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

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.

Figure 1

Maternal-perinatal black carbon load and residential black carbon exposure during pregnancy Association between mothers' black carbon exposure during the whole pregnancy and the amount of black carbon particles present in maternal and cord blood (A) and term placental tissue (B) from 60 mother-neonate pairs of the ENVIRONAGE birth cohort study. In panels A and B, datapoints correspond to the geometric mean black carbon load in each sample, the solid lines indicate the regression lines, and shaded areas show the 95% CIs. (C) Heatmap showing association between different biological samples and black carbon load, with two-sided Pearson correlation. The stronger the positive association, the darker the colour of the blue box and similar for the red colour indicating a negative association.

Figure 2

Fetal black carbon load Presence of intra-tissue black carbon particles in the fetal liver (A), lung (B), brain (C), and preterm placenta (D) samples, as indicated by zoomed in squares and arrows. (E) Plot of log₁₀-transformed number of detected black carbon particles in each sample (fetal liver n=36, lung n=36, brain n=14, and preterm placenta n=36), with datapoints corresponding to geometric mean black carbon load in each sample, with horizontal lines showing the geometric mean, and the whiskers showing the corresponding 95% CIs. (F) Heat map of association between black carbon load in different tissues, with corresponding two-sided Pearson correlation values. The stronger the positive association, the darker the colour of the blue box and similar for the red colour indicating a negative association.