J Med Microbiol 55 (2006), 943-946; DOI: 10.1099/jmm.0.46346-0
© 2006 Society for General Microbiology
ISSN 1473-5644
Frequency of recovery of pathogens causing acute maxillary sinusitis in adults before and after introduction of vaccination of children with the 7-valent pneumococcal vaccine
Itzhak Brook,
Perry A. Foote and
Jeffrey N. Hausfeld
Departments of Pediatrics, Georgetown University School of Medicine and Alachua General and North Florida Regional Hospitals, Gainesville, Florida, USA
Correspondence
Itzhak Brook
ib6{at}georgetown.edu
Received 27 September 2005
Accepted 22 March 2006
The objective of the study was to compare the proportions of the recovery of pathogens of acute maxillary sinusitis in adults in the 4-year period prior to the 5-year period that followed the introduction of vaccination of children with the 7-valent pneumococcal vaccine (PCV7). Cultures were obtained through endoscopy from 385 adults with acute maxillary sinusitis, 156 between 1997 and 2000, and 229 between 2001 and 2005. One hundred and seventeen potentially pathogenic organisms were isolated from the cultures obtained between 1997 and 2000. The predominant organisms were Streptococcus pneumoniae (54 or 46 % of all isolates), Haemophilus influenzae non-type b (42 or 36 %), Moraxella catarrhalis (7 or 6 %), Streptococcus pyogenes (8 or 7 %) and Staphylococcus aureus (6 or 5 %). One hundred and sixty-seven potentially pathogenic organisms were isolated from the cultures obtained between 2001 and 2005. The most predominant organisms were H. influenzae non-type b (71 or 43 % of all isolates), Strep. pneumoniae (58 or 35 %), M. catarrhalis (13 or 8 %), Strep. pyogenes (12 or 7 %) and Staph. aureus (13 or 8 %). Significant statistical differences were noted in the rates of recovery of H. influenzae non-type b (P<0.05) and Strep. pneumoniae (P<0.05). A decrease occurred in the recovery of Strep. pneumoniae resistant to penicillin from 41 to 29 %, and an increase was noted in the isolation of beta-lactamase-producing H. influenzae from 33 to 39 %; however, neither change was statistically significant. These data illustrate that a significant shift occurred in the causative pathogens of acute maxillary sinusitis in adults in the 5 years after the introduction of vaccination of children with the PCV7 compared to the previous 4 years.
Abbreviations: AOM, acute otitis media; PCV7, 7-valent pneumococcal vaccine.
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INTRODUCTION
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The growing resistance to antimicrobial agents of all respiratory tract bacterial pathogens has made the management of bacterial sinusitis more difficult. Failure of antimicrobials to clear the infection can be due to persistence of the pathogen(s) because of inadequate pharmacokinetic and pharmacodynamic qualities of the antimicrobials, and the development of resistance to the antimicrobial used (Brook & Gober, 2004; Brook, 2005; Pichichero & Pichichero, 1995; Craig & Andes, 1996).
The Sinus and Allergy Partnership recently published guidelines for the diagnosis and optimal treatment of acute bacterial rhinosinusitis (Sinus and Allergy Health Partnership, 2004). They based their recommendations on predicted bacterial efficacy rates from mathematical modelling of acute sinusitis based on pathogen distribution, resolution rates without treatment, and in vitro microbiological efficacy. Since the above recommendations are based on the frequency of recovery of the pathogenic organisms, awareness of the effect of the recent introduction of the Streptococcus pneumoniae conjugated vaccine (in April 2000) on the frequency of recovery of pathogens is of great practical use. A shift in the frequency of recovery of causative pathogens was recently demonstrated in children with acute otitis media (AOM) who were vaccinated with the 7-valent pneumococcal vaccine (PCV7) (Casey & Pichichero, 2004; Block et al., 2004); however, no evaluation of the effect on the introduction of the vaccine on the recovery of respiratory pathogens was done in adults.
This study compared the proportion of recovery of pathogens of acute maxillary sinusitis in the 4 years before and the 5 years after the introduction of vaccination of children with the PCV7.
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METHODS
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Patients.
The population studied was middle class, residing in suburban locations in the vicinity of Washington, DC. The patients were consecutively seen in the outpatient clinic between 1997 and 2005 and were diagnosed as suffering from acute bacterial maxillary sinusitis. They each had symptoms lasting between 10 and 30 days. None had had ear or sinus infection for at least 3 months before their initial visit, and they had not received antimicrobial therapy for at least 2 months.
Patients' complaints included facial pain, frontal headache, purulent nasal discharge, fever and malaise. Occipitomental (Waters' view), lateral, oblique and verticomental views or computed tomography were obtained. Sinusitis was defined radiographically as complete sinus opacity, an air-fluid level, or mucous-membrane thickening of at least 6 mm in the maxillary sinus. For the Waters' view, mucosal thickening of the maxillary sinuses was measured as the shortest distance from the air–mucosal interface to the most lateral part of the maxillary sinus wall. Specimens were obtained through endoscopy and the sinus secretions were collected with calcium-alginate-tipped micro-swabs. The study was granted an Institutional Review Board approval.
Microbiology.
Cultures were obtained using endoscopic aspiration before therapy using calcium alginate swabs that were immediately plated into media supportive of the growth of aerobic bacteria. The method of specimen collection has been described previously (Brook et al., 1996). The collectors of cultures and the microbiologist were blinded to the patients' therapy. Specimens were processed semi-quantitively, and organisms were identified using standard methods (Murray et al., 1995). All isolates of Strep. pneumoniae were screened for penicillin susceptibility with a 1 µg oxacillin disc by the Kirby–Bauer disc-diffusion method. Intermediate resistance to penicillin was defined as a MIC of 0.1–1.0 µg ml–1 and high resistance to penicillin was defined as MIC 
2.0 µg ml–1.
MIC values of all antimicrobials were determined by the broth microdilution methodology following the guidelines of the National Committee for Clinical Laboratory Standards (NCCLS) with cation-adjusted Mueller–Hinton broth (Difco Laboratories) supplemented with 5 % lysed horse blood for Strep. pneumoniae and Streptococcus pyogenes. MIC values of amoxycillin and amoxycillin/clavulanate were determined by using Haemophilus test medium for Haemophilus species and Moraxella catarrhalis (National Committee for Clinical Laboratory Standards, 1995). MIC values were interpreted according to the NCCLS M100-S10 MIC testing supplemental tables (National Committee for Clinical Laboratory Standards, 2000). Beta-lactamase production was determined by the chromogenic cephalosporin methodology, by using nitrocefin as the substrate (O'Callaghan et al., 1972). Statistical significance was calculated by Fishers exact test (two-sided) unadjusted.
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RESULTS
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Three hundred and eighty five patients with acute maxillary sinusitis were studied, 156 in the 4 years between 1997 and 2000, and 229 in the 5 years between 2001 and 2005. Their ages ranged from 19 to 73 years; 218 were males. No differences were noted in the age distribution and gender of the patients in the two study periods.
One hundred and seventeen potentially pathogenic organisms were isolated from the cultures obtained between 1997 and 2000. Organisms were isolated in 89 patients (57 %). A single isolate was recovered from 64 patients, two were found in 22, and three in three individuals. The predominant organisms were Strep. pneumoniae (54 or 46 % of all isolates), Haemophilus influenzae non-type b (42 or 36 %), M. catarrhalis (7 or 6 %), Streptococcus pyogenes (8 or 7 %) and Staphylococcus aureus (6 or 5 %) (Table 1
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Table 1. Recovery of acute maxillary sinusitis pathogens in 156 patients between 1997 and 2000, and 229 patients between 2001 and 2005
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One hundred and sixty seven potentially pathogenic organisms were isolated from the cultures obtained between 2001 and 2005. Organisms were isolated in 134 patients (59 %). A single isolate was recovered from 105 patients, two were found in 25, and three in four. The most predominant organisms were H. influenzae non-type b (71 or 43 % of all isolates), Strep. pneumoniae (58 or 35 %), M. catarrhalis (13 or 8 %), Strep. pyogenes (12 or 7 %), and Staph. aureus (13 or 8 %). Significant statistical differences were noted in the rates of recovery of H. influenzae non-type b (P<0.05) and Strep. pneumoniae (P<0.05).
A decrease occurred in the recovery of Strep. pneumoniae resistant to penicillin (total number of penicillin-intermediate-susceptible and penicillin-resistant strains) from 41 % between 1997 and 2000 to 29 % between 2000 and 2005 (Table 2). An increase was noted in the isolation of beta-lactamase-producing H. influenzae from 33 % between 1997 and 2000 to 39 % (Table 3). However, neither of these changes was statistically significant.
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Table 2. Susceptibility to penicillin of Strep. pneumoniae recovered in 156 patients with acute maxillary sinusitis between 1997 and 2000, and 229 patients between 2001 and 2005
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Table 3. Beta-lactamase production by H. influenzae recovered in 156 patients with acute maxillary sinusitis between 1997 and 2000, and 229 patients between 2001 and 2005
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DISCUSSION
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These data illustrate that a statistically significant shift occurred in the causative pathogens of acute maxillary sinusitis in adults in the 5 years following the introduction of vaccination of children with the PCV7 compared to the previous 4 years. While the proportion of Strep. pneumoniae declined by 11 %, the proportion of H. influenzae increased by 6 %. A small (not statistically significant) increase also took place in the isolation of other pathogens (M. catarrhalis, Strep. pyogenes and Staph. aureus), which accounted for 18 % of the isolates between 1997 and 2000, and increased to 23 % between 2001 and 2005. Although there was a 12 % decrease in the resistance of Strep. pneumoniae to penicillin and a 6 % increase in the recovery of beta-lactamase-producing H. influenzae, these changes were not statistically significant.
The significant changes in the recovery of sinusitis pathogens in adults as a result of the introduction of the Strep. pneumoniae conjugated vaccine to children younger than 2 years may be due to indirect or herd immunity in adults. Our findings are in concordance with previous studies in Israel that observed an overall reduction in colonization by vaccine-type Strep. pneumoniae in the community due to herd immunity (Dagan, 2004). The use of PCV7 was found to reduce nasopharyngeal acquisition of vaccine-specific serotypes of Strep. pneumoniae, which in turn reduced the incidence of pneumococcal disease among vaccinated as well as non-vaccinated individuals. Since most antibiotic resistance in Strep. pneumoniae is confined to vaccine-type serotypes, vaccine use also reduces antibiotic resistance (Givon-Lavi et al., 2003; O'Brien & Dagan, 2003). Since we did not identify the serotypes of the Strep. pneumoniae isolates, we could not determine whether there was a change in the recovery of these serotypes after 2001.
A shift in the frequency of recovery of causative pathogens was recently demonstrated in children with AOM (Casey & Pichichero, 2004; Block et al., 2004). Casey & Pichichero (2004) determined whether a change occurred in the frequency and distribution of the causative pathogens in persistent AOM after the introduction of the pneumococcal conjugate vaccine in 2000. In a 9-year period between 1995 to 2003 they evaluated 551 children with AOM who had not responded to or failed amoxycillin treatment. The rate of recovery of Strep. pneumoniae declined from 44 % prior to 2001 to 31 % after that time, while the isolation of H. influenzae increased from 43 to 57 %. Fewer Strep. pneumoniae isolates were penicillin resistant and more H. influenzae isolates became beta-lactamase producing.
Block et al. (2004) determined the changes in the microbiology of AOM before and after community-wide implementation of PCV7. They compared 336 AOM isolates from 1992 to 1998 with 83 AOM isolates from 2000 to 2003 in children who had received three or four doses of PCV7. The proportion of Strep. pneumoniae decreased from 48 to 31 % (P=0.009), and nontypable H. influenzae increased from 41 to 56 % (P=0.01); the increase in beta-lactamase-positive H. influenzae, 56 versus 64 %, was not significant. The proportions of intermediate penicillin non-susceptible pneumococci (PNSP) and resistant PNSP were 16 and 9 % versus 13 and 6 % pre- and post-PCV7, respectively. Post-PCV7, Gram-negative bacteria and beta-lactamase-producing organisms accounted for two-thirds and one-half of all AOM isolates, respectively.
Further studies are needed to ascertain the continuous effects of PCV7 on the bacterial causes of acute sinusitis. It is important to carefully monitor the bacterial causes of sinusitis and whether replacement with potential virulent organisms and development of antibiotic resistance in non-vaccine-type pneumococci will occur over time.
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ACKNOWLEDGEMENTS
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The authors acknowledge the statistical analysis by William E. Jackson.
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REFERENCES
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Block, S. L., Hedrick, J., Harrison, C. J., Tyler, R., Smith, A., Findlay, R. & Keegan, E. (2004). Community-wide vaccination with the heptavalent pneumococcal conjugate significantly alters the microbiology of acute otitis media. Pediatr Infect Dis J 23, 829–833.[Medline]
Brook, I. (2005). Microbiology and antimicrobial management of sinusitis. J Laryngol Otol 119, 251–258.[CrossRef][Medline]
Brook, I. & Gober, A. E. (2004). Antimicrobial resistance in the nasopharyngeal flora of children with acute maxillary sinusitis and maxillary sinusitis recurring after amoxicillin therapy. J Antimicrob Chemother 53, 399–402.[Abstract/Free Full Text]
Brook, I., Frazier, E. H. & Foote, P. A. (1996). Microbiology of the transition from acute to chronic maxillary sinusitis. J Med Microbiol 45, 372–375.[Abstract]
Casey, J. R. & Pichichero, M. E. (2004). Changes in frequency and pathogens causing acute otitis media in 1995–2003. Pediatr Infect Dis J 23, 824–828.[Medline]
Craig, W. A. & Andes, D. (1996). Pharmacokinetics and pharmacodynamics of antibiotics in otitis media. Pediatr Infect Dis J 15, 255–259.[CrossRef][Medline]
Dagan, R. (2004). The potential effect of widespread use of pneumococcal conjugate vaccines on the practice of pediatric otolaryngology: the case of acute otitis media. Curr Opin Otolaryngol Head Neck Surg 12, 488–494.[CrossRef][Medline]
Givon-Lavi, N., Fraser, D. & Dagan, R. (2003). Vaccination of day-care center attendees reduces carriage of Streptococcus pneumoniae among their younger siblings. Pediatr Infect Dis J 22, 524–532.[Medline]
Murray, P. R., Barron, E. J., Pfaller, M. A., Tenover, F. C. & Yolken, R. H. (1995). Manual of Clinical Microbiology, 6th edn. Washington, DC: American Society for Microbiology.
National Committee for Clinical Laboratory Standards (1995). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 4th edn. NCCLS document M7-A4. Villanova, PA: National Committee for Clinical Laboratory Standards.
National Committee for Clinical Laboratory Standards (2000). MIC testing supplemental tables (M 100-S10). Wayne, PA: National Committee for Clinical Laboratory Standards.
O'Brien, K. L. & Dagan, R. (2003). The potential indirect effect of conjugate pneumococcal vaccines. Vaccine 21, 1815–1825.[CrossRef][Medline]
O'Callaghan, D. H., Morris, A., Kirby, S. M. & Shingler, A. H. (1972). Novel method for detection of beta-lactamase by using a chromogenic cephalosporin substrate. Antimicrob Agents Chemother 1, 283–288.[Abstract/Free Full Text]
Pichichero, M. E. & Pichichero, C. L. (1995). Persistent otitis media: I causative pathogen. Pediatr Infect Dis J 14, 178–183.[Medline]
Sinus and Allergy Health Partnership (2004). Antimicrobial treatment guidelines for acute bacterial rhinosinusitis. Otolaryngol Head Neck Surg 130 (supplement 1), 1–45.[Medline]
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INTRODUCTION
METHODS
