BJD

C L I N I C A L A N D LA B O R A T O R Y I N V E S T I G A T I O N S British Journal of Dermatology

Occupational ultraviolet light exposure increases the risk

for the development of cutaneous squamous cell
carcinoma: a systematic review and meta-analysis
J. Schmitt, A. Seidler,* T.L. Diepgen and A. Bauer
Department of Dermatology, *Institute and Polyclinic for Occupational and Social Medicine, Carl Gustav Carus Faculty of Medicine, Technische Universität
Dresden, Fetscherstraße 74, Dresden 01307, Germany
Department of Social Medicine, Occupational and Environmental Dermatology, University Clinic of Heidelberg, Bergheimerstraße 58, Heidelberg 69115,
Germany

Summary

Correspondence Background Despite the fact that ultraviolet (UV) light exposure is the most impor-
Jochen Schmitt. tant risk factor for cutaneous squamous cell carcinoma (SCC) there is an ongoing
E-mail: Jochen.Schmitt@uniklinikum-dresden.de debate concerning the relationship between cumulative work-related UV expos-
ure and SCC occurrence.
Accepted for publication
6 October 2010 Objectives To analyse comprehensively the relationship between work-related UV
exposure and SCC risk.
Funding sources Methods We conducted a systematic electronic literature search in PubMed (up to
No external funding.
5 May 2010) supplemented by a hand search, which identified 18 relevant stud-
Conflicts of interest ies that were included in the review. Data abstraction and study quality assess-
None declared. ment was done independently by two reviewers. Maximally adjusted odds ratios
(ORs) and corresponding 95% confidence intervals (CIs) of all included studies
DOI 10.1111/j.1365-2133.2010.10118.x were pooled in a random-effects meta-analysis. Sensitivity analysis included
meta-regression on study-specific covariates to explore the robustness of the
results and to identify sources of heterogeneity between studies. Eighteen studies
(six cohort studies, 12 case–control studies) met the eligibility criteria and were
included in the systematic review.
Results Sixteen studies (89%) found an increased risk of SCC in individuals with
occupational UV light exposure compared with individuals without occupational
UV light exposure, reaching statistical significance in 12 studies. Two studies
found no association between occupational UV light exposure and SCC
occurrence. The pooled OR (95% CI) was 1Æ77 (1Æ40–2Æ22) and did not differ
significantly between cohort studies [OR (95% CI): 1Æ68 (1Æ08–2Æ63)] and
case–control studies [OR (95% CI): 1Æ77 (1Æ37–2Æ30)]. Meta-regression analyses
suggested an increasing strength of the association between occupational UV light
exposure and SCC risk with decreasing latitude.
Conclusions In summary, there is consistent epidemiological evidence for a positive
association between occupational UV light exposure and SCC risk.

Cutaneous squamous cell carcinoma (SCC) is among the most
frequent malignancies worldwide and constitutes a significant
public health problem.1 The age-adjusted incidence of SCC has
grown by 50–200% over the past 20–40 years.2–4 Exposure to
ultraviolet (UV) radiation is the most common and most
important known cause of cutaneous SCC.5 Cutaneous SCC
occurs mainly on sun-exposed body sites such as the face.6,7
Its frequency can be reduced by sun protective measures.1 It
has been shown that cumulative lifetime UV exposure is most
important in the pathogenesis of SCC, whereas intermittent
UV exposure is considered to be primarily relevant in the aeti-
ology of other types of skin cancer such as melanoma or basal
cell carcinoma (BCC).5
An individual’s risk of developing SCC depends on pheno-
typic, genotypic and environmental factors: compared with
women, men are about twice as frequently affected; 80% of
cases occur in people aged 60 years and older. Individual UV
susceptibility is an important phenotypic risk factor for the de-
velopment of SCC: Caucasians with fair skin, and light eye
and hair colour are at increased risk.1 Smoking has also been

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BJD  2011 British Association of Dermatologists 2011 164, pp291–307 291
292 Occupational UV exposure and cutaneous SCC, J. Schmitt et al.
shown to be an important risk factor for the development of
SCC.8,9 Geographic variation in SCC occurrence is mainly
explained by ambient UV light exposure: SCC incidence is as-
sociated with proximity to the equator.6,10–13
Although the biological underpinnings of the causal role of
UV light exposure and the development of cutaneous SCC are
well understood and epidemiological data from various
sources provided indirect but substantial evidence that solar
UV light exposure is by far the most relevant risk factor for
SCC on the population level, there is ongoing debate about
the relationship between occupational exposure to solar UV
light and the risk of cutaneous SCC.14–17 Relevant proportions
of the working population experience high levels of chronic
or intermittent work-related exposure to solar UV light. In
Germany, for example, approximately two million individuals
are working in typical outdoor occupations, e.g. as construc-
tion workers, farmers, winegrowers, roadmen, seafarers, for-
esters or lumbermen, or fishermen.15 German law aims to
protect individuals with relevant work-related exposure result-
ing in adverse medical outcomes.18 Although it is reasonable
to assume that outdoor workers are at higher risk of develop-
ing cutaneous SCC compared with indoor workers, UV light-
induced work-related cutaneous SCC is not officially accepted
as an occupational disease in Germany. The major reason is
the lack of a comprehensive summary of the epidemiological
literature regarding the relationship between work-related UV
exposure and cutaneous SCC.
In order to fill this research gap we conducted a systematic
review and meta-analysis to analyse the relationship between
work-related exposure to solar UV radiation and the develop-
ment of cutaneous SCC. We hypothesized that (i) occupational
UV exposure is a significant independent risk factor for SCC
occurrence; (ii) the strength of the association between occu-
pational UV exposure and SCC risk increases with the dose of
individual occupational UV exposure; and (iii) the geographi-
cal region is one important source of heterogeneity between
studies, i.e. that the strength of the association between occu-
pational UV exposure and SCC occurrence increases with
decreasing latitude.
Materials and methods
Study design
We systematically reviewed original articles reporting on cohort
studies or case–control studies to investigate the relationship
between work-related exposure to solar UV light and the occur-
rence of cutaneous SCC. The presented systematic review was
performed in accordance with the principles of the Meta-analy-
sis of Observational Studies in Epidemiology (MOOSE) group.19
Eligibility criteria and identification of articles
We included all cohort studies or case–control studies report-
ing on the occurrence of cutaneous SCC with regard to previ-
ous work-related exposure to solar UV light and ⁄or outdoor
BJD  2011 British Association of Dermatologists 2011 164, pp291–307
occupation. If not specified in the paper, we considered the
following occupations as outdoor occupations with high levels
of work-related UV light exposure: asphalt workers, construc-
tion workers, farmers, winegrowers, roadmen, fishermen ⁄
seafarers ⁄deck crew, foresters ⁄lumbermen, or gardeners.20,21
SCC and BCC are frequently summarized as nonmelanoma skin
cancer (NMSC). Because the most relevant pattern of UV light
exposure differs between SCC and BCC (cumulative exposure
vs. intermittent exposure), we excluded studies that reported
only on the occurrence of NMSC without differentiating
between the exact histopathological entities.5 However, aiming
for a very sensitive search strategy we extended the literature
search beyond SCC and also included search terms for BCC
and NMSC.
A systematic electronic literature search in PubMed was
done from inception up to 5 May 2010. We searched for
combinations of the following search terms:
‘risk’ OR ‘incidence’ OR ‘epidemiologic studies’ [MeSH
terms]
AND
‘Carcinoma, squamous cell’ OR ‘Carcinoma, basal cell’ OR
‘skin cancer’ [MeSH terms]
AND
‘sunlight’ OR ‘ultraviolet rays’ OR ‘ultraviolet light’
AND
‘occupational’ OR ‘occupation’ OR ‘outdoor work’ OR ‘work’
OR ‘workplace’
We limited the systematic electronic search to original arti-
cles reporting on humans and articles with abstracts, but did
not apply any language constraints. The electronic search was
supplemented by hand searching the reference lists of all iden-
tified articles and other review papers for additional relevant
publications.
Data abstraction
Screening for eligibility of articles, data abstraction from the
articles included, and study quality assessment were done
independently by two reviewers. Disagreements were resolved
by discussion between all authors. The data abstraction form
included information on relevant study characteristics such as
geographical region, study design, source population, number
of participants, data sources, as well as participant characteris-
tics (age, sex, ethnicity, smoking status, family history of cuta-
neous SCC). The latitude of the geographical region in which
the individual studies were performed was identified from
Google Maps (http://www.gorissen.info/Pierre/maps/google-
MapLocationv3.php).
With regard to our research question it is critically impor-
tant to differentiate between work-related and recreational
exposure to solar UV light. Imprecise exposure assessment
may introduce nondifferential misclassification bias.22 There-
fore, we abstracted detailed information on exposure assess-
ment and definition and categorization of occupational UV
exposure. Study results were abstracted both descriptively and
quantitatively with the main outcome of interest being the
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association between occupational UV exposure and SCC occur-
rence expressed as maximally adjusted odds ratios (ORs) and
corresponding 95% confidence intervals (CIs). We also
abstracted information on whether adjustment was performed
for important potential confounding factors, i.e. age, sex, UV
sensitivity, nonoccupational UV exposure, family history of
skin cancer, and smoking status.1,4,5,23 If not reported in the
paper, ORs were calculated from the numbers presented
whenever possible.
For both the results tables as well as for the quantitative
analysis, tumour frequencies among outdoor and indoor
workers were compared with each other whenever possible.
In studies in which occupational exposure to UV light was
quantified differently, workers with the greatest UV exposure
were compared with those with the least. If the study
included an actual stratification by occupational groups of out-
door workers, the largest occupational group with a high like-
lihood to actually perform outdoor work, i.e. asphalt workers,
construction workers, farmers, winegrowers, roadmen, fisher-
men ⁄seafarers ⁄deck crew, foresters ⁄lumbermen, or gardeners
was taken as the measure.20,21 In case of reporting of different
anatomical localizations of SCC occurrence, localizations with
a high likelihood of UV exposure such as lips, hands or face
were considered.
Study quality assessment
Methodological quality was assessed by means of the New-
castle–Ottawa scale (NOS).24 The NOS is a validated and stan-
dardized instrument for judging the quality of cohort studies
and case–control studies by means of eight criteria regarding
selection of study participants, comparability, outcome assess-
ment and exposure assessment.24 For the criterion ‘compara-
bility’ full credit was given if age, sex, UV sensitivity and
individual nonoccupational UV exposure was controlled for by
the study design or in data analysis. Studies that considered
age, but failed to consider one or more of the other relevant
confounders were given half credit.24 In addition to the study
quality criteria captured by the NOS we considered the fol-
lowing items as important for our research question: assess-
ment of individual UV light exposure, exploration of effect
modification, and likelihood of recall bias (in case–control
studies). The criterion ‘exploration of effect modification’ was
included in light of an investigation by Marks et al.12 on the
relationship between outdoor work and SCC occurrence that
found this relationship to be significantly modified by age.
Whenever obvious, additional possible methodological limita-
tions and the direction of the bias introduced were recorded.
Quantitative analysis
ORs of all included studies were pooled using random-effects
meta-analysis (DerSimonian–Laird method).25 Fully adjusted
ORs of the individual studies were used for meta-analysis,
because we considered adjusted ORs as the best estimate of
the true independent association between work-related UV
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BJD  2011 British Association of Dermatologists 2011 164, pp291–307
Occupational UV exposure and cutaneous SCC, J. Schmitt et al. 293
light exposure and SCC risk. A minority of the included stud-
ies reported rate ratios (RRs) instead of ORs. Because RRs and
ORs are almost identical if the prevalence of the outcome of
interest is as low as the prevalence of SCC,22 we decided not
to differentiate between OR and RR in the qualitative and
quantitative analysis.
To explore the robustness of our findings a set of sensitivity
analyses was carried out. As part of the sensitivity analysis
pooled ORs were calculated separately for cohort studies and
case–control studies. Heterogeneity based on study-specific
covariates such as the absolute value of latitude, utilization of
cancer registry data for exposure assessment vs. assessment of
individual work-related UV light exposure, and study quality
criteria was examined by meta-regression. Both crude meta-
regression models and models adjusted for study type were
calculated. Publication bias was explored by regressing the
study result (OR) on sample size adjusting for study type.26
All analyses were carried out using STATA, version 10 (Stata
Corporation, College Station, TX, U.S.A.).
Results
We reviewed the abstracts of all 194 citations yielded by the
electronic search, excluded 162 articles after title and abstract
review, and another 21 articles after full text review because
Standardized electronic
literature search (PubMed,
up to 5 May 2010)
194 articles identified by
review of abstracts
162 articles excluded
32 full text articles screened
for eligibility
21 articles excluded
11 studies included
Hand search: identification of
7 additional studies meeting
the eligibility criteria
18 studies included in the
systematic review
Fig 1. Flow chart of study identification.
294 Occupational UV exposure and cutaneous SCC, J. Schmitt et al.
they did not meet the eligibility criteria. In addition to the 11
studies identified through the electronic literature search that
met our predefined eligibility criteria, seven additional eligible
studies were identified through a hand search so that a total
of 18 studies could be included in the systematic review
(Fig. 1).
Qualitative analysis of studies included
The characteristics of the six cohort studies11,12,27–30 and 12
case–control-studies8,9,14,21,31–38 included are summarized in
Table 1. Eleven studies were conducted in Europe, five in
North America, and two in Australia. All except one cohort
study11 were recruited from the general population. In the
case–control studies, cases were identified directly from the
general population or from population-based cancer registries
in nine studies and from selected dermatological centres in
three studies. Eleven studies utilized cancer registry data exclu-
sively or supplemented by questionnaire data, while seven
studies relied exclusively on primary data collected by ques-
tionnaire, interview and ⁄or clinical examination (Table 1).
There was significant heterogeneity in the definition of
‘occupational UV exposure’: eight studies looked at specific
occupations typically involving outdoor work such as farming,
construction work or seafaring. Five studies estimated occupa-
tional UV light exposure on a continuous scale and compared
participants with high vs. low cumulative exposure. Five stud-
ies reported only whether outdoor work was performed ever
or at a specific point in time without providing further details
(Table 2). In the majority of the studies included (14 of 18
studies; 78%) the reference group was defined as ‘mainly
indoor work’, ‘low occupational UV light exposure’, or
included occupations actually performing outdoor work,
mixed indoor ⁄outdoor work, or the general population. This
imprecise definition of the unexposed group is an important
source of nondifferential misclassification introducing bias
towards the null effect (Table 2).22 Five studies were restricted
to males. Information on important characteristics and
potential confounders such as ethnicity, smoking status and
family history of skin cancer were frequently not reported
(Table 2).
Thirteen studies assessed individual occupational UV light
exposure while five studies exclusively relied on census or
registry data and used the job description as a proxy for occu-
pational UV light exposure (Table 3). A quantification of
occupational UV light exposure was given in 10 papers and
was not assessed in the remaining eight papers (Table 3).
Table 3 reveals information on the measurement of occupa-
tional and nonoccupational UV light exposure in the 18 stud-
ies included.
Sixteen studies (89%) found an increased risk of SCC in
individuals with occupational UV light exposure compared
with individuals without ⁄with lower occupational UV light
exposure. The positive association reached statistical signifi-
cance in 12 studies. Two studies found no association between
occupational UV light exposure and SCC occurrence. None of
BJD  2011 British Association of Dermatologists 2011 164, pp291–307
the studies found an inverse relationship between occupational
UV light exposure and SCC occurrence (Table 4). Seventeen
(94%) and sixteen studies (89%) considered age and age and
sex as important confounders, respectively. Other relevant
confounders such as UV sensitivity, nonoccupational UV ex-
posure, and smoking status were considered only in a minor-
ity of studies. None of the studies adjusted for family history
of skin cancer (Table 4).
Details on study quality assessment are summarized in
Table 5. None of the studies adequately met all of the pre-
defined quality criteria. Some of the study quality items such
as assessment of exposure, adequacy of follow-up, absence of
outcome of interest at baseline, selection of controls ⁄nonex-
posed cohort, and representativeness of exposed cohort ⁄cases
were met by the majority of studies. Methodological weak-
nesses included the exploration of effect modification, which
was done only in the study by Marks et al.12 In this study,
significant interaction of the relationship between outdoor
work and SCC risk by age was detected (P = 0Æ034) and there
was an increase in SCC risk only in outdoor workers above
age 55 years.12 The limitations in the assessment of individual
occupational UV light exposure most likely introduced non-
differential misclassification resulting in bias towards the null
effect.22 In six out of 12 case–control studies (50%) we
judged recall bias not to be unlikely – a possible source of
bias introducing an overestimation of the true relationship
between occupational UV light exposure and SCC risk
(Table 4).22
Quantitative results – meta-analysis
Meta-analysis indicated that individuals with outdoor UV light
exposure are at significantly increased risk of developing cuta-
neous SCC. The pooled OR (95% CI) of the random-effects
meta-analysis including all 18 studies was 1Æ77 (1Æ40–2Æ22)
(P < 0Æ001) (P for heterogeneity < 0Æ001; moment-based esti-
mate of between studies variance = 0Æ131). The pooled OR
(95% CI) was virtually identical in cohort studies [n = 6; OR
1Æ68 (1Æ08–2Æ63); P = 0Æ022] (P for heterogeneity < 0Æ001;
moment-based estimate of between studies variance = 0Æ231)
and case–control studies [n = 12; OR 1Æ77 (1Æ37–2Æ30);
P < 0Æ001] (P for heterogeneity = 0Æ002; moment-based esti-
mate of between studies variance = 0Æ087) (Fig. 2).
Meta-regression analysis identified significant sources of
heterogeneity between studies. The strength of the association
between occupational UV light exposure and SCC risk in-
creased significantly with decreasing latitude of the geographi-
cal region where the study was conducted [P = 0Æ022 in the
adjusted model; P < 0Æ001 in the unadjusted model (Fig. 3)].
Despite this statistically significant association, some individual
studies found a low risk of SCC among outdoor workers
despite low latitude27,36 or indicated high risk of SCC among
outdoor workers despite high latitude (Fig. 3).11,33
Studies utilizing registries found significantly weaker associ-
ations between occupational UV light exposure and SCC than
studies using only primary data and selected cases without the
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Table 1 Characteristics of included studies

Source population; In case–control Number of

Time source from which studies: method participants ⁄
References Geographical region conducteda Latitude Study design cases were identified used to select controls py includedb Data sourcesc
Marks et al. 12
Australia, Maryborough 1982–86 )37 Cohort General population NA n = 2669 Questionnaires and physical
(Victoria) examinations
Green et al.27 Australia, Queensland 1986–92 )27 Cohort General population NA n = 2095 Questionnaires and physical
examinations
Pukkala and Saarni28 Finland 1967–92 Unclear Cohort General population; NA n = 30 490 Registry data (cancer
(seafarers) cancer registry 642 000 py registry, pension fund)
Adami et al.29 Sweden 1960–89 59 Cohort General population; NA n = 4 171 175 Cancer registry, census data
cancer registry 69 639 237 py
Hakansson et al.11 Sweden 1971–93 59 Cohortd Participants of occupational NA n = 323 860 Cancer registry,
health service programme 4 542 911 py occupational health
programme
Radespiel-Tröger et al.30 Germany, Bavaria 2001–05 48 Cohort General population; cancer NA 2 156 336 py Cancer registry
registry
Aubry and MacGibbon8 Canada, Montreal 1977–78 45 Case–controle Hospitalized patients Hospital controls, 2 : 1 n = 266 Questionnaire
matched by age, sex, Ca: n = 92

Occupational UV exposure and cutaneous SCC, J. Schmitt et al. 295

location Co: n = 174
Hogan et al.31 Canada, Saskatchewan 1982–83 50 Case–control General population; cancer Population controls, n = 462 Questionnaire
registries matched Ca: n = 178
by age, sex, location Co: n = 284
Gafa et al.32 Italy, Sicily 1987–90 37 Case–control General population; 2 controls per case – one n = 399 Cancer registry,
cancer registry hospital control, one (including questionnaire
friend ⁄ relative, matched 25 SCC cases)
by age and sex
Gallagher et al.33 Canada, Alberta 1983–84 53 Case–control General population; Population controls, n = 586 Interview by blinded
cancer registries matched by age and Ca: n = 180 investigators
sex Co: n = 406
Rosso et al.34 Southern Europe 1989–93 45 Case–control General population; Population controls n = 2023 Interview, physical
(Italy, Spain, France), Turin cancer registries; (majority of centres) Ca: n = 228 examination
dermatological outpatient Co: n = 1795
centres ⁄ clinics
Perea-Milla López et al.9 Spain, Granada 1987–99 37 Case–controld General population; 2 : 1 population n = 344 Cancer registry, interview
cancer registry controls matched by Ca: n = 105
age and sex Co: n = 239
 296 Occupational UV exposure and cutaneous SCC, J. Schmitt et al.
Table 1 Continued

Source population; In case–control Number of

Time Study source from which studies: method participants ⁄
References Geographical region conducteda Latitude design cases were identified used to select controls py includedb Data sourcesc
35
Masini et al. Italy, Rome 1999–2000 42 Case–control Dermatological Dermatological n = 130 Questionnaire,
outpatient patients without Ca: n = 46 physical
centres ⁄ clinics current or previous Co: n = 84 examination
skin cancer,
frequency matched
by age and sex
Mitropoulos and U.S.A., Arizona 1992–96 33 Case–controlf General population; Random digit n = 795 Cancer registry,
Norman36 cancer registry dialling, ‘block Ca: n = 404 structured
controls’, Co: n = 391 interview
frequency matched
by age and sex
Seidler et al.21 Germany, Rhineland- 1998–2003 50 Case–control General population; All other cases of n = 109 230 Cancer registry
Palatinate cancer registry cancer with Ca: n = 5041
same sex Co: n = 104 189
Zanetti et al.37 Europe (11 of 14 centres in 2001–02 45 Case–control Dermatological Male hospital controls n = 488 Interview,
BJD  2011 British Association of Dermatologists 2011 164, pp291–307

southern Europe), Turin patients; frequency matched Ca: n = 139 cancer registry
dermatological by age Co: n = 349
clinics
Marehbian et al.38 U.S.A., New Hampshire 1994–95 43 Case–control General population; Controls randomly n = 824 Cancer registry,
cancer registry selected from Ca: n = 290 interview,
driver’s licence Co: n = 534 questionnaire
registry and
Medicare ⁄ Medicaid
services; frequently
matched for
age and sex
Kenborg et al.14 Denmark 1970–2003 55 Case–control General population; Controls randomly n = 9600 Registry data
cancer registry selected from Danish Ca: 4800g (cancer
Central Person registry,
Registry, matched pension fund)
1 : 1 by age and sex
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Ca, cases; Co, Controls; SCC, squamous cell carcinoma; py, person years; NA, not applicable. aPeriod of time in which data were collected. bTotal number of participants; in case–control study n (cases
with SCC) + n (controls for cases with SCC). ce.g. Interview, questionnaire, repeated physical examination, cancer registry data. dSCC of the lip. eExcluding SCC of the lip. fNonmetastatic SCC. gUnclear,
higher numbers in Table 4.
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Table 2 Characteristics of study population and definition of occupational ultraviolet (UV) exposure

Participants’ characteristicsa

Definition of reference group Smoking Family history

(with regard to occupational status of skin cancer
References Definition of ‘occupational UV exposure’ UV exposure) Age (years) Sex (% female) Ethnicity (%) (%) (% positive)
Marks et al.12 Occupation ‘outdoors or mainly outdoors’ Occupation ‘indoors or mainly indoors’ 59 (± 12) 56 NR NR NR
Green et al.27 Occupation ‘mainly outdoors’ Occupation ‘mainly indoors’ 20–69 56 NR NR NR
Pukkala and Saarni28 Occupation as seafarer within study period General population NR NR NR NR NR
Adami et al.29 Occupation at census 1960; categorization Occupation at census 1960; categorization NR 40 NR NR NR
into outdoor, mixed indoor ⁄ outdoor, and into outdoor, mixed indoor ⁄ outdoor, and
indoor occupations by industrial hygienist indoor occupations by industrial hygienist
Hakansson et al.11 Construction workers with high individual Construction workers with no ⁄ low Mean 35 0 NR NR NR
work-related UV exposure individual work-related UV exposure
Radespiel-Tröger et al.30 Longest occupation as ‘outdoor’ worker: Longest occupation as ‘indoor’ worker; Median: NR NR NR NR
boatmen, construction workers, farmers, last occupation used if data on longest 60–79
fishery workers, forestry workers, garden- occupation were not available
ers, seamen, roof tilers Last occupation
used if data on longest occupation were
not available
Aubry and MacGibbon8 Highest quartile of occupational UV Lowest quartile of occupational UV Mean Ca: 65; Co: 34 Irish ⁄ British ⁄ Current NR
exposure exposure 65 Scottish: Ca: 48

Occupational UV exposure and cutaneous SCC, J. Schmitt et al. 297

Ca: 53 Co: 32
Co: 50
Hogan et al.31 Agricultural occupation All other occupations Mean Ca: 72; Co: Ca: 30 NR NR NR
70 Co: 32
Gafa et al.32 Working in agriculture for ‡ 10 years Working in agriculture for < 10 years or 40 or older Ca: 41 NR NR Ca: 68
working in other occupations Co: 41 Co: 5 (OR 10;
3Æ6–27Æ6)
Gallagher et al.33 Highest quartile of occupational UV Lowest quartile of occupational UV 25–79 0 Mother’s origin NR NR
exposure per year within past exposure per year within past Celtic:
10 years and ever 10 years and ever Ca: 68
Co: 53
Rosso et al.34 Highest quartile of cumulative occupational Lowest quartile of cumulative NR NR NR NR NR
UV exposure based on sun exposure index occupational UV exposure based
on sun exposure index
Perea-Milla López et al.9 Lifetime cumulative UV exposure during Lifetime cumulative UV exposure 20–70 0 NR Ever NR
work: highest quartile during work: none Ca: 98
Co: 84
Masini et al.35 ‘Outdoor work’, no further description ‘Indoor work’, no further description 33–94 Ca: 30 NR Ever Ca: 22
Co: 39 Ca: 67 Co: 0 (OR 47Æ6;
Co: 65 2Æ7–835Æ2)
 298 Occupational UV exposure and cutaneous SCC, J. Schmitt et al.
Table 2 Continued

Participants’ characteristicsa

Definition of reference group Smoking Family history

(with regard to occupational status of skin cancer
References Definition of ‘occupational UV exposure’ UV exposure) Age (years) Sex (% female) Ethnicity (%) (%) (% positive)
Mitropoulos and Occupational categories: construction, All other occupations 31–91 44 Caucasians NR NR
Norman36 farming, chemicals, auto ⁄ machines 98
Seidler et al.21 Longest or present occupation as ‘outdoor’ White collar or production workers NR NR NR NR NR
worker: winegrower, construction
workers, farmers, forestry workers,
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gardeners
Zanetti et al.37 Highest quartile of cumulative occupational No occupational UV exposure 20–75 0 Caucasians NR NR
UV exposure based on sun exposure index 100
Marehbian et al.38 Several individual occupations assessed; All other occupations 25–74 41 Caucasians: NR NR
Standard Occupational Classification (SOC) > 97
used for coding
Kenborg et al.14 Ever ‘outdoor occupation’, i.e. ‡ 40% of All other occupations (including those Mean 63Æ9 0 NR NR NR
employees spend > 50% of work involving outdoor work, but do not meet
time outdoors criteria for ‘outdoor occupation’)

NR, not reported; OR, odds ratio aIn cohort and cross-sectional studies for total study population, in case–control studies separately for cases (Ca) and (Co) controls (if reported).
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Table 3 Assessment of occupational and nonoccupational ultraviolet (UV) exposure

Measurement of occupational UV exposure Measurement of nonoccupational UV exposure

Individual Individual
exposure Period of Quantification exposure Period of time Quantification
References Data source assessed time considered of exposure Data source assessed considered of exposure
Marks et al.12 Questionnaire Yes NR NA NA NA NA NA
Green et al.27 Questionnaire Yes Present and past occupations NA Questionnaire Yes Ever Hours spent outdoors;
number of painful
sunburns
Pukkala and Saarni28 Pension fund No Age range unclear; observation Years employed NA NA NA NA
period 1960–80 as seafarer
Adami et al.29 Census ⁄ industrial No Current occupation 1960 NA NA NA NA NA
hygienist (outcome SCC 1971–89)
Hakansson et al.11 Industrial hygienist Yes Present occupation Using Likert scale NA NA NA NA
Radespiel-Tröger et al.30 Cancer registry No Longest occupation NA NA NA NA NA
Aubry and Questionnaire Yes 7–37 years prior to assessment Sun exposure index Questionnaire Yes Lifetime Sun exposure index
MacGibbon8 (weighted hours ⁄ (weighted hours ⁄
lifetime) lifetime)
Hogan et al.31 Questionnaire Yes NR NR Questionnaire Yes NR NR
Gafa et al.32 Questionnaire Yes Whole life Years working in Questionnaire Yes NR Hours ⁄ day
agriculture

Occupational UV exposure and cutaneous SCC, J. Schmitt et al. 299

Gallagher et al.33 Interview Yes Whole life (all jobs ‡ 6 Sun exposure index Interview Yes Whole life Sun exposure index
months’ duration) (weighted hours ⁄ (weighted hours ⁄
lifetime) lifetime)
Rosso et al.34 Interview Yes Whole life Sun exposure index Interview Yes Whole life Sun exposure index
(weighted hours ⁄ (weighted hours ⁄
lifetime) lifetime)
Perea-Milla López et al.9 Interview Yes Whole life Sun exposure index Interview Yes Whole life Sun exposure index
(weighted hours ⁄ (weighted hours ⁄ lifetime)
lifetime)
Masini et al.35 Questionnaire Yes NR NR Questionnaire Yes NR NR
Mitropoulos and Norman36 Interview Yes Longest occupation NA NA NA NA NA
Seidler et al.21 Cancer registry No Present and longest occupation NA NA NA NA NA
Zanetti et al.37 Interview Yes Whole life Sun exposure index Interview Yes Whole life Sun exposure index
(weighted hours ⁄ (weighted hours ⁄ lifetime)
lifetime)
Marehbian et al.38 Interview Yes Whole working life after age 15 years Years exposed Interview Yes NR Hours exposed during
warm months
Kenborg et al.14 Pension fund, No Employment history age 25–48 Years spent in NA NA NA NA
job-exposure years (lag time of 10 years) ‘outdoor occupation’
matrices

NA, not assessed; NR, not recorded; SCC, squamous cell carcinoma.
 300 Occupational UV exposure and cutaneous SCC, J. Schmitt et al.
Table 4 Qualitative and quantitative results of studies included in the systematic review

Consideration of relevant confounders in study design

and ⁄ or statistical analysis

Dose–response UV Nonoccupational
References Qualitative result relationship Quantitative result (OR, 95% CI) Age Sex sensitivity UV exposure Smoking
Marks et al.12 Nonsignificant increase in SCC risk among No 1Æ7, 0Æ9–3Æ3; outdoor vs. indoor •
outdoor workers; significant interaction of workers
the relationship between outdoor work
and SCC risk by age (P = 0Æ034): increase
in SCC risk in outdoor workers above age
55 years
Green et al.27 Nonsignificant increase in SCC risk among No SCC: 1Æ4, 0Æ8–2Æ3; outdoor vs. • • •a
outdoor workers; significantly increased indoor workers. AK: 2Æ2, 1Æ5–3Æ1;
AK risk in outdoor workers; significant > 11 vs. 0; AKs in outdoor vs.
self-selection among outdoor workers indoor workers
with underrepresentation of skin types I & II
Pukkala and Saarni28 More cases of SCC in deck officers and deck Yes 2Æ4, 1Æ3–3Æ9; SIR deck officers • •
crew than expected compared with general population
Adami et al.29 No association between outdoor occupation Unclear [Yes (females) Men 1Æ0, 0Æ9–1Æ0. Women 1Æ3, • •
and SCC occurrence in men, but No (males)] 1Æ1–1Æ6
significantly increased SCC risk in female
BJD  2011 British Association of Dermatologists 2011 164, pp291–307

outdoor workers
Hakansson et al.11 SCC of the lip significantly increased in No 2Æ2, 1Æ0–4Æ5 • • •
construction workers with high UV
exposure
Radespiel-Tröger et al.30 SCC risk significantly increased in male and NA Men 2Æ5; 1Æ4–4Æ7. Women 3Æ6, • •
female outdoor workers compared with 1Æ6–8Æ1; RR outdoor vs. indoor
indoor workers worker
Aubry and MacGibbon8 Positive association between lifetime NA 9Æ1, 2Æ0–84Æ5; occupational UV • • • •
occupational UV exposure and SCC exposure modelled as binary
occurrence variable, details NR
Hogan et al.31 Significant association between agricultural NA Men 1Æ5, 1Æ2–1Æ8. Women 1Æ8; • • •
occupation and SCC risk in both men and 1Æ2–2Æ7 Agricultural vs. other
women occupations
Gafa et al.32 Significantly increased risk of SCC in NA 2Æ4, 1Æ0–5Æ6
individuals working in agriculture for
10 years or longer
 2011 The Authors

Gallagher et al.33 Significant association between SCC Yes 4Æ0, 1Æ2–13Æ1; high vs. low mean • • •
occurrence and mean annual occupational annual occupational UV exposure
UV exposure in past 10 years; nonsignificant in past 10 years
association between SCC occurrence and
mean annual lifetime occupational
BJD  2011 British Association of Dermatologists 2011 164, pp291–307
 2011 The Authors

Table 4 Continued

Consideration of relevant confounders in study design

and ⁄ or statistical analysis

Dose–response UV Nonoccupational
References Qualitative result relationship Quantitative result (OR, 95% CI) Age Sex sensitivity UV exposure Smoking
34
Rosso et al. Outdoor work significantly associated with Yes 1Æ6, 1Æ0–2Æ5; high vs. low occupational UV • • • •
SCC occurrence exposure
Perea-Milla López et al.9 Significant positive association between No 11Æ9, 1Æ3–108Æ9; highest quartile vs. no • • • •b
cumulative occupational UV exposure and occupational UV exposure
SCC occurrence
Masini et al.35 Outdoor work significantly associated with NA 4Æ3, 1Æ6–11Æ9; outdoor work vs. indoor • •
SCC occurrence work
Mitropoulos and Norman36 No significant association between NA 1Æ4, 0Æ6–3Æ1; construction workers vs. • • •
occupation and SCC occurrence non-

Occupational UV exposure and cutaneous SCC, J. Schmitt et al. 301

high-risk occupations
Seidler et al.21 Positive association between SCC and NA 1Æ5, 1Æ2–1Æ9; male construction workers vs. • •
outdoor occupations white collar workers
Zanetti et al.37 Significant positive association between Yes 2Æ2, 1Æ1–4Æ1; highest quartile vs. no • • •
cumulative occupational UV exposure and occupational UV exposure
SCC occurrence
Marehbian et al.38 Significantly increased SCC risk among Yes 17Æ0, 1Æ7–172Æ4; male agricultural • • • • •
agricultural occupations, groundskeepers, occupations ‡ 5 years vs. never
gardeners
Kenborg et al.14 No association between outdoor occupation No 1Æ0, 0Æ8–1Æ3; SCC on head for > 10 years • • •
and SCC risk outdoor occupation vs. no outdoor
occupation

AK, actinic keratosis; CI, confidence interval; NA, not assessed; NR, not recorded; OR, odds ratio; SCC, squamous cell carcinoma; SIR, standardized incidence ratio. aAdjustment only in SCC model;
b
adjusted for leaving cigarette on lip. Bold indicates numbers used for meta-analysis.
 302 Occupational UV exposure and cutaneous SCC, J. Schmitt et al.
Table 5 Methodological quality, likelihood of bias, and limitations of studies included in the systematic reviews

Newcastle–Ottawa scale

Outcome
of Adequacy
interest Comparability of follow-
Selection Ascertainment was not of cohorts up of Assessment
Representativeness of of individual present on basis of Assessment Adequate cohorts ⁄ of individual Effect Other Direction
of exposed nonexposed occupational at start of design or of follow-up follow-up nonoccupational modification relevant of bias
References cohort cohort exposure study analysis outcome time rate adequate UV exposure explored limitations introduced

Cohort studies
Marks et al.12 • • • • •s • • s s • None
Green et al.27 • • • • •s • s • • s None
Pukkala and Saarni28 • s s • •s • • • s s None
Adami et al.29 • • s • •s • • • s s Cumulative Towards OR = 1
occupational
BJD  2011 British Association of Dermatologists 2011 164, pp291–307

exposure unclear
Hakansson et al.11 s • • • •s • • • s s Only current Towards OR = 1
occupation at
time of examination
assessed;
change of
occupation
introduces
nondifferential
misclassification
bias
Radespiel-Tröger et al.30 • • • • •s • s • s s 74% missing None
data on
occupational
exposure; missing
at random assumed
 2011 The Authors
BJD  2011 British Association of Dermatologists 2011 164, pp291–307
 2011 The Authors

Table 5 Continued

Newcastle–Ottawa scale

Comparability
of cases Ascertain- Same method
and controls ment of of exposure Assessment
on basis of individual assessment in of individual Recall Effect
Case definition Representativeness Selection of Definition design and occupational cases and Nonresponse nonoccupational bias modification other relevant Direction of
adequate of cases controls of controls analysis exposure controls rate UV exposure unlikelya explored limitations bias introduced

Case–control studies
Aubry and MacGibbon8 • s s • •• s • s • s s None
Hogan et al.31 • s • s •s s • s • s s Reference group Towards
contains individuals OR = 1
with outdoor occupation
Gafa et al.32 • • s s ss s • s • • s Inappropriate control group, Overestimation of effect
selective reporting of results
Gallagher et al.33 • • • • •s • • s • • s None
Rosso et al.34 • • • • •• s • s • s s None
Perea-Milla López et al.9 • • • s •s s • s • s s None
Masini et al.35 • s s • •s s • s • s s None
Mitropoulos • s • • •s s • s s • s Only longest Towards OR = 1

Occupational UV exposure and cutaneous SCC, J. Schmitt et al. 303

and Norman36 occupation
assessed fi
nondifferential
misclassification
Overadjustment for actinic keratoses Towards OR = 1
Seidler et al.21 • • • • •s s • • s • s 50% missing data on occupational None
exposure; missing at random assumed
Small numbers in most occupations fi
low power
Zanetti et al.37 • • s s •s • • s • s s Exclusion of potential outdoor workers Overestimation of effect
among controls fi selection bias
Marehbian et al.38 • • • s •• s • s • • s Reference group contains individuals with Towards OR = 1
outdoor occupation
Small numbers in most occupations fi low power None
Kenborg et al.14 • • • • •s s • • s • s Inadequate observation period: only participants ages Towards OR = 1
25–58 occupational exposure until age 48 considered,
average age at diagnosis 64 years
Missing information on occupational exposure in elderly Towards OR = 1
participants, nondifferential misclassification bias

• Criterion met. s Criterion not met. aRecall bias unlikely if occupation recorded.
304 Occupational UV exposure and cutaneous SCC, J. Schmitt et al.

Marks et al. 1989

Green et al. 1996
Pukkala et al. 1996
Adami et al. 1999
Hakansson et al. 2001
Radespiel-Tröger et al. 2009
Aubry et al. 1985
Hogan et al. 1990
Gafa et al. 1991
Gallagher et al. 1995
Rosso et al. 1996
Perea-Miller López et al. 2003
Masini et al. 2003
Mitropoulos et al. 2005
Seidler et al. 2006
Zanetti et al. 2006
Marehbian et al. 2007
Kenborg et al. 2010

Combined

0·75 1·0 1·5 2·0 4·0 8·0

Odds ratio

Fig 2. Results of random-effects meta-analysis for squamous cell carcinoma of the skin of individuals with outdoor occupation ⁄ occupational
ultraviolet (UV) exposure vs. indoor occupation ⁄ no occupational UV exposure.

occupational UV light exposure and SCC than studies estimat-

3

ing occupational UV light exposure solely from the job

description or job title (P = 0Æ020; adjusted model). Studies
adjusting for individual UV light sensitivity found stronger
relationships between occupational UV light exposure and SCC
2

* than studies not adjusting for this potential confounder

logOR

(P = 0Æ06). None of the other study quality criteria assessed

β = –0·0343; P<0·001 significantly influenced the study results. Publication bias was
1

not detected by regressing the study result (OR) on sample

size adjusting for study type (P = 0Æ84).
0

20 30 40 50
Latitude†
Fig 3. Relationship between latitude and strength of association
between occupational ultraviolet (UV) exposure and squamous cell
carcinoma of the skin. The circle corresponding to each study has an
area inversely proportional to the variance of the log-odds ratio. The
superimposed line is obtained by weighted regression using a
restricted maximum likelihood (REML) estimate of residual
heterogeneity variance.41 *Log-odds ratio (OR) of the relationship
between occupational UV light exposure and squamous cell carcinoma
of the skin. Absolute value of latitude.
use of a cancer registry (P = 0Æ049; adjusted model). Studies
that directly assessed individual occupational UV light expos-
ure of study participants found stronger associations between
60 Discussion
Our paper is the first meta-analysis that comprehensively sum-
marizes the published epidemiological evidence regarding the
relationship between work-related UV light exposure and the
risk of cutaneous SCC. The presented results indicate that out-
door work constitutes a relevant, independent, and robust risk
factor for the development of cutaneous SCC. Our findings are
highly relevant as currently SCC is among the most frequent
malignancies worldwide with rapidly increasing incidence rates
over past decades.1–4 Our results are biologically plausible, as
the cumulative exposure to UV radiation is the most common
and the most important known cause of cutaneous SCC.5
There are several reasons why we believe that the observed
increase in the risk for cutaneous SCC among individuals
with work-related UV light exposure compared with indoor

 2011 The Authors

BJD  2011 British Association of Dermatologists 2011 164, pp291–307

workers is an underestimation of the true association. Firstly,
only three studies8,34,38 considered the most important con-
founders of the relationship between occupational UV light
exposure and SCC occurrence, i.e. age, sex, individual UV sen-
sitivity, and individual nonoccupational UV exposure by the
study design or in data analysis. Two of these studies found
strong, statistically significant associations between occupa-
tional UV light exposure and SCC occurrence with ORs above
10,8,38 and the other study34 observed only a weak, but also
statistically significant association. Overall, studies with incom-
plete consideration of confounders found less strong associa-
tions between occupational UV light exposure and SCC
occurrence suggesting the possible presence of residual con-
founding. Green et al.27 observed significant self-selection
among outdoor workers, whereby people with fair or med-
ium complexions and a tendency to sunburn were systemati-
cally underrepresented among those in long-term outdoor
occupations. The assumption of residual confounding leading
to an underestimation of the true effect is also strengthened
by results from the presented meta-regression analysis indicat-
ing that studies adjusting for individual UV light sensitivity
found significantly stronger relationships between occupational
UV light exposure and SCC than studies not adjusting for indi-
vidual UV light sensitivity. Another source of bias towards the
null effect that was present in 14 of the 18 studies included
in the review was an imprecise definition of the reference
group, i.e. individuals not exposed to solar UV light at the
workplace. The reference group was actually not truly unex-
posed in the majority of the studies included in the review.
Five studies failed to collect information on individual expos-
ure to solar UV light at the workplace and relied exclusively
on census or registry data and ⁄or used the job description as a
proxy for occupational UV light exposure. Adami et al.29
hypothesized that the potential misclassification of exposures
that are inferred in job titles and industry categories is non-
differential but often substantial, as it may reduce and obscure
true relevant associations. Consistent with this hypothesis we
were able to show that studies directly assessing individual
occupational UV light exposure found stronger associations
between occupational UV light exposure and SCC occurrence
than studies estimating occupational UV light exposure solely
from the job description or job title. In addition to these limi-
tations of individual studies that led to an underestimation of
the true association between work-related UV light exposure
and SCC risk, other sources of bias that may have led to an
overestimation of the true association were also identified in
some of the studies included in the review: recall bias was
considered to be unlikely in six of the 12 case–control studies.
Exclusion of potential outdoor workers among controls in the
study by Zanetti et al.37 may have introduced selection bias.
Selective outcomes reporting was suspected in the study by
Gafa et al.32
Our study extends previous research by providing evidence
that the strength of the association between occupational UV
exposure and development of SCC increases with decreasing
latitude. This is biologically plausible and provides one
 2011 The Authors
BJD  2011 British Association of Dermatologists 2011 164, pp291–307
Occupational UV exposure and cutaneous SCC, J. Schmitt et al. 305
possible explanation why the Scandinavian studies by Kenborg
et al.14 and Adami et al.29 were the only studies that found no
association between occupational UV light exposure and SCC
occurrence. However, both studies that found no association
between occupational UV light exposure and SCC occurrence
also have other significant limitations: both studies did not
actually measure or assess occupational UV light exposure, but
used job titles or job descriptions as a proxy for individual UV
light exposure, harbouring the risk of introducing nondiffer-
ential misclassification bias. Additionally, the observation
period was inadequate in the study by Kenborg et al.:14 only
participants aged 25–58 with occupational exposure until age
48 were considered for the analysis concerning the relation-
ship between occupational UV light exposure and SCC occur-
rence, although the average age at diagnosis of SCC was
64 years in this population. This is problematic as the study
by Marks et al.12 reported significant interaction of the rela-
tionship between outdoor work and SCC risk by age with an
increase in SCC risk only in outdoor workers above age
55 years. Another limitation of this study is missing informa-
tion on occupational exposure in elderly participants, also
introducing nondifferential misclassification bias towards the
null effect.22
Our study followed a priori defined procedures, which also
met the criteria in the MOOSE checklist for performing a sys-
tematic review of epidemiological studies.19 Despite all the
efforts undertaken, we cannot guarantee that we identified all
relevant articles on the issue. We conducted several sensitivity
analyses that provide evidence for the robustness of our find-
ings and independence of the observed significant relationship
between occupational solar UV light exposure and SCC risk
from the study type and several study quality criteria. Another
strength of our meta-analysis is the identification of relevant
sources of heterogeneity by means of meta-regression analy-
ses. One caveat is that the results of meta-regression analyses
should be interpreted cautiously39 in that the associations
found should be considered hypothesis-generating rather than
regarded as a proof of causality.40
As discussed above, some of the individual studies included
in this review have methodological limitations, most of
which, however, cannot explain the observed association
between occupational solar UV light exposure and SCC occur-
rence, but most likely introduced bias towards the null effect.
Our findings are of the utmost relevance for occupational
medicine and public health, as substantial proportions of the
working populations are regularly exposed to solar UV light at
the workplace. Our findings may serve as a robust and reliable
evidence base to implement targeted primary prevention strat-
egies for outdoor workers. Ideally, such preventive strategies
should be designed involving all relevant stakeholders, i.e.
outdoor workers, occupational health experts, dermatologists,
health educators and industry representatives.
In Germany, our findings have already induced a discussion
about the introduction of a new occupational disease ‘SCC of
the skin among outdoor workers’, which is likely to result in
significant preventive measures for individuals with high levels
306 Occupational UV exposure and cutaneous SCC, J. Schmitt et al.
of work-related UV light exposure. Hopefully, similar public
health and health policy impact will result in other countries.
What’s already known about this topic?
• Cutaneous squamous cell carcinoma (SCC) is among the
most prevalent malignancies worldwide with steadily in-
creasing incidence rates over past decades.
• Although UV light exposure in general is an established
risk factor for the development of cutaneous SCC there
is an ongoing debate in the epidemiological and derma-
tological literature about the relationship between work-
related UV light exposure and the risk of cutaneous SCC.
What does this study add?
• This systematic appraisal of the epidemiological litera-
ture and meta-analysis clearly indicates that occupational
UV light exposure is a substantial and robust risk factor
for the development of cutaneous SCC.
• These findings are of significant public health impact as
they highlight the need for preventive measures for
individuals with high levels of work-related UV light ex-
posure.
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