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180 Original article

Study of tinea corporis in patients attending the Dermatology


Clinic of Al-Hussein University Hospital, Cairo, Egypt
Fadia A. Sorour, Hamed M. Abdo and Mohamed A. Ebada

Department of Dermatology, Faculty of Medicine, Background


Al Azhar University, Cairo, Egypt
The etiology of tinea corporis is varied and frequently changing.
Correspondence to Hamed M. Abdo, MD, Department Objective
of Dermatology, Faculty of Medicine, Al Azhar
University, 11633 Cairo, Egypt The aim of the study was to detect the current prevailing fungi of tinea corporis among
Tel: + 20 106 633 9011; fax: + 20 (2)25104146; patients in our locality.
e-mail: hamed392@yahoo.com
Patients and methods
Skin scrapings were taken from 50 patients with circinate lesion(s) and examined by
Received 16 November 2014 direct microscopy and culture. One set of scrapings was mounted in 20% potassium
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Accepted 27 March 2015 hydroxide solution and examined for the presence of fungal elements. The second set
Journal of the Egyptian Women’s Dermatologic was inoculated onto Sabouraud’s dextrose agar to identify the causative fungus.
Society 2015, 12:180–185 Results
Out of the 50 patients, 29 were males and 21 were females. Their ages ranged from 1
to 55 years (mean ± SD 19.34 ± 13.1 years). The duration of the disease ranged from
3 to 60 days (mean ± SD 15.96 ± 9.3 days). Direct microscopy was positive in 46
(92%) cases and mycological cultures in 45 (90%) cases. Trichophyton violaceum
was isolated in 17 (34%) patients, followed by Trichophyton rubrum (13 patients;
26%), Microsporum audouinii (five patients; 10%), Microsporum canis (four patients;
8%), Trichophyton verrucosum (four patients; 8%), and Trichophyton tonsurans in two
(4%) patients.
Conclusion
The isolated anthropophilic fungi outnumbered zoophilic ones as an etiological cause of tinea
corporis. T. violaceum and T. rubrum were the most common agents, followed by other fungi.

Keywords:
dermatophytes, Egypt, fungal culture, potassium hydroxide mount, tinea corporis

J Egypt Women Dermatol Soc 12:180–185


& 2015 Egyptian Women’s Dermatologic Society
1687-1537

species, as geoclimatic and social conditions interfere with


Introduction the distribution of dermatophyte species [6].
Fungi are ubiquitous in nature and there is essentially no
part of our earth where fungi are not found. Of the The ringworm (tinea corporis) is the typical infection of the
thousands of fungal species that are free-living in exposed glabrous skin and can be caused by all known
nature, only a small group is known to be pathogenic dermatophytes, but the prevailing fungi in a particular region
for humans and animals [1]. Superficial fungal infections are likely to be the most frequently found infective agents [7].
are among the world’s most common diseases, and Mycological diagnosis of tinea corporis consists of a 10–20%
the prevalence of superficial mycotic infections has risen potassium hydroxide (KOH) preparation from skin scrapings,
to such a level that skin mycoses affect more than and fungal culture on Sabouraud’s dextrose agar (SDA).
20–25% of the world’s population [2]. Dermatophyte Examination of the infected scales from the leading edge of
infections are one of the earliest known fungal infections the lesion may reveal septate hyphae coursing through the
of mankind and are very common throughout the squamas [8]. Cultures incubated at room temperature should
world [3]. grow the causative organism within 2–4 weeks [9].
The prevalence of dermatomycoses has been studied in Knowledge of the zoophilic or anthropophilic origin of the
different parts of the world. The relative occurrence of dermatophyte may allow setting up prophylactic mea-
the etiologic agents of these infections varies from country sures such as treatment of cats, dogs, or pets whose
to country and from one climatic region to another [4]. owners develop skin disease [10]. Also, knowledge of the
Dermatophytosis is common in tropical countries and may predominant causative species provides a clearer under-
reach epidemic proportions in areas with a high rate of standing of risk factors for superficial fungal infections
humidity, overpopulation, and poor hygienic condi- and future epidemiologic trends [11]. The purpose of
tions [5]. Generally, dermatophytes exhibit a cosmopoli- this work was to find out the predominant etiological
tan problem; that is, they are found in different regions of agent(s) of tinea corporis to detect and record the current
the world with variations in the frequency of particular prevailing fungi of such condition in our area.
1687-1537 & 2015 Egyptian Women’s Dermatologic Society DOI: 10.1097/01.EWX.0000464890.25449.5e

Copyright r 2015 Egyptian Women’s Dermatologic Society. Unauthorized reproduction of this article is prohibited.
Study of tinea corporis Sorour et al. 181

Patients and methods history (five tinea circinata and three tinea capitis). Forty-
Fifty patients with clinical diagnosis of tinea corporis were one (82%) patients did not suffer from any other form of
randomly chosen to participate in the study after strict ringworm infection, whereas nine (18%) patients suffered
inclusion and exclusion criteria. The study was approved from other forms of tinea (four tinea cruris, two tinea
by the Al Azhar University Medical Ethics Committee, capitis, two tinea pedis, and one onychomycosis). Half of
and prior written informed consent was obtained from the patients (50%) had no history of animal contact,
every participant. For junior participants, consent was whereas 16 (32%) were in close contact with cats, five
taken from their parents/guardians. For every patient, (10%) with dogs, and four (8%) with sheep. Three
duplicate sets of skin scrapings were collected from the patients with Microsporum canis infection and one with
lesions. One set of skin scrapings was examined by direct Trichophyton verrucosum had a history of contact with cats,
microscopy and the other by culture. All cultures were whereas only one case with M. canis infection was exposed
done on Petri dishes. to a dog.
Regarding the site of the lesion, many patients showed
Direct microscopy lesions on the extremities (24 cases; 48%), followed by
After cleaning the lesion with 70% alcohol, skin scales were the face (12 cases; 24%), with the chest and trunk being
collected by scraping the affected site. The specimen was the least affected (six cases; 12% each). Only two (4%)
placed on a clean glass slide, and a drop of 20% KOH/40% cases showed disseminated lesions.
dimethyl sulfoxide mixture was added (dimethyl sulfoxide
increases the sensitivity of the preparation and softens The correlation between the mean duration of disease
keratin more quickly than KOH alone in the absence of and the isolated species showed that the longer disease
heat) [12]. A coverslip was applied with gentle pressure to duration was associated with Trichophyton rubrum infection
drain away excess solution. The sample was then examined (18.69 days), followed by T. verrucosum (17.5 days),
thoroughly for the presence of filamentous, septate, Trichophyton violaceum (16.17 days), Trichophyton tonsurans
branched hyphae with or without arthrospores. (12 days), M. canis (11.25 days), and Microsporum audouinii
(10 days).
Fungal culture
The second set of scrapings was inoculated onto two Mycological findings
types of SDA culture media: one with cycloheximide (to Direct microscopy was positive in 46 of 50 (92%) cases,
suppress the growth of contaminant fungi) and the other whereas mycological culture showed positive result in 45
without cycloheximide. Chloramphenicol was added to (90%) cases. Mycological culture has comparable sensi-
both culture media to prevent bacterial overgrowth. The tivity to that of KOH mount (90 vs. 92%). All culture-
media were then incubated in a warm, moist environment positive cases were also KOH positive. Only one case was
at 281C and examined regularly to detect growth of any KOH positive but culture negative.
fungus. Observation for growth was done periodically up
Microscopically positive KOH results were characterized
to 4 weeks, after which the cultures were reported as
by the presence of long tubular branched septated
positive or negative.
structures (hyphae) with or without arthroconidia.
Regarding the identification of dermatophytes, we relied Examination of the postculture mounts revealed T.
upon macromorphological and micromorphological char- violaceum (Fig. 1a and b) in 17 (34%) patients followed
acters of the isolates. The fungi were identified by noting by T. rubrum (Fig. 2a and b) (13 patients; 26%), M.
their growth rate, colonial macroscopic morphology, and audouinii (Fig. 3a and b) (five patients; 10%), M. canis
microscopic structures. Macroscopic examination in- (four patients; 8%), T. verrucosum (four patients; 8%), and
cluded color, size, texture, and topography of the colony. T. tonsurans (two patients; 4%) (Table 1).
The microscopic structures of fungi usually provide
Although M. audouinii and M. canis may share some
definitive identification [13]. Using the tease mount
macroscopic characters, the method we used for M.
technique, the following microscopic features were
audouinii identification depends mainly on microscopic
looked for: the type, size, shape, and arrangement of
morphology. In all isolated cases, there were no macro-
spores and the size, color, septation, and special shapes of
conidia, but microconidia were occasionally seen. Chla-
hyphae.
mydoconidia were common and presented mostly as
terminal and intercalary. The terminal ones have char-
acteristic pointed appearance at the tip (finger-like
Results projection) (Fig. 3b). Racquet and pectinate (comb-like)
Demographic and clinical findings hyphae were also observed. The above-mentioned
Out of the 50 patients with tinea corporis 29 (58%) were features are consistent with M. audouinii.
male and 21 (42%) were female. Their ages ranged from 1
to 55 years (mean ± SD 19.34 ± 13.1 years). The duration
of the disease ranged from 3 to 60 days (mean ± SD
Discussion
15.96 ± 9.3 days).
The epidemiology of most of the dermatophytic infec-
Forty-two (84%) cases had no family history of tinea tions has substantially changed over the last years. Some
infection, whereas eight (16%) cases showed positive species are distributed worldwide, such as T. rubrum,

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182 Journal of the Egyptian Women’s Dermatologic Society

Figure 1. Figure 2.

(a) Macroscopic morphology of Trichophyton rubrum: colonies are flat


(a) Macroscopic morphology of Trichophyton violaceum: colonies are to slightly raised, white to cream, suede-like to downy. (b) Microscopic
glabrous, heaped, folded, and deep violet in color. (b) Microscopic morphology of T. rubrum: typical smooth thin-walled cigar-shaped
morphology of T. violaceum: hyphae are relatively broad, tortuous, much septate macroconidia of T. rubrum (granular type). Water,  100.
branched, and distorted. No conidia are seen. Few chlamydoconidia are
present but these are usually numerous in older cultures. Water,  100.

and female individuals to pathogenic fungi. Despite a


Trichophyton mentagrophytes var. interdigitale, M. canis, and history of animal exposure in 40% of patients, the
Epidermophyton floccosum. Others have partial geographic majority of isolated organisms were anthropophilic
restriction, such as Trichophyton schoenleinii (Eurasia, species. This may denote that fungal infectivity is diverse
Africa), Trichophyton soudanense (Africa), T. violaceum (Africa, and heterogenous.
Asia, and Europe), and Trichophyton concentricum (Pacific
Islands, Far East, and India) [11]. There are very few data on Of the studied patients, 41 (82%) did not suffer from any
superficial mycoses from our region. Therefore, the present other type of tinea. The remaining nine had other
study was conducted to find out the predominant agents of associated forms of tinea, including tinea cruris in four
tinea corporis among 50 patients attending the Dermatology (8%) cases, tinea capitis in two (4%) cases, tinea pedis in
Clinic, Al-Hussein University Hospital, Cairo, Egypt. two (4%) cases, and onychomycosis in one (2%) case.
Some similarity is noticeable in the study conducted in
In the present work, although not significantly different, Rome by Panasiti et al. [18], in which tinea corporis, the
men were more affected than women (58 vs. 42%). prevalent dermatophytosis, was followed in frequency by
Similar result was reported by Ibrahim et al. [14]. Also, tinea cruris and tinea capitis. Corporal tinea may result
other reports showed a nonsignificant difference between from or contribute to other forms of ringworm infections.
male and female patients as in Kuwait [15] and
Mexico [16]. Other studies showed greater prevalence In this study, 48% of patients had skin lesions on the
of infection in the female population [6,17]. The reason extremities, 24% on the face, 12% on both the neck and
for these variations is not fully understood, but it may trunk, whereas 4% had disseminated disease. This result is
indicate that sex has an influence on susceptibility to in accordance with the result obtained by Nejad et al. [19],
particular forms of tinea. The acquisition of fungi may be who detected that patients had tinea corporis lesions on the
due to varied forms of outdoor/indoor exposure of male upper limbs (33%), lower limbs (27%), head (13%), face

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Study of tinea corporis Sorour et al. 183

Figure 3. (13%), trunk (9%), groin (9%), neck (3%), and nail (1%) in a
descending manner. The most involved areas affected by
tinea corporis are usually related to the site of maximum
exposure to sources of infection, such as the extremities and
face, whereas the least involved sites such as the neck and
trunk are somewhat more hidden and protected.
Of the 45 isolates, T. violaceum was recovered in 17 cases
followed by T. rubrum in 13 cases. This result is similar to
that of Ellabib et al. [20], who isolated T. violaceum and T.
rubrum as important causes of tinea corporis in Libya.
Epidemiological studies carried out in Egypt reported
high isolation rate of T. violaceum. Zaki et al. [21] reported
that the most frequently isolated dermatophyte species
was T. violaceum (71.1% of all recovered dermatophytes).
Amer et al. [22] demonstrated that T. violaceum was the
most commonly isolated pathogen (44%) in cases of
dermatophytosis in Al Sharkia Governorate. Also agreeing
with this study, Ansari and Siddiqui [23] in their
epidemiological study reported that T. violaceum was the
most prevalent organism, isolated in 41% of cases.
The increasing incidence of T. violaceum as a major cause
of tinea corporis in Egypt is probably because the fungus
is indigenous to North Africa [20]. T. violaceum has been
reported as the most common etiologic agent causing
dermatophytosis in Egypt [24]. Abdo et al. [25] and Azab
et al. [26] reported that T. violaceum was the chief isolate
from scalp infection (eight out of 35 and 21 out of 33,
respectively). Azab et al. [26] also isolated it from tinea
corporis lesions (three out of 33). In Egypt, large family
sizes, close familial contact, and sharing of personal items
such as hairbrushes, hats, and towels are common. This,
in addition to overpopulation, hot humid atmosphere, and
(a) Macroscopic morphology of Microsporum audouinii: colonies are
flat, spreading, grayish-white to light tan-white in color, and have a increased environmental exposure to fungi, may be
dense suede-like surface, which show some radial grooves. (b) responsible for the predominance of certain dermato-
Microscopic morphology of M. audouinii: typical terminal chlamydoco- phytes causing tinea infections. Dispersal of fungi from
nidia are often present, which have short, finger-like projections
showing a pointed appearance at the tip. Most cultures are sterile the patient’s scalp or foot lesions to the trunk and limbs
and macroconidia and microconidia are only rarely produced. Water, or from sharing of nonpersonal objects can also occur.
 200.
In contrast, Bhavsar Hitendra et al. [27] isolated T. rubrum as
the main dermatophyte (55.26%) from tinea corporis and
tinea cruris cases, followed by T. mentagrophytes (27.63%).
Table 1. Results of potassium hydroxide test and fungal culture They failed to isolate any T. violaceum from skin lesions.
n (%) Other studies also revealed that T. rubrum was the main
KOH test (n = 50) dermatophyte isolated from ringworm lesions, particularly
Result tinea corporis [5,28,29]. This difference in dermatophyte
Positive cases 46 (92) isolation could be explained by different samples of the
Negative cases 4 (8)
Total 50 (100) study population and again emphasizes the role of different
Fungal culture (n = 50) environmental conditions and degree of exposure to the
Result pathogens. The predominance of certain dermatophytes
Positive cases 45 (90)
Negative cases 5 (10) varies geographically depending on ethnicity and different
Total 50 (100) environmental factors such as climate, humidity, occupa-
Isolated fungi (n = 45) tion, and different lifestyles.
Isolated dermatophytes
Trichophyton violaceum 17 (34) On comparing the two methods of fungal detection, the
Trichophyton rubrum 13 (26)
Microsporum audouinii 5 (10) KOH test was found to be positive in 46 (92%) cases,
Microsporum canis 4 (8) whereas culture was positive in 45 (90%) cases, showing
Trichophyton verrucosum 4 (8) nearly similar sensitivity. This finding concurred with that
Trichophyton tonsurans 2 (4)
Total positive 45 (90) of Asticcioli et al. [30], who reported that the KOH test
No growth 5 (10) and fungal culture positivity was 96.9 and 100%,
Total 50 (100) respectively. In the literature, KOH versus fungal culture
KOH, potassium hydroxide. sensitivity has conflicting results. Abdelal et al. [31]

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184 Journal of the Egyptian Women’s Dermatologic Society

reported that KOH preparation has better sensitivity than et al. [14] that the isolation rate of M. audouinii was 46.42%
culture (67 vs. 46%). Abdo et al. [25], Bhavsar Hitendra (13 out of 28 isolates from different clinical types of
et al. [27], Patel et al. [28], Shenoy et al. [32], Ali et al. [33], dermatophytosis). Their result, however, is questionable.
and Nawal et al. [34] also reported higher KOH sensitivity The isolation of M. audouinii in Egypt could be explained
(85.70 vs. 60.00%, 68.16 vs. 20.15%, 62.12 vs. 29.29%, by the fact that, because of its anthropophilic nature, the
53.00 vs. 35.00%, 65.50 vs. 50.00%, and 72.40 vs. 62.80%, fungus is accessible to the general population who was
respectively). These results thus document that mycolo- exposed to it during their routine living conditions. This
gical culture is less sensitive than KOH mount; however, is particularly enhanced by the increased national and
the latter is unable to identify and isolate the causative international immigration.
dermatophytes. On the other side, high culture positivity
Although the dysgonic strains of M. canis are rare,
was depicted in studies showing culture as the better
sometimes it is necessary to differentiate them from M.
method of detection of fungi from clinical samples. Sen
audouinii. Dysgonic M. canis colonies are typically heaped
and Rasul [35] showed that out of 100 samples 49 (49%)
and folded and yellow-brown in color, whereas those of M.
were positive by direct KOH examination, whereas
audouinii (on SDA) are flat, spreading, grayish-white to
culture was positive in 51 (51%) cases. Ansari et al. [36]
light tan-white in color, and have a dense suede-like to
reported positive KOH mount in 34 (68%) samples,
downy surface, which may show some radial grooves
whereas fungal culture was positive in 37 (74%) of the 50
(Fig. 3a). Similar to M. audouinii, macroconidia are usually
samples tested.
absent in these strains. However, typical colonies and
In this study, only one (2%) case was KOH positive but macroconidia of M. canis are usually produced by this
culture negative. Conversely, Asticcioli et al. [30] isolated variant when subcultured onto polished rice grains [37].
3.1% of dermatophytes from skin scrapings that were The poor growth of M. audouinii on rice grains serves to
negative for fungal filaments on KOH examination. They distinguish the species from M. canis. Also, M. audouinii
explained this by the probability that fungal elements does not perforate hair, whereas M. canis does [38].
were few and were missed in the observation. In any In conclusion, the isolated anthropophilic dermatophytes
study, the high percentage of positivity of either method outnumbered zoophilic agents as a cause of tinea corporis
depends mainly on strict criteria of patient selection, in our locality. T. violaceum was the most common
good sample collection and processing, and the profes- etiological agent responsible for 34% of the cases.
sional experience of the investigators. Although this finding matches with many studies, it
In our opinion, cultures can be false negative for several differs significantly from others. We recommend further
factors: (i) fungi may be present in the specimen but not nation-wide epidemiological research highlighting the
viable, or because only a small specimen was taken; (ii) if socioeconomic factors attributed to the prevalence of
the fungi were alive in the tissue, they may have died superficial fungal infections to find out in more detail the
during sample transportation, processing, or culturing; species responsible for such infections.
(iii) the patient may have already had some form of
antifungal treatment; and (iv) cycloheximide can some-
times inhibit the growth of some fungi. Therefore, in the Acknowledgements
presence of lesions suspected to be mycotic, it is useful to Conflicts of interest
perform direct microscopic examination besides culture There are no conflicts of interest.
to aid the diagnosis. In this situation, if there is a positive
direct KOH test and a negative culture, there are two
explanations: (i) the KOH test may be falsely interpreted
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