All cause mortality and incidence of cancer in workers in bauxite mines and alumina refineries
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1 Int. J. Cancer: 123, (2008) ' 2008 Wiley-Liss, Inc. All cause mortality and incidence of cancer in workers in bauxite mines and alumina refineries Lin Fritschi 1 *, Jan Lucas Hoving 2, Malcolm R. Sim 3, Anthony Del Monaco 3, Ewan MacFarlane 3, Dean McKenzie 3, Geza Benke 3 and Nicholas de Klerk 4 1 Western Australian Institute for Medical Research, Perth, Australia 2 Coronel Institute for Occupational and Environmental Health, Universiteit van Amsterdam, The Netherlands 3 Monash Centre for Occupational & Environmental Health, Department of Epidemiology & Preventive Medicine, Monash University, Melbourne, Australia 4 Telethon Institute for Child Health Research, Perth, Australia Bauxite is a reddish clay that is refined to produce alumina, which is then reduced to aluminium. There have been studies examining the health of workers in aluminium smelters, but not workers in bauxite mining and alumina refining. A cohort of employees of 1 large aluminium company since 1983 was assembled (n 5 6,485, 5,828 men). Deaths and incident cancers to 2002 were ascertained by linkage to national and state cancer and death registries. SIRs and SMRs were calculated compared to national rates standardizing for calendar year, sex and 5-year age group. The mortality from all causes (SMR 0.68, 95% CI: ), and from circulatory and respiratory diseases, all cancers combined and injury in the male cohort were lower than in the Australian male population and were similar across work groups and with duration of employment. The only significant increased mortality risk was from pleural mesothelioma. The incidence of all cancers combined was similar to the Australian rate. The cohort had a lower risk of incident lymphohaematopoietic cancer (SIR 0.50, 95% CI: ) and a higher risk of melanoma (SIR 1.30, 95% CI: ) although no dose-responses were seen. There was also an increased risk of mesothelioma (SIR 3.49, 95% CI: ), which was associated with exposures outside the aluminium industry. This study is the first to examine cancer and mortality amongst workers in bauxite mines and alumina refineries and found little evidence for increased cancer incidence or mortality in these workers. ' 2008 Wiley-Liss, Inc. Key words: mortality; cancer; bauxite mining; alumina refining; occupation Bauxite is a reddish clay that is refined to produce alumina (AL 2 O 3 ), which is then reduced to make the metal aluminium. While there has been interest in the health of workers in aluminium smelters, 1 3 there are few studies examining the health of workers in other areas of the primary aluminium industry: bauxite mining and alumina refining. Bauxite mining is not traditionally an industry with high levels of hazardous chemical exposures. Bauxite miners are exposed to bauxite dust, and may be exposed to other minerals within that dust such as silica 4 although the ores have negligible radioactivity 5 and serum aluminium levels are not increased. 6 Workers in alumina refineries, where the bauxite is converted to alumina in the presence of caustic soda and heat, are exposed to bauxite dust, alumina dust and caustic soda mist. 4 Alumina refining is possibly associated with radiographic abnormalities on lungs 7 although previous work in our cohort did not show consistent associations between exposure and respiratory symptoms or loss of lung function. 8,9 Australia has 40% of the world s bauxite reserves and has significant refining and smelting industries. We have been undertaking a cohort study of employees in the aluminium industry for some years (Healthwise). The sites for the study comprise 3 bauxite mines, 3 alumina refineries and 2 aluminium smelters. This paper examines the all cause mortality and the cancer incidence in the workers in the bauxite mines and alumina refineries which are located in the state of Western Australia. Material and methods Subjects Former and current employees of a large aluminium company were eligible for inclusion in the cohort if they had been employed for at least 90 days at any of the bauxite mines or alumina refineries on or after 1st January 1983 (the commencement date of national cancer registration in Australia). Workers in maintenance, production and office jobs were eligible but the cohort does not include contractors as a full enumeration of this group was not possible. The cohort study commenced with a survey of workers employed at the sites in 1996 (n 5 3,324). This survey had 89% participation and participants in this survey comprise 51% of the total cohort. For these subjects, demographic details and a full job history were obtained during interview. Workers employed at Alcoa after 1st January 1983 for more than 90 days who had left before the 1996 survey were identified using company records. This group (n 5 2,625) made up 41% of the total cohort and demographic details and a full job history were obtained from human resources records. Employees new to the company after the 1996 survey until December 1999 were invited to join the study when commencing employment and 73% participated. These employees (n 5 536) comprise the remaining 8% of the total cohort. Outcome ascertainment Mortality and cancer incidence was assessed by linkage to the Australian Institute of Health and Welfare (AIHW) for linkage to the National Death Index (NDI) and the National Cancer Statistics Clearing House (NCSCH). The NDI and NCSCH provide complete national coverage of deaths and cancer diagnoses, respectively, from 1983 onwards. At the time of the linkage, complete national information was available to Linkage to the NCSCH and NDI was undertaken using a probabilistic record linkage software package, Integrity version 3.5 (Ascential Software). Linkage is performed using multiple passes that group the data based on increasingly more liberal matching criteria each time. 10 After each pass, a clerical review by AIHW staff is undertaken to exclude improbable matches. As all eligible industry sites are located in Western Australia, we also linked the cohort database directly to the Western Australia Cancer Registry. 11 Because of the different programs and systems used to match cohorts with the registries, and the addi- Grant sponsor: Alcoa of Australia Ltd. *Correspondence to: Western Australian Institute for Medical Research, B block, Hospital Avenue, Sir Charles Gairdner Hospital, Nedlands, WA, 6009 Australia. Fax: fritschi@waimr.uwa.edu.au Received 20 August 2007; Accepted after revision 12 February 2008 DOI /ijc Published online 13 May 2008 in Wiley InterScience ( wiley.com). Publication of the International Union Against Cancer
2 MORTALITY AND CANCER IN BAUXITE AND ALUMINA WORKERS 883 tional personal information held on the state registry, some matches previously undetected by AIHW were now included. In addition, we checked whether matches identified in a previous NCSCH and NDI linkage up to 1996 were included in the present match. Three investigators independently reviewed all potential matches provided by AIHW or the WA Cancer Registry to determine whether or not to accept them. Where the investigators reached different conclusions, a consensus decision was reached. All mesothelioma cases were investigated further using the Western Australian Mesothelioma Registry (WAMR). Every case of mesothelioma reported to the WA Cancer Registry is actively investigated by the WAMR. 12 Relevant exposure information is collected by the WAMR either from the patient or the next of kin. The data collected are assessed by a panel of independent experts who determine the most likely sources of asbestos exposure for each case and therefore the likely cause of the mesothelioma. The most likely cause of the mesothelioma, as determined by the panel, was extracted for each case in our cohort. Exposure assessment Each job was classified as office, maintenance or production and for each employee we calculated the total years spent working in each category. Employees without job history information (n 5 58, <1% of total cohort) were excluded from the analysis. Work histories of the survey participants were only available until the end of 1996, so the assumption was made that each of these employees remained in their 1996 job until the end of 2002 or the date of leaving the company, whichever came first. We classed workers as ever or never employed in each of the 3 work categories. An employee could appear as having ever worked in more than 1 work category. We undertook a further analysis based on length of time spent in production or maintenance jobs in 3 categories: 3 months to <10 years, years and >20 years. Statistical analyses Subjects commenced contributing to person-years when they began work with the company or on the 1st of January 1983, whichever was later. They continued to contribute person-years until 31st December 2002, or until the date of death, whichever came first. Standardized Mortality Ratios (SMR) 13 for all-cause mortality and for specific causes of death were calculated using the national mortality rates and standardizing for sex, 5-year age group and calendar year. Standardized incidence ratios (SIR) were calculated similarly. Results are only presented for those cells with >2 observed cases. We calculated the incidence rate ratios (IRR) with 95% confidence intervals (CI) to investigate whether there was a significant trend for cancer and duration of employment. These calculations show the change in risk between categories of exposure. The test for trend was performed using the GLM (Generalized Linear Models) procedure in Stata 8, which utilizes Poisson regression to carry out trend analyses on SIRs. 14 Robust standard errors (obtained using the cluster option) which allow for multiple cancers were used. 14 As the conventional SIR analysis method assumes independence of observations, the presence of more than 1 primary cancer per person should be taken into account for the analysis of the allcause cancer SIR. In these analyses we adjusted for any dependence between or clustering of observations by using jack-knifing with strata, 15,16 implemented in the STRATE procedure of Stata 8 (Stata Corporation, 2001). More specifically, the following decision rules were applied: If a second primary was at the same site as the first (i.e. the same 3 digit ICD-10 codes) then only the first cancer of the 2 was included in the analysis. TABLE I CHARACTERISTICS OF THE COHORT OF BAUXITE MINE AND ALUMINA REFINERY WORKERS Men Women Number of employees 5, Industry Mine Refinery 5, Age started, mean (SD) 29.0 (8.5) 29.0 (8.1) Duration of employment, N (%) 4 years 1,137 (19.5) 255 (38.8) 5 9 years 974 (16.7) 181 (27.5) years 2,189 (37.6) 172 (26.2) 20 years 1,528 (26.2) 49 (7.5) Year started, N (%) Before (5.9) 4 (0.6) ,603 (27.5) 93 (14.2) ,700 (46.3) 311 (47.3) ,181 (20.3) 249 (37.9) Person years , ,124 1, ,025 2, ,655 2, ,383 2,594 If the second primary was at a different site then both cancers were counted separately in specific analyses and the person was considered at risk of the second cancer independently of the first cancer. For SIR analyses of a specific site, the calculation of person years for each individual stopped at the time of the first cancer of that type, or at the end of the follow-up period or death. For SIR analyses of all cancers, the calculation of person years for each individual stopped at the end of the follow-up period, or death. We performed a 10 year latency analysis in which job exposures were lagged by 10 years and person-years were accrued excluding the first 10 years since commencement of employment at Alcoa. Ethics approvals Ethics committee approval was obtained from the Monash University Standing Committee on Ethics in Research Involving Humans, the University of Western Australia Human Research Ethics Committee. Ethical clearances were also obtained from each of the state cancer registries and from the AIHW. Results The cohort consisted of 6,485 employees, 5,828 men (89.9%) and 657 women (10.1%) (Table I). The mean age at which employees started work was 29.0 years. Nearly two-thirds of male employees had worked for over 10 years, whereas most females had commenced employment more recently so that there were many fewer person-years in the female employee cohort. There were a total of 11 deaths and 25 cancers in women in the cohort. Because of the small number of deaths and cancers in the women, the rest of the paper refers to only the male members of the cohort. Of the men, 754 had started work in the mines and 5,074 in the refineries. Mortality The mortality from all causes in the male cohort was significantly lower than in the Australian male population (SMR 0.68, 95% CI: ) with 256 observed deaths and 376 expected deaths (Table II). The all-cause cancer mortality was not significantly different from the comparison population. Of the separate types of cancer deaths, the only significant difference was an increased risk of death from pleural mesothelioma (SMR 2.84,
3 884 FRITSCHI ET AL. TABLE II STANDARDISED MORTALITY RATIOS (SMR) AND 95% CONFIDENCE INTERVALS (95% CI) FOR DEATHS TO THE END OF 2002: MALE MINE/REFINERY EMPLOYEES TOTAL NUMBER AND DIVIDED INTO NONEXCLUSIVE GROUPS ACCORDING TO WHETHER THEY EVER WORKED IN PRODUCTION, MAINTENANCE OR OFFICE Cause of death categories All mine/refinery (N 5 5,770) Ever production (N 5 2,680) Ever maintenance (N 5 2,901) Ever office (N 5 1,438) O E* SMR (95% CI) O E SMR (95% CI) O E SMR (95% CI) O E SMR (95% CI) Overall cancer ( ) ( ) ( ) ( ) Colorectal ( ) ( ) ( ) ( ) Prostate ( ) ( ) Bladder ( ) ( ) Kidney ( ) Trachea, bronchus, lung ( ) ( ) ( ) ( ) Pleura, mesothelioma ( ) ( ) ( ) Melanoma ( ) ( ) Overall circulatory ( ) ( ) ( ) ( ) Cardiovascular ( ) ( ) ( ) ( ) Cerebrovascular ( ) ( ) ( ) ( ) Overall respiratory ( ) ( ) Obstructive disease ( ) ( ) Fibrosis Overall injury/trauma ( ) ( ) ( ) ( ) Other or unknown causes ( ) ( ) ( ) ( ) Total ( ) ( ) ( ) ( ) TABLE III STANDARDISED MORTALITY RATIOS (SMR) AND 95% CONFIDENCE INTERVALS (95% CI) FOR DEATHS : MALE MINE/REFINERY EMPLOYEES BY DURATION OF EMPLOYMENT IN PRODUCTION OR MAINTENANCE Cause of death categories Never employed in production or Duration of employment in production or maintenance maintenance 3 months to <10 years years >20 years O E* SMR (95% CI) O E SMR (95% CI) O E SMR (95% CI) O E SMR (95% CI) Overall Cancer ( ) ( ) ( ) ( ) Colorectal ( ) ( ) ( ) Prostate ( ) Bladder ( ) Kidney Trachea, bronchus, lung ( ) ( ) ( ) ( ) Pleura, mesothelioma ( ) Melanoma ( ) Overall circulatory ( ) ( ) ( ) ( ) Cardiovascular ( ) ( ) ( ) ( ) Cerebrovascular ( ) ( ) Overall respiratory ( ) Obstructive disease ( ) Fibrosis Overall injury/trauma ( ) ( ) ( ) Other or unknown causes ( ) ( ) ( ) Total ( ) ( ) ( ) ( )
4 MORTALITY AND CANCER IN BAUXITE AND ALUMINA WORKERS % CI: ). There were significantly decreased risks of death from circulatory and respiratory diseases, injury and other or unknown causes. The patterns seen were similar across the 3 different types of job (office, production and maintenance). The all cause SMRs were similar and significantly low across all duration of employment categories (Table III). There was a significant excess of deaths from pleural cancers in the people who were employed in production or maintenance jobs for between 10 and 20 years (SMR , 95% CI: ). Deaths from lung cancer were also significantly elevated in the group employed for 1 10 years in production or maintenance jobs, but not in higher duration categories. All other results were at or below the expected values. There were no statistically significant trends seen with duration of employment for any of the causes of death. Cancer incidence There were 295 incident cancers in the male cohort members. The incidence of all cancers combined was very similar to the rate in the Australian male population for all mine/refinery employees (Table IV). The cohort showed a statistically significant excess of both melanoma (SIR 1.30, 95% CI: ) and mesothelioma (SIR 3.49, 95% CI: ). Lymphohaematopoietic cancer incidence was significantly lower than that in the general population (SIR 0.50, 95% CI: ). The incidence of mesothelioma was significantly increased over all 3 categories of type of work (Table IV). Melanoma incidence was also increased in all 3 categories, but did not reach statistical significance. Lymphohaematopoietic cancer incidence was lower in all 3 categories but not significantly. The incidence of thyroid/endocrine gland cancer was significantly elevated in those who had ever worked in the office category, with an SIR of 5.35 (95% CI: ). All 6 cancers in this category were cancers of the thyroid. There were no associations between duration of work in maintenance or production and risk of cancer, although numbers were small in many categories (Table V). Trend analysis indicated that the SIRs for all cancers and melanoma showed a significant negative trend with duration of employment in production and/or maintenance jobs (IRR 0.87, 95% CI: 0.78, 0.98 and 0.77, 95% CI: respectively). Although an increased risk of mesothelioma was found for those who had ever worked with the company (Table IV), there was no statistically significant relationship with duration of employment (IRR 0.93, 95% CI: ). There was a significantly increasing trend for brain cancer incidence across the duration categories (IRR 1.81, 95% CI: ); however, the numbers were small, with only 7 brain cancers in total and there were no significant excesses in any of the individual work type or duration categories. Using a 10 year lag for melanoma, the increased risk for the lowest duration group (less than 10 years) was no longer statistically significant although it was still raised. The trend analysis results remained statistically significant (IRR 0.62, 95% CI: , p ). For all cancers however, the trend analysis result was no longer statistically significant when a 10 year lag was used (IRR 0.89, 95% CI: , p ). In total, 9 male members of the refinery and mines cohort had developed mesothelioma up to the end of These cases were investigated further by extracting the most likely cause of the mesothelioma, which was independently assigned by the Western Australian Mesothelioma Registry (WAMR) panel. The WAMR panel had identified clear environmental and/or occupational asbestos exposure and in all but 1 case, this occurred in contexts other than the aluminium industry. For 5 of the cases, the asbestos exposure was related to Wittenoom, a town in rural Western Australia where crocidolite was mined. Discussion The overall mortality in these workers in alumina refineries and bauxite mines was significantly lower than that in the Australian population. Mesothelioma was the only cause of death with an overall increased risk of death. This lower mortality for cardiovascular and respiratory disease is consistent with findings in other industries and is generally attributed to the healthy worker effect", i.e., that people at the time of their employment are generally healthier than the average population with regard to current risk factors for future disease. 17 The healthy worker effect is generally considered to be less strong for cancer than for other disease groups because of our limited ability to predict future risk of cancer. 18 The cancer mortality in these alumina and bauxite workers is within the expected range in comparison to the general population mortality, but is relatively increased compared to the internal all-cause mortality. For example, the risk of death from lung cancer (SMR of 1.12) is not significantly different from the mortality of the general population, but is increased by about 65% compared to the internal all-cause mortality. On the other hand, the fact that we did not see an increase in risk of cancer mortality in the production jobs compared to the office jobs, or in the duration of employment in production jobs argues against a causal effect of work in the aluminium industry although numbers were small in these analyses and must be interpreted cautiously. Incident cancer of all types combined occurred in this cohort of workers at about the same rate as in the general population. There were significant increases in mesothelioma and melanoma incidence and a significant decrease in risk of lymphohaematopoietic cancers. The increased incidence and death from mesothelioma was present across all work categories. Consistent with the poor survival of mesothelioma in general, all but 1 of the mesothelioma cases identified in the cancer registry linkage were also found in the death registry linkage. However, 3 of the 8 deaths in men with mesothelioma were registered with primary cause of death as lung cancer. Notwithstanding the apparent misclassification of a few of the mesothelioma deaths, mesothelioma mortality in this cohort was still in excess compared to the general Australian population. However, asbestos exposure is relatively common in Western Australia and the independent WAMR expert panel determined that environmental or occupational circumstances not associated with employment in the aluminium industry were the most probable sources of asbestos exposure and subsequent development of mesothelioma in all but 1 of the cases. The higher than expected incidence of thyroid cancers in office workers was surprising. Excess thyroid cancers have not been reported in previous aluminium industry studies, 19,20 nor in alumina refineries or mines. There is no known exposure related to office work in this industry, and the finding may be an artefact of the large number of analyses performed in this study. There was a significant increase in the risk of melanoma, which appeared to be predominantly due to an increase in risk in more recent employees. Another Australian study found an increased risk of melanoma in coal miners which was confined to those working in open cut mines. 21 The bauxite workers in our cohort are open cut mine workers. About 40% are heavy equipment operators, 20% are maintenance and the rest operate fixed plants such as crushers. Since the early 1980s, most of the mobile plant operators have been in enclosed cabins, which protect the worker from the sun, prior to that there may have been some sun exposure from open cabins. Some of the maintenance and fixed plant operators may have some sun exposure, especially in earlier years. Smoking is known to be a potential confounder for respiratory cancers. Smoking rates (by age category) in this cohort are similar to those of the Australian population, but smoking behavior may differ between work groups As such, differences in smoking rates between production, maintenance and office workers could at least partially explain the differences in lung cancer rates in the different work types. Unfortunately, smoking information is missing for about a quarter of the cohort. However, we do have good quality smoking data for the survey participants, who contribute about half of the total male cohort, and these data show that a his-
5 886 FRITSCHI ET AL. TABLE IV STANDARDISED INCIDENCE RATIOS (SIR) AND 95% CONFIDENCE INTERVALS (95% CI) FOR CANCERS : MALE MINE/REFINERY EMPLOYEES TOTAL NUMBER AND DIVIDED INTO NON-EXCLUSIVE GROUPS DEPENDING ON WHETHER THEY EVER WORKED IN PRODUCTION, MAINTENANCE OR OFFICE Cancer categories All mine/refinery (n 5 5,828) Ever production (N 5 2,673) Ever maintenance (N 5 2,898) Ever office (N 5 1,437) O E SIR (95% CI) O E SIR (95% CI) O E SIR (95% CI) O E SIR (95% CI) Lip, oral cavity, pharynx ( ) ( ) ( ) ( ) Digestive organs ( ) ( ) ( ) ( ) Stomach ( ) ( ) Colorectal ( ) ( ) ( ) ( ) Respiratory, intrathoracic ( ) ( ) ( ) ( ) Larynx ( ) Trachea, bronchus, lungs ( ) ( ) ( ) ( ) Melanoma ( ) ( ) ( ) ( ) Mesothelioma ( ) ( ) ( ) ( ) Male genital organs ( ) ( ) ( ) ( ) Prostate ( ) ( ) ( ) ( ) Testis ( ) ( ) ( ) Urinary tract ( ) ( ) ( ) ( ) Kidney ( ) ( ) Bladder ( ) ( ) ( ) Brain, CNS ( ) ( ) Thyroid, endocrine ( ) ( ) ( ) Lymphoid, haematopoietic ( ) ( ) ( ) ( ) All Lymphomas ( ) ( ) ( ) Leukaemia ( ) ( ) ( ) Other or unknown causes ( ) ( ) ( ) ( ) All cancer ( ) ( ) ( ) ( ) TABLE V STANDARDISED INCIDENCE RATIOS (SIR) AND 95% CONFIDENCE INTERVALS (95% CI) FOR CANCERS : MALE MINE/REFINERY EMPLOYEES BY DURATION OF EMPLOYMENT IN PRODUCTION OR MAINTENANCE Cancer categories Never employed in production or Duration of employment in production or maintenance maintenance 3 months to <10 years years >20 years O E SIR (95% CI) O E SIR (95% CI) O E SIR (95% CI) O E SIR (95% CI) Lip, oral cavity, pharynx ( ) ( ) ( ) ( ) Digestive organs ( ) ( ) ( ) ( ) Stomach ( ) Colorectal ( ) ( ) ( ) ( ) Respiratory intrathoracic ( ) ( ) ( ) ( ) Melanoma ( ) ( ) ( ) ( ) 10 year lag ( ) ( ) (0.33, 1.65) Mesothelioma ( ) Male genital organs ( ) ( ) ( ) ( ) Prostate ( ) ( ) ( ) ( ) Testis ( ) Urinary tract ( ) ( ) ( ) ( ) Kidney Bladder ( ) Brain, CNS ( ) Lymphoid, haematopoietic ( ) ( ) ( ) All Lymphomas All cancer ( ) ( ) ( ) ( ) 10 year lag ( ) ( ) (0.70, 1.08) ( )
6 MORTALITY AND CANCER IN BAUXITE AND ALUMINA WORKERS 887 tory of ever smoking was highest among production workers (66.7%), followed by maintenance (57.8%) and office workers (50.9%). Indeed the SIRs for lung cancer were highest in the production group (SIR 0.93), however maintenance workers had lower, rather than higher, SIRs for lung cancer than the office workers (SIR 0.52 and 0.73 respectively). Other smoking related conditions should also be considered when discussing the possible role of cigarette smoking in this cohort. Looking at deaths from cardiovascular disease across different work groups shows that, while SMRs in all groups were equal to or less than expected, office workers have a lower SMR than that for the other 2 groups. A similar pattern is seen for deaths from respiratory disease, although the number of deaths is considerably smaller. This suggests that perhaps there is some residual confounding from smoking. The low mortality rates may be partially explained by an underestimate of cases during the matching process. This was confirmed by the finding that 18 deaths identified in a previous mortality search undertaken in 1999 were missed in the current NDI linkage, although apparently the same processes were followed. Certainly fewer potential matches were returned by AIHW compared to the 1999 search for the same time period. Although these earlier deaths were included in the current analysis, there may be some missing deaths from 1996 onwards. The lower matching rates may be due to a more conservative approach to the matching and clerical review process by AIHW and possibly due to recent changes in interpretation of privacy legislation in Australia. 11 In addition, many of the earlier NDI records have age at death instead of date of birth, which makes linkage of cohorts to the NDI problematic. We are more confident of our results for the cancer matches, primarily because of our additional matching with the state registry. The use of both state and national registries proved vital to ensuring as complete ascertainment as possible in the present study. Limiting the matches to only those provided by the NCSCH would have resulted in a considerable underestimate of the number of cancer cases found in the cancer cohort. 11 In conclusion, our study is the first to examine cancer and mortality among workers in bauxite mines and alumina refineries and found little evidence for increased cancer incidence or mortality in this work group. Acknowledgements The authors thank the following members of the Healthwise team: Professor Bill Musk, Professor Michael Abramson, Dr. Martine Dennekamp, Professor Andrew Forbes, Ms. Jill Blackman, Ms. Shelley Fair, Mr. Peter Ittak. References 1. Spinelli J, Demers P, Le N, Friesen M, Lorenzi M, Fang R, Gallagher R. Cancer risk in aluminium reduction plant workers (Canada). Can Causes Cont 2006;17: Romundstad P, Andersen A, Haldorsen T. Cancer incidence among workers in six Norwegian aluminum plants. Scand J Work Environ Health 2000;26: Moulin JJ, Clavel T, Buclez B, Laffitte-Rigaud G. A mortality study among workers in a French aluminium reduction plant. Int Arch Occup Environ Health 2000;73: Benke G, Abramson M, Sim M. Exposures in the alumina and primary aluminium industry: an historical review. Ann Occup Hyg 1998;42: Abbady AG, El-Arabi AM. Naturally occurring radioactive material from the aluminium industry-a case study: the Egyptian Aluminium Company. Nag Hammady Egypt J Radiol Prot 2006;26: de Kom JF, Dissels HM, van der Voet GB, de Wolff FA. Serum aluminium levels of workers in the bauxite mines. J Toxicol Clin Toxicol 1997;35: Townsend MC, Sussman NB, Enterline PE, Morgan WK, Belk HD, Dinman BD. Radiographic abnormalities in relation to total dust exposure at a bauxite refinery and alumina-based chemical products plant. Am Rev Respir Dis 1988;138: Musk AW, de Klerk NH, Beach JR, Fritschi L, Sim MR, Benke G, Abramson M, McNeil JJ. Respiratory symptoms and lung function in alumina refinery employees. Occup Environ Med 2000;57: Beach JR, de Klerk NH, Fritschi L, Sim MR, Musk AW, Benke G, Abramson MJ, McNeil JJ. Respiratory symptoms and lung function in bauxite miners. Int Arch Occup Environ Health 2001;74: Sadkowsky K. Epidemiology research using the National Cancer Statistics Clearing House and the National Death Index databases. Aust Epidemiol 2001;8: Hoving J, Del Monaco A, MacFarlane E, Fritschi L, Benke G, McKenzie D, Sim M. Methodological issues in linking study participants to Australian cancer registries using different methods: lessons from a cohort study. Aust N Z J Public Health 2005;29: Threlfall TJ, Thompson JR, Olsen N. Cancer in Western Australia: incidence and mortality 2003 and mesothelioma Department of Health, Western Australia, Perth. Statistical series number 74, Selvin S. Practical biostatistical methods. Belmont, CA: Duxbury, McCullagh P, Nelder JA. Generalized linear models, 2nd edn. London: Chapman & Hall, Mosteller F, Tukey JW. Data analysis and regression. Reading, MA: Addison-Wesley, Shao J, Tu D. The jackknife and bootstrap. New York: Springer-Verlag, McMichael AJ. Standardized mortality ratios and the healthy worker effect : scratching beneath the surface. J Occup Med 1976;18: Li C-Y, Sung F-C. A review of the healthy worker effect in occupational epidemiology. Occup Med 1999;49: Ronneberg A, Andersen A. Mortality and cancer morbidity in workers from an aluminium smelter with prebaked carbon anodes Part II: cancer morbidity. Occup Environ Med 1995;52: Ronneberg A, Langmark F. Epidemiologic evidence of cancer in aluminum reduction plant workers. Am J Ind Med 1992;22: Brown AM, Christie D, Taylor R, Seccombe MA, Coates MS. The occurrence of cancer in a cohort of New South Wales coal miners. Aust N Z J Public Health 1997;21: Hill DJ. Australian patterns of tobacco smoking in Med J Aust 1988;149: Hill DJ, White VM, Gray NJ. Australian patterns of smoking in Med J Aust 1991;54: Hill DJ, White VM. Australian adult smoking prevalence in Aust J Pub Health 1995;19: Hill DJ, White VM, Scollo MM. Smoking behaviours of Australian adults in 1995: trends and concerns. Med J Aust 1998;168:
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