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Contents lists available at SciVerse ScienceDirect

International Journal of Pediatric Otorhinolaryngology

journal homepage: www.elsevier.com/locate/ijporl

Bacteriology of chronic suppurative otitis media (CSOM) in children in Garissa

district, Kenya: A point prevalence study
Dickens S.O. Aduda a,*, Isaac M. Macharia a, Peter Mugwe a, Herbert Oburra a, Brian Farragher b,
Bernard Brabin c, Ian Mackenzie d
a
University of Nairobi, School of Health Sciences, Department of Surgery, ENT/Head & Neck Surgery, Kenya
b
Liverpool School of Tropical Medicine, Medical Statistics, United Kingdom
c
Liverpool School of Tropical Medicine, Department of Tropical Paediatrics, United Kingdom
d
Liverpool School of Tropical Medicine, Aintree Hospital Foundation Trust, United Kingdom

A R T I C L E I N F O A B S T R A C T

Article history: Objectives: To identify by type and sensitivity to drugs the bacteria found in ears of school-going children
Received 11 January 2013 with chronic otitis media in Garissa district.
Received in revised form 12 April 2013 Methods: Study design: This was a descriptive prevalence study of CSOM bacterial flora in eligible ears
Accepted 15 April 2013
conducted among a cohort of children attending public and private primary as well as Islamic religious
Available online xxx
schools, screened for chronic ear discharge in Garissa district, Kenya. Procedure and bacteriological
techniques: We used sterile swab-sticks to collect a specimen of the discharge from eligible ears of
Keywords:
consenting pupils at the induction stage of the zinc supplementation trial for treatment of chronic
Bacteriology
Aerobic and anaerobic bacteria
suppurative otitis media conducted between January and July 2010. All pupils below 18 years present on
Chronic otitis media day of visit were eligible. Both aerobic and anaerobic bacterial cultures were done to identify clinically
Antibiotic sensitivity and epidemiologically important bacteria. Sensitivity tests were based on disc diffusion methods.
School-going children Results are presented as frequencies and proportions.
Kenya Results: Of the pupils seen, 61% were still in pre- or lower primary school. Majority were aged 13 and 14
years. Of the 261 ear swab samples processed, 336 isolates – either in mixed or pure flora – were
identified, being almost exclusively aerobes. Proteus spp., Enterococcus, Staphylococcus aureus and
Pseudomonas spp. were isolated in 32.7%, 28.6%, 12.8% and 11.3% respectively. Proteus was susceptible to
majority of the antibiotics tested for, while Enterococcus was poorly susceptible.
Conclusions: Aerobic bacteria were most prevalent in this study. Several of the bacteria identified are
known to require iron for their growth. This may be important for CSOM treatment if biofilm formation is
involved in pathogenesis. Majority of the isolates were susceptible to basic antibiotics compared to
Enterococcus bacteria. This portends an important consideration for clinical management and
therapeutic decision-making. Additionally, given the prevalence of Enterococcus bacteria, which is an
indicator of faecal contamination of the environment, there is need to consider relevant public health
components in managing childhood CSOM besides the clinical ones alone.
ß 2013 Elsevier Ireland Ltd. All rights reserved.

1. Introduction disease associated with irreversible pathology of the middle ear

Chronic suppurative otitis media (CSOM) is a persistent,
insidious ear condition characterised by discharge into the
external ear canal continuing for over two weeks and associated
with perforation of the tympanic membrane. It is a multietiologic
* Corresponding author at: University of Nairobi, Department of Surgery, ENT/
Head & Neck Surgery, P.O. Box 6734, Kondele, Kisumu, Kenya.
Tel.: +254 722385291.
E-mail addresses: omondisda@yahoo.com, omondisda@gmail.com
(Dickens S.O. Aduda).
tissues [1]. The prevalence of CSOM and its complications are
poorly documented globally, but it is estimated that approximately
65–330 million individuals, especially children are affected [2]. Of
these, 60% have significant hearing loss, mainly as a result of long-
term suppuration, persisting perforation of the tympanic mem-
brane and disruption of the middle ear structures due to
complications. Fatalities attributable to CSOM are estimated at
28,000 per year [1]. Although poorly understood, risk factors
commonly attributed to CSOM include persistent local gram
positive and/or negative bacterial infection, recurrent acute otitis
media, recurrent upper respiratory infections, poor hygiene,
trauma to the middle ear and tympanostomy tube insertion

0165-5876/$ – see front matter ß 2013 Elsevier Ireland Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ijporl.2013.04.011

Please cite this article in press as: D.S.O. Aduda, et al., Bacteriology of chronic suppurative otitis media (CSOM) in children in Garissa
district, Kenya: A point prevalence study, Int. J. Pediatr. Otorhinolaryngol. (2013), http://dx.doi.org/10.1016/j.ijporl.2013.04.011
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[3,4]. Nutritional deficiencies may also be important [5,6]. The 2. Methods

current standard treatment regime for CSOM [7] is significantly
effective in enhancing resolution in ear discharge as well as better 2.1. Study design
hearing. However, in 41% of the children, ear discharge persists [7].
The present study sought to identify by type the bacteria found in We performed a school-based screening exercise over a period
school-going children with chronic ear discharge, and their of eight weeks in early 2010 to identify the proportion of pupils
antibiotic sensitivity patterns. who had chronic ear discharge, lasting 14 days or longer, among a
Presence of bacterial infection in the middle ear considerably cohort of primary school-going children in Garissa district. We
prolongs or may complicate the healing process, but their specific then took aural swabs from the eligible ears of consenting pupils
role in the pathogenesis of CSOM is hitherto poorly understood. for microbiology. The main outcome measures were types of
Some studies indicate that the occurrence of clinical and bacteria isolated and their susceptibility to antibiotics. The study
pathological complications of CSOM is related to the bacteriologic was part of a randomised clinical trial designed to determine the
types present [8,9]. Proliferation of these pathogens in the middle role of zinc in the treatment of CSOM among school-going children
ear may be perpetuated by chronic inflammatory processes or high in Garissa district, Kenya.
humidity [1]. It is postulated that the mode of the middle ear
infection is by translocation of bacteria from the external ear, since 2.2. Setting
the bacteria isolated from middle ear exudates have been observed
to be similar to those from the external auditory canal regardless of The study was conducted among primary school-going pupils
the sampling techniques used [10]. The most commonly encoun- attending public and private primary schools as well as Islamic
tered bacteria patterns in CSOM include: Pseudomonas aeroginosa, religious schools (Madrasas and Duksis) who had been screened for
Streptococcus pyogenes, Staphylococcus aureus, Klebsiella species, CSOM within Garissa district. This is an arid rural district in the
Proteus species (aerobes) and Bacteriodes, Peptostreptococcus and north eastern part of Kenya (Fig. 1).
Proprionibacterium (anaerobes) while those often observed in Informed consent for school participation was obtained from
acute suppurative otitis media (ASOM) are Streptococcus pneumo- school staff and representatives of parent–teacher associations,
neae, Haemophilus influenza, S. aureus and Micrococcus catarrhalis while each child assented to assessments after their legal
[10–14]. guardian(s) were taken through and signed a witnessed written
The relative importance of the bacterial isolates can be informed consent.
determined by considering both the level of bacterial counts The ear swab specimens were collected at the induction stage
and the pathological importance of the strains obtained. Poly- when eligible pupils were being enrolled into the clinical trial for
bacterial recoveries involving both aerobes and anaerobes are zinc supplementation in the treatment of chronic suppurative
commonly reported in samples obtained from ears with CSOM otitis media. The zinc supplementation trial was conducted
although prevalence relative to pure cultures widely varies. S. between January and July 2010 (during the first and second
aureus is the commonest pathogen in pure samples. Anaerobes school terms).
rarely occur singly in pure cultures signifying a potentially
symbiotic, or synergistic suppurative process [8]. Reported
occurrence of anaerobic bacteria is variable, probably due to
differences in bacteriological techniques used, as well as variable
study aims and epidemiological methods [8–10,13]. Whereas the
prevalence of anaerobic bacteria isolates was previously reported
as low [8], more recent observations report a wide range from 8% to
74% [9–12,14]. The anaerobic isolates commonly observed in ear
swabs are similar to those predominant in the oral flora as well as
those found in chronic sinusitis and head/neck abscesses [11].
However more scrupulous procedural standards are required for
collecting, transporting and processing the specimen to ensure the
validity of results reported [15].
Bacteriological studies of CSOM are important for determin-
ing effective antibiotic choices and surveillance of bacterial
patterns and their relative sensitivities. This is essential for risk
analysis and planning mitigation and logistics strategies.
Antibiotic treatments when given are directed at eradication
of pathogens from the middle ear cleft. Failure of treatment may
be associated with emergence of resistance, or proliferation of
new bacteria in the middle ear [11]. Resistance may occur due to
increased use of, or inappropriate exposure, to antibiotics.
Presence of b-lactamase enzyme activity has been reported to
be responsible for bacterial resistance to penicillin and
cephalosporin antimicrobials in more than half of the middle
ear aspirates [11].
The aim of the present study was to determine the point
prevalence of bacteria associated with chronic suppurative otitis
media in school-going Kenyan children. Specific objectives were to
identify bacteria isolates from eligible ears of children with chronic
suppurative otitis media and to study the antibiotic susceptibility
pattern of a sample of bacterial isolates to the commonly used Fig. 1. Map of the greater Garissa district.
antimicrobial agents. Source: http://www.kenyampya.com/index.php?county=Garissa.

Please cite this article in press as: D.S.O. Aduda, et al., Bacteriology of chronic suppurative otitis media (CSOM) in children in Garissa
district, Kenya: A point prevalence study, Int. J. Pediatr. Otorhinolaryngol. (2013), http://dx.doi.org/10.1016/j.ijporl.2013.04.011
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2.3. Inclusion and exclusion criteria
Only school-going pupils aged between 5 and 18 years with
perforated ear drums and visible suppuration in the external ear
canal for the past two weeks or more present at study induction
time and were eligible. Presence of cholesteatoma, mastoid abscess
or other conditions that required urgent surgery or other medical
attention was causes for exclusion. Pupils who had received or
were receiving any medication prior to enrolment were also
excluded. Ear swabs were collected if both the parent(s) and the
child had consented.
and Technology and other collaborating institutions as required.
The study was part of the chronic otitis media study in Kenya
(Clinical Trial number_ISRCTN86106121; more details about this
trial online: http://www.controlled-trials.com/ISRCTN86106121).
2.6. Statistical analysis
Descriptive methods were used and frequency tables and charts
plotted on Microsoft excel.
3. Results

2.4. Sampling and bacteriological techniques 3.1. Socio-demographic characteristics of the participants: study
population
After obtaining consent/assent from identified pupils pure tone
audiometry was carried out by the project nurse to establish hearing More than half (61.5%) of all the pupils assessed for bacterial
thresholds before treatment commenced. After audiometric tests, the ear infection were still in lower primary and the nursery school:
ENT Clinical Officer performed bilateral otoscopy and collected a in nursery section (28%) and lower primary 1–3 (33.5%).
single specimen from the eligible ear(s) with commercially prepared Majority of them were between age 13 and 14 years with
sterile fine cotton swabs from the eligible ear(s) under aseptic slightly more of males. The age and sex distribution of patients
conditions. Screw-tightened collection bottles containing Robertson are presented in Fig. 2.
Cooked Meat (RCM) medium were doubly used as transport medium Of the 9100 pupils screened, 300 had suppurative middle ear
and to facilitate multiplication of the organisms present. The screw discharge, representing a CSOM prevalence of about 3.3% in this
capped bottles were further sealed with ‘parafilm’ to ensure they population. A total of 261 samples were successfully cultured out
were airtight. At the end of each field visit – on average 6 h post of which 84 sensitivities were completed (being a sample from the
collection – we transported the specimen in cooler boxes, without total isolates considered for bacterial susceptibility tests due to
icepacks, to the nearby provincial hospital laboratory, located within lack of sensitivity discs. The samples were selected sequentially
the main town centre. The cooler boxes were used to protect the from each batch that had pure and mixed cultures, taking from the
specimen from ultraviolet rays due to direct exposure to sunlight in first available one in each case). No growth was obtained from 12
the prevailing hot environment. The microbiologist at the provincial (4.6%) of the cultures. There were 336 isolates identified, all of
hospital laboratory incubated all received specimen for 48 h before them aerobes with no anaerobes obtained, except for one case
shipping them to the University of Nairobi Laboratory for culture and
sensitivity analysis.
Processing of the specimen for culture was done for both
aerobic and anaerobic bacteria, according to the standard
operating protocols for the University of Nairobi/Kenyatta Hospital
Laboratory. Specimens were inoculated onto two blood agar plates
as follows: (i) 1 blood agar plus MacConkey agar for aerobic
incubation and (ii) 1 blood agar plate containing a Metronidazole
disc for anaerobic incubation. The plates were incubated at 37 8C.
Anaerobic incubation was done using the GasPak jar methods and
was read after 48–72 h, while aerobic cultures were read within
18–24 h. Any growths obtained from the anaerobic cultures were
further sub-cultured onto fresh blood agar and MacConkey agar
and incubated aerobically to rule out presence of facultative
aerobes. All clinically and epidemiologically important bacteria
were identified from positive cultures by their colonial morpholo-
gy on the respective media and Gram-staining reaction and further
Fig. 2. Age–sex distribution of pupils with CSOM from whom ear swabs were taken
confirmed by the pattern of reaction using standard biochemical for culture and sensitivity (N = 261). Error bars with standard error.
test methods using [15]. Negative cultures were also reported.
Sensitivity tests based on the disc diffusion methods [16] were Table 1
conducted using commercially available kits. The following Types of pathogens isolated and prevalence in the isolates.
antibiotics were tested using standard laboratory procedures:
Pathogen N = 348 Total (%)
sulphamethoxazole, gentamicin, chloramphenical, ciprofloxacin,
ceftazidime, amikacin, augmentin, doxycycline, ampicilin, linco- (%) – in single (%) – in mixed
isolates isolates
mycin, polymixin B, cephalothin, suprapen and framicetin. These
drugs are widely used in both the out-patient and in-patient units 1. Proteus 67 19.25% 43 12.4% 31.7
2. Enterococcus spp. 40 11.49% 56 16.1% 27.6
in Kenya. Inhibition zones in each case were compared against that
3. S. aureus 27 7.8% 16 4.6% 12.4
of the control organisms. The results were reported on the 4. Pseudomonas spp. 20 5.7% 18 5.2% 10.9
laboratory request forms for each respective organism as either 5. E. coli 10 2.9% 15 4.3% 7.2
‘sensitive’ or resistant. 6. Klebsiella spp. 2 0.6% 10 2.9% 3.5
7. Anthracoides 1 0.3% 9 2.6% 2.9
8. Diptheroides 1 0.3% 1 0.3% 0.6
2.5. Regulatory approval 9. Clostridium tetani 1 1 0.3 0.3

Total 168 48.3% 168 48.3% 96.6

All regulatory approvals for the study were granted by Kenyatta
No growth was obtained in 12 (3.4%) cultures 100%
National Ethics Committee and Kenya National Council of Science

Please cite this article in press as: D.S.O. Aduda, et al., Bacteriology of chronic suppurative otitis media (CSOM) in children in Garissa
district, Kenya: A point prevalence study, Int. J. Pediatr. Otorhinolaryngol. (2013), http://dx.doi.org/10.1016/j.ijporl.2013.04.011
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Table 2
Distribution analysis of bacterial susceptibility to selected antibiotics.

Antibiotic Sensitivity Proteus spp. Enterococcus S. aureus Pseudomonas spp. E. coli Klebsiella spp.
N (%) N (%) N (%) N (%) N (%) N (%)

Sulphamethoxazole Sensitive 20 (71) 0 4 (100) 1 6 (85.7) 5 (100)

Resistance 8 (29) 3 (100) 0 0 1 (14.3) 0

Gentamicin Sensitive 24 (85.7) 1 3 (60) 1 6 (85.7) 5 (100)

Resistance 4 (14.3) 0 2 (40) 0 1 (14.3) 0

Chloramphenical Sensitive 23 (79.3) 17 (73.9) 5 (83.3) 8 (80) 7 (100) 5 (100)

Resistance 6 (20.7) 6 (26.1) 1 (16.7) 2 (20) 0 0

Ciprofloxacin Sensitive 24 (92.3) 15 (65.2) 3 (100) 7 (70) 6 (85.7) 4 (80)

Resistance 2 (7.7) 8 (34.8)) 0 3 (30) 1 (14.3) 1 (20)

Ceftazidime Sensitive 15 (93.8) 0 3 (100) 0 5 (83.3) 5 (100)

Resistance 1 (6.2) 0 0 0 1 (16.7) 0

Amikacin Sensitive 21 (87.5) 1 2 (100) 1 3 (100) 3 (100)

Resistance 3 (12.5) 0 0 1 0 0

Augmentin Sensitive 0 11 (52.4) 1 7 (88) 0 0

Resistance 0 10 (47.6) 0 112) 0 0

Doxycycline Sensitive 0 6 (37.5) 0 5 (63) 0 0

Resistance 0 10 (62.5) 1 3 (37) 0 0

Ampicilin Sensitive 0 2 0 2 (50) 0 0

Resistance 0 1 0 2 (50) 0 0

Lincomycin Sensitive 0 4 (25) 1 (33.3) 6 (75) 0 0

Resistance 0 12 (75) 2 (66.7) 2 (25) 0 0

Polymixin B Sensitive 0 0 0 0 0 0
Resistance 4 (100) 0 1 0 2 (100) 0

Cephalothin Sensitive 0 1 0 0 0 0
Resistance 0 0 0 0 0 0

of Clostridium tetani. Table 1 shows the frequency distribution of
the isolates. The commonest bacteria found were Proteus spp.
(31.7%), Enterococcus (27.6%), S. aureus (12.4%) and Pseudomonas
spp. (10.9%). Of the isolates recovered, only 84 (half of each from
pure and mixed bacterial isolations) were sampled for sensitivity
analyses. The drugs tested were: sulphamethoxazole, gentamicin,
chloramphenical, ciprofloxacin, ceftazidime, amikacin, augmentin
(amoxiclav), doxycycline, ampicilin, lincomycin, polymixin B and
cephalothin. On average, Proteus showed susceptibility to anti-
biotics tested for in 81.9% of the cases, while Enterococcus was
susceptible in 53.7% of the tests, which was the lowest across the
sensitivity tests (Table 2). Specifically, Enterococcus was only
moderately susceptible to ciprofloxacin and augmentin (amox-
iclav) – the drugs of choice in this context, but largely resistant to
lincomycin, doxicycline and sulphamethoxazole. Klebsiella, Escher-
ichia coli and Proteus were highly sensitive to all the drugs tested
for.
4. Discussion
Understanding the bacterial patterns prevalent in the commu-
nity is critical for effective planning of treatment interventions and
supplies. In routine ear care, pus swabs are not customarily
obtained from patients suffering from chronic suppurative otitis
media (CSOM) in our context, unless in protracted or recurrent
cases as well as when clinical exacerbations of CSOM or its
complications occur. These events are more likely to occur from
bacterial infection, although the role of biofilms has also been
adduced [17]. For example, S. aureus has been frequently observed
in cholesteatomas, while Proteus has been implicated in extra-
cranial and intra-cranial complications of chronic suppurative
otitis media [18]. An isolate of C. tetani was obtained from culture
and sensitivity. The occurrence of otogenic tetani is rarely reported
in literature [19]; however it is necessary for practitioners to be on
the lookout for symptoms as persistent otorrhoea is a high risk
factor for occurrence of otogenic tetani [19,20]. Children from low
socio-economic regions may be more susceptible [19,20].
In this study cohort no related complications of CSOM were
observed, although in majority of the cases, presence of bacteria
was demonstrated. This is similar to other studies [8] and which
indicates the overwhelming importance of bacterial activity in
CSOM. The higher prevalence of bacterial infection among children
aged 13–14 years (with similar male to female ratio) in these
children was unexplained. The commonest bacteria identified
were Proteus spp. and Enterococcus. This is similar to a study in
Malawi which also reported increased prevalence of Proteus and
Enterococci [21]. However, in a study reported by Moshi et al. [22],
and conducted among primary school going children in Tanzania,
similar bacterial strains including Pseudomonas aeruginosa (51.7%),
S. aureus (17.2%), Proteus mirabilis (13.2%), Klebsiella spp. (8.0%) and
E. coli (5.8%) were isolated, but with varying prevalence from the
present study. Enterococci were also not reported in this series. In a
retrospective review of 375 ear swab specimen from clients
attending ENT clinic in Ilorin Nigeria, with a participant age range
of 8 months–70 years, predominant prevalence of P. aeruginosa,
Proteus spp. and S. aureus was reported [23]. This indicates existing
variations in microbial prevalence within given regions which may
be due to unique epidemiological or methodological differences.
However, it is not clear whether period difference or seasonal
variations contribute to the prevailing bacterial patterns. Never-
theless, some studies have indicated that increasing colonization
by enteric bacteria is more likely with warmer temperatures [24].
Another factor which should be considered in relation to
bacterial prevalence estimates is the subjects iron status. This is
because several of the bacteria identified are known to require iron
for their growth. This may also relate to biofilm production which
can influence bacterial growth [25]. Bacterial biofilms have been
described as a growth mode specialised for long term colonization

Please cite this article in press as: D.S.O. Aduda, et al., Bacteriology of chronic suppurative otitis media (CSOM) in children in Garissa
district, Kenya: A point prevalence study, Int. J. Pediatr. Otorhinolaryngol. (2013), http://dx.doi.org/10.1016/j.ijporl.2013.04.011
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of mucosal surfaces, and they predispose to recurrent and
treatment-resistant infections. Biofilm formation seems to require
a higher level of iron than is needed for growth [26]. This may be
important for CSOM if biofilm formation is involved in pathogen-
esis. In addition, aerobic, or facultative pathogens, often secrete
iron chelators, which scavenge host iron from iron-binding and
heme-containing proteins. For these reasons iron availability to
bacteria in the middle ear cavity, through secretions and exudates,
may influence pathogenesis, and bacterial virulence.
Failure to demonstrate presence of anaerobic bacteria in this
cohort was not explained. But using swabs might have been a
limiting sampling technique in children with narrower external ear
canals. Studies specifically conducted to detect the occurrence of
anaerobes in CSOM have established they play a role in the aetiology
and prognosis of CSOM [12]. The relative high prevalence of 39.6% of
enteric bacteria, such as Enterococcus, E. coli, and Klebsiella indicates
poor environmental hygiene and sanitation patterns in this
community, which increases chances of human contact with faecal
matter from animals and man. It is not known if these observations
have any bearing on the prevalence of CSOM in this region. However,
we suggest that instituting appropriate public health interventions
alongside clinical management may be critical in combating both
bacterial resistance and CSOM recurrence [21,27].
The overall sensitivity of Enterococcus to ciprofloxacin was 65%
and 52% for augmentin, but generally resistant to lincomycin and
doxicycline. This may signify inappropriate exposure to, or
increased use of these antibiotics in the general population.
However, resistance could be due to innate bacterial character-
istics and emerging tendency to form bacterial biofilms [28]. This
phenomenon may pose difficulties in treatment of cases with
mixed infections involving Enterococcus bacteria. Environmental
contamination with drug-resistant bacteria is more likely to
significantly contribute to children’s carriage of antibiotic-resis-
tant bacterial strains [29]. Also, relative increased exposure to
antibiotics, use of low quality drugs, indiscriminate or in
appropriate use of antibiotic may increase the likelihood of
colonization with resistant bacterial strains and subsequent
horizontal spread in the community, especially in settings with
high crowding index. Pluralistic drug use involving known and
herbal formulations to treat minor ailments among children in
Kenya has been observed previously [27,30]. Hence, periodic
surveillance of the prevalence of the main bacterial infectious
agents and their antimicrobial susceptibility as well as instituting
appropriate public health promotion activities at community level
is desirable. Also, since childhood CSOM is a common condition
leading to poor education, it is important for it to be treated with
cost effective antibiotics so that finite resources are not wasted.
Authors’ contributions
D.S.O. Aduda, I.M. Macharia, P. Mugwe, H. Oburra, B. Farragher,
I. Mackenzie provided study concept and design.
D.S.O. Aduda, I.M. Macharia, B. Farragher, I. Mackenzie, Bernard
Brabin contributed to the analysis and interpretation and drafting
the manuscript.
Conflict of interest statement
Authors declare there is no conflict of interest.
Acknowledgements
The authors acknowledge UoN Microbiology Laboratory Staff,
Clinical and Nursing plus all support staff on COMIKS project 2010/
2011.
Please cite this article in press as: D.S.O. Aduda, et al., Bacteriology of chronic suppurative otitis media (CSOM) in children in Garissa
district, Kenya: A point prevalence study, Int. J. Pediatr. Otorhinolaryngol. (2013), http://dx.doi.org/10.1016/j.ijporl.2013.04.011
5
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