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c Radiogenic Cancer at Specific Sites LEUKEMIA The induction of leukemia by ionizing radiation has been well docu- mented in humans and laboratory animals. The types of leukemia induced and their rates of induction vary markedly, depending on the species, strain, age at irradiation, sex, and physiological state of the exposed individuals. They also depend on the dose, dose rate, anatomical distribution, and LET of the radiation, among other variables. The early literature has been summarized elsewhere (NRC80, UN77, UN82, UN86, UNDO. Human Data The most extensive human data on the dose-incidence relationship come from studies of the Japanese atomic-bomb survivors and patients treated with x rays for ankylosing spondylitis. In the atomic-bomb survivors of the Life Span Study Cohort, a total of 202 deaths from leukemia were recorded for the period from 1950 to 1985, during which there were an esti- mated 2,185,335 person-years of follow-up. Analyzed in terms of absorbed dose to the bone marrow as estimated with the new DS86 dosimetry, the dose response for Nagasaki rises less steeply than for Hiroshima, especially in the dose range below 0.5 Gy, but the difference between the two cities is smaller with the DS86 dosimetry than with the T65D dosimetry and is no longer significant (Sham. For the combined data, the rate of mortality is significantly elevated at 0.4 Gy and above but not at lesser doses. At bone marrow doses of 3-4 Gy, the estimated dose-response curve pecks and 242
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RADIOGENIC CANCER AT SPECIFIC SITES ~ 1 5 o cn [,J 1 0 o a) Q An I LD LL y 0 1 2 243 ~(32)t(18)~(21) 1 (10) 1 (10) 1 (6) 1 i: 5 0( it. / - - - ~0 Number of cases in the ( ) I indicated dose interval 3 4 5 6 MARROW DOSE EQUIVALENT (Sv) 7 8 9 FIGURE 5-1 Cumulative leukemia mortality in Hiroshima and Nagasaki as a function of the estimated dose equivalent to the bone marrow under DS86. By 1985, there were 51 cases in the O Sv category and 31 cases in the 0.01-0.1 Sv stratum. turns downward (Figure 5-1~. As noted below, this pattern is characteristic of the leukemia response in other irradiated populations. The saturation of the leukemia response at high doses has been attributed to the reduced survival of potentially transformed myeloblasts in the range above 3-4 Gy (Unapt. Based on a simple linear dose-response model, which in the opinion of RERF analysts fit the LSS data for leukemia mortality as well as a linear- quadratic model and better than a simple quadratic model, the excess relative risk per Sievert was estimated to range from 4.24 to 5.21, and the number of excess deaths per 104 person-year-Sv was estimated to range from 2.40 for a neutron RBE of 20 to 2.95 for an RBE of 1 (Sham. The excess mortality from leukemia reached a peak within 10 years after irradiation and has persisted at a diminished level (Figure 5-2~. No excess cases of chronic lymphocytic leukemia have been observed (Pr87a). Among 14,106 patients who were followed for up to 48 years after a single course of x-ray therapy for ankylosing spondylitis, 39 deaths from leukemia were recorded versus a total of 12.29 expected cases (ratio of observed to expected deaths, 3.17) (Damp. The excess deaths became detectable within two years after irradiation, reached a peak within the first 5 years, and declined thereafter; however, the excess death rate remained significantly elevated (relative risk, 1.87) for more than 15 years, after which it appeared to persist with little change (Damp. The relative risk did not vary significantly with age at the time of treatment, but it was higher in males (3.43) than in females (1.79~. The relative risk also varied with the hematologic type of the disease, being higher for those with acute myeloid l
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244 EFFECTS OF EXPOSURE TO LOW LE~LS OF lONIZI`VG MOTION 25 10 ID t CD s y En 111 > 111 llJ En ILL 1 4 ~ \ \ .. - 54-~- 573 All Cancers Except Leukemia (+4.8%/year) 0.5 1 1 1 1 1 1 1 1 _ 26 _ Leukemia T ~-0.7%/year, 18 ., 22 1 ~' 1 856 26 - _ _ 942 :] 922 1950- 1955- 1959- 1963- 1967- 1971- 1975- 1979 1954 1958 1962 1966 1970 1974 1978 1982 INTERVAL OF FOLLOW-UP FIGURE 5-2 Relative risk of mortality from leukemia and all cancers other than leukemia in A-bomb survivors, 1950-1982, in relation to time after inadiation. The number of deaths in each interval of follow-up and 99~o confidence intervals are indicated (Pr874.
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RADIOGENIC CANCER AT SPECIFIC SITES TABLE 5-1 Observed, as Compared with Expected, Numbers of Deaths from Leukemia in Persons Treated with Spinal Irradiation for Ankylosing Spondylitisa Number of Deaths Type of Leukemia Observed - Expected Myeloid leukemia Acute 17 4.34 3.92 Chronic 3 2.05 1.46 Unspecified 4 0.71 5.63 All types 24 7.10 3.38 Lymphatic leukemia Acute 2 0.93 2.15 Chronic 2 z.38 0.84 Unspecified 3 0.38 7.89 All types 7 3.69 1.89 Unspecified leukemia 3 0.28 10.71 All types 36 11.29 3.19 Ratio of Observed/Expected a From Darby et al. (Dated. b Observed and expected deaths from leukemia occurring more than one year after first treatment at ages less than 85 years by age at first treatment and by type of leukemia as recorded on the death certificate. Retreated patients were included for 12 months following treatment. 245 leukemia than for those with other types of leukemia. It was not elevated for those with chronic lymphatic leukemia Amble 5-1~. Analyzed in relation to the average dose to the bone marrow, which was estimated to be 3.21 Gy, the excess relative risk amounted to O.98/Gy, or 0.45 additional cases of leukemia per 104 PYGy (Smirk. The smaller magnitude of the risk per Gy in patients with anlylosing spondylitis, compared with that in atomic-bomb survivors, may be ascribable to the younger average age of atomic-bomb survivors at the time of exposure and to the fact that they received instantaneous whole-bady irradiation, whereas in the patients with anlylosing spondylitis only a portion of the active marrow was irradiated and the dose was received in fractionated exposures that usually totaled more than 5 Gy within a given treatment field (Leafy. Murrhead and Darby have proposed different models of leukemia risk for the spondylitics and the A-bomb survivors. They proposed a relative risk model for the spondylitics and an absolute risk model for the atomic-bomb survivors (Mush. In an international case-control study of 30,000 women treated with fractionated doses of radiation for carcinoma of the uterine cervix, the risk was estimated to be increased by about 70%/Gy, corresponding to an excess of 0~48 cases of leukemial104 PYGy (Bo87' Bosh. As in the
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246 EFFECTS OF EXPOSURE TO LOW LEVELS OF IONIZING EDITION Observed Data 2.8 2.6 2.4 Y 2.2 G lo > g tar 2.0 1.8 1.6 1.4 1.2 1.0 Off - Quadratic Exponential Linear Exponential (A w) Linear-Exponential (d) Linear ~- , ., L l I i I l l l l l 0 2 4 6 8 10 12 14 16 18 AVERAGE BONE MARROW DOSE (Gy) FIGURE 5-3 Relative risk of acute leukemia and chronic myeloid leukemia in women treated with radiation for carcinoma of the uterine cervix, as influenced by the average dose to the bone marrow. A better fit was obtained with a linear exponential model (~W) which considered the weighted dose to each marrow component as opposed to the average dose over all compartments (d) (Bomb. A-bomb survivors mentioned previously, the excess cases were confined to leukemias other than those of the chronic lymphatic type. The relative risk was maximal within the first 5 years after irradiation, was larger in women who were irradiated when they were under age 45 than in those who were irradiated when they were over age 45, and reached a peak at an average bone marrow dose of 2.5-5.0 Gy, above which it decreased (Figure 5-3~. The data conformed to a linear-exponential model in which the total risk equaled the sum of incremental risks to individually irradiated masses of marrow. The latter risks, in turn, were taken to increase linearly with the mass exposed and inversely with the total mass of marrow in the body; they were also taken to increase curvilinearly in a manner consistent with the dose-dependent killing of marrow cells (Bomb. In view of the decreased risk- per Gy at high doses, it is not surprising that the average risk per Gy in the women of this series was appreciably lower than that which has been observed in women treated with smaller doses of ~ rave for h~.nian gynecologic disorders (Bomb. ~d ~ ~ _ ^ ~ ~ ^ one Incidence of leukemia has been observed to be elevated similarly in patients treated with radiation for cancers of other sites (Bo84, Cu84, Waged. An association between previous diagnostic irradiation and adult
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RADIOGENIC CANCER AT SPECIFIC SITES 247 onset myeloid or monocytic leukemia has been suggested by three case- control studies (St62, Gu64, Gimpy; however, the data in the first and largest of the three studies (St62) have since been reinterpreted to argue against a causal relationship on the grounds that "the 'extra' examinations all happened within 5 years of the onset" of symptoms of leukemia (Steal. No association between previous diagnostic irradiation and adult-onset myeloid or monocytic leukemia was observed in a fourth case-control study (Light. On the basis of extrapolation from the leukemogenic effects of irradiation in atomic-bomb survivors and other relatively heavily irradiated groups, it has been estimated that about 1% of all leukemia cases in the general population may be attributable to diagnostic radiography (Every. The risk has not been confined to acutely irradiated populations, such as those mentioned above. Early cohorts of radiologists in the United States (Le63, Ma84), the United Kingdom (Co58), and the People's Re- public of China (WaS8), who were exposed to x rays occupationally in the days preceding modern safety standards, also have shown an increased inci- dence of acute leukemia and chronic granulocytic leukemia. These diseases have, likewise, been observed to occur with increased frequency in patients previously injected with radium-224 or Thorotrast (NRC80~. Because of uncertainty about the doses to the bone marrow in the occupationally and internally irradiated populations, it is not clear how their risks per unit dose compare with those in the more acutely irradiated populations described above. An excess number of cases of leukemia have been observed in children who were exposed to diagnostic x-irradiation in utero; the excess is larger per unit dose than that in children who were irradiated during postnatal life. The magnitude of the excess and the extent to which it may signify an unusually high susceptibility of the embryo and fetus are discussed in Chapter 6 of this report. Reports of an increased incidence of leukemia in children residing in the vicinity of nuclear installations in the United Kingdom are reviewed in Chapter 7. Committee Analysis For purposes of risk estimation, the Committee's analysis was restricted to the total mortality from leukemias of all hematologic types combined, excluding chronic lymphogytic leukemia. Modeling in terms of the various types of leukemia was not possible because of limitations in the available data. The different types vary markedly in the age distributions of their occurrence in the general population and in their relative frequencies with time after irradiation, depending on age at the time of exposure. To this extent, the Committee's risk model for leukemia is a gross simplification. For both the Life Span Study (LSS) and the Ankylosing Spondylitis
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248 EFFECTS OF EXPOSURE TO LOW LEVELS OF IONIZING MOTION (ASS) data, essentially comparable fits could be obtained using either additive or relative risk models, although somewhat different modifying effects were required in the two models and the relative risk model was consistently more parsimonious. It must be remembered that follow-up of the LSS cohort did not begin until five years after exposure, by which time the peak in the excess rate had already occurred in the ASS data. Despite this and other differences between the two studies, the modifying effects are reasonably consistent. The preferred model from the ASS data is a relative risk model with a decreasing effect in time after exposure. However, the addition of an effect of age at exposure significantly improves the fit of the LSS data. The magnitude of this effect and also the effect of time after exposure depends on whether exposure occurred before or after age 20. The ASS cohort did not include individuals younger than 20 years of age at exposure, so the age factor could not be tested in that data set. Dose-response in the LSS data was significantly improved by the addi- tion of a quadratic term in dose. (Here, the linear term includes both the gamma and neutron components, the latter weighted by the assumed RBE of 20; the quadratic component includes only the gamma component.) The "cross-over dose" (the dose at which the linear and quadratic contributions are equal) was estimated to be about 0.9 Gy. However, ratios of log likeli- hood estimates are biased and for these data the uncertainty is very large (see Annex 4F). Similarly, the "dose rate effectiveness factor" (DREF, the ratio of the fitted slopes of the pure linear and the linear~uadratic models) is estimated as 2 but again with a very large uncertainty. The final preferred model for leukemia mortality used in the risk projections is given by equation 4-3 reproduced below. /(d) = ID + ~3d2 ~ _ J exit < 15) + ,B2I(15 < T < 25~] if E ~ 20 9 ~ exp~3I(T ~ 25) + 341(25 20 Thy model is plotted as a function of attained age in Figure 5-4 and excess risk as a function of time after exposure for males is shown in Figure 5-5. The abrupt changes in risk with age at the time of irradiation that are specified in the model reflect simplifying compromises in model fitting and are not based on hypotheses concerning the biological mechanism of age dependent changes in susceptibility. Insofar as different types of leukemia vary in age distribution in the general population, their causative mechanisms and temporal distributions in irradiated populations might be expected to vary as well. This leukemia model is based on LSS data, which do not include information prior to five years post exposure. A number of fitted models
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4.6 4.2 3.8 >` 3.4 So a) Q 3.0 An ~ 2.6 LIJ > - LL 1.8 1.4 1.0 RADIOGENIC CANCER AT SPECIFIC SITES 0 10 20 249 Age at Exposure 5 15 25 45 60 30 40 50 AfrAINED AGE i 60 70 80 FIGURE 5-4 The relative risk of leukemia due to low LET radiation for both sexes by attained age from age 7 to age 75 for exposure at various ages. were tested but these produced rather varied and unreliable risk estimates in extrapolations to this early, first 5-year period. Sources of data, other than that from A-bomb survivors, provide some guidance on this point. The cervical cancer study by Boice et al. (Bo87) indicates that excess leukemia cases were observed only within the first five years post exposure. On the other hand, the spondylitic cohort shows a mixture of excess cases before and after five years post exposure (Damp. In that study, 14 cases with 1.6 expected were observed in the first five years, and 25 cases with 10.7 expected after five years post exposure. One could then reasonably argue that nearly one-half of the excess leukemias would be observed within the first five years after exposure. The Committee chose to model the 2- to S-year post-exposure period by extrapolating to two years the excess relative risk observed for the S- to 10-year post-exposure period. This method resulted in an approximately 15% increase in the lifetime risks. The Committee's extrapolation procedure for the 2- to S-year post- exposure period may lead to an underestimate of the actual risk, and this should be kept in mind when interpreting the Committee's risk estimates for leukemia.
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250 EFFECTS OF EXPOSE TO LOW LEVELS OF IONIZING MOTION 16 14 - >~ CD ~ 12 _ 0 _ Q 10 - cn I 8 6 LLJ C] co llJ X 4 2 _ , _~\ 1' / / /\ ~I ./ I ~1 '' .~1 ' 1 Age at Exposure __ i O1 1 1 1 1 1 1 1 1 1 1 1 ~ _ 0 4 8 12 16 20 24 28 32 36 40 TIME AFTER EXPOSURE a FIGURE 5-5 Excess leukemia deaths by time after exposure to low-LET radiation for U.S. males at various ages of exposure. Leukemia Studies in Animals In mice, rats, dogs, swine, and other laboratory animals, a variety of lymphoid and myeloid leukemias have been induced by irradiation (UN77, UN86, NRC80~. In such animals, the dose-incidence relationship has been observed to vary from one type of leukemia to another, but in no instance does it conform to a simple, linear nonthreshold function. The most extensively studied of the experimental leukemias are T-cell neoplasms that arise in the mouse thymus. The induction of these growths is inhibited drastically by shielding a portion of the hemopoietic marrow (UN77) and may involve the activation of a latent leukemia virus (Red LV) (Yo86~. The dose-incidence curve for the disease is of the threshold type in mice of certain strains (UNTO. In the range of 0.5-1.0 Gy, the RBE of fast neutrons for induction of these neoplasms has been observed to range from a value of 1.0-2.0 with single or fractionated exposures to a value exceeding 10 with continuous, duration-of-life irradiation (UN77, UN86 Fecal.
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RADIOGENIC CANCER AT SPECIFIC SITES 251 Less thoroughly investigated are experimentally induced myeloid leu- kemias, which have been observed in mice (Up70, Ma78, Hu87), dogs (Fr73), and swine (Ho70) that were subjected to various regimens of external or internal irradiation. The dose-incidence curve for myeloid leukemia in mice rises with increasing dose of acute whole-body x or gamma radiation, passes through a maximum at 2-3 Gy of x or gamma rays (lower dose of neutrons), and decreases at higher doses (Figure 5-6~; in the dose range below 1 Gy, the shape of the curve appears to vary among strains (UN86, U187~. The downturn in the dose-incidence curse at doses above 2-3 Gy is consistent with the reduction in numbers of potentially transformed myelopoietic cells surviving such doses (Gr65, Ba78, Ro78, Ma78, UNDO. In the low to intermediate dose range, the curve rises more steeply with fast neutrons than with x rays or gamma rays (Up70, Mo82, U187, Pr87a), and on fractionation or protraction, the incidence per Gy decreases markedly with x or gamma irradiation but decreases less markedly, if at all, with fast neutron irradiation (Figure 5-6~. As a result, the neutron RBE increases with decreasing dose rate, from a value of 2-3 at dose rates exceeding 0.1 Gy/minute to a value as high as 16 at dose rates of less than 0.01 Gy/minute (Upper. Various models have been fitted to the observed dose-incidence data, all of which have included cell-killing terms to account for the diminution of the response at intermediate to high dose levels (UNTO. Although the data do not exclude a linear dose term in the low to intermediate dose range, all models also include higher power dose terms to account for the fact that the incidence per Gy of low-LET radiation increases with increasing dose at high dose rates in the intermediate dose range but is substantially reduced at low dose rates (UNDO. The induction of myeloid leukemia, in contrast to induction of thymic lymphoma, is not inhibited disproportionately by shielding part of the hemopoietic system (Upon. The incidence of myeloid leukemia per Gy has been observed to be increased in mice in which granulocyte turnover is accelerated by injection of turpentine and decreased in mice in which granulocyte turnover is reduced by the elimination of microflora, implying that induction of the disease is promoted by proliferation of granulocyte precursors (Upped. Susceptibility to the induction of lymphoid and myeloid leukemias also varies among mice of different strains and in relation to age at the time of irradiation (UNTO. There is no evidence, however, that susceptibility in mice is unusually high during prenatal life; on the contrary, the data imply that it may be substantially reduced at that time of life (Up66, Si81, UNDO. Whereas the incidence of lymphoid and myeloid leukemias is typically increased by whole-body irradiation in most strains of mice, depending on the conditions of irradiation, the incidence of reticulum cell
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252 EFFECTS OF EXPOSURE TO LOW LEVELS OF IONIZING RADIATION 40 llJ A llJ z 20 n n x 10 ,,-'' I/ ~ /~K'/ \ ~6 in' \ - - -8 - 5 4 5 DOSE (Gy) \4 1 6 FIGURE 5-6 Lifetime incidence of myeloid leukemia (in excess of control incidence) in male mice of different strains, in relation to dose and dose rate of whole body neutron-, x-, or y-irradiation. REM mice (U187~: acute neutron irradiation (curve 1~; acute y-irradiation (curve 2~; CBA mice (Mo82, Mo83a, Mo83b). acute neutron irradiation (curve 3~; acute x-irradiation (curve 4~; protracted -radiation (curve 5~. RF/[Jp mice (Upper: acute neutron irradiation (curve 6~; protracted neutron irradiation (curve 7~; acute x-irradiation (curve 8~; protracted y-irradiation (curve 9~. neoplasms in such animals has usually been observed to decrease with increasing dose (UN77, UNBID. Summary The risks of acute leukemia and of chronic myeloid leukemia are increased by irradiation of hemopoietic cells, the magnitude of the increase depending on the dose of radiation, its distribution in time and space, and the age and sex of the exposed individuals, among other variables. The mean latent period preceding the clinical onset of the leukemia also varies, depending on the hematologic type of the disease as well as age at the time of irradiation. The data do not suffice to define the dose-incidence relationship precisely, but the dose-response curve for the total excess cases of leukemia appears to increase in slope with increasing mean dose to the marrow, to pass through a maximum in the dose range of 3-4 Gy, and to decrease with a further increase in the dose.
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RADIOGENIC CANCER AT SPECIFIC SITES 341 Ho80a Holm, L.-E., I. Dahlqvist, A. Israelsson, and G. Lundell. 1980. Malignant thyroid tumors after iodine-131 therapy. N. Engl. J. Med. 303:188-191. Ho80b Holm, L.-E., G. Eklund, and G. Lundell. 1980. Incidence of malignant thyroid tumors in humans after exposure to diagnostic doses of iodine-131. II. Estimation of thyroid gland size, thyroid radiation dose, and predicted versus observed number of malignant thyroid tumors. J. Natl. Cancer Inst. 65:1221-1224. Ho80c Holm, L-E., G. Lundell, and G. Walinder. 1980. Incidence of malignant thyroid tumors in humans after exposure to diagnostic doses of iodine-131. I. Retrospective cohort study. J. Natl. Cancer Inst. 64:1055-1059. Ho84b Holm, L.-E. 1984. Malignant disease following iodine-131 therapy in Sweden. Pp. 263-271 in Radiation Carcinogenesis: Epidemiology and Biological Sig nificance. J. D. Boice, Jr., and J. F. Fraumeni, Jr., eds. New York: Raven Press. Ho88 Holm, L-E., K E. Wicklund, G. E. Lundell, J. D. Boice, N. ~ Bergman, G. Bjelkengren, E. S. Cederquist, U.-B. C. Ericsson, L.-G. Larsson, M. E. Lidberg, R. S. Lindberg, and H. V. W~cklund. 1988. Thyroid cancer after diagnostic doses of iodine-131: A retrospective study. J. Natl. Cancer Inst. 80:1132-1136. Ho70 Howard, E. B., and W. J. Clarke. 1970. Strontium-90-induced hematopoietic neoplasms in miniature swine. Pp. 379-401 in Myeloproliferative Disorders of Animals and Man. U.S.AE.C. Div. Tech. Info., W. J. Clarke, E. B. Howard, and P. L. Hackett, eds. Hr89 Hrubec, Z., J. Boice, R. Monson, and M. Rosenstein. 1989. Breast cancer after multiple chest fluoroscopies: Second follow-up of Massachusetts women with tuberculosis. Cancer Res. 49:229-234. Hu63 Huggins, C., and R. Fukunishi. 1963. Cancer in the rat after single exposures to irradiation or hydrocarbons. Radiat. Res. 20:493-503. Hu87 Humphreys, E. R., J. F. Loutit, and V. A. Stones. 1987. The induction by 239 Pu of myeloid leukemia and outsosarcoma in female CBA mice. Int. J. Radiat. Biol. 51:331-339. Ic79 Ichimaru, M., T. Ishimaru, M. Mikami, and M. Matsunaga. 1979. Multiple myeloma among atomic bomb su~vivors, Hiroshima and Nagasaki, 1950-1976. Technical Report 9-79. Hiroshima: Radiation Effects Research Foundation. ICRP80 International Commission on Radiological Protection (ICRP). 1980. Pp. 1-108 in Biological Effects of Inhaled Radionuclides. ICRP Publication 31. Oxford: Pergamon. ICRP87 International Commission on Radiological Protection (ICRP). 1987. Pp. 1-60 in Lung Cancer Risk from Indoor Exposures to Radon Daughters. ICRP Publication 50. Oxford: Pergamon. Ir85 Ireland, J. P., S. J. Fleming, D. A. Levison, W. R. Cattell, and L. R. I. Baker. 1985. Parathyroid carcinoma associated with chronic renal failure and previous radiotherapy to the neck. J. Clin. Pathol. 38:1114-1118. Ja70 Jablon, S., and H. Kato. 1970. Childhood cancer in relation to prenatal exposure to atomic-bomb radiation. Lancet ii:1000-1003. Ja71 Janower, M. L., and O. S. Miettinen. Neoplasms after childhood irradiation of the thymus gland. J. Am. Med. Assoc. 215:753-756. Ka82 Kato, H., and W. J. Schull. 1982. Studies of the mortality of a-bomb survivors. 7. Mortality 1950-1978: part 1. Cancer mortality. Radiat. Res. 90: 395-432. Ka83 Katz, A., and G. D. Braunstein. 1983. Clinical, biochemical, and patho logic features of radiation-associated hyperparathyroidism. Arch. Intern. Med. 143:79-82.
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Representative terms from entire chapter: