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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 8 Occupational Radiation Studies INTRODUCTION The risk of cancer among physicians and other persons exposed to ionizing radiation in the workplace has been a subject of study since the 1940s, when increased mortality from leukemia was reported among radiologists compared to mortality among other medical specialists (March 1944; Dublin and Spiegelman 1948). An extensive retrospective cohort study (Court Brown and Doll 1958) confirmed the earlier reports and also noted excess mortality from other cancers. Since then, numerous studies have considered the mortality and cancer incidence of various occupationally exposed groups, in medicine (radiologists and radiological technicians), nuclear medicine, specialists (dentists and hygienists), industry (nuclear and radiochemical industries, as well as other industries where industrial radiography is used to assess the soundness of materials and structures), defense, research, and even transportation (airline crews as well as workers involved in the maintenance or operation of nuclear-powered vessels). The type of ionizing radiation exposure varies among occupations, with differing contributions from photons, neutrons, and α- and β-particles. Studies of populations with occupational radiation exposure are of relevance for radiation protection in that most workers have received protracted low-level exposures (a type of exposure of considerable importance for radiation protection of the public and of workers). Further, studies of some occupationally exposed groups, particularly in the nuclear industry, are well suited for direct estimation of the effects of low doses and low-dose rates of ionizing radiation (Cardis and others 2000) for the following reason: large numbers of workers have been employed in this industry since its beginning in the early to mid-1940s (more than 1 million workers worldwide); these populations are relatively stable; and by law, individual real-time monitoring of potentially exposed personnel has been carried out in most countries with the use of personal dosimeters (at least for external higher-energy exposures) and the measurements have been kept. Individual epidemiologic studies of occupational exposure to ionizing radiation, however, face a number of obstacles with respect to assessment of the dose-response relationship in the low-dose region (e.g., NRC 1990; Ron 1998; Boice and others 2000): The statistical power necessary to detect an adverse health effect from the low doses encountered in occupational settings requires a large number of exposed workers and sufficiently long follow-up to account for the latency periods. Thus, follow-ups of individual cohorts of workers ordinarily have insufficient statistical power. A number of large, combined multinational studies and analyses of mortality among nuclear industry workers have been carried out in order to address these issues (Cardis and others 2000). In some studies, such as those of radiologists and other medical personnel, the lack of individual dose estimates is a major limitation, as is the lack of a suitable comparison group. The usefulness of analyses involving external comparison groups is limited due to the “healthy worker effect” often found in many occupational cohorts (Howe and others 1988; Carpenter and others 1990). Articles included in this chapter were identified principally from searching the PubMed database of published articles from 1990 through December 2004. Searches were restricted to human studies and were broadly defined: key words included radiation; neoplasms; cancers; radiation-induced; occupational radiation; nuclear industry; nuclear workers; radiation workers; Mayak; Chernobyl; accident recovery workers; liquidators; radiologists; radiological technologists; radiotherapists; radiotherapy technicians; dentists; dental technicians; pilots; airline crew; airline personnel; and flight attendants. Articles were also identified from UNSCEAR (2000b), from references cited in papers reviewed, and from direct contacts with some of the main scientists who have been involved with studies of occupational exposures in recent years.
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 Studies of occupationally exposed persons have been reviewed in BEIR V (NRC 1990) and in more detail in UNSCEAR (2000b). Because of the large number of studies of radiation workers, they are not described exhaustively in this chapter, which focuses mainly on the most informative studies for the current BEIR VII evaluation (i.e., studies in which the sample size is sufficiently large and the historical individual dosimetric information is sufficiently complete for radiation risk estimation). As in the other review chapters in this report, studies were judged to be informative for the purpose of radiation risk estimation if (1) the study design was adequate and no major bias could be identified (see Chapter 5 concerning informative study designs and limitations); (2) individual quantitative estimates of radiation dose to the organ of interest were available for study subjects; (3) if so, the details of the dose reconstruction or estimation approach were evaluated; and (4) a quantitative estimate of disease risk in relation to radiation dose—in the form of an excess relative risk (ERR) or excess absolute risk (EAR) per gray—was provided. The data and confidence intervals are those given in the cited papers. NUCLEAR INDUSTRY WORKERS A direct assessment of the carcinogenic effects of protracted, generally low-level radiation exposure can be made from studies of cancer risk among workers in the nuclear industry, many of whom have been exposed to above-background levels of ionizing radiation over several decades and whose exposures have been monitored through the use of personal dosimeters. Throughout this report, the term “nuclear industry” will be used to refer to facilities engaged in the production of nuclear power, the manufacture of nuclear weapons, the enrichment and reprocessing of nuclear fuel, or reactor research. Uranium mining is not included. Principal References Many studies of mortality—and, in some instances, cancer incidence—among nuclear industry workers have been carried out over the past 20 years. Published studies have covered workers in Canada, Finland, France, India, Japan, Russia, Spain, the United Kingdom, and the United States. Most have been cohort studies. The main studies in which mortality or morbidity has been examined by level of individual radiation dose are listed in Table 8-1. The characteristics of the cohorts and results are summarized briefly in Table 8-2. A number of published studies are not described in Table 8-2, for the following reasons: The studies of Mayak workers in the former USSR are described in the next section of this chapter. Many of these workers received mixed exposures to low- and high-LET (linear energy transfer) ionizing radiation, including considerable doses from internal contamination with plutonium-239. Studies of nuclear industry workers in which analyses were not reported in relation to individual external dose estimates are not discussed further in this chapter. These are studies of the employees of the U.S. Department of Energy (DOE) facilities of Linde (Dupree and others 1987), Oak Ridge Y-12 plant (workers employed between 1943 and 1947; Polednak and Frome 1981), Pantex (Acquavella and others 1985), Savannah River (Cragle and others 1988), and United Nuclear Corporation (Hadjimichael and others 1983); studies of mortality of nuclear industry workers in Slovakia (Gulis 2003) and at the French Atomic Energy Commission (Telle-Lamberton and others, 2004); and the proportional mortality studies of workers in nuclear installations in India (Nambi and Soman 1990; Nambi and others 1991, 1992). Nested case-control studies of specific cancers in the cohort studies including melanoma (Austin and Reynolds 1997; Moore and others 1997); leukemia (Stern and others 1986); prostate cancer (Rooney and others 1993); and lung cancer (Rinsky and others 1988; Petersen and others 1990) are not included. Studies of combined cohorts comprising many of the workers included in individual studies have been carried out in the United Kingdom and the United States, as well as studies of all workers included in the national dose registries in Canada, Japan, and the United Kingdom. In the USA, combined analyses of the data on workers from Hanford, Rocky Flats, and Oak Ridge National Laboratory (ORNL) have been reported by Gilbert and collaborators (1989, 1993a). The latest analysis included 35,933 workers, followed until the end of 1986 (Gilbert and others 1993a). A study of workers employed in one of 15 commercial nuclear power facilities was also conducted (Howe and others 2004). The study included 53,698 workers followed up for mortality from 1979 to 1997. The British study of the National Registry of Radiation Workers (NRRW; Kendall and others 1992a, 1992b; Little and others 1993; Muirhead and others 1999) includes 124,743 monitored workers in the above-mentioned U.K. cohorts as well as employees of Nuclear Electric, the Defense Radiological Protection Service, and a number of other nuclear facilities. The latest publication covers follow-up for mortality until the end of December 1992. Combined analyses of three U.K. nuclear industry workforces (the Atomic Energy Authority [AEA], Atomic Weapons Establishment [AWE] and Sellafield) with follow-up extended to the end of 1988 have also been carried out (Carpenter and others 1994, 1998). In Canada, the study of the National Dose Registry (NDR) covered 206,620 workers in the industrial, medical, and dental fields, as well as nuclear power, followed for mortality through 1987 (Ashmore and others 1998) and cancer incidence through 1988 (Sont and others 2001). About 25% of these were nuclear industry workers, but detailed results were not presented for this group. The average dose of the entire cohort is low (6.6 mSv). The average length of follow-
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 TABLE 8-1 Cohort Studies of Nuclear Workers in Which Mortality or Morbidity Has Been Studied by Level of Individual Radiation Dose Country Cohort Reference Canada Chalk River plant of Atomic Energy of Canada Ltd. Howe and others (1987); Gribbin and others (1993) France Electricité de France Rogel and others (2005) Finland Finnish power plants and research reactor Auvinen and others (2002) Spain Spanish Nuclear Energy Board Artalejo and others (1997) United Kingdom Atomic Energy Authority Duncan and Howell (1970); Beral and others (1985); Fraser and others (1993) Atomic Weapons Establishment Beral and others (1988); Atkinson and others (2004) Sellafield Smith and Douglas (1986); Douglas and others (1994); Omar and others (1999) Chapelcross Binks and others (1989) Capenhurst McGeoghegan and Binks (2000b) Springfields McGeoghegan and Binks (2000a) United States Fernald Ritz (1999) Hanford Site Kneale and others (1981); Gilbert and others (1989); Gilbert and others (1993b); Kneale and Stewart (1993) Mound Facility Wiggs and others (1991a, 1991b) Oak Ridge National Laboratory Checkoway and others (1985); Wing and others (1991); Richardson and Wing (1999b) Oak Ridge Y-12 Plant Checkoway and others (1988); Loomis and Wolfe (1996, 1997) Oak Ridge X-10 Plant Frome and others (1997) Rocketdyne/Atomics International Ritz and others (1999a) Rocky Flats Wilkinson and others (1987); Voelz and others (1997) Portsmouth Naval Shipyard Rinsky and others (1981) up was slightly less than 10 years in the incidence study, which covered a total of 191,333 person-years of follow-up. A study of mortality in the subgroup of nuclear power industry workers registered in the NDR has recently been published (Zablotska and others 2004). The study included 45,468 workers monitored for more than 1 year between 1957 and 1994. The average cumulative dose was 1.5 mSv. The average length of follow-up was 13.4 years (607,979 person-years of follow-up). In Japan, the study (ESGNWJ 1997) covered a large cohort of 114,900 Japanese nuclear workers. The follow-up time was short (average 4.6 years), and the cumulative dose was relatively low (average 13.9 mSv). Consequently the study had little power to assess possible health effects of occupational ionizing radiation exposure; in particular, the test for trend for all cancers had a one-sided p-value of 0.65, and the test for trend for leukemia had a one-sided p-value of 0.22 (ESGNWJ 1997). In addition to the national combined analyses, a multinational combined analysis was carried out to maximize the information from studies of nuclear industry workers (IARC 1994, 1995; Cardis and others 1995). Individual data from seven of the cohorts are included in Table 8-2 (Hanford, ORNL, Rocky Flats, AEA, AWE, Sellafield, and the Chalk River plant of Atomic Energy of Canada Ltd. [AECL]) and from the U.S. Rocky Flats facility (Wilkinson and others 1987). Overall, 95,673 workers employed between 1943 and 1988 in one of the participating facilities were included. They contributed 2,124,526 person-years of follow-up (an average follow-up of 22.2 years). The collective dose was 3843 Sv, most of which (98%) was received by men. Characteristics of Studies of Nuclear Industry Workers In the majority of the studies listed above, study subjects are defined as workers employed in the nuclear industry for whom detailed individual external dose estimates were available. Exceptions include the Canadian NDR study (Ashmore and others 1998), which included many other types of radiation workers, and a number of cohorts (Hanford, ORNL, Sellafield, AEA, and AWE) in which both monitored and nonmonitored workers are included. In the latter studies, estimates of risk per unit dose are restricted to monitored workers, except in the study of ORNL (Wing and others 1991; Richardson and Wing 1999b), where doses were estimated for a number of workers who had not been monitored.
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 TABLE 8-2 Main Characteristics of Principal Studies of Nuclear Industry Workers Study Population References Dates of Exposure Dates of Follow-up No. of Subjects Person-Years Average Radiation Dose (Sv) Collective Dose (Sv) Comments United States Hanford Site Gilbert and others (1993b) 1944–1978 1944–1986 32,643a 0.026 854 Workers employed 6 months or more Oak Ridge National Laboratory Richardson and Wing (1999b) 1943–1985 1943–1990 14,095 425,486 NA Cohort includes white males Oak Ridge (X-10, Y-12) Frome and others (1997) 1943–1985 1943–1984 28,347 603,365 NA Rocky Flats Gilbert and others (1993a) 1951–1979 1952–1983 5,952 81,237b 0.041 241 White males Los Alamos Wiggs and others (1994) 1943–1977 1943–1990 15,727 456,637 NA White males Mound Facility Wiggs and others (1991b) 1947–1979 1947–1979 3,229 54,151 0.030 1625 Monitored white males Savannah River Site Cragle and others (1994) 1943–1986 1952–1986 9,860 NA 0.041 Rocketdyne/AI Ritz and others (1999a;1999b) 1950–1993 1950–1994 4,563 118,749 0.012 Portsmouth Naval Shipyard Rinsky and others (1981) 1952–1977 1952–1977 7615c 98,223 0.028 212 White males United Kingdom Sellafield Douglas and others (1994) 1947–1975 1947–1988 (1971–86—incidence) 10,276d 370,329e 0.128 1317 Mortality and morbidity study Omar and others (1999) 1947–1975 1947–1992 (1971–86—incidence) 10,382f 415,431 0.130 1352 All workers—mortality and morbidity study AEA Fraser and others (1993) 1946–1979 1946–1986 39,718 873,796 0.022 Mortality and morbidity study AWE Beral and others (1988) 1951–1982 1951–1982 22,552 419,467 0.003 Springfields McGeoghegan and Binks (2000a) 1946–1995 1946–1995 13,960 479,146g 0.020–0.023 Capenhurst McGeoghegan and Binks (2000b) 1946–1995 1946–1995 3,244 334,473g 0.010 32 Canada AECL Gribbin and others (1993) 1956–1980 1956–1985 8,977 157,101 0.015 Males France Electricité de France (EDF) Rogel and others (2005) 1961–1994 1961–1994 22,395 5.5 (median) 402 EDF Combined Cohorts Canadian NDR Ashmore and others (1998) 1951–1983 1951–1983 206,620 2,861,093 0.063 Canadian nuclear workers Zablotska and others (2004) 1957–1994 1957–1994 45,468 607,979 13.5 Canadian nuclear workers
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 Study Population References Dates of Exposure Dates of Follow-up No. of Subjects Person-Years Average Radiation Dose (Sv) Collective Dose (Sv) Comments Sont and others (2001) 1951–1983 1969–1988 191,333 2,667,903 0.066 Morbidity study Combined analyses of U.K. nuclear workers Carpenter and others (1994) Varied 1946–1988 1946–1988 75,006 1,800,144 0.037 NRRW Muirhead and others (1999) <1976–1992 <1976–1992 124,743 2,063,300 0.031 3810 Combined analyses of U.S. workers (Hanford, ORNL, Rocky Flats) Gilbert and others (1993a) Varied 1944–1979 Varied 1944–1986 44,943 835,070 0.027 1237 U.S. nuclear facility workers Howe and others (2004) 1945–1997 1979–1997 53,698 698,051 25.7 Three-country combined analyses (Canada, U.K., U.S.) Cardis and others (1995) Varied 1943–1982 Varied 1943–1988 95,673 2,124,526 0.04 3843 NOTE: NA = not available. aMonitored workers only. bExcludes first 5 years of follow-up. cIncludes only workers with doses >0.001 rem. dRadiation workers. eIncludes nonradiation workers. fIncluding 5203 plutonium workers. gIncludes nonradiation workers (more than 5000 at Springfields and more than 9000 at Capenhurst). The number of workers and person-years of follow-up in the major studies are listed in Table 8-2. In general, exposure in most of these cohorts was predominantly to low levels of external radiation (X- and γ-rays and some neutrons). Internal contamination (through inhalation, ingestion, skin absorption, or wounds) by tritium, plutonium, uranium, and other radionuclides occurred in some subgroups of workers. Assessment of Exposure to Radiation Control of radiation dose to workers in occupational settings is achieved by demarcating radiation levels in work areas, conducting routine radiation monitoring (e.g., by air sampling and the use of in situ radiation monitors), and by individual monitoring of workers. The studies of nuclear industry workers considered here are based on workers for whom individual monitoring of dose from external “higher”-energy (300–3000 keV) photon radiation was carried out routinely. Individual monitoring at its simplest consists of assigning radiation-sensitive dosimeters to each worker. Dosimeters, which consist of one or more of ionization chambers, photographic film, luminescent phosphors, or electronic devices, are worn by workers while they are present in designated radiation areas. Dosimeters are normally placed on the chest, and it is usually assumed that the measured radiation dose is representative of the whole-body dose (i.e., estimates “whole-body equivalent dose”); the dose to different parts of the body is assumed to be uniform. In nearly all cases, dosimeters are sensitive to the penetrating photon radiation of intermediate (>100 keV) to higher photon (i.e., X- and γ-rays) energies typical of radiation fields in the respective facilities. Specialized dosimeters and calibration methods are generally needed to measure accurately the dose from low-energy photons, beta, or neutron radiation present in some occupational environments. Monitoring for the intake of radioactive material is performed by bioassay, by whole-body in vivo counting, or by wearing personal air samplers. In most of the facilities that have been the object of the epidemiologic studies described above, measurements of dose to individuals have generally been recorded on a routine basis using the available dosimetry technology. Occupational radiation dose data constitute the most complete and detailed information currently available to researchers for studying the carcinogenic effects of low-dose,
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 protracted exposures to ionizing radiation. They are generally presented in the form of annual summaries of doses from different types of radiation (penetrating photons, beta, and where appropriate and measured, tritium and neutrons). These data were, however, compiled to monitor worker exposure for compliance with radiation protection guidelines, which have changed over time, and not specifically for epidemiologic purposes. Overall, the accuracy and precision of recorded individual doses and their comparability will therefore depend on: the dosimetry technology, which includes the physical capabilities of the dosimetry system, such as the response to different types and energies of radiation, in particular in mixed radiation fields; the radiation fields in the work environment, which may include mixed types of radiation, variations in exposure geometries, and environmental conditions; and the administrative practices adopted by facilities to calculate and record personnel dose based on technical, administrative, and statutory compliance considerations. Consequently, detailed examination of dosimetry practices, including sources and magnitude of errors, is important in considering whether sufficiently accurate and precise estimates of dose can be obtained for use in an epidemiologic study. Information on internal contamination with radionuclides other than tritium is generally sparse, particularly in early years, and consists of information on the fact of monitoring or on a percentage of the annual limit of intake. Very few studies have attempted to reconstruct individual doses from nuclides other than tritium. One exception is the study of Sellafield workers in the United Kingdom, where efforts have been made to reconstruct plutonium exposures (Omar and others 1999). In high-dose studies, the majority of excess deaths from cancer have been demonstrated in subjects exposed to doses of at least 1 Sv. There were approximately 3000 such subjects among atomic bomb survivors. Doses received by employees of nuclear industry facilities are considerably lower. In the Sellafield cohort (Douglas and others 1994), in which the highest doses among the nuclear industry worker studies have been reported, only about 60 out of more than 10,000 individuals monitored for external radiation exposure had received doses of 1 Sv or more, and these doses were accumulated over the course of a working life. The mean cumulative radiation dose in the three-country combined analyses was 40.2 mSv per worker and the collective dose was 3843 Sv (IARC 1995). Women comprised fewer than 15% of the workers, and their mean cumulative dose was low (6.2 mSv) compared to that of men (46.0 mSv). Overall, the distribution of doses was very skewed; almost 60% of subjects had cumulative doses less than 10 mSv, 80% were less than 50 mSv, and less than 2% had doses greater than 400 mSv. The majority of cohort studies collected only information that could readily be obtained from employment and dosimetry records. This consists, in addition to information on individual annual radiation dose from different types of radiation, date of birth, date and cause of death, sex, socioeconomic status based on occupational group or education, and dates of beginning and end of employment. Nested case-control studies have allowed the exploration of additional factors including tobacco smoking and other occupational exposures. Results In most of the nuclear industry workers studies, death rates among worker populations were compared with national or regional rates. In most cases, rates for all causes and all cancer mortality in the workers were substantially lower than in the reference populations. Possible explanations include the healthy worker effect and unknown differences between nuclear industry workers and the general population. In most studies where external radiation dose estimates were available, death rates were also compared in relation to levels of radiation exposure within the study population. For all cancer mortality (excluding leukemia), the estimates of radiation-induced excess risk varied from negative to several times greater than those derived from linear extrapolation from high-dose studies (Table 8-3). Moreover, because of the large degree of uncertainty, many of these estimates were consistent with an even wider range of possibilities, from negative risks to excess risks at least an order of magnitude greater than those on which the current radiation protection recommendations have been based. In most of the large studies of nuclear industry workers, estimates of ERR1 per gray (ERR/Gy) have been derived, mostly using Poisson regression. Estimates of excess death rate per 106 person-years (PY) per gray have also been presented in some studies. Results of such analyses are shown in Tables 8-3 and 8-4 for all cancers excluding leukemia and for leukemia, respectively. Table 8-5 is a listing of the results from other studies of nuclear workers that could not be used in computation of ERRs or EARs.2 Cancer mortality was observed to increase significantly with increasing level of exposure in four studies: AWE (Beral and others 1988), ORNL (Wing and others 1991; Richardson and Wing 1998), Canadian NDR (Ashmore and others 1998), and Rocketdyne (Ritz and others 1999a). The ERR estimate based on the three-country combined analysis was close to zero, but was compatible with a range of possi- 1 ERR is the rate of disease in an exposed population divided by the rate of disease in an unexposed population minus 1.0. 2 EAR is the rate of disease in an exposed population minus the rate of disease in an unexposed population.
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 TABLE 8-3 Radiation Risk Estimates in Studies of Nuclear Industry Workers—Summary of Risk Estimates per Gray for Mortality from All Cancers Excluding Leukemia Study Population References Number of Cancer Deaths ERR/Sv (90% CI) EAR/104 PY/Sv (90% CI) Comments United States Hanford Gilbert and others (1993b) 1413 −0.0 (<0, 1.9) ORNL Richardson and Wing (1999a) 879 — 1.21%/10 mGy (SE 0.65) 4.98%/10 mGy (SE 1.48) Leukemias included Restricted to dose received after age 45 Oak Ridge Y-10, X-12 Frome and others (1997) 1134 1.45 (0.15, 3.48)a — Leukemias included Rocky Flats Gilbert and others (1993a) 114 <0 (<0, 0) — United Kingdom AEA Fraser and others (1993) 720 0.8 (−1.0, 3.1)a 20.3 (−26.0, 71.1)a AWE Beral and others (1988) 275 7.6 (0.4, 15.3)a Capenhurst McGeoghegan and Binks (2000b) 174 −1.3 (<0, 2.4) Males only Sellafield Douglas and others (1994) 567 0.11 (−0.4, 0.8) 5.6 (90% CI 15.86, 27.15)b Springfields McGeoghegan and Binks (2000a) 939 0.64 (−0.95, 2.7) Males only Canada AECL Gribbin and others (1993) 221 0.049 (−0.68, 2.17) Combined cohorts Canadian NDR Ashmore and others (1998) 1632 3.0 (1.1, 4.8) — Canadian nuclear workers Zablotska and others (2004) 531 2.80 (−0.038, 7.13)a Combined UK nuclear industry workforce Carpenter and others (1994, 1998) 1824 −0.02 (−0.5, 0.6)a −0.68 (−23.3, 20.9)a NRRW Muirhead and others (1999) 3020 0.086 (−0.28, 0.52)a — Hanford, ORNL, Rocky Flats Gilbert and others (1993a) 1789 0.0 (<0.8)a — U.S. nuclear facility workers Howe and others (2004) 368c 0.506 (−2.01, 4.64)a Three-country combined analyses (Canada, U.K., U.S.) Cardis and others (1995) 3830 −0.07 (−0.39, 0.30) — NOTE: Doses are lagged by 10 years unless otherwise indicated. a95% confidence interval. bDoses are lagged by 15 years. cAll solid cancers only.
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 TABLE 8-4 Radiation Risk Estimates in Main Studies of Nuclear Industry Workers—Summary of Risk Estimates per Gray for Mortality from Leukemia Excluding Chronic Lymphocytic Leukemia Study Population References Observed Cases ERR/Sv (90% CI) EAR/104 PY/Sv Comments United States Hanford Gilbert and others (1993b) 44 −1.1 (<0, 3.0) — ORNL Wing and others (1991) 28 6.4 (-11.2, 24.0) Hanford, ORNL, Rocky Flats Gilbert and others (1993a) 67 −1.0 (<0, 2.2)a — United Kingdom UKAEA Fraser and others (1993) 31 −4.2 (-5.7, 2.6) UKAWE Beral and others (1988) 4 Capenhurst McGeoghegan and Binks (2000b) 4 −1.27 (<0, 2.75) Males only Sellafield Douglas and others (1994) 12 13.92 (90% CI 1.94, 70.52) 2.47 (90% CI 1.21, NE) Upper bound for EAR could not be estimated (NE) Springfields McGeoghegan and Binks (2000a) 23 −1.89 (< −1.97, 13.1) Males only Canada AECL Gribbin and others (1993) 4 19.0 (0.14, 113) — Combined Cohorts Canadian NDR Ashmore and others (1998) 46 0.4 (−4.9, 5.7) — Males Canadian nuclear workers Zablotska and others (2004) 18 52.5 (0.21, 291)a Combined U.K. nuclear industry workforce Carpenter and others (1994, 1998) 49 4.18 (0.4, 13.4)a 2.10 (0.4, 3.6)b 2-year lag; adjusted for age, sex, calendar period, social class, and facility NRRW Muirhead and others (1999) 91 2.55 (−0.032, 7.16) — 2-year lag Hanford, ORNL, Rocky Flats Gilbert and others (1993a) 67 −1.0 (<0, 2.2)a U.S. nuclear facility workers Howe and others (2004) 26 5.67 (−2.56, 30.4)a Three-country combined analyses (Canada, U.K., U.S.) Cardis and others (1995) 119 2.18 (0.13, 5.7) — 2-year lag; adjusted for age, socioeconomic status, facility, and calendar time NOTE: Doses are lagged by 2 years unless otherwise specified. a95% confidence interval. bAbsolute risk estimate is number of deaths per person-year per sievert.
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 TABLE 8-5 Results of Studies of Nuclear Industry Workers with Individual External Dosimetry that Did Not Provide ERRs or EARs Country Facility No. of Subjects All Cancers Leukemia No. of Deaths Results (90% CI) No. of Deaths Results (90% CI) United States Mound (Wiggs and others 1991a, 1991b) 3,229 66 No association with radiation dose 4 Significant (p < .01) positive trend with radiation dose Los Alamos (Wiggs and others 1994) 15,727 732 No association with radiation dose 44 No association with radiation dose Portsmouth Naval Shipyard (Rinsky and others 1981) 7,615 201 No association with radiation dose 7 No association with radiation dose Rocky Flats (Wilkinson and others 1987) 5,413 50 Slope = −3.65/10 mSv (−12.02, 4.71) 4 RR = 1.0 (0.8, 9.1) for 10mSv vs. <10 mSv Rocketdyne (Ritz and others 1999a) 4,563 258 Significant (p = .036) trend 28a Significant (p = .003) trend United Kingdom BNFL (McGeoghegan and Binks 1999) 2,467 —b Significant (p < .01) positive trend when doses are lagged by 15 years —b No association with radiation dose AWE (Atkinson and others 2004) 26,395 1560 No association with radiation dose 38 No association with radiation dose Slovakia Jaslovske Bohunice power plant (Gulis 2003) 2,776 14 No association with radiation dose 0 France Electricité de France (Rogel and others 2005) 22,395 116 No association with radiation dose 5 No association with radiation dose aHemato- and lymphopoietic cancers. bNot specified. bilities, from a reduction of risk at low doses to risks twice those on which current radiation protection recommendations are based. In most studies, analyses of mortality in relation to cumulative external radiation dose were conducted for many specific types of cancer. These studies have generally not shown significant increases in risk among exposed workers for most cancer types examined, although a few positive associations have been found (Table 8-3). For leukemia, risk estimates varied considerably from study to study (Table 8-4). In the pooled study of workers in the United States (Gilbert and others 1993a), the estimate of ERR per gray based on the combined data was negative, although the upper confidence bound was slightly larger than the estimate currently recommended by the International Commission on Radiological Protection (ICRP 1991). By contrast, significant positive associations were observed in AECL and nuclear worker studies in Canada (Gribbin and others 1993; Zablotska and others 2004) and in the U.K. study of Sellafield workers (Douglas and others 1994), as well as in the NRRW cohort (Muirhead and others 1999) and the three-country combined analyses (Cardis and others 1995). The confidence intervals in these studies were wide, and the estimates of risk were consistent with those on which current radiation protection recommendations are based. Statistically significant (p < .05, one-sided) positive associations between cumulative external radiation dose and mortality from multiple myeloma were found in the Hanford (Gilbert and others 1989) and Sellafield (Douglas and others 1994) studies. A similar association was also found in the NRRW (Muirhead and others 1999) and three-country analyses (Cardis and others 1995), largely reflecting the previously reported associations in individual cohorts. The association in the Hanford study was not significant when follow-up was extended to 1986 (Gilbert and others 1993b). An association between radiation dose and mortality from cancer of the prostate was found in two studies, the AEA (Beral and others 1985; Fraser and others 1993) and the AWE (Beral and others 1988); in AWE workers it was statistically significant only among workers who had been
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 monitored for exposure to radionuclides (Rooney and others 1993) in the period 1946–1979. No such increase was observed in the NRRW (Muirhead and others 1999), which included all of the monitored workers in these two studies. A significant positive association with lung cancer was observed in the AWE and ORNL studies (Beral and others 1988; Wing and others 1991), particularly among those exposed to radionuclides in the AWE and in nonmonthly workers at ORNL. Information on tobacco smoking was available systematically in these studies. A few other significant associations were reported in single studies (Table 8-4). Given the number of associations examined, some of the significant results observed may have been due to chance. Several points must be kept in mind when making comparisons of these worker-based risk estimates and confidence intervals with those based on high-dose-rate studies. The most important are possible biases and uncertainties in dose estimates, errors in outcome data, and inadequate adjustment for confounders. Design Issues Among the very large and potentially most informative cohort studies reviewed in this chapter, two present a number of problems that limit their informativeness. In the Canadian NDR study (Ashmore and others 1998), the very low standardized mortality ratio (SMR)3 for all-cause mortality (61) suggests that record linkage procedures between the Canadian National Dose Registry and the Canadian Mortality Data Base may have been imperfect. There could have been some confounding of the dose-response because of associations between the probability of successful linkage and factors (e.g., socioeconomic status [SES]) associated with occupational radiation dose. This is the only study in which associations have been observed between radiation dose and all-cause mortality, all cancer mortality (without any clear relation to specific cancers), mortality due to cardiovascular diseases (males and females), and fatal accidents (males only). Moreover, no information is available on SES—a factor that has been shown in a number of previous cohorts to be a confounder of the association between radiation dose and cancer risk. Almost three-quarters of the cohort consists of radiation workers employed in different settings (dentistry, medicine, industrial radiography), where radiation control may be very different (possibly less uniform and systematic due to the much smaller numbers of persons monitored in individual workplaces) than in the nuclear industry. In the Japanese NDR study (ESGNWJ 1997), SES information is also not available. Further, because of difficulties in carrying out vital status follow-up in Japan, the very large cohort had to be restricted to those who were employed in the previous 5 years; hence the follow-up time of this cohort is very short, and older workers as well as workers with higher doses (who were employed in early years and left employment more than 5 years in the past) have been excluded from the follow-up. Consequently the study has little power to estimate possible health risks associated with occupational radiation exposure. Adequacy of the Dose Estimates High-Energy Photon Doses The accuracy and precision of individual dose estimates in the nuclear industry is a function of time, place, radiation energy and quality, the geometry of the radiation exposure, and the location of the dosimeter on the body of the worker. Efforts were made in some of the studies (AEA, Sellafield, ORNL, U.S. DOE combined analyses, three-country study, Saclay site in France) to assess the importance of dosimetric errors due to administrative practices adopted by facilities to calculate and record personnel dose based on technical, administrative, and statutory compliance considerations (Adams and Langmead 1962; Smith and Inskip 1985; Taylor 1991; Telle 1995; Tankersley and others 1996; Mitchell and others 1997; Watkins and others 1997; Telle-Lamberton and others 1998). Results of reanalyses of data using different approaches to estimate doses from missing dosimeters or below-threshold readings have yielded similar results to the analyses based on original data (Inskip and others 1987; Little and others 1993). In the three-country combined analyses, a retrospective dosimetry study was carried out to identify the various sources of biases and random errors in dosimetry for workers in each of the facilities included and to estimate the magnitude of these errors. As a result, it was concluded that for the majority of workers with predominant high-energy (300–3000 keV) photon exposures at levels greater than the detection threshold of the dosimeter, there is no strong reason to believe that available dose estimates substantially underestimate or overestimate deep dose. The dose estimates were judged to be compatible across facilities and over time. However, available dose estimates may have overestimated dose to the bone marrow by up to 20%. Estimation of leukemia risk adjusting for this overestimation yielded an ERR of 2.6 Sv−1 instead of 2.2. For deep organs, the factor is likely to be smaller, of the order of several percent. Random errors in dose estimates are likely to bias the risk estimates downwards, compared to estimates from high-dose studies, which have been based on organ doses. At lower exposure levels however, practices for recording subthreshold doses have resulted in a slight underestimation of doses from predominant higher-energy photon exposure (Fix and others 1997). At the Hanford plant in the United States, based on experiments and expert assessments, efforts were made to 3 SMR is the ratio (multiplied by 100) of the mortality rate from a disease in the population being studied divided by the comparable rate in a standard population.
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 quantify systematic errors related to the dosimetry technology and radiation fields as well as errors related to laboratory practices (Fix and others 1994, 1997; Gilbert 1998). When these errors were taken into account in the risk estimation process, it resulted in a widening of the confidence intervals around the ERR (Gilbert and Fix 1995) as shown in Table 8-6. Doses from Neutrons, Low- and Very-High-Energy Photons, and Internal Contamination In the three-country study, efforts were also made to identify workers with substantial doses from radiations other than high-energy photons (mainly from neutrons, low-energy radiation, and contamination with radionuclides, particularly plutonium), for whom recorded dose estimates may be in error. Although it was not possible to identify all such workers, risk estimates based on restricted dosimetry analyses, which excluded all such workers who could be identified, did not differ greatly from those based on the standard approach (-0.04 and 2.05 Sv−1 respectively, for all cancers excluding leukemia and for leukemia excluding chronic lymphocytic leukemia (CLL) compared to -0.07 and 2.18 Sv−1 in the standard population). In addition, the estimate of risk for all cancers excluding leukemia and lung cancer (the organ that would receive the majority of the dose from plutonium contamination) was identical to that of all cancers excluding leukemia (−0.07 Sv−1; 90% CI −0.39, 0.30). It is therefore unlikely that the risk estimates in this study are substantially biased by inclusion in the analyses of a minority of workers with dose from neutrons, low-energy photons, and internal contamination (Cardis and others 1995). Possible Confounding and Modifying Factors Tobacco Smoke As in most occupational cohort studies, information on life-style factors such as smoking habits, diet, and other oc TABLE 8-6 Estimates of the ERR per Sievert with 90% CIs for the Hanford Worker Study Based on Recorded Doses and Based on Estimated Organ Doses All Cancers Excluding Leukemia Leukemia Excluding CLL Recorded doses 0.23 (90% CI <0, 1.5) −0.9 (90% CI <0, 2.7) Organ doses (corrected for systematic errors related to radiation fields) 0.20 (90%CI <0, 1.7) −1.3 (90% CI <0, 3.6) NOTE: CLL = chronic lymphocytic leukemia. cupational exposures could not be obtained retrospectively for all members of the cohort. In the three-country combined analyses, there was little indirect evidence for an association between cumulative dose and mortality from smoking-related cancers, respiratory diseases, or liver cirrhosis; thus, it is unlikely that smoking or alcohol consumption are strongly correlated with radiation dose (Cardis and others 1995). This is supported by the observation that the risk estimates for all cancers excluding leukemia and all cancers excluding both leukemia and lung cancer were nearly identical (Cardis and others 1995): also, the results of two studies, carried out within the Hanford (Petersen and others 1990) and AEA (Carpenter and others 1989) cohorts, respectively, showed little evidence for an association between smoking and occupational radiation dose. A positive association between smoking and occupational radiation dose was found in the AECL cohort in Canada (Howe and others 1987). Socioeconomic Status A positive association between radiation dose and mortality from circulatory disease was observed in the four cohorts included in the three-country study in which information on SES was least detailed (Rocky Flats, Sellafield, AECL, Canadian NDR). It may reflect residual confounding by life-style factors for which the SES variable is an inadequate proxy. Radionuclides in the Working Environment At uranium fuel production facilities, inhalation of airborne uranium dust may represent an important potential source of radiation exposure. Workers in these facilities have two main possible sources of radiological exposure to tissues of the whole body: external γ-ray exposure and internal depositions that deliver radiation doses (mainly from α-particles) primarily to the lung and lymphatic system. If the uranium dust is soluble, exposure of other tissues may also occur such as liver, kidney, and bone, although organ doses would be expected to be small. Low-LET radiation risk estimates for tumors in these organs are possibly confounded by high-LET radiation exposure for workers at uranium production facilities, since workers with a significant dose from internal contamination are often persons with substantial external exposure. A number of studies of such workers have been reviewed (Cardis and Richardson 2000; NRC 2000). Comparison of findings among uranium-processing facilities is complicated by the fact that processes and historical periods of operation have differed among facilities, leading to differences in exposure conditions and follow-up among cohorts. Further, assessment of past internal uranium exposure of nuclear workers is complicated by the methodological difficulties of internal dosimetry, as well as by inadequate historical information with which to quantify internal radiation doses accurately. These exposure measurement
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 problems pose significant difficulties for epidemiology: the inability to classify workers accurately by level of internal radiation exposure may lead to confounding of the analyses of association between external low-LET radiation dose and cancer risk. Lung cancer has been the primary outcome of interest in studies of workers in fuel enrichment and production facilities. Lung cancer mortality was found to be significantly elevated, compared to national rates, among workers in nuclear fuel processing facilities in three reports (Loomis and Wolf 1997; Checkoway and others 1988; Frome and others 1990), but not in others (Brown and Bloom 1987; Dupree and others 1987, 1995; Ritz and others 1999b). An association between external low-LET radiation dose and lung cancer mortality was observed in two cohorts in the United States (Fernald and Y-12; Checkoway and others 1988; Ritz and others 1999a), and an association with lung cancer incidence (using a 20-year lag) was observed in one study in the United Kingdom (McGeoghegan and Binks 2000a). No association was found in other papers on the U.S. (Hadjimichael and others 1983; Ritz and others 2000) and U.K. (McGeoghegan and Binks 2000b) cohorts. No information on dose to the lung from internal contamination was available for analysis in these studies. In studies where estimation of dose to the lung from internal contamination was carried out, an association was observed at Y-12, but not at Rocketdyne (Ritz and others 1999a). In contrast, a U.S. multifacility case-control study of lung cancer among workers exposed to uranium dust at TEC, Y-12, Fernald, and Mallinckrodt found no such association; there was a suggestion, however, of positive associations among workers hired over age 45 (Dupree and others 1995). Therefore, risk estimates for low-LET radiation-induced lung cancer risk in these cohorts should be treated with caution. Following the observation of increased prostate cancer mortality related to cumulative external radiation dose in the AEA (Beral and others 1988; Rooney and others 1993) a nested case-control study was conducted of prostate cancer risk among employees of that facility. The study showed that exposure to five radionuclides (tritium, chromium-51, iron-59, cobalt-60, and zinc-65), evaluated separately, was associated with an increased risk of prostate cancer. Analyses of the association between external radiation dose and prostate cancer risk were carried out both for workers with probable exposure to these radionuclides and for those who had no such exposure. The association between external dose and prostate cancer was restricted to those with radionuclide exposure. In the Combined UK Industrial Workforce study, Carpenter and colleagues (1998) carried out analyses of cancer mortality in relation to external radiation dose in two groups—those who had been monitored for internal radionuclide contamination and those who had not. A positive association was seen in both groups of workers, although it was statistically significant only among those who had been monitored for internal contamination. Cancer mortality and incidence was studied among Sellafield workers in relation to exposure to plutonium and to external low-LET radiation (Omar and others 1999). A significant association between mortality from leukemia excluding CLL (13 deaths) was seen in relation to external radiation dose using a 2-year lag, as had been seen in the previous follow-up of this cohort (Douglas and others 1994). When analyses were restricted to plutonium workers and took into account both external low-LET radiation dose and estimated plutonium dose, the association was no longer statistically significant, based on six deaths. Other Occupational Exposures Wing and colleagues (1993) evaluated the effect of potential exposure to beryllium, lead, and mercury in the ORNL cohort by identifying workers with potential for these exposures from employment records. Adjustment for these potential exposures had little effect on the radiation risk estimates. The interpretation of these results is limited by the absence of individual exposure estimates for the chemicals considered. Rinsky and colleagues (1981) considered exposure to a number of workplace carcinogens in a case-control study of lung cancer among civilian employees of the Portsmouth naval shipyard. Asbestos and welding by-products were found to confound the association between radiation exposure and lung cancer risk in this population, where radiation workers appear to be more heavily exposed to asbestos and welding fumes than other workers. The unadjusted lung cancer odds ratio for workers with a cumulative dose of 10–49.99 mSv was 1.8 (95% CI 1.1, 3.1) compared to workers with no history of radiation exposure; adjustment for asbestos and welding fumes reduced it slightly to 1.7 (95% CI 1.0, 2.9). Modifiers of Radiation Risk Several authors have reported an association between age at exposure and/or attained age and the risk of radiation-induced cancer. This has been reported in the Hanford, ORNL, and Rocketdyne cohorts (Gilbert and others 1993a; Stewart and Kneale 1996; Richardson and Wing 1999a; Ritz and others 1999b), but not in five other cohorts in which it was considered—Rocky Flats, AECL, AEA, AWE, and Sellafield (Cardis and others 1995; IARC 1995). The three-country and the NRRW studies (Cardis and others 1995; Muirhead and others 1999) of nuclear industry workers currently provide the most comprehensive and precise direct estimates of the effects of protracted exposures to low levels of low-LET radiation. Although the estimates are lower than the linear estimates obtained from studies of atomic bomb survivors, as seen in Table 8-7, they are compatible with a range of possibilities, from a reduction of risk at low doses, to risks twice those on which current radiation
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 TABLE 8-7 Comparison of Estimates of ERR/Gy Between Major Nuclear Industry Workers Combined Analyses and the Atomic Bomb Survivors Study Population All Cancers but Leukemia Leukemia, Excluding CLL Atomic bomb survivorsa 0.24 (0.12, 0.4) 2.2 (0.4, 4.7) Nuclear workers Three-country study −0.07 (−0.39, 0.30) 2.2 (0.1, 5.7) NRRW 0.09 (−0.28, 0.52) 2.6 (−0.03, 7.2) aBased on male atomic bomb survivors, aged 20–60 years at exposure, as presented by Muirhead and others (1999). protection recommendations are based. Overall, they do not suggest that current radiation risk estimates for cancer at low levels of exposure are appreciably in error. Uncertainty concerning the exact size of this risk, remains, however, as indicated by the width of the confidence intervals presented. WORKERS FROM THE MAYAK FACILITY A cohort of about 21,000 Russian nuclear workers who worked at the Mayak plutonium production complex between 1948 and 1972 is under study. The Mayak complex, which is located in the Chelyabinsk region of the Russian Federation, includes three main plants: a reactor complex, a radiochemical separation plant, and a plutonium production plant. Workers at all three plants had the potential for exposure to external radiation, and workers at the radiochemical and plutonium production plants also had the potential for exposure to plutonium. Recently, data on workers at two auxiliary plants, who had much less potential for exposure, have been added to the cohort under study to expand the comparison group. As for other nuclear worker cohorts, estimates of annual external doses are available from individual film badge monitoring data. Some workers were also monitored for plutonium exposure; however, since routine testing based on large urine samples did not begin until about 1970, only about 40% of workers with the potential for such exposure have been monitored. External exposures and exposures of Mayak workers to plutonium far exceed those of other nuclear worker cohorts discussed previously in this chapter. For example, for the nearly 11,000 monitored workers hired before 1959, the mean cumulative external dose was 1.2 Gy, more than an order of magnitude higher than any of the cohorts described in Table 8-2. Thus, the Mayak cohort offers a unique opportunity to obtain reasonably precise estimates of risks from medium- to high-dose protracted external exposure that can then be compared to estimates based on acute exposure, such as those obtained from A-bomb survivors. The first estimates of risk from external exposure were reported by Shilnikova and colleagues (2003). Analyses focused on leukemia (excluding CLL); cancers of the lung, liver, and bone (analyzed as a group); and solid cancers excluding lung, liver, and bone (also analyzed as a group). Lung, liver, and bone are the organs that receive the largest doses from plutonium, and excess cancers in all three organs have been linked clearly to plutonium exposure among Mayak workers (Gilbert and others 2000; Koshurnikova and others 2000; Kreisheimer and others 2000). Analyses were adjusted for internal exposure to plutonium by using the estimated body burden for workers who had plutonium-moni-toring data and by using a plutonium surrogate variable for workers who were not monitored for plutonium. The plutonium surrogate variable was developed recently from detailed work histories. For leukemia, the estimated ERR/Gy was 6.9 (90% CI 2.9, 15) for the period 3–5 years after exposure and 0.5 (90% CI 0.1, 1.1) for the period 5 or more years after exposure. The estimate based on the entire period was 1.0 (90% CI 0.5, 2.0). There was no statistically significant departure from linearity and no evidence of modification by sex or age at hire. Estimates and confidence intervals for the solid cancer end points are shown in Table 8-8. For these end points, linear-quadratic functions provided significantly better fits than linear functions with a “downturn” in the dose-response at high doses. This may have resulted from overestimation of doses of certain workers in early years due to inadequacies in early film dosimeters. If this is the case, estimates of the linear term from the fitted linear-quadratic function may be more reliable. The estimates for cancers of the lung, liver, and bone were higher than those for other organs, possibly because the adjustment for plutonium exposure was less adequate for these cancers. There was no evidence of modification of the dose-response by sex, age at hire, or time since exposure. TABLE 8-8 Estimated ERR/Gy for Solid Cancers Among Mayak Workers Model ERR/Sv (90% CI) Lung, Liver, or Bone Other Solid Cancers All Solid Cancers Linear 0.30 (0.18, 0.46) 0.08 (0.03, 0.14) 0.15 (0.09, 0.20) Linear quadratica 0.54 (0.27, 0.89) 0.21 (0.06, 0.37) 0.30 (0.18, 0.43) aEstimates are for the linear coefficient of a fitted linear-quadratic function.
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 Summary Studies of workers employed at the Mayak complex in the Russian Federation offer a unique opportunity, because of the magnitude of the doses received (mean cumulative external dose of 1.2 Gy among monitored workers hired before 1959), to obtain reasonably precise estimates of risk from medium- to high-dose protracted external exposures. Substantial doses from plutonium have also been received by a number of these workers. Estimates of the radiation-related risks of leukemia; solid cancers; and lung, liver, and bone cancer have been derived from this cohort. Uncertainties in external dose estimates and in plutonium doses to specific organs must be considered in the interpretation of these results. Further studies of this population will be important to understand the effects of protracted exposure. CHERNOBYL CLEANUP WORKERS The Chernobyl accident resulted in widespread radioactive contamination of areas populated by millions of people in the three most affected countries of Belarus, the Russian Federation, and Ukraine. The populations at risk can be separated into the following groups (see Table 8-9): the “liquidators,” also referred to as “cleanup workers,” include persons who participated in the cleanup of the accident (cleanup of the reactor; construction of the sarcophagus; decontamination; building of roads; destruction and burial of contaminated buildings, forests, and equipment), as well as many others, including physicians, teachers, cooks, and interpreters who worked in the contaminated territories; TABLE 8-9 Estimates of Collective Effective Doses for Chernobyl Population Groups of Interest Population Number Collective Effective Dose (Sv) Evacuees 135,000 1,300 Liquidators (1986–1987) 200,000 20,000 Persons living in contaminated areasa Deposition density of 137Cs >15 Ci km−2 270,000 10,000–20,000 Deposition density of 137Cs >1 to 15 Ci km−2 3,700,000 20,000–60,000 aDoses are for 1986–1995; over the longer term (1996–2056) the collective dose will increase by approximately 50%. SOURCE: Cardis and others (1996). the “evacuees” who were evacuated from the town of Pripyat and the 30 km zone around the Chernobyl reactor in April–May 1986; the residents of the “strict control zones”—those members of the general population who have continued to live in the more heavily contaminated areas (with levels of 137Cs deposition greater than 555 kBq m−2), typically within a few hundred kilometers of the Chernobyl Nuclear Power Plant (NPP). Within these areas, radiation monitoring and preventive measures have been taken to maintain doses within permissible levels; and the general population of the contaminated territories in the three countries. The “liquidation” of the consequences of the Chernobyl accident lasted for about 3 years (1986–1989). During that time, different tasks were carried out, including the initial localization of the catastrophe (firefighting; closing down unaffected units of the power plant); evacuation of Pripyat and the population in the 30 km zone; decontamination of the inside of the Chernobyl NPP buildings, as well as the roofs of nearby buildings and nearby territories; renovation and maintenance of the other blocks of the power plant; construction of the sarcophagus; actions to decrease the spread of radioactive materials in the environment; safeguard of the 30 km zone and settlements and miscellaneous activities in the 30 km zone (health care, ecological monitoring, bringing in food, water, etc., for the liquidators). Different groups of liquidators were involved in these tasks; they worked under differing conditions of radiation monitoring and safety and were exposed to various types and levels of radiation. From 600,000 to 800,000 persons took part in the cleanup activities to liquidate the consequences of the Chernobyl accident. The exposure level was highest for those (approximately 200,000 liquidators) who worked in the 30 km zone in 1986–1987. Follow-up In 1987, an “All-Union Distributed Registry” was established following a directive of the Ministry of Public Health of the USSR (Tsyb and others 1989). The objective was to set up a comprehensive registration and active follow-up system for the persons most affected by the Chernobyl accident, including the liquidators. This system foresees an annual medical examination in which individuals are examined systematically by a general practitioner and a number of different specialists. All data on diseases diagnosed during the annual medical examination, as well as any other time during the year, are sent to the Chernobyl Registry for inclusion in the registry database. A study in Russia (Cardis and Okeanov 1996) indicates that the diagnostic information in the Chernobyl Registry is not always completely accurate. The lack of verification and quality control is actively being remedied but must be kept in mind when interpreting results
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 of studies of cancer frequency among exposed populations in these countries. Results from this follow-up may also be biased because participation in the annual examination may be related to illness and/or to level of exposure. Means also exist in the affected countries to carry out “passive” follow-up of exposed persons and of the general population with the use of population registries—of mortality, cancer, and other diseases. In each country of the former USSR, population registration is carried out at the local level in the address bureaus (where the addresses of current residents are kept) and the ZAGS (buro zapicii akta grazhdanskovo sostoyania), which compiles all information about birth, marriage, divorce, and death of persons living in the administrative area. No centralized registry exists, however, and results of a pilot study (Cardis and Okeanov 1996) indicate that considerable time and effort may be needed to trace subjects who have moved from one area to another. A computerized national Cancer Registry has been functioning in Belarus since the 1970s and registers all cases of malignant neoplasms. A comprehensive registry of hematological diseases also exists in Belarus, in the Institute of Haematology and Blood Transfusology. In Russia and the Ukraine, no centralized cancer registration system was in place at the time of the accident. Work has been carried out in both countries to set one up—at least in contaminated areas in Russia (Okeanov and others 1996; Storm and others 1996)—and quality control activities are continuing. Information is also available systematically on the general (i.e., not only cancer) morbidity of the population of the three countries. In the countries of the former USSR, regional outpatient clinics systematically collect information on disease diagnoses on all the residents of the region they cover (not only those included in the Chernobyl Registry). This information is summarized locally and is sent on special statistical reporting forms at yearly intervals to the Ministry of Health. These forms contain information about the number of cases of acute and chronic diseases diagnosed in a given year in the population in all areas of the country. This information is not broken down by age or sex. No verification of completeness or duplicates is possible. This passive system of collecting morbidity data on the population contrasts with the active follow-up carried out, as described above, for persons included in the Chernobyl Registry. Comparisons of morbidity based on these sources must therefore be interpreted with caution. Radiation Doses to Different Groups: Dose Levels and Available Estimates The dosimetric information available for liquidators is subject to controversy because personal dosimeters in use in the early days after the accident were too few and generally too sensitive. A reasonable estimate of the average dose received by the group of 200,000 people who worked in 1986–1996 is 100 mSv (Ivanov and others 1996). Thus, the collective effective dose would be approximately 20,000 Sv. Some workers received their dose in a few minutes—for example working on the roof of the reactor—while others received it over months or even years, and the predominant radiation type and route of exposure varied according to the time and activity of liquidators. Dose estimates have generally been derived in one of three ways: individual dosimetry: the liquidator was given a personal dosimeter; group dosimetry: an individual dosimeter was assigned to one member of a group of liquidators; or itineraries: measurements of γ-ray levels were made at various points where liquidators worked, and an individual’s dose was estimated as a function of the points where he or she worked and the time spent in these places. Liquidators are in principle included in the State Chernobyl Registries of Belarus, Russia, and Ukraine. Doses for a substantial proportion of them are missing from these registries. Liquidators who worked in the first year generally had higher recorded doses than those who worked in subsequent years. The level of dosimetric control and the adequacy of dose estimates vary between civilian liquidators (construction workers, logistic support), military liquidators (soldiers and officers who worked in decontamination, dosimetric control, and evacuation), and radiation specialists. Results Increases (doubling or tripling) in the incidence of leukemia and thyroid cancer have been observed in most of the studies of liquidators from Belarus, Russia, and Ukraine. Increases in leukemia risk are not unexpected since predictions from risk estimates in atomic bomb survivors have shown that if the experience of the A-bomb survivors is applicable to the Chernobyl situation, a tripling of leukemia mortality could be expected in the first 10–12 years following exposure (Cardis and others 1996). These results are difficult to interpret since, as indicated above, the follow-up of liquidators is much more active than that of the general population in the three countries. There are questions about the adequacy and completeness of the diagnostic information on liquidators in the Chernobyl Registry (Cardis and others 1996). For thyroid cancer in adults, the depth of screening to which the liquidators are subjected may greatly influence the observed incidence. In a case-control study based on the limited dosimetric data of the Chernobyl Registry in Russia, no significant association was seen between the risk of leukemia and radiation dose (Ivanov and others 1997a, 1997b). A recent cohort study of Russian liquidators showed no association between external radiation dose and risk of thyroid cancer among 72,000 liquidators from six regions (Ivanov and others
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 2002); no information on internal dose from iodine isotope was available in this study. It is noteworthy that no increase in the incidence of leukemia or thyroid cancer has been reported to date among Baltic country liquidators (Kesminiene and others 1997; Rahu and others 1997). These findings do not contradict the findings reported in Belarus, Russia, and Ukraine in that the number of liquidators in the Baltic countries is small, and the results are also consistent with a radiation-related increase. At this time, no conclusion can be drawn concerning the presence or absence of a radiation-related excess of cancer—particularly leukemia—among Chernobyl accident recovery workers. There is a pressing need for well-designed, sound analytical studies of recovery workers from Belarus, Russia, Ukraine, and the Baltic countries, in which special attention is given to individual dose reconstruction and the effect of screening and other possible confounding factors. Summary Studies of Chernobyl cleanup workers offer an important opportunity to evaluate the effects of protracted exposure in the low- to medium-dose range. No reliable risk estimates can be drawn at present from studies of these workers, however, because of the difficulties of follow-up and lack of validated individual dose estimates. AIRLINE AND AEROSPACE EMPLOYEES Airline pilots and flight attendants are exposed to increased cosmic radiation during flights. In 1991, the ICRP recommended that exposures to natural cosmic radiation should be considered occupational exposures for aircrews (ICRP 1991). Although aircrew members are not thought to exceed the National Council on Radiation Protection and Measurements (NCRP 1995) recommendation for occupationally exposed workers of 20 mSv per year averaged over 5 years, they do exceed the safety level set for the general public (1 mSv per year). The exposure varies with altitude, latitude, and solar flare activity. Solar activity varies on an 11-year cycle; however, prediction of short-term intense periods of activity is not possible. At 41,000 feet over the poles, the equivalent dose may vary from a norm of about 12 μSv to an extreme of 100 μSv (Friedberg and others 1989). The mean annual dose from galactic cosmic radiation can be modeled using knowledge of altitude, latitude, solar activity, and the Earth’s geomagnetic field. Friedberg and colleagues (1989) estimated the annual equivalent doses that would be received on 32 U.S. domestic and international flight routes as 0.2–9.1 mSv, considerably less than recommended annual adult occupational exposures. Several review articles have been published recently on epidemiologic studies of the occupational cancer risk for pilots and flight attendants (Blettner and others 1998; Blettner and Zeeb 1999; Boice and others 2000). The ability of studies to detect an association with ionizing radiation has been limited by several factors. Few studies have included internal comparisons, basing results instead on proportional mortality ratios, SMRs, or standardized incidence ratios. As a group, pilots and flight attendants differ appreciably from the general population. Pilots and other aircrew members are required to be very healthy and undergo frequent medical checkups, leading to the possibility of enhanced early detection of cancers in this occupational group. Disrupted circadian rhythms and, in females, relatively late age of first parity are other characteristics that complicate the choice of a suitable comparison group. Increased sun exposure, exposure to elevated ozone levels, fuel exhaust fumes, and electromagnetic fields are factors that may also confound any relationship observed between adverse health effects and cosmic radiation. Moreover, small study group sizes and the relatively low exposure levels of restricted range are further obstacles to the precise quantification of any risk. Whether epidemiologic studies of airline personnel can have sufficient power and precision to detect so small an association has been questioned. Based on published values of annual radiation exposure of aircrew flying at high altitudes, Boice and colleagues (1992) estimated that a flying career of 20–30 years duration would result in only an 80–180 mSv cumulative dose, corresponding to a relative risk (RR) of only about 1.06, if causal. The cosmic radiation to which aircrews are exposed is predominantly in the form of high-LET neutrons and low-LET γ-radiation, the former of which can contribute as much as half of the total equivalent dose at typical flight altitudes (Boice and others 1992; Hammer and others 2000). The choice of an appropriate weighting factor for the conversion of neutron dose estimates to equivalent doses is thus crucial for dosimetry in this occupational group and for assessment of the contribution of low-LET γ-radiation to any adverse health effects. At present, the evidence for an adverse health effect in aircrews due to ionizing radiation is inconclusive. Summary Studies of airline and aerospace employees do not currently provide estimates of radiation-related risks because dose estimates have not been used in the studies to derive quantitative risk estimates. MEDICAL AND DENTAL OCCUPATIONAL EXPOSURES Early studies of patterns of mortality among radiologists and other physician specialists produced a suggestion of an excess risk of specific cancers. Excess mortality from leukemia and lymphoma, especially multiple myeloma, and also from skin, lung, pancreatic, and prostate cancer (e.g., Matanoski and others 1975a, 1975b; Smith and Doll 1981; Logue and others 1986; Wang and others 1988) have been suggested, although findings were not consistent across
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 studies for all cancers. Matanoski and colleagues (1987) reported higher overall mortality and higher cancer mortality in radiologists compared to other specialists with lower expected exposures. A survey of the health of radiologic technologists (Boice and others 1992) gathered information on risk factors including smoking status, reproductive history, use of oral contraceptives, personal exposure to radiographs, height, weight, use of hair dye, and postmenopausal estrogens, and family and personal medical history of cancer. Members of the study population (n = 143,517, registered for more than 2 years with the American Registry of Radiologic Technologists, ARRT) were predominantly female and white. Personal dosimetric information was available for 64% of all the registered technologists, but only 34% of the breast cancer cases and 35% of the controls. Cases and controls were generally older and more likely to have stopped work before computerized records of dosimetry information were begun in 1979. Occupational exposure was estimated through the number of years worked as a technologist obtained from questionnaire data. A cohort study using the ARRT database (Doody and others 1998) reported SMRs and RRs adjusted for age, calendar year of follow-up, and gender. No significant excess mortality among radiological technologists was observed for lung cancer, breast cancer, or leukemia. The SMR for all malignant neoplasms exhibited a significant trend with the number of years certified (p < .001), as it did for breast cancer. In the absence of complete personal dosimetry information, accurate estimates of risk due to exposures to ionizing radiation are not possible. Yoshinaga and colleagues (1999) reported results from a retrospective cohort study of radiological technologists in Japan. External comparisons were also made with all workers and with professional and technical workers to address the issue of the healthy worker effect. The study used all Japanese men as the external comparison group; the SMR for all cancers in this study was 0.81 (95% CI 0.73, 0.95). Although elevated SMRs were observed for cancers of the colon, skin, lymphoma, multiple myeloma, and leukemia, none was statistically significant. The SMR for leukemia was significant in comparison to the total workforce as the reference group (SMR = 1.99; 95% CI 1.09, 3.33) and also for professional and technical workers as the reference group (SMR = 1.82; 95% CI 1.00, 3.06). No quantitative information on dosimetry was given in the report, nor was there an internal comparison, thus limiting the usefulness of the report for the estimation of risk. Since 1990, a number of studies of radiologists have been published that utilized measurements of individual exposure (Andersson and others 1991). Andersson and colleagues (1991) studied the cancer risk among staff at two radiotherapy departments in Denmark. The average cumulative radiation dose was 18.4 mSv, although 63% of the persons had doses <5 mSv. The expected number of cancers was estimated using cancer incidence rates from the Danish Cancer Registry. The overall relative risk was 1.07 (95% CI 0.91, 1.25) for all cancers, and no significant dose-response was observed. The risks for cancers that are considered radiation sensitive were not elevated. Berrington and colleagues (2001) reported the results of 100 years of follow-up of British radiologists who registered with a radiological society between 1897 and 1979 and who were followed until January 1, 1997. A progressive increase was observed in the SMRs for cancer with number of years since first registration. It appears that excess risk of cancer mortality in the period more than 40 years after first registration is likely a long-term effect of radiation exposure for radiologists registering between 1921 and 1954. Radiologists whose first registration was after 1954 demonstrated no increase in cancer mortality, possibly because of their lower overall radiation exposure. SUMMARY Epidemiologic studies of radiation workers and other persons exposed to ionizing radiation in the workplace started in the late 1950s with the study of British radiologists. Since then, numerous studies have considered the mortality and cancer incidence of various occupationally exposed groups in medicine, industry, defense, research, and aviation. Studies of occupationally exposed groups are, in principle, well suited for the direct estimation of the effects of low doses and low dose rates of ionizing radiation. Potentially, the most informative studies at present are those of nuclear industry workers (including the workers of Mayak in the former USSR), for whom individual real-time estimates of doses have been collected since the 1940s with the use of personal dosimeters. More than 1 million workers have been employed in this industry since its beginning. However, studies of individual worker cohorts are limited in their ability to estimate precisely the potentially small risks associated with low levels of exposure. Risk estimates from these studies are variable, ranging from no risk to risks an order of magnitude or more than those seen in atomic bomb survivors. Combined analyses of data from multiple cohorts offer an opportunity to increase the sensitivity of such studies and provide direct estimates of the effects of long-term, low-dose, low-LET radiation. The most comprehensive and precise estimates to date are those derived from the U.K. National Registry of Radiation Workers and the three-country study (Canada-United Kingdom-United States), which have provided estimates of leukemia and all cancer risks. Although the estimates are lower than the linear estimates obtained from studies of atomic bomb survivors, they are compatible with a range of possibilities, from a reduction of risk at low doses to risks twice those upon which current radiation protection recommendations are based. Overall, there
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Health Risks from Exposure to Low Levels of Ionizing Radiation: Beir VII Phase 2 is no suggestion that the current radiation risk estimates for cancer at low levels of exposure are appreciably in error. Uncertainty regarding the size of this risk remains as indicated by the width of the confidence intervals. Because of the absence of individual dose estimates in most of the cohorts, studies of occupational exposures in medicine and aviation provide minimal information useful for the quantification of these risks. Because of the uncertainty in occupational risk estimates and the fact that errors in doses have not formally been taken into account in these studies, the committee has concluded that the occupational studies are currently not suitable for the projection of population-based risks. These studies, however, provide a comparison to the risk estimates derived from atomic bomb survivors. As with survivors of the atomic bomb explosions, persons exposed to radiation at Mayak and at Chernobyl should continue to be followed for the indefinite future. Summary Studies of medical and dental occupational exposures do not currently provide quantitative estimates of radiation-related risks, due to the absence of radiation dose estimates.
Representative terms from entire chapter: