Bacteriology of Chronic Sinusitis and Acute Exacerbation of Chronic Sinusitis

ORIGINAL ARTICLE Bacteriology of Chronic Sinusitis and Acute Exacerbation of Chronic Sinusitis

Itzhak Brook, MD, MSc

Objective: To establish the microbiological character- ria were recovered from 17 specimens (53%). A total of istics of acute exacerbation of chronic sinusitis (AECS). 89 isolates (40 aerobic and facultatives, and 49 anaerobic) were recovered from the 30 patients (3.0 per speci- Setting: Academic medical center. men) with AECS. Aerobes were recovered in 8 instances (27%), anaerobes only in 11 (37%), and mixed Patients: Thirty-two patients with chronic sinusitis and aerobes and anaerobes were recovered in 11 (37%). The 30 patients with AECS. predominant aerobes were Streptococcus pneumoniae, En- terobacteriaceae, and S aureus. The predominant anaer- Main Outcome Measure: The aerobic and anaerobic obes were Peptostreptococcus subspecies, Fusobacterium microbiology of maxillary AECS and chronic maxillary subspecies, anaerobic gram-negative bacilli, and P ac- sinusitis. nes. Thirty-six ␤-lactamase–producing bacteria were recovered from 28 specimens (53%). Results: A total of 81 isolates (33 aerobic and 48 anaerobic) were recovered from the 32 cases (2.5 per speci- Conclusions: This study demonstrates that the organ- men) with chronic sinusitis. Aerobes alone were recov- isms isolated from patients with AECS were predomi- ered in 8 specimens (25%), anaerobes only were isolated nantly anaerobic and were similar to those generally re- in 11 (34%), and mixed aerobes and anaerobes were recovered in patients with chronic sinusitis. However, covered in 13 (41%). The predominant aerobic and fac- aerobic bacteria that are usually found in acute infec- ultative bacteria were Enterobacteriaceae and Staphylo- tions (eg, S pneumoniae, Haemophilus influenzae, and Mo- coccus aureus. The predominant anaerobic bacteria were raxella catarrhalis) can also emerge in some of the epi- Peptostreptococcus subspecies, Fusobacterium subspe- sodes of AECS. cies, anaerobic gram-negative bacilli, and Propionibacte- rium acnes. Twenty-one ␤-lactamase–producing bacte- Arch Otolaryngol Head Neck Surg. 2006;132:1099-1101

CUTE EXACERBATION OF riod of studying the aerobic and anaerobic chronic sinusitis (AECS) microbiology of AECS of the maxillary si- represents a sudden wors- nus and comparing my findings with those ening of baseline chronic of chronic maxillary sinusitis. sinusitis with either wors- eningA or new symptoms. Typically, the METHODS acute (not chronic) symptoms resolve completely between occurrences.1 The Sixty-two patients (32 with chronic sinusitis and microbiology of acute sinusitis is well 30 with AECS) were studied between June 1987 established where the major pathogens and June 2004. Excluded were 17 additional pa- are aerobic and facultative bacteria— tients whose maxillary sinusitis yielded no bac- Streptococcus pneumoniae, Haemophilus terial growth. The patients studied were seen in influenzae, and Moraxella catarrhalis.2 an outpatient clinic in suburban Washington, Similarly, the bacterial origin of chronic DC; the Hospital for Sick Children, Washing- sinusitis has been studied extensively,3,4 ton, DC; and the Naval Hospital, Bethesda, Md. and the predominant isolates are anaero- Patients’ ages ranged from 11 to 73 years (mean age, 48 years 4 months); 39 were males. bic bacteria. In contrast to acute and Ͻ chronic sinusitis, the microbiology of AECS, Ten patients were children ( 18 years). No dif- ferences in gender and age was noted be- to my knowledge, has not been studied between the 2 groups. Antimicrobial therapy was Author Affiliation: Department fore. Establishing the microbiological char- administered to 33 patients (53%) in the month of Pediatrics, Georgetown acteristics of AECS is of great scientific and prior to sample collection. These included 18 University School of Medicine, practical importance. This article de- patients with chronic sinusitis and15 patients Washington, DC. scribes my experience during a 17-year pe- with AECS.

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©2006 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 anaerobes the material was plated onto prereduced vitamin K1- Table. Organisms Isolated From Patients With Chronic enriched Brucella blood agar, an anaerobic blood agar plate con- Maxillary Sinusitis or Maxillary Acute Exacerbation taining kanamycin and vancomycin, an anaerobic blood plate of Chronic Sinusitis (AECS)* containing colistin and nalidixic acid, and an enriched thiogly- 5 colate broth (containing hemin and vitamin K1). The anaero- Patients With Patients bic plates were incubated in anaerobic jars (GasPak jars; Balti- Chronic Sinusitis With AECS more Biological Laboratories) and examined at 48 and at 96 hours. Bacteria (n = 32) (n = 30) Aerobic and anaerobic bacteria were identified by conven- Aerobic bacteria tional methods.5,6 ␤-Lactamase activity was determined by use ␣-Hemolytic streptococcus 7 5 of the chromogenic cephalosporin analog 87/312 method.7 Sta- Microaerophilic streptococci 3 4 tistical analysis was performed using the t test. Streptococcus pneumoniae 17† Streptococcus pyogenes 11 Group G streptococcus 1 1 RESULTS Group F streptococcus 2 0 Staphylococcus aureus 5 (5) 4 (4) CHRONIC SINUSITIS Staphylococcus epidermidis 2 (1) 1 Klebsiella pneumoniae 2 (2) 2 (2) Escherichia coli 2 (1) 1 (1) A total of 81 isolates were recovered from the 32 pa- Proteus mirabilis 3 (2) 2 (1) tients (2.5 per specimen), 33 aerobic and facultative iso- Pseudomonas aeruginosa 2 (2) 1 (1) lates (1.0 per specimen), and 48 anaerobic isolates (1.5 Haemophilus influenzae 2 (2) 9† (5) per specimen). The number of isolates per specimen var- Moraxella catarrhalis 0 2 (2) ied from 1 to 4. Aerobic and facultative organisms alone Subtotal 33 (15) 40 (16) were recovered in 8 specimens (25%), anaerobes only were Anaerobic bacteria isolated in 11 (34%), and mixed aerobic and anaerobic Peptostreptococcus species 16 14 Propionibacterium acnes 34 bacteria were recovered in 13 (41%). The predominant Fusobacterium species 3 (1) 4 (3) aerobic and facultative isolates were ␣-hemolytic strep- Fusobacterium nucleatum 5 (1) 6 (4) tococci, Enterobacteriaceae (Escherichia coli, Proteus mi- Bacteroides species 2 3 (2) rabilis, Klebsiella pneumoniae), and S aureus (Table). The Prevotella melaninogenica 4 (1) 6 (5) predominant anaerobic bacteria were Peptostreptococ- Prevotella intermedia 6 (2) 4 (3) cus subspecies (16), Fusobacterium subspecies (8), an- Prevotella oralis 4 5 (1) Porphyromonas asaccharolytica 5 (1) 3 (2) aerobic gram-negative bacilli (21, including pigmented Subtotal 48 (6) 49 (20) Prevotella and Porphyromonas subspecies), and Propioni- Total 81 (21) 89 (36) bacterium acnes. Twenty-one ␤-lactamase–producing bacteria (BLPB) were recovered from 17 specimens (53%). *Data are given as the number of isolates (the number of ␤-lactamase–producing bacteria). ACUTE EXACERBATION OF CHRONIC SINUSITIS †PϽ.03. A total of 89 isolates were recovered from the 30 pa- Only patients fulfilling the following criteria were in- tients (3.0 per specimen), 40 aerobic and facultative iso- cluded in the study: typical clinical symptoms of sinusitis (head- lates (1.3 per specimen), and 49 anaerobic isolates (1.6 ache, fever, nasal drainage, and others), positive radiographic per specimen). The number of isolates varied from 1 to findings, positive maxillary sinus bacterial culture results, and 5. Aerobic and facultative organisms were recovered in biopsy specimens demonstrating chronic inflammation of the 8 instances (27%), anaerobes only in 11 (37%), and mixed sinus mucosal lining, or clinical and radiologic findings com- patible with maxillary sinusitis followed by clinical and radio- aerobic and anaerobic bacteria in 11 (37%). The pre- logic improvement following surgery and/or treatment with an- dominant aerobic and facultatives were S pneumoniae, tibiotic therapy. Sinusitis was considered chronic if symptoms ␣-hemolytic streptococci, Enterobacteriaceae (E coli, P persisted for longer than 3 months. Patients with AECS had to mirabilis, and K pneumoniae), and S aureus (Table). The fulfill the following 3 criteria: have chronic maxillary sinus- predominant anaerobic bacteria were Peptostreptococ- itis, exhibit significant acute aggravation of their sinusitis symp- cus subspecies (14 isolates), Fusobacterium subspecies toms (lasting Ͼ30 days), and have bacteria isolated from cul- (10), anaerobic gram-negative bacilli (21, including pig- tures of their sinuses. mented Prevotella and Porphyromonas subspecies), and The specimens were obtained using inferior meatal antros- P acnes (4). Thirty-six BLPB were recovered from 28 speci- tomy after disinfection of the oral mucosa with 10% povidone- mens (53%) (PϽ.001, compared with patients with iodine and were transported to the laboratory in a syringe sealed with a rubber stopper after evacuation of the air or in an an- chronic sinusitis). aerobic transport tube (Port-A-Cul; Baltimore Biological Labo- ratories, Cockeysville, Md). The time between the collection COMMENT of materials and inoculation of the specimen was generally shorter than 60 minutes for syringes and shorter than 3 hours To my knowledge, this study describes, for the first time, for the anaerobic transport tube. Specimens were inoculated onto 5% sheep’s blood, choco- the microbiology of AECS of the maxillary sinus. The or- late agar, and MacConkey agar plates for the growth of aerobic ganisms isolated from these patients were predomi- and facultative organisms. The plates were incubated at 37°C aero- nantly anaerobic and were similar to those generally re- bically (MacConkey) or under 5% carbon dioxide (5% sheep’s covered in chronic sinusitis (Prevotella, Porphyromonas, blood and chocolate) and examined at 24 and at 48 hours. For Peptostreptococcus, and Fusobacterium subspecies).3

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©2006 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 The recovery of anaerobic bacteria in all instances con- Further studies of the microbiology and effect of an- firms their importance in chronic maxillary sinusitis and timicrobial therapy of AECS are warranted. These stud- confirms previous studies where adequate methods for ies should investigate whether the use of antimicrobial specimen transportation and bacterial isolation were agents effective against resistant organisms will be used.3,4 However, this study demonstrates that, in addi- able to reduce the occurrence of recurrences in these tion to the predominance of the anaerobic organisms, aero- patients. bic bacteria that are usually found in acute infections (eg, S pneumoniae, H influenzae, and M catarrhalis)1,2 can also Submitted for Publication: March 26, 2006; accepted emerge in some of the episodes of AECS.4 The number May 6, 2006. of S pneumoniae and H influenzae was statistically sig- Correspondence: Itzhak Brook, MD, MSc, 4431 Albemarle nificantly higher in patients with AECS compared with St NW, Washington DC 20016 ([email protected]). those with chronic sinusitis (PϽ.03). Author Contributions: Dr Brook had full access to all The frequent involvement of anaerobes in chronic si- the data in the study and takes responsibility for the in- nusitis probably may be related to the poor drainage and tegrity of the data and the accuracy of the data analysis. increased intranasal pressure that develops during in- Financial Disclosure: None reported. flammation.8 This can reduce the oxygen tension in the inflamed sinus9 by decreasing the mucosal blood flow10 REFERENCES and depressing the ciliary action.11 The lowering of the oxygen content and pH of the sinus cavity supports the 1. Clement PA, Bluestone CD, Gordts F, et al. Management of rhinosinusitis in chil- growth of anaerobic organisms by providing them with dren: consensus meeting, Brussels, Belgium, September 13, 1996. Arch Oto- 11 laryngol Head Neck Surg. 1998;124:31-34. an optimal oxidation-reduction potential. 2. Jousimies-Somer HR, Savolainen S, Ylikoski JS. Bacteriological findings of acute Resistance to antimicrobial agents through the pro- maxillary sinusitis in young adults. J Clin Microbiol. 1988;26:1919-1925. duction of ␤-lactamase was observed more often in iso- 3. Brook I. Bacteriological features of chronic sinusitis in children. JAMA. 1981;246: lates that were recovered from patients with AECS. Thirty- 967-969. 4. Nord CE. The role of anaerobic bacteria in recurrent episodes of sinusitis and six such isolates (40% of the total number of isolates) were tonsillitis. Clin Infect Dis. 1995;20:1512-1524. found in those with AECS compared with 21 isolates (26% 5. Summanen P, Barron EJ, Citron DM, Stong C, Wexler HM, Finegold SM. Wadsworth of the total) that were recovered in those with chronic Anaerobic Bacteriology Manual. 5th ed. Belmont, Calif: Star Publishing; 1993. sinusitis. An increase was also found in the recovery rate 6. Murray PR, Barron EJ, Jorenson JH, et al. Manual of Clinical Microbiology. 8th ed. Washington, DC: ASM Press; 2003. of S pneumoniae that were resistant to penicillin, from none 7. O’Callaghan CH, Morris A, Kirby SM, Shingler AH. Novel method for detection of in chronic sinusitis to 4 in AECS. beta-lactamase by using a chromogenic cephalosporin substrate. Antimicrob This finding highlights the importance of obtaining Agents Chemother. 1972;1:283-288. cultures from patients with AECS for guidance in selec- 8. Drettner B, Lindholm CE. The borderline between acute rhinitis and sinusitis. Acta Otolaryngol. 1967;64:508-513. tion of proper antimicrobial therapy. As recurrences oc- 9. Carenfelt C, Lundberg C. Purulent and non-purulent maxillary sinus secretions

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