Biologically-based mechanistic models of radiation-related carcinogenesis applied to epidemiological data

References

• Agrawal N, Akbani R, Aksoy BA, Ally A, Arachchi H, Asa SL, Auman JT, Balasundaram M, Balu S, Baylin SB, et al. 2014. Integrated genomic characterization of papillary thyroid carcinoma. Cell. 159:676–690.
   PubMed Web of Science ®Google Scholar
• Armitage P, Doll R. 1954. The age distribution of cancer and a multistage theory of carcinogenesis. Br J Cancer. 8:1–12.
   PubMed Web of Science ®Google Scholar
• Armitage P, Doll R. 1957. A two-stage theory of carcinogenesis in relation to the age distribution of human cancer. Br J Cancer. 11:161–169.
   PubMed Web of Science ®Google Scholar
• Boice JD Jr. 2015. How low can you go: learning to live with uncertainty. Health Phys News, The Boice Report 33:28–29.
   Google Scholar
• Brenner DJ. 2009. Extrapolating radiation-induced cancer risks from low doses to very low doses. Health Phys. 97:505–509.
   PubMed Web of Science ®Google Scholar
• Collisson EA, Campbell JD, Brooks AN, Berger AH, Lee W, Chmielecki J, Beer DG, Cope L, Creighton CJ, Danilova L, et al. (383 collaborators). 2014. Comprehensive molecular profiling of lung adenocarcinoma. Nature. 511:543–550.
   PubMed Web of Science ®Google Scholar
• Costanzo M, VanderSluis B, Koch E, Baryshnikova A, Pons C, Tan G, Wang W, Usaj M, Hanchard J, Lee SD, et al. 2016. A global genetic interaction network maps a wiring diagram of cellular function. Science. 353:1381.
   Web of Science ®Google Scholar
• Doll R, Wakeford R. 1997. Risk of childhood cancer from fetal irradiation. Br J Radiol. 70:130–139.
   PubMed Web of Science ®Google Scholar
• Eidemüller M, Holmberg E, Jacob P, Lundell M, Karlsson P. 2009. Breast cancer risk among Swedish hemangioma patients and possible consequences of radiation-induced genomic instability. Mutat Res. 669:48–55.
   PubMed Web of Science ®Google Scholar
• Eidemüller M, Ostroumova E, Krestinina L, Epiphanova S, Akleyev A, Jacob P. 2010. Comparison of mortality and incidence solid cancer risk after radiation exposure in the Techa River Cohort. Radiat Environ Biophys. 49:477–490.
   PubMed Web of Science ®Google Scholar
• Eidemüller M, Jacob P, Lane RSD, Frost SE, Zablotska LB. 2012. Lung cancer mortality (1950–1999) among Eldorado uranium workers: a comparison of models of carcinogenesis and empirical excess risk models. PLoS One. 7:e41431.
   PubMed Web of Science ®Google Scholar
• Eidemüller M, Holmberg E, Jacob P, Lundell M, Karlsson P. 2015a. Breast cancer risk and possible mechanisms of radiation-induced genomic instability in the Swedish hemangioma cohort after reanalyzed dosimetry. Mutat Res. 775:1–9.
   PubMed Web of Science ®Google Scholar
• Eidemüller M, Kaiser JC, Luebeck EG, Accomando WP, Unger K, Van de Wiel M, Behr J, Chadeau-Hyam M, Dekkers F, Enderling H. 2015b. OPERRA workshop report: modelling of pathogenesis [Internet]. Available from: http://www.helmholtz-muenchen.de/en/iss/research/work-groups/radiation-risk/highlights/operra-modelling-workshop/index.html
   Google Scholar
• Fisher JC, Hollomon JH. 1951. A hypothesis for the origin of cancer foci. Cancer. 4:916–918.
   PubMed Web of Science ®Google Scholar
• Gasparrini A. 2014. Modeling exposure-lag-response associations with distributed lag non-linear models. Stat Med. 33:881–899.
   PubMed Web of Science ®Google Scholar
• George J, Lim JS, Jang SJ, Cun Y, Ozretić L, Kong G, Leenders F, Lu X, Fernández-Cuesta L, Bosco G, et al. 2015. Comprehensive genomic profiles of small cell lung cancer. Nature. 524:47–53.
   PubMed Web of Science ®Google Scholar
• Hamada N, Maeda M, Otsuka K, Tomita M. 2011. Signaling pathways underpinning the manifestations of ionizing radiation-induced bystander effects. Curr Mol Pharmacol. 4:79–95.
   PubMedGoogle Scholar
• Hamada N. 2014. What are the intracellular targets and intratissue target cells for radiation effects? Radiat Res. 181:9–20.
   PubMed Web of Science ®Google Scholar
• Hammerman PS, Lawrence MS, Voet D, Jing R, Cibulskis K, Sivachenko A, Stojanov P, McKenna A, Lander ES, Gabriel S, et al. (412 collaborators). 2012. Comprehensive genomic characterization of squamous cell lung cancers. Nature. 489:519–525.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell. 100:57–70.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell. 144:646–674.
   PubMed Web of Science ®Google Scholar
• Hazelton WD, Luebeck EG, Heidenreich WF, Moolgavkar SH. 2001. Analysis of a historical cohort of Chinese tin miners with arsenic, radon, cigarette smoke, and pipe smoke exposures using the biologically based two-stage clonal expansion model. Radiat Res. 156:78–94.
   PubMed Web of Science ®Google Scholar
• Hazelton WD, Moolgavkar SH, Curtis SB, Zielinski JM, Ashmore JP, Krewski D. 2006. Biologically based analysis of lung cancer incidence in a large Canadian occupational cohort with low-dose ionizing radiation exposure, and comparison with Japanese atomic bomb survivors. J Toxicol Environ Health. 69:1013–1038.
   PubMed Web of Science ®Google Scholar
• Heidenreich WF, Jacob P, Paretzke HG. 1997. Exact solutions of the clonal expansion model and their application to the incidence of solid tumors of atomic bomb survivors. Radiat Environ Biophys. 36:45–58.
   PubMed Web of Science ®Google Scholar
• Heidenreich WF, Luebeck EG, Hazelton WD, Paretzke HG, Moolgavkar SH. 2002. Multistage models and the incidence of cancer in the cohort of Atomic bomb survivors. Radiat Res. 158:607–614.
   PubMed Web of Science ®Google Scholar
• Heidenreich WF, Nyberg U, Hall PA. 2003. A biologically based model for liver cancer risk in the Swedish thorotrast patients. Radiat Res. 159:656–662.
   PubMed Web of Science ®Google Scholar
• Heidenreich WF, Tomasek L, Rogel A, Laurier D, Tirmarche M. 2004. Studies of radon-exposed miner cohorts using a biologically based model: comparison of current Czech and French data with historic data from China and Colorado. Radiat Environ Biophys. 43:247–256.
   PubMed Web of Science ®Google Scholar
• Heidenreich WF, Cullings HM, Funamoto S, Paretzke HG. 2007. Promoting action of radiation in the Atomic bomb survivor carcinogenesis data? Radiat Res. 168:750–756.
   PubMed Web of Science ®Google Scholar
• Heidenreich WF, Cullings HM. 2010. Use of the individual data of the a-bomb survivors for biologically based cancer models. Radiat Environ Biophys. 49:39–46.
   PubMed Web of Science ®Google Scholar
• Heidenreich WF, Tomasek L, Grosche B, Leuraud K, Laurier D. 2012. Lung cancer mortality in the European uranium miners cohorts analyzed with a biologically based model taking into account radon measurement error. Radiat Environ Biophys. 51:263–275.
   PubMed Web of Science ®Google Scholar
• Hess J, Thomas G, Braselmann H, Bauer V, Bogdanova T, Wienberg J, Zitzelsberger H, Unger K. 2011. Gain of chromosome band 7q11 in papillary thyroid carcinomas of young patients is associated with exposure to low-dose irradiation. Proc Natl Acad Sci USA. 108:9595–9600.
   PubMed Web of Science ®Google Scholar
• Jacob V, Jacob P, Meckbach R, Romanov SA, Vasilenko EK. 2005. Lung cancer in Mayak workers: interaction of smoking and plutonium exposure. Radiat Environ Biophys. 44:119–129. [Erratum (2006) Radiat Environ Biophys. 44: 307.]
   PubMed Web of Science ®Google Scholar
• Jacob P, Meckbach R, Sokolnikov M, Khokhryakov VV, Vasilenko E. 2007. Lung cancer risk of Mayak workers: modelling of carcinogenesis and bystander effect. Radiat Environ Biophys. 46:383–394.
   PubMed Web of Science ®Google Scholar
• Jacob P, Walsh L, Eidemüller M. 2008. Modeling of cell inactivation and carcinogenesis in the atomic bomb survivors with applications to the mortality from all solid, stomach and liver cancer. Radiat Environ Biophys. 47:375–388.
   PubMed Web of Science ®Google Scholar
• Jacob P, Meckbach R, Kaiser JC, Sokolnikov M. 2010. Possible expressions of radiation-induced genomic instability, bystander effects or low-dose hypersensitivity in cancer epidemiology. Mutat Res. 687:34–39.
   PubMed Web of Science ®Google Scholar
• Kai M, Luebeck EG, Moolgavkar SH. 1997. Analysis of the incidence of solid cancer among atomic bomb survivors using a two-stage model of carcinogenesis. Radiat Res. 148:348–358.
   PubMed Web of Science ®Google Scholar
• Kaiser JC, Heidenreich WF. 2004. Comparing regression methods for the two-stage clonal expansion model of carcinogenesis. Stat Med. 23:3333–3350.
   PubMed Web of Science ®Google Scholar
• Kaiser JC, Jacob P, Meckbach R, Cullings HM. 2012. Breast cancer risk in atomic bomb survivors from multi-model inference with incidence data 1958–1998. Radiat Environ Biophys. 51:1–14.
   PubMed Web of Science ®Google Scholar
• Kaiser JC, Meckbach R, Jacob P. 2014. Genomic instability and radiation risk in molecular pathways to colon cancer. PLoS One. 9:e111024.
   PubMed Web of Science ®Google Scholar
• Kaiser JC, Meckbach R, Eidemüller M, Selmansberger M, Unger K, Shpak V, Blettner M, Zitzelsberger H, Jacob P. 2016. Integration of a radiation biomarker into modeling of thyroid carcinogenesis and post-Chernobyl risk assessment. Carcinogenesis. 37:1152–1160.
   PubMed Web of Science ®Google Scholar
• Kendal GM, Little MP, Wakeford R, Bunch KJ, Miles JCH, Vincent TJ, Meara JR, Murphy MFG. 2013. A record-based case-control study of natural background radiation and the incidence of childhood leukaemia and other cancers in Great Britain during 1980–2006. Leukemia. 27:3–9.
   PubMed Web of Science ®Google Scholar
• Koboldt DC, Fulton RS, McLellan MD, Schmidt H, Kalicki-Veizer J, McMichael JF, Fulton LL, Dooling DJ, Ding L, Mardis ER, et al. (357 collaborators). 2012. Comprehensive molecular portraits of human breast tumours. Nature. 490:61–70.
   PubMed Web of Science ®Google Scholar
• Knudson AG. 1971. Mutation and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci USA. 68:820–823.
   PubMed Web of Science ®Google Scholar
• Krewski D, Zielinski JM, Hazelton WD, Garner MJ, Moolgavkar SH. 2003. The use of biologically based cancer risk models in radiation epidemiology. Radiat Prot Dosimetry. 104:367–376.
   PubMed Web of Science ®Google Scholar
• Leenhouts HP, Brugmans MJP. 2000. An analysis of bone and head sinus cancers in radium dial painters using a two-mutation carcinogenesis model. J Radiol Prot. 20:169–188.
   PubMedGoogle Scholar
• Leenhouts HP, Brugmans MJP, Andersson M, Storm H. 2002. A reanalysis of liver cancer incidence in Danish patients administered thorotrast using a two-mutation carcinogenesis model. Radiat Res. 158:597–606.
   PubMed Web of Science ®Google Scholar
• Little MP. 1996. Generalisation of the two-mutation and classical multi-stage models of carcinogenesis fitted to the Japanese atomic bomb survivor data. J Radiol Prot. 16:7–24.
   Google Scholar
• Little MP, Haylock RGE, Muirhead CR. 2002. Modelling lung tumour risk in radon-exposed uranium miners using generalizations of the two-mutation model of Moolgavkar, Venzon and Knudson. Int J Radiat Biol. 78:49–68.
   PubMed Web of Science ®Google Scholar
• Little MP, Wright EG. 2003. A stochastic carcinogenesis model incorporating genomic instability fitted to colon cancer data. Math Biosci. 183:111–134.
   PubMed Web of Science ®Google Scholar
• Little MP, Li G. 2007. Stochastic modelling of colon cancer: is there a role for genomic instability? Carcinogenesis. 28:479–487.
   PubMed Web of Science ®Google Scholar
• Little MP, Vineis P, Li G. 2008. A stochastic carcinogenesis model incorporating multiple types of genomic instability fitted to colon cancer data. J Theor Biol. 254:229–238.
   PubMed Web of Science ®Google Scholar
• Little MP, Heidenreich WF, Li G. 2009. Parameter identifiability and redundancy in a general class of stochastic carcinogenesis models. PLoS One. 4:e8520.
   PubMed Web of Science ®Google Scholar
• Little MP. 2010a. Do non-targeted effects increase or decrease low dose risk in relation to the linear-non-threshold (LNT) model? Mutat Res. 687:17–27.
   PubMed Web of Science ®Google Scholar
• Little MP. 2010b. Cancer models, genomic instability and somatic cellular Darwinian evolution. Biol Direct. 5:19.
   PubMed Web of Science ®Google Scholar
• Little MP, Hendry JH, Puskin JS. 2016. Lack of correlation between stem-cell proliferation and radiation- or smoking-associated cancer risk. PLoS One. 11:e0150335.
   PubMed Web of Science ®Google Scholar
• Lubin JH, Boice JD Jr, Edling C, Hornung RW, Howe G, Kunz E, Kusiak RA, Morrison HI, Radford EP, Samet JM, et al. 1995. Radon-exposed underground miners and inverse dose-rate (protraction enhancement) effects. Health Phys. 69:494–500.
   PubMed Web of Science ®Google Scholar
• Luebeck EG, Moolgavkar SH. 2002. Multistage carcinogenesis and the incidence of colorectal cancer. Proc Natl Acad Sci USA. 99:15095–15100.
   PubMed Web of Science ®Google Scholar
• Luebeck EG, Heidenreich WF, Hazelton WD, Paretzke HG, Moolgavkar SH. 1999. Biologically based analysis of the data for the Colorado uranium miners cohort: age, dose and dose-rate effects. Radiat Res. 152:339–351.
   PubMed Web of Science ®Google Scholar
• Luebeck EG, Curtius K, Jeon J, Hazelton WD. 2013. Impact of tumor progression on cancer incidence curves. Cancer Res. 73:1086–1096.
   PubMed Web of Science ®Google Scholar
• Moolgavkar SH, Venzon DJ. 1979. Two-event models for carcinogenesis: incidence curves for childhood and adult tumors. Math Biosci. 47:55–77.
   Web of Science ®Google Scholar
• Morgan WF. 2003a. Non-targeted and delayed effects of exposure to ionizing radiation. I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res. 159:567–580.
   PubMed Web of Science ®Google Scholar
• Morgan WF. 2003b. Non-targeted and delayed effects of exposure to ionizing radiation. II. Radiation-induced genomic instability and bystander effects in vivo, clastogenic factors and transgenerational effects. Radiat Res. 159:581–596.
   PubMed Web of Science ®Google Scholar
• Muzny DM, Bainbridge MN, Chang K, Dinh HH, Drummond JA, Fowler G, Kovar CL, Lewis LR, Morgan MB, Newsham IF, et al. (326 collaborators). 2012. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 487:330–336.
   PubMed Web of Science ®Google Scholar
• Nikkilä A, Erme S, Arvela H, Holmgren O, Raitanen J, Lohi O, Auvinen A. 2016. Background radiation and childhood leukemia: a nationwide register-based case-control study. Int J Cancer. 139:1975–1982.
   PubMed Web of Science ®Google Scholar
• Noble R, Kaltz O, Hochberg ME. 2015. Peto’s paradox and human cancers. Phil Trans R Soc B. 370:20150104.
   PubMed Web of Science ®Google Scholar
• Nordling CO. 1953. A new theory on cancer-inducing mechanism. Br J Cancer. 7:68–72.
   PubMed Web of Science ®Google Scholar
• Novak MA, Komarova NL, Sengupta A, Jallepalli PV, Shih IM, Vogelstein B, Lengauer C. 2002. The role of chromosomal instability in tumor initiation. Proc Natl Acad Sci USA. 99:16226–16231.
   PubMed Web of Science ®Google Scholar
• Pearce MS, Salotti JA, Little MP, McHugh K, Lee C, Kim KP, Howe NL, Ronckers CM, Rajaraman P, Sir Craft AW, et al. 2012. Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet. 380:499–505.
   PubMed Web of Science ®Google Scholar
• Pernot E, Hall J, Baatout S, Benotmane MA, Blanchardon E, Bouffler S, El Saghire H, Gomolka M, Guertler A, Harms-Ringdahl M, et al. 2012. Ionizing radiation biomarkers for potential use in epidemiological studies. Mutat Res. 751:258–286.
   PubMed Web of Science ®Google Scholar
• Pierce DA, Mendelsohn ML. 1999. A model for radiation-related cancer suggested by atomic bomb survivor data. Radiat Res. 152:642–654.
   PubMed Web of Science ®Google Scholar
• Pierce DA. 2003. Mechanistic models for radiation carcinogenesis and the atomic bomb survivor data. Radiat Res. 160:718–723.
   PubMed Web of Science ®Google Scholar
• Platt R. 1955. Clonal aging and cancer. Lancet. 265:867.
   Google Scholar
• Preston DL, 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.
   PubMed Web of Science ®Google Scholar
• Preston J. 2015. Integrating basic radiobiological science and epidemiological studies: why and how. Health Phys. 108:125–130.
   PubMed Web of Science ®Google Scholar
• Rühm W, Woloschak GE, Shore RE, Azizova TV, Grosche B, Niwa O, Akiba S, Ono T, Suzuki K, Iwasaki T, et al. 2015. Dose and dose-rate effects of ionizing radiation: a discussion in the light of radiological protection. Radiat Environ Biophys. 54:379–401.
   PubMed Web of Science ®Google Scholar
• Selmansberger M, Feuchtinger A, Zurnadzhy L, Michna A, Kaiser JC, Abend M, Brenner A, Bogdanova T, Walch A, Unger K, et al. 2015a. CLIP2 as radiation biomarker in papillary thyroid carcinoma. Oncogene. 34:3917–3925.
   PubMed Web of Science ®Google Scholar
• Selmansberger M, Kaiser JC, Hess J, Güthlin D, Likhtarev I, Shpak V, Tronko M, Brenner A, Abend M, Blettner M, et al. 2015b. Dose-dependent expression of CLIP2 in post-Chernobyl papillary thyroid carcinomas. Carcinogenesis 36:748–756.
   PubMed Web of Science ®Google Scholar
• Selmansberger M, Braselmann H, Hess J, Bogdanova T, Abend M, Tronko M, Brenner A, Zitzelsberger H, Unger K. 2015c. Genomic copy number analysis of Chernobyl papillary thyroid carcinoma in the Ukrainian-American Cohort. Carcinogenesis 36:1381–1387.
   PubMed Web of Science ®Google Scholar
• Shuryak I, Hahnfeldt P, Hlatky L, Sachs RK, Brenner DJ. 2009a. A new view of radiation-induced cancer: integrating short- and long-term processes. Part I: approach. Radiat Environ Biophys. 48:263–274.
   PubMed Web of Science ®Google Scholar
• Shuryak I, Hahnfeldt P, Hlatky L, Sachs RK, Brenner DJ. 2009b. A new view of radiation-induced cancer: integrating short- and long-term processes. Part II: second cancer risk estimation. Radiat Environ Biophys. 48:275–286.
   PubMed Web of Science ®Google Scholar
• Shuryak I, Sachs RK, Brenner DJ. 2010. Cancer risks after radiation exposure in middle age. J Natl Cancer Inst. 102:1628–1636.
   PubMed Web of Science ®Google Scholar
• Spycher BD, Lupatsch JE, Zwahlen M, Röösli M, Niggli F, Grotzer MA, Rischewski J, Egger M, Kuehni CE. 2015. Background ionizing radiation and the risk of childhood cancer: a census-based nationwide cohort study. Environ Health Perspect. 123:622–628.
   PubMed Web of Science ®Google Scholar
• Tomasetti C, Vogelstein B, Parmigiani G. 2013. Half or more of the somatic mutations in cancers of self-renewing tissues originate prior to tumor initiation. Proc Natl Acad Sci USA. 110:1999–2004.
   PubMed Web of Science ®Google Scholar
• Tomasetti C, Marchionni L, Nowak MA, Parmigiani G, Vogelstein B. 2015. Only three driver gene mutations are required for the development of lung and colorectal cancers. Proc Natl Acad Sci USA. 112:118–123.
   PubMed Web of Science ®Google Scholar
• Tomasetti C, Vogelstein B. 2015. Cancer etiology. Variation in cancer risk among tissues can be explained by the number of stem cell divisions. Science. 347:78–81.
   PubMed Web of Science ®Google Scholar
• United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR). 2012. UNSCEAR 2012 Report to the General Assembly, with scientific annexes. Available from: http://www.unscear.org/unscear/en/publications/2012.html
   Google Scholar
• Van Dillen T, Dekkers F, Bijwaard H, Kreuzer M, Grosche B. 2011. Lung cancer from radon: a two-stage model analysis of the WISMUT cohort, 1955–1998. Radiat Res. 175:119–130.
   PubMed Web of Science ®Google Scholar
• Wakeford R, Little MP. 2003. Risk coefficients for childhood cancer after intrauterine irradiation: a review. Int J Radiat Biol. 79:293–309.
   PubMed Web of Science ®Google Scholar
• Walsh L, Kaiser JC. 2011. Multi-model inference of adult and childhood leukaemia excess relative risks based on the Japanese A-bomb survivors’ mortality data (1950–2000). Radiat Environ Biophys. 50:21–35.
   PubMed Web of Science ®Google Scholar
• Wu S, Powers S, Zhu W, Hannun YA. 2016. Substantial contribution of extrinsic risk factors to cancer development. Nature. 529:43–47.
   PubMed Web of Science ®Google Scholar
• Zaballa I, Eidemüller M. 2016. Mechanistic study on lung cancer mortality after radon exposure in the Wismut cohort supports important role of clonal expansion in lung carcinogenesis. Radiat Environ Biophys. 55:299–315.
   PubMed Web of Science ®Google Scholar
• Zöllner S, Sokolnikov ME, Eidemüller M. 2015. Beyond two-stage models for lung carcinogenesis in the Mayak workers: implications for plutonium risk. PLoS One. 10:e0126238.
   PubMed Web of Science ®Google Scholar