Medical Radiology and Radiation Safety. 2024. Vol. 69. № 1


G.V. Zhuntova, T.V. Azizova, M.V. Bannikova

Multiple Primary Malignant Tumors in Workers Chronically Exposed to Ionizing Radiation

Southern Urals Biophysics Institute, Ozyorsk, Russia

Contact person: G.V. Zhuntova, e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.



Purpose: To characterize multiple primary malignant tumors (MPMTs) in workers occupationally chronically exposed to ionizing radiation. 

Material and methods: The study included 22,377 workers employed at reactors, plutonium-production plant and radiochemical plant of the Mayak Production Association (PA) who had been hired in 1948–1982. The study considered cases of MPMTs (verified with the morphological examination) that had been diagnosed in workers before 31 December 2018. The paper describes the structure and provides the comparative characteristics of synchronous and metachronous MPMTs.

Results: 320 cases of MPMTs that were verified with the morphological examination were registered in the cohort: 68.4 % in males and 31.6 % in females. 3 and more malignant tumors were registered in 20 % of workers with MPMTs. MPMTs accounted for 10.5 % of total malignant tumors registered in the cohort. Synchronous MPMTs accounted for 22.8 % in males and for 18.8 % in females. 36.6 % of metachronous MPMTs were diagnosed with an interval of more than 10 years. The structure of MPMTs was dominated by tumors of digestive organs, skin, genital organs (both sexes), respiratory organs (for males), and breast (for females). As for a histological type of tumor, adenocarcinomas and basal-cell carcinomas (both sexes), squamous-cell carcinomas (for males), ductal and lobular tumors (for females) were the most frequent.

Groups of workers with synchronous and metachronous MPMTs demonstrated some significant differences: synchronous MPMTs were diagnosed in later age than the primary metachronous tumor; the numbers of smokers and heavy alcohol drinkers were bigger in the group of workers with synchronous MPMTs, as well as the smoking index. Neither radiation doses nor the duration of occupational exposure at a date of diagnosis of synchronous MPMTs and a primary metachronous tumor were significantly different. Compared to the entire study cohort, the number of workers occupationally exposed at high doses was bigger in workers with MPMTs (above 1.0 Sv for external gamma-ray exposure, and above 1.0 Gy for internal alpha exposure).

Conclusion: MPMTs in workers of the nuclear enterprise were characterized in relation to non-radiation and occupation-related factors.
In the future it is planned to assess the impact of the occupational radiation exposure on the risk of MPMTs in workers of the study cohort considering non-radiation factors.

Keywords: occupational chronic exposure to ionizing radiation, Mayak PA workers, multiple primary malignant tumors, risk factors

For citation: Zhuntova GV, Azizova TV, Bannikova MV. Multiple Primary Malignant Tumors in Workers Chronically Exposed to Ionizing Radiation. Medical Radiology and Radiation Safety. 2024;69(1):67–72. (In Russian). DOI:10.33266/1024-6177-2024-69-1-67-72



1. Copur M.S., Manapuram S. Multiple Primary Tumors Over a Lifetime. Oncology (Williston Park). 2019;33;7:629384. 

2. Vogt A., Schmid S., Heinimann K., Frick H., Herrmann C., Cerny T., Omlin A. Multiple Primary Tumours: Challenges and Approaches, a Review. ESMO Open. 2017;2;2:e000172. 

3. Demoor-Goldschmidt C., de Vathaire F. Review of Risk Factors of Secondary Cancers among Cancer Survivors. Br. J. Radiol. 2019;92;1093:20180390. 

4. Li C.I., Nishi N., McDougall J.A., Semmens E.O., Sugiyama H., Soda M., Sakata R., Hayashi M., Kasagi F., Suyama A., Mabuchi K., Davis S., Kodama K., Kopecky K.J. Relationship between Radiation Exposure and Risk of Second Primary Cancers among Atomic Bomb Survivors. Cancer Res. 2010;70;18:7187-198. 

5. Nakashima M., Kondo H., Miura S., Soda M., Hayashi T., Matsuo T., Yamashita S., Sekine I. Incidence of Multiple Primary Cancers in Nagasaki Atomic Bomb Survivors: Association with Radiation Exposure. Cancer Sci. 2008;99;1:87-92. 

6. Richardson D.B., Cardis E., Daniels R.D., Gillies M., Haylock R., Leuraud K., Laurier D., Moissonnier M., Schubauer-Berigan M.K., Thierry-Chef I., Kesminiene A. Site-Specific Solid Cancer Mortality after Exposure to Ionizing Radiation: A Cohort Study of Workers (INWORKS). Epidemiology. 2018;29;1:31-40. 

7. Gillies M., Kuznetsova I., Sokolnikov M., Haylock R., O’Hagan J., Tsareva Y., Labutina E. Lung Cancer Risk from Plutonium: A Pooled Analysis of the Mayak and Sellafield Worker Cohorts. Radiat Res. 2017;188;6:645-660.

8. Sokolnikov M., Preston D., Stram D.O. Mortality from Solid Cancers other than Lung, Liver, and Bone in Relation to External Dose among Plutonium and Non-Plutonium Workers in the Mayak Worker Cohort. Radiat Environ Biophys. 2017;56;1:121-125. 

9. Azizova T.V., Day R.D., Wald N., Muirhead C.R., O’Hagan J.A., Sumina M.V., Belyaeva Z.D., Druzhinina M.B., Teplyakov I.I., Semenikhina N.G., Stetsenko L.A., Grigoryeva E.S., Krupenina L.N., Vlasenko E.V. The «Clinic» Medical-Dosimetric Database of Mayak Production Association Workers: Structure, Characteristics and Prospects Of Utilization. Health Phys. 2008;94;5:449-458. 

10. Working Group Report. International Rules for Multiple Primary Cancers (ICD-0 Third Edition). Eur. J. Cancer Prev. 2005;14;4:307-308.

11. Birchall A., Vostrotin V., Puncher M., Efimov A., Dorrian M.D., Sokolova A., Napier B., Suslova K., Miller S., Zhdanov A., Strom D.J., Scherpelz R., Schadilov A.  The Mayak Worker Dosimetry System (MWDS-2013) for Internally Deposited Plutonium: an Overview. Radiat. Prot. Dosimetry. 2017;176;1-2:10-31. 

12. Zar J.H. Biostatistical Analysis. New Jersey, Prentice Hall, 1999. 663 p.

13. Каприн А.Д., Старинский В.В., Петрова Г.В. Злокачественные новообразования в России в 2018 году (заболеваемость и смертность). М., 2019. 250 с. [Kaprin A.D., Starinskiy V.V., Petrova G.V. Zlokachestvennyye Novoobrazovaniya v Rossii v 2018 Godu (Zabolevaemost’ I Smertnost’) = Malignant Neoplasms in Russia in 2018 (Morbidity and Mortality). Moscow Publ., 2019. 250 p. (In Russ.)].

14. Feller A., Matthes K.L., Bordoni A., Bouchardy C., Bulliard J.L., Herrmann C., Konzelmann I., Maspoli M., Mousavi M., Rohrmann S., Staehelin K., Arndt V.; NICER Working Group. The Relative Risk of Second Primary Cancers in Switzerland: a Population-Based Retrospective Cohort Study. BMC Cancer. 2020;21;20;1:51. doi: 10.1186/s12885-019-6452-0. 

15. Hawkins M., Bhatia S., Henderson T.O., Nathan P.C., Yan A., Teepen J.C., Morton L.M. Subsequent Primary Neoplasms: Risks, Risk Factors, Surveillance, and Future Research. Pediatr. Clin. North. Am. 2020;67;6:1135-1154. doi: 10.1016/j.pcl.2020.07.006.

16. Demoor-Goldschmidt C., Supiot S., Mahé M.A., Oberlin O., Allodji R., Haddy N., Helfre S., Vigneron C., Brillaud-Meflah V., Bernier V., Laprie A., Ducassou A., Claude L., Diallo I., de Vathaire F. Clinical and Histological Features of Second Breast Cancers Following Radiotherapy for Childhood and Young Adult Malignancy. B. J. Radiol. 2018;91;1086:20170824. doi: 10.1259/bjr.20170824.

17. Adjei Boakye E., Wang M., Sharma A., Jenkins W.D. Risk of Second Primary Cancers in Individuals Diagnosed with Index Smoking- And Non-Smoking- Related Cancers. J. Cancer Res. Clin. Oncol. 2020;146;7:1765-1779. doi: 10.1007/s00432-020-03232-8. 

18. Druesne-Pecollo N., Keita Y., Touvier M., et al. Alcohol Drinking and Second Primary Cancer Risk in Patients with Upper Aerodigestive Tract Cancers: a Systematic Review and Meta-Analysis of Observational Studies. Cancer Epidemiol Biomarkers Prev. 2014;23;2:324–331. 

19. Jégu J., Colonna M., Daubisse-Marliac L., Trétarre B., Ganry O., Guizard A.V., Bara S., Troussard X., Bouvier V., Woronoff A.S., Velten M. The Effect of Patient Characteristics on Second Primary Cancer Risk in France. BMC Cancer. 2014;14:94. doi: 10.1186/1471-2407-14-94. 

20. Осипов М.В., Сокольников М.Э. Предшествующее злокачественное новообразование как фактор риска второго рака в когорте работников предприятия ядерно-промышленного комплекса // Российский онкологический журнал. 2016. Т.21, № 4. С. 190-94. DOI: 10.18821/1028-9984-2016-21-4-190-194. [Osipov M.V., Sokolnikov M.E. Prior Malignant Neoplasms as a Risk Factor for the Second Cancer in a Cohort of Employees of Enterprises of the Nuclear Industrial Complex. Rossiyskiy Onkologicheskiy Zhurnal = Russian Journal of Oncology. 2016;21;4:190–194. DOI: 10.18821/1028-9984-2016-21-4-190-194. (In Russ.)].



 PDF (RUS) Full-text article (in Russian)


Conflict of interest. The authors declare no conflict of interest.

Financing. This study was carried out with the support of the Federal Medical and Biological Agency of Russia under state contract No. 27.501.21.2 dated June 11, 2021. «Modernization of high-tech methods aimed at identifying the medical effects of radiation exposure on the personnel of the Mayak software and the population of the Ural region.»

Contribution. Article was prepared with equal participation of the authors.

Article received: 20.10.2023. Accepted for publication: 27.11.2023.