AJCN EB Program 2010
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Mendez, M. A
Right arrow Articles by Sunyer, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Mendez, M. A
Right arrow Articles by Sunyer, J.
Agricola
Right arrow Articles by Mendez, M. A
Right arrow Articles by Sunyer, J.
American Journal of Clinical Nutrition, Vol. 87, No. 6, 1906-1913, June 2008
© 2008 American Society for Nutrition

ORIGINAL RESEARCH COMMUNICATION

Maternal smoking very early in pregnancy is related to child overweight at age 5–7 y1,2,3

Michelle A Mendez, Maties Torrent, Carlos Ferrer, Nuria Ribas-Fitó and Jordi Sunyer

1 From the Centre de Recerca en Epidemiologia Ambiental, Institut Municipal d'Investigació Médica, Barcelona, Spain (MAM, CF, NR-F, and JS), CIBER Epidemiologia y Salud Pública, Spain (MAM and JS), and Àrea de Salut de Menorca, Ib-Salut, Menorca, Spain (MT)

2 Supported by grants from the Spanish Ministry of Health (FIS-97/0588, FIS-00/0021-02), Instituto de Salud Carlos III (Red INMA G03/176), Fundació La Caixa (00/077-00), and European Commission (Concerted Action, contract number QLK4-2000-00263). MAM received funding support from the EU sixth framework project EARNEST FOOD-CT-2005-007036.

3 Address reprint requests and correspondence to MA Mendez, Centre de Recerca en Epidemiologia Ambiental, 88 Dr. Aiguader Street, Barcelona, Spain 08003. E-mail: mmendez{at}imim.es.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Despite being associated with lower birth weight, maternal smoking in the last 2 trimesters of pregnancy has been associated with increased risk of offspring overweight in several studies. To date, only one study has examined whether smoking in the first trimester only, which is not associated with birth weight, is also associated with childhood overweight.

Objective: This study uses prospective data to examine associations between maternal smoking in the first compared with later trimesters of pregnancy and child overweight at age 5–7 y.

Design: Data from a prospective cohort of 369 Spanish children born in 1997–1998 were used. Logistic regression was used to estimate associations between maternal smoking during different time periods and odds of child overweight later in life.

Results: Maternal smoking during the first trimester was more strongly associated with overweight (adjusted odds ratio: 2.65; 95% CI: 1.26, 5.54) than smoking later in pregnancy (1.88, 0.85, 4.15). Smoking limited to the first month of pregnancy was also associated with child overweight. Neither paternal smoking nor maternal smoking before or after pregnancy was associated with child overweight. Significant interactions with breastfeeding duration indicated that first-trimester smoking was associated with overweight only among children breastfed for <6 mo, suggesting prolonged breastfeeding may help to counter adverse effects of smoking in early pregnancy.

Conclusions: These data suggest maternal smoking very early in pregnancy may increase risk of later overweight in children and provide further support for promoting smoking cessation before rather than during early pregnancy. Further studies are needed to confirm these results.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
During the past few decades, levels of childhood obesity worldwide have escalated (1). Within Europe, current levels are especially high in southern countries, including Spain and Italy (2). These trends are problematic because childhood overweight is strongly associated with adult obesity and chronic disease risk (3). Recent evidence suggests growth trajectories leading to overweight and obesity may begin very early in life, with strong associations between rapid growth in early infancy and overweight later in childhood and adolescence (4). As a result of this data, a growing body of literature has begun to explore whether in utero exposures may influence long-term risk of obesity (5, 6).

Maternal smoking during pregnancy is one prenatal exposure hypothesized to influence child obesity risk and has been associated with greater overweight, body mass index (BMI), or weight in numerous studies (6-25), with few exceptions (26). Smoking in pregnancy is associated with lower birth weights (27). Whereas higher birth weights tend to be associated with later obesity (5), smaller size at birth has also been associated with increased adiposity and central fatness in later life (5). It has been hypothesized that metabolic adaptations linked to maternal smoking may promote prenatal growth retardation through pathways that may increase risk of obesogenic growth in the postnatal environment (9).

Previous studies (27, 28) suggest that although smoking throughout or in late pregnancy adversely affects fetal growth, smoking limited to early pregnancy has little effect on size at birth. It is uncertain how the timing of exposure to maternal smoking may be relevant for obesity risk in offspring. The majority of studies have defined exposure based on smoking at any time in pregnancy, or based on assessments made at variable times in the course of pregnancy, usually in the second or third trimester (9-11). However, one prospective study (16) in which virtually all mothers who smoked in pregnancy did so exclusively in the first trimester (T1), with no smoking in the second and/or third trimesters (T2/3), reported significantly more overweight at age 3 y associated with maternal smoking. Another cross-sectional study (20) reported that obesity at 5–6 y was associated with recalled smoking either exclusively in T1 or throughout pregnancy, with somewhat stronger associations for T1 smoking. Despite the promotion of smoking cessation for women planning to conceive, a substantial proportion of women smoke in early pregnancy (29, 30). Therefore, studies are needed to determine whether smoking in early pregnancy may affect risk of future disorders, including obesity, in children.

In this study we assess associations between maternal smoking in different trimesters of pregnancy and risk of child overweight at age 5–7 y by the use of data from a population-based prospective pregnancy cohort from the Spanish island of Menorca.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study participants
Data come from the Menorca cohort of the Asthma Multicenter Infant Cohort Study, which enrolled 95% of pregnant women receiving prenatal care at a primary care center over 12 mo in 1997–1998. Details on the protocol have been described previously (31). Briefly, 482 women were recruited early in T2, at around 20 wk of gestation. Mothers provided signed informed consent, and the study was approved by the ethics committee of the Institut Municipal d'Investigació Mèdica. Data on infant characteristics were collected at birth, 6 mo, and 1 y. Four hundred twenty-two (87.6%) children were included in a follow-up survey at age 5–7 y in which height and weight were measured. Preterm births (n = 23) were excluded because catch-up growth patterns vary compared with term births (32). An additional 30 children were excluded from the analysis sample (n = 369, 76.5% of baseline) because of missing covariate data (maternal overweight, social class, and breastfeeding). There were no differences among those lost to follow-up or excluded in terms of maternal smoking in pregnancy, other maternal characteristics (age, social class, overweight/obesity), birth weight (among full-term infants), breastfeeding duration, or father's smoking habits (chi-square or t test P values not statistically significant).

Study variables
At recruitment, interviewer-administered questionnaires were used to collect data from mothers on maternal age, social class (from maternal occupation based on the UK Registrar General classification system: professional; managerial/technical; and manual skilled, partially skilled or unskilled) (33), parity, cigarette-smoke exposure, self-reported prepregnancy weight, and diet in pregnancy estimated through use of a 50-item semiquantitative food frequency questionnaire (34). Maternal height was measured by trained interviewers by use of standard techniques. Infant height and weight were obtained by trained nurses at birth. Infant feeding practices, including breastfeeding duration, were reported by mothers in interviews at 6 mo and 1 y postpartum. At 5–7 y, child weight and height, without shoes and in light clothing, was measured by trained interviewers through the use of standard techniques. Questionnaires on children's usual diets in the past year (a validated 100-item food frequency questionnaire) (35) and physical activity patterns (hours per week of TV watching and participation in sports) were also administered to mothers at this time.

Child overweight/at-risk of overweight (hereafter "overweight") was defined based on BMI (in kg/m2) through use of the age- and sex-specific 85th percentile of the World Health Organization/National Center for Health Statistics reference as the cutoff (36). BMI z-scores were also calculated through the use of this reference. To examine relations between maternal smoking and height compared with weight growth, mean annual changes in height and weight since birth were calculated by dividing the change in each measure by the exact age at the 5–7 y interview. Changes in sex-specific height-for-age and weight-for-age percentiles from birth to the time of interview were also calculated.

Maternal smoking in pregnancy was defined based on self-reported habits at recruitment, which included questions about past smoking as well as cessation before or in months 1, 2, or 3 of pregnancy. Women were initially defined as never-smokers, past smokers who stopped before pregnancy, smokers who stopped during T1, and current smokers at recruitment in T2. Because overweight in offspring of never-smokers and past smokers who stopped before pregnancy were similar (see results), these groups were combined in the main models. To assess whether associations with timing of smoking in pregnancy were explained by differences in the lifetime duration of smoking, timing was further stratified based on whether women reported having smoked for ≤10 y compared with 11+ y (roughly the median). Women were also classified based on smoking at any time during pregnancy (yes/no).

The primary covariates included (1) maternal characteristics potentially associated with child obesity [age, social class, parity, prepregnancy overweight (BMI ≥25 and <30)] and obesity (BMI ≥30); (2) child sex, birth weight, and current age at measurement; and (3) infant feeding patterns that may influence obesity (breastfeeding duration ≥the recommended 6 mo). Current maternal smoking (yes/no) at age 5–7 y, as well as paternal smoking in pregnancy and at follow-up (coded as for mothers), were included as covariates to assess confounding by passive smoke exposure. Measures of children's current diet (percentage of energy from fat, grams of meat intake in tertiles) and activity patterns (low/medium/high weekly hours of television viewing and sports/exercise) were also examined as potential confounders, but adjusting for these variables had no meaningful effect (ie, odd ratios changed by <5%). Similarly, several other variables were excluded from the final models because they had no meaningful effect, including smoking by other members of the household (3.4% of women); degree of tobacco smoke exposure at work (none, sporadic, little, substantial, do not work); alcohol consumption in pregnancy (18.8% of women); health conditions such as gestational diabetes, hypertension, and anemia; and interconceptional interval (firstborn, 1–3 y, 4–5 y, 6 y+). Excluding or adjusting for twin births (n = 6) also had no effect.

Statistical analysis
Characteristics of the sample according to maternal smoking habits in pregnancy were compared through use of chi-square tests and analysis of variance (P < 0.05 significant). Patterns in girls and boys were examined separately and did not differ from those presented for the overall sample (not shown).

Analysis of overweight
Multivariate logistic regression was used to examine associations between maternal smoking in pregnancy and child overweight at 5–7 y, adjusting in a series of models for (1) child age and sex, (2) the primary covariates listed earlier, and (3) additionally adjusting for current maternal smoking. In supplementary models, we examined effects of adjusting for paternal smoking. Because these adjustments had no meaningful effect, paternal smoking variables, which had additional missing values (n = 17), were not included in all models (see results). Similarly, adjusting for maternal education in addition to social class did not change effect estimates (not shown). Odds ratios (ORs) with 95% CIs are reported for each measure of maternal smoking (smoking in different trimesters, any smoking during pregnancy). ORs presented in the text are fully adjusted unless otherwise specified. We decided a priori to examine interactions between maternal smoking and breastfeeding duration because differential effects of breastfeeding in smoking compared with nonsmoking mothers were reported in a recent study (37) of child overweight. Moreover, one of the hypothesized mechanisms linking maternal smoking to child overweight involves impaired programming of appetite control, whereas breastfeeding is postulated to play a protective role in the programming of appetite (38). Interactions with sex were also examined but were not significant (not shown).

Analysis of birth weight, BMI z-scores, and weight-compared-with-height growth since birth
Multivariate linear regression was used to examine relations between maternal smoking in pregnancy and children's birth weight, BMI z-scores at age 5–7 y, and mean changes in weight and height since birth (absolute changes/y and age-sex specific percentile changes). Coefficients and standard errors from these models reflect the mean difference in each outcome associated with the relevant smoking variable. Birth weight models were adjusted for the maternal characteristics listed previously, child sex, and analyses of BMI z-scores; weight and height change models also included current child age, birth weight and height, and breastfeeding duration.

Model diagnostics included confirming results were similar after: excluding potentially influential observations identified the use of {Delta}-betas; excluding subjects with large (>2.0 SD) annual height and weight changes; and additionally adjusting for or excluding low birth weight (n = 17) infants (not shown). Similar results were also obtained through use of log-transformed variables for continuous outcomes or through use of BMI rather than BMI z-scores (not shown). The use of International Obesity Task Force (IOTF) cutoffs to define child overweight and obesity (39) yielded similar results. All analysis used STATA (version 8.1; STATACORP, College Station, TX).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Overall, 36.0% of mothers in the analysis sample smoked at some time during pregnancy; 15.7% reported smoking in T1 only. At age 5–7 y, 27.4% of the sample (30.0% of boys and 24.9% of girls) were overweight, with slightly lower estimates through use of the IOTF cutoffs (23.6% overweight/obese).

Table 1Go characterizes the sample according to maternal smoking habits in pregnancy. Child overweight prevalence was higher among mothers who smoked in pregnancy than among nonsmokers (chi-square P < 0.05), with the highest prevalence (39.7%) among mothers who smoked in T1 only. Smoking during pregnancy was also associated with lower weights and heights at birth (t test P < 0.05). However, these deficits were limited to offspring of women who smoked beyond T1 (deficit in weight –197 g; t test P < 0.05 for 2-way comparison), with no deficit if mothers smoked in T1 only (–23g; t test P > 0.10). Overall, about one-third (38.5%) of women reported breastfeeding for at least 6 mo, with significantly lower rates among mothers who smoked in pregnancy (chi-square P < 0.05).


View this table:
[in this window]
[in a new window]

  		TABLE 1. Sample characteristics by maternal smoking habits in pregnancy

 
Multivariate associations between smoking in pregnancy and overweight
Maternal smoking in T1 was associated with a more than 2-fold increase in odds of overweight at age 5–7 y after multivariate adjustment, with weaker, nonsignificant associations for smoking later in pregnancy (Table 2Go). Restricting early smoking to women who reported smoking cessation in the first month of pregnancy (77.6% of T1 smokers) had little effect (OR: 2.96; 95% CI: 1.33, 6.53). Additional models were run excluding adjustment for birth weight, because it is uncertain whether size at birth is on the causal pathway between maternal smoking and child overweight, with little effect on associations for T1 smoking (fully adjusted OR: 2.64, 1.27, 5.50; for T2/3 smoking 1.62; 0.74, 3.55). Associations were similar through use of IOTF overweight definitions (OR for T1 smoking 2.77; 1.28, 5.95; for T2/3 smoking 2.02, 0.89, 4.62). After further stratifying timing of smoking by lifetime duration of smoking, smoking in T1 remained strongly and significantly associated with child obesity (OR for ≤10 y smoking: 3.5; 1.1, 11.6; for 11+ y smoking 2.5, 1.1, 6.0). Associations with T2/3 smoking remained more modest and did not reach significance regardless of duration (OR for ≤10 y: 1.7; 0.5, 5.1; for 11+ y: 1.8; 0.7, 4.8).


View this table:
[in this window]
[in a new window]

  		TABLE 2. Associations between maternal smoking habits and child overweight at 5–7y1

 
Associations between parental smoking and child overweight were specific to maternal smoking during pregnancy. Although correlated with smoking in pregnancy (Spearman's r = 0.69), current maternal smoking was not associated with child overweight (Table 2Go; Figure 1Go). Furthermore, in models separating never from past smokers, smoking before pregnancy was not associated with child overweight (Figure 1Go). Similarly, paternal smoking, either in pregnancy or currently, was not associated with child overweight (Figure 1Go).


Figure 1
View larger version (6K):
[in this window]
[in a new window]

  		FIGURE 1.. Associations between parental smoking and child overweight at age 5–7 y from multivariate logistic regression models: odds ratios and 95% CIs. Referent is never-smokers for mothers, nonsmokers for fathers. Adjusted for child age, sex, birth weight, breastfeeding duration, as well as maternal age, height, prepregnancy overweight or obesity, education, parity, and other smoking variables shown. Y axis on logarithmic scale.

 
Effect of breastfeeding duration on associations with child overweight
Because there were significant interactions between T1 smoking and prolonged breastfeeding (interaction P < 0.05), associations were examined in models stratified by breastfeeding duration. Among children breastfed <6 mo, T1 smoking was strongly associated with overweight at 5–7 y (Table 2Go). However, there was no clear association in children breastfed ≥6 mo.

Similar results were obtained in linear models through use of BMI z-scores at 5–7 y as a continuous outcome (interaction P < 0.05 for early smoking x breastfeeding duration). Among children breastfed <6 mo, maternal smoking in T1 was associated with higher BMI z-scores (multivariate-adjusted β ± SE 0.51 ± 0.18, P < 0.05). In contrast, among children breastfed for ≥ 6 mo, T1 smoking was associated with lower BMI z-scores (multivariate-adjusted β ± SE – 0.46 ± 0.30, P < 0.10). Smoking later in pregnancy was associated with higher BMI z-scores at 5–7 y, although coefficients were not as large (overall multivariate-adjusted β ± SE 0.31 ± 0.12, P < 0.05) as those for smoking in T1 in children breastfed <6 mo.

Smoking in pregnancy and birth weight, postnatal height, and weight growth
Maternal smoking later in pregnancy was associated with lower birth weight (in grams) after multivariate adjustment (β ± SE – 222.2 ± 54.5, P < 0.05), with no effect of smoking in T1 only (β ± SE – 35.2 ± 59.8, P > 0.10). Similar associations with smoking in late pregnancy, but not in T1, were observed for height at birth (not shown).

Associations between smoking in early pregnancy and mean annual postnatal weight gain also varied depending on the duration of breastfeeding (interaction P < 0.05). Among children breastfed <6 mo, children of T1 smokers had higher postnatal weight gains than did offspring of nonsmokers, despite having similar birth weights (Table 3Go; P < 0.05). However, among children breastfed ≥6 mo, postnatal weight gain was not associated with maternal smoking in early pregnancy. Moreover, T1 smoking was not associated with postnatal height growth. Smoking later in pregnancy was nonsignificantly associated with increases in postnatal weight gain and was not associated with postnatal changes in height. Results were similar when changes in weight-for-age and height-for-age percentiles were analyzed (not shown).


View this table:
[in this window]
[in a new window]

  		TABLE 3. Associations between maternal smoking in pregnancy and annual height and weight growth1

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this longitudinal cohort from Spain, maternal smoking in T1 of pregnancy was associated with increased child overweight at 5–7 y, independent of socioeconomic status, parity, maternal obesity, and birth weight. This association was observed even among children whose mothers reported smoking in only the first month of pregnancy. Although more prevalent in this sample, maternal smoking later in pregnancy was not clearly associated with overweight at age 5–7 y; overweight among children in this group was only slightly higher than among children of nonsmoking mothers. Associations between smoking in late pregnancy and child obesity were somewhat smaller in magnitude and did not reach significance, despite the higher prevalence of smoking later in pregnancy than smoking in T1 only. These findings are consistent with a previous cross-sectional study(20) that reported stronger associations between child obesity and maternal smoking in T1 than in later trimesters, and another (16) that found increased obesity associated with maternal smoking in T1. We found no association with smoking before pregnancy (16), findings that agree with earlier studies. Thus, these results suggest that smoking cessation before rather than early in pregnancy may be necessary to reduce risk of future obesity in offspring.

These data also suggest that prolonged breastfeeding may reduce risk of child obesity associated with smoking in early pregnancy. In this sample, smoking in T1 was associated with overweight only in children breastfed <6 mo, as a consequence of relatively large postnatal gains observed in weight but not in height. It is important to note that when classified simply as any compared with no smoking, as in the majority of existing studies, interactions between smoking in pregnancy and breastfeeding duration were not significant. Indeed, children whose mothers continued to smoke later in pregnancy gained slightly more weight between birth and age 5–7 y than children of nonsmokers, regardless of breastfeeding duration. To our knowledge, this finding has not been reported in previous studies on smoking in pregnancy and child obesity and should be explored in future studies.

Consistent with these findings, numerous studies have reported more rapid growth in the first 2 y of life in children whose mothers smoked in pregnancy, often characterized as catch-up growth (15, 40). However, as reported elsewhere, smoking in T1, unlike smoking later in pregnancy, was not associated with lower weight or height at birth (27, 28). These data suggest that maternal smoking in early pregnancy may be associated with developmental changes that predispose these offspring to rapid postnatal growth, whether or not catch-up is warranted. In recent studies, rapid growth in early life has been consistently related with later overweight, independently of birth weight (4, 40).

The mechanisms through which smoking in pregnancy may promote offspring weight gain and obesity are uncertain. It has been hypothesized that maternal smoking may alter fetal energy metabolism to adapt to smoking-related hypoxia, perhaps including influences on appetite via effects on hypothalamic centers, analogous to hypothesized effects of nicotine withdrawal in adults (16, 41). Animal studies provide some support for a relation. Higher postnatal weight and fat gains were observed starting at 10 wk postpartum in rat offspring exposed to nicotine in gestation (42). Metabolic changes consistent with risk of diabetes and obesity, including impaired glucose tolerance and increased β-cell apoptosis, have also been observed in offspring of rats injected with nicotine during gestation (43). Conversely, in adult rats, initiating cigarette smoke exposure has been found to reduce appetite and promote weight and fat mass loss (44, 45). Given recent evidence that prolonged breastfeeding may help to regulate appetite control, it is possible that this mode of feeding may partly counter any adverse effects of intrauterine nicotine exposure (38, 41), although the absence of associations between maternal T1 smoking and overweight among children breastfed for the recommended 6 mo may also be the result of other differences in care or feeding practices. Despite the lack of clear mechanisms, one recent study (13) found that maternal smoking in pregnancy was associated with higher fat mass measured by dual-energy X-ray absorptiometry as well as with higher BMI at age 9.9 y. That study did not explore effects of different smoking behaviors over the course of pregnancy but stated that mothers reported relatively stable habits (18.1% smoked in T1, 14.0% in 2T, and 14.3% in 3T).

This study has several limitations, notably the modest sample size, as a result of which the number of children exposed to smoking in T1 only was small. Confirmation, particularly of interactions with breastfeeding, is needed in future studies. It is possible that associations between child overweight and smoking in later pregnancy did not reach significance because of inadequate statistical power. Nonetheless, despite the higher prevalence of more prolonged smoking, the magnitude of associations for smoking later in pregnancy was consistently smaller than those for T1 smoking, as reported in a previous study (20). Although attrition was modest, given the small sample size we assessed possible effects in a sensitivity analysis by estimating associations alternatively, assigning all children lost to follow-up to either the overweight or nonoverweight categories. Because mothers of most children lost to follow-up did not smoke in pregnancy (59.0%), assuming all these children were overweight slightly attenuated associations (adjusted OR for T1 smoking: 2.57; 1.29, 5.11 if breastfed <6 mo). Assuming all children were normal weight had little effect (OR: 3.58; 1.71, 7.51).

Another limitation is that smoking habits were self-reported, which may underestimate levels of active smoking (46). However, an important strength is that maternal smoking habits were assessed early in T2 of pregnancy, 6 y before children's weight status. Given the prospective design, it seems probable that any misclassification of maternal smoking is nondifferential and unlikely to exaggerate associations. We were also unable to satisfactorily separately examine effects of heavier compared with lighter smoking in late pregnancy because few women reported moderately heavy smoking (n = 9 women in the analysis sample used >10 cigarettes/d; n = 28 smoked >5 cigarettes/d) (15, 27). Adjusting for number of cigarettes/day did not affect ORs for T1 smoking. However, maternal smoking >5 cigarettes/d appeared to be more strongly associated with odds of later obesity than did less intensive smoking (multivariate-adjusted OR: 1.90; 0.75, 4.33 for ≤5/d; OR: 2.68; CI 0.89, 8.02 for >5/d).

An important strength is the availability of data on paternal smoking in pregnancy and smoking habits of both parents at follow-up. We found no association between a father's smoking during the mother's pregnancy and child overweight or BMI z-scores, and there was no heterogeneity by breastfeeding duration (not shown). Similarly, neither maternal nor paternal smoking at 5–7 y was related to child overweight or BMI. Accordingly, adjusting for these passive-smoking measures had little effect on relations with maternal smoking in pregnancy. Thus, unlike a previous study (13), which found slight increases in childhood BMI associated with paternal smoking in pregnancy, these data suggest effects specific to maternal smoking during gestation.

These findings provide additional support for promoting smoking cessation before conception among women planning a pregnancy. However, given the fairly small sample size and limited follow-up time, additional studies are needed to confirm whether smoking early in pregnancy may increase risk of overweight that persists beyond childhood years. Studies are also needed to explore associations between smoking early in pregnancy and other obesity-related health outcomes. Findings from the British Longitudinal Birth Cohort suggest that maternal smoking at some time in pregnancy may be related to obesity and diabetes in adulthood (17, 47). Other researchers (9, 16) have reported maternal smoking in pregnancy to be associated with small increases in childhood blood pressure, although associations were not significant after adjusting for current weight or BMI. Additional studies are needed to assess directly whether smoking in early pregnancy appears to increase long-term risk of these and other obesity-related disorders as well as with obesity per se.


   ACKNOWLEDGMENTS
 
We are grateful to Raquel Garcia Esteban for data management and statistical support and to Maria Victoria Iturriaga for coordinating/conducting the fieldwork.

The authors’ responsibilities were as follows—MAM: conceived the hypotheses and the analysis plan, undertook the analysis, and wrote the manuscript; MT and JS: developed and supervised the fieldwork, undertook preliminary work examining smoking patterns in pregnancy in this cohort, and reviewed the manuscript; CF helped conduct the literature review and reviewed the manuscript; NR-F and JS reviewed the analysis plan, preliminary and final results, and reviewed/edited the manuscript. All authors approved the final version of the manuscript. None of the authors had a conflict of interest, financial or otherwise.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 2006;295:1549–55.[Abstract/Free Full Text]
  2. Lobstein T, Frelut ML. Prevalence of overweight among children in Europe. Obes Rev 2003;4:195–200.[Medline]
  3. Reilly JJ. Descriptive epidemiology and health consequences of childhood obesity. Best Pract Res Clin Endocrinol Metab 2005;19:327–41.[Medline]
  4. Baird J, Fisher D, Lucas P, Kleijnen J, Roberts H, Law C. Being big or growing fast: systematic review of size and growth in infancy and later obesity. BMJ 2005;331:929.[Abstract/Free Full Text]
  5. Oken E, Gillman MW. Fetal origins of obesity. Obes Res. 2003;11:496–506.[Medline]
  6. Huang JS, Lee TA, Lu MC. Prenatal programming of childhood overweight and obesity. Matern Child Health J 2007;11(5):461–73.[Medline]
  7. Adams AK, Harvey HE, Prince RJ. Association of maternal smoking with overweight at age 3 y in American Indian children. Am J Clin Nutr 2005;82:393–8.[Abstract/Free Full Text]
  8. Bergmann KE, Bergmann RL, von Kries R, et al. Early determinants of childhood overweight and adiposity in a birth cohort study: role of breast-feeding. Int J Obes Relat Metab Disord 2003;27:162–72.[Medline]
  9. Blake KV, Gurrin LC, Evans SF, et al. Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum Dev 2000;57:137–47.[Medline]
  10. Chen A, Pennell ML, Klebanoff MA, Rogan WJ, Longnecker MP. Maternal smoking during pregnancy in relation to child overweight: follow-up to age 8 years. Int J Epidemiol 2006;35:121–30.[Abstract/Free Full Text]
  11. Dubois L, Girard M. Early determinants of overweight at 4.5 years in a population-based longitudinal study. Int J Obes (Lond) 2006;30:610–7.[Medline]
  12. Hill SY, Shen S, Locke WJ, Rickin E, Lowers L. Offspring from families at high risk for alcohol dependence: increased body mass index in association with prenatal exposure to cigarettes but not alcohol. Psychiatry Res 2005;135:203–16.[Medline]
  13. Leary SD, Smith GD, Rogers IS, Reilly JJ, Wells JC, Ness AR. Smoking during pregnancy and offspring fat and lean mass in childhood. Obesity (Silver Spring) 2006;14:2284–93.[Medline]
  14. Al Mamun A, Lawlor DA, Alati R, O'Callaghan MJ, Williams GM, Najman JM. Does maternal smoking during pregnancy have a direct effect on future offspring obesity? Evidence from a prospective birth cohort study. Am J Epidemiol 2006;164:317–25.[Abstract/Free Full Text]
  15. Nafstad P, Jaakkola JJ, Hagen JA, et al. Weight gain during the first year of life in relation to maternal smoking and breast feeding in Norway. J Epidemiol Community Health 1997;51:261–5.[Abstract/Free Full Text]
  16. Oken E, Huh SY, Taveras EM, Rich-Edwards JW, Gillman MW. Associations of maternal prenatal smoking with child adiposity and blood pressure. Obes Res 2005;13:2021–8.[Medline]
  17. Power C, Jefferis BJ. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol 2002;31:413–9.[Abstract/Free Full Text]
  18. Salsberry PJ, Reagan PB. Dynamics of early childhood overweight. Pediatrics 2005;116:1329–38.[Abstract/Free Full Text]
  19. Toschke AM, Koletzko B, Slikker W Jr., Hermann M, von Kries R. Childhood obesity is associated with maternal smoking in pregnancy. Eur J Pediatr 2002;161:445–8.[Medline]
  20. Toschke AM, Montgomery SM, Pfeiffer U, von Kries R. Early intrauterine exposure to tobacco-inhaled products and obesity. Am J Epidemiol 2003;158:1068–74.[Abstract/Free Full Text]
  21. Vik T, Jacobsen G, Vatten L, Bakketeig LS. Pre- and post-natal growth in children of women who smoked in pregnancy. Early Hum Dev 1996;45:245–55.[Medline]
  22. von Kries R, Koletzko B, Sauerwald T, et al. Breast feeding and obesity: cross sectional study. BMJ 1999;319:147–50.[Abstract/Free Full Text]
  23. von Kries R, Toschke AM, Koletzko B, Slikker W Jr. Maternal smoking during pregnancy and childhood obesity. Am J Epidemiol 2002;156:954–61.[Abstract/Free Full Text]
  24. Wideroe M, Vik T, Jacobsen G, Bakketeig LS. Does maternal smoking during pregnancy cause childhood overweight? Paediatr Perinat Epidemiol 2003;17:171–9.[Medline]
  25. Whitaker RC. Predicting preschooler obesity at birth: the role of maternal obesity in early pregnancy. Pediatrics 2004;114:e29–e36.[Abstract/Free Full Text]
  26. Kanellopoulos TA, Varvarigou AA, Karatza AA, Beratis NG. Course of growth during the first 6 years in children exposed in utero to tobacco smoke. Eur J Pediatr 2007;166(7):685–92.[Medline]
  27. Fried PA, Watkinson B, Gray R. Growth from birth to early adolescence in offspring prenatally exposed to cigarettes and marijuana. Neurotoxicol Teratol. 1999;21:513–25.[Medline]
  28. Lieberman E, Gremy I, Lang JM, Cohen AP. Low birthweight at term and the timing of fetal exposure to maternal smoking. Am J Public Health 1994;84:1127–31.[Abstract/Free Full Text]
  29. Torrent M, Sunyer J, Cullinan P, et al. Smoking cessation and associated factors during pregnancy. Gac Sanit 2004;18:184–9.[Medline]
  30. Lu Y, Tong S, Oldenburg B. Determinants of smoking and cessation during and after pregnancy. Health Promot Int 2001;16:355–65.[Abstract/Free Full Text]
  31. Sunyer J, Anto JM, Harris J, et al. Maternal atopy and parity. Clin Exp Allergy 2001;31:1352–5.[Medline]
  32. Sauer PJ. Can extrauterine growth approximate intrauterine growth? Should it? Am J Clin Nutr 2007;85(suppl):608S–13S.[Abstract/Free Full Text]
  33. Sunyer J, Torrent M, Munoz-Ortiz L, et al. Prenatal dichlorodiphenyldichloroethylene (DDE) and asthma in children. Environ Health Perspect 2005;113:1787–90.[Medline]
  34. Chatzi L, Torrent M, Romieu I, et al. Mediterranean diet in pregnancy protective for wheeze and atopy in childhood. Thorax [Epub ahead of print 15 January 2008].
  35. Vioque J. Validez de la evaluación de la ingesta dietética. In: Serra ML, Aranceta J, eds. Nutrición y Salud Pública. Barcelona, Spain: Elsevier-Masson, 2006 (in Spanish).
  36. Centers for Disease Control and Prevention (CDC) Growth Charts, United States. National Center for Health Statistics. Internet: http://www.cdc.gov/growthcharts/ (accessed February 2007).
  37. Bogen DL, Hanusa BH, Whitaker RC. The effect of breast-feeding with and without formula use on the risk of obesity at 4 years of age. Obes Res 2004;12:1527–35.[Medline]
  38. Cripps RL, Martin-Gronert MS, Ozanne SE. Fetal and perinatal programming of appetite. Clin Sci (Lond) 2005;109:1–11.[Medline]
  39. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 2000;320:1240–3.[Abstract/Free Full Text]
  40. Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ 2000;320:967–71.[Abstract/Free Full Text]
  41. McDonald SD, Walker M, Perkins SL, et al. The effect of tobacco exposure on the fetal hypothalamic-pituitary-adrenal axis. BJOG 2006;113:1289–95.[Medline]
  42. Gao YJ, Holloway AC, Zeng ZH, et al. Prenatal exposure to nicotine causes postnatal obesity and altered perivascular adipose tissue function. Obes Res 2005;13:687–92.[Medline]
  43. Holloway AC, Lim GE, Petrik JJ, Foster WG, Morrison KM, Gerstein HC. Fetal and neonatal exposure to nicotine in Wistar rats results in increased beta cell apoptosis at birth and postnatal endocrine and metabolic changes associated with type 2 diabetes. Diabetologia 2005;48:2661–6.[Medline]
  44. Chen H, Hansen MJ, Jones JE, et al. Regulation of hypothalamic NPY by diet and smoking. Peptides 2007;28:384–9.[Medline]
  45. Chen H, Hansen MJ, Jones JE, et al. Cigarette smoke exposure reprograms the hypothalamic neuropeptide Y axis to promote weight loss. Am J Respir Crit Care Med 2006;173:1248–54.[Abstract/Free Full Text]
  46. Russell T, Crawford M, Woodby L. Measurements for active cigarette smoke exposure in prevalence and cessation studies: why simply asking pregnant women isn't enough. Nicotine Tob Res 2004;6(suppl)2:S141–S51.[Abstract]
  47. Montgomery SM, Ekbom A. Smoking during pregnancy and diabetes mellitus in a British longitudinal birth cohort. BMJ 2002;324:26–7.[Free Full Text]
Received for publication November 16, 2007. Accepted for publication March 10, 2008.




This article has been cited by other articles:


Home page
 Am J EpidemiolHome page
M. Guxens, M. A. Mendez, J. Julvez, E. Plana, J. Forns, X. Basagana, M. Torrent, and J. Sunyer
Cognitive Function and Overweight in Preschool Children
Am. J. Epidemiol., August 15, 2009; 170(4): 438 - 446.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Mendez, M. A
Right arrow Articles by Sunyer, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Mendez, M. A
Right arrow Articles by Sunyer, J.
Agricola
Right arrow Articles by Mendez, M. A
Right arrow Articles by Sunyer, J.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS