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Published in final edited form as: Environ Res. 2022 Oct 6;216(Pt 1):114492. doi: 10.1016/j.envres.2022.114492

Particle radioactivity from radon decay products and reduced pulmonary function among chronic obstructive pulmonary disease patients

Veronica A Wang a, Petros Koutrakis a, Longxiang Li a, Man Liu a, Carolina LZ Vieira a, Brent A Coull a,b, Edward F Maher a, Choong-Min Kang a, Eric Garshick c,d,e,*
PMCID: PMC9701170  NIHMSID: NIHMS1843994  PMID: 36209792

Abstract

Background:

Radon (222Rn) decay products can attach to particles in the air, be inhaled, and potentially cause airway damage.

Research question:

Is short-term exposure to particle radioactivity (PR) attributable to radon decay products emitted from particulate matter ≤2.5 μm in diameter (PM2.5) associated with pulmonary function in chronic obstructive pulmonary disease (COPD) patients?

Study design and methods:

In this cohort study, 142 elderly, predominantly male patients with COPD from Eastern Massachusetts each had up to 4 one-week long seasonal assessments of indoor (home) and ambient (central site) PR and PM2.5 over the course of a year (467 assessments). Ambient and indoor PR were measured as α-activity on archived PM2.5 filter samples. Ratios of indoor/ambient PR were calculated, with higher ratios representing PR from an indoor source of radon decay. We also considered a measure of outside air infiltration that could dilute the concentrations of indoor radon decay products, the indoor/ambient ratio of sulfur concentrations in PM2.5 filter samples. Spirometry pre- and post-bronchodilator (BD) forced expiratory volume in 1 s (FEV1) and forced vital capacity (FVC) were conducted following sampling. Generalized additive mixed models were adjusted for meteorologic variables, seasonality, and individual-level determinants of pulmonary function. We additionally adjusted for indoor PM2.5 and black carbon (BC).

Results:

PR exposure metrics indicating radon decay product exposure from an indoor source were associated with a reduction in FEV1 and FVC. Patients in homes with high indoor PR (≥median) and low air infiltration (<median) compared to others had a −26.9 (95% CI: −61.4, 7.7) mL and −75.4 (95% CI: −128.6, −22.2) mL reduction in post-BD FEV1 and FVC, respectively. These associations remained similar after PM2.5 and BC adjustment.

Interpretation:

Our findings raise concern about the harmful effects of PR exposures attributable to residential radon on pulmonary function in patients with COPD.

Keywords: Particle radioactivity, Pulmonary function, Radiation, Chronic obstructive pulmonary disease, Radon, Spirometry

1. Introduction

With over 12 million adults diagnosed (5% of the United States adult population), chronic obstructive pulmonary disease (COPD) is a leading cause of disability and death that poses substantial economic and social burden (Centers for Disease Control and Prevention, 2022). In 2010, approximately $32 billion was spent on COPD-related patient care, and medical costs were projected to grow to $49 billion by 2020 (Ford et al., 2015). Yet, approaches to mitigate its global burden, including identification of environmental factors that may worsen its impact on health has been under-funded compared to other leading causes of death (Quaderi and Hurst, 2018).

Consistent with the existing literature on ambient particulate matter (PM) exposure (Bloemsma et al., 2016; Doiron et al., 2019), our previous studies found that indoor PM was associated with increased systemic inflammation and oxidative stress and reduced pulmonary function among COPD patients in Eastern Massachusetts (Hart et al; Garshick et al., 2018; Grady et al., 2018). It has recently been recognized that an attribute of PM with potential to promote pulmonary damage after inhalation is radionuclides attached to PM (Vieira et al., 2019; Nyhan et al., 2019), referred to as particle radioactivity (PR). Though ionizing radiation has many sources (e.g., cosmic radiation and medical procedures), the majority of natural background radiation (and, thus, of PR) is from radon (222Rn), which decays into α-, β-, and γ-emitting decay products (Keith et al., 2012; Schauer, Linton). Although radon gas itself is rapidly exhaled, freshly generated radon decay products (also referred to a radon progeny) can rapidly attach to particles in the ambient and indoor air and be inhaled into the airways. After deposition, particles continue to emit radiation in the lungs with a residence time that can range from several days to months (Möller et al., 2004). Compared to β- and γ-emissions from radionuclides, α-emitting particles are considered the most toxic due to their high energy and large mass (Institute of Medicine (US), 1995). Since α-radiation cannot penetrate the intact epidermis, inhalation is the predominant route of exposure, and evidence that α-radiation may cause pulmonary damage is suggested by its effects on inducing inflammation and reactive oxygen species in human lung fibroblasts as well as up-regulating gene pathways in human pulmonary epithelial cells associated with inflammatory and respiratory diseases (Narayanan et al., 1999; Chauhan et al., 2012). Our previous studies used Boston-area measurements of ambient particle β- and γ-activity (radiation) from the Environmental Protection Agency (EPA) and found that short-term exposures were associated with reduced pulmonary function in elderly men and COPD patients, respectively (Vieira et al., 2019; Nyhan et al., 2019). In contrast to our previous studies, the present study has several advantages, including the direct assessment of indoor exposure (i.e., in-home living space versus ambient measurements) and use of a more relevant exposure metric to health (i.e., particle α-activity versus β- and γ-activity).

Since there is no cure, minimizing the inhalation of hazards that may further reduce pulmonary function is important in COPD patients, a population that is particularly vulnerable to air pollution (Heinrich and Schikowski, 2018). In this report, for the first time, we assessed associations of ambient and indoor exposures to particle α-activity determined from indoor PM ≤ 2.5 μm (PM2.5) filter samples with pulmonary function among COPD patients in Eastern Massachusetts and its vicinity over a year in 2012–2017.

2. Materials and methods

2.1. Study population

The COPD and Air Pollution Study cohort consists of patients with chronic airflow obstruction from Eastern Massachusetts and its vicinity. Individuals who were at least 40 years old, were not current smokers, and had a forced expiratory volume in 1 s (FEV1) to forced vital capacity (FVC) ratio (FEV1/FVC) of less than 0.7 measured by post-bronchodilator (BD) spirometry or emphysema based on a clinical CT scan report were recruited at the Veterans Affairs Boston Healthcare System in 2012–2017, as previously described (Hart et al., 2018). Of the 224 individuals who consented, 49 were excluded due to current smoking or report of regular in-home combustion sources, 6 did not return after consent, and an additional person was excluded due to a new diagnosis of multiple sclerosis. Participants with confirmed eligibility were scheduled to return 4 times seasonally over one year, with each visit about 3 months apart. Each visit was at least 2 weeks after antibiotics or steroids for COPD exacerbation were completed (stable clinical status). We excluded 22 persons with less than 10 pack-years of smoking, which was consistent with the definition for COPD commonly used in large treatment trials and epidemiologic studies, to minimize disease overlap with chronic asthma (COPDGene; Tashkin et al., 2008; Albert et al., 2011). Only study visits where the home PM sampler was returned within 8 days before the pulmonary function tests were included. The final study sample consisted of 8 participants with 1 visit, 7 participants with 2 visits, 3 participants with 3 visits, and 109 participants with 4 visits, giving a total of 142 participants with 467 assessments (e-Fig. 1).

2.2. Assessment of ambient and indoor PM2.5

The PM2.5 sampling and analysis methods have been described in detail previously (Busenkell et al., 2022). Briefly, participants were asked to place a particle sampler in the room they spend the most time in their home, apart from the kitchen, for the week prior to each follow-up visit. Though we did not have information about sampling location for one participant, about 68% and about 20% of the remaining participants placed the sampler in their living room and bedroom, respectively. The integrated filter measures reflect average exposures during the sampling period (mean ± SD = 173.6 ± 20.2 h based on an internal timer over 7.7 ± 0.8 days). PM2.5 was collected on Teflon filters at a flow rate of 1.8 L/min. The samples were analyzed for mass using gravimetric analysis and for black carbon (BC) using a SootScan Transmissometer (OT21, Magee Scientific, Berkeley, CA) by measuring optical absorbance at 880 nm on the filters. At the Harvard Supersite (located on the roof of Francis A. Countway Library, Boston, MA, 6 stories above ground level), daily ambient PM2.5 was determined gravimetrically, and hourly BC was measured using an aethalometer (AE-22, Magee Scientific, Berkeley, CA) at 880 nm and was averaged into daily values. Ambient PM2.5 measurements from this Supersite have been previously shown to capture temporal variability in indoor PM2.5 samples in this cohort (Tang et al., 2018). Daily ambient values were averaged over the indoor sampling dates.

2.3. Assessment of ambient and indoor PR

Particle α-activity from long-lived radionuclides attributable to radon decay was measured from archived ambient and indoor PM2.5 filters using a low-background proportional counter (Model LB4200; Canberra Industries, Inc., Meriden, CT) with a P10 carrier gas. It is known that following the rapid decay of short-lived radon progeny with half-lives of seconds to minutes, α-activity on filters represents the decay of 210Pb, the longest-lived radionuclide (t1/2 = 22 years), to α-emitter 210Po (t1/2 = 138 days) (EPA). After about one and a half years, particle α-radiation from 210Po decay is limited by the rate of 210Pb day. Therefore, since radioactivity was measured 3 years or more after sample collection, particle α-activity at the original time of sampling can be back-calculated from α-activity at the time of analysis based on the decay constant of 210Po and volume of air passing through the sampler as described in more detail elsewhere (Liu et al., 2020; Kang et al., 2020). One indoor sample measured over 9 standard deviations above the study mean and was excluded from further analysis ((e-Fig. 2).

Indoor PR originates from indoor sources of radon and from the infiltration of outdoor PR (Kang et al., 2020). The indoor/ambient PR ratio was derived from the directly measured indoor and ambient PR. A higher ratio indicates a greater contribution of an indoor radon source to indoor PR concentrations. Since greater air infiltration can reduce the contribution of indoor radon to indoor PR, we also derived a metric, referred to as high indoor PR with low air infiltration, where observations are grouped into two categories: (1) homes that had median or higher PR and lower than median air filtration and (2) the remaining observations (reference). Outdoor air infiltration was based on the sampling period specific indoor/ambient sulfur concentration ratio, a well-described proxy for outdoor PM2.5 infiltration into the indoor space (Sarnat et al., 2002). Ambient and indoor sulfur on the PM2.5 filters were measured using an energy dispersive X-ray fluorescence spectrometer (Epsilon 5; PANalytical, The Netherlands). The distributions of indoor/ambient PR and indoor/ambient sulfur ratio are shown in Supplemental Materials (e-Figs. 3–5). Three indoor/ambient PR values and 2 indoor/ambient sulfur values were over 5 standard deviations above their respective sample means. These values were considered implausible and were excluded from analysis.

2.4. Pulmonary function

Pre- and post-BD FEV1, FVC, and FEV1/FVC were obtained from spirometry (Hdpft 1000; Nspire) that was conducted pre- and post- 2 puffs of 180 μg albuterol using a valved space during each study visit following methods recommended by the American Thoracic Society (Miller, 2005). Other pulmonary medications were not withheld prior to the test, and we used the highest values of FEV1 in L and FVC in L from acceptable efforts, which were also used to calculate the FEV1/FVC ratio. In over 90% of visits, the sampler was returned within 1 day prior to pulmonary function testing.

2.5. Covariates

Individual-level sociodemographic variables and determinants of pulmonary function were collected using questionnaires. Additionally, height in cm and weight in kg were measured, pulmonary medication use was updated, and any respiratory illness in the last 2 weeks was recorded at each visit. Body mass index in kg/m2 was derived from the height and weight measurements. Age at each study visit was calculated from date of birth. Based on the latitude and longitude of each participant’s residential address, we used average ambient temperature in °C and ambient dew point temperature in °C matched to the indoor sampling dates obtained from the Parameter-elevation Regression on Independ Slopes Model developed by the Northwest Alliance for Computational Science & Engineering (PRISM Climate Group) at the 4 km grid scale to calculate ambient relative humidity in %. The corresponding ambient temperature in °C and relative humidity values for the central site (at Francis A. Countway Library) were obtained from the Boston Logan International Airport weather station managed by the National Oceanic Atmospheric Administration’s National Centers for Environmental Information (NOAA).

2.6. Statistical analysis

To examine the association of PR with pulmonary function, we used generalized additive mixed models with a random intercept for each subject to account for correlated measures within an individual. We adjusted for age in years (continuous), body mass index (continuous), sex (male/female), race (White/non-White), educational attainment (<high school, high school, >high school), cold or other respiratory illness in the last 2 weeks (no/yes), use of short-acting BD medication within 6 h of the pulmonary function tests (no/yes), use of any long-acting BD (no/yes), and use of any inhaled steroids (no/yes). Height (continuous) was included in models assessing FEV1 and FVC. Seasonality was adjusted for using sine and cosine terms based on the pulmonary function test date, sin(2π∗day of year365) and cos(2π∗day of year365), respectively. Penalized splines were used for continuous covariates, including exposure, to allow for potential non-linearities.

In secondary analyses, we controlled for PM2.5 and BC separately in our models to estimate the independent effects of PR, as common air pollutant exposures have been previously found to be associated with pulmonary function in our study cohort (Hart et al, 2018). We controlled for indoor air pollutants in our secondary models except for those with ambient PR exposure, where ambient air pollutants were used. Likewise, we controlled for ambient temperature and relative humidity based on the central site or residential address depending on the exposure metric in all analyses. We also conducted additional analysis restricted to male participants. All statistical analyses were performed with R version 4.0.4 (R Development Core Team, Vienna, Austria).

3. Results

As shown in Table 1, participants were predominantly male (90.1%) with a mean ± SD age of 72.8 ± 8.2 years and a body mass index of 30.3 ± 5.7 kg/m2 at study baseline. Most had completed at least a high school education (85.9%). Short-acting BD, long-acting BD, and inhaled steroid use were common, 78.2, 78.9, and 73.2%, respectively. These characteristics remained similar over all study visits. Summary statistics describing the distribution of environmental exposures and pulmonary function outcomes are presented in Table 2. Median (25th percentile, 75th percentile) ambient PR, indoor PR, and indoor/ambient PR during the study period (2012–2017) were 1.62 (1.33, 1.99) mBq/m3, 1.24 (0.95, 1.62) mBq/m3, and 0.76 (0.62, 0.91), respectively. About 21% of the observations were categorized as high indoor PR with low air infiltration. Median (25th percentile, 75th percentile) pre-BD FEV1, FVC, and FEV1/FVC were 1.77 (1.36, 2.27) L, 3.24 (2.74, 3.76) L, and 0.57 (0.47, 0.64), respectively, and post-BD values were similar. Ambient and indoor PR were strongly correlated (Spearman ρ = 0.62).

Table 1.

Sociodemographic and medical characteristics of the study population (142 participants, 467 clinical visits).

Baseline (n = 142) All visits (n = 467)
Age, years 72.8 ± 8.2 73.2 ± 8.3
Body mass index, kg/m2 30.3 ± 5.7 30.3 ± 5.8
Height, cm 172.0 ± 6.5 172.0 ± 6.5
Female 3 (2.1%) 10 (2.1%)
Non-white 14 (9.9%) 46 (9.9%)
Educational attainment
<High school 20 (14.1%) 69 (14.8%)
High school 49 (34.5%) 153 (32.8%)
>High school 73 (51.4%) 245 (52.5%)
Respiratory illness ≤2 weeks ago 23 (16.2%) 83 (17.8%)
Short-acting bronchodilator <6 h ago 111 (78.2%) 365 (78.2%)
Long-acting bronchodilator 112 (78.9%) 367 (78.6%)
Inhaled steroids 104 (73.2%) 347 (74.3%)
Pre-BD FEV1% predicted, % 65.3 ± 21.4 65.8 ± 21.3
Pre-BD FVC% predicted, % 86.6 ± 19.3 86.6 ± 19.6
Post-BD FEV1% predicted, % 69.1 ± 21.8 69.5 ± 21.7
Post-BD FVC% predicted, % 89.8 ± 19.7 89.7 ± 20.0
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Summary statistics of continuous variables were reported as mean ± standard deviation while discrete variables were reported as n (%).

BD = bronchodilator; FEV1 = forced expiratory volume in 1 s; FVC = forced vital capacity.

Table 2.

Summary statistics of PR exposures and pulmonary function outcomes from 142 chronic obstructive pulmonary disease patients with 467 sampling sessions in Eastern Massachusetts, USA (2012–2017).

Mean ± SD Median (25th percentile, 75th percentile) (Minimum, Maximum)
Exposures
Ambient PR, mBq/m3 1.69 ± 0.54 1.62 (1.33, 1.99) (0.30, 3.55)
Indoor PR, mBq/m3 1.30 ± 0.54 1.24 (0.95, 1.62) (0.15, 3.73)
Indoor/ambient PR 0.78 ± 0.27 0.76 (0.62, 0.91) (0.08, 1.74)
High indoor PR with low ventilation – 97 (20.8%)* –
Ambient PM2.5, μg/m3 6.12 ± 2.11 5.61 (4.67, 7.34) (1.88, 13.44)
Indoor PM2.5, μg/m3 8.52 ± 6.13 6.80 (4.75, 10.40) (0.17, 45.88)
Ambient BC, μg/m3 0.52 ± 0.22 0.46 (0.36, 0.61) (0.18, 1.53)
Indoor BC, μg/m3 0.61 ± 0.25 0.58 (0.45, 0.72) (0.17, 2.24)
Indoor/ambient sulfur ratio 0.70 ± 0.26 0.69 (0.54, 0.86) (0.00, 1.88)
Central ambient temperature, °C 11.1 ± 9.0 10.2 (3.81, 19.57) (−7.8, 27.0)
Residential ambient temperature, °C 10.3 ± 9.3 9.8 (2.60, 19.13) (−10.6, 27.4)
Central ambient relative humidity, % 64.9 ± 8.2 64.8 (58.96, 70.86) (41.2, 85.4)
Residential ambient relative humidity, % 64.5 ± 7.4 65.0 (58.99, 70.01) (42.8, 82.3)
Outcomes
Pre-BD FEV1, L 1.80 ± 0.61 1.77 (1.36, 2.27) (0.46, 3.47)
Pre-BD FVC, L 3.29 ± 0.83 3.24 (2.74, 3.76) (1.05, 5.99)
Pre-BD FEV1/FVC 0.55 ± 0.13 0.57 (0.47, 0.64) (0.20, 0.91)
Post-BD FEV1, L 1.92 ± 0.62 1.91 (1.48, 2.40) (0.50, 3.77)
Post-BD FVC, L 3.43 ± 0.83 3.33 (2.86, 3.88) (1.09, 6.14)
Post-BD FEV1/FVC 0.56 ± 0.13 0.58 (0.47, 0.65) (0.21, 0.87)
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SD = standard deviation; PR = particle radioactivity; BD = bronchodilator; FEV1 = forced expiratory volume in 1 s; FVC = forced vital capacity; PM2.5 = particulate matter ≤2.5 μm; BC = black carbon.

*

N (%) of participants exposed to high indoor PR (≥median) with low ventilation (<median).

The effective degrees of freedom for continuous PR exposures when penalized splines were used were estimated to be one in almost all models, except for ambient PR, where higher order polynomials were estimated. The estimated non-linear associations for ambient PR are shown in e-Fig. 6. Because the confidence intervals (CIs) were wide at the more extreme values of ambient PR where the non-linearities occurred, we decided to use a linear term for all PR exposures in all models for consistency and ease of interpretability. We reported the estimated difference in pulmonary function outcome per interquartile range (IQR) increase in continuous PR exposure with 95% CIs.

Directly measured ambient and indoor PR were not associated with pre- or post-BD FEV1 and FVC ((e-Tables 1 and 2). However, metrics representing PR primarily from an indoor radon decay source were negatively associated with FEV1 and FVC, especially post-BD. An IQR increase in indoor/ambient PR had a −8.9 (95% CI: −24.2, 6.3) mL reduction in average post-BD FEV1 and −7.7 (95% CI: −31.6, 16.2) mL reduction in average post-BD FVC. The greatest effects were in homes with high indoor PR and low air infiltration, a −26.9 (95% CI: −61.4, 7.7) mL reduction in post-BD FEV1 and −75.4 (95% CI: −128.6, −22.2) mL reduction in post-BD FVC, compared to others (Fig. 1). The associations for pre-BD FEV1 and FVC were similar to post-BD findings, although attenuated (e-Tables 1–2). There was no consistent effect of any metric of PR exposure on pre- and post-BD FEV1/FVC (e-Table 3). The results for all pulmonary function outcomes were essentially the same after adjusting for PM2.5 or BC (e-Tables 1–3) and after we restricted our analysis to male participants (e-Fig. 7).

Fig. 1.

Fig. 1.

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The association of particle radioactivity (PR) exposures with post-bronchodilator (BD) forced expiratory volume in 1 s (FEV1) and forced volume capacity (FVC). The numeric estimates represent the estimated difference in pulmonary outcome for an interquartile range (IQR) increase in PR exposure. However, for the high indoor PR with low ventilation exposure metric the numeric estimates represent the estimated difference in pulmonary outcome of those exposed to median or higher indoor PR and lower than median air infiltration compared to the rest of the observations. Each estimate was from a separate generalized additive mixed model with a random intercept for each subject and was adjusted for age, body mass index, height, sex, race, educational attainment, respiratory illness in the past 2 weeks, pulmonary medication use, seasonality, temperature, and relative humidity. Summary statistics for each PR exposure are shown in Table 2.

4. Discussion

Although the association between radon exposure and lung cancer is well established (Li et al., 2020), associations with other health-related effects are limited. Conde-Sampayo et al. (2020) previously hypothesized that prolonged exposure to radon may result in chronic pulmonary inflammation and contribute to COPD pathophysiology and highlighted two studies conducted in the general population, where residential radon was associated with increased COPD mortality in the United States (Turner et al., 2012) and COPD prevalence and hospital admission in Galacia (Barbosa-Lorenzo et al., 2017). A recent study by Pando-Sandoval et al. (2022) investigated the association of long-term exposure radon gas (measured over 90 days) and pulmonary function (based on measurements made within 3 years of the radon measurement) in patients with COPD and did not find an association. In contrast, in the current study we measured PR attributable to radon decay over a week prior to the assessment of pulmonary function up to 4 times per patient. Our findings suggest that short-term exposures to PR attributable to radon decay products in the home may reduce pulmonary function among COPD patients and appears to have a greater effect on FVC than FEV1, including after adjustment for PM2.5 and BC.

Our findings are consistent with our previous studies assessing short-term associations of PR measured as γ-activity and β-activity with pulmonary function. In a subset of this cohort, we previously studied the effects of ambient particle γ-activity measured over the week before pulmonary function testing, which is attributable to radon decay but also from atmospheric cosmic rays, using measurements in the Boston area from the EPA (Vieira et al., 2019). Indoor particle γ-activity was estimated using the indoor/ambient sulfur ratio and was negatively associated with FEV1 and FVC, with magnitudes that were similar to, if not slightly greater than, those for ambient particle γ-activity. Associations with FEV1/FVC were inconsistent. Outside of the present cohort, associations of pulmonary function with 7-, 14-, 21-, and 28-day ambient particle β-activity was assessed in the Department of Veterans Affairs Normative Aging Study cohort, which, like this study, consists predominately of elderly, white men (Nyhan et al., 2019). The greatest decrement per IQR increase in ambient particle β-activity for FEV1 (−2.4%) and FVC (−2.4%) was observed at 28-days. Our current study, in comparison, addresses a research gap and is the first to assess effects of directly measured indoor PR. The greater effect of PR on FVC relative to FEV1 post-BD and the lack of association with a reduced FEV1/FVC suggests that PR may be associated with a restrictive ventilatory defect, rather than reducing FEV1/FVC further in our COPD participants.

Since exposure to PR was assessed on archived PM2.5 samples (long-lived radionuclides), it was not possible to measure α-activity from short-lived radon decay products generated early in the radon decay chain. However, we did derive two exposure metrics, indoor/ambient PR ratio and high indoor PR with low air infiltration, to represent exposure from an indoor radon source as a surrogate of exposure to these short-lived radon products. Based on our previous work where both products early and late in the decay chain were measured simultaneously in occupied Boston-area homes, these short-lived radon products emit more α-activity (approximately 4 orders of magnitude greater) and are, thus, potentially more harmful to human health than the long-lived radon decay products we measured in this current study (Kang et al., 2020). Therefore, it is likely that an effect of directly measured indoor long-lived particle α-activity was not found to be associated with pulmonary function in this study because short-lived particle α-activity is primarily responsible. While we did find associations with the exposure metrics for exposure from an indoor source, future work with direct, real-time measurements of short-lived radon products are needed to fully characterize the health effects of radon.

The mechanisms responsible for the associations observed are uncertain. However, there is an extensive literature on the biological mechanisms for lung injury from radiotherapy, which distinctively differs from exposure to particle radiation in the air in terms of dose, duration, source, and purpose (Ying et al., 2021; Käsmann et al., 2020), where the level of radiation dosage from particle-bound radiation is far lower, more chronic, and internal (as opposed to external). Experimental studies assessing the cellular effects of α-radiation and radon support common biological mechanisms, such as oxidative damage and inflammation (Narayanan et al., 1999; Nie et al., 2012). Delays in particle clearance (Möller et al., 2004, 2008) suggest that continued exposure to higher levels of indoor radon decay products pollution could be a risk factor for impaired pulmonary function in COPD patients. For example, Möller et al. (2004) found that even in healthy non-smokers, where mucociliary clearance removes a large proportion of particles from the lung within 24 h after particle deposition, there is long-term retention of a notable fraction of inhaled particles (Möller et al., 2004). In smokers and COPD patients, mucociliary clearance is impaired, and ultrafine particles have been found to be largely retained and to accumulate in the lungs even after 48 h after particle deposition (Möller et al., 2008).

The Bureau of Environmental Health’s Radiation Control Program and the EPA found in 1988 that approximately one-fourth of homes in Massachusetts had indoor radon concentrations above the EPA action level of 4 pCi/L (148 Bq/m3), although more recent estimates are unavailable (Massachusetts Environmental Public Health Tracking, 2022). Compared to the EPA threshold, the radiation concentration for PR is notably lower, where indoor PR ranged from 0.15 to 3.73 mBq/m3 in the present study. Thus, interventions for radon remediation on the individual-to policy-level should be prioritized considering the known risk that radon poses to lung cancer as well as emerging evidence of adverse impacts on other health endpoints at radiation concentration levels far below the EPA standard.

Our study has numerous strengths. To the best of our knowledge, this study is the first to investigate the association of ambient and indoor PR, as measured by particle α-activity, with pulmonary function. Furthermore, by having indoor air pollution samples, which were sampled in the indoor space where participants spent most of their time (sample mean = 17 h/day), we were also able to investigate the impact of novel environmental exposure metrics and motivate future studies to measure and study short-lived radon progeny. However, our study also has some limitations. Because the COPD and Air Pollution study was designed to study exposure to PM, highly energetic short-lived radon progeny generated early in the radon decay chain and radon concentration (useful for result comparison) were not directly measured. Future studies designed to examine radon and its decay products in their gas and particle phases together with longitudinal assessment of pulmonary function are needed to further assess short- and long-term effects on pulmonary function. Another limitation of our study is that our study population consists predominantly of elderly, white men, so our results may not be generalizable to all COPD patients. In studies with larger sample sizes and that are more representative of the general public, investigators may wish to assess for effect modification by sex (Barnes, 2016), race/ethnicity (Gim et al., 2020), socioeconomic status (Gershon et al., 2012), and smoking status (Tan et al., 2015) given potential variation in COPD characteristics in the literature.

5. Conclusions

In conclusion, α-activity attributable to radon decay products in the home was associated with reduced pulmonary function in COPD patients, which motivates future research on the pulmonary effects of short- and long-lived radon decay products and support efforts to limit PR from radon.

Supplementary Material

Supplement

Acknowledgements

The authors would like to thank the COPD and Air Pollution study participants for their dedicated participation. Additionally, we would like to thank Stephanie Grady and Christina Collins for study and database management as well as Mike Wolfson, Denise Lee, Anisa Khadraoui, and Daniel Bernard for their assistance in collecting data for this study.

Funding

This work was supported by the National Institute of Environmental Health Sciences [NIH Grants R01 ES019853, R21 ES029637] and by resources and the use of facilities at the Veterans Affairs Boston Healthcare System. The contents do not represent the views of the US Department of Veterans Affairs or the United States Government. This publication was also made possible by US EPA grants RD-83479801 and RD-83587201. Its contents are solely the responsibility of the grantee and do not necessarily represent the official views of the US EPA. Further, US EPA does not endorse the purchase of any commercial products or services mentioned in the publication.

Footnotes

Ethics approval

The Institutional Review Boards of Veterans Affairs Boston and Harvard Medical School approved the procedures in this study, and inform consent was obtained for all participants.

Credit author statement

Eric Garshick: Conceptualization, Methodology, Writing- Review & Editing, Resources, Supervision, Funding acquisition. Choong-Min Kang: Conceptualization, Methodology, Writing- Review & Editing, Resources. Edward F. Maher: Conceptualization, Methodology, Writing- Review & Editing. Brent A. Coull: Methodology, Writing- Review & Editing. Carolina L.Z. Vieira: Writing- Review & Editing. Man Liu: Methodology, Writing- Review & Editing, Resources. Longxiang Li: Conceptualization, Methodology, Writing- Review & Editing. Petros Koutrakis: Conceptualization, Methodology, Software, Formal analysis, Writing- Review & Editing, Resources, Supervision. Veronica A. Wang: Conceptualization, Methodology, Software, Formal analysis, Writing- Original Draft.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Appendix A.: Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.envres.2022.114492.

Data availability

The data that has been used is confidential.

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