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Sun protection is recommended for skin cancer prevention, yet little is known about the role of sun protection on vitamin D levels. Our aim was to investigate the relationship between different types of sun protective behaviors and serum 25(OH)D levels in the general US population.
Cross-sectional, nationally representative survey of 5,920 adults aged 18–60 years in the US National Health and Nutrition Examination Survey 2003–2006. We analyzed questionnaire responses on sun protective behaviors: staying in the shade, wearing long sleeves, wearing a hat, using sunscreen and SPF level. Analyses were adjusted for multiple confounders of 25(OH)D levels and stratified by race. Our primary outcome measures were serum 25(OH)D levels (ng/ml) measured by radioimmunoassay and vitamin D deficiency, defined as 25(OH)D levels <20 ng/ml.
Staying in the shade and wearing long sleeves were significantly associated with lower 25(OH)D levels. Subjects who reported frequent use of shade on a sunny day had −3.5 ng/ml (ptrend < 0.001) lower 25(OH)D levels compared to subjects who reported rare use. Subjects who reported frequent use of long sleeves had −2.2 ng/ml (ptrend = 0.001) lower 25(OH)D levels. These associations were strongest for whites, and did not reach statistical significance among Hispanics or blacks. White participants who reported frequently staying in the shade or wearing long sleeves had double the odds of vitamin D deficiency compared with those who rarely did so. Neither wearing a hat nor using sunscreen was associated with low 25(OH)D levels or vitamin D deficiency.
White individuals who protect themselves from the sun by seeking shade or wearing long sleeves may have lower 25(OH)D levels and be at risk for vitamin D deficiency. Frequent sunscreen use does not appear to be linked to vitamin D deficiency in this population.
Sun protection is widely recommended to prevent both melanoma and non-melanoma skin cancer. The World Health Organization , the American Academy of Dermatology  and the American Medical Association  advise individuals to wear protective clothing, including hat and sunglasses, seek shade during midday hours, and use broad-spectrum sunscreen SPF 30 + liberally.
However, recent findings on the benefits of vitamin D [4–6] have led to concerns that rigorous sun protection may negatively impact health by reducing vitamin D to suboptimal levels [7–9]. Vitamin D deficiency has been associated with an increased risk of autoimmune disease , fractures , cancer  and cardiovascular disease [12, 13] in observational studies. Prior studies within the National Health and Nutrition Examination Survey (NHANES) suggest a significant association between low serum vitamin D levels and all-cause mortality . However, not all studies on vitamin D are consistent, and controversy remains on this issue . Several systematic reviews and randomized controlled trials have not found supplementation to be effective in fracture prevention [15–17] or colorectal cancer prevention [18, 19]. Yet a meta-analysis of studies on total mortality by vitamin D use in RCTs indicates a lower risk in those who were randomized to vitamin D .
In a recent position statement, the American Academy of Dermatology recommends oral vitamin D supplementation especially for those patients that adhere to strict photo-protection . Yet, there are limited studies addressing the relationship between specific sun protective behaviors and vitamin D levels in the general population. Sunscreen use reduces vitamin D production in strictly controlled conditions , but it is unclear whether typical usage results in similar deficiencies . Even less is known about the impact that other recommended sun protective behaviors (e.g., staying in the shade, wearing long sleeves, wearing a hat) have on vitamin D levels, or how these factors vary with race. Furthermore, data on the prevalence of different sun protection behaviors in the US population is limited, especially among nonwhites.
The goal of this study is to assess the relationship between reported use of different types of sun protection and 25(OH)D levels in Americans of different races.
The National Health and Nutrition Examination Survey (NHANES) is a biennial, nationally representative, cross-sectional survey including data collected via household interviews and standardized physical examinations conducted in specially equipped mobile examination centers . Self-reported sun protection information was collected on only two NHANES cycles 2003–2004 and 2005–2006. We therefore restricted our analysis to adult participants during these years. Between 2003 and 2006, 20,470 individuals were surveyed by NHANES. The dermatology questionnaire was administered to a subset of NHANES participants (n = 6,549). Of these, 5,920 also had serum 25(OH)D measurements. Participants with missing data on 25(OH)D or covariates were excluded (n = 629).
As part of the dermatology questionnaire, participants were asked the following questions: “When you go outside on a very sunny day, for more than one hour, how often do you: (a) stay in the shade? (b) wear a hat that shades your face ears and neck? (c) wear a long sleeved shirt? (d) use sunscreen?”. Possible answers included: never, rarely, sometimes, most of the time, or always. In order to have intuitive categories and stable estimates, we collapsed these responses into three prespecified frequency categories: rare (never or rarely), moderate (sometimes) and frequent (most of the time or always). Overall, sun protection was assessed using an additive score from the 4 behaviors (staying in the shade, wearing a long sleeved shirt, wearing a hat, using sunscreen). Each of these behaviors was scored 1, 2 or 3 for rare, moderate or frequent use, respectively. The sum resulted in an overall sun protection score ranging from 4 to 12 and this score was subsequently divided into rare (4–6), moderate (7–9) or frequent (10–12).
Subject self-report of sun sensitivity was assessed based on the following question: “If after several months of not being in the sun, you then went out in the sun without sunscreen or protective clothing for a half hour, which one of these would happen to your skin?” Possible responses included (a) severe sunburn with blisters, (b) severe sunburn for a few days with peeling, (c) mild burn with some tanning, (d) turn darker without a sunburn or (e) nothing would happen in half an hour. Due to low frequency, categories (a) and (b) were combined in these analyses. Sun exposure was assessed by the total number of sunburns reported by each subject based on the following question: “How many times in the past year have you had a sunburn?” Numerical responses were categorized into 4 groups: 0, 1, 2, or 3 + sunburns.
A smaller, random subset of NHANES 2003–2004 participants (n = 2,900) also had standardized photographs of selected parts of the skin taken during physical examination as previously described . Two independent dermatologists reviewed the photographs in order to assign a skin type on a scale of 1–6 according to the following scale: “1: pale white skin, 2: white skin, 3: light brown skin, 4: moderate brown skin, 5: dark brown skin, 6: deeply pigmented dark brown to black skin .” Dermatologist-assessed skin-type scores were highly correlated with subject self-report of sun sensitivity (r = 0.85, p < 0.001). Thus, we used subject sun sensitivity in our models as this was recorded in more subjects (n = 5,290).
Detailed descriptions of blood collection and processing are provided in the NHANES Laboratory/Medical Technologists Procedures Manual. Serum 25(OH)D was measured by radioimmunoassay (RIA) (DiaSorin, Stillwater MN)  by the National Center for Environmental Health, Centers for Disease Control (CDC). Issues pertaining to serum 25(OH)D assay variability after 2000 have been addressed by the CDC  and were found by Looker et al.  to have a minimal effect on analyses from this time period. NHANES blood samples were drawn in the summer season for Northern regions and in the winter for Southern regions. This inherent season-geography design was implemented to maximize subject participation in the mobile examination centers for blood collection and laboratory measurements as previously described . We stratified by season and found that sun protective behaviors had a greater effect on lowering 25OHD levels in the summer as would be expected since participants are more likely to practice sun protection in the summer. The interaction between sun protective habits and season was significant (p < 0.05). Serum PTH was measured using an electrochemiluminescent process, Elecsys 1010 autoanalyzer (Roche Diagnostics, Mannheim, Germany). Three levels of control specimens were used to assess the quality of each serum PTH run. Coefficients of variation for serum PTH remained 10% throughout the study period.
All statistical analyses were adjusted for weighted sampling technique (STATA 10.0 SVY commands) making results applicable to the entire US population. Linear regression models were adjusted for variables previously reported to affect 25(OH)D levels: age, BMI, gender, season of blood collection (summer vs. winter), physical activity compared to peers (more, same, less), multivitamin or vitamin D supplement use (yes/no), sun sensitivity, number of sunburns, milk intake in the past week (never, rarely, varied, sometimes, often), and socioeconomic status as assessed by education (highest level of schooling or degree) and family income (in $5,000 increments). All analyses were stratified by ethnicity according to these categories: white, black or Hispanic (Mexican–American or other Hispanic). Other ethnicities (including Asian, Native American, Pacific Islander, multi-racial or “other”) were analyzed separately, but because of small numbers and overall similar results, data is not presented here. We used a Bonferroni correction to adjust for multiple comparisons.
Logistic regression was performed using 20 ng/ml as the cutoff for vitamin D deficiency. We chose this cutoff because this is the level at which health effects have been noted and also the level at which parathyroid hormone (PTH) levels begin to rise  and based on the recommendations of the recent institute of medicine report . However, since a single cutoff for vitamin D deficiency is not established, we performed a sensitivity analysis repeating our analyses using 10, 15 and 30 ng/ml as alternative cutoffs. Because our results did not change appreciably, we present data using the 20 ng/ml definition. Given the 20 comparisons made, only p values less than 0.0025 are considered statistically significant after adjustments for multiple comparisons.
A total of 5,367 NHANES participants with 25(OH)D measurements and sun protective information were included in this analysis. The prevalence of sun protective behaviors for each racial group is shown in Fig. 1. More than half of all Americans frequently use at least one form of sun protection, although the type varies by race (Fig. 1). The most striking difference in sun protective behaviors was sunscreen usage. The majority of whites reported moderate to frequent usage of sunscreen (56%), while 31% of Hispanics and only 14% of blacks reported the same usage. As expected, we found that sunscreen was more frequently used in subjects who were more likely to sunburn. Of whites who reported frequent sunscreen use, 70% reported prior sunburn. In contrast, frequently staying in the shade was more common in blacks (43%) and Hispanics (37%) than in whites (25%).
Table 1 reports unadjusted mean levels of 25(OH)D for each racial group according to usage of sun protective behaviors. As previously reported, 25(OH)D levels were strongly related to race, with blacks having the lowest baseline levels . In unadjusted analyses, frequent use of shade and long sleeves were associated with 4–6 ng/ml decrease in 25(OH)D compared to rare use in whites. There was no statistically significant association between vitamin D and use of any sun protective behavior in Hispanics or blacks. Frequent sunscreen use was associated with higher mean serum 25(OH)D levels in all races. Figure 2 shows the prevalence of sun protective behaviors in the highest and lowest groups of 25(OH)D levels. Moderate–frequent use of shade and long sleeves was more common in subjects with the lowest 25(OH)D levels compared to subjects with the highest levels (p < 0.01). Use of sunscreens were similar in the lowest and highest 25(OH)D groups.
Table 2 presents results from multivariate analyses, adjusted for known covariates that affect 25(OH)D levels: BMI, age, gender, season, vitamin D supplement use, physical activity, milk consumption, subject sun sensitivity, number of sunburns, income and education. For all races combined, overall sun protection, staying in the shade and wearing long sleeves were significantly associated with lower 25(OH)D levels, while frequency of wearing hats or sunscreen were not. Subjects who reported frequent use of shade on a sunny day had −3.5 ng/ml (95% CI: −4.2, −2.8, ptrend < 0.001) lower 25(OH)D levels compared to subjects who reported rare use. Subjects who reported frequent use of long sleeves had −2.2 ng/ml (95% CI: −3.5, 1.0, ptrend < 0.001) lower 25(OH)D levels. This association appeared to be primarily driven by the effect among white participants.
The overall prevalence of vitamin D deficiency was approximately 40%, although this was higher among participants who frequently stayed in the shade (53%) and wore long sleeves (55%), and lower for participants who frequently used sunscreen (32%). Table 3 presents the association of each sun protective behavior with the odds of vitamin D deficiency defined as 25(OH)D levels ≤20 ng/ml. White participants who reported frequently staying in the shade or wearing long sleeves had double the odds of vitamin D deficiency compared with those who rarely did so (Shade OR = 2.16, 95% CI: 1.41, 3.32, ptrend = 0.001; Long sleeves OR = 2.11, 95% CI: 1.48, 3.00, ptrend=0.02) (Table 3, Fig. 3). The odds of vitamin D deficiency were 44% higher in whites who reported frequent overall sun protection compared with whites who reported rare sun protection (ptrend = 0.06, Table 3). These associations persisted in a sensitivity analysis using different cutoffs for vitamin D deficiency or insufficiency (e.g., ≤10, ≤15, or ≤30 ng/ml). Use of sunscreen was not associated with vitamin D deficiency even when analysis was restricted to subjects using sunscreens with SPF > 15 or SPF > 30.
Additional analysis on the relationship between sun protective behaviors and PTH levels showed that shade use, long sleeve use, and overall sun protection was associated with commensurate increases in PTH levels (Supplemental Table 1). The association between sun protective behaviors and 25(OH)D levels was not significantly modified by age or gender. When stratified by season, frequent use of shade and long sleeves was more predictive of lower 25(OH)D levels in the summer compared with the winter. In all multivariate analyses, higher BMI and older age were significantly associated with lower 25(OH)D, and frequent milk consumption and vitamin supplementation with higher levels, consistent with previous reports . Sensitivity analysis using dermatologist-assessed skin type in the multivariable model did not change our results.
To our knowledge, this is the first large, nationally representative, population-based study to quantify the differential association between sun protective clothing, shade use and sunscreen and 25(OH)D levels. Staying in the shade and wearing long sleeves were significantly associated with lower 25(OH)D levels and vitamin D deficiency, especially in whites, but wearing a hat and using sunscreen use were not. These results persisted despite adjustment for established confounders of serum vitamin D, including milk intake and supplement use, season of blood collection, race and subject sensitivity to sun. The relationships between sun protective behaviors and lower 25(OH)D levels were much weaker among Hispanics and blacks, possibly because of the inherent natural sun protective effect of melanin in darkly pigmented skin. Since the natural pigment in darker skin is a potent UV blocker, any additional sun protection above and beyond this may have a minimal relative impact. Alternatively, the smaller number of nonwhite participants in our study may also explain why these associations did not reach statistical significance.
Our results are consistent with one prior study suggesting an association between overall sun protection and lower 25(OH)D levels  and a recent study on lower vitamin D levels in skin cancer patients . Our findings add to the literature by providing further detail on the specific types of sun protective behaviors that impact vitamin D, and the racial groups in which they are significant. Our findings on sunscreen use are also consistent with prior studies in Australian whites showing that sunscreen as used by the general population does not cause lower 25(OH)D levels [22, 33, 34]. Despite the fact that sunscreens can block UV-induced vitamin D synthesis in strictly controlled conditions , we found that frequent sunscreen use was not related to lower 25(OH)D levels. This might be explained by confounding due to application of sunscreen prior to intentional prolonged sun exposure. This theory is supported by several studies showing that sunscreens are used as tanning aids , and are often associated with prolonged sun exposure  and sunburns .
Few studies to date have examined the prevalence of sun protective behaviors among blacks [38, 39]. Our findings are consistent with these studies, showing that blacks report infrequent use of sunscreen, and more frequent shade-seeking behavior. Vitamin D deficiency is very common in this group, and has been suggested as one possible explanation for racial disparities in health [40, 41]. Therefore, even borderline trends toward lower vitamin D levels associated with sun protection in blacks may be important clinically.
The magnitude of the 2–4 ng/ml difference in 25(OH)D associated with frequent shade and long sleeve use is modest. A possible explanation for this effect size, is that synthesis of pre-vitamin D in skin reaches a maximum after about 1/3 minimal erythemal dose (MED) , so even while participants may consciously be avoiding sun exposure, most will still get sufficient UV for some amount of vitamin D synthesis. Although this 2–4 ng/ml effect size is modest, it approximates the increase in 25(OH)D levels achieved with 200–400 IUs of oral vitamin D supplementation  and is comparable with the increases achieved in some vitamin D supplementation trials that found health benefits . It is also important to note that this cross-sectional measurement may be a better reflection of long-term vitamin D status compared with short-term intervention trials. Furthermore, small differences at the population level may reflect much larger health benefits for certain individuals within that population (e.g., people with low baseline serum vitamin D or those with additional risk factors for chronic disease).
Since this is a cross-sectional study, we are unable to confirm a causal relationship between sun protective behaviors and vitamin D levels. We rely on self-report of sun protective habits and did not directly observe these behaviors. However, the validity of self-reported sun protection has been shown to be adequate, with correlations between self-reporting and observation ranging from 0.51 to 0.83 [44, 45]. Another potential limitation is the single measurement of 25(OH)D, which may have been affected by assay variations over time. Both the CDC and prior investigators have noted that this is likely to have minimal effects on analyses of this particular dataset . However, the same sun protective behaviors (shade, long sleeve use) that were associated with lower 25(OH)D levels were also associated with commensurate increases in PTH levels. Another potential limitation to our study is the NHANES survey structure where southern regions were sampled in the winter, while northern regions in the summer, may not give fully representative vitamin D levels over a year; because sun protection may also vary by season this is a potential source of bias. Nonetheless, this is unlikely to lead to systematic bias in our results, and we addressed this by controlling for season. Also, we acknowledge that the three racial groups used in this analysis (white, Hispanic, black) each include a wide range of skin pigmentation; however, all multivariate analyses were adjusted for subject sensitivity to sun to additionally control for confounding by skin pigmentation. Similar results were found in analysis of a subset of participants adjusting for dermatologist-assessed skin types. Finally, a major limitation is that we did not have any direct quantification of sun exposure habits and cannot capture the multiple facets of sun exposure behaviors including the desire to tan and cultural differences in ideal skin color. In an attempt to control for some of these factors, we adjusted for subject self-report of sun sensitivity, physical activity, and number of sunburns in the past year and stratified the results by racial groups. As this is an observational study, our findings may be confounded by unmeasured variables such as general attitudes to health and prevention that may influence both sun protection and vitamin D levels. We attempted to control for these factors by adjusting for income and education, which may be proxies for healthy behaviors.
Although sunscreens are a widely used method of sun protection in the United States, our results demonstrate that in a large representative sample of US adults, typical sunscreen use is unlikely to lower vitamin D levels. In whites, frequently staying in the shade or wearing long sleeves on a sunny day is associated with lower 25(OH)D levels and increased odds for vitamin D deficiency. White individuals who protect themselves from the sun by seeking shade or wearing long sleeves may require higher oral intake of vitamin D than the currently recommended 200–400 IU. In this study, we did not detect a statistically significant association between sun protective behaviors and lower 25(OH)D levels in Hispanics or blacks. Future longitudinal, prospective studies and randomized trials are required to further elucidate the magnitude of the effect of sun protective behaviors on vitamin D levels.
The authors would like to thank Steven L. Chang MD, and Ervin Epstein MD for helpful discussions.
Electronic supplementary material The online version of this article (doi:10.1007/s10552-011-9862-0) contains supplementary material, which is available to authorized users.
Eleni Linos, Department of Dermatology, Stanford University School of Medicine, Pavilion B 2nd Floor, 450 Broadway St, Redwood City, CA 94063, USA.
Elizabeth Keiser, Department of Dermatology, Stanford University School of Medicine, Pavilion B 2nd Floor, 450 Broadway St, Redwood City, CA 94063, USA.
Matthew Kanzler, Department of Dermatology, Stanford University School of Medicine, Pavilion B 2nd Floor, 450 Broadway St, Redwood City, CA 94063, USA. Division of Dermatology, Santa Clara Valley Medical Center, San Jose, CA, USA.
Kristin L. Sainani, Department of Health Research and Policy, Stanford University School of Medicine, Stanford, CA 94305, USA.
Wayne Lee, Department of Dermatology, Stanford University School of Medicine, Pavilion B 2nd Floor, 450 Broadway St, Redwood City, CA 94063, USA.
Eric Vittinghoff, Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, CA, USA.
Mary-Margaret Chren, Department of Dermatology, University of California San Francisco, San Francisco, CA, USA.
Jean Y. Tang, Department of Dermatology, Stanford University School of Medicine, Pavilion B 2nd Floor, 450 Broadway St, Redwood City, CA 94063, USA.