Leukemia was the first late effect to be noticed among the atomic-bomb survivors and has always been strongly associated with exposure to ionizing radiation. A very recent paper on incidence of leukemia and other hematopoietic malignancies (Hodgkin and non-Hodgkin lymphomas, multiple myeloma) provides results for various subtypes and combinations of subtypes of leukemia (Hsu et al. 2013). The primary result is for a combination of the three types of leukemia generally considered to be increased by radiation exposure: acute myeloid leukemia (AML), acute lymphoblastic leukemia (ALL), and chronic myeloid leukemia (CML). The best-fitting dose response was a linear-quadratic function of dose with substantial upward curvature and ERR of 1.74 at 1 Gy, considerably larger than the ERR of all solid cancer. However, because the baseline incidence of leukemia is much smaller than that of all solid cancer, the absolute excess rates are much smaller. There were 312 cases of AML/ALL/CML in the 51 y follow-up of the LSS from 1950 to 2001 (Hsu et al. 2013) versus 17,448 first primary solid cancers in the 40 y follow-up from 1958–1998 (Preston et al. 2007). However, ∼94 of those 312 cases were considered to be associated with the radiation exposure. The relative risk of leukemia was larger for younger age at exposure, as with all solid cancer but more so—the risk was very high for times shortly after exposure at young ages, and the decline with age or time after exposure was much more marked than for solid cancer. The EARs, not just the ERR, declined with age or time since exposure, although the excess risk had not disappeared by the end of follow-up; even for the last 12 y of follow-up, 45–55 y after exposure, the radiation-associated risk at 1 Gy was estimated to be twice as large as the baseline risk. Measures of lifetime detriment have not been estimated in recent RERF papers on leukemia mortality in the LSS, but the BEIR VII report (NA/NRC 2006) gives estimates of lifetime attributable risk of mortality on the order of 0.03–0.05% for exposure to 0.1 Gy, depending on age at exposure, based primarily on analysis of the LSS mortality data. Furthermore, it is clear from the patterns of age-time modification noted above that LLE is dramatically larger for those exposed at younger ages. Regarding hematopoietic malignancies other than leukemia, there was a weak indication of a radiation risk of non-Hodgkin lymphoma among men, but not women, and no other remarkable risks among these malignancies (Hsu et al. 2013).
Mortality due to noncancer diseases as a group was first noticed to be in excess at high doses in the LSS after ∼30 y of follow-up (Kato et al. 1982) and has been more and more soundly established as a demonstrated radiation risk in the LSS reports (Shimizu et al. 1992), although with a substantially lower ERR than solid cancer. The effects of age at exposure and attained age on risk were examined in LSS Report 13 (Preston et al. 2003). In the period from 1966–2003, which was chosen to minimize the effect of selection bias due to the fact that members of the cohort had to have survived early effects and concomitant injury and disease, the ERR was estimated to be 0.13 for all noncancer diseases combined at 1 Gy, using a linear-quadratic model with slight upward curvature (Ozasa et al. 2012). Correspondingly, only ∼353 of 35,685 deaths were considered to be associated with the radiation exposure. Estimated and projected numbers of radiation-associated excess noncancer deaths in the LSS as a function of calendar time are shown in Fig. 5. In regard to lifetime detriment, Furukawa et al. (2009) give an estimated REID of ∼10% for women and 5% for men for those exposed to >1 Gy for most ages at exposure. As noted above under “Solid Cancer,” for radiation-associated cancer and noncancer mortality combined, they estimate a LLE of ∼15 y for women and 10 y for men, for those exposed to >1 Gy at <5 y of age (Furukawa et al. 2009).
Cataract has long been a recognized effect of ionizing radiation exposure, and recent work by RERF investigators has suggested that vision-impairing cataracts occur at substantially lower doses than previously appreciated. A recent paper suggested a threshold of 0.5 Gy for cataracts requiring surgery, with a linear dose response having ERR of 0.32 Gy−1 at 70 y of age for exposure at 20 y of age, with higher ERRs at younger ages at exposure (Neriishi et al. 2012), although the threshold estimate must be viewed cautiously, especially in light of the lack of evidence of curvature. The estimated EAR was 33 cases per 10,000 persons per year per gray (0.33% y−1 Gy−1); corresponding estimates of excess cases in the full LSS or lifetime detriment are not immediately available.
RERF results also suggest a risk of hyperparathyroidism, with an estimated ERR of ∼3 Gy−1 and some indication of increased risk at lower age at exposure (Fujiwara et al. 1992). The estimated prevalence rates were ∼2% in males and 5% in females in the groups with highest dose and lowest age at exposure, although the confidence bounds on all of the noted values are wide due to the small numbers of cases. There has also been evidence of radiation risk of benign as well as malignant thyroid nodules (Imaizumi et al. 2006) and another form of benign neoplasm: uterine myoma (fibroma) (Kawamura et al. 1997). Many of these findings have been confirmed by analysis of longitudinal data from the AHS (Yamada et al. 2004).
In addition to clinically manifest disease, the effect of radiation exposure is seen in a number of biomarkers among the survivors, whose implications remain to be completely elucidated. Perhaps the best known is the cytogenetic evidence of chromosomal aberrations, which is clearly related to radiation dose (Kodama et al. 2001). A number of immunological changes have also been observed and have been hypothesized to be related to disease via chronic inflammation (Kusunoki et al. 2002, 2010; Kusunoki and Hayashi 2008).
In a literal sense, evaluating the psychosocial effects of the radiation from the bombs per se is problematic for various reasons, including that the radiation was accompanied by so many other stresses and that survivors generally did not know and understand the extent of the doses that they had received personally. Hence studies have been predicated not on radiation dose but on the survivors’ experience related to the general situation. A study by RERF investigators concluded that persons who had been in the cities at the times of the bombings exhibited more anxiety and somatization symptoms that those who had not been in the cities (Yamada and Izumi 2002). Bromet (1998) has reviewed research on the psychosocial effects of the atomic bombs and other radiation disasters.
RERF analyses have suggested some special concerns about exposure in utero, based on studies of the related cohort. Perhaps most noted have been neurological effects, particularly the indication of a developmental effect on cognitive ability, which has been related to various measures such as school performance, intelligence tests, and diagnoses of severe developmental disability, and was specific to particular periods of gestation: 8 to 15 wk, and to a lesser extent, 16 to 25 wk after ovulation. The prevalence of severe developmental disability was estimated to be ∼40% for exposure to 1 Gy in the 8–15 wk period, with an indication of a threshold of at least 0.3 Gy, but the results were quite uncertain, being based on only 30 cases (Otake and Schull 1998; Douple et al. 2011). In regard to induction of cancer and leukemia, RERF studies have not confirmed some of the more extreme indications from elsewhere of a very high radiosensitivity for exposure in utero in contrast to postnatal exposure, although it should be noted that the ABCC/RERF follow-up of in utero survivors did not begin until 5 or 6 y of age for mortality and 11 or 12 y of age for incidence, and the risk estimates for prenatal exposure from RERF studies are not necessarily inconsistent with those of other major studies (Wakeford and Little 2003). RERF studies seem to indicate that the impact on survivors exposed in utero is not markedly greater than that for those exposed in early childhood, as discussed in the sections above, in regard to either mortality due to leukemia or solid cancer (Delongchamp et al. 1997) or incidence of solid cancer (Preston et al. 2008).
The dose distribution among in utero survivors exposed with DS02 dose estimates is very similar to that of the women in the LSS, as in utero doses are basically proportional to mothers’ doses, and there does not appear to have been any relation of pregnancy and shielded kerma (i.e., dose in air at the survivor’s shielded location). Because the cohort is so small and its members are younger than the youngest members of the LSS, the total number of cancers to date is very small, with only 94 cancers being eligible for the study in the most recent analysis of cancer incidence (Preston et al. 2008), and the estimated number of excess cases is tiny. As the group ages, given the points noted above regarding dose distribution and risk estimates, one might expect that excess numbers of cases in this group would be similar in proportion to the size of the cohort to those among persons exposed in childhood in the LSS, although there would be some minor differences because the dose distribution of in utero survivors is somewhat different from that of those exposed as children (Delongchamp et al. 1997). In regard to noncancer disease, a study involving clinical follow-up of survivors from the in utero clinical cohort failed to find clear evidence of radiation risk of hypertension, hypercholesterolemia, or cardiovascular disease, but the small size of the group (n = 506) and their young age at the time of the study (follow-up through 53 or 54 y of age) was very limiting (Tatsukawa et al. 2008). Much interest has been generated by findings that in utero exposed survivors did not have as many chromosomal aberrations as their mothers (Ohtaki et al. 2004), which runs counter to conventional ideas about the high radiosensitivity of the fetus and may be related to the lack of any particularly high apparent radiosensitivity noted above in regard to leukemia (Delongchamp et al. 1997). However, this phenomenon, which was observed in lymphocytes as are all typical chromosomal aberration assays, might be tissue specific, and ongoing research, including that in animal models, is investigating this question among others (Nakano et al. 2012).
The possibility of genetic effects was a very early concern in the work of ABCC and the subject of a major early study involving a population-based cohort of some 77,000 registered pregnancies to determine whether parental exposure to radiation was associated with untoward birth outcomes (Neel and Schull 1991). No significant effects were found. In the ensuing decades, ABCC and RERF have performed numerous studies that have changed in methodology with improvements in science and technology and are still ongoing, always aimed at detecting any inherited effect of parental radiation exposure but with no statistically significant results to date (Douple et al. 2011). Neither cancer incidence (Izumi et al. 2003a) nor mortality (Izumi et al. 2003b) among the children has shown an effect of parental exposure. Currently, a cohort of survivors’ children is receiving clinical follow-up to evaluate the incidence of multifactorial diseases of adulthood, with negative results to date (Tatsukawa et al. 2013). The distribution of parental doses in the F1 cohorts is very highly skewed: among 11,951 in the F1 Clinical Study cohort just mentioned, only 226 have mothers’ gonadal doses >1 Gy, and only 125 have fathers’ gonadal doses >1 Gy. Techniques for detecting mutations inherited from irradiation of parents’ gonads are currently being refined at the level of high-density arrays of probes for comparative genomic hybridization for planned studies of sets of related parents and children, which may be extended to DNA sequencing in the future. That radiation is a known mutagen would suggest that there must be some effect, however subtle or low in probability, but such an impact on the survivors’ children remains to be identified, let alone quantified.
RERF continues to conduct a wide variety of research aimed at elucidating the effects of the atomic bomb survivors’ radiation exposure. Some topical research interests include whether radiation increases the risk of diabetes or of conditions of the eye other than cataract, questions about the mechanisms of radiation-associated circulatory disease in the survivors, and other lines of research related to carcinogenesis, mutagenesis, and immunological effects. Interactions with other risk factors are a focus of research interest, as are the shapes of dose responses for major late effects in the low-dose range. Critical data are accumulating and being evaluated on the health experience of survivors who were exposed in utero or in childhood as they progress into old age.
A rather large fraction of survivors, perhaps one-fourth or more of proximal (<2 km) survivors, may have experienced early effects in the form of signs and symptoms of acute radiation injury. The fractions of survivors experiencing late effects appear smaller, with the number of estimated radiation-associated deaths to date being on the order of 1,000, or ∼3% of proximal survivors in the LSS, although projections suggest that number could double in the next couple of decades, and dying at a younger age due to radiation exposure has obviously grave implications. A full picture of the impact of cancer on the survivors must include the elevated risk of incidence as well as mortality. Furthermore, there are other late effects with a clear impact on health and quality of life, such as cataract. For survivors who were in utero at the times of the bombings, exposure to doses of a fraction of a gray or more during critical periods of gestation may have led to severe developmental consequences in a rather large proportion of those so exposed. In addition, survivors were subject to a psychosocial impact as well, although this was related to the general experience of being in the cities at the times of the bombings rather than to radiation dose per se.
The author is especially grateful to Don Pierce for valuable discussions and to Kyoji Furukawa for his kind provision of several unpublished figures from his work on risk projection. The Radiation Effects Research Foundation (RERF), Hiroshima and Nagasaki, Japan, is a private, nonprofit foundation funded by the Japanese Ministry of Health, Labour and Welfare (MHLW) and the U.S. Department of Energy (DOE), the latter in part through U.S. DOE Award DE-HS0000031 to the National Academy of Sciences. This publication was supported by RERF Research Protocols 18–59 and 1–75. The views of the author do not necessarily reflect those of the two governments.
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