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Investigation of exposures to commercial asbestos in northeastern Minnesota iron miners who developed mesothelioma
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Regulatory Toxicology and Pharmacology 52 (2008) S116–S120 www.elsevier.com/locate/yrtph
Investigation of exposures to commercial asbestos in northeastern Minnesota iron miners who developed mesothelioma Wendy M. Brunner *, Allan N. Williams, Alan P. Bender Chronic Disease and Environmental Epidemiology, Minnesota Department of Health, 85 East 7th Place, P.O. Box 64882, St. Paul, MN 55164-0882, USA Received 5 September 2007 Available online 5 October 2007
Abstract A 70% excess of mesothelioma, an asbestos-related cancer, has been reported among men in northeastern Minnesota, where iron mining has been the major industry. The Minnesota Department of Health has studied iron miners who developed mesothelioma to identify possible sources of asbestos exposure. A database of all Minnesota residents diagnosed with mesothelioma between 1988 and 1996 was linked to a database of approximately 72,000 current and former Minnesota iron-mining employees to identify cases who had ever worked in the mining industry. The job histories of the cases were examined to determine if any of their jobs could have involved exposure to commercial asbestos. Seventeen individuals diagnosed with mesothelioma in Minnesota between 1988 and 1996 were found to have worked in the iron mining industry. Of the 15 for whom adequate work histories were available, 14 had identifiable sources of exposure to commercial asbestos in jobs held both inside and outside of the mining industry. The time between employment in these asbestosexposed occupations and the diagnosis of mesothelioma is consistent with the 20 or more year latency period that has been observed in other studies of this cancer. Ó 2007 Elsevier Inc. All rights reserved. Keywords: Mesothelioma; Asbestos; Iron miners; Taconite; Epidemiology; Case series
1. Introduction There has long been concern about a possible link between the iron mining industry in northeastern Minnesota and the occurrence of cancers and respiratory diseases in that region. In 1973, amphibole fibers were found in the Duluth water supply and traced to tailings that had been disposed of in Lake Superior by the Reserve Mining Company. This finding prompted studies of the fibers (Langer et al., 1979), the effects of ingestion of the fibers (Hilding et al., 1981; Levy et al., 1976), and the morbidity and mortality of iron ore workers (Clark et al., 1980; Cooper et al., 1988, 1992; Higgins et al., 1983; Lawler et al., 1985), among other studies. *
Corresponding author. Fax: +1 651 201 5898. E-mail address: [email protected] (W.M. Brunner).
0273-2300/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.yrtph.2007.09.014
In 1997, the Minnesota Cancer Surveillance System (MCSS) reported that the rate of mesothelioma, a rare asbestos-related cancer, was 70% higher than the statewide average among men in northeastern Minnesota during the period 1988–1994 (standardized morbidity ratio = 1.72; 95% confidence interval = 1.22–2.35) (Breslow and Day, 1987; Minnesota Cancer Surveillance System, 1997). Subsequent data from MCSS showed a continuing excess in men in this region—at 81% for the 12-year period 1988– 1999 (Minnesota Cancer Surveillance System, 2003). No excess has been found among females. Mesothelioma is a cancer of the lining of the lung or abdomen. A past history of exposure to asbestos can be identified among most victims of this disease. Mesothelioma has not been associated with smoking. There are approximately 60 cases of mesothelioma per year in Minnesota. Due to a latency period of 20 or more years, it is
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often difficult to determine exactly when or where an individual diagnosed with mesothelioma may have been exposed to asbestos. Mesothelioma is rapidly fatal; consequently, it is often not possible to obtain direct interviews with the subjects themselves. In addition, historical monitoring data are often not available. For this reason, many studies use past work histories and job titles as a surrogate for potential exposures. It was not clear what sources of asbestos led to the elevated rate of this cancer among men in northeastern Minnesota. Exposures related to cancers that were diagnosed in the 1980s and early 1990s would have had to have taken place in the 1940s to the 1970s, or earlier. While an increased rate was observed in men, the rate in women was not elevated, pointing to the likelihood of an occupational exposure. It was known that between 1958 and 1974, the Conwed Corporation plant in Cloquet, Minnesota, also located in the northeast region of the state, used several types of asbestos as a raw material in the manufacturing of mineral board and ceiling tile (Bender et al., 1993; Williams, 1994). However, preliminary evidence indicated that it was unlikely that Conwed was the sole explanation for the elevated rate of mesothelioma (Minnesota Cancer Surveillance System, 1999). Because the iron mining industry has been a major employer in this region and because of the history of concern about the mineral fibers, concern remained that there may be some mining process that resulted in asbestos exposure. In 1998, the Minnesota Department of Health (MDH) began a series of investigations to determine to what extent, if any, employment in the iron mining industry was associated with the excess of mesothelioma or other occupational respiratory diseases. To investigate the mesothelioma excess, record linkage was conducted to identify cases of mesothelioma that may have occurred among former iron miners. A case series study was then conducted to determine the extent to which mesothelioma in miners could be explained by exposures to commercial asbestos (commercially-available asbestos and asbestos-containing materials, such as insulation). Such exposures—known to be associated with mesothelioma risk in many other industries—would need to be identified and accounted for in assessing health risks to miners. If no commercial asbestos exposures could be identified, other exposures (e.g., taconite fibers) would have to be evaluated. 2. Methods 2.1. Minnesota Iron Miner cohort The Minnesota Iron Miner cohort was assembled by the University of Minnesota, School of Public Health in the early 1980s, with the support of the Minnesota Iron Range Resources and Rehabilitation Board and the cooperation of the seven mining companies then in operation. The cohort consists of approximately 72,000 individuals who had worked in the iron mining industry in northeastern Minnesota between the 1930s and the early 1980s, including taconite workers and persons who had worked in
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certain natural ore operations. (Reserves of natural ore were largely depleted by the 1970s. Taconite, a lower-grade iron ore, has been mined commercially in Minnesota since 1955.) In addition to demographic information, the cohort records contain the employment histories of these workers.
2.2. Identification of Minnesota iron miners who developed mesothelioma MCSS records for all Minnesota residents diagnosed with mesothelioma between 1988 and 1996 (years of data available when the study began) were linked to the Minnesota Iron Miner cohort database, to identify cases who had ever been employed in the mining industry. Because former iron miners could have moved out of the seven counties of northeastern Minnesota, the iron miner database was linked to MCSS records for all Minnesota residents. The records were matched on first, middle and last name, date of birth, and social security number. The computerized matches were performed using a probabilistic record linkage program (Fellegi and Sunter, 1969).
2.3. Identification of mining and non-mining jobs held by miners who developed mesothelioma Mining jobs held by workers who developed mesothelioma were identified using records from the Minnesota Iron Miner cohort. Non-mining jobs were identified using employment applications included in the iron miner records, workers compensation claim records, and newspaper death notices.
2.4. Identification of possible exposures in mining occupations The first step in the qualitative assessment of possible exposures to commercial asbestos in the mining jobs involved interviewing people who had worked in these jobs. An advisory committee to MDH provided technical assistance in the development of a questionnaire that was used to ask workers about potential exposures to commercial asbestos in different mining jobs. Questions asked about materials handled and tasks that may have involved direct or indirect exposures to asbestos (Fletcher et al., 1993), referring to the work environment as it existed in the 1940s–1970s. This study did not include any assessments of exposure to taconite dust. A list of job titles for each of the mining companies was developed consisting of jobs held by workers from that company, if any, who had been diagnosed with mesothelioma, plus other randomly-chosen jobs. The extra jobs were added so that the interviewees and those assessing the jobs could not assume that the job they were reporting on, or evaluating, had been held by a worker who developed mesothelioma. More than 350 telephone interviews were conducted covering 122 different job titles from the seven different mining companies (two of which were no longer in operation at the time of the study). Ninety-six percent of the respondents had experience in the job they reported on, while the remaining 4% were coworkers and/or supervisors. An attempt was made to interview at least three persons per job title. The interviews were summarized by MDH’s consulting certified industrial hygienist (CIH) who examined the interview responses and used them to assign an initial rating of exposure to commercial asbestos for each job. An assessment panel for each company was convened to make the final exposure determinations. Each panel consisted of knowledgeable union and management representatives, plus a non-mining industrial hygienist or safety engineer. The panels used the initial ratings, the interview responses (with identifying information removed), available job descriptions from the relevant time period, and their own knowledge of the mining environment to estimate the potential for exposure to commercial asbestos in each of the jobs. The panels considered regular (everyday) and shutdown responsibilities separately. (Shutdowns are scheduled periods when regular processing at a mining operation stops so that equipment can be retooled or maintained. Workers may change jobs or even move to a different facility to perform shutdown duties.) The panels rated
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the jobs as exposed (in terms of high likelihood/high intensity; high likelihood/low intensity; low likelihood/high intensity or low likelihood/low intensity), not exposed, or unknown exposure. When no interviews were available (i.e., no interviewees could be found), the panels made determinations using other information (e.g., job descriptions and their own knowledge). If no determination could be made, the potential for exposure was marked unknown.
Table 1 Summary of estimated exposures to commercial asbestos 20 or more years prior to diagnosis for 17 iron-mining employees who developed mesothelioma Likelihood of exposure to commercial asbestos
Total No.
Exposure in nonmining occupation(s)
Exposure in mining occupation(s)
Exposure in both mining and non-mining occupations
Probable Possible None identified Unknown due to incomplete job histories
11 3 1 2
3a 1 — —
4 0 — —
4 2 — —
2.5. Identification of possible exposures in non-mining occupations Other studies of asbestos-exposed occupations were reviewed to determine whether a particular non-mining job could have involved exposure to commercial asbestos. In addition, the list of miners with mesothelioma was checked against a roster of former Conwed employees (Minnesota Department of Health, 1989), to see how many had also worked at that facility. Any Conwed job was considered as having potential commercial asbestos exposure. A final review of these jobs was provided by the CIH.
a Includes two individuals who also had non-mining occupations with possible exposure.
3. Results 3.1. Description of the case series Of the 340 male Minnesota residents diagnosed with mesothelioma between 1988 and 1996, 17 were found to have worked in the iron mining industry. Two of the 17 also worked at Conwed. None of the 92 female Minnesotans diagnosed with mesothelioma between 1988 and 1996 were found in the iron miner cohort. Fifteen of the 17 were diagnosed with pleural mesothelioma while two had peritoneal mesothelioma. The age at diagnosis ranged from 55 to 82. Fourteen were diagnosed while residing in northeastern Minnesota while three were diagnosed while living elsewhere in Minnesota. Since MCSS only collects cancer data for Minnesota residents, it is not known how many, if any, miners may have developed mesothelioma outside of Minnesota. 3.2. Occupational histories The number of different iron mining jobs held by each of the 17 men varied, as did the length of their employment in the mining industry, ranging from 2 months to 40 years. With the addition of known non-mining jobs, the extent of the employment history documented for the 17 men ranged from 5 to 60 years. The years of their employment ranged from the 1930s through the 1980s. Complete job histories for the relevant exposure period were available for 10 of the 17 cases. For five cases, there were small gaps in job history information. Thus, for 15 cases, occupational histories were sufficiently complete to allow evaluation of potential exposures to commercial asbestos. A listing of occupations held by the cases is included in the MDH report (Minnesota Department of Health, 2003). 3.3. Exposures to commercial asbestos Table 1 contains a summary of the panel exposure estimates for the 17 cases in terms of ‘‘probable’’ and ‘‘possible’’ likelihood of exposure. Probable was used when the
panel exposure estimate was: high likelihood/high intensity; high likelihood/low intensity or low likelihood/high intensity. Possible was used when panel exposure estimate was low likelihood/low intensity. Fourteen of the 15 miners who developed mesothelioma had potential exposures to commercial asbestos: 11 had job(s) with probable exposure to commercial asbestos and another 3 had job(s) with possible exposure to commercial asbestos. One of the 15 had no apparent occupational exposures to commercial asbestos based on the information that was available. For two of the 17, a potential source of exposure could not be determined because the jobs they held for significant portions of their job histories were unknown. Potential exposures to commercial asbestos were found in both mining and non-mining occupations. Many of the asbestos-exposed occupations held by the cases, like plumbing, were common to both mining and non-mining industries. Examples of mining jobs identified as having potential exposures to commercial asbestos were carpenter, maintenance mechanic and plumber. Non-mining jobs having potential exposures included boiler operator, sheet metal worker and Conwed (Cloquet, Minnesota) worker. The exposure determinations for the mining jobs are company-specific. That is, the panels rated the jobs as they existed at certain companies in the time period of interest, so exposure ratings may not be true for the same job title at a different operation. The time between employment in these asbestos-exposed occupations and the diagnosis of mesothelioma in this study was consistent with the 20 or more year latency period that has been observed in other studies of this cancer. Of the 14 cases who held occupations in which exposure was possible or probable, mining occupations were the only identified source for 4; non-mining occupations were the only identified source for 4; and both mining and non-mining occupations were identified for 6. As noted in Table 1, 2 cases who had a non-mining job with probable exposure and a mining job with possible exposure were categorized as ‘‘probable/non-mining’’.
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4. Discussion This study identified 17 Minnesota iron miners who were diagnosed with mesothelioma between 1988 and 1996. While the mesothelioma risk among miners cannot be quantified in this study and is not solely attributable to exposures within the mining workplace, this finding is in sharp contrast to previously published death certificate-based studies of Minnesota iron ore miners that have not found mesotheliomas or excesses of other respiratory diseases (Cooper et al., 1988, 1992; Higgins et al., 1983; Lawler et al., 1985). This finding, along with the results of the exposure assessment, demonstrates that exposure to asbestos has occurred in the iron mining industry during previous decades. Because of the long latency of asbestosrelated diseases, these risks will continue into the future even in the absence of ongoing exposures. 4.1. Limitations and strengths Case series studies, such as this study, must be cautiously interpreted. While exposures among the cases are categorized and explicitly described, there is no control group for comparison, and thus exposures among non-cases can only be implicitly assumed based on historical data or other knowledge. However, where there is a very strong relationship between exposure and disease, useful insights may be obtained even in the absence of controls (Cummings and Weiss, 1998). As with analytic studies, other sources of bias should still be addressed. The major limitation of this study was the assessment of previous commercial asbestos exposure. This assessment was based on job titles and occupational histories—not actual monitoring data—and utilized existing records. Due to statutory limitations, study protocols did not allow contact of next of kin to gain more information about the work histories and potential exposures of the 17 individuals diagnosed with mesothelioma who worked in the mining industry. Complete work histories were not found for 2 of the 17. For one, documentation only up to age 26 was available. Complete information may or may not have been found regarding an individual’s work outside of the mining industry. This depended on whether the prior work history was included in their employment records, or was available through other sources (e.g., death notices). In addition, nothing was known about any non-occupational asbestos exposures (e.g., hobbies, home environment, spouse’s occupational exposures). Quantitative exposure data on which to base the assignment of asbestos exposure were not available. Even with qualitative exposure estimates, assumptions were made that a particular job title in a particular year at a particular mine conferred a particular probability of exposure. In addition, nothing was known about possible use of personal protective equipment.
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Despite these limitations, this study has several strengths. First, a major strength is this study’s use of cancer registry data, rather than death certificates, to identify all mesothelioma cases in the state. MCSS data come from the pathology reports and clinical records confirming that a cancer has been diagnosed. Quality control studies confirm the completeness and accuracy of these data. In contrast, death certificate-based studies (prior to the change from the International Classification of Disease revision 9 to revision 10 in 1999) will likely miss many, if not most, cases of mesothelioma that are often coded to other causes of death (such as lung cancer) (Lilienfeld and Gunderson, 1986). Among the 17 cases of mesothelioma in this study, only one would have been detected by the cause-of-death codes used for mesothelioma on death certificates (despite the fact that most of the death certificates had some mention of mesothelioma on the death certificate itself). A second strength is the study’s use of the previously established Minnesota Iron Miner cohort. Because those diagnosed with mesothelioma or their next of kin could not be contacted for this study, it would have been much more difficult and much less accurate to determine whether persons diagnosed with mesothelioma had ever worked in the mining industry without the mining cohort information. Mining cohort data also provided most of the information about the job titles and dates of employment for the study subjects. A third strength was the protocol that blinded the assessment of potential exposures to commercial asbestos. None of the participants in the study knew which job titles were associated with miners who later developed mesothelioma. Finally, the involvement of a technical advisory group provided information that was vital to the satisfactory completion of this study. The collaboration between labor and industry in the development of the protocol for this study allowed current and former iron miners to be interviewed about exposures to commercial asbestos in their jobs, in a way that ensured the confidentiality of their responses. In addition, the use of assessment panels consisting of mining company, labor and other industrial hygiene/safety professionals brought the most knowledgeable people together to make the best assessments with the available information. 4.2. Health issues not addressed by this study While the study findings establish that miners are at some risk of mesothelioma and that past exposure to commercial asbestos is a likely explanation, this study does not address other significant health questions. In particular, this study does not address the morbidity and mortality among iron miners from all types of cancer or respiratory diseases, nor does it attempt to address potential health risks from exposures to respirable mineral dusts from taconite ore and its processing (silica, taconite, cummingtonite-grunerite, cleavage fragments, etc.). Other types of epidemiologic studies, such as a mortality follow-up study
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(in which death rates and causes of death among miners would be compared to that for the overall population) or a medical screening of iron miners (which could look at lung abnormalities), would be required to address these questions. 5. Conclusion Our findings demonstrate an unquantified risk of mesothelioma among former Minnesota iron miners and suggest that commercial asbestos exposure (inside and outside of the mining industry) is the likely cause of mesothelioma in this case series. However, at least one miner had no identifiable source of exposure to commercial asbestos and other causes cannot be ruled out. Conflict of Interest The authors declare that they have no conflicts of interest. Funding Source Funded by the state of Minnesota. References Bender, A.P., Williams, A.N., Parker, D.L., 1993. Experiences of a statesponsored notification and screening program for asbestos workers. Am. J. Ind. Med. 23, 161–169. Breslow, N.E., Day, N.E., 1987. Statistical methods in cancer research. Volume II—the design and analysis of cohort studies. IARC Sci. Publ. 82, 1–406. Clark, T.C., Harrington, V.A., Asta, J., Morgan, W.K., Sargent, E.N., 1980. Respiratory effects of exposure to dust in taconite mining and processing. Am. Rev. Respir. Dis. 121, 959–966. Cooper, W.C., Wong, O., Graebner, R., 1988. Mortality of workers in two Minnesota taconite mining and milling operations. J. Occup. Med. 30, 506–511. Cooper, W.C., Wong, O., Trent, L.S., Harris, F., 1992. An updated study of taconite miners and millers exposed to silica and non-asbestiform amphiboles. J. Occup. Med. 34, 1173–1180.
Cummings, P., Weiss, N., 1998. Case series and exposure series: the role of studies without controls in providing information about the etiology of injury or disease. Inj. Prev. 4, 54–57. Fellegi, I., Sunter, A., 1969. A theory for record linkage. J. Am. Stat. Assoc. 25, 172–178. Fletcher, A., Engholm, G., Englund, A., 1993. The risk of lung cancer from asbestos among Swedish construction workers: self-reported exposure and a job exposure matrix compared. Int. J. Epidemiol. 22 (Suppl. 2), S29–S35. Higgins, I.T., Glassman, J.H., Oh, M.S., Cornell, R.G., 1983. Mortality of Reserve Mining Company employees in relation to taconite dust exposure. Am. J. Epidemiol. 118, 710–719. Hilding, A.C., Hilding, D.A., Larson, D.M., Aufderheide, A.C., 1981. Biological effects of ingested amosite asbestos, taconite tailings, diatomaceous earth and Lake Superior water in rats. Arch. Environ. Health 36, 298–303. Langer, A.M., Maggiore, C.M., Nicholson, W.J., Rohl, A.N., Rubin, I.B., Selikoff, I.J., 1979. The contamination of Lake Superior with amphibole gangue minerals. Ann. NY Acad. Sci. 330, 549–572. Lawler, A.B., Mandel, J.S., Schuman, L.M., Lubin, J.H., 1985. A retrospective cohort mortality study of iron ore (hematite) miners in Minnesota. J. Occup. Med. 27, 507–517. Levy, B.S., Sigurdson, E., Mandel, J., Laudon, E., Pearson, J., 1976. Investigating possible effects of asbestos in city water: surveillance of gastrointestinal cancer incidence in Duluth, Minnesota. Am. J. Epidemiol. 103, 362–368. Lilienfeld, D.E., Gunderson, P.D., 1986. The ‘‘missing cases’’ of pleural malignant mesothelioma in Minnesota, 1979–81: preliminary report. Public Health Rep. 101, 395–399. Minnesota Cancer Surveillance System, 1997. Cancer rates and trends in Northeastern Minnesota. MCSS Epidemiology Report 97:1. Minnesota Cancer Surveillance System, 1999. Cancer incidence rates in Northeastern Minnesota. MCSS Epidemiology Report 99:2. Minnesota Cancer Surveillance System, 2003. Cancer incidence rates in Northeastern Minnesota with an emphasis on mesothelioma, MCSS Epidemiology Report 03:1. Minnesota Department of Health, 1989. Medical screening for asbestos-related lung disease among Conwed Corporation (Cloquet) workers and their spouses: preliminary report to the Minnesota Legislature. Minnesota Department of Health, 2003. Exposures to commercial asbestos in Northeastern Minnesota iron miners who developed mesothelioma. Minneapolis; November 7, 2003. Available online: http://www.health.state.mn.us/divs/hpcd/cdee/occhealth/reports.html. Williams, A.N., 1994. An epidemiologic study of radiographic abnormalities among asbestos ceiling tile workers and their spouses. University of Minnesota, Minneapolis.
Regulatory Toxicology and Pharmacology 52 (2008) S116–S120 www.elsevier.com/locate/yrtph
Investigation of exposures to commercial asbestos in northeastern Minnesota iron miners who developed mesothelioma Wendy M. Brunner *, Allan N. Williams, Alan P. Bender Chronic Disease and Environmental Epidemiology, Minnesota Department of Health, 85 East 7th Place, P.O. Box 64882, St. Paul, MN 55164-0882, USA Received 5 September 2007 Available online 5 October 2007
Abstract A 70% excess of mesothelioma, an asbestos-related cancer, has been reported among men in northeastern Minnesota, where iron mining has been the major industry. The Minnesota Department of Health has studied iron miners who developed mesothelioma to identify possible sources of asbestos exposure. A database of all Minnesota residents diagnosed with mesothelioma between 1988 and 1996 was linked to a database of approximately 72,000 current and former Minnesota iron-mining employees to identify cases who had ever worked in the mining industry. The job histories of the cases were examined to determine if any of their jobs could have involved exposure to commercial asbestos. Seventeen individuals diagnosed with mesothelioma in Minnesota between 1988 and 1996 were found to have worked in the iron mining industry. Of the 15 for whom adequate work histories were available, 14 had identifiable sources of exposure to commercial asbestos in jobs held both inside and outside of the mining industry. The time between employment in these asbestosexposed occupations and the diagnosis of mesothelioma is consistent with the 20 or more year latency period that has been observed in other studies of this cancer. Ó 2007 Elsevier Inc. All rights reserved. Keywords: Mesothelioma; Asbestos; Iron miners; Taconite; Epidemiology; Case series
1. Introduction There has long been concern about a possible link between the iron mining industry in northeastern Minnesota and the occurrence of cancers and respiratory diseases in that region. In 1973, amphibole fibers were found in the Duluth water supply and traced to tailings that had been disposed of in Lake Superior by the Reserve Mining Company. This finding prompted studies of the fibers (Langer et al., 1979), the effects of ingestion of the fibers (Hilding et al., 1981; Levy et al., 1976), and the morbidity and mortality of iron ore workers (Clark et al., 1980; Cooper et al., 1988, 1992; Higgins et al., 1983; Lawler et al., 1985), among other studies. *
Corresponding author. Fax: +1 651 201 5898. E-mail address: [email protected] (W.M. Brunner).
0273-2300/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.yrtph.2007.09.014
In 1997, the Minnesota Cancer Surveillance System (MCSS) reported that the rate of mesothelioma, a rare asbestos-related cancer, was 70% higher than the statewide average among men in northeastern Minnesota during the period 1988–1994 (standardized morbidity ratio = 1.72; 95% confidence interval = 1.22–2.35) (Breslow and Day, 1987; Minnesota Cancer Surveillance System, 1997). Subsequent data from MCSS showed a continuing excess in men in this region—at 81% for the 12-year period 1988– 1999 (Minnesota Cancer Surveillance System, 2003). No excess has been found among females. Mesothelioma is a cancer of the lining of the lung or abdomen. A past history of exposure to asbestos can be identified among most victims of this disease. Mesothelioma has not been associated with smoking. There are approximately 60 cases of mesothelioma per year in Minnesota. Due to a latency period of 20 or more years, it is
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often difficult to determine exactly when or where an individual diagnosed with mesothelioma may have been exposed to asbestos. Mesothelioma is rapidly fatal; consequently, it is often not possible to obtain direct interviews with the subjects themselves. In addition, historical monitoring data are often not available. For this reason, many studies use past work histories and job titles as a surrogate for potential exposures. It was not clear what sources of asbestos led to the elevated rate of this cancer among men in northeastern Minnesota. Exposures related to cancers that were diagnosed in the 1980s and early 1990s would have had to have taken place in the 1940s to the 1970s, or earlier. While an increased rate was observed in men, the rate in women was not elevated, pointing to the likelihood of an occupational exposure. It was known that between 1958 and 1974, the Conwed Corporation plant in Cloquet, Minnesota, also located in the northeast region of the state, used several types of asbestos as a raw material in the manufacturing of mineral board and ceiling tile (Bender et al., 1993; Williams, 1994). However, preliminary evidence indicated that it was unlikely that Conwed was the sole explanation for the elevated rate of mesothelioma (Minnesota Cancer Surveillance System, 1999). Because the iron mining industry has been a major employer in this region and because of the history of concern about the mineral fibers, concern remained that there may be some mining process that resulted in asbestos exposure. In 1998, the Minnesota Department of Health (MDH) began a series of investigations to determine to what extent, if any, employment in the iron mining industry was associated with the excess of mesothelioma or other occupational respiratory diseases. To investigate the mesothelioma excess, record linkage was conducted to identify cases of mesothelioma that may have occurred among former iron miners. A case series study was then conducted to determine the extent to which mesothelioma in miners could be explained by exposures to commercial asbestos (commercially-available asbestos and asbestos-containing materials, such as insulation). Such exposures—known to be associated with mesothelioma risk in many other industries—would need to be identified and accounted for in assessing health risks to miners. If no commercial asbestos exposures could be identified, other exposures (e.g., taconite fibers) would have to be evaluated. 2. Methods 2.1. Minnesota Iron Miner cohort The Minnesota Iron Miner cohort was assembled by the University of Minnesota, School of Public Health in the early 1980s, with the support of the Minnesota Iron Range Resources and Rehabilitation Board and the cooperation of the seven mining companies then in operation. The cohort consists of approximately 72,000 individuals who had worked in the iron mining industry in northeastern Minnesota between the 1930s and the early 1980s, including taconite workers and persons who had worked in
S117
certain natural ore operations. (Reserves of natural ore were largely depleted by the 1970s. Taconite, a lower-grade iron ore, has been mined commercially in Minnesota since 1955.) In addition to demographic information, the cohort records contain the employment histories of these workers.
2.2. Identification of Minnesota iron miners who developed mesothelioma MCSS records for all Minnesota residents diagnosed with mesothelioma between 1988 and 1996 (years of data available when the study began) were linked to the Minnesota Iron Miner cohort database, to identify cases who had ever been employed in the mining industry. Because former iron miners could have moved out of the seven counties of northeastern Minnesota, the iron miner database was linked to MCSS records for all Minnesota residents. The records were matched on first, middle and last name, date of birth, and social security number. The computerized matches were performed using a probabilistic record linkage program (Fellegi and Sunter, 1969).
2.3. Identification of mining and non-mining jobs held by miners who developed mesothelioma Mining jobs held by workers who developed mesothelioma were identified using records from the Minnesota Iron Miner cohort. Non-mining jobs were identified using employment applications included in the iron miner records, workers compensation claim records, and newspaper death notices.
2.4. Identification of possible exposures in mining occupations The first step in the qualitative assessment of possible exposures to commercial asbestos in the mining jobs involved interviewing people who had worked in these jobs. An advisory committee to MDH provided technical assistance in the development of a questionnaire that was used to ask workers about potential exposures to commercial asbestos in different mining jobs. Questions asked about materials handled and tasks that may have involved direct or indirect exposures to asbestos (Fletcher et al., 1993), referring to the work environment as it existed in the 1940s–1970s. This study did not include any assessments of exposure to taconite dust. A list of job titles for each of the mining companies was developed consisting of jobs held by workers from that company, if any, who had been diagnosed with mesothelioma, plus other randomly-chosen jobs. The extra jobs were added so that the interviewees and those assessing the jobs could not assume that the job they were reporting on, or evaluating, had been held by a worker who developed mesothelioma. More than 350 telephone interviews were conducted covering 122 different job titles from the seven different mining companies (two of which were no longer in operation at the time of the study). Ninety-six percent of the respondents had experience in the job they reported on, while the remaining 4% were coworkers and/or supervisors. An attempt was made to interview at least three persons per job title. The interviews were summarized by MDH’s consulting certified industrial hygienist (CIH) who examined the interview responses and used them to assign an initial rating of exposure to commercial asbestos for each job. An assessment panel for each company was convened to make the final exposure determinations. Each panel consisted of knowledgeable union and management representatives, plus a non-mining industrial hygienist or safety engineer. The panels used the initial ratings, the interview responses (with identifying information removed), available job descriptions from the relevant time period, and their own knowledge of the mining environment to estimate the potential for exposure to commercial asbestos in each of the jobs. The panels considered regular (everyday) and shutdown responsibilities separately. (Shutdowns are scheduled periods when regular processing at a mining operation stops so that equipment can be retooled or maintained. Workers may change jobs or even move to a different facility to perform shutdown duties.) The panels rated
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the jobs as exposed (in terms of high likelihood/high intensity; high likelihood/low intensity; low likelihood/high intensity or low likelihood/low intensity), not exposed, or unknown exposure. When no interviews were available (i.e., no interviewees could be found), the panels made determinations using other information (e.g., job descriptions and their own knowledge). If no determination could be made, the potential for exposure was marked unknown.
Table 1 Summary of estimated exposures to commercial asbestos 20 or more years prior to diagnosis for 17 iron-mining employees who developed mesothelioma Likelihood of exposure to commercial asbestos
Total No.
Exposure in nonmining occupation(s)
Exposure in mining occupation(s)
Exposure in both mining and non-mining occupations
Probable Possible None identified Unknown due to incomplete job histories
11 3 1 2
3a 1 — —
4 0 — —
4 2 — —
2.5. Identification of possible exposures in non-mining occupations Other studies of asbestos-exposed occupations were reviewed to determine whether a particular non-mining job could have involved exposure to commercial asbestos. In addition, the list of miners with mesothelioma was checked against a roster of former Conwed employees (Minnesota Department of Health, 1989), to see how many had also worked at that facility. Any Conwed job was considered as having potential commercial asbestos exposure. A final review of these jobs was provided by the CIH.
a Includes two individuals who also had non-mining occupations with possible exposure.
3. Results 3.1. Description of the case series Of the 340 male Minnesota residents diagnosed with mesothelioma between 1988 and 1996, 17 were found to have worked in the iron mining industry. Two of the 17 also worked at Conwed. None of the 92 female Minnesotans diagnosed with mesothelioma between 1988 and 1996 were found in the iron miner cohort. Fifteen of the 17 were diagnosed with pleural mesothelioma while two had peritoneal mesothelioma. The age at diagnosis ranged from 55 to 82. Fourteen were diagnosed while residing in northeastern Minnesota while three were diagnosed while living elsewhere in Minnesota. Since MCSS only collects cancer data for Minnesota residents, it is not known how many, if any, miners may have developed mesothelioma outside of Minnesota. 3.2. Occupational histories The number of different iron mining jobs held by each of the 17 men varied, as did the length of their employment in the mining industry, ranging from 2 months to 40 years. With the addition of known non-mining jobs, the extent of the employment history documented for the 17 men ranged from 5 to 60 years. The years of their employment ranged from the 1930s through the 1980s. Complete job histories for the relevant exposure period were available for 10 of the 17 cases. For five cases, there were small gaps in job history information. Thus, for 15 cases, occupational histories were sufficiently complete to allow evaluation of potential exposures to commercial asbestos. A listing of occupations held by the cases is included in the MDH report (Minnesota Department of Health, 2003). 3.3. Exposures to commercial asbestos Table 1 contains a summary of the panel exposure estimates for the 17 cases in terms of ‘‘probable’’ and ‘‘possible’’ likelihood of exposure. Probable was used when the
panel exposure estimate was: high likelihood/high intensity; high likelihood/low intensity or low likelihood/high intensity. Possible was used when panel exposure estimate was low likelihood/low intensity. Fourteen of the 15 miners who developed mesothelioma had potential exposures to commercial asbestos: 11 had job(s) with probable exposure to commercial asbestos and another 3 had job(s) with possible exposure to commercial asbestos. One of the 15 had no apparent occupational exposures to commercial asbestos based on the information that was available. For two of the 17, a potential source of exposure could not be determined because the jobs they held for significant portions of their job histories were unknown. Potential exposures to commercial asbestos were found in both mining and non-mining occupations. Many of the asbestos-exposed occupations held by the cases, like plumbing, were common to both mining and non-mining industries. Examples of mining jobs identified as having potential exposures to commercial asbestos were carpenter, maintenance mechanic and plumber. Non-mining jobs having potential exposures included boiler operator, sheet metal worker and Conwed (Cloquet, Minnesota) worker. The exposure determinations for the mining jobs are company-specific. That is, the panels rated the jobs as they existed at certain companies in the time period of interest, so exposure ratings may not be true for the same job title at a different operation. The time between employment in these asbestos-exposed occupations and the diagnosis of mesothelioma in this study was consistent with the 20 or more year latency period that has been observed in other studies of this cancer. Of the 14 cases who held occupations in which exposure was possible or probable, mining occupations were the only identified source for 4; non-mining occupations were the only identified source for 4; and both mining and non-mining occupations were identified for 6. As noted in Table 1, 2 cases who had a non-mining job with probable exposure and a mining job with possible exposure were categorized as ‘‘probable/non-mining’’.
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4. Discussion This study identified 17 Minnesota iron miners who were diagnosed with mesothelioma between 1988 and 1996. While the mesothelioma risk among miners cannot be quantified in this study and is not solely attributable to exposures within the mining workplace, this finding is in sharp contrast to previously published death certificate-based studies of Minnesota iron ore miners that have not found mesotheliomas or excesses of other respiratory diseases (Cooper et al., 1988, 1992; Higgins et al., 1983; Lawler et al., 1985). This finding, along with the results of the exposure assessment, demonstrates that exposure to asbestos has occurred in the iron mining industry during previous decades. Because of the long latency of asbestosrelated diseases, these risks will continue into the future even in the absence of ongoing exposures. 4.1. Limitations and strengths Case series studies, such as this study, must be cautiously interpreted. While exposures among the cases are categorized and explicitly described, there is no control group for comparison, and thus exposures among non-cases can only be implicitly assumed based on historical data or other knowledge. However, where there is a very strong relationship between exposure and disease, useful insights may be obtained even in the absence of controls (Cummings and Weiss, 1998). As with analytic studies, other sources of bias should still be addressed. The major limitation of this study was the assessment of previous commercial asbestos exposure. This assessment was based on job titles and occupational histories—not actual monitoring data—and utilized existing records. Due to statutory limitations, study protocols did not allow contact of next of kin to gain more information about the work histories and potential exposures of the 17 individuals diagnosed with mesothelioma who worked in the mining industry. Complete work histories were not found for 2 of the 17. For one, documentation only up to age 26 was available. Complete information may or may not have been found regarding an individual’s work outside of the mining industry. This depended on whether the prior work history was included in their employment records, or was available through other sources (e.g., death notices). In addition, nothing was known about any non-occupational asbestos exposures (e.g., hobbies, home environment, spouse’s occupational exposures). Quantitative exposure data on which to base the assignment of asbestos exposure were not available. Even with qualitative exposure estimates, assumptions were made that a particular job title in a particular year at a particular mine conferred a particular probability of exposure. In addition, nothing was known about possible use of personal protective equipment.
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Despite these limitations, this study has several strengths. First, a major strength is this study’s use of cancer registry data, rather than death certificates, to identify all mesothelioma cases in the state. MCSS data come from the pathology reports and clinical records confirming that a cancer has been diagnosed. Quality control studies confirm the completeness and accuracy of these data. In contrast, death certificate-based studies (prior to the change from the International Classification of Disease revision 9 to revision 10 in 1999) will likely miss many, if not most, cases of mesothelioma that are often coded to other causes of death (such as lung cancer) (Lilienfeld and Gunderson, 1986). Among the 17 cases of mesothelioma in this study, only one would have been detected by the cause-of-death codes used for mesothelioma on death certificates (despite the fact that most of the death certificates had some mention of mesothelioma on the death certificate itself). A second strength is the study’s use of the previously established Minnesota Iron Miner cohort. Because those diagnosed with mesothelioma or their next of kin could not be contacted for this study, it would have been much more difficult and much less accurate to determine whether persons diagnosed with mesothelioma had ever worked in the mining industry without the mining cohort information. Mining cohort data also provided most of the information about the job titles and dates of employment for the study subjects. A third strength was the protocol that blinded the assessment of potential exposures to commercial asbestos. None of the participants in the study knew which job titles were associated with miners who later developed mesothelioma. Finally, the involvement of a technical advisory group provided information that was vital to the satisfactory completion of this study. The collaboration between labor and industry in the development of the protocol for this study allowed current and former iron miners to be interviewed about exposures to commercial asbestos in their jobs, in a way that ensured the confidentiality of their responses. In addition, the use of assessment panels consisting of mining company, labor and other industrial hygiene/safety professionals brought the most knowledgeable people together to make the best assessments with the available information. 4.2. Health issues not addressed by this study While the study findings establish that miners are at some risk of mesothelioma and that past exposure to commercial asbestos is a likely explanation, this study does not address other significant health questions. In particular, this study does not address the morbidity and mortality among iron miners from all types of cancer or respiratory diseases, nor does it attempt to address potential health risks from exposures to respirable mineral dusts from taconite ore and its processing (silica, taconite, cummingtonite-grunerite, cleavage fragments, etc.). Other types of epidemiologic studies, such as a mortality follow-up study
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(in which death rates and causes of death among miners would be compared to that for the overall population) or a medical screening of iron miners (which could look at lung abnormalities), would be required to address these questions. 5. Conclusion Our findings demonstrate an unquantified risk of mesothelioma among former Minnesota iron miners and suggest that commercial asbestos exposure (inside and outside of the mining industry) is the likely cause of mesothelioma in this case series. However, at least one miner had no identifiable source of exposure to commercial asbestos and other causes cannot be ruled out. Conflict of Interest The authors declare that they have no conflicts of interest. Funding Source Funded by the state of Minnesota. References Bender, A.P., Williams, A.N., Parker, D.L., 1993. Experiences of a statesponsored notification and screening program for asbestos workers. Am. J. Ind. Med. 23, 161–169. Breslow, N.E., Day, N.E., 1987. Statistical methods in cancer research. Volume II—the design and analysis of cohort studies. IARC Sci. Publ. 82, 1–406. Clark, T.C., Harrington, V.A., Asta, J., Morgan, W.K., Sargent, E.N., 1980. Respiratory effects of exposure to dust in taconite mining and processing. Am. Rev. Respir. Dis. 121, 959–966. Cooper, W.C., Wong, O., Graebner, R., 1988. Mortality of workers in two Minnesota taconite mining and milling operations. J. Occup. Med. 30, 506–511. Cooper, W.C., Wong, O., Trent, L.S., Harris, F., 1992. An updated study of taconite miners and millers exposed to silica and non-asbestiform amphiboles. J. Occup. Med. 34, 1173–1180.
Cummings, P., Weiss, N., 1998. Case series and exposure series: the role of studies without controls in providing information about the etiology of injury or disease. Inj. Prev. 4, 54–57. Fellegi, I., Sunter, A., 1969. A theory for record linkage. J. Am. Stat. Assoc. 25, 172–178. Fletcher, A., Engholm, G., Englund, A., 1993. The risk of lung cancer from asbestos among Swedish construction workers: self-reported exposure and a job exposure matrix compared. Int. J. Epidemiol. 22 (Suppl. 2), S29–S35. Higgins, I.T., Glassman, J.H., Oh, M.S., Cornell, R.G., 1983. Mortality of Reserve Mining Company employees in relation to taconite dust exposure. Am. J. Epidemiol. 118, 710–719. Hilding, A.C., Hilding, D.A., Larson, D.M., Aufderheide, A.C., 1981. Biological effects of ingested amosite asbestos, taconite tailings, diatomaceous earth and Lake Superior water in rats. Arch. Environ. Health 36, 298–303. Langer, A.M., Maggiore, C.M., Nicholson, W.J., Rohl, A.N., Rubin, I.B., Selikoff, I.J., 1979. The contamination of Lake Superior with amphibole gangue minerals. Ann. NY Acad. Sci. 330, 549–572. Lawler, A.B., Mandel, J.S., Schuman, L.M., Lubin, J.H., 1985. A retrospective cohort mortality study of iron ore (hematite) miners in Minnesota. J. Occup. Med. 27, 507–517. Levy, B.S., Sigurdson, E., Mandel, J., Laudon, E., Pearson, J., 1976. Investigating possible effects of asbestos in city water: surveillance of gastrointestinal cancer incidence in Duluth, Minnesota. Am. J. Epidemiol. 103, 362–368. Lilienfeld, D.E., Gunderson, P.D., 1986. The ‘‘missing cases’’ of pleural malignant mesothelioma in Minnesota, 1979–81: preliminary report. Public Health Rep. 101, 395–399. Minnesota Cancer Surveillance System, 1997. Cancer rates and trends in Northeastern Minnesota. MCSS Epidemiology Report 97:1. Minnesota Cancer Surveillance System, 1999. Cancer incidence rates in Northeastern Minnesota. MCSS Epidemiology Report 99:2. Minnesota Cancer Surveillance System, 2003. Cancer incidence rates in Northeastern Minnesota with an emphasis on mesothelioma, MCSS Epidemiology Report 03:1. Minnesota Department of Health, 1989. Medical screening for asbestos-related lung disease among Conwed Corporation (Cloquet) workers and their spouses: preliminary report to the Minnesota Legislature. Minnesota Department of Health, 2003. Exposures to commercial asbestos in Northeastern Minnesota iron miners who developed mesothelioma. Minneapolis; November 7, 2003. Available online: http://www.health.state.mn.us/divs/hpcd/cdee/occhealth/reports.html. Williams, A.N., 1994. An epidemiologic study of radiographic abnormalities among asbestos ceiling tile workers and their spouses. University of Minnesota, Minneapolis.