Skip to main content

Advertisement

We’d like to understand how you use our websites in order to improve them. Register your interest.
Download PDF

Radiation-related occupational cancer and its recognition criteria in South Korea

Annals of Occupational and Environmental Medicine volume 30, Article number: 9 (2018) Cite this article

Abstract

Ionizing radiation is a well-known carcinogen, and is listed as one carcinogenic agent of occupational cancer. Given the increase in the number of workers exposed to radiation, as well as the increase in concern regarding occupational cancer, the number of radiation-related occupational cancer claims is expected to increase. Unlike exposure assessment of other carcinogenic agents in the workplace, such as asbestos and benzene, radiation exposure is usually assessed on an individual basis with personal dosimeters, which makes it feasible to assess whether a worker’s cancer occurrence is associated with their individual exposure. However, given the absence of a threshold dose for cancer initiation, it remains difficult to identify radiation exposure as the root cause of occupational cancer. Moreover, the association between cancer and radiation exposure in the workplace has not been clearly established due to a lack of scientific evidence. Therefore, criteria for the recognition of radiation-related occupational cancer should be carefully reviewed and updated with new scientific evidence and social consensus. The current criteria in Korea are valid in terms of eligible radiogenic cancer sites, adequate latent period, assessment of radiation exposure, and probability of causation. However, reducing uncertainty with respect to the determination of causation between exposure and cancer and developing more specific criteria that considers mixed exposure to radiation and other carcinogenic agents remains an important open question.

Background

Ionizing radiation is classified as a Group 1 carcinogen in humans by the International Agency for Research on Cancer (IARC), and is listed as one carcinogenic agent of occupational cancer by the International Labor Organization (ILO) and the Enforcement Decree of the Labor Standards Act in Korea [1,2,3]. Ionizing radiation is called “radiation” henceforth in this paper. Radiation is utilized for various purposes, and both the number of radiation-related facilities and the number of radiation workers have also increased by about 10 and 4% per year, respectively [4]. Radiation exposure has been well managed under 5% of the occupational dose limit which is a 100 mSv in 5 years with a maximum of 50 mSv in any single year, in most radiation workers in Korea. However, some occupations, such as workers who perform non-destructive testing (NDT) and radiologists, are exposed to relatively higher radiation levels than other radiation-related occupations [5]. Moreover, due to an increase in social concerns about occupational cancer, the number of occupational cancer claims related to radiation exposure is increasing, especially among semiconductor manufacturing and NDT workers. In general, criteria for the recognition of radiation-related occupational cancer are based on the type of cancer, exposure assessment, probability of causation, and general principles of compensation for occupational diseases. These criteria should be updated with new scientific evidence and social consensus. The aim of this study, therefore, was to review the recognition criteria for radiation-related occupational cancer and identify the characteristics of radiation exposure and diagnosed cases in the workplace in Korea. This review provides a comprehensive reference for understanding criteria for the recognition of radiation-related occupational cancer, which can help to guide reasonable and scientific decision making.

Review

Occupational exposure in Korea

Exposure assessment is essential for identifying whether cancer incidence among workers is caused by harmful agents in the workplace. In Korea, depending on the occupation type, radiation exposure in individual workers has been monitored and managed by two government institutes, the Nuclear Safety and Security Commission (NSSC) and the Centers for Disease Control and Prevention (CDC), with their own National Dose Registries (NDR). To determine whether cancer occurrence in the workplace is associated with radiation exposure, these NDRs are investigated first for radiation exposure assessment. Radiation workers in the NDR who are managed by the NSSC are grouped into nine categories: public institution, educational institution, non-destructive industry, industrial organization, research institute, nuclear power plant, medical institution (except for workers using diagnostic x-ray generators), military, and production and sales [6]. Since the NDR was started in 1984, the average exposure dose for radiation workers has been in steady decline to nearly 1 mSv per year or less, except for NDT workers, whose exposure levels were the highest with average doses of 2.37–3.87 mSv/year in the recent five years (Table 1) [5, 6]. Exposure doses of diagnostic radiation workers, who mainly work with x-ray generators in hospitals, were managed by the CDC’s NDR and grouped into five categories: radiologic technologists, physicians, dentists, dental hygienists, and other radiation workers [7]. Exposure doses have been in steady decline over the last 10 years among diagnostic radiation workers. Exposure levels were highest among radiologic technologists, with average doses of 0.85–1.21 mSv/year in the recent 5 years (Table 1) [8].

Table 1 Number of workers and exposure dose (mSv) according to occupation type in Korea
Full size table

Radiation carcinogenesis

The initial mechanism of radiation-induced cancer is not different from the mechanisms of other harmful agents, such as toxic chemicals and ultraviolet radiation, in terms of DNA damage. It is well-known that many innate defense mechanisms against radiation damage occur in various ways (e.g., removal of oxidative stress and damaged cells, DNA repair) in the human body, and damaged cells or DNA that remain may cause tissue or organ dysfunction and malignant disease such as cancer and heritable disease. In general, health risks from radiation exposure are classified into two groups: tissue reactions, which are conventionally referred to as deterministic effects, and stochastic effects. Tissue reaction effects include organ malfunction such as skin burns, bone marrow failure, and intestinal damage, which occur above a threshold dose below which there is no increased risk and are considered non-cancer damaging effects. In contrast, stochastic effects are assumed to have no threshold dose and occur by chance, with the probability of the effect increasing as exposure dose increases. The main risks associated with stochastic effects are cancer and genetic defects, and generally occur 1–2 years after exposure for leukemia and 5–10 years after exposure for solid cancer. Thus, radiation-related occupational cancer can be considered a stochastic effect of radiation exposure.

The IARC and the U.S. National Toxicology Program (NTP) classify radiation (commonly referred to as ionizing radiation), including x-rays and gamma rays, as “Group 1” and “Known” carcinogens, respectively, according to their own classification criteria [9]. The European Agency for Safety and Health at Work similarly interprets radiation carcinogenesis according to the classification of carcinogens, mutagens, and reprotoxicants (CMR) substances, based largely on human evidence [10]. Regarding the evaluation of a causal association between radiation exposure (i.e., x-ray and gamma rays) for individual cancer (organ) sites, the IARC has categorized cancer sites into “strong evidence” and “potentially having limited or inadequate evidence” based on up-to-date scientific evidence [9]. Cancer sites with “strong evidence” are listed in Table 2, and these evaluations were carried out based on biological data and epidemiological evidence.

Table 2 Cancer sites/ tumors with sufficient evidence for causal associations with x-ray and gamma-ray exposure
Full size table

Review of epidemiological studies of cancer risk

Atomic bomb survivors and the Chernobyl accident

One major source of epidemiological data to evaluate health risks from radiation exposure is the Life Span Study (LSS) of atomic bomb survivors, which found a proportional relationship between cancer risk and exposure dose. Although numerous findings from the study provide scientific evidence for increased cancer risk from radiation exposure, radiation-associated cancer risk remains unclear at low-dose ranges under 100 mSv [11]. Studies related to the Chernobyl accident also demonstrated cancer risks from radiation exposure, especially an increase in thyroid cancer among children with high thyroid-absorbed doses. Except for this result, however, no definitive conclusions have been made regarding other cancers among Chernobyl residents who were exposed to low doses of radiation [12,13,14,15]. Some studies that have investigated the health of Chernobyl workers exposed to prolonged low to medium doses of radiation (average effective dose of 100 mSv) have reported increased risks of cancer as well as non-cancer diseases, such as cataracts and cardiovascular diseases [16,17,18,19,20,21]. However, due to screening effects (e.g., medical examinations) and limited sample sizes, it is difficult to draw definitive conclusions from these studies. Thus, it remains necessary to continue follow-ups of these cohorts with accurate assessments of exposure dose, health outcomes, and confounding factors [14, 22].

Occupational exposure in radiation workers

A major distinction between occupational exposure and accidental exposure is the period and dose levels of exposure. Whereas accidental exposure usually involves a single large exposure (acute), occupational exposure involves protracted exposures to low-dose radiation (chronic). A number of epidemiological investigations have been conducted among radiation workers in individual countries as well as in large-scale international cohort studies, and the cancer risk from occupational exposure to radiation continues to be updated. A few studies have reported elevated risks of cancer with statistical significance. One of the largest occupational studies in radiation workers is the 15-country collaborative study, which included 407,391 nuclear industry workers over 5.2 million person-years of follow-up [23]. In this study, an elevated risk of all-cancer mortality was observed, with an excess relative risk (ERR/Sv) of 0.97 (95% CI: 0.27, 1.8). However, this risk diminished after excluding data from workers in Canada, in whom the dose measurement was uncertain, and the observed risk was no longer significant. As a follow-up to the 15-country collaborative study, risks of leukemia and lymphoma were investigated among 308,297 radiation workers in France, the U.K., and the U.S. [24]. The association between exposure dose and cancer mortality was statistically significant with an ERR of 2.96 per Gy (90% CI: 1.17, 5.21) for leukemia, excluding chronic lymphocytic leukemia (CLL). The highest ERR/Gy of 10.45 (90% CI: 4.48, 19.65) was found for chronic myeloid leukemia, indicating a strong association between leukemia mortality and protracted low-dose radiation exposure [24]. Although the ERR of leukemia, excluding CLL, was not attenuated for doses less than 100 mGy, the 90% CIs were too wide to make a definitive conclusion about the low-dose ranges.

Cohort studies of the Mayak nuclear complex workers also reveal an elevated cancer risk [25,26,27]. Because this cohort had a broad range of cumulative doses due to high exposure levels during the early stages of the facility operation, the dose-response relationship had a degree of precision that is rarely observed in other studies of radiation workers, who are usually exposed to low-dose levels [26]. In addition to the Mayak cohort studies, other studies of radiation workers have reported increased risks of certain types of cancer, such as leukemia (excluding CLL), esophageal cancer, and lung cancer [28,29,30,31]. However, risks for individual cancer sites are inconsistent across most radiation epidemiological studies, and many studies do not find statistically significant results. Cancer risks from major health studies in nuclear workers are summarized in Tables 3 and 4.

Table 3 Risks of solid cancers in epidemiological studies of nuclear workers
Full size table
Table 4 Risks of leukemia (excluding CLL) in epidemiological studies of nuclear workers
Full size table

Aircrews, such as pilots and flight attendants, are exposed to cosmic radiation. Although aircrews are not included in the national registry for radiation workers in Korea, they should be considered radiation workers and monitored for radiation exposure and health risks, because they are exposed to similar or even higher levels of radiation compared to common radiation-related occupations, such as nuclear workers and radiologists. An average effective dose in an aircrew flying over the poles at high latitudes is estimated to be 2–5 mSv/year, which may reach a cumulative dose of about 75 mSv over the course of a worker’s career [32]. Many interesting health studies have been conducted in aircrews based in Nordic countries, the U.S., and Canada. These studies have reported higher risks of breast cancer, prostate cancer, brain cancer, skin cancer, non-Hodgkin’s lymphoma, and acute myeloid leukemia among aircrews, compared with the general population [33,34,35,36,37]. However, given that no demonstrated dose-response relationship was found, these elevated cancer risks do not imply a causal relationship with radiation exposure.

In summary, despite the existence of several epidemiological studies in radiation workers, cancer risks from occupational exposure, especially for doses less than 100 mSv, remain poorly understood due to uncertainty about exposure dose and confounding factors, possible misclassification of health outcomes, and limited statistical power [24, 38].

Diagnosed cases of radiation-related occupational cancer in Korea

Recognition of work-related disease is made through the Occupational Disease Approval Committee of the Korea Workers’ Compensation and Welfare Service (COMWEL). According to Article 38 of the Industrial Accident Compensation Insurance Act (IACIA) and Article 7 of the enforcement regulations of the IACIA, the following are diseases that do not require deliberation from COMWEL: (1) pneumoconiosis, (2) carbon disulfide poisoning, (3) diseases with serious acute syndromes from acute exposures to high levels of hazardous agents and relevant risk, and (4) obvious occupation-related disease. In general, criteria for the diagnosis of radiation-related cancers include the cancer site, exposure dose, latent period of cancer, and probability of causation. More strict diagnostic criteria have been applied to thyroid cancer because it is the most common type of cancer found by chance. Table 5 summarizes the characteristics of diagnosed cases of radiation-related occupational cancer in Korea from the occupational disease annual reports (2000–2015) of the Korea Occupational Safety and Health Agency (KOSHA). This list excludes acute diseases due to acute exposure to high levels of hazardous agents and relevant risk according to Article 25 of the enforcement regulations of the IACI Act. Of 43 deliberated cases that may possibly be related to occupational exposure, approximately 70% included male workers, six cases were classified as having a “strong relationship” with occupational exposure, and two cases remained classified as “issues”. All eight cases involved male workers, the youngest of whom was 37 years old. Most of these eight cases had leukemia, including acute myeloid leukemia (AML), acute lymphocytic leukemia (ALL), and chronic myeloid leukemia (CML). Cancers other than leukemia included anaplastic large cell lymphoma, brain cancer, and carcinoma with an unknown primary site.

Table 5 Diagnosed cases of radiation-related occupational cancer in Korea (2000~ 2015)
Full size table

Considerations in the recognition criteria for occupational cancer

Recognition criteria in Korea

Several criteria should be met cumulatively to obtain the recognition of radiation-related occupational cancer. These criteria are well described in Notification No. 2014-78 of the NSSC regarding regulations on occupational disease among radiation workers. The major criteria are summarized here. First, cancer must be eligible for radiation-induced cancer: liver cancer, except those cancers that involve cirrhosis or the hepatitis virus (e.g., types B or C); thyroid cancer; ovarian cancer; brain cancer; multiple myeloma; colon cancer; bladder cancer; Non-Hodgkin lymphoma; esophagus cancer; kidney cancer; female breast cancer; stomach cancer; pancreatic cancer; salivary gland cancer; lung cancer; skin cancer; and leukemia, excluding CLL. Several cancers are not recognized as radiation-related occupational cancer, namely Hodgkin’s lymphoma, melanoma, malignant mesothelioma, and CLL. These classifications are based mainly on findings from epidemiological studies. For example, mesothelioma is a well-known asbestos-related cancer, and approximately 80–90% of mesotheliomas are caused by long-term inhalation of asbestos [39]. As another example, whereas leukemia is a radiation-sensitive cancer, CLL has not been associated with radiation exposure in most epidemiological studies (Table 6). Second, radiation exposure must be identified by dose assessment or circumstantial evidence. For the assessment of exposure levels, dose records from the NDR are considered a priority. Additional assessments, such as dose reconstruction, are necessary for unclear or omitted cases. Third, a latent period (i.e., time between the first exposure and the appearance of a tumor) must be considered as sufficient or relevant to cancer incidence. For example, solid cancer can be recognized as occupational cancer only if the cancer occurs at least 5 years after the first exposure, whereas leukemia (excluding CLL) can be recognized as occupational cancer only if the cancer occurs at least 2 years after the first exposure and within 20 years after the last exposure. Lastly, the probability of causation (PC), which is defined as the probability that a cancer was caused by occupational radiation exposure during employment, determines whether an individual’s cancer is “at least as likely as not” (i.e., a PC of 50% or greater) related to occupational exposure [40]. The PC is calculated as cancer risk attributable to radiation exposure divided by the sum of baseline cancer risk to the general population plus the risk attributable to radiation exposure, considering personal information (e.g., birth year, gender), medical information (e.g., type of cancer, year of diagnosis), and exposure information (e.g., age at exposure, radiation dose). Given that a threshold dose for cancer has not been identified yet, risks of cancer are stochastic effects, and therefore the PC is an important objective measure to assess a causal relationship with radiation exposure. Based on the current guidelines from the NSSC, PCs for solid cancer and leukemia should exceed 50% and 33%, respectively. However, PC includes an estimation error due to uncertainties about dose and the dose rate effectiveness factor (DDREF), as well as a risk transfer error between different populations; therefore, there exist cases with a PC less than 50% that are fully or partially recognized as occupational cancer in civil litigation.

Table 6 Risk of chronic lymphocytic leukemia in epidemiological studies of radiation exposure
Full size table

Recognition criteria in other countries

The recognition criteria for radiation-related occupational cancer are based on scientific evidence. However, ultimately, their acceptable range and levels are often affected by several factors unrelated to science, such as social, cultural, and economic factors. In particular, complex elements, such as the social status of the radiation-related occupation, number of workers, cancer incidence rate in the general population, specific risk perceptions of certain cancers, and economic wealth, factor into the recognition of occupational cancer. For these reasons, recognition criteria differ across countries or even across occupations within the same country. For example, CLL is generally excluded as an occupational cancer due to lack of scientific evidence regarding radiation-induced CLL. However, CLL is considered as being potentially caused by radiation, and hence, as potentially compensable under the Energy Employees Occupational Illness Compensation Program Act of 2000 (EEOICPA), effective March 7, 2012 in the U.S. In addition, eligible cancer sites differ according to occupation (e.g., special exposure cohort, uranium workers, energy employees, soldiers). Regarding the PC, the EEOICPA applies the upper 99% credibility (i.e., confidence) limit of the PC instead of the point estimate (i.e., 50th percentile) to the determination of causation between exposure and cancer, which provides each worker with the benefit of the doubt before a final compensation decision is made. In France, the criteria for recognition or compensation for cases not relevant to the regulatory guidelines are more relaxed through individual case assessments, meaning that cases with non-radiogenic disease or an inadequate latent period can be possibly compensated when the disease is obviously related to occupational exposure and the disability from the disease is over 25% [41]. Major recognition criteria of Korea and other countries are compared in Table 7.

Table 7 Comparison of the recognition criteria of Korea, the U.K., the U.S., and France
Full size table

Conclusions

Based on the scientific evidence and compared with the guidelines of other countries, the current recognition criteria for radiation-related occupational cancer in Korea are valid in terms of the eligibility of cancer sites, adequacy of the latent period, assessment of radiation exposure, and probability of causation. However, the exact quantification of exposure dose is often not possible, and therefore the recognition criteria involve some degree of uncertainty. Therefore, it is proposed that exposure doses of all radiation-related workers be carefully monitored without a dead zone in exposure management, and more relaxed criteria be considered for a margin of uncertainty through the use of the upper 95% or 99% credibility limit of the PC. In addition, further recognition criteria are necessary for more complex exposures, e.g., to two or more carcinogenic agents, including radiation.

Abbreviations

ALL:

Acute lymphocytic leukemia

AML:

Acute myeloid leukemia

CAREX:

Carcinogen exposure database

CDC:

Centers for Disease Control and Prevention

CLL:

Chronic lymphocytic leukemia

CML:

Chronic myeloid leukemia

COMWEL:

Korea Workers’ Compensation and Welfare Service

DDREF:

Dose and the dose rate effectiveness factor

EEOICPA:

Energy Employees Occupational Illness Compensation Program Act of 2000

ERR:

Excess relative risk

IACIA:

Industrial Accident Compensation Insurance Act

IARC:

International Agency for Research on Cancer

ILO:

International Labor Organization

KOSHA:

Korea Occupational Safety and Health Agency

NDR:

National Dose Registries

NDT:

Non-destructive testing

NSSC:

Nuclear Safety and Security Commission

NTP:

U.S. National Toxicology Program

PC:

Probability of causation

References

  1. 1.

    IARC. Radiation: A Review of Human Carcinogens. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Lyon: IARC; 2012. p. 1–362.

  2. 2.

    List of occupational diseases (revised 2010). Identification and recognition of occupational diseases: Criteria for incorporating diseases in the ILO list of occupational diseases. Geneva: International Labour Office; 2010.

  3. 3.

    Enforcement Decree of the Labor Standards Act. http://www.moleg.go.kr/english/korLawEng ;jsessionid=Z6jy3UxayMlMOS1NdCVG9zjfXT8ks QsO3U21F6JbJoj4ZCCz6guDcUa1cfJvw4ov.moleg_a1_servlet_engine2?pstSeq = 57979&pageI ndex=5. Accessed 17 July 2017.

  4. 4.

    Lee YJ, Lee JW, Jeong GS. The increased use of radiation requires enhanced activities regarding radiation safety control. J Radiat Ind. 2015;9(2):103–9.

  5. 5.

    NSSC, KINS, KINAC. 2015 Nuclear Safety Yearbook. 2016.

  6. 6.

    Choi SY, Kim TH, Chung CK, Cho CK, Paik NS. Analysis of radiation workers’ dose records in the Korean National Dose Registry. Radiat Prot Dosimetry. 2001;95(2):143–8.

  7. 7.

    Lee WJ, Cha ES, Ha M, Jin YW, Hwang SS, Kong KA, et al. Occupational radiation doses among diagnostic radiation workers in South Korea, 1996-2006. Radiat Prot Dosimetry. 2009;136(1):50–5.

  8. 8.

    KCDC. 2014 occupational radiation exposure in diagnostic radiology in Korea. 2015.

  9. 9.

    El Ghissassi F, Baan R, Straif K, Grosse Y, Secretan B, Bouvard V, et al. A review of human carcinogens--part D: radiation. Lancet Oncol. 2009;10(8):751–2.

  10. 10.

    European Agency for Safety and Health at Work. Exposure to carcinogens and work- related cancer: A review of assessment methods. Luxembourg: Publications Office of the European Union; 2014.

  11. 11.

    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(3):229–43.

  12. 12.

    Cardis E, Howe G, Ron E, Bebeshko V, Bogdanova T, Bouville A, et al. Cancer consequences of the Chernobyl accident: 20 years on. J Radiol Prot. 2006;26(2):127–40.

  13. 13.

    Charles M. UNSCEAR report 2000: sources and effects of ionizing radiation. United Nations Scientific Comittee on the Effects of Atomic Radiation. J Radiol Prot. 2001;21(1):83–6.

  14. 14.

    Jacob P, Bogdanova TI, Buglova E, Chepurniy M, Demidchik Y, Gavrilin Y, et al. Thyroid cancer risk in areas of Ukraine and Belarus affected by the Chernobyl accident. Radiat Res. 2006;165(1):1–8.

  15. 15.

    Likhtarov I, Kovgan L, Vavilov S, Chepurny M, Ron E, Lubin J, et al. Post-Chernobyl thyroid cancers in Ukraine. Report 2: risk analysis. Radiat Res. 2006;166(2):375–86.

  16. 16.

    Ivanov VK, Chekin SY, Kashcheev VV, Maksioutov MA, Tumanov KA. Risk of thyroid cancer among Chernobyl emergency workers of Russia. Radiat Environ Biophys. 2008;47(4):463–7.

  17. 17.

    Ivanov VK, Maksioutov MA, Chekin SY, Petrov AV, Biryukov AP, Kruglova ZG, et al. The risk of radiation-induced cerebrovascular disease in Chernobyl emergency workers. Health Phys. 2006;90(3):199–207.

  18. 18.

    Ivanov VK, Tsyb AF, Khait SE, Kashcheev VV, Chekin SY, Maksioutov MA, et al. Leukemia incidence in the Russian cohort of Chernobyl emergency workers. Radiat Environ Biophys. 2012;51(2):143–9.

  19. 19.

    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(1):13–23.

  20. 20.

    Kesminiene A, Evrard AS, Ivanov VK, Malakhova IV, Kurtinaitis J, Stengrevics A, et al. Risk of hematological malignancies among Chernobyl liquidators. Radiat Res. 2008;170(6):721–35.

  21. 21.

    Kesminiene A, Evrard AS, Ivanov VK, Malakhova IV, Kurtinaitise J, Stengrevics A, et al. Risk of thyroid cancer among chernobyl liquidators. Radiat Res. 2012;178(5):425–36.

  22. 22.

    Jargin SV. Solid cancer increase among Chernobyl liquidators: alternative explanation. Radiat Environ Biophys. 2015;54(3):373–5.

  23. 23.

    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(4):396–416.

  24. 24.

    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(7):e276–e81.

  25. 25.

    Shilnikova NS, Preston DL, Ron E, Gilbert ES, Vassilenko EK, Romanov SA, et al. Cancer mortality risk among workers at the Mayak nuclear complex. Radiat Res. 2003;159(6):787–98.

  26. 26.

    Hunter N, Kuznetsova IS, Labutina EV, Harrison JD. Solid cancer incidence other than lung, liver and bone in Mayak workers: 1948-2004. Br J Cancer. 2013;109(7):1989–96.

  27. 27.

    Gilbert ES, Koshurnikova NA, Sokolnikov ME, Shilnikova NS, Preston DL, Ron E, et al. Lung cancer in Mayak workers. Radiat Res. 2004;162(5):505–16.

  28. 28.

    Akiba S, Mizuno S. The third analysis of cancer mortality among Japanese nuclear workers, 1991-2002: estimation of excess relative risk per radiation dose. J Radiol Prot. 2012;32(1):73–83.

  29. 29.

    Matanoski GM, Tonascia JA, Correa-Villasenor A, Yates KC, Fink N, Elliott E, et al. Cancer risks and low-level radiation in U.S. shipyard workers. J Radiat Res. 2008;49(1):83–91.

  30. 30.

    Metz-Flamant C, Laurent O, Samson E, Caer-Lorho S, Acker A, Hubert D, et al. Mortality associated with chronic external radiation exposure in the French combined cohort of nuclear workers. Occup Environ Med. 2013;70(9):630–8.

  31. 31.

    Richardson DB, Wing S. Leukemia mortality among workers at the Savannah River Site. Am J Epidemiol. 2007;166(9):1015–22.

  32. 32.

    Zeeb H, Hammer GP, Blettner M. Epidemiological investigations of aircrew: an occupational group with low-level cosmic radiation exposure. J Radiol Prot. 2012;32(1):N15–9.

  33. 33.

    Band PR, Le ND, Fang R, Deschamps M, Coldman AJ, Gallagher RP, et al. Cohort study of Air Canada pilots: mortality, cancer incidence, and leukemia risk. Am J Epidemiol. 1996;143(2):137–43.

  34. 34.

    Hammer GP, Auvinen A, De Stavola BL, Grajewski B, Gundestrup M, Haldorsen T, et al. Mortality from cancer and other causes in commercial airline crews: a joint analysis of cohorts from 10 countries. Occup Environ Med. 2014;71(5):313–22.

  35. 35.

    Pinkerton LE, Waters MA, Hein MJ, Zivkovich Z, Schubauer-Berigan MK, Grajewski B. Cause-specific mortality among a cohort of U.S. flight attendants. Am J Ind Med. 2012;55(1):25–36.

  36. 36.

    Pukkala E, Aspholm R, Auvinen A, Eliasch H, Gundestrup M, Haldorsen T, et al. Incidence of cancer among Nordic airline pilots over five decades: occupational cohort study. BMJ. 2002;325(7364):567.

  37. 37.

    Wartenberg D, Stapleton CP. Risk of breast cancer is also increased among retired US female airline cabin attendants. BMJ. 1998;316(7148):1902.

  38. 38.

    Seong KM, Seo S, Lee D, Kim MJ, Lee SS, Park S, et al. Is the Linear No-Threshold Dose- Response Paradigm Still Necessary for the Assessment of Health Effects of Low Dose Radiation? J Korean Med Sci. 2016;31(Suppl 1):S10–23.

  39. 39.

    Kim HRAY, Jung SH. Epidemiologic Characteristics of Malignant Mesothelioma in Korea. J Korean Med Assoc. 2009;52:449–55.

  40. 40.

    Jeong MS, Jin YW, Kim CS. Program for estimating the probability of causation to Korean radiation workers with cancer. J Radiat Prot Res. 2004;29(4):221–30.

  41. 41.

    IAEA. Approaches to attribution of detrimental health effects to occupational ionizing Radiation exposure and their application in compensation programmes for cancer. Occupational safety and health series 73. 2010.

  42. 42.

    Boice JD Jr, Engholm G, Kleinerman RA, Blettner M, Stovall M, Lisco H, et al. Radiation dose and second cancer risk in patients treated for cancer of the cervix. Radiat Res. 1988;116(1):3–55.

  43. 43.

    Mattsson A, Hall P, Ruden BI, Rutqvist LE. Incidence of primary malignancies other than breast cancer among women treated with radiation therapy for benign breast disease. Radiat Res. 1997;148(2):152–60.

  44. 44.

    Carr ZA, Kleinerman RA, Stovall M, Weinstock RM, Griem ML, Land CE. Malignant neoplasms after radiation therapy for peptic ulcer. Radiat Res. 2002;157(6):668–77.

  45. 45.

    Preston DL, Shimizu Y, Pierce DA, Suyama A, Mabuchi K. Studies of mortality of atomic bomb survivors. Report 13: Solid cancer and noncancer disease mortality: 1950-1997. Radiat Res. 2003;160(4):381–407.

  46. 46.

    Preston DL, Ron E, Tokuoka S, Funamoto S, Nishi N, Soda M, et al. Solid cancer incidence in atomic bomb survivors: 1958-1998. Radiat Res. 2007;168(1):1–64.

  47. 47.

    Darby SC, Reeves G, Key T, Doll R, Stovall M. Mortality in a cohort of women given X-ray therapy for metropathia haemorrhagica. Int J Cancer. 1994;56(6):793–801.

  48. 48.

    Weiss HA, Darby SC, Doll R. Cancer mortality following X-ray treatment for ankylosing spondylitis. Int J Cancer. 1994;59(3):327–38.

  49. 49.

    Gilbert ES, Stovall M, Gospodarowicz M, Van Leeuwen FE, Andersson M, Glimelius B, et al. Lung cancer after treatment for Hodgkin's disease: focus on radiation effects. Radiat Res. 2003;159(2):161–73.

  50. 50.

    Schneider AB, Shore-Freedman E, Ryo UY, Bekerman C, Favus M, Pinsky S. Radiation-induced tumors of the head and neck following childhood irradiation. Prospective studies. Medicine (Baltimore). 1985;64(1):1–15.

  51. 51.

    Ron E, Modan B, Preston D, Alfandary E, Stovall M, Boice JD Jr. Radiation-induced skin carcinomas of the head and neck. Radiat Res. 1991;125(3):318–25.

  52. 52.

    Ron E, Preston DL, Kishikawa M, Kobuke T, Iseki M, Tokuoka S, et al. Skin tumor risk among atomic-bomb survivors in Japan. Cancer Causes Control. 1998;9(4):393–401.

  53. 53.

    Little MP, Charles MW, Hopewell JW, Mayall A, Lloyd DC, Edwards AA, et al. Assessment of skin doses. NRPB. 1997;8:1–43.

  54. 54.

    Shore RE, Moseson M, Xue X, Tse Y, Harley N, Pasternack BS. Skin cancer after X-ray treatment for scalp ringworm. Radiat Res. 2002;157(4):410–8.

  55. 55.

    Howe GR, McLaughlin J. Breast 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 breast cancer mortality in the atomic bomb survivors study. Radiat Res. 1996;145(6):694–707.

  56. 56.

    Preston DL, Mattsson A, Holmberg E, Shore R, Hildreth NG, Boice JD Jr. Radiation effects on breast cancer risk: a pooled analysis of eight cohorts. Radiat Res. 2002;158(2):220–35.

  57. 57.

    Lundell M, Hakulinen T, Holm LE. Thyroid cancer after radiotherapy for skin hemangioma in infancy. Radiat Res. 1994;140(3):334–9.

  58. 58.

    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(6):735–40.

  59. 59.

    Ron E, Lubin JH, Shore RE, Mabuchi K, Modan B, Pottern LM, et al. Thyroid cancer after exposure to external radiation: a pooled analysis of seven studies. Radiat Res. 1995;141(3):259–77.

  60. 60.

    Little MP, Weiss HA, Boice JD Jr, Darby SC, Day NE, Muirhead CR. Risks of leukemia in Japanese atomic bomb survivors, in women treated for cervical cancer, and in patients treated for ankylosing spondylitis. Radiat Res. 1999;152(3):280–92.

  61. 61.

    Travis LB, Andersson M, Gospodarowicz M, van Leeuwen FE, Bergfeldt K, Lynch CF, et al. Treatment-associated leukemia following testicular cancer. J Natl Cancer Inst. 2000;92(14):1165–71.

  62. 62.

    Preston DL, Pierce DA, Shimizu Y, Cullings HM, Fujita S, Funamoto S, et al. Effect of recent changes in atomic bomb survivor dosimetry on cancer mortality risk estimates. Radiat Res. 2004;162(4):377–89.

  63. 63.

    Muirhead CR, O’Hagan JA, Haylock RG, Phillipson MA, Willcock T, Berridge GL, et al. Mortality and cancer incidence following occupational radiation exposure: third analysis of the National Registry for Radiation Workers. Br J Cancer. 2009;100(1):206–12.

  64. 64.

    Ahn YS, Park RM, Koh DH. Cancer admission and mortality in workers exposed to ionizing radiation in Korea. J Occup Environ Med. 2008;50(7):791–803.

  65. 65.

    Jeong M, Jin YW, Yang KH, Ahn YO, Cha CY. Radiation exposure and cancer incidence in a cohort of nuclear power industry workers in the Republic of Korea, 1992-2005. Radiat Environ Biophys. 2010;49(1):47–55.

  66. 66.

    Howe GR, Zablotska LB, Fix JJ, Egel J, Buchanan J. Analysis of the mortality experience amongst U.S. nuclear power industry workers after chronic low-dose exposure to ionizing radiation. Radiat Res. 2004;162(5):517–26.

  67. 67.

    Zablotska LB, Lane RS, Thompson PA. A reanalysis of cancer mortality in Canadian nuclear workers (1956-1994) based on revised exposure and cohort data. Br J Cancer. 2014;110(1):214–23.

  68. 68.

    Merzenich H, Hammer GP, Troltzsch K, Ruecker K, Buncke J, Fehringer F, et al. Mortality risk in a historical cohort of nuclear power plant workers in Germany: results from a second follow-up. Radiat Environ Biophys. 2014;53(2):405–16.

  69. 69.

    Weiss HA, Darby SC, Fearn T, Doll R. Leukemia mortality after X-ray treatment for ankylosing spondylitis. Radiat Res. 1995;142(1):1–11.

  70. 70.

    Damber L, Larsson LG, Johansson L, Norin T. A cohort study with regard to the risk of haematological malignancies in patients treated with x-rays for benign lesions in the locomotor system. I. Epidemiological analyses. Acta Oncol. 1995;34(6):713–9.

  71. 71.

    Inskip PD, Kleinerman RA, Stovall M, Cookfair DL, Hadjimichael O, Moloney WC, et al. Leukemia, lymphoma, and multiple myeloma after pelvic radiotherapy for benign disease. Radiat Res. 1993;135(1):108–24.

  72. 72.

    Curtis RE, Boice JD Jr, Stovall M, Flannery JT, Moloney WC. Leukemia risk following radiotherapy for breast cancer. J Clin Oncol. 1989;7(1):21–9.

  73. 73.

    Curtis RE, Boice JD Jr, Stovall M, Bernstein L, Holowaty E, Karjalainen S, et al. Relationship of leukemia risk to radiation dose following cancer of the uterine corpus. J Natl Cancer Inst. 1994;86(17):1315–24.

  74. 74.

    Romanenko AY, Finch SC, Hatch M, Lubin JH, Bebeshko VG, Bazyka DA, et al. The Ukrainian-American study of leukemia and related disorders among Chornobyl cleanup workers from Ukraine: III. Radiation risks. Radiat Res. 2008;170(6):711–20.

  75. 75.

    The Compensation Scheme for Radiation Linked Diseases. http://www.csrld.org.uk/html/making_claim.php. Accessed 10 May 2016.

  76. 76.

    Division of Energy Employees Occupational Illness Compensation (DEEOIC). https://www.dol.gov/owcp/energy/. Accessed 10 May 2016.

  77. 77.

    Electronic Code of Federal Regulations. http://www.ecfr.gov/cgi-bin/text- idx?rgn=div5&node=38:1.0.1.1.4. Accessed 10 May 2016.

  78. 78.

    Radiation Exposure Compensation Act. https://www.justice.gov/civil/common/reca. Accessed 10 May 2016.

Download references

Acknowledgements

This research was supported by the Nuclear Safety Research Program through the Korea Foundation Of Nuclear Safety (KOFONS), granted financial resource from the Nuclear Safety and Security Commission (NSSC), Republic of Korea (No. 1303028 and 1503008).

Funding

This work was supported by the Nuclear Safety Research Program through the Korea Foundation Of Nuclear Safety (KOFONS), granted financial resource from the Nuclear Safety and Security Commission (NSSC), Republic of Korea (No. 1303028 and 1503008).

Availability of data and materials

Data sharing no applicable to this article as no datasets were generated or analysed during the current study.

Author information

Affiliations

  1. National Radiation Emergency Medical Center, Korea Institute of Radiological & Medical Sciences, 75, Nowon-ro, Nowon-gu, Seoul, 01812, Republic of Korea
    • Songwon Seo
    • , Dalnim Lee
    • , Ki Moon Seong
    • , Sunhoo Park
    •  & Young Woo Jin
  2. Department of Preventive Medicine, Korea University College of Medicine, Seoul, Korea
    • Songwon Seo
  3. Department of Occupational Medicine, Sungkyunkwan University, School of Medicine, Seoul, Korea
    • Soo-Geun Kim
  4. The Institute for Occupational Health, Yonsei University College of Medicine, Seoul, Korea
    • Jong-Uk Won
Authors
  1. Songwon Seo
    View author publications
    You can also search for this author in
  2. Dalnim Lee
    View author publications
    You can also search for this author in
  3. Ki Moon Seong
    View author publications
    You can also search for this author in
  4. Sunhoo Park
    View author publications
    You can also search for this author in
  5. Soo-Geun Kim
    View author publications
    You can also search for this author in
  6. Jong-Uk Won
    View author publications
    You can also search for this author in
  7. Young Woo Jin
    View author publications
    You can also search for this author in

Contributions

YWJ and SS designed this study and wrote this manuscript. DL, KMS, and SP contributed to the draft of the manuscript and identification of related references. SGK and JUW provided valuable inputs in developing the study design and contents. All authors reviewed and approved the final manuscript.

Corresponding author

Correspondence to Young Woo Jin.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Seo, S., Lee, D., Seong, K.M. et al. Radiation-related occupational cancer and its recognition criteria in South Korea. Ann of Occup and Environ Med 30, 9 (2018). https://doi.org/10.1186/s40557-018-0219-y

Download citation

Keywords

  • Radiation exposure
  • Occupational cancer
  • Recognition
  • Korea

Annals of Occupational and Environmental Medicine

ISSN: 2052-4374

Contact us