Radon exposure and lung cancer: risk in nonsmokers among cohort studies
© Oh et al. 2016
Received: 2 February 2016
Accepted: 3 March 2016
Published: 9 March 2016
Eleven cohorts of miners occupationally exposed to relatively high concentrations of radon showed a statistically significantly high risk of lung cancer, while three cohorts from the general population showed a relatively low concentration, but the results were not statistically significant. However, the risk of lung cancer tended to increase with increased radon exposure. The risk is likely to have been underestimated due to low statistical power. Therefore, additional well-designed studies on the risk of lung cancer in nonsmokers in the general population with relatively low concentrations of radon exposure are needed in the future.
In addition, country-specific preventive policies are needed in order to actively reduce radon exposure and lung cancer incidence in nonsmokers.
Radon is the second most common cause of lung cancer, and the most common cause in nonsmokers. Lung cancer has gradually been on the increase, especially in nonsmokers. To identify the cause of cancer in nonsmokers is very important because unlike some other types of cancer, early detection is difficult.
Epidemiological studies designed to assess human health risks from exposure to radon mainly consist of cohort mortality studies, residential case-control studies and ecological studies. The International Agency for Research on Cancer has declared radon to be a cause of lung cancer in humans, based on the results of experimental and epidemiological studies . Compelling evidence of radon-induced health effects in humans derives from numerous studies of underground miners, particularly uranium miners exposed beginning in the middle part of the twentieth century in the United States and several European countries. Although these cohort mortality studies typically involved rather crude estimates of radon exposure levels in the working environment and inherent uncertainty due to confounding factors such as smoking status and coexposure to known or suspected human carcinogens (diesel exhaust, arsenic and silica dust), the results nevertheless consistently demonstrate increased risk of lung cancer with increasing exposure to radon in the working environment. These results are consistent across the various individual studies of mining cohorts and with analyses of pooled data from multiple cohorts.
In this paper, we reviewed the risk of lung cancer from radon for nonsmokers by examining occupational cohorts of miners and the general population among all the studies that are found through Pubmed.
Studies of cohorts of radon-exposed miners
Yunnan, China 
Relative risk of lung cancer by smoking status and radon exposure 
Cumulative radon exposure (WLM)
> − 800
Among subjects with available data, 3 % of the lung cancer cases and 7 % of the noncases identified themselves as nonsmokers at the time of the survey. The RR of lung cancer increased with cumulative radon exposure (WLM) within nonsmokers. Smokers have a two to threefold excess risk of lung cancer compared to nonsmokers (data not shown).
West Bohemia, Czech Republic 
Lung cancer in miners according to smoking status 
Person-years at risk
Ratio of risk in smokers and nonsmokers
Observed (95 % CI)
Smoking history was obtained for only a portion of the miners (75 %). The observed lung cancer rate in the nonsmokers was compared with the expected cancer rate according to statistics on the male population in Czechoslovakia. The attributable annual lung cancer rate per 1 WLM in smokers was found to be 1.6 times higher than in nonsmokers. The ratio of the observed to expected lung cancer rate in nonsmokers was, however, considerably higher than in smokers.
Colorado Plateau, USA 
Standardized mortality ratios and standardized rate ratios by smoking status and cumulative radon progeny exposure category (lagged 5 years) for lung cancer among Colorado Plateau uranium miners, 1960–2005 
Cumulative exposure to radon progeny from uranium mining (WLM)
Trend slope, cases/WLM person-year
120– < 400
400– < 1000
> − 1000
4.5 × 10−6c
SMR (95 % CI)
SRR (95 % CI)
Nearly half (n = 34) of the lung cancer deaths among never-smokers occurred among American Indian miners. The standardized mortality ratio increased directly with WLM exposure level. The standardized rate ratios increased monotonically with WLM exposure for most never-smokers. Tests of trend were highly significant for never-smokers.
Ontario, Canada 
In this study, uranium miners were defined as men who either attended a chest clinic after 1954 and reported that they had worked for at least two weeks in a uranium mine in Ontario, or who were reported by a uranium mining company to have been exposed to short-lived radon progeny underground in a uranium mine in Ontario. In all 26,674 uranium miners including 1344 uranium mill workers were identified. 21,346 male uranium miners remained after exclusions.
About 20 % of the uranium miners in these surveys reported that they had never smoked. A logistic regression analysis of the smoking histories showed that an association between the proportion of uranium miners who never regularly smoked and the miner’s year of birth could be detected (X 2 24.2, p = 9 × 10−7). The results of the logistic regression analysis also indicated that the proportion of uranium miners who never regularly smoked increased 2 % for each 10-year increment in the year of birth (data not shown).
Newfoundland, Canada 
Relative risk of lung cancer and fitted models, underground Newfoundland fluorspar miners, by cumulative radon progeny exposure and smoking status 
Cumulative radon progeny exposure (WLM)
500– < 1500
1500– < 2500
Excess risk of lung cancer, per WLM, by smoking status in underground fluorspar miners of known smoking status, Newfoundland, 1950–1990 
Lung cancer deaths
95 % CI
Among nonsmokers, the RRs increased with increasing radon progeny exposure: 1.0, 4.8, 5.17 and 5.22. The ERR/WLM was 0.0025. This result was higher for current smokers than nonsmokers (p = 0.03). Attributable risk among never-smokers in this cohort was 0.65 ().
Malmberget, Sweden 
Results of cohort studies of risk estimates of lung cancer in underground miners from exposure to radon progeny 
Mean years of follow-up after start of work
Absolute risk coefficient/106 person-yr/WLM
Relative risk coefficient/WLM
Sweden iron, 1951–76
The relative risk coefficient for the nonsmokers was 0.107/WLM. This suggests that the dose required to double the risk of lung cancer is less than 10 WLM. Such a low value indicates that when a lag of 30 years is applied to calculations of effects of background doses of 0.1 WLM per year from radon indoors, a major proportion of the cases of lung cancer observed in nonsmokers among the general population may be accounted for by exposure to radon.
New Mexico, USA 
Relative risks for lung cancer by exposure to radon progeny, with and without adjustment for cigarette smoking, in a cohort of New Mexico underground uranium miners 
Number of cases
Unadjusted (95 % CI)
Adjusted (95 % CI)
The relative risk for ever smokers compared with never smokers was 3.6 (95 % CI 1.3-10.0). The relative risk values changed little with adjustment for smoking. However, the deviance for the model including smoking was significantly less than for the model without smoking, indicating that smoking was an important risk factor.
Eldorado Beaverlodge, Canada 
The Beaverlodge uranium mine began operation in 1949, commenced full production in 1953, and closed in 1982. The cohort consisted of all male former employees who had worked at the mine since 1948, together with males currently employed at the mine at the termination of the follow-up period (31 December 1980). The cohort, so defined, consisted of 10,945 individuals, after excluding the Beaverlodge cohort consisting of 8487 individuals, 77.5 % of those originally defined as eligible.
This study did not collect data on smoking.
Uranium mining began in France in 1946. The first mines, operated by the Commissariat a l’Energie Atomique (CEA), were in the Massif Central. The inclusion criteria are defined in terms of the period of first exposure and duration of exposure to radon and its decay products: this cohort includes all the uranium miners with a first experience of underground mining in the years 1946–1972 and with more than 2 years of underground mining.
This cohort was used to carry out a nested case-control study for lung cancer in order to examine the association of factors such as smoking.
Eldorado Port Radium, Canada 
The Port Radium uranium mine opened in 1930 and closed in 1960, with a brief closure between 1940 and 1942. The initial cohort consisted of all male workers employed at the mine since 1940 and who were known to be alive as of January 1, 1945. The final cohort study comprised 2103 workers employed between 1942 and 1960 at a uranium mine in the Northwest Territories, Canada.
This study did not collect data on smoking.
Radium Hill, Australia 
The Radium Hill mine was located in a remote area of eastern South Australia, and operated from 1952 to the end of 1961, producing uranium for export to Britain and the US. The mine was owned and operated by the South Australian Department of Mines. The study participants included 2574 persons employed at Radium Hill. Workers’ names, birthdates and job particulars (job type, starting date, stopping date) were abstracted from records kept by the South Australian Department of Mines. These records included only wage earners employed by the Department. The list did not include salaried employees (geologists, management and other professional staff) or contractors.
In this cohort, no risk for lung cancer was found among nonsmokers.
Estimated excess lifetime risk of radon-induced lung cancer death (REID) in males and females up to age 75 years from age 30, based on a lifetime exposure constant at various radon concentrations using various risk models, assuming a multiplicative model for radon and smoking 
Lifetime risk of lung cancer death from radon exposure at home (%)
Radon concentration (Bq/m3)
BEIR VI cohort miner model
European cohort miner model
Ex-smoker from age 50
Ex-smoker from age 50
Table 8 shows estimates of REID for a European population. These calculations are based on exposure from age 30 up to 75 years to a constant radon concentration of 20, 50, 80, 200, 400 or 600 Bq/m3 using cohort models. Risks are presented separately for males and females, and for continuing smokers, never-smokers and persons who stopped smoking by age 50.
The lifetime risk of radon-induced lung cancer death by age 75 years for a male never-smoker, assuming that this individual has lived from age 30 years in a home with a radon concentration of 50 Bq/m3 (the European long-term average), is estimated to be in the range 0.08–0.11 %, according to the risk model used. These estimates rise to 0.30–0.42 % for male never-smokers in homes with a radon concentration of 200 Bq/m3 and to 0.90–1.27 % at 400 Bq/m3.
Studies of residential radon cohorts
High-level occupational radon exposure is an established risk factor for lung cancer. Although a number of residential case-control studies have been published, few cohort studies have assessed the relationship between residential radon exposure and the development of lung cancer.
American Cancer Society Cohort 
Adjusted HRs (95 % CIs) for lung cancer mortality per 100 Bq/m3 mean county-level residential radon concentrations (LBL) at enrollment (1982) stratified by selected risk factors, effect modification multiplicative scale, follow-up 1982–1988, CPS-II cohort, United States 
Lung cancer deaths
Fully adjusted HR (95 % CI)
Age, race, gender and state stratified and adjusted for education, marital status, BMI, BMI squared, cigarette smoking status, cigarettes per day, cigarettes per day squared, duration of smoking, duration of smoking squared, age started smoking, passive smoking, vegetable/fruit/fiber consumption, fat consumption, industrial exposure and occupation dirtiness index where appropriate.
No significant effect modification was observed by cigarette smoking status.
In the present study, a number of risk factors for lung cancer were less prevalent among participants. This would result in an underestimation of the association between radon and lung cancer risk.
Danish Cohort 
Incidence rate ratio for lung cancer associated with the concentration of radon at the residence 
All residences, IRR (95 % CI)
Linear trend per 100 Bq/m 3
Adjusted incidence rate ratios for lung cancer in association with a 100 Bq/m3 increase in domestic radon within strata of sex, NOx at the residential address, and ETS 
Nonsmokers IRR (95 % CI)
NOx at front (ug/m3)
Among nonsmokers, the incidence rate ratio was 1.67 (95 % CI: 0.69–4.04) and the incidence rate ratio was dose-dependently higher over the four radon exposure quartiles.
There was no evidence that the association between radon and risk of lung cancer was modified by sex, traffic-related air pollution or environmental tobacco smoke.
This cohort showed an insignificant association between radon and risk for lung cancer with an associated convincing dose-response pattern over the four quartiles of radon exposure. The lack of a significant linear response amongst nonsmokers was surprising, but only 99 nonsmokers developed lung cancer and power constraints may explain this.
Spain cohort 
Between 1992 and 1994, 241 randomly selected controls were enrolled in a population-based case-control study on residential radon and lung cancer by using 1991 census data for the Santiago de Compostela Health District. Initially, 500 persons from the general population were selected through sex-stratified random sampling. Of these, 391 met the eligibility criteria and 241 were finally included. Cohort follow-up ended on 31 May 2007.
In this cohort, no risk for lung cancer among nonsmokers was found.
To date, cohort studies of miners with exposure at high concentrations of radon have shown increases the risk of lung cancer in nonsmokers. However, the risk is unclear at the relatively low concentration of radon exposure experienced by a few cohorts in residential settings. In the future, well-designed prospective cohort studies are needed.
This research is supported by Korea Ministry of Environment (MOE) as “the Environmental Health Action Program”. (Grant Number 2015001350002).
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