Abstract
Background
Increased risk of skin cancer by indoor tanning has drawn public attention. However, there are arguments that tanning bed use increases vitamin D production, which may therefore prevent internal cancers.
Methods
We follow 73,358 female nurses for 20 years (1989–2009) in the Nurses’ Health Study II and investigated the frequency of tanning bed use during high school/college and at ages 25–35 in relation to the incidence of total cancers (excluding skin cancers). We used multivariate Cox proportional hazards models to estimate the hazard ratios (HRs) and 95% confidence intervals (CIs) of total cancers and each individual major cancer with more than 100 cases.
Results
During follow-up, a total of 4,271 internal cancer cases were diagnosed. No association was found between tanning bed use and risk of total cancers (multivariable-adjusted HR, 0.99; 95% CI, 0.95–1.04 for every 4 times/year use on average during high school/college and at ages 25–35). In addition, no association was found for the risk of any individual major cancers, such as breast cancer, thyroid cancer, colorectal cancer, non-Hodgkin lymphoma, or endometrial cancer.
Conclusion
Our data do not suggest any association between the use of tanning beds and risk of internal cancers.
Impact
Based on the strong evidence of increase in skin cancer risk and no evidence of reduction in internal cancer risk by tanning bed use, it is important to warn the public against indoor tanning.
Keywords: Indoor tanning, Internal cancer, Vitamin D, Cohort study
Introduction
We previously reported that use of tanning beds increased the risk of all three types of skin cancers (basal cell carcinoma, BCC; squamous cell carcinoma, SCC; and melanoma) by following up 73,494 female nurses for 20 years in the Nurses’ Health Study II (NHSII) (1). Our findings were further confirmed by two recent meta-analyses for both melanoma and non-melanoma skin cancers (2, 3). However, there are arguments that use of tanning beds may be a good source of vitamin D, which has potential health benefits (4). Here we report our investigation on tanning bed use in relation to the incidence of total internal cancers as well as individual major cancers in the same cohort. We carefully adjusted for outdoor sun exposure, UV index of residence, and dietary and supplemental vitamin D intake in addition to the known risk factors for cancers.
Materials and Methods
Study population
Our study population consisted of participants in the NHSII, a prospective cohort study established in 1989 and enrolled 116,678 female registered nurses aged 25–42 and residing in the United States. Details of this cohort have been described previously (5). The protocol for this study was approved by the Institutional Review Board at Brigham and Women’s Hospital and the Harvard School of Public Health.
In the 2005 questionnaire, we collected information on the frequency of tanning bed usage during high school/college and at ages 25–35 (none, 1–2 times/year, 3–5 times/year, 6–11 times/year, 12–23 times/year, and 24+ times/year). We obtained information regarding outdoor ultraviolet exposure, dietary and supplemental vitamin D intake and other risk factors for cancer from the follow-up questionnaires. More details were described in our previous publications (6).
Eligible cases consisted of women with incident cancers diagnosed any time after the baseline up to the 2009 follow-up cycle. Only pathologically confirmed invasive cancer cases were included, except for breast cancer, which included both invasive and in situ cases.
Statistical Analysis
All participants in this analysis were US non-Hispanic Caucasians. We also excluded the participants with missing information on tanning bed use or with self-reported cancers at baseline. We grouped women into four categories based on their self-reported frequency of tanning bed usage (none, 1–2 times/year, 3–5 times/year, and ≥6 times/year) and created a continuous variable for linear trend test using the median value of each category. Participants contributed person-time data from the baseline in June 1989 to the first report (followed by confirmation) of a primary cancer, death, or the end of follow-up, whichever came earlier. We used age-adjusted and multivariate Cox proportional hazards models to calculate the hazard ratios (HRs) and 95% confidence intervals (CIs) of total cancer and each type of major cancer with more than 100 cases. All of the statistical analyses were carried out using Statistical Analysis System software (version 9.1.3; SAS Institute, Cary, NC). All p-values were two-sided.
Results
During 20-year follow-up of 73,358 female nurses from 1989 to 2009, a total of 4,271 cancer cases (excluding skin cancers) were diagnosed. The first primary cancers for which at least 100 cases were diagnosed were breast cancer (n=2,779), thyroid cancer (n=306), colorectal cancer (n=186), non-Hodgkin lymphoma (n=185), and endometrial cancer (n=100). In Table 1, we present the basic characteristics of participants according to the frequencies of tanning bed usage based on information collected in baseline questionnaire in 1989. People who used tanning beds more often either during high school/college or from ages 25–35 were more likely to be current smokers and oral contraceptive users. No substantial difference was found for other cancer risk factors across the different categories.
Table 1.
Characteristics 1 | Tanning bed use during high school/college
|
Tanning bed use at ages 25–35
|
||||||
---|---|---|---|---|---|---|---|---|
none | 1–2 times/year | 3–5 times/year | >6 times/year | none | 1–2 times/year | 3–5 times/year | >6 times/year | |
Mean age at baseline (years) | 34.8 | 32.8 | 32.3 | 31.6 | 35.0 | 33.2 | 32.7 | 32.2 |
Height, m (SD) | 1.6 (0.1) | 1.7 (0.1) | 1.7 (0.1) | 1.7 (0.1) | 1.6 (0.1) | 1.7 (0.1) | 1.7 (0.1) | 1.7 (0.1) |
Body mass index, kg/m (SD) | 24.0 (5.0) | 23.5 (4.7) | 23.4 (4.4) | 23.4 (4.4) | 24.0 (5.0) | 23.3 (4.3) | 23.6 (4.5) | 23.6 (4.7) |
Body mass index at age 18, kg/m (SD) | 21.3 (3.3) | 21.0 (3.1) | 20.9 (2.8) | 20.9 (3.3) | 21.3 (3.2) | 21.0 (3.1) | 21.2 (3.3) | 21.2 (3.4) |
Alcohol consumption at 1991, gm/day (SD) | 3.2 (6.1) | 3.9 (7.6) | 4.2 (6.7) | 3.5 (5.8) | 3.0 (6.0) | 4.0 (6.7) | 3.9 (6.3) | 4.0 (7.1) |
Physical activity, met-h/week (SD) | 27.2 (66.6) | 27.9 (65.1) | 36.5 (92.7) | 29.8 (52.1) | 26.5 (65.0) | 30.4 (70.2) | 34.4 (81.6) | 32.0 (68.5) |
Multi-vitamin use, % | 45.8 | 49.1 | 49.3 | 48.8 | 46.1 | 47.8 | 47.8 | 44.9 |
Current smoker, % | 11.8 | 13.7 | 13.6 | 14.6 | 11.0 | 14.0 | 15.5 | 18.8 |
Current oral contraceptive use, % | 12.1 | 13.5 | 14.7 | 15.6 | 11.3 | 14.2 | 16.0 | 16.9 |
Postmenopausal women, % | 5.8 | 5.9 | 4.2 | 6.3 | 5.3 | 7.4 | 7.8 | 9.6 |
History of benign breast disease, % | 29.1 | 31.7 | 33.0 | 31.7 | 29.0 | 29.6 | 32.2 | 31.5 |
Family history of breast cancer, % | 5.9 | 6.6 | 7.6 | 6.2 | 6.0 | 5.6 | 6.0 | 5.8 |
Age at menarche, years | 13.4 (1.4) | 13.5 (1.4) | 13.5 (1.4) | 13.4 (1.5) | 13.4 (1.4) | 13.4 (1.5) | 13.5 (1.4) | 13.4 (1.5) |
Age at first birth, years (SD) | 25.6 (3.9) | 25.8 (4.4) | 25.9 (4.4) | 25.4 (4.7) | 25.7 (3.9) | 24.9 (4.2) | 24.6 (4.4) | 24.1 (4.3) |
Parity among parous women, times | 1.5 (1.2) | 1.3 (1.2) | 1.3 (1.2) | 1.3 (1.2) | 1.5 (1.2) | 1.3 (1.2) | 1.3 (1.2) | 1.3 (1.1) |
Vitamin D intake at 1991, IU/d (SD) | 380.2 (249.6) | 387.0 (256.2) | 389.5 (258.3) | 387.5 (259.3) | 384.5 (249.8) | 376.2 (260.1) | 379.4 (254.1) | 357.8 (261.2) |
Outdoor sun exposure, 5+ hours/week (%) | ||||||||
At high school/college | 60 | 64.2 | 72.3 | 75.5 | 59.6 | 62.6 | 65.1 | 71 |
At ages 25–35 | 50.2 | 52.9 | 59.2 | 60.2 | 48.7 | 54.3 | 57.5 | 66.4 |
UV index in the state of residence, 7+ (%) | ||||||||
At birth | 18.5 | 19.9 | 20 | 22.1 | 18.2 | 20 | 20.5 | 23.8 |
At age 15 | 18.8 | 19.3 | 18.7 | 21.1 | 18.5 | 20.1 | 20.6 | 24.1 |
At age 30 | 25.1 | 26 | 24.3 | 27.2 | 25.1 | 24.8 | 25.2 | 27.3 |
Based on information collected in baseline questionnaire in 1989 unless otherwise specified.
As a result, no association was found between tanning bed use and total cancer risk (Table 2). Both age- and multivariable-adjusted HRs were 0.99 (95% CIs, 0.95–1.04) for an average of every 4 times/year use during high school/college and at ages 25–35. Separately for the use during high school/college and at ages 25–35, no association was found for the use during either period of time (multivariable-adjusted HR, 1.02; 95% CI, 0.97–1.07 for an average of 4 times/year use during high school/college; and multivariable-adjusted HR, 0.99; 95% CI, 0.96–1.02 for an average of 4 times/year use at ages 25–35). In addition, none of the individual major cancers (with at least 100 cases) was associated with tanning bed use in our cohort (Table 2).
Table 2.
Cancers | Cases (717,310 Person-years) | Average use of tanning beds (4 times/year) 1 | Use of tanning beds during high school/college (4 times/year) | Use of tanning beds at ages 25–35 (4 times/year) | |||
---|---|---|---|---|---|---|---|
| |||||||
Age-adjusted HR | Multivariable-adjusted HR2 | Age-adjusted HR | Multivariable-adjusted HR2 | Age-adjusted HR | Multivariable-adjusted HR2 | ||
Total cancer | 4,271 | 0.99 (0.95–1.04) | 0.99 (0.95–1.04) | 1.02 (0.97–1.07) | 1.02 (0.97–1.07) | 0.99 (0.96–1.02) | 0.99 (0.96–1.02) |
Breast cancer | 2,779 | 1.00 (0.94–1.06) | 0.99 (0.94–1.06) 3 | 1.04 (0.99–1.10) | 1.03 (0.98–1.09) 3 | 0.98 (0.94–1.02) | 0.98 (0.94–1.02) 3 |
Thyroid cancer | 306 | 0.95 (0.80–1.13) | 0.97 (0.81–1.16) | 1.01 (0.85–1.19) | 1.01 (0.86–1.20) | 0.95 (0.84–1.07) | 0.97 (0.86–1.09) |
Colorectal cancer | 186 | 1.06 (0.86–1.30) | 1.07 (0.86–1.31) | 0.87 (0.63–1.20) | 0.87 (0.63–1.20) | 1.05 (0.92–1.20) | 1.06 (0.92–1.21) |
Non-Hodgkin lymphoma | 185 | 1.10 (0.90–1.34) | 1.10 (0.90–1.34) | 1.09 (0.89–1.33) | 1.09 (0.89–1.33) | 1.05 (0.92–1.21) | 1.05 (0.91–1.20) |
Endometrial cancer | 100 | 0.80 (0.50–1.27) | 0.82 (0.52–1.30) 4 | 0.93 (0.60–1.43) | 0.97 (0.64–1.50) 4 | 0.86 (0.63–1.16) | 0.89 (0.66–1.19) 4 |
Other Cancers | 715 | 0.97 (0.87–1.09) | 0.95 (0.85–1.07) | 0.93 (0.82–1.06) | 0.92 (0.81–1.05) | 1.01 (0.94–1.08) | 0.99 (0.92–1.06) |
Average number of tanning bed uses during high school/college and at ages 25–35;
Adjusted for age, body mass index (BMI, <25, 25–29, 30–34, 35+ kg/m2), alcohol consumption (none, 1–4, 5–9, 10–14, 15+ gm/week), physical activity (<3, 3–8, 9–17, 18–26, 27+ met-h/week), multi-vitamin use (yes, no), smoking status (never, past smoker, current smoker), oral contraceptive use (never, past use, current use), menopausal status and use of hormone replacement therapy (pre-menopause, post-menopause without hormone replacement therapy, post-menopause with hormone replacement therapy), outdoor sun exposure during high school/college and at ages 25–35, UV index of residence (at birth, age 15, and age 30), as well as dietary and supplemental vitamin D intake;
Additionally adjusted for the history of benign breast disease (yes, no), family history of breast cancer (yes, no), parity and age at first birth (nulliparous, age at first birth<25 and parity 1–2, age at first birth 25–29 and parity 1–2, age at first birth 30+ and parity 1–2, age at first birth<25 and parity 3+, age at first birth 25+ and parity 3+), age at menarche (<12, 12, 13, 14+), height (<1.60, 1.60–1.64, 1.65–1.70, 1.70+ m) and BMI at age 18 (<20, 20–22.4, 22.5–24, 25+ kg/m2);
Additionally adjusted for parity and age at first birth (nulliparous, age at first birth<25 and parity 1–2, age at first birth 25–29 and parity 1–2, age at first birth 30+ and parity 1–2, age at first birth<25 and parity 3+, age at first birth 25+ and parity 3+), and age at menarche (<12, 12, 13, 14+).
We further conducted a secondary analysis restricted to incident cancer cases diagnosed after their report of tanning bed usage in 2005 (n=1,315). The results were very similar to those of our primary analysis using overall cases (multivariable-adjusted HR for total cancers, 0.94; 95% CI, 0.86–1.03 for an average of 4 times/year use during high school and at ages 25–35). No substantial difference was found for the risks of individual major cancers, nor did we find any significant association between dietary and supplemental vitamin D intake and cancer risk in the multivariable models (data not shown).
Discussion
In this large, well-characterized cohort study, we found no inverse association between tanning bed use and the risk of internal cancer after following 73,358 female nurses for 20 years. Our finding provided epidemiological evidence to dispute against the claims by the indoor tanning industry that tanning bed use may has potential health benefits on cancer prevention by promoting vitamin D production. Of note, we have previously reported significantly increased risk of skin cancers with a dose-response relationship for the use of tanning beds in the same cohort (1), which further suggested an overall harmful effect of tanning bed use.
One limitation of our study is that we collected information on tanning bed usage in the 2005 questionnaire cycle, which may introduce survival bias. To address this issue, we have conducted a secondary analysis restricted to the incident cancer cases diagnosed after report of tanning bed usage in the 2005 questionnaire cycle; the results were very similar to those of our primary analysis using overall cases (multivariable-adjusted HR, 0.94; 95% CI, 0.86–1.03 vs. multivariable-adjusted HR, 0.99; 95% CIs, 0.95–1.04 for every 4 times/year use).
In conclusion, our data do not suggest any association between the use of tanning beds and internal cancer risk. Based on the strong evidence of increase in risk of skin cancers (including melanoma) and no evidence of reduction in risk of internal cancers, it is important to warn the public against indoor tanning and increase regulations on the tanning industry.
Acknowledgments
Funding sources: The NHSII cohort is supported by NIH grant CA176726.
We thank Dr. Walter Willett for his insightful comments and Ms. Tricia Li for her statistical and programming support. We thank the participants in the Nurses’ Health Study II for their dedication and commitment. In addition, we would like to thank the participants and staff of the Nurses’ Health Study II for their valuable contributions as well as 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.
Footnotes
Conflict of interest
The authors declare that there are no conflicts of interest.
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