Maternal overweight before pregnancy and asthma in offspring followed for 8 years

Abstract

Objective:

The aim of this study was to investigate the association between maternal overweight before pregnancy and offspring asthma in an ongoing birth cohort study. Maternal overweight may affect the pulmonary and immunological development of the fetus in utero because of the increased levels of inflammatory factors associated with being overweight and thereby increase the asthma risk in childhood.

Design:

Birth cohort study with follow-up until 8 years of age.

Subjects:

The study population included 3963 children and their mothers who participated in the Prevention and Incidence of Asthma and Mite Allergy study.

Measurements:

Maternal overweight before pregnancy was defined as a body mass index (BMI) above 25 kg m−2. Data on wheeze, dyspnea and prescription of inhaled corticosteroids of the child were reported yearly by the parents in a questionnaire. Sensitization to inhalant allergens and bronchial hyperresponsiveness (BHR) were determined at 8 years. Effect modification by predisposition for asthma in the child was tested. Data were analyzed by logistic regression and generalized estimating equations analyses.

Results:

At 8 years, 14.4% (n=571) of the children had asthma. In total, 20.9% (n=830) of the mothers were overweight before pregnancy. In children predisposed for asthma (n=1058), maternal overweight before pregnancy was associated with an increased risk of asthma in the child at 8 years (OR=1.52, 95% CI: 1.05–2.18) after adjustment for confounding factors, birth weight and the child's BMI. No association was observed in children without a predisposition (OR=0.86, 95% CI: 0.60–1.23). There was no association with sensitization or BHR.

Conclusion:

Children with a predisposition for asthma may have a higher risk to develop asthma during childhood when their mothers are overweight before pregnancy, irrespective of the child's BMI.

Introduction

It has been hypothesized repeatedly that prenatal factors have a function in the development of asthma during childhood by prenatal influences on the development of the fetal lungs and the fetal immune system. Literature suggests a higher asthma risk in children who were exposed in utero to smoking, allergic reactions in the mother and certain nutrients.1, 2, 3 Maternal overweight is another factor that could influence the development of the lungs and immune system during fetal life and thereby affect the asthma risk during childhood.

Overweight has been associated with increased levels of proinflammatory cytokines, such as interleukin 6 and C-reactive protein, and leptin, also during pregnancy.4, 5, 6, 7 This way, children of overweight mothers are exposed to increased levels of proinflammatory factors during fetal life. These high levels of proinflammatory factors may affect the immunological and pulmonary development in the unborn child and possibly result in a higher risk of asthma symptoms after birth. As children of asthmatic parents are already at increased risk to develop asthma during childhood because of a genetic predisposition, these children may in particular be sensitive for high levels of proinflammatory factors.

Recently, Reichman and Nepomnyaschy8 showed that children of obese mothers were more likely to have asthma at age 3. In this study no distinction was made between children with and without a predisposition to develop asthma.

In an earlier study, we showed that overweight children have a higher risk to develop asthma and bronchial hyperresponsiveness (BHR).9 In this study, we investigate the association between maternal overweight before pregnancy and asthma symptoms in children in the first 8 years after birth and assessed effect modification by parental allergy and asthma. In addition, we studied BHR and sensitization at 8 years of age as outcome measures. Because maternal and child overweight are strongly correlated, we also studied to what extent the observed associations could be explained by body mass index (BMI) of the child.

Methods

Study design and study population

The study population consisted of 3963 Dutch children born in 1996–1997 who participated in the Prevention and Incidence of Asthma and Mite Allergy (PIAMA) birth cohort study. A detailed description of the study design has previously been published.10 Briefly, pregnant women were recruited from the general population by means of a validated screening questionnaire on maternal allergy,11 distributed to the women when visiting a prenatal clinic in the Netherlands. On the basis of this screening, 7862 women (2779 allergic mothers and 5083 nonallergic mothers) were invited to participate in the study. Approximately 50% of the invited pregnant women (n=4146) agreed for participation. Of multiple births, only one of the children was included in the study. After birth, the baseline study population consisted of 3963 children. Questionnaires were sent to the participating parents during pregnancy, at 3 months and yearly from 1 to 8 years of age, around the child's birthday.

At 8 years of age, a subgroup of the study population (n=1682), consisting of all children of allergic mothers (n=1076) and a random sample of the children of nonallergic mothers (n=606), was invited for a hospital-based medical examination when a blood sample was collected and BHR was determined. Of the invited children, 1236 participated. In this subgroup, 66.0% (n=816) of the children had an allergic mother compared to 31.2% (n=1237) in the total study population. The study protocol was approved by the medical ethics committees of the participating institutes, and all parents gave written informed consent.

Outcome assessment

In the yearly questionnaires, we asked the parents to report whether the child had an episode of wheeze, an episode of dyspnea or a prescription of inhaled corticosteroids for respiratory or lung problems prescribed by a medical doctor in the preceding year. In the PIAMA study, ‘asthma’ is defined as at least one episode of wheeze and/or at least one episode of dyspnea and/or a prescription of inhaled corticosteroids by a medical doctor. In addition, wheeze without a cold and dyspnea without exercise were studied as outcome variables.

In the collected blood samples at 8 years of age, we determined specific IgE on the following common inhalant allergens: house dust mite (Dermatophagoides pteronyssinus), cats, dogs, grass (Dactylis glomerata), birch and Alternaria alternata. Sensitization to inhalant allergens was defined as a specific IgE concentration of at least 0.70 IU ml−1 on at least one of the inhalant allergens. BHR was determined according to the protocol of the European Community Respiratory Health Survey,12 defined as a decrease of 20% in FEV1 at a cumulative dose of 0.61 mg methacholine bromide or below.

Anthropometric measures

In the questionnaire administered to the parents when the child was about 1 year of age, we asked the mother to report her current height (in cm) and we asked ‘Do you know how much you weighed before you became pregnant?’ She could answer ‘I do not know’ or report her weight (in kg). In the questionnaire administered when the child was 8 years of age, we asked the parents to report the current weight and height of the father. BMI was calculated as body weight in kilograms divided by height squared in meters ( kg m−2). Overweight was defined as a BMI above 25 kg m−2, moderate overweight as a BMI between 25 and 30 kg m−2 and obesity as a BMI above 30 kg m−2.

The child's body weight (in kg), height (in cm) and date when the child was last measured were reported yearly by the parents. We calculated gender-specific standard deviation scores (s.d.s.) of BMI for age using an external reference, the reference growth curves of the Dutch Fourth Nation-wide Growth Study carried out in 1997.13

Assessment of other variables

A predisposition for allergy in the child was defined as having at least one parent with an allergy. Maternal and paternal allergy were reported during pregnancy and were defined as current allergy to house dust mites or pets, current hay fever or ever asthma.

A predisposition for asthma in the child was defined as having at least one parent with current asthma. In the questionnaire administered 3 months after birth of the child, we asked the parents to report whether the mother or the father wheezed, had dyspnea, had an asthma attack or used inhaled medicine for breathing problems in the last 12 months. The parent was categorized as asthmatic when a positive answer was given on at least one of the items.

Maternal education, maternal smoking during pregnancy (any smoking by the mother during pregnancy after the fourth week of pregnancy), mode of delivery (cesarean section versus vaginal delivery) and the child's birth weight were reported by the parents. Maternal education was measured as the highest education completed and then divided into three categories (low, intermediate and high education). Total breastfeeding duration (in weeks) was assessed by questions on infant feeding in the questionnaires administered at 3 months and at 1 year.

Statistical analyses

Data analysis was conducted using SAS software version 9.1 (SAS Institute Inc., Cary, NC, USA). The associations between maternal overweight and maternal BMI and the outcome variables at 8 years of age were analyzed by logistic regression. In addition, we analyzed the association between maternal moderate overweight (versus normal weight) and the outcome variables, and the association between maternal obesity (versus normal weight) and the outcome variables. Also the association between paternal overweight (when the child was 8 years of age) and the outcome variables was assessed. Generalized estimating equations (GEE) were used to study the associations between maternal overweight and asthma longitudinally, taking into account the correlation between repeated measures in the same individual. A Toepitz working correlation structure fitted the data best. An interaction between maternal overweight and age was included in the GEE model to allow the association between maternal overweight and the outcomes to vary with age.

Maternal education, maternal smoking during pregnancy, smoking inside the house at 8 years, mode of delivery, breastfeeding duration and gender were considered as confounding factors, because these factors have been shown to be associated with childhood asthma in previous studies and may also be associated with maternal overweight. Only the variables that changed the association between maternal overweight and the outcome variables in children were included in the adjusted analyses. The associations were not routinely adjusted for the child's birth weight and BMI because these factors might be factors in the causal pathway. We therefore analyzed the associations with adjustment for the child's birth weight and BMI s.d.s. at 8 years of age as a sensitivity analysis. We choose to adjust for the child's BMI at 8 years of age because most outcomes were analyzed at 8 years of age and the associations between the outcome variables and BMI are most pronounced with current BMI of the child. Furthermore, we stratified the analyses on children with and without a predisposition for allergy and on children with and without a predisposition for asthma because these factors are potential effect modifiers. We tested the interaction between maternal overweight and the child's predisposition for allergy, and the interaction between maternal overweight and the child's predisposition for asthma. Effect modification by maternal allergy was analyzed because recruitment of the mothers was based on maternal allergy. P-values below 0.05 were considered to be statistically significant.

Missing data and multiple imputations

At 8 years of age, 8% (310/3963) of the children of the baseline study population were lost to follow-up. Of the children who were still participating in the PIAMA study at 8 years of age, 90% (3269/3653) completed and returned the questionnaire. For 470 children, data on maternal overweight before pregnancy (n=274), data on one of the outcome variables (n=55) or data on one of the confounder variables (n=141) were missing, leaving 2799 children available for the complete case analysis. Of the children with missing data, 34% missed only one variable.

Because in the PIAMA study data are unlikely to be ‘missing completely at random’, a complete case analysis may lead to biased results.14, 15 To avoid bias, we imputed missing data by ‘multiple imputation’. This technique uses information available in the data set to impute the missing data and is considered the best available method to deal with missing data.16 Missing data were imputed multiple times using the ‘Multivariate Imputation by Chained Equations’ procedure17 that runs under the statistical program R version 2.6.1 (www.R-project.org). After 50 iterations, convergence was achieved resulting in 5 imputed data sets. Each imputed data set was analyzed by standard complete data procedures, which ignore the distinction between real and imputed values. The results of the analyses were combined using PROC MIANALYZE in SAS. All analyses were performed on the complete case data and on the imputed data.

Results

At 8 years of age, 7.6% (n=301) of the children wheezed, 9.9% (n=394) had dyspnea, 7.3% (n=289) had a prescription of inhaled corticosteroids and 14.4% (n=571) had asthma in the last year. The prevalence of wheeze, dyspnea and asthma decreased from 3 to 8 years of age, whereas the prevalence of prescription of inhaled corticosteroids was constant (data not shown). At all ages, the prevalence of the outcome variables was higher in children who were predisposed to develop asthma (n=1058) than in children who were not predisposed to develop asthma (n=2905) (data not shown). Before pregnancy, 20.9% (n=830) of the mothers were overweight (Table 1).

Table 1 Descriptive statistics of the study population based on complete case data and imputed data

In the population as a whole, maternal overweight before pregnancy was nonsignificantly associated with an increased risk of wheeze, dyspnea, prescription of inhaled corticosteroids and asthma at 8 years of age. The odds ratio of the crude association between maternal overweight and asthma at 8 years in the total population was 1.28, 95% CI: 1.03–1.60, P=0.026. After adjustment for confounding factors (maternal education, maternal smoking during pregnancy, mode of delivery and breastfeeding duration; adjusted model 1), the odds ratio was 1.17, 95% CI: 0.93–1.46, P=0.179, and after additional adjustment for birth weight and the child's BMI (adjusted model 2), the odds ratio was 1.12, 95% CI: 0.89–1.41, P=0.348. The adjusted association between maternal obesity and asthma at 8 years was borderline significant: 1.46, 95% CI: 0.97–2.18, P=0.067.

There was effect modification by the child's predisposition for asthma (the child had at least one parent with asthma) (test for interaction P=0.05). In the children with a predisposition for asthma, we found a positive and significant association with wheeze, dyspnea, a prescription of inhaled corticosteroids and asthma at 8 years (Table 2). After adjustment for confounder variables and possible intermediate factors (birth weight and BMI of the child), the associations were somewhat attenuated. BMI of the child accounted for the greatest proportion in attenuation. In children without a predisposition for asthma, we observed no association between maternal overweight before pregnancy and any of the outcome variables at 8 years of age (Table 2). The interaction between the child's predisposition for allergy and maternal overweight was not significant (test for interaction P=0.95) as well as the interaction between maternal allergy and maternal overweight (test for interaction P=0.30).

Table 2 Prevalences and associations between maternal overweight (normal weight is the reference) and maternal BMI before pregnancy and outcomes at 8 years of age in children with and without a predisposition to develop asthma (imputed data, n=3963)

The child's risk of asthma increased with increasing maternal BMI in children with a predisposition for asthma (Table 2). Maternal obesity before pregnancy (versus normal weight) was more strongly associated with asthma at 8 years than maternal moderate overweight (versus normal weight). In children with a predisposition for asthma, we found that the adjusted odds ratio (model 2) was 2.43 95% CI: 1.27–4.65, P=0.008 for maternal obesity and 1.30 95% CI: 0.86–1.97, P=0.207 for maternal moderate overweight. Paternal overweight was not associated with any of the outcomes in children of asthmatic and nonasthmatic parents (data not shown).

The association between maternal overweight before pregnancy and asthma in children with or without a predisposition for asthma did not change with age of the child (Figures 1 and 2).

Figure 1
figure1

Adjusted (model 2) associations between maternal overweight before pregnancy and asthma from 3 to 8 years of age in children without a predisposition to develop asthma (n=2905).

Figure 2
figure2

Adjusted (model 2) associations between maternal overweight before pregnancy and asthma from 3 to 8 years of age in children with a predisposition to develop asthma (n=1058).

At 8 years of age, 31.3% (n=526) of the children were sensitized for at least one inhalant allergen and 43.3% (n=728) of the children had BHR. Table 3 presents the associations between maternal overweight before pregnancy and sensitization and BHR in children with and without a predisposition for asthma. There were no significant associations between maternal overweight before pregnancy and sensitization and BHR in either subgroup (Table 3).

Table 3 Prevalences and associations between maternal overweight and maternal BMI before pregnancy (normal weight is reference) and sensitization and BHR at 8 years of age in children with and without a predisposition to develop asthma (imputed data, n=1682)

The analyses presented in the text and tables are all based on imputed data. In Table 1, the descriptive statistics of the study population are presented based on the imputed data and the complete case data. This table shows that the population with imputed data (n=3963) differed only slightly from the complete case data (n=2799) with regard to the study characteristics. In the imputed data, the prevalence of smoking during pregnancy was somewhat higher and the mean duration of breastfeeding was lower than in the complete case data. Most associations differed slightly between the complete case data and the imputed data, but the conclusions remained similar. For example, the odds ratio of the crude association between maternal overweight before pregnancy and asthma at 8 years of age in children with a predisposition for asthma was 1.70, 95% CI: 1.20–2.39 in the imputed data and 1.58, 95% CI: 1.03–2.44 in the complete case data.

Discussion

Our longitudinal data showed that in children who were predisposed to develop asthma, because they had a least one asthmatic parent, exposure to maternal overweight during pregnancy was associated with an increased risk to develop asthma in childhood. The strength of the association increased with increasing maternal BMI. Although the association could partly be explained by confounding factors and the child's own weight status, children of overweight mothers still had a higher asthma risk than children of normal weight mothers. In contrast, in children without a predisposition to develop asthma the risk was not increased.

In the total population, maternal overweight was nonsignificantly associated with an increased asthma risk in offspring at 8 years of age, and the association between maternal obesity and childhood asthma was borderline significant. These results corresponded with the conclusions of Reichman and Nepomnyaschy8 in their paper. They observed an increased asthma risk at 3 years of age in children of obese mothers. The Reichman and Nepomnyaschy study did not stratify by parental asthma.

Strengths of this study are the longitudinal study design, the follow-up until 8 years of age with repeated data collection on the outcome variables, and the large study population with a low attrition rate. In addition to data on asthma symptoms, we collected data on prescription of inhaled corticosteroids and measured sensitization and BHR. The observed associations could not be explained by confounding factors such as breastfeeding and maternal education, because those variables were included in all analyses. We dealt with possible selection bias due to loss to follow-up or missing data on individual variables by multiple imputation of the missing data. To analyze the complete or available cases only, may not only affect precision but may also cause bias because the mechanism in which missing data occur is often not completely at random.16

A limitation of this study was that maternal weight before pregnancy and height were self-reported retrospectively when the child was 1 year of age. Weight is likely to be underreported among women. A study among Dutch women showed that the mean BMI based on reported weight and height was 0.6 kg m−2 lower than BMI based on measured data.18 The fact that weight was reported retrospectively may have further contributed to the underestimation of the weight data. This bias may have led to misclassification of maternal overweight and may have attenuated the association between maternal overweight and childhood asthma. The higher prevalence of maternal overweight among children with a predisposition for asthma compared with children without a predisposition for asthma could have influenced our results to some extent. However, it is unlikely that the large difference in the associations between maternal overweight and childhood asthma between children with and without a predisposition for asthma can be fully explained by maternal overweight. Our asthma definition was based on wheeze, dyspnea and prescription of inhaled corticosteroids reported by the parents. Although these important indicators for asthma in children are also common symptoms of respiratory infections in young children, wheeze, dyspnea and use of inhaled corticosteroids in children of 8 years of age are more suggestive of asthma than of infections. Furthermore, a feeling of dyspnea may be related to obesity-related physiological impairment and may not be indicative of asthma. However, the associations remained after adjustment for the child's BMI and the association between maternal overweight and dyspnea without exercise was in the same direction as dyspnea in general.

Potentially, our results could be due to bias when parents who are both asthmatic and obese would be more likely to observe or report asthma symptoms and medication use in their children. As shown, we did not find an association between maternal overweight and asthma in children with nonasthmatic parents, suggesting there is no tendency in overweight no-asthmatic mothers to report more asthma in their children. The relationship between maternal and child asthma is well established, as opposed to a relationship between maternal overweight before pregnancy and asthma in 8-year-old children, and we do not consider it likely that the relationship we found is primarily explained by differential awareness of this possible relationship between parents with and without asthma.

The child's birth weight and BMI are important intermediate factors in the association between maternal overweight and childhood asthma. Children of overweight mothers are born with a higher birth weight and are more at risk to develop overweight themselves. A high birth weight and childhood overweight are associated with an increased risk for the child to develop asthma.9, 19, 20, 21 When birth weight and the child's BMI were taken into account in our analyses, the associations attenuated but remained. This observation suggests that although part of the association between maternal overweight and childhood asthma runs through the child's own weight status, maternal overweight before pregnancy has an independent and lasting effect on the risk for childhood asthma, at least until 8 years of age. The results of the longitudinal analysis confirm that maternal overweight before pregnancy has a lasting effect on the asthma risk in the child. The figures show no attenuation of the effect of maternal overweight by age of the child.

Some residual confounding may still be present in the association between maternal overweight and the outcomes in children because reported weight and height are less optimal for the definition of the child's BMI compared to measured weight and height. At 4 years of age, a slight difference between measured and parental reported weight and height was observed in the children who participated in the PIAMA study.22 Furthermore, if the association between overweight and asthma in the child is mediated through increased levels of inflammatory factors, the actual risk measure of interest is total fat mass or percentage body fat, because the levels of inflammatory factors are increased by an increase in total fat mass. However, BMI is thought to be a valid proxy for fat mass in children, because of its strong association with total fat mass.23 Adjustment of the associations between maternal overweight and asthma outcomes in the child for the child's fat mass may result in a greater attenuation of the observed associations. In addition, we cannot exclude the possibility of residual confounding by factors that were not measured in our study, such as complications during pregnancy. However, important possible confounding factors, such as maternal smoking during pregnancy and breastfeeding duration, were included in our analyses and did not affect the associations to a large extent and did not change our conclusions.

We observed no association between maternal overweight and sensitization to inhalant allergens in the child at 8 years of age. In our study on childhood overweight and asthma, no association was observed with sensitization either, which was in accordance with two other studies.24, 25 It has been speculated that overweight increases the risk for nonatopic asthma, but does not affect atopic asthma.24 Also, we did not observe a significant association with BHR, although the child's BMI was associated with BHR in our earlier study. As we did not have information on sensitization and BHR in all children, the study population of children of asthmatic parents may have been too small to observe a significant effect.

In particular, parental asthma modified the asthma risk in children of overweight mothers, whereas parental allergy had only a minor effect. Parental allergy was mainly based on hay fever and allergy to pets and house dust mites. Possibly a predisposition for asthma and not allergy in general is needed to increase the asthma risk in children of overweight mothers.

This study fits with the hypothesis on fetal exposure and disease outcomes in later life and agrees with the results of other studies on fetal exposure and asthma in childhood.1, 2, 3 For example, studies on maternal nutrition during pregnancy showed that certain foods or nutrients decreased the risk of childhood asthma.26, 27, 28

Challier et al.7 showed that pregnant obese women have higher serum levels of proinflammatory cytokines than normal weight pregnant women. In the same study, the authors reported that obese pregnant women had an increased inflammatory response in the placenta compared with normal weight women, which results in an inflammatory environment in utero. If a fetus is exposed to the increased inflammatory state due to the increased fat mass of the mother, this might affect the fetus’ intrauterine immunological or pulmonary development adversely. The high levels of inflammatory factors may in particular affect the intrauterine immunological or pulmonary development of a child with a genetic predisposition to develop asthma. However, insight in the biological mechanism behind the relation with fetal immunological or pulmonary development is still lacking. Besides the increased systemic inflammatory state of obese women, other metabolic or hormonal factors associated with obesity, including high glucose, insulin and lipid levels, could affect fetal development.29

In conclusion, children with a predisposition to develop asthma, because at least one of the parents has asthma, may have a higher risk to develop asthma during childhood when their mothers are overweight before pregnancy, irrespectively of the child's own weight status. Future studies that contain detailed data on the immunological status of the mother during pregnancy or the presence of inflammatory factors in cord blood may give insight in the underlying mechanism of the association between maternal overweight and asthma in offspring.

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Acknowledgements

This work was supported by the Netherlands Organisation for Health Research and Development, the Netherlands Asthma Foundation, the Netherlands Ministry of Health, Welfare and Sport and Numico Research, the Netherlands. The funding source had no involvement in the study design, in the collection of the data, data analysis, interpretation of the data, writing the report and in the decision to submit the paper for publication.

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Scholtens, S., Wijga, A., Brunekreef, B. et al. Maternal overweight before pregnancy and asthma in offspring followed for 8 years. Int J Obes 34, 606–613 (2010). https://doi.org/10.1038/ijo.2009.194

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Keywords

  • overweight
  • pregnancy
  • asthma
  • birth cohort study

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