MYCOBIOTA ASSOCIATED WITH CAMEL HAIR AT TAIZ CITY, YEMEN الفطريات المصاحبة لشعر الجمال بمدينة تعز- اليمن

Document Type : Original Article

Abstract

ABSTRACT:
The mycobiota of 50 camel hair samples collected from different localities in Taiz city were estimated using the soil plating technique and Sabouraud''s dextrose agar at 28°C. Forty-three species belonging to 15 genera were collected. The most prevalent genera were: Chysosporium, Aspergillus and Scopulariopsis. Some dermatophytic species were also recovered and these were represented by Microsporum canis, M. gypseum Trichophyton rubrum and T. verrucosum. Camel hair seem to represent an adequate reservoir for several pathogenic fungi.
الملخص العربي :
استهدف البحث التعرف على الأحياء الفطرية لخمسين عينة من شعر الجمال جمعت من أماکن مختلفة من مدينة تعز وذلک باستخدام طريقة مصائد التربة والوسط الغذائي سبارود اجار والتحضين عند درجة حرارة 28°موقد  تم عزل34 نوعاً فطرياً تنتمي إلى 15 جنساً وکان أکثر الأجناس شيوعاً وانتشاراً هو جنس کريزوسبورم يليه اسبرجلس ثم جنس اسکوبيولاريوبيسس کما تم أيضاً عزل أنواع من الفطريات الجلدية تنتمي إلي الميکروسبورم والتريکوفيتون ولوحظ أن العديد من الفطريات المعزولة يمکن أن تکون ممرضة للإنسان. 

Highlights


Ass. Univ. Bull. Environ. Res. Vol. 17 No. 2 October   2014

 

 

 

AUCES

 

MYCOBIOTA ASSOCIATED WITH CAMEL HAIR AT TAIZ CITY, YEMEN

  1. M. H. Sallam*, Gamal A. AL-Ameri**

Applied Microbiology Department, Faculty of Science*, Microbiology Department, Faculty of Medicine**,Taiz University, Taiz, Yemen

 

ABSTRACT:

                     The mycobiota of 50 camel hair samples collected from different localities in Taiz city were estimated using the soil plating technique and Sabouraud''s dextrose agar at 28°C. Forty-three species belonging to 15 genera were collected. The most prevalent genera were: Chysosporium, Aspergillus and Scopulariopsis. Some dermatophytic species were also recovered and these were represented by Microsporum canis, M. gypseum Trichophyton rubrum and T. verrucosum. Camel hair seem to represent an adequate reservoir for several pathogenic fungi.

Kew words: Animal hairs, dermatophytes, keratinophilic fungi, camel .  

 


INTRODUCTION:

     Animals are known to play an important role in the epidemiology of both animal and human mycoses. They can act as a reservoir or vectors for these diseases (Rippon, 1982; Ogbonna et al., 1986; and Ali- Shtayeh et al., 1989).  

      Keratinophilic fungi have received considerable attention in recent years. These organisms include dermatophytes which are able to degrade various types of keratinous substances. These substances occurr in nature mainly in the form of hairs, wools, feathers, horns, hooves, nails, skin and other cornified appendages and constitute natural baits for these keratonophilic fungi (Khanam and Jain, 2002; Singh et al., 2009).

       Keratinophilic fungi include a variety of filamentous fungi belonging mainly to hyphomycetes and several other taxonomic groups. Hyphomycetes include dermatophytes and a great variety of non- dermatophytic filamentous fungi (Mukesh and Sharma, 2010). Keratinophilic fungi can be considered as potential pathogens (Marcella and Mercantini, 1986).

Several studies have been conducted on mycobiota associated with hair of different kinds of animals in many parts of the world (Moses and Sunday, 2001; Shukia, et al. 2003; Periasamy et al., 2004; Dobrowolska et al., 2006; Ulfig, 2007; Maghraby et al., 2008; Mandeel et al., 2009; Nichita and Marcu, 2010; Rostami, et al., 2010; Sallam and Alkolaibe, 2010;  Shokri and Khosravi, 2011; and Kraemer et al., 2012) .

In Yemen there are no records available on dermatophytes and keratinopilic fungi associated with camel hair. The aim of the present work was to survey those fungi and identify the mycobiota associated with camel hair which might be causal agents for human mycosis..

 

MATERIALS AND METHODS:

The areas of study:

Hair-baiting technique was used for isolation of keratinophilic fungi as employed by Ress (1967) with some modifications. Fifty samples of camel hair were collected from different localities at Taiz city, Yemen during the period from October 2011 to December 2012.  These samples were placed in clean plastic bags and transferred immediately to the laboratory. Five hair segments were placed on dry sterile clay soil (25- 50 g) in each sterile Petri-dish (3 plates for each sample) moistened with sterilized distilled water (20-25% moisture content) and remoistened whenever necessary. The plates were incubated at 28ºC for 10-12 weeks. The moulds which appeared on hair fragments were transferred to the surface of Sabouraud''s dextrose agar medium (Moss and McQuown, 1969), supplemented with chloramphenicol (0.5 mg/ml) and cyclohexamide (0.5 mg/ml). Cultures were then incubated at 28ºC for 2-3 weeks and the developing fungi were counted, identified (based on morphological and microscopic characters) following the keys of Moubasher (1993) and de Hoog et al. (2000). Fungal colonies were calculated per 15 hair fragments for each sample.

Results and Discussion :

 

A total of 34 species appertaining to 15 genera were recovered from camel hair samples (Table 1). These fungi included dermatophytes such as Trichophyton, and Microsporum, as well as true keratinophilic fungal species belonging to Chrysosporium and Scopulariopsis. Other cycloheximide- resistant were also recorded.

Chrysosporium was the most frequent genus being recovered from 62% of samples and representing 41% of all fungal isolates. This genus was also isolated from goat and sheep hairs in Libya  by El-Said et al. (2009) who found that Chrysosporium was recorded in 92% and 96% of the samples and 91.2% and 87.8% of the total fungi of goat and sheep hairs, respectively.In Egypt,  Bagy and Abdel-Hafez (1985) indicated also that Chrysosporium was the most frequent genus of the camel (98.3%) and goat (91.7%) hair samples from Al-Arish. Also, Abdel-Gawad (1997) observed that Chrysosporium was the most common fungus on sheep wool. In Italy, Marcella et al. (1985) found that, out of 115 animals examined, 54 presented keratinophilic fungi of which Chrysosporium spp. were the most common. In the current study Chrysosporium was represented by four species, of which C. tropicum was the most frequent. It was found in 46% of the samples, and comprised 23% of all isolates. The remaining Chrysosporium species (C. indicum, C. keratinophilum, and C. georgii) were isolated in low frequency of occurrence. They were identified from 38%, 32% and 28% of the samples, constituting 10.4%, 4.5% and 2.4% of the total fungi, respectively (Table1). This is in agreement with the results obtained from sheep wool in Egypt by Abdel-Gawad (1997) who reported that C. tropicum was the most common species occurring in 58% of the samples. Ali-Shtayeh et al. (1988a) observed that C. keratinophilum and C. tropicum were found respectively in 7.9% and 6.7% of goat hairs from West Bank of Jordan. Deshmukh (2004) reported that C. indicum was the most common species in feathers of pigeon and was represented in 24% of the samples. The above species and other Chrysosporium spp. were also isolated but with different frequencies from animal hairs (Deshmukh, 2004; Mandeell, et al. 2009 and Dokuzeylul et al. 2013) .

Aspergillus was the second most frequent genus on camel hair, contaminating 48% of the samples matching 24.8% of total fungi. It was represented by 7 species of which A. flavus and A. niger were the most prevalent species (22 & 32% of samples and 5.7% & 11.7 % of total fungi). A. ustus (12% of the samples), A. terreus (8%), A. ochraceus (6%), A. fumigatus and A. wentii (4% each) were isolated in rare frequency of occurrence (Table 1).In Egypt,  Barakat and El-Shanawany (1998) reported that Aspergillus was the second most frequent genus on the hair of donkey. They noticed that A. fumigatus, A. sydowii, and A. versicolor were the most common species. Also, these Aspergillus species have been reported from hairs of camel, cow, donkey and goat in Egypt (Bagy and Abdel-Hafez, 1985; Bagy, 1986), from hair of cows, donkeys, goats, rabbits, cats and dogs in the west bank of Jordan (Ali Shtayeh et al. 1988a,b) and from hair of goats and wool of sheep inYemen (Sallam and Alkolaibe 2010)

In the present study , Scopulariopsis (2 species) occupied the third place in the number of cases of isolation. It was isolated from 28% of samples comprising 8% of total fungi. From the two species isolated S. brevicaulis was the most prevalent while, S. candida was less frequent (Table 1). Several authors reported the prevalence of Scopulariopsis species on hairs of camel (Bagy and Abdel-Hafez, 1985, Nasser et al. 1998; Shokri and Khosravi, 2011) as well as on other animals and birds in Portugal (Bernardo et al. 2005), Bahrin (Mandeell et al. 2009), and Iran (Rostami et al. 2010).

Emericella (2 species), Penicillium (3), Acremonium (2) and Geotrichum (1) were isolated from 7 or 8 samples (out of 50) contributing 3.4%, 2.8%, 3.6% and 1.9% of total fungi, respectively. From the above genera E. nidulans, P. chrysogenum, A. strictum and G. candidum were the most common species.

Dermatophytes represented by two genera (Microsporum and Trichophyton) were recovered from 7 samples, matching 1.2% and 1.1% of total fungi, respectively. From these genera, M. canis, M. gypseum, T. rubrum and T. verrucosum were identified in rare occurrence. These species were also isolated with different frequencies from hair of different animals as reported by Prado et al. (2008); Madhavi et al. (2011); Gangil et al. (2012); Dokuzeylul et al. (2013) and Mohammed (2013).

Alternaria (2 species), Chaetomium (2), Fusarium (3), Paecillomyces (1) and Thermoascus (1) were isolated in rare frequency of occurrence. They emerged in 8-10% of the samples, accounting collectively 8.6% of total fungi (Table1). These species were also isolated in different frequencies from various keratinous substrates as reported by several authors (Bagy, 1986: Sallam and Alkolaibe, 2010: and Mohammed, 2013).

Conclusion

The present study gives an insight on the mycobiota of camel hair in Taiz, Yemen. The prevalence of dermatophytes and non-dermatophytes emphasises that camels have a potentiality for shedding fungi in the environment and serve as reservoirs for human pathogens.


 


Table (1): fungi isolated from camel hair (out of 50) samples using

soil- plating technique on Saubroud''s dextrose agar at 28ºC.

Genera & Species

TC

 

NCI & OR

 

Acremonium

    A. rutilum W. Gams

    A. strichum W. Gams

Alternaria

    A. alternata (Fr.) Keissler

    A. tenuissima (Kunze) Wiltshire

Aspergillus                                                                           

    A. flavus  link

    A. fumigatus Fresenius

    A. niger  van Tieghem

    A. terreus Thom

    A. ochraceus Wilhelm

    A. ustus (Bain.) Thom & Church

    A. wentii Wehmer

Chaetomium

C. globosum kunze

C. spirale Zopf

Chrysosporium 

C. indicum (Rand. & Sand.) Garg

C. keratinophilum D.Frey ex Carm.

C. tropicum Carmichael

C. georgii (Vars. & Ajello) Oorcshot

Chrysosporium sp.

Emericella

E. nidulans (Eidam.) Vuill.

E. ruglosa (Thom & Raper) Benjamin

Fusarium

F. verticillioides (Saccardo)Nirenberg

F. oxysporum Schlecht.

F. solani (Mart.) Sacc.

Geotrichum candidum Link

Microsporum

M. canis Bodin

M. gypsum (Bodin) Gulart & Grigorakis

Mucor hiemalis Wehmer

Paecillomyces lilacinus (Thom) Samson

Penicillium

P. chrysogenum Thom

P. funiculosum Thom

Penicillium sp.

Scopulariopsis

S. brevicaulis (Sacc.) Bain.

S. candida (Gueguen) Vuillemin

Thermoascus aurantiacus Miehe

Trichophyton

T. rubrum (Castellani) Sabouraud

T. verrucosum Bodin

Sterile mycelia

    27

     8

    19

    18

    13

5

188

43

5

89

16

14

18

3

24

19

5

311

79

34

173

18

                       7

26

22

4

13

7

3

3

14

9

6

3

5

4

21

16

2

3

77

61

16

6

8

2

6

8

 

7 L

3 R

4 R

5 R

4 R

3 R

24 M

11 L

2 R

16 M

4 R

3 R

6 R

2 R

5 R

4 R

3 R

31 H

19 M

16 M

23 M

14 M

6 R

8 L

6 R

2 R

6 R

4 R

2 R

2 R

7 L

7 L

5 R

2 R

3 R

4 R

8 L

4 R

2 R

3 R

14 L

10 L

6 R

5 R

7 L

2 R

5 R

7 L

 

Gross total counts

759

 

No. of genera

15

 

 

No. of species

34

 

  TC= Total count; NCI= number of cases of isolation; OR= occurrence remark: H= high occurrence, 25-50 (out of 50) cases; M= moderate occurrence, 13- 24 cases; L= low occurrence, 7- 12 cases; R= rare occurrence, 1-6 cases.

 

References

Abdel-Gawad, K. M. (1997): Mycological and some physiological studies of keratinophilic and other moulds associated with sheep wool. Microbiol. Res. 152: 181-188.

Ali-Shtayeh, M. S.; Arda, H. M.; Hassouna, M. and Shaheen, S. F. (1988a): Keratinophilic fungi on the hair of goats from the West Bank, Jordan. Mycopathologia 104: 103-108.

Ali-Shtayeh, M. S.; Arda, H. M.; Hassouna, M. and Shaheen, S. F. (1988b): Keratinophilic fungi on the hair of cows, donkey, rabbits, cats and dogs from the West Bank Jordan. Mycopathologia 149: 193-121.

Ali-Shtayeh, M. S.; Arda, H. M.; Hassouna, M.; and Shaheen, S. F. (1989): Keratinophilic fungi on sheep hairs from West Bank of Jordan. Mycopathologia 106: 95-101

Bagy, M. M. K. and Abdel- Hafez, A. I. I. (1985): Mycoflora of camel and goat hairs from Al- Arish, Egypt. Mycopathologia 92: 125-128.

Bagy, M .M .K. (1986): Fungi on the hair of large mammals in Egypt. Mycopathologia 93: 73-75.

Barakat, A. and El-Shanawany, A. A. (1998): Studies on the mycoflora associated with donkey hair at Assiut. Assiut Vet. Med. J. 8(15-17): 283-294.

Bernardo, F.; Lanca, A.; Guerra, M. M. and Martins, H. M. (2005):  Dematophytes

 

isolated from pet, dogs and cats, in Lisbon, Portugal (2000-2004). Rev. Port. Cienc. Vet. 100: 85-88.

De Hoog G. S., Guarro J., Gene J. and Figueras M. J. (2000): Atlas of Clinical Fungi. Centraalbureau voor Schimmellcultures, Universitat Rovira I Virgili. Reus. Spain.

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Dobrowolskh, A.; Staczek, P.; Kaszuba, A. and Kozlowska, M. (2006): PCR-RFLP analysis of the dermatophytes isolated from patient in central Poland. J. Dermatological Science 42: 71-74.

Dokuzeylul, B.; Kahraman, B. B. and Sigirci, B. D. (2013): Dermatophytosis caused by a Chrysosporium species in two cats in Turkey: a case report. Veterinarni Medicina 58: 633-636.

El-Said, A. H. M.; Sohair, T. H. and El-Hadi, A. G. (2009): Fungi associated with the hairs of goat and sheep in Libya. Mycobiology 37(2): 82-89

Gangil, R.; Dutta, P. and Tripathi, R. (2012): Incidence of dermatophytosis in canine cases presented at Apollo Veterinary College, Rajashtan, India. Vet. World 5(11): 682-684.

Khanam, S. J. P. and Jain, P. C. (2002): Isolation of keratin degrading fungi from soil of Damoh, India. Asian J. Microbiol. Biotechnol. Environ. Sci. 4: 251-254.

Kraemer, A.; Mueller, R. S.; Werckenthin, C.; Straubinger, R. K. and Hein, J. (2012): Dermatophytes in pet Guinea pigs and rabbits . Veterinary Microbiology 157: 208-213.

Madhavi, S.; Rama, R. M. V. and Jyothsna, K. (2011): Mycological study of dermatophytosis in rural population. Annuals Biological Research 2(3): 88-93.

Maghraby, A. T.; Gherbawy, Y. A. M. H. and Hussein, A. M. (2008): Keratinophilic fungi inhabiting floor dusts of student houses at South Valley University in Egypt. Aerobiologia 24: 99-106.

Mandeel, Q.; Nardoni, S. and Mancianti, F. (2009): Keratinophilic fungi of feathers on common clinically healthy birds in Bahrain. Mycoses 54: 71-77

Marcella, R.; Mercantini, R.; Spinelli, P. and Volterra, L. (1985): Occurrence of keratinophilic fungi in animals of the zoological park of Roma. Mykosen 28: 507-512.

Marcella, R. and Mercantini, R. (1986): Keratinophilic fungi isolated from soils of the Abruzzo National Park, Italy.  Mycopathologia 94: 97-107.

Mohammed, S. J. (2013): Dermatophytes isolated from dogs suspected of dermatophytosis in Baghdad City. Diyala J. Pure Sci. 9(4): 61-66.

Moses, O. E. and Sunday, O. F. (2001): Occurrence of keratinophilic fungi and dermatophytes on birds in Nigeria. Mycopathologia 153: 87-89.

Moss, E. S. and McQuown, A. I. (1969): Atlas of medical mycology 3rded. The Williams and Wilkins Company, Baltimore U.S.A.

Moubasher A. H. (1993): Soil fungi in Qatar and other Arab countries. Scientific and Applied Research Center. University of Qatar,566 pp.

Mukesh, S. and Sharma, M. (2010): Incidence of dermatophytes and other keratiophilic fungi in schools and college playground soils of Jaipur, India. Afr. J. Microbial. Research 4(24): 2647-2654.

Nasser, L. A.; El-Shanawany, A. A. and Barakat, A. (1998): Ecological and physiological studies on fungi associated with camel hairs from Saudi-Arabia. Assiut Vet. Med. J. 8(15-17): 243-254.

Nichita, I. and Marcu, A. (2010): The fungal microbiota isolated from cats and dogs. Animal Science and Biotechnologies 43(1): 411-414.

Ogbonna, C. I. C.; Enweani, I. B. and Ogueri, S. C. (1986): The distribution of ringworm infections amongst Nigerian nomadic fulani herdsmen. Mycopathologia 96: 45-51.

Periasamy, A.; Hilda, A. and Subash, C. B. G. (2004): Keratinophilic fungi of poultry farm and feather damping soil in Tamil Nadu, India.  Mycopathologia 158: 303-309.

Prado, M .R.; Brilhante, R .S. M. and Cordeiro, R. A. (2008): Frequency of yeasts and dermatophytes from healthy and diseased dogs. J. Vet. Diagn. Invest. 20: 197-202.

Ress, R. G. (1967): Keratinophilic fungi from Queensland. 11. Isolation from animal hairs and scales. Sabouraudia 5: 165-172.

Rippon, J. W. (1982): The pathogenic fungi and the pathogenic actinomycetes. Philadelphia: W. B. Saunders Company.

Rostami, A.; Shirani, D.; Shokri, H.; Khosravi, A. R.; Daieghazvini, R. and Tootian, Z. (2010): Fungal flora of the hair coat of Persian squirrel (Sciurus anomalus) with and without skin lesion in Tehran, Iran. J. de Mycologie Medicale 20: 21-25.

Sallam, A. M. H. and Alkolaibe, A. M. (2010): Distribution pattern of other keratinophilic fungi on goats hair and sheep wool,Taiz city, Yemen. J. Environmental Sciences 39 (3): 345-356.

Shokri, H. and Khosravi, A. R. (2011): Fungal        

        flora isolated from the skin of healthy    

        dromedary camels Camelus dromedaries.    

        Int. J. Vet. Res. 5 (2): 109-112.

Shukia, P.; Shukla, C. B.; Kango, N. and Skukla, A. H. (2003): Isolation and characterization of a dermatophyte, Microsporium gypseum from soils of Rewa (Madhya Pradesh), India. Pak. J. Bio. Sci. 6: 622-625.

Singh, I.; Mishra, A. and Kushwaha, R. (2009): Dermatophytes, related keratinophilic and opportunistic fungi in indoor dust of houses and hospitals. Indian J. Med. Microbial. 27: 242-246.

Ulfig, K. (2007): Influence of peptone, ammonia, water and urea supplements on keratinolytic and associated non-keratinolytic fungi in sewage sludge. Int. Biodeterioration & Biodegradation 59: 62-68.


 

 

 

 

 

 

 

 

 

الملخص العربي

الفطريات المصاحبة لشعر الجمال بمدينة تعز- اليمن

علي محمد حسن سلام*    جمال العامري**

قسم الميکروبيولوجى التطبيقى - کلية العلوم * قسم الميکروبيولوجي کلية الطب**– جامعة تعز- اليمن

 

استهدف البحث التعرف على الأحياء الفطرية لخمسين عينة من شعر الجمال جمعت من أماکن مختلفة من مدينة تعز وذلک باستخدام طريقة مصائد التربة والوسط الغذائي سبارود اجار والتحضين عند درجة حرارة 28°موقد  تم عزل34 نوعاً فطرياً تنتمي إلى 15 جنساً وکان أکثر الأجناس شيوعاً وانتشاراً هو جنس کريزوسبورم يليه اسبرجلس ثم جنس اسکوبيولاريوبيسس کما تم أيضاً عزل أنواع من الفطريات الجلدية تنتمي إلي الميکروسبورم والتريکوفيتون ولوحظ أن العديد من الفطريات المعزولة يمکن أن تکون ممرضة للإنسان. 

Keywords



Ass. Univ. Bull. Environ. Res. Vol. 17 No. 2 October   2014

 

 

 

AUCES

 

MYCOBIOTA ASSOCIATED WITH CAMEL HAIR AT TAIZ CITY, YEMEN

  1. M. H. Sallam*, Gamal A. AL-Ameri**

Applied Microbiology Department, Faculty of Science*, Microbiology Department, Faculty of Medicine**,Taiz University, Taiz, Yemen

 

ABSTRACT:

                     The mycobiota of 50 camel hair samples collected from different localities in Taiz city were estimated using the soil plating technique and Sabouraud's dextrose agar at 28°C. Forty-three species belonging to 15 genera were collected. The most prevalent genera were: Chysosporium, Aspergillus and Scopulariopsis. Some dermatophytic species were also recovered and these were represented by Microsporum canis, M. gypseum Trichophyton rubrum and T. verrucosum. Camel hair seem to represent an adequate reservoir for several pathogenic fungi.

Kew words: Animal hairs, dermatophytes, keratinophilic fungi, camel .  

 


INTRODUCTION:

     Animals are known to play an important role in the epidemiology of both animal and human mycoses. They can act as a reservoir or vectors for these diseases (Rippon, 1982; Ogbonna et al., 1986; and Ali- Shtayeh et al., 1989).  

      Keratinophilic fungi have received considerable attention in recent years. These organisms include dermatophytes which are able to degrade various types of keratinous substances. These substances occurr in nature mainly in the form of hairs, wools, feathers, horns, hooves, nails, skin and other cornified appendages and constitute natural baits for these keratonophilic fungi (Khanam and Jain, 2002; Singh et al., 2009).

       Keratinophilic fungi include a variety of filamentous fungi belonging mainly to hyphomycetes and several other taxonomic groups. Hyphomycetes include dermatophytes and a great variety of non- dermatophytic filamentous fungi (Mukesh and Sharma, 2010). Keratinophilic fungi can be considered as potential pathogens (Marcella and Mercantini, 1986).

Several studies have been conducted on mycobiota associated with hair of different kinds of animals in many parts of the world (Moses and Sunday, 2001; Shukia, et al. 2003; Periasamy et al., 2004; Dobrowolska et al., 2006; Ulfig, 2007; Maghraby et al., 2008; Mandeel et al., 2009; Nichita and Marcu, 2010; Rostami, et al., 2010; Sallam and Alkolaibe, 2010;  Shokri and Khosravi, 2011; and Kraemer et al., 2012) .

In Yemen there are no records available on dermatophytes and keratinopilic fungi associated with camel hair. The aim of the present work was to survey those fungi and identify the mycobiota associated with camel hair which might be causal agents for human mycosis..

 

MATERIALS AND METHODS:

The areas of study:

Hair-baiting technique was used for isolation of keratinophilic fungi as employed by Ress (1967) with some modifications. Fifty samples of camel hair were collected from different localities at Taiz city, Yemen during the period from October 2011 to December 2012.  These samples were placed in clean plastic bags and transferred immediately to the laboratory. Five hair segments were placed on dry sterile clay soil (25- 50 g) in each sterile Petri-dish (3 plates for each sample) moistened with sterilized distilled water (20-25% moisture content) and remoistened whenever necessary. The plates were incubated at 28ºC for 10-12 weeks. The moulds which appeared on hair fragments were transferred to the surface of Sabouraud's dextrose agar medium (Moss and McQuown, 1969), supplemented with chloramphenicol (0.5 mg/ml) and cyclohexamide (0.5 mg/ml). Cultures were then incubated at 28ºC for 2-3 weeks and the developing fungi were counted, identified (based on morphological and microscopic characters) following the keys of Moubasher (1993) and de Hoog et al. (2000). Fungal colonies were calculated per 15 hair fragments for each sample.

Results and Discussion :

 

A total of 34 species appertaining to 15 genera were recovered from camel hair samples (Table 1). These fungi included dermatophytes such as Trichophyton, and Microsporum, as well as true keratinophilic fungal species belonging to Chrysosporium and Scopulariopsis. Other cycloheximide- resistant were also recorded.

Chrysosporium was the most frequent genus being recovered from 62% of samples and representing 41% of all fungal isolates. This genus was also isolated from goat and sheep hairs in Libya  by El-Said et al. (2009) who found that Chrysosporium was recorded in 92% and 96% of the samples and 91.2% and 87.8% of the total fungi of goat and sheep hairs, respectively.In Egypt,  Bagy and Abdel-Hafez (1985) indicated also that Chrysosporium was the most frequent genus of the camel (98.3%) and goat (91.7%) hair samples from Al-Arish. Also, Abdel-Gawad (1997) observed that Chrysosporium was the most common fungus on sheep wool. In Italy, Marcella et al. (1985) found that, out of 115 animals examined, 54 presented keratinophilic fungi of which Chrysosporium spp. were the most common. In the current study Chrysosporium was represented by four species, of which C. tropicum was the most frequent. It was found in 46% of the samples, and comprised 23% of all isolates. The remaining Chrysosporium species (C. indicum, C. keratinophilum, and C. georgii) were isolated in low frequency of occurrence. They were identified from 38%, 32% and 28% of the samples, constituting 10.4%, 4.5% and 2.4% of the total fungi, respectively (Table1). This is in agreement with the results obtained from sheep wool in Egypt by Abdel-Gawad (1997) who reported that C. tropicum was the most common species occurring in 58% of the samples. Ali-Shtayeh et al. (1988a) observed that C. keratinophilum and C. tropicum were found respectively in 7.9% and 6.7% of goat hairs from West Bank of Jordan. Deshmukh (2004) reported that C. indicum was the most common species in feathers of pigeon and was represented in 24% of the samples. The above species and other Chrysosporium spp. were also isolated but with different frequencies from animal hairs (Deshmukh, 2004; Mandeell, et al. 2009 and Dokuzeylul et al. 2013) .

Aspergillus was the second most frequent genus on camel hair, contaminating 48% of the samples matching 24.8% of total fungi. It was represented by 7 species of which A. flavus and A. niger were the most prevalent species (22 & 32% of samples and 5.7% & 11.7 % of total fungi). A. ustus (12% of the samples), A. terreus (8%), A. ochraceus (6%), A. fumigatus and A. wentii (4% each) were isolated in rare frequency of occurrence (Table 1).In Egypt,  Barakat and El-Shanawany (1998) reported that Aspergillus was the second most frequent genus on the hair of donkey. They noticed that A. fumigatus, A. sydowii, and A. versicolor were the most common species. Also, these Aspergillus species have been reported from hairs of camel, cow, donkey and goat in Egypt (Bagy and Abdel-Hafez, 1985; Bagy, 1986), from hair of cows, donkeys, goats, rabbits, cats and dogs in the west bank of Jordan (Ali Shtayeh et al. 1988a,b) and from hair of goats and wool of sheep inYemen (Sallam and Alkolaibe 2010)

In the present study , Scopulariopsis (2 species) occupied the third place in the number of cases of isolation. It was isolated from 28% of samples comprising 8% of total fungi. From the two species isolated S. brevicaulis was the most prevalent while, S. candida was less frequent (Table 1). Several authors reported the prevalence of Scopulariopsis species on hairs of camel (Bagy and Abdel-Hafez, 1985, Nasser et al. 1998; Shokri and Khosravi, 2011) as well as on other animals and birds in Portugal (Bernardo et al. 2005), Bahrin (Mandeell et al. 2009), and Iran (Rostami et al. 2010).

Emericella (2 species), Penicillium (3), Acremonium (2) and Geotrichum (1) were isolated from 7 or 8 samples (out of 50) contributing 3.4%, 2.8%, 3.6% and 1.9% of total fungi, respectively. From the above genera E. nidulans, P. chrysogenum, A. strictum and G. candidum were the most common species.

Dermatophytes represented by two genera (Microsporum and Trichophyton) were recovered from 7 samples, matching 1.2% and 1.1% of total fungi, respectively. From these genera, M. canis, M. gypseum, T. rubrum and T. verrucosum were identified in rare occurrence. These species were also isolated with different frequencies from hair of different animals as reported by Prado et al. (2008); Madhavi et al. (2011); Gangil et al. (2012); Dokuzeylul et al. (2013) and Mohammed (2013).

Alternaria (2 species), Chaetomium (2), Fusarium (3), Paecillomyces (1) and Thermoascus (1) were isolated in rare frequency of occurrence. They emerged in 8-10% of the samples, accounting collectively 8.6% of total fungi (Table1). These species were also isolated in different frequencies from various keratinous substrates as reported by several authors (Bagy, 1986: Sallam and Alkolaibe, 2010: and Mohammed, 2013).

Conclusion

The present study gives an insight on the mycobiota of camel hair in Taiz, Yemen. The prevalence of dermatophytes and non-dermatophytes emphasises that camels have a potentiality for shedding fungi in the environment and serve as reservoirs for human pathogens.


 


Table (1): fungi isolated from camel hair (out of 50) samples using

soil- plating technique on Saubroud's dextrose agar at 28ºC.

Genera & Species

TC

 

NCI & OR

 

Acremonium

    A. rutilum W. Gams

    A. strichum W. Gams

Alternaria

    A. alternata (Fr.) Keissler

    A. tenuissima (Kunze) Wiltshire

Aspergillus                                                                           

    A. flavus  link

    A. fumigatus Fresenius

    A. niger  van Tieghem

    A. terreus Thom

    A. ochraceus Wilhelm

    A. ustus (Bain.) Thom & Church

    A. wentii Wehmer

Chaetomium

C. globosum kunze

C. spirale Zopf

Chrysosporium 

C. indicum (Rand. & Sand.) Garg

C. keratinophilum D.Frey ex Carm.

C. tropicum Carmichael

C. georgii (Vars. & Ajello) Oorcshot

Chrysosporium sp.

Emericella

E. nidulans (Eidam.) Vuill.

E. ruglosa (Thom & Raper) Benjamin

Fusarium

F. verticillioides (Saccardo)Nirenberg

F. oxysporum Schlecht.

F. solani (Mart.) Sacc.

Geotrichum candidum Link

Microsporum

M. canis Bodin

M. gypsum (Bodin) Gulart & Grigorakis

Mucor hiemalis Wehmer

Paecillomyces lilacinus (Thom) Samson

Penicillium

P. chrysogenum Thom

P. funiculosum Thom

Penicillium sp.

Scopulariopsis

S. brevicaulis (Sacc.) Bain.

S. candida (Gueguen) Vuillemin

Thermoascus aurantiacus Miehe

Trichophyton

T. rubrum (Castellani) Sabouraud

T. verrucosum Bodin

Sterile mycelia

    27

     8

    19

    18

    13

5

188

43

5

89

16

14

18

3

24

19

5

311

79

34

173

18

                       7

26

22

4

13

7

3

3

14

9

6

3

5

4

21

16

2

3

77

61

16

6

8

2

6

8

 

7 L

3 R

4 R

5 R

4 R

3 R

24 M

11 L

2 R

16 M

4 R

3 R

6 R

2 R

5 R

4 R

3 R

31 H

19 M

16 M

23 M

14 M

6 R

8 L

6 R

2 R

6 R

4 R

2 R

2 R

7 L

7 L

5 R

2 R

3 R

4 R

8 L

4 R

2 R

3 R

14 L

10 L

6 R

5 R

7 L

2 R

5 R

7 L

 

Gross total counts

759

 

No. of genera

15

 

 

No. of species

34

 

  TC= Total count; NCI= number of cases of isolation; OR= occurrence remark: H= high occurrence, 25-50 (out of 50) cases; M= moderate occurrence, 13- 24 cases; L= low occurrence, 7- 12 cases; R= rare occurrence, 1-6 cases.

 

References

Abdel-Gawad, K. M. (1997): Mycological and some physiological studies of keratinophilic and other moulds associated with sheep wool. Microbiol. Res. 152: 181-188.

Ali-Shtayeh, M. S.; Arda, H. M.; Hassouna, M. and Shaheen, S. F. (1988a): Keratinophilic fungi on the hair of goats from the West Bank, Jordan. Mycopathologia 104: 103-108.

Ali-Shtayeh, M. S.; Arda, H. M.; Hassouna, M. and Shaheen, S. F. (1988b): Keratinophilic fungi on the hair of cows, donkey, rabbits, cats and dogs from the West Bank Jordan. Mycopathologia 149: 193-121.

Ali-Shtayeh, M. S.; Arda, H. M.; Hassouna, M.; and Shaheen, S. F. (1989): Keratinophilic fungi on sheep hairs from West Bank of Jordan. Mycopathologia 106: 95-101

Bagy, M. M. K. and Abdel- Hafez, A. I. I. (1985): Mycoflora of camel and goat hairs from Al- Arish, Egypt. Mycopathologia 92: 125-128.

Bagy, M .M .K. (1986): Fungi on the hair of large mammals in Egypt. Mycopathologia 93: 73-75.

Barakat, A. and El-Shanawany, A. A. (1998): Studies on the mycoflora associated with donkey hair at Assiut. Assiut Vet. Med. J. 8(15-17): 283-294.

Bernardo, F.; Lanca, A.; Guerra, M. M. and Martins, H. M. (2005):  Dematophytes

 

isolated from pet, dogs and cats, in Lisbon, Portugal (2000-2004). Rev. Port. Cienc. Vet. 100: 85-88.

De Hoog G. S., Guarro J., Gene J. and Figueras M. J. (2000): Atlas of Clinical Fungi. Centraalbureau voor Schimmellcultures, Universitat Rovira I Virgili. Reus. Spain.

Deshmuka, S. K. (2004): Keratinophilic fungi on feathers of pigeon in Maharashtra, India. Mycoses 47: 213-215.

Dobrowolskh, A.; Staczek, P.; Kaszuba, A. and Kozlowska, M. (2006): PCR-RFLP analysis of the dermatophytes isolated from patient in central Poland. J. Dermatological Science 42: 71-74.

Dokuzeylul, B.; Kahraman, B. B. and Sigirci, B. D. (2013): Dermatophytosis caused by a Chrysosporium species in two cats in Turkey: a case report. Veterinarni Medicina 58: 633-636.

El-Said, A. H. M.; Sohair, T. H. and El-Hadi, A. G. (2009): Fungi associated with the hairs of goat and sheep in Libya. Mycobiology 37(2): 82-89

Gangil, R.; Dutta, P. and Tripathi, R. (2012): Incidence of dermatophytosis in canine cases presented at Apollo Veterinary College, Rajashtan, India. Vet. World 5(11): 682-684.

Khanam, S. J. P. and Jain, P. C. (2002): Isolation of keratin degrading fungi from soil of Damoh, India. Asian J. Microbiol. Biotechnol. Environ. Sci. 4: 251-254.

Kraemer, A.; Mueller, R. S.; Werckenthin, C.; Straubinger, R. K. and Hein, J. (2012): Dermatophytes in pet Guinea pigs and rabbits . Veterinary Microbiology 157: 208-213.

Madhavi, S.; Rama, R. M. V. and Jyothsna, K. (2011): Mycological study of dermatophytosis in rural population. Annuals Biological Research 2(3): 88-93.

Maghraby, A. T.; Gherbawy, Y. A. M. H. and Hussein, A. M. (2008): Keratinophilic fungi inhabiting floor dusts of student houses at South Valley University in Egypt. Aerobiologia 24: 99-106.

Mandeel, Q.; Nardoni, S. and Mancianti, F. (2009): Keratinophilic fungi of feathers on common clinically healthy birds in Bahrain. Mycoses 54: 71-77

Marcella, R.; Mercantini, R.; Spinelli, P. and Volterra, L. (1985): Occurrence of keratinophilic fungi in animals of the zoological park of Roma. Mykosen 28: 507-512.

Marcella, R. and Mercantini, R. (1986): Keratinophilic fungi isolated from soils of the Abruzzo National Park, Italy.  Mycopathologia 94: 97-107.

Mohammed, S. J. (2013): Dermatophytes isolated from dogs suspected of dermatophytosis in Baghdad City. Diyala J. Pure Sci. 9(4): 61-66.

Moses, O. E. and Sunday, O. F. (2001): Occurrence of keratinophilic fungi and dermatophytes on birds in Nigeria. Mycopathologia 153: 87-89.

Moss, E. S. and McQuown, A. I. (1969): Atlas of medical mycology 3rded. The Williams and Wilkins Company, Baltimore U.S.A.

Moubasher A. H. (1993): Soil fungi in Qatar and other Arab countries. Scientific and Applied Research Center. University of Qatar,566 pp.

Mukesh, S. and Sharma, M. (2010): Incidence of dermatophytes and other keratiophilic fungi in schools and college playground soils of Jaipur, India. Afr. J. Microbial. Research 4(24): 2647-2654.

Nasser, L. A.; El-Shanawany, A. A. and Barakat, A. (1998): Ecological and physiological studies on fungi associated with camel hairs from Saudi-Arabia. Assiut Vet. Med. J. 8(15-17): 243-254.

Nichita, I. and Marcu, A. (2010): The fungal microbiota isolated from cats and dogs. Animal Science and Biotechnologies 43(1): 411-414.

Ogbonna, C. I. C.; Enweani, I. B. and Ogueri, S. C. (1986): The distribution of ringworm infections amongst Nigerian nomadic fulani herdsmen. Mycopathologia 96: 45-51.

Periasamy, A.; Hilda, A. and Subash, C. B. G. (2004): Keratinophilic fungi of poultry farm and feather damping soil in Tamil Nadu, India.  Mycopathologia 158: 303-309.

Prado, M .R.; Brilhante, R .S. M. and Cordeiro, R. A. (2008): Frequency of yeasts and dermatophytes from healthy and diseased dogs. J. Vet. Diagn. Invest. 20: 197-202.

Ress, R. G. (1967): Keratinophilic fungi from Queensland. 11. Isolation from animal hairs and scales. Sabouraudia 5: 165-172.

Rippon, J. W. (1982): The pathogenic fungi and the pathogenic actinomycetes. Philadelphia: W. B. Saunders Company.

Rostami, A.; Shirani, D.; Shokri, H.; Khosravi, A. R.; Daieghazvini, R. and Tootian, Z. (2010): Fungal flora of the hair coat of Persian squirrel (Sciurus anomalus) with and without skin lesion in Tehran, Iran. J. de Mycologie Medicale 20: 21-25.

Sallam, A. M. H. and Alkolaibe, A. M. (2010): Distribution pattern of other keratinophilic fungi on goats hair and sheep wool,Taiz city, Yemen. J. Environmental Sciences 39 (3): 345-356.

Shokri, H. and Khosravi, A. R. (2011): Fungal        

        flora isolated from the skin of healthy    

        dromedary camels Camelus dromedaries.    

        Int. J. Vet. Res. 5 (2): 109-112.

Shukia, P.; Shukla, C. B.; Kango, N. and Skukla, A. H. (2003): Isolation and characterization of a dermatophyte, Microsporium gypseum from soils of Rewa (Madhya Pradesh), India. Pak. J. Bio. Sci. 6: 622-625.

Singh, I.; Mishra, A. and Kushwaha, R. (2009): Dermatophytes, related keratinophilic and opportunistic fungi in indoor dust of houses and hospitals. Indian J. Med. Microbial. 27: 242-246.

Ulfig, K. (2007): Influence of peptone, ammonia, water and urea supplements on keratinolytic and associated non-keratinolytic fungi in sewage sludge. Int. Biodeterioration & Biodegradation 59: 62-68.


 

 

 

 

 

 

 

 

 

الملخص العربي

الفطريات المصاحبة لشعر الجمال بمدينة تعز- اليمن

علي محمد حسن سلام*    جمال العامري**

قسم الميکروبيولوجى التطبيقى - کلية العلوم * قسم الميکروبيولوجي کلية الطب**– جامعة تعز- اليمن

 

استهدف البحث التعرف على الأحياء الفطرية لخمسين عينة من شعر الجمال جمعت من أماکن مختلفة من مدينة تعز وذلک باستخدام طريقة مصائد التربة والوسط الغذائي سبارود اجار والتحضين عند درجة حرارة 28°موقد  تم عزل34 نوعاً فطرياً تنتمي إلى 15 جنساً وکان أکثر الأجناس شيوعاً وانتشاراً هو جنس کريزوسبورم يليه اسبرجلس ثم جنس اسکوبيولاريوبيسس کما تم أيضاً عزل أنواع من الفطريات الجلدية تنتمي إلي الميکروسبورم والتريکوفيتون ولوحظ أن العديد من الفطريات المعزولة يمکن أن تکون ممرضة للإنسان. 

References
Abdel-Gawad, K. M. (1997): Mycological and some physiological studies of keratinophilic and other moulds associated with sheep wool. Microbiol. Res. 152: 181-188.
Ali-Shtayeh, M. S.; Arda, H. M.; Hassouna, M. and Shaheen, S. F. (1988a): Keratinophilic fungi on the hair of goats from the West Bank, Jordan. Mycopathologia 104: 103-108.
Ali-Shtayeh, M. S.; Arda, H. M.; Hassouna, M. and Shaheen, S. F. (1988b): Keratinophilic fungi on the hair of cows, donkey, rabbits, cats and dogs from the West Bank Jordan. Mycopathologia 149: 193-121.
Ali-Shtayeh, M. S.; Arda, H. M.; Hassouna, M.; and Shaheen, S. F. (1989): Keratinophilic fungi on sheep hairs from West Bank of Jordan. Mycopathologia 106: 95-101
Bagy, M. M. K. and Abdel- Hafez, A. I. I. (1985): Mycoflora of camel and goat hairs from Al- Arish, Egypt. Mycopathologia 92: 125-128.
Bagy, M .M .K. (1986): Fungi on the hair of large mammals in Egypt. Mycopathologia 93: 73-75.
Barakat, A. and El-Shanawany, A. A. (1998): Studies on the mycoflora associated with donkey hair at Assiut. Assiut Vet. Med. J. 8(15-17): 283-294.
Bernardo, F.; Lanca, A.; Guerra, M. M. and Martins, H. M. (2005):  Dematophytes
 
isolated from pet, dogs and cats, in Lisbon, Portugal (2000-2004). Rev. Port. Cienc. Vet. 100: 85-88.
De Hoog G. S., Guarro J., Gene J. and Figueras M. J. (2000): Atlas of Clinical Fungi. Centraalbureau voor Schimmellcultures, Universitat Rovira I Virgili. Reus. Spain.
Deshmuka, S. K. (2004): Keratinophilic fungi on feathers of pigeon in Maharashtra, India. Mycoses 47: 213-215.
Dobrowolskh, A.; Staczek, P.; Kaszuba, A. and Kozlowska, M. (2006): PCR-RFLP analysis of the dermatophytes isolated from patient in central Poland. J. Dermatological Science 42: 71-74.
Dokuzeylul, B.; Kahraman, B. B. and Sigirci, B. D. (2013): Dermatophytosis caused by a Chrysosporium species in two cats in Turkey: a case report. Veterinarni Medicina 58: 633-636.
El-Said, A. H. M.; Sohair, T. H. and El-Hadi, A. G. (2009): Fungi associated with the hairs of goat and sheep in Libya. Mycobiology 37(2): 82-89
Gangil, R.; Dutta, P. and Tripathi, R. (2012): Incidence of dermatophytosis in canine cases presented at Apollo Veterinary College, Rajashtan, India. Vet. World 5(11): 682-684.
Khanam, S. J. P. and Jain, P. C. (2002): Isolation of keratin degrading fungi from soil of Damoh, India. Asian J. Microbiol. Biotechnol. Environ. Sci. 4: 251-254.
Kraemer, A.; Mueller, R. S.; Werckenthin, C.; Straubinger, R. K. and Hein, J. (2012): Dermatophytes in pet Guinea pigs and rabbits . Veterinary Microbiology 157: 208-213.
Madhavi, S.; Rama, R. M. V. and Jyothsna, K. (2011): Mycological study of dermatophytosis in rural population. Annuals Biological Research 2(3): 88-93.
Maghraby, A. T.; Gherbawy, Y. A. M. H. and Hussein, A. M. (2008): Keratinophilic fungi inhabiting floor dusts of student houses at South Valley University in Egypt. Aerobiologia 24: 99-106.
Mandeel, Q.; Nardoni, S. and Mancianti, F. (2009): Keratinophilic fungi of feathers on common clinically healthy birds in Bahrain. Mycoses 54: 71-77
Marcella, R.; Mercantini, R.; Spinelli, P. and Volterra, L. (1985): Occurrence of keratinophilic fungi in animals of the zoological park of Roma. Mykosen 28: 507-512.
Marcella, R. and Mercantini, R. (1986): Keratinophilic fungi isolated from soils of the Abruzzo National Park, Italy.  Mycopathologia 94: 97-107.
Mohammed, S. J. (2013): Dermatophytes isolated from dogs suspected of dermatophytosis in Baghdad City. Diyala J. Pure Sci. 9(4): 61-66.
Moses, O. E. and Sunday, O. F. (2001): Occurrence of keratinophilic fungi and dermatophytes on birds in Nigeria. Mycopathologia 153: 87-89.
Moss, E. S. and McQuown, A. I. (1969): Atlas of medical mycology 3rded. The Williams and Wilkins Company, Baltimore U.S.A.
Moubasher A. H. (1993): Soil fungi in Qatar and other Arab countries. Scientific and Applied Research Center. University of Qatar,566 pp.
Mukesh, S. and Sharma, M. (2010): Incidence of dermatophytes and other keratiophilic fungi in schools and college playground soils of Jaipur, India. Afr. J. Microbial. Research 4(24): 2647-2654.
Nasser, L. A.; El-Shanawany, A. A. and Barakat, A. (1998): Ecological and physiological studies on fungi associated with camel hairs from Saudi-Arabia. Assiut Vet. Med. J. 8(15-17): 243-254.
Nichita, I. and Marcu, A. (2010): The fungal microbiota isolated from cats and dogs. Animal Science and Biotechnologies 43(1): 411-414.
Ogbonna, C. I. C.; Enweani, I. B. and Ogueri, S. C. (1986): The distribution of ringworm infections amongst Nigerian nomadic fulani herdsmen. Mycopathologia 96: 45-51.
Periasamy, A.; Hilda, A. and Subash, C. B. G. (2004): Keratinophilic fungi of poultry farm and feather damping soil in Tamil Nadu, India.  Mycopathologia 158: 303-309.
Prado, M .R.; Brilhante, R .S. M. and Cordeiro, R. A. (2008): Frequency of yeasts and dermatophytes from healthy and diseased dogs. J. Vet. Diagn. Invest. 20: 197-202.
Ress, R. G. (1967): Keratinophilic fungi from Queensland. 11. Isolation from animal hairs and scales. Sabouraudia 5: 165-172.
Rippon, J. W. (1982): The pathogenic fungi and the pathogenic actinomycetes. Philadelphia: W. B. Saunders Company.
Rostami, A.; Shirani, D.; Shokri, H.; Khosravi, A. R.; Daieghazvini, R. and Tootian, Z. (2010): Fungal flora of the hair coat of Persian squirrel (Sciurus anomalus) with and without skin lesion in Tehran, Iran. J. de Mycologie Medicale 20: 21-25.
Sallam, A. M. H. and Alkolaibe, A. M. (2010): Distribution pattern of other keratinophilic fungi on goats hair and sheep wool,Taiz city, Yemen. J. Environmental Sciences 39 (3): 345-356.
Shokri, H. and Khosravi, A. R. (2011): Fungal        
        flora isolated from the skin of healthy    
        dromedary camels Camelus dromedaries.    
        Int. J. Vet. Res. 5 (2): 109-112.
Shukia, P.; Shukla, C. B.; Kango, N. and Skukla, A. H. (2003): Isolation and characterization of a dermatophyte, Microsporium gypseum from soils of Rewa (Madhya Pradesh), India. Pak. J. Bio. Sci. 6: 622-625.
Singh, I.; Mishra, A. and Kushwaha, R. (2009): Dermatophytes, related keratinophilic and opportunistic fungi in indoor dust of houses and hospitals. Indian J. Med. Microbial. 27: 242-246.
Ulfig, K. (2007): Influence of peptone, ammonia, water and urea supplements on keratinolytic and associated non-keratinolytic fungi in sewage sludge. Int. Biodeterioration & Biodegradation 59: 62-68.