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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8 Occupational Radiation Studies INTRODUCTION Individual epidemiologic studies of occupational expo- sure to ionizing radiation, however, face a number of ob- The risk of cancer among physicians and other persons stacles with respect to assessment of the dose-response rela- exposed to ionizing radiation in the workplace has been a tionship in the low-dose region (e.g., NRC 1990; Ron 1998; subject of study since the 1940s, when increased mortality Boice and others 2000): from leukemia was reported among radiologists compared to mortality among other medical specialists (March 1944; • The statistical power necessary to detect an adverse Dublin and Spiegelman 1948). An extensive retrospective health effect from the low doses encountered in occupational cohort study (Court Brown and Doll 1958) confirmed the settings requires a large number of exposed workers and suf- earlier reports and also noted excess mortality from other ficiently long follow-up to account for the latency periods. cancers. Since then, numerous studies have considered the Thus, follow-ups of individual cohorts of workers ordinarily mortality and cancer incidence of various occupationally have insufficient statistical power. A number of large, com- exposed groups, in medicine (radiologists and radiological bined multinational studies and analyses of mortality among technicians), nuclear medicine, specialists (dentists and hy- nuclear industry workers have been carried out in order to gienists), industry (nuclear and radiochemical industries, as address these issues (Cardis and others 2000). well as other industries where industrial radiography is used • In some studies, such as those of radiologists and other to assess the soundness of materials and structures), defense, medical personnel, the lack of individual dose estimates is a research, and even transportation (airline crews as well as major limitation, as is the lack of a suitable comparison workers involved in the maintenance or operation of nuclear- group. powered vessels). The type of ionizing radiation exposure • The usefulness of analyses involving external compari- varies among occupations, with differing contributions from son groups is limited due to the “healthy worker effect” of- photons, neutrons, and α- and β-particles. ten found in many occupational cohorts (Howe and others Studies of populations with occupational radiation expo- 1988; Carpenter and others 1990). sure are of relevance for radiation protection in that most Articles included in this chapter were identified princi- workers have received protracted low-level exposures (a type pally from searching the PubMed database of published ar- of exposure of considerable importance for radiation protec- ticles from 1990 through December 2004. Searches were tion of the public and of workers). Further, studies of some restricted to human studies and were broadly defined: key occupationally exposed groups, particularly in the nuclear words included radiation; neoplasms; cancers; radiation-in- industry, are well suited for direct estimation of the effects duced; occupational radiation; nuclear industry; nuclear of low doses and low-dose rates of ionizing radiation (Cardis workers; radiation workers; Mayak; Chernobyl; accident re- and others 2000) for the following reason: large numbers of covery workers; liquidators; radiologists; radiological tech- workers have been employed in this industry since its begin- nologists; radiotherapists; radiotherapy technicians; dentists; ning in the early to mid-1940s (more than 1 million workers dental technicians; pilots; airline crew; airline personnel; and worldwide); these populations are relatively stable; and by flight attendants. Articles were also identified from law, individual real-time monitoring of potentially exposed UNSCEAR (2000b), from references cited in papers re- personnel has been carried out in most countries with the use viewed, and from direct contacts with some of the main sci- of personal dosimeters (at least for external higher-energy entists who have been involved with studies of occupational exposures) and the measurements have been kept. exposures in recent years. 189

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190 BEIR VII Studies of occupationally exposed persons have been re- • Studies of nuclear industry workers in which analyses viewed in BEIR V (NRC 1990) and in more detail in were not reported in relation to individual external dose esti- UNSCEAR (2000b). Because of the large number of studies mates are not discussed further in this chapter. These are of radiation workers, they are not described exhaustively in studies of the employees of the U.S. Department of Energy this chapter, which focuses mainly on the most informative (DOE) facilities of Linde (Dupree and others 1987), Oak studies for the current BEIR VII evaluation (i.e., studies in Ridge Y-12 plant (workers employed between 1943 and which the sample size is sufficiently large and the historical 1947; Polednak and Frome 1981), Pantex (Acquavella and individual dosimetric information is sufficiently complete others 1985), Savannah River (Cragle and others 1988), and for radiation risk estimation). As in the other review chap- United Nuclear Corporation (Hadjimichael and others 1983); ters in this report, studies were judged to be informative for studies of mortality of nuclear industry workers in Slovakia the purpose of radiation risk estimation if (1) the study de- (Gulis 2003) and at the French Atomic Energy Commission sign was adequate and no major bias could be identified (see (Telle-Lamberton and others, 2004); and the proportional Chapter 5 concerning informative study designs and limita- mortality studies of workers in nuclear installations in India tions); (2) individual quantitative estimates of radiation dose (Nambi and Soman 1990; Nambi and others 1991, 1992). to the organ of interest were available for study subjects; • Nested case-control studies of specific cancers in the (3) if so, the details of the dose reconstruction or estimation cohort studies including melanoma (Austin and Reynolds approach were evaluated; and (4) a quantitative estimate of 1997; Moore and others 1997); leukemia (Stern and others disease risk in relation to radiation dose—in the form of an 1986); prostate cancer (Rooney and others 1993); and lung excess relative risk (ERR) or excess absolute risk (EAR) per cancer (Rinsky and others 1988; Petersen and others 1990) gray—was provided. The data and confidence intervals are are not included. those given in the cited papers. 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 NUCLEAR INDUSTRY WORKERS studies of all workers included in the national dose registries A direct assessment of the carcinogenic effects of pro- in Canada, Japan, and the United Kingdom. In the USA, tracted, generally low-level radiation exposure can be made combined analyses of the data on workers from Hanford, from studies of cancer risk among workers in the nuclear Rocky Flats, and Oak Ridge National Laboratory (ORNL) industry, many of whom have been exposed to above-back- have been reported by Gilbert and collaborators (1989, ground levels of ionizing radiation over several decades and 1993a). The latest analysis included 35,933 workers, fol- whose exposures have been monitored through the use of lowed until the end of 1986 (Gilbert and others 1993a). A personal dosimeters. Throughout this report, the term study of workers employed in one of 15 commercial nuclear “nuclear industry” will be used to refer to facilities engaged power facilities was also conducted (Howe and others 2004). in the production of nuclear power, the manufacture of The study included 53,698 workers followed up for mortal- nuclear weapons, the enrichment and reprocessing of nuclear ity from 1979 to 1997. fuel, or reactor research. Uranium mining is not included. The British study of the National Registry of Radiation Workers (NRRW; Kendall and others 1992a, 1992b; Little Principal References and others 1993; Muirhead and others 1999) includes 124,743 monitored workers in the above-mentioned U.K. co- Many studies of mortality—and, in some instances, can- horts as well as employees of Nuclear Electric, the Defense cer incidence—among nuclear industry workers have been Radiological Protection Service, and a number of other carried out over the past 20 years. Published studies have nuclear facilities. The latest publication covers follow-up for covered workers in Canada, Finland, France, India, Japan, mortality until the end of December 1992. Combined analy- Russia, Spain, the United Kingdom, and the United States. ses of three U.K. nuclear industry workforces (the Atomic Most have been cohort studies. The main studies in which Energy Authority [AEA], Atomic Weapons Establishment mortality or morbidity has been examined by level of indi- [AWE] and Sellafield) with follow-up extended to the end of vidual radiation dose are listed in Table 8-1. The character- 1988 have also been carried out (Carpenter and others 1994, istics of the cohorts and results are summarized briefly in 1998). Table 8-2. A number of published studies are not described In Canada, the study of the National Dose Registry (NDR) in Table 8-2, for the following reasons: covered 206,620 workers in the industrial, medical, and den- • The studies of Mayak workers in the former USSR are tal fields, as well as nuclear power, followed for mortality described in the next section of this chapter. Many of these through 1987 (Ashmore and others 1998) and cancer inci- workers received mixed exposures to low- and high-LET dence through 1988 (Sont and others 2001). About 25% of (linear energy transfer) ionizing radiation, including con- these were nuclear industry workers, but detailed results siderable doses from internal contamination with pluto- were not presented for this group. The average dose of the nium-239. entire cohort is low (6.6 mSv). The average length of follow-

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OCCUPATIONAL RADIATION STUDIES 191 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, ORNL, Rocky Flats, AEA, AWE, Sellafield, and the Chalk which covered a total of 191,333 person-years of follow-up. River plant of Atomic Energy of Canada Ltd. [AECL]) and A study of mortality in the subgroup of nuclear power indus- from the U.S. Rocky Flats facility (Wilkinson and others try workers registered in the NDR has recently been pub- 1987). Overall, 95,673 workers employed between 1943 and lished (Zablotska and others 2004). The study included 1988 in one of the participating facilities were included. They 45,468 workers monitored for more than 1 year between contributed 2,124,526 person-years of follow-up (an aver- 1957 and 1994. The average cumulative dose was 1.5 mSv. age follow-up of 22.2 years). The collective dose was The average length of follow-up was 13.4 years (607,979 3843 Sv, most of which (98%) was received by men. person-years of follow-up). In Japan, the study (ESGNWJ 1997) covered a large co- Characteristics of Studies of Nuclear Industry Workers hort of 114,900 Japanese nuclear workers. The follow-up time was short (average 4.6 years), and the cumulative dose In the majority of the studies listed above, study subjects was relatively low (average 13.9 mSv). Consequently the are defined as workers employed in the nuclear industry for study had little power to assess possible health effects of whom detailed individual external dose estimates were avail- occupational ionizing radiation exposure; in particular, the able. Exceptions include the Canadian NDR study (Ashmore test for trend for all cancers had a one-sided p-value of 0.65, and others 1998), which included many other types of radia- and the test for trend for leukemia had a one-sided p-value of tion workers, and a number of cohorts (Hanford, ORNL, 0.22 (ESGNWJ 1997). Sellafield, AEA, and AWE) in which both monitored and In addition to the national combined analyses, a multina- nonmonitored workers are included. In the latter studies, es- tional combined analysis was carried out to maximize the timates of risk per unit dose are restricted to monitored work- information from studies of nuclear industry workers (IARC ers, except in the study of ORNL (Wing and others 1991; 1994, 1995; Cardis and others 1995). Individual data from Richardson and Wing 1999b), where doses were estimated seven of the cohorts are included in Table 8-2 (Hanford, for a number of workers who had not been monitored.

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192 BEIR VII TABLE 8-2 Main Characteristics of Principal Studies of Nuclear Industry Workers Average Dates of Dates of No. of Person- Radiation Collective Study Population References Exposure Follow-up Subjects Years Dose (Sv) Dose (Sv) Comments United States Hanford Site Gilbert and 1944–1978 1944–1986 32,643a 0.026 854 Workers employed others (1993b) 6 months or more Oak Ridge Richardson and 1943–1985 1943–1990 14,095 425,486 NA Cohort includes white National Laboratory Wing (1999b) males Oak Ridge Frome and 1943–1985 1943–1984 28,347 603,365 NA (X-10, Y-12) others (1997) Rocky Flats Gilbert and 1951–1979 1952–1983 5,952 81,237b 0.041 241 White males others (1993a) Los Alamos Wiggs and 1943–1977 1943–1990 15,727 456,637 NA White males others (1994) Mound Facility Wiggs and 1947–1979 1947–1979 3,229 54,151 0.030 1625 Monitored white males others (1991b) Savannah River Site Cragle and 1943–1986 1952–1986 9,860 NA 0.041 others (1994) Rocketdyne/AI Ritz and others 1950–1993 1950–1994 4,563 118,749 0.012 (1999a;1999b) Portsmouth Naval Rinsky and 1952–1977 1952–1977 7615c 98,223 0.028 212 White males Shipyard others (1981) United Kingdom Sellafield Douglas and 1947–1975 1947–1988 10,276d 370,329e 0.128 1317 Mortality and others (1994) (1971–86— morbidity study incidence) Omar and 1947–1975 1947–1992 10,382f 415,431 0.130 1352 All workers— others (1999) (1971–86— mortality and incidence) morbidity study AEA Fraser and 1946–1979 1946–1986 39,718 873,796 0.022 Mortality and others (1993) morbidity study AWE Beral and 1951–1982 1951–1982 22,552 419,467 0.003 others (1988) Springfields McGeoghegan 1946–1995 1946–1995 13,960 479,146g 0.020–0.023 and Binks (2000a) Capenhurst McGeoghegan 1946–1995 1946–1995 3,244 334,473g 0.010 32 and Binks (2000b) Canada AECL Gribbin and 1956–1980 1956–1985 8,977 157,101 0.015 Males others (1993) France Electricité de Rogel and others 1961–1994 1961–1994 22,395 5.5 (median) 402 EDF France (EDF) (2005) Combined Cohorts Canadian NDR Ashmore and 1951–1983 1951–1983 206,620 2,861,093 0.063 others (1998) Canadian nuclear Zablotska and 1957–1994 1957–1994 45,468 607,979 13.5 Canadian nuclear workers others (2004) workers continues

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OCCUPATIONAL RADIATION STUDIES 193 TABLE 8-2 Continued Average Dates of Dates of No. of Person- Radiation Collective Study Population References Exposure Follow-up Subjects Years Dose (Sv) Dose (Sv) Comments Sont and others 1951–1983 1969–1988 191,333 2,667,903 0.066 Morbidity study (2001) Combined analyses Carpenter and Varied 1946–1988 75,006 1,800,144 0.037 of U.K. nuclear others (1994) 1946–1988 workers NRRW Muirhead and <1976–1992 <1976–1992 124,743 2,063,300 0.031 3810 others (1999) Combined analyses Gilbert and others Varied Varied 44,943 835,070 0.027 1237 of U.S. workers (1993a) 1944–1979 1944–1986 (Hanford, ORNL, Rocky Flats) U.S. nuclear facility Howe and others 1945–1997 1979–1997 53,698 698,051 25.7 workers (2004) Three-country Cardis and others Varied Varied 95,673 2,124,526 0.04 3843 combined analyses (1995) 1943–1982 1943–1988 (Canada, U.K., U.S.) 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 are worn by workers while they are present in designated the major studies are listed in Table 8-2. In general, expo- radiation areas. Dosimeters are normally placed on the chest, sure in most of these cohorts was predominantly to low lev- and it is usually assumed that the measured radiation dose is els of external radiation (X- and γ-rays and some neutrons). representative of the whole-body dose (i.e., estimates Internal contamination (through inhalation, ingestion, skin “whole-body equivalent dose”); the dose to different parts of absorption, or wounds) by tritium, plutonium, uranium, and the body is assumed to be uniform. other radionuclides occurred in some subgroups of workers. In nearly all cases, dosimeters are sensitive to the pen- etrating photon radiation of intermediate (>100 keV) to higher photon (i.e., X- and γ-rays) energies typical of radia- Assessment of Exposure to Radiation tion fields in the respective facilities. Specialized dosimeters Control of radiation dose to workers in occupational set- and calibration methods are generally needed to measure tings is achieved by demarcating radiation levels in work accurately the dose from low-energy photons, beta, or areas, conducting routine radiation monitoring (e.g., by air neutron radiation present in some occupational environ- sampling and the use of in situ radiation monitors), and by ments. Monitoring for the intake of radioactive material is individual monitoring of workers. The studies of nuclear in- performed by bioassay, by whole-body in vivo counting, or dustry workers considered here are based on workers for by wearing personal air samplers. In most of the facilities whom individual monitoring of dose from external “higher”- that have been the object of the epidemiologic studies de- energy (300–3000 keV) photon radiation was carried out scribed above, measurements of dose to individuals have routinely. generally been recorded on a routine basis using the avail- Individual monitoring at its simplest consists of assigning able dosimetry technology. radiation-sensitive dosimeters to each worker. Dosimeters, Occupational radiation dose data constitute the most com- which consist of one or more of ionization chambers, photo- plete and detailed information currently available to re- graphic film, luminescent phosphors, or electronic devices, searchers for studying the carcinogenic effects of low-dose,

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194 BEIR VII protracted exposures to ionizing radiation. They are gener- The majority of cohort studies collected only information ally presented in the form of annual summaries of doses from that could readily be obtained from employment and dosim- different types of radiation (penetrating photons, beta, and etry records. This consists, in addition to information on where appropriate and measured, tritium and neutrons). individual annual radiation dose from different types of ra- These data were, however, compiled to monitor worker diation, date of birth, date and cause of death, sex, socioeco- exposure for compliance with radiation protection guide- nomic status based on occupational group or education, and lines, which have changed over time, and not specifically for dates of beginning and end of employment. Nested case- epidemiologic purposes. Overall, the accuracy and precision control studies have allowed the exploration of additional of recorded individual doses and their comparability will factors including tobacco smoking and other occupational therefore depend on: exposures. • the dosimetry technology, which includes the physical Results capabilities of the dosimetry system, such as the response to different types and energies of radiation, in particular in In most of the nuclear industry workers studies, death mixed radiation fields; rates among worker populations were compared with na- • the radiation fields in the work environment, which may tional or regional rates. In most cases, rates for all causes include mixed types of radiation, variations in exposure ge- and all cancer mortality in the workers were substantially ometries, and environmental conditions; and lower than in the reference populations. Possible explana- • the administrative practices adopted by facilities to cal- tions include the healthy worker effect and unknown dif- culate and record personnel dose based on technical, admin- ferences between nuclear industry workers and the general istrative, and statutory compliance considerations. population. In most studies where external radiation dose estimates Consequently, detailed examination of dosimetry practices, were available, death rates were also compared in relation to including sources and magnitude of errors, is important in levels of radiation exposure within the study population. For considering whether sufficiently accurate and precise esti- all cancer mortality (excluding leukemia), the estimates of mates of dose can be obtained for use in an epidemiologic radiation-induced excess risk varied from negative to sev- study. eral times greater than those derived from linear extrapola- Information on internal contamination with radionuclides tion from high-dose studies (Table 8-3). Moreover, because other than tritium is generally sparse, particularly in early of the large degree of uncertainty, many of these estimates years, and consists of information on the fact of monitoring were consistent with an even wider range of possibilities, or on a percentage of the annual limit of intake. Very few from negative risks to excess risks at least an order of mag- studies have attempted to reconstruct individual doses from nitude greater than those on which the current radiation pro- nuclides other than tritium. One exception is the study of tection recommendations have been based. Sellafield workers in the United Kingdom, where efforts In most of the large studies of nuclear industry workers, have been made to reconstruct plutonium exposures (Omar estimates of ERR1 per gray (ERR/Gy) have been derived, and others 1999). mostly using Poisson regression. Estimates of excess death In high-dose studies, the majority of excess deaths from rate per 106 person-years (PY) per gray have also been pre- cancer have been demonstrated in subjects exposed to doses sented in some studies. Results of such analyses are shown of at least 1 Sv. There were approximately 3000 such sub- in Tables 8-3 and 8-4 for all cancers excluding leukemia and jects among atomic bomb survivors. Doses received by em- for leukemia, respectively. Table 8-5 is a listing of the re- ployees of nuclear industry facilities are considerably lower. sults from other studies of nuclear workers that could not be In the Sellafield cohort (Douglas and others 1994), in which used in computation of ERRs or EARs.2 the highest doses among the nuclear industry worker studies Cancer mortality was observed to increase significantly have been reported, only about 60 out of more than 10,000 with increasing level of exposure in four studies: AWE individuals monitored for external radiation exposure had (Beral and others 1988), ORNL (Wing and others 1991; received doses of 1 Sv or more, and these doses were accu- Richardson and Wing 1998), Canadian NDR (Ashmore and mulated over the course of a working life. The mean cumu- others 1998), and Rocketdyne (Ritz and others 1999a). The lative radiation dose in the three-country combined analyses ERR estimate based on the three-country combined analysis was 40.2 mSv per worker and the collective dose was was close to zero, but was compatible with a range of possi- 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 dis- 1ERR is the rate of disease in an exposed population divided by the rate tribution of doses was very skewed; almost 60% of subjects of disease in an unexposed population minus 1.0. had cumulative doses less than 10 mSv, 80% were less than 2EAR is the rate of disease in an exposed population minus the rate of 50 mSv, and less than 2% had doses greater than 400 mSv. disease in an unexposed population.

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OCCUPATIONAL RADIATION STUDIES 195 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 Number of Study Population References Cancer Deaths ERR/Sv (90% CI) EAR/104 PY/Sv (90% CI) Comments United States Hanford Gilbert and 1413 –0.0 (<0, 1.9) others (1993b) ORNL Richardson and 879 — 1.21%/10 mGy (SE 0.65) Leukemias included Wing (1999a) 4.98%/10 mGy (SE 1.48) Restricted to dose received after age 45 Oak Ridge Frome and 1134 1.45 (0.15, 3.48)a — Leukemias included Y-10, X-12 others (1997) Rocky Flats Gilbert and 114 <0 (<0, 0) — others (1993a) United Kingdom AEA Fraser and 720 0.8 (–1.0, 3.1)a 20.3 (–26.0, 71.1)a others (1993) AWE Beral and 275 7.6 (0.4, 15.3)a others (1988) Capenhurst McGeoghegan 174 –1.3 (<0, 2.4) Males only and Binks (2000b) Sellafield Douglas and 567 0.11 (–0.4, 0.8) 5.6 (90% CI 15.86, 27.15)b others (1994) Springfields McGeoghegan 939 0.64 (–0.95, 2.7) Males only and Binks (2000a) Canada AECL Gribbin and 221 0.049 (–0.68, 2.17) others (1993) Combined cohorts Canadian NDR Ashmore and 1632 3.0 (1.1, 4.8) — others (1998) Canadian nuclear Zablotska and 531 2.80 (–0.038, 7.13)a workers others (2004) Combined UK Carpenter and 1824 –0.02 (–0.5, 0.6)a –0.68 (–23.3, 20.9)a nuclear industry others (1994, 1998) workforce NRRW Muirhead and 3020 0.086 (–0.28, 0.52)a — others (1999) Hanford, ORNL, Gilbert and 1789 0.0 (<0 .8)a — Rocky Flats others (1993a) U.S. nuclear Howe and 368c 0.506 (–2.01, 4.64)a facility workers others (2004) Three-country Cardis and 3830 –0.07 (–0.39, 0.30) — combined analyses others (1995) (Canada, U.K., U.S.) 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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196 BEIR VII 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 44 –1.1 (<0, 3.0) — others (1993b) ORNL Wing and others 28 6.4 (-11.2, 24.0) (1991) Hanford, ORNL, Gilbert and others 67 –1.0 (<0, 2.2)a — Rocky Flats (1993a) United Kingdom UKAEA Fraser and others 31 –4.2 (-5.7, 2.6) (1993) UKAWE Beral and others (1988) 4 Capenhurst McGeoghegan and 4 –1.27 (<0, 2.75) Males only Binks (2000b) Sellafield Douglas and others 12 13.92 2.47 (90% CI 1.21, NE) Upper bound for EAR (1994) (90% CI 1.94, 70.52) could not be estimated (NE) Springfields McGeoghegan and 23 –1.89 (< –1.97, 13.1) Males only Binks (2000a) Canada AECL Gribbin and others 4 19.0 (0.14, 113) — (1993) Combined Cohorts Canadian NDR Ashmore and others 46 0.4 (–4.9, 5.7) — Males (1998) Canadian nuclear Zablotska and 18 52.5 (0.21, 291)a workers others (2004) Combined U.K. Carpenter and 49 4.18 (0.4, 13.4)a 2.10 (0.4, 3.6)b 2-year lag; adjusted for nuclear industry others (1994, 1998) age, sex, calendar period, workforce social class, and facility NRRW Muirhead and 91 2.55 (–0.032, 7.16) — 2-year lag others (1999) Hanford, ORNL, Gilbert and 67 –1.0 (<0, 2.2)a Rocky Flats others (1993a) U.S. nuclear Howe and 26 5.67 (–2.56, 30.4)a facility workers others (2004) Three-country Cardis and 119 2.18 (0.13, 5.7) — 2-year lag; adjusted for combined analyses others (1995) age, socioeconomic status, (Canada, U.K., U.S.) 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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OCCUPATIONAL RADIATION STUDIES 197 TABLE 8-5 Results of Studies of Nuclear Industry Workers with Individual External Dosimetry that Did Not Provide ERRs or EARs All Cancers Leukemia No. of No. of No. of Country Facility Subjects Deaths Results (90% CI) Deaths Results (90% CI) United States Mound (Wiggs and others 3,229 66 No association with 4 Significant (p < .01) positive 1991a, 1991b) radiation dose trend with radiation dose Los Alamos (Wiggs and 15,727 732 No association with 44 No association with radiation others 1994) radiation dose dose Portsmouth Naval Shipyard 7,615 201 No association with 7 No association with radiation (Rinsky and others 1981) radiation dose dose Rocky Flats (Wilkinson 5,413 50 Slope = –3.65/10 mSv 4 RR = 1.0 (0.8, 9.1) for and others 1987) (–12.02, 4.71) 10mSv vs. <10 mSv Rocketdyne (Ritz and 4,563 258 Significant (p = .036) 28a Significant (p = .003) trend others 1999a) trend United Kingdom BNFL (McGeoghegan and 2,467 —b Significant (p < .01) —b No association with radiation Binks 1999) positive trend when dose doses are lagged by 15 years AWE (Atkinson and others 26,395 1560 No association with 38 No association with radiation 2004) radiation dose dose Slovakia Jaslovske Bohunice power 2,776 14 No association with 0 plant (Gulis 2003) radiation dose France Electricité de France (Rogel 22,395 116 No association with 5 No association with radiation and others 2005) radiation dose dose aHemato- and lymphopoietic cancers. bNot specified. bilities, from a reduction of risk at low doses to risks twice well as in the NRRW cohort (Muirhead and others 1999) those on which current radiation protection recommenda- and the three-country combined analyses (Cardis and others tions are based. 1995). The confidence intervals in these studies were wide, In most studies, analyses of mortality in relation to cumu- and the estimates of risk were consistent with those on which lative external radiation dose were conducted for many spe- current radiation protection recommendations are based. cific types of cancer. These studies have generally not shown Statistically significant (p < .05, one-sided) positive asso- significant increases in risk among exposed workers for most ciations between cumulative external radiation dose and cancer types examined, although a few positive associations mortality from multiple myeloma were found in the Hanford have been found (Table 8-3). (Gilbert and others 1989) and Sellafield (Douglas and others For leukemia, risk estimates varied considerably from 1994) studies. A similar association was also found in the study to study (Table 8-4). In the pooled study of workers in NRRW (Muirhead and others 1999) and three-country analy- the United States (Gilbert and others 1993a), the estimate of ses (Cardis and others 1995), largely reflecting the previ- ERR per gray based on the combined data was negative, ously reported associations in individual cohorts. The asso- although the upper confidence bound was slightly larger than ciation in the Hanford study was not significant when the estimate currently recommended by the International follow-up was extended to 1986 (Gilbert and others 1993b). Commission on Radiological Protection (ICRP 1991). By An association between radiation dose and mortality from contrast, significant positive associations were observed in cancer of the prostate was found in two studies, the AEA AECL and nuclear worker studies in Canada (Gribbin and (Beral and others 1985; Fraser and others 1993) and the others 1993; Zablotska and others 2004) and in the U.K. AWE (Beral and others 1988); in AWE workers it was sta- study of Sellafield workers (Douglas and others 1994), as tistically significant only among workers who had been

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198 BEIR VII monitored for exposure to radionuclides (Rooney and others cohort had to be restricted to those who were employed in 1993) in the period 1946–1979. No such increase was ob- the previous 5 years; hence the follow-up time of this cohort served in the NRRW (Muirhead and others 1999), which is very short, and older workers as well as workers with included all of the monitored workers in these two studies. higher doses (who were employed in early years and left A significant positive association with lung cancer was employment more than 5 years in the past) have been ex- observed in the AWE and ORNL studies (Beral and others cluded from the follow-up. Consequently the study has little 1988; Wing and others 1991), particularly among those ex- power to estimate possible health risks associated with occu- posed to radionuclides in the AWE and in nonmonthly work- pational radiation exposure. ers at ORNL. Information on tobacco smoking was available systematically in these studies. A few other significant asso- Adequacy of the Dose Estimates ciations were reported in single studies (Table 8-4). Given the number of associations examined, some of the signifi- High-Energy Photon Doses cant results observed may have been due to chance. Several points must be kept in mind when making com- The accuracy and precision of individual dose estimates parisons of these worker-based risk estimates and confidence in the nuclear industry is a function of time, place, radiation intervals with those based on high-dose-rate studies. The energy and quality, the geometry of the radiation exposure, most important are possible biases and uncertainties in dose and the location of the dosimeter on the body of the worker. estimates, errors in outcome data, and inadequate adjustment Efforts were made in some of the studies (AEA, Sella- for confounders. field, ORNL, U.S. DOE combined analyses, three-country study, Saclay site in France) to assess the importance of do- simetric errors due to administrative practices adopted by Design Issues facilities to calculate and record personnel dose based on Among the very large and potentially most informative technical, administrative, and statutory compliance consid- cohort studies reviewed in this chapter, two present a num- erations (Adams and Langmead 1962; Smith and Inskip ber of problems that limit their informativeness. In the Cana- 1985; Taylor 1991; Telle 1995; Tankersley and others 1996; dian NDR study (Ashmore and others 1998), the very low Mitchell and others 1997; Watkins and others 1997; Telle- standardized mortality ratio (SMR)3 for all-cause mortality Lamberton and others 1998). Results of reanalyses of data (61) suggests that record linkage procedures between the using different approaches to estimate doses from missing Canadian National Dose Registry and the Canadian Mortal- dosimeters or below-threshold readings have yielded similar ity Data Base may have been imperfect. There could have results to the analyses based on original data (Inskip and been some confounding of the dose-response because of as- others 1987; Little and others 1993). sociations between the probability of successful linkage and In the three-country combined analyses, a retrospective factors (e.g., socioeconomic status [SES]) associated with dosimetry study was carried out to identify the various occupational radiation dose. This is the only study in which sources of biases and random errors in dosimetry for work- associations have been observed between radiation dose and ers in each of the facilities included and to estimate the mag- all-cause mortality, all cancer mortality (without any clear nitude of these errors. As a result, it was concluded that for relation to specific cancers), mortality due to cardiovascular the majority of workers with predominant high-energy (300– diseases (males and females), and fatal accidents (males 3000 keV) photon exposures at levels greater than the detec- only). Moreover, no information is available on SES—a tion threshold of the dosimeter, there is no strong reason to factor that has been shown in a number of previous cohorts believe that available dose estimates substantially underesti- to be a confounder of the association between radiation dose mate or overestimate deep dose. The dose estimates were and cancer risk. Almost three-quarters of the cohort consists judged to be compatible across facilities and over time. How- of radiation workers employed in different settings (den- ever, available dose estimates may have overestimated dose tistry, medicine, industrial radiography), where radiation to the bone marrow by up to 20%. Estimation of leukemia control may be very different (possibly less uniform and sys- risk adjusting for this overestimation yielded an ERR of tematic due to the much smaller numbers of persons moni- 2.6 Sv–1 instead of 2.2. For deep organs, the factor is likely tored in individual workplaces) than in the nuclear industry. to be smaller, of the order of several percent. Random errors In the Japanese NDR study (ESGNWJ 1997), SES infor- in dose estimates are likely to bias the risk estimates down- mation is also not available. Further, because of difficulties wards, compared to estimates from high-dose studies, which in carrying out vital status follow-up in Japan, the very large 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 predomi- 3SMR is the ratio (multiplied by 100) of the mortality rate from a disease nant higher-energy photon exposure (Fix and others 1997). in the population being studied divided by the comparable rate in a standard At the Hanford plant in the United States, based on ex- population. periments and expert assessments, efforts were made to

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OCCUPATIONAL RADIATION STUDIES 199 quantify systematic errors related to the dosimetry technol- cupational exposures could not be obtained retrospectively ogy and radiation fields as well as errors related to labora- for all members of the cohort. In the three-country combined tory practices (Fix and others 1994, 1997; Gilbert 1998). analyses, there was little indirect evidence for an association When these errors were taken into account in the risk esti- between cumulative dose and mortality from smoking-re- mation process, it resulted in a widening of the confidence lated cancers, respiratory diseases, or liver cirrhosis; thus, it intervals around the ERR (Gilbert and Fix 1995) as shown in is unlikely that smoking or alcohol consumption are strongly Table 8-6. 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 Doses from Neutrons, Low- and Very-High-Energy Photons, leukemia and lung cancer were nearly identical (Cardis and and Internal Contamination others 1995): also, the results of two studies, carried out In the three-country study, efforts were also made to iden- within the Hanford (Petersen and others 1990) and AEA tify workers with substantial doses from radiations other than (Carpenter and others 1989) cohorts, respectively, showed high-energy photons (mainly from neutrons, low-energy ra- little evidence for an association between smoking and oc- diation, and contamination with radionuclides, particularly cupational radiation dose. A positive association between plutonium), for whom recorded dose estimates may be in smoking and occupational radiation dose was found in the error. Although it was not possible to identify all such work- AECL cohort in Canada (Howe and others 1987). ers, risk estimates based on restricted dosimetry analyses, which excluded all such workers who could be identified, Socioeconomic Status did not differ greatly from those based on the standard ap- proach (-0.04 and 2.05 Sv–1 respectively, for all cancers ex- A positive association between radiation dose and mor- cluding leukemia and for leukemia excluding chronic lym- tality from circulatory disease was observed in the four co- phocytic leukemia (CLL) compared to -0.07 and 2.18 Sv–1 horts included in the three-country study in which informa- in the standard population). In addition, the estimate of risk tion on SES was least detailed (Rocky Flats, Sellafield, for all cancers excluding leukemia and lung cancer (the or- AECL, Canadian NDR). It may reflect residual confounding gan that would receive the majority of the dose from pluto- by life-style factors for which the SES variable is an inad- nium contamination) was identical to that of all cancers ex- equate proxy. cluding leukemia (–0.07 Sv–1; 90% CI –0.39, 0.30). It is therefore unlikely that the risk estimates in this study are Radionuclides in the Working Environment substantially biased by inclusion in the analyses of a minor- At uranium fuel production facilities, inhalation of air- ity of workers with dose from neutrons, low-energy photons, borne uranium dust may represent an important potential and internal contamination (Cardis and others 1995). source of radiation exposure. Workers in these facilities have two main possible sources of radiological exposure to tis- Possible Confounding and Modifying Factors sues of the whole body: external γ-ray exposure and internal depositions that deliver radiation doses (mainly from Tobacco Smoke α-particles) primarily to the lung and lymphatic system. If the uranium dust is soluble, exposure of other tissues may As in most occupational cohort studies, information on also occur such as liver, kidney, and bone, although organ life-style factors such as smoking habits, diet, and other oc- doses would be expected to be small. Low-LET radiation risk estimates for tumors in these organs are possibly con- founded by high-LET radiation exposure for workers at ura- nium production facilities, since workers with a significant TABLE 8-6 Estimates of the ERR per Sievert with 90% dose from internal contamination are often persons with sub- CIs for the Hanford Worker Study Based on Recorded stantial external exposure. A number of studies of such workers Doses and Based on Estimated Organ Doses have been reviewed (Cardis and Richardson 2000; NRC 2000). All Cancers Leukemia Comparison of findings among uranium-processing fa- Excluding Leukemia Excluding CLL cilities is complicated by the fact that processes and histori- cal periods of operation have differed among facilities, lead- Recorded doses 0.23 –0.9 ing to differences in exposure conditions and follow-up (90% CI <0, 1.5) (90% CI <0, 2.7) among cohorts. Further, assessment of past internal uranium Organ doses (corrected 0.20 –1.3 exposure of nuclear workers is complicated by the method- for systematic errors (90%CI <0, 1.7) (90% CI <0, 3.6) ological difficulties of internal dosimetry, as well as by inad- related to radiation fields) equate historical information with which to quantify internal radiation doses accurately. These exposure measurement NOTE: CLL = chronic lymphocytic leukemia.

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200 BEIR VII problems pose significant difficulties for epidemiology: the Cancer mortality and incidence was studied among inability to classify workers accurately by level of internal Sellafield workers in relation to exposure to plutonium and radiation exposure may lead to confounding of the analyses to external low-LET radiation (Omar and others 1999). A of association between external low-LET radiation dose and significant association between mortality from leukemia ex- cancer risk. cluding CLL (13 deaths) was seen in relation to external Lung cancer has been the primary outcome of interest in radiation dose using a 2-year lag, as had been seen in the studies of workers in fuel enrichment and production facili- previous follow-up of this cohort (Douglas and others 1994). ties. Lung cancer mortality was found to be significantly When analyses were restricted to plutonium workers and elevated, compared to national rates, among workers in took into account both external low-LET radiation dose and nuclear fuel processing facilities in three reports (Loomis estimated plutonium dose, the association was no longer sta- and Wolf 1997; Checkoway and others 1988; Frome and tistically significant, based on six deaths. others 1990), but not in others (Brown and Bloom 1987; Dupree and others 1987, 1995; Ritz and others 1999b). An Other Occupational Exposures association between external low-LET radiation dose and lung cancer mortality was observed in two cohorts in the Wing and colleagues (1993) evaluated the effect of po- United States (Fernald and Y-12; Checkoway and others tential exposure to beryllium, lead, and mercury in the ORNL 1988; Ritz and others 1999a), and an association with lung cohort by identifying workers with potential for these expo- cancer incidence (using a 20-year lag) was observed in one sures from employment records. Adjustment for these po- study in the United Kingdom (McGeoghegan and Binks tential exposures had little effect on the radiation risk esti- 2000a). No association was found in other papers on the U.S. mates. The interpretation of these results is limited by the (Hadjimichael and others 1983; Ritz and others 2000) and absence of individual exposure estimates for the chemicals U.K. (McGeoghegan and Binks 2000b) cohorts. No infor- considered. mation on dose to the lung from internal contamination was Rinsky and colleagues (1981) considered exposure to a available for analysis in these studies. In studies where esti- number of workplace carcinogens in a case-control study of mation of dose to the lung from internal contamination was lung cancer among civilian employees of the Portsmouth carried out, an association was observed at Y-12, but not at naval shipyard. Asbestos and welding by-products were Rocketdyne (Ritz and others 1999a). In contrast, a U.S. found to confound the association between radiation expo- multifacility case-control study of lung cancer among sure and lung cancer risk in this population, where radiation workers exposed to uranium dust at TEC, Y-12, Fernald, workers appear to be more heavily exposed to asbestos and and Mallinckrodt found no such association; there was a sug- welding fumes than other workers. The unadjusted lung can- gestion, however, of positive associations among workers cer odds ratio for workers with a cumulative dose of 10– hired over age 45 (Dupree and others 1995). Therefore, risk 49.99 mSv was 1.8 (95% CI 1.1, 3.1) compared to workers estimates for low-LET radiation-induced lung cancer risk in with no history of radiation exposure; adjustment for asbes- these cohorts should be treated with caution. tos and welding fumes reduced it slightly to 1.7 (95% Following the observation of increased prostate cancer CI 1.0, 2.9). mortality related to cumulative external radiation dose in the AEA (Beral and others 1988; Rooney and others 1993) a Modifiers of Radiation Risk nested case-control study was conducted of prostate cancer risk among employees of that facility. The study showed that Several authors have reported an association between age exposure to five radionuclides (tritium, chromium-51, iron- at exposure and/or attained age and the risk of radiation- 59, cobalt-60, and zinc-65), evaluated separately, was associ- induced cancer. This has been reported in the Hanford, ated with an increased risk of prostate cancer. Analyses of the ORNL, and Rocketdyne cohorts (Gilbert and others 1993a; association between external radiation dose and prostate can- Stewart and Kneale 1996; Richardson and Wing 1999a; Ritz cer risk were carried out both for workers with probable ex- and others 1999b), but not in five other cohorts in which it posure to these radionuclides and for those who had no such was considered—Rocky Flats, AECL, AEA, AWE, and exposure. The association between external dose and prostate Sellafield (Cardis and others 1995; IARC 1995). cancer was restricted to those with radionuclide exposure. The three-country and the NRRW studies (Cardis and In the Combined UK Industrial Workforce study, Car- others 1995; Muirhead and others 1999) of nuclear industry penter and colleagues (1998) carried out analyses of cancer workers currently provide the most comprehensive and pre- mortality in relation to external radiation dose in two cise direct estimates of the effects of protracted exposures to groups—those who had been monitored for internal radio- low levels of low-LET radiation. Although the estimates are nuclide contamination and those who had not. A positive lower than the linear estimates obtained from studies of association was seen in both groups of workers, although it atomic bomb survivors, as seen in Table 8-7, they are com- was statistically significant only among those who had been patible with a range of possibilities, from a reduction of risk monitored for internal contamination. at low doses, to risks twice those on which current radiation

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OCCUPATIONAL RADIATION STUDIES 201 TABLE 8-7 Comparison of Estimates of ERR/Gy The first estimates of risk from external exposure were Between Major Nuclear Industry Workers Combined reported by Shilnikova and colleagues (2003). Analyses fo- Analyses and the Atomic Bomb Survivors cused on leukemia (excluding CLL); cancers of the lung, liver, and bone (analyzed as a group); and solid cancers ex- All Cancers but Leukemia, cluding lung, liver, and bone (also analyzed as a group). Study Population Leukemia Excluding CLL Lung, liver, and bone are the organs that receive the largest doses from plutonium, and excess cancers in all three organs Atomic bomb survivorsa 0.24 (0.12, 0.4) 2.2 (0.4, 4.7) have been linked clearly to plutonium exposure among Nuclear workers Mayak workers (Gilbert and others 2000; Koshurnikova and Three-country study –0.07 (–0.39, 0.30) 2.2 (0.1, 5.7) others 2000; Kreisheimer and others 2000). Analyses were NRRW 0.09 (–0.28, 0.52) 2.6 (–0.03, 7.2) adjusted for internal exposure to plutonium by using the es- timated body burden for workers who had plutonium-moni- aBased on male atomic bomb survivors, aged 20–60 years at exposure, toring data and by using a plutonium surrogate variable for as presented by Muirhead and others (1999). workers who were not monitored for plutonium. The pluto- nium surrogate variable was developed recently from de- tailed work histories. For leukemia, the estimated ERR/Gy was 6.9 (90% CI protection recommendations are based. Overall, they do not 2.9, 15) for the period 3–5 years after exposure and 0.5 (90% suggest that current radiation risk estimates for cancer at low CI 0.1, 1.1) for the period 5 or more years after exposure. levels of exposure are appreciably in error. Uncertainty con- The estimate based on the entire period was 1.0 (90% CI 0.5, cerning the exact size of this risk, remains, however, as indi- 2.0). There was no statistically significant departure from cated by the width of the confidence intervals presented. linearity and no evidence of modification by sex or age at hire. Estimates and confidence intervals for the solid cancer WORKERS FROM THE MAYAK FACILITY end points are shown in Table 8-8. For these end points, lin- A cohort of about 21,000 Russian nuclear workers who ear-quadratic functions provided significantly better fits than worked at the Mayak plutonium production complex be- linear functions with a “downturn” in the dose-response at tween 1948 and 1972 is under study. The Mayak complex, high doses. This may have resulted from overestimation of which is located in the Chelyabinsk region of the Russian doses of certain workers in early years due to inadequacies Federation, includes three main plants: a reactor complex, a in early film dosimeters. If this is the case, estimates of the radiochemical separation plant, and a plutonium production linear term from the fitted linear-quadratic function may be plant. Workers at all three plants had the potential for expo- more reliable. The estimates for cancers of the lung, liver, sure to external radiation, and workers at the radiochemical and bone were higher than those for other organs, possibly and plutonium production plants also had the potential for because the adjustment for plutonium exposure was less ad- exposure to plutonium. Recently, data on workers at two equate for these cancers. There was no evidence of modifi- auxiliary plants, who had much less potential for exposure, cation of the dose-response by sex, age at hire, or time since have been added to the cohort under study to expand the exposure. comparison group. As for other nuclear worker cohorts, esti- mates of annual external doses are available from individual film badge monitoring data. Some workers were also moni- tored for plutonium exposure; however, since routine testing based on large urine samples did not begin until about 1970, TABLE 8-8 Estimated ERR/Gy for Solid Cancers Among only about 40% of workers with the potential for such expo- Mayak Workers sure have been monitored. External exposures and exposures of Mayak workers to ERR/Sv (90% CI) plutonium far exceed those of other nuclear worker cohorts discussed previously in this chapter. For example, for the Lung, Liver, Other Solid All Solid Model or Bone Cancers Cancers nearly 11,000 monitored workers hired before 1959, the mean cumulative external dose was 1.2 Gy, more than an Linear 0.30 0.08 0.15 order of magnitude higher than any of the cohorts described (0.18, 0.46) (0.03, 0.14) (0.09, 0.20) in Table 8-2. Thus, the Mayak cohort offers a unique oppor- Linear quadratica 0.54 0.21 0.30 tunity to obtain reasonably precise estimates of risks from (0.27, 0.89) (0.06, 0.37) (0.18, 0.43) medium- to high-dose protracted external exposure that can then be compared to estimates based on acute exposure, such aEstimates are for the linear coefficient of a fitted linear-quadratic func- as those obtained from A-bomb survivors. tion.

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202 BEIR VII Summary 2. the “evacuees” who were evacuated from the town of Pripyat and the 30 km zone around the Chernobyl reactor in Studies of workers employed at the Mayak complex in April–May 1986; the Russian Federation offer a unique opportunity, because 3. the residents of the “strict control zones”—those of the magnitude of the doses received (mean cumulative members of the general population who have continued to external dose of 1.2 Gy among monitored workers hired be- live in the more heavily contaminated areas (with levels of fore 1959), to obtain reasonably precise estimates of risk 137Cs deposition greater than 555 kBq m–2), typically within from medium- to high-dose protracted external exposures. a few hundred kilometers of the Chernobyl Nuclear Power Substantial doses from plutonium have also been received Plant (NPP). Within these areas, radiation monitoring and by a number of these workers. Estimates of the radiation- preventive measures have been taken to maintain doses related risks of leukemia; solid cancers; and lung, liver, and within permissible levels; and bone cancer have been derived from this cohort. Uncertain- 4. the general population of the contaminated territories ties in external dose estimates and in plutonium doses to in the three countries. specific organs must be considered in the interpretation of these results. Further studies of this population will be im- The “liquidation” of the consequences of the Chernobyl portant to understand the effects of protracted exposure. accident lasted for about 3 years (1986–1989). During that time, different tasks were carried out, including the initial CHERNOBYL CLEANUP WORKERS localization of the catastrophe (firefighting; closing down unaffected units of the power plant); evacuation of Pripyat The Chernobyl accident resulted in widespread radioac- and the population in the 30 km zone; decontamination of tive contamination of areas populated by millions of people the inside of the Chernobyl NPP buildings, as well as the in the three most affected countries of Belarus, the Russian roofs of nearby buildings and nearby territories; renovation Federation, and Ukraine. The populations at risk can be sepa- and maintenance of the other blocks of the power plant; con- rated into the following groups (see Table 8-9): struction of the sarcophagus; actions to decrease the spread of radioactive materials in the environment; safeguard of the 1. the “liquidators,” also referred to as “cleanup work- 30 km zone and settlements and miscellaneous activities in ers,” include persons who participated in the cleanup of the the 30 km zone (health care, ecological monitoring, bringing accident (cleanup of the reactor; construction of the sar- in food, water, etc., for the liquidators). Different groups of cophagus; decontamination; building of roads; destruction liquidators were involved in these tasks; they worked under and burial of contaminated buildings, forests, and equip- differing conditions of radiation monitoring and safety and ment), as well as many others, including physicians, teach- were exposed to various types and levels of radiation. From ers, cooks, and interpreters who worked in the contaminated 600,000 to 800,000 persons took part in the cleanup activi- territories; ties 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. TABLE 8-9 Estimates of Collective Effective Doses for Follow-up Chernobyl Population Groups of Interest In 1987, an “All-Union Distributed Registry” was estab- Collective Effective lished following a directive of the Ministry of Public Health Population Number Dose (Sv) of the USSR (Tsyb and others 1989). The objective was to set up a comprehensive registration and active follow-up Evacuees 135,000 1,300 system for the persons most affected by the Chernobyl acci- Liquidators (1986–1987) 200,000 20,000 dent, including the liquidators. This system foresees an Persons living in annual medical examination in which individuals are exam- contaminated areasa ined systematically by a general practitioner and a number Deposition density of of different specialists. All data on diseases diagnosed dur- 137Cs >15 Ci km–2 270,000 10,000–20,000 ing the annual medical examination, as well as any other Deposition density of time during the year, are sent to the Chernobyl Registry for 137Cs>1 to 15 Ci km–2 3,700,000 20,000–60,000 inclusion in the registry database. A study in Russia (Cardis and Okeanov 1996) indicates that the diagnostic information aDoses are for 1986–1995; over the longer term (1996–2056) the collec- in the Chernobyl Registry is not always completely accurate. tive dose will increase by approximately 50%. The lack of verification and quality control is actively being SOURCE: Cardis and others (1996). remedied but must be kept in mind when interpreting results

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OCCUPATIONAL RADIATION STUDIES 203 of studies of cancer frequency among exposed populations tive effective dose would be approximately 20,000 Sv. Some in these countries. Results from this follow-up may also be workers received their dose in a few minutes—for example biased because participation in the annual examination may working on the roof of the reactor—while others received it be related to illness and/or to level of exposure. over months or even years, and the predominant radiation Means also exist in the affected countries to carry out type and route of exposure varied according to the time and “passive” follow-up of exposed persons and of the general activity of liquidators. population with the use of population registries—of mortal- Dose estimates have generally been derived in one of ity, cancer, and other diseases. In each country of the former three ways: USSR, population registration is carried out at the local level in the address bureaus (where the addresses of current resi- 1. individual dosimetry: the liquidator was given a per- dents are kept) and the ZAGS (buro zapicii akta grazh- sonal dosimeter; danskovo sostoyania), which compiles all information about 2. group dosimetry: an individual dosimeter was assigned birth, marriage, divorce, and death of persons living in the to one member of a group of liquidators; or administrative area. No centralized registry exists, however, 3. itineraries: measurements of γ-ray levels were made at and results of a pilot study (Cardis and Okeanov 1996) indi- various points where liquidators worked, and an individual’s cate that considerable time and effort may be needed to trace dose was estimated as a function of the points where he or subjects who have moved from one area to another. she worked and the time spent in these places. A computerized national Cancer Registry has been func- tioning in Belarus since the 1970s and registers all cases of Liquidators are in principle included in the State Cher- malignant neoplasms. A comprehensive registry of hemato- nobyl Registries of Belarus, Russia, and Ukraine. Doses for logical diseases also exists in Belarus, in the Institute of a substantial proportion of them are missing from these reg- Haematology and Blood Transfusology. In Russia and the istries. Liquidators who worked in the first year generally Ukraine, no centralized cancer registration system was in had higher recorded doses than those who worked in subse- place at the time of the accident. Work has been carried out quent years. The level of dosimetric control and the adequacy in both countries to set one up—at least in contaminated of dose estimates vary between civilian liquidators (construc- areas in Russia (Okeanov and others 1996; Storm and others tion workers, logistic support), military liquidators (soldiers 1996)—and quality control activities are continuing. and officers who worked in decontamination, dosimetric Information is also available systematically on the gen- control, and evacuation), and radiation specialists. eral (i.e., not only cancer) morbidity of the population of the three countries. In the countries of the former USSR, re- Results gional outpatient clinics systematically collect information on disease diagnoses on all the residents of the region they Increases (doubling or tripling) in the incidence of leuke- cover (not only those included in the Chernobyl Registry). mia and thyroid cancer have been observed in most of the This information is summarized locally and is sent on spe- studies of liquidators from Belarus, Russia, and Ukraine. cial statistical reporting forms at yearly intervals to the Min- Increases in leukemia risk are not unexpected since predic- istry of Health. These forms contain information about the tions from risk estimates in atomic bomb survivors have number of cases of acute and chronic diseases diagnosed in a shown that if the experience of the A-bomb survivors is ap- given year in the population in all areas of the country. This plicable to the Chernobyl situation, a tripling of leukemia information is not broken down by age or sex. No verifica- mortality could be expected in the first 10–12 years follow- tion of completeness or duplicates is possible. This passive ing exposure (Cardis and others 1996). system of collecting morbidity data on the population con- These results are difficult to interpret since, as indicated trasts with the active follow-up carried out, as described above, the follow-up of liquidators is much more active than above, for persons included in the Chernobyl Registry. Com- that of the general population in the three countries. There parisons of morbidity based on these sources must therefore are questions about the adequacy and completeness of the be interpreted with caution. diagnostic information on liquidators in the Chernobyl Reg- istry (Cardis and others 1996). For thyroid cancer in adults, the depth of screening to which the liquidators are subjected Radiation Doses to Different Groups: Dose Levels and may greatly influence the observed incidence. Available Estimates In a case-control study based on the limited dosimetric The dosimetric information available for liquidators is data of the Chernobyl Registry in Russia, no significant as- subject to controversy because personal dosimeters in use in sociation was seen between the risk of leukemia and radia- the early days after the accident were too few and generally tion dose (Ivanov and others 1997a, 1997b). A recent cohort too sensitive. A reasonable estimate of the average dose re- study of Russian liquidators showed no association between ceived by the group of 200,000 people who worked in 1986– external radiation dose and risk of thyroid cancer among 1996 is 100 mSv (Ivanov and others 1996). Thus, the collec- 72,000 liquidators from six regions (Ivanov and others

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204 BEIR VII 2002); no information on internal dose from iodine isotope ies to detect an association with ionizing radiation has been was available in this study. limited by several factors. Few studies have included inter- It is noteworthy that no increase in the incidence of leuke- nal comparisons, basing results instead on proportional mor- mia or thyroid cancer has been reported to date among Baltic tality ratios, SMRs, or standardized incidence ratios. As a country liquidators (Kesminiene and others 1997; Rahu and group, pilots and flight attendants differ appreciably from others 1997). These findings do not contradict the findings the general population. Pilots and other aircrew members reported in Belarus, Russia, and Ukraine in that the number are required to be very healthy and undergo frequent medi- of liquidators in the Baltic countries is small, and the results cal checkups, leading to the possibility of enhanced early are also consistent with a radiation-related increase. detection of cancers in this occupational group. Disrupted At this time, no conclusion can be drawn concerning the circadian rhythms and, in females, relatively late age of first presence or absence of a radiation-related excess of cancer— parity are other characteristics that complicate the choice of particularly leukemia—among Chernobyl accident recovery a suitable comparison group. Increased sun exposure, expo- workers. There is a pressing need for well-designed, sound sure to elevated ozone levels, fuel exhaust fumes, and analytical studies of recovery workers from Belarus, Russia, electromagnetic fields are factors that may also confound Ukraine, and the Baltic countries, in which special attention any relationship observed between adverse health effects is given to individual dose reconstruction and the effect of and cosmic radiation. Moreover, small study group sizes screening and other possible confounding factors. 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 Summary have sufficient power and precision to detect so small an Studies of Chernobyl cleanup workers offer an important association has been questioned. Based on published values opportunity to evaluate the effects of protracted exposure in of annual radiation exposure of aircrew flying at high alti- the low- to medium-dose range. No reliable risk estimates tudes, Boice and colleagues (1992) estimated that a flying can be drawn at present from studies of these workers, how- career of 20–30 years duration would result in only an 80– ever, because of the difficulties of follow-up and lack of vali- 180 mSv cumulative dose, corresponding to a relative risk dated individual dose estimates. (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 AIRLINE AND AEROSPACE EMPLOYEES which can contribute as much as half of the total equivalent Airline pilots and flight attendants are exposed to in- dose at typical flight altitudes (Boice and others 1992; creased cosmic radiation during flights. In 1991, the ICRP Hammer and others 2000). The choice of an appropriate recommended that exposures to natural cosmic radiation weighting factor for the conversion of neutron dose esti- should be considered occupational exposures for aircrews mates to equivalent doses is thus crucial for dosimetry in (ICRP 1991). Although aircrew members are not thought to this occupational group and for assessment of the contribu- exceed the National Council on Radiation Protection and tion of low-LET γ-radiation to any adverse health effects. Measurements (NCRP 1995) recommendation for occupa- At present, the evidence for an adverse health effect in air- tionally exposed workers of 20 mSv per year averaged over crews due to ionizing radiation is inconclusive. 5 years, they do exceed the safety level set for the general public (1 mSv per year). The exposure varies with altitude, Summary latitude, and solar flare activity. Solar activity varies on an 11-year cycle; however, prediction of short-term intense pe- Studies of airline and aerospace employees do not cur- riods of activity is not possible. At 41,000 feet over the poles, rently provide estimates of radiation-related risks because the equivalent dose may vary from a norm of about 12 µSv dose estimates have not been used in the studies to derive to an extreme of 100 µSv (Friedberg and others 1989). The quantitative risk estimates. mean annual dose from galactic cosmic radiation can be modeled using knowledge of altitude, latitude, solar activity, MEDICAL AND DENTAL OCCUPATIONAL EXPOSURES and the Earth’s geomagnetic field. Friedberg and colleagues (1989) estimated the annual equivalent doses that would be Early studies of patterns of mortality among radiologists received on 32 U.S. domestic and international flight routes and other physician specialists produced a suggestion of an as 0.2–9.1 mSv, considerably less than recommended annual excess risk of specific cancers. Excess mortality from leu- adult occupational exposures. kemia and lymphoma, especially multiple myeloma, and Several review articles have been published recently on also from skin, lung, pancreatic, and prostate cancer (e.g., epidemiologic studies of the occupational cancer risk for pi- Matanoski and others 1975a, 1975b; Smith and Doll 1981; lots and flight attendants (Blettner and others 1998; Blettner Logue and others 1986; Wang and others 1988) have been and Zeeb 1999; Boice and others 2000). The ability of stud- suggested, although findings were not consistent across

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OCCUPATIONAL RADIATION STUDIES 205 studies for all cancers. Matanoski and colleagues (1987) re- estimated using cancer incidence rates from the Danish Can- ported higher overall mortality and higher cancer mortality cer Registry. The overall relative risk was 1.07 (95% CI in radiologists compared to other specialists with lower ex- 0.91, 1.25) for all cancers, and no significant dose-response pected exposures. was observed. The risks for cancers that are considered ra- A survey of the health of radiologic technologists (Boice diation sensitive were not elevated. and others 1992) gathered information on risk factors in- Berrington and colleagues (2001) reported the results of cluding smoking status, reproductive history, use of oral 100 years of follow-up of British radiologists who regis- contraceptives, personal exposure to radiographs, height, tered with a radiological society between 1897 and 1979 and weight, use of hair dye, and postmenopausal estrogens, and who were followed until January 1, 1997. A progressive in- family and personal medical history of cancer. Members of crease was observed in the SMRs for cancer with number of the study population (n = 143,517, registered for more than years since first registration. It appears that excess risk of 2 years with the American Registry of Radiologic Technolo- cancer mortality in the period more than 40 years after first gists, ARRT) were predominantly female and white. Per- registration is likely a long-term effect of radiation expo- sonal dosimetric information was available for 64% of all sure for radiologists registering between 1921 and 1954. Ra- the registered technologists, but only 34% of the breast can- diologists whose first registration was after 1954 demon- cer cases and 35% of the controls. Cases and controls were strated no increase in cancer mortality, possibly because of generally older and more likely to have stopped work before their lower overall radiation exposure. computerized records of dosimetry information were begun in 1979. Occupational exposure was estimated through the SUMMARY number of years worked as a technologist obtained from questionnaire data. Epidemiologic studies of radiation workers and other A cohort study using the ARRT database (Doody and persons exposed to ionizing radiation in the workplace others 1998) reported SMRs and RRs adjusted for age, cal- started in the late 1950s with the study of British radiolo- endar year of follow-up, and gender. No significant excess gists. Since then, numerous studies have considered the mortality among radiological technologists was observed mortality and cancer incidence of various occupationally for lung cancer, breast cancer, or leukemia. The SMR for all exposed groups in medicine, industry, defense, research, malignant neoplasms exhibited a significant trend with the and aviation. number of years certified (p < .001), as it did for breast can- Studies of occupationally exposed groups are, in prin- cer. In the absence of complete personal dosimetry informa- ciple, well suited for the direct estimation of the effects of tion, accurate estimates of risk due to exposures to ionizing low doses and low dose rates of ionizing radiation. Poten- radiation are not possible. tially, the most informative studies at present are those of Yoshinaga and colleagues (1999) reported results from a nuclear industry workers (including the workers of Mayak retrospective cohort study of radiological technologists in in the former USSR), for whom individual real-time esti- Japan. External comparisons were also made with all work- mates of doses have been collected since the 1940s with the ers and with professional and technical workers to address use of personal dosimeters. More than 1 million workers the issue of the healthy worker effect. The study used all have been employed in this industry since its beginning. Japanese men as the external comparison group; the SMR However, studies of individual worker cohorts are limited for all cancers in this study was 0.81 (95% CI 0.73, 0.95). in their ability to estimate precisely the potentially small Although elevated SMRs were observed for cancers of the risks associated with low levels of exposure. Risk estimates colon, skin, lymphoma, multiple myeloma, and leukemia, from these studies are variable, ranging from no risk to risks none was statistically significant. The SMR for leukemia an order of magnitude or more than those seen in atomic was significant in comparison to the total workforce as the bomb survivors. reference group (SMR = 1.99; 95% CI 1.09, 3.33) and also Combined analyses of data from multiple cohorts offer for professional and technical workers as the reference an opportunity to increase the sensitivity of such studies and group (SMR = 1.82; 95% CI 1.00, 3.06). No quantitative in- provide direct estimates of the effects of long-term, low- formation on dosimetry was given in the report, nor was dose, low-LET radiation. The most comprehensive and pre- there an internal comparison, thus limiting the usefulness of cise estimates to date are those derived from the U.K. Na- the report for the estimation of risk. tional Registry of Radiation Workers and the three-country Since 1990, a number of studies of radiologists have been study (Canada-United Kingdom-United States), which have published that utilized measurements of individual exposure provided estimates of leukemia and all cancer risks. Al- (Andersson and others 1991). Andersson and colleagues though the estimates are lower than the linear estimates ob- (1991) studied the cancer risk among staff at two radio- tained from studies of atomic bomb survivors, they are com- therapy departments in Denmark. The average cumulative patible with a range of possibilities, from a reduction of risk radiation dose was 18.4 mSv, although 63% of the persons at low doses to risks twice those upon which current radia- had doses <5 mSv. The expected number of cancers was tion protection recommendations are based. Overall, there

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206 BEIR VII is no suggestion that the current radiation risk estimates for the projection of population-based risks. These studies, cancer at low levels of exposure are appreciably in error. however, provide a comparison to the risk estimates derived Uncertainty regarding the size of this risk remains as indi- from atomic bomb survivors. As with survivors of the cated by the width of the confidence intervals. atomic bomb explosions, persons exposed to radiation at Because of the absence of individual dose estimates in Mayak and at Chernobyl should continue to be followed for most of the cohorts, studies of occupational exposures in the indefinite future. medicine and aviation provide minimal information useful for the quantification of these risks. Summary Because of the uncertainty in occupational risk estimates and the fact that errors in doses have not formally been taken Studies of medical and dental occupational exposures do into account in these studies, the committee has concluded not currently provide quantitative estimates of radiation-re- that the occupational studies are currently not suitable for lated risks, due to the absence of radiation dose estimates.