Warning: mkdir(): Permission denied in /home/virtual/lib/view_data.php on line 81 Warning: fopen(/home/virtual/audiology/journal/upload/ip_log/ip_log_2024-04.txt): failed to open stream: No such file or directory in /home/virtual/lib/view_data.php on line 83 Warning: fwrite() expects parameter 1 to be resource, boolean given in /home/virtual/lib/view_data.php on line 84 Nasal Colonization of Methicillin-Resistant <i xmlns="">Staphylococcus aureus</i> in Patients with Chronic Suppurative Otitis Media

Nasal Colonization of Methicillin-Resistant Staphylococcus aureus in Patients with Chronic Suppurative Otitis Media

Article information

Korean J Audiol. 2012;16(2):75-79
Publication date (electronic) : 2012 September 20
doi : https://doi.org/10.7874/kja.2012.16.2.75
Department of Otorhinolaryngology, Yonsei University College of Medicine, Seoul, Korea.
Address for correspondence: Eun Jin Son, MD, PhD. Department of Otorhinolaryngology, Yonsei University College of Medicine, Gangnam Severance Hospital, 211 Eonju-ro, Gangnam-gu, Seoul 135-720, Korea. Tel +82-2-2019-3460, Fax +82-2-3463-4750, ejson@yuhs.ac
Received 2012 August 12; Revised 2012 August 28; Accepted 2012 September 06.

Abstract

Background and Objectives

Methicillin-resistant Staphylococcus aureus (MRSA) is one of major pathogens in patients with chronic suppurative otitis media (CSOM). In addition to intrinsic MRSA infection of the mastoid air cell system, nasal colonization of MRSA, a known predictor of postoperative surgical site infection, may pose increased risk of postoperative complications. The purpose of this study is to describe microbiology of preoperative nasal swab screening and localized middle ear specimens in patients undergoing otologic surgeries.

Subjects and Methods

Forty-nine consecutive patients with CSOM who underwent middle ear surgery were included. Preoperative nasal swabs for MRSA, and preoperative and intraoperative middle ear swabs were collected and compared for pathogens.

Results

Preoperative nasal swab screening confirmed MRSA colonization in 3/49 patients (6.1%) and methicillin-resistant coagulase-negative Staphylococcus (MRCNS) in 9/49 patients (18.4%). Correlation with preoperative culture results and nasal swab screening results were compatible in 2/4 patients with positive nasal swab for MRSA and 1/9 patients with positive nasal swab for MRCNS. Postoperative conversion to MRSA was observed in 3 patients.

Conclusions

The rate of nasal MRSA colonization among patients with CSOM was higher than among the general community. Preoperative MRSA colonization was associated with MRSA from middle ear specimens. Further studies are warranted to investigate the possible benefit of preoperative treatment of MRSA colonized patients undergoing middle ear surgeries.

Introduction

Chronic suppurative otitis media (CSOM) is an inflammatory disease of the middle ear and mastoid air cell system, which can result in irreversible changes not only in the middle ear structures but also in the inner ear.1) Dysfunction of the Eustachian tube and the bacterial infection are important factors in the multifactorial pathogenesis of CSOM. In order to eradicate inflammation, prevent recurrence and restore middle ear structures and hearing, both medical and surgical treatment modalities are important in CSOM. It has been emphasized that selection of appropriate antibiotics should be based on the bacteriologic studies to identify the pathogens and determine sensitivities.2,3)

Recent bacteriologic studies of the middle ear discharge in CSOM in Korea have reported increasing prevalence of methicillin-resistant Staphylococcus aureus (MRSA).2,4,5) In addition, Staphylococcus aureus (S. aureus) and Pseudomonas species were most predominant from the postoperative otorrhea cultures.3) Higher rates of postoperative otorrhea and reperforation after tympanomastoid surgeries were reported in CSOM patients with MRSA cultured from preoperative ear discharge.6)

In addition to intrinsic MRSA infection of the mastoid air cell system, nasal colonization of MRSA may pose increased risk of postoperative infection. Nasal colonization rate of MRSA and it is a known predictor of postoperative surgical site infection.7,8) Previous studies have identified bacterial pathogens from the middle ear and the mastoid air cells, or nasopharynx as a bacterial reservoir in CSOM.4,5,9-12)

However, few studies have focused on the effect of nasal MRSA colonization in the otologic surgery. The aims of this study are to examine the prevalence of nasal MRSA colonization in patients undergoing otologic surgeries and to determine the association between MRSA colonization and the pathogens identified from perioperative culture studies.

Subjects and Methods

The study included 66 consecutive patients (25 males and 41 females) undergoing tympanomastoid surgeries from May 2010 to December 2011 at the Yonsei University College of Medicine Gangnam Severance Hospital. Patients with intracranial or extratemporal complications of CSOM, known history of external radiation, known history of corticosteroid therapy preoperatively, or those undergoing emergency operations were excluded. The mean age at operation was 51.7±15.7 years (range 34-74 years), and the right ear was operated in 34 ears, the left in 32 ears.

Upon the initial visit in the outpatient department, the external auditory canal was cleaned, and the middle ear discharge was collected with collected with cotton swabs through sterile otoscopes, taking care not to touch the external auditory canal skin. To assess nasal colonization of S. aureus, a nasal swab was taken before the operation in addition to routine preoperative testing. The nasal samples were obtained by cotton swab from the anterior vestibular of the nares by the physician. During the operation, intraoperative culture specimens were taken in cases with overt discharge in the middle ear cavity. During postoperative period of 1 month, postoperative culture specimens were again taken in cases with otorrhea through the external auditory canal. All culture samples were in Stuart transport medium and transported to the laboratory, where the samples were inoculated onto blood agar, MacConkey's agar, and chocolate agar plates. All plates were incubated at 37-C aerobically under 5% (v/v) CO2 and examined 24 and 48 hours later. Bacteria were identified morphologically using Gram staining and biochemically. Susceptibility testing was performed using disk diffusion. Identified pathogen species and antimicrobial susceptibility were compared between nasal swab and perioperative (preoperative, intraoperative and postoperative otorrhea) cultures. Statistical analysis was performed with Fisher's exact testusing SPSS statistical software (version 15.0; SPSS Inc., Chicago, IL, USA). The criterion for statistical significance was p<0.05.

Results

Among the 67 patients undergoing operation for CSOM, nasal swab confirmed bacterial colonization in 37 (55.2%) patients (Table 1). Clinically importantly, nasal cavity colonization of S. aureus was noted in 10/67 (14.9%) of patients, and 4/67 (6.0%) patients were positive for MRSA. Also, methicillin-sensitive Staphylococcus aureus (MSSA) was identified in 9/37 (23.4%) and methicillin-resistant coagulase-negative Staphylococcus (MRCNS) in 11/67 (13.4%) of patients. Preoperative ear culture studies identified pathogens in 39/67 (58.2%) of the patients: the most commonly identified species was Staphylococcus [MRCNS 26.9%, methicillin-sensitive coagulase-negative Staphylococcus (MSCNS) 1.5%, MRSA 13.4% and MSSA 11.9%]. Intraoperatively, overt discharge from the middle ear mucosa was noted in 40 ears. Most of the intraoperative culture results were negative (28/40 ears, 71.8%). MRSA was found in 3/40 (4.5%) ears, MSSA in 2 ears (3.0%), MRCNS in 2 ears (3.0%) and MSCNS in 1 ear (1.5%). After the surgery, 11 of the 67 patients developed otorrhea within 1 month postoperatively. The postoperative culture studies identified MRSA in 3/11 (27.3%) and Acinetobacter species in 1/11 (9.1%) and fungus in 2/11 (18.1%) patients (Table 2). No pathogens were identified in the remaining 5 patients (45.5%).

Table 1

Organisms identified from nasal swabs, compared to the preoperative otorrhea, intraoperative middle ear culture results

Table 2

Organisms identified from postoperative otorrhea cultures from 11 patients that developed postoperative infection

The isolated organisms were compared between the nasal swab and perioperative cultures (Fig. 1). Preoperative ear culture results and nasal swab culture results showed significant difference (p=0.001), as well as intraoperative middle ear cultures and postoperative otorrhea culture results showed significant difference (p=0.023). However, no significant difference was noted between preoperative ear and postoperative otorrhea culture results (p=0.493). Then we compared the culture results according to the presence of bacterial growth and reports of no growth (Fig. 2). No significant difference was noted between preoperative ear culture, and nasal swab culture results (p=0.055), between preoperative ear and postoperative otorrhea culture results (p=0.068), or nasal swab and postoperative otorrhea culture results (p=0.094). Lastly, the culture results were compared according to the presence of antibiotic resistance (Fig. 3). No significant difference was noted between the antibiotic-susceptible and resistant strains identified between preoperative ear culture and nasal swab cultures (p=0.098), or between preoperative ear and postoperative otorrhea cultures (p=0.053).

Fig. 1

Comparison of organisms identified from perioperative cultures and nasal swab. (A) Preoperative ear culture results (Preop ear) and nasal swab (Nasal) culture results showed significant difference (p=0.001). However, no significant correlation was noted between Preop ear and postoperative (Postop) culture results (B). (C) Intraoperative middle ear cultures (Intraop) and Postop culture results showed significant difference (p=0.023). *p<0.05.

Fig. 2

Comparison of culture results according to the presence of bacterial growth. No significant difference was noted between the presence of bacterial growth or no growth when the culture results were compared: (A) preoperative ear culture (Preop ear), and nasal swab (Nasal), (B) Preop ear and postoperative (Postop) culture, or (C) Nasal and Postop.

Fig. 3

Comparison of culture results according to the presence of antibiotic resistance. No significant difference was noted between the antibiotic-susceptible and resistant strains identified when the culture results were compared between (A) preoperative ear culture (Preop ear), and nasal swab (Nasal), (B) Preop ear and postoperative (Postop) culture.

Then we analyzed the correlation of isolated organisms from the nasal swab and other cultures in patients with nasal colonization of antibiotic-resistant strains (Fig. 4). Among 4 patients with identified with nasal MRSA colonization, preoperative ear cultures were also positive for MRSA in 3 patients (75.0%). However, intraoperative culture identified MRSA in only one patient, and none of the patients developed MRSA infection postoperatively. Twelve patients were identified with nasal MRCNS colonization. Preoperative ear cultures reported MRSA in 1, MRCNS in 1, and MSCNS in 7, ciprobay-resistant Pseudomonas in 1, and no growth in 2 patients. MRCNS was identified from intraoperative culture in only 1 patient. Again, only 1 patient developed otorrhea due to MRSA in the postoperative period.

Fig. 4

Diagram to show the analysis of the perioperative culture results from the patients identified with nasal MRSA or MRCNS colonization. MRSA: methicillin-resistant Staphylococcus aureus, MRCNS: methicillin-resistant coagulase-negative Staphylococcus, MSCNS: methicillin-sensitive coagulase-negative Staphylococcus, CRP: ciprobay-resistant Pseudomonas.

Discussion

Staphylococcus and Pseudomonas species are most frequent pathogens in CSOM. Increasing incidence of antibiotic-resistant bacterial strains in CSOM patients poses a challenge to not only the selection of appropriate antibiotics therapy, but also to prevent the emergence of resistance to glycopeptides, the main drugs chosen for MRSA. It has been reported that patients who are colonized with S. aureus are the main source of S. aureus in hospitals, and that nasal carriage of MRSA increases the risk of postoperative infection. Since the rate of methicillin resistance is higher in Korean CSOM patients compared to other countries, we examined the rate of nasal MRSA colonization. The rate of nasal carriage of MRSA in CSOM patients was higher than among healthy individuals reported as 0.2-2.8% of the United States population.7) Although this study was limited to small number of patients, the finding may suggest that in addition to nosocomial infection, community-acquired MRSA infection may contribute partially to the relatively higher rate of MRSA in CSOM patients in Korea. On the other hand, the rates of bacterial isolation from preoperative ear discharge, intraoperative middle ear discharge, or postoperative otorrhea cultures in our patients were lower. Also, the perioperative culture studies frequently reported no growth of pathogens. Given that the patients were prescribed with antibiotics prior to surgery, it may signify that current antibiotics are effective in infection control during the tympanomastoid surgery. Furthermore, the interpretation of the culture results from postoperative otorrhea is limited since antibiotics were routinely used postoperatively in all patients and culture samples were taken from the external auditory canal in cases with overt otorrhea or from wet surface of the grafted tympanic membrane immediately after removal of the packing material at 2 weeks postoperatively. The culture results can only reflect that MRSA infection that could not be controlled by routine antibiotics, which may be clinically significant.

MRSA is a common pathogen in otologic diseases. MRSA has been identified not only in CSOM patients,2,3,5,13) but also in patients with external otitis.14) S. aureus has been implicated in biofilm formation complicating cochlear implants.15-17) Nasal MRSA colonization deserves attention since transmission from nasal carriage to surgical site infections or bacteremia is possible, and it is associated with increased morbidity and mortality. Previous studies have reported that elimination of nasal MRSA colonization reduces the risk of postoperative infections.8,18,19) Application of 2% mupirocin calcium ointment to the nares has been proven to be effective, and chlorhexidine-based solutions is used to reduce the density of skin colonization of MRSA preoperatively.18-20) A recent study compared the rates of MRSA infection in otolaryngology surgeries, before and after implementation of preoperative screening and treatment of nasal MRSA carriage.21) Further studies are warranted to investigate the possible benefit of preoperative treatment of MRSA colonized patients undergoing middle ear surgeries.

Conclusion

The rate of nasal MRSA colonization among patients with CSOM was higher than among the general community. Preoperative MRSA colonization was associated with MRSA from middle ear specimens. Further studies are warranted to investigate the possible benefit of preoperative treatment of MRSA colonized patients undergoing middle ear surgeries.

References

1. Bluestone CD. Epidemiology and pathogenesis of chronic suppurative otitis media: implications for prevention and treatment. Int J Pediatr Otorhinolaryngol 1998;42:207–223. 9466224.
2. Lee SK, Yeo SG, Hong SM, Sim JS, Hong CK, Lee YC, et al. Bacteriology of chronic otitis media: changing of detection rate of methicillin-resistant Staphylococcus aureus and Pseudomonas aeruginosa. Korean J Otorhinolaryngol-Head Neck Surg 2008;51:9–15.
3. Shim HJ, Park CH, Kim MG, Lee SK, Yeo SG. A pre- and postoperative bacteriological study of chronic suppurative otitis media. Infection 2010;38:447–452. 20700754.
4. Yu YI, Cha CI, Lee IY, Byun JY, Cho JS. Current bacteriology of chronic suppurative otitis media. Korean J Otolaryngol-Head Neck Surg 2004;47:607–611.
5. Ahn JH, Kim MN, Suk YA, Moon BJ. Preoperative, intraoperative, and postoperative results of bacterial culture from patients with chronic suppurative otitis media. Otol Neurotol 2012;33:54–59. 22143302.
6. Nam EC, Kim MN, Lee KS. Surgical results of MRSA (Methicillin-resistant S. aureus)-isolated chronic otitis media. Korean J Otolaryngol-Head Neck Surg 1999;42:1238–1243.
7. Ellis MW, Hospenthal DR, Dooley DP, Gray PJ, Murray CK. Natural history of community-acquired methicillin-resistant Staphylococcus aureus colonization and infection in soldiers. Clin Infect Dis 2004;39:971–979. 15472848.
8. Kuehnert MJ, Kruszon-Moran D, Hill HA, McQuillan G, McAllister SK, Fosheim G, et al. Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001-2002. J Infect Dis 2006;193:172–179. 16362880.
9. Albert RR, Job A, Kuruvilla G, Joseph R, Brahmadathan KN, John A. Outcome of bacterial culture from mastoid granulations: is it relevant in chronic ear disease? J Laryngol Otol 2005;119:774–778. 16259653.
10. Chang J, Lee SH, Choi J, Im GJ, Jung HH. Nasopharynx as a microbiologic reservoir in chronic suppurative otitis media: preliminary study. Clin Exp Otorhinolaryngol 2011;4:122–125. 21949577.
11. Madana J, Yolmo D, Kalaiarasi R, Gopalakrishnan S, Sujatha S. Microbiological profile with antibiotic sensitivity pattern of cholesteatomatous chronic suppurative otitis media among children. Int J Pediatr Otorhinolaryngol 2011;75:1104–1108. 21715027.
12. Yeo SG, Park DC, Hong SM, Cha CI, Kim MG. Bacteriology of chronic suppurative otitis media--a multicenter study. Acta Otolaryngol 2007;127:1062–1067. 17851935.
13. Jung H, Lee SK, Cha SH, Byun JY, Park MS, Yeo SG. Current bacteriology of chronic otitis media with effusion: high rate of nosocomial infection and decreased antibiotic sensitivity. J Infect 2009;59:308–316. 19715725.
14. Walshe P, Rowley H, Timon C. A worrying development in the microbiology of otitis externa. Clin Otolaryngol Allied Sci 2001;26:218–220. 11437845.
15. Antonelli PJ, Lee JC, Burne RA. Bacterial biofilms may contribute to persistent cochlear implant infection. Otol Neurotol 2004;25:953–957. 15547425.
16. Brady AJ, Farnan TB, Toner JG, Gilpin DF, Tunney MM. Treatment of a cochlear implant biofilm infection: a potential role for alternative antimicrobial agents. J Laryngol Otol 2010;124:729–738. 20214837.
17. Pawlowski KS, Wawro D, Roland PS. Bacterial biofilm formation on a human cochlear implant. Otol Neurotol 2005;26:972–975. 16151345.
18. Doebbeling BN, Reagan DR, Pfaller MA, Houston AK, Hollis RJ, Wenzel RP. Long-term efficacy of intranasal mupirocin ointment. A prospective cohort study of Staphylococcus aureus carriage. Arch Intern Med 1994;154:1505–1508. 8018006.
19. Reagan DR, Doebbeling BN, Pfaller MA, Sheetz CT, Houston AK, Hollis RJ, et al. Elimination of coincident Staphylococcus aureus nasal and hand carriage with intranasal application of mupirocin calcium ointment. Ann Intern Med 1991;114:101–106. 1898585.
20. Pofahl WE, Ramsey KM, Nobles DL, Cochran MK, Goettler C. Importance of methicillin-resistant Staphylococcus aureus eradication in carriers to prevent postoperative methicillin-resistant Staphylococcus aureus surgical site infection. Am Surg 2011;77:27–31. 21396301.
21. Richer SL, Wenig BL. The efficacy of preoperative screening and the treatment of methicillin-resistant Staphylococcus aureus in an otolaryngology surgical practice. Otolaryngol Head Neck Surg 2009;140:29–32. 19130957.

Article information Continued

Fig. 1

Comparison of organisms identified from perioperative cultures and nasal swab. (A) Preoperative ear culture results (Preop ear) and nasal swab (Nasal) culture results showed significant difference (p=0.001). However, no significant correlation was noted between Preop ear and postoperative (Postop) culture results (B). (C) Intraoperative middle ear cultures (Intraop) and Postop culture results showed significant difference (p=0.023). *p<0.05.

Fig. 2

Comparison of culture results according to the presence of bacterial growth. No significant difference was noted between the presence of bacterial growth or no growth when the culture results were compared: (A) preoperative ear culture (Preop ear), and nasal swab (Nasal), (B) Preop ear and postoperative (Postop) culture, or (C) Nasal and Postop.

Fig. 3

Comparison of culture results according to the presence of antibiotic resistance. No significant difference was noted between the antibiotic-susceptible and resistant strains identified when the culture results were compared between (A) preoperative ear culture (Preop ear), and nasal swab (Nasal), (B) Preop ear and postoperative (Postop) culture.

Fig. 4

Diagram to show the analysis of the perioperative culture results from the patients identified with nasal MRSA or MRCNS colonization. MRSA: methicillin-resistant Staphylococcus aureus, MRCNS: methicillin-resistant coagulase-negative Staphylococcus, MSCNS: methicillin-sensitive coagulase-negative Staphylococcus, CRP: ciprobay-resistant Pseudomonas.

Table 1

Organisms identified from nasal swabs, compared to the preoperative otorrhea, intraoperative middle ear culture results

Table 1

MRSA: methicillin-resistant Staphylococcus aureus, MSSA: methicillin-sensitive Staphylococcus aureus, MRCNS: methicillin-resistant coagulase-negative Staphylococcus, MSCNS: methicillin-sensitive coagulase-negative Staphylococcus, CRP: ciprobay-resistant Pseudomonas, CSP: ciprobay-sensitive Pseudomonas, Fungus: Aspergillus or Candida spp.

Table 2

Organisms identified from postoperative otorrhea cultures from 11 patients that developed postoperative infection

Table 2

MRSA: methicillin-resistand Staphylococcus aureus, Fungus: Aspergillus or Candida spp.