Radiation and Environmental Biophysics

, Volume 58, Issue 1, pp 39–47 | Cite as

Meta-analysis of case–control studies on the relationship between lung cancer and indoor radon exposure

  • Georgy MalinovskyEmail author
  • Ilia Yarmoshenko
  • Aleksey Vasilyev
Original Article


Indoor exposure to natural radon is a factor that influences lung cancer risk worldwide. The present study includes a meta-analysis of epidemiological data on the relationship between lung cancer and indoor radon. Altogether, 31 case–control studies with 20,703 cases, 34,518 controls and 140 individual odds ratio (OR) estimates are included in the meta-analysis. Weighted median OR was calculated for five radon intervals. The following parameters were used for the weighting: standard error of OR, duration of radon concentration measurement, and relative number of controls in reference intervals. The dependence of the weighted median OR on the radon concentration was estimated applying linear non-threshold and threshold models. The results obtained suggest a significant linear no-threshold exposure–effect relationship for radon concentrations above 100 Bq/m3, with a slope of 0.14 (95% confidence interval 0.08–0.21) per 100 Bq/m3.


Radon Lung cancer Risk Meta-analysis Non-threshold relationship 



This work was supported by the Grant for Young Scientist of the President of Russia, Grant number MK-3437.2017.4.

Compliance with ethical standards

Conflict of interest

The authors declare they have no actual or potential competing financial interests.


  1. Alavanja MCR, Brownson RC, Lubin JH, Berger E, Chang J, Boice JD Jr (1994) Residential radon exposure and lung cancer among nonsmoking women. J Natl Cancer Inst 86:1829–1837CrossRefGoogle Scholar
  2. Alavanja MC, Lubin JH, Mahaffey JA, Brownson RC (1999) Residential radon exposure and risk of lung cancer in Missouri. Am J Public Health 89:1042–1048CrossRefGoogle Scholar
  3. Auvinen A, Makelainen I, Hakama M, Castrén O, Pukkala E, Reisbacka H, Rytömaa T (1996) Indoor radon exposure and risk of lung cancer: a nested case–control study in Finland. J Natl Cancer Inst 88:966–972CrossRefGoogle Scholar
  4. Barros-Dios JM, Barreiro MA, Ruano-Ravina A, Figueiras A (2002) Exposure to residential radon and lung cancer in Spain: a population-based case–control study. Am J Epidemiol 156:548–555CrossRefGoogle Scholar
  5. Barros-Dios JM, Ruano-Ravina A, Perez-Rios M, Castro-Bernárdez M, Abal-Arca J, Tojo-Castro M (2012) Residential radon exposure, histologic types, and lung cancer risk. A case–control study in Galicia, Spain. Cancer Epidemiol Biomark Prev 21:951–958CrossRefGoogle Scholar
  6. Baysson H, Tirmarche M, Tymen G, Gouva S, Caillaud D, Artus JC, Vergnenegre A, Ducloy F, Laurier D (2004) Indoor radon and lung cancer in France. Epidemiology 15:709–716CrossRefGoogle Scholar
  7. BEIR (Biological Effects of Ionizing Radiation) (1999) Committee on Health Risks of Exposure to Radon (BEIR VI). Health effects of exposure to radon. National Academy Press, Washington, DCGoogle Scholar
  8. Blot WJ, Xu ZY, Boice JD Jr, Zhao DZ, Stone BJ, Sun J, Jing LB, Fraumeni JF Jr (1990) Indoor radon and lung cancer in China. J Natl Cancer Inst 82:1025–1030CrossRefGoogle Scholar
  9. Bochicchio F, McLaughlin JP, Walsh C (2003) Comparison of radon exposure assessment results: Po-210 surface activity on glass objects vs. contemporary air radon concentration. Radiat Meas 36:211–215CrossRefGoogle Scholar
  10. Bochicchio F, Forastiere F, Farchi S, Quarto M, Axelson O (2005) Residential radon exposure, diet and lung cancer: a case–control study in a Mediterranean region. Int J Cancer 114:983–991CrossRefGoogle Scholar
  11. Cohen BL (1995) Test of the linear no-threshold theory of radiation carcinogenesis for inhaled radon decay products. Health Phys 68:157–174CrossRefGoogle Scholar
  12. Darby S, Whitley E, Silcocks P, Thakrar B, Green M, Lomas P, Miles J, Reeves G, Fearn T, Doll R (1998) Risk of lung cancer associated with residential radon exposure in south-west England: a case–control study. Br J Cancer 78:394–408CrossRefGoogle Scholar
  13. Darby S, Hill D, Auvinen A, Barros-Dios JM, Baysson H, Bochicchio F, Deo H, Falk R, Forastiere F, Hakama M, Heid I, Kreienbrock L, Kreuzer M, Lagarde F, Mäkeläinen I, Muirhead C, Oberaigner W, Pershagen G, Ruano-Ravina A, Ruosteenoja E, Rosario AS, Tirmarche M, Tomásek L, Whitley E, Wichmann HE, Doll R (2005) Radon in homes and risk of lung cancer: collaborative analysis of individual data from 13 European case–control studies. BMJ 330:223–226CrossRefGoogle Scholar
  14. Darby S, Hill D, Deo H, Auvinen A, Barros-Dios JM, Baysson H, Bochicchio F, Falk R, Farchi S, Figueiras A, Hakama M, Heid I, Hunter N, Kreienbrock L, Kreuzer M, Lagarde F, Mäkeläinen I, Muirhead C, Oberaigner W, Pershagen G, Ruosteenoja E, Rosario AS, Tirmarche M, Tomásek L, Whitley E, Wichmann HE, Doll R (2006) Residential radon and lung cancer—detailed results of a collaborative analysis of individual data on 7148 persons with lung cancer and 14,208 persons without lung cancer from 13 epidemiologic studies in Europe. Scand J Work Environ Health 32:1–83CrossRefGoogle Scholar
  15. Dobrzyński L, Fornalski KW, Reszczyńska J (2018) Meta-analysis of thirty-two case–control and two ecological radon studies of lung cancer. J Radiat Res 59(2):149–163CrossRefGoogle Scholar
  16. Fearn T, Hill D, Darby S (2008) Measurement error in the explanatory variable of a binary regression: regression calibration and integrated conditional likelihood in studies of residential radon and lung cancer. Stat Med 27:2159–2176MathSciNetCrossRefGoogle Scholar
  17. Field RW, Steck DJ, Smith BJ, Brus CP, Fisher EL, Neuberger JS, Platz CE, Robinson RA, Woolson RF, Lynch CF (2000) Residential radon gas exposure and lung cancer. The Iowa Radon Lung Cancer Study. Am J Epidemiol 151:1091–1102CrossRefGoogle Scholar
  18. Fornalski KW, Dobrzyński L (2011) Pooled Bayesian analysis of twenty-eight studies on radon induced lung cancers. Health Phys 101(3):265–273CrossRefGoogle Scholar
  19. Garzillo C, Pugliese M, Loffredo F, Quarto M (2017) Indoor radon exposure and lung cancer risk: a meta-analysis of case–control studies. Transl Cancer Res 6:S934–S943CrossRefGoogle Scholar
  20. Gaskin J, Coyle D, Whyte J, Krewksi D (2018) Global estimate of lung cancer mortality attributable to residential radon. Environ Health Perspect 126(5):057009CrossRefGoogle Scholar
  21. Hystad P, Brauer M, Demers PA, Johnson KC, Setton E, Cervantes-Larios A, Poplawski K, McFarlane A, Whitehead A, Nicol AM (2014) Geographic variation in radon and associated lung cancer risk in Canada. Can J Public Health 105:e4–e10CrossRefGoogle Scholar
  22. ICRP (International Commission on Radiological Protection) (1993) Protection against radon-222 at home and at work. ICRP Publication 65. Ann ICRP 23(2):1–45Google Scholar
  23. ICRP (1994) Human respiratory tract model for radiological protection. ICRP Publication 66. Ann ICRP 24(1–3):1–482Google Scholar
  24. ICRP (2010) Lung cancer risk from radon and progeny and statement on radon. ICRP Publication 115. Ann ICRP 40(1):1–64CrossRefGoogle Scholar
  25. ICRP (2014) Radiological protection against radon exposure. ICRP Publication 126. Ann ICRP 43(3):5–73CrossRefGoogle Scholar
  26. ICRP (2017) Occupational intake of radionuclides: part 3. ICRP Publication 137. Ann ICRP 46 (3/4):1–486Google Scholar
  27. Kirdin IA, Lezhnin VL, Yarmoshenko IV, Ekidin A (2002) Radon and lung cancer case–control study in Middle Ural. In: Proceedings of the IRPA regional congress on radiation protection in Central Europe; 2001 May 20–25, Dubrovnik, Croatia, Zagreb. Rep. 3o-05Google Scholar
  28. Kreienbrock L, Kreuzer M, Gerken M, Dingerkus G, Wellmann J, Keller G, Wichmann HE (2001) Case–control study on lung cancer and residential radon in Western Germany. Am J Epidemiol 153:42–52CrossRefGoogle Scholar
  29. Kreuzer M, Heinrich J, Wolke G, Schaffrath Rosario A, Gerken M, Wellmann J, Keller G, Kreienbrock L, Wichmann HE (2003) Residential radon and risk of lung cancer in Eastern Germany. Epidemiology 14:559–568CrossRefGoogle Scholar
  30. Kreuzer M, Sobotzki C, Fenske N, Marsh JW, Schnelzer M (2017) Leukaemia mortality and low-dose ionising radiation in the WISMUT uranium miner cohort (1946–2013). Occup Environ Med 74(4):252–258CrossRefGoogle Scholar
  31. Krewski D, Lubin JH, Zielinski JM, Alavanja M, Catalan VS, Field RW, Klotz JB, Létourneau EG, Lynch CF, Lyon JI, Sandler DP, Schoenberg JB, Steck DJ, Stolwijk JA, Weinberg C, Wilcox HB (2005) Residential radon and risk of lung cancer. A combined analysis of 7 North American case–control studies. Epidemiology 16(2):137–145CrossRefGoogle Scholar
  32. Kropat G, Bochud F, Jaboyedoff M, Laedermann JP, Murith C, Palacios M, Baechler S (2014) Major influencing factors of indoor radon concentrations in Switzerland. J Environ Radioact 129:7–22CrossRefGoogle Scholar
  33. Lagarde F, Pershagen G, Akerblom G, Axelson O, Bäverstam U, Damber L, Enflo A, Svartengren M, Swedjemark GA (1997) Residential radon and lung cancer in Sweden: risk analysis accounting for imprecision in the exposure assessment. Health Phys 72:269–276CrossRefGoogle Scholar
  34. Lagarde F, Falk R, Almren K, Nyberg F, Svensson H, Pershagen G (2002) Glass-based radon-exposure assessment and lung cancer risk. J Expo Anal Environ Epidemiol 12:344–354CrossRefGoogle Scholar
  35. 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):773–785ADSCrossRefGoogle Scholar
  36. Letourneau EG, Krewski D, Choi NW, Goddard MJ, McGregor RG, Zielinski JM, Du J (1994) Case–control study of residential radon and lung cancer in Winnipeg, Manitoba, Canada. Am J Epidemiol 140:310–322CrossRefGoogle Scholar
  37. 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):375–387ADSCrossRefGoogle Scholar
  38. Lubin JH, Boice JD Jr, Edling C, Hornung RW, Howe GR, Kunz E, Kusiak RA, Morrison HI, Radford EP, Samet JM, Tirmarche M, Woodward A, Yao SX, Pierce DA (1995) Lung cancer in radon-exposed miners and estimation of risk from indoor exposure. J Natl Cancer Inst 87(11):817–827CrossRefGoogle Scholar
  39. Lubin JH, Boice JD (1997) Lung cancer risk from residential radon: meta-analysis of eight epidemiologic studies. J Natl Cancer Inst 89:49–57CrossRefGoogle Scholar
  40. Malinovsky G, Yarmoshenko I, Zhukovsky M (2018) Radon, smoking and HPV as lung cancer risk factors in ecological studies. Int J Radiat Biol 94:62–69CrossRefGoogle Scholar
  41. Miles JC (2001) Temporal variation of radon levels in houses and implications for radon measurement strategies. Radiat Prot Dosim 93(4):369–376CrossRefGoogle Scholar
  42. Onishchenko AD, Varaksin AN, Zhukovsky MV (2017) Analysis of approaches to the formation of a control group in radon epidemiological case–control studies. Radiatsionnaya Gygiena Radiat Hyg 10(3):76–89 (in Russ.) CrossRefGoogle Scholar
  43. Pershagen G, Liang ZH, Hrubec Z, Svensson C, Boice JD Jr (1992) Residential radon exposure and lung cancer in Swedish women. Health Phys 63:179–186CrossRefGoogle Scholar
  44. Pershagen G, Akerblom G, Axelson O, Clavensjö B, Damber L, Desai G, Enflo A, Lagarde F, Mellander H, Svartengren M, Swedjemark GA (1994) Residential radon exposure and lung cancer in Sweden. N Engl J Med 330:159–164CrossRefGoogle Scholar
  45. Pisa FE, Barbone F, Betta A, Bonomi M, Alessandrini B, Bovenzi M (2001) Residential radon and risk of lung cancer in an Italian alpine area. Arch Environ Health 56:208–215CrossRefGoogle Scholar
  46. 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):717–730CrossRefGoogle Scholar
  47. Ruosteenoja E, Makelainen I, Rytomaa T, Hakulinen T, Hakama M (1996) Radon and lung cancer in Finland. Health Phys 71:185–189CrossRefGoogle Scholar
  48. Sandler DP, Weinberg CR, Shore DL, Archer VE, Stone MB, Lyon JL, Rothney-Kozlak L, Shepherd M, Stolwijk JA (2006) Indoor radon and lung cancer risk in Connecticut and Utah. J Toxicol Environ Health 69:633–654CrossRefGoogle Scholar
  49. Schoenberg JB, Klotz JB, Wilcox HB, Nicholls GP, Gil-del-Real MT, Stemhagen A, Mason TJ (1990) Case–control study of residential radon and lung cancer among New Jersey women. Cancer Res 50:6520–6524Google Scholar
  50. Sobue T, Lee VS, Ye W, Tanooka H, Mifune M, Suyama A, Koga T, Morishima H, Kondo S (2000) Residential radon exposure and lung cancer risk in Misasa, Japan: a case–control study. J Radiat Res 41:81–92CrossRefGoogle Scholar
  51. Thompson RE, Nelson DF, Popkin JH, Popkin Z (2008) Case–control study of lung cancer risk from residential radon exposure in Worcester County, Massachusetts. Health Phys 94:228–241CrossRefGoogle Scholar
  52. Tomasek L (2012) Lung cancer mortality among Czech uranium miners—60 years since exposure. J Radiol Prot 32(3):301–314CrossRefGoogle Scholar
  53. 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. 882CrossRefGoogle Scholar
  54. Torres-Duran M, Ruano-Ravina A, Parente-Lamelas I, Leiro-Fernández V, Abal-Arca J, Montero-Martínez C, Pena-Álvarez C, González-Barcala FJ, Castro-Añón O, Golpe-Gómez A, Martínez C, Mejuto-Martí MJ, Fernández-Villar A, Barros-Dios JM (2014) Lung cancer in never-smokers: a case–control study in a radon- prone area (Galicia, Spain). Eur Respir J 44:994–1001CrossRefGoogle Scholar
  55. UNEP (United Nations Environment Programme) (2016) Radiation: effects and sources. UNEP, Vienna. ISBN 978-92-807-3517-8Google Scholar
  56. UNSCEAR (United Nations Scientific Committee on the Effects of Atomic Radiation) (2000) United Nations Report 2000—Annex B: exposures from natural radiation sources. UNSCEAR, New YorkGoogle Scholar
  57. UNSCEAR (2009) United Nations Report 2006—Annex E. Sources-to-effects assessment for radon in homes and workplaces. UNSCEAR, New YorkGoogle Scholar
  58. Vasilyev AV, Yarmoshenko IV, Zhukovsky MV (2015) Low air exchange rate causes high indoor radon concentration in energy-efficient buildings. Radiat Prot Dosim 164:601–605CrossRefGoogle Scholar
  59. Walsh L, Grosche B, Schnelzer M, Tschense A, Sogl M, Kreuzer M (2015) A review of the results from the German Wismut uranium miners cohort. Radiat Prot Dosim 164(1–2):147–153CrossRefGoogle Scholar
  60. Wang Z, Lubin JH, Wang L, Zhang S, Boice JD Jr, Cui H, Zhang S, Conrath S, Xia Y, Shang B, Brenner A, Lei S, Metayer C, Cao J, Chen KW, Lei S, Kleinerman RA (2002) Residential radon and lung cancer risk in a high-exposure area of Gansu Province, China. Am J Epidemiol 155:554–564CrossRefGoogle Scholar
  61. Wichmann HE, Rosario AS, Heid IM, Kreuzer M, Heinrich J, Kreienbrock L (2005) Lung cancer risk due to radon in dwellings—evaluation of the epidemiological knowledge. Int Congr Ser 1276:54–57CrossRefGoogle Scholar
  62. Wilcox HB, Al-Zoughool M, Garner MJ, Jiang H, Klotz JB, Krewski D, Nicholson WJ, Schoenberg JB, Villeneuve PJ, Zielinski JM (2008) Case–control study of radon and lung cancer in New Jersey. Radiat Prot Dosim 128:169–179CrossRefGoogle Scholar
  63. Yarmoshenko IV, Kirdin IA, Zhukovsky MV, Astrakhantseva SY (2005) Meta-analysis of twenty radon and lung cancer case–control studies. Radioact Environ 7:762–771CrossRefGoogle Scholar
  64. Yarmoshenko IV, Vasilyev AV, Malinovsky GP, Bossew P, Žunić ZS, Onischenko A, Zhukovsky M (2016) Variance of indoor radon concentration: major influencing factors. Sci Total Environ 15(541):155–160ADSCrossRefGoogle Scholar
  65. Zhukovsky M, Onishchenko A, Varaksin A, Vasilyev A (2011) The influence of radon measurement errors on the uncertainties of epidemiological case–control studies. Radiat Prot Dosim 145(2–3):243–247CrossRefGoogle Scholar
  66. Zunic ZS, Yarmoshenko IV, Birovljev A, Bochicchio F, Quarto M, Obryk B, Paszkowski M, Celiković I, Demajo A, Ujić P, Budzanowski M, Olko P, McLaughlin JP, Waligorski MP (2007a) Radon survey in the high natural radiation region of Niška Banja, Serbia. J Environ Radioact 92:165–174CrossRefGoogle Scholar
  67. Zunic ZS, Yarmoshenko IV, Kelleher K, Paridaens J, Mc Laughlin JP, Celiković I, Ujić P, Onischenko AD, Jovanović S, Demajo A, Birovljev A, Bochicchio F (2007b) Comparison of retrospective and contemporary indoor radon measurements in a high-radon area of Serbia. Sci Total Environ 387:269–275ADSCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Institute of Industrial Ecology UB RASYekaterinburgRussia

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