Discrepancies in the recovery of bacteria from multiple sinuses in acute and chronic sinusitis

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1 Journal of Medical Microbiology (2004), 53, DOI /jmm Short Communication Correspondence Itzhak Brook Received 1 March 2004 Accepted 18 May 2004 Discrepancies in the recovery of bacteria from multiple in acute and chronic sinusitis Itzhak Brook Department of Pediatrics, Georgetown University School of Medicine, 4431 Albemarle St NW, Washington DC 20016, USA The microbiology of acute and chronic sinusitis has been studied extensively. Establishing the concomitant distribution of the causative organisms in cases that involve multiple is of scientific and practical importance. This study evaluated the aerobic and anaerobic microbiology of acute and chronic sinusitis in patients with involvement of multiple. The 155 patients evaluated had sinusitis of either the maxillary, ethmoid or frontal (any combination) and had organisms recovered from two to four concomitantly infected. Similar aerobic, facultatively anaerobic and anaerobic organisms were recovered from all groups of patients. In patients who had organisms isolated from two and had acute sinusitis, 31 (56 %) of the 55 were found only in a single sinus, and 24 (44 %) were recovered concomitantly from two. In those with chronic infection 31 (34 %) of the 91 were recovered only from a single sinus, and 60 (66 %) were found concomitantly from two. bacteria were more often isolated concomitantly from two (50 of 70) than aerobic and facultatively anaerobic (ten of 21, P, 0. 05). Similar findings were observed in patients who had organisms isolated from three or four. â-lactamase-producing bacteria were more often isolated from patients with chronic infection (58 83 %) as compared to those with acute infections (32 43 %). These findings illustrate that there are differences in the distribution of organisms in single patients who suffer from infections in multiple and emphasize the importance of obtaining cultures from all infected. Introduction The microbiology of acute and chronic sinusitis is well established; where the major pathogens causing acute infection are aerobic and facultatively anaerobic bacteria (e.g. Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis) (Jousimies-Somer et al., 1988), and the bacterial aetiology of chronic sinusitis is anaerobic bacteria (Brook, 1981; Nord, 1995). Many patients with these infections suffer from infections in more than. However, most studies that investigated the microbiology of sinusitis reported the number of bacteria isolated in a single sinus cavity and ignored the bacteriological findings in other concomitantly infected. Establishing the distribution of organisms in cases that involve multiple is of scientific and practical importance, as it can shed light on the reliability of obtaining culture from only a single sinus cavity when more than one is infected. This report describes the author s experience over a 26-year period of studying the aerobic and anaerobic microbiology of acute and chronic maxillary, ethmoid and frontal sinus in patients with involvement of multiple. Abbreviation: BLPB, â-lactamase producing bacteria. Patients and Methods The 155 patients included in the report were studied between June 1977 and June All had sinusitis of either the maxillary, ethmoid or frontal sinusitis (any combination). The combinations cultured were of right or left sides of either of the involved. They included 42 patients with acute sinusitis and 38 with chronic sinusitis who had organisms recovered from two, 22 with acute sinusitis and 24 with chronic sinusitis who had organisms recovered from three, and 14 with acute sinusitis and 15 with chronic sinusitis who had organisms recovered from four. Excluded were 37 additional patients whose showed no bacterial growth. The patients were seen in suburban Washington DC and Maryland. Patients ages ranged from 11 to 75 years (mean 49.5 years), 86 were males and 11 were children (younger than 18 years old). No differences in gender and age were noted between the patient groups. Antimicrobial therapy was administered to 76 patients (49 %) in the month prior to sample collection, 58 with chronic and 26 with acute infection. Only cases fulfilling the following criteria were included in the evaluation: typical clinical symptoms of sinusitis (headache, fever, nasal drainage, etc.), positive radiographic findings, positive sinus bacterial cultures. Sinusitis was considered acute if symptoms resolved within 30 days, and chronic if symptoms persisted for more than 3 months. The specimens were obtained using inferior meatal antrostomy after disinfection of the oral mucosa with Bethadine, or during surgery, and were transported to the laboratory in a syringe sealed with a rubber & 2004 SGM Printed in Great Britain IP:

2 I. Brook stopper after evacuation of air or in an anaerobic transport tube (Port- A-Cul; Baltimore Biological Laboratories, Cockeysville, MD). The time between the collection of materials and inoculation of the specimen was generally less than 30 min for syringes and less than 3 h for the transport tube. Specimens were inoculated onto 5 % sheep s blood, chocolate agar, and MacConkey agar plates for aerobic and facultatively anaerobic organisms. The plates were incubated at 37 8C aerobically (MacConkey) or under 5 % carbon dioxide (5 % sheep s blood and chocolate) and examined at 24 and 48 h. For anaerobes the material was plated onto pre-reduced vitamin-k 1 -enriched Brucella blood agar, an anaerobic blood agar plate containing kanamycin and vancomycin, an anaerobic blood plate containing colistin and nalidixic acid and an enriched thioglycolate broth (containing haemin and vitamin K 1 ) (Summanen et al., 1993). The anaerobic plates were incubated in anaerobic jars (GasPak jars; Baltimore Biological Laboratories) and examined at 48 and 96 h. Isolates with different morphology were recovered from the original plates and subsequently identified. Anaerobes were identified by techniques described previously. (Summanen et al., 1993). bacteria were identified by conventional methods (Murray et al., 1999). â-lactamase activity was determined in each isolate by use of the chromogenic cephalosporin analogue 87/312 method (O Callaghan et al., 1972). Statistical analysis was performed using Chi-squared and Student s t-tests. Results Similar aerobic, facultatively anaerobic and anaerobic organisms were recovered from all of the groups of patients. No differences were of note in the recovery of the organisms from the different. The aerobic and facultatively anaerobic found in acute sinusitis were Streptococcus pneumoniae, H. influenzae, M. catarrhalis, Staphylococcus aureus and Streptococcus pyogenes. The anaerobic bacteria were Peptostreptococcus spp., Fusobacterium spp., Prevotella spp. and Propionibacterium acnes. The aerobic and facultatively anaerobic recovered in chronic sinusitis were Streptococcus pneumoniae, H. influenzae, M. catarrhalis, Staphylococcus aureus, Streptococcus pyogenes, Klebsiella pneumoniae, Escherichia coli, Proteus mirabilis and Pseudomonas aeruginosa. The anaerobic bacteria were Peptostreptococcus spp., Fusobacterium spp., anaerobic Gram-negative bacilli (including pigmented Prevotella and Porphyromonas spp.) and Propionibacterium acnes. There was no change in the prevalence of â-lactamase producing bacteria (BLPB) as the study proceeded over the period of 26 years. Comparisons of 80 patients with sinusitis who had organisms recovered from two Acute sinusitis (Table 1). A total of 55 were recovered from the 42 cases (1. 3/case), 45 aerobic and facultatively anaerobic (1. 1/case) and ten anaerobic (0. 2/ case). The number of per specimen varied from one to three. and facultatively anaerobic organisms alone were recovered in 36 patients (86 %), anaerobes only in two (5 %) and mixed aerobic and anaerobic bacteria in four (9 %). Seventeen BLPB were recovered from 15 (36 %) individuals. Thirty-one (56 %) of the 55 were found only in a single sinus, and 24 (44 %) were recovered concomitantly from two. Chronic sinusitis (Table 2). A total of 91 were obtained from the 38 cases (2. 4/case), 21 aerobic and facultatively anaerobic (0. 6/case) and 70 anaerobic (1. 8/ case). The number of per specimen varied from one to five. and facultatively anaerobic organisms Table 1. Isolates from 42 patients with acute sinusitis who had organisms recovered from two Streptococcus pneumoniae H. influenzae 12 (5) 7 (3) 5 (2) M. catarrhalis 6 (6) 4 (4) 2 (2) Staphylococcus aureus 4 (3) 2 (2) 2 (1) Streptococcus pyogenes Subtotal: 45 (14) 26 (9) 19 (5) Peptostreptococcus species Prevotella intermedia 3 (2) 1 (1) 2 (1) Fusobacterium nucleatum 1 (1) 1 (1) 0 Propionibacterium acnes Subtotal: 10 (3) 5 (2) 5 (1) Total 55 (17) 31 (11) 24 (6) 880 IP: Journal of Medical Microbiology 53

3 Discrepancies in bacteriology in multiple Table 2. Isolates from 38 patients with chronic sinusitis who had organisms recovered from two Streptococcus pneumoniae H. influenzae 2 (1) 1 1 (1) Staphylococcus aureus 5 (5) 2 (2) 3 (3) Streptococcus pyogenes K. pneumoniae E. coli Proteus mirabilis Pseudomonas aeruginosa 4 (3) 2 (2) 2 (1) Subtotal: 21 (9) 11 (4) 10 (5) Peptostreptococcus species Prevotella melaninogenica 6 (3) 2 (1) 4 (2) Prevotella intermedia 12 (8) 2 (2) 10 (6) Prevotella oralis 6 (1) 1 5 (1) Porphyromonas asaccharolytica 5 (3) 1 (1) 4 (2) Bacteroides species F. nucleatum 8 (5) 2 (1) 6 (4) Fusobacterium species 4 (2) 2 (1) 2 (1) Propionibacterium acnes Subtotal: 70 (22) 20 (6) 50 (16) Total 91 (31) 31 (10) 60 (21) alone were recovered in three patients (8 %), anaerobes only in 19 (50 %) and mixed aerobic and anaerobic bacteria in 16 (42 %). Thirty-one BLPB were recovered from 22 (58 %) individuals. Twelve (40 %) of the 30 were recovered only from a single sinus, 11 (37 %) were concomitantly present in two, and seven (23 %) were recovered from three. bacteria were never isolated from three. Thirty-one (34 %) of the 91 were recovered only from a single sinus, and 60 (66 %) were present concomitantly in two. bacteria were more often isolated concomitantly from two (50 of 70) than aerobic and facultatively anaerobic (ten of 21, P, 0. 05). Proteus mirabilis and Propionibacterium acnes were only isolated from a single sinus. Comparisons of 46 patients with sinusitis who had organisms recovered from three Acute sinusitis (Table 3). A total of 30 were recovered from the 22 cases (1. 4/case), 25 aerobic and facultatively anaerobic (1. 2/case) and 5 anaerobic (0. 2/case). The number of per specimen varied from one to three. and facultatively anaerobic organisms alone were recovered from 18 patients (82 %), anaerobes only in one (5 %), and mixed aerobic and anaerobic bacteria in three (13 %). Eight BLPB were recovered from seven (32 %) individuals. Chronic sinusitis (Table 4). A total of 67 were recovered from the 24 cases (2. 8/case), 17 aerobic and facultatively anaerobic (0. 7/case) and 50 anaerobic (2. 1/ case). The number of per specimen varied from one to five. and facultatively anaerobic organisms alone were recovered in one patient (4 %), anaerobes only in 13 (54 %), and mixed aerobic and anaerobic bacteria in ten (42 %). Twenty-seven BLPB were recovered from 20 (83 %) individuals. Seventeen (25 %) of the 67 were recovered only from a single sinus, 32 (48 %) were concomitantly present in two, and 18 (27 %) were recovered from three. There were no differences in the recovery rate between aerobic and facultatively anaerobic and anaerobic bacteria in single or multiple. However, Streptococcus pneumoniae, Proteus mirabilis and Propionibacterium acnes were only isolated from a single sinus. IP:

4 I. Brook Table 3. Isolates from 22 patients with acute sinusitis who had organisms recovered from three Streptococcus pneumoniae H. influenzae 8 (3) 3 3 (2) 2 (1) M. catarrhalis 3 (3) 2 (2) 1 (1) 0 Staphylococcus aureus 2 (1) 0 1 (1) 1 Streptococcus pyogenes Subtotal: 25 (7) 9 (2) 9 (4) 7 (1) Peptostreptococcus species Prevotella melaninogenica 1 (1) 1 (1) 0 0 Prevotella intermedia F. nucleatum Subtotal: 5 (1) 3 (1) 2 0 Total 30 (8) 12 (3) 11 (4) 7 (1) Table 4. Isolates from 24 patients with chronic sinusitis who had organisms recovered from three Streptococcus pneumoniae H. influenzae 2 (2) 2 (2) 0 0 M. catarrhalis 2 (2) 1 (1) 1 (1) 0 Staphylococcus aureus 1 (1) 0 1 (1) 0 Streptococcus pyogenes K. pneumoniae 2 (1) 0 1 (1) 1 E. coli Proteus mirabilis Pseudomonas aeruginosa 4 (2) 1 2 (1) 1 (1) Subtotal: 17 (8) 7 (3) 7 (4) 3 (1) Peptostreptococcus species Prevotella melaninogenica 3 (2) 0 2 (1) 1 (1) Prevotella intermedia 8 (5) 2 3 (3) 3 (2) Prevotella oralis 3 (1) (1) Porphyromonas asaccharolytica 4 (3) 0 2 (2) 2 (1) Bacteroides species 3 (1) 1 2 (1) 0 F. nucleatum 7 (5) 1 (1) 4 (3) 2 (1) Fusobacterium species 3 (2) 0 2 (1) 1 (1) Propionibacterium acnes Subtotal: 50 (19) 10 (1) 25 (11) 15 (7) Total 67 (27) 17 (4) 32 (15) 18 (8) 882 IP: Journal of Medical Microbiology 53

5 Discrepancies in bacteriology in multiple Comparisons of 29 patients with sinusitis who had organisms recovered from four Acute sinusitis (Table 5). A total of 26 were recovered from the 14 cases (1. 9/case), 21 aerobic and facultatively anaerobic (1. 5/case) and five anaerobic (0. 4/ case). The number of per specimen varied from one to three. and facultatively anaerobic organisms alone were recovered from 11 patients (79 %), and mixed aerobic and anaerobic bacteria in three (21 %). Nine BLPB were recovered from six (43 %) individuals. Seven (27 %) of the 26 were recovered only from a single sinus, eight (31 %) were concomitantly present in two, eight (31 %) were recovered from three, and three (11 %) were isolated in four. bacteria were never isolated from four. Chronic sinusitis (Table 6). A total of 53 were recovered from the 15 cases (3. 5/case), 14 aerobic and facultatively anaerobic (0. 9/case) and 39 anaerobic (2. 6/ case). The number of per specimen varied from one to five. and facultatively anaerobic organisms alone were recovered in two patients (13 %), anaerobes only in eight (53 %), and mixed aerobic and anaerobic bacteria in five (33 %). Eighteen BLPB were recovered from 12 (80 %) individuals. Ten (19 %) of the 67 were recovered only from a single sinus, 17 (32 %) were concomitantly present in two, 17 (32 %) were recovered from three, and nine (17 %) were found in four. There were no differences in the recovery rate between aerobic and facultatively anaerobic and anaerobic bacteria in single or multiple. However, no aerobic or facultatively anaerobic bacteria were present in all four and Propionibacterium acnes was not recovered from three or four. Discussion This study confirms the importance of aerobic and facultatively anaerobic bacteria Streptococcus pneumoniae, H. influenzae and M. catarrhalis in acute sinusitis (Jousimies- Somer et al., 1988) and the predominance of anaerobic bacteria in chronic infection. (Brook, 1981; Nord, 1995) This study describes, for the first time, the discrepancies in recovery of bacteria in concomitantly infected in individuals with acute and chronic sinusitis. A similar discrepancy in the recovery of organisms between the left and right ears in bilateral otitis media has been described previously (Brook & Yocum, 1995). These findings illustrate that there are differences in the distribution of organisms in patients who suffer from infections in multiple. The data suggest that when cultures are obtained to assist in the selection of antimicrobial therapy, when possible they should be obtained from all of the involved. Since % of the we recovered were present only in a single sinus, a large proportion of the would have been missed if only a single sinus were studied. Obtaining cultures from all infected is especially important in acute sinusitis as the aerobic and facultatively anaerobic bacteria recovered in this infection were more often found in a single sinus. This was more important than in chronic sinusitis because the anaerobic bacteria found in this type of infection were more often recovered from multiple. The lack of recovery of any organisms from 37 additional patients is consistent with the experience of other investiga- Table 5. Isolates from 14 patients with acute sinusitis who had organisms recovered from four Present in four Streptococcus pneumoniae H. influenzae 6 (2) (1) 1 (1) M. catarrhalis 4 (4) 2 (2) 2 (2) 0 0 Staphylococcus aureus 3 (2) (1) 1 (1) Streptococcus pyogenes Subtotal: 21 (8) 5 (2) 7 (2) 6 (2) 3 (2) Peptostreptococcus species Prevotella intermedia 1 (1) F. nucleatum Fusobacterium species Subtotal: 5 (1) Total 26 (9) 7 (2) 8 (2) 8 (2) 3 (2) IP:

6 I. Brook Table 6. Isolates from 15 patients with chronic sinusitis who had organisms recovered from four Number of BLPB bacteria is shown in parentheses. Present in four Streptococcus pneumoniae H. influenzae 2 (2) 1 (1) 1 (1) 0 0 Staphylococcus aureus 4 (4) 0 2 (2) 2 (2) 0 Streptococcus pyogenes K. pneumoniae E. coli Proteus mirabilis Pseudomonas aeruginosa 2 (1) (1) 0 Subtotal: 14 (7) 2 (1) 8 (3) 4 (3) 0 Peptostreptococcus species Prevotella melaninogenica 4 (2) (2) Prevotella intermedia 6 (4) 1 1 (1) 2 (2) 2 (1) Prevotella oralis 2 (1) (1) 0 Porphyromonas asaccharolytica 3 (1) (1) 1 Bacteroides species F. nucleatum 4 (3) 0 1 (1) 2 (1) 1 (1) Fusobacterium species Propionibacterium acnes Subtotal: 39 (11) 8 9 (2) 13 (5) 9 (4) Total 53 (18) 10 (1) 17 (5) 17 (8) 9 (4) tors. This may be due to various reasons such as the effects of previous antimicrobial therapy, and inappropriate collection and/or transportation of specimens (Nord, 1995). Resistance to antimicrobials through the production of â- lactamase was observed in this study more often in that were recovered from patients with chronic infection. BLPB were more often isolated from patients with chronic infection (58 83 %) as compared to those with acute infection (32 43 %). The recovery of BLPB is not surprising, since about half of our patients had received antimicrobial agents including â-lactams within the past month, which might have selected for these organisms. A growing number of aerobic and anaerobic organisms isolated from patients with acute and chronic bacterial sinusitis produce â-lactamases (Brook et al., 1996). â-lactamase activity was seen in 86 % of sinus aspirates that contained â-lactamase producing organisms. It has been suggested that the â-lactamase present in sinus fluid may protect other non-blpb (Brook, 1984). The treatment of bacterial sinusitis has become more difficult in the last decade because of the increased antimicrobial resistance of the major pathogens recovered in acute and chronic infection. The growing resistance of Streptococcus pneumoniae to penicillin and other antimicrobials such as trimethoprim-sulfamethoxazole and macrolides (Ednie et al., 1997) and the production of â-lactamase by H. influenzae, M. catarrhalis (Brook & Gober, 1984), pigmented Prevotella, Porphyromonas spp. and Fusobacterium spp. (Wexler & Finegold, 1998) are the major causes of resistance. Selection of antimicrobial agents for the therapy of bacterial sinusitis can be improved by obtaining cultures from all the involved sinus(es), by knowledge of the resistance pattern of the organisms in the community, and by consideration of the effect of previous antimicrobial therapy (Jacobs, 2003) or prophylaxis (Brook & Gober, 1996) that may select resistant strains. Further studies of the microbiology and effect of antimicrobial therapy of acute and chronic sinusitis are warranted. These studies should investigate whether the use of antimicrobials effective against all the potential pathogens, including the resistant organisms, will be able to enhance resolution of the infection in these patients. The use of molecular approaches in future studies may reveal a greater number of species and a more diverse flora in infected (Paju et al., 2003). References Brook, I. (1981). Bacteriological features of chronic sinusitis in children. JAMA 246, Brook, I. (1984). The role of â-lactamase-producing bacteria in the persistence of streptococcal tonsillar infection. Rev Infect Dis 6, Brook, I. & Gober, A. E. (1984). Emergence of â-lactamase-producing aerobic and anaerobic bacteria in the oropharynx of children following penicillin chemotherapy. Clin Pediatr (Phila) 23, IP: Journal of Medical Microbiology 53

7 Discrepancies in bacteriology in multiple Brook, I. & Yocum, P. (1995). Bacteriology and â-lactamase activity in ear aspirates of acute otitis media that failed amoxicillin therapy. Pediatr Infect Dis J 14, Brook, I. & Gober, A. E. (1996). Prophylaxis with amoxicillin or sulfisoxazole for otitis media: effect on the recovery of penicillinresistant bacteria from children. Clin Infect Dis 22, Brook, I. Yocum, P. & Frazier, E. H. (1996). Bacteriology and â- lactamase activity in acute and chronic maxillary sinusitis. Arch Otolaryngol Head Neck Surg 122, Ednie, L. M., Spangler, S. K., Jacobs, M. R. & Appelbaum, P. C. (1997). Susceptibilities of 228 penicillin- and erythromycin-susceptible and -resistant pneumonococci to RU 64004, a new ketolide, compared with susceptibilities to 16 other agents. Antimicrob Agents Chemother 41, Jacobs, M. R. (2003). Worldwide trends in antimicrobial resistance among common respiratory tract pathogens in children. Pediatr Infect Dis J 22 (8 Suppl.), S109 S119. Jousimies-Somer, H. R., Savolainen, S. & Ylikoski J. S. (1988). Bacteriological findings of acute maxillary sinusitis in young adults. J Clin Microbiol 26, Murray, P. R., Baron, E. J., Pfaller, M. A., Tenover, P. C. & Yolken, R. H. (1999). Manual of Clinical Microbiology, 7th edn. Washington, DC: American Society for Microbiology. Nord, C. E. (1995). The role of anaerobic bacteria in recurrent episodes of sinusitis and tonsillitis. Clin Infect Dis 20, O Callaghan, C. H., Morris, A., Kirby, S. M. & Shingler, A. H. (1972). Novel method for detection of â-lactamases by using a chromogenic cephalosporin substrate. Antimicrob Agents Chemother 1, Paju, S., Bernstein, J. M., Haase, E. M. & Scannapieco, F. A. (2003). Molecular analysis of bacterial flora associated with chronically inflamed maxillary. J Med Microbiol 52, Summanen, P., Baron, E. J., Citron, D. M., Strong, C. A., Wexler, H. M. & Finegold, S. M. (1993). Wadsworth Bacteriology Manual, 5th edn. Belmont, CA: Star Publishing. Wexler, H. M. & Finegold, S. M. (1998). Current susceptibility patterns of anaerobic bacteria. Yonsei Med J 39, IP: