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Original article
Cancer incidence and mortality from exposure to radon progeny among Ontario uranium miners
  1. Garthika Navaranjan1,
  2. Colin Berriault1,
  3. Minh Do1,
  4. Paul J Villeneuve1,2,3,
  5. Paul A Demers1,3
  1. 1Occupational Cancer Research Centre, Cancer Care Ontario, Toronto, Ontario, Canada
  2. 2Department of Health Sciences, Carleton University, Ottawa, Ontario, Canada
  3. 3Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada
  1. Correspondence to Garthika Navaranjan, Occupational Cancer Research Centre, Cancer Care Ontario, 525 University Avenue, 3rd floor, Toronto, Ontario, Canada M5G 2L3; garthika.navaranjan{at}occupationalcancer.ca

Abstract

Objectives The study objectives were to extend the follow-up of the Ontario uranium miners cohort, one of the largest cohorts of uranium miners with low cumulative exposures, to examine the relationship between radon exposure and lung cancer mortality and, for the first time incidence, and address gaps in the literature, including dose–response relationship between radon exposure and other cancer sites, and non-cancer mortality.

Methods The cohort of mine and mill workers was created using data from Canada's National Dose Registry and the Ontario Mining Master File. The follow-up for the cohort was recently extended for mortality (1954–2007) and for the first time includes cancer incidence (1969–2005). The Poisson regression was used to estimate relative risks (RR) and excess relative risks (ERR) and their 95% CIs with levels of cumulative radon exposure.

Results The cohort consisted of 28 546 male miners with a mean cumulative radon exposure of 21.0 working level months (WLM). An increased risk of lung cancer and a dose–response relationship was observed with cumulative radon exposure. Miners exposed to >100 WLM demonstrated a twofold increase in the risk of lung cancer incidence (RR=1.89, CI 1.43 to 2.50) compared with the non-exposed group, and a linear ERR of 0.64/100 WLM (CI 0.43 to 0.85), with similar results observed for mortality. No association was observed for other cancer sites (stomach, leukaemia, kidney and extrathoracic airways) or non-cancer sites (cardiovascular diseases) with increasing cumulative exposure to radon.

Conclusions These findings suggest no increased risk of cancer sites other than lung or non-cancer mortality from relatively low cumulative exposure to radon.

  • uranium miners
  • lung cancer
  • cohort study

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What this paper adds

  • A number of studies have reported on associations between radon and lung cancer mortality among uranium miners; however, relatively few have examined associations with cancer incidence, and for sites other than lung, especially at low cumulative radon exposures.

  • The Ontario Uranium Miners’ Cohort, one of the largest cohorts of uranium miners with relatively low doses of radon exposure compared with other uranium miners, has the power to examine exposure–response relationships with radon exposure not previously examined.

  • Lung cancer risks from cumulative radon exposure remained elevated in this cohort with similar results seen for incidence and mortality, while no dose–response relationship was observed for leukaemia, stomach, kidney cancer or cancers of the extrathoracic airways or for cardiovascular disease mortality.

  • These findings suggest no increased risk of cancer sites other than lung or non-cancer mortality from relatively low cumulative exposure to radon. The low cumulative exposures experienced by Ontario uranium miners are comparable to exposure levels among present-day miners, and help inform current radiation protection practices.

Introduction

Radon is a radioactive gas released from the natural decay of uranium. Underground workers, in particular, underground uranium miners, are exposed to the highest concentrations through the inhalation of radon and its decay products. Cohort studies of uranium miners have long provided evidence for health effects associated with radon exposure, leading to the classification of radon-222 and its decay products as a lung carcinogen by the International Agency for Research on Cancer (IARC) in 1988.1

Studies of uranium miners to date have demonstrated strong evidence for an excess of lung cancer deaths compared with the general population, as well as a strong dose–response relationship with cumulative exposure to radon and lung cancer mortality.2–8 However, there is evidence from dosimetry studies that radon reaches other organs as well. One study observed that the kidney received the second highest dose of inhaled radon progeny outside of the respiratory tract, although an order of magnitude lower.9 Studies have also suggested that a non-negligible dose of α radiation is delivered to bone marrow from inhaled radon,10 ,11 and ingestion of water contaminated with radon can cause exposure to the stomach lining.12 This suggests a need to further explore the association between radon exposure among uranium miners and the risk of cancer at sites other than the lung. Epidemiological studies of uranium miners provide some evidence of an excess risk for other cancer sites, including stomach cancer,5 ,7 ,13 ,14 leukaemia15 and kidney cancer.4 However, these findings are largely based on comparisons of cancers observed in the cohort with rates in the general population. This approach for assessing risk is susceptible to biases, including the healthy worker effect that can diminish any true effects seen with these cancer sites.16 Therefore, internal cohort comparisons are needed to avoid healthy worker bias and to also provide insight into levels of radon exposure that may be relevant for these sites. With the exception of a few studies,15 ,17 these epidemiological studies of other cancers sites have also primarily examined mortality largely because of the ease of access to and availability of vital statistics compared with incidence data. However, incidence is important to examine for cancers with a good survival rate, such as kidney cancer, where many of the cancers would not be captured in death certificates and therefore missed in mortality studies. Incidence data also provide greater power compared with mortality since there are more incident than decedent cases and allows for a better examination of latency and histological subgroups. Further studies with a larger sample size are needed to better characterise the risk of cancer incidence associated with radon exposure over a broad range of exposure levels.

Uranium mining and milling in Ontario began in the mid-1950s and continued until 1996 with the closure of the last uranium mine.18 The Ontario uranium miners' cohort study was created to better understand the health effects associated with radon exposure following a 1974 report by Muller that observed an increased risk of lung cancer deaths among Ontario miners.19 Subsequent studies of this cohort have examined lung cancer mortality with the last follow-up from 1955 to 1986.8 However, cancer incidence has not been examined in this cohort. As one of the largest cohorts of uranium miners with extensive exposure data and over 20 years of additional follow-up, an update of this cohort also provides the opportunity to investigate several gaps in the literature, including the examination of dose–response relationships for radon exposure and cancer for sites other than the lung. This follow-up also extends beyond the closure of the last uranium mines in Ontario, capturing the entire work history of these miners.

The objectives of this study are to examine the dose–response relationship between radon exposure and cancer incidence and mortality, including analyses of cancers other than lung, and to examine radon exposure and non-cancer mortality.

Methods

Creation of the cohort

The present study uses the cohort of Ontario uranium miners created to assess ionising radiation exposure and congenital anomalies, and expanded for a study examining gastrointestinal cancers.20 ,21 The cohort was identified from Ontario's Mining Master File (MMF) and Canada's National Dose Registry (NDR).22 ,23 The Ontario MMF was created in 1928 as a result of the Ontario Silicosis Act,8 which required all miners in the province to undergo annual medical exams with chest X-rays to be certified as fit for underground work. The MMF has detailed work histories for each miner, including annual radon exposure information from 1954 to 1986. The inclusion criteria for this cohort were male miners from the MMF who worked in a uranium mine in Ontario between 1954 and 1986 for at least 2 weeks.20 To capture all miners employed in Ontario uranium mines up to the closure in 1996, miners were also identified from the NDR.

The NDR was created in 1951 and is a mandatory registry maintained by the Radiation Protection Bureau of Health Canada to monitor all workers with potential exposure to ionising radiation.22 The registry contains detailed radiation history records for workers beginning in the 1940s.22 Individuals from the NDR who had ever worked in an Ontario uranium mine with complete work history and radiation exposure information were included in this cohort. Some miners had continued employment in radiation exposed industries after the closure of the uranium mines in 1996 and therefore have work histories and radiation exposure records, which were included in our analysis, extending up to 2004, when data were extracted from the NDR for this study.

Workers with data quality issues such as missing data or invalid dates (n=1144), as well as duplicates, were excluded from the cohort (n=103). Miners who were too young to be employed (those with age at first employment younger than or equal to 15 (n=27) were excluded from this study. As well, a small number of miners who were recorded as being older than 65 years at start of employment were excluded (n=15) since these miners were not linked to a death record and contributed person-years beyond expected for their advanced age. Miners from the NDR without at least one uranium mining record were also excluded (n=600). Individuals hired after 1996, when the last mine in Ontario closed, were excluded (n=66) since these miners were likely to be involved with decommissioning of the mines, but were not true miners.

Exposure to radon decay products

Ontario uranium miners' exposure to radon decay products were estimated using stationary area sampling. In the early 1950s, annual average radon levels were estimated based on mine-specific extrapolations made by mining engineers.23 ,24 After 1958, measurements of radon decay products were taken by mine operators in different areas of the mines, including heading, stopes, raises and travelways,25 and individual exposure was estimated based on an approximate percentage of time spent in work areas versus travelways.26 From 1968, area sampling of radon decay products became more frequent across several different locations in the mine.20 These measurements were used with information on how much time the miner spent in different locations of the mine, collected from time cards filled out daily, to estimate individual exposure to radon.25 Annual radon doses were provided in the NDR for the period 1954 to 2004 and in the MMF from 1954 to 1986. Workers found only in the MMF had their radon doses taken from the MMF. Similarly, if a worker was found only in the NDR, then their radon doses were taken from the NDR. Where miners had doses in both sources for a given year, the NDR measurement was used as the preferred radon concentration, as NDR data tended to be more complete. Miner's annual cumulative exposure to radon was measured in working level months (WLM). Figure 1 presents the mean annual radon exposure of Ontario miners from 1954 to 1996. There was a significant drop in radon exposure in the late 1960s, which coincided with the introduction in 1967 of new ventilation requirements and radon exposure regulation by the Ontario Department of Mines.27 To examine the effects of radon exposure after significant reductions occurred in mines, miners who started employment after 1970 were also examined separately.

Figure 1

Male uranium miners mean annual radon exposure and employment 1954–1996.

Linkage and mortality ascertainment

The cohort file was first linked to the Historic Summary Tax File to verify and update personal identifiers in the work history records to aid with the linkage. Using personal identifiers, the cohort was linked to the Canadian Mortality Database for mortality ascertainment from 1954 to 2007 and to the Canadian Cancer Database for cancer incidence follow-up from 1969 to 2005. All linkages were performed by Statistics Canada using a probabilistic linking programme (Generalised Iterative Record Linkage System).28 Underlying causes of death were available for all miners and were coded according to the version of the International Classification of Diseases (ICD) that was in effect at the time of death. The different ICD versions used and corresponding codes for sites of interest are provided in online supplementary table S1. Incident cancer cases were coded using ICD-9 for diagnoses before 1992 and ICD-O-3 for diagnoses 1992 and onward. The linkages underwent manual review by Statistics Canada and Canadian Nuclear Safety Commission employees. When a link was not found, workers were assumed to be alive due to the completeness of the national mortality databases.

Supplementary table

Causes of death and associated ICD codes (revisions 6 through 10)

Statistical analyses

For incidence analyses, miners contributed person-years from the latest of 1 January 1969 or date of first employment until the earliest of date of death, 31 December 2005 or date of diagnosis for cancer of interest. Multiple cancer diagnoses were considered for each miner. For multiple primaries of the same cancer site, only the first primary was used for the dose–response analyses. For mortality analyses, miners contributed person-years at risk from the latest of 1 January 1954 (start of study period) or date of first employment until date of death or 31 December 2007, whichever occurred the earliest. We also applied an age cut-off of 85 years of age for end of follow-up to minimise any effect from loss to follow-up, while not losing too many cases.

Person-years at risk were cross-classified by attained age (>15–35, >35–45, >45–55, >55–65, >65 years), calendar period (1954–1975, 1976–1995, 1996+) and cumulative radon exposure (0, >0–1, >1–5, >5–10, >10–20, >20–30, >30–50, >50–100 and >100 WLM). Cumulative radon exposure was treated as a dynamic variable, with workers contributing person-years and event data to the cumulative exposure category they belonged to in a given year of follow-up. Categories for cumulative exposure were chosen to have an approximately equal distribution of lung cancer cases and sufficient numbers to provide reliable risk estimates. A similar approach was taken when choosing cumulative exposure categories for other cancer sites. To account for the latency between exposure and cancer outcome, a range of different lag periods (2, 5, 10, 15 and 20 years) were examined for each cancer outcome. The lag period that yielded the highest risk estimates was chosen to examine the most relevant exposure period and based on the principle that reduced non-differential misclassification should produce the strongest results.29 Since this approach for selecting lag may be susceptible to bias,30 the lag period was further validated by examining lag periods used in other studies examining radon exposure and based on the development of the specific cancer site.

Cancer incidence and mortality of this cohort was compared with that of the general Canadian population to provide a benchmark. National rates of cancer incidence and cause-specific mortality were obtained from the Public Health Agency of Canada by sex, 5-year age and 5-year calendar periods for the 1969–2007 period for cancer incidence and 1950–2009 for mortality. Standardised incidence and mortality ratios and their 95% CIs were calculated assuming cancers and deaths followed a Poisson distribution.31

In order to better understand dose–response relationships, internal cohort analyses were conducted using the Poisson regression to estimate relative risks (RR). The general equation for Poisson regression modelling is:

Embedded Image 1

Where λ represents the mortality/incidence rates for specific values of X1, X2, X3, …, Xj, λo represents the background or baseline mortality/incidence rate, X1–Xj represent the independent variables and β1–βj represent the regression coefficients to be predicted from the model, which represent the effect of the predictor variable. To examine WLM as a continuous parameter, the linear excess relative risk (ERR) model was used. This model RR=1+βX1, where β represents the increase in the ERR per unit increase in cumulative exposure (X1), assumes a linear relationship between cumulative radon exposure and risk. All models were adjusted for the calendar period and attained age. Groupings for the calendar period and attained age were collapsed for analyses where model convergence could not be reached. Wald-based 95% CIs were calculated for all risk estimates. All Poisson regression modelling was conducted using the AMFIT module in EPICURE.32

Results

There were 30 914 uranium workers identified from the NDR and MMF. After exclusions, the final cohort included 28 546 male miners and 413 female mine employees. Owing to the small number of female miners, they were not included in the dose–response analyses, but were in the external analyses comparing cancer in the cohort with the Canadian population. Table 1 provides an overview of the characteristics of this cohort. The mean age at entry into the study was 28.8 years for male miners and 27.9 years for female workers. The mean cumulative exposure was 21.0 WLM for male miners and 0.2 for female workers over an average of 5.3 and 5.9 years of total employment, respectively. About one-third of male miners also had experience mining gold (32%) and copper/nickel (37%) in Ontario, with remaining experiences accounting for <5% per ore mined. Other uranium experience consisted of 6% mining uranium outside of Ontario and 5% had uranium milling experience. Female miners had no uranium mining experience outside of Ontario and <2% had additional experience working in uranium mills and in other ores.

Table 1

Characteristics of the Ontario uranium miners cohort

Between 1969 and 2005, there were 3976 incident malignant cancers (excluding non-melanoma skin cancers) including 1291 lung cancers observed among male miners. Between 1954 and 2007, 8318 deaths, including 2734 malignant cancer deaths (1230 due to lung cancer), were observed among men. For female mine workers, there were 19 incident cancers and a total of 18 deaths observed, including 7 from all cancers. Table 2 provides an overview of cancer incidence, and mortality of uranium miners compared with the Canadian population for men. There was a deficit in cancer incidence observed among male uranium miners compared with the Canadian population (SIR=0.79, CI 0.77 to 0.82). In comparison, there was no deficit in the overall cancer mortality (SMR=0.99, CI 0.96 to 1.03). For lung cancer, similar excesses were observed for incidence and mortality (SIR=1.30, CI 1.23 to 1.37; SMR=1.34, CI 1.27 to 1.42). Other cancers observed to be increased in previous studies of uranium miners, including stomach cancer and leukaemia, were not significantly different from the general population or displayed a significant deficit. For female mine employees (results not presented), there were no excesses observed for cancer incidence (SIR=0.75, CI 0.45 to 1.17), or mortality (SMR=0.73, CI 0.29 to 1.50). There was a small, non-significant excess (SIR=1.20, CI 0.24 to 3.52) observed for female lung cancer incidence, whereas lung cancer mortality (SMR=0.90, CI 0.11 to 3.25) did not differ from the general population. However, observed death and incident cancer counts were too small to provide stable estimates for specific cancer sites.

Table 2

Cancer incidence (1969–2005) and mortality (1954–2007) of male Ontario uranium miners compared with the Canadian male population

Table 3 provides an overview of the association between lung cancer risk by level of cumulative radon exposure. There were 2073 unexposed workers with no cumulative radon exposure. A 5-year lag period was applied to cumulative radon exposure to account for the latency between radon exposure and lung cancer incidence, as well as mortality, because it yielded somewhat stronger results, although varying lag periods yielded similar results. Overall, a positive dose–response relationship was observed with lung cancer incidence and mortality. There was just under a twofold increase in the risk of lung cancer incidence in the highest cumulative exposure category (>100 WLM) (RR=1.89, CI 1.43 to 2.50) and over a twofold increase in the risk of lung cancer mortality (RR=2.32, CI 1.72 to 3.14) compared with the unexposed group. A small peak in risk was also observed at very low doses (>0–1WLM) for lung cancer mortality (RR=1.43, CI 1.04 to 1.95). Lung cancer risks among miners employed during the lowest exposure period after 1970 were similar to the full cohort for the categories that could be examined (results not presented).

Table 3

Lung cancer incidence and mortality by cumulative exposure to radon progeny in working level months (WLM)* among Ontario male miners

Similarly, a statistically significant increase in risk was also observed using the linear ERR model. The ERR estimate was 0.64/100 WLM (CI 0.43 to 0.85) for incidence and was similar for mortality (ERR=0.66/100 WLM, CI 0.44 to 0.87), with a 5-year lag applied. In comparing results, it should be noted that the period of follow-up for mortality (1954–2007) differs from cancer incidence (1969–2005).

Dose–response analyses were also conducted to examine incidence, as well as mortality for other suspected cancer sites, including stomach and kidney cancer, cancers of the extrathoracic airways as well as leukaemia (table 4). Overall, there was no clear dose–response or increased risks observed for stomach cancer, kidney cancer or leukaemia. With no lag applied, RRs in the highest exposure category were null for all other cancer sites. The corresponding ERR also suggested no increased risk for any of the cancer sites with cumulative radon exposure. When examining subtype of leukaemia, there were no increased risks observed for chronic lymphocytic leukaemia (CLL) or for leukaemia excluding CLL (table 4). Lagging the cumulative exposure yielded similar results with no increased risks observed.

Table 4

Cancer incidence and mortality for sites other than lung by cumulative exposure to radon progeny in working level months (WLM) among Ontario male miners

In examining non-cancer mortality, there was no dose–response relationship observed with cardiovascular disease mortality. Similar to other cancer sites, there was also no increased risk observed in any of the exposure categories, including the highest exposure category >50 WLM (RR=1.10, CI 0.94 to 1.29; ERR=0.065/100WLM, CI −0.041 to 0.17), with a 10-year lag applied. There were also no dose–response relationships observed for cerebrovascular disease (ERR=0.22/100 WLM, CI −0.12 to 0.58) and ischaemic heart disease (ERR=0.044/100 WLM, CI −0.080 to 0.17) with a 10-year lag applied.

Discussion

This is the first follow-up of this cohort using tumour registry records and results based on cancer incidence produced similar results to mortality. This included an excess of lung cancer incidence and similar to previous updates, an excess of lung cancer mortality.8 ,19 ,23 ,25 In the most recent previous update (1955–1986) by Kusiak et al,8 when examining the entire cohort, this yields an SMR of 1.71 (95% CI 1.52 to 1.91) for lung cancer. While our excess for lung cancer mortality was smaller compared with past updates, this is expected, given the substantial extension of follow-up in this update, which now extends far past the period prior to 1970 when the exposures were much higher. A positive dose–response relationship was observed for lung cancer incidence and mortality, especially among miners with >50 WLM of cumulative radon exposure. The ERR per 100 WLM was 0.64 (95% CI 0.43 to 0.85) for lung cancer incidence and 0.66 (95% CI 0.44 to 0.87) for lung cancer mortality. A past update of this cohort with follow-up to 1977 observed an ERR per 100 WLM of 1.50 for lung cancer mortality.23 A recent study by Kreuzer et al33 also examined the risk of lung cancer mortality from low radon exposure rates among a subcohort of miners hired in 1960 or later and observed an ERR/100 WLM of 1.30 (95% CI 0.70 to 2.10). In reviewing other studies that have examined low-dose radon exposure, Kreuzer et al observed that the ERR/100 WLM estimates from these studies ranged from 0.40 to 4.20, which is consistent with our mortality estimate of 0.66 WLM/100 WLM. The longer follow-up in this update provides a more complete assessment of the risk of miners employed during the earliest period, when exposures were the highest in Ontario uranium mines.

Cancer incidence and mortality in the cohort for cancer sites other than lung, including overall mortality and incidence, was lower than that for the Canadian population. This may be due to the healthy worker effect, although its impact is likely to be stronger for non-malignant diseases.34 The healthy worker effect is likely to be more pronounced in this cohort due to the fact that the majority of miners were required to undergo a certification for underground work, including an annual physical and lung function test.23

In this study, there was no association observed with cumulative radon exposure and incidence, or mortality, of cancers of the stomach, kidney and leukaemia. Only a few other studies have investigated the dose–response relationship between radon and cancers other than lung. A recent review of the German uranium miners cohort studies, which examined radon exposure and mortality from cancers other than lung, noted a statistically significant excess of stomach cancer (ERR/100 WLM=0.022; 95% CI 0.001 to 0.042), but no increase in risk for kidney cancer (ERR/100 WLM=0.017; 95% CI −0.023 to 0.058), leukaemia (ERR/100 WLM=0.005; 95% CI −0.034 to 0.045) or other major cancer sites.7 A study of Czech uranium miners examined the incidence of haematopoietic malignancies. The study observed an increased incidence of all leukaemias (RR=1.75, 95% CI 1.10 to 2.78) and separately CLL (RR=1.98, 95% CI 1.10 to 3.59) among miners with cumulative radon exposure of 110 WLM compared with 3 WLM. Excesses were observed for Hodgkin lymphoma and myeloid leukaemia; however, these were not statistically significant.15 Based on dosimetry studies, the evidence for stomach cancer comes largely from ingestion of water containing high concentrations of radon, which is water-soluble. Once ingested, the radon is held in the stomach for several minutes before being passed out of the body.12 For leukaemia, studies have suggested that a non-negligible dose of α radiation is delivered to bone marrow from inhaled radon.10 ,11 Owing to its solubility in fat, radon gas may be taken up by bone marrow fat cells and emitted to neighbouring cells over time.35 Although this provides evidence that there may be an increased risk among uranium miners, to date, the evidence comes from studies of ionising radiation exposure. Also, in this study, we did not attempt to estimate bone marrow doses and instead used the concentration of radon progeny in the air, expressed as WLM.

We also observed no association with cumulative exposure and cardiovascular disease mortality. This is consistent with other studies of uranium miners.2 ,36 ,37 Of the previous cohort studies of uranium miners, only the French cohort observed an association between cumulative radon exposure and cerebrovascular disease (ERR/100 WLM=0.41, 95% CI 0.04 to 1.03).4

There are several strengths to the present update of the Ontario uranium miners cohort. This is one of the largest cohorts of uranium miners in the world.24 The cohort size was increased in this update with the use of two sources of data to identify miners, the NDR and the MMF, while past updates only used the MMF. Also, with the follow-up extended by over two decades, this resulted in a greater number of cases and thus more power to detect any true associations. Since Ontario miners have historically been known to have exposure to relatively low doses of radon compared with other cohorts,24 the large size provided enough power to examine a broad range of low-dose radon exposure that can apply to many different exposure scenarios. The large sample size also allowed for an examination of the dose–response relationship with cancers other than lung. The Ontario cohort has also been known to have high-quality exposure assessment.18 ,24 The additional use of the NDR exposure data with this update increases the validity of the exposure assignment by supplementing missing exposure data, as well as extending the availability of exposure data past 1986 to cover the entire period of exposure for uranium mining in Ontario. Another strength of this cohort is the national linkage for mortality and cancer incidence, which allowed for the identification of more incident cancers among miners who may have left the province after employment. According to the North American Association of Central Cancer Registries (NAACR), case ascertainment from the Canadian provincial registries are said to be 90–95% complete.3 Similarly, mortality coverage is near complete due to compulsory registration in Canada. Evaluations of vital ascertainment of cohorts linked to the Canadian Mortality Database have estimated accuracies of 97.6–98.2% for deaths and 99.8–100% for living participants.38 ,39 This update also provided enough follow-up to truly capture effects experienced by miners in the early period, when exposures were the highest in Ontario mines, and allowed for an initial assessment of miners employed much later, during periods of lower exposure. The last major strength of this cohort was the examination of cancer incidence, which allowed for a complete examination of cancer sites with good survival such as kidney cancer.

Underground uranium miners also have the potential for exposures to other carcinogens, which could not be accounted for in the present study. These include crystalline silica, diesel engine exhaust and arsenic.24 For instance, there were 47 deaths of silicosis among uranium miners in the Ontario cohort, which highlights silica as an important confounder. Exposure to these carcinogens could explain the peak in lung cancer mortality observed in the low cumulative radon exposure category (>0–1 WLM). Work is underway to construct a database to examine historical mining exposures in Ontario, which may be able to account for potential confounders and effect modifiers in future work with this cohort. Exposure to γ radiation serves as another important cofounder in underground uranium mines. There are currently limited data available on γ exposure from the NDR starting in 1981; however, work is underway to develop a model to estimate γ exposure over the entire work history for these miners. This work may provide more insight into the effects of exposure to γ radiation. Another important confounder and effect modifier for lung cancer that the present study did not have data on was smoking. Although smoking data were not available in the present update, a case–control study of lung cancer cases in the Ontario cohort found a possible multiplicative interaction between smoking and radon exposure.25 A study by Kusiak et al,8 which combined data from surveys and medical examinations from 1974 to 1991 for 4971 cohort members, determined there was an 80% prevalence of cohort members having been regular cigarette smokers. However, there was no association observed between the proportion of smokers and cumulative RDP exposure. In this study, other diseases known to be related to tobacco use were not increased in comparison to the Canadian population, including circulatory diseases overall and in most circumstances non-malignant respiratory disease, excluding occupationally related pneumoconiosis.

Historically, as seen in Ontario with the first Muller report on uranium miners,19 these studies have provided invaluable information to inform and improve occupational exposure conditions. Studies of uranium miners have also been valuable for estimating risks associated with residential radon exposure by extrapolating models to low levels experienced in homes.40 This update builds on past work and addresses several gaps in the literature on uranium miners. This includes the characterisation of cancer incidence from radon exposure and a more indepth examination of cancer sites other than lung suspected of being associated with long-term radon exposure. As one of the largest cohorts of uranium miners, Ontario miners can provide valuable information about the effects of low-dose radon exposure, which may be comparable to exposure levels among present-day miners. This study can also help inform current radiation protection practices, including occupational exposure limits set in Canadian uranium mines by assessing the effectiveness of the current exposure limit of 20 mSv annually, which is roughly equivalent to the exposure limit of 4 WLM annually used in the Ontario uranium mining sector. The dose–response results also provide information on the level of radon exposure that may be relevant for lung cancer compensation. This work also highlights the need for consistent monitoring of underground uranium miners.

Acknowledgments

The authors would like to acknowledge Loraine Marrett, John McLaughlin and Sang-Myong Nahm for their involvement in the development of the cohort and initiation of this project. Thanks are also due to the staff at the Canadian Nuclear Safety Commission (Rachel Lane, Pascale Reinhardt, Patsy Thompson, Adelene Gaw and Lee Casterton) for their contribution to the manual resolution of record linkages, scientific comments and suggestions. Special thanks are due to Robert Semenciw of the Public Health Agency of Canada who assisted with Canadian mortality and cancer incidence rates and to Douglas Chambers for his valuable insights and suggestions.

References

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Footnotes

  • Funding This study was funded by the Canadian Nuclear Safety Commission. The Occupational Cancer Research Centre is also supported by the Canadian Cancer Society and the Ontario Ministry of Labour.

  • Competing interests None declared.

  • Ethics approval Approval for this study was obtained from Health Canada's Research Ethics Board (REB 2007–0015), and data access agreements from Ontario Workplace Safety and Insurance Board (WSIB) and Health Canada for the use of the MMF and the NDR, respectively. Ethics approval was received from the University of Toronto to conduct the analyses.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Data sharing statement No additional data are available.

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