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Alcohol is a teratogen; its consumption during pregnancy can lead to negative birth outcomes, collectively referred to as fetal alcohol spectrum disorders. Neurodevelopmental delays in higher-order cognitive functions that affect development of executive functions are a common feature. Studies on executive function in children have focused on children diagnosed with fetal alcohol spectrum disorder, and there is a lack of information on the impact on children not diagnosed with fetal alcohol spectrum disorder but who had been exposed to alcohol.
The aim of this study was to compare the development of executive function in children between 4 and 6 years of age with and without prenatal exposure to alcohol.
Children both exposed and not exposed to alcohol were recruited as part of a feasibility RCT evaluating a computer-based cognitive training program for improving executive function development. The study was conducted in a low–socioeconomic status community in South Africa with a high prevalence of fetal alcohol spectrum disorder. Neurodevelopment was assessed in participating children; NEPSY-II standardized scores for executive function domains were compared using a multivariate analysis of variance with group membership as the predictor variable.
No significant differences in executive functions assessments (
We expected that alcohol exposure would have a measurable impact on executive function development. The lack of differences highlights the prevalence of developmental delays in low–socioeconomic status communities in South Africa and suggests that children are exposed to various threats to cognitive development.
RR2-10.2196/14489
Alcohol is a known teratogen when consumed during pregnancy and can lead to a number of negative outcomes including a characteristic pattern of dysmorphic facial features, growth retardation, deficient brain growth, and neurodevelopmental delays in the newborn child [
The most common form of fetal alcohol spectrum disorder is alcohol-related neurodevelopmental disorder, for which physical features are not evident. As such, it is also the most difficult of the fetal alcohol spectrum disorders to diagnose [
Elementary and higher-order intellectual functions can be affected in individuals with fetal alcohol spectrum disorder, and dysfunction can be present regardless of whether the physical features of fetal alcohol spectrum disorder are present [
Deficits in executive function are hallmarks of fetal alcohol spectrum disorder, with far-reaching consequences for affected individuals [
Executive function in children is amenable to intervention [
If a diagnosis of fetal alcohol spectrum disorder is required for inclusion in studies on prenatal alcohol exposure’s effect on executive function, the picture of alcohol’s impact in utero will be incomplete. The aim of this paper was to compare executive function in children who had been exposed with those who had not been exposed to alcohol during prenatal development. Data for the analyses were obtained as part of a feasibility RCT of a computer-based cognitive training game. Assessments of executive function were conducted on children both exposed and nonexposed to alcohol. The primary hypothesis for this paper was that children in the alcohol-exposed group would perform poorer than those in the nonexposed group on standardized measures of executive function.
This paper reports the findings of baseline assessments from a feasibility RCT of a computer-based cognitive training game (International Standard Randomized Controlled Trial Number; ISRTCN17244156). The trial protocol has been published [
CONSORT diagram.
Saldanha Bay municipality largely comprises Saldanha Bay, a harbor city with a population of 113,239 as of 2017 and main industries of agriculture, forestry, fishing, and manufacturing [
Because we were interested in a population of children between the ages of 4 and 6 years, we approached an organization called Saldanha Bay ECD forum that serves ECD centers in low–socioeconomic status areas of the Saldanha Bay municipality. After giving an overview of the RCT, meetings were set up with the individual ECD center principals. At these meetings, the project was discussed in more depth, and the principals were asked if they would be willing to facilitate access to the parents of the children in their schools (ie, inform parents of the study and ask if they would like to participate).
We obtained the contact details of parents willing to allow their children to participate in the study, and community workers contacted these parents, obtained informed consent, and conducted interviews with biological mothers. The order in which parents from participating ECD centers were contacted was determined by randomly allocated numbers using Microsoft Excel. All consenting mothers identified by a particular ECD center were contacted for interviews before we moved on to mothers from another ECD. If, however, there were consenting mothers who were unavailable for interviews, we still moved on to a new ECD center. We followed up to see if they became available for interview at a later stage. New ECD centers were included until 80 participants exposed to alcohol had been identified, following which the 40 unexposed participants were selected.
Ethics approval was obtained from the Health Research Ethics Committee at Stellenbosch University (N16/05/063). Data were deidentified after participants were allocated study IDs, and test administrators were blinded to alcohol exposure status during assessments.
The structured interview used with the children’s mothers has been used extensively in fetal alcohol spectrum disorder epidemiological studies in South Africa [
Children who were exposed to more than 3 standard drinks in 1 drinking session during pregnancy were defined as having had prenatal alcohol exposure.
Neurodevelopmental assessments of the children were conducted by trained psychometrists using NEPSY-II, a battery of individually administered tests that has been shown to reliably diagnose a range of childhood disorders [
NEPSY-II domains and subtests.
Domain | Subtest |
Attention and executive function |
Statue |
Language |
Comprehension of instructions |
Memory and learning |
Memory for designs content Memory for designs spatial Memory for designs Narrative memory free and cued Narrative memory and recognition contrasted Sentence repetition |
Data were collected using REDCap [
To evaluate whether alcohol exposure predicted test performance, multivariate analysis of variance with group membership as the predictor variable was conducted to test the scaled scores of the 8 subtests. A Box
After engaging with the ECD forum, 27 ECD centers agreed to participate. To obtain 80 children with prenatal alcohol exposure, 235 interviews were completed in 14 ECD centers. Upon review of the assessment data, 4 children were excluded for being too young, and their data were excluded from analysis. The final sample (n=116) included 76 children in the alcohol-exposed group and 40 children in the nonexposed group (
There was a significant difference in age (
Characteristics of children and their mothers included in the randomized controlled trial.
Characteristic | Alcohol exposure (n=76) | No alcohol exposure (n=40) | ||||||||||
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RCTa intervention (n=39) | RCT control (n=37) |
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Age (years), mean (SD) | 4.72 (0.50) | 4.83 (0.54) | 5.14 (0.44) | .001 | |||||||
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.92 | |||||||
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Female | 17 | 16 | 19 |
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Male | 22 | 21 | 21 |
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Age (years), mean (SD) | 28.15 (5.32) | 30.41 (5.85) | 31.17 (6.18) | .08 | |||||||
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Number of living children, mean (SD) | 1.87 (0.95) | 2.35 (1.27) | 2.15 (1.21) | .19 | |||||||
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Years of schooling, mean (SD)b | 10.67 (1.69) | 11.03 (1.78) | 10.71 (2.07) | .66 | |||||||
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Gravidity, mean (SD) | 2.21 (1.10) | 2.51 (1.40) | 2.45(1.47) | .57 | |||||||
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Monthly household income (ZAR)c, mean (SD)d | 4953.24 (4619.59) | 4610.56 (3375.28) | 5474.86 (6233.52) | .75 | |||||||
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.27 | |||||||
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Yes | 11 (28) | 12 (32) | 18 (45) |
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No | 28 (72) | 25 (68) | 22 (55) |
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.22 | |||||||||
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Yes | 30 (76) | 29 (78) | 25 (62) |
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No | 9 (24) | 8 (22) | 15 (38) |
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.59 | |||||||
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Yes | 26 (68) | 26 (70) | 24 (60) |
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No | 12 (32) | 11 (30) | 16 (40) |
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aRCT: randomized controlled trial.
bMissing data: n=1, n=4, and n=2 in the intervention, control, and no exposure groups, respectively.
cZAR: South African Rand; an approximate exchange rate of ZAR 1 to US $0.07 is applicable at the time of publication.
dMissing data: n=3, n=4, and n=3 in the intervention, control, and no exposure groups, respectively.
eMissing data: n=2 and n=3 in the intervention and control groups, respectively.
There was no significant difference in monthly household income (mean difference ZAR 690.62, 95% CI −1259.95 to 2641.18,
Alcohol-exposed (combined intervention and control groups) and nonexposed group mean scaled scores for all NEPSY-II subtests (except statue) fell into the borderline performance category (between the 11th and 25th percentiles) or lower. Children in the alcohol exposed group and the nonexposed group performed below the expected level (at or below the tenth percentile) for comprehension of instructions (means 4.97 and 5.37, respectively), narrative memory recall (means 5.10 and 5.14, respectively), and sentence repetition (means 6.24 and 5.46, respectively) subtests. Performance on the statue subtest was at the expected level for both the alcohol exposed (mean 10.68) and nonexposed (mean 10.26) groups.
Some participants were unable to successfully complete all subtests in the chosen battery (based on the NEPSY-II guidelines for discontinuation [
Between-participant effects with alcohol exposure as the predictor variable.
Dependent variable | Type III sum of squares | Partial eta squared | |||
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Comprehension of instructions | 3.753 | 0.560 (1) | 0.005 | .46 |
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Memory for designs content | 3.263 | 0.482 (1) | 0.005 | .49 |
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Memory for designs spatial | 20.849 | 3.566 (1) | 0.033 | .06 |
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Memory for designs | 6.172 | 2.076 (1) | 0.019 | .15 |
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Narrative memory free and cued | 0.049 | 0.008 (1) | 0.000 | .93 |
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Narrative memory and recognition contrasted | 4.636 | 0.427 (1) | 0.004 | .52 |
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Sentence repetition | 14.291 | 2.625 (1) | 0.024 | .11 |
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Statue | 4.222 | 0.518 (1) | 0.005 | .47 |
Performance on the NEPSY-II was poor, regardless of alcohol exposure. The data did not show any significant differences between the alcohol-exposed and nonexposed groups (
The differences in demographic characteristics of the mothers of children in the RCT intervention, RCT control, and nonexposed groups were not significant (age:
The lack of difference between the alcohol-exposed and nonexposed groups was surprising given the strong associations that have been shown between alcohol use and deficits in executive function [
NEPSY-II performance was similar for the exposed and nonexposed children. The finding of borderline scores on the NEPSY-II subtests for the entire group is unexpected and concerning. We hypothesized that the alcohol-exposed group would generally perform below expectation, and this was indeed the case. The nonexposed group, barring other causes of poor development, were expected to perform at age-appropriate levels. This did not prove to be the case, with no differences found between children in the alcohol-exposed group and nonexposed group.
It is possible that development of children in the alcohol-exposed group has not been impacted, with development occurring at the same rate as their peers. This does not imply that development of children in the alcohol-exposed groups will remain on par with that of their peers. It has been shown that the developmental trajectory of children with prenatal alcohol-exposure diverges from expected norms as they become older, which makes diagnosis and identification easier as time passes [
As participants were recruited from underresourced and low–socioeconomic status areas, overall low performance may be linked to exposure to adverse childhood experiences. Adverse childhood experiences have a detrimental impact on cognitive development, social development, and mental health [
With 84 out of 116 (72%) households relying upon social grants, which amounts to only ZAR 410.00 (approximately US $27) each month per child for child support, these data indicate there are high levels of poverty and adversity. There is little that differentiates the alcohol exposed and unexposed groups, except for mothers’ reported alcohol use. The Saldanha Bay municipal area also experiences problems with violence and crime [
It is also possible that NEPSY-II cannot detect differences between groups. It may be that the NEPSY-II is not sensitive enough to detect the difference in executive function between alcohol-exposed and nonexposed groups. There are, however, no other assessments used in research on executive function or fetal alcohol spectrum disorder that have more suitable norms or that are more culturally appropriate for a South African context. Measuring executive function in these age groups is complicated by the way in which executive function develops; different aspects of executive function develop at different times and at different rates. Attention control, for example, develops and matures before cognitive flexibility (which is related to working memory and inhibition). This development is consistent with spurts of growth and development in the frontal lobe [
We must also acknowledge that there may be children exposed to alcohol in the normative group. Although selection was based on a confirmation of prenatal alcohol exposure, some mothers may have been reluctant to admit drinking or they may have misreported the amount that they drank during pregnancy because alcohol use during pregnancy is heavily stigmatized [
One of the study limitations is the lack of local norms for the NEPSY-II. The lack of local norms for neurodevelopmental assessments is an acknowledged problem in South Africa [
Another limitation is that we relied upon self-reporting of alcohol use. Underreporting of alcohol use was a concern due to possible reluctance on the part of the mother to admit to alcohol use. Mothers may also have found it difficult to recall alcohol use 5 years earlier. Some of the children in the nonexposed group may in fact have been exposed to alcohol. Inclusion due to alcohol use was based on recall of an average drinking session during pregnancy. Participants in the nonexposed group may, therefore, have been exposed to alcohol over a longer period of time but their reported alcohol use placed them in the nonexposed category because the level of exposure did not meet the threshold indicated in the fetal alcohol spectrum disorder diagnostic criteria [
Due to the size of the ECD centers, it was not possible to reach the total sample size in a single area or ECD center. Although the ECD centers were located in similar communities, there were still differences between centers that could have impacted on the performance of the children on the psychometric assessments. Some of these factors could include the number of children per ECD practitioner or the availability of toys and equipment for stimulation. It is well established that poverty has a negative impact on cognitive assessments [
We compared the performance of children exposed and not exposed to alcohol in utero on measures of executive function. We expected that alcohol exposure would have a measurable negative impact, but in our sample, there was none. This highlights that developmental delays are widely prevalent in resource poor and low–socioeconomic status communities in South Africa. As developmental delays form part of the diagnostic criteria of fetal alcohol spectrum disorder, this study also shows that caution should be used when interpreting normed scores. It is possible that a borderline or below average score may not necessarily support a diagnosis of fetal alcohol spectrum disorder as there are clearly other possible causes of poor development that must be excluded.
This paper also identified important avenues for further research. The lack of difference between alcohol-exposed and nonexposed groups needs to be further explored. Does this lack of difference remain as participants age? What is the prevalence of adverse childhood experiences and to what extent do adverse childhood experiences explain the lack of difference between the groups? Overall, this paper adds to the understanding that alcohol exposure in utero and its sequelae are only part of the possible developmental challenges faced by children in South African communities.
early childhood development
randomized controlled trial
South African Rand
This study received funding from the Association for Alcohol Responsibility and Education (AWARE). We would also like to acknowledge the dedication of our community workers who conducted the interviews and the willingness of the participants and caregivers to participate in the study. We would also like to thank the Saldanha Bay ECD forum and the ECD centers in the Saldanha Bay municipality for their support.
JGL, LO, MB, LB, and MV are employed by the Foundation for Alcohol Related Research, which designed and developed the game used in the intervention. The other authors have no conflicts to declare.