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1
Department of Clinical
Medicine, Aalborg University,
Aalborg, Denmark
2
Department of Occupational
and Environmental Medicine,
Danish Ramazzini Center,
Aalborg University Hospital,
Aalborg, Denmark
3
Institute of Cancer
Epidemiology, Danish Cancer
Society, Copenhagen, Denmark
4
Department of Oncology,
Aalborg University Hospital,
Aalborg, Denmark
5
Department of Clinical and
Molecular Medicine, Norwegian
University of Science and
Technology, Trondheim, Norway
Correspondence to
Sofie Bünemann Dalsgaard,
Department of Occupational
and Environmental Medicine,
Danish Ramazzini Center,
Aalborg University Hospital,
Aalborg, Denmark;
​ksbunemann@​hotmail.​com
Received 31 July 2018
Revised 7 November 2018
Accepted 10 December 2018
© Author(s) (or their
employer(s)) 2019. No
commercial re-use. See rights
and permissions. Published
by BMJ.
To cite: Dalsgaard SB,
Würtz ET, Hansen J, et al.
Occup Environ Med Epub
ahead of print: [please include
Day Month Year]. doi:10.1136/
oemed-2018-105392
Original article
Environmental asbestos exposure in childhood and
risk of mesothelioma later in life: a long-term follow-
up register-based cohort study
Sofie Bünemann Dalsgaard,1,2 Else Toft Würtz,2 Johnni Hansen,3 Oluf Dimitri Røe,4,5
Øyvind Omland1,2
Abstract
Objective To examine the risk of malignant
mesothelioma (MM) in former pupils who attended
primary school near an asbestos cement plant.
Methods A cohort of 12 111 former pupils, born
1940–1970, was established from individual historical
records from four primary schools located at a distance
of 100–750 m in the prevailing wind direction from
an asbestos cement plant operating from 1928 to
1984 in Aalborg, Denmark. The school cohort and a
comparison cohort consisting of 108 987 gender and
5-year frequency-matched subjects were followed up
(2015) for MM in the Danish Cancer Registry. Using
Cox regression, HRs were estimated for the incidence of
MM. Adjustments for occupational and familial asbestos
exposure were made with a job exposure matrix. An
SIR analysis including latency periods testing the cancer
incidence rate was performed with the comparison
cohort as the reference rate.
Results The median person-years of follow-up were
62.5 years in the school cohort and 62.2 years in the
comparison cohort. There were 32 males and 6 females
of the former pupils who developed MM during the
follow-up: HRmale 7.01 (95% CI 4.24 to 11.57), HRfemale
7.43 (95% CI 2.50 to 22.13). Those who attended
school 250 m north of the plant had the highest HR for
MM, 10.65 (95% Cl 5.82 to 19.48). No significant trend
between school distance and risk of MM was established
(p=0.35).
Conclusion  Our results suggest that boys and girls who
attended schools and lived in the neighbourhood of an
asbestos cement plant later in life have a significantly
increased risk of MM.
Introduction
Malignant mesothelioma (MM) is a rare malig-
nancy arising in the pleura, peritoneum, pericar-
dium and in the tunica vaginalis.1 The association
between occupational asbestos exposure and MM
was first documented by Wagner et al. In the
Wagner et al study, environmental exposure as a risk
factor for MM was also shown, and several studies
have verified that living nearby an asbestos-emit-
ting source can increase the risk of MM.2 3 Mari-
naccio et al documented in a large epidemiological
national surveillance study from Italy that 10.2%
of MM cases are due to non-occupational expo-
sure to asbestos.4 Magnani et al found an increased
risk of pleural MM from environmental asbestos
Dalsgaard SB, et al. Occup Environ Med 2019;0:1–7. doi:10.1136/oemed-2018-105392
Key messages
 What is already known about this subject?
►► It is well documented that asbestos exposure
causes malignant mesothelioma.
►► Previous studies on malignant mesothelioma
have mainly focused on occupational asbestos
exposure in adulthood.
What are the new findings?
►► We found a significantly increased risk of
malignant mesothelioma in a cohort that
had been environmentally (predominantly
chrysotile) asbestos-exposed during childhood.
How might this impact on policy or clinical
practice in the foreseeable future?
►► Our study will have an impact on the
compensation policy debate.
►► Today, in Denmark, compensation is only paid
to mesothelioma cases who themselves have
been occupationally asbestos-exposed or if
a family member has been occupationally
asbestos-exposed.
exposure, controlled for other sources of asbestos
exposure, and suggested that environmental expo-
sure caused a greater risk than domestic exposure.5
In the cities of Casale Monferrato and Bari in Italy,
the mesothelioma risk increased with proximity
of residence to an asbestos plant.6 7 To distinguish
between occupational and environmental asbestos
exposure, the Italian studies retrieved data by inter-
view supplemented with register data. However, the
attributable risks from Italy are place-specific and
time-specific and cannot be extrapolated to account
for the conditions in Denmark or other countries.
Denmark has, during the last century, been
a producer of asbestos-containing products. In
Denmark, nearly 90% of the imported raw asbestos
was used in the manufacture of asbestos cement
products. The only asbestos cement plant in
Denmark was located in Aalborg in the North
Denmark Region, a city reaching 100 000 inhabi-
tants in the 1960s, and it was situated in a densely
populated area of the city.8 From 1928, when the
production began, and until 1984, a total of approx-
imately 620 000 tons of asbestos were consumed
(89% chrysotile).9
1
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Figure 1  The distribution of the four schools in an area of 250 m north and 100–750 m northeast of the asbestos plant. The picture shows the location of
the asbestos plant. The arrow shows the prevailing wind direction from the plant.
Only few studies have investigated whether asbestos exposure
in childhood increases the risk of MM.10
The aim of our study is to analyse the impact of neighbour-
hood environmental asbestos exposure in childhood and the risk
of mesothelioma later in life.
Materials and methods
Study design
This is a cohort study using individual data from high-quality
national registers: the Civil Registration System (CRS),11 the
Danish Cancer Registry (DCR)12 and the Danish Supplemen-
tary Pension Fund Register (ATP).13 Further, a country-specific
job exposure matrix (JEM) was applied to assess occupational
asbestos exposures.14
Population
The four schools included were located at a distance of 100–750
m in the prevailing wind direction15 from the asbestos cement
plant (see figure 1). Compulsory individual seventh-grade school
records were used to identify former pupils. The pupils were
identified by their name and birthplace or personal identifica-
tion number, a unique 10-digit number all residents in Denmark
are assigned from the CRS since April 1968. The flow chart
(see  figure 2) shows how the cohort was established. School
records were excluded if either the personal identification
number was missing or not validated in the CRS, or if a pupil
was born before 1940 or after 1970.
2
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From the CRS we obtained information on place of birth,
civil status, emigration, disappearance, death, and identity of
parents, siblings spouses and children.11 The unique identifica-
tion number enables linkage of information between all national
registers. The CRS was used to obtain a random cohort for
comparison that was frequency matched (1:9) according to age
and gender.
Subjects from both the school cohort and the comparison
cohort were excluded because of emigration, death or cancer
diagnosed before school start in the year of their 12th birthday.
The final cohort comprised 12 111 former pupils (50.3% males
and 49.7% females) and 108 987 comparison subjects.
Malignant mesothelioma
From the DCR we identified the MM cases registered in the period
from April 1968 (start of CRS) to the end of 2015, including
tumour characteristics. The DCR is regarded as virtually complete
and contains cancer diagnosis registered since 1943, classified
according to an extended Danish version of the International
Classification of Diseases, 7th Revision (ICD-7), which included
the diagnosis of mesothelioma (1943–1977), ICD-O (1978–2003)
and ICD-10 (2004 and onwards).12 The MM diagnosis in the
cancer registry covered validated ICD-10 codes for mesothelioma
with location in the pleura, peritoneum and pericardium.
Assessment of asbestos exposure
High levels of airborne asbestos were measured at the asbestos
plant and the relatively low-tech industry rendered workers
Dalsgaard SB, et al. Occup Environ Med 2019;0:1–7. doi:10.1136/oemed-2018-105392

Figure 2  Flow chart showing the establishment of the cohorts. CRS, Civil Registration System.
highly exposed,16 and until 1972 asbestos was transported from
the port to the plant in leaky hessian bags, with spill in the air.17
In this respect, we assume there has been substantial asbestos
pollution from the plant to the neighbourhood.
We assume the environmental asbestos exposure for the
school cohort began when the subjects became residents in the
area close to the asbestos plant. From the CRS registry no exact
residential history was available before 197718; therefore, data
from seventh-grade school records have been used as a proxy for
all childhood environmental asbestos exposure.
A Danish version of the Nordic Occupational Cancer Study
(NOCCA) JEM was used to assess occupational asbestos
exposure. The development of the NOCCA JEM has been
described by Kauppinen et al; in brief, the occupational expo-
sure was characterised by three metrics: the proportion of
exposed subjects within a job, the mean level of exposure
and four periods of calendar time (1945–1959, 1960–1974,
1975–1984 and 1985–1994).14 We have evaluated, edited
and supplemented the NOCCA JEM for it to be compatible
with the Danish industry codes (DSE77). Since 1 April 1964
all employees in Denmark have been compulsory members
of the ATP, and information on all employments, including
start and end dates, on a company and industry type level
(DSE classification) has been registered and kept for wage
earners aged 16–66 years working minimum 9 hours/week.13
Furthermore, the occupationally related asbestos exposure
has been evaluated by two specialists in occupational medi-
cine identifying local asbestos risk companies, for example,
work with recycling of hessian bags and work in the asbestos
cement plant.
A subject was defined as ever occupationally asbestos-exposed
if the exposure prevalence in the JEM exceeded 50% in at least
Dalsgaard SB, et al. Occup Environ Med 2019;0:1–7. doi:10.1136/oemed-2018-105392
Environment
Occup Environ Med: first published as 10.1136/oemed-2018-105392 on 25 February 2019. Downloaded from http://oem.bmj.com/ on 26 February 2019 by guest. Protected by copyright.
 
one job in the period from April 1964 until 31 December 1994.
By this categorisation, 9.99% of the comparison cohort were
occupationally asbestos-exposed. This is in line with previous
estimation that approximately 150 000 persons in Denmark
have been occupationally exposed to asbestos until the asbestos
ban in 1986,19 corresponding to approximately 10% of the
working population.
Relatives, that is, mother, father, siblings under 18, spouses
and children were identified by the unique identification number
in the CRS. To assess relatives’ occupational asbestos exposure,
we extracted the employment history from the ATP and used the
edited NOCCA JEM. Relatives were defined as ever occupation-
ally asbestos-exposed if exposure took place in the period from
the index subject was born (the earliest April 1964) to the 18th
birthday (the legal age of majority in Denmark). Spouses and
children were defined as ever occupationally asbestos-exposed
if the index subject was 18+ years old and under 18 years old,
respectively. Relatives’ occupational asbestos exposure is in our
study termed ‘familial occupational asbestos exposure’. An indi-
vidual from the school cohort was defined as environmentally
asbestos exposed in the absence of both occupational asbestos
exposure and familial occupational asbestos exposure.
Statistics
The χ2 test was used to compare categorical variables between
the two groups of the study population. Age medians were
calculated by the Wilcoxon-Mann-Whitney test. Associations
between environmental asbestos exposure and mesothelioma
were tested by regression analysis based on a Cox proportional
hazards model with adjustment for occupational and familial
asbestos exposure. The analyses were supplemented by test for
3
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Table 1  Description of the study population
School cohort Comparison cohort
Characteristics n (%) or years (range) n (%) or years (range) P values
Cohort size 12 111 108 987
Sex 0.985
 Male 6087 (50.3) 54 787 (50.3)
 Female 6024 (49.7) 54 200 (49.7)
Birth year
 1940–1944 2409 (19.9) 21 687 (19.9)
 1945–1949 2961 (24.5) 26 645 (24.5)
 1950–1954 2671 (22.1) 24 029 (22.1)
 1955–1959 2166 (17.9) 19 498 (17.9)
 1960–1964 1451 (12.0) 13 047 (12.0)
 1965–1970 453 (3.7) 4081 (3.7)
Person-years at risk 592 942 5 131 226
Median age 62.5 (13.5–76.0) 62.2 (12.0–76.0) 0.001
Born in Denmark* 11 834 (97.7) 95 098 (87.3) 0.000
Type of asbestos exposure†,‡ 0.000
 Only environmental/unknown asbestos exposure 8013 (66.2) 83 525 (76.6)
 Occupational asbestos exposure 1761 (14.5) 9685 (8.9)
 Familial occupational asbestos exposure 1916 (15.8) 10 398 (9.5)
 Occupational and familial occupational asbestos exposure 287 (2.4) 1203 (1.1)
 Missing Supplementary Pension Fund Register data 134 (1.1) 4176 (3.8)
*No data on local authority where the birthplace was registered (n); school cohort (164), comparison cohort (625).
†Occupational asbestos exposure dichotomisation has been found using the JEM industry asbestos exposure prevalence >50% once in the period 1960–1994.
‡In the school cohort all subjects have been environmentally asbestos-exposed, although some have been additionally asbestos-exposed as described in the subgroups.
JEM, job exposure matrix.

trend using school distance as an ordinal variable. We used likeli-
hood ratio test to examine the interactions between occupational
and familial asbestos exposure.
Person-years at risk for each of the two cohorts were calcu-
lated from 2 April 1968 (start of CRS) or 1 August, the year the
subjects turned 12 years old (seventh-grade school start) if born
after 2 April 1968. Accumulation of person-years at risk ended
at the date of diagnosis of MM, date of death, emigration or
disappearance or on 31 December 2015, whichever came first.
Sensitivity analyses were performed by (1) recoding subjects
without ATP data (self-employed) into having occupational
asbestos exposure, (2) excluding all subjects born prior to
year 1948 in order to have complete employment records, (3)
excluding all subjects not born in Denmark, (4) excluding all
subjects born after year 1955 to find the HR for the oldest age
groups, and using different cut-points for categorising a subject
as occupationally asbestos-exposed by exposure prevalence, (5)
0%, (6) 10%, (7) 25% and (8) 75%.
We estimated SIR as the ratio of the observed and the expected
cases with 95% CI. Further, lag time analyses deferring start of
follow-up (10, 20 and 30 years) were performed for the SIR
(see online supplementary table s1).
All analyses were performed using Stata V.15.1.
Results
The main characteristics of the cohorts are described in table 1.
In the school cohort the median follow-up time was 62.5 years
and and for the comparison cohort was 62.2 years.
All subjects in the school cohort have been environmen-
tally asbestos-exposed. Further potential occupational asbestos
exposure was detected in 2048 subjects (16.9%) in the school
cohort and in 10 888 subjects (10.0%) in the comparison cohort.
Subjects with familial occupational asbestos exposure were
estimated as 1916 subjects (15.8%) in the school cohort, and in
the comparison cohort 10 398 subjects (9.5%) had relatives with
asbestos-related work.
Mesothelioma risk
A total of 76 incident MM cases (38 MM cases in the school
cohort and 38 MM cases in the comparison cohort) occurred
during the follow-up period (table 2). This represented an
elevated relative risk for the school cohort compared with the
comparison group (SIR 8.77; 95% CI 6.38 to 12.05). The school
cohort had a HR for MM of 7.15 (95% CI 4.54 to 11.27),
adjusted for index subject’s occupational asbestos exposure and
familial occupational asbestos exposure (table 3). The HR for
males was HRmale 7.01 (95% CI 4.24 to 11.57); the unadjusted
HR for females was 7.43 (95% CI 2.50 to 22.13).
No evidence of interaction between index subjects’ occupa-
tionally asbestos-exposure and relatives’ occupationally asbes-
tos-exposure was found (results not shown). Restricting the
analysis to subjects with neither occupational nor familial occu-
pational asbestos exposure resulted in a HR for MM of 5.12
(95% CI 2.49 to 10.57). The distribution of cases regarding
anatomical site was not significantly different in the two cohorts
(table 2).
School distance and mesothelioma risk
Table 3 presents the analysis of distance between the asbestos
cement plant and the school attended and risk of MM. The
highest HR was found for children who attended school at about
250 m north of the plant: HR for MM 10.65 (95% CI 5.82 to
19.48). No significant trend between school distance and risk of
MM was established (p=0.347).

4 Dalsgaard SB, et al. Occup Environ Med 2019;0:1–7. doi:10.1136/oemed-2018-105392

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Table 2  Description of malignant mesothelioma cases
School cohort Comparison cohort
Characteristics n (%) or years (range) n (%) or years (range) P values
Sex 0.761
 Male 32 (84.2) 31 (81.6)
 Female 6 (15.8) 7 (18.4)
Birth year 0.756
 1940–1944 17 (44.7) 18 (47.4)
 1945–1949 9 (23.7) 10 (26.3)
 1950–1954 9 (23.7) 5 (13.2)
 1955–1959 2 (5.3) 4 (10.5)
 1960–1964 1 (2.6) 1 (2.6)
 1965–1970 0 (0.0) 0 (0.0)
Median age at diagnosis 61.0 (39.9–74.4) 60.2 (42.5–73.0) 0.819
Born in Denmark 37 (97.4) 36 (94.7) 0.157
Anatomical site, n (%)
 Pleural 35 (92.1) 36 (94.7) 0.503
 Peritoneal 1 (2.6) 2 (5.3)
 Heart/Pericardial 1 (2.6) 0 (0.0)
 Mesothelioma, unspecified 1 (2.6) 0 (0.0)
Type of asbestos exposure*,† 0.067
 Only environmental/unknown asbestos exposure 11 22
 Occupational asbestos exposure 20 13
 Familial occupational asbestos exposure 4 1
 Occupational and familial occupational asbestos exposure 3 2
 Missing Supplementary Pension Fund Register data 0 0
*Occupational asbestos exposure dichotomisation has been found using the JEM industry asbestos exposure prevalence >50% once in the period 1960–1994.
†In the school cohort all subjects have been environmentally asbestos-exposed, although some have been additionally asbestos-exposed as described in the subgroups.
JEM, job exposure matrix.

Characteristics of asbestos exposure in mesothelioma cases Sensitivity analyses

In the school cohort 29% (6 males/5 females, ratio 1.2:1) had no
other known asbestos-assessed exposure than the environmental
asbestos exposure from attending school and living nearby the
asbestos plant. Out of 38 cases in the comparison cohort, 58%
(15 males/7 females, ratio 2.1:1) had neither occupational nor
familial occupational asbestos exposure.
Using our JEM, 61% (23 males) from the school cohort and
39% (15 males) from the comparison cohort worked in an
industry with potential asbestos exposure with a mean cumu-
lated time of employment of 7.1 years (range 0.1–35.1) and 8.3
years (range 0.1–42.2), respectively. Table 4 shows the details
on occupational asbestos exposure among mesothelioma cases;
shipyard workers were the most prevalent, followed by workers
in carpentry, electrical and insulations firms, and in total three
persons were employed at the asbestos cement plant. For the
shipyard workers, nine out of the ten cases in the school cohort
had worked in the Aalborg Shipyard, while all shipyard workers
in the comparison cohort had worked in shipyards elsewhere.
In a sensitivity analysis 134 subjects from the school cohort
and 4176 subjects from the comparison group without ATP
records were added to be in an occupationally and/or familial
occupationally asbestos-exposed group. This did not change the
adjusted HR for MM significantly (see online supplementary
table s1 [a]).
We performed a subanalysis excluding all subjects born before
April 1948, that is, aged at least 16 years old, having available
employment information on all subjects (see  online supplemen-
tary table s1 [b]). This did not change the HR either. All meso-
thelioma cases had information about their employment history
from the ATP.
In order to exclude potential natural-occurring asbestos expo-
sure in childhood before the seventh grade, a sensitivity analysis
was made restricting the analysis to subjects born in Denmark; no
change in HR was found (see online supplementary table s1 [c]).
The HR did not change either for those born before year 1955
(see online supplementary table s1 [d]). The majority (89%) of

Table 3  Risk of malignant mesothelioma in relation to school attended near an asbestos cement plant
Overall school School A School B School C School D
Cohort, n (%) 12 111 3792 2304 3134 3690
Distance from the 100 250 750 750
asbestos plant, m
Mesothelioma HR 7.15 (4.54 to 11.27) 8.21 (4.25 to 15.84) 10.65 (5.82 to 19.48) 7.71 (3.82 to 15.57) 6.07 (2.92 to 12.62)
(95% CI)*
796 former pupils went to more than one school. They have been counted at each school attended and thereby counted more than once.
*Adjusted for occupational asbestos exposure and familial occupational asbestos exposure.

Dalsgaard SB, et al. Occup Environ Med 2019;0:1–7. doi:10.1136/oemed-2018-105392 5

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median age at diagnosis was not significantly different in the
Table 4  Work industries for mesothelioma cases with occupational
two cohorts. Furthermore, no significant difference was found
asbestos exposure
in the median age at diagnosis between those in the school
School cohort Comparison cohort
cohort only environmentally asbestos-exposed and those who
Duration of Duration of also had been occupationally asbestos-exposed. This might
Industry (DSE77) n=23 employment (range) n=15 employment (range)
indicate that the environmental asbestos exposure is substan-
Asbestos cement 2 1.0–3.6 1 0.6
plant
tial enough to cause mesothelioma, and for some occupation-
Iron shipyards 10 0.1–21.3* 6 0.2–42.2* ally asbestos-exposed cases it could be a reflection of very brief
Building and 3 0.5–9.0 4 0.3–12.6 occupational exposure (see table 4). Alternatively, age at diag-
carpentry firms nosis might not depend on either level of exposure or time of
Plumbing 0 – 1 9.7 exposure.
businesses
Electrical 4 0.1–3.1 2 0.1–8.7
As for the diagnosis of mesothelioma, the more than
contracting firms 70-year-old DCR was used to identify all subjects diagnosed
Insulation firms 3 3.2–35.1 0 – with mesothelioma in the study period.12 The asbestos cement
Railroads 1 29.3 1 0.2 plant was an important workplace in the city of Aalborg, with
*In both cohorts 50% of the iron shipyards workers worked less than 1 year in this industry. more than 8000 employees in the period between 1928 and
DSE77 Danish industry codes.
1984.26 This could have caused a greater focus and awareness
towards asbestos-related diseases, which may have led to bias
in terms of more people being diagnosed with mesothelioma in
all cases were born before 1955. The HRs calculated with the Aalborg compared with other cities. In a subanalysis, the propor-
variant proportions of asbestos workers are also with overlap- tion of the school cohort mesothelioma cases who at the end of
ping CIs and considered statistically similar (see online supple- follow-up lived in the Aalborg area (0.4%) was not significantly
mentary table s1 [e–h]). different from those who did not live in the Aalborg area at the
end of follow-up (0.2%) (p=0.08). In view of the small number
Age at diagnosis and latency time of cases, these results are difficult to interpret; however, it gives
No significant difference in the median age at diagnosis was an indication that bias from living in Aalborg at time of diagnosis
found in the cohorts. In the school cohort the median age at is not present to a large extent.
diagnosis for those only environmentally asbestos-exposed was In this study population, all children have been assigned to a
61.5 years. For those also occupationally and/or familial asbes- school district according to the distance to their living address.
tos-exposed, the median age at diagnosis was 60.9 and 61.6 Therefore, we used the seventh-grade school exposure as a
years in the school cohort and comparison cohort, respectively. proxy to the overall environmental asbestos exposure because
Lag time analyses deferring start of follow-up 10, 20 and 30 it captures both the exposure in school time and the residen-
years (see online supplementary table s2) show that the majority tial asbestos exposure. Residence close to an asbestos factory
of cases (97%) developed MM more than 30 years after their was also used as proxy to environmental exposure in previous
seventh-grade school attendance. studies. Newhouse and Thompson reported a relative risk of 2.2
for subjects who lived within half a mile (~805 m) of an asbestos
Discussion factory in the London area.27
In this register-based cohort study, we found, as assumed for In a follow-up study of children living close to the crocidolite
an environmentally asbestos-exposed cohort, a similar HR for mine of Wittenoom, Reid et al found an increased incidence and
MM among males and females. We found a significantly higher mortality of MM among ‘former Wittenoom children’ compared
risk for MM for pupils who attended either of the four schools with the West Australian population.28
included in the study, but no trend between school distance to A larger proportion of the school cohort had been occupa-
the asbestos plant and risk of MM could be established. tionally asbestos-exposed and/or had relatives occupationally
Further, the risk of MM in the school cohort was also signifi- asbestos-exposed, which is not surprising given the many people
cantly higher when the analysis was restricted to subjects without living nearby, and thus having a potential for employment at the
occupational or familial occupational asbestos exposure. asbestos cement plant or at the shipyard in Aalborg.
Our results are in line with previous studies finding non-oc- Defining environmental exposure was based on exclusion of
cupational exposure to asbestos to be associated with increased occupational asbestos exposure by means of a JEM. However,
MM risk.20 21 The SIR of 8.77 (95% CI 6.38 to 12.05) included misclassification might be introduced involving the JEM.
all asbestos exposure groups and was found to be in the same Analysing for risk of MM by using lower or higher proportions
range as the SIR calculated by Mensi et al from Broni, an Italian of asbestos workers to define an asbestos workplace did not
town which had an asbestos cement factory operating for more change the risk estimate for neither environmental or occupa-
than 60 years (SIR 8.4; 95% CI 7.1 to 9.9).22 tional asbestos exposure. We therefore think our risk estimate
Our results on mesothelioma risk are also consistent with the for developing MM by attending school nearby the asbestos
results by Magnani et al, who found an increased risk of MM plant is valid and not skewed by exposure misclassification.
for people who never worked in the asbestos cement industry In the school cohort the male to female ratio for the environ-
and who attended their grammar school in Casale Monferrato in mentally asbestos-exposed cases was 1.2:1. This male to female
Italy, a city with an asbestos plant located as in Aalborg.5 ratio might be influenced by residual confounding. Consistent
The few previous studies reporting on non-occupational with the male to female ratio found in our study, Magnani et
asbestos exposure in childhood are inconsistent.10 Some studies al reported in a study from Casale Monferrato, Italy, a male to
reported asbestos exposure to be more harmful when exposed female ratio of 1.2:1 (35 men and 29 women) for those not occu-
in the younger ages,23 24 while Reid et al found a lower meso- pationally or paraoccupationally asbestos-exposed.29 A higher
thelioma rate in those exposed as children compared with male to female ratio of 1:2.3 for a population with non-occupa-
those first exposed at >15 years of age.25 In our study the tional exposure was reported by Marinaccio et al.4

6 Dalsgaard SB, et al. Occup Environ Med 2019;0:1–7. doi:10.1136/oemed-2018-105392


In the comparison cohort 22 cases (male to female ratio
of 2.1:1) had no apparent occupational nor familial occupa-
tional asbestos exposure. The higher number of male cases with
unknown asbestos exposure could indicate that some expected
misclassification from the use of the JEM has happened.
The strengths of this study are the large population size, the
long follow-up time and the validated relevant information that
was gathered and available through nationwide high-quality
registries.
Occupational and familial occupational asbestos exposure esti-
mation by linkage to a JEM could be considered both a strength
and a limitation of the study. Our JEM estimates the historical
occupational asbestos exposures avoiding recall bias. However,
due to the heterogeneity of both exposure and probability of
exposure within jobs, together with lack of information on
employments before April 1964 and self-employments, misclas-
sification of asbestos exposure is unavoidable, but unlikely to
explain our overall results. The performed sensitivity analyses
did not reveal large changes in the results, which suggests that
the misclassification in our study may be limited.
MM is still a disease of importance since the incidence in
Denmark is increasing despite cessation of the use of asbestos
in the 1980s.30 In Denmark, patients with MM are entitled to
financial compensation if they have been either occupationally
or familial asbestos-exposed, but no compensation is granted if
the exposure has only been environmental. In the Netherlands, it
is possible to apply for compensation if either the asbestos expo-
sure has been work-related or non-work-related, for example,
environmental asbestos exposure.31 In France, the Social Secu-
rity Law of 2000 created the fund of indemnification, which
gives compensation to all asbestos victims—also those non-occu-
pationally asbestos-exposed.32
Conclusion
In conclusion, our study adds to the evidence that environmental
asbestos exposure by school attendance near an asbestos cement
factory significantly increases the risk of MM. Even though occu-
pational asbestos exposure is a powerful determinant of MM
risk, our results suggest that childhood environmental asbestos
exposure is also an important risk factor. In light of our results,
we suggest considerations towards altering the Danish compen-
sation regulations to apply for all mesothelioma cases regardless
of type of asbestos exposure.
Acknowledgements  The authors thank the Aalborg City Archives, the Danish
Civil Registration System, the Danish Cancer Registry and the Danish Supplementary
Pension Fund Register for providing data used in the study. We also thank Dr Vasiliki
Panou for helping with data on female mesothelioma cases.
Contributors  ØO designed the study. JH collected, cleaned and coded raw data
from registries. JH constructed the asbestos JEM. SBD performed the statistical
analyses and drafted the manuscript in collaboration with ETW and ØO. All
coauthors have assisted with interpretation of the findings and revised the
manuscript critically. The final version has been approved by all authors.
Funding  This study has been financially supported by Aalborg University.
Competing interests  None declared.
Patient consent  Not required.
Ethics approval  The study has been performed in accordance with the Helsinki
Declaration and approved by the Danish Data Protection Agency (j no: 2016-41-
4787).
Provenance and peer review  Not commissioned; externally peer reviewed.
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