Objectives: Exposure to ionizing radiation may increase the risk of circulatory diseases, including heart disease. A limited number of cohort studies of underground miners have investigated these associations. We previously reported a positive but non-statistically significant association between radon progeny and heart disease in a cohort of Newfoundland fluorspar miners. In this study, we report updated findings that incorporate 15 additional years of follow-up. Methods: The cohort included 2050 miners who worked in the fluorspar mines from 1933 to 1978. Statistics Canada linked the personal identifying data of the miners to Canadian mortality data to identify deaths from 1950 to 2016. We used previously derived individual-level estimates of annual radon progeny exposure in working-level months. Cumulative exposure was categorized into quantiles. We estimated relative risks and their 95% confidence intervals using Poisson regression for deaths from circulatory, ischemic heart disease and acute myocardial infarction. Relative risks were adjusted for attained age, calendar year, and the average number of cigarettes smoked daily. Results: Relative to the Newfoundland male population, the standardized mortality ratio for circulatory disease in this cohort was 0.82 (95% CI 0.74–0.91). Those in the highest quantile of cumulative radon progeny exposure had a relative risk of circulatory disease mortality of 1.03 (95% CI 0.76–1.40) compared to those in the lowest quantile. The corresponding estimates for ischemic disease and acute myocardial infarction were 0.99 (95% CI 0.66–1.48), and 1.39 (95% CI 0.84–2.30), respectively. Conclusions: Our findings do not support the hypothesis that occupational exposure to radon progeny increases the risk of circulatory disease.
Keywords: Radon progeny; Cardiovascular disease; Miner; Cohort study
A correction to this article is available online at https://doi.org/10.1007/s00420-022-01945-6.
The possibility that exposure to ionizing radiation increases the risk of circulatory system disease at low and moderate doses has important implications given the widespread and increasing use of medical applications such as computed topography scans, nuclear medicine, and radiotherapy (Mettler [
Findings from epidemiological investigations across a diverse series of study populations provide compelling evidence that ionizing radiation causes circulatory disease. This evidence includes higher rates of heart disease following radiotherapy treatment (> 30 Gy) for breast cancer (Darby et al. [
Studies of miners have provided important insights into the relationship between radon and cancer (especially lung cancer); however, relatively few have assessed the dose–response relationship between radon and circulatory diseases. Most of this research has relied on comparisons of circulatory disease death rates among miners to the general population (Little et al. [
The source of radon progeny exposure among the fluorspar miners was via the groundwater that ran through the mines. As a result, exposure–response analyses of radon and health outcomes in this cohort are not confounded by other sources of radiation, however, these workers were exposed to other substances such as diesel and silica that are recognized carcinogens and that increase the risk of cardiovascular disease. We have previously analyzed associations between radon and circulatory disease mortality in this cohort The earlier paper included mortality follow-up from 1950 to 1990 and found elevated, but not statistically significant, relative risks for coronary heart disease (CHD) mortality among miners with a cumulative radon exposure exceeding 1,000 WLMs (RR = 1.5, 95% CI 0.77–2.75) (Villeneuve and Morrison [
Our objective is to conduct an updated analysis of the relationship between radon exposure and circulatory disease in the cohort of Newfoundland fluorspar miners, with an additional 15 years of mortality follow-up (1950–2016) since our previous analysis. The additional follow-up provides the increased statistical power to assess these associations in a cohort that is relatively small (~ 2000 miners). In this paper, we use the term "radon" throughout, and this refers to radon (
A detailed description of the cohort of Newfoundland Fluorspar miners has previously been published (Morrison et al. [
Employees lacking the personal identifying data required for record linkage to Canada's national mortality databases were excluded. Most of these workers were employed for a short time during World War II. Miners who died prior to the start of mortality follow-up in 1950, and 19 miners born before 1900 for whom no matching death record was found were excluded from analyses. These miners were either lost to follow-up or died before 1950 when death registration in the Canadian Mortality Database was incomplete. Newfoundland was the last province to join the Canada confederation on 31 March 1949.
For each underground miner, an annual measure of exposure to radon was derived by combining sampling measures with information on mine location and architecture, amount of water inflow, miners' working hours, general working conditions, and place of residence (1933–1960). Those who worked on the surface were assumed to have only background levels of radon exposure.
The method of radon sampling differed from the start of commercial mining in 1933 to the last mine's closure in 1978. Prior to 1960, radon levels were not monitored, rather 80 samples were taken from 50 underground locations in the principal mine—the radon concentrations of these samples ranged from 0.4 to 193 working levels (WLs). To assign pre-1960 exposures, Corkill and Dory performed a retrospectively reconstructed estimated doses using data from the 80 samples supplemented with information collected from inspector reports, Commission hearings and miners' themselves (Corkill and Dory [
In 1960, mechanical ventilation was installed in the mines. Shortly thereafter, regular monitoring of radon levels began. Between 1961 and 1967, between 400 and 700 samples were taken annually to measure radon progeny in the mines (Morrison et al. [
Later, from 1968 to 1978, radon levels were measured daily for each miner at the location in the mine they worked. For underground miners, the mean exposure from 1968 to 1978 decreased to 0.6 WLM.
A series of smoking surveys were administered to miners in 1966, 1970, and 1978 (Morrison et al. [
A linked file that contained occupational data and mortality status from the 2007 mortality update (Villeneuve et al. [
We classified the underlying cause of death for each miner according to the International Classification of Disease 9th (prior to 2000) and 10th revisions (2000 onwards). For this paper, deaths were categorized as described in Table 1. We also considered investigating the relationship between radon exposure and hypertension however, the relatively small numbers of death (~ 10) precluded exposure–response modeling.
Table 1 Number of deaths (1950–2016) for selected circulatory diseases among the cohort of Newfoundland fluorspar miners
Underlying cause of death ICD-9 codes ICD-10 codes Deathsa (rounded) Circulatory diseases 390–459 I00–I99 480 Ischemic heart disease 410–414 I20–I25 290 Acute myocardial infarction 410 I21–I22 175 Stroke (cerebrovascular disease) 430–438 I63 60 Hypertension 401–405 I10 10
ICD International classification of diseases The number of deaths were rounded to the base unit of 5 as per Statistics Canada's rules of disclosure governing the use of files linked to national mortality data
We first described the cohort in terms of key characteristics: type of miner (surface or underground), year of death, year of birth, lifetime smoking status, and age at first exposure to radon. We classified the data by categories of attained age (5-year age categories), and calendar period (10-year categories). The software program Epicure was used to tabulate the person-years of follow-up.
We used Poisson regression to perform internal cohort comparisons to describe the risk of mortality in relation to cumulative radon exposure. We did undertake a comparison of the mortality of the cohort to the general population as circulatory deaths, however, it is important to recognize that the standardized mortality ratio is prone to the healthy worker effect bias. The program EPICURE was used to calculate the person-years of follow-up and to fit the Poisson regression models (Preston [
Graph
This excess relative risk was adjusted for attained age, calendar period and average number of cigarettes smoked daily. We categorized the number of cigarettes smoked daily by using tertile–based cut-points (< 15, 15–21.7, > 21.7) such that the number of deaths from the circulatory disease were approximately equal. This is done to optimize the standard errors of the derived risk estimates for smoking. We repeated these analyses after excluding those with no smoking data to assess possible selection bias.
All presented frequencies, including counts, deaths and person-years, were rounded to the base unit five to adhere to Statistics Canada's rules of disclosure governing the use of records linked to national mortality data. However, all relative risks were estimated using the actual (not rounded) mortality counts. We performed all analyses at Statistics Canada's Research Data Center Network.
This study was funded by the Canadian Nuclear Safety Commission. Ethical approval was received by Carleton University's Research Ethics Board (Clearance #: 108564). As part of its record linkage process, Statistics Canada reviewed and approved the study.
The authors have no disclosures to report.
In total, the cohort included 315 miners who worked exclusively on the surface, while 1735 miners worked underground (Table 2). From 1950 to 2016, our study had 81,650 person-years of mortality follow-up, with 67% of miners deemed dead and 690 miners deemed to still be alive based on the record linkage. Among 2055 miners, 1080 (52.6%) miners had some cigarette smoking data, and of these 85% had ever smoked.
Table 2 Descriptive characteristics of the cohort of Newfoundland fluorspar miners with mortality follow-up from 1950 to 2016
Characteristics Number of miners % Surface miner (exclusively) 315 15.3 Underground miner 1735 84.7 Age at first exposure < 20 year 375 18.2 Age at first exposure 20–24 year 535 26.0 Age at first exposure 25–29 year 290 14.1 Age at first exposure 30–39 year 320 15.6 Age at first exposure 40 + year 215 10.5 Birth year Before 1900 175 8.5 1900–1909 170 8.3 1910–1919 390 19.0 1920–1939 420 20.4 1940–1949 340 16.5 1950–1959 475 23.1 Death year 1935–1949 25 1.2 1950–1959 90 4.4 1960–1969 185 9.0 1970–1979 230 11.2 1980–1989 230 11.2 1990–1999 240 11.7 2000–2009 330 16.1 2010–2016 135 6.7 Alive at end of follow-up 690 33.6 First employment 1933–1939 285 13.9 1940–1944 590 28.6 1945–1949 115 5.6 1950–1954 190 9.3 1955–1959 80 4.0 1960–1964 240 11.6 1965–1969 375 18.2 1970–1976 180 8.8 Lifetime smoking status Never 160 14.5 Ever 940 85.5 Unknown 955 Cigarettes smoked daily Never smoker 160 7.8 < 10 45 2.2 10–19 270 13.1 20–29 420 20.4 30–39 120 5.9 40 + 65 3.2 Unknown 970 47.2
The number of miners were rounded to the base unit of 5 as per Statistics Canada's rules of disclosure governing the use of files linked to national mortality data
The relative risks of mortality for selected circulatory causes of death according to the average number of cigarettes smoked daily are presented in Table 3. The risk of circulatory disease mortality among those who smoked more than 21.7 cigarettes per day relative to those smoking less than 15 cigarettes a day was 1.55 (95% CI 1.10–2.19). Increased risks from smoking were also observed for ischemic heart disease mortality and myocardial infarction. Due to the small numbers of death from cerebrovascular disease, we were unable to present these smoking risk estimates.
Table 3 Relative risk of selected circulatory disease mortality (1950–2016) by the average number of cigarettes smoked daily among the cohort of Newfoundland fluorspar miners
Cigarettes smoked daily Deaths Person-years of follow-up Relative Risk* (95% CI) Relative Risk*† (95% CI) Circulatory disease mortality < 15 50 13,520 1.0 1.0 15– < 21.7 75 16,933 1.09 0.76–1.56 1.12 0.79–1.60 21.7 + 85 14,900 1.55 1.10–2.19 1.61 1.13–2.27 Unknown 265 36,300 1.16 0.86–1.58 Ischemic heart disease < 15 30 13,520 1.0 1.0 15– < 21.7 45 16,933 0.99 0.63–1.57 1.02 0.65–1.62 21.7+ 60 14,900 1.67 1.09–2.57 1.71 1.11–2.64 Unknown 150 36,300 1.14 0.78–1.68 Acute myocardial infarction < 15 20 13,520 1.0 1.0 15– < 21.7 25 16,933 0.88 0.49–1.59 0.90 0.50–1.53 21.7+ 35 14,900 1.61 0.93–2.78 1.62 0.94–2.79 Unknown 90 36,300 1.05 0.64–1.71
*Relative risks were adjusted by attained age, calendar period, and average number of cigarettes smoked daily
The relative risks of cause-specific circulatory disease mortality across quintiles of cumulative radon exposure are shown in Table 4. Similar risk patterns were observed among the restricted cohort that had smoking data available, however, the confidence intervals of these estimates were larger. The linear excess relative risks (ERR) per 100 WLM for all circulatory diseases, ischemic heart disease, acute myocardial infarction and cerebrovascular mortality were: 0.002 (95% CI − 0.020 to 0.023), 0.005 (95% CI − 0.031 to 0.022), 0.026 (95% CI − 0.018 to 0.070) and − 0.35 (95% CI − 0.76 to 0.00) [data not shown]. None of these estimates attained statistical significance (at p < 0.05). The relative risk of circulatory disease mortality in the highest quintile relative to the lowest was 1.03 (95% CI 0.76–1.40). An increased risk was observed in the highest quintile for an acute myocardial infraction, while a lower risk was observed for cerebrovascular disease (Table 4). However, neither was statistically significant, and there was no statistically significant linear trend observed between any of the four circulatory causes of death and radon in the cohort.
Table 4 Relative risk of selected circulatory disease mortality (1950–2016) by cumulative radon exposure among the cohort of Newfoundland fluorspar miners
Cumulative exposure to radon in WLM (quantiles) Deaths Person-years of follow-up Relative Risk* (95% CI) Relative Risk (95% CI)*† Circulatory disease mortality 0 105 17,510 1.0 1.0 > 0– < 4.6 90 24,315 0.99 0.73–1.34 1.05 0.55–1.99 4.6– < 25.9 95 16,715 1.00 0.75–1.34 1.23 0.66–2.02 25.9– < 94.7 95 11,400 1.10 0.82–1.47 1.21 0.70–2.14 94.7+ 95 11,710 1.03 0.76–1.40 1.06 0.61–1.85 Ischemic heart disease 0 55 17,510 1.0 1.0 > 0– < 4.6 55 24,315 0.98 0.66–1.45 1.24 0.55–2.80 4.6– < 25.9 60 16,715 1.06 0.73–1.56 1.31 0.63–2.72 25.9– < 94.7 60 11,400 1.19 0.82–1.74 1.31 0.62–2.77 94.7+ 55 11,710 0.99 0.66–1.48 1.14 0.55–2.37 Acute myocardial infarction 0 30 17,510 1.0 1.0 > 0– < 4.6 30 24,315 1.08 0.64–1.82 1.30 0.42–3.98 4.6– < 25.9 30 16,715 1.01 0.60–1.70 1.26 0.47–3.41 25.9– < 94.7 40 11,400 1.36 0.83–2.23 1.13 0.41–3.12 94.7+ 40 11,710 1.39 0.84–2.30 1.56 0.60–4.06 Cerebrovascular disease 0 10 17,510 1.0 > 0– < 4.6 10 24,315 0.81 0.33–2.01 RRs suppressed 4.6– < 25.9 15 16,715 1.56 0.72–3.40 Due to small 25.9– < 94.7 15 11,400 1.26 0.56–2.85 Counts 94.7+ 10 11,710 0.69 0.26–1.86
*Relative risks were adjusted by attained age, calendar period, and average number of cigarettes smoked daily
This paper presents updated risk estimates for occupational radon exposure and circulatory disease in the Newfoundland fluorspar miners' cohort. These analyses extend previous analyses of the same outcome and now include over 65 years of mortality follow-up overall, and includes internal cohort analyses for myocardial infarction and cerebrovascular disease. There were no statistically significant associations between cumulative exposure to radon and any of the four circulatory disease causes of death studied. Indeed, the relative risk of mortality for all circulatory deaths and ischemic heart disease (among those in the highest quintile of exposure compared to the lowest) were null. The findings are consistent with previously published analyses of this cohort (Villeneuve et al. [
We pursued these updated analyses due to the availability of an additional 15 years of follow-up, which was anticipated to increase our statistical power. The number of observed circulatory disease deaths increased by 22% (from 389 to 475) with the longer follow-up. While the number of circulatory deaths is much less than the number in the German uranium cohort (475 vs 5417), it is more than the number of deaths examined via internal cohort analysis in the French uranium cohort (475 versus 76). Despite the increased number of deaths, the general patterns of risk for each cause of death did not change substantially. It is our view that further extension of the mortality follow-up of the cohort will not yield any further insights on possible associations between radon and circulatory diseases in this cohort. Our findings do not support the hypothesis that exposure to radon increases the risk of mortality from these causes.
As with previous analyses of this cohort, we excluded miners who died before 1950. This was done because national death registrations were incomplete before this time. It is also important to note that Newfoundland did not join Canada until 1949. The decision to exclude these workers, who would have had higher exposure to radon could introduce some selection bias. However, it is our view that this potential selection bias would not have changed our findings in a meaningful way. First, relative to the total number of deaths in the cohort during the nearly 70 years of follow-up time, the number of deaths before 1950 would have been small given that: mining operations began in the early 1930s, and the miners would have had to be young and healthy enough to work. Moreover, while Statistics Canada did identify 24 deaths before 1950, only four of these deaths were from circulatory disease, and three of these miners had accrued no cumulative exposure to radon. As a whole though, the cumulative exposure to radon among these 24 miners was nearly double the exposure (636 vs 318 WLM) relative to those who were followed from 1950 onwards.
Unlike many other studies of underground miners, we were able to adjust for the possible confounding role of cigarette smoking. As expected, smoking was positively related to the four circulatory diseases under study. While we were able to adjust for smoking, attained age, and calendar period effects, we recognize that a limitation of this work is that we are unable to adjust for other cardiovascular disease risk factors including hypercholesterolemia, diabetes, hypertension, or obesity—these risk factor data were not collected, and conditions such as diabetes and hypertension are not reliably captured on death certificates. The four aforementioned risk factors, along with cigarette smoking, are estimated to be responsible more than half of cardiovascular deaths in the United States (Patel et al. [
As done with prior studies, including those examining lung cancer outcomes, a five-year lag was incorporated into the modelling (Kreuzer et al. [
The characterization of occupational exposure to radon in this cohort is subject to exposure measurement error. The magnitude of this error is larger shortly after the mines began operation in the 1930s. The estimates of exposure during this early period were based on a back-extrapolation of measured concentrations, knowledge of the architecture of the mine, and well as interviews to understand the working conditions at the time. We categorized miners into quintiles of cumulative exposure to minimize the impacts of this measurement error.
In summary, this study confirms findings from the previous analysis of this cohort indicating that chronic low-level doses of radon do not statistically significantly elevate the risk of circulatory system disease. This work adds to the body of evidence on the health effects of occupational radiation exposure to support radiation protection regulations.
The study was funded by the Canadian Nuclear Safety Commission. We thank Dr. Toyib Olaniyan for his assistance with the record linkage of the cohort to Canadian national mortality data.
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By Paul J. Villeneuve; Howard I. Morrison; Karena Volesky and Rachel S. D. Lane
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