Tanning salons and skin cancer

Abstract

Indoor tanning has substantially grown in USA and Europe, more especially in the sun-deprived Northern countries, but also in more sunny countries such as Queensland, Australia. Several studies have specifically addressed the prevalence of sunbed use by children and adolescents in Northern Europe and in the USA, and showed that up to 40–50% of teenagers 15–18 years old had ever used indoor tanning, the highest figures being observed among girls in Scandinavia and Minnesota. Indoor tanning among adults is mostly prevalent in age classes younger than 45. Epidemiological studies have shown that exposure to sunbeds increases the risk of both melanoma and non-melanoma skin cancers: a meta-analysis of 19 studies published before 2006 showed that ever-use of sunbeds was positively associated with melanoma (summary relative risk, 1.15; 95% CI, 1.00–1.31), and first exposure before 35 years of age significantly increased melanoma risk (7 studies, RR = 1.75; 95% CI, 1.35–2.26). Further epidemiological data documented the links between artificial UV tanning and melanoma: two large case-control studies in Minnesota and Australia yielded higher melanoma risks for ever use of sunbeds: 1.74 (95%CI, 1.42–2.14) and 1.41 (95%CI, 1.01–1.96) respectively, risk increasing with greater use and earlier age at first use. The most compelling evidence derives from a large cohort of Norwegian and Swedish women which showed that melanoma risk increased with accumulating exposure (RR for solarium use ≥1 time per month in two or three decades, 10–39 years, 2.37 (95%CI, 1.37–4.08)). In addition, the analysis of a melanoma epidemic observed in Iceland between 1995 and 2002, on the trunk of women younger than 50, pointed out the possible role of the explosion of exposure to sunbeds in this country after 1985. Exposure to artificial ultraviolet is a risk factor for melanoma. Risk appears modest in the general population, but concentrates in the population that started sunbed use before the age of 35; the risk attributable to sunbed use in melanoma patients younger than 30 may be as high as 43 to 76%. Of particular concern is the use of sunbeds by adolescents. Use of sunbeds should be strongly discouraged, and banned under the age of 18.

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Introduction

Indoor tanning is an artificial source of intense and intermittent UV radiation exposure that has gained in popularity since the early 1980s. The indoor tanning industry began to develop in Europe and the USA a time when UVA radiation was thought to be harmless, with the introduction of tanning appliances emitting UVA at levels similar to or even exceeding those from natural sunlight. All tanning devices, other than the high-pressure UVA emitters, emit some UVB as well as UVA. Therefore, the biological consequences are not solely from UVA even though the percentage of UVA can be as much as 99%. The biological effects can be seriously skewed by the small amount of UVB present. The majority of modern canopy-like UV-tanning units are equipped with low-pressure fluorescent lamps with a spectrum mainly emitting in the UVA range plus some UVB (necessary for the induction of a deep long-lasting tan). Sunbeds deliver UVA dosages that are 5–15 times higher than what is delivered by the summer midday sun on a Mediterranean beach. Compared with the summer midday sunlight, these machines emit much higher fluxes of UVA and lower fluxes of UVB.

The indoor tanning industry has grown substantially in Europe over the last three decades, more especially in the sun-deprived Northern countries, but also in more sunny countries such as Italy, and is even developing in Queensland, the sunniest Australian state. In the USA, indoor tanning is now a strong part of the American small business community, with a total number of professional indoor tanning facility businesses of 19 000 in thousands of towns throughout USA, employing 160 000 persons. It is estimated that approximately 30 million Americans visit indoor tanning salons each year.¹ A recent survey of commercial indoor tanning facilities in 116 large cities in the United States found that the average number of tanning salons exceeded the average number of Starbucks cafés or McDonald's restaurants.² This high availability of commercial indoor tanning in urban areas may help explain the high usage of indoor tanning.

Prevalence of sunbed use

Attitudes towards sun exposure have greatly changed in occidental societies over the last century. While before the First World War, women from the upper classes tended to preserve their pale complexion, after the Second World War, the development of mass tourism and holidays in sunny resorts has led to a change in the social perception of tanning which nowadays appears as a sign of good health. The desire of a “good looking” tan all the year round has fuelled the development of indoor artificial tanning. However, there is still limited information on who uses sunbeds, and frequency of use. Prevalence of indoor tanning in various countries can be approached by considering the figures from the controls in case-control studies of sunbed exposure and occurrence of melanoma or other skin cancers. These figures vary greatly from one country to another, and according to age of participants and to the time period considered. Generally speaking, it appears that prevalence of sunbed use for tanning purpose is higher in white-skinned populations from Northern Europe, and in young or middle-aged women.

Surveys have been conducted in Europe, USA and Australia to more specifically address the characteristics of sunbed users, their motivation and their perception of the risks of tanning. 26 of these surveys are summarized in Table 1.^3–28 Several studies have specifically addressed the prevalence of sunbed use by children and adolescents in Northern Europe and in the USA, and showed that up to 40–50% of teenagers 15–18 years old had ever used indoor tanning, the highest figures being observed among girls in Scandinavia, but also in Minnesota. Indoor tanning among adults is mostly prevalent in age classes younger than 45.

Table 1 Prevalence of sunbed use in Europe, USA and Australia (sorted by age of the youngest participants)

Country	Period	Age (years)	Sample size	Sample source	% sunbed use	Reference
a ≥4 times in the previous year.
UK, Scotland	June 2003	8–11	1405	Survey in 23 primary schools	7 (previous 6 months)	Hamlet & Kennedy, 2004^3
					1.1 (regular use)
Denmark	August–October 2008	8–18	1871	Cross sectional survey (random digit dialing)	17 (previous year, 2% once a week or more)	Krarup et al., 2011^4
					2 (8–11)
					13 (12–14)
					43 (15–18)
UK, Nationwide and Six Cities (Liverpool, Stoke/Stafford, Sunderland, Bath/Gloucester, Oxford/Cambridge, Southampton)	National Prevalence study: February 2008–April 2009	11–17	3101 National Prevalence study	Population based	National Prevalence study: 6.8 (ever; 11.2 in 15–17, 8 in girls)	Thompson et al., 2010^5
	Six Cities study: April–May (pilot) and October–November 2008		6209 Six Cities study		Six Cities study: 10 to 11 (ever; higher in Liverpool and Sunderland, and up to 50% in I5–17 girls in these cities)
USA	August–November 1998	11–18	1613	National, population based, telephone survey	11 (previous year)	Cokkinides et al., 2002, 2009^6,7
USA	1999	12–18	10 079	Children of the participants from the Nurses Health Study	9.5 (previous year)	Geller et al., 2002^8
					14.4 (girls), 2.4 (boys),
					24.6 (girls 15–18),
					4.7 (girls 12–14)
USA, Minnesota and Massachusetts	Autumn 2000	14–17	1273	Targeted age list	42 (girls, ever)	Lazovich et al., 2004^9
					12 (boys, ever)
USA	January–December 2005	14–17	6125	Survey in 100 most populous cities	17.1 (girls)	Mayer et al., 2011^10
					3.2 (boys)
					(previous year)
USA	January–December 2005	14–17	5274	Telephone survey in 100 US most populous cities	11.2 (previous year)	Hoerster et al., 2007^11
Germany, Saxony	January–June 2009	14–34	11 773	Participants to a skin cancer screening program	13.4 (ever)	Schmitt et al., 2011^12
					16.4 (women)
					8.7 (men)
Germany	2007	≥14	1501	Representative population telephone survey	28 (ever)	Börner et al., 2009^13
Sweden, Stockholm	1993 and 1999	15–19	1252 (1993)	Questionnaire survey in 60 randomly selected classes (1993)	70 (girls, 1993)^a	Boldeman et al., 2003^14
			2950 (1999)		44 (boys, 1993)^a
					45 (girls, 1999)
					19 (boys, 1999)
Denmark	March 2007	15–59	3437	Population-based sample	29 (previous tear)	Köster et al., 2009^15
					59 (females 15–19)
Italy, Naples	November 1996–February 1997	16–21	756	Random selection at 10 high schools	12.3	Monfrecola et al., 2000^16
UK, Northern Ireland	2004, 2008	≥16	3623	2200 random population samples each year	28 (2004, ever)	Boyle et al., 2010^17
					20 (2008, ever)
USA, Indiana	September 1999	<17– >27	489	Selection of students from the University of Indiana	47 (previous year)	Knight et al., 2002^18
		(80% 17–22)			61 (ever)
USA	November–December 2003	18–23	164	Selection of students from the University at Albany NY	35 (previous year)	Danhoff-Burg and Mosher, 2006^19
Sweden, Stockholm	May 2001	18–37	1752	Random population-based sample	35 (current use)	Bränström et al., 2004^20
Germany, Mannheim	February–May 2008	18–45	500	Population based	46.7 (ever)	Schneider et al., 2009^21
					21 (previous year, 12.5% 1–10 times during the preceding month)
					Average current user: 15 visits per year
USA	2005	18–64	821	Random subset of Health Information National Trends Study	18.1 (women, previous year)	Choi et al., 2010^22
					6.3 (men, previous year)
Spain, Madrid	2007	18–64	2007	Cross sectional survey, representative sample from telephone directory	4.3 (previous year)	Galan et al., 2011^23
					1.9 (men)
					6.6 (women)
					8 (18–29)
USA	2005	≥18	29 394	National Health Interview Survey	13.5 (previous year)	Heckman et al., 2008^24
					From 20.4 (18–29) to 7.8 (≥65)
USA	December 2005	19–25	745	Selection among indoor tanning undergraduate students at Rutgers University	100 (ever)	Bagdasarov et al., 2008^25
Australia, Queensland	February–November 2004	20–75	9298	Population-based telephone interview	<1 (previous year)	Lawler et al., 2006^26
					8.8 (ever)
France	2001	35–60	7303	Participants to SUVIMAX cohort	15 (ever)	Ezzedine et al., 2007^27
UK, Bradford	1996	Not specified	470	Employees at Bradford Hospital	46 (“to some extent”)	Amir et al., 2000^28

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According to a recent review,²⁹ the typical sunbed user is female, between 17 and 30 years old, and tends to live a comparatively unhealthy lifestyle: users smoke cigarettes and drink alcohol more frequently and eat less healthy food than non-users. Users are characterized by a lack of knowledge about health risks of sun and ultraviolet radiation exposure, and prompted by the frequent use of sunbeds by friends or family members and the experience of positive emotions and relaxation by indoor tanning. There is still a lack of information among users, particularly among young people regarding the safety of solariums.

Sunbed use is associated with skin cancer (melanoma and non-melanoma) occurrence

IARC comprehensive review

Observational studies from 1994 to 2005 have documented that exposure of sun-susceptible individuals to sunbed can trigger both melanoma and non-melanoma skin cancers, mainly when this exposure started before 30 years of age. These earlier studies were the subject of a meta-analysis.^30,31

To assess the association between exposure to artificial ultraviolet radiation from sunbeds and cutaneous malignant melanoma and other skin cancers, an International Agency for Research on Cancer working group conducted a comprehensive review of the literature up to March 2006. Only case-control, cohort or cross-sectional studies were selected (Table 2). Based on 19 informative studies, ever-use of sunbeds was positively associated with melanoma (summary relative risk, 1.15; 95% CI, 1.00–1.31), although there was no consistent evidence of a dose–response relationship. First exposure to sunbeds before 35 years of age significantly increased the risk of melanoma, based on 7 informative studies (summary relative risk, 1.75; 95% CI, 1.35–2.26). Based on 5 informative studies, a first exposure distant in time, i.e. 10–20 years before the diagnosis of melanoma, was associated with an increased melanoma risk (summary relative risk, 1.49; 95% CI, 0.93–2.38).

Table 2 Meta-analysis of studies of exposure to artificial UV radiation and risk for melanoma and non-melanoma skin cancers (IARC, 2006)^30,31

Diagnosis	Summary relative risk	95% confidence interval	Number of studies
Melanoma	1.15	1.00–1.31	19
Exposure before the age of 35	1.75	1.35–2.26	7
Exposure distant in time	1.49	0.93–2.38	5
Squamous cell carcinoma	2.25	1.08–4.70	3
Basal cell carcinoma	1.03	0.56–1.90	4

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The summary relative risk of 3 studies of squamous cell carcinoma showed an increased risk (2.25. 95% CI, 1.8–4.7). For basal cell carcinoma, the studies did not support an association. In addition, the evidence does not support a protective effect of the use of sunbeds against damage to the skin from subsequent sun exposure.

Other (major) studies

Epidemiological data published after the IARC report of 2006³⁰ further documented the links between artificial UV tanning and melanoma. These included a survey and two case–control studies in the USA,^32–34 a case-control study in Australia,³⁵ the prospective US Nurse's Health Study³⁶ and the confirmation of previous results of the Norwegian–Swedish cohort study.³⁷ (Table 3).

Table 3 Recent major epidemiological studies of exposure to sunbeds and risk of melanoma

Reference	Country, catchment area	Study period	Cases	Controls	Age limits (years)	Adjustments	Exposure metrics	Adjusted ORs (95% CI)
Lazovich et al., 2010^34	USA, Minnesota	December 2004–March 2009	1617, state-wide registry	1101, driver's licence list, age and sex matched	25–59	Multiple	Ever vs. never	1.74 (1.42–2.14)
							Devices:
							UVB enhanced	2.86 (2.03–4.03)
							primarily UVA	4.44 (2.45–8.02)
							Frequency of use (sessions):
							≤10	1.34 (1.00–1.81)
							11–24	1.80 (1.30–2.49)
							25–100	1.68 (1.25–2.26)
							>100	2.72 (2.04–3.63)
Cust et al., 2011^35	Australia, Sydney, Melbourne, Brisbane	1st July 2000–31st December 2002	604, population-based state cancer registries, diagnosed 1st July 2000–31st December 2002	479, 232 population controls from electoral rolls (compulsory) + 247 spouse/friend controls, frequency matched to cases by city, age and sex	18–39	Multiple (age, sex, city, skin colour and type, sun exposure	Ever vs. never	1.41 (1.01–1.96)
							Age at first use:
							<25 years	1.64 (1.07–2.51)
							≥25 years	1.06 (0.66–1.72)
							Number of lifetime sessions:
							1–10	1.08 (0.72–1.61)
							>10	2.01 (1.22–3.31)
							Age at diagnosis (>10 sessions):
							18–29	6.57 (1.41–30.49)
							30–39	1.60 (0.92–2.77)
Han et al., 2006^36	USA, Nurses’ Health Study, sub-cohort of 32 826 with blood sampling in 1989 and 1980	From 1989–90 blood sampling to 1 June 1998 for SCCs and BCCs and 1st June 2000 for melanomas	200 melanoma, 275 SCC, 283 BCC	804, age matched	30–55 at inclusion (1976)	Multiple (age, constitutional susceptibility score)	Ever vs. never:
							melanoma	2.06 (1.30–3.26)
							SCC	1.44 (0.93–2.24)
							BCC	1.32 (0.87–2.03)
Veierod et al., 2010^37	Norway, Sweden	From 1991–1992, follow-up to 2005	412	106 366	30–50 at inclusion (1991–1992)	Multiple (age, region of residence, hair and skin colour, sun exposure)	Solarium use ≥1 time/mo
							30–39 y	1.49 (1.11–2.00)
							40–49 y	1.61 (1.10–2.35)
							Combined 10–39 y
							rarely, 10–39 y	1.24 (0.96–1.61)
							≥1 time/mo in one decade, 10–39 y	1.38 (0.98–1.94)
							≥1 time/mo in two or three decades, 10–39 y	2.37 (1.37–4.08)

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Despite it including only patients and suffered from a low response rate (36.3%), a survey conducted among patients from an academic dermatology clinic (n = 1518) found that exposure to tanning beds increases the risk of malignant melanoma, especially in women aged 45 years or younger.³² The “ever-use” of tanning beds was a significant risk factor for the development of melanoma (odds ratio (OR), 1.64; 95% confidence interval (95% CI), 1.01–2.67). The risk was greater in women aged 45 years or younger (OR, 3.22; 95% CI, 1.01–11.46). Patients with a history of melanoma were significantly more likely to report tanning bed sessions exceeding 20 min (OR, 3.18; 95% CI, 1.48–6.82); this association was even stronger for women aged 45 years or younger (OR, 4.12; 95% CI, 1.41–12.02).

A population-based case-control study of 423 cases of melanoma and 678 controls in the state of New Hampshire was conducted to estimate the separate effects of sunlamp and sunbed use on melanoma risk. Results suggested a modest association between sunlamp use and melanoma risk, and increasing risk with greater frequency and duration of use. A non-significant association with tanning bed use was found.³³ About 17% of participants ever used a sunlamp, and most use (89%) occurred before 1980. The OR was 1.39 (95% CI 1.00–1.96) for ever using a sunlamp, 1.23 (95% CI 0.81–1.88) for those starting sunlamp use <20 years, and 1.71 (95% CI 1.00–2.92) for those starting ≤20 years. Data suggested increasing risk with number of sunlamp uses and with duration of use (tests of trend p = 0.02). The overall prevalence of tanning bed use was 22% and most use (83%) occurred after 1980. The OR was 1.14 (95% CI 0.80–1.61) for ever using a tanning bed; there was no evidence that risk increased with frequency or duration of use. The OR was 1.96 (95% CI 1.06–3.61) for having used both devices.

A population-based case-control study of indoor tanning in relation to risk of melanoma, the Skin Health Study, was initiated in 2004.³⁴ It was specifically designed to address the limitations of prior research. The study was conducted in Minnesota, a state with documented high prevalence of the behavior.³⁸ More detailed information than most studies was collected to overcome limitation of previous studies (poor information on sun exposure, lack of dose-response data, no distinction among tanning devices) and to assess not only melanoma risk associated with frequent use, years of use, and age at which use began, but also with specific devices and period of use to distinguish exposure to UVB or UVA. Information was also obtained on known confounders, and the study enrolled a sufficiently large sample size to allow for subgroup analyses which had previously rarely been possible.

This large population-based case-control study included 1167 melanoma cases and 1101 controls 25–59 years of age. Key features and results from this study are presented in Table 3. Results were adjusted for multiple factors (age, gender, skin hair and eye colour, sun exposure, outdoor activities). Briefly, risk increased with use: years (P < 0.006), hours (P < 0.0001), or sessions (P = 0.0002). ORs were elevated within each initiation age category; among indoor tanners, years used was more relevant for melanoma development. Thus, in a highly exposed population, frequent indoor tanning increased melanoma risk, regardless of age when indoor tanning began. Elevated risks were observed across devices. This study could overcome limitations of earlier case-control studies and provides strong support for the recent classification by the IARC of tanning devices as carcinogenic in humans.³⁹

Even in Australia, one of the sunniest countries in the world, a case-control study organized within the Australian Melanoma Family Study found sunbed use during adolescence and early adulthood to be associated with increased risk of early-onset melanoma, with risk increasing with greater use, an earlier age at first use and for earlier onset disease.³⁵ 604 cases diagnosed with melanoma at an age between 18 and 39, and 479 controls were recruited in Sydney, Melbourne and Brisbane (the three largest urban populations in Australia comprising about 50% of the Australian population and accounting for a similar proportion of melanoma incidence). Compared with having never used a sunbed, the OR for melanoma associated with ever-use was 1.41 (95% confidence interval (CI) 1.01–1.96), and 2.01 (95% CI 1.22–3.31) for more than 10 lifetime sessions. The association was stronger for earlier age at first use (P_trend 0.02). The association was also stronger for melanoma diagnosed when aged 18–29 years (OR for more than 10 lifetime sessions = 6.57, 95% CI 1.41–30.49) than for melanoma diagnosed when 30–39 years (OR 1.60, 95% CI 0.92–2.77; P_interaction 0.01). Among those who had ever used a sunbed and were diagnosed between 18–29 years of age, three quarters (76%) of melanomas were attributable to sunbed use.

The Nurses' Health Study cohort, initiated in 1976, enrolled 121 700 female registered nurses between the ages of 30 and 55. Between 1989 and 1990, blood samples were collected from 32 826 of the cohort members. The study³⁶ involved 200 histologically confirmed melanoma cases, 275 histologically confirmed SCC cases and 283 self-reported BCC cases (randomly selected from about 2600 self-reported cases). Ever sunlamp usage or tanning salon attendance was a risk factor for melanoma after adjusting for potential confounding variables (OR for ever vs. never usage, 2.06, 95% CI 1.30–3.26), but not significantly for SCCs and BCCs (ORs, 1.44, 95% CI 0.93–2.24, and 1.32, 95% CI 0.87–2.03, respectively).

The Norwegian-Swedish Women's Lifestyle and Health Cohort Study³⁷ included women 30–50 years at enrolment in 1991–1992, and followed them during an average of 14 years. Among 106 366 women with complete follow-up through 2005, 412 melanoma cases were diagnosed. Melanoma risk increased significantly with solarium use at ages 30 to 39 and 40 to 49 years (RRs for solarium use ≥1 time per month, 1.49 (95% CI, 1.11–2.00) and 1.61 (95% CI 1.10–2.35), respectively; P_trend ≤ 0.02). Risk of melanoma associated with solarium use increased with accumulating exposure across additional decades of life (RR for solarium use ≥1 time per month in two or three decades, 10–39 years, 2.37 (95%CI, 1.37–4.08)). This prospective cohort study provides the most compelling epidemiological evidence of a link between sunbed use and cutaneous melanoma.

A melanoma epidemic in Iceland

Iceland is a Nordic country situated at 64–66° north latitude where bright, sunny days are rare. In a collaborative work with the Iceland Cancer Registry and Icelandic dermatologists, we described an epidemic of melanoma starting in 1995.⁴⁰ Before 1995, the melanoma incidence in Iceland was lower than in Denmark and Sweden. In 1990s, it started to rise steeply and after 2000 it surpassed the incidence in other Nordic countries. This phenomenon was mainly noticeable among women. In women, the slow increase in trunk melanoma incidence before 1995 was followed by a significantly sharper increase in incidence, mainly among women aged less than 50 years, resembling an epidemic incidence curve (estimated annual percent change 1995–2002: 20.4%, 95% confidence interval: 9.3, 32.8). In 2002, the melanoma incidence on the trunk had surpassed the incidence on the lower limbs for women; this latter aspect was in sharp contrast with the usual observations prior to 1995 whereby the greatest increase in melanoma incidence in women occurred on lower limbs.

Our investigation concluded that the only plausible explanation for this epidemic was the massive exposure of Icelandic youths to artificial tanning devices after 1985. In 1979, there were only 3 salons in Reykjavik, and by 1988 56 salons with 207 sunbeds were operating. Sunbed use in Iceland expanded rapidly after 1985, mainly among young women, and in 2000 it was approximately 2 and 3 times the levels recorded in Sweden and in the United Kingdom, respectively. In 2002, 70% of women and 35% of men had ever used sunbed for tanning purpose in Iceland. Travels abroad were more prevalent among older Icelanders. The high prevalence of sunbed use probably contributed to the sharp increase in the incidence of melanoma in Iceland. The decrease in incidence of trunk melanoma incidence observed in women after 2002 is most probably due to campaigns initiated by the Icelandic health services end of the 1990s. A campaign by health authorities in 2004 to discourage sunbed use especially by teenage girls resulted in a 50% reduction in the number of sunbeds by 2008.

Conclusions

Although there may be some signs of a discrete decrease in sunbed use in some Northern countries (Sweden, Northern Ireland, Iceland),^14,17,40 prevalence is still very high in most countries where it developed during the last decades. Of particular concern is the use of sunbeds by adolescents in the 15–19 class of age. Contrary to claims by the tanning industry that “to date, no well-designed studies support the connection between melanoma and UV exposure from tanning beds” (www.theita.com, accessed on June 14, 2011), it is now clear that exposure to artificial ultraviolet is a risk factor for melanoma, and to a lesser extent for squamous cell carcinoma. Although the increase in risk may appear modest in the general population (+15%, according to the 2006 IARC report³⁰), most of the risk concentrates in the population that started sunbed use before the age of 35 (+75%, according to the 2006 IARC report,³⁰ and up to more than +200% for frequent use in the 10–39 years period³⁷). Thus, the fraction of risk attributable to sunbed use in patients diagnosed with a melanoma before the age of 30 may be very high: 76% in Australia,³⁵ and 43% in France.⁴¹

Even if there may be some indication that UVA may induce less aggressive melanomas,⁴² and if a participation of the small amount of UVB radiation emitted by tanning devices in their biological effects cannot be ruled out, this tumour remains a potentially lethal one and does represent a public health challenge. Hence, use of sunbeds should be strongly discouraged, and banned under the age of 18. In the USA, in states with policies regarding minors' access to indoor tanning, the prevalence stayed the same or decreased from 1998 to 2004, whereas it increased in states without such policies.⁷

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Footnote

† Contribution to the themed issue on the biology of UVA.

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