Hormesis as a Confounding Factor in Epidemiological Studies of Radiation Carcinogenesis

  • Sanders Charles L. (Department of Nuclear & Quantum Engineering, Korea Advanced Institute of Science and Technology)
  • Published : 2006.06.30


Biological mechanisms for ionizing radiation effects are different at low doses than at high doses. Radiation hormesis involves low-dose-induced protection and high-dose-induced harm. The protective component is associated with a reduction in the incidence of cancer below the spontaneous frequency, brought about by activation of defensive and repair processes. The Linear No-Threshold (LNT) hypothesis advocated by the International Commission on Radiological Protection (ICRP) and the Biological Effects of ionizing Radiation (BEIR) Report VII for cancer risk estimations Ignores hormesis and the presence of a threshold. Cancer incidences significantly less than expected have been found in a large number of epidemiological studies including, airline flight personnel, inhabitants of high radiation backgrounds, shipyard workers, nuclear site workers in scores of locations throughout the world, nuclear power utility workers, plutonium workers, military nuclear test site Participants, Japanese A-bomb survivors, residents contaminated by major nuclear accidents, residents of Taiwan living in $^{60}Co$ contaminated buildings, fluoroscopy and mammography patients, radium dial painters, and those exposed to indoor radon. Significantly increased cancer was not found at doses <200 $mSv^*$. Evidence for radiation hormesis was seen in both sexes for acute or chronic exposures, low or high LET radiations, external whole- or partial body exposures, and for internal radionuclides. The ubiquitous nature of the Healthy Worker Effect (HWE)-like responses in cellular, animal and epidemiological studies negates the HWE as an explanation for radiation hormesis. The LNT hypothesis is wrong and does not represent the true nature of the dose-response relationship, since low doses or dose-rates commonly result in thresholds and reduce cancer incidences below the spontaneous rate. Radiation protection organizations should seriously consider the cost and health implications of radiation hormesis.


  1. Calabrese EJ, Baldwin LA. Radiation hormesis: Its historical foundations as a biological hypothesis. Hum. Exper. Toxicol. 2000;19:41-75 https://doi.org/10.1191/096032700678815602
  2. Calabrese EJ, Baldwin LA. Hormesis: The Dose-response revolution. Annu. Rev. Pharmacol. Toxicol. 2003;43:175-197 https://doi.org/10.1146/annurev.pharmtox.43.100901.140223
  3. Luckey TD. Physiological benefits from low-level ionizing radiation. Health Phys. 1982;43:771-789 https://doi.org/10.1097/00004032-198212000-00001
  4. Luckey TD. Nurture with ionizing radiation: A Provocative hypothesis. Nutrition and Cancer 1999;34:1-11 https://doi.org/10.1207/S15327914NC340101
  5. Kant K, Chauhan RP, Sharma GS, et al. Hormesis in humans exposed to low-level ionizing radiation. Intern. J. Low Radiat. 2003;1:76-87 https://doi.org/10.1504/IJLR.2003.003483
  6. Frigerio NA, Eckerman KF, Stowe RS. Carcinogenic hazard from low-level, low-rate radiation, Part I, rep. Argonne, IL: Argonne Natl. Lab., 1973: ANL/ES-26
  7. Jaworowski Z. Stimulating effects of ionizing radiation: New issues for regulatory policy. Regulatory Toxicology and Pharmacology 1995;22:172-179 https://doi.org/10.1006/rtph.1995.1082
  8. Rockwell T. Bad science in service of a bad hypothesis. Health Physics News 34:9-10
  9. Lewis E. Leukemia and ionizing radiation. Science 1957;43:965
  10. ICRP Draft Report of Committee I/Task Group. Low Dose Extrapolation of Radiation Related Cancer Risk, Dec, 2004
  11. NCRP (National Council on Radiation Protection and Measurements). Evaluation of the linear-nonthreshold dose-response model for ionizing radiation. NCRP Report No. 136, Bethesda, MD, 2001
  12. Mortazavi SMJ, Ikushima T. Open Questions Regarding Implications of Radioadaptive Response in the Estimation of the Risks of Low-Level Exposures in Nuclear Workers. Intern. J. Low Radiation 2006;2:88-96 https://doi.org/10.1504/IJLR.2006.007899
  13. Craig L, Seidman H. Leukemia and lymphoma mortality in relation to cosmic radiation, Blood, 1961:17, 319
  14. Ankathil R, Nair RK, Padmavathi J, et. al. Review of studies in high level natural radiation areas in India. Proceedings of the Forty-Eighth Annual Meeting of the Japan Radiation Research Society/ the First Asian Congress of Radiation Research, Research Institute for Radiation Biology and Medicine, Hiroshima University, Japan, 2005;Abstract S4-1-1:79
  15. Ghiassi-Nejad M, Mortazavi M. Radiation Adaptive Response Observed in Residents in High Level Natural Area of Ramsar. Proceedings of the Forty-Eighth Annual Meeting of the Japan Radiation Research Society/ the First Asian Congress of Radiation Research, Research Institute for Radiation Biology and Medicine, Hiroshima University, Japan, 2005;Abstract S4-2-2:81
  16. Blettner M, Zeeb H, Auviven A, et al. Mortality from cancer and other causes among male airline cockpit crew in Europe. Intern. J. Cancer 2003;106:946-952 https://doi.org/10.1002/ijc.11328
  17. Zeeb H, Blettner M, Langner MI, et al. Mortality from cancer and other causes among airline cabin attendants in Europe: A collaborative study in eight countries. Amer. J. Epidemiol. 2003;158:35-46 https://doi.org/10.1093/aje/kwg107
  18. Wing S, Richardson D. Age at exposure to ionizing radiation and cancer mortality among Hanford workers: Follow-up through 1994. Occup. Environ. Med. 2005;62:465-472 https://doi.org/10.1136/oem.2005.019760
  19. Frome EL, Cragle DL, Watkins JP, et al. A mortality study of employees of the nuclear industry in Oak Ridge, Tennessee. Radiat. Res. 1997;148:64-80 https://doi.org/10.2307/3579540
  20. Iwasaki T, Murata M, Ohshima S, et al. Second analysis of nuclear industry workers in Japan, 1986-1997. Radiat. Res. 2003;159:228-238 https://doi.org/10.1667/0033-7587(2003)159[0228:SAOMON]2.0.CO;2
  21. Beral V, Fraser P, Both M, et al. Epidemiological studies of workers in the nuclear industry. In: Jones, R.R. and R. Southwood (editors), Radiation & Health, Wiley, N.Y., 1987:97-106
  22. Carpenter LM, Beral V, Smith PG. Cancer mortality in relation to monitoring for radionuclide exposure in three UK nuclear industry workforces. British Journal of Cancer, 1998;78:1224-1232 https://doi.org/10.1038/bjc.1998.659
  23. Cardis E, Vrijheid M, Blettner M, et al. Risk of cancer after low doses of ionizing radiation: Retrospective cohort study in 15 countries. Brit. Med. J. 2005;331:77-80 https://doi.org/10.1136/bmj.38499.599861.E0
  24. Ahn Y, Bae J. A Chronic Exposure of Low-dose Radiation and Cancer Risks among Nuclear Power Plant Workers in Korea. Proceedings of the Forty-Eighth Annual Meeting of the Japan Radiation Research Society/ the First Asian Congress of Radiation Research, Research Institute for Radiation Biology and Medicine, Hiroshima University, Japan, Abstract Sl1-2, 2005:89
  25. Krestinina LYu, Preston DL, Ostroumova EV, et al. Protracted radiation exposure and cancer mortality in the Techa River cohort. Radiat. Res. 2005;164:602-611 https://doi.org/10.1667/RR3452.1
  26. Ivanov V, Iiyin L, Gorski A, et al. Radiation and epidemiological analysis for solid cancer incidence among nuclear workers who participated in recovery operations following the accident at the Chernobyl NPP. J. Radiat. Res. (Tokyo) 2004;45:41-44 https://doi.org/10.1269/jrr.45.41
  27. Zhumadilov K, Ivannikov A, Apsalikov K, et al. Dose Reconstruction by Tooth Enamel EPR Dosimetry for Residents of Settlements Placed in Vicinity of the Radioactive Fallout Trace of the First Test in SNTS. Proceedings of the Forty-Eighth Annual Meeting of the Japan Radiation Research Society/ the First Asian Congress of Radiation Research, Research Institute for Radiation Biology and Medicine, Hiroshima University, Japan, Abstract W-2-3, 2005:103
  28. Stewart AM. Healthy worker and healthy survivor effects in relation to the cancer risks of radiation workers. Amer. J. Ind. Med. 1990;17:151-154 https://doi.org/10.1002/ajim.4700170201
  29. Mine M, Okumura M, Ichimara S, et al. Apparently beneficial effect of low to intermediate doses of A -bomb radiation on human lifespan. Int. J. Rad. Biol. 1990;58:1035-1043 https://doi.org/10.1080/09553009014552341
  30. Sont WN, Zielinski JM, Ashmore JP, et al. First analysis of cancer incidence and occupational radiation exposure based on the National Dose Registry of Canada. Amer. J. Epidemiol. 2001;153:309-318 https://doi.org/10.1093/aje/153.4.309
  31. Tokarskaya ZB, Okladnikova ND, Belyaeva ZD, et al. The Influence of Radiation and Nonradiation Factors on the Lung Cancer Incidence among the Workers of the Nuclear Enterprise 'Mayak'. Health Physics 1995;69:356-366 https://doi.org/10.1097/00004032-199509000-00007
  32. Shilnikova, N.S., D.L. Preston, E. Ron,et al. 2003. Cancer mortality risk among workers at the Mayak nuclear complex. Radiat. Res. 159:787-798 https://doi.org/10.1667/0033-7587(2003)159[0787:CMRAWA]2.0.CO;2
  33. Voelz GL, Lawrence JNP and Johnson ER. Fifty Years of Plutonium Exposure to the Manhattan Project Plutonium Workers: An Update. Health Physics 1997;73:611-619 https://doi.org/10.1097/00004032-199710000-00004
  34. Kauffman JM. Radiation hormesis: Demonstrated, deconstructed, denied, dismissed, and some implications for public policy. J. Scientific Exploration 2003;17:389-407
  35. Lubin, JH, Wang ZY, Boice JD, et al. Risk of lung cancer and residential radon in China: Pooled results of two studies. Intern. J. Cancer 2004;109:132-137 https://doi.org/10.1002/ijc.11683
  36. Morlier JP, Morin M, Chameaud J, et al. Importance of exposure rate on tumour induction in rats after radon exposure. C. R. Acad. Sci. Paris Serie III 1992;315:463-466
  37. Lubin JH, Boice JD, Hornung RW, et al. Radon and lung cancer risk: a joint analysis of 11 underground studies. NIH Publication No. 94-3644, 1994
  38. Krewski D, Rai SN, Zielinski JM, et al. Characterization of uncertainty and variability in residential radon cancer risks. Ann. N.Y. Acad. Sci. 1999;895:245-272 https://doi.org/10.1111/j.1749-6632.1999.tb08090.x
  39. Kaletsch U, Kaatsch P, Meinert R, et a1. Childhood cancer and residential radon exposureresults of a population-based case-control study in Lower (Germany). Radiat. Environ. Biophys. 1999;38:211-215 https://doi.org/10.1007/s004110050158
  40. Keirim-Markus IB. New Recommendations on the Radiation Safety in 60 and 61 ICRP Publications. Editsinskaya Radiologiya 1993N 6:35-41
  41. Haynes RM. The distribution of domestic radon concentrations and lung cancer mortality in England and Wales. Rad. Prot. Dosim. 1988;25:93-96 https://doi.org/10.1093/oxfordjournals.rpd.a080357
  42. Baverstock KF, Papworth D. The UK radium luminizer survey. In: Tayler, D.M., C.W. Mays, G.B. Gerber et al (eds), Risks from Radium and Thorotrast, British Institute of Radiology, 1989:72-76
  43. Spousler R, Cameron JR. Nuclear shipyard worker study (1980-1988): A large cohort exposed to low-dose-rate gamma radiation. Int. J. Low Radiation 2005;1:463-478 https://doi.org/10.1504/IJLR.2005.007915
  44. Thomas RH. LNT once Again. Health Physics News, December, 2005:7
  45. Berrington A, Darby SC, Weiss HA, et al. 100 years of observation on British radiologists: Mortality from cancer and other causes 1987-1997. Brit. J. Radiol. 2001;74:507-519 https://doi.org/10.1259/bjr.74.882.740507
  46. Tatsumi K, Ohshima S, Kudo S, et al. Analysis of Cancer Mortality of Nuclear Industry Workers in Japan. Proceedings of the Forty-Eighth Annual Meeting of the Japan Radiation Research Society/ the First Asian Congress of Radiation Research, Research Institute for Radiation Biology and Medicine, Hiroshima University, Japan, Abstract S11-l, 2005:89
  47. Bol'shov LA, Gabaraev BA, It'in LA, et al. Comparison of accident risks in different energy systems: Comments from Russian specialists. 2000: IAEA Bulletin 42/4/2000
  48. Sandler DP, Comstock GW, Matanoski GM. Neoplasms following childhood radium irradiation of the nasopharynx. J. Natl. Cancer Inst. 1982;68:3-8
  49. Howe GR, Nair RC, Newcombe HB, et al. Lung cancer mortality (1950-1980) in relation to radon daughter exposure in a cohort of workers at the Eldorado Port Radium uranium mine : possible modification of risk by exposure rate. J. Natl. Cancer Inst. 1987;79:1255-1260
  50. Gilbert ES, Petersen GR, Buchanan J. Mortality of workers at the Hanford site: 1945-1981. Health Physics 1989;56:11-25 https://doi.org/10.1097/00004032-198901000-00001
  51. Little MP, Muirhead CR. Derivation of low dose extrapolation factors from analysis of the curvature in the cancer incidence dose response in Japanese atomic bomb survivors. Intern. J. Radiat. Biol. 2000;76:939-953 https://doi.org/10.1080/09553000050050954
  52. Jacob V, Jacob P, Meckbach R, et al. Lung cancer in Mayak workers: Interaction of smoking and plutonium exposure. Radiat. Environ. Biophys. 2005:44:119-129 https://doi.org/10.1007/s00411-005-0012-5
  53. Friedman GD, Collen MF, Fireman BH. Multiphasic health checkup evaluation: A 16-year follow-up. J. Chronic Dis. 1986;39:453-463 https://doi.org/10.1016/0021-9681(86)90112-8
  54. Calabrese EJ, Baldwin LA. Scientific foundations of hormesis. Crit. Rev. Toxicol. 2001:31:351-624 https://doi.org/10.1080/20014091111721
  55. Baverstock K, Williams D. Chernobyl: An overlooked aspect- Letters, Science 2002;299:44
  56. Kumatori T, Ishihara T, Hirshima K, et al. Follow-up studies over a 25-year period on the Japanese fishermen exposed to radioactive fallout in 1954. In: Hubner, K.F. and A.A. Fry (eds), The Medical Basis for Radiation Preparedness, Elsevier, NY, 1980: 33-54
  57. Nystrom L, Andersson I, Bjurstam N, et al. Long-term effects of mammography screening: Updated overview of the Swedish randomized trials. Lancet 2002;359:909-919 https://doi.org/10.1016/S0140-6736(02)08020-0
  58. Lubin JH, Boice JD. Lung cancer risk from residential radon: Meta-analysis of eight epidemiological studies. J. Natl. Cancer Inst. 1997;89:49-57 https://doi.org/10.1093/jnci/89.1.49
  59. Cohen BL. Tests of the linear, no-threshold dose-response relationship for high-LET radiation. Health Phys. 1987;52:629-636 https://doi.org/10.1097/00004032-198705000-00015
  60. Goldsmith JR. What do we expect from an occupational cohort? Occupat. Med. 1975;17:126-131 https://doi.org/10.1097/00043764-197502000-00016
  61. Doody MM, Mandel JS, Lubin JH, et al. Mortality among USA radiologic technologists 1926-1990. Cancer Causes Control 1998;9:67-75 https://doi.org/10.1023/A:1008801404245
  62. Lorenz E, Hollcroft JW, Miller E, et al. Long-term effects of acute and chronic radiation in mice. I. Survival and tumor incidence following acute irradiation of 0.11 r per day. J. Natl. Cancer Inst. 1955;15:1049
  63. Chernobyl Forum (IAEA, WHO, UNDP, UNEP, UN-OCHA, UNSCEAR, World Bank). Chernobyl's Legacy: Health, Environmental and Socio-Economic Impacts. The work is in three volumes and 600 pages by more than 100 scientists, 2005
  64. Robinette C, Jablob S, Preston TL. Studies of participants in nuclear tests. Final Rep. DOE/EV/0157, Nat. Res. Council, Washington, D.C, 1985
  65. Koshurnikova NA, Bolotnikova MG, Iyin LA, et al. Lung cancer risk due to exposure of incorporated plutonium. Radiat. Res. 1998;149:366-371 https://doi.org/10.2307/3579699
  66. Gilbert ES, Omohundro E, Buchanan JA, et al. Mortality of workers at the Hanford site: 1945-1986. Health Phys. 1993;64:577-590 https://doi.org/10.1097/00004032-199306000-00001
  67. Khokryakov VF, Romanov, SA. Radiation Impact on Lung Cancer. Nauchno-informatsionny byulleten yadernogo obshestva SSSR N 1992;4:16-17
  68. Gilbert ES, Koshurnikova NA, Sokolnikov M, et al. Liver Cancers in Mayak Workers. Radiat. Res. 2000;154:246-252 https://doi.org/10.1667/0033-7587(2000)154[0246:LCIMW]2.0.CO;2
  69. Wilkinson GS, TrieffN, Graham R, et al. Final Report. Study of Mortality Among Female Nuclear Weapons Workers. Grant Numbers: 1R01 OHO3274, R01/CCR214546, R01/CCR61 2934-01, National Institute for Occupational Safety and Health, Centers for Disease Control and Prevention, 2000
  70. Cox R, Hendry J, Kellerer A, etal. Biological and epidemiological information on health risks attributable to ionizing radiation: A summary of judgments for the purposes of radiological protection of humans. Committee 1 Task Group Report: C1 Foundation Document (FD-C-l), International Commission on Radiological Protection, 2005
  71. Darby SC, Whitley E, Howe GR, et al. Radon and cancers other than lung cancer in underground miners: a collaborative analysis of 11 studies. J. Natl. Cancer Inst. 87:378-384 https://doi.org/10.1093/jnci/87.5.378
  72. Luckey TD. Radiation Hormesis. Boca Raton, FL, CRC Press, 1991
  73. Fry SA, Dupree EA, Sipe AH, et al. A study of mortality and morbidity among persons occupationally exposed to >50 mSv in a year: Phase I, mortality through 1984. Appl. Occup. Environ. Hyg. 1996;11:334-343 https://doi.org/10.1080/1047322X.1996.10389333
  74. Howe GR, Zablotska LB, Fix JJ, et al. Analysis of the mortality experience amongst U.S. nuclear power industry workers after chronic low-dose exposure to ionizing radiation. Radiat. Res. 2004;162:517-526 https://doi.org/10.1667/RR3258
  75. Chen WL, Luan YC, Shieh MC, et al. Is chronic radiation an effective prophylaxis against cancer? J. Amer. Physicians and Surgeons 2004;9:6-10
  76. Howe GR. Lung Cancer Mortality Between 1950 and 1987 after Exposure to Fractionated Moderate-Dose-Rate Ionizing Radiation in the Canadian Fluoroscopy Cohort Study and a Comparison with Lung Cancer Mortality in the Atomic Bomb Survivors Study. Radiat. Res. 1995;142:295-304 https://doi.org/10.2307/3579139
  77. Mohan AK, Hauptmann M, Freedman DM, et al. Cancer and other causes of mortality among radiologic technologists in the United States. Intern. J. Cancer 2003;103:259-267 https://doi.org/10.1002/ijc.10811
  78. Tietjen GL. Plutonium and lung cancer. Health Physics 1987;52:625-628 https://doi.org/10.1097/00004032-198705000-00014
  79. Cohen BL. Test of the linear no-threshold theory of radiation carcinogenesis for inhaled radon decay products. Health Physics 1993;56:154-174
  80. Pollycove M, Feinendegen LE. Molecular biology, epidemiology and the demise of the linear no-threshold (LNT) hypothesis. In: CR Acad. Sci., Paris, Life Sciences 1999;322:197-204 https://doi.org/10.1016/S0764-4469(99)80044-4
  81. ICRP. Draft For Consultation. Recommendations of the International Commission on Radiological Protection, 2005
  82. Hatch M, Ron E, Bouville A, et al. The Chernobyl disaster: Cancer following the accident at the Chernobyl nuclear power plant. Epidemiol. Reviews 2005;27:56-66 https://doi.org/10.1093/epirev/mxi012
  83. Wang JX, Zhang LA, Bx Li, et al. Cancer incidence and risk estimation among medical x-ray workers in China 1950-1995. Health Phys. 2002;82:455-466 https://doi.org/10.1097/00004032-200204000-00004
  84. Tokarskaya ZB, Okladnikova ND, Belyaeva ZD, et al. Multifactorial Analysis of Lung Cancer Dose-Response Relationships for Workers at the Mayak Nuclear Enterprise. Health Physics 1997;73:899-905 https://doi.org/10.1097/00004032-199712000-00003
  85. Voelz GL, Wilkinson CS, Acquavelle JF. An Update of Epidemiologic Studies of Plutonium Workers. Health Physics 1983:44 (Suppl 1):493-503 https://doi.org/10.1097/00004032-198306001-00048
  86. Kusiak RA, Ritchie AC, Muller J, et al. Mortality from lung cancer in Ontario uranium miners. Br. J. Ind. Med. 50:920-928
  87. Aurengo A, Averbeck D, Bonnin A, et al. Dose- Effect Relationships and Estimation of the Carcinogenic Effectsof Low Doses of Ionizing Radiation. Executive Summary. French Academy of Sciences, French National Academy of Medicine, 2005
  88. Preston DL, Pierce DA, Shimizu Y, et al. Effect of recent changes in atomic bomb survivor dosimetry on cancer mortality risk estimates. Radiat. Res. 2004;162:377-389 https://doi.org/10.1667/RR3232
  89. Cohen BL. A test of the linear no-threshold theory of radiation carcinogenesis. Environ. Res.1990;53:193-220 https://doi.org/10.1016/S0013-9351(05)80119-7
  90. Toth E, Lazar I, Selmeczi D, et al.Lower cancer risk in medium high radon. Pathol. Oncol. Res. 1998;4:125-129 https://doi.org/10.1007/BF02904706
  91. Tubiana M, Aurengo A. Dose-Effect Relationship and Estimation of the Carcinogenic Effect of Low Doses of Ionizing Radiation. International Journal of Low Radiation 2005;2(3/4):134-151
  92. Bauer S, Gusev BI, Pivina LM, et al. 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. 2005;164:409-419 https://doi.org/10.1667/RR3423.1
  93. Yoshinaga S, Mabuchi K, Sigurdson AJ, et al. Cancer Risks Among Radiologists and Radiologic Technologists: A Review of Epidemiological Studies. Annual Report 2002-2003, National Institute of Radiological Sciences, Chiba, Japan, 2003
  94. Luckey TD. Hormesis with Ionizing Radiation. Boca Raton, FL: CRC Press, 1980
  95. Caratero A, Courtade M, Bonnet L, et al. Effect of a continuous gamma irradiation at a very low dose on the life span of mice. Gerontology 1998;44:272-276 https://doi.org/10.1159/000022024
  96. Frigerio NA, Stowe RS. Carcinogenic and genetic hazard from background radiation. In: Proc. Symp. On Biological Effects of Low-Level Radiation Pertinent to Protection of Man and His Environment, Chicago, IL, IAEA-SM-202/805, Vol. 2, International Atomic Energy Agency, Vienna, Austria, 1975:385- 393
  97. Brown SC, Schonbeck MF, McClure D, et al. Lung cancer and internal lung doses among plutonium workers at the Rocky Flats Plant: A case-control study. Amer. J. Epidemiol. 2004;160:163-172 https://doi.org/10.1093/aje/kwh192
  98. Thomas RG. The US radium luminisers. A case for a policy 'below regulatory concern'. J. Radiat. Protect. 1994;14:141-153 https://doi.org/10.1088/0952-4746/14/2/005
  99. Heidenreich WF, Paretzke HG, Jacob P. No evidence for increased tumor rates below 200 mSv in the atomic bomb survivors data. Radiat. Environ. Biophys. 1997;36:205-207 https://doi.org/10.1007/s004110050073
  100. Khohryakov V, Romanov S. Lung cancer in radiochemical industry workers. The Science of the Total Environment 1994;142:25-28 https://doi.org/10.1016/0048-9697(94)90069-8
  101. Kang HK, Bullman TA, Mahan CM. A mortality follow-up of World War II submariners who received nasopharyngeal radium irradiation treatment. Am. J. Ind. Med. 2000;38:441-446 https://doi.org/10.1002/1097-0274(200010)38:4<441::AID-AJIM10>3.0.CO;2-3
  102. McGeoghegan D, Binks K. The mortality and cancer morbidity experience of employees at the Chapelcross plant of British Nuclear Fuels pic, 1955-95. J. Radiol. Prot. 2001;21:221-250 https://doi.org/10.1088/0952-4746/21/3/302
  103. Mortazavi SMJ, Ghiassi-Nejad M, Karam PA, et al. Cancer Incidence in Areas with Elevated Levels of Natural Radiation. Intern. J. Low Radiation 2006;2:20-27 https://doi.org/10.1504/IJLR.2006.007892
  104. Cohen BL. Test of the linear no-threshold theory of radiation carcinogenesis for inhaled radon decay products. Health Phys. 1995;68:157-174 https://doi.org/10.1097/00004032-199502000-00002
  105. Rahu M, Tekkel M, Veidebaum T, et al. The Estonian study of Chernobyl cleanup workers: II. Incidence of cancer and mortality. Radiat. Res. 1997;147:641-652 https://doi.org/10.2307/3579631
  106. Band PR, Le ND, Fang R, et al. Cohort study of Air Canada pilots: Mortality, cancer incidence, and leukemia risk. Amer. J. Epidemiol. 1996;143:137-143 https://doi.org/10.1093/oxfordjournals.aje.a008722
  107. Yoshinaga S, Mabuchi K, Sigurdson AJ, et al. Cancer risks among radiologists and radiologic technologists: review of epidemiologic studies. Radiology 2004;233:313-321 https://doi.org/10.1148/radiol.2332031119
  108. Atkinson, WD, Law DV, Bromley KJ, et al. Mortality of employees of the United Kingdom Atomic Energy Authority, 1946-97. Occup. Environ. Med. 2004;61:577-585 https://doi.org/10.1136/oem.2003.012443
  109. National Research Council. Committee on Health Risks of Exposure to Radon, Health Effects of Exposure to Radon (BEIR VI), National Academy Press, Washington, DC, 199
  110. Committee to Assess Health Risks from Exposure to Low Levels of Ionizing Radiation. BEIR VII Phase 2, Health Risks from Exposure to Low Levels of Ionizing Radiation, National Research Council (National Academy of Sciences), 2005
  111. Loomis D, Wolf S. Mortality of workers at a nuclear materials production plant in Oak Ridge, Tennessee, 1947-1990. Amer. J. Ind. Med. 1996;29:131-141 https://doi.org/10.1002/(SICI)1097-0274(199602)29:2<131::AID-AJIM3>3.0.CO;2-V
  112. Wiggs LD, Johnson ER, Cox-DeVore CA, et al. Mortality through 1990 among white male workers at Los Alamos National Laboratory: Considering exposures to plutonium and external ionizing radiation. Health Phys. 1991;67:577-588
  113. Okumura Y, Mine M.Effects of low doses of A-bomb radiation on human lifespan. IAEA-TECDOC-976, IAEA-CN-67/129, 1997:414-416
  114. National Council on Radiation Protection and Measurements (NCRP). Exposures from the uranium series with emphasis on radon and its daughters. NCRP Report No. 77 (Bethseda, MD: NCRP) , 1984
  115. Arndt D. Die Strahlenexposition in den Bergbaugebieten Sachsens und Thuringens, In: Reiners, Chr. etal. (ed). Stranhlenschutz in Forschung und Parxis, 1992;33:47-60, Stuttgart, Germany
  116. Pierce DA, Shimizu Y, Preston DL, et al. Studies of the Mortality of Atomic Bomb Survivors. Report 12, Part 1, Cancer: 1950-1990. Radiat. Res. 1996;146:1-27 https://doi.org/10.2307/3579391
  117. UNSCEAR. United Nations Scientific Committee on the Effects of AtomicRadiation. Sources and Effects of Ionizing Radiation. UNSCEAR 1993 Report to the General Assembly with Scientific Annexes, United Nations, NY, 1993
  118. Pollycove M, Feinendegen LE. Biologic responses to low doses of ionizing radiation: Detriment versus hormesis. Part 2: Dose responses to organisms. J. Nucl. Med. 2001;42:26N-37N
  119. Imanaka, T, Fukutani S, Yamamoto M, et al. External Dose Assessment for Dolon Village due to Fallouts from the Semipalatinsk Nuclear Test Site. Proceedings of the Forty-Eighth Annual Meeting of the Japan Radiation Research Society/ the First Asian Congress of Radiation Research, Research Institute for Radiation Biology and Medicine, Hiroshima University, Japan, Abstract W2-5, 2005:104
  120. Rowland RE. Bone sarcoma in humans induced by radium: A threshold response? In: Radioprotection colloques, proceedings of the twenty-seventh annual meeting of the European Society for Radiation Biology 1997;32: Cl/331-338
  121. Raabe OG, Rosenblatt LS, Schlenker RA. Interspecies scaling of risk for radium-induced bone cancer. Intern. J. Radiat. Biol. 1990;57:1047-1061 https://doi.org/10.1080/09553009014551151
  122. Wilkinson GS, Tietjen GL, Wiggs LD, et al. Mortality among plutonium and other radiation workers at a plutonium weapons facility. Amer. J. Epidemiol. 1987;125:231-250 https://doi.org/10.1093/oxfordjournals.aje.a114523
  123. Arrighi HM, Hertz-Picciotto L. The evolving concept of the healthy worker survivor effect. Epidemiology 19945:189-196 https://doi.org/10.1097/00001648-199403000-00009
  124. Miller AB, Howe GR, Sherman GJ, et al. Mortality from breast cancer after irradiation during fluoroscopic examinations in patients being treated for tuberculosis. New England J. Med. 1989;321:1285-1289 https://doi.org/10.1056/NEJM198911093211902
  125. Matanoski GM. Health effects of low-level radiation in shipyard workers. Final Report. Report No. DOE DE-AC02-79EV10095. US Department of Energy, Washington, D.C, 1991
  126. EPA (Environmental Protection Agency). Estimating Radiogenic Cancer Risks. EPA Report 402-R-93-076, Washington, D.C, 1994
  127. Wei L, Sugahara T. An introductory overview of the epidemiological study on the population at the high background radiation areas in Yangjiang, China. J. Radiat. Res. (Tokyo), 2000;41 Suppl: 1-7 https://doi.org/10.1269/jrr.41.1
  128. Nambi KSV, Soman SD. Environmental radiation and cancer in India. Health Physics 1987;52:653-657 https://doi.org/10.1097/00004032-198705000-00018
  129. Yoshinaga S, Aoyama T, Yoshimotot Y, et al. Cancer mortality among radiological technologists in Japan: updated analysis of follow-up data from 1969 to 1993. J. Epidemiol. 1999;9:61-72 https://doi.org/10.2188/jea.9.61
  130. Shy C, Wing S. A report on mortality among workers of Oak Ridge National Laboratory: Follow up through 1990. (PO3C-70837, Final Report). Oak Ridge, TN: Oak Ridge Associated Universities, 1994:21
  131. Ivanov VK, Tsyb AF, Rastopchin EM, et al. Cancer Incidence among Nuclear Workers in Russia Based on Data from the Institute of Physics and Power engineering: A Preliminary analysis. Radiat. Res. 2001;155:801-808 https://doi.org/10.1667/0033-7587(2001)155[0801:CIANWI]2.0.CO;2
  132. Mifune M, Sobue T, Arimoto H, et al. Cancer mortality survey in a spa area (Misasa, Japan) with a high radon background. Jpn. J. Cancer Res. 1992;83:1-5 https://doi.org/10.1111/j.1349-7006.1992.tb02342.x
  133. Boice JD, Morin MM, Glass AG, et al. Diagnostic x-ray procedures and risk of leukemia, lymphoma and multiple myeloma. JAMA 1991;265:1290-1294 https://doi.org/10.1001/jama.265.10.1290
  134. Ivanov VK, Gorski AI, Maksioutov MA, et al. Mortality among the Chernobyl emergency workers: Estimation of radiation risks (preliminary analysis). Health Phys. 2001;81:514-521 https://doi.org/10.1097/00004032-200111000-00005
  135. Sun SQ, Li SY, Yuan LY. Radioepidemiological studies in the nuclear industry of China. Zhonghua Liu Xing Bing Xue Za Zhi 1996;17:333-336
  136. Khokhrykov VF, Romanov SA. Estimation of the temporal distribution and dose dependency of lung cancer among workers of nuclear fuel reprocessing plant. Health Physics 1996;71:83-85 https://doi.org/10.1097/00004032-199607000-00013
  137. Shimizu Y, Kato H, Schull WJ. Studies on the mortality of A-bomb survivors. 9, Mortality, 1950-1985: Part 2, Cancer mortality based on the recently revised doses (DS86), Radiation Research 1990;121:120-141 https://doi.org/10.2307/3577495
  138. Schull WJ, Otakee M, Neel JV. Genetic effects of the atomic bomb: Reappraisal. Science 1981;213:1220-1227 https://doi.org/10.1126/science.7268429
  139. Yalow RS. Radiation and public perception. In: Young, J.P. and R.S. Yalow (editors), Radiation and Public Perception, Benefits and Risks, American Chemical Society, Washingston, D.C., 1995:13-22
  140. Auvenin A, Maekelaeinen I, Hakama M, et a1. Indoor radon exposure and risk of lung cancer: A nested case-control study in Finland. J. Natl. Cancer Inst. 1996;88:966-972 https://doi.org/10.1093/jnci/88.14.966
  141. Evans RD. Radium in Man. Health Physics 1974;27:497-510 https://doi.org/10.1097/00004032-197411000-00010
  142. Franks P, Gold MR, Clancy CM. Use of care and subsequent mortality: The importance of gender. Health Serv. Res. 1996;31:347-363
  143. Feinendegen LE, Bond VP, Booz J, et al. Biochemical and cellular mechanisms of low-dose effects. Int. J. Radiat. Biol. 1988;53:23-37 https://doi.org/10.1080/09553008814550391
  144. Moss W, Eckhardt R. The human plutonium injection experiments. Los Alamos Science 1995;23:177-233
  145. Deetjen P, Falkenbach A (eds). Radon und Gesundheit, P. Land, Frankfurt, Germany, 1999
  146. Zakeri F, Ghiassi-Nejad M, Kanda MR, et al. Chromosome aberrations in lymphocytes of individuals living in high background radiation areas of Ramsar-Iran. Proceedings of the Forty-Eighth Annual Meeting of the Japan Radiation Research Society/ the First Asian Congress of Radiation Research, Research Institute for Radiation Biology and Medicine, Hiroshima University, Japan, 2005;Abstract S4-1-2:80
  147. Kostyuchenko VA, Krestina L. Long-term irradiation effects in the population evacuated from the East-Urals radioactive trace area. The Sci. Total Environ. 1994;142:119-125 https://doi.org/10.1016/0048-9697(94)90080-9
  148. Spengler RF, Cook DH, Clarke EA, et al. Cancer mortality following cardiac catheterization: A preliminary follow-up study on 4,891 irradiated children. Pediatrics 1983;71:235-239
  149. USDHHS (U.S. Department of Health and Human Services, Center for Disease Control and Prevention, National Center for Environmental Health). The Hanford Thyroid Disease Study (http://www.cdc.gov/nceh/radiation/hanford/htdsweb/index.htm), 2002
  150. Dousset M, Jammet H. Comparaison de la mortalite par cancer dans le Limousin et le Poitou-Charentes. Radioprotection 1985;20:61-67 https://doi.org/10.1051/radiopro/19852001061
  151. ICRP Publication 60. Recommendations of the International Commission on Radiological Protection, Annals of the ICRP 21 (1-3), 1991
  152. Howe GR, Nair RC, Hewcombe HG, et al. Lung cancer mortality (1950-1980) in relation to radon daughter exposures in a cohort of workers at the Eldorado Beaverlodge uranium mine. J. Natl. Cancer Inst. 1986;77:357-362
  153. Pollycove M. Nonlinearity of radiation health effects. Environ. Health Perspect. 1998;106:363-368 https://doi.org/10.2307/3433939
  154. Cardis E, Gilbert ES, Carpenter L, et al. Effects of low doses and low dose rates of external ionizing radiation: Cancer mortality among nuclear industry workers in three countries. Radiat. Res. 1995;142:117-132 https://doi.org/10.2307/3579020
  155. Mayya YS. 2005. A Study of Cancer Mortality Among Indian Atomic Energy. Proceedings of the Forty-Eighth Annual Meeting of the Japan Radiation Research Society/ the First Asian Congress of Radiation Research, Research Institute for Radiation Biology and Medicine, Hiroshima University, Japan, Abstract Sl1-4, 2005:89-90
  156. Chmelevsky, D, Kellerer AM, Land CE, et al. Time and dose dependency of bone-sarcomas in patients injected with radium-224. Radiat. Environ. Biophys. 1988;27:103-114 https://doi.org/10.1007/BF01214600
  157. Howe GR, McLaughlin J. Breast cancer mortality between 1950 and 1987 after exposure to fractionated moderate-dose-rate ionizing radiation in the Canadian fluoroscopy cohort study and a comparison with breast cancer mortality in the atomic bomb survivors study. Radiat. Res. 1996;149:694-707
  158. Darby S, Hill D, Auvinen A, et al. Radon in homes and risk of lung cancer: Collaborative analysis of individual data from 13 European case-control studies. Brit. Med. J. 2005;330:223-226 https://doi.org/10.1136/bmj.38308.477650.63
  159. Neuberger JS. Residential radon exposure and lung cancer: an overview of ongoing studies. Health Phys. 1992;63:503-509 https://doi.org/10.1097/00004032-199211000-00001
  160. Zablotska LB, Ashmore JP, Howe GR. Analysis of mortality among Canadian nuclear power industry workers after chronic low-dose exposure to ionizing radiation. Radiat. Res. 2004;161:633-641 https://doi.org/10.1667/RR3170
  161. Koshurnikova NA, Gilbert ES, Sokolnikov M, et al. Bone Cancers in Mayak Workers. Radiat. Res. 2000;154:237-245 https://doi.org/10.1667/0033-7587(2000)154[0237:BCIMW]2.0.CO;2
  162. Blettner M., Zeeb H, Langner I, et al. Mortality from cancer and other causes among airline cabin attendants in Germany, 1960-1997. Amer. J. Epidemiol. 2002;156:556-565 https://doi.org/10.1093/aje/kwf083
  163. Bowie C, Bowie SHU. Radon and health. Lancet 1991;337:409-413 https://doi.org/10.1016/0140-6736(91)91177-V
  164. Davis FG, Boice J, Hrubec D, et al. Lung cancer mortality in a radiation-exposed cohort of Massachusetts tuberculosis patients. 1989: Cancer Res. 49:6130-6136
  165. Lubin JH, Linet MS, Boice JD, et al. Patient-control study of childhood acute lymphoblastic leukaemia and residential radon exposure. J. Natl. Cancer Inst. 1998;90:294-300 https://doi.org/10.1093/jnci/90.4.294
  166. Calabrese EJ, Baldwin LA. The hormetic dose-response model is more common than the threshold model in toxicology. Toxicol. Sci. 2003;71:246-250 https://doi.org/10.1093/toxsci/71.2.246
  167. Tubiana M. The Carcinogenic Effect of Low Doses: the Validity of the Linear No-Threshold Relationship. Intern. J. Low Radiation 2003;1:1-33 https://doi.org/10.1504/IJLR.2003.003489
  168. Wiggs LD, Cox-DeVore CA,Voelz G. Mortality among a cohort of workers monitored for $^{210}Po$ exposure: 1944-1972. Health Physics 1991;61:71-76 https://doi.org/10.1097/00004032-199107000-00007
  169. UNSCEAR. Sources and effects of ionizing radiation. United Nations Scientific Committee on the Effects of Atomic Radiation 2000 Report to the General Assembly, with Annexes. Volume II: Effects. No. E.00.IX.4, United Nations, New York, NY, 2000
  170. Shadley JD, Wieneke JK. Induction of the adaptive response by X-rays is dependent on radiation intensity. Int. J. Radiat. Biol. 1989;56:107-118 https://doi.org/10.1080/09553008914551231
  171. Luan Y, Shieh MC, Chen ST, et al. Health Effects from Different Radiation. Proceedings of the Forty-Eighth Annual Meeting of the Japan Radiation Research Society/ the First Asian Congress of Radiation Research, Research Institute for Radiation Biology and Medicine, Hiroshima University, Japan, Abstract S10-2, 2005: 88
  172. Land CE. Estimating cancer risks from low doses of ionizing radiation. Science 1980;209:1197 https://doi.org/10.1126/science.7403879
  173. Spiers FW, Lucas HF, Rundo J, et al. Leukemia incidence in the U.S. dial workers, Health Phys. 1983;44 (Suppl. 1):65-72 https://doi.org/10.1097/00004032-198306001-00004
  174. Skelcher B. Healthy worker effect. J. Radiol. Prot. 2001;21:71-72 https://doi.org/10.1088/0952-4746/21/1/105