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Turkish Journal of Medical Sciences Turk J Med Sci

(2015) 45: 820-826


http://journals.tubitak.gov.tr/medical/
© TÜBİTAK
Research Article doi:10.3906/sag-1407-17

Epidemiology, causative agents, and risk factors affecting human


otomycosis infections
1 2 1 2,
Metwally ABDELAZEEM , Ahmed GAMEA , Hanan MUBARAK , Nessma ELZAWAWY *
1
Department of Botany, Faculty of Science, Tanta University, Tanta, Egypt
2
Department of Otorhinolaryngology, Faculty of Medicine, Tanta University, Tanta, Egypt

Received: 04.07.2014 Accepted/Published Online: 15.11.2014 Printed: 30.07.2015

Background/aim: Otomycosis, or fungal otitis externa, has typically been described as fungal infection of the external auditory canal,
with infrequent complications involving the middle ear. This study assessed a mycological analysis of fungal debris from external
auditory canals of patients at Tanta University Hospital, Gharbia Governorate, Egypt.
Materials and methods: The samples were collected over a year from the 110 patients that were clinically diagnosed to have otomycosis.
The samples were then inoculated and culture plates were examined for the presence of fungal growth.
Results: The results showed that Aspergillus niger was the most common fungus causing otomycosis. It was more common among males
aged 21–40 years. The incidence was higher in the summer and spring seasons. Manual workers and students had the highest frequency
based on occupational incidence. The most common presenting complaint was itching. Trauma to the external auditory canal was the
most common predisposing factor.
Conclusion: The epidemiological profile of otomycosis infection varied according to different factors in the study population.

Key words: Otomycosis, Aspergillus niger, clinical features

1. Introduction infection is prevalent in Brazil and constitutes about 30%


Otomycosis is a subacute or chronic fungal infection of the of the mycotic diseases of the external auditory canal
external auditory canal with some complications involving (3). Otomycosis is also frequently seen in Turkey (4). In
the middle ear. Egypt, there has been no recent survey on otomycosis
There are several factors that play important roles in epidemiology, risk factors, and complications. The last
otomycosis infection, such as humidity, moisture, high study recorded was that of Hammad (5) on otomycosis
temperature, the entrance of water into the ear during in the El-Minia University hospitals, where he locally
swimming or sweat secretions, increased use of topical diagnosed otomycosis through direct examination by
antibiotics, weak immune function, and cleaning of ear otoscope, and collected 250 otomycotic fungal samples
wax (1). over a 12-month period without any detailed identification
Molds and yeasts are common in the auditory canals studies or new approaches in the treatment with natural
of otomycosis patients. The predominance of thermophile products.
Aspergillus and Candida species are related to the
inflammatory processes of the ear. The molds mostly 2. Materials and methods
isolated from the ear are Aspergillus niger, Aspergillus 2.1. Study group
fumigatus, Aspergillus flavus, Aspergillus nidulans, Mycological analysis was carried out on debris, scrapings,
Aspergillus terreus, Mucor species, and Penicillium species or exudate samples from the auditory canals of 110
(2). patients clinically diagnosed to have otomycosis infection.
Otomycosis has a worldwide distribution. It is This was achieved by visiting the outpatient clinic of the
estimated that approximately 25% of the total cases of otorhinolaryngology department twice a week during
ear infections are due to fungi, and the disease was more a year from January 2011 to December 2011 at Tanta
prevalent in warm and humid climates. Otomycosis University Hospital, Gharbia Governorate, Egypt.
* Correspondence: dr.nessmaelzawawy@yahoo.com
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Data collected and analyzed included duration of A. niger and A. flavus, respectively. Table 2 shows the
follow-up, presenting symptoms, disease complications, distribution of otomycosis among different age groups,
fungal species identified, history of patients, and prior as 10 cases of otomycosis were detected in the age group
treatments. Statistical analysis was carried out using a of <10 years old, while 40 cases were detected in the age
Pearson chi-square test to evaluate the significance of all group of 11–20 years, 50 cases were detected in the age
the studied factors and the spread of otomycosis. group of 21–40 years, and 10 cases were detected in the
2.2. Collection of samples age group of >40 years. Figure 2 shows that otomycosis
The samples were collected from patients that were was more common in males (63.5%) compared to females
clinically diagnosed to have otomycosis under aseptic (36.5%).
conditions with the help of a sterile cotton swab from the Statistical analysis revealed that the differences
external auditory canal or a sterile scalpel blade (6). between the patient’s age and sex were highly significant
2.3 Culture at P <0.001. The data represented in Table 3 shows that
Samples were inoculated on Sabouraud dextrose agar otomycosis was more common among manual workers
medium; the plates were incubated at 25 °C. The culture (50 cases), followed by students (40 cases) and housewives
plates were examined for the presence of growth after 3–4 (15), but less common among farmers (5 cases). The
days (7). highest incidence of otomycosis was observed in summer
2.4 Identification (60 cases), followed by spring (28 cases). Autumn (15 cases)
All cultured plates were examined under microscope and winter (7 cases) showed a low incidence of otomycosis
(400× and 1000×), photographed, and identified according (Figure 3). Figure 4 shows that the predominant complaint
to methods previously described (8–12). of the patients was itching (100%), followed by pain (41%)
and hearing loss (31.8%), and the least common complaint
3. Results was ear discharge (18.2%). Nine percent of patients had all
Otomycosis was clinically diagnosed in 110 patients and complaints.
confirmed by positive culture results for fungal growth. The most common predisposing factor was traumatic
Table 1 shows that the most common fungi isolated injury to the ear canal (59%), followed by water entry
from otomycosis cases during the present survey was A. during swimming (45%) (Table 4). Table 4 also shows the
niger (it was positively isolated from 100 cases), followed by high percentage of antibiotic ear drop treatment (59%)
A. flavus, which was isolated from 10 cases of otomycosis affecting the incidence of otomycotic infection and that it
and showed a low incidence in the present study. was more common in patients with systemic diseases (e.g.,
Figures 1A and 1B show the otoscopic direct hypertension, diabetes, or an immune disease) .
examinations of external ear canals of different otomycosis Finally, wax was absent in 91% of cases and present in
patients. Subfigure 1 of Figure 1A shows one of the severe 9% of cases. This means that wax plays an important role
cases of otomycosis with tympanic membrane perforation in protecting patients against otomycosis (Figure 5).
due to A. niger infection. Subfigure 1 of Figure 1B presents All these studied factors were found to be highly
otomycosis due to A. flavus infection. In addition, significant at P < 0.001 in distinguishing the variation
subfigures 2 and 3 of Figures 1A and 1B represent the among otomycosis cases, which was confirmed by a chi-
pure culture and the microscopic examination of isolated square test as shown.

Table 1. Distribution of fungal isolates among otomycotic cases during the year of the
survey (2011).

Fungal isolate No. of cases Percentage of total cases


Aspergillus niger (Tiegh, 1867) 100 91
Aspergillus flavus (Link, 1809) 10 9
Total 110 100
χ2 72.009
Chi-square
P-value <0.001*

*P-value is statistically highly significant at the 0.001 level.

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Figure 1. Otoscopic, culture, and microscopic appearance of A. niger (A-1, -2, and -3) and A. flavus (B-1, -2, and -3).

Table 2. Distribution of otomycosis among different sex and age groups during the year of the survey (2011).

No. of cases
Percentage of total
Age group Sex
Total cases
Male Female
≤10 5 5 10 9.0
11–20 15 25 40 36.5
21–40 40 10 50 45.5
41–60 10 0 10 9.0
Total 70 40 110 100
Percentage of total cases 63.5 36.5 100 100
χ2 24.112
Chi-square
P-value <0.001
*P-value is statistically highly significant at the 0.001 level.

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Female = 36.5%

Male = 63.5%

Figure 2. Percentage of otomycosis among different sexes during the year of the survey (2011).

Table 3. Distribution of otomycosis among different occupational careers during the


year of the survey (2011).

Occupational career No. of cases Percentage of total cases


Manual workers 50 45.5
Students 40 36.5
Housewives 15 13.5
Farmers 5 4.5
Total 110 100
χ2 48.182
Chi-square
P-value <0.001*

*P-value is statistically highly significant at the 0.001 level.

Autumn
Winter
=15 cases=
=7 cases=6.4%
13.6%

All= 10 cases =
Spring 9%
=28 cases=
25.5% Ear discharge=
20 cases = 18.2%
Pain
= 45 cases =41%

Summer Hearing loss


=60 cases= =35 cases=
54.5% 31.78%
Figure 3. Seasonal incidence of otomycosis during the year of the Figure 4. Incidence of different complications accompanying
survey (2011). otomycosis during the year of the survey (2011).

4. Discussion common reason for all otomycosis cases representing


Otomycosis has been observed to be a common disease many complications. These records were similar to those
in patients applying to the outpatient clinic of the of Tang et al. (13), as they recorded 90 cases of otomycosis
otorhinolaryngology department at Tanta University in Texas over 12 months. Moreover, Ashish (14) stated
Hospital, Tanta, Egypt. In the present survey, a total of that the incidence of otomycosis was noticeable in India;
110 cases were recorded with otomycosis over 12 months he reported 102 cases of otomycosis during 1 year. On the
(January–December 2011). Fungal infection was the other hand, only 26 cases of otomycosis were recorded in

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Table 4. Effect of different predisposing factors on the incidence of otomycotic infections during the year of the
survey (2011).

Predisposing factors Study parameters No. of cases Percentage of total cases


Water entry during swimming 45 41.0
Source of infection Traumatic injury of canal wall 65 59.0
Total 110 100
χ2 3.28
Chi-square
P-value 0.07
Antibiotic 65 59.0
Wax solvent 25 22.8
Eardrop treatment
None 20 18.2
Total 110 100
χ 2
33.182
Chi-square
P-value <0.01
Diabetes 60 54.5

Associated systemic Hypertension 30 27.3


diseases None 20 18.2
Total 110 100
χ2 9.344
Chi-square
P-value 0.002
Wax present 10 9.0
Wax formation Wax absent 100 91.0
Total 110 100
χ2 72.009
Chi-square
P-value <0.003

*P-value is statistically significant at the 0.005 level and highly significant at the 0.001 level.

New York by Jackman et al. (15) in about 12 months. This was the most common isolated species in otomycosis,
may be due to the high humidity in the eastern region followed by A. fumigatus. These differences could be due
throughout the year. The epidemiology of otomycosis to the geographic patterns of fungi in different places, but
varies geographically, but it commonly occurs in warm limited epidemiological data are available for comparison.
and tropical climates. Regarding the age and sex distribution, the present
The most common fungal species isolated from survey revealed that otomycosis was more common
otomycosis cases in the present survey was A. niger (91%), among patients between 21 and 40 years of age (45.4%)
followed by A. flavus (9%). This was similar to many and higher in males (63.6%) than females (36.4%). That
screening reports for otomycosis in many regions of the could be explained by the increased outdoor activities of
world. Hoshino and Matsumoto (16) isolated A. niger males compared to females in Egypt; thus, males are more
as an abundant causative organism of otomycosis from exposed to the risks of diseases. This result could also be
all their cases. This was contrary to the observations of attributed to the difference in surface lipids between males
Jackman et al. (15), as they revealed that Candida albicans and females, as surface lipids are under the control of sex

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ABDELAZEEM et al. / Turk J Med Sci

could be explained by the warmer climate, wind, and


Wax present other environmental factors suitable for fungal growth
= 10 cases = 9% and the establishment of infection. All the patients in our
study (100%) presented with itching, and other common
complaints were pain (41%), hearing loss (31.8%), and
ear discharge (18.2%). The aforementioned complaints
and their incidence were in accordance with the findings
of Ashish (14). Although pain tended to be the dominant
complaint in bacterial infections, the most common
complaint in otomycosis was severe itching sensations
deep inside the canal.
The predisposing factors taken into consideration
were a history of swimming or water entering the ear
canal while bathing, normal or ritualistic dips in rivers or
ponds, the use of local antibiotic or steroid drops, trauma
to the external canal, or any associated medical disease.
The most predominant predisposing factors were trauma
Wax absent to the external canal, swimming, and the use of antibiotic
= 100 cases = 91% drops. Trauma was caused by of use of match sticks or
finger tips to clean the external canals, aural syringing,
Figure 5. Effect of wax formation on the incidence of otomycotic or poorly maintained mastoid cavity. The percentage of
infections during the year of the survey (2011). patients in this group was 70%. A history of swimming
in local ponds or swimming pools was present in 50% of
hormones. These findings were relatively close to those of a cases as a predisposing factor, and these findings were in
previous study in Texas, which recorded that the incidence accordance with the study of Ahmed (17), who found 72%
of otomycosis in males (56%) was higher than that in of cases due to trauma and 45% due to swimming. The
females (44%) aged up to 30 years old (13). In contrast, lipid mantle layer formed by the cerumen in the external
Ahmed (17) found that otomycosis affected female patients canal has long been considered as the key factor for the
at the ages of 11 to 30 years more than males. The ages of protection of the canal wall, and its removal by frequent
patients with otomycosis varied in several reports, and this irrigation of the external layer is thought to be the reason
could be explained by the periodic activity of sebaceous why frequent bathing in tropical climates is incriminated
glands, eccrine glands, and apocrine glands. Changes in as a cause of recurrent otomycosis.
the water content and the pH of the ear canal have also In the present study, 65% of the patients had a history of
been shown to affect the survival of fungus. the use of antibiotic drops. This was in accordance with the
The distribution of otomycosis among patients of study of Fasunla et al. (18), who found 42% of cases with
different occupations could be explained by the greater the same predisposing factor. However, this was not similar
possibility of manual workers to be exposed to otomycosis, with Pontes et al. (19), who noted that there has been no
as they are faced with surroundings such as machinery, significant increase in the incidence of otomycosis with the
foundries, and moving parts of machines, which generate widespread use of topical combinations of antibiotic and
heat and thus prepare the conditions to become an ideal steroid drops. There is also a weak relationship between
hot, humid, and dusty atmosphere, suitable for initiation otomycosis infection and other systemic diseases such as
of the disease. This was followed by students, who play diabetes, hypertension, and pregnancy, as supported by
sports on playgrounds where dust containing fungal Ahmed (17). Furthermore, 91% of otomycotic cases in the
spores mixes with the air of the atmosphere and acts as present study had no cerumen in the external canal and
a predisposing agent for the initiation of the disease. The this was in accordance with the study of Pontes et al. (19),
next group of moderate incidence is housewives from who showed that ear wax contains numerous amino acids
surrounding villages and towns, as they frequently clean and lysozymes that have an inhibitory effect on fungi.
and sweep the house floors and are exposed to a similar It was concluded that the overall clinicomycological and
environment, followed by farmers. All these findings were epidemiological profile of otomycosis infection observed
supported by Ahmed (17). at Tanta University Hospital, Tanta, Egypt, does not differ
This study shows that otomycosis was more common significantly from those observed by previous researchers
in the summer (54.5%) and spring (25.5%) than in around the world, and any variation is probably due to the
autumn or winter (13.6 and 6.4%, respectively). That differences in climates of the different study populations.

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ABDELAZEEM et al. / Turk J Med Sci

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