Review
Do suncreens protect us? Douglas L. Maslin, MA, MB, BCHIR
Addenbrooke’s Hospital, Cambridge, UK
Abstract Sunlight stimulates a multitude of important biological effects on skin, causing, amongst
Correspondence Douglas Maslin, MA, MB, BCHIR Downing College Cambridge CB2 1DQ UK E-mail: [email protected] Conflicts of interest: None.
other pathological changes, photocarcinogenesis. Sunscreens are designed to provide protection against these harmful properties of ultraviolet radiation, and public health campaigns have been employed to encourage their use. Despite this, there has been a continued rise in the incidence and mortality of the most harmful skin cancer, malignant melanoma. This review article therefore looks at the role of ultraviolet radiation in causing skin cancer; summarizes the available evidence on both the beneficial and harmful effects of sunscreen use; and concludes with practical advice on how we might advise our patients to best protect themselves from photocarcinogenesis.
Introduction “Slip, Slop, Slap, Seek and Slide” is one of many campaigns worldwide designed to encourage the use of sunscreens among the public.1 As the popular belief has been that sunscreens protect us from the damaging effects of the sun, such campaigns have implored us to “slop on the sunscreen” as a key way of gaining such protection. The topic of sunlight and sunscreens raises considerable interest within the media. Sunlight stimulates a multitude of important biological effects on skin; causing sunburn, photoaging, photocarcinogenesis, and immune suppression. Both academic and media interest has centered on the continual rapid rise in the incidence of malignant melanoma – largely due to this form of skin cancer carrying with it the highest mortality rate and affecting the younger demographic.2 Given that sales of sunscreen have also increased over the same time period,3 is sunscreen providing the protection it should? Improving our understanding of how to protect ourselves from skin cancer is of huge public health significance. What Is the Danger? Epidemiological studies initially revealed that sunlight is a significant risk factor for skin cancer. First, melanoma is proportionally more common in those living nearer to the equator.4 Secondly, those with skin types 1, 2, and 3 – who have less melanin pigment to absorb the ultraviolet (UV) light – are more susceptible. Thirdly, non-melanoma skin cancers and lentigo maligna melanoma are commonly found on sun-exposed sites such as the face, and superfiª 2014 The International Society of Dermatology
cial spreading melanomas are commonly located on the back and lower leg of a male and female, respectively.5 Sunlight reaching the Earth's surface is composed of differing wavelengths of the electromagnetic spectrum, ranging from infrared through to visible and UV light. It is the UV portion of the spectrum, specifically UVB and UVA (between 280 and 400 nm), that is the most damaging to our skin.6 This UV light is able to cause DNA damage, initiating the formation of genetic mutations which may, for example, progress into the “hallmarks of cancer”.7 Such mutations may be caused by UV-induced free radical damage6 or by the formation of pyrimidine dimers. For example, when nucleotide excision repair fails to recognize that a pyrimidine dimer has transformed from a CC to a TT dimer, this may result in loss of a critical tumor suppressor gene.8 UVA constitutes 95% of the UV energy reaching the equator. Its longer wavelength explains why UVA is able to penetrate into deeper layers of the skin than UVB, with a greater percentage penetrating the basal epidermis cells.3 Recent studies have contradicted previous beliefs that UVA is not significant in the pathogenesis of cancer, with data suggesting a role for UVA in melanoma.9 UVA potentiates the carcinogenic effects of UVB and stimulates generation of carcinogenic free radicals within the skin. In contrast to UVA, only a small proportion of UV light that penetrates our skin is of the UVB spectrum. Despite this, the specific properties of UVB implicate it as the predominant factor in the pathogenesis of melanoma, basal cell, and squamous cell skin cancers. UV radiation, particularly UVB, may stimulate the inflammatory erythema commonly referred to as sunburn, International Journal of Dermatology 2014, 53, 1319–1323
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Table 1 UK incidence and mortality of skin cancer
Non-melanoma skin cancer Melanoma
UK incidence (2010)
UK mortality (2010)
99 549 12 818
585 2209
and the public commonly attempt to avoid sunburn by applying sunscreen. Importantly, evidence shows a strong positive correlation between a history of sunburn and the incidence of both melanoma and non-melanoma skin cancers.10,11 However, protecting ourselves from sunburn is unlikely to be sufficient, as lower doses of UV light may be carcinogenic. Therefore, it is clear that there is a strong association between sunlight exposure and skin cancer. The importance of these cancers in the UK is depicted in Table 1.2 The high mortality rate of melanoma highlights the importance of protecting ourselves from the sun. Melanoma disproportionally affects the younger population, with one-third of cases occurring in those under 55. Finally, the incidence rates across all ages is rising more than that of any other adult cancer.2 It would appear that we are not doing enough to protect ourselves from the damaging effects of the sun. How Should We Use Sunscreen? The ideal sunscreen would prevent 100% of all wavelengths of UV radiation from penetrating the skin and would provide long-term protection without the need for reapplication. Unfortunately, such sunscreen does not exist, and to maximize the protection sunscreen may provide, it is important to understand how to use it effectively. There are many different types of sunscreen, each containing a combination of agents with different chemical groups, designed to either absorb or reflect a proportion of the incoming UV energy. A significant factor affecting the protection sunscreens provide is the sun protection factor (SPF). This is defined as the ratio of UV radiation required to produce minimal sunburn with sunscreen, compared to without it. This means that the application of an appropriate amount of SPF 5 sunscreen to an individual who would burn within one hour without it, would instead only burn after five hours. It would therefore seem logical that a higher SPF would lead to greater protection from the damaging effects of the sun; but this is not necessarily the case.12 This is, in part, due to factors other than the SPF that contribute to the effect of a sunscreen, such as the amount applied, the frequency of reapplication, and the skin type of the individual. BehavInternational Journal of Dermatology 2014, 53, 1319–1323
ior is a key factor: individuals who apply a higher SPF may become complacent and so tend to spend more time in the sunlight (including at noon when doses of UV radiation are highest), while reapplying the sunscreen less frequently. In calculating the SPF, the Food and Drug Administration (FDA) uses a dose of 2.2 mg/cm2 of exposed skin. However, in practice individuals apply as little as onequarter of this recommended dose.13 This may have the effect of reducing the SPF factor by the fourth route – with the effect of reducing, for example, SPF 100 to SPF 3.2.14 Of additional importance is the timing of application and reapplication. Although the exact recommendations vary between studies, it is clear that sunscreen is not applied often enough by the general public and that applying sunscreen once is insufficient. One recommendation is that sunscreen should be applied 30 minutes before going out into the sun and then reapplied both 30 minutes after sun exposure begins and after any activity that may remove the sunscreen.15 Sunscreens are effective against only a proportion of the entire UV wavelength spectrum, and the specific wavelengths covered will affect the protection that the sunscreen provides against sunlight-induced damage. As discussed previously, both UVA and UVB have been causally linked to inducing skin cancer; therefore, sunscreens should aim to cover this entire range of wavelengths. Despite this, the SPF value mainly refers to the protection against UVB, as UVA does not produce significant erythema. More recent ‘broad-spectrum’ sunscreen products attempt to cover both UVB and short-wave UVA. In the UK, there is now a five-star rating system based on the reduction of UVA radiation penetration, and new guidelines have been announced by the FDA in the USA. However, some experts argue that the protection offered by many of these products against UVA remains insufficient. Indeed, this broad-spectrum cover has been the subject of nine lawsuits against sunscreen manufacturers. When applied appropriately, there is evidence that sunscreen protects the individual from absorbing a proportion of the UV radiation and therefore offers a degree of protection from sunburn and DNA damage.16 This has been shown to reduce many of the signs of aging, including pigmentation, collagen loss, and blood vessel dilatation.17 However, to what extent does this afford protection against skin cancer? Protection Against Skin Cancer? There is some conflicting evidence regarding the role of sunscreen in skin cancer prevention. While a mathematical model predicts that regular sunscreen use would greatly reduce the lifetime incidence of non-melanoma skin canª 2014 The International Society of Dermatology
Maslin
cers,18 clinical trials have not been as clear. A randomized controlled trial found the daily use of sunscreen over 4½ years significantly reduced the incidence of squamous cell carcinoma but not of basal cell carcinoma.19 More recent studies have had similar results – the risk of squamous cell carcinoma is decreased, but the results for basal cell carcinoma are equivocal. However, the major controversy surrounds the link between sunscreen and melanoma. Initially, it was assumed that sunscreen would reduce melanoma incidence by blocking harmful UV radiation. However, there has been evidence from case–control studies to suggest that sunscreen is, in fact, a risk factor for melanoma formation;20 although a quantitative review of the data found no such association.21 As such, the results of case– control and cohort studies has so far been unhelpful in resolving this debate. Importantly, 10-year follow-up results from a randomization trial on sunscreen application have recently been published.22 The population applying sunscreen daily, as opposed to on a discretionary basis, developed significantly fewer melanomas – 11 melanomas in 812 participants, compared to 22 of 809 (P = 0.051). In addition, there were three invasive melanomas in the treatment arm, compared to 11 in the comparison group (P = 0.045). This study is useful and provides evidence for a possible benefit of sunscreen use in melanoma. Unfortunately, however, meta-analyses have been unable to resolve the conflict in results of other studies, and further evidence is awaited.23 It is important to try to understand reasons for the disparity in these results. One explanation is the presence of confounding risk factors in many of the studies. For example, fairer-skinned individuals may be more likely to use sunscreen and are more likely to develop skin cancer. Other factors such as childhood UV exposure or previous sunburns were often not taken into account. Additionally, such results may be accounted for by the improper application of sunscreen or by the increased amount of time that those applying sunscreen spend in the sun.24 Finally, the sunscreens used in previous studies are of different formulations to modern sunscreens available today and provided less UVB and UVA protection. However, due to the possibility that sunscreens have a causal effect in melanoma development, it is important to explore the possible explanations for this association. First, an association between reduced vitamin D levels and cancers, including skin cancer, has been identified. As UVB radiation is required to produce vitamin D3 in the skin, the hypothesis is that sunscreen may cause skin cancer by reducing vitamin D synthesis. Experts disagree on whether small doses of unprotected sun exposure each week, to stimulate vitamin D synthesis, will
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increase or decrease the risk of skin cancer in the individual.25 Furthermore, there are other ingredients in sunscreens, which have the potential to cause harm. Retinyl palmitate, a form of vitamin A added to many sunscreens, has been linked with cancer formation. However, current evidence “fails to demonstrate … that retinyl palmitate imparts an increased risk of skin cancer”.26 This same review concluded that oxybenzone, zinc oxide, and titanium oxide – all found in sunscreens – are unlikely to be harmful. One function of sunscreen is to reduce the formation of damaging free radical species, which may have a role in melanoma formation. However, the chemicals within sunscreen products release free radicals themselves. In most situations, the result is that sunscreens reduce overall free radical formation. However, when sunscreens are not applied effectively the balance may tip in favor of excess production of these reactive oxygen species, resulting in predisposition to their carcinogenic effects.27 This assessment of the evidence helps us to understand the recent FDA guidelines.28 Only the labels of broadspectrum sunscreens (those passing the standard UVA and UVB protection tests) with an SPF value of at least 15, will state that they not only protect against sunburn but, if used as directed with other sun protection measures, can reduce the risk of cancer and early skin aging. Higher SPF values, up to a maximum of 50+, will indicate a greater level of protection. Conclusion: The Burning Issue of Sunscreen Education It remains to be proven whether sunscreen protects us from the deadliest skin cancer, and whether there is any harm in applying sunscreen regularly. One view is that “individuals should be advised not to use sunscreen, but rather to … set strict limits on the time they spend in the sun”.12 In contrast, other experts suggest that, “despite the lack of evidence demonstrating the efficacy of modern sunscreens in preventing melanoma … it would be irresponsible not to encourage their use”.29 Finally, the International Agency for Research on Cancer has stated, “sunscreens should not be the first choice for skin cancer prevention and should not be used as the sole agent for protection against the sun”.28 Therefore, current campaigns such as ‘Slip, Slop, Slap, Seek and Slide’ are sending out the right message: to optimize protection from the damaging effects of the sun we should not just ‘slop on the sunscreen’ but also ‘slip on a t-shirt, slap on a hat, seek shade, and slide on sunglasses’. Importantly, none of these steps is sufficient on their own, and all should be carried out together.
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To this end, education of the population is likely to be the most effective intervention. It is extremely important to educate the public regularly about: (i) the risks of sunlight or sunbeds in causing skin cancer; (ii) how to recognize a malignant melanoma; (iii) the role and use of sunscreen; and (vi) the importance of methods other than sunscreen, such as avoiding peak sun, seeking shade, and wearing protective clothing. These messages should be targeted to all age groups and perhaps particularly to young adults, who may be at particularly high risk. In a study of 10,000 teenagers, only two-fifths admitted to the use of sunscreen, while 80% experienced at least one episode of sunburn in the previous summer; implying that the majority are not using sunscreen effectively.30 An area currently neglected is regarding the education of how to apply sunscreen effectively. This review has highlighted the significance of applying and reapplying the correct amounts of sunscreen and of choosing a product with UVA cover. A survey of 423 individuals found that less than a third of respondents knew to apply sunscreen 30 minutes before going into the sun, and a similar minority knew how to reapply the sunscreen appropriately. Furthermore, just 18% knew the correct dose of sunscreen to apply.31 Does sunscreen protect us? An assessment of the current evidence shows no conclusive data to demonstrate that sunscreens harm us. The degree of protection provided by modern sunscreens is more difficult to assess, but it is likely that any protection will be significantly enhanced when sunscreen is applied appropriately and when use of such sunscreen does not encourage our sunseeking behavior. However, studies in the future need to address whether modern sunscreens are protective in the way the public are actually using them. References 1 SunSmart Campaign. http://www.sunsmart.com.au/ news_and_media/media_campaigns/slip-slop-slapseek-and-slide. [Accessed October 7, 2013]. 2 Skin cancer statistics. http://info.cancerresearchuk.org/ cancerstats/types/skin/incidence. [Accessed October 7, 2013]. 3 Euromonitor Report: Suncare in the US, 2013. http:// www.euromonitor.com/sun-care. [Accessed January 16, 2014]. 4 Gallagher RP, Hill GB, Bajdik CD, et al. Sunlight exposure, pigmentation factors, and risk of nonmelanocytic skin cancer. II. Squamous cell carcinoma. Arch Dermatol 1995; 131: 164–169. 5 Elwood JM, Lee JA, Walter SD, et al. Relationship of melanoma and other skin cancer mortality to latitude and ultraviolet radiation in the United States and Canada. Int J Epidemiol 1974; 3: 325–332. International Journal of Dermatology 2014, 53, 1319–1323
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6 Naylor M, Farmer K. Sun damage and prevention. Electronic Textbook of Dermatology: The Internet Dermatology Society, 1995. http://telemedicine.org/ sundam/sundam2.4.1.html. [Accessed January 16, 2014]. 7 Hanahan D, Weinbery RA. The hallmarks of cancer. Cell 2000; 100: 57–70. 8 Goodsell D. The molecular perspective: ultraviolet light and pyrimidine dimers. Oncologist 2001; 6: 298–299. 9 Wang SQ, Setlow R, Berwick M, et al. Ultraviolet A and melanoma: a review. J Am Acad Dermatol 2001; 44: 837–846. 10 Green AC, et al. Sunburn and malignant melanoma. Br J Cancer 1985; 51: 393–397. 11 Green A, Siskind V, Bain C, et al. Sunlight exposure, pigmentary factors, and risk of nonmelanocytic skin cancer. I. Basal cell carcinoma. Arch Dermatol 1995; 131: 157–163. 12 Autier P. Sunscreen abuse for intentional sun exposure. Br J Dermatol 2009; 161(Suppl. 3): 40–45. 13 Reich A, Harupa M, Bury M, et al. Application of sunscreen preparation: a need to change the regulations. Photodermatol Photoimmunol Photomed 2009; 25: 242– 244. 14 Schalka S, dos Reis VM, Cuce LC. The influence of the amount of sunscreen applied and its sun protection factor (SPF): evaluation of two sunscreens including the same ingredients at different concentrations. Photodermatol Photoimmunol Photomed 2009; 25: 175–180. 15 Diffey B. When should sunscreen be reapplied? J Am Acad Dermatol 2001; 45: 882–885. 16 Freeman SE, Ley RD, Ley KD. Sunscreen protection against UV-induced pyrimidine dimers in DNA of human skin in situ. Photodermatol 1988; 5: 243–247. 17 Seite S, Colige A, Piquemal-Vivenot P, et al. A full-UV spectrum absorbing daily use cream protects human skin against biological changes occurring in photoaging. Photodermatol Photoimmunol Photomed 2000; 16: 147– 155. 18 Stern RS, Weinstein MC, Baker SG, et al. Risk reduction for nonmelanoma skin cancer with childhood sunscreen use. Arch Dermatol 1986; 122: 537–545. 19 Green A, Williams G, Neale R, 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: 723–729. 20 Westerdahl J, Ingvar C, M^ asb€ ack A, et al. Sunscreen use and malignant melanoma. Int J Cancer 2000; 87: 145– 150. 21 Dennis LK, Beane Freeman LE, VanBeek MJ. Sunscreen use and the risk for melanoma: a quantitative review. Ann Intern Med 2003; 139: 966–978. 22 Green AC, Williams GM, Logan V, et al. Reduced melanoma after sunscreen use: randomized trial follow-up. J Clin Oncol 2011; 29: 257–263.
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23 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: 1173–1177. 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: 1–5. 25 Grant W. An estimate of premature cancer mortality in the U.S. due to inadequate doses of solar ultraviolet-B radiation. Cancer 2002; 94: 1867–1875. 26 Burnett M, Wang S. Current sunscreen controversies: a critical review. Photodermatol Photoimmunol Photomed 2011; 27: 58–67. 27 Hanson K. Sunscreen enhancement of UV-induced reactive oxygen species in the skin. Free Radic Biol Med 2006; 41: 1205–1212.
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28 U.S. Department of Health and Human Services: Labeling and effectiveness testing; sunscreen drug products for over-the-counter human use. Fed Regist 2011; 76: 35620–35665. 29 Diffey B. Sunscreens as a preventative measure in melanoma: an evidence-based approach or the precautionary principle? Br J Dermatol 2009; 161(Suppl. 3): 25–27. 30 Geller AC, Oliveria SA, Bishop M, et al. Study of health outcomes in school children: key challenges and lessons learned from the Framingham Schools Natural History of Nevi Study. J Sch Health 2007; 77: 312–318. 31 Wang SQ, Dusza SW. Assessment of sunscreen knowledge: a pilot survey. Br J Dermatol 2009; 161 (Suppl. 3): 28–32.
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Do suncreens protect us? Douglas L. Maslin, MA, MB, BCHIR
Addenbrooke’s Hospital, Cambridge, UK
Abstract Sunlight stimulates a multitude of important biological effects on skin, causing, amongst
Correspondence Douglas Maslin, MA, MB, BCHIR Downing College Cambridge CB2 1DQ UK E-mail: [email protected] Conflicts of interest: None.
other pathological changes, photocarcinogenesis. Sunscreens are designed to provide protection against these harmful properties of ultraviolet radiation, and public health campaigns have been employed to encourage their use. Despite this, there has been a continued rise in the incidence and mortality of the most harmful skin cancer, malignant melanoma. This review article therefore looks at the role of ultraviolet radiation in causing skin cancer; summarizes the available evidence on both the beneficial and harmful effects of sunscreen use; and concludes with practical advice on how we might advise our patients to best protect themselves from photocarcinogenesis.
Introduction “Slip, Slop, Slap, Seek and Slide” is one of many campaigns worldwide designed to encourage the use of sunscreens among the public.1 As the popular belief has been that sunscreens protect us from the damaging effects of the sun, such campaigns have implored us to “slop on the sunscreen” as a key way of gaining such protection. The topic of sunlight and sunscreens raises considerable interest within the media. Sunlight stimulates a multitude of important biological effects on skin; causing sunburn, photoaging, photocarcinogenesis, and immune suppression. Both academic and media interest has centered on the continual rapid rise in the incidence of malignant melanoma – largely due to this form of skin cancer carrying with it the highest mortality rate and affecting the younger demographic.2 Given that sales of sunscreen have also increased over the same time period,3 is sunscreen providing the protection it should? Improving our understanding of how to protect ourselves from skin cancer is of huge public health significance. What Is the Danger? Epidemiological studies initially revealed that sunlight is a significant risk factor for skin cancer. First, melanoma is proportionally more common in those living nearer to the equator.4 Secondly, those with skin types 1, 2, and 3 – who have less melanin pigment to absorb the ultraviolet (UV) light – are more susceptible. Thirdly, non-melanoma skin cancers and lentigo maligna melanoma are commonly found on sun-exposed sites such as the face, and superfiª 2014 The International Society of Dermatology
cial spreading melanomas are commonly located on the back and lower leg of a male and female, respectively.5 Sunlight reaching the Earth's surface is composed of differing wavelengths of the electromagnetic spectrum, ranging from infrared through to visible and UV light. It is the UV portion of the spectrum, specifically UVB and UVA (between 280 and 400 nm), that is the most damaging to our skin.6 This UV light is able to cause DNA damage, initiating the formation of genetic mutations which may, for example, progress into the “hallmarks of cancer”.7 Such mutations may be caused by UV-induced free radical damage6 or by the formation of pyrimidine dimers. For example, when nucleotide excision repair fails to recognize that a pyrimidine dimer has transformed from a CC to a TT dimer, this may result in loss of a critical tumor suppressor gene.8 UVA constitutes 95% of the UV energy reaching the equator. Its longer wavelength explains why UVA is able to penetrate into deeper layers of the skin than UVB, with a greater percentage penetrating the basal epidermis cells.3 Recent studies have contradicted previous beliefs that UVA is not significant in the pathogenesis of cancer, with data suggesting a role for UVA in melanoma.9 UVA potentiates the carcinogenic effects of UVB and stimulates generation of carcinogenic free radicals within the skin. In contrast to UVA, only a small proportion of UV light that penetrates our skin is of the UVB spectrum. Despite this, the specific properties of UVB implicate it as the predominant factor in the pathogenesis of melanoma, basal cell, and squamous cell skin cancers. UV radiation, particularly UVB, may stimulate the inflammatory erythema commonly referred to as sunburn, International Journal of Dermatology 2014, 53, 1319–1323
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Table 1 UK incidence and mortality of skin cancer
Non-melanoma skin cancer Melanoma
UK incidence (2010)
UK mortality (2010)
99 549 12 818
585 2209
and the public commonly attempt to avoid sunburn by applying sunscreen. Importantly, evidence shows a strong positive correlation between a history of sunburn and the incidence of both melanoma and non-melanoma skin cancers.10,11 However, protecting ourselves from sunburn is unlikely to be sufficient, as lower doses of UV light may be carcinogenic. Therefore, it is clear that there is a strong association between sunlight exposure and skin cancer. The importance of these cancers in the UK is depicted in Table 1.2 The high mortality rate of melanoma highlights the importance of protecting ourselves from the sun. Melanoma disproportionally affects the younger population, with one-third of cases occurring in those under 55. Finally, the incidence rates across all ages is rising more than that of any other adult cancer.2 It would appear that we are not doing enough to protect ourselves from the damaging effects of the sun. How Should We Use Sunscreen? The ideal sunscreen would prevent 100% of all wavelengths of UV radiation from penetrating the skin and would provide long-term protection without the need for reapplication. Unfortunately, such sunscreen does not exist, and to maximize the protection sunscreen may provide, it is important to understand how to use it effectively. There are many different types of sunscreen, each containing a combination of agents with different chemical groups, designed to either absorb or reflect a proportion of the incoming UV energy. A significant factor affecting the protection sunscreens provide is the sun protection factor (SPF). This is defined as the ratio of UV radiation required to produce minimal sunburn with sunscreen, compared to without it. This means that the application of an appropriate amount of SPF 5 sunscreen to an individual who would burn within one hour without it, would instead only burn after five hours. It would therefore seem logical that a higher SPF would lead to greater protection from the damaging effects of the sun; but this is not necessarily the case.12 This is, in part, due to factors other than the SPF that contribute to the effect of a sunscreen, such as the amount applied, the frequency of reapplication, and the skin type of the individual. BehavInternational Journal of Dermatology 2014, 53, 1319–1323
ior is a key factor: individuals who apply a higher SPF may become complacent and so tend to spend more time in the sunlight (including at noon when doses of UV radiation are highest), while reapplying the sunscreen less frequently. In calculating the SPF, the Food and Drug Administration (FDA) uses a dose of 2.2 mg/cm2 of exposed skin. However, in practice individuals apply as little as onequarter of this recommended dose.13 This may have the effect of reducing the SPF factor by the fourth route – with the effect of reducing, for example, SPF 100 to SPF 3.2.14 Of additional importance is the timing of application and reapplication. Although the exact recommendations vary between studies, it is clear that sunscreen is not applied often enough by the general public and that applying sunscreen once is insufficient. One recommendation is that sunscreen should be applied 30 minutes before going out into the sun and then reapplied both 30 minutes after sun exposure begins and after any activity that may remove the sunscreen.15 Sunscreens are effective against only a proportion of the entire UV wavelength spectrum, and the specific wavelengths covered will affect the protection that the sunscreen provides against sunlight-induced damage. As discussed previously, both UVA and UVB have been causally linked to inducing skin cancer; therefore, sunscreens should aim to cover this entire range of wavelengths. Despite this, the SPF value mainly refers to the protection against UVB, as UVA does not produce significant erythema. More recent ‘broad-spectrum’ sunscreen products attempt to cover both UVB and short-wave UVA. In the UK, there is now a five-star rating system based on the reduction of UVA radiation penetration, and new guidelines have been announced by the FDA in the USA. However, some experts argue that the protection offered by many of these products against UVA remains insufficient. Indeed, this broad-spectrum cover has been the subject of nine lawsuits against sunscreen manufacturers. When applied appropriately, there is evidence that sunscreen protects the individual from absorbing a proportion of the UV radiation and therefore offers a degree of protection from sunburn and DNA damage.16 This has been shown to reduce many of the signs of aging, including pigmentation, collagen loss, and blood vessel dilatation.17 However, to what extent does this afford protection against skin cancer? Protection Against Skin Cancer? There is some conflicting evidence regarding the role of sunscreen in skin cancer prevention. While a mathematical model predicts that regular sunscreen use would greatly reduce the lifetime incidence of non-melanoma skin canª 2014 The International Society of Dermatology
Maslin
cers,18 clinical trials have not been as clear. A randomized controlled trial found the daily use of sunscreen over 4½ years significantly reduced the incidence of squamous cell carcinoma but not of basal cell carcinoma.19 More recent studies have had similar results – the risk of squamous cell carcinoma is decreased, but the results for basal cell carcinoma are equivocal. However, the major controversy surrounds the link between sunscreen and melanoma. Initially, it was assumed that sunscreen would reduce melanoma incidence by blocking harmful UV radiation. However, there has been evidence from case–control studies to suggest that sunscreen is, in fact, a risk factor for melanoma formation;20 although a quantitative review of the data found no such association.21 As such, the results of case– control and cohort studies has so far been unhelpful in resolving this debate. Importantly, 10-year follow-up results from a randomization trial on sunscreen application have recently been published.22 The population applying sunscreen daily, as opposed to on a discretionary basis, developed significantly fewer melanomas – 11 melanomas in 812 participants, compared to 22 of 809 (P = 0.051). In addition, there were three invasive melanomas in the treatment arm, compared to 11 in the comparison group (P = 0.045). This study is useful and provides evidence for a possible benefit of sunscreen use in melanoma. Unfortunately, however, meta-analyses have been unable to resolve the conflict in results of other studies, and further evidence is awaited.23 It is important to try to understand reasons for the disparity in these results. One explanation is the presence of confounding risk factors in many of the studies. For example, fairer-skinned individuals may be more likely to use sunscreen and are more likely to develop skin cancer. Other factors such as childhood UV exposure or previous sunburns were often not taken into account. Additionally, such results may be accounted for by the improper application of sunscreen or by the increased amount of time that those applying sunscreen spend in the sun.24 Finally, the sunscreens used in previous studies are of different formulations to modern sunscreens available today and provided less UVB and UVA protection. However, due to the possibility that sunscreens have a causal effect in melanoma development, it is important to explore the possible explanations for this association. First, an association between reduced vitamin D levels and cancers, including skin cancer, has been identified. As UVB radiation is required to produce vitamin D3 in the skin, the hypothesis is that sunscreen may cause skin cancer by reducing vitamin D synthesis. Experts disagree on whether small doses of unprotected sun exposure each week, to stimulate vitamin D synthesis, will
ª 2014 The International Society of Dermatology
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increase or decrease the risk of skin cancer in the individual.25 Furthermore, there are other ingredients in sunscreens, which have the potential to cause harm. Retinyl palmitate, a form of vitamin A added to many sunscreens, has been linked with cancer formation. However, current evidence “fails to demonstrate … that retinyl palmitate imparts an increased risk of skin cancer”.26 This same review concluded that oxybenzone, zinc oxide, and titanium oxide – all found in sunscreens – are unlikely to be harmful. One function of sunscreen is to reduce the formation of damaging free radical species, which may have a role in melanoma formation. However, the chemicals within sunscreen products release free radicals themselves. In most situations, the result is that sunscreens reduce overall free radical formation. However, when sunscreens are not applied effectively the balance may tip in favor of excess production of these reactive oxygen species, resulting in predisposition to their carcinogenic effects.27 This assessment of the evidence helps us to understand the recent FDA guidelines.28 Only the labels of broadspectrum sunscreens (those passing the standard UVA and UVB protection tests) with an SPF value of at least 15, will state that they not only protect against sunburn but, if used as directed with other sun protection measures, can reduce the risk of cancer and early skin aging. Higher SPF values, up to a maximum of 50+, will indicate a greater level of protection. Conclusion: The Burning Issue of Sunscreen Education It remains to be proven whether sunscreen protects us from the deadliest skin cancer, and whether there is any harm in applying sunscreen regularly. One view is that “individuals should be advised not to use sunscreen, but rather to … set strict limits on the time they spend in the sun”.12 In contrast, other experts suggest that, “despite the lack of evidence demonstrating the efficacy of modern sunscreens in preventing melanoma … it would be irresponsible not to encourage their use”.29 Finally, the International Agency for Research on Cancer has stated, “sunscreens should not be the first choice for skin cancer prevention and should not be used as the sole agent for protection against the sun”.28 Therefore, current campaigns such as ‘Slip, Slop, Slap, Seek and Slide’ are sending out the right message: to optimize protection from the damaging effects of the sun we should not just ‘slop on the sunscreen’ but also ‘slip on a t-shirt, slap on a hat, seek shade, and slide on sunglasses’. Importantly, none of these steps is sufficient on their own, and all should be carried out together.
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To this end, education of the population is likely to be the most effective intervention. It is extremely important to educate the public regularly about: (i) the risks of sunlight or sunbeds in causing skin cancer; (ii) how to recognize a malignant melanoma; (iii) the role and use of sunscreen; and (vi) the importance of methods other than sunscreen, such as avoiding peak sun, seeking shade, and wearing protective clothing. These messages should be targeted to all age groups and perhaps particularly to young adults, who may be at particularly high risk. In a study of 10,000 teenagers, only two-fifths admitted to the use of sunscreen, while 80% experienced at least one episode of sunburn in the previous summer; implying that the majority are not using sunscreen effectively.30 An area currently neglected is regarding the education of how to apply sunscreen effectively. This review has highlighted the significance of applying and reapplying the correct amounts of sunscreen and of choosing a product with UVA cover. A survey of 423 individuals found that less than a third of respondents knew to apply sunscreen 30 minutes before going into the sun, and a similar minority knew how to reapply the sunscreen appropriately. Furthermore, just 18% knew the correct dose of sunscreen to apply.31 Does sunscreen protect us? An assessment of the current evidence shows no conclusive data to demonstrate that sunscreens harm us. The degree of protection provided by modern sunscreens is more difficult to assess, but it is likely that any protection will be significantly enhanced when sunscreen is applied appropriately and when use of such sunscreen does not encourage our sunseeking behavior. However, studies in the future need to address whether modern sunscreens are protective in the way the public are actually using them. References 1 SunSmart Campaign. http://www.sunsmart.com.au/ news_and_media/media_campaigns/slip-slop-slapseek-and-slide. [Accessed October 7, 2013]. 2 Skin cancer statistics. http://info.cancerresearchuk.org/ cancerstats/types/skin/incidence. [Accessed October 7, 2013]. 3 Euromonitor Report: Suncare in the US, 2013. http:// www.euromonitor.com/sun-care. [Accessed January 16, 2014]. 4 Gallagher RP, Hill GB, Bajdik CD, et al. Sunlight exposure, pigmentation factors, and risk of nonmelanocytic skin cancer. II. Squamous cell carcinoma. Arch Dermatol 1995; 131: 164–169. 5 Elwood JM, Lee JA, Walter SD, et al. Relationship of melanoma and other skin cancer mortality to latitude and ultraviolet radiation in the United States and Canada. Int J Epidemiol 1974; 3: 325–332. International Journal of Dermatology 2014, 53, 1319–1323
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6 Naylor M, Farmer K. Sun damage and prevention. Electronic Textbook of Dermatology: The Internet Dermatology Society, 1995. http://telemedicine.org/ sundam/sundam2.4.1.html. [Accessed January 16, 2014]. 7 Hanahan D, Weinbery RA. The hallmarks of cancer. Cell 2000; 100: 57–70. 8 Goodsell D. The molecular perspective: ultraviolet light and pyrimidine dimers. Oncologist 2001; 6: 298–299. 9 Wang SQ, Setlow R, Berwick M, et al. Ultraviolet A and melanoma: a review. J Am Acad Dermatol 2001; 44: 837–846. 10 Green AC, et al. Sunburn and malignant melanoma. Br J Cancer 1985; 51: 393–397. 11 Green A, Siskind V, Bain C, et al. Sunlight exposure, pigmentary factors, and risk of nonmelanocytic skin cancer. I. Basal cell carcinoma. Arch Dermatol 1995; 131: 157–163. 12 Autier P. Sunscreen abuse for intentional sun exposure. Br J Dermatol 2009; 161(Suppl. 3): 40–45. 13 Reich A, Harupa M, Bury M, et al. Application of sunscreen preparation: a need to change the regulations. Photodermatol Photoimmunol Photomed 2009; 25: 242– 244. 14 Schalka S, dos Reis VM, Cuce LC. The influence of the amount of sunscreen applied and its sun protection factor (SPF): evaluation of two sunscreens including the same ingredients at different concentrations. Photodermatol Photoimmunol Photomed 2009; 25: 175–180. 15 Diffey B. When should sunscreen be reapplied? J Am Acad Dermatol 2001; 45: 882–885. 16 Freeman SE, Ley RD, Ley KD. Sunscreen protection against UV-induced pyrimidine dimers in DNA of human skin in situ. Photodermatol 1988; 5: 243–247. 17 Seite S, Colige A, Piquemal-Vivenot P, et al. A full-UV spectrum absorbing daily use cream protects human skin against biological changes occurring in photoaging. Photodermatol Photoimmunol Photomed 2000; 16: 147– 155. 18 Stern RS, Weinstein MC, Baker SG, et al. Risk reduction for nonmelanoma skin cancer with childhood sunscreen use. Arch Dermatol 1986; 122: 537–545. 19 Green A, Williams G, Neale R, 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: 723–729. 20 Westerdahl J, Ingvar C, M^ asb€ ack A, et al. Sunscreen use and malignant melanoma. Int J Cancer 2000; 87: 145– 150. 21 Dennis LK, Beane Freeman LE, VanBeek MJ. Sunscreen use and the risk for melanoma: a quantitative review. Ann Intern Med 2003; 139: 966–978. 22 Green AC, Williams GM, Logan V, et al. Reduced melanoma after sunscreen use: randomized trial follow-up. J Clin Oncol 2011; 29: 257–263.
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23 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: 1173–1177. 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: 1–5. 25 Grant W. An estimate of premature cancer mortality in the U.S. due to inadequate doses of solar ultraviolet-B radiation. Cancer 2002; 94: 1867–1875. 26 Burnett M, Wang S. Current sunscreen controversies: a critical review. Photodermatol Photoimmunol Photomed 2011; 27: 58–67. 27 Hanson K. Sunscreen enhancement of UV-induced reactive oxygen species in the skin. Free Radic Biol Med 2006; 41: 1205–1212.
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28 U.S. Department of Health and Human Services: Labeling and effectiveness testing; sunscreen drug products for over-the-counter human use. Fed Regist 2011; 76: 35620–35665. 29 Diffey B. Sunscreens as a preventative measure in melanoma: an evidence-based approach or the precautionary principle? Br J Dermatol 2009; 161(Suppl. 3): 25–27. 30 Geller AC, Oliveria SA, Bishop M, et al. Study of health outcomes in school children: key challenges and lessons learned from the Framingham Schools Natural History of Nevi Study. J Sch Health 2007; 77: 312–318. 31 Wang SQ, Dusza SW. Assessment of sunscreen knowledge: a pilot survey. Br J Dermatol 2009; 161 (Suppl. 3): 28–32.
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