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Gender differences in the association between maternal smoking during pregnancy and childhood growth trajectories: multilevel analysis

International Journal of Obesity volume 35, pages 53–59 (2011)Cite this article

Subjects

Abstract

Objectives:

This study examines the gender differences in the association between maternal smoking during pregnancy and later growth in childhood.

Design:

Ongoing prospective cohort study, which is called ‘the Project Koshu’, initiated in the foetal stage to the age of 9–10 years.

Setting:

Koshu City which was in Japanese rural area

Participants:

The study population comprised children born between 1 April 1991 and 31 March 1999 in Koshu City, Japan, and their mothers. Maternal smoking during early pregnancy was the exposure studied.

Main outcome measures:

Childhood body mass index (BMI) and BMI z-score trajectories of the children born to the smoking and non-smoking mothers by gender. Multilevel analysis that includes both individual and age as different-level variables was used for statistical analyses.

Results:

The participating mothers delivered 1619 babies during the study period. Birth weight and anthropometric data were collected from 1603 (at birth, 99.0%), 1358 (at age 3, 83.9%), 1248 (at age 5, 77.1%), 1270 (at age 7–8, 78.4%) and 1274 (at age 9–10, 78.7%) of these children. The mean birth weight of both the male and female children whose mothers had smoked during pregnancy was significantly low compared with those born to non-smoking mothers (P<0.01). However, the childhood BMI at each subsequent checkup age significantly increased only among the male children born to the smoking mothers. Moreover, this increase was continuously observed after 3 years of age. The results of BMI z-score analysis were also similar to these of BMI analysis.

Conclusions:

Smoking by pregnant women decreases the infant birth weight irrespective of gender but increases childhood weight gain especially by male children. The results might be valuable to explore the mechanism of fetal programming.

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References

  1. Barker DJ, Osmond C . Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986; 1: 1077–1081.

    Article  CAS  PubMed  Google Scholar 

  2. Barker DJ . Obesity and early life. Obes Rev 2007; 8 (Suppl 1): 45–49.

    Article  PubMed  Google Scholar 

  3. Barker DJ . Mothers, Babies, and Disease in Later Life. BMJ Publishing: London, UK, 1994.

    Google Scholar 

  4. Barker DJ . In utero programming of chronic disease. Clin Sci (Lond) 1998; 95: 115–128.

    Article  CAS  Google Scholar 

  5. Phillips DI . Insulin resistance as a programmed response to fetal undernutrition. Diabetologia 1996; 39: 1119–1122.

    Article  CAS  PubMed  Google Scholar 

  6. Eriksson JG, Forsén T, Tuomilehto J, Osmond C, Barker DJ . Early adiposity rebound in childhood and risk of Type 2 diabetes in adult life. Diabetologia 2003; 46: 190–194.

    Article  CAS  PubMed  Google Scholar 

  7. Bhargava SK, Sachdev HS, Fall CH, Osmond C, Lakshmy R, Barker DJ et al. Relation of serial changes in childhood body-mass index to impaired glucose tolerance in young adulthood. N Engl J Med 2004; 350: 865–875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Barker DJ, Osmond C, Forsén TJ, Kajantie E, Eriksson JG . Trajectories of growth among children who have coronary events as adults. N Engl J Med 2005; 353: 1802–1809.

    Article  CAS  PubMed  Google Scholar 

  9. Kramer MS . Determinants of low birth weight: methodological assessment and meta-analysis. Bull World Health Organ 1987; 65: 663–737.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Windham GC, Hopkins B, Fenster L, Swan SH . Prenatal active or passive tobacco smoke exposure and the risk of preterm delivery or low birth weight. Epidemiology 2000; 11: 427–433.

    Article  CAS  PubMed  Google Scholar 

  11. England LJ, Kendrick JS, Wilson HG, Merritt RK, Gargiullo PM, Zahniser SC . Effects of smoking reduction during pregnancy on the birth weight of term infants. Am J Epidemiol 2001; 154: 694–701.

    Article  CAS  PubMed  Google Scholar 

  12. Suzuki K, Tanaka T, Kondo N, Minai J, Sato M, Yamagata Z . Is maternal smoking during early pregnancy a risk factor for all low birth weight infants? J Epidemiol 2008; 18: 89–96.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Montgomery SM, Ekbom A . Smoking during pregnancy and diabetes mellitus in a British longitudinal birth cohort. BMJ 2002; 324: 26–27.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Toschke AM, Montgomery SM, Pfeiffer U, von Kries R . Early intrauterine exposure to tobacco-inhaled products and obesity. Am J Epidemiol 2003; 158: 1068–1074.

    Article  CAS  PubMed  Google Scholar 

  15. Oken E, Levitan EB, Gillman MW . Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes (Lond) 2008; 32: 201–210.

    Article  CAS  Google Scholar 

  16. Mizutani T, Suzuki K, Kondo N, Yamagata Z . Association of maternal lifestyles including smoking during pregnancy with childhood obesity. Obesity (Silver Spring) 2007; 15: 3133–3139.

    Article  Google Scholar 

  17. Suzuki K, Ando D, Sato M, Tanaka T, Kondo N, Yamagata Z . The association between maternal smoking during pregnancy and childhood obesity persists to the age of 9–10 years. J Epidemiol 2009; 19: 136–142.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Abraham S, Collins G, Nordsieck M . Relationship of childhood weight status to morbidity in adults. HSMHA Health Rep 1971; 86: 273–284.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Charney E, Goodman HC, McBride M, Lyon B, Pratt R . Childhood antecedents of adults obesity. Do chubby infants become obese adults? N Engl J Med 1976; 295: 6–9.

    Article  CAS  PubMed  Google Scholar 

  20. Dietz WH . Childhood weight affects adult morbidity and mortality. J Nutr 1998; 128: 411S–414S.

    Article  CAS  PubMed  Google Scholar 

  21. de Zegher F, Devlieger H, Eeckels R . Fetal growth: boys before girls. Horm Res 1999; 51: 258–259.

    CAS  PubMed  Google Scholar 

  22. Fitzmaurice GM, Laird NM, Ware JH . Applied Longitudinal Analysis. Wiley-Interscience: New Jersey, US, 2004.

    Google Scholar 

  23. World Health Organization (WHO). Multicentre Growth Reference Study Group. WHO child growth standards: length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development. World Health Organization 2006.

  24. Lambers DS, Clark KE . The maternal and fetal physiologic effects of nicotine. Semin Perinatol 1996; 20: 115–126.

    Article  CAS  PubMed  Google Scholar 

  25. Sardinha FL, Telles MM, Albuquerque KT, Oyama LM, Guimarães PA, Santos OF et al. Gender difference in the effect of intrauterine malnutrition on the central anorexigenic action of insulin in adult rats. Nutrition 2006; 22: 1152–1161.

    Article  CAS  PubMed  Google Scholar 

  26. Lu F, Bytautiene E, Tamayo E, Gamble P, Anderson GD, Hankins GD et al. Gender-specific effect of overexpression of sFlt-1 in pregnant mice on fetal programming of blood pressure in the offspring later in life. Am J Obstet Gynecol 2007; 197: 418.e1–418.e5.

    Article  Google Scholar 

  27. Grigore D, Ojeda NB, Alexander BT . Sex differences in the fetal programming of hypertension. Gend Med 2008; 5 (Suppl A): S121–S132.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Gariepy J, Denarie N, Chironi G, Salomon J, Levenson J, Simon A . Gender difference in the influence of smoking on arterial wall thickness. Atherosclerosis 2000; 153: 139–145.

    Article  CAS  PubMed  Google Scholar 

  29. Gardiner HM . Early environmental influences on vascular development. Early Hum Dev 2007; 83: 819–823.

    Article  PubMed  Google Scholar 

  30. Smith LM, Cloak CC, Poland RE, Torday J, Ross MG . Prenatal nicotine increases testosterone levels in the fetus and female offspring. Nicotine Tob Res 2003; 5: 369–374.

    Article  CAS  PubMed  Google Scholar 

  31. Blouin K, Boivin A, Tchernof A . Androgens and body fat distribution. J Steroid Biochem Mol Biol 2008; 108: 272–280.

    Article  CAS  PubMed  Google Scholar 

  32. Klebanoff MA, Levine RJ, Morris CD, Hauth JC, Sibai BM, Ben Curet L et al. Accuracy of self-reported cigarette smoking among pregnant women in the 1990s. Paediatr Perinat Epidemiol 2001; 15: 140–143.

    Article  CAS  PubMed  Google Scholar 

  33. Lelong N, Kaminski M, Saurel-Cubizolles MJ, Bouvier-Colle MH . Postpartum return to smoking among usual smokers who quit during pregnancy. Eur J Public Health 2001; 11: 334–339.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank all the study participants for allowing the use of their personal data. We also thank the staff of the Administrative Office of Koshu City for their cooperation. This work was supported by a Grant-in-Aid for Scientific Research (KAKENHI 20590639) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.

Author contributions

K Suzuki was primarily responsible for the data collection, analysis, interpretation and preparation of this report. N Kondo participated in the analysis and interpretation of data. M Sato, T Tanaka and D Ando were involved in the data collection and interpretation of data. Z Yamagata was the lead investigator of Project Koshu, and advised on issues of study design, participated in the analysis and interpretation of data and helped in the preparation of this report.

Author information

Authors and Affiliations

  1. Department of Health Sciences, School of Medicine, University of Yamanashi, Chuo, Yamanashi, Japan

    K Suzuki, N Kondo, M Sato, T Tanaka & Z Yamagata

  2. Department of Physical Education, National Defence Academy, Yokosuka, Kanagawa, Japan

    D Ando

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  1. K Suzuki
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  2. N Kondo
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  4. T Tanaka
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  5. D Ando
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  6. Z Yamagata
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Corresponding author

Correspondence to Z Yamagata.

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The authors declare no conflict of interest.

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Suzuki, K., Kondo, N., Sato, M. et al. Gender differences in the association between maternal smoking during pregnancy and childhood growth trajectories: multilevel analysis. Int J Obes 35, 53–59 (2011). https://doi.org/10.1038/ijo.2010.198

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