Radiation and Environmental Biophysics

, Volume 52, Issue 4, pp 435–449 | Cite as

A review of non-cancer effects, especially circulatory and ocular diseases

  • Mark P. Little
Review Article


There is a well-established association between high doses (>5 Gy) of ionizing radiation exposure and damage to the heart and coronary arteries, although only recently have studies with high-quality individual dosimetry been conducted that would enable quantification of this risk adjusting for concomitant chemotherapy. The association between lower dose exposures and late occurring circulatory disease has only recently begun to emerge in the Japanese atomic bomb survivors and in various occupationally exposed cohorts and is still controversial. Excess relative risks per unit dose in moderate- and low-dose epidemiological studies are somewhat variable, possibly a result of confounding and effect modification by well-known (but unobserved) risk factors. Radiation doses of 1 Gy or more are associated with increased risk of posterior subcapsular cataract. Accumulating evidence from the Japanese atomic bomb survivors, Chernobyl liquidators, US astronauts, and various other exposed groups suggests that cortical cataracts may also be associated with ionizing radiation, although there is little evidence that nuclear cataracts are radiogenic. The dose–response appears to be linear, although modest thresholds (of no more than about 0.6 Gy) cannot be ruled out. A variety of other non-malignant effects have been observed after moderate/low-dose exposure in various groups, in particular respiratory and digestive disease and central nervous system (and in particular neuro-cognitive) damage. However, because these are generally only observed in isolated groups, or because the evidence is excessively heterogeneous, these associations must be treated with caution.


Circulatory disease Radiation Heart disease Stroke Cataract Central nervous system Review 



This work was supported by the Intramural Research Program of the National Institutes of Health, the National Cancer Institute, Division of Cancer Epidemiology and Genetics. The author is grateful for the detailed and helpful comments of Dr Alice Sigurdson and the two referees.


  1. Adams MJ, Hardenbergh PH, Constine LS, Lipshultz SE (2003) Radiation-associated cardiovascular disease. Crit Rev Oncol Hematol 45:55–75CrossRefGoogle Scholar
  2. Adams MJ, Grant EJ, Kodama K, Shimizu Y, Kasagi F, Suyama A, Sakata R, Akahoshi M (2012) Radiation dose associated with renal failure mortality: a potential pathway to partially explain increased cardiovascular disease mortality observed after whole-body irradiation. Radiat Res 177:220–228CrossRefGoogle Scholar
  3. Advisory Group on Ionising Radiation (2010) Circulatory disease risk. Report of the independent Advisory Group on Ionising Radiation. Health Protection Agency, Holborn Gate, 330 High Holborn, London, pp 1–116Google Scholar
  4. Ainsbury EA, Bouffler SD, Dörr W, Graw J, Muirhead CR, Edwards AA, Cooper J (2009) Radiation cataractogenesis: a review of recent studies. Radiat Res 172:1–9CrossRefGoogle Scholar
  5. Azizova TV, Muirhead CR, Druzhinina MB, Grigoryeva ES, Vlasenko EV, Sumina MV, O’Hagan JA, Zhang W, Haylock RGE, Hunter N (2010a) Cardiovascular diseases in the cohort of workers first employed at Mayak PA in 1948–1958. Radiat Res 174:155–168CrossRefGoogle Scholar
  6. Azizova TV, Muirhead CR, Druzhinina MB, Grigoryeva ES, Vlasenko EV, Sumina MV, O’Hagan JA, Zhang W, Haylock RGE, Hunter N (2010b) Cerebrovascular diseases in the cohort of workers first employed at Mayak PA in 1948–1958. Radiat Res 174:851–864CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR (1998) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York, pp 1–496CrossRefGoogle Scholar
  8. Burns DM (2003) Epidemiology of smoking-induced cardiovascular disease. Prog Cardiovasc Dis 46:11–29CrossRefGoogle Scholar
  9. Chen W-L, Hwang J-S, Hu T-H, Chen M-S, Chang WP (2001) Lenticular opacities in populations exposed to chronic low-dose-rate gamma radiation from radiocontaminated buildings in Taiwan. Radiat Res 156:71–77CrossRefGoogle Scholar
  10. Chodick G, Bekiroglu N, Hauptmann M, Alexander BH, Freedman DM, Doody MM, Cheung LC, Simon SL, Weinstock RM, Bouville A, Sigurdson AJ (2008) Risk of cataract after exposure to low doses of ionizing radiation: a 20-year prospective cohort study among US radiologic technologists. Am J Epidemiol 168:620–631CrossRefGoogle Scholar
  11. Chylack LT Jr, Peterson LE, Feiveson AH, Wear ML, Manuel FK, Tung WH, Hardy DS, Marak LJ, Cucinotta FA (2009) NASA study of cataract in astronauts (NASCA). Report 1: cross-sectional study of the relationship of exposure to space radiation and risk of lens opacity. Radiat Res 172:10–20CrossRefGoogle Scholar
  12. Chylack LT Jr, Feiveson AH, Peterson LE, Tung WH, Wear ML, Marak LJ, Hardy DS, Chappell LJ, Cucinotta FA (2012) NASCA report 2: longitudinal study of relationship of exposure to space radiation and risk of lens opacity. Radiat Res 178:25–32CrossRefGoogle Scholar
  13. Ciraj-Bjelac O, Rehani MM, Sim KH, Liew HB, Vano E, Kleiman NJ (2010) Risk for radiation-induced cataract for staff in interventional cardiology: is there reason for concern? Catheter Cardiovasc Interv 76:826–834Google Scholar
  14. Claeskens G, Hjort NL (2008) Model selection and model averaging. In: Cambridge series in statistical and probabilistic mathematics. Cambridge University Press, Cambridge, pp 1–312Google Scholar
  15. Cogan DG, Donaldson DD, Reese AB (1952) Clinical and pathological characteristics of radiation cataract. AMA Arch Ophthalmol 47:55–70CrossRefGoogle Scholar
  16. Committee to Assess Health Risks from Exposure to Low Levels of Ionizing Radiation. National Research Council (2006) Health risks from exposure to low levels of ionizing radiation: BEIR VII—phase 2. National Academy Press, Washington, DC, pp 1–406Google Scholar
  17. Danesh J, Whincup P, Lewington S, Walker M, Lennon L, Thomson A, Wong Y-K, Zhou X, Ward M (2002) Chlamydia pneumoniae IgA titres and coronary heart disease—prospective study and meta-analysis. Eur Heart J 23:371–375CrossRefGoogle Scholar
  18. Darby SC, Ewertz M, McGale P, Bennet AM, Blom-Goldman U, Brønnum D, Correa C, Cutter D, Gagliardi G, Gigante B, Jensen M-B, Nisbet A, Peto R, Rahimi K, Taylor C, Hall P (2013) Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med 368:987–998CrossRefGoogle Scholar
  19. Day R, Gorin MB, Eller AW (1995) Prevalence of lens changes in Ukrainian children residing around Chernobyl. Health Phys 68:632–642Google Scholar
  20. Delcourt C, Dupuy A-M, Carriere I, Lacroux A, Cristol J-P (2005) Albumin and transthyretin as risk factors for cataract: the POLA study. Arch Ophthalmol 123:225–232CrossRefGoogle Scholar
  21. Devi A, Raina PL, Singh A (1965) Abnormal protein and nucleic acid metabolism as a cause of cataract formation induced by nutritional deficiency in rabbits. Br J Ophthalmol 49:271–275CrossRefGoogle Scholar
  22. Edwards AA, Lloyd DC (1998) Risks from ionising radiation: deterministic effects. J Radiol Prot 18:175–183CrossRefGoogle Scholar
  23. Folley JH, Borges W, Yamawaki T (1952) Incidence of leukemia in survivors of the atomic bomb in Hiroshima and Nagasaki, Japan. Am J Med 13:311–321CrossRefGoogle Scholar
  24. Gluckman PD, Hanson MA, Beedle AS (2007) Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol 19:1–19CrossRefGoogle Scholar
  25. Grantham-McGregor S (1995) A review of studies of the effect of severe malnutrition on mental development. J Nutr 125:2233S–2238SGoogle Scholar
  26. Grosche B, Lackland DT, Land CE, Simon SL, Apsalikov KN, Pivina LM, Bauer S, Gusev BI (2011) Mortality from cardiovascular diseases in the Semipalatinsk historical cohort, 1960–1999, and its relationship to radiation exposure. Radiat Res 176:660–669CrossRefGoogle Scholar
  27. Hall P, Granath F, Lundell M, Olsson K, Holm L-E (1999) Lenticular opacities in individuals exposed to ionizing radiation in infancy. Radiat Res 152:190–195CrossRefGoogle Scholar
  28. Hall P, Adami H-O, Trichopoulos D, Pedersen NL, Lagiou P, Ekbom A, Ingvar M, Lundell M, Granath F (2004) Effect of low doses of ionising radiation in infancy on cognitive function in adulthood: Swedish population based cohort study. BMJ 328:19CrossRefGoogle Scholar
  29. Hammer GP, Scheidemann-Wesp U, Samkange-Zeeb F, Wicke H, Neriishi K, Blettner M (2013) Occupational exposure to low doses of ionizing radiation and cataract development: a systematic literature review and perspectives on future studies. Radiat Environ Biophys 52:303–319Google Scholar
  30. Harding JJ, Crabbe MJC (1984) The eye (3rd edition). In: Davson H (ed) The lens: development, proteins, metabolism and cataract. Academic Press, Orlando, pp 207–492Google Scholar
  31. Hourihan F, Mitchell P, Cumming RG (1999) Possible associations between computed tomography scan and cataract: the Blue Mountains Eye Study. Am J Public Health 89:1864–1866Google Scholar
  32. Hsieh WA, Lin I-F, Chang WP, Chen W-L, Hsu YH, Chen M-S (2010) Lens opacities in young individuals long after exposure to protracted low-dose-rate γ radiation in 60Co-contaminated buildings in Taiwan. Radiat Res 173:197–204CrossRefGoogle Scholar
  33. Imamura Y, Nakane Y, Ohta Y, Kondo H (1999) Lifetime prevalence of schizophrenia among individuals prenatally exposed to atomic bomb radiation in Nagasaki City. Acta Psychiatr Scand 100:344–349CrossRefGoogle Scholar
  34. International Commission on Radiological Protection (2012) ICRP statement on tissue reactions and early and late effects of radiation in normal tissues and organs—threshold doses for tissue reactions in a radiation protection context. ICRP publication 118. Ann ICRP 41(1–2):1–322Google Scholar
  35. Ivanov VK, Maksioutov MA, Chekin SY, Petrov AV, Biryukov AP, Kruglova ZG, Matyash VA, Tsyb AF, Manton KG, Kravchenko JS (2006) The risk of radiation-induced cerebrovascular disease in Chernobyl emergency workers. Health Phys 90:199–207CrossRefGoogle Scholar
  36. Jones JA, McCarten M, Manuel K, Djojonegoro B, Murray J, Feiversen A, Wear M (2007) Cataract formation mechanisms and risk in aviation and space crews. Aviat Space Environ Med 78:A56–A66Google Scholar
  37. Kleiman NJ, Worgul BV (1994) Duane’s foundations of clinical ophthalmology, volume 1. In: Tasman W, Jaeger EA (eds) Lens. JP Lippincott and Co., Philadelphia, PA, pp 1–39Google Scholar
  38. Klein BEK, Klein R, Linton KLP, Franke T (1993) Diagnostic X-ray exposure and lens opacities: the Beaver Dam eye study. Am J Public Health 83:588–590CrossRefGoogle Scholar
  39. Klein BEK, Klein R, Moss SE (2000) Exposure to diagnostic x-rays and incident age-related eye disease. Ophthalmic Epidemiol 7:61–65Google Scholar
  40. Krestinina LY, Epifanova S, Silkin S, Mikryukova L, Degteva M, Shagina N, Akleyev A (2013) Chronic low-dose exposure in the Techa River cohort: risk of mortality from circulatory diseases. Radiat Environ Biophys 52:47–57CrossRefGoogle Scholar
  41. Kreuzer M, Kreisheimer M, Kandel M, Schnelzer M, Tschense A, Grosche B (2006) Mortality from cardiovascular diseases in the German uranium miners cohort study, 1946–1998. Radiat Environ Biophys 45:159–166CrossRefGoogle Scholar
  42. Kreuzer M, Dufey F, Sogl M, Schnelzer M, Walsh L (2013) External gamma radiation and mortality from cardiovascular diseases in the German WISMUT uranium miners cohort study, 1946–2008. Radiat Environ Biophys 52:37–46CrossRefGoogle Scholar
  43. Kuck J (1970) Biochemistry of the eye. In: Graymore CN (ed) Metabolism of the lens. Academic Press, London, pp 261–318Google Scholar
  44. Kusunoki Y, Kyoizumi S, Hirai Y, Suzuki T, Nakashima E, Kodama K, Seyama T (1998) Flow cytometry measurements of subsets of T, B and NK cells in peripheral blood lymphocytes of atomic bomb survivors. Radiat Res 150:227–236CrossRefGoogle Scholar
  45. Kuszak JR, Brown HG (1994) Principles and practice of ophthalmology: basic sciences. In: Albert DM, Jackobiec FA (eds) Embryology and anatomy of the lens. WB Saunders, Philadelphia, pp 82–96Google Scholar
  46. Lane RS, Frost SE, Howe GR, Zablotska LB (2010) Mortality (1950–1999) and cancer incidence (1969–1999) in the cohort of Eldorado uranium workers. Radiat Res 174:773–785CrossRefGoogle Scholar
  47. Laurent O, Metz-Flamant C, Rogel A, Hubert D, Riedel A, Garcier Y, Laurier D (2010) Relationship between occupational exposure to ionizing radiation and mortality at the French electricity company, period 1961–2003. Int Arch Occup Environ Health 83:935–944CrossRefGoogle Scholar
  48. Little MP (2002) Absence of evidence for differences in the dose-response for cancer and non-cancer endpoints by acute injury status in the Japanese atomic-bomb survivors. Int J Radiat Biol 78:1001–1010CrossRefGoogle Scholar
  49. Little MP (2004) Threshold and other departures from linear-quadratic curvature in the non-cancer mortality dose-response curve in the Japanese atomic bomb survivors. Radiat Environ Biophys 43:67–75CrossRefGoogle Scholar
  50. Little MP, Charles MW (1990) Bomb survivor selection and consequences for estimates of population cancer risks. Health Phys 59:765–775CrossRefGoogle Scholar
  51. Little MP, Tawn EJ, Tzoulaki I, Wakeford R, Hildebrandt G, Paris F, Tapio S, Elliott P (2008) A systematic review of epidemiological associations between low and moderate doses of ionizing radiation and late cardiovascular effects, and their possible mechanisms. Radiat Res 169:99–109CrossRefGoogle Scholar
  52. Little MP, Gola A, Tzoulaki I (2009) A model of cardiovascular disease giving a plausible mechanism for the effect of fractionated low-dose ionizing radiation exposure. PLoS Comput Biol 5:e1000539MathSciNetCrossRefGoogle Scholar
  53. Little MP, Tawn EJ, Tzoulaki I, Wakeford R, Hildebrandt G, Paris F, Tapio S, Elliott P (2010) Review and meta-analysis of epidemiological associations between low/moderate doses of ionizing radiation and circulatory disease risks, and their possible mechanisms. Radiat Environ Biophys 49:139–153CrossRefGoogle Scholar
  54. Little MP, Azizova TV, Bazyka D, Bouffler SD, Cardis E, Chekin S, Chumak VV, Cucinotta FA, de Vathaire F, Hall P, Harrison JD, Hildebrandt G, Ivanov V, Kashcheev VV, Klymenko SV, Kreuzer M, Laurent O, Ozasa K, Schneider T, Tapio S, Taylor AM, Tzoulaki I, Vandoolaeghe WL, Wakeford R, Zablotska LB, Zhang W, Lipshultz SE (2012a) Systematic review and meta-analysis of circulatory disease from exposure to low-level ionizing radiation and estimates of potential population mortality risks. Environ Health Perspect 120:1503–1511CrossRefGoogle Scholar
  55. Little MP, Kleinerman RA, Stovall M, Smith SA, Mabuchi K (2012b) Analysis of dose response for circulatory disease after radiotherapy for benign disease. Int J Radiat Oncol Biol Phys 84:1101–1109CrossRefGoogle Scholar
  56. Little MP, Azizova TV, Bazyka D, Bouffler SD, Cardis E, Chekin S, Chumak VV, Cucinotta FA, de Vathaire F, Hall P, Harrison JD, Hildebrandt G, Ivanov V, Kashcheev VV, Klymenko SV, Laurent O, Ozasa K, Tapio S, Taylor AM, Tzoulaki I, Vandoolaeghe WL, Wakeford R, Zablotska L, Zhang W, Lipshultz SE (2013a) Comment on “Dose-responses from multi-model inference for the non-cancer disease mortality of atomic bomb survivors” (Radiat. Environ. Biophys (2012) 51:165–178) by Schöllnberger et al. Radiat Environ Biophys 52:157–159Google Scholar
  57. Little MP, Zablotska LB, Lipshultz SE (2013b) Ischemic heart disease after breast cancer radiotherapy. N Engl J Med 368:2523–2524CrossRefGoogle Scholar
  58. McAvoy JW (1978) Cell division, cell elongation and distribution of α-, β- and γ-crystallins in the rat lens. J Embryol Exp Morphol 44:149–165Google Scholar
  59. McGale P, Darby SC (2005) Low doses of ionizing radiation and circulatory diseases: a systematic review of the published epidemiological evidence. Radiat Res 163:247–257, 711Google Scholar
  60. McGale P, Darby SC (2008) Commentary: a dose-response relationship for radiation-induced heart disease–current issues and future prospects. Int J Epidemiol 37:518–523CrossRefGoogle Scholar
  61. McGeoghegan D, Binks K, Gillies M, Jones S, Whaley S (2008) The non-cancer mortality experience of male workers at British Nuclear Fuels plc, 1946–2005. Int J Epidemiol 37:506–518CrossRefGoogle Scholar
  62. Minamoto A, Taniguchi H, Yoshitani N, Mukai S, Yokoyama T, Kumagami T, Tsuda Y, Mishima HK, Amemiya T, Nakashima E, Neriishi K, Hida A, Fujiwara S, Suzuki G, Akahoshi M (2004) Cataract in atomic bomb survivors. Int J Radiat Biol 80:339–345CrossRefGoogle Scholar
  63. Mitchel RE, Hasu M, Bugden M, Wyatt H, Little MP, Gola A, Hildebrandt G, Priest ND, Whitman SC (2011) Low-dose radiation exposure and atherosclerosis in ApoE −/− mice. Radiat Res 175:665–676CrossRefGoogle Scholar
  64. Mrena S, Kivelä T, Kurttio P, Auvinen A (2011) Lens opacities among physicians occupationally exposed to ionizing radiation—a pilot study in Finland. Scand J Work Environ Health 37:237–243CrossRefGoogle Scholar
  65. Muirhead CR, O’Hagan JA, Haylock RGE, Phillipson MA, Willcock T, Berridge GLC, Zhang W (2009) Mortality and cancer incidence following occupational radiation exposure: third analysis of the National Registry for Radiation Workers. Br J Cancer 100:206–212CrossRefGoogle Scholar
  66. Mulrooney DA, Yeazel MW, Kawashima T, Mertens AC, Mitby P, Stovall M, Donaldson SS, Green DM, Sklar CA, Robison LL, Leisenring WM (2009) Cardiac outcomes in a cohort of adult survivors of childhood and adolescent cancer: retrospective analysis of the Childhood Cancer Survivor Study cohort. BMJ 339:b4606CrossRefGoogle Scholar
  67. Nakashima E, Carter RL, Neriishi K, Tanaka S, Funamoto S (1995) Height reduction among prenatally exposed atomic-bomb survivors: a longitudinal study of growth. Health Phys 68:766–772CrossRefGoogle Scholar
  68. Nakashima E, Neriishi K, Minamoto A (2006) A reanalysis of atomic-bomb cataract data, 2000–2002: a threshold analysis. Health Phys 90:154–160CrossRefGoogle Scholar
  69. Neriishi K, Nakashima E, Akahoshi M, Hida A, Grant EJ, Masunari N, Funamoto S, Minamoto A, Fujiwara S, Shore RE (2012) Radiation dose and cataract surgery incidence in atomic bomb survivors, 1986–2005. Radiology 265:167–174CrossRefGoogle Scholar
  70. Otake M, Schull WJ (1993) Radiation-related small head sizes among prenatally exposed A-bomb survivors. Int J Radiat Biol 63:255–270CrossRefGoogle Scholar
  71. Otake M, Schull WJ (1998) Radiation-related brain damage and growth retardation among the prenatally exposed atomic bomb survivors. Int J Radiat Biol 74:159–171CrossRefGoogle Scholar
  72. Ozasa K, Shimizu Y, Suyama A, Kasagi F, Soda M, Grant EJ, Sakata R, Sugiyama H, Kodama K (2012) Studies of the mortality of atomic bomb survivors, report 14, 1950–2003: an overview of cancer and noncancer diseases. Radiat Res 177:229–243CrossRefGoogle Scholar
  73. 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 160:381–407CrossRefGoogle Scholar
  74. 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 168:1–64CrossRefGoogle Scholar
  75. Rafnsson V, Olafsdottir E, Hrafnkelsson J, Sasaki H, Arnarsson A, Jonasson F (2005) Cosmic radiation increases the risk of nuclear cataract in airline pilots: a population-based case-control study. Arch Ophthalmol 123:1102–1105CrossRefGoogle Scholar
  76. Rastegar N, Eckart P, Mertz M (2002) Radiation-induced cataract in astronauts and cosmonauts. Graefes Arch Clin Exp Ophthalmol 240:543–547Google Scholar
  77. Richardson DB, Wing S (1999) Radiation and mortality of workers at Oak Ridge National Laboratory: positive associations for doses received at older ages. Environ Health Perspect 107:649–656CrossRefGoogle Scholar
  78. Ridker PM (1998) Inflammation, infection, and cardiovascular risk: how good is the clinical evidence? Circulation 97:1671–1674CrossRefGoogle Scholar
  79. Ross L, Johansen C, Dalton SO, Mellemkjær L, Thomassen LH, Mortensen PB, Olsen JH (2003) Psychiatric hospitalizations among survivors of cancer in childhood or adolescence. N Engl J Med 349:650–657CrossRefGoogle Scholar
  80. Sadetzki S, Chetrit A, Mandelzweig L, Nahon D, Freedman L, Susser E, Gross R (2011) Childhood exposure to ionizing radiation to the head and risk of schizophrenia. Radiat Res 176:670–677CrossRefGoogle Scholar
  81. Schervish MJ (1995) Theory of statistics. Springer, New York, pp 1–724zbMATHGoogle Scholar
  82. Schöllnberger H, Kaiser JC, Jacob P, Walsh L (2012) Dose-responses from multi-model inference for the non-cancer disease mortality of atomic bomb survivors. Radiat Environ Biophys 51:165–178CrossRefGoogle Scholar
  83. Schöllnberger H, Kaiser JC, Walsh L, Jacob P (2013) Reply to Little et al.: dose-responses from multi-model inference for the non-cancer disease mortality of atomic bomb survivors. Radiat Environ Biophys 52:161–163CrossRefGoogle Scholar
  84. Schull WJ, Otake M (1999) Cognitive function and prenatal exposure to ionizing radiation. Teratology 59:222–226CrossRefGoogle Scholar
  85. Schultz-Hector S, Trott K-R (2007) Radiation-induced cardiovascular diseases: is the epidemiologic evidence compatible with the radiobiologic data? Int J Radiat Oncol Biol Phys 67:10–18CrossRefGoogle Scholar
  86. Shimizu Y, Kodama K, Nishi N, Kasagi F, Suyama A, Soda M, Grant EJ, Sugiyama H, Sakata R, Moriwaki H, Hayashi M, Konda M, Shore RE (2010) Radiation exposure and circulatory disease risk: Hiroshima and Nagasaki atomic bomb survivor data, 1950–2003. BMJ 340:b5349CrossRefGoogle Scholar
  87. Skilton MR, Gosby AK, Wu BJ, Ho LML, Stocker R, Caterson ID, Celermajer DS (2006) Maternal undernutrition reduces aortic wall thickness and elastin content in offspring rats without altering endothelial function. Clin Sci 111:281–287CrossRefGoogle Scholar
  88. Stewart AM, Kneale GW (1984) Non-cancer effects of exposure to A-bomb radiation. J Epidemiol Community Health 38:108–112CrossRefGoogle Scholar
  89. Stewart AM, Kneale GW (2000) A-bomb survivors: factors that may lead to a re-assessment of the radiation hazard. Int J Epidemiol 29:708–714CrossRefGoogle Scholar
  90. Syndikus I, Tait D, Ashley S, Jannoun L (1994) Long-term follow-up of young children with brain tumors after irradiation. Int J Radiat Oncol Biol Phys 30:781–787CrossRefGoogle Scholar
  91. Talbott EO, Youk AO, McHugh-Pemu KP, Zborowski JV (2003) Long-term follow-up of the residents of the Three Mile Island accident area: 1979–1998. Environ Health Perspect 111:341–348CrossRefGoogle Scholar
  92. Tatsukawa Y, Nakashima E, Yamada M, Funamoto S, Hida A, Akahoshi M, Sakata R, Ross NP, Kasagi F, Fujiwara S, Shore RE (2008) Cardiovascular disease risk among atomic bomb survivors exposed in utero, 1978–2003. Radiat Res 170:269–274CrossRefGoogle Scholar
  93. 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 160:691–706CrossRefGoogle Scholar
  94. Tüchsen F, Hannerz H, Burr H (2006) A 12 year prospective study of circulatory disease among Danish shift workers. Occup Environ Med 63:451–455CrossRefGoogle Scholar
  95. Tukenova M, Guibout C, Oberlin O, Doyon F, Mousannif A, Haddy N, Guérin S, Pacquement H, Aouba A, Hawkins M, Winter D, Bourhis J, Lefkopoulos D, Diallo I, de Vathaire F (2010) Role of cancer treatment in long-term overall and cardiovascular mortality after childhood cancer. J Clin Oncol 28:1308–1315CrossRefGoogle Scholar
  96. United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) (2008a) UNSCEAR 2006 report. Annex A. Epidemiological Studies of Radiation and Cancer. United Nations, New York, pp 13–322Google Scholar
  97. United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) (2008b) UNSCEAR 2006 report. Annex B. Epidemiological Evaluation of Cardiovascular Disease and other Non-Cancer Diseases following Radiation Exposure. United Nations, New York, pp 325–383Google Scholar
  98. van Heyningen R (1975) What happens to the human lens in cataract. Sci Am 233:70–81CrossRefGoogle Scholar
  99. von Sallmann L (1957) The lens epithelium in the pathogenesis of cataract. Trans Am Acad Ophthalmol Otolaryngol 61:7–19Google Scholar
  100. von Sallmann L, Grimes P, McElvain N (1962) Aspects of mitotic activity in relation to cell proliferation in the lens epithelium. Exp Eye Res 1:449–456CrossRefGoogle Scholar
  101. Vrijheid M, Cardis E, Ashmore P, Auvinen A, Bae J-M, Engels H, Gilbert E, Gulis G, Habib RR, Howe G, Kurtinaitis J, Malker H, Muirhead CR, Richardson DB, Rodriguez-Artalejo F, Rogel A, Schubauer-Berigan M, Tardy H, Telle-Lamberton M, Usel M, Veress K (2007) Mortality from diseases other than cancer following low doses of ionizing radiation: results from the 15-Country Study of nuclear industry workers. Int J Epidemiol 36:1126–1135CrossRefGoogle Scholar
  102. Wang C, Parmigiani G, Dominici F (2012) Bayesian effect estimation accounting for adjustment uncertainty. Biometrics 68:661–671CrossRefzbMATHGoogle Scholar
  103. Whincup P, Danesh J, Walker M, Lennon L, Thomson A, Appleby P, Hawkey C, Atherton J (2000) Prospective study of potentially virulent strains of Helicobacter pylori and coronary heart disease in middle-aged men. Circulation 101:1647–1652CrossRefGoogle Scholar
  104. Wilde G, Sjöstrand J (1997) A clinical study of radiation cataract formation in adult life following γ irradiation of the lens in early childhood. Br J Ophthalmol 81:261–266CrossRefGoogle Scholar
  105. Wilson PW, D’Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB (1998) Prediction of coronary heart disease using risk factor categories. Circulation 97:1837–1847CrossRefGoogle Scholar
  106. Worgul BV, Merriam GR Jr, Medvedovsky C (1989) Cortical cataract development—an expression of primary damage to the lens epithelium. Lens Eye Toxic Res 6:559–571Google Scholar
  107. Worgul BV, Kundiyev YI, Sergiyenko NM, Chumak VV, Vitte PM, Medvedovsky C, Bakhanova EV, Junk AK, Kyrychenko OY, Musijachenko NV, Shylo SA, Vitte OP, Xu S, Xue X, Shore RE (2007) Cataracts among Chernobyl clean-up workers: implications regarding permissible eye exposures. Radiat Res 167:233–243CrossRefGoogle Scholar
  108. Yamada M, Wong FL, Fujiwara S, Akahoshi M, Suzuki G (2004) Noncancer disease incidence in atomic bomb survivors, 1958–1998. Radiat Res 161:622–632CrossRefGoogle Scholar
  109. Yamada M, Naito K, Kasagi F, Masunari N, Suzuki G (2005) Prevalence of atherosclerosis in relation to atomic bomb radiation exposure: an RERF Adult Health Study. Int J Radiat Biol 81:821–826CrossRefGoogle Scholar
  110. Zoric L, Miric D, Novakovic T, Pavlovic A, Videnovic G, Trajkovic G (2008) Age-related cataract and serum albumin concentration. Curr Eye Res 33:587–590CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg (outside the USA) 2013

Authors and Affiliations

  1. 1.Radiation Epidemiology BranchNational Cancer InstituteBethesdaUSA

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