Skip to main content
Top
Published in: Osteoporosis International 4/2015

01-04-2015 | Original Article

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

Authors: D. H. M. Heppe, C. Medina-Gomez, A. Hofman, F. Rivadeneira, V. W. V. Jaddoe

Published in: Osteoporosis International | Issue 4/2015

Login to get access

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.
Appendix
Available only for authorised users
Literature
1.
go back to reference Cooper C, Westlake S, Harvey N, Javaid K, Dennison E, Hanson M (2006) Review: developmental origins of osteoporotic fracture. Osteoporos Int 17:337–347CrossRefPubMed Cooper C, Westlake S, Harvey N, Javaid K, Dennison E, Hanson M (2006) Review: developmental origins of osteoporotic fracture. Osteoporos Int 17:337–347CrossRefPubMed
2.
go back to reference Salihu HM, Wilson RE (2007) Epidemiology of prenatal smoking and perinatal outcomes. Early Hum Dev 83:713–720CrossRefPubMed Salihu HM, Wilson RE (2007) Epidemiology of prenatal smoking and perinatal outcomes. Early Hum Dev 83:713–720CrossRefPubMed
3.
go back to reference 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 16:1694–1703CrossRefPubMed 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 16:1694–1703CrossRefPubMed
4.
go back to reference 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 1:35–41CrossRefPubMedCentralPubMed 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 1:35–41CrossRefPubMedCentralPubMed
5.
go back to reference 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 165:1207–1215CrossRefPubMed 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 165:1207–1215CrossRefPubMed
6.
go back to reference 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 22:1323–1334CrossRefPubMed 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 22:1323–1334CrossRefPubMed
7.
go back to reference 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 24:7–18CrossRefPubMed 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 24:7–18CrossRefPubMed
8.
9.
go back to reference Jauniaux E, Burton GJ (2007) Morphological and biological effects of maternal exposure to tobacco smoke on the feto-placental unit. Early Hum Dev 83:699–706CrossRefPubMed Jauniaux E, Burton GJ (2007) Morphological and biological effects of maternal exposure to tobacco smoke on the feto-placental unit. Early Hum Dev 83:699–706CrossRefPubMed
10.
go back to reference Yan C, Avadhani NG, Iqbal J (2011) The effects of smoke carcinogens on bone. Curr Osteoporos Rep 9:202–209CrossRefPubMed Yan C, Avadhani NG, Iqbal J (2011) The effects of smoke carcinogens on bone. Curr Osteoporos Rep 9:202–209CrossRefPubMed
11.
go back to reference Jones G, Riley M, Dwyer T (1999) Maternal smoking during pregnancy, growth, and bone mass in prepubertal children. J Bone Miner Res 14:146–151CrossRefPubMed Jones G, Riley M, Dwyer T (1999) Maternal smoking during pregnancy, growth, and bone mass in prepubertal children. J Bone Miner Res 14:146–151CrossRefPubMed
12.
go back to reference 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 24:1605–1611CrossRefPubMed 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 24:1605–1611CrossRefPubMed
13.
go back to reference 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 22:1809–1819CrossRefPubMedCentralPubMed 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 22:1809–1819CrossRefPubMedCentralPubMed
14.
go back to reference Smith GD (2008) Assessing intrauterine influences on offspring health outcomes: can epidemiological studies yield robust findings? Basic Clin Pharmacol Toxicol 102:245–256CrossRefPubMed Smith GD (2008) Assessing intrauterine influences on offspring health outcomes: can epidemiological studies yield robust findings? Basic Clin Pharmacol Toxicol 102:245–256CrossRefPubMed
15.
go back to reference 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 62:714–717CrossRefPubMedCentralPubMed 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 62:714–717CrossRefPubMedCentralPubMed
16.
go back to reference 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 13:663–668CrossRefPubMed 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 13:663–668CrossRefPubMed
17.
go back to reference Jaddoe VW, van Duijn CM, Franco OH et al (2012) The Generation R Study: design and cohort update 2012. Eur J Epidemiol 27:739–756CrossRefPubMed Jaddoe VW, van Duijn CM, Franco OH et al (2012) The Generation R Study: design and cohort update 2012. Eur J Epidemiol 27:739–756CrossRefPubMed
18.
go back to reference 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 98:224–232CrossRefPubMed 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 98:224–232CrossRefPubMed
19.
go back to reference 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 19:1369–1378CrossRefPubMed 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 19:1369–1378CrossRefPubMed
20.
go back to reference 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 351-352PubMed 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 351-352PubMed
21.
go back to reference 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 60:837–842PubMed 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 60:837–842PubMed
22.
go back to reference 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 87:244–249CrossRefPubMed 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 87:244–249CrossRefPubMed
23.
go back to reference Netherlands S (2004) [Allochtonen in Nederland]. Voorburg/Heerlen Netherlands S (2004) [Allochtonen in Nederland]. Voorburg/Heerlen
25.
go back to reference 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 105:1704–1711CrossRefPubMed 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 105:1704–1711CrossRefPubMed
26.
go back to reference 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 94:164–171CrossRefPubMed 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 94:164–171CrossRefPubMed
27.
go back to reference 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:b2393CrossRefPubMedCentralPubMed 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:b2393CrossRefPubMedCentralPubMed
28.
go back to reference Nohr EA, Frydenberg M, Henriksen TB, Olsen J (2006) Does low participation in cohort studies induce bias? Epidemiology 17:413–418CrossRefPubMed Nohr EA, Frydenberg M, Henriksen TB, Olsen J (2006) Does low participation in cohort studies induce bias? Epidemiology 17:413–418CrossRefPubMed
29.
go back to reference Lanting CI, Segaar D, Crone MR, van Wouwe JP (2007) Slight decrease in the prevalence of smoking around pregnancy. Ned Tijdschr Geneeskd 151:2566–2569PubMed Lanting CI, Segaar D, Crone MR, van Wouwe JP (2007) Slight decrease in the prevalence of smoking around pregnancy. Ned Tijdschr Geneeskd 151:2566–2569PubMed
30.
go back to reference 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 15:140–143CrossRefPubMed 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 15:140–143CrossRefPubMed
31.
go back to reference 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 85:1331–1337CrossRefPubMed 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 85:1331–1337CrossRefPubMed
32.
go back to reference 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) 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.
go back to reference 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 26:73–78CrossRefPubMed 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 26:73–78CrossRefPubMed
34.
go back to reference 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 24:522–533CrossRefPubMedCentralPubMed 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 24:522–533CrossRefPubMedCentralPubMed
36.
go back to reference 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 20:185–194CrossRefPubMed 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 20:185–194CrossRefPubMed
Metadata
Title
Does fetal smoke exposure affect childhood bone mass? The Generation R Study
Authors
D. H. M. Heppe
C. Medina-Gomez
A. Hofman
F. Rivadeneira
V. W. V. Jaddoe
Publication date
01-04-2015
Publisher
Springer London
Published in
Osteoporosis International / Issue 4/2015
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-014-3011-z

Other articles of this Issue 4/2015

Osteoporosis International 4/2015 Go to the issue