Dermatophytes from urban soils in João Pessoa, Paraíba, Brazil

Z.B.V. Da Silva Pontes^1,*, A.C. Oliveira¹

¹ Federal University of Paraíba, Health Sciences Center, Department of Pharmaceutic Sciences, Mycology Laboratory, 58.038.910 João Pessoa, PB, Brazil,

*Correspondence. E-mail: ponteszelia@ccs.ufpb.br

ABSTRACT A total of 68 soil samples was collected from "favelas" (slums), schools, public squares, beaches and vacant lots in the city of João Pessoa-PB, Brazil. A search for dermatophytes in these soils was carried out by using the Vanbreuseghem technique. As a result, 48 strains and 6 dermatophytes species were isolated. Trichophyton terrestre (25.0%), Microsporum gypseum (20.8%) and Anthroderma gypsea (2.1%) were identified among the geophilic species, and T. mentagrophytes var. mentagrophytes (37.5%) among the zoophilic species and T. tonsurans (4.2%), among the anthropophilic species. The growth of 75% of dermatophytes occurred in alkaline pH (7.02-9.00) and their presence in the soil should not be underestimated, since some of the identified species are aetiological agents of dermatophytoses in humans and animals.

Key words: Dermatophytes; Keratinophilic fungi; Soil

RESUMEN

Dermatofitos de suelos urbanos de João Pessoa, Paraíba, Brasil. Se informan los resultados obtenidos tras la búsqueda de dermatofitos utilizando la técnica de Vanbreuseghem en un total de 68 muestras de suelo recolectadas de favelas, escuelas, plazas, playas y sitios deshabitados en la ciudad de João Pessoa, PB, Brasil. Se aislaron 48 cepas pertenecientes a 6 especies distintas de dermatofitos a partir de estos suelos. Dentro de las especies geofílicas fueron identificadas Trichophyton terrestre (25,0%), Microsporum gypseum (20,8%) y Anthroderma gypsea (2,1%); dentro de las zoofílicas, T. mentagrophytes var. mentagrophytes (37,5%) y entre las antropofílicas T. tonsurans (4,2%). El crecimiento del 75% de los dermatofitos se dio a pH alcalino (7,02-9,00). Se concluye que la presencia de estos dermatofitos en el suelo no debería ser subestimada, dado que algunas de las especies identificadas son agentes de dermatofitosis para los humanos y los animales.

Palabras clave: Dermatofitos; Hongos queratinofílicos; Suelo

Dermatophytes ( Epidermophyton, Microsporum and Trichophyton) are keratinophilic fungi, which according to their natural habitat, are divided into anthropophilic, zoophilic and geophilic species. Some species are cosmopolitan while others present restricted geographical distribution ^{(2, 13, 15)}. Vanbreuseghem ⁽¹⁴⁾ considered the soil as a reservoir of dermatophytes, where he obtained the first isolation of Microsporum gypseum and Keratinomyces ajelloi. The occurrence of fungi in the soil is influenced by biological and non-biological factors, such as soil pH, temperature, humidity, pluviometric level, environmental light, climate, chemical composition and amount of organic material in the soil ^{(4, 7, 8)}. The aim of this study was to investigate the presence of dermatophytes and the influence of pH in the soil of João Pessoa
The soil samples were collected in the urban area (schools, public squares, "favelas" (slums), beaches and vacant lots) of João Pessoa city and the search for dermatophytes was carried out by using the "hair-bait technique" of Vanbreuseghem ⁽¹⁴⁾. Approximately 100 g of soil at a depth of 3 to 5 centimetres were collected, placed in polyethylene bags and brought to be processed at the Laboratory of Mycology in the Department of Pharmaceutic Sciences at the Federal University of Paraíba.
The pH of each soil sample (20 g) was measured using a pH meter, after dilution in sterile distilled water (20 ml) with 20 minutes of agitation and decantation. Each sample was distributed in sterile Petri plates, moistened with sterile water (20 ml) and some sterile human hair strips were placed over each surface. The plates were identified and incubated (27-30 °C) and from the 5^th to the 70^th day, the hair strips were regularly observed with magnifying glasses for signs of fungal growth. Hair strips with development of prominent fungal growth around them, were placed between slide and coverslide, coloured in lactophenol blue cotton and examined under a microscope (10X and 40X). They were cultivated in Sabouraud dextrose agar medium with chloramphenicol (0.05 mg/ml) and in Mycobiotic agar® and incubated at room temperature for another minimum period of 2 weeks.
The identification of the species was based on macromorphology and micromorphology (slide-culturing), urea hidrolysis, hair perforation and pigmentation in agar. The classification was based on Rebell and Taplin ⁽¹⁰⁾.
The results of the isolations are presented in Table 1.

Table 1. Dermatophytes isolated from soils from João Pessoa city

The data revealed that 55.7% of 68 soil samples presented fungal growth. The isolation of dermatophytes was observed in the soils of slums, schools, public squares, beaches and vacant lots. A total of 48 dermatophyte strains were isolated and 6 species were identified. Both the geophilic and zoophilic species corresponded to 48% of the identification. Among the geophilic species, Trichophyton terrestre (25.0%), followed by M. gypseum (20.8%) and Arthroderma gypsea (2.1%) (teleomorph - M. gypseum) were identified whereas Trichophyton mentagrophytes var. mentagrophytes (37.5%) and Trichophyton verrucosum (10.4%) were the identified zoophilic species and Trichophyton tonsurans (4.2%) was the only anthropophilic species isolated in the studied soil samples. In five samples, the growth of more than one species of dermatophytes was observed.
The pH analysis from the soil samples showed that dermatophytes developed in a large pH margin: both acid and alkaline (4.50-9.06), and 75% of these isolations were in alkaline pH (7.02-9.00) (Table 2). Geophilic dermatophytes have their habitat reservoir in the soil, the degraded keratin or organic substances which are constantly thrown into the soil. Some species are pathogenic to both humans and animals ^{(5, 9)}. In this study, 6 dermatophyte species, among them, geophilic (48.0%), zoophilic (48.0%) and anthropophilic species (4.0%), were identified in the soil of João Pessoa city.

Table 2. Distribution of dermatophytes in different soil pH

The geophilic species T. terrestre (25.0%) was isolated from the soils of slums, public squares and schools. This positive index is probably related to the collection places where the presence of people and animals is usual, as well as to residues of organic material which favor fungal growth. Other geophilic species isolated in this study were M. gypseum (20.8%) and A. gypsea (2.1%). In the soil of Manaus city, the isolation percentage of M. gypseum was 19.0% ⁽¹⁵⁾ whereas in the soil of other Brazilian cities, it accounted for 31.0% in the State of Rio de Janeiro ⁽²⁾, 30.0% in São Paulo ⁽¹²⁾ and 26.8% in Belo Horizonte ⁽¹²⁾. Nevertheless, the highest indexes found were in the soils of Goiás (53.3%) ⁽⁶⁾, and Rio Grande do Sul (39.4%) ⁽¹⁾. In the soil of other countries such as Argentina (89.0%), India (64.0%) and Iran (11.7%) the isolation of this fungal species could be achieved ^{(7, 9, 13)}. Although M. gypseum has universal distribution when compared to other dermatophytes isolated from human injuries, the percentages referred to in the literature are very low ⁽⁵⁾. In this study, 80% of the isolation of
The zoophilic species have animals and sometimes human beings as favourite hosts. T. mentagrophytes is the species with most incidence in Brazil as an important agent of dermatophytoses ⁽⁵⁾. Its isolation was informed in the states of Amazonas, Belo Horizonte, São Paulo and Goiás ^{(6, 12, 15)} in the Brazilian soil, as well as in several other parts of the world such as Argentina, Italy, Nigeria, India, Nepal and Iran. These soil samples were from different places such as gardens, parks, beaches, caves, poultry yards, corrals and residences ^{(7-10, 13)}. In this study, T. mentagrophytes var. mentagrophytes (37.5 %) was the most frequent zoophilic species isolated from all soil samples followed by the isolation of T. verrucosum.
The anthropophilic species are perfectly adaptable to human skin and particularly to keratinized tissue (cornea layer, hair and nails), being responsible for most cases of dermatophytoses ^{(5, 6)}. Thus, Goulart ⁽²⁾ referred to the presence of T. tonsurans in the soils of Rio de Janeiro and João Pessoa. The isolation percentage of this anthropophilic species accounted for 3.8%. One of the five soil samples from the beaches presented the zoophilic species T. mentagrophytes var. mentagrophytes.
The influence of pH on the development of keratinophilic fungi in the soil is widely discussed. Thus, the results of this study point to an influence of the alkaline pH (7.02-9.00) on the development of 75.0% of dermatophytes. Kaul and Sumbali ⁽⁴⁾, Mangiaterra and Alonso ⁽⁷⁾ and Mercantini et al ⁽⁸⁾ also recorded that the keratinophilic fungi develop much better in alkaline pH. However, in other studies the growth of keratinophilic fungi in ⁽⁹⁾.
The presence of dermatophytes in the soil of João Pessoa should not be underestimated since most of the identified species are aetiological agents of dermatophytoses both in humans and animals.

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Recibido: 16/04/2007
Aceptado: 14/05/08