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American Journal of OtolaryngologyHead and Neck Medicine and Surgery 32 (2011) 470 476
www.elsevier.com/locate/amjoto

Antibiotic resistance and otomycosis in the draining ear:


culture results by diagnosis
James E. Saunders, MD, FACSa,, Ryan P. Raju, MD, MBAb , John L. Boone, MDc ,
Nathan W. Hales, MDd , Wayne E. Berryhill, MDb
a

Abstract

Section of Otolaryngology, Dartmouth-Hitchcock Medical Center, Lebanon, NH, USA


Department of Otorhinolaryngology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA
c
University of Texas Health Science Center, San Antonio, TX, USA
d
San Antonio Head and Neck, San Antonio, TX, USA
Received 31 August 2010

Objective: The objective of the study was to better define changes in the bacteriology of suppurative
otitis in recent years and the role of cultures in the management of these patients.
Study Design: A retrospective review was performed.
Methods: Outpatient records from 170 patients collected over 3 years with information regarding the
bacteria cultured, antibiotic resistance, and clinical diagnosis were analyzed.
Results: A large variety of organisms were seen, with Staphylococcus aureus, Corynebacterium sp,
and Pseudomonas aeruginosa being the most common. Forty percent of cultures showed bacteria
with moderate antibiotic resistance, whereas 5% were sensitive to only intravenous antibiotics.
Resistant bacteria were found in all diagnosis categories and were significantly higher in cases of
chronic mastoiditis. The rate of methicillin-resistant S aureus infections was 7.8% and was
significantly higher in cases of chronic myringitis. Fungus was often cultured in patients without
clinical signs of otomycosis.
Conclusions: Community-acquired ear infections may be caused by antibiotic-resistant bacteria in a
substantial number of patients. In our opinion, outpatient cultures play an important role in the
management of suppurative otitis.
2011 Elsevier Inc. All rights reserved.

1. Introduction
The draining ear is a frequently encountered complaint
in an otolaryngologic practice. Aural drainage may be due
to a variety of causes including otitis externa, myringitis,
otitis media with perforation, infected cholesteatoma,
otorrhea following tympanoplasty tube placement, and
mastoiditis. Ototopical agents and oral antibiotics are the
cornerstone of treatment of the draining ear. These
treatments are generally based on empirical decisions
regarding the most common bacteria for a given diagnosis.
Corresponding author. Section of Otolaryngology, Dartmouth-Hitchcock
Medical Center, One Medical Center Dr, Lebanon, NH 03756, USA.
Tel.: +1 603 650 8124; fax: +1 603 650 0052.
E-mail address: james.saunders@hitchcock.org (J.E. Saunders).
0196-0709/$ see front matter 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.amjoto.2010.09.009

Previous studies have shown relatively low rates of resistant


bacteria. Hence, cultures are not often obtained from
draining ears. There is a paucity of literature describing
the role for culturing in the management of the draining
ear. Based on a significant rise in recent years of resistant
bacteria in the outpatient setting, the role of culture in the
treatment of the draining ear requires reevaluation.
Perhaps the most worrisome of these trends is the growing
incidence of methicillin-resistant Staphylococcus aureus
(MRSA) in both nosocomial and community-acquired
infections over the past decade. In 2003, approximately
60% of staphylococcus isolates were shown to be MRSA [1].
Community-acquired MRSA infections have been rising as
well [2]. The otologic incidence of MRSA has been reviewed
by a few authors, with reported rates between 6% and 12%
[3,4]. Other bacterial genii, such as Pseudomonas and

J.E. Saunders et al. / American Journal of OtolaryngologyHead and Neck Medicine and Surgery 32 (2011) 470476

471

specific data included the organism, the presence of


resistance, and the sensitivity spectrum. Because of complexity of analyzing multiple bacteria and sensitivities for
each infection cultured, the sensitivity of each culture isolate
was graded on a Likert scale as follows: 0 = sensitive to all
appropriate antibiotics; 1 = resistant to some appropriate oral
or topical antibiotics; and 2 = resistant to all oral antibiotics,
only sensitive to intravenous antibiotics. Bacteria given a
score of 1 or 2 were deemed to be resistant. Cultures that
showed intermediate resistance (Minimium Inhibitory Concentration [MIC] = 8) to a particular antibiotic were
considered sensitive to that antibiotic for the purposes of
this study. It should be noted that sensitivity to linezolid was
not included in the culture data.
The patient charts were also reviewed for clinical findings
suggestive of a fungal infection (fungal mats or spores).
Patients with persistent or recurrent infections within 3 months
were considered a single infection event rather than separate
infections. Culture results were, therefore, considered to be
from separate events if 3 months had elapsed between cultures.
Bacterial resistances, correlation with previous treatment, and
diagnosis were analyzed statistically using a Fisher exact t test.
The level of statistical significance was set at P .05.

Corynebacterium, have also demonstrated resistance patterns that are often refractory to traditional therapy [5,6]. In
addition to identifying resistant strains of bacteria, obtaining
a culture may help identify cases of otomycosis which
commonly present as a painful, draining ear and can be a
great imitator of resistant otorrhea [7,8]. Approximately
10% of otitis externa is of fungal origin [8] and is less likely
to respond to standard antibacterial treatment [9]. The
incidence of fungal infections as a cause for post
tympanostomy tube otorrhea has risen in the period since
the advent of fluoroquinolone drops, with Candida and Aspergillus being the most commonly isolated species [10].
The purpose of this study is to examine trends in culture
data from chronically draining ears over the past 3 years and,
in particular, look for correlations between the specific
diagnosis at the time of culture, the organism(s) cultured, and
the resistance patterns of the bacteria isolated.

2. Methods
The clinic charts and culture results of 170 patients with
draining ears that were cultured and with various underlying
diagnoses were retrospectively reviewed. These diagnoses
included otitis externa, myringitis, otitis media with
perforation, infected cholesteatoma, otorrhea following
tympanostomy tube placement, and mastoiditis. It is our
practice to obtain a culture in ears that do not respond to
empirical therapy, show signs of impending complications,
have a history of resistant organisms, have evidence of
granulation tissue, or show signs suspicious of otomycosis.
Cultures obtained in chronic mastoiditis were taken from
open mastoid cavities. Although cultures were not obtained
from all patients with aural drainage, cultures were obtained
from the vast majority of such cases. All culture specimens
were obtained in the outpatient setting of an academic
otology practice from October 1, 2003, to September 30,
2006. Funding for this study was interdepartmental.
Information obtained from the clinical chart included the
primary and secondary diagnoses, suspicion of fungus at the
time of the initial examination, and culture results. Antibiotic
sensitivity and resistance patterns were assigned according to
National Committee for Clinical and Laboratory Standards
approved procedures for antibiotic sensitivity testing and
reporting. In this way, the antibiotic spectra tested reflect
appropriate antibiotics for the specific bacterial type. Culture

2.1. Ethical considerations


There were no specific ethical concerns in this retrospective study. Patient health information confidentiality was
maintained during the acquisition and analysis of data. This
study was approved by the Institutional Review Board of the
University of Oklahoma Health Sciences Center.
3. Results
Clinical information from 170 patients was reviewed,
comprising 243 infection events from 188 ears and 286
different cultures. The distribution was predominantly male
(101:79), and the patient ages ranged from 3 months to 90
years, with a mean age of 34.6 years. The number of patients,
the number of infection events, and the total number of
bacterial isolates for each diagnosis category are listed in
Table 1. Despite the tertiary clinical setting, many of these
patients (54%) had not been previously treated. The
distributions of specific bacterial isolates for each diagnosis
category are demonstrated in Table 2. Staphylococcus
aureus, Corynebacterium sp, and Pseudomonas aeruginosa

Table 1
Bacteriology results per diagnosis

No. of patients
No. of infections
No. of cultures
No. of bacterial isolates
Cultures with resistant bacteria

Otitis
externa

Myringitis

Chronic otitis
media

Infected
cholesteatoma

Posttube
otorrhea

Chronic
mastoiditis

32
37
39
49
6

32
40
48
47
16

40
55
72
74
17

12
15
16
20
8

48
67
74
92
18

24
29
36
40
15

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J.E. Saunders et al. / American Journal of OtolaryngologyHead and Neck Medicine and Surgery 32 (2011) 470476

Table 2
Specific bacteria by diagnosis
Bacteria
Achromobacter xylosoxidans
Acinetobacter baumannii
Alcaligenes xylosoxidans
Bacteroides
Corynebacterium sp
Diphtheroids
Enterobacter cloacae
Escherichia coli
Fusobacterium nucleatum
Gram-neg rod
Haemophilus influenzae
Klebsiella pneumoniae
Morganella morganii
Moraxella catarrhalis
MRSA
Peptostreptococcus sp
Propionibacterium acnes
Proteus mirabilis
P aeruginosa
P fluorescens
Serratia
S aureus
S auricularis
S epidermidis
Staphylococcus, coag neg
Staphylococcus sp
Stenotrophomonas maltophilia
Streptococcus -hem
Streptococcus group A
Streptococcus pneumoniae
S viridans
Other

Otitis externa

Myringitis

Otitis media
w/ perforation

Cholesteatoma

Posttube
otorrhea

Mastoiditis

1 (1.82%)

1(2.00%)

1 (1.75%)

8 (14.04%)
1 (1.75%)

1 (4.76%)

7 (12.73%)

2 (2.15%)
9 (9.68%)
1 (1.08%)
1 (1.08%)
1 (1.08%)

2 (9.52%)
3 (14.29%)

5 (5.38%)
1 (1.08%)
2 (3.64%)

3 (5.26%)

7 (12.73%)

1 (1.75%)
13 (22.81%)

1 (1.82%)
11 (20.00%)

1 (1.75%)
12 (21.05%)

2 (3.64%)

4 (7.02%)

1 (1.82%)
8 (4.55%)
1 (1.82%)
1 (1.82%)

1 (1.75%)

7 (7.53%)
2 (2.15%)
1 (1.08%)
13 (13.98%)
1 (1.08%)
2 (2.15%)
12 (12.90%)
2 (2.15%)
1 (1.08%)
2 (2.15%)

1 (4.76%)
2 (9.52%)
1 (4.76%)
1 (4.76%)

1
1
2
1
1
1

(4.76%)
(4.76%)
(9.52%)
(4.76%)
(4.76%)
(4.76%)

2 (3.64%)

3 (3.23%)
1 (1.08%)
1 (1.08%)

1 (4.76%)

(2.00%)
(20.00%)
(4.00%)
(4.00%)

1 (2.00%)
2 (4.00%)

1 (4.76%)
1 (1.08%)
5 (5.38%)

1 (1.82%)

1 (1.75%)

1
10
2
2

1 (0.96%)
1 (0.96%)
1 (0.96%)
4 (3.85%)

2 (3.51%)
1 (1.75%)

2 (1.92%)
4 (3.85%)
16 (15.38%)
2 (1.92%)

1 (2.00%)
1 (0.96%)
2 (1.92%)
1 (0.96%)
2 (1.92%)

1 (2.00%)

12 (11.54%)

3 (6.00%)

16 (15.38%)

8 (16.00%)

2 (1.92%)
10 (9.62%)

2 (4.00%)
2 (4.00%)
2 (4.00%)

2 (1.92%)
1 (0.96%)
7 (6.73%)
1 (0.96%)
5 (4.81%)

3 (6.00%)

Percentages are of total culture isolates.


Non-MRSA staph aureus or MSSA (methicillin sensative Staph aureus).

were the most commonly isolated bacteria. Polymicrobial


cultures were seen in 49.7% (142/286) of instances. Cultures
containing both bacteria and fungus were seen in 20.2% (58/

Fig. 1. Frequency of resistant bacterial isolates by diagnosis as a percentage


of the total infection events.

Table 3
Species of resistant bacteria
Bacteria species

No. of isolates

Corynebacterium sp
S aureus
S epidermis
P aeruginosa
A xylosoxidans
S pneumoniae
Bacteroides sp
E coli
M moraxella
S maltophilia
H influenzae
P acnes
Serratia marcescens
S auricularis
S capitis
P mirabilis
-Hemolytic Streptococcus sp
Staphylococcus sp
Peptococcus sp

14
12
12
7
4
4
3
3
3
3
2
2
2
2
2
1
1
1
1

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473

and Pseudomonas being the most commonly isolated. The


percentage of infection events with MRSA is demonstrated
in Fig. 2 as a percentage of the total infection events for each
diagnosis. The MRSA infections were more common in
cases of chronic myringitis (17.5%) compared with the rate
in all other diagnoses (7.8%). This relationship was
statistically significant (P = .0213).
The data were compared for the 3 consecutive years of the
study (October 2003 to September 2006) and are shown in
Table 4. There was no difference in the overall number of
infections with resistant bacteria on culture (26.6%, 29.6%,
and 26.9%, respectively). Although there was a slight
increase in the percentage of MRSA infections seen for
these 3 years (6.3% to 8.6%), these differences were not
statistically significant (P N .05). Likewise, the number of
cultures demonstrating bacteria with quinolone resistance
(2.5%, 8.4%, and 4.3%, respectively) demonstrated no
statistical trend in the short period of this study.
Positive fungal cultures were fairly common in our
population (58 of 243 infections) and were distributed across
all diagnosis categories as demonstrated in Fig. 3. The most
common species of fungus overall were Candida albicans
(15 isolates) and C parapsilosis (15 isolates), followed by
Aspergillus niger (10 isolates) and A fumigatus (5 isolates).
Other less common fungal isolates found in this group of
patients included Scedosporium apiospermum, Scopularius
sp, Absidia sp, Penicillium sp, and Rhodotorula rubra. The
specific fungal isolates for each diagnosis are shown in
Table 5. Eighty percent (58/72) of the positive fungal
cultures were mixed infections with positive bacterial
cultures as well. Documented clinical findings suggestive
of otomycosis were present in only 38% of positive fungal
cultures. The total number of fungal isolates for each
diagnosis and the percentage of these that did not have
documented findings indicating a fungal infection are also
shown in Fig. 3.

Fig. 2. Frequency of MRSA infections by diagnosis as a percentage of total


infection events.

286) cultures. Fungus alone grew in 4.9% (14/286) of


cultures, and 16.4% of the cultures showed no growth.
Further analysis of the culture results demonstrated that
14.3% (41/286) were sensitive to all commonly used
antibiotics (resistance grade = 0) and that 40.2% (115/286)
of cultures contained a bacteria with resistance to some oral
antibiotics (resistance grade = 1). Bacteria resistant to all oral
antibiotics (resistance grade = 2) were found in 5.2% of
cultures. The remaining 40.3% of cultures showed no growth
or did not have sensitivities performed. When looking at
infection events, 14.8% (36/243) had cultures that were
resistance grade = 0; 45.3% (110/243) were resistance
grade = 1; and 5.3% (13/243) cultures had bacteria with
resistance grade = 2.
Overall, resistant bacteria were found in 45.5% (132/286)
of cultures and 50.6% (121/142) of infection events. The
numbers of cultures with at least one resistant bacterial
isolate are also demonstrated for each diagnosis in Fig. 1.
Note that cultures with resistant bacteria were found across
all diagnosis categories. Infected cholesteatoma, mastoiditis,
and myringitis showed the highest percentages of resistant
bacteria (53%, 52%, and 40%, respectively). Of these
diagnoses, only chronic mastoiditis was statistically significant (P = .0087) when compared with the other diagnoses.
Methicillin-resistant S Aureus was found in 7.8% (19/
243) of infection events. Quinolone resistance was noted in
4.5% (11/243) of infection events. As evidenced in Table 3,
antibiotic resistance was also found in a wide variety of
different bacteria, with Corynebacterium, Staphylococcus,

4. Discussion
Antibiotic therapy has greatly facilitated the management
of ear infections; however, frequent antibiotic use and misuse
have led to the development of resistant strains, complicating
the management of the draining ear. The role of culture in
chronic infections of the ear has not been clearly defined. In
this study, we found a wide variety of both bacterial and
fungal organisms. Staphylococcus, Corynebacterium, and

Table 4
Bacterial resistance trends
Year

Infection
events

Total
cultures

MRSA % of
infections

% of infections with
resistant bacteria

Cultures with
quinolone resistance

Oct 2003-Sep 2004


Oct 2004-Sep 2005
Oct 2005-Sep 2006

79
71
93

104
80
102

6.3%
8.5%
8.6%

26.6%
29.6%
26.9%

2.5%
8.4%
4.3%

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J.E. Saunders et al. / American Journal of OtolaryngologyHead and Neck Medicine and Surgery 32 (2011) 470476

Fig. 3. Number of fungal isolates by diagnosis and portion of fungal isolates


with and without clinical signs of otomycosis.

Pseudomonas were the most common genii found. Approximately half of the cultures showed resistance to commonly
used antibiotics including second- and third-generation
penicillins, cephalosporins, azithromycin, clindamycin, and
some fluoroquinolones. When looking at specific diagnoses,
chronic mastoiditis in an open cavity was also found be
significantly associated with a higher incidence of resistant
bacteria. The clinical significance of this rate of resistance is
unclear, as mechanical debridement plays an important role
in the management of these infections.
A worrisome finding is the presence of highly resistant
bacteria that were resistant to all oral antibiotics. These
patients have been challenging to treat successfully and
sometimes require hospitalization or long-term intravenous
antibiotics. The presence of fluoroquinolone-resistant cultures is also concerning, as these medications are routinely
used in patients with otorrhea and are given routinely after
tympanostomy tube placement. Quinolone-resistant Pseudomonas has been reported in a group of pediatric patients
with recurrent otorrhea refractory to initial treatment [11].
In this study, MRSA was isolated from 7.8% of infection
events. This is comparable to previous reports [3,4]. Trends
across the 3 years studied failed to show significant increases

in resistant bacteria, including MRSA. Three years is likely


too short of a period to derive significant trends. Methicillinresistant S aureus was more commonly found in patients
with chronic myringitis (17.5%), followed by chronic otitis
media and otitis externa. The increased presence of MRSA in
patients with chronic myringitis was shown to be statistically
significant. These patients tend to require longer courses and
multiple rounds of antibiotic treatment that may result in
increased resistance. Linezolid may provide another option
in treating MRSA infections.
In addition to MRSA, we found a significant number of
infections in our study due to resistant bacteria that were
previously considered to be nonpathogenic, including
resistant strains of Corynebacterium sp and S epidermidis.
These trends are consistent with altered behavior of these
bacteria observed elsewhere, but have not been previously
described in the ear [6,12]. Both Corynebacterium sp and S
epidermidis are competent biofilm formers [13-15], and
biofilms have been shown to play an important role in
chronic otitis media and cholesteatoma [16-18]. In addition,
S epidermidis have been isolated in 9.1% of otitis externa
[19] and 3.8% of middle ear effusions [20]. Likewise, Corynebacterium sp have been isolated in adenoid biofilms [21]
as well as in 7.4% of middle ear cultures at the time of tube
insertion [22] and have also been implicated as a causative
factor in otitis media [23]. Corynebacteria sp are generally
thought to be commensal, but are considered emerging
pathogens at other sites [15]. It has also been proposed that
the high resistance of these bacteria may serve as a gene
reservoir for other bacteria. Based on these observations and
our finding of these bacteria as the sole isolate in purulent
aspirates, we consider these bacteria as potential pathogens.
It seems likely that they are playing at least a contributory
role in these infections.
Previous studies have suggested that the diagnosis of
fungal otitis can be made based on physical findings [7]. The
appearance of fungal mats and fruiting bodies suggests a
fungal infection. Thick, white debris suggests candidiasis;
and black hyphae are characteristic of Aspergillus infections

Table 5
Specific fungal isolates by diagnosis
Otitis
externa
S apiospermum
Scopulariopsis sp
Absidia sp
Penicillium sp
R rubra
A flavus
A fumigatus
A niger
C albicans
C lipolytica
C parapsilosis
C tropicalis

Myringitis

Otitis media
w/ perforation

Cholesteatoma

Posttube
otorrhea

Mastoiditis

1 (2.0%)
1 (0.96%)
1 (1.08%)
1 (1.82%)
1 (1.75%)
2 (3.5%)
3 (5.26%)

1 (1.82%)
1 (1.82%)
1 (1.82%)

2 (3.51%)

6 (10.91%)

Percentages are of total culture isolates.

1 (1.08%)
1 (1.08%)
5 (5.38%)
5 (5.38%)
1 (1.08%)
5 (5.38%

2 (1.92%)
2 (1.92%)
4 (3.85%)
1 (4.75%)

1 (0.96%)
1 (0.96%

3
1
2
2

(6.0%)
(2.0%)
(4.0%)
(4.0%)

J.E. Saunders et al. / American Journal of OtolaryngologyHead and Neck Medicine and Surgery 32 (2011) 470476

[6,7]. In our study, only 38% of positive fungal cultures had


documented findings suggestive of otomycosis. The
expected physical findings may be obscured by the presence
of mixed bacterial and fungal infections, as was seen in 81%
of patients with positive fungal cultures in this study. These
results suggest that a fungal infection may be present in the
absence of classic physical findings and should therefore be a
consideration in treating the draining ear.
There are some limitations to this study. All patients in
this study were treated in a large academic setting, primarily
by otologists. This tertiary referred practice may be reflected
in that 46% of patients in this study had been previously
treated with antibiotics, which may lead to a higher rate of
resistance. The relationship between prior treatment and
antibiotic resistance is dealt with in a separate report. The
retrospective nature of this study may present some recall
bias particularly in regard to physical findings at the time of
diagnosis. Regional variations in bacterial resistance may
also affect the ability to generalize these findings to other
populations [24].
The role of ototopical treatment in culture-directed
therapy also bears mentioning. The clinical significance of
bacterial resistance with the availability of ototopical
medications is unclear given potentially high concentrations
of these drugs in the ear. The high concentration of drops in
the middle ear space may overcome the MIC of certain
bacteria. However, variable concentrations of ototopical
drops have been reported at the middle ear mucosa and may
be dependent on the amount of drainage from the ear [25]
Ideally, cultures should be taken before initiating
antibiotic treatment; however, this does add to the cost of
patient care. The cost of a culture at our institution, including
gram stain, bacterial culture, fungal culture, and sensitivity,
is approximately $75.00. This cost must be weighed against
potential savings in shortening the course of treatment and
decreased recurrence rates. Cultures at initial presentation are
also less likely to be contaminated by topical therapy,
potentially altering culture results.
Based on our findings, we would recommend obtaining
cultures in cases of chronic otitis media, infected chronic
myringitis, cholesteatoma, otitis externa, chronic mastoiditis, and posttympanostomy tube otorrhea that are
refractory to initial treatment. Based on the significantly
higher levels of MRSA in patients with chronic myringitis,
we also feel that cultures should be considered at initial
presentation in these patients. The cost benefit of initial
cultures in these diagnoses remains unresolved. We are
currently analyzing treatment outcomes and the effects of
prior treatment from our data.

5. Conclusion
A wide variety of bacterial and fungal pathogens were
isolated from cultures of chronically draining ears. Resistant
organisms were seen in 50.6% of infectious events, and

475

highly resistant organisms were seen in approximately 5% of


infections. Methicillin-resistant S aureus was found to be
significantly higher in patients with chronic myringitis. The
presence of fungus was also demonstrated in ears without
clinical suspicion for otomycosis. Future studies may help to
further clarify the role of culture in the management of
suppurative otitis.

References
[1] Rice LB. Antimicrobial resistance in gram-positive bacteria. Am J Med
2006;119(6, Suppl 1):S11-9.
[2] Eady E, Cove J. Staphylococcal resistance revisited: communityacquired methicillin resistant Staphylococcus aureusan emerging
problem for the management of skin and soft tissue infections. Curr
Opin Infect Dis 2003;16:103-24.
[3] Walshe P, Rowley H, Timon C. A worrying development in the
microbiology of otitis externa. Clin Otolaryngol 2001;26:218-20.
[4] Hwang J, Chu C, Liu T. Changes in bacteriology of discharging ears. J
Laryngol Otol 2002;116:686-9.
[5] Coticchia J, Dohar J. Methicillin-resistant Staphylococcus aureus
otorrhea after tympanostomy tube placement. Arch Otolaryngol Head
Neck Surg 2005;131:868-73.
[6] Otsuka Y, Kawamura Y, Koyama T. Corynebacterium resistens sp.
nov., a new multidrug-resistant coryneform bacterium isolated from
human infections. J Clin Microbiol 2005:3713-7.
[7] Ho T, Vrabec J, Yoo D. Otomycosis: clinical features and treatment
implications. Otolaryngol Head Neck Surg 2006;135:787-91.
[8] Vijay J, Pal M, Mishra G. Etiological significance of Candida albicans
in otitis externa. Mycopathologia 2003;156:313-5.
[9] Osguthorpe J, Nielsen D. Otitis externa: review and clinical update.
Am Fam Physician 2006:1510-6.
[10] Martin T, Kerschner J, Flanary V. Fungal causes of otitis externa and
tympanostomy tube otorrhea. Int J Pediatr Otorhinolaryngol
2005;69:1503-8.
[11] Jang C, Park S. Emergence of ciprofloxacin-resistant pseudomonas
in pediatric otitis media. Int J Pediatr Otorhinolaryngol 2003;67:
313-6.
[12] Hueber J, Goldman J. Coagulase-negative staphylococci: role as
pathogens. Annu Rev Med 1990;50:223-36.
[13] Stevens NT, Greene CM, O'Gara JP, et al. Biofilm characteristics of
Staphylococcus epidermidis isolates associated with device-related
meningitis. J Med Micorbiol 2009;58(Pt 7):855-62.
[14] Otto M. Staphylococcus epidermidisthe accidental' pathogen. Nat
Rev Microbiol Aug 2009;7:555-67.
[15] Gomes DL, Martins CA, Faria LM, et al. Corynebacterium diphtheriae
as an emerging pathogen in nephrostomy catheter-related infection:
evaluation of traits associated with bacterial virulence. J Med
Microbiol 2009;58:1419-27.
[16] Chole RA, Faddis BT. Evidence for microbial biofilms in cholesteatomas. Arch Otolaryngol Head Neck Surg 2002;128:1129-33.
[17] Dohar JE, Hebda PA, Veeh R, et al. Mucosal biofilm formation on
middle-ear mucosa in a nonhuman primate model of chronic
suppurative otitis media. Laryngoscope 2005;115:1469-72.
[18] Saunders J, Murray M, Alleman A (2010) Biofilms in chronic
suppurative otitis media and cholesteatoma: scanning electron
microscopy findings Am J Otolaryngol [Epub ahead of print].
[19] Roland PS, Stroman DW. Microbiology of acute otitis externa.
Laryngoscope 2002;112(7 Pt 1):1166-77.
[20] Parkinson AJ, Cuthbert M, Bulkow L, et al. Bacterial pathogens in
chronic otitis media with effusion in Alaska Native children. Alaska
Med 1999;41:27-33.
[21] Kania RE, Lamers GE, Vonk MJ, et al. Characterization of mucosal
biofilms on human adenoid tissues. Laryngoscope 2008;118:128-34.

476

J.E. Saunders et al. / American Journal of OtolaryngologyHead and Neck Medicine and Surgery 32 (2011) 470476

[22] Poetker DM, Lindstrom DR, Edmiston CE, et al. Microbiology of


middle ear effusions from 292 patients undergoing tympanostomy tube
placement for middle ear disease. Int J Pediatr Otorhinolaryngol
2005;69:799-804.
[23] Simonet M, De Briel D, Boucot I, et al. Coryneform bacteria isolated
from middle ear fluid. J Clin Microbiol 1993;31:1667-8.

[24] Marple B, Brunton S, Ferguson B. Acute bacterial rhinosinusitis: a


review of U.S. treatment guidelines. Otolaryngol Head Neck Surg
2006;135:341-8.
[25] Ohyama M, Furuta S, Ueno K. Ofloxacin solution in patients
with otitis media. Arch Otolaryngol Head Neck Surg 1999;125:
337-40.