American Journal of Epidemiology
Copyright © 1994 by The Johns Hopkins University School of Hygiene and Public Health
All rights reserved
Vol. 140, No. 8
Printed in U.S.A.
Use of Sunbeds or Sunlamps and Malignant Melanoma in
Southern Sweden
Johan Westerdahl,1 Hakan Olsson,2 Anna Masback,3 Christian Ingvar,1
Nils Jonsson,3 Lars Brandt,2 Per-Ebbe Jonsson,1 and Torgil Moller4
melanoma; ultraviolet rays
(1). Exposure to sunlight is believed to be
an important risk factor for the development of malignant melanoma (2). Casecontrol studies have implied that melanoma
patients have suffered sunburns more often
than have controls (3-5).
Until recently, little attention has been
paid to the possible association between the
use of sunbeds or sunlamps and malignant
melanoma, and the results so far are inconsistent. Case reports have suggested such a
relation (6, 7). In two case-control studies,
Swerdlow et al. (8) and Walter et al. (9)
have pointed out an association between
exposure to sunbeds or sunlamps and malignant melanoma. In four other casecontrol studies, no significant risk was
found (5, 10-12).
Malignant melanoma shows the most
pronounced increase of all malignancies in
Sweden. Between 1970 and 1989, the mean
increase in the age-standardized cancer incidence rate was 5.2 percent per year for
men and 3.7 percent per year for women
Received for publication November 2, 1993, and in
final form June 20, 1994.
Abbreviations: Cl, confidence interval; OR, odds
ratio.
1
Department of Surgery, University Hospital,
S-221 85 Lund, Sweden.
2
Department of Oncology, University Hospital,
S-221 85 Lund, Sweden.
3
Department of Pathology, University Hospital,
S-221 85 Lund, Sweden.
4
Southern Swedish Regional Tumor Registry,
University Hospital, S-221 85 Lund, Sweden.
Reprint requests to Dr. Johan Westerdahl, Department of Surgery, University Hospital, S-221 85 Lund,
Sweden.
691
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In a population-based, matched case-control study from the South Swedish Health
Care Region, which has the highest risk for melanoma in Sweden, the relation between
the use of sunbeds or sunlamps and malignant melanoma was investigated . Between
July 1, 1988, and June 30, 1990, a total of 400 melanoma patients and 640 healthy
controls aged 15-75 years answered a comprehensive questionnaire containing different epidemiologic variables. Questions regarding the use of sunbeds or sunlamps
were included. The odds ratio for developing malignant melanoma after ever having
used sunbeds or sunlamps was 1.3. Considering all age groups, the odds ratio was
significantly elevated after exposure more than 10 times a year to sunbeds or sunlamps (odds ratio (OR) = 1.8). When the study was restricted to patients and controls
younger than age 30 years because the use of tanning devices is much more common
among young persons, the odds ratio was higher (OR = 7.7 for more than 10 times a
year vs. none). These findings were independent of constitutional factors and factors
regarding sun exposure. A dose-response relation was evident. Furthermore, among
melanoma patients in this young age group, the ratio of females to males was
significantly higher than in older patients. When different melanoma presentation sites
were considered, only lesions of the trunk were significantly associated with sunbed
or sunlamp use (OR = 4.2 for more than 10 times a year vs. none). Am J Epidemiol
1994;140:691-9.
692
Westerdahl et al.
MATERIALS AND METHODS
The study identified 509 patients (272
females, 53.4 percent; 237 males, 46.6 percent), aged 15-75 years, in the South Swedish Health Care Region (around the 56th
latitude, the region with the highest risk of
malignant melanoma in Sweden (1)) with a
first diagnosis of invasive malignant melanoma between July 1, 1988, and June 30,
1990, according to the population-based
Regional Tumor Registry. There are about
1.5 million residents in this region. The
population is ethnically quite homogenous.
The background level of ultraviolet radiation is low. Because of the Swedish system
of double reporting to the Cancer Registry,
the risk of underregistration is small (less
than 3 percent) (14). Information from the
Tumor Registry about the presentation site
of the tumor was used.
The permission of the physician responsible for the treatment of the patient was
sought. In 22 cases, the physicians did not
respond, and we did not contact the patients. Of the remaining patients (n =
487), 33 were considered ineligible by the
treating physician (21 were ineligible for
psychologic reasons, four had not been
fully informed about their diagnosis, four
had metastases, two were deceased, one
had moved, and one did not want to
participate).
The remaining 454 patients (211 males
and 243 females) were mailed a comprehensive questionnaire including different
epidemiologic variables (constitutional factors, family history, educational level, medical history, medicaments, ultraviolet radi-
ation exposure, smoking habits, alcohol
use, and use of oral contraceptives or other
hormonal treatment) within 2 months after
diagnosis. A total of 403 patients (88.8 percent; 196 of 211 males, 92.9 percent; 207 of
243 females, 85.2 percent) responded to the
questionnaire. Three of these were found to
have no matched control and were thus
excluded.
During the same time period, 913 healthy
controls (427 males and 486 females), randomly selected from the National Population Registry of residents of the South
Swedish Health Care Region, were mailed
the same questionnaire. A total of 707 controls (77.4 percent) responded. Two controls were matched to each patient by sex,
age (within a year), and parish. Sixty-seven
of these were found to have no matched
case and were thus excluded.
The following information was collected
with regard to ultraviolet radiation: sunbathing habits; vacations spent in sunny
places (places visited for sunbathing and
for skiing); number of painful (severe) sunburns and age at the time; episodes of blistering sunburn (sun blisters); formation of
ulcera due to excessive sun exposure (sun
ulcera); the use of sunscreen agents; outdoor employment; and duration of each residential period in the Mediterranean or
a similarly located country during the 10year period before interview. For cases and
controls, questions concerning exposure to
sunbeds or sunlamps included: "Have you
ever used or do you ever use sunbeds or
sunlamps? If yes, how often (number of
times per year)?"
Questions were also asked regarding constitutional factors, including number of
nevi, number of raised nevi (on the left
arm), freckles, hair color, and eye color.
Family history of malignant melanoma and
other tumors was also examined.
Histopathologic sections were reviewed,
and the characteristics were recorded by
two pathologists (A. M. and N. J.). All of
the 25 reported melanoma patients younger
than age 30 years were found to have invasive malignant melanoma. Among the individuals older than age 30 years, 100 ran-
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Because of the fashion of tanning in
Sweden and other industrialized countries, where sunshine is relatively sparse,
tanning devices have become increasingly
popular during recent years. In a study from
Belgium, exposure to sunbeds or sunlamps
has been shown to be particularly common
among young persons (13). The aim of this
study was to investigate whether such exposure may be associated with malignant
melanoma.
Sunbeds or Sunlamps and Malignant Melanoma 6 9 3
sent was sought from the treating physician,
the patient, and the healthy control.
RESULTS
In figure 1, the use of sunbeds or sunlamps among controls in different age
groups is demonstrated. Among controls
younger than age 30 years, 46 percent (95
percent confidence interval (CI) 30-63)
had ever used sunbeds or sunlamps (females: 56 percent (95 percent CI 37-75);
males: 12 percent (95 percent CI 0—35)). In
controls older than age 30 years, 24 percent
(95 percent CI 21-27) had ever used sunbeds or sunlamps (females: 31 percent (95
percent CI 26-36); males: 16 percent (95
percent CI 12-20)). The difference between
the younger and the older age groups was
statistically significant. Women in both age
groups were significantly more exposed
than men.
Of the 400 melanoma patients (205 females, 51.2 percent; 195 males, 48.8 percent) included in the analyses, 25 (20 females, 80 percent; five males, 20 percent)
were younger than age 30 years. The ratio
of women to men among malignant melanoma patients younger than age 30 years
was significantly higher than among the
older patients (p < 0.01).
% exposed to sunbeds/sunlamps
ppmalo rrtntrnlQ
— rcHiaic ^uiiuuio
- Male controls
806040-
<'
1
T
1
"1
1
1
4
1
200
T
1
1
•
l
1
I
i
1
15-24
25-34
35-44
45-54
>54
Age groups
FIGURE 1. Age-specific exposure to sunbeds or sunlamps among controls in a matched case-control study of
malignant melanoma in the South Swedish Health Care Region between 1988 and 1990. The estimated percentages are given with 95% confidence intervals.
Downloaded from http://aje.oxfordjournals.org/ at Pennsylvania State University on May 17, 2016
domly selected cases were reviewed, and
all were found to have invasive malignant
melanoma.
The use of sunbeds or sunlamps was categorized into four levels: never; 1-3 times a
year; 4-10 times a year; and more than 10
times a year.
Cases with a primary tumor site on the
extremity or head and neck region were
compared with cases with melanoma of the
trunk.
Odds ratios were computed, based on
matched pairs, using both univariate and
multivariate methods. In the multivariate
analyses, conditional logistic regression
was used. A p value of less than 0.05 was
considered significant, and 95 percent confidence intervals were used. The interaction
between age and the use of sunbeds or
sunlamps was studied both by a stratified
analysis of different age categories and by
using a multiplicative interaction term in
the model. The statistical program STATA
was utilized (Computing Resource Center,
Santa Monica, California). Occasional
missing values for some variables caused a
slight variation in the numbers of cases and
controls used for each analysis.
The study was approved by the Ethical
Committee of the Medical Faculty of Lund
University, Lund, Sweden. Informed con-
694
Westerdahl et al.
than 10 times a year to sunbeds or sunlamps
vs. never (table 4). A dose-response relation was evident.
Analyses adjusted for other constitutional
factors and/or factors regarding exposure to
sunlight gave essentially the same odds
ratios.
DISCUSSION
The aim of this research was to investigate whether exposure to sunbeds or sunlamps is associated with malignant melanoma. The results demonstrate that the odds
ratio for developing malignant melanoma
was significantly elevated after exposure
more than 10 times a year. The odds ratio
was higher when the study was restricted to
persons younger than age 30 years. Lesions
of the trunk were strongly associated with
the use of sunbeds or sunlamps, while lesions of the extremity or head and neck
were not. Furthermore, among melanoma
patients younger than age 30 years, the
proportion of females to males was significantly higher than in older patients.
We decided to focus the study on persons
younger than age 30 years because exposure to sunbeds or sunlamps has been
shown to be particularly common among
young persons (13). A similar usage pattern
was also demonstrated in this study.
The sunlamps in use before the late
1970s produced significant fractions of ultraviolet B (wavelengths, 280-320 nm).
Because of government regulations, these
"old" devices are no longer sold. The sunbeds or sunlamps currently on the market
produce mainly ultraviolet A (wavelengths,
320-400 nm), but also produce a small
TABLE 1. Case-control comparison of exposure to sunbeds or sunlamps in individuals younger than age
3 years in a matched case-control study of malignant melanoma in the South Swedish Health Care
Region between 1988 and 1990
Cases (n = 25)
Controls (n = 35)
Exposure to sunbeds or sunlamps
No.
Never
Ever
8
17
%
32
68
No.
19
16
%
54
46
Adjusted
odds ratio*
1.0
2.7
95%
confidence
interval
0.7-9.8
* Adjusted for history of sunburns, blond hair color, red hair color, raised nevi, and history of frequent sunbathing during the
summer.
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The odds ratio for developing malignant
melanoma after ever having used sunbeds
or sunlamps was 1.3 (95 percent CI 0.91.8), adjusted for history of sunburns, blond
hair color, red hair color, raised nevi, and
history of frequent sunbathing during the
summer. In individuals younger than age 30
years, the odds ratio was higher (adjusted
odds ratio (OR) = 2.7, 95 percent CI 0.79.8) (table 1).
When all cases were considered, an elevated odds ratio for the disease after exposure more than 10 times a year to sunbeds
or sunlamps was found, adjusted for family
history of malignant melanoma, sunburns,
history of frequent sunbathing during the
summer, and some host factors (table 2). As
can be seen, significantly elevated odds ratios were also found for history of sunburns, red hair color, blond hair color, number of raised nevi, and family history of
malignant melanoma.
In an analysis of exposure to sunbeds or
sunlamps by site of melanoma, lesions of
the trunk were significantly associated with
the use of sunbeds or sunlamps (adjusted
OR = 4.2, 95 percent CI 1.6-11.0 for more
than 10 times a year versus never) (table 3).
This association, however, was not found
for lesions of the extremity or head and
neck region.
The age interaction was studied by modeling age and the use of sunbeds or sunlamps as a continuous interaction term
giving a p value of 0.06.
When analyses of different age strata
were performed, melanoma patients
younger than age 30 years demonstrated the
highest odds ratio (adjusted OR = 7.7, 95
percent CI 1.0-63.6) for exposure more
Sunbeds or Sunlamps and Malignant Melanoma
695
TABLE 2. Odds ratios for developing malignant melanoma in relation to use of sunbeds or sunlamps,
history of sunburns, some constitutional factors, and family history of malignant melanoma in a matched
case-control study of malignant melanoma in the South Swedish Health Care Region between 1988 and
1990
No. of
cases
No. of
controls
282
44
479
67
30
41
55
33
History of sunburns
No
Yes
233
158
437
199
1.0t
Blond/fair hair color
No
Yes
366
32
601
29
1.0t
Red hair color
No
Yes
379
18
615
15
332
68
576
64
1-0t
History of malignant
melanoma in immediate family
No
Yes
368
29
604
33
1-0t
Sunbathing frequently
during the summer
(April-September)
No
Yes
301
99
501
139
Factor and category
No. of raised nevi
None
95%
confidence
interval
p value
Test for trend
p value
1.0t
1.1
1.1
1.8
1.5
1.9
0.7-1.9
0.7-1.9
1.0-3.2
0.23T-
1.1-1.9
0.007
1.1-3.5
0.03
1.1-5.1
0.03
1.1-1.6
0.04
1.0-3.3
0.05
0.9-1.7
0.25
0.06
i.ot
2.4
1.3
1.8
1-0t
1.2
* Adjusted odds ratios obtained from a model that contained all other variables included in this table.
t Reference category.
t p value based on likelihood ratio test.
fraction of ultraviolet B because ultraviolet
B is essential for a longer-lasting tan. In our
study, no information was available on the
types of lamp or sunbed used, but we believe that people in the young age group
were mostly exposed to "new" devices producing mainly ultraviolet A. However, if an
effect of age at start was present, there
exists a possibility that the elevated odds
ratio in the younger age group may have
resulted from exposure to old devices at a
very early age, during the 1960s and early
1970s.
Our results are in accordance with previous reports from Scotland (8) and Canada
(9). These two studies showed a significant
association between the use of sunbeds or
sunlamps and melanoma, with a higher risk
for longer duration of use and in persons
exposed more than 5 years before diagnosis. Interestingly, a higher risk was associated with domestic use of sunbeds or sun-
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No. of exposures to
sunbeds or sun
lamps (times/year)
Never
1-3
4-10
>10
Adjusted
odds ratio*
696
Westerdahl et al.
TABLE 3. Adjusted odds ratios for subgroups off melanoma by body sitte in relation to use of sunbeds
or sunlamps in a matched case-control study of malignant melanoma in the South Swedish Health Care
Region between 1988 and 1990
Factor and category
No. of
cases
No. of
controls
Adjusted
odds ratio*
95%
confidence
interval
p valuef
Test for trend
(p value)
Primary melanoma on the trunk
No. of exposures to
sunbeds and sun
lamps (times/year)
Never
97
14
4-10
>10
9
15
172
22
16
9
1.0*
1.1
1.3
4.2
0.5-2.2
0.6-3.2
1.6-11.0
0.015
0.04
0.20
0.83
Primary melanoma on the exrtremity or he ad and neck
No. of exposures to
sunbeds or sun
lamps times/year)
Never
1-3
4-10
>10
156
27
252
37
18
17
33
24
1.0*
1.1
1.1
1.1
0.6-2.0
0.6-2.1
0.6-2.3
•Adjusted for history of sunburns, blond/fair and red hair color, raised nevi, family history, and history of frequent sunbathing
during the summer.
t p value on liklihood ratio test.
t Reference category.
lamps. Although a nonsignificant increase
in risk was found for subjects first exposed
before age 30 years, Swerdlow et al. (8) did
not see an overall relation to age. Our results imply an age effect with a high exposure and a high odds ratio in young people.
This has not been properly addressed in
previous studies, and therefore the estimated risks may have been underestimated.
The higher odds ratio in individuals
younger than age 30 years may be due to
the high exposure in this age group per se,
or it may be an age at start effect, with the
skin of a young person being more susceptible to ultraviolet radiation than the skin of
an older person. It is likely that among
subjects over age 30 years some first used
sunbeds or sunlamps before age 30 years.
Unfortunately, the questionnaire does not
allow us to find out when these products
were first used. Four additional casecontrol studies have reported briefly on this
issue, and they have not found any significantly elevated risk (5, 10-12). However,
in these studies, only a small percentage of
subjects had ever used sunbeds and/or sun-
lamps, so the statistical power to show a
small risk elevation may have been insufficient. The rate of use of sunbeds or sunlamps in our study as well as in the other
two studies that showed an association with
melanoma (8, 9) was higher.
Only lesions of the trunk were significantly associated with use of sunbeds or
sunlamps. In a previous report, Walter et al.
(9) suggested a slightly stronger effect for
lesions of the face, head, neck, and arms.
However, in their paper, the odds ratios for
lesions of the trunk were the only ones that
were significantly elevated. We have no
specific data on what parts of the body were
exposed to sunbeds or sunlamps, but since
the common practice in Sweden is a wholebody exposure for 20-30 minutes, excluding the genital region and the eyes, it seems
likely that the trunk is most often exposed
whenever these devices are used. On the
other hand, a study by Stierner et al. (15)
has shown that ultraviolet exposure might
play a role in melanoma development not
only in exposed but also in covered skin.
One interpretation of our results is that the
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1-3
Sunbeds or Sunlamps and Malignant Melanoma
697
TABLE 4. Odds ratios for developing malignant melanoma in relation to use of sunbeds or sunlamps in
different age groups in a matched case-control study of malignant melanoma in the South Swedish
Health Care Region between 1988 and 1990
Factor and category*
No. of
cases
No. of
controls
Adjusted
odds ratiot
95%
confidence
interval
p value!
Test for trend
(p value)
0.5-8.0
1.0-63.6
0.09
0.02
0.7-1.6
0.7-2.7
0.21
0.69
0.6-3.3
0.4-10.1
0.23
0.16
Patients younger than age 30 years
>10
8
19
1.0§
9
8
13
3
2.0
7.7
Patients between ages 30 and 60 years
No. of exposures to
sunbeds or sun
lamps (times/year)
Never
1-10
>10
142
51
24
230
90
31
1.0§
1.0
1.4
Patients older than age 60 years
No. of exposures to
sunbeds or sun
lamps (times/year)
Never
1-10
>10
139
233
14
5
19
3
1.0§
1.4
2.1
* Due to the small number of individuals, the use of sunbeds or sunlamps was categorized into only three levels in this
young age group.
t Adjusted for history of sunburns, blond/fair and red hair color, raised nevi, and history of frequent sunbathing during the
summer.
t p value based on liklihood ratio test.
§ Reference category.
skin of the trunk may be less adapted to
ultraviolet radiation than the skin of, for
instance, the face and the arms. Our material was too small to allow site-specific
analyses in different age groups, and for
this reason the analysis was limited to the
most common sites (trunk and extremity or
head and neck). In two additional studies
(8, 11), no effects of sunbed or sunlamp
exposure at particular body sites were
found. In one of them, as mentioned above,
the statistical power was probably insufficient (11).
A possible causal relation between malignant melanoma and the use of tanning
devices is supported by the evident doseresponse relation and the higher odds ratio
found among young, for whom the use of
sunbeds or sunlamps was especially common. In addition to the epidemiologic evidence presented, ultraviolet B is known to
be a potent carcinogen (16, 17) and, although less well studied, ultraviolet A radiation has also been shown to be carcinogenic in animals (18, 19). In humans, it has
been suggested that ultraviolet A sunbeds
may cause melanocytic lesions with malignant potential (20, 21). Furthermore, there
is quite good evidence that 8-methoxypsoralen plus ultraviolet radiation is carcinogenic in humans (22) and also that ultraviolet A radiation is probably carcinogenic
(23).
Our results for exposure to sunbeds or
sunlamps were based on average past and
present use. The number of times per year
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No. of exposures to
sunbeds or sun
lamps (times/year)
Never
1-10
698
Westerdahl et al.
Artificial ultraviolet light has been used
for many years therapeutically, e.g., treating a wide range of skin disorders, vitamin
D deficiency, and neonatal jaundice. Since
the late 1970s, exposure to sunbeds or sunlamps has expanded rapidly due to the fashion of tanning. If the use of tanning devices
is responsible for at least a proportion of the
increase in the incidence of malignant melanoma, this knowledge may provide important opportunities for prevention. Further
studies, both retrospective and prospective,
addressing the issue are needed to give detailed information about exposure, ageexposure relation, duration, and wavelengths.
ACKNOWLEDGMENTS
Supported by grants from the Swedish
Cancer Society and the Medical Faculty of
Lund University, Lund, Sweden.
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was thus possibly based on the average of
very different numbers for different
periods. This may have introduced nondifferential misclassification of exposure, and
in that case, rather reduced our estimated
odds ratios. In future studies, measurements
of age when these products were first used,
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probably give additional information. The
results are unlikely to be biased since the
study was population based, and since,
without knowing our hypothesis, a large
percentage of the cases and controls answered the comprehensive questionnaire,
which asked about a variety of different
epidemiologic variables. At the time when
cases and controls answered the questionnaire (1988-1990), the general population
was unaware of a possible relation between
the use of sunbeds or sunlamps and the
development of malignant melanoma. We
therefore do not think that cases have reported their exposure to sunbeds or sunlamps differently than healthy controls.
Furthermore, reported smoking habits,
which are the object of health concern
among the general population, did not differ between cases and controls, reducing
the likelihood of recall bias. We have no
reason to believe that nonresponders have
seriously biased our results. Moreover, adjustments for possible confounders (constitutional factors, factors regarding ultraviolet radiation exposure and reaction, and
family history of melanoma) gave essentially the same odds ratios. However, when
the study was restricted to cases and controls younger than age 30 years, the material was too small to allow sex-specific
case-control comparisons. A follow-up
study addressing people younger than age
30 years is therefore in progress at our
institution.
Sunbeds or Sunlamps and Malignant Melanoma
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