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Prevalência de fungos anemófilos no Brasil e a correlação com doenças respiratórias e infecções fúngicas
Prevalence of airborne fungi in Brazil and correlations with respiratory diseases and fungal infections

Marcelo Batista Suehara. Universidade Federal da Integração Latino-Americana - Unidade PTI: Foz do Iguacu, Paraná, BR. E-mail: marcelosuehara@gmail.com; ORCID: https://orcid.org/0000-0002-9631-3372
Mayara Cristina Pinto da Silva. Universidade Federal do Maranhão, São Luís, Maranhão,BR. E-mail:mayara.silva@ufma.br; ORCID: https://orcid.org/0000-0002-1868-6931

RESUMO
Fungos anemófilos se dispersam na natureza através do ar atmosférico. O presente estudo objetivou caracterizar a prevalência da microbiota fúngica anemófila no Brasil e correlacionar o crescimento fúngico com doenças respiratórias e quadros infecciosos. Este trabalho é uma revisão integrativa de literatura construída a partir da busca nas bases de dados PUBMED, BIREME, SCIELO e LILACS, com inclusão de trabalhos brasileiros publicados entre 2000 e 2022, em língua portuguesa ou inglesa com texto online integral. O universo do estudo foi constituído por 147 publicações, das quais 25 compuseram a amostra por atenderem aos critérios de inclusão. Os gêneros de fungos aerotransportados mais prevalentes no Brasil são: Aspergillus sp., Penicillium sp., Cladosporium sp., Curvularia sp. e Fusarium sp. Os locais de origem dos estudos incluem Maranhão, Ceará, Piauí, Sergipe, Mato Grosso, Pernambuco, Rio Grande do Sul, Santa Catarina, Rio de Janeiro, São Paulo, Minas Gerais. Além disso, foi possível determinar a relação dos fungos com parâmetros meteorológicos e sazonalidade, a sensibilização de indivíduos atópicos aos fungos e as principais micoses nosocomiais relatadas na literatura. Assim, o trabalho destaca a importância da manutenção da qualidade microbiológica do ar com vistas a se prevenir possíveis doenças transmitidas pelo ar.
Palavras-chave: Fungo. Microbiologia do ar. Brasil.

ABSTRACT
Airborne fungi are dispersed through the air. The aim of this study was to determine the prevalence of airborne fungi in Brazil and understand the relationship between fungal growth and respiratory diseases and infections. We conducted an integrative literature review of studies conducted in Brazil based on searches of the PubMed, MEDLINE-BIREME, SciELO, and LILACS databases for full-text articles published between 2000 and 2022. The searches returned 147 studies, of which only 25 met the inclusion criteria. The most prevalent genera of airborne fungi in Brazil are Aspergillus, Penicillium, Cladosporium, Curvularia, and Fusarium. The studies were conducted in the states of Maranhão, Ceará, Piauí, Sergipe, Mato Grosso, Pernambuco, Rio Grande do Sul, Santa Catarina, Rio de Janeiro, São Paulo, and Minas Gerais. The findings also show the relationship between fungi and meteorological factors and seasonality, the sensitivity of atopic individuals to fungi, and the main nosocomial mycoses reported in the literature. This work demonstrates the importance of maintaining good microbiological air quality to prevent potential airborne diseases.
Keywords: Fungi. Air microbiology. Brazil.

INTRODUCTION
Fungi are ubiquitous heterotrophic eukaryotic microorganisms. They are widespread in the air, soil, oceans, deserts, glaciers, plants, humans, animals, and even insects. They have a chitin cell wall and cell organizations range from unicellular to highly complex filaments (1,2). Fungi are highly diverse, playing an important role in natural cycles, and fungal metabolites have great biotechnological potential, being exploited to acquire bioproducts such as antibiotics, vitamins, and enzymes used in clinical research (3).
Airborne or anemophilous fungi are classified into different genera and species and have spores that remain dry and hydrophobic due to cysteine-rich proteins on their surface (4). Air dispersal requires the presence of propagules, whose dispersal is influenced by temperature, air humidity, volumetric precipitation, atmospheric pressure, and wind speed, as well as vegetation and pollution (5,6).
Widespread airborne fungal microbiota are associated with adverse health effects (7). The inhalation of fungal spores can cause allergic respiratory diseases such as asthma, rhinitis, and sinusitis (8). The prevalence of fungi-induced allergic respiratory diseases was estimated to be between 20 and 30% among atopic patients and 6% in the general population (9). Alternaria sp., Penicillium sp., Aspergillus sp., and Cladosporium sp. are among the genera most commonly associated with hypersensitivity (10).
The diversity of airborne fungal spores varies depending on location (indoor or outdoor), geographic region, and season (10). Fungal growth is favored by high temperatures and relative humidity, with these conditions triggering greater sporulation and, consequently, a rise in allergic respiratory symptoms (6,11).
In general, levels of fungal microbiota in the air in indoor environments is a reflection of the diversity of fungi in the outdoor environment and airborne species are the most frequently observed contaminants in climatized environments (12). Poor air quality in enclosed spaces can lead to short- and long-term infections and increase the risk of occupational diseases. Even non-pathogenic fungi pose a risk of causing mycotoxicosis and ear and nail infections (13). Once introduced into enclosed spaces, spores find suitable substrates to colonize and multiply, presenting a potential occupational biological hazard (8,14).
Fungal contamination in hospital environments poses a risk of hospital infection (15). More well-known complications caused by fungal infections include invasive pulmonary aspergillosis, allergic fungal sinusitis, otomycosis, and mycotoxin-induced severe toxic reactions, which can lead to death in immunocompromised patients (9).
The World Health Organization (WHO) highlights the rising global health threat of invasive fungal diseases, emphasizing diagnosis and treatment challenges and reinforcing concerns with their resistance to currently available antifungal agents (16). The coronavirus disease (COVID-19) pandemic raised the alert over the incidence of fungal infection comorbidities, with aspergillosis, mucormycosis, and candidemia gaining prominence in the literature (17).
According to National Health Surveillance Agency (ANVISA) Resolution 9 (January 2003), microbiological contamination is a reference parameter for air quality in indoor climatized environments. The resolution sets a contamination limit of 750 CFU/m3 (where CFU is colony forming units) and an indoor/outdoor (I/O) fungi quantity ratio of ≤ 1.5 (18).
The aim of this study was to determine the prevalence of airborne fungi in the country, demonstrate the relationship between fungal allergens and respiratory allergies, and understand the relationship between airborne fungi with pathogenic potential and the occurrence of infection.
This work is justified by the need to update knowledge and data on the prevalence of airborne fungal microbiota in Brazil. Integrative reviews of the prevalence of airborne fungi and the human health impacts of these microorganisms have yet to be undertaken in Brazil. The data generated by this study constitute a source of information on air quality, microbial contamination, and airborne disease prevention.

METHODS
We conducted an integrative review of the literature involving the following stages: formulation of the guiding question; definition of criteria for article selection; database search; data collection, analysis, and interpretation; and discussion of results. The guiding question was as follows: “What are the main airborne fungi found in Brazil and their correlation with respiratory diseases and fungal infections?”.
Searches were performed of the following databases between February 2021 and December 2022: PubMed; Medical Literature Analysis and Retrieval System Online (MEDLINE), accessed using the Regional Library of Medicine (BIREME) interface; Scientific Electronic Library Online (SciELO); and Latin American and the Caribbean Literature on Health Sciences (LILACS). The review involved the following stages.
First, we performed database searches for studies relating to the topic that met the inclusion and exclusion criteria. The Health Sciences Descriptors (DeCs) “fungos”, “anemófilos”, and “Brasil” were used together with the corresponding Medical Subject Headings (MeSH) in English, “fungi”, “airborne”, and “Brazil”. The inclusion criteria were full-text Brazilian articles available online written in English or Portuguese published in national and international journals between 2000 and 2022. Articles that did not address the guiding question, were unrelated to the study topic, and duplicate papers were excluded.
The second stage consisted of data collection and exportation of references to Rayyan QCRI, a reference selection platform that helps remove duplicates and facilitates the title and abstract screening process. The aim of this stage was to identify articles for full-text screening. Exploratory reading was performed, consisting of rapid reading of the selected articles to ascertain whether the studies met the study requirements. Selective reading was then performed, consisting of a more in-depth analysis of the selected articles.
The third stage consisted of the analysis and interpretation of the study results. The articles were catalogued in a table using the following categories: article title, objectives, and main results. The aim of this stage was to organize the content of the articles to obtain responses to the guiding question.
The fourth stage was the discussion of the results, in which the content of the selected studies is analyzed and discussed drawing on the frame of reference.
RESULTS
The searches returned 147 studies, 122 of which were excluded because they were duplicates, were not related to the study topic, or did not meet the eligibility criteria, resulting in a final review sample of 25 studies (Figure 1).
For the search of LILACS, a combination of the keywords “fungi”, “anemófilos” and “Brasil” were used together with the Boolean operator “AND”. For the MEDLINE-BIREME search, the term “microbiologia do ar” (air microbiology) was used. The searches yielded 15 and 30 articles, respectively.
For the searches of PubMed and SciELO, the terms “fungi”, “airborne”, and “Brazil” were used together with the Boolean operator “AND”, resulting in 86 and 16 articles, respectively.
The studies were categorized in a table containing the following headings: article title, objectives, and main results (Table 1).
Of the 25 articles reviewed by this study, six were conducted in the South, seven in the Southeast, one in the North, nine in the Northeast, and two in the Midwest (Figure 2). The studies show that Brazil has a high diversity of airborne fungal microbiota and that the diversity of composition varies according to region. The following genera had a high incidence across regions: Aspergillus sp., Penicillium sp., Cladosporium sp., Fusarium sp., Curvularia sp., and Alternaria sp.
While the findings show that the hot climate of the tropics is conducive to the occurrence of airborne fungi, the role relative humidity plays in the dispersal process and fungal growth is not clear. The results suggest that humidity facilitates the concentration of fungi, but excess humidity can have a negative effect on the transport of fungal spores. In contrast, sunlight and wind increase the atmospheric dispersal of spores.
The works compiled in this review make an important contribution to existing knowledge of fungal allergies. Exposure to fungal spores increases the risk of asthma or rhinitis attacks in atopic patients. The studies assessed by this review identified a diverse range of species of fungal aeroallergens associated with respiratory diseases. Besides allergic reactions, the literature has documented fungal infections caused by airborne fungi. Fungi with pathogenic potential from the genera Aspergillus sp., Penicillium sp., and Cladosporium sp. were found in controlled hospital environments. Hospital-acquired infections caused by fungi have a high impact on patient morbidity and mortality, meaning that effective aerobiological monitoring of these settings is essential to prevent infection.
DISCUSSION
The discussion of the selected articles is divided into three categories: a) prevalence of airborne fungi in Brazil; b) Airborne fungi and implications for allergic reactions; and c) Airborne fungi and implications for fungal infections.

Prevalence of airborne fungi in Brazil

Airborne fungi are abundant ubiquitous organisms and have the capacity to produce spores or fungal propagules (19). Spores are ubiquitous and essential structures for fungal dispersal and colonization. Their concentration, aerodynamic diameter, and taxonomic compositions vary considerably and are greatly influenced by environmental factors such as temperature, relative humidity, and season (14,20).
According to the findings of the studies, tropical climates are conducive to fungal growth, with the climate in countries like Brazil resulting in the release of large numbers of spores and generating high concentrations of fungi in the atmosphere (14,21). With suitable levels of oxygen, temperature, and humidity, airborne fungi produce metabolites that favor their development in available substrates (12). Current knowledge of the transport of bioaerosols shows that meteorological factors influence the spread of fungal spores, with higher temperatures, sunlight, and wind enhancing airborne dispersal (22). A positive correlation was found between humidity and fungi quantities, in contrast to older studies pointing to higher spore counts in dry and hot seasons (21,23).
There is no consensus in the literature regarding seasonality and spore dispersal. A study in Porto Alegre reported higher spore counts in the summer than in the autumn, while research in Fortaleza demonstrated that the concentration of spores was higher in slightly lower temperatures in January and June (20,21). A study evaluating the air quality of ICUs in the South found a pronounced variation in fungi counts between seasons, with the autumn months showing the highest prevalence rates (23). There are stark differences in climate between the South and Northeast of Brazil, making it difficult to establish a pattern of fungal growth. In 2021, Bernardi and do Nascimento corroborated the results of a study in Manaus showing that certain genera are more common in specific seasons, with Cladosporium sp. having higher incidence in the rainy season and Aspergillus sp., Curvularia sp. and Penicillium sp. being more prevalent in the dry season (24,25).
Some genera of airborne fungi, such as Alternaria sp., Aspergillus sp., and Cladosporium sp., occur worldwide (20). The distribution of fungi differs according to season and the type of environment (indoor or outdoor) (21). This compilation of studies of airborne fungi shows that the same high-incidence genera of fungi were found outdoors in different cities at different times of the year (14,26).
A pioneering study of the prevalence of airborne fungi in Porto Alegre published in 2001 showed that the most prevalent genera were Cladosporium sp., Aspergillus sp., Penicillium sp., Curvularia sp., Alternaria sp., Fusarium sp., and others (21). Similar results were found in 2021 in Pelotas, where the following genera were identified: Cladosporium sp. (18.22%), Alternaria sp. (13.84%), Penicillium sp. (10.20%), Curvularia sp. (7.47%), and Aspergillus sp. (3.28%) (24). In a similar study in Fortaleza in 2004, the most prevalent genera were Aspergillus sp., Penicillium sp., Curvularia sp., Cladosporium sp., Mycelia sterilia, Fusarium, Rhizopus, Neurospora sp., Rhodotorula sp., and Aureobasidium sp., while in Recife and Natal, cities with identical climates, Aspergillus sp. and Penicillium sp. were the most frequent (20). In São Luís, the most prevalent genera in outdoor environments were Aspergillus sp., Penicillium sp., Cladosporium sp., Curvularia sp., and Fusarium sp. (14). The results of these studies are consistent with the findings of a similar study undertaken in the Metropolitan Area of Sao Paulo, which reported that Penicillium sp. and Aspergillus sp. were the most prevalent species in both indoor and outdoor environments (27).
The findings reveal the constant presence of spores from the genera Aspergillus sp., Penicillium sp., Cladosporium sp., Curvularia sp., and Fusarium sp. across Brazil over the ten-year study period.
This review also included studies that demonstrated the prevalence of airborne fungi in indoor environments. A study in the state of Pernambuco evaluating the microbiological quality of environments in a university identified the following genera: Aspergillus sp., Penicillium sp., Talaromyces sp., Curvularia sp., and Paecilomyces sp. The frequency of Aspergillus sp. and Penicillium sp. was 50% and 21%, respectively (12). In a study investigating the diversity of airborne fungi in a library in the state of Mato Grosso, Júnior et al. found that Aspergillus sp. was one of the most prevalent fungi, being identified in 89.6% of the samples. Penicillium sp. was identified in 10.4% of the samples (19). Another study that monitored the microbiota of the air in a library in São José do Rio Preto in 2020 identified Aspergillus sp., Cladosporium sp., Penicillium sp., Scopulariopsis sp., and Trichoderma sp. (28). Similarly, a study in Rio de Janeiro evaluating the impact of the demolition of a hospital wing on the concentration of fungi found that the most frequent genus was Cladosporium sp. (mean of 45.09 CFU/m3 of air), followed by Penicillium sp. (mean of 14.35 CFU/m3) and Aspergillus sp. (mean of 9.22 CFU/m3) (29).
Airborne fungi can be used as bioindicators for environmental monitoring (30). A study conducted in 2020 investigating correlations between airborne fungi and air pollutants found that a reduction in the circulation of vehicles due to a truck driver strike had an influence on fungal growth. During the strike, there was an 80% increase in the number of atmospheric fungi, representing a significant difference (p < 0.05) when compared to previous periods before the strike (31).

Airborne fungi and implications for allergic reactions

Fungal spores are aeroallergens that can be inhaled and are associated with various respiratory diseases, including allergic rhinitis and allergic asthma (20). Groups of fungi that release airborne spores include zygomycetes, ascomycetes, basidiomycetes, and deuteromycetes. It is in the latter group that the allergens Aspergillus sp., Penicillium sp., Cladosporium sp., and Alternaria sp. are found (26).
Human beings are constantly exposed to bioaerosols and fungal spores during their personal and professional lives, constituting a potential occupational biological hazard (14). High concentrations of spores in the air can lead to hypersensitivity of the respiratory tract and increase symptoms that are typical of the sick building syndrome, such as pneumonia, allergic rhinitis and sinusitis, lack of concentration, and fatigue (23,32).
Skin tests and measures of specific IgE antibody levels for airborne fungi were used in a study in Porto Alegre, which demonstrated that 15.38% of atopic individuals with asthma and/or rhinitis had sensitivity to airborne fungi (26). A study in São Luís with 100 children reported increased concentrations of IgE in 96.9% of patients with allergic asthma and/or rhinitis. Seventy-five per cent of the children tested positive for Aspergillus, 87% for Penicillium, 46% for Neurospora, and 45% for Fusarium (33). A similar study in São Luís analyzing IgE antibody levels against airborne fungi in atopic adults found that 79.7% tested positive for Penicillium, 77.8% for Neurospora, and 44.9% for Aspergillus (34).
In a study in Fortaleza that performed skin tests on individuals with respiratory allergies using fungal extracts, all patients had positive reactions to extracts of Aspergillus, Alternaria, and Drechslera and 70% had positive reactions to extracts of Penicillium and Curvularia. None of the patients from the control group had positive skin test reactions (35).
The characterization of airborne fungal microbiota helps guide epidemiological research and the diagnosis and treatment of allergic reactions (12). The allergies addressed by the studies demonstrate the capacity of airborne fungi to cause reactions in individuals who are predisposed to producing IgE response to environmental allergens.

Airborne fungi and implications for fungal infections

It is known that airborne fungi are important biological air contaminants; however,
according to ANVISA, the presence of pathogenic or toxigenic species in the air is unacceptable when assessing the air quality of indoor environments (18). Fungal infections caused by airborne microorganisms, especially hospital-acquired infections, have received much attention in the medical literature in recent years. The patients most affected by opportunistic mycoses are immunocompromised patients, such as cancer, transplant, AIDS, and polytraumatized patients and neonates (36,37). Nosocomial infections are particularly associated with fungi from the following genera: Aspergillus sp., Cladosporium sp., Paecilomyces sp., Penicillium sp., and Scopulariopsis sp., and, to a lesser extent, Candida sp., Rhodotorula sp., Cryptococcus sp., and Trichosporon sp. (22).
A quantitative evaluation of fungi in the air of three ICUs in Porto Alegre showed a marked predominance of the genera Cladosporium sp. in indoor environments and Penicillium sp. in outdoor environments, followed by species from the genus Aspergillus sp. (predominantly A. fumigatus, A. niger, and A. flavus) (23). These results are similar to those of a study conducted in an ICU in Pelotas, which found that the most prevalent genera were Penicillium, Aspergillus, and Cladosporium (15).
Similar results were found in a study in an ICU in Mato Grosso, which reported that the most frequent genera were Aspergillus sp., Penicillium sp., and Cladosporium sp. (38). A study in the surgical center and adult and neonatal ICUs in a hospital in Araraquara found that the most prevalent genera were Cladophialophora sp., Fusarium sp., Penicillium sp., Chrysosporium sp., and Aspergillus sp. (39).
In contrast, a study of ICUs and wards in two hospitals in Fortaleza isolated four genera of yeast not found in studies in the south of the country: Candida sp., Rhodotorula sp., Trichosporon sp., and Saccharomyces sp. (22). A study in Sergipe isolated four genera of fungi in the surgical center, four in the intensive care center, four in the IUC, and five in the burn unit. The following genera were found: Aspergillus sp. (43%), Penicillum sp. (12%), Fusarium sp. (11%), Candida sp. (6%), and Curvularia sp. (5%) (40). Finally, a study evaluating air conditioners in public and private ICUs in the state of Piauí, in the northeast region, found that the predominant genus was Aspergillus sp. The most prevalent species was A. niger, followed by A. fumigatus, Trichoderma koningii, A. flavus, and A. tamarii (32).
The results of this review demonstrate a high diversity of fungal microbiota in the air of hospital environments in Brazil, with the predominance of the genera Aspergillus sp., Penicillium sp., Cladosporium sp., Fusarium sp., and Candida sp.. Aspergillus sp. makes an evident contribution to the composition of this microbiota and implications include occupational health problems and infection.
The toxicity of species from the genera Aspergillus sp., resulting from their capacity to produce aflatoxin that can cause poisoning, is widely documented in the literature (36).
Aspergillosis is a type of mycosis caused by the inhalation of spores from the genus Aspergillus sp., which can develop into allergic bronchopulmonary aspergillosis and other invasive and systemic conditions. The etiologic agents most involved in these conditions are A. fumigatus, A. flavus, and A.niger (19,32). Invasive aspergillosis is common in patients with neutropenia and chronic obstructive pulmonary disease and has been increasingly identified in non-neutropenic patients admitted to ICUs (23). A. flavus is associated with pulmonary infections in immunocompromised patients, A. fumigatus is the main agent involved in aspergillosis, and A. niger is frequent in otomycosis (32).
The genus Cladosporium sp. is also common in hospital environments. This fungus influences seasonal allergies and is associated with central nervous system infections such as the formation of brain abscesses (41).
Another genus commonly found in hospital environments is Penicillium sp.. Though widely known for its role in the development of antimicrobials, this genus includes fungal air pollutants that can cause penicilliosis when inhaled by immunosuppressed individuals. This disease initially affects the lungs and develops into a systemic disorder (12,19,23). Penicillium sp. is also associated with disseminated infections, such as multiple brain abscesses, peritonitis, and pneumonia in immunocompromised patients (15).
Airborne fungal infections in hospital environments can involve different transmission mechanisms, including the inhalation of fungal spores transported and distributed by contaminated ventilation or air condition systems and contact with surgical wounds, surgical instruments, or the clothing and hands of medical staff (22,37). This review focused on airborne fungi and therefore the most documented mode of transmission is certainly inhalation.
The literature underlines that air conditioning systems are key sources of dissemination of fungal spores, highlighting the importance of installing high efficiency particulate air filtration systems in health services as a way to improve indoor air quality (38,39).
This study shows the importance of determining the prevalence of fungi in the environment and understanding the different mechanisms through which airborne fungi cause complications, health problems, and even death. Health professionals need to be aware of the various forms of fungal contamination in order to improve health care delivery. It is important to promote the adoption of preventive measures such as the use of personal protective equipment, raising awareness of fungal infections, and investment in adequate ventilation systems, including regular cleaning of air conditioners and the use of filters.

CONCLUSION
The study of airborne fungi in Brazil is a diverse field and has gained increasing prominence recently. The large concentration of airborne spores in both internal and external environments and potential contamination with airborne microorganisms highlights the importance of this study. The most prevalent genera of airborne fungi in Brazil are Aspergillus sp., Penicillium sp., Cladosporium sp., Curvularia sp. and Fusarium sp. High concentrations of spores in the air can lead to hypersensitivity and symptoms that are typical of the sick building syndrome, such as allergic rhinitis and sinusitis, lack of concentration, and fatigue. Allergic reactions mainly affect atopic individuals. Airborne fungi can be both pathogenic and toxigenic, causing invasive fungal diseases with disastrous consequences for immunosuppressed patients.
Study limitations include only including articles written in Portuguese and English and limiting the focus to Brazil. Unfortunately, there are few studies addressing airborne fungal microbiota in Brazil and therefore the sample of articles selected for this review was not very robust.
Given the importance of the study topic, further research should be conducted in this area in Brazil. This review seeks to contribute to discussions on the development of public health policies addressing microbiological air quality.
FUNDING
This study received financial support from the Coordination for the Improvement of Higher Education Personnel (CAPES, funding code 001), the National Council for Scientific and Technological Development (CNPq), the State of Maranhão Research Foundation (FAPEMA, BIC-01741/20), and Maranhão Federal University (PIBIC/CNPq/FAPEMA/UFMA 2020-2021).
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