Advertisement

Mortality analyses in the updated French cohort of uranium miners (1946–2007)

  • E. Rage
  • S. Caër-Lorho
  • D. Drubay
  • S. Ancelet
  • P. Laroche
  • D. Laurier
Original Article

Abstract

Purpose

The objectives are to analyze mortality risks in the extended follow-up of the French uranium miners’ cohort and to examine their potential relation to occupational exposure to ionizing radiation (IR).

Methods

The total cohort includes 5,086 uranium miners employed in the CEA-COGEMA group and followed up from 1946 to 2007. Vital status, causes of death, and cumulative radon exposures were recorded. The post-55 subcohort includes 3,377 miners first employed after 1955, for whom long-lived radionuclides (LLR) and external gamma-ray exposure were also recorded. External mortality analyses were performed by computing standardized mortality ratios (SMR). Excess relative risks (ERRs) due to IR exposures were estimated from Poisson regression models.

Results

The miners included in the total cohort were followed up for 35.4 years and exposed to 36.6 working level months (WLM) on average. There was no evidence of a difference in overall mortality between miners and the general French male population. Miners had a statistically significant excess mortality rate from lung cancer (SMR = 1.34 [95 % CI 1.16–1.53]) and from kidney cancer (SMR = 1.60 [1.03–2.39]). Cumulative radon exposure was significantly associated with lung cancer risk (ERR/100 WLM = 0.71 [0.31–1.30]) and cerebrovascular risk (ERR/100 WLM = 0.41 [0.04–1.03]). In the post-55 subcohort, this excess mortality from lung cancer remained associated with exposure to radon, and also with exposure to LLR and external gamma rays.

Conclusions

The analyses in the extended follow-up strengthen the results previously observed among French uranium miners about their excess risk of mortality and its association with their occupational IR exposure.

Keywords

Occupational cohort Uranium miners Mortality risk Ionizing radiation Radon exposure 

Notes

Acknowledgments

We thank the following from the Bessines sur Gartempe site, for their assistance with data collection from the mines’ archives and their helpfulness: P.C. Guiollard from AREVA-NC, S. Bernhard from Algade, and J.L. Filloux from the Association Interprofessionnelle pour la Santé au Travail (AIST 87). The authors also thank Jo Ann Cahn for her critical reading of the manuscript. This work was partly supported by AREVA-NC in the framework of a bilateral IRSN-AREVA-NC research agreement.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Allodji RS, Leuraud K, Bernhard S, Henry S, Benichou J, Laurier D (2012) Assessment of uncertainty associated with measuring exposure to radon and decay products in the French uranium miners cohort. J Radiol Prot 32(1):85–100. doi: 10.1088/0952-4746/32/1/85 CrossRefGoogle Scholar
  2. Amabile JC, Leuraud K, Vacquier B, Caer-Lorho S, Acker A, Laurier D (2009) Multifactorial study of the risk of lung cancer among French uranium miners: radon, smoking and silicosis. Health Phys 97(6):613–621CrossRefGoogle Scholar
  3. Archer VE (1995) Reversal of the healthy-worker effect. Int J Occup Environ Health 1(1):33–36CrossRefGoogle Scholar
  4. Armitage P (1955) Tests for linear trends in proportions and frequencies. Biometrics 11:375–386CrossRefGoogle Scholar
  5. Azizova TV, Muirhead CR, Druzhinina MB, Grigoryeva ES, Vlasenko EV, Sumina MV, O’Hagan JA, Zhang W, Haylock RG, Hunter N (2010) Cerebrovascular diseases in the cohort of workers first employed at Mayak PA in 1948–1958. Radiat Res 174(6):851–864. doi: 10.1667/rr1928.1 CrossRefGoogle Scholar
  6. Azizova TV, Muirhead CR, Moseeva MB, Grigoryeva ES, Vlasenko EV, Hunter N, Haylock RG, O’Hagan JA (2012) Ischemic heart disease in nuclear workers first employed at the Mayak PA in 1948–1972. Health Phys 103(1):3–14. doi: 10.1097/HP.0b013e3182243a62 CrossRefGoogle Scholar
  7. Baillargeon J (2001) Characteristics of the healthy worker effect. Occup Med 16(2):359–366Google Scholar
  8. Boice J Jr, Cohen S, Mumma MT, Chadda B, Blot WJ (2008) A cohort study of uranium millers and miners of Grants, New Mexico, 1979–2005. J Radiol Prot 28(3):303–325CrossRefGoogle Scholar
  9. Breslow N, Day N (1987) Statistical methods in cancer research. Volume II—the design and analysis of cohort studies. IARC Sci Publ 82:1–406Google Scholar
  10. Cardis E, Vrijheid M, Blettner M, Gilbert E, Hakama M, Hill C, Howe G, Kaldor J, Muirhead CR, Schubauer-Berigan M, Yoshimura T, Bermann F, Cowper G, Fix J, Hacker C, Heinmiller B, Marshall M, Thierry-Chef I, Utterback D, Ahn YO, Amoros E, Ashmore P, Auvinen A, Bae JM, Bernar J, Biau A, Combalot E, Deboodt P, Sacristan AD, Eklöf M, Engels H, Engholm G, Gulis G, Habib RR, Holan K, Hyvonen H, Kerekes A, Kurtinaitis J, Malker H, Martuzzi M, Mastauskas A, Monnet A, Moser M, Pearce MS, Richardson DB, Rodriguez-Artalejo F, Rogel A, Tardy H, Telle-Lamberton M, Turai I, Usel M, Veress K (2007) The 15-country collaborative study of cancer risk among radiation workers in the nuclear industry: estimates of radiation-related cancer risks. Radiat Res 167(4):396–416CrossRefGoogle Scholar
  11. Darby SC, Whitley E, Howe GR, Hutchings SJ, Kusiak RA, Lubin JH, Morrison HI, Tirmarche M, Tomásek L, Radford EP 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):378–384CrossRefGoogle Scholar
  12. Drubay D, Ancelet S, Acker A, Kreuzer M, Laurier D, Rage E (2014a) Kidney cancer mortality and ionizing radiation among French and German uranium miners. Radiat Environ Biophys 53(3):505–513. doi: 10.1007/s00411-014-0547-4 CrossRefGoogle Scholar
  13. Drubay D, Caer-Lorho S, Laroche P, Acker A, Laurier D, Rage E (2014b) 0194 Circulatory system disease mortality among French uranium miners. Occup Environ Med 71(Suppl 1):A24–A25. doi: 10.1136/oemed-2014-102362.76 CrossRefGoogle Scholar
  14. Dufey F, Walsh L, Sogl M, Tschense A, Schnelzer M, Kreuzer M (2013) Radiation dose dependent risk of liver cancer mortality in the German uranium miners cohort 1946–2003. J Radiol Prot 33(1):175–185. doi: 10.1088/0952-4746/33/1/175 CrossRefGoogle Scholar
  15. International Agency for Research on Cancer (IARC) (1988) Monographs on the evaluation of carcinogenic risks to humans: manmade fibres and radon. International Agency for research on Cancer, FranceGoogle Scholar
  16. International Commission in Radiological Protection (2010) Lung cancer risk from radon and progeny and statement on radon. ICRP Publication 115, Ann. ICRP 40(1)Google Scholar
  17. Kreuzer M, Walsh L, Schnelzer M, Tschense A, Grosche B (2008) Radon and risk of extrapulmonary cancers: results of the German uranium miners’ cohort study, 1960–2003. Br J Cancer 99(11):1946–1953CrossRefGoogle Scholar
  18. Kreuzer M, Grosche B, Schnelzer M, Tschense A, Dufey F, Walsh L (2010) Radon and risk of death from cancer and cardiovascular diseases in the German uranium miners cohort study: follow-up 1946–2003. Radiat Environ Biophys 49(2):177–185CrossRefGoogle Scholar
  19. 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(1):37–46. doi: 10.1007/s00411-012-0446-5 CrossRefGoogle Scholar
  20. 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(6):773–785CrossRefGoogle Scholar
  21. 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(8):935–944. doi: 10.1007/s00420-010-0509-3 CrossRefGoogle Scholar
  22. Laurier D, Tirmarche M, Mitton N, Valenty M, Richard P, Poveda S, Gelas JM, Quesne B (2004) An update of cancer mortality among the French cohort of uranium miners: extended follow-up and new source of data for causes of death. Eur J Epidemiol 19(2):139–146CrossRefGoogle Scholar
  23. Leuraud K, Billon S, Bergot D, Tirmarche M, Caër S, Quesne B, Laurier D (2007) Lung cancer risk associated to exposure to radon and smoking in a case-control study of French uranium miners. Health Phys 92(4):371–378CrossRefGoogle Scholar
  24. Leuraud K, Schnelzer M, Tomasek L, Hunter N, Timarche M, Grosche B, Kreuzer M, Laurier D (2011) Radon, smoking and lung cancer risk: results of a joint analysis of three European case–control studies among uranium miners. Radiat Res 176(3):375–387CrossRefGoogle Scholar
  25. Moolgavkar SH, Venzon DJ (1987) A method for computing profile likelihood-based confidence bounds. Ann Stat 15:346–359CrossRefGoogle Scholar
  26. Morrison HI, Villeneuve PJ, Lubin JH, Schaubel DE (1998) Radon-progeny exposure and lung cancer risk in a cohort of Newfoundland fluorspar miners. Radiat Res 150(1):58–65CrossRefGoogle Scholar
  27. National Research Council, Committee on Health Risks of Exposure to Radon. BEIR VI (1999) Health effects of exposure to radon. National Academy Press, Washington DCGoogle Scholar
  28. Nusinovici S, Vacquier B, Leuraud K, Metz-Flamant C, Caër-Lorho S, Acker A, Laurier D (2010) Mortality from circulatory system diseases and low-level radon exposure in the French cohort study of uranium miners, 1946–1999. Scand J Work Environ Health 36(5):373–383CrossRefGoogle Scholar
  29. Preston DL, Lubin JH, Pierce DA, McConney ME (1993) EPICURE user’s guide. Hirosoft International Corp, SeattleGoogle Scholar
  30. 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(4):381–407CrossRefGoogle Scholar
  31. Rage E, Vacquier B, Blanchardon E, Allodji RS, Marsh JW, Caër-Lorho S, Acker A, Laurier D (2012) Risk of lung cancer mortality in relation to lung doses among French uranium miners: follow-up 1956–1999. Radiat Res 177(3):288–297CrossRefGoogle Scholar
  32. 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):818–822CrossRefGoogle Scholar
  33. Rodriguez Artalejo F, Lara SC, de Andres Manzano B, Garcia Ferruelo M, Iglesias Martin L, Calero JR (1997) Occupational exposure to ionising radiation and mortality among workers of the former Spanish Nuclear Energy Board. Occup Environ Med 54(3):202–208CrossRefGoogle Scholar
  34. Samson E, Telle-Lamberton M, Caër-Lorho S, Bard D, Giraud JM, Metz-Flamant C, Neron MO, Quesne B, Acker A, Tirmarche M, Hill C (2011) Cancer mortality among two different populations of French nuclear workers. Int Arch Occup Environ Health 84(6):627–634. doi: 10.1007/s00420-011-0636-5 CrossRefGoogle Scholar
  35. Schnelzer M, Hammer GP, Kreuzer M, Tschense A, Grosche B (2010) Accounting for smoking in the radon-related lung cancer risk among German uranium miners: results of a nested case-control study. Health Phys 98(1):20–28CrossRefGoogle Scholar
  36. Schubauer-Berigan MK, Daniels RD, Pinkerton LE (2009) Radon exposure and mortality among white and American Indian uranium miners: an update of the Colorado Plateau cohort. Am J Epidemiol 169(6):718–730CrossRefGoogle Scholar
  37. Sogl M, Taeger D, Pallapies D, Brüning T, Dufey F, Schnelzer M, Straif K, Walsh L, Kreuzer M (2012) Quantitative relationship between silica exposure and lung cancer mortality in German uranium miners, 1946–2003. Br J Cancer 107(7):1188–1194. doi: 10.1038/bjc.2012.374 CrossRefGoogle Scholar
  38. Sokolnikov ME, Gilbert ES, Preston DL, Ron E, Shilnikova NS, Khokhryakov VV, Vasilenko EK, Koshurnikova NA (2008) Lung, liver and bone cancer mortality in Mayak workers. Int J Cancer 123(4):905–911CrossRefGoogle Scholar
  39. Tarone RE (1982) The use of historical control information in testing for a trend in Poisson means. Biometrics 38:457–462CrossRefGoogle Scholar
  40. Tirmarche M, Raphalen A, Allin F, Chameaud J, Bredon P (1993) Mortality of a cohort of French uranium miners exposed to relatively low radon concentrations. Br J Cancer 67(5):1090–1097CrossRefGoogle Scholar
  41. Tomasek L (2011) Interaction of radon and smoking among Czech uranium miners. Radiat Prot Dosim 145(2–3):238–242CrossRefGoogle Scholar
  42. Tomasek L (2012) Lung cancer mortality among Czech uranium miners-60 years since exposure. J Radiol Prot 32(3):301–314. doi: 10.1088/0952-4746/32/3/301 CrossRefGoogle Scholar
  43. Tomasek L, Darby SC, Swerdlow AJ, Placek V, Kunz E (1993) Radon exposure and cancers other than lung cancer among uranium miners in West Bohemia. Lancet 341(8850):919–923CrossRefGoogle Scholar
  44. Tomasek L, Swerdlow AJ, Darby SC, Placek V, Kunz E (1994) Mortality in uranium miners in west Bohemia: a long-term cohort study. Occup Environ Med 51(5):308–315CrossRefGoogle Scholar
  45. Travis LB, Hauptmann M, Gaul LK, Storm HH, Goldman MB, Nyberg U, Berger E, Janower ML, Hall P, Monson RR, Holm LE, 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(6):691–706CrossRefGoogle Scholar
  46. United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) (2008) Effect of ionizing radiation: UNSCEAR 2006 report, vol I—report to the general assembly, Annex A: Epidemiological studies of radiation and cancer United Nations, New YorkGoogle Scholar
  47. Vacquier B, Caer S, Rogel A, Feurprier M, Tirmarche M, Luccioni C, Quesne B, Acker A, Laurier D (2008) Mortality risk in the French cohort of uranium miners: extended follow-up 1946–1999. Occup Environ Med 65(9):597–604CrossRefGoogle Scholar
  48. Vacquier B, Rage E, Leuraud K, Caër-Lorho S, Houot J, Acker A, Laurier D (2011) The influence of multiple types of occupational exposure to radon, gamma rays and long-lived radionuclides on mortality risk in the French “post-55” sub-cohort of uranium miners: 1956–1999. Radiat Res 176(6):796–806CrossRefGoogle Scholar
  49. Villeneuve PJ, Morrison HI (1997) Coronary heart disease mortality among Newfoundland fluorspar miners. Scand J Work Environ Health 23(3):221–226CrossRefGoogle Scholar
  50. Villeneuve PJ, Morrison HI, Lane R (2007) Radon and lung cancer risk: an extension of the mortality follow-up of the Newfoundland fluorspar cohort. Health Phys 92(2):157–169CrossRefGoogle Scholar
  51. Vrijheid M, Cardis E, Ashmore P, Auvinen A, Bae JM, Engels H, Gilbert E, Gulis G, Habib R, Howe G, Kurtinaitis J, Malker H, Muirhead C, Richardson D, Rodriguez-Artalejo F, Rogel A, Schubauer-Berigan M, Tardy H, Telle-Lamberton M, Usel M, Veress K (2007a) 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(5):1126–1135. doi: 10.1093/ije/dym138 CrossRefGoogle Scholar
  52. Vrijheid M, Cardis E, Blettner M, Gilbert E, Hakama M, Hill C, Howe G, Kaldor J, Muirhead CR, Schubauer-Berigan M, Yoshimura T, Ahn YO, Ashmore P, Auvinen A, Bae JM, Engels H, Gulis G, Habib RR, Hosoda Y, Kurtinaitis J, Malker H, Moser M, Rodriguez-Artalejo F, Rogel A, Tardy H, Telle-Lamberton M, Turai I, Usel M, Veress K (2007b) The 15-country collaborative study of cancer risk among radiation workers in the nuclear industry: design, epidemiological methods and descriptive results. Radiat Res 167(4):361–379CrossRefGoogle Scholar
  53. Walsh L, Dufey F, Tschense A, Schnelzer M, Grosche B, Kreuzer M (2010) Radon and the risk of cancer mortality-internal poisson models for the german uranium miners cohort. Health Phys 99(3):292–300CrossRefGoogle Scholar
  54. Walsh L, Dufey F, Tschense A, Schnelzer M, Sogl M, Kreuzer M (2012) Prostate cancer mortality risk in relation to working underground in the Wismut cohort study of German uranium miners, 1970–2003. BMJ Open 2(3). doi: 10.1136/bmjopen-2012-001002

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • E. Rage
    • 1
  • S. Caër-Lorho
    • 1
  • D. Drubay
    • 1
  • S. Ancelet
    • 1
  • P. Laroche
    • 2
  • D. Laurier
    • 1
  1. 1.Institute for Radiological Protection and Nuclear Safety (IRSN), PRP-HOM, SRBE, LEPIDFontenay-aux-Roses CedexFrance
  2. 2.AREVA, Direction SantéParis La Défense CedexFrance

Personalised recommendations