B. A. Gilchrest, MD
Department of Dermatology, Boston University School of Medicine, Boston, MA, USA
Ultraviolet (UV) radiation is a carcinogen that also compromises skin appearance and function. Since the UV action spectra for DNA damage, skin cancer, and vitamin D photosynthesis are identical, and vitamin D is readily available from oral supplements, why has sun protection become controversial? First, the media and, apparently, some researchers are hungry for a new message. They have also drawn attention to the emerging evidence of possible vitamin D benefits other than for bone health. Second, the controversy is fueled by a powerful special interest group: the tanning industry. This industry does not target the frail elderly or inner-city ethnic minorities, which are the groups at greatest risk of vitamin D deficiency, but rather fair-skinned teenagers and young adults, who are at highest risk of UV photodamage. Third, evolution does not keep pace with civilization. When nature gave humans the appealing capacity for cutaneous vitamin D photosynthesis, life expectancy was less than 40 years of age; long-term photodamage was not a concern, and vitamin D deficiency, with its resulting skeletal abnormalities (rickets), was likely to be fatal in early life. This article briefly reviews the “pseudo-controversy”, as well as the data supporting a revision of the recommendations for vitamin D supplementation. It concludes with a suggested message for patients, many of whom are understandably confused by recent media coverage of the topic.
vitamin D, photosynthesis, sun protection
The media and certain elements within the biomedical research community have created a “controversy” regarding the allegedly conflicting goals of skin cancer prevention through sun protection on the one hand, and achieving optimal vitamin D homeostasis on the other. I will attempt to distinguish this pseudo-controversy from the true controversy surrounding the rather poorly documented health benefits of very high vitamin D levels, however achieved.
The somewhat elusive basis of the pseudo-controversy lies in the often unstated assumption that vitamin D levels, specifically, levels of the inactive prehormone 25-hydroxyvitamin D [25(OH)D], which is measured in serum, are best achieved from increased ultraviolet (UV) exposure to enhance photosynthesis of vitamin D within the irradiated epidermis. This assumption has framed discussions in the popular press and on the internet, even though all intervention studies that suggest a benefit for increasing the conventional “normal” or “sufficient” 25(OH)D level in specific population groups have examined the effect of oral vitamin D supplements, not increased exposure to sun or other UV sources.1
This formulation of the debate also fails to acknowledge that the major motivation for sun exposure in the population at large is not for improved general health, but rather, it is to attain the cosmetic and lifestyle goal of tanning, at least for people genetically capable of tanning. Thus, reports continue on the “debate” between professional groups with primary interests in skin health versus those who specialize in endocrinologic health, even though often no such debate exists. These deliberations can create confusion among the general public regarding recommended health behaviors.
In recent years, numerous newspaper reporters, freelance journalists, and television news anchors have reported on a “medical controversy” that pits the unwanted effects of acute sunburn, photoaging, and skin cancer against both well-established and postulated benefits of vitamin D photosynthesis. Simplistically stated, these articles and reports ask if the public should maximize vitamin D levels (measured as the biologically inactive storage form of 25(OH)D in serum)2 through intentional UV exposure to reduce their risk of internal cancers, hypertension, diabetes, multiple sclerosis, and a litany of other disorders that some attribute to “insufficient” vitamin D levels.3
By framing the issue in this way, the media reports ignore the fact that people can obtain ample vitamin D levels from a combination of diet, supplements, and incidental protected sun exposure,1,4-7 and that, to date, most intervention studies suggesting a benefit of increased 25(OH)D levels have used oral supplements, not UV exposure.1,2,8
Reports often cite low or low normal levels of vitamin D in darkly pigmented individuals, such as inner-city minority groups, or among the frail elderly in order to justify promoting unprotected sun exposure. However, these at-risk groups have inefficient cutaneous vitamin D photosynthesis.
In darkly pigmented people melanin absorbs UV photons that generate vitamin D,9 and the thinned epidermis of the elderly appears to contain less 7-dehydrocholesterol, which is the cell membrane constituent that UVB converts to pre-vitamin D.10,11 As well, population groups most attracted to sunbathing, i.e., healthy Caucasian teenagers and young adults, including many fair-skinned individuals who tan poorly,12 are at lowest risk of vitamin D insufficiency, yet at greatest risk of long-term photodamage.
What is Vitamin D Insufficiency?
It is virtually impossible to find a definition of this recently coined term in the literature. It loosely refers to levels of 25(OH)D above those classically associated with bone disease and below those found in various observational or epidemiologic studies to be statistically associated with a higher risk of the studied disorder, for example, cancer. These upper cut-off values vary enormously from study to study and author to author, from perhaps 50nmol/L to 150nmol/L, often 75-80nmol/L.1
A recent study13 of 93 healthy young adults who were recruited from the University of Hawaii and a Honolulu skateboard shop, questioned the frequently suggested serum 25(OH)D “sufficiency” cut-off value of 75nmol/L. The investigators based recruitment of this convenience sample of prototypic “surfer dudes” (mean age 24 years, mean body-mass index 23.6 kg/m2) on a self-reported minimum outdoor sun exposure of 15 hours (mean 29 hours) per week during the preceding 3 months; 40% reported never using sunscreen and the group overall reported an average of 22.4 hours per week of unprotected sun exposure. All were clinically tanned. Nevertheless, the group’s mean 25(OH)D level, measured by 2 standard techniques (high-performance liquid chromatography and radioimmunoassay), was 79nmol/L, and 51% had a level below the suggested 75nmol/L cut-off for “sufficiency”.13 These data suggest that a public health goal of >75nmol/L for the entire population might be unachievable through sun exposure.
Regardless of the cut-off used, the great majority of people with insufficient 25(OH)D levels have no detectable disease or health problem and, statistically, they probably never will. On an individual basis, there is no detectable benefit from a high 25(OH)D level and, conversely, no harm from a lower level. Even more curious, in many instances the statistical associations on which the “insufficient” status is based are not measured 25(OH)D levels, but instead presumptive correlates such as insolation (i.e., the amount and intensity of incident UV irradiation) in the general geographic region of residence. In fact, latitude, altitude, season, cloud cover, smog, and other variables affect insolation, which is generally high near the equator and low near the poles; and lifestyle choices introduce enormous variation in sun exposure, even among individuals in identical climates.
The True Controversy
The real controversy is whether increasing a person’s conventionally normal serum 25(OH)D level has health benefits, as some epidemiologic studies have suggested, but prospective randomized studies, with the one exception noted below, have not confirmed. A thorough discussion of the quality and consistency of the epidemiologic and observational data available through 2005, which some interpreted to support a health benefit of serum 25(OH)D levels far above those associated with normal skeletal maintenance, is available elsewhere1 and is beyond the scope of this editorial. However, because prevention of colorectal cancer is often cited as the best established benefit of unconventionally high 25(OH)D levels, a brief discussion of this example is instructive. Several much-referenced reports link colorectal cancer incidence14-16 to “low” vitamin D levels within the conventional normal range or to a presumptive proxy, i.e., little sun exposure, usually based on residence in a poorly insolated area, as noted above. Although other epidemiologic or observational studies of similar size and design (grade B, level 2 or 3 in the hierarchy of evidence-based medicine)17 found no statistical relationship or even an inverse relationship between sun exposure and colorectal cancer or closely related diseases,18-22 the popular media coverage of the topic has selectively and prominently cited the positive reports at the suggestion of interviewed “experts.”
In 2006, a prospective, randomized, placebo-controlled trial (grade A, level 1 for medical decision making)17 of vitamin D supplementation (400 IU/day) for 7 years or longer involving more than 36,000 post-menopausal women found no relationship between colorectal cancer risk (incidence or mortality; tumor grade, stage, or size) and supplement use, total vitamin D intake, or amount of sun exposure (crudely and indirectly calculated, as in the positive epidemiologic studies).8 Although the investigators found an inverse correlation with baseline serum 25(OH)D levels, they found no indication that increasing initially low vitamin D levels by supplementation reduced cancer risk over the subsequent 7 years.8 An accompanying editorial23 and the investigators themselves noted that 7 years of supplementation might be too short, the subjects might have received a dose of vitamin D that was too low, they might have had a lifestyle that was too healthy, or they might have been too young (62 years on average) to develop this cancer in large numbers. In brief, the authors concluded that no result is ever definitively negative. Yet, less than 2 months later, the media prominently covered a far less definitive, multivariable model study that statistically inversely linked the risk of cancer, including colorectal cancer, to 6 indirect historical measures of sun exposure and presumptively correlated vitamin D levels,24 with no reference to the “gold-standard” negative colorectal cancer study.8
Most recently, the American Journal of Clinical Nutrition published a 4-year randomized, prospective blinded study of 1,179 presumptively healthy postmenopausal Caucasian women in rural Nebraska who were followed for 4 years while taking a calcium (Ca) supplement (n=445), a Ca plus vitamin D (Ca-D) supplement (n=446), or a placebo only (n=288).2 This study was designed to assess bone fracture risk, but data were also analyzed to assess cancer incidence.2 The women were interviewed by a study nurse every 6 months and, if they reported a new diagnosis of nonskin cancer, their medical records were reviewed. Fifty women with a newly diagnosed cancer (19 with breast cancer, 3 with colon cancer, and 28 with other cancers) were identified, 13 in year 1 and 37 in years 2-4, representing 6.9% of the placebo group and 3.8% and 2.9% of the Ca and Ca-D groups, respectively, which indicated a significantly reduced relative risk of 0.4 for the Ca-D group. The vitamin D dose (1,000 IU/day) was higher than the current RDA of 400-600 IU/day, depending on age, and increased the average 25(OH)D level in all groups from approximately 71 to 96nmol/L in the Ca-D group by the end of year 1. For the initial and control groups, 25(OH)D levels are of interest in that they are very close to the commonly recommended “sufficient” level of 25(OH)D of =75nmol/L and the average 25(OH)D level of 79nmol/L observed in a population of healthy, tanned young men in Hawaii with a self-reported unprotected sun exposure of 22.4 hours/week.13 The article does not report the 25(OH)D levels of the 50 women who developed cancer vs. the 1,129 who did not, either at baseline or during supplementation; nor does it report data for the original primary endpoint, bone fracture incidence.2 The apparent protective effect of high dose Ca-D supplementation on cancer risk is certainly of interest, however, and confirmatory studies are eagerly awaited.
Irrelevance of Both Controversies to Sun Protection
A neglected but critical point is that the “true” optimal level of 25(OH)D for musculoskeletal health, cancer prevention, or any of the other claimed benefits is irrelevant to the proven value of sun protection. Whatever this optimal level, ample vitamin D can be obtained from diet, supplements, and incidental sun exposure.1,4-7 Intentional unprotected sun exposure to increase vitamin D photosynthesis is not only unnecessary, but also inefficient for those at highest risk of vitamin D deficiency.9-11 The groups most responsive to the media’s unprotected sun exposure message are those who have the statistically lowest risk of vitamin D deficiency: healthy fair-skinned adolescents and young adults. Indeed, surveys in the US show that more than 70% of tanning bed users are Caucasian women aged 16-49 years12 and 95% of all users exceed the exposure levels recommended by the US FDA25 for maximizing vitamin D photosynthesis. The demographics and exposure habits of the sunbathing public are similar to those of tanning bed users, although the average age is probably even younger and exposures even greater. The safe-sun message promulgated by dermatologists and the American Academy of Dermatology does not target dark-skinned individuals, who already have excellent endogenous sun protection in the form of epidermal melanin. Moreover, the groups at demonstrated risk of vitamin D deficiency have not embraced the “UV advantage” message,3 perhaps because this message does not target them.
The interest among the media and public in the pseudo-controversy is nevertheless real and persistent. Why? The sun protection message is old, dating back at least 23 years,26 and its intended audience views it as wimpy, like the “buckle up” seatbelt message. Real men, and rebellious, fun-loving, and spontaneous adolescents do not wear sunscreen (or seatbelts). Moreover, many people, especially teenagers, want to sunbathe to acquire a “sexy” tan, not to reduce their risk of age-associated disease decades later.27 In addition, relaxing in the sun and making one’s own vitamin D have a back-to-nature holistic appeal for many individuals. It is therefore not surprising that the print and electronic media continue to cover the pseudo-controversy: it sells. However, press releases crafted by representatives and employees of the USD $5 billion/year indoor tanning industry28,29 have greatly facilitated the media’s natural tendency to pursue a “new” and controversial story, especially if it is one their audience wishes to hear.
The indoor tanning industry’s concern for the public health would be more credible if its coverage of the issues were more balanced, and a decade or so of extolling the virtues of UVA lamps (not the UVB lamps that it now touts as “healthful”) had not preceded the current campaign.30-32 Before publication of the epidemiologic studies questioning the adequacy of conventional vitamin D recommendations, the industry argued strenuously that indoor tanning was superior to natural sun exposure precisely because people could tan with less UVB exposure (and, of course, less vitamin D photosynthesis).33 Indeed, a review of the industry’s public positions over the 30 years of its dramatic growth in annual revenues34 reveals a series of opportunistic, contradictory positions. There can be no doubt that the goal of the tanning industry is to sell tanning sessions, not to safeguard the public’s health.
One Dermatologist’s Recommendation to Patients
Common sense and overwhelming medical/scientific literature support the fact that fair-skinned people benefit from regular, lifelong, safe sun practices. Moreover, people who wear high-sun protection factor (SPF) sunscreen in season, probably synthesize vitamin D maximally in exposed areas during incidental sun exposure.35 Although some have claimed that sunscreens block all UV (and hence, all vitamin D photosynthesis36) this is not the case. By definition, sunscreens allow continuous transmission of a fraction of erythemogenically weighted incident UV photons equal to 1/SPF of the total (e.g., 1/15th or 7% for an SPF 15 product). Moreover, studies have shown that sunscreen users customarily apply half or less of the FDA-stipulated amount of product required to generate the stated level of protection (2mg/cm2) and hence achieve far less protection.37 If people require 2-8 minutes of unprotected summer sun exposure to maximize their cutaneous vitamin D synthesis,3 they could accomplish this in approximately 10-20 minutes of exposure after applying an SPF 15-30 sunscreen in the customary manner.37,38 Most critically, regardless of one’s complexion, or the extent of UV exposure, daily oral vitamin D supplementation can completely compensate for the lack of cutaneous vitamin D photosynthesis.1 Of note, those rare individuals with compromised absorption of orally-administered vitamin D should be advised to use intramuscular injections or very high-dose oral supplements.
Despite the above considerations, many patients ask their dermatologist to recommend a “safe” or “prudent” amount of sun exposure. Such recommendations must be individualized, as the risk-benefit ratio varies enormously within the population. Moderate or even generous sun exposure might have little effect on a darkly pigmented person’s risk of subsequent photoaging and skin cancer while promoting higher 25(OH)D levels; but even quite modest exposure could promote development of precancerous and cancerous lesions in already-photodamaged fair skin without increasing the already maximized vitamin D photosynthesis. A rule of thumb might be that any sunburn dose is too much by a factor of at least 3, as maximal vitamin D synthesis is achieved after approximately one-third of a minimal erythema dose.39
Individuals who never sunburn or who live in climates that never allow them to sunburn are relatively “safe” from the damaging effects of unprotected sun exposure. People with complexions or living circumstances associated with the possibility of frequent sunburns probably have no “safe”, minimum unprotected exposures. Such unprotected exposures would only be a few minutes in length, but in the course of their routine activities, this higher-risk group would almost certainly exceed the prudent exposure time on a daily basis.
Although the much discussed epidemic of vitamin D insufficiency has been linked by some to the overuse of sunscreens, there is little or no evidence that this is the case, even if such an epidemic exists. Those population groups most likely to be vitamin D deficient (and presumably insufficient, if that term is accepted) are indeed unlikely to use sunscreens at all; these groups include inner city dark-skinned minorities, frail elderly who are often home-bound or institutionalized, and Middle Eastern women who wear the bourka, and therefore expose very little skin to the sun.
Strong evidence suggests that many individuals in these groups derive at least a musculoskeletal benefit from vitamin D supplementation, although they infrequently consult a dermatologist in this regard. Strong evidence also suggests that long-term oral vitamin D supplementation at doses up to 10 times the current RDAs are safe,4,40 and many endocrinologists and nutritionists now suspect that the RDAs are too low. Therefore, it seems quite reasonable to recommend to all older patients who practice sun safety and to anyone even remotely concerned about vitamin D “sufficiency” that he/she take 1,000 IU of vitamin D daily, especially in the winter months. Routine measurement of the serum 25(OH)D level does not seem warranted, as the test is expensive and the “normal” or “optimal” range is debatable; in any case, the treatment for “low” levels is supplementation at this dose.
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- Lappe JM, Travers-Gustafson D, Davies KM, et al. Vitamin D and calcium supplementation reduces cancer risk: results of a randomized trial. Am J Clin Nutr 85(6):1586-91 (2007 Jun).
- Holick MF, Jenkins M. The UV Advantage. ibooks, Incorporated (2004).
- Vieth R. Vitamin D supplementation, 25-hydroxyvitamin D concentrations, and safety. Am J Clin Nutr 69(5):842-56 (1999 May).
- Boucher BJ. Sunlight “D”ilemma. Lancet 357(9260):961 (2001 Mar 24).
- Calvo MS, Whiting SJ, Barton CN. Vitamin D intake: a global perspective of current status. J Nutr 135(2):310-6 (2005 Feb).
- Utiger RD. The need for more vitamin D. N Engl J Med 338(12):828-9 (1998 Mar 19).
- Wactawski-Wende J, Kotchen JM, Anderson GL, et al. Calcium plus vitamin D supplementation and the risk of colorectal cancer. N Engl J Med 354(7):684-96 (2006 Feb 16).
- Clemens TL, Adams JS, Henderson SL, et al. Increased skin pigment reduces the capacity of skin to synthesise vitamin D3. Lancet 1(8263):74-6 (1982 Jan 9).
- Bell NH. Vitamin D metabolism, aging, and bone loss. J Clin Endocrinol Metab 80(4):1051 (1995 Apr).
- Need AG, Morris HA, Horowitz M, et al. Effects of skin thickness, age, body fat, and sunlight on serum 25-hydroxyvitamin D. Am J Clin Nutr 58(6):882-5 (1993 Dec).
- Swerdlow AJ, Weinstock MA. Do tanning lamps cause melanoma? An epidemiologic assessment. J Am Acad Dermatol 38(1):89-98 (1998 Jan).
- Binkley N, Novotny R, Krueger D, et al. Low vitamin D status despite abundant sun exposure. J Clin Endocrinol Metab 92(6):2130-5 (2007 Jun).
- Garland CF, Garland FC, Gorham ED. Can colon cancer incidence and death rates be reduced with calcium and vitamin D? Am J Clin Nutr 54(1 Suppl):193S-201S (1991 Jul).
- Garland CF, Garland FC, Gorham ED. Calcium and vitamin D. Their potential roles in colon and breast cancer prevention. Ann N Y Acad Sci 889:107-19 (1999).
- Holick MF. Vitamin D: Photobiology, metabolism, mechanism of action, and clinical applications. In: Favus M, editor. Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism. 4th ed. Philadelphia: Lippincott Williams & Wilkins; p92-8 (1999).
- Bigby M, Szklo M. Evidence-based dermatology. In: Freedberg IM, Eisen AZ, Wolff K, Austen KF, Goldsmith LA, Katz SI, editors. Fitzpatrick’s Dermatology in General Medicine. 6th ed. New York: McGraw-Hill; p2301-11 (2003).
- Grau MV, Baron JA, Sandler RS, et al. Vitamin D, calcium supplementation, and colorectal adenomas: results of a randomized trial. J Natl Cancer Inst 95(23):1765-71 (2003 Dec 3).
- Tuohimaa P, Tenkanen L, Ahonen M, et al. Both high and low levels of blood vitamin D are associated with a higher prostate cancer risk: a longitudinal, nested case-control study in the Nordic countries. Int J Cancer 108(1):104-8 (2004 Jan 1).
- Gross MD. Vitamin D and calcium in the prevention of prostate and colon cancer: new approaches for the identification of needs. J Nutr 135(2):326-31 (2005 Feb).
- Hartman TJ, Albert PS, Snyder K, et al. The association of calcium and vitamin D with risk of colorectal adenomas. J Nutr 135(2):252-9 (2005 Feb).
- Majewski S, Skopinska M, Marczak M, et al. Vitamin D3 is a potent inhibitor of tumor cell-induced angiogenesis. J Investig Dermatol Symp Proc 1(1):97-101 (1996 Apr).
- Forman MR, Levin B. Calcium plus vitamin D3 supplementation and colorectal cancer in women. N Engl J Med 354(7):752-4 (2006 Feb 16).
- Giovannucci E, Liu Y, Rimm EB, et al. Prospective study of predictors of vitamin D status and cancer incidence and mortality in men. J Natl Cancer Inst 98(7):451-9 (2006 Apr 5). 25. use: are we exceeding Food and Drug Administration limits? J Am Acad Dermatol 49(4):655-61 (2003 Oct).
- Hornung RL, Magee KH, Lee WJ, et al. Tanning facility use: are we exceeding Food and Drug Administration limits? J Am Acad Dermatol 49(4):655-61 (2003 Oct).
- Robinson JK, Rigel DS, Amonette RA. Trends in sun exposure knowledge, attitudes, and behaviors: 1986 to 1996. J Am Acad Dermatol 37(2 Pt 1):179-86 (1997 Aug).
- Geller AC, Brooks DR, Colditz GA, et al. Sun protection practices among offspring of women with personal or family history of skin cancer. Pediatrics 117(4):688-94 (2006 Apr).
- Demierre MF. Time for the national legislation of indoor tanning to protect minors. Arch Dermatol 139(4):520-4 (2003 Apr).
- Dellavalle RP, Parker ER, Cersonsky N, et al. Youth access laws: in the dark at the tanning parlor? Arch Dermatol 139(4):443-8 (2003 Apr).
- Westerdahl J, Ingvar C, Masback A, et al. Risk of cutaneous malignant melanoma in relation to use of sunbeds: further evidence for UV-A carcinogenicity. Br J Cancer 82(9):1593-9 (2000 May).
- US Department of Health and Human Services, Public Health Service, National Toxicology Program. Exposure to sunlamps or sunbeds. In: Report on carcinogens. 11th ed. (2005).
- Spencer JM, Amonette RA. Indoor tanning: risks, benefits, and future trends. J Am Acad Dermatol 33(2 Pt 1):288-98 (1995 Aug).
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- Gilchrest BA. Sun exposure and vitamin D sufficiency. J Natl Cancer Inst 2008: in press.
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- Bech-Thomsen N, Wulf HC. Sunbathers’ application of sunscreen is probably inadequate to obtain the sun protection factor assigned to the preparation. Photodermatol Photoimmunol Photomed 9(6):242-4 (1992 Dec).
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- Hollis BW. Circulating 25-hydroxyvitamin D levels indicative of vitamin D sufficiency: implications for establishing a new effective dietary intake recommendation for vitamin D. J Nutr 135(2):317-22 (2005 Feb).