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Staphylococcus aureus Is a Major Pathogen in Acute Bacterial Rhinosinusitis: A Meta-Analysis

  1. Spencer C. Payne and
  2. Michael S. Benninger
  1. Department of Otolaryngology–Head and Neck Surgery, Henry Ford Health System, Detroit, Michigan
  1. Reprints or correspondence: Dr. Michael S. Benninger, Dept. of Otolaryngology–Head and Neck Surgery, Henry Ford Health System, 2799 W. Grand Blvd., K-8, Detroit, MI 48202 (mbenning{at}hfhs.org).
 
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Abstract

Background. Acute bacterial rhinosinusitis is a common health problem in the United States. Appropriate recommendations for the treatment of acute bacterial rhinosinusitis are based on the prevalence and expected antimicrobial susceptibilities of specific pathogens.

Methods. A meta-analysis was performed on the English language literature from the period 1990–2006, including prospective studies of antibiotic therapy for acute bacterial rhinosinusitis for which sinus cultures were required in the form of either maxillary sinus taps or middle meatal cultures. Weighted mean culture rates for Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, and Staphylococcus aureus were abstracted from the included articles and compared according to culture technique.

Results. Culture rates (i.e., the percentage of patients with positive culture results) were 32.7% for S. pneumoniae, 31.6% for H. influenzae, 10.1% for S. aureus, and 8.8% for M. catarrhalis. No statistically significant difference was seen between the culture rates for S. aureus and M. catarrhalis. Analysis of the effect of culture technique on the culture rates revealed no statistically significant difference.

Conclusions. The prevalence of S. aureus among sinus cultures warrants its reconsideration as a major pathogen in acute bacterial rhinosinusitis. As a result, increasing trends of drug-resistant strains may complicate antibiotic recommendations.

Acute rhinosinusitis is one of the most common health problems in the United States, with an estimated 20 million cases occurring annually [1]. Current recommendations for the diagnosis and treatment of acute bacterial rhinosinusitis (ABRS) are based on the expected prevalence and specific drug-resistance patterns of pathogens [2]. "The most common bacterial species isolated from the maxillary sinuses of patients with ABRS are Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis, the latter being more common in children. Other streptococcal species, anaerobic bacteria, and Staphylococcus aureus cause a small percentage of cases" [2, p. 2]. Numerous studies, using varying culture techniques, have researched the culture rates of these specific bacteria in an attempt to determine the exact prevalence of these bacteria. However, deep nasal swab cultures or nasopharyngeal cultures have traditionally been thought to be associated with a high rate of contamination, and the results of these tests have been unreliable [3], often casting doubt on the prevalence of S. aureus as a true pathogen in acute disease. As such, the prevalence and drug-resistance patterns of bacteria in ABRS have been determined on the basis of maxillary sinus tap results, which have indicated prevalence rates of 20%–43% for S. pneumoniae, 22%–35% for H. influenzae, 2%–10% for M. catarrhalis, and 0%–8% for S. aureus [2].

A recent study by Benninger et al. [4] indicated a strong concordance between the results of maxillary sinus taps and endoscopically guided middle meatal cultures. The study also showed a higher rate of S. aureus found on culture than had been published in the previous literature. Although M. catarrhalis infection appears to be more prevalent among children, it is uncertain whether the prevalence is similar among adults. Furthermore, this bacterium has a spontaneous resolution rate of ∼80% [2]; thus, the importance of M. catarrhalis as a major pathogen in ABRS in adults may not be as great as that of S. aureus. In addition, because of the increasing presence of community-acquired methicillin-resistant S. aureus (MRSA) infection [5], determining the rate of S. aureus in ABRS on the basis of a large scale of information has become an even more important factor in treating the disease.

Most previous studies on the rates of bacteria causing ABRS are either limited studies or case series and reviews. However, in the course of proving the efficacy of antibiotics for treating ABRS, multiple studies have been published that both required sinus cultures and provided this data to show bacteriologic cure rates. These studies were often performed on a large scale, making their data much more useful for a higher-powered analysis. The purpose of this study was to determine both the prevalence of the major pathogens causing ABRS in adults through a meta-analysis of the culture data provided by these antibiotic trials and whether the prevalence of S. aureus was greater than had previously been reported.

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Methods

Selection of studies. A retrospective review of the English language literature was performed, targeting prospective antibiotic trials of ABRS. A search of the Medline database was performed to obtain literature from the period January 1990–May 2006; the search was restricted to English language literature and human studies. The search strategy was modeled after a recent Cochrane database review of antibiotic trials of ABRS [6], using multiple search parameters to maximize the identification of prospective trials of rhinosinusitis. The abstracts identified by the search were then screened for inclusion or exclusion. Specifically, inclusion criteria included the article being a prospective antibiotic trial of adult ABRS in which cultures were performed using maxillary sinus tap or endoscopic middle meatal swab and/or aspiration. Furthermore, the culture data for major pathogens, including S. aureus, had to be provided.

All articles with abstracts that either met the inclusion criteria or did not provide sufficient information were then reviewed for exclusion. Articles were excluded if they involved pediatric patients aged <15 years, used either an unspecified or alternate culture technique (e.g., nasopharyngeal, nasal discharge, or deep nasal swab), included acute exacerbations of chronic sinusitis (unless the data were presented separately within the article), or were duplicate publications, pooled analyses, meta-analyses, or article reviews. In addition, the references of each article were reviewed for inclusion or exclusion.

Data extraction. Basic bibliographic information was recorded from each article. Data were then extracted, including demographic characteristics (age and sex distributions), the number of patients who had culture performed, the number of patients who had positive culture results, culture technique (either maxillary sinus tap or middle meatal swab and/or aspiration), and the number of isolates of the designated pathogens of interest (S. pneumoniae, H. influenzae, M. catarrhalis, and S. aureus).

Not all of the articles presented patient population or culture information in a similar manner. Culture data were presented either for the original intent-to-treat population or for the per-protocol population (i.e., those completing the study protocol). In articles in which data were available for both, data were extracted for the intent-to-treat population. In addition, culture data were provided either as the number of patients with a culture that was positive for a pathogen or the number of isolates of each pathogen cultured. Because sinus cultures can reveal multibacterial growth, the former method can be converted to the latter for data abstraction but not vice-versa. Therefore, the method of presentation of the culture data was also recorded for each study.

Statistical analysis. Analysis was performed using SAS for Windows, version 9.0 (SAS Institute). Culture rates for each of the designated pathogens were computed per article. In addition, data from the included articles were pooled, and weighted mean culture rates were computed per isolate (including all articles) and per patient (including only those articles in which data were presented on a per-patient basis). Assuming that nonparametric data were presented, the Wilcoxon signed-rank test was used to determine statistical differences between the culture rates of each of the designated pathogens of interest. The Wilcoxon rank-sum test was used to determine statistical differences between the culture rates of studies using maxillary sinus taps alone or between the culture rates of studies using either middle meatal cultures alone or in combination with maxillary sinus taps.

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Results

The initial search identified 1419 abstracts. On review, 86 met the inclusion criteria. These articles were evaluated, and after a more in-depth evaluation, 61 more articles were excluded (table 1), leaving only 25 articles for the final analysis (table 2). Sixteen articles reported the use of only maxillary sinus taps for sinus culture, and 9 articles reported the use of middle meatal culture, either alone (2 studies) or in combination with maxillary sinus taps (7 studies). Data were available for a total of 3649 cultured isolates from the specimens from ∼3126 patients who had positive culture results (2 articles did not list the number of patients from whom the isolates were derived [17, 28]). Of the 25 articles analyzed, 16 studies presented enough data to calculate the rate of positive culture results for patients with acute rhinosinusitis. The weighted mean rate of positive culture results among 5790 patients with acute rhinosinusitis was 49.3% (95% CI, 48.1%–50.6%). Data comparing the rate of positive culture results in articles reporting the use of only maxillary sinus taps with that in studies reporting the use of middle meatal cultures are shown in table 3. The rates noted are comparable to previously published information [3]. All of the included studies required radiographic verification of sinus disease, either through sinus radiograph or CT. In addition, most of the studies required a combination of these radiographic findings and 1 or 2 major signs or symptoms of ABRS, including facial pain or tenderness, nasal congestion, or purulent discharge. Four articles listed only "clinical diagnosis of ABRS" as an enrollment criterium [9, 10, 17, 19].

Table 1
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Table 1

Derivation of articles for final analysis.

Table 2
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Table 2

Characteristics of and culture rates in 25 antibiotic studies of acute bacterial rhinosinusitis.

Table 3
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Table 3

Percentage of patients who had positive culture results.

A weighted mean value analysis for the 25 articles was performed to determine the culture rates for the 4 major pathogens. For all 25 articles, the mean values were computed for both the percentage of cultures yielding each pathogen in relation to the total number of isolates found on culture. For the 16 articles that presented data on a per-patient basis, and the percentage of the patients for whom each pathogen was found on culture was also calculated (table 4). Overall, S. pneumoniae and H. influenzae were the most frequently cultured bacteria; 32.7% and 31.6% of patients, respectively, had these pathogens isolated by culture. S. aureus was found on culture for 10.1% of patients, and 8.8% of patients had cultures positive for M. catarrhalis.

Table 4
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Table 4

Weighted mean culture rates in reviewed studies on a per-isolate and per-patient basis.

Of the 25 included articles, 15 articles excluded patients who had received antibiotic therapy before their respective study periods. Of the remaining 9 articles, 1 specifically mentioned that prior antibiotic therapy did not exclude enrollment [17], and 8 did not specifically mention this factor [9, 12, 14, 16, 19,20–21, 27]. The weighted rates for the articles that specifically excluded patients who had received prior antibiotic therapy were also calculated and found to not be significantly different from rates calculated including all articles. On a per-isolate basis, the weighted rates for articles excluding patients who had received prior antibiotic therapy were 28.4%, 26.4%, 7.2%, and 8.7% for S. pneumoniae, H. influenzae, M. catarrhalis, and S. aureus, respectively. On a per-patient basis, the rates were 32.0%, 32.1%, 7.8%, and 9.0%, respectively. Therefore, possible inclusion of patients who had previously received antibiotic therapy did not play a significant role in redistributing bacterial culture rates.

Analyses were also performed to determine whether culture rates were affected by the method of culture performed (table 5). The culture rates on a per-isolate basis for all bacteria except M. catarrhalis were not found to significantly differ between studies using only maxillary sinus taps and those that used middle meatal cultures. M. catarrhalis was isolated more frequently in studies using middle meatal swabs than in those using maxillary sinus taps (11.1% vs. 6.3%; P = .05). On a per-patient basis (data not shown), there was no statistically significant difference between the tests for any bacterium (P > .22, by Wilcoxon rank sum).

Table 5
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Table 5

Weighted mean culture rates per total isolates according to the culture technique used in the studies.

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Discussion

Recommendations for antibiotic therapy for ABRS are periodically reviewed and updated by the Sinus and Allergy Health Partnership and the American Academy of Otolaryngology–Head and Neck Surgery [2]. These recommendations use a mathematical algorithm [32] based on expected bacterial prevalence, spontaneous resolution rates, and susceptibility to various antibiotics. Primarily based on the traditionally stated major ABRS pathogens S. pneumoniae, H. influenzae, and M. catarrhalis, these recommendations relegate S. aureus to the minor or other pathogen category, because the prevalence of S. aureus has been thought to be lower than that of other pathogens, owing, in part, to concerns over the pathogen being a contaminant. Recent literature, however, has indicated an increasing prevalence of S. aureus in sinus cultures, with rates comparable to those in this study [4, 33].

This information becomes increasingly important in light of the increasing number of isolates of community-acquired MRSA. Approximately 2 million people in the United States are thought to be colonized with MRSA [34]. Naimi et al. [35] found that 25% of all isolates of S. aureus were MRSA, with 12% of these isolates being community acquired. Of the community-acquired isolates, 6% were determined by respiratory culture. Another study publishing the results of the SENTRY antibacterial-resistance surveillance project also noted that the rate of MRSA carriage has been increasing in the community; in 1999, MRSA accounted for 25%–30% of isolates. In a review of a series of patients with ABRS by Huang et al. [33], the authors found that 9.3% of patients had cultures that were positive for S. aureus and that 38.7% of these patients were colonized with a MRSA strain.

Studies researching the drug-resistance patterns of S. aureus have luckily found that the mechanisms of community-acquired strains are different from those of strains that are health care related [36]. As a result, community-acquired strains are often only resistant to β-lactam antibiotics and are most often susceptible to tetracyclines, clindamycin, and trimethoprim-sulfamethoxazole [35]. However, these are not the recommended first-line therapies, because these medications are not as effective against S. pneumoniae and H. influenzae infections. Furthermore, these therapies are based on an algorithm that underplays the prevalence of S. aureus, a bacterium for which the spontaneous resolution rate is not as well documented as it is for other pathogens in ABRS.

In this study, we show that 10.1% of patients have cultures positive for S. aureus and that 9.7% of all cultured isolates are S. aureus; these percentages are greater than those for M. catarrhalis, although the difference is not statistically significant. These findings are not a result of non–gold standard culture techniques, as demonstrated by a comparison between studies using 2 highly concordant techniques. The concerns related to S. aureus cultures being contaminants seem to be unfounded according to the present data. Maxillary sinus tap results would be expected to be evidence of accurate culture results, and given the data supporting the equivalence between middle meatal cultures and maxillary sinus taps [3, 4], this would suggest that the rates are accurate. Of interest is that the rate of maxillary sinus taps yielding M. cararrhalis is lower than the rate of middle meatal cultures yielding M. cararrhalis.

This study, like any meta-analysis, is limited by its attempt to pool potentially heterogeneous data. Although no formal test of heterogeneity was performed, the included articles resulted from a very narrowly restricted set of criteria, and potential confounders, such as culture technique, were accounted for in the analysis. Culture rates were not shown to significantly vary between the 2 culture techniques. Another concern is the potential variability among the studies with regard to the determination of a positive culture result. The majority of articles did not publish the specific lower limit value for their colony count criteria, but those that did typically used more-stringent criteria for S. aureus because of the concern over the pathogen being a potential contaminant. As a result, data derived from these studies may actually underrepresent the true prevalence of this bacterium in ABRS.

In conclusion, the data suggest that S. aureus should be included as a major pathogen in ABRS, in addition to the accepted pathogens of S. pneumoniae, H. influenzae, and M. catarrhalis. Because of the high spontaneous resolution rate of M. catarrhalis infection and the increasing presence of community-acquired MRSA, treatment of S. aureus infection in patients with ABRS may become difficult if current trends continue.

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Acknowledgments

We thank Dr. Stedman Scott Sankey for providing the statistical analysis for this project.

Potential conflicts of interest. M.S.B. has recently received research funding for Naryx; has been a consultant for Bayer, Ortho-McNeil, Abbott, and Sanofi-Aventis; and has served on the speakers' bureau for Abbott. S.C.P.: no conflicts.

  • Received April 10, 2007.
  • Accepted July 25, 2007.
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  1. Clin Infect Dis. (2007) 45 (10): e121-e127. doi: 10.1086/522763
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