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MEDICINE
REVIEW ARTICLE
The Relationship Between Occupational Sun
Exposure and Non-Melanoma Skin Cancer
Clinical Basics, Epidemiology, Occupational Disease Evaluation, and Prevention
Manigé Fartasch, Thomas Ludwig Diepgen, Jochen Schmitt, Hans Drexler
SUMMARY
Background: The cumulative effect of solar ultraviolet (UV) radiation is respon-
sible for the worldwide increase in non-melanoma skin cancer, a category that
includes squamous cell carcinoma and its precursors (the actinic keratoses) as
well as basal-cell carcinoma. Non-melanoma skin cancer is the most common
type of cancer in areas of the world with a light-skinned population. The occu-
pational exposure to UV radiation is high in many outdoor occupations; recent
studies suggest that persons working in such occupations are more likely to
develop non-melanoma skin cancer.
Methods: On the basis of a selective review of the literature, we present the
current state of knowledge about occupational and non-occupational UV expo-
sure and the findings of meta-analyses on the association of outdoor activity
with non-melanoma skin cancer. We also give an overview of the current rec-
ommendations for prevention and for medicolegal assessment.
Results: Recent meta-analyses have consistently documented a significantly
higher risk of squamous cell carcinoma of the skin among persons who work
outdoors (odds ratio [OR] 1.77, 95% confidence interval [CI] 1.40–2.22,
p<0.001). There is also evidence for an elevated risk of basal-cell carcinoma
(OR 1.43, 95% CI 1.23–1.66, p = 0.0001), but the effect is of lesser magnitude
and the study findings are not as uniform.
Conclusion: The association of occupational exposure to solar UV radiation with
squamous cell carcinoma, including actinic keratosis, has been conclusively
demonstrated. It follows that, in Germany, suspected non-melanoma skin
cancer in persons with high occupational exposure to UV radiation should be
reported as an occupational disease under § 9, paragraph 2 of the Seventh
Book of the German Social Code (Sozialgesetzbuch, SGB VII). Preventive
measures are urgently needed for persons with high occupational exposure to
UV radiation.
►Cite this as:
Fartasch M, Diepgen TL, Schmitt J, Drexler H: The relationship between
occupational sun exposure and non-melanoma skin cancer—clinical basics,
epidemiology, occupational disease evaluation, and prevention.
Dtsch Arztebl Int 2012; 109(43): 715–20. DOI: 10.3238/arztebl.2012.0715
C
utaneous squamous cell carcinomas and their
precursor lesions, actinic keratoses, as well as
basal cell carcinomas, are described as non-melanoma
skin cancer (NMSC). These disorders are among the
commonest forms of cancer in Western countries with
an incidence of around 100 per 100 000 individuals in
Europe (1, e1, e2). They are called NMSC or “white
skin cancer” to distinguish them from melanoma or
“black skin cancer”.
Most often affected are those with pale skin,
especially light-sensitive individuals with Fitzpatrick
skin types I and II (1, 2, e3).
There are no exact data from German-speaking
countries on the incidence of actinic keratosis, also
known as squamous cell carcinoma in situ, but studies
from Great Britain show a prevalence of actinic kera-
toses in patients over 70 years of age of 34% in men
and 18% in women (e4). The higher prevalence in men
is partially explained by a greater exposure to sun, in
part without protection, during the performance of
outdoor work (e5).
In many work situations employees are exposed to
natural UV radiation, often in significant (or consider-
able) amounts (3, 4). UV radiation is the single most
important cause of squamous cell carcinoma and its
precursors, as well as of basal cell carcinoma (e6).
UV-induced skin cancer is not yet recognized in
Germany as an occupational disease in accordance with
the Ordinance on Occupational Diseases (BKV,
Berufkrankheitsverordnung) (5). There is active
discussion at the present time about adding such
diseases—specifically cutaneous squamous cell
carcinoma and its precursors—to the list of recognized
occupational diseases (Attachment 1 to the BKV).
Until this is finalized, cutaneous malignancies caused
by UV exposure can be designated as “quasi occupa-
tional diseases” under § 9, paragraph 2 of the Seventh
Book of the German Social Code (Sozialgesetzbuch,
SGB VII). A document known as the “Bamberger Code
of Practice—Part 2” prepared by the Task Force for
Occupational and Environmental Dermatology (ABD,
Arbeitsgemeinschaft für Berufs- und Unweltdermato-
logie) and the German Social Accident Insurance
(DGUV, Deutsche gesetzliche Unfallversicherung)
provides guidance on assessing the causality and
Department of Clinical and Experimental Occupatioal Dermatology, Institute for Prevention and Occupa-
tional Medicine of the German Social Accident Insurance (DGUV), Institute of the Ruhr-University of
Bochum (IPA): Prof. Dr. med. Fartasch
Department of Clinical Social Medicine, Heidelberg University Hospital: Prof. Dr. med. Diepgen
Social Medicine and Health Services Research, Institute and Policlinic for Occupational and Social Medi-
cine at Technische Universität Dresden, and Center for Evidence Based Health Care (ZEGV) at the Univer-
sity Hospital Carl Gustav Carus, Dresden: Prof. Dr. med. Schmitt
Institute of Occupational and Environmental Medicine, Friedrich-Alexander-Universität Erlangen- Nürnberg:
Prof. Dr. med. Drexler
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determining pension liability when the earning capacity
has been reduced (6).
The goal of this review is to detail the role and
relative importance of workplace factors in the devel-
opment of squamous cell carcinoma and its precursors,
as well as to update information on the quantification of
UV exposure as well as the relation between occupational
and recreational UV exposure. In addition, the current
status of workplace protective measures, prevention
and occupational disease evaluation is reviewed.
Methods
The epidemiologic evidence is derived from meta-
analyses (7–9) of the relationship between occupational
solar UV exposure and squamous cell carcinoma (7, 8)
or basal cell carcinoma, respectively (9). The system-
atic reviews were carried out according to the Meta-
analysis of Observational Studies in Epidemiology
(MOOSE) group checklist (e7). The literature search
was performed in MEDLINE (PubMed) using various
groupings of MeSH terms for relevant key words
(Meta-analyses [7–9]):
●
For study type: “risk“ OR “incidence“ OR
“epidemiologic studies“ AND “carcinoma, squa-
mous cell” OR “carcinoma, basal cell” OR “skin
cancer” OR “skin neoplasm”.
●
For UV radiation exposure: “sunlight” OR “ultra-
violet rays” OR “ultraviolet light”.
●
For work-related exposure: “occupational” OR
“occupation” OR “outdoor work” OR “work” OR
“workplace”.
In addition, the current dermatology and occupation-
al dermatology guidelines and recommendations as
well as new legal exposure standards and comparative
dosimetry studies on UV exposure were all reviewed.
UV-induced cutaneous reactions
and tumor induction
Ultraviolet radiation belongs to the group of optical
radiation (wavelengths 100 nm to 1 mm). UV radiation
falls in the range between 100 nm and 400 nm and is
divided into UVC, UVB and UVA depending on wave-
length (Figure 1). Because of the ozone layer, only
UVA and UVB reach the earth’s surface; 95% of the
natural UV radiation is in the UVA range. The biologi-
cal reactions induced by UV radiation are complex and
can only be touched upon here (review [e8]). Because
of the absorption spectrum of the skin, UVA—even
though it has less energy than UVB—penetrates deeper
and causes not only epidermal damage but also dermal
changes (Figure 2, Table). Nonetheless UVB has the
most carcinogenic effect. UVA enhances the carcino-
genic effect through immunosuppression (10) and by
inducing the formation of reactive oxygen species
(ROS). These in turn damage deoxyribonucleic acid
(DNA), cell membranes and enzymes. The end result is
damage to the epidermal keratinocytes and the dermal
connective tissue (Figure 2) (review [e9].
The negative effects of UV radiation on the skin
depend on the type, duration and intensity of the UV
Warming
Drying
Radiation
Medical uses
1 nm 1 mm 1 m 1 km1 μm
Inductive warmth
Capacitive warmth
IR radiation
Diathermy
X-radiation
Radium radiation
Phototherapy
(UVA/UVB)
UV + IR
UVC UVB UVA IRA
Visible light
IRB IRC
UV IR
10
-12
10
-10
10
-8
10
-6
10
-4
10
-2
10
0
10
2
10
4
10
6
10
8
100 nm 280 315 400 780 nm 1.4 3 1 mm
Optical radiation 100 nm – 1 mm UV
FIGURE 1
Spectrum of electromagnetic radiation; UV, ultraviolet; IR, infrared
Skin
Artificial
UV radiation
Sun
Free
mediators
Benign
changes
Cell death
Somatic
mutations
Erythema
Atrophy,
depigmentation
Elastosis, wrinkles,
comedones, cysts
Acute damage
Chronic damage
Squamous cell
carcinoma, basal
cell carcinoma,
melanoma
FIGURE 2
Cutaneous consequences of acute and chronic excessive UV exposure
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exposure and can lead to acute erythema (sunburn) or
with cumulative exposure to the clinical picture of
chronic actinic damage (extrinsic photoaging) (clinical
symptoms see Table, Figure 2). Although there are
various international methods to grade the severity of
light damage (review [11]), reliable data on the
sensitivity and specificity and the role of certain
markers such as solar elastosis are not available (11,
12). Exact dose-effect relationships based on spectrum
and source of the UV radiation are not established for
humans (13).
Squamous cell carcinoma and basal cell
carcinoma secondary to occupational UV
exposure
Type of tumor and form of UV exposure
There is active discussion currently on the relationship
between occupational UV exposure and non-melanoma
skin cancer (basal cell carcinoma and squamous cell
carcinoma including precursor lesions). Although the
development of some types of melanoma shows a
certain dependence on UV exposure (14), there is insuf-
ficient data on occupational exposure so that at this
time melanomas are not under consideration as tumors
induced by occupational UV exposure.
The age-adjusted incidence of basal cell carcinoma
in Germany is estimated as 80 new cases per 100 000
individuals (2, e6, e10). This locally destructive tumor
does not metastasize and is usually surgically removed.
It appears most often in body regions with marked UV
exposure (see areas of marked exposure, Table), but
also can occur on non-exposed areas (for example,
retroauricular) so that a direct relationship to UV expo-
sure is not regularly found in exposure studies (1, 15).
Squamous cell carcinoma has an age-adjusted inci-
dence of 29 new cases per 100 000 individuals (1, e2,
e10); tumors grow in a destructive way and can
metastasize. Both squamous cell carcinomas and
actinic keratoses, which are limited to the epidermis
(carcinomata in situ), appear almost exclusively in
areas with UV exposure, especially on the head and
neck or on the décolleté, arms, backs of hands, and the
vermilion of the lip (transitional epithelium). The tran-
sition from actinic keratosis to invasive squamous cell
carcinoma is often difficult to establish (e11); thus the
presence of actinic keratoses is an indication for
therapy (16).
Exposure to UV radiation is the most important
causative exogenous factor in the development of
cutaneous squamous cell carcinoma (1). Other known
exogenous factors include arsenic, tar and other carci-
nogens as well as ionizing radiation today play a lesser
role in the development of skin cancer (e12).
The currently accepted standard when describing
UV exposure is to distinguish between cumulative con-
tinuous, intermittent, and mixed exposure patterns as
well as identifying the peaks of exposure with resultant
erythema (sunburns) (Figure 3).
The relationship between UV exposure and
cutaneous malignancies is probably different for the
various tumor types. Squamous cell carcinoma
generally develops following years of cumulative UV
exposure. Here the increased risk following years of
exposure is most easily identified (review [1]. In addi-
tion, there is a clear correlation with the latitude at
which one lives. For basal cell carcinoma, additional
factors such as the intensity of sun exposure in child-
hood and adolescence may be relevant (2).
Epidemiology
Recent epidemiological studies (review [7, 8, e13])
show that cumulative occupational exposure leads to an
increased risk for outdoor workers. The meta-analyses
(7, 8) demonstrate that the published epidemiologic
evidence consistently indicates a relevantly increased
risk (pooled odds ratio of 1.77, 95% confidence interval
1.40–2.22 [p<0.001, variance = 0.131]) for the devel-
opment of squamous cell carcinomas in individuals
with high occupational UV exposure (outdoor
workers). In this selective review, a total of 18 studies
(6 cohort studies and 12 case-control studies) were
identified that studied the relationship between occupa-
tional UV exposure and the risk of squamous cell
carcinoma.
Sixteen studies describe a positive relationship be-
tween occupational UV exposure and the development
of squamous cell carcinoma. The relationship was
statistically significant in 12 studies. Occupational ex-
posure was assessed differently in the various studies:
Typical outdoor workers (farmers, foresters, construc-
tion workers, sailors) were compared with control
groups consisting of either individuals who worked in-
doors with relatively little occupational UV exposure or
else to the general population. Although the association
was probably underestimated in some studies due to
TABLE
Benign clinical symptoms of chronic light damage
(modified from Yaar 2007 [e9]—a selection)
* Areas of maximum exposure: head and scalp (including helices, lower lip),
décolleté, shoulders, backs of hands, forearms
Benign clinical symptoms
Dry skin
Pigmentary changes:
− irregular pigmentation
− senile lentigo
− idiopathic guttate hypomelanosis
Changes in the connective tissue
– wrinkles and elastosis
Telangiectases
Purpura (easy bruising)
Comedones (Favre-Racouchot
disease) and sebaceous gland
hyperplasia
Changes in the epidermis and dermis,
especially in areas of maximum exposure*
Thickening of the skin barrier and changes in
the epidermal proliferation rate
Both increase and decrease in epidermal
melanocytes, increase in dermal melanophages
Changes in the connective tissue, especially
collagen and elastic fibers
Proliferation of small vessels often with atrophic
walls, extravasation of erythrocytes and peri-
vascular inflammation
Dilation and cornification of the superficial com-
ponent of the sebaceous follicle, proliferation of
sebaceous glands
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methodological weaknesses, one can state that the epi-
demiologic evidence points to an approximate doubling
of the risk for squamous cell carcinoma in those
individuals with extensive occupational UV exposure.
The evidence from the meta-analysis of the 24
studies (5 cohort and 19 case-control studies) also sug-
gests a significant association between outdoor work
and the risk of developing a basal cell carcinoma
(pooled odds ratio of 1.43, 95% confidence interval
1.23–1.66 [p = 0.0001) [9]). The study results are less
uniform than for squamous cell carcinoma and the ef-
fect is less clear (11 studies show a significant positive
association, 5 studies show a non-significant increase,
and 5 studies even show a non-significant risk reduc-
tion).
Dosimetric studies in selected occupational groups
Results from both international and national dosimetric
studies are available. Numerous studies from Northern
and Central Europe investigate increased UV exposure
during outdoor work. In these studies the dose
required to induce erythema (H
er
or erythema dose) is
expressed as the SED (Standard Erythema Dose) (see
Box) [e14]).
Thieden and coworkers (17) showed with dosimetric
studies that gardeners in Denmark had a 1.7 fold
increased exposure on work days because of their occu-
pation. Other publications have also proven that certain
outdoor workers such as farmers, fishermen, policemen
and sports teachers have an increased risk of skin
cancer because of increased UV exposure (18). Newer
more personalized dosimetric studies (3, 19, 20) show
that, for example, construction workers have a 4.7-fold
increased annual UV exposure compared to indoor
workers. A markedly increased exposure can also be
shown in mountain guides and ski teachers (21). Based
on the work of Knuschke et al. (3) showing that the
median estimated reference exposure of the German
population as H
er(Germany)
= 130 SED yearly, then an
outdoor worker has a 2- to 3-fold higher UV exposure.
Individual levels of solar UV exposure deviate from
the mean depending on the type of outdoor work, the
origination of the work place and the recreational activ-
ities. The causes of the variation are the duration and
intensity of the UV exposure. The intensity varies with
the work clothing, time of day, and season, as well as
the latitude, elevation and albedo (reflection potential)
of the work site.
Occupational disability laws,
workplace protection, and prevention
Protection of employees and the current legal situation
The employer is already obligated under the German
Occupational Safety and Health Act (Arbeitsschutzge-
setz) to help employees avoid or minimize damage
from excessive UV exposure through appropriate pro-
tective measures. However, there are no legal limits for
the amount of exposure to natural UV radiation.
Regarding exposure to artificial UV radiation, since
2006 there has been an exposure limit, as stated in the
Guideline 2006/25/EG of the European parliament
(radiation H
eff
30 J/m
2
over 8 hours, see Box); this value
for protection of employees from risks related to artifi-
cial optical radiation was adopted as German law on 19
July 2010 (22). The limit of exposure to artifical UV
radiation was determined to avoid acute skin damage.
Delayed effects were not considered in calculating this
value.
Primary occupational prevention
Many studies have shown that inadequate sun protec-
tion measures are utilized by outdoor workers (review
[23]).
UV exposure can be minimized in the workplace
with a variety of technical, organizational and personal
strategies (24) combined with adequate training (e15,
e16). Examples of technical measures include:
●
the use of awnings
●
planning of work schedules to reduce work during
high midday sun
●
optimal use of personal protective measures
(clothing, hats, sun glasses)
●
use of sunscreens on uncovered skin surfaces.
Many randomized clinical studies have shown that
the prophylactic use of sunscreens reduces the develop-
ment of skin cancers—especially actinic keratoses and
squamous cell carcinomas—but also melanomas (14,
e17–e21). A long-term study over 4.5 years (e17)
showed that the incidence of squamous cell carcinoma
in individuals who used sunscreens was reduced by
40% in comparison to the control group. More recent
studies have shown that one must pay very close atten-
tion to the amount of sunscreen applied. The solar
protection factor is based on the application of 2 mg of
sunscreen per cm
2
of skin. On average only 0.5 mg/cm
2
were applied—leading to an exponential decline in the
degree of protection (e22). In addition, most of the
chemical sunscreens protect against UVB but only a
few provide adequate UVA coverage (for details see
[25]).
Chronic sun-damaged
skin
= extrinsic photoaging
Cumulative
exposure
UVA
Actinic keratoses,
squamous cell carcinomas
UVB
(+ UVA)
Basal cell carcinoma (other
carcinogens, genetic factors,
types of basal cell carcinoma)
Intermittent
and
cumulative
exposure
Melanoma
(types of melanoma)
FIGURE 3
UV-induced skin
damage and skin
cancer
718
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Sunscreens cannot provide complete UV protection
and should not mislead the employee into ignoring the
use of physical protective measures (clothing) or reduc-
ing the duration of exposure.
Occupational disability laws
and disability evaluation
The significantly increased incidence of skin cancer in
outdoor workers and the epidemiologically and experi-
mentally proven relationship between UV exposure and
skin malignancies show that these disorders can result
from occupational UV exposure. Today such diseases
are recognized by the occupational disability insurance
officials in Germany as “quasi occupational diseases“
according to § 9 paragraph 2 SGB VII.
Every physician, or more specifically every derma-
tologist in Germany who suspects that a skin cancer is
due to occupational UV exposure should report this
with an Occupational Disease Notification (Berufs -
krankheiten (BK)-Anzeige) (Form F6000 of the Ger-
man Social Accident Insurance) to the responsible
worker’s compensation agency. It seems likely that
UV-induced squamous cell carcinoma including its pre-
cursors will be recognized as new occupational disease
in the List of Occupational Diseases (BK-Liste).
According to German law, a disorder can only be
recognized as an occupational disease under § 9, para-
graph 1 SGB VII and then be eligible for compensation
if a certain occupational group is exposed to “a
markedly higher degree than the rest of the popu-
lation.”
Since UV exposure is ubiquitous, to determine the
cause of a skin malignancy, the relation between occu-
pational UV exposure and that experienced during
vacation and recreational activity must be analyzed (12,
13). A multicenter study is currently developing
methods to help analyze the non-occupational and oc-
cupational UV exposure and the resulting skin damage
in individual cases. These instruments should enable a
standardized, reproducible quantification of the light
damage at sites of occupational and non-occupational
exposure. In addition, it must document (primarily
through history) the occupational/recreational
exposure/damage from UV radiation (11, 12).
The issue of induction of skin cancers through occu-
pational exposure to artifical UV radiation remains
open. There are too few epidemiologic studies avail-
able to support this assertion.
Conflict of interest statement
Prof. Diepgen has received honoraria for advisory roles and lectures from
Spirig Pharma and Leo Pharma.
Prof. Fartasch, Prof. Schmitt, and Prof. Drexler declare that no conflicts of in-
terest exist.
Manuscript received on 11 January 2012, revised version accepted on
18 April 2012.
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BOX
Definitions and terms regarding
UV radiation exposure
H
er
Dose of radiation required to induce erythema, which
takes into account the different wave lengths of solar
radiation with their varying ability to cause erythema.
Erythema weighting function s
er
(λ) after ISO
17166/CIE S 007
SED Standard Erythema Dose
Unit of the H
er
,
1 SED = 100 J/m
2
:
1.5–3 SED cause erythema in skin type II:
6 SED cause marked erythema
10 SED cause painful erythema
H
eff
Effective radiation dose
− A measurement of the amount of cutaneous radia-
tion that can produce damage. The weighting
function s (λ) (EU guideline 2006/25/EG
[2006/25/EG]) allows for the different degrees of
damage associated with different wave lengths.
− Measurements of artifical UV exposure in the work
place are usually expressed as H
eff
H
eff
30 J/m
2
in 8 hours The UV-exposure limit according to national law in
order to protect the employee from acute damage
from artificial optical radiation in the workplace.
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Corresponding author
Prof. Dr. med. Manigé Fartasch
Abteilung für klin. & exp. Berufsdermatologie
Institut für Prävention und Arbeitsmedizin der DGUV
Institut der Ruhr-Universität Bochum (IPA)
Bürkle-de-la-Camp-Platz 1
44789 Bochum, Germany
fartasch@ipa.ruhr-uni-bochum.de
@
For eReferences please refer to:
www.aerzteblatt-international.de/ref4312
KEY MESSAGES
●
Current studies show that outdoor workers have an increased risk for actinic
keratoses and squamous cell carcinomas on skin sites with occupational UV
exposure.
●
There also appears to be an increased risk for basal cell carcinoma—but the
study results are less consistent and the effects less dramatic, so that this
must remain a subject of further research.
●
At this time if the treating physician suspects an occupationally induced skin
cancer, he or she should prepare an Occupational Disease Notification (BK-
Anzeige) according to § 9 paragraph 2 SGB VII.
●
To insure uniform expertise and recognition of occupational disease, instru-
ments must be developed to compare the doses of occupational and rec-
reational UV exposure, as well as to judge the distribution and severity of
sun-damage in occupationally and recreationally exposed skin sites as well as
non-exposed sites.
●
Appropriate prevention measures should be employed to reduce the risk for
outdoor workers; these include technical and organizational measures such as
using awnings and minimizing midday sun exposure, as well as personal pro-
tective measures such as wearing appropriate clothing and headgear, and
regularly using sunscreens.
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Dtsch Arztebl Int 2012; 109(43): 715−20
MEDICINE
Deutsches Ärzteblatt International
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Dtsch Arztebl Int 2012; 109(43)
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Fartasch et al.: eReferences
I
REVIEW ARTICLE
The Relationship Between Occupational Sun
Exposure and Non-Melanoma Skin Cancer
Clinical Basics, Epidemiology, Occupational Disease Evaluation, and Prevention
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