Keratinophilic Fungi on the Hair of Goats from the West Bank of Jordan

Mycopathologia 104:103-108 (1988) Kluwer Academic Publishers, Dordrecht - Printed in the Netherlands 103

Keratinophilic fungi on the hair of goats from the West Bank of Jordan

M. S. Ali-Shtayeh, 1 H. M. Arda, 2 M. Hassouna 3 & S. E Shaheen 4 1Department of Biological Sciences, The University, Nablus, West Bank of Jordan; 2Arda Dermatology Clinic, Nablus, West Bank of Jordan; 3Department of Veterinary, Nablus, West Bank of Jordan; 4Department of Public Health, Nablus, West Bank of Jordan, Israel

Key words: keratinophilic fungi, dermatophytes, goats, epidemiology

Abstract

The mycoflora of the hair in 178 goats from the West Bank of Jordan was analysed and the frequency of occurrence and the relative importance value for the different keratinophilic fungi found were calculated. One hundred and seven species which belong to 38 genera were isolated. Thirty six of these species were either well recognised agents of mycoses (Trichophyton mentagrophytes, T. verrucosum, and M. nahum), or have been frequently isolated from human and animal lesions (Arthroderma spp., Acremonium kiliense, Alternaria alternata, Aspergillusflavus, Cladosporium carionii, and several other species). These potentially pathogenic fungal species comprised 66.9% of all keratinophilic fungi found on the hair of goats. The role of this animal as a reservoir for dermatophytes and other potentially pathogenic fungi is discussed.

Introduction able on these fungi on goat hairs. This paper reports the results of a survey on the dermatophytes and oth- Animals play an important role in the transmission er kreatinophilic fungi on the healthy hair of goats and persistence of dermatophytes and other poten- from the West Bank of Jordan in an attempt to eluci- tially pathogenic fungi [6, 9, 24]. A knowledge of the date the role of these animals in the epidemiology frequency and extension of etiological agents of hu- of animal and human mycoses. man and animal mycoses and other potentially pathogenic fungi on the hair of domestic animals is of prime importance for the understanding of the Materials and methods epidemiological cycles of these fungi [15, 21, 24]. A limitied number of investigations has been car- Healthy hair samples, about 200 hairs each, were ried out on the dermatophytes and other ker- collected from 178 goats from different localities in atinophilic fungi on healthy hair of domestic the West Bank of Jordan (Table 1). Hair samples animals in different parts of the world [4, 5, 17, 24]. were placed in sterile plastic bags and brought back The accumulation of such information together to the laboratory where they kept at room tempera- with an increased awarenenss of opportunistic ture until processed within 36 hours. The samples mycotic diseases will be of great importance in ex- were placed on sterile soil moistened with sterile dis- panding knowledge about human and animal my- tilled water. Two plates were used for each sample. coses [9, 231. The plates were incubated at room temperature for In the West Bank of Jordan, Ali-Shtayeh et al. [3] 16 weeks. During this period soil in the plates was studied the dermatophytes and other keratinophilic remoistened with sterile distilled water whenever fungi on healthy sheep but there are no records avail- necessary and hairs were periodically transferred 104

Table 1. Types, distribution, total numbers of animals exam- veloped fungal colonies examined and identified. ined, and numbers of positive animals; percentages of +ve Four such transfers were carried out on each sample animals are shown in parentheses. of hairs.

Locality Goats Frequency of occurrence as percentage of animals on which the fungal species was found and the rela- No. +ve % tive importance value (RIV) was calculated for each species [3]. Nablus 68 68 (100) Jenin 65 65 (100) Tulkarm 15 15 (100) Bethlehem & Ramalla 17 17 (100) Results Hebron 13 12 (92) One hundred and seven species of keratinophilic Totals 178 177 (99) fungi which belong to 38 genera, were recovered from goat hairs (Table 2). Alternaria alternata, Cladosporium herbarum, onto Sabouraud agar medium amended with cyclo- Fusarium moniliforme, Paecilomyces marquandii, heximide (0.5 mg/ml) and chloramphenicol (0.05 Aspergillus flavus, and Chrysosporium ker- mg/ml). Two hairs, taken at random from each plate, atinophilum were the most frequent and common were transfered on Sabouraud agar plates and the keratinophilic fungi on the hair of goats. These spe- agar plates incubated at 27C for 2 weeks and the de- cies had the highest relative importance values

Table 2. Keratinophilic fungi found on the hair of goats (number of animals examined 178) from the West Bank of Jordan. +, pathogenic and potentially pathogenic fungi.

Fungal species No. of +ve Percentage No. of RIV animals/ of + ve animals/ isolates/ species species species

+ Arthroderma cuniculi 3 1.7 6 2.4 +A. curreyi 3 1.7 6 2\4 +A. tuberculatum 4 2.3 13 3.8

Chrysosporium asperatum 3 1.7 6 2.4 C. evolceanui 6 3.4 9 4.4 C. indicum 2 1.1 7 1.9 C. keratiuophilum 14 7.9 29 11.3 + C. pannorum 1 0.6 2 0.8 + C. tropicum 12 6.7 26 9.8

+ Microsporum audonuinii 3 1.7 9 2.7 + M. nanum 2 1.1 2 1.3

+ Trichophyton mentagrophytes 11 6.2 21 8.6 + T. verrucosum 7 3.9 10 5.2

+ Acremonium falciforme 1 0.6 1 0.7 A. furcatum 1 0.6 1 0.7 A. fusidioides 2 1.1 3 1.5 + A. kiliense 3 1.7 5 2.3

+ Alternaria alternata 78 43.8 257 73.8 Aspergillus alutaceus 1 0.6 1 0.7 A. candidus 8 4.5 8 5.5 A. chevalieri 1 0.6 1 0.7 A. erythrocephalus 1 0.6 1 0.7 105

Table 2. Continued.

Fungal species No. of +ve Percentage No. of RIV animals/ of +ve animals/ isolates/ species species species

A. flavipes 1 0.6 1 0.7 + A. flavus 16 9.0 23 11.7 + A. fumigatus 1 0.6 1 0.7 + A. niger 11 6.2 13 7.8 A. parasiticus 2 1.1 3 1.5 A. repens 1 0.6 1 0.7 + A. restrictus 2 1.1 4 1.6 A. ustus 3 1.7 4 2.2 + A. versicolor 3 1.7 24 4.5 A. wentii 3 1.7 3 2.1

Botrytis sp. 1 0.6 1 0.7

Chaetomidium fimeti 4 2.3 5 2.9

+ Cladosporium bantianum 6 3.4 8 4.3 + C. carionii 6 3.4 7 4.2 + C. cladosporiodes 1 0.6 1 0.7 C. herbarum 27 15.2 31 18.9 C. resinae 1 0.6 1 0.7

Emericella nidulans 1 0.6 2 0.8 E. nivea 1 0.6 2 0.8

Exophiala mansonii 1 0.6 1 0.7

Fennellia flavipes 1 0.6 1 0.7

Fusarium fusarioides 1 0.6 1 0.7 F. heterosporum 1 0.6 1 0.7 + F. moniliforme 18 10.1 29 13.6 + F. oxysporum 5 2.8 8 3.7 F. poae 1 0.6 1 0.7 + F. solani 2 1.1 3 1.5

+ Gliocladium roseum 8 4.5 25 7.4 G. solani 1 0.6 2 0.8 G. viride 1 0.6 2 0.8

Glomerularia corni 1 0.6 1 0.7

Harposporium oxycoracum 1 0.6 2 0.8

Humicola fuscoatra 2 1.1 2 1.3 H. grisea 1 0.6 i 0.7

Memnoniella echinata 5 2.8 5 3.5

Monilia sitophila 8 4.5 10 5.7

Monoaseus ruber 2 1.1 3 1.5

Mucor piriformis 1 0.6 1 0.7 M. strictus 3 1.7 4 2.2 + M. saturninus 1 0.6 1 0.7

Oidiodendron griseum 1 0.6 1 0.7

Paecilomyces carneus 3 1.7 4 2.2 P. farinosus 5 2.8 9 3.8 106

Table 2. Continued.

Fungal species No. of +ve Percentage No. of RIV animals/ of +ve animals/ isolates/ species species species

+ P. lilacinus 9 5.1 18 7.2 P. marquandii 17 9.6 32 13.3 + P. variotii 1 0.6 t 0.7

Penicillium canescens 3 1.7 3 2.1 P. chrysogenum 2 t.1 2 1.3 + P. citrinum 2 1.1 6 1.8 P. daleae 1 0.6 1 0.7 P. expansum 1 0.6 1 0.7 P. frequentans 1 0.6 2 0.8 P. funiculosum t 0.6 3 0.8 P. griseofulvum 1 0.6 t 0.7 + P. herquei 1 0.6 13 2.1 P. islandicum 2 1.1 3 1.5 P. janthinellum 2 1.1 4 1.6 P. nigricans 1 0.6 1 0.7 P. oxallicum 1 0.6 1 0.7 P. purpurogenum 2 1.1 3 1.5 + P. rubrum 1 0.6 2 0.8 + P. simplicissimum 1 0.6 1 0.7 P. stoloniferum 1 0.6 1 0.7 P. variabile 1 0.6 1 0.7

Phialophora atra 1 0.6 1 0.7 P. cyclaminis 1 0.6 1 0.7

Plectosphaerella cucumerina 1 0.6 t 0.7

+ Rhizopus stolonifer 2 1.1 2 1.3

Scopulariopsis acremonium 1 0.6 1 0.7 + S. brevicaulis 8 4.5 10 5.7 + S. brumptii 2 1.1 4 1.6 S. candida 5 2.8 5 3.4

Sporendonema casei 1 0.6 1 0.7

+ Sporothrix schenckii 1 0.6 4 1.0

Staphylotrichum corcosporum 2 1.1 2 1.3

Syncephalstrum racemosum 3 1.7 4 2.2

Trichosporiella cerebriformis 1 0.6 3 0.9

Trichothecium roseum 1 0.6 1 0.07 + Ulocladium chartarum 2 1.1 2 1.3

Verticillium albo-atrum 2 1.1 3 1.5 V. lamellicola 1 0.6 1 0.7 V. lecanii 3 1.7 6 2.4 V. nigrescens 1 0.6 2 0.8 V. psalliotae 5 2.8 10 4.0

Sterile hyphae 7 3.9 8 4.8

Total number of isolates 849 107

(RIV's): 73.8, 18.9, 13.6, 13.3, 11.7 and 11.3 respec- on the hair of goats. It comprised 5.1% (43/849 iso- tively. lates) of all fungi and was represented by 6 species. Dermatophytes and related fungi (i.e., Arthroder- Other frequent genera were: Gliocladium (4.3 %), ma spp, Chrysosporium spp) were represented by VerticilHum (2.6%), and Scopulariopsis (2.4%). fourteen species. These comprised about 17.3% Other fungi were less frequent and less common (147/849 isolates) of all fungi isolated. The dermato- on the hair of goats. phytes species comprised about 5 % (42/849 isolates) of hair mycoflora. Trichophyton mentagrophytes was the most common and frequent dermatophyte Discussion species on the hair of goats, it was found in 6.2% of all goats investigated and it comprised 2.5% of all The present investigation of mycoflora of the hair of fungal isolates recovered. Trichopyton verrucosum goats from the West Bank of Jordan has revealed was the second most frequent dermatophyte, it was that Trichophyton mentagrophytes, T. verrucosum, found in 3.9% of the animals and comprised 1.2% and Microsporum audouinii were the most frequent of all fungi isolated. Other dermatophytes recovered dermatophyte species encountered on these animals. were Microsporum audouinii (on 1.7% of animals), The first two species have also been reported from and M. nanum (on 1.1% of animals). goats by a few workers [1, 13]. The other two der- The genus Chrysosporium was represented by 6 matophyte species present on goat hair were M. na- species. It comprised 9.3% (79/849 isolates) of all num, and M. audouinii which were recorded for the keratinophilic fungi recovered. Chrysosporium ker- first time from goat hair in the area. It is interesting atinophilum was the most frequent and common of to note that these dermatophyte species were not these species, it was found in 7.9% of the animals recovered from goat hairs in neighbouring Israel and comprised 3.4% (29/849) of all fungal isolates [12], and Egypt [5]. Microsporum canis was absent recovered. The genus Arthroderma was represented from goat hair mycoflora in the West Bank but was by 3 species, and comprised 2.9% (25/849 isolates) isolated from goats in Norway [22] and Germany of all keratinophilic fungi recovered. [11]. The genus Alternaria was the most common and It is interesting to note that T. mentagrophytes and frequent fungus found on the hair of goats. It was T. verrucosum have also been reported from human found in 4328% of all animals, and it comprised mycoses in the West Bank of Jordan [2, 20]. The two 30.3% (257/849) of all fungal isolates recovered. species comprised 73.8% (31/42 isolates) of the der- Aspergillus was the second most frequent genus matophytes found on goat hair. It is also noteworthy found on the hair of goats. It comprised 10.4% to mention that all the dermatophyte species found (88/849) of all fungal isolates recovered. It was on goat hair except M. audouinii, were also reco- represented by fourteen species, of which A. flavus vered from sheep hair in the West Bank [3]. was the most common. Chrysosporium keratinophilum and C. tropicum Paecilomyces came fourth behind Chrysospo- seem to be quite common on goat hairs. They were rium. It comprised 7.5% (64/849) of all fungal iso- found in 7.9% and 6.7% of all animals examined lates found. It was repesented by 5 species, of which respectively. This is in agreement with the results of P. marquandii was the most common. a similar study on goat hair from Egypt by Bagy & Penicillium and Cladosporium were among the Abdel-Hafez [5], who found C. keratinophilum and common fungi on the hair of goats, they comprised C. tropicum on 55% and 45% of the goats they ex- 5.8 % (49/849 isolates) and 5.7 % (48/849) of all fun- amined, respectively. These species were also isolat- gi recovered, respectively. Penicillium was represented from mammals in different parts of the world [8, ed by eighteen species, of which P. herquei was the I0, 14, 16, 18]. most frequent, whereas Cladosporium was Arthroderma tuberculatum was found in 2.3 % of represented by five species of which C. herbarum the goats examined in our study and was also found was the most frequent. The genus Fusarium_was the in 6.7% of the goats examined in Egypt [5]. Another next (behind Cladosporium) most common fungus two species A. cuniculi, and A. curreyi were also 108 found in our work but were absent from goat hair sis of the sands of a box for children's play. Mycopathologia in Egypt. 1982; 80:43-54. 8. Gugnani HC, Wattal BL, Sandhu RS. Dermatophytes and It is interesting to note that 35 species (marked' +' other keratinophilic fungi recovered from small mammals in in Table 2) of the keratinophilic fungi recovered from India. Mykosen 1975; 18:529-38. the hair of goats from the West Bank of Jordan were 9. Hall NK, Larsh HW. Epidemiology of the mycoses. In: either well-known mycotic agents of human and Howard DH, ed. Fungi pathogenic for humans and animals animals such as Trichophyton mentagrophytes, T. (in three parts): Part B: Pathogenicity and detection. New York: Marcel Dekker, Inc. 1985; 3:195-228. verrucosum, and Microsporum audouinii, or patho- 10. Haffmann R, Kolipp D, Koch HA. Die Bedeutung von Mous- genic and potentialy pathogenic fungi [1, 7, 9, 12, en und anderen kleinsaugern fur die verbreit-ung von Der- 19]. The latter fungi included Acremonium kiliense, matophyten und anderen keratinophilen Pilzen. Mykosen Alternaria alternata, Aspergillus flavus, Cladospo- 1970; 13:353-87. rium bantianum, Fusarium moniliforme, 11. Kuntze A, Gemeinhardt H, Bensch GJ. Uber eine Microspo- Paecilomyces lilacinus, Scopulariopsis acremoni- rum canis-Endemie bei zootieren mitverufsbedingten Infek- tionen beim Menschen. Mykosen 1967; 10:7-18. um, and others. These potentially pathogenic fungi 12. Kuttin ES, Beemer AM. Fungi isolated from birds and comprised 66.9% (568/849) of all fungal isolates animals in Israel. In: Iwata K. ed. Recent advances in medical found on the hair of goats. This fact leads us to con- and veterinary mycology. Baltimore: University Park Press clude that goats are important domestic animals in 1975; 151-55. 13. Monga DP, Mohapatra LN. 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