Abstract
Photoprotection is a critical health prevention strategy to reduce the deleterious effects of ultraviolet radiation (UVR) and visible light (VL). Methods of photoprotection are reviewed in this paper, with an emphasis on sunscreen. The most appropriate sunscreen formulation for personal use depends on several factors. Active sunscreen ingredients vary in their protective effect over the UVR and VL spectrum. There are dermatologic diseases that cause photosensitivity or that are aggravated by a particular action spectrum. In these situations, sunscreen suggestions can address the specific concern. Sunscreen does not represent a single entity. Appropriate personalized sunscreen selection is critical to improve compliance and clinical outcomes. Health care providers can facilitate informed product selection with awareness of evolving sunscreen formulations and counseling patients on appropriate use. This review aims to summarize different forms of photoprotection, discuss absorption of sunscreen ingredients, possible adverse effects, and disease-specific preferences for chemical, physical or oral agents that may decrease UVR and VL harmful effects.
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Introduction
Photoprotection is a critical health prevention strategy to reduce the deleterious effects of ultraviolet radiation (UVR) and visible light (VL). Photoprotection may prevent and mitigate sunburns, tanning, photoaging, hyperpigmentation, skin cancers, as well as flares of photodermatoses and photoaggravated skin diseases [1, 2]. Photoprotection includes sun avoidance, use of clothing, hats and sunglasses, seeking shade and sunscreen use. The aims of this review are to summarize these different forms of photoprotection with a focus on sunscreens, as the growing arsenal of sunscreen compounds necessitates an update. Sunscreen ingredients, their absorption, possible dermatologic adverse effects, and disease-specific preferences for sunscreens will be reviewed (Table 1). Physicians can facilitate informed product selection by discussing the benefits and possible adverse effects of various sunscreen formulations.
Ultraviolet radiation
Clinically relevant ultraviolet (UV) wavelengths are UVB (290–320 nm) and UVA (320–400 nm) [3]. At temperate latitudes UVB exposure is greatest in the summer, causing acute changes (i.e., tanning, sunburn) as well as DNA damage and photocarcinogenesis [4, 5]. UVA exposure is more constant throughout the year, causing DNA damage and degradation of elastin and collagen [4, 6,7,8] leading to photoaging, hyperpigmentation, and photocarcinogenesis. Broad-spectrum protection is required to prevent the adverse effects of UV radiation (UVR) [9, 10].
Visible light (VL)
While UVR accounts for 5% of terrestrial sunlight, 50% is visible light (VL; 400–700 nm) [2]. Exposure is insignificantly increased by electronic devices. Recent literature highlights the importance of protection from VL [2]. VL is part of the action spectrum for chronic actinic dermatitis [11], solar urticaria [12, 13], and the primary action spectrum for porphyrias [14], meaning these wavelengths typically trigger flares of the conditions. VL also worsens melasma, post-inflammatory hyperpigmentation, and maturational dyschromia [15,16,17,18].
Types of photoprotection
People should be encouraged to avoid outdoor activities during peak sun hours, seek shade, apply sunscreen, wear sun protective clothing, and sunglasses [19].
Sunscreen
Sunscreen ingredients decrease UVR and VL from reaching the skin. UVR is absorbed or scattered and VL is reflected. Many sunscreens combine chemical (organic) and physical (inorganic) ingredients to maximize UV protection [20]. The American Academy of Dermatology (AAD) and the Canadian Dermatology Association (CDA) recommend a minimum Sun Protection Factor (SPF) of 30 [21]. SPF is a measure of UV-induced erythema, thus primarily denotes UVB protection, as UVB is 1000 times more erythemogenic than UVA [22]. According to Health Canada and the FDA, the term “broad spectrum” means UVA protection with a critical wavelength of at least 370 nm. UVA protection is primarily measured by Critical Wavelength [22]. The European Commission addressed the need to quantify UVA protection with the symbol , indicating that the UVA protection is at least one third of the stated SPF [23]. VL is not necessarily covered by sunscreen. Filters that cover VL are outlined in the “Physical/Inorganic Sunscreens,” “Filters not listed as Active,” and “Tinted Sunscreen” sections.
The quantity and frequency of sunscreen application are common concerns. SPF is determined with a standard amount of sunscreen (2 mg/cm2) under laboratory conditions, but people typically apply much less (0.8 mg/cm2 in one study) [24]. Early reapplication is also helpful, as two applications of 1 mg/cm2 produced the same SPF as a single larger application of 2 mg/cm2 [25].
Use of a sunscreen with a higher SPF partially compensates for the insufficient amount applied [24, 26]. A consumer in-use double-blind randomized split-face study compared the efficacy of sunscreen with SPF 50 versus SPF 85 to assess if there is additional benefit to extra-high SPF. They found that SPF 85 provided significantly more protection against sunburns [27]. Ou-Yang et al. performed a single center, evaluator blinded, randomized trial of 237 participants with Fitzpatrick skin types I–III comparing SPFs 30, 50, 70, and 100 at four different sunscreen densities (0.5, 1.0, 1.5, and 2.0 mg/cm2) in a controlled laboratory setting [28]. Results demonstrated that mean SPF value was progressively lower with decreasing application densities. However, reduced application densities resulted in proportionately higher mean SPF values for products with higher labeled SPFs. The follow-up study of n = 65 compared the same sunscreens at only 0.5 and 1 mg/cm2 to reflect consumer usage [28]. The mean actual SPF of the 0.5 mg/cm2 dose was approximately 25% of the labeled SPF for all products. Ou-Yang et al., therefore, suggested using an SPF of 70 and above, which yields at least an actual SPF of 19 when used in concentrations as low as 0.5 mg/cm2 [28].
The Food and Drug Administration (FDA) and Health Canada suggest sunscreen reapplication every 2 h based on a small observational study [29]. A larger study suggests that a single application remains beneficial for 6 h if there is no water exposure [30]. When active outdoors, sweating, or in contact with water, reapplication is required [26].
Chemical/organic sunscreens
Chemical (organic) sunscreens represent 75% of current products [31]. Multiple ingredients are often combined for broad-spectrum coverage [32]. Many are aromatic compounds conjugated with a carbonyl group, which absorb high-energy UVR. The different active ingredients are reviewed in Table 1. There are several chemical filters approved outside of the USA including Mexoryl XL, Tinosorb M and Tinosorb S [33, 34]. Mexoyrl SX has limited use in the USA [35].
Physical/inorganic sunscreens
The FDA and Health Canada have approved zinc oxide (ZnO) and titanium dioxide (TiO2) as physical (inorganic) compounds protecting against a broad range of UVR (Table 1) [36]. The creation of nanoparticles improved the esthetics of these formulations while maintaining UV protection [37]. The photostability of TiO2 and ZnO is increased by coating them with silica and dimethicone [38].
Filters not listed as Active
Iron oxide can be used to reduce VL exposure [2]. However, iron oxide is not listed as an active compound in the FDA and Health Canada monographs. Thus it is listed as an inactive ingredient in the sunscreens that contain it.
Tinted sunscreens
Tinted sunscreens contain iron oxides and less commonly pigmentary TiO2 [39]. Synthetic mica is often used to enhance radiance and create an optical blurring effect to reduce color mismatch [39].
Systemic photoprotection and oral agents
Evidence for the use of systemic agents is limited. A comprehensive 2020 review of systemic photoprotection discusses the evidence for vitamins C, E, and D, carotenoids (beta-carotene, lycopene, xanthopylls), nicotinomide, retinoids, and dietary botanicals including polyphenols, polypodium leucotomos extract (PLE), non-steroidal anti-inflammatory drugs (NSAIDs), and afamelanotide [19].
In animal models, PLE upregulates p53 gene expression for enhanced DNA repair, modulates inflammatory cytokines, and inhibits UVR-induced cyclooxygenase-2 expression [40,41,42,43]. PLE is reported to be well-tolerated, reduce UVR-induced erythema in human trials, and reduce UV damage at the cellular level [19, 44,45,46,47,48,49]. However, the protective effect was of short duration and studies to-date are limited [19]. There is no conclusive long-term data from large studies to suggest that oral agents provide sufficient photoprotection when used alone.
Sun protective clothing
The ultraviolet protection factor (UPF) indicates the amount of UVR penetration through different fabrics. UPF does not account for body surface area (BSA) covered [50]. UPF clothing is particularly important for those who are exposed to UVR through their occupation due to increased risk of keratinocyte carcinoma [50]. In 2018 BSA and UPF were both considered when Downs et al. created the garment protective factor (GPF). This has yet to be widely adopted [51].
Less than 30% of cotton fabrics have UPF values of 30 + [51, 52]. The denser the weave of the material and smaller the pore size, the better protection the fabric offers. Natural fabrics (cotton, silk, linen) and lighter colors offer less photoprotection than synthetic fabrics or wool. Darker colors absorb more UVR and looser clothing offers more photoprotection [53,54,55]. Optical whitening agents and UV-absorbing laundry additives can be used, if available [34]. Clothing specifically made for sun protection will have a labeled UPF.
The Skin Cancer Foundation defined adequate UPF as 30, very good protection as UPF 30–49, and excellent UPF as 50 + [56]. Only European testing standard requires UVA protection thresholds, which is important to inform patients with UVA action spectrum photodermatoses [50].
Wearing appropriate UPF clothing is an effective method of sun protection, although protection can be provided by clothing without a UPF label, determined by color and the factors listed above.
Sunglasses and hats
Sunglasses reduce ocular UVR and VL exposure, thus decreasing the risk of damage to periocular skin (malignancies, photoaging), the lens (cataracts), and cornea (keratitis) [57]. Hats provide important protection for the scalp. An older study using polymer film polysulfone to measure UVR exposure demonstrated wide-brimmed (> 7.5 cm brim) options provide optimal head and neck coverage [58]. Diffey and Cheesman determined that most hat styles provide sufficient forehead coverage, but a brim of at least 7.5 cm is necessary to provide reasonable protection of the nose and cheeks [58].
Adverse effects
Absorption of sunscreens
Superficial cutaneous absorption
The potential for adverse reactions to sunscreen is largely dependent on whether the ingredients penetrate the stratum corneum. In vitro models suggest chemical UV filters (octocrylene, benzophenone, avobenzone, octinoxate, and padimate O) may penetrate the stratum corneum [59,60,61,62,63]. It remains unclear if this exposure causes keratinocyte injury. Anaphylactic reactions to oxybenzone have rarely been reported [64, 65]. UV-induced dehydration of the stratum corneum may increase percutaneous absorption [66]. Certain formulations, such as concentrated sprays or chemical sunscreen compounds encapsulated into mesoporous silica or bio-adhesive nanoparticles optimize delivery and decrease penetration [67,68,69,70]. Alcohol-based formulations may penetrate the stratum corneum more easily than lipophilic formulations [71].
The use of nanoparticles in sunscreens with ZnO and TiO2 initially raised concern about skin penetration, but they do not penetrate the stratum corneum after application in vivo [20, 36, 60, 72,73,74,75,76,77,78,79,80,81,82]. Nanoparticles are undetectable past the stratum corneum on biopsy at 24 and 48 h post-application [83].
Systemic absorption
Studies using benzophenone-3, octylmethoxycinnamate, and 4-methylbenzylidene camphor applied 1–2 times a day showed accumulation in plasma and urinary excretion at 1–2 h after first application continuing until 4–5 days after the last application [84, 85].
After maximal use (4 times a day to 75% body surface area), increasing plasma concentrations above the FDA’s safe threshold of 0.5 ng/mL were found between days 1–4 after application [86]. While concentrations for avobenzone, octocrylene, homosalate, octisalate, and octinoxate ranged from 7–50 times the FDA threshold, benzophenone-3 was detected at levels 500 times the FDA approval level [87]. Chemical sunscreen ingredients have also been identified in semen and breast milk [88, 89]. Importantly, there is no evidence to suggest this confers any health risk. Sunscreens have been used for many years without a signal that they are causing harm [90, 91].
Concerns have been raised about sunscreen effects on the endocrine, reproductive, and developmental systems. Most studies use animal models, and the disturbances appear more likely related to biological variation than the application of sunscreen [92,93,94,95,96,97,98,99]. Furthermore, the use of sunscreen in these studies does not always reflect human practice. The report of abnormal uterine growth comes from a 2001 study where rats were fed high doses of chemical sunscreen [100]. Janjua et al. investigated the impact of benzophenone-3, octyl-methoxycinnamate, and 3-(4-methylbenzylidene) camphor on reproductive hormones in humans with whole-body topical application of 2 mg/cm2 [99]. The study demonstrated that follicle stimulating hormone, luteinizing hormone, and sex hormone binding globulin were unchanged, but a minor statistically significant decrease in testosterone was noted in males [99]. A detailed evaluation of humans’ long term use of sunscreen at 2 mg/cm2 volume is warranted to delineate health risks after decades of use.
For infants, the American Academy of Pediatrics suggests physical sunscreens with a minimum SPF of 30 until more safety data are available on chemical filters [101]. However, the data on absorption of sunscreen ingredients in the pediatric population are scarce. Future investigations are needed to evaluate the safety of chemical UV filters in this population.
Contact dermatitis
Allergic and irritant contact dermatitis (ACD and ICD) are the most common side effects associated with sunscreen use [102,103,104,105]. Inactive sunscreen ingredients may also be implicated (e.g., preservatives, fragrances, vehicles).
Photoallergic reactions are rare and have only been reported to a few chemical sunscreen ingredients (Fig. 1). When combined, the strong UV protective effects of physical sunscreens and chemical UVA absorbers may prevent photoallergic reactions to other chemical sunscreen ingredients [106, 107]. Patch and photopatch testing can help determine the culpable allergens [108]. If a contact or photocontact allergy to a particular compound is found on testing, a sunscreen without that compound can be used.
Vitamin D deficiency
It does not appear that regular use of sunscreen prevents vitamin D synthesis. This may be due to inadequate use of sunscreen [109, 110]. Nevertheless, the AAD recommends a daily oral intake of 1000 International Units of vitamin D for individuals who practice rigorous photoprotection [111].
Disease-specific sunscreen use (Table 2)
Hyperpigmentation: melasma, post-inflammatory hyperpigmentation and maturational dyschromia
Patients with hyperpigmentation require diligent daily application of broad-spectrum UVR and VL protection (i.e., Fe2O3) [18, 112, 113]. Tinted broad spectrum sunscreens with iron oxide may reduce the appearance of hyperpigmentation after only 2 months of daily application [18, 114,115,116]. Broad-spectrum UVA and UVB protection was shown to be more effective in preventing post-inflammatory hyperpigmentation (PIH) with the combination of terephthalylidene dicamphor sulfonic acid (TDSA, MexorylSX) and drometrizole trisiloxane (DT, MexorylXL) compared to TDSA alone [113, 117, 118]. Maturational dyschromia or hyperpigmentation is one reason for recommending broad-spectrum UVR and VL photoprotection for all skin types [119].
The data on possible benefit of PLE for patients with melasma are conflicting, and sample sizes are small [120]. A double-blind, placebo-controlled, randomized trial (n = 40) evaluated twice daily PLE 240 mg for 12 weeks in patients concomitantly treated with broad-spectrum sunscreen and hydroquinone 4% cream. The group with adjunct PLE treatment had a greater reduction in disease severity [120, 121]. However, another randomized, double-blind study (n = 33) showed no benefit of PLE [122].
Frontal fibrosing alopecia/lichen planopilaris
There is a controversial, poorly substantiated association between the facial use of sunscreen and frontal fibrosing alopecia (FFA) [123,124,125,126,127]. Only two case reports link long-term use of chemical sunscreen with the onset of LPP [128, 129]. Recent studies demonstrated an association between FFA and many other cosmetics (e.g., moisturizers) [125, 130]. With limited and conflicting data, sunscreen avoidance to prevent FFA is not recommended.
Photosensitivity disorders
Photosensitivity disorders can be divided into those caused by sun exposure (photodermatoses) and those that are aggravated by it (photoaggravated diseases). The UV wavelengths that typically trigger flares are the action spectrum for that condition.
Photodermatoses
Photodermatoses can be idiopathic or secondary. Idiopathic photodermatoses include polymorphous light eruption (PMLE), solar urticaria, actinic prurigo, hydroa vacciniforme, and chronic actinic dermatitis [11]. Secondary photodermatoses are triggered by sun exposure, as part of an underlying disease, such as lupus erythematosus and dermatomyositis [131]. Most photodermatoses include UVA in their action spectrum. Therefore, broad spectrum sunscreens are necessary. Solar urticaria and chronic actinic dermatitis include VL in the action spectrum and therefore may benefit from the addition of iron oxide. Depending on severity, protective car window filters and home window coverings can be considered [132].
In addition to broad spectrum sunscreen (± iron oxide), there are photodermatosis-specific therapies beyond the scope of this paper [14].
Drug-induced photosensitivity
Drug-induced photosensitive reactions may be phototoxic or photoallergic and are primarily related to UVA exposure with the culprit medication. Common photosensitizing medications include thiazide diuretics, sulfonamide antibiotics, sulfonylureas, phenothiazines, tetracyclines, NSAIDs, amiodarone [11]. The clinical presentation appears as an acute sunburn (phototoxicity) or as a dermatitis (photoallergy). In some cases the reactions persist long after the UV exposure [11]. Continued drug exposure may lead to extreme photosensitivity persisting for months or years after the drug is withdrawn [11]. Management includes drug identification and discontinuation, topical corticosteroids, and sun avoidance [11]. The latter involves using physical barriers and broad-spectrum high SPF sunscreens [11].
Systemic, subacute, and chronic cutaneous lupus erythematosus
Consistent photoprotection is critical for patients with systemic (SLE), subacute (SCLE), and chronic cutaneous (CCLE) lupus erythematosus (particularly discoid and tumid lupus) to minimize UV-induced flares [133].
Both UVA and UVB may induce flares [134,135,136,137,138,139]. UVA penetrates window glass so indoor exposure is often sufficient to trigger skin eruptions [140, 141]. Lesions may appear as late as 3 weeks after UV exposure [133].
In addition to broad spectrum high SPF sunscreens for adequate UVA coverage, there are case reports suggesting that adjuvant PLE may help reduce flares in patients with SCLE [142,143,144,145]. Systemic medication is often required to treat the photosensitive reactions in patients with lupus.
Photoaggravated skin diseases
Photoaggravated skin diseases are worsened by UV exposure. The list of skin conditions is broad including common diseases such as atopic dermatitis (10% photoaggravated), rosacea, and acne vulgaris (can have improvement or photoaggravation) [146]. Given the wide action spectrum, broad-spectrum high SPF sunscreens are recommended. The same suggestion can be made for DNA repair syndromes [14].
In cutaneous porphyrias the action spectrum is primarily VL (400–410 nm), therefore tinted sunscreens containing iron oxide offer the greatest benefit [14].
Keratinocyte carcinomas (non-melanoma skin cancers) and melanoma
The American Cancer Society and the CDA recommend regular use of broad-spectrum sunscreen with SPF30 + to prevent keratinocyte carcinomas [147, 148]. Increased cumulative lifetime sun exposure increases the risk for squamous cell carcinoma (SCC) and actinic keratoses (AKs) [149]. Repeated intermittent high dose UVR exposure is associated with basal cell carcinoma (BCC) and melanoma [19, 150, 151].
Solid organ transplant recipients are 65–250 times more likely to develop SCC [152] and 10 times more likely to develop BCC compared to the general population due to immune suppression [153].
Barriers to sunscreen use: cosmesis, cost, and environmental impact
Esthetic considerations are important. Patients with sensitive skin typically describe stinging, burning and itching sensations, but the pathophysiology remains unclear [154]. Physical sunscreens are recommended for sensitive skin and pigmentary dyschromia (VL coverage), but some have cosmetic disadvantages. Reduced absorption and the scattering of incident light can create a white cast over the skin [104]. Micronization and nanoparticles have greatly improved the cosmesis, but it may remain a concern for patients with darker skin types [155]. Dermatologists should familiarize themselves with acceptable sunscreen options for all skin types [156]. Tints cosmetically enhance physical sunscreen options. Aerosol sprays have some cosmetic advantages because they are light and nongreasy, but they can leave a film and the application process is less controlled [157].
The cost of sunscreen and accessibility should be considered. Knowing more affordable options can be helpful. People can blend the appropriate foundation with sunscreen to provide a tinted option so long as the recommended quantity of sunscreen is still used.
There is concern that UV filters may cause coral bleaching [158, 159]. However, the studies done to date examine coral samples in a laboratory setting with high concentrations of chemical sunscreen ingredients [158]. Ocean warming due to climate change is a major factor in the release of zooxanthelae from coral that leads to bleaching [160]. The possible environmental impact of chemical sunscreen on coral reefs has led to local bans of benzophenone-3 and octinoxate in Hawaii [161].
Conclusion
A personalized approach to sunscreen selection may help in improving patient adherence, short-term and long-term clinical outcomes. Physicians should be aware of sunscreen labeling claims, potential side effects, and sunscreen preferences based on the action spectrum of specific diseases.
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McDonald, K.A., Lytvyn, Y., Mufti, A. et al. Review on photoprotection: a clinician’s guide to the ingredients, characteristics, adverse effects, and disease-specific benefits of chemical and physical sunscreen compounds. Arch Dermatol Res 315, 735–749 (2023). https://doi.org/10.1007/s00403-022-02483-4
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DOI: https://doi.org/10.1007/s00403-022-02483-4