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SUPPLEMENT ARTICLE

Association of sunbed use with skin cancer risk factors in Europe: an investigation within the Euromelanoma skin cancer prevention campaign

M. Suppa,1,* S. Gandini,2H. Njimi,1J.L. Bulliard,3O. Correia,4,5,6,7A.F. Duarte,4,5,8K. Peris,9

A.J. Stratigos,10E. Nagore,11,12 M.I. Longo,13M. Bylaite-Bucinskiene,14R. Karls,15H. Helppikangas,16 Euromelanoma Working Group,aV. del Marmol1

1Department of Dermatology, H^opital Erasme, Universite Libre de Bruxelles, Brussels, Belgium

2Molecular and Pharmaco-Epidemiology Unit, Department of Experimental Oncology, European Institute of Oncology, IRCCS, Milan, Italy

3Institute of Social and Preventive Medicine (IUMSP), Lausanne University Hospital, Lausanne, Switzerland

4Centro de Dermatologia Epidermis, Instituto CUF, Porto, Portugal

5Portuguese Skin Cancer Association, Lisbon, Portugal

6Center for Health Technology and Services Research (CINTESIS), Porto,Portugal

7Basic and Clinical Immunology Unit, Department of Pathology, Faculty of Medicine, University of Porto, Porto, Portugal

8Department of Community Medicine, Information and Health Decision Sciences (MEDCIDS), Faculty of Medicine, University of Porto, Porto, Portugal

9Institute of Dermatology, Catholic University, Rome, Italy

10First Department of Dermatology, National and Kapodistrian University of Athens School of Medicine, Andreas Sygros Hospital, Athens, Greece

11Department of Dermatology, Instituto Valenciano de Oncologıa, Valencia, Spain

12Universidad Catolica de Valencia San Vicente Ferrer, Valencia, Spain

13Department of Dermatology, University of Florida College of Medicine, Gainesville, FL, USA

14Clinic of Infectious, Chest diseases, Dermatovenereology and Allergology, Faculty of Medicine, Vilnius University, Vilnius, Lithuania

15Department of Infectiology and Dermatology, Riga Stradins University, Riga, Latvia

16Dermatology Department, Clinical Center, University of Sarajevo, Sarajevo, Bosnia and Herzegovina

*Correspondence: M. Suppa.E-mail: dr.marianosuppa@gmail.com

Abstract

Introduction Sunbed use has been signicantly associated with increased risk of melanoma and non-melanoma skin cancer (NMSC), but its relationship with melanomas risk factors such as high nevus count, atypical nevi and lentigines is poorly studied. Euromelanoma is a skin cancer prevention campaign conducted all over Europe. It offers a once-a-year screening during which participantsdata, including sunbed use and phenotype, are collected via questionnaires.

Objectives To investigate the association of sunbed use with nevus count, atypical nevi, lentigines and suspicion of skin cancer.

Methods To ensure reliability of the data, we dened inclusion and exclusion criteria for countrieseligibility for the risk analysis. Multivariate logistic regression models (including age, gender, education, skin type, family history of melanoma, personal history of skin cancer, any sun exposure and any sunscreen use) were used to calculate summary odds ratios (SORs) of each clinical endpoint for ever sunbed use.

Results Overall, 227 888 individuals from 30 countries completed the Euromelanoma questionnaire. After the data quality check, 16 countries were eligible for the multivariate analysis, for a total of 145 980 participants (64.8% females;

median age 43 years; 62.3% highly educated; 28.5% skin type III; 11.0% ever sunbed use). Ever sunbed use was inde- pendently associated with nevus count>50 [SOR=1.05 (1.011.10)], atypical nevi [SOR=1.04 (1.001.09)], lentigines [SOR=1.16 (1.041.29)] and suspicion of melanoma [SOR=1.13 (1.001.27)]. Conversely, no signicant association was found between ever sunbed use and suspicion of NMSC [SOR=1.00 (0.911.10)].

Conclusions Indoor tanning is signicantly associated with well-recognized risk factors for melanoma (including high nevus count, presence of atypical nevi and lentigines) as well as suspicion of melanoma within the Euromelanoma scree- nees. In order to reduce the prevalence of melanoma risk factors, avoidance/discontinuation of sunbed use should always be encouraged, especially but not exclusively for individuals with high-risk phenotypes.

Received: 14 May 2018; Accepted: 20 September 2018

aEuromelanoma Working Group members’details are listed in Appendix 1.

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Conflict of interest None.

Funding sources

During the study period, the Euromelanoma campaign was supported by Almirall, Leo Pharma, Meda, La Roche-Posay.

Introduction

The use of artificial tanning lamps for cosmetic purposes is extremely common in developed areas of the world including Europe.1This raises concern among health providers and leg- islators, as sunbed use has been associated with an increased risk of melanoma and non-melanoma skin cancer (NMSC) by several studies, summarized in meta-analyses.2–8 Indeed, the International Agency for Research on Cancer (IARC) cur- rently regards the whole spectrum of ultraviolet (UV) radia- tion as well as UV-emitting tanning devices as first-group carcinogens alongside tobacco smoking and asbestos.9,10 Asso- ciations between indoor tanning exposure and melanoma’s risk factors such as high nevus count, atypical nevi and lentigines have also been suggested, though not extensively studied up to date.11–19

Euromelanoma is a skin cancer prevention campaign that is conducted all over Europe since almost two decades.20–22 Its main goal is to promote awareness of skin cancer among the general public. Euromelanoma aims therefore to inform and educate the population as to how to prevent skin cancer by avoiding modifiable risk factors, and to recognize suspicious skin lesions by skin self-examination. Moreover, Euromelanoma offers once-a-year free screenings to the general public, during which screenees and physicians are requested to complete a questionnaire enquiring about participants’ socio-demographics, phenotype, risk factors (including sunbed use) and several clini- cal findings.

The objective of this study was to investigate the association of sunbed use with established melanoma’s risk factors such as high nevus count, presence of atypical nevi and lentigines as well as with suspected skin cancers detected by dermatologists during the Euromelanoma screening.

Materials and methods

Euromelanoma campaign and questionnaire

The Euromelanoma campaign was organized annually by the Euromelanoma Networking Group, under the auspices of the European Academy of Dermatology and Venereology (EADV) and the European Association of Dermato-Oncology (EADO).

Every year, a media campaign focusing on particular aspects of skin cancer prevention was conducted on TV, radio, newspa- pers/magazines and Internet (www.euromelanoma.org) during

the month of April. The campaign then culminated each year with the Euromelanoma day (usually in May), during which free-of-charge skin examinations were offered by both public and private dermatology clinics in several European countries.

As previously described,20,21 participants were evaluated by means of the Euromelanoma questionnaire, which was standard- ized for all participating countries since 2009. The questionnaire was divided in two sections: the first was to be completed by the screenees and enquired about their demographics and risk fac- tors; the second was then filled in by the screening dermatologist and focused on clinical findings that emerged during the visit.

Questionnaires were sent to the coordinator centre of each country and data were then entered in a unique database (devel- oped with Limesurvey version 1.82+), located at the Department of Dermatology, Universite Libre de Bruxelles, Brussels, Bel- gium.

Statistical analysis

The variable ‘any sunscreen use’ (no/yes) was created by pooling together sunscreen use when outdoors for>1 h and sunscreen use when sunbathing. The variable ‘any sun exposure’ (no/yes) was created by pooling together outdoor occupation, history of sunburn and sunny holidays.

Sunbed use was investigated by two questions: ‘Do you use solarium?’ (possible answers ‘No’, ‘Yes,≤20 sessions/year’, ‘Yes,

>20 sessions/year’) enquired about current sunbed use; and

‘Number of years using solarium (including in the past only)’

enquired about duration of ever sunbed use. Participants not reporting current sunbed use but reporting duration of sunbed use were considered ever users along with those reporting cur- rent use.

The following clinical variables were used as endpoints: pres- ence of suspected melanoma, presence of suspected basal cell carcinoma (BCC), presence of suspected squamous cell carci- noma (SCC), presence of actinic keratoses (AKs), nevus count, presence of atypical nevi (defined as nevi with asymmetric, ill- defined borders, irregular pigmentation and diameter>6 mm) and presence of lentigines on the back/chest, all categorized as no/yes variables.

Descriptive statistics, with frequencies, median values and interquartile ranges, are presented to report the socio-demo- graphic characteristics of the surveyed population. Percentages and 95% confidence intervals (CIs) are presented to define the

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Table1Frequencyofthemainclinicalvariablesforeachparticipatingcountry CountryNSuspected melanomaSuspectedBCCSuspectedSCCSuspectedAKsNevuscountAtypicalnevi(≥1)Lentigines n%n%n%n%n%n%n% Belgium10179Missing3413.4Missing3253.2Missing3613.6Missing7397.3Missing3623.6Missing4354.3Missing4394.3 No958994.2No957794.1No978796.2No872285.750844783.0No805479.1No544353.5 Yes2492.5Yes2772.7Yes310.3Yes7187.1>50137013.5Yes(≥1)169016.6Yes429742.2 Bosnia- Herze govina

7187Missing1562.2Missing2253.1Missing2433.4Missing2904.0Missing1662.3Missing2273.2Missing2573.6 No687495.6No662092.1No689696.0No604884.250658491.6No523472.8No408256.8 Yes1572.2Yes3424.8Yes480.7Yes84911.8>504376.1Yes172624.0Yes284839.6 Croatia4800Missing1453.0Missing2104.4Missing2224.6Missing2284.8Missing972.0Missing1944.0Missing2004.2 No393181.9No445592.8No455494.9No401183.650415486.5No327568.2No273557.0 Yes72415.1Yes1352.8Yes240.5Yes56111.7>5054911.4Yes133127.7Yes186538.9 Cyprus35Missing00.0Missing00.0Missing00.0Missing00.0Missing00.0Missing00.0Missing00.0 No3188.6No35100.0No35100.0No2777.1503188.6No2674.3No1851.4 Yes411.4Yes00.0Yes00.0Yes822.9>50411.4Yes925.7Yes1748.6 Czech Republic

16992Missing1240.7Missing1661.0Missing1761.0Missing2111.2Missing5843.4Missing1931.1Missing2041.2 No1623495.5No1650597.1No1678098.8No1551991.3501551491.3No1406182.8No1403082.6 Yes6343.7Yes3211.9Yes360.2Yes12627.4>508945.3Yes273816.1Yes275816.2 Denmark2487Missing2469.9Missing2399.6Missing25610.3Missing43917.7Missing24910.0Missing37215.0Missing40216.2 No215286.5No209484.2No218387.8No182573.450205882.8No188275.7No164966.3 Yes893.6Yes1546.2Yes481.9Yes2239.0>501807.2Yes2339.4Yes43617.5 Estonia1318Missing50.4Missing30.2Missing50.4Missing30.2Missing534.0Missing131.0Missing24618.7 No127096.4No127997.0No131099.4No126095.650116588.4No103378.4No67751.4 Yes433.3Yes362.7Yes30.2Yes554.2>501007.6Yes27220.6Yes39530.0 Georgia2689Missing30.1Missing70.3Missing30.1Missing50.2Missing150.6Missing40.2Missing100.4 No263297.9No259296.4No267599.5No248792.550252693.9No221582.4No235387.5 Yes542.0Yes903.4Yes110.4Yes1977.3>501485.5Yes47017.5Yes32612.1 Germany9347Missing211022.6Missing232524.9Missing244626.2Missing8328.9Missing4875.2Missing117112.5Missing145815.6 No666871.3No658470.4No675472.3No749580.250691274.0No610165.3No433246.4 Yes5696.1Yes4384.7Yes1471.6Yes102010.9>50194820.8Yes207522.2Yes355738.1 Greece33252Missing31679.5Missing32599.8Missing335510.1Missing23357.0Missing16164.9Missing17045.1Missing15414.6 No2949988.7No2952488.8No2978789.6No2906587.4502791584.0No2330270.1No2141064.4 Yes5861.8Yes4691.4Yes1100.3Yes18525.6>50372111.2Yes824624.8Yes1030131.0 Hungary13256Missing10117.6Missing10337.8Missing10858.2Missing4553.4Missing3963.0Missing6424.8Missing4973.8 No1188589.7No1184489.4No1212591.5No1133685.5501171988.4No960672.5No800360.4 Yes3602.7Yes3792.9Yes460.4Yes146511.1>5011418.6Yes300822.7Yes475635.9 Ireland380Missing5314.0Missing5414.2Missing5715.0Missing6316.6Missing3910.3Missing6617.4Missing6617.4 No31683.2No31683.2No32284.7No27071.15033889.0No29778.2No24664.7 Yes112.9Yes102.6Yes10.3Yes4712.4>5030.8Yes174.5Yes6817.9 Italy3529Missing3008.5Missing3269.2Missing3479.8Missing68119.3Missing2537.2Missing49714.1Missing60517.1 No316189.6No311388.2No317389.9No263174.650301885.5No248570.4No150642.7 Yes681.9Yes902.6Yes90.3Yes2176.2>502587.3Yes54715.5Yes141840.2

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Table1Continued CountryNSuspected melanomaSuspectedBCCSuspectedSCCSuspectedAKsNevuscountAtypicalnevi(≥1)Lentigines n%n%n%n%n%n%n% Latvia2400Missing43918.3Missing40416.8Missing44318.5Missing632.6Missing692.9Missing743.1Missing532.2 No193980.8No192180.0No195581.5No210487.750208386.8No194581.0No130154.2 Yes220.9Yes753.1Yes20.1Yes2339.7>5024810.3Yes38115.9Yes104643.6 Lithuania5902Missing4267.2Missing4467.6Missing4647.9Missing4858.2Missing4026.8Missing4938.4Missing4878.3 No523588.7No528389.5No541691.8No448476.050486182.4No432873.3No315053.4 Yes2414.1Yes1732.9Yes220.4Yes93315.8>5063910.8Yes108118.3Yes226538.4 Mace donia (FYROM)

1292Missing00.0Missing00.0Missing00.0Missing00.0Missing30.2Missing00.0Missing00.0 No123895.8No118091.3No127198.4No99777.250117590.9No96274.5No71755.5 Yes544.2Yes1128.7Yes211.6Yes29522.8>501148.8Yes33025.5Yes57544.5 Malta432Missing40.9Missing51.2Missing51.2Missing143.2Missing81.9Missing153.5Missing143.2 No41495.8No41997.0No42798.8No37687.05039290.7No36684.7No23754.9 Yes143.2Yes81.9Yes00.0Yes429.7>50327.4Yes5111.8Yes18141.9 Moldova56Missing00.0Missing00.0Missing00.0Missing00.0Missing610.7Missing00.0Missing00.0 No4885.7No5089.3No5598.2No4275.0504987.5No3257.1No3664.3 Yes814.3Yes610.7Yes11.8Yes1425.0>5011.8Yes2442.9Yes2035.7 Norway1323Missing856.4Missing987.4Missing1068.0Missing765.7Missing282.1Missing705.3Missing604.5 No117889.0No117488.7No121591.8No116187.850106880.7No101776.9No84864.1 Yes604.5Yes513.9Yes20.2Yes866.5>5022717.2Yes23617.8Yes41531.4 Poland8391Missing116313.9Missing119514.2Missing125414.9Missing134116.0Missing3794.5Missing98911.8Missing112913.5 No710084.6No696883.0No711184.8No632075.350706984.3No542364.6No591370.5 Yes1281.5Yes2282.7Yes260.3Yes7308.7>5094311.2Yes197923.6Yes134916.1 Portugal7655Missing2503.3Missing2553.3Missing2873.8Missing2122.8Missing2202.9Missing2753.6Missing2593.4 No731495.6No718793.9No734295.9No706892.350685889.6No597778.1No486963.6 Yes911.2Yes2132.8Yes260.3Yes3754.9>505777.5Yes140318.3Yes252733.0 Romania2875Missing1605.6Missing1796.2Missing1836.4Missing1886.5Missing923.2Missing832.9Missing2087.2 No269493.7No263991.8No268693.4No235982.150267593.0No222477.4No174860.8 Yes210.7Yes572.0Yes60.2Yes32811.4>501083.8Yes56819.8Yes91932.0 Russia19400Missing729237.6Missing753138.8Missing771739.8Missing381119.6Missing236412.2Missing691535.6Missing696835.9 No1165260.1No1139158.7No1153359.5No899146.4501577581.3No967749.9No833343.0 Yes4562.4Yes4782.5Yes1500.8Yes659834.0>5012616.5Yes280814.5Yes409921.1 Serbia9080Missing6707.4Missing8269.1Missing9009.9Missing7077.8Missing3984.4Missing6407.1Missing6667.3 No746082.2No792287.3No812989.5No644571.050796487.7No639370.4No544760.0 Yes95010.5Yes3323.7Yes510.6Yes192821.2>507187.9Yes204722.5Yes296732.7 Slovenia808Missing50.6Missing70.9Missing50.6Missing50.6Missing101.2Missing10.1Missing20.3 No74792.5No78396.9No79898.8No76794.95066482.2No56269.6No40650.3 Yes566.9Yes182.2Yes50.6Yes364.5>5013416.6Yes24530.3Yes40049.5 Spain5191Missing123923.9Missing125224.1Missing124724.0Missing122023.5Missing119122.9Missing122023.5Missing121923.5 No389575.0No382873.7No392975.7No366070.550382573.7No326963.0No293756.6 Yes571.1Yes1112.1Yes150.3Yes3116.0>501753.4Yes70213.5Yes103519.9

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frequency of the clinical endpoints in each country. Chi-square and Fisher’s exact tests were used to determine associations with clinical endpoints in univariate analysis to select variables to be included in multivariate analysis.

Multivariate logistic regression models (including age, gen- der, education, skin type, family history of melanoma, per- sonal history of skin cancer, any sun exposure and any sunscreen use) were used to calculate the odds ratio (OR) of each clinical endpoint for ever sunbed use in each country.

Summary ORs (SORs) of estimates from each country were then calculated for each clinical endpoint, with 95% CI, and forest plots were presented with estimates for each country.

Between-country heterogeneities were assessed by Higgins and Thompson’s I2 statistics,23 which can range from zero to 100% – zero indicating a lack of heterogeneity, that is, that the ORs are consistent with each other. All statistical tests were considered significant forP-values≤0.05. Statistical anal- yses were carried out using SAS 9.2.

Data quality control: inclusion and exclusion criteria for countries’eligibility

Important clinical endpoints of this study were represented by suspected skin cancers; indeed, if a suspicious lesion was found during the screening, patients were advised for further diagnostics and treatment, but follow-up data on diagnosis were not collected in all countries due to privacy and legisla- tive issues. Taking into consideration the lack of histopatho- logical confirmation of suspected lesions, we performed a strict data quality check by which we formulated two inclu- sion criteria and two exclusion criteria for countries’ partici- pation in the multivariate analysis. Inclusion/exclusion criteria and related explanations are listed below.

Inclusion criterion 1:<15% of missing values for suspected melanoma and/or suspected BCC and/or suspected SCC.

Missingness can significantly distort the validity of the con- clusions, by reducing the representativeness of the sample.24

Inclusion criterion 2: <20% adolescents among partici- pants. Adolescents are likely not to have had enough time to develop health consequences due to sunbed use, such as melanoma; indeed, a previous investigation showed an increased risk of melanoma associated with sunbed use rang- ing from 19% (non-significant) among adolescents to 49%

and 61% (both significant) among 30–39 and 40–49 year olds.25

Exclusion criterion 1: >10% of adolescents diagnosed with AKs. Estimates from these countries were judged unreliable, as AKs are extremely rare among adolescents.26

Exclusion criterion 2: >20% of subjects with atypical nevi considered to have also a suspected melanoma. Probably, in these countries, atypical nevi were erroneously considered as suspected melanomas and therefore excised, although nevi and atypical nevi only rarely transform into melanomas.27–30 Table1Continued CountryNSuspected melanomaSuspectedBCCSuspectedSCCSuspectedAKsNevuscountAtypicalnevi(≥1)Lentigines n%n%n%n%n%n%n% Sweden17978Missing13157.3Missing12386.9Missing14037.8Missing16519.2Missing12256.8Missing14197.9Missing14378.0 No1606189.3No1565687.1No1646391.6No1447980.5501504383.7No1428879.5No1033057.5 Yes6023.4Yes10846.0Yes1120.6Yes184810.3>5017109.5Yes227112.6Yes621134.6 Switzer land

19751Missing14457.3Missing14057.1Missing14987.6Missing17208.7Missing494825.1Missing18079.2Missing19389.8 No1767389.5No1753288.8No1808191.5No1571979.6501265964.1No1505676.2No1161758.8 Yes6333.2Yes8144.1Yes1720.9Yes231211.7>50214410.9Yes288814.6Yes619631.4 Turkey1854Missing42022.7Missing42522.9Missing44023.7Missing27514.8Missing20711.2Missing22512.1Missing21111.4 No139275.1No139175.0No140775.9No149380.550153082.5No122766.2No105356.8 Yes422.3Yes382.1Yes70.4Yes864.6>501176.3Yes40221.7Yes59031.8 Ukraine18049Missing501327.8Missing521228.9Missing534429.6Missing500027.7Missing184710.2Missing439424.3Missing510528.3 No1273470.6No1236868.5No1262469.9No1177665.2501440979.8No1091360.5No974354.0 Yes3021.7Yes4692.6Yes810.5Yes12737.1>5017939.9Yes274215.2Yes320117.7 N,numberofparticipantsforeachcountry;n,frequencies;AK,actinickeratosis;BCC,basalcellcarcinoma;FYROM,FormerYugoslavRepublicofMacedonia;SCC,squamouscellcarcinoma.

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Results

Thirty countries took part in the Euromelanoma campaigns 2009–2014, for a total of 227 888 participants. Details of coun- tries’ participation over time are provided in Table S1.

Fourteen countries were not eligible for the multivariate sta- tistical analysis, as they failed the data quality check. In particu- lar, seven countries could not be considered as they did not satisfy inclusion criteria: Germany, Latvia, Russia, Spain, Turkey and Ukraine did not meet inclusion criterion 1 (they all had

>15% of missing values for suspected melanoma and/or sus- pected BCC and/or suspected SCC; Table 1); Romania did not meet inclusion criterion 2 (30.2% of participants were adoles- cents; Table S2). Moreover, seven other countries had to be

subsequently removed as they fulfilled exclusion criteria: Mol- dova met exclusion criterion 1, as Russia would have done too had it been included (12.5% and 13.1% of adolescents diagnosed with AKs, respectively; Table S3); Croatia, Cyprus, Denmark, Lithuania, Malta and Serbia met exclusion criterion 2 (>20% of subjects with atypical nevi considered to have also a suspected melanoma), as Germany would have done too had it been included (Table 2).

Consequently, 16 countries were included in the main analy- sis, for a total of 145 980 participants. Details about the demo- graphic, phenotypic and sunbed variables for each eligible country are presented in Table S4. Overall, 64.8% were females and 35.2% males; median age was 43 years (interquartile range 31–59, 6.9% adolescents); 62.3% attained high education and 37.7% low education; 28.5% reported skin type I–II and 71.5%

skin type III–VI. Ever use of sunbed was reported by 11.0% of those who responded to the sunbed questions (15 650/142 204).

Melanoma suspicion rate varied from 1.2% (Portugal) to 7.0% (Slovenia) and was higher than BCC suspicion rate in 6 of 16 (37.5%) countries and than SCC suspicion rate in 16 of 16 (100%) countries (Table 3).

The summary estimate suggested a significant, independent association between suspected melanoma and ever sunbed expo- sure, with between-country heterogeneity [SOR=1.13 (1.00–

1.27), I2=11%] (Fig. 1a).

The SOR of suspected NMSC (pooling together suspected BCC, suspected SCC and AKs) for ever sunbed use was 1.00 (0.91–1.10), without between-country heterogeneity (I2=0%;

Fig. 1b). Models assessing the association of ever sunbed use with suspected NMSC combined in different ways (including suspected BCC and suspected SCC but excluding AKs or includ- ing suspected BCC alone, suspected SCC alone or AKs alone) produced similar results (data not shown).

Furthermore, the summary estimates suggested significant, independent associations between ever sunbed use and: nae- vus count >50 [SOR=1.05 (1.01–1.10), I2=0%] (Fig. 2);

presence of atypical nevi [SOR=1.04 (1.00–1.09), I2=0%]

(Fig. 3); and lentigines, [SOR=1.16 (1.05–1.29), I2=68%]

(Fig. 4).

Estimates for dose–response effect were not available due to low numbers of intermediate and high sunbed users (data not shown).

Discussion

The use of sunbeds is currently permitted in Europe, but restric- tions related to age and skin type of users have been put in place in several European countries. The European legislation for sun- beds, which falls within the Low Voltage Directive (2014/35/EU) for electrical equipment, sets the limits for UV radiation emis- sion to 300 mW/m2 of total effective irradiance (harmonized European standard EN 60335-2-27:2013). Recently, though, arti- ficial tanning has been declared unsafe by the European Table 2 Prevalence of suspected melanoma according to atypical

nevi status for each participating country Prevalence of suspected melanoma

in the absence of atypical nevi

Prevalence of suspected melanoma

in the presence of atypical nevi

Belgium 70 (0.9) 167 (10.3)

Bosnia- Herzegovina

60 (1.2) 91 (5.3)

Croatia 107 (3.3) 603 (46.0)

Cyprus 2 (7.7) 2 (22.2)

Czech Republic 120 (0.9) 507 (18.6)

Denmark 28 (1.5) 54 (23.9)

Estonia 25 (2.4) 18 (6.6)

Georgia 25 (1.1) 29 (6.2)

Germany 151 (3.4) 367 (20.1)

Greece 172 (0.8) 399 (5.3)

Hungary 71 (0.8) 268 (9.5)

Ireland 6 (2.1) 3 (18.8)

Italy 10 (0.4) 52 (10.0)

Latvia 11 (0.7) 11 (3.2)

Lithuania 28 (0.7) 209 (21.3)

Macedonia (FYROM)

28 (2.9) 26 (7.9)

Malta 3 (0.8) 11 (22.9)

Moldova 5 (15.6) 3 (12.5)

Norway 18 (1.8) 40 (18.7)

Poland 25 (0.5) 94 (6.0)

Portugal 35 (0.6) 53 (3.9)

Romania 7 (0.3) 11 (2.1)

Russia 122 (1.6) 212 (11.8)

Serbia 96 (1.6) 806 (41.6)

Slovenia 11 (2.0) 45 (18.5)

Spain 15 (0.5) 42 (6.0)

Sweden 234 (1.7) 335 (15.8)

Switzerland 248 (1.7) 343 (12.7)

Turkey 7 (0.7) 34 (9.7)

Ukraine 122 (1.2) 126 (5.9)

N(%) shown in each box. Countries in which>20% of subjects with atypi- cal nevi were considered to have also a suspected melanoma are high- lighted in bold.

(7)

Commission, whose Scientific Committee on Health, Environ- mental and Emerging Risks (SCHEER) stated that there is no safe limit for exposure to UV radiation from sunbeds.31To cor- roborate the official opinion of the SCHEER, we decided to exploit the Euromelanoma database, which included informa- tion about a large number of participants from 30 countries.

Our goal was to investigate the association of sunbed use with well-established risk factors, namely suspected skin cancer, nevus count, presence of atypical nevi and lentigines.

Our multivariate analysis found a significant association between ever exposure to sunbeds and suspected melanoma, after adjustment for potential confounders. Although it was impossible in this study to ascertain whether suspected mela- nomas were confirmed as such by histopathology, this result appears to confirm the current evidence that sunbed use increases melanoma risk. In particular, our estimate was con- sistent with those found in previous meta-analyses assessing melanoma risk associated with ever using sunbeds: 15% by the IARC,2 16% (10% for Europe alone) by Colantonio et al.,6 19% by Burgard et al.,7 20% by Boniol et al.,4 22%

by Hirst et al.,3 and 25% by Gallagher et al.8 Like others before,6,32 Burgard and co-workers recently raised criticisms about the association between sunbed use and melanoma risk, including limitations of individual studies (selection and recall biases, typical of case-control studies; non-adjustment for certain confounders) and lack of large randomized or prospective studies (which in the case of sunbeds would be unethical or too costly, respectively). Yet, they found similar

results in their meta-analysis, even using a different statistical method.7 In spite of their scepticism then, we believe their recent meta-analysis actually adds to the body of evidence suggesting that sunbed use should be strongly discouraged in order to reduce melanoma risk.

Although the relationship between sunbed use and increased risk of NMSC has been established by previous meta-analyses,2–5 unfortunately, we were not able to confirm this association. Pos- sible explanations include the lack of histopathological confir- mation of the suspected NMSC and the relatively young age of the screenees (median 43 years), which could suggest that par- ticipants did not have sufficient time to develop NMSC–which usually occurs later in life than melanoma.33This is corrobo- rated by the fact that in the present study, NMSC was suspected less than melanoma in multiple countries, in spite of NMSC being much more common than melanoma in epidemiological investigations.34–37

We found a significant association between ever sunbed use and lentigines after adjustment for potential confounders, including sun exposure and sunscreen use. This confirms previ- ous case reports of lentigines occurring after sunbed expo- sure.14–19 Interestingly, these observations reported that the lentigines induced by artificial tanning (so-called ‘sunbed lentigi- nes’) have more worrisome pathologic and ultra-structural fea- tures than common solar lentigines, such as the presence of melanocytic nuclear atypia and abnormally clumped, pleomor- phic melanosomes. Moreover, excised ‘sunbed lentigines’ lacked solar elastosis, which is instead typical of common solar Table 3 Prevalence of the main clinical variables for the 16 countries eligible for the multivariate risk analysis.

Suspected melanoma

Suspected BCC

Suspected SCC

Suspected AKs Nevus count

>50

Atypical nevi1 Solar lentigos

% 95% CI % 95% CI % 95% CI % 95% CI % 95% CI % 95% CI % 95% CI

Belgium 2.5 2.22.9 2.8 2.53.2 0.3 0.20.5 7.6 7.18.2 14.0 13.314.7 17.3 16.618.1 44.1 43.145.1 Bosnia-

Herzegovina

2.2 1.92.6 4.9 4.45.5 0.7 0.50.9 12.3 11.513.1 6.2 5.76.8 24.8 23.825.8 41.1 39.942.3 Czech Republic 3.8 3.54.1 1.9 1.72.1 0.2 0.20.3 7.5 7.17.9 5.4 5.15.8 16.3 15.716.9 16.4 15.917.0 Estonia 3.3 2.44.4 2.7 1.93.8 0.2 0.10.7 4.2 3.25.4 7.9 6.59.5 20.8 18.723.2 36.8 34.039.8 Georgia 2.0 1.52.6 3.4 2.74.1 0.4 0.20.7 7.3 6.48.4 5.5 4.76.5 17.5 16.119.0 12.2 11.013.5 Greece 1.9 1.82.1 1.6 1.41.7 0.4 0.30.4 6.0 5.76.3 11.8 11.412.1 26.1 25.726.6 32.5 32.033.0 Hungary 2.9 2.73.3 3.1 2.83.4 0.4 0.30.5 11.4 10.912.0 8.9 8.49.4 23.8 23.124.6 37.3 36.438.1 Ireland 3.4 1.75.9 3.1 1.55.6 0.3 0.01.7 14.8 11.119.2 0.9 0.22.6 5.4 3.28.5 21.7 17.226.6 Italy 2.1 1.62.7 2.8 2.33.4 0.3 0.10.5 7.6 6.78.7 7.9 7.08.9 18.0 16.719.5 48.5 46.750.3 Macedonia

(FYROM)

4.2 3.25.4 8.7 7.210.3 1.6 1.02.5 22.8 20.625.2 8.8 7.410.5 25.5 23.228.0 44.5 41.847.3 Norway 4.8 3.76.2 4.2 3.15.4 0.2 0.00.6 6.9 5.68.5 17.5 15.519.7 18.8 16.721.1 32.9 30.335.5 Poland 1.8 1.52.1 3.2 2.83.6 0.4 0.20.5 10.4 9.711.1 11.8 11.112.5 26.7 25.727.8 18.6 17.719.5 Portugal 1.2 1.01.5 2.9 2.53.3 0.4 0.20.5 5.0 4.65.6 7.8 7.28.4 19.0 18.119.9 34.2 33.135.3 Slovenia 7.0 5.39.0 2.2 1.33.5 0.6 0.21.5 4.5 3.26.2 16.8 14.319.6 30.4 27.233.7 49.6 46.153.1 Sweden 3.6 3.33.9 6.5 6.16.9 0.7 0.60.8 11.3 10.811.8 10.2 9.810.7 13.7 13.214.3 37.5 36.838.3 Switzerland 3.5 3.23.7 4.4 4.14.7 0.9 0.81.1 12.8 12.313.3 14.5 13.915.1 16.1 15.616.6 34.8 34.135.5 AK, actinic keratosis; BCC, basal cell carcinoma; CI, condence interval; FYROM, Former Yugoslav Republic of Macedonia; SCC, squamous cell carcinoma.

Ábra

Fig. 1b). Models assessing the association of ever sunbed use with suspected NMSC combined in different ways (including suspected BCC and suspected SCC but excluding AKs or  includ-ing suspected BCC alone, suspected SCC alone or AKs alone) produced similar
Figure 1 Forest plots of association of suspected skin cancer with ever use of sunbeds
Figure 2 Forest plot of association of high nevus count ( &gt; 50 nevi) with ever use of sunbeds
Figure 4 Forest plot of association of lentigines on back/chest with ever use of sunbeds

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