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Impact of environmental changes on Dermatology How to cite this article: Haddad Junior V, Mendes AL, Talhari CC, Miot HA. Impact of environmental changes on Dermatology. An Bras Dermatol. 2021;96:210-23. ,☆☆ ☆☆ Study conducted at the Department of Dermatology, Faculty of Medicine, Universidade Estadual Paulista, Botucatu, SP, Brazil.

Abstract

Urbanization, pollution and the modification of natural landscapes are characteristics of modern society, where the change in human relations with the environment and the impact on biodiversity are environmental determinants that affect the health-disease relationship. The skin is an organ that has a strong interface with the environment and, therefore, the prevalence patterns of dermatoses may reflect these environmental changes. In this article, aspects related to deforestation, fires, urbanization, large-scale agriculture, extensive livestock farming, pollution and climatic changes are discussed regarding their influence on the epidemiology of skin diseases. It is important that dermatologists be aware of their social responsibility in order to promote sustainable practices in their community, in addition to identifying the impacts of environmental imbalances on different dermatoses, which is essential for the prevention and treatment of these diseases.

KEYWORDS
Climatic variations; Environment; Pollution; Radiation; Sustainability; Urbanization

Introduction

Since its inception around 100-200 thousand years ago, the history of Homo sapiens has comprised a strong interaction with the environment, especially from migrations outside Africa, where climatic, geographical and vegetation contingencies imposed adaptive pressures that resulted in much of the diversity of the species.11 Tattersall I. Out of Africa: modern human origins special feature: human origins: out of Africa. Proc Natl Acad Sci USA. 2009;106:16018-21. Without adapting to the different environmental challenges, humankind would not have occupied the entire planet.

Therefore, environmental determinants have influenced both the evolution of the species and the health of humans.22 Ellwanger JH, Kulmann-Leal B, Kaminski VL, Valverde-Villegas JM, da Veiga ABG, Spilki FR, et al. Beyond diversity loss and climate change: Impacts of Amazon deforestation on infectious diseases and public health. An Acad Bras Cienc. 2020;92:e20191375. For instance, the most accepted hypothesis for the differentiation of skin tones is due to the evolutionary gain resulting from the skin synthesis of vitamin D by UVB radiation and the folate photolysis by UVA radiation, selecting lighter skin colors in low-latitude regions.33 Rees JL, Harding RM. Understanding the evolution of human pigmentation: recent contributions from population genetics. J Invest Dermatol. 2012;132:846-53.

4 Yuen AW, Jablonski NG. Vitamin D: in the evolution of human skin colour. Med Hypotheses. 2010;74:39-44.
-55 Jablonski NG, Chaplin G. The evolution of human skin coloration. J Hum Evol. 2000;39:57-106. Geographic isolation, associated with genetic drift and sexual selection, were also important in defining the characteristics of major human groups.66 Jablonski NG, Chaplin G. Colloquium paper: human skin pigmentation as an adaptation to UV radiation. Proc Natl Acad Sci USA. 2010;107(Suppl 2):8962-8. However, this genotypic variability has implicated not only in different phenotypes, but also in the development of different physiological responses, leading to disease propensities, immunologic, metabolic and therapeutic responses.77 Flores C, Ma SF, Pino-Yanes M, Wades MS, Pérez-Méndez L, Kittles RA, et al. African ancestry is associated with asthma risk in African Americans. PLoS ONE. 2012;7:e26807.

8 Pinto P, Salgado CG, Santos N, Alencar DO, Santos S, Hutz MH, et al. Polymorphisms in the CYP2E1 and GSTM1 genes as possible protection factors for leprosy patients. PLoS ONE. 2012;7:e47498.

9 Lalueza-Fox C, Rompler H, Caramelli D, Stäubert C, Catalano G, Hughes D, et al. A melanocortin 1 receptor allele suggests varying pigmentation among Neanderthals. Science. 2007;318:1453-5.

10 Sortica Vde A, Ojopi EB, Genro JP, Callegari-Jacques S, dos Santos AR, de Moraes MO, et al. Influence of genomic ancestry on the distribution of SLCO1B1, SLCO1B3 and ABCB1 gene polymorphisms among Brazilians. Basic Clin Pharmacol Toxicol. 2012;110:460-8.

11 Suarez-Kurtz G, Pena SD. Pharmacogenomics in the Americas: the impact of genetic admixture. Curr Drug Targets. 2006;7:1649-58.

12 D'Elia MP, Brandao MC, de Andrade Ramos BR, da Silva MG, Miot LDBM, dos Santos SEMB, et al. African ancestry is associated with facial melasma in women: a cross-sectional study. BMC Med Genet. 2017;18:17.

13 Franceschini N, Chasman DI, Cooper-DeHoff RM, Arnett DK. Genetics, ancestry, and hypertension: implications for targeted antihypertensive therapies. Curr Hypertens Rep. 2014;16:461.
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While the Homo sapiens species evolved, it intensively interacted with the environment, interfering in the health-disease relationship. Human hunter and gatherer groups (such as Pygmies and Amerindian groups) caused a discreet environmental impact, as they had a shorter life expectancy and were more exposed to environmental problems, such as accidents caused by animals, floods, infestations, zoonoses and dietary restrictions (e.g., long periods of drought).1515 Prous A. O Brasil antes dos brasileiros: a pré-história do nosso país. Rio de Janeiro: Zahar; 2006.

From the moment Homo sapiens acquired a certain domain of agriculture, fishing and domestication of animals, they began to settle into territories, establishing the first population centers. This required greater use of natural resources and modification of the local environment. Thus, there was a gain in longevity, protection against natural hazards and the possibility of territorial expansion.1616 Feldens F. O Homem a Agricultura a História. 1th ed. Lajeado: Editora Univates; 2018.

With the development of industrialization and changes in the means of production, there have been demographic explosions, urbanization and migratory flows to urban areas. These factors resulted in great environmental impact, causing air, soil and water pollution, in addition to the unsustainable consumption of natural resources.1717 Kroll M, Bharucha E, Kraas F. Does rapid urbanization aggravate health disparities? Reflections on the epidemiological transition in Pune, India. Glob Health Action. 2014;7:23447.,1818 Rossi-Espagnet A, Goldstein GB, Tabibzadeh I. Urbanization and health in developing countries: a challenge for health for all. World Health Stat Q. 1991;44:185-44. From a medical point of view, the different forms of work have led to the emergence of occupational diseases and globalized transportation has disseminated infectious diseases, such as syphilis and AIDS, in addition to favoring pandemics such as the Black Plague, influenza and the disease caused by the new coronavirus (COVID-19).1919 Alchorne Ade O, Alchorne MM, Silva MM. Occupational dermatosis. An Bras Dermatol. 2010;85:137-45.

20 Mas-Coma S, Jones MK, Marty AM. COVID-19 and globalization. One Health. 2020;9:100132.

21 Krishnan L, Ogunwole SM, Cooper LA. Historical Insights on Coronavirus Disease 2019 (COVID-19), the 1918 Influenza Pandemic, and Racial Disparities: Illuminating a Path Forward. Ann Intern Med. 2020:173-474-81.

22 Shanks GD. COVID-19 versus the 1918 influenza pandemic: different virus, different age mortality patterns. J Travel Med. 2020.

23 Cohn SK. Epidemiology of the Black Death and successive waves of plague. Med Hist Suppl. 2008;:74-100.

24 Bossak BH. AIDS and the Black Death. Qjm. 2007;100:144-5.
-2525 Skorka P, Grzywacz B, Moron D, Lenda M. The macroecology of the COVID-19 pandemic in the Anthropocene. PLoS One. 2020;15:e0236856.

The historical condition of humankind reinforces its bilateral relationship with the environment, as well as establishes sociological and economic relations and determines specific health conditions. Considering the high degree of interaction between human skin and the external environment, Dermatology especially reflects the changes in the environment. The main impacts of environmental changes in the specialty will be discussed below.

Environmental degradation

Deforestation

Both urban and rural expansion modify natural landscapes, restrict native vegetation coverage, modify the geography, water and waste flow, with a direct impact on biodiversity.2626 Flies E, Clarke L, Brook BW, Jones P. Urbanisation reduces the abundance and diversity of airborne microbes-but what 1 does that mean for our health? A systematic review. Sci Total Environ. 2020;:1-8.

27 Wang R, Wu J, Yiu KF, Shen P, Lam PKS. Long-term variation in phytoplankton assemblages during urbanization: A comparative case study of Deep Bay and Mirs Bay, Hong Kong, China. Sci Total Environ. 2020;745:140993.

28 Corlett RT. The Anthropocene concept in ecology and conservation. Trends Ecol Evol. 2015;30:36-41.
-2929 Gibb R, Redding DW, Chin KQ, Donnelly CA, Blackburn TM, Newbold T, et al. Zoonotic host diversity increases in human-dominated ecosystems. Nature. 2020;584:392-02.

Deforestation, pasture development, crops and underground resources exploration have been historically associated with the emergence of arboviruses, zoonoses and other infectious diseases that arise in outbreaks or endemically, depending on how the deforestation is carried out. As forests are reduced (or become unbalanced) and the reservoirs of certain diseases are extinct, humans become involved in their natural cycle.22 Ellwanger JH, Kulmann-Leal B, Kaminski VL, Valverde-Villegas JM, da Veiga ABG, Spilki FR, et al. Beyond diversity loss and climate change: Impacts of Amazon deforestation on infectious diseases and public health. An Acad Bras Cienc. 2020;92:e20191375.,2929 Gibb R, Redding DW, Chin KQ, Donnelly CA, Blackburn TM, Newbold T, et al. Zoonotic host diversity increases in human-dominated ecosystems. Nature. 2020;584:392-02.

30 Walsh JF, Molyneux DH, Birley MH. Deforestation: effects on vector-borne disease. Parasitology. 1993;106(Suppl):S55-75.
-3131 Pignatti MG. Health and environment: emergent diseases in Brazil. Ambient Soc. 2004;7:133-47.

Examples that emerged from this imbalance: malaria epidemics after the construction of the Panama Canal, mining and the construction of railroads in the northern region of Brazil; the yellow fever epidemic on the coast of northeastern Brazil during the 17th century sugarcane expansion and the rabies outbreak on the island of Marajó (2018), Brazil, after agricultural expansion.3232 Hurtado LA, Caceres L, Chaves LF, Calzada JE. When climate change couples social neglect: malaria dynamics in Panama. Emerg Microbes Infect. 2014;3:e27.

33 Jarcho S. Ferreyra da Rosa on yellow fever in Pernambuco. Bull N Y Acad Med. 1972;48:1343-5.

34 Hofman MPG, Hayward MW, Heim M, Marchand P, Holandsen JM, Urbano F, et al. Right on track? Performance of satellite telemetry in terrestrial wildlife research. PLoS One. 2019;14:e0216223.

35 Pereira AS, Casseb LMN, Barbosa TFS, Begot AL, Brito RMO, Vasconcelos PFC, et al. Rabies Virus in Bats, State of Para, Brazil, 2005-2011. Vector Borne Zoonotic Dis. 2017;17:576-81.
-3636 Benchimol JL, Silva AFCd. Railroads, disease, and tropical medicine in Brazil under the First Republic. História, Ciências. Saúde - Manguinhos. 2008;15:719-62. Likewise, the recent COVID-19 pandemic originated in an industrialized area in China (Wuhan), possibly caused by human interaction with contaminated bats as a result of restrictions in their ecosystem, which should alert humankind about the emergence of environmental issues as a priority in the sustainable development of modern society.2525 Skorka P, Grzywacz B, Moron D, Lenda M. The macroecology of the COVID-19 pandemic in the Anthropocene. PLoS One. 2020;15:e0236856.,3737 Tollefson J. Why deforestation and extinctions make pandemics more likely. Nature. 2020;584:175-6.,3838 Carlson CJ, Chipperfield JD, Benito BM, Telford RJ, O'Hara RB. Don't gamble the COVID-19 response on ecological hypotheses. Nat Ecol Evol. 2020;4:1155.

In Dermatology, American tegumentary leishmaniasis (ATL) is caused by protozoa of the genus Leishmania, which causes skin ulcers (Fig. 1) and can affect mucous membranes in later stages. It is transmitted by mosquitoes of the genus Phlebotomus, and has a zoonotic cycle in mammals, especially marsupials and rodents.3939 Gontijo B, de Carvalho Mde L. [American cutaneous leishmaniasis]. Rev Soc Bras Med Trop. 2003;36:71-80.

40 Ashford RW. Leishmaniasis reservoirs and their significance in control. Clin Dermatol. 1996;14:523-32.
-4141 Roque AL, Jansen AM. Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wildl. 2014;3:251-62. In Brazil, the description of ATL was first reported during the construction of the Northwest Railway, in the beginning of the 20th century. This railroad was designed to transport the coffee production from the countryside of the Brazilian states of São Paulo and Mato Grosso. This entire area has large populations of sandflies, and the disease received the name of “Bauru ulcer” because Bauru is an important city in that region.3636 Benchimol JL, Silva AFCd. Railroads, disease, and tropical medicine in Brazil under the First Republic. História, Ciências. Saúde - Manguinhos. 2008;15:719-62.

Figure 1
American cutaneous leishmaniasis. Facial ulcer, with an erythematous, infiltrated border and granular bottom; in a farmer from the Tietê river valley.

The incidence of ATL has been increasing in the last 30 years in practically all states of Brazil, with outbreaks being described in the Southeast, Midwest, Northeast and Amazon regions. Most cases of ATL are associated with the predatory process of colonization, road construction, new population centers and expansion of agricultural activities.4242 ECSd Vale, Furtado T. Tegumentary leishmaniasis in Brazil: a historical review related to the origin, expansion and etiology. An Bras Dermatol. 2005;80:421-8.,4343 Lima AP, Minelli L, Teodoro U, Comunello É. Tegumentary leishmaniasis distribution by satellite remote sensing imagery, in Paraná State, Brazil. An Bras Dermatol. 2002;77:681-92.

Deforestation can cause the migration of infectious agents into vectors in urban areas, favoring epidemics. This has been observed with yellow fever, previously transmitted by the Haemagogus mosquito in wild areas, which showed phases of intense transmission in the cities by the Aedes aegypti.4444 Couto-Lima D, Madec Y, Bersot MI, Campos SS, Motta MA, dos Santos FB, et al. Potential risk of re-emergence of urban transmission of Yellow Fever virus in Brazil facilitated by competent Aedes populations. Sci Rep. 2017;7:4848. Similarly, Aedes albopictus, the other disseminator of viral diseases originally from Asia and Africa, was recently introduced in Brazil and is also a vector of dengue fever, zika and chikungunya.4545 Barrett AD, Monath TP. Epidemiology and ecology of yellow fever virus. Adv Virus Res. 2003;61:291-315.,4646 Wilkinson RL. Yellow fever: ecology, epidemiology, and role in the collapse of the Classic lowland Maya civilization. Med Anthropol. 1995;16:269-94. Deforestation and the depletion of natural reservoirs is the main explanation for the occurrence of autochthonous cases of ATL in metropolitan areas, Chagas disease and (human) rabies caused by attacks of hematophagous bats in cities.4747 Bernardes Filho F, Bonatto DC, Martins G, Maier Lde M, Nery JA, Azulay-Abulafia L. Occurrence of two autochthonous cases of American cutaneous leishmaniasis in the neighborhood of Caju, city of Rio de Janeiro, Brazil. An Bras Dermatol. 2014;89:848-50.

48 Carneiro FRO, Amin GA, Cruz LBP, Daher BA. Urban American cutaneous leishmaniasis. An Bras Dermatol. 2018;93:156-8.

49 Gil JF, Nasser JR, Cajal SP, Juarez M, Acosta M, Cimino RO, et al. Urban transmission of American cutaneous leishmaniasis in Argentina: spatial analysis study. Am J Trop Med Hyg. 2010;82:433-40.

50 Passos VM, Falcao AL, Katz N. Urban American cutaneous leishmaniasis in the Metropolitan Region of Belo Horizonte, Minas Gerais State, Brazil. Mem Inst Oswaldo Cruz. 1990;85:243-4.

51 Schneider MC, Aron J, Santos-Burgoa C, Uieda W, Ruiz-Velazco S. Common vampire bat attacks on humans in a village of the Amazon region of Brazil. Cad Saude Publica. 2001;17:1531-6.

52 Sousa ADSJ, Palacios V, Miranda CDS, da Costa RJF, Catete CP, Chagasteles EJ, et al. Space-temporal analysis of Chagas disease and its environmental and demographic risk factors in the municipality of Barcarena, Para, Brazil. Rev Bras Epidemiol. 2017;20:742-55.

53 Mendes Wda S, Silva AA, Neiva RF, Costa NM, de Assis MS, Vidigal PMO, et al. An outbreak of bat-transmitted human rabies in a village in the Brazilian Amazon. Rev Saude Publica. 2009;43:1075-7.
-5454 Benicio E, Cordeiro M, Monteiro H, Moura MAS, Oliveira C, Gadelha EPN, et al. Sustained Presence of Cutaneous Leishmaniasis in Urban Manaus, the Largest Human Settlement in the Amazon. Am J Trop Med Hyg. 2015;93:1208-13.

The “fogo selvagem” subtype of pemphigus foliaceus differs from the type described by Cazenave in that it affects younger patients (under 45 years old) and has an endemic characteristic (between longitudes 45°-60 °W and latitudes 5°-25 °S, and at altitudes between 500-800 m). Endemic pemphigus foliaceus is an autoimmune bullous dermatosis characterized by an erythematous-desquamative rash with exulcerations due to the rupture of fragile bullous lesions with a craniocaudal distribution, with photosensitivity and without mucosal involvement (Fig. 2). The pathogenesis of the disease is associated with epitope spreading, in which repeated exposure to insect bites (Simulium nigrimanum) would increase the production of pathogenic antibodies of the IgG4 subclass that lead to the recognition of the EC1 and EC2 domains of Desmoglein-1.5555 Aoki V, Lago F, Yamazaki MH, Santi CG, Maruta CW. Significance of epitope spreading in the pathogenesis of pemphigus vulgaris and foliaceus. An Bras Dermatol. 2008;83:157-61.,5656 Li N, Aoki V, Hans-Filho G, Rivitti EA, Diaz LA. The role of intramolecular epitope spreading in the pathogenesis of endemic pemphigus foliaceus (fogo selvagem). J Exp Med. 2003;197:1501-10. During the 20th century, there was a great increase in the incidence of the disease along areas of deforestation in the countryside of Brazil, especially in the states of São Paulo, Mato Grosso, Goiás and Minas Gerais, following large river basins.5757 Campbell I, Reis V, Aoki V, Cunha P, Filho GH, Alves G, et al. Endemic pemphigus foliaceous. An Bras Dermatol. 2001:13-33.

Figure 2
Fogo selvagem or endemic pemphigus foliaceus. Extensive exulcerations with hematic crusts on the back in a young resident of the Tietê river valley.

Territorial and biodiversity restrictions promoted by deforestation affect the reproduction of large predators, which demand a greater food load. Moreover, the recent description of attacks on humans by wild animals (e.g., monkeys, jaguars, anteaters, coatis) can be justified by food restrictions that affect the animals and their forced proximity to urban centers.5858 Neto MF, Garrone Neto D, Haddad V. Attacks by jaguars (Panthera onca) on humans in central Brazil: report of three cases, with observation of a death. Wilderness Environ Med. 2011;22:130-5.

59 Bittner GC, Ritter Hans N, Hans Neto G, Morais MO, Hans Filho G, Haddad V. Coati (Nasua nasua) attacks on humans: case report. Wilderness Environ Med. 2010;21:349-52.
-6060 Haddad V, Assuncao MC, de Mello RC, Duarte MR. A fatal attack caused by a lowland tapir (Tapirus terrestris) in southeastern Brazil. Wilderness Environ Med. 2005;16:97-100.

The numerical restriction (or extinction) of predators may also explain the proliferation and increased incidence of accidents with scorpions, especially in the Northeast and Southeast regions of Brazil.6161 Chippaux JP. Epidemiology of envenomations by terrestrial venomous animals in Brazil based on case reporting: from obvious facts to contingencies. J Venom Anim Toxins Incl Trop Dis. 2015;21:13.,6262 Reckziegel GC, Pinto Junior VL. Analysis of the scorpionism in Brazil from 2000 to 2010. Rev Pan-Amaz Saude. 2014;5:67-8.

The occurrence of spotted fever outbreaks in the countryside of the state of São Paulo is attributed to the increase in the population of capybaras and other natural reservoirs of Rickettsia sp., which are protected by the prohibition of hunting. Also, with the decrease in the number of predators such as large felines, the populations of capybaras have increased exponentially and this has contributed to the spread of infected ticks (mainly Amblyomma sp.) spreading the disease to areas where domestic animals and the human population live.3131 Pignatti MG. Health and environment: emergent diseases in Brazil. Ambient Soc. 2004;7:133-47.,6363 de Lima VL, Figueiredo AC, Pignatti MG, Modolo M. [Spotted fever in the town of Pedreira, Sao Paulo state, Brazil. The relationship between the occurrence of cases and human parasitism by ixodid ticks]. Rev Soc Bras Med Trop. 1995;28:135-7.,6464 Santos M, Haddad Júnior V, Ribeiro-Rodrigues R, Talhari S. Borreliose de Lyme. An Bras Dermatol. 2010;85:930-8.

As a result of the same environmental imbalance, Lyme disease in the American continent is caused mainly by the spirochete Borrelia burgdorferi (sensu lato) and transmitted by tick bites. It originally occurs among wild animals, being described in European and North American deer populations. However, it is also present in Brazil, affecting both deer and capybaras, whichspread the disease to domestic animals and humans when living close to urban centers. The disease has an early cutaneous manifestation (erythema chronicum migrans), which can trigger sclerodermiform reactions and is potentially severe (Fig. 3).6565 Santos M, Ribeiro-Rodrigues R, Talhari C, Ferreira LC, Zelger B, Talhari S. Presence of Borrelia burgdorferi "Sensu Lato" in patients with morphea from the Amazonic region in Brazil. Int J Dermatol. 2011;50:1373-8. The Brazilian variant of Lyme disease (borreliosis-like illness, or Baggio-Yoshinari syndrome) needs further studies, especially since its incidence seems to be underestimated considering the number of clinical manifestations that may not be exactly the same as classic Lyme disease (European or North American).6666 LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci USA. 2003;100:567-71.

67 Vien VP, Bassi R, Maxim T, Bogoch II. Lyme disease vs Baggio-Yoshinari syndrome in a returned traveller from Brazil. J Travel Med. 2017;24.

68 Gouveia EA, Alves MF, Mantovani E, Oyafuso LK, Bonoldi VL, Yoshinari NH. Profile of patients with Baggio-Yoshinari Syndrome admitted at "Instituto de Infectologia Emilio Ribas". Rev Inst Med Trop Sao Paulo. 2010;52:297-303.

69 Yoshinari NH, Mantovani E, Bonoldi VL, Marangoni RG, Gauditano G. [Brazilian lyme-like disease or Baggio-Yoshinari syndrome: exotic and emerging Brazilian tick-borne zoonosis]. Rev Assoc Med Bras (1992). 2010;56:363-9.
-7070 Talhari S, de Souza Santos MN, Talhari C, Ferreira LCL, Silva Jr RM, Zelger B, et al. Borrelia Burgdorferi "sensu lato" in Brazil: Occurrence confirmed by immunohistochemistry and focus floating microscopy. Acta Trop. 2010;115:200-4.

Figure 3
(A), Erythema chronicum migrans as the early manifestation of borreliosis-like illness. (B), Remission of clinical picture after treatment with doxycycline (Kindly provided by Prof. Sinésio Talhari).

Brazil has the largest freshwater network in the world. Due to this fact, the main national energy matrix was developed based on the construction of hydroelectric power plants, especially starting from the 1950s, leading to the flooding of more than 34,000 km2.7171 Oliveira NCC. The Great Acceleration and Hydroelectric Dam Building in Brazil. Varia Historia. 2018;34:315-46. Large water dams, however, promote profound and damaging changes to the geography and the riverside ecosystem. The influence of the changes in the local microclimate (temperature and rainfall) will be discussed later. Changes in the aquatic fauna, both by reducing river flows and by the non planned introduction of fish species, are environmental determinants of health problems.7272 de Queiroz AR, Motta-Veiga M. [Analysis of the social and health impacts of large hydroelectric plants: lessons for a sustainable energy management]. Cien Saude Colet. 2012;17:1387-98.

73 Giongo CR, Mendes JMR, Santos FK. Development, health and environment: contradictions in the construction of dams. Serv Soc Soc. 2015;:501-22.
-7474 Haines A, Smith KR, Anderson D, Epstein PR, McMichael AJ, Roberts I, et al. Policies for accelerating access to clean energy, improving health, advancing development, and mitigating climate change. Lancet. 2007;370:1264-81.

Freshwater stingrays, for instance, are native animals from the North and Midwest regions of Brazil. After the construction of rainwater dams, natural barriers were reduced. This favored the mobilization of fish downstream the Paraná river, precipitating severe accidents involving fishermen and bathers in the Southeastern region, including the state of São Paulo and the Tietê river (Fig. 4). 7575 Garrone Neto D, Haddad Junior V. [Stingrays in rivers in southeastern Brazil: occurrence localities and impact on the population]. Rev Soc Bras Med Trop. 2010;43:82-8. Similarly, piranhas have settled in dammed areas and have caused a series of accidents among bathers in the summer season (Fig. 5).7676 Haddad V, Sazima I. Piranha attacks in dammed streams used for human recreation in the State of Sao Paulo, Brazil. Rev Soc Bras Med Trop. 2010;43:596-8.,7777 Haddad V, Sazima I. Piranha attacks on humans in southeast Brazil: epidemiology, natural history, and clinical treatment, with description of a bite outbreak. Wilderness Environ Med. 2003;14:249-54.

Figure 4
Freshwater stingrays (Potamotrygon sp.) associated with severe accidents with bathers and fishermen at the Paraná River basin. Detail of the serrated stinger. Skin lesions due to stingray accidents: lower-limb ulcers on an extensive livedoid base (< 72 h) that develops into necrosis and eschar (> 7 days).

Figure 5
River resort (municipality of Adolfo-SP, 21°09'56"S, 49°43'03"W) at a reservoir area of the Tietê River. Accidents due to piranha attacks on bathers: punched-out ulcers in the foot. Details of the adult animal and the triangular teeth (Serrasalmus maculatus).

Finally, deforestation has also changed the regional rainfall cycle, where the impact on biodiversity extends beyond the deforested area. In the beginning of the 20th century, the city of São Paulo was known as the “land of drizzle” due to the intense rainfall resulting from the surrounding dense Atlantic forest and its rich hydrography. Currently, it is the largest megalopolis in Latin America, and the extensive urban “heat island” has substantially modified the region's microclimate. The progressive deforestation of the Amazon region is also noticeable with the reduction of the pluviometric index in the Northern region of Brazil that has occurred in the last 50 years.7878 Amorim TX, Senna MCA, Cataldi M. Impactos do desmatamento progressivo da Amazônia na precipitação do Brasil. Rev Bras Climatol. 2019;24:151-74.

A process of deforestation of small areas used by indigenous and quilombola populations is the burning of vegetation (coivaras), which consists in a controlled and restricted use of fire. The fire is limited by firebreaks, which are deforested areas to interrupt the continuity of combustion, causing minimal environmental damage. However, the recent fires in extensive areas of the Brazilian Pantanal and the Amazon rainforest (as in Australia and Argentina) are attributed both to spontaneous combustion during drought periods and to the deforestation practice by residents, mainly for the expansion of pastures and agriculture.7979 Leonel M. O uso do fogo: o manejo indígena e a piromania da monocultura. Estudos Avançados. Estudo Av. 2000;14:231-50.

The reduction of rainfall favors the spread of fire outbreaks, which in addition to the massive air pollution and damage to biodiversity, promote the rapid migration of wild animals and disease vectors fleeing their burning habitat. In this context, the chances of accidents with animals and the transmission of zoonoses in urban areas near the burned regions increase.

Large-scale agriculture

The production of food for the planet's current population demand depends on the improvement of production techniques and this includes the mechanization of crops, genetic engineering and the use of pesticides.

Since the 1950s, pesticides have been gradually included in Brazilian agriculture. However, the training of farmers for their use and management has not accompanied this trend, causing damage to human health and the environment. The lack of individual protection when handling the pesticides favors skin and respiratory toxicity.8080 Ribas PP, Matsumura ATS. A química dos agrotóxicos: impacto sobre a saúde e meio ambiente. Revista Liberato. 2009;10:149-58.,8181 Spiewak R. Pesticides as a cause of occupational skin diseases in farmers. Ann Agric Environ Med. 2001;8:1-5.

Occupational or industrial exposure to chlorinated hydrocarbons (dinitrophenol, pentachlorophenol) leads to chloracne-like acneiform rashes (Fig. 6).1919 Alchorne Ade O, Alchorne MM, Silva MM. Occupational dermatosis. An Bras Dermatol. 2010;85:137-45. The handling of organophosphates, carbamates, pyrethroids and dipyridyls leads to the development of allergic and irritant contact dermatitis.8080 Ribas PP, Matsumura ATS. A química dos agrotóxicos: impacto sobre a saúde e meio ambiente. Revista Liberato. 2009;10:149-58. Exposure to pesticides has also been identified as a risk factor for some types of skin cancer, including squamous cell carcinoma and melanoma. Arsenic is believed to be the main carcinogen involved in this process.8282 Dennis LK, Lynch CF, Sandler DP, Alavanja MC. Pesticide use and cutaneous melanoma in pesticide applicators in the agricultural heath study. Environ Health Perspect. 2010;118:812-7.,8383 Kennedy C, Bajdik CD, Willemze R, Bouwes Bavinck JN. Chemical exposures other than arsenic are probably not important risk factors for squamous cell carcinoma, basal cell carcinoma and malignant melanoma of the skin. Br J Dermatol. 2005;152:194-7.

Figure 6
Chloracne. Farmer from the Tietê river valley with extensive papulopustular eruption with comedones. He reports unprotected handling of pesticides containing hexachlorobenzene (banned from use in Brazil in the 1980s). Three other family members were affected.

The mechanization of agriculture has greatly reduced the direct contact of farmers with the land and vegetation, which, in addition to requiring fewer professionals to perform the same activity, has also required greater professional qualification in the field. In the context of Dermatology, besides reducing occupational accidents and those caused by poisonous animals, the mechanization has also promoted a reduction in cases of deep mycoses in rural areas.8484 Miguel LMZ, Jorge MFS, Rocha B, Miot HA. Incidence of skin diseases diagnosed in a public institution: comparison between 2003 and 2014. An Bras Dermatol. 2017;92:423-5. The incidence of paracoccidioidomycosis has been steadily declining in the last 30 years, also because there is the interference of air humidity, water reservoirs and atmospheric pressure on the viability of fungi in the soil. States in the Amazon region (e.g. Rondônia), still maintain the most significant indicators due to a more most recent development of the agricultural activity.8585 Vieira Gde D, Alves Tda C, Lima SM, Camargo LM, Sousa CM. Paracoccidioidomycosis in a western Brazilian Amazon State: clinical-epidemiologic profile and spatial distribution of the disease. Rev Soc Bras Med Trop. 2014;47:63-8.

86 Hrycyk MF, Garcia Garces H, Bosco SMG, de Oliveira SL, Marques SA, Bagagli E. Ecology of Paracoccidioides brasiliensis, P. lutzii and related species: infection in armadillos, soil occurrence and mycological aspects. Med Mycol. 2018;56:950-62.
-8787 Restrepo A. The ecology of Paracoccidioides brasiliensis: a puzzle still unsolved. Sabouraudia. 1985;23:323-34.

Genetic modifications of seeds (transgenic plants), the cultivation of non-native species, large-scale agriculture and extensive livestock farming demand deforestation and promote an important reduction in biodiversity, favoring the emergence of health problems.

Urbanization

The Brazilian demographic transition of the last century was characterized by rural-urban population migration, industrialization and the modification of the age pyramid. Few municipalities, however, showed a planned and sustainable development, resulting in problems related to housing, access to health, drinking water and basic sanitation (Fig. 7).8888 Vasconcelos AMN, Gomes MMF. . Demographic transition: the Brazilian experience. Epidemiol Serv Saude. 2012;21:539-48.,8989 Libânio PAC, Chernicharo CAdL, Nascimento NdO. The water quality dimension: an evaluation of the relationship between social, water availability, water services and public health indicators. Eng Sanit Amb. 2005;10:219-28. This situation constitutes a major challenge for public health policies because it depends on the knowledge and modification of its social determinants, instead of just promoting diagnoses and offering medications.9090 Buss PM, Pellegrini Filho A. Health and its social determinants. Physis. 2007;17:77-93.

Figure 7
Non planned urbanization process in an indigenous village in the upper Solimões region, state of Amazonas (Kindly provided by Prof. Sinésio Talhari).

Large urban agglomerations as well as the need for means of mass transportation (e.g., trains, buses) constitute challenges for the control of diseases with respiratory transmission such as tuberculosis and COVID-19; their progression in large cities is more evident than in municipalities with low population density.9191 Lima SVMA, Rocha JVM, de Araujo KCGM, Nunes MAP, Nunes C. Determinants associated with areas with higher tuberculosis mortality rates: an ecological study. Trop Med Int Health. 2020;25:338-45.,9292 Maroko AR, Nash D, Pavilonis BT. COVID-19 and Inequity: a Comparative Spatial Analysis of New York City and Chicago Hot Spots. J Urban Health. 2020;97:461-70.

In Dermatology, ectoparasitoses are mainly influenced by urban agglomerations and poor sanitary conditions. The prevalence of scabies in the slums in the Brazilian Northeast region affects up to 8.8% of residents, while pediculosis can affect 43.4%.9393 Heukelbach J, Wilcke T, Winter B, Feldmeier H. Epidemiology and morbidity of scabies and pediculosis capitis in resource-poor communities in Brazil. Br J Dermatol. 2005;153:150-6. As a complicating factor, the indiscriminate use of pyrethroids to treat pediculosis of the scalp allowed the emergence of resistant strains of Pediculus humanus var. capitis, resulting in greater difficulty in infestation control and in restricting the epidemic (Fig. 8).9494 Hemingway J, Miller J, Mumcuoglu KY. Pyrethroid resistance mechanisms in the head louse Pediculus capitis from Israel: implications for control. Med Vet Entomol. 1999;13:89-96.,9595 Larkin K, Rodriguez CA, Jamani S, Fronza G, Roca-Acevedo G, Sanchez A, et al. First evidence of the mutations associated with pyrethroid resistance in head lice (Phthiraptera: Pediculidae) from Honduras. Parasit Vectors. 2020;13:312.

Figure 8
Pediculus humanus capitis. Causal agent of pediculosis of the scalp, endemic in large urban agglomerations.

Sexually-Transmitted Infections (STIs), especially syphilis, Human Papillomavirus (HPV) anogenital warts, Human Immunodeficiency Virus (HIV), gonorrhea, non-gonococcal urethritis (e.g., Chlamydia sp.) and genital herpes have shown an increased incidence in the last two decades in several countries.9696 Avelleira JCR, Bottino G. Syphilis: diagnosis, treatment and control. An Bras Dermatol. 2006;81:111-26.,9797 Gerbase AC, Rowley JT, Mertens TE. Global epidemiology of sexually transmitted diseases. Lancet. 1998;351(Suppl 3):2-4. The economic development associated with urbanization favors the increase of prostitution and more sexual intercourse, maximizing the risk of STI transmission.22 Ellwanger JH, Kulmann-Leal B, Kaminski VL, Valverde-Villegas JM, da Veiga ABG, Spilki FR, et al. Beyond diversity loss and climate change: Impacts of Amazon deforestation on infectious diseases and public health. An Acad Bras Cienc. 2020;92:e20191375.,9898 Boon ME, van Ravenswaay Claasen HH, van Westering RP, Kok LP. Urbanization and the incidence of abnormalities of squamous and glandular epithelium of the cervix. Cancer. 2003;99:4-8.,9999 Ressler RW, Waters MS, Watson JK. Contributing factors to the spread of sexually transmitted diseases: The case of welfare. Am J Econ Sociol. 2006;65:943-61. The formation of new communities of workers for the construction of hydroelectric power plants, mining parks or planned cities (e.g., Brasilia, Teresina and Palmas) have historically accompanied an increase in firearm violence and STIs.100100 Figueiredo ACP, Saraiva LJC. A prostituição em grandes projetos na Amazônia: o impacto do grande capital nos fluxos de mão de obra na UHE Belo Monte. Nova Revista Amazônica. 2018;6:69-77.

101 White JH. The drowned prostitute: national development, public morality, and the shifting geography of sexual commerce in Alto Parana, Paraguay, 1974-1982. J Lat Amer Geogr. 2013;:125-49.

102 Neto VJ, dos Santos JC. The frontier violence practices: study on diamond mining in Juína, MT (1987-1994). História: Debates e Tendências. 2018;18:214-28.
-103103 Dos Santos JC, Castravechi LA. Relações de trabalho na Amazônia Mato-Grossense: o uso da violência contra peões e garimpeiros. Élisée-Revista de Geografia da UEG. 2014;3:26-48.

Some animals previously found only in rural areas have adapted to cities due to the lack of predators and to obtain food supplies from produced by humans such as the Loxosceles spider, which cause severe accidents with ulcer formation and kidney damage in its victims (Fig. 9).104104 Málaque CMSa, Castro-Valencia JE, Cardoso JLC, FranÇa FOdS, Barbaro KC, Hui WF. Clinical and epidemiological features of definitive and presumed loxoscelism in Sao Paulo. Brazil. Rev Inst Med Trop Sao Paulo. 2002;44:139-43. Certain cities such as Curitiba, in the southern region of Brazil, record thousands of accidents annually.105105 Marques-da-Silva E, Souza-Santos R, Fischer M, Rubio G. Loxosceles spider bites in the state of Paraná, Brazil: 1993-2000. J Venom Anim Toxins Incl Trop Dis. 2006;12:110-23. Another example is the proliferation of pigeons from Europe and North Africa (Columba livia) in urban areas, increasing the risk of systemic mycoses such as cryptococcosis and infestations such as gamasoidosis, which have been recorded in several parts of the country.106106 de Oliveira Alves A, Bernardes Filho F. Gamasoidosis (bird mite dermatitis): A case series in a family. Pediatr Neonatol. 2018;59:102-3.

107 Suzuki CMP, Stolf HO, Camargo RMPd, Haddad V. Gamasoidose ou dermatite por ácaros aviários: relato de caso. Diagn Tratamento. 2014;19:74-6.

108 Costa AK, Sidrim JJ, Cordeiro RA, Brilhante RS, Monteiro AJ, Rocha MF. Urban pigeons (Columba livia) as a potential source of pathogenic yeasts: a focus on antifungal susceptibility of Cryptococcus strains in Northeast Brazil. Mycopathologia. 2010;169:207-13.
-109109 Spina-Tensini T, Muro MD, Queiroz-Telles F, Strozzi I, Moraes ST, Petterle RR, et al. Geographic distribution of patients affected by Cryptococcus neoformans/Cryptococcus gattii species complexes meningitis, pigeon and tree populations in Southern Brazil. Mycoses. 2017;60:51-8.

Figure 9
Skin ulcer with necrotic eschar formation derived from an accident caused by a spider of the genus Loxosceles (>96 h). Example of an adult brown spider (Loxosceles sp.).

The non planned urbanization of municipalities promotes important changes in the natural landscape, with an impact that goes beyond biodiversity and affects the local microclimate. The systematic drainage of water courses associated with extensive waterproofing of the soil and reduction of the vegetation cover, modify both the thermal stabilization capacity of water bodies and the terrestrial albedo (solar energy reflection coefficient). These elements promote a significant increase in temperature, amplified by the reduction of air circulation resulting from the successive construction of skyscrapers and by the production of heat from human activity (e.g., automobile traffic). The formation of these heat islands resultant from urbanization can change the temperature in the center of an urban area by more than 6 °C in relation to the adjacent rural area, with an important decrease in humidity and a reduction in the dispersion of air pollutants, which can favor several risks to human health.110110 Zhou B, Rybski D, Kropp JP. The role of city size and urban form in the surface urban heat island. Sci Rep. 2017;7:4791.

111 Gui X, Wang L, Yao R, Yu D, Li C. Investigating the urbanization process and its impact on vegetation change and urban heat island in Wuhan, China. Environ Sci Pollut Res Int. 2019;26:30808-25.

112 Mariani L, Parisi SG, Cola G, Lafortezza R, Colangelo G, Sanesi G. Climatological analysis of the mitigating effect of vegetation on the urban heat island of Milan, Italy. Sci Total Environ. 2016;569-570:762-73.

113 Susca T, Gaffin SR, Dell'osso GR. Positive effects of vegetation: urban heat island and green roofs. Environ Pollut. 2011;159:2119-26.

114 Costa DFd, Silva HR, Peres LdF. Identification of urban heat islands in Ilha Solteira - SP municipality using geotecnologies. Eng Agr. 2010;30:974-85.
-115115 Lemes MdCR, Reboita MS, Torres RR. Mudança no uso e cobertura da terra na bacia do rio tietê e seus impactos na temperatura da superfície (TS). Rev Bras Climatol. 2020;27:224-40.

Fig. 10 shows the effect the heat island inflicted on air temperature and humidity in the last 70 years in the metropolitan area of the municipality of São Paulo (Latitude: 23°32'56”S, Longitude: 46°38'20”W; altitude: 745 m), compared to the small rural municipality of São Simão (Latitude: 21°28'41”S, Longitude: 47°33'3”W; altitude: 663 m). There has been a consistent and progressive increase in the average temperature (+ 3.2 °C) and a reduction in the relative humidity of the air (-10%) in the metropolitan area, while the temperature and humidity naturally oscillated during the temporal series in the rural municipality.

Figure 10
Temporal series (1960 to 2019) of monthly temperature averages (A and B) and relative humidity (C and D) in the municipalities of São Paulo-SP and São Simão-SP. (Source: INMET).

The modification of the terrestrial albedo by construction of buildings and the paving of soil also promotes greater reflection of ultraviolet radiation, which potentially worsens photoinduced dermatoses, such as melasma, rosacea, lupus erythematosus and the skin field cancerization.8484 Miguel LMZ, Jorge MFS, Rocha B, Miot HA. Incidence of skin diseases diagnosed in a public institution: comparison between 2003 and 2014. An Bras Dermatol. 2017;92:423-5.,116116 Schalka S, Steiner D, Ravelli FN, Steiner T, Terena AC, Marçon CR, et al. Brazilian consensus on photoprotection. An Bras Dermatol. 2014;89:1-74.

Large cities (especially megalopolises) create vast islands of heat and air pollution, which are primarily associated with diseases linked to hypersensitivity, such as asthma, conjunctivitis and atopic dermatitis.117117 Wong LP, Alias H, Aghamohammadi N, Aghazadeh S, Nik Sulaiman NM. Physical, Psychological, and Social Health Impact of Temperature Rise Due to Urban Heat Island Phenomenon and Its Associated Factors. Biomed Environ Sci. 2018;31:545-50.

118 Heaviside C, Macintyre H, Vardoulakis S. The Urban Heat Island: Implications for Health in a Changing Environment. Curr Environ Health Rep. 2017;4:296-305.
-119119 Tan J, Zheng Y, Tang X, Guo C, Li L, Song G, et al. The urban heat island and its impact on heat waves and human health in Shanghai. Int J Biometeorol. 2010;54:75-84. The specific effects of air pollution on the skin will be discussed below.

Heat islands also interfere with the activity and reproduction of insects and arachnids. In Curitiba, the number of accidents by brown spiders showed a seasonal behavior, especially when the surface temperature exceeded 30 °C.120120 Pinto LR, de Assis Mendonça F, Araújo WM. A influência das variações térmicas nos acidentes loxoscélicos em Curitiba/PR. Rev Bras Climatol. 2017;5:55-69.

The effect of heat on cultural rites linked to clothing (suits, synthetic clothes, closed shoes) and the manner of working (e.g., poorly ventilated production lines), promotes sweating and increased sebum production, which favor bacterial and fungal infections.

Urbanization, when associated with the lack of control of proliferation of stray domestic animals such as dogs and cats, in parallel with the lack of predators in the urban environment, also favors the emergence of zoonoses. Sporotrichosis is a subcutaneous mycosis caused by the fungus Sporothrix schenckii, more frequently found in countries with tropical or subtropical climates. In the skin, it manifests mainly as ulcers and ascending nodular lymphangitis (Fig. 11).121121 Orofino-Costa R, Macedo PM, Rodrigues AM, Bernardes-Engemann AR. Sporotrichosis: an update on epidemiology, etiopathogenesis, laboratory and clinical therapeutics. An Bras Dermatol. 2017;92:606-20.

Figure 11
Cutaneous-lymphatic sporotrichosis, ulcer on the left hand dorsum, accompanied by ascending nodular lymphangitis in a young adult male who “adopted” an infected street animal. Picture detail showing the cat with an ulcer on the nose, a characteristic representation of feline sporotrichosis.

In Brazil, sporotrichosis of occupational origin, caused by trauma with vegetables (“gardener's disease”) had its incidence reduced to the detriment of contamination by animals, which is on the rise among young adults, especially due to scratches or bites by contaminated cats, the main agents involved in this zoonotic chain.122122 Cordeiro FN, Bruno CB, Paula CD, Motta Jde O. Familial occurrence of zoonotic sporotrichosis. An Bras Dermatol. 2011;86:S121-4. Felines have a high fungal load due to the habit of scratching trees, traveling long distances and engaging in fights, which favors contamination. The access of non-neutered cats to the streets, the abandonment or sacrifice of sick animals by the guardian, inadequate disposal of carcasses, associated with the lack of integration between the Epidemiological Surveillance and the Zoonosis Control Center of the municipalities are acts of negligence that contribute to the dynamic of disease transmission. Zoonotic sporotrichosis has been described in several states in Brazil and has become endemic in the Southeastern Region of the country, especially in Rio de Janeiro, in the last 20 years.123123 da Silva MB, Costa MM, Torres CC, Galhardo MCG, do Valle ACF, Magalhães MAFM, et al. [Urban sporotrichosis: a neglected epidemic in Rio de Janeiro, Brazil]. Cad Saude Publica. 2012;28:1867-80.

Similarly, as a result of great urban mobility (such as international travel), lack of predators and emergence of resistance to pyrethroids, usually employed in residential pest control, bedbug (Cimex lectularius) bite epidemics have been described in several urban centers around the world.124124 Romero A, Potter MF, Potter DA, Haynes KF. Insecticide resistance in the bed bug: a factor in the pest's sudden resurgence?. J Med Entomol. 2007;44:175-8.,125125 Criado PR, Belda Junior W, Criado PRF, Vasconcelos e Silva R, Vasconcellos C. Bedbugs (Cimicidae infestation): the worldwide renaissance of an old partner of human kind. Braz J Infect Dis. 2011;15:74-80. Cimidiasis clinically manifests as pruritic edematous papules, especially on the extremities, which can assume a linear aspect (the bug's “breakfast, lunch and dinner”), typical of fleas and bedbugs.126126 Criado PR, Criado RF. Bedbugs (Heteroptera, Cimicidae): an etiology of pruritus to be remembered. An Bras Dermatol. 2011;86:163-4.,127127 Peres G, Yugar LBT, Haddad Junior V. Breakfast, lunch, and dinner sign: a hallmark of flea and bedbug bites. An Bras Dermatol. 2018;93:759-60. An additional concern regarding skin hypersensitivity reactions is the possibility that bedbugs can be vectors of other infectious diseases, evidence that is not yet a consensus among researchers.128128 Salazar R, Castillo-Neyra R, Tustin AW, Borrini-Mayori K, Naquira C, Levy MZ. Bed bugs (Cimex lectularius) as vectors of Trypanosoma cruzi. Am J Trop Med Hyg. 2015;92:331-5.

129 Leulmi H, Bitam I, Berenger JM, Lepidi H, Rolain JM, Almeras L, et al. Competence of Cimex lectularius Bed Bugs for the Transmission of Bartonella quintana, the Agent of Trench Fever. PLoS Negl Trop Dis. 2015;9:e0003789.
-130130 Taylor P, Morrison J. Cimex lectularis as a vector of Hepatitis B. Cent Afr J Med. 1980;26:198-200.

Pollution

One of the most damaging effects of modernity is the compromising of our environment (soil, air and water) with residues from human production. Environmental changes do not occur in isolation in the community. Deforestation, reduction of biodiversity, urbanization and pollution of the environment are usually shown to be interrelated as marks of modern human activity. Water contamination, noise pollution and waste disposal are of the utmost importance in public health.131131 Manisalidis I, Stavropoulou E, Stavropoulos A, Bezirtzoglou E. Environmental and Health Impacts of Air Pollution: A Review. Front Publ Health. 2020;8:14.

132 Dzhambov AM, Dimitrova DD. Urban green spaces' effectiveness as a psychological buffer for the negative health impact of noise pollution: a systematic review. Noise Health. 2014;16:157-65.

133 Gozzo F, Poupaert JH. Xenoestrogens, pollution & health: a critical review. J Pharm Belg. 1998;53:278-86.

134 Newell K, Kartsonaki C, Lam KBH, Kurmi OP. Cardiorespiratory health effects of particulate ambient air pollution exposure in low-income and middle-income countries: a systematic review and meta-analysis. Lancet Planet Health. 2017;1:e368-80.
-135135 Triassi M, Alfano R, Illario M, Nardone A, Caporale O, Montuori P. Environmental pollution from illegal waste disposal and health effects: a review on the "triangle of death". Int J Environ Res Public Health. 2015;12:1216-36.

From the dermatological viewpoint, the skin is affected by particulate air pollution and volatile gases, especially nitrogen dioxide (NO2), sulfur dioxide (SO2), ozone (O3), and carbon dioxide (CO2). The main mediators of air pollution in the skin are the Aryl Hydrocarbon receptors (AhR) present in all skin structures, which are activated by aromatic hydrocarbons such as dioxins, widely present in vehicular smoke.136136 Krutmann J, Liu W, Li L, Pan X, Crawford M, Sore G, et al. Pollution and skin: from epidemiological and mechanistic studies to clinical implications. J Dermatol Sci. 2014;76:163-8.,137137 Mancebo SE, Wang SQ. Recognizing the impact of ambient air pollution on skin health. J Eur Acad Dermatol Venereol. 2015;29:2326-32.

Air pollution contributes to extrinsic skin aging, and mostly derives from the burning of fossil fuels and industrial activity in urban centers. Skin that is submitted to intense air pollution has a barrier deficit, with less squalene production, in addition to oxidative consumption of tocopherol and the formation of lentigos and wrinkles.136136 Krutmann J, Liu W, Li L, Pan X, Crawford M, Sore G, et al. Pollution and skin: from epidemiological and mechanistic studies to clinical implications. J Dermatol Sci. 2014;76:163-8.,138138 Schikowski T, Huls A. Air Pollution and Skin Aging. Curr Environ Health Rep. 2020;7:58-64. In the dermis, particulate pollution can induce inflammatory phenotypes in fibroblasts, with increased metalloprotein (MMP-1, MMP-3) synthesis, reduced collagen (COL1A1, COL1A2), and elastin synthesis.139139 Park SY, Byun EJ, Lee JD, Kim S, Kim HS. Air Pollution, Autophagy, and Skin Aging: Impact of Particulate Matter (PM10) on Human Dermal Fibroblasts. Int J Mol Sci. 2018;19.

The specific damage from air pollution depends on the type of pollutant, the skin integrity and the intensity of exposure.140140 Drakaki E, Dessinioti C, Antoniou CV. Air pollution and the skin. Front Envir Sci. 2014;2. Aromatic hydrocarbons promote different epithelial stimuli; in addition to the abovementioned ones, there is the formation of epoxy and diols which bind directly to DNA, promoting epigenetic changes in cell growth, potentiating the development of neoplasms, especially if there is joint stimulation with ultraviolet radiation.141141 Fernandes AO, Banerji AP. Inhibition of benzopyrene-induced forestomach tumors by field bean protease inhibitor(s). Carcinogenesis. 1995;16:1843-6.

142 Kelfkens G, de Gruijl FR, van der Leun JC. Tumorigenesis by short-wave ultraviolet A: papillomas versus squamous cell carcinomas. Carcinogenesis. 1991;12:1377-82.
-143143 Xu F, Yan S, Wu M, Li F, Song W, Zhao J, et al. Ambient ozone pollution as a risk factor for skin disorders. Br J Dermatol. 2011;165:224-5.

In addition to aging and carcinogenesis, air pollution favors the development of inflammatory dermatoses, such as eczema and acne. Aromatic hydrocarbons, especially dioxins, are known to induce acne mediated by AhR activation, acting on sebocytes, endothelium and epidermis.143143 Xu F, Yan S, Wu M, Li F, Song W, Zhao J, et al. Ambient ozone pollution as a risk factor for skin disorders. Br J Dermatol. 2011;165:224-5.

144 Liu W, Pan X, Vierkotter A, Guo Q, Wang X, Wang Q, et al. A Time-Series Study of the Effect of Air Pollution on Outpatient Visits for Acne Vulgaris in Beijing. Skin Pharmacol Physiol. 2018;31:107-13.
-145145 Krutmann J, Moyal D, Liu W, Kandahari S, Lee GS, Nopadon N, et al. Pollution and acne: is there a link?. Clin Cosmet Investig Dermatol. 2017;10:199-204. Individuals who traveled to areas with high air pollution levels reported an inflammatory acne outbreak. In Beijing, demand for acne care has been correlated with higher indicators of air pollution.144144 Liu W, Pan X, Vierkotter A, Guo Q, Wang X, Wang Q, et al. A Time-Series Study of the Effect of Air Pollution on Outpatient Visits for Acne Vulgaris in Beijing. Skin Pharmacol Physiol. 2018;31:107-13.

The incidence of atopic dermatitis is influenced by low humidity, temperature and pollutants. Particulate pollution consists of numerous salts, heavy metals and aromatic hydrocarbons, which penetrate the skin through hair follicles and acrosyringea complex. Sweat increases the transepidermal penetration, promoting oxidative damage and inducing an inflammatory response in the dermis and epidermis, which culminates in damage to the barrier function.110110 Zhou B, Rybski D, Kropp JP. The role of city size and urban form in the surface urban heat island. Sci Rep. 2017;7:4791.,137137 Mancebo SE, Wang SQ. Recognizing the impact of ambient air pollution on skin health. J Eur Acad Dermatol Venereol. 2015;29:2326-32. In a four-year Chinese temporal series, the demand for eczema care was associated with daily air pollution indicators.146146 Li A, Fan L, Xie L, Ren Y, Li L. Associations between air pollution, climate factors and outpatient visits for eczema in West China Hospital, Chengdu, south-western China: a time series analysis. J Eur Acad Dermatol Venereol. 2018;32:486-94. Pollution is one of the factors responsible for the increased incidence of atopic dermatitis in Europe, which occurs more significantly in urban centers than in rural communities.131131 Manisalidis I, Stavropoulou E, Stavropoulos A, Bezirtzoglou E. Environmental and Health Impacts of Air Pollution: A Review. Front Publ Health. 2020;8:14.,140140 Drakaki E, Dessinioti C, Antoniou CV. Air pollution and the skin. Front Envir Sci. 2014;2.

Forest fires, whether accidental or controlled fires aiming deforestation for agriculture, promote, in addition to deforestation, a reduction in biodiversity, reduction in soil water content and launch a large amount of gases and particles into the air. This shows that changes in the environment are not only measurable due to their direct effects, but also on the entire ecosystem as well.

In addition to the ozone that pollutes the atmosphere, promoting oxidative damage to the skin with a reduction in microflora and consumption of tocopherol, ozone also naturally forms in the stratosphere, around 20 to 30 km above sea level depending on the reaction of solar ultraviolet radiation with atmospheric oxygen.147147 He QC, Tavakkol A, Wietecha K, Begum-Gafur R, Ansari SA, Polefka T. Effects of environmentally realistic levels of ozone on stratum corneum function. Int J Cosmet Sci. 2006;28:349-57. It plays a major role in completely blocking UVC radiation emitted by the sun (extremely mutagenic) and approximately 90% of UVB radiation. This equilibrium between ozone synthesis and degradation in the stratosphere ensures that a tolerable amount of mutagenic radiation reaches the planet surface.148148 Slaper H, Velders GJ, Daniel JS, de Gruijl FR, van der Leun JC. Estimates of ozone depletion and skin cancer incidence to examine the Vienna Convention achievements. Nature. 1996;384:256-8.

The ozone layer that circumscribes the Earth is not homogeneous, and has thinner areas, especially at the poles. There is an intense discussion about the cyclical variation in the configuration of the ozone layer and its degradation by air pollutants. Atmospheric emissions of halogenated compounds such as chlorofluorocarbon (CFC), halon, hydrochlorofluorocarbon (HFC), methyl bromide, carbon tetrachloride (CTC), methyl chloroform and hydrobromofluorocarbons (HBFC) have been associated with the reduction of the ozone layer in the atmosphere.148148 Slaper H, Velders GJ, Daniel JS, de Gruijl FR, van der Leun JC. Estimates of ozone depletion and skin cancer incidence to examine the Vienna Convention achievements. Nature. 1996;384:256-8. The use of these compounds in soft drinks, propellants and foams has been reduced since the 1990s worldwide, with the expectation of complete interruption of use in the next 30 years.

It is estimated that a 1% reduction in the ozone layer promotes an increase of 2% in the incidence of UVB and, consequently, an increase of 2% in the incidence of skin cancer.149149 Goldsmith LA. Skin effects of air pollution. Otolaryngol Head Neck Surg. 1996;114:217-9. In fact, in inhabited regions with lower concentrations of stratospheric ozone, higher rates of cutaneous and mucous neoplasms (basal cell carcinoma, squamous cell carcinoma and melanoma) are recorded in humans and animals, demanding greater stringency in photoprotection strategies.150150 Moan J, Dahlback A. The relationship between skin cancers, solar radiation and ozone depletion. Br J Cancer. 1992;65:916-21.

151 Lee SG, Ko NY, Son SW, Bae HJ, Ha JS, Pak HY, et al. The impact of ozone depletion on skin cancer incidence in Korea. Br J Dermatol. 2013;169:1164-5.

152 Abarca JF, Casiccia CC. Skin cancer and ultraviolet-B radiation under the Antarctic ozone hole: southern Chile, 1987-2000. Photodermatol Photoimmunol Photomed. 2002;18:294-302.

153 Madronich S, de Gruijl FR. Stratospheric ozone depletion between 1979 and 1992: implications for biologically active ultraviolet-B radiation and non-melanoma skin cancer incidence. Photochem Photobiol. 1994;59:541-6.
-154154 Diffey BL. Stratospheric ozone depletion and the risk of non-melanoma skin cancer in a British population. Phys Med Biol. 1992;37:2267-79.

Climatic changes

Climate can be defined as the set of atmospheric changes in a certain region of the planet such as temperature, precipitation and winds, with patterns that tend to be repeated in a certain period of time (e.g., it is hot and rainy in January, in the city of Rio de Janeiro). Conventionally, the climatic behavior is evaluated in 30-year periods, and the main characteristic of the climate is its natural variability according to the years, with a complex interaction between the factors that determine it. It is important to differentiate “climate” from “meteorological weather”, which considers the state of the local atmosphere at a given time (e.g., today has been the hottest day of the year in the city of São Paulo).

The variation in the temperature of the oceans (the El Niño and La Niña phenomena and the decadal oscillation of the Pacific Ocean), solar activity (solar cycles), orbital trajectory (more circular or more elliptical), Earth's axis inclination, volcanic activity and gravitational changes (lunar cycles) are the main global climate modifiers.155155 Kerr RA. Milankovitch Climate Cycles Through the Ages: Earth's orbital variations that bring on ice ages have been modulating climate for hundreds of millions of years. Science. 1987;235:973-4.

156 Hakkinen S, Rhines PB. Decline of subpolar North Atlantic circulation during the 1990s. Science. 2004;304:555-9.

157 Minnis P, Harrison EF, Stowe LL, Gibson GG, Denn FM, Doelling DR, et al. Radiative climate forcing by the mount pinatubo eruption. Science. 1993;259:1411-5.

158 Carslaw KS, Harrison RG, Kirkby J. Cosmic rays, clouds, and climate. Science. 2002;298:1732-7.

159 Tollefson J. Climate change: The case of the missing heat. Nature. 2014;505:276-8.
-160160 Mochizuki T, Ishii M, Kimoto M, Chikamato Y, Watanabe M, Nozawa T, et al. Pacific decadal oscillation hindcasts relevant to near-term climate prediction. Proc Natl Acad Sci USA. 2010;107:1833-7. Its main determinants in a given region comprise the latitude, altitude, continentality (distance from the coast), cloud density, ocean temperatures, sea currents, vegetation/urbanization (albedo), water masses and geography.111111 Gui X, Wang L, Yao R, Yu D, Li C. Investigating the urbanization process and its impact on vegetation change and urban heat island in Wuhan, China. Environ Sci Pollut Res Int. 2019;26:30808-25.,115115 Lemes MdCR, Reboita MS, Torres RR. Mudança no uso e cobertura da terra na bacia do rio tietê e seus impactos na temperatura da superfície (TS). Rev Bras Climatol. 2020;27:224-40.,161161 Carslaw K. Atmospheric physics: Cosmic rays, clouds and climate. Nature. 2009;460:332-3.,162162 Singer SF. Global climate controversy. Jama. 1996;276:373-4. This justifies the immense variability of climatic characteristics around the planet.

During the evoltion of humankind several global climate changes were recorded, such as small ice ages in Europe between 540 and 550 and between 1350 and 1850 due to less solar activity, changes in the Earth's orbit and greater volcanic activity.163163 Riley P, Lionello R, Linker JA, Owens MJ. The State of the Solar Wind, Magnetosphere, and Ionosphere During the Maunder Minimum. Proc Int Astron Union. 2018;13:247-50.

164 Eddy JA. The maunder minimum. Science. 1976;192:1189-202.
-165165 Solanki SK, Schussler M, Fligge M. Evolution of the Sun's large-scale magnetic field since the Maunder minimum. Nature. 2000;408:445-7. There have also been significant warming periods, such as the Roman Warm Period (between 250 BC to 400 C.E.), and the medieval period (between 800 and 1200 C.E.) detected in the northern hemisphere. All of these changes resulted in social, economic and health impacts on the population.

There is currently an intense discussion with geopolitical repercussions on whether the focal environmental changes promoted by human activity can influence global climate, to the detriment of the evident abovementioned loco-regional changes and the natural variability of the planet's climate cycles. However, this specific discussion goes beyond the scope of this article.

There is a clear seasonality in the incidence of dermatological diseases: psoriasis shows lower prevalence or severity in summer, due to ultraviolet radiation. However, there is a higher incidence of staphylococcal infections, actinic keratoses and accidents by venomous animals due to the type of leisure activities practiced during this time of the year. In contrast, there are more respiratory infections during the winter, when immunological imbalance favors leprosy reactions.166166 Brito LAR, Nascimento A, Marque C, Miot HA. Seasonality of the hospitalizations at a dermatologic ward (2007-2017). An Bras Dermatol. 2018;93:755-8.

167 Wang X, Towers S, Panchanathan S, Chowell G. A population based study of seasonality of skin and soft tissue infections: implications for the spread of CA-MRSA. PLoS One. 2013;8:e60872.
-168168 Andrade PR, Pinheiro RO, Sales AM, Ximena IR, de Mattos BMG, Ozório MM, et al. Type 1 reaction in leprosy: a model for a better understanding of tissue immunity under an immunopathological condition. Expert Rev Clin Immunol. 2015;11:391-407. It is therefore expected that climatic changes may interfere with the incidence of dermatoses.

Humidity and the increase in temperature constitute factors known to influence the rate of reproduction and activity of mosquitoes, the main vectors of infectious diseases.169169 Viana DV, Ignotti E. The ocurrence of dengue and weather changes in Brazil: A systematic review. Rev Bras Epidemiol. 2013;16:240-56.,170170 Kovats RS, Bouma MJ, Hajat S, Worrall E, Haines A. El Nino and health. Lancet. 2003;362:1481-9. A temporal series showed that the incidence of ATL in the Amazon region was strongly influenced by warm temperatures and changes in rainfall patterns caused by El Niño.171171 Ferreira de Souza RA, Andreoli RV, Toshie Kayano M, Lima Carvalho A. American cutaneous leishmaniasis cases in the metropolitan region of Manaus, Brazil: association with climate variables over time. Geospat Health. 2015;10:314.

In another series, in Peru, with 3,294 cases (2004-2007), the incidence of viral warts, actinic keratosis, rosacea and eczema was influenced by the climatic phenomena of the Pacific (El Niño / La Niña).172172 Gutierrez EL, Galarza C, Ramos W, Mendoza M, Smith ME, Ortega-Loayza AG. Influence of climatic factors on the medical attentions of dermatologic diseases in a hospital of Lima, Peru. An Bras Dermatol. 2010;85:461-8. These studies show that changes in regional microclimates promoted by deforestation, flooding/damming, agglomerations and urban heat islands are potential environmental determinants in the incidence of dermatoses.

In conclusion, environmental changes have an impact on human health/disease association, included in an ecological context. Currently, urbanization, large-scale agriculture, pollution of the environment and deforestation are the environmental determinants that should have the greatest impact on the incidence of dermatoses.173173 Gouveia N. Saúde e meio ambiente nas cidades: os desafios da saúde ambiental. Saude Soc. 1999;8:49-61. Dermatologists should be aware of their social responsibility in order to promote sustainable practices in their community, in addition to identifying the environmental imbalances that favor each dermatosis, which is crucial for the prevention and treatment of these diseases.

  • Financial support
    None declared.
  • How to cite this article: Haddad Junior V, Mendes AL, Talhari CC, Miot HA. Impact of environmental changes on Dermatology. An Bras Dermatol. 2021;96:210-23.
  • ☆☆
    Study conducted at the Department of Dermatology, Faculty of Medicine, Universidade Estadual Paulista, Botucatu, SP, Brazil.

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Publication Dates

  • Publication in this collection
    07 May 2021
  • Date of issue
    Mar-Apr 2021

History

  • Received
    13 Nov 2020
  • Accepted
    24 Nov 2020
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