Occupational Exposure to Asbestos in Casale Monferrato, Italy

362 Occupational and Environmental Medicine 1995;52:362-367 Pleural malignant mesothelioma and non- Occup Environ Med: first published as 10.1136/oem.52.6.362 on 1 June 1995. Downloaded from occupational exposure to asbestos in Casale Monferrato, Italy

Corrado Magnani, Benedetto Terracini, Cristiana Ivaldi, Mario Botta, Angelo Mancini, Alberto Andrion

Abstract alleged cancer clusters of environmental Objectives-To assess and quantify the (non occupational) origin. occurrence of pleural malignant mesotheliomas in people who neither (Occup Environ Med 1995;52:362-367) experienced occupational exposure to asbestos nor were married to (or known Keywords: pleural malignant mesothelioma; asbestos; to live with) workers exposed to asbestos non-occupational exposure; environmental cancer in the workplace. The study was conducted in the area of the local health The largest Italian factory that produces authority of Casale Monferrato, in north asbestos cement (owned by Eternit) was western Italy, where a large factory that active in the town of Casale Monferrato in produced asbestos cement was active up north western Italy from 1907 to 1985. to 1985. No other major activities related Mortality of workers in the factory has been to asbestos have ever been present in the reported. From 1964 to 1986, 117 workers of area. both sexes died from lung cancer, 89 from Methods-A retrospective survey cover- asbestosis and 43 from pleural malignancies v ing the period 1980 to 1991 identified 126 corresponding expected figures of 42 4, 01, incident pleural malignant mesothe- and 1-3.1 An excess of pleural malignancies liomas histologically diagnosed among (based on six cases) was also found in wives of residents in the local health authority asbestos cement workers although they had (population at the 1981 census 98 000). not been employed in the plant.2 Submission of 83 of 95 cases diagnosed In the 1981 census,3 populations of the during 1980-9 for revision by a panel of administrative area corresponding to the local

five expert pathologists led to the exclu- health authority and of Casale Monferrato http://oem.bmj.com/ sion of 21. The 31 cases diagnosed in (the main town in the authority) were 97 800 1990-1 were not submitted for revision. and 41 700 respectively. The whole area is For 64 ofthe 105 retained cases, informa- away from the hinterland of large industrial tion derived from different sources (ros- cities. Its main productive activities have been ters of the employees in the asbestos agriculture, asbestos cement production, cement factory dated back to 1907, list of cement production, and light mechanical their spouses, clinical records) did not industry (printing machinery, refrigerators, on September 26, 2021 by guest. Protected copyright. suggest occupational or paraoccupational etc). Apart from Eternit, no other asbestos exposure to asbestos. industries or industrial activities likely to Cancer Epidemiology Results-Incidence excludes cases for entail notable use of asbestos, such as chemical Unit, Local Health which there was some suggestion ofoccu- or car industries, were ever present in Casale Authority and University ofTorino, pational or paraoccupational exposure to Monferrato or other towns within the local Torino, Italy asbestos. Incidence of histologically con- health authority. At both the 1961 and 1971 C Magnani firmed malignant mesothelioma among censuses, the textile and chemical industries B Terracini C Ivaldi residents in the local health authority and metal works employed less than 1%, less (annual x 100 000; age adjusted) was 4'2 than 1%, and 10% of the population, Special Project on respec- Asbestos Cement in men and 2-3 in women (based on 26 tively.45 In 1960, in 1970, and in 1980 the M Botta and 18 cases respectively). In both sexes, asbestos cement factory employed 1650, Public Health Unit, rates in 1985-9 were higher than in the 1200, and 800 workers. In 1980 it reported an Local Health previous quinquennium. Corresponding output of 200 000 tonnes of asbestos cement Authority, Casale Monferrato, Italy estimates for 1990-1 (based on unrevised products. A Mancini diagnoses) suggest similar rates in men The Eternit factory was located less than Division of and women. 1000 m from the town centre of Casale Pathological Conclusion-Rate ratios which are four Monferrato. Because of the short distance and Anatomy, City to six times those measured by conven- of the direction of winds, airborne Hospital, Asti, Italy asbestos A Andrion tional Italian cancer registries can hardly contamination was probable within the town. Correspondence to: be totally explained by bias produced by Measurements outside the factory started only Dr Corrado Magnani, lack of recognition of occupational or in 1984: in the town, asbestos concentrations Cancer Epidemiology Unit, Via Santena 7, 10126 paraoccupational exposure. The problem (fibres longer than 5 pm) were in the range of: Torino, Italy. of proving this type of negative data is less than 0-4 (detection limit) to 19- 1 M, with Accepted 30 January 1995 common to other circumstances of mean values ranging from 1 to 11 1 f/l. These Pleural malignant mesothelioma and non-occupational exposure to asbestos in Casale Monferrato, Italy 363

fibre counts refer to SEM analysis with fibre able, and definitely not malignant mesothe- identification by energy dispersive x ray analy- lioma, according to the criteria defined by sis.6 The management has reported that as Jones et al. 4 There was no consensus meeting. Occup Environ Med: first published as 10.1136/oem.52.6.362 on 1 June 1995. Downloaded from late as 1980 crocidolite accounted for 10% of Of the 83 reviewed cases, 62 were retained as the total amount of asbestos that was used.' they were rated either as definite or probable In 1984-9 the local health authority annual malignant mesothelioma by three or more mortality (age adjusted to the 1981 Italian reviewers (60 cases) or as probable or definite population x 100 000) for pleural malig- malignant mesothelioma by two reviewers and nancy was 15-9 among men and 5-7 among possible malignant mesothelioma by all the women, based on 60 and 33 deaths, respec- remaining three (two cases). tively.7 Asbestos (particularly crocidolite and VERIFICATION OF EXPOSURE TO ASBESTOS amosite), erionite, and, to a lesser degree, ion- Patients with malignant mesothelioma who ising radiation are the only known causes of had ever been employed in Eternit or were malignant mesothelioma in humans.8 We have wives of asbestos cement workers were identi- systematically surveyed incident malignant fied in either the roster of employees of the mesotheliomas of the pleura, histologically plant or in the cohort assembled for a previ- diagnosed since 1980, of residents in the local ous study.2 The completeness of the roster health authority, and less than a half of them and the accuracy of the procedure used for had been employed in the asbestos cement identification were validated in two ways. plant.9 Thus it is reasonable to hypothesise Firstly, the roster of employees was that some malignant mesotheliomas might checked against complete occupational histo- have been caused by asbestos pollution in the ries collected for individual workers within an general atmosphere, as reported elsewhere.' o1' ongoing case-control study on pleural malig- To evaluate the soundness of the hypothesis- nant mesothelioma. That study is based on and because histological diagnoses of malig- interviews with the next of kin of residents nant mesothelioma may be problematic"1- from the local health authority who died in findings of a preliminary report have now 1987 to 1990. Among 129 subjects whose been extended in time,9 most cases diagnosed questionnaire was reviewed (blindly for case- in the 1980s have been reviewed by a panel of control status), there was agreement between pathologists and more sensitive criteria have the two sets of data for 128, 12 of whom had been used to identify occupational or paraoc- worked at Eternit and 116 had not. The cupational (domestic, for people who share exception was one person whose employment their household with asbestos cement work- at Eternit was reported in the roster but not in ers) exposure to asbestos. the questionnaire. Secondly, clinical records were available for 116 of 126 subjects diagnosed to have malig- Material and methods nant mesothelioma (before revision). It is gen- COLLECTION OF CASES erally acknowledged that information given on http://oem.bmj.com/ Histological diagnoses of malignant mesothe- clinical documents about occupational anam- liomas of the pleura recorded since 1980 in neses is limited: however, this was not a good residents in the local health authority were reason for not using them as another set of retrospectively identified by a medical doctor data against which completeness of the rosters who perused the registers of the pathology of Eternit employees and their spouses could units in the hospital of Casale Monferrato and be estimated. Out of 31 cases of malignant

six other hospitals (including three teaching mesothelioma included in the roster of Eternit on September 26, 2021 by guest. Protected copyright. hospitals) whose catchment areas include resi- workers, 24 were correctly quoted as such in dents in the local health authority. It is the clinical record and two were reported as believed that retrieval of cases was exhaustive. exposed to asbestos. On the contrary, only No systematic effort has been made to iden- two cases that were reported in the clinical tify cases not diagnosed histologically. These record as employed in Eternit for short peri- have not been considered in the present analy- ods (six and 18 months) did not appear in the ses. The survey identified 126 people with roster of Eternit workers (one was also incident pleural malignant mesothelioma- reported to have been compensated for that is, 95 diagnosed in 1980-9 and 31 in asbestosis). In the computation of rates, these 1990-1. two subjects were considered as occupationally exposed. CONFIRMATION OF THE HISTOLOGICAL Also, eight clinical records mentioned DIAGNOSIS engagement (with no further details) for Eighty three malignant mesotheliomas diag- unspecified periods in occupations that, nosed before 1989 were reviewed by five according to the scientific literature'5 might expert pathologists.'3 The remaining 12 were have entailed exposure to asbestos: two con- excluded because the pathology laboratory struction workers, two car mechanics, two either did not submit any material (four electricians, one worker in cable making, and cases), submitted it too late (two cases), or the one metal worker with exposure to asbestos. case was identified during the update of the Similarly, clinical records reported domestic survey (six cases). Each pathologist indepen- exposure to asbestos for two subjects. All dently reviewed the slides for each case and these cases were considered to have been rated his diagnosis according to an ordinal occupationally or paraoccupationally exposed scale, definite, probable, possible, improb- to asbestos. 364 Magnani, Terracini, Ivaldi, Botta, Mancini, Andrion

Table 1 Confirmed cases ofpleural malignant mesotheliomas diagnosed in 1980-9 among residents in the local health authority ofCasale Monferrato (and in three subareas) for whom there was no suggestion ofoccupational or paraoccupational exposure to asbestos (rates reported by the Cancer Registry of Varese'4 and by the Italian Cancer Occup Environ Med: first published as 10.1136/oem.52.6.362 on 1 June 1995. Downloaded from Registries22 are includedfor comparison: rates are annual x 100 000; age adjusted on the 1981 Italian population over the range 0 +) Local health Other Pool of authority Town of towns within Province Italian ofCasale Casale Adjacent the local of cancer Monferrato Monferrato towns health authority Varese registries Men: n 26 20 4 2 18 159 Rate (95% CI) 4-2 (2-4-6 0) 8-2 (4-3-12-2) 3 4 (0-0-8 0) 0-6 (0-0-1-6) 1-0 () 1-8 Population at 1981 census x 1000 46-7 19-6 8-1 19-0 Women: n 18 16 0 2 7 70 Rate (95% CI) 2 3 (1 1-3 5) 5-1 (2 4-7 8) - 0 7 (00-1 9) 0 3 (-) 06 Population at 1981 census x 1000 51-1 22-1 8-8 20-3

STATISTICAL ANALYSES the Italian population. The range of inci- As only cases diagnosed in 1980-9 were sub- dences measured by the Italian Cancer mitted for diagnostic revision, rates have been Registries (x 100 000 person-years, age computed separately for 1980-9 and for adjusted to the 1981 Italian population) spans 1990-1. The 12 cases that were not traced in from 0-6 to 7-0 among men and 0-2 to 1-7 time for revision were part of the 1980-9 among women. In both sexes, the highest group. Incidence was computed for the entire rates are found in Genova and Trieste: both local health authority and for three subareas: are coastal cities with harbours and dock- the town of Casale Monferrato, the towns yards. adjacent to Casale Monferrato-that is, those sharing boundaries with it-and the other towns of the local health authority. Results Population figures (age and sex specific) were Our survey originally identified 126 residents available for each municipality from the 1981 in the local health authority to whom a malig- census and from estimates for each year up to nant mesothelioma of the pleura was histolog- 1987.16 The 1987 data were used as proxies ically diagnosed in 1980-91. As explained for the population structure for age and sex in above, out of 95 cases diagnosed in 1980-9 the following four years, during which no 23 were not confirmed; rates for this period major changes in total population occurred. include the 62 revised cases and 12 cases that The rates reported in table 1 and elsewhere were not submitted for histological review. Of http://oem.bmj.com/ in the text excluded cases for which occupa- the 21 rejected cases, those that reported tional or paraoccupational exposure to occupational or paraoccupational exposure asbestos was known or suggested from avail- were three out of 10 men and five out of 11 able information-that is, cases mentioned in women. None of the 31 malignant mesothe- table 2. Rates were standardized for age with liomas diagnosed in 1990-1 underwent the 1981 Italian population in the age range review by the panel of expert pathologists.

0 +, broken down in quinquennial age Table 3 shows the distribution of the 105 on September 26, 2021 by guest. Protected copyright. groups. Ninety five per cent confidence inter- cases retained by whether or not occupational vals (95% CIs) of age standardized rates have or paraoccupational exposure to asbestos was been estimated as previously described.'7 reported, sex, age, place of birth, year of diag- Rates have been compared with those pro- nosis, source of the histological specimen, and duced by the Cancer Registry of Varese in histological type. Distribution of these vari- 1983-718 and with a weighted average of rates ables was similar in the two groups: differ- estimated by the nine active Italian Cancer ences in sex distribution and proportion of Registries'9 that serve a total of about 10% of necropsy diagnoses are interesting but not significant. Also not significant was the higher proportion of women originating from outside the local health authority among the non- Table 2 Distribution ofincident pleural mesothelioma (1 980-91) according to evidence exposed cases. The cases not submitted for ofoccupational orparaoccupational exposure to asbestos (see textfor details on assessment ofexposure and definitions) histological review (for the reasons already given) were 15 among those occupationally or Men Women paraoccupationally exposed and among the n (%/o) n (%/1) others. Occupational record in the asbestos cement plant 19 (30 2) 9 (21-4) Wife of asbestos cement worker (no occupation in the same plant) (-) 1 (1-6) Table 2 describes the distribution of the None of the above mentioned but asbestosis or asbestos cases retained by the sources of information cement mentioned in the clinical record 2 (3-2) (-) None of the above mentioned but domestic exposure (-) 2 (3 2) on occupational or paraoccupational exposure mentioned in the clinical record to asbestos. Table 1 reports incidences in None of the above mentioned but occupation reported 7 (11 1) 1 (1-6) in clinical record may have entailed asbestos exposure * 1980-9 computed for the cases with no sug- None of the above mentioned 35 (55-6) 29 (46-0) gestion of such exposure (the last category in Total 63 (-) 42 (-) table 2). Table 1 also reports the incidences *List in materials and methods. from the Italian Cancer Registries. Pleural malignant mesothelioma and non-occupational exposure to asbestos in Casale Monferrato, Italy 365

Table 3 Distribution ofincident pleural mesothelioma in to necropsy (which makes the diagnosis more (1980-91) (see textfor definition ofoccupational or

reliable). On the basis of the available infor- Occup Environ Med: first published as 10.1136/oem.52.6.362 on 1 June 1995. Downloaded from paraoccupational exposure to asbestos) mation, four may have experienced occupa- Occupational orparaoccupational tional exposure to asbestos (in the exposure to asbestos electromechanical industry, construction Yes No work with exposure to asbestos-cement, an n () n (%) electrician, and a worker in the production of Sex: Men 28 (68-3) 35 (54-7) electrical cables). Women 13 (31-7) 29 (45 3) Age: Men: Mean (SD) 63-4 (12-4) 62-5 (13-1) Discussion Range (32-87) (30-81) to investigate the occurrence of Women: The need Mean (SD) 60-8 (8 3) 68-9 (10-8) malignant mesotheliomas attributable to non- Range (49-80) (45-85) to asbestos in the area Place of birth: occupational exposure Men: of Casale Monferrato was prompted by the Local health authority 17 (41-5) 27 (42-2) that the excesses among Elsewhere 11 (26 8) 8 (12-5) consideration Women: asbestos cement workers in Eternit and their Local health authority 10 (24-4) 15 (23-4) partially explain the high Elsewhere 3 (7 3) 14 (21-9) wives could only Period of diagnosis: mortality and incidence. Previous reports on 1980-4 7 (17-1) 13 (20 3) mesotheliomas in people not occu- 1985-9 23 (56-1) 31 (484) malignant 1990-1 11 (26-8) 20 (31-3) pationally exposed to asbestos consisted of Hospital where diagnosed: either reviews of occupational histories in Local 16 (39.0) 28 (43 8) Teaching 21 (51-2) 33 (51-6) necropsy or surgical pathology series or case- Other 4 (9-8) 3 (4-7) control Around the crocidolite mine Source of pathological tissue: studies.'0 Necropsy 8 (19-5) 5 (7 8) of Wittenoom, Western Australia, 24 cases of Surgery 7 (17-1) 13 (20 3) malignant mesothelioma included nine wives Thoracoscopy 15 (36 6) 33 (51-6) Needle biopsy 6 (14-6) 5 (7-8) and nine children of exposed workers among Unspecified biopsy 5 (12-2) 8 (12-5) 4890 people for whom there was no record of Histological type (original diagnosis): Epithelial 13 (31-7) 28 (43 8) employment in the mine." None of these Mixed 9 (22 0) 11 (17-9) studies reported rates or number of person- Fibrosarcomatous 3 (7-3) 5 (7 8) Unspecified 16 (39 0) 20 (31-3) years of observation. Total 41 64 In our study, case identification was satis- factory. We have no suggestions or indications of patients with malignant mesothelioma liv- ing in the local health authority of Casale who Of the 44 cases included in table 1, 13 were diagnosed or treated in hospitals but not (eight men and five women) were diagnosed included in our survey. Had they occurred during 1980-4 and 31 (18 and 13) during rates in the general population and rate ratios v 1985-9. In men, annual age adjusted rates conventional registries would have been http://oem.bmj.com/ x 100 000 (95% CI) were 2-4 (0-6-'43) and underestimated. 5.9 (2 9-9 0) respectively. Estimates for The quality of diagnoses was high. Seventy women were 1-3 (0d1-2-5) and 3-3 (1-3-5-3). five per cent were diagnosed on specimens Of the 31 cases diagnosed in 1990-1 (table obtained at necropsy, surgery, or thora- 3), available data suggested occupational or coscopy. Visual inspection and the possibility paraoccupational exposure to asbestos for 11. of taking multiple biopsies render thora-

The other 20 (nine men and 11 women) coscopy as sensitive and reliable as surgery.20 on September 26, 2021 by guest. Protected copyright. corresponded to annual age adjusted rates Moreover, in another study of ours," diagnos- x 100 000 of 7-4 (2-0-12-9) in men and tic agreement on histological sets obtained 7*1 (2-4-11 7) in women. Corresponding fig- from surgery or at necropsy paralleled that of ures among residents in Casale Monferrato material from thoracoscopies. Further, the were: 15-9 (3-6-28-3) among men and 15-4 panel reviewed routinely stained (haema- (4-9-25-9) among women. As the cases were toxylin and eosin) slides only. Preliminary not submitted for histological revision, these results of an ongoing investigation made on rates are not strictly comparable with those the same material' suggest that systematic shown in table 1. To increase comparability use of immunocytochemistry reduces the pro- we also computed corrected rates, obtained portion of slides rated as possible malignant by applying the corresponding proportion of mesothelioma and increases that of slides cases accepted among those diagnosed in rated as definite or probable malignant 1985-9 and submitted for histological revi- mesothelioma. sion to the sex specific rates. Resulting rates In the interpretation of episodes of local were 5 9 among men and 5-3 among women excesses of disease postulated to be related to in the entire local health authority, and 12-8 the release of a hazardous contaminant from a and 11-5 in the town of Casale. plant into the general environment, a major Over the whole series of 105 retained cases, problem is discriminating between the respec- 10 (eight men and two women) were younger tive roles of occupational and environmental than 50 at diagnosis. Eight of these were resi- (non-occupational) exposure. In the local dent in the town of Casale Monferrato. Out of health authority of Casale Monferrato, results six diagnosed in 1980-9, three were con- of measurements outside the factory are inad- finned after review by the panel. An addi- equate for this purpose so that surrogate data tional one, diagnosed in 1990, was submitted must be used. 366 Magnani, Terracini, Ivaldi, Botta, Mancini, Andrion

The most obvious surrogate is dichoto- Although based on small absolute num-

mous in nature-that is, having or not having bers, rates of malignant mesotheliomas with- Occup Environ Med: first published as 10.1136/oem.52.6.362 on 1 June 1995. Downloaded from experienced exposure to asbestos in the work- out occupational or paraoccupational place. This issue could be resolved in Casale, exposure were higher in the town of Casale because of likely concentration of asbestos Monferrato and decreased with distance from related to work in one firm. The exercise it. Although this observation may reinforce entails all the difficulties of proving a negative. the hypothesis of a point source of asbestos, it A major limitation of our study is that individ- requires further confirmation. ual occupational or paraoccupational expo- As elsewhere, domestic exposure to sure to asbestos was assessed only from asbestos was considered to be relevant as it databases related to work at Eternit, with the was customary for workers to bring home exception of sporadic and debatable informa- their working clothes. In our study, domestic tion retrieved from clinical records. As no exposure was taken into account only for complete anamnesis was collected for the 64 wives of asbestos cement workers or when it cases for whom there was no suggestion of was mentioned in the clinical record. Most occupational or paraoccupational exposure to likely, domestic exposure in childhood has asbestos, opportunities for such exposures been missed in the clinical records. The during life cannot be ruled out. design of our study could not properly con- The main concern is for exposure to sider questions of such detail. More refined asbestos in workplaces other than Eternit and methods for quantifying or excluding occupa- the extent to which occupational exposures tional or paraoccupational exposure are unrelated to the production of asbestos needed to improve our estimates of the risk cement can account for the rate ratios being ensuing from pollution of the general environ- 2-5 to four times greater than those of the ment. An ongoing case-control study started Italian Cancer Registries. In fact, these rate after the present analyses will provide more ratios are underestimated. Conventional adequate estimates of the respective roles of Cancer Registries record cases associated with occupational, environmental, and domestic occupational exposure to asbestos, cases that exposure. lack histological confirmation,22 and those We acknowledge the great contribution of Mrs Marinella that have not had histological slides submitted Nonnato, Dr Giampiero Borgo, and Dr Enzo Borlengo to the collection and quality control of all data and of Mrs Rita for review by expert pathologists. Thus, com- Giacometti who edited the text. We are particularly grateful to pared with rates reported in table 1, rates of the heads and staff of the Pathology Departments and of the Archives of Clinical Records of the Hospitals included in the the conventional cancer registry are inflated. survey. The study was conducted thanks to financial contribu- Most Italian Cancer Registries operate in tions from the International Agency for the Research on Cancer, the Italian Association for Cancer Research (AIRC), industrialised or harbour areas. On the con- the Administration of the local health authority 76, the Italian trary, as well as the production of asbestos Ministry for University and Scientific Research, and the cement, no other industrial activities likely to EEC-Europe against Cancer Program. entail exposure to asbestos have ever been carried out in the local health authority of 1 Magnani C, Terracini B, Bertolone GP, Castagneto B, http://oem.bmj.com/ Cocito V, De Giovanni D, et al. Mortality per tumori e Casale Monferrato. Of concern in this author- altre malattie del sistema respiratorio tra i lavoratori ity are construction works, for which asbestos dell'amianto a Casale Monferrato. Uno studio di coorte storico. 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IntJY Cancer 1993;54:578-8 1. mitted for histological revision, but neither 12 McCaughey WTE, Colby TV, Battifora H, Churg A, Corson JM, Greenberg SD, et al. Diagnosis of diffuse sex nor suggestion of exposure seem to be malignant mesothelioma: experience of a US/Canadian associated with probability of retention or mesothelioma panel. Mod Pathol 199 1;4:342-53. rejection at revision. 13 Andrion A, Magnani C, Betta PG, Donna A, Mollo F, Pleural malignant mesothelioma and non-occupational exposure to asbestos in Casale Monferrato, Italy 367

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