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Antimicrobial Agents and Chemotherapy, October 1999, p. 2417-2422, Vol. 43, No. 10
Departments of Medicine, Pathology, and Community Health,
New England Medical Center, Tufts University School of Medicine,
Boston, Massachusetts1; Danbury
Hospital, Danbury, Connecticut5; Duke
University Medical Center, Durham, North
Carolina3; University of Florida,
Jacksonville, Florida6; Loyola
University Medical Center, Maywood, Illinois4;
University of Michigan Medical Center, Ann Arbor,
Michigan7; Pittsburgh Veterans
Administration Medical Center, Pittsburgh,
Pennsylvania8; and Wadsworth
Veterans Administration Hospital, Los Angeles,
California2
Received 29 March 1999/Returned for modification 2 June
1999/Accepted 1 August 1999
Antimicrobial resistance, including plasmid-mediated resistance,
among the species of the Bacteroides fragilis group is well documented. An analysis of the in vitro susceptibility of B. fragilis group species referred between 1995 and 1996 as well as
during a 7-year (1990 to 1996), prospective, multicenter survey of over 4,000 clinical isolates of B. fragilis group species was
undertaken to review trends in the percent resistance to and geometric
mean MICs of the antibiotics tested. There was a trend toward a
decrease in the geometric mean MICs of most Antimicrobial resistance among
Bacteroides fragilis and related species has been known to
vary among institutions, species, and countries (1, 2, 4,
5). Furthermore, the past decade has seen an increase in
resistance in this group of anaerobic pathogens (17, 19).
B. fragilis is the most common anaerobic organism to seed
the human bloodstream, with an attributable mortality of 19.3%
(15), and it is the most common anaerobic isolate
complicating intra-abdominal sepsis (6, 12). Appropriate
antimicrobial therapy has been shown to be associated with an improved
outcome (11), and there has been at least one study which
has documented that there is a relationship between in vitro antibiotic
sensitivity and outcome of Bacteroides infections, although
this is still considered controversial (16, 18).
There has been an ongoing need to document changing patterns of
antimicrobial resistance among B. fragilis group species, especially with the recognition of both in vitro and in vivo transfer of antimicrobial resistance among the species of the B. fragilis group (23). For over 15 years, a multicenter
survey of resistance of Bacteroides to a variety of
antimicrobials has been conducted in the United States by using the
methodology described in this report (1, 2, 4, 5, 9, 17-19, 22,
24, 25). This report describes the susceptibility of members of
the B. fragilis group isolated from 1995 to 1996 and
analyzes the trends over a 7-year period, 1990 to 1996.
Medical centers.
Eight medical centers participated in the
study from 1995 to 1996. Two of the centers, the University of Florida
and Danbury Hospital, referred isolates during 1995 only. The
participating medical centers were as follows: Danbury Hospital,
Danbury, Conn.; Duke University Medical Center, Durham, N.C.; Loyola
University Medical Center, Maywood, Ill.; New England Medical Center,
Boston, Mass.; Pittsburgh Veterans Administration Medical Center,
Pittsburgh, Pa.; University of Florida Medical Center, Jacksonville,
Fla.; University of Michigan Medical Center, Ann Arbor, Mich.; and
Wadsworth Veterans Administration Hospital, West Los Angeles, Calif.
Bacterial isolates.
Nonduplicated clinical isolates of the
B. fragilis group species collected from the eight centers
during 1995 and 1996 were referred for susceptibility testing to the
New England Medical Center. The isolates were shipped on prereduced
chopped meat agar slants (Carr Scarborough Microbiologicals, Stone
Mountain, Ga.) and were stored frozen ( Antimicrobial agents.
Standard powders were obtained from
the following manufacturers: cefoxitin and imipenem, Merck Sharp and
Dohme (West Point, Pa.); ampicillin, sulbactam, and trovafloxacin,
Pfizer Inc. (New York, N.Y.); ticarcillin and clavulanic acid,
SmithKline-Beecham (Philadelphia, Pa.); piperacillin and tazobactam,
Wyeth-Ayerst Pharmaceuticals (St. Davids, Pa.); cefotetan and
meropenem, Zeneca Pharmaceuticals (Wilmington, Del.); clindamycin and
cefmetazole, Pharmacia Upjohn (Kalamazoo, Mich.); and metronidazole and
chloramphenicol, Sigma Chemical (St. Louis, Mo.).
0066-4804/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Multicenter Study of In Vitro Susceptibility of the
Bacteroides fragilis Group, 1995 to 1996, with Comparison
of Resistance Trends from 1990 to 1996
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
-lactam antibiotics,
while the percent resistance to most agents was less affected. Within the species B. fragilis, the geometric mean MICs
showed significant (P < 0.05) decreases for
piperacillin-tazobactam, ticarcillin-clavulanate, piperacillin,
ticarcillin, ceftizoxime, cefotetan, and cefmetazole; a significant
increase was observed for clindamycin and cefoxitin. For the
non-B. fragilis species, a significant decrease in the geometric mean MICs was observed for meropenem, ampicillin-sulbactam, ticarcillin-clavulanate, piperacillin, ticarcillin, ceftizoxime, and
cefmetazole; a significant increase was observed for cefoxitin. Significant increases in percent resistance were observed within the
B. fragilis strains for ticarcillin and ceftizoxime and
within the non-B. fragilis isolates for cefotetan.
Significant increases in percent resistance among all B. fragilis group species were observed for clindamycin, while
imipenem showed no significant change in resistance trends. The trend
analysis for trovafloxacin was limited to 3 years, since the quinolone
was tested only in 1994, 1995, and 1996. During the 7 years analyzed,
there was no resistance to metronidazole or chloramphenicol observed.
The data demonstrate that resistance among the B. fragilis
group species has decreased in the past several years, the major
exception being clindamycin. The majority of the resistance decrease
has been for the -lactams in B. fragilis, compared to
other species. The reasons for these changes are not readily apparent.
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
70°C) until time of testing.
The identification of the isolates was confirmed by means of standard
methodology (7, 21). In all tests, B. fragilis
ATCC 25285 and Bacteroides thetaiotaomicron ATCC 29741 were
used as controls. All runs in which control values were beyond the
limits specified by the National Committee for Clinical Laboratory
Standards (NCCLS) were repeated. For the 7-year analysis of trends,
data for isolates from 1990 to 1994 (19) were added.
70°C until
the day of use. Susceptibilities to metronidazole and chloramphenicol
were screened at two concentrations, 1 and 8 µg/ml. Imipenem and
meropenem were tested at a concentration range of 0.125 to 8 µg/ml,
and trovafloxacin was tested at 0.12 to 16 µg/ml. Cefotetan was
tested at a range of 0.25 to 256 µg/ml. All other antibiotics were
tested at a range of 0.12 to 128 µg/ml. To prepare the combinations
of -lactam--lactamase inhibitors, constant amounts of clavulanic
acid (2 µg/ml) and tazobactam (4 µg/ml) were combined with serial
twofold dilutions of ticarcillin and piperacillin, respectively;
ampicillin-sulbactam was tested at a fixed ratio of 2:1.
Susceptibility testing. The susceptibilities of all the isolates collected from 1990 to 1996 were determined by a modified agar dilution method using brain heart infusion agar (BBL; Becton Dickinson, Cockeysville, Md.) supplemented with 5% sheep erythrocytes and 0.005% vitamin K1 (22). The antibiotic-containing plates were prepared in house on the day of the test by adding serial twofold dilutions of the corresponding antibiotics to molten agar. The bacteria were grown to logarithmic phase in brain heart infusion-supplemented broth (Carr Scarborough Microbiologicals) and were diluted with the same broth to ~107 CFU/ml. A Steers replicator was used to deliver the inocula (104 CFU/spot) onto the surface of the agar plates. The plates were incubated for 48 h in an anaerobic chamber (Coy Systems, Grand Lake, Mich.) at 37°C. The MIC was defined as the lowest concentration of antibacterial agent that inhibited visible growth. The interpretive criteria for resistance breakpoints were based on recommendations by the Subcommittee on Antimicrobial Susceptibility Testing of the NCCLS (10). These are the breakpoints used during the 6 years of the study period (10). We used the resistance breakpoint for full resistance, as intermediate susceptibility was considered susceptibility.
Data analysis. Data were stored using Lotus 1-2-3 (Lotus Development, Cambridge, Mass.). Statistical calculations were performed using SAS, version 6.12 (SAS Institute Inc.). Resistance rates between groups were compared using the chi-square test for categorical data, and resistance rates within groups were compared using McNemar's test for paired data. Trends were analyzed using regression methods. Resistance rates over time were compared using the Wald chi-square test extracted from univariate logistic regression analyses predicting resistance from year to year. Geometric mean MICs over time were compared using the t test extracted from univariate linear regressions predicting mean MICs from year to year. An alpha level of 0.05 was used to determine statistical significance.
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Distribution of the isolates.
Table
1 lists the distribution of the isolates
by species within the B. fragilis group for 1995 and 1996. B. fragilis, the most commonly isolated species, constituted
more than half of the total isolates referred. B. thetaiotaomicron was the second most common species, followed by
Bacteroides ovatus, Bacteroides distasonis, and
Bacteroides vulgatus. Less commonly seen were Bacteroides uniformis, Bacteroides caccae, and
Bacteroides stercoris.
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Susceptibilities of the isolates.
All 961 isolates were
susceptible to metronidazole and chloramphenicol at concentrations of
1 and 8 µg/ml, respectively (data not shown). The susceptibility
rates of the B. fragilis group for 1995 and 1996 to 13 antibiotics are shown in Table 2. There
appeared to be a trend for the resistance rates to be higher for the
1995 isolates than for the 1996 isolates; however, the difference in
rate per year was only significant for piperacillin and trovafloxacin
(P = 0.004 and 0.015, respectively). The most active of
all agents were the carbapenems, imipenem and meropenem, with only one
resistant strain isolated in 1995 and none in 1996. Both antibiotics
showed similar MICs (geometric means, MICs at which 50% of the
isolates are inhibited [MIC50s], and MIC90s) which were the lowest among the drugs evaluated.
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-lactams with -lactamase inhibitors were the
second most active agents. Within this group, piperacillin-tazobactam was the most active of the three combinations, with no 1995 isolate showing resistance and only one resistant strain isolated in 1996. Although the MICs for piperacillin-tazobactam were considerably higher
than those of imipenem and meropenem, the percent resistance for the
2-year period was the same as for the carbapenems.
Ticarcillin-clavulanate was the second most active agent of this group,
but its activity was not significantly different from that of
piperacillin-tazobactam. Ampicillin-sulbactam was the least active of
the -lactam--lactamase inhibitor combinations, but only a few
isolates were resistant. The rare strains resistant to
ticarcillin-clavulanate and ampicillin-sulbactam (3 and 12, respectively) were isolated in both 1995 and 1996. Piperacillin was
significantly more active than ticarcillin in both 1995 and 1996 isolates (P < 0.001).
Cefoxitin was significantly more active than the other three
cephalosporins (P < 0.001 for all three comparisons);
it was approximately three times more active than ceftizoxime and
cefmetazole and slightly over five times more active than cefotetan.
Ceftizoxime and cefmetazole had statistically equivalent activities,
while cefotetan was significantly less active than both ceftizoxime and
cefmetazole (P < 0.001 for both). The resistance rates
for clindamycin were similar for both years, and its activity was slightly higher than that of ceftizoxime (P = 0.051).
Trovafloxacin, at a breakpoint of 8 µg/ml, showed activity similar to
that of cefoxitin (P = 0.283) but was significantly
more active than clindamycin (P < 0.001).
Resistance rates.
Table 3 shows
the 2-year combined resistance rates by species within the B. fragilis group. The only strain resistant to the carbapenems was
B. fragilis, while the only strain resistant to
piperacillin-tazobactam was B. uniformis. Resistance to
ticarcillin-clavulanate was observed in two strains of B. fragilis and one strain of B. uniformis. Twelve
isolates were resistant to ampicillin-sulbactam: five B. fragilis, two B. distasonis, two B. thetaiotaomicron, one B. ovatus, and two B. uniformis. B. vulgatus was the most resistant of the species
against both clindamycin and trovafloxacin. The highest mean resistance
rate for all antibiotics was noted among B. ovatus isolates
(19.4%). The lowest mean resistance rates were noted for B. vulgatus (8.4%) and B. fragilis (9.1%).
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-lactam--lactamase inhibitor combinations (data not shown) indicated that for all but 4 of 13 strains (69.2%) the carbapenem MICs were elevated (
2 µg/ml), as were those of ticarcillin-clavulanate and cefoxitin (32 µg/ml); for seven
strains, the MICs of piperacillin-tazobactam were elevated (32
µg/ml); all but five strains were highly resistant to
clindamycin (MIC 256 µg/ml); and two strains (15.4%) were
resistant to trovafloxacin (MIC 8 µg/ml). Twelve strains were
resistant to ampicillin-sulbactam; one strain was resistant to
ticarcillin-clavulanate but not ampicillin-sulbactam. Analysis of
cross-resistance among the 971 isolates showed obvious cross-resistance
among the -lactam antibiotics but no significant cross-resistance
between nonrelated antibiotics. The resistance patterns of clindamycin
and cefoxitin were significantly different (P < 0.001), as were those of clindamycin and trovafloxacin
(P < 0.001). The resistance patterns of clindamycin
and ceftizoxime were marginally different (P = 0.051),
while those of trovafloxacin and ceftizoxime were significantly
different (P < 0.001).
Resistance trends.
Table 4 shows
an analysis of the trends in antimicrobial resistance from 1990 to
1996, a 7-year period including more than 4,000 isolates. The trends
are analyzed as predicted annual changes in geometric mean MICs
(µg/ml) and percent resistance (expressed as the annual percent
change). For the isolates of the B. fragilis species, a
significant decrease (P < 0.05) in the geometric mean MIC was observed for piperacillin-tazobactam, ticarcillin-clavulanate, piperacillin, ticarcillin, ceftizoxime, cefotetan, and cefmetazole. A
significant increase in the geometric mean MIC was observed for
cefoxitin and clindamycin. For this same group of isolates, a
significant decrease in the percent resistance was observed only for
cefmetazole, while increases were shown for ticarcillin, ceftizoxime,
and clindamycin.
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DISCUSSION |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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At the completion of this study period in 1996, after 16 years of
ongoing surveillance of the in vitro susceptibility of the B. fragilis group, no strains resistant to either metronidazole or
chloramphenicol had been isolated. The carbapenems, imipenem and
meropenem, and the -lactam--lactamase inhibitor combinations, piperacillin-tazobactam, ticarcillin-clavulanate, and
ampicillin-sulbactam, continue to be the most active -lactam
antibiotics against this group of pathogens. However, strains resistant
to these agents have been isolated, albeit rarely. The relative
activity of these antibiotics appears to be related not only to the
type and amount of -lactamase produced by the isolate but also to
factors such as differences in penicillin binding proteins and the
ability of the antibiotic to permeate the outer membrane of the
bacterial cell, or to combinations of these factors (3, 8, 13, 14, 26, 27). Although there was no cross-resistance between the carbapenem-resistant strain and the strain resistant to
piperacillin-tazobactam, the antibiotic(s) in question showed elevated
MICs for both strains. The strain resistant to the carbapenems was also
resistant to ticarcillin-clavulanate, ampicillin-sulbactam,
ticarcillin, and the cephalosporins but not to piperacillin, while the
piperacillin-tazobactam-resistant isolate was resistant to all
other -lactams with the exception of ticarcillin-clavulanate.
These differences in activities merit further characterization of the
mechanisms of the resistance produced by these isolates. Within the
-lactam--lactamase inhibitor combinations, resistance appears to
be closely related to the intrinsic activity of the -lactam
component (i.e., piperacillin is more active than ticarcillin, and
ticarcillin is more active than ampicillin) and to the amount of
inhibitor in the combination.
Cefoxitin was the most active of the cephalosporins evaluated. Its activity was significantly higher than that of ceftizoxime, piperacillin, cefmetazole, ticarcillin, or cefotetan. The percentage of isolates resistant to cefoxitin (approximately 6%) appears to have been quite stable over the last 7 years; however, a significant increase in the geometric mean MIC was observed during this same period, which could serve as a predictor for a possible increase in future resistance rates.
Rates of resistance to clindamycin, although they did not increase during 1995 and 1996, continued to be high (16%), and a significant trend for an increase in resistance from 1990 to 1996 raises questions about the usefulness of this antibiotic in today's therapeutic armamentarium against the B. fragilis group. Trovafloxacin, the quinolone with anaerobic activity, was similar to cefoxitin but significantly exceeded the activity of clindamycin. The trend of susceptibility of B. fragilis group species to trovafloxacin was unchanged over the 3 years of testing, although this agent has only been available for clinical use since 1998.
B. ovatus was the most resistant of the B. fragilis group species. This observation is in contrast to
previous years, when the highest resistance to all antibiotics was
noted among isolates of B. distasonis. Resistance to the
carbapenems occurred in a B. fragilis isolate, and
resistance to ampicillin-sulbactam was also found in five isolates of
this species, two of which were also resistant to
ticarcillin-clavulanate. Of interest is the observation that isolates
of B. uniformis, a species that has been included in the
study only since 1990, showed resistance to all three of the
-lactam--lactamase inhibitor combinations. Resistance among
B. fragilis and B. vulgatus continues to be lower than among the rest of the other species. Nonetheless, resistance to
the carbapenems, ticarcillin-clavulanate, and ampicillin-sulbactam occurred in B. fragilis strains, and the highest rates of
resistance to both clindamycin and trovafloxacin were observed among
isolates of B. vulgatus. Similar association of this species
and resistance to trovafloxacin was previously observed by Snydman and
McDermott (20). The association of resistance with specific
antibiotic-species combinations implies that complete identification
(genus and species) of isolates by clinical laboratories will help in
the selection of therapy and that susceptibility testing panels with
currently used antibiotics should be reevaluated to include those
antibiotics with low rates of resistance.
We analyzed the data using the currently recommended NCCLS breakpoints for fully resistant strains. Although NCCLS medium was not employed, the medium used for testing has been employed for 17 years (1, 2, 4, 17, 18, 24, 25). Given the good growth of Bacteroides in most media, the medium employed should not affect the analysis. While the breakpoints have not been validated in this medium, they have been used in most recent surveys and form a basis of comparison over time (17-20).
It appears from the comparison of the results from 1995 and 1996 to
those of previous years that resistance rates for most of the
antibiotics evaluated may be decreasing (5, 17, 19). Explanations for this change are not readily apparent but could be due
to decreased -lactam use, alternative agents, and combinations which
include metronidazole. Continued surveillance should establish the
nature of the trend.
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ACKNOWLEDGMENTS |
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Major financial support for these studies was provided by a research grant from Pfizer Pharmaceuticals. Additional support was provided by Wyeth-Ayerst Pharmaceuticals, Zeneca Pharmaceuticals, and Merck and Company.
We thank Roselia Martinez for her careful preparation of the manuscript and June Cox-St. Pierre and Barbara Rapino for their technical support.
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FOOTNOTES |
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* Corresponding author. Mailing address: Departments of Medicine, Pathology, and Community Health, New England Medical Center, Tufts University School of Medicine, 750 Washington St., Boston, MA 02111-1526. Phone: (617) 636-5788. Fax: (617) 636-8525. E-mail: dsnydman{at}es.nemc.org.
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Antimicrobial Agents and Chemotherapy, October 1999, p. 2417-2422, Vol. 43, No. 10
0066-4804/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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