Skip to main content


We’d like to understand how you use our websites in order to improve them. Register your interest.

Enzymatic and toxigenic ability of opportunistic fungi contaminating intensive care units and operation rooms at Assiut University Hospitals, Egypt


Total of 110 isolates belonging to 8 fungal species collected from intensive care units (ICUs) and operation rooms (ORs) at Assiut University hospitals were examined for their ability to produce some extracellular enzymes and mycotoxins which are considered as important factors involved in for fungal pathogenicity. The results revealed that 73, 92 and 78 out of the 110 tested isolates produced protease, lipase and urease respectively; meanwhile, 77 of the tested isolates exhibited some hemolytic activities. Chromatographic analysis (TLC) of the crude extract of the fungal isolates tested revealed that 79 isolates of them had the ability to produce at least one of these mycotoxic compounds (aflatoxins B1, B2, G1, gliotoxin, fumigillin, T-2, zearalenone, roridin A & E, verrucarin A & J, trichoveroids, satratoxin H & E). These results demonstrate that the opportunistic fungal species isolated from (ICUs) and (ORs) and tested exhibited some enzymatic and mycotoxic ability which are the most effective virulence factors contributing to fungal pathogenicity indicating that the management of infection control unit at Assiut University hospitals must be aware of not only bacterial but also fungal contamination.


Members belonging to the Aspergillus, Fusarium and Mucorales genera are regarded as the main cause of fungal infections at hospitals (Alberti et al., 2001; Faure et al., 2000; Perdelli et al., 2006). Indeed fungi contaminating hospital rooms may grow on organic matter including various building materials and develop microcolonies. Prior to possible dissemination spores emanating from these colonies could be inhaled by immuno-suppressed patients resulting in local infections (Singh & Paterson, 2005). The ability of fungi to cause human diseases (mycoses) as pathogens appears to be accidental and such diseases are primarily related to the immunological status of the host and environmental exposure, rather than to the infecting organism (Rippon, 1988; Kwon-Chung & Bennett, 1992; Ellis, 1994). A relationship between fungal contamination in hospital environments and the incidence of invasive aspergillosis has been demonstrated (Alberti et al., 2001) and more than 500 cases of post-operative aspergillosis in immuno-competent individuals have been reported (Pasqualotto and Denning, 2006). Aspergillus fumigatus and A. flavus are the leading species of the genus Aspergillus causing invasive aspergillosis (Pasqualotto, 2008). Outbreaks of nosocomial aspergillosis are attributed to airborne sources and even small concentrations of spores have been associated with outbreaks (Vonberg and Gastmeier, 2006).

Fungi are known to elaborate extracellular enzymes based on the substrate they utilize for growth. Extracellularly produced enzymes have been described in certain fungi such as Candida (Borg & Ruchel, 1988) and Aspergillus species (Hanzi et al., 1993). Production and secretion of hydrolytic enzymes, such as proteases, lipases and phospholipases are very important virulence factors. These enzymes play a role in nutrition, tissue damage, fungal dissemination within the human body, iron acquisition and overcoming the host immune system which strongly affects fungal pathogenicity (Ibrahim et al., 1995). Secretion of enzymes into extracellular environments might be an important adaptive mechanism during the life cycle of fungi (Monod et al., 2002). Earlier studies on fungal enzymatic activities aimed at establishing the role of enzymes in fungal pathogenicity, as well as their capacity to induce inflammatory reactions in the host (Rippon, 1982). It is logical to suppose that these enzymes could act by enabling tissue invasion easier, but they could also participate in causing infection by impairing some mechanisms of the immune system and/or assist in obtaining of nutrients, thus causing injury to the host (Birch et al., 2004; Da Silva et al., 2005). Hussein and Brasel et al., (2001) examined the ability of 80 fungal isolates from keratitis patients to produce extracellular enzymes in growth medium and found that most of these isolates could produce protease, lipase, urease and catalase enzymes but at varying levels.

Mycotoxins are an extremely adverse group of low molecular weight fungal secondary metabolites which when ingested, inhaled or absorbed through the skin; can cause lowered performance, sickness or even death in man and animals including birds (Pitt, 1996; and Van Egmond & Speijers, 1999). They may affect the reproductive, immune, gastrointestinal systems, specific target organs, in addition they may exhibit hormonal activity, developmental defects including those relating to birth (tetragenic and neurotoxic) (Richard, 1991 ; Sharma, 1993 ; Kuiper-Goodman, 2004). Although fungal spores may have the highest concentrations of mycotoxins, the vegetative part of the fungus, the mycelium or the substrate upon which the fungus grows can also contain these toxins. Viability of spores is not essential to toxicity. In other words, a dead spore can still be a source of toxin (Keller, et al., 2005). Infants and children are considered more susceptible to different toxins than adults, because of their lower body weight, higher metabolic rate, incomplete development of some organs and tissues such as those in the central nervous system (WHO, 1986 ; NAS, 1993). Nonetheless, human illnesses caused by mycotoxins may be a public health problem than one realizes because some of these cases (chronic) may go un-noticed for an extended period of time unless large amounts of mycotoxins are consumed resulting in acute symptomology (Hesseltine, 1985). Like the case may be for other hospital infection control units elsewhere, Assiut University hospitals only focus on bacterial infection. This study was directed to examine the potential of the most common fungal species isolated from the atmospheric air and dust samples collected from air conditioners of ICUs and ORs to produce extracellular hydrolytic enzymes and mycotoxic compounds which are important virulence factors involved in fungal pathogenicity.

Materials and methods

Screening of fungal isolates for extracellular enzyme production

A total of 110 filamentous fungi isolated from air as well as filters of air conditioning systems in intensive care units and operation rooms (noted in our laboratory) were screened for their ability to produce extracellular enzymes in solid media. The following fungal species were tested: i.e. Aspergillus flavus (20 isolates), A. fumigatus (16), A. niger (19), Cladosporium cladosporioides ( 5 ), Fusarium solani (17), F. oxysporum (6), Myrothecium roridum (1) and Stachybotrys elegans (26).

Protease activity was determined using a Casein hydrolysis medium in which skim milk gives an opaque final appearance and hydrolysis of the casein resulted in a clear zone around the fungal colony. (Paterson & Bridge, 1994). Lipase activity was measured using the method of Ullman & Blasins (1974) with some modification this time using Tween 80 instead of Tween 20. The lipolytic producing ability was observed as a visible precipitate due to the formation of crystals of calcium salt of the oleic acid liberated by the enzyme. Urease activity was determined using urease medium described by Paterson & Bridge (1994). Isolates capable of producing urease turned the yellow color of the acidic medium to purple-red or deep pink color., meanwhile hemolytic activity of fungal isolates was measured using human blood agar medium (Ronald, 2000).

Screening of fungal isolates for mycotoxin production

Cultivation of fungal isolates and extraction of their mycotoxins

One-hundred and ten isolates were cultivated in a 15 cm Petri dish containing solid Czapek’s glucose agar under aseptic conditions and incubated at 25 ±2°C for 10 days. The plates containing Fusarium, Stachybotrys and Myrothecium isolates were transferred into a refrigerator for another 10 days. At the end of incubation periods, an agar plug technique was employed for the extraction of mycotoxins in culture materials, whereby, all the agar medium with fungal mycelia were cut into small pieces, transferred into a 250 ml Erlenmeyer flask containing 50 ml 96% methanol. The content was shaken on a rotary shaker (200 r.p.m., 24 h) and filtered through filter paper (Aboul-Nasr; Obied-Allah, 2013).

The extracted material was then washed using 25 ml of the same extractin solvent. The methanol extracts were combined, dried over anhydrous sodium sulphate, and concentrated under a vacuum. The residue was transferred to a dram vial and further evaporated to near dryness.

Thin layer chromatographic analysis

For the screening of mycotoxins in extracts, a thin-layer chromatographic technique adopted by El- kady and Moubasher (1982) was employed.

Results and discussion

The ability of clinical fungal strains from various ICUs and ORs at Assiut University hospital units were tested for their ability to produce extracellular enzymes in solid media and data presented in Table 1. Data indicated that more than 66% of tested isolates (73 out of 110) of five fungal genera; 3 Aspergillus spp. (55 isolates), one Cladosporium sp. (5 isolates), 2 Fusarium spp. (23 isolates), one Stachybotrys sp. (26 isolates) and one isolate of Myrothecium sp. had the ability to produce protease. Nearly similar percent (70.9%) of the tested fungal isolates (78 out of 110) were recorded as lipase producers in this study. Salyers and Witt (1994) reported that microbial cells secrete hydrolytic enzymes that destroy the constituents of host cell membranes leading to membrane dysfunction, physical disruption as well as aid in the invasion of host tissues. Proteolytic degradation of lung tissues has been suggested as one of the key events involved in the physiopathology of A. fumigatus (Kothary et al., 1984). Also, several species of Aspergillus such as A. fumigatus, A. flavus, A. oryzae and A. sojae are known to secrete protease as reported by Monod et al., (1993). Stehr et al., (2003) found that extracellular lipases play a role during microbial infections and suggested their role is to digest lipids for nutrient acquisition by pathogenic microbe and that these enzymes help the microbe (bacteria or fungi) to grow in environments where lipids are the sole carbon source.

Table 1 Extracellular enzymes produced by the tested fungal isolates collected from ICUs and ORs at Assiut University hospitals

A majority of the fungal isolates under study (92 out of 110: 83.6%) were able to produce urease. Urease catalyses the hydrolysis of urea to ammonia and carbamate, in which the latter by-product is further hydrolyzed to ammonia and carbonic acid resulting in an increase in pH (Zimmer, 2000). Urease activity has been found in several bacteria and fungi and has been shown to be an important pathogenic factor (Eaton et al., 1991; Cox et al., 2000). It has also been postulated that much of the tissue damage induced by Helicobacter pylori is as a result of ammonium hydroxide produced through the actions of urease. Studies have shown that the actions of urease may alter the function of white blood cells (Mai et al., 1992 ; Mobley, 1996). In this study, about 70.9% of the tested fungal isolates (78 out of 110) exhibited a lysis activity (heamolysis) on human blood. Vesper et al. (1999; 2001) isolated stachylysin a hemolytic agent from Stachybotrys chartarum. ( Donohue et al., 2004) isolated chrysolysin another hemolytic agent from P. chrysogenum.

The toxigenic potentials of these fungal isolates previously tested herein for their enzymatic activity were also evaluated and the data presented in Table 2 revealed that 79 out of the 110 tested fungal isolates (71.82%) were recorded as mycotoxin producers. Several mycotoxins including aflatoxins, gliotoxin, fumigillin, cladosporin, T-2 toxin, zearalenone, roridins, verrucarins, trichoveroides and satratoxins were produced by different fungal isolates in this study. Aflatoxins B1 & B2 were recorded in extracts obtained from cultures of 11 A. flavus with one positive isolates being able to produce additionally aflatoxins G1 & G2. Aflatoxins are produced by many strains of A. flavus. They are toxic, having carcinogenic, mutagenic and teratogenic effects in laboratory animals (Abdel-Wahhab et al., 1998 2006). Aflatoxin B1 is the most potent carcinogenic substance naturally produced mainly by A. flavus (Squire, and A. parasiticus 1981) and is classified by the International Agency of Research on Cancer as a group 1 human carcinogen (IARC, 1982). Gliotoxin and fumigillin were produced by all the 16 tested isolates of A. fumigatus. Also, 7 out of 19 tested isolates of A. niger had the ability to produce gliotoxin. Aspergillus members especially A. fumigatus and A. niger are the most common causal agents of aspergillosis. Invasive aspergillosis is very common among immuno-compromised patients, with reported incidence rates of 17-26% among lung transplants patients, 5-15% allogenic bone marrow transplants patients, 5-24% of those with acute leukaemia and 2-13% heart transplants patients (Curtis et al., 2004). Kupfahl et al., (2008) investigated the presence of gliotoxin-producing Aspergillus strains among clinical isolates collected from different parts of Germany and Austria. In that light, we collected and examined 158 different Aspergillus isolates consisting of 100 A. fumigatus, 27 A. terrus, 15 A. flavus and 16 A. niger strains from different medical centers and other environmental samples. According to that study, gliotoxin was recovered from 98, 56, 37 and 13% of A. fumigatus, A. niger, A. terreus and A. flavus, respectively. Nielsen (2003) found that A. fumigatus and A. niger are frequently isolated as indoor moulds, with the former isolate having the ability to produce fumitoxins, fumitremergens, gliotoxin and other mycotoxins, while the later produced only ochratoxin A. Cladosporin was produced by five tested isolates of C. cladospoioides in this study. This species is one of the causative agents of skin lesions, keratitis, nail fungus and pulmonary infections. Also, acute symptoms of exposure to this fungus are edema and bronchiospasr which may lead to pulmonary amphysema. Zearalenone was produced by all six tested isolates of F. oxysporum and three out of 17 isolates of F. solani. This toxin has an estrogenic activity and this estrogenic property enables exposure to its products a concern for human health (Niyo et al., 1988, Richard, 1991). In humans, the major effect of zearalenone bears on the reproductive system affecting reproductive organs' structure and function that may lead to hyperestrogenism (Kuiper-Goodman et al., 1993). T-2 toxin productivity by 11 of the 17 tested F. solani isolate was recorded in this study. This toxin is a representative of a large group of non-macrocyclic trichothecenes whose major effect and that of other trichothecenes is their ability to inhibit protein synthesis which is followed by a secondary disruption of DNA and RNA synthesis (Niyo et al., 1988; Richard, 1991). Verrucarin A & J as well as roridin A & E are mycotoxins produced by as M. roridium found in this study. Also, verrucarin J was produced by 11 out of 26 tested isolates of S. elegans (Eppley, with 5 of this species found to produce satratoxins H & E. Meanwhile 19 of the same species were able to synthesize trichoveroides.Verrucarins, roridins, trichoveroides and satratoxins. Different types of macrocyclic trichothecenes produced mainly by Stachybotrys 1977; Eppley and Bailey, 1973; Eppley et al., 1980). The involvement of macrocyclic trichothecenes in stachybotryotoxicosis were suggested by isolation of satratoxins from straws fed to sheep and cattle with stachybotryotoxicosis (Harrach and Bata, 1983; Harrach et al., 1983). Bata et al. (1985) found that all 17 strains of Stachybotrys atra ( isolated in Middle Europe and found to produce each of the five macrocyclic trichothecenes that included satratoxins H & G, verrucarin A, E & J, trichoveroides and roridin A & E. Islam et al., 2006) suggested that neurotoxicity and inflammation in the nose and brain are potential adverse health effects of exposure to satratoxins.

Table 2 Mycotoxigenicity of fungal isolates collected from ICUs and ORs at Assiut University hospital


In conclusion, hydrolytic enzymes and mycotoxic compounds which are considered the most important virulence factors influencing the pathogenicity of opportunistic fungal infections were detected in most of the cultures of fungal isolates tested herein. Thus the personnel managing the infection control unit of Assiut University hospitals must be aware of not only bacterial contamination, but there is a potential for the distribution of fungal infection as well.


  1. Abdel-Wahhab MA, Nada SA, Farag IM, Abbas NF, Amra HA: Potential protective effect of HSCAS and bentonite against dietary aflatoxicosis in rat: with special reference to chromosomal aberrations. Nat J Toxins 1998, 6: 211-218. 10.1002/(SICI)1522-7189(199809/10)6:5<211::AID-NT31>3.0.CO;2-8

  2. Abdel-Wahhab MA, Ahmed HH, Hagazi MM: Prevention of aflatoxin B1-initiated hepatotoxicity in rat by marine algae extracts. J Appl Toxicol 2006, 26: 229-238. 10.1002/jat.1127

  3. Aboul-Nasr MB, Obied-Allah MR: Biological and Chemical Detection of Fumonisins Produced on Agar Medium by Fusarium verticillioides Isolates Collected from Corn in Sohag-Egypt. J Microbiol 2013. Epub ahead of print

  4. Alberti C, Bouakline A, Ribaud P, Lacroix C, Rousselot P, Leblanc T: Relationship between environmental fungal contamination and the incidence of invasive aspergillosis in haematology patients. J Hosp Infect 2001, 48: 198-206. 10.1053/jhin.2001.0998

  5. Bata A, Balazs H, Ujszaszi K, Kis-Tamas A, Lasztity R: Macrocyclic trichothecene toxins produced by Stachybotrys atra strains isolated in Middle Europe. J Appl & Environ Microbiol 1985, 49(3):678-681.

  6. Birch M, Denning DW, Robson GD: Comparison of extracellular phospholipase activities in clinical and environmental Aspergillus fumigatus isolates. J Med Mycol 2004, 42: 81-86. 10.1080/13693780310001610029

  7. Borg M, Ruchel R: Expression of extracellular acid proteinase by proteolytic Candida species during experimental infection of oral mucosa. J Infect Immun 1988, 56: 626-663.

  8. Cox GM, Mukherjee J, Cole GT, Casadevall A, Perfect JR: Urease as a virulence factor in experimental cryptococcosis. J Infect Immun 2000, 68: 443-448. 10.1128/IAI.68.2.443-448.2000

  9. Curtis MS, Allen CIH, Lieberman MD, Martha SMD, William R, Marsha VMD: Adverse Health Effects of Indoor Mould. Aust College of Nutri & Environ Medicine 2004, 23(1):3-8.

  10. Da Silva BCM, Auler ME, Ruiz LS: Trichophyton rubrum isolated from AIDS and human immunodeficiency virus-infected patients in São Paulo, Brazil: antifungal susceptibility and extracellular enzyme production. J Chemotherapy 2005, 51: 21-26. 10.1159/000084019

  11. Donohue M, ChungY MML, Ward M, Selgrade MJ, Vesper SJ: Hemolysin Chrysolysin from Penicillium chrysogenum promotes inflammatory response. Int J Hyg Environ Health 2004, 208(4):279-85.

  12. Eaton KA, Brooks CL, Morgan DR, Krakowka S: Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. J Infect Immun 1991, 59: 2470-2475.

  13. El-Kady , Moubasher MH: Toxigenicity and toxin of Stachybotrys chartarum isolates from wheat straw samples in Egypt. J Exp Mycol 1982, 6: 25-31. 10.1016/0147-5975(82)90060-3

  14. Ellis D: The Human Opportunistic Mycoses. J Clin Mycol 1994, 36(1):166.

  15. Eppley RM: Mycotoxins in human and animal health. Park Forest South, Ill. V. Rodricks: Pathotox Publishers; 1977:285-293.

  16. Eppley RM, Bailey WJ: 12, 13 Epoxy-A9-trichothecenes as the probable mycotoxins responsible for stachybotryotoxicosis. J Sci 1973, 191: 758-760.

  17. Eppley RM, Highet RJ, Bailey WJ: Structure of satratoxin H, a metabolite of Stachbotrys atra application of proton and carbon – 13 nuclear magnetic resonance. J Org Chem 1980, 42: 240-243.

  18. Faure O, Fricker-Hidalgo H, Lebeau B, Mallaret MR, Ambroise-Thomas P, Grillot R: Eight year surveillance of environmental fungal contamination in hospital operating rooms and haematologic units. J Hosp Infect 2000, 50: 155-160.

  19. Hanzi M, Shimizu M, Hearn VM, Monod M: A study of alkaline protease secreted by different Aspergillus species. J Myco 1993, 36: 351-356.

  20. Harrach B, Bata A, Bajmoczy E, Benko M: Isolation of satratoxins from the bedding straw of a sheep-flock with fatal stachybotryotoxicosis. J Appl Environ Microbiol 1983, 45: 1419-1422.

  21. Hesseltine CW: Global significance of mycotoxins. In J Mycotox and Phyco- toxins. Edited by: Steyn PS, Vleggaar R. Elsevier Scientific Publishing Co., Amsterdam; 1985:1-18.

  22. Hussein HS, Brasel JM: Toxicity, metabolism, and impact of mycotoxins on humans and animals. J Toxicol 2001, 167(2):101-134. 10.1016/S0300-483X(01)00471-1

  23. Ibrahim AS, Mirbod F, Filler SG, Banno Y, Cole GT, Kitajima Y, Edwards JE Jr, Nozawa Y, Ghannoum MA: Evidence implicating phospholipase as a virulence factor of Candida albicans . J Infect Immun 1995, 63: 1993-1998.

  24. International Agency for Research on Cancer (IARC): The evaluation of the carcinogenic risk of chemicals to humans. Monograph Supplement 4. International Agency for Research on Cancer, Lyon, France; 1982.

  25. Islam J, Harkema R, Pestka JJ: Satratoxin G from the Black Mold Stachybotrys chartarum Evokes Olfactory Sensory Neuron Loss and Inflammation in the Murine Nose and Brain. J Environ Health Perspect 2006, 114: 1099-1107. 10.1289/ehp.8854

  26. Keller NP, Turner G, Bennett JW: Fungal secondary metabolism – from biochemistry to genomics. J Nat Rev Microbiol 2005, 3(12):937-947. 10.1038/nrmicro1286

  27. Kothary MH, Chase T Jr, MacMillan JD: Correlation of elastase production by some strains of Aspergillus fumigatus with ability to cause pulmonary invasive Aspergillosis in mice. J Infect Immun 1984, 43: 320-325.

  28. Kuiper-Goodman T: Chapter 1. Risk assessment and risk manage- ment of mycotoxins in food. Edited by: Mogan N, Olsen M. Mycotoxins in Food, Detection and Control. CRC Press, New York; Wood head Publishing Limited, Cam- bridge, England; 2004:3-31.

  29. Kuiper-Goodman T, Ominiski K, Marquardt RR, Malcolm S, McMullen E, Lombaert GAE, Morten T: Estimating human exposure to ochratoxin A in Canada. In Human Ochratoxicosis and Its Pathologies, Montrouge. Edited by: Creppy E, Dirheimer G. John Libbey, Eurotech, London; 1993:167-74.

  30. Kupfahl AM, Cornelia LF, Guido F, Gerhard H, Thomas R, Gernot G, Herbert H: Gliotoxin production by clinical and environmental Aspergillus fumigatus strains. Med Microbiol 2008, 298(3–4):319-327.

  31. Kwon-Chung KJ, Bennett JE: Mycosis. J Med Mycol, Lea & Febiger, Philadelphia 1992, 31(1):560-593.

  32. Mai UEH, Perez-Perez GI, Allen JB, Wahl SM, Blaser MJ, Smith PD: Surface proteins from Helicobacter pylori exhibit chemotactic activity for human leukocytes and are present in gastric mucosa. J Exp Med 1992, 175: 517-525. 10.1084/jem.175.2.517

  33. Marc Z: Molecular mechanics evaluation of the proposed mechanisms for the degradation of urea by urease. J Biomol Struct Dyn 2000, 17(5):787-97. 10.1080/07391102.2000.10506568

  34. Mobley HL: The role of Helicobacter pylori urease in the pathogenesis of gastritis and peptic ulceration. J Aliment Pharmacol Ther 1996, 10: 57-64.

  35. Monod M, Paris S, Sarfati J, Jaton-Ogay P, Ave P, Latge´ JP: Virulence of alkaline protease-deficient mutants of Aspergillus fumigatus . FEMS Microbiol. Letters 1993, 106: 39-46. 10.1111/j.1574-6968.1993.tb05932.x

  36. Monod M, Capoccia S, Lechenne B: Secreted proteases from pathogenic fungi. Int Med J Microbiol 2002, 292: 405-419. 10.1078/1438-4221-00223

  37. NAS: Pesticides in the Diets of Infants and Children. National Academy Press, Washington, DC; 1993:253-258.

  38. Nielsen KF: Mycotoxin production by indoor molds. Fungal Genet Biol 2003, 39: 103-117. 10.1016/S1087-1845(03)00026-4

  39. Niyo KA, Richard JL, Tiffany LH: Effect of T-2 mycotoxin ingestion on phagocytosis of Aspergillus fumigatus conidia by rabbit alveolar macrophages and on hematologic, serum biochemical, and pathologic changes in rabbits. J Vet Res 1988, 49: 1766-1773.

  40. Pasqualotto AC: Differences in pathogenicity and clinical syndromes due to Aspergillus fumigatus and Aspergillus flavus . J Med Mycol 2008, 47(1):1-10.

  41. Pasqualotto AC, Denning DW: Post-operative aspergillosis. Clinic Microbiol Infect 2006, 12: 1060-1076. 10.1111/j.1469-0691.2006.01512.x

  42. Paterson RRM, Bridge PD: Biochemical techniques for filamentous fungi. Int J Mycol Instit 1994, 1: 21.

  43. Perdelli F, Cristina ML, Sartini M, Spagnolo AM, Dallera M, Ottria G: Fungal contamination in hospital environments. J Infect Cont Hosp Epidemiol 2006, 27: 44-47. 10.1086/499149

  44. Pitt JI: What are mycotoxins? Austral. Mycotoxin Newsletter 1996, 7(4):1-3.

  45. Richard J: Mycotoxins as immunomodulators in animal systems. In Mycotoxins, Cancer, and Health. Edited by: Bray GA, Ryan DH. Pennington Center Nutrition Series. Louisiana State University Press, Baton Rouge, LA; 1991:197-220.

  46. Rippon JW: The Pathogenic Fungi and the Pathogenic Actinomycetes, 3rd ed., WB Saunders, Philadelphia, 3rd ed. J Med Mycol 1988, 797.

  47. Ronald MA: Hand book of Microbiological Media. 10th edition. CRC press, Inc, USA; 2000:137,333,785,279.

  48. Salyers A, Witt D: Virulence factors that damage the host. Bacterial pathogenesis: a molecular approach. ASM Press, Washington, D.C; 1994:47-62.

  49. Sharma RP: Immunotoxicity of mycotoxins. J Dairy Sci 1993, 76: 892-897. 10.3168/jds.S0022-0302(93)77415-9

  50. Singh N, Paterson DL: Aspergillus infections in transplant recipients, Review. J Clin Microbiol 2005, 18: 44-69. 10.1128/CMR.18.1.44-69.2005

  51. Squire RA: Ranking animal carcinogens: a proposed regulatory approach. Sci 1981, 214: 877-880. 10.1126/science.7302565

  52. Stehr F, Kretschmar M, Kroger C, Hube B, Schafer W: Microbial lipases as virulence factors. Molecular Catalysis, B: Enzymatic 2003, 22: 347-355. 10.1016/S1381-1177(03)00049-3

  53. Ullman V, Blasins G: A simple medium for the detection of different lipolytic activity of microorganisms. Zentrabl Bakteriol J Hyg II Abt A 1974, 229: 264-267.

  54. van Egmond HP, Speijers GA: Natural toxins I. Mycotoxins. In International Food Safety Handbook, Science, International Regulation, and Control. Edited by: van der Heijden K, Younes M, Fishbone L, Miller S. Marcel Dekker, Inc,New York, Basel; 1999:342-355.

  55. Vesper SJ, Dearborn DG, Yike I, Sorenson WG, Haugland RA: Hemolysis, toxicity, and randomly amplified polymorphic DNA analysis of Stachybotrys chartarum strains. J Appl Environ Microbiol 1999, 65: 3175-3181.

  56. Vesper SJ, Magnuson S, Dearborn D, Yike I, Haugland RA: Initial characterization of the hemolysin from Stachybotrys chartarum . J Infect Immun 2001, 69: 912-916. 10.1128/IAI.69.2.912-916.2001

  57. Vonberg RP, Gastmeier P: Nosocomial aspergillosis in outbreak settings. J Hosp Infect 2006, 63: 246-254. 10.1016/j.jhin.2006.02.014

  58. WHO (Environmental Health Criteria): Principles for evaluating health risks from chemicals during infancy and early childhood; the need for a special approach. IPCS, Geneva; 1986.

Download references

Author information



Corresponding author

Correspondence to Mohamed Bassam Aboul-Nasr.

Additional information

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

MBA designed the research plan, followed the research plan execution point by point, helped in drafting the manuscript, revised it and was the corresponding author. AAZ helped in identifying the toxic profile and planed the enzyme profile experiments. EMA carried out the research plane point by point, identifying fungi and toxins under the supervision of MBA and helped in drafting the manuscript. All authors read and approved the final manuscript.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reprints and Permissions

About this article

Cite this article

Aboul-Nasr, M.B., Zohri, A.A. & Amer, E.M. Enzymatic and toxigenic ability of opportunistic fungi contaminating intensive care units and operation rooms at Assiut University Hospitals, Egypt. SpringerPlus 2, 347 (2013).

Download citation


  • Airborne fungi
  • Enzymes
  • Mycotoxins and pathogenicity