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External radiation dose and cancer mortality among French nuclear workers: considering potential confounding by internal radiation exposure

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Abstract

Objectives

French nuclear workers have detailed records of their occupational exposure to external radiation that have been used to examine associations with subsequent cancer mortality. However, some workers were also exposed to internal contamination by radionuclides. This study aims to assess the potential for bias due to confounding by internal contamination of estimates of associations between external radiation exposure and cancer mortality.

Methods

A cohort of 59,004 workers employed for at least 1 year between 1950 and 1994 by CEA (Commissariat à l’Energie Atomique), AREVA NC, or EDF (Electricité de France) and badge-monitored for external radiation exposure were followed through 2004 to assess vital status and cause of death. A flag based on a workstation–exposure matrix defined four levels of potential for internal contamination. Standardized mortality ratios were assessed for each level of the internal contamination indicator. Poisson regression was used to quantify associations between external radiation exposure and cancer mortality, adjusting for potential internal contamination.

Results

For solid cancer, the mortality deficit tended to decrease as the levels of potential for internal contamination increased. For solid cancer and leukemia excluding chronic lymphocytic leukemia, adjusting the dose–response analysis on the internal contamination indicator did not markedly change the excess relative risk per Sievert of external radiation dose.

Conclusions

This study suggests that in this cohort, neglecting information on internal dosimetry while studying the association between external dose and cancer mortality does not generate a substantial bias. To investigate more specifically the health effects of internal contamination, an effort is underway to estimate organ doses due to internal contamination.

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References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723

    Article  Google Scholar 

  • Arrighi HM, Hertz-Picciotto I (1994) The evolving concept of the healthy worker survivor effect. Epidemiology 5:189–196

    Article  CAS  Google Scholar 

  • Blanchardon E, Flüry-Herard A, Paquet F (2007) Les méthodes et les limites de la dosimétrie après contamination interne. Radioprotection 42:501–517

    Article  CAS  Google Scholar 

  • Boice JD, Cohen SS, Mumma MT, Ellis ED, Cragle DL, Eckerman KF, Wallace PW, Chadda B, Sonderman JS, Wiggs LD, Richter BS, Leggett RW (2014) Mortality among mound workers exposed to Polonium-210 and other sources of radiation, 1944–1979. Radiat Res 181:208–228. doi:10.1667/RR13395.1

    Article  CAS  Google Scholar 

  • Breslow NE, Day NE (1987) Statistical methods in cancer research. International Agency for Research on Cancer, Lyon

    Google Scholar 

  • 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 Y-O, Amoros E, Ashmore P, Auvinen A, Bae J-M, Solano JB, Biau A, Combalot E, Deboodt P, Sacristan AD, Eklof M, Engels H, Engholm G, Gulis G, Habib R, 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 (2005) Risk of cancer after low doses of ionising radiation: retrospective cohort study in 15 countries. Br Med J 331:77. doi:10.1136/bmj.38499.599861.E0

    Article  CAS  Google Scholar 

  • Cardis E, Vrijheid M, Blettner M, Gilbert E, Hakama M, Hill C, Howe G, Kaldor J, Muirhead C, Schubauer-Berigan M et al (2007) The 15-country collaborative study of cancer risk among radiation workers in the nuclear industry: estimates of radiation-related cancer risks. Radiat Res 167:396–416

    Article  CAS  Google Scholar 

  • Douple EB, Mabuchi K, Cullings HM, Preston DL, Kodama K, Shimizu Y, Fujiwara S, Shore RE (2011) Long-term radiation-related health effects in a unique human population: lessons learned from the atomic bomb survivors of Hiroshima and Nagasaki. Disaster Med Public Health Prep 5:S122–S133. doi:10.1001/dmp.2011.21

    Article  Google Scholar 

  • Eisen EA, Robins JM (2005) Healthy worker effect. In: Armitage P, Colton T (ed) Encyclopedia of biostatistics. Wiley, USA

  • Gilbert E, Sokolnikov M, Preston D, Schonfeld S, Schadilov A, Vasilenko E, Koshurnikova N (2013) Lung cancer risks from plutonium: an updated analysis of data from the Mayak worker cohort. Radiat Res 179:332–342

    Article  CAS  Google Scholar 

  • Goldsmith JR (1975) What do we expect from an occupational cohort. J Occup Environ Med 17:126–128

    Article  CAS  Google Scholar 

  • Hammer GP, Fehringer F, Seitz G, Zeeb H, Dulon M, Langner I, Blettner M (2007) Exposure and mortality in a cohort of German nuclear power workers. Radiat Environ Biophys 47:95–99. doi:10.1007/s00411-007-0134-z

    Article  Google Scholar 

  • Hsu WL, Preston DL, Soda M, Sugiyama H, Funamoto S, Kodama K, Kimura A, Kamada N, Dohy H, Tomonaga M, Iwanaga M, Miyazaki Y, Cullings HM, Suyama A, Ozasa K, Shore RE, Mabuchi K (2013) The incidence of leukemia, lymphoma and multiple myeloma among atomic bomb survivors: 1950–2001. Radiat Res 179:361–382. doi:10.1667/RR2892.1

    Article  CAS  Google Scholar 

  • ICRP (2007) The 2007 recommendations of the international commission on radiological protection. Annals of the ICRP, Elsevier, Amsterdam

    Google Scholar 

  • 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 83:935–944

    Article  CAS  Google Scholar 

  • Li C-Y, Sung F-C (1999) A review of the healthy worker effect in occupational epidemiology. Occup Med 49:225–229. doi:10.1093/occmed/49.4.225

    Article  CAS  Google Scholar 

  • McMichael AJ (1976) Standardized mortality ratios and the ‘Healthy Worker Effect’: scratching beneath the surface. J Occup Environ Med 18:165–168

    Article  CAS  Google Scholar 

  • Merzenich H, Hammer GP, Tröltzsch K, Ruecker K, Buncke J, Fehringer F, Blettner M (2014) Mortality risk in a historical cohort of nuclear power plant workers in Germany: results from a second follow-up. Radiat Environ Biophys 53:405–416

    Article  Google Scholar 

  • Metz-Flamant C, Samson E, Caër-Lorho S, Acker A, Laurier D (2011) Solid cancer mortality associated with chronic external radiation exposure at the French atomic energy commission and nuclear fuel company. Radiat Res 176:115–127

    Article  CAS  Google Scholar 

  • Metz-Flamant C, Samson E, Caër-Lorho S, Acker A, Laurier D (2012) Leukemia risk associated with chronic external exposure to ionizing radiation in a French cohort of nuclear workers. Radiat Res 178:489–498

    Article  CAS  Google Scholar 

  • Metz-Flamant C, Laurent O, Samson E, Caër-Lorho S, Acker A, Hubert D, Richardson D, Laurier D (2013) Mortality associated with chronic external radiation exposure in the French combined cohort of nuclear workers. Occup Environ Med 70:630–638

    Article  CAS  Google Scholar 

  • Monson RR (1986) Observations on the healthy worker effect. J Occup Environ Med 28:425–433

    Article  CAS  Google Scholar 

  • Muirhead C, O’Hagan J, Haylock R, Phillipson M, Willcock T, Berridge G, Zhang W (2009a) Third analysis of the national registry for radiation workers: occupational exposure to ionising radiation in relation to mortality and cancer incidence. Health Protection Agency, Radiation Protection Division, London

    Google Scholar 

  • Muirhead CR, O’Hagan JA, Haylock RGE, Phillipson MA, Willcock T, Berridge GLC, Zhang W (2009b) Mortality and cancer incidence following occupational radiation exposure: third analysis of the National Registry for Radiation Workers. Br J Cancer 100:206–212. doi:10.1038/sj.bjc.6604825

    Article  CAS  Google Scholar 

  • National Research Council, Committee to Asses Health Risks from Exposure to Low Level of Ionizing Radiations (2006) Health risks from exposure to low levels of ionizing radiation: BEIR VII phase 2. The national academies press, Washington

  • 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 177:229–243. doi:10.1667/RR2629.1

    Article  CAS  Google Scholar 

  • Preston DL, Lubin JH, Pierce DA, McConney ME (1993) Epicure user’s guide. Hirosoft International, Seattle

  • Preston DL, Kusumi S, Tomonaga M, Izumi S, Ron E, Kuramoto A, Kamada N, Dohy H, Matsui T, Nonaka H et al (1994) Cancer incidence in atomic bomb survivors. Part III: leukemia, lymphoma and multiple myeloma, 1950–1987. Radiat Res 137:S68–S97

    Article  CAS  Google Scholar 

  • Preston D, Ron E, Tokuoka S, Funamoto S, Nishi N, Soda M, Mabuchi K, Kodama K (2007) Solid cancer incidence in atomic bomb survivors: 1958-1998. Radiat Res 168:1–64

    Article  CAS  Google Scholar 

  • Richardson DB (2010) Occupational exposures and lung cancer: adjustment for unmeasured confounding by smoking. Epidemiology 21:181–186. doi:10.1097/EDE.0b013e3181c6f7d9

    Article  Google Scholar 

  • Rogel A, Carré N, Amoros E, Bonnet-Belfais M, Goldberg M, Imbernon E, Calvez T, Hill C (2005) Mortality of workers exposed to ionizing radiation at the French National Electricity Company. Am J Ind Med 47:72–82

    Article  Google Scholar 

  • Rogel A, Joly K, Metz-Flamant C, Laurent O, Tirmarche M, Hubert D, Garcier Y, Laurier D (2009) Cohorte des travailleurs du nucléaire à Électricité de France: mortalité des agents statutaires sur la période 1968–2003. Rev Epidemiol Sante Publique 57:257–265

    Article  CAS  Google Scholar 

  • Samson E, Telle-Lamberton M, Caër-Lorho S, Bard D, Giraud J-M, Metz-Flamant C, Neron M-O, Quesne B, Acker A, Tirmarche M et al (2011) Cancer mortality among two different populations of French nuclear workers. Int Arch Occup Environ Health 84:627–634

    Article  Google Scholar 

  • Samson E, Piot I, Zhivin S, Richardson DB, Laroche P, Serond A-P, Laurier D, Laurent O (2016) Cancer and non-cancer mortality among French uranium cycle workers: the TRACY cohort. BMJ Open 6:e010316. doi:10.1136/bmjopen-2015-010316

    Article  Google Scholar 

  • Shilnikova NS, Preston DL, Ron E, Gilbert ES, Vassilenko EK, Romanov SA, Kuznetsova IS, Sokolnikov ME, Okatenko PV, Kreslov VV, Koshurnikova NA (2003) Cancer mortality risk among workers at the Mayak nuclear complex. Radiat Res 159(6):787–798

    Article  CAS  Google Scholar 

  • Silver SR, Bertke SJ, Hein MJ, Daniels RD, Fleming DA, Anderson JL, Pinney SM, Hornung RW, Tseng C-Y (2013) Mortality and ionising radiation exposures among workers employed at the Fernald Feed Materials Production Center (1951–1985). Occup Environ Med. doi:10.1136/oemed-2012-100768

    Google Scholar 

  • Telle-Lamberton M, Samson E, Caër S, Bergot D, Bard D, Bermann F, MGélas J, Giraud J-M, Hubert P, Metz-Flamant C et al (2007) External radiation exposure and mortality in a cohort of French nuclear workers. Occup Environ Med 64:694–700

    Article  CAS  Google Scholar 

  • Thierry-Chef I, Pernicka F, Marshall M, Cardis E, Andreo P (2002) Study of a selection of 10 historical types of dosemeter: variation of the response to Hp (10) with photon energy and geometry of exposure. Radiat Prot Dosim 102:101–113

    Article  CAS  Google Scholar 

  • Thierry-Chef I, Marshall M, Fix JJ, Bermann F, Gilbert ES, Hacker C, Heinmiller B, Murray W, Pearce MS, Utterback D, Bernar K, Deboodt P, Eklof M, Griciene B, Holan K, Hyvonen H, Kerekes A, Lee M-C, Moser M, Pernicka F, Cardis E (2007) The 15-country collaborative study of cancer risk among radiation workers in the nuclear industry: study of errors in dosimetry. Radiat Res 167:380–395. doi:10.1667/RR0552.1

    Article  CAS  Google Scholar 

  • Vrijheid M, Cardis E, Blettner M, Gilbert E, Hakama M, Hill C, Howe G, Kaldor J, Muirhead CR, Schubauer-Berigan M, Yoshimura T, Ahn Y-O, Ashmore P, Auvinen A, Bae J-M, 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 (2007) The 15-country collaborative study of cancer risk among radiation workers in the nuclear industry: design, epidemiological methods and descriptive results. Radiat Res 167:361–379. doi:10.1667/RR0554.1

    Article  CAS  Google Scholar 

  • Wilcosky T, Wing S (1987) The healthy worker effect: selection of workers and work forces. Scand J Work Environ Health 13:70–72

    Article  CAS  Google Scholar 

  • World Health Organization (1967) International classification of disease: manual of the international statistical classification of diseases, injuries, and causes of death. World Health Organization, Geneva

    Google Scholar 

  • World Health Organization (1977) International classification of diseases, injuries and causes of death. World Health Organization, Geneva

    Google Scholar 

  • World Health Organization (2004) International statistical classification of diseases and health related problems (The) ICD-10. World Health Organization, Geneva

    Google Scholar 

  • Zhivin S, Laurier D, Guseva Canu I (2014) Health effects of occupational exposure to uranium: do physicochemical properties matter? Int J Radiat Biol 90:1104–1113. doi:10.3109/09553002.2014.943849

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank Dr DB Richardson from the University of North Carolina for his helpful and constructive comments that contributed to improving the final version of the manuscript and Irwin Piot for his work updating the internal contamination indicator.

Funding

The construction of the French cohort was realized by the Institut de Radioprotection et de Sûreté Nucléaire, with partial funding from AREVA and Electricité de France. The Institut de Radioprotection et de Sûreté Nucléaire thanks all persons from the Commissariat à l’énergie atomique et aux énergies alternatives, AREVA, and Electricité de France who cooperated in the elaboration of the French cohort.

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Correspondence to L. Fournier.

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Conflict of interest

The authors declare that they have no conflict of interest. P. Laroche and B. Le Guen are employed by AREVA and EDF, respectively. They have provided access to data sources needed for the construction of the cohort. They had no role in the study design analysis or interpretation of results or the writing of the paper.

Ethics approval

The Commission Nationale de l’Informatique et des Libertés (CNIL) approved this study.

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Fournier, L., Laurent, O., Samson, E. et al. External radiation dose and cancer mortality among French nuclear workers: considering potential confounding by internal radiation exposure. Int Arch Occup Environ Health 89, 1183–1191 (2016). https://doi.org/10.1007/s00420-016-1152-4

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  • DOI: https://doi.org/10.1007/s00420-016-1152-4

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