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Abstract

Objective: Turicella otitidis and Staphylococcus auricularis have been considered normal aural flora. Their significance in active infection is controversial. We examined a series of patients presenting with acute and chronic otitis media whose ear canal culture isolated T. otitidis and S. auricularis and explored possible pathogenicity, associated factors, and outcomes. Methods: This is a retrospective chart review of patients who presented to a tertiary center outpatient clinic between 2017 and 2022 with otologic microscopic examination of active infection and ear canal culture isolating T. otitidis or S. auricularis only. Clinical course was collected including history, microscopic otoscopy findings, interventions given, outcomes, and sensitivity results. Results: A total of 13 patients (10 with T. otitidis and 3 with S. auricularis) were included. Majority of the patients had a history of otologic surgery (92%) and tympanic membrane perforation (62%). All were treated with combinations of antibiotic otic drops (ie, fluoroquinolone, sulfa, or aminoglycoside based) ± oral antibiotics (ie, penicillin or trimethoprim/sulfamethoxazole). Otorrhea resolved among majority of patients. Otorrhea and mucosalization returned or continued among 4 patients. Sensitivity results demonstrated that 2 of 3 strains of T. otitidis were resistant to clindamycin. There was no resistance against S. auricularis for tested antibiotics. Conclusions: Our findings suggest the potential pathogenicity of T. otitidis and S. auricularis, especially among patients with prior ear surgery and tympanic membrane perforation. Violation of the epithelial barrier from surgery or trauma may contribute to their pathogenicity. Future study is warranted to elucidate pathogenicity of normal aural flora and its mechanisms.

Keywords

otitis media ear infection

Introduction

Turicella otitidis and Staphylococcus auricularis are part of the normal flora of the external auditory canal.¹ Isolation of T. otitidis and S. auricularis from otorrhea in patients presenting with active infection is considered normal and not a treatment target.¹ Treatment is focused on common pathogens: Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, and Pseudomonas aeruginosa.

Prior reports demonstrate the possible pathogenicity of T. otitidis and S. auricularis, while the degree remains controversial.^1-3 These cases focused on pediatric patients. One study isolated T. otitidis via spontaneous drainage or direct tympanocentesis from 7 pediatric patients presenting with otitis media.² Another case report described a 3-year-old female with a posterior auricular abscess; T. otitidis was isolated in pure culture in the setting of obvious infection.³ The ability of T. otitidis to cause inflammation in a location other than the external auditory canal points toward possible pathogenicity and its ability as an organism to cause infection.

While T. otitidis is generally considered normal aural flora in the external auditory canal and found in 12% of healthy external auditory canals in young adults (ages 19-22 years),⁴ its prevalence in middle ear fluid is lower at 6.3% based on a cohort of pediatric patients in Madrid.¹ A total of 71% of those with T. otitidis in middle ear fluid had a history of prior perforation.¹ Comparatively, S. auricularis is found in 20% of healthy external auditory canals in young adults (ages 19-22 years), making it a common organism.⁴ However, the pathogenicity of S. auricularis has been described such as its capacity to form biofilms on implanted medical devices and ability to adhere to and destroy epithelial cells.⁵ There have been little to no reports describing S. auricularis in middle ear fluid or its role in otitis media.

Despite a few prior case reports describing the potential pathogenicity of the organisms that were considered normal aural flora, no study has synthesized the clinical presentation, treatment outcomes, and sensitivity results of the organisms. This case series presents 13 patients with otorrhea whose fluid culture isolated T. otitidis and S. auricularis with their clinical history, examination findings, and outcomes.

Patients and Methods

A retrospective chart review was performed over a 5 year period (2017-2022) at a tertiary surgery center in Minnesota to identify patients who had active otorrhea on otologic microscopy examination, and the culture from the external auditory canal isolated T. otitidis or S. auricularis. Eligible patients were aged 18 years and older. Patient selection is outlined in Figure 1. This study was approved by the University of Minnesota Institutional Review Board (STUDY00016223).

Figure 1.

Algorithm for patient selection.

Patient demographics (age, sex, and race) and detailed clinical characteristics (history, otologic microscopy examination, prior history of ear surgeries, presence of tympanic membrane perforation, interventions given, and outcomes) were collected from chart review.

The isolation technique for T. otitidis and S. auricularis after external auditory canal collection was as follows. The specimens were inoculated and streaked on 5% sheep blood agar, chocolate agar, MacConkey agar, and Haemophilus isolation agar, and incubated aerobically in 5% CO₂. Growth was observed at daily intervals. Any bacterial growth had gram stains performed, and bacterial colonies were identified by MALDI-TOP (matrix-assisted laser desorption/ionization time of flight) mass spectrometry on a VITEK MS instrument (bioMerieux). Any bacteria that was written as “normal flora” was then speciated to ensure all flora isolated were specifically named.

Antibiotic sensitivity results were available among a subset of patients per discretion of the microbiology laboratory at the time of culture. The drug susceptibility testing for T. otitidis used individual gradient antibiotic strips, the ETEST (bioMerieux). S. auricularis used the gram-positive antibiotic panels on the VITEK 2 instrument (bioMerieux). Antibiotics were then chosen based on these results.

Descriptive statistics and logistic regression analysis was performed to explore the factors associated with resolution of otorrhea.

Results

Patient characteristics are summarized in Table 1. The mean age was 38 years (SD: 17.8, range 18-79 years), and 62% were female. Majority of patients had a history of prior otologic surgery [including pressure-equalizing (PE) insertion; (n = 12, 92%)] and/or tympanic membrane perforation (n = 8, 61.5%). Only 4 of the patients had a major otologic surgery (30.8%).

Table 1.

Summary of Case Report Patient Characteristics (N = 13).

Characteristics	n (%)
Age (in years), mean [SD (range)]	38.3 [17.8 (18-79)]
Sex
Male	5 (38%)
Female	8 (62%)
Race
White	11 (84.6%)
Hispanic	1 (7.7%)
Unknown	1 (7.7%)
Prior otologic surgery
No	1 (7.7%)
Yes	12 (92.3%)
History of tympanic perforation
No	5 (38.5%)
Yes	8 (61.5%)

Table 2 summarizes the patient history, the otologic microscope findings, interventions, and outcomes. There was evidence of active infection on examination for all patients, while the otorrhea culture only grew T. otitidis among 10 patients and S. auricularis among 3 patients. Common pathogens accountable for otitis media or externa like Streptococcus pneumonia, Haemophilus influenzae, Moraxella catarrhalis, Pseudomonas aeruginosa, or Staphylococcus aureus were not cultured. In our clinical practice, P. aeruginosa has been the most common bacteria in patients with chronic ear disease.

Table 2.

Summary of Patient Clinical History, Physical Examination Findings, Treatment, and Outcomes.

Participant	Patient history	Microscope otoscopy examination findings	Treatment	Outcome
Turicella otititids
1	18-y-old female with a history of Turner syndrome and multiple sets of PE tubes presenting with left otorrhea.	Left ear with PE tube in the posterior inferior quadrant with perforation around it. Granulation tissue with mucoid effusion surrounding the perforation.	Ciprofloxacin-dexamethasone otic drops for 7 d. PE tube was removed in clinic.	Otorrhea resolved
2	25-y-old female with a history of PE tube placement 2 y ago for recurrent otitis media presenting with chronic right otorrhea. Prior culture grew Klebsiella, and this was treated with ciprofloxacin-dexamethasone otic drops.	Right ear with purulent otorrhea on the surface of the anterior superior TM.	Started on ciprofloxacin-dexamethasone otic drops for Klebsiella infection. At 3 wk follow-up, T. otitidis cultured and was switched to steroid-only ear drops for 2 wk.	Otorrhea resolved
3	44-y-old female with a history of left t-tube placement for TM retraction and recurrent ear infections 4 y ago presenting with left otorrhea, intermittently sanguineous. She is a bilateral hearing aid user for congenital hearing loss.	Left ear with mucoid otorrhea around a t-tube in the anterior superior quadrant.	Ciprofloxacin-dexamethasone otic drops for 14 d and amoxicillin bid for 14 d.	Lost to follow-up
4	22-y-old male with a history of right Jahn tube placement 3 y ago for chronic eustachian tube dysfunction presenting with right otorrhea and pain for 1 y.	Right ear polypoid tissue surrounding the shaft of the Jahn tube which was cultured. TM was intact and the middle ear was well aerated. Intraoperative culture was obtained during Jahn tube replacement.	Ciprofloxacin-dexamethasone otic drops for 1 mo.	Otorrhea resolved
5	61-y-old male with a history of cleft palate repair along with adenoidectomy and bilateral PE tube placement 8 y ago presenting with left ear otorrhea.	Left ear otorrhea near the hypotympanic retraction. Stable mucosalization of the TM with a perforation over the hypotympanum.	Ciprofloxacin-dexamethasone otic drops as needed. Steroid otic drops 2-3 times per week to keep ear dry.	Continuing mucosalization of left TM without signs of acute infection
6	47-y-old female with a history of right-sided chronic otitis media and cholesteatoma who underwent canal wall down tympanomastoidectomy and bone anchored hearing aid placement 4 y ago presenting with constant right otorrhea.	Right mastoid cavity with perforation of superior area of the neo-TM with extensive mucosalization of the TM down to the mastoid cavity and onto the anterior ear canal.	Oral penicillin for 21 d.	Continues to have mucosalization of mastoid cavity as well as a perforation in the superior portion of the TM
7	26-y-old male with a history of primary ciliary dyskinesia and associated recurrent otitis media who underwent multiple sets of PE tubes presenting with otorrhea.	Left ear with 40% central perforation with effusion in the middle ear.	Sulfacetamide 5 drops 2×/d to left ear for 14 d.	Otorrhea resolved
8	31-y-old female with a history of bilateral eustachian tube dysfunction who underwent multiple sets of PE tubes and right canal wall up tympanomastoidectomy 10 y ago for cholesteatoma.	Right ear with lateralized TM from prior tympanoplasty and thick surface mucosalization. 10% central perforation superiorly and a second pinpoint perforation inferiorly.	Boric acid powder application.	Otorrhea resolved
9	18-y-old female with a history of chronic otitis media and mucosalization of the TM who underwent multiple trichloroacetic acid treatment of the TM surface and left lateral graft tympanoplasty and resurfacing using a split-thickness skin graft.	Left ear with a small central anterior inferior quadrant TM perforation and mucosalization covering the inferior TM. Serous otorrhea pooling on TM.	Ofloxacin otic drops switched to sulfacetamide otic drops after culture results for 7 d. Oral clindamycin for 3 wk (switched from penicillin, doxycycline, and Bactrim due to allergic reaction).	Mucosalization and otorrhea resolved initially. Partial mucosalization returned after 6 mo
10	42-y-old male with a history of right canal wall down tympanomastoidectomy for cholesteatoma 7 y ago presenting with otorrhea and pain from right ear for several months.	Right mastoid cavity with mucoid otorrhea along the facial ridge. There was a thin layer of recurrent cholesteatoma on remnant of the malleus that was removed in clinic.	Alcohol/vinegar 10 drops once a day 3 times per week.	Otorrhea resolved
Staphylococcus auricularis
12	40-y-old female with a history of bilateral eustachian tube dysfunction who underwent bilateral tympanomastoidectomy for cholesteatoma and bilateral t-tube placement presenting for follow-up.	Left ear with t-tube in position with mucoid effusion coming through the lumen.	Hydrocortisone-acetic acid otic drops switched to fluroquinolone otic drops.	Otorrhea resolved
13	79-y-old male with a history of cholesteatoma requiring a radical mastoidectomy 40 y ago and bilateral eustachian tube dysfunction who underwent bilateral PE tube placement presenting with left otorrhea.	Left ear with t-tube in place and mucoid effusion at the base.	Sulfacetamide-prednisolone otic drops for 14 d.	Otorrhea resolved
14	45-y-old female with a history of right canal wall up tympanomastoidectomy followed by radical mastoidectomy for cholesteatoma 7 y ago presenting for follow-up. She has intermittent right otorrhea once a month.	Right mastoid cavity with a strip of mucosalization on the floor and overlying yellow-green otorrhea with crusting.	Ciprofloxacin-dexamethasone otic drops switched to gentamicin otic drops after culture results	Improved but continuing otorrhea

Abbreviations: bid, twice a day; PE, pressure equalizing; TM, tympanic membrane.

Ten out of 13 (77%) patients took antibiotic otic drops. Among the 10 patients whose culture isolated T. otitidis, 6 patients started fluoroquinolone-based otic drops, and 1 patient began sulfacetamide otic drops. Two patients completed a course of oral antibiotics: amoxicillin or penicillin. Among 3 patients whose ear canal culture isolated S. auricularis, 2 patients were started on fluoroquinolone-based otic drops and 1 on sulfacetamide otic drops. The majority of the drainage resolved after treatment. However, in 4 patients (31%), drainage and mucosalization of the tympanic membrane returned after treatment. Logistic regression analysis was performed to explore the factors associated with resolution of otorrhea. There was no significant association of otorrhea resolution with age, sex, history of perforation, or surgery. Interpretation of the results were limited due to low sample size.

Table 3 summarizes the antibiotic sensitivity results against T. otitidis and S. auricularis among a subset of patients. Of the 10 patients whose otorrhea isolated T. otitidis, 3 patients had sensitivity results available. All 3 strains were sensitive to ceftriaxone, penicillin, trimethoprim/sulfamethoxazole, and vancomycin. Two strains were resistant to clindamycin. One patient had sensitivity results available for S. auricularis. This strain of S. auricularis was sensitive to ciprofloxacin, clindamycin, erythromycin, gentamicin, levofloxacin, oxacillin, tetracycline, and vancomycin, and was not resistant to any tested antibiotics. Additional antibiotic sensitivity results for both pathogens based on prior literature are summarized in Table 3.

Table 3.

Summary of Antibiotic Sensitivity for Turicella otitidis (n = 3) and Staphylococcus auricularis (n = 1) From the Subset of Case Report Patients Who Had Sensitivity Results Available and Review of the Prior Literature.

	Susceptible	Resistant	Literature review results	Details
T. otitidis
Ceftriaxone	3 of 3		Sensitive	20/20 strains sensitive (pediatric population in Zurich)⁶
Clindamycin	1 of 3	2 of 3	Mixed	3/7 (43%) strains sensitive (pediatric population in Madrid)²
Meropenem	2 of 2		Sensitive	19/20 (95%) strains sensitive (pediatric population in Zurich)⁶
Penicillin	3 of 3		Sensitive	7/7 (100%) strains sensitive (pediatric population in Madrid)²
Trimethoprim/Sulfamethoxazole	3 of 3		Mixed	9/20 (45%) strains sensitive (pediatric population in Zurich)⁶
Vancomycin	3 of 3		Sensitive	7/7 (100%) strains sensitive (pediatric population in Madrid).² 3-y-old female with a posterior auricular abscess sensitive (Montreal)³
S. auricularis
Ciprofloxacin	1 of 1		Mixed	9/11 (82%) sensitive (hospitalized patients in Poland)⁴
Clindamycin	1 of 1		Mixed	2 resistant phenotypes from 17 calves (Luxembourg).⁷ 72% resistant in methicillin-resistant strains and 18% resistant in methicillin-sensitive strains (blood samples of patients in Turkey)⁸
Erythromycin	1 of 1		Mixed	80% resistant in methicillin-resistant strains and 37% resistant in methicillin-sensitive strains (blood samples of patients in Turkey)⁸
Gentamicin	1 of 1		Mixed	1 resistant phenotype from 17 calves (Luxembourg).⁷ 90% resistant in methicillin-resistant strains and 17% resistant in methicillin-sensitive strains (blood samples of patients in Turkey)⁸
Levofloxacin	1 of 1		N/A	N/A
Oxacillin	1 of 1		Mixed	2 resistant phenotypes from 17 calves (Luxembourg).⁷ 23.6% sensitive and 76.4% resistant (clinical isolates from 42 countries)⁹
Tetracycline	1 of 1		Mixed	2 resistant phenotypes from 17 calves (Luxembourg)⁷
Vancomycin	1 of 1		Sensitive	>99.9% of 22,000 sensitive (clinical isolates from 42 countries)⁹

Discussion

We report a series of patients who had evidence of active ear infection on the examination while the culture of the otorrhea isolated only T. otitidis or S. auricularis. Prior case reports suggest T. otitidis and S. auricularis as pathogens of complicated otitis media including mastoiditis,¹ subperiosteal abscess,³ and otorrhea with maxilla-labio-palatine cleft surgery.³ Our findings add to the prior reports and suggest T. otitidis and S. auricularis as potential pathogens of the ear despite the standard of care considering them normal aural pathogens that do not merit treatment.

The previous notion that T. otitidis was not pathogenic comes from findings of a low rate of T. otitidis cultured in the middle ear effusion compared to the external auditory canal of children with otitis media with effusion. T. otitidis was found simultaneously in both the external auditory canal and middle ear effusion in only 10% of patients.¹⁰ This led to the conclusion that T. otitidis grows exclusively in the external auditory canal and should not be a treatment target.¹⁰

In this cohort, all patients presenting with otorrhea with isolation of T. otitidis and S. auricularis had a prior history of otologic surgery and/or tympanic membrane perforation. The etiology for each patient’s tympanic membrane perforation is not completely understood, it does suggest that a violation of the ear canal skin from previous surgery or tympanic membrane perforation may change the microbiome in the canal and middle ear, causing normal aural flora to become pathogenic. The most common surgeries among this case series were PE tubes and tympanomastoidectomy.

A perforated tympanic membrane also provides a route of transmission for T. otitidis and S. auricularis. Prior studies found that a history of tympanic membrane perforation increases the incidence of T. otitidis in the middle ear fluid.¹ T. otitidis does not colonize the nasopharynx or ascend from the eustachian tube to the middle ear as other common pathogens of otitis media.¹ Less than 1% of nasopharyngeal swabs showed T. otitidis,¹¹ suggesting that tympanic membrane perforation may allow T. otitidis to colonize the middle ear space, leading to an active infection.

Studies have focused on the possible pathogenicity of T. otitidis in otitis media, leaving the role of S. auricularis in question. The similarities of S. auricularis to T. otitidis in habitat and clinical presentation strongly suggest that prior otologic surgeries or tympanic membrane perforation could leave the middle ear susceptible to S. auricularis infection. Past research found S. auricularis to have pathogenic potential through adherence to epithelial cells, biofilm formation, and destruction of human cells.⁵ This was determined from bacterial strains isolated from hospitalized patients and biofilm formation was found using crystal violet.⁵ One patient in the cohort had an osseointegrated middle ear ventilating tube in bilateral ears which may have created an environment for S. auricularis to form biofilm and become pathogenic. S. auricularis has been isolated in 2.5% of cases with otitis media. However, when present in middle ear fluid, it was present in a larger quantity which suggested its ability to replicate in the middle ear, contributing to its infectious potential.¹²

The sensitivity results for T. otitidis from our cohort were similar to prior studies that reported sensitivity to tetracycline and amoxicillin and resistance against clindamycin. Clinical samples over 5 years in Zurich reported resistance against sulfamethoxazole.¹ Varying sensitivity of different strains of T. otitidis should be considered when deciding on a course of antibiotic otic drops or oral antibiotics. The sensitivity of S. auricularis is less documented. It is sensitive to tigecycline with rifampin when growing on implanted medical devices.⁵ We did not find any antibiotic resistance for S. auricularis in our patients.

There are several limitations in this study. First, the small sample size limits our ability to determine the pathogenic potential of T. otitidis and S. auricularis (n = 13). Still, our report represents the largest series of adult patients presenting with active infection and isolation of T. otitidis and S. auricularis. Second, our report is a retrospective chart review. We are unable to establish the causality of the active infection from the pathogens isolated from culture. There may have been other pathogenic organisms that were not isolated from the culture due to sampling errors of the swab or these pathogens may have been isolated from contamination. The lack of longitudinal culture results at multiple time points from this study also makes it difficult to establish causality. Third, sensitivity results were available among a limited subset of patients as sensitivities are not typically obtained for these organisms in our laboratory and required a separate call to the microbiology laboratory to run sensitivity studies. Further study including a larger number of patients and strains of T. otitidis and S. auricularis may demonstrate other antibiotic resistance.

Our findings add to prior literature suggesting T. otitidis and S. auricularis are potential pathogens of otologic infections. Treatment against these organisms warrants consideration when isolated, especially among patients with a history of prior otologic surgery or tympanic membrane perforation. Further research is needed to examine the degree of pathogenic potential of T. otitidis and S. auricularis and their role in acute and chronic otitis media.

Footnotes

Acknowledgements

The authors thank the technical staff of the Infectious Diseases Diagnostic Laboratory at the University of Minnesota Medical Center, MHealth Fairview, and the senior Medical Director, Patricia Ferrieri, MD.

Data Availability

Data supporting this case series are not publicly available due to ethical and legal reasons as it contains sensitive patient information that patients, in this case series, have not released to the public.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Madeline M. Marker

Janet S. Choi

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