Research Article: Risk of malignant skin neoplasms in a cohort of workers occupationally exposed to ionizing radiation at low dose rates

Date Published: October 5, 2018

Publisher: Public Library of Science

Author(s): Tamara V. Azizova, Maria V. Bannikova, Evgeniya S. Grigoryeva, Valentina L. Rybkina, Suminori Akiba.

http://doi.org/10.1371/journal.pone.0205060

Abstract

Recently an increasing trend in skin cancer rates has been observed in various populations including those exposed to different radiation types. Risk and dose-response following prolonged radiation exposure remain unclear. The present study was aimed to assess skin melanoma (SM) and non-melanoma skin cancer (NMSC) incidence risks in a cohort of workers occupationally exposed to ionizing radiation at low dose rates over prolonged periods. The study cohort included workers of a Russian nuclear production facility, Mayak Production Association (PA), who were first employed in 1948–1982 and followed up till the end of 2013 (the total of 22,377 individuals with 25% of females). Using AMFIT module of EPICURE software, relative risk and excess relative risk per unit dose (RR and ERR/Sv) were calculated. 60 SM and 294 NMSC cases were registered in members of the study cohort. SM and NMSC incidence was dependent on sex, attained age, age at first employment at the enterprise, type of facility, education level and was not dependent on calendar period of first employment, calendar period of diagnosis, duration of employment, smoking and alcohol consumption statuses. The risk of NMSC incidence was found to be significantly increased in workers occupationally exposed to ionizing radiation at cumulative doses above 2.0 Sv (RR = 2.52; 95% CI: 1.60, 3.97) compared to a reference dose category (0–0.05 Sv). NMSC incidence was found to be significantly associated with cumulative external gamma-dose with ERR/Sv of 0.49 (95% CI: 0.22, 0.90) without an adjustment for neutron dose and 0.51 (95% CI: 0.22, 0.93) while adjusted for neutron dose. Results of the analysis did not reveal a significant association of SM incidence with cumulative dose from external gamma-rays with ERR/Sv of 0.22 (95% CI: -0.29, 1.46) not including a neutron dose adjustment and of 0.15 (95% CI: -0.41, 1.31) while adjusted for dose from neutron exposure.

Partial Text

Malignant skin neoplasms (MSN) including skin melanomas (SM) and non-melanoma skin cancers (NMSC) are the most common malignancies tending to increase during the recent decades consistently [1–3], The main factors contributing to MSN are sex, age, genetic susceptibility, skin phenotype, UV-exposure, etc [3–7]. MSN risks were reported for various cohorts of individuals exposed to different types of radiation [3,7–13]. A review by the UK Independent Advisory Group on Ionising Radiation3 gives a detailed systematic and critical review of skin cancer studies considering a range of exposure scenarios. The authors conclude that dose-effect studies are limited due to the lack of dosimetry data. Risk estimates and dose-response model type remain unclear for prolonged exposure at low dose rates. Thus, this study as aimed to assess SM and NMSC incidence risks in a cohort of Mayak Production Association (PA) workers occupationally exposed to radiation over prolonged periods at low dose rates. Earlier, studies of this cohort demonstrated increased radiogenic incidence and mortality risks for leukemia and solid cancers, lung, liver and bone cancers [14–20].

The present record-based epidemiological study did not require any contact with cohort members. The study was reviewed and approved by Institutional Review Board (IRB) of the Southern Urals Biophysics Institute. SUBI IRB confirmed that no signed consents were needed from members of the study cohort. The study was performed in accordance with the Declaration of Helsinki.

Over the follow-up period in the study Mayak worker cohort 60 cases of SM and 294 cases of NMSC were registered within 571 462 and 565 019 person-years of follow-up, respectively. The vast majority of SM and NMSC cases were registered in workers at the age above 50 (85.0% and 86.4%, respectively). Age is known to be one of the main risk factors for malignant neoplasm development [3–5]. SM and NMSC cases were mostly registered during 1986–2013 period (86.7% and 80.3%, respectively), mainly, due to attained age of workers of the study cohort in this period. Standardized SM incidence rates were 8.51 ± 1.46 in males and 8.78 ± 2.27 in females per 100,000 workers while the corresponding rates for NMSC were 46.04 ± 3.40 and 37.40 ± 4.72, respectively (unpublished data in print). Standardized incidence rates for SM and NMSC in the study cohort markedly increased by the end of the follow-up (Fig 4). Significant log-linear trends were revealed for NMSC incidence rate increase by the end of the follow-up period both for males and females of the study cohort (APC = 2.69 and 3.82, respectively, P < 0.10) as well as the insignificant trend of SM incidence rate increase for male workers (APC = 2.37, P = 0.2) (Fig 4). The obtained results agree well with findings of other studies and support the common pattern of the increase of MSN incidence rate [1–3]. This upward trend for MSN incidence rate in Russia is driven by the increased expectation of life as well as by improvements in procedures needed to register the disease diagnosis. Results of the current study provide evidence to association of MSN incidence in the cohort of Mayak PA workers with sex, attained age, age at first employment at the facility, facility type and education as well as to the fact that MSN incidence was not dependent on calendar period of employment, calendar period of diagnosis, duration of employment, alcohol consumption and smoking. The increase of MSN incidence rates with increasing attained age could be expected and is driven by the age causation of the disease. Information on role of other non-radiation factors (for example, smoking, alcohol consumption) for MSN development reported in different studies is inconsistent [26–28]. Meanwhile results of epidemiological and clinical studies prove that UVI is the main ambient factor, which increases MSN risk [3, 6, 7]. Within the present retrospective study, we could not investigate sufficiently such factor as UVI. However, the risk analysis conducted for various MSN sites based on the study cohort data showed that incidence rates for SM and NMSC localized in face and neck regions were significantly decreased compared to body localizations while other studies demonstrated that if the UVI index was high, then risk of facial and neck MSN increased significantly [29]. It should be noted that all workers of the study cohort were living in the city of Ozyorsk in the Southern Urals in the same climate with the low index of UVI over the whole follow-up period. Also, it is worth noting that all workers of the study cohort were working only indoors. The study results demonstrated that SM and NMSC incidence was dependent on sex, attained age, age at first employment at the enterprise, type of facility, education level and was not dependent on calendar period of first employment, calendar period of diagnosis, duration of employment, smoking and alcohol consumption statuses. The risk of NMSC incidence was found to be significantly increased in workers occupationally exposed to ionizing radiation at cumulative doses above 2.0 Sv (RR = 2.52; 95% CI: 1.60, 3.97) compared to a reference dose category (0–0.05 Sv). NMSC incidence was found to be significantly associated with cumulative external gamma-dose with ERR/Sv of 0.49 (95% CI: 0.22, 0.90) without an adjustment for neutron dose and 0.51 (95% CI: 0.22, 0.93) while adjusted for neutron dose. Results of the analysis did not reveal a significant association of SM incidence with cumulative dose from external gamma-rays with ERR/Sv of 0.22 (95% CI: -0.29, 1.46) not including a neutron dose adjustment and of 0.15 (95% CI: -0.41, 1.31) while adjusted for dose from neutron exposure.   Source: http://doi.org/10.1371/journal.pone.0205060

 

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