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Do sunscreens really protect us? Do sunscreens really protect us? As a nation our sun exposure habits have become dysfunctional. We live and work increasingly indoors. We are only in direct sunlight for minutes a day, shuttling between home, office and supermarket shielded by the windows of cars, buses or trains. This low-level of UV exposure contrasts with the holiday habits of most of the British population. The overseas holiday is so widely accepted as an annual ritual that holidays within the UK now have a novelty to them: where for Blair it was the Tuscany villas, now it is the Camerons’ Cornish “staycation” [1]. With the overseas holiday comes the expectation of a tan. In younger age groups, especially for women, there is a societal pressure to be tanned. The cult of celebrity equates a tan with attractiveness, desirability and health. With the indestructible feeling of youth and a belief in modern and future medicine, the young are often cavalier when it comes to protecting themselves from the sun, especially when the immediate payout (for most) of a tan is socially rewarded. This phenomenon has made some interesting news stories in recent years, including a travel firm running a competition for photos of the worst sunburns [2], and the mother who allowed her 5 month old son to develop sunburn necessitating hospital admission [3]. In Wales, with its notably tanned celebrities (Gavin Henson, Charlotte Church et al.), there has been a recent push to ban coin-operated non-attended tanning booths [4]. These booths allowed under-16s to re-use them immediately and repeatedly, exposing themselves to levels of UV certain to cause harm [4]. Page 1 of 14 Do sunscreens really protect us? Why does it matter how much sun exposure we have (or don’t have)? Whilst the public conscious is dimly aware that the sun is dangerous, the public’s understanding of the risks is poor – perhaps why so many choose the short term benefit of a tan, given an ill-informed weighing of the risks and benefits of UV exposure. Over- or under-exposure to sunlight can damage our health in a number of different ways. Sunlight is a large sample of the electromagnetic spectrum and at the Earth’s surface can be considered as 4 wavelength regions: ultraviolet B (UVB, 280315 nm), ultraviolet A (UVA, 315-400 nm), visible light (400-760 nm) and infrared (760-106 nm) [5]. Infrared waves are the ‘warmth’ of sunlight and are widely regarded as safe – infrared light bulbs are used as food warmers in restaurants. Excluding the effects of visible light on the retina, UVA and UVB are the biologically active components of sunlight [5]. UVB rays are of higher energy than UVA [6]. Only a small proportion of UVB reaches the dermis and causes injury by direct DNA damage, whereas UVA penetrates the dermis and causes damage through the generation of reactive oxygen species [6]. The skin pathologies caused by the UV component of sunlight can be divided into chronic and acute. Chronic changes include photo-ageing, actinic keratoses, keratoacanthomata and malignancies associated with UV exposure: basal cell carcinoma, squamous cell carcinoma and malignant Page 2 of 14 Do sunscreens really protect us? melanoma [7]. UVA and UVB have differing roles in mediating these changes, probably because of their different penetrations and mechanisms of molecular injury. Sunburn is caused by UVB, but there is increasing evidence that the other pathologies, including photo-ageing are caused by both UVA and UVB, perhaps in synergy [8]. Sunlight can exacerbate pre-existing diseases and is often helpful in making the diagnosis. The photosensitive rash of systemic lupus erythematosus is the best example. Rosacea, psoriasis, Darier’s disease and herpes simplex infections can all be worsened by sunlight exposure [9]. Acute pathologies caused by sunlight include sunburn (solar erythema) and photosensitivity reactions which can be caused by UV or visible light. Patients who have taken a photosensitising drug or had contact with photosensitising plants are at particular risk. Photosensitivity is the only dermatological pathology that visible light is known to cause. There are a number of very rare acute reactions to light, including polymorphic light eruption, solar urticaria, actinic prurigo, juvenile spring eruption, hydroa vacciniforme, photosensitive eczema, porphyrias, pellagra and xeroderma pigmentosum [9]. Proving the efficacy by comparing sunscreens (with a strong theoretical argument for benefit and small risks [discussed later]) to placebo (no benefits, no risks) is ethically questionable, especially for exquisitely UV-sensitive conditions such as xeroderma pigmentosum. Achieving statistical proof is further complicated by the low incidence of these conditions. Page 3 of 14 Do sunscreens really protect us? Sunscreen was developed in the 1930s answering a demand for protection from sunburn due to the fashion for tanning in light skinned populations [10]. Early sunscreens attempted to block UVB preventing sunburn and providing some protection from chronic UV responses. Compounds used in sunscreens can be divided into two classes: physical or chemical blockers. Physical blockers (zinc oxide, titanium dioxide) reflect UV light preventing it from reaching the epidermis [6]. Chemical blockers absorb the UV and release it at a different, non-toxic wavelength [6]. The efficacy of sunscreen has been measured using the sun protection factor (SPF). This measures the ratio between the time needed to develop sunburn with and without the sunscreen. As an example, a person using SPF15 who normally burns in 10 minutes, can expect to burn after 150 minutes of exposure. Doubling an SPF does not half the UV dose at the epidermis: SPF15 blocks 94% of UVB and SPF30 blocks 97% [6]. The FDA are phasing out the complicated SPF to replace it with simpler categories of protection: low (SPF2-15), medium (15-30), high (30-50) and highest (50+) [11]. An SPF makes no statement about the protection conferred against UVA. There are differences in the UVA protection between different physical blockers – with titanium dioxide inferior to zinc oxide [12] – and a number of chemical blockers offer little or no UVA protection [13]. In Europe, UVA protection is currently scored with a star rating, frequently printed on the reverse of the bottle. Epidemiological studies of skin cancer have established a strong link between skin cancer and sunburn history [14]. Animal models of skin cancers show Page 4 of 14 Do sunscreens really protect us? the protective effect of sunscreen [15-17]. There is however no model for melanoma [14]. More recently, UVA has been implicated in skin cancer pathogenesis [18]. A similar evidence base exists for the link between smoking and lung cancer and a number of other diseases, including coronary heart disease [19]. In the UK, a smoking ban in 2007 resulted in a 2.4% reduction in emergency admissions for myocardial infarction, equating to 1200 fewer admissions a year [19]. A similar result might be expected with widespread usage of sunscreen, with the UV protection afforded by sunscreen reducing cancer rates. Large case-control studies report the opposite effect, where sunscreen use is associated with an increased risk of melanoma [14]. Population studies also show an increased rate of skin cancer despite wider availability of sunscreen [20]. Sunscreen use by schoolaged children is associated with an increased risk of basal cell carcinoma and more acquired melanocytic naevi – predictors of future malignant melanoma [21-23]. One explanation for this discrepancy is that sunscreen provides effective protection from sunburn, but not from UV-induced DNA damage [14]. Users of sunscreen spend longer in the sun, as they are protected from sunburn and therefore feel protected from carcinogenic damage [24]. Most sunscreens offer low protection against UVA and modest to good protection against UVB [11]. ‘Un-blocked’ UVA might contribute to the increased cancer rates in sunscreen users, as the delay in sunburn development (due to UVB) allows for a larger UVA exposure. Exposure to UV radiation does not affect only the skin. associated pathologies of the eye, Page 5 of 14 including There are UV- photokeratitis and Do sunscreens really protect us? photoconjunctivitis in the short term and cataracts, pterygium and squamous cell carcinoma of the cornea or conjunctiva with chronic exposure [25]. The World Health Organisation estimates that of the 18 million people in the world rendered blind by cataracts, 5% (0.9 million) are attributable to UV exposure [25]. As mentioned earlier, herpes simplex infection of mucosal epithelium can be exacerbated by UV light. These ‘non-skin’ UV-associated pathologies will not be influenced by the use or otherwise of sunscreen. Wearing sunglasses in sunlight is an important step in protecting eyes from UV damage and a hat will provide ophthalmological and dermatological protection for the face and neck. Despite the numerous pathological associations, UV exposure does have benefits to health [25]. Vitamin D can be synthesised in the skin by the action of UVB light on dehydrocholesterol and is a fat-soluble vitamin. There is evidence that sunscreens can prevent vitamin D production in skin [26]. Vitamin D has two recognised biological roles. The first role is in calcium metabolism and appropriate bone mineralisation depends on vitamin D. Vitamin D deficiency causes rickets in children and osteoporosis and osteomalacia in adults. These diseases carry a significant impact on quality of life. A model of the effects of UV exposure predicted that in the year 2000 between 1.3 and 1.7 million disability-adjusted life years (DALYs) were lost to the UV-related pathologies already discussed [7]. Modelling a UV exposure of 0 generated the prediction of 3,304 million DALYs lost to rickets, osteomalacia and osteoporosis [7]. From these data, UV exposure can be considered a positive factor in global health. Page 6 of 14 The balance for Western Do sunscreens really protect us? populations is probably more equivocal, as high-fat Western diets will deliver a larger component of the vitamin D requirement. Vitamin D’s second role is immunomodulation. The early mice studies linking UV exposure with carcinogenesis demonstrated a UV-mediated suppression of anti-tumour responses [27]. Transplant of the UV-induced tumours into immunocompetent hosts resulted in tumour rejection [28]. recipients did not reject the tumours [28]. UV-exposed Together these experiments implicate UV-generated vitamin D as an important immunomodulator. The immune effects of vitamin D are still not fully understood. Locally produced vitamin D activates the innate immune system by, for example, increasing production of antimicrobial peptides (e.g. cathelicidin) by monocytes and macrophages [27]. Vitamin D has the opposite effect on the adaptive system, with an inhibitory effect on T cell differentiation and plasma cell development [27]. There are associations between a gene (CYP27B1) involved in vitamin D metabolism and human autoimmune diseases, including type 1 diabetes [29], linking disturbances of vitamin D metabolism with immune pathology. It has been shown that responses to particular tumour vaccination strategies can be enhanced with pre-vaccine UV exposure [27]. As vitamin D has activatory and inhibitory effects on components of the immune system, it is the balance of these effects is critical in determining the overall outcome of vitamin D signalling. This balance is likely to be disturbed by a number of other immunological signals, not least the presence of microbial products. Page 7 of 14 Do sunscreens really protect us? Immunomodulation with UV light therapy can be used in the treatment of dermatological diseases, most notably psoriasis. Light therapy is given as a narrower spectrum (311-313nm) of UVB than found in sunlight [27]. UVB radiation disturbs cytokine signalling in psoriatic skin, suppressing IL-23 and IL-17, integral parts of the Th17 differentiation pathway [27]. Narrow band UVB probably causes little or no vitamin D production [27], and so presumably acts independently of vitamin D. Supplementing UVB therapy with topical vitamin D has a synergistic effect and is commonplace in the treatment of psoriasis. UVA can also be used in light therapy, often in conjunction with psoralen, a photosensitiser. Can the next generation of sunscreens keep the benefits of UV exposure whilst still mitigating its deleterious effects? There are a number of promising lines of research. The first is examining UV protection afforded by microbial products. Microbes have been exposed to UV light for a substantial portion of their evolution – since the composition of the atmosphere stabilised. There are a number of microbially produced sunscreens, including mycosporins and bacterial melanins, which are now reaching the market for human sunscreens [5]. Nanoparticles of zinc oxide and titanium dioxide have re-popularised these physical barriers, as new formulations are less conspicuous [30]. Some of these nanoparticles can be found systemically, raising the possibility of trans-dermal drug delivery by nanoparticle carriage [30]. Perhaps the most intriguing research is based on coral’s photo-protection mechanism. A mycosporin-like amino acid (MAA) sunscreen is synthesised by algae living within the coral structure [31]. This MAA is passed to the coral host via Page 8 of 14 Do sunscreens really protect us? exocytosis from the algae [31], where it is presumed to prevent photobleaching. The same MAA molecule has been identified in tropical fish, suggesting that the MAA can travel up the food chain [32]. This is the first description of the enteric delivery of a sunscreen. If this MAA can be massproduced, and it proves safe in mammals, this might provide a novel approach offering better UV protection and, by being tablet-based, improved concordance, sparing the user regular re-application after swimming, toweling, sweating or prolonged exposure. A pragmatic alternative is to use UV-meters to formally quantify exposure, allowing individuals to tailor their activities for adequate vitamin D synthesis without excessive UV dosing [14]. In summary, there is no straightforward answer to the question ‘do sunscreens really protect us?’. In principle, sunscreens provide protection from UVB-mediated pathologies, including sunburn and - at least in vitro and in animal models - from dermatological malignancy. They also provide some protection for UVA-mediated pathology. The data concerning sunscreen use by humans is more conflicting. Perhaps sunscreen provides a false protection, preventing sunburn and therefore allowing an increased exposure to carcinogenic levels of UV. Responsible use of sunscreen probably does prevent skin cancer, so the best advice to give to a single patient remains to use sunscreen (high SPF, with UVA protection), alongside emphasizing the importance of judicious use, hats, sunglasses and seeking shade in the early afternoon (12-3pm). Sunscreens are not harmless, they do have the potential to cause disease, through vitamin D deficiency. The systemic effects of vitamin D deficiency (rickets, osteoporosis and osteomalacia) are significant Page 9 of 14 Do sunscreens really protect us? sources of morbidity worldwide and their link with little or no UV exposure well described. The World Health Organisation has predicted a larger DALY loss with no UV exposure than with no improvements in sun protection. Immunomodulation via local effects of vitamin D is less well understood and could include immunosuppression or autoimmune disease predisposition. Light therapy suggests the existence of other immunomodulatory pathways independent of vitamin D. Whilst appropriate use of sunscreen does protect us from dermatological malignancy, whether they provide a definite overall health improvement is unclear. This assessment hinges on the possibility of a undefined immunomodulatory pathway independent of vitamin D, alongside our growing understanding of vitamin D and its immunological function. References 1. Staycations? There's nothing to smile about [http://www.telegraph.co.uk/travel/familyholidays/7960345/StaycationsTheres-nothing-to-smile-about.html] 2. Sunburn contest branded 'irresponsible' by ASA [http://www.bbc.co.uk/news/uk-15178664] 3. Brighton beach sunburn baby discharged from hospital [http://news.bbc.co.uk/1/hi/8705520.stm] 4. Banned sunbeds: 'No redeeming features', says top medic [http://www.bbc.co.uk/news/uk-wales-15506099] 5. Gao Q, Garcia-Pichel F: Microbial ultraviolet sunscreens. Nat Rev Microbiol 2011, 9(11):791-802. Page 10 of 14 Do sunscreens really protect us? 6. Koshy JC, Sharabi SE, Jerkins D, Cox J, Cronin SP, Hollier LH, Jr.: Sunscreens: evolving aspects of sun protection. J Pediatr Health Care 2010, 24(5):343-346. 7. Global burden of disease from solar ultraviolet radiation [http://www.who.int/uv/health/solaruvradfull_180706.pdf] 8. Yaar M, Gilchrest BA: Photoageing: mechanism, prevention and therapy. Br J Dermatol 2007, 157(5):874-887. 9. Graham-Brown R, Burns T: Lecture Notes Dermatology, 9th edn: Blackwell; 2007. 10. Albert MR, Ostheimer KG: The evolution of current medical and popular attitudes toward ultraviolet light exposure: part 3. J Am Acad Dermatol 2003, 49(6):1096-1106. 11. Final Rule: Labeling and Effectiveness Testing; Sunscreen Drug Products for Over-the-Counter Human Use [http://www.gpo.gov/fdsys/pkg/FR-2011-06-17/pdf/2011-14766.pdf] 12. Beasley DG, Meyer TA: Characterization of the UVA protection provided by avobenzone, zinc oxide, and titanium dioxide in broadspectrum sunscreen products. Am J Clin Dermatol 2010, 11(6):413-421. 13. Antoniou C, Kosmadaki MG, Stratigos AJ, Katsambas AD: Sunscreens--what's important to know. J Eur Acad Dermatol Venereol 2008, 22(9):1110-1118. 14. Autier P: Sunscreen abuse for intentional sun exposure. Br J Dermatol 2009, 161 Suppl 3:40-45. Page 11 of 14 Do sunscreens really protect us? 15. Synder DS, May M: Ability of PABA to protect mammalian skin from ultraviolet light-induced skin tumors and actinic damage. J Invest Dermatol 1975, 65(6):543-546. 16. Kligman LH, Akin FJ, Kligman AM: Sunscreens prevent ultraviolet photocarcinogenesis. J Am Acad Dermatol 1980, 3(1):30-35. 17. Wolf P, Donawho CK, Kripke ML: Effect of sunscreens on UV radiation-induced enhancement of melanoma growth in mice. J Natl Cancer Inst 1994, 86(2):99-105. 18. Runger TM: C-->T transition mutations are not solely UVB- signature mutations, because they are also generated by UVA. J Invest Dermatol 2008, 128(9):2138-2140. 19. Sims M, Maxwell R, Bauld L, Gilmore A: Short term impact of smoke- free legislation in England: retrospective analysis of hospital admissions for myocardial infarction. BMJ 2010, 340:c2161. 20. Handel AE, Ramagopalan SV: The questionable effectiveness of sunscreen. Lancet 2010, 376(9736):161-162; author reply 162. 21. 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(1):13-23. 22. Autier P, Dore JF, Cattaruzza MS, Renard F, Luther H, Gentiloni-Silverj F, Zantedeschi E, Mezzetti M, Monjaud I, Andry M et al: Sunscreen use, wearing clothes, and number of nevi in 6- to 7-year-old European children. European Organization for Research and Treatment of Cancer Melanoma Cooperative Group. J Natl Cancer Inst 1998, 90(24):1873-1880. Page 12 of 14 Do sunscreens really protect us? 23. Bauer J, Buttner P, Wiecker TS, Luther H, Garbe C: Effect of sunscreen and clothing on the number of melanocytic nevi in 1,812 German children attending day care. Am J Epidemiol 2005, 161(7):620627. 24. Autier P, Boniol M, Dore JF: Sunscreen use and increased duration of intentional sun exposure: still a burning issue. Int J Cancer 2007, 121(1):1-5. 25. Ultraviolet radiation and human health [http://www.who.int/mediacentre/factsheets/fs305/en/index.html] 26. Reichrath J: Skin cancer prevention and UV-protection: how to avoid vitamin D-deficiency? Br J Dermatol 2009, 161 Suppl 3:54-60. 27. Hart PH, Gorman S, Finlay-Jones JJ: Modulation of the immune system by UV radiation: more than just the effects of vitamin D? Nat Rev Immunol 2011, 11(9):584-596. 28. Kripke ML: Antigenicity of murine skin tumors induced by ultraviolet light. J Natl Cancer Inst 1974, 53(5):1333-1336. 29. Bailey R, Cooper JD, Zeitels L, Smyth DJ, Yang JH, Walker NM, Hypponen E, Dunger DB, Ramos-Lopez E, Badenhoop K et al: Association of the vitamin D metabolism gene CYP27B1 with type 1 diabetes. Diabetes 2007, 56(10):2616-2621. 30. Delouise LA: Applications of Nanotechnology in Dermatology. J Invest Dermatol 2012. 31. Starcevic A, Dunlap WC, Cullum J, Shick JM, Hranueli D, Long PF: Gene expression in the scleractinian Acropora microphthalma exposed Page 13 of 14 Do sunscreens really protect us? to high solar irradiance reveals elements of photoprotection and coral bleaching. PLoS One 2010, 5(11):e13975. 32. Coral could be used to create sunscreens [http://www.kcl.ac.uk/newsevents/news/newsrecords/2011/08August/Tropicalcoral-create-novel-sun-screens-human-use-scientists.aspx] Page 14 of 14