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Antimicrobial Agents and Chemotherapy, February 1999, p. 385-389, Vol. 43, No. 2
Medical Microbiology Division, Department of
Pathology, University of Iowa College of Medicine, Iowa City, Iowa
Received 13 April 1998/Returned for modification 28 July
1998/Accepted 31 October 1998
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
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 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
0066-4804/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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)
ABSTRACT
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-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 -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%).
TEXT
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-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
-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 -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, -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).
-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 -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.
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.
-Lactamase-mediated ampicillin resistance among
respiratory tract isolates of H. influenzae and
M. catarrhalis from U.S. and Canadian medical centers
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 -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
-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 -lactamase. Among centers with at least 20 isolates, rates of -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 -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
-lactams was most common with cefaclor (12.8%). Resistance was also
uncommon with selected non--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.
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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 -lactamase-producing isolates in
this study were 
4 µg/ml; for only 1 of 716 -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 -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 -lactamase-production in
H. influenzae. The following cefaclor MICs were
obtained with -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
-lactamase-positive and -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 -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).
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Amoxicillin MICs for the 464 -lactamase-producing isolates of
M. catarrhalis in this study varied substantially
(range, 0.06 to >8 µg/ml). The number of -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 -lactamase-positive isolates.
The results of this survey indicate that the prevalence of
-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 -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 -lactamase production in the
United States (34.2%) and Canada (31.3%). Amoxicillin resistance among -lactamase-negative strains and amoxicillin-clavulanate resistance among -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
-lactamase-producing isolates than in organisms that lacked -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 -lactamase production
among respiratory tract isolates of M. catarrhalis (2, 8, 18, 30). Overall, 92.2% of 503 isolates
produced -lactamase, 92.0% in the United States and 93.0% in
Canada. Amoxicillin MICs were 1 µg/ml for 22.2% of
-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
-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 -lactamase does not actually result in
ampicillin-amoxicillin resistance. All -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 -lactamase. As a result of
-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.
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ACKNOWLEDGMENTS |
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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.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Pathology, C606 GH, University of Iowa College of Medicine, Iowa City, IA 52242. Phone: (319) 356-8616. Fax: (319) 356-4916. E-mail: gary-doern{at}uiowa.edu.
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Antimicrobial Agents and Chemotherapy, February 1999, p. 385-389, Vol. 43, No. 2
0066-4804/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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45: 4051-4053
[Abstract] [Full Text] -
Hotomi, M., Fujihara, K., Billal, D. S., Suzuki, K., Nishimura, T., Baba, S., Yamanaka, N.
(2007). Genetic Characteristics and Clonal Dissemination of {beta}-Lactamase-Negative Ampicillin-Resistant Haemophilus influenzae Strains Isolated from the Upper Respiratory Tract of Patients in Japan. Antimicrob. Agents Chemother.
51: 3969-3976
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Jain, A., Kumar, P., Awasthi, S.
(2006). High ampicillin resistance in different biotypes and serotypes of Haemophilus influenzae colonizing the nasopharynx of healthy school-going Indian children. J Med Microbiol
55: 133-137
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Cober, M. P., Johnson, C. E
(2005). Otitis Media: Review of the 2004 Treatment Guidelines. The Annals of Pharmacotherapy
39: 1879-1887
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Heilmann, K. P., Rice, C. L., Miller, A. L., Miller, N. J., Beekmann, S. E., Pfaller, M. A., Richter, S. S., Doern, G. V.
(2005). Decreasing Prevalence of {beta}-Lactamase Production among Respiratory Tract Isolates of Haemophilus influenzae in the United States. Antimicrob. Agents Chemother.
49: 2561-2564
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Capparelli, E. V., Reed, M. D., Bradley, J. S., Kearns, G. L., Jacobs, R. F., Damle, B. D., Blumer, J. L., Grasela, D. M.
(2005). Pharmacokinetics of Gatifloxacin in Infants and Children. Antimicrob. Agents Chemother.
49: 1106-1112
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Subcommittee on Management of Acute Otitis Media,
(2004). Diagnosis and Management of Acute Otitis Media. Pediatrics
113: 1451-1465
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Morikawa, Y., Kitazato, M., Mitsuyama, J., Mizunaga, S., Minami, S., Watanabe, Y.
(2004). In Vitro Activities of Piperacillin against {beta}-Lactamase-Negative Ampicillin-Resistant Haemophilus influenzae. Antimicrob. Agents Chemother.
48: 1229-1234
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Low, D. E., Pichichero, M. E., Schaad, U. B.
(2004). Optimizing Antibacterial Therapy for Community-Acquired Respiratory Tract Infections in Children in an Era of Bacterial Resistance. CLIN PEDIATR
43: 135-151
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Morrissey, I., Tillotson, G.
(2004). Activity of gemifloxacin against Streptococcus pneumoniae and Haemophilus influenzae. J Antimicrob Chemother
53: 144-148
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Galan, J.-C., Morosini, M.-I., Baquero, M.-R., Reig, M., Baquero, F.
(2003). Haemophilus influenzae blaROB-1 Mutations in Hypermutagenic {Delta}ampC Escherichia coli Conferring Resistance to Cefotaxime and {beta}-Lactamase Inhibitors and Increased Susceptibility to Cefaclor. Antimicrob. Agents Chemother.
47: 2551-2557
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Zhanel, G. G., Palatnick, L., Nichol, K. A., Low, D. E., The CROSS Study Group,, , Hoban, D. J.
(2003). Antimicrobial Resistance in Haemophilus influenzae and Moraxella catarrhalis Respiratory Tract Isolates: Results of the Canadian Respiratory Organism Susceptibility Study, 1997 to 2002. Antimicrob. Agents Chemother.
47: 1875-1881
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Levy, R. M., Huang, E. Y., Roling, D., Leyden, J. J., Margolis, D. J.
(2003). Effect of Antibiotics on the Oropharyngeal Flora in Patients With Acne. Arch Dermatol
139: 467-471
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Dabernat, H., Delmas, C., Seguy, M., Pelissier, R., Faucon, G., Bennamani, S., Pasquier, C.
(2002). Diversity of {beta}-Lactam Resistance-Conferring Amino Acid Substitutions in Penicillin-Binding Protein 3 of Haemophilus influenzae. Antimicrob. Agents Chemother.
46: 2208-2218
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Schmitz, F.-J., Beeck, A., Perdikouli, M., Boos, M., Mayer, S., Scheuring, S., Kohrer, K., Verhoef, J., Fluit, A. C.
(2002). Production of BRO {beta}-Lactamases and Resistance to Complement in European Moraxella catarrhalis Isolates. J. Clin. Microbiol.
40: 1546-1548
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Karlowsky, J. A., Critchley, I. A., Blosser-Middleton, R. S., Karginova, E. A., Jones, M. E., Thornsberry, C., Sahm, D. F.
(2002). Antimicrobial Surveillance of Haemophilus influenzae in the United States during 2000-2001 Leads to Detection of Clonal Dissemination of a {beta}-Lactamase-Negative and Ampicillin-Resistant Strain. J. Clin. Microbiol.
40: 1063-1066
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Heath, P T, Breathnach, A S
(2002). Treatment of infections due to resistant organisms: Childhood respiratory infections. Br Med Bull
61: 231-245
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Verduin, C. M., Hol, C., Fleer, A., van Dijk, H., van Belkum, A.
(2002). Moraxella catarrhalis: from Emerging to Established Pathogen. Clin. Microbiol. Rev.
15: 125-144
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Guthrie, R.
(2001). Community-Acquired Lower Respiratory Tract Infections : Etiology and Treatment. Chest
120: 2021-2034
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Subcommittee on Management of Sinusitis and Commit,
(2001). Clinical Practice Guideline: Management of Sinusitis. Pediatrics
108: 798-808
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File, T. M. Jr, Schlemmer, B., Garau, J., Cupo, M., Young, C., the 049 Clinical Study Group,
(2001). Efficacy and safety of gemifloxacin in the treatment of community-acquired pneumonia: a randomized, double-blind comparison with trovafloxacin. J Antimicrob Chemother
48: 67-74
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Chamberland, S., Blais, J., Hoang, M., Dinh, C., Cotter, D., Bond, E., Gannon, C., Park, C., Malouin, F., Dudley, M. N.
(2001). In Vitro Activities of RWJ-54428 (MC-02,479) against Multiresistant Gram-Positive Bacteria. Antimicrob. Agents Chemother.
45: 1422-1430
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Gales, A., Sader, H., Jones, R. N.
(2001). Activities of BMS 284756 (T-3811) against Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae Isolates from SENTRY Antimicrobial Surveillance Program Medical Centers in Latin America (1999). Antimicrob. Agents Chemother.
45: 1463-1466
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Barry, A. L., Fuchs, P. C., Brown, S. D.
(2001). Identification of {beta}-Lactamase-Negative, Ampicillin-Resistant Strains of Haemophilus influenzae with Four Methods and Eight Media. Antimicrob. Agents Chemother.
45: 1585-1588
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Karlowsky, J. A., Verma, G., Zhanel, G. G., Hoban, D. J.
(2000). Presence of ROB-1 {beta}-lactamase correlates with cefaclor resistance among recent isolates of Haemophilus influenzae. J Antimicrob Chemother
45: 871-875
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Zhanel, G. G., Karlowsky, J. A., Low, D. E., Canadian Respiratory Infection Study Group, t., Hoban, D. J.
(2000). Antibiotic resistance in respiratory tract isolates of Haemophilus influenzae and Moraxella catarrhalis collected from across Canada in 1997-1998. J Antimicrob Chemother
45: 655-662
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Hsueh, P.-R., Liu, Y.-C., Shyr, J.-M., Wu, T.-L., Yan, J.-J., Wu, J.-J., Leu, H.-S., Chuang, Y.-C., Yeu-Jen Lau, , Luh, K.-T.
(2000). Multicenter Surveillance of Antimicrobial Resistance of Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis in Taiwan during the 1998-1999 Respiratory Season. Antimicrob. Agents Chemother.
44: 1342-1345
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Yano, H., Suetake, M., Kuga, A., Irinoda, K., Okamoto, R., Kobayashi, T., Inoue, M.
(2000). Pulsed-Field Gel Electrophoresis Analysis of Nasopharyngeal Flora in Children Attending a Day Care Center. J. Clin. Microbiol.
38: 625-629
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Thornsberry, C., Jones, M. E., Hickey, M. L., Mauriz, Y., Kahn, J., Sahm, D. F.
(1999). Resistance surveillance of Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis isolated in the United States, 1997-1998. J Antimicrob Chemother
44: 749-759
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Thornsberry, C., Ogilvie, P. T., Holley, H. P. Jr., Sahm, D. F.
(1999). Survey of Susceptibilities of Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis Isolates to 26 Antimicrobial Agents: a Prospective U.S. Study. Antimicrob. Agents Chemother.
43: 2612-2623
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