Prenatal Exposure to PM2.5 Oxidative Potential and Lung Function in Infants and Preschool- Age Children: A Prospective Study

Abstract

Background: Fine particulate matter (${\mathrm{PM}}_{2.5}$) has been found to be detrimental to respiratory health of children, but few studies have examined the effects of prenatal ${\mathrm{PM}}_{2.5}$ oxidative potential (OP) on lung function in infants and preschool children.

Objectives: We estimated the associations of personal exposure to ${\mathrm{PM}}_{2.5}$ and OP during pregnancy on offspring objective lung function parameters and compared the strengths of associations between both exposure metrics.

Methods: We used data from 356 mother-child pairs from the SEPAGES cohort. PM filters collected twice during a week were analyzed for OP, using the dithiothreitol (DTT) and the ascorbic acid (AA) assays, quantifying the exposure of each pregnant woman. Lung function was assessed with tidal breathing analysis (TBFVL) and nitrogen multiple-breath washout ($N_2\text{MBW}$) test, performed at 6 wk, and airwave oscillometry (AOS) performed at 3 y. Associations of prenatal ${\mathrm{PM}}_{2.5}$ mass and OP with lung function parameters were estimated using multiple linear regressions.

Results: In neonates, an interquartile (IQR) increase in ${\text{OP}}_v^{\mathrm{DTT}}$ ($0.89{\text{nmol}/\text{min}/m}^3$) was associated with a decrease in functional residual capacity (FRC) measured by $N_2\text{MBW}$ [$\beta =-2.26\mathrm{mL}$; 95% confidence interval (CI): $-4.68$, 0.15]. Associations with ${\mathrm{PM}}_{2.5}$ showed similar patterns in comparison with ${\text{OP}}_v^{\mathrm{DTT}}$ but of smaller magnitude. Lung clearance index (LCI) and TBFVL parameters did not show any clear association with the exposures considered. At 3 y, increased frequency-dependent resistance of the lungs (${\text{Rrs}}_{7-19}$) from AOS tended to be associated with higher ${\text{OP}}_v^{\mathrm{DTT}}$ ($\beta =0.09\text{hPa}\times s/L$; 95% CI: $-0.06$, 0.24) and ${\text{OP}}_v^{\mathrm{AA}}$ ($\text{IQR}=1.14{\text{nmol}/\text{min}/m}^3$; $\beta =0.12\text{hPa}\times s/L$; 95% CI: $-0.04$, 0.27) but not with ${\mathrm{PM}}_{2.5}$ ($\text{IQR}=6.9{\mu g/m}^3$; $\beta =0.02\text{hPa}\times s/L$; 95% CI: $-0.13$, 0.16). Results for FRC and ${\text{Rrs}}_{7-19}$ remained similar in OP models adjusted on ${\mathrm{PM}}_{2.5}$.

Discussion: Prenatal exposure to ${\text{OP}}_v^{\mathrm{DTT}}$ was associated with several offspring lung function parameters over time, all related to lung volumes. https://doi.org/10.1289/EHP11155.

Figure 1.

Flow chart for the selection of the study population. Note: *${\mathrm{PM}}_{2.5}$ net weight $<4\mathrm{\mu }\mathrm{g}$. AOS, airwave oscillometry; LF, lung function; ${\mathrm{N}}_2\text{MBW}$, nitrogen multiple-breath washout; OP, oxidative potential; PM, particulate matter; ${\mathrm{PM}}_{2.5}$, PM with aerodynamic diameter $<2.5\mathrm{\mu }\mathrm{m}$; TBFVL, tidal breathing flow-volume loops.

Figure 2.

Monthly distribution of personal measurements of ${\mathrm{PM}}_{2.5}$ (left), ${\text{OP}}_{\mathrm{v}}^{\mathrm{DTT}}$ (center), and ${\text{OP}}_{\mathrm{v}}^{\mathrm{AA}}$ (right). See Table S2 for corresponding numeric data. Note: Boxes represent 25th–75th percentiles; the middle horizontal line represents the median; whiskers extend to the most extreme point within 1.5 IQRs of the box and the dots outside boxes indicate outliers. Note: AA, ascorbic acid; DTT, dithiothreitol; IQR, interquartile range; ${\text{OP}}_{\mathrm{v}}^{\mathrm{AA}}$, volume-normalized oxidative potential measured by the AA assay (nmol${/\text{min}/\mathrm{m}}^3$); ${\text{OP}}_{\mathrm{v}}^{\mathrm{DTT}}$, volume-normalized oxidative potential measured by the DTT assay (nmol${/\text{min}/\mathrm{m}}^3$); PM, particulate matter; ${\mathrm{PM}}_{2.5}$, PM with an aerodynamic diameter $<2.5\mathrm{\mu }\mathrm{m}$ ($\mathrm{\mu }\mathrm{g}{/\mathrm{m}}^3$).

Figure 3.

Association between personal exposure to ${\mathrm{PM}}_{2.5}$, ${\text{OP}}_{\mathrm{v}}^{\mathrm{DTT}}$, and ${\text{OP}}_{\mathrm{v}}^{\mathrm{AA}}$ during pregnancy and lung function parameters measured at 6 wk in the univariate and multiple linear models and in the sensitivity analyses. Outcomes and exposures were scaled by their IQR. See Tables S4 and S6 for corresponding numeric data. Whiskers represent the 95% confidence interval around the estimate. The main model was adjusted on child’s height, weight, sex, age, season of sampling, breastfeeding, environmental tobacco smoke, maternal age and BMI before pregnancy, parental level of education, parental history of rhinitis, and mean temperature during pregnancy. In addition, “2 sampling periods” are the analyses reduced to the children that had 2 wk of prenatal measurements of air pollution (63%–66% of the population); “Excluding extreme values” are the analyses excluding the exposures and outcomes below the first percentile and above the 99th (exclusion of approximately 5% of the population); “Adjusted on PM” corresponds to adding personal exposure to ${\mathrm{PM}}_{2.5}$ in the set of confounders, “Adjusted on ${\mathrm{NO}}_2$” corresponds to adding personal exposure to ${\mathrm{NO}}_2$ in the set of confounders, and the last analyses were performed excluding children that had the highest hypoventilation degree during the nitrogen multiple breath washout test (excluding 25% of the population). Note: AA, ascorbic acid; BMI, body mass index; DTT, dithiothreitol; FRC, functional residual capacity; IQR, interquartile range; LCI, lung clearance index; ${\text{OP}}_{\mathrm{v}}^{\mathrm{AA}}$, volume-normalized oxidative potential measured by the AA assay (${\text{nmol}/\text{min}/\mathrm{m}}^3$); ${\text{OP}}_{\mathrm{v}}^{\mathrm{DTT}}$, volume-normalized oxidative potential measured by the DTT assay (nmol${/\text{min}/\mathrm{m}}^3$); PM, particulate matter; ${\mathrm{PM}}_{2.5}$, PM with an aerodynamic diameter $<2.5\mathrm{\mu }\mathrm{m}$ (${\mathrm{\mu }\mathrm{g}/\mathrm{m}}^3$); ${\mathrm{t}}_{\text{PTEF}}{/\mathrm{t}}_{\mathrm{E}}$, ratio of time to peak tidal expiratory flow to expiratory time; ${\mathrm{V}}_{\mathrm{T}}$, tidal volume.

Figure 4.

Association between personal exposure to ${\mathrm{PM}}_{2.5}$, ${\text{OP}}_{\mathrm{v}}^{\mathrm{DTT}}$, and ${\text{OP}}_{\mathrm{v}}^{\mathrm{AA}}$ during pregnancy and lung function parameters measured at 3 y in the univariate and multiple linear models and in the sensitivity analyses. Outcomes and exposures were scaled by their IQR. See Tables S5 and S7 for corresponding numeric data. Whiskers represent the 95% confidence interval around the estimate. The main model was adjusted on child’s height, weight, sex, age, season of sampling, breastfeeding, environmental tobacco smoke, maternal age and BMI before pregnancy, parental level of education, parental history of rhinitis and mean temperature during pregnancy. In addition, “2 sampling periods” are the analyses reduced to the children that had 2 wk of prenatal measurements of air pollution (61% of the population); “Excluding extreme values” are the analyses excluding the exposures and outcomes below the first percentile and above the 99th (exclusion of approx. 5% of the population); “Adjusted on PM” corresponds to adding personal exposure to ${\mathrm{PM}}_{2.5}$ in the set of confounders; “Adjusted on ${\mathrm{NO}}_2$” corresponds to adding personal exposure to ${\mathrm{NO}}_2$ in the set of confounders. Note: AA, ascorbic acid; AX, area under the reactance curve; BMI, body mass index; DTT, dithiothreitol; IQR, interquartile range; ${\text{OP}}_{\mathrm{v}}^{\mathrm{AA}}$, volume-normalized oxidative potential measured by the AA assay (nmol${/\text{min}/\mathrm{m}}^3$); ${\text{OP}}_{\mathrm{v}}^{\mathrm{DTT}}$, volume-normalized oxidative potential measured by the DTT assay (nmol${/\text{min}/\mathrm{m}}^3$); PM, particulate matter; ${\mathrm{PM}}_{2.5}$, PM with an aerodynamic diameter $<2.5\mathrm{\mu }\mathrm{m}$ (${\mathrm{\mu }\mathrm{g}/\mathrm{m}}^3$); ${\text{Rrs}}_7$, resistance at a frequency of 7 Hz; ${\text{Rrs}}_{7–19}$, difference between the resistance at 7 Hz and at 19 Hz; ${\text{Xrs}}_7$, reactance at a frequency of 7 Hz.