Study of fungal contamination of indoor public swimming pools in Uromia, Iran

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1 Study of fungal contamination of indoor public swimming pools in Uromia, Iran H. Nanbakhsh 1, K. Diba 2 & K. Hazarty 2 1 Department of Environmental Health, Uromia University of Medical Sciences, Iran 2 Department of Parasitology and Mycology, Uromia University of Medical Sciences, Iran Abstract The water in swimming pools cannot be a good carrier for transmission of fungal diseases but can be a source of fungus, so environmental surfaces may be contaminated by many species of fungi, and they then transmit them to swimmers. The fungal contaminations of four indoor swimming pools were studied by using membrane filtration and a swab sampling method. A total of 384 samples including water and environmental surfaces were collected and tested for the presence of fungi in different seasons within one year. Findings indicated that the average temperature, ph, residual chlorine and turbidity of water in the swimming pools within one year were respectively 29.9 C, 8.1,.6 ppm and.8 NTU. The most common fungi recovered were as follows: Aspergillus spp %, Candida spp. 22.9%, Rhizopus spp %, other filamentous fungi 16.6% and other yeast species 2.8% isolated from water. The fungi such as Alternaria, Cladosporium, philophora and Trichophyton mentagrophytis were isolated from dressing rooms, bathing rooms and other environmental places out of the pools. According to these results and previous studies on pools, it has been indicated that contamination of the swimming pools by fungi in our study was not significant in water of pools and the environment. The presence of dermatophytic fungus from dressing rooms was probably due to human contact. Key words: indoor public, swimming pool, fungi, contamination.

2 178 1 Introduction Detandt and Nolard [1] stated that public indoor swimming pools are one of the recreation centers which many people use them every day so that, can be contaminated by infectious agents, saprophytic fungi and other micro organisms. Mercantini et al [2] reported that Fungi are found in the different environment with variable distribution patterns depending on various factors. The most important of which is human association. Bolanos [3] studied about tinea pedis among students enrolled in swimming courses at university pool. Tinea pedis was determined on twelve of swimmers. The most common agent of tinea pedis in a study was Trichophyton rubrum (82%), infections by Trichophyton mentagrophytis (9%) and Epidermophyton floccosum (9%) was less common. Results also showed that, no dermatophyte was seen from any of 3 floor samples taken from the bathroom and pool facilities. Although in the other study, the following dermatophytes were isolated from the students feet; Trichophyton mentagrophytis (7%), Trichophyton rubrum (17.6%) and Candida albicans (11.8%). On this occasion T.mentagrophytis was recovered from 5 out of 3 floor samples. Another study was carried out by Attye et al [4] regarding Athletes feet. Result showed a significant incidence of occult athletes feet in swimmers. They concluded that, controlling of this endemic problem, adequate preventive measures must be taken. According to these results, It has been proven that, swimming pools may contribute to the spread of fungi and to be a source of fungal infections. Several authors; Mercantini et al [2], Fischer [5], Maghazy et al [6] and Mangiarotti and Caretta [7] have reported on the occurrence of dermatophytes, as well as other fungi, from swimming pools. The main objective of this research, was to determine fungal contamination of four indoor public swimming pools for the first time in Uromia, in order to promote the knowledge of swimmers and people to observe health regulations to control and prevent the fungal Disease. 2 Materials and methods The method of study in this research was a descriptive-cross sectional. Samples from water of four indoor public swimming pools (1, 2, 3, 4) of Uromia province were taken in four seasons during one year, in 21. A plastic handle pump was used to take sample from swimming pools. From total 348 samples, 248 samples were collected from disinfected swimming pools in compliance with APHA (American Public Health Association) standard methods. A sufficient amount of sodium thiosulfate was present in the sampling bottles to neutralize the chlorine residual in the samples. All samples were processed immediately upon arrival. Sampling was carried out two times per month, first and fifteenth, for each swimming pool. Samples were filtrated through Millipore filters with.45 micrometer size. The filters were transferred to three different culture media included Saboroud Dextrose Agar, Saboroud + Chloramphenicole +

3 179 Cyclohexamide and Malt extract Agar 2%. The plates incubated at 25 C for 3 weeks and examined at frequent intervals. 1 other samples were collected from environmental places of swimming pools such as: foot washing sink, bathrooms, dried sauna rooms, walls and floor around of pools. Sampling was carried by Carpet (a piece of sterilized carpet in the size of 4 6 cm²). Sampling from dried surfaces and Swab sampling for wet samples that were rubbed against the surfaces and then wrapped in sterile aluminum foil and transferred to laboratory. All the pieces of carpet were shaken over the culture media and the swabs were rubbed inoculating to Agar under a biologic hood. The plates were incubated for 3 weeks at 25ºC and tested at frequent intervals and fungal growth was determined by the routine laboratory method, especially slide culture method. 3 Results Findings of this research regarding to the physical and chemical parameters indicated that the average temperature, ph, residual chlorine and turbidity of water were respectively: 29ºC, 8.1,.6, mg/l and.8 NTU. Moreover, the average daily number of swimmers during summer season was more than others (Mean = 385). The fungi isolated from water of swimming pools were included saprophytic filamentous fungi and species of yeasts. The fungi isolated from environmental surfaces were: saprophytic filamentous, yeast species and a dermatophytic fungus, Trychophyton mentagrophytis (isolated from dressing room). Table 1 shows the frequency and percentage of above fungi in each swimming pool with related environmental surfaces. Findings indicated that no dermatophyte was recovered from water samples, indeed the fungi isolated from water samples were common saprophytic flora and their presence in pools water were not significant. Frequency and percentage of the fungi isolated from environmental different places of swimming pools are shown in table 2. According to results, the species of fungi such as: Aspergillus, Penicillium, Cladosporium, and Candida were in high frequency that isolated from environmental surfaces. Moreover dermatophytic fungus; Trichophyton mentagrophytis was the most important fungus, which isolated from dressing room. The most frequent fungi isolated from environmental surfaces were: Aspergillus 53%, Penicillium 51%, Cladosporium 45%, Candida spp 23% and low frequent were; Exophiala, Crysosporium, Dermatophyte and phoma. Results also showed that from total 284 samples of water pools 48 cases (18.6 %) of fungal contaminations were observed and the most common of them were; Aspergillus 56.25%, Rhizopus 4.16%, Candida 29.9% and 16.6% others (table 3 and figure 1). 4 Discussion According to Lee and Fleece [8] and Detandt and Nolard [1] many studies have indicated that, the sanitary quality of indoor public swimming pools is concerned for swimmers due to swallow and contact with water. Furthermore, it has been shown that, swimming pools contribute to spread of fungi and other organisms,

4 18 because of common usage of them. Thus, the environmental sanitation of swimming pools is very important. Testing of some factors such as: ph, temperature, and residual chlorine are critical for swimming pools. A study has been carried out by Roy [9] in the United States and showed that, with assessing the above factors with 95% confidence level, can justify the contamination of swimming pools. Table 1: cases pool Total Frequency and percentage of fungal groups in water and environmental surfaces. place of sample Dermetophyte yeast filamentous N % N % N % water places Water places water places water places water places Table 2: Types of fungi in different places of four swimming pools. Pool Total Fungi N % N % N % N % N % Ulocladium Aspergillus Alternaria Fusorium Rhizopus Penicillium Acremonium Cladosporium Arthriniumq Rhodotorub Candida Phialophrera Exophiala Crysosporium Phomo Trichophyton Mucor

5 181 Table 3: Number and percentage of occurrence of fungal cases in swimming pools. Fungi candida Rhizopus Aspergillus Others Total N % N % N % N % N % pool Total swimming 7.3 Candida Rhizopus Aspergillus Other Figure 1: Types of isolated fungi from swimming pools. In the present study, we examined these factors during one year (4 seasons) for swimming pools; water and environments then compared them with standard levels. The average of free residual chlorine in swimming pools water was.6 ppm, less than standard level (standard level, 1-2 ppm). Moreover 85% of swimming pools had free residual chlorine less than standard level. Fischer [5] stated that, normal concentration of chlorine does not inhibit the growth of fungi. The average temperature of water swimming pools was 3.1ºC, more than standard level (standard level 24.5 C- 25.5ºC). Increasing these factors more than standard level may create growing of biological agents in the swimming pools. Anderson [1] in 1979 illustrated that; the optimum temperature for the growth of fungi is between 2 C and 3 C,while the temperature upper than 45 C is caused to stop growing of fungi. Feuerman [11] believed that swimming pools, which have been disinfected with chlorine, no dermatophyte was isolated. Some authors; Detandt and Nolard [1], Fischer [5], and Maghazy et al [6] have studied about the presence of dermatophytes in the water and different places of swimming pools. A study was carried out by Nomayendeh [12] in 4 swimming pools in Tehran Iran, she isolated 4 (1%) dematophytes from water of swimming pools. Shadzi et al [13] have investigated in 4 indoor swimming pools in Isfahan - Iran and concluded that, dematophytes were only isolated from

6 182 dressing rooms and bathrooms. Vissent [16] in France isolated; T.mentagrophytes, T.rubrum and Epidermaphytone Flacosum from water of swimming pools. In our study a strain of dermatophytic fungus, Trichophyton menta grophytis was only isolated from dressing room for once. Presence of this dermatophyte could be related to contact of swimmers with tinea pedis, tinea corporis or the other type of dermatophytosis to floor or walls of the room. Bolanos [3], Attye et al [4], Reiffers and Laugier [14] indicated that, swimmers with tinea pedis could spread debris-containing dermatophytes on the floor of pools. Maghzay et al [6] isolated Trichophyton terrestre, T.mentagrophytis and Microsporum gypseum from water of two swimming pools in Egypt. The authors stated that, isolation of above dermatophytes might be a continuous contamination of the swimming pool water by fungi through air, soil and human bodies. In our study, no dermatophytes were isolated from water; the reason may be related to the different techniques used for research or residual chlorine in water. Zaror et al [15] isolated T.mentagrophytis from the bathrooms, which support our findings. Our findings showed a relationship between the numbers of swimmers and number of isolated fungal cases. The higher number of isolated fungal cases may be related to the higher of swimmers (average daily 385) and lowest amount of residual chlorine (.6mg/l) where as, swimming pool no 4 with lower number of swimmers (15 daily) and high amount of residual chlorine (1.5mg/l) had the lowest number of isolated fungi (table 3). The most common fungi isolated from swimming pools were: Candida 45% in swimming pool no 2, Rhizopus 5% in swimming pools no.1 and 2, Aspergillus 48% in swimming pool no.1. 5 Conclusion Through this study, we can conclude that, rarely occurrence of dermatophytes and some pathogenic fungi in swimming pools are related to high controlling of hygiene of pools, efficiency of residual chlorine for inhibiting growth of these fungi. However, it is recommended that the manager of swimming pools must pay more attention to the residual chlorine based on standard level and environmental sanitation of swimming pools because of high frequency isolation of saprophytic filamentous fungi and yeasts from water of swimming pools. Acknowledgement We would like to thank vice research chancellor of Urmia University of Medical science who funded this research. References [1] Detandt, M. & Nolard, N., Dermatophytes and swimming pools seasonal fluctuation. Mycoses, 31(1), pp.495 5, 1988.

7 183 [2] Mercantini, A. M. Marsella, R. lambiase, L. and Fulvi, E., Isolation of keratinophilic fungi from floors in Roman in primary school. Mycopathalogia, 82,pp , [3] Bolanos, B., Dermatophytes to feet infection among students enrolled in swimming courses at a university pool. Bol ASO Med PR, 5, pp , [4] Attye, A. Auger, P. Joly, J., Incidence of occult athletes foot in swimmings. Eur-J- Epidemol 6(3), pp , 199. [5] Fischer, E., How long can dematophytic fungi survive in water of swimming pools. Dematologica, 165,pp , [6] Maghazy, S. M. N. Abdel- Mallek, A.Y. Bagy M M K., fungi in two swimming pools in Assiut town. Egypt zientrabl. Microbial 144, pp , [7] Mangiarotti, A.M.& Caretta, Ge., Kerantinophilic fungi isolated from a small pool. Mycopathologia, 85,pp. 9 11, [8] Lee, j. Deininger, R.A. fleece, R.M., Rapid Determination of Bacteria in pools. Environmental Health, vol (6), July and August, pp 9-13, 21. [9] Roy, A. Paul., An Environmental model for swimming pool Bacteriology. Am. J. public Health, 62, pp , [1] Anderson, I. H., In Vitro survival of human pathogenic fungi in Havaiian Beach Sand. Sabouradia,17: pp.13-22, [11] Feuerman, E.J., On the occurrence pathogenic dematophytes on some swimming pools from Telaviv area. Castellania, 5(6),pp , [12] Nomayendeh, N., Study of dermatophytic flora of public swimming pools and souna. MSPH thesis University of Tehran, farsi trnslation, pp.24-57,1993. [13] Shadzi, S. Pourmoghadas, H. Chadeganipour, M. Zare, A., Fungal contamination in four swimming pools in Isfahan, I JBMS, 4(1), pp.5-53, 21. [14] Reiffers, J. Laugier, P., Mycoses des pieds. Schwaiz Rundschau Med, 63(28),pp , [15] Zaror, L. fischman, O. forjaz, M. H. H. Oliveria A., Dermatophytes in sporting activities. Mykosen, 28(8),pp , [16] Vissent, M. F., Dermatophytes isolated in a swimming pool in Vant on the loive atlantic beaches. Rev of Med. Veterinary mycology, 13 (1), 2, 1973.

Study of Fungal Contamination of Indoor Public Swimming Pools

Iranian J Publ Health, Vol. 33, No. 1, Iranian pp.6-65, J Publ 24 Health, Vol. 33, No. 1, pp.6-65, 24 Study of Fungal Contamination of Indoor Public Swimming Pools *H Nanbakhsh 1, K Diba 2, K Hazarti 2