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Does fetal smoke exposure affect childhood bone mass? The Generation R Study

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Abstract

Summary

We assessed the intrauterine influence of maternal smoking on childhood bone mass by comparing parental prenatal and postnatal smoking habits. We observed higher bone mass in children exposed to maternal smoking, explained by higher body weight. Maternal smoking or related lifestyle factors may affect childhood weight gain rather than skeletal growth.

Introduction

Maternal smoking during pregnancy may adversely affect bone health in later life. By comparing the associations of maternal and paternal smoking and of prenatal and postnatal exposure with childhood bone measures, we aimed to explore whether the suggested association could be explained by fetal programming or reflects confounding by familial factors.

Methods

In 5565 mothers, fathers and children participating in a population-based prospective cohort study, parental smoking habits during pregnancy and current household smoking habits were assessed by postal questionnaires. Total body bone mineral content (BMC), bone area (BA) and bone mineral density (BMD) were measured by dual-energy X-ray absorptiometry (DXA) at the median age of 6.0 years (IQR 0.37).

Results

In confounder-adjusted models, maternal smoking during pregnancy was associated with a higher BMC of 11.6 g (95 % confidence interval (CI) 5.6, 17.5), a larger BA of 9.7 cm2 (95 % CI 3.0, 16.4), a higher BMD of 6.7 g/cm2 (95 % CI 2.4, 11.0) and a higher BMC of 5.4 g (95 % CI 1.3, 9.6) adjusted for BA of the child. Current weight turned out to mediate these associations. Among mothers who did not smoke, paternal smoking did not show evident associations with childhood bone measures. Also, household smoking practices during childhood were not associated with childhood bone measures.

Conclusions

Our results do not support the hypothesis of fetal smoke exposure affecting childhood bone mass via intrauterine mechanisms. Maternal smoking or related lifestyle factors may affect childhood weight gain rather than skeletal growth.

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References

  1. Cooper C, Westlake S, Harvey N, Javaid K, Dennison E, Hanson M (2006) Review: developmental origins of osteoporotic fracture. Osteoporos Int 17:337–347

    Article  PubMed  Google Scholar 

  2. Salihu HM, Wilson RE (2007) Epidemiology of prenatal smoking and perinatal outcomes. Early Hum Dev 83:713–720

    Article  CAS  PubMed  Google Scholar 

  3. Godfrey K, Walker-Bone K, Robinson S, Taylor P, Shore S, Wheeler T, Cooper C (2001) Neonatal bone mass: influence of parental birthweight, maternal smoking, body composition, and activity during pregnancy. J Bone Miner Res 16:1694–1703

    Article  CAS  PubMed  Google Scholar 

  4. Harvey N, Javaid MK, Arden NK, Poole JR, Crozier SR, Robinson SM, Inskip HM, Godfrey KM, Dennison EM, Cooper C (2010) Maternal predictors of neonatal bone size and geometry: the Southampton Women’s Survey. J Dev Orig Health Dis 1:35–41

    Article  PubMed Central  PubMed  Google Scholar 

  5. Jaddoe VW, Verburg BO, de Ridder MA, Hofman A, Mackenbach JP, Moll HA, Steegers EA, Witteman JC (2007) Maternal smoking and fetal growth characteristics in different periods of pregnancy: the Generation R Study. Am J Epidemiol 165:1207–1215

    Article  PubMed  Google Scholar 

  6. Baird J, Kurshid MA, Kim M, Harvey N, Dennison E, Cooper C (2011) Does birthweight predict bone mass in adulthood? A systematic review and meta-analysis. Osteoporos Int 22:1323–1334

    Article  CAS  PubMed  Google Scholar 

  7. Martinez-Mesa J, Restrepo-Mendez MC, Gonzalez DA, Wehrmeister FC, Horta BL, Domingues MR, Menezes AM (2013) Life-course evidence of birth weight effects on bone mass: systematic review and meta-analysis. Osteoporos Int 24:7–18

    Article  CAS  PubMed  Google Scholar 

  8. Wong PK, Christie JJ, Wark JD (2007) The effects of smoking on bone health. Clin Sci 113:233–241

    Article  CAS  PubMed  Google Scholar 

  9. Jauniaux E, Burton GJ (2007) Morphological and biological effects of maternal exposure to tobacco smoke on the feto-placental unit. Early Hum Dev 83:699–706

    Article  CAS  PubMed  Google Scholar 

  10. Yan C, Avadhani NG, Iqbal J (2011) The effects of smoke carcinogens on bone. Curr Osteoporos Rep 9:202–209

    Article  PubMed  Google Scholar 

  11. Jones G, Riley M, Dwyer T (1999) Maternal smoking during pregnancy, growth, and bone mass in prepubertal children. J Bone Miner Res 14:146–151

    Article  CAS  PubMed  Google Scholar 

  12. Jones G, Hynes KL, Dwyer T (2012) The association between breastfeeding, maternal smoking in utero, and birth weight with bone mass and fractures in adolescents: a 16-year longitudinal study. Osteoporos Int 24:1605–1611

    Article  PubMed  Google Scholar 

  13. Macdonald-Wallis C, Tobias JH, Davey Smith G, Lawlor DA (2011) Parental smoking during pregnancy and offspring bone mass at age 10 years: findings from a prospective birth cohort. Osteoporos Int 22:1809–1819

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Smith GD (2008) Assessing intrauterine influences on offspring health outcomes: can epidemiological studies yield robust findings? Basic Clin Pharmacol Toxicol 102:245–256

    Article  CAS  PubMed  Google Scholar 

  15. Noakes PS, Thomas R, Lane C, Mori TA, Barden AE, Devadason SG, Prescott SL (2007) Association of maternal smoking with increased infant oxidative stress at 3 months of age. Thorax 62:714–717

    Article  PubMed Central  PubMed  Google Scholar 

  16. Blum M, Harris SS, Must A, Phillips SM, Rand WM, Dawson-Hughes B (2002) Household tobacco smoke exposure is negatively associated with premenopausal bone mass. Osteoporos Int 13:663–668

    Article  CAS  PubMed  Google Scholar 

  17. Jaddoe VW, van Duijn CM, Franco OH et al (2012) The Generation R Study: design and cohort update 2012. Eur J Epidemiol 27:739–756

    Article  PubMed  Google Scholar 

  18. Heppe DH, Medina-Gomez C, Hofman A, Franco OH, Rivadeneira F, Jaddoe VW (2013) Maternal first-trimester diet and childhood bone mass: the Generation R Study. Am J Clin Nutr 98:224–232

    Article  CAS  PubMed  Google Scholar 

  19. Lewiecki EM, Gordon CM, Baim S et al (2008) Special report on the 2007 adult and pediatric Position Development Conferences of the International Society for Clinical Densitometry. Osteoporos Int 19:1369–1378

    Article  CAS  PubMed  Google Scholar 

  20. Heaney RP (2003) Bone mineral content, not bone mineral density, is the correct bone measure for growth studies. Am J Clin Nutr 78:350–351, author reply 351-352

    CAS  PubMed  Google Scholar 

  21. Prentice A, Parsons TJ, Cole TJ (1994) Uncritical use of bone mineral density in absorptiometry may lead to size-related artifacts in the identification of bone mineral determinants. Am J Clin Nutr 60:837–842

    CAS  PubMed  Google Scholar 

  22. Warner JT, Cowan FJ, Dunstan FD, Evans WD, Webb DK, Gregory JW (1998) Measured and predicted bone mineral content in healthy boys and girls aged 6-18 years: adjustment for body size and puberty. Acta Paediatr 87:244–249

    Article  CAS  PubMed  Google Scholar 

  23. Netherlands S (2004) [Allochtonen in Nederland]. Voorburg/Heerlen

  24. (2005) http://www.cos.rotterdam.nl. Centre for Research and Statistics, Rotterdam

  25. Durmus B, van Rossem L, Duijts L, Arends LR, Raat H, Moll HA, Hofman A, Steegers EA, Jaddoe VW (2011) Breast-feeding and growth in children until the age of 3 years: the Generation R Study. Br J Nutr 105:1704–1711

    Article  CAS  PubMed  Google Scholar 

  26. Durmus B, Kruithof CJ, Gillman MH, Willemsen SP, Hofman A, Raat H, Eilers PH, Steegers EA, Jaddoe VW (2011) Parental smoking during pregnancy, early growth, and risk of obesity in preschool children: the Generation R Study. Am J Clin Nutr 94:164–171

    Article  CAS  PubMed  Google Scholar 

  27. Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, Wood AM, Carpenter JR (2009) Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ 338:b2393

    Article  PubMed Central  PubMed  Google Scholar 

  28. Nohr EA, Frydenberg M, Henriksen TB, Olsen J (2006) Does low participation in cohort studies induce bias? Epidemiology 17:413–418

    Article  PubMed  Google Scholar 

  29. Lanting CI, Segaar D, Crone MR, van Wouwe JP (2007) Slight decrease in the prevalence of smoking around pregnancy. Ned Tijdschr Geneeskd 151:2566–2569

    CAS  PubMed  Google Scholar 

  30. Klebanoff MA, Levine RJ, Morris CD, Hauth JC, Sibai BM, Ben Curet L, Catalano P, Wilkins DG (2001) Accuracy of self-reported cigarette smoking among pregnant women in the 1990s. Paediatr Perinat Epidemiol 15:140–143

    Article  CAS  PubMed  Google Scholar 

  31. George L, Granath F, Johansson AL, Cnattingius S (2006) Self-reported nicotine exposure and plasma levels of cotinine in early and late pregnancy. Acta Obstet Gynecol Scand 85:1331–1337

    Article  CAS  PubMed  Google Scholar 

  32. Durmus B, Heppe DH, Taal HR, Manniesing R, Raat H, Hofman A, Steegers EA, Gaillard R, Jaddoe VW (2014) Parental smoking during pregnancy and total and abdominal fat distribution in school-age children: the Generation R Study. Int J Obes (Lond)

  33. Rocher E, Chappard C, Jaffre C, Benhamou CL, Courteix D (2008) Bone mineral density in prepubertal obese and control children: relation to body weight, lean mass, and fat mass. J Bone Miner Metab 26:73–78

    Article  PubMed  Google Scholar 

  34. Timpson NJ, Sayers A, Davey-Smith G, Tobias JH (2009) How does body fat influence bone mass in childhood? A Mendelian randomization approach. J Bone Miner Res 24:522–533

    Article  PubMed Central  PubMed  Google Scholar 

  35. Clark EM, Ness AR, Tobias JH (2006) Adipose tissue stimulates bone growth in prepubertal children. J Clin Endocrinol Metab 91:2534–2541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Blackburn CM, Bonas S, Spencer NJ, Coe CJ, Dolan A, Moy R (2005) Parental smoking and passive smoking in infants: fathers matter too. Health Educ Res 20:185–194

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The Generation R Study is conducted by the Erasmus Medical Center in close collaboration with the School of Law and the Faculty of Social Sciences at the Erasmus University, Rotterdam; the Municipal Health Service, Rotterdam area; and the Stichting Trombosedienst and Artsenlaboratorium Rijnmond (Star-MDC), Rotterdam. We gratefully acknowledge the contribution of general practitioners, hospitals, midwives and pharmacies in Rotterdam.

Funding

The general design of the Generation R Study was made possible by financial support from the Erasmus Medical Center, Rotterdam; the Erasmus University Rotterdam; the Dutch Ministry of Health, Welfare and Sport; and the Netherlands Organization for Health Research and Development (ZonMw). Vincent Jaddoe and Fernando Rivadeneira received an additional grant from the Netherlands Organization for Scientific Research (VIDI 016.136.361 and VIDI 016.136.367). The funding agencies had no role in the design, implementation, analysis or interpretation of the data. All authors read and approved the final manuscript.

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Correspondence to V. W. V. Jaddoe.

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Heppe, D.H.M., Medina-Gomez, C., Hofman, A. et al. Does fetal smoke exposure affect childhood bone mass? The Generation R Study. Osteoporos Int 26, 1319–1329 (2015). https://doi.org/10.1007/s00198-014-3011-z

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  • DOI: https://doi.org/10.1007/s00198-014-3011-z

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