Elsevier

Environmental Research

Volume 180, January 2020, 108841
Environmental Research

Short-term exposures to particulate matter gamma radiation activities and biomarkers of systemic inflammation and endothelial activation in COPD patients

https://doi.org/10.1016/j.envres.2019.108841Get rights and content

Highlights

  • A novel study about systemic effects of PM radioactivity in COPD patients.

  • We assessed PM gamma activities indoor, where patients spend most their time.

  • We found positive associations between PM gamma activities with CRP and IL-6.

  • Our results indicated toxicity of current ambient radiation associated with PM.

Abstract

Background

We hypothesized that particulate matter (PM) gamma activity (gamma radiation associated with PM) is associated with systemic effects.

Objective

Examine short-term relationships between ambient and indoor exposures to PM gamma activities with systemic inflammation and endothelial activation in chronic obstructive pulmonary disease (COPD) patients.

Methods

In 85 COPD patients from Eastern Massachusetts, USA from 2012 to 2014, plasma C-reactive protein (CRP), interleukin-6 (IL-6), and soluble vascular cell adhesion molecule-1 (sVCAM-1) were measured seasonally up to four times. We used US EPA RadNet data measuring ambient gamma radiation attached to PM adjusted for background radiation, and estimated in-home gamma radiation exposures using the ratio of in-home-to-ambient sulfur in PM2.5. Linear mixed-effects regression models were used to determine associations between moving averages of PM gamma activities through the week before phlebotomy with these biomarkers. We explored ambient and indoor PM2.5, black carbon (BC), and NO2 as confounders.

Results

Ambient and indoor PM gamma activities measured as energy spectra classes 3 through 9 were positively associated with CRP and IL-6. For example, averaged from phlebotomy day through previous 6 days, each IQR increase in indoor PM gamma activity for each spectra class, was associated with an CRP increase ranging from 7.45% (95%CI: 2.77, 12.4) to 13.4% (95%CI: 5.82, 21.4) and for ambient exposures were associated with an increase of 8.75% (95%CI: −0.57, 18.95) to 14.8% (95%CI: 4.5, 26.0). Indoor exposures were associated with IL-6 increase of 3.56% (95%CI: 0.31, 6.91) to 6.46% (95%CI:1.33, 11.85) and ambient exposures were associated with an increase of 0.03% (95%CI: −6.37, 6.87) to 3.50% (95%CI: −3.15, 10.61). There were no positive associations with sVCAM-1. Sensitivity analyses using two-pollutant models showed similar effects.

Conclusions

Our results demonstrate that short-term exposures to environmental PM gamma radiation activities were associated with systemic inflammation in COPD patients.

Introduction

Chronic obstructive pulmonary disease (COPD) is a progressive and debilitating chronic disease that affects more than 15.7 million people in the United States and was the fourth leading cause of death in the United States in 2016 (Croft et al., 2018; Wheaton et al., 2015). Biomarkers of systemic inflammation are elevated in COPD patients and associated with more severe disease and increased mortality (Agusti, 2005; Agusti et al., 2003, 2012; Mackay et al., 2016; Shaw et al., 2014; Su et al., 2016). Exposure to air pollution has be linked to increased levels of systemic inflammation (Jiang et al., 2016), especially in COPD patients who may also be more vulnerable to the detrimental effects of air pollutants (Garshick, 2014; Garshick et al., 2018; Heinrich and Schikowski, 2018).

In addition to air pollution, humans are exposed to ionizing radiation, including alpha, beta, and gamma radiation from the decay of radionuclides (EPA, 1972). Ionizing radiation can disrupt chemical bonds in the structural components of cells, damage molecules, and induce DNA strand breaks (Henner et al., 1982; Foray et al., 1999; Mishra, 2004). The largest sources of ionizing radiation are natural terrestrial and extra-terrestrial radiation sources (e.g., the decay of progenies of uranium-238, thorium-232 and potassium-40 in earth's crust and products of galactic cosmic rays) (EPA, 1972; Shahbazi-Gahrouei et al., 2013).

Inhalation of particulate matter (PM) radioactivity is an important route of ionizing radiation exposure (Karam, 2004). Alpha radiation, which is more damaging compared to other types of ionizing radiation (beta and gamma radiation), cannot penetrate the epidermis. Therefore, exposure to alpha radiation may occur through internal exposure (inhalation or ingestion). Environmental radioactive nuclei from background sources (natural terrestrial and extra-terrestrial) can attach to respirable PM (Mohamed et al., 2014; Porstendörfer, 1994, 2001). Once inhaled, PM with attached radioactive nuclei deposit on the respiratory tract and can translocate into systemic circulation (Marsh and Bailey, 2013). As the emission of alpha or beta radiation is frequently accompanied by the emission of gamma activities, PM gamma activities can be considered as surrogates of total radioactivity including alpha and beta activities (Stacey, 2007). We previously reported associations between increases in PM gamma activities and a reduction in forced expiratory volume in 1 s (FEV1) and forced vital capacity (FVC) (Vieira et al., 2019). However, up to our best knowledge, there is no study about the effects of PM gamma activities on systemic inflammation or vascular endothelial activation biomarkers, which may contribute to the development of both pulmonary and systemic endothelial dysfunction, in COPD patients (Polverino et al., 2018).

The objective of this research is to investigate the systemic effects of PM radioactivity in COPD patients. We explored relationships between ambient PM gamma activities (surrogates of ambient PM radioactivity) and the indoor infiltration of ambient PM radioactivity on plasma biomarkers of systemic inflammation (IL-6 and CRP) and vascular endothelial activation (sVCAM-1) in COPD patients from Eastern Massachusetts, USA.

Section snippets

Population

This study is part of the COPD and Air Pollution Study (CAPS), where we previously reported exposure-response relationships between indoor black carbon (BC) and biomarkers of systemic inflammation (Garshick et al., 2018). We recruited 85 COPD patients from Eastern Massachusetts between October 2012 and December 2014 as previously described (Garshick et al., 2018). Eligibility was confirmed at an in-person visit that included pre- and post-bronchodilator spirometry. The inclusion criteria were:

Subject characteristics

Characteristics of the 85 study participants and 263 clinic visits are presented in Table 1. The analysis included 35 patients with 4 clinic visits, 31 with 3 clinic visits, 11 with 2 clinic visits, and 8 with 1 clinic visit (Fig. S2 in the Supplementary Material). The median (25–75th percentile) time between the first and last study visit was 312 (207–327) days. All participants were male and 89.4% were white. The average participant age was 72.7 ± 8.6 years old and 45% had a BMI ≥30 kg/m2.

Discussion

We investigated the effects of ambient and indoor PM gamma activities with moving averages up to 7 days before phlebotomy on biomarkers of systemic inflammation (i.e., IL-6, CRP) and endothelial activation (i.e., sVCAM-1). There were positive associations with ambient and indoor PM gamma activities with IL-6 and CRP, with stronger effects for CRP; however, there were no consistent associations with sVCAM-1. We conducted a sensitivity analysis to consider possible confounding by indoor or

Conclusion

This study has implications for understanding effects of low-level radiation associated with PM on systemic effects that have not previously been appreciated. We observed positive associations between ambient and indoor PM gamma activities as surrogates of PM radioactivity and biomarkers of systemic inflammation in COPD patients. Our finding suggests that PM with attached radionuclides may contribute to adverse health effects.

Declaration of competing interest

The authors do not have any competing financial interests, including relevant financial interests, activities, relationships, and affiliations.

Acknowledgements

This publication was funded by the National Institute of Health (NIH) grants (P01-ES009825 and R01-ES019853), the National Institute of Environmental Health Sciences (NIEHS) (P30-ES000002), and was conducted with resources and the use of facilities at the VA Boston Healthcare System. The contents do not reflect the position of the Department of Veterans Affairs or the United States Government. This publication was also made possible by USEPA grant (RD-835872-01) through the Harvard University

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