Ferrucci 2014
Ferrucci 2014
Ferrucci 2014
Background: Indoor tanning increases skin cancer risk. Beyond early research describing melanoma and
sun lamps, few recent reports describe where individuals indoor tan and whether skin cancer risk varies by
location (business, home-based).
Objective: We sought to assess where individuals tanned indoors and skin cancer risk by tanning device location.
Methods: Multivariate logistic regression was conducted in 2 US case-control studies of melanoma (1161
cases, 1083 controls, ages 25-59 years) and early-onset basal cell carcinoma (375 cases, 382 controls, age
\40 years) conducted between 2004 and 2010.
Results: Most indoor tanners (86.4%-95.1%), especially younger individuals, tanned exclusively in
businesses. Persons who used indoor tanning exclusively in businesses were at increased risk of melanoma
(odds ratio 1.82, 95% confidence interval 1.47-2.26) and basal cell carcinoma (odds ratio 1.69, 95%
confidence interval 1.15-2.48) compared with non-users. Melanoma risk was also increased in the small
number who reported tanning indoors only at home relative to non-users (odds ratio 4.14, 95% confidence
interval 1.75-9.78); 67.6% used sun lamps.
Conclusion: Business-only tanning, despite claims of ‘‘safe’’ tanning, was positively associated with a
significant risk of melanoma and basal cell carcinoma. Home tanning was uncommon and mostly from sun
lamps, which were rarely used by younger participants. Regardless of location, indoor tanning was associated
with increased risk of skin cancer. ( J Am Acad Dermatol 2014;71:882-7.)
Key words: basal cell carcinoma; epidemiology; indoor tanning; melanoma; nonmelanoma skin cancer;
skin cancer.
From the Yale School of Public Healtha and Yale Cancer the NCI of the National Institutes of Health (R01CA106807 and
Center,b New Haven; and Masonic Cancer Centerc and Division P30CA77598).
of Epidemiology and Community Health,d University of Conflicts of interest: None declared.
Minnesota. Accepted for publication June 28, 2014.
The Yale Study of Skin Health in Young People was supported by Reprint requests: Leah M. Ferrucci, PhD, MPH, Yale School of Public
the Yale SPORE in Skin Cancer funded by the National Cancer Health, 55 Church St, Suite 801, New Haven, CT 06510. E-mail:
Institute (NCI) of the National Institutes of Health (NIH) leah.ferrucci@yale.edu.
(P50CA121974; R. Halaban, principal investigator), with Published online July 23, 2014.
additional support from the NCI of the National Institutes of 0190-9622/$36.00
Health (F32CA144335). The Skin Health Study was supported Ó 2014 by the American Academy of Dermatology, Inc.
by the American Cancer Society (RSGPB-04-083-01-CCE) and http://dx.doi.org/10.1016/j.jaad.2014.06.046
882
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melanoma.2,3 Despite the scientific evidence on the self-administered questionnaire and computer-
dangers of indoor tanning, it continues to be popular, assisted telephone interview. Detailed measures of
especially among young people.4 In 2012, indoor sun exposure, sunscreen use, education, income,
tanning salons in the United States had more than and family history of melanoma were collected via
$4.9 billion in revenue; 58.7% was generated directly telephone interview and information on skin, hair
from UV indoor tanning.5 These industry data and eye color, and presence and pattern of freckles
suggest that in the United States approximately and moles were collected via self-administered
22,145 tanning salons are questionnaire. The Skin
frequented by 28 million Health Study was approved
CAPSULE SUMMARY
people each year,5 of which by the institutional review
2.3 million are teenagers.6 d Indoor tanning increases risk of skin board at the University
From this industry infor- of Minnesota (protocol num-
cancer; variation in risk by tanning
mation, it is clear that a ber 0403M58561; approved
device location (home, business) is
substantial amount of recent August 24, 2004) and infor-
understudied.
indoor tanning in the United med consent was obtained
States has taken place in d Indoor tanning occurs predominantly in from the participants.
business locations, yet pub- businesses. All indoor tanning, regardless
lished epidemiologic data of location, is associated with increased Yale Study of Skin Health
have seldom delineated risk of skin cancer. in Young People: BCC
where individuals use indoor d Tanning device proliferation in The Yale Study of Skin
tanning devices. Although all commercial and private settings should Health in Young People was
indoor tanning devices emit be discouraged. a case-control study of early-
UV radiation, the actual UV onset BCC conducted in
exposure may vary substan- Connecticut, described in
tially by setting because of different device types, detail elsewhere.8,9 BCC cases and controls with
exposure time, and safety practices. Thus, location of minor benign skin conditions (both evaluated by
indoor tanning may be a potential determinant of skin biopsy) diagnosed between July 2006 and
skin cancer risk. September 2010 were identified through Yale
To better understand the risks of skin cancer University’s dermatopathology database, as BCC is
associated with where individuals use indoor not collected in the state cancer registry. Eligible
tanning devices (ie, in business, home, other, or participants had to be younger than 40 years at the
mixed locations), we analyzed data from 2 recent US time of skin biopsy, reside in Connecticut, speak
case-control studies: (1) melanoma among indivi- English, and be capable of completing all study
duals ages 25 to 59 years; and (2) early-onset basal components. A total of 389 BCC cases enrolled
cell carcinoma (BCC) among individuals younger (participation rate 72.8%). Randomly sampled
than 40 years. With a younger study population than controls were frequency matched to BCC cases on
prior studies of indoor tanning and study recruitment age at biopsy, gender, and biopsy site, with a total of
from 2004 through 2010, these data provide a 458 controls enrolling (participation rate 60.7%).
relatively current picture of patterns and associated The most common conditions among controls
risks of indoor tanning in the United States. were cyst (16.4%), seborrheic keratosis (16.2%),
and wart (11.4%). All other conditions were
METHODS present among less than 10% of control subjects.
Skin Health Study: Melanoma Analyses are restricted to the non-Hispanic white
Methods for the Skin Health Study, a case-control participants: 96.9% of cases and 85.2% of controls.
study of melanoma, have been published else- Participants completed an in-person interview and
where.7 In brief, persons in Minnesota given the self-administered questionnaires. The structured
diagnosis of invasive cutaneous melanoma from in-person interview assessed numerous characteris-
2004 to 2007 between ages 25 and 59 years were tics, including sociodemographics, sun exposure,
ascertained through the state cancer registry. Persons sunscreen, family history, medical history; self-
without melanoma were frequency matched to reported skin, hair, and eye color; and skin reaction
cases on age and gender, and were randomly to UV exposure. Yale University’s Institutional
selected from the state driver license list (including Review Board approved the study (protocol num-
persons with state identification cards). A total ber 0612002107; approved February 2, 2007) and
of 1167 melanoma cases and 1101 controls (84.6% study participants (or guardians) provided informed
and 69.2% of eligible, respectively) completed a consent.
884 Ferrucci et al J AM ACAD DERMATOL
NOVEMBER 2014
Assessment of indoor tanning and tanning evaluation were excluded and persons who never
device location tanned indoors served as the reference group.
Indoor tanning exposure data were obtained in Multivariate models were adjusted for characteristics
both studies using a questionnaire developed for previously evaluated and reported as potential
the Skin Health Study; details are published else- confounders in the primary indoor tanning analyses
where.7,9 Briefly, participants were asked about their (regardless of device location) in the respective study
indoor tanning history and had color photographs of populations.7,9 The Skin Health Study models were
different tanning devices as visual aids. Both studies adjusted for gender, age at reference date, eye color,
queried ever use of indoor tanning, which included hair color, skin color, freckles, moles, income,
regular tanning beds/booths, high-speed/high- education, family history of melanoma, lifetime
intensity tanning beds/booths, and high-pressure routine sun exposure, lifetime sun exposure from
tanning beds/booths. Data were collected across outdoor activities, lifetime sun exposure from out-
5-year periods between ages 11 and 59 years in the door jobs, lifetime sunburns, and lifetime sunscreen
Skin Health Study and across 4 age periods starting at use. These potential confounders were defined a
age 11 years (ages 11-15, 16-20, 21-30, and 31-40 priori and included in the final models regardless of
years) in the Yale Study of Skin Health. In both statistical significance. Models for the Yale Study of
studies, participants reported the location of the Skin Health were adjusted for age at diagnosis, body
tanning devices (home, business, or other) during site, gender, skin color, family history of melanoma
each time period; no additional descriptions/ and/or nonmelanoma skin cancer, first exposure of
definitions were given for the location descriptions the season to 1 hour of summer sun, prolonged
and participants were not asked to report a specific exposure to the sun, and melanocortin 1 receptor
type of business. With the older age of the Skin gene (MC1R) nonsynonymous variants. These vari-
Health Study population, sun lamp use was also ables were study frequency matching variables,
assessed in this manner. In the Yale Study of altered risk estimates by at least 10%, or were sig-
Skin Health population, participants reported ever nificantly associated with BCC. Analyses were con-
use of sun lamps on a self-administered mailed ducted using SAS software (Version 9.3, SAS Institute
questionnaire; home use was assumed. Inc, Cary, NC) and statistical tests were 2-sided.
Table I. Location of indoor tanning devices among location.7,9 In addition, despite infrequent exclusive
control subjects who reported a history of indoor home indoor tanning, a strong association with
tanning in 2 US case-control studies melanoma was observed, although the CIs were
Skin Health Study Yale Study of Skin Health
wide.
Control subjects Control subjects Our analysis represents a detailed assessment of
Location of indoor N = 545 N = 246 the skin cancer risk associated with recent indoor
tanning device N (%) N (%)
tanning patterns and our results provide data to
Business only 471 (86.4) 234 (95.1) refute a claim made by the indoor tanning industry
Home only 8 (1.5) 2 (0.8) that the risk of skin cancer associated with indoor
Other only or 66 (12.1) 10 (4.1)
tanning in recent studies is ‘‘misleading because
mixed location
researchers often included tanning beds used in
homes and doctors’ offices in addition to those at
salons.’’10 Although the location prevalence data
We observed statistically significant increased risks among controls from our 2 studies are most
of melanoma (OR 1.82, 95% CI 1.47-2.26) and BCC generalizable to the general US population, the
(OR 1.69, 95% CI 1.15-2.48) among individuals who pattern of locations was mirrored in the cases.
reported tanning indoors exclusively in business In older melanoma studies that reported on
locations compared with those who never tanned location, indoor tanning devices in homes do appear
indoors (Table II). The association between business- to have been more common than in our current
only indoor tanning and BCC was unchanged analysis11-14 and is in line with our finding that older
(OR 1.74, 95% CI 1.17-2.58) when we removed individuals were more likely to report home-based
28 individuals (19 reported business-only indoor indoor tanning. However, our data in tandem with
tanning) who reported any UV light therapy for contemporary economic data on tanning salons
medical conditions (eg, acne, psoriasis); this infor- indicate that business-based tanning accounts for
mation was not queried in the Skin Health Study. the vast majority of recent indoor tanning. A pooled
Because of infrequent home tanning, the risk analysis cited by the indoor tanning industry on
of skin cancer associated with indoor tanning tanning salon use being harmless in relation to skin
exclusively in the home could only be examined in cancer relied on data from study populations
the Skin Health Study. The majority (67.6%) of the 34 composed of older individuals and is outdated given
home-only indoor tanners reported using only sun the rapidly changing pattern of indoor tanning in the
lamps. For individuals who reported exposure to any United States.15,16 Furthermore, only a subset of
tanning device only at home, the risk of melanoma studies from a large meta-analysis17 were included
was 4.14 (95% CI 1.75-9.78). in the pooled study and the authors conducted only a
Among indoor tanners who reported other univariate pooled analysis without adjustment for
locations only or a combination of any 2 locations, potential confounders.15,16 An additional limitation
we observed a statistically significant increased risk of the older data is that most studies did not evaluate
of melanoma (OR 1.63, 95% CI 1.08-2.46). There exclusive use in each location11-13 and 1 only
was no clear association with BCC (OR 1.24, 95% CI evaluated location among frequent tanners.13
0.38-4.04), although the sample size was limited. Medical phototherapy is prescribed for select
conditions, particularly skin-related conditions, such
DISCUSSION as psoriasis. Even in our BCC population, who sought
In 2 recent US skin cancer case-control studies, we care from a dermatologist, less than 5% of individuals
observed a high prevalence of prior indoor tanning. reported prescribed medical phototherapy, so it is
Indoor tanning was more common in the Yale Study likely exposure to UV for medical reasons would
of Skin Health than in the Skin Health Study, which compose a small percentage of total exposure to
was expected given the younger participants. artificial UV in the United States. In addition, the
Among those who tanned indoors, nearly all tanning indoor tanning industry risk estimate for melanoma
occurred in business settings, with exclusive indoor associated with medical phototherapy is based on
tanning in businesses most common among younger 1 study from 1990 in which 27 individuals reported
individuals in both studies. Given the low prevalence such use,11 resulting in a nonsignificant univariate
of indoor tanning outside of business locations, association (OR 1.96, 95% CI 0.89-4.33).15,16
the associations we observed with business-based Importantly, in a sensitivity analysis in our BCC
indoor tanning and skin cancer were very similar or population that removed persons who reported
identical to those we previously reported in these medical phototherapy, the risk estimate for business-
populations for all indoor tanning, regardless of only indoor tanning did not appreciably change.
886 Ferrucci et al J AM ACAD DERMATOL
NOVEMBER 2014
Table II. Odds ratios and 95% confidence intervals for the association between indoor tanning by location and
basal cell carcinoma (age \40 years) and melanoma (ages 25-59 years)
Skin Health Study Yale Study of Skin Health
Melanoma Multivariate BCC Multivariate
Characteristics Cases/controls OR* (95% CI) Cases/controls ORy (95% CI)
Indoor tanning in businesses only
Never 433/538 1.00 129/136 1.00
Ever 622/471 1.82 (1.47-2.26) 238/234 1.69 (1.15-2.48)
Indoor tanning at home only
Never 433/538 1.00 129/136 -
Ever 26/8 4.14 (1.75-9.78) 0/2 -
Indoor tanning in other locations
only or mixed locations
Never 433/538 1.00 129/136 1.00
Ever 80/66 1.63 (1.08-2.46) 8/10 1.24 (0.38-4.04)
BCC, Basal cell carcinoma; CI, confidence interval; OR, odds ratio.
*Adjusted for gender, age at reference date (in years), eye color (gray/blue, green, hazel, or brown), hair color (red, blond, light brown, or
dark brown/black), skin color (very fair, fair, light olive, versus dark olive, brown, very dark brown or black), freckles (none, very few, few,
some/many), moles (none, very few, few, some/many), annual income ( # $60,000, [$60,000, missing), education (completed college, did
not complete college), family history of melanoma (yes, no, missing), lifetime routine sun exposure (continuous), lifetime sun exposure from
outdoor activities (continuous), lifetime sun exposure from outdoor jobs (continuous), lifetime sunburns (continuous), and lifetime
sunscreen use (continuous).
y
Adjusted for age at diagnosis (continuous), body site (head/neck, trunk, extremity), gender, skin color (olive, fair, very fair), family history of
melanoma and/or nonmelanoma skin cancer (yes, no), first exposure of the season to 1 hour of summer sun (turn brown with no sunburn,
mild sunburn followed by some degree of tanning, painful sunburn for a few days followed by peeling, severe sunburn with blistering),
prolonged exposure to the sun (very brown and deeply tanned, moderately tanned, only mildly tanned because of tendency to peel, only
freckled or no suntan at all), and MC1R nonsynonymous variants (0, 1, $ 2 variants).
Larger studies are needed to clarify if differences data on health risks associated with indoor tanning in
exist between home-based versus business-based these locations are not available and these other
use of tanning devices in relation to skin cancer risk. types of businesses are likely to represent a very
For home-based tanning, older devices emitting small percentage of business-only tanning in our
higher levels of UVB compared with normal solar populations. Also, although unlikely, it is possible
UV radiation7 may still be in use or use may be more some participants reported medical phototherapy as
frequent if a device is located in one’s home. Nearly business-related tanning. However, phototherapy
two thirds of the home indoor tanners reported using as assessed by a separate question in our BCC
only sun lamps and overall sun lamp use was more population was very rare. Finally, the control groups
common in older study participants. Sun lamps have were different in these 2 studies, each of which
largely become obsolete, so are unlikely to may be subject to potential selection bias, but,
contribute to skin cancer risk in future cohorts. importantly, risk estimates and prevalence figures
Because the risk of skin cancer with use of newer were similar despite the differing control popula-
tanning beds, located primarily in business locations, tions (skin biopsy and driver license controls).
is high,18 it is reasonable to assume similar or even Our findings indicate that indoor tanning is
higher risks if these devices proliferate in homes, associated with an increased risk of skin cancer
suggesting a possible regulatory need. regardless of location. As states and countries around
Although these 2 case-control studies capture the the world enact legislation to restrict minors from
indoor tanning patterns of respondents over the past commercial indoor tanning,19-21 regulatory and
few decades, it should be recognized that very policy efforts should consider all indoor tanning
recently, tanning beds/booths have become fixtures venues, including the home, as some may allow
in fitness centers, hair salons, spas, and apartment indoor tanning access to minors otherwise restricted
complexes. Unfortunately, we did not collect this from tanning salons.
level of detail on tanning location, as tanning outside In conclusion, indoor tanning in businesses has
of salons is a more recent phenomenon. Many of accounted for the majority of recent indoor tanning
these newer indoor tanning locations are likely to exposure in young and middle-aged people alike.
have less supervision than a tanning salon and In addition, despite federal and some state-level
introduce additional safety risks. To our knowledge, provisions requiring indoor tanning salons to adhere
J AM ACAD DERMATOL Ferrucci et al 887
VOLUME 71, NUMBER 5
to exposure limits, indoor tanning in businesses was 9. Ferrucci LM, Cartmel B, Molinaro AM, Leffell DJ, Bale AE, Mayne
associated with increased risk of melanoma and ST. Indoor tanning and risk of early-onset basal cell carcinoma.
J Am Acad Dermatol 2012;67:552-62.
nonmelanoma skin cancer. This risk, combined 10. Serrano J. With youth tanning law, Texas aims to lower
with the prevalence data on business-based indoor melanoma risk. New York Times. August 30, 2013; A15A.
tanning, indicates that indoor tanning in businesses 11. Walter SD, Marrett LD, From L, Hertzman C, Shannon HS, Roy P.
accounts for a large percentage of the current total The association of cutaneous malignant melanoma with the use
indoor tanning attributable risk for skin cancer in of sunbeds and sunlamps. Am J Epidemiol 1990;131:232-43.
12. Bataille V, Boniol M, De Vries E, Severi G, Brandberg Y, Sasieni P,
the United States. Indoor tanning, regardless of et al. A multicenter epidemiological study on sunbed use and
location, is harmful to health, and proliferation of cutaneous melanoma in Europe. Eur J Cancer 2005;41:2141-9.
indoor tanning devices in all locations should be 13. Westerdahl J, Ingvar C, Masback A, Jonsson N, Olsson H.
discouraged. Risk of cutaneous malignant melanoma in relation to use
of sunbeds: further evidence for UV-A carcinogenicity. Br J
Cancer 2000;82:1593-9.
REFERENCES 14. Chen YT, Dubrow R, Zheng T, Barnhill RL, Fine J, Berwick M.
1. El Ghissassi F, Baan R, Straif K, Grosse Y, Secretan B, Bouvard V, Sunlamp use and the risk of cutaneous malignant melanoma:
et al. A review of human carcinogensepart D: radiation. a population-based case-control study in Connecticut. USA.
Lancet Oncol 2009;10:751-2. Int J Epidemiol 1998;27:758-65.
2. Boniol M, Autier P, Boyle P, Gandini S. Cutaneous melanoma 15. Papas M, Chappelle A, Grant W. Differential risk of malignant
attributable to sunbed use: systematic review and meta- melanoma by sunbed exposure type [abstract]. Am J Epide-
analysis. BMJ 2012;345:e4757. miol 2011;173:S251.
3. Wehner MR, Shive ML, Chren MM, Han J, Qureshi AA, Linos E. 16. Levy J. Connecticut SB54 opposition testimony. Available
Indoor tanning and non-melanoma skin cancer: systematic from: URL:http://www.cga.ct.gov/2012/PHdata/Tmy/2012SB-
review and meta-analysis. BMJ 2012;345:e5909. 00054-R000307-Joseph%20Levy,%20Executive%20Director,
4. Guy GP, Berkowitz Z, Watson M, Holman DM, Richardson LC. %20International%20Smart%20Tan%20Network-TMY.PDF. Ac-
Indoor tanning among young non-Hispanic white females. cessed October 23, 2013.
JAMA Intern Med 2013;173:1920-2. 17. International Agency for Research on Cancer Working Group on
5. IBISWorld. IBISWorld industry report 81219c: tanning salons in Artificial Ultraviolet Light and Skin Cancer. The association of
the United States. Available from: URL:http://clients1.ibisworld. use of sunbeds with cutaneous malignant melanoma and other
com/reports/us/industry/ataglance.aspx?entid=1721. Acce- skin cancers: a systematic review. Int J Cancer 2007;120:1116-22.
ssed August 5, 2013. 18. Colantonio S, Bracken MB, Beecker J. The association of indoor
6. Levine JA, Sorace M, Spencer J, Siegel DM. The indoor UV tanning and melanoma in adults: systematic review and
tanning industry: a review of skin cancer risk, health benefit meta-analysis. J Am Acad Dermatol 2014;70:847-57.e18.
claims, and regulation. J Am Acad Dermatol 2005;53:1038-44. 19. Dellavalle RP, Guild S. Additional restrictions of indoor UV
7. Lazovich D, Vogel RI, Berwick M, Weinstock MA, Anderson KE, tanning. Arch Dermatol 2012;148:1093-5.
Warshaw EM. Indoor tanning and risk of melanoma: a 20. Pawlak MT, Bui M, Amir M, Burkhardt DL, Chen AK, Dellavalle
case-control study in a highly exposed population. Cancer RP. Legislation restricting access to indoor tanning
Epidemiol Biomarkers Prev 2010;19:1557-68. throughout the world. Arch Dermatol 2012;148:1006-12.
8. Ferrucci LM, Cartmel B, Molinaro AM, Gordon PB, Leffell DJ, 21. Gosis B, Sampson BP, Seidenberg AB, Balk SJ, Gottlieb M,
Bale AE, et al. Host phenotype characteristics and MC1R in Geller AC. Comprehensive evaluation of indoor tanning
relation to early-onset basal cell carcinoma. J Invest Dermatol regulations: a 50-state analysis, 2012. J Invest Dermatol
2012;132:1272-9. 2014;134:620-7.