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  • Review
  • Open Access

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

  • 1, 2,
  • 1,
  • 1,
  • 1,
  • 3,
  • 4 and
  • 1Email author
Annals of Occupational and Environmental MedicineThe official journal of the Korean Society of Occupational and Environmental Medicine201830:9

https://doi.org/10.1186/s40557-018-0219-y

  • Received: 3 March 2017
  • Accepted: 17 January 2018
  • Published:

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.

Keywords

  • Radiation exposure
  • Occupational cancer
  • Recognition
  • Korea

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 [13]. 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

Year

2010

2011

2012

2013

2014

Category

Number of workers

Mean dose

Number of workers

Mean dose

Number of workers

Mean dose

Number of workers

Mean dose

Number of workers

Mean dose

Radiation workers

Medical institutes

3833

0.99

4133

0.96

4376

0.87

4734

0.73

5038

0.55

Industry

5464

0.10

5456

0.03

6352

0.07

5842

0.16

5237

0.02

NDT

5852

2.43

6075

2.39

6792

3.43

7166

3.87

7530

2.37

Production and sales

1243

0.67

1573

0.53

1563

0.85

1702

0.41

1912

0.29

Research institutes

2062

0.07

2139

0.05

2232

0.03

2198

0.03

2183

0.02

Educational institutes

4876

0.05

4954

0.05

4816

0.04

4788

0.04

4521

0.06

Public institutes

466

0.02

827

0.61

872

0.57

932

0.42

961

0.41

Military

236

0.05

241

1.81

264

0.02

280

0.03

264

0.08

Nuclear power plant

13,236

1.20

14,758

0.80

15,023

0.73

14,780

0.82

14,253

0.58

Total

37,268

0.96

40,156

0.81

42,290

0.96

42,422

1.07

41,899

0.72

Diagnostic radiation workers

Radiation technologist

18,722

1.21

19,791

1.16

20,523

1.01

21,636

0.94

22,419

0.85

Physician

11,661

0.34

12,622

0.36

13,076

0.32

13,738

0.32

14,950

0.31

Dentist

12,822

0.16

13,849

0.18

14,424

0.15

14,905

0.15

15,951

0.15

Dental hygienist

6110

0.13

7088

0.15

7727

0.12

8064

0.12

8912

0.12

Diagnostic radiologist

1468

0.41

1545

0.29

1456

0.32

1448

0.31

1475

0.24

Nurse

2177

0.4

2936

0.37

3171

0.33

3397

0.32

4891

0.22

Nursing assistant

817

0.3

927

0.26

873

0.24

846

0.3

1081

0.19

Medical assistant

161

0.3

198

0.34

168

0.55

222

0.49

329

0.34

Others

1676

0.47

1474

0.42

1517

0.33

1676

0.68

1088

0.34

Total

55,614

0.58

60,430

0.56

62,935

0.48

65,932

0.47

71,096

0.41

Source: 2015 Nuclear Safety yearbook [5] and 2014 Occupational Radiation Exposure in Diagnostic Radiology in Korea [8]

NDT non-destructive testing

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

Organ site

Selected key studies

Stomach

Boice et al. (1988) [42], Mattsson et al. (1997) [43], Carr et al.

Colon

(2002) [44], Preston et al. (2003, 2007) [45, 46]

Lung

Darby et al. (1994) [47], Preston et al. (2003, 2007) [45, 46]

Basal cell skin carcinoma

Weiss et al. (1994) [48], Carr et al. (2002) [44], Gilbert et al.

(2003) [49], Preston et al. (2003, 2007) [45, 46]

Schneider et al. (1985) [50], Ron et al. (1991, 1998) [51, 52], Little et al. (1997) [53], Shore et al. (2002)[54], Preston et al. (2007) [46]

Female breast

Howe & McLaughlin (1996) [55], Preston et al. (2002, 2003, 2007) [45, 46, 56]

Thyroid

Lundell et al. (1994) [57], Lindberg et al. (1995) [58], Ron et al. (1995) [59], Preston et al. (2007) [46]

Leukemia, excluding CLL

Little et al. (1999) [60], Travis et al. (2000) [61], Preston et al. (2003, 2004) [45, 62], Muirhead et al. (2009) [63]

Source: Monographs on the evaluation of carcinogenic risks to humans [9]. CLL, chronic lymphocytic leukemia

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 [1215]. 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 [1621]. 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 [2527]. 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 [2831]. 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

     

Mean

  

Number of event cases

  

Country

Study

Cohort size

Exposure period

Follow-up period

cumulative dose (mSv)

Person years

Types of events

ERR (95% CI)

SMR or SIR (95% CI)

15-country

Cardis et al. (2007) [23]

407,391

1943-2000

1943-2000

19.4

5,192,710

Mortality

5,024

4,820

0.97

b(0.27, 1.8)c

0.58

b

(-0.1, 1.39)

a1.03 (0.65, 1.53)

Korea

aAhn et al. (2008) [64]

79,679

1984-2004

1984-2004

1992-2004

1989-2005

6.1

6.1

633,159

415,298

Mortality

Morbidity

256

564

7.2

b(-5, 21) 2.6 (-4, 10)b

0.73 (0.64, 0.82)

 

Jeong et al. (2010) [65]

8,429

1978-2005

1992-2005

19.86

63,503

Incidence

96

2.06 (-191, 9)

1.06 (0.86, 1.29)

U.K.

Muirhead et al. (2009) [63]

174,541

1946-2001

1965-2001

24.9

3,900,000

Mortality

Incidence

7,455

10,855

0.28 (-0.03, 0.62) 0.27 (0.00, 0.56)

0.84 (0.82, 0.86)

U.S.

Howe et al. (2004) [66]

53,698

Mid-1960s

1979-1997

25.7

698,051

Mortality

368

0.51 (-2.01, 4.64)

0.65 (0.59, 0.72)

Canada

Zablotska et al. (2014) [67]

45,316

1951-1994

1956-1994

21.64

613,648

Mortality

468

1.2

(-0.73, 4.33)

0.72 (0.66, 0.78)

France

Flamant et al. (2013) [30]

59,021

1950-2004

1968-2004

16.1

1,467,611

Mortality

2,312

0.34

b(-0.56, 1.38)

-

Germany

Merzenich et al. (2014) [68]

8,972

1966-2008

1991-2008

29.5

130,737

Mortality

119

-

0.63 (0.5, 0.8)

Japan

Akiba et al. (2012) [28]

200,583

1977-2002

1991-2002

12.2

1,373,000

Mortality

2,636

1.26 (-0.27, 3)

-

Russia

Shilnikova et al. (2003) [25]

21,557

1948-1997

1948-1997

810 mGy

720,000

Mortality

1,730

0.15

b(0.09, 0.2)

-

 

Hunter et al. (2013) [26]

22,366

1948-2004

1948-2004

510 mGy

535,932

Incidence

1,447

0.07 (0.01, 0.15)

-

a all cancer; b 90% confidence interval; c 15-country excluding Canada; ERR, excess relative risk; SMR, standardized mortality ratio; SIR, standardized incidence ratio

Table 4

Risks of leukemia (excluding CLL) in epidemiological studies of nuclear workers

     

Mean

  

Number of event cases

  

Country

Study

Cohort size

Exposure

period

Follow-up

period

cumulative

dose

(mSv)

Person

years

Types of events

ERR

(95% CI)

SMR or SIR (95% CI)

15-country

Cardis et al. (2007) [23]

407,391

1943-2000

1943-2000

19.4

5,192,710

Mortality

196

1.93

b(<0, 7.14)

-

3-country

(INWORKS)

Leuraud et al. (2015) [24]

308,297

1943-2005

1944-2005

15.9mGy

8,220,000

Mortality

531

2.96 (1.17, 5.21)

-

Korea

aAhn et al. (2008) [64]

79,679

1984-2004

1984-2004

1992-2004

1989-2005

6.1

6.1

633.159

415,298

Mortality

Morbidity

9

14

16.8

b(-34, 149) 15.8

b(-31, 108)

0.59 (0.28, 1.06)

 

Jeong et al. (2010) [65]

8,429

1978-2005

1992-2005

19.86

63,503

Incidence

3

NC

1.34 (0.27, 3.92)

U.K.

Muirhead et al. (2009) [63]

174,541

1946-2001

1965-2001

24.9

3,900,000

Mortality

Incidence

198

234

1.71 (-0.17, 4.92) 1.78 (-0.06, 4.99)

0.89 (0.76, 1.03)

U.S.

Howe et al. (2004) [66]

53,698

Mid-1960s

1979-1997

25.7

698,051

Mortality

26

5.67 (-2.56, 30.4)

a

1.07 (0.71, 1.53)

Canada

Zablotska et al. (2014) [67]

45,316

1951-1994

1956-1994

21.64

613,648

Mortality

17

9.79 (<-1.49, 107)

0.78 (0.45, 1.25)

France

Flamant et al. (2013) [30]

59,021

1950-2004

1968-2004

16.1

1,467,611

Mortality

60

3.96

b(<0, 16.82)

-

Germany

Merzenich et al. (2014) [68]

8,972

1966-2008

1991-2008

29.5

130,737

Mortality

7

-

1.19 (0.41, 2.75)

aJapan

Akiba et al. (2012) [28]

200,583

1977-2002

1991-2002

12.2

1,373,000

Mortality

80

-1.93 (-6.12, 8.57)

-

Russia

Shilnikova et al. (2003) [25]

21,557

1948-1997

1948-1997

810 mGy

720,000

Mortality

66

1

b(0.5, 2)

-

a all leukemia; b 90% CI; NC was no convergence of deviance after maximum iteration. CLL, chronic lymphocytic leukemia

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 [3337]. 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)

Year

Gender

Age

Occupation

Employment period (year)

Exposure dose (mSv)

Cancer site

Association with occupation

2015

Female

34

Nurse

11.3

Below limits

Breast cancer

Low

Female

43

Semiconductor manufacturing

7

Below limits

Breast cancer

Low

Female

42

Semiconductor manufacturing

5.6

0.33

Breast cancer

Low

Female

35

Semiconductor manufacturing

8.7

Below limits

Breast cancer

Low

Female

29

Artifact preservation

6.8

Below limits

Intraepithelial carcinoma

Low

Male

40

Semiconductor manufacturing

5.5

Below limits

Thyroid papillary carcinoma

Low

Female

33

Semiconductor manufacturing

3.1

Below limits

Brain tumor

Low

2013~ 2014

Male

43

NDT

0.3

7.23

Acute myeloid leukemia

Low

Male

38

NDT

10

28.84 (for 5 years)

Acute lymphocytic leukemia

High

Male

47

Radiation oncology specialist

0.8

Possibly over exposure dose limit

Acute lymphocytic leukemia

High

Male

41

NDT

11

Below limits

Malignant lymphoma

Low

Male

37

Semiconductor equipment mechanic

13

20.15~ 34.71

Chronic myelomonocytic leukemia

Low

Male

52

Radiologist

26

Below limits

Rectal cancer

Low

Female

38

Hospital infection management

11

Below limits

Glioblastoma

Low

Female

50

Dental nurse

6.4

1.87~ 93.48

Thyroid cancer

Low

Female

43

Radiologist

18

Below limits

Thyroid cancer

Low

Male

58

NDT

5

80.77

Aplastic anemia

Low

2012

Male

45

Radiologist

21

204.17

Chronic myeloid leukemia

High

Male

58

Power plant equipment mechanic

21

1.71

Acute lymphocytic leukemia

Low

Male

40

X-ray apparatus seller

10.5

140~ 260

Anaplastic large cell lymphoma

High

Male

53

CT radiographer

18

24.34

Thrombocytopenia

Low

Male

48

Nuclear worker

7.8

12.25

Stomach cancer

Low

Female

33

Semiconductor implant operation

4.7

Below limits

Breast cancer

Low

Male

44

Melting furnace operation

19.6

Below limits

Kidney cancer

Low

2011

Male

42

Artifact preservation

7.2

Below limits

Acute lymphocytic leukemia

Low

Male

35

Production

1.4

Below limits

Acute myeloid leukemia

Low

2010

Male

39

Machine operator

11

16.51 + potential additional exposure

Acute myeloid leukemia

Issue

Female

32

Cleaning

5

Below limits

Acute myeloid leukemia

Low

Male

47

Manufacturing

21

Below limits

Acute myeloid leukemia

Low

Male

52

Process technician

20

Possible exposure

Brain tumor

Issue

2009

Male

47

Electric power generation worker

21.4

98.32

Stomach and pancreatic cancer

cancer

Low

Male

36

Hospital worker

8

4.5~ 55.4

Thyroid cancer

Low

2008

Female

21

Semiconductor manufacturing

2.5

Below limits

Acute myeloid leukemia

Low

Male

31

Semiconductor manufacturing

7

Below limits

Acute lymphocytic leukemia

Low

Female

30

Semiconductor manufacturing

11

Below limits

Acute myeloid leukemia

Low

2005

Male

47

NDT

0.7

Possibly twice over exposure dose limit

Carcinoma of unknown primary site

High

2004

Male

45

Laboratory worker

14

Below limits

Thyroid cancer

Low

Male

59

Administration

23

51.79

Pancreatic cancer

Low

2002

Male

43

Electric power generation worker

8

1.24

Lung cancer

Low

2001

Male

41

Welder

7

37.87

Non-Hodgkin lymphoma

Low

2000

Male

53

Administration

23

Below limits

Lung cancer

Low

Male

37

Welder

10

18.5

Acute myeloid leukemia

High

Male

28

Analyst

2

Below limits

Panmyelophthisis

Low

Below limits: Exposure dose was estimated at natural exposure levels or below the dose limit of radiation workers

NDT non-destructive testing, CT computed tomography

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

Cohort (patients or workers)

Study

Events

Cohort

size

Number of events

Risk

Ankylosing spondylitis

Weiss et al. (1995) [69]

Mortality

15,577

7

RR=1.44 (95% CI: 0.62, 2.79)

Benign locomotor lesions

Damber et al. (1995) [70]

Incidence

20,024

50

SIR=1.07 (95% CI: 0.80, 1.41)

Benign gynecological disease

Inskip et al. (1993) [71]

Mortality

12,955

21

RR=1.1 (90% CI: 0.5, 3.0)

Breast cancer

Curtis et al. (1989) [72]

Incidence

22,753

10

RR=1.84 (90% CI: 0.5, 6.7)

Uterine corpus cancer

Curtis et al. (1994) [73]

Incidence

110,000

54

RR=0.90 (95% CI: 0.4, 1.9)

International Radiation

Boice et al. (1988) [42]

   

OR=1.03 (90% CI: 0.3, 3.9)

Study of Cervical Cancer Patients

Incidence

11,030

52

Chernobyl liquidators

Romanenko et al. (2008) [74]

Incidence

110,645

39

ERR/Sv=4.09 (95% CI: <0, 14.41)

Chernobyl liquidators

Kesminiene et al. (2008) [20]

Incidence

146,000

21

ERR/Sv=4.7 (90% CI: -®, 76.1)

France nuclear workers

Flamant et al. (2013) [30]

Mortality

59,021

18

ERR/Sv=-1.36 (90% CI: <0, 14.94)

IARC 15-country

nuclear

workers

Cardis et al. (2007) [23]

Mortality

407,391

47

ERR/Sv=-1.0 (90% CI: -5.0, 3.7)

U.K. NRRW

Muirhead et al.

(2009) [63]

Mortality

174,541

69

ERR/Sv=<-1.92 (90% CI: <-1.92, 1.23)

 

Incidence

174,541

128

ERR/Sv=-0.117

  

(90% CI: -1.42, 2.71)

INWORKS

Leuraud et al. (2015) [24]

Mortality

308,297

138

ERR/Gy=-1.06 (90% CI: <0, 1.81)

RR, relative risk; OR, odds ratio; ERR, excess relative risk; CI, confidence interval; IARC, International Agency for Research on Cancer; NRRW, National Registry for Radiation Workers; INWORKS, International Nuclear Workers Study; ; SIR, standardized incidence ratio

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

Criteria items

Korea

U.K.

U.S. a

France

Eligible cancer sites

Liver (without cirrhosis or hepatitis virus), Thyroid, Ovary, Brain, Multiple myeloma, Colon, Bladder, Non-Hodgkin lymphoma, Esophagus, Kidney, Female breast, Stomach, Pancreas, Salivary gland, Lung, Skin, Leukemia (except CLL)

Bladder, Bone, Brain and central nervous system, Female breast, Colon, Leukemia (except CLL) , Liver, Esophagus, Respiratory/Lung, Prostate, Ovary, Skin (non-melanoma), Uterus, Thyroid, Other tissues

Leukemia with or without CLL, Lymphomas (except Hodgkin lymphomas), Multiple myeloma, Thyroid, Breast, Ovary, Stomach, Lung, Colon, Liver, Bladder, Esophagus, Pancreas, Bone, Salivary gland, Kidney, Brain and central nervous system, Pharynx, Small intestine, Biliary tract and gall bladder, Skin, Rectum, Larynx, Prostate, Pharynx

Leukemia, Primary lung (due to inhalation), Bone sarcoma

Exposure period

-

-

Employed at least 1 year -Uranium miner: >40 months

-

Latency period (since first exposure)

Cancer (except leukemia): 5 years Leukemia (except CLL): 2 years

-

Leukemia (except CLL): 2 years Others: 5 years

-

Occurrence period (after exposure)

Within 20 years

-

Bone cancer: within 30 years Leukemia: any time Others: >5 years

Leukemia and lung cancer: within 30 years Bone sarcoma: within 50 years

PC (Probability of causation) or degree of disability

Cancer (except leukemia): >50% Leukemia (except CLL): >33%

>20% (Compensated at different rates according to the PC and >50% for full compensation)

>50% (upper 99% confidence level)

Degree of disability: >25%

Reference

Notification (No. 2014-78) of the NSSC

Occupational safety and health series 73 [41], Compensation scheme for radiation-linked diseases [75]

Occupational safety and health series 73 [41], Energy employees occupational illness compensation program [76], electronic code of federal regulations [77], radiation exposure compensation Act [78],

Occupational safety and health series 73 [41]

a Eligible cancer sites differ across occupations; exposure period applies only to uranium workers, including uranium miners, millers, ore transporters, and non-military participants in atomic weapons testing; latency period applies only to energy employees employed at the U.S. Department of Energy (DOE) and other specified contractor facilities; occurrence period only applies to soldiers

CLL, chronic lymphocytic leukemia; NSSC, Nuclear Safety and Security Commission

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

Declarations

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.

Authors’ 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.

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

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Open AccessThis 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.

Authors’ Affiliations

(1)
National Radiation Emergency Medical Center, Korea Institute of Radiological & Medical Sciences, 75, Nowon-ro, Nowon-gu, Seoul, 01812, Republic of Korea
(2)
Department of Preventive Medicine, Korea University College of Medicine, Seoul, Korea
(3)
Department of Occupational Medicine, Sungkyunkwan University, School of Medicine, Seoul, Korea
(4)
The Institute for Occupational Health, Yonsei University College of Medicine, Seoul, Korea

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