BACKGROUND: Despite reductions in exposure for workers and the general public, radon remains a leading cause of lung cancer. Prior studies of underground miners depended heavily upon information on deaths among miners employed in the early years of mine operations when exposures were high and tended to be poorly estimated. OBJECTIVES: To strengthen the basis for radiation protection, we report on the follow-up of workers employed in the later periods of mine operations for whom we have more accurate exposure information and for whom exposures tended to be accrued at intensities that are more comparable to contemporary settings. METHODS: We conducted a pooled analysis of cohort studies of lung cancer mortality among 57,873 male uranium miners in Canada, Czech Republic, France, Germany, and the United States, who were first employed in 1960 or later (thereby excluding miners employed during the periods of highest exposure and focusing on miners who tend to have higher quality assessments of radon progeny exposures). We derived estimates of excess relative rate per 100 working level months (ERR/100 WLM) for mortality from lung cancer. RESULTS: The analysis included 1.9 million person-years of observation and 1,217 deaths due to lung cancer. The relative rate of lung cancer increased in a linear fashion with cumulative exposure to radon progeny (ERR/100 WLM=1.33; 95% CI: 0.89, 1.88). The association was modified by attained age, age at exposure, and annual exposure rate; for attained ages <55 y, the ERR/100 WLM was 8.38 (95% CI: 3.30, 18.99) among miners who were exposed at ≥35 years of age and at annual exposure rates of <0.5 working levels. This association decreased with older attained ages, younger ages at exposure, and higher exposure rates. DISCUSSION: Estimates of association between radon progeny exposure and lung cancer mortality among relatively contemporary miners are coherent with estimates used to inform current protection guidelines. https://doi.org/10.1289/EHP10669.

Colorado School of Public Health Aurora Colorado USA

Federal Office for Radiation Protection Munich Germany

Institute for Radiological Protection and Nuclear Safety Fontenay aux Roses France

International Agency for Research on Cancer Lyon France

National Institute for Occupational Safety and Health Cincinnati Ohio USA

National Radiation Protection Institute Prague Czech Republic

New Mexico Tumor Registry Albuquerque New Mexico USA

Occupational Cancer Research Centre Toronto Canada

University of California Irvine Irvine California USA

University of California San Francisco San Francisco California USA

University of New Mexico Albuquerque New Mexico USA

See more in PubMed

Rhodes R. 1986. The Making of the Atomic Bomb. New York, NY: Simon & Schuster, Inc.

United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR). 2017. Annex D: biological effects of selected internal emitters—uranium. In: Sources and Effects of Ionizing Radiation. UNSCEAR 2016 Report to the General Assembly. Scientific Annexes A, B, C and D. New York, NY: United Nations.

International Agency for Research on Cancer. 2012. A Review of Human Carcinogens. Part D: Radiation. Lyon, France: International Agency for Research on Cancer.

National Research Council Panel on Dosimetric Assumptions Affecting the Application of Radon Risk Estimates. 1991. Comparative Dosimetry of Radon in Mines and Homes. Washington, DC: National Academies Press. PubMed

National Research Council Committee on Health Risks of Exposure to Radon. 1999. Health Effects of Exposure to Radon: BEIR VI. Washington, DC: National Academies Press. PubMed

Lubin JH, Boice JD Jr, Edling C, Hornung RW, Howe G, Kunz E, et al. . 1994. Radon and Lung Cancer Risk: A Joint Analysis of 11 Underground Miners Studies. Washington, DC: U.S. Department of Health and Human Services.

United Nations Scientific Committee on the Effects of Atomic Radiation. 1988. Sources, Effects, and Risks of Ionizing Radiation. New York, NY: United Nations.

United Nations Scientific Committee on the Effects of Atomic Radiation. 2000. Sources, Effects, and Risks of Ionizing Radiation. New York, NY: United Nations.

United Nations Scientific Committee on the Effects of Atomic Radiation. 2006. Effects of Ionizing Radiation. New York, NY: United Nations. https://www.unscear.org/unscear/en/publications/2006_1.html.

United Nations Scientific Committee on the Effects of Atomic Radiation. 2019. Sources, Effects, and Risks of Ionizing Radiation. New York, NY: United Nations.

Tirmarche M, Harrison JD, Laurier D, Paquet F, Blanchardon E, Marsh JW, et al. . 2010. ICRP publication 115. Lung cancer risk from radon and progeny and statement on radon. Ann ICRP 40(1):1–64, PMID: , 10.1016/j.icrp.2011.08.011. PubMed DOI

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):718–730, PMID: , 10.1093/aje/kwn406. PubMed DOI

Rage E, Caër-Lorho S, Drubay D, Ancelet S, Laroche P, Laurier D. 2015. Mortality analyses in the updated French cohort of uranium miners (1946–2007). Int Arch Occup Environ Health 88(6):717–730, PMID: , 10.1007/s00420-014-0998-6. PubMed DOI

Tomasek L. 2012. Lung cancer mortality among Czech uranium miners—60 years since exposure. J Radiol Prot 32(3):301–314, PMID: , 10.1088/0952-4746/32/3/301. PubMed DOI

Navaranjan G, Berriault C, Do M, Villeneuve PJ, Demers PA. 2016. Cancer incidence and mortality from exposure to radon progeny among Ontario uranium miners. Occup Environ Med 73(12):838–845, PMID: , 10.1136/oemed-2016-103836. PubMed DOI

Kreuzer M, Schnelzer M, Tschense A, Walsh L, Grosche B. 2010. Cohort profile: the German uranium miners cohort study (WISMUT cohort), 1946–2003. Int J Epidemiol 39(4):980–987, PMID: , 10.1093/ije/dyp216. PubMed DOI

Kreuzer M, Sobotzki C, Schnelzer M, Fenske N. 2018. Factors modifying the radon-related lung cancer risk at low exposures and exposure rates among German uranium miners. Radiat Res 189(2):165–176, PMID: , 10.1667/RR14889.1. PubMed DOI

Walsh L, Tschense A, Schnelzer M, Dufey F, Grosche B, Kreuzer M. 2010. The influence of radon exposures on lung cancer mortality in German uranium miners, 1946–2003. Radiat Res 173(1):79–90, PMID: , 10.1667/RR1803.1. PubMed DOI

Rage E, Richardson DB, Demers PA, Do M, Fenske N, Kreuzer M, et al. . 2020. PUMA—Pooled Uranium Miners Analysis: cohort profile. Occup Environ Med 77(3):194–200, PMID: , 10.1136/oemed-2019-105981. PubMed DOI PMC

Richardson DB, Rage E, Demers PA, Do MT, DeBono N, Fenske N, et al. . 2021. Mortality among uranium miners in North America and Europe: the Pooled Uranium Miners Analysis (PUMA). Int J Epidemiol 50(2):633–643, PMID: , 10.1093/ije/dyaa195. PubMed DOI

Field RW, Smith BJ, Steck DJ, Lynch CF. 2002. Residential radon exposure and lung cancer: variation in risk estimates using alternative exposure scenarios. J Expo Anal Environ Epidemiol 12(3):197–203, PMID: , 10.1038/sj.jea.7500215. PubMed DOI

National Research Council Committee on the Biological Effects of Ionizing Radiation (BEIR IV). 1988. Health Risks of Radon and other Internally Deposited Alpha-Emitters. Washington, DC: National Academies Press. PubMed

Xuan XZ, Lubin JH, Li JY, Yang LF, Luo AS, Lan Y, et al. . 1993. A cohort study in southern China of tin miners exposed to radon and radon decay products. Health Phys 64(2):120–131, PMID: , 10.1097/00004032-199302000-00001. PubMed DOI

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):157–169, PMID: , 10.1097/01.HP.0000239127.43136.89. PubMed DOI

Björ O, Damber L, Jonsson H, Nilsson T. 2015. A comparison between standard methods and structural nested modelling when bias from a healthy worker survivor effect is suspected: an iron-ore mining cohort study. Occup Environ Med 72(7):536–542, PMID: , 10.1136/oemed-2014-102251. PubMed DOI

Björ O, Jonsson H, Damber L, Wahlström J, Nilsson T. 2013. Reduced mortality rates in a cohort of long-term underground iron-ore miners. Am J Ind Med 56(5):531–540, PMID: , 10.1002/ajim.22168. PubMed DOI

Lane RSD, 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):773–785, PMID: , 10.1667/RR2237.1. PubMed DOI

Navaranjan G, Berriault C, Do M, Villeneuve PJ, Demers PA. 2015. Ontario Uranium Miners Cohort Study Report. Final report prepared for the Canadian Nuclear Safety Commission. Toronto, ON, Canada: University of Toronto.

Samet JM, Pathak DR, Morgan MV, Key CR, Valdivia AA, Lubin JH. 1991. Lung cancer mortality and exposure to radon progeny in a cohort of New Mexico underground uranium miners. Health Phys 61(6):745–752, PMID: , 10.1097/00004032-199112000-00005. PubMed DOI

World Health Organization (WHO). 1998. International Classification of Diseases, Ninth Revision (ICD-9).

Tomasek L, Rogel A, Tirmarche M, Mitton N, Laurier D. 2008. Lung cancer in French and Czech uranium miners: radon-associated risk at low exposure rates and modifying effects of time since exposure and age at exposure. Radiat Res 169(2):125–137, PMID: , 10.1667/RR0848.1. PubMed DOI

Navaranjan G, Chambers D, Thompson PA, Do M, Berriault C, Villeneuve PJ, et al. . 2019. Uncertainties associated with assessing Ontario uranium miners’ exposure to radon daughters. J Radiol Prot 39(1):136–149, PMID: , 10.1088/1361-6498/aaf1eb. PubMed DOI

Richardson D, Loomis D. 2004. The impact of exposure categorization for grouped analyses of cohort data. Occup Environ Med 61(11):930–935, PMID: , 10.1136/oem.2004.014159. PubMed DOI PMC

Lubin JH. 1988. Models for the analysis of radon-exposed populations. Yale J Biol Med 61(3):195–214, PMID: . PubMed PMC

Breslow NE, Day NE. 1987. Statistical Methods in Cancer Research. Vol II, The Design and Analysis of Cohort Studies. Lyon, France: International Agency for Research on Cancer. PubMed

Richardson DB, Langholz B. 2012. Background stratified Poisson regression analysis of cohort data. Radiat Environ Biophys 51(1):15–22, PMID: , 10.1007/s00411-011-0394-5. PubMed DOI PMC

Selvin S. 1996. Statistical Analysis of Epidemiologic Data. 2nd ed. New York, NY: Oxford University Press.

SAS Institute Inc. SAS OnlineDoc® 9.2. PDF Files. 2nd ed. Cary, NC: SAS Institute Inc.

Preston DL, Lubin JH, Pierce DA, McConney ME, Shilnikova NS. 2008. Epicure Risk Regression and Person-Year Computation Software: Command Summary and User Guide. Ottawa, ON, Canada: Risk Sciences International.

National Institute for Occupational Safety and Health. 1987. A Recommended Standard for Occupational Exposure to Radon Progeny in Underground Mines. Cincinnati, OH: National Institute for Occupational Safety and Health.

Daniels RD, Schubauer-Berigan MK. 2017. Radon in US workplaces: a review. Radiat Prot Dosimetry 176(3):278–286, PMID: , 10.1093/rpd/ncx007. PubMed DOI PMC

International Atomic Energy Agency. 2004. Radiation, People and the Environment. Vienna, Austria: IAEA Publications.

Field RW. 1999. Radon occurrence and health risk. https://cheec.uiowa.edu/sites/cheec.uiowa.edu/files/radon_occ.pdf [accessed 16 May 2022].

Archer VE, Coons T, Saccomanno G, Hong DY. 2004. Latency and the lung cancer epidemic among United States uranium miners. Health Phys 87(5):480–489, PMID: , 10.1097/01.hp.0000133216.72557.ab. PubMed DOI

Sevc J, Kunz E, Placek V. 1977. Lung cancer in uranium miners and long-term exposure to radon daughter products. Health Phys 30:433–437, PMID: , 10.1097/00004032-197606000-00001. PubMed DOI

Tomasek L. 2020. Lung cancer lifetime risks in cohort studies of uranium miners. Radiat Prot Dosimetry 191(2):171–175, PMID: , 10.1093/rpd/ncaa143. PubMed DOI

Tomasek L, Rogel A, Laurier D, Tirmarche M. 2008. Dose conversion of radon exposure according to new epidemiological findings. Radiat Prot Dosimetry 130(1):98–100, PMID: , 10.1093/rpd/ncn117. PubMed DOI

Allodji RS, Leuraud K, Bernhard S, Henry S, Bénichou 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, PMID: , 10.1088/0952-4746/32/1/85. PubMed DOI

Laurier D, Marsh JW, Rage E, Tomasek L. 2020. Miner studies and radiological protection against radon. Ann ICRP 49(1 suppl):57–67, PMID: , 10.1177/0146645320931984. PubMed DOI

Tomasek L. 2014. Effect of age at exposure in 11 underground miners studies. Radiat Prot Dosimetry 160(1–3):124–127, PMID: , 10.1093/rpd/ncu068. PubMed DOI

Kreuzer M, Fenske N, Schnelzer M, Walsh L. 2015. Lung cancer risk at low radon exposure rates in German uranium miners. Br J Cancer 113(9):1367–1369, PMID: , 10.1038/bjc.2015.324. PubMed DOI PMC

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):20–28, PMID: , 10.1097/HP.0b013e3181b8ce81. PubMed DOI

Tomasek L. 2013. Lung cancer risk from occupational and environmental radon and role of smoking in two Czech nested case-control studies. Int J Environ Res Public Health 10(3):963–979, PMID: , 10.3390/ijerph10030963. PubMed DOI PMC

L’Abbé KA, Howe GR, Burch JD, Miller AB, Abbatt J, Band P, et al. . 1991. Radon exposure, cigarette smoking, and other mining experience in the Beaverlodge Uranium Miners Cohort. Health Phys 60(4):489–495, PMID: , 10.1097/00004032-199104000-00002. PubMed DOI

Leuraud K, Billon S, Bergot D, Tirmarche M, Caër S, Quesne B, et al. . 2007. Lung cancer risk associated to exposure to radon and smoking in a case-control study of French uranium miners. Health Phys 92(4):371–378, PMID: , 10.1097/01.HP.0000252259.72683.2a. PubMed DOI

Leuraud K, Schnelzer M, Tomasek L, Hunter N, Timarche M, Grosche B, et al. . 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):375–387, PMID: , 10.1667/rr2377.1. PubMed DOI

Sogl M, Taeger D, Pallapies D, Brüning T, Dufey F, Schnelzer M, et al. . 2012. Quantitative relationship between silica exposure and lung cancer mortality in German uranium miners, 1946–2003. Br J Cancer 107(7):1188–1194, PMID: , 10.1038/bjc.2012.374. PubMed DOI PMC

Samet JM, Pathak DR, Morgan MV, Coultas DB, James DS, Hunt WC. 1994. Silicosis and lung cancer risk in underground uranium miners. Health Phys 66(4):450–453, PMID: , 10.1097/00004032-199404000-00012. PubMed DOI

Percy C, Stanek E III, Gloeckler L. 1981. Accuracy of cancer death certificates and its effect on cancer mortality statistics. Am J Public Health 71(3):242–250, PMID: , 10.2105/ajph.71.3.242. PubMed DOI PMC

Demers PA, Vaughan TL, Checkoway H, Weiss NS, Heyer NJ, Rosenstock L. 1992. Cancer identification using a tumor registry versus death certificates in occupational cohort studies in the United States. Am J Epidemiol 136(10):1232–1240, PMID: , 10.1093/oxfordjournals.aje.a116431. PubMed DOI

Rushton L, Hutchings SJ, Fortunato L, Young C, Evans GS, Brown T, et al. . 2012. Occupational cancer burden in Great Britain. Br J Cancer 107(suppl 1):S3–S7, PMID: , 10.1038/bjc.2012.112. PubMed DOI PMC

Marsh JW, Tomášek L, Laurier D, Harrison JD. 2021. Effective dose coefficients for radon and progeny: a review of ICRP and UNSCEAR values. Radiat Prot Dosimetry 195(1):1–20, PMID: , 10.1093/rpd/ncab106. PubMed DOI

Harrison JD. 2021. Lung cancer risk and effective dose coefficients for radon: UNSCEAR review and ICRP conclusions. J Radiol Prot 41(2):433, PMID: , 10.1088/1361-6498/abf547. PubMed DOI

Lifetime excess absolute risk for lung cancer due to exposure to radon: results of the pooled uranium miners cohort study PUMA

Radon and lung cancer in the pooled uranium miners analysis (PUMA): highly exposed early miners and all miners