Introduction
Chronic otitis media is an inflammatory disorder that causes irreversible changes in the mucosa of the middle ear and mastoid cavity. Chronic middle-ear inflammation can lead to changes in middle-ear structures, including tympanic perforation, granulation, and deformities of the ossicles and ossicular chain, resulting in conductive or sensorineural hearing loss.Reference Sakagami, Maeda, Node, Sone and Mishiro 1 The general management of chronic otitis media includes surgery to remove the middle-ear and mastoid lesions, and reconstruction of the tympanic membrane and ossicular chain. In addition, antibiotics are used for the complete eradication of bacteria.
Prior to the selection of appropriate antibiotics, it is important to cure chronic otitis media, and bacteriological testing must be performed to determine antibiotic sensitivities.Reference Khanna, Chander, Nagarkar and Dass 2 Because of the increase in methicillin-resistant Staphylococcus aureus (MRSA) and quinolone-resistant Pseudomonas aeruginosa, broad-spectrum antibiotics may be required. In previous studies, the reported prevalence of S aureus in ear discharge ranged from 9.9 to 54.1 per cent, while that of MRSA isolates ranged from 0.3 to 24.8 per cent.Reference MacNeil, Westerberg and Romney 3
We conducted a retrospective analysis to: (1) determine the bacteriological profile during the pre-, peri- and post-operative periods of surgery for chronic otitis media; (2) assess the bacterial flora of patients with post-operative otorrhoea; and (3) facilitate the pre-operative antibiotic selection process to avoid otorrhoea after chronic otitis media surgery.
Materials and methods
We analysed the medical records of 156 patients (65 males and 91 females; 156 ears) who underwent chronic otitis media surgery at Daejeon St Mary's Hospital, Korea, from March 2012 to September 2015. Mean patient age (± standard deviation (SD)) was 51.2 ± 15.7 years (range, 6–79 years). The results of culture and antibiotic sensitivity tests performed on otorrhoea in out-patient clinics were analysed retrospectively. All patients were diagnosed with chronic otitis media, with or without cholesteatoma, based on otoscopic findings, temporal bone computed tomography, and the presence or absence of cholesteatoma for surgery. Of the 156 patients, 111 had chronic otitis media without cholesteatoma and 45 had chronic otitis media with cholesteatoma. All patients underwent surgery: 60 underwent tympanoplasty only, and 96 underwent mastoidectomy with tympanoplasty. The mean follow-up period (± SD) was 2.01 ± 1.0 years (Table I).
Table I Patient demographics
SD = standard deviation; COM = chronic otitis media; M&T = mastoidectomy with tympanoplasty
At each patient's initial visit, a pre-operative bacterial culture was prepared using otorrhoea. The external auditory canal was well cleaned and the aural discharge was collected with cotton swabs, while preventing contact with the external auditory canal, using a sterilised otoscope. If a patient did not show otorrhoea, we swabbed the mucosa of the middle-ear cavity for bacterial culture.
If the culture results revealed MRSA, the patient underwent peri-operative prophylactic antibiotic treatment with vancomycin. If the culture result was quinolone-resistant P aeruginosa, then a peri-operative prophylactic antibiotic was selected based on susceptibility testing of the pre-operative bacterial culture. If the culture result revealed other susceptible strains, then ceftizoxime (a third-generation cephalosporin) was selected as the peri-operative prophylactic antibiotic.
Chronic otitis media surgery was performed after otorrhoea had stopped for at least two weeks. A peri-operative culture was prepared with granulation tissue from either the middle ear or mastoid cavity. If the peri-operative culture result showed MRSA or quinolone-resistant P aeruginosa which was not identified in the pre-operative culture, the post-operative antibiotic was changed in accordance with the antibiotic sensitivity of the bacteria. For example, if the peri-operative culture results revealed MRSA, the post-operative antibiotic selected was trimethoprim/sulfamethoxazole. Finally, a post-operative culture was performed when otorrhoea developed after surgery.
Statistical analysis
The chi-square test or Fisher's exact test was used to compare categorical variables, and the Mann–Whitney U test was used for continuous variables. For all statistical analyses, we used SPSS® software (version 20.0); p-values of less than 0.05 were considered statistically significant.
Ethical considerations
The study protocol was reviewed and approved by the institutional review board of the Catholic University Hospital, Korea, (institutional review board number: DC16RISI0017). Informed consent was exempted by the board.
Results
Among the 156 ears, positive results from the pre-operative cultures were confirmed in 71 patients (45.5 per cent) and negative results were confirmed in 85 patients (54.5 per cent). Overall, MRSA (32.4 per cent) was the most common species, followed by methicillin-sensitive S aureus (29.6 per cent), quinolone-resistant P aeruginosa (7.0 per cent), fungus (5.6 per cent), quinolone-sensitive pseudomonas species (1.4 per cent) and other bacteria (24.0 per cent). Among the peri-operative cultures, positive results were confirmed in 21 patients (13.5 per cent); in comparison, the post-operative cultures were positive in 7 patients (4.5 per cent). Methicillin-resistant S aureus was the most common bacteria identified in all pre-, peri- and post-operative tests – it was identified in 23 of 71 cases (32.4 per cent), 11 of 21 cases (52.4 per cent), and 5 of 7 cases (71.4 per cent), respectively. Additionally, the percentage of MRSA increased from the peri- to the post-operative period (Table II).
Table II Organisms cultured during pre-, peri- and post-operative periods
Data represent numbers of cases (and percentages of bacterial pathogens divided by the total number of positive culture cases). MSSA = methicillin-sensitive Staphylococcus aureus; MRSA = methicillin-resistant S aureus; QSP = quinolone-sensitive Pseudomonas aeruginosa; QRP = quinolone-resistant Pseudomonas aeruginosa
Among 23 cases of MRSA revealed in pre-operative tests, 6 cases showed MRSA in peri-operative tests and 3 cases showed MRSA in post-operative tests; however, 2 cases of MRSA in post-operative tests did not show MRSA in either pre- or peri-operative tests. Two cases of MRSA in post-operative tests showed graft failure (Figure 1).
Fig. 1 Flow chart of organisms cultured during the pre-operative (Pre-op), peri-operative (Peri-op) and post-operative (Post-op) periods. *Two cases were positive for methicillin-resistant Staphylococcus aureus (MRSA) pre-operatively. †Case positive for methicillin-sensitive S aureus. QRP = quinolone-resistant Pseudomonas aeruginosa
For the chronic otitis media without cholesteatoma patients, culture results were positive in: 46 cases (41.4 per cent) in pre-operative tests, 10 cases (9.0 per cent) in peri-operative tests and 5 cases (4.5 per cent) in post-operative tests. For the chronic otitis media with cholesteatoma patients, culture results were positive in: 25 cases (55.6 per cent) in pre-operative tests, 11 cases (24.4 per cent) in peri-operative tests and 2 cases (4.4 per cent) in post-operative tests. Rates of positive peri-operative culture were higher in chronic otitis media with cholesteatoma patients than in chronic otitis media without cholesteatoma patients (p = 0.018), but the pre- and post-operative culture results did not show a positive relationship according to diagnosis.
Comparing tympanoplasty-only cases and mastoidectomy with tympanoplasty cases, the positive culture rates for all pre-, peri- and post-operative tests were significantly higher in the mastoidectomy with tympanoplasty cases (Table III).
Table III Relationship of positive culture result with diagnosis and operation
Data represent numbers of (and percentages) of positive culture results, unless indicated otherwise. *n = 111; † n = 45; ‡ n = 60; **n = 96. § p < 0.05. COM = chronic otitis media; M&T = mastoidectomy with tympanoplasty
The mean air–bone gap was greater in those with positive peri-operative culture results than in those with negative results (29.0 ± 10.2 vs 24.4 ± 8.5 dBHL, p = 0.014) (Table IV).
Table IV Relationship of culture result with post-operative abg
*t-test; ‡Mann–Whitney U test. † p < 0.05. ABG = air–bone gap; post-op = post-operative; pre-op = pre-operative; peri-op = peri-operative
Discussion
Although there have been many bacteriological studies of chronic otitis media, continuous and periodic evaluations are important because of: changes in the bacteria and antibiotic sensitivity, the emergence of antibiotic-resistant strains of bacteria due to the misuse of antibiotics, and nosocomial infections.Reference Jung, Lee, Cha, Byun, Park and Yeo 4 In addition, the bacteriological analysis of post-operative otorrhoea is important; failure to appropriately treat post-operative otorrhoea prevents the cure of chronic otitis media.Reference Shim, Park, Kim, Lee and Yeo 5
Pre-operative cultures of 71 (45.5 per cent) of 156 ears were positive for bacterial species; this rate is higher than the 8.3–20 per cent reported previously.Reference Indudharan, Haq and Aiyar 6 – Reference Yeo, Park, Hong, Cha and Kim 9 Among the cultured pathogens, the most common pre-operative pathogenic bacterial species identified was MRSA (32.4 per cent), followed by methicillin-sensitive S aureus (19 per cent) and P aeruginosa (including both quinolone-sensitive and quinolone-resistant pseudomonas species; 8.4 per cent). In contrast, previous studies in Korea showed that P aeruginosa was the most common pathogen identified (31.8 per cent).Reference Yeo, Park, Hong, Cha and Kim 9
Methicillin-resistant S aureus has become particularly prevalent in Europe and the USA. The proportion of cultures containing nosocomial MRSA increased worldwide from 2 per cent in 1974 to 50 per cent in 1997.Reference Lowy 10 Methicillin-resistant S aureus was first reported in England, two years after methicillin began to be used in clinics, and it subsequently became more prevalent in Europe and the USA. In Korea, the MRSA culture rate in the otorrhoea of patients with chronic otitis media increased continuously from the late 1970s to the 1990s, rising to 18.8 per cent in 1997. The prevalence of MRSA was 24.2 per cent in 2005, representing a further increase since 1997.Reference Sim, Kim, Lee and Yun 11
Methicillin-resistant S aureus was the most common bacteria identified in all pre-, peri- and post-operative tests, and the proportion of MRSA cases increased from the pre- to the post-operative period (Table II). Of 23 cases of MRSA identified in pre-operative tests, 6 cases showed MRSA in peri-operative tests and 3 cases showed MRSA in post-operative tests. The other two cases of post-operative MRSA showed no growth in either pre-operative or peri-operative tests. Only about half of the cases that showed antibiotic-resistant bacteria in post-operative otorrhoea had produced the same result in pre-operative and peri-operative tests; the other cases showed ‘no growth’ in pre-operative and/or peri-operative tests (Figure 1).
A lack of bacteria was evident in 54.5 per cent of patients pre-operatively and 86.5 per cent peri-operatively. ‘No growth’ does not mean the absence of bacteria. The failure to culture organisms from patients with chronic otitis media may have been because of the use of antibiotics prior to bacteriological testing;Reference Peters, van Agtmael, Danner, Savelkoul and Vandenbroucke-Grauls 12 in this bacteriostatic state, the amplification and/or proliferation of pathogens is reduced. Alternatively, in these patients, infection may have been caused by slowly proliferating pathogens. Therefore, culture and antibiotic sensitivity testing should be performed before the empirical use of antibiotics to decrease the frequency of post-operative otorrhoea.Reference Shim, Park, Kim, Lee and Yeo 5
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• Distribution of bacterial strains in the middle ear changed during chronic otitis media surgery
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• The percentage of resistant strains (especially methicillin-resistant Staphylococcus aureus) increased
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• Post-operative otorrhoea bacterial culture results showed low agreement with pre- or peri-operative results
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• Re-identification of bacterial strains is required if post-operative otorrhoea develops
Furthermore, if post-operative otorrhoea does occur, culture retesting should be considered, even if the cases showed negative results in pre- and peri-operative tests, and antibiotics should be selected following consideration of antibiotic-resistant bacteria.
Conclusion
According to the results of peri- and post-operative bacterial cultures, the distribution of bacterial strains in the middle ear changed during chronic otitis media surgery. The positive ratio of culture results decreased from the pre- to post-operative tests, but the percentage of resistant strains (especially MRSA) increased. As the bacterial culture results for post-operative otorrhoea showed low agreement with those for the pre- or peri-operative tests, re-identification of bacterial strains is required if post-operative otorrhoea develops.
Acknowledgement
This work was supported by the Basic Science Research Program through the National Research Foundation of Korea, funded by the Ministry of Science, ICT and Future Planning (2014R1A1A1002911).
