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Soil of Recreational Areas As a Reservoir of Keratinolytic Mould Fungi and Dermatophytes Potentially Pathogenic for Humans

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Soil of Recreational Areas As a Reservoir of Keratinolytic Mould Fungi and Dermatophytes Potentially Pathogenic for Humans Pol. J. Environ. Stud. Vol. 24, No. 3 (2015), 993-1002 DOI: 10.15244/pjoes/32506 Original Research Soil of Recreational Areas as a Reservoir of Keratinolytic Mould Fungi and Dermatophytes Potentially Pathogenic for Humans Katarzyna Góralska1*, Piotr Kurnatowski1, Joanna Błaszkowska2, Anna Wójcik1 1Department of Biology and Medical Parasitology, Medical University of Lodz, Haller Sqr. 1, 90-647 Lodz, Poland 2Department of Diagnostics and Treatment of Mycoses and Parasitic Diseases, Medical University of Lodz, Poland Received: 26 March 2014 Accepted: 2 November 2014 Abstract The aim of our study was to determine the prevalence of keratinophilic and keratinolytic fungi in the soil of recreational areas in Lodz, with a particular emphasis on species potentially pathogenic for humans. The material consisted of 104 soil samples collected from the surface layer and 10-15 cm below the sur- face at 26 recreational areas in Lodz. Soil samples were inoculated on Sabouraud, Czapek-Dox, and PDA media. In order to isolate the common dermatophytes from the collected soil, hair bait tests were prepared. From the collected soil samples, 83 species of fungi belonging to 53 genera were isolated. The most numerous were those of the genera Penicillium, Fusarium, and Cladosporium. Dermatophytes were isolated from 79 out of 104 of soil samples from 24 examined sites. They were classified into eight species from five genera. The most numerous was the genus Trichophyton. The presence of dermatophytes and mould fungi with keratinolytic properties in the soil of recreational areas may pose a significant risk to human health, especially for children and young teenagers. The results obtained in this study and an analysis of the literature suggests the need for monitoring the soil of places of active leisure for potentially pathogenic fungi species. Keywords: keratinophylic fungi, dermatophytes, soil, recreational areas Introduction and plant organisms. Especially in the case of plants, decay processes can be started by participating fungi that produce Fungi are one of the most common organisms on earth. enzymes that degrade the cellulose contained in the plant Most species are cosmopolitan organisms found in any cli- cell walls. A few bacteria also possess cellulase, yet decom- mate, and are present in every ecosystem. In the structure of position of plant debris depends on the presence of fungi the biocenosis they usually represent a group of decom- [1]. posers responsible for the re-inclusion of chemical ele- Some species of saprotrophic fungi found in the soil are ments in the cycle of matter. Most of the processes of parasitic for other organisms. Many fungi of the genus destruction of dead organic matter is carried out in the soil. Fusarium often invade corn and wheat, the genus of The surface layer of the soil is humus, rich in organic com- Alternaria is seen on the leaves and fruits of tomato plants, pounds and minerals. Reducers, the bacteria and fungi, are and Penicillium invade fruit. In addition to the destruction responsible for the natural decomposition of dead animal of tissue, these fungi can produce several mycotoxins which are not destroyed at high temperatures and can be *e-mail: [email protected] accumulated in the bodies of the animals consuming them, 994 Góralska K., et al. leading to toxicosis. Zearalenone, produced by the genus ational areas in Lodz, with a particular emphasis on species Fusarium, causes the so-called estrogenic syndrome, and potentially pathogenic for humans. aflatoxins produced by fungi of the genus Aspergillus and ochratoxin A produced by Penicillium and Aspergillus have carcinogenic properties. Fumonisins — genus Fusarium, Materials and Methods and penitrem — genus Penicillium, demonstrate neurotox- ic effects, and trichothecenes produced by Fusarium have The material consisted of 104 soil samples collected haemorrhagic, dermatotoxic, and cytotoxic activity [2]. from the surface layer and 10-15 cm below the surface at 26 Fungi occurring in the soil may also be responsible for recreational areas in Łódź in the districts of Polesie, Bałuty, superficial and systemic infection. Because of their ability Śródmieście, Widzew, and Górna: 2 beaches located in the to cause lesions, fungi are classified into three levels of areas of recreational facilities, unfenced and public; 2 resi- biosafety (BSL) to humans. BSL 1 includes saprotrophes dential playgrounds, public, with a low fence; 13 school and plant pathogens, which can cause mild superficial fields, including one partially enclosed and one unfenced; 8 infections on rare occasions. Group BSL 2 are pathogens public playgrounds located in parks, including two responsible for superficial and deep opportunistic infec- unfenced; and one lane park, adjacent to a fenced play- tions in patients with disorders of the immune system. The ground. At the same time, sand from sandpits located in last class, BSL 3, are fungi capable of inducing severe sys- parks, playgrounds, residential areas, and schools in Lodz temic infections in healthy individuals [3]. was analyzed [10]. Infections associated with fungi present in the soil often Soil samples were collected in two research seasons: concern people who come into contact with the soil, mainly spring and autumn. Soil samples weighing 0.5 g were dilut- farmers, gardeners, and people who dig. Dermatomycosis ed in 10 ml of sterile distilled water, shaken, and then 0.5 can affect up to 55% of farmers [4]. The most common etio- ml was inoculated on Sabouraud medium and incubated at logical agents of fungal infections associated with the soil are 23ºC for 7 to 14 days. Colonies of mould fungi were pas- keratinophilic fungi that can break down epidermis, hair, and saged on Czapek-Dox and PDA (potato-glucose agar) nails [5], and this group includes such common dermato- media to obtain axenic strains of morphology typical for the phytes as Trichophyton, Microsporum, Epidermophyton, and species. From the obtained colonies, microscope prepara- Keratinomyces genera that, under natural conditions, can tions in lactophenol were prepared according to Gerlach survive for several months or years in the lithosphere. [11]. In order to isolate the common dermatophytes from These genera are responsible for the majority of fungal the collected soil, hair bait tests were prepared using sterile infections of glabrous skin, scalp, feet, hands, and nails [6]. hair from children, and these were evaluated after 4-8 Similar capabilities are also shown by some mould fungi, weeks of incubation at 23ºC. Positive cultures were pas- although they more often penetrate the human body saged onto Mycoline medium. Fungi were identified to through small mechanical damage to the skin. species or genus on the basis of macro- and microscopic Hialohyphomycosis caused by species belonging to characteristics using the DeHoog et al. [12] and Fassatiova Fusarium, Acremonium, and Penicillium pose a significant [13] keys. Taxonomy was determined on the basis of a list danger, especially for people with severely weakened of species according to Index Fungorum. The biosafety immune systems [7-9]. assessment of the fungi was based on the International The appearance of developmental forms of fungi in the Classification of BSL [3]. soil is associated with the presence of animals. Bird drop- Statistical analysis of the data was performed using pings can contain cells and spores of Cryptococcus and Student's t test with a significance level of p<0.05 with Histoplasma, while epidermal products such as fur, claws, STATISTICA 10 software. and feathers found in the soil can act as substrates for species with keratinolytic properties. Cycling and skate- boarding, jogging, and other recreational activities can Results result in falls and abrasions soiled with sand, through which fungi can easily penetrate into the body. Minor and major From the collected soil samples, 83 species of fungi injuries can also occur on the playing fields and children's were isolated belonging to 53 genera. The most numerous playgrounds, and in many cases children ignore the injury were those of the genera Penicillium, Fusarium, and and don't disinfect the wound. Recreational areas such as Cladosporium (Table 1). fields and parks contain not only the remains of pet dogs Most frequently isolated was Fusarium oxysporum and cats, but also the feces, hair, and feathers of wild mice, (8.06%), occurring also in the largest number of localities, hedgehogs, squirrels and birds, and, in areas on the outskirts followed by Cladosporium herbarum (6.05%) and of cities, also the footsteps of foxes and wild boar. This Penicillium chrysogenum (5.54%). Haematonectria availability of organic material (keratinized animal tissues haematococca = Fusarium solani constituted 4.53% of the and various plant tissues) favors the occurrence of patho- total number of identified species, Sarocladium kiliense genic fungi in recreational areas, which may pose a threat syn. Acremonium kiliense 4.28%, Alternaria alternata to the health and vitality of people. 4.03%, Paecilomyces variotii and Sarocladium strictum The aim of our study was to determine the prevalence syn. Acremonium strictum 3.78%, while Purpureocillium of keratinophilic and keratinolytic fungi in the soil of recre- lilacinum syn. Paecilomyces liliacinus constituted 3.53% Soil of Recreational Areas... 995 Table 1. Taxonomic spectrum of isolated fungi according to Index Fungorum. Total Autum Spring Number of No. Species BSL Number % Number % Number % posts 1 Acremonium alabamense 2 0.50 2 0.80 0 0 2 1 2 Alternaria alternata 16 4.03 9 3.61 7 4.73 11 1 3 Alternaria chlamydospora 2 0.50 1 0.40 1 0.68 2 1 4 Alternaria tennuissima 1 0.25 0 0 1 0.68 1 1 Aphanoascus keratinophilus = 5 2 0.50 2 0.80 0 0 1 2 Chrysosporium keratinophilum 6 Apophysomyces elegans 2 0.50 2 0.80 0 0 1 2 7 Arthrinium phaeospermum 5 1.26 3 1.20 2 1.35 3 1 8 Arthrographis kalrae 2 0.50 1 0.40 1 0.68 2 2 9 Aspergillus flavus 6 1.51 6 2.41 0 0 4 2 10 Aspergillus fumigatus 1 0.25 0 0 1 0.68 1 2 11 Aspergillus niger 2 0.50 1 0.40 1 0.68 2 1 12 Aureobasidium pullulans 3 0.76 3 1.20 0 0 3 1 13 Bipolaris sp.
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