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mycoses

Diagnosis,Therapy and Prophylaxis of Fungal Diseases

Original article

Dermatophytes as a cause of epizoonoses in dairy cattle and humans


in Iran: epidemiological and clinical aspects
Mohammad Reza Aghamirian1 and Seyed Amir Ghiasian2
1

Medical 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 20062007. 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 diseases are widespread throughout the world, which can
be mainly transmitted from domestic animals to
humans and from animals to animals. Increasing
incidence of dermatophytoses in animals has been
observed in crowded housing areas, especially in winter
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: s.a.ghiasian@umsha.ac.ir
Accepted for publication 29 October 2009

doi:10.1111/j.1439-0507.2009.01832.x

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.13 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 considerations, a number of limited surveys have been published
on cattle ringworm from Middle East countries. Furthermore, there was a scarcity of information on the
identification and geographical distribution of dermatophytic 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

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Dermatophytosis in cattle and humans in Iran

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 temperature 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 equipments. A total of 6789 head of cows were examined in
this 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 the
margin 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 containing 50 mg l)1 chloramphenicol and 500 mg l)1 cycloheximide (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 forming
chains of chlamydoconidia. Chlamydoconidia was
visualised in T. verrucosum only after keeping the
positive slide at 37 C for 5 days.4

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 (1015 micron in diameter) and from the
cultures, only T. verrucosum was isolated (100%). In
addition, our data indicate that only 3.7% of the
samples 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
1318 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 dermatophytosis was varied from farm to farm with a range of
050%.
Table 1 Results of culture and direct smear of the cattle with
suspected dermatophytosis.
Culture

Human sampling

Direct smear

Positive

Negative

Total

During the study, 43 herdsmen who had close contact


with infested livestock and were suspected of having
dermatophytoses were referred to the Mycology

Positive
Negative
Total

338
14
352

0
28
28

338
42
380

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M. R. Aghamirian and S. A. Ghiasian

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 percentage 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 or
culture. 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, tinea
unguium and tinea capitis (each 14.8%).
The dermatophyte pathogens isolated from the positive
culture of the patients were mostly T. verrucosum

90
Percentage of involved sites

80
70
60
50
40
30
20
10
0

Head

Neck

Chest

Belly

Waist and Tail and


haunch
limbs
Table 2: Involved sites by dermatophytosis in various
body regions of cattle in Qazvin province during 20062007

Figure 1 Involved sites by dermatophytosis in various body regions of cattle in Qazvin province during 20062007.

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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 our study, a study on the
dermatophytes isolated from domestic animals in Iran
showed that T. verrucosum was the second most frequently
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 were
ignored 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 inflammation 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 1554 months. Therefore having enough time to
infect 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

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Dermatophytosis in cattle and humans in Iran

Table 2 Isolated dermatophyte species according to the type of tinea in Iranian dairy farmers (20062007).
Type of tinea
Culture results

Tinea cruris

Tinea corporis

Tinea pedis

Tinea unguium

Tinea capitis

Total

T. verrucosum
T. rubrum
E. floccosum
T. mentagrophytes var. mentagrophytes
T. mentagrophytes var. interdigitale
No growth
Total of cases

1 (25)
0
3 (75)
0
0
0
4

6
1
1
1
0
0
9

2
1
0
2
1
0
6

1 (25)
2 (50)
0
0
0
1 (25)
4

4 (100)
0
0
0
0
0
4

14
4
4
3
1
1
27

(66.7)
(11.1)
(11.1)
(11.1)

(33.3)
(16.7)
(33.3)
(16.7)

(51.8)
(14.8)
(14.8)
(11.1)
(3.7)
(3.7)

Values are given as n (%).


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

(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 prevalence of ringworm in cattle were 5.6%. This figure is in
sharp contrast to those of some previous studies1316
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, headto-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 Sweden
showed 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.

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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 cases
examined, 14 (51.8%) patients were infected with T.
verrucosum through direct contact with diseased animals (Table 2). Ming et al. [15] reported dermatophytosis 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 cause
4.7% 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 examination. These results are in contrast to a study reporting
that direct microscopic examination could present
positive results in 4060% 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, treatment of infected livestock and national vaccination
planning are necessary for efficacious control of dermatophytosis as a major public and veterinary health
problem. Finally, it must conduct regular sterilization of

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M. R. Aghamirian and S. A. Ghiasian

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.

14

15

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

16

17

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