Maternal personal exposure to airborne benzene and intrauterine growth

Rémy Slama, Olivier Thiebaugeorges, Valérie Goua, Lucette Aussel, Paolo Sacco, Aline Bohet, Anne Forhan, Béatrice Ducot, Isabella Annesi-Maesano, Joachim Heinrich, Guillaume Magnin, Michel Schweitzer, Monique Kaminski, Marie-Aline Charles, EDEN Mother-Child Cohort Study Group, Rémy Slama, Olivier Thiebaugeorges, Valérie Goua, Lucette Aussel, Paolo Sacco, Aline Bohet, Anne Forhan, Béatrice Ducot, Isabella Annesi-Maesano, Joachim Heinrich, Guillaume Magnin, Michel Schweitzer, Monique Kaminski, Marie-Aline Charles, EDEN Mother-Child Cohort Study Group

Abstract

Background: Studies relying on outdoor pollutants measures have reported associations between air pollutants and birth weight.

Objective: Our aim was to assess the relation between maternal personal exposure to airborne benzene during pregnancy and fetal growth.

Methods: We recruited pregnant women in two French maternity hospitals in 2005-2006 as part of the EDEN mother-child cohort. A subsample of 271 nonsmoking women carried a diffusive air sampler for a week during the 27th gestational week, allowing assessment of benzene exposure. We estimated head circumference of the offspring by ultrasound measurements during the second and third trimesters of pregnancy and at birth.

Results: Median benzene exposure was 1.8 microg/m(3) (5th, 95th percentiles, 0.5, 7.5 microg/m(3)). Log-transformed benzene exposure was associated with a gestational age-adjusted decrease of 68 g in mean birth weight [95% confidence interval (CI), -135 to -1 g] and of 1.9 mm in mean head circumference at birth (95% CI, -3.8 to 0.0 mm). It was associated with an adjusted decrease of 1.9 mm in head circumference assessed during the third trimester (95% CI, -4.0 to 0.3 mm) and of 1.5 mm in head circumference assessed at the end of the second trimester of pregnancy (95% CI, -3.1 to 0 mm).

Conclusions: Our prospective study among pregnant women is one of the first to rely on personal monitoring of exposure; a limitation is that exposure was assessed during 1 week only. Maternal benzene exposure was associated with decreases in birth weight and head circumference during pregnancy and at birth. This association could be attributable to benzene and a mixture of associated traffic-related air pollutants.

Keywords: atmospheric pollution; benzene; birth weight; cohort; fetal growth; head circumference; personal monitoring; sensitivity analysis; ultrasonography.

Figures

Figure 1
Figure 1
Head circumference as a function of gestational age at measurement and maternal benzene exposure. Head circumference was assessed between 19 gestational weeks and birth (A), between 19 and 27 gestational weeks (by ultrasonography) (B), between 27 and 35 gestational weeks (by ultrasonography) (C), and between 35 and 43 gestational weeks (after birth) (D). The predicted curves are adjusted for gestational age at examination (polynomial coding and interaction terms with all adjustment variables but education and center), sex, maternal passive smoking (questionnaire data), urinary cotinine level, prepregnancy weight, height, parity, maternal occupational exposure to paints or pesticides, month of conception, maternal education, and center.
Figure 2
Figure 2
Sensitivity analysis: estimated effect of benzene levels (≥ 2.6 μg/m3, the reference being < 1.4 μg/m3) on head circumference after exclusion of specific subgroups of the population or adjustment for additional variables. Diamonds indicate point estimates; horizontal lines indicate the 95% CIs. Abbreviations: ETS, environmental tobacco smoke; SGA, small for gestational age. (A) Benzene and head circumference after birth (average of two measurements). (B) Benzene and head circumference at the third trimester (29–36 gestational weeks) ultrasound examination. aThe sample sizes correspond to the adjusted analyses and thus slightly differ from those given in Table 3 or Table 4. bExclusion of women occupationally exposed to paints or pesticides. cExclusion of air samplers stored for ≥ 3 months during any period including a day in the warm season (June–September). dThe single measure of head circumference performed right after birth was used instead of the average of the two independent measures performed shortly after birth.

References

    1. Aguilera I, Sunyer J, Fernandez-Patier R, Hoek G, Aguirre-Alfaro A, Meliefste K, et al. Estimation of outdoor NOx, NO2, and BTEX exposure in a cohort of pregnant women using land use regression modeling. Environ Sci Technol. 2008;42(3):815–821.
    1. ATSDR. Toxicological Profile for Benzene. Atlanta, GA: Agency for Toxic Substances and Disease Registry; 2007.
    1. Ballesta PP, Field RA, Connolly R, Cao N, Baeza Caracena A, De Saeger E. Population exposure to benzene: one day cross-sections in six European cities. Atmos Environ. 2006;40(18):3355–3366.
    1. Blondel B, Supernant K, Du Mazaubrun C, Breart G. Trends in perinatal health in metropolitan France between 1995 and 2003: results from the National Perinatal Surveys [in French] J Gynecol Obstet Biol Reprod (Paris) 2006;35(4):373–387.
    1. Bruinen de Bruin Y, Koistinen K, Kephalopoulos S, Geiss O, Tirendi S, Kotzias D. Characterisation of urban inhalation exposures to benzene, formaldehyde and acetaldehyde in the European Union: comparison of measured and modelled exposure data. Environ Sci Pollut Res Int. 2008;15(5):417–430.
    1. Chen D, Cho SI, Chen C, Wang X, Damokosh AI, Ryan L, et al. Exposure to benzene, occupational stress, and reduced birth weight. Occup Environ Med. 2000;57(10):661–667.
    1. Choi H, Jedrychowski W, Spengler J, Camann DE, Whyatt RM, Rauh V, et al. International studies of prenatal exposure to polycyclic aromatic hydrocarbons and fetal growth. Environ Health Perspect. 2006;114:1744–1750.
    1. Cocheo V, Boaretto C, Sacco P. High uptake rate radial diffusive sampler suitable for both solvent and thermal desorption. Am Ind Hyg Assoc J. 1996;57:897–904.
    1. Cocheo V, Sacco P, Boaretto C, De Saeger E, Ballesta PP, Skov H, et al. Urban benzene and population exposure. Nature. 2000;404(6774):141–142.
    1. Cuzick J. A Wilcoxon-type test for trend. Stat Med. 1985;4(1):87–90.
    1. Dempsey D, Jacob P, III, Benowitz NL. Accelerated metabolism of nicotine and cotinine in pregnant smokers. J Pharmacol Exp Ther. 2002;301(2):594–598.
    1. Drouillet P, Kaminski M, De Lauzon-Guillain B, Forhan A, Ducimetière P, Schweitzer M, et al. Association between maternal seafood consumption before pregnancy and fetal growth: evidence for an association in overweight women. The EDEN mother-child cohort. Paediatr Perinatal Epidemiol. 2009;23(1):76–86.
    1. Feng S, Kapur S, Sarkar M, Muhammad R, Mendes P, Newland K, et al. Respiratory retention of nicotine and urinary excretion of nicotine and its five major metabolites in adult male smokers. Toxicol Lett. 2007;173(2):101–106.
    1. Ghosh R, Rankin J, Pless-Mulloli T, Glinianaia S. Does the effect of air pollution on pregnancy outcomes differ by gender? A systematic review. Environ Res. 2007;105(3):400–408.
    1. Glinianaia SV, Rankin J, Bell R, Pless-Mulloli T, Howel D. Particulate air pollution and fetal health: a systematic review of the epidemiologic evidence. Epidemiology. 2004;15(1):36–45.
    1. Hadlock FP. Ultrasound évaluation of fetal growth. In: Callen PW, editor. Ultrasonography in Obstetrics and Gynecology. Philadelphia: W.B. Saunders; 1994. pp. 129–143.
    1. Hansen CA, Barnett AG, Pritchard G. The effect of ambient air pollution during early pregnancy on fetal ultrasonic measurements during mid-pregnancy. Environ Health Perspect. 2008;116:362–369.
    1. Ilgen E, Levsen K, Angerer J, Schneider P, Heinrich J, Wichmann HE. Aromatic hydrocarbons in the atmospheric environment. Part II: univariate and multivariate analysis and case studies of indoor concentrations. Atmos Environ. 2001a;35:1253–1264.
    1. Ilgen E, Levsen K, Angerer J, Schneider P, Heinrich J, Wichmann HE. Aromatic hydrocarbons in the atmospheric environment. Part III: personal monitoring. Atmos Environ. 2001b;35:1265–1279.
    1. Jedrychowski W, Bendkowska I, Flak E, Penar A, Jacek R, Kaim I, et al. Estimated risk for altered fetal growth resulting from exposure to fine particles during pregnancy: an epidemiologic prospective cohort study in Poland. Environ Health Perspect. 2004;112:1398–1402.
    1. Jedrychowski W, Perera F, Mrozek-Budzyn D, Mroz E, Flak E, Spengler JD, et al. Gender differences in fetal growth of newborns exposed prenatally to airborne fine particulate matter. Environ Res. 2009;109(4):447–456.
    1. Jo WK, Park KH. Concentrations of volatile organic compounds in the passenger side and the back seat of automobiles. J Expo Anal Environ Epidemiol. 1999;9(3):217–227.
    1. Kannan S, Misra DP, Dvonch JT, Krishnakumar A. Exposures to airborne particulate matter and adverse perinatal outcomes: a biologically plausible mechanistic framework for exploring potential effect modification by nutrition. Environ Health Perspect. 2006;114:1636–1642.
    1. Krzyzanowski M, Kuna-Dibbert B, Schneider J, editors. Health Effects of Transport-Related Air Pollution. Copenhagen: World Health Organization, Regional Office for Europe; 2005. [[accessed 9 July 2009]]. Available: .
    1. Lacasana M, Esplugues A, Ballester F. Exposure to ambient air pollution and prenatal and early childhood health effects. Eur J Epidemiol. 2005;20(2):183–199.
    1. Lindley AA, Benson JE, Grimes C, Cole TM, III, Herman AA. The relationship in neonates between clinically meas ured head circumference and brain volume estimated from head CT-scans. Early Hum Dev. 1999;56(1):17–29.
    1. Mamelle N, Munoz F, Grandjean H. Fetal growth from the AUDIPOG study. I. Establishment of reference curves [in French] J Gynecol Obstet Biol Reprod (Paris) 1996;25(1):61–70.
    1. Parker JD, Woodruff TJ, Basu R, Schoendorf KC. Air pollution and birth weight among term infants in California. Pediatrics. 2005;115(1):121–128.
    1. Perera FP, Rauh V, Whyatt RM, Tang D, Tsai WY, Bernert JT, et al. A summary of recent findings on birth outcomes and developmental effects of prenatal ETS, PAH, and pesticide exposures. Neurotoxicology. 2005;26(4):573–587.
    1. Perera FP, Rauh V, Whyatt RM, Tsai WY, Tang D, Diaz D, et al. Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3 years of life among inner-city children. Environ Health Perspect. 2006;114:1287–1292.
    1. Proctor CJ, Warren ND, Bevan MAJ, Baker-Rogers J. A comparison of methods of assessing exposure to environmental tobacco smoke in non-smoking British women. Environ Int. 1991;17(4):287–297.
    1. Ritz B, Wilhelm M. Ambient air pollution and adverse birth outcomes: methodologic issues in an emerging field. Basic Clin Pharmacol Toxicol. 2008;102(2):182–190.
    1. Ritz B, Yu F. The effect of ambient carbon monoxide on low birth weight among children born in southern California between 1989 and 1993. Environ Health Perspect. 1999;107:17–25.
    1. Rocha ESIR, Lichtenfels AJ, Amador Pereira LA, Saldiva PH. Effects of ambient levels of air pollution generated by traffic on birth and placental weights in mice. Fertil Steril. 2008;90(5):1921–1924.
    1. Rothman KJ, Greenland S. Modern Epidemiology. 2nd ed. Philadelphia: Lippincott-Raven; 1998.
    1. Schauer JJ, Kleeman MJ, Cass GR, Simoneit BR. Measurement of emissions from air pollution sources. 2. C1 through C30 organic compounds from medium duty diesel trucks. Environ Sci Technol. 1999;33(10):1578–1587.
    1. Schauer JJ, Kleeman MJ, Cass GR, Simoneit BR. Measurement of emissions from air pollution sources. 5. C1–C32 organic compounds from gasoline-powered motor vehicles. Environ Sci Technol. 2002;36(6):1169–1180.
    1. Slama R, Darrow LA, Parker JD, Woodruff TJ, Strickland M, Nieuwenhuijsen M, et al. Atmospheric pollution and human reproduction: report of the Munich International Workshop. Environ Health Perspect. 2008a;116:791–798.
    1. Slama R, Khoshnood B, Kaminski M. How to control for gestational age in studies of effects of environmental factors on fetal growth? [Letter] Environ Health Perspect. 2008b;116:A284.
    1. Slama R, Werwatz A. Controlling for continuous confounding factors: non- and semi-parametric approaches. Rev Epidemiol Sante Publique. 2005;53(2S):S65–S80.
    1. Takeda K, Tsukue N, Yoshida S. Endocrine-disrupting activity of chemicals in diesel exhaust and diesel exhaust particles. Environ Sci. 2004;11(1):33–45.
    1. Topp R, Cyrys J, Gebefugi I, Schnelle-Kreis J, Richter K, Wichmann HE, et al. Indoor and outdoor air concentrations of BTEX and NO2: correlation of repeated measurements. J Environ Monit. 2004;6(10):807–812.
    1. Veras MM, Damaceno-Rodrigues NR, Caldini EG, Maciel Ribeiro AA, Mayhew TM, Saldiva PH, et al. Particulate urban air pollution affects the functional morphology of mouse placenta. Biol Reprod. 2008;79(3):578–584.
    1. Wallace L. Environmental exposure to benzene: an update. Environ Health Perspect. 1996;104(suppl 6):1129–1136.
    1. Wang X, Chen D, Niu T, Wang Z, Wang L, Ryan L, et al. Genetic susceptibility to benzene and shortened gestation: evidence of gene-environment interaction. Am J Epidemiol. 2000;152(8):693–700.
    1. Wilhelm M, Ritz B. Residential proximity to traffic and adverse birth outcomes in Los Angeles County, California, 1994–1996. Environ Health Perspect. 2003;111:207–216.
    1. Yanney M, Marlow N. Paediatric consequences of fetal growth restriction. Semin Fetal Neonatal Med. 2004;9(5):411–418.
    1. Zaren B, Lindmark G, Bakketeig L. Maternal smoking affects fetal growth more in the male fetus. Paediatr Perinat Epidemiol. 2000;14(2):118–126.
    1. Zhu Y, Eiguren-Fernandez A, Hinds WC, Miguel AH. In-cabin commuter exposure to ultrafine particles on Los Angeles freeways. Environ Sci Technol. 2007;41(7):2138–2145.

Source: PubMed

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