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Chronic lymphocytic leukemia radiogenicity: a systematic review

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Abstract

Objective

Chronic lymphocytic leukemia (CLL) is generally considered to be non-radiogenic and is excluded from several programs that compensate workers for illnesses resulting from occupational exposures. Questions about whether this exclusion is justified prompted a Congressional mandate to the National Institute for Occupational Safety and Health (NIOSH) to, further, examine the radiogenicity of CLL. This study revisits the question of CLL radiogenicity by examining epidemiologic evidence from occupationally and medically-exposed populations.

Methods

A systematic review of radiation-exposed cohorts was conducted to investigate the association between radiation and CLL. Exploratory power calculations for a pooled occupational study were performed to examine the feasibility of assessing CLL radiogenicity epidemiologically.

Results

There is a bias against reporting CLL results, because of the disease’s presumed non-radiogenicity. In medical cohort studies that provide risk estimates for CLL, risk is elevated, though non-significantly, in almost all studies with more than 15 years average follow-up. The results of occupational studies are less consistent.

Conclusions

Studies with adequate follow-up time and power are needed to better understand CLL radiogenicity. Power analyses show that a pooled study might detect risk on the order of radiation induced non-CLL leukemia, but is unlikely to detect smaller risks.

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References

  1. Ghia P, Caligaris-Cappio F (2006) The origin of B-cell chronic lymphocytic leukemia. Semin Oncol 33(2):150–156

    PubMed  CAS  Google Scholar 

  2. Caporaso N (2006) Chips, candidate genes, and CLL. Blood 108(2):415–416

    CAS  Google Scholar 

  3. Sgambati MT, Linet MS, Devesa SS (2001) Chronic lymphocytic leukemia: epidemiological, familial, and genetic aspects. Marcel Dekker, Cheson BDNew York, pp 33–62

    Google Scholar 

  4. Goldin LR, Pfeiffer RM, Li X, Hemminki K (2004) Familial risk of lymphoproliferative tumors in families of patients with chronic lymphocytic leukemia: results from the Swedish Family-Cancer Database. Blood 104(6):1850–1854

    PubMed  CAS  Google Scholar 

  5. Wiernik PH, Ashwin M, Hu XP, Paietta E, Brown K (2001) Anticipation in familial chronic lymphocytic leukaemia. Br J Haematol 113(2):407–414

    PubMed  CAS  Google Scholar 

  6. Amadori D, Nanni O, Falcini F et al (1995) Chronic lymphocytic leukaemias and non-Hodgkin’s lymphomas by histological type in farming-animal breeding workers: a population case–control study based on job titles. Occup Environ Med 52(6):374–379

    PubMed  CAS  Google Scholar 

  7. Gonzalez CA, Agudo A (1999) Occupational cancer in Spain. Environ Health Perspect 107(Suppl 2):273–277

    PubMed  Google Scholar 

  8. Lee E, Burnett CA, Lalich N, Cameron LL, Sestito JP (2002) Proportionate mortality of crop and livestock farmers in the United States, 1984–1993. Am J Ind Med 42(5):410–420

    PubMed  Google Scholar 

  9. Institute of Medicine of the National Academies of Sciences (2003) Committee to review the health effects in Vietnam Veterans of exposure to herbicides (fourth biennial update). Veterans and agent orange: update 2002. The National Academies Press, Washington, DC, pp 372–377

    Google Scholar 

  10. Preston DL, Kato H, Kopecky K, Fujita S (1987) Studies of the mortality of A-bomb survivors. 8. Cancer mortality, 1950–1982. Radiat Res 111(1):151–178

    PubMed  CAS  Google Scholar 

  11. Boice JD, Blettner M, Kleinerman RA et al (1987) Radiation dose and leukemia risk in patients treated for cancer of the cervix. J Natl Cancer Inst 79(6):1295–1311

    PubMed  Google Scholar 

  12. Darby SC, Doll R, Gill SK, Smith PG (1987) Long term mortality after a single treatment course with X-rays in patients treated for ankylosing spondylitis. Br J Cancer 55(2):179–190

    PubMed  CAS  Google Scholar 

  13. Boice JD, Engholm G, Kleinerman RA et al (1988) Radiation dose and second cancer risk in patients treated for cancer of the cervix. Radiat Res 116(1):3–55

    PubMed  Google Scholar 

  14. National Research Council Committee on the Biological Effects of Ionizing Radiations (1990) Health effects of exposure to low levels of ionizing radiation: BEIR V. National Academy Press, Washington, DC

    Google Scholar 

  15. Guidelines for Determining the Probability of Causation Under the Energy Employees Occupational Illness Compensation Act of 2000; Final Rule. 42 CFR Part 81 (2202)

  16. Radiation Exposure Compensation Act (1990) Public Law no. 101–426 (104 Stat. 925, 42 U.S.C. 2210)

  17. National Institute for Occupational Safety and Health (2005) Report of public meeting to seek input on gaps in chronic lymphocytic leukemia (CLL) radiogenicity research held July 21, 2004. National Institute for Occupational Safety and Health; (NIOSH) 2006-100, Cincinnati, OH

  18. Rozman C, Montserrat E (1995) Chronic lymphocytic leukemia. N Engl J Med 333(16):1052–1057

    PubMed  CAS  Google Scholar 

  19. Gale RP, Foon KA (1987) Biology of chronic lymphocytic leukemia. Semin Hematol 24(4):209–229

    PubMed  CAS  Google Scholar 

  20. Montserrat E , Rozman C (1995) Chronic lymphocytic leukemia: present status. Ann Oncol 6(3):219–235

    PubMed  CAS  Google Scholar 

  21. Egret Siz: Sample Size, Power for Nonlinear Regression [computer program] (1997) Cytel Statistical Software Services, Version 1. Cytel Inc., Cambridge, MA

    Google Scholar 

  22. Land C, Gilbert E, Smith JM et al (2003). Report of the NCI–CDC working group to revise the 1985 NIH radioepidemiological tables. National Institutes of Health; NIH Publication No. 03-5387, Bethesda MD

    Google Scholar 

  23. Centers for Disease Control and Prevention (CDC) CDC Wonder Compressed Mortality Data. Accessed 09/28/2005. Available from: http://www.wonder.cdc.gov

  24. Oscier D, Fegan C, Hillmen P et al (2004) Guidelines on the diagnosis and management of chronic lymphocytic leukaemia. Br J Haematol 125(3):294–317

    PubMed  CAS  Google Scholar 

  25. Schubauer-Berigan MK, Macievic GV, Utterback DF, Tseng C, Flora JT (2005) An epidemiologic study of mortality and radiation-related risk of cancer among workers at the Idaho National Engineering and Environmental Laboratory. National Institute for Occupational Safety and Health; NIOSH publication 2005-131, Cincinnati, OH

    Google Scholar 

  26. Muirhead CR, Goodill AA, Haylock RG et al (1999) Occupational radiation exposure and mortality: second analysis of the National Registry for Radiation Workers. J Radiol Prot 19(1):3–26

    PubMed  CAS  Google Scholar 

  27. Ashmore JP, Krewski D, Zielinski JM, Jiang H, Semenciw R, Band PR (1998) First analysis of mortality and occupational radiation exposure based on the National Dose Registry of Canada. Am J Epidemiol 148(6):564–574

    PubMed  CAS  Google Scholar 

  28. Ivanov VK, Tsyb AF, Gorsky AI et al (1997) Leukaemia and thyroid cancer in emergency workers of the Chernobyl accident: estimation of radiation risks (1986–1995). Radiat Environ Biophys 36(1):9–16

    PubMed  Google Scholar 

  29. National Institute for Occupational Safety and Health (2001) PC-Life Table Analysis System version 1.0d. National Institute for Occupational Safety and Health

  30. Holowaty EJ, Darlington GA, Gajalakshmi CK, Toogood PB, Levin W (1995) Leukemia after irradiation for endometrial cancer in Ontario. Cancer 76(4):644–649

    PubMed  CAS  Google Scholar 

  31. Curtis RE, Boice JD, Stovall M, Flannery JT, Moloney WC (1989) Leukemia risk following radiotherapy for breast cancer. J Clin Oncol 7(1):21–29

    PubMed  CAS  Google Scholar 

  32. Smith PG, Doll R (1982) Mortality among patients with ankylosing spondylitis after a single treatment course with X rays. Br Med J (Clin Res Ed) 284(6314):449–460

    Article  CAS  Google Scholar 

  33. Hall P, Holm LE (1995) Cancer in iodine-131 exposed patients. J Endocrinol Invest 18(2):147–149

    PubMed  CAS  Google Scholar 

  34. Kleinerman RA, Liebermann JV, Li FP (1985) Second cancer following cancer of the male genital system in Connecticut, 1935–82. Natl Cancer Inst Monogr 68:139–147

    PubMed  CAS  Google Scholar 

  35. Shilnikova NS, Preston DL, Ron E et al (2003) Cancer mortality risk among workers at the Mayak nuclear complex. Radiat Res 159(6):787–798

    PubMed  CAS  Google Scholar 

  36. Gilbert ES, Omohundro E, Buchanan JA, Holter NA (1993) Mortality of workers at the Hanford site: 1945–1986. Health Phys 64(6):577–590

    Article  PubMed  CAS  Google Scholar 

  37. Thaul S, Page WF, Crawford H, O’Maonaigh H (2005). The five series study: mortality of military participants in US nuclear weapons tests. National Academy Press, Washington, DC

    Google Scholar 

  38. Silver SR, Daniels RD, Taulbee TD et al (2004) Differences in mortality by radiation monitoring status in an expanded cohort of Portsmouth Naval Shipyard workers. J Occup Environ Med 46(7):677–690

    PubMed  Google Scholar 

  39. Frome EL, Cragle DL, Watkins JP et al (1997) A mortality study of employees of the nuclear industry in Oak Ridge, Tennessee. Radiat Res 148(1):64–80

    PubMed  CAS  Google Scholar 

  40. Telle-Lamberton M, Bergot D, Gagneau M et al (2004) Cancer mortality among French Atomic Energy Commission workers. Am J Ind Med 45(1):34–44

    PubMed  CAS  Google Scholar 

  41. Mohan AK, Hauptmann M, Freedman DM et al (2003) Cancer and other causes of mortality among radiologic technologists in the United States. Int J Cancer 103(2):259–267

    PubMed  CAS  Google Scholar 

  42. Hall P, Berg G, Bjelkengren G et al (1992) Cancer mortality after iodine-131 therapy for hyperthyroidism. Int J Cancer 50(6):886–890

    PubMed  CAS  Google Scholar 

  43. Darby SC, Reeves G, Key T, Doll R, Stovall M (1994) Mortality in a cohort of women given X-ray therapy for metropathia haemorrhagica. Int J Cancer 56(6):793–801

    PubMed  CAS  Google Scholar 

  44. Blettner M, Zeeb H, Langner I, Hammer GP, Schafft T (2002) Mortality from cancer and other causes among airline cabin attendants in Germany, 1960–1997. Am J Epidemiol 156(6):556–565

    PubMed  Google Scholar 

  45. Zeeb H, Blettner M, Hammer GP, Langner I (2002) Cohort mortality study of German cockpit crew, 1960–1997. Epidemiology 13(6):693–699

    PubMed  Google Scholar 

  46. Movsas B, Hanlon AL, Pinover W, Hanks GE (1998) Is there an increased risk of second primaries following prostate irradiation? Int J Radiat Oncol Biol Phys 41(2):251–255

    PubMed  CAS  Google Scholar 

  47. Brenner DJ, Curtis RE, Hall EJ, Ron E (2000) Second malignancies in prostate carcinoma patients after radiotherapy compared with surgery. Cancer 88(2):398–406

    PubMed  CAS  Google Scholar 

  48. Bokemeyer C, Schmoll HJ (1993) Secondary neoplasms following treatment of malignant germ cell tumors. J Clin Oncol 11(9):1703–1709

    PubMed  CAS  Google Scholar 

  49. Travis LB, Boice JD, Travis WD (2003) Second primary cancers after thymoma. Int J Cancer 107(5):868–870

    PubMed  CAS  Google Scholar 

  50. Lavey RS, Eby NL, Prosnitz LR (1990) Impact of radiation therapy and/or chemotherapy on the risk for a second malignancy after breast cancer. Cancer 66(5):874–881

    PubMed  CAS  Google Scholar 

  51. Boice JD, Day NE, Andersen A et al (1985) Second cancers following radiation treatment for cervical cancer. An international collaboration among cancer registries. J Natl Cancer Inst 74(5):955–975

    PubMed  Google Scholar 

  52. Osterlind A, Rorth M, Prener A (1985) Second cancer following cancer of the male genital system in Denmark, 1943–80. Natl Cancer Inst Monogr 68:341–347

    PubMed  CAS  Google Scholar 

  53. Redman JR, Vugrin D, Arlin ZA et al (1984) Leukemia following treatment of germ cell tumors in men. J Clin Oncol 2(10):1080–1087

    PubMed  CAS  Google Scholar 

  54. Horwich A, Bell J (1994) Mortality and cancer incidence following radiotherapy for seminoma of the testis. Radiother Oncol 30(3):193–198

    PubMed  CAS  Google Scholar 

  55. Kleinerman RA, Boice JD, Storm HH et al (1995) Second primary cancer after treatment for cervical cancer. An international cancer registries study. Cancer 76(3):442–452

    PubMed  CAS  Google Scholar 

  56. Fossa SD, Langmark F, Aass N, Andersen A, Lothe R, Borresen AL (1990) Second non-germ cell malignancies after radiotherapy of testicular cancer with or without chemotherapy. Br J Cancer 61(4):639–643

    PubMed  CAS  Google Scholar 

  57. Weiss HA, Darby SC, Fearn T, Doll R (1995) Leukemia mortality after X-ray treatment for ankylosing spondylitis. Radiat Res 142(1):1–11

    PubMed  CAS  Google Scholar 

  58. Wick RR, Nekolla EA, Gossner W, Kellerer AM (1999) Late effects in ankylosing spondylitis patients treated with 224Ra. Radiat Res 152(6 Suppl):S8–S11

    PubMed  CAS  Google Scholar 

  59. Inskip PD, Kleinerman RA, Stovall M et al (1993) Leukemia, lymphoma, and multiple myeloma after pelvic radiotherapy for benign disease. Radiat Res 135(1):108–124

    PubMed  CAS  Google Scholar 

  60. Davis FG, Boice JD, Hrubec Z, Monson RR (1989) Cancer mortality in a radiation-exposed cohort of Massachusetts tuberculosis patients. Cancer Res 49(21):6130–6136

    PubMed  CAS  Google Scholar 

  61. Ryberg M, Lundell M, Nilsson B, Pettersson F (1990) Malignant disease after radiation treatment of benign gynaecological disorders. A study of a cohort of metropathia patients. Acta Oncol 29(5):563–567

    PubMed  CAS  Google Scholar 

  62. Moller H, Mellemgaard A, Jacobsen GK, Pedersen D, Storm HH (1993) Incidence of second primary cancer following testicular cancer. Eur J Cancer 29A(5):672–676

    PubMed  CAS  Google Scholar 

  63. Hellbardt A, Mirimanoff RO, Obradovic M, Mermillod B, Paunier JP (1990) The risk of second cancer (SC) in patients treated for testicular seminoma. Int J Radiat Oncol Biol Phys 18(6):1327–1331

    PubMed  CAS  Google Scholar 

  64. Hay JH, Duncan W, Kerr GR (1984) Subsequent malignancies in patients irradiated for testicular tumours. Br J Radiol 57(679):597–602

    Article  PubMed  CAS  Google Scholar 

  65. Damber L, Larsson LG, Johansson L, Norin T (1995) A cohort study with regard to the risk of haematological malignancies in patients treated with X-rays for benign lesions in the locomotor system. I. Epidemiological analyses. Acta Oncol 34(6):713–719

    PubMed  CAS  Google Scholar 

  66. Storm HH (1988) Second primary cancer after treatment for cervical cancer. Late effects after radiotherapy. Cancer 61(4):679–688

    PubMed  CAS  Google Scholar 

  67. Dent SF, Klaassen D, Pater JL, Zee B, Whitehead M (2000) Second primary malignancies following the treatment of early stage ovarian cancer: update of a study by the National Cancer Institute of Canada—Clinical Trials Group (NCIC-CTG). Ann Oncol 11(1):65–68

    PubMed  CAS  Google Scholar 

  68. Harvey EB, Brinton LA (1985) Second cancer following cancer of the breast in Connecticut, 1935–82. Natl Cancer Inst Monogr 68:99–112

    PubMed  CAS  Google Scholar 

  69. Travis LB, Curtis RE, Boice JD, Platz CE, Hankey BF, Fraumeni JF (1996) Second malignant neoplasms among long-term survivors of ovarian cancer. Cancer Res 56(7):1564–1570

    PubMed  CAS  Google Scholar 

  70. Travis LB, Curtis RE, Storm H et al (1997) Risk of second malignant neoplasms among long-term survivors of testicular cancer. J Natl Cancer Inst 89(19):1429–1439

    PubMed  CAS  Google Scholar 

  71. Volk N, Pompe-Kirn V (1997) Second primary cancers in breast cancer patients in Slovenia. Cancer Causes Control 8(5):764–770

    PubMed  CAS  Google Scholar 

  72. Curtis RE, Hoover RN, Kleinerman RA, Harvey EB (1985) Second cancer following cancer of the female genital system in Connecticut, 1935–82. Natl Cancer Inst Monogr 68:113–137

    PubMed  CAS  Google Scholar 

  73. Curtis RE, Boice JD, Stovall M et al (1994) Relationship of leukemia risk to radiation dose following cancer of the uterine corpus. J Natl Cancer Inst 86(17):1315–1324

    PubMed  CAS  Google Scholar 

  74. Boice JD, Morin MM, Glass AG et al (1991) Diagnostic X-ray procedures and risk of leukemia, lymphoma, and multiple myeloma. JAMA 265(10):1290–1294

    PubMed  Google Scholar 

  75. Gibson R, Graham S, Lilienfeld A, Schuman L, Dowd JE, Levin ML (1972) Irradiation in the epidemiology of leukemia among adults. J Natl Cancer Inst 48(2):301–311

    PubMed  CAS  Google Scholar 

  76. Boivin JF, Hutchison GB, Evans FB, Abou-Daoud KT, Junod B (1986) Leukemia after radiotherapy for first primary cancers of various anatomic sites. Am J Epidemiol 123(6):993–1003

    PubMed  CAS  Google Scholar 

  77. Travis LB, Hauptmann M, Gaul LK et al (2003) Site-specific cancer incidence and mortality after cerebral angiography with radioactive Thorotrast. Radiat Res 160(6):691–706

    PubMed  CAS  Google Scholar 

  78. van Kaick G, Dalheimer A, Hornik S et al (1999) The German Thorotrast study: recent results and assessment of risks. Radiat Res 152(6 Suppl):S64–S71

    PubMed  Google Scholar 

  79. Andersson M, Carstensen B, Storm HH (1995) Mortality and cancer incidence after cerebral arteriography with or without Thorotrast. Radiat Res 142(3):305–320

    PubMed  CAS  Google Scholar 

  80. 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(4):521–534

    PubMed  CAS  Google Scholar 

  81. Ron E, Doody MM, Becker DV et al (1998) Cancer mortality following treatment for adult hyperthyroidism. Cooperative Thyrotoxicosis Therapy Follow-up Study Group. JAMA 280(4):347–355

    PubMed  CAS  Google Scholar 

  82. de Vathaire F, Schlumberger M, Delisle MJ et al (1997) Leukaemias and cancers following iodine-131 administration for thyroid cancer. Br J Cancer 75(5):734–739

    PubMed  Google Scholar 

  83. Dottorini ME, Lomuscio G, Mazzucchelli L, Vignati A, Colombo L (1995) Assessment of female fertility and carcinogenesis after iodine-131 therapy for differentiated thyroid carcinoma. J Nucl Med 36(1):21–27

    PubMed  CAS  Google Scholar 

  84. Brincker H, Hansen HS, Andersen AP (1973) Induction of leukemia by 131-I treatment of thyroid carcinoma. Br J Cancer 28(3):232–237

    PubMed  CAS  Google Scholar 

  85. Cardis E, Gilbert ES, Carpenter L et al (1995) Effects of low doses and low dose rates of external ionizing radiation: cancer mortality among nuclear industry workers in three countries. Radiat Res 142(2):117–132

    PubMed  CAS  Google Scholar 

  86. Cardis E, Vrijheid M, Blettner M et al (2005) Risk of cancer after low doses of ionising radiation: retrospective cohort study in 15 countries. BMJ 331(7508):77

    PubMed  CAS  Google Scholar 

  87. Sont WN, Zielinski JM, Ashmore JP et al (2001) First analysis of cancer incidence and occupational radiation exposure based on the National Dose Registry of Canada. Am J Epidemiol 153(4):309–318

    PubMed  CAS  Google Scholar 

  88. Zablotska LB, Ashmore JP, Howe GR (2004) Analysis of mortality among Canadian nuclear power industry workers after chronic low-dose exposure to ionizing radiation. Radiat Res 161(6):633–641

    PubMed  CAS  Google Scholar 

  89. Howe GR, Zablotska LB, Fix JJ, Egel J, Buchanan J (2004) Analysis of the mortality experience amongst U.S. nuclear power industry workers after chronic low-dose exposure to ionizing radiation. Radiat Res 162(5):517–526

    PubMed  CAS  Google Scholar 

  90. McGeoghegan D, Binks K (2000) The mortality and cancer morbidity experience of workers at the Springfields uranium production facility, 1946–95. J Radiol Prot 20(2):111–137

    PubMed  CAS  Google Scholar 

  91. Kubale TL, Daniels RD, Yiin JH et al (2005) A nested case–control study of leukemia mortality and ionizing radiation at the Portsmouth Naval Shipyard. Radiat Res 164(6):810–819

    PubMed  CAS  Google Scholar 

  92. Konogorov AP , Ivanov VK, Chekin SY, Khait SE (2000) A case–control analysis of leukemia in accident emergency workers of Chernobyl. J Environ Pathol Toxicol Oncol 19(1–2):143–151

    PubMed  CAS  Google Scholar 

  93. Wiggs LD, Cox-DeVore CA, Wilkinson GS, Reyes M (1991) Mortality among workers exposed to external ionizing radiation at a nuclear facility in Ohio. J Occup Med 33(5):632–637

    PubMed  CAS  Google Scholar 

  94. Wiggs LD, Johnson ER, Cox-DeVore CA, Voelz GL (1994) Mortality through 1990 among white male workers at the Los Alamos National Laboratory: considering exposures to plutonium and external ionizing radiation. Health Phys 67(6):577–588

    Article  PubMed  CAS  Google Scholar 

  95. Atkinson WD, Law DV, Bromley KJ, Inskip HM (2004) Mortality of employees of the United Kingdom Atomic Energy Authority, 1946–97. Occup Environ Med 61(7):577–585

    PubMed  CAS  Google Scholar 

  96. 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(7–8):1288–1301

    PubMed  CAS  Google Scholar 

  97. Wartenberg D, Brown S, Mohr S, Cragle D, Friedlander B (2001) Are African-American nuclear workers at lower mortality risk than Caucasians? J Occup Environ Med 43(10):861–871

    PubMed  CAS  Google Scholar 

  98. Hadjimichael OC, Ostfeld AM, D’Atri DA, Brubaker RE (1983) Mortality and cancer incidence experience of employees in a nuclear fuels fabrication plant. J Occup Med 25(1):48–61

    PubMed  CAS  Google Scholar 

  99. Koshurnikova NA, Buldakov LA, Bysogolov GD, Bolotnikova MG, Komleva NS, Peternikova VS (1994) Mortality from malignancies of the hematopoietic and lymphatic tissues among personnel of the first nuclear plant in the USSR. Sci Total Environ 142(1–2):19–23

    PubMed  CAS  Google Scholar 

  100. Boice JD, Holm LE (1997) Radiation risk estimates for leukemia and thyroid cancer among Russian emergency workers at Chernobyl. Radiat Environ Biophys 36(3):213–214

    PubMed  Google Scholar 

  101. Rahu M, Tekkel M, Veidebaum T et al (1997) The Estonian study of Chernobyl cleanup workers: II. Incidence of cancer and mortality. Radiat Res 147(5):653–657

    PubMed  CAS  Google Scholar 

  102. Hatch M, Ron E, Bouville A, Zablotska L, Howe G (2005) The Chernobyl disaster: cancer following the accident at the Chernobyl nuclear power plant. Epidemiol Rev 27:56–66

    PubMed  CAS  Google Scholar 

  103. Darby SC, Whitley E, Howe GR et al (1995) Radon and cancers other than lung cancer in underground miners: a collaborative analysis of 11 studies. J Natl Cancer Inst 87(5):378–384

    PubMed  CAS  Google Scholar 

  104. Rericha V, Kulich M, Rericha R, Shore DL, Sandler DP (2006) Incidence of leukemia, lymphoma, and multiple myeloma in Czech uranium miners: a case-cohort study. Environ Health Perspect 114(6):818–822

    Article  PubMed  CAS  Google Scholar 

  105. Smith PG, Doll R (1981) Mortality from cancer and all causes among British radiologists. Br J Radiol 54(639):187–194

    PubMed  CAS  Google Scholar 

  106. Doody MM, Mandel JS, Lubin JH, Boice JD (1998) Mortality among United States radiologic technologists, 1926–90. Cancer Causes Control 9(1):67–75

    PubMed  CAS  Google Scholar 

  107. Sigurdson AJ, Doody MM, Rao RS et al (2003) Cancer incidence in the US radiologic technologists health study, 1983–1998. Cancer 97(12):3080–3089

    PubMed  Google Scholar 

  108. Linet MS, Freedman DM, Mohan AK et al (2005) Incidence of haematopoietic malignancies in US radiologic technologists. Occup Environ Med 62(12):861–867

    PubMed  CAS  Google Scholar 

  109. Pukkala E, Aspholm R, Auvinen A et al (2003) Cancer incidence among 10,211 airline pilots: a Nordic study. Aviat Space Environ Med 74(7):699–706

    PubMed  Google Scholar 

  110. Langner I, Blettner M, Gundestrup M et al (2004) Cosmic radiation and cancer mortality among airline pilots: results from a European cohort study (ESCAPE). Radiat Environ Biophys 42(4):247–256

    PubMed  CAS  Google Scholar 

  111. Muirhead CR , Bingham D, Haylock RG et al (2003) Follow up of mortality and incidence of cancer 1952–98 in men from the UK who participated in the UK’s atmospheric nuclear weapon tests and experimental programmes. Occup Environ Med 60(3):165–172

    PubMed  CAS  Google Scholar 

  112. Muirhead CR, Bingham D, Haylock RG et al (2003). Mortality and cancer incidence 1952–1998 in UK participants in the UK atmospheric nuclear weapon tests and experimental programmes. National Radiological Protection Board; NRPB-W27, Didcot Oxfordshire

    Google Scholar 

  113. Richardson DB, Wing S, Schroeder J, Schmitz-Feuerhake I, Hoffmann W (2005) Ionizing radiation and chronic lymphocytic leukemia. Environ Health Perspect 113(1):1–5

    PubMed  CAS  Google Scholar 

  114. Dyagil I, Adam M, Beebe GW et al (2002) Histologic verification of leukemia, myelodysplasia, and multiple myeloma diagnoses in patients in Ukraine, 1987–1998. Int J Hematol 76(1):55–60

    PubMed  Google Scholar 

  115. Finch SC, Linet MS (1992) Chronic leukaemias. Baillieres Clin Haematol 5(1):27–56

    PubMed  CAS  Google Scholar 

  116. Romanov SA, Vasilenko EK, Khokhryakov VF, Jacob P (2002) Studies on the Mayak nuclear workers: dosimetry. Radiat Environ Biophys 41(1):23–28

    PubMed  CAS  Google Scholar 

  117. Kisselev M, Kellerer AM (2002) The potential for studies in other nuclear installations. On the possibility of creating medico-dosimetry registries of workers at the Siberian Chemical Industrial Complex (SCIC) and the Mountain Chemical Industrial Complex (MCIC) in Tomsk, Krasnoyarsk. Radiat Environ Biophys 41(1):81–83

    PubMed  CAS  Google Scholar 

  118. Carpenter LM, Higgins CD, Douglas AJ et al (1998) Cancer mortality in relation to monitoring for radionuclide exposure in three UK nuclear industry workforces. Br J Cancer 78(9):1224–1232

    PubMed  CAS  Google Scholar 

  119. Wiggs LD, Cox-DeVore CA, Voelz GL (1991) Mortality among a cohort of workers monitored for 210Po exposure: 1944–1972. Health Phys 61(1):71–76

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

Funding for this study was provided through an agreement between the U.S. Department of Energy (DOE) and the U.S. Department of Health and Human Services (DHHS). Required disclaimer - The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the National Institute for Occupational Safety and Health.

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Correspondence to Sharon R. Silver.

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Silver, S.R., Hiratzka, S.L., Schubauer-Berigan, M.K. et al. Chronic lymphocytic leukemia radiogenicity: a systematic review. Cancer Causes Control 18, 1077–1093 (2007). https://doi.org/10.1007/s10552-007-9048-y

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