Annals of Oncology Advance Access originally published online on September 13, 2006
Annals of Oncology 2006 17(12):1842-1847; doi:10.1093/annonc/mdl307
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© 2006 European Society for Medical Oncology
epidemiology |
Occupational exposure to diesel exhausts and risk for lung cancer in a population-based case–control study in Italy
1 Unit of Cancer Epidemiology, CeRMS and Centre for Oncologic Prevention, University of Turin, Italy
2 Unit of Occupational Safety and Health, ASUR Marche – Local Department n. 8, Civitanova Marche, Italy
3 Unit of Environmental Cancer Epidemiology, International Agency for Research on Cancer, Lyon, France
* Correspondence to: Dr L. Richiardi, Unit of Cancer Epidemiology, University of Turin, V. Santena 7, 10126, Torino, Italy. Tel: +39-011-6334673; Fax: +39-011-6334664; E-mail: Lorenzo.Richiardi{at}unito.it
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Abstract |
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 Top Abstract introductionpatients and methodsresultsdiscussionappendixAcknowledgementsReferences |
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Background: We studied the effect of exposure to diesel exhausts on lung cancer risk in a population-based case–control study in the city of Turin, Italy.
Patients and methods: Information on occupational histories of 595 incident lung cancer cases diagnosed in 1991–1992 and 845 population controls was obtained. During the interviews, diesel job-specific modules (D-JSMs) were administered whenever subjects had worked in occupations included in the following nine categories: railroad workers, miners, professional drivers and transport conductors, heavy-machine operators, mechanics and testers, filling station attendants, motor-vehicle park attendants, transport equipment operators, and occupations carried out in/near urban roads. All D-JSMs were evaluated for probability, intensity and frequency of exposure.
Results: The odds ratio for ever exposure to diesel exhausts was 1.04 (95% confidence interval 0.79–1.37), after adjusting for age, sex, smoking and having worked in occupations entailing exposure to known lung carcinogens. No association was found with intensity, probability and duration of exposure.
Conclusions: Although misclassification of the exposure may have contributed to the negative results, we did not find an association between occupational exposure to diesel exhausts and lung cancer risk.
Key words: diesel exhausts, lung cancer, occupational exposure, case–control studies, exposure assessment
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introduction |
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TopAbstractintroductionpatients and methodsresultsdiscussionappendixAcknowledgementsReferences |
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Occupational exposure to diesel exhausts is experienced by a large number of workers employed in a number of different occupations [1]. Scientific organizations and government agencies, including the International Agency for Research on Cancer [2], the US Environmental Protection Agency [3] and the National Toxicology Program [4] classify diesel exhausts as a probable human carcinogen. These judgments are based mainly on studies on experimental animals. The epidemiological evidence on humans is considered limited or strong but not sufficient in itself. Several epidemiological studies have been conducted on selected groups of workers likely to be exposed to high levels of diesel exhausts, including railroad workers, truck and bus drivers and garage and maintenance workers [5–7]. An increased risk of lung cancer has been found in a number of these studies, although there were limitations due to confounding by smoking and, especially, difficulties in the exposure assessment and in the estimate of the dose–response relationship. There is thus a need for further epidemiological research, also considering that some reviews have focused on methodological weaknesses or inconsistencies of previous evidence in criticizing the hypothesis of a carcinogenic effect of diesel exhausts [8–10].
Many of the epidemiological studies conducted so far on the effect of occupational exposure to diesel exhausts lack detailed information on the intensity and type of exposure at the individual level. In those studies, the exposure assessment was usually based on a rather crude occupational history, i.e. lists of jobs either obtained by interviews or using registers of occupations. Thus, the same level of exposure was assigned to all workers within the same job title in the same industry, which were considered as ‘homogeneous groups’. In only a few instances, the use of job-exposure matrixes or expert assessments based on more detailed occupational histories permitted the investigators to obtain semi-quantitative indexes of exposure, regardless of the occupational category [6].
We carried out a population-based case–control study to assess lung cancer risk associated with occupational exposure to diesel exhausts, using both lists of jobs and job-specific additional information collected at the individual level.
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patients and methods |
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TopAbstractintroductionpatients and methodsresultsdiscussionappendixAcknowledgementsReferences |
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Data for this study come from a population-based case–control study that we conducted in 1991–1992 among residents in the city of Turin, Italy (about 900 000 inhabitants) [11]. Cases were incident primary lung cancers occurring in individuals aged less than 76. They were identified by weekly monitoring of the hospitals of the city. Both radiologically (5.3%) and histologically or citologically (94.7%) confirmed tumors were considered as eligible. Controls were randomly selected from the Turin population register frequency matching for sex and 5-year age class. Subjects were asked questions on basic demographic details, smoking habits, lifetime occupational history and exposure to passive smoking. For each occupational period lasting at least 6 months, information was obtained on the year of beginning and end as well as the job title and branch of industry. In addition, interviewers administered specific supplementary modules whenever subjects had carried out an occupation, which a priori could entail exposure to diesel exhausts. For this purpose, we developed nine diesel job-specific modules (D-JSMs) for: railroad workers, miners, professional drivers and transport conductors, heavy machine operators, mechanics and testers, filling station attendants, motor-vehicle park attendants, transport equipment operators and occupations carried out in/near urban roads (hereafter referred as ‘urban-road related exposure’), which included several types of workers, such as street vendors, policemen and deliverymen. Questions of each D-JSM aimed to distinguish between exposure to diesel and gasoline engine exhausts and to ascertain the daily frequency and the level of exposure.
All D-JSMs (1096) were evaluated for exposure to diesel exhausts by an industrial hygienist (RC) who assessed the probability, intensity and daily frequency of exposure (Appendix). Most of the D-JSMs (82%) reported quantitative information on the weekly frequency of exposure, which was translated into the categorical variable. When quantitative information was not available, the category of frequency was assigned by the rater on the basis of his own judgment.
By multiplying the daily frequency of exposure, the duration of the occupational period and the intensity of exposure we estimated the cumulative exposure. Weights for intensity were 20, 50, 160 and 300 for categories 1, 2, 3 and 4. They were developed a priori on the basis of the levels of particulate matter less than 2.5 µm in aerodynamic diameter (PM2.5) in environments similar to those described under the definition of our categories of intensity [12–16] (Appendix). For instance, the weight of 20 for category 1 refers to a median annual concentration of PM2.5 of 17.7 µg/m3, measured in cities and small communities in The Netherlands in 1999–2000 [12]. Diesel exhausts are one of the most relevant sources of PM2.5, although there are methodological difficulties in estimating their relative importance in determining the total amount of PM2.5. Depending on the time, place and method used, some apportionment studies revealed that diesel (and gasoline) exhausts account for 10%–50% of the PM10 levels in urban settings [3]. When calculating cumulative indexes, we input missing values of quantitative weekly frequency using the median weekly frequency for each of the four categories of frequency assigned by the industrial hygienist among subjects with data for both the quantitative and the categorical variables.
To validate the assessments, two other industrial hygienists (DM and AO) independently re-evaluated 10% of the D-JSMs. The agreement between the original assessment and the repeated assessments was reasonably good, with weighted kappa values between 0.4 and 0.6 [17].
Information on occupational history also permitted the identification of subjects who worked in occupations entailing exposure to known lung carcinogens. A list of such occupations (list A) has been proposed since 1983 [18] and has been repeatedly updated [19, 20]. We coded job titles and branches of industry according to the International Standard Classification of Occupations (ISCO) [21] and the International Standard Industrial Classification (ISIC) [22] and we used combinations of ISCO–ISIC codes to identify subjects who had worked in list A occupations [23].
Odds ratios (ORs) of lung cancer, and corresponding 95% confidence intervals (CI), were estimated by logistic regression [24] using the software SAS [25]. The last 10 years of exposure were not included in the analyses, as this window of exposure was not considered to be etiologically relevant. In all analyses, subjects having either no D-JSMs or only D-JSMs associated with a probability of exposure of zero were the reference group. We estimated the OR for having at least one D-JSM (ever exposure to diesel exhausts) and for the different types of D-JSM separately. Probability and intensity (using the highest value in the occupational history of each subject) as well as duration (irrespective of probability and intensity levels) and the cumulative exposure were evaluated in separate analyses. Continuous variables (i.e. duration and cumulative exposure) were categorized on the basis of tertiles of their distribution among controls.
Covariates used in the analyses were age (5-year groups), gender, cigarette smoking, exposure to list A occupations and educational level. Variables were treated as shown in Table 1. Adjustment for years of exposure to list A occupations did not change the results more than marginally. Smoking exerted a modest confounding effect with a change of around 10% from the unadjusted estimates to the smoking-adjusted estimates. Never-smokers had smoked less than 400 cigarettes during their life.
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Models were fitted with and without adjustment for educational level and both sets of results were reported in the tables. The rationale for doing so is that although educational level is a risk factor for lung cancer, it is also associated with having worked in occupations entailing exposures to known and unknown lung carcinogens, including diesel exhausts [26]. We reported in the text ORs unadjusted for education.
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results |
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The response rate was 80.5% (642) among cases and 84.8% (860) among controls. After exclusion of subjects with incomplete smoking history, 595 cases (500 men and 95 women) and 845 controls (670 men and 175 women) remained for analysis.
Cases were more frequently smokers, had a lower educational level and had more frequently worked in list A occupations than controls (Table 1). Squamous cell carcinoma was the most frequent histological type.
Overall, 159 cases and 196 controls had been occupationally exposed to diesel exhausts. The OR for lung cancer was 1.04 (95% CI 0.79–1.37) that decreased to 0.95 (95% CI 0.72–1.26) after adjusting for educational level (Table 2). Table 2 also reports the ORs of lung cancer for the occupational categories evaluated in our study. We found an OR of 1.47 (95% CI 0.95–2.26) for urban-road related exposure and an OR of 2.04 (95% CI 0.62–6.75, based on eight exposed cases) for filling-station attendants.
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None of the indicators of exposure based on the industrial hygienist's assessment was associated with lung cancer risk (Table 3), neither in the complete dataset nor in analyses restricted to occupational categories, including at least 15 exposed cases, namely urban-road related exposure, professional drivers and transport equipment operators.
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Increasing the lag-time from the occurrence of the last exposure to lung cancer diagnosis from 10 years to 20 and 30 years did not change risk estimates much. We also conducted some subgroup analyses. First, we restricted analyses to cases with histological or cytological confirmed diagnosis and found an OR of 1.01 (95% CI 0.76–1.33, 149 exposed cases) associated with being exposed to diesel exhausts. Analyses restricted to cases with a squamous cell carcinoma revealed an OR of 1.03 (95% CI 0.76–1.40, 117 exposed cases). Secondly, analyses were restricted to subjects aged 60 or less (232 cases and 272 controls), who were likely to have better recall of their occupational history. Among these subjects, the adjusted OR for exposure to diesel exhausts was 1.19 (95% CI 0.72–1.96, based on 56 exposed cases), with no evidence of increasing risk with intensity and duration.
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discussion |
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We did not observe a clear association between exposure to diesel exhausts and lung cancer risk, neither did we find evidence of a dose–response effect.
A strength of the study is the method of exposure assessment. Several previous investigations identified exposed subjects using job codes with a potential exposure to diesel exhausts (e.g. truck drivers, ISCO code: 9855). This method assumes the same mean exposure level among all subjects who have worked in a specific occupation. Since we administered D-JSMs, we obtained additional information on exposure at the individual level, which was evaluated by an industrial hygienist.
There are, however, several sources of possible misclassification of the exposure, most of them likely to be non-differential with regard to case/control status. First, although we evaluated only occupational exposures, all subjects in the general population have an environmental or para-occupational exposure to diesel exhausts. The lack of information on this source of exposure implies that overall exposure to diesel emissions was misclassified in our study. This is a major problem in the city of Turin, where levels of particulate matter less than 10 µm in aerodynamic diameter (PM10) and of NO2 are among the highest in Europe [27]. In a 7-year period, between 1990 and 1997, estimated median levels of PM10 and NO2 in 24 h were 65 µg/m3 and 76 µg/m3, respectively, which corresponded to the second category of intensity in our study (Appendix). A second source of misclassification is the exposure to diesel exhausts that may have occurred in occupations not included in the nine occupational groups that we evaluated through the D-JSMs. Finally, retrospective collection of occupational histories may always lead to problems of validity and precision. The fact that we found somewhat higher ORs when we restricted the analyses to subjects aged 60 or less may derive from poor recall among older subjects. In addition, the younger subjects of our study (that was performed in 1991–1992) were born in 1930 onwards and have spent their entire working life after the 1950s. Relatively recent industrial processes and circumstances of exposure are better documented and known by the industrial hygienists.
The association between occupational exposure to diesel exhausts and the risk for lung cancer has been investigated in several cohort and case–control studies. A meta-analysis revealed a pooled relative risk of 1.33 (95% CI 1.21–1.46), based on 39 risk estimates, most of them coming from studies of selected categories of workers, rather than studies assessing exposure to diesel exhausts [5, 6].
Studies on truck drivers and railroad workers have provided consistent evidence for an increased lung cancer risk [6, 28–31], although some studies report negative results [11, 32]. For these two occupational categories, pooled relative risks of 1.47 (95% CI 1.33–1.63) and 1.45 (95% CI 1.08–1.93) have been estimated in nine and six studies, respectively [6]. In contrast, small excess risks for lung cancer below 50% or no evidence of association have in general been found in studies that investigated the effect of occupational exposure to diesel exhausts, regardless of the occupational category [30, 33–41], although there is some evidence of a dose–response relationship [30, 35, 36, 40]. The largest previous population-based incident case–control studies report an excess risk of lung cancer for exposure to diesel exhausts between 10% and 40% in Germany [30], Sweden [40] and the US [35]. In the US study, the increased risk was found for lung squamous cell carcinoma [35]. Our estimates, taken with their confidence intervals, do not contrast with these previous studies.
Two main sources of bias, which are not mutually exclusive, may explain the inconsistencies between studies investigating exposure to diesel exhausts and studies on truck drivers and railroad workers: (1) non-differential misclassification of the exposure biasing risk estimates toward the null in the former studies; and (2) residual confounding resulting in a bias upwards in the latter studies. In two previous US studies, the Railroad Worker study [42, 43] and the Teamsters Union Trucking Industry study [44], industrial hygiene surveys have been carried out to associate semi-quantitative categories of dose of exposure to diesel exhausts with specific job titles. In the Railroad Worker study, the concentration of respirable particulate was measured at the beginning of the 1980s for around 530 workers employed in the railroad industry to support that job titles a priori considered to entail a higher exposure were in fact exposed to higher levels of diesel exhausts [15]. The cohort of railroad workers has been followed-up from 1959 to 1996, revealing an overall 40% excess risk of lung cancer mortality among exposed workers compared with those unexposed [31]. However, the risk did not increase with increasing years of work. The Teamsters Union Trucking Industry study is a mortality case–control study of around 1000 cases and controls selected from union members of the truck industry between 1982 and 1983 [44]. Hygiene surveys of exposure to elemental carbon, a proxy for diesel exhausts, were conducted in 1990 to measure the levels of exposure for different job titles (e.g. mechanics and local drivers), circumstances of exposure (e.g. highways) and weather conditions [45]. The highest exposure levels were found for the mechanics who also had the highest risk of lung cancer (OR = 1.69), whereas the lowest level of exposure to elemental carbon was found among dock workers, whose OR in the case–control study was 0.93 [44, 45]. As suggested by a review from the Health Effects Institute, although these studies indicate that job titles are proxies of the exposure to diesel exhausts and that the use of hygiene surveys improves the exposure assessment, strong assumptions should be made to reconstruct the individual historical exposure [46]. Given the population-based design of our study, we used a different approach, as the historical exposure was assessed by an industrial hygienist in the absence of quantitative data.
Our findings on urban-road related exposure give some support to an association between exposure to diesel exhausts and lung cancer risk, although there was no dose–response relationship. This circumstance of exposure occurs in a heterogeneous group of workers, whose main source of exposure to diesel exhausts is urban traffic. In addition, we found an increased risk, albeit statistically not significant, among filling-station attendants, who are exposed, among other pollutants, to diesel emissions from urban traffic.
In conclusion, although we found a small excess risk, non-statistically significant, among workers exposed to urban traffic emissions, our study did not support previous evidence of an association between occupational exposure to diesel exhausts and risk for lung cancer.
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appendix |
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Definition of categories of intensity, probability and frequency used by the industrial hygienist, Turin, Italy, 1991–1992
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a See Le Tertre et al. [47] for levels of PM10 in Milan and Rome, compared with other European cities.
b NA, not applicable.
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Acknowledgements |
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This study was partially supported by the Italian Association for Cancer Research (AIRC); MIUR; the Regione Piemonte-Ricerca Finalizzata; the Compagnia San Paolo/FIRMS, Special Project Oncology; the ‘Scuola Elementare D'Azeglio, Classe IV C’, Torino, in memory of Pierluigi Rampa. We thank Professor Neil Pearce for his useful comments on the manuscript.
Received for publication May 8, 2006. Revision received July 13, 2006. Accepted for publication July 18, 2006.
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