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Population Cancer Risks Associated with Coal Mining: A Systematic Review

  • Wiley D. Jenkins ,

    wjenkins@siumed.edu

    Affiliation Center for Clinical Research, Department of Family and Community Medicine, Southern Illinois University School of Medicine, Springfield, Illinois, United States of America

  • W. Jay Christian,

    Affiliation College of Public Health, University of Kentucky, Lexington, Kentucky, United States of America

  • Georgia Mueller,

    Affiliation Center for Clinical Research, Southern Illinois University School of Medicine, Springfield, Illinois, United States of America

  • K. Thomas Robbins

    Affiliation Simmons Cancer Institute, Department of Surgery, Southern Illinois University School of Medicine, Springfield, Illinois, United States of America

Population Cancer Risks Associated with Coal Mining: A Systematic Review

  • Wiley D. Jenkins, 
  • W. Jay Christian, 
  • Georgia Mueller, 
  • K. Thomas Robbins
PLOS
x

Abstract

Background

Coal is produced across 25 states and provides 42% of US energy. With production expected to increase 7.6% by 2035, proximate populations remain at risk of exposure to carcinogenic coal products such as silica dust and organic compounds. It is unclear if population exposure is associated with increased risk, or even which cancers have been studied in this regard.

Methods

We performed a systematic review of English-language manuscripts published since 1980 to determine if coal mining exposure was associated with increased cancer risk (incidence and mortality).

Results

Of 34 studies identified, 27 studied coal mining as an occupational exposure (coal miner cohort or as a retrospective risk factor) but only seven explored health effects in surrounding populations. Overall, risk assessments were reported for 20 cancer site categories, but their results and frequency varied considerably. Incidence and mortality risk assessments were: negative (no increase) for 12 sites; positive for 1 site; and discordant for 7 sites (e.g. lung, gastric). However, 10 sites had only a single study reporting incidence risk (4 sites had none), and 11 sites had only a single study reporting mortality risk (2 sites had none). The ecological study data were particularly meager, reporting assessments for only 9 sites. While mortality assessments were reported for each, 6 had only a single report and only 2 sites had reported incidence assessments.

Conclusions

The reported assessments are too meager, and at times contradictory, to make definitive conclusions about population cancer risk due to coal mining. However, the preponderance of this and other data support many of Hill’s criteria for causation. The paucity of data regarding population exposure and risk, the widespread geographical extent of coal mining activity, and the continuing importance of coal for US energy, warrant further studies of population exposure and risk.

Introduction

Cancers are several of the leading causes of death in the US, and disparities persist in both incidence and mortality. The American Cancer Society (ACS) and the National Cancer Institute (NCI) report that one in every four American deaths is attributable to cancer. The ACS estimates 901,230 new cancer diagnoses and 279,710 cancer deaths in the US are attributable to cancers at the four most common sites: female breast, colorectal, lung and bronchus, and prostate (B/C/L/P) [1]. According to the NCI Cancer Trends Progress Report, improvements in personal lifestyle behaviors, such as smoking, nutrition and physical activity could reduce cancer deaths by 50–75 percent [2]. However, a disproportionate cancer burden exists among people who cannot reduce their risk by personal choice. While the overall mortality and incidence rates for cancer are declining in our country, certain populations continue to show higher risk and worse outcomes in cancer-related illness (e.g., blacks are more likely to develop and die from cancer, and be diagnosed at a later stage, than other races and ethnicities) [3].

A complex set of economic, geographic, and social determinants of health create cancer health disparities. Some risk factors, such as age and family history, are largely due to biological mechanisms and the accumulation of risks and exposures over time and cannot be modified [4]. However, there remain potentially modifiable risk factors to which individuals may be exposed without their knowledge, and to disparate levels based upon race and location [5]. Location is particularly relevant when considering exposure to industrial operations. While there are studies showing increased cancer risk due to occupational exposure to carcinogens, there is a paucity of data examining the impact of industrial operations to the cancer rates of potentially exposed surrounding populations (non-occupationally exposed) [6][8]. The potential for such exposure is large, as the United State Environmental Protection Agency Enforcement Division pursued 1,754 civil and 64 criminal cases for violation of the federal Clean Air and Water Acts in 2012 alone [9]. The health effects to the surrounding populations are largely unknown, and it is important to determine if proximity to specific industries is associated with increased cancer risk so that appropriate protective measures may be taken. This is of increased importance for industries which are of large scale or great geospatial extent, and thus present increased potential for widespread exposure.

In recent years the extraction of fossil fuels has attracted substantial attention for its potentially damaging effects to the environment and human health [10][12]. The US mined >1 billion tons of coal in 2011, with 90% being used for domestic electricity production in 580 coal-fired power plants [13]. Coal fuels nearly half (42%) of the 4 trillion kilowatt-hours of electricity generated in the United States in 2011 [14]. Coal is produced in 25 states across three major coal-producing regions (see Figure 1). US production is estimated to increase 7.6% by 2035, and current production rates result in an estimated coal reserve exceeding 200 years [14], [15]. Oil and gas reserves at the global level are estimated to be sufficient through 2100, but there is risk to US national security in reliance upon foreign sources of power. For example, 22% of imported petroleum comes from the Persian Gulf states and another 11% from Venezuela [16]. These circumstances, and the development of more effective scrubbing mechanisms and other technological advances, have resulted in sustained interest in coal as a source of fuel (especially for large-scale electrical generation). As coal mining both continues and expands in large areas of the continental US, it is therefore important to understand the health risks potentially associated with such activity so that preventive measures may be adopted as needed. The geospatial extent of coal bearing fields is considerable (Figure 1), underlying, for example, 33% of Missouri and 68% of Illinois [17].

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Figure 1. Distribution of coal-bearing stratifications in the 48 contiguous United States.

https://doi.org/10.1371/journal.pone.0071312.g001

Our objective was to review recent peer-reviewed literature to assess the evidence of a relationship between exposure to coal mining activities and cancer incidence and mortality. We will thus explore studies relating to several specific cancer sites, as well as different sources and routes of exposures, to identify gaps or weaknesses in the literature where future research may be profitably directed.

Methods

Eligibility criteria included: English language, peer-review, publication since 1980, basis in human subjects, and explicit examination of coal mining and associated or subsequent cancer of any kind. Furthermore, we excluded studies focusing on investigations of radiological associations with cancer as they are not specific to coal mining. We searched PubMed, EbscoHost (Academic Search Premier and MEDLINE Complete), and Cochrane Library using the terms: ‘cancer’ in TITLE and ‘coal mining’ in ANY FIELD as well as ‘coal mining’ in TITLE and ‘cancer’ in ANY FIELD. Retrieved articles’ bibliographies were reviewed for additional manuscripts not otherwise identified. The authors reviewed study abstracts retrieved by the search and determined eligibility by consensus. We extracted the following information from each study, as available: study design, population studied and size, exposure type, reported cancer end points and strengths of association (e.g. OR, RR, SMR), and statistical significance (e.g. p-values or confidence intervals).

There are several risks of bias at the level of the individual study. For example, occupational studies of coal miners may suffer from ‘healthy worker effect” whereby only those individuals who are of greater health engage in this physically demanding profession – resulting in a lower estimate of risk compared to the general population [18], [19]. On the other hand, coal miners are subject to a considerable number of long-term studies of health and health outcomes – resulting in perhaps greater surveillance and identification of disease than experienced by the general population. Bias at a larger scale may be due to publication bias present in the underreporting/under publishing of studies showing no association between coal mining and cancer.

Results

The initial search criteria returned 98 unique manuscripts (45 from PubMed, 46 from EbscoHost, and additional 7 from bibliographic review). All abstracts were reviewed by WDJ and GM for inclusion based upon study criterion and rejection/retention determined by consensus. From these, 64 were removed as not directly examining associations between coal mining activity and human cancer or duplicate reporting of study results (Figure 2). The remaining 34 studies were separated into two main categories: A) 27 studies of coal mining as an occupational risk factor for cancer [19][45], and B) 7 ecological/cross-sectional studies of coal mining and associated cancer risk in the surrounding population [46][52]. The occupation studies may be further classified as: A1) those that examined cohorts of coal miners (standardized incidence/mortality ratios calculated; SIR/SMR; relative risks (RR)) [19][28], and A2) those examining coal mining as a risk factor in case-control analysis (odds ratios (OR) calculated) [29][45]. While categories A1 and A2 both explicitly examine coal mining and associated cancer risk, category A1 does so by specifically selecting coal miners for comparison to others (e.g. cohort studies) while category A2 includes coal mining as a risk factor. Table 1 lists all retained studies and important information from each. Tables 2 and 3 describe the cancer risks drawn from these studies. As studies were performed over differing time periods and in differing places, there was some inconsistency in how cancer was reported and we have thus condensed results of studies of similar cancers into single categories (e.g. ‘gastric’ and ‘stomach’ into the category ‘Digestive/Gastric/Stomach’). The evidence presented by these studies is both inconsistent in that some examine incidence, others mortality, and some both, as well as frequently contradictory in the direction of the results.

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Table 1. Manuscripts identified by the systematic review and stratified by A1) occupational cohorts, A2) occupational risk factors, and B) ecological population-level studies.

https://doi.org/10.1371/journal.pone.0071312.t001

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Table 2. Estimations of cancer risks reported from occupational studies (both occupation as cohort and case-control risk factor).

https://doi.org/10.1371/journal.pone.0071312.t002

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Table 3. Estimations of cancer risks reported from population (ecological) studies.

https://doi.org/10.1371/journal.pone.0071312.t003

The 10 studies comprising category A1 were conducted from the 1950s through 2006 and include anywhere from 1,602 to 24,736 miners, while the 17 studies in category A2 (all case/control except for Une et al which used population split into cohorts) were conducted from the late 1960s through 1994 and are generally smaller in scale with sample sizes ranging from 92 to >16,000 (only 4 exceeded 1,000 individuals). Individual cancer results are shown in Table 2; these studies variously report incidence and/or mortality for 19 cancer sites/categories. Consistent assessment of risk exists for bone, brain, colon/rectum, kidney, leukemia/aleukemia, lymphomas, melanoma, mouth/buccal cavity/oral, multiple myeloma, pancreas, prostate and testis (no increased risk), and liver (increased mortality). Several studies report multiple risk assessments based upon different adjustments, exposures, or populations studied. The 7 studies from category B (ecological/cross-sectional) are generally much more recent, using data ranging from 1969–2006, and are generally larger, including, for example, all administrative areas in Japan or Appalachian counties [49], [52]. Individual cancer results are shown in Table 3; these studies variously report incidence and/or mortality for 9 cancer sites/categories. Consistent assessment of risk is found for breast, digestive/gastric/stomach, oral and urinary (no increased risk), and colon/rectum and total/combined (increased incidence or mortality). Again, one study here reported differing risks based upon gender.

Table 4 lists all cancer sites for which risks were assessed and reported, and the numbers of studies for each. While the digestive/gastric/stomach and lung/trachea/bronchus/respiratory categories have multiple assessments of both incidence and mortality, 4 cancers lack any assessment of incidence risk (breast, liver, pancreas, urinary), 2 lack any assessment of mortality risk (kidney and laryngeal/hypolaryngeal), and 11 have only a single study reporting risk assessment of incidence or mortality.

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Table 4. Listing of cancers specifically assessed by selected studies* and the number reporting incidence and mortality for each.

https://doi.org/10.1371/journal.pone.0071312.t004

Discussion

We identified 34 studies published since 1980 specifically examining the increased risk of cancer associated with coal mining and associated activities. Twenty-seven of these explicitly examined coal miners/coal mining as an occupational cohort or risk factor. Coal miners as a group have long been studied for adverse health outcomes, and liver was the only cancer site for which only an increased risk was reported (mortality; single study). There were only 7 studies found specifically examining the association between proximity to coal mining activities and cancer risk in the general population, and unequivocal increased risk was found for colon/rectum (mortality) and total (combined) cancer (incidence and mortality). However, increased risks for population subsets were also unequivocally reported for bladder (males, mortality) and leukemia/aleukemia (combined genders, mortality). While the population studies are generally more likely to report increased risk, this may be attributed in part to publication bias, or perhaps the tendency for coal mining regions to have high poverty rates. Some areas with both high cancer rates and coal mining activity also face increased smoking, overweight, and other cancer risk factors [49], [51]. Overall, it is difficult to ascertain cancer risk associated with exposure to coal mining, due to the contradictory results of research examining commonly studied cancer sites, the paucity of studies examining other sites, and the weaknesses inherent in cross-sectional, population-level studies.

However, given the wide scale and extent of coal mining in the US, the potential exposure of large populations to mining activities, the potential for significantly increased risk of cancer incidence and mortality, and the perhaps modifiable nature of the exposures, our position is that a closer and more rigorous examination of cancer risk associated with coal mining exposure is warranted based upon the Hill criteria [53]. These criteria were originally developed for application to infectious disease, and so some may not be as suitable (e.g. specificity) or easily evaluated (e.g. temporality) when applied to cancer. For example, the cohort studies included here contribute data concerning the temporal relationship between mining activity and cancer, but this is more problematic for the case-control studies where there may be biases in remembering exposure types, dates and duration. There is some evidence that increasing exposure leads to increased cancer risk (dose-response relationship). In miners, this was seen in increased risk with longer exposure (years mining) [27], [37]. Of the seven ecological/cross-sectional studies we identified, six of them showed increased cancer risk (strength of association), with calculated RR and OR significantly increased for 7 specific cancers reported in 7 studies, as well as total cancer reported in 3 studies (Table 3). While the data from ecological/cross-sectional studies are sparse, they fairly consistently show an increased risk of cancer in association with residence near coal mining (consistency). However, only the results regarding colon and rectal cancers and total cancers are unequivocal, with some cancer risks specific to location or gender [48].

Plausibility is perhaps the strongest criteria here. Whong et al showed that the nitrosation of coal extracts via acid exposure increased mutagenic activity – possibly contributing to the observed increase gastric cancer risk [54]. Studies of coal dust exposure (not definitively related to coal mining and thus not previously included) report increased risk of lung cancer [55][57]. As coal may contain high amounts of carcinogens such as silica dust, polyaromatic hydrocarbons, cadmium, arsenic and others, it is plausible to consider a link between coal dust inhalation into the lungs and subsequent cancer [58], [59]. Indeed, studies have shown increased lung cancer risk in homes using coal as a fuel for cooking or heating and the IARC has determined that indoor emissions from the household combustion of coal are carcinogenic [60][62]. One study has even detailed chronic poisoning effects from burning coal containing high levels of arsenic (100–9,000 ppm) [63]. Other findings suggesting that exposure to coal components increases risk include increased malignancy/cell proliferation of kidney cells exposed to large molecular weight compounds mobilized from lignite beds [64], greatly increased levels of crystalline silica in coal in areas of high lung cancer [65], association between high female lung cancer mortality and high-silica coal mine proximity [59], and increased DNA mutations found in mice and rats living in coal mining areas compared to non-exposed controls [66]. Finally, there are studies showing that coal mining contaminates the surrounding air and water [67][70].

Taken together, the concern that exposure to coal mining may result in increased risk of cancer is reasonable, and fits with models of exposure, pathogenicity, and outcome (coherence). Minerals associated with coal deposits often include human carcinogens (e.g. As, silica). Individuals may be exposed to them in multiple routes (e.g. inhalation, ingestion). There are biologically plausible pathways whereby exposure may result in cancer genesis/promotion. And finally there are population-level studies showing that residing near coal mining increases an individual’s cancer risk.

The last two of Hill criteria, alternate explanations and experiment, are not likely to add or detract from our position. For example, it is well known that smoking is the greatest risk factor for lung cancer and may at times be poorly captured or adjusted for, and second-hand smoke exposure even more difficult to ascertain. It is likely that there will be few cancers for which alternative explanations do not contribute.

There are limitations to this study. For example, included studies encompass a wide time frame (1980 through 2012) and were conducted in 12 countries. It is likely that there are substantial variations in culture, as well as exposure and safety mechanisms across time and location, which are not accounted for. Complicating the direct comparison of cancer risk is the differences in how cancer sites were described (e.g. ‘gastric’ and ‘stomach’), frequently with no clear definition. We therefore grouped studies together as seemed appropriate, but may be in error. Some studies did not include measures of confidence or significance, limiting our ability to objectively determine if there was in fact increased risk observed. To be conservative, we assumed non-significance in the absence of other confidence or significance data, but this may be in error. For the ecological studies, their cross-sectional nature limits their ability to impute strong association. Finally, the diversity of data collected, cancer sites reported and populations studied precludes the utility of meta-analysis, making our study much more qualitative in nature.

Given the increasing use of coal for energy production in the US, the large numbers of individuals potentially exposed to agents associated with coal mining activities, the equivocal nature of existing studies, and the plausibility for exposure to increase cancer risk, further investigation is needed. Specifically, the available data indicate that there is a need to purposefully and prospectively examine the risk of cancer to the surrounding population from coal mining activity. At this point little is known concerning routes, duration and timing of exposures; which specific agent(s) may be associated with increased cancer risk; or the population at risk in terms of residential proximity. Furthermore, while much study has been made in general concerning personal attributes and behaviors which may aggravate/mitigate exposure and cancer risk, it is unknown how these interact with exposure to coal mining activities. Such items need to be investigated if effective interventions are to be designed, implemented, and evaluated. Such studies, however, would need to be large in scale and long-term. One occupational study, for example, showed lung cancer risk lagging exposure by 15 years.29 Recognizing that such studies are likely quite expensive and perhaps infeasible, we propose that interim markers of exposure or increased cancer risk be developed, validated and used as proxies.

Supporting Information

Author Contributions

Conceived and designed the experiments: WDJ WJC GM. Performed the experiments: WDJ WJC GM. Analyzed the data: WDJ WJC GM. Wrote the paper: WDJ WJC GM KTR.

References

  1. 1. American Cancer Society. Learn about cancer. Available: http://www.cancer.org/cancer/index. Accessed 2012 Dec 17.
  2. 2. National Institutes of Health. National Cancer Institute. Cancer Trends Progress Report - 2011/2012. Available: http://progressreport.cancer.gov/index.asp. Accessed 2012 Dec 3.
  3. 3. American Cancer Society. Cancer disparities: key statistics. Available: http://www.cancer.org/cancer/news/features/cancer-disparities-key-statistics. Accessed 2012 Dec 17.
  4. 4. National Institutes of Health. National Cancer Institute. What you need to know about cancer. Available: http://www.cancer.gov/cancertopics/wyntk/cancer/page3. Accessed 2012 Dec 16.
  5. 5. Wagner SE, Hurley DM, Hébert JR, McNamara C, Bayakly AR, et al. (2012) Cancer mortality-to-incidence ratios in Georgia: describing racial cancer disparities and potential geographic determinants. Cancer 118: 4032–45.
  6. 6. Berry G, Reid A, Aboagye-Sarfo P, de Klerk NH, Olsen NJ, et al. (2012) Malignant mesotheliomas in former miners and millers of crocidolite at Wittenoom (Western Australia) after more than 50 years follow-up. Br J Cancer 106: 1016–20.
  7. 7. Elliott L, Loomis D, Dement J, Hein MJ, Richardson D, et al. (2012) Lung cancer mortality in North Carolina and South Carolina chrysotile asbestos textile workers. Occup Environ Med 69: 385–90.
  8. 8. Schnatter AR, Nicolich MJ, Lewis RJ, Thompson FL, Dineen HK, et al. (2012) Lung cancer incidence in Canadian petroleum workers. Occup Environ Med 69: 877–82.
  9. 9. US Environmental Protection Agency. Enforcement and Compliance History Online (ECHO). Available: http://www.epa-echo.gov/echo/#. Accessed 2013 Feb 13.
  10. 10. Thompson H (2012) Fracking boom spurs environmental audit. Nature 485: 556–7.
  11. 11. Mitka M (2012) Rigorous evidence slim for determining health risks from natural gas fracking. JAMA 307: 2135–6.
  12. 12. Howarth RW, Ingraffea A, Engelder T (2011) Natural gas: Should fracking stop? Nature 477: 271–5.
  13. 13. US Energy Information Administration. Electric Power Annual 2010. Available: http://www.eia.gov/electricity/annual/. Accessed 16 January 2013.
  14. 14. US Energy Information Administration. Coal. Available: http://www.eia.gov/coal/. Accessed 2012 Oct 7.
  15. 15. US Energy Information Administration. What is the role of coal in the United States. Available: http://www.eia.gov/energy_in_brief/article/role_coal_us.cfm. Accessed 2012 Dec 18.
  16. 16. US Energy Information Administration. How dependent are we on foreign oil? Available: http://www.eia.gov/energy_in_brief/foreign_oil_dependence.cfm. Accessed 2012 Oct 7.
  17. 17. U.S. Department of the Interior. Office of Surface Mining Reclamation and Enforcement. Available: http://www.mcrcc.osmre.gov/MCR/States/Missouri.shtm?tab=1#TabbedPanels1. Accessed 2013 Feb 1.
  18. 18. Fox AJ, Collier PF (1976) Low mortality rates in industrial cohort studies due to selection for work and survival in the industry. Br J Prev Soc Med 30: 225–30.
  19. 19. Morfeld P, Lampert K, Ziegler H, Stegmaier C, Dhom G, et al. (1997) Overall mortality and cancer mortality of coal miners: attempts to adjust for healthy worker selection effects. Ann Occup Hyg 41: 346–51.
  20. 20. Acheson ED, Cowdell RH, Rang EH (1981) Nasal cancer in England and Wales: an occupational survey. Br J Ind Med 38: 218–24.
  21. 21. Attfield MD, Kuempel ED (2008) Mortality among U.S. underground coal miners: a 23-year follow-up. Am J Ind Med 51: 231–45.
  22. 22. Atuhaire LK, Campbell MJ, Cochrane AL, Jones M, Moore F (1986) Gastric cancer in a south Wales valley. Br J Ind Med 43: 350–2.
  23. 23. Brown AM, Christie D, Taylor R, Seccombe MA, Coates MS (1997) The occurrence of cancer in a cohort of New South Wales coal miners. Aust N Z J Public Health 21: 29–32.
  24. 24. Kuempel ED, Stayner LT, Attfield MD, Buncher CR (1995) Exposure-response analysis of mortality among coal miners in the United States. Am J Ind Med 28: 167–84.
  25. 25. Miller BG, Jacobsen M (1985) Dust exposure, pneumoconiosis, and mortality of coalminers. Br J Ind Med 42: 723–33.
  26. 26. Miller BG, MacCalman L (2010) Cause-specific mortality in British coal workers and exposure to respirable dust and quartz. Occup Environ Med 67: 270–6.
  27. 27. Swaen GM, Meijers JM, Slangen JJ (1995) Risk of gastric cancer in pneumoconiotic coal miners and the effect of respiratory impairment. Occup Environ Med 52: 606–10.
  28. 28. Tomaskova H, Jirak Z, Splichalova A, Urban P (2012) Cancer incidence in Czech black coal miners in association with coalworkers’ pneumoconiosis. Int J Occup Med Environ Health 25: 137–44.
  29. 29. Ames RG (1983) Gastric cancer and coal mine dust exposure. A case-control study. Cancer 52: 1346–50.
  30. 30. Ames RG, Gamble JF (1983) Lung cancer, stomach cancer, and smoking status among coal miners. A preliminary test of a hypothesis. Scand J Work Environ Health 9: 443–8.
  31. 31. Ames RG, Amandus H, Attfield M, Green FY, Vallyathan V (1983) Does coal mine dust present a risk for lung cancer? A case-control study of U.S. coal miners. Arch Environ Health 38: 331–3.
  32. 32. Coggon D, Barker DJ, Cole RB (1990) Stomach cancer and work in dusty industries. Br J Ind Med 47: 298–301.
  33. 33. Cordier S, Clavel J, Limasset JC, Boccon-Gibod L, Le Moual N, et al. (1993) Occupational risks of bladder cancer in France: a multicentre case-control study. Int J Epidemiol 22: 403–11.
  34. 34. Goldberg P, Leclerc A, Luce D, Morcet JF, Brugère J (1997) Laryngeal and hypopharyngeal cancer and occupation: results of a case control-study. Occup Environ Med 54: 477–82.
  35. 35. Golka K, Bandel T, Schlaefke S, Reich SE, Reckwitz T, et al. (1998) Urothelial cancer of the bladder in an area of former coal, iron, and steel industries in Germany: a case-control study. Int J Occup Environ Health 4: 79–84.
  36. 36. González CA, Sanz M, Marcos G, Pita S, Brullet E, et al. (1991) Occupation and gastric cancer in Spain. Scand J Work Environ Health 17: 240–7.
  37. 37. Hosgood HD 3rd, Chapman RS, Wei H, He X, Tian L, et al. (2012) Coal mining is associated with lung cancer risk in Xuanwei, China. Am J Ind Med 55: 5–10.
  38. 38. Jöckel KH, Ahrens W, Jahn I, Pohlabeln H, Bolm-Audorff U (1998) Occupational risk factors for lung cancer: a case-control study in West Germany. Int J Epidemiol 27: 549–60.
  39. 39. Lloyd OL, Ireland E, Tyrrell H, Williams F (1986) Respiratory cancer in a Scottish industrial community: a retrospective case-control study. J Soc Occup Med 36: 2–8.
  40. 40. Meijers JM, Swaen GM, Slangen JJ, van Vliet C (1988) Lung cancer among Dutch coal miners: a case-control study. Am J Ind Med 14: 597–604.
  41. 41. Schifflers E, Jamart J, Renard V (1987) Tobacco and occupation as risk factors in bladder cancer: a case-control study in southern Belgium. Int J Cancer 39: 287–92.
  42. 42. Swaen GM, Aerdts CW, Slangen JJ (1987) Gastric cancer in coalminers: final report. Br J Ind Med 44: 777–9.
  43. 43. Swanson GM, Lin CS, Burns PB (1993) Diversity in the association between occupation and lung cancer among black and white men. Cancer Epidemiol Biomarkers Prev 2: 313–20.
  44. 44. Une H, Esaki H, Osajima K, Ikui H, Kodama K, et al. (1995) A prospective study on mortality among Japanese coal miners. Ind Health 33: 67–76.
  45. 45. Weinberg GB, Kuller LH, Stehr PA (1985) A case-control study of stomach cancer in a coal mining region of Pennsylvania. Cancer 56: 703–13.
  46. 46. Christian WJ, Huang B, Rinehart J, Hopenhayn C (2011) Exploring geographic variation in lung cancer incidence in Kentucky using a spatial scan statistic: elevated risk in the Appalachian coal-mining region. Public Health Rep 126: 789–96.
  47. 47. Davies JM (1980) Stomach cancer mortality in Worksop and other Nottinghamshire mining town. Br J Can 41: 438–45.
  48. 48. Fernández-Navarro P, García-Pérez J, Ramis R, Boldo E, López-Abente G (2012) Proximity to mining industry and cancer mortality. Sci Total Environ 435–436: 66–73.
  49. 49. Hendryx M, O’Donnell K, Horn K (2008) Lung cancer mortality is elevated in coal-mining areas of Appalachia. Lung Cancer 62: 1–7.
  50. 50. Hendryx M, Fedorko E, Anesetti-Rothermel A (2010) A geographical information system-based analysis of cancer mortality and population exposure to coal mining activities in West Virginia, United States of America. Geospat Health 4: 243–56.
  51. 51. Hendryx M, Wolfe L, Luo J, Webb B (2012) Self-reported cancer rates in two rural areas of West Virginia with and without mountaintop coal mining. J Community Health 37: 320–7.
  52. 52. Minowa M, Stone BJ, Blot WJ (1988) Geographic pattern of lung cancer in Japan and its environmental correlations. Jpn J Cancer Res 79: 1017–23.
  53. 53. Hill AB (1965) The environment and disease: association or causation. Proc Roy Soc Med 58: 295–300.
  54. 54. Whong WZ, Long R, Ames RG, Ong TM (1983) Role of nitrosation in the mutagenic activity of coal dust: a postulation for gastric carcinogenesis in coal miners. Environ Res 32: 298–304.
  55. 55. Morabia A, Markowitz S, Garibaldi K, Wynder EL (1992) Lung cancer and occupation: results of a multicentre case-control study. Br J Ind Med 49: 721–7.
  56. 56. Levin LI, Zheng W, Blot WJ, Gao YT, Fraumeni JF Jr (1988) Occupation and lung cancer in Shanghai: a case-control study. Br J Ind Med 45: 450–8.
  57. 57. Wu-Williams AH, Xu ZY, Blot WJ, Dai XD, Louie R, et al. (1993) Occupation and lung cancer risk among women in northern China. Am J Ind Med 24: 67–79.
  58. 58. World Health Organization. International Agency for Research on Cancer. Volume 68 Silica. Available: http://monographs.iarc.fr/ENG/Monographs/vol68/volume68.pdf. Accessed 2012 16 Dec 16.
  59. 59. Large DJ, Kelly S, Spiro B, Tian L, Shao L, et al. (2009) Silica-volatile interaction and the geological cause of the Xuan Wei lung cancer epidemic. Environ Sci Technol 43: 9016–21.
  60. 60. Cullen J, Bogen KT (2001) Historical U.S. residential coal use and female lung cancer mortality. Human and Ecological Risk Assessment 7: 369–86.
  61. 61. Hosgood HD 3rd, Wei H, Sapkota A, Choudhury I, Bruce N, et al. (2011) Household coal use and lung cancer: systematic review and meta-analysis of case-control studies, with an emphasis on geographic variation. Int J Epidemiol 40: 719–28.
  62. 62. Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F, et al. (2006) Carcinogenicity of household solid fuel combustion and of high-temperature frying. Lancet Oncol 7: 977–8.
  63. 63. Liu J, Zheng B, Aposhian HV, Zhou Y, Chen ML, et al. (2002) Chronic arsenic poisoning from burning high-arsenic-containing coal in Guizhou, China. Environ Health Perspect 110: 119–22.
  64. 64. Bunnell JE, Tatu CA, Lerch HE, Orem WH, Pavlovic N (2007) Evaluating nephrotoxicity of high-molecular-weight organic compounds in drinking water from lignite aquifers. J Toxicol Environ Health A 70: 2089–91.
  65. 65. Dai S, Tian L, Chou C-L, Zhou Y, Zhang M, et al. (2008) Mineralogical and compositional characteristics of Late Permian coals from an area of high lung cancer rate in Xuan Wei, Yunnan, China: Occurrence and origin of quartz and chamosite. Int J Coal Geol 76: 318–27.
  66. 66. León G, Pérez LE, Linares JC, Hartmann A, Quintana M (2007) Genotoxic effects in wild rodents (Rattus rattus and Mus musculus) in an open coal mining area. Mutat Res 15: 42–9.
  67. 67. Ghose MK, Majee SR (2007) Characteristics of hazardous airborne dust around an Indian surface coal mining area. Environ Monit Assess 130: 17–25.
  68. 68. Ghose MK (2007) Generation and quantification of hazardous dusts from coal mining in the Indian context. Environ Monit Assess 130: 35–45.
  69. 69. McAuley SD, Kozar MD Ground-water quality in unmined areas and near reclaimed surface coal mines in the northern and central Appalachian coal regions, Pennsylvania and West Virginia: U.S. Geological Survey Scientific Investigations Report 2006–5059. Available: http://pubs.usgs.gov/sir/2006/5059/. Accessed 2013 Feb 1.
  70. 70. Hitt NP, Hendryx M (2010) Ecological integrity of streams related to human cancer mortality rates. Ecohealth 7: 91–104.