1 Institute of Social Pediatrics and Adolescent Medicine, Ludwig Maximilian University of Munich, Munich, Germany.
2 Dr. von Haunersches Kinderspital, Ludwig Maximilian University of Munich, Munich, Germany.
3 Division of Neurotoxicology, National Center for Toxicological Research, Food and Drug Administration, Jefferson, AR.
Received for publication January 4, 2002; accepted for publication June 4, 2002.
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
child; obesity; pregnancy; risk factors; smoking
Abbreviations: Abbreviation: CI, confidence interval.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
A higher skinfold thickness in 5-year-old children of mothers who smoked during pregnancy has been reported in a cohort study that enrolled 530 children in 1996 (8). We recently found a statistical association between maternal smoking during pregnancy and overweight/obesity in children at school entry in a cross-sectional study on the interdependencies of breastfeeding and childhood obesity (9).
The relation between maternal smoking during pregnancy and overweight/obesity in children was therefore further investigated in a cross-sectional study performed as part of the 19992000 Bavarian school entry health examination with an extensive questionnaire on a wide range of sociodemographic and lifestyle factors possibly related to overweight and obesity in children.
![]() |
MATERIALS AND METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The analysis was confined to German children aged 5.006.99 years who had information on body mass index and maternal smoking. With 273 children outside this age range, 281 "non-German" children, and 67 children with missing values on body mass index and 397 children with missing values on maternal smoking and with some children being included in more than one group, a total of 6,483 questionnaires remained for the analyses. Height and weight were measured as part of the routine health examination. As proposed by the European Childhood Obesity group (10), overweight was defined as a body mass index greater than the 90th percentile (girls: 17.4 kg/m2 (5 years), 17.7 kg/m2 (6 years); boys: 17.2 kg/m2 (5 years), 17.5 kg/m2 (6 years)), and obesity was defined as a body mass index greater than the 97th percentile (girls: 19.4 kg/m2 (5 years), 19.9 kg/m2 (6 years); boys: 19.2 kg/m2 (5 years), 19.8 kg/m2 (6 years)). We used the most recent German reference values that had been generated during the 1997 school health examination in Bavaria, where 115,530 German children in the age range of 5.006.99 years had been studied (3).
Questionnaire
The questionnaire was self-administered. The question on smoking was as follows: "Does the mother smoke now or did the mother smoke during any of the following time periods: in the childs first year of life, during breastfeeding, during pregnancy, in the year before pregnancy?" Each of these questions was supposed to be answered with "no" or "yes." If yes, the number of cigarettes smoked daily was asked for by categories of less than 10, 1020, and more than 20 for each time period separately. The main explanatory variable in this study was smoking during pregnancy; it was coded as one if the mother had smoked during pregnancy and as zero if the mother had never smoked.
We considered the following variables as potential confounders of the association between maternal smoking during pregnancy and childhood overweight/obesity:
Parental educationhighest level attained by either parent, ordinal in degrees (self-reported by parents; dichotomized to less than 10 years vs. 10 or more years) (11);
Parental obesitymetric self-reporting, height in cm and weight in kg (body mass index of 30 in either parent) (12, 13);
Single parenthooddichotomous (yes/no) (self-reported by parents) (14);
Population densityfrom statistical yearbook according to the region of the respective public health office (living in a region with 250 or more inhabitants/km2 vs. living in a region with less than 250 inhabitants/km2) (11);
Time of introduction of complementary foodscontinuous in months when introduced (self-reported by parents; dichotomized to before or after the fourth month of life) (15);
Caloric bottle to sleep in the first year of lifedichotomous (yes/no) (derived from five questions: tea without sugar, tea with sugar, juice, milk, other drinks) (self-reported by parents);
High birth weight (11)continuous measurements in kilograms from well-baby check-up book, dichotomized using cutoff points from German percentiles (90th percentile), accounting for sex and duration of pregnancy (16);
High weight gain during the first year of life1) weight at birth (a) and weight at about 1 year (b) from the well-baby check-up book measurements, 2) (difference of b a divided by the months of observation) multiplied by 12 to account for 1 year (12 months), 3) dichotomized by cutoff points at the third quartile (weight gain of 2.34 times the childs birth weight) (17);
Watching television or playing video gamesboth were asked for by hours per day (self-reported by parents) and cumulated by addition, with a cutoff point at 1 hour daily to allow for sufficient numbers in the respective categories (18, 19);
Regular sports activities in a clubdichotomous (yes/no) (self-reported by parents) (20);
Eating snacks while watching televisionordinal, with frequency per 5 day/week categories (self-reported by parents) dichotomized to never versus ever (21);
Having main meals aloneordinal, with frequency per 5 day/week categories (self-reported by parents) dichotomized to ever versus never;
Present total caloric intakefood frequency questionnaire with 64 kinds of food and options for usual portions per week and day (self-reported by parents), with the total daily caloric intake estimated from the "Bundeslebensmittelschlüssel," a data source of the average calorie content of different food items in Germany published by Statistical Office Germany, and dichotomized to above versus below the 90th percentile (1,921 kcal) (22);
Breastfeedingdichotomized to ever versus never from continuous reporting in months (0x months; self-reported by parents) (9); and
Having a warm meal for supperdichotomized to yes/no (self-reported by parents).
Statistical analyses
The prevalences of overweight and obesity were calculated by maternal smoking and the amount of cigarettes smoked. Crude and adjusted odds ratios and their respective confidence intervals for maternal smoking and overweight/obesity were calculated using logistic regression analysis. All covariates significantly associated (p < 0.05) with both maternal smoking and overweight/obesity were considered as potential confounders. We defined confounding by an at least 10 percent change of the odds ratio for maternal smoking during pregnancy and overweight or obesity when the potential confounder was added to the model of maternal smoking during pregnancy and overweight/obesity. To account for missing values that might potentially result in selection bias in the logistic regression model, we replaced all missing values for covariates with the respective means (23). The final logistic regression model was created by forward selection. For all the variables considered, we assessed potential multicollinearity (Pearsons correlation coefficient, Spearmans correlation coefficient, Pearsons contingency coefficient as appropriate). Multicollinearity was assumed if the respective coefficients exceeded 0.4. We considered a number of possible interactions (e.g., parental education and maternal smoking) in the association of the main exposure and covariates with the main outcome. All confounders and independent significant (p < 0.05) risk factors were included after excluding multicollinearity. All calculations were carried out with SAS version 6.12 software (SAS Institute, Inc., Cary, North Carolina).
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The prevalences of overweight and obesity for maternal smoking during pregnancy, expressed as percentages, increased with the amount of cigarettes: never smoked (overweight: 8.1, 95 percent CI: 7.2, 9.0; obesity: 2.2, 95 percent CI: 1.7, 2.7); less than 10 cigarettes daily (overweight: 14.1, 95 percent CI: 11.1, 17.7; obesity: 5.7, 95 percent CI: 3.7, 8.2); and 10 or more cigarettes daily (overweight: 17.0, 95 percent CI: 10.1, 26.2; obesity: 8.5, 95 percent CI: 3.7, 16.1). There was a dose response with respect to the numbers of cigarettes smoked (p < 0.001; Cochran-Armitage trend test).
The association of maternal smoking during pregnancy with a number of potential risk factors for overweight/obesity is shown in table 1. Most of these risk factors were associated with maternal smoking throughout pregnancy with the exceptions of living in a densely populated area, given a bottle containing milk or tea with carbohydrates to sleep, and a high present total caloric intake.
|
|
|
The final logistic regression model is shown in table 4. All interaction terms that were considered failed to meet the criteria for logistic regression models (p > 0.05; data not shown). The magnitude of the effect on obesity was highest for high parental body mass index, followed by high birth weight, maternal smoking during pregnancy, and watching television or playing video games for more than 1 hour daily. Parental education, breastfeeding, snacking in front of the television, and television watching or playing video games for more than 1 hour daily were confounders accounting for a more than 10 percent change of the odds ratio for maternal smoking during pregnancy and overweight/obesity. Although these factors reduced the crude odds ratios considerably from 1.97 (95 percent CI: 1.52, 2.56) to 1.43 (95 percent CI: 1.07, 1.90) for maternal smoking during pregnancy and overweight and from 2.96 (95 percent CI: 1.97, 4.46) to 2.06 (95 percent CI: 1.31, 3.23) for maternal smoking during pregnancy and obesity, these effects remained significant in the final logistic regression model.
|
When the 85th and 95th percentiles were used as is customary for epidemiologic studies in the United States, the results were similar: adjusted odds ratios of 1.42 (95 percent CI: 1.11, 1.82) for a body mass index of greater than the 85th percentile and 1.76 (95 percent CI: 1.23, 2.51) for a body mass index of greater than the 95th percentile.
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Similar effects of maternal smoking during pregnancy have been observed in two cohort studies. The first included only 530 children (8), however, and in the second on 11,359 young adults, adjustment was possible for only a limited number of potential confounders (24). Regarding the other risk factors considered in our study, the results match well with previous publications. Like others, we failed to find an association between caloric intake and childhood overweight/obesity (25), and the effect of regular sports activities did not remain significant in the final logistic regression model. Although some studies suggested a protective role for physical activity (20, 26, 27), recent studies have failed to find an association between activity-related energy expenditure and obesity in children (28). The effect of breastfeeding failed to remain significant after adjustment, as in another recent study (29). Genetic factors (13, 30, 31), estimated from the marker of parental obesity, were the most important predictors for childhood overweight and obesity. Highest parental education was another important predictor for overweight/obesity. Other questions to assess social class, family income in particular, are not answered satisfactorily in Germany (32). Asking for family income information may account for a selection bias by nonresponse. We therefore confined assessment of social class to the parents educational level. High birth weight was another important risk factor for overweight and obesity (11, 12, 33), underscoring the impact of genetic factors and prenatal priming on childhood overweight. The impact of television watching has been confirmed in numerous studies since its first description in 1985 (18, 19). Frequent consumption of snacks while watching television was another independent lifestyle factor that accounts for an increased risk of overweight in children that is amenable to prevention. A role for the consumption of snacks in childhood obesity has previously been suggested (12, 34).
The association between maternal smoking during pregnancy and childhood obesity may appear surprising with respect to the long-known association of maternal smoking during pregnancy and low birth weight (35, 36). A tempting explanation for the observed findings could be the recently described impact of catch-up growth in the first years of life on childhood obesity. These data have shown that children with catch-up growth had a considerably higher body mass index, skinfold thickness, and waist circumference at the age of 5 years (17). During the first year of life, there is rapid catch-up growth regarding weight in children of mothers who smoked during pregnancy (37, 38). A high weight gain was associated with an increased risk for overweight and obesity in our data as well. A high weight gain was highly correlated with birth weight (r = 0.68) and was therefore not included in the final logistic regression model. If weight gain instead of birth weight was included in the model, the odds ratio for maternal smoking throughout pregnancy changed only marginally, however, suggesting that catch-up growth does not explain the effect of maternal smoking during pregnancy.
There are a number of papers on the long-term effects of adverse exposures during pregnancy. Maternal smoking in pregnancy has been associated with the highest educational qualification achieved at the age of 23 years after adjustment for confounding due to socioeconomic factors (39). Data from the Dutch famine study showed increased obesity rates in recruits whose nutrition was deprived in the first half of pregnancy (40). Maternal dietary factors associated with smoking in pregnancy might be an explanation for the observed association between maternal smoking and overweight/obesity. Some women smoke in order to lose weight (41), and smoking has been associated with a poor diet (42).
Additionally, there are data from animal studies published over the last two decades that suggest another possible mechanism to attribute the effects of maternal smoking on obesity to nicotine inhaled by the mother. The offspring of pregnant rats exposed to an active component of tobacco smoke, nicotine, demonstrate both appetitive learning and attentional deficits (4345). These behavioral effects are associated with alterations of both the cholinergic and catecholaminergic neurotransmitter systems of the brain (43). Alterations of the cholinergic system have been linked to learning deficits, whereas the catecholaminergic system has been associated with the brains reward system (46). Therefore, it is postulated that exposure to nicotine in utero due to maternal smoking during pregnancy may result in persistent behavioral effects, including deficits in impulse control. As a result, food consumption and other appetitive behaviors may be under less control than in children of mothers who did not smoke during pregnancy.
Clinical observations by Kandel et al. (47) appear to support this concept. Children of mothers who smoke are more likely to smoke themselves than are children of fathers who smoke; daughters of mothers who smoked during pregnancy were four times more likely to smoke too.
There are some methodological constraints related to our study. Maternal smoking during pregnancy was ascertained retrospectively using a self-administered questionnaire. Validation of reported smoking using objective measures was not accomplished. Mothers appear to remember pregnancy-related issues including smoking rather well, however (48). Results from other studies suggest that self-reported smoking is accurate in general (49), although digit preference appears to be a problem if the precise number of cigarettes is an issue (50). Another study suggested that smoking during pregnancy is reported satisfactorily as well (51). In this study, five of 25 mothers claimed to have stopped smoking; however, they had critical cotinine concentrations in the saliva (51), suggesting that some smoking mothers will deny smoking in pregnancy. In our study, the proportion of mothers who admitted having smoked during pregnancy (11.2 percent) was much lower compared with figures from Sweden (52) (23 percent in 1991 and 21.8 percent in 1992), suggesting that some mothers may have falsely denied smoking during pregnancy. In particular, some of the mothers who reported smoking before pregnancy are likely to have smoked throughout pregnancy, and most are likely to have smoked until they knew that they were pregnant. Children of these mothers were excluded because of insufficient and unreliable information as to whether and when they stopped smoking during pregnancy. The mean birth weight of these children was between that of children whose mothers had never smoked and that of children whose mothers smoked throughout pregnancy. The prevalence of overweight/obesity in children of mothers who smoked before pregnancy but said they had stopped during pregnancy (overweight: 11.6 percent; obesity: 3.2 percent) was higher than in children of never-smoking mothers (overweight: 8.1 percent; obesity: 2.2 percent) but lower than in children of mothers who smoked throughout pregnancy (overweight: 14.6 percent; obesity: 6.1 percent).
Random misclassification of the outcome in the different centers might account for bias toward unity, although the nurses had been instructed to measure weight and height in a standardized manner.
Several other potential sources of bias have been considered. Causal inference from cross-sectional studies is limited because of potential bias due to reverse causation and nonrandomized exposure. In the case of maternal smoking in pregnancy and obesity in children aged 5 or 6 years, reverse causation is not an issue because pregnancy always precedes childhood, however.
Despite the outlined methodological constraints, we believe that our data are valid. The observed association between maternal smoking during pregnancy and childhood overweight/obesity may have important implications for the understanding of priming of the body composition later in life by factors acting early in development and for prevention of overweight and obesity. The size of the association between maternal smoking and childhood overweight/obesity in the final logistic regression model was comparable with that of other significant risk factors amenable to prevention, such as frequent television viewing, playing of video games, and frequent consumption of snacks while watching television. All three might therefore be worthwhile targets for preventive strategies.
![]() |
ACKNOWLEDGMENTS |
---|
![]() |
NOTES |
---|
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|