Вы находитесь на странице: 1из 7

Published by Oxford University Press on behalf of the International Epidemiological Association The Author 2007; all rights reserved.

. Advance Access publication 3 December 2007

International Journal of Epidemiology 2008;37:210216 doi:10.1093/ije/dym239

Parental smoking and childhood obesityis maternal smoking in pregnancy the critical exposure?
Michael Toschke1,3, for the GME Ru diger von Kries,1* Gabriele Bolte,2 Ladan Baghi,1 Andre a Study Group

Accepted

24 October 2007

Background The concept of priming of childhood obesity by prenatal exposure to maternal smoking is based on a number of consistent studies. A recent paper found similar associations between paternal smoking and childhood obesity, questioning the presumed causal effect attributed to the prenatal exposure. Is the relation to paternal smoking consistent? Does it explain the effect of maternal smoking before or in pregnancy? Methods Data from a cross sectional study on 5899 children in the setting of the 2005 school entrance health examinations in Bavaria were analysed. Associations between paternal smoking or maternal smoking before or in pregnancy and childhood obesity were assessed with adjustment for potential confounders.

Downloaded from http://ije.oxfordjournals.org/ by guest on October 4, 2012

Institute of Social Pediatrics and Adolescent Medicine, Ludwig-Maximilian-University, Heiglhofstr. 63, 81337 Munich, Germany. Department of Environmental Health, Bavarian Health and rstrae Food Safety Authority, Veterina 2, 85764 Oberschleiheim, Germany. Division of Health and Social Care Research, Department of Public Health Sciences, Kings College London, UK.

* Corresponding author. Institute of Social Pediatrics and Adolescent Medicine, Ludwig-Maximilian-University, Heiglhofstr. 63, 81377 Mu nchen, Germany. E-mail: r.kriesvon@kinderzentrum-muenchen.de a GME Study Group: Bavarian Health and Food Safety Authority, Oberschleissheim (Gabriele Bolte, Hermann Fromme, Annette Heissenhuber, Michael Mosetter, Gabriele Morlock, Christine Mitschek, Manfred Wildner); Health Authority of the District Office of Bamberg (Winfried Strauch, Wiltrud Doerk, Rosemarie Sittig, Heidi Thamm); Health Authority of the District Office of Guenzburg (Roland Schmid, Tatjana Friess-Hesse, Gudrun Winter); Health Authority of the City Ingolstadt (Elisabeth Schneider, Traudl Tontsch, Christine Gampenrieder, Margot Motzet, Gerlinde Woelk); Department of Health and Environment, City of Munich (Brigitte Weise, Heidi Mayrhofer, Sylvia Kranebitter, Gertraud Rohrhirsch); Health Authority of the District Office of Schwandorf (Maximilian Kuehnel, Kornelia Baranek, Gitte Koch-Singer); Institute of Social Pediatrics and Adolescent Medicine, Ludwig-Maximilian-University Munich (Ruediger von Kries, Ladan Baghi); Bavarian State Ministry of the Environment, Public Health and Consumer Protection (Bernhard Liebl).

210

PARENTAL SMOKING AND CHILDHOOD OBESITY

211

Results

The childrens mean age was 5.8 years. The unadjusted odds ratio for obesity and paternal smoking was 2.0 (95% CI: 1.5, 2.6) and similar to that for maternal smoking before or in pregnancy with 2.3 (95% CI: 1.8, 3.1). After adjustment for a number of potential confounders and paternal smoking at interview the odds ratio for maternal smoking before or in pregnancy and childhood obesity was 1.9 (95% CI: 1.3, 2.7). There was no evidence for interaction between paternal smoking and maternal smoking before or in pregnancy (P 0.38).

Conclusions Although of similar magnitude, the association of paternal smoking could only partially explain the effect of maternal smoking before or in pregnancy on childhood obesity. Whether this persistent association reflects residual confounding or causality is unclear. Keywords Growth and development, pre-natal programming, nutritional and metabolic diseases, pre-natal nutritional physiology
Downloaded from http://ije.oxfordjournals.org/ by guest on October 4, 2012

Introduction
A growing body of epidemiological and experimental evidence indicates that the pre-natal period is a sensitive period for later health outcomes and prenatal priming is a term increasingly used to describe the long-term effects on health outcomes programmed by pre-natal and early post-natal factors.1 The effect of pre-natal exposure to maternal smoking on low birth weight has been established for more than three decades now.2 Paradoxically, a number of recent cross sectional and cohort studies using body mass index (BMI) based cut-off values or skin fold thickness to define overweight or obesity,315 or dual energy x-ray absoptiometry (DXA) measurement to assess fat mass16 reported an association between maternal smoking in pregnancy and obesity later in childhood. These observations suggest in utero priming of the obesity risk by maternal smoking. A recent study, however, reported similar associations between paternal smoking and childhood obesity as well.16 To our knowledge there is no empirical or biological evidence for a causal association between environmental tobacco smoke (ETS) exposure during early childhood and childhood obesity. Smoking by the father therefore might rather be a surrogate for other risk factors associated to childhood obesity. By using a data set of considerable size we attempted to disentangle potential effects of smoking by fathers at interview and maternal smoking before or in pregnancy.

Methods
Study population and data sources In the framework of the health monitoring units in Bavaria, Germany, a cross-sectional survey of

childrens environmental health was performed during the 2005 school entrance health examinations by public health offices of three rural and three urban regions. Details of the study are given elsewhere.17 Together with the invitation for the school entrance health examination parents of the children were given a self-administered questionnaire. Briefly, parents of 6349 out of 8127 children attending the examination completed the questionnaire (return rate 78%). In 5899 questionnaires (73%) data on paternal and maternal smoking at interview, before or in pregnancy and on the childs weight and height were given. These questionnairesproviding information on the main exposures and a number of potential confounderswere considered in the further analyses. Smoking in temporal relation to pregnancy was asked in mothers only: Did the mother smoke during pregnancy?, Did the mother smoke in the last three months before pregnancy? Smoking before or in pregnancy was combined to one category. Parental smoking at the time of interview was ascertained by the questions: Does the father or mother smoke in the house/apartment or on the balcony/terrace and how much on average? Any smoking by father or mother was categorized as a dichotomous variable maternal smoking at interview or paternal smoking at interview. Established risk factors for obesity in children were considered as potential confounders of the association between smoking and childhood obesity: highest paternal or maternal educational degree in an ordered categorical scale from one (no degree) to basic school degree (two), intermediate school degree (three), qualified for university studies (four) and to five (university diploma),14 paternal and maternal BMI (continuous),14 birth weight in grams (continuous),18 breastfeeding in an ordered categorical scale from zero

212

INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

(no breastfeeding or breastfeeding for less than 1 month) to one (breastfeeding for more than 1 month but less than 4 months), two (breastfeeding for more than 3 months but less than 6 months), three (any breastfeeding for more than 6 months),19 high TV consumption (binary; defined by TV in the childs bedroom or watching for more than 1 h per day on week days or for more than 3 h per day on weekends).20 Physical activity21 was assessed as a binary variable, much physical activity defined by at least three of the following activities at least once a week: playing with a ball, climbing on trees or alike, playing catching, riding a bike or scooter or roller skating. The outcome parameters were based on BMI derived from measurements of height and weight carried out by the public health nurses during the school entry health examinations. Although the measurement procedures and equipment within each public health office were uniform there was no standardization between public health offices. Overweight and obesity were defined by the age and gender specific cut-off values as suggested by Cole et al.22 These international percentiles use an extrapolation of an adult BMI value of 25 into children as a cut-off to define overweight and an extrapolation of adult BMI values of 30 as a cut-off to define obesity.

software package SAS version 9.1 (SAS Institute Inc., Cary, NC, USA).

Ethics and data protection Ethical approval was obtained from the local ethics committee. This study was carried out in accordance with the German data protection laws. Informed consent was obtained from the parents answering the questionnaire.

Results
The final data included 5899 children with a mean age of 5.8 years (0.43 SD) with 3067 boys and 2832 girls. There were 3792 (64%) children for whom no exposure to smoking by any family member was reported. The proportion of maternal smoking in or during pregnancy or at interview or paternal smoking at interview is shown in Table 1. The overall prevalence of overweight and obesity in children exposed to any smoking parent was 18.6% (95% CI: 16.9, 20.3) and 6.3%, (95% CI: 5.3, 7.4) respectively. Children born and living in families with no smoking parent were less likely to be overweight or obese, whereas children in families with smoking parents were more likely to be overweight or obese. The respective 95% confidence intervals for overweight and obesity by paternal or maternal smoking at interview and maternal smoking before or in pregnancy overlapped. The CochraneArmitage trend by number of smoking parents and maternal smoking before or during pregnancy indicated a positive association to overweight/obesity (P < 0.001; data not shown). Children born and living in families with no smoking parent were more likely to have less heavy parents, a higher birth weight, to be breastfed, to have mothers with a higher school education score and to be more physically active. These children were

Downloaded from http://ije.oxfordjournals.org/ by guest on October 4, 2012

Statistical analyses The prevalence estimates for overweight and obesity with exact confidence limits were calculated. Additionally we assessed a possible dose-response effect for a categorical smoking variable defined by zero: no smoking parent; one: sum of smoking mothers either before or in pregnancy smoking mother at interview smoking father at interview 1; two sum 2; three sum 3) with the Cochrane Armitage trend test. Crude and adjusted odds ratios for paternal and maternal smoking at interview and maternal smoking before or in pregnancy were calculated using logistic regression. Pre-defined potential confounders were entered block wise starting with (i) paternal/maternal BMI and education, childs birth weight, pre-mature birth and breastfeeding (ii) childs physical activity and TV watching (iii) paternal (maternal) smoking as applicable. Multicollinearity was assessed by the variance inflation factor (with values above 2.5 considered indicative). Interaction terms for paternal and maternal smoking were introduced in multivariable models assessed. Additionally, we calculated a logistic model for obesity including maternal smoking in or before pregnancy and paternal smoking as only exposures. We compared the sum of the two corresponding adjusted point estimates with the sum of their unadjusted point estimates. With this, we assessed the proportion of confounding due to factors associated with both exposure variables, maternal smoking in or before pregnancy and paternal smoking. All calculations were carried out with the

Table 1 Smoking parents and childhood overweight and obesity (smoking categories not exclusive) Overweight Smoking parent Overall No smoking parent Obesity 95% CI 3.4, 4.4 2.1, 3.2 4.9, 7.8

n percent 95% CI percent 5899 13.7 12.8, 14.6 3.9 3792 10.9 10.0, 12.4 18.3 16.2, 20.6 2.6 6.3

Father 1211 (at interview) Mother - At interview 1056 - Before or in 1230 pregnancy

20.4 17.9, 22.9 19.0 16.9, 21.3

8.3 6.7, 10.0 6.9 5.6, 8.6

PARENTAL SMOKING AND CHILDHOOD OBESITY Table 2 Distribution of potential confounders by parental smoking (categories not mutually exclusive) Parental smoking Potential confounders BMI mother (kg/m2) BMI father (kg/m2) Birth weight (g) Parental school education score (points on a 15 scale) Breastfed (%) Premature births (%) High TV consumption (%) High physical activity (%) No smoking parent Mean SE 23.50 0.07 25.87 0.06 3353.51 9.76 3.13 0.02 80.21 0.65 7.06 0.42 38.4 0.79 36.39 0.78 Paternal smoking at Maternal smoking at interview Mean SE interview Mean SE 24.21 0.14 23.79 0.14 26.04 0.11 3292.6 17.54 2.68 0.03 70.78 1.32 8.22 0.8 60.02 1.41 33.06 1.35 26.14 0.13 3264.44 18.65 2.61 0.03 64.26 1.5 9.00 0.89 59.98 1.51 34.47 1.46

213

Maternal smoking before or in pregnancy Mean SE 23.78 0.13 26.07 0.11 3266.08 17.60 2.72 0.03 64.59 1.38 8.22 0.79 55.55 1.42 34.89 1.36

Downloaded from http://ije.oxfordjournals.org/ by guest on October 4, 2012

Table 3 Odds ratios for parental smoking categories on childhood overweight and obesity with adjustment for pre/perinatal and post-natal risk factors, parental education and BMI and for maternal or paternal smoking, respectively Odds ratio for overweight 95% CI Maternal smoking at interview No Unadjusted Adjusted for maternal/paternal BMI and education, childs birth weight, premature birth and breastfeeding Additionally adjusted for childs physical activity and TV watching Additionally adjusted for paternal smoking at interview Paternal smoking at interview No Unadjusted Adjusted for maternal/paternal BMI and education, childs birth weight, premature birth and breastfeeding Additionally adjusted for childs physical activity and TV watching Additionally adjusted for maternal smoking at interview Maternal smoking before or in pregnancy No Unadjusted Adjusted for maternal/paternal BMI and education, childs birth weight, premature birth and breastfeeding Additionally adjusted for childs physical activity and TV watching Additionally adjusted for paternal smoking at interview 1 1.7 1.5 1.5 1.3 1.4, 1.9 1.2, 1.9 1.2, 1.8 1.1, 1.7 1 2.3 2.2 2.2 1.9 1.8, 3.1 1.5, 3.1 1.5, 3.1 1.3, 2.7 1 1.6 1.6 1.5 1.4 1.3, 1.9 1.3, 1.9 1.3, 1.9 1.1, 1.7 1 2.0 2.0 1.9 1.3 1.5, 2.6 1.4, 2.9 1.3, 2.7 0.9, 1.9 1 1.6 1.6 1.6 1.3 1.5, 2.2 1.3, 2.0 1.2, 1.9 1.0, 1.7 1 2.9 2.9 2.8 2.5 2.2, 3.9 2.1, 4.2 1.9, 4.0 1.7, 3.7 Odds ratio for obesity 95% CI

less likely to be born pre-maturely or to watch TV extensively (Table 2). Odds ratios for paternal and maternal smoking at interview and for smoking before or in pregnancy and

overweight/obesity are shown in Table 3. The crude odds ratios for maternal and paternal smoking at interview and smoking before or in pregnancy were similar with widely overlapping 95% confidence

214

INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

intervals. Adjustment for pre- and perinatal factors, parental BMI and education accounted for only marginal changes of the maternal before or in pregnancy-smoking effect. Addition of TV viewing and a score for childs physical activity did not change the odds ratios either. Maternal smoking at interview and paternal smoking, and smoking before or in pregnancy and paternal smoking were highly correlated (chi square 1006.0; P < 0.0001 and chi square 317.3; P < 0.0001, respectively). When paternal smoking at interview was added to the model for smoking before or in pregnancy or for maternal smoking at interview the odds ratios decreased slightly. A model considering maternal smoking in or before pregnancy and paternal smoking for obesity yielded point estimates of mat 0.73 and pat 0.48 corresponding to odds ratios of 2.08 and 1.62. The sum of these effects was with 0.73 0.48 1.21 lower compared with the sum of the unadjusted effects with log(2.3) 0.83 for maternal smoking in or before pregnancy, log(2.0) 0.69 for paternal smoking and 0.69 0.83 1.52. The sum of the adjusted estimates is with 11.21/1.52 20% reduced compared with the sum of the unadjusted estimates. Interaction terms in multivariate models for paternal smoking and maternal smoking at interview yielded P-values of 0.14 and for paternal smoking and maternal smoking before or in pregnancy P-values of 0.38, respectively. Additionally, the variance inflation factors for neither of these single exposures exceeded 1.3. The analyses presented in Table 3 were also carried out for maternal smoking in pregnancy only instead of maternal smoking before or in pregnancy. For the outcome obesity e.g. the odds ratios were 2.9 (95% CI: 2.1, 3.9) for the unadjusted model and 2.8 (95% CI: 1.8, 4.3) with adjustment for maternal/paternal BMI and education, childs birth weight, pre-mature birth and breastfeeding. Further adjustment for childs physical activity and TV watching reduced the odds ratio to 2.6 (95% CI: 1.7. 4.0). With additional adjustment for paternal smoking at interview the odds ratio was 2.3 (95% CI: 1.5, 3.6). Similar results were observed with overweight as outcome (data not shown).

Discussion
The main finding of this study is that associations between parental smoking and childhood obesity are not confined to maternal smoking in pregnancy: a similar association was found for paternal smoking at childs age 6 years. Paternal smoking was a confounder, but did only partially explain the effect of maternal smoking on childhood obesity. A meaningful risk of maternal smoking before or in pregnancy on childhood obesity persisted after adjustment for paternal smoking and there was no evidence for interaction between maternal and paternal smoking. The association between paternal smoking and

childhood obesity was also found in an older data set based on data collected during the 1997 school entry health examination. When paternal smoking was added to the logistic regression model for maternal smoking in pregnancy and childhood overweight/obesity the odds was similarly reduced but only partially explained the effect of maternal smoking in pregnancy (data not shown). Previous research on the interdependencies of parental smoking has focussed on maternal smoking in pregnancy. Maternal smoking in pregnancy is associated with a considerable reduction in birth weight of the offspring.2 Cotinine levels in smoking pregnant women were about 10 times higher than in mothers exposed to ETS.23 While in this study the reduction in birth weight in children of mothers exposed to ETS was only marginal. There was a mean reduction in birth weight in the range of 77.7232.7 g depending on the tertile of the serum cotinine levels determined in smoking women in the 27th and 28th week since the last menstrual period.23 Assuming that all fathers who smoked at interview were indeed the biological fathers and partners during pregnancy as well and had smoked during the index pregnancyunfortunately we have no data on paternal smoking during pregnancyand that the effect of paternal smoking were caused by ETS inhaled by the mother during pregnancy, the effect of paternal smoking should be much lower than for maternal smoking before or in pregnancy. However, the effects of maternal smoking before or in pregnancy and the effect of paternal smoking were similar. Therefore the effect of paternal smoking at interview might either be explained by a causal association between concomitant ETS and childhood obesity, or by paternal smoking at interview acting as a surrogate marker for obesogenic lifestyle factors. Since, to our knowledge, there is no published biological or empirical evidence for a causal association between post-natal ETS and childhood obesity the observed associations between maternal and paternal smoking at interview and childhood obesity are more likely to be a surrogate for risk factors associated with childhood obesity. Some possible sources of bias have to be considered: underestimation of the true effect of smoking during pregnancy because of combining maternal smoking before and smoking during pregnancy into one exposure category: in a number of data sets13,24 and this one (data not shown) smoking before or during pregnancy yielded similar associations to childhood obesity. This seemingly implausible finding was specifically addressed in one study:24 Most mothers who smoke before pregnancy do so at least during the first weeks of pregnancy and higher odds ratios related to smoking throughout pregnancy in bivariate analyses could be explained by confounding. Since the critical period for smoking in pregnancy for childhood overweight and obesity appears to be the first trimester,24 and because all mothers who smoked

Downloaded from http://ije.oxfordjournals.org/ by guest on October 4, 2012

PARENTAL SMOKING AND CHILDHOOD OBESITY

215

throughout did so in the first trimester as well whereas only 33 had started smoking during pregnancy, we combined before and in pregnancy smoking into one category: smoking before or during pregnancy. It is well possible, that other priming effects of maternal smoking in pregnancy e.g. on blood pressure25 require smoking throughout pregnancy. The measurement of height and weight was not standardized between the public health offices involved. The mean BMI, however, was similar between the public health offices (data not shown). Some random measurement error between the children assessed within the public health offices is likely. The latter, however, is unlikely to affect our effect estimates. Complete data on the exposure and of BMI was available for about three-fourth of the children. For these the proportion with a birth weight of 3000 g or above or the proportion of children with pre-mature birth was similar to the Bavarian perinatal statistics (data not shown). Assessment of the smoking exposure seems to be valid2628 and bias due to differential misclassification of the outcome defined by height and weight measurement appears to be unlikely since the public health nurses involved in the anthropometric measurements were not aware of the research hypothesis. Even if social desirability had influenced reporting of parental smoking this would unlikely be differential between parents of obese and non-obese children, because the hypothesis of a potential association between parental smoking and childhood obesity is new and unknown to the public. Paternal smoking was a confounder of the association of maternal smoking before or in pregnancy and

childhood obesity. However, the reduction of only 20% of the unadjusted maternal smoking in or before pregnancy estimate by paternal smoking implies (i) that maternal smoking in or before pregnancy and paternal smoking at interview have limited collinearity and (ii) their effect on childs obesity cannot only be due to confounding by the same factor(s). A meaningful association to maternal smoking before or in pregnancy persisted after adjustment for paternal smoking. Animal experiments suggest biological plausibility for a potential causal association between maternal smoking in pregnancy and childhood obesity: a higher average weight in rats randomly exposed to nicotine in utero was reported and several potential biological mechanisms, an altered insulin metabolism e.g. were suggested.2932 In summary, strong associations between paternal smoking and childhood obesity could be confirmed. Paternal smoking was a confounder of the association between maternal smoking before or in pregnancy but a meaningful effect on the risk for childhood obesity persisted after adjustment. Whether this association reflects residual confounding or causality is unclear.

Downloaded from http://ije.oxfordjournals.org/ by guest on October 4, 2012

Acknowledgement
This work was supported by the Bavarian State Ministry of the Environment, Public Health and Consumer Protection and by the LMU innovative research priority project MC-Health (sub-project I). Conflict of interest: None declared.

KEY MESSAGES  Maternal smoking before or in pregnancy was associated with a higher prevalence of overweight and obesity in 5- or 6-year old children.  Paternal smoking at interview was associated with a similarly increased prevalence of overweight and obesity.  Paternal smoking at interview, however, only partially explained the effect of maternal smoking before or in pregnancy on the prevalence of overweight and obesity in children.

References
1 2

Gillman MW. Developmental origins of health and disease. N Engl J Med 2005;353:184850. Butler NR, Goldstein H, Ross EM. Cigarette smoking in pregnancy: its influence on birth weight and perinatal mortality. Br Med J 1972;1972ii:12730. 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;82:39398. Al Mamun A, Lawlor DA, Alati R, OCallaghan 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;164:31725. Bergmann KE, Bergmann RL, Von Kries R et al. Early determinants of childhood overweight and adiposity in

216

INTERNATIONAL JOURNAL OF EPIDEMIOLOGY


20

10

11

12

13

14

15

16

17

18

19

a birth cohort study: role of breast-feeding. Int J Obes Relat Metab Disord 2003;27:16272. 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;35:12130. Dubois L, Girard M. Early determinants of overweight at 4.5 years in a population-based longitudinal study. Int J Obes (Lond) 2006;30:61017. 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;13:202128. Power C, Jefferis BJ. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol 2002;31:39398. Reilly JJ, Armstrong J, Dorosty AR et al. Early life risk factors for obesity in childhood: cohort study. Br Med J 2005;330:1357. Salsberry PJ, Reagan PB. Dynamics of early childhood overweight. Pediatrics 2005;116:132938. Toschke AM, Ehlin AG, von-Kries R, Ekbom A, Montgomery SM. Maternal smoking during pregnancy and appetite control in offspring. J Perinat Med 2003;31:25156. Toschke AM, Koletzko B, Slikker W Jr, Hermann M, vonKries R. Childhood obesity is associated with maternal smoking in pregnancy. Eur J Pediatr 2002;161:44548. von-Kries R, Toschke AM, Koletzko B, Slikker W Jr. Maternal smoking during pregnancy and childhood obesity. Am J Epidemiol 2002;156:95461. Wideroe M, Vik T, Jacobsen G, Bakketeig LS. Does maternal smoking during pregnancy cause childhood overweight? Paediatr Perinat Epidemiol 2003;17:17179. 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;14:228493. Bolte G, Heissenhuber A, von Kries R et al. Health monitoring units in Bavaria: concept, aims and thematic focus of the first survey on childrens environment and health. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2007;50:47683. Rasmussen F, Johansson M. The relation of weight, length and ponderal index at birth to body mass index and overweight among 18-year-old males in Sweden. Eur J Epidemiol 1998;14:37380. von-Kries R, Koletzko B, Sauerwald T et al. Breast feeding and obesity: cross sectional study. Br Med J 1999;319:14750.

21

22

23

24

25

26

27

28

29

30

31

32

Dietz WH Jr., Gortmaker SL. Do we fatten our children at the television set? Obesity and television viewing in children and adolescents. Pediatrics 1985;75:80712. Moore LL, Nguyen US, Rothman KJ, Cupples LA, Ellison RC. Preschool physical activity level and change in body fatness in young children. The Framingham childrens study. Am J Epidemiol 1995;142:98288. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 2000;320:124043. Eskenazi B, Trupin LS. Passive and active maternal smoking during pregnancy, as measured by serum cotinine, and postnatal smoke exposure. II. Effects on neurodevelopment at age 5 years. Am J Epidemiol 1995;142(Suppl 9):S19S29. Toschke AM, Montgomery SM, Pfeiffer U, von Kries R. Early intrauterine exposure to tobacco-inhaled products and obesity. Am J Epidemiol 2003;158:106874. Lawlor DA, Najman JM, Sterne J, Williams GM, Ebrahim S, Davey Smith G. Associations of parental, birth, and early life characteristics with systolic blood pressure at 5 years of age: findings from the MaterUniversity study of pregnancy and its outcomes. Circulation 2004;110:241723. Parazzini F, Davoli E, Rabaiotti M et al. Validity of selfreported smoking habits in pregnancy: a saliva cotinine analysis. Acta Obstet Gynecol Scand 1996;75:35254. Tomeo CA, Rich-Edwards JW, Michels KB et al. Reproducibility and validity of maternal recall of pregnancy-related events. Epidemiology 1999;10:77477. Klesges RC, Debon M, Ray JW. Are self-reports of smoking rate biased? Evidence from the second national health and nutrition examination survey. J Clin Epidemiol 1995;48:122533. 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;48:266166. Chen WJ, Kelly RB. Effect of prenatal or perinatal nicotine exposure on neonatal thyroid status and offspring growth in rats. Life Sci 2005;76:124958. Gao YJ, Holloway AC, Zeng ZH et al. Prenatal exposure to nicotine causes postnatal obesity and altered perivascular adipose tissue function. Obes Res 2005;13:68792. Newman MB, Shytle RD, Sanberg PR. Locomotor behavioral effects of prenatal and postnatal nicotine exposure in rat offspring. Behav Pharmacol 1999;10:699706.

Downloaded from http://ije.oxfordjournals.org/ by guest on October 4, 2012

Вам также может понравиться