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. 1999 Feb;43(2):385–389. doi: 10.1128/aac.43.2.385

Haemophilus influenzae and Moraxella catarrhalis from Patients with Community-Acquired Respiratory Tract Infections: Antimicrobial Susceptibility Patterns from the SENTRY Antimicrobial Surveillance Program (United States and Canada, 1997)

Gary V Doern 1,*, Ronald N Jones 1, Michael A Pfaller 1, Kari Kugler 1; The Sentry Participants Group1
PMCID: PMC89085  PMID: 9925540

Abstract

Between February and June of 1997, a large number of community-acquired respiratory tract isolates of Haemophilus influenzae (n = 1,077) and Moraxella catarrhalis (n = 503) from 27 U.S. and 7 Canadian medical centers were characterized as part of the SENTRY Antimicrobial Surveillance Program. Overall prevalences of β-lactamase production were 33.5% in H. influenzae and 92.2% in M. catarrhalis with no differences noted between isolates recovered in the United States and those from Canada. Among a total of 21 different antimicrobial agents tested, including six cephalosporins, a β-lactamase inhibitor combination, three macrolides, tetracycline, trimethoprim-sulfamethoxazole (TMP-SMX), rifampin, chloramphenicol, five fluoroquinolones, and quinupristin-dalfopristin, resistance rates of >5% with H. influenzae were observed only with cefaclor (12.8%) and TMP-SMX (16.2%).

The empiric management of community-acquired respiratory tract infections such as otitis media, sinusitis, acute purulent exacerbation of chronic bronchitis, and community-acquired pneumonia has been complicated by the emergence of high rates of antimicrobial resistance in three major pathogens: Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis. Of these, only S. pneumoniae has been the focus of numerous recent studies, perhaps because of its greater virulence and the fact that antimicrobial resistance in this pneumococcus has reached extraordinary levels over a very short period in North America (1, 2, 7, 12, 26). However, H. influenzae and M. catarrhalis remain a problem in the context of antimicrobial resistance.

At least 11 systematic, nationwide surveillance studies of antimicrobial resistance in H. influenzae have been conducted in North America during the past 15 years, eight in the United States (2, 6, 9, 10, 17, 18, 23, 30) and three in Canada (24, 25, 27). The earliest of these studies, performed from 1983 to 1984, characterized 3,356 clinical isolates of H. influenzae from 22 U.S. medical centers and revealed an overall prevalence of β-lactamase-mediated ampicillin resistance of 15.2% (9). The two most recent studies, both conducted in the United States from 1994 to 1995, revealed overall rates of β-lactamase production of 35.6% among 1,605 isolates from 30 centers and 36.1% among 2,278 strains from 187 institutions (6, 17). In general, the prevalences of β-lactamase-producing isolates of H. influenzae in the United States and Canada have been roughly comparable. Resistance to other antimicrobial agents such as the cephalosporins, β-lactamase inhibitor combinations, macrolides, tetracycline, chloramphenicol, trimethoprim-sulfamethoxazole (TMP-SMX), and the fluoroquinolones has remained relatively uncommon with H. influenzae in North America (2, 6, 17, 30).

β-Lactamase-mediated resistance to penicillins in M. catarrhalis is even more common than in H. influenzae. Four large, multicenter, national surveillance studies conducted in the United States during the 1990s revealed an overall rate of β-lactamase production in M. catarrhalis of between 90.1 and 96.8% (2, 8, 18, 30). Resistance to other antimicrobials has not emerged as a significant problem with this organism.

The question arises: what is the current prevalence of antimicrobial resistance in respiratory tract isolates of H. influenzae and M. catarrhalis in North America? In an attempt to answer this question, a 5-month, multicenter surveillance study was performed in the United States and Canada during 1997. This investigation was conducted as part of the SENTRY Antimicrobial Surveillance Program, a prospective, longitudinal, multinational study aimed at tracking the emergence of antimicrobial resistance worldwide.

During the 5-month period from February through June 1997, a total of 837 isolates of H. influenzae and 374 isolates of M. catarrhalis were recovered in the clinical microbiology laboratories of 27 medical centers in the United States (Table 1). A total of 240 isolates of H. influenzae and 129 isolates of M. catarrhalis were recovered in the laboratories of seven Canadian hospitals during the same period (Table 1). All isolates were transported to the coordinating laboratory, the University of Iowa College of Medicine (Iowa City), where stock cultures were prepared in defibrinated rabbit blood and frozen at −70°C. Only organisms judged to be the cause of defined respiratory tract infections in outpatients were included in this study. Criteria in place at individual laboratories were used to assess clinical significance. Frozen isolates were thawed and subcultured twice on 5% sheep blood agar plates prior to further characterization.

TABLE 1.

β-Lactamase-mediated ampicillin resistance among respiratory tract isolates of H. influenzae and M. catarrhalis from U.S. and Canadian medical centers

Country Site H. influenzae
M. catarrhalis
No. of isolates % β-Lactamase positive No. of isolates % β-Lactamase positive
United States Veterans Administration Medical Center, Boston, Mass. 35 20.0 18 88.9
Columbia Presbyterian Medical Center, New York, N.Y. 37 29.7 15 93.3
Long Island Jewish Medical Center, New Hyde Park, N.Y. 31 25.8 7 100.0
Strong Memorial Hospital, Rochester, N.Y. 39 43.6 19 89.5
The Medical Center of Delaware, Wilmington 32 43.8 19 84.2
University of Virginia Health Sciences Center, Charlottesville 16 37.5 5 100.0
Carolinas Medical Center, Charlotte, N.C. 40 37.5 19 89.5
University Medical Center, Jacksonville, Fla. 37 27.0 20 85.0
University of Mississippi Medical Center, Jackson 21 38.1 9 100.0
University of Louisville Hospital, Louisville, Ky. 33 30.3 20 95.0
Summa Health Systems, Akron, Ohio 37 32.4 6 66.7
Henry Ford Hospital, Detroit, Mich. 38 47.4 15 93.3
Methodist Hospital of Indiana, Indianapolis 39 23.1 16 87.5
Northwestern Memorial Hospital, Chicago, Ill. 15 33.3 4 100.0
University of Illinois Hospital, Chicago 22 50.0 10 90.0
Froedtert Memorial Lutheran Hospital, Milwaukee, Wis. 40 37.5 10 70.0
Barnes-Jewish Hospital, St. Louis, Mo. 21 23.8 10 80.0
University of Iowa Hospitals and Clinics, Iowa City 35 48.6 20 100.0
Creighton University Medical Center, Omaha, Nebr. 37 29.7 18 88.9
Parkland Health & Hospital System, Dallas, Tex. 9 11.1 7 85.7
University of Texas Medical Branch at Galveston, Galveston 24 33.3 21 100.0
Denver General Hospital, Denver, Colo. 29 34.5 4 66.7
University of New Mexico Hospital, Albuquerque 39 38.5 10 100.0
St. Jude Medical Center, Fullerton, Calif. 36 30.6 11 100.0
Kaiser Regional Laboratory, Berkeley, Calif. 31 35.5 17 100.0
Sacred Heart Medical Center, Spokane, Wash. 33 18.2 21 95.2
University of Washington, Seattle 25 48.0 10 100.0
Subtotal (United States) 837 34.2 374 92.0
Canada Queen Elizabeth II Health Sciences Centre, Halifax, Nova Scotia 39 48.7 21 85.7
Royal Victoria Hospital, Montreal, Quebec 34 23.5 16 75.0
Ottawa General Hospital, Ottawa, Ontario 38 21.1 20 100.0
Mount Sinai Hospital, Toronto, Ontario 19 26.3 20 100.0
The Hospital for Sick Children, Toronto, Ontario 37 37.8 17 100.0
Health Sciences Centre, Winnipeg, Manitoba 35 28.6 23 95.7
University of Alberta Hospital Site, Edmonton 38 28.9 12 91.7
Subtotal (Canada) 240 31.3 129 93.0
Grand total 1,077 33.5 503 92.2
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At the coordinating study center, the identity of isolates was confirmed by using conventional criteria (4, 20) and the MICs of 21 antimicrobial agents were determined by a reference broth microdilution method (21). The following antimicrobials were tested: amoxicillin, amoxicillin-clavulanate, cefaclor, cefuroxime, cefixime, cefpodoxime, cefotaxime, cefepime, azithromycin, clarithromycin, erythromycin, chloramphenicol, tetracycline, TMP-SMX, rifampin, ciprofloxacin, levofloxacin, gatifloxacin, sparfloxacin, trovafloxacin, and quinupristin-dalfopristin. Dehydrated microdilution trays were obtained commercially (Dade-MicroScan, Inc., Sacramento, Calif.). Drugs were tested over concentration ranges that yielded on-scale MICs with >98% of organism-antimicrobial combinations. Haemophilus test medium broth, 100 μl per well, was employed as a growth medium for H. influenzae during MIC determinations (11, 19, 21). Cation-adjusted Mueller-Hinton broth, 100 μl per well, was used in MIC determinations for M. catarrhalis (21). The final inoculum concentration was approximately 5 × 105 CFU/ml. Trays were incubated for 20 to 24 h at 35°C in ambient air prior to MIC determinations. MICs were defined as the lowest concentration of drug that yielded no visible evidence of growth of the test organism. H. influenzae ATCC 49247 and ATCC 49766 were used as control organisms throughout this study. Production of β-lactamase was assessed by use of the Cefinase disk test (Becton Dickinson Microbiology Systems, Cockeysville, Md.).

A total of 1,077 isolates of H. influenzae were characterized, 837 from 27 U.S. medical centers and 240 from seven Canadian institutions (Table 1). The overall prevalences of β-lactamase-producing strains were 34.2% in the United States and 31.3% in Canada (P = 0.09). Collectively in North America, 33.5% of respiratory tract isolates of H. influenzae produced β-lactamase. Among centers with at least 20 isolates, rates of β-lactamase production varied between 18.2 and 50.0% (Table 1).

Results of MIC determinations with 14 selected antimicrobial agents against this collection of H. influenzae are summarized in Table 2. Isolates from U.S. and Canadian medical centers were grouped together for purposes of this analysis because when they were analyzed separately, no significant differences were noted between the two countries (data not shown). Among β-lactam agents, resistance was not detected with cefixime (MIC at which 90% of the isolates are inhibited [MIC90], 0.12 μg/ml), cefpodoxime (MIC90, 0.25 μg/ml), cefotaxime (MIC90, 0.06 μg/ml), and cefepime (MIC90, 0.25 μg/ml). Resistance was uncommon with amoxicillin-clavulanate (0.2% of isolates) and cefuroxime (1.5%). Resistance among β-lactams was most common with cefaclor (12.8%). Resistance was also uncommon with selected non-β-lactam antimicrobial agents, i.e., azithromycin (0.2%), clarithromycin (3.9%), chloramphenicol (0.7%), tetracycline (0.9%), and rifampin (0.1%). In contrast, 16.2% of H. influenzae isolates were resistant to TMP-SMX.

TABLE 2.

In vitro activities of 14 antimicrobial agents against 1,077 respiratory tract isolates of H. influenzae from North American medical centers

Antimicrobial agent MIC (μg/ml)
% by categorya
Breakpointa
50% 90% Range Mode Susceptible Resistant Susceptible Resistant
Amoxicillin-clavulanate 0.5 2 ≤0.06–16 0.25–2 99.8 0.2 ≤4/2 ≥8/4
Cefaclor 2 32 ≤0.25–>32 2 79.6 12.8 ≤8 ≥32
Cefuroxime 0.5 2 ≤0.06–16 0.5 95.7 1.5 ≤4 ≥16
Cefixime ≤0.03 0.12 ≤0.03–1 ≤0.03 100.0 ≤1
Cefpodoxime 0.06 0.25 ≤0.03–1 0.06 100.0 ≤2
Cefotaxime 0.015 0.06 ≤0.008–0.5 0.015 100.0 ≤2
Cefepime 0.12 0.25 ≤0.06–2 0.12 100.0 ≤2
Azithromycin 2 2 ≤0.12–>16 2 99.8 0.2 ≤4
Clarithromycin 8 16 ≤0.25–>32 8 61.4 3.9 ≤8 ≥32
Erythromycin 4 8 ≤0.25–>32 4
Chloramphenicol ≤2 ≤2 ≤2–>16 ≤2 99.0 0.7 ≤2 ≥8
Tetracycline ≤2 ≤2 ≤2–>16 ≤2 98.6 0.9 ≤2 ≥8
TMP-SMX ≤0.25 8 ≤0.25–>8 ≤0.25 77.3 16.2 ≤0.5 ≥4
Rifampin ≤1 ≤1 ≤1–>2 ≤1 95.7 0.1 ≤1 ≥4
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a

Breakpoints are those advocated by the NCCLS for use in MIC determinations with H. influenzae (17). 

Among the five fluoroquinolones examined in this study, i.e., ciprofloxacin, levofloxacin, sparfloxacin, trovafloxacin, and gatifloxacin, a nearly uniform activity was observed for study strains of H. influenzae for which the MIC50s, MIC90s, and modal MICs were ≤0.06 μg/ml. The highest MIC obtained with any of these agents was 0.25 μg/ml (data not shown). The combination quinupristin-dalfopristin was characterized by a MIC50, MIC90, and modal MIC of 4, 8, and 4 μg/ml, respectively.

Amoxicillin MICs for all of the 361 β-lactamase-producing isolates in this study were ≥4 μg/ml; for only 1 of 716 β-lactamase-negative isolates (i.e., 0.1%) was the amoxicillin MIC 8 μg/ml, indicating resistance. The amoxicillin-clavulanate MIC for this isolate was 8/4 μg/ml. Two β-lactamase-positive isolates of H. influenzae (i.e., 0.2%) that were resistant to amoxicillin-clavulanate (MICs of ≥8/4 μg/ml) were recovered in this study. The amoxicillin-clavulanate MICs for these two strains were confirmed by repeat testing. Other than amoxicillin, of the antimicrobial agents examined in this study, only cefaclor activity appeared to be adversely influenced by β-lactamase-production in H. influenzae. The following cefaclor MICs were obtained with β-lactamase-positive and -negative strains, respectively: MIC50s, 8 and 2 μg/ml; MIC90s, >32 and 8 μg/ml; modal MICs, 8 and 2 μg/ml; susceptibility rates, 54.0 and 92.5%; and resistance rates, 32.7 and 2.5%. Essentially comparable in vitro activity was noted with all other agents when the results obtained with these agents were compared with β-lactamase-positive and β-lactamase-negative strains (data not shown).

A total of 503 isolates of M. catarrhalis were characterized in this study, 374 from the United States and 129 from Canada (Table 1). The overall prevalence of β-lactamase production was 92.2% and very uniform between the two countries, i.e., 92.0% in the United States and 93.0% in Canada. MICs are listed for 14 selected antimicrobial agents in Table 3. All of these compounds were consistently active against this collection of M. catarrhalis isolates. In addition, the five fluoroquinolones examined in this study were uniformly active against M. catarrhalis at very low concentrations. The MIC90s of these agents were as follows: ciprofloxacin, ≤0.03 μg/ml; levofloxacin, ≤0.05; gatifloxacin, ≤0.03 μg/ml; sparfloxacin, ≤0.12 μg/ml; and trovafloxacin, ≤0.03 μg/ml. The highest MICs obtained with each of these fluoroquinolones were 1, 2, 1, 0.5, and 0.5 μg/ml, respectively (data not shown). The MIC50 and MIC90 of quinupristin-dalfopristin were both 0.5 μg/ml (range, ≤0.06 to >8 μg/ml).

TABLE 3.

In vitro activities of 14 antimicrobial agents against 503 respiratory tract isolates of M. catarrhalis from North American medical centers

Antimicrobial agent MIC (μg/ml)
% by categorya
Breakpointa
50% 90% Range Mode Susceptible Resistant Susceptible Resistant
Amoxicillin-clavulanate 0.12 0.25 ≤0.06–4 0.25 100.0 0.0 ≤8/4  ≥16/8  
Cefaclor 1 2 ≤0.25–32 0.50 99.6 0.2 ≤8 ≥32
Cefuroxime 1 2 0.12–8 1 99.2 0.0 ≤4 ≥32
Cefixime 0.25 0.5 ≤0.03–2 0.25 99.4 0.0 ≤1 ≥4
Cefpodoxime 1 2 ≤0.03–>4 1 99.0 0.2 ≤2 ≥8
Cefotaxime 0.5 1 ≤0.008–2 0.5 100.0 0.0 ≤8 ≥64
Cefepime 1 4 ≤0.06–8 1 100.0 0.0 ≤8 ≥32
Azithromycin ≤0.12 ≤0.12 ≤0.12–0.25 ≤0.12 100.0 0.0 ≤2 ≥8
Clarithromycin ≤0.25 ≤0.25 ≤0.25–1 ≤0.25 100.0 0.0 ≤2 ≥8
Erythromycin ≤0.25 0.5 ≤0.25–1 ≤0.25 99.0 0.0 ≤0.5 ≥8
Chloramphenicol ≤2 ≤2 ≤2 ≤2 100.0 0.0 ≤8 ≥32
Tetracycline ≤2 ≤2 ≤2 ≤2 100.0 0.0 ≤4 ≥16
TMP-SMX ≤0.25 0.5 ≤0.25–8 ≤0.25 99.2 0.2 ≤2/38 ≥8/152
Rifampin ≤1 ≤1 ≤1 ≤1 100.0 0.0 ≤1 ≥4
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a

Breakpoints are those advocated by the NCCLS for use in MIC determinations with nonfastidious bacteria that grow well on unsupplemented Mueller-Hinton medium (17). 

Amoxicillin MICs for the 464 β-lactamase-producing isolates of M. catarrhalis in this study varied substantially (range, ≤0.06 to >8 μg/ml). The number of β-lactamase-positive isolates for which amoxicillin MICs were ≤1, 2, 4, and ≥8 μg/ml were 103 (22.2%), 61 (13.1%), 89 (19.2%), and 211 (45.5%), respectively. By contrast, amoxicillin-clavulanate MICs were ≤1 μg/ml for all 464 β-lactamase-positive isolates.

The results of this survey indicate that the prevalence of β-lactamase production among respiratory tract isolates of H. influenzae (i.e., 33.5%) may have leveled off in North America. Two recent multicenter U.S. surveillance studies which emphasized respiratory tract isolates of H. influenzae, both conducted in 1994 to 1995, revealed overall rates of β-lactamase production of 35.6 and 36.1% (6, 11). As has been observed in previous studies (6, 17, 24, 25, 27), only small differences were noted in the current investigation between the rates of β-lactamase production in the United States (34.2%) and Canada (31.3%). Amoxicillin resistance among β-lactamase-negative strains and amoxicillin-clavulanate resistance among β-lactamase-positive strains, as has been described recently (6), were uncommon in the current survey (i.e., 0.1 and 0.2%, respectively).

Among the 19 other antimicrobial agents examined in this study, only two compounds were characterized by resistance rates greater than 5% in H. influenzae, cefaclor (12.8%) and TMP-SMX (16.2%). With cefaclor, much higher resistance rates were noted in β-lactamase-producing isolates than in organisms that lacked β-lactamase production. The actual clinical implications of these findings remain to be defined. Several recent studies have questioned the clinical predictive value of MICs obtained with oral antimicrobial agents used to treat localized respiratory tract infections caused by H. influenzae (5, 15, 16).

The results of this study corroborate the findings of previous investigators regarding the high prevalence of β-lactamase production among respiratory tract isolates of M. catarrhalis (2, 8, 18, 30). Overall, 92.2% of 503 isolates produced β-lactamase, 92.0% in the United States and 93.0% in Canada. Amoxicillin MICs were ≤1 μg/ml for 22.2% of β-lactamase-producing isolates, which probably would be considered to indicate susceptibility. Similar observations have been made previously with M. catarrhalis and may reflect the fact that some β-lactamase-positive strains produce a BRO-2 enzyme (3, 28, 29). This enzyme is produced in small amounts, remains tightly cell associated, and has a low affinity for aminopenicillins such as ampicillin and amoxicillin. Ampicillin and amoxicillin MICs for BRO-2-producing strains of M. catarrhalis are typically found to be low (3, 28) and represent one example of where production of a β-lactamase does not actually result in ampicillin-amoxicillin resistance. All β-lactamase-producing strains of M. catarrhalis were inhibited by concentrations of ≤4/2 μg of amoxicillin-clavulanate per ml.

The 19 remaining antimicrobial agents examined in this investigation were almost uniformly active against M. catarrhalis (Table 3). The activities of these agents were assessed based on breakpoints advocated by the National Committee for Clinical Laboratory Standards (NCCLS) for use in testing nonfastidious bacteria that grow well on unsupplemented Mueller-Hinton medium, as is the case with M. catarrhalis (13). Two previous studies demonstrated that such breakpoints were applicable to M. catarrhalis (13, 14). Based on these breakpoints, resistance was observed with only three compounds (cefaclor, cefotaxime, and TMP-SMX) and then only with a single isolate each.

In conclusion, in this multicenter, North American surveillance study, 33.5 and 92.2% of community-acquired respiratory tract isolates of H. influenzae and M. catarrhalis, respectively, were found to produce β-lactamase. As a result of β-lactamase production, amoxicillin resistance with these two organisms is common. In contrast, with the exception of cefaclor and TMP-SMX tested against H. influenzae, all of the alternative antimicrobials examined in this investigation were nearly uniformly active against both organisms. Because of the longitudinal nature of the SENTRY Antimicrobial Surveillance Program, we will continue to track the susceptibility trends of both H. influenzae and M. catarrhalis in North America over the next several years.

Acknowledgments

We thank Kay Meyer for excellent secretarial support and Meridith Erwin and Douglas Biedenbach for technical assistance. We also acknowledge Monnie Beach for timely and accurate data analysis. We are indebted to the following individuals at contributing study centers for provision of isolates: Lynn Steele-Moore, The Medical Center Delaware, Wilmington; Gerald Denys, Methodist Hospital of Indiana, Indianapolis; Carol Staley, Henry Ford Hospital, Detroit, Mich.; Joseph R. Dipersio, Summa Health Systems, Akron, Ohio; Michael Saubolle, Good Samaritan Regional Medical Center, Phoenix, Ariz.; Michael L. Wilson, Denver General Hospital, Denver, Colo.; Gary D. Overturf, University of New Mexico Hospital, Albuquerque; Lance R. Peterson, Northwestern Memorial Hospital, Chicago, Ill.; Paul C. Schreckenberger, University of Illinois at Chicago, Chicago; Ronald N. Jones, University of Iowa Hospitals and Clinics, Iowa City; Stephen Cavalieri, Creighton University, Omaha, Nebr.; Sue Kehl, Froedtert Memorial Lutheran Hospital-East, Milwaukee, Wis.; Stephen Brecher, Boston Veterans Administration Medical Center, Boston, Mass.; Phyllis Della-Latta, Columbia Presbyterian Medical Center, New York, N.Y.; Henry Isenberg, Long Island Jewish Medical Center, New Hyde Park, N.Y.; Dwight Hardy, Strong Memorial Hospital, Rochester, N.Y.; Dennis Koga, St. Jude Medical Center, Fullerton, Calif.; Judy Fusco, Kaiser Laboratory, Berkeley, Calif.; Marcy Hoffmann, Sacred Heart Medical Center, Spokane, Wash.; Thomas Fritsche, University of Washington, Seattle; Patrick R. Murray, Barnes-Jewish Hospital, St. Louis, Mo.; Paul Southern, Parkland Health & Hospital System, Dallas, Tex.; Audrey Wanger, The University of Texas Medical School, Houston; Gail L. Woods, University of Texas Medical Branch at Galveston, Galveston; Joseph Chiao, University Medical Center, Jacksonville, Fla.; James Snyder, University of Louisville Hospital, Louisville, Ky.; Joe Humphrey, University of Mississippi Medical Center, Jackson; Steve Jenkins, Carolinas Medical Center, Charlotte, N.C.; Kevin Hazen, University of Virginia Health Sciences Center, Charlottesville; Robert Rennie, University of Alberta Hospital, Edmonton, Canada; Michael Noble, The Vancouver Hospital & Health Science Center, Vancouver, British Columbia, Canada; Daryl Hoban, Health Sciences Centre, Winnipeg, Manitoba, Canada; Keven Forward, Queen Elizabeth II Health Sciences Centre, Halifax, Nova Scotia, Canada; Don Low, Mount Sinai Hospital, Toronto, Ontario, Canada; Baldwin Toye, Ottawa General Hospital, Ottawa, Ontario, Canada; Andrew Simor, Sunnybrook Health Science Centre, Toronto, Ontario, Canada; Susan Richardson, The Hospital for Sick Children, Toronto, Ontario, Canada; Hugh Robson, Royal Victoria Hospital, Montreal, Quebec, Canada; and Joseph Blondeau, Royal University Hospital, Saskatoon, Saskatchewan, Canada.

The SENTRY Antimicrobial Surveillance Program is being conducted under the auspices of a research grant from Bristol-Myers Squibb and Co.

REFERENCES

  • 1.Ballow C H, Jones R N, Johnson D M, Deinhart J A, Schentag J J the SPAR Study Group. Comparative in vitro assessment of sparfloxacin activity and spectrum using results from over 14,000 pathogens isolated at 190 medical centers in the USA. Diagn Microbiol Infect Dis. 1998;29:173–186. doi: 10.1016/s0732-8893(97)81807-x. [DOI] [PubMed] [Google Scholar]
  • 2.Barry A L, Pfaller M A, Fuchs P C, Packer R R. In vitro activities of 12 orally administered antimicrobial agents against four species of bacterial respiratory pathogens from U.S. medical centers in 1992 and 1993. Antimicrob Agents Chemother. 1994;38:2419–2425. doi: 10.1128/aac.38.10.2419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Bootsma H J, van Dijk H, Verhoef J, Fleer A, Mooi F R. Molecular characterization of the BRO β-lactamase of Moraxella (Branhamella) catarrhalis. Antimicrob Agents Chemother. 1996;40:966–972. doi: 10.1128/aac.40.4.966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Campos J M. Haemophilus. In: Murray P R, Baron E J, Pfaller M A, Tenover F C, Yolken R H, editors. Manual of clinical microbiology. 6th ed. Washington, D.C: ASM Press; 1995. pp. 556–565. [Google Scholar]
  • 5.Dagan R, Abramson O, Leibovitz E, Greenberg D, Lang R, Goshen S, Yagupsky P, Leiberman A, Fliss D M. Bacteriologic response to oral cephalosporins: are established susceptibility breakpoints appropriate in the case of acute otitis media? J Infect Dis. 1997;176:1253–1259. doi: 10.1086/514120. [DOI] [PubMed] [Google Scholar]
  • 6.Doern G V, Brueggemann A B, Pierce G, Holley H P, Jr, Rauch A. Antibiotic resistance among clinical isolates of Haemophilus influenzae in the United States in 1994 and 1995 and detection of β-lactamase-positive strains resistant to amoxicillin-clavulanate: results of a national multicenter surveillance study. Antimicrob Agents Chemother. 1997;41:292–297. doi: 10.1128/aac.41.2.292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Doern G V, Brueggemann A, Holley H P, Jr, Rauch A M. Antimicrobial resistance of Streptococcus pneumoniae recovered from outpatients in the United States during the winter months of 1994 to 1995: results of a 30-center national surveillance study. Antimicrob Agents Chemother. 1996;40:1208–1213. doi: 10.1128/aac.40.5.1208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Doern G V, Brueggemann A B, Pierce G, Hogan T, Holley H P, Jr, Rauch A. Prevalence of antimicrobial resistance among 723 outpatient clinical isolates of Moraxella catarrhalis in the United States in 1994 and 1995: results of a 30-center national surveillance study. Antimicrob Agents Chemother. 1996;40:2884–2886. doi: 10.1128/aac.40.12.2884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Doern G V, Jorgensen J H, Thornsberry C, Preston D A the Haemophilus influenzae Surveillance Group. Prevalence of antimicrobial resistance among clinical isolates of Haemophilus influenzae: a collaborative study. Diagn Microbiol Infect Dis. 1986;4:95–107. doi: 10.1016/0732-8893(86)90143-4. [DOI] [PubMed] [Google Scholar]
  • 10.Doern G V, Jorgensen J H, Thornsberry C, Preston D A, Tubert T, Redding J S, Maher L A. National collaborative study of the prevalence of antimicrobial resistance among clinical isolates of Haemophilus influenzae. Antimicrob Agents Chemother. 1988;32:180–185. doi: 10.1128/aac.32.2.180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Doern G V, Jorgensen J H, Thornsberry C, Snapper H. Disk diffusion susceptibility testing of Haemophilus influenzae using haemophilus test medium. Eur J Clin Microbiol Infect Dis. 1990;9:329–336. doi: 10.1007/BF01973739. [DOI] [PubMed] [Google Scholar]
  • 12.Doern, G. V., M. A. Pfaller, K. Kugler, J. Freeman, and R. N. Jones. Prevalence of antimicrobial resistance among respiratory tract isolates of Streptococcus pneumoniae in North America: 1997 results from the SENTRY Antimicrobial Surveillance Program. Clin. Infect. Dis., in press. [DOI] [PubMed]
  • 13.Doern G V, Tubert T. Disk diffusion susceptibility testing of Branhamella catarrhalis with ampicillin and seven other antimicrobial agents. Antimicrob Agents Chemother. 1987;31:1519–1523. doi: 10.1128/aac.31.10.1519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Doern G V, Tubert T. In vitro activities of 39 antimicrobial agents for Branhamella catarrhalis and comparison of results with different quantitative susceptibility test methods. Antimicrob Agents Chemother. 1988;32:259–261. doi: 10.1128/aac.32.2.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Doern, G. V. 1992. In vitro activity of loracarbef and effects of susceptibility test methods. Am. J. Med. 92(Suppl. 6A):6A–7S. [DOI] [PubMed]
  • 16.Doern G V. Does there exist a rational, objective in vitro basis for the management of selected infections of the respiratory tract? Infect Dis Clin Pract. 1994;3:75–80. [Google Scholar]
  • 17.Jones R N, Jacobs M R, Washington J A, Pfaller M A. A 1994–95 survey of Haemophilus influenzae susceptibility to ten orally administered agents. A 187 clinical laboratory center sample in the United States. Diagn Microbiol Infect Dis. 1997;27:75–83. doi: 10.1016/s0732-8893(96)00219-2. [DOI] [PubMed] [Google Scholar]
  • 18.Jorgensen J H, Doern G V, Maher L A, Howell A W, Redding J S. Antimicrobial resistance among respiratory isolates of Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae in the United States. Antimicrob Agents Chemother. 1990;34:2075–2080. doi: 10.1128/aac.34.11.2075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Jorgensen J H, Redding J S, Maher L A, Howell A W. Improved medium for antimicrobial susceptibility testing of Haemophilus influenzae. J Clin Microbiol. 1987;25:2105–2113. doi: 10.1128/jcm.25.11.2105-2113.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Knapp J S, Rice R J. Neisseria and Branhamella. In: Murray P R, Baron E J, Pfaller M A, Tenover F C, Yolken R H, editors. Manual of clinical microbiology. 6th ed. Washington, D.C: ASM Press; 1995. pp. 324–340. [Google Scholar]
  • 21.National Committee for Clinical Laboratory Standards. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. 4th ed. Approved standard M7-A4. Wayne, Pa: National Committee for Clinical Laboratory Standards; 1997. [Google Scholar]
  • 22.National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility testing. Eighth informational supplement M100-S8. Wayne, Pa: National Committee for Clinical Laboratory Standards; 1998. [Google Scholar]
  • 23.Rittenhouse S F, Miller L A, Kaplan R L, Mosely G H, Poupard J A. A survey of β-lactamase-producing Haemophilus influenzae. An evaluation of 5750 isolates. Diagn Microbiol Infect Dis. 1995;21:223–225. doi: 10.1016/0732-8893(95)00028-9. [DOI] [PubMed] [Google Scholar]
  • 24.Scriver S R, Low D E, Simor A E, Toye B, McGeer A, Jaeger R Canadian Haemophilus Study Group. Broth microdilution testing of Haemophilus influenzae with haemophilus test medium versus lysed horse blood broth. J Clin Microbiol. 1992;30:2284–2289. doi: 10.1128/jcm.30.9.2284-2289.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Scriver S R, Walmsley S L, Kau C L, Hoban D J, Brunton J, McGeer A, Moore T C, Witwicki E, Low D E Canadian Haemophilus Study Group. Determination of antimicrobial susceptibilities of Canadian isolates of Haemophilus influenzae and characterization of their β-lactamases. Antimicrob Agents Chemother. 1994;38:1678–1680. doi: 10.1128/aac.38.7.1678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Thornsberry C, Burton P H, Vanderhoof B H. Activity of penicillin and three third-generation cephalosporins against US isolates of Streptococcus pneumoniae: a 1995 surveillance study. Diagn Microbiol Infect Dis. 1996;25:89–95. doi: 10.1016/s0732-8893(96)00098-3. [DOI] [PubMed] [Google Scholar]
  • 27.Tremblay L D, L’Ecuyer J, Provencher P, Bergeron M G Canadian Haemophilus Study Group. Susceptibility of Haemophilus influenzae to antimicrobial agents used in Canada. Can Med Assoc J. 1990;143:895. [PMC free article] [PubMed] [Google Scholar]
  • 28.Wallace R J, Jr, Nash D R, Steingrube V A. Antibiotic susceptibilities and drug resistance in Moraxella (Branhamella) catarrhalis. Am J Med. 1990;88:5A–46S. doi: 10.1016/0002-9343(90)90262-c. [DOI] [PubMed] [Google Scholar]
  • 29.Wallace R J, Jr, Steingrube V A, Nash D R, Hollis D G, Flanagan C, Brown B A, Labidi A, Weaver R E. BRO β-lactamases of Branhamella catarrhalis and Moraxella subgenus Moraxella, including evidence for chromosomal β-lactamase transfer by conjugation in B. catarrhalis, M. nonliquefaciens, and M. lacunata. Antimicrob Agents Chemother. 1989;33:1845–1854. doi: 10.1128/aac.33.11.1845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Washington J A the Alexander Project Group. A multicenter study of the antimicrobial susceptibility of community-acquired lower respiratory tract pathogens in the United States, 1992–1994. The Alexander Project. Diagn Microbiol Infect Dis. 1996;25:183–190. doi: 10.1016/s0732-8893(96)00128-9. [DOI] [PubMed] [Google Scholar]

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