Ecology of Dermatophytes and Other Keratinophilic Fungi in Swimming Pools and Polluted and Unpolluted Streams

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Ecology of dermatophytes and other keratinophilic fungi in swimming pools and polluted and unpolluted streams

Article in Mycopathologia · February 2002 DOI: 10.1023/A:1023311411004 · Source: PubMed

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Ecology of dermatophytes and other keratinophilic fungi in swimming pools and polluted and unpolluted streams

M.S. Ali-Shtayeh1, Tayseer Kh. M. Khaleel1 & Rana M. Jamous2 1Department of Biological Sciences, An-Najah University, Nablus; 2Biodiversity and Environmental Research Center, Til, Nablus, Palestinian Authority, via Israel

Received 16 May 2001; accepted in ﬁnal form 21 October 2001

Abstract The biodiversity and richness of keratinophilic fungal communities including dermatophytes were assessed in three stream sites and three swimming pools in the Nablus district in Palestine, using hair baiting (HBT) and surface dilution plate (SDP) techniques, over 8- and 6-month periods, respectively. The effect of wastewater effluent and selected ecological factors on these fungi in relation to species diversity and population densities were also considered. Fifty keratinophilic fungal species were recovered from the aquatic habitats studied, of which 42 were recovered from stream sites and 22 from swimming pools. Of these fungi 6 were either dermatophytes (Microsporum gypseum,andTrichophyton mentagrophytes) or dermatophyte related species (Chrysosporium merdarium, Ch. tropicum, Ch. keratinophilum and T. terrestre). The most frequently isolated species in the three pools were Acremonium strictum and Cladosporium cladosporioides, using Sabouraud dextrose agar medium (SDA). The most abundant species were Acr. strictum,andAspergillus flavus. However, only 4 species were isolated using the SDA medium amended with 5-flurocytosine (5-FC). The most frequent and abundant species in the three stream sites using SDA medium were Geotricum candidum,andPenicillium chrysogenum.Themost frequent species in the three sites using the 5-FC medium, was Paecilomyces lilacinus. Using HBT, the most abundant and frequent species in the three stream sites were G. candidum,andPa. lilacinus, on SDA medium, and Pa. lilacinus,andGliocladium nigrovirens on the 5-FC medium. The 5-FC medium was more suitable for the isolation of dermatophytes and closely related species than the SDA medium; 6 were recovered on 5-FC, whereas only one on the SDA medium. Variation in the levels of keratinophilic fungal populations from the three stream sites sampled 5 times over an 8-month period, followed comparable fluctuation patterns. Wastewater affected fungal population densities with the highest levels in the un-polluted stream sites, and lowest in the heavily polluted sites. Swimming pools, polluted and un-polluted stream sites were found to be rich in pathogenic and potentially pathogenic fungi.

Key words: dermatophytes, keratinophilic fungi, polluted streams, stream water, swimming pools, tinea pedis

Introduction in the levels of water contamination with sewage and natural environmental factors [5]. The occurrence and distribution of dermatophytes The distribution and occurrence of dermatophytes and other keratinophilic fungi in swimming pools have and keratinophilic fungi in aquatic habitats including been the subject of a number of investigations [7– wastewater have been studied by various investigators 14]. Dermatophytes commonly isolated from swim- [1–6]. Communities of keratinophilic fungi vary both ming pools include Trichophyton mentagrophytes, T. quantitatively and qualitatively in different aquatic rubrum and Epidermophyton floccosum.Thesethree habitats. This has been mainly attributed to variations species are known to be the most common etiological agents of tinea pedis over the entire world. Beside * Published in 2003. these three species, other pathogenic dermatophytes 194 have been isolated from swimming pools, e.g., Mi- with the Al-Bathan stream at a point 200 m down crosporum gypseum, M. canis and T. verrucosum [8, stream. Pollution with wastewater is highest at the 12, 13]. Dermatophytes show seasonal fluctuations meeting point, and decreases down stream through in their occurrence with more dermatophytes being natural, biological, and physical processes. isolated during the summer and spring months [13]. Three sites, along the Al-Bathan stream, located Keratinophilic fungi commonly isolated from swim- about 7 km north east of Nablus city, were selected as ming pools include species of Alternaria, Aspergillus, representative aquatic habitats with different wastewa- Cladosporium, Fusarium, Geotrichum, Penicillum, ter pollution levels. The first site was located 100 and Phoma [9, 12]. m before the wastewater-stream water mixing point, The occurrence and distribution patterns of derma- the second was 100 m down stream from the mix- tophytes and keratinophilic fungi in aquatic habitats ing point, and the third about 1000 m down stream depend on many ecological, physical and chemical from the second site. The first site (A) was adjacent factors particularly pH, dissolved oxygen concentra- to a water source (dissolved oxygen, DO2 = 7.4–9.4 tions, temperature, heavy metals, and organic matter mg/L, electrical conductivity, EC = 420–550 µMHOS, especially keratinaceous substances [15, 16]. Water Temp = 19–22 ◦C), and did not receive any wastewater pollution was found to reduce the diversity of sens- discharge, therefore, it was not expected to be pol- itive fungal species (e.g., Alternaria species), while luted. The second site (B) was expected to be the site increasing the number of those less sensitive e.g., with the highest pollution level being adjacent to the (Chrysosporium species) [6, 17, 18]. wastewater-stream water mixing point (DO2 =7.2– Polluted water habitats can be sources of envir- 7.4 mg/L, EC = 500–750 µMHOS, Temp = 18–24 ◦C), onmental contamination and disease. People exposed followed by the third site (C), which was expected to to such contaminated environments are likely to con- be moderately polluted being 1100 m down stream tract fungal infection [4]. Some keratinophilic spe- from site B (DO2 = 6.8–7.1 mg/L, EC = 600–800 cies such as T. mentagrophytes, M. persicolor and µMHOS, Temp = 19–24 ◦C). Water samples were col- M. canis isolated from polluted habitats can cause lected every other month (5 times) over eight months superfacial mycoses. Others such as Aphanoascus ful- during the period between March and October 1998. vescens, M. gypseum, Trichosporon beigelli, T. ajelloi, Three swimming pools located in the Nablus area Scopulariopsis brevicaulis,andGeotrichum candidum (TMSS children’s pool, DO2 = 7.0–8.8 mg/L, pH 7.0– cause opportunistic mycoses [4]. Swimming pools 7.2, EC = 600–1200 µMHOS, Temp = 20.5–29 ◦C; have also been established to be sources of tinea pedis TMK adult’s pool, DO2 = 7.2–8.4 mg/L, pH 7.2-8.4, [11, 13, 14]. People walking bare-footed on contam- EC = 1000-1700 µMHOS, Temp = 22–28 ◦C; and WB inated places with dermatophytes, which come from adults’ pool, DO2 = 7.2–8.6 mg/L, pH 7.3–7.6, EC = shed infected skin scales, may acquire infections. 420–700 µMHOS, Temp = 17–22 ◦C), were chosen The present study was therefore aimed at providing for the present study. Water samples were collected data on the ecology of dermatophytes and other kerat- every other month (3–4 times) in the period between inophilic fungi in swimming pools and polluted and March and August 1998. non-polluted streams. Their role in the epidemiology On each sampling occasion two water samples, of dermatophytoses and other mycotic infections were about 4 L each, were collected from each site from investigated as well as the effect of wastewater effluent the surface using sterile 2-L plastic bottles. Some on these fungi in relation to species diversity, popula- ecological factors were determined at the time of col- tion densities; and the effect of ecological factors on lection. These included dissolved oxygen (DO2)using population densities and biodiversity of these fungi. a dissolved oxygen meter (YSI Model 518), pH, and salinity, temperature and electrical conductivity (EC) using an EC meter (YSI Model 33 S-C-T meter). Materials and methods Isolation of dermatophytes and other keratinophilic Sampling sites and collection of samples fungi

Wastewater (domestic and industrial) produced in the I. Surface dilution plating (SDP) eastern part of Nablus is currently discharged in Wadi Preparation of inocula. About 1.5 L of each water Al-Sajour, which extends north eastward and meets sample were separately filtered through 0.45 µ mil- 195 lipore filters using a filtration unit. The filters were 5-fluorocytosine.The plates were incubated at 25 ◦C, then removed from the filtration unit and the su- and moistened when necessary. After two weeks of pernatants were either re-suspended in 15 ml sterile incubation, 16 hairs from each subsample were trans- distilled water (SDW) amended with, per liter, 500 mg ferred to the surface of agar plates (4 hairs/plate), and cycloheximide, 50 mg chloramphenicol, and 100 mg the process was repeated a second time for another 2 gentamicine sulfate or in 15 ml SDW amended with weeks. The inoculated plates were incubated at 25 ◦C the above antibiotics plus 5-flurocytosine (50 mg/L). for 5–7 days and the grown colonies were sub-cultured A series of dilutions (100 : 1, 20 : 1, 10 : 1) were then on SDA medium plates and identified as in the SDP prepared as follows: the suspensions were divided into method. three equal parts (5 ml each), 20 ml of SDW amended The following indicator of fungal occurrence and with antibiotics were added to the first part (20 : 1), 45 abundance was used: relative importance value (RIV). ml SDW were added to the second part (10 : 1), while The RIV for each species was calculated as follows: the third part was left without further dilution (100 : 1). frequency of occurrence of a species = A-value, Mean Agar medium preparation. Sabouraud dextrose sample frequency = B-value, Relative mean frequency agar medium (Oxoid) (SDA) amended with, per liter, = C-value. A-value = number of sites in which the 500 mg cycloheximide, and 50-mg chloramphenicol, species was found/number of sites examined. B-value and gentamicine sulfate (100 mg/L), or SDA sup- = (number of isolates of the species/total number of plemented with the above mentioned antibiotics and hairs transferred from all samples) ×100. C-value = 5-flurocytosine (50 mg/L) (5-FC medium) [13]. B-value of the species/sum of B-values of all species Inoculation of agar plates. About 0.5 ml of the pre- recovered. RIV = (A-value + C-value) × 100. pared suspensions were pippetted onto the surface of the agar plates. The inoculum was spread over the surface of the plates using a sterile bent glass rod, and the Results plate was rotated gently by hand. Ten plates of either the SDA or 5-FC media were used for each dilution. Biodiversity of dermatophytes and other Determination of the inoculum density and identi- keratinophilic fungal species in swimming pools fication of fungi. The inoculated plates were incubated ◦ at 25 C for one week. The growing colonies were then Results on the biodiversity, distribution, and frequency marked on the back of the plates. The plates were in- of the mycobiota (dermatophytes and other keratino- cubated for an additional ten days to allow the growth philic fungi) of swimming pools are presented in of slow growing fungi. The grown colonies were ini- Tables 1–3. tially divided into groups on the basis of their gross Twenty-two keratinophilic fungi were isolated morphology (i.e., growth rate, color and texture). Rep- from three swimming pools using HBT and SDP resentative colonies were sub-cultured on SDA agar (Table 1). Fourteen keratinophilic fungal species, be- plates and identified using standard procedures and longing to nine genera, were isolated from the three taxonomic keys [19–21]. The mean number of colon- swimming pools over a 6-month period using either ies was determined as the number of colonies per liter HBT or SDP with SDA and 5-FC media (Table 1). of water sample. Seven species were isolated by both techniques. Of all of the species recovered, one was a dermatophyte- II. Hair baiting technique (HBT) related keratinophilic species (Chrysosporium kerat- Six 500-m1 aliquots of water were filtered separately inophilum). using the filtration unit through 0.45 µ Millipore filter Thirteen species were isolated from the three pools paper. The filter paper was then removed from the fil- using the SDP with SDA media, whereas four species tration unit, placed in a sterile Petri dish with about 10 were isolated using the 5-FC medium. Three (21.4%) ml of sterile sand, and l cm long pieces of autoclaved of these species (Acremonium strictum, Aspergillus human hair were sprinkled over the filter paper. Three flavus,andPenicillium chrysogenum) were common of the plates were moistened with SDW supplemented to both media. The most frequently isolated species with, 500 mg cycloheximide 50mg chloramphenicol, (% +ve samples) in the three pools were Acr. strictum and 100 mg gentamicine sulfate, per liter. The other (80) and Cladosporium cladosporioides (80), using three plates were moistened with SDW supplemented the SDA medium. The most abundant (CFU L−1)spe- with the above mentioned antibiotics plus 50 mg/L cies were Acr. strictum (95.5), A. flavus (17.9) and C. 196

Table 1. Keratinophilic fungi isolated from three swimming pools and three stream sites using surface-soil-dilution and hair baiting techniques Isolated species Swimming pools Stream sites SDP HBT SDP HBT Dermatophytes and related fungi Chrysosporium merdarium –– +– + Chrysosporium tropicum39b –– ++ + Chrysosporium keratinophilum40a –+ –– + Microsporum gypseum72a,41b –– +– + Trichophyton mentagrophytes47b,22a –– +– + Trichophyton terrestre43a –– +– Other fungi + Absidia corymbifera57a –– +– + Acremonium cerealis21d –+ ++ + Acremonium kiliense69a +– –– Acremonium rutilum –– +– + Acremonium strictum51a ++ –+ + Alternaria alternata66d,47a,b ++ ++ + Aspergillus ﬂavus64a ++ +– Aspergillus sp. + – –– + Beauveria bassiana63b,74a,75c ++ ++ Chrysosporium sp. – – +– + Cladosporium cladosporioides70a +– +– + Cladosporium herbarum67b –+ –+ + Exophiala dermatitids58d –– +– + Fusarium heterosporum71c –– –+ + Fusarium lateritium71c –– ++ + Fusarium moniliforme33a,65b,66d,71c –– –+ Fusarium tricinctum –– ++ − + Fusarium oxysporum71c,d,52 54a –+ –– + Geotrichum candidum62d,46a,45a ++ ++ Gliocladium catenulatum –– ++ Gliocladium nigrovirens –– ++ Gliocladium viride –– +– Monascus ruber –– +– + Mucor hiemalis56a –– +– Necteria ventricosa –– –+ Paecilomyces carneus +– –– + Paecilomyces farinosus75c –+ –– + Paecilomyces lilacinus48a,49a,50a,75c ++ ++ Paecilomyces marquandii –– ++ + Paecilomyces variotii77a,76b –– –+ Penicillium brevicompactum –– –+ + Penicillium chrysogenum55a,59a ++ ++ + Penicillium citrinum68a +– –– + Penicillium frequentans60a –– –+ + Penicillium oxalicum78d –+ –– + Scopulariopsis brevicaulis73a –– +– Trichoderma viride –– ++ + Verticillium albo-atrum66d –– –+ Verticillium chlamydosporium –– –+ Verticillium fungicola –– +– + Vetricillium lecanii75c +– ++ + Verticillium nubilum61d –– –+ Verticillium sp. + – –+ Unidentiﬁed hyphomycetes sp. – + –+ + Pathogenic or potentially pathogenic fungi to ahumans; banimals; cinsects; and dplants. 197

− Table 2. Mean population densities CFU L 1 and frequency of occurrence (% +ve samples) of keratinophilic fungi in three swimming ∗ ∗ pools sampled 3–4 times over a 6-month period with SDA medium and 2 times over a 3-month period with 5-FC medium

Isolated species Swimming pools WB adults’ pool TMSS children’s pool TMK adults’ pool Mean (%) SDA 5-FC SDA 5-FC SDA 5-FC SDA 5-FC

+ Acremonium kiliense 0 0 5.8 (34) 0 0 0 1.9 (10) 0 + Acremonium strictum 3.8 (50) 0 256 (100) 7.3 (100) 28 (66) 0 95.9 (80) 2.4 (17) + Alternaria alternata 0 0 0 7.7 (50) 0 0 0 2.6 (17) + Aspergillus ﬂavus 0 0 26 (34) 11.9 (50) 27.8 (34) 24.4 (50) 17.9 (20) 12.1 (34) Aspergillus sp. 0 0 1.3 (34) 0 0 0 0.34 (10) 0 + Beauveria bassiana 0.8 (50) 0 0 0 0 0 0.27 (20) 0 + Cladosporium cladosporioides 4.6 (75) 0 16 (100) 0 17.7 (66) 0 12.8 (80) 0 + Geotrichum candidum 3.2 (25) 0 0 0 0 0 1.1 (10) 0 Paecilomyces carneus 0.8 (25) 0 0 0 0 0 0.3 (10) 0 + Paecilomyces lilacinus 0 0 0 0 1.7 (66) 0 0.6 (20) 0 + Penicillium chrysogenum 1.8 (25) 0 13.1 (34) 60 (50) 18.7 (100) 20.6 (50) 11.2 (50) 26.9 (34) + Penicillilum citrinum 0 0 14.6 (34) 0 14 (34) 0 9.5 (20) 0 + Verticillium lecanii 0 0 0 0 6.9 (34) 0 2.3 (10) 0 Verticillium sp. 0 0 0 0 2.3 (34) 0 0.8 (10) 0

Mean population densities 15 0 332.8 83.3 117.1 45 155.3 42.8

Total No. of species 6 0 7 4 8 2 13 4

∗ SDA, Sabouraud dextrose agar amended; 5-FC, SDA amended with 5-flurocytosine; + Pathogenic and potentially pathogenic fungi. cladosporioides (12.8). Species frequency and popu- Biodiversity and seasonal fluctuation in population lation levels evaluated on the 5-FC or SDA media are levels of dermatophytes and other keratinophilic showninTable2. fungal species in stream sites Using HBT with SDA or the 5-FC media, fifteen species of keratinophilic fungi, belonging to nine gen- The results of the ecologic studies of dermatophytes era, were isolated from the three pools (Table 3). All and other keratinophilic fungi in polluted and non- species, except C. herbarum, were recovered on SDA polluted stream sites are presented in Tables 1, 4, and medium plates, whereas only seven of the species were 5. recovered on 5-FC medium plates. The three pools Forty-two keratinophilic fungal species were isol- differed in community composition and number of ated from the three stream sites (A, B, C) sampled over species (Table 3). Dermatophyte related fungi were an 8-month period using the HB and SDP techniques represented by only one species: Ch. keratinophilum. (Table 1). Twenty-nine and twenty-seven species were The most frequent and abundant species (as shown isolated using SDP and HBT, respectively. Fourteen by their relative importance values, RIV’s) on SDA species (33.3%) were common to both techniques. medium plates (Table 3) were Acr. strictum (74.7) and Five of the species recovered (11.9%) were either Alt. alternata (69.4) in the three pools, Geotrichum dermatophytes: M. gypseum,andT. mentagrophyes candidum (94.3) and Ch. keratinophilum (37.3) in WB or dermatophyte related keratinophilic species: Ch. adults’ pool, and Acr. strictum (88.2-124), and Alt. merdarium, Ch. tropicum and T. terrestre. alternata (82.9-96.8) in TMK adults’ and TMSS chil- Twenty-nine keratinophilic fungal species, belong- dren’s pools. Comparable results were obtained on the ing to nineteen genera, were isolated from the three 5-FC medium plates (Table 3). sites using SDP with the SDA and 5-FC media (Table 4). Nine species were isolated using SDA, whereas twenty-five species were isolated using the 5-FC medium. Five (17.8%) species were common to both media. Dermatophytes and related species were represented by five species: M. gypseum, T. mentagro- 198 ended RIV mportance values of 245 –– – –– – –– – –– – –– – –– – 0 50.9 64.9 0 0 66.7 0 159.6 63.1 0 137 138.1 0 52.5 66.7 70.5 0 0 19 200 168 –– – –– – 129.5 0 0 WB TMSS TMK HBT with 5-FC Positive samples 1 16.7 18.1 –– – –– – –– – –– – –– – 2 33.3 40.3 –– – –– – –– – 1 16.7 23.9 4 66.7 102.7 Total %1 RIV 16.7 20.2 3 50 86.7 2 33.3 41.8 Isolates 51.3 7 –– –– –– 28 7.2 27 7 –– –– –– –– –– 14 3.6 33 8.5 387 100 138 35.7 Total % 142 36.7 s and their percentage of all samples; relative i RIV hnique (HBT) with either Sabouraud dextrose agar medium (SDA) or SDA am Children’s pool; TMK, Adults’ pool. 95 6 0 48.4 38.9 0 44.9 0 00 35.5 0 0 44.9 0 88.2 142 –– – 58.8 0 0 30.3 0 0 30.3 0 0 35.7 0 0 30.2 0 0 94.3 0 0 25.6 67.6 45.9 37.5 0 0 169 284 269 WB TMSS TMK 32.1 82.9 96.8 HBT with SDA Positive samples ––– 2 20 21.1 Total % RIV 2 20 27.3 1 10 11.3 1 10 11.3 1 10 14.3 1 10 12.5 11 10 10.8 10 14.3 5 50 69.4 1 10 11.3 1 10 20.3 5 50 74.7 3 30 47.4 1 10 12.9 lated colonies and % pools, number of positive sample – Isolates thogenic fungi; WB, Adults’ pool; TMSS, 91.3 91.3 60.8 91.3 ∗ 14 15 2.1 53 7.3 31 4.3 18 2.6 31 4.3 75 10.3 21 2.9 722 100 Total % 140 19.4 178 24.6 – 126 17.4 Keratinophilic fungi isolated from swimming pools using, the hair baiting tec Aspergillus flavus Other fungi Geotrichum candidum Penicillium chrysogenum Alternaria alternata Fusarium lateritium Unidentified spp. Paecilomyces lilacinus Cladosporium herbarum Paecilomyces carneus Fusarium oxysporum Acremonium strictum Penicillium oxalicum Paecilomyces farinosus Isolated species Dermatophyte-related fungus Chrysosporium keratinophilum Total isolates Total spp. Acremonium cerealis + + + + + + + + + + + + Absent; +, Pathogenic or potentially pa species from all pools RIV, RIV at each pool) Table 3. ∗ with 5-flurocytosine (5-FC) (total number of iso 199

− Table 4. Mean population densities CFU L 1, and frequency of occurrence % +ve samples of dermatophytes and other keratinophilic fungi from three stream sites sampled 5 times over an 8-month period with Sabouraud dextrose agar medium (SDA) and 3 times over a 5-month period ∗ with 5-FC medium

Isolated species Population densities (%) Site a (nonpolluted) Site b (polluted) Site c (polluted) Mean (%) SDA 5-FC SDA 5-FC SDA 5-FC SDA 5-FC

Dermatophytes and related fungi Chrysosporium merdarium 0 0.4(34)0000 00.1(11) + Chrysosporium tropicum 0 0 00 01.7(34)00.6(11) + Microsporum gypseum 0 0.2(34)0000 00.07(11) + Trichophyton mentagrophytes 0 2.7(66)0000 00.9(22) + Trichophyton terrestre 0 0 00 01.1(34)00.4(11) Other fungi + Absidia corymbifera 0 1.8(34)0000 00.6(11) + Acremonium cerealis 0 2.9(34)0000 01(11) Acremonium rutilum 0 0 00 01.1(34)00.4(11) + Alternaria alternata 4 (40) 0 0.4 (20) 0 0.8 (20) 0 1.7(27) 0 + Aspergillus ﬂavus 0 0 03.3(34)0001.1(11) + Beauveria bassiana 0 2.1(66)0000 00.7(22) Chrysosporium species0 2.9(34)0000 01(11) + Cladosporium cladosporioides 2.6 (20) 0 0 0 0.7 (20) 0.23 (34) 1.1(13) 0.08 (11) + Exophilia dermatitidis 0 0.2(34)0000 00.07(11) + Fusarium lateritium 0 0 00 00.43(34)00.2(11) + Fusarium tricinctum 0 2.3 (34) 0 0 0 0 0 0.8 (11) + Geotrichum candidum 170.8 (100) 0 42.7 (100) 0 68.3 (100) 0 93.9 (100) 0 Gliocladium catenulatum 0 0 0 0 0.23 (20) 0 0.08 (7) 0 Gliocladium nigrovirens 0 12.4 (66) 0 0 1.3 (20) 0 0.4 (7) 3.1 (22) Gliocladium viride 0 0 00 00.23(34)00.08(11) Monascus ruber 0 0 0 0 0 12.2 (34) 0 4.1 (11) + Mucor hiemalis 0 0 0.2 (20) 0 1.5 (20) 0 0.6 (13) 0 + Paecilomyces lilacinus 0 7.8 (66) 0 2.2 (66) 1.3 (20) 7.8 (66) 0.4 (7) 5.9 (66) Paecilomyces marquandii 0.4 (20) 7.3 (34) 0 0 0.3 (20) 0 0.2 (13) 2.4 (11) + Penicillium chrysogenum 1.6 (40) 0 2.4 (20) 0 27.6 (60) 21.7 (34) 10.5 (40) 7.2 (11) + Scopulariopsis brevicualis 0 0 00 01.1(34)00.4(11) Trichoderma viride 0 0.7 (34) 0 0 0 1.1 (34) 0 1 (22) Verticillium fungicola 0 0.2(34)0000 00.07(11) + Verticillium lecanii 0 0.2(34)0000 00.07(11)

Mean population densities 179.5 44.1 45.7 5.5 102.03 48.7 109.1 32.8

Total No. of spp. 5 15 4 2 9 11 9 25

∗ 5-FC, SDA amended with 5-ﬂurocytosine; + Pathogenic or potentially pathogenic fungi. phytes, T. terrestre, Ch. merdarium and Ch. tropicum. (22), Trichoderma viride (22) and T. mentagrophytes The most frequent (% +ve samples) and abundant (22). The most abundant species were P. chrysogenum (CFU L−1) species in the three stream sites using (7.2), Pa. lilacinus (5.9) and Monascus ruber (4.1). the SDA medium, were G. candidum (100 %, 93.9 The frequency and population levels (CFU L−1)eval- CFU L−1), P. chrysogenum (40, 10.5) and Alt. altern- uated on the 5-FC or SDA media are shown in Table ata (27, 1.7). The most frequent species in the three 4. sites using the 5-FC medium, were Pa. lilacinus (66 Variation in the levels of keratinophilic fungal %), Beauveria bassiana (22), Gliocladium nigrovirens populations (CFU L−1) from the three stream sites 200

Table 5. Keratinophilic fungi isolated from water of streams using the hair baiting technique (HBT) with either Sabouraud dextrose agar medium(SDA) or SDA amended with 5-ﬂurocytosine (5-FC) (total number of isolated colonies and % in streams, number of positive samples and their percentage of all samples, and relative importance values of the species, RIV, RIV at each stream site

HBT with SDA HBT with 5-FC Isolates Positive samples RIV Isolates Positive samples RIV Isolated species Total % Total % RIV A B C Total % Total % RIV A B C

Dermatophytes and related fungi + Chrysosporium tropicum –∗ – – – – – – – 8 1.4 2 22 23.4 0 35.4 35.7 Other fungi + Acremonium cerealis 6 0.8 1 7 7.8 21.8 0 0 – – – – – – – – + Acremonium strictum 3 0.4 1 7 7.4 0 0 21.3 – – – – – – – – + Alternaria alternata 1 0.1 1 7 7.1 20.3 0 0 – – – – – – – – + Beaouveria bassiana – – – – – – – – 3 0.6 1 11 11.5 0 35.4 0 + Cladosporium herbarum 3 0.4 1 7 7.4 0 20.2 0 – – – – – – – – + Fusarium heterosporum 3 0.4 1 7 7.4 20.9 0 0 38 6.7 2 22 28.6 0 43.7 44.4 + Fusarium lateritium 12 1.6 1 7 8.6 0 0 0 4 0.7 1 11 11.7 0 0 35.3 + Fusarium moniliforme 13 1.8 2 13 14.7 44 0 0 – – – – – – – – + Fusarium tricinctum 6 0.8 1 7 7.8 0 0 22.7 18 3.2 2 22 25.2 36.1 0 39.1 + Geotrichum candidum 491 66.9 15 100 167 164 173 166.9 – – – – – – – – Gliocladium catenulatum 6 0.8 2 13 13.8 0 22.5 20.4 – – – – – – – – Gliocladium nigrovirens 38 6.7 2 22 28.8 45.2 0 39.5 Necteria ventricosa 2 0.3 1 7 7.3 20.5 0 0 – – – – – – – – + Paecilomyces lilacinus 95 12.9 7 47 60 51.3 117 51.3 417 74.2 9 100 174 179 167.4 173 + Paecilomyces variotii 1 0.1 1 7 7.1 0 0 20.4 8 1.4 1 11 12.4 36.4 0 0 Paecilomyces marquandii 52 7.1 3 20 27 31 20.3 24.6 – – – – – – – – Penicillium brevicompactum 4 0.5 1 7 7.5 0 20.2 0 – – – – – – – – + Penicillium chrysogenum 1 0.1 1 7 7.1 20.3 0 0 – – – – – – – – + Penicillium frequentans 2 0.3 1 7 7.3 20.5 0 0 – – – – – – – – Trichoderma viride – – – – – – – – 1 0.2 1 11 11.2 33.8 0 0 + Verticillium albo-atrum – – – – – – – – 13 2.3 1 11 13.3 0 42.3 0 + Verticilium nubilum 15 2 2 13 15 20.6 0 25.9 – – – – – – – – + Verticillium lecanii 1 0.1 1 7 7.1 20.3 0 0 – – – – – – – – Verticillium chlamydosporium 7 1 2 13 14 35.5 0 29.2 10 1.8 1 11 12.8 0 40 0 Verticillium sp – – – – – – – – 4 0.7 1 11 11.7 35.2 0 0 Unidentiﬁed hyphomycetes spp 9 1.3 1 7 8.2 22.8 0 0 0 0 0 0 0 0 Total isolates 733 100 327 188 218 562 100 211 141 210 Total spp. 21 14 6 10 12 6 6 6

∗ Absent; +, Pathogenic or potentially pathogenic fungi; A, unpolluted stream site; B & C, waste-water polluted site. sampled 5 times over an 8-month period of time, fol- quandii (27). The most abundant and frequent species lowed comparable ﬂuctuation patterns (Table 6). The in the three sites using the 5-FC medium were Pa. highest population levels in the unpolluted sites were lilacinus (174), Gl. nigrovirens (28.8) and Fusarium detected in May and August, whereas the highest pop- heterosporum (28.6). The three stream sites differed ulation levels in the more polluted site (site B) were in community structure and number of species (Table detected in March and October, and in the lightly 5). Dermatophyte-related species were represented by polluted site C in May and October. Ch. tropicum (Table 5). Using the HBT with the SDA and 5-FC media, 27 keratinophilic fungal species belonging to fourteen Effect of ecological factors on water population levels genera were isolated from the three stream sites (Table 5). Twenty-one of these species were recovered on the Population levels of keratinophilic fungi in the aquatic SDA medium, whereas twelve species were recovered habitats varied signiﬁcantly (P < 0.05) with time in on the 5-FC medium. Five species were common to two of the studied stream sites (the nonpolluted and the both media. The most abundant and frequent species less polluted site C), and in two of the pools (TMSS, on the SDA medium (as shown by their RIV’s) were TMK). G. candidum (167), Pa. lilacinus (60), and Pa. mar- However, the mean population levels of keratinophilic fungi were found to be either positively or negat- 201

∗ − Table 6. Mean population levels CFU L 1 of keratinophilic fungi in three stream sites sampled 5 times over an 8-month period using Sabouraud dextrose agar medium

Site March May June August October Mean ± SD ⊗ A: Unpolluted site 164.0a 228.0a 188.0a 225.3a 92.0b 179.5a± 55.7 B: Polluted site 48.0c 46.0c 35.3b 36.0b 62.7b 45.6c± 11.1 C: Polluted site 118.7b 158.0b 71.3b 16.0c 144.7a 101.7b± 58.2 ∗ Each value = mean of three replicates. ⊗ Values on the same sampling date followed by the same letter are not significantly different as assessed by least significant differences (LSD) at 5% level of probability. ively correlated with several ecological factors, which frequent in aquatic habitats where keratin occurs [2, were expected to influence population levels in these 3, 12, 34]. habitats. According to correllation coefficient (r2)val- The results (Tables 2–5) demonstrated that the 5- ues, no strong correlations were detected between FC medium was more suitable for the isolation of these factors and the mean population levels, and no dermatophytes and closely related species than the single factor could, on its own, explain differences in SDA medium; six of the dermatophyte species were population changes in these sites. recovered on 5-FC medium plates, whereas only one dermatophyte related fungus (Ch. keratinophilum) was recovered on the SDA medium plates. This may be attributed to the fact that 5-flurocytosine increases Discussion the growth rates of dermatophytes but it inhibits the growth of other species such as G. candidum [35]. It This study is a stage in an investigation designed to can thus be concluded that the use of a combination evaluate the distribution of dermatophytes and other of these two media rather than only one medium may closely related keratinophilic fungi in the Palestinian be necessary to give a more accurate picture about area as human risk factors. It was preceded by sur- keratinophilic fungal communities in aquatic habitats. veys of dermatophyte distributions in humans, school Furthermore, the SDP technique yielded a higher playgrounds, floor dust, polluted and unpolluted field number of fungal species (36) from these habitats than soils and the hair of domestic animals [6, 18, 22–31]. HBT (32). This may be attributed to the fact that HBT The present investigation was, therefore, centered on favors fungal species with strong keratinophilic activ- the ecology of dermatophytes and other keratinophilic ity (e.g., species of Chrysosporium and Fusarium) fungal species in swimming pools and polluted and [5], whereas SDP favors heavily sporulating species unpolluted streams and their role in the epidemiology (e.g., species of Penicillium and Acremonium) [6]. The of human mycotic infections especially tinea pedis. absence of highly keratinolytic active species (e.g., The present results are in agreement with those species of Microsporum,andTrichophyton)inthe of previous investigations that indicated a possible HBT may be attributed to the fact that those species relationship between this important group of fungi are found to be latter successors on human hair and, and the environment [22, 23, 31-33]. A total of 50 therefore, require longer incubation periods in HBT to fungal species were isolated from aquatic habitats, develop [6, 18]. many of which (33, 66%) were found to be pathogens The current study revealed differences in species or potentially pathogenic to humans, animals, insects biodiversity in the pools. The number of keratinophilic and plants (Table 1). Of these latter fungi T. men- fungal species ranged between 9–13 in the three pools tagrophytes and M. gypseum are two dermatophyte (Tables 2 and 3). The mean population levels also species that have been isolated from humans infec- varied significantly (F (2, 6) = 22.055, P = 0.002) ted with cutaneous mycoses. Other species, such as among these three pools, with the highest mean pop- Scopulariopsis brevicaulis, G. candidum, Alt. altern- ulation level encountered in the TMSS children’s pool ata, T. terrestre and A. flavus are considered to be followed by the TMK adults pool and the WB adult etiological agents of opportunistic mycoses. The res- pool. The higher population levels of keratinophilic ults are in agreement with those of similar surveys fungi in the children’s swimming pool can be attrib- that showed that keratinophilic fungi are especially 202 uted to the shallowness of the water in this pool, and of population levels in the three examined stream sites the more frequent use by a larger number of bathers. (Table 6), with the lowest mean population levels en- This indicates that children might be more exposed to countered in the polluted sites (B and C), followed by fungal diseases than adults in these habitats and that the unpolluted site. The richer biodiversity, in terms improvements in the hygienic conditions in such hab- of mean population densities and number of species in itats is needed (e.g., frequent water changes and proper the less polluted stream site (site C) as compared to the chlorination) to eliminate the risk of fungal disease more polluted stream site (site B), may be attributed to contraction in these pools (Table 7). The differences the lower levels of pollutants in the less polluted site in population levels between the adult pools (WB and (site C) due to physical and biological processes, or TMK) may also be attributed to differences in number adsorption of these materials by the plants that grow of visitors and frequency of water changes and chlor- on the two sides of the stream, that take place in the ination in those pools. This is in agreement with other water running down stream. similar reports [13, 36] that showed that the number Water pollution was found to reduce the biod- of bathers was positively correlated with swimming iversity of sensitive fungal species while, on the other pools contamination. Further work is needed to evalu- hand, it increased that of the less sensitive fungi [17]. ate the role of symptomatic and asymptomatic visitors This could explain the considerable increase in the in swimming pool contamination. number of such fungi as Chrysosporium and Penicil- Trichophyton mentagrophytes was isolated from lium spp, which seemed to be less sensitive to organic stream sites in this work and was the only dermato- pollutants in the raw city wastewater receiving sites (as phyte species isolated from the floors of swimming compared to unpolluted sites), and the decreased num- pools in Khaleel’s study [37]. English and Gibson [7], bers of Altrernaria and Geotrichum colonies, which and Detandt & Norlard [13] also reported this spe- seemed to be sensitive to organic pollutants (Table 4). cies from swimmers and swimming pools. Contam- However, based on r2 values, no strong correlation was ination of swimming pools by dermatophyte species detected between the studied factors and mean popu- especially, T. mentagrophytes, T. rubrum and Epider- lation levels. Therefore, no single factor could, on its mophyton floccusum, mainly comes from the shed skin own, explain the differences in population changes in scales of bathers who usually walk bare footed on the these sites. floors of the swimming pools. Bathers are, therefore The abundance and frequency data (Tables 2–5) apt to contract fungal skin infections including tinea show that the most dominant and stable compon- pedis. To avoid such infections, visitors are advised to ent species in the unpolluted stream site were: G. wash their feet as soon as getting home, and also man- candidum, Pa. lilacinus,andFusarium moniliforme agers should clean swimming pools floors frequently constituting 79.2% of all the fungal isolates (by HBT), and carefully, especially irregular floor surfaces [35]. (Table 5). With the exception of F. moniliforme,these Comparison between the mycobiota of polluted dominant species in addition to Pa. marquandii and and unpolluted stream sites revealed differences in Verticillium nubilum were the most stable and abund- the biodiversity of their component fungi. The num- ant species in the polluted stream sites constituting ber of recovered keratinophilic fungi ranged between 93.6–83.9% of all fungal isolates (Table 5). However, 15–28 species in these three stream sites, with the low- Acr. strictum, Alt. alternata and P. chrysogenum were est number found in the more polluted stream (site the most abundant and stable component species in the B) (Tables 4 and 5). This may be attributed to the TMSS children’s pool constituting 84.1% (by HBT) presence of toxic industrial pollutants (e.g., cyanides, (Table 3). In addition to the above mentioned species, detergents and phenol) in the polluted stream that G. candidum, Ch. keratinophilum and F. oxysporum resulted from pollution by the industrial wastewater were the most stable and dominant species in the released from nearby factories in the eastern part of adult’s pools (TMK and WB) constituting 73.1% of Nablus [5]. Further work is needed to evaluate these all fungal isolates (Table 3). industrial chemical wastes and their effects on fungal The results show that the aquatic habitats were rich biodiversity. in pathogenic or potentially pathogenic fungi (marked Water pollutants seem also to affect the mean pop- by + in Table 1), with the highest percentage in swim- ulation levels of keratinophilic fungi in aquatic habit- ming pools (77.3 %) followed by polluted stream sites ats. This was indicated by the significant difference (F (71.4%), and un-polluted stream sites (64.2%). These (2, 6) = 103.808, P < 0.001) found among the means species are either well-known agents of human and 203

− Table 7. Mean population levels CFU L 1 of keratinophilic fungi in three pools sampled three times over a 4-month period using Sabouraud dextrose agar medium

Sites May 1998 June 1998 August 1998 Mean ± SD ⊗ WB Adults’ pool 4.7b 34.0a 18.0b 18.9b ± 14.7 TMSS children’s pool 118.0a 26.7a 853.3a 332.7a ± 453.2 TMK Adults’ pool 87.3a 25.3a 238.0b 116.9b ± 109.4 ∗ Each value = mean of three replicates. ⊗ Values on the same date followed by the same letter are not significantly different as assessed by least significant differences (LSD) at 5% level of probability. animal mycoses (M. gypseum and T. mentagrophytes), creasingly frequent human and animal skin infections or have been isolated from various types of lesions in all over the world [30, 41, 42]. animals and humans (G. candidum, Alt. alternata and The genus Trichophyton was represented by two Pa. lilacinus)(Table1). species (T. mentagrophytes and T. terrestre). Tricho- Polluted and unpolluted stream sites and swim- phyton mentagrophytes is known to be a major causat- ming pools allowed the growth of a number of derma- ive agent of human dermatophytoses in the Palestinian tophytes and closely related keratinophilic species. area (West Bank) [22]. It was isolated from swimming The genus Chrysosporium was represented by three pools and unpolluted stream sites. This was in agree- species, of which Ch. keratinophilum was character- ment with the results of many similar studies [e.g., 11, istic of the adult pool (WB), Ch. merdarium of the 13] that also reported these species from sewage water unpolluted stream site and Ch. tropicum of the pol- and swimming pools. luted stream sites. Chrysosporium tropicum and Ch. Trichophyton terrestre was only isolated from the keratinophilum have a global distribution in aquatic less polluted site (site C) in the present study. It has habitats. They have been isolated from sewage sludge been commonly isolated by several investigators [2, in Egypt [2], from beach sediments of the river Tor- 12, 34, 38] from polluted water and swimming pools. dera in Spain [4]; from sediments of surface waters It is a potentially, pathogenic keratinophilic species, [34], and from a small pool in Italy [38]. Although and has been isolated from a mycotic granuloma on a the pathogenecity of Chrysosporium species to hu- woman’s arm [43]. mans and other animals is uncertain, their spores were Dermatophytes of the type responsible for fungal found to remain viable for several weeks in the bod- skin infections among Palestinians [22, 23] have not ies of experimentally infected animals, and hence they only been observed in swimming pools, polluted and could become pathogens [39]. Also C. keratinophilum un-polluted streams in this study (M. gypseum and T. has been isolated from human cases of onychomycosis mentagrophytes), but also from soil receiving raw city [40]. wastewater, schools playgrounds, children’s sandpits, The absence of T. mentagrophytes and M. gypseum and floor dusts (Microsporum audounii, M. gypseum, in polluted sites may be attributed to their sensitivity T. mentagrophytes and T. verrucosum) [24, 25, 28, 29]. to the organic wastes found in these sites or that these However, their concentration in these habitats would sites are less frequently used by humans and animals. seem to be too low to suggest that they are the main On the other hand, T. terrestre was isolated only from source of infections. polluted sites. This species and other species occurred Swimming pools and other aquatic habitats have in the polluted sites and had not been found in the un- been found to play a role in the epidemiology of skin polluted site can be considered to be originating from mycoses especially, tinea pedis [14, 44]. Among the raw city wastewater (Tables 4 and 5). main causative agents of this disease (E. floccusum, T. Microsporum gypseum is a dermatophyte that has mentagrophytes,andT. rubrum). Trichophyton men- been isolated from various environments, such as soil, tagrophytes was frequently isolated from the floors sewage and swimming pools [6, 12, 16, 38]. In the of swimming pools and swimmers feet [14, 44]. In present study, it was isolated only from the unpolluted this study this species was recovered from the pools stream site. This species has been reported to cause in- and un-polluted stream sites. 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