Original Contributions

What Is the Bacteriology in Adults?

Hassan H. Ramadan, MD, FACS
Purpose: Recent advances in imaging and endoscopy has increased our awareness of chronic sinusitis. The teaching. has been that chronic sinusitis is mainly caused by anaerobes; however, recent studies have found that the role of anaerobes is small, especially in children. Materials and Methods: A prospective study was conducted on 76 adults who failed medical treatment for chronic sinusitis and were scheduled for endoscopic sinus surgery. Specimens were obtained on all 76 patients at the time of surgery and were sent for aerobic and anaerobic cultures. Results: Anaerobic organisms were isolated in 7.6% of the cases, and aerobes were isolated in 76.3% of the patients. The most common aerobic organism was the Staphylococcus species, whereby resistance to the most commonly used antibiotics was 21.7%. Conclusion: All past studies on the bacteriology in adults were made before the era of endoscopic sinus surgery and the newer-generation antibiotics. According to our results, it seems there is a change in trend in the bacteriology of chronic sinusitis in adults. Copyright 0 1995 by W.B. Saunders Company

of Chronic

Sinusitis

Endoscopic sinus surgery (ESS) has challenged our understanding of sinus disease. The improved ability to diagnose and anatomically define sinus disease, provided by nasal endoscopes and computed tomography, has revolutionized the treatment of chronic sinusitis. The mainstay of treatment of chronic sinusitis continues to be medical treatment, including antibiotics, topical and systemic decongestants, and control of allergies. Patients who have failed maximum medical therapy become candidates for ESS. To provide the best medical therapy, knowledge of the bacteriology of chronic sinusitis is extremely important. Despite numerous publications in the
From the Department of Otolaryngology-Head and Neck Surgery, West Virginia University, Morgantown. Presented at American Rhinologic Society, West Palm Beach, FL, May 7-9, 1994. Address reprint requests to Hassan H. Ramadan, MD, Department of Otolaryngology-Head and Neck Surgery, West Virginia University, 2222 Robert C. Byrd Health Sciences South, PO Box 9200, Morgantown, WV 265069200. Copyright 0 1995 by W.B. Saunders Company 0196-0709/95/l 605-0003$5.00/O American Journal of Otolaryngology,

literature, the bacteriology of chronic sinusitis remains uncertain. Reports published between the early 1940s and the late 1960s do not address the role of anaerobes. In 1974, Frederick and Braude published their report on patients with chronic sinusitis who had a Caldwell-Luc or an external ethmoidectomy procedure performed. Fifty-two percent of their cultures grew anaerobes. Articles in the 1970s and 1980s stressed the importance of anaerobes in chronic sinusitis.-5 Recently a number of reports have been published, pertaining mainly to children, that have shown either a minimal or no role for anaerobes in patients with chronic sinusitis.6-g Of importance is the fact that recent studies examined tissue from the ethmoid sinuses that was obtained during ESS instead of from the maxillary sinuses during Caldwell-Luc or antral punctures. It seemed to us that since the introduction of ESS, the bacteriology of chronic sinusitis is different, especially in children. Two recent reports of adults with chronic sinusitis that examined tissue obtained from the ethmoid sinuses demonstrated no anaerobic
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growth.. We decided to prospectively evaluate the bacteriology of our adult patient population with chronic sinusitis that were undergoing ESS. MATERIALS AND METHODS

TABLE 1. Bacterial Chronic Sinusitis Organisms

Isolates

in 76 Patients

With

No.

Cultured 46 12 4 3 3 2 3 2

A prospective study was conducted at West Virginia University between June 1992 and June 1993. Patients with chronic sinusitis who failed maximal medical therapy and were scheduled for ESS were enrolled. Maximal medical therapy consisted of at least 12 weeks of antibiotics as well as nasal steroids, nasal decongestants, and mucolytics. These patients had symptoms of nasal obstruction and stuffiness, rhinorrhea, postnasal drainage, and facial pains and had been undergoing medical treatment for at least 6 months. Patients with immunodeficiency and cystic fibrosis were excluded from this study. A total of 76 patients with an age range of 24 to 72 years and a mean of 42.7 years form the cohort of this study. There were 46 women and 30 men. All patients were evaluated with a coronal CT scan of their paranasal sinuses at the end of at least 4 weeks of antibiotics. Based on hisiory, physical examination, and CT findings, these patients were advised to undergo endoscopic sinus surgery. None of the patients in this study had been on antibiotic therapy within at least 1 week of their procedure. Patients who needed to be on antibiotic therapy were excluded. At the time of surgery, the face and nose were scrubbed with iodine, and then the endoscopic procedure as described by Kennedy et al was performed. After removal of the uncinate process, the bulla ethmoidalis was entered. Tissue from the anterior ethmoid air cells was placed in a culture tube and sent to the laboratory for aerobic and anaerobic cultures. The anaerobic culture technique described by Lennette et all3 was used. RESULTS A total of 76 specimens were obtained. Fifty-eight patients (76.3%) had growth of one or more organism, while 18 (23.7%) did not show any growth. Forty (69%) of the culturepositive patients had growth of a single organism, while 18 (31%) had 2 or more organisms. Forty-six (79.9%) grew Staphylococcus species coagulase-negative organisms, and 12 specimens (20.7%) grew Staphylococcus aureus. Twelve specimens grew miscellaneous organisms (Table 1) with low titers. Ten of the Staphylococcus coagulase-negative group (21.7%) were resistant to the most commonly used antibiotics and were only sensitive to vancomycin. Five strains were resistant

Aerobes Coagulase-negative Staphylococcus S aureus Pseudomonas species Haemophilus influenzae Streptococcus pneumoniae Diphteroid species Anaerobes Propionibacterium acnes Peptostreptococcus species Peptococcus species

to all except ciprofluxacin, sulfa drugs, and vancomycin. Six patients (7.9%) grew anaerobes. All patients who grew anaerobes also grew one or more aerobic organism. DISCUSSION The literature is rich with studies on the bacteriology of chronic sinusitis. It seems that studies that were done before the popularization of ESS have stressed the importance of anaerobes. Most of these studies obtained their specimens while doing a Caldwell-Luc procedure. In 1974, Frederick and Braude obtained tissue and pus from the maxillary sinuses of 83 patients undergoing a lynch or Caldwell-Luc procedure. They defined their patients as those who had a history of chronic purulent nasal discharge for more than a year. Purulence was present in all cases at surgery. There was no mention of the medical treatment that these patients had received before undergoing surgery. Also there was no mention of whether they had any radiologic evaluation. The diagnosis of chronic sinusitis was made upon evaluation of the mucous membrane. Whether that was based on clinical observation or pathological examination is not clear. The most common aerobic organisms were S aureus and Staphylococcus viridans, and anaerobes were recovered in 52% of their patients. Karma et al2 in 1979 studied 40 consecutive patients in whom symptoms of chronic sinusitis were diagnosed for at least 3 months. These patients had usually been treated by repeated antral punctures

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and no mention was made about radiographic evaluation. Cultures were obtained from secretions collected during a CaldwellLuc procedure. Anaerobes were cultured in 18% of the specimens. Su et al3 in 1983 obtained secretions during a Caldwell-Luc operation from 48 patients who were diagnosed with chronic sinusitis, based on history. No mention was made on how the patients were treated before undergoing surgery. Anaerobes were recovered in 40% of the cases. In 1988, Maisel and Kimberley4 recovered anaerobes in 25% of 50 patients undergoing a CaldwellLuc procedure for chronic sinusitis; the most common aerobic organism was S aureus. Brook in 1989 obtained secretions from 72 patients who were having a Caldwell-Luc procedure for sinusitis of at least 3 weeks duration. Anaerobes were recovered in 88% of the cases. The most common aerobic bacteria was a-hemolytic streptococcus. S aureus was detected in 17% of the specimens. Recent studies in children in which the specimens were obtained from the ethmoid sinuses during ESS have shown that anaerobes play a minimal role in chronic sinusitis. In 1989, Tinkelman and Silk found no anaerobes in the specimens obtained during ESS in 35 children. The triad of aerobic organisms H influenzae, S pneumoniae, and Branhamella catarrhalis were most commonly identified. In 1991, Muntz and Lusk7 obtained mucosa from the ethmoid sinuses during ESS. They demonstrated anaerobes in 6% of the patients with a 19% incidence of S aureus. In 1991, Orobello et al8 obtained specimens on children undergoing ESS; anaerobes were isolated in 4% and S aureus in 13% of the cases. In 1993, Sturdivant and Cannon9 obtained specimens through direct sinus aspirations from the maxillary sinus through the natural ostia on 25 children with chronic sinusitis. Anaerobes were recovered in 4% and S aureus in 24% of the specimens. In 1991, Doyle and Woodham in a study of 59 adults with chronic sinusitis obtained mucosal specimens from the anterior ethmoid air cells. They found no anaerobes in their patients. The most common aerobic organism was S aureus, which was cultured in 32% of the specimens. In 1992, Hoyt found no anaerobes and a 23% incidence of S aureus in

specimens collected from the ethmoid sinuses in 197 adults during ESS. In our study, 58 (76.3%) of the patients were culture-positive, and aerobes were detected in all 58 patients. Polymicrobial infections were present in 31% of the patients. In only 6 (7.9%) of 76 patients were anaerobes isolated. The predominant aerobic bacteria were coagulase-negative Staphylococcus in 46 (79.3%) specimens and S aureus in 12 (20.7%) specimens. In recent studies, coagulase-negative Staphylococcus organisms have been commonly cultured in both children and adults. Muntz and Lusk7 had a 44% incidence in their specimens. Orobello et al in 1991 had a 24% growth in their series. In 1991, Doyle and Woodham in a study of 59 adults had a 71% incidence. The question is whether Staphylococcus epidermidis should be looked at as a contaminant or as a pathogen. Several reports in the literature have suggested that it should be dealt with as a pathogen especially since in some individuals, it is the only organism recovered.4.15 In our series, this happened in 33 patients (43%). It was resistant to the most commonly used antibiotics in 10 (21.7%) patients, whereby it was sensitive only to vancomycin. S aureus has been the most common aerobic organism isolated in both recent and previous studies, whether specimens were obtained from the ethmoid or the maxillary sinuses. The results of our study concur with recent studies that anaerobes do not play a significant role in chronic sinusitis. It also seems that Staphylococcus species are the major aerobic organisms encountered. It remains to be seen whether the low rate of anaerobes in those studies where specimens were obtained from the ethmoid sinus is due to the fact that ethmoid sinuses are not blocked, compared to specimens obtained from obstructed maxillary sinuses, even though Orobello et al have shown that cultures obtained from the ethmoid and maxillary specimens were comparable. We do not think that error in technique is the cause of the low anaerobic growth because numerous studies from different centers have shown similar results. In the last decade, our understanding of chronic sinusitis has changed dramatically. Messerklingersl work defined the patho-

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physiology of chronic sinusitis differently than had been understood previously. Nasal endoscopy, CT scans, and newer-generation antibiotics have revolutionized the treatment of chronic sinusitis. Studies performed before the era of ESS are not comparable with those obtained in the ESS era. We now stress the importance of antibiotics in the treatment of chronic sinusitis. This may have not been the case in the past. Karma et al2 in 1979 treated the majority of the patients by antral punctures and washings. The duration of treatment with the antibiotics is different. We now treat for at least 2 weeks and in some cases up to 6 weeks. CONCLUSION After reviewing the recent data on the bacteriology of chronic sinusitis, we conclude that there seems to be a minimal role for anaerobes. The teaching that anaerobes are the most common organisms seems to be no longer true. Staphylococcus species are the most common organisms encountered in patients for whom medical therapy failed and who underwent surgery. These findings raise several questions that we need to address in order to arrive at a better understanding of the bacteriology of chronic sinusitis: (1.) Has the definition of chronic sinusitis changed since the advent of nasal endoscopy and CT scan? (2.) Are the new generations of antibiotics the cause of the change in bacteriology? (3.) Did CT scans change our surgical indications so that we are now dealing with a highly select group that is not responsive to medical therapy? ACKNOWLEDGMENT
The author tance in the thanks Kimberly Reveal for preparation of the manuscript. her assis-

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