Australian Journal of Basic and Applied Sciences, 4(2): 122-126, 2010 ISSN 1991-8178

Opportunistic Pathogenic Fungi of the House Dust in Turubah, Kingdom of Saudi Arabia

Al-Humiany, A.A.

Department of Medical Microbiology, Faculty of Applied Medical Sciences, Taif University, Turubah, KSA

Abstract: Xerophilic-, yeast-, thermophilic-, thermotolerant and keratinophilic fungi were isolated from house dust of Turubah, Taif, kSA. Thirty six samples were collected during November, 2009. Using the appropriate medium for each fungal group, 371x10³ CFU were recovered belonging to forty two taxa, in addition to five taxa of keratinophilic fungi. The most abundant molds are Aspergillus flavus, A. penicilloides, A. repens, Penicilium glabrum, Mucor racemosus. Aspergillus fumigatus, Rhizomucor pusillus, Thermomyces lanuginosus and Thermophymatospora fibuligera are the most thermotolerant and thermophilic molds. The most frequent yeast fungi are Candida albicans, Trichosporon cutaneum and Exophiala spinifera. Three geophilic dermatophytes namely; Trichophyton terrestre, Scopulariopsis brevicaulis and S. candida were isolated by human hair baiting technique. Many of the identified fungi are toxigenic, opportunistic pathogenic, pathogenic and/or antigenic. Regular cleaning of indoor environment is a must.

Key words: Fungi, house dust, Turubah, KSA.

INTRODUCTION

Xerophilic fungi are among the major biological components of the house dust. Indoor fungi are able to propagate in almost any home (Bronswijk et al., 1986). Exposure to these fungi induces several human-health hazards. Allergy, bronchial asthma (Gent et al., 2009), superficial, deep- and systemic mycoses may induced especially in the immunocompromised persons (McGinis, 1980). Dust fungi play an important role in the dissemination of human diseases (Cooley et al., 2004). Several reports about fungal component of house dust allover the world are available e.g., in New Jersey (Schaffer et al., 1953); Britain (Davies, 1960 and Lustgraaf and Bronswijk, 1977); Cairo (Saad, 1985); Riyadh (Saad and El-Gindy, 1990); Germany (Ostrowski, 1999 and Kock et al., 2000); Polanda (Pastuska et al., 2000); Ontario ( Scott, 2001); Aden (El-Gindy et al., 2002); Taiwan (Su et al., 2001 and Wu et al., 2004); Argentina (Basilico et al., 2007) and Austria (Haas et al., 2007). Here, the fungi in the house dust of Turubah near Taif, KSA was investigated.

MATERIALS AND METHODS

Collection of House Dust Samples: Thirty six samples were collected from indoor of home at Turubah. Floor dust of bedrooms, living rooms, filters of air -conditions and window frames were mixed to give a composite sample for each home. Each dust sample was kept in clean plastic bag at 4-6o C until processed.

Isolation of Fungi: Ten mg of each dust sample were transferred aseptically to 9 mm sterile Petri dish. Ten ml of the appropriate medium (45o C) were added, hand swirlled and left to solidify. Thermophilic fungi were isolated at 50o C for 4-6 days, while others were incubated at 28o C for 5-7 days. Count (C) of colony forming units per g dust (CFU/g dust), percentage of total count (% TC), number of cases of isolation (NCI) and occurrence remark (OR) were calculated.

Media: Sabouraud’s glucose agar: (Peptone, 10 g; glucose, 40g and agar, 20g in 1000 ml tap water) was used for isolation xerophilic fungi.

Corresponding Author: Al-Humiany, A.A., Department of Medical Microbiology, Faculty of Applied Medical Sciences, Taif University, Turubah, KSA. E-mail: [email protected] 122 Aust. J. Basic & Appl. Sci., 4(2): 122-126, 2010

Yeast glucose agar: (Yeast extract, 5g; glucose, 10g and agar, 20g in 1000 ml tap water) was used for isolation of thermophilic-, thermotolerant and yeast fungi. Isolation of keratinophilic fungi: The hair – baiting technique (Vanbreuseghem, 1952) was used for isolation of keratinophilic fungi. Choramphenicol (0.25gl ¹) was added to the adopted media to eliminate bacterial growth and to delay the appearance of fast growing fungi. Pure culture of the isolated fungi were identified according the following descriptive manuals, Morton and Smith (1963); Raper and Fennell (1965); Ajello (1968); Ames (1969); Rifai (1969); Ellis (1971 & 1976); Booth (1977); Domsch et al. (1980); Pitt (1985); Moubasher (1993) and Ho et al. (1999).

RESULTS AND DISCUSSION

House dust inhabiting fungi are an important group of indoor fungi that are able to propagate in almost any home (Bronswijk et al., 1986 and Portony et al., 2007). The total fungal load (CFU) per gram house dust was 3.71 x 105 in addition to keratinophilic fungi. Forty two fungal species belonging to twenty four genera were isolated from house dust of Turubah (Table 1 – 4). Among these fungi thirty species have human health risk. They may be opportunistic pathogens and ' or antigenic according to McGinis (1980). Most of these fungi have been previously reported from house dust (Schaffer et al., 1953; Davies, 1960; Lustgraaaf and Bronswijk, 1977; Saad, 1985; Bronswijk et al., 1986; Saad and El-Gindy, 1990; Ostrowski, 1999; koch et al., 2000; Scott, 2001; El-Gindy et al., 2002 and Wu et al., 2004). Results in Table (1) show that twenty species belonging to eleven genera were isolated .The most abundant fungi were Aspergillus flavus (10.32 %), Penicillium glabrum (9.4 %), A. penicilloides (7.06 %), A. repens (7.06 %) and Mucor racemosus (7.06 %). A. flavus has a worldwide distribution especially in tropics. It is highly toxigenic to humans and animals. Aflatoxins produced by this fungus are carcinogenic. It is associated with reports of asthma, aspergillosis and occasionally corneal-, otomycosis- and nasoorbital infections (Ostrowski, 1999). Penicillium glabrum is toxigenic and allergenic (McGinis, 1980). A. penicilloides and A. repens are xerophilic fungi associated with house dust mites and have a possible human and animal potential pathogenicity (Samson and Lustgraaf, 1978). Mucor, Rhizopus and Cunninghamella are involved in zygomycosis (McGinis, 1980). The health implication of other fungi will be mentioned instantly here after. F. solani is frequently involved in eye, skin and nail infections. Phoma glomerata cause phaeohyphomycosis. Trichoderma viride is toxigenic and pathogenic (McGinis, 1980). Aspergillus versicolor produces human toxigeni volatile metabolites at indoor environment (Pasanen et al., 1997). Concerning yeast-fungi, results in Table (2) show that five yeast species belonging to three genera were isolated (77x10³ CFU'g dust). These yeast fungi were reported in house dust of Cairo (Saad, 1985). Candida albicans and Trichosporon cutaneum were the most frequent comprising 38.96 and 35.84% of the total yeast count respectively. C. albicans is cosmopolitan in distribution with socio-economic environment differences. Mycosis caused by Candida is called candidiasis: oral, intestinal, vaginal, pulmonary and meningeal candidiasis (Winner and Hurley, 1964). Trichosporon cutaneum was isolated from house dust of Germany (Ostrowski, 1999). Candida guilliermondii was isolated from five house dust samples comprising 7.01 % of the total yeast count. It is the etiological agent of endocarditis ( Winner and Hurley, 1964). Exophiala exophiale was isolated from six dust samples while E. spinifera was isolated from seven samples comprising 7.53 and 10.64 % of the total yeast count respectively. These black yeasts were isolated from house dust of Cairo (Saad, 1985). They cause human skin phaeohyphomycosis (McGinis, 1980). Regarding thermophilous fungi, results in Table (3) show that their load was 76x10³ CFU'g dust. Twelve species belonging to nine genera were recovered. The most abundant fungi were Aspergillus fumigatus, Rhizomucor pusillus, Thermomyces lanuginosus and Thermophymatospora fibuligera, each comprising 10.78% of the total count of thermophilous fungi. The first two fungi were repeatedly isolated from house dust (Saad, 1985; Ostrowski, 1999 and Scott, 2001). Allergenic thermophilic fungi were isolated from house dust of asthmatics (Srinivasan et al., 2005). A. fumigatus is a mjor pathogen. It is responsible for about 90% of all invasive mold infections world-wide (Ostrowski, 1999 and Latge, 2003). R. pusipllus is involved in zygomycosis (McGinis, 1980). Thermophymatospora fibuligera was previously isolated from an Iraqi date palm plantation (Abdullah and Al-Bader, 1999). Thermomyces lanuginosus was the first established thermophile with worldwide distribution. The human health hazard of other opportunistic pathogenic thermophilous fungi will be mentioned hereafter instantly. Absidia corymbifera is involved in mucormycosis. Aspergillus terreus cause aspergillosis, cystic fibrosis, otomycosis and nail infections (McGinis, 1980). Concerning keratinophilic fungi results in Table (4) show their low occurrence (4-6 dust samples out of 36). Nectria haematococca is the teleomoph of Fusarium solani which is health hazardous fungus as mentioned before. Scopularopsis spp. are toxigenic, allergenic and can cause skin and nail infections.

123 Aust. J. Basic & Appl. Sci., 4(2): 122-126, 2010

Table 1: Number of Colony Forming Units (C) in Thousands Per g Dust , Percentage of Total Count (%TC) , Number of Cases of Isolation (NCI) and Occurrence Remark (OR) of Xerophilic House Dust Fungi. Fungi C %TC NCI OR* Aspergillus flavus** 22.5 10.32 18 L A. niger 5.4 2.47 5 L A . penicilloides** 15.4 7.06 8 M A.repens** 15.4 7.06 8 M A. versicolor** 8.2 3.76 6 H Chaetomium bostrychodes 5.4 2.47 5 L C. globosum** 5.4 2.47 5 L Cladosporium sphaerospermum** 8.2 3.76 7 L Cunninghamella elegans** 10.6 4.86 9 M Fusarium solani** 10.6 4.86 9 M Mucor mucedo** 10.6 4.86 10 M M. racemosus** 15.4 7.06 8 M Penicillium glabrum** 20.5 9.40 17 H P. verrucosum** 5.4 2.47 5 L P. purpurogenum 5.4 2.47 6 L Phoma glomerata** 10.6 4.86 8 M Rhizopus oryzae** 5.4 2.47 4 L R.stolonifer** 10.6 4.86 9 M Trichoderma viride** 6.4 2.93 5 L Wallemia sebi 10.6 4.86 8 M Total count 218.0 *Occurrence remark: H = High, 17 Cases out of 36; M = Moderate, 8- 16 Cases out of 36 and L = Low, 4-7 cases out of 36. **Toxigenic, antigenic and ' or opportunistic pathogenic or pathogenic fungi.

Table 2: Number of Colony Forming Units (C) in Thousands Per g Dust, Percentage of Total Count (%TC), Number of Cases of Isolation (NCI) and Occurrence Remark (OR) of Yeast Fungi of the House Dust. Yeast C %TC NCI OR Candida albicans** 30.0 38.96 20 H C. guilliermondii** 5.4 7.01 5 L Exophial exophiale** 5.8 7.53 6 L E. spinifera** 8.2 10.64 7 L Trichosporon cutaneum** 27.6 35.84 18 H Total count 77.0 and **as described at the legend of Table 1.

Table 3: Number of Colony Forming Units (C) in Thousands Per g Dust , Percentage of Total Count (%TC), Number of Cases of Isolation (NCI) and Occurrence Remark (OR) of Thermophilous House Dust Fungi . Fungi C %TC NCI OR* Absidia corymbifera** 5.4 7.11 4 L Aspergillus aculeatus 5.4 7.11 4 L A.flavipes 5.4 7.11 4 L A.fumigatus** 8.2 10.78 6 L A.terreus** 5.4 7.11 4 L Chaetomium thermophile 5.4 7.11 4 L Emericella nidulans** 5.4 7.11 4 L Rhizomucor pusillus ** 8.2 10.78 6 L Rhizopus rhizopodiformis 5.4 7.11 4 L Talaromyces thermophilus 5.4 7.11 4 L Thermomyces lanuginosus 8.2 10.78 7 L Thermophmatospora fibuligera 8.2 10.78 7 L Total count 76.0 *and **as described at the legend of Table 1.

Table 4: Number of Cases of Isolation (NCI) and Occurrence Remark (OR) of Keratinophilic Fungi in The House Dust. Fungi NCI OR* Aspergillus niger 4L Nectria haematococca** 6L Scopulariopsis brevecaulis** 5L S. candida** 4L Trichophyton terrestre** 4 L*and **as described at the legend of Table 1.

S. brevicaulis is pathogenic to human causing deep ulcers, skin infections and chronic onychomycosis (Morton & Smith, 1963 and Ajello, 1968). Trichophyton terrestre was reported from mycotic granuloma of arm of a woman (Frey et al., 1979). Occurrence of dermatophytes as saprophytes in dust growing on keratinous debris of human or animal origin is an established fact especially for geophilic dermatophytes and other related fungi.

124 Aust. J. Basic & Appl. Sci., 4(2): 122-126, 2010

Conclusion: Turubah is a dusty city. Regular meticulous cleaning is very important to prevent dust accumulation at indoor environment and consequently the propagation of indoor fungi.

REFERENCES

Abdulla, S.K. and S.M. Al-bader, 1990. On The Thermophilic and Thermotolerant Mycoflora of Iraq. Sydowia, 42: 1-7. Ajello, W.L., 1968. A Taxonomic Review of The Dermatophytes and Related Species. Sabouradia, 6: 147- 159. Ames, T.A., 1969. A Monograph of Chaetomiaceae. Wheldon and Wesltey L.T.D. Strechert-Hasner Service Agency. Inc. Codict, Herts New York, pp: 55. Basilico, M.Z., C. Chiericati, E.E. Aringoli, R.L. Althaus and J.C. Basilico, 2007. Influence of Environmental Facters on Airbone Fungi in Houses of Santafe City, Argentina. Sci. of The Total Environ., 376(1-3): 143-150. Booth, C., 1977. Fusarium Laboratory Guide to The Identification of Major Species. Commonwealth Mycological Institute, Kew, Surrey, England. Bronswijk, J.E.M.H., G. Rijckaert and B.V.D. Lustgraaf, 1986. Indoor Fungi, Distribution and Allergencity. Acta Bot. Neerl., 35(3): 329-345. Cooley, J.D., W.C. Wong, C.A. Jumper and D.C. Straus, 2004. Fungi and The Indoor Environment: Their Impact on Human Health. Advances in Appl. Microbiol., 55: 1-30. Davies, R.R., 1960. Viable Molds in House Dust. Trans. Brit. Mycol. Soc., 43: 617-630. Domsch, K.H., W. Gams and T.H. Anderson, 1980. Compendium of Soil Fungi. Academic Press, London. El-Gindy, A.A., Z.M. Ibrahim and A.H. Dughaish, 2002. Fungi of House Dust in Aden-Yemen. Afr. J. of Mycol. and Biotechnol., 10(1): 49-61. Ellis, M.B., 1971. Dematiaceous Hyphomycetes . Commonwealth Mycological Institute, Kew, Surrey, England. Ellis, M.B., 1976. More Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey, England. Frey, D., R.J. Oldfield and R.C. Bridger, 1979. A Colour Atlas of Pathogenic Fungi. Wolfe Medical Publication Ltd., Wolfe House 3-5 Conway Street, London WIP 6HE, pp: 168. Gent, F.J., K. Belanger, E.W. Triche, M.B. Bracken, W.S. Beckett and B.P. Leaderer, 2009. Association of Pediatric Asthma Severity With Exposure to Common Household Dust Allergens . Envion. Res., 109(6): 768-774. Haas, D., J. Habib, H. Galler, W. Buzina, R. Schlacher, E. Marth and F.F. Reinthaler, 2007. Assessment of Indoor Air in Austrian Apartments With and Without Mold Growth. Atmosph. Environ., 41(25): 5192-5201. Ho, M.H.M., R.F. Castaneda, F.M. Dugan, and S.C. Jong, 1999. Cladosporium and Cladophialophora in Culture ; Description and Expanded Key. LXXII: 115-157. Koch, A., K.J. Heilemann, W. Bischof, J. Heinrich and H.E. Wichmann, 2000. Indoor Viable Mold spores : A Comparision Between Two Cities , Erfurt (Eastern Germany) and Hamburg (Western Germany). Allergy, 55(2): 176-180. Latge, J.P., 2003. Aspergillus fumigatus, a Saprophytic Pathogenic Fungus. Mycologist, 17(2): 56-61. Lustgraaf, B.V.D. and J.E.M.H. Bronswijk, 1977. Fungi in House Dust . Ann. Allergy., 39: 152. McGinis, R., 1980. Laboratory Handbook of Medical Mycology . Academic Press , New York . Morton, F.J. and G. Smith, 1963. The Genus Scopulariopsis, Microascus and Doratomyces, Mycological Paper, 86: 1-96. Commonwealth Mycological Institute, Kew, Surrey, England. Moubasher, A.H., 1993. Soil Fungi in Qatar and Other Arab Countries .The Scientific and Applied Research Center, University of Qatar, Doha, Qatar. Ostrowaski, R., 1999. Exposure Assessment of Molds in Indoor Environments in Relations to Chronic Respiratory Diseases. Dt. Zentralbibliotek F. Medizin, Copyright Shaker Verlag. Pasanen, P., A. Korpi, P. Kalliokoski and A.L. Pasanen, 1997. Growth and Volatile Metabolite Production of Aspergillus versicolor in House Dust. Environ. Internation. J., 23(4): 425-432. Pastuska, J.S., V.K. Tha Paw, D.D. Lis, A.O. Wlazl and K. Ulfig, 2000. Bacteria and Fungi Aerosol in Indoor Environment in Upper Silesia, Poland. Atmosph. Environ., 34(22): 3833-3842. Pitt, J.I., 1985. A Laboratory Guide to Common Penicillium Species. Commonwealth Scientific and Industrial Research Organization, Division of Food Research, P: 184.

125 Aust. J. Basic & Appl. Sci., 4(2): 122-126, 2010

Portony, J.M., C.S. Barnes and K. Kennedy, 2007. Samping for Indoor Fung. J. Allergy and Clinical Immunol., 113(2) : 189-198. Raper, K.B. and D.J. Fennell, 1965. The Genus Aspergillus. Williams and Wilkins Baltimore, USA. Rifai , M.A., 1969. A Revision of The Genus Trichoderma. Mycological Paper., 116: 56. Saad, R.R., 1985. The House Dust and Its Role in The Dissimination of Some Human Diseases. Ph.D. Thesis, Department of Botany, Faculty of Science, Ain-Shams University. Saad, R.R. and A.A. El-Gindy, 1990. Fungi of The House Dust in Riyadh, Saudi Arabia. Zentralb., 1(145): 65-68. Samson, R.A. and B.V.D. Lustgraaf, 1978. Aspergillus penicilloides and Eurotium halophilicum Association with House – Dust Mites. Mycopathologia , 64(1): 13-16. Schaffer, N.M.D., E.N.J. Orange, E.E.M.D. Seidmon, N.J. Plainfield and S.B.S. Bruskin, 1953. The Clinical Evaluation of Air-Borne and House Dust in New Jersey. J. Allergy, 24: 348-353. Scott, J.A., 2001. Studies on Indoor Fungi. Doctor Thesis, Department of Botany, University of Tornto, Canada. Srinivasan, B., U.K. Kannaian and V.B.P. Ranga, 2005. Allergenic Thermophilic Fungi from House Dust of Asthmatics J. of Allergy and Clin. Immunol., 115(2): S26. Su, H.J., P.C. Wu, H.L. Chen, F.C. Lee and L.L. Lin, 2001. Exposure Assessment of Indoor Allergens, Endotoxins and Airbone Fungi from Homes in Southern Taiwan . Environ. Res., 85(2): 135-144. Vanbreuseghem, R., 1952. Biological Technique for The Isolation of Dermatophytes from Soil. Annal. Soc. Belge. Med. Tropicale, 32: 173. Winner, W.L. and R. Hurley, 1964. Candida albicans. Boston, Little, Brown. Wu, P.C., J.C. Tsai, F.C. Li, S.C. Lung, and H.J. Su, 2004. Increased Levels of Ambinent Fungal Spores in Taiwan Are Associated With Dust Events from China. Atmosph. Environ., 38(29): 4879-4886.

126