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Radiation Research 160(4):381-407. 2003
doi: 10.1667/RR3049

Studies of Mortality of Atomic Bomb Survivors. Report 13: Solid Cancer and Noncancer Disease Mortality: 1950–1997

Dale L. Preston1a, Yukiko Shimizub, Donald A. Piercea, Akihiko Suyamac, and Kiyohiko Mabuchid

aDepartment of Statistics, Radiation Effects Research Foundation, Hiroshima, Japan

bDepartment of Epidemiology, Radiation Effects Research Foundation, Hiroshima, Japan

cDepartment of Epidemiology, Radiation Effects Research Foundation, Nagasaki, Japan

dRadiation Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland

1Address for correspondence: Department of Statistics, Radiation Effects Research Foundation, 5-2 Hijiyama Koen, Minami-ku, Hiroshima, 732-0815, Japan;

Abstract

Preston, D. L., Shimizu, Y., Pierce, D. A., Suyama, A. and Mabuchi, K. Studies of Mortality of Atomic Bomb Survivors. Report 13: Solid Cancer and Noncancer Disease Mortality: 1950–1997. Radiat. Res. 160, 381–407 (2003).

This continues the series of general reports on mortality in the cohort of atomic bomb survivors followed up by the Radiation Effects Research Foundation. This cohort includes 86,572 people with individual dose estimates, 60% of whom have doses of at least 5 mSv. We consider mortality for solid cancer and for noncancer diseases with 7 additional years of follow-up. There have been 9,335 deaths from solid cancer and 31,881 deaths from noncancer diseases during the 47-year follow-up. Of these, 19% of the solid cancer and 15% of the noncancer deaths occurred during the latest 7 years. We estimate that about 440 (5%) of the solid cancer deaths and 250 (0.8%) of the noncancer deaths were associated with the radiation exposure. The excess solid cancer risks appear to be linear in dose even for doses in the 0 to 150-mSv range. While excess rates for radiation-related cancers increase throughout the study period, a new finding is that relative risks decline with increasing attained age, as well as being highest for those exposed as children as noted previously. A useful representative value is that for those exposed at age 30 the solid cancer risk is elevated by 47% per sievert at age 70. There is no significant city difference in either the relative or absolute excess solid cancer risk. Site-specific analyses highlight the difficulties, and need for caution, in distinguishing between site-specific relative risks. These analyses also provide insight into the difficulties in interpretation and generalization of LSS estimates of age-at-exposure effects. The evidence for radiation effects on noncancer mortality remains strong, with risks elevated by about 14% per sievert during the last 30 years of follow-up. Statistically significant increases are seen for heart disease, stroke, digestive diseases, and respiratory diseases. The noncancer data are consistent with some non-linearity in the dose response owing to the substantial uncertainties in the data. There is no direct evidence of radiation effects for doses less than about 0.5 Sv. While there are no statistically significant variations in noncancer relative risks with age, age at exposure, or sex, the estimated effects are comparable to those seen for cancer. Lifetime risk summaries are used to examine uncertainties of the LSS noncancer disease findings.

Received: December 12, 2002; Accepted: May 6, 2003



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APPENDIX: SUMMARY ESTIMATES OF SOLID CANCER SITE-SPECIFIC RISKS


The following tables provide site-specific summary risk estimates based on organ-specific survivor dose estimates. These estimates are based on age-constant ERR models with site-specific age-at-exposure effects for major sites where these can be reasonably estimated, and the reported ERR is for age at exposure 30. For minor sites, this effect is set to zero. The summary EAR estimate is the ratio of the estimated number of excess deaths to the total PY-Sv. The cohort attributable risk is the estimated number of excess deaths divided by the number of deaths among those whose estimated dose is at least 5 mSv.

FIG. 1. Excess cancer rates by calendar periods and age-at-exposure categories: absolute and relative to background rates

FIG. 2. Solid cancer dose–response function averaged over sex for attained age 70 after exposure at age 30. The solid straight line is the linear slope estimate, the points are dose category-specific ERR estimates, the dashed curve is a smoothed estimate derived from the points. The dotted curves indicate upper and lower one-standard-error bounds on the smoothed estimate

FIG. 3. Primary descriptions of the excess risks of solid cancer. The left panel presents fitted sex-averaged ERR estimates using both attained-age-declining (dark solid line) and attained-age-constant (dashed lines) forms, for age-at-exposure groups 0–9, 10–19, 20–39 and 40. ERR estimates for women are about 25% greater and ERR estimates for men are 25% lower than the values shown. The right panel presents fitted EAR estimates for the same dose groups. There is no evidence of significant sex differences in the fitted EAR. The details of these models are given in Section 3.3

FIG. 4. Estimates of the site-specific solid cancer ERR with 90% confidence intervals and one-sided P values for testing the hypothesis of no dose response. Except for sex-specific cancers (breast, ovary, uterus and prostate), the estimates are averaged over sex. All estimates and P values are based on a model in which the age-at-exposure and attained-age effects were fixed at the estimates for all solid cancers as a group. The light dotted vertical line at 0 corresponds to no excess risk, while the dark solid vertical line indicates the sex-averaged risk for all solid cancers.

FIG. 5. Age–time patterns for the solid cancer ERR and EAR for age-at-exposure groups 0–9, 10–19, 20–39 and 40 or more. The curves are power functions of attained age fitted separately for each age-at-exposure category. The points are estimated values for decades of attained age within each age at exposure group.

FIG. 6. Estimates of LSS lifetime solid cancer mortality risk and years of life lost per excess death, by age at exposure and sex and for a 100-mSv exposure. Estimates are based on age-declining (dark solid lines) and age-constant (light dashed lines) ERR models and an EAR model (dark dashed lines). The parameter estimates for these models are given in Tables 5 and 6 and the estimated excess risks were plotted in Fig. 3

FIG. 7. Site-specific age–time patterns in the radiation-associated risks for stomach, colon and liver cancer. The dark curves are fitted age–time patterns in the ERR (left side) and EAR (right side). The light dashed curves are the patterns obtained when the age and age-at-exposure effects are constrained to equal that for all other solid cancers. The curves are sex-averaged estimates of the risk at 1 Sv for people exposed at age 10, 30 and 50 with attained ages corresponding to the follow-up period

FIG. 8. Site-specific age–time patterns in the radiation-associated risks for lung, breast and all solid cancers other than stomach, colon, liver, lung and breast. The dark curves are fitted age–time patterns in the ERR (left side) and EAR (right side). The light dashed curves are the patterns obtained when the age and age-at-exposure effects are constrained to equal that for all other solid cancers. The curves are sex-averaged estimates of the risk at 1 Sv for people exposed at age 10, 30 and 50 with attained ages corresponding to the follow-up period

FIG. 9. Comparison of fitted noncancer mortality dose–response curves for early (1950–1967) and late (1968–1997) portions of the follow-up period. The solid curves are fits made using only proximal survivor data. The dashed curves are based on the data for the full cohort with no allowance for selection effects

FIG. 10. Noncancer dose–response function for the period 1968–1997. The solid straight line indicates the fitted linear ERR model without any effect modification by age at exposure, sex or attained age. The points are dose category-specific ERR estimates, the solid curve is a smoothed estimate derived from the points, and the dashed lines indicate upper and lower one-standard-error bounds on the smoothed estimate. The right panel shows the low-dose portion of the dose–response function in more detail

FIG. 11. Fitted noncancer ERR and EAR models. The ERR models shown in the left panel include a constant ERR model (solid line) and alternatives in which the ERR varies with either attained age (light dashed curve) or age at exposure (dashed-dotted lines). As described in the text, neither the attained age nor age-at-exposure effects significantly improve the fit. The EAR models (right panel) include a basic description in which the EAR increases in proportion to age power (dark curve) and a model in which the EAR is also allowed to depend on age at exposure (dash-dotted curves)

FIG. 12. Estimates of LSS noncancer disease lifetime risk and years of life lost per excess death by age at exposure and sex, and for a 1-Sv exposure. Estimates are based on constant ERR (dark solid lines) and age-at-exposure and sex-dependent (light dashed lines) ERR models and an EAR model (dark dashed-dotted lines). The parameter estimates for these models are described in the text and the estimated excess risks were plotted in Fig. 11

FIG. 13. Cause-specific dose–response functions for noncancer deaths. The plots display the best-fitting linear ERR models together with nonparametric ERR estimates for 20 dose categories

FIG. 14. Total and radiation-associated deaths per year for all causes and for cancers including leukemia. The solid lines show the data for the 1950 through 1997 follow-up period while the dashed lines are projections based on the primary ERR models discussed in this paper. The solid cancer model includes both age-at-exposure and attained-age effects while the linear constant relative risk model was used for noncancer. Background rates were projected assuming the birth cohort effects seen in the cohort to date will continue into the future. Assuming no future changes in background rates has little impact on the nature of the plot

table

TABLE 1 LSS Vital Status and Cause of Death Summary by Age at Exposure as of January 1, 1998

table

TABLE 2 Observed and Expected Solid Cancer Deaths 1950–1997 by Dose Group

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TABLE 3 Cancer Deaths and Excess Rates by Calendar Period and Age at Exposure

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TABLE 4 Excess Relative Risk Estimates for Selected Dose Ranges

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TABLE 5 Solid Cancer Excess Relative Risk Model Parameter Estimates

table

TABLE 6 Solid Cancer Excess Absolute Rate Model Parameter Estimates

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TABLE 7 Estimated Lifetime Risk of Radiation-Associated Solid Cancer Deaths in the LSS after Exposure to 0.1 Sv

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TABLE 8 Comparison of Baseline Rate Birth Cohort Effect and Age-at-Exposure Effects on the Solid Cancer ERR and EAR

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TABLE 9 Sex Ratios in Radiation Risk and Background Rates

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TABLE 10 Observed and Expected Noncancera Deaths 1950–1997

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TABLE 11 Noncancer Dose–Response Parameter Estimates for the Period of 1968–1997

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TABLE 12 Noncancer Dose–Response Parameter Estimates for the Period of 1950–1967

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TABLE 13 Life-Span Study Cause-Specific Noncancer Disease ERR Estimates 1968–1997

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TABLE A1 LSS Male Site-Specific Summary Mortality Risk Estimates: Solid Cancers 1950–1997

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TABLE A2 LSS Female Site-Specific Summary Mortality Risk Estimates: Solid Cancers 1950–1997

Formerly Department of Epidemiology, Radiation Effects Research Foundation, Hiroshima, Japan.

Cited by

Peter

Morfeld,

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Harry M. Cullings a, Shoichiro Fujita a, Sachiyo Funamoto a, Eric J. Grant b, George D. Kerr c, and Dale L. Preston d. (2006) Dose Estimation for Atomic Bomb Survivor Studies: Its Evolution and Present Status. Radiation Research 166:1, 219-254
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L. Yu Krestinina a, D. L. Preston b, E. V. Ostroumova a, M. O. Degteva a, E. Ron c, O. V. Vyushkova a, N. V. Startsev a, M. M. Kossenko a, and A. V. Akleyev a. (2005) Protracted Radiation Exposure and Cancer Mortality in the Techa River Cohort. Radiation Research 164:5, 602-611
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M. M. Kossenko a, T. L. Thomas b, A. V. Akleyev a, L. Yu Krestinina a, N. V. Startsev a, O. V. Vyushkova a, C. M. Zhidkova a, D. A. Hoffman c, D. L. Preston d, F. Davis e, and E. Ron b. (2005) The Techa River Cohort: Study Design and Follow-up Methods. Radiation Research 164:5, 591-601
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Marco Durante . (2005) Biomarkers of Space Radiation Risk. Radiation Research 164:4, 467-473
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Dale L. Preston b, Donald A. Pierce c, Yukiko Shimizu c. (2005) Response to Letter on Curvature in the Dose Response of the Life Span Study Cancer Mortality Data by Linda Walsh et al. Radiation Research 163:4, 478-478
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Paul McGale and Sarah C. Darby . (2005) Low Doses of Ionizing Radiation and Circulatory Diseases: A Systematic Review of the Published Epidemiological Evidence. Radiation Research 163:3, 247-257
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Nori Nakamura . (2005) A Hypothesis: Radiation-Related Leukemia is Mainly Attributable to the Small Number of People who Carry Pre-existing Clonally Expanded Preleukemic Cells. Radiation Research 163:3, 258-265
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S. J. Ko a, X-Y. Liao a, S. Molloi b, E. Elmore a, and J. L. Redpath a. (2004) Neoplastic Transformation In Vitro after Exposure to Low Doses of Mammographic-Energy X Rays: Quantitative and Mechanistic Aspects. Radiation Research 162:6, 646-654
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Geoffrey R. Howe a, Lydia B. Zablotska a, Jack J. Fix b, John Egel c, and Jeff Buchanan b. (2004) Analysis of the Mortality Experience amongst U.S. Nuclear Power Industry Workers after Chronic Low-Dose Exposure to Ionizing Radiation. Radiation Research 162:5, 517-526
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E. S. Gilbert a, N. A. Koshurnikova b, M. E. Sokolnikov b, N. S. Shilnikova b, D. L. Preston c, E. Ron a, P. V. Okatenko b, V. F. Khokhryakov b, E. K. Vasilenko d, S. Miller e, K. Eckerman f, and S. A. Romanov b. (2004) Lung Cancer in Mayak Workers. Radiation Research 162:5, 505-516
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Mieko Kodaira a, Shizue Izumi b, Norio Takahashi a, and Nori Nakamura a. (2004) No Evidence of Radiation Effect on Mutation Rates at Hypervariable Minisatellite Loci in the Germ Cells of Atomic Bomb Survivors. Radiation Research 162:4, 350-356
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Dale L. Preston a, Donald A. Pierce a, Yukiko Shimizu b, Harry M. Cullings a, Shoichiro Fujita a, Sachiyo Funamoto a, and Kazunori Kodama b. (2004) Effect of Recent Changes in Atomic Bomb Survivor Dosimetry on Cancer Mortality Risk Estimates. Radiation Research 162:4, 377-389
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R

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Colin R. Muirhead . (2004) Radiation and Noncancer Diseases. Radiation Research 161:6, 748-748
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Lydia B. Zablotska a, J. Patrick Ashmore b, Geoffrey R. Howe a. (2004) Analysis of Mortality among Canadian Nuclear Power Industry Workers after Chronic Low-Dose Exposure to Ionizing Radiation. Radiation Research 161:6, 633-641
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Donald A. Pierce . (2003) Mechanistic Models for Radiation Carcinogenesis and the Atomic Bomb Survivor Data. Radiation Research 160:6, 718-723
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David J.

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