© 2007 European Society for Medical Oncology
lung cancer |
Lung cancer mortality among silicotic workers in Hong Kong—no evidence for a link
1 Department of Community and Family Medicine, The Chinese University of Hong Kong
2 Pneumoconiosis Clinic, Tuberculosis and Chest Service, Department of Health, Hong Kong SAR, China
* Correspondence to: Dr I. T. S. Yu, The Chinese University of Hong Kong, Department of Community and Family Medicine, 4/F School of Public Health, Prince of Wales Hospital, Shatin, N.T., Hong Kong SAR, China. Tel: +852-2252-8773; Fax: +852-2606-3500; E-mail: iyu{at}cuhk.edu.hk
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Abstract |
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Background: The link between silica dust/silicosis and lung cancer is still very controversial. We examined the relationship between silica dust exposure and/or silicosis and lung cancer in a large cohort of silicotic workers in Hong Kong.
Patients and methods: All workers with silicosis in Hong Kong diagnosed during the period 1981–1998 were followed up till the end of 1999 to ascertain their vital status and causes of death. Standardized mortality ratio (SMR) for lung cancer and other major causes of death were calculated. Axelson's indirect method was used to adjust for smoking effect. Multiple Cox regression models were carried out to examine the exposure–response relationship between silica dust and lung cancer.
Results: About 10% (86) of all 853 deaths were from lung cancer, giving a SMR of 1.69 [95% confidence interval (CI) 1.35–2.09]. Lung cancer SMR for caisson and surface construction workers were 2.39 (95% CI 1.50–3.62) and 1.61 (95% CI 1.21–2.10), respectively, which became 1.56 (95% CI 0.98–2.36) and 1.09 (95% CI 0.82–1.42) after adjusting for smoking. No consistent exposure–response relationship was detected between silica dust or severity of silicosis and lung cancer death.
Conclusion: Our cohort study did not offer positive support to a link between silica or silicosis and lung cancer.
Key words: epidemiology, exposure–response relationship, lung neoplasms, mortality, silicosis, smoking
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introduction |
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TopAbstractintroductionpatients and methodsresultsdiscussionAppendix 1AcknowledgementsReferences |
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Silicosis is a fibrotic disease of the lungs caused by inhalation, retention, and pulmonary reaction to crystalline silica [1]. It has long been recognized that silicosis might cause premature deaths due to secondary pulmonary tuberculosis, chronic obstructive pulmonary disease (COPD), and pulmonary heart disease. In 1997, the International Agency for Research on Cancer (IARC) classified crystalline silica as a human lung carcinogen [2]. However, the IARC Working Group noted that carcinogenicity was not detected in all industrial circumstances studied, and a long debate continued since then [3–6]. In 2001, an IARC multicentre study, pooling 10 cohorts of silica-exposed workers, was published and revealed a weak exposure–response relationship between silica dust and lung cancer [7]. This finding was supported by an updated cohort of North American industrial sand workers [8], but could not be repeated in a more recent retrospective cohort study from seven UK quarries [9].
A recent systematic review published in this journal reanalyzed epidemiological investigations on silica exposure and lung cancer (1996–2005) and concluded that the association with lung cancer was consistent for silicotics, but the data were limited for nonsilicotics and not easily explained for workers with undefined silicosis status [10]. The combined standardized mortality ratio (SMR) for lung cancer from seven cohort studies of silicotics (with 11 subgroups of exposed workers) included in the review was 1.69 [95% confidence interval (CI) 1.32–2.16], but not adjusted for cigarette smoking [10]. Furthermore, workers included in most of the cited cohort studies could have other occupational exposures to carcinogens.
Lung cancer mortality among silicotics has been reported previously in Hong Kong but was probably overestimated because the two previous studies either used only prevalent cases or a convenient sample of silicosis as their study subjects [11, 12]. We report here the mortality experience of a complete cohort of all silicotic workers newly diagnosed in Hong Kong during the period 1981–1998, with minimized selection bias. Moreover, the available detailed cigarette smoking and occupational history of individual workers allowed us to explore the exposure–response relationship between silica dust and lung cancer not reported in the previous two studies. Results from this cohort of silicotic workers could provide further insights to the relationships among silica dust/silicosis, smoking, and lung cancer.
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patients and methods |
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the cohort and follow-up
Details of cohort enumeration and follow-up of this study have been described elsewhere [13, 14]. Briefly, the cohort comprised of all newly diagnosed male cases (incident cases) of silicosis seen at the Pneumoconiosis Clinic of the Tuberculosis and Chest Service of the Department of Health (the only referral center for all patients with pneumoconiosis in Hong Kong) between 1 January 1981 and 31 December 1998, adding
1500 cases to those used in an earlier study [12]. Each worker's demographic information, smoking habit, lifetime occupational history, and medical history were abstracted from the records kept by the pneumoconiosis clinic. The presence of silicosis was defined as profusion category 1/0 or higher following the recommendations of International Labor Organization and the diagnosis of silicosis was made by a panel of doctors including two chest physicians and an occupational physician [1]. Any discrepancy with regard to the classification of small and/or large opacities, if present, was resolved by consensus between the two readers after reviewing the radiographs again. To avoid contamination, cases with a history of cancer or past occupational exposure to asbestos were excluded.
All silicotics were followed up till the end of 1999 to ascertain the vital status through various means. The date of death, death registry entry number, and causes of death as stated in the death certificate were reviewed. The relevant information of the deceased was sent to the Census and Statistics Department to retrieve the codes of the underlying causes of death. The ninth version of the International Classification of Disease was used throughout the study period.
retrospective exposure assessment
Exposure assessment of silica dust in this cohort of silicotic workers has been validated in another paper [14]. In summary, a clear exposure–response relationship was documented between nonmalignant respiratory disease (NMRD) mortality and cumulative dust exposure (CDE) or mean dust concentration (MDC) [14], indicating that our exposure assessments were quite valid.
Subjects of this cohort were categorized into surface construction workers (51%), underground caisson workers (37%), and workers in other dusty occupations (12%) according to their possible exposures to radon and other occupational lung carcinogens [13]. Underground caisson workers were exposed to very high levels of silica dust and radon daughters but less likely exposed to diesel exhaust or oil mists, as the machine compressors (if used) were placed on the surface during caisson digging [15]. Manual excavation of soil and rock using hand shovel, pneumatic drill, and hand wedge was the standard in local caisson practice. Surface construction workers were those who spent their whole career in surface construction work and/or quarrying and were believed to be only exposed to silica dust. Workers who had silica dust exposure but not classifiable into the above two groups were separately grouped. They could have occupational exposures to other lung carcinogens.
statistical analyses
The entry date of follow-up for each subject was defined as the date of diagnosis of silicosis. The exit date represented the date of death, the date of lost-to-follow-up, or the study end date—31 December 1999. SMR was calculated as the ratio of the observed number of deaths to the expected number of deaths for various causes of death. The 95% CI for the SMR was derived assuming a Poisson distribution for the observed numbers [16]. The expected number of deaths for each cause was calculated by multiplying the age-period-specific person-years at risk by the corresponding rates of the Hong Kong male general population. Indirect method proposed by Axelson and Steenland [17] was used to adjust for the potential confounding effect of tobacco smoking. We applied the relative risk (RR) of lung cancer for ever smokers compared with nonsmokers obtained from a local (Hong Kong) study for the indirect adjustment [18]. Smoking prevalence in the male general population in Hong Kong during the corresponding period in the corresponding age group was obtained from regular general household surveys conducted by the Government Census authority [19].
Multiple Cox proportional hazard models were used to fit a possible exposure–response relationship between lung cancer mortality and silica dust exposure. Age at entry into cohort, smoking status, and calendar year of first exposure to silica (an indirect indicator of changes of dust exposure over time) were regarded as potential confounding factors in the multiple regression analyses. As the correlations between silica dust exposures and the confounders in the models were weak (all <0.5), inclusion of age at entry into cohort and other covariates in the models should not have overcontrolled for confounding effects.
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results |
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main characteristics of the cohort
A total of 2925 newly diagnosed cases of silicosis were seen at the pneumoconiosis clinic between 1 January 1981 and 31 December 1998. We excluded 21 female cases, 53 cases with a history of cancer and 62 cases with a history of occupational exposure to asbestos, leaving 2789 subjects for follow-up. They contributed a total of 24992.6 person-years of observations. The vital status was successfully ascertained in 2707 workers (97.1%) of this cohort and 853 known deaths (30.6% of the cohort) had occurred by the end of 1999. Death certificates were obtained for 809 (94.8%) deaths and the causes of death were known for 804 deaths (94.3%). The characteristics of silicotic workers in the three occupational groups are presented in Table 1. In general, caisson workers were more likely to have migrated from Mainland China and were younger at the diagnosis of silicosis and died earlier. They were more likely to smoke but had smoked for a shorter duration. They had a shorter duration of silica dust exposure, a shorter follow-up period, and a shorter latency between first exposure and lung cancer death.
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overall mortality pattern
Table 2 gives the SMRs for various causes of death in the entire cohort. The SMR for all causes was 2.10 (95% CI 1.96–2.25). Mortality from NMRDs, tuberculosis, and pulmonary heart diseases increased substantially accounting for 74.25% of all deaths. There were 185 deaths from malignant neoplasm (21.7%), giving a SMR of 1.23 (95% CI 1.06–1.42). The elevated SMR of all cancers was mainly attributable to the deaths from lung cancer (SMR 1.69, 95% CI 1.35–2.09) and esophageal cancer (SMR 2.22, 95% CI 1.36–3.43).
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The SMRs for major causes of death in three occupational groups are presented in Table 3. Overall, mortality was increased in all three groups, being most pronounced in the caisson workers. Comparing with surface construction workers, underground caisson workers had increased risk of mortality from tuberculosis by 4.36 times, COPD by 2.73 times, and pulmonary heart disease by 2.55 times, while that for lung cancer was only 1.48 times. Workers in other dusty trades had generally lower SMRs than those of the other two occupational subgroups.
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lung cancer mortality
About 10% (86) of all deaths were due to lung cancer in this cohort and all except two lung cancer deaths occurred in smokers. By applying a RR (4.99) of lung cancer for male ever smokers obtained in the local Chinese population [18] (this figure was the best available evidence among the Hong Kong male population and should give the best estimate of the possible magnitude of the confounding effect of smoking) and using Axelson's indirect adjustment method (see Appendix 1 for detailed calculations), the SMR of lung cancer for the entire cohort was reduced to 1.12 (95% CI 0.89–1.38). The smoking-adjusted SMR of lung cancer was 1.56 (95% CI 0.98–2.36) for caisson workers, 1.09 (95% CI 0.82–1.42) for surface construction workers, and 0.81 (95% CI 0.37–1.54) for workers in other dusty trades.
Table 4 shows the SMR of lung cancer by radiological severity of silicosis and indices of silica dust exposure. Lung cancer SMR for workers with large opacities was higher than that for workers with small opacities only. This difference was less marked in surface construction workers. The risk of lung cancer death appeared to increase with the size of large opacities but the numbers in each category were too small for drawing any conclusion. There were no clear trends between lung cancer SMR and the profusion of small opacities, duration of silica dust exposure, CDE, and MDC.
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Results from multiple Cox regression models did not show a clear relationship between various exposure indices (CDE and MDC) and lung cancer mortality after controlling for the confounding effects of age at entry, smoking status, and year of first exposure (Table 5). Age at entry and cigarette smoking were the only significant predictors in all of the models.
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discussion |
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TopAbstractintroductionpatients and methodsresultsdiscussionAppendix 1AcknowledgementsReferences |
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The present historical cohort study, including all incident cases of silicosis in Hong Kong during the period 1981–1998, revealed an increased risk of deaths from all cancers, mainly as result of the excess risks for cancer of the lungs (1.69) and esophagus (2.22). The SMR of lung cancer was higher in the subgroup that had worked in underground caissons (2.39) than surface construction workers (1.61), which became 1.56 and 1.09 after adjusting for smoking. No consistent exposure–response relationship was detected between silica dust or severity of silicosis and lung cancer death. The detailed analysis for esophageal cancer has been reported elsewhere [13].
concomitant occupational exposures to other known lung carcinogens
Our unadjusted findings were in line with a recently published systematic review in this journal and other silicosis studies that reported an association between silicosis and lung cancer before 1997 [10, 20]. However, many of these studies included silicotic workers with mixed occupational exposures, such as workers in the underground mining and metallurgical industries. Confounding effects from concomitant occupational exposures to other lung carcinogens (radon daughters, etc.) in these working environments made the interpretation of the relationship between silicosis and lung cancer difficult. Confounding by exposures to radon was likely in our study because 38% of the cohort had ever worked in underground caissons. It was reported that local underground caissons usually generated up to 71.4 working levels of natural radon [21], but a high level of respirable dust was also detected [15]. The borderline increased risk of lung cancer death (smoking indirectly adjusted SMR = 1.59, 95% CI 0.98–2.36) among caisson workers could be the result of radon exposure or more heavy silica dust exposure. On the other hand, surface construction workers who were only exposed to silica dust did not have an increased risk for lung cancer death after adjusting for smoking (SMR = 1.09, 95% CI 0.82–1.42).
An increased lung cancer mortality has been reported in compensation-based silicosis cohorts with exposure only to silica dust [22–27]. However, many compensation schemes required evidence of respiratory impairment to qualify and this might lead to the selection of silicotic workers with more severe symptoms and lung function impairments into the cohorts [22–24, 26, 27]. If the more severe symptoms and lung function impairments were due to heavier smoking among these subjects, this might artificially magnify the association between silicosis and lung cancer even after making appropriate adjustments for the high prevalence of smoking among silicotic workers. In Hong Kong, compensation would be paid out for all confirmed cases of silicosis even if they had normal lung function and were asymptomatic, thus minimizing the selection bias of our cohort, i.e. we were studying all subjects with silicosis and not only those who were more symptomatic or had poor lung function, which could have resulted from other coexisting lung pathologies. Our surface construction workers who were exposed solely to silica dust had therefore shown a relatively low risk of lung cancer mortality (SMR 1.61) compared with other compensation-based studies despite the relatively high exposures to silica dust (shown in Table 1).
possible confounding by cigarette smoking and socioeconomic status
The increase in lung cancer mortality became very limited in our entire cohort (12%), in particular among surface construction workers (9%) after adjusting for smoking. As no good local data on the risk of lung cancer were available separately for current smokers and ex-smokers, our indirect adjustments were only done with information on ever smokers. Hence, they could only be considered as best estimates of the possible magnitude of the confounding effects due to smoking.
The recent systematic review published in this journal did not adjust the risk estimates for differences in smoking prevalence between the cohorts and reference populations. Higher smoking prevalence in the cohorts of silicotics when compared with the general population would account for a certain proportion of the excess lung cancer risk observed. The exact magnitude of risk attributable to smoking depends on the prevalence of smokers and ex-smokers in the study cohorts and reference populations, as well as the RR for smokers and ex-smokers in those populations. We do not have all the detailed information available for accurate estimation, but the actual risk of lung cancer would be <1.69, as in the case of our cohort. Furthermore, the excess risk of lung cancer could not be attributed to silica dust exposure alone, as most of the reviewed studies were potentially confounded by other concomitant exposures to occupational lung carcinogens. Only two cohorts of silicotic workers exposed solely to silica dust were included in the review with conflicting findings regarding lung cancer risk: no increase risk (SMR = 1.02, 95% CI 0.72–1.40) was found in Poland ceramic and quarry workers [25] but a 2.40-fold increase risk (95% CI 1.37–3.90) was detected in German stone and quarry workers [27]. Nevertheless, lung cancer mortality was probably overestimated in the German cohort because the silicotic workers identified represented a highly selected group: only those with X-ray classification as 
1/1 by the International Labor Organization classification (1980) and also with reduced lung function exceeding at least 20% were studied [27]. Furthermore, no adjusting for smoking was done in calculating the SMR in both Poland and German studies. No associations between indices of silica exposure (duration, average, and cumulative exposure) and lung cancer risk were observed in the German silicotic cohort [27]. Hence, a link between silicosis and lung cancer has not yet been firmly established.
Some studies showed that low socioeconomic status could lead to an inflation of the lung cancer risk by 30%–40%, apart from the effects of smoking [28]. Our silicotic workers had generally lower socioeconomic status in society (>90% were illiterate or had only attended primary schools, compared with 60% in 1976 and 43.3% in 1986 among the Hong Kong male general population) and hence might have a higher risk of lung cancer as a result. The increased lung cancer risk attributable to low socioeconomic status in our cohort could more than offset the 5%–6% underestimation of the lung cancer SMR from possible misclassification of the cause of death and unknown causes of death (see below). The final-adjusted SMR would unlikely deviate much from unity.
misclassification of the underlying cause of death
Misclassification of the underlying cause of death was possible, but should not be serious [29]. Another possible source of bias was from 44 deaths (5.16%) whose underlying causes of death could not be determined. Under the assumption of similar mortality experiences to the rest of the cohort, there would be four to five lung cancer deaths underreported and the SMR of lung cancer would have been underestimated by 5%–6% consequently.
exposure–response relationship with silica dust exposure and radiological classification
Our study did not show any consistent exposure–response relationship between silica dust exposure and lung cancer mortality, which contrasted with some studies that had revealed positive findings [7, 8], but was consistent with many other recently published studies [9, 27]. A limitation of our exposure assessment was that changes of exposure intensity over the years were not considered because of the limited hygiene data available. However, our exposure indices were found to have good exposure–response relationships with mortality from NMRDs [14].
Evidence on exposure–response relationship between radiological severity of silicosis and lung cancer was far from being consistent [22, 30]. We found workers with different profusion categories of small opacities experienced similar risk of lung cancer death but the risk for workers with large opacities was higher. Potential misclassification between large opacities of silicosis and lung cancer could not be ruled out. The large opacities present in the initial chest X-ray could be shadows of early lung cancers, or they could have obscured early cancer lesions, which would otherwise have been excluded from the present study.
In conclusion, results from our cohort study did not offer positive support to a link between silica dust or silicosis and lung cancer after taking into consideration the confounding effects of cigarette smoking, socioeconomic class, and concomitant occupational exposures to other lung carcinogens (by restricting the analysis to the subgroup of surface construction workers with no exposures to other carcinogens). The poor exposure–response relationship with the various exposure indices and the radiological severity also did not offer support for a causal link. The classification of silica dust as a human lung carcinogen might need to be reviewed.
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Appendix 1 |
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TopAbstractintroductionpatients and methodsresultsdiscussionAppendix 1AcknowledgementsReferences |
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Axelson's indirect method used to adjust for the effect of different smoking prevalence between the study cohort and the general population
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Therefore, the relative risk of lung cancer in this cohort due to the higher prevalence of ever smokers compared with the Hong Kong general population was: RR = IS/IG= ((4.59) (I0))/((3.05) (I0)) = 1.51.
The SMR for lung cancer adjusted indirectly for smoking among this silicotic cohort was 1.12 (1.69/1.51 = 1.12), with a 95% CI of 0.89–1.38.
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Acknowledgements |
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TopAbstractintroductionpatients and methodsresultsdiscussionAppendix 1AcknowledgementsReferences |
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The authors would like to thank William Foo of the Hong Kong Cancer Registry, Fung Hong of the Hospital Authority and officers of the Immigration Department and Census and Statistics Department for assisting us in the follow-up of the vital status of our cohort and in supplying us with the information on the underlying causes of death. The authors declare that they have no competing interests. The work described in this paper was substantially supported by a grant from the Research Grants Council of the Hong Kong Special Administrative Region, China (Project No. CUHK4328/99M).
Received for publication September 30, 2006. Revision received December 28, 2006. Accepted for publication February 12, 2007.
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References |
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