Understanding the health effects of low doses of ionizing radiation from medical procedures: challenges for epidemiology
- Autores: Elisa Pasqual
- Directores de la Tesis: Elisabeth Cardis (dir. tes.), Isabelle Thierry Chef (codir. tes.)
- Lectura: En la Universitat Pompeu Fabra ( España ) en 2019
- Idioma: español
- Tribunal Calificador de la Tesis: Florent de Vathaire (presid.), Martine Vrijheid (secret.), Mark S. Pearce (voc.)
- Programa de doctorado: Programa de Doctorado en Biomedicina por la Universidad Pompeu Fabra
- Materias:
- Enlaces
- Tesis en acceso abierto en: TDX
- Resumen
The application of ionising radiation (IR) in the medical sector is undoubtedly lifesaving. There are, however, risks associated with IR and there is growing concern among public health and radiation protection experts, in particular for the increasing medical radiological exposure in children. The aim of this dissertation is to contribute to a better characterisation of the IR risk in patients.
A hospital-based cohort study of childhood cancer survivors was developed as a basis for future analysis and, nested within the cohort, a cross-sectional study on neurodevelopmental effect after non-cranial radiotherapy was implemented. A descriptive analysis of the mental health status of the cohort is presented here.
The association between cumulative IR from medical diagnostic procedures and cancer (adult lymphoma and childhood/adolescent brain cancer), in two large international case-control studies, were estimated and a dosimetry estimation was developed.
Evidence of a neurodevelopmental effect at low-to moderate IR dose was synthesized in a systematic review and was found to be limited to inadequate.
The estimated effect at this low dose range requires greater effort from epidemiologists to design more informative studies, and collaboration with clinicians is key for future research in radiation epidemiology.
The main conclusions of the present thesis are: This dissertation explored the effects of medical Ionizing Radiation exposure. In summary, the thesis showed: a) Very little evidence of increased risk of brain tumour in young people and no clear evidence of an effect of lymphoma in adults after exposure to common diagnostic examinations.
b) The brain absorbed dose from dental X-rays and paediatric skull and neck X-rays have decreased over time. The contribution to the cumulative dose of these procedures is very small, and consequently it is extremely difficult to detect any increased health risk.
c) The evidence for neurodevelopmental impairment after exposure to low to moderate IR exposure, especially for the general cognition and the language domain was limited.
d) There was inadequate evidence that exposure during foetal and early life might bear a higher risk of brain cancer and neurodevelopmental impairment compared to postnatal exposure.
e) Establishing and fostering a long term follow up for childhood cancer survivors in Spain is feasible and is needed to contribute to this important research field.
f) The mental health status of the hospital-based Childhood Cancer Survivors cohort was comparable to that of the large US cohort of CCSs. Lower mental health was found for those reporting suffering from any chronic medical conditions, pointing to the importance of a clinical surveillance of this population Bibliography: Adams MJ, Shore RE, Dozier A, Lipshultz SE, Schwartz RG, Constine LS, et al. Thyroid cancer risk 40+ years after irradiation for an enlarged thymus: an update of the Hempelmann cohort. Radiat Res 2010;174:753–62. doi:10.1667/RR2181.1.
Alemany S, Vilor-Tejedor N, García-Esteban R, Bustamante M, Dadvand P, Esnaola M, et al. Traffic-Related Air Pollution, APOEε4 Status, and Neurodevelopmental Outcomes among School Children Enrolled in the BREATHE Project (Catalonia, Spain). Environ Health Perspect 2018;126:087001. doi:10.1289/EHP2246.
Allodji RS, Haddy N, Vu-Bezin G, Dumas A, Fresneau B, Mansouri I, et al. Risk of subsequent colorectal cancers after a solid tumor in childhood: Effects of radiation therapy and chemotherapy. Pediatr Blood Cancer 2019;66:e27495. doi:10.1002/pbc.27495.
Armenian SH, Robison LL. Childhood cancer survivorship: an update on evolving paradigms for understanding pathogenesis and screening for therapy-related late effects. Curr Opin Pediatr 2013;25:16–22. doi:10.1097/MOP.0b013e32835b0b6a.
Asdahl PH, Winther JF, Bonnesen TG, De Fine Licht S, Gudmundsdottir T, Anderson H, et al. The Adult Life After Childhood Cancer in Scandinavia (ALiCCS) Study: Design and Characteristics. Pediatr Blood Cancer 2015;62:2204–10. doi:10.1002/pbc.25661.
Baerlocher MO, Talanow R, Baerlocher AF. Radiation passport: an iPhone and iPod touch application to track radiation dose and estimate associated cancer risks. J Am Coll Radiol 2010;7:277–80. doi:10.1016/j.jacr.2009.09.016.
Benadjaoud MA, Bezin J, Veres A, Lefkopoulos D, Chavaudra J, Bridier A, et al. A multi-plane source model for out-of-field head scatter dose calculations in external beam photon therapy. Phys Med Biol 2012;57:7725–39. doi:10.1088/0031-9155/57/22/7725.
Berkson J. Are There Two Regressions? Journal of the American Statistical Association 1950;45:164–80.
Bernier M-O, Baysson H, Pearce MS, Moissonnier M, Cardis E, Hauptmann M, et al. Cohort Profile: the EPI-CT study: A European pooled epidemiological study to quantify the risk of radiation-induced cancer from paediatric CT. Int J Epidemiol 2018. doi:10.1093/ije/dyy231.
Bernier M-O, Journy N, Baysson H, Jacob S, Laurier D. Potential cancer risk associated with CT scans: Review of epidemiological studies and ongoing studies. Progress in Nuclear Energy 2015;84:116–9. doi:10.1016/j.pnucene.2014.07.011.
Berrington de González A, Darby S. Risk of cancer from diagnostic X-rays: estimates for the UK and 14 other countries. Lancet 2004a;363:345–51. doi:10.1016/S0140-6736(04)15433-0.
Berrington de González A, Darby S. Risk of cancer from diagnostic X-rays: estimates for the UK and 14 other countries. Lancet 2004b;363:345–51. doi:10.1016/S0140-6736(04)15433-0.
Berrington de Gonzalez A, Ekbom A, Glass AG, Galanti MR, Grimelius L, Allison MJ, et al. Comparison of documented and recalled histories of exposure to diagnostic x-rays in case-control studies of thyroid cancer. Am J Epidemiol 2003;157:652–63.
Berrington de Gonzalez A, Gilbert E, Curtis R, Inskip P, Kleinerman R, Morton L, et al. Second solid cancers after radiation therapy: a systematic review of the epidemiologic studies of the radiation dose-response relationship. Int J Radiat Oncol Biol Phys 2013;86:224–33. doi:10.1016/j.ijrobp.2012.09.001.
Berrington de Gonzalez A, Journy N, Lee C, Morton LM, Harbron R, Stewart DR, et al. No association between radiation dose from pediatric CT scans and risk of subsequent Hodgkin lymphoma. Cancer Epidemiol Biomarkers Prev 2017. doi:10.1158/1055-9965.EPI-16-1011.
Berrington de Gonzalez A, Salotti JA, McHugh K, Little MP, Harbron RW, Lee C, et al. Relationship between paediatric CT scans and subsequent risk of leukaemia and brain tumours: assessment of the impact of underlying conditions. Br J Cancer 2016;114:388–94. doi:10.1038/bjc.2015.415.
Bezin JV, Veres A, Lefkopoulos D, Chavaudra J, Deutsch E, de Vathaire F, et al. Field size dependent mapping of medical linear accelerator radiation leakage. Phys Med Biol 2015;60:2103–6. doi:10.1088/0031-9155/60/5/2103.
Bhatia S, Armenian SH, Armstrong GT, van Dulmen-den Broeder E, Hawkins MM, Kremer LCM, et al. Collaborative Research in Childhood Cancer Survivorship: The Current Landscape. J Clin Oncol 2015;33:3055–64. doi:10.1200/JCO.2014.59.8052.
Bithell JF, Stewart AM. Pre-natal irradiation and childhood malignancy: a review of British data from the Oxford Survey. Br J Cancer 1975;31:271–87.
Black SE, Bütikofer A, Devereux PJ, Salvanes KG. This Is Only a Test? Long-Run Impacts of Prenatal Exposure to Radioactive Fallout. National Bureau of Economic Research; 2013. doi:10.3386/w18987.
Blomstrand M, Holmberg E, Aberg MAI, Lundell M, Björk-Eriksson T, Karlsson P, et al. No clinically relevant effect on cognitive outcomes after low-dose radiation to the infant brain: a population-based cohort study in Sweden. Acta Oncol 2014;53:1143–50. doi:10.3109/0284186X.2014.899434.
Boice JD. Radiation epidemiology and recent paediatric computed tomography studies. Ann ICRP 2015;44:236–48. doi:10.1177/0146645315575877.
Boice JD, Morin MM, Glass AG, Friedman GD, Stovall M, Hoover RN, et al. Diagnostic x-ray procedures and risk of leukemia, lymphoma, and multiple myeloma. JAMA 1991;265:1290–4.
Boice JD, Rosenstein M, Trout ED. Estimation of breast doses and breast cancer risk associated with repeated fluoroscopic chest examinations of women with tuberculosis. Radiat Res 1978;73:373–90.
Bosch de Basea M, Moriña D, Figuerola J, Barber I, Muchart J, Lee C, et al. Subtle excess in lifetime cancer risk related to CT scanning in Spanish young people. Environ Int 2018;120:1–10. doi:10.1016/j.envint.2018.07.020.
Bosch de Basea M, Pearce MS, Kesminiene A, Bernier M-O, Dabin J, Engels H, et al. EPI-CT: design, challenges and epidemiological methods of an international study on cancer risk after paediatric and young adult CT. Journal of Radiological Protection 2015;35:611–28. doi:10.1088/0952-4746/35/3/611.
Brenner DJ, Doll R, Goodhead DT, Hall EJ, Land CE, Little JB, et al. Cancer risks attributable to low doses of ionizing radiation: assessing what we really know. Proc Natl Acad Sci USA 2003;100:13761–6. doi:10.1073/pnas.2235592100.
Burtt JJ, Thompson PA, Lafrenie RM. Non-targeted effects and radiation-induced carcinogenesis: a review. J Radiol Prot 2016;36:R23-35. doi:10.1088/0952-4746/36/1/R23.
Cardis E, Vrijheid M, Blettner M, Gilbert E, Hakama M, Hill C, et al. The 15-Country Collaborative Study of Cancer Risk among Radiation Workers in the Nuclear Industry: estimates of radiation-related cancer risks. Radiat Res 2007;167:396–416. doi:10.1667/RR0553.1.
Cardis E, Vrijheid M, Blettner M, Gilbert E, Hakama M, Hill C, et al. Risk of cancer after low doses of ionising radiation: retrospective cohort study in 15 countries. BMJ 2005;331:77. doi:10.1136/bmj.38499.599861.E0.
Chang DS, Lasley FD, Das IJ, Mendonca MS, Dynlacht JR. Oxygen Effect, Relative Biological Effectiveness and Linear Energy Transfer. In: Chang DS, Lasley FD, Das IJ, Mendonca MS, Dynlacht JR, editors. Basic Radiotherapy Physics and Biology, Cham: Springer International Publishing; 2014, p. 235–40. doi:10.1007/978-3-319-06841-1_22.
Childhood Cancer Survivor Study: An Overview. National Cancer Institute 2007. https://www.cancer.gov/types/childhood-cancers/ccss (accessed July 12, 2019).
Claus EB, Calvocoressi L, Bondy ML, Schildkraut JM, Wiemels JL, Wrensch M. Dental x-rays and risk of meningioma. Cancer 2012;118:4530–7. doi:10.1002/cncr.26625.
COG. Long-Term Follow-Up Guidelines for Survivors of Childhood, Adolescent and Young Adult Cancers". Children’s Oncology Group; 2018.
Darby SC, Doll R, Gill SK, Smith PG. Long term mortality after a single treatment course with X-rays in patients treated for ankylosing spondylitis. Br J Cancer 1987;55:179–90.
Davis FG, Boice JD, Hrubec Z, Monson RR. Cancer mortality in a radiation-exposed cohort of Massachusetts tuberculosis patients. Cancer Res 1989;49:6130–6.
Davis FG, Yu KL, Preston D, Epifanova S, Degteva M, Akleyev AV. Solid Cancer Incidence in the Techa River Incidence Cohort: 1956-2007. Radiat Res 2015;184:56–65. doi:10.1667/RR14023.1.
Doll R, Wakeford R. Risk of childhood cancer from fetal irradiation. Br J Radiol 1997;70:130–9. doi:10.1259/bjr.70.830.9135438.
Dose DataMed II. Dose DataMed II 2015. http://ddmed.eu/ (accessed September 30, 2016).
Dreger S, Poettgen S, Samkange-Zeeb F, Merzenich H, Ningo A, Breckow J, et al. Retrospective assessment of self-reported exposure to medical ionizing radiation: results of a feasibility study conducted in Germany. BMC Research Notes 2015;8. doi:10.1186/s13104-015-1268-8.
Eidemüller M, Holmberg E, Jacob P, Lundell M, Karlsson P. Breast cancer risk and possible mechanisms of radiation-induced genomic instability in the Swedish hemangioma cohort after reanalyzed dosimetry. Mutat Res 2015;775:1–9. doi:10.1016/j.mrfmmm.2015.03.002.
EURAMED. Common strategic research agenda for radiation protection in medicine. Insights Imaging 2017;8:183–97. doi:10.1007/s13244-016-0538-x.
European Commision. Directive 2013/59/Euratom - protection against ionising radiation - Safety and health at work - EU-OSHA 2013. https://osha.europa.eu/en/legislation/directives/directive-2013-59-euratom-protection-against-ionising-radiation (accessed August 30, 2019).
Evrard A-S, Hémon D, Billon S, Laurier D, Jougla E, Tirmarche M, et al. Childhood leukemia incidence and exposure to indoor radon, terrestrial and cosmic gamma radiation. Health Phys 2006;90:569–79. doi:10.1097/01.HP.0000198787.93305.35.
Fazel R, Krumholz HM, Wang Y, Ross JS, Chen J, Ting HH, et al. Exposure to low-dose ionizing radiation from medical imaging procedures. N Engl J Med 2009;361:849–57. doi:10.1056/NEJMoa0901249.
Feldman A. A sketch of the technical history of radiology from 1896 to 1920. RadioGraphics 1989;9:1113–28. doi:10.1148/radiographics.9.6.2685937.
Frush DP, Donnelly LF, Rosen NS. Computed Tomography and Radiation Risks: What Pediatric Health Care Providers Should Know. Pediatrics 2003;112:951–7. doi:10.1542/peds.112.4.951.
Gatta G, Botta L, Rossi S, Aareleid T, Bielska-Lasota M, Clavel J, et al. Childhood cancer survival in Europe 1999–2007: results of EUROCARE-5—a population-based study. The Lancet Oncology 2014;15:35–47. doi:10.1016/S1470-2045(13)70548-5.
Gatta G, Capocaccia R, Stiller C, Kaatsch P, Berrino F, Terenziani M, et al. Childhood cancer survival trends in Europe: a EUROCARE Working Group study. J Clin Oncol 2005;23:3742–51. doi:10.1200/JCO.2005.00.554.
van der Geest IMM, van Dorp W, Hop WCJ, Neggers SJCMM, de Vries ACH, Pieters R, et al. Emotional distress in 652 Dutch very long-term survivors of childhood cancer, using the hospital anxiety and depression scale (HADS). J Pediatr Hematol Oncol 2013;35:525–9. doi:10.1097/MPH.0b013e31829f2799.
Grabow D, Kaiser M, Hjorth L, Byrne J, Alessi D, Allodji RS, et al. The PanCareSurFup cohort of 83,333 five-year survivors of childhood cancer: a cohort from 12 European countries. Eur J Epidemiol 2018;33:335–49. doi:10.1007/s10654-018-0370-3.
Graignic-Philippe R, Dayan J, Chokron S, Jacquet A-Y, Tordjman S. Effects of prenatal stress on fetal and child development: A critical literature review. Neuroscience & Biobehavioral Reviews 2014;43:137–62. doi:10.1016/j.neubiorev.2014.03.022.
Grant EJ, Brenner A, Sugiyama H, Sakata R, Sadakane A, Utada M, et al. Solid Cancer Incidence among the Life Span Study of Atomic Bomb Survivors: 1958-2009. Radiat Res 2017;187:513–37. doi:10.1667/RR14492.1.
Guyatt GH, Oxman AD, Schünemann HJ, Tugwell P, Knottnerus A. GRADE guidelines: a new series of articles in the Journal of Clinical Epidemiology. J Clin Epidemiol 2011;64:380–2. doi:10.1016/j.jclinepi.2010.09.011.
Hall J, Jeggo PA, West C, Gomolka M, Quintens R, Badie C, et al. Ionizing radiation biomarkers in epidemiological studies - An update. Mutat Res 2017;771:59–84. doi:10.1016/j.mrrev.2017.01.001.
Hall P, Adami H-O, Trichopoulos D, Pedersen NL, Lagiou P, Ekbom A, et al. Effect of low doses of ionising radiation in infancy on cognitive function in adulthood: Swedish population based cohort study. BMJ 2004;328:19. doi:10.1136/bmj.328.7430.19.
Hammer GP, Seidenbusch MC, Regulla DF, Spix C, Zeeb H, Schneider K, et al. Childhood cancer risk from conventional radiographic examinations for selected referral criteria: results from a large cohort study. AJR Am J Roentgenol 2011;197:217–23. doi:10.2214/AJR.10.4979.
Hamra GB, Richardson DB, Cardis E, Daniels RD, Gillies M, O’Hagan JA, et al. Cohort Profile: The International Nuclear Workers Study (INWORKS). Int J Epidemiol 2015. doi:10.1093/ije/dyv122.
Haupt R, Essiaf S, Dellacasa C, Ronckers CM, Caruso S, Sugden E, et al. The “Survivorship Passport” for childhood cancer survivors. Eur J Cancer 2018;102:69–81. doi:10.1016/j.ejca.2018.07.006.
HLEG. High level and expert group on european low dose risk research. High level and expert group report on european low dose risk research—Radiation protection. European Commission EUR 23884; 2009.
Howe GR. Lung cancer mortality between 1950 and 1987 after exposure to fractionated moderate-dose-rate ionizing radiation in the Canadian fluoroscopy cohort study and a comparison with lung cancer mortality in the Atomic Bomb survivors study. Radiat Res 1995;142:295–304.
Hsu W-L, Preston DL, Soda M, Sugiyama H, Funamoto S, Kodama K, et al. The incidence of leukemia, lymphoma and multiple myeloma among atomic bomb survivors: 1950-2001. Radiat Res 2013;179:361–82. doi:10.1667/RR2892.1.
Huang L, Snyder AR, Morgan WF. Radiation-induced genomic instability and its implications for radiation carcinogenesis. Oncogene 2003;22:5848–54. doi:10.1038/sj.onc.1206697.
Huang W-Y, Muo C-H, Lin C-Y, Jen Y-M, Yang M-H, Lin J-C, et al. Paediatric head CT scan and subsequent risk of malignancy and benign brain tumour: a nation-wide population-based cohort study. British Journal of Cancer 2014;110:2354–60. doi:10.1038/bjc.2014.103.
IAEA, WHO. Bonn Call for Action: 10 Actions to Improve Radiation Protection in Medicine in the Next Decade 2012.
IARC. World Cancer Report 2014. IARC E-Bookshop 2014. http://shop.iarc.fr/products/wcr2014 (accessed October 11, 2016).
ICRP. ICRP Publication 103. Recommendations of the International Commission on Radiological Protection. Oxford: Pergamon: ICRP; 2007a.
ICRP. The 2007 Recommendations of the International Commission on Radiological Protection. 2007b.
ICRP. Low-dose Extrapolation of Radiation-related Cancer Risk. International Commission on Radiological Protection. Pergamon Press; 2005.
ICRP. The Use of Effective Dose as a Radiological Protection Quantity. ICRP; In press.
Institut Curie. Marie Curie: the fight goes on. Institut Curie 2019. https://institut-curie.org/actualite/openness/marie-curie-fight-goes (accessed August 30, 2019).
Jain J, Qorri B, Szewczuk MR. The crucial role of primary care providers in the long-term follow-up of adult survivors of childhood cancer. Cancer Manag Res 2019;11:3411–8. doi:10.2147/CMAR.S197644.
Jankovic M, Haupt R, Spinetta JJ, Beck JD, Byrne J, Calaminus G, et al. Long-term survivors of childhood cancer: cure and care-the Erice Statement (2006) revised after 10 years (2016). J Cancer Surviv 2018;12:647–50. doi:10.1007/s11764-018-0701-0.
Jiang M, Bennani NN, Feldman AL. Lymphoma classification update: T-cell lymphomas, Hodgkin lymphomas, and histiocytic/dendritic cell neoplasms. Expert Rev Hematol 2017a;10:239–49. doi:10.1080/17474086.2017.1281122.
Jiang M, Bennani NN, Feldman AL. Lymphoma classification update: B-cell non-Hodgkin lymphomas. Expert Rev Hematol 2017b;10:405–15. doi:10.1080/17474086.2017.1318053.
Johnson PI, Sutton P, Atchley DS, Koustas E, Lam J, Sen S, et al. The Navigation Guide - evidence-based medicine meets environmental health: systematic review of human evidence for PFOA effects on fetal growth. Environ Health Perspect 2014;122:1028–39. doi:10.1289/ehp.1307893.
Journy, Lee C, Harbron RW, McHugh K, Pearce MS, Berrington de González A. Projected cancer risks potentially related to past, current, and future practices in paediatric CT in the United Kingdom, 1990-2020. Br J Cancer 2017;116:109–16. doi:10.1038/bjc.2016.351.
Journy N, Roué T, Cardis E, Le Pointe HD, Brisse H, Chateil J-F, et al. Childhood CT scans and cancer risk: impact of predisposing factors for cancer on the risk estimates. J Radiol Prot 2016;36:N1-7. doi:10.1088/0952-4746/36/1/N1.
Kadhim M, Salomaa S, Wright E, Hildebrandt G, Belyakov OV, Prise KM, et al. Non-targeted effects of ionising radiation-Implications for low dose risk. Mutat Res 2013;752:84–98. doi:10.1016/j.mrrev.2012.12.001.
Karlsson P, Holmberg E, Lundell M, Mattsson A, Holm LE, Wallgren A. Intracranial tumors after exposure to ionizing radiation during infancy: a pooled analysis of two Swedish cohorts of 28,008 infants with skin hemangioma. Radiat Res 1998;150:357–64.
Kashcheev VV, Chekin SY, Maksioutov MA, Tumanov KA, Kochergina EV, Kashcheeva PV, et al. Incidence and mortality of solid cancer among emergency workers of the Chernobyl accident: assessment of radiation risks for the follow-up period of 1992-2009. Radiat Environ Biophys 2015;54:13–23. doi:10.1007/s00411-014-0572-3.
Kempf SJ, Azimzadeh O, Atkinson MJ, Tapio S. Long-term effects of ionising radiation on the brain: cause for concern? Radiat Environ Biophys 2013;52:5–16. doi:10.1007/s00411-012-0436-7.
Kitahara CM, Berrington de Gonzalez A, Bouville A, Brill AB, Doody MM, Melo DR, et al. Association of Radioactive Iodine Treatment With Cancer Mortality in Patients With Hyperthyroidism. JAMA Intern Med 2019. doi:10.1001/jamainternmed.2019.0981.
Kleinerman RA. Cancer risks following diagnostic and therapeutic radiation exposure in children. Pediatric Radiology 2006;36:121–5. doi:10.1007/s00247-006-0191-5.
Krestinina LY, Davis FG, Schonfeld S, Preston DL, Degteva M, Epifanova S, et al. Leukaemia incidence in the Techa River Cohort: 1953-2007. Br J Cancer 2013;109:2886–93. doi:10.1038/bjc.2013.614.
Kreuzer M, Auvinen A, Bouffler S, Cardis E, Durante M, Jourdain J-R, et al. MELODI Strategic Research Agenda 2017. The MELODI Platform; 2017.
Krille L, Dreger S, Schindel R, Albrecht T, Asmussen M, Barkhausen J, et al. Risk of cancer incidence before the age of 15 years after exposure to ionising radiation from computed tomography: results from a German cohort study. Radiation and Environmental Biophysics 2015;54:1–12. doi:10.1007/s00411-014-0580-3.
Krille L, Zeeb H, Jahnen A, Mildenberger P, Seidenbusch M, Schneider K, et al. Computed tomographies and cancer risk in children: a literature overview of CT practices, risk estimations and an epidemiologic cohort study proposal. Radiation and Environmental Biophysics 2012;51:103–11. doi:10.1007/s00411-012-0405-1.
Krull KR, Sabin ND, Reddick WE, Zhu L, Armstrong GT, Green DM, et al. Neurocognitive function and CNS integrity in adult survivors of childhood hodgkin lymphoma. J Clin Oncol 2012;30:3618–24. doi:10.1200/JCO.2012.42.6841.
Land CE. Estimating cancer risks from low doses of ionizing radiation. Science 1980;209:1197–203.
Larson SM, Carrasquillo JA, Cheung N-KV, Press O. Radioimmunotherapy of human tumours. Nat Rev Cancer 2015;15:347–60. doi:10.1038/nrc3925.
Lee C, Journy N, Moroz BE, Little M, Harbron R, McHugh K, et al. Organ dose estimation accounting for uncertainty for pediatric and young adult ct scans in the united kingdom. Radiat Prot Dosimetry 2018. doi:10.1093/rpd/ncy184.
Leuraud K, Richardson DB, Cardis E, Daniels RD, Gillies M, O’Hagan JA, et al. Ionising radiation and risk of death from leukaemia and lymphoma in radiation-monitored workers (INWORKS): an international cohort study. Lancet Haematol 2015;2:e276-281. doi:10.1016/S2352-3026(15)00094-0.
Lindberg S, Karlsson P, Arvidsson B, Holmberg E, Lunberg LM, Wallgren A. Cancer incidence after radiotherapy for skin haemangioma during infancy. Acta Oncol 1995;34:735–40.
Lindor NM, McMaster ML, Lindor CJ, Greene MH. Concise Handbook of Familial Cancer Susceptibility Syndromes - Second Edition. J Natl Cancer Inst Monogr 2008;2008:3–93. doi:10.1093/jncimonographs/lgn001.
Linet MS, Freedman DM, Mohan AK, Doody MM, Ron E, Mabuchi K, et al. Incidence of haematopoietic malignancies in US radiologic technologists. Occup Environ Med 2005;62:861–7. doi:10.1136/oem.2005.020826.
Linet MS, Kim K pyo, Rajaraman P. Children’s exposure to diagnostic medical radiation and cancer risk: epidemiologic and dosimetric considerations. Pediatric Radiology 2009;39:S4–26. doi:10.1007/s00247-008-1026-3.
Linet MS, Slovis TL, Miller DL, Kleinerman R, Lee C, Rajaraman P, et al. Cancer risks associated with external radiation from diagnostic imaging procedures. CA Cancer J Clin 2012;62:75–100. doi:10.3322/caac.21132.
Little MP, Zablotska LB, Brenner AV, Lipshultz SE. Circulatory disease mortality in the Massachusetts tuberculosis fluoroscopy cohort study. Eur J Epidemiol 2016;31:287–309. doi:10.1007/s10654-015-0075-9.
Lundell M, Fürst CJ, Hedlund B, Holm LE. Radium treatment for hemangioma in early childhood. Reconstruction and dosimetry of treatments, 1920-1959. Acta Oncol 1990;29:551–6.
Lundell M, Holm LE. Mortality from leukemia after irradiation in infancy for skin hemangioma. Radiat Res 1996;145:595–601.
March HC. Leukemia in radiologists in a 20 year period. Am J Med Sci 1950;220:282–6.
Mathews JD, Forsythe AV, Brady Z, Butler MW, Goergen SK, Byrnes GB, et al. Cancer risk in 680 000 people exposed to computed tomography scans in childhood or adolescence: data linkage study of 11 million Australians. BMJ 2013;346:f2360–f2360. doi:10.1136/bmj.f2360.
McLean AR, Adlen EK, Cardis E, Elliott A, Goodhead DT, Harms-Ringdahl M, et al. A restatement of the natural science evidence base concerning the health effects of low-level ionizing radiation. Proc Biol Sci 2017a;284. doi:10.1098/rspb.2017.1070.
McLean AR, Adlen EK, Cardis E, Elliott A, Goodhead DT, Harms-Ringdahl M, et al. A restatement of the natural science evidence base concerning the health effects of low-level ionizing radiation. Proc Biol Sci 2017b;284. doi:10.1098/rspb.2017.1070.
Melo DR, Brill AB, Zanzonico P, Vicini P, Moroz B, Kwon D, et al. Organ Dose Estimates for Hyperthyroid Patients Treated with 131 I: An Update of the Thyrotoxicosis Follow-Up Study. Radiation Research 2015;184:595–610. doi:10.1667/RR14160.1.
MELODI. MELODI Statement and priorities 2015 2015. http://www.melodi-online.eu/doc/MELODI%20Statement%20and%20priorities%2010082015.pdf (accessed January 12, 2016).
Mettler Jr FA, Huda W, Yoshizumi TT, Mahesh M. Effective Doses in Radiology and Diagnostic Nuclear Medicine: A Catalog 1. Radiology 2008;248:254–263.
Meulepas JM, Ronckers CM, Smets AMJB, Nievelstein RAJ, Gradowska P, Lee C, et al. Radiation Exposure From Pediatric CT Scans and Subsequent Cancer Risk in the Netherlands. J Natl Cancer Inst 2019;111:256–63. doi:10.1093/jnci/djy104.
Milbank D. Opinion | Radiation? Chemicals? No big deal, says the Trump administration. Washington Post 2018.
Miller AB, Howe GR, Sherman GJ, Lindsay JP, Yaffe MJ, Dinner PJ, et al. Mortality from breast cancer after irradiation during fluoroscopic examinations in patients being treated for tuberculosis. N Engl J Med 1989;321:1285–9. doi:10.1056/NEJM198911093211902.
Mohan AK, Hauptmann M, Freedman DM, Ron E, Matanoski GM, Lubin JH, et al. Cancer and other causes of mortality among radiologic technologists in the United States. Int J Cancer 2003;103:259–67. doi:10.1002/ijc.10811.
Moore K, Persaud TVN. The Developing Human - 10th Edition. 10th ed. Saunders; 2015.
Morgan RL, Thayer KA, Bero L, Bruce N, Falck-Ytter Y, Ghersi D, et al. GRADE: Assessing the quality of evidence in environmental and occupational health. Environ Int 2016;92–93:611–6. doi:10.1016/j.envint.2016.01.004.
Morton LM, Slager SL, Cerhan JR, Wang SS, Vajdic CM, Skibola CF, et al. Etiologic Heterogeneity Among Non-Hodgkin Lymphoma Subtypes: The InterLymph Non-Hodgkin Lymphoma Subtypes Project. J Natl Cancer Inst Monogr 2014a;2014:130–44. doi:10.1093/jncimonographs/lgu013.
Morton LM, Swerdlow AJ, Schaapveld M, Ramadan S, Hodgson DC, Radford J, et al. Current knowledge and future research directions in treatment-related second primary malignancies. EJC Suppl 2014b;12:5–17. doi:10.1016/j.ejcsup.2014.05.001.
Mulvihill DJ, Jhawar S, Kostis JB, Goyal S. Diagnostic Medical Imaging in Pediatric Patients and Subsequent Cancer Risk. Acad Radiol 2017;24:1456–62. doi:10.1016/j.acra.2017.05.009.
National Research Council (U.S.), editor. Health risks from exposure to low levels of ionizing radiation: BEIR VII Phase 2. Washington, D.C: National Academies Press; 2006.
NCRP Report No. 160. Ionizing Radiation Exposure of the Population of the United State. 2009.
Nordenskjöld AC, Palme M, Kaijser M. X-ray exposure in utero and school performance: a population-based study of X-ray pelvimetry. Clin Radiol 2015;70:830–4. doi:10.1016/j.crad.2015.04.002.
Ozasa K. Epidemiological research on radiation-induced cancer in atomic bomb survivors. J Radiat Res 2016. doi:10.1093/jrr/rrw005.
Ozasa K, Cullings HM, Ohishi W, Hida A, Grant EJ. Epidemiological studies of atomic bomb radiation at the Radiation Effects Research Foundation. Int J Radiat Biol 2019;95:879–91. doi:10.1080/09553002.2019.1569778.
Ozasa K, Grant EJ, Kodama K. Japanese Legacy Cohorts: The Life Span Study Atomic Bomb Survivor Cohort and Survivors’ Offspring. J Epidemiol 2018;28:162–9. doi:10.2188/jea.JE20170321.
Ozasa K, Shimizu Y, Suyama A, Kasagi F, Soda M, Grant EJ, et al. Studies of the mortality of atomic bomb survivors, Report 14, 1950-2003: an overview of cancer and noncancer diseases. Radiat Res 2012;177:229–43.
Padovani L, André N, Constine LS, Muracciole X. Neurocognitive function after radiotherapy for paediatric brain tumours. Nat Rev Neurol 2012;8:578–88. doi:10.1038/nrneurol.2012.182.
PDQ Pediatric Treatment Editorial Board. Late Effects of Treatment for Childhood Cancer (PDQ®): Health Professional Version. PDQ Cancer Information Summaries, Bethesda (MD): National Cancer Institute (US); 2002.
Pearce MS. Patterns in paediatric CT use: An international and epidemiological perspective: Editorial. Journal of Medical Imaging and Radiation Oncology 2011;55:107–9. doi:10.1111/j.1754-9485.2011.02240.x.
Pearce MS, Salotti JA, Little MP, McHugh K, Lee C, Kim KP, et al. Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. The Lancet 2012a;380:499–505.
Pearce MS, Salotti JA, Little MP, McHugh K, Lee C, Kim KP, et al. CT scans in childhood and risk of leukaemia and brain tumours–Authors’ reply. The Lancet 2012b;380:1736–1737.
Pogoda JM, Nichols PW, Ross RK, Stram DO, Thomas DC, Preston-Martin S. Diagnostic radiography and adult acute myeloid leukaemia: an interview and medical chart review study. Br J Cancer 2011;104:1482–6. doi:10.1038/bjc.2011.114.
Polednak AP, Stehney AF, Rowland RE. Mortality among women first employed before 1930 in the U.S. radium dial-painting industry. A group ascertained from employment lists. Am J Epidemiol 1978;107:179–95. doi:10.1093/oxfordjournals.aje.a112524.
Popay J, Roberts H, Sowden A, Petticrew M, Arai L, Rodgers M, et al. Guidance on the Conduct of Narrative Synthesis in Systematic Reviews 2006:92.
Preston DL, Pierce DA, Shimizu Y, Ron E, Mabuchi K. Dose response and temporal patterns of radiation-associated solid cancer risks. Health Phys 2003;85:43–6.
Preston DL, Ron E, Yonehara S, Kobuke T, Fujii H, Kishikawa M, et al. Tumors of the nervous system and pituitary gland associated with atomic bomb radiation exposure. Journal of the National Cancer Institute 2002;94:1555–63.
Preston-Martin S, Mack W, Henderson BE. Risk factors for gliomas and meningiomas in males in Los Angeles County. Cancer Res 1989;49:6137–43.
Preston-Martin S, Pogoda JM. Estimation of radiographic doses in a case-control study of acute myelogenous leukemia. Health Phys 2003;84:245–59.
Preston-Martin S, Thomas DC, White SC, Cohen D. Prior exposure to medical and dental x-rays related to tumors of the parotid gland. J Natl Cancer Inst 1988;80:943–9. doi:10.1093/jnci/80.12.943.
PROCARDIO study group. Final Report Summary - PROCARDIO (Cardiovascular Risk from Exposure to Low-dose and Low-dose-rate Ionizing Radiation) | Report Summary | PROCARDIO | FP7 | CORDIS | European Commission 2015. https://cordis.europa.eu/project/rcn/100539/reporting/en (accessed August 3, 2019).
Reynolds K, Spavor M, Brandelli Y, Kwok C, Li Y, Disciglio M, et al. A comparison of two models of follow-up care for adult survivors of childhood cancer. J Cancer Surviv 2019. doi:10.1007/s11764-019-00774-w.
Richardson DB, Cardis E, Daniels RD, Gillies M, O’Hagan JA, Hamra GB, et al. Risk of cancer from occupational exposure to ionising radiation: retrospective cohort study of workers in France, the United Kingdom, and the United States (INWORKS). BMJ 2015;351:h5359. doi:10.1136/bmj.h5359.
Robison LL, Armstrong GT, Boice JD, Chow EJ, Davies SM, Donaldson SS, et al. The Childhood Cancer Survivor Study: a National Cancer Institute-supported resource for outcome and intervention research. J Clin Oncol 2009;27:2308–18. doi:10.1200/JCO.2009.22.3339.
Rodvall Y, Pershagen G, Hrubec Z, Ahlbom A, Pedersen NL, Boice JD. Prenatal X-ray exposure and childhood cancer in Swedish twins. Int J Cancer 1990;46:362–5.
Ron E, Modan B, Floro S, Harkedar I, Gurewitz R. Mental function following scalp irradiation during childhood. Am J Epidemiol 1982;116:149–60.
Ronckers CM, Land CE, Miller JS, Stovall M, Lonstein JE, Doody MM. Cancer mortality among women frequently exposed to radiographic examinations for spinal disorders. Radiat Res 2010;174:83–90. doi:10.1667/RR2022.1.
Röntgen WC. ON A NEW KIND OF RAYS. Science 1896;3:227–31. doi:10.1126/science.3.59.227.
Rowland RE, Stehney AF, Lucas HF. Dose-response relationships for female radium dial workers. Radiat Res 1978;76:368–83.
Sadetzki S, Chetrit A, Freedman L, Stovall M, Modan B, Novikov I. Long-term follow-up for brain tumor development after childhood exposure to ionizing radiation for tinea capitis (vol 163, pg 424, 2005). Radiation Research 2005;164:234–234.
Sadetzki S, Chetrit A, Lubina A, Stovall M, Novikov I. Risk of thyroid cancer after childhood exposure to ionizing radiation for tinea capitis. J Clin Endocrinol Metab 2006;91:4798–804. doi:10.1210/jc.2006-0743.
Sadetzki S, Chetrit A, Mandelzweig L, Nahon D, Freedman L, Susser E, et al. Childhood exposure to ionizing radiation to the head and risk of schizophrenia. Radiat Res 2011;176:670–7.
Salomaa S, Prise KM, Atkinson MJ, Wojcik A, Auvinen A, Grosche B, et al. State of the art in research into the risk of low dose radiation exposure—findings of the fourth MELODI workshop. J Radiol Prot 2013;33:589–603. doi:10.1088/0952-4746/33/3/589.
Salonen E, Nyman H, Kizling I, Geijerstam J-LA, Flodmark O, Aspelin P, et al. Cognitive function following head CT in childhood: a randomized controlled follow-up trial. Acta Radiol 2018;59:221–8. doi:10.1177/0284185117708471.
Savitz DA, Wellenius GA, Trikalinos TA. The Problem with Mechanistic Risk of Bias Assessments in Evidence Synthesis of Observational Studies and a Practical Alternative: Assess the Impact of Specific Sources of Potential Bias. Am J Epidemiol 2019. doi:10.1093/aje/kwz131.
Shore RE, Moseson M, Harley N, Pasternack BS. Tumors and other diseases following childhood x-ray treatment for ringworm of the scalp (Tinea capitis). Health Phys 2003;85:404–8.
Smith-Bindman R, Wang Y, Chu P, Chung R, Einstein AJ, Balcombe J, et al. International variation in radiation dose for computed tomography examinations: prospective cohort study. BMJ 2019;364:k4931. doi:10.1136/bmj.k4931.
Stewart A, Webb J, Hewitt D. A survey of childhood malignancies. Br Med J 1958;1:1495–508. doi:10.1136/bmj.1.5086.1495.
Suades-González E, Gascon M, Guxens M, Sunyer J. Air Pollution and Neuropsychological Development: A Review of the Latest Evidence. Endocrinology 2015;156:3473–82. doi:10.1210/en.2015-1403.
Sunyer J, Esnaola M, Alvarez-Pedrerol M, Forns J, Rivas I, López-Vicente M, et al. Association between traffic-related air pollution in schools and cognitive development in primary school children: a prospective cohort study. PLoS Med 2015;12:e1001792. doi:10.1371/journal.pmed.1001792.
Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H, Siebert R, et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood 2016;127:2375–90. doi:10.1182/blood-2016-01-643569.
Tettamanti G, Shu X, Adel Fahmideh M, Schüz J, Röösli M, Tynes T, et al. Prenatal and Postnatal Medical Conditions and the Risk of Brain Tumors in Children and Adolescents: An International Multicenter Case-Control Study. Cancer Epidemiol Biomarkers Prev 2017;26:110–5. doi:10.1158/1055-9965.EPI-16-0451.
The Cochrane Collaboration. Cochrane Handbook for Systematic Reviews of Interventions. Version 5.1.0 [updated March 2011]. 2011.
Thierry-Chef I, Simon SL, Weinstock RM, Kwon D, Linet MS. Reconstruction of absorbed doses to fibroglandular tissue of the breast of women undergoing mammography (1960 to the present). Radiat Res 2012;177:92–108.
Tikellis G, Dwyer T, Paltiel O, Phillips GS, Lemeshow S, Golding J, et al. The International Childhood Cancer Cohort Consortium (I4C): A research platform of prospective cohorts for studying the aetiology of childhood cancers. Paediatr Perinat Epidemiol 2018;32:568–83. doi:10.1111/ppe.12519.
Trama A, Botta L, Foschi R, Ferrari A, Stiller C, Desandes E, et al. Survival of European adolescents and young adults diagnosed with cancer in 2000-07: population-based data from EUROCARE-5. Lancet Oncol 2016;17:896–906. doi:10.1016/S1470-2045(16)00162-5.
Tran V, Zablotska LB, Brenner AV, Little MP. Radiation-associated circulatory disease mortality in a pooled analysis of 77,275 patients from the Massachusetts and Canadian tuberculosis fluoroscopy cohorts. Sci Rep 2017;7:44147. doi:10.1038/srep44147.
UNSCEAR. UNSCEAR 2017 Report, Sources, effects and risks of ionizing radiation. Annex B: Epidemiological studies of cancer risk due to low-dose-rate radiation from environmental sources. Childhood leukaemia studies. New York: United Nations; 2018.
UNSCEAR. UNSCEAR 2013 report - Vol. II, ANNEX B 2013. http://www.unscear.org/unscear/en/publications/2013_1.html (accessed July 31, 2015).
UNSCEAR. UNSCEAR 2008 report - Vol. I 2008a. http://www.unscear.org/unscear/en/publications/2008_1.html (accessed March 23, 2016).
UNSCEAR. UNSCEAR 2008 Report-Vol I, Annex A 2008b. http://www.unscear.org/docs/reports/2008/09-86753_Report_2008_Annex_A.pdf (accessed August 12, 2015).
UNSCEAR. UNSCEAR 2006 Report, Scientific Report: Effects of Ionising Radiation, Vol. 1: Scientific Annex A - Epidemiological studies of radiation and cancer. United Nations, Vienna; 2006.
US EPA O. EPA Administrator Pruitt Proposes Rule To Strengthen Science Used In EPA Regulations. US EPA 2018. https://www.epa.gov/newsreleases/epa-administrator-pruitt-proposes-rule-strengthen-science-used-epa-regulations (accessed July 23, 2019).
Van den Bergh BRH, van den Heuvel MI, Lahti M, Braeken M, de Rooij SR, Entringer S, et al. Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neuroscience & Biobehavioral Reviews 2017. doi:10.1016/j.neubiorev.2017.07.003.
Vered Y, Chetrit A, Sgan-Cohen HD, Amitai T, Mann J, Even-Nir H, et al. Caries Experience among Adults Exposed to Low to Moderate Doses of Ionizing Radiation in Childhood - The Tinea Capitis Cohort. Front Public Health 2016;4:18. doi:10.3389/fpubh.2016.00018.
Verreet T, Quintens R, Van Dam D, Verslegers M, Tanori M, Casciati A, et al. A multidisciplinary approach unravels early and persistent effects of X-ray exposure at the onset of prenatal neurogenesis. J Neurodev Disord 2015;7:3. doi:10.1186/1866-1955-7-3.
Villoing D, Drozdovitch V, Simon SL, Kitahara CM, Linet MS, Melo DR. Estimated Organ Doses to Patients from Diagnostic Nuclear Medicine Examinations over Five Decades: 1960-2010. Health Phys 2017;113:474–518. doi:10.1097/HP.0000000000000721.
Vostrotin VV, Napier BA, Zhdanov AV, Miller SC, Sokolova AB, Bull RK, et al. THE MAYAK WORKER DOSIMETRY SYSTEM (MWDS-2016): INTERNAL DOSIMETRY RESULTS AND COMPARISON WITH MWDS-2013. Radiat Prot Dosimetry 2019;184:201–10. doi:10.1093/rpd/ncy200.
Vũ Bezin J, Allodji RS, Mège J-P, Beldjoudi G, Saunier F, Chavaudra J, et al. A review of uncertainties in radiotherapy dose reconstruction and their impacts on dose-response relationships. J Radiol Prot 2017;37:R1–18. doi:10.1088/1361-6498/aa575d.
Weiss HA, Darby SC, Doll R. Cancer mortality following X-ray treatment for ankylosing spondylitis. Int J Cancer 1994;59:327–38.
Weiss HA, Darby SC, Fearn T, Doll R. Leukemia mortality after X-ray treatment for ankylosing spondylitis. Radiat Res 1995;142:1–11.
Whaley P, Letcher RJ, Covaci A, Alcock R. Raising the standard of systematic reviews published in Environment International. Environ Int 2016;97:274–6. doi:10.1016/j.envint.2016.08.007.
WHO WHO. Communicating radiation risks in paediatric imaging. Geneva, Switzerland: 2016.
Winther JF, Kenborg L, Byrne J, Hjorth L, Kaatsch P, Kremer LCM, et al. Childhood cancer survivor cohorts in Europe. Acta Oncol 2015;54:655–68. doi:10.3109/0284186X.2015.1008648.
Wrensch M, Miike R, Lee M, Neuhaus J. Are prior head injuries or diagnostic X-rays associated with glioma in adults? The effects of control selection bias. Neuroepidemiology 2000;19:234–44. doi:26261.
Xu XG, Bednarz B, Paganetti H. A review of dosimetry studies on external-beam radiation treatment with respect to second cancer induction. Phys Med Biol 2008;53:R193-241. doi:10.1088/0031-9155/53/13/R01.
Zablotska LB, Little MP, Cornett RJ. Potential increased risk of ischemic heart disease mortality with significant dose fractionation in the Canadian Fluoroscopy Cohort Study. Am J Epidemiol 2014;179:120–31. doi:10.1093/aje/kwt244.
Zeltzer LK, Lu Q, Leisenring W, Tsao JCI, Recklitis C, Armstrong G, et al. Psychosocial outcomes and health-related quality of life in adult childhood cancer survivors: a report from the childhood cancer survivor study. Cancer Epidemiol Biomarkers Prev 2008;17:435–46. doi:10.1158/1055-9965.EPI-07-2541.
