Final Evidence Summary
Skin Cancer: Counseling, 2012
May 15, 2012
Recommendations made by the USPSTF are independent of the U.S. government. They should not be construed as an official position of the Agency for Healthcare Research and Quality or the U.S. Department of Health and Human Services.
A Review of the Evidence for the U.S. Preventive Services Task Force
Release Date: February 2011
By Jennifer S. Lin, MD, MCR; Michelle Eder, PhD; and Sheila Weinmann, PhD, MPH
The information in this article is intended to help clinicians, employers, policymakers, and others make informed decisions about the provision of health care services. This article is intended as a reference and not as a substitute for clinical judgment.
This article may be used, in whole or in part, as the basis for the development of clinical practice guidelines and other quality enhancement tools, or as a basis for reimbursement and coverage policies. AHRQ or U.S. Department of Health and Human Services endorsement of such derivative products may not be stated or implied.
This article was first published in Annals of Internal Medicine on February 1, 2011 (Ann Intern Med 2011;154:190-201; http://www.annals.org).
Background: More than 2 million cases of skin cancer are diagnosed annually in the United States, and melanoma incidence is increasing.
Purpose: To assist the U.S. Preventive Services Task Force in updating its 2003 recommendation on behavioral counseling to prevent skin cancer.
Data Sources: Existing systematic reviews, database searches through February 2010, and outside experts.
Study Selection: English-language, primary care-relevant counseling trials to promote sun-protective behaviors and studies examining the association between sun-protective behaviors and skin cancer outcomes or potential adverse effects were included.
Data Extraction: Each study was appraised by using design-specific quality criteria. Important study details were abstracted into evidence tables.
Data Synthesis: 11 fair- or good-quality, randomized, controlled trials examined the counseling interventions' effect on sun-protective behaviors. In young women, appearance-focused behavioral interventions decrease indoor tanning and ultraviolet exposure. In young adolescents, computer support can decrease midday sun exposure and increase sunscreen use. Thirty-five mainly fair-quality observational studies examined the relationship between ultraviolet exposure or sunscreen use and skin cancer. Increasing intermittent sun exposure in childhood is associated with an increased risk for squamous cell carcinoma, basal cell carcinoma, and melanoma. Evidence suggests that regular or early use of indoor tanning may increase melanoma risk. On the basis of 1 fair-quality trial, regular sunscreen use can prevent squamous cell carcinoma, but it is yet unclear if it can prevent basal cell carcinoma or melanoma.
Limitations: There are limited rigorous counseling trials. Observational studies are limited by the complexity of measuring ultraviolet exposure and sunscreen use, and inadequate adjustment for important confounders.
Conclusion: Randomized, controlled trials suggest that primary care-relevant counseling can increase sun-protective behaviors and decrease indoor tanning.
Primary Funding Source: Agency for Healthcare Research and Quality.
In the United States, more than 2 million cases of nonmelanoma skin cancer are diagnosed each year. Of these cases, about two thirds are basal cell carcinoma and one quarter are squamous cell carcinoma1. Although melanoma is considerably less common than basal cell or squamous cell carcinoma, it now accounts for about 75% of skin cancer deaths1. Age-adjusted incidence rates for melanoma among white Americans have increased from approximately 8.7 per 100,000 in 1975 to 25.3 per 100,000 in 20072. Several factors may contribute to this increase in incidence, including increased ultraviolet exposure, increased public awareness of the warning signs of melanoma, and increased screening by clinicians3-5.
Skin cancer has well-known host and environmental risk factors. Several phenotypic characteristics are associated with skin cancer risk, including hair and eye color, freckles, and tendency to sunburn6,7. Exposure to solar ultraviolet radiation is the most important environmental risk factor for all types of skin cancer8. Therefore, the primary strategies for preventing skin cancer include limiting ultraviolet exposure by avoiding midday sun, wearing protective clothing and broad-brimmed hats, applying sunscreen, and avoiding indoor tanning7. However, sun-protective counseling in primary care varies in frequency and content9-11, despite data suggesting that these behaviors need to be improved12. Among adolescents in the United States, for example, about 83% reported at least 1 sunburn during the previous summer, only 34% reported sunscreen use, and nearly 10% of adolescents and 20% of young adults reported indoor tanning during the previous year13,14.
In 2003, the U.S. Preventive Services Task Force (USPSTF) concluded that evidence was insufficient to recommend for or against routine counseling by primary care clinicians to prevent skin cancer because of the uncertainty surrounding whether clinician counseling is effective in changing patient behaviors to reduce skin cancer, the uncertainty about potential harms of sun-protective behaviors, and availability of only fair-quality evidence linking sunscreen use or indoor tanning to skin cancer outcomes15. Therefore, using the USPSTF methods16, we developed an analytic framework with 5 key questions focusing on the evidence gaps identified in 2003 (Appendix Figure 1).
Key question 1: Is there direct evidence that counseling patients on sun-protective behaviors reduces sunburns, nevi, actinic keratoses, or skin cancer?
Key question 2: Do primary care-relevant counseling interventions change sun-protective behaviors?
Key question 3: Do primary care-relevant counseling interventions have adverse effects?
Key question 4: Are certain behaviors (for example, changes in sun exposure, indoor tanning, or sunscreen use) associated with skin cancer outcomes?
Key question 5: Are sun-protective behaviors associated with adverse effects?
Data Sources and Searches
We initially searched for existing systematic reviews from 2001 to March 2008 and evaluated 15 relevant systematic reviews, in addition to the previous evidence report, for quality and their potential in answering questions or identifying primary research for each question15,17-31. We used 10 reviews to identify primary evidence and subsequently searched from the end dates of existing systematic reviews through February 2010 (Table 1)15,17,18,21,23,32-36. Details of the existing systematic reviews search are included in the full report37. We identified 6132 abstracts through MEDLINE and the Cochrane Central Register of Controlled Trials and 165 articles from outside experts and reviewing bibliographies of other relevant articles and existing systematic reviews (Appendix Figure 2).
We reviewed all abstracts and articles for potential inclusion on the basis of a priori-determined inclusion criteria (Appendix Table 1). For key questions 1 to 3, we included randomized or controlled clinical trials evaluating behavioral interventions that were conducted in primary care settings, judged to be feasible for delivery in primary care (for example, mailed or electronic interventions) or widely available for referral from primary care. Outcomes for key question 2 included self-reported or directly observed measures of sun-protective behaviors (for example, limitation or avoidance of midday sun, use of sun-protective clothing, use of sunscreen, or limitation or avoidance of indoor tanning) at 3 months of follow-up or longer. For key questions 4 and 5, we included trials, cohort studies, and population-based case-control studies. We excluded cross-sectional studies that were ecological analyses and hospital-based case-control studies because hospital-based control participants are not generally representative of the community, and hospital-based cases can introduce considerable selection bias38,39. Outcomes for key question 5 included potentially clinically important harms (for example, paradoxical increase in sun exposure, reduced physical activity, dysphoric mood, vitamin D deficiency, and increased incidence of nonskin cancer).
Two investigators independently screened 6132 abstracts, 73 articles for key questions 1 to 3, and 309 articles for key questions 4 and 5.
Data Abstraction and Quality Assessment
Two investigators independently assessed study quality using the USPSTF's study design-specific quality criteria and the Newcastle-Ottawa Scale for assessing cohort and case-control studies16,40. All poor-quality studies were excluded. Listings of all excluded articles are included in the full evidence report37.
We found no trials for key question 1, 13 articles (11 unique trials) for key questions 2 and 3, 60 articles (35 unique studies) for key question 4, and 19 articles (17 unique studies) for key question 5. One primary reviewer abstracted relevant information into standardized evidence tables for each included article. A second reviewer checked the abstracted data for accuracy and completeness.
Data Synthesis and Analysis
We were unable to conduct quantitative synthesis primarily because of the heterogeneity of the populations addressed and counseling intervention methods and measurement of exposures and outcomes. Instead, we qualitatively synthesized our results, stratified by population counseled (adults, young adults with a mean age of 18 to 21 years, and children) or type of exposure.
Role of the Funding Source
The Agency for Healthcare Research and Quality funded this research under a contract to support the USPSTF, provided project oversight, reviewed the draft evidence synthesis, and assisted in external review of the draft evidence synthesis. The Agency for Healthcare Research and Quality had no role in the study selection, quality assessment, or evidence synthesis.
Key Questions 1 and 2: Effectiveness of Counseling to Promote Sun-Protective Behaviors
We found no trials meeting our inclusion criteria that directly examined whether behavioral counseling interventions can reduce skin cancer. We included 11 fair-quality, randomized, controlled trials (RCTs) examining counseling interventions that included sun-protective behavior outcomes (Table 2). Quality considerations for these trials are summarized in Table 2.
In adults, 1 trial was conducted in the United Kingdom41 and 4 trials were conducted in the United States42-45. All of the trials used tailored risk feedback to promote sun-protective behaviors. Three of the counseling interventions conducted in the United States were coupled with in-office computer support on the basis of the transtheoretical model to generate printed stage-based tailored feedback43-45. The trial conducted in the United Kingdom used a self-directed computer station in primary care practice to deliver the counseling intervention41. Populations studied included predominantly middle-aged white men and women. Interventions ranged from a single 15-minute self-directed session to several sessions with in-person counseling, phone counseling, or written assessments followed by tailored written feedback. Overall, 4 of 5 trials (6949 participants) showed that primary care-relevant counseling with tailored feedback (with or without computer support) can modestly affect self-reported sun-protective behaviors, as measured by composite behavior scores (Table 2)42-44. The differences in these scores, although statistically significant, were small, and it is unclear whether these differences translate into clinically meaningful behavior change. In the 1 trial (724 participants) that also reported individual types of behavior change, only the change in use of sunglasses was statistically significant (Table 2)42. One trial conducted among siblings of patients with melanoma, which evaluated a similar counseling intervention, did not show any statistically significant changes in sun-protective behaviors (Table 2)45. This trial, however, used different outcome measures than the other trials and had only 64% follow-up at 12 months.
Four trials in young adults were conducted in university settings and used "appearance-based" behavioral interventions that emphasized the effects of photoaging effects of ultraviolet exposure and norms about tanning and appearing tan instead of a primarily "health-based" message about skin cancer prevention46-49. Interventions ranged from a written self-guided booklet to a brief video and to a 30-minute 1:1 peer-counseling session. In 3 trials (897 participants), the appearance-focused counseling intervention successfully reduced indoor tanning among women who had the intention to tan indoors (Table 2)46,48,49. Although the interventions decreased indoor tanning behavior by up to 35%46, follow-up for these trials was only 3 to 6 months. In another RCT (133 participants), a brief video intervention with or without an ultraviolet facial photograph produced a moderate decrease in objectively measured skin pigmentation (using skin reflectance spectrophotometry) at 12 months (Table 2)47. The change in pigmentation was judged "moderate" on the basis of the Cohen d statistic.
In children, we found only 2 trials50,51. Participants in both trials were predominantly white. In 1 trial (819 participants), young adolescents randomly assigned to brief counseling by their primary care providers, coupled with in-office computer support to generate printed tailored feedback, reported both higher composite sun-protection scores and a greater likelihood of avoiding or limiting midday sun exposure or using sunscreen on the face or sun-exposed areas at 24 months than the attention control group (Table 2). The other cluster RCT, conducted in a large managed care organization, integrated counseling into 4 sequential well-child visits at the discretion of the primary care provider51. Parents of newborns (728 participants) in practices randomly assigned to receive the intervention reported higher composite sun-protection scores at 36-month follow-up than those in control practices (Table 2). The clinical significance of these higher scores, however, is unclear, given the very small numerical differences and the lack of statistically significant differences in 6 of 7 sun-protection questions that contribute to the composite score.
Key Question 4: Association Between Sun Exposure, Sunscreen Use, and Indoor Tanning and Skin Cancer
Sixty articles representing 35 unique fair- or good-quality studies evaluated the epidemiologic association between sun exposure, indoor tanning, or sunscreen use and skin cancer (Table 3 and Appendix Table 2). We found only 1 good-quality trial, the Nambour Skin Cancer and Actinic Eye Disease Prevention Trial (The Nambour Trial)53,85,87-89; 6 fair- or good-quality cohort studies52,54-56,64,86; and 28 fair- or good-quality, population-based, case-control studies31,57-63,65-84, 3 of which were nested case-control studies57,73,75. Odds ratios (ORs) and risk ratios provide a general estimate of the magnitude of the association between the highest- and lowest-risk groups. The ORs and risk ratios, however, should not be compared between studies because the studies used very different measures of exposures and choice of reference groups. Although measures of sun exposure varied greatly among studies, they can be generally categorized as intermittent, which includes measures of recreational sun exposure; chronic, which includes occupational measures of sun exposure; or total, which are cumulative estimates of sun exposure. This section for key question 4 includes a higher-level synthesis of results (Table 3) and a summary of the major limitations of these results; interested readers may refer to Appendix Table 2 for individual study details with outcome data.
On the basis of 5 fair- or good-quality cohort studies and 7 fair- or good-quality case-control studies, increasing intermittent sun exposure in childhood and during one's lifetime is associated with an increased risk for both squamous cell carcinoma and basal cell carcinoma (range of ORs, 1.27 to 3.86) (Appendix Table 2)52-63. The evidence is more consistent for intermittent sun exposure in childhood leading to an increased risk for squamous cell carcinoma and basal cell carcinoma than in adulthood52,58,60,62. Although few studies examined the association between total (or cumulative) and chronic (or occupational) sun exposure, most existing studies did not suggest a strong association between total or chronic sun exposure and squamous cell carcinoma or basal cell carcinoma (Appendix Table 2)53,54,58,59,61,62.
On the basis of 1 fair-quality cohort study and 13 fair-quality case-control studies, it seems that increasing intermittent sun exposure is generally associated with an increased risk for melanoma (Appendix Table 2). A large, fair-quality cohort study from Norway and Sweden showed a statistically significant trend between frequency of sunbathing vacations (childhood and adulthood) and the risk for melanoma64. Of the 8 case-control studies that examined lifetime recreational sun exposure31,57,65,66,69,70,72,76, 5 studies showed that increasing total recreational sun exposure was associated with melanoma risk (range of ORs, 1.3 to 5.0)57,65,66,69,70. Three of 4 case-control studies that examined recreational sun exposure during childhood suggest that increasing sun-bathing behavior in childhood is associated with an increased risk for melanoma (range of ORs, 1.7 to 3.5)70,71,73,75. On the basis of fair-quality case-control studies, it seems that both total and chronic sun exposure are not as strongly associated with melanoma. Six case-control studies included some measure of total sun exposure, either during childhood, during the recent past, or over the lifetime (Appendix Table 2)65,67,69,79-81. These studies showed mixed results: two studies found a statistically significant association between total lifetime sun exposure and melanoma65,81 and 4 did not67,69,79,80. All 3 studies that examined total sun exposure during childhood, however, showed a statistically significant association between increasing sun exposure and melanoma (range of ORs, 1.81 to 4.4)67,79,81. Nine case-control studies included some measure of chronic or occupational sun exposure (Appendix Table 2)65,66,68,69,71,77-80. Three of these studies suggest that occupational sun exposure is associated with an increased risk for melanoma. These studies, however, used crude measures of occupational sun exposure66,77,78, and 1 study showed an increased risk only with the highest level of occupational exposure (>20 years' exposure)78. In contrast, 5 of the remaining 6 studies suggest that occupational sun exposure is inversely associated with melanoma risk65,68,69,79,80.
Five fair-quality case-control studies examined the association between indoor tanning and the risk for squamous cell carcinoma or basal cell carcinoma (Appendix Table 2)57,59,61,62,82. Four of 5 studies used only a crude dichotomous measure of indoor tanning, and none of these studies found a statistically significant association between ever and never use57,59,61,62. Three studies adjusted for both skin phenotype and sun exposure57,61,62. One fair-quality case-control study that was larger and had a slightly higher proportion of exposed persons showed a statistically significant association between indoor tanning and risk for squamous cell carcinoma and basal cell carcinoma, with greater risk for persons who reported early first use (before age 20 years). This study, however, did not adjust for sun exposure82.
We found 1 fair-quality cohort study and 11 fair-quality case-control studies that examined the association between indoor tanning and melanoma (Appendix Table 2)31,57,64,66,68,72-74,76,83,84,90. Most studies used crude measures of indoor tanning exposure. The Norwegian-Swedish Women's Lifestyle and Health Cohort Study found that women who reported regular solarium use (≥1 time per month over 2 or 3 decades) from age 10 to 39 years had an increased risk for melanoma (risk ratio, 2.37 [95% CI, 1.37 to 4.08]) after adjustment for important confounders, including skin phenotype and intermittent sun exposure64. Six of 11 case-control studies did not find a statistically significant association between ever or never use of indoor tanning and melanoma (Appendix Table 2)66,68,72,73,84,90. Only 1 of 6 negative studies adjusted for both skin phenotype and some measure of sun exposure90. Of the 4 studies that found a statistically significant association between indoor tanning exposure and melanoma, 2 adjusted for both skin phenotype and some measure of sun exposure57,76 and 1 adjusted only for skin phenotype74. These studies suggest that regular or higher frequency of indoor tanning or use at a younger age may increase risk for melanoma. Only 1 study examined sun lamp (older technology) and tanning bed (newer technology) exposure separately. Although only frequent sun lamp use was associated with increased melanoma risk, study investigators caution that sufficient lag time may not have elapsed to assess a potential effect, given the more recent use of tanning beds83.
We found 1 RCT (1621 participants) examining whether regular sunscreen use can prevent squamous cell carcinoma or basal cell carcinoma85,87,88. After 8 years of follow-up, persons randomly assigned to regular sunscreen use had a decreased risk for squamous cell carcinoma (risk ratio, 0.65 [CI, 0.45 to 0.94]) but not basal cell carcinoma (risk ratio, 1.02 [CI 0.78 to 1.35]). Two fair-quality cohort studies from the Nurses' Health Study did not show a decrease in squamous cell carcinoma or basal cell carcinoma risk with sunscreen use after adjusting for skin phenotype and sun exposure (Appendix Table 2)55,56. Both of these studies, however, used only a crude dichotomous measure of sunscreen use. Although 2 fair-quality case-control studies suggest a protective effect of sunscreen for basal cell carcinoma, both used crude measures of sunscreen use and neither adjusted for sun exposure (Appendix Table 2)58,59.
On the basis of 1 fair-quality cohort and 4 fair-quality case-control studies, sunscreen use has no clear protective or harmful effect on the risk for melanoma (Appendix Table 2)31,66,66,76,86. One cohort and 1 case-control study found no significant association between a crude dichotomous measure of sunscreen use and risk for melanoma66,86. One study found a protective effect for women who reported always using sunscreen compared with those who reported sometimes or never using sunscreen. This study adjusted for skin phenotype and sunburn, but not sun exposure68. Two studies conducted in Sweden found a statistically significant harmful effect of sunscreen, such that persons who reported always or almost always using sunscreen were at increased risk for melanoma, after adjustment for both skin phenotype and sun exposure31,76.
Study Heterogeneity and Methodological Limitations
This body of epidemiologic evidence examining sun exposure, indoor tanning, and sunscreen use has several important limitations. There was great heterogeneity in the actual measurement of sun exposure among studies, the categorization of levels of exposure, and in choice of reference groups. Sun-exposure measurements used different definitions and assessment methods and often covered different periods of a person's life. Measurement of sunscreen rarely included important details, such as sun protection factor, amount, frequency and duration, and years because sunscreens have changed over time. Likewise, measurement of indoor tanning rarely included important details, such as rationale or motivation of use, frequency and duration, and years because indoor tanning devices have also changed over time. Adjustment for important confounders and stratification to examine effect modification also varied across studies. Studies examining sun exposure generally adjusted for age, sex, and some measure of skin phenotype or sun sensitivity. Several studies examining indoor tanning and sunscreen use did not adjust for sun exposure. Some studies also may have overadjusted for confounding, such as adjustment for nevi, freckling, or sunburn history, because these are probably intermediate steps in carcinogenesis or surrogates for sun exposure. Finally, only 4 studies presented results stratified by skin phenotype; these studies suggest an interaction between skin phenotype and skin cancer25,57,75,91. Therefore, simply adjusting for skin type as a confounder in logistic regression may be insufficient to illuminate the effect of sun exposure in at-risk populations (for example, poor tanners). Lack of adequate adjustment and lack of stratification for skin phenotype may explain the lack of association seen in some studies or inverse association reported with occupational sun exposure.
Key Questions 3 and 5: Potential Harms of Sun-Protective Behaviors
On the basis of the trials included in key questions 1 and 2, we found no evidence for harms of counseling to prevent skin cancer. In addition, we found 17 fair- or good-quality studies that directly examined the potential harms of sun-protective behaviors (Table 4)92-107. Overall validity concerns are summarized in Table 4. One fair-quality trial that examined whether adherence to sun-protective behaviors in children reduces physical activity found no difference in body mass index or self-reported time spent outdoors at long-term follow-up between children receiving sun-protection curricula versus standard health-education curricula in schools92. This finding is consistent with 1 of the included counseling trials that found no difference in self-reported measures of physical activity50,106,107. Six fair- or good-quality trials examined whether sunscreen use leads to increased sun exposure93-95,108-110. These RCTs suggest that sunscreen with a higher sun protection factor may increase intentional sun exposure in healthy student volunteers on vacation. Sunscreen use in general, however, does not promote increased sun exposure. Three fair-quality studies examined the effect of sun exposure or sunscreen use on vitamin D levels96,97,111. One small, fair-quality trial showed that sunscreen use during the summer did not significantly decrease vitamin D levels or cause vitamin D deficiency96. Two fair-quality cohort studies demonstrated that vitamin D levels were influenced by sun exposure, such that post- or perimenopausal women living at high altitudes were at risk for transient vitamin D deficiency during winter months97,111.
It is hypothesized that sun exposure may be protective against some types of cancer through vitamin D production. Seven fair- or good-quality studies examined the relationship between sun exposure and risk for nonskin cancer98,99,101-105. On the basis of a sparse body of fair- or good-quality cohort and case-control studies, it seems that sun exposure in lighter pigmented persons may be inversely related to risk for advanced breast and prostate cancer after adjustment for well-established risk factors and that intermittent sun exposure may be inversely related to risk for non-Hodgkin lymphoma98,100-103,105. None of these studies, however, directly measured vitamin D status.
New evidence since the 2003 USPSTF recommendation suggests that counseling relevant to primary care can change sun-protective behaviors (Table 4). In young women, appearance-focused behavioral interventions can decrease indoor tanning behaviors and ultraviolet exposure in the short term. In young adolescents, primary care counseling with computer support can decrease midday sun exposure and increase sunscreen use. Evidence in adults and parents of newborns suggests that behavioral interventions can minimally increase composite scores measuring sun-protective behaviors. It is unclear, however, whether the small differences in composite scores of self-reported sun-protective behaviors translate into clinically meaningful behavior change to prevent skin cancer or sunburns.
Most of the counseling interventions that were effective in promoting sun-protective behaviors in adults incorporated computerized support providing tailored patient education. This type of computerized support is not widely available, although it is unclear whether it is essential to the effectiveness of the interventions. All trials conducted in young adults used appearance-focused behavioral interventions primarily aimed at women. It is possible that different counseling messages will be effective for populations of different age or sex. More primary care-relevant counseling trials to promote sun-protective behaviors are needed, especially in younger persons. On the basis of the epidemiologic evidence, childhood seems to be the ideal time to intervene in terms of sun-protective behaviors. Trials of successful interventions need to be replicated in other populations, however, and trials should incorporate more consistent and robust measures of ultraviolet exposure, sun-protective behaviors, and indoor tanning 112,113.
Overall, we found little evidence that sun-protective counseling or practicing sun-protective behaviors cause important harms, including decreasing physical activity, paradoxically increasing sun exposure, or causing clinically significant vitamin D deficiency. A recent report from the World Health Organization International Agency for Research on Cancer addresses the complex relationship between serum vitamin D levels and sun exposure 114. Although cutaneous vitamin D synthesis varies among persons, it generally happens relatively quickly, such that maximum vitamin D synthesis occurs at suberythemogenic ultraviolet doses 114. In addition, this report recognizes the importance of dietary vitamin D during the winter when skin synthesis of vitamin D is insufficient 114. Finally, it has been hypothesized that vitamin D production may be protective against certain types of cancer. The few casecontrol studies published on this topic suggest that intermittent sun exposure in lighter-pigmented persons may be inversely related to risk for advanced breast cancer, prostate cancer, and non-Hodgkin lymphoma. However, this literature is sparse, and the available population-based casecontrol studies lack adjustment for vitamin D intake and direct measurement of vitamin D levels. Furthermore, given the limited number of published studies, it is likely that this body of literature is affected by publication bias 114.
Fair-quality cohort and casecontrol studies examining the relationship between sun exposure and skin cancer suggests that increasing intermittent (or recreational) sun exposure is associated with an increased risk for all types of skin cancer (Table 4). Fewer studies examined the association of total and chronic (or occupational) sun exposure. These studies do not suggest a strong association between total or chronic sun exposure and skin cancer. Our findings are generally consistent with other existing reviews examining the association between ultraviolet exposure and skin cancer 23,115. A limited number of studies using crude measures of indoor tanning exposure examined the risk for squamous cell carcinoma and basal cell carcinoma, after adjusting for all important confounders. However, a slightly larger body of higher-quality evidence suggests that regular or early use of indoor tanning may increase the risk for melanoma. Again, this finding is consistent with an existing review by the International Agency for Research on Cancer Working Group on artificial ultraviolet light and skin cancer that found evidence to suggest that first use of indoor tanning equipment before age 35 years increases risk for melanoma 17. Regular sunscreen use can prevent squamous cell carcinoma, but it is unclear whether it can prevent basal cell carcinoma or melanoma. This finding is consistent with a fair-quality systematic review and meta-analysis by Dennis and colleagues 18 that found no significant association between melanoma and sunscreen use. Therefore, behavioral counseling to promote skin cancer prevention should focus on improving several behaviors to reduce ultraviolet exposure and not on increasing sunscreen use alone.
Despite the number of relevant cohort and population-based casecontrol studies, the available literature is limited because of the complex and variable nature of measuring sun exposure and sunscreen use; inconsistent and inadequate evaluation of important confounders and effect modifiers; and problems with recall bias, retest reliability, and other errors in determining true exposure 116. However, 1 included study found little evidence of important recall bias of ultraviolet exposure 73. In addition, the associations observed in these studies may not apply to current use of indoor tanning or sunscreen because these technologies have changed in the recent past. Indoor tanning devices produced before 1980 had higher ultraviolet B (UVB) content, and those produced after 1980 had higher ultraviolet A (UVA) content 83. Furthermore, modern tanning beds have undergone technologic advances to enrich UVB that allow shorter duration of exposure. In practice, however, the proportion of UVB output of indoor tanning devices varies 17. Likewise, sunscreens have also changed over time. Sun protection factor was introduced in 1978, and protection for UVA was not added until 1989. Ultraviolet sun exposure is approximately 5% UVB and 95% UVA 17. In addition, current sunscreens offer higher-level sun protection factor and water resistance.
More and better-designed studies are needed to examine the potential harms of sunscreen use and decreased sun exposure on vitamin D and other diseases hypothesized to be affected by vitamin D, including nonskin cancer. Currently, no evidence suggests that sun-protective behavior messages aimed at reducing prolonged or intense sun exposure and sunburns cause important harms, such as vitamin D deficiency or increasing risk for cancer. Additional studies with more detailed assessment of sunscreen and indoor tanning are needed. It is important that these studies consistently adjust for both important host and environmental factors. Survey instruments to assess for these types of exposure must be reliable and validated. This body of evidence would be strengthened if studies used the same or similar measurements to facilitate comparisons across studies. It will probably take decades to see a potential protective effect of regular use of sunscreens on melanoma risk or potential harms of current tanning beds on melanoma risk. Therefore, studies evaluating current sunscreens and indoor tanning will continue to be necessary well into the future.
Source: This article was first published in Annals of Internal Medicine (Ann Intern Med 2011;154:190-201).
Acknowledgments: The authors thank Daphne Plaut, MLS, for conducting the literature searches; Kevin Lutz, MFA, for his editorial support; Sarah Zuber, MSW, and Tracy Beil, MS, for their assistance in conducting the evidence review; and Evelyn Whitlock, MD, MPH, for her guidance. The authors also thank the Agency for Healthcare Research and Quality and the U.S. Preventive Services Task Force, as well as the expert reviewers for their contribution to this evidence review.
Grant Support: By the Oregon Evidence-based Practice Center under contract to the Agency for Healthcare Research and Quality (contract HHS-290-2007-10057-I, task order 3).
Requests for Single Reprints: Jennifer S. Lin, MD, MCR, Center for Health Research, Kaiser Permanente Northwest, 3800 North Interstate Avenue, Portland, OR 97227; e-mail, email@example.com.
Current author addresses and author contributions are available at http://www.annals.org.
- Is there direct evidence that counseling patients on sun-protective behaviors (decreasing sun exposure, avoidance of indoor tanning, and using sunscreen) reduces intermediate outcomes (sunburns, nevi, or actinic keratoses) or skin cancer (melanoma, SCC, or BCC)?
- Do primary care-relevant counseling interventions change sun-protective behaviors (decreasing sun exposure, avoidance of indoor tanning, and using sunscreen)?
- Do primary care-relevant counseling interventions have adverse effects?
- Is sun exposure (intentional or unintentional), indoor tanning, or sunscreen use associated with skin cancer outcomes?
- Are sun-protective behaviors associated with adverse effects (e.g., paradoxical increase in sun exposure, reduced physical activity, dysphoric mood, vitamin D deficiency)?
BCC = basal cell carcinoma; KQ = key question; SCC = squamous cell carcinoma.
|Key Question||Skin Cancer||Systematic Review Used to Locate Primary Research||Search Date*|
|1-3: Counseling||Any||Primary: Helfand and Krages, 200315
Others: Saraiya et al, 200432
|2001 to February 2010|
|4: Sun exposure||Melanoma
|Primary: Helfand and Krages, 200315
Others: Gandini et al, 200523; Saraiya et al, 200432
No systematic review found
|2001 to February 2010
1966 to February 2010
|4: Indoor tanning||Any||Primary: IARC, 200717
Others: Gallagher et al, 200521
|2005 to February 2010|
|Primary: Dennis et al, 200318
Others: Huncharek and Kupelnick, 200233; Gefeller and Pfahlberg, 200234
No systematic review found
|2002 to February 2010
1966 to February 2010
|5: Harms||Any||Primary: No systematic review found
Others: Helfand and Krages, 200315; Grant, 200735; Autier et al, 200736
|1966 to February 2010|
BCC = basal cell carcinoma; IARC = International Agency for Research on Cancer; SCC = squamous cell carcinoma.
* Start date for searches is 1 y before the end search date used in the primary existing systematic review.
|Study, Year (Reference); Study Design||Setting and Population||Intervention||Outcomes||Validity Concerns|
|Glanz et al, 201042; RCT||Home (primary care);
n = 724; mean age, 42 y; high risk
|3 mailed packages with tailored risk feedback and recommendations||Sun-protection score (6-item, higher is safer), adjusted mean (±SE)
|Fair quality: 82% follow-up; short follow-up; for individual behavior results, only sunglasses use was significant|
|Glazebrook et al, 200641; cluster RCT||Primary care; n = 589; mean age, 38 y; high risk||~15-min self-directed computer session, “Skin Safe program”||Sun-protection score (8-item, higher is safer), mean (SD)
Mean difference, 0.30 (95% CI, 0.100.51)
|Fair quality: 78% follow-up, higher follow-up in intervention group, composite score only|
|Prochaska et al, 200543; RCT||Home (primary care); n = 3834; mean age, 45 y; stage of change||4 phone sessions (unknown duration), written survey assessments with computer-generated tailored materials||Sun-avoidance score (4-item, higher is safer), mean (SD)
Sunscreen-use score (3-item, higher is safer), mean (SD)
|Fair quality: <80% follow-up, higher follow-up in control group, some gaps in reporting, composite scores only|
|Prochaska et al, 200444; RCT||Home (school); n = 1802; mean age, 42 y; stage of change||4 phone sessions (unknown duration), written survey assessments with computer-generated tailored materials||Sun-avoidance score (4-item, higher is safer), mean (SD)
Sunscreen-use score (3-item, higher is safer), mean (SD)
|Fair quality: <80% follow-up, higher follow-up in control group, some gaps in reporting, composite scores only|
|Geller et al, 200645; cluster RCT||Home (dermatology); n = 494; mean age, 58 y; family history||4 (~15-min) phone sessions with computer-generated tailored materials||Tanned by the end of previous summer
Adjusted OR, 0.72 (CI, 0.47-1.09)
Routinely use sunscreen with SPF ≥15
Adjusted OR, 0.96 (CI, 0.67-1.38)
|Fair quality: only 64% follow-up at 12 mo, different behavioral outcomes reported|
|Hillhouse et al, 200846; RCT||University; n = 430; mean age, 19 y; women who use indoor tanning||Professionally produced booklet, appearance-focused||Indoor tanning sessions for previous 3 mo, mean ( ±SE)
|Fair quality: good (96%) follow-up but some gaps in reporting|
|Mahler et al, 2007 47; RCT||University; n = 133; mean age, 20 y; 80% women||11-min appearance-focused video on photoaging (plus or minus UV facial photo)||Skin color using skin-reflectance spectrophotometry, change in L* scale (measure of lightness or black versus white) at 12 mo (higher is lighter; exact numbers NR)
Sun-protection score (8-item, higher is safer), Z scores adjusted for baseline (±SE) at 12 mo
|Fair quality: only 63% follow-up, results not presented vs. control group|
|Stapleton et al, 201048; RCT||University; n = 362; mean age, 19 y; women who use indoor tanning||Professionally produced booklet, appearance-focused||Indoor tanning sessions in previous 3 mo, mean (SD) (results presented by subgroups only)
|Fair quality: <80% follow-up, only 3-mo follow-up, some gaps in reporting, results by subgroup only|
|Turrisi et al, 200849; RCT||University; n = 105; mean age, NR; women who frequently indoor tan||IG1: 30-min appearance-focused peer-counseling session with graphic feedback
IG2: mailed graphic feedback only
|Indoor tanning sessions in previous 3 mo, mean difference (SD)
|Fair quality: follow-up 3 mo NR, only 3-mo follow-up|
|Norman et al, 200750; RCT||Primary care; n = 819; mean age, 13 y; not selected for risk||Two 20-min computer sessions with tailored materials, 4 phone sessions, brief primary care physician counseling||Adjusted mean sun-protection scale (7-item, higher is safer)
Exact numbers NR
At 6, 12, and 24 mo for IG, a statistically significant increase in sun-protection scores compared with CG, with trajectory of scores flattening (but still statistically significant) from 12-24 mo
|Fair quality: 80% follow-up; some gaps in reporting; for individual behavior results, only avoid or limit midday sun exposure were significant|
|Crane et al, 200651; cluster RCT||Primary care; n = 728; new parents; not selected for risk||Counseling and written materials given by primary care physician at 4 well-child visits||Mean sun-protection score (7-item, higher is safer)
|Fair quality: >75% follow-up, none of the individual behavior results was statistically significant|
CG = control group; IG = intervention group; NR = not reported; NS = not significant; OR = odds ratio; RCT = randomized, controlled trial; SPF = sun protection factor; UV = ultraviolet.
|Exposure||Skin Cancer||Total in Study Type (Reference)||Total, n||Findings|
|Intermittent or recreational sun exposure||SCC or BCC
|Increased risk (OR, 1.3-5.0); more consistent in studies with timing of sun exposure in childhood|
|Chronic or occupational sun exposure||SCC or BCC
|No significant association
Mixed findings; 5 of 9 studies show inverse association
|Total or cumulative sun exposure||SCC or BCC
|No significant association
Increased risk (OR, 1.8-4.4) in studies with sun exposure in childhood
|Indoor tanning||SCC or BCC
|Very limited evidence available
Increased risk (OR, 1.6-2.3) with regular use or use at a younger age
|Sunscreen use||SCC or BCC
4 case-control 31,66,68,76
|Regular use can prevent SCC (RR, 0.65); no significant association for BC
Mixed findings; no clear protective or harmful association
BCC = basal cell carcinoma; OR = odds ratio; RR = relative risk; SCC = squamous cell carcinoma.
|Key Question||Studies||Findings||Validity Concerns|
|1||No trials identified|
|2: Adults||5 RCTs (n = 7443)||Counseling with tailored risk feedback (with or without computer support) can make small increases in sun-protective behavior composite scores||No good-quality trials; samples selected for skin-cancer risk factors or suboptimal sun-protective behaviors; trials used composite scores|
|2: Young adults||4 RCTs (n = 1030)||Appearance-focused counseling in college-aged women who indoor tan can decrease self-reported tanning and objectively measured sun exposure||No good-quality trials; samples selected for women who indoor tan; none conducted in primary care; trials had short-term follow-up|
|2: Adolescents||1 RCT (n = 819)||Counseling with computer support for adolescents can decrease self-reported sun exposure||Only 1 fair-quality trial|
|2: Children||1 RCT (n = 728)||Counseling integrated into well-child visits for infants can make small increases in sun-protective behavior composite scores||Only 1 fair-quality trial; none of the individual sun-protective behavior changes was significant|
|4: Sun exposure||6 cohort (n = 335,835)
25 case-control (n = 20,425
|Intermittent sun exposure, especially sun exposure in childhood, can increase the risk for all types of skin cancer||Overall fair-quality evidence with large variation in measurement of exposure and inconsistent adjustment of confounders; cohort studies not primarily designed to measure sun exposure|
|4: Indoor tanning||1 cohort (n = 106,366)
15 case-control (n = 15,079)
|Limited evidence to suggest that regular or early use of indoor tanning may increase the risk for melanoma
Regular sunscreen use can prevent SCC, but benefit is unclear for BCC or melanoma
|Overall fair- to poor-quality evidence using crude measures of indoor tanning and sunscreen use and inconsistent (sometimes inadequate) adjustment for confounders; concerns about applicability owing to change in indoor tanning and sunscreen technology over past 20-30 y|
|4: Sunscreen||1 RCT (n = 1621)
3 cohort (n = 369,421)
6 case-control (n = 5708)
|3 or 5: Activity||2 RCTs (n = 2434)
6 RCTs (n = 4482)
plus the 8 RCTs from key question 2
|No evidence for decrease in physical activity in youth; potential harms include increased sun exposure with higher SPF sunscreen (but not sunburns) in young adults who are intentionally sunbathing; evidence for an inverse association of cancer risk due to sun exposure (through vitamin D) is very limited at this point||Overall, fair-quality evidence; evidence was sparse for lack of harms for vitamin D deficiency owing to inclusion criteria; evidence was sparse with methodological limitations for increased cancer risk; probable publication bias|
|3 or 5: Sun exposure||6 RCTs (n = 4482)
plus the 8 RCTs from key question 2
|5: Vitamin D||1 RCT
2 cohort (n = 2116)
|5: Cancer||1 cohort
(n = 26,037)
BCC = basal cell carcinoma; RCT = randomized, controlled trial; SCC = squamous cell carcinoma; SPF = sun protection factor; UV = ultraviolet.
|Variable||Key Questions 1-3 (Counseling)||Key Questions 4 (Association) and 5 (Harms)|
|Include||Randomized or controlled clinical trials||Trials or observational studies (including cohort or population-based case-control studies)|
|Exclude||Any observational study||Hospital-based case-control studies, ecological analyses, cross-sectional studies, case series, and case reports|
|Include||English-speaking countries, primary care or setting judged to be generalizable to primary care||Any setting|
|Exclude||Inpatient hospital units, emergency departments, pharmacies, recreational or occupational settings, other community-based settings (e.g., schools or churches)||None|
|Include||Any age person without current or past skin cancer or precancerous skin lesions||Any sample (sample description must be reported)|
|Exclude||Persons with syndromes that substantially increase risk for skin cancer (e.g., xeroderma pigmentosum, albinism, persons being treated with psoralen or UV treatment, or familial syndromes or strong family history of melanoma)|
|Intervention or exposure|
|Include||Counseling involving individual-level identification of person, conducted in primary care, or judged to be feasible to be conducted in primary care (e.g., mailed or electronic interventions), or referable from primary care (i.e., delivered as part of the health care setting or widely available at a national level in the community)||Exposure to UV radiation (sun or indoor tanning) or sunscreen use, with description of how exposure was measured|
|Exclude||Noncounseling interventions, counseling for skin self-examinations, nonreferable interventions (through work or school), social marketing, or policy interventions||None|
|Include||Skin cancer incidence or associated morbidity or mortality; intermediate outcomes (sunburns, nevi, or actinic keratosis); behavioral outcomes (decrease in UV exposure through avoidance or reduction during midday or peak hours, wearing protective clothing, avoidance of indoor tanning, and use of sunscreen); adverse outcomes (e.g., paradoxical increase in sun exposure, reduced physical activity, dysphoric mood, vitamin D deficiency, increased incidence of nonskin cancer)|
|Exclude||Any trial with >40% attrition or no behavioral outcome beyond 3 mo; attitude, knowledge, or ability changes||None|
UV = ultraviolet.
Study, Year (Reference);
|Total Sun Exposure (RR or OR [95% CI])*||Intermittent Sun Exposure (RR or OR [95% CI])*||Chronic Sun Exposure (RR or OR [95% CI])*||Adjustments Reported|
|Association between sun exposure and skin cancer (SCC or BCC)|
|Chen et al, 201060; fair||Case-control; Taiwan; 87 cases, 216 controls||
Lifetime sun exposure (tertile) for SCC
Second: 2.98 (1.36-6.53)
Third: 3.95 (1.81-8.59)
Early-age sun exposure (tertile)
Second: 1.49 (0.72-3.09)
Third: 2.43 (1.25-4.75)
|NR||Age, sex, smoking status, BMI|
|Gallagher et al, 199561, Bajdik et al, 1996117; fair||Case-control; Alberta, Canada; 180 cases, 406 controls||
Mean cumulative sun exposure per year for SCC
<11.5 h/wk summer: reference
11.5-19 h/wk summer: 1.8 (0.9-3.3)
19-28 h/wk summer: 1.2 (0.6-2.3)
≥28 h/wk summer: 1.0 (0.4-2.1)
Mean recreational sun exposure per year
Age 0-19 y
<3.8 h/wk summer: reference
3.8-7.5 h/wk summer: 1.2 (0.6-2.5)
7.5-12.5 h/wk summer: 1.1 (0.5-2.6)
≥12.5 h/wk summer: 1.6 (0.6-4.5)
<2.8 h/wk summer: reference
2.8-5.6 h/wk summer: 0.6 (0.3-1.1)
5.6-8.5 h/wk summer: 0.8 (0.3-1.8)
≥8.5 h/wk summer: 0.3 (0.1-0.9)
Mean occupational sun exposure per year
<3.5 h/wk summer: reference
3.5-14 h/wk summer: 0.8 (0.3-2.0)
14-25 h/wk summer: 1.5 (0.6-4.2)
≥25 h/wk summer: 1.4 (0.4-4.3)
|Age, sex, mother's ethnic origin, hair color, skin color|
|Gallagher et al, 199561, Bajdik et al, 1996117; fair||Case-control; Alberta, Canada; 180 cases, 406 controls||NR||
Mean recreational sun exposure per year
Age 0-19 y
<3.8 h/wk summer: reference
3.8-7.5 h/wk summer: 1.1 (0.6-2.0)
7.5-12.5 h/wk summer: 1.4 (0.7-3.0)
≥12.5 h/wk summer: 2.6 (1.1-6.5)
<2.8 h/wk summer: reference
2.8-5.6 h/wk summer: 0.9 (0.5-1.7)
5.6-8.5 h/wk summer: 0.6 (0.3-1.3)
≥8.5 h/wk summer: 0.4 (0.2-1.0)
Mean occupational sun exposure per year
<3.5 h/wk summer: reference
3.5-14 h/wk summer: 1.0 (0.6-1.8)
14-25 h/wk summer: 1.3 (0.8-2.3)
≥25 h/wk summer: 1.4 (0.8-2.4)
|Age, sex, mother's ethnic origin, hair color, skin color|
|Green et al, 199654, Nambour Skin Cancer Study; fair||Cohort; Queensland, Australia; n = 2095||NR||
Mainly indoors: reference
Indoors/outdoors: 0.81 (0.37-1.80)
Mainly outdoors: 1.29 (0.66-2.52)
Mainly indoors: reference
Indoors/outdoors: 0.93 (0.63-1.37)
Mainly outdoors: 0.85 (0.59-1.21)
Mainly indoors: reference
Indoors/outdoors: 0.82 (0.47-1.43)
Mainly outdoors: 1.37 (0.80-2.34)
Mainly indoors: reference
Indoors/outdoors: 1.07 (0.79-1.46)
Mainly outdoors: 1.25 (0.88-1.78)
|Age, sex, skin color|
|Grodstein et al, 199555, NHS; good||Cohort; United States (11 states); n = 107,900||NR||
Regular time outdoors in summer
Yes (use sunscreen): reference
Yes (no sunscreen): 0.9 (0.6-1.2)
No: 0.7 (0.4-1.1)
|NR||Age, smoking status, region, hair color, reaction to sun, lifetime number of sunburns|
|Han et al, 200657, NHS; fair||Nested case-control; United States (11 states); 275 SCC cases, 283 BCC cases, 804 controls||NR||
Total lifetime sun exposure while wearing a bathing suit (tertile)
Intermediate: 1.28 (0.85-1.93)
High: 2.15 (1.45-3.19)
Intermediate: 1.71 (1.14-2.56)
High: 2.05 (1.38-3.06)
|NR||Age, constitutional susceptibility, family history of skin cancer, number of lifetime severe sunburns that blistered, sunlamp use or tanning salon attendance, region|
|Hunter et al, 199056, NHS; fair||Analytic cohort; United States (11 states); n = 73,366||NR||
Regular time outdoors in summer
Yes (with sunscreen): reference
Yes (no sunscreen): 0.70 (0.60-0.82)
No: 0.73 (0.59-0.90)
|NR||Age, time period, region, time spent outdoors in summer and sunscreen habit, hair color, childhood tendency to burn, lifetime number of severe sunburns|
|Kricker et al, 199158, Kricker et al, 199525, Kricker et al, 199591, English et al, 1998118, English et al, 199820; fair||Case-control; Western Australia; 248 total cases; 226 BCC cases; 45 SCC cases; 1015 total controls; 1021 BCC controls; 1064 SCC controls||
Total hours (thousands) sun exposure from 9 a.m.-5 p.m.
40.5-56.4: 0.99 (0.61-1.58)
56.4-81.6: 1.42 (0.86-2.35)
≥81.6: 0.77 (0.43-1.40)
Age >15 y
14.8-27.7: 1.25 (0.79-1.97)
27.8-49.3: 1.17 (0.72-1.90)
≥49.4: 0.86 (0.50-1.51)
Total ambient sunlight in accumulated global radiance (mWh/cm2 X 105)
8.8-10.1: 1.32 (0.69-2.55)
10.1-11.4: 1.72 (0.72-4.09)
≥11.4: 2.18 (0.82-5.82)
Intermittent sun exposure, age 15-19 y
41-58%: 1.49 (0.88-2.52)
59-99%: 1.82 (1.01-3.28)
100%: 3.86 (1.93-7.75)
Lifetime hours of sun exposure on vacation
602-2268: 1.65 (1.01-2.70)
2268-3794: 1.68 (1.00-2.80)
≥3794: 1.85 (1.09-3.13)
Lifetime frequency of sunbathing
1-200: 1.57 (0.98-2.51)
201-700: 1.08 (0.68-1.72)
701-9000: 1.02 (0.63-1.64)
Total hours of sun exposure on working days
11,500-19,999: 0.93 (0.42-2.1)
20,000-32,999: 1.7 (0.81-3.8)
≥33,000: 1.3 (0.58-2.8)
|Age, sex, ability to tan, total sun exposure (for recreational sun exposure)|
|Neale et al, 200753, Nambour Skin Cancer Trial; fair||Cohort; Queensland, Australia; n = 1517||NR||
Leisure exposure (head, trunk [respectively])
Both: 0.93 (0.64-1.35); 1.15 (0.62-2.12)
Outdoors: 0.99 (0.60-1.63); 0.84 (0.32-2.17)
Occupational exposure (head, trunk [respectively])
Both: 0.95 (0.60-1.49); 1.07 (0.60-1.93)
Outdoors: 0.86 (0.53-1.40); 1.12 (0.60-2.11)
|Rosso et al, 199959; fair||Case-control; Switzerland; 146 cases, 144 controls||
Total lifetime hours
5001-64,200: 1.78 (0.18-17.67)
≥64,200: 1.42 (0.53-3.85)
15,001-15,800: 1.09 (0.62-1.92)
15,801-64,200: 0.99 (0.35-2.79)
≥64,200: 0.70 (0.20-2.39)
Lifetime hours at the beach on vacation
≥2260: 0.78 (0.26-2.40)
<300: 1.46 (0.52-4.07)
381-1140: 1.39 (0.72-2.66)
1140-2260: 0.92 (0.44-1.91)
≥2260: 1.20 (0.61-2.34)
Lifetime hours of outdoor work
≤47,900: 1.84 (0.30-11.09)
47,901-77,200: 2.02 (0.60-6.78)
≥77,200: 1.88 (0.30-11.70)
≤12,000: 0.98 (0.58-1.66)
12,001-47,900: 1.30 (0.69-2.46)
47,901-77,200: 0.78 (0.52-1.19)
≥77,200: 0.90 (0.51-1.59)
|van Dam et al, 199952, HPFS; fair||Cohort; United States (multistate); n = 44,591||NR||
Frequency outdoors in swimsuit as teenager in summer
<1 time/wk: reference
1 time/wk: 1.30 (1.14-1.47)
2 times/wk: 1.34 (1.19-1.52)
Several times/wk: 1.36 (1.22-1.52)
Daily: 1.42 (1.24-1.63)
|NR||Age, time period, region, hair color, eye color, skin reaction to sun, ancestry, BMI|
|Vlajinac et al, 200063; fair||Case-control; Yugoslavia; 200 cases, 399 controls||NR||
Vacations at seaside before age 10 y
Not statistically significant, OR not reported
Average number of weeks per year spent at seaside
≥7: 1.81 (1.24-2.64)
|Association between sun exposure and skin cancer (melanoma)|
|Berwick et al, 199665, Lea et al, 2007119, Chen et al, 1996120; fair||
Connecticut; 650 cases, 549 controls
Total lifetime sun exposure
Moderate: 1.26 (0.69-2.29)
Heavy: 2.20 (1.21-4.01)
Very heavy: 2.63 (1.25-5.54)
1-14: 1.1 (0.8-1.7)
15-90: 0.9 (0.5-1.4)
|Age, sex, skin self-examination, total nevi, family history skin cancer, skin type, hair/eye color, freckle, ever severely sunburned|
|Fargnoli et al, 200466; fair||Case-control; central Italy; 100 cases, 200 controls||NR||
Hours of recreational sun exposure per year
60-120: 0.761 (0.420-1.378)
121-240: 1.641 (0.799-3.370)
>240: 5.010 (2.110-11.891)
Occupational sun exposure
Yes: 2.57 (1.40-4.73)
|Age, sex, ethnicity, region, hair color, eye color, skin type|
Gallagher et al, 198669, Elwood et al, 1985121, Elwood et al, 1984122, Western Canada Melanoma Study;
|Case-control; western Canada; 595 cases, 595 controls||
Total hours annual sun exposure
50-99: 1.5 (0.8-2.7)
100-149: 1.5 (0.9-2.7)
150-199: 1.6 (0.9-2.9)
200-299: 1.0 (0.6-1.7)
300-399: 1.1 (0.6-1.9)
400-499: 1.6 (0.9-2.7)
≥500: 1.2 (0.7-2.0)
Total hours of recreational exposure in summer
<1-19: 1.1 (0.7-1.6)
20-79: 1.7 (1.2-2.5)
80-159: 1.8 (1.2-2.7)
≥160: 1.7 (1.1-2.7)
Total hours of vacation in summer
1-6: 0.9 (0.7-1.3)
7-19: 0.9 (0.6-1.4)
20-39: 1.9 (1.3-3.0)
≥40: 1.5 (1.0-2.3)
Total sunny vacations per decade of life
<1: 1.1 (1.0-1.1)
1-3: 1.3 (1.1-1.5)
≥4: 1.7 (1.2-2.3)
Occupation hours, summer season
1-99: 1.8 (1.2-2.5)
100-199: 1.0 (0.7-1.5)
200-399: 0.9 (0.6-1.4)
≥400: 0.9 (0.6-1.5)
|Age, sex, hair/skin color, freckling, ethnic origin|
|Garbe et al, 198977; fair||
Germany; 200 cases, 200 controls
Occupational sun exposure
Sometimes: 1.18 (0.56-2.48)
Often: 11.62 (2.13-63.33)
|Green and O'Rourke, 198567, Green et al, 1986123; fair||Case-control; Queensland, Australia; 183 cases, 183 controls||
Total hours sun exposure
2000: 2.3 (1.0-5.1)
50,000: 1.7 (0.4-7.8)
Ages 10-19 y
500: 1.0 (0.5-2.0)
5000: 4.4 (1.8-184.5)
Recreational hours on the beach
1: 0.6 (0.2-1.4)
500: 0.3 (0.1-0.8)
5000: 1.3 (0.4-4.3)
Ages 10-19 y
1: 1.1 (0.6-2.0)
500: 0.8 (0.4-1.9)
|NR||Age, sex, presence of nevi on the arms, hair color, sunburn propensity|
|Han et al, 200657, NHS; fair||Nested case-control; United States (11 states); 200 cases, 804 controls||NR||
Total lifetime sun exposure while wearing a bathing suit (tertile)
Intermediate: 1.20 (0.73-1.97)
High: 2.37 (1.51-3.73)
|NR||Age, constitutional susceptibility, family history of skin cancer, number of lifetime severe sunburns, indoor tanning, region|
|Holly et al, 199568; fair||Case-control; San Francisco, CA; 452 cases, 930 controls||NR||
Time spent outdoors on weekend
Previous 10 y
<25% of time: 0.72 (0.35-1.4)
25%-50% of time: 0.71 (0.37-1.4)
50%-75% of time: 0.86 (0.42-1.8)
≥75% of time: 0.84 (0.37-1.9)
Frequency of sunbathing in typical year
Time spent outdoors on weekday
Previous 10 y
<25% of time: 0.71 (0.49-1.0)
25%-50% of time: 0.83 (0.53-1.3)
≥75% of time: 0.83 (0.46-1.5)
|Age, sex, region|
|LeMarchand et al, 200671; fair||Case-control; Hawaii; 278 cases, 278 controls||NR||
Lifetime hours worked outdoors
439-1644: 1.0 (0.5-2.0)
1645-3360: 0.7 (0.4-1.5)
≥3361: 1.3 (0.7-2.7)
|Age, sex, height, education, hair color, ability to tan, drinking status|
|Nagore et al, 201078; fair||Case-control; Valencia, Spain; 160 cases, 318 controls||NR||NR||
Years of occupational sun exposure
≤20: 0.6 (0.3-1.3)
≥20: 2.1 (1.1-4.0)
|Age, hair color, personal history of NMSC, severe sunburns, smoking status, multiple nevi|
|Osterlind et al, 198872, Osterlind et al, 1988124; fair||Case-control; East Denmark; 474 cases, 926 controls||NR||
At some time: 1.6 (1.1-2.4)
1-9 y: 1.9 (0.9-3.9)
10-24 y: 1.6 (1.1-2.5)
25-39 y: 1.7 (1.1-2.5)
≥40 y: 1.9 (1.3-2.9)
Vacations spent in sun
Sunny: 1.0 (0.8-1.3)
Very sunny: 1.4 (1.0-2.1)
|NR||Sex, nevi, freckles, hair color, history of sunbathing, sunburning|
|Parr et al, 200973, NOWAC; fair||Nested case-control; Norway; 162 cases, 1242 controls||NR||
Sunbathing vacations, by age category
Age <10 y
≤1 per year: 2.10 (1.02-4.35)
≥2 per year: 1.11 (0.65-1.91)
Age 10-19 y
≤1 per year: 1.04 (0.59-1.84)
≥2 per year: 1.37 (0.86-2.21)
|NR||Age, region, hair color|
|Shors et al, 200181, Soloman et al, 2004125; fair||Case-control; Washington; 386 cases, 727 controls||
Lifetime average days with >4 h sun (quartile)
Second: 1.3 (0.86-1.9)
Third: 1.4 (0.92-2.0)
Fourth: 1.4 (0.95-2.0)
Lifetime overall UV exposure (quartile)
|NR||NR||Age, sex, income, tendency to burn, number of sunburns age 2-10 y|
|Tabenkin et al, 199979; fair||Case-control; Israel; 168 cases, 325 controls||
Number of hours of sun exposure
Age 6-13 y
Statistically significant difference, OR not reported
Age ≥14 y
Not statistically significant, OR not reported
Occupational sun exposure from age 21 y
No: 2.44 (1.01-5.91)
|Veierød et al, 201064, Veierød et al, 2003126, Norwegian-Swedish Women's Lifestyle and Health Cohort Study; fair||Cohort; Norway and Sweden; n = 106,366||NR||
Annual weeks on sunbathing vacation
Age 10-19 y
1: 1.12 (0.84-1.48)
2-3: 1.12 (0.84-1.48)
≥4: 1.87 (1.35-2.58)
Age 10-39 y
≥1: 1.54 (1.12-2.12)
|NR||Age, region of residence, hair/skin color|
|Walter et al, 199974, Walter et al, 1990127; fair||Case-control; Ontario, Canada; 583 cases, 608 controls||NR||
Beach vacation in previous 5 y
Yes: 1.04 (0.82-1.32)
|NR||Age, sex, reaction to initial summer sun exposure|
|Weinstock et al, 199175, NHS; fair||Nested case-control; United States (multistate); 130 cases, 300 controls||NR||
|Westerdahl et al, 199476, Westerdahl et al, 1994128, Westerdahl et al, 199529; fair||Case-control; Sweden; 400 cases, 640 controls||NR||
Frequent sunbathing during the summer
Yes: 1.2 (0.9-1.7)
|NR||Age, sex, region, indoor tanning, history of sunburns, hair color, number of nevi, history of malignant melanoma in immediate family|
|Westerdahl et al, 200031; fair||Case-control; Sweden; 558 cases, 891 controls||NR||
|NR||Age, sex, region, sunburns after age 19 y, skin phototype, hair color|
|White et al, 199480; fair||Case-control; Washington; 256 cases, 273 controls||
Average hours of yearly sun exposure
Previous 10 y
1-201: 1.16 (0.72-1.87)
202-499: 0.80 (0.45-1.42)
500-2880: 0.88 (0.47-1.64)
Lifetime occupational sun exposure
<50%: 0.89 (0.60-1.32)
≥50%: 0.64 (0.33-1.23)
|Age, sex, education|
|Zanetti et al, 199270; fair||Case-control; Turin, Italy; 260 cases, 416 controls||NR||
Weeks of sunny vacation in childhood
1-59: 2.8 (1.6-4.6)
≥60: 1.7 (1.0-2.9)
Sunny vacations in lifetime
BCC = basal cell carcinoma; BMI = body mass index; HPFS = Health Professionals Follow-up Study; NHS = Nurses' Health Study; NMSC = nonmelanoma skin cancer; NOWAC = Norwegian Women and Cancer Study; NR = not reported; OR = odds ratio; RCT = randomized, controlled trial; RR = relative risk; SCC = squamous cell carcinoma; UV = ultraviolet.
*Adjusted unless otherwise stated.
- American Cancer Society. Skin Cancer Facts. Accessed at www.cancer.org/Cancer/CancerCauses/SunandUVExposure/skin-cancer-facts?sitearear+PED2008 on 10 December 2010.
- Altekruse SF, Kosary CL, Krapcho M, Neyman N, Aminou R, Waldron W, et al. SEER Cancer Statistics Review, 1975-2007, National Cancer Institute. Bethesda, MD. Accessed at http://seer.cancer.gov/csr/1975_2007/ on 14 December 2010.
- Berwick M, Wiggins C. The current epidemiology of cutaneous malignant melanoma. Front Biosci. 2006;11:1244-54. [PMID: 16368510]
- Linos E, Swetter SM, Cockburn MG, Colditz GA, Clarke CA. Increasing burden of melanoma in the United States. J Invest Dermatol. 2009;129:1666-74. [PMID: 19131946]
- Purdue MP, Freeman LE, Anderson WF, Tucker MA. Recent trends in incidence of cutaneous melanoma among US Caucasian young adults [Letter]. J Invest Dermatol. 2008;128:2905-8. [PMID: 18615112]
- Gandini S, Sera F, Cattaruzza MS, Pasquini P, Zanetti R, Masini C, et al. Meta-analysis of risk factors for cutaneous melanoma: III. Family history, actinic damage and phenotypic factors. Eur J Cancer. 2005;41:2040-59. [PMID: 16125929]
- Markovic SN, Erickson LA, Rao RD, Weenig RH, Pockaj BA, Bardia A, et al; Melanoma Study Group of the Mayo Clinic Cancer Center. Malignant melanoma in the 21st century, part 1: epidemiology, risk factors, screening, prevention, and diagnosis. Mayo Clin Proc. 2007;82:364-80. [PMID: 17352373]
- IARC Working Group Reports. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans: Solar and Ultraviolet Radiation. vol. 55. Lyon, France: IARCPress; 1992.
- Balk SJ, O’Connor KG, Saraiya M. Counseling parents and children on sun protection: a national survey of pediatricians. Pediatrics. 2004;114:1056-64. [PMID: 15466105]
- Gritz ER, Tripp MK, de Moor CA, Eicher SA, Mueller NH, Spedale JH. Skin cancer prevention counseling and clinical practices of pediatricians. Pediatr Dermatol. 2003;20:16-24. [PMID: 12558840]
- Hornung RL, Hansen LA, Sharp LK, Poorsattar SP, Lipsky MS. Skin cancer prevention in the primary care setting: assessment using a standardized patient. Pediatr Dermatol. 2007;24:108-12. [PMID: 17461802]
- Kasparian NA, McLoone JK, Meiser B. Skin cancer-related prevention and screening behaviors: a review of the literature. J Behav Med. 2009;32:406-28. [PMID: 19521760]
- Geller AC, Colditz G, Oliveria S, Emmons K, Jorgensen C, Aweh GN, et al. Use of sunscreen, sunburning rates, and tanning bed use among more than 10,000 US children and adolescents. Pediatrics. 2002;109:1009-14. [PMID: 12042536]
- Coups EJ, Manne SL, Heckman CJ. Multiple skin cancer risk behaviors in the U.S. population. Am J Prev Med. 2008;34:87-93. [PMID: 18201637]
- Helfand M, Krages KP. Counseling to Prevent Skin Cancer: A Summary of the Evidence. (AHRQ Pub. No. 03–521B). Rockville, MD: Agency for Healthcare Research and Quality; 2003.
- U.S. Preventive Services Task Force. U.S. Preventive Services Task Force Procedure Manual. (AHRQ Publication No. 08-05118-EF). Rockville, MD: Agency for Healthcare Research and Quality; 2008. Accessed at www.uspreventiveservicestaskforce.org/uspstf08/methods/procmanual.htm on 10 December 2010.
- International Agency for Research on Cancer Working Group on artificial ultraviolet (UV) light and skin cancer. The association of use of sunbeds with cutaneous malignant melanoma and other skin cancers: a systematic review. Int J Cancer. 2007;120:1116-22. [PMID: 17131335]
- Dennis LK, Beane Freeman LE, VanBeek MJ. Sunscreen use and the risk for melanoma: a quantitative review. Ann Intern Med. 2003;139:966-78. [PMID: 14678916]
- Elwood JM, Jopson J. Melanoma and sun exposure: an overview of published studies. Int J Cancer. 1997;73:198-203. [PMID: 9335442]
- English DR, Armstrong BK, Kricker A, Winter MG, Heenan PJ, Randell PL. Demographic characteristics, pigmentary and cutaneous risk factors for squamous cell carcinoma of the skin: a case-control study. Int J Cancer. 1998;76:628-34. [PMID: 9610717]
- Gallagher RP, Spinelli JJ, Lee TK. Tanning beds, sunlamps, and risk of cutaneous malignant melanoma. Cancer Epidemiol Biomarkers Prev. 2005;14:562-6. [PMID: 15767329]
- Gandini S, Sera F, Cattaruzza MS, Pasquini P, Abeni D, Boyle P, et al. Meta-analysis of risk factors for cutaneous melanoma: I. Common and atypical naevi. Eur J Cancer. 2005;41:28-44. [PMID: 15617989]
- Gandini S, Sera F, Cattaruzza MS, Pasquini P, Picconi O, Boyle P, et al. Meta-analysis of risk factors for cutaneous melanoma: II. Sun exposure. Eur J Cancer. 2005;41:45-60. [PMID: 15617990]
- Gorham ED, Mohr SB, Garland CF, Chaplin G, Garland FC. Do sunscreens increase risk of melanoma in populations residing at higher latitudes? Ann Epidemiol. 2007;17:956-63. [PMID: 18022535]
- Kricker A, Armstrong BK, English DR, Heenan PJ. A dose-response curve for sun exposure and basal cell carcinoma. Int J Cancer. 1995;60:482-8. [PMID: 7829261]
- Nelemans PJ, Rampen FH, Ruiter DJ, Verbeek AL. An addition to the controversy on sunlight exposure and melanoma risk: a meta-analytical approach. J Clin Epidemiol. 1995;48:1331-42. [PMID: 7490596]
- Oliveria SA, Saraiya M, Geller AC, Heneghan MK, Jorgensen C. Sun exposure and risk of melanoma. Arch Dis Child. 2006;91:131-8. [PMID: 16326797]
- Rosso S, Zanetti R, Pippione M, Sancho-Garnier H. Parallel risk assessment of melanoma and basal cell carcinoma: skin characteristics and sun exposure. Melanoma Res. 1998;8:573-83. [PMID: 9918420]
- Westerdahl J, Olsson H, Måsbäck A, Ingvar C, Jonsson N. Is the use of sunscreens a risk factor for malignant melanoma? Melanoma Res. 1995;5:59-65. [PMID: 7734957]
- Westerdahl J, Ingvar C, Måsbäck A, Jonsson N, Olsson H. Risk of cutaneous malignant melanoma in relation to use of sunbeds: further evidence for UV-A carcinogenicity. Br J Cancer. 2000;82:1593-9. [PMID: 10789730]
- Westerdahl J, Ingvar C, Måsbäck A, Olsson H. Sunscreen use and malignant melanoma. Int J Cancer. 2000;87:145-50. [PMID: 10861466]
- Saraiya M, Glanz K, Briss PA, Nichols P, White C, Das D, et al. Interventions to prevent skin cancer by reducing exposure to ultraviolet radiation: a systematic review. Am J Prev Med. 2004;27:422-66. [PMID: 15556744]
- Huncharek M, Kupelnick B. Use of topical sunscreens and the risk of malignant melanoma: a meta-analysis of 9067 patients from 11 case-control studies. Am J Public Health. 2002;92:1173-7. [PMID: 12084704]
- Gefeller O, Pfahlberg A. Sunscreen use and melanoma: a case of evidence-based prevention? Photodermatol Photoimmunol Photomed. 2002;18:153-6; discussion 156. [PMID: 12207681]
- Grant WB. A meta-analysis of second cancers after a diagnosis of nonmelanoma skin cancer: additional evidence that solar ultraviolet-B irradiance reduces the risk of internal cancers. J Steroid Biochem Mol Biol. 2007;103:668-74. [PMID: 17208438]
- Autier P, Boniol M, Doré JF. Sunscreen use and increased duration of intentional sun exposure: still a burning issue. Int J Cancer. 2007;121:1-5. [PMID: 17415716]
- Lin JS, Eder M, Weinmann S, Zuber SP, Beil TL, Plaut D, et al. Behavioral Counseling to Prevent Skin Cancer: Systematic Evidence Review to Update the 2003 U.S. Preventive Services Task Force Recommendation. Evidence Synthesis No. 82. AHRQ Publication No. 11-05152-EF-1. Rockville, MD: Agency for Healthcare Quality and Research; February 2011.
- Bastuji-Garin S, Diepgen TL. Cutaneous malignant melanoma, sun exposure, and sunscreen use: epidemiological evidence. Br J Dermatol. 2002;146(Suppl 61):24-30. [PMID: 11966729]
- Koepsell T, Weiss N. Epidemiologic Methods: Studying the Occurrence of Illness. New York: Oxford Univ Pr; 2003.
- Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Accessed at www.ohri.ca/programs/clinical_epidemiology/oxford.htm on 10 December 2010.
- Glazebrook C, Garrud P, Avery A, Coupland C, Williams H. Impact of a multimedia intervention “Skinsafe” on patients’ knowledge and protective behaviors. Prev Med. 2006;42:449-54. [PMID: 16580059]
- Glanz K, Schoenfeld ER, Steffen A. A randomized trial of tailored skin cancer prevention messages for adults: Project SCAPE. Am J Public Health. 2010;100:735-41. [PMID: 20167900]
- Prochaska JO, Velicer WF, Redding C, Rossi JS, Goldstein M, DePue J, et al. Stage-based expert systems to guide a population of primary care patients to quit smoking, eat healthier, prevent skin cancer, and receive regular mammograms. Prev Med. 2005;41:406-16. [PMID: 15896835]
- Prochaska JO, Velicer WF, Rossi JS, Redding CA, Greene GW, Rossi SR, et al. Multiple risk expert systems interventions: impact of simultaneous stage-matched expert system interventions for smoking, high-fat diet, and sun exposure in a population of parents. Health Psychol. 2004;23:503-16. [PMID: 15367070]
- Geller AC, Emmons KM, Brooks DR, Powers C, Zhang Z, Koh HK, et al. A randomized trial to improve early detection and prevention practices among siblings of melanoma patients. Cancer. 2006;107:806-14. [PMID: 16832795]
- Hillhouse J, Turrisi R, Stapleton J, Robinson J. A randomized controlled trial of an appearance-focused intervention to prevent skin cancer. Cancer. 2008;113:3257-66. [PMID: 18937268]
- Mahler HI, Kulik JA, Gerrard M, Gibbons FX. Long-term effects of appearance-based interventions on sun protection behaviors. Health Psychol. 2007;26:350-60. [PMID: 17500622]
- Stapleton J, Turrisi R, Hillhouse J, Robinson JK, Abar B. A comparison of the efficacy of an appearance-focused skin cancer intervention within indoor tanner subgroups identified by latent profile analysis. J Behav Med. 2010;33:181-90. [PMID: 20058183]
- Turrisi R, Mastroleo NR, Stapleton J, Mallett K. A comparison of 2 brief intervention approaches to reduce indoor tanning behavior in young women who indoor tan very frequently [Letter]. Arch Dermatol. 2008;144:1521-4. [PMID: 19015434]
- Norman GJ, Adams MA, Calfas KJ, Covin J, Sallis JF, Rossi JS, et al. A randomized trial of a multicomponent intervention for adolescent sun protection behaviors. Arch Pediatr Adolesc Med. 2007;161:146-52. [PMID: 17283299]
- Crane LA, Deas A, Mokrohisky ST, Ehrsam G, Jones RH, Dellavalle R, et al. A randomized intervention study of sun protection promotion in well-child care. Prev Med. 2006;42:162-70. [PMID: 16376977]
- van Dam RM, Huang Z, Rimm EB, Weinstock MA, Spiegelman D, Colditz GA, et al. Risk factors for basal cell carcinoma of the skin in men: results from the health professionals follow-up study. Am J Epidemiol. 1999;150:459-68. [PMID: 10472945]
- Neale RE, Davis M, Pandeya N, Whiteman DC, Green AC. Basal cell carcinoma on the trunk is associated with excessive sun exposure. J Am Acad Dermatol. 2007;56:380-6. [PMID: 17097387]
- Green A, Battistutta D, Hart V, Leslie D, Weedon D. Skin cancer in a subtropical Australian population: incidence and lack of association with occupation. The Nambour Study Group. Am J Epidemiol. 1996;144:1034-40. [PMID: 8942434]
- Grodstein F, Speizer FE, Hunter DJ. A prospective study of incident squamous cell carcinoma of the skin in the Nurses’ Health Study. J Natl Cancer Inst. 1995;87:1061-6. [PMID: 7616597]
- Hunter DJ, Colditz GA, Stampfer MJ, Rosner B, Willett WC, Speizer FE. Risk factors for basal cell carcinoma in a prospective cohort of women. Ann Epidemiol. 1990;1:13-23. [PMID: 1669486]
- Han J, Colditz GA, Hunter DJ. Risk factors for skin cancers: a nested case-control study within the Nurses’ Health Study. Int J Epidemiol. 2006;35:1514-21. [PMID: 16943234]
- Kricker A, Armstrong BK, English DR, Heenan PJ. Pigmentary and cutaneous risk factors for non-melanocytic skin cancer—a case-control study. Int J Cancer. 1991;48:650-62. [PMID: 2071226]
- Rosso S, Joris F, Zanetti R. Risk of basal and squamous cell carcinomas of the skin in Sion, Switzerland: a case-control study. Tumori. 1999;85:435-42. [PMID: 10774562]
- Chen YC, Christiani DC, Su HJ, Hsueh YM, Smith TJ, Ryan LM, et al. Early-life or lifetime sun exposure, sun reaction, and the risk of squamous cell carcinoma in an Asian population. Cancer Causes Control. 2010;21:771-6. [PMID: 20084542]
- Gallagher RP, Hill GB, Bajdik CD, Coldman AJ, Fincham S, McLean DI, et al. Sunlight exposure, pigmentation factors, and risk of nonmelanocytic skin cancer. II. Squamous cell carcinoma. Arch Dermatol. 1995;131:164-9. [PMID: 7857112]
- Gallagher RP, Hill GB, Bajdik CD, Fincham S, Coldman AJ, McLean DI, et al. Sunlight exposure, pigmentary factors, and risk of nonmelanocytic skin cancer. I. Basal cell carcinoma. Arch Dermatol. 1995;131:157-63. [PMID: 7857111]
- Vlajinac HD, Adanja BJ, Lazar ZF, Bogavac AN, Bjekic, MD, Marinkovic JM, et al. Risk factors for basal cell carcinoma. Acta Oncol. 2000;39:611-6. [PMID: 11093369]
- Veierød MB, Adami HO, Lund E, Armstrong BK, Weiderpass E. Sun and solarium exposure and melanoma risk: effects of age, pigmentary characteristics, and nevi. Cancer Epidemiol Biomarkers Prev. 2010;19:111-20. [PMID: 20056629]
- Berwick M, Begg CB, Fine JA, Roush GC, Barnhill RL. Screening for cutaneous melanoma by skin self-examination. J Natl Cancer Inst. 1996;88:17-23. [PMID: 8847720]
- Fargnoli MC, Piccolo D, Altobelli E, Formicone F, Chimenti S, Peris K. Constitutional and environmental risk factors for cutaneous melanoma in an Italian population. A case-control study. Melanoma Res. 2004;14:151-7. [PMID: 15057047]
- Green AC, O’Rourke MG. Cutaneous malignant melanoma in association with other skin cancers. J Natl Cancer Inst. 1985;74:977-80. [PMID: 3858585]
- Holly EA, Aston DA, Cress RD, Ahn DK, Kristiansen JJ. Cutaneous melanoma in women. I. Exposure to sunlight, ability to tan, and other risk factors related to ultraviolet light. Am J Epidemiol. 1995;141:923-33. [PMID: 7741122]
- Gallagher RP, Elwood JM, Hill GB. Risk factors for cutaneous malignant melanoma: the Western Canada Melanoma Study. Recent Results Cancer Res. 1986;102:38-55. [PMID: 3738186]
- Zanetti R, Franceschi S, Rosso S, Colonna S, Bidoli E. Cutaneous melanoma and sunburns in childhood in a southern European population. Eur J Cancer. 1992;28A:1172-6. [PMID: 1627390]
- Le Marchand L, Saltzman BS, Hankin JH, Wilkens LR, Franke AA, Morris SJ, et al. Sun exposure, diet, and melanoma in Hawaii Caucasians. Am J Epidemiol. 2006;164:232-45. [PMID: 16524953]
- Osterlind A, Tucker MA, Stone BJ, Jensen OM. The Danish case-control study of cutaneous malignant melanoma. II. Importance of UV-light exposure. Int J Cancer. 1988;42:319-24. [PMID: 3417359]
- Parr CL, Hjartåker A, Laake P, Lund E, Veierød MB. Recall bias in melanoma risk factors and measurement error effects: a nested case-control study within the Norwegian Women and Cancer Study. Am J Epidemiol. 2009;169:257-66. [PMID: 19011116]
- Walter SD, King WD, Marrett LD. Association of cutaneous malignant melanoma with intermittent exposure to ultraviolet radiation: results of a case-control study in Ontario, Canada. Int J Epidemiol. 1999;28:418-27. [PMID: 10405843]
- Weinstock MA, Colditz GA, Willett WC, Stampfer MJ, Bronstein BR, Mihm MC Jr, et al. Melanoma and the sun: the effect of swimsuits and a “healthy” tan on the risk of nonfamilial malignant melanoma in women. Am J Epidemiol. 1991;134:462-70. [PMID: 1897502]
- Westerdahl J, Olsson H, Ingvar C. At what age do sunburn episodes play a crucial role for the development of malignant melanoma. Eur J Cancer. 1994;30A:1647-54. [PMID: 7833138]
- Garbe C, Krüger S, Stadler R, Guggenmoos-Holzmann I, Orfanos CE. Markers and relative risk in a German population for developing malignant melanoma. Int J Dermatol. 1989;28:517-23. [PMID: 2583889]
- Nagore E, Hueso L, Botella-Estrada R, Alfaro-Rubio A, Serna I, Guallar J et al. Smoking, sun exposure, number of nevi and previous neoplasias are risk factors for melanoma in older patients (60 years and over). J Eur Acad Dermatol Venereol. 2010;24:50-7. [PMID: 19563496]
- Tabenkin H, Tamir A, Sperber AD, Shapira M, Shvartzman P. A case-control study of malignant melanoma in Israeli kibbutzim. Isr Med Assoc J. 1999;1:154-7. [PMID: 10731323]
- White E, Kirkpatrick CS, Lee JA. Case-control study of malignant melanoma in Washington State. I. Constitutional factors and sun exposure. Am J Epidemiol. 1994;139:857-68. [PMID: 8166136]
- Shors AR, Solomon C, McTiernan A, White E. Melanoma risk in relation to height, weight, and exercise (United States). Cancer Causes Control. 2001;12:599-606. [PMID: 11552707]
- Karagas MR, Stannard VA, Mott LA, Slattery MJ, Spencer SK, Weinstock MA. Use of tanning devices and risk of basal cell and squamous cell skin cancers. J Natl Cancer Inst. 2002;94:224-6. [PMID: 11830612]
- Clough-Gorr KM, Titus-Ernstoff L, Perry AE, Spencer SK, Ernstoff MS. Exposure to sunlamps, tanning beds, and melanoma risk. Cancer Causes Control. 2008;19:659-69. [PMID: 18273687]
- Bataille V, Boniol M, De Vries E, Severi G, Brandberg Y, Sasieni P, et al. A multicentre epidemiological study on sunbed use and cutaneous melanoma in Europe. Eur J Cancer. 2005;41:2141-9. [PMID: 16125927]
- Green A, Williams G, Neale R, Hart V, Leslie D, Parsons P, et al. Daily sunscreen application and betacarotene supplementation in prevention of basal-cell and squamous-cell carcinomas of the skin: a randomised controlled trial. Lancet. 1999;354:723-9. [PMID: 10475183]
- Cho E, Rosner BA, Feskanich D, Colditz GA. Risk factors and individual probabilities of melanoma for whites. J Clin Oncol. 2005;23:2669-75. [PMID: 15837981]
- Green A, Battistutta D, Hart V, Leslie D, Marks G, Williams G, et al. The Nambour Skin Cancer and Actinic Eye Disease Prevention Trial: design and baseline characteristics of participants. Control Clin Trials. 1994;15:512-22. [PMID: 7851112]
- Pandeya N, Purdie DM, Green A, Williams G. Repeated occurrence of basal cell carcinoma of the skin and multifailure survival analysis: follow-up data from the Nambour Skin Cancer Prevention Trial. Am J Epidemiol. 2005;161:748-54. [PMID: 15800267]
- van der Pols JC, Williams GM, Pandeya N, Logan V, Green AC. Prolonged prevention of squamous cell carcinoma of the skin by regular sunscreen use. Cancer Epidemiol Biomarkers Prev. 2006;15:2546-8. [PMID: 17132769]
- Chen YT, Dubrow R, Zheng T, Barnhill RL, Fine J, Berwick M. Sunlamp use and the risk of cutaneous malignant melanoma: a population-based case-control study in Connecticut, USA. Int J Epidemiol. 1998;27:758-65. [PMID: 9839730]
- Kricker A, Armstrong BK, English DR, Heenan PJ. Does intermittent sun exposure cause basal cell carcinoma? a case-control study in Western Australia. Int J Cancer. 1995;60:489-94. [PMID: 7829262]
- Milne E, Simpson JA, Johnston R, Giles-Corti B, English DR. Time spent outdoors at midday and children’s body mass index. Am J Public Health. 2007;97:306-10. [PMID: 17194858]
- Autier P, Dorá JF, Négrier S, Liénard D, Panizzon R, Lejeune FJ, et al. Sunscreen use and duration of sun exposure: a double-blind, randomized trial. J Natl Cancer Inst. 1999;91:1304-9. [PMID: 10433619]
- Autier P, Doré JF, Reis AC, Grivegnée A, Ollivaud L, Truchetet F, et al. Sunscreen use and intentional exposure to ultraviolet A and B radiation: a double blind randomized trial using personal dosimeters. Br J Cancer. 2000;83:1243-8. [PMID: 11027441]
- Dupuy A, Dunant A, Grob JJ; Réseau d’Epidémiologie en Dermatologie. Randomized controlled trial testing the impact of high-protection sunscreens on sun-exposure behavior. Arch Dermatol. 2005;141:950-6. [PMID: 16103322]
- Marks R, Foley PA, Jolley D, Knight KR, Harrison J, Thompson SC. The effect of regular sunscreen use on vitamin D levels in an Australian population. Results of a randomized controlled trial. Arch Dermatol. 1995;131:415-21. [PMID: 7726582]
- Brot C, Vestergaard P, Kolthoff N, Gram J, Hermann AP, Sørensen OH. Vitamin D status and its adequacy in healthy Danish perimenopausal women: relationships to dietary intake, sun exposure and serum parathyroid hormone. Br J Nutr. 2001;86(Suppl 1):S97-103. [PMID: 11520426]
- John EM, Schwartz GG, Dreon DM, Koo J. Vitamin D and breast cancer risk: the NHANES I Epidemiologic follow-up study, 1971-1975 to 1992. National Health and Nutrition Examination Survey. Cancer Epidemiol Biomarkers Prev. 1999;8:399-406. [PMID: 10350434]
- Kampman E, Slattery ML, Caan B, Potter JD. Calcium, vitamin D, sunshine exposure, dairy products and colon cancer risk (United States). Cancer Causes Control. 2000;11:459-66. [PMID: 10877339]
- Hughes AM, Armstrong BK, Vajdic CM, Turner J, Grulich A, Fritschi L, et al. Pigmentary characteristics, sun sensitivity and non-Hodgkin lymphoma. Int J Cancer. 2004;110:429-34. [PMID: 15095310]
- Hughes AM, Armstrong BK, Vajdic CM, Turner J, Grulich AE, Fritschi L, et al. Sun exposure may protect against non-Hodgkin lymphoma: a case-control study. Int J Cancer. 2004;112:865-71. [PMID: 15386383]
- Smedby KE, Hjalgrim H, Melbye M, Torrång A, Rostgaard K, Munksgaard L, et al. Ultraviolet radiation exposure and risk of malignant lymphomas. J Natl Cancer Inst. 2005;97:199-209. [PMID: 15687363]
- John EM, Schwartz GG, Koo J, Van Den Berg D, Ingles SA. Sun exposure, vitamin D receptor gene polymorphisms, and risk of advanced prostate cancer. Cancer Res. 2005;65:5470-9. [PMID: 15958597]
- Hartge P, Lim U, Freedman DM, Colt JS, Cerhan JR, Cozen W, et al. Ultraviolet radiation, dietary vitamin D, and risk of non-Hodgkin lymphoma (United States). Cancer Causes Control. 2006;17:1045-52. [PMID: 16933055]
- John EM, Schwartz GG, Koo J, Wang W, Ingles SA. Sun exposure, vitamin D receptor gene polymorphisms, and breast cancer risk in a multiethnic population. Am J Epidemiol. 2007;166:1409-19. [PMID: 17934201]
- Patrick K, Calfas KJ, Norman GJ, Zabinski MF, Sallis JF, Rupp J, et al. Randomized controlled trial of a primary care and home-based intervention for physical activity and nutrition behaviors: PACE+ for adolescents. Arch Pediatr Adolesc Med. 2006;160:128-36. [PMID: 16461867]
- Rosenberg DE, Norman GJ, Sallis JF, Calfas KJ, Patrick K. Covariation of adolescent physical activity and dietary behaviors over 12 months. J Adolesc Health. 2007;41:472-8. [PMID: 17950167]
- Autier P, Severi G, Doré JF. Betacarotene and sunscreen use [Letter]. Lancet. 1999;354:2163-4. [PMID: 10609840]
- Gallagher RP, Rivers JK, Lee TK, Bajdik CD, McLean DI, Coldman AJ. Broad-spectrum sunscreen use and the development of new nevi in white children: A randomized controlled trial. JAMA. 2000;283:2955-60. [PMID: 10865273]
- Bauer J, Büttner P, Wiecker TS, Luther H, Garbe C. Interventional study in 1,232 young German children to prevent the development of melanocytic nevi failed to change sun exposure and sun protective behavior. Int J Cancer. 2005;116:755-61. [PMID: 15849749]
- Burgaz A, Akesson A, Michaëulsson K, Wolk A. 25-hydroxyvitamin D accumulation during summer in elderly women at latitude 60 degrees N. J Intern Med. 2009;266:476-83. [PMID: 19570054]
- Glanz K, Yaroch AL, Dancel M, Saraiya M, Crane LA, Buller DB, et al. Measures of sun exposure and sun protection practices for behavioral and epidemiologic research. Arch Dermatol. 2008;144:217-22. [PMID: 18283179]
- Lazovich D, Stryker JE, Mayer JA, Hillhouse J, Dennis LK, Pichon L, et al. Measuring nonsolar tanning behavior: indoor and sunless tanning. Arch Dermatol. 2008;144:225-30. [PMID: 18283180]
- IARC Working Group Reports. Vitamin D and Cancer. vol. 5. Lyon, France: International Agency for Research on Cancer; 2008.
- Chang YM, Barrett JH, Bishop DT, Armstrong BK, Bataille V, Bergman W, et al. Sun exposure and melanoma risk at different latitudes: a pooled analysis of 5700 cases and 7216 controls. Int J Epidemiol. 2009;38:814-30. [PMID: 19359257]
- Worswick SD, Cockburn M, Peng D. Measurement of ultraviolet exposure in epidemiological studies of skin and skin cancers. Photochem Photobiol. 2008;84:1462-72. [PMID: 18494760]
- Bajdik CD, Gallagher RP, Astrakianakis G, Hill GB, Fincham S, McLean DI. Non-solar ultraviolet radiation and the risk of basal and squamous cell skin cancer. Br J Cancer. 1996;73:1612-4. [PMID: 8664139]
- English DR, Armstrong BK, Kricker A, Winter MG, Heenan PJ, Randell PL. Case-control study of sun exposure and squamous cell carcinoma of the skin. Int J Cancer. 1998;77:347-53. [PMID: 9663594]
- Lea CS, Scotto JA, Buffler PA, Fine J, Barnhill RL, Berwick M. Ambient UVB and melanoma risk in the United States: a case-control analysis. Ann Epidemiol. 2007;17:447-53. [PMID: 17395487]
- Chen YT, Dubrow R, Holford TR, Zheng T, Barnhill RL, Fine J, et al. Malignant melanoma risk factors by anatomic site: a case-control study and polychotomous logistic regression analysis. Int J Cancer. 1996;67:636-43. [PMID: 8782651]
- Elwood JM, Gallagher RP, Hill GB, Pearson JC. Cutaneous melanoma in relation to intermittent and constant sun exposure—the Western Canada Melanoma Study. Int J Cancer. 1985;35:427-33. [PMID: 3988369]
- Elwood JM, Gallagher RP, Hill GB, Spinelli JJ, Pearson JC, Threlfall W. Pigmentation and skin reaction to sun as risk factors for cutaneous melanoma: Western Canada Melanoma Study. Br Med J. 1984;288:99-102. [PMID: 6419839]
- Green A, Bain C, McLennan R, Siskind V. Risk factors for cutaneous melanoma in Queensland. In: Gallagher RP, ed. Epidemiology of Malignant Melanoma. Heidelberg: Springer-Verlag; 1986:76-97.
- Osterlind A, Tucker MA, Hou-Jensen K, Stone BJ, Engholm G, Jensen OM. The Danish case-control study of cutaneous malignant melanoma. I. Importance of host factors. Int J Cancer. 1988;42:200-6. [PMID: 3403065]
- Solomon CC, White E, Kristal AR, Vaughan T. Melanoma and lifetime UV radiation. Cancer Causes Control. 2004;15:893-902. [PMID: 15577291]
- Veierød MB, Weiderpass E, Thörn M, Hansson J, Lund E, Armstrong B, et al. A prospective study of pigmentation, sun exposure, and risk of cutaneous malignant melanoma in women. J Natl Cancer Inst. 2003;95:1530-8. [PMID: 14559875]
- Walter SD, Marrett LD, From L, Hertzman C, Shannon HS, Roy P. The association of cutaneous malignant melanoma with the use of sunbeds and sunlamps. Am J Epidemiol. 1990;131:232-43. [PMID: 2296977]
- Westerdahl J, Olsson H, Måsbäck A, Ingvar C, Jonsson N, Brandt L, et al. Use of sunbeds or sunlamps and malignant melanoma in southern Sweden. Am J Epidemiol. 1994;140:691-9. [PMID: 7942771]