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Dermatophytes as a cause of epizoonoses in dairy cattle and humans

in Iran: epidemiological and clinical aspects

Mohammad Reza Aghamirian1 and Seyed Amir Ghiasian2

1Medical Parasitology and Mycology Department, Qazvin University of Medical Sciences and Health Services, Qazvin, Iran and 2Medical Parasitology and

Mycology Department, School of Medicine, Hamadan University of Medical Sciences and Health Services, Hamadan, Iran

Summary Zoophilic dermatophytosis is a major public and veterinary health problem globally

widespread among cattle. To identify the causative agent and geographical distribution

of dermatophytes involved in cattle ringworm and to establish if they would be related

to human diseases in Iran, a study was carried out on 6789 heads of cows and 130

herdsmen during 2006–2007. Samples were taken from 380 cattle and 43 herdsmen

with suspected dermatophytosis. The causative agents were identified macroscopically

and microscopically by KOH examination and culture isolation. Only 352 cases of

dermatophytosis were identified in cattle and Trichophyton verrucosum was the exclusive

fungus isolated from animals. Moreover, 27 cases of human dermatophytosis were

identified and T. verrucosum was the prevalent causative agent for dermatophytosis in

the body, scalp, foot, nail and groin of the patients. The obtained results showed that

T. verrucosum was the predominant cause of dermatophytosis in livestock and dairy

farmers. There is a scarcity of information on isolation and identification of

the epizoonotic agents of dermatophytoses in cattle in Iran. This study showed the

occurrence of dermatophytosis in humans and cattle and confirms that the

dermatozoonoses are responsible for predominant forms of the disease in people who

were in contact with cattle.

Key words: Animal dermatophytosis, Trichophyton verrucosum, human infection.

Introduction

Dermatophytosis is a major public and veterinary health

problem, which would trigger the disease in humans

and various animals. Zoophilic dermatophytes are one

of the most important fungi that predominantly infect

animals but infrequently infect humans. Zoonotic dis-

eases are widespread throughout the world, which can

be mainly transmitted from domestic animals to

humans and from animals to animals. Increasingincidence of dermatophytoses in animals has been

observed in crowded housing areas, especially in winter

season.1

A large body of literature suggests that in

recent years, a notable increase in cattle ringworm and

more contact between people and animals has been

responsible for its transmission to human.1–3 Human

dermatophytosis mostly occurs through contact with

infected cats and dogs in urban areas, whereas in rural

areas, it occurs through contact with cattle.1

This skin

disease results in decimated meat and milk, loss of

weight and low quality leather, which consequently

results in high economic losses.1

Taking into account the above mentioned consider-

ations, a number of limited surveys have been published

on cattle ringworm from Middle East countries. Fur-

thermore, there was a scarcity of information on the

identification and geographical distribution of dermat-

ophytic infections in cattle in Iran. The aim of the

present study was to identify the causative agents of

dermatophytosis in cattle in Qazvin province and its

outskirts and to establish their relate to the outbreak of

Correspondence: Seyed Amir Ghiasian, Medical Parasitology and Mycology

Department, School of Medicine, Hamadan University of Medical Sciences

and Health Services, P.O. Box 65155-518 Hamadan, Iran.

Tel.: +98 811 827 6295. Fax: +98 811 827 6299

E-mail: [email protected]

Accepted for publication 29 October 2009

Original article

doi:10.1111/j.1439-0507.2009.01832.x 2009 Blackwell Verlag GmbH • Mycoses 54, e52–e56

mycosesDiagnosis,Therapy and Prophylaxis of Fungal Diseases

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this disease in people residing in the area, especially

those who are in contact with the cattle.

Materials and methods

Qazvin is a province situated to the north-west of

Iranian capital, Tehran. The average summer temper-

ature ranges from 25 to 35 C and humidity is up to

50%. The duration of this descriptive study was 1 year,

i.e. from December 2006 to December 2007.

Animal sampling

Twenty-eight cowsheds were chosen randomly from the

outskirts of the Qazvin province. The cowsheds were

either run by the state or private owners. They were

either operated with industrialised or traditional equip-

ments. A total of 6789 head of cows were examined inthis study either from Holstein pure breed, Iranian

Sarabi breed or crossbred from two different breeds,

Sarabi and Holstein.

All parts of the body of each animal were carefully

examined for evidence of ringworm infection. Care was

taken so that the cows under study were not receiving

treatment for the infection until 3 days ahead of the

sampling operation. Samples were taken from suspected

dermatophytosis-affected cows. The skin-scale samples

were taken by scraping of the margin of the affected

area using a sterile forceps and a scalpel. Hair samples

were collected by removing dull broken hairs from themargin of the lesion using sterile tweezers. In direct

smear, several hair and skin samples were examined

microscopically using 15% KOH. The samples were

cultured on Sabourauds dextrose agar plates contain-

ing 50 mg l)1 chloramphenicol and 500 mg l)1 cyclo-

heximide (SCC).

To track the presence of T. verrucosum, one of the

cultures was incubated at 37 C for 3 days. The slide

culture technique was used to demonstrate the mode in

which conidia are formed. In cases where T. verrucosum

was present, chlamydoconidia was identified in the

inoculated samples in plates and the colony number

increased after 5 days with the fungus virtually formingchains of chlamydoconidia. Chlamydoconidia was

visualised in T. verrucosum only after keeping the

positive slide at 37 C for 5 days.4

Human sampling

During the study, 43 herdsmen who had close contact

with infested livestock and were suspected of having

dermatophytoses were referred to the Mycology

Reference Laboratory of the Medical School at the

Qazvin University of Medical Sciences. All parts of the

body of each patient were thoroughly examined for

evidence of scaling, crusting, follicular inflammation,

hair loss or erythema. The skin scrapings were collected

from the affected areas in the scalp, body, nail, feet,

arms, groin and face using a sterile scalpel. In addition,

hairs roots were pulled out from the affected scalp using

a sterile flat-headed tweezer. The causative agents were

identified macroscopically and microscopically by KOH

examination and culture isolation.

To determine the T. mentagrophytes varieties, the

isolates were differentiated according to their

macroscopic and microscopic characteristics and were

identified as T. mentagrophytes var. interdigitalis and

T. mentagrophytes var. mentagrophytes.

Results

Overall, 391 clinically suspected cows were identified of

which 380 heads underwent sampling operation. The

remaining suspected cases [11] were not examined

because of the lack of cooperation from cowsheds

officials to accord necessary cooperation. A total of

352 samples (92.6%) were proved positive in direct

smear and ⁄ or in culture (Table 1). All the positive cases

in direct smear were infected by ectothrix with large

spores (10–15 micron in diameter) and from the

cultures, only T. verrucosum was isolated (100%). In

addition, our data indicate that only 3.7% of thesamples examined were negative by direct examination

but were positive by culture method.

Regarding the age of cattle, 219 (57.7%) were 6- to

12-month-old calves, while 131 (34.5%) were calves

13–18 months of age and 30 (7.8%) were cows over

18 months old. The difference among the age groups

was significant so that the scale of infection decreased

with increase in age (P < 0.01), but there was no

significant difference between the sex and the three

different breeds sampled. The prevalence of dermato-

phytosis was varied from farm to farm with a range of

0–50%.

Table 1 Results of culture and direct smear of the cattle with

suspected dermatophytosis.

Direct smear

Culture

Positive Negative Total

Positive 338 0 338

Negative 14 28 42

Total 352 28 380

Dermatophytosis in cattle and humans in Iran

2009 Blackwell Verlag GmbH • Mycoses 54, e52–e56 e53

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The most important clinical lesions observed on the

affected cows were widespread scaly alopecia with or

without erythema and ⁄ or broad greyish-white hairless

skin patches and rarely pruritic skin reactions affecting

the head, neck, trunk, tail and limbs. The observed

lesions continued for more than 3 months. The per-

centage of animals infected in the four main regions of

body, i.e. head and neck, trunk, limb and tail is

presented in Fig. 1. Regarding the scale of infection,

head, neck, chest, belly, waist, haunch, tail and limbs

were infected in decreasing order. The preferential sites

on head were around the eyes, ears, cheeks and muzzle.

The number of damage in every cow or calf ranged from

3 to 30 cases.

With regarding to herdsmen, with of 130 persons

who lived and ⁄ or worked in dairy farms and had close

contact with infested cattle, 27 (20.8%) patients were

mycologically positive by direct microscopy and ⁄ orculture. In general, the male to female ratio of herdsmen

was 3.2 : 1 and males were affected more frequently

than females with the ratio of 3.5 : 1.

The seven dermatophyte species isolated along with

their frequencies of occurences are shown in Table 2.

Trichophyton verrucosum was the most frequent isolate

(51.8%), followed by T. rubrum and Epidermophyton

floccosum (each 14.8%), T. mentagrophytes var.

mentagrophytes (11.1%) and T. mentagrophytes var.

interdigitalis (3.7%). Tinea corporis (33.3%) was the

most common type of cutaneous mycotic infection,

followed by tinea pedis (22.2%), tinea cruris, tineaunguium and tinea capitis (each 14.8%).

The dermatophyte pathogens isolated from the positive

culture of the patients were mostly T. verrucosum

pathogens, i.e. identified in 14 cases. Furthermore, the

most prevalent agent causing dermatophytosis in

the body and scalp of the patients was T. verrucosum with

six cases (42.9), and four cases (28.6) respectively

(Table 2).

Discussion

The ringworm in cattle is predominantly caused

by T. verrucosum.5 According to Quinn et al. [6] T.

verrucosum, T. mentagrophytes and T. megninii have been

the major dermatophytes causing ringworm in cattle. In

this study, of interest, obtained results showed that

dermatophytosis of cattle were exclusively caused by T.

verrucosum (100%). In support of ourstudy, a studyon the

dermatophytes isolated from domestic animals in Iran

showed that T. verrucosum wasthe second mostfrequently

isolated dermatophyte.7 Furthermore, Nooruddin & Dey[8] could only isolate T. verrucosum from 130 heads of

infected cows in Bangladesh.

In the present study, there was a high proportion

(57.5%) of positive results in calves less than 1 year of

age. In support of our study, Oldenkamp [9] argued that

cattle under the age of 12 months are highly proved to

dermatophytosis. It has also been found that the pH of

the skin reduces with age, and hence young animals are

most susceptible to ringworm infection, which could be

due to their high skin pH as well as to their weak

immunity.1 Most of the animals had small, widespread

annular lesions, which either may go unnoticed or wereignored by their owners. One of the important factors

contributing to the frequency of dermatophytosis in

cattle is the close association between them.5

Cattle

ringworm can cause general discomfort and inflamma-

tion of the skin with an irritating itch so that the

affected animals are forced to rub against one another,

or against other objects such as wooden columns, fences

and trees to relieve the irritation. This rubbing can

result in further spreading of the infection.

According to Pandey [10], T. verrucosum could

remain viable and infectious in the infected skin or hair

of cattle and on the wooden parts of the cowshed fence

for 15–54 months. Therefore having enough time toinfect the newcomer cattle and the same source might

affect humans too.3

The crowded conditions with increased contact

between animals and the presence of infected debris in

barns account for the higher incidence of the disease in

calves and the greater infection rate in winter.1

Most of

the dairy farms in our study were traditional and their

conditions were even worse. Furthermore, the incidence

of dermatophytosis in cattle was higher in winter

0

10

20

30

40

50

60

70

80

90

Head Neck Chest Belly Waist and

haunch

Tail and

limbs

Table 2: Involved sites by dermatophytosis in various

body regions of cattle in Qazvin province during 2006–2007

P e r c e n t a g

e

o f i n v o l v e d

s i t e s

Figure 1 Involved sites by dermatophytosis in various body re-

gions of cattle in Qazvin province during 2006–2007.

M. R. Aghamirian and S. A. Ghiasian

e54 2009 Blackwell Verlag GmbH • Mycoses 54, e52–e56

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(37.7%) than during spring (27%), which is concordant

with the majority of studies worldwide.1,11,12

Of interest, obtained results showed that the preva-

lence of ringworm in cattle were 5.6%. This figure is insharp contrast to those of some previous studies

13–16

that reported the prevalence of ringworm in cattle in

Italy, China, Sweden and Switzerland, which were 19%,

20%, 29% and 74%, respectively.

With regard to gender, Haab et al. [17] considers no

less incidence of infection in female cattle than in male

cattle. The results of the present study also showed no

difference between the two genders in this regard.

With respect to the organs involved, Wabacha et al.

[18] considers the scalp of cows as the hardest hit

organ. The present study also identified 80% of infection

cases in the scalp. It seems that two habits, that is, head-to-head fighting and licking each other could partly

explain the particular prevalence of lesions on the head

and neck.

Trichophyton verrucosum may be responsible for skin

diseases in cattle and people who have close contact

with infected animals are in danger of this epizoonotic

infection.2,5 This study showed the occurrence of

dermatophytosis in humans and confirmed that T.

verrucosum was responsible for the basic forms of

dermatophytosis in people who were in contact with

cattle. In our study, the predominant causative agent of

dermatophytosis in infected dairy farmers was T.

verrucosum. An epidemiological study from Swedenshowed a positive correlation between dermatophytosis

in human and cattle.16

Contagion may happen through

inoculation of environmental spores into the skin of

people living in countryside areas or even via contagion

between individuals.19

Certain groups of people such as

farmers, veterinarians and prepuberty school children

are especially vulnerable. About one-third of our

patients were prepuberty children who directly or

indirectly exposed to the infected animals.

In most cattle cases, T. verrucosum is the pathogen

behind dermatophytosis in man.20 In this study, T.

verrucosum was the predominant dermatophytes

causing dermatophytosis in humans. Of 27 tinea casesexamined, 14 (51.8%) patients were infected with T.

verrucosum through direct contact with diseased ani-

mals (Table 2). Ming et al. [15] reported dermatophy-

tosis outbreak in cowshed staff, west of China, triggered

by T. verrucosum. Furthermore, our previous study on

the epidemiology of tineas among people resident in

Qazvin showed that T. verrucosum was the main agent of

tinea capitis (60%), tinea faciei (33.4%) and tinea

corporis (45.8%).21

However, in two studies carried out

in central and west of Iran, T. verrucosum was the major

dermatophyte isolated from humans.22,23

In a study in

southern Tehran, T. verrucosum was reported to cause4.7% of the dermatophytosis cases.24

Regarding the affected areas, the unexposed area

(70%) was more frequently affected than exposed areas

(30%), and the trunk was the most common site. Our

results in contrast to those of Lee et al. [25] in while the

exposed area (71.4%) was the more frequently affected

area.

Our results showed that 88.9% of the samples

examined were positive by direct microscopic examina-

tion. These results are in contrast to a study reporting

that direct microscopic examination could present

positive results in 40–60% of samples from which

dermatophytes were cultured.26

In conclusion, the results of the present study

revealed similarities among the isolated dermatophyte

species from infected herds of cattle and those isolated

from the herdsmen. Furthermore, our study suggests

that the periodic epidemiological investigations, treat-

ment of infected livestock and national vaccination

planning are necessary for efficacious control of der-

matophytosis as a major public and veterinary health

problem. Finally, it must conduct regular sterilization of

Table 2 Isolated dermatophyte species according to the type of tinea in Iranian dairy farmers (2006–2007).

Culture results

Type of tinea

Tinea cruris Tinea corporis T inea pedis T inea unguium Tinea capitis Total

T. verrucosum 1 (25) 6 (66.7) 2 (33.3) 1 (25) 4 (100) 14 (51.8)T. rubrum 0 1 (11.1) 1 (16.7) 2 (50) 0 4 (14.8)

E. floccosum 3 (75) 1 (11.1) 0 0 0 4 (14.8)

T. mentagrophytes var. mentagrophytes 0 1 (11.1) 2 (33.3) 0 0 3 (11.1)

T. mentagrophytes var. interdigitale 0 0 1 (16.7) 0 0 1 (3.7)

No growth 0 0 0 1 (25) 0 1 (3.7)

Total of cases 4 9 6 4 4 27

Values are given as n (%).

T ., Trichophyton; E., Epidermophyton; M ., Microsporum.

Dermatophytosis in cattle and humans in Iran

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land, water resources, surrounding fences and walls,

and carry out hygienic regulations regarding the

workers and the incoming cattle so as to prevent

dermatophytic epizoonoses in cattle and human.

Acknowledgments

We are grateful to Dr A. H. Maghsood for revising the

manuscript.

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