Photokeratitis induced by ultraviolet radiation in travelers: A major health problem

Abstract

Ultraviolet (UV) irradiation is one of the several environmental hazards that may cause inflammatory reactions in ocular tissues, especially the cornea. One of the important factors that affect how much ultraviolet radiation (UVR) humans are exposed to is travel. Hence, traveling is considered to include a more acute UVR effect, and ophthalmologists frequently evaluate and manage the ocular manifestations of UV irradiation, including UV-induced keratitis. The purpose of this paper is to provide an evidence-based analysis of the clinical effect of UVR in ocular tissues. An extensive review of English literature was performed to gather all available articles from the National Library of Medicine PubMed database of the National Institute of Health, the Ovid MEDLINE database, Scopus, and ScienceDirect that had studied the effect of UVR on the eye and its complications, between January 1970 and June 2014. The results show that UVR at 300 nm causes apoptosis in all three layers of the cornea and induces keratitis. Apoptosis in all layers of the cornea occurs 5 h after exposure. The effect of UVR intensity on the eye can be linked to numerous factors, including solar elevation, time of day, season, hemisphere, clouds and haze, atmospheric scattering, atmospheric ozone, latitude, altitude, longitudinal changes, climate, ground reflection, and geographic directions. The most important factor affecting UVR reaching the earth's surface is solar elevation. Currently, people do not have great concern over eye protection. The methods of protection against UVR include avoiding direct sunlight exposure, using UVR-blocking eyewear (sunglasses or contact lenses), and wearing hats. Hence, by identifying UVR intensity factors, eye protection factors, and public education, especially in travelers, methods for safe traveling can be identified.

Introduction

Everybody is exposed to ultraviolet radiation (UVR). The natural source of UVR is sunlight. Other artificial sources of UVR include sun-tanning beds, welding arcs, photographic flood lamps, lightning, electric sparks, and halogen desk lamps. UVR has been shown to affect human health.[1] Besides the skin, the eyes have a high potential for damage by UVR. Although the eyebrows, eyelashes, and pupillary constriction create a defense against extreme light and UVR, the eyes are still susceptible.

UVR is electromagnetic radiation in wavelengths ranging from 100 to 400 nm and is divided into three bands: ultraviolet A (UVA) (315–400 nm), ultraviolet B (UVB) (280–315 nm), and ultraviolet C (UVC) (100–280 nm). However, environmental photobiologists and dermatologists frequently define this division as UVA at 320–400 nm, UVB at 290–320 nm, and UVC at 200–290 nm. UVR is invisible to the human eye. Shorter wavelengths of UVR have more energy, and this higher energy raises the potential for ocular damage.[2,3] The biological damage potential at 300 nm is 600 times more than the biological damage potential at 325 nm.[4] The ozone layer absorbs shorter wavelengths efficiently. Sunlight passes through the ozone layer, and all UVC and approximately 95% of UVB radiations are absorbed. Therefore, the longer range of ultraviolet (UV) radiation that reaches the earth is 95% UVA and approximately 5% UVB.[5] Traveling is one of many factors that can increase exposure to UVR.

The purpose of this review is to evaluate the risk factors that increase ocular exposure of the eyes and also the protective methods against this exposure, according to evidence-based medical guidelines. The mechanisms of the effect of UVR on the eyes, complications to the cornea of UVR, the amount of UVR reaching the eyes, and the methods to protect against UVR during travel were reviewed.

Methods

All studies in English literature evaluating the effect of UVR on eyes, corneal complications of UVR, and the methods to protect against UVR during travel between January 1970 and June 2014 were analyzed. For this purpose, an electronic search was performed using the National Library of Medicine PubMed database of the National Institute of Health and the Ovid MEDLINE database, using the phrase “travel” in combination with one of the following terms: “ultraviolet-induced keratitis,” “cornea,” “eye,” “ultraviolet,” “sunlight,” “medicine,” and “sun protection factor.” We sought additional articles by performing the same search strategy in the databases of Scopus, ScienceDirect, and Google Scholar. We then combined all searches and removed the duplicate articles and excluded irrelevant articles by reading their title and abstract. Finally, 43 studies were used for this review article.

Results

Effect of ultraviolet radiation on eyes

UVR exposure in ocular tissues can cause photochemical reactions that result in acute and chronic damage to ocular structures.[3] Chronic effects include basal cell carcinoma and squamous cell carcinoma of the eyelid,[6,7,8] pterygium,[9] pinguecula,[10] ocular surface squamous neoplasia,[11] cataracts,[12,13] climatic droplet keratopathy,[14] age-related macular degeneration,[15] and uveal melanoma.[16,17] An acute ocular effect of UVR is photokeratitis.[14] Photokeratitis represents the acute corneal response to UVB and UVC radiation exposure. Traveling is considered to have a more acute effect. Therefore, photokeratitis has been discussed in detail.

Photokeratitis, also known as snow blindness or welder's arc, is a painful, superficial, punctate keratopathy caused by acute exposure to UVR. Symptoms include tearing, ocular redness and pain, photophobia, swollen eyelids, headache, halos around lights, blurred vision, and temporary loss of vision. This is a transient inflammatory condition that usually appears up to 6 h after exposure to UVR and resolves within 48 h, typically without long-term consequences.[14,18] Acosta et al. discussed reasons for the discomfort sensations experienced after exposure to UVR. Sensitization of the nociceptor and depression of cold thermoreceptor activity following UVR appear to result from an action of inflammatory agents, possibly mediated through changes in the activity of TRPA1 and TRPV1 channels in parallel with an inhibition of TRPM8 channels. Changes in nerve activity possibly cause discomfort sensations associated with corneal inflammation induced by UVR.[19] Some inflammatory agents expressed by UVR include nuclear factor kappa-light-chain-enhancer of activated B cells and prostaglandin E2.[20]

The effects of UVR on corneal epithelium are described in four categories: inhibition of mitosis, nuclear fragmentation, vacuole formation, and loosening of the epithelial layer. Inhibition of mitosis is observed with small doses of UVR and in the early phase of photokeratitis. Nuclear fragmentation occurs with higher doses of UVR and includes four stages: nuclear swelling, aggregation of chromatin reticulum, bursting of the nuclear membrane, and swelling of the cell body.[21]

Kronschläger et al. demonstrated apoptosis in rat cornea after exposure to UVR at 300 nm. Rat cornea was exposed to UVR-300 nm for 15 min, and then, for the detection of apoptosis, terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) staining was performed. Exposure to UVR-300 nm caused apoptosis in all layers of the cornea, which occurred 5 h after exposure. In addition, the effects of the TUNEL staining peaked at 24 h after UVR exposure.[22]

Photokeratitis causes corneal cell apoptosis through direct damage to the cell membrane, DNA damage, and reactive oxygen species induction, in addition to being a result of an inflammatory reaction.[23]

Photokeratitis occurs in situations where the environmental UVR dose is extremely high such as during skiing, mountain climbing, or during excessive time spent at the beach. Occupational exposure is also a significant artificial source of UVR causing photokeratitis. An example of occupational exposure is the “welder's flash” during arc welding.[24]

Distribution of ultraviolet exposure

Important factors affecting the extent to which humans are exposed to UVR include solar elevation, time of day, season, hemisphere, clouds and haze, atmospheric scattering, atmospheric ozone, latitude, altitude, longitudinal changes, climate, ground reflection, and geographic directions [Figure 1]. These factors are described below.

Figure 1.

Important factors affecting the extent to which humans are exposed to ultraviolet radiation

Solar elevation

Solar elevation has the most important effect on UVR reaching the earth's surface.[25,26] Solar elevation changes with the time of day, season, and geographical location (latitude and altitude). As solar elevation decreases in the sky, the intensity of UVR reaching the earth's surface decreases at all wavelengths, especially those shorter than 320 nm, because there is more air and ozone atmosphere for UVR to pass through. One study demonstrated that extreme ocular UV exposure is different at higher solar elevation.[27] The maximum ocular UVR is in the morning and afternoon when solar elevation is low.[28,29]

Time of day

Solar UVR is frequently the strongest at local noon times from 11:00 A.M. to 13:00 P.M.[27,30] Although UVR peaks around noon, UVR reaching the eyes depends mainly on solar elevation. Ocular damage due to UVR can occur in the early morning and afternoon because of solar elevation in relation to the eyes at those times. As the sun rises in the sky, direct ocular exposure to UVR increases until the sun crosses the brow ridge, and the upper lid begins a shadow over the cornea. Sasaki et al. showed cornea damage by UVR was higher between 8:00 and 10:00 A.M. and between 14:00 and 16:00 P.M than at noon. At these times, the potential ocular damage is generally considered to be reduced compared with the peak of the day.[29]

Season

Regardless of the time of day, seasons have the most profound effect on ambient UVR. The highest dose of UVR reaching earth occurs during summer followed by spring, autumn, and winter. This occurs because of decreasing solar elevation.[31,32,33] There are variations in distance between the earth and the sun due to the elliptical orbit. Therefore, how much UVR reaches the earth varies by about ±3.5% throughout the year and it is at a maximum in summer and at a minimum in winter. In the mid-latitudes of the Northern hemisphere, maximum and minimum total UVR was determined in the spring and late autumn, respectively.[34] In different seasons, the time of peak UVR exposure changes more than does the total daytime exposure. The highest ocular exposure in autumn occurs during midmorning and midafternoon, while in the winter, it occurs at noon. This difference is due to changes in the solar angles in various seasons.[29]

Hemisphere

One factor that affects the amount of UVB reaching the earth is the distance from the earth to the sun, particularly during the summer. The Northern hemisphere is 1.7% further away from the sun in the summer than is the Southern hemisphere. During this time, the intensity of UVB decreases approximately 7% in the Northern hemisphere.[35] On the other hand, due to the clear atmospheric conditions and ozone depletion observed over the Antarctic, total UVR is 12%–15% greater in the Southern than in the Northern hemisphere.[36]

Clouds

Clouds significantly impact UVR and have dual effects on UVR reaching the earth's surface. Some studies have shown that cloud cover usually can reduce UVR by about 10%–38%.[36,37,38,39] The mean reduction of UVR by clouds is usually 15%–30%.[26] Cloud attenuation effect depends on different cloud properties such as cloud amount, cloud optical thickness, relative position between the sun and clouds, cloud type, and the number of cloud layers. On the other hand, cloud enhancement effect on UVR has been revealed in various studies.[40,41,42,43,44] Overall, the cloud effect on UVR is usually that of a reducing effect.[45]

Atmospheric scattering

Atmospheric scattering is caused by particulate matter or air pollution suspended within the atmosphere. These materials can prevent UVR from reaching the earth's surface due to scattering and absorption of UVR. The effect of scattering depends strongly on wavelength of UV, especially shorter wavelengths because they have greater intensity than longer wavelengths (proportionate to inverse fourth power of wavelength, Rayleigh's law). Therefore, UVB is scattered to a significantly higher extent than UVA. The amount of extinction of UVR varies. In different studies, this reduction has been reported as having a great range, between 5% and 50%, but it is usually below 20%.[41,46,47]

Atmospheric ozone

The most important factor for the quality and quantity of solar UVR reaching the earth's surface is atmospheric ozone layer. UVC and most UVB radiation are absorbed in the ozone layer. UVB intensity at the earth's surface depends strongly on the amount of atmospheric ozone. Stratospheric ozone column varies at different locations or on different days.[36] In recent decades, an increase in ozone column depletion has occurred and it ranges from 0.5% ±1.3% per decade around the equator to 8.9% ±2.0% per decade in the Antarctic.[45] A decrease of 1% in the total column of ozone can lead to about 2% increase in UVB radiation.[48] Compared with Central Europe and parts of North America, Australia has greater levels of solar UVR because of its lower levels of stratospheric ozone.[35] In the summer, solar UVR is higher in New Zealand compared with Germany due to the reduction of stratospheric ozone in New Zealand and increase of tropospheric ozone in Germany.[24]

Latitude

The most common method for calculating the weighing of biological effects of UVR is the Commission Internationale de 1’Eclairage erythema action spectrum,[49] which was used for estimating UVR intensity. At mid-latitudes (28–46”) around the world, the increase in erythemal effective UVR for every degree of latitude toward the equator is between 3% increase in UVR/°N decrease in the Northern hemisphere and 3.6% in UVR/°S decrease in the Southern hemisphere.[33,35,50] At higher latitudes (60–68”), i.e., in Finland in Northern Europe, the change is even higher with about 4.2% increase in UVR/°N decrease.[51]

Altitude

UVR increases with altitude because of the shorter optical path that the solar radiation has to cross to reach the surface. Therefore, the amount of absorbers in the overlaying atmosphere decreases with altitude. The altitude effect depends on the wavelength, cloudiness levels, solar elevation, atmospheric turbidity, and the ground reflection of the terrain. The altitude effect shows an obvious stronger increase at shorter wavelengths than that of global irradiance. Irradiance increases 9% per 1000 m at 370 nm, 11% per 1000 m at 320 nm, and then more rapidly to 24% per 1000 m at 300 nm.[52] Various studies conducted in the United States have reported an increase in UVR per 300 m of ascent in elevation, which was calculated between 2.1%–3.8%.[33,53,54]

Therefore, not only higher ambient UVR is caused by higher altitude but also higher levels of shorter wavelengths. El Chehab et al. showed that ocular phototoxicity in mountaineer guides was significantly higher compared with people living in plain areas because guides are exposed to a higher amount of UVR in relation to altitude and ground reflection of snow.[55]

Ground reflection

Part of the solar UVR reaching the earth's surface is absorbed by the ground and part of it is reflected back to space. For geometric and anatomic reasons, ground reflection plays a larger role in UVR ocular exposure than in skin exposure.[56] The amount of reflected radiation depends on the properties of the surface and wavelength. This amount is usually <10%.[57] The main exceptions include fresh pure snow reflecting 60%–94%, ice 7%–75%, green grass 24%, and black asphalt 4%–11%.[51,58,59,60,61] Fresh snow reflection is highly dependent on the type and age of snow.[62] Yu et al. revealed that surface reflection of bare land without snow cover in the winter is about 23% while the fresh snow reflection is about 85%.[63] Sand can reflect up to 25% of UVR and this is important in increasing UV exposure at the beach.[59]

Geographic directions

Geographical directions are an important factor in ocular exposure to UVR. Since the sun rises from the East and sets in the West, ocular exposure to UVR has one peak during the morning and one in the afternoon near the east and west geographical directions, respectively.[64]

Prevention

It is unfortunate that people currently have little concern about eye protection.[65] There are several methods of photoprotection that can reduce the risk of UVR in potentially causing damage to the eyes, including avoidance of direct sunlight exposure, the use of UVR-blocking eyewear (sunglasses or contact lenses), wearing hats, and using an umbrella. The most effective way is to avoid sunlight. Even in cloudy weather conditions, people should be recommended to avoid sun exposure.[66,67]

Another common way to protect against UVR is to wear sunglasses that provide adequate protection against UVR. Sunglasses should ideally block all UVR and some blue light as well and have minimal effects on contrast acuity and color discrimination.[68,69] In 1972, the first article that outlined the American National Standards Institute (ANSI Z80.3) standards for sunglasses was published.[70] Color discrimination and contrast acuity are less affected by gray-tinted lenses than by any other colored lenses.[68,69] Other important factors in photoprotection are the size, style, and position of the sunglasses. The eyes can be damaged by UVR from scattered and reflected light from the periphery of eyes. Therefore, small sunglasses increase the probability of UVR reaching the eyes from the side of the sunglasses.[71] It is particularly important under special conditions that UVR bounces off the ground, snow, water, and sand indirectly. In addition, moving sunglasses about 6 mm away from the forehead leads to >20% increase in the amount of UVR reaching the eyes.[72] Therefore, decreasing the exposure of eyes to UVR can be achieved using tight-fitting wrap-around designs, side shields, and closing up sunglasses around the eyes.[73] More expensive brand-name sunglasses do not guarantee optimal protection against UVR.[74] To prevent UV damage to the eyes, people should wear sunglasses for outdoor activities such as driving, participating in sports, or taking a walk.

Shade, sunglasses, and prescription glasses provide some defense against direct solar exposure of the eyes. However, they may not protect the eyes from diffuse, ambient, scattered, and surface-reflected UVR and may cause a decrease in normal defense reactions such as squinting and pupillary constriction in the absence of direct solar light.[75,76] The newest method of eye protection against UVR is UVR-blocking contact lenses that can block peripheral light that sunglasses cannot block.[77] The ideal ocular photoprotection is to completely block UVR to the front of the cornea and to adjacent limbal and conjunctival stem cells from all sources of ambient solar UVR. The only form of ocular protection that could achieve this purpose is UVR-blocking contact lenses.[78] According to the ANSI Z80.20 standards, two different classifications of UVR-blocking contact lenses exist. Class one lenses block 90% of UVA and 99% of UVB radiation and are recommended for high exposure environments such as mountains or beaches. Class two lenses block 70% of UVA and 95% of UVB rays and are recommended for general environments. Contact lenses should be used in conjunction with more conventional methods for protecting the eyelids and nonvisual ocular media. The main risk in wearing contact lenses is developing keratitis, and the major single risk factor for microbial keratitis is contact lens wear.[79] Prevention efforts to decrease complications related to wearing contact lenses should focus on improving hygiene behaviors such as keeping all water away from the contact lenses, discarding used disinfecting solution from the case, cleaning with fresh solution each day, and replacing the contact lens case every 3 months.[80]

Management of photokeratitis

When photokeratitis occurs, avoidance of further exposure to UVR is mandatory. Photokeratitis is a self-limiting disorder, so relief from its symptoms occurs within 24–72 h spontaneously.[81] Cool compress, preservative-free lubricants, topical anti-inflammatory drugs, and cycloplegics can improve symptoms.[82] Topical anesthetic drops should not be used because they slow corneal healing. Furthermore, in severe cases of irrational use of topical anesthetic drops, melting of the cornea can occur.[83]

The differential diagnoses of photokeratitis include conjunctivitis, episcleritis, acute angle-closure glaucoma, acute anterior uveitis, and superficial keratitis. Some evidence may point to specific diseases. Discharge may present in conjunctivitis and be an infectious cause of superficial keratitis. Focal conjunctival hyperemia occurs in episcleritis. Severe ocular pain, severe reduced vision, and mid-dilated pupils that are not reactive to light are seen in angle-closure glaucoma. Constrictive pupils with poor reactivity to light occur in acute anterior uveitis.[84]

The clinical features of most cases of superficial keratitis include diffuse conjunctival hyperemia, moderate-to-severe ocular pain, moderately reduced vision, and hazy cornea. The causes of superficial keratitis are dry eyes, topical ocular medications, exposure to UVR, using contact lenses, blepharitis, and eyelid abnormalities. The accurate diagnosis and appropriate management of these diseases requires a slit-lamp examination, and consultation with an ophthalmologist is recommended.[84]

Conclusion

The role of UVR in ocular diseases is an important public health issue. Ocular exposure to UVR can be associated with acute and chronic complications. Acute effects of UVR can occur during travel. Photokeratitis is a painful, superficial, punctate keratopathy caused by acute exposure to UVR. This disorder usually appears up to 6 h after UVR exposure. Numerous factors affecting the reach of UVR intensity to humans include solar elevation, time of day, season, hemisphere, clouds and haze, atmospheric scattering, atmospheric ozone, latitude, altitude, longitudinal changes, climate, ground reflection, and geographic directions. There are various ways of photoprotection which reduce UVR exposure to the eyes, including avoiding direct sunlight exposure, using sunglasses or UVR-blocking contact lenses, and wearing hats. The most important action in the prevention of potential UVR damage to the eyes is more education of the general public about factors affecting UVR exposure and ways to prevent exposure.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.