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The joint effects of prenatal exposure to PM2.5 constituents and reduced fetal growth on children’s accelerated growth in the first 3 years: a birth cohort study

Abstract

Background

Prenatal fine particulate matter (PM2.5) constituents exposure and reduced fetal growth may be risk factors for accelerated growth in early childhood, an important indicator for lifelong health.

Objective

The study investigated whether the joint effects are present between PM2.5 constituents and reduced fetal growth.

Methods

The study was embedded in a birth cohort in China, including 5424 mother-child pairs. Prenatal PM2.5 and its constituents’ [organic carbon (OC), elementary carbon (EC), ammonium (NH4+), nitrate (NO3), and sulfate (SO42−)] concentrations were estimated based on maternal residential addresses. Fetal growth was evaluated by fetal growth trajectory in utero and preterm birth (PTB), low birth weight (LBW), and small for gestational age (SGA). Children’s accelerated growth was defined as body mass index (BMI) Z-score change of >0.67 between birth and 3 years. Generalized logistic regression was used to analyze the effects of prenatal PM2.5 constituents exposure and fetal growth on children’s accelerated growth. Joint effect was tested on multiplicative scale and additive scale with the relative excess risk due to interaction (RERI).

Results

Children with lower fetal growth trajectory, PTB, LBW, and SGA had increased odds of children’s accelerated growth, with odds ratios (ORs) ranging from 1.704 to 11.605. Compared with lower exposure (≤median), higher exposure (>median) of PM2.5, OC, and SO42− were significantly associated with increased odds of children’s accelerated growth, varying in ORs from 1.163 to 1.478. Prenatal exposure to OC had joint effects with lower fetal growth on children’s accelerated growth. We observed that the interaction was statistically significant on an additive scale in OC and lower fetal growth trajectory (RERI: 0.497, 95% CI: 0.033,0.962).

Impact

Fine particulate matter (PM2.5) is a huge threat to human health worldwide, causing 6.7 million death globally in 2019. According to the theory of DOHaD, prenatal PM2.5 exposure could influence early childhood growth, which is important for lifelong health. We found that prenatal exposure to PM2.5, OC, and SO42− was associated with higher risk of accelerated childhood growth in the first 3 years. More importantly, reduced fetal growth moderated these associations. Our findings highlight the need for policies and interventions on PM2.5 constituents to improve lifelong health, especially for those vulnerable populations with reduced fetal growth.

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Fig. 1: The joint effects of prenatal exposure to PM2.5 or its constituents and fetal growth trajectory on children’s accelerated growth from birth to 3 years old.

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Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Barker DJP. The origins of the developmental origins theory. J Intern Med. 2007;261:412–7.

    Article  CAS  PubMed  Google Scholar 

  2. Matthews EK, Wei J, Cunningham SA. Relationship between prenatal growth, postnatal growth and childhood obesity: a review. Eur J Clin Nutr. 2017;71:919–30.

    Article  CAS  PubMed  Google Scholar 

  3. Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 2000;320:967–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Eriksson JG, Forsén T, Tuomilehto J, Osmond C, Barker DJP. Early growth and coronary heart disease in later life: longitudinal study. BMJ. 2001;322:949–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Linda SA, Tim JC. Rapid child growth raises blood pressure in adolescent boys who were thin at birth. Hypertension. 2003;41:451–6.

    Article  Google Scholar 

  6. Mao G, Nachman RM, Sun Q, Zhang X, Koehler K, Chen Z, et al. Individual and joint effects of early-life ambient exposure and maternal prepregnancy obesity on childhood overweight or obesity. Environ Health Perspect. 2017;125:067005.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chiu Y-HM, Hsu H-HL, Wilson A, Coull BA, Pendo MP, Baccarelli A, et al. Prenatal particulate air pollution exposure and body composition in urban preschool children: examining sensitive windows and sex-specific associations. Environ Res. 2017;158:798–805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Fleisch AF, Rifas-Shiman SL, Koutrakis P, Schwartz JD, Kloog I, Melly S, et al. Prenatal exposure to traffic pollution: associations with reduced fetal growth and rapid infant weight gain. Epidemiology. 2015;26:43–50.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Fleisch AF, Luttmann-Gibson H, Perng W, Rifas-Shiman SL, Coull BA, Kloog I, et al. Prenatal and early life exposure to traffic pollution and cardiometabolic health in childhood. Pediatr Obes. 2017;12:48–57.

    Article  CAS  PubMed  Google Scholar 

  10. Sears CG, Mueller-Leonhard C, Wellenius GA, Chen A, Ryan P, Lanphear BP, et al. Early-life exposure to traffic-related air pollution and child anthropometry. Environ Epidemiol. 2019;3:e061.

  11. Patterson WB, Glasson J, Naik N, Jones RB, Berger PK, Plows JF, et al. Prenatal exposure to ambient air pollutants and early infant growth and adiposity in the Southern California Mother’s Milk Study. Environ Health. 2021;20:67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Starling AP, Moore BF, Thomas DSK, Peel JL, Zhang W, Adgate JL, et al. Prenatal exposure to traffic and ambient air pollution and infant weight and adiposity: the Healthy Start study. Environ Res. 2020;182:109130.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Cho H-J, Lee S-H, Lee S-Y, Kim H-C, Kim H-B, Park MJ, et al. Mid-pregnancy PM2.5 exposure affects sex-specific growth trajectories via ARRDC3 methylation. Environ Res. 2021;200:111640.

    Article  CAS  PubMed  Google Scholar 

  14. Kim JS, Alderete TL, Chen Z, Lurmann F, Rappaport E, Habre R, et al. Longitudinal associations of in utero and early life near-roadway air pollution with trajectories of childhood body mass index. Environ Health. 2018;17:64.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Fossati S, Valvi D, Martinez D, Cirach M, Estarlich M, Fernández-Somoano A, et al. Prenatal air pollution exposure and growth and cardio-metabolic risk in preschoolers. Environ Int. 2020;138:105619.

    Article  CAS  PubMed  Google Scholar 

  16. Rosofsky AS, Fabian MP, Ettinger de Cuba S, Sandel M, Coleman S, Levy JI, et al. Prenatal ambient particulate matter exposure and longitudinal weight growth trajectories in early childhood. Int J Environ Res Public Health. 2020;17:1444.

  17. Fleisch AF, Aris IM, Rifas-Shiman SL, Coull BA, Luttmann-Gibson H, Koutrakis P, et al. Prenatal exposure to traffic pollution and childhood body mass index trajectory. Front Endocrinol. 2019;9:771.

    Article  Google Scholar 

  18. Sun X, Liu C, Liang H, Miao M, Wang Z, Ji H, et al. Prenatal exposure to residential PM2.5 and its chemical constituents and weight in preschool children: a longitudinal study from Shanghai, China. Environ Int. 2021;154:106580.

    Article  CAS  PubMed  Google Scholar 

  19. Moore BF, Starling AP, Martenies SE, Magzamen S, Dabelea D. Joint effects of ambient air pollution and maternal smoking on neonatal adiposity and childhood BMI trajectories in the Healthy Start study. Environ Epidemiol. 2021;5:e142.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bell ML, Dominici F, Ebisu K, Zeger SL, Samet JM. Spatial and temporal variation in PM2.5 chemical composition in the United States for health effects studies. Environ Health Perspect. 2007;115:989–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gillman MW. Developmental origins of health and disease. N Engl J Med. 2005;353:1848–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Wei Y, Zhang JJ, Li Z, Gow A, Chung KF, Hu M, et al. Chronic exposure to air pollution particles increases the risk of obesity and metabolic syndrome: findings from a natural experiment in Beijing. FASEB J. 2016;30:2115–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bolton JL, Smith SH, Huff NC, Gilmour MI, Foster WM, Auten RL, et al. Prenatal air pollution exposure induces neuroinflammation and predisposes offspring to weight gain in adulthood in a sex-specific manner. FASEB J. 2012;26:4743–54.

    Article  CAS  PubMed  Google Scholar 

  24. Lin L, Li Q, Yang J, Han N, Jin C, Xu X, et al. The associations of particulate matters with fetal growth in utero and birth weight: a birth cohort study in Beijing, China. Sci Total Environ. 2020;709:136246.

    Article  CAS  PubMed  Google Scholar 

  25. Zhou S, Lin L, Bao Z, Meng T, Wang S, Chen G, et al. The association of prenatal exposure to particulate matter with infant growth: a birth cohort study in Beijing, China. Environ Pollut. 2021;277:116792.

    Article  CAS  PubMed  Google Scholar 

  26. Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK. Estimation of fetal weight with the use of head, body, and femur measurements—a prospective study. Am J Obstet Gynecol. 1985;151:333–7.

    Article  CAS  PubMed  Google Scholar 

  27. Genolini C, Falissard B. KmL: k-means for longitudinal data. Comput Stat. 2010;25:317–28.

    Article  Google Scholar 

  28. WHO: recommended definitions, terminology and format for statistical tables related to the perinatal period and use of a new certificate for cause of perinatal deaths. Modifications recommended by FIGO as amended October 14, 1976. Acta Obstet Gynecol Scand. 1977;56:247–53.

  29. Villar J, Ismail LC, Victora CG, Ohuma EO, Bertino E, Altman DG, et al. International standards for newborn weight, length, and head circumference by gestational age and sex: the Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet. 2014;384:857–68.

    Article  PubMed  Google Scholar 

  30. World Health Organization. Training course on child growth assessment. Geneva: WHO; 2008.

  31. WHO Multicentre Growth Reference Study Group, de Onis M. WHO Child Growth Standards based on length/height, weight and age. Acta Paediatr. 2006;95:76–85.

    Article  Google Scholar 

  32. Duran I, Martakis K, Rehberg M, Stark C, Schafmeyer L, Schönau E. Reference centiles for the evaluation of nutritional status in children using body fat percentage, fat mass and lean body mass index. J Clin Densitom. 2020;23:349–63.

    Article  PubMed  Google Scholar 

  33. den Dekker HT, Jaddoe VWV, Reiss IK, de Jongste JC, Duijts L. Fetal and infant growth patterns and risk of lower lung function and asthma. The Generation R Study. Am J Respir Crit Care Med. 2018;197:183–92.

    Article  Google Scholar 

  34. Sonnenschein-van der Voort AMM, Jaddoe VWV, Raat H, Moll HA, Hofman A, de Jongste JC, et al. Fetal and infant growth and asthma symptoms in preschool children: the Generation R Study. Am J Respir Crit Care Med. 2012;185:731–7.

    Article  PubMed  Google Scholar 

  35. Heppe DHM, Kiefte-de Jong JC, Durmuş B, Moll HA, Raat H, Hofman A, et al. Parental, fetal, and infant risk factors for preschool overweight: the Generation R Study. Pediatr Res. 2013;73:120–7.

    Article  CAS  PubMed  Google Scholar 

  36. Chen G, Li S, Knibbs LD, Hamm NAS, Cao W, Li T, et al. A machine learning method to estimate PM(2.5) concentrations across China with remote sensing, meteorological and land use information. Sci Total Environ. 2018;636:52–60.

    Article  CAS  PubMed  Google Scholar 

  37. Hu J, Li X, Huang L, Ying Q, Zhang Q, Zhao B, et al. Ensemble prediction of air quality using the WRF/CMAQ model system for health effect studies in China. Atmos Chem Phys. 2017;17:13103–18.

    Article  CAS  Google Scholar 

  38. Skamarock WC, Klemp JB, Dudhia J, Gill DO, Barker DM, Duda MG, et al. A description of the advanced research WRF version 3, NCAR Technical Note. Boulder, CO, USA: National Center for Atmospheric Research; 2008. p. 113.

  39. Guenther A, Jiang X, Heald CL, Sakulyanontvittaya T, Duhl TA, Emmons, et al. The model of emissions of gases and aerosols from nature version 2.1 (MEGAN2. 1): an extended and updated framework for modeling biogenic emissions. Geosci Model Dev. 2012;5:1471–92.

    Article  Google Scholar 

  40. Hu J, Wang P, Ying Q, Zhang H, Chen J, Ge X, et al. Modeling biogenic and anthropogenic secondary organic aerosol in China. Atmos Chem Phys. 2017;17:77–92.

    Article  CAS  Google Scholar 

  41. Randell H, Gray C, Grace K. Stunted from the start: early life weather conditions and child undernutrition in Ethiopia. Soc Sci Med. 2020;261:113234.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Tutz G, Ramzan S. Improved methods for the imputation of missing data by nearest neighbor methods. Comput Stat Data Anal. 2015;90:84–99.

    Article  Google Scholar 

  43. Tyler JV, Mirjam JK. A tutorial on interaction. Epidemiol Methods. 2014;3:33–72.

    Google Scholar 

  44. Sánchez BN, Hu H, Litman HJ, Téllez-Rojo MM. Statistical methods to study timing of vulnerability with sparsely sampled data on environmental toxicants. Environ Health Perspect. 2011;119:409–15.

    Article  PubMed  Google Scholar 

  45. Tingley D, Yamamoto T, Hirose K, Keele L, Imai K. Mediation: R package for causal mediation analysis. 2014.

  46. Yang Y, Ruan Z, Wang X, Yang Y, Mason TG, Lin H, et al. Short-term and long-term exposures to fine particulate matter constituents and health: a systematic review and meta-analysis. Environ Pollut. 2019;247:874–82.

    Article  CAS  PubMed  Google Scholar 

  47. Durmuş B, Mook-Kanamori DO, Holzhauer S, Hofman A, van der Beek EM, Boehm G, et al. Growth in foetal life and infancy is associated with abdominal adiposity at the age of 2 years: the generation R study. Clin Endocrinol. 2010;72:633–40.

    Article  Google Scholar 

  48. Bloomfield FH, Oliver MH, Harding JE. The late effects of fetal growth patterns. Arch Dis Child Fetal Neonatal Ed. 2006;91:F299–304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ju L, Hua L, Xu H, Li C, Sun S, Zhang Q, et al. Maternal atmospheric particulate matter exposure and risk of adverse pregnancy outcomes: a meta-analysis of cohort studies. Environ Pollut. 2023;317:120704.

    Article  CAS  PubMed  Google Scholar 

  50. Kroener L, Wang ET, Pisarska MD. Predisposing factors to abnormal first trimester placentation and the impact on fetal outcomes. Semin Reprod Med. 2016;34:027–35.

    Article  Google Scholar 

  51. Turpin BJ, Huntzicker JJ. Identification of secondary organic aerosol episodes and quantitation of primary and secondary organic aerosol concentrations during SCAQS. Atmos Environ. 1995;29:3527–44.

    Article  CAS  Google Scholar 

  52. Bové H, Bongaerts E, Slenders E, Bijnens EM, Saenen ND, Gyselaers W, et al. Ambient black carbon particles reach the fetal side of human placenta. Nat Commun. 2019;10:3866.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Breier BH, Vickers MH, Ikenasio BA, Chan KY, Wong WPS. Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001;185:73–79.

    Article  CAS  PubMed  Google Scholar 

  54. Oken E, Gillman MW. Fetal origins of obesity. Obes Res. 2003;11:496–506.

    Article  PubMed  Google Scholar 

  55. Romano M, Guagnano MT, Pacini G, Vigneri S, Falco A, Marinopiccoli M, et al. Association of inflammation markers with impaired insulin sensitivity and coagulative activation in obese healthy women. J Clin Endocrinol Metab. 2003;88:5321–6.

    Article  CAS  PubMed  Google Scholar 

  56. Chang C-J, Jian D-Y, Lin M-W, Zhao J-Z, Ho L-T, Juan C-C. Evidence in obese children: contribution of hyperlipidemia, obesity-inflammation, and insulin sensitivity. PLoS ONE. 2015;10:e0125935.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Chen L, Bell EM, Caton AR, Druschel CM, Lin S. Residential mobility during pregnancy and the potential for ambient air pollution exposure misclassification. Environ Res. 2010;110:162–8.

    Article  CAS  PubMed  Google Scholar 

  58. Pereira G, Bracken MB, Bell ML. Particulate air pollution, fetal growth and gestational length: the influence of residential mobility in pregnancy. Environ Res. 2016;147:269–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

The present study was supported by the National Natural Science Foundation of China (Grant No. 81973053). SZ was supported by the China Scholarship Council at the Erasmus University Medical Centre, Rotterdam, The Netherlands (202106010220) as well as the Innovation Fund for Outstanding PhD Candidates of Peking University Health Science Centre.

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Contributions

SZ: conceptualization, methodology, writing—original draft, formal analysis. TTL, KZ, GBC, YZ, QL, JLH, TL, HR and YMG: methodology, software, writing—review and editing. NH, YLJ, JL and HW: investigation, resources, writing—review and editing. HJW: supervision, conceptualization, project administration, writing—review and editing.

Corresponding author

Correspondence to Haijun Wang.

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The study was approved by the Institutional Review Board of Peking University Health Science Center (No. IRB00001052-21023).

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Zhou, S., Li, T., Han, N. et al. The joint effects of prenatal exposure to PM2.5 constituents and reduced fetal growth on children’s accelerated growth in the first 3 years: a birth cohort study. J Expo Sci Environ Epidemiol (2024). https://doi.org/10.1038/s41370-024-00658-x

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  • DOI: https://doi.org/10.1038/s41370-024-00658-x

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