9
Environmental Radiation Studies

INTRODUCTION

A considerable number of epidemiologic studies have been reported that have attempted to determine whether persons exposed, or potentially exposed, to ionizing radiation from environmental sources are at an increased risk of developing cancer. All epidemiologic studies are inherently uncertain, because they are observational in nature rather than experimental. Nevertheless, not all study designs are equally informative regarding the estimation of radiation risk to humans, and not all epidemiologic studies are of the same quality. Therefore, in evaluating the evidence regarding the risk of exposure to environmental sources of radiation, it is important to consider carefully the specific methodological features of the study designs employed.

Studies of environmental radiation exposure are of three basic designs: (1) descriptive studies, often referred to as ecologic; (2) case-control studies; and (3) cohort or followup studies. The existing published literature consists primarily of reports that are descriptive in nature and ecologic in design. The preponderance of this type of study is due to the fact that they are relatively easy to carry out and are usually based on existing data. Such investigations have utilized incidence, mortality, and prevalence data to estimate disease rates and, typically, to evaluate whether rates of disease vary in a manner that might be related to radiation exposure. If these analyses are based on large numbers of cases or large population groups, such studies may give the appearance of very precise results. Most often, geopolitical boundaries or distance from a source of radiation are used as surrogate means to define radiation exposure. For example, cancer incidence rates might be evaluated as a function of distance from a nuclear facility, or specialized statistical techniques might be employed to determine whether cases of cancer cluster or aggregate in a particular region or time period characterized by potential radiation exposure more than would be expected to occur by chance (i.e., in the absence of any exposure).

Weaknesses associated with studies of this type make them of limited value in assessing risk. The primary limitation is that the unit of analysis is not the individual; thus, generally little or no information is available that is specific to the individual circumstances of the people under study. Of most concern in this regard is the definition of radiation exposure. Ecologic studies generally do not include estimates of individual exposure or radiation dose. Either aggregate population estimates are used to define population dose for groups of people, or surrogate indicators such as distance or geographic location are used to define the likelihood or potential for exposure or, in some cases, an approximate magnitude or level of exposure. This approach has serious limitations. It implies, for example, that residents who live within a fixed distance from a facility are assumed to have received higher radiation doses than those who live at greater distances or than individuals in the larger population as a whole who do not live in the vicinity of the facility. Further, it assumes that everyone within the boundary that defines exposure (or a given level of exposure) is equally exposed or has the same opportunity for exposure. In most situations, such assumptions are unlikely to be accurate, and variability in exposure of individuals within the population may be substantially greater than the exposure attributed on a population basis. The resulting almost certain misclassification of exposure can lead to a substantial overestimation or underestimation of the association of the exposure with the disease under study.

Similarly, there is usually no information available in ecologic studies regarding other factors that might influence the risk of developing the disease(s) under study (i.e., other risk factors). Thus, there is no way to evaluate the impact of such factors in relation to the potential effect of radiation exposure. This inability to evaluate or account for the potential confounding effect of other important factors, or the modifying effect of such factors on risk, makes the ecologic approach of limited use in deriving quantitative estimates of radiation risk.



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9 Environmental Radiation Studies INTRODUCTION Weaknesses associated with studies of this type make them of limited value in assessing risk. The primary limita- A considerable number of epidemiologic studies have tion is that the unit of analysis is not the individual; thus, been reported that have attempted to determine whether per- generally little or no information is available that is specific sons exposed, or potentially exposed, to ionizing radiation to the individual circumstances of the people under study. from environmental sources are at an increased risk of de- Of most concern in this regard is the definition of radiation veloping cancer. All epidemiologic studies are inherently exposure. Ecologic studies generally do not include esti- uncertain, because they are observational in nature rather mates of individual exposure or radiation dose. Either aggre- than experimental. Nevertheless, not all study designs are gate population estimates are used to define population dose equally informative regarding the estimation of radiation risk for groups of people, or surrogate indicators such as distance to humans, and not all epidemiologic studies are of the same or geographic location are used to define the likelihood or quality. Therefore, in evaluating the evidence regarding the potential for exposure or, in some cases, an approximate risk of exposure to environmental sources of radiation, it is magnitude or level of exposure. This approach has serious important to consider carefully the specific methodological limitations. It implies, for example, that residents who live features of the study designs employed. within a fixed distance from a facility are assumed to have Studies of environmental radiation exposure are of three received higher radiation doses than those who live at greater basic designs: (1) descriptive studies, often referred to as distances or than individuals in the larger population as a ecologic; (2) case-control studies; and (3) cohort or follow- whole who do not live in the vicinity of the facility. Further, up studies. The existing published literature consists prima- it assumes that everyone within the boundary that defines rily of reports that are descriptive in nature and ecologic in exposure (or a given level of exposure) is equally exposed or design. The preponderance of this type of study is due to the has the same opportunity for exposure. In most situations, fact that they are relatively easy to carry out and are usually such assumptions are unlikely to be accurate, and variability based on existing data. Such investigations have utilized in- in exposure of individuals within the population may be sub- cidence, mortality, and prevalence data to estimate disease stantially greater than the exposure attributed on a popula- rates and, typically, to evaluate whether rates of disease vary tion basis. The resulting almost certain misclassification of in a manner that might be related to radiation exposure. If exposure can lead to a substantial overestimation or under- these analyses are based on large numbers of cases or large estimation of the association of the exposure with the dis- population groups, such studies may give the appearance of ease under study. very precise results. Most often, geopolitical boundaries or Similarly, there is usually no information available in eco- distance from a source of radiation are used as surrogate logic studies regarding other factors that might influence the means to define radiation exposure. For example, cancer in- risk of developing the disease(s) under study (i.e., other risk cidence rates might be evaluated as a function of distance factors). Thus, there is no way to evaluate the impact of such from a nuclear facility, or specialized statistical techniques factors in relation to the potential effect of radiation expo- might be employed to determine whether cases of cancer sure. This inability to evaluate or account for the potential cluster or aggregate in a particular region or time period char- confounding effect of other important factors, or the modify- acterized by potential radiation exposure more than would ing effect of such factors on risk, makes the ecologic ap- be expected to occur by chance (i.e., in the absence of any proach of limited use in deriving quantitative estimates of exposure). radiation risk. 207

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208 BEIR VII A third limitation of the ecologic design is that disease value in testing specific hypotheses or providing quantita- outcome usually is not confirmed at the individual level. tive estimates of risk in relation to specific sources of envi- Most studies rely on routine reporting, either of mortality ronmental radiation. Epidemiologic studies, in general, have through death certificates or of cancer incidence through limited ability to define the shape of the radiation dose-re- cancer registration and surveillance systems. Such sources sponse curve and to provide quantitative estimates of risk in of information vary in their degree of accuracy and com- relation to radiation dose, especially for relatively low doses. pleteness, and they can sometimes vary in relation to the To even attempt to do so, a study should (1) be based on surrogate measures being used to define exposure (e.g., geo- accurate, individual dose estimates, preferably to the organ graphic area). This can lead to the identification of spurious of interest; (2) contain substantial numbers of people in the associations. dose range of interest; (3) have long enough follow-up to Fourth, ecologic studies seldom estimate or account for include adequate numbers of cases of the disease under population migration or movement. This, too, can result in study; and (4) have complete and unbiased follow-up. Un- the appearance of spurious associations if aggregate or popu- fortunately, the published literature on environmental radia- lation measures of radiation exposure actually reflect under- tion exposures is not characterized by studies with such fea- lying changes in population mobility with factors such as tures. time, age, or geographic area. The accompanying tables provide a summary of the prin- Finally, descriptive studies are often based on a small cipal studies of environmental radiation exposure published number of cases of disease. Such studies have low statistical since the BEIR V report (NRC 1990). Articles included in power to detect an association if it truly exists, and they are this summary were identified principally from searching the very sensitive to random fluctuations in the spatial and/or PubMed database of published articles from 1990 through temporal distribution(s) of the disease(s) under study. This July 2004. Searches were restricted to human studies and is especially true for diseases such as cancer, particularly were broadly defined: key words included radiation; neo- childhood cancer, which are relatively uncommon on a popu- plasms; radiation-induced; radioactive fallout; and environ- lation basis. mental radiation. Searches specific to the Chernobyl acci- There have also been attempts to evaluate the effect of dent included Chernobyl, Russia, Ukraine, and Belarus as environmental radiation exposures using the two most com- key words. Articles were also identified from UNSCEAR mon analytical study designs employed in epidemiology: the (2000b) and from the usual scientific interactions with other case-control and the cohort study. Such studies are almost investigators. The tables are organized according to the type always based on individual-level data and thus are not sub- of exposure situation under study as follows: (1) populations ject to many of the limitations summarized above for eco- living around nuclear facilities; (2) populations exposed logic studies. Nevertheless, each of these study designs is from atmospheric testing, fallout, or other environmental subject to specific weaknesses and limitations. Of most con- releases of radiation; (3) populations exposed from the cern in case-control studies is the potential bias that can re- Chernobyl accident; (4) populations exposed from natural sult in relation to the selection of cases and controls, such background; and (5) children of adults exposed to radiation. that the two groups are differentially representative of the Within each type of exposure situation, the tables are further same underlying population. A second important source of grouped according to study design: ecologic studies, case- bias can be differential recall of information about exposure control studies, and cohort studies. Each table contains a for cases relative to controls. In cohort studies, a common brief description of the principal design features and results limitation is the relatively small number of cases for uncom- of each study. The principal criteria used to assess the utility mon disease outcomes and the resultant low statistical power. of each study in evaluating the risk of disease in relation to A second concern is the completeness of follow-up of the radiation exposure were the following: (1) Was there a quan- cohort under study, and equal follow-up and determination titative estimate of radiation dose; (2) if so, was the estimate of disease status according to exposure. Such limitations of for individuals in the study (i.e., individual-level estimates both types of analytic epidemiologic studies may be particu- of radiation dose received); and (3) was there a quantitative larly problematic in investigations of low doses and rela- estimate of disease risk in relation to radiation dose? tively small increases in disease risk. Under such circum- stances, the magnitude of the impact on risk estimates of POPULATIONS LIVING AROUND NUCLEAR small or modest biases may be as great or greater than the FACILITIES magnitude of the true disease risk. In summary, most existing published studies of environ- Table 9-1A lists 16 ecologic studies of populations living mental radiation exposure are ecologic in design. Such stud- around nuclear facilities, 13 of the locations being outside ies are limited in their usefulness in defining the risk of dis- the United States. Most define exposure, or potential for ex- ease in relation to radiation exposure or dose. They can posure, based on a measure of distance from the facility, sometimes be informative in generating new hypotheses or although the two studies of exposures at Three Mile Island suggesting directions of study but seldom, if ever, are of by Hatch (1992) utilized some information on measurements

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TABLE 9-1A Populations Living Around Nuclear Facilities—Ecologic Studies Incidence/ Type of Dates of Number Reference Mortality Population Studied Exposure Accrual Type of Dosimetry Outcomes Studied of Cases Summary of Results Hatch and Incidence Residents (ages 0–24) Background 1975–1985 Outdoor measurements All cancer; leukemia 49 (0–14) Increased risk for highest vs. Susser (1990) and mortality within 10 miles of gamma taken in 1976 104 (0–24) lowest quartile; childhood Three Mile Island cancer and leukemia Hatch and Incidence Residents within Xenon and 1975–1985 Dispersion modeling, All cancer; childhood 5493 total No evidence of an effect on others (1990) 10 miles of Three Mile iodine based on monitoring cancer (ages 0–14, cancer incidence Island data 0–24); leukemia (ages 0–14, 0–24, 25); and all lymphoma Jablon and Mortality Residents of 107 Unspecified 1950–1984 County with a nuclear 15 cancer sites; benign 900,000 No evidence of excess mortality others (1991) counties in U.S. with facility that began and unspecified deaths in in study counties or near nuclear operation before 1982, neoplasms 107 counties installations or an adjacent county if at least 20% of the county was within a 16 km radius Sofer and Incidence Children and young Unspecified 1960–1985 Distance from Negev Leukemia 192 No overall increase; some others (1991) adults living near nuclear plant increase with time among 0–9 in nuclear plant in Israel Western Negev; increase in girls 0–4 from 1970 to 1979 Michaelis and Incidence Children living near Unspecified 1980–1990 Distance from nuclear Childhood cancer; 81 within No increase for all cancer, acute others (1992) nuclear installations facility acute leukemia 5 km leukemia; suggested increases in in Germany subgroups of early ages or close proximity McLaughlin Incidence Children born to Unspecified 1950–1987 Distance from nuclear Leukemia in children Range by Suggestion of some excess over and others and mortality mothers residing near facility facility: 2–72 expected for some analyses; (1993b) nuclear installations none significant in Ontario, Canada Bithell and Incidence Children in England Unspecified 1966–1987 Distance from nuclear Leukemia and non- Range for Linear risk score significantly others (1994) and Wales facilities based on ward Hodgkin’s lymphoma 25 km zones: elevated in Sellafield and (NHL) 7–570 Burghfield Black and Incidence Residents of Dalgety Particles of 1975–1990 Routine monitoring All cancer; 211 (total) No evidence of increase over others (1994a) Bay, Scotland radium-226 measurements 18 specific sites expected Black and Incidence Children and young Contamination 1968–1991 Distance from Dounreay Leukemia and NHL 12 in nearest Evidence of increase over others (1994a) adults in Dounreay, from nuclear zone expected in nearest zone Scotland reprocessing plant continues 209

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TABLE 9-1A Continued 210 Incidence/ Type of Dates of Number Reference Mortality Population Studied Exposure Accrual Type of Dosimetry Outcomes Studied of Cases Summary of Results Zaridze and Incidence Children in Kazakhstan Unspecified 1981–1990 Distance from nuclear All cancer; six Total: 1408; Increase in leukemia in areas others (1994) testing sites specific sites leukemia: 512 closest to testing sites; some evidence of increase in brain tumors Viel and Incidence People under age 25 Unspecified 1978–1992 Distance from the Leukemia 25 Cluster of cases located close to others (1995) living around La Hague La Hague plant La Hague plant reprocessing plant in France Waller and Incidence Children in 2594 Unspecified 1980–1990 Distance from nuclear Acute lymphocytic 656 No significant clustering of others (1995) parishes of Sweden facility leukemia (ALL) cases found Gulis and Incidence Residents of Trnava, Unspecified 1986–1995 Distance from nuclear 13 cancer sites Range for Suggestion of increasing Fitz (1998) Slovakia power plant zones: 0–323 incidence closer to the site; nonsignificant Kaatsch and Incidence Children living near Unspecified 1991–1995 Distance from a nuclear All cancer; leukemia; Total 550; No evidence of an increase others (1998) nuclear facilities in facility lymphoma; selected leukemia 182 in incidence Germany sites Guizard and Incidence Residents under age 25 Unspecified 1978–1998 Distance from the Leukemia 38 Increase over expected in area others (2001) in areas around the La Hague plant less than 10 km from site La Hague plant in France Boutou and Incidence Nord Cotentin, France Population 1979–1998 Population mixing index Childhood leukemia Incidence rate ratio 2.7 in rural others (2002) mixing—near per geographic unit in persons under communes in highest tertile of nuclear power (commune), based on age 25 mixing, relative to urban plant and number of workers born communes. Positive trend in reprocessing outside department of leukemia with increasing mixing unit La Manche index. Risk stronger for ALL in children 1–6

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ENVIRONMENTAL RADIATION STUDIES 211 taken around the site after the accident. All but one (Jablon kemia, one in children under age 15 (Urquhart and others and others 1991) are based on incidence data, and one study 1991) and the other in people under age 25 (Pobel and Viel in Canada (McLaughlin and others 1993a) uses mortality 1997). Both studies are based on a small number of cases data as well as incidence data. The focus of most of these and focus primarily on parental radiation exposure and X- investigations is leukemia and/or childhood cancer, although ray exposure of the child. Neither study found an increased a few include all cancers as an outcome. The size of the risk associated with these types of radiation exposure. Both, studies, in terms of numbers of cases, ranges from very small however, did find an increased risk associated with playing (Black and others, 1994a; 12 cases in the most highly on beaches near the nuclear facility. The third study (Shields exposed zone) to extremely large (Jablon and others 1991). and others 1992) focuses on congenital and perinatal condi- Notably, most of the studies do not specify the nature of the tions, stillbirths, and infant deaths in relation to exposures radiation exposure, and none of the 16 contains individual from uranium mines. Exposures include environmental ex- estimates of radiation dose. Although some of these studies posures from living near a mine or mine dumps or tailings, report an increased occurrence of cancer that could poten- or living in a home made from mine rock, as well as from tially be related to environmental radiation exposures, none working in a uranium mine. This study does not provide an provides a direct quantitative estimate of risk in relation to estimate of radiation risk associated with any of the indica- radiation dose. tors of exposure. Table 9-1B summarizes three case-control studies of per- In summary, most of the studies of populations living sons living around a nuclear facility. Two studies are of leu- around nuclear facilities have not included individual esti- TABLE 9-1B Populations Living Around Nuclear Facilities—Case-Control Studies Number of Population Studied Subjects Dates of Type of Type of Reference Cases Controls Cases Controls Accrual Exposure Dosimetry Summary of Results Urquhart Leukemia Selected from 14 55 Diagnosis Paternal Employment at No increased risk with (1991) and NHL birth register; 1970–1986 preconception Dounreay; recorded employment at Dounreay, in children matched by zone whole-body dose from employment recorded radiation dose, under age 15 of residence at dose; antenatal records; questionnaire antenatal X-ray; evidence resident in birth, date of X-ray for X-ray of increased risk from Caithness birth, sex playing on beaches within 50 km of Dounreay Shields Congenital Chronologically 266 266 1964–1981 Environmental Environment: time Only significant and others and perinatal nearest normal exposure from prior to child’s birth association with mother (1992) conditions, single birth; working or worked in uranium living near tailings or stillbirths, matched by sex, living near, or mine; residence within mine dumps. Overall, infant deaths mother’s age working in 0.5 mile of mine, associations with within 5 years, uranium mines dumps, or tailings; measures of radiation gravidity living in home made exposure were weak with mine rock. Workers: recorded WLM, estimated gonadal dose Pobel and Leukemia Sample of 27 192 1978–1993 Antenatal and For parents employed No association with Viel (1997) diagnosed children cared postnatal in nuclear facility, occupational radiation in people for by general X-ray exposure; whole-body external exposure of parents; <25 years of practitioners of parental dose (mSv) was increased risk for use of age living the cases; occupational obtained from company local beaches, within 35 km matched to cases exposures records. Other consumption of local fish, of La Hague on sex, age, (including information obtained length of residence in nuclear plant place of birth; radiation); viral by questionnaire granitic area or house and residence at infections, diagnosis of case life-style

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212 BEIR VII TABLE 9-2A Populations Exposed from Atmospheric Testing, Fallout, or Other Environmental Release of Radiation— Ecologic Studies Incidence/ Population Type of Outcomes Number Reference Mortality Studied Exposure Dates of Accrual Type of Dosimetry Studied of Cases Summary of Results Darby Incidence Children Fallout Denmark (1948), Estimates of bone Leukemia Not Little increase in high-fallout years; and others under from Finland, Norway, marrow dose to given slightly elevated in high vs. (1992) age 15 in nuclear Iceland (1958), fetus, 1-year-old, medium group Nordic weapons Sweden (1961– testes, received countries tests 1987) during fallout period: low, medium, high Gilbert Incidence United Fallout Deaths: 1957– Mean thyroid dose Thyroid 4602 No increased risk with cumulative (1998) and States from 1994; incident by county, derived cancer deaths; dose or dose received at ages 1–15; mortality nuclear cases: 1973– from measurements 12,657 suggested increase for those weapons 1994 and environmental incident exposed under age 1 and those in tests in modeling cases 1950–1959 birth cohort Nevada mates of radiation dose and have therefore not provided an In contrast, a recent study of U.S. veterans (Dalager and estimate of disease risk. The three case-control studies de- others 2000) who participated in atmospheric nuclear weap- scribed above found no increased risk of disease associated ons tests reported a significant increase in death from all with radiation exposure. causes, and for all lymphopoietic cancers combined, al- though the number of cases in the latter group was very small. This study focused on veterans whose external POPULATIONS EXPOSED FROM ATMOSPHERIC γ-radiation dose, as recorded on film badges, was 5 rem, TESTING, FALLOUT, OR OTHER ENVIRONMENTAL and compared mortality in this group to veterans who par- RELEASE OF RADIATION ticipated in one nuclear test and whose dose was 0.25 rem. Table 9-2A describes two ecologic studies of populations The mean dose among the 5 rem group was 7.8 rem and exposed to fallout from atmospheric nuclear testing, fallout, among the controls was 0.08. or other sources of environmental release of radiation. The Also included in Table 9-2B are several studies of the nature of the exposure is not specified beyond “fallout.” population of residents living near the Techa River in the These studies utilize population-based measures of exposure southern Urals of the Russian Federation. More than 25,000 rather than individual estimates of radiation dose. They ad- residents were exposed to external γ-radiation as well as in- dress two separate outcomes (leukemia and thyroid cancer), ternally from fission products (primarily cesium-137, stron- but provide no quantitative estimates of risk associated with tium-90, ruthenium-106, and zirconium-95) released into the the exposure. Techa River from the nearby Mayak plutonium production Table 9-2B summarizes two cohort studies of persons facility, predominately in the early 1950s. Studies have been who participated in U.K. atmospheric nuclear weapons tests. conducted of cancer mortality in residents and their off- The study by Darby and colleagues (1993) is an extension of spring, as well as pregnancy outcomes. Initial dose estimates an earlier analysis from this cohort and uses doses from film were based on average doses reconstructed for settlements. badges to characterize individual external whole-body ra- Efforts to estimate individual doses for members of this diation dose. It investigates all causes of mortality as well as resident cohort continue. To date, there is no evidence of a all major forms of cancer. Overall, the study found no in- decrease in birth rate or fertility in the exposed population, creased risk of developing cancer or other fatal diseases as a and there is no increased incidence of spontaneous abortions function of estimated dose received, based on follow-up or stillbirths (Kossenko and others 1994). There is some evi- through 1991 and relatively large numbers of cases. There dence of a statistically significant increase in total cancer was some evidence of an increase in leukemia, based on only mortality (Kossenko 1996). Current estimates of the excess 29 cases. The most recent update of this cohort (Muirhead absolute risk (EAR)1 of leukemia in this cohort is 0.85 per and others 2003) found little increase in overall mortality or 10,000 person-years (PY) per gray (95% CI 0.2, 1.5), and for cancer incidence and no increase in other types of cancer, but continuing evidence of a small increased risk of non- chronic lymphocytic leukemia (CLL). 1EAR is the rate of disease in an exposed population minus the rate of disease in an unexposed population.

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TABLE 9-2B Populations Exposed from Atmospheric Testing, Fallout, or Other Environmental Release of Radiation—Cohort Studies Incidence/ Cohort Comparison Dates of Type of Type of Outcomes Number Reference Mortality Definition Group Accrual Exposure Dosimetry Studied of Cases Summary of Results Darby and Incidence Persons who Men identified 1950s– External Recorded on Broad causes All causes: No effect on risk of developing others (1993) and mortality participated in from Ministry of 1991 whole-body film badges of death; 27 2753 (control cancer or other fatal diseases; some U.K. atmospheric Defense archives dose obtained from specific cancer group—2939) evidence of an increase over nuclear weapons who did not Ministry of sites expected for leukemia, based on tests participate Defense 29 cases Kossenko and Pregnancy Children born to Unexposed 1953– External Gonadal doses Birth rate, 56 cancer No decrease in birth rate or fertility others (1994) outcome and 28,100 residents populations living 1974 and internal estimated as fertility, fetal deaths in exposed population; no mortality exposed to discharges in the same area dose: average for loss, infant increased incidence of spontaneous of radioactive waste primarily each settlement mortality abortions or stillbirths; no change into Techa River from 137Cs, in cancer mortality 90Sr, 106Ru, 95Zr Kossenko and Mortality 28,000 residents Unexposed 1950– External Average All cancer and 163 cancers Increase in total cancer mortality. others (1994) exposed to discharges populations living 1982 and internal absorbed dose 13 major site in exposed Leukemia: absolute risk 0.85 per of radioactive waste in the same area dose: to bone marrow categories population 10,000 PY per gray; relative risk into Techa River, primarily estimated for for esophagus, stomach, and lung 1950–1953 from 137Cs, each settlement similar to atomic bomb survivors 90Sr, 106Ru, 95Zr Kossenko Mortality 28,000 residents Matched control 33-year External Average Leukemia and Leukemia: absolute risk 0.85 per (1996) exposed to discharges group from period and internal absorbed dose solid cancer in 10,000 PY per gray; solid cancer: of radioactive waste unexposed area from dose: to bone marrow residents; relative risk 0.65 Gy–1. No increase into Techa River 1949 primarily estimated for cancer in in offspring of exposed residents through from 137Cs, each settlement offspring 1982 90Sr, 106Ru, 95Zr Davis and Cumulative Persons born to Internal control Birth Primarily Estimated Thyroid cancer 19 thyroid No increase in thyroid cancer or others (2001) incidence mothers resident according to through 131I individual and 12 cancer cases any noncancer thyroid disease in one of 7 counties estimated date of absorbed dose categories of outcome associated with increasing surrounding Hanford individual thyroid exam in to thyroid noncancer radiation dose to the thyroid Site from 1940 to radiation dose 1992– thyroid 1946 1997 diseases Dalager and Mortality Persons who Navy veterans Date of External Film badges All deaths; 300 deaths in All-cause mortality: relative risk others (2000) participated in who participated first gamma lymphopoietic, veterans with (RR) 1.22 (95% CI 1.04–1.44); U.S. atmospheric in HARDTACK exposure dose leukemia, 5 rem; lymphopoietic cancer 3.72 (95% nuclear weapons and received through digestive, 11 cases of CI 1.28–10.83) tests and received minimal 1996 respiratory, lymphopoietic highest doses radiation dose other cancer cancer continues 213

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TABLE 9-2B Continued 214 Incidence/ Cohort Comparison Dates of Type of Type of Outcomes Number Reference Mortality Definition Group Accrual Exposure Dosimetry Studied of Cases Summary of Results Kossenko and Mortality 10,459 offspring of None 1950– External None Cancer 25 cancer Descriptive analyses only—no others (2000) parents exposed to 1992 and internal deaths estimates of risk discharges of dose: radioactive waste primarily into Techa River from 137Cs, 90Sr, 106Ru, 95Zr Koshurnikova Mortality Ozyorsk 72,185 persons 1948– Fallout None Deaths, 4636 deaths; Thyroid cancer 3–4 times expected and others and incidence Population living in Ozyorsk 1988 from cancer deaths, 371 cancer relative to Russia; 1.5–2-fold (2002) for at least 1 year Mayak leukemia, deaths; higher based on Chelyabinsk under age 15 and facility thyroid cancer 53 leukemia Oblast rates born 1948–1988; deaths; or born elsewhere 31 thyroid 1934–1988 but cancer cases moved to Ozyorsk before age 15 Muirhead and Mortality 21,357 persons 22,333 men who 1952– External Film badge All deaths, 2089 deaths; Little difference in overall others (2003) and incidence who participated did not participate 1998 gamma readings and 27 types of 785 cancer mortality or cancer incidence in the U.K. in tests identified potential for cancer deaths; between exposed and controls; no atmospheric nuclear from Ministry of exposure based 16 leukemia increase in multiple myeloma; weapons tests Defense records, on duties deaths; evidence of a small risk of non- matched on a 2641 cases of CLL leukemia number of cancer; characteristics 67 cases of leukemia Takahashi Prevalence 3709 Marshall Island Internal control 1993– Fallout Surrogate Thyroid cancer 57 cases Prevalence increased with quartile and others Residents born before according to 1997 from Castle estimates of of estimated dose, but was not (2003) the Castle BRAVO estimated dose BRAVO dose based on significant atmospheric nuclear level test 137Cs soil weapons tests on deposition March 1, 1954 levels

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ENVIRONMENTAL RADIATION STUDIES 215 solid tumors the relative risk estimate is 0.65 Gy–1 (95% CI miologic studies have been carried out since the Chernobyl –0.3, 1.0). Median dose estimates for soft tissue in this co- accident to investigate the potential late health consequences hort are 7 mSv (maximum 456 mSv) and for bone marrow of exposure to ionizing radiation from the accident. These 253 mSv (maximum 2021 mSv). Estimates of the relative studies have focused largely on thyroid cancer in children, risk for cancer of the esophagus, stomach, and lung are simi- but have also included investigations of recovery operation lar to those reported for atomic bomb survivors. There is no workers and residents of contaminated areas, and have in- evidence of an increase in cancer mortality in the offspring vestigated the occurrence of leukemia and solid tumors other of exposed residents (Kossenko 1996). There has also been than thyroid cancer among exposed individuals. one study (Koshurnikova and others 2002) of persons living Overwhelmingly, the published findings are from studies in the town of Ozyorsk exposed to fallout from the nearby that are ecologic in design and therefore do not provide quan- Mayak nuclear facility. This study reported an excess of thy- titative estimates of disease risk based on individual expo- roid cancer three to four times that expected relative to rates sure circumstances or individual estimates of radiation dose. for all of Russia and a somewhat lower excess (1.5 to two- Most reports are descriptive incidence and prevalence stud- fold higher) based on a comparison with Chelyabinsk Oblast ies that utilize population or aggregate estimates of radiation rates. No estimates of radiation dose were included in this dose. The principal studies are summarized in Table 9-3A. study. Only four analytical studies are published that report dose- Two other cohort studies of persons exposed to atmo- response results based on individual dose estimates (Table 9- spheric releases of radioactive materials are also summarized 3B). In the sections that follow, current evidence is summa- in Table 9-2B. One is a follow-up study of 3440 persons rized separately regarding the risk of thyroid cancer, exposed as young children to atmospheric releases of prima- leukemia, and other solid tumors associated with radiation rily 131I from the Hanford nuclear facility in eastern Wash- exposure from the Chernobyl accident. Studies of recovery ington State (Davis and others 2001, 2004a). No increased operations workers are considered in Chapter 8 on occupa- risk of thyroid cancer was found associated with individual tional exposures. radiation dose to the thyroid. The other (Takahashi and others 2003) is a prevalence study of thyroid cancer conducted Thyroid Cancer through screening of 3,709 Marshall Island residents born before the Castle BRAVO atmospheric nuclear weapons test An increase in the incidence of thyroid cancer first began on March 1, 1954. Radiation dose was based on a surrogate to appear in Belarus and Ukraine in 1990. After the initial constructed from age-specific doses estimated for the Utirik few reports, there was immediate skepticism that such in- atoll and 137Cs deposition levels on atolls where the partici- creases were related directly to radiation exposure from pants resided. There was some indication that the prevalence Chernobyl. The very early onset of disease after exposure of thyroid cancer increased with quartile of estimated dose, (only 4 years) was unexpected based on existing knowledge but the increase was not statistically significant. of the latent period for radiation-related thyroid cancer; there In summary, some but not all studies of persons exposed was doubt about the certainty of the pathologic diagnoses; to fallout or other environmental releases of radiation have and there was speculation that the apparent increases were found increased risks of specific disease outcomes. Most largely the result of widespread population screening. notable are findings of a significant increase in death from Numerous reports have continued to describe an increas- all causes and for all lymphopoietic cancers combined in a ing number of cases of thyroid cancer, particularly in the recent study of U.S. veterans who participated in atmospheric most heavily contaminated regions of Ukraine and Belarus, nuclear weapons tests, and evidence of an increase in total and also in Russia. Collectively, findings reported to date cancer mortality and thyroid cancer incidence among resi- have demonstrated an association between radiation expo- dents living near the Techa River in the southern Urals of the sure from the Chernobyl accident and an increase in thyroid Russian Federation. cancer incidence. Among those under age 18 at the time of the accident, it has been estimated that approximately 2000 thyroid cancers were diagnosed from 1990 to 1998 in POPULATIONS EXPOSED FROM THE CHERNOBYL Ukraine, Belarus, and Russia. The increase in all three coun- ACCIDENT tries for this period was approximately fourfold, with the The explosion at the Chernobyl Power Station Unit 4 in highest increase observed in the Gomel region in Belarus. Ukraine on April 26, 1986, released large quantities of ra- More recent data indicate that excess thyroid cancer contin- dionuclides into the atmosphere, resulting in the contamina- ues to occur among people in Belarus, Ukraine, and the con- tion of a large geographic area. Initially exposures were due taminated regions of Russia. This increase cannot be ex- principally to radioisotopes of iodine, primarily iodine-131 plained only by the aging of the cohort and the improvement (131I), and subsequently to radiocesium, primarily cesium- in case detection and reporting. Although there is now little 137 (137Cs), from both external exposure and the consump- doubt that an excess of thyroid cancer has occurred in highly tion of contaminated milk and other foods. Numerous epide- contaminated areas, there is still very little information re-

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TABLE 9-3A Populations Exposed from the Chernobyl Accident—Ecologic Studies 216 Incidence/ Type of Dates of Number Reference Mortality Population Studied Exposure Accrual Type of Dosimetry Outcomes Studied of Cases Summary of Results Prisyazhiuk Incidence Three contaminated Fallout from 1981–1990 Calendar year (before and Leukemia, thyroid Leukemia: 105; Overall, incidence rates were not and others districts in Ukraine: Chernobyl after accident) and district cancer, all other thyroid: 25; different before and after the (1991) Polesskoye, Naroditchy, (contaminated areas) cancer all other: 3804 accident. Leukemia in age 65+ Ovrutch group increased in 1987 and remained 2–3 times higher; three cases of thyroid cancer diagnosed in 1990 in <14 age group (none 1981–1989); all others increased in 1987 by a third Ramsay and Incidence Population of Lothian, Fallout from 1978–1989 Calendar year (i.e., from Down’s syndrome Ave.: 12.4 Significant increase in 1986– others (1991) Scotland Chernobyl Chernobyl, before and cases per year; 1987 after accident) range 7 (1989)– 26 (1987) Baverstock Incidence Belarus Fallout from 1986–1992 Calendar year and region Thyroid cancer 104 Marked increase beginning in and others Chernobyl 1990; highest rates in Gomel (1992) Kazakov and Incidence Six regions of Belarus Fallout from 1986–1992 Calendar year and region Thyroid cancer 131 Average of 4 cases per year others (1992) and Minsk city Chernobyl 1986–1989; 55 in 1991; projected 60 in 1992. Most increase in Gomel Ivanov and Incidence Belarus: children ages Fallout from 1979–1991 Two time periods: 1979– Childhood leukemia Not given No change in incidence after others (1993) 0–14 Chernobyl 1985; 1986–1991. Three Chernobyl accident, and no levels of contamination increase after accident in areas by region or city with higher contamination levels Parkin and Incidence 20 European countries: Fallout from 1980–1988 Estimated dose (effective Childhood leukemia 3679 Risk of leukemia 1987–1988 others (1993) children ages 0–14 Chernobyl equivalent dose) in 30 relative to before 1986 was not countries or regions, related to radiation exposure obtained from UNSCEAR Auvinen and Incidence Finland: children 0–14 Fallout from 1976–1992 Estimated cumulative Childhood leukemia Not given Incidence did not increase in others (1994) in 1976–1992 Chernobyl dose in 2 years after the 1976–1992. Relative excess in accident. Based on 1989–1992 was not significantly measurements of dose different from zero rate in 455 municipalities. Internal dose estimated from whole-body measurements on sample of 81 children. Municipalities divided into fifths of exposure

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Hjalmars and Incidence Sweden: children 0–15 Fallout from 1980–1992 137Cs contamination by Childhood acute 888 No significant increase in others (1994) Chernobyl geographic area leukemia childhood acute leukemia in contaminated areas Petridou and Incidence Greece: children 0–14 Fallout from 1980–1991 Three time periods: Childhood leukemia 968 No evidence of an increased others (1994) Chernobyl 1980–June 1986; incidence of childhood leukemia July 1986–June 1988; in periods after Chernobyl July 1988–June 1991. accident. No association Mean fallout levels between childhood leukemia and (based on 137Cs region by radiation fallout level measurements) grouped into 17 geographic regions Likhtarev Incidence Ukraine: children ages Fallout from 1986–1993 Calendar year; Thyroid cancer 418 cases in Increase beginning in 1989; rate and others 0–14 Chernobyl 7 geographic zones 0–14 year olds; in 1993 was 5 times higher than (1995) defined by estimated 248 cases in 1986; higher incidence in zones average thyroid dose those 15 and with higher contamination levels to children older Prisyazhiuk Incidence Four districts in Fallout from 1980–1993 Three time periods: 1980– All cancer; leukemia Not given Statistically significant increase and others Ukraine: Naroditchy, Chernobyl 1985 (before accident); and lymphoma; in thyroid cancer after the (1995) Ovrutch, Ivankov, 1986–1993 (after thyroid cancer accident; no significant increase Polesskoye accident); 1980–1993 in all cancer, or leukemia and lymphoma Stsjazhko Incidence Belarus, Russia, Fallout from 1981–1994 Three time periods: 1981– Thyroid cancer Since the Increase in thyroid cancer and others Ukraine Chernobyl 1985 (before accident); accident: incidence after the accident; (1995) 1986–1990; 1991–1994; Belarus, 333; most pronounced in most 6 geographic regions Russia, 23; heavily contaminated areas Ukraine, 209 Sugenoya Prevalence Two cities in Belarus Fallout from October Contamination levels Thyroid abnormalities 888 screened in Significantly higher prevalence and others (Chechelsk and Chernobyl 1991– (137Cs): Chechelsk Chechelsk; of multiple micronodular lesions (1995) Bobruisk): children August 5–>40 Ci/km2; Bobruisk, 521 screened in in diffuse goiter in contaminated ages 10–15 1992 control area Bobruisk city Gunay and Incidence Bursa, Turkey: Fallout from 1986–1995 Calendar year, 1986–1995 Acute leukemia, Acute leukemia: Significant increase in acute others (1996) pediatric cases of Chernobyl lymphoma, solid 101; lymphoma: leukemia after 1986; no malignancy tumors 44; solid tumor: significant increase in 31 lymphoma or solid tumor Ivanov and Incidence Seven regions of Fallout from 1982–1994 Calendar year; Childhood leukemia Not given No increase associated with others Belarus: children 0–15 Chernobyl 7 geographic regions calendar; no difference in rates (1996) by geographic region Kumpusalo Prevalence Two villages in Fallout from 1993 Contaminated area Thyroid ultrasound 302 screened No pathological U.S. findings in and others Bryansk region of Chernobyl (Mirnyi) and control area findings in Mirnyi; 200 either city. Prevalence of thyroid (1996) Russia (Mirnyi and (Krasnyi) screened in abnormalities higher in Krasnyi): residents Krasnyi contaminated area: ages 0–9, ages 3–34 8.1% in Mirnyi; 1.6% in Krasnyi continues 217

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228 BEIR VII urothelial biopsies of Ukrainian patients, they concluded that few studies of the incidence of or mortality from solid can- activation of DNA damage repair was detected more fre- cers other than thyroid cancer in populations exposed to ra- quently among residents of contaminated areas, compared to diation from the Chernobyl accident, and there is no evi- those of putatively uncontaminated areas (Romanenko and dence of an increase in any solid cancer type to date. others 2002). Morimura and colleagues (2004) observing p53 gene mutations in 54.5% of 11 and 16.7% of 18 Ukrai- POPULATIONS EXPOSED FROM NATURAL nian bladder cancers collected before and after the Chernobyl BACKGROUND accident, respectively, suggesting the possibility of distinct molecular genetic pathways of bladder cancer induction be- Table 9-4 summarizes four studies of populations ex- fore and after the accident. Romanenko and colleagues posed from natural background radiation. Two were con- (2000) have also reported that renal carcinoma incidence has ducted in China, one in Great Britain, and one in India. A increased from 4.7 to 7.5 per 100,000 PY. number of different cancer outcomes were studied, based on In summary, there is now little doubt that an excess of incidence, mortality, and prevalence data. These studies did thyroid cancer has occurred in areas highly contaminated by not find higher disease rates in geographic areas with high radiation from the Chernobyl accident. Analytical studies background levels of radiation exposure compared to areas further indicate that exposure to radiation from Chernobyl is with lower background levels. However, these studies were associated with an increased risk of thyroid cancer and that ecologic in design and utilized population-based measures the relationship is dose dependent. Quantitative estimates of of exposure rather than individual estimates of radiation risk from these studies are consistent with estimates from dose. Thus, they cannot provide any quantitative estimates other radiation-exposed populations. There is evidence that of disease risk associated with the exposure levels found in young age at exposure and iodine deficiency may be impor- the areas studied. tant modifiers of the risk of radiation-induced thyroid can- cer. There is no convincing evidence that the incidence of CHILDREN OF ADULTS EXPOSED TO RADIATION leukemia has increased in children or adult residents of the exposed populations; however, few studies of leukemia have Table 9-5A lists three ecologic studies of children of been conducted to date and most have employed ecologic adults exposed to radiation. The focus is on preconception designs that are relatively insensitive. There have been very parental exposure and the risk of leukemia and lymphoma in TABLE 9-4 Populations Exposed from Natural Background Radiation—Ecologic Studies Incidence/ Population Type of Dates of Outcomes Number Reference Mortality Studied Exposure Accrual Type of Dosimetry Studied of Cases Summary of Results Wang Prevalence Women ages Natural 1986 Measured external Thryoid nodularity, Nodules in No difference in and others 50–65 living in background (survey) exposure (average serum thyroid high areas prevalence of nodules; (1990) Yangjiang, (mostly annual dose in high- hormone levels, (95); in no difference in thyroid China, vs. external background area: chromosome control hormone levels; nearby control whole-body 330 mR; in control aberrations areas (93) increased frequency of areas gamma) area: 114 mR) unstable chromosome aberrations Lu-xin Mortality Population of Natural 1970– Measured annual 11 cancer sites High- No increase in high- (1994) Yangjiang, background 1986 external exposure exposure background areas except China, vs. radiation (mR) area 914; cervix control area control (not specified) 1032 Richardson Incidence Children under Natural 1969– Survey of radon and Leukemia 6691 No association of and others age 15 in Great background 1983 gamma concentrations childhood leukemia with (1995) Britain (gamma in homes; gamma indoor or outdoor and radon) outside; 459 districts gamma levels Nair Incidence Population of Thorium 1990– Gamma measurements All cancers Not given No evidence of higher and others Karunagappally deposited 1996 made in each house incidence of cancer in (1999) tuluk in Kerala, along areas of higher natural India coastal gamma radiation areas exposure (gamma)

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ENVIRONMENTAL RADIATION STUDIES 229 TABLE 9-5A Children of Adults Exposed to Radiation—Ecologic Studies Incidence/ Population Type of Dates of Outcomes Number Reference Mortality Studied Exposure Accrual Type of Dosimetry Studied of Cases Summary of Results Kinlen Incidence Residents of Paternal 1951– Lifetime preconception Leukemia Leukemia: Significant excess of leukemia (1993a) Seascale below preconception 1991 dose obtained from and NHL 5 in Seascale; and NHL in Seascale among age 25 in whole-body employment records NHL: 3 in those born in Seascale, and 1951–1991 dose (mSv) Seascale those born elsewhere Parker NA Children born Paternal NA Total cumulative and Radiation 9256 births 7% of collective and others in Cumbria preconception 6-month preconception doses (no to fathers preconception dose is (1993) from 1950 to whole-body dose, obtained from disease exposed to associated with children born 1989 to fathers dose employment records outcomes) radiation in Seascale; mean individual employed at before preconception doses Sellafield conception consistently lower in Seascale Wakeford Incidence Residents of Paternal 1968– Cumulative Leukemia 41 Increased incidence in some and West Cumbria preconception 1985 preconception dose groups defined by area and Parker under age 25 whole-body obtained from worker age; no increase associated (1996) dose records with paternal preconception dose the offspring of exposed parents. These studies followed the to radionuclides in the 6 months prior to the conception of findings first published by Gardner and colleagues (Gardner 14,869 children dying of cancer. For all childhood cancers, and others 1990a, 1990b) suggesting that an excess incidence the RR was 2.9 (95% CI 1.2, 7.1) for those potentially of leukemia in children in West Cumbria may be due to pa- exposed to radionuclides. There was no evidence of an asso- rental preconception exposure to ionizing radiation during ciation between external ionizing radiation and cancer risk. employment at the nearby Sellafield nuclear fuel processing The most recent study by Draper and colleagues (1997) plant. All three studies were conducted in relation to expo- found an increased risk of childhood leukemia and NHL sures received by parents working at the Sellafield nuclear among children whose fathers were radiation workers (RR facility in Great Britain. One study (Parker and others 1993) 1.8; 95% CI 1.1, 3.0). The risk was also elevated for all other is a radioecologic study, examining the distribution of pos- childhood cancers among offspring of mothers who were sible doses received by fathers employed at Sellafield of chil- radiation workers (RR 5.0; 95% CI 1.4, 26.9). There was no dren born in Cumbria from 1950 to 1989; it does not address evidence of a dose-response trend. In summary, none of the disease outcome. Although there is some evidence of an in- studies provides quantitative information from dose- creased risk associated with measures of individual dose in response analyses or quantitative estimates of the risk of dis- the other two studies, the findings are based on very small ease associated with exposure, and results across studies are numbers of cases and the results across studies are not con- inconsistent. sistent. Table 9-5C describes cohort studies published regarding A larger number of case-control studies have been con- the risk of cancer and adverse reproductive outcomes in chil- ducted to investigate the possible relationship between ra- dren of adults exposed to radiation. Two are studies by diation exposure of adults and subsequent cancer in their Gardner and colleagues (1987) that are not based on indi- offspring. Table 9-5B summarizes the results of seven pub- vidual estimates of radiation dose but rather on proximity to lished case-control studies. Six of the seven studies included the Sellafield nuclear plant at different ages (at birth and in the table are investigations that are related to findings first while attending school). A third (Roman and others 1999) is published by Gardner and colleagues (1990b). The six stud- an attempt to confirm Gardner’s findings of an increased ies summarized here include investigations in England and risk of leukemia and lymphoma in children born to fathers Wales, Scotland, and Canada. All but one investigated leu- with preconception radiation exposure. Individual paternal kemia and/or childhood cancer. The seventh study by Sever preconception exposure was estimated from employment and colleagues (1988) is a study of congenital malforma- records. Person-years at risk were accrued from date of birth tions. All but the study by Sorahan and Roberts (1993) used for 39,557 children of male workers and 8883 children of employment records and recorded doses to estimate indi- female workers until age 25, cancer diagnosis, or death. A vidual preconception radiation dose. The study by Sorahan total of 111 cases of malignant cancer were found, but there and Roberts (1993) used job histories to estimate paternal was no evidence of increased risk relative to the general exposure to ionizing radiation and the potential for exposure population. Rate ratios for all cancers (adjusted for calendar

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TABLE 9-5B Children of Adults Exposed to Radiation—Case-Control Studies 230 Population Studied Number of Subjects Dates of Type of Reference Cases Controls Cases Controls Accrual Type of Exposure Dosimetry Summary of Results Sever Congenital malformations, Selected from hospital 672 977 1957–1980 External whole-body Recorded doses Overall, no association with and others identified from 3 hospitals delivery room records, next radiation obtained from employment at Hanford; (1988) in two counties near live birth, matched by sex, Hanford records; suggestion of increase with Hanford mother’s age (5 years), race estimates in parental preconception dose; millisieverts some increases evident in subgroups Gardner Leukemia and lymphoma From birth register, Leukemia (52); 1001 Diagnosis: Total and 6-month Doses from Leukemia and NHL higher in and others in people under 25 born in matched by date of birth NHL (22); 1950–1985 external whole-body worker radiation children born near Sellafield, (1990b) West Cumbria and sex: local group, Hodgkin’s preconception records (British and with fathers employed at the matched by parish; area disease (23) exposure; antenatal Nuclear Fuels) plant especially those with high group, unmatched X-ray preconception doses Kinlen Leukemia and lymphoma Randomly selected from 1024 3783 1958–1990 Total, 3-month, and Doses from No significant excess in any (1993b) in people born in Scotland births, matched by county leukemia; 6-month preconception worker records subgroup; no association with since 1958, diagnosed and sex 237 NHL external whole-body (Scottish nuclear preconception radiation dose under age 25 dose industry) McLaughlin Children in Ontario, 0–14, Selected from births, 112 890 Deaths: Whole-body external Recorded doses No increased risk for any and others died from leukemia 1950– matched to case by date of 1950–1963; dose, whole-body from National exposure period or exposure (1993a) 1963 or diagnosed 1964– births (3 months) and diagnosis: external tritium dose, Dose Registry type 1988, born to mothers region of mother’s 1964–1988 radon dose living near nuclear facility residence at child’s birth Roman Leukemia or NHL, Two controls per case 54 324 1972–1989 Exposure to radiation Record of Cases were more likely to have a and others diagnosed ages 0–4, born selected from birth at work employment in parent employed in the nuclear (1993) in West Berkshire, registers; four per case nuclear industry; industry; fathers of cases were Basingstoke, and North from delivery registers in recorded film more likely to be monitored for Hampshire study area; matched by sex, badge dose if radiation; no dose-response date of birth (6 months), monitored evident for fathers monitored area of residence at birth, time of diagnosis Sorahan Children dying of cancer Selected from birth register, 15,279 15,279 1953–1981 6-month preconception; Expert No association with external and Roberts under age 16 in England, matched by local authority, external whole-body assignment, exposure; increased risk with (1993) Wales, and Scotland sex, date of birth dose; exposure to based on job potential exposure to radionuclides (unsealed titles radionuclides sources) Draper Childhood cancer in Great Selected from birth register 35,949 38,323 Great Total, 3-month and Doses recorded Fathers of cases more likely to and others Britain and Scotland for same area, born within Britain: 6-month preconception by National be radiation workers; no dose- (1997) 6 months of case, same sex 1952–1986; external whole-body Registry for response for any exposure Scotland: dose Radiation periods for fathers or mothers 1987–1990 Workers

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TABLE 9-5C Children of Adults Exposed to Radiation—Cohort Studies Incidence/ Cohort Comparison Dates of Type of Type of Outcomes Number Reference Mortality Definition Group Accrual Exposure Dosimetry Studied of Cases Summary of Results Gardner and Mortality Children attending U.K. national Beginning Presumed Attending school Major categories Total deaths: 10 No increase in relation to others (1987) school in Seascale up rates school– exposures from in community near of causes of national rates for all cancer, all to 11/84, born since 6/30/86 Sellafield Sellafield plant death causes, leukemia, or lymphoma 1950 Gardner and Mortality Children born to U.K. national 1950– Presumed Born in Major categories Total deaths 27; Approximately tenfold excess others (1987) mothers resident in rates 6/30/86 exposures from community near of causes of leukemia 5 of leukemia deaths vs. national Seascale from 1950 Sellafield Sellafield plant death rates; 2.5-fold excess for other to 1983 cancer; no increase for other causes Black and Incidence Children born in Scottish national 1969–1988 Presumed Born in or living Leukemia and Total cancer Increased incidence of others (1992) Dounreay area 1969– rates by tumor site, exposures from in Dounreay area NHL, Hodgkin’s cases in birth leukemia in both birth and 1988; children sex, age, and Dounreay of Caithness, disease, other cohort 5; total school cohorts: birth cohort attending local calendar year nuclear Scotland cancers cases in school O/E – 2.3 (0.7, 5.4); schools schools in the same reprocessing cohort 3 cohort O/E – 6.7 (1.4, 19.5) period born elsewhere plant Dickinson and Incidence 260,060 singleton Children of parents 1950–1989 External dose Recorded radiation Sex ratio Live births to Significantly higher sex ratio others (1996) births to mothers who worked at from ionizing dose obtained from fathers with (1.09; CI 1.06, 1.13) for resident in Cumbria, Sellafield anytime radiation to Sellafield facility dose prior to children of fathers exposed at U.K. between 1947 and fathers prior to conception: Sellafield than other Cumbria 1989 conception of 10,272 children. Increased sex ratio the child (1.4; CI 1.13–1.73) for children of fathers with >10 mSv in 90 d prior to conception Dummer and Mortality 256,066 live and Observed and 1950–1989 Presumed Proximity to and Stillbirths Live births to No evidence that proximity to others (1998) 4034 stillbirths to expected stillbirth exposures from direction from mothers within Sellafield increased risk of mothers resident in rates by distance Sellafield Sellafield of 25 km of stillbirth. No significant Cumbria, U.K. (in circles of 5, 10, mother’s residence Sellafield: increase in stillbirths with 15, 20, and 25 km) 54,746; distance within any of six and direction. stillbirths 888 directional sectors Expected estimated from rates in remainder of Cumbria Parker and Mortality 248,097 live and Children of father 1950–1989 External and Recorded radiation Stillbirths Live births in Significant increase in stillbirth others (1999) 3715 stillbirths to who worked at internal dose dose obtained from fathers exposed with father’s external radiation mothers resident in Sellafield anytime from ionizing Sellafield facility prior to dose prior to conception: OR Cumbria, U.K. between 1947 and radiation to conception: per 100 mSV 1.24 (CI 1.04, 1989 fathers prior to 9078; stillbirths 1.45). Risk higher for conception of 130 stillbirths with congenital the child anomaly and highest for neural tube defects 231

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TABLE 9-5C Children of Adults Exposed to Radiation—Cohort Studies 232 Incidence/ Cohort Comparison Dates of Type of Type of Outcomes Number Reference Mortality Definition Group Accrual Exposure Dosimetry Studied of Cases Summary of Results Roman and Incidence Children under age 25 External: national For external External Employment in All cancer, Total cancer No excess incidence over others (1999) of male employees of rates from England analyses: whole-body nuclear industry; leukemia, and 111 leukemia expected; leukemia in children three nuclear and Wales. born 1965 preconception whether monitored NHL 28 whose fathers received >100 authorities in Great Internal: within the or later; dose for radiation mSv preconception dose was Britain cohort by radiation for internal, exposure; dose 5.8 times that in children exposure levels born 1985 estimates from conceived prior to father’s or later records employment, based on 3 cases; no evidence of any dose- response for leukemia Doyle and Incidence Employees of AWE, Within the cohort 1993–1996 External and Whether monitored Fetal deaths and Live births: Risk of fetal death and others (2000) and mortality AEA and BNF, and by radiation internal dose for radiation congenital women 3048; congenital malformations not for AEA and BNF exposure level from ionizing exposure; if so, malformations men 20,899 related to whether father was past employees <75 radiation to dose estimates Fetal deaths: monitored for radiation prior to years old who were fathers prior to from records of the women 526; conception or to the dose of included in the conception of nuclear facility men 2723 radiation received. Risk of pension database the child early miscarriage (<13 weeks) was higher if mother was monitored before conception (OR 1.3; CI 1.0, 1.6), but no trend with radiation dose. Risk of stillbirth was also higher (OR 2.2; CI 1.0, 4.6). Risk of any major malformation not associated with maternal monitoring or dose prior to conception

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ENVIRONMENTAL RADIATION STUDIES 233 period, age and sex of child, and the number of children born founding by year of birth, a time-varying uncertainty (30%) to each parent) were significantly greater than 1.0 among in the recorded film badge doses, and the absence of infor- offspring of fathers who received cumulative external doses mation on concurrent exposures to organic chemicals in the of 100 mSv or 10 mSv in the 6 months prior to conception workplace. An earlier study of stillbirth rates around (4.1, 95% CI 1.4, 11.8, 5.1, 95% CI 1.6, 16.9), respectively. Sellafield (Dummer and others 1998) found no increase in It should be noted that these results were based on very few stillbirths in the resident population within 25 km of the cases (four and three, respectively). No trend of increasing facility. risk with cumulative dose was apparent. None of the three The Nuclear Industry Family Study in the United King- studies provide quantitative estimates of risk based on dose- dom has also investigated possible links between occupa- response analyses, and the results across studies are not con- tional radiation exposures and reproductive health (Mac- sistent. Thus, there is little evidence from epidemiologic onochie and others 1999). This study population includes all studies of a link between parental preconception exposure to current employees of the Atomic Energy Authority, Atomic ionizing radiation and childhood leukemia or other cancers. Weapons Establishment, and BNF, as well as past employees Other possible indices of the occurrence of transmissible who were under age 75 and on record at the pension admin- genetic damage from preconception exposures include spon- istration office. Information on reproductive health and taneous abortions, congenital malformations, neonatal mor- health of children was obtained through a mailed question- tality, stillbirths, and the sex ratio of offspring. Relatively naire and linked with data from the employers on occupa- few epidemiologic studies have been conducted to evaluate tional exposure to ionizing radiation. The database consists these outcomes in relation to preconception radiation expo- of 53,672 pregnancies, 39,557 reported by men and 8,883 by sure. Dickinson and colleagues (1996) examined the sex ra- women. Results of the analysis of fetal deaths and congeni- tio among children born to fathers employed at Sellafield. tal malformations were reported by Doyle and colleagues Exposure was assessed using two methods: total cumulative (2000). The risk of neither fetal death nor major congenital radiation dose prior to conception and dose received in the malformation was related to paternal preconception radia- 90 days prior to conception. Total cumulative dose did not tion dose. Although early miscarriage was more common account for a significant amount of variation in the sex ratio among mothers who had been monitored prior to conception during the period 1950–1988. No significant trend was ob- (OR 1.3; 95% CI 1.0, 1.6), there was no evidence of a dose- served between sex ratio and exposure 90 d prior to concep- response. Risk of fetal death was higher among mothers who tion, although the sex ratio was increased in children of fa- had been monitored prior to conception (OR 2.2; 95% CI thers in the highest-dose category (>10 mSv). Chance could 1.0–4.6). ORs were adjusted for parental age, birth order, not be ruled out as the reason for this result. previous fetal loss, calendar year of the end of pregnancy, A companion study investigated stillbirths in the offspring and manual versus nonmanual job status. No dose response of men employed at Sellafield (Parker and others 1999). In- was evident. dividual film badge doses were available by record linkage In summary, there have been a number of studies of chil- with the British Nuclear Fuels (BNF) dosimetry database. dren of adults exposed to radiation. Ecologic studies are Significant positive associations between both the total cu- based on very small numbers, and none provide quantitative mulative dose (OR per 100 mSv = 1.24; 95% CI 1.04, 1.45) information from dose-response analyses or quantitative es- and the dose during the 90 d prior to conception (OR per 100 timates of the risk of disease associated with exposure. There mSv = 1.86; 95% CI 1.21, 2.76) and risk of stillbirth were is little conclusive evidence from epidemiologic studies of a observed.3 A nested case-control study was conducted link between parental preconception exposure to radiation among radiation workers alone using live births matched on and childhood leukemia or other cancers. Few studies have sex and date of birth. In contrast with the cohort analysis, the been conducted to evaluate other possible indices of the oc- adjusted OR for exposure 90 d preconception was not sig- currence of transmissible genetic damage from preconcep- nificantly different from 1.00 (OR per 100 mSv = 1.08; 95% tion radiation exposures, such as spontaneous abortions, con- CI 0.68, 1.74). The total cumulative dose, however, did show genital malformations, neonatal mortality, stillbirths, and the a significant association with the occurrence of stillbirth (OR sex ratio of offspring. Some but not all studies have found a per 100 mSv = 1.24; 95% CI 1.04, 1.45). Although based on significant positive association between total cumulative only a few exposed individuals, neither analysis indicated dose, as well as dose during the 90 d prior to conception, and the presence of an association with internal exposure to the risk of stillbirth. The risk of neither fetal death nor major radionuclides. Limitations of the study noted by the authors congenital malformation has been related to paternal pre- included the possibility of the existence of residual con- conception radiation dose. EXPOSURE TO RADIOACTIVE IODINE 131 3OR represents the odds of being exposed among diseased persons di- In evaluating the evidence regarding the risk of cancer vided by the odds of being exposed among nondiseased persons. associated with exposure to environmental sources of radia-

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234 BEIR VII tion, internal exposure to 131I is of particular concern regard- (when analyzed separately), they were not statistically sig- ing the risk of thyroid cancer. In contrast to the considerable nificant. The study was limited by small numbers of exposed amount of information that is available from numerous stud- individuals and a low incidence of thyroid neoplasms and by ies of external radiation exposure, there is relatively little the fact that the examiners were not blinded to exposure. In information regarding the risk of thyroid cancer in humans contrast, a follow-up study of 3440 persons exposed as young exposed to 131I. Existing evidence comes from studies of 131I children to atmospheric releases of primarily 131I from the administered for therapeutic or diagnostic purposes and from Hanford Site found no increased risk of thyroid cancer asso- various environmental exposure settings, most notably from ciated with individual radiation dose to the thyroid (Davis recent studies of persons exposed to radiation from the and others 2001, 2004a). Chernobyl accident (reviewed above). The explanation for the apparent difference in results in Studies of therapeutic and diagnostic 131I exposures are the Utah study and the Hanford study is not clear. One pos- described in detail in Chapter 7. In brief, early studies of sibility is that the exposures were substantially different in persons receiving therapeutic 131I for hyperthyroidism found terms of the mix of radionuclides and the dose rate. Thyroid no convincing evidence that the risk of thyroid cancer was dose at Hanford was due almost entirely to 131I, whereas in increased (Dobyns and others 1974; Safa and others 1975; Utah there was greater contribution from other radioiodines Holm and others 1980a; Holm 1984); most of the partici- as well as external sources. Exposures in Utah were also pants were adults at the time of exposure, were followed for more concentrated and episodic than at Hanford, correspond- very short periods, had existing thyroid disease at the time of ing to specific nuclear tests. This likely resulted in doses treatment, and were treated with radiation doses that were being delivered at substantially higher dose rates (although quite high (generally 20,000–100,000 mGy). Results from a the total dose among 3545 study participants for whom thy- follow-up (Ron and others 1998a) of one of these studies roid doses could be estimated [mean 98 mGy] was similar to (Dobyns and others 1974) suggest an increased risk of death Hanford doses). A second possibility is that the Utah study’s from thyroid cancer in patients previously treated with 131I, estimated dose-response could have been biased in the di- but the numbers of excess deaths were small and it is likely rection of finding an association because the collection of that underlying thyroid disease might have contributed to dietary consumption data took place after thyroid disease these results. Similar results were obtained from a study of classification was known for each participant. 7400 patients who were treated with radioiodine from 1950 Extensive evaluation of the population of the Marshall to 1991 in England (Franklyn and others 1999). Studies have Islands has shown an increase in benign and malignant thy- also evaluated persons exposed to much lower doses (gener- roid nodules in residents of the northern atolls of Rongelap ally 500–1000 mGy) through diagnostic procedures (Holm and Utirik (Conard 1980, 1984). In addition, a retrospective and others 1980a, 1980b; Hall and others 1996). Although cohort study of more than 7000 Marshall Islanders showed there is some evidence of a small increase in thyroid cancer that the prevalence of palpable thyroid nodularity ( 1.0 cm) associated with such exposures, there is a lack of consis- decreased linearly with increased distance from the Bikini tency and the small increases in thyroid cancer in some stud- test site (Hamilton and others, 1987). More recently, there ies are likely due to the underlying thyroid condition. As for has been extensive investigation of populations exposed to the therapeutic studies described above, these too are prima- radioactive fallout (including 131I as a substantial compo- rily of persons exposed as adults. The thyroid gland is more nent) after the Chernobyl accident. Findings from these stud- radiosensitive in children than adults, most likely because of ies are reviewed and summarized above. more rapid growth in infants and children (Williams 2003) In summary, studies of exposure to 131I from therapeutic and because of differences in metabolism (Mettler and oth- and diagnostic uses provide some evidence of a small in- ers 1996). crease in thyroid cancer associated with such exposures, but Only a few studies have evaluated the effects of environ- there is lack of consistency in the findings. Furthermore, the mental exposure to radioactive iodine. In contrast to the small increases in thyroid cancer observed in some studies medical exposures summarized above, which were due ex- are likely due to the underlying thyroid condition, not to ra- clusively to 131I, environmental exposures have generally diation exposure. Results from environmental exposures contained mixtures of 131I, external radiation, and short-lived have been inconsistent. Findings of an increase in thyroid radioiodines. Initial studies of thyroid disease incidence in neoplasia in persons exposed to fallout in the Marshall Is- Utah schoolchildren exposed to fallout from atmospheric lands are limited by the lack of individual dosimetry. No nuclear weapons testing at the Nevada Test Site appeared to excess risk of thyroid cancer was found in residents exposed show no difference in thyroid disease outcomes compared to to radiation from Hanford, and the slight excess risk of thy- children from unexposed areas (Rallison and others 1975). roid neoplasms associated with radioiodine exposure of Utah However, a follow-up study reported a slight excess risk of residents from the Nevada Test Site was based on small thyroid neoplasms associated with radioiodine exposure numbers. (Kerber and others 1993). Although positive dose-response In contrast, substantial increases in thyroid cancer have trends were also noted for total nodules and thyroid cancer been reported in areas contaminated with radioactive fallout

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ENVIRONMENTAL RADIATION STUDIES 235 from Chernobyl, primarily among children. Although much being outside the United States. Most define exposure, or of the thyroid dose from Chernobyl is due to 131I, exposure potential for exposure, based on a measure of distance from to a mix of other radionuclides and the lack of individual the facility, and the focus of most of these investigations is dose estimates in most of the studies to date have made it leukemia and/or childhood cancer, although a few include difficult to develop quantitative risk estimates for radiation all cancers as an outcome. Notably, most of the studies do dose from 131I. However, there is now emerging evidence not specify the nature of the radiation exposure, and none of indicating that exposure to radiation from Chernobyl is asso- the 16 contain individual estimates of radiation dose. Al- ciated with an increased risk of thyroid cancer and that the though some of these studies report an increased occurrence relationship is dose dependent. These findings are based on of cancer that could be related potentially to environmental individual estimates of thyroid radiation dose and reveal radiation exposures, none provide a direct quantitative esti- strong and statistically significant dose-related increased mate of risk in relation to radiation dose. There have been risks that are consistent across studies. Thus, although the three case-control studies of persons living around a nuclear precise quantitative relationship between radiation dose from facility. One focuses on congenital and perinatal conditions, 131I and the development of thyroid neoplasia remains un- stillbirths, and infant deaths in relation to exposure from ura- certain at this time, recent findings from studies around nium mines. This study does not provide an estimate of ra- Chernobyl and Hanford provide important quantitative esti- diation risk associated with any of the indicators of expo- mates of risk as a function of dose. sure. The other two are of leukemia in children and young adults. Neither study found an increased risk associated with parental radiation exposure and X-ray exposure of the child, DISCUSSION but both did find an increased risk associated with playing A considerable number of papers have been published on beaches near the nuclear facility. from studies that have attempted to determine whether per- Several cohort studies have been reported of persons ex- sons exposed, or potentially exposed, to ionizing radiation posed to environmental radiation under various circum- from environmental sources are at an increased risk of de- stances: participation in atmospheric nuclear weapons tests veloping cancer. The existing published literature consists conducted by the United Kingdom and the United States; primarily of reports that are descriptive in nature and eco- residents and their offspring living near the Techa River in logic in design. Such studies are limited in their usefulness the southern Urals of the Russian Federation and exposed in defining risk of disease in relation to radiation exposure or from the nearby Mayak nuclear complex; residents living dose. They can sometimes be informative in generating new near the Hanford Site in eastern Washington State; and resi- hypotheses or suggesting directions for study, but seldom, if dents of the Marshall Islands. Overall, studies of persons ever, are they of value in testing specific hypotheses or pro- who participated in U.K. atmospheric nuclear weapons tests viding quantitative estimates of risk in relation to specific found no increased risk of developing cancer or other fatal sources of environmental radiation. Fewer attempts have diseases as a function of estimated dose received, but there been made to evaluate the effect of environmental radiation was some evidence of an increase in non-CLL leukemia. In exposures using the two most common analytical study de- contrast, a recent study of U.S. veterans who participated in signs employed in epidemiology: the case-control study and atmospheric nuclear weapons tests reported a significant in- the cohort study. Such studies are almost always based on crease in death from all causes and for all lymphopoietic individual-level data and thus are not subject to many of the cancers combined. limitations inherent in ecologic studies. They can potentially Results from studies of residents living near the Techa provide quantitative estimates of risk based on individual River have found no evidence of a decrease in birth rate or radiation dose. fertility in the exposed population and no increased incidence Epidemiologic studies, in general, have limited ability to of spontaneous abortions or stillbirths. There is some evi- define the shape of the radiation dose-response curve and to dence of a statistically significant increase in total cancer provide quantitative estimates of risk in relation to radiation mortality. Estimates of the relative risk for cancer of the dose, especially for relatively low doses. To be informative esophagus, stomach, and lung are similar to those reported in this regard a study should (1) be based on accurate, indi- for atomic bomb survivors. There is no evidence of an in- vidual dose estimates, preferably to the organ of interest; crease in cancer mortality in the offspring of exposed resi- (2) contain substantial numbers of people in the dose range dents. The one study of persons living in the town of Ozyorsk of interest; (3) have long enough follow-up to include ad- exposed to fallout from the nearby Mayak nuclear facility equate numbers of cases of the disease under study; and reported an excess of thyroid cancer three to four times that (4) have complete and unbiased follow-up. Unfortunately, expected relative to rates for all of Russia and a somewhat the published literature on environmental radiation expo- lower excess (1.5 to twofold higher) based on a comparison sures is not characterized by studies with such features. with Chelyabinsk Oblast rates. Sixteen ecologic studies of populations living around A follow-up study of persons exposed as young children nuclear facilities are summarized, thirteen of the locations to atmospheric releases primarily of 131I from the Hanford

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236 BEIR VII Site in eastern Washington State found no increased risk of tive risks per unit dose for males and females. Iodine defi- thyroid cancer associated with individual radiation dose to ciency also appears to be an important modifier of the risk of the thyroid. A prevalence study of thyroid cancer conducted radiation-induced thyroid cancer, and there is some evidence through screening of 3709 Marshall Island residents born that iodine deficiency enhances the risk of thyroid cancer before the Castle BRAVO atmospheric nuclear weapons test following radiation exposure. Finally, relatively little has on March 1, 1954, found some indication that the prevalence been published regarding thyroid outcomes other than thy- of thyroid cancer increased with quartile of estimated dose, roid cancer, although one study has reported an elevated risk but the increase was not statistically significant. of benign thyroid tumors and there have been reports of in- Numerous epidemiologic studies have been carried out creases in autoimmune disease and antithyroid antibodies since the Chernobyl accident to investigate the potential late following childhood exposure to Chernobyl. health consequences of exposure to ionizing radiation from Evidence from epidemiologic studies regarding the risk the accident. These studies have focused largely on thyroid of leukemia in the general population reflects low-dose-rate cancer in children, but have also included investigations of exposure (primarily from 137Cs), which has occurred for a recovery operation workers and residents of contaminated number of years and will continue to occur in the future. areas, and have investigated the occurrence of leukemia and These resident populations were exposed at all ages, but stud- solid tumors other than thyroid cancer among exposed indi- ies of residents are primarily of persons exposed as children viduals. Overwhelmingly, the published findings are from and/or in utero. studies that are ecologic in design and therefore do not pro- At present, the available evidence from ecologic studies vide quantitative estimates of disease risk based on indi- does not convincingly indicate an increased risk of leukemia vidual exposure circumstances or individual estimates of ra- among persons exposed in utero to radiation from Cher- diation dose. Most reports are descriptive incidence and nobyl. There are no data from analytic epidemiologic studies prevalence studies that utilize population or aggregate esti- in which individual dose estimates are available. The exist- mates of radiation dose. Only three analytical studies are ing evidence does not support the conclusion that the rates of published that report dose-response results based on indi- childhood leukemia have increased as a result of radiation vidual dose estimates. exposure from the Chernobyl accident. However, ecologic Numerous reports have continued to describe an increas- studies of the types conducted to date are not particularly ing number of cases of thyroid cancer, particularly in the sensitive to detecting relatively small changes in the inci- most heavily contaminated regions of Ukraine and Belarus, dence of a disease as uncommon as childhood leukemia over as well as in Russia. Collectively, findings reported to date time or by different geographic areas. The single analytical have demonstrated an association between an increase in study is insufficient to draw conclusions regarding leukemia thyroid cancer incidence and radiation exposure from the risk after exposure of children to Chernobyl. There is also no Chernobyl accident. This increase cannot be explained only convincing evidence that the incidence of leukemia has in- by the aging of the cohort and the improvement of case de- creased in adult residents of the exposed populations that tection and reporting. Although there is now little doubt that have been studied in Russia and Ukraine. However, few studies an excess of thyroid cancer has occurred in highly contami- of the general adult population have been conducted, and they nated areas, there is still very little information regarding the have employed ecologic designs that are relatively insensitive. quantitative relationship between radiation dose to the thy- There has been relatively little study of the incidence or roid from Chernobyl and the risk of thyroid cancer. Results mortality from solid cancers other than thyroid cancer in from three analytical studies published indicate that expo- populations exposed to radiation from the Chernobyl acci- sure to radiation from Chernobyl is associated with an in- dent. Two studies have investigated solid cancer incidence creased risk of thyroid cancer and that the relationship is in liquidation workers. They reported increases of cancer dose dependent. The findings from these studies are consis- incidence during the periods, but generally the excesses were tent with descriptive reports from contaminated areas of relatively small and not statistically significant. No descrip- Ukraine and Belarus, and the quantitative estimate of thy- tive or analytical epidemiologic studies of breast cancer risk roid cancer risk is generally consistent with estimates from in populations exposed to radiation from Chernobyl have other radiation-exposed populations. Available data on ex- been published in the peer-reviewed literature; however, one posure from the Chernobyl accident are largely in agreement monograph has cited elevated breast cancer incidence rates with observations from other studies showing that exposure based on Ukrainian registries. Similarly, although no de- at the youngest ages is associated with the greatest risk of scriptive or analytical epidemiologic studies of bladder or thyroid cancer. At present no data are available from kidney cancer risk in relation to Chernobyl have been pub- Chernobyl regarding the risk of thyroid cancer from in utero lished in the peer-reviewed literature, there has been a series exposure. Fifteen years after the Chernobyl accident, thy- of papers investigating aspects of possible radiation carcino- roid cancer incidence is still highly elevated. An increase in genesis in these organs. thyroid cancer has been observed in both males and females, Four ecologic studies of populations exposed to natural and most of the Chernobyl studies have reported similar rela- background radiation have been reported. Two were con-

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ENVIRONMENTAL RADIATION STUDIES 237 ducted in China, one in Great Britain, and one in India. These radiation dose and reveal strong and statistically significant studies did not find any association between disease rates dose-related increased risks that are consistent across stud- and indicators of high background levels of radiation, and ies. They provide important quantitative estimates of risk as they do not provide any quantitative estimates of disease risk. a function of dose, primarily from 131I. Three ecologic studies of children of adults exposed to radiation have been published, with a focus on preconcep- SUMMARY tion parental exposure and the risk of leukemia and lym- phoma in the offspring of exposed parents. All three studies This chapter reviews the evidence from peer-reviewed were conducted in relation to exposures received by parents articles published since BEIR V (NRC 1990) of the relation- working at the Sellafield nuclear facility in Great Britain. ship between exposure to ionizing radiation from environ- Although there is some evidence of an increased risk associ- mental sources and human health. ated with measures of individual dose, the findings are based Ecologic studies of populations living around nuclear fa- on very small numbers of cases and the results across studies cilities neither contain individual estimates of radiation dose are not consistent. A larger number of case-control studies nor provide a direct quantitative estimate of risk in relation have been conducted to investigate the possible relationship to radiation dose. Similarly, the one case-control study of between radiation exposure of adults and subsequent cancer congenital and perinatal conditions, stillbirths, and infant in their offspring. In summary, none of the studies provide deaths in relation to exposures from uranium mines does not quantitative information from dose-response analyses or provide an estimate of the risk associated with any of the quantitative estimates of the risk of disease associated with indicators of exposure, and two ecologic studies of popula- exposure, and results across studies are inconsistent. There tions exposed to fallout from atmospheric nuclear testing or have been three cohort studies published regarding the risk other sources of environmental release of radiation provide of cancer in children of adults exposed to radiation. None of no quantitative estimates of the risk associated with pre- the three provide quantitative estimates of risk based on sumed exposure. dose-response analyses, and the results across studies are Several cohort studies have been reported of persons not consistent. Thus, there is little conclusive evidence from exposed to environmental radiation under various circum- epidemiologic studies of a link between parental preconcep- stances. No increased risk of developing cancer or other fatal tion exposure to ionizing radiation and childhood leukemia diseases was found in persons who participated in U.K. or other cancers. atmospheric nuclear weapons tests, but there was some evi- Other possible indices of the occurrence of transmissible dence of an increase in non-CLL leukemia. U.S. veterans genetic damage from preconception exposures include spon- who participated in atmospheric nuclear weapons tests re- taneous abortions, congenital malformations, neonatal mor- ported a significant increase of death from all causes and for tality, stillbirths, and the sex ratio of offspring. Relatively all lymphopoietic cancers combined. There is no evidence of few epidemiologic studies have been conducted to evaluate a decrease in birth rate or fertility or an increased incidence these outcomes in relation to preconception radiation expo- of spontaneous abortions or stillbirths in residents living near sure, and there is no consistent evidence of an association of the Techa River in the Russian Federation. There is some any such outcomes with exposure to environmental sources evidence of a statistically significant increase in total cancer of radiation. mortality, but no evidence of an increase in cancer mortality Studies of exposure to 131I from therapeutic and diagnos- in the offspring of exposed residents. Persons living in the tic uses provide some evidence of a small increase in thyroid town of Ozyorsk (Russia) exposed to fallout from the nearby cancer, but the small increase observed is likely due to the Mayak nuclear facility reported an excess of thyroid cancer underlying thyroid condition, not to radiation exposure. (1.5–4 times higher than expected). No increased risk of thy- Findings of an increase in thyroid neoplasia in persons ex- roid cancer was found associated with individual radiation posed to fallout in the Marshall Islands are limited by the dose to the thyroid in persons exposed as young children to lack of individual dosimetry. No excess risk of thyroid can- atmospheric releases primarily of 131I from the Hanford Site cer was found in residents exposed to radiation from in eastern Washington State. There is some indication that Hanford, and only a slight excess risk of thyroid neoplasms the prevalence of thyroid cancer among Marshall Island resi- was found associated with radioiodine exposure of Utah resi- dents born before the Castle BRAVO atmospheric nuclear dents from the Nevada Test Site. In contrast, substantial in- weapons test increased with quartile of estimated dose, but creases in thyroid cancer have been reported in areas con- the increase was not statistically significant. taminated with radioactive fallout from Chernobyl, primarily There continues to be an increasing number of cases of among children. Recent evidence from three population- thyroid cancer in populations exposed to radiation from the based case-control studies indicates that exposure to radia- Chernobyl accident that cannot be explained only by the ag- tion from Chernobyl is associated with an increased risk of ing of the cohort and the improvement in case detection and thyroid cancer and that the relationship is dose dependent. reporting. Results from three analytical studies indicate that These findings are based on individual estimates of thyroid exposure to radiation from Chernobyl is strongly associated

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238 BEIR VII with an increased risk of thyroid cancer in a dose-dependent are based on very small numbers of cases and the results manner, and the quantitative estimate of thyroid cancer risk across studies are not consistent. A larger number of case- generally is consistent with estimates from other radiation- control studies provides no quantitative estimates of the risk exposed populations and is observed in both males and fe- of disease in offspring of exposed parents, and results across males. At present, no data are available from Chernobyl re- studies are inconsistent. None of three published cohort stud- garding the risk of thyroid cancer from in utero exposure. ies provide quantitative estimates of risk based on dose-re- Iodine deficiency appears to be an important modifier of risk, sponse analyses, and the results across studies are not con- enhancing the risk of thyroid cancer following radiation ex- sistent. Relatively few epidemiologic studies have been posure from Chernobyl. Relatively little has been published conducted to evaluate outcomes such as spontaneous abor- regarding thyroid outcomes other than thyroid cancer, al- tions, congenital malformations, neonatal mortality, still- though one study has reported an elevated risk of benign births, and the sex ratio in relation to preconception radia- thyroid tumors and there have been reports of increases in tion exposure, and there is no consistent evidence of an autoimmune disease and antithyroid antibodies following association of any such outcomes with exposure to environ- childhood exposure to Chernobyl. mental sources of radiation. Evidence from ecologic studies does not indicate an in- In contrast to the considerable amount of information that creased risk of leukemia among persons exposed in utero to is available from numerous studies of external radiation ex- radiation from Chernobyl nor that rates of childhood leuke- posure, there is relatively little information regarding the risk mia have increased. A single analytical study is insufficient of thyroid cancer in humans exposed internally to 131I. There to draw conclusions regarding leukemia risk after exposure is some evidence of a small increase in thyroid cancer asso- of children to Chernobyl. There is no convincing evidence ciated with exposure to 131I from therapeutic and diagnostic that the incidence of leukemia has increased in adult resi- uses, but the findings are inconsistent and the small increases dents of the exposed populations that have been studied in in thyroid cancer observed in some studies are likely due to Russia and Ukraine. There has been very little study of the the underlying thyroid condition, not to radiation exposure. incidence or mortality from solid cancers other than thyroid Results from environmental exposures have also been in- cancer in populations exposed to radiation from the Cher- consistent. An increase in thyroid neoplasia has been ob- nobyl accident, and there is no evidence of significant ex- served in persons exposed to fallout in the Marshall Islands, cesses of any other solid cancer type. but no excess risk of thyroid cancer was found in residents Four ecologic studies of populations exposed from natu- exposed to radiation from Hanford, and the slight excess risk ral background radiation did not find any association be- of thyroid neoplasms associated with radioiodine exposure tween disease rates and indicators of high background levels in Utah residents from the Nevada Test Site was based on of radiation exposure (for a general discussion of the limita- very small numbers. In contrast, substantial increases in thy- tions of ecologic studies see the introduction to this chapter roid cancer have been reported in areas contaminated with and, more specifically in reference to studies of populations radioactive fallout from Chernobyl, primarily among chil- exposed from natural background radiation, see Appendix dren. Recent evidence indicates that exposure to radiation D, “Hormesis and Epidemiology”). from Chernobyl is associated with an increased risk of thy- Ecologic studies of children of adults exposed to radia- roid cancer and that the relationship is dose dependent. These tion while working at the Sellafield nuclear facility in Great findings are based on individual estimates of thyroid radia- Britain have suggested some increased risk of leukemia and tion dose and reveal strong and statistically significant dose- lymphoma associated with individual dose, but the findings related increased risks that are consistent across studies.