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Published in: International Archives of Occupational and Environmental Health 8/2016

01-11-2016 | Original Article

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

Authors: L. Fournier, O. Laurent, E. Samson, S. Caër-Lorho, P. Laroche, B. Le Guen, D. Laurier, K. Leuraud

Published in: International Archives of Occupational and Environmental Health | Issue 8/2016

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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.
Literature
go back to reference Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723CrossRef Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723CrossRef
go back to reference Arrighi HM, Hertz-Picciotto I (1994) The evolving concept of the healthy worker survivor effect. Epidemiology 5:189–196CrossRef Arrighi HM, Hertz-Picciotto I (1994) The evolving concept of the healthy worker survivor effect. Epidemiology 5:189–196CrossRef
go back to reference Blanchardon E, Flüry-Herard A, Paquet F (2007) Les méthodes et les limites de la dosimétrie après contamination interne. Radioprotection 42:501–517CrossRef Blanchardon E, Flüry-Herard A, Paquet F (2007) Les méthodes et les limites de la dosimétrie après contamination interne. Radioprotection 42:501–517CrossRef
go back to reference 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 CrossRef 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 CrossRef
go back to reference Breslow NE, Day NE (1987) Statistical methods in cancer research. International Agency for Research on Cancer, Lyon Breslow NE, Day NE (1987) Statistical methods in cancer research. International Agency for Research on Cancer, Lyon
go back to reference 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 CrossRef 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 CrossRef
go back to reference 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 167:396–416CrossRef 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 167:396–416CrossRef
go back to reference 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 CrossRef 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 CrossRef
go back to reference Eisen EA, Robins JM (2005) Healthy worker effect. In: Armitage P, Colton T (ed) Encyclopedia of biostatistics. Wiley, USA Eisen EA, Robins JM (2005) Healthy worker effect. In: Armitage P, Colton T (ed) Encyclopedia of biostatistics. Wiley, USA
go back to reference 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 179:332–342CrossRef 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 179:332–342CrossRef
go back to reference Goldsmith JR (1975) What do we expect from an occupational cohort. J Occup Environ Med 17:126–128CrossRef Goldsmith JR (1975) What do we expect from an occupational cohort. J Occup Environ Med 17:126–128CrossRef
go back to reference 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 CrossRef 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 CrossRef
go back to reference 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 CrossRef 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 CrossRef
go back to reference ICRP (2007) The 2007 recommendations of the international commission on radiological protection. Annals of the ICRP, Elsevier, Amsterdam ICRP (2007) The 2007 recommendations of the international commission on radiological protection. Annals of the ICRP, Elsevier, Amsterdam
go back to reference 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 83:935–944CrossRef 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 83:935–944CrossRef
go back to reference McMichael AJ (1976) Standardized mortality ratios and the ‘Healthy Worker Effect’: scratching beneath the surface. J Occup Environ Med 18:165–168CrossRef McMichael AJ (1976) Standardized mortality ratios and the ‘Healthy Worker Effect’: scratching beneath the surface. J Occup Environ Med 18:165–168CrossRef
go back to reference 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 53:405–416CrossRef 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 53:405–416CrossRef
go back to reference 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 176:115–127CrossRef 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 176:115–127CrossRef
go back to reference 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 178:489–498CrossRef 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 178:489–498CrossRef
go back to reference 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 70:630–638CrossRef 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 70:630–638CrossRef
go back to reference Monson RR (1986) Observations on the healthy worker effect. J Occup Environ Med 28:425–433CrossRef Monson RR (1986) Observations on the healthy worker effect. J Occup Environ Med 28:425–433CrossRef
go back to reference 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 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
go back to reference 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 CrossRef 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 CrossRef
go back to reference 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 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
go back to reference 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 CrossRef 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 CrossRef
go back to reference Preston DL, Lubin JH, Pierce DA, McConney ME (1993) Epicure user’s guide. Hirosoft International, Seattle Preston DL, Lubin JH, Pierce DA, McConney ME (1993) Epicure user’s guide. Hirosoft International, Seattle
go back to reference 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–S97CrossRef 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–S97CrossRef
go back to reference 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 168:1–64CrossRef 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 168:1–64CrossRef
go back to reference 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 47:72–82CrossRef 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 47:72–82CrossRef
go back to reference 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 57:257–265CrossRef 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 57:257–265CrossRef
go back to reference 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 84:627–634CrossRef 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 84:627–634CrossRef
go back to reference 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 CrossRef 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 CrossRef
go back to reference 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):787–798CrossRef 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):787–798CrossRef
go back to reference 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 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
go back to reference 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 64:694–700CrossRef 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 64:694–700CrossRef
go back to reference 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 102:101–113CrossRef 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 102:101–113CrossRef
go back to reference 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 CrossRef 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 CrossRef
go back to reference 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 CrossRef 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 CrossRef
go back to reference Wilcosky T, Wing S (1987) The healthy worker effect: selection of workers and work forces. Scand J Work Environ Health 13:70–72CrossRef Wilcosky T, Wing S (1987) The healthy worker effect: selection of workers and work forces. Scand J Work Environ Health 13:70–72CrossRef
go back to reference 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 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
go back to reference World Health Organization (1977) International classification of diseases, injuries and causes of death. World Health Organization, Geneva World Health Organization (1977) International classification of diseases, injuries and causes of death. World Health Organization, Geneva
go back to reference World Health Organization (2004) International statistical classification of diseases and health related problems (The) ICD-10. World Health Organization, Geneva World Health Organization (2004) International statistical classification of diseases and health related problems (The) ICD-10. World Health Organization, Geneva
Metadata
Title
External radiation dose and cancer mortality among French nuclear workers: considering potential confounding by internal radiation exposure
Authors
L. Fournier
O. Laurent
E. Samson
S. Caër-Lorho
P. Laroche
B. Le Guen
D. Laurier
K. Leuraud
Publication date
01-11-2016
Publisher
Springer Berlin Heidelberg
Published in
International Archives of Occupational and Environmental Health / Issue 8/2016
Print ISSN: 0340-0131
Electronic ISSN: 1432-1246
DOI
https://doi.org/10.1007/s00420-016-1152-4

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