AM ER IC AN JOURNAL OF OT OLARYNGOLOGYH E A D A N D NE CK M E D IC IN E A ND S U RGE RY 3 7 (2 0 1 6) 4 254 3 0

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Malignant external otitis: Factors predicting patient

outcomes,,

Sagit Stern Shavit, MD a, b,, Ethan Soudry, MD a, b ,

Yaniv Hamzany, MD a, b , Ben Nageris, MD b, c,
a
Department of Otolaryngology-Head and Neck Surgery, Rabin Medical Center, Petach Tikva, Israel
b
Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
c
Department of Otolaryngology-Head and Neck Surgery, Meir Medical Center, Kfar Saba, Israel

ARTI CLE I NFO A BS TRACT

Article history: Objective: Malignant external otitis (MEO) is an aggressive infection, primarily affecting
Received 23 February 2016 elderly diabetic patients. It begins in the external ear canal and spreads to adjacent
structures. This study investigated the clinical characteristics of patients diagnosed and
treated for MEO and analyzed factors affecting patient outcomes.
Study design: Historical cohort.
Setting: Tertiary medical center.
Methods: Medical records of all patients diagnosed and treated for MEO from 1990 to 2013, were
retrospectively reviewed. Clinical features, laboratory, imaging and outcomes were analyzed.
Results: 88 patients were included, mean age was 73 11.5 years, 61 (69%) were male. Of these, 75%
had diabetes. Mean follow-up was 60 months. The most common presenting symptoms were otalgia
(89%), external ear canal edema (86%) and otorrhea (84%). Pseudomonas aeruginosa was isolated in 61% of
ear cultures. All patients were treated with antibiotics, 22% had surgery and 8% hyperbaric oxygen.
Overall survival rate was 38% in 5 years, with disease specific mortality 14%. DM, facial nerve palsy,
positive CT scan and age above 70 were found to correlate and predict disease-specific mortality.
Conclusions: MEO carries a grave prognosis. The presence of two or more of the following
features, DM, facial nerve palsy, positive CT scan and age above 70, predicts poor outcome,
and highlights the need for prolonged, vigorous treatment.
2016 Elsevier Inc. All rights reserved.

1. Introduction 1968 due to the high, disease-specific mortality rate of over

50% prior to the introduction of appropriate antibiotic
Malignant (necrotizing) external otitis (MEO) is an aggressive treatment [1]. MEO predominantly affects elderly patients
infection. It begins in the external ear canal and spreads to and those with diabetes, although it has been described
adjacent structures. It was termed malignant by Chandler in among non-diabetics as well [2]. Pseudomonas aeruginosa, the

Author Disclosures.

Sponsorship: None.

Funding source: None.
Correspondence to: S.S. Shavit, Rabin Medical Center, 39 Jabotinsky St., Petach Tikva, Israel 49100. Tel.: +972 3 9376458; fax: +972 3 9376467.
Correspondence to: B. Nageris, Dept. of Otolaryngology-Head and Neck Surgery, Meir Medical Center, 89 Tshernichovsky St., Kfar
Saba, Israel 4428164. Tel.: +972 9 7472553; fax: +972 9 7471291.
E-mail addresses: sagitst@clalit.org.il (S.S. Shavit), bennyn@clalit.org.il (B. Nageris).

http://dx.doi.org/10.1016/j.amjoto.2016.04.005
0196-0709/ 2016 Elsevier Inc. All rights reserved.
426 AM ER IC AN JOURNAL OF OT OLA RYNGOLOGYH E A D A N D NE CK M E D ICI N E AN D S U RGE RY 3 7 (2 0 1 6) 4 25 4 3 0
most common pathogen known to cause MEO, is responsible
for over 90% of cases. Staphylococcus aureus, Proteus mirabilis
and fungi, mostly aspergillus and candida species have also
been described [35].
In 1987, Cohen and Friedman described diagnostic criteria
to stratify disease severity. Major criteria include otalgia,
otorrhea, edema, granulation tissue, positive 99mTc scan,
failure to response to treatment after more than a week and P.
aeruginosa isolation. Minor criteria are positive radiograph,
diabetes mellitus, old age and cranial nerve involvement [6].
MEO is diagnosed if all major criteria are present. If some are
absent, then a 13 week trial of intensive local and systemic
treatment is recommended; failure to respond clarifies the
diagnosis [7]. Treatment includes systemic anti-pseudomonas
antibiotics for at least 6 weeks and topical therapy. If insufficient
response, modalities such as surgery and hyperbaric oxygen
treatment are considered, as well as additional antibiotic or
antifungal treatment.
Due to the difficulty of diagnosis and its low incidence,
evidence-based knowledge is derived from small case series
or historical cohorts, several of which are based on our
institutional experience [2,4,79]. The goals of the current
study were to evaluate and identify characteristics and
factors predicting outcomes and to design a prognostic tool
to predict mortality.
2. Materials and methods
The computerized database of the Department of
Otolaryngology-Head and Neck Surgery of a university-
affiliated medical center was retrospectively reviewed for all
adult patients admitted for MEO between January 2009 and
December 2013. The medical center is a major referral site for
MEO. Patients were diagnosed with MEO if presenting with all
of the following criteria: (1) external otitis with compatible
physical examination severe otalgia, external ear canal
edema, exudate and granulations, (2) failure to respond to
antibiotic treatment for at least one week, (3) positive finding
on bone scan (technetium with or without gallium) or
evidence of bone destruction on CT scan, (4) histological
findings compatible with inflammation (patients with
diagnoses such as squamous cell carcinoma of the external
ear were excluded), and (5) microabscess in specimens
obtained at surgery, if performed. If one criterion was lacking
and disease failed to improve after 1 week of intravenous
antibiotics and aggressive local treatment, MEO was diagnosed,
as well.
According to departmental protocol, all patients undergo
technetium scan for diagnosis of MEO. Those with a positive
scan undergo gallium scan to strengthen the diagnosis. CT is
routinely performed to identify disease spread. All patients
undergo biopsy of the external ear canal for histological
confirmation of inflammation and to exclude squamous cell
carcinoma. Antibiotics are prescribed for at least 6 weeks.
Follow up examinations, CRP and ESR measurements, and
gallium scans are repeated as needed until disease resolution.
Cure from disease is defined as a complete resolution of
clinical symptoms, normal sedimentation rate and negative
gallium scan.
All patients who met the diagnostic criteria for MEO (n =
31) were added to the previous cohort of patients diagnosed
with MEO in our department from 1990 through 2008 (n = 57)
[9]. Diagnosis and treatment for all patients was according to
the departmental protocol, which was not altered from 1990
till 2013. The following information was collected from the
medical records: age, sex, comorbidities, physical examina-
tion features, treatment, biochemical results, culture and
biopsy results, imaging, follow-up data and prognosis for all
88 patients.
2.1. Statistical analysis
All statistical analyses were carried out using SAS 9.2
software. Continuous variables are presented as mean and
standard deviation. Normally distributed variables were
compared using t-test and categorical data were analyzed
using chi-square or Fisher exact test, as appropriate. Kaplan
Meier with log Rank test was performed for univariate
analysis. Multi-variable and hazard ratios were calculated
using Cox regression and the Fine and Gray model for
competing risks. Logistic regression was performed to design
a prognostic model. Statistical significance was inferred at
P < 0.05.
3. Results
3.1. Ethical considerations
The study protocol was approved by the local Institutional
Review Board. Informed consent was not required.
From 2009 through 2013, 31 patients were diagnosed with
MEO and added to the previous cohort of patients with MEO
diagnosed in our department from 1990 through 2008. Overall,
mean follow up was 60.6 54 (range 1268) months. The
mean age was 73 11.5 years and 61 (69%) were male. Most
patients (72%) had 2 or more comorbidities and 9 (10%) had
more than 4. The most common were diabetes mellitus (DM)
(66/88, 75%), hypertension (HTN) (64%) and ischemic heart
disease (IHD) (34%).
3.2. Physical examination and imaging
Among the 88 patients, all but 13 had unilateral MEO, only 3
presented with simultaneous bilateral ear disease. Mean
duration of otalgia prior to hospitalization was 41 38 days.
All patients failed to improve after at least one week of topical
and oral antibiotics prior to diagnosis. Physical examinations
signs at presentation included: otalgia in 79 patients (90%),
edema 76 (86%), otorrhea 74 (84%), granulations 66 (75%),
facial nerve palsy 15 (17%), bone erosions 4 (4.5%) and trismus
1 (1%).
Technetium scan was performed on 85/88 patients. Three
patients with aggressive disease died before having the scan;
all 3 had a positive CT scan. Almost all technetium scans
(95%) demonstrated positive findings in the petrous (32%),
mastoid (25%), other temporal bone location (28%) or multiple
locations. Fifty patients underwent gallium scan to strengthen
the diagnosis, of which 64% had positive gallium absorption.
 AM ER IC AN JOURNAL OF OT OLARYNGOLOGYH E A D A N D NE CK M E D IC IN E A ND S U RGE RY 3 7 (2 0 1 6) 4 254 3 0
Localization in the technetium and gallium scans agreed in all
but 2 patients. A total of 61 patients underwent CT scan as well,
with 75% demonstrating features compatible with external ear
infection and 84% indicating disease spread to adjacent structures:
temporomandibular joint (TMJ) (41%), infratemporal fossa (20%),
nasopharynx (13%) and skull base (11%).
Gallium scan was repeated during patient follow-up in
54%. The second scan was negative or demonstrated a significant
improvement in 59%.
3.3. Bacteriology and treatment
Bacterial cultures were taken from all admitted patients; 20/
88 cultures were negative. There were a total of 78 positive
bacterial or fungal isolates. Among these, 68 patients had a
single organism and 10 had 2 or more. Bacterial and fungal
species are elaborated in Table 1. Fungal infection was found
in 12, of which 7 also had bacterial infection and one had both
aspergillus and candida growth.
All patients received antibiotic treatment, 73% intrave-
nously, mostly with ceftazidime. High-dose oral quinolones
were given to 27%. Five patients with fungal isolates only in
repeat cultures received voriconazole in addition to antibiotic
therapy. Thirteen patients received 2 and 2 were treated by a
3-drug cocktail. Mean treatment duration was 47 27 days,
maximum 180 days.
Surgery was a second treatment modality for 20 (23%)
patients, of whom 12 had external canal debridement only.
Mastoidectomy was performed in 8 patients, of whom 4 had
canal wall-down procedure and 4 canal wall-up. Hyperbaric
oxygen was administered as an additional modality to 7 patients,
4 after surgery and 3 while receiving antibiotics.
3.4. Prognosis and risk factors
The survival rate after a mean follow-up of 61 months was
38%. There was 14% disease-specific mortality and 48%
mortality from other causes. Mean time-to-death from MEO
diagnosis was 9.5 13 months, while time to death from
other causes was 56.5 46 months (P = 0.001).
Disease persisted beyond the initial 6 week treatment
period in 24 patients (27%), who required additional antibiotic
treatment for an average of 63 80 days. A third of these were
treated with multiple modalities, including surgery (37.5%),
hyperbaric oxygen (25%) or both (37.5%).
Table 1 Bacterial and fungal species isolated from ear
cultures.
Bacteria/Fungus Positive cultures N (%)
Pseudomonas aeruginosa 39 (50)
Enterobacteriace 18 (23)
Candida 10 (13)
Staphylococcus aureus 7 (9)
Aspergillus 2 (3)
Streptococcus 1 (1.3)
Coagulase negative 1 (1.3)
Normal flora/Negative 20
Based on a total of 78 positive isolates among 88 patients.
427
Disease recurred in 12 patients (14%) after a mean of 7
3.5 months. These patients were treated with a second, 6-week
course of antibiotics, most with a combination of ceftazidime
and voriconazole. Additional treatment modalities were used
in 42%, including surgery (20%), hyperbaric oxygen (40%), or
both (40%).
Univariate analysis was performed to identify which
criteria affect overall patient mortality risk. Granulation during
physical examination (P = 0.023), positive CT scan (P = 0.0046),
facial nerve palsy (P = 0.024) and older age (P = 0.014) were
significant. (Fig. 1).
Other variables, including sex, other physical examination
findings, bacterial cultures, and positive technetium or
gallium scans were not found to affect the prognosis. No
significant relationship was found between persistent disease,
recurrence and treatment modalities and mortality. Compari-
son of prognoses between the populations followed from 2009
through 2013 and the previous cohort from 1990 through 2008
demonstrated no difference in disease specific mortality
between the two cohorts.
Diabetes was a risk factor for overall mortality. However, it
was an extremely strong risk factor for disease-specific
mortality (P < 0.0001). Disease distribution according to CT
scan (anterior invasion to TMJ, nasopharynx, infratemporal
fossa, posterior invasion to mastoid or invasion to skull base)
was not related to prognosis.
A multivariate analysis for disease-specific mortality
demonstrated that DM, positive CT scan, facial nerve palsy
and older age increased the hazard ratio (Table 2). A regression
model using these four variables was built to predict mortality
within a year of diagnosis in order to create a prognostic scale.
Each variable received one point. Three or more points predicted
an 8-fold increased risk of mortality (range 227) with 75%
sensitivity and 72% specificity.
4. Discussion
Malignant external otitis is a rare disease affecting elderly
diabetic patients and caries a poor prognosis. Since it was
described by Chandler in 1968, data regarding disease
prevalence, diagnosis and outcomes have been derived from
small case series and historical cohorts. Some of the largest
series were described among Israeli patients [2,610]. This
finding is attributed to the warm, humid climate.
Many studies include the definition and diagnosis of MEO,
as well as bacterial and imaging findings. Since the numbers
are small, only a few were able to identify factors affecting
patient outcomes. Stevens et al. published a protocol that
stratified MEO into severe and non-severe based on a
literature review. Severe MEO was defined by clinical features
such as seven nerve palsy, fungal culture, disease relapse and
requirement of surgerysurgical intervention, and imaging
features such as TMJ, ITF, Tegmen, NP and intracranial
involvement. In a series of 28 patients, those with two or
more positive criteria, had a worse prognosis [11].
The current study aimed to identify factors predicting patient
outcomes in the largest cohort in the literature and includes our
total institutional experience since 1990, describing 88 patients.
428 AM ER IC AN JOURNAL OF OT OLA RYNGOLOGYH E A D A N D NE CK M E D ICI N E AN D S U RGE RY 3 7 (2 0 1 6) 4 25 4 3 0

Fig. 1 KaplanMeier curves reporting follow up (FU) in days, from diagnosis, demonstrate increased mortality related to (A)
granulation tissue upon examination, (B) positive CT scan, (C) CN7 nerve palsy and (D) age above 70 at presentation.

They were diagnosed with Type 1 MEO according to Cohen and Multivariate analysis was conducted to identify which
Friedman criteria [6]. All patients were elderly, most with DM diagnostic criteria affect patient risk for disease-specific
(75%) and positive ear culture for P. aeruginosa (50%). These mortality. Age above 70 years, DM, facial nerve palsy and
findings are similar to reports from other countries, including positive findings on CT scan at diagnosis were significant
USA, UK, Australia, and Singapore among others [1215]. factors. Persistent or recurrent disease was not found to
By the 5-year follow-up, 14% of the 88 patients had died increase mortality, compatible with a previous report from
from the disease within a year and an additional 48% died our institution [9].
from unrelated causes within 4.5 years of diagnosis. Initial
reports of MEO mortality prior to the advent of anti-pseudomonas 4.1. Older age
antibiotics were 50% [1]. Despite a clear decline in disease-specific
mortality, MEO has high mortality for an infectious disease. The Patients older than 70 had up to 11-fold higher risk for
overall mortality of 62% is not surprising taking into account mortality; comparable with previous findings [9]. Older
patients' ages and comorbidities. patients are at higher risk for all cause mortality and for
disease-specific mortality. In Israel, MEO in patients over
70 years of age increases the mortality rate by a factor of 6
(5.47% vs. 32.88%) [16]. Franco-Vidal et al. in an analysis of 46
patients and Loh and colleagues in an analysis of 19, did not
Table 2 Relation of prognostic factors to disease specific
find that age affected patient outcomes [14,17].
mortality.
Odds 95% Wald p 4.2. Diabetes mellitus
ratio value
confidence limits
Early publications suggested that MEO occurs exclusively in
Positive CT scan 4.5 1.513.6 <.0001
patients with DM [1]. Since then, several studies have reported
Diabetes mellitus 1.6 0.475.4 0.009
MEO in non-diabetic patients, as well [2,1114,18,19]. Contem-
Facial nerve palsy 3.3 110.6 <.0001
Old age 11 1.590 0.0021 porary studies diagnosed MEO in as many as 49% of non-
diabetic patients [13] and in as few as 5% [14]. Similar to other
 AM ER IC AN JOURNAL OF OT OLARYNGOLOGYH E A D A N D NE CK M E D IC IN E A ND S U RGE RY 3 7 (2 0 1 6) 4 254 3 0
reports [17,20], 25% of the patients in our series did not have
diabetes.
The classic form of MEO is thought to be due to
P. aeruginosa infection in diabetic patients. In a series of 20
patients, Candace et al. demonstrated that fewer MEO
patients with other bacteria (MRSA for example) have
diabetes (55% vs. 100%) [15]. Chen et al. described similar
findings [18]. Our results differed in that 75% of patients in
each group (those with and without positive P. aeruginosa
culture) had diabetes. Diabetes predisposes patients to MEO
by causing microangiopathy and impaired blood circulation
in the external auditory canal, hence, interfering with the
ability of immune cells to respond to P. aeruginosa and other
bacterial infections [1920]. Chin et al. followed 24 patients
with MEO, of which 54% were diabetic, with an average HA1C
of 9% (range 7.4%13.4%). They suggested that poor glycemic
control contributes to disease development [12]. However,
others failed to demonstrate a relationship between glycemic
control and disease outcomes [14,20].
Diabetes was found to be a significant risk factor for
disease-specific mortality, since all patients who died from
causes related to MEO, within a year had diabetes and it
increased mortality by 3-fold. These results can be attributed
to other mortality risk factors, such as decreased renal
function and vasculopathies that are attributed to diabetes
and influence patient response and tolerance to treatment.
4.3. Facial nerve palsy
Early publications about MEO reported cranial nerve paralysis
at disease presentation, of which the facial nerve is most
commonly involved [1,21]. This factor was reported to
increase mortality by 50% [21]. A previous report from our
institution, compared 7 patients with facial paralysis at
disease presentation to 41 patients without paralysis and
found no significant difference in survival. More severe
manifestation was seen on CT in the facial paralysis group
[8]. Similarly, Mani et al. found no difference in mortality for 6
patients with facial nerve paralysis among 23 with MEO. Their
results demonstrated that patients with facial nerve palsy did
not regain complete recovery despite medical treatment [22].
Franco-Vidal et al. published their experience of 46 patients
and showed that facial paralysis presented in 20% and was a
significant risk factor for mortality [17]. Loh et al. showed a
similar trend in 19 patients 4 of whom presented with palsy
[14]. According to the classification of Stevens et al., facial
nerve palsy defines a severe form of MEO and was correlated
to increased mortality [11].
Among the 88 patients with MEO in our center, 15
presented with facial nerve paralysis, of which 5 died from
the disease (42% disease-specific mortality). Facial nerve
paralysis was related to a 3-fold increased risk of mortality
in the first year compared to patients with no paralysis.
The facial nerve is in close proximity to the external
auditory canal. Hence, it is the first cranial nerve to be
affected by the disease. It is logical to assume that the
aggressive inflammatory features of MEO can penetrate to
the temporal bone and other adjacent nerves. Small sample
sizes might have prevented previous series from finding a
significant correlation.
429
4.4. Positive CT scan
Many imaging methods have been suggested for diagnosing
and following MEO patients. CT scan has been proven as a
useful diagnostic tool. However, its role in routine follow-up
and prognosis is debatable. CT-positive features such as bone
erosion, which occurs after bone demineralization, may take
months to develop and are irreversible [23].
We found that positive CT scan findings in disease
diagnosis, increase mortality within the first year 4.5-fold.
However, no specific area of involvement TMJ, NP, IFT,
mastoid or skull base and no anterior or posterior involvement
was a significant cause of increased mortality. Peleg et al.
suggested that MEO patients with severe disease will
have involvement of two or more of the following areas in
CT scan TMJ, temporal bone and skull base [10].
Chin et al. designed an imaging grading system, where grade I
represents soft tissue involvement, II mastoid, III temporal bone and
IV anterior or posterior skull base. They found a positive correlation
between hospitalization days and the grading system [12].
Loh et al. correlated prognosis to minor (EAC tissue
swelling, mastoid involvement) and major (IFT, TMJ and NP
involvement) CT findings, but found no significant correlation.
However, among 5 patients in which imaging demonstrated
clivus involvement, a positive correlation to mortality was seen
[14]. Sudhoff et al. found no correlation with prognosis [23].
Stevens et al. included involvement of 2 sites on CT scan as a
designation of severe MEO [11].
We advocate CT scan for all patients when MEO is
suspected. Positive CT findings will not only help confirm
the diagnosis, but also predict a more severe outcome. In
contrast to others who evaluated CT as prognostic tool, we did
not find specific areas of involvement correlated with
prognosis and we believe that when any site involve with
disease in a CT scan is sufficient to predict worse outcomes.
Other imaging techniques commonly used in our center are Tc
and gallium scans. Technetium scan is highly sensitive for diagnosing
MEO, but less specific, since it is also positive for malignancies and
trauma. The scan will remain positive until cessation of osteoblastic
activity, thus its limited role in follow up [6,13]. Gallium scan is the
imaging of choice for follow-up, since it returns to normal once
inflammation subsides. However, both methods do not provide
adequate anatomical reference for disease spread and neither was
found to correlate with disease severity in our results. MRI was shown
to be useful for soft tissue involvement; [10,24] but it is less accessible
than other imaging modalities in our center.
Recently, other advanced nuclear imaging techniques have
been suggested [25]. These methods combine physiological as well
as anatomical views of the infection and will hopefully provide a
single, superior method for the diagnosis and follow up of MEO.
This study is limited by its retrospective design, relatively
small sample, and restriction to single-center experience.
5. Conclusion
5.1. Proposed prognostic scale
We propose the following model as a prognostic scale for
disease-specific mortality. It is a simple scale based on clinical
430 AM ER IC AN JOURNAL OF OT OLA RYNGOLOGYH E A D A N D NE CK M E D ICI N E AN D S U RGE RY 3 7 (2 0 1 6) 4 25 4 3 0
and imaging information available from patients diagnosis to
evaluate prognosis directly from patients presentation and
may help in determining treatment aggressiveness and
patient and family education. Each of the following variables
has a disease-specific mortality risk and will receive one
point: age above 70 years, DM, facial nerve palsy, and positive
CT scan findings. Our results demonstrate that having more
than 2 points increases mortality in the first year, 8-fold
compared to having 2 points or fewer. Larger, prospective
studies are needed to improve understanding of this devas-
tating disease.
Author contributions
Sagit Stern - conception and design, acquisition and analysis
of data drafted the article.
Yaniv Hamzany - conception and design, acquisition of
data, drafted the article.
Ethan Soudry - conception and design, acquisition of data,
drafted the article,
Ben Nageris - conception and design, acquisition and analysis
of data, drafted the article.
All authors gave final approval of version to be published.
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