Impact of prenatal alcohol exposure on neurodevelopmental outcomes: a systematic review

Figures & data

Table 1. Inclusion/exclusion criteria.

	Inclusion	Exclusion
Population	Pregnant women sampled from the population and their offspring (under the age of 18 years at time of outcome assessment)	Postnatal women Adult off-spring
Exposure	Any level of prenatal alcohol consumption. Must include a quantitative measure of alcohol consumption	Alcohol must be the main exposure, or if multiple exposures, it must be an independently evaluated variable
Comparator	Women that did not consume alcohol in pregnancy.	Studies without a comparator will be excluded
Outcome	Neurodevelopmental outcomes related to FASD: e.g. developmental delay; motor skills/function; neurophysiology; cognition; cognitive development; language; academic achievement; IQ; memory; attention; executive function; affect regulation; behaviour complications; adaptive behaviour; social skills; communication	Studies of unrelated outcomes will be excluded
Study Design	Prospective cohort studies	Retrospective and case-control studies. N > 1000

Figure 1. PRISMA flow chart of included studies.

Table 2. Summary of study outcome characteristics.

Outcome assessed	N	%
Neurodevelopmental domain assessed
Neurophysiology	0	0
Motor Skills	5	16.7
Cognition	11	36.7
Language	3	10.0
Academic achievement	5	16.7
Memory	0	0
Attention	8	26.7
Executive function	3	10.0
Affect regulation	13	43.3
Adaptive behaviour, social skills, or communication	2	6.7
Age at outcome assessment
<2 years of age	9	30.0
3–5 years of age	12	40.0
6–12 years of age	9	30.0
13–18 years of age	3	10.0
Up to 19 years of age	1	3.3

Note: Studies reported on multiple outcomes, therefore the percentages displayed above do not add to 100.

Table 3. Summary of each study included in the analysis.

Author, year	Country	Number of (offspring) participants in analysis	Neurophysiological domain(s) investigated	Outcome(s) measure or scale	Timing of PAE	Offspring age at assessment	Association between PAE and neurophysiological domain investigated
Alati et al., 2013	UK	7062	Academic Achievement	Key Stage 2 (KS2)	Alcohol consumption during first trimester, measured at 18 weeks of gestation	11 years	Academic achievement: No association with daily drinking, but association between consumption of four or more drinks per occasion and lower academic abilities
Alati et al., 2008	UK	4332	Cognition	IQ – WISC-III	Alcohol consumption during first trimester, measured at 18 weeks of gestation	8 years	Cognition: no significant association
Alvik et al., 2013	Norway	1138	Affect regulation	SDQ	Alcohol consumption during 0–6 weeks of pregnancy, measured at 17 weeks	5.5 years	Affect regulation: binge drinking during the early stages of pregnancy predicted scores in the Abnormal and Borderline range of the SDQ among the cohort of 5.5-year-olds. A binge drinking rate of less than once a week was associated with higher Total Problem scores on the SDQ, and greater than or equal to once a week predicted elevated risk of abnormal or borderline scores for total problems, emotional subscale, and conduct subscale
Alvik et al., 2011	Norway	1330	Affect regulation	Infant Characteristics Questionnaire:temperament	Alcohol consumption during 0–6, 7–12 and 13 + weeks of pregnancy, measured at 17 weeks	6 months	Affect regulation: Binge drinking more than once a week during 0–6weeks is associated with a difficult temperament
D’Souza et al., 2019	New Zealand	5768	Language, Affect Regulation	Comorbidity of language and behavioural difficulties (MB-CDI and SDQ)	Assessed in the 3rd trimester covering the 1st trimester.	2 years	Language: consumption of one or more drinks per week in the first trimester was associated with reduced likelihood of language difficulties, relative to those who abstained. Affect regulation: no significant association
Donald et al., 2019	South Africa	734	Motor skills, Cognition, Language	BSID-III subscale	Recruited at 28–32 weeks gestation, alcohol consumption assessed covering the whole pregnancy	2 years	Motor skills: No significant association Cognition: No significant association Language: significant positive association with receptive language deficits
Faebo Larsen et al., 2013	Denmark	33,354	Motor skills	DCDQ’07	16 weeks gestation covering the first trimester	7 years	Motor skills: No association between PAE and developmental co-ordination disorder
Falgreen Eriksen et al., 2012	Denmark	1628	Cognition	IQ (WPPSI-R)	17 weeks gestation covering ‘early pregnancy’	5 years	Cognition: PAE of greater than or equal to nine drinks per week in early pregnancy increased risk of low full-scale and verbal IQ. No differences were observed when mothers reported consuming 1–4 standard drinks or 5–8 standard drinks per week relative to those who abstained
Halliday et al., 2017	Australia	554	Motor Skills, cognition, language, affect regulation, (adaptive behaviour, social skills or communication)	BSID-III subscale Brief Infant Toddler Social Emotional Assessment – Competence scale	19, 26 weeks gestation, following birth. Exposure categories Trimester 1 (pre-pregnancy awareness), Trimester 2 (post-awareness), Trimester 2 and Trimester 3	2 years	Motor skills: No significant association Cognition: protective effect of low levels of drinking on improved cognition, but this difference was accounted for by moderating variables Language: no association with language deficits Affect regulation: found that early binge drinking with continued low level alcohol consumption over the duration of the pregnancy was associated with lower sensation avoidance scores in offspring at age 2 Adaptive behaviour, social skills or communication: no significant associations with social competencies
Hutchinson et al., 2019	Australia	1324	Motor skills, cognition	BISD-III	Trimester one (weeks 0–6), trimester one (weeks 7-12), trimester two, trimester three	12 months	Motor skills: no significant association Cognition: no significant association
Kesmodel, Bertrand, et al., 2012	Denmark	1628	Cognition, Attention, Executive function	WPPSI-R, TEACh-5, BRIEF	17 weeks gestation covering early to mid-pregnancy	5 years	Cognition: no significant association Attention: no significant association Executive function: no significant association
Kesmodel, Eriksen, et al., 2012	Denmark	1617	Cognition	WPPSI-R	17 weeks gestation covering early to mid-pregnancy	5 years	Cognition: no significant difference in IQ between the children of mothers who reported binge drinking and mothers with no binge episodes, however, they did find that binge drinking during gestational weeks 1–2 was associated with reduced risk of low full-scale IQ compared to those unexposed to binge drinking
Kilburn et al., 2015	Denmark	1628	Executive Function	CRT and Information processing time	17 weeks gestation covering early pregnancy	60–64 months	Executive function: no significant effect on reaction time or information processing
McCormack et al., 2018	Australia	1331	Cognition	BSID-III	Trimester one (weeks 0–6), trimester one (weeks 7–12), trimester two, trimester three	12 months	Cognition: low level consumption of alcohol during the second and third trimester was associated with slightly higher cognitive scores, relative to mothers who abstained
Negrao et al., 2020	Brazil	1006	Motor skills, Cognition	BSID-III subscale	A few days after birth of the child covering the whole pregnancy	2 years	Motor: found an association between concomitant use of alcohol and tobacco and fine motor skills, but not for gross motor skill or for alcohol consumption alone. Children whose mothers’ used alcohol and tobacco concomitantly during pregnancy were at increased risk for motor delays in fine motor skills, but not in gross motor delay Cognition: no significant association
Niclasen, Andersen, et al., 2014	Denmark	37,315	Affect Regulation	SDQ	Weeks 16 and 30 gestation, and 6 months postpartum.	7 years	Affect regulation: association between affect regulation and exposure to binge episodes only in male children. Exposure to binge episodes was associated with an increased change in mean for externalising behaviours compared to children whose mothers reported no binge episodes and internalising behaviours – although the effect was not significant at four or more binge episodes
Niclasen, Nybo Andersen, et al., 2014 (Teasdale)	Denmark	37,315	Attention, Affect Regulation, (Adaptive behaviour, social skills, or communication)	SDQ subscale(s)	Weeks 16 and 30 gestation, and 6 months postpartum.	7 years	Attention: no association with hyperactivity Affect regulation: significant association between binge drinking and externalising scores in early pregnancy and late pregnancy Adaptive behaviour, social skills or communication: there was a significant increased risk of abnormal or borderline scores on the peer problems scale for children not exposed to alcohol compared to children to a cumulative 15–45 drinks over the pregnancy), no association for other amounts of alcohol exposure
O’Callaghan et al., 2007	Australia	5139	Cognition, Academic achievement, attention	Raven progressive matrices WART-R; learning difficulties CBCL subscale	20 weeks gestation, days after delivery covering early and late pregnancy	14 years	Cognition: significant association between binge drinking and IQ. No significant association between alcohol exposure in early pregnancy and IQ, however, there was a higher prevalence of children with poor Raven's scores in children exposed to binge drinking and children exposed to alcohol in late pregnancy. The adjusted model found that there was an increased risk for low IQ for children whose mother reported engaging in binge drinking compared to those that reported no binge episodes Academic achievement: no association with low scores on the WRAT-R Attention: no significant association
Robinson et al., 2010	Australia	1860	Affect Regulation	CBCL	Assessed 18 and 34 weeks – covering the whole pregnancy	2, 5, 8, 10 and 14 years	Affect regulation: light to moderate levels of drinking in early pregnancy was associated with a reduced likelihood of scores above the clinical cut-off on the CBCL in children aged between 2 and 14 years compared to unexposed children on the externalising, internalising, and total behaviour
Rodriguez et al., 2009	Denmark, Finland	21,678	Attention	SDQ subscale or Rutter Scale subscale	Between 12- and 32-weeks gestation covering the whole pregnancy	15 years	Attention: no significant association with hyperactivity/inattention
Sayal et al., 2013	UK	10,558	Academic Achievement, Affect regulation	KS2	18 weeks gestation covering the first trimester	11 years	Academic achievement: no significant associations Affect Regulation: no significant associations
Sayal et al., 2014	UK	7965	Academic Achievement, Attention, Affect regulation	KS2 SDQ subscale	18- and 32-weeks gestation covering the first trimester	10–11 years	Academic achievement: drinking 4 + drinks per occasion was significantly associated with lower KS2 scores Attention: significant association for girls at age 11 on the parent rated SDQ hyperactivity/inattention subscale and binge drinking. Further analyses separating the effects of daily drinking and binge drinking found significant effects for the exposure category 4 + drinks but not daily drinking and the parent rated SDQ subscale for girls and the teacher rated SDQ subscale for the whole sample. Affect regulation: binge pattern of alcohol consumption was associated with elevated conduct problem scores among girls (age 11) compared to the children of mothers who reported no binge episodes, as well for total problems. There was no significant association in male children or for daily non-binge drinking patterns.
Sayal et al., 2009	UK	8240	Cognition Attention Affect regulation	WPPSI-R SDQ	18- and 32- weeks gestation covering the first trimester	47 months	Cognition: no association with IQ score Attention: 4 plus drinks a day were significantly associated with higher scores (more problematic) on the hyperactivity/inattention subscale of the SDQ. Affect regulation: binge patterns of alcohol consumption during the second and third trimester was associated with poorer scores on both the conduct and total problems scale of the SDQ among girls at 47 months compared to children not exposed to binge drinking. Elevated scores on the conduct problems subscale and total problems were apparent across the whole sample during the 81-month data collection window.
Sayal et al., 2007	UK	47 months (N = 9086), 81 months (N = 8046), 93 and 108 months (N = 5648)	Affect regulation	SDQ	18 weeks gestation covering the first trimester	47, 81, 93, 108 months	Affect Regulation: alcohol intake at less than one drink per week was associated with poor total problems scores at 47 months, 81 months, and 93-108 months among girls. Teacher rated conduct score were also elevated in this exposure category for the whole sample at 93–108 months. However, the association between PAE and total problems scores was not significant for one or more drinks per week or for male children.
Schoeps et al., 2018	New Zealand	6156	Affect regulation	Infant Behaviour Questionnaire (IBQ-R VSF); SDQ	Last trimester covering the first and last trimester	9 months and 2 years	Affect regulation: four or more drinks per week was associated with children with higher total difficulties.
Skogerbo et al., 2013	Denmark	1628	Affect Regulation	SDQ	17 weeks covering early pregnancy	5 years	Affect Regulation: no significant associations
Skogerbo et al., 2012	Denmark	1628	Executive function	Parent rated BRIEF	17 weeks covering early pregnancy	5 years	Executive function: significant associations between binge drinking in gestational week 9 or later and elevated parent ratings on the behaviour regulation index and teacher rated metacognition index
Underbjerg et al., 2012	Denmark	1628	Attention	TEACh-5	17 weeks covering early pregnancy	5 years	Attention: significant association between consumption of 9 or more drinks per week and low overall attention score, no associations between binge drinking and attention
Weile et al., 2020	Denmark	48,072	Attention	ADHD diagnosis	11 weeks gestation covering early pregnancy	Up to 19 years of age	Attention: no significant associations with ADHD diagnosis
Zuccolo et al., 2013	UK	4061 – 8 years 6268 – 11 years	Cognition, academic achievement	WISC, KS2	18 weeks gestation covering the first trimester	Age 8 and 11	Cognition: no significant association Academic achievement: no significant association

Table

#	Search terms	Results
S1	TI (((alcohol use) OR alcohol) AND (consum* OR expos* OR drink*)) OR AB (((alcohol use) OR alcohol) AND (consum* OR expos* OR drink*)) OR MW (((alcohol use) OR alcohol) AND (consum* OR expos* OR drink*))	52,344
S2	TI (matern* or pregnan* or f?etal or prenatal) OR AB (matern* or pregnan* or f?etal or prenatal) OR MW (matern* or pregnan* or f?etal or prenatal)	315,248
S3	TI (motor skills or neurophysiology or cognition or language or academic achievement or memory or attention or executive function or affect regulation or adaptive behavio?r or social skills or communication or fine motor or gross motor or IQ or intelligence or ((education* or school) and achievement) or inattention or emotional development or emotional regulation or behavio?r problems or developmental delay or neurodevelopment*) OR AB (motor skills or neurophysiology or cognition or language or academic achievement or memory or attention or executive function or affect regulation or adaptive behavio?r or social skills or communication or fine motor or gross motor or IQ or intelligence or ((education* or school) and achievement) or inattention or emotional development or emotional regulation or behavio?r problems or developmental delay or neurodevelopment*) OR MW (motor skills or neurophysiology or cognition or language or academic achievement or memory or attention or executive function or affect regulation or adaptive behavio?r or social skills or communication or fine motor or gross motor or IQ or intelligence or ((education* or school) and achievement) or inattention or emotional development or emotional regulation or behavio?r problems or developmental delay or neurodevelopment*)	565,786
S4	TI (prospective or longitudinal or follow-up or cohort) OR AB (prospective or longitudinal or follow-up or cohort) OR MW (prospective or longitudinal or follow-up or cohort)	818,896
S5	S1 AND S2	4085
S6	S3 AND S4 AND S5	173

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