Abstract
Background
Frequent exposure to ultraviolet light in early life has more detrimental and long-term effects on skin than in adulthood. Teenagers with strong sun-seeking behaviors may be more likely to use an indoor tanning bed than those who seek less sun, probably due to addictiveness of ultraviolet exposure. We aimed to examine associations between sun exposure behaviors and average annual indoor tanning usage frequency during high school/college in US females.
Methods
In this cross-sectional study, we used data from The Nurses’ Health Study II, a large prospective cohort of US female nurses. We included a total of 81,746 white females who answered the average annual frequency of indoor tanning during high school/college. Our study exposures were average weekly time spent outdoors in a swimsuit and average percentage of time of wearing sunscreen at the pool or beach during their teenage years, average weekly hours spent outdoors in direct sunlight in daytime during high school/college, and the number of severe sunburns which blistered between ages 15–20. Main outcomes was average annual frequency of indoor tanning bed usage during high school/college.
Results
In multivariable-adjusted logistic regression, we demonstrated positive associations between the sun exposure behaviors and the indoor tanning habit. Specifically, teenagers who spent daily outdoors in a swimsuit (adjusted odds ratio [aOR], 95% confidence interval [CI] for daily vs. <1/week: 2.68, 1.76–4.09) or who had ≥ 10 sunburns that blistered (aOR, 95% CI for ≥ 10 vs. never: 2.18, 1.53–3.10) were more likely to use indoor tanning beds ≥ 12 times/year. Also, teenagers/undergraduates who spent ≥ 5hours/week outdoors in direct sunlight during daytime used indoor tanning ≥ 12 times/year (aOR, 95% CI: 2.18, 1.39–3.44) than those who spent < 1/week. However, there was not a significant association between average uses of sunscreen at the pool/beach and indoor tanning bed. Multivariable-adjusted linear regression models also showed similar results.
Conclusions
Teenagers who spent more time outdoors or got more sunburns tended to use indoor tanning more frequently. These findings provide evidence that teenagers with strong sun-seeking behaviors may have excessive exposure to artificial ultraviolet radiation as well.
Introduction
Skin cancer is the most common malignancy in the United States (1). Ultraviolet (UV) radiation is the major etiologic agent of skin cancer development and has been classified as “carcinogenic to humans” (group1) by the International Agency for Research on Cancer in 2009 (2). Tanning is defined as intentional exposure to UV radiation that darkens the skin for cosmetic purposes, typically achieved through outdoor sun exposure for a long time or use of indoor tanning beds that emit artificial UV radiation (3, 4). Despite risks associated with tanning, people still pursue it, probably due to the reinforcing effects of UV radiation on tanning behaviors. Such reinforcing effects are created by the many neuropeptides released from the skin after exposure to UV radiation, which can offer relaxation and increase the sense of well-being (5, 6). In fact, tanning is becoming more and more popular in the US. Among American college students, over 70% students intentionally seek a tan outdoors (7); according to a review published in 2018 (3), more than 10 million people use indoor tanning each year in the US, many of whom are adolescent girls and young females (8). However, exposure to UV in early ages has more harmful and longer effects on skin cancer risk than in adults (9). Therefore, understanding tanning behaviors during early life is important for skin cancer prevention and reduction in burden of the skin cancer among young US females.
Among 6,903 non-Hispanic white adolescents aged 13 to 19 years (51.4% females), frequent sunbathers were females and far more likely to use indoor tanning beds than those who never sunbathed (10). Similarly, another study consisting of 281 white females under age 40 reported that female indoor tanners (73.3% of the females in the sample) during early ages more frequently sunbathed than females who never tanned indoors (11). However, these studies were limited by a lack of information of frequency of indoor tanning bed use during early life and outdoor sun-seeking behaviors as well as modest sample size. In addition, the studies reported that females excessively used tanning beds more than males during early life indicating that females are more likely to develop skin cancer and benefit from skin cancer screening (10, 11). Accordingly, female-focused larger investigation on association between outdoor and indoor tanning behaviors in their early ages is warranted.
Given the above facts, we hypothesized that females who had stronger sun-seeking behaviors would tend to use indoor tanning facilities more frequently. Thus, we sought to investigate the association between a series of outdoor sun-seeking behaviors and frequency of indoor tanning using data from the Nurses’ Health Study II (NHS II), a large well-characterized cohort of US females.
Methods
Study Population
The NHS II is a large prospective cohort focusing on health and disease risk factors. In 1989, the cohort enrolled 116,429 female nurses aged 25 to 42 years who resided in 1 of 14 US states with a large number of registered nurses. The initial self-administered questionnaires asked demographic factors, medical/familial histories, and health-related information of their early life. Some health habits in early ages were additionally asked in follow-up surveys. Details of this cohort have been described previously (12). In this study, we included white females who answered the average annual frequency of indoor tanning during high school/college. The study protocol was approved by the institutional review boards of the Brigham and Women’s Hospital and Harvard T.H. Chan School of Public Health, and those of participating registries as required. Written informed consent was also obtained from all study participants. This study followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guidelines.
Outcome
Participants reported their frequency of tanning bed use during high school/college by choosing from the following 6 categories: none, 1–2, 3–5, 6–11, 12–23, and ≥ 24 times per year in questionnaire. We recategorized the average annual indoor tanning frequencies to 4 categories (none, 1–2, 3–11, and ≥ 12 times per year). Also, we converted the responses from the original 6 categories to continuous values by assuming each level of the categories as 0, 1.5, 4.5, 9, 18, and 24 times per year, respectively (13).
Exposures
We collected participants’ responses to the outdoor sun-seeking behavior-related questions that include average weekly time spent outdoors in a swimming suit as a teenager (5 categories: <1, 1, 2, several, and daily per week), average percentage of time of wearing sunscreen at the pool/beach as a teenager (5 categories: 100%, 75%, 50%, 25%, and 0%), average weekly hours spent outdoors in direct sunlight in daytime during high school/college (3 categories: <1, 2–4, and ≥ 5 hours per week), and the number of severe sunburns which blistered between ages 15–20 (5 categories: never, 1–2, 3–4, 5–9, and ≥ 10 times).
Covariates
We included the following participants-reported variables as our covariates - age, average number of cigarettes per day at age 15–24, number of drinks of alcohol at age 15–22, average frequencies of strenuous physical activity/sports at least twice per week during high school and ages 18–22, hair color (red, blonde, light brown, dark brown and black), family history of melanoma (yes vs. no), personal history of major chronic diseases (yes vs. no), and moles on lower legs (none, 1–2, 3–9, and ≥ 10). We defined a participant had major chronic diseases when they reported any cancer, myocardial infarction, stroke, type 2 diabetes, hypertension, inflammatory bowel disease, rheumatoid arthritis, and/or multiple sclerosis in their medical history question.
Statistical Analysis
We calculated age-standardized characteristics and outdoor sun-seeking behaviors according to average annual frequency of indoor tanning bed usage during high school/college. Continuous variables were presented as mean (standard deviation, SD) and categorical variables were presented as percentage. We performed age and multivariable-adjusted multinomial logistic regression using the 4 categorized outcome to calculate adjusted odds ratios (aORs) with 95% confidence intervals (CIs) for the association between outdoor sun-seeking behaviors and the average annual frequency of indoor tanning bed use during early life. In the multivariable-adjusted model, for each exposure variable, we adjusted for all covariates described above. In the same way, we conducted age- and multivariable-adjusted linear regression but using the continuous outcome values, yielding adjusted β (95% CI). In all regression models, to reduce the number of observations deleted because of missing values in covariates, we created indicator variables of the missing data in all covariates and adjusted them as well.
All statistical tests were two-sided, and we determined statistical significance using a threshold of p-value < 0.05. All analyses were carried out using Statistical Analysis System software (version 9.4; SAS Institute, Cary, NC).
Results
Age-standardized characteristics of participants according to frequencies of tanning bed usage during high school/college are shown in Table 1. A total of 81,746 eligible female nurses were included in the study. 7,415 (9.1%) females used indoor tanning beds during high school/college, among whom 1,227 (1.5%) reported that they used indoor tanning beds with high frequency (≥ 12 times/year). Females who used tanning beds more often during early life tended to be younger and were heavier smokers and drinkers during their early life. They also tended to engage in more strenuous physical activity or sports during their early life and had higher nevus counts on their lower legs. The distributions of other characteristics, such as hair color, family history of melanoma, and history of major chronic diseases, were similar across the 4 categories of the average frequency of indoor tanning bed usage.
Table 1.
Age-standardized characteristics according to average annual frequency of indoor tanning bed usage during high school/college in US femalesa
| Characteristics | None | 1–2 | 3–11 | ≥12 |
|---|---|---|---|---|
| Number of participants | 74,331 | 3,400 | 2,788 | 1,227 |
| Age, years | 34.8 (4.6) | 32.8 (5.0) | 32.2 (5.0) | 31.3 (4.8) |
| Average number of cigarettes per day at age 15–24 | 11.1 (7.6) | 10.9 (8.1) | 11.1 (8.4) | 12.1 (8.6) |
| Number of drinks of alcohol at age 15–22 b | 1.8 (2.9) | 2.1 (2.9) | 2.3 (3.2) | 2.5 (3.5) |
| Average frequencies of strenuous physical activity/sports at least twice per week during high school and ages 18–22 c | 4.7 (3.6) | 5.0 (3.6) | 5.1 (3.6) | 5.2 (3.6) |
| Hair color | ||||
| Red, % | 3.6 | 2.7 | 3.5 | 1.9 |
| Blonde, % | 14.6 | 16.1 | 16.1 | 17.8 |
| Dark brown, % | 35.7 | 34.1 | 36.2 | 32.8 |
| Black, % | 3.1 | 1.2 | 1.3 | 0.8 |
| Family history of melanoma, % | 4.2 | 4.8 | 6.5 | 5.0 |
| History of major chronic diseases, % d | 12.3 | 12.7 | 10.9 | 10.6 |
| The number of moles on lower legs | ||||
| 1–2, % | 18.5 | 18.4 | 19.6 | 18.0 |
| 3–9, % | 16.6 | 17.3 | 18.4 | 17.0 |
| 10+, % | 14.1 | 16.9 | 15.2 | 19.7 |
| Average weekly time spent outdoors in a swimsuit as a teenager | ||||
| 1, % | 9.5 | 8.3 | 7.3 | 4.8 |
| 2, % | 16.0 | 14.9 | 14.0 | 10.6 |
| Several, % | 45.1 | 50.9 | 51.7 | 53.9 |
| Daily, % | 15.4 | 18.0 | 20.4 | 25.1 |
| Average percentage of time of wearing sunscreen at the pool or beach as a teenager | ||||
| 75, % | 4.1 | 3.7 | 3.1 | 3.1 |
| 50, % | 9.9 | 9.7 | 9.4 | 7.9 |
| 25, % | 22.4 | 26.2 | 23.7 | 20.5 |
| 0, % | 62.2 | 59.5 | 63.1 | 67.0 |
| Average weekly hours spent outdoors in direct sunlight in the middle of the day during high school/college | ||||
| 2–4, % | 32.9 | 31.1 | 24.0 | 19.6 |
| 5+, % | 59.6 | 64.2 | 72.8 | 77.2 |
| The number of severe sunburns which blistered between ages 15–20 | ||||
| 1–2, % | 38.3 | 42.6 | 40.4 | 39.0 |
| 3–4, % | 16.6 | 20.2 | 18.4 | 18.3 |
| 5–9, % | 7.2 | 8.6 | 9.7 | 11.0 |
| 10+, % | 2.4 | 3.1 | 3.6 | 5.6 |
Note:
Values are means (SD) for continuous variables, percentages for categorical variables, and are standardized to the age distribution of the study population except for baseline age;
Number of usual drinks equals total of bottles/cans of beer, plus 4 oz. glasses of wine, plus shots of liquor;
Strenuous (aerobic) physical activity or sports mean swimming, aerobics, field hockey, basketball, cycling, and running;
Major chronic diseases include cancer, myocardial infarction, stroke, type 2 diabetes, hypertension, inflammatory bowel disease, rheumatoid arthritis, and multiple sclerosis.
The age- and multivariable-adjusted odds ratios for the association between outdoor sun-seeking behaviors and indoor tanning frequency during high school or college are presented in Table 2. In multivariable-adjusted models, being outdoors more often in a swimsuit as a teenager, spending more time outdoors in direct sunlight in the middle of the day during high school/college, and experiencing more severe sunburns between ages 15–20 were significantly associated with higher frequency of average annual indoor tanning bed usage. Specifically, teenagers who spent daily outdoors in a swimsuit (aOR, 95% CI for daily vs. <1 per week: 2.68, 1.76–4.09) or who had ≥ 10 sunburns that blistered (aOR, 95% CI for ≥ 10 vs. never: 2.18, 1.53–3.10) were more likely to use indoor tanning beds ≥ 12 times/year. Also, teenagers/undergraduates who spent ≥ 5 hours per week outdoors in direct sunlight during daytime used indoor tanning ≥ 12 times/year (aOR, 95% CI: 2.18, 1.39–3.44) than those who spent < 1 per week. However, there was not a significant association between sunscreen usage at the pool/beach and the frequency of indoor tanning bed usage.
Table 2.
Age and multivariable-adjusted logistic regression for the association of sun-seeking behaviors with average annual frequency of indoor tanning bed usage during high school/college
| None | 1–2 | 3–11 | ≥12 | |||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Na | Na | Model 1 | Model 2b | Na | Model 1 | Model 2b | Na | Model 1 | Model 2b | |
| Average weekly time spent outdoors in a swimsuit as a teenager | ||||||||||
| <1 | 9,270 | 215 | 1.00 | 1.00 | 140 | 1.00 | 1.00 | 54 | 1.00 | 1.00 |
| 1 | 6,323 | 230 | 1.49 (1.23–1.79) | 1.31 (1.00–1.71) | 164 | 1.60 (1.27–2.01) | 1.45 (1.06–1.98) | 51 | 1.25 (0.85–1.84) | 1.34 (0.79–2.27) |
| 2 | 10,603 | 444 | 1.65 (1.40–1.95) | 1.50 (1.19–1.89) | 331 | 1.84 (1.51–2.25) | 1.44 (1.09–1.91) | 110 | 1.52 (1.10–2.11) | 1.22 (0.76–1.96) |
| Several | 29,759 | 1,553 | 1.99 (1.72–2.30) | 1.69 (1.38–2.07) | 1,304 | 2.48 (2.08–2.96) | 2.01 (1.58–2.55) | 578 | 2.70 (2.04–3.58) | 2.45 (1.65–3.64) |
| Daily | 10,133 | 559 | 2.07 (1.77–2.44) | 1.80 (1.43–2.26) | 523 | 2.87 (2.37–3.47) | 2.25 (1.73–2.93) | 276 | 3.71 (2.76–4.98) | 2.68 (1.76–4.09) |
| Average percentage of time of wearing sunscreen at the pool or beach as a teenager | ||||||||||
| 100% | 950 | 34 | 1.00 | 1.00 | 20 | 1.00 | 1.00 | 18 | 1.00 | 1.00 |
| 75% | 2,575 | 127 | 1.29 (0.88–1.90) | 1.16 (0.68–1.96) | 92 | 1.56 (0.95–2.55) | 2.23 (1.05–4.76) | 44 | 0.81 (0.46–1.41) | 0.63 (0.29–1.38) |
| 50% | 6,296 | 317 | 1.34 (0.93–1.92) | 1.09 (0.67–1.78) | 270 | 1.91 (1.20–3.02) | 2.39 (1.16–4.92) | 101 | 0.78 (0.47–1.30) | 0.66 (0.33–1.33) |
| 25% | 14,310 | 871 | 1.67 (1.18–2.37) | 1.42 (0.89–2.27) | 660 | 2.14 (1.37–3.37) | 2.43 (1.19–4.95) | 266 | 0.96 (0.59–1.56) | 0.88 (0.46–1.70) |
| 0% | 40,614 | 1,646 | 1.31 (0.93–1.85) | 1.07 (0.67–1.71) | 1,412 | 2.03 (1.30–3.17) | 2.29 (1.13–4.64) | 635 | 1.11 (0.69–1.78) | 0.88 (0.46–1.69) |
| Average weekly hours spent outdoors in direct sunlight in the middle of the day during high school/college | ||||||||||
| Average weekly time spent outdoors in a swimsuit as a teenager | ||||||||||
| <1 | 5,574 | 142 | 1.00 | 1.00 | 76 | 1.00 | 1.00 | 33 | 1.00 | 1.00 |
| 2–4 | 24,162 | 1,013 | 1.53 (1.28–1.83) | 1.59 (1.23–2.06) | 655 | 1.80 (1.42–2.29) | 1.86 (1.31–2.65) | 222 | 1.36 (0.94–1.96) | 1.12 (0.70–1.81) |
| ≥5 | 43,564 | 2,221 | 1.76 (1.48–2.09) | 1.59 (1.24–2.04) | 2,033 | 2.89 (2.29–3.64) | 2.83 (2.01–3.98) | 958 | 2.96 (2.09–4.20) | 2.18 (1.39–3.44) |
| The number of severe sunburns which blistered between ages 15–20 | ||||||||||
| Never | 26,144 | 911 | 1.00 | 1.00 | 784 | 1.00 | 1.00 | 341 | 1.00 | 1.00 |
| 1–2 | 28,317 | 1,444 | 1.45 (1.33–1.58) | 1.42 (1.25–1.62) | 1,161 | 1.35 (1.23–1.48) | 1.24 (1.08–1.42) | 490 | 1.31 (1.14–1.50) | 1.03 (0.84–1.26) |
| 3–4 | 12,289 | 656 | 1.56 (1.41–1.73) | 1.57 (1.35–1.82) | 492 | 1.36 (1.22–1.53) | 1.27 (1.08–1.51) | 211 | 1.36 (1.14–1.61) | 1.10 (0.87–1.41) |
| 5–9 | 5,374 | 280 | 1.55 (1.35–1.77) | 1.49 (1.22–1.81) | 251 | 1.63 (1.41–1.88) | 1.48 (1.20–1.82) | 119 | 1.81 (1.46–2.23) | 1.39 (1.04–1.87) |
| Average weekly time spent outdoors in a swimsuit as a teenager | ||||||||||
| ≥10 | 1,803 | 98 | 1.61 (1.30–2.00) | 1.64 (1.24–2.15) | 92 | 1.78 (1.43–2.23) | 1.72 (1.30–2.29) | 62 | 2.82 (2.14–3.72) | 2.18 (1.53–3.10) |
Note:
Number of participants;
Adjusted for age (continuous), average number of cigarettes per day at age 15–24 (continuous), number of drinks of alcohol at age 15–22 (continuous), average frequencies of strenuous physical activity/sports at least twice per week during high school and ages 18–22 (continuous), hair color (red, blonde, light brown, dark brown and black), family history of melanoma (yes, no), personal history of major chronic diseases (yes, no) and moles on lower legs (none, 1–2, 3–9, 10+).
Table 3 shows the linear regression results on the association. Overall, the significant associations we observed in the logistic regression were also seen in the linear models. Teenagers who spent daily outdoors in a swimsuit (adjusted β, 95% CI for daily vs. <1 per week: 0.25, 0.16–0.34) or who had ≥ 10 sunburns that blistered (adjusted β, 95% CI for ≥ 10 vs. never: 0.45, 0.29–0.62) were more likely to use indoor tanning beds. Also, teenagers/undergraduates who spent ≥ 5 hours per week outdoors in direct sunlight during daytime used indoor tanning more (adjusted β, 95% CI: 0.29, 0.18–0.40) than those who spent < 1 per week.
Table 3.
Age and multivariable-adjusted linear regression for the association of sun-seeking behaviors with average annual frequency of indoor tanning bed usage during high school/college
| Na | Model 1 | Model 2b | |
|---|---|---|---|
| Average weekly time spent outdoors in a swimsuit as a teenager | |||
| <1 | 9,679 | 1.00 | 1.00 |
| 1 | 6,768 | 0.07 (−0.01–0.16) | 0.05 (−0.07–0.17) |
| 2 | 11,488 | 0.13 (0.05–0.20) | 0.03 (−0.08–0.13) |
| Several | 33,194 | 0.50 (0.42–0.57) | 0.32 (0.21–0.43) |
| Daily | 11,491 | 0.32 (0.26–0.38) | 0.25 (0.16–0.34) |
| Average percentage of time of wearing sunscreen at the pool or beach as a teenager | |||
| 100% | 1,022 | 1.00 | 1.00 |
| 75% | 2,838 | −0.002 (−0.20–0.19) | −0.07 (−0.35–0.21) |
| 50% | 6,984 | 0.03 (−0.15–0.21) | −0.02 (−0.28–0.23) |
| 25% | 16,107 | 0.12 (−0.05–0.30) | 0.08 (−0.16–0.33) |
| 0% | 44,307 | 0.13 (−0.04–0.30) | 0.03 (−0.21–0.27) |
| Average weekly hours spent outdoors in direct sunlight in the middle of the day during high school/college | |||
| <1 | 5,825 | 1.00 | 1.00 |
| 2–4 | 26,052 | 0.09 (0.01–0.17) | 0.07 (−0.04–0.18) |
| ≥5 | 48,776 | 0.39 (0.31–0.46) | 0.29 (0.18–0.40) |
| The number of severe sunburns which blistered between ages 15–20 | |||
| Never | 28,180 | 1.00 | 1.00 |
| 1–2 | 31,412 | 0.13 (0.09–0.18) | 0.01 (−0.05–0.08) |
| 3–4 | 13,648 | 0.15 (0.10–0.21) | 0.06 (−0.02–0.15) |
| 5–9 | 6,024 | 0.29 (0.21–0.37) | 0.17 (0.06–0.28) |
| ≥10 | 2,055 | 0.53 (0.41–0.66) | 0.45 (0.29–0.62) |
Note:
Number of participants;
Adjusted for age (continuous), average number of cigarettes per day at age 15–24 (continuous), number of drinks of alcohol at age 15–22 (continuous), average frequencies of strenuous physical activity/sports at least twice per week during high school and ages 18–22 (continuous), hair color (red, blonde, light brown, dark brown and black), family history of melanoma (yes, no), personal history of major chronic diseases (yes, no) and moles on lower legs (none, 1–2, 3–9, 10+).
Discussion
Here we investigated the association between outdoor sun-seeking behaviors and average annual frequency of indoor tanning during early life using the observational data from the NHS II. We found that females who spent more time outdoors in a swimsuit or in direct sunlight in the middle of the day, or experienced more severe sunburns were higher-frequency indoor tanners during their early life.
The significant association between outdoor sun-seeking behaviors and indoor tanning habit should cause concern, because exposure to excessive UV radiation from indoor tanning and spending outdoor in direct natural sunlight can be made (10) and such excessive exposure leads to profound health risks, e.g., atrophy, pigmentary changes, wrinkling, and malignancy (14). Furthermore, It is well-known that such exposure is linked to three most common types of skin cancer, i.e., basal cell carcinoma, squamous cell carcinoma, and malignant melanoma (15), among which melanoma is the leading cause of death in US females aged 25 to 30 and second leading cause of death in females aged 30 to 35 (16). Despite the risks, why the outdoor sun-seeking behaviors and indoor tanning habit were significantly associated can be explained by the known fact that UV radiation can increase the blood flow associated with central reward mechanisms to encourage excessive tanning (17). To be specific, exposure to UV radiation, triggering DNA damage to the skin, activates the p53 protein to induce production of pro-opiomelanocortin (POMC) and its derivative β-endorphin (18). β-endorphin, the most abundant endogenous opioid, acts on central neural dopamine receptors to make the tanner relaxed and increase her sense of well-being (5, 19). Moreover, frequent tanning may chronically elevate tanners’ endorphin levels, creating reinforcing effects (20).
We observed significant associations between the time spent outdoors in a swimsuit or in direct sunlight in daytime as a teenager and indoor tanning bed use during high school/college. Weekly frequency of spending outdoors wearing a swimsuit or in direct sunlight reflect almost the same characteristics of a participant, i.e., an individual’s sun-seeking degree and both in high frequency may come with higher risk for skin cancer because of the increased exposure to UV rays. This can also strengthen stimulation of the reward system and increase the sun-seeking desire more (21). Such increased sun-seeking needs may also lead to increased use of indoor tanning facilities that emits far more intense UV lights than that of natural sunlight, which in turn becomes a series of vicious cycles (17). Thus, education should be provided to teenagers with strong sun-seeking behaviors to prevent them from being long exposed to direct sunlight outside in the middle of the day or to artificial UV lights in indoor equipment. Furthermore, because teenagers’ behavior is more likely to be influenced by others because of the psychological pressure to conform (22, 23), school health stakeholders or parents should make teenagers keep practicing sun safety according to their own will.
Sunburn is an inflammatory reaction to UV radiation damage to skin’s outermost layers (24). Repeated sunburns raise the risk for skin cancer by an altered tumor-suppressing gene that lowers the chance to prevent from progressing to cancer (25). Especially, blistering sunburns that occur in childhood or adolescence pose the greatest risk for cutaneous melanoma in adulthood (26). Five or more sunburns increased the risk of development of melanoma (27). In addition to the severe sunburns, indoor tanning bed use is also an established risk factor for melanoma (28, 29). In our study, we found the strongest positive associations between undergoing ≥ 10 severe sunburns which blistered between ages 15–20 and usage of indoor tanning beds of ≥ 12. Such relationship was also observed in other studies reporting that indoor tanning was positively associated with sunburns because of their tan-seeking behaviors (30, 31). To mitigate the aggravated risk, dermatologists may need to make a consensus on the proper guideline of indoor tanning usage in teenagers with severe sunburns and public health offi cers or school health teachers also need to provide preventive education for protecting teenagers from severe sunburns, such as encouragement of use of sunscreen outdoors.
Sunscreens are an important protection against UV exposure and can effectively reduce the incidence of skin cancers (32). However, our study did not demonstrate the inverse association between the percentage of time of wearing sunscreen at the pool/beach and the use of indoor tanning beds, which is a different result from previous findings (22, 33, 34). A study among US high school students found that white female students who reported always using sunscreen were significantly less likely to use indoor tanning equipment (33). Another study pointed out that non-use of sunscreen at the pool/beach was an independent predictor of indoor tanning use habit (22). Moreover, a study based on US 2015 National Health Interview Survey data also found that those who frequently tanned indoors were more likely to rarely/never use sunscreen (34). It might be due to safety frigidity that frequent users of indoor tanning beds were less likely to wear sunscreen, even though sunscreen use is the one of most important aspects of sun protective behavior. In addition, they might think using sunscreen would prevent the bronzing of their skin especially in the 70s and 80s when there were not bronzing sunscreens. In fact, inconvenience and no perceived need for applying sunscreen are known as the major reasons for not using sunscreen (35). However, the indoor tanning-seeking behavior may be more likely to be due to addictiveness of UV exposure regardless of how they perceive the importance of the use of sunscreen, which may partially explain such no association we observed in our study.
Many countries have recently moved to ban those younger than 18 from using indoor tanning beds (36–38). However, adults who use tanning beds also deserve special attention, especially those under age 25. Our data showed that people who used tanning beds more often during early life tended to be younger, and also had more moles on their lower legs, which was consistent with the results of a previous study (13). As shown in Table 1, heavier smokers as well as drinkers tended to use tanning beds more often. As the reward mechanisms affected by smoking are similar to those associated with indoor tanning bed use (39), those interactions deserve further study. Females who engaged in more strenuous physical activity or sports sought to use indoor tanning beds more, which might be due to needs for relaxing and relieving pain. Persistent indoor tanning is positively associated with both risk taking (40) and unhealthy lifestyle (10) behaviors. Therefore, those results suggest that teenagers with a cluster of such unhealthy behaviors should be paid closer attention by considering them as high-risk groups.
Our study has several strengths, including a relatively large sample size (N = 81,746) compared to the previous studies with similar research topics. In addition, detailed collection of baseline, lifestyle, and medical history using well-designed and validated self-reported questionnaires allowed us to adjust for widely recognized potential confounders in the relationship of interest and to develop valid reference for the association. Moreover, we used the average data of high-quality sun-seeking or indoor tanning-seeking behaviors during high school/college, which may be more valuable than data or records during shorter period in measuring habit of the participants that affected their indoor tanning facilities usage during early life.
Our study also has several limitations. First, the information we collected on study variables may introduce recall bias; however, there was only slim chance that participants would exaggerate or understate their actual habit/values because when they reported, they did not have any pressure to do so in cohort study design. Second, residual and unmeasured confounding cannot be fully ruled out because of the nature of the observational data; but we adjusted many well-known confounding factors. Third, some misclassification is inherent from self-reported questionnaires; yet the questionnaire has been extensively validated in subsamples of this cohort, and any misclassification would likely be some nondifferential error to bias our results toward the null. Lastly, we studied only compliant healthy professional female nurses belonging to a specific social stratum, which may create a lack of external validity; nevertheless, the results could be applied to females with similar sun-seeking behaviors and lifestyles.
In conclusion, our study reveals associations between outdoor sun-seeking behaviors and average annual frequency of indoor tanning bed usage, suggesting that young females who spent more time outdoors and had more severe sunburns tended to use indoor tanning more frequently than those with fewer sun-seeking behaviors. If properly publicized, these findings could change perceptions about indoor tanning bed usage and guide potential interventions among young females with strong outdoor sun-seeking behaviors. This work may contribute vital information for public health messaging about young female skin health and guide potential interventions for control of sun-seeking behaviors and indoor tanning use in high-risk groups.
Key Points.
Question:
How are outdoor sun-seeking behaviors associated with indoor tanning frequency?
Findings:
This large study using data from the Nurses’ Health Study II (NHSII) found that female who spent more time outdoors or got more sunburns tended to use indoor tanning more frequently than those who rarely or never engaged in outdoor sun-seeking behaviors.
Meaning:
The findings reveal the associations between outdoor sun-seeking behaviors and frequency of indoor tanning, which could change perceptions about indoor tanning and guide potential interventions directed at young females with frequent outdoor sun-seeking behaviors.
Acknowledgements:
We gratefully acknowledge the contributions of the Channing Division of Network Medicine for manuscript development. We are indebted to the participants in the NHSII for their dedication to this research. We would like to thank the following state cancer registries for their help: AL, AZ, AR, CA, CO, CT, DE, FL, GA, ID, IL, IN, IA, KY, LA, ME, MD, MA, MI, NE, NH, NJ, NY, NC, ND, OH, OK, OR, PA, RI, SC, TN, TX, VA, WA, WY.
Funding:
The present study was supported by National Institutes of Health (NIH) P01 CA87969, UM1 CA186107 and UM1 CA176726. Dr. Jiali Han is partially supported by the Walther Cancer Foundation. The content is solely the responsibility of the authors and does not necessarily represent the offi cial views of the NIH.
Funding Statement
The present study was supported by National Institutes of Health (NIH) P01 CA87969, UM1 CA186107 and UM1 CA176726. Dr. Jiali Han is partially supported by the Walther Cancer Foundation. The content is solely the responsibility of the authors and does not necessarily represent the offi cial views of the NIH.
Footnotes
Ethics approval and consent to participate: The study protocol was approved by the institutional review boards of the Brigham and Women’s Hospital (study protocol: 1999P003389) and Harvard T.H. Chan School of Public Health (study protocol: 10162) and those of participating registries as required. Written informed consent was also obtained from all study participants. All methods were carried out in accordance with relevant guidelines and regulations
Consent for publication: Informed consent for publication was also obtained from all study participants.
Competing interests: The authors declare no conflicting interests.
Manuscript contribution: The findings reveal the associations between outdoor sun-seeking behaviors and frequency of indoor tanning, which could change perceptions about indoor tanning and guide potential interventions directed at young females with frequent outdoor sun-seeking behaviors.
Contributor Information
Bojung Seo, Indiana University.
Sheng Yang, Indiana University.
Eunyoung Cho, Alpert Medical School of Brown University.
Abrar A Qureshi, Alpert Medical School of Brown University.
Jiali Han, Indiana University.
Availability of data and materials:
The data that support the findings of this study are available from Brigham and Women’s Hospital and Harvard T.H. Chan School of Public Health but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data described in the manuscript, code book, and analytic code are however available from the authors upon reasonable request to corresponding author and with permission of Brigham and Women’s Hospital and Harvard T.H. Chan School of Public Health.
References
- 1.Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–33. [DOI] [PubMed] [Google Scholar]
- 2.El Ghissassi F, Baan R, Straif K, Grosse Y, Secretan B, Bouvard V, et al. A review of human carcinogens–part D: radiation. The Lancet Oncology. 2009;10(8):751–2. [DOI] [PubMed] [Google Scholar]
- 3.Stapleton JL, Hillhouse J, Levonyan-Radloff K, Manne SL. Review of interventions to reduce ultraviolet tanning: Need for treatments targeting excessive tanning, an emerging addictive behavior. Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors. 2017;31(8):962–78. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Fisher DE, James WD. Indoor tanning--science, behavior, and policy. The New England journal of medicine. 2010;363(10):901–3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Feldman SR, Liguori A, Kucenic M, Rapp SR, Fleischer AB Jr., Lang W, et al. Ultraviolet exposure is a reinforcing stimulus in frequent indoor tanners. Journal of the American Academy of Dermatology. 2004;51(1):45–51. [DOI] [PubMed] [Google Scholar]
- 6.Garssen J, Buckley TL, Van Loveren H. A role for neuropeptides in UVB-induced systemic immunosuppression. Photochemistry and photobiology. 1998;68(2):205–10. [PubMed] [Google Scholar]
- 7.Poorsattar SP, Hornung RL. UV light abuse and high-risk tanning behavior among undergraduate college students. Journal of the American Academy of Dermatology. 2007;56(3):375–9. [DOI] [PubMed] [Google Scholar]
- 8.Guy GP Jr., Berkowitz Z, Holman DM, Hartman AM. Recent Changes in the Prevalence of and Factors Associated With Frequency of Indoor Tanning Among US Adults. JAMA dermatology. 2015;151(11):1256–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Green AC, Wallingford SC, McBride P. Childhood exposure to ultraviolet radiation and harmful skin effects: epidemiological evidence. Prog Biophys Mol Biol. 2011;107(3):349–55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Demko CA, Borawski EA, Debanne SM, Cooper KD, Stange KC. Use of indoor tanning facilities by white adolescents in the United States. Arch Pediatr Adolesc Med. 2003;157(9):854–60. [DOI] [PubMed] [Google Scholar]
- 11.Lostritto K, Ferrucci LM, Cartmel B, Leffell DJ, Molinaro AM, Bale AE, et al. Lifetime history of indoor tanning in young people: a retrospective assessment of initiation, persistence, and correlates. BMC Public Health. 2012;12:118. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Bertone-Johnson ER, Hankinson SE, Johnson SR, Manson JE. Timing of alcohol use and the incidence of premenstrual syndrome and probable premenstrual dysphoric disorder. Journal of women’s health. 2009;18(12):1945–53. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Li WQ, Cho E, Han J, Wu S, Qureshi AA. Pigmentary traits and use of indoor tanning beds in a cohort of women. The British journal of dermatology. 2017;176(2):526–30. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.D’Orazio J, Jarrett S, Amaro-Ortiz A, Scott T. UV radiation and the skin. Int J Mol Sci. 2013;14(6):12222–48. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Narayanan DL, Saladi RN, Fox JL. Ultraviolet radiation and skin cancer. Int J Dermatol. 2010;49(9):978–86. [DOI] [PubMed] [Google Scholar]
- 16.Cancer Facts & Figures 2020: American Cancer Society; 2020. [Available from: https://www.cancer.org/research/cancer-facts-statistics/all-cancer-facts-figures/cancer-facts-figures-2020.html. [Google Scholar]
- 17.Harrington CR, Beswick TC, Graves M, Jacobe HT, Harris TS, Kourosh S, et al. Activation of the mesostriatal reward pathway with exposure to ultraviolet radiation (UVR) vs. sham UVR in frequent tanners: a pilot study. Addiction biology. 2012;17(3):680–6. [DOI] [PubMed] [Google Scholar]
- 18.Cui R, Widlund HR, Feige E, Lin JY, Wilensky DL, Igras VE, et al. Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell. 2007;128(5):853–64. [DOI] [PubMed] [Google Scholar]
- 19.Fell GL, Robinson KC, Mao J, Woolf CJ, Fisher DE. Skin beta-endorphin mediates addiction to UV light. Cell. 2014;157(7):1527–34. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Kaur M, Liguori A, Lang W, Rapp SR, Fleischer AB Jr., Feldman SR. Induction of withdrawal-like symptoms in a small randomized, controlled trial of opioid blockade in frequent tanners. Journal of the American Academy of Dermatology. 2006;54(4):709–11. [DOI] [PubMed] [Google Scholar]
- 21.Iacopetta K, Collins-Praino LE, Buisman-Pijlman FTA, Hutchinson MR. Can neuroimmune mechanisms explain the link between ultraviolet light (UV) exposure and addictive behavior? Brain, behavior, and immunity. 2018;73:125–32. [DOI] [PubMed] [Google Scholar]
- 22.Cokkinides VE, Weinstock MA, O’Connell MC, Thun MJ. Use of indoor tanning sunlamps by US youth, ages 11–18 years, and by their parent or guardian caregivers: prevalence and correlates. Pediatrics. 2002;109(6):1124–30. [DOI] [PubMed] [Google Scholar]
- 23.Rodriguez VM, Daniel CL, Welles BF, Geller AC, Hay JL. Friendly tanning: young adults’ engagement with friends around indoor tanning. Journal of behavioral medicine. 2017;40(4):631–40. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Nicolaou A, Pilkington SM, Rhodes LE. Ultraviolet-radiation induced skin inflammation: dissecting the role of bioactive lipids. Chem Phys Lipids. 2011;164(6):535–43. [DOI] [PubMed] [Google Scholar]
- 25.Steinberg ML, Hubbard K, Utti C, Clas B, Hwang BJ, Hill HZ, et al. Patterns of persistent DNA damage associated with sun exposure and the glutathione S-transferase M1 genotype in melanoma patients. Photochem Photobiol. 2009;85(1):379–86. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Dennis LK, Vanbeek MJ, Beane Freeman LE, Smith BJ, Dawson DV, Coughlin JA. Sunburns and risk of cutaneous melanoma: does age matter? A comprehensive meta-analysis. Ann Epidemiol. 2008;18(8):614–27. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Wu S, Han J, Laden F, Qureshi AA. Long-term ultraviolet flux, other potential risk factors, and skin cancer risk: a cohort study. Cancer Epidemiol Biomarkers Prev. 2014;23(6):1080–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Elwood JM, Jopson J. Melanoma and sun exposure: an overview of published studies. International journal of cancer. 1997;73(2):198–203. [DOI] [PubMed] [Google Scholar]
- 29.Veierod MB, Weiderpass E, Thorn M, Hansson J, Lund E, Armstrong B, et al. A prospective study of pigmentation, sun exposure, and risk of cutaneous malignant melanoma in women. Journal of the National Cancer Institute. 2003;95(20):1530–8. [DOI] [PubMed] [Google Scholar]
- 30.Guy GP Jr., Watson M, Seidenberg AB, Hartman AM, Holman DM, Perna F. Trends in indoor tanning and its association with sunburn among US adults. Journal of the American Academy of Dermatology. 2017;76(6):1191–3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Guy GP Jr., Berkowitz Z, Everett Jones S, Watson M, Richardson LC. Prevalence of Indoor Tanning and Association With Sunburn Among Youth in the United States. JAMA dermatology. 2017;153(5):387–90. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Lautenschlager S, Wulf HC, Pittelkow MR. Photoprotection. Lancet. 2007;370(9586):528–37. [DOI] [PubMed] [Google Scholar]
- 33.Sheng Y, Einstadter D, Bordeaux J. Association Between Sunscreen Use and Indoor Tanning Use Among American High School Students. Dermatologic surgery : official publication for American Society for Dermatologic Surgery [et al]. 2018;44(6):897–9. [DOI] [PubMed] [Google Scholar]
- 34.Fischer AH, Wang TS, Yenokyan G, Kang S, Chien AL. Association of Indoor Tanning Frequency With Risky Sun Protection Practices and Skin Cancer Screening. JAMA dermatology. 2017;153(2):168–74. [DOI] [PubMed] [Google Scholar]
- 35.Diehl K, Schneider S, Seuffert S, Greinert R, Gorig T. Who Are the Nonusers of Sunscreen, and What Are Their Reasons? Development of a New Item Set. J Cancer Educ. 2021;36(5):1045–53. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Lim HW, James WD, Rigel DS, Maloney ME, Spencer JM, Bhushan R. Adverse effects of ultraviolet radiation from the use of indoor tanning equipment: time to ban the tan. Journal of the American Academy of Dermatology. 2011;64(5):893–902. [DOI] [PubMed] [Google Scholar]
- 37.Taddeo D, Stanwick R, Canadian Paediatric Society AHC. Banning children and youth younger than 18 years of age from commercial tanning facilities. Paediatrics & child health. 2012;17(2):89–90. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Balk SJ, Council on Environmental H, Section on D. Ultraviolet radiation: a hazard to children and adolescents. Pediatrics. 2011;127(3):e791–817. [DOI] [PubMed] [Google Scholar]
- 39.McClernon FJ, Addicott MA, Sweitzer MM. Smoking abstinence and neurocognition: implications for cessation and relapse. Current topics in behavioral neurosciences. 2015;23:193–227. [DOI] [PubMed] [Google Scholar]
- 40.Bagdasarov Z, Banerjee S, Greene K, Campo S. Indoor tanning and problem behavior. Journal of American college health : J of ACH. 2008;56(5):555–61. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from Brigham and Women’s Hospital and Harvard T.H. Chan School of Public Health but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data described in the manuscript, code book, and analytic code are however available from the authors upon reasonable request to corresponding author and with permission of Brigham and Women’s Hospital and Harvard T.H. Chan School of Public Health.