Maternal exposure to ambient black carbon particles and their presence in maternal and fetal circulation and organs: an analysis of two independent population-based observational studies

Eva Bongaerts, Laetitia L Lecante, Hannelore Bové, Maarten B J Roeffaers, Marcel Ameloot, Paul A Fowler, Tim S Nawrot* (Corresponding Author)

*Corresponding author for this work

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Abstract

BACKGROUND: Maternal exposure to particulate air pollution during pregnancy has been linked to multiple adverse birth outcomes causing burden of disease later in the child's life. To date, there is a paucity of data on whether or not ambient particles can both reach and cross the human placenta to exert direct effects on fetal organ systems during gestation.

METHODS: In this analysis, we used maternal-perinatal and fetal samples collected within the framework of two independent studies: the ENVIRONAGE (Environmental Influences on Ageing in Early Life) birth cohort of mothers giving birth at the East-Limburg Hospital in Genk, Belgium, and the SAFeR (Scottish Advanced Fetal Research) cohort of terminated, normally progressing pregnancies among women aged 16 years and older in Aberdeen and the Grampian region, UK. From the ENVIRONAGE study, we included 60 randomly selected mother-neonate pairs, excluding all mothers who reported that they ever smoked. From the SAFeR study, we included 36 fetuses of gestational age 7-20 weeks with cotinine concentrations indicative of non-smoking status. We used white light generation under femtosecond pulsed illumination to detect black carbon particles in samples collected at the maternal-fetal interface. We did appropriate validation experiments of all samples to confirm the carbonaceous nature of the identified particles.

FINDINGS: We found evidence of the presence of black carbon particles in cord blood, confirming the ability of these particles to cross the placenta and enter the fetal circulation system. We also found a strong correlation (r ≥0·50; p<0·0001) between the maternal-perinatal particle load (in maternal blood [n=60], term placenta [n=60], and cord blood [n=60]) and residential ambient black carbon exposure during pregnancy. Additionally, we found the presence of black carbon particles in first and second trimester tissues (fetal liver [n=36], lung [n=36], and brain [n=14]) of electively terminated and normally progressing pregnancies from an independent study.

INTERPRETATION: We found that maternally inhaled carbonaceous air pollution particles can cross the placenta and then translocate into human fetal organs during gestation. These findings are especially concerning because this window of exposure is key to organ development. Further studies are needed to elucidate the mechanisms of particle translocation.

FUNDING: European Research Council, Flemish Scientific Research Foundation, Kom op Tegen Kanker, UK Medical Research Council, and EU Horizon 2020.

Original languageEnglish
Pages (from-to)e804-e811
Number of pages8
JournalThe lancet. Planetary health
Volume6
Issue number10
Early online date5 Oct 2022
DOIs
Publication statusPublished - 5 Oct 2022

Bibliographical note

Funding
European Research Council, Flemish Scientific Research Foundation, Kom op Tegen Kanker, UK Medical Research Council, and EU Horizon 2020.

Acknowledgments
The ENVIRONAGE birth cohort was initiated by the European Research Council (ERC-2012-StG 310898) and received additional funding from the Flemish Scientific Research Foundation and Kom op Tegen Kanker (KoTK). The detection equipment was funded by the METHUSALEM Program and the INCALO project (ERC-PoC). We acknowledge the Flemish Scientific Research Foundation (FWO; 1150920N to EB and G082317N). The SAFeR study was funded by the UK Medical Research Council (MR/L010011/1 and MR/P011535/1) and the EU's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie project PROTECTED (grant agreement number 722634) and FREIA project (grant agreement number 825100) as well as by NHS Grampian Endowments grants (16/11/056, 17/034, 18/14, 19/029, and 20/031) to PAF. We thank the midwives from the maternity ward of the East-Limburg Hospital in Genk, Belgium, for coordinating and supporting the study at the ward. We thank the Advanced Optical Microscopy Centre for the maintenance of the microscopic instruments. Moreover, we thank our colleagues from the Centre for Environmental Sciences for their hard work in collecting and processing the samples for the ENVIRONAGE birth cohort. Additionally, we thank the NHS Grampian Research Nurses and NHS Grampian R&D for their tireless recruitment work for the SAFeR study. We thank the past and present SAFeR team for their hard work with the fetuses and placentae. Finally, we thank the NHS Grampian Biorepository for their oversight role in SAFeR and assistance in processing and preparation of tissue sections.

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