DÄ internationalArchive4/2021Mortality in Underground Miners in a Former Uranium Ore Mine

Original article

Mortality in Underground Miners in a Former Uranium Ore Mine

Results of a Cohort Study Among Former Employees of Wismut AG in Saxony and Thuringia

Dtsch Arztebl Int 2021; 118: 41-8. DOI: 10.3238/arztebl.m2021.0001

Kreuzer, M; Deffner, V; Schnelzer, M; Fenske, N

Background: From 1946 to 1990, more than 400 000 people were employed by Wismut AG, a Soviet/Soviet-German corporation (German abbreviation: SAG/SDAG), in the East German states of Saxony and Thuringia. In the early years in particular, employees were exposed to large amounts of radon and respirable crystalline silica.

Methods: In a cohort of 35 204 former underground employees of Wismut AG, mortality was analyzed in comparison to the general male population of East Germany, and the pertaining standardized mortality ratios (SMRs) were calculated.

Results: 18 510 persons in the study cohort died in the follow-up period 1960–2013. Mortality from lung cancer was 2.36 higher in the study cohort than in the general population (95% confidence interval, [2.28; 2.45]); the associated SMRs rose markedly with increasing radon exposure. Mortality from silicosis and other types of pneumoconiosis was elevated by a factor of 22.62 [21.20; 24.11], and the associated SMRs rose exponentially with increasing exposure to respirable crystalline silica. Mortality from both of these causes was still markedly elevated more than 20 years after Wismut AG had ceased its activities. Mortality from a wide range of other diseases was elevated as well, with the following SMRs: stomach cancer, 1.28 [1.17; 1.40]; liver cancer, 1.34 [1.15; 1.55]; all tumors other than lung cancer, 1.06 [1.02; 1.09]; infections, 1.18 [1.01; 1.38]; cerebrovascular diseases, 1.33 [1.26; 1.41]; and influenza/pneumonia, 1.13 [1.01; 1.27]. Mortality from a small number of other causes was found to be markedly lowered in the study cohort (mental illness, renal diseases, and nervous system diseases). The role of occupational risk factors, lifestyle differences and other reasons for the latter results is unclear.

Conclusion: Underground miners employed by Wismut AG displayed marked excess mortality due to silicosis/other pneumoconiosis and lung cancer. The contribution of individual occupational risk factors for these and other causes of death with increased SMR are being further investigated in analyses within the study cohort.

LNSLNS

More than 400 000 persons worked in the uranium mine in Saxony and Thuringia between 1946 and 1990. As employees of the Soviet, later Soviet-German incorporated company (SAG/SDAG) Wismut, they mined more than 230 000 tons of uranium ore (1) which was used to build Soviet nuclear weapons. The employees of Wismut were exposed to a variety of occupational risk factors, primarily the inhalation of radon and its progeny as well as silica dust (respirable crystalline silica), but also to uranium dust, arsenic and diesel exhaust. In addition, there was exposure to external gamma radiation, heat, vibration, and noise. Since in the early years, hardly any radiation protection and occupational health and safety measures were in place, the level of exposure to radon and silica dust was very high. In 1955, working conditions started to improve significantly and reached the level of international radiation protection standards by about 1971.

The German Federal Office for Radiation Protection (BfS, Bundesamt für Strahlenschutz) started to establish the German uranium miners cohort in the 1990s. The cohort includes 58 974 men who worked at Wismut AG in Saxony and Thuringia for at least six months between 1946 and 1989 (2, 3). The aim of this long-term study is to assess the health consequences of occupational radiation and dust exposure. These insights are critical for radiation protection and occupational health and safety measures as well as the recognition procedures for occupational diseases.

Radon is a well-established lung carcinogen (4, 5). For other diseases, a low radon-related risk, if any, can be assumed, because the expected organ doses outside of the respiratory tract are very low (4). Silica dust exposure is known to cause silicosis, but also lung cancer, pulmonary tuberculosis and pneumonia. Furthermore, there is evidence of an association with kidney disease and autoimmune disease, stomach cancer and cardiovascular disease (6, 7).

The aim of our analyses is to compare the mortality in der Wismut cohort with the mortality in the male Eastern German general population during the follow-up period from 1960 to 2013. Since the exposure to radon and silica dust was significantly higher underground compared to surface, open pit mining or processing/milling, this analysis is limited to a sub-cohort of underground miners, referred to below as “underground cohort“.

Methods

The cohort and the procedures for mortality follow-ups and exposure estimation have been described in detail in earlier publications (2, 3). For each cohort member, a file-based mortality follow-up is performed using information from local registration offices, local health authorities and the former pathology archive of Wismut AG. The vital status was determined and in deceased persons the underlying cause of death was identified based on copies of death certificates or autopsy findings. The cut-off day for the last completed follow-up was 31 December 2013. The underground cohort comprised 35 204 male persons who had worked underground for at least six months and had at no time worked in open pit mining or processing/milling. The analyses refer to the follow-up period from 1960 to 2013, since external mortality rates are only available from 1960 onwards. Thus, persons who died or were lost to follow-up before 1960 were not included in the analyses.

Using a job-exposure matrix (JEM), the exposure to radon progeny was estimated for each person. The detailed JEM was developed by the Miners’ Occupational Compensation Board (BBG, Bergbau-Berufsgenossenschaft) in Gera and the Main Association of Commercial Occupational Compensation Boards (HVBG, Hauptverband der gewerblichen Berufsgenossenschaften) at that time (8, 9). The JEM is based on available ambient air measurement data from 1955 onwards. For the time periods before 1955, it is based on detailed experts’ estimates. The Institute for Hazardous Substances Research (IGF, Institut für Gefahrstoff-Forschung) in Bochum developed a JEM for silica dust, fine dust and arsenic (9, 10). For each member of the cohort, data on the cumulative exposure to radon and its progeny in working level months (WLM) and to silica dust in mg/m3-years are available.

Commonly applied statistical methods were used to compare the mortality in the Wismut cohort with the mortality in the general population (11). The standardized mortality ratio (SMR) was calculated as the ratio of observed deaths (O) divided by expected deaths (E) in the study. The expected deaths are the deaths which one would expect in the Wismut cohort on the basis of the mortality in the general population. These were calculated by applying the calendar year- and age-specific (5-year intervals) mortality rates of the male Eastern German general population to the calendar year-specific age distribution of the cohort. The latter is derived from the sum of the periods under risk for persons in the respective age category (person-years under risk). The ICD-10 coding of causes of death in the cohort was performed by trained coders of State Statistical Offices based on the plain texts of the medical death certificates. The existing external rates in ICD-6, ICD-8 and ICD-9 were converted to ICD-10 and missing external rates were linearly interpolated using the available rates of the years that preceded and followed (eTable 1). SMRs for person groups with different levels of exposure were assessed using the Poisson trend statistic.

Description of the cohort of underground miners of Wismut AG in the followup period from 1960 to 2013
Table 1
Description of the cohort of underground miners of Wismut AG in the followup period from 1960 to 2013
ICD-6, 8, 9, 10 cause-of-death coding and calendar years with imputed external mortality rates
eTable 1
ICD-6, 8, 9, 10 cause-of-death coding and calendar years with imputed external mortality rates

SMRs were calculated for cancer- and non-cancer causes of death in the entire underground cohort and also separately for persons who started to work at Wismut before and after 1960. Those whose employment started before 1960 were exposed to extremely high mean levels of exposure to radon and dust. By contrast, for the latter the exposure was comparable to today’s workplace conditions. For selected causes of death (p-value for SMR ≤ 5%), SMRs were additionally calculated by calendar year and—as far as an association is discussed in the literature—by cumulative occupational exposure to radon and silica dust.

Results

The cohort of the former underground miners comprised 35 204 men with altogether 1 269 326 person-years under risk during the follow-up period from 1960 to 2013 (Table 1). About half of the cohort died during the follow-up period; among those with begin of employment between 1946 and 1959 this figure was as high as 81%. The cause of death used for this analysis was established by autopsy in 25% of the deceased; among those who died before 1990 more than 50% of the cause-of-death information was autopsy-based.

The mean cumulative exposure to radon and silica dust was 364 WLM and 7.6 mg/m3-years, respectively. For radon, a 29-fold increase in these values was noted in the group with begin of employment between 1946 and 1959, while for silica dust a 14-fold increase was observed in the group with begin of employment after 1960. For comparison: The natural residential exposure to radon of 100 Bq/m3 over a period of 30 years amounts to about 12 WLM. The mean annual levels of exposure to radon and silica dust started to significantly decline in the cohort with the introduction of mine ventilation and wet drilling in 1955 and reached values basically in line with international radiation protection standards in the 1970s (eFigure).

Timeline of the mean annual cumulative silica dust exposure in mg/m3-years and of the mean cumulative radon exposure in working level months (WLM) for the underground cohort of Wismut employees
eFigure
Timeline of the mean annual cumulative silica dust exposure in mg/m3-years and of the mean cumulative radon exposure in working level months (WLM) for the underground cohort of Wismut employees

Table 2 shows the SMRs for selected cancers as causes of death. Altogether, there were 6 113 cancer deaths, almost half of which could be attributed to lung cancer. Lung cancer mortality was 2.36 times higher than in the general population. In addition, there was a notable excess in mortality from stomach cancer, liver cancer and for all cancer-related causes of death without lung cancer. This SMR pattern was also observed when the miners with early (1946–1959) and those with late (1960+) begin of employment were analyzed separately (Table 3). In the group with early begin of employment (1946–1959), overall cancer mortality was 50% (95% confidence interval: [46; 55]) higher than in the general population and in the group with begin of employment after 1960 it was found increased by 15% [8; 23]. In both groups, the increase in risk was primarily attributable to lung cancer.

Observed and expected cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013
Table 2
Observed and expected cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013
Observed and expected cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013 by begin of employment before and after 1960
Table 3
Observed and expected cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013 by begin of employment before and after 1960

Among the non-cancer causes of death (Table 4), a 1.86-fold increased risk of mortality related to non-malignant respiratory diseases was observed. This was largely attributable to silicosis/other pneumoconiosis and influenza/pneumonia, but not to chronic obstructive pulmonary disease (COPD). All in all, 941 cases with silicosis/other pneumoconiosis as underlying cause of death occurred during the follow-up period; almost all of these were persons with begin of employment before 1960 (Table 5). Mortality from infection and cerebrovascular disease was also increased. In contrast, mortality from mental disease (mainly dementia, alcohol-related behavioral disorders), diseases of the nervous system and the circulatory system overall as well as kidney disease was reduced. As shown in Table 5, overall mortality from non-cancer respiratory diseases was only increased among miners with begin of employment before 1960. Remarkable among miners with begin of employment after 1960 is the increase in mortality from infection as well as injury and poisoning.

Observed and expected non-cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013
Table 4
Observed and expected non-cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013
Observed and expected non-cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013 by begin of employment before and after 1960
Table 5
Observed and expected non-cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013 by begin of employment before and after 1960

Trend tests for selected causes of death with increased SMR by cumulative radon exposure are shown in eTable 2. For lung cancer, liver cancer and the overall group of all types of cancer except lung cancer, the SMR increased with radon exposure. There was no indication of a trend for stomach cancer. With regard to cumulative exposure to silica dust, a clear trend in the SMRs was only observed for silicosis/other pneumoconiosis (eTable 3), but for no other causes of death with overall increased SMRs; lung cancer as a cause of death was not included in this analysis.

SMRs for selected causes of death by cumulative radon exposure in working level months (WLM)
eTable 2
SMRs for selected causes of death by cumulative radon exposure in working level months (WLM)
SMRs for selected causes of death by cumulative silica dust exposure in mg/m³-years
eTable 3
SMRs for selected causes of death by cumulative silica dust exposure in mg/m³-years

Discussion

In the cohort of former underground miners of Wismut AG, lung cancer mortality and pneumoconiosis mortality were found considerably increased compared to the general population This increase in risk was significantly higher among miners employed already in the 1940s and 1950s, who were exposed to high levels of radon and dust, compared to miners in later years. But also other causes of death were found to be clearly increased compared to the general population, most notably stomach cancer, liver cancer, infections, influenza/pneumonia, and cerebrovascular disease. In contrast, mental disorders, kidney disease and diseases of the nervous system were considerably less common causes of death in the underground cohort.

As a general rule, when interpreting the results of external comparisons one should take into account that differences in mortality between an occupational group and the general population are not only caused by occupational risk factors but also by potential differences in social status, lifestyle factors, healthcare offerings, etc. In the early years, the employees of Wismut AG often received, besides cigarettes, alcohol in larger quantities (1). Thus, an increased consumption of alcohol and cigarettes is likely. Approximate data on smoking behavior are available for a third of the Wismut cohort and for the sample of a nested case-control study on lung cancer (12). These are indicative of a high prevalence of smoking. In further two case-control studies on lung cancer in Saxony and Thuringia, detailed information about smoking was collected, both in the general population (13) and among Wismut employees (14). The proportion of persons who never smoked was significantly lower among Wismut employees (15%) compared to the male general population (26%). Therefore, it can be assumed that the increased SMRs for causes of death related to smoking behavior are to some extent explained by this difference. The same might be true for alcohol consumption, but no alcohol-related data are available for the Wismut cohort.

Possible differences in social status between underground miners and the general population could be associated with a less healthy lifestyle and thus result in a trend towards higher SMRs for certain causes of death. Wismut AG, however, had its own healthcare system with regular occupational health examinations and this may have resulted in improved medical care for employees. Furthermore, it is likely that higher autopsy rates among Wismut employees have resulted in higher detection rates for certain causes of deaths.

Against this background, the risk increases observed in the cohort are discussed below. With 2960 observed cases compared to 1252 expected cases, the risk of lung cancer was considerably increased. Both radon (4) and silica dust (15, 16) are well-established lung carcinogens, especially among underground miners (5, 17, 18). Both risk factors show a strong correlation in the Wismut cohort (Pearson correlation: 0.84). Earlier risk analyses within the Wismut cohort which—unlike our analyses—used a model where both variables were considered simultaneously showed that radon was the dominant risk factor for lung cancer in the Wismut cohort (19, 20). For this reason, an SMR analysis for lung cancer in relation to silica dust exposure was not performed. Earlier internal analyses showed a linear increase in lung cancer risk with increasing cumulative radon exposure as well as modifying effects of age at and time since exposure and exposure rate (21, 22). From about 10 mg/m3-years, a significantly increased lung cancer risk related to silica dust was noted (20). Our external comparisons also revealed an SMR increase with increasing radon exposure. Furthermore, a decrease in SMR over time was observed; however, the SMR remained markedly elevated until the end of the follow-up period (eTable 4).

SMRs for selected causes of death with increased SMR by calendar year
eTable 4
SMRs for selected causes of death with increased SMR by calendar year

Mortality from cancer other than lung cancer was found increased by 6% in the Wismut AG underground cohort compared to the general population [2; 9]. Conspicuously, liver cancer mortality was considerably increased among Wismut employees. Increased alcohol consumption may be one possible explanation. However, this is inconsistent with the fact that mortality from liver cirrhosis was not increased. Elevated rates of liver cancer were observed in many other (23, 24, 25) but not all studies on uranium miners. Another conceivable explanation could be that liver metastasis of a primary lung tumor was misclassified as a primary liver tumor. This could explain the SMR increase associated with radon exposure.

The increased stomach cancer rate among underground miners of Wismut AG compared to the general population is remarkable and has already been noted in earlier follow-up assessments (26, 27). Evidence of increased rates of stomach cancer is available from other studies on radon-exposed miners (23, 25, 28), but also from studies on coal miners and other workplaces with high levels of dust exposure. A recently published meta-analysis found a 1.25-fold (95% confidence interval: [1.18; 1.34]) increased stomach cancer risk for persons with occupational silica dust exposure compared to non-exposed persons (29). As a mechanism, it was postulated that dust has a noxious effect on gastric mucosa after it has been inhaled, cleared by the lungs and then swallowed (30). Our SMR analyses found no association of stomach cancer with radon or silica dust exposure.

As expected, the large increase in mortality from pneumoconiosis among miners stood out among the non-cancer diseases. In the underground cohort, the underlying cause of death was silicosis in 739 persons and silicotuberculosis in 207 persons. Half of these causes of death were based on autopsy findings. Pneumoconiosis can occur years after the end of exposure to silica dust (6). This is the most likely reason for the still markedly increased mortality from pneumoconiosis among Wismut employees.

A considerably increased risk for infections of the respiratory tract (pneumonia, lung tuberculosis) was observed in several occupational cohorts with silica exposure (6, 28). This increase is also seen in employees of Wismut AG. However, mortality from COPD is not increased in the Wismut cohort, while this is the case in some of the other dust-exposed occupational cohorts (6, 7, 31). Here, however, silicosis could act as a concurrent cause of death. There are only a few reports in the literature indicating a potential association between cardiovascular disease and silica dust (7, 32, 33). In our analysis, mortality from circulatory disease was lower among the miners compared to the general population, but markedly increased for the subgroup of cerebrovascular disease. It remains unclear whether this increase was caused by misclassification of the cause of death, because only 16% of all documented causes of death of the circulatory disease group were based on autopsy findings.

The strengths of our analysis include the large size of the cohort, the long follow-up period and the availability of data on occupational exposure. Besides the lack of information about non-occupational risk factors, the weaknesses of this study include the absence of incidence data and a lack of validity of causes of death. Furthermore, there is a lack of information about approximately 4% of causes of death in the cohort overall, resulting in an underestimation of the SMRs. This applies in particular to employees who died between 1960 and1969; in this period, 25% of cause-of-death data are missing. Persons who died (n = 180) or left the company (n = 641) before 1960 were excluded from the analysis, potentially giving rise to the healthy worker survivor effect. Since no correction for multiple testing was applied, our results are exploratory in nature.

Conclusion

Its large size, long observation period and the availability of information about occupational radon and dust exposure make the Wismut cohort unique. For the first time, a comprehensive comparison of the mortality among former underground miners of Wismut AG and the general population was performed. It showed a highly increased mortality from silicosis and lung cancer which were still present more than 20 years after the closure of Wismut. Findings for other causes of death were also conspicuous. The effects of various occupational risk factors on mortality are currently being explored in more detailed risk analyses within the Wismut cohort as well in a worldwide joint analysis of studies among uranium miners (34, 35).

Acknowledgement
We would like to thank Mrs. Hochstrat and Dr. Güthlin of the Federal Office for Radiation Protection for their invaluable preparatory work. We also extend our thanks to Dr. Otten of the German Social Accident Insurance (DGUV, former Federation of Institutions for Statutory Accident Insurance and Prevention in Sankt Augustin) for his continuous support over many years, especially with the set-up of the study. Furthermore, we thank Dr. Lehmann of the Miners’ Occupational Compensation Board (Bergbau-Berufsgenossenschaft) in Gera (now the German Social Accident Insurance Institution for the Raw Materials and Chemical Industry, BG RCI) for his leading role in the creation of the Job-Exposure Matrix for Radiation as well as Dr. Dahmann of the Institute for Hazardous Substances Research in Bochum for the creation of the Job Exposure Matrix for Dust and Arsenic. Special thanks also go to the staff of the Central Support Center Wismut (ZeBWis, Zentrale Betreuungsstelle Wismut) for obtaining the data of the Wismut employees from the payroll records. Particular thanks go to the working group “Steering Committee on the German Uranium Mining Studies“ of the German Commission on Radiological Protection for their valuable scientific suggestions.

Conflict of interest
The authors declare no conflict of interest.

Manuscript received on 7 May 2020, revised version accepted on 13 July 2020

Translated from the original German by Ralf Thoene, MD.

Corresponding author
PD Dr. rer. hum. biol. Michaela Kreuzer
Bundesamt für Strahlenschutz
Abteilung Wirkungen und Risiken von ionisierender und
nichtionisierender Strahlung
Ingolstädter Landstr. 1, 85764 Neuherberg, Germany
mkreuzer@bfs.de

Cite this as:
Kreuzer M, Deffner V, Schnelzer M, Fenske N: Mortality in underground miners in a former uranium ore mine—results of a cohort study among former employees of Wismut AG in Saxony and Thuringia. Dtsch Arztebl Int 2021; 118: 41–8. DOI: 10.3238/arztebl.m2021.0001

Supplementary material

eTables, eFigure:www.aerzteblatt-international.de/21m0041

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Department of Effects and Risks of Ionizing and Non-Ionizing Radiation, Federal Office for Radiation Protection, Neuherberg, Germany: PD Dr. rer. hum. biol. Michaela Kreuzer, Dr. rer. nat. Veronika Deffner, Dr. phil. Maria Schnelzer, Dr. rer. nat. Nora Fenske
Description of the cohort of underground miners of Wismut AG in the followup period from 1960 to 2013
Table 1
Description of the cohort of underground miners of Wismut AG in the followup period from 1960 to 2013
Observed and expected cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013
Table 2
Observed and expected cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013
Observed and expected cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013 by begin of employment before and after 1960
Table 3
Observed and expected cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013 by begin of employment before and after 1960
Observed and expected non-cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013
Table 4
Observed and expected non-cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013
Observed and expected non-cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013 by begin of employment before and after 1960
Table 5
Observed and expected non-cancer deaths in the cohort of former underground miners of Wismut AG compared to the general population in Eastern Germany during the follow-up period from 1960 to 2013 by begin of employment before and after 1960
Timeline of the mean annual cumulative silica dust exposure in mg/m3-years and of the mean cumulative radon exposure in working level months (WLM) for the underground cohort of Wismut employees
eFigure
Timeline of the mean annual cumulative silica dust exposure in mg/m3-years and of the mean cumulative radon exposure in working level months (WLM) for the underground cohort of Wismut employees
ICD-6, 8, 9, 10 cause-of-death coding and calendar years with imputed external mortality rates
eTable 1
ICD-6, 8, 9, 10 cause-of-death coding and calendar years with imputed external mortality rates
SMRs for selected causes of death by cumulative radon exposure in working level months (WLM)
eTable 2
SMRs for selected causes of death by cumulative radon exposure in working level months (WLM)
SMRs for selected causes of death by cumulative silica dust exposure in mg/m³-years
eTable 3
SMRs for selected causes of death by cumulative silica dust exposure in mg/m³-years
SMRs for selected causes of death with increased SMR by calendar year
eTable 4
SMRs for selected causes of death with increased SMR by calendar year
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