Abstract
The association between exposure to particulate matter (PM) during pregnancy and abnormal birth outcomes is still inconclusive. This study aims to provide more evidence for this public health concern by investigating birth outcomes and the growth of offspring in mice exposed to PM during pregnancy. C57BL/6 J pregnant mice were exposed to PM via nasal drip at three doses or solvent control. The dam weight gain was recorded during pregnancy. The number of pups, pup weight, and placental weight were recorded at embryonic day 18.5 (E18.5) necropsy. For mice that gave birth naturally, we calculated the gestation length and measured the body weight of offspring once a week from the 1st to the 6th week after birth. The results showed that there were no significant differences in maternal body weight gain, conception rate, pregnancy duration, and litter size among different groups. There were no significant differences in fetal weight, placental weight, and fetal/placental weight ratio at E18.5. Weight gain in offspring was reduced after birth. The average body weight of offspring in the high-dose group was significantly lower than that in the control group at weeks 5 in female pups. There were no significant differences in the body weight of male offspring among groups from 1st to the 6th. Together, our study indicated that maternal exposure to PM did not significantly impact birth outcomes of C57BL/6 J mice but affected growth trajectories in offspring after birth in a dose- and fetal sex-dependent manner.
Similar content being viewed by others
Data availability
Additional data are available in the Supplementary materials. The data analyzed in the current study are available from the corresponding author on reasonable request.
References
Akhbarizadeh, R., Dobaradaran, S., Torkmahalleh, M. A., Saeedi, R., Aibaghi, R., & Ghasemi, F. F. (2021). Suspended fine particulate matter (PM2.5), microplastics (MPs), and polycyclic aromatic hydrocarbons (PAHs) in air: Their possible relationships and health implications. Environmental Research, 192(1096–0953 (Electronic)), 110339. https://doi.org/10.1016/j.envres.2020.110339
Balakrishnan, K., Ghosh, S., Thangavel, G., Sambandam, S., Mukhopadhyay, K., Puttaswamy, N., Sadasivam, A., Ramaswamy, P., Johnson, P., Kuppuswamy, R., Natesan, D., Maheshwari, U., Natarajan, A., Rajendran, G., Ramasami, R., Madhav, S., Manivannan, S., Nargunanadan, S., Natarajan, S., et al. (2018). Exposures to fine particulate matter (PM(2.5)) and birthweight in a rural-urban, mother-child cohort in Tamil Nadu, India. Environmental Research, 161, 524–531. https://doi.org/10.1016/j.envres.2017.11.050
Behlen, J. C., Lau, C. H., Li, Y., Dhagat, P., Stanley, J. A., Rodrigues Hoffman, A., Golding, M. C., Zhang, R., & Johnson, N. M. (2021). Gestational exposure to ultrafine particles reveals sex- and dose-specific changes in offspring birth outcomes, placental morphology, and gene networks. Toxicological Sciences, 184(2), 204–213. https://doi.org/10.1093/toxsci/kfab118
Behnke, M., Smith, V. C., Committee on Substance, A., Committee on, F., & Newborn. (2013). Prenatal substance abuse: short- and long-term effects on the exposed fetus. Pediatrics, 131(3), e1009–1024. https://doi.org/10.1542/peds.2012-3931.
Blond, K., Carslake, D., Gjaerde, L. K., Vistisen, D., Sorensen, T. I. A., Smith, G. D., & Baker, J. L. (2021). Instrumental variable analysis using offspring BMI in childhood as an indicator of parental BMI in relation to mortality. Scientific Reports. https://doi.org/10.1038/s41598-021-01352-w
Boyce, W. T. (2014). The lifelong effects of early childhood adversity and toxic stress. Pediatric Dentistry, 36(2), 102–108.
Brinksma, A., Roodbol, P. F., Sulkers, E., Hooimeijer, H. L., Sauer, P. J., van Sonderen, E., de Bont, E. S., & Tissing, W. J. (2015). Weight and height in children newly diagnosed with cancer. Pediatric Blood & Cancer, 62(2), 269–273. https://doi.org/10.1002/pbc.25301
Chen, M., Liang, S., Zhou, H., Xu, Y., Qin, X., Hu, Z., Wang, X., Qiu, L., Wang, W., Zhang, Y., & Ying, Z. (2017). Prenatal and postnatal mothering by diesel exhaust PM2.5-exposed dams differentially program mouse energy metabolism. Particle and Fibre Toxicology, 14(1), 3. https://doi.org/10.1186/s12989-017-0183-7
Chen, M. J., Liang, S., Zhou, H. F., Xu, Y. Y., Qin, X. B., Hu, Z. Y., Wang, X. K., Qiu, L. L., Wang, W. J., Zhang, Y. H., & Ying, Z. K. (2017). Prenatal and postnatal mothering by diesel exhaust PM2.5-exposed dams differentially program mouse energy metabolism. Particle and Fibre Toxicology. https://doi.org/10.1186/s12989-017-0183-7
Cho, H. J., Lee, S. H., Lee, S. Y., Kim, H. C., Kim, H. B., Park, M. J., Yoon, J., Jung, S., Yang, S. I., Lee, E., Ahn, K., Kim, K. W., Suh, D. I., Sheen, Y. H., Won, H. S., Lee, M. Y., Kim, S. H., Lee, K. J., Choi, S. J., et al. (2021). Mid-pregnancy PM2.5 exposure affects sex-specific growth trajectories via ARRDC3 methylation. Environmental Research, 200, 111640. https://doi.org/10.1016/j.envres.2021.111640
Crump, C. (2020). An overview of adult health outcomes after preterm birth. Early Human Development, 150, 105187. https://doi.org/10.1016/j.earlhumdev.2020.105187
Dang, S., Ding, D., Lu, Y., Su, Q., Lin, T., Zhang, X., Zhang, H., Wang, X., Tan, H., Zhu, Z., & Li, H. (2018). PM2.5 exposure during pregnancy induces hypermethylation of estrogen receptor promoter region in rat uterus and declines offspring birth weights. Environmental Pollution, 243(Pt B), 851–861. https://doi.org/10.1016/j.envpol.2018.09.065
Deyssenroth, M. A., Rosa, M. J., Eliot, M. N., Kelsey, K. T., Kloog, I., Schwartz, J. D., Wellenius, G. A., Peng, S. N., Hao, K., Marsit, C. J., & Chen, J. (2021). Placental gene networks at the interface between maternal PM2.5 exposure early in gestation and reduced infant birthweight. Environmental Research, 199, 111342. https://doi.org/10.1016/j.envres.2021.111342
Dobaradaran, S., Geravandi, S., Goudarzi, G., Idani, E., Salmanzadeh, S., Soltani, F., Yari, A. R., & Mohammadi, M. J. (2016). Determination of cardiovascular and respiratory diseases caused by PM10 exposure in Bushehr, 2013. Journal of Mazandaran University of Medical Sciences, 26(139), 42–52.
Doroodzani, A. K., Dobaradaran, S., Akhbarizadeh, R., Raeisi, A., Rahmani, E., Mahmoodi, M., Nabipour, I., Keshmiri, S., Darabi, A. H., Khamisipour, G., Mahmudpour, M., & Keshtkar, M. (2021). Diet, exposure to polycyclic aromatic hydrocarbons during pregnancy, and fetal growth: A comparative study of mothers and their fetuses in industrial and urban areas in Southwest Iran. Environmental Pollution, 276, 116668. https://doi.org/10.1016/j.envpol.2021.116668
Dutta, A., Alexander, D., Karrison, T., Morhasson-Bello, O., Wilson, N., Atalabi, O. M., Adu, D., Ibigbami, T., Adekunle, S., Adepoju, D., Olamijulo, J., Akinwunmi, O., Afolabi, O. S., Deji-Abiodun, O., Adedokun, B., Aschebrook-Kilfoy, B., Ojengbede, O., & Olopade, C. O. (2021). Household air pollution, ultrasound measurement, fetal biometric parameters and intrauterine growth restriction. Environ Health, 20(1), 74. https://doi.org/10.1186/s12940-021-00756-5
Erickson, A. C., & Arbour, L. (2014). The shared pathoetiological effects of particulate air pollution and the social environment on fetal-placental development. Journal of Environmental and Public Health, 2014, 901017. https://doi.org/10.1155/2014/901017
Erickson, A. C., Ostry, A., Chan, L. H., & Arbour, L. (2016). The reduction of birth weight by fine particulate matter and its modification by maternal and neighbourhood-level factors: a multilevel analysis in British Columbia, Canada. Environmental Health, 15, 51. https://doi.org/10.1186/s12940-016-0133-0
Ezzati, M., Bentham, J., Di Cesare, M., Bilano, V., Bixby, H., Zhou, B., Stevens, G. A., Riley, L. M., Taddei, C., Hajifathalian, K., Lu, Y., Savin, S., Cowan, M. J., Paciore, C. J., Chirita-Emandi, A., Hayes, A. J., Katz, J., Kelishadi, R., Kengne, A. P., et al. (2017). Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: A pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults. Lancet, 390(10113), 2627–2642. https://doi.org/10.1016/S0140-6736(17)32129-3
Faraji Ghasemi, F., Dobaradaran, S., Saeedi, R., Nabipour, I., Nazmara, S., Ranjbar Vakil Abadi, D., Arfaeinia, H., Ramavandi, B., Spitz, J., Mohammadi, M. J., & Keshtkar, M. (2020). Levels and ecological and health risk assessment of PM(2.5)-bound heavy metals in the northern part of the Persian Gulf. Environmental Science and Pollution Research, 27(5), 5305–5313. https://doi.org/10.1007/s11356-019-07272-7
Feng, S., Gao, D., Liao, F., Zhou, F., & Wang, X. (2016). The health effects of ambient PM2.5 and potential mechanisms. Ecotoxicol and Environmental Safety, 128, 67–74. https://doi.org/10.1016/j.ecoenv.2016.01.030
de Gamarra-Oca, L. F., Ojeda, N., Gómez-Gastiasoro, A., Peña, J., Ibarretxe-Bilbao, N., García-Guerrero, M. A., Loureiro, B., & Zubiaurre-Elorza, L. (2021). Long-term neurodevelopmental outcomes after moderate and late preterm birth: A Systematic review. The Journal of Pediatrics, 237, 168–176. https://doi.org/10.1016/j.jpeds.2021.06.004
Freeman, M. E., Kanyicska, B., Lerant, A., & Nagy, G. (2000). Prolactin: structure, function, and regulation of secretion. Physiological Reviews, 80(4), 1523–1631. https://doi.org/10.1152/physrev.2000.80.4.1523
Fujita, E. M., Campbell, D. E., Arnott, W. P., Johnson, T., & Ollison, W. (2014). Concentrations of mobile source air pollutants in urban microenvironments. Journal of the Air & Waste Management Association, 64(7), 743–758. https://doi.org/10.1080/10962247.2013.872708
Gaillard, R. (2015). Maternal obesity during pregnancy and cardiovascular development and disease in the offspring. European Journal of Epidemiology, 30(11), 1141–1152. https://doi.org/10.1007/s10654-015-0085-7
Gallant, M. J., & Ellis, A. K. (2020). Prenatal and early-life exposure to indoor air-polluting factors and allergic sensitization at 2 years of age. Annals of Allergy, Asthma & Immunology, 124(3), 283–287.
Georgescu, T., Swart, J. M., Grattan, D. R., & Brown, R. S. (2021). The prolactin family of hormones as regulators of maternal mood and behaviour. Frontiers in Global Women’s Health, 2, 767467. https://doi.org/10.3389/fgwh.2021.767467
González-Mariscal, G. (2001). Neuroendocrinology of maternal behavior in the rabbit. Hormones and Behavior, 40(2), 125–132.
Goudarzi, G., Alavi, N., Geravandi, S., Idani, E., Behrooz, H. R. A., Babaei, A. A., Alamdari, F. A., Dobaradaran, S., Farhadi, M., & Mohammadi, M. J. (2018). Health risk assessment on human exposed to heavy metals in the ambient air PM10 in Ahvaz, southwest Iran. International Journal of Biometeorology, 62(6), 1075–1083. https://doi.org/10.1007/s00484-018-1510-x
Grandjean, P., Barouki, R., Bellinger, D. C., Casteleyn, L., Chadwick, L. H., Cordier, S., Etzel, R. A., Gray, K. A., Ha, E. H., Junien, C., Karagas, M., Kawamoto, T., Lawrence, B. P., Perera, F. P., Prins, G. S., Puga, A., Rosenfeld, C. S., Sherr, D. H., Sly, P. D., et al. (2015). Life-long implications of developmental exposure to environmental stressors: New perspectives. Endocrinology, 156(10), 3408–3415. https://doi.org/10.1210/En.2015-1350
Grippo, A., Zhang, J., Chu, L., Guo, Y., Qiao, L., Myneni, A. A., & Mu, L. (2018). Air pollution exposure during pregnancy and spontaneous abortion and stillbirth. Reviews on Environmental Health, 33(3), 247–264. https://doi.org/10.1515/reveh-2017-0033
Hajizadeh, Y., Jafari, N., Fanaei, F., Ghanbari, R., Mohammadi, A., Behnami, A., Jafari, A., Aghababayi, M., & Abdolahnejad, A. (2021). Spatial patterns and temporal variations of traffic-related air pollutants and estimating its health effects in Isfahan city, Iran. Journal of Environmental Health Science and Engineering, 19(1), 781–791. https://doi.org/10.1007/s40201-021-00645-6
Hajizadeh, Y., Jafari, N., Mohammadi, A., Momtaz, S. M., Fanaei, F., & Abdolahnejad, A. (2020). Concentrations and mortality due to short- and long-term exposure to PM(2.5)in a megacity of Iran (2014–2019). Environmental Science and Pollution Research, 27(30), 38004–38014. https://doi.org/10.1007/s11356-020-09695-z
Hannam, K., McNamee, R., Baker, P., Sibley, C., & Agius, R. (2014). Air pollution exposure and adverse pregnancy outcomes in a large UK birth cohort: Use of a novel spatio-temporal modelling technique. Scandinavian Journal of Work Environment & Health, 40(5), 518–530. https://doi.org/10.5271/sjweh.3423
Hougaard, K. S., Jensen, K. A., Nordly, P., Taxvig, C., Vogel, U., Saber, A. T., & Wallin, H. (2008). Effects of prenatal exposure to diesel exhaust particles on postnatal development, behavior, genotoxicity and inflammation in mice. Particle and Fibre Toxicology. https://doi.org/10.1186/1743-8977-5-3
Huang, L. T. (2020). Maternal and early-life nutrition and health. International Journal of Environmental Research and Public Health, 17(21), 7982. https://doi.org/10.3390/ijerph17217982
Idani, E., Geravandi, S., Akhzari, M., Goudarzi, G., Alavi, N., Yari, A. R., Mehrpour, M., Khavasi, M., Bahmaei, J., Bostan, H., Dobaradaran, S., Salmanzadeh, S., & Mohammadi, M. J. (2020). Characteristics, sources, and health risks of atmospheric PM10-bound heavy metals in a populated middle eastern city. Toxin Reviews, 39(3), 266–274. https://doi.org/10.1080/15569543.2018.1513034
Jin, L., Zhou, T., Fang, S., Zhou, X., & Bai, Y. (2022). Association of air pollutants and hospital admissions for respiratory diseases in Lanzhou, China, 2014–2019. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-022-01256-2
Kannan, S., Misra, D. P., Dvonch, J. T., & Krishnakumar, A. (2006). Exposures to airborne particulate matter and adverse perinatal outcomes: a biologically plausible mechanistic framework for exploring potential effect modification by nutrition. Environmental Health Perspectives, 114(11), 1636–1642. https://doi.org/10.1289/ehp.9081
Kelly, F. J., & Fussell, J. C. (2015). Air pollution and public health: Emerging hazards and improved understanding of risk. Environmental Geochemistry and Health, 37(4), 631–649. https://doi.org/10.1007/s10653-015-9720-1
Kirwa, K., Feric, Z., Manjourides, J., Alshawabekeh, A., Vega, C. M. V., Cordero, J. F., Meeker, J. D., & Suh, H. H. (2021). Preterm birth and PM25 in Puerto Rico: Evidence from the PROTECT birth cohort. Environmental Health, 20(1), 69. https://doi.org/10.1186/s12940-021-00748-5
Korten, I., Ramsey, K., & Latzin, P. (2017). Air pollution during pregnancy and lung development in the child. Paediatric Respiratory Reviews, 21, 38–46. https://doi.org/10.1016/j.prrv.2016.08.008
Kumar, N. (2016). The exposure uncertainty analysis: The association between birth weight and trimester specific exposure to particulate matter (PM2.5 vs. PM10). International Journal of Environmental Research and Public Health, 13(9), 906. https://doi.org/10.3390/ijerph13090906
Lafuente, R., García-Blàquez, N., Jacquemin, B., & Checa, M. A. (2016). Outdoor air pollution and sperm quality. Fertility and Sterility, 106(4), 880–896. https://doi.org/10.1016/j.fertnstert.2016.08.022
Lee, C. K., Kang, S. G., Lee, J. T., Lee, S. W., Kim, J. H., Kim, D. H., Son, B. C., Kim, K. H., Suh, C. H., Kim, S. Y., & Park, Y. B. (2015). Effects of perfluorooctane sulfuric acid on placental PRL-family hormone production and fetal growth retardation in mice. Molecular and Cellular Endocrinology, 401, 165–172. https://doi.org/10.1016/j.mce.2014.10.026
Lertxundi, A., Baccini, M., Lertxundi, N., Fano, E., Aranbarri, A., Martinez, M. D., Ayerdi, M., Alvarez, J., Santa-Marina, L., Dorronsoro, M., & Ibarluzea, J. (2015). Exposure to fine particle matter, nitrogen dioxide and benzene during pregnancy and cognitive and psychomotor developments in children at 15 months of age. Environment International, 80, 33–40. https://doi.org/10.1016/j.envint.2015.03.007
Li, X. Y., Huang, S. Q., Jiao, A. Q., Yang, X. H., Yun, J. F., Wang, Y. X., Xue, X. W., Chu, Y. Y., Liu, F. F., Liu, Y. S., Ren, M., Chen, X., Li, N., Lu, Y. A., Mao, Z. F., Tian, L. Q., & Xiang, H. (2017). Association between ambient fine particulate matter and preterm birth or term low birth weight: An updated systematic review and meta-analysis. Environmental Pollution, 227, 596–605. https://doi.org/10.1016/j.envpol.2017.03.055
Liang, Z., Yang, Y., Qian, Z., Ruan, Z., Chang, J., Vaughn, M. G., Zhao, Q., & Lin, H. (2019). Ambient PM(2.5) and birth outcomes: Estimating the association and attributable risk using a birth cohort study in nine Chinese cities. Environment International, 126, 329–335. https://doi.org/10.1016/j.envint.2019.02.017
Lindsay, K. L., Buss, C., Wadhwa, P. D., & Entringer, S. (2019). The interplay between nutrition and stress in pregnancy: Implications for fetal programming of brain development. Biological Psychiatry, 85(2), 135–149.
Liu, W., Zhou, Y., Yong, L., Qin, Y., Yu, L., Li, R., Chen, Y., & Xu, Y. (2020). Effects of PM2.5 exposure during gestation on maternal gut microbiota and pregnancy outcomes. Chemosphere, 247, 125879. https://doi.org/10.1016/j.chemosphere.2020a.125879
Liu, W., Zhou, Y., Yong, L., Qin, Y., Yu, L., Li, R., Chen, Y., & Xu, Y. (2020). Effects of PM(2.5) exposure during gestation on maternal gut microbiota and pregnancy outcomes. Chemosphere, 247, 125879. https://doi.org/10.1016/j.chemosphere.2020b.125879
Liu, Y., Tian, Z., He, X., Wang, X., & Wei, H. (2021). Short-term effects of indoor and outdoor air pollution on the lung cancer morbidity in Henan Province, Central China. Environmental Geochemistry and Health, 44(8), 2711–2731. https://doi.org/10.1007/s10653-021-01072-0
Liu, Y., Wang, L., Wang, F., & Li, C. (2016). Effect of fine particulate matter (PM2.5) on rat placenta pathology and perinatal outcomes. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research, 22, 3274–3280. https://doi.org/10.12659/msm.897808
Liu, Y., Xu, J., Chen, D., Sun, P., & Ma, X. (2019). The association between air pollution and preterm birth and low birth weight in Guangdong, China. BMC Public Health, 19(1), 1–10.
Lu, X., Li, R. Q., & Yan, X. X. (2021). Airway hyperresponsiveness development and the toxicity of PM2.5. Environmental Science and Pollution Research, 28(6), 6374–6391.
Luu, T. M., Mian, M. O. R., & Nuyt, A. M. (2017). Long-term impact of preterm birth: Neurodevelopmental and physical health outcomes. Clinics in Perinatology, 44(2), 305–314. https://doi.org/10.1016/j.clp.2017.01.003
Maluf, M., Perin, P. M., Januário, D. A. N. F., & Saldiva, P. H. N. (2009). In vitro fertilization, embryo development, and cell lineage segregation after pre-and/or postnatal exposure of female mice to ambient fine particulate matter. Fertility and Sterility, 92(5), 1725–1735. https://doi.org/10.1016/j.fertnstert.2008.08.081
Means, R. T. (2020). Iron deficiency and iron deficiency anemia: Implications and impact in pregnancy, fetal development, and early childhood parameters. Nutrients. https://doi.org/10.3390/nu12020447
Momtazan, M., Geravandi, S., Rastegarimehr, B., Valipour, A., Ranjbarzadeh, A., Yari, A. R., Dobaradaran, S., Bostan, H., Farhadi, M., Darabi, F., Khaniabadi, Y. O., & Mohammadi, M. J. (2019). An investigation of particulate matter and relevant cardiovascular risks in Abadan and Khorramshahr in 2014?2016. Toxin Reviews, 38(4), 290–297. https://doi.org/10.1080/15569543.2018.1463266
Moore, B. F., Starling, A. P., Martenies, S. E., Magzamen, S., & Dabelea, D. (2021). Joint effects of ambient air pollution and maternal smoking on neonatal adiposity and childhood BMI trajectories in the Healthy Start study. Environmental Epidemiology, 5(3), e142. https://doi.org/10.1097/EE9.0000000000000142
Motesaddi Zarandi, S., Shahsavani, A., Khodagholi, F., & Fakhri, Y. (2019). Concentration, sources and human health risk of heavy metals and polycyclic aromatic hydrocarbons bound PM2.5 ambient air, Tehran, Iran. Environmental Geochemistry and Health, 41(3), 1473–1487. https://doi.org/10.1007/s10653-018-0229-2
Nephew, B. C., Nemeth, A., Hudda, N., Beamer, G., Mann, P., Petitto, J., Cali, R., Febo, M., Kulkarni, P., Poirier, G., King, J., Durant, J. L., & Brugge, D. (2020). Traffic-related particulate matter affects behavior, inflammation, and neural integrity in a developmental rodent model. Environmental research, 183, 109242. https://doi.org/10.1016/j.envres.2020.109242
Peng, R. D., Bell, M. L., Geyh, A. S., McDermott, A., Zeger, S. L., Samet, J. M., & Dominici, F. (2009). Emergency admissions for cardiovascular and respiratory diseases and the chemical composition of fine particle air pollution. Environ Health Perspect, 117(6), 957–963. https://doi.org/10.1289/ehp.0800185
Pun, V. C., Dowling, R., & Mehta, S. (2021). Ambient and household air pollution on early-life determinants of stunting-a systematic review and meta-analysis. Environmental Science and Pollution Research, 28(21), 26404–26412. https://doi.org/10.1007/s11356-021-13719-7
Schembari, A., de Hoogh, K., Pedersen, M., Dadvand, P., Martinez, D., Hoek, G., Petherick, E. S., Wright, J., & Nieuwenhuijsen, M. J. (2015). Ambient air pollution and newborn size and adiposity at birth: differences by maternal ethnicity (the Born in Bradford Study Cohort). Environmental Health Perspectives, 123(11), 1208–1215. https://doi.org/10.1289/ehp.1408675
Shaddick, G., Thomas, M. L., Mudu, P., Ruggeri, G., & Gumy, S. (2020). Half the world’s population are exposed to increasing air pollution. Npj Climate and Atmospheric Science, 3(1), 23. https://doi.org/10.1038/s41612-020-0124-2
Shou, Y. K., Huang, Y. L., Zhu, X. Z., Liu, C. Q., Hu, Y., & Wang, H. H. (2019). A review of the possible associations between ambient PM2.5 exposures and the development of Alzheimer’s disease. Ecotoxicology and Environmental Safety, 174, 344–352.
Slama, R., Darrow, L., Parker, J., Woodruff, T. J., Strickland, M., Nieuwenhuijsen, M., Glinianaia, S., Hoggatt, K. J., Kannan, S., Hurley, F., Kalinka, J., Sram, R., Brauer, M., Wilhelm, M., Heinrich, J., & Ritz, B. (2008). Meeting report: Atmospheric pollution and human reproduction. Environmental Health Perspectives, 116(6), 791–798. https://doi.org/10.1289/ehp.11074
Soares, M. J., Konno, T., & Alam, S. K. (2007). The prolactin family: Effectors of pregnancy-dependent adaptations. Trends in Endocrinology & Metabolism, 18(3), 114–121. https://doi.org/10.1016/j.tem.2007.02.005
Song, L., Jiang, S., Pan, K., Du, X., Zeng, X., Zhang, J., Zhou, J., Sun, Q., Xie, Y., & Zhao, J. (2020). AMPK activation ameliorates fine particulate matter-induced hepatic injury. Environmental Science and Pollution Research, 27(17), 21311–21319. https://doi.org/10.1007/s11356-020-08624-4
Stieb, D. M., Chen, L., Eshoul, M., & Judek, S. (2012). Ambient air pollution, birth weight and preterm birth: A systematic review and meta-analysis. Environmental Research, 117, 100–111. https://doi.org/10.1016/j.envres.2012.05.007
Suh, C. H., Cho, N. K., Lee, C. K., Lee, C. H., Kim, D. H., Kim, J. H., Son, B. C., & Lee, J. T. (2011). Perfluorooctanoic acid-induced inhibition of placental prolactin-family hormone and fetal growth retardation in mice. Molecular and Cellular Endocrinology, 337(1–2), 7–15. https://doi.org/10.1016/j.mce.2011.01.009
Sun, S., Zhang, Q., Sui, X. M., Ding, L., Liu, J., Yang, M., Zhao, Q. H., Zhang, C., Hao, J. H., Zhang, X. J., Lin, S. L., Ding, R., & Cao, J. Y. (2021). Associations between air pollution exposure and birth defects: a time series analysis. Environmental Geochemistry and Health, 43(11), 4379–4394. https://doi.org/10.1007/s10653-021-00886-2
Sun, X. L., Luo, X. P., Zhao, C. M., Ng, R. W. C., Lim, C. E. D., Zhang, B., & Liu, T. (2015). The association between fine particulate matter exposure during pregnancy and preterm birth: a meta-analysis. Bmc Pregnancy and Childbirth, 15, 300. https://doi.org/10.1186/s12884-015-0738-2
Suzuki, K. (2018). The developing world of DOHaD. Journal of Developmental Origins of Health and Disease, 9(3), 266–269. https://doi.org/10.1017/S2040174417000691
Tang, W., Li, Z., Huang, Y., Du, L., Wen, C., Sun, W., Yu, Z., Huang, S., & Chen, D. (2021). In utero exposure to fine particles decreases early birth weight of rat offspring and TLR4/NF-kappaB expression in lungs. Chemical Research in Toxicology, 34(1), 47–53. https://doi.org/10.1021/acs.chemrestox.0c00056
Tanwar, V., Gorr, M. W., Velten, M., Eichenseer, C. M., Long, V. P., 3rd., Bonilla, I. M., Shettigar, V., Ziolo, M. T., Davis, J. P., Baine, S. H., Carnes, C. A., & Wold, L. E. (2017). In utero particulate matter exposure produces heart failure, electrical remodeling, and epigenetic changes at adulthood. Journal of the American Heart Association. https://doi.org/10.1161/jaha.117.005796
Tsukue, N., Tsubone, H., & Suzuki, A. K. (2002). Diesel exhaust affects the abnormal delivery in pregnant mice and the growth of their young. Inhalation Toxicology, 14(6), 635–651. https://doi.org/10.1080/08958370290084548
Uwak, I., Olson, N., Fuentes, A., Moriarty, M., Pulczinski, J., Lam, J., Xu, X., Taylor, B. D., Taiwo, S., Koehler, K., Foster, M., Chiu, W. A., & Johnson, N. M. (2021). Application of the navigation guide systematic review methodology to evaluate prenatal exposure to particulate matter air pollution and infant birth weight. Environment International, 148, 106378. https://doi.org/10.1016/j.envint.2021.106378
Vinikoor-Imler, L. C., Davis, J. A., Meyer, R. E., Messer, L. C., & Luben, T. J. (2014). Associations between prenatal exposure to air pollution, small for gestational age, and term low birthweight in a state-wide birth cohort. Environmental Research, 132, 132–139. https://doi.org/10.1016/j.envres.2014.03.040
Wang, H., Peng, X., Cao, F., Wang, Y., Shi, H., Lin, S., Zhong, W., & Sun, J. (2017). Cardiotoxicity and mechanism of particulate matter 2.5 (PM2.5) exposure in offspring rats during pregnancy. Medical Science Monitor, 23, 3890–3896. https://doi.org/10.12659/msm.903006
Wang, J. N., Li, T. T., Lv, Y. B., Kraus, V. B., Zhang, Y., Mao, C., Yin, Z. X., Shi, W. Y., Zhou, J. H., Zheng, T. Z., Kinney, P. L., Ji, J., Tang, S., & Shi, X. M. (2020). Fine particulate matter and poor cognitive function among chinese older adults: Evidence from a community-based, 12-year prospective cohort study. Environmental Health Perspectives, 128(6), 067013.
Weldy, C. S., Liu, Y. G., Liggitt, H. D., & Chin, M. T. (2014). In utero exposure to diesel exhaust air pollution promotes adverse intrauterine conditions, resulting in weight gain, altered blood pressure, and increased susceptibility to heart failure in adult mice. PLoS One, 9(2), e88582. https://doi.org/10.1371/journal.pone.0088582
Wen, Y., Ding, X., Guan, Q., Hu, W., Wang, B., Hu, Q., Bigambo, F. M., Zhou, Z., Wang, X., & Xia, Y. (2021). Effects of exposure to urban particulate matter SRM 1648a during pregnancy on the neurobehavioral development of offspring mice. Ecotoxicology and Environmental Safety, 215, 112142. https://doi.org/10.1016/j.ecoenv.2021.112142
Wisborg, K., Henriksen, T. B., Hedegaard, M., & Secher, N. J. (1996). Smoking during pregnancy and preterm birth. British Journal of Obstetrics & Gynaecology, 103(8), 800–805. https://doi.org/10.1111/j.1471-0528.1996.tb09877.x
Wu, G., Brown, J., Zamora, M. L., Miller, A., Satterfield, M. C., Meininger, C. J., Steinhauser, C. B., Johnson, G. A., Burghardt, R. C., Bazer, F. W., Li, Y., Johnson, N. M., Molina, M. J., & Zhang, R. (2019). Adverse organogenesis and predisposed long-term metabolic syndrome from prenatal exposure to fine particulate matter. Proceedings of the National Academy of Sciences USA, 116(24), 11590–11595. https://doi.org/10.1073/pnas.1902925116
Wu, X. Q., Pan, B., Liu, L. J., Zhao, W. A., Zhu, J., Huang, X. P., & Tian, J. (2019). In utero exposure to PM2.5 during gestation caused adult cardiac hypertrophy through histone acetylation modification. Journal of Cellular Biochemistry, 120(3), 4375–4384. https://doi.org/10.1002/jcb.27723
Xing, Y. F., Xu, Y. H., Shi, M. H., & Lian, Y. X. (2016). The impact of PM2.5 on the human respiratory system. Journal of Thoracic Disease, 8(1), E69-74. https://doi.org/10.3978/j.issn.2072-1439.2016.01.19
Xu, X., & Zhang, C. (2020). Estimation of ground-level PM2.5 concentration using MODIS AOD and corrected regression model over Beijing, China. PLoS One, 15(10), e0240430. https://doi.org/10.1371/journal.pone.0240430
Yu, H., Feng, J., Su, X., Li, Y., & Sun, J. (2020). A seriously air pollution area affected by anthropogenic in the central China: Temporal-spatial distribution and potential sources. Environmental Geochemistry and Health, 42(10), 3199–3211. https://doi.org/10.1007/s10653-020-00558-7
Yuan, L., Zhang, Y., Gao, Y., & Tian, Y. (2019). Maternal fine particulate matter (PM2.5) exposure and adverse birth outcomes: An updated systematic review based on cohort studies. Environmental Science and Pollution Research, 26(14), 13963–13983. https://doi.org/10.1007/s11356-019-04644-x
Yuan, L., Zhang, Y., Wang, W., Chen, R., Liu, Y., Liu, C., Kan, H., Gao, Y., Tian, Y., & Shanghai Birth Cohort, S. (2020). Critical windows for maternal fine particulate matter exposure and adverse birth outcomes: The Shanghai birth cohort study. Chemosphere, 240, 124904. https://doi.org/10.1016/j.chemosphere.2019.124904
Zeng, X., Xu, X. J., Qin, Q. L., Ye, K., Wu, W. D., & Huo, X. (2019). Heavy metal exposure has adverse effects on the growth and development of preschool children. Environmental Geochemistry and Health, 41(1), 309–321. https://doi.org/10.1007/s10653-018-0114-z
Zhang, J., Liu, Y., Cui, L. L., Liu, S. Q., Yin, X. X., & Li, H. C. (2017). Ambient air pollution, smog episodes and mortality in Jinan, China. Scientific Reports, 7, 11209. https://doi.org/10.1038/s41598-017-11338-2
Zhang, M., Liu, W., Zhou, Y., Li, Y., Qin, Y., & Xu, Y. (2018). Neurodevelopmental toxicity induced by maternal PM2.5 exposure and protective effects of quercetin and Vitamin C. Chemosphere, 213, 182–196. https://doi.org/10.1016/j.chemosphere.2018.09.009
Funding
This study was supported by the National Natural Science Foundation of China [41991314] and Shanghai Municipal Health Commission [2020CXJQ01; GWV-10.1-XK07].
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by SL, BL, and YL. The first draft of the manuscript was written by SL and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethics approval
Animal care practices and all experiments were reviewed and approved by the Animal Committee of Fudan University School of Medicine, Shanghai, China (Date. April 12/No. 202204029Z).
Consent to participate
No personal data are contained in this study.
Consent to publish
The manuscript has been approved by all authors for publication. The work described was original research that has not been published previously, nor is it being considered for publication elsewhere, in whole or in part.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, S., Liu, B., Liu, Y. et al. Effects of maternal urban particulate matter SRM 1648a exposure on birth outcomes and offspring growth in mice. Environ Geochem Health 45, 2387–2400 (2023). https://doi.org/10.1007/s10653-022-01352-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10653-022-01352-3