Traffic-related air pollution is associated with glucose dysregulation, blood pressure, and oxidative stress in children

doi:10.1016/j.envres.2021.110870

Environmental Research

Volume 195, April 2021, 110870

https://doi.org/10.1016/j.envres.2021.110870 Get rights and content

Highlights

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Traffic-related air pollution was associated with metabolic outcomes in children.
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Children were ages 6–8 and predominantly low-income and of color (Latinx or Black).
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Air pollutants included polycyclic aromatic hydrocarbons and elemental carbon.
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Outcomes included HbA1c, systolic blood pressure, and oxidative stress.

Abstract

Background

Metabolic syndrome increases the risk of cardiovascular disease in adults. Antecedents likely begin in childhood and whether childhood exposure to air pollution plays a contributory role is not well understood.

Objectives

To assess whether children's exposure to air pollution is associated with markers of risk for metabolic syndrome and oxidative stress, a hypothesized mediator of air pollution-related health effects.

Methods

We studied 299 children (ages 6–8) living in the Fresno, CA area. At a study center visit, questionnaire and biomarker data were collected. Outcomes included hemoglobin A1c (HbA1c), urinary 8-isoprostane, systolic blood pressure (SBP), and BMI. Individual-level exposure estimates for a set of four pollutants that are constituents of traffic-related air pollution (TRAP) – the sum of 4-, 5-, and 6-ring polycyclic aromatic hydrocarbon compounds (PAH456), NO₂, elemental carbon, and fine particulate matter (PM_2.5) – were modeled at the primary residential location for 1-day lag, and 1-week, 1-month, 3-month, 6-month, and 1-year averages prior to each participant's visit date. Generalized additive models were used to estimate associations between each air pollutant exposure and outcome.

Results

The study population was 53% male, 80% Latinx, 11% Black and largely low-income (6% were White and 3% were Asian/Pacific Islander). HbA1c percentage was associated with longer-term increases in TRAP; for example a 4.42 ng/m³ increase in 6-month average PAH456 was associated with a 0.07% increase (95% CI: 0.01, 0.14) and a 3.62 μg/m³ increase in 6-month average PM_2.5 was associated with a 0.06% increase (95% CI: 0.01, 0.10). The influence of air pollutants on blood pressure was strongest at 3 months; for example, a 6.2 ppb increase in 3-month average NO₂ was associated with a 9.4 mmHg increase in SBP (95% CI: 2.8, 15.9). TRAP concentrations were not significantly associated with anthropometric or adipokine measures. Short-term TRAP exposure averages were significantly associated with creatinine-adjusted urinary 8-isoprostane.

Discussion

Our results suggest that both short- and longer-term estimated individual-level outdoor residential exposures to several traffic-related air pollutants, including ambient PAHs, are associated with biomarkers of risk for metabolic syndrome and oxidative stress in children.

Introduction

Metabolic syndrome is a cluster of conditions that increases the risk of cardiovascular disease, type 2 diabetes mellitus, and all-cause mortality. Insulin resistance, abdominal obesity, dyslipidemia, and hypertension are several of the known risk factors that contribute to the syndrome (Huang 2009). Metabolic syndrome is now recognized as a worldwide public health problem (Alberti et al., 2009) leading to calls for research on potentially modifiable risk factors, including air pollution (Hutcheson and Rocic 2012). Evidence has been accumulating that risk factors likely associated with adult metabolic syndrome are also impacted in children through exposure to air pollutants. Such risk factors include diabetes, obesity and systolic blood pressure (Faienza et al., 2016; Lim and Thurston 2019). If modifiable environmental risk factors for metabolic syndrome can be identified, especially in high-risk populations, then strategies at the community and individual level – known and yet to be developed – to reduce childhood exposures to these factors should be prioritized for implementation. Here we present an examination of air pollution among children as one such modifiable environmental risk factor for several indices of metabolic syndrome.

The Children's Health and Air Pollution Study (CHAPS) in the San Joaquin Valley (SJV) of California is a research project investigating the adverse health effects of early childhood exposure to air pollution. The SJV has some of the worst air pollution in the U.S., a large Hispanic/Latinx population, and a high rate of poverty. Compared with other ethnic groups, Latinx children and adolescents in the United States are disproportionately affected by obesity (Ogden et al., 2012). Babey et al. showed that a high proportion of Latinx adults living in the San Joaquin Valley have pre-diabetes or type 2 diabetes (Babey et al., 2016).

We have collected extensive air pollution exposure data for many years in Fresno and more recently in Bakersfield, the two most populous cities in the SJV, including ambient polycyclic aromatic hydrocarbon (PAH) concentrations (Noth et al. 2011, 2016, 2020). The spatial variability in ambient PAHs in Fresno is primarily due to traffic and rail lines. PAHs are putative endocrine disruptors, which have been associated with obesity and metabolic dysregulation, and thus are of particular interest (Zhang et al., 2016).

Capitalizing on our extensive air pollution exposure data, we conducted a study of the potential effects of PAHs and other traffic-related air pollutants on anthropometric measures and biomarkers of metabolic dysfunction in young children enrolled in CHAPS. Our overall paradigm was that oxidative stress induced by exposure to traffic-related air pollution, especially ambient PAHs, leads to systemic inflammation that contributes to abnormal fat and glucose metabolism and thereby increases risk of obesity and diabetes. The measures and biomarkers we examined were anthropometry to assess childhood obesity (BMI-percentile, percent body fat and waist-to-height ratio), glycosolated hemoglobin (HbA1c) as a measure of glucose dysregulation, adipokines involved with both glucose and fat metabolism (leptin and adiponectin), 8-isoprostane as a measure of oxidative stress, and blood pressure. This set of measurements provides an approach to the assessment of metabolic syndrome risk in children. Here we report the results of a cross-sectional analysis of the associations between residential concentrations of traffic-related air pollutants and markers of metabolic dysfunction among the CHAPS children (ages 6–8 years).

Section snippets

Study population and recruitment

We partnered with the Fresno Unified School District (FUSD) to recruit children ages 6–8 years who were enrolled in FUSD in 2015–2017. In 2017, FUSD had a student population of 70,725, with 88.9% of children classified as socioeconomically disadvantaged (California Department of Education 2017). Recruiting through the public elementary school system allowed us to recruit a group of predominantly low-income children, distributed spatially across Fresno.

Since FUSD schools operate primarily as

Descriptive statistics

The study population consisted of 299 children. The sociodemographic characteristics of the participating children are shown in Table 1. The potential participants were screened at ages 6–8 and seen for their baseline visit at ages 6–9. The population was 53% male, 80% Hispanic/Latinx, and 11% Black. The remaining participants were Non-Hispanic White (6.0%) and Asian/Pacific Islander (3.0%). Nearly 80% of the study population lived in rented homes and nearly 30% was from a family with <$15,000

Discussion

In a well-characterized cohort of young children, we found that estimated average ambient residential exposure to several traffic-related air pollutants was associated with a marker of potential risk for metabolic syndrome (HbA1c), as well as oxidative stress (urinary 8-isoprostane), a hypothesized mediator of air pollution-related health effects. The associations with HbA1c were seen for 3- and 6-month average pollutant exposures, as expected based on the known half-life of HbA1c, while those

Credit author statement

JKM and LL co-equally led the data collection, data management and data analysis and made major contributions to the interpretation of the data and writing of the manuscript; SMH assisted with data analysis, data interpretation and manuscript revision; HGM, AMN, EAE and SC assisted with data analysis and interpretation; TT, MP, and KN assisted with data collection; NH and GT performed the biomarker assays; EMN, FL, and SKH conducted the air pollution exposure assessment; JRB conceived the

Funding

This research was supported by the Children's Health and Air Pollution Study (CHAPS), an NIH / EPA-funded Children's Environmental Health Research Center (EPA: RD83543501, NIH: ES022849) and an additional grant (NIH: F31ES0277510). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Gwen Tindula received a Student/New Investigator Travel Award of $750.00 to attend and present at the 2019

Declaration of competing interest

The authors report no conflicts of interest.

Acknowledgements

The authors would like to thank the UCSF Fresno research team (Griselda Aguilar, Christian Bonilla, Karina Corona, Cynthia Cortez, Alexa Lopez, Carolina Orozco and Janna Blaauw) for their hard work in conducting the clinical visits, Brian Nguyen and Kelly Nabaglo for their assistance with blood and urine analyses in the Holland laboratory, Barune Thapa and Beth MacDonald for general assistance with study management, and all of the participating children and families for their patience and

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Four electronic databases were searched for related epidemiological studies published up to September 13, 2022. Stata 14.0 was applied to examine the heterogeneity among the studies and evaluate the combined effect sizes per 10 μg/m³ increase of PM by selecting the corresponding models. Besides, subgroup analysis, sensitivity analysis, and publication bias test were also conducted.
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Both prenatal and postnatal exposure to PM can increase BP, contributing to a higher prevalence of hypertension in children and adolescents.
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PM_2.5 exposure during the prenatal period and the first 3-years of life was associated with lower FVC and FEV₁ assessed at ages 6–9. Specifically, an increase from the 5th percentile of the observed monthly average exposure (7.55 μg/m³) to the median observed exposure (12.69 μg/m³) for the duration of the window was associated with 0.42 L lower FVC (95% confidence interval (CI): −0.82, −0.03) and 0.38 L lower FEV₁ (95% CI: −0.75, −0.02). The shape of the lag-response indicated that the second half of pregnancy may be a particularly influential window of exposure. Associations for ozone were not as strong and typically CIs included the null.
Our findings indicate that prenatal and early-life exposures to PM_2.5 are associated with decreased lung function later in childhood. Exposures during the latter months of pregnancy may be especially influential.
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Metabolic syndrome (MetS) is considered a main public health issue as it remarkably adds the risk of cardiovascular disease, leading to a heavy burden of disease. There is growing evidence linking fine particulate matter (PM_2.5) exposure to MetS. However, the influences of PM_2.5 constituents, especially in children and adolescents, remain unclear. Our study was according to a national analysis among Chinese children and adolescents to examine the associations between long-term exposure to PM_2.5 main constituents and MetS. A total of 10,066 children and adolescents aged 10–18 years were recruited in 7 provinces in China, with blood tests, health exams, and questionnaire surveys. We estimated long-term exposures to PM_2.5 mass and its five constituents, containing black carbon (BC), organic matter (OM), inorganic nitrate (NO₃⁻), sulfate (SO₄²⁻), and soil particles (SOIL) from multi-source data fusion models. Mixed-effects logistic regression models were used with the adjustment of a variety of covariates. In the surveyed populations, 2.9% were classified as MetS. From the single-pollutant models, we discovered that long-term exposures to PM_2.5 mass, BC, OM, NO₃⁻, as well as SO₄²⁻, were significantly associated with the prevalence of MetS, with odds ratios (ORs) per 1 μg/m³ that were 1.02 (95% confidence interval (CI): 1.01, 1.03) for PM_2.5 mass, 1.24 (95% CI: 1.14, 1.35) for BC, 1.07 (95% CI: 1.04, 1.11) for OM, 1.09 (95% CI: 1.04, 1.13) for NO₃⁻, and 1.14 (95% CI:1.04, 1.24) for SO₄²⁻. The influence of BC on the prevalence of MetS was robust in both the multi-pollutant model and the PM_2.5-constituent joint model. The paper indicates long-term exposure to PM_2.5 mass and specific PM_2.5 constituents, particularly for BC, was significantly associated with a higher MetS prevalence among children and adolescents in China. Our results highlight the significance of establishing further regulations on PM_2.5 constituents.
Association of urinary and ambient black carbon, and other ambient air pollutants with risk of prediabetes and metabolic syndrome in children and adolescents
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Citation Excerpt :
We further dichotomized the outcome variables (prediabetes and MetS) and performed multiple logistic regressions to cross-sectionally analyze its association with urinary or ambient BC, PM2.5 and NO2 as a single pollutant or residential distance or proximity to major roads, separately at T3. In previous studies differences in association were reported w.r.t sex, obesity (normal weight vs. overweight/obese) or residential distance to major road (≤250 m vs. >250 m) (Clementi et al., 2019; Mann et al., 2021; Zhang et al., 2021a). We therefore performed stratified analysis on these variables to investigate for possible effect modification.
The effects of exposure to black carbon (BC) on various diseases remains unclear, one reason being potential exposure misclassification following modelling of ambient air pollution levels. Urinary BC particles may be a more precise measure to analyze the health effects of BC. We aimed to assess the risk of prediabetes and metabolic syndrome (MetS) in relation to urinary BC particles and ambient BC and to compare their associations in 5453 children from IDEFICS/I. Family cohort. We determined the amount of BC particles in urine using label-free white-light generation under femtosecond pulsed laser illumination. We assessed annual exposure to ambient air pollutants (BC, PM_2.5 and NO₂) at the place of residence using land use regression models for Europe, and we calculated the residential distance to major roads (≤250 m vs. more). We analyzed the cross-sectional relationships between urinary BC and air pollutants (BC, PM_2.5 and NO₂) and distance to roads, and the associations of all these variables to the risk of prediabetes and MetS, using logistic and linear regression models. Though we did not observe associations between urinary and ambient BC in overall analysis, we observed a positive association between urinary and ambient BC levels in boys and in children living ≤250 m to a major road compared to those living >250 m away from a major road. We observed a positive association between log-transformed urinary BC particles and MetS (OR_{per unit increase} = 1.72, 95% CI = 1.21; 2.45). An association between ambient BC and MetS was only observed in children living closer to a major road. Our findings suggest that exposure to BC (ambient and biomarker) may contribute to the risk of MetS in children. By measuring the internal dose, the BC particles in urine may have additionally captured non-residential sources and reduced exposure misclassification. Larger studies, with longitudinal design including measurement of urinary BC at multiple time-points are warranted to confirm our findings.
Association of long-term air pollution exposure with the risk of prediabetes and diabetes: Systematic perspective from inflammatory mechanisms, glucose homeostasis pathway to preventive strategies
2023, Environmental Research
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Limited evidence suggests the association of air pollutants with a series of diabetic cascades including inflammatory pathways, glucose homeostasis disorder, and prediabetes and diabetes. Subclinical strategies for preventing such pollutants-induced effects remain unknown.
We conducted a cross-sectional study in two typically air-polluted Chinese cities in 2018–2020. One-year average PM₁, PM_2.5, PM₁₀, SO₂, NO₂, and O₃ were calculated according to participants' residence. GAM multinomial logistic regression was performed to investigate the association of air pollutants with diabetes status. GAM and quantile g-computation were respectively performed to investigate individual and joint effects of air pollutants on glucose homeostasis markers (glucose, insulin, HbA1c, HOMA-IR, HOMA-B and HOMA-S). Complement C3 and hsCRP were analyzed as potential mediators. The ABCS criteria and hemoglobin glycation index (HGI) were examined for their potential in preventive strategy.
Long-term air pollutants exposure was associated with the risk of prediabetes [Prevalence ratio for O₃ (PR_O₃) = 1.96 (95% CI: 1.24, 3.03)] and diabetes [PR_PM₁ = 1.18 (95% CI: 1.05, 1.32); PR_PM_2.5 = 1.08 (95% CI: 1.00, 1.16); PR_O₃ = 1.35 (95% CI: 1.03, 1.74)]. PM₁, PM₁₀, SO₂ or O₃ exposure was associated with glucose-homeostasis disorder. For example, O₃ exposure was associated with increased levels of glucose [7.67% (95% CI: 1.75, 13.92)], insulin [19.98% (95% CI: 4.53, 37.72)], HOMA-IR [34.88% (95% CI: 13.81, 59.84)], and decreased levels of HOMA-S [-25.88% (95% CI: −37.46, −12.16)]. Complement C3 and hsCRP played mediating roles in these relationships with proportion mediated ranging from 6.95% to 60.64%. Participants with HGI ≤ −0.53 were protected from the adverse effects of air pollutants.
Our study provides comprehensive insights into air pollutant–associated diabetic cascade and suggests subclinical preventive strategies.

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Traffic-related air pollution is associated with glucose dysregulation, blood pressure, and oxidative stress in children

Highlights

Abstract

Background

Objectives

Methods

Results

Discussion

Introduction

Section snippets

Study population and recruitment

Descriptive statistics

Discussion

Credit author statement

Funding

Declaration of competing interest

Acknowledgements

Circulation

Longitudinal associations between ambient air pollution with insulin sensitivity, β-cell function, and adiposity in Los Angeles Latino children

Diabetes

Diagnosis and classification of diabetes mellitus

Diabetes Care

Impact of ambient air pollution on obesity: a systematic review

Int. J. Obes.

Prediabetes in California: nearly half of California adults on path to diabetes

Policy Brief UCLA Cent Health Policy Res Mar;(PB2016-1)

Insights into the mechanisms and mediators of the effects of air pollution exposure on blood pressure and vascular function in healthy humans

Hypertension

California School Dashboard District Performance Overview: Fresno Unified

National Health and Nutrition Examination Survey Anthropometry Procedures Manual

National Health and Nutrition Examination Survey Physician Physical Examination Procedures Manual

A SAS Program for the 2000 CDC Growth Charts (Ages 0 to <20 Years)

Effects of chronic and acute ozone exposure on lipid peroxidation and antioxidant capacity in healthy young adults

Environ. Health Perspect.

Secondhand smoke exposure is associated with increased carotid artery intima-media thickness: the Bogalusa Heart Study

Atherosclerosis

Tracking of blood pressure from childhood to adulthood: a systematic review and meta-regression analysis

Circulation

Prenatal particulate air pollution exposure and body composition in urban preschool children: examining sensitive windows and sex-specific associations

Environ. Res.

Reference values for leptin and adiponectin in children below the age of 10 based on the IDEFICS cohort

Int. J. Obes.

Association between ambient air pollution and diabetes mellitus in Europe and North America: systematic review and meta-analysis

Environ. Health Perspect.

The dangerous link between childhood and adulthood predictors of obesity and metabolic syndrome

Intern Emerg Med

Exposure to parental smoking in childhood or adolescence is associated with increased carotid intima-media thickness in young adults: evidence from the Cardiovascular Risk in Young Finns study and the Childhood Determinants of Adult Health Study

Eur. Heart J.

Estimating body composition of young children by using bioelectrical resistance

J Appl Physiol (1985

A comprehensive definition for metabolic syndrome

Dis Model Mech

The metabolic syndrome, oxidative stress, environment, and cardiovascular disease: the great exploration

Exp Diabetes Res 2012

Utility of different blood pressure measurement components in childhood to predict adult carotid intima-media thickness

Hypertension

Sex-specific difference of the association between ambient air pollution and the prevalence of obesity in Chinese adults from a high pollution range area: 33 Communities Chinese Health Study

Atmos. Environ.

Associations between long-term exposure to air pollution and blood pressure and effect modifications by behavioral factors

Environ. Res.

Residential proximity to major roadways, fine particulate matter, and adiposity: the Framingham heart study

Obesity

Short-term exposure to air pollution and biomarkers of oxidative stress: the Framingham Heart Study

J Am Heart Assoc

Ambient air pollution, adipokines, and glucose homeostasis: the Framingham Heart Study

Environ. Int.

Air pollution, oxidative stress, and diabetes: a life course epidemiologic perspective

Curr. Diabetes Rep.

Performance of eleven simplified methods for the identification of elevated blood pressure in children and adolescents

Hypertension

Altered pulmonary function in children with asthma associated with highway traffic near residence

Int. J. Environ. Health Res.