of
1303 pregnant women aged 1845 years.
Questionnaires assessed alcohol consumption before
pregnancy and for the three trimesters separately.
Categories of alcohol consumption were divided into
2 units/week and >2 units/week with a non-
drinking category as referent. This was related to size
at birth and preterm delivery, adjusting for
confounders including salivary cotinine as a biomarker
of smoking status.
Results Nearly two-thirds of women before
pregnancy and over half in the rst trimester reported
alcohol intakes above the Department of Health (UK)
guidelines of 2 units/week. Associations with birth
outcomes were strongest for intakes >2 units/week
before pregnancy and in trimesters 1 and 2 compared
to non-drinkers. Even women adhering to the
guidelines in the rst trimester were at signicantly
higher risk of having babies with lower birth
weight, lower birth centile and preterm birth
compared to non-drinkers, after adjusting for
confounders (p<0.05).
Conclusions We found the rst trimester to be the
period most sensitive to the effect of alcohol on the
developing fetus. Women adhering to guidelines in
this period were still at increased risk of adverse birth
outcomes. Our ndings suggest that women should
be advised to abstain from alcohol when planning to
conceive and throughout pregnancy.
INTRODUCTION
Alcohol was conrmed as a teratogen in the late 1970s
after observations made in France and the USA in
infants born to alcoholic mothers.
12
Evidence regard-
ing the damaging effects of heavy drinking in preg-
nancy is now well established. However, there is a lack
of consensus regarding the impact of low intakes on
adverse birth outcomes such as preterm birth and
small for gestational age (SGA), with studies reporting
a wide range and even a protective effect of low
intakes in reviews of the evidence.
310
This is reected
in the different country-level policies regarding
alcohol consumption during pregnancy and
highlighted in a recent review by OLeary et al on
alcohol policies in English-speaking countries.
11
Some, such as the USA, recommend abstinence.
12
Others advise abstinence but state that small amounts
of alcohol are unlikely to cause harm.
13
In the UK, the
Department of Health (DH) recommends that preg-
nant women and women trying to conceive should
avoid alcohol altogether and never drink more than
12 units once or twice a week.
14
The National
Institute for Health and Care Excellence (NICE) add-
itionally emphasises the advice to avoid drinking
alcohol in the rst 3 months of pregnancy as this may
be associated with an increased risk of miscarriage.
15
According to the UK Health Survey 2011, 52% of
women of childbearing age who drink exceed the
daily limit of 23 units per day and 25% drink more
than twice the recommendations.
16
Resu lt s from the
most recent UK Infant Feeding Survey (IFS) which
included data from over 15 000 women, showed that
40% drank alcohol during pregnancy but only 3%
drank more than 2 units per week.
17
Data suggest that over 40% of pregnancies in the
UK are unplanned.
18 19
With such high rates of
unplanned pregnancies and excess drinking, early
pregnancy is likely to be the period of highest
intake for women who are unaware of their preg-
nancy, and this could put them and their unborn
baby at risk.
Alcohol crosses the placenta and results in nearly
equal concentrations in the mother and fetus. The
mechanisms whereby alcohol affects fetal growth
and development are complex as these are staged
processes, and the sensitivity of the fetus to alcohol
will likely depend on the timing of the exposure.
6
Few studies have taken into account the effect of
timing of alcohol exposure on birth outcomes.
Examination of alcohol consumption before preg-
nancy and for all trimesters separately showed con-
icting results as to which period is most sensitive;
some studies found an association between alcohol
intake and SGA and preterm birth at all levels of
exposure, while others suggested no association
even at high levels of intake.
2023
The aims of this paper were to investigate the
relationship between maternal alcohol intake
during pregnancy with both birth weight and gesta-
tional age, and to assess whether these relationships
differed by timing of exposure during pregnancy.
We also aimed to investigate the effect of maternal
drinking prior to pregnancy on birth outcomes.
This was accomplished using data from a prospect-
ive cohort.
Nykjaer C, et al.J Epidemiol Community Health 2014;0:18. doi:10.1136/jech-2013-202934 1
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JECH Online First, published on March 10, 2014 as 10.1136/jech-2013-202934
Copyright Article author (or their employer) 2014. Produced by BMJ Publishing Group Ltd under licence.
METHODS
Study design, participants and data collection
The Caffeine and Reproductive Health (CARE) Study was a
prospective study into maternal diet and birth outcomes.
Between 2003 and 2006, low risk pregnant women aged 1845
were prospectively recruited from the Leeds Teaching Hospitals
Trust. The study methodology has been described in detail else-
where.
24
Women were excluded if they had any concurrent
medical disorders, psychiatric illness, HIV infection or hepatitis
B infection. A total of 5959 women were considered, of whom
4571 met the eligibility criteria. Eligible women were sent
detailed information about the study and 1374 consented to
participate. The study was approved by the Leeds West Local
Research Ethics Committee (ref 03/054).
Assessment of alcohol consumption and diet
Alcohol intake was assessed throughout pregnancy using a food
frequency approach adapted from the UK Womens Cohort
Study administered at enrolment (1218 weeks gestation), week
28 and postpartum (weeks 4650).
25
Consumption was assessed
for 4 weeks prior to pregnancy through to week 12 of gestation,
weeks 1328 and weeks 2940. Participants were asked how
often (never, less than once/month, 13 times/month, once/
week, 24 times/week, 56 times/week, once/day, 23 times/day,
45 times/day and >6 times/day) they consumed different types
of alcohol (wine, beer/lager/stout, cider, port/sherry/liqueurs,
vodka kick and spirits). Frequency of alcohol consumption
derived from the questionnaires was converted to times per
week, which was then multiplied by the units of alcohol in each
of the alcoholic beverages listed on the questionnaire to obtain
weekly consumption in units for each of the time periods. For
wine, the units of alcohol per portion for each type of alcoholic
beverage was 2.3 for beer, 2.0 for cider, 1.0 for port and spirits,
and 1.5 for vodka kick. This is in accordance with the conver-
sion factors used since 2006 in the Health Survey of England,
one unit of alcohol equating to 10 mL by volume or 8 g by
weight.
16
Dietary intake was reported on a 24 h dietary recall question-
naire administered by a research midwife at 16 weeks gestation.
Daily total energy intake was derived from the reported food
intake.
Assessment of outcomes
Information on birth outcomes was obtained from hospital
maternity records. The primary outcome assessed was size at
birth, recorded as grams, as well as customised birth centiles
which took into account maternal height, weight, ethnicity,
parity, neonatal birth weight and sex.
26
The relationship with
preterm delivery (<37 weeks gestation) and SGA (<10th
centile) was also investigated.
Assessment of participant characteristics
Salivary cotinine levels were measured at enrolment using
ELISA (Cozart Bioscience, Abingdon, UK). Participants were
classied on the basis of cotinine concentrations as active
smokers (>5 ng/mL), passive smokers (15 ng/mL) or non-
smokers (<1 ng/mL).
27
Maternal characteristics such as pre-pregnancy weight, height,
age, ethnicity (European, Asian, Afro-Caribbean, African,
Mixed/Other origin), parity (0, 1, 2, 3, 4+), caffeine intake and
maternal education (none, O-level, A-level, degree) were
obtained via a self-reported questionnaire administered at
enrolment.
Statistical power calculation
Comparison of birth weight between non-drinkers and drinkers
and the SD of birth weight identied in the study (SD=576 g)
demonstrated that the study had 85% power to detect a differ-
ence of just over 100 g in birth weight for a two-sided t test at
p<0.05 in trimester 1.
Statistical methods
Analysis was undertaken using the continuous weekly alcohol
variable divided into categories of intake based on the DH
(2008) guidelines of no more than 2 units/week with the inclu-
sion of a non-drinking category which was used as the reference
group (0 units/week, 2 units/week and >2 units/week).
Univariable analyses were performed using one-way ANOVA
for normally distributed outcomes and the KruskalWallis test
otherwise. The χ
2
test was used for categorical outcomes.
Data were further analysed using multivariable linear regres-
sion for continuous outcomes and multivariable logistic regres-
sion for binary outcomes. Maternal pre-pregnancy weight,
height, parity, ethnicity, gestation and babys sex were taken into
account when calculating the customised birth centile and were
adjusted for in the model for birth weight and preterm delivery.
Further statistical adjustment was made, based on a priori
knowledge from the literature, for maternal age, salivary coti-
nine levels, caffeine intake and maternal education (as a proxy
for socioeconomic status). Because of the possible correlation
between alcohol consumption and energy intake, energy intake
obtained from the 24 h recalls was included in the model, as it
was important to distinguish between the separate effects of
alcohol and energy intake on birth outcomes.
28
Extreme values
for energy intake (1% highest and 1% lowest) were excluded
based on the method proposed by Meltzer et al.
29
The robust-
ness of the results to excluding women with conditions known
to predispose to adverse birth outcomes, including a previous
low birthweight (LBW) baby, gestational diabetes and gestational
hypertension, as well as women of childbearing age who were
risky drinkers(dened by the Centers for Disease Control
and Prevention as those consuming more than 7 US drinks per
week, corresponding to 10 UK units
30
) was also assessed.
All analyses were carried out using Stata V.12 (Stata, College
Station, Texas, USA).
RESULTS
A total of 1303 women were recruited, and of these 1294 had
data available on birth outcomes. Five women had terminations
and were therefore excluded from this analysis. An additional
25 women were excluded due to extreme energy intakes (the
1% highest and 1% lowest intakes).
Alcohol intake
Of the remaining 1264 women, 1153 (91%), 1135 (90%), 793
(66%) and 377 (30%) completed the questions on alcohol
intake before pregnancy, and during the 1st trimester, 2nd tri-
mester and 3rd trimester, respectively (table 1). Alcohol intakes
before pregnancy and in the rst trimester were signicantly
higher (p<0.0001) than in the 2nd and 3rd trimesters (11.2,
4.0, 1.8 and 1.9 units/week, respectively). The prevalence of
women consuming more than 2 units per week was highest
before pregnancy (74%) and in the 1st trimester (53%), with
mean intakes for women reaching 15.1 units (95% CI 14.1 to
16.1) and 7.2 units (95% CI 6.6 to 7.9) per week, respectively.
The prevalence of risky drinkerswas relatively low at 11%,
2% and 3% for trimesters 1, 2 and 3, respectively, but much
2 Nykjaer C, et al.J Epidemiol Community Health 2014;0:18. doi:10.1136/jech-2013-202934
Research report
higher before pregnancy, with 38% of women consuming more
than 10 units/week.
Characteristics of women according to categories of alcohol
intake
Table 2 shows the characteristics of participants according to
alcohol consumption. Women with alcohol intakes above 2
units per week were more likely to be older, have a university
degree and be of European origin and less likely to live in an
area within the most deprived Index of Multiple Deprivation
(IMD) quartile. These characteristics were consistent across all
trimesters. However, in trimester 1, women in the high con-
sumption category were also more likely to have a higher total
energy intake compared to the other two categories and to have
no children. Apart from differences in energy intake, the same
differences between the women seen in trimester 1 were also
true for the 4 weeks before pregnancy (results not shown).
Birth outcomes
Of the 1264 women with information on birth outcomes, 166
(13.1%) babies weighed less than the 10th centile. Fifty-seven
(4.4%) were LBW (<2500 g) and 54 (4.3%) were delivered
preterm (<37 weeks gestation).
Relationship between alcohol intake and size at birth
There was a strong association between alcohol intake before
pregnancy and birth weight and birth centile after adjustments
for maternal pre-pregnancy weight, height, parity, ethnicity, ges-
tation, babys sex, maternal age, salivary cotinine levels, caffeine
intake and maternal education (table 3). Women who adhered
to the guidelines were not at increased risk, but compared to
non-drinkers, alcohol intakes of >2 units/week were associated
with a 7.7 (95% CI 12.8 to 2.6) decrease in customised
birth centile (adjusted p
trend
=0.009).
For consumption during pregnancy, after adjustments, alcohol
consumption was associated with an approximately 100 g reduc-
tion in birth weight for women consuming >2 units/week in tri-
mester 1 (p
trend
=0.007). Compared to non-drinkers, alcohol
intakes of <2 units/week and >2 units/week in trimester 1 were
associated with an adjusted 5.8 (95% CI 10.8 to 0.7) and a
8.2 (95% CI 12.6 to 3.7) decrease in customised birth
centile, respectively (p
trend
=0.002). The adjusted ORs for SGA
were 1.7 (95% CI 0.9 to 3.1) for intakes <2 units/week and 2.0
(95% CI 1.2 to 3.4) for intakes >2 units/week in trimester 1
(p
trend
=0.03) compared to non-drinkers. These associations
were attenuated in trimester 2 and 3.
Relationship between alcohol intake and preterm birth
Compared to non-drinkers in trimester 1, the adjusted OR for
having a preterm baby were 4.6 (95% CI 1.4 to 14.7) for
intakes <2 units/week and 3.5 (1.1 to 11.2) for intakes >2
units/week (table 4). For the 4 weeks before pregnancy (table 3)
and in trimesters 2 and 3 (table 4), the association was
non-signicant.
Sensitivity analysis
Including total energy intake in the model further strengthened
the association between maternal alcohol intakes during preg-
nancy and birth outcomes; however, it did not inuence results
for intakes before pregnancy.
Excluding women with high risk pregnancies (n=182) and
risky drinkersdid not alter the results, although the CIs
became wider due to the reduction in numbers (results not
shown).
DISCUSSION
This is one of very few prospective studies
2023 31 32
and the
rst in a British cohort which has looked at alcohol exposures
before pregnancy and in each of the trimesters separately, and
their association with adverse birth outcomes. Maternal alcohol
intake during the rst trimester was found to have the strongest
association with fetal growth and gestational age. Women who
adhered to guidelines in this period were still at increased risk
of adverse birth outcomes even after adjustment for known risk
factors. Maternal alcohol intakes which exceeded the recom-
mendations in the period leading up to pregnancy were also
found to be associated with fetal growth, suggesting that the
peri-conceptual period could be particularly sensitive to the
effects of alcohol on the fetus. Our results highlight the need
for endorsing the abstinence-only message, and further illumin-
ate how timing of exposure is important in the association of
alcohol with birth outcomes, with the rst trimester being the
most vulnerable period.
Alcohol intake and maternal characteristics
As expected, intakes of alcohol were highest in the 4 weeks
before pregnancy, with decreasing levels observed as pregnancy
progressed. The proportion of women drinking during preg-
nancy (79%, 63% and 49% for trimesters 1, 2 and 3, respect-
ively) was considerable higher than reported from the IFS.
17
IFS
data, however, were collected postpartum and are therefore
subject to under-reporting. The characteristics of drinking
mothers in our study are consistent with those observed in the
IFS where mothers aged 35 or over, from managerial and pro-
fessional occupations and from a white ethnic background were
more likely to drink during pregnancy.
17
Despite the high
Table 1 Self-reported alcohol intake among pregnant women in
the CARE study
Characteristic n (% total sample) Mean 95% CI
Alcohol intake (units/week)*
4 Weeks before pregnancy 1153 (100.0) 11.2 10.4 to 12.1
First trimester 1135 (98.4) 4.0 3.6 to 4.4
Second trimester 793 (68.8) 1.8 1.6 to 2.0
Third trimester 377 (32.7) 1.9 1.5 to 2.3
Categories of intake 4 weeks before pregnancy
Non-drinkers 157 (13.6) 0 0
2 Units/week 148 (12.8) 0.9 0.9 to 1.1
>2 Units/week 848 (73.6) 15.1 14.1 to 16.1
Categories of intake trimester 1
Non-drinkers 243 (21.4) 0 0
2 Units/week 292 (25.7) 0.8 0.7 to 0.8
>2 Units/week 600 (52.9) 7.2 6.6 to 7.9
Categories of intake trimester 2
Non-drinkers 291 (36.7) 0 0
2 Units/week 278 (35.1) 0.8 0.8 to 0.9
>2 Units/week 224 (28.3) 5.4 4.8 to 5.9
Categories of intake trimester 3
Non-drinkers 193 (51.2) 0 0
2 Units/week 80 (21.2) 0.9 0.8 to 1.0
>2 Units/week 104 (27.6) 6.3 5.2 to 7.3
*1 unit of alcohol is 10 mL by volume or 8 g by weight of pure alcohol.
Categories based on the Department of Health (2008) weekly recommendations of
no more than 2 units/week.
14
CARE, Caffeine and Reproductive Health.
Nykjaer C, et al.J Epidemiol Community Health 2014;0:18. doi:10.1136/jech-2013-202934 3
Research report
Table 2 Characteristics of mothers by alcohol intake during pregnancy reported in three questionnaires*
First trimester (n=1135) Second trimester (n=808) Third trimester (n=384)
Non-drinkers 2 Units/week >2 Units/week
p Value
Non-drinkers 2 Units/week >2 Units/week
p Value
Non-drinkers 2 Units/week >2 Units/week
p Value(n=243) (n=298) (n=594) (n=300) (n=282) (n=226) (n=197) (n=82) (n=105)
Age (years), mean (95% CI) 29.4 (28.7 to 30.1) 29.5 (28.9 to 30.1) 30.5 (30.1 to 30.9) 0.002 28.9 (28.3 to 29.5) 30.7 (30.2 to 31.3) 31.8 (31.2 to 32.3) <0.0001 28.5 (27.8 to 29.3) 30.8 (29.9 to 31.7) 30.7 (29.8 to 31.6) 0.0005
Pre-pregnancy BMI (kg/m
2
),
mean (95% CI)
25.0 (24.4 to 25.7) 24.7 (24.1 to 25.3) 24.5 (24.1 to 24.9) 0.5 25.1 (24.4 to 25.8) 24.5 (23.9 to 25.0) 23.9 (23.3 to 24.4) 0.1 25.5 (24.6 to 26.4) 24.0 (23.0 to 25.0) 23.9 (23.2 to 24.8) 0.1
Total energy intake (kcal),
mean (95% CI)
2060 (1778 to 2136) 2079 (2012 to 2146) 2162 (2111 to 2213) 0.04 2075 (2007 to 2144) 2169 (2099 to 2239) 2181 (2097 to 2264) 0.08 2080 (1990 to 2170) 2142 (2013 to 2277) 2156 (2036 to 2276) 0.5
Caffeine intake (mg/day),
mean (95% CI)
176.1 (152.7 to 199.4) 174.2 (153.3 to 195.1) 202.0 (186.3 to 217.8) 0.06 163.0 (139.2 to 186.8) 158.0 (138.8 to 177.3) 175.7 (155.8 to 195.6) 0.009 206.1 (171.4 to 240.9) 223.3 (170.8 to 275.7) 189.4 (158.9 to 219.8) 0.4
Smoker at 12 weeks, % (n) 17.4 (40) 18.3 (53) 14.9 (85) 0.6 14.6 (41) 12.4 (33) 9.6 (21) 0.2 22.7 (42) 18.8 (15) 11.9 (12) 0.2
IMD most deprived quartile, % (n) 37.5 (87) 32.7 (93) 23.3 (134) 0.0001 32.7 (91) 21.4 (58) 16.3 (35) 0.0001 34.1 (63) 25.6 (20) 15.5 (15) 0.003
University degree, % (n) 34.6 (84) 39.3 (117) 43.6 (259) 0.05 35.1 (102) 49.1 (137) 51.6 (115) 0.0002 28.5 (55) 40.0 (32) 50.9 (53) 0.0001
European origin, % (n) 85.5 (206) 94.9 (283) 98.2 (582) 0.0001 92.0 (266) 96.8 (270) 99.1 (220) 0.001 94.8 (181) 96.3 (77) 99.0 (102) 0.4
Primigravida, % (n) 36.6 (89) 43.7 (119) 53.8 (317) 0.0001 52.4 (152) 49.8 (138) 47.9 (107) 0.6 52.1 (100) 47.5 (38) 56.7 (59) 0.5
Preterm labour, % (n) 2.1 (5) 6.0 (18) 4.7 (28) 0.08 5.2 (15) 3.9 (11) 4.5 (10) 0.8 7.3 (14) 7.5 (6) 5.8 (6) 0.9
Pre-eclampsia, % (n) 5.8 (14) 5.1 (15) 4.0 (28) 0.8 5.9 (17) 7.3 (20) 2.3 (5) 0.05 7.5 (14) 5.1 (4) 2.9 (3) 0.3
Past history of miscarriage, % (n) 26.3 (63) 22.4 (66) 22.3 (133) 0.5 27.2 (78) 23.1 (64) 22.1 (49) 0.3 23.2 (44) 17.5 (14) 23.5 (24) 0.5
*Division of alcohol intake is based on the Department of Health (2008) weekly recommendations of no more than 2 units/week.
14
p Value using one-way ANOVA for normally distributed and KruskalWallis test for non-normally distributed continuous variables, and the χ
2
test and Fishers exact test for categorical variables. Significant difference at p<0.05.
BMI, body mass index; IMD, Index of Multiple Deprivation.
4 Nykjaer C, et al.J Epidemiol Community Health 2014;0:18. doi:10.1136/jech-2013-202934
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prevalence of drinking in our cohort, very few women were
considered risky drinkers. The low level of intake could in part
be explained by under-reporting, a common phenomenon in
alcohol assessment.
6
Reported alcohol consumption in surveys
only accounts for approximately 60% of total alcohol sales and
a recent study found evidence that excess alcohol drinking in
the UK may be higher than previously thought.
33
The actual
level of intake may therefore be higher than reported, and asso-
ciations with adverse birth outcomes could be with higher levels
of intake.
Timing of exposure and birth outcomes
We found consistently adverse associations between intakes of
alcohol above 2 units/week prior to pregnancy and in the 1st
and 2nd trimester and birth weight. In a prospective US cohort
study, a reduction in birth weight was found in women drinking
more than 2 units/week across all trimesters.
32
However, the
numbers were small once divided into categories of intake, and
the reduction was not signicant with very wide CIs.
We found a signicant twofold increase in the odds of babies
being born SGA to mothers drinking more than 2 units/week
compared to non-drinkers in trimester 1. OLeary et al reported
signicantly increased odds of infants being born SGA to
women drinking up to 60 g alcohol/week (7.5 UK units)
3 months prior to pregnancy, an association, however, which
was not observed at higher levels of alcohol or for consumption
during pregnancy.
22
Two studies
21 31
found an elevated risk of
babies being born SGA to drinking mothers, but the threshold
of intake was much higher than observed in our study.
Chiaffarino et al reported signicantly increased odds of a baby
being born SGA at daily intakes above 3 units compared to
abstainers across all trimesters and before pregnancy, but the
association was strongest for intakes in trimester 1.
21
Feldman
et al found a doseresponse relationship with a 16% increase
for reduced birth weight for every one drink increase per day in
the second half of trimester 1 and for all of trimester 2.
31
We found an elevated risk of preterm birth in drinkers com-
pared to abstainers in trimester 1 only. This is comparable to
ndings reported by other studies.
22 23
However, the threshold
of increased risk was much higher than that observed in our
study. In contrast, a recent study found a decreased risk in
women consuming up to three drinks per week compared to
abstainers in the third trimester.
20
The differences between our ndings and those of other
studies are partly due to heterogeneity between studies; in par-
ticular, we looked at very low intakes of alcohol and their
associations with birth outcomes. Where studies have found
similar associations, this has been in relation to a much higher
intake.
We have included studies which accounted for timing of
exposure, but the methodology of studies differed greatly. None
used the same method of alcohol assessment. In addition, the
period before pregnancy was not specied in some studies,
21 23
and for others, numbers were very small in the higher categories
of intake, limiting their power to detect a true association.
21 22 32
Moreover, choice of confounders was also highly inconsistent
across studies; in our study, for example, we adjusted for coti-
nine levels and energy intake, both of which have not been
adjusted for in previous research. Additionally, inconsistency in
ndings between countries may be a reection of differences in
drinking patterns. Finally, differences could also be due to poly-
morphisms linked to the metabolism of alcohol,
34
which may
vary between populations. This heterogeneity makes it hard to
compare results.
Table 3 The relationship between maternal alcohol intake 4 weeks before pregnancy and size at birth and preterm delivery (n=1152)
Unadjusted change (95% CI) p Value* Adjusted change(95% CI) p Value*
Birth weight (g)
Non-drinkers 0.0 0.9 0.0 0.03
2 Units/week 14.6 (147.4 to 118.1) 70.2 (167.4 to 26.9)
>2 Units/week 23.2 (123.6 to 77.1) 105.7 (183.5 to 27.9)
Customised birth centile
Non-drinkers 0.0 0.1 0.0 0.009
2 Units/week 2.8 (9.4 to 3.9) 4.2 (10.9 to 2.4)
>2 Units/week 4.9 (9.9 to 0.1) 7.7 (12.8 to 2.6)
Unadjusted OR (95% CI) p Value*Adjusted OR(95% CI) p Value*
SGA (<10th centile)
Non-drinkers 1.0 0.5 1.0 0.2
2 Units/week 1.4 (0.7 to 2.7) 1.7 (0.8 to 3.5)
>2 Units/week 1.4 (0.8 to 2.3) 1.8 (0.9 to 3.2)
Low birth weight (2500 g)
Non-drinkers 1.0 0.5 1.0 0.4
2 Units/week 0.6 (0.2 to 1.7) 0.4 (0.1 to 2.7)
>2 Units/week 0.9 (0.4 to 2.2) 1.1 (0.2 to 6.1)
Preterm birth (<37 weeks gestation)
Non-drinkers 1.0 0.9 1.0 0.5
2 Units/week 1.4 (0.7 to 2.7) 1.7 (0.6 to 6.4)
>2 Units/week 1.4 (0.8 to 2.3) 2.0 (0.7 to 6.2)
*p For trend for categories of alcohol intake.
Adjusted for maternal pre-pregnancy weight, height, age, parity, ethnicity, salivary cotinine levels, caffeine intake, education, energy intake, gestation and babys sex in a multivariable
linear regression for continuous outcomes and a multivariable logistic regression for categorical outcomes.
Takes into account maternal pre-pregnancy weight, height, parity, ethnicity, gestation and babyssex.
SGA, small for gestational age.
Nykjaer C, et al.J Epidemiol Community Health 2014;0:18. doi:10.1136/jech-2013-202934 5
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Table 4 The relationship between maternal alcohol intake during pregnancy and size at birth and preterm delivery
Trimester 1 (n=1135) Trimester 2 (n=793) Trimester 3 (n=377)
Unadjusted change
(95% CI) p Value*
Adjusted change
(95% CI) p Value*
Unadjusted change
(95% CI) p Value*
Adjusted change
(95% CI) p Value*
Unadjusted change
(95% CI) p Value*
Adjusted change
(95% CI) p Value*
Birth weight (g)
Non-drinkers 0.0 0.02 0.0 0.007 0.0 0.5 0.0 0.04 0.0 0.6 0.0 0.6
2 Units/week 124.8 (225.4 to 24.3) 98.5 (170.9 to 26.1) 51.3 (42.5 to 145.0) 37.6 (108.1 to 32.8) 4.2 (162.4 to 170.7) 34.5 (153.1 to 84.1)
>2 Units/week 105.9 (193.9 to 17.9) 100.4 (165.8 to 34.9) 12.9 (56.5 to 112.2) 99.6 (175.8 to 22.3) 73.7 (78.6 to 226.1) 50.4 (161.2 to 60.3)
Customised birth centile
Non-drinkers 0.0 0.01 0.0 0.002 0.0 0.5 0.0 0.06 0.0 0.8 0.0 0.7
2 Units/week 4.1 (9.1 to 0.9) 5.8 (10.8 to 0.7) 1.4 (6.3 to 3.5) 3.6 (8.6 to 1.4) 1.4 (9.4 to 6.6) 3.1 (11.1 to 4.9)
>2 Units/week 6.7 (11.1 to 2.3) 8.2 (12.6 to 3.7) 2.9 (8.2 to 2.2) 6.4 (11.8 to 1.1) 1.2 (6.1 to 8.5) 1.8 (9.3 to 5.7)
Unadjusted OR
(95% CI) p Value*
Adjusted OR
(95% CI) p Value*
Unadjusted
OR (95% CI) p Value*
Adjusted OR
(95% CI) p Value*
Unadjusted OR
(95% CI) p Value*
Adjusted OR
(95% CI) p Value*
SGA (<10th centile)
Non-drinkers 1.0 0.08 1.0 0.03 1.0 0.2 1.0 0.2 1.0 0.9 1.0 0.7
2 Units/week 1.4 (0.8 to 2.5) 1.7 (0.9 to 3.1) 0.7 (0.4 to 1.0) 0.8 (0.5 to 1.3) 0.9 (0.5 to 1.5) 0.9 (0.5 to 1.6)
>2 Units/week 1.7 (1.1 to 2.8) 2.0 (1.2 to 3.4) 0.9 (0.6 to 1.5) 1.2 (0.8 to 2.1) 0.9 (0.6 to 1.6) 1.2 (0.7 to 2.1)
Low birth weight (2500 g)
Non-drinkers 1.0 0.20 1.0 0.8 1.0 0.4 1.0 0.7 1.0 0.7 1.0 0.7
2 Units/week 0.4 (0.2 to 1.0) 1.6 (0.3 to 7.4) 1.4 (0.7 to 2.8) 0.7 (0.2 to 2.9) 1.1 (0.5 to 2.4) 0.3 (0.02 to 4.1)
>2 Units/week 0.6 (0.2 to 1.3) 1.6 (0.4 to 6.4) 1.6 (0.7 to 3.4) 1.5 (0.3 to 8.4) 1.4 (0.6 to 3.2) 1.8 (0.1 to 29.8)
Preterm birth (<37 weeks gestation)
Non-drinkers 1.0 0.08 1.0 0.04 1.0 0.8 1.0 0.8 1.0 0.9 1.0 0.9
2 Units/week 3.1 (1.1 to 8.6) 4.6 (1.4 to 14.7) 0.8 (0.3 to 1.7) 0.8 (0.3 to 1.8) 1.0 (0.4 to 2.8) 1.0 (0.3 to 3.2)
>2 Units/week 2.3 (0.9 to 6.1) 3.5 (1.1 to 11.2) 0.9 (0.4 to 1.9) 0.9 (0.43 to 2.1) 0.8 (0.3 to 2.1) 1.0 (0.3 to 2.9)
*p For trend for categories of alcohol intake in a multivariable linear regression for continuous outcomes and a multivariable logistic regression for categorical outcomes.
Adjusted for maternal pre-pregnancy weight, height, age, parity, ethnicity, salivary cotinine levels, caffeine intake, education, energy intake, gestation and babys sex in a multivariable linear regression for continuous outcomes and a multivariable logistic
regression for categorical outcomes.
Takes into account maternal pre-pregnancy weight, height, parity, ethnicity, gestation and babyssex.
SGA, small for gestational age.
6 Nykjaer C, et al.J Epidemiol Community Health 2014;0:18. doi:10.1136/jech-2013-202934
Research report
Methodological considerations
Alcohol intake was averaged to weekly consumption and then
divided into categories. This was done so as to better reect the
current UK guidelines on alcohol consumption for pregnant
women and women trying to conceive, and to make the results
more applicable in a public health context. Although this pre-
vented us looking at associations with patterns of intake, such as
binge drinking, the number of risky drinkers was very low and
we would have had little power to detect a true association.
Furthermore, the categories included a non-drinking referent
and compared low levels of drinking, which is appropriate in a
moderate to low drinking population. Units and their alcohol
content were clearly dened in our study. Serving sizes and the
alcohol content of drinks, however, may differ between
mothers. The calculation of alcoholic content of beverages was
in line with the alcoholic prole of beers, wine and spirits at the
time of data collection, a detail often omitted in other studies.
31
This is important to prevent exposure misclassication which
may obscure any relationship with birth outcomes as the alcohol
prole of beverages is known to change over time.
16
A major strength of this study is the objective measurement of
smoking, one of the biggest confounders in the relationship
between alcohol and adverse birth outcomes, by using cotinine
as a biomarker.
Considering timing of exposure is important so that variation
in alcohol consumption throughout pregnancy can be identied.
Moreover, the timing of exposure will affect birth outcomes dif-
ferently as fetal development is a staged process and, for this
reason, according to Day and Richardson,
35
drinking measures
should be at least trimester specic. A major strength of this
study was the assessment of intake at three time points covering
several windows of exposure. Recent reviews have shown that
many studies fail to account for timing of exposure, which is
likely one of the causes of the contradictory evidence surround-
ing alcohol intake and birth outcomes.
7910
This study was designed for the assessment of caffeine intake
and not alcohol consumption. However, the questionnaire was
validated with reference to caffeine intake
36
and is comparable
to other methods used in the assessment of alcohol. Despite
intakes being self-reported and thus presenting the issue of
under-reporting, alcohol exposure was assessed prospectively in
trimesters 1 and 2, reducing the potential for differential meas-
urement (recall) bias. Ideally, alcohol intake should have been
validated using a biomarker, but as yet, there are no biomarkers
which can adequately assess low alcohol intakes and identify
patterns of intake.
37
Another limitation is the low sample size observed in the 3rd tri-
mester. The original study of caffeine and birth outcomes planned
to follow up women several weeks after delivery to investigate
how their caffeine metabolism had returned to normal, using a caf-
feine challenge. This proposed data collection was expensive. To
reduce costs without introducing selection bias, all cases (SGA and
LBW infants) were recruited for postpartum follow-up, but only a
sample of controls, taken to be the next two births that were not
SGA or LBW. We found little difference between the controls who
completed follow-up compared to those who did not, apart from
the fact that women who stayed in the study were less likely to live
in a deprived area (22% compared to 29% in non-completers,
data not shown).
Despite the limitations discussed, the potential risk to the
fetus presented by even low maternal alcohol intakes prior to
and during pregnancy warrants further investigation. Future
studies should also take into account timing of exposure,
including the period leading up to pregnancy. Maternal alcohol
consumption usually decreases throughout pregnancy, as shown
in our study, and therefore, averaging exposure measured at one
time point in pregnancy to reect exposure across the whole of
pregnancy may obscure any true associations.
CONCLUSION
This analysis of prospectively collected data of a British cohort
has demonstrated that low levels of maternal alcohol consump-
tion, in particular in the rst trimester, have a negative associ-
ation with fetal growth and gestational age and greatly increase
the odds of babies being born SGA and preterm. Pregnant
women and women planning to become pregnant should be
advised to abstain from drinking, as even those women who
adhered to the UK guidelines of 12 units once or twice a week
in the rst trimester were at risk of having babies with reduced
birth weight and born preterm when compared to mothers who
abstained from alcohol.
What is already known on this subject
Alcohol is a known teratogen.
There is a lack of consensus in the evidence regarding the
level and timing of maternal alcohol consumption during
pregnancy that is considered to be safe.
This lack of consensus is reected in the different
country-level policies regarding alcohol consumption during
pregnancy.
What this study adds
This study measured alcohol intake at four time points,
before pregnancy and in trimesters 1, 2 and 3.
The association with adverse birth outcomes was strongest
in trimester 1, where there was a twofold increase in the
odds of babies being born small for gestational age to
mothers drinking more than 2 units/week compared to
non-drinkers.
A similar association was observed for preterm birth, where
even women who adhered to the Department of Health
guidance limiting alcohol to no more than 2 units per week
were at risk of having babies born preterm compared to
women who abstained from alcohol.
Policy implications
Public health messages about abstaining from alcohol when
pregnant and planning to conceive need to be promoted.
Acknowledgements We would like to acknowledge the women participating in
this study and the research midwifes for their invaluable contribution, Sinead Boylan
for recruitment and data collection, Susan Shires for laboratory analysis of cotinine
and caffeine levels, and James Thomas and Neil Hancock for database management.
Nykjaer C, et al.J Epidemiol Community Health 2014;0:18. doi:10.1136/jech-2013-202934 7
Research report
Contributors The CARE study was designed by and carried out under the
leadership of JEC and NABS. CN conducted the statistical analysis with assistance
from DCG and NAA and led the drafting of the manuscript. AWMH and KLMW
carried out the laboratory investigations. All authors contributed to subsequent
drafts of the manuscript and have read and approved the nal manuscript.
Funding The CARE study was supported by a grant from the Food Standard
Agency, UK (T01033). Camilla Nykjaers PhD Studentship is jointly funded by the
Medical Research Council (MR/K500914/1) and the Rank Prize Foundation.
Competing interest None.
Ethics approval Leeds West Local Research Ethics Committee approved this study
(ref 03/054).
Provenance and peer review Not commissioned; externally peer reviewed.
Open Access This is an Open Access article distributed in accordance with the
terms of the Creative Commons Attribution (CC BY 3.0) license, which permits
others to distribute, remix, adapt and build upon this work, for commercial use,
provided the original work is properly cited. See: http://creativecommons.org/
licenses/by/3.0/
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Objectives To compare the executive functions in adolescents of fathers with alcohol dependence (AOFADs) with a control group of adolescents without a paternal history of alcohol dependence and examine the association between executive functioning problems and behavioral and emotional problems. Materials and Methods The study included 39 AOFADs and 45 adolescent offspring of fathers without a history of alcohol-use disorders, who were matched for age and sex. They were assessed using standardized measures of executive functions and emotional and behavioral problems. Statistical Analysis A comparison was made between the two groups about the parental report of adolescents' executive functions and adolescents' self-reported emotional and behavioral problems. ANCOVA was performed to understand the covariance of educational and socio-economic status on executive functions. Correlation between executive functions, emotional and behavioral problems, and the duration of father's alcohol dependence was examined with Spearman's rho. Results AOFAD group showed significant impairment on all subdomains of executive functions and emotional and behavioral disturbances (p < 0.01) but not on the prosocial behavioral dimension (p < 0.01). The group differences were independent of child's education and family income. Executive functional impairments positively correlated with psychopathology (p < 0.01). Problems with executive functions and psychopathology correlated with the duration of the father's alcohol dependence. Conclusions AOFADs are at risk for executive function impairments which in turn are strongly associated with emotional and behavioral problems. The association is independent of child's education and family economic status. The duration of alcohol dependence in fathers is associated with these problems. It has implications for targeted interventions for both adolescents and families.
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Global trends demonstrate increasing alcohol consumption among women of childbearing age, social acceptability of women’s alcohol use, as well as recent changes in alcohol use patterns due to the COVID-19 pandemic. Increasing levels of consumption may put many pregnancies at higher risk for prenatal alcohol exposure (PAE), which can cause fetal alcohol spectrum disorder (FASD). Therefore, alcohol use screening of women who are or may become pregnant has become more important than ever and should be a public health priority. The current literature review presents the state of the science on various existing alcohol use screening strategies, including the clinical utility of validated alcohol use screening instruments. It also discusses barriers for decreasing alcohol use in pregnancy, such as low uptake of screening during prenatal care, practitioner beliefs and training/time constraints, unplanned pregnancies, delayed access to prenatal care, and stigma associated with substance use in pregnancy as well as recommendations to address these barriers. By implementing consistent alcohol use screening, health-care providers increase opportunities for pregnant women to access counseling, brief interventions, and referral for treatment. Increased use of these strategies would reduce risk of adverse outcomes to women and their children, decrease new cases of FASD and recurrence of FASD in families, and thus would improve maternal and child health.Key wordsAlcoholPregnancyScreeningFetal alcohol spectrum disorderFetal alcohol syndromePreventionChildbearing aged women
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