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Is the radon risk overestimated? Neglected doses in the estimation of the risk of lung cancer in uranium underground miners. Philippe Duport, Ph.D. International Centre for Low Dose Radiation Research, Institute of the Environment, University of Ottawa, PO Box 450, Stn A, Ottawa, Canada K1N 6N5 Radiation Protection Dosimetry, March 2002 |
AbstractOnly the exposure to inhaled radon decay products is usually taken into account in the determination of the risk of radiogenic lung cancer in uranium miners. However, the elevated lung cancer risk in uranium miners is due to the total dose of radiation received by that organ, not to the dose from inhaled Radon-222 decay products (222Rn D.P.) alone. Lung doses from sources other than 222Rn D.P. may reach 25% to 75% of total effective dose, absorbed dose or equivalent lung dose, are correlated to 222Rn D.P. doses and are quite variable between facilities. Therefore, to neglect these doses leads to a systematic overestimation of the risk of lung cancer per unit 222Rn D.P. exposure, both through dose underestimation and dose misclassification. Correction for neglected doses and dose misclassification would pull the risk per unit radon exposure downward by a factor of at least two or three and bring the overall dose-effect relationship towards the no-effect null hypothesis, thereby increasing the likelihood of thresholds for lung cancer risk at indoor and today’s uranium mine exposures. Keywords: Radon, uranium mines, effective dose, lung dose, equivalent dose, risk coefficient. Introduction A comprehensive analysis of the risk of lung cancer in eleven cohorts of underground miners exposed to 222Rn decay products (222Rn D.P.) has been published by Lubin et al.(1). Eight of the eleven cohorts worked in Australian, Canadian, Czech, French and US uranium mines(2-9). Lubin et al. provide a summary of 222Rn D.P. measurements and of “other mine” exposures, which are comprised of exposures to arsenic, nickel and silica at the workplace, and during employment at other hard rock mines. They also provide corrections of the Excess Relative Risk per unit exposure of 222Rn D.P. (Excess Relative Risk per Working Level Month or ERR/WLM) for those miner cohorts with documented non-radiation exposures or years of work at other mines, but not for doses from radiation sources other than inhaled 222Rn D.P., to which miners are exposed simultaneously. The BEIR VI Report(10) also mentions exposures to carcinogens such as tobacco smoke and arsenic but not to radiation from sources other than 222Rn D.P. Historically, the risk of lung cancer in uranium mines has been attributed to inhaled 222Rn D.P. alone because doses from other sources of radiation were deemed negligible (ICRP 65, par. A.12 (11)). However, at all workplaces in a uranium mine the ore is either broken, hauled or crushed and it is virtually impossible to be exposed to 222Rn D.P. and not to the other sources of radiation, including thoron progeny when thorium is present in significant quantities in the ore. In the summary of collective exposures received in uranium mines, the 1993 UNSCEAR Report(12) reveals that individual doses from each source of radiation have not been consistently monitored or estimated in different countries and facilities and there is no indication of individual doses from sources other than 222Rn D.P. in uranium miner epidemiological studies (2-9). For example, at the Elliot Lake mines in Canada, individual gamma dosimetry was not performed before 1981(13) and airborne long-lived radioactive dust (LLRD) as well as 220Rn decay products (220Rn D.P.) were not monitored. The 1993 UNSCEAR Report(12) indicates that the totality of the effective dose received by uranium miners in the USA is due to inhaled 222Rn D.P. when Harley et al.(14) suggest that the absorbed annual doses from LLRD and 222Rn D.P. may be comparable in two US uranium mines. Exposures to sources other than 222Rn D.P. were not monitored in the mines subject to epidemiological studies, at the exception of French uranium mines in which individual doses from all sources were monitored and recorded. Therefore, doses from radiation sources other than 222Rn D.P. could not have been taken into consideration in epidemiological studies of radon-induced lung cancer and it is important to assess to what extent neglecting these doses might have affected the estimation of lung cancer risk due to inhaled 222Rn D.P. The bias in risk estimation due neglected doses should not be a concern in non-uranium mines in which 222Rn D.P. are deemed to be the only source of ionizing radiation, unless dissolved 226Ra and long-lived 222Rn D.P. were present in the mine water and inhaled in the form of ultrafine particles after the evaporation of water droplets. Such airborne long-lived alpha emitters cannot be detected in routine WL measurements based on gross alpha counting because their contribution to the filter total alpha activity in the few minutes after the end of sampling would be negligible. That question does not seem to have been investigated. Some authors have discussed the influence of errors in exposure data on risk estimates (for example Hornung and Meinhardt(15)), but neglected gamma and LLRD doses were not considered among the possible sources of error. Furthermore, the lung seems to be the only organ at risk of radiogenic cancer in miners exposed to 222Rn D.P. (Table 1 and (3, 6-8, 10, 16-18)). Among cancers other than lung, the increased cancer risk in cancer of the liver observed in French uranium miners(8) or that of the mouth and buccal cavity in Czech uranium miners(7) can probably be attributed to particular lifestyles (alcohol consumption, smoking or both). The risk of radiogenic cancer in any organ is, in theory, linearly proportional to the dose received by that organ(19). Therefore, the overall risk of lung cancer in uranium miners is proportional to the total lung dose and not to the dose from 222Rn D.P. alone. However, the discrepancy between epidemiological observations and dosimetric predictions led the ICRP to renounce using a dosimetric approach and to recommend a “conversion convention factor” based on epidemiological considerations, not on dosimetry, to relate 222Rn D.P. exposures and lung cancer risk(11). Nevertheless, whatever the definition of dose used in risk calculations, neglecting doses from sources other than 222Rn D.P. would affect only the apportionment of excess cancer cases according to the contribution of each radiation source to the dose, not the excess relative risk per unit exposure (ERR/WLM) if the doses from different sources were not correlated. This would not be true, and the ERR/WLM would be overestimated if they were correlated. Materials and methods Dosimetry data used to estimate lung doses from each source of radiation In order to compare, with the best possible confidence, the contribution of each radiation source to the total effective dose, to the absorbed dose and to the equivalent lung dose the dosimetry data used for the present comparison were obtained with the same instrument, a personal dosimeter (called Personal Alpha Dosimeter, or PAD) especially developed for monitoring individual exposures to each source of radiation present in uranium mines(20). The PAD contains a thermo-luminescent dosimeter for gamma radiation. It samples, continuously, the air at the belt of the worker and measures directly time-integrated exposures to 222Rn D.P., 220Rn D.P., LLRD and gamma radiation. It was used by all underground personnel in a French uranium mine beginning in 1976. Its use became mandatory for all underground personnel in all French uranium mines in 1982(21). In Elliot Lake mines, the same PAD was used to measure exposure to 222Rn D.P., airborne radioactive dust and thoron progeny(22) on a subset of underground personnel. Separate thermo-luminescent dosimeters were used to measure exposures to gamma radiation(13, 22). Personal, time-integrated, simultaneous measurements of 222Rn D.P., 220Rn D.P., LLRD and gamma exposures are subject to instrumental errors such as flow rate fluctuation and to statistical counting uncertainties. A critique sometimes addressed to PADs is that they measure airborne radioactivity at the belt level and not in the breathing zone. That critique is not valid because the settling velocity of submicron particles (carrying 222Rn D.P.) is of the order of 10-7 m/s and that of inhalable ore dust particles (typically 0.5 to 5.0 mm in diameter) less than 10-3 m/s(23). Such low settling velocities cannot affect the homogeneity of aerosol concentration in highly turbulent (Reynolds number approximately 105 to 106) air flow at the workplace, with air velocities often exceeding 1 m/s(24). Conversely, grab sampling measurements, the common practice in radiation monitoring in mines are, in addition to conventional instrumental and counting errors, subject to uncertainties due to their short duration – a few minutes – and their usually low frequency – once per week or month, or less, which call for the assumption that each measurement is representative of the entire period between consecutive samples. To illustrate the variability of instantaneous WL values in an active stope, variations by a factor of 5 were observed during a field calibration of PADs in their earlier stage of development. These variations were not random but followed clear temporal patterns(25). Piechowski et al. have shown that even individual exposures to 222Rn D.P. based on daily grab sampling of radon are not strongly correlated or even not correlated at all to exposures measured, simultaneously, with continuous personal samplers(26). Still in French uranium mines, Pradel et al. (27) identified seventeen sources of error in grab sampling dosimetry; four of them tend to increase the standard deviation in individual exposures whereas thirteen would lead to an underestimation of 222Rn D.P. exposures. Contribution of each source of radiation to the equivalent dose to the lung, HT According to the ICRP definitions(19) the equivalent lung dose from each source of radiation is obtained by
where Ei is the effective dose from source i (i = 222Rn progeny, 220Rn progeny, LLRD, gamma radiation); HT,i is the equivalent dose to the lung from source i in tissue T wT the tissue weighting factor (wT = 0.12 for the lung); and E,
the total effective dose, is given by
(since the lung is the organ of interest here, wT refers to weighting factor for the lung and HT to the lung equivalent dose in the remainder of the text
The total equivalent dose to the lung is
Equivalent lung dose from inhaled 222Rn progeny, HT, Rn-222 Equivalent lung doses from 222Rn D.P. were calculated from the effective doses reported for the populations examined here. At the time dosimetry data were collected in the Elliot Lake uranium mines, the regulatory annual limit on exposure to 222Rn D.P. was 4 WLM, deemed to be equivalent to an effective dose of 50 mSv (1 WLM º 12.5 mSv). In French uranium mines, the annual limit on intake was 20 mJ, also deemed to be equivalent to 50 mSv and to 4,7 WLM (1 WLM º 10.7 mSv). These values are comparable to the value of 15 mSv/WLM found by Birchall and James from rigorous dosimetric calculations(28). No attempt was made to standardize effective and equivalent doses at French and Elliot Lake mines, but standardizing them would alter the conclusions only by the difference between the mSv/WLM conversion factors used in each country. In comparison, the ICRP gives a conversion convention factor for the effective dose
E = 5.06 mSv per WLM(11), or
Equivalent lung dose from inhaled 220Rn progeny, HT, Rn-220 The equivalent dose per unit exposure of 220Rn D.P. is taken as one third of that of 222Rn, that is, 37.5 mSv/WLM of 222Rn D.P.(29).Equivalent lung dose from inhaled long-lived radioactive dust, HLLRD The equivalent lung dose from inhaled LLRD is the effective LLRD dose divided by the tissue weighting factor for the lung (wT = 0.12). Equivalent lung dose from gamma radiation, HT, gPersonal gamma dosimeters (thermoluminescent in Canada, photographic in the early years of French mining followed by TLDs in the 1980’s) were used to measure the external dose incurred by the lung.Absorbed, effective and equivalent dose received by lung tissues in uranium mines for different values of the weighting factor for alpha radiation, wRThe contribution of each a-emitting radiation source to the absorbed dose to the lung, DT, was calculated as The effective dose to the lung, HT, was calculated according to
Radiation weighting factors different from the value of 20 recommended by the ICRP are also used because the literature offers many examples suggesting that wR for alpha radiation may be lower than 20, particularly at low doses and dose rates. For example, in humans, an apparent threshold at about 2 Gy has been observed by Andersson et al. in patients injected with Thorotrast®(30). Evans et al.(31) and Rowlands(32, 33) indicate the existence of “practical” thresholds at about 10 Gy for internally deposited 226Ra in dial painters. In animals, Sanders observed thresholds in rats after inhalation of 239PuO2(34) and Monchaux et al. have shown that a low dose of 222Rn D.P. delivered at a relatively high dose rate (25 WLM (0.35 J.h.m-3) at a concentration of 100 WL (2.08 J.m-3)) significantly increases the risk of lung cancer in rats, whereas the same low dose delivered at a much lower dose rate (2 WL or 4.16 10-2 J.m-3) does not increase the risk and may even reduce it(35). Birchall and James(28) cite a RBE value of 12 for alpha particles, relative to X rays, for mutations induced by 222Rn D.P. in cells irradiated in vitro and indicate that wR may be different for different tissues and different types of cancer. Studies of RBE for cell survival give RBE values between 2.2 and 3.8, about one seventh of the ICRP recommended value(36, 37). These observations seem to indicate that the carcinogenic effectiveness of internally deposited alpha emitters is reduced at low doses and dose rates. Since the tissue weighting factor, wT, is fixed and based on the contribution of each organ to the total radiological detriment(19), the reduced carcinogenic effectiveness of low doses of alpha radiation can only be expressed by a reduction of the radiation weighting factor, wR. Therefore, HT values were also calculated using a radiation weighting factor wR = 3, 7 and 12, in addition to conventional HT values calculated with wR = 20. Absorbed and equivalent lung doses were calculated using equations 1, 2 and 3. Contribution of each radiation source to the effective and equivalent dose in Elliot Lake mines In a pilot project, PADs were given to a subset (about 10% of the workforce on two mines) of the Elliot Lake (Canada) underground miners(22). Worker’s participation in the project was voluntary and compliance was not perfect. However, thirty-seven sets of annual doses and one hundred forty eight sets of quarterly doses from each source of radiation were collected. These data indicate that doses from 222Rn D.P. constitute only about 55% of the total effective dose received by these workers, whereas LLRD, 220Rn D.P., LLRD and gamma radiation contribute 10%, 10%, and 26%, respectively. 222Rn D.P. contribute 40% of the absorbed dose in the lung and 55 t0 70% of the equivalent lung dose, depending on the value attributed to wR (Table 2). Correlation between doses from each radiation source in Elliot Lake mines The correlation coefficients between individual doses from gamma radiation, inhaled ore dust, and 220Rn D.P. doses vs 222Rn D.P. doses for the Elliot Lake miners(22) are as follows:
Gamma radiation vs 222Rn D.P. R=0.275 Inhaled ore dust vs 222Rn D.P. R=0.460 220Rn progeny vs 222Rn D.P. R=0.953
More recent information indicates a correlation coefficient of 0.58 between individual gamma doses and individual exposures to 222Rn progeny (calculated from grab sample WL measurements and time sheets) in 1983 at one of the Elliot Lake mines(38). At the time of the personal monitoring project, measuring exposures to 220Rn D.P. and LLRD was not mandatory in the Elliot Lake uranium mines, which have since been shut down. Radon and ore dust exposures prior to forced ventilation Prior to the introduction of forced ventilation at the Elliot Lake mines the source of “fresh air” at the face was compressed air released by drilling equipment and sometimes compressed air released through a “cracked open” valve. A reconstitution, in a production stope, of the environmental and radiological conditions that prevailed at the workplace under such conditions indicate that compressed air had some efficiency at controlling the concentration of 222Rn D.P. at levels below what they would have been without ventilation at all, but was less effective at removing the LLRD(39). Before the installation of forced ventilation the concentration of 222Rn D.P. at the face was about twice what it was with forced ventilation; the concentration of airborne LLRD was 4.5 to 7.5 times higher. Therefore, the contribution of LLRD to the effective dose, relative to that of 222Rn D.P. was about 2 or 3 times higher than under forced ventilation. The ore grade was fairly homogenous in the Elliot Lake mines and the dose from gamma radiation relatively homogenous throughout the mines. During the limited PAD program and under forced ventilation, 222Rn, 220Rn, LLRD and gamma radiation contributed about 54%, 10%, 10%, and 25%, respectively, to the total effective dose (Table 2). Before the introduction of forced ventilation, these respective contributions would have been about 45%, 10%, 20%, and 25%. Contribution of each radiation source to the effective and equivalent dose in French mines As shown in Table 3, the contribution of 222Rn D.P. contribute from 34 to 67% of the effective dose, from 25 to 57% of the absorbed lung dose and from 36 to 74% of the equivalent lung dose, depending on the mine and value attributed to wR . In these mines, it is obvious that 222Rn D.P. exposure is not a reliable surrogate to the effective dose or the absorbed and equivalent lung doses received by the miners. Correlation between doses from each radiation source in French uranium mines The analysis of one year (1988) of personal dosimetry data for all the French uranium miners (about 950 persons) in the three uranium mining Districts(40) reveals good correlations between effective doses from 222Rn D.P. and effective doses from the gamma radiation and inhaled uranium ore dust (example in Figure 1; similar graphs (not shown) are obtained for the correlation between LLRD and 222Rn D.P. doses and for gamma and 222Rn D.P. doses in all three French uranium mining Districts). The slopes of linear fits between annual 222Rn D.P. doses and doses from other sources and corresponding correlation coefficients are given, for each mining District, in Table 4. It is worth noting that the slopes of linear fits between individual 222Rn D.P. doses and doses from other sources are about 10 times higher in District 3 than in Districts 1 and 2. A scatter plot of annual individual gamma doses vs 222Rn D.P. doses for the three mining Districts together (Figure 2) clearly shows that the contribution of each radiation source relative to that of 222Rn D.P. is very different between Districts and that annual individual doses belong to very distinct distributions in different mining Districts. Uncertainty in lung dosimetry in uranium mines When discussing the relationship between radon exposure and lung cancer risk, it might be helpful to recall briefly the sources and magnitude of the error that affect radon dosimetry. The point is complex because the equivalent dose is derived from only one measured value, the concentration of potential alpha energy in air (WL), and a series of assumed parameters (occupancy time (except when PADs are used), radioactive equilibrium, aerosol characteristics and unattached fraction, breathing pattern and rate, aerosol deposition in the respiratory tract, distribution of target cells, etc.). Uncertainties in WL measurements may reach about 20%, for example (28, 29) whereas the overall uncertainty in dose per unit intake due the combined uncertainties in every assumed parameter may be many-fold, as illustrated by the ICRP recommendation to use a conversion convention factor based on detriment rather than on dosimetry(11). Discussion It is impossible that underground uranium miners be exposed to 222Rn D.P. and not to the other sources of radiation. Also, the characteristics of the ore body as well as mining and protection techniques have evolved over time in all mines. Dry drilling was used in the early years of uranium mining, resulting in high concentration of airborne ore dust at the workplace. Forced ventilation was introduced progressively in the 1950’s. In the early years of uranium mining, pieces of uranium-rich pitchblende were sometimes handpicked, a practice leading to high exposures of gamma radiation. In the Elliot Lake mines, after the introduction of forced ventilation, PAD data indicate that 222Rn D.P. contribute about 55% of the total effective dose, 40% of the absorbed lung dose and 57 to 70% of the equivalent lung dose, depending on the value assigned to wR and the dose neglected in the determination of 222Rn D.P. risk varies from 30 to 60%. In ten French uranium mines, 222Rn D.P. contributed from 34 to 67% to the effective dose, 25 to 57% to the absorbed lung dose and 36 to 74% to the equivalent lung dose, depending on the wR value and the mine. Therefore, for the time periods covered by PAD data, the effective doses and the absorbed or equivalent lung doses neglected in the determination of radon risk range form 33 to 75% of the corresponding total doses. Uncertainties are attached to neglected doses as they are to 222Rn D.P. exposures. These uncertainties can be evaluated rigorously only when personal dosimetry data are available. This cannot be done for miner populations for which 222Rn D.P. measurements were limited and gamma radiation and radioactive dust measurements inexistent. For such populations, uncertainties in the actual lung dose (absorbed or equivalent) can be many-folds but cannot be estimated with confidence. A further difficulty, not related to radiation exposures, is that most, if not all uranium miners were exposed to silica dust, which is a known lung carcinogen(41). There is no information on a possible synergism between inhaled silica and inhaled alpha emitters at concentrations for both pollutants found in the early years of uranium mining but the overall relative risk of 5 for lung cancer in French iron mines(42) and up to 15 in Czech iron mines(43) indicates that silica dust may present a greater risk of lung cancer than the mixture of airborne alpha emitters found in uranium mines (see Table 1), in which silica was also present in significant quantities. Impact of neglected doses on calculated ERR/WLM valuesIn order to assess the extent to which neglected doses may affect the estimation of the ERR/WLM it is necessary to keep in mind that (a) the ERR/WLM is largely governed by the incidence of lung cancer in the highest exposure groups and (b) the miners who received the highest exposures were likely exposed before effective ventilation systems were installed, that is, when radiation sources other than 222Rn D.P. contributed relatively more to lung doses than after the introduction of forced ventilation. Therefore, the neglected doses were likely larger in those miners who worked in the early years of uranium mining than in those who started working after the introduction of wet drilling and forced ventilation. Neglecting a sizeable fraction of the total dose to the lung introduces a proportional systematic bias in the ERR/WLM. Simultaneously, the high variability of neglected doses between facilities and the uncertainties in individual cumulated doses from inhaled 222Rn D.P. lead to unknown but potentially large errors in lifetime total doses and result in the misclassification of workers within exposure ranges which, in turn, pulls the dose-effect relationship towards the null hypothesis of no radiation effect, the larger the geometric standard deviation in dose measurements (in the sense used in epidemiology), the larger the downward bias(44). Errors due to neglected doses and dose misclassification reinforce each other towards the no-effect null hypothesis. Unfortunately, these errors can be quantified only in populations for which reliable personal dosimetry data exist, that is, in French uranium miners who started working after 1982, a very small fraction of the world population of uranium miners subject to published epidemiological studies. Since doses from the different sources are correlated, the excess of lung cancers due to radiation should be apportioned according to the contribution of each source to the total lung dose, that is, the ERR/WLM for radon alone should be corrected by a factor k where “lung dose” is the absorbed lung dose DT or the equivalent lung dose, HT, for various values of wR. For the French uranium miners, k may range from about 0.26 to about 0.75, and from 0.55 to 0.45 in the Elliot Lake mines. To the extent that neglected doses, relative to 222Rn progeny doses, are comparable in the various populations of uranium miners for which no personal dosimetry data exist and that the pre-ventilation conditions re-created in one of the Elliot Lake mines are representative of the conditions that prevailed in other uranium mines of the same era, the risk coefficients for 222Rn D.P. found in the literature may be too high be a factor of 2 or 3. This correction factor does not take into account misclassification due to neglected doses and is, therefore, itself underestimated. If neglected doses alone were taken into account to correct risk coefficients, the excess relative risk per WLM (ERR/WLM) reported by Lubin et al. for the Elliot Lake and French uranium miners, 0.89%/WLM and 0.36%/WLM(1), would become about 0.45% and 0.18%, respectively. A significantly lesser risk or an absence of risk at low radon exposures in uranium mines would also be consistent with the apparent ineffectiveness of low doses and dose rates of alpha emitters to induce cancer in animals, for example(34, 35, 45) and in humans, for example(30-33, 46). In this regard, Saccomanno(47) and Roscoe(48) mention that the lowest cumulated exposure received by non smoking uranium miners who developed lung cancer was about 465 WLM, well above exposures at which an excess risk is observed in miners who smoked cigarettes. Conclusions
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a Excess liver
cancer probably due to cirrhosis Table 1. Standardized Mortality Ratio (SMR) or Relative Risk (RR) for all cancers except lung in underground miners exposed to 222Rn decay products.
Table 2. Effective dose from each radiation source and contribution of 222Rn decay products to the effective dose and to the absorbed and equivalent lung dose for different radiation weighting factors, wR, in Elliot Lake mines.
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