Silicosis and Lung Function Decrements among Female Ceramic Workers in Italy
Francesco Forastiere1,
David F. Goldsmith2,
Alessandra Sperati1,
Elisabetta Rapiti1,
Maria Miceli1,
Fulvio Cavariani3 and
Carlo A. Perucci1
1 Department of Epidemiology, Health Authority Rome E, Rome, Italy.
2 Department of Environmental and Occupational Health, George Washington University, Washington, DC.
3 Local Health Authority, Civitacastellana, Viterbo, Italy.
Received for publication August 17, 1998; accepted for publication June 19, 2002.
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ABSTRACT
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It is well known that male ceramic workers have elevated risks of chronic silicosis. The objective of this study was to assess whether female ceramic workers also have an increased risk of silicosis and whether these women have decreased lung function related to silica exposure. Ceramic workers from Civitacastellana, Italy, were enrolled in health surveillance during the 1970s. A total of 642 women were under surveillance; a respiratory monitoring program was conducted from 1974 to 1987, with follow-up through 1991 that included annual chest radiography and measurement of lung function. Radiography findings were defined as silicosis if the chest films were
1/0 with small, rounded opacities. Multiple linear regression models for repeated measures (generalized estimating equations) were run to evaluate associations of forced vital capacity (FVC) and forced expiratory volume in 1 second (FEV1) with years of exposure and radiograph opacities. Nine cases of silicosis were identified on the basis of radiographic evidence. Silicosis risk was not associated with smoking but was related to employment before 1970 and demonstrated a dose-response gradient for years of exposure. FVC and FEV1 both showed significant (p < 0.05) associations with duration of exposure and with positive radiography findings. The results for female ceramic workers are consistent with those for male employees regarding exposure to fibrogenic dusts.
ceramics; lung diseases; pulmonary fibrosis; radiography; silicosis; smoking; women; x-rays
Abbreviations:
Abbreviations: FEV1, forced expiratory volume in 1 second; FVC, forced vital capacity.
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INTRODUCTION
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The epidemiologic and clinical aspects of silicosis and the pulmonary disease risks for male dusty-trades workers exposed to silica, including during ceramic production, have been well documented (13). Although there are sizable numbers of female workers in silica-exposed occupations such as dental laboratory technicians, artists, agriculture, and ceramics and in more strenuous jobs such as mining and foundry work, pulmonary disease risks for female workers generally have not been characterized. We found few epidemiologic studies on respiratory diseases in silica-exposed female workers. Some studies have evaluated gender differences regarding silicosis (46), with no firm results. One mortality study of female mine workers exposed to silica found a standardized mortality ratio of 1.38 for nonmalignant respiratory disease (7); a recent death certificate study in the United States detected an extremely high proportional mortality ratio for pneumoconiosis (13.6) for women working in occupations or industries in which exposure to silica was possible, whereas the corresponding proportional mortality ratio for men was 3.8 (8). Two investigations were found regarding lung function. A study comparing workers with silicosis (men and women) with healthy controls found that positive radiography readings were associated with a faster decline in lung function (9); a second study of female pottery workers demonstrated lower forced expiratory volume in 1 second (FEV1) and forced vital capacity (FVC) when these women were compared with unexposed controls (10).
Ceramic workers from about 100 plants in the community of Civitacastellana in central Italy (north of Rome, Lazio region) have been surveyed since 1974 by a local health unit for occupational diseases, and male workers have been studied for various conditions, including lung cancer, silicosis, and end-stage renal disease, over the past 15 years (1113). The objective of this research has been to evaluate the risk of respiratory diseases, including radiographically diagnosed silicosis and impaired lung function, for women employed in the ceramic industry.
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MATERIALS AND METHODS
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The environmental and radiologic surveillance program in Civitacastellana has been described previously (12). The local industry in Civitacastellana produces both sanitary ware (sinks and toilet bowls) and crockery dishware (ceramic dishes manufactured from porous, opaque clay), and dust levels have usually been higher in the sanitary ware process, especially in the molding, furnace, firing, and reclaim jobs. Of approximately 3,700 workers in the ceramic industry under surveillance in 19741987 with annual, standard posteroanterior chest radiographs and medical examinations, 814 women were initially investigated with a standard posteroanterior chest radiograph.
All chest films were read by a radiologist from the local health authority by using standardized International Labor Office criteria (14, 15). Each radiograph was evaluated for profusion level and for size and type of opacity. Two subjects had a baseline 0/1 reading; for the other 812 women, the profusion level was 0/0 at the initial radiography examination. The incidence of silicosis was evaluated among 642 women who had at least one subsequent chest radiograph before December 1991. The workers were followed for an average of 6.7 years (standard deviation, 4.1) and had an average of 5.9 (standard deviation, 3.0) chest radiographs. The excluded 172 women for whom there were no follow-up data were younger and worked for a shorter period of time in the ceramic industry than the study group did, and they were likely to have left the industry soon after their first examination. It is unlikely that data on these women biased our findings because these workers probably left the industry for non-health-related reasons. We used a radiographic reading of
1/0 (rounded opacities) to define workers with silicosis. On the basis of accurate autopsy data, it has been shown that the sensitivity for such a cutoff point is higher than that obtained by using a reading of 1/1, while the specificity is still very high (16). The initial date on which the category 1/0 reading was identified was considered the time of diagnosis. We sought the files of women with positive radiographic changes during follow-up to reevaluate their diagnoses. One B-reader certified by the National Institute for Occupational Safety and Health (Cincinnati, Ohio), blinded with regard to exposure history, reread the initial radiographs to validate the diagnoses.
For the present analysis, we considered existing work histories on file to characterize subjects primary work area (sanitary ware or crockery). The term "mixed" was applied when subjects had changed from one sector of the industry to another or when no specific work area could be determined. The following additional variables were available for analysis: year of first employment in the ceramic industry, duration of employment, smoking status, and number of cigarettes smoked per day reported during the initial medical visit. Cumulative incidence of radiologic changes was evaluated in relation to type of job, period of first exposure, duration of exposure, and smoking. Odds ratios and 95 percent confidence intervals for the association with silicosis were derived from a logistic model.
As part of the surveillance program, standardized lung function tests were performed, beginning in 1983, by using a pneumotachograph; each subject was seated while wearing a nose clip. The best FEV1 and FVC readings from any acceptable curve were recorded. An acceptable FVC reading was within 5 percent or 200 ml of other measurements (whichever was less) and was judged by a trained technician to be an adequate maneuver. The original spirometric tracings were revised according to American Thoracic Society criteria (17), and an acceptable test was obtained for 475 subjects (74.0 percent of the whole cohort). A subsample of 380 women underwent an additional lung function examination after an average of 4.7 years (standard deviation, 2.1). To evaluate the longitudinal association of duration of exposure and presence of silicosis with lung function (FVC, FEV1), we used the marginal model for repeated measures. The generalized estimating equation method was used to estimate the regression coefficients (mean change in lung function) and the within-person correlation matrix (18). In this model, the marginal expectation of pulmonary performance is modeled as a function of explanatory variables while considering the within-person correlation. The marginal expectation is intended as the average lung function level for the specific subpopulations. Adjustments were made for height, age, ceramic process, and smoking status. We found that the relation with age was not linear and that inclusion of an age-squared term better fitted the data. We also considered the daily number of cigarettes smoked by smokers, as reported at the initial visit, as an additional adjustment variable. The analysis was conducted by using STATA software (19).
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RESULTS
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Table 1 provides descriptive information on the 642 women enrolled in the study for whom there were no radiographic signs of silicosis at the initial visit. Most members of this cohort were young; 547 were less than 45 years of age at the time of the initial visit. A total of 563 women began work between 1970 and 1987, and very few subjects (n = 38) worked exclusively in sanitary ware production. At enrollment, workers had an average duration of exposure of 4.7 years. About half of the cohort members (49.5 percent) were current or former smokers at the time of the initial visit. Table 1 also reports the baseline characteristics of the 475 women who underwent an initial assessment of lung function as well as the features of those 380 workers for whom a subsequent lung function test was available. Compared with nonparticipants, women for whom lung function data were available (and also those with a lung function follow-up) were slightly older at baseline, were more likely to be employed in the crockery process, had a slightly longer duration of employment, and were more likely to be smokers. Lung function data at baseline were very similar for those with a follow-up and those who underwent an initial assessment only.
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TABLE 1. Baseline characteristics of the women enrolled in the study of silicosis and lung function decrements, of the sample with initial lung function data, and of the sample with lung function follow-up data, Lazio, Italy, 19741991
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Of the 642 female workers, nine had a radiologic finding of 1/0 or higher (1.4 percent), including four whose films showed 1/1 profusion (table 2). We were able to locate six of nine original radiographs (those for three women were not in their files), and all six were confirmed as showing either 1/0 or 1/1 abnormalities by a B-reader. The radiographs of two cases (7 and 8) were scored 1/1 during the revision instead of 1/0. Age at diagnosis ranged from 40 to 55 years. Three of the nine cases began working in ceramics before age 20 years. It is noteworthy that all but one (case 4) of the remaining silicosis cases first joined the ceramic industry before 1970, when dust control was beginning to be improved. All subjects but one (case 9) were employed in either mixed or crockery work areas; two had the specific job of molder, and four worked in biscuit firing preparation. The cases were exposed for different lengths of time that ranged from 11 to 28 years. Six cases were nonsmokers, two were current smokers, and one was a former smoker.
Table 3 shows the cumulative incidence of silicosis and the odds ratios obtained from a logistic model. Since year of employment and duration of employment were clearly collinear, two logistic models were fitted and each of these two variables was entered in turn. Age was a predictor of silicosis: the odds ratios rose from 1.0 for women aged 1744 years to 3.1 for those aged 4554 years to 8.0 for those older than age 55 years. Work area showed no apparent trends, whereas starting employment before 1970 was a strong risk factor for silicosis among these women; the adjusted odds ratio was 57.9. Odds ratios for number of years of exposure showed a clear dose-response relation. They ranged from 2.0 (1519 years) to 17.8 (2024 years) to 26.0 (
25 years) when women with less than 15 years of employment were considered the reference (odds ratio = 1.0); the latter two odds ratios were statistically significant. Among these women, smoking was not a risk factor for silicosis. When compared with nonsmokers, smokers had an odds ratio of 0.6.
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TABLE 3. Cumulative incidence of radiologic signs of silicosis and association with various factors, Lazio, Italy, 19741991
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Table 4 provides the results of the FVC and FEV1 analyses that included 475 women, of whom 380 had two lung function measurements. Both FVC and FEV1 were significantly associated (p < 0.05) with duration of employment. The linear effect was a 9.2 ml (95 percent confidence interval: 15, 3) change in FVC and a 5.7 ml (95 percent confidence interval: 12, 0) change in FEV1 for each year spent in the ceramic industry. A positive radiographic finding (of the nine silicosis cases, eight had at least one lung function test and seven had repeated tests) was also associated with a decline in lung function, after adjustment for duration of exposure. When number of cigarettes smoked and radiographic results were included in the multivariate models, no relevant changes in the effect of duration of exposure were detected (data not shown).
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TABLE 4. Association between years of employment in the ceramic industry, radiologic signs of silicosis, and lung function, Lazio, Italy, 19741991*
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DISCUSSION
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Crystalline silica dust levels vary in ceramics processing because the material blend must be wet so the uncured pieces can be formed. Silica levels are higher during molding, after firing, when higher levels of cristobalite are formed in some mixing jobs, and when pieces that fail inspection are handled (12). We think that this is the first study of the respiratory health effects of silica exposure derived from surveillance data among female workers. Our findings suggest that dust exposure is correlated with positive radiographic results for silicosis; smoking appears to have played no significant role in the occurrence of silicosis in this cohort of women. Results suggest that risks of pulmonary health effects were related to past silica exposures, before dust controls were introduced in 1970. In addition, exposure to silica is associated with a decline in lung function.
We recognize that our study has limitations, especially because we studied a relatively young group of women. Information on past industrial hygiene levels was not available, so individual cumulative silica exposure levels could not be evaluated. We can estimate that, at least in sanitary ware work, levels of respirable silica during the 1960s were about three- to fivefold higher than the current 0.1 mg/m3 standard, whereas they approximately met the current standard in the crockery process (12). Because we considered surveillance data, we initially relied on only one radiograph reader to determine silicosis status; therefore, it is likely that silicosis status was misclassified (16). However, when read by a B-reader who had no knowledge of exposure status, six of six of the recovered radiographs demonstrated concordance with the initial diagnosis. We might have overestimated the risk because we considered minimal signs (1/0) as positive, but autopsy data suggest that more stringent criteria (1/1 or higher) have a very low sensitivity (16). All workers who retired or left the industry were not considered in our analysis, and it is possible that silicosis in these workers could have been undetected. Finally, when lung function decrements were evaluated, the possibility of residual confounding by smoking cannot be ruled out since smoking status and not duration of smoking was considered. However, when number of cigarettes smoked was introduced in the multivariate models, no relevant changes in the effect of duration of exposure were detected. Study limitations notwithstanding, this research is the first known attempt at a longitudinal evaluation of respiratory health among a cohort of women in a comprehensive surveillance project.
These results indicate that there is a risk of silicosis for women, and, in this context, they parallel the long-held view of the silicosis risk for men. The steepness of the association between duration of exposure and silicosis was basically the same for women in this study and for men from the same industry (12). However, the cumulative risk (for 1/1) reached 20.4 percent for men after 20 years of exposure (mainly in sanitary ware production), whereas the cumulative risk (for 1/0) in this study was 11.5 percent for women after 25 years of exposure (mainly in crockery production). A lower level of respirable silica in the crockery process, as well as employment in the later period among women, could have been responsible for the differences. A study in Sweden found a more pronounced progression of silicosis among women when compared with men (4). However, although there are examples of other exposures (20, 21) for which a larger effect on pulmonary diseases has been detected in women in comparison to men, we do not see a biologic basis for anticipating that gender would modify response to silica. Epidemiologic studies on effect modification by gender will eventually require large numbers and very well characterized occupational histories. There was no apparent association of silicosis with smoking in our data, whereas an association was found for men (12). However, there were only two current and one former smoker in the group of nine silicosis cases, so power to detect a difference was limited. To be able to compare future research findings, additional active surveillance of female ceramic workers is clearly needed. Surveillance should include cumulative exposure information, respiratory symptom surveys, and serial lung function testing and chest radiography. Additional assessments of autoimmune diseases (22) and renal injury (13) appear to be warranted in light of the new studies linking these conditions to occupational silica exposures (23).
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ACKNOWLEDGMENTS
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Supported by project 639A of the Public Health Institute, Berkeley, California. Dr. Forastiere was partially supported by the International Union against Cancer (UICC) Yamagiwa-Yoshida Grant while on sabbatical in Berkeley.
The authors thank Dr. Antonio Di Pietro for data collection and revision of lung function tests, Dr. Giovanna Maseri for rereading the original radiographs, and Patrizia Compagnucci for editing the manuscript. They also thank Faye Rice for the bibliographic review.
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NOTES
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Reprint requests to Dr. Francesco Forastiere, Department of Epidemiology, Health Authority Rome E, Via Santa Costanza 53, 00198 Rome, Italy (e-mail: epiamb1{at}asplazio.it). 
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