The microbiology of chronic rhinosinusitis: Results of a community surveillance study.

Abstract

In view of the rapidly changing patterns of antibiotic resistance, community surveillance studies are providing important information to help guide practitioners in making their choice of antibiotics. For this community surveillance study, we performed a retrospective chart review of nasal and sinus culture data obtained from 83 patients with typical symptoms of chronic rhinosinusitis who visited a community otolaryngologist in Rochester, New York. Pathogens were isolated in 59 of these patients (71%). The most common were coagulase-negative staphylococci (31% of isolates). Among the other isolated pathogens were Hemophilus influenzae (25%), Streptococcus pneumoniae (12%), Moraxella catarrhalis (10%), Pseudomonas aeruginos a (7%), alpha-hemolytic streptococci (5%), and Staphylococcus aureus (3%). Approximately 39% of the coagulase-negative staphylococci isolates were resistant to penicillin. Some 20% of the Hinfluenzae isolates were beta-lactamase-positive, and 14% of all isolates were resistant to multiple a ntibiotics. Approximately 12% of the 83 patients cultured positive for multiple organisms. Our findings provide important surveillance information about the resistance patterns of pathogens in our area. Although the prevalence of betalactamase-positive H influenzae that we observed was consistent with those of other reports, we found a lower prevalence of polymicrobial flora. Our findings suggest that culture- and sensitivity-directed therapy should be effective in the treatment of chronic rhinosinusitis.

Introduction

Community-acquired rhinosinusitis is an increasingly common disorder that adversely affects quality of life and places a financial burden on the healthcare system. Community-acquired rhinosinusitis is becoming increasingly common. Its growing prevalence presents a problem with regard to our patients' perceived need for antimicrobial therapy and the costs involved in providing such treatment. Patients with symptoms of rhinosinusitis frequently consult primary care physicians and otolaryngologists.

As defined by the International Rhinosinusitis Advisory Board, acute infectious rhinosinusitis is a condition in which inflammation and infection of the nasal and sinus mucosa are of limited duration--that is, less than 12 weeks. [1] Although these infections can recur, the mucosa does recover between episodes.

The definition of chronic sinusitis is more nebulous and continues to evolve. According to the international advisory board, chronic sinusitis lasts longer than 12 weeks and often causes residual damage to the sinus mucosa, which can lead to long-term symptoms. Chronic rhinosinusitis has been estimated to affect 14.6% of the population. [1]

We are faced with critical questions regarding the etiology of chronic rhinosinusitis and its optimal treatment. It is commonly believed that the complexity of the flora increases as a result of selection pressure from multiple courses of antibiotics. The polymicrobial nature of chronic sinusitis, coupled with increasing antibiotic resistance, makes chronic rhinosinusitis a challenge to manage. Ideally, antibiotic therapy should be directed by culture and sensitivity results.

Many bacterial organisms have been identified in the sinus tracts of patients with chronic rhinosinusitis and are reported in the literature, but there is no consensus as to their microbiology [2-10] Initial studies by Frederick and Braude in the 1970s implicated polymicrobial pathogens and emphasized the importance of anaerobes [9] More recent studies, however, have downplayed the role of anaerobes (anaerobes accounted for [less than]6% of isolates in most series) and have implicated Staphylococcus and Streptococcus spp as major pathogens. [2-8,10] Some of these authors have suggested that the inconsistencies in reporting are the result of variations in culture techniques and the fastidious nature of anaerobes.

Two recent studies suggested that coagulase-negative staphylococci are important pathogens in chronic rhinosinusitis.[2,8] Most studies that have evaluated the microbiology of chronic rhinosinusitis have been conducted in major medical centers, where organisms can differ from those that are prevalent in the community. As reported by Biel et al in 1998, the widespread use of broad-spectrum oral antibiotics can alter the nature of pathogens that cause chronic rhinosinusitis, including their resistance patterns.[2] With the current emphasis on the judicious use of antimicrobial agents, the importance of community surveillance studies cannot be underestimated.[11] Physicians who treat chronic rhinosinusitis in a community setting need timely and accurate information on resistance patterns in their area.

In this article, we describe our study of the organisms encountered in a community otolaryngologic practice in patients with chronic rhinosinusitis. It was our objective to better understand the prevalence of organisms and the patterns of antibiotic resistance in the community of Rochester, New York. The data presented in this article support other findings that have implicated coagulasenegative staphylococci as potential pathogens, and they complement existing data regarding the increasing prevalence of beta-lactamase-positive Hemophilus influenzae. Our findings also support the practice of culture- and sensitivity-directed therapy, because we believe that polymicrobial chronic rhinosinusitis is not as prevalent as has been previously thought.

Materials and methods

We retrospectively reviewed culture data in the charts of 83 patients who had been diagnosed with either an acute exacerbation of chronic rhinosinusitis or with persistent disease. These patients had been seen between June 1997 and June 1998, and they had reported the typical symptoms of chronic rhinosinusitis as defined by the International Rhinosinusitis Advisory Board: persistent posterior nasal drainage, nasal congestion, nasal obstruction, headache, chronic cough, and/or facial pain.[1] Most of these patients had been previously treated with antibiotics, either at a primary care physician's office or by one of the otolaryngologist authors (J.H.). A subset of patients had also undergone previous surgical treatment.

Culture specimens had been obtained after the nasal passage was sterilized and anesthetized with a topical solution of 4% cocaine. A swab was passed into the middle meatus under endoscopic guidance and directed to the site of mucopurulent discharge. In those patients who had previously undergone sinus surgery, the swab was passed directly into the maxillary sinus or ethmoid cavity. All swabs were cultured for aerobes by standard techniques. In addition, a fungal culture was obtained from one patient who had a known history of allergic fungal sinusitis. Because these cultures had been obtained in an outpatient setting, the media for culture and the methods of transport to the laboratory precluded obtaining anaerobic cultures. Specimens were cultured in accordance with standard typing and identification techniques, and sensitivity tests were performed according to the Kirby-Bauer method.

Results

Fifty-nine of the 83 patients (71%) yielded identifiable isolates (table 1). Multiple organisms were identified in 10 patients (12%), while 41 patients (49%) had only one infecting organism (table 2).

Coagulase-negative staphylococci were the most common pathogens (31% of all isolates), followed by H influenzae (25%), Streptococcus pneumoniae (12%), Moraxella catarrhalis (10%), Pseudomonas aeruginosa (7%), alpha-hemolytic streptococci (5%), and Staphylococcus aureus (3%). Of the 18 cases of coagulase-negative staphylococci, seven (39%) were penicillin-resistant. Of the 15 H influenzae isolates, three (20%) were betalactamase-positive. Overall, eight of the 58 isolates (14%) were resistant to multiple antibiotics.

Discussion

The predominant aerobic bacteria reported in previous studies of chronic rhinosinusitis were staphylococcal and streptococcal spp. [2,5,7,8] The primary organisms were often coagulase-negative staphylococci. Our findings are consistent with those of these earlier studies in that coagulase-negative staphylococci were the most prevalent isolates (31%). These organisms have been reported to be present in 22 to 75% of all isolates, and they have long been considered to be a contaminant. In 1995, Ramadan suggested that coagulase-negative staphylococci might in fact be a pathogen [8] Coagulase-negative staphylococci were the only isolates in 43% of Ramadan's patients with chronic rhinosinusitis. The study by Biel et al found that coagulase-negative staphylococci were the sole isolates in 53% of their cases. [2] Our findings are consistent with these reports. The pathogenicity of these isolates is further supported by sensitivity results. Seven of the 18 coagulase-negative staphylococci isolates (39%) were found to be penicillin-resistant. Although the exact role of coagulase-negative staphylococci in chronic rhinosinusitis requires further clarification, our study provides additional evidence of its role as a pathogen.

Beta-lactamase-positive strains of H influenzae have been reported in 25 to 50% of isolates, and this number is increasing annually. [4] Recent data suggest that the antimicrobial agents traditionally used for acute rhinosinusitis (e.g., amoxicillin and trimethoprim/sulfamethoxazole) might be undergoing a decline in efficacy. [11,12] Our findings demonstrate that beta-lactamase-positive strains of H influenzae are indeed prevalent (three of the 15 H influenzae isolates [20%] were found to be beta-lactamase-positive), and they are also consistent with those of previous reports. Brook et al previously suggested that in patients with polymicrobial flora, the presence of betalactamase-producing strains can decrease the efficacy of antibiotics by shielding bacteria from them. [4] Further studies in this area are warranted, given the high percentage of positive beta-lactamase strains.

It is generally believed that the paranasal sinuses of patients with chronic rhinosinusitis are colonized by multiple organisms. Our study suggests that the percentage of polymicrobial infections in these patients is less than previously thought. Only 10 of our 83 patients (12%) were infected with more than one organism, which suggests that narrow-spectrum antibiotic coverage might be as effective as a broad-spectrum agent. This idea, long advocated for the treatment of acute rhinosinusitis, appears to be advisable for the treatment of chronic rhinosinusitis, as well.

The continuing rise in antimicrobial resistance complicates the antibiotic selection process and increases the failure rate of empiric broad-spectrum treatments. [13] Culture and sensitivity results remain the gold standard for directing appropriate therapy, and they are even more valuable when the flora are monomicrobial.

In conclusion, recent studies evaluating the impact of chronic rhinosinusitis on a patient's physical well-being have revealed that these patients experience major decrements in their health. [14] Moreover, the total number of prescriptions for antibiotics and the total cost of treatment are both increasing. [13] Concomitant with the increase in antibiotic use is an increase in antibiotic resistance by bacterial organisms. Therefore, the role of community surveillance becomes most crucial. Our findings suggest that coagulase-negative staphylococci are likely a pathogen and that beta-lactamase-positive strains of H influenzae are increasingly prevalent. Therefore, we recommend sensitivity testing and culture-directed therapy in view of our belief that the organisms involved in chronic rhinosinusitis are less polymicrobial than previously reported.

From the Division of Otolaryngology, University of Rochester School of Medicine and Dentistry, Rochester, N.Y.

Reprint requests: James Hadley, MD, Division of Otolaryngology, University of Rochester School of Medicine and Dentistry, 1065 Senator Keating Blvd., Suite 210, Rochester, NY 14618. Phone: [phone]; fax: [phone]; e-mail: [e-mail]

References

(1.) International Rhinosinusitis Advisory Board. Infectious Rhinosinusitis in Adults: Classification, Etiology and Management. Ear Nose Throat J 1997;76(12 Suppl):5-17.

(2.) Biel MA, Brown CA, Levinson RM, et al. Evaluation of the microbiology of chronic maxillary sinusitis. Ann Otol Rhinol Laryngol 1998;107:942-5.

(3.) Wald ER. Microbiology of acute and chronic sinusitis in children and adults. Am J Med Sci 1998;316:13-20.

(4.) Brook I, Yocum P. Frazier EH. Bacteriology and beta-lactamase activity in acute and chronic maxillary sinusitis. Arch Otolaryngol Head Neck Surg 1996;122:418-23.

(5.) Brook I, Thompson DH, Frazier EH. Microbiology and management of chronic maxillary sinusitis. Arch Otolaryngol Head Neck Surg 1994;120:1317-20.

(6.) Brook I. Bacteriology of chronic maxillary sinusitis in adults. Ann Otol Rhinol Laryngol 1989;98:426-8.

(7.) Brook I. Aerobic and anaerobic bacterial flora of normal maxillary sinuses. Laryngoscope 1981;91:372-6.

(8.) Ramadan HR. What is the bacteriology of chronic sinusitis in adults? Am J Otolaryngol 1995:16:303-6.

(9.) Frederick J, Braude AI. Anaerobic infection of the paranasal sinuses. N Engl J Med 1974:290:135-7.

(10.) Doyle PW, Woodham JD. Evaluation of the microbiology of chronic ethmoid sinusitis. J Clin Microbiol 1991;29:2396-400.

(11.) Poole MD. Antimicrobial therapy for sinusitis. Otolaryngol Clin North Am 1997:30:331-9.

(12.) Muntz HR, Lusk RP. Bacteriology of the ethmoid bullae in children with chronic sinusitis. Arch Otolaryngol Head Neck Surg 1991:117:179-81.

(13.) Kaliner MA, Osguthorpe JD, Fireman P. et al. Sinusitis: Bench to bedside. Current findings, future directions. J Allergy Clin Immuno] 1997;99(Suppl):S829-48.

(14.) Gliklich RE, Metson R. The health impact of chronic sinusitis in patients seeking otolaryngologic care. Otolaryngol Head Neck Surg 1995;l 13:104-9.

Table 1. Number (%) of organisms isolated from 59 positive cultures
obtained from 83 patients with chronic rhinosinustis
Isolate                    n (%)
Coagulase-negative        18 (31)
staphylococci
Hemophilus influenzae     15 (25)
Streptococcus pneumoniae   7 (12)
Moraxella catarrhalis      6 (10)
Pseudomonas aeruginosa     4 (7)
Aipha-hemolytic            3 (5)
streptococci
Staphylococcus aureus      2 (3)
Fungus                     1 (2)
Proteus spp                1 (2)
Group B streptococci       1 (2)
Enterobacter aerogenes     1 (2)
Table 2. Number (%) of patients categorized by the number of isolates
  No. isolates    No. patients (%)
       0               32 (39)
       1               41 (49)
       2                9 (11)
[greater than or         1 (1)
  equal to] 3
     Total            83 (100)