Abstract
After ingestion or inhalation of radionuclides, internal organs of the human body will be exposed to ionising radiation. Current risk estimates of radiation-associated cancer from internal emitters are largely based on extrapolation of risk from high-dose externally exposed groups. Concerns have been expressed that extrapolated risk estimates from internal emitters are greatly underestimated, by factors of ten or more, thus implying a severe underestimation of the true risks. Therefore, data on cancer mortality and incidence in a number of groups who received exposure predominantly from internal emitters are examined and excess relative risks per Sv are compared with comparable (age at exposure, time since exposure, gender) matched subsets of the Japanese atomic bomb survivor cohort. Risks are examined separately for low LET and high LET internal emitters. There are eight studies informative for the effects of internal low LET radiation exposure and 12 studies informative for the effects of internal high LET radiation. For 11 of the 20 cancer endpoints (subgroups of particular study cohorts) examined in the low LET internal emitter studies, the best estimate of the excess relative risk is greater than the corresponding estimate in the Japanese atomic bomb survivors and for the other nine it is less. For four of these 20 studies, the relative risk is significantly (2-sided P < 0.05) different from that in the Japanese atomic bomb survivors, in three cases greater than the atomic bomb survivor relative risk and in one case less. Considering only those six low LET studies/endpoints with 100 or more deaths or cases, for four out of six studies/endpoints the internal emitter risk is greater than that in the Japanese atomic bomb survivors. For seven of the 24 cancer endpoints examined in the high LET internal emitter studies the best estimate of the ERR in the internal emitter study is greater than the corresponding estimate in the Japanese atomic bomb survivors and for the other 17 it is less. For six studies, the relative risk is significantly (2-sided P < 0.05) different from that in the Japanese atomic bomb survivors, in one case greater than the atomic bomb survivor relative risk and in five cases less. Considering only those eight high LET studies/endpoints with 100 or more deaths or cases, for five out of eight studies/endpoints the internal emitter risk is greater than that in the Japanese atomic bomb survivors. These results suggest that excess relative risks in the internal emitter studies do not appreciably differ from those in the Japanese atomic bomb survivors. However, there are substantial uncertainties in estimates of risks in the internal emitter studies, particularly in relation to lung cancer associated with radon daughter (alpha particle) exposure, so a measure of caution should be exercised in these conclusions.
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References
International Commission on Radiological Protection (ICRP) (1991) 1990 Recommendations of the International Commission on Radiological Protection. ICRP publication 60. Annals ICRP 21 (Pt 1-3), 1–201. Pergamon, Oxford
United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) (2000) Sources and effects of ionizing radiation. UNSCEAR 2000 Report to the General Assembly, with Scientific Annexes, vol II: effects. United Nations, New York
Krestinina LY, Preston DL, Ostroumova EV, Degteva MO, Ron E, Vyushkova OV, Startsev NV, Kossenko MM, Akleyev AV (2005) Protracted radiation exposure and cancer mortality in the Techa River cohort. Radiat Res 164:602–611
Omar RZ, Barber JA, Smith PG (1999) Cancer mortality and morbidity among plutonium workers at the Sellafield plant of British Nuclear Fuels. Br J Cancer 79:1288–1301
Committee Examining Radiation Risks from Internal Emitters (CERRIE) (2004) Final Report [downloaded 20 October 2004]. Available from URL: http://www.cerrie.org/report/
Committee on Medical Aspects of Radiation in the Environment (COMARE) (2004) Advice to government on the review of the radiation risks from radioactive internal emitters carried out and published by the Committee Examining Radiation Risks from Internal Emitters (CERRIE). National Radiological Protection Board, Chilton
European Committee on Radiation Risk (ECRR) (2003) 2003 Recommendations of the European Committee on Radiation Risk. The health effects of ionising radiation exposure at low doses and low dose rates for radiation protection purposes: regulators’ edition. Green Audit Press, Aberystwyth
Little MP (2001) Comparison of the risks of cancer incidence and mortality following radiation therapy for benign and malignant disease with the cancer risks observed in the Japanese A-bomb survivors. Int J Radiat Biol 77:431–464, 77:745–760
Little MP (2002) Comparisons of lung tumour mortality risk in the Japanese A-bomb survivors and in the Colorado Plateau uranium miners: support for the ICRP lung model. Int J Radiat Biol 78:145–163
Harrison JD, Muirhead CR (2003) Quantitative comparison of cancer induction in humans by internally deposited radionuclides and external radiation. Int J Radiat Biol 79:1–13
Preston DL, Kusumi S, Tomonaga M, Izumi S, Ron E, Kuramoto A, Kamada N, Dohy H, Matsuo T, Nonaka H, Thompson DE, Soda M, Mabuchi K (1994) Cancer incidence in atomic bomb survivors. Part III: leukemia, lymphoma and multiple myeloma, 1950–1987. Radiat Res 137:S68–S97, 139:129
Preston DL, Ron E, Tokuoka S, Funamoto S, Nishi N, Soda M, Mabuchi K, Kodama K (2007) Solid cancer incidence in atomic bomb survivors: 1958–1998. Radiat Res 168:1–64
Pierce DA, Shimizu Y, Preston DL, Vaeth M, Mabuchi K (1996) Studies of the mortality of atomic bomb survivors. Report 12, part I. Cancer: 1950-1990. Radiat Res 146:1–27
Preston DL, Shimizu Y, Pierce DA, Suyama A, Mabuchi K (2003) Studies of mortality of atomic bomb survivors. Report 13: solid cancer and noncancer disease mortality: 1950-1997. Radiat Res 160:381-407
Preston DL, Pierce DA, Shimizu Y, Cullings HM, Fujita S, Funamoto S, Kodama K (2004) Effect of recent changes in atomic bomb survivor dosimetry on cancer mortality risk estimates. Radiat Res 162:377–389
Little MP, Muirhead CR, Haylock RGE, Thomas JM (1999) Relative risks of radiation-associated cancer: comparison of second cancer in therapeutically irradiated populations with the Japanese atomic bomb survivors. Radiat Environ Biophys 38:267–283
Holm L-E, Hall P, Wiklund K, Lundell G, Berg G, Bjelkengren G, Cederquist E, Ericsson U-B, Hallquist A, Larsson L-G, Lidberg M, Lindberg S, Tennvall J, Wicklund H, Boice JD Jr (1991) Cancer risk after iodine-131 therapy for hyperthyroidism. J Natl Cancer Inst 83:1072–1077
Ron E, Doody MM, Becker DV, Brill AB, Curtis RE, Goldman MB, Harris BSH 3rd, Hoffman DA, McConahey WM, Maxon HR, Preston-Martin S, Warshauer ME, Wong FL, Boice JD Jr (1998) Cancer mortality following treatment for adult hyperthyroidism. J Am Med Assoc 280:347–355
Nekolla EA, Kellerer AM, Kuse-Isingschulte M, Eder E, Spiess H (1999) Malignancies in patients treated with high doses of radium-224. Radiat Res 152(Suppl 6):S3–S7
Nekolla EA, Kreisheimer M, Kellerer AM, Kuse-Isingschulte M, Gössner W, Spiess H (2000) Induction of malignant bone tumors in radium-224 patients: risk estimates based on the improved dosimetry. Radiat Res 153:93–103, 153:848
Wick RR, Nekolla EA, Gössner W, Kellerer AM (1999) Late effects in ankylosing spondylitis patients treated with 224Ra. Radiat Res 152(Suppl 6):S8–S11
Dickman PW, Holm LE, Lundell G, Boice JD Jr, Hall P (2003) Thyroid cancer risk after thyroid examination with I-131: a population-based cohort study in Sweden. Int J Cancer 106:580–587
Roesch WC (ed) (1987) US-Japan joint reassessment of atomic bomb radiation dosimetry in Hiroshima and Nagasaki, vol 1. Radiation Effects Research Foundation, Hiroshima
Young RW, Kerr GD (eds) (2005) Report of the Joint US–Japan Working Group. Reassessment of the atomic bomb radiation dosimetry for Hiroshima and Nagasaki. Radiation Effects Research Foundation, Hiroshima
McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman & Hall, London
Wong FL, Yamada M, Sasaki H, Kodama K, Akiba S, Shimaoka K, Hosoda Y (1993) Noncancer disease incidence in the atomic bomb survivors: 1958-1986. Radiat Res 135:418-430
United States National Research Council (2006) Committee to assess health risks from exposure to low levels of ionizing radiation. Health risks from exposure to low levels of ionizing radiation: BEIR VII-Phase 2. United States National Academy of Sciences. National Academy Press, Washington
United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) (1993) Sources and effects of ionizing radiation. UNSCEAR 1993 Report to the General Assembly, with Scientific Annexes. United Nations, New York
US National Academy of Sciences (1999) Committee on health risks of exposure to radon (BEIR VI). Health effects of exposure to radon. National Academy Press, Washington
Birchall A, James AC (1994) Uncertainty analysis of the effective dose per unit exposure from radon progeny and implications for ICRP risk-weighting factors. Radiat Prot Dosimetry 53:133–140
Wang Z, Lubin JH, Wang L, Zhang S, Boice JD Jr, Cui H, Zhang S, Conrath S, Xia Y, Shang B, Brenner A, Lei S, Metayer C, Cao J, Chen KW, Lei S, Kleinerman RA (2002) Residential radon and lung cancer risk in a high-exposure area of Gansu Province, China. Am J Epidemiol 155:554–564
Darby S, Hill D, Auvinen A, Barros-Dios JM, Baysson H, Bochicchio F, Deo H, Falk R, Forastiere F, Hakama M, Heid I, Kreienbrock L, Kreuzer M, Lagarde F, Mäkeläinen I, Muirhead C, Oberaigner W, Pershagen G, Ruano-Ravina A, Ruosteenoja E, Rosario AS, Tirmarche M, Tomášek L, Whitley E, Wichmann HE, Doll R (2005) Radon in homes and risk of lung cancer: collaborative analysis of individual data from 13 European case-control studies. Br Med J 330:223–226
Krewski D, Lubin JH, Zielinski JM, Alavanja M, Catalan VS, Field RW, Klotz JB, Letourneau EG, Lynch CF, Lyon JI, Sandler DP, Schoenberg JB, Steck DJ, Stolwijk JA, Weinberg C, Wilcox HB (2005) Residential radon and risk of lung cancer: a combined analysis of 7 North American case-control studies. Epidemiology 16:137–145
Strom DJ, Reif RH, Andrews DA, George AC, George JL, James AC, Jones CR, Langner GH Jr, Gavrilas-Guinn M, Neton JW, Rabovsky JL, Runkle GE, Carlosn DS, Dudney CS, Gammage RB, Maisler JA, Rose S, Wilson DL (1996) Occupational exposure to radon and thoron. US Department of Energy Radiological Control Coordinating Committee. Radon Subcommittee. PNNL Report 14108
van Kaick G, Dalheimer A, Hornik S, Kaul A, Liebermann D, Luhrs H, Spiethoff A, Wegener K, Wesch H (1999) The German Thorotrast study: recent results and assessment of risks. Radiat Res 152(Suppl 6):S64–S71
Mori T, Fukutomi K, Kato Y, Hatakeyama S, Machinami R, Tanooka H, Ishikawa Y, Kumatori T (1999) 1998 results of the First series of follow-up studies on Japanese Thorotrast patients and their relationships to an autopsy series. Radiat Res 152(Suppl 6):S72–S80
dos Santos Silva I, Malveiro F, Jones ME, Swerdlow AJ (2003) Mortality after radiological investigation with radioactive Thorotrast: a follow-up study of up to fifty years in Portugal. Radiat Res 159:521–534
Travis LB, Hauptmann M, Gaul LK, Storm HH, Goldman MB, Nyberg U, Berger E, Janower ML, Hall P, Monson RR, Holm L-E, Land CE, Schottenfeld D, Boice JD Jr, Andersson M (2003) Site-specific cancer incidence and mortality after cerebral angiography with radioactive Thorotrast. Radiat Res 160:691–706
Boice JD Jr (2001) Radiation and breast carcinogenesis. Med Pediatr Oncol 36:508–513
Preston DL, Lubin JH, Pierce DA, McConney ME (1998) Epicure Release 2.10. HiroSoft International, Seattle
Schervish MJ (1995) Theory of statistics. Springer, New York
Bauer S, Gusev BI, Pivina LM, Apsalikov KN, Grosche B (2005) Radiation exposure due to local fallout from Soviet atmospheric nuclear weapons testing in Kazakhstan: solid cancer mortality in the Semipalatinsk historical cohort, 1960–1999. Radiat Res 164:409–419
Cardis E, Kesminiene A, Ivanov V, Malakhova I, Shibata Y, Khrouch V, Drozdovitch V, Maceika E, Zvonova I, Vlassov O, Bouville A, Goulko G, Hoshi M, Abrosimov A, Anoshko J, Astakhova L, Chekin S, Demidchik E, Galanti R, Ito M, Korobova E, Lushnikov E, Maksioutov M, Masyakin V, Nerovnia A, Parshin V, Parshkov E, Piliptsevich N, Pinchera A, Polyakov S, Shabeka N, Suonio E, Tenet V, Tsyb A, Yamashita S, Williams D (2005) Risk of thyroid cancer after exposure to 131I in childhood. J Natl Cancer Inst 97:724–732
Davis S, Day RW, Kopecky KJ, Mahoney MC, McCarthy PL, Michalek AM, Moysich KB, Onstad LE, Stepanenko VF, Voillequé PG, Chegerova T, Falkner K, Kulikov S, Maslova E, Ostapenko V, Rivkind N, Shevchuk V, Tsyb AF (2006) Childhood leukaemia in Belarus, Russia, and Ukraine following the Chernobyl power station accident: results from an international collaborative population-based case-control study. Int J Epidemiol 35:386–396
Ostroumova E, Gagniere B, Laurier D, Gudkova N, Krestinina L, Verger P, Hubert P, Bard D, Akleyev A, Tirmarche M, Kossenko M (2006) Risk analysis of leukaemia incidence among people living along the Techa River: a nested case-control study. J Radiol Prot 26:17–32
Gilbert ES, Koshurnikova NA, Sokolnikov ME, Shilnikova NS, Preston DL, Ron E, Okatenko PV, Khokhryakov VF, Vasilenko EK, Miller S, Eckerman K, Romanov SA (2004) Lung cancer in Mayak workers. Radiat Res 162:505–516
United States National Research Council. Committee on the Biological Effects of Ionizing Radiations (BEIR V) (1990) Health effects of exposure to low levels of ionizing radiation. National Academy of Sciences. National Academy Press, Washington
Davis S, Kopecky KJ, Hamilton TE, Onstad L (2004) Thyroid neoplasia, autoimmune thyroiditis, and hypothyroidism in persons exposed to iodine 131 from the Hanford nuclear site. J Am Med Assoc 292:2600–2613
Greenland S, Robins J (1994) Invited commentary: ecologic studies—biases, misconceptions, and counterexamples. Am J Epidemiol 139:747–760
United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) (1994) Sources and effects of ionizing radiation. UNSCEAR 1994 Report to the General Assembly, with Scientific Annexes. United Nations, New York
Little MP, Boice JD Jr (1999) Comparison of breast cancer incidence in the Massachusetts tuberculosis fluoroscopy cohort and in the Japanese atomic bomb survivors. Radiat Res 151:218–224
Preston DL, Mattsson A, Holmberg E, Shore R, Hildreth NG, Boice JD Jr (2002) Radiation effects on breast cancer risk: a pooled analysis of eight cohorts. Radiat Res 158:220–235, 666
Muirhead CR, Darby SC (1987) Modelling the relative and absolute risks of radiation-induced cancers. J Royal Stat Soc A 150:83–118
Little MP, Muirhead CR, Charles MW (1999) Describing time and age variations in the risk of radiation-induced solid tumour incidence in the Japanese atomic bomb survivors using generalized relative and absolute risk models. Statist Med 18:17–33
Wakeford R (2005) Alpha-emitters in the workplace. In: Oeh U, Roth P, Paretzke HG (eds) Proceedings of the 9th international conference on health effects of incorporated radionuclides. Emphasis on radium, thorium, uranium and their daughter products (GSF-National Research Center for Environment and Health, Neuherberg, Germany, Nov 29–Dec 1 2004) (HEIR 2004). Institut für Strahlenschutz, GSF, Neuherberg, Germany, pp 117–127
Breslow NE, Day NE (1987) Statistical methods in cancer research, vol 2: the design and analysis of cohort studies. Scientific publication No 82, International Agency for Research on Cancer, Lyon
Acknowledgments
The authors are grateful for the detailed and helpful comments of the two referees. This report makes use of data obtained from the Radiation Effects Research Foundation (RERF) in Hiroshima and Nagasaki, Japan. RERF is a private, non-profit foundation funded by the Japanese Ministry of Health, Labour and Welfare (MHLW) and the U.S. Department of Energy (DOE), the latter through the National Academy of Sciences. The data include information obtained from the Hiroshima City, Hiroshima Prefecture, Nagasaki City and Nagasaki Prefecture Tumour Registries and the Hiroshima and Nagasaki Tissue Registries. The conclusions in this report are those of the authors and do not necessarily reflect the scientific judgment of RERF or its funding agencies. The work was funded in part by the UK Department of Health and by the European Commission under contract FI6R-CT-2003-508842 (RISC-RAD).
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Little, M.P., Hall, P. & Charles, M.W. Are cancer risks associated with exposures to ionising radiation from internal emitters greater than those in the Japanese A-bomb survivors?. Radiat Environ Biophys 46, 299–310 (2007). https://doi.org/10.1007/s00411-007-0122-3
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DOI: https://doi.org/10.1007/s00411-007-0122-3