Content uploaded by Elizabet Saes da Silva
Author content
All content in this area was uploaded by Elizabet Saes da Silva on Mar 09, 2019
Content may be subject to copyright.
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
doi:10.1684/ejd.2018.3251
186 EJD, vol. 28, n◦2, March-April 2018
To cite this article: Silva Esd, Tavares R, Paulitsch Fds, Zhang L. Use of sunscreen and risk of melanoma and non-melanoma skin cancer: a systematic review and
meta-analysis. Eur J Dermatol 2018; 28(2): 186-201 doi:10.1684/ejd.2018.3251
Clinical report Eur J Dermatol 2018; 28(2): 186-201
Elizabet saes da SILVA1
Roberto TAVARES2
Felipe da silva PAULITSCH3
Linjie ZHANG4
1Physiotherapy and Dermatology Clinic,
Postgraduate Program in Public Health,
Faculty of Medicine, Federal University of
Rio Grande, Rio Grande-RS, Brazil
2Faculty of Medicine, Federal University of
Rio Grande, Rio Grande-RS, Brazil
3Postgraduate Program in Public Health,
Faculty of Medicine, Federal University of
Rio Grande, Rio Grande-RS, Brazil
4Postgraduate Program in Public Health and
Postgraduate Program in Health Sciences,
Faculty of Medicine, Federal University of
Rio Grande, Rio Grande-RS, Brazil
Reprints: L. Zhang
<lzhang@furg.br>
Article accepted on 28/08/2017
Use of sunscreen and risk of melanoma
and non-melanoma skin cancer:
a systematic review and meta-analysis
Background: The use of sunscreen is a key component of public health
campaigns for skin cancer prevention, but epidemiological studies have
raised doubts on its effectiveness in the general population. Objectives:
This systematic review and meta-analysis aimed to assess the association
between risk of skin cancer and sunscreen use. Materials & methods:
We searched PubMed, BIREME and Google Scholar from inception
to May 17, 2017, to identify observational studies and controlled tri-
als. We used a random-effects model for conventional and cumulative
meta-analyses. Results: We included 29 studies (25 case-control, two
cohort, one cross-sectional, and one controlled trial) involving 313,717
participants (10,670 cases). The overall meta-analysis did not show a sig-
nificant association between skin cancer and sunscreen use (odds ratio
(OR) = 1.08; 95% CI: 0.91-1.28, I2= 89.4%). Neither melanoma (25
studies; 9,813 cases) nor non-melanoma skin cancer (five studies; 857
cases) were associated with sunscreen use, with a pooled OR (95% CI)
of 1.10 (0.92-1.33) and 0.99 (0.62-1.57), respectively. The cumulative
evidence before the 1980s showed a relatively strong positive association
between melanoma and sunscreen use (cumulative OR: 2.35; 95% CI:
1.66-3.33). The strength of the association between risk of skin can-
cer and sunscreen use has constantly decreased since the early 1980s,
and the association was no longer statistically significant from the early
1990s. Conclusions: While the current evidence suggests no increased
risk of skin cancer related to sunscreen use, this systematic review does
not confirm the expected protective benefits of sunscreen against skin
cancer in the general population.
Key words: sunscreen, skin cancer, melanoma, systematic review,
meta-analysis
Skin cancer is one of the most common malignan-
cies in the world and is an important public health
concern. The incidence of both melanoma and non-
melanoma skin cancer has increased over the past decades
[1, 2]. Globally, around 350,000 melanomas and 13 mil-
lion non-melanoma skin cancers occur each year leading
to approximately 81,000 deaths [3,4]. In the Unites States,
the average annual number of adults treated for skin cancer
increased from 3.4 million in 2002-2006 to 4.9 million in
2007-2011 [5]. During the same period, the average annual
total cost for skin cancer increased from $3.6 billion to $8.1
billion.
Exposure to ultraviolet (UV) radiation from sunlight is
considered a major modifiable environmental risk factor
for skin cancer [6]. Therefore, primary prevention of skin
cancer focuses on reducing UV exposure through sun pro-
tection behaviours. The use of sunscreen is thought to be an
important adjunct to other types of protection against UV
radiation from sunlight, and is a key component of pub-
lic health campaigns for skin cancer prevention. However,
epidemiological studies have yielded conflicting informa-
tion about the relationship between risk of skin cancer
and use of sunscreen. Some studies [7-11] show that reg-
ular sunscreen use could significantly reduce the risk of
skin cancer while other studies [12-20] report an increased
risk of skin cancer related to sunscreen application. Four
previous systematic reviews have assessed the associa-
tion between risk of melanoma and sunscreen use [21-24].
Despite the differences in the number of included studies
and some inconsistencies in data extraction, all four reviews
show no significant overall association between risk of
melanoma and use of sunscreen. However, non-melanoma
skin cancer, which represents more than 90% of all cases
of skin cancer [4, 25], has not been addressed in previous
reviews.
We conducted this systematic review and meta-analysis
of observational and experimental epidemiological stud-
ies to assess the relationship between risk of skin cancer
(melanoma and non-melanoma) and sunscreen use in adults
and children. Besides the conventional meta-analysis, we
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
EJD, vol. 28, n◦2, March-April 2018 187
performed cumulative meta-analysis to track how the body
of evidence has shifted over time. We also explored the
possible reasons for conflicting results across studies. We
hypothesized that the strength and direction of the associ-
ation between risk of skin cancer and sunscreen use may
have changed significantly over the last three decades.
Methods
We followed the PRISMA (Preferred Reporting Items for
Systematic Reviews and Meta-Analyses) guidelines [26]
to conduct and report this review. The review protocol was
completed in 2015 and approved by a panel of experts,
consisting of two epidemiologists and one dermatologist.
Databases and search strategy
We searched PubMed, Google Scholar, and the Virtual
Health Library of the Latin American and Caribbean Center
on Health Sciences Information (BIREME), which con-
tains Medline, LILACS, and more than 20 other databases
(http://bvsalud.org). All databases were initially searched
from inception until November 30, 2015, with no language
restrictions. We updated the literature search on May 17,
2017. We used the following search terms for PubMed:
(sunscreen OR sunblock OR “suntan lotion” OR “sunburn
cream” OR “sun cream” OR “block out” OR “solar pro-
tector”) AND (“skin cancer” OR “skin tumor” OR “skin
neoplasm” OR melanoma OR “basal cell carcinoma” OR
“squamous cell carcinoma”). We used “human species” as a
search limit. For Google Scholar and BIREME, we used the
following search strategy: sunscreen AND (“skin cancer”
OR melanoma OR “basal cell carcinoma” OR “squamous
cell carcinoma”). Different types of articles (case-control,
cross-sectional, cohort and controlled trial) were used as
search limits on BIREME. Given the excessive number of
records on Google Scholar, we searched only the titles of
articles. We examined the reference lists of retrieved pri-
mary studies and systematic reviews to identify additional
relevant studies.
Selection of studies
To be included in this review, studies had to meet all of the
following criteria: (1) Study design: observational studies
(case-control, cross-sectional or cohort) or controlled tri-
als; (2) Participants: adults, children or both; (3) Exposure
of interest: use of sunscreen classified into two or more
categories according to frequency of use; (4) Outcomes:
any type of skin cancer (melanoma, basal cell carcinoma or
squamous cell carcinoma).
Three review authors independently assessed the titles and
abstracts of all citations identified by the searches. The
definitive inclusion of studies was made after reviewing
the full-text articles.
Data extraction
Two review authors independently extracted the data from
each study using a standardized data extraction form. We
extracted the following data: (1) Study characteristics: name
of the first author, year of publication, country and set-
ting of study and study sponsor; (2) Participants: age,
gender, inclusion and exclusion criteria, type of sampling
and sample size; (3) Methods: study design, classifica-
tion of exposure (sunscreen use), definition of outcomes
(melanoma, basal cell carcinoma, and squamous cell car-
cinoma), instruments for data collection or data source,
potential confounders, and statistical analysis methods; and
(4) Results: for case-control studies: the number of cases,
number of controls, number of exposed and non-exposed in
each group, crude and/or adjusted odds ratio (OR), and 95%
confidence intervals (95% CI); for cross-sectional studies
and cohort studies: the total number of participants, number
of participants in exposed and non-exposed groups, num-
ber of persons with skin cancer in each group, crude and/or
adjusted relative risk (RR) and 95% CI; for randomized
controlled trials: the number of participants in the interven-
tion and control groups, number of persons with skin cancer
in each group, RR, and 95% CI.
We obtained the altitude (meters from sea level) and lati-
tude (degrees from the equator) of the study setting from
MyGeoPosition.com (http://mygeoposition.com). For mul-
ticentre studies, we used only geographical data from the
coordinating centre.
Study quality assessment
Two review authors independently assessed the quality of
each study according to the criteria of the National Institutes
of Health (NIH) [27, 28]. The study quality was rated good,
fair or poor, mainly based on the potential risk of selection
bias, information bias, measurement bias, and confounding
factors.
Statistical analysis
We used the random-effects model for conventional and
cumulative meta-analysis. The association between risk of
skin cancer and sunscreen use was assessed by pooled OR
and 95% CI. When RR and 95% CI were used as the mea-
sures of association in the primary studies, we estimated
the OR and 95% CI by reconstructing a 2 ×2 contingency
table. If there were no available data for reconstruction, we
used the RR and 95% CI for the meta-analysis given that
the RR is close to the OR when the outcome is a relatively
uncommon event such as skin cancer. For the overall meta-
analysis, we combined two or more categories of sunscreen
use as a single category “sunscreen use”, compared to the
reference category “no or rare use.
We assessed the heterogeneity of results between studies
using I2statistic that ranges from 0% to 100%, with values
of 25%, 50%, and 75% corresponding to low, moderate,
and high heterogeneity, respectively [29].
To investigate the possible sources of heterogeneity, we
conducted a prior subgroup analyses based on type of skin
cancer, study design, sampling method, control for con-
founding factors, age group, date of data collection, latitude
of study location, and comparison of the frequency of sun-
screen use. We also conducted a post-hoc subgroup analysis
according to study quality. We conducted meta-regression
to assess the influence of geographical factors (altitude and
latitude) of study location on the sunscreen effects.
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
188 EJD, vol. 28, n◦2, March-April 2018
Full-text articles assessed
for eligibility ( n = 117)
Records identified through
databases and screened
PubMed (n = 1509)
BIREME (n = 66)
30 papers reporting 29 studies
included in the review
Excluded on basis of
titles and abstracts
(n = 1619)
Additional studies
identified from the
reference lists of
retrieved studies and
systematic reviews
(n = 1) Articles excluded (n = 88)
- Other outcomes (n = 70)
- Other types of articles (n = 5)
- Insufficient data (n = 5)
Duplicates (n = 8)
Figure 1. PRISMA flow diagram of study selection showing the process of identification, screening, assessment for eligibility,
and inclusion of studies.
We assessed publication bias using a funnel plot and
Egger’s test. All meta-analyses were performed using Stata
version 11.0 (Stata-Corp, College Station, TX, USA).
Results
The search strategy identified 1,736 records from PubMed,
BIREME and Google Scholar, and 29 articles met the
inclusion criteria. One additional paper was found through
reviewing the reference lists of systematic reviews. Thus, a
total of 30 papers [7-20, 30-45] reporting 29 studies were
included in the review (figure 1). Table 1 summarizes the
characteristics of the 29 included studies, of which 28 were
observational studies (25 case-control, two cohort, and one
cross-sectional) and one was a randomized controlled trial.
A total of 313,717 participants (10,670 cases of skin cancer)
were recruited from 13 countries across three continents
(11 studies from America, 12 studies from Europe, and six
studies from Asia-Pacific).
The overall meta-analysis including all 29 studies showed
no significant association between the risk of skin can-
cer and sunscreen use (OR = 1.08; 95% CI: 0.91-1.28;
I2= 89.4%). The pooled OR was 1.11 (95% CI: 0.93-1.33;
I2= 90.2%) for 28 observational studies.
Table 2 shows the results of subgroup analyses. The
subgroup “melanoma” included 25 studies [7-10, 12-
20, 31, 33-36, 38, 39, 41-45] involving a total of 203,948
participants (9,813 cases). Ten studies showed an increased
risk of melanoma related to sunscreen use while five stud-
ies reported a protective effect of sunscreen use against
melanoma. The pooled results of 25 studies revealed that
the risk of melanoma was not significantly associated with
sunscreen use (OR = 1.10; 95% CI: 0.92-1.33; I2= 89.4%).
The subgroup “non-melanoma skin cancer” included five
studies [11, 30, 32, 37, 40] involving 110,914 participants
(857 cases). Four studies showed no significant associa-
tion, but one study revealed a protective effect of sunscreen
against squamous cell carcinoma. The pooled results of
five studies showed no significant association between
the risk of non-melanoma skin cancer and sunscreen use
(OR = 0.99; 95% CI: 0.62-1.57; I2= 87.3%). In the sub-
group analysis according to latitude of study location, the
pooled OR was 1.54 (95% CI: 1.23-1.92, I2= 90%) for
10 studies [13, 14, 16, 18-20, 30, 36, 39, 43] (3,933 cases)
conducted at latitude ≥450from the equator, whereas it
was 0.89 (95% CI: 0.71-1.10, I2= 79%) for 19 studies
[7-12, 15, 17, 31-35, 37, 38, 40-42, 44, 45] (6,737 cases)
conducted at latitude <450(p=0.001 for subgroup differ-
ence). There were no significant differences in the effect
size of sunscreen between other subgroups. The substantial
heterogeneity remained in all subgroups.
Figure 2 shows the results of cumulative meta-analysis.
A relatively strong positive association between risk of
melanoma and sunscreen use (cumulative OR = 2.35;
95% CI: 1.66-3.33) was observed when the analysis
included only three studies [12,15,16] conducted before the
1980s, involving a total of 1,364 participants (619 cases of
melanoma). The strength of the association between risk
of skin cancer and sunscreen use has constantly reduced
since the early 1980s, but the association remained sta-
tistically significant until the analysis included 13 studies
[8, 10, 12-16, 18, 19, 30-33] with data collection com-
pleted until the early 1990s (119,756 participants, 4,841
cases of skin cancer; cumulative OR = 1.25; 95% CI: 1.0-
1.56; p= 0.05). From then on, the association was no longer
statistically significant, and the cumulative point estimate
of OR has continued to move towards the null hypothe-
sis value (OR = 1). The cumulative OR and 95% CI have
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
EJD, vol. 28, n◦2, March-April 2018 189
Table 1. Characteristics of included studies.
Source, location Type of cancer Study design and
sampling
Cases/sample
size (n)
Age range (yr)
Overall
association
between skin
cancer and
“sunscreen use”
(OR, 95% CI)
Association between
skin cancer and
frequency of sunscreen
use (OR/RR*/HR**,
95% CI)
Confounding
factors controlled
Study
quality
rating
Autier et al.,
1995 [13],
Brussels,
Belgium/ France
/Germany
Melanoma Hospital-based
case-control 418/856
≥20 1.50, 1.09-2.06 Never: 1.0
Regular use: 1.50,
1.09-2.06
Age, sex, hair
colour, number
of holidays,
weeks spent
every year in
sunny resorts
Fair
Bakos et al.,
2002 [7], Porto
Alegre, Brazil
Melanoma Hospital-based
case-control 103/309
20-84 0.52, 0.31-0.87
(SPF<8,
SPF8-15,
SPF15+;
combined as
“sunscreen use”)
Never: 1.0
Use of sunscreens
SPF<8: 0.4, 0.2-1.0
SPF8-15: 0.3, 0.1-0.7
SPF15+: 0.1, 0.0-0.5
Age, sex, race,
eye colour, hair
colour,
phototype,
number of nevi,
sunburn
episodes, use of
physical
protection
Fair
Beitner et al.,
1990 [14],
Sweden
Melanoma Population-based
case-control 523/1028
?1.58, 1.19-2.11
(seldom, often,
very often;
combined as
“sunscreen use”)
RR, 95% CI
Never: 1.0
Seldom: 1.4, 0.9-2.0
Often, very often: 1.8,
1.2-2.7
Age, sex, hair
colour Fair
Cress et al., 1995
[8], San
Francisco,
United States
Melanoma Population-based
case-control 338/1210
25-59 0.86, 0.75-0.97
(2x2
contingency table
reconstructed; 4
tan groups
combined;
almost always,
sometimes;
combined as
“sunscreen use”)
Tan with no burn
Almost always: 1.0
Sometimes: 1.2,
0.50-2.8
Never: 2.1, 0.99-4.3
Burn with moderate
tan
Almost always: 1.0
Sometimes: 4.8,
1.7-13.2
Never: 4.2, 1.6-11.0
Burn with light tan
Almost always: 1.0
Sometimes: 1.4,
0.78-2.6
Never: 1.4, 0.82-2.5
Burn with no tan
Almost always: 1.0
Sometimes: 1.5,
0.76-3.1
Never: 1.7, 0.91-3.4
No Fair
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
190 EJD, vol. 28, n◦2, March-April 2018
Table 1. (Continued)
Source, location Type of cancer Study design and
sampling
Cases/sample
size (n)
Age range (yr)
Overall
association
between skin
cancer and
“sunscreen use”
(OR, 95% CI)
Association
between skin
cancer and
frequency of
sunscreen use
(OR/RR*/HR**,
95% CI)
Confounding
factors controlled
Study quality
rating
Espinosa Arranz
et al., 1999 [9],
Madrid, Spain
Melanoma Hospital-based
case-control 116/351
21-87 0.47, 0.34-0.71
(with OR
converted to “no
sunscreen use”)
Use of sunscreen
Yes: 1.0
No: 2.1, 1.4-2.9
Age, skin type,
naevi count Fair
Fargnoli et al.,
2004 [45],
L’Aquila, Italy
Melanoma Hospital-based
case-control 100/300
18-74 0.92, 0.55-1.56 Use of sunscreen
No: 1.0
Yes: 0.92,
0.55-1.56
Age, gender,
ethnicity, hair
colour, eye
colour, skin type,
number of
melanocytic
naevi
Fair
Ghiasvand et al.,
2016 [43], Oslo,
Norway
Melanoma Population-based
cohort 543/109,886
40-75 1.25, 0.97-1.6 (2
x 2 contingency
table
reconstructed;
consistently SPF
<15, SPF ≥15
on at least one
occasion,
none/SPF <15-,
SPF <15/none;
combined as
“sunscreen use”)
Sunscreen use in
high/low
latitudes reported
at both baseline
and follow-up,
HR, 95% CI
SPF: <15/SPF <
15 (consistently
SPF<15: 1.0
SPF ≥15 on at
least one
occasion: 0.69,
0.55-0.88
None/SPF <15,
SPF <15/none:
0.92, 0.75-1.14
None/none: 0.63,
0.46- 0.86
Age, hair colour,
freckling,
ambient UV
radiation of
residence,
cumulative
number of weeks
sunbathing,
cumulative
number of
sunburns, indoor
tanning
Good
Gon et al., 2011
[40], Londrina,
Brazil
Basal cell
carcinoma Hospital-based
case-control 127/407
18-80 1.69, 0.82-3.49
(with OR,
converted to
“never”)
Sunscreen use
Frequently: 1.0
Never or rarely:
0.59, 0.29-1.21
Age, sex, eye
colour, hair
colour, skin type,
family history of
skin cancer,
presence of
actinic keratosis
Fair
Graham et al.,
1985 [15], New
York, United
States
Melanoma Hospital-based
case-control 218/419
All 2.20, 1.2-4.1 Sun screening
lotion
No use: 1.0
Use: 2.20,
1.20-4.10
No Poor
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
EJD, vol. 28, n◦2, March-April 2018 191
Table 1. (Continued)
Source, location Type of cancer Study design and
sampling
Cases/sample
size (n)
Age range (yr)
Overall
association
between skin
cancer and
“sunscreen use”
(OR, 95% CI)
Association
between skin
cancer and
frequency of
sunscreen use
(OR/RR*/HR**,
95% CI)
Confounding
factors controlled
Study quality
rating
Green et
al., 1999 [37],
Queensland,
Australia
Basal cell and
squamous cell
carcinomas
Randomized
controlled trial 128 (basal cell
carcinoma) + 47
(squamous cell
carcinoma)/1,383
25-75
Basal cell
carcinoma
1.03, 0.73-1.46
Squamous cell
carcinomas
0.88, 0.50-1.55
Broad-spectrum
sunscreen SPF
15+, RR, 95% CI
Basal cell
carcinoma
No daily
sunscreen: 1.0
Daily sunscreen:
1.03, 0.73-1.46
Squamous cell
carcinoma
No daily
sunscreen: 1.0
Daily sunscreen:
0.88, 0.50-1.55
Randomization Good
Green et
al., 2011 [38],
Queensland,
Australia
Melanoma 10-year
follow-up of the
trial of Green et
al. 1999
33/1,621
35-85 0.49, 0.24-1.02 Broad-spectrum
sunscreen SPF
15+, HR, 95% CI
No daily
sunscreen: 1.0
Daily sunscreen:
0.49, 0.24- 1.02
Sex, skin type,
numbers of nevi,
previous history
of skin cancer,
sun exposure
Good
Grodstein et
al., 1995 [32],
Boston, United
States
Squamous cell
carcinoma Population-based
cohort 197/107,900
30-55 1.11, 0.83-1.66
(with RR,
converted to “no
sunscreen use”)
RR, 95% CI
Use sunscreen:
1.0
No sunscreen:
0.90, 0.60-1.20
Age, smoking,
region, hair
colour, reaction
to sun, number of
sunburns,
tendency to tan,
number of moles,
time spent in the
sun
Good
Herzfeld et
al., 1993[12],
United States
Melanoma Population-based
case-control 324/739
≥18 2.60, 1.40-4.70 Suntan lotion
Never: 1.0
Always: 2.60,
1.40-4.70
Age, sex, race,
residence Data not
available
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
192 EJD, vol. 28, n◦2, March-April 2018
Table 1. (Continued)
Source, location Type of cancer Study design and
sampling
Cases/sample
size (n)
Age range (yr)
Overall
association
between skin
cancer and
“sunscreen use”
(OR, 95% CI)
Association
between skin
cancer and
frequency of
sunscreen use
(OR/RR*/HR**,
95% CI)
Confounding
factors controlled
Study quality
rating
Holly et al., 1995
[10], San
Francisco,
United States
Melanoma Population-based
case-control 452/1,382
25-59 0.47, 0.36-0.59
(3 groups
combined; with
OR, converted to
“never”)
Sunscreen use
Cutaneous
malignant
melanoma
Almost always:
1.0
Sometimes: 1.50,
1.10-2.20
Never: 2.10,
1.50-3.0
Superficial
spreading
melanoma
Almost always:
1.0
Sometimes: 1.70,
1.20-2.60
Never: 2.20,
1.50-3.2
Nodular
melanoma
Almost always:
1.0
Sometimes: 0.8,
0.33-1.90
Never: 2.0,
1.0-4.0
Age, ethnicity,
hair colour, skin
colour, history of
skin cancer,
sunburns up to 12
yr, skin reaction
to sun, number of
large nevi
Fair
Holman et
al., 1986 [31],
Perth, Australia
Melanoma Population-based
case-control 511/1,022
<80 1.10, 0.83-1.45
(2 groups
combined as
“sunscreen use”)
Duration of use
<10 yr
Never: 1.0
Sunscreen use:
1.06, 0.71-1.57
Duration of use
≥10 yr
Never: 1.0
Sunscreen use:
1.15, 0.78-1.68
Age, sex,
residence, hair
colour, ethnicity,
skin reaction to
sunlight, age at
arrival in
Australia
Fair
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
EJD, vol. 28, n◦2, March-April 2018 193
Table 1. (Continued)
Source, location Type of cancer Study design and
sampling
Cases/sample
size (n)
Age range (yr)
Overall
association
between skin
cancer and
“sunscreen use”
(OR, 95% CI)
Association
between skin
cancer and
frequency of
sunscreen use
(OR/RR*/HR**,
95% CI)
Confounding
factors controlled
Study quality
rating
Klepp et
al., 1979 [16],
Montebello,
Norway
Melanoma Hospital-based
case-control 77/206
≥20 2.26, 1.25-4.09
(2x2
contingency table
reconstructed;
sometimes, quite
often, almost
always,
combined as
“sunscreen use”)
Sun lotion/oil,
RR
Almost
never/very
rarely: 1.0
Sometimes /quite
often/almost
always: 2.27
No Poor
Klug et al., 2010
[33], United
States
Melanoma Hospital-based
case-control 717/1,662
20-79 0.90, 0.7-1.19 Sunscreen:
No use: 1.0
Sunscreen use:
0.90, 0.70-1.19
Age, gender,
study site, UVB
intensity at site
of residency,
hours outdoors as
an adult,
tan-type, number
of sunburns
Fair
Kricker et
al., 1995 [30],
Nedlands,
Australia
Basal cell
carcinoma Population-based
case-control 192/892
40-64 1.51, 0.99-2.31
(half the time or
more: 1-9 years,
10+ years,
combined as
“sunscreen use”)
Sunscreen,
SPF10+
Never, <half of
the time: 1.0
half the time or
more:
1-9 years: 1.92,
1.17-3.13
10+ years: 1.25,
0.82-1.90
Age, sex, ability
to tan and site Fair
Lazovich et
al., 2011 [41],
Minnesota,
United States
Melanoma Population-based
case-control 1167/2,268
25-59 1.07, 0.86-1.34
(Middle, frequent
in both decades,
combined as
“sunscreen use”)
Sunscreen
SPF15+ during
outdoor activities
Non-user in both
decades: 1.0
Middle: 1.06,
0.80-1.40
Frequent in both
decades: 1.10,
0.77-1.57
Age, gender,
phenotypic risk
score, moles,
high income,
college
education, family
history of
melanoma,
lifetime
sunburns, routine
sun exposure,
activity leading
to sun exposure,
occasional
indoor tanning
Fair
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
194 EJD, vol. 28, n◦2, March-April 2018
Table 1. (Continued)
Source, location Type of cancer Study design and
sampling
Cases/sample
size (n)
Age range (yr)
Overall
association
between skin
cancer and
“sunscreen use”
(OR, 95% CI)
Association
between skin
cancer and
frequency of
sunscreen use
(OR/RR*/HR**,
95% CI)
Confounding
factors controlled
Study quality
rating
Luiz et al., 2012
[42], São Paulo,
Brazil
Melanoma Hospital-based
case-control 202/424
15-79 0.32, 0.11-0.97
(with OR,
converted to
“never/almost
never”)
Lifetime
sunscreen use
Often: 1.0
Occasionally:
3.53, 0.59-21.21
Never/almost
never: 3.08,
1.03-9.22
Age, sex,
educational level,
ethnicity, eye
colour, sunburn
at 15-19 yr,
lifetime severe
sunburn
Fair
Naldi et al., 2000
[36], Milan, Italy Melanoma Hospital-based
case-control 542/1,080
?0.89, 0.69-1.15
(Sometimes,
often, combined
as “sunscreen
use”)
Never: 1.0
Sometimes: 0.97,
0.69-1.35
Often: 0.80,
0.54-1.17
Age, sex,
geographic area,
education, skin,
eye, and hair
colour, number
of freckles, large
nevi, history of
sunburns,
tanning pattern,
sunny holidays
Fair
Olsen et al., 2015
[17],
Queensland,
Australia
Melanoma Population-based
cross-sectional 1433/40,172
40-69 1.56, 1.41-1.73
(2x2
contingency table
reconstructed)
Prevalence
proportion ratio
No regular
sunscreen use:
1.0
Regular
sunscreen use:
1.77, 1.59-1.97
Age, sex,
educational level Fair
Osterlind et
al., 1988 [18],
Copenhagen,
Denmark
Melanoma Population-based
case-control 474/1,400
20-79 1.22, 1.01-1.47
(Occasional/always
used, combined
as “sunscreen
use”)
RR, 95% CI
Never: 1.0
Occasional use:
1.30, 0.99 = 1.60
Always: 1.10,
0.8-1.50
Constitutional
factors, sex, age Fair
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
EJD, vol. 28, n◦2, March-April 2018 195
Table 1. (Continued)
Source, location Type of cancer Study design and
sampling
Cases/sample
size (n)
Age range (yr)
Overall
association
between skin
cancer and
“sunscreen use”
(OR, 95% CI)
Association
between skin
cancer and
frequency of
sunscreen use
(OR/RR*/HR**,
95% CI)
Confounding
factors controlled
Study quality
rating
Ródenas et
al., 1996 [44],
Granada, Spain
Melanoma Hospital-based
case-control 105/243
20-29 0.41, 0.15-1.15
(Sometimes,
always,
combined as
“sunscreen use”)
Never: 1.0
Sometimes: 0.60,
0.26-1.42
Always: 0.20,
0.04-0.79
Age, skin colour,
skin type, hours
of sun exposure,
number of nevi
Fair
Sànchez and
Nova, 2013 [11],
Bogota,
Colombia
Squamous cell
carcinoma Hospital-based
case-control 166/332
32-94 0.43, 0.33-0.56
(Failure to use
sunscreen before
age 15 yr, age
15-30 yr, after
age 30 yr;
combined as “no
use”; with OR,
“no use”)
Use sunscreen:
1.0
Failure to use
sunscreen before
age 15 yr: 2.96,
0.15-176.9
Failure to use
sunscreen aged:
15-30 yr 0,
0-3.25
Failure to use
sunscreen after
age: 30 yr 1.74,
0.22-13.6
No Poor
Westerdahl et
al., 1995 [19],
Lund, Sweden
Melanoma Population-based
case-control 400/1,040
15-75 1.48, 1.08-2.03
(Sometimes,
almost always,
combined as
“sunscreen use”)
Never: 1.0
Sometimes 1.30,
0.90-1.90
Almost always
1.80, 1.10-2.80
Sunburn,
sunbathing,
outdoor
employment, eye
and hair colour,
freckling, naevi
Fair
Westerdahl et
al., 2000 [39],
Lund, Sweden
Melanoma Population-based
case-control 571/1,484
16-80 1.28, 0.89-1.84
(Sometimes,
always initially +
sometimes,
always,
combined as
“sunscreen use”)
Never 1.0
Sometimes: 1.30,
0.90-1.90
Always initially
+ sometimes:
0.90, 0.60-1.50
Always: 1.80,
1.10-2.90
Hair colour,
sunburns,
sunbathing,
duration of each
episode of
sunbathing
Fair
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
196 EJD, vol. 28, n◦2, March-April 2018
Table 1. (Continued)
Source, location Type of cancer Study design and
sampling
Cases/sample
size (n)
Age range (yr)
Overall
association
between skin
cancer and
“sunscreen use”
(OR, 95% CI)
Association
between skin
cancer and
frequency of
sunscreen use
(OR/RR*/HR**,
95% CI)
Confounding
factors controlled
Study quality
rating
Whiteman et
al., 1997 [34],
Queensland,
Australia
Melanoma Population-based
case-control 52/208
≤15 1.21, 0,69-2.14
(Sunscreen on
holiday and at
school;
sometimes,
often, always;
combined as
“sunscreen use”)
Sunscreen use
on holiday
Never/rarely: 1.0
Sometimes: 1.50,
0.30-8.20
Often: 1.50,
0.30-7.4
Always: 2.20,
0.40-11.6
Sunscreen use at
school
Never/rarely: 1.0
Sometimes: 0.80,
0.30-2.10
Often: 1.60,
0.50-5.50
Always 0.70,
0.10-6.0
Sex, school,
grade, tanning
ability, freckles,
number of nevi
Fair
Wolf et al., 1998
[20], Graz,
Austria
Melanoma Hospital-based
case-control 193/512
15-89 3.47, 1.81-6.64
(Often vs. never) Never: 1.0
Rarely: 1.30,
0.70-2.39
Often: 3.47,
1.81-6.64
Age, sex, hair
and skin colour,
skin phototype,
sun sensitivity,
sunbathing,
sunburns
Fair
Youl et al., 2002
[35],
Queensland,
Australia
Melanoma Population-based
case-control 201/406
15-19 0.97, 0.71-1.34
(2x2
contingency table
reconstructed;
sunscreen use at
home and on
holiday;
often/always,
sometimes;
combined as
“sunscreen use”)
Lifetime
sunscreen use at
home
Often/always: 1.0
Sometimes: 0.90,
0.50-1.70
Never/rarely:
0.90, 0.50-1.70
Lifetime
sunscreen use
on holidays
Often/always: 1.0
Sometimes: 1.30,
0.80-2.00
Never/rarely: 1.0,
0.50-1.80
Age, sex,
residency Fair
*RR: relative risk (risk ratio, rate ratio, relative risk); **HR: hazard ratio; SPF: sun protection factor.
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
EJD, vol. 28, n◦2, March-April 2018 197
Table 2. Subgroup analyses of the association between risk of skin cancer and sunscreen use.
Subgroups Number
of studies
Number
of cases
OR (95% CI) I2(%) for
heterogeneity
Type of skin cancer
Melanoma 25 9813 1.11 (0.93-1.33) 89.3
Non-melanoma 5 857 0.99 (0.62-1.57) 87.3
Study design
Retrospective (case-control,
cross-sectional) 26 9722 1.08 (0.90-1.30) 89.8
Prospective (cohort and
randomized trial) 3 948 1.09 (0.67-1.76) 86.1
Study quality
Good 3 1.08 (0.67-1.75) 86.1
Fair 23 1.06 (0.89-1.27) 88.3
Poor 3 1.25 (0.36-4.45) 95.2
Sampling method
Population-based 16 7586 1.17 (0.97-1.42) 87.5
Hospital- or clinic-based 13 3084 0.96 (0.69-1.35) 87.5
Control for confounding factors
At least one factor 18 6585 0.99 (0.78-1.27) 87.1
Factors including skin
colour/type and/or hair
colour
12 3983 1.00 (0.76-1.34) 86.1
No 11 4807 1.25 (0.99-1.57) 89.9
Date of data collection
Before 1990 9 3109 1.30 (0.95-1.78) 90.1
1990-1999 13 3823 0.98 (0.79-1.21) 77.0
2000 and thereafter 7 3738 1.06 (0.68-1.65) 94.4
Latitude of study location
<450from the equator
≥450from the equator 19
10 6737
3933 0.89 (0.72-1.11)
1.54 (1.23-1.92) 90.2
79.0
Frequency of sunscreen use
Maximum frequency
(always/almost always vs.
never/rarely)
10 2995 1.14 (0.78-1.68) 83.1
Occasional vs. never/rarely 29 10670 1.08 (0.92-1.29) 89.3
Age groups
Adults and adolescents 27 10417 1.08 (0.90-1.29) 90.0
Children and adolescents 2 253 1.02 (0.78-1.35) 0
remained almost unchanged since the early 2000s, even
though seven studies [11, 17, 40-43, 45] involving a total
of 187,747 participants (3,738 cases of skin cancer) were
added to the analysis.
The meta-regression analysis showed an inverse relation-
ship between the OR (log scale) and the altitude of study
setting (coefficient of -0.0004; p=0.02). However, the
results were not statistically significant after adjusting for
covariates (p=0.69). The meta-regression analysis revealed
a significant positive association between the OR (log
scale) and the latitude of study setting (coefficient of 0.02;
p=0.003), i.e. the higher the absolute latitude from the
equator, the greater the odds ratio, and the less the pro-
tective effect of sunscreen against skin cancer, or even the
higher the risk of skin cancer associated with sunscreen use.
The results remained statistically significant after adjusting
for altitude, type of cancer, study design, sampling method,
control of confounding factors (skin type/colour and/or hair
colour), and date of data collection (coefficient of 0.023;
p=0.01).
The funnel plot and Egger’s test did not reveal a significant
publication bias (figure 3).
Discussion
This systematic review and meta-analysis of 28 obser-
vational studies and one community-based randomized
trial, with a total of 313,717 participants (10,670 cases),
showed no significant overall association between the risk
of melanoma and non-melanoma skin cancers and use of
sunscreen. The geographical latitude seemed to influence
the effects of sunscreen, that is, the higher the latitude
where people live, the less the protective effect of sunscreen
against skin cancer.
The cumulative evidence before the 1980s revealed a rel-
atively strong positive association between the risk of
melanoma and sunscreen use. However, the strength of the
association between risk of skin cancer and sunscreen use
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
198 EJD, vol. 28, n◦2, March-April 2018
Study
Klepp 1979 Melanoma 1974-1975 77 206 2.26 (1.25, 4.09)
2.42 (1.58, 3.70)
2.35 (1.66, 3.33)
1.85 (1.14, 3.01)
1.72 (1.24, 2.39)
1.56 (1.21, 2.00)
1.43 (1.08, 1.90)
1.26 (0.91, 1.75)
1.28 (0.95, 1.74)
1.26 (0.95, 1.66)
1.28 (0.98, 1.65)
1.29 (1.01, 1.65)
1.25 (1.00, 1.56)
1.21 (0.97, 1.51)
1.13 (0.90, 1.42)
1.14 (0.91, 1.41)
1.20 (0.96, 1.50)
1.18 (0.96, 1.46)
1.15 (0.95, 1.40)
1.14 (0.95, 1.38)
1.11 (0.92, 1.34)
1.12 (0.94, 1.34)
1.09 (0.91, 1.30)
1.08 (0.91, 1.28)
1.09 (0.92, 1.29)
1.11 (0.94, 1.31)
1.12 (0.95, 1.32)
1.08 (0.91, 1.29)
1.07 (0.91, 1.25)
1.09 (0.93, 1.28)
945
1364
2386
3414
4814
6024
7406
8298
116198
117238
118094
119756
119999
120350
120558
121070
121476
122556
124177
124177
125661
125970
126270
126677
128945
129369
273213
313385
313717
15
.1
Favours sunscreen use Favours no sunscreen use
401
619
1130
1653
2127
2465
2917
3109
3306
3706
4124
4841
4946
5062
5114
5307
5508
6050
6225
6258
6829
6932
7032
7159
8326
8528
9071
10504
10670
1977-1979
1974-1980
1980-1981
1978-1983
1982-1985
1981-1986
1981-1986
1987-1988
1982-1990
1988-1990
1991-1992
1991-1992
1989-1993
1990-1994
1987-1994
1993-1994
1987-1994
1992-1995
1992-1996
1992-1996
1995-1997
1995-1998
2000-2001
2006-2007
2004-2007
2004-2008
1997-2010
2011
2010-2011
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Melanoma
Basal-cell carcinoma
Basal-cell carcinoma
Squamous-cell carcinoma
Squamous-cell carcinoma
Basal- & Squamous-cell carcinoma
Herzfeld 1993
Graham 1985
Holman 1986
Beitner 1990
Osterlind 1988
Cress 1995
Holly 1995
Kricker 1995
Grodstein 1995
Westerdahl 1995
Autier 1995
Klug 2010
Ródenas 1996
Espinosa Arranz 1999
Whiteman 1997
Wolf 1998
Youl 2002
Naldi 2000
Green 1999
Green 2011
Westerdahi 2000
Bakos 2002
Fargnoli 2004
Gon 2011
Lazovich 2011
Luiz 2012
Ghiasvand 2016
Olsen 2015
Sànchez 2013
Type of cancer
Dates of data
collection
Cumulative
number
of cases
Cumulative
sample size
Cumulative odds ratio
ES (95% Cl)
Figure 2. Cumulative meta-analysis of the association between skin cancer and sunscreen use. The solid squares represent point
estimates of cumulative odds ratio and the horizontal lines represent 95% CIs.
has constantly reduced since the early 1980s, and the asso-
ciation was no longer statistically significant from the early
1990s. Several hypotheses have been proposed to explain
the positive association between risk of skin cancer, espe-
cially melanoma, and use of sunscreen, as shown by earlier
observational studies, including compensation hypothesis,
inconsistent use, vitamin D deficiency, and lack of control
for confounding factors [46-49]. The median Sun Protection
Factor (SPF) of commonly used sunscreens in the 1970s and
1980s was 4-10 [48], and these sunscreens incorporated
active UV filters, limited largely to the UVB waveband.
People who use low SPF/UVB sunscreens may stay longer
in the sun because of reduced risk of sunburn, and thus
increase their exposure to UVA radiation which may lead
to an increased risk of carcinogenesis.
The constant shift of the cumulative point estimate of the
association between skin cancer and sunscreen use towards
the null hypothesis value through the 1990s may be partly
explained by the improved efficacy of sunscreens in protect-
ing against solar UV radiation, particularly UVA rays, and
the growing public awareness of the risk of excessive sun
exposure. These results may alleviate public concern about
the increased risk of skin cancer related to sunscreen use, as
reported by earlier epidemiological studies. However, the
expected protective benefits of sunscreen against skin can-
cer were not revealed by the cumulative meta-analysis, even
though seven new studies conducted in the 2000s, involv-
ing a large number of participants and cases of skin cancer,
were added to the analysis. This may raise the question as
to whether the use of sunscreens really protects against skin
cancer.
A 4.5-year community-based randomized controlled trial
conducted at Nambour, Australia, has been widely cited
to show the efficacy of daily use of a broad-spectrum
SPF15+ sunscreen in protecting against skin cancers in
adults [37, 38, 50]. However, caution should be taken when
extrapolating the results of this trial to the general popula-
tion. This trial was conducted in the low-latitude township
of Nambour, situated at 26◦south latitude, where cumula-
tive sun exposure may affect the risk of skin cancer. The
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
EJD, vol. 28, n◦2, March-April 2018 199
-1 -.5
.6 .4 .2 0
0
p=0.53 (Egger test for small-study effects)
log odds ratio (OR)
Standard error of the log OR
.5 11.5
Figure 3. Funnel plot with pseudo 95% confidence limits, with log odds ratio (OR) against its standard error. The circles represent
risk estimates for each study. The vertical line represents the pooled effect estimate expressed as a log OR. Dashed lines represent
pseudo-95% confidence limits. The Egger test (p=0.53) suggests no small-study effects.
practicality and the cost of daily application of sunscreen
should also be considered.
While randomized trials assess the efficacy of an interven-
tion under “ideal” circumstances, epidemiological studies
can provide valid insights into the effectiveness of the inter-
vention in the “real” world. Why have most epidemiological
studies, even recently conducted ones, not demonstrated
the expected effects of sunscreens in protecting against
skin cancer in the general population? The inappropriate
application of sunscreen has been postulated as the major
cause for the lack of protective benefits of sunscreen, even
broad-spectrum ones [48, 51, 52]. People usually do not
apply enough sunscreen to achieve the claimed SPF, and
the actual SPF received may be only 20% to 50% of the
labelled SPF marked on the bottle. Additionally, reappli-
cation is generally considered a key element for obtaining
the most effective protection from sunscreen [52, 53], but
many people do not regularly reapply sunscreen [54]. Vita-
min D deficiency and confounding factors may also have
contributed to the lack of protective effects of sunscreen
use, as shown by epidemiological studies.
The meta-regression analysis revealed an inverse relation-
ship between protective effect of sunscreen against skin
cancer and latitude of study location. Additionally, the
subgroup analysis showed that use of sunscreens was asso-
ciated with a non-significant decreased risk of skin cancer at
latitude <45◦from the equator, whereas use of sunscreens
could significantly increase the risk of skin cancer at latitude
≥45◦. The influence of latitude on the association between
the risk of melanoma and sunscreen use has previously been
reported by Gorham et al. [23]. The authors hypothesized
that the influence of latitude on the effect of sunscreen could
be explained by differences in skin type, rather than geo-
physical effects of ultraviolet radiation at higher latitudes.
However, the findings of the present systematic review do
not totally support this hypothesis given that the latitudinal
dependence of the effect of sunscreen on the risk of skin can-
cer remains after adjusting for several covariates, including
skin type and hair colour. We believe that the influence of
the latitude on the effect of sunscreen could be mediated
by UV radiation levels. It has been reported that, within
some countries, the incidence rates of melanoma and non-
melanoma skin cancers increase with decreasing latitude,
i.e. higher UV radiation levels [55-58]. It seems reasonable
that regular sunscreen use would have a greater protective
effect for persons at higher risk of skin cancer because they
live at lower latitudes and are exposed to higher levels of
UV radiation. In contrast, for people who live at higher
latitudes where UV radiation is weaker and less constant,
regular sunscreen use may provide less protection against
skin cancer, or even increase the risk of carcinogenesis.
While the current evidence suggests no increased risk of
skin cancer related to sunscreen, this systematic review and
meta-analysis does not confirm the expected protective ben-
efits of sunscreen use against skin cancer in the general
population. These results support a wide range of strategies
besides sunscreen use for primary prevention of skin can-
cer. These strategies include wearing hats and protective
clothing, seeking shade, limiting exposure during peak sun
hours, and avoiding tanning beds and other artificial UV
radiation sources [59-61].
Meta-analyses of observational studies are generally prone
to heterogeneity and bias [62, 63]. In this study, there
was substantial heterogeneity with regards to the over-
all meta-analysis and the heterogeneity remained high in
subgroup analyses according to study design, study qual-
ity, sampling method, control for confounding factors, age
group, frequency of sunscreen use, and date of data col-
lection. As many of these factors could simultaneously
affect the study results, it is difficult to identify the inde-
pendent contribution of each factor to the heterogeneity.
Moreover, other covariates may also influence the effects
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
200 EJD, vol. 28, n◦2, March-April 2018
of sunscreens and contribute to the heterogeneity. These
may include genetic predisposition, behaviour and lifestyle
habits, socioeconomic status, sun exposure habits, use of
other sun protection methods, components of sunscreens,
and techniques of sunscreen application. Unfortunately,
these covariates have rarely been taken into account in
primary studies.
The quality of evidence provided by this review could only
be graded as low, mainly due to inconsistency of the results
between studies, retrospective design, and potential risk
of bias (selection bias, information bias, and confound-
ing factors) in most of the primary studies. Given that the
quality of current evidence is low and new sunscreen prod-
ucts that efficiently block both UVA and UVB have been
available on the market for more than two decades, it is
time to investigate the effects of new broad-spectrum sun-
screens on protecting against skin cancer in the general
population. Randomized controlled trials are considered
the “gold standard” for assessing the efficacy of an inter-
vention. However, such design requires large sample size
and long trial duration. Moreover, the applicability of the
trial results to the general population is limited. Prospective,
real-world, population-based observational studies would
be good options. Future studies should involve collection of
data on both sunscreen use and appropriateness of applica-
tion (amount of sunscreen applied and reapplication). The
data on confounding factors, such as genetic predisposi-
tion, behaviour and lifestyle habits, socioeconomic status,
sun sensitivity, sun exposure, and use of other sun protec-
tion methods, should be collected and taken into account in
the analysis. The potential impact of latitude on the effects
of sunscreen on skin cancer risk should also be assessed in
further studies.
Disclosure. Financial support: none. Conflict of interest:
none.
References
1. Merrill SJ, Ashrafi S, Subramanian M, Godar DE. Exponentially
increasing incidences of cutaneous malignant melanoma in Europe
correlate with low personal annual UV doses and suggests 2 major
risk factors. Dermatoendocrinol 2015; 7: e1004018.
2. Lomas A, Leonardi-Bee J, Bath-Hextall F. A systematic review of
worldwide incidence of nonmelanoma skin cancer. Br J Dermatol
2012; 166: 1069-80.
3. Lucas R, McMichael T, Smith W, Armstrong B. Solar ultraviolet
radiation: global burden of disease from solar ultraviolet radiation.
In: Environmental Burden of Disease Series No. 13. Geneva: WHO
Public Health and the Environment, 2006.
4. Karimkhani C, Green AC, Nijsten T, et al. The global burden of
melanoma: results from the Global Burden of Disease Study 2015.Br
J Dermatol 2017; 177: 134-40.
5. Guy GP Jr., Machlin SR, Ekwueme DU, Yabroff KR. Prevalence and
costs of skin cancer treatment in the U.S., 2002-2006 and 2007-2011.
Am J Prev Med 2015; 48: 183-7.
6. Armstrong BK, Kricker A. The epidemiology of UV induced skin
cancer. J Photochem Photobiol B 2001; 63: 8-18.
7. Bakos L, Wagner M, Bakos RM, Leite CS, Sperhacke CL, Dzeka-
niak KS, et al. Sunburn, sunscreens, and phenotypes: some risk factors
for cutaneous melanoma in southern Brazil. Int J Dermatol 2002; 41:
557-62.
8. Cress RD, Holly EA, Ahn DK. Cutaneous melanoma in women. V.
Characteristics of those who tan and those who burn when exposed to
summer sun. Epidemiology 1995; 6: 538-43.
9. Espinosa Arranz J, Sanchez Hernandez JJ, Bravo Fernandez P,
et al. Cutaneous malignant melanoma and sun exposure in Spain.
Melanoma Res 1999; 9: 199-205.
10. Holly EA, Aston DA, Cress RD, Ahn DK, Kristiansen JJ. Cutaneous
melanoma in women. I. Exposure to sunlight, ability to tan, and other
risk factors related to ultraviolet light. Am J Epidemiol 1995; 141:
923-33.
11. Sánchez G, Nova J. Risk factors for squamous cell carcinoma,
a study by the National Dermatology Centre of Colombia. Actas Der-
mosifiliogr 2013; 104: 672-8.
12. Herzfeld PM, Fitzgerald EF, Hwang SA, Stark A. A case-control
study of malignant melanoma of the trunk among white males in upstate
New York. Cancer Detect Prev 1993; 17: 601-8.
13. Autier P, Doré JF, Schifflers E, et al. Melanoma and use of
sunscreens: an Eortc case-control study in Germany, Belgium and
France. The EORTC Melanoma Cooperative Group. Int J Cancer
1995; 61: 749-55.
14. Beitner H, Norell SE, Ringborg U, Wennersten G, Mattson B.
Malignant melanoma: aetiological importance of individual pigmen-
tation and sun exposure. Br J Dermatol 1990; 122: 43-51.
15. Graham S, Marshall J, Haughey B, et al. An inquiry into
the epidemiology of melanoma. Am J Epidemiol 1985; 122:
606-19.
16. Klepp O, Magnus K. Some environmental and bodily charac-
teristics of melanoma patients. A case-control study. Int J Cancer
1979; 23: 482-6.
17. Olsen CM, Thompson BS, Green AC, Neale RE, Whiteman
DC, & QSkin Sun, Health Study Group. Sun protection and skin
examination practices in a setting of high ambient solar radia-
tion: a population-based cohort study. JAMA Dermatol 2015; 151:
982-90.
18. Osterlind A. Epidemiology on malignant melanoma in Europe.
Acta Oncol 1992; 31: 903-8.
19. Westerdahl J, Olsson H, Måsbäck A, Ingvar C, Jonsson N. Is the
use of sunscreens a risk factor for malignant melanoma? Melanoma
Res 1995; 5: 59-65.
20. Wolf P, Quehenberger F, Müllegger R, Stranz B, Kerl H. Pheno-
typic markers, sunlight-related factors and sunscreen use in patients
with cutaneous melanoma: an Austrian case-control study. Melanoma
Res 1998; 8: 370-8.
21. Dennis LK, Beane Freeman LE, VanBeek MJ. Sunscreen use
and the risk for melanoma: a quantitative review. Ann Intern Med
2003; 139: 966-78.
22. Huncharek M, Kupelnick B. Use of topical sunscreens and the risk
of malignant melanoma: a meta-analysis of 9067 patients from 11
case-control studies. Am J Public Health 2002; 92: 1173-7.
23. Gorham ED, Mohr SB, Garland CF, Chaplin G, Garland FC. Do
sunscreens increase risk of melanoma in populations residing at higher
latitudes? Ann Epidemiol 2007; 17: 956-63.
24. Xie F, Xie T, Song Q, Xia S, Li H. Analysis of association between
sunscreens use and risk of malignant melanoma. Int J Clin Exp Med
2015; 8: 2378-84.
25. Perera E, Sinclair R. An estimation of the prevalence of non-
melanoma skin cancer in the U.S. F1000Res 2013; 2: 107.
26. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement
for reporting systematic reviews and meta-analyses of studies that
evaluate healthcare interventions: explanation and elaboration. BMJ
2009; 339: b2700.
27. National Heart, Lung, and Blood Institute. Quality Assess-
ment Tool for Observational Cohort and Cross-Sectional Studies.
Available at: https://www.nhlbi.nih.gov/health-pro/guidelines/in-
develop/cardiovascular-risk-reduction/tools/cohort.(accessed 09
May 2016).
28. National Heart, Lung, and Blood Institute. Quality Assessment
of Case-Control Studies. Available at: https://www.nhlbi.nih.gov/
health-pro/guidelines/in-develop/cardiovascular-risk-reduction/
tools/case-control.(accessed 09 May 2016).
29. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring incon-
sistency in meta-analyses. BMJ 2003; 327: 557-60.
Journal Identification = EJD Article Identification = 3251 Date: April 26, 2018 Time: 3:15pm
EJD, vol. 28, n◦2, March-April 2018 201
30. Kricker A, Armstrong BK, English DR, Heenan PJ. Does intermit-
tent sun exposure cause basal cell carcinoma? a case-control study in
Western Australia. Int J Cancer 1995; 60: 489-94.
31. Holman CD, Armstrong BK, Heenan PJ, et al. The causes of malig-
nant melanoma: results from the West Australian Lions Melanoma
Research Project. Recent Results Cancer Res 1986; 102: 18-37.
32. Grodstein F, Speizer FE, Hunter DJ. A prospective study of incident
squamous cell carcinoma of the skin in the nurses’ health study. J Natl
Cancer Inst 1995; 87: 1061-6.
33. Klug HL, Tooze JA, Graff-Cherry C, et al. Sunscreen preven-
tion of melanoma in man and mouse. Pigment Cell Melanoma Res
2010; 23: 835-7.
34. Whiteman DC, Valery P, McWhirter W, Green AC. Risk fac-
tors for childhood melanoma in Queensland, Australia. Int J Cancer
1997; 70: 26-31.
35. Youl P, Aitken J, Hayward N, et al. Melanoma in adolescents: a
case-control study of risk factors in Queensland, Australia. Int J Cancer
2002; 98: 92-8.
36. Naldi L, Gallus S, Imberti GL, Cainelli T, Negri E, La Vecchia
C. Sunscreens and cutaneous malignant melanoma: an Italian case-
control study. Int J Cancer 2000; 86: 879-82.
37. Green A, Williams G, Neale R, et al. Daily sunscreen applica-
tion and betacarotene supplementation in prevention of basal-cell and
squamous-cell carcinomas of the skin: a randomised controlled trial.
Lancet 1999; 354: 723-9.
38. Green AC, Williams GM, Logan V, Strutton GM. Reduced
melanoma after regular sunscreen use: randomized trial follow-up.J
Clin Oncol 2011; 29: 257-63.
39. Westerdahl J, Ingvar C, Mâsbäck A, Olsson H. Sunscreen use and
malignant melanoma. Int J Cancer 2000; 87: 145-50.
40. Gon A, Minelli L. Risk factors for basal cell carcinoma in a
southern Brazilian population: a case-control study. Int J Dermatol
2011; 50: 1286-90.
41. Lazovich D, Vogel RI, Berwick M, Weinstock MA, Warshaw
EM, Anderson KE. Melanoma risk in relation to use of sunscreen
or other sun protection methods. Cancer Epidemiol Biomarkers Prev
2011; 20: 2583-93.
42. Luiz OC, Gianini RJ, Gonc¸alves FT, et al. Ethnicity and cutaneous
melanoma in the city of Sao Paulo, Brazil: a case-control study. PLoS
One 2012; 7: e36348.
43. Ghiasvand R, Weiderpass E, Green AC, Lund E, Veierød MB. Sun-
screen use and subsequent melanoma risk: a population-based cohort
study. J Clin Oncol 2016; 34: 3976-83.
44. Ródenas JM, Delgado-Rodríguez M, Herranz MT, Tercedor J,
Serrano S. Sun exposure, pigmentary traits, and risk of cutaneous
malignant melanoma: a case-control study in a Mediterranean pop-
ulation. Cancer Causes Control 1996; 7: 27-83.
45. Fargnoli MC, Piccolo D, Altobelli E, Formicone F, Chimenti S,
Peris K. Constitutional and environmental risk factors for cutaneous
melanoma in an Italian population. A case-control study. Melanoma
Res 2004; 14: 151-7.
46. Garland CF, Garland FC, Gorham ED. Rising trends in
melanoma. An hypothesis concerning sunscreen effectiveness. Ann
Epidemiol 1993; 3: 103-10.
47. Weinstock MA. Do sunscreens increase or decrease melanoma
risk: an epidemiologic evaluation. J Investig Dermatol Symp Proc
1999; 4: 97-100.
48. Diffey BL. Sunscreens and melanoma: the future looks bright.BrJ
Dermatol 2005; 153: 378-81.
49. Planta MB. Sunscreen and melanoma: is our prevention message
correct? J Am Board Fam Med 2011; 24: 735-9.
50. van der Pols JC, Williams GM, Pandeya N, Logan V, Green AC.
Prolonged prevention of squamous cell carcinoma of the skin by regular
sunscreen use. Cancer Epidemiol Biomarkers Prev 2006; 15: 2546-8.
51. Stenberg C, Larkö O. Sunscreen application and its importance
for the sun protection factor. Arch Dermatol 1985; 121: 1400-2.
52. Petersen B, Wulf HC. Application of sunscreen-theory and reality.
Photodermatol Photoimmunol Photomed 2014; 30: 96-101.
53. Diffey BL. When should sunscreen be reapplied? J Am Acad Der-
matol 2001; 45: 882-5.
54. Pruim B, Wright L, Green A. Do people who apply sunscreens,
re-apply them? Australas J Dermatol 1999; 40: 79-82.
55. Auerbach H. Geographic variation in incidence of skin cancer in
the United States. Public Health Rep 1961; 76: 345-8.
56. Bulliard JL, Cox B, Elwood JM. Latitude gradients in melanoma
incidence and mortality in the non-Maori population of New Zealand.
Cancer Causes Control 1994; 5: 234-40.
57. Moan J, Dahlback A, Setlow RB. Epidemiological support for an
hypothesis for melanoma induction indicating a role for UVA radiation.
Photochem Photobiol 1999; 70: 243-7.
58. Cicarma E, Juzeniene A, Porojnicu AC, Bruland ØS AC, Moan J.
Latitude gradient for melanoma incidence by anatomic site and gender
in Norway 1966-2007. J Photochem Photobiol B 2010; 101: 174-8.
59. Moyer VA, & U.S., Preventive Services Task Force. Behavioral
counseling to prevent skin cancer: U.S. Preventive Services Task Force
recommendation statement. Ann Intern Med 2012; 157: 59-65.
60. National Institute for Health and Care Excellence. Public Health
Guideline (PH32): Skin Cancer Prevention. Available at: https://www.
nice.org.uk/guidance/ph32.(accessed 20 June 2017).
61. Cancer Council Australia. Preventing skin cancer. Available
at: http://www.cancer.org.au/preventing-cancer/sun-protection/
preventing-skin-cancer.(accessed 20 June 2017).
62. Egger M, Schneider M, Davey Smith G. Spurious precision? Meta-
analysis of observational studies. BMJ 1998; 316: 140-4.
63. Dwyer T, Couper D, Walter SD. Sources of heterogeneity in the
meta-analysis of observational studies: the example of SIDS and sleep-
ing position. J Clin Epidemiol 2001; 54: 440-7.
