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Effects of climate changes on skin diseases Expert Review of Anti-infective Therapy Downloaded from informahealthcare.com by Washington University Library on 01/01/15 For personal use only.

Expert Rev. Anti Infect. Ther. 12(2), 171–181 (2014)

Nicola Balato, Matteo Megna*, Fabio Ayala, Anna Balato, Maddalena Napolitano and Cataldo Patruno Department of Dermatology, University of Naples Federico II, Via Pansini, 5, 80131 Napoli, Italy *Author for correspondence: Tel.: +39 081 746 2457 Fax: +39 081 746 2442 [email protected]

Global climate is changing at an extraordinary rate. Climate change (CC) can be caused by several factors including variations in solar radiation, oceanic processes, and also human activities. The degree of this change and its impact on ecological, social, and economical systems have become important matters of debate worldwide, representing CC as one of the greatest challenges of the modern age. Moreover, studies based on observations and predictive models show how CC could affect human health. On the other hand, only a few studies focus on how this change may affect human skin. However, the skin is the most exposed organ to environment; therefore, it is not surprising that cutaneous diseases are inclined to have a high sensitivity to climate. The current review focuses on the effects of CC on skin diseases showing the numerous factors that are contributing to modify the incidence, clinical pattern and natural course of some dermatoses. KEYWORDS: allergy . climate change . extreme whether events . skin cancers . skin diseases . skin infections .

vector-borne diseases

.

water-borne diseases

Climate change (CC) is defined by significant and lasting variations in regional or global climates over relatively long periods. It includes major changes in average and peak temperature, humidity, atmospheric pressure, precipitations, wind patterns and ocean pH and salinity, as well as polar glaciers [1,2]. In recent years, CC has been considered as the cause of global warming (average surface temperature has augmented by 0.6˚C over the past 100 years [1] and it will probably increase by 2˚C by the end of 2100) [3,4], decreased precipitation, atmospheric humidity changes and global rise in extreme climatic events [5–7]. Indeed, climatic factors are able to influence the frequency and intensity of extreme weather events [1,2]. For example, sea levels are tending to rise, thus leading to more floods [8]. Moreover, changing climate also explains shifts in the distribution and behavior of several insect species, and consequently, of the related diseases [9]. CC can be conditioned by several natural factors such as variations in solar radiation received by earth, oceanic processes, plate tectonics and volcanic eruptions. Furthermore, human activities including use of fossil fuel and consequent accumulation of greenhouse gases (carbon dioxide, chlorofluorocarbons, methane and nitrous oxide) in the atmosphere, land www.expert-reviews.com

10.1586/14787210.2014.875855

consumption, deforestation and industrial processes as well as some agriculture practices deeply contribute to global CC [1–3]. Magnitude, causes and impact of CCs on human life have become important matters of debate worldwide, making CC one of the greatest challenges of the modern age. Although many articles have been written based on observations and various predictive models of how CC could affect social, economic and health systems, only few studies focus on how this change may affect human skin [2,10–15]. However, it is known that the skin is the major border organ of the human body, being the most exposed to environmental variations; therefore, it is not surprising that many skin diseases are inclined to have a high sensitivity to climate. Climatic factors can influence several skin features facilitating or worsening the incidence as well as the symptoms of many skin diseases, especially for chronic ones such as psoriasis and atopic dermatitis, which are very inclined to be conditioned by environmental conditions [11]. In another example, global warming, deforestation and changes in precipitation have been linked to variations in the geographical distribution of vectors of some infectious diseases of skin (i.e., leishmaniasis, borreliosis) by changing their spread, whereas warm and humid

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Balato, Megna, Ayala, Balato, Napolitano & Patruno

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Table 1. Main examples of the influences of climate change on skin diseases. Climatic factors

Influences on skin diseases

Global warming and changes in precipitation

Variations in the spread of some skin infectious diseases (i.e., leishmaniasis, borreliosis, etc.)

Global warming, variations in humidity

Increase of bacterial and fungal skin infections

Global climate change (especially in humidity and temperature)

Influences on the natural course of chronic skin diseases (i.e., psoriasis and atopic dermatitis)

El Nin˜o phenomenon

Increase of incidence of leishmaniasis, dengue, rickettsiosis

Rainfall, flooding, increased temperature

Water-borne diseases (i.e., cyanobacteria, bloom-related diseases, etc.)

Variations in frequency and intensity of extreme weather events

Skin and soft-tissue infections, scabies, papular urticaria, leishmaniasis

Changes in ozone layer, relative humidity, temperature and cloud cover

Increase of skin cancers

environment can also encourage the colonization of the skin by bacteria and fungi [11]. The present review focuses on the wide and complex relationship between CC and skin diseases showing the numerous factors that might contribute to modify the incidence and the clinical pattern of many dermatoses (TABLE 1). Skin & climate

Before analyzing the relevant influences of climatic factors on skin diseases, a concise as well as informative overview on the relationships between skin characteristics and climate is strictly necessary. Indeed, changes in climate and several environmental factors can affect several intrinsic skin characteristics facilitating and/or conditioning the outbreak of pathologic processes. For example, low environmental humidity is able to increase skin permeability [16], to thicken the epidermis and to stimulate the production of inflammatory mediators [17,18]. These changes can be observed in patients with chronic inflammatory dermatoses such as psoriasis, atopic dermatitis and senile xerosis, in which pruritus is more severe in cold dry climates. Moreover, experimental studies conducted by Hosoi et al. showed that the intensity of the induction and elicitation phases of contact sensitization is greater in individuals housed under low relative humidity, and is associated with increase of the number of Langerhans cells in the epidermis as well as of the migration of the antigen to the regional lymph nodes [19]. Similarly, low temperatures and low relative humidity have been shown to lead to an increase in irritant reactions in humans, as well as in weakly positive reactions to various substances used for patch testing with the German Standard Series [20]. Sebum secretion tends to be greater in the warmer months and in younger patients [21]. Several studies have shown that between 30 and 50% of young people suffering from acne complained an aggravation of their cutaneous disease during summer principally due to increased sweating [22,23]. However, there are also studies which reported that about one-third of patients with acne relate an improvement during summertime, therefore, it is very difficult to make predictions in this setting [22]. Climate 172

can also affect the amount of cutaneous water which depends on the gradient between the water content of epidermis and environmental relative humidity as well as on transepidermal water loss which is itself influenced by environmental relative humidity [24]. Egawa et al. verified that exposure to a low relative humidity of 10% for 6 h led to a reduction in water levels in the stratum corneum, in transepidermal water loss and in skin temperature [25]. Low environmental humidity (especially when this occurs abruptly), in combination with low temperatures, increases transepidermal water loss and decreases lipid and natural hydrating factor levels, leading to dry skin, worsening pruritus and other symptoms of skin diseases such as atopic dermatitis and psoriasis [26]. However, despite the indisputable importance of the relative humidity regarding the degree of skin hydration, other factors may also be involved. Indeed, many products such as detergents (especially those containing sodium lauryl sulfate) and drugs (retinoids, hypolipidemic agents, clofazimine, cimetidine or lithium carbonate) may lead to dry skin hastening the capacity to change skin pH, as well decreasing sebum secretion and altering lipid composition, respectively [26]. Moreover, skin hydration and sensations of dryness is also influenced by age. People over 60 years of age tend to be more affected by relative humidity (skin and eye dryness can be sensed at 30% relative humidity and at 10% relative humidity there is also dryness of the nasal mucous membrane with impairment of ciliary function), but subjectively they need more time to perceive it and take any measures necessary [27]. Vector-borne diseases & skin infections

There are many evidences describing the indisputable effects exerted by CC on vector-borne diseases as well as skin infections [9,28–54]. For the former, the interrelationship between climatic and social factors with certain arthropods-related diseases is very intricate, involving many possible confounding factors such as improved diagnostic methods of diseases, vector resistance to antibiotics and insecticides, environmental humidity and demographic shifts [28,29]. The literature continues to be Expert Rev. Anti Infect. Ther. 12(2), (2014)

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enriched by surveys that show evidences of the importance of CC with regard to this topic. Indeed, it has been reported that CC could have significant impacts on the distribution and seasonality of some vector-borne diseases (i.e., leishmaniasis, tickborne diseases, malaria, dengue fever, etc.) [28,30–32]. Particularly, global warming, variations in the frequency and intensity of precipitations as well as human activities by means of land use, deforestation and the employment of certain pesticides seem to have contributed to deeply change the geographical distribution of some vectors. Above all, temperature is considered a critical factor for the ability of a vector-borne disease to become epidemic, since vector density and its ability to transmit the pathogen depend on temperature, which also affects vector survival and the population growth rate, influencing the vector’s susceptibility to the pathogens, the incubation period of the pathogen inside the vector and its transmission pattern [33]. Temperature rise has also increased the length of the breeding season of many mosquitoes and their ability to colonize higher latitudes. For example, in Sweden, along with the construction of rural housing (thus increasing contact between humans, vectors and disease reservoirs), the greater average temperatures constitute a valid explanation for the observed increase in cases of Lyme disease [34]. Other examples of the expansion of vectors’ geographical ranges into more northern latitudes include the spread northward in eastern Canada of the ixodid tick which transmits Lyme disease and the extension of schistosomiasis water survival zone north in eastern China [35]. However, global warming does not represent the only factor regulating the diffusion of vector-borne diseases. Indeed, more precipitation can lead to greater plant density, creating local wet microclimates that favor the spread of insects, increasing also the food supply available to disease reservoirs, such as rodents and other herbivores [33]. On the other hand, droughts in wet areas also leave pools that amplify the size of the breeding areas and the feeding requirements of fertile females, thus raising the number of bites. Nevertheless, arthropods life cycles are modified by many other factors such as land use, water availability, demographic shifts and changes in intermediate hosts or natural reservoirs; thus, it is to be expected that these changes will be modulated by such local factors [36]. Moreover, the increased production of CO2 caused by human activities should not be ignored. Its accumulation is able to favor, by stimulating plant growth, the spread of insects, whereas urban growth facilitates epidemics, especially in unhygienic conditions [32]. Deforestation and the use of certain pesticides have also to be taken into account but usually present more variable effects. There are many studies which underline the impact of CC on vector-borne diseases, strengthening its key role. Tong et al. [37] reported significant correlations of incidence of Ross River virus infection to rainfall, maximum temperature and relative humidity in the Australian region of Townsville. In 2003, Subak [38] analyzed the effect of inter-annual climate variability on Lyme disease transmission in seven northeastern states of the USA, where Lyme disease cases had increased dramatically over the past decade. He reported a significant positive correlation of early summer www.expert-reviews.com

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disease incidence with the June moisture index in the region 2 years previously, reflecting the enhanced nymph tick survival in wetter conditions. Hence, the study gave this as a possible explanation regarding the increased incidence of Lyme disease. In addition, the spatial-temporal variability of human West Nile cases and the transmission of West Nile virus (WNV) to sentinel chickens were reported to be associated with the spatial-temporal variability of drought and wetting in southern Florida by Shaman et al. [39]. The authors indicated that widespread drought in the spring followed by wetting during summer can greatly increase the probability of a WNV epidemic by bringing avian hosts and vector mosquitoes into close contact and facilitating the epizootic cycling and amplification of arboviruses within these populations. Some major climatic events such as El Nin˜o, a climatic phenomenon associated with more frequent storms, floods, rain, drought as well as warmer temperatures, also seems to have clearly contributed to higher incidences of vector-borne infectious diseases [36–45]. El Nin˜o phenomenon was reported to lead to a 30% increase in the number of cases of malaria in Venezuela and Colombia by Kovats et al. [43], as a result of production of a generalized increase in the sea surface temperature over the eastern and central parts of the Equatorial Pacific. The authors also related that El Nin˜o is able to affect the incidence of Murray Valley encephalitis, Rift Valley fever and visceral leishmaniasis in different geographical zones. Other health effects of El Nin˜o phenomenon were registered by Tipayamongkholgul et al. [44], who reported a dengue-related outbreak in Thailand, whereas Cardenas et al. [45] described that El Nin˜o climatic fluctuations during 1985–2002 were responsible to enhance the incidence of leishmaniasis in Colombia. However, important implications of changing climate and global warming also lies in their effect on pathogen outbreaks apart from ones related to vector-borne diseases. As a result of global warming, temperatures at many highland localities are shifting toward the growth optimum of pathogens encouraging their outbreak [55], giving a possible explanation of the enhanced incidence of skin infections. Indeed, it is well known that Staphylococcus spp., Streptococcus spp. and enteric bacteria tend to colonize humans more readily in warmer climates [46,47]. Pyoderma is more prevalent in warmer areas, especially when there is high relative humidity [48–50]. Thus, it was reported that in the black population in the southern USA, the incidence of bacterial skin infection in the warm, humid months is reported to be as high as 50% in children aged from 2 years to 6 years, but it decreases to 4% in winter [51]. Given that most of these infections are caused by normal skin flora, Grampositive bacteria predominate, including Staphylococcus aureus and Streptococcus pyogenes, which are the pathogens responsible for most of these infections [52]. Conversely, it is known that a warm, humid environment may also encourage the colonization of the skin by Gram-negative bacteria as reported by McBride et al. [53]. The authors studied the changes in incidence of Gram-negative carriage from three skin sites in a climate-controlled chamber at 35˚C and 90% humidity for 173

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Balato, Megna, Ayala, Balato, Napolitano & Patruno

64 h. They showed that high temperatures and humidity increased the overall frequency of isolation of Gram-negative bacteria, although with individual differences. Another example of encouraged skin infection induced by changing climate comes from cryptococcal diseases. Indeed, CC has been linked to variations of incidence of cryptococcal infection, which was thought to be an exclusively tropical disease. Before 1999, human cases were limited to Australia and other tropical and subtropical regions. However, during January 2004–July 2010, a total of 60 people with Cryptococcus gattii infection had been reported to the US Center for Disease Control (CDC) in the Pacific Northwest of the USA, prompting them to issue an alert for patients showing signs of a cryptococcal infection [54]. This emergence fits with the redistribution of infectious diseases predicted by climate models. However, the CDC report emphasized that other factors apart from CC could have contribute to the disease’s spread such as the hypothesis that environmental conditions favorable to the fungus are broader than previously thought. However, all the data and observations outlined above support the fact that the incidence and distribution pattern of vector-borne diseases and skin infections in general, are being deeply influenced by changing climate. Water-borne diseases

Water-borne diseases can occur via contaminated water (e.g., fecal contamination), seafood (due to natural microbial hazards, toxins or wastewater disposal) or fresh produce (irrigated or processed with contaminated water). Weather is able to influence the transport and dissemination of these microbial agents via rainfall and runoff and the survival and/or growth through such factors as temperature. Therefore, climate variability may affect the risk of contamination events having a great impact on water-borne diseases [56,57]. Many different viral, bacterial and parasitic diseases have been associated with water-borne transmission [57]. Some diseases have been spread through drinking water whereas others by recreational water contact. Although intestine infections presenting with diarrhea and abdominal pain are the most common consequences of waterborne microbial pathogens, they can also affect human skin. This is the case of Dracunculus medinensis which can cause painful ulcers on lower limbs and feet, Francisella tularensis which is linked to suppurative skin lesions, Cyanobacteria which have been connected with dermatitis and Mycobacteria spp. which determine wound infections and several different clinical form of skin diseases. There are numerous evidences that heavy rainfall events, flooding and increased temperature represent the most important factors regarding the impact of climate on the epidemiology of water-borne diseases. Many investigations noted that heavy rainfall may precede the outbreak of waterborne diseases [58–61]. Heavy rainfall may also lead to changes in the direction of flow of water systems involving channels that would not normally occur. For surface water sources, they can lead to overflow of storm drains that may be combined with the sewage system allowing substantial amounts of fecally 174

polluted water into rivers [62]. Heavy rainfall has been linked with high counts of indicator bacteria and potential pathogens in river [63] and marine waters [64]; moreover, they may be followed by floods with subsequent health risk which tends to focus on infectious diseases. Generally, these outbreaks have been associated with flows of contaminated water into the groundwater or the interference with the effectiveness of water treatment [65]. For developing nations, there is evidence of outbreaks following floods (outbreaks of leptospirosis in Rio de Janeiro [66] and in the Philippines [67]). By contrast, epidemics do not tend to follow floods in developed countries [68,69]. It would seem to be the case that when infrastructure is adequate, epidemics of infection do not follow flood events unless the flooding has directly compromised the security of the water supply [68]. However, increased average temperature plays an important role in the outbreak of water-borne diseases. Global warming has been linked to the blooms of various planktonic species that are directly or indirectly hazardous to human health. Several planktonic species have been implicated in causing diseases in humans such as Cyanobacteria (blue-green algae), which have been involved in various clinical syndromes such as dermatitis, respiratory problems and hepatitis [70] by consumption of water containing toxins or contact with water or blooms during bathing. Most blooms occur during the summer months because relatively high water temperatures are necessary for algal growth and bloom formation [71,72]. There is a strong impression that algal blooms are becoming more common in Europe [73,74]. Should this trend continue, water-borne diseases will became more frequent not only in developing nations but also in developed countries, representing a new challenge for general medicine as they can affect various systems such as intestinal, urinary and respiratory one apart from the skin. Cutaneous diseases & natural disasters

Global warming and CC may alter the frequency, timing, intensity and duration of extreme weather events such as hurricanes, floods, severe storms and drought. Published literature indicates that the commonest skin diseases after flood-related disaster are skin infections and infestations [75], mainly caused by bacteria (Gram-negative bacteria above all) [76], frequently reported to be antibiotic-resistant [77]. However, these infections may be caused by various pathogens ranging from common bacteria and fungi [76] to more uncommon, such as Burkholderia pseudomallei [78] and Mycobacterium abscessus [79]. In 2005, wound infections with methicillin-resistant S. aureus, Vibrio parahaemolyticus and Vibrio vulnificus were reported in evacuees of hurricane Katrina, whereas tinea corporis, folliculitis, miliaria and arthropod bites were commonly registered among rescue workers. The prolonged flooding and exposure to contaminated water following the occurrence of hurricane Katrina was considered responsible to this outbreak of skin infections [80]. In addition, cases of V. vulnificus infection were reported by Rhoads in 2006 in New Orleans area [81]. They had been linked to the extensive flooding of below-sea-level, and toxic waters contamination of many areas of the town. Further Expert Rev. Anti Infect. Ther. 12(2), (2014)

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Effects of climate changes on skin diseases

evidence regarding the link between extreme whether events and skin infections are reported by survey concerning cutaneous diseases developed after the massive tsunami that hit Indian Ocean nations in December 2004. Hiransuthikul et al. [76] reported that 515 (66.3%) tsunami survivors with traumatic wounds were diagnosed to have skin and soft-tissue infections, with the most common organisms isolated being Aeromonas spp. Multidrug-resistant bacteria, polymicrobial infections and infections with uncommon pathogens, such as Cladophialophora bantiana, B. pseudomallei and M. abscessus, were also reported as the result of exposure to contaminated freshwater due to flooding [82–84]. Apart from skin infections, other common cutaneous implications associated with flood-related and other kind of natural disasters are reported to be scabies [85], papular urticaria [86], eczema [87] as well as leishmaniasis [88]. In 2010 during the floods in Pakistan, 40 health facilities in 4 flood-affected districts of Baluchistan, the greatest region of Pakistan, shared daily reports showing that between 29 July and 12 August, 2377 patients (16.5% of the total 14,404 patients visited) were reported with scabies and 3380 (23.5%) with malaria [85]. Moreover, Noe et al. [86] reported that 58/136 (42.6%) workers repairing buildings damaged by hurricane Katrina and hurricane Rita were affected by a skin rash. The most common cause of this rash was papular urticaria (65.9%) maybe because huts previously flooded as a result of the hurricanes and used for sleeping have harbored mites, a likely source of papular urticaria. Additionally in 2008, a survey to evaluate the most common skin diseases during floods in Thailand was conducted by Vachiramon et al. [87]. Eczema was the most prevalent dermatosis, which accounted for 34.5% of the total skin problems, the great majority being diagnosed as irritant contact dermatitis. Allergic diseases

The prevalence of allergic diseases has increased dramatically in the last decades [89]. Together with genetic predisposition, climatic and environmental factors may also play a significant role in their enhanced frequency [90]. It is indubitable that allergen exposure has changed during the past decades both quantitatively and qualitatively. For example, better insulated houses have increased growth of house dust mites whereas there is an augmented tendency to having pets even in small apartments. These factors should be taken into account considering the influences of environment on allergy. Moreover, environment play a major role in allergy not only for the presence of actingallergens but also for the existence of adjuvant factors such as environmental pollutants (e.g., substances from tobacco smoke can exert allergy-enhancing effects both for allergic respiratory diseases and skin diseases like atopic eczema) [91]. As regards, the effects of CC on allergic diseases, increased temperature and concomitant CO2 concentration are affecting plant growth leading to more, new and altered pollens. Indeed, in the last decades a prolonged vegetation period of pollinating plants has been observed in the northern hemisphere with a consequent increased exposure to outdoors allergens from pollens [92]. At www.expert-reviews.com

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the same time, several studies from different regions of the world have shown that higher temperatures are related to higher pollen counts [93,94], stronger allergenicity [95] as well as an earlier start and longer duration of the pollen season [96]. On the other hand, global warming also led to alterations of flora and fauna. For instance, in Germany Ambrosia artemisiifolia (ragweed) was extremely rare few decades ago whereas now it represents a common allergen (sensitization can be observed in about 15% of individuals attending the outpatient clinic of dermatology and allergy of Munich) [90]. All these influences of climatic factors on pollens are not only important for respiratory diseases, but also for skin disorders. Indeed, pollens can also exacerbate dermatitis and pruritus in patients with atopic eczema. This has been shown by induction of inflammation after application of pollen grains extract upon normal untreated human skin [97]. CC can also affect the diffusion of several organisms inducing allergy. Indeed, an increased occurrence of caterpillar-inducing irritant dermatitis and less frequently allergies such as ones caused by oak processionary caterpillar (Taumatopoea processionaria) is more recurrently registered [90]. Therefore, even if the greatest impact of CC for allergy and disreactive diseases relies on respiratory diseases, possible effects on cutaneous pathologies should take into account, principally for relevant influences on the natural course and the intensity of the symptoms such as the case of atopic dermatitis. Sunlight & skin tumors

Sunlight, particularly ultraviolet (UV) radiation, can lead to development of skin cancers through both a direct mechanism (inducing mutations) and an indirect mechanism (immunosuppression). Therefore, the amount of UV radiation that reaches the earth’s surface is the principal actor of the photocarcinogenesis process. The quantity of UV radiation which reaches the earth is modified by several factors: the hour of the day, latitude, season, altitude. In addition, there are other factors involved in this regulation. They are represented by the ozone layer, relative humidity (as relative humidity decreases, UV radiation increases) and cloud cover: all these factor are all deeply influenced by CC [98,99]. Particularly, as regards the stratospheric ozone, it is well known that its rate is slowing down more and more in the last decades [100,101]. As a consequence, UV radiation on earth’s surface is expected to continually rise. CC can influence the ozone layer by accelerating air circulation in the stratosphere from the Equator northward, reducing the amount of ozone in equatorial and tropical zones, which are already subject to greater UV-B radiation because light travels less distance through the atmosphere at these latitudes [102]. Climate variations may also be able to lower temperatures and the amount of water vapor in the stratosphere, leading to greater ozone loss in polar regions [102]. As a result, it is estimated that UV index will probably increase 4% in tropical zones and 20% at higher latitudes of the southern hemisphere by the end of spring and beginning of summer in 2100 [102]. As regards the relationship between skin cancers and changes in the ozone layer, models predict values ranging 175

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between an increased incidence of 9% in 2050 (if the release of all compounds that damage the ozone layer cease immediately) and 300% in the worst-case scenario [103]. It is estimated that for each 1% reduction in the thickness of the ozone layer the incidence of melanoma will probably increase between 1 and 2% [104]. The same percentage reduction in thickness may increase risk for squamous cell carcinoma between 3 and 4.6% and risk for basal cell carcinoma between 1.7 and 2.7% [105,106]. Thus, the annual age-adjusted incidence rate of melanoma tripled between 1975 and 2004 in the USA, increasing from 6.8 cases to 18.5 cases per 100,000 population [107], whereas it has been estimated that the incidence of nonmelanoma skin cancer in the Netherlands will probably double between 2000 and 2015, partly due to a large increase in population aging, but also to increased UV radiation [108]. However, it is important to note that the estimates are based on modeling the increased incidence of skin cancer due to the destruction of the ozone layer while assuming that the other factors remain unchanged. Although stratospheric ozone depletion has traditionally been held as the major factor responsible for the changes in terrestrial UV radiation, CC may also modify UV radiation through influences on other variables, such as clouds and aerosols [109]. Animal studies have shown that elevated temperatures enhance UV-induced skin cancer in comparison with that observed at room temperature. Assuming that ambient temperature would have a similar effect in humans, van der Leun and de Gruijl [103] have speculated that the longterm elevation of temperature by 2˚C, as a consequence of CC, may increase the carcinogenic effectiveness of solar UV by 10%. Hence, the harmful effects of UV-B radiation become worse at higher temperatures. Freeman and Knox have demonstrated that tumor induction increases 3–7% for every increase in temperature of 1˚C in mice [110]. Assuming a tumor induction efficacy of 5%, it is calculated that for global warming of 2˚C, tumors attributable to increased UV-B exposure would increase by 9–11% by 2050 [103]. Although climatologic factors may determine the levels of UV radiation at the earth’s surface, the behavior of individuals outdoors also plays a greater impact on personal UV exposure. Indeed, Diffey [101] proposed that behavior associated with global warming, rather than ozone depletion, may be the largest determinant of sun exposure, with a consequent impact on skin cancer. Global warming and increased temperature with warmer and drier summers increase the tendency to spend more time outdoors. As a result, the population exposure to sunlight and the UV radiation associated with it increase, contributing to enhance the risk to develop skin cancers. For example, a study in 1996 examined the different causes of UV exposure in children from different parts of the UK demonstrating that children in the warmer south-east of England received a greater amount of UV radiation during recreational activities when compared with children in the colder north-east [111]. Further studies as well as an interdisciplinary approach are necessary for deepen studying the complex effects of CC on the amount of UV radiation that reaches the earth’s surface. In 176

particular, global warming, cloud cover, relative humidity as well as temperature, air circulation and water vapor in stratosphere should be taken into account in order to analyze all the possible climatic factors that can influence exposure to UV radiation and so affect human skin. Other skin diseases

The clinical practice commonly support the concept that many different dermatoses may show marked seasonal variations regarding symptoms and degree of clinical severity. However, an accurate relationship between CC and the variations concerning several skin diseases, the intensity of their symptoms as well as their course remain still not so clear and not sufficiently investigated. The incidences of numerous cutaneous diseases change over time, and well-known seasonal variation occurs in skin diseases such as seborrheic dermatitis, scabies, miliaria [112], acne [22], psoriasis [113], pyoderma [114] and fungal dermatoses [115]. For instance, seborrheic dermatitis tends to be more prevalent during winter because the low temperature and humidity during this season are among many of its presumed etiological factors [112,116]. On the other hand, cases of papular urticaria are inclined to be more common during the rainy season; this may be attributed to the biting habits and the life cycle of the insects involved which are greatly influenced by environmental factors [117]: rainy season is a favorable time for the breeding of insects. Moreover, high temperature and humidity of summer and rainy seasons also favor rapid proliferation of pyogenic bacteria, hence high prevalence of bacterial skin infections. For example, according to Sahl and Mathewson [118], the incidence of impetigo is greatest during the summer when there is common close contact between children. Another skin disease which is deeply affected by changes in climatic factors such as temperature, humidity as well as solar radiation is atopic dermatitis [119]. Environmental factors have a strong impact on the number of flare-ups of atopic dermatitis and the intensity of symptoms, and therefore on the ensuing social effects. Thus, marked improvements are found in warm, humid climates [119]. The worsening of this dermatosis owes as much to low relative humidity which aggravates changes in the skin barrier [120] and enhances skin roughness [121]; on the other hand, low temperatures enhance skin irritability [122,123] whereas UV radiation can decrease the severity of symptoms in many people [124]. Recently, CC has also been reported to deeply affect the prevalence of atopic dermatitis [125] and, at the same time, it is well known that atopic dermatitis prevalence rates are constantly rising [11]. Consequently, CC represents one of the possible factors involved in causing the increase of the atopic eczema prevalence. Preventive measures

Human-induced CC is a reality which not only threatens our biosphere but also poses a serious threat to human health. Certainly, urgent actions at the national and international level are required to decrease emissions of greenhouse gases, which represent one of the main factors responsible for human-induced Expert Rev. Anti Infect. Ther. 12(2), (2014)

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alteration of global climate. Waiting for these interventions to act, a set of different preventive measures are needed from the point of view of the dermatologist in order to limit the impact of climatic variations on skin diseases. Indubitably, one of the key points of these actions are public health campaigns to reduce tanning and to protect the skin from sun burn, together with continuing input and indications from dermatologists for a high quality and effective photo-protection. Indeed, CC (with increased levels of UV radiation at the earth’s surface) as well as the behavior of individuals (with growing in outdoor leisure activities) is determining an increased risk of developing skin cancers through increases in sunlight exposure. But it is not just photo-protection from too much sun that must be focused upon. Special emphasis should be placed on behavioral measures that prevent major changes in the skin barrier as climatic factors are involved in modifying the natural course and intensity of symptoms of common and chronic dermatoses such as psoriasis and atopic dermatitis. These prevention measures may include, for example, maintaining a high grade of skin hydration with use of emollients, bathing in warm water using non-aggressive gels, avoiding intense friction, avoiding washing the hands and face too frequently or using breathable loose-fitting clothing. Moreover, as described above, even variations in humidity are involved in developing of skin diseases (mainly outbreak of skin infections) and alterations of skin barrier (since the optimal relative humidity to maintain correct skin hydration ranges between 40 and 60%). For these reasons, home-made humidification methods can be employed. They may include placing containers of water on radiators or using top-range air conditioners in order to regulate both, humidity and temperature to obtain optimal levels of each as well as avoiding airflow directed toward the user in the case of air conditioning or acclimatizers, whereas dwellings should be appropriately ventilated. Finally, should global warming continue, dermatologists may one day encounter outbreaks of infectious diseases with uncommon pathogens. As these organisms have a significant potential for inherent resistance to antimicrobials or for the development of antimicrobial resistance, it is strictly necessary to avoid the indiscriminate and arbitrary use of antibiotics, above all, in order to limit challenges that dermatologists may encounter in treating this climate-induced skin diseases.

Perspective

are also able to influence the frequency and the intensity of natural disasters, leading to a global rise in extreme climatic events. The skin is the most exposed organ to environment; therefore, it is not surprising that cutaneous diseases are inclined to have a high sensitivity to climate. Indeed, numerous evidences about the strict relationship between climate and skin diseases are getting more and more attention by health authorities as well as mass media. Global warming, deforestation and changes in precipitation have been linked to variations in the geographical distribution of vectors of some infectious diseases (malaria, leishmaniasis, Lyme disease, etc.) by changing their spread, so that they are getting more common even in developed countries. Global warming is responsible for a warm and humid environment which can encourage the colonization of the skin by bacteria and fungi, causing an increased incidence of skin infections. Global CC may also increase the frequency, intensity and duration of extreme weather events leading to skin infections (mostly caused by antibiotic-resistant bacteria), scabies, papular urticaria as well as leishmaniasis as highlighted by surveys regarding recent natural disasters that occurred in the USA and South-Eastern Asia. Moreover, changing climate can also influence factors that are able to regulate the amount of UV radiation on the earth’s surface like the ozone layer, the cloud cover and relative humidity leading to increased incidence of melanoma, squamous cell carcinoma and basal cell carcinoma. Finally, the incidences of some cutaneous diseases are changing over time, and well-known seasonal variation occurs in several skin diseases such as seborrheic dermatitis, scabies, miliaria, acne, psoriasis, pyoderma and fungal dermatoses. It is so clear that climatic factors are able to affect several skin diseases and their natural course. This may facilitate or worsen the incidence as well as the symptoms of many skin diseases. Therefore, climatic factors may constitute an additional challenge for dermatologists to take control of cutaneous disorders. This is true not only for chronic and common diseases such as psoriasis and atopic dermatitis which are very inclined to be influenced by environmental factors but also for infrequent and not widespread ones, especially for developed countries, such as vector- and water-borne diseases. For all the reasons reported above, CC seems to represent one of the greatest challenges of the modern age. Skin diseases we encounter may change, and we should be well prepared to face the challenges that lie ahead.

Expert commentary

Global climate appears to be changing at an unprecedented rate not only due to variations of several natural factors such as solar radiation received by earth, oceanic processes, plate tectonics, but also due to human-induced alterations of the natural world including use of fossil fuel, land consumption, deforestation and industrial processes as well as some agriculture practices. The increase of average surface temperature in the last decades draws attention to the current trend toward global warming which represents one of the most evident effects of changing climate together with variations in precipitation, atmospheric humidity changes. Moreover, all these factors www.expert-reviews.com

Five-year view

The world’s climate is constantly changing. Most recently, a great impact on this accelerated change has been attributed to global warming. Increases in average temperature cause variations in the distributions of several living organisms, including infectious pathogens and their vectors. Extreme weather conditions are increasingly reported as well as marked alterations of precipitation, humidity and wind patterns. Without proactive measures to fight CC and global warming, more than one million animal and plant species could face extinction by 2050 under various predictions. With CC promoting infectious 177

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Perspective

Balato, Megna, Ayala, Balato, Napolitano & Patruno

diseases and eroding biodiversity, the urgency to reduce greenhouse gas concentrations is now undeniable. The health impacts of global warming could be significant and should not be ignored. Given the superior adaptive capacity of mankind, it is likely that we will be able to survive global warming. The effects of climate on skin health and diseases will be an important topic for dermatology in the next decades; indeed, awareness about the potential impacts of CC on human health seems to be growing. Currently, there is some literature describing how certain skin diseases may be affected by climatic change, but more research and data collection are needed for the future. Undoubtedly, this is the time to initiate controlled action and oriented investigations to overcome the new dermatologic challenges which may characterize the modern age.

In this view, dermatologists will have to play a key role. Indeed, since the skin represents the principal exposed organ to environment, variations in cutaneous disorders are expected to be as one of the earliest as well as the most common effects of changing climate on human health. Financial & competing interests disclosure

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending or royalties. No writing assistance was utilized in the production of this manuscript.

Key issues .

Climate change (CC) includes major variations in average and peaks temperature, humidity, atmospheric pressure, precipitations, wind patterns, ocean pH and salinity, and polar glaciers which all also influence the frequency of extreme weather events.

.

The skin is the most exposed organ to environment so the cutaneous diseases are inclined to have a high sensitivity to climate.

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CC could have significant impact on the distribution and seasonality of some vector-borne diseases (i.e., malaria, dengue fever, leishmaniasis, tick-borne diseases).

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Frequent cutaneous implications associated with natural disaster are reported to be scabies, papular urticaria, eczema and leishmaniasis. In particular, flood-related disasters are commonly associated with skin infections, mostly caused by bacteria of which many are reported to be relatively antibiotic-resistant.

.

Climate variability may affect the risk of contamination events having a great impact on water-borne diseases which can also affect human skin as is the case of those caused by Dracunculus medinensis, Cyanobacter spp., Francisella tularensis and Mycobacter spp.

.

The incidences of some cutaneous diseases change over time, and well-known seasonal variation occurs in several skin diseases such as seborrheic dermatitis, scabies, miliaria, acne, psoriasis, pyoderma and fungal dermatoses.

.

There is some literature describing how certain skin diseases may be affected by climatic change, but more research and data collection are needed for the future.

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Dermatologists will play a crucial role since modifications of skin diseases are expected to be one of the most common effects of CC on human health.

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