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Romanian Biotechnological Letters
Copyright © 2016 University of Bucharest
Vol. 22, No. 1, 2017
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ORIGINAL PAPER
Microbial etiology of acute otitis externa - a one year study
Received for publication, August 10, 2015
Accepted, December 9, 2015
DANIELA CIRPACIU 1, 3, CRISTINA MARIA GOANŢĂ1,3*, M. TUSALIU1,2,
C. CURUTIU4, V.A. BUDU1
1University of Medicine and Pharmacy “Carol Davila”, Bucharest, Romania
2Institute of Phonoaudiology and Functional ENT Surgery “Prof. Dr. D. Hociotă”,
Bucharest, Romania
3Clinical Emergency Hospital “Sf. Pantelimon”, Bucharest, Romania
Research Institute of the University of Bucharest, ICUB and Faculty of Biology,
University of Bucharest, Romania
*Address correspondence to: Cristina Maria Goanţă, e-mail: [email protected]
Abstract
Acute otitis externa is a diffuse inflammation of the external ear canal, caused by bacterial
and/or fungal infections that may cause persistent, severe pain, swelling of the skin and detritus
accumulation in the auditory canal accompanied by mild hearing loss. Microbiological samples were
collected from the external ear canal of 59 outpatients and analyzed for the presence of aerobic
pathogens responsible for otitis externa and the isolated strains sensitivity to currently tested
antibiotics. Staphylococcus aureus was the most common microorganism encountered in the external
ear canal (31 of 59 cases), followed by Pseudomonas aeruginosa (12 of 59 cases), Escherichia coli (4 cases)
and Proteus vulgaris (3 cases). The unexpected high incidence of Staphylococcus aureus (58% of all
cases), compared to data found in the literature that report a much smaller percent, was accompanied
by a high level of resistance of the isolated Staphylococcus aureus strains to usual antibiotics such as
ciprofloxacin (32%), cefuroxim (36%), azithromycin (40%), gentamicin (26%) and chloramphenicol
(27%). Although otitis externa is considered a trivial pathology and many times receives empiric
treatment, the results of our survey highlight the need for determination of the specific microbial
etiology and of antibiotic susceptibility spectrum to enable a targeted treatment.
Keywords: acute otitis externa, Staphylococcus aureus, antibiotic resistance
1. Introduction
Acute otitis externa (AOE) is a diffuse inflammation of the external ear canal, caused
by a bacterial and/or fungal infection, generally without involvement of the tympanic membrane.
It may cause persistent, severe pain, swelling of the skin and detritus accumulation in the auditory
canal, mild hearing loss. The disease usually results from high humidity, warm swimming
pools, local trauma, and the use of hearing aids (BEERS [1], OSGUTHORPE & NIELSEN [2],
MOSGES & al. [3]). The most important environmental factor is excessive moisture, which
increases the pH and decreases cerumen (SANDER [4], MITTAL & KUMAR [5]).
The most common agents responsible for acute diffuse external otitis are Pseudomonas
(P.) aeruginosa followed by Staphylococcus (S.) aureus, Proteus vulgaris, Streptococcus
species, Candida albicans, Aspergillus niger and in some cases even mixed infections were
found (ANNIKO & al. [6]). The aim of this study was to identify the microorganisms responsible
for the cases of otitis externa presenting to ENT Department within Alexandria County Emergency
Hospital, Romania, over twelve months period, between August 2014 and July 2015. The
authors also investigated the susceptibility of the pathogenic bacteria isolated to selected
antibiotics. These findings were compared with previously published studies in order to evaluate
whether treatment recommendations currently proposed by the international literature apply to
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Microbial etiology of acute otitis externa - a one year study
this region of Romania and to draw attention to the need of inland data for guiding future empiric
treatment. Inland data are needed because the bacterial colonization of a normal ear canal and
the microbiology of external otitis may differ due to climate, health seeking behaviors, topical
or systemic available treatment, socio-economic level that influences local hygiene or other
habits. It is generally accepted for treatment the use of topical antibiotics with or without steroids,
antiseptic and anti-inflammatory agents, after a thorough cleaning of the ear canal. Topical
drying agents such as Castellani solution, gentian violet or iodopovidone are also recommended
(ANNIKO & al. [6]). Clinicians should prescribe non-ototoxic antibiotic (ear drops) when the
patient has a known or suspected perforation of the tympanic membrane, including a tympanostomy
tube (ROSENFELD & al. [7]). If the ear canal is occluded, topical solutions should be applied
on a sterile ear wick. Oral antibiotics are indicated in cases of severe external otitis with
cellulitis or lymphadenitis, and always in diabetic patients (ANNIKO & al. [6]). Patients not
responding to this therapy or presenting complications should be hospitalized.
2. Materials and Methods
The authors present the results of a retrospective study carried out on a 12 months
period between august 2014 and July 2015, on outpatients who addressed the ENT
department of Alexandria County Emergency Hospital, Romania, developing signs of acute
external otitis (pain, swelling of the auditory canal, discharge, hearing loss etc.). The study
included outpatients between 10 and 84 years old, with acute unilateral or bilateral external
otitis, disregarding associated mild to moderate general pathology. Patients with chronic
external otitis, otitis media or mastoid involvement, recently hospitalized, and recently treated
with ear drops containing antibiotics or systemic antibiotics, general diseases associated with
severe immunosuppression were excluded. Microbiologic samples from external ear canal
were collected by the same otologist on the first contact with the patient before any topical or
systemic antibiotic and anti-fungal medication started, using sterile swabs. The specimens
collected were immediately transported to the hospital microbiology laboratory for routine
aerobic culture and identification. The strains identification was realized using biochemical
conventional tests and the antibiotic susceptibility testing was performed by Kirby-Bauer
standard disk diffusion method (CLSI, 2014, 2115 editions).
3. Results
A number of 59 patients (35 men and 24 women) aged between 10 and 84 years old,
from which ¼ were children (14 of these 59 patients were between 10 and 19 years old)
were analyzed. From all the samples were isolated 34 Gram positive bacteria (31 S. aureus,
2 Streptococcus sp. and 1 Enterococcus sp.) and 20 Gram negative bacteria (12
P. aeruginosa, 4 Escherichia (E.) coli, 3 Proteus vulgaris and 1 Klebsiella sp. strains). In five
cases, the cultures were negative (figure 1). An unexpected finding was a significantly high
incidence of S. aureus (57% of all cases), compared to data found in the literature that
report a much smaller percent, varying by different authors approximately between 7 and
20 percent (PRASANNA & al. [8], DIBB [9]). Most cases were recorded during the warm
season, from June to September. In all cases a single species was isolated. In order to orient
future empiric treatment, the sensitivity of these strains to usually administrated antibiotics
was tested. We mention that all patients included in this study received empiric treatment
before finding out the results of bacteriology, topic or systemic antibiotics, based on the
clinical severity of symptoms and co-morbidities. An unexpected finding was the high level
of resistance to usual antibiotics of some S. aureus strains, as showed in figure 2.
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DANIELA CIRPACIU, CRISTINA MARIA GOANŢĂ, M. TUSALIU, C. CURUTIU, V.A. BUDU
Figure 1. Bacterial strains isolated from patients with AOE
32% of tested staphylococci were resistant to ciprofloxacin that is currently prescribed
for external otitis in Romania. Also, 26% were resistant to gentamicin and 27% to
chloramphenicol (used in ear drops). We found a 40 % resistance to azithromycin and 50%
resistance to clarithromycin in the tested S. aureus strains. For cefuroxime, the tests
performed by the hospital laboratory, showed 36 percent resistance rate. Only one MRSA in
the swabs taken from the ear of a 11 years boy who had no significant history, no previous
hospitalization, no previous antibiotic treatment for his external otitis or any known cause of
immunosuppression. This boy was referred to a laboratory specialized in infectious diseases
in order to benefit of an appropriate antibiotic therapy.
Figure 2. S. aureus sensitivity and resistance rates to tested antibiotics
P. aeruginosa had a higher sensitivity to the tested antibiotics tested compared to
S. aureus. All twelve Pseudomonas strains proved to be sensitive to ciprofloxacin.
A significant degree of resistance was registered to cefuroxime, chloramphenicol, colistin and
augmentin, as showed in figure 3.
4. Discussions
Excessive cleaning of the ear canal wax and local trauma are known to decrease local
protection and to favor external otitis. The results of this study showed an unexpected high
incidence of S.aureus isolated from ear patients suffering from external otitis, the most common
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Microbial etiology of acute otitis externa - a one year study
Figure 3. P. aeruginosa sensitivity and resistance rates to the tested antibiotics
organism encountered (31 of 59 cases), followed by P. aeruginosa (12 of 59 cases), E. coli
(4 cases) and Proteus sp. (3 cases). Since for this study were chosen only outpatients
diagnosed with external otitis by the ENT doctor, who had not recent hospitalization or had
been recently treated with antibiotics as ear drops or systemic therapy, the question about the
source of contamination is legitime. Staphylococci are the most abundant skin-colonizing bacteria
and one of the most important causes of nosocomial infections and community-associated
skin infections (MICHAEL [10]). The nose is the principal site of S. aureus colonization
(KLUYTMANS & WERTHEIM [11]), but is also found in the pharynx, perineum, axillae and
the skin (WERTHEIM & al. [12]). Approximately 50% of the population is non-carriers, 30%
carry S. aureustransiently while 20% of the population is persistent colonized with S. aureus
(KLUYTMANS & WERTHEIM [11]). P. aeruginosa is a Gram-negative species commonly
found in soil and water but also an opportunistic humanpathogen, which could colonize immunocompromised patients, like those with cystic fibrosis, cancer, or AIDS (BOTZENHARDT &
DORING [13]). P. aeruginosa has a great capacity to form biofilms, which are complex
bacterial communities very hard to destroy that adhere to a variety of surfaces, including
metals, plastics, medical implant materials and tissue (BROWN & SMITH [14]). In a study
performed on 100 healthy individuals, with normal ear canal, published in 2015, the authors
reported S. aureus in 24.7% of healthy subjects, Diphteroids in 7.5%, E. coli in 5.4% and
Pseudomonas in 3.2% of cases and concluded that some pathogenic bacteria which can cause
otitis externa are present as normal commensals in the external ear canal (PRASANNA & al.
[8]). Another Norwegian study reported Staphylococcus aureus in 7% of cases (DIBB [9]).
These data are sustained by the results of this study that proved that in the most of the cases
infection is produced by commensal species, normally found in ear canal.
On the other hand, these results are quite different by those found in the literature
regarding bacteriological profiles found in external otitis by researchers from other countries.
A study of acute otitis externa at Wellington Hospital, 2007–2011, reported that P. aeruginosa
was the most common organism (46.5%), while S. aureus was the second most common (31.9%)
(JAYAKAR & al. [15]). Roland et al. studied 2039 subjects with acute otitis externa and
reported that the largest percentages of recovered organisms were Gram negative (53%) and
45.3% of all recovered organisms were Gram positive. The most commonly bacterial strains
isolated from ear specimens of otitis externa were P. aeruginosa (37.7%), S. epidermidis (9%)
and S. aureus (7%) (ROLAND & STROMAN [16]). In 2010 a prospective British study identified
P. aeruginosa in 45.1% of cases and S. aureusin 9% of patients with acute otitis externa referred
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DANIELA CIRPACIU, CRISTINA MARIA GOANŢĂ, M. TUSALIU, C. CURUTIU, V.A. BUDU
to a large teaching hospital over a six-month period (NINKOVIC[17]). A microbiological study
of external otitis in Rosario City, Argentina found P. aeruginosa in 18.6% of cases, Proteus
mirabilis in 10.9% of cases, and S. aureus in 10.9% and also three associations of P. aeruginosa
and Proteus mirabilis (1.4%) (AMIGOT & al. [18]). Another observation resulting from this
study was the alarming rate of S. aureus resistance to usual antibiotics such as ciprofloxacin,
cefuroxime, azithromycin, gentamicin or chloramphenicol. This should be an alarm sign that
bacteriological profile in external otitis changed and the indiscriminate use of antibiotics by
primary care physicians or specialists may generate multiple drug resistance in common pathogens.
5. Conclusions
Otitis externa is considered a trivial pathology and many times receives empiric treatment.
The high incidence of Staphylococcus and the high rate resistance to antibiotics should be an
alarm sign for clinicians and impose routine microbiological sampling and discriminate what
antibacterial agents will be used based on antibiotic susceptibility test. Inland data regarding
the most common pathogens responsible for external otitis are important in selecting the most
appropriate treatment. Thus further studies are necessary to draw conclusions reliable enough
to generate recommendations applicable as treatment protocols in otitis externa in Romania.
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