Bacterial agents of the discharging middle ear among children seen at the University of Nigeria Teaching Hospital, Enugu
Gideon Chukwudalu Ilechukwu1, Chioma Azuka Ilechukwu1, Agozie Chukwunedum Ubesie2,&, Ijeoma Okoroafor3, Basil Chukwuemeka Ezeanolue3, Ngozi Chinyelu Ojinnaka2
1Department of Paediatrics, Whiston Hospital, Prescot, United Kingdom, 2Department of Paediatrics, University of Nigeria,University of Nigeria Teaching Hospital, Enugu, 3Department of Otorhinolaryngology, University of Nigeria/University of Nigeria Teaching Hospital, Enugu
Agozie Chukwunedum Ubesie, Department of Paediatrics, University of Nigeria,University of Nigeria Teaching Hospital, Enugu
discharging middle ear continues to be one of the commonest problems seen in the developing world. There is an ever growing need to carry out studies periodically to determine the common bacterial agents responsible for discharging otitis media and their antibiotic sensitivity especially in set-ups characterized with minimal laboratory services. The study sought to determine the common bacterial agents causing discharging middle ear among children presenting at the University of Nigeria Teaching Hospital, Enugu and their sensitivity to the commonly available antibiotics.
middle ear swabs were collected from 100 children aged 1 month to 17 years at the Children Out-Patient and Otorhinolaryngology Clinics of the University of Nigeria Teaching Hospital, Enugu, Nigeria. The specimens were cultured for aerobic bacterial organisms and their sensitivity determined.
among those with acute discharge, Staphylococcal aureus was isolated in 31.3% and Proteus species in 25.0%. In chronically discharging ears, Proteus Species dominated (39.1%), followed by Staphylococcal aureus (28.3%).
Staphylococcal aureus and Proteus species were the commonest bacterial
agents in acute and chronic otitis media respectively. Most isolates showed
high sensitivity to the fluoroquinolone antibiotics.
Otitis media is one of the most common infectious diseases of childhood
worldwide . It is the inflammation of the mucous
membrane of the middle ear cleft which includes the middle ear
cavity, mastoid antrum, the mastoid air cells and the Eustachian
When the inflammation is associated with a discharge from the ear
through a perforation in the tympanic membrane or via a ventilatinig
(or discharging) otitis media results. Otitis media may be acute
(less than 6 weeks) or chronic (at least 6 weeks) .
Discharging ear or otorrhea is drainage exiting the ear which may
be serous, serosanguineous,
or purulent . Bacteria have remained the most important
aetiological agents in suppurative or discharging otitis media.
While non-typable Haemophilus
influenzae, Streptooccus pneumonia and Moraxella catarrhalis are
commonly reported as aetiological agents in acutely discharging
ears in the developed countries , local studies done
in Nigeria suggest that Moraxella catarrhalis is not a predominant
organism in acutely discharging otitis media in Nigerian children
aeruginosa is commonly implicated in chronic discharging otitis media
in Nigerian children [5, 6].
Complications of discharging otitis media are numerous and include hearing
impairment, mastoiditis, facial nerve paralysis, cholesteatoma,
tympanosclerosis, bacterial meningitis and brain abscess, to mention
a few. Treatment of otitis
media is usually based on empiric knowledge of aetiologic organisms
and their sensitivity pattern. There is emerging evidence of multi-drug
of bacterial isolates with reduction in antibiotic efficacy [7, 8].
Many paediatricians and general practitioners base their treatment
of otitis media on empiric evidence of the aetiologic agents and
their sensitivities to various antimicrobial agents. In view of
these, it is important
the trend in Enugu, to aid in appropriate treatment of this condition
and help prevent its complications which may arise if otitis media
is not treated
or is improperly treated. This paper therefore, aims to present
the aerobic bacteriological agents (and their antibiotic susceptibilities)
in discharging ears of children in Enugu.
study was conducted at the Children Out-Patient and Otorhinolaryngology Clinics of the University of Nigeria Teaching Hospital, Enugu, Nigeria.
the convenience sampling technique was used: each consecutive patient seen at
the Paediatric and Otorhinolaryngology clinics with ear discharge with or without
other symptoms of otitis media was recruited. Data were collected between July
and September 2007.
Sample size calculation:
the sample size was calculated using the formula: N= Z2 p(100-p)/D2.
Where N = minimum sample size,
Z = confidence interval (1.96),
P = prevalence with reference to a previous study (6%),
D = standard error (5%).
Substitutions in the above formula give a minimum sample size of 87 participants.
Adding an attrition rate of 10% will bring the minimum sample size to 96 participants,
rounded up to 100 participants
the participants were 100 children aged 0 to 17 years who presented who presented
with discharging middle ear. Children with foreign bodies in or infection of
the external auditory meatus were excluded; as well as those who had taken antibiotics
within the preceding two weeks to their presentation.
a structured questionnaire designed for this study was used to record information
on participants by two of the researchers. A pilot study to test information
collection tool was conducted on 35 patients who qualified for the inclusion
criteria. Information collected included the child's name, age, sex, place of
abode, parents' educational level and occupation, presenting symptoms of the
patient, duration of ear discharge and immunization status of the patient. After
otoscopic examination to document presence of perforated tympanic membrane and
pus in the middle ear, the external ears were cleaned with normal saline and
70% alcohol solution and allowed to dry for 1-2 minutes. After this, an ear
swab from the discharging ear was taken with the aid of sterile cotton-tipped
applicators taking care not to touch the skin of the external auditory meatus
to limit contamination of the specimen. In patients with bilateral discharging
otitis media, samples were collected from only one ear which was preferred by
the patient or mother. The swabs were then quickly transported to the microbiology
laboratory of the Eastern Nigeria Medical Center Enugu, a nearby specialist
center located very close to the University of Nigeria Teaching Hospital Enugu.
Sample processing and analysis:
samples of the ear discharge were promptly plated onto freshly prepared chocolate,
blood and cystine-lactose-electrolyte-deficient (CLED) agar. The blood and cystine-lactose-electrolyte-deficient
(CLED) agar plates were incubated aerobically at 37o
C for 24 hours
while the chocolate agar plates were incubated microaerobically using the candle
]. After the 24 hour incubation period, the plates
were examined for growth and individual colonies were further analysed for their
physical characteristics such as morphology, colour (pigmentation), odour and
in case of blood agar, haemolysis. No anaerobic cultures were carried out and
mycobacteria were not searched for because of unavailability of the required
laboratory materials. A Gram stain was carried out on all cultured isolates.
Thereafter, characterization to species level was carried out using standard
bacteriological methods [10
]. Antibiotic susceptibility
tests with multi-discs were carried out for various drugs using the disc diffusion
]. Choice of the antibiotics to be tested for
was based primarily on knowledge of commonly available antibiotic discs. Zones
of inhibition for each antibiotic, if formed were then measured to the nearest
millimeter and documented. Interpretation of these results in terms of resistance
or susceptibility was according to accepted protocol [10
ethical Clearance for this study was obtained from the ethical committee of the
University of Nigeria Teaching Hospital Enugu before the study was commenced.
Informed written consent was obtained from parents and guardian of the participants
and assent was obtained from children where appropriate.
data were entered into a computer database and were analyzed using SPSS version
11.0. Chi-square tests (χ2
) were used to test for significance;
and probability value (p-value) of less than 0.05 was taken as being statistically
The subject were aged 1 month to 17years (median 3 years). The male:
female ratio was 1:0.9. Majority of the participants (70%) were
aged 1month to 5years while 30 (30%) were between 6 and 17years. Fifteen
were from the upper socio-economic class, while 32 (32.0%) and
53 (53.0%) participants were from the middle and lower socio-economic class
Ninety-one (91.0%) ear swab samples grew isolates on culture while
9(9.0%) were sterile. Out of these 91 samples with positive bacterial yield,
samples yielded multiple isolates while the rest 88(96.7%) yielded
single isolates on culture. On the whole, 94 isolates were got from the
cultures. Forty (42.6%) were gram positive; whereas 54(57.4%) were
Among the isolates from patients with acute discharging otitis media, gram positives
constituted 43.8% while gram negatives formed 56.3% of them. The
leading organisms in acutely discharging ears were: staphylococcus aureus15(31.3%)
followed by Proteus species 12(25.0%), and then by Pseudomonas aeruginosa11(22.9%)
Among the 49 cases of chronically discharging
otitis media, gram positive and gram negative organisms accounted
for 41.3% and 58.7% of them respectively.
The commonest causative isolated agent in these chronic cases
was Proteus species 18 (39.1%), followed by Staphylococcus aureus13(28.3%).
Others were Pseudomonas aeruginosa6(13.0%), Streptococcus
Klebsiella species 3(6.5%) and Non haemolytic Streptococcus 1(2.2%)
1). No significant difference was found among the isolates cultured
in acute and chronic discharging ears (Table
As otitis media in children is documented to be commonest in children less
than 5 years , the pattern of bacterial isolates
in those less than 5 years of age and in those at least 5 years
of age was
sought as is depicted in Table
2. No relationship of statistical significance was observed when
chi-square (with Yates correction for continuity) was calculated
for the different organisms. Staphylococcus aureusand Streptococcus
showed 95.7% and 100% sensitivity respectively to ofloxacin;
and 75.0% and 100.0% sensitivity
respectively to gentamycin. Cloxacillin, and amoxicillin-clavulanate combination
were also seen to show good in vitro activity against Staphylococcus aureus.However, Staphylococcus
aureusand Streptococcus pneumonia were poorly sensitive to some
other commonly used antibiotics like cefuroxime, co-trimoxazole and amoxicillin
Proteus species and Pseudomonas aeruginosa showed 95.5% and 100.0% sensitivity
respectively to ofloxacin; and on the other extreme, they were both 100.0%
resistant to cloxacillin. However, gentamycin and to a lesser extent, chloramphenicol
good antibacterial activity against them. While Proteus was 100.0% sensitive
to ceftriaxone, Pseudomonas aeruginosawas only 66.7% sensitive to it
3). In general, all the major isolates showed excellent in vitro sensitivity
to ofloxacin, and ciprofloxacin.
It was noted in this study that Staphylococcus aureuswas the leading
isolate among the acute cases of discharging otitis media, closely
followed by Proteus species and Pseudomonas aeruginosa.This pattern
seems to resemble observations by different researchers in Nigeria
but does not mimic the trend in the developed world where non-typable Haemophilus
influenzae, Streptococcus pneumoniae and Moraxella catarrhalis assume
important predominant roles in acute otitis media [4, 11, 12].
Among the chronic cases of discharging otitis media, Proteus species
was the leading causative isolate, followed closely by Staphylococcus aureus,
and Pseudomonas aeruginosa.These three organisms seem to be the predominant
ones in Europe, Middle East,  United States of America
and within Nigeria [5, 14, 15]. Streptococcus
pneumoniae was a less common isolate in this study; and this was likewise
observed in Lagos . The pattern of cultured isolates
in chronically discharging ears is nearly similar to that observed
by Tiedt and colleagues  in South Africa where the
commonest isolates were Proteus Mirabilis, Pseudomonas aeruginosa and Haemophilus
influenzae. The overall picture of bacteriology in this study also compares
with the study carried out by Abera and Kibret in Ethiopia 
and suggests that geographical location has a large part in the aetiology
of discharging otitis media. Type of ear discharge did not seem to
affect or influence the causative agent. Again, age of participants
did not seem
to have any bearing on the pattern of bacterial isolates. There is
paucity of information in the literature regarding the possible role
of age on the
bacteriology of discharging otitis media.
All the major isolates showed excellent in vitro sensitivity to the fluoroquinolone
group of antibiotics (which in this study are ofloxacin and ciprofloxacin). This
observation is same as that noted by Oni and fellow workers 
in Ibadan. Although gentamycin and chloramphenicol had moderately good in vitro
activity against Staphylococcus aureus and Streptococcus pneumoniae in
this study, the research by Ako-Nai and colleagues  in
Ile-Ife showed that these gram positive organisms were only weakly susceptible
to gentamycin and chloramphenicol in vitro.
However, the number of isolates
tested for sensitivity to gentamycin were five and three for Staphylococcus
aureus and Streptococcus pneumoniae respectively, compared with
twenty-eight and eight in this index study. This difference in number of isolates
well be a potential source of bias. On the other hand, in Ibadan (Nigeria)
and in Ethiopia , gentamycin was noted to have good
antibacterial effectiveness against Staphylococcus aureus. The varying
sensitivity of isolates to particular antibiotics found within a country and
may well be a result of chronic and perhaps appropriateness of exposure of
organisms to antibiotics. The fluoroquinolone group of antibiotics is a broad-spectrum
class, which acts by inhibiting Deoxyribonucleic acid (DNA) gyrase. Its coverage
includes the organisms most commonly associated with otitis media (Streptococcus
pneumoniae regardless of susceptibility to penicillin, Haemophilus influenzae, Moraxella
catarrhalis regardless of β-lactamase status, Pseudomonas aeruginosa and Staphylococcus
aureus) . Resistant strains are however emerging
Systemic use of this group of antibiotics has been limited in children because
of the observation that these antibiotics, when administered systemically,
may have an adverse effect on the development of weight-bearing joints in juvenile
animals [18, 19].
Ohyama and co-workers 
in Japan demonstrated that 0.3% ofloxacin otic solution was efficacious without
ototoxic effects in discharging otitis media of the chronic variety. Again,
Dohar and fellow workers  showed that otic formulation
of 0.3% ofloxacin in a dose of 0.25ml twice daily for 10 days eradicated
in 96.3% of the participants tested without much adverse effects. Many researchers
have documented good in vitro efficacy of gentamycin against Pseudomonas
aeruginosa, Klebsiella species and Proteus species [5-7].
Indeed, Coker and colleagues  had observed that gentamycin
appeared to be the most effective antibiotic against strains of Pseudomonas
aeruginosa, Proteus and Klebsiella species and went on to recommend its
topical application in chronic forms of middle ear discharge. Wariso and
in Port Harcourt and some other researchers in Ethiopia 
also recommended it as the first drug of choice in treating chronic otitis
The results of this study suggest that there exists
a high level of resistance
of bacterial isolates to a number of commonly used antibiotics like cloxacillin,
amoxicillin, erythromycin, ampiclox, co-trimoxazole, amoxicillin-clavulanate
and even cefuroxime in in vitro testing. The increasing prevalence
of multi-drug resistant bacteria is of epidemiological importance especially
in attempts to control infection in the event of an epidemic caused by these
agents. Such resistance may have arisen due to injudicious use of antibiotics
especially as they are commonly used as 'over-the-counter'drugs with
no qualified medical personnel's prescription. It is therefore being recommended
that the Ministry of Health should restrict injudicious sale of antibiotics.
They should only be sold on qualified health personnel's prescription to minimize
their abuse. We also recommend that for acutely discharging ears, systemic Ofloxacin
or ciprofloxacin could be used as the drug of choice until ear swab bacteriologic
results are out. Gentamycin or ofloxacin or ciprofloxacin could serve as logical
choice in chronically discharging ears until swab culture and sensitivity results
Staphylococcal aureus and Proteus species were the most common bacterial agents in acute and chronic otitis media respectively. Fluoroquinolones were found to be effective in their treatment.
What is known about this topic
- Bacterial agents are known causes of both acute and chronic otitis media. Antibiotic therapy is key in the management of otitis media. In resource poor countries like Nigeria, empirical therapy is not uncommon, hence the need for implicating agents and susceptible antibiotics.
What this study adds
- This study shows that the leading organisms in both acutely and chronically
discharging otitis media among Nigerian children were Staphylococcal aureus and
Proteus species, these organisms were more sensitive to fluoroquinolones group
of antibiotics and should now be the first-line antibiotic management of otitis
media among Nigerian children.
The authors declare no competing interests.
Gideon Chukwudalu Ilechukwu, Chioma Azuka Ilechukwu, Agozie Chukwunedum Ubesie , Ijeoma Okoroafor , Basil Chukwuemeka Ezeanolue and Ngozi Chinyelu Ojinnaka conceptualized and designed the study. Gideon Chukwudalu Ilechukwu and Chioma Azuka Ilechukwu collected the data. Gideon Chukwudalu Ilechukwu,Chioma Azuka Ilechukwu, Agozie Chukwunedum Ubesie and Ngozi Chinyelu Ojinnaka did data analysis. All the authors participated in writing, re-writing and approval of the final manuscript.
We are thankful to the children and their families who participated in this study. Our gratitude also goes to the Medical Laboratory Scientist, Mr Chris Ireoba.
Table 1: frequency distribution of cultured isolates in participants with acute and chronic discharging otitis media and their p-values
Table 2: pattern of bacterial isolates in different age groups and their probability values
Table 3: antibiotic sensitivity and resistance of principal isolates to some common antibiotics
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