IJE Advance Access originally published online on August 5, 2005
International Journal of Epidemiology 2005 34(5):1047-1053; doi:10.1093/ije/dyi163
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Article |
Maternal smoking during pregnancy and offspring IQ
1 Department of Epidemiology, Michigan State University, College of Human Medicine, East Lansing, MI 48824, USA
2 New York City Department of Health and Mental Hygiene, Bureau of STD Control, NY, USA
* Corresponding author. Michigan State University, B645 West Fee Hall, East Lansing, MI 48824, USA. E-mail: breslau{at}epi.msu.edu
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Background Maternal smoking in pregnancy lowers birthweight. It is unclear, however, whether smoking during pregnancy lowers offspring IQ, and, if it does, whether it is through the smoking effect on fetal growth.
Method Representative samples of low birthweight (<2500 g) and normal birthweight children born in 1983–85 from inner-city and suburban communities in southeast Michigan, USA were assessed at ages 6, 11, and 17, using Wechsler intelligence tests. Smoking during pregnancy was ascertained from mothers at the first assessment; and smoking at any time was ascertained at the first and second assessment. Generalized estimating equation models were used, with children's IQ at all three assessments as outcomes (n = 798).
Results Without adjustment, offspring of mothers who smoked during pregnancy scored 6.8 IQ points lower than offspring of mothers who never smoked, on average. Low birthweight children scored 5.4 IQ points lower than normal birthweight children, on average. The statistical association of maternal smoking with offspring IQ was confounded by maternal characteristics, chiefly, maternal cognitive ability as measured by IQ and education; adjustment for these factors eliminated the association. By contrast, adjustment for maternal IQ and education as well as smoking during pregnancy had a negligible effect on the low birthweight-related IQ deficit. Low birthweight did not mediate the association of smoking and lowered IQ in offspring.
Conclusion Maternal smoking during pregnancy is a proxy for a matrix of vulnerabilities for adverse child cognitive development and has no direct causal effect on child's IQ. The relationship of low birthweight and IQ is independent of maternal smoking and maternal cognitive abilities.
Keywords Maternal smoking during pregnancy, children's IQ, low birthweight
Accepted 21 July 2005
Maternal smoking during pregnancy has been associated with a wide range of adverse outcomes in offspring.1,2 Despite a large body of evidence from samples of geographically diverse populations, a direct causal link between maternal smoking during pregnancy and neurodevelopment has not been established. Alternative explanations center on the possibility that smoking during pregnancy might be a proxy for factors causally associated with children's behaviour problems and poor cognitive development.3
The hypothesis that maternal smoking during pregnancy might have an adverse influence on children's cognitive development is suggested by evidence of a direct effect of maternal smoking on low birthweight,4–6 together with the evidence of low birthweight-related IQ deficits (for reviews see Refs 7 and 8). It could be argued that maternal smoking in pregnancy is causally related to adverse cognitive development through its effect on low birthweight. Alternatively, the low birthweight–IQ association might be unrelated to smoking during pregnancy, given that smoking during pregnancy is but one of a myriad of factors influencing low birthweight.5,6 Empirical studies have yielded mixed results. Several studies reported an association between maternal smoking and decreased scores on measures of children's cognitive abilities, learning and memory, language development, and academic achievement.9–18 (Publications in Refs 9–11 are from a single sample.) Associations with intelligence (in males) and achievement scores in early adulthood were also reported.19–21 In some of the studies low birthweight was not a mediator between maternal smoking and offspring's IQ.19,20 Other studies reported no association between maternal smoking during pregnancy and children's cognitive abilities, when potential confounders were taken into account.22–26
In this study, we examine the hypothesis that maternal smoking during pregnancy influences children's IQ, using data from a longitudinal study of low birthweight and normal birthweight children, in which IQ was measured at ages 6, 11, and 17 years. Data on maternal smoking during pregnancy were obtained at the first assessment in a section of the baseline interview that focused on prenatal history. In addition, data on maternal smoking at any time, without reference to pregnancy, were gathered in a separate part of the interview. We address the following questions: (i) Do children whose mothers smoked during pregnancy score lower on IQ tests, compared to children whose mothers did not smoke during pregnancy? (ii) Does low birthweight mediate the association between maternal smoking in pregnancy and children's IQ? (iii) Do key maternal characteristics associated with children's cognitive development, namely, maternal IQ and education (both are measures of cognitive abilities), account for any observed association of maternal smoking with children's IQ?
We estimate first the unadjusted association between maternal smoking and children's IQ. We then examine whether the maternal smoking–children's IQ association is mediated by low birthweight. Evidence that the smoking–IQ association is reduced substantially when low birthweight is added to the equation would indicate that low birthweight mediates the association. Finally, we examine the effects of potential confounders, that is, preexisting factors associated with both maternal smoking during pregnancy as well as children's IQ. Evidence that the association between prenatal exposure to smoking and children's IQ is reduced substantially and is no longer significant would indicate that the statistical association is confounded with other risk factors for children's cognitive development.
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Sample and follow-up
Data are from a longitudinal study of low birthweight (<2500 g) and normal birthweight children who were assessed at ages 6, 11, and 17 designed to evaluate the neuropsychiatric sequelae of low birthweight. Complete information on the population, sampling, and assessment is presented elsewhere27–30 and is summarized briefly here. We targeted the 1983–85 birth year cohorts of newborns who were 6–7 years of age in 1990–92, the scheduled period of the initial fieldwork. Two major hospitals in southeast Michigan, one in the city of Detroit and the other in a middle-class suburb, were selected. In each hospital, for each year from 1983 through 1985, random samples of low birthweight and normal birthweight newborns were drawn from discharge records. Children with severe disabilities, identified at birth and at age 6, were excluded. Of the 1095 in the target sample, 823 (75%) participated. The second assessment was conducted in 1995–97, with children assessed as they passed their 11th birthday. Of the 791 children remaining in the Detroit area, 717 (90.6%) were reassessed at age 11, 87.1% of the initial sample.
In 2000–02, when the children passed their 17th birthday, we assessed the sample a third time. A total of 713 children were assessed, including 56 children who were not assessed at age 11. The Institutional Review Boards of the participating institutions from which the samples were drawn and of Michigan State University, where the analysis of the existing data was conducted, approved the study.
Measurement of key variables
The Wechsler Intelligence Scale for Children-Revised (WISC-R)31 was used to measure IQ at ages 6 and 11. The Wechsler Adult Intelligence Scale-third edition (WAIS-III) was used at age 17, as the appropriate test for this age.32 The IQ tests are age-standardized and have a mean of 100 and a standard deviation of 15 in the general population. Children were assessed individually under the same standardized laboratory conditions at all ages. Psychometricians were trained to a uniform standard, and all test files were scored by two independent testers. Periodic monitoring for testers' adherence to test administration rules, as specified in the official manuals, was conducted throughout each assessment period. Testers were blind to low birthweight status and to the results of previous assessments. Correlation of IQ scores between ages 6 and 11 was 0.85, and between ages 11 and 17 was 0.90.
Maternal IQ was measured at the first assessment, when the children were 6–7 years of age. We used the Two-Subtest Short-Form of the Wechsler Adult Intelligence Scale-Revised (WAIS-R).33 The two subtests—Vocabulary and Block Design—have high reliabilities, and their combination has a high correlation with the full-scale WAIS-R.33 Information on children's birthweight was abstracted from medical records.
Maternal smoking during pregnancy was ascertained at baseline interview, when children were 6 years of age. Mothers were asked if they smoked daily for 2 months or longer during pregnancy of the index child. A positive answer was followed-up by an inquiry about the number of cigarettes smoked daily. These questions were in a section of the interview that focused on pregnancy, delivery and child's early health history.34 At baseline, a separate interview schedule, administered before the inquiry about perinatal history, included a section on tobacco use disorder, which opens with the question ‘Did you ever smoke daily for a month or more?’ At the 5 year re-assessment, mothers were asked about daily smoking during the preceding 12 months. The availability of information on daily smoking at any time up to baseline and at re-assessment allows us to evaluate the association between smoking during pregnancy and offspring's IQ relative to two reference groups: mothers who never smoked and mothers who smoked but not during pregnancy.
Statistical analysis
We used multiple regression analysis, applying generalized estimating equations (GEE),35–37 to test the relationship of maternal smoking during pregnancy with IQ at ages 6, 11, and 17 years. GEE analysis utilizes data on all respondents, including those with incomplete data. Analysis was conducted on 798 children with data on maternal smoking in pregnancy. (Informants for 25 children were caregivers other than mothers.) Successive GEE models are presented to address the sequence of questions, formulated above. In each model that follows the first unadjusted model, we introduce a new variable (or set of variables) to first test if low birthweight mediates the initially observed association between maternal smoking and children's IQ, and then whether the association holds-up when potential confounders are controlled. GEE permits simultaneous modelling of the relation of specific risk factors with children's IQ based on all three assessments. The use of interaction terms enables us to examine whether the relationship of IQ with a specific risk factor (e.g. maternal smoking in pregnancy) varied with age of assessment. In the absence of age interactions, the approach yields an estimate of the association of a risk factor with IQ across all assessments. GEE estimates regression coefficients and their standard errors, taking into account the correlation between IQ scores at ages 6, 11, and 17 years. It yields valid and robust estimates of variance, even when there is known positive correlation between the multiple outcomes within subjects. The exchangeable correlation option was used as the working correlation. The analysis provides estimates of unstandardized regression coefficients, which are IQ points, based on the weighted scores from the three assessments.
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A description of the sample is presented in Table 1. On sociodemographic characteristics, the urban and suburban groups differed widely. However, within each group, low birthweight and normal birthweight subsets differed little. Data on maternal smoking in pregnancy are available on 798 subjects, 97.0% of the sample. Of the total sample, 247 (31.0%) smoked daily during pregnancy for a period of 2 months or longer, 39.7% of mothers of low birthweight and 19.3% of mothers of normal birthweight children. Of those who smoked during pregnancy, 47 (19.0%) smoked
5 cigarettes per day, 128 (51.8%) smoked 6–19 cigarettes per day, and 72 (29.2%), smoked 
20 cigarettes per day. Table 2 presents descriptive data on children's IQ at ages 6, 11, and 17. Table 3 displays the pair-wise correlations of children's IQ, maternal IQ, and education.
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Table 4 compares mothers who smoked during pregnancy with mothers who smoked, but not during pregnancy, and mothers who never smoked on education, single mother status, urban residence, low birthweight offspring, age, and IQ. Mothers who smoked during pregnancy had the lowest mean IQ score, lowest educational attainment, and lowest age. They were more likely to be single, to live in the urban area, and to have low birthweight offspring. Mothers who smoked during other periods (not during pregnancy) had intermediate values on these variables. Maternal characteristics associated with smoking during pregnancy were inter-correlated. For example, the correlation between maternal IQ and education (a 4-level variable) was 0.55, between maternal IQ and maternal age at index child's birth, 0.42, and between maternal IQ and single mother status, –0.44.
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Table 5 presents results of successive GEE models designed to address the research questions. Model 1 estimates the unadjusted association between maternal smoking during pregnancy and children's IQ. It shows that, compared to offspring of mothers who never smoked daily (i.e. neither during pregnancy nor at any other time), offspring of mothers who smoked during pregnancy scored 6.85 IQ points lower, on average. Offspring of mothers who smoked daily for a month or more but not during pregnancy scored 3.26 points lower than the reference group, on average. Both IQ deficits were significant (P < 0.05). Further, the difference between the IQ deficits associated with maternal smoking during pregnancy and maternal smoking not during pregnancy was significant (P = 0.01).
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Model 2 (of Table 5) tests whether low birthweight mediated the association between maternal smoking and children's IQ. The results show that it did not. Although low birthweight children scored 5.38 IQ points lower than normal birthweight children, the association of maternal smoking during pregnancy with children's IQ is only slightly attenuated. Model 3 introduces urban vs suburban residence, which is a feature of the sampling design and is associated with children's IQ as well as maternal smoking during pregnancy. Urban children scored
1 SD below suburban children. The IQ deficit associated with maternal smoking during pregnancy remained significant, albeit reduced by more than one-third. Also, the IQ deficit associated with maternal smoking not during pregnancy, although reduced, remained significant. Model 4 examines whether the association between maternal smoking and children's IQ is accounted for by maternal cognitive abilities. It introduces two inter-related variables that measure maternal cognitive abilities, standardized IQ scores and education, and shows that these variables account entirely for the association. In an additional model (not displayed) we included single mother status and maternal age and found that both variables were related significantly to children's IQ. However, as we have shown in Model 4, the statistical relationship between maternal smoking and children's IQ was accounted for entirely by maternal IQ and education and these additional variables are redundant in this analysis. We tested interactions between smoking during pregnancy and low birthweight (vs normal birthweight) and with urban (vs suburban) but neither one was significant at 
= 0.15. Two additional observations are noteworthy. The first is that a model with maternal IQ and education, but without controlling for urban vs suburban, yielded the same results as in Model 4: controlling for maternal IQ and education was sufficient to eliminate the effect of smoking on children's IQ (not displayed). The second is that the effect of low birthweight on IQ held-up, when we controlled for the same variables that accounted for the relationship between maternal smoking and children's IQ. The low birthweight-related IQ deficit was independent of urban residence, maternal IQ and education.
We examined the relationship of children's IQ with intensity of smoking during pregnancy, measured by number of cigarettes smoked per day (Table 6). IQ of offspring of mothers who smoked 20 cigarettes daily was 8.07 points lower than mothers who never smoked, and IQ of offspring of mothers who smoked fewer cigarettes was approximately 6.00 IQ points lower than the reference group of mothers who never smoked (Model 1). Only the estimated deficit associated with smoking 20 cigarettes (–8.07) was significantly greater than the deficit associated with ever smoking daily but not during pregnancy (–3.26) (P = 0.03). Low birthweight did not mediate the association between level of smoking and children's IQ (Model 2). Maternal cognitive abilities, measured by IQ and education, accounted for the deficits in children's IQ associated with all levels of smoking. The large IQ deficit associated with smoking 20 cigarettes daily, was reduced from 8 to <2 points and was no longer significant (Model 4).
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Our results provide the following answers to the research questions. First, offspring of mothers who smoked during pregnancy scored significantly lower on standardized IQ tests, compared with offspring of mothers who did not smoke in pregnancy. However, the observed association between maternal smoking during pregnancy and children's IQ was accounted for entirely by maternal cognitive abilities, measured by standardized IQ tests and level of education. Thus, the observed statistical association is highly confounded with other known factors in children's cognitive development. Smoking during pregnancy is unlikely to be a causal factor in children's IQ. Second, low birthweight did not mediate the smoking–IQ association. Although low birthweight was associated with IQ deficits, controlling for its effect resulted in only a negligible reduction in the IQ deficit associated with maternal smoking during pregnancy. Third, the low birthweight-related IQ deficit was not accounted for by maternal cognitive abilities or other variables in the model (i.e. urban residence or maternal smoking).
We found that adjusting for urban vs suburban community reduced somewhat the unadjusted association between maternal smoking in pregnancy and children's IQ. However, we also found that maternal cognitive abilities, measured by IQ and education, accounted for the smoking–IQ association, even when urban vs suburban community was not controlled. Maternal IQ and education are correlated with urban vs suburban residence; the critical factor in relation to children's IQ is maternal cognitive abilities, measured by IQ and education.
A potential limitation of observational studies, such as this one, is that they might under-control for variables that can possibly confound the association between suspected risk factors and hypothesized outcomes. A comprehensive list of pre-existing factors associated with both maternal smoking during pregnancy and children's IQ include maternal heavy use of other substances, maternal anti-social behaviour, or paternal IQ. However, because the observed association between maternal smoking and children's IQ did not withstand the adjustment for maternal IQ and education, under-control is not a threat to the validity of the results.
The use of self-reports of maternal smoking during pregnancy in this study, as in most other studies in this area, is another potential limitation. In this regard, the availability of data about daily smoking at any time, obtained outside the context of the inquiry about pregnancy, provides some safeguard for the integrity of the results. As we report above, IQ of offspring of mothers who smoked daily at any time (as a separate group from offspring of mothers who smoked during pregnancy) scored significantly lower than offspring of mothers who never smoked daily; their IQ deficits, as the deficits of offspring of mothers who smoked in pregnancy, were accounted for entirely by maternal IQ and education. To the extent that mothers' under-reporting of smoking during pregnancy was captured in the broader, and less socially undesirable, category of ever smoking daily, our analysis addresses this concern by using mothers who never smoked daily as reference.
The overall percentage of mothers who smoked during pregnancy in our sample of 1983–85 birth cohorts was 31.0%, a higher figure than the 22.6% in the state of Michigan for 1990.38 However, our overall figure is influenced by the sampling design, which called for a disproportionately high percentage (57%) of low birthweight children, whose mothers had a higher rate of smoking during pregnancy than mothers of normal birthweight children (39.7% vs 19.3%). A weighted (corrected) overall percentage of smoking during pregnancy would be 21.4%, if we assume a 10% low birthweight and applied the specific percentages of smoking during pregnancy observed in this study for the low birthweight and normal birthweight subsets.
Important strengths of the study deserve mention. They include the longitudinal design of the study, with assessments of children's IQ at ages 6, 11, and 17 and a statistical analysis that uses data from all three assessments. The multiple assessments provide a robust measure of children's IQ up to late adolescence and thus improve the probability that the hypothesized relationship between maternal smoking and children's IQ would be detected. Additionally, the probability of detection is enhanced by the use of mothers who never smoked daily as reference, rather than mothers who did not smoke during pregnancy, a group that also includes mothers who smoked but not during pregnancy. The availability of birthweight information from medical records and a standardized measure of maternal IQ offered an opportunity to examine key factors implicated in the maternal smoking–children's IQ nexus.
Our results shed new light on the phenomenon of maternal smoking during pregnancy as well as the relationship between low birthweight and IQ. First, they show that maternal smoking during pregnancy is, in fact, a proxy for a matrix of vulnerabilities for adverse cognitive development. Second, as in previous reports from earlier phases of this study, we found that IQ deficits associated with low birthweight were independent of maternal IQ and education, as well as the web of adversities associated with growing-up in a disadvantaged inner-city area.27,39 Explanations for the cognitive deficits associated with low birthweight, and more generally, for the gradient relationship between birthweight and IQ,27 must be sought in mechanisms other than those that connect maternal smoking during pregnancy to decreased birthweight. There is by now wide consensus that maternal smoking in pregnancy influences birthweight primarily via its adverse effect on intra-uterine growth.5,6 Preterm birth, which apparently is not influenced by maternal smoking, and various causes of intra-uterine growth retardation other than maternal smoking40 might be potential mechanisms that link birthweight with IQ.
KEY MESSAGES
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This study was supported by grant MH-44586 from the National Institutes of Health, Bethesda, MD (Dr Breslau).
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