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J Med Microbiol 53 (2004), 879-885; DOI: 10.1099/jmm.0.45655-0
© 2004 Society for General Microbiology
ISSN 0022-2615

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

Itzhak Brook

Department of Pediatrics, Georgetown University School of Medicine, 4431 Albemarle St NW, Washington DC 20016, USA

Correspondence Itzhak Brook ib6{at}georgetown.edu

Received March 1, 2004
Accepted May 18, 2004

The microbiology of acute and chronic sinusitis has been studied extensively. Establishing the concomitant distribution of the causative organisms in cases that involve multiple sinuses 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 sinuses. The 155 patients evaluated had sinusitis of either the maxillary, ethmoid or frontal sinuses (any combination) and had organisms recovered from two to four concomitantly infected sinuses. Similar aerobic, facultatively anaerobic and anaerobic organisms were recovered from all groups of patients. In patients who had organisms isolated from two sinuses and had acute sinusitis, 31 (56 %) of the 55 isolates were found only in a single sinus, and 24 (44 %) were recovered concomitantly from two sinuses. In those with chronic infection 31 (34 %) of the 91 isolates were recovered only from a single sinus, and 60 (66 %) were found concomitantly from two sinuses. Anaerobic bacteria were more often isolated concomitantly from two sinuses (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 sinuses. ß-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 sinuses and emphasize the importance of obtaining cultures from all infected sinuses.

Abbreviation: BLPB, ß-lactamase producing bacteria.


   Introduction
TOP
 Introduction
Patients and Methods
 Results
 Discussion
 References
 
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 one sinus. 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 sinuses. Establishing the distribution of organisms in cases that involve multiple sinuses 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 sinuses.


   Patients and Methods
TOP
 Introduction
 Patients and Methods
Results
 Discussion
 References
 
The 155 patients included in the report were studied between June 1977 and June 2003. 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 sinuses. They included 42 patients with acute sinusitis and 38 with chronic sinusitis who had organisms recovered from two sinuses, 22 with acute sinusitis and 24 with chronic sinusitis who had organisms recovered from three sinuses, and 14 with acute sinusitis and 15 with chronic sinusitis who had organisms recovered from four sinuses. Excluded were 37 additional patients whose sinuses 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 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 °C 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-K1-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 K1) (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). Aerobic bacteria were identified by conventional methods (Murray et al., 1999). ß-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
TOP
 Introduction
 Patients and Methods
 Results
Discussion
 References
 
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 sinuses. The aerobic and facultatively anaerobic isolates 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 isolates 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 ß-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 sinuses

Acute sinusitis (Table 1).


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  		Table 1. Isolates from 42 patients with acute sinusitis who had organisms recovered from two sinuses Number of BLPB is shown in parentheses.
 

A total of 55 isolates 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 isolates per specimen varied from one to three. Aerobic 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 isolates were found only in a single sinus, and 24 (44 %) were recovered concomitantly from two sinuses.

Chronic sinusitis (Table 2).


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  		Table 2. Isolates from 38 patients with chronic sinusitis who had organisms recovered from two sinuses Number of BLPB is shown in parentheses.
 

A total of 91 isolates 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 isolates per specimen varied from one to five. Aerobic and facultatively anaerobic organisms 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.

Thirty-one (34 %) of the 91 isolates were recovered only from a single sinus, and 60 (66 %) were present concomitantly in two sinuses. Anaerobic bacteria were more often isolated concomitantly from two sinuses (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 sinuses

Acute sinusitis (Table 3).


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  		Table 3. Isolates from 22 patients with acute sinusitis who had organisms recovered from three sinuses Number of BLPB is shown in parentheses.
 

A total of 30 isolates 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 isolates per specimen varied from one to three. Aerobic 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.

Twelve (40 %) of the 30 isolates were recovered only from a single sinus, 11 (37 %) were concomitantly present in two sinuses, and seven (23 %) were recovered from three sinuses. Anaerobic bacteria were never isolated from three sinuses.

Chronic sinusitis (Table 4).


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  		Table 4. Isolates from 24 patients with chronic sinusitis who had organisms recovered from three sinuses Number of BLPB is shown in parentheses.
 

A total of 67 isolates 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 isolates per specimen varied from one to five. Aerobic 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 isolates were recovered only from a single sinus, 32 (48 %) were concomitantly present in two sinuses, and 18 (27 %) were recovered from three sinuses. There were no differences in the recovery rate between aerobic and facultatively anaerobic and anaerobic bacteria in single or multiple sinuses. However, Streptococcus pneumoniae, Proteus mirabilis and Propionibacterium acnes were only isolated from a single sinus.

Comparisons of 29 patients with sinusitis who had organisms recovered from four sinuses

Acute sinusitis (Table 5).


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  		Table 5. Isolates from 14 patients with acute sinusitis who had organisms recovered from four sinuses Number of BLPB is shown in parentheses.
 

A total of 26 isolates 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 isolates per specimen varied from one to three. Aerobic 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 isolates were recovered only from a single sinus, eight (31 %) were concomitantly present in two sinuses, eight (31 %) were recovered from three sinuses, and three (11 %) were isolated in four sinuses. Anaerobic bacteria were never isolated from four sinuses.

Chronic sinusitis (Table 6).


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  		Table 6. Isolates from 15 patients with chronic sinusitis who had organisms recovered from four sinuses Number of BLPB bacteria is shown in parentheses.
 

A total of 53 isolates 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 isolates per specimen varied from one to five. Aerobic 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 isolates were recovered only from a single sinus, 17 (32 %) were concomitantly present in two sinuses, 17 (32 %) were recovered from three sinuses, and nine (17 %) were found in four sinuses. There were no differences in the recovery rate between aerobic and facultatively anaerobic and anaerobic bacteria in single or multiple sinuses. However, no aerobic or facultatively anaerobic bacteria were present in all four sinuses and Propionibacterium acnes was not recovered from three or four sinuses.


   Discussion
TOP
 Introduction
 Patients and Methods
 Results
 Discussion
References
 
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 sinuses 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 sinuses. 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 sinuses. Since 19–56 % of the isolates we recovered were present only in a single sinus, a large proportion of the isolates would have been missed if only a single sinus were studied. Obtaining cultures from all infected sinuses 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 sinuses.

The lack of recovery of any organisms from 37 additional patients is consistent with the experience of other investigators. 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 ß-lactamase was observed in this study more often in isolates 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 ß-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 ß-lactamases (Brook et al., 1996). ß-Lactamase activity was seen in 86 % of sinus aspirates that contained ß-lactamase producing organisms. It has been suggested that the ß-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 ß-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 sinuses (Paju et al., 2003).


   References
TOP
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

  • Brook, I. (1981). Bacteriological features of chronic sinusitis in children. JAMA 246, 967–969.[Abstract]

  • Brook, I. (1984). The role of ß-lactamase-producing bacteria in the persistence of streptococcal tonsillar infection. Rev Infect Dis 6, 601–607.[Medline]

  • Brook, I. & Gober, A. E. (1984). Emergence of ß-lactamase-producing aerobic and anaerobic bacteria in the oropharynx of children following penicillin chemotherapy. Clin Pediatr (Phila) 23, 338–341.

  • Brook, I. & Yocum, P. (1995). Bacteriology and ß-lactamase activity in ear aspirates of acute otitis media that failed amoxicillin therapy. Pediatr Infect Dis J 14, 805–809.[Medline]

  • Brook, I. & Gober, A. E. (1996). Prophylaxis with amoxicillin or sulfisoxazole for otitis media: effect on the recovery of penicillin-resistant bacteria from children. Clin Infect Dis 22, 143–145.[Medline]

  • Brook, I. Yocum, P. & Frazier, E. H. (1996). Bacteriology and ß-lactamase activity in acute and chronic maxillary sinusitis. Arch Otolaryngol Head Neck Surg 122, 418–423.[Abstract]

  • 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, 1033–1036.[Abstract]

  • 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.[CrossRef][Medline]

  • Jousimies-Somer, H. R., Savolainen, S. & Ylikoski J. S. (1988). Bacteriological findings of acute maxillary sinusitis in young adults. J Clin Microbiol 26, 1919–1925.[Abstract/Free Full Text]

  • 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, 1512–1524.[Medline]

  • O'Callaghan, C. H., Morris, A., Kirby, S. M. & Shingler, A. H. (1972). Novel method for detection of ß-lactamases by using a chromogenic cephalosporin substrate. Antimicrob Agents Chemother 1, 283–288.[Abstract/Free Full Text]

  • Paju, S., Bernstein, J. M., Haase, E. M. & Scannapieco, F. A. (2003). Molecular analysis of bacterial flora associated with chronically inflamed maxillary sinuses. J Med Microbiol 52, 591–597.[Abstract/Free Full Text]

  • Summanen, P., Baron, E. J., Citron, D. M., Strong, C. A., Wexler, H. M. & Finegold, S. M. (1993). Wadsworth Anaerobic 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, 495–501.[Medline]





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