Abstract
It has been observed that air pollution can affect newborn health due to the negative effects of pollutants on pregnancy development. However, few studies have evaluated the impact of maternal exposure to urban air pollution on head circumference (HC) at birth. Reduced head growth during pregnancy may be associated with neurocognitive deficits in childhood. The objectives of this study were to evaluate the association between maternal exposure to air pollution and HC at birth and to provide context with a systematic review to investigate this association. This was a prospective study of low-risk pregnant women living in São Paulo, Brazil. Exposure to pollutants, namely, nitrogen dioxide (NO2) and ozone (O3), was measured during each trimester using passive personal samplers. We measured newborn HC until 24 h after birth. We used multiple linear regression models to evaluate the association between pollutants and HC while controlling for known determinants of pregnancy. To perform the systematic review, four different electronic databases were searched through November 2018: CENTRAL, EMBASE, LILACS, and MEDLINE. We selected longitudinal or transversal designs associating air pollution and HC at birth. Two reviewers evaluated the inclusion criteria and risk of bias and extracted data from the included papers. Thirteen studies were selected for the systematic review. We evaluated 391 patients, and we did not observe a significant association between air pollution and HC. Regarding the systematic review, 13 studies were selected for the systematic review, 8 studies showed an inverse association between maternal exposure to pollutants and HC, 4 showed no association, and one observed a direct association. In the city of São Paulo, maternal exposure to pollutants was not significantly associated with HC at birth. The systematic review suggested an inverse association between air pollution and HC at birth.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Arbex MA, Pereira LA, Carvalho-Oliveira R, Saldiva PH, Braga AL (2014) The effect of air pollution on pneumonia-related emergency department visits in a region of extensive sugar cane plantations: a 30-month time-series study. J Epidemiol Community Health 68(7):669–674. https://doi.org/10.1136/jech-2013-203709
Babson SG, Henderson NB (1974) Fetal undergrowth: relation of head growth to later intellectual performance. Pediatrics 53(6):890–894
Bertin M, Chevrier C, Serrano T, Monfort C, Cordier S, Viel JF (2015) Sex-specific differences in fetal growth in newborns exposed prenatally to traffic-related air pollution in the PELAGIE mother-child cohort (Brittany, France). Environ Res 142:680–687. https://doi.org/10.1016/j.envres.2015.09.006
Brasil. Ministério da Saúde (2011) Secretaria de Atenção à Saúde. Departamento de Ações Programáticas e Estratégicas. Atenção à saúde do recém-nascido: guia para os prossionais de saúde – Brasília : Ministério da Saúde. 4 v. : il. – (Série A. Normas e Manuais Técnicas)
Canfield MA, Ramadhani TA, Langlois PH, Waller DK (2006) Residential mobility patterns and exposure misclassification in epidemiologic studies of birth defects. J Expo Sci Environ Epidemiol 16(6):538–543. https://doi.org/10.1038/sj.jes.7500501
Carneiro MFH, Ribeiro FQ, Fernandes-Filho FN, Lobo DJA, Barbosa F Jr, Rhoden CR, Mauad T, Saldiva PHN, Carvalho-Oliveira R (2011) Pollen abortion rates, nitrogen dioxide by passive diffusive tubes and bioaccumulation in tree barks are effective in the characterization of air pollution. Environ Exp Bot 72:272–277
Carvalho MA, Bernardes LS, Hettfleisch K, Pastro LD, Vieira SE, Saldiva SR, Saldiva PH, Francisco RP (2016) Associations of maternal personal exposure to air pollution on fetal weight and fetoplacental Doppler: a prospective cohort study. Reprod Toxicol 62:9–17. https://doi.org/10.1016/j.reprotox.2016.04.013
Cattaneo A, Taronna A, Garramone A, Peruzzo C, Schlitt C, Consonni D (2010) Comparison between personal and individual exposure to urban air pollutants. Aerosol Sci Technol 44:370–379
Choi H, Jedrychowski W, Spengler J, Camann DE, Whyatt RM, Rauh V, Tsai WY, Perera FP (2006) International studies of prenatal exposure to polycyclic aromatic hydrocarbons and fetal growth. Environ Health Perspect 114(11):1744–1750
Clemens T, Turner S, Dibben C (2017) Maternal exposure to ambient air pollution and fetal growth in North-East Scotland: a population-based study using routine ultrasound scans. Environ Int 107:216–226. https://doi.org/10.1016/j.envint.2017.07.018
Conceição GM, Miraglia SG, Kishi HS, Saldiva PH, Singer JM (2001) Air pollution and child mortality: a time-series study in São Paulo, Brazil. Environ Health Perspect 109(Suppl 3):347–350
Dadvand P, Parker J, Bell ML, Bonzini M, Brauer M, Darrow LA, Gehring U, Glinianaia SV, Gouveia N, Ha EH, Leem JH, van den Hooven EH, Jalaludin B, Jesdale BM, Lepeule J, Morello-Frosch R, Morgan GG, Pesatori AC, Pierik FH, Pless-Mulloli T, Rich DQ, Sathyanarayana S, Seo J, Slama R, Strickland M, Tamburic L, Wartenberg D, Nieuwenhuijsen MJ, Woodruff TJ (2013) Maternal exposure to particulate air pollution and term birth weight: a multi-country evaluation of effect and heterogeneity. Environ Health Perspect 121(3):267–373. https://doi.org/10.1289/ehp.1205575
de André CDS, de André PA, Rocha FM, Saldiva PHN, de Oliveira RC, Singer JM (2014) Reliability of reflectance measures in passive filters. Atmos Environ 92:178–181
Edwards SC, Jedrychowski W, Butscher M, Camann D, Kieltyka A, Mroz E, Flak E, Li Z, Wang S, Rauh V, Perera F (2010) Prenatal exposure to airborne polycyclic aromatic hydrocarbons and children’s intelligence at 5 years of age in a prospective cohort study in Poland. Environ Health Perspect 118(9):1326–1331. https://doi.org/10.1289/ehp.0901070
Eriksen HL, Kesmodel US, Underbjerg M, Kilburn TR, Bertrand J, Mortensen EL (2013) Predictors of intelligence at the age of 5: family, pregnancy and birth characteristics, postnatal influences, and postnatal growth. PLoS One 8(11):e79200. https://doi.org/10.1371/journal.pone.0079200
Estarlich M, Ballester F, Aguilera I, Fernández-Somoano A, Lertxundi A, Llop S, Freire C, Tardón A, Basterrechea M, Sunyer J, Iñiguez C (2011) Residential exposure to outdoor air pollution during pregnancy and anthropometric measures at birth in a multicenter cohort in Spain. Environ Health Perspect 119(9):1333–1338. https://doi.org/10.1289/ehp.1002918
Greaves S, Issarayangyun T, Liu Q (2008) Exploring variability in pedestrian exposure to fine particulates (PM2.5) along a busy road. Atmos Environ 42(8):1665–1676
Gulliver J, Briggs DJ (2004) Personal exposure to particulate air pollution in transport microenvironments. Atmos Environ 38(1):1–8
Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK (1985) Estimation of fetal weight with the use of head, body, and femur measurements--a prospective study. Am J Obstet Gynecol 151(3):333–337
Hadlock FP, Shah YP, Kanon DJ, Lindsey JV (1992) Fetal crown-rump length: reevaluation of relation to menstrual age (5-18 weeks) with high-resolution real-time US. Radiology 182(2):501–505. https://doi.org/10.1148/radiology.182.2.1732970
Hansen C, Neller A, Williams G, Simpson R (2007) Low levels of ambient air pollution during pregnancy and fetal growth among term neonates in Brisbane, Australia. Environ Res 103(3):383–389. https://doi.org/10.1016/j.envres.2006.06.010
Heinonen K, Räikkönen K, Pesonen AK, Kajantie E, Andersson S, Eriksson JG, Niemelä A, Vartia T, Peltola J, Lano A (2008) Prenatal and postnatal growth and cognitive abilities at 56 months of age: a longitudinal study of infants born at term. Pediatrics 121(5):e1325–e1333. https://doi.org/10.1542/peds.2007-1172
Hettfleisch K, Bernardes LS, Carvalho MA, Pastro LD, Vieira SE, Saldiva SR, Saldiva P, Francisco RP (2016) Short-term exposure to urban air pollution and influences on placental vascularization indexes. Environ Health Perspect 125:753–759. https://doi.org/10.1289/EHP300
Hjortebjerg D, Andersen AM, Ketzel M, Pedersen M, Raaschou-Nielsen O, Sørensen M (2016) Associations between maternal exposure to air pollution and traffic noise and newborn's size at birth: a cohort study. Environ Int 95:1–7. https://doi.org/10.1016/j.envint.2016.07.003
Hogan MK, Kovalycsik T, Sun Q, Rajagopalan S, Nelson RJ (2015) Combined effects of exposure to dim light at night and fine particulate matter on C3H/HeNHsd mice. Behav Brain Res 294:81–88. https://doi.org/10.1016/j.bbr.2015.07.033
Jedrychowski W, Perera F, Mrozek-Budzyn D, Mroz E, Flak E, Spengler JD, Edwards S, Jacek R, Kaim I, Skolicki Z (2009) Gender differences in fetal growth of newborns exposed prenatally to airborne fine particulate matter. Environ Res 109(4):447–456. https://doi.org/10.1016/j.envres.2009.01.009
Kaur S, Nieuwenhuijsen M, Colvile R (2005) Personal exposure of street canyon intersection users to PM2.5, ultrafine particle counts and carbon monoxide in Central London, UK. Atmos Environ 39(20):3629–3641
Lamichhane DK., Ryu J, Leem JH, Ha M, Hong YC, Park H, Kim Y, Jung DY, Lee JY, Kim HC, Ha EH (2018) Air pollution exposure during pregnancy and ultrasound and birth measures of fetal growth: a prospective cohort study in Korea. Sci Total Environ 619–620:834–841. https://doi.org/10.1016/j.scitotenv.2017.11.058
Lindley AA, Benson JE, Grimes C, Cole TM, Herman AA (1999) The relationship in neonates between clinically measured head circumference and brain volume estimated from head CT-scans. Early Hum Dev 56(1):17–29
Malmqvist E, Liew Z, Källén K, Rignell-Hydbom A, Rittner R, Rylander L, Ritz B (2017) Fetal growth and air pollution-a study on ultrasound and birth measures. Environ Res 152:73–80. https://doi.org/10.1016/j.envres.2016.09.017
Miller A, Siffel C, Correa A (2010) Residential mobility during pregnancy: patterns and correlates. Matern Child Health J 14(4):625–634. https://doi.org/10.1007/s10995-009-0492-z
Novaes P, do Nascimento Saldiva PH, Kara-José N, Macchione M, Matsuda M, Racca L, Berra A (2007) Ambient levels of air pollution induce goblet-cell hyperplasia in human conjunctival epithelium. Environ Health Perspect 115(12):1753–1756. https://doi.org/10.1289/ehp.10363
Pedersen M, Giorgis-Allemand L, Bernard C, Aguilera I, Andersen AM, Ballester F, Beelen RM, Chatzi L, Cirach M, Danileviciute A, Dedele A, Eijsden M, Estarlich M, Fernández-Somoano A, Fernández MF, Forastiere F, Gehring U, Grazuleviciene R, Gruzieva O, Heude B, Hoek G, de Hoogh K, van den Hooven EH, Håberg SE, Jaddoe VW, Klümper C, Korek M, Krämer U, Lerchundi A, Lepeule J, Nafstad P, Nystad W, Patelarou E, Porta D, Postma D, Raaschou-Nielsen O, Rudnai P, Sunyer J, Stephanou E, Sørensen M, Thiering E, Tuffnell D, Varró MJ, Vrijkotte TG, Wijga A, Wilhelm M, Wright J, Nieuwenhuijsen MJ, Pershagen G, Brunekreef B, Kogevinas M, Slama R (2013) Ambient air pollution and low birthweight: a European cohort study (ESCAPE). Lancet Respir Med 1(9):695–704. https://doi.org/10.1016/S2213-2600(13)70192-9
Perera FP, Li Z, Whyatt R, Hoepner L, Wang S, Camann D, Rauh V (2009) Prenatal airborne polycyclic aromatic hydrocarbon exposure and child IQ at age 5 years. Pediatrics 124(2):e195–e202. https://doi.org/10.1542/peds.2008-3506
Peterson BS, Rauh VA, Bansal R, Hao X, Toth Z, Nati G, Walsh K, Miller RL, Arias F, Semanek D, Perera F (2015) Effects of prenatal exposure to air pollutants (polycyclic aromatic hydrocarbons) on the development of brain white matter, cognition, and behavior in later childhood. JAMA Psychiatry 72(6):531–540. https://doi.org/10.1001/jamapsychiatry.2015.57
Piechocki-Minguy A, Plaisance H, Schadkowski C, Sagnier I, Saison JY, Galloo JC, Guillermo R (2006) A case study of personal exposure to nitrogen dioxide using a new high sensitive diffusive sampler. Sci Total Environ 366(1):55–64. https://doi.org/10.1016/j.scitotenv.2005.08.009
Saenen ND, Plusquin M, Bijnens E, Janssen BG, Gyselaers W, Cox B, Fierens F, Molenberghs G, Penders J, Vrijens K, De Boever P, Nawrot TS (2015) In utero fine particle air pollution and placental expression of genes in the brain-derived neurotrophic factor signaling pathway: an ENVIRONAGE birth cohort study. Environ Health Perspect 123(8):834–840. https://doi.org/10.1289/ehp.1408549
Schembari A, de Hoogh K, Pedersen M, Dadvand P, Martinez D, Hoek G, Petherick ES, Wright J, Nieuwenhuijsen MJ (2015) Ambient air pollution and newborn size and adiposity at birth: differences by maternal ethnicity (the born in Bradford study cohort). Environ Health Perspect 123(11):1208–1215. https://doi.org/10.1289/ehp.1408675
Schulman J, Selvin S, Shaw GM, Malcoe LH (1993) Exposure misclassification due to residential mobility during pregnancy in epidemiologic investigations of congenital malformations. Arch Environ Health 48(2):114–119. https://doi.org/10.1080/00039896.1993.9938404
Shaw GM, Malcoe LH (1992) Residential mobility during pregnancy for mothers of infants with or without congenital cardiac anomalies: a reprint. Arch Environ Health 47(3):236–238. https://doi.org/10.1080/00039896.1992.9938355
Slama R, Thiebaugeorges O, Goua V, Aussel L, Sacco P, Bohet A, Forhan A, Ducot B, Annesi-Maesano I, Heinrich J, Magnin G, Schweitzer M, Kaminski M, Charles MA, EDEN Mother-Child Cohort Study Group (2009) Maternal personal exposure to airborne benzene and intrauterine growth. Environ Health Perspect 117(8):1313–1321. https://doi.org/10.1289/ehp.0800465
Steinle S, Reis S, Sabel CE (2013) Quantifying human exposure to air pollution--moving from static monitoring to spatio-temporally resolved personal exposure assessment. Sci Total Environ 443:184–193. https://doi.org/10.1016/j.scitotenv.2012.10.098
Stieb DM, Chen L, Eshoul M, Judek S (2012) Ambient air pollution, birth weight and preterm birth: a systematic review and meta-analysis. Environ Res 117:100–111. https://doi.org/10.1016/j.envres.2012.05.007
Suades-González E, Gascon M, Guxens M, Sunyer J (2015) Air pollution and neuropsychological development: a review of the latest evidence. Endocrinology 156(10):3473–3482. https://doi.org/10.1210/en.2015-1403
Tang D, Li TY, Chow JC, Kulkarni SU, Watson JG, Ho SS, Quan ZY, Qu LR, Perera F (2014) Air pollution effects on fetal and child development: a cohort comparison in China. Environ Pollut 185:90–96. https://doi.org/10.1016/j.envpol.2013.10.019
van den Hooven EH, Pierik FH, de Kluizenaar Y, Willemsen SP, Hofman A, van Ratingen SW, Zandveld PY, Mackenbach JP, Steegers EA, Miedema HM, Jaddoe VW (2012) Air pollution exposure during pregnancy, ultrasound measures of fetal growth, and adverse birth outcomes: a prospective cohort study. Environ Health Perspect 120(1):150–156. https://doi.org/10.1289/ehp.1003316
Wu C-F, Delfino RJ, Floro JN, Quintana PJE, Samimi BS, Kleinman MT (2005) Exposure assessment and modeling of particulate matter for asthmatic children using personal nephelometers. Atmos Environ 39(19):3457–3469
Wylie BJ, Kishashu Y, Matechi E, Zhou Z, Coull B, Abioye AI, Dionisio KL, Mugusi F, Premji Z, Fawzi W, Hauser R, Ezzati M (2017) Maternal exposure to carbon monoxide and fine particulate matter during pregnancy in an urban Tanzanian cohort. Indoor Air 27(1):136–146. https://doi.org/10.1111/ina.12289
Funding
This research was supported by the São Paulo Research Foundation (FAPESP), grant number 2008/57717-6 and grant number 2016/14433-4, FAPESP. This study was also financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation and data collection were performed by Mariana Azevedo Carvalho, Karen Hettfleisch, and Lisandra Stein Bernardes. The first draft of the manuscript was written by Mariana Azevedo Carvalho. Agatha S. Rodrigues and Mariana Azevedo Carvalho performed the statistical analysis. Alexandra Benachi, Sandra Elisabete Vieira, Silvia R D M Saldiva, Paulo Hilário N. Saldiva, and Rossana P. V. Francisco commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
This study was approved by the Research Ethics Committee of São Paulo University School of Medicine (number 132/10), and the study was performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.
Competing interests
The authors declare that they have no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Carvalho, M., Hettfleisch, K., Rodrigues, A.S. et al. Association between exposure to air pollution during intrauterine life and cephalic circumference of the newborn. Environ Sci Pollut Res 28, 9701–9711 (2021). https://doi.org/10.1007/s11356-020-11274-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-11274-1