Dermatophytes from urban soils in João Pessoa, Paraíba, Brazil
Z.B.V. Da Silva Pontes1,*, 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 5th to the 70th 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.
1. Fischman O, Ramos CD. Geophilic dermatophytes recovered from Rio Grande do Sul soil. Mycopathol Micol Appl 1967; 33: 157-61.
2. Goulart EG, Lima SMF, Carvalho MA, Oliveira JA, Jesus MM, Campos RE et al. Isolamento de fungos patogênicos do solo do município do Rio de Janeiro - RJ, Brasil. F Méd 1986; 93: 15-20.
3. Gugnani HC, Paliwal-Joshi A, Rahman H, Padhye AA, Singh TSK, Das TK et al. Occurrence of pathogenic fungi in soil of burrows of rats and of other sites in bamboo plantations in India and Nepal. Mycoses 2007; 50: 507-11.
4. Kaul S, Sumbali G. Impact of some ecological factors on the occurrence of poultry soil-inhabiting keratinophiles. Mycopathol 1999; 143: 155-9.
5. Lima EO, Pontes ZBVS, Oliveira NMC, Carvalho MFFP, Guerra MFL, Santos JP. Freqüência de dermatofitoses em João Pessoa - Paraíba - Brasil. An Bras Dermatol 1999; 74: 127-32.
6. Machado OP. Ocorrência de dermatófitos em solo no município de Goiânia - Goiás. Rev Pat Trop 1977; 6: 53-67.
7. Mangiaterra ML, Alonso JM. Keratinophilic fungi in soils of Corrientes city (Argentina). Bol Micol 1989; 4: 129-33.
8. Mercanti R, Marsella R, Caprilli F, Dovgiallo G. Isolation of dermatophytes and correlated species from the soil of public gardens and parks in Rome. Sabouradia 1980; 18: 123-8.
9. Ogbonna CIC, Pugh GJF. Keratinophilic fungi from Nigerian soil. Mycopathol 1987; 99: 115-8.
10. Periasamy AHA, Subash CBG. Keratinophilic fungi of poultry farm and feather dumpling soil in Tamil Nadu, India. Mycopathol 2004; 158: 303-9.
11. Rebell G, Taplin D. Dermatophytes, their recognition and identification. 2nd Ed. Coral Gables, Florida, University of Miami Press, 1970; p. 124.
12. Rogers AL, Beneke EJ. Human pathogenic fungi recovered from Brazilian soil. Mycopathol Micol Appl 1964; 22: 15-20.
13. Shadzi S, Chadeganipour M, Alimoradi M. Isolation of keratinophilic fungi from elementary schools and public parks in Isfahan, Iran. Mycoses 2002; 45: 496-9.
14. Vanbreuseghem R. Technique biologique pour l'isolement des dermatophytes de sol. Ann Soc Belge Méd Trop 1952; 32: 173-8.
15. Vilela EM, Moraes MAP. Isolamento de Microsporum gypseum e Trichophyton mentagrophytes no solo da cidade de Manaus, Amazonas (Brasil). Rev Inst Med Trop São Paulo 1962; 4: 299-301.
Recibido: 16/04/2007
Aceptado: 14/05/08