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Table. 
Organisms Isolated From Patients With Chronic Maxillary Sinusitis or Maxillary Acute Exacerbation of Chronic Sinusitis (AECS)*
Organisms Isolated From Patients With Chronic Maxillary Sinusitis or Maxillary Acute Exacerbation of Chronic Sinusitis (AECS)*
1.
Clement  PABluestone  CDGordts  F  et al.  Management of rhinosinusitis in children: consensus meeting, Brussels, Belgium, September 13, 1996. Arch Otolaryngol Head Neck Surg 1998;12431- 34
PubMedArticle
2.
Jousimies-Somer  HRSavolainen  SYlikoski  JS Bacteriological findings of acute maxillary sinusitis in young adults. J Clin Microbiol 1988;261919- 1925
PubMed
3.
Brook  I Bacteriological features of chronic sinusitis in children. JAMA 1981;246967- 969
PubMedArticle
4.
Nord  CE The role of anaerobic bacteria in recurrent episodes of sinusitis and tonsillitis. Clin Infect Dis 1995;201512- 1524
PubMedArticle
5.
Summanen  PBarron  EJCitron  DMStong  CWexler  HMFinegold  SM Wadsworth Anaerobic Bacteriology Manual. 5th ed. Belmont, Calif: Star Publishing; 1993
6.
Murray  PRBarron  EJJorenson  JH  et al Manual of Clinical Microbiology. 8th ed. Washington, DC: ASM Press; 2003
7.
O’Callaghan  CHMorris  AKirby  SMShingler  AH Novel method for detection of beta-lactamase by using a chromogenic cephalosporin substrate. Antimicrob Agents Chemother 1972;1283- 288
PubMedArticle
8.
Drettner  BLindholm  CE The borderline between acute rhinitis and sinusitis. Acta Otolaryngol 1967;64508- 513
PubMedArticle
9.
Carenfelt  CLundberg  C Purulent and non-purulent maxillary sinus secretions with respect to pO2, pCO2 and pH. Acta Otolaryngol 1977;84138- 144
PubMedArticle
10.
Aust  RDrettner  B Oxygen tension in the human maxillary sinus under normal and pathological conditions. Acta Otolaryngol 1974;78264- 269
PubMedArticle
11.
Carenfelt  C Pathogenesis of sinus empyema. Ann Otol Rhinol Laryngol 1979;8816- 20
PubMed
12.
Ednie  LMSpangler  SKJacobs  MRAppelbaum  PC 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 1997;411033- 1036
PubMed
13.
Brook  IGober  AE Emergence of beta-lactamase-producing aerobic and anaerobic bacteria in the oropharynx of children following penicillin chemotherapy. Clin Pediatr (Phila) 1984;23338- 341
PubMedArticle
14.
Wexler  HMFinegold  SM Current susceptibility patterns of anaerobic bacteria. Yonsei Med J 1998;39495- 501
PubMed
15.
Brook  IGober  AE Prophylaxis with amoxicillin or sulfisoxazole for otitis media: effect on the recovery of penicillin-resistant bacteria from children. Clin Infect Dis 1996;22143- 145
PubMedArticle
Original Article
October 2006

Bacteriology of Chronic Sinusitis and Acute Exacerbation of Chronic Sinusitis

Author Affiliations

Author Affiliation: Department of Pediatrics, Georgetown University School of Medicine, Washington, DC.

Arch Otolaryngol Head Neck Surg. 2006;132(10):1099-1101. doi:10.1001/archotol.132.10.1099
Abstract

Objective  To establish the microbiological characteristics of acute exacerbation of chronic sinusitis (AECS).

Setting  Academic medical center.

Patients  Thirty-two patients with chronic sinusitis and 30 patients with AECS.

Main Outcome Measure  The aerobic and anaerobic microbiology of maxillary AECS and chronic maxillary sinusitis.

Results  A total of 81 isolates (33 aerobic and 48 anaerobic) were recovered from the 32 cases (2.5 per specimen) with chronic sinusitis. Aerobes alone were recovered in 8 specimens (25%), anaerobes only were isolated in 11 (34%), and mixed aerobes and anaerobes were recovered in 13 (41%). The predominant aerobic and facultative bacteria were Enterobacteriaceae and Staphylococcus aureus. The predominant anaerobic bacteria were Peptostreptococcus subspecies, Fusobacterium subspecies, anaerobic gram-negative bacilli, and Propionibacterium acnes. Twenty-one β-lactamase–producing bacteria were recovered from 17 specimens (53%). A total of 89 isolates (40 aerobic and facultatives, and 49 anaerobic) were recovered from the 30 patients (3.0 per specimen) with AECS. Aerobes were recovered in 8 instances (27%), anaerobes only in 11 (37%), and mixed aerobes and anaerobes were recovered in 11 (37%). The predominant aerobes were Streptococcus pneumoniae, Enterobacteriaceae, and S aureus. The predominant anaerobes were Peptostreptococcus subspecies, Fusobacterium subspecies, anaerobic gram-negative bacilli, and P acnes. Thirty-six β-lactamase–producing bacteria were recovered from 28 specimens (53%).

Conclusions  This study demonstrates that the organisms isolated from patients with AECS were predominantly anaerobic and were similar to those generally recovered in patients with chronic sinusitis. However, aerobic bacteria that are usually found in acute infections (eg, S pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis) can also emerge in some of the episodes of AECS.

Acute exacerbation of chronic sinusitis (AECS) represents a sudden worsening of baseline chronic sinusitis with either worsening or new symptoms. Typically, the acute (not chronic) symptoms resolve completely between occurrences.1 The microbiology of acute sinusitis is well established where the major pathogens are aerobic and facultative bacteria—Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis.2 Similarly, the bacterial origin of chronic sinusitis has been studied extensively,3,4 and the predominant isolates are anaerobic bacteria. In contrast to acute and chronic sinusitis, the microbiology of AECS, to my knowledge, has not been studied before. Establishing the microbiological characteristics of AECS is of great scientific and practical importance. This article describes my experience during a 17-year period of studying the aerobic and anaerobic microbiology of AECS of the maxillary sinus and comparing my findings with those of chronic maxillary sinusitis.

METHODS

Sixty-two patients (32 with chronic sinusitis and 30 with AECS) were studied between June 1987 and June 2004. Excluded were 17 additional patients whose maxillary sinusitis yielded no bacterial growth. The patients studied were seen in an outpatient clinic in suburban Washington, DC; the Hospital for Sick Children, Washington, DC; and the Naval Hospital, Bethesda, Md.

Patients' ages ranged from 11 to 73 years (mean age, 48 years 4 months); 39 were males. Ten patients were children (<18 years). No differences in gender and age was noted between the 2 groups. Antimicrobial therapy was administered to 33 patients (53%) in the month prior to sample collection. These included 18 patients with chronic sinusitis and 15 patients with AECS.

Only patients fulfilling the following criteria were included in the study: typical clinical symptoms of sinusitis (headache, fever, nasal drainage, and others), positive radiographic findings, positive maxillary sinus bacterial culture results, and biopsy specimens demonstrating chronic inflammation of the sinus mucosal lining, or clinical and radiologic findings compatible with maxillary sinusitis followed by clinical and radiologic improvement following surgery and/or treatment with antibiotic therapy. Sinusitis was considered chronic if symptoms persisted for longer than 3 months. Patients with AECS had to fulfill the following 3 criteria: have chronic maxillary sinusitis, exhibit significant acute aggravation of their sinusitis symptoms (lasting >30 days), and have bacteria isolated from cultures of their sinuses.

The specimens were obtained using inferior meatal antrostomy after disinfection of the oral mucosa with 10% povidone-iodine and were transported to the laboratory in a syringe sealed with a rubber stopper after evacuation of the 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 shorter than 60 minutes for syringes and shorter than 3 hours for the anaerobic transport tube.

Specimens were inoculated onto 5% sheep's blood, chocolate agar, and MacConkey agar plates for the growth of aerobic and facultative 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 at 48 hours. For anaerobes the material was plated onto prereduced 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 hemin and vitamin K1).5 The anaerobic plates were incubated in anaerobic jars (GasPak jars; Baltimore Biological Laboratories) and examined at 48 and at 96 hours.

Aerobic and anaerobic bacteria were identified by conventional methods.5,6 β-Lactamase activity was determined by use of the chromogenic cephalosporin analog 87/312 method.7 Statistical analysis was performed using the t test.

RESULTS
CHRONIC SINUSITIS

A total of 81 isolates were recovered from the 32 patients (2.5 per specimen), 33 aerobic and facultative isolates (1.0 per specimen), and 48 anaerobic isolates (1.5 per specimen). The number of isolates per specimen varied from 1 to 4. Aerobic and facultative organisms alone were recovered in 8 specimens (25%), anaerobes only were isolated in 11 (34%), and mixed aerobic and anaerobic bacteria were recovered in 13 (41%). The predominant aerobic and facultative isolates were α-hemolytic streptococci, Enterobacteriaceae (Escherichia coli, Proteus mirabilis, Klebsiella pneumoniae), and S aureus (Table). The predominant anaerobic bacteria were Peptostreptococcus subspecies (16), Fusobacterium subspecies (8), anaerobic gram-negative bacilli (21, including pigmented Prevotella and Porphyromonas subspecies), and Propionibacterium acnes. Twenty-one β-lactamase–producing bacteria (BLPB) were recovered from 17 specimens (53%).

ACUTE EXACERBATION OF CHRONIC SINUSITIS

A total of 89 isolates were recovered from the 30 patients (3.0 per specimen), 40 aerobic and facultative isolates (1.3 per specimen), and 49 anaerobic isolates (1.6 per specimen). The number of isolates varied from 1 to 5. Aerobic and facultative organisms were recovered in 8 instances (27%), anaerobes only in 11 (37%), and mixed aerobic and anaerobic bacteria in 11 (37%). The predominant aerobic and facultatives were S pneumoniae, α-hemolytic streptococci, Enterobacteriaceae (E coli, P mirabilis, and K pneumoniae), and S aureus (Table). The predominant anaerobic bacteria were Peptostreptococcus subspecies (14 isolates), Fusobacterium subspecies (10), anaerobic gram-negative bacilli (21, including pigmented Prevotella and Porphyromonas subspecies), and P acnes (4). Thirty-six BLPB were recovered from 28 specimens (53%) (P<.001, compared with patients with chronic sinusitis).

COMMENT

To my knowledge, this study describes, for the first time, the microbiology of AECS of the maxillary sinus. The organisms isolated from these patients were predominantly anaerobic and were similar to those generally recovered in chronic sinusitis (Prevotella, Porphyromonas, Peptostreptococcus, and Fusobacterium subspecies).3

The recovery of anaerobic bacteria in all instances confirms their importance in chronic maxillary sinusitis and confirms previous studies where adequate methods for specimen transportation and bacterial isolation were used.3,4 However, this study demonstrates that, in addition to the predominance of the anaerobic organisms, aerobic bacteria that are usually found in acute infections (eg, S pneumoniae, H influenzae, and M catarrhalis)1,2 can also emerge in some of the episodes of AECS.4 The number of S pneumoniae and H influenzae was statistically significantly higher in patients with AECS compared with those with chronic sinusitis (P<.03).

The frequent involvement of anaerobes in chronic sinusitis probably may be related to the poor drainage and increased intranasal pressure that develops during inflammation.8 This can reduce the oxygen tension in the inflamed sinus9 by decreasing the mucosal blood flow10 and depressing the ciliary action.11 The lowering of the oxygen content and pH of the sinus cavity supports the growth of anaerobic organisms by providing them with an optimal oxidation-reduction potential.11

Resistance to antimicrobial agents through the production of β-lactamase was observed more often in isolates that were recovered from patients with AECS. Thirty-six such isolates (40% of the total number of isolates) were found in those with AECS compared with 21 isolates (26% of the total) that were recovered in those with chronic sinusitis. An increase was also found in the recovery rate of S pneumoniae that were resistant to penicillin, from none in chronic sinusitis to 4 in AECS.

This finding highlights the importance of obtaining cultures from patients with AECS for guidance in selection of proper antimicrobial therapy. As recurrences occur, the bacterial cause and antimicrobial susceptibility may change.

The growing resistance of S pneumoniae to penicillin and other antimicrobial agents such as trimethoprim-sulfamethoxazole and macrolides12 and the production of β-lactamase by H influenzae, M catarrhalis,13 pigmented Prevotella and Porphyromonas subspecies, and Fusobacterium subspecies14 are the major causes of resistance. Selection of antimicrobial agents for the therapy of AECS can be improved by obtaining cultures from 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 therapy13 or prophylaxis15 that may select resistant strains.

Further studies of the microbiology and effect of antimicrobial therapy of AECS are warranted. These studies should investigate whether the use of antimicrobial agents effective against resistant organisms will be able to reduce the occurrence of recurrences in these patients.

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Article Information

Correspondence: Itzhak Brook, MD, MSc, 4431 Albemarle St NW, Washington DC 20016 (ib6@georgetown.edu).

Submitted for Publication: March 26, 2006; accepted May 6, 2006.

Author Contributions: Dr Brook had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Financial Disclosure: None reported.

References
1.
Clement  PABluestone  CDGordts  F  et al.  Management of rhinosinusitis in children: consensus meeting, Brussels, Belgium, September 13, 1996. Arch Otolaryngol Head Neck Surg 1998;12431- 34
PubMedArticle
2.
Jousimies-Somer  HRSavolainen  SYlikoski  JS Bacteriological findings of acute maxillary sinusitis in young adults. J Clin Microbiol 1988;261919- 1925
PubMed
3.
Brook  I Bacteriological features of chronic sinusitis in children. JAMA 1981;246967- 969
PubMedArticle
4.
Nord  CE The role of anaerobic bacteria in recurrent episodes of sinusitis and tonsillitis. Clin Infect Dis 1995;201512- 1524
PubMedArticle
5.
Summanen  PBarron  EJCitron  DMStong  CWexler  HMFinegold  SM Wadsworth Anaerobic Bacteriology Manual. 5th ed. Belmont, Calif: Star Publishing; 1993
6.
Murray  PRBarron  EJJorenson  JH  et al Manual of Clinical Microbiology. 8th ed. Washington, DC: ASM Press; 2003
7.
O’Callaghan  CHMorris  AKirby  SMShingler  AH Novel method for detection of beta-lactamase by using a chromogenic cephalosporin substrate. Antimicrob Agents Chemother 1972;1283- 288
PubMedArticle
8.
Drettner  BLindholm  CE The borderline between acute rhinitis and sinusitis. Acta Otolaryngol 1967;64508- 513
PubMedArticle
9.
Carenfelt  CLundberg  C Purulent and non-purulent maxillary sinus secretions with respect to pO2, pCO2 and pH. Acta Otolaryngol 1977;84138- 144
PubMedArticle
10.
Aust  RDrettner  B Oxygen tension in the human maxillary sinus under normal and pathological conditions. Acta Otolaryngol 1974;78264- 269
PubMedArticle
11.
Carenfelt  C Pathogenesis of sinus empyema. Ann Otol Rhinol Laryngol 1979;8816- 20
PubMed
12.
Ednie  LMSpangler  SKJacobs  MRAppelbaum  PC 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 1997;411033- 1036
PubMed
13.
Brook  IGober  AE Emergence of beta-lactamase-producing aerobic and anaerobic bacteria in the oropharynx of children following penicillin chemotherapy. Clin Pediatr (Phila) 1984;23338- 341
PubMedArticle
14.
Wexler  HMFinegold  SM Current susceptibility patterns of anaerobic bacteria. Yonsei Med J 1998;39495- 501
PubMed
15.
Brook  IGober  AE Prophylaxis with amoxicillin or sulfisoxazole for otitis media: effect on the recovery of penicillin-resistant bacteria from children. Clin Infect Dis 1996;22143- 145
PubMedArticle
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