Malignant Mesotheliomas in Textile Rag Sorters

Ann. Occup. Hyg., 2015, Vol. 59, No. 5, 547–553
doi:10.1093/annhyg/meu114
Advance Access publication 19 February 2015
Malignant Mesotheliomas in Textile Rag Sorters
Elisabetta Chellini1*, Gianrocco Martino2, Annalisa Grillo3,
Aldo Fedi3, Andrea Martini1, Laura Indiani2 and Luigi Mauro3
1.Unit of Environmental and Occupational Epidemiology, Cancer Prevention and Research Institute, Firenze I-50141, Italy;
2.Specialization School in Hygiene and Public Health, University of Florence, Florence I-50139, Italy;
3.Occupational Health Service, Local Health Authority of Prato, Prato I-59100, Italy
*Author to whom correspondence should be addressed. Tel: +39-055-7972558; fax: +39-055-7972588; e-mail: e.chellini@ispo.toscana.it
Submitted 28 February 2014; revised 1 December 2014; revised version accepted 2 December 2014.
A B ST R A CT
Objectives: To analyse the asbestos exposure characteristics and mesothelioma trend in textile workers operating in the larger Tuscan textile industrial province of Prato between 1988 and 2012.
Methods: All cases of textile workers recorded by the Tuscan mesothelioma register are considered.
The demographic and clinical characteristics and asbestos exposure of cases working in the province of
Prato are examined. Crude incidence rates between 1988 and 2012 and their 95% confidence intervals
(CI) are calculated in rag sorters and other textile workers. The trends of standardized rates are also
evaluated, as well as the sources of occupational asbestos exposure from occupational histories of cases
affected by other asbestos-related diseases in rag sorters.
Results: One hundred and seventy-two malignant mesotheliomas (MMs) have been diagnosed in
textile workers in Tuscany. Among these, 46.5% were residents in the province of Prato at the time of
diagnosis, half of whom working as rag sorters. All rag sorters with MM are classified as occupationally
asbestos exposed, while 71.7% are other textile workers exposed to asbestos. The estimated crude incidence rate in rag sorters in Prato ranges from 74.1 × 100 000 (95% CI: 52.5–101.8) to 166.8 × 100 000
(95% CI: 118.1–229.0). The standardized rates in Prato rag sorters appeared higher throughout the
1990s while in other Prato textile workers the rates increased later on, at the very end of the 1990s.
Another 40 cases of asbestos-related diseases in rag sorters were also collected.
Conclusions: A very high incidence of MMs was observed in textile workers in Prato, especially among
rag sorters. This result, together with the high number of other asbestos-related diseases in rag sorters,
strongly supports the hypothesis of diffuse asbestos exposure in rag sorting, in the absence of any other
relevant aetiological factor for malignant mesothelioma.
K E Y W O R D S : asbestos; asbestos occupational exposure; malignant mesothelioma; textile rag
sorters; textile workers
I N T RO D U CT I O N
Malignant mesothelioma (MM) is a rare cancer, the
pathogenesis of which is closely related to exposure to
asbestos (IARC, 2012), detectable in around 70–90%
of male cases and less frequently in female cases.
Other natural mineral fibres, such as erionite (Baris
and Grandjean, 2006), vermiculite (Whitehouse et al.,
2008), and fluoro-edenite (Bruno et al., 2006), as well
as artificial fibres (IARC, 2002) and high aspect ratio
nanomaterials (Donaldson et al., 2011; Fubini et al.,
© The Author 2015. Published by Oxford University Press on behalf of the British Occupational Hygiene Society.
• 547
548 • Malignant mesotheliomas
2011) have been suggested to play an aetiological
role on MM occurrence. In Italy, the geographical and
temporal differences in disease incidence are basically
due to past occupational and environmental asbestos
uses and exposure (Facchini et al., 1986; Mastrantonio
et al., 2002; Marinaccio et al., 2005; Marinaccio et al.,
2008).
During the 1980s, a survey of MM conducted in
Tuscany showed for the first time a large amount of
pleural MMs in textile industry workers in the province of Prato (22 cases out of 61 registered MMs),
16 cases of which were diagnosed in rag sorters (Paci
et al., 1987, 1991). Following, the Tuscan mesothelioma register was created (Buiatti and Chellini, 1989;
Chellini et al., 1992), even before enforcement of the
national laws on preventive asbestos intervention
(Legislative Decree no. 277/1991 and Decree of the
President of the Council of Ministers no. 308/2002)
that provided for the establishment of a national mesothelioma register called RENAM. At that time, the
Tuscan register was also incorporated, as an Operating
Regional Centre (COR), into the national epidemiological surveillance system RENAM (Nesti et al.,
2001, 2004).
In the mid 1980s, following the unexpected
detection of MMs among workers in Prato, the
Occupational Health Service (OHS) of the Local
Health Authority of Prato performed an industrial
hygiene survey to evaluate the presence of asbestos in
rag sorting workplaces. A long and widespread practice of recycling sacks made of jute and polypropylene
coming from Italian asbestos cement factories, was
registered (Monechi et al., 1987; Quinn et al., 1987).
Other sources of asbestos exposure for rag sorters
were also suggested during the tearing up of military
uniforms containing asbestos in the years immediately
after the second world war, and for other textile workers during the 1960s, when 8% of asbestos was added
to wool fabrics intended for the US market in order to
avoid the high import taxes for pure wool in force in
that country (Quinn et al., 1987).
From that time on, many other cases were recorded
in textile rag sorters in Prato by the Tuscan mesothelioma COR, a separate registry from the population
cancer registry, which uses standardized procedures
to ascertain Tuscan mesothelioma cases and their
occupational and non-occupational asbestos exposure
(Chellini et al., 2013).
The objective of this study was to examine the
characteristics and trends of MMs, diagnosed in the
1988–2012 period, in Tuscan textile workers, especially those operating in the industrial province of
Prato, and to further evaluate their possible past asbestos exposure.
The textile industry in Prato, mainly involved in the
production of reprocessed wool, was very prosperous
up to the last two decades when the national economic
crisis also affected the textile sector, changing the local
industrial scenario, despite the counter effect due to
the increasing number of migrants from China working in this industrial sector, although mainly engaged
in clothing activities (Berti et al., 2013). In the past
rags arrived in Prato from national and international
rag markets for being recycled. These included clippings from package industries, waste materials from
textile industries, and second-hand clothes and fabrics. The reprocessed wool was produced by breaking
down used wool garments and re-forming the wool to
make yarn for re-weaving. The first step in reprocessed
wool making is called rag sorting, characterized by
two different phases: an initial sorting phase which
includes hand tearing out of linings, fur coat collars,
and other unusable accessories, and a second one in
which materials are classified by type of fabric, conservation level, and colour. The dispersion of inhalable
fibres, including asbestos, when present, would have
been possible, especially during the first sorting phase.
M ET H O D S
All MM cases diagnosed between 1988 and 2012 in
textile workers, recorded by the Tuscan mesothelioma COR, are considered. For each case working
in the Prato textile industries, their demographic
information (gender, age at diagnosis and residence),
clinical information (diagnostic procedure, cancer
topography, histotype, and survival), employment
history (job, company location, and work period) and
asbestos exposure grading were extracted from the
COR database. All data are collected and registered
by the Tuscan mesothelioma COR using standardized national procedures (Nesti et al., 2003): personal
occupational and lifestyle histories are detected by
means of a specific national questionnaire by trained
interviewers; if the case is deceased or not able to
carry out an interview, a next-of-kin or a workmate
is interviewed; asbestos exposure is evaluated and
Malignant mesotheliomas • 549
classified by industrial hygienists and occupational
health physicians.
For each case, a latency period was calculated as
the difference between the beginning of supposed
exposure (first year of job activity) and year of MM
diagnosis.
The distribution of demographic and clinical characteristics and asbestos exposure in rag sorters and
other textile workers was examined and compared
using the Chi-Square (χ2) statistical significance test
(<0.05 for statistically significant differences) or
Fisher’s exact test.
Crude incidence rates from 1988 to 2012 and their
95% confidence intervals (CI) were calculated for rag
sorters and other textile workers.
The number of textile workers in the province of
Prato, both rag sorters and other textile workers, at risk
of having an MM diagnosis in the 1988–2012 period
was assumed as stable throughout the whole period,
considering that those at risk of MM had worked from
the 1950s to the 1980s (with mesothelioma latency
lasting about 30–40 years), a prosperous economic
period for textile industry in Prato, and experienced
the same mortality pattern as the Prato population in
the following years.
In the absence of any official data, the number of
rag sorters in Prato at risk of MM in the observation
period was estimated on the assumption that there
was a stable yearly amount of processed rags (those
imported in 1985 equal to 94 292 tons), and a stable
daily work time necessary to pick out an amount of
rags ranging between 200 and 450 kg per day per person, as reported in a previous survey (Monechi et al.,
1987), but arbitrarily halved considering that a rag
sorter’s working day was also devoted to other activities, such as rag receiving and packaging.
The number of other textile workers at risk of MM
was calculated as the difference between the number
of workers in the Prato textile industrial sector, as
recorded by national statistics in 1981 (ISTAT, 1982),
and the estimated number of rag sorters.
Although the total number of rag sorters by year
and age class is unknown, a time trend of the mesothelioma rates for these workers was evaluated using the
age class distribution of the general population of the
province of Prato and the Tuscany region as denominators for calculating the age specific incidence rates
of Prato and Tuscan textile workers, respectively.
Five-year standardized incidence rates were calculated
using the European population as a reference.
Possible past asbestos exposure in the Prato textile
sector was further evaluated through an examination
of working histories collected for other asbestosrelated diseases in textile workers registered by the
OHS of the Local Health Authority of the province of
Prato.
R E S U LTS
One hundred and seventy-two MMs were diagnosed
in the 1988–2012 period in textile workers residing
in Tuscany, 52 (30.2%) of whom were rag sorters (44
males and 8 females). Table 1 shows the characteristics of this case series by job.
The average age at diagnosis was 69 years both
in rag sorters and other textile workers. The median
survival from diagnosis was 9 months (range: 0.2–
51.5 months) in rag sorters, excluding one case discovered at post-mortem examination. In the other
group, the median survival was 8 months (range:
0.1–75.4 months).
The vast majority of cases had a histological diagnosis (85.5%): the most common histotype was epithelial mesothelioma (81 cases, 55.1%), followed
by biphasic (29 cases, 19.7%) and fibrous (4 cases,
2.7%); there were 33 cases (22.4%) of not otherwise
specified mesotheliomas. No difference was observed
in histotype distribution between rag sorters and
other textile industry workers (P = 0.4375 in Fisher’s
exact test).
A higher frequency of male cases was observed
in rag sorters compared to other textile workers
(χ2 = 16.84 and P < 0.001). The vast majority of cases
in rag sorters at the time of diagnosis lived in the province of Prato (rag sorters: 39 in Prato versus 13 in other
provinces; other textile workers: 41 in Prato versus 79
in other provinces; χ2 = 24.31 and P < 0.001), and
worked in Prato (rag sorters: 46 in Prato versus 6 in
other provinces; other textile workers: 48 in Prato versus 72 in other provinces; χ2 = 34.38 and P < 0.001).
Most textile workers were classified as occupationally
exposed to asbestos (138 cases, 80.2%) and this was
the case for all rag sorters. Job duration was on average 15.6 years in rag sorters, and 21.3 in other textile
workers; 19 cases (36.5%) were ‘always’ engaged as rag
sorters, while 33 rag sorters had other jobs in textile
industries or less frequently in other industrial sectors.
550 • Malignant mesotheliomas
Table 1. Characteristics of MM cases in subjects residing and working in the textile industry in
Tuscany, diagnosed between 1988 and 2012.
Characteristics
Rag sorters
Other textile workers
Total textile workers
No.
%
No.
%
No.
%
Gender
Male
Female
44
8
84.6
15.4
61
59
50.8
49.2
105
67
61.0
39.0
Age at diagnosis
≤64
65–74
≥75
15
21
16
8.8
40.4
30.8
39
41
40
32.5
34.2
33.3
54
62
56
31.5
36.0
32.5
Province of residence at
the time of diagnosis
Prato
Othersa
39
13
75.0
25.0
41
79
34.2
65.8
80
92
46.5
53.5
MM topography
Pleura
Peritoneum
52
—
100.0
—
115
5
95.8
4.2
167
5
97.1
2.9
Diagnostic procedure
Histological
42
80.8
105
87.5
147
85.5
Province of work place
location
Prato
Othersa
46
6
88.5
11.5
48
72
40.0
60.0
94
78
54.7
45.3
Work duration
<1 year
1–5
6–10
>10
3
11
9
29
5.7
21.2
17.3
55.8
2
18
20
80
1.8
15.0
16.6
66.6
5
29
29
109
2.8
16.9
16.9
63.4
Classification of asbestos
exposure
Certain occupational
Probable occupational
Possible occupational
Otherb
5
—
47
—
9.6
—
90.4
—
19
12
55
34
15.9
10.0
45.8
28.3
24
12
102
34
14.0
6.9
59.3
19.8
Lucca, Florence, Pisa, and Pistoia.
Household, environmental, non-professional, unlikely, unknown, and unclassified.
a
b
The number of rag sorters with <5 years’ occupation
was high compared to other textile workers (26.9%
versus 16.8%, respectively).
In rag sorters, the average latency period between
the beginning of occupation and mesothelioma
diagnosis was 51.4 years (range: 20–76), whereas
Malignant mesotheliomas • 551
for the other textile workers it was 41.7 years (range:
8–75).
The asbestos exposure grading of 47 cases in rag
sorters was ‘possibly professional’, almost double that
observed for cases in other textile workers (90.4% versus
45.8%, χ2 = 29.21 and P < 0.001). Only five rag sorters
(9.6%) were classified as cases with ‘certain’ occupational
asbestos exposure because a large amount of crocidolite
was detected in their lung tissue (3 cases), pleural plaques
were observed during post-mortem examination (1
case), or they declared when interviewed that rags were
stored in sacks previously containing asbestos (1 case).
The crude incidence rates of MMs in the 1988–
2012 period in rag sorters (both genders) working in
the province of Prato was equal to 74.1 per 100 000
(95% CI: 52.5–101.8) assuming that each worker was
able to pick out half of 200 kg of rags daily, or 166.8
per 100 000 (95% CI: 118.1–229.0) assuming that
each worker was able to pick out half of 450 kg of rags
daily with an estimated total of 2050 or 911 yearlyworking rag sorters, respectively. In other textile
workers in Prato the crude incidence rate (both genders) was equal to 3.5 per 100 000 (95% CI: 2.5–4.7).
During the 25 years of observation, the 5-year standardized incidence rates in Prato rag sorters appeared
to double throughout the 1990s while for the other
Prato textile workers the incidence rate increased
later on, at the very end of the 1990s, and then
decreased immediately afterwards. At the beginning
and at the end of the observation period, the 5-year
standardized incidence rates in Prato rag sorters and
other textile workers were similar and were five times
higher than those calculated for the textile workers in
Tuscany as a whole.
Twenty eight cases of other diseases associated
with asbestos exposure (10 diffuse pleural thickening,
9 asbestosis, and 9 pleural plaques), as well as another
12 MMs diagnosed before 1988, were registered by
the OHS of the public Local Health Authority of
Prato, in rag sorters operating in Prato. From interviews with these cases, the past use was also recorded
of compressed air systems to clean textile machinery and workplaces that could have caused extensive
indoor dispersion of asbestos fibres.
DISCUSSION
The process to select and separate wool fabrics (the rag
sorting process) has been relevant in Prato in the past
decades, contributing to the great development of the
reprocessed wool industry in that area after the second
world war.
The large number of mesotheliomas in rag sorters
suggests important past asbestos exposure of these
workers, difficult to investigate and retrieve from the
exposure histories or the companies’ documentation.
A significant number of sacks made of jute or polypropylene previously containing asbestos, which were
labelled with the country of origin, the manufacturer,
the word ‘Asbestos’ and the warnings about the danger
of their content in English, was discovered in two rag
sorting workplaces during the investigation conducted
in the 1980s (Monechi et al., 1987). Before being used
in rag packaging, these sacks, which came from Italian
asbestos-cement factories, were opened with electric
cutters, causing dispersion of asbestos fibres in the
environment. Furthermore, the presence of asbestos
fibres was observed in breathing zone samples, collected during the above-mentioned survey from workers assigned to cut sacks and press and package sorted
rags (Quinn et al., 1987). Similar sacks were also recycled for other uses during the same period in Italy,
such as genuine raw materials in the textile industry,
product padding for couches, mattresses, jackets, and
coats (Quinn et al., 1987), and in agriculture for harvesting and trading agricultural products such as cereals, olives, and hazelnuts (Barbieri et al., 2008). Other
asbestos uses and exposure have been suggested in the
textile industry: asbestos was used for its antifriction
properties in brakes and clutches of mechanical textile
looms, and in building structures for its heat-resistant properties (Chiappino et al., 2003). Exposure to
asbestos, when present, was also possible due to past
use of compressed air systems to clean textile machinery and workplaces.
The crude incidence rate of MMs in rag sorters
in Prato appears incredibly high, 41–92 times higher
than that calculated for the general resident population in the province of Prato (1.8 per 100 000; 95% CI:
1.5–2.2), while the crude incidence rate of mesothelioma in other textile workers is double. Considering
the poor prognosis of mesothelioma with almost
equal incidence and mortality rates, the observed
crude rate in rag sorters appears consistent with the
pleural mesothelioma crude rate that can be calculated
using the number of deaths for pleural and peritoneal
cancer and the person-years at risk reported for the
552 • Malignant mesotheliomas
cohort of the Italian asbestos cement workers of the
Eternit plant of Casale Monferrato from 1965 to 2003
(Magnani et al., 2008). This is between three to seven
times higher than that of the Breda cohort of railway
rolling-stock workers in Tuscany from 1960 to 2004
(Gasparrini et al., 2008), and the cohort of chrysotile asbestos miners in North Italy from 1946 to 2003
(Pira et al., 2009).
Unfortunately, data on past age and sex distribution of textile workers in Prato by job, including rag
sorters, are not available: this is a heavy setback for
estimating a standardized incidence rate of MM in
this working population. Only an estimation of the
total number of rag sorters at risk of MM from 1988
to 2012 was possible. Nevertheless, standardized
incidence rates have been calculated using the ageclass distribution of the general population of the
province of Prato for the resident cases in this province, and the general population for all Tuscan cases
in textile workers. Despite definitely being underestimated, these rates gave information about the time
trend of MM in workers. Standardized incidence
rates (standard population: Italy 2001) are available
for pleural MM in the general Italian and Tuscan
population in the 1993–2004 period: equal to 3.49
per 100 000 in Italian men and 1.25 per 100 000 in
Italian women, while in Tuscany they were 2.63 per
100 000 and 0.75 per 100 000 by gender, respectively
(Marinaccio et al., 2012).
Other drawbacks related to asbestos exposure
identification include the difficulty in gathering accurate information from cases on past occupational
asbestos exposure at the time of diagnosis so many
years after possible exposure, and, in the same cases,
the difficulty in collecting information directly from
subjects (only 45.8% of the interviews were conducted directly with the cases and 54.2% with proxies). There were direct interviews with all 5 cases
of rag sorters and 16 out of the 19 cases (84.2%) of
other textile workers, characterized by ‘certain’ occupational asbestos exposure.
According to the RENAM classification of asbestos
exposure, a case known to have worked in an economic
sector in which the presence of/use of asbestos had
been revealed, without any other relevant individual
occupational exposure to asbestos, is classified as ‘possibly’ occupationally exposed (Nesti et al., 2003). This
is the case for the vast majority of rag sorters affected
by MM, as a consequence of the information gathered
during the aforementioned survey conducted at the
end of the 1980s in two rag sorting sites (Monechi
et al., 1987; Quinn et al., 1987). Only 5 cases were
classified as ‘certain’ occupationally asbestos-exposed
because they had a diagnosis of pleural plaques, asbestos fibres were detected in lung tissue, or asbestos
exposure at work was reported. However, the high
number of MMs, and the observation of another 40
asbestos-related diseases in rag sorters strongly support the hypothesis of widespread asbestos exposure
in the rag sorting process, in the absence of any other
relevant aetiological factors for MM. Moreover, a casecontrol study conducted in the early 1990s on the aetiology of lung cancer in textile workers in Prato showed
a higher risk, adjusted for smoking, place of birth, and
age, in rag sorters compared to other textile workers
(Zappa et al., 1993).
CO N C LU S I O N S
This study confirms the high incidence of MM in rag
sorters, highlighting the asbestos exposure in these
workers and in the entire textile sector in Prato. It
also suggests the opportunity of adding epidemiological criteria to those used for asbestos-exposure
classification of cases recorded by the regional and
national mesothelioma registries: nowadays only an
evident personal history of occupational asbestos
exposure and well-known exposure data in specific
industrial workplaces results in a high-level asbestosexposure grading. A similar high-level grading of professional asbestos exposure should be attributed to
occupations with documented high-incidence rates
of MM, such as rag sorting, despite the limitations,
and uncertainties of available individual exposure
data.
A C K N O W L E D G E M E N TS
The authors would like to express special thanks
to the staff of the Tuscan mesothelioma register
and the Occupational Health Service of the Local
Health Authority of Prato for their support, and to
Susan Mary Cadby for LEXIS srl, Firenze, for the
English revision of the article. The study was carried
out within the institutional activity of the Tuscan
mesothelioma register at the Cancer Prevention and
Research Institute, an Institute of the Public Regional
Health System.
Malignant mesotheliomas • 553
The authors declare that they have no conflict of
interest.
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