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Journal of Clinical Microbiology, February 2000, p. 542-546, Vol. 38, No. 2
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Detection of Extended-Spectrum
-Lactamases in
Clinical Isolates of Enterobacter cloacae and
Enterobacter aerogenes
Eva
Tzelepi,1
Panagiota
Giakkoupi,1
Danai
Sofianou,2
Veneta
Loukova,1
Anastassia
Kemeroglou,2 and
Athanassios
Tsakris3,*
Department of Bacteriology, Hellenic Pasteur
Institute, 115 21 Athens,1 Department of
Microbiology, Hippokration General Hospital, 54642 Thessaloniki,2 and Department of
Microbiology, Medical School, Aristotle University of Thessaloniki,
54006 Thessaloniki,3 Greece
Received 12 July 1999/Returned for modification 30 September
1999/Accepted 28 October 1999
 |
ABSTRACT |
The aim of the present study was to investigate the frequency of
extended-spectrum
-lactamases (ESBLs) in a consecutive collection of
clinical isolates of Enterobacter spp. The abilities of
various screening methods to detect ESBLs in enterobacters were
simultaneously tested. Among the 68 consecutive isolates (56 Enterobacter cloacae and 12 Enterobacter
aerogenes isolates) that were analyzed for
-lactamase content,
21 (25 and 58%, respectively) possessed transferable ESBLs with pIs of
8.2 and phenotypic characteristics of SHV-type enzymes, 8 (14.3%) of
the E. cloacae isolates produced a previously nondescribed,
clavulanate-susceptible ESBL that exhibited a pI of 6.9 and that
conferred a ceftazidime resistance phenotype on Escherichia
coli transconjugants, and 2 E. cloacae isolates
produced both of these enzymes. Among the total of 31 isolates that
were considered ESBL producers, the Vitek ESBL detection test was
positive for 2 (6.5%) strains, and the conventional double-disk
synergy test (DDST) with amoxicillin-clavulanate and with
expanded-spectrum cephalosporins and aztreonam was positive for 5 (16%) strains. Modifications of the DDST consisting of closer
application of the disks (at 20 instead of 30 mm), the use of cefepime,
and the use of both modifications increased the sensitivity of this
test to 71, 61, and 90%, respectively. Of the 37 isolates for which isoelectric focusing failed to determine ESBLs, the Vitek test was
false positive for 1 isolate and the various forms of DDSTs were
false-positive for 3 isolates.
 |
INTRODUCTION |
The occurrence of
extended-spectrum
-lactamases (ESBLs) in enterobacteria that
possess inducible Bush group 1 chromosomal
-lactamases is
increasingly reported worldwide (1, 2, 4-9, 10, 12, 15, 17,
18). In these species, the detection of ESBLs by methods based on
the inhibitory effects of clavulanic acid is expected to be difficult
and is dependent on the level of chromosomal enzyme production
(3). From a clinical point of view, the discrimination
between ESBLs and overproduced class C
-lactamases may not be
critical, since the therapeutic options for infections caused by
organisms that possess any of these mechanisms of resistance are
similarly limited (22). Nevertheless, the detection of such
"hidden" ESBLs is still of epidemiological importance for the
hospital environment (3).
Derepressed production of the AmpC
-lactamase has previously been
documented as a prevalent mechanism of
-lactam resistance in
Enterobacter cloacae strains isolated in Greece
(24). On the other hand, there are no studies on the
occurrence of ESBLs in enterobacters, although high frequencies of such
enzymes have repeatedly been reported in strains of Klebsiella
pneumoniae, Escherichia coli, and Serratia
marcescens isolated in Greek hospitals (9, 19, 23). In
the present study we attempted to determine the frequency of ESBLs in a
consecutive sample of clinical isolates of E. cloacae and
Enterobacter aerogenes by using various screening procedures, as well as isoelectric focusing and conjugal transfer of
-lactamases.
 |
MATERIALS AND METHODS |
Bacterial strains.
A total of 68 isolates of
Enterobacter spp. (56 E. cloacae and 12 E. aerogenes isolates) were studied. The isolates were nonrepetitive (one per patient) and were obtained consecutively from clinical specimens in the Hippokration General Hospital, Thessaloniki, Greece,
from January 1998 through March 1999. Species identification was done
by using the Vitek automated identification system (bioMérieux, Marcy l'Etoile, France) and was confirmed with the ATB-GN system (bioMérieux).
Antimicrobial susceptibility testing and screening for
ESBLs.
The susceptibilities of the isolates to antibiotics were
determined by the standard disk diffusion method as described in the
guidelines of the National Committee for Clinical Laboratory Standards
(16). The MICs of selected
-lactams were determined for
isolates with representative susceptibility phenotypes and E. coli transconjugants by the Etest method (AB Biodisk, Solna, Sweden). All susceptibility results were interpreted by using the
breakpoints from the National Committee for Clinical Laboratory Standards (16). The isolates were screened for the presence of ESBLs by the Vitek ESBL detection test (bioMérieux) by using cefotaxime and ceftazidime alone (at 0.5 µg/ml) and in combination with clavulanic acid (4 µg/ml). Double-disk synergy tests (DDSTs) (14) were also performed by placing disks of ceftazidime,
cefotaxime, ceftriaxone, aztreonam, cefepime, and cefpirome (30 µg
each) at distances of 30 and 20 mm (center to center) from a disk
containing amoxicillin plus clavulanate (Amc; 20 g and 10 µg, respectively).
Conjugal transfer experiments.
Strains with resistance or
decreased susceptibility to expanded-spectrum cephalosporins (ESCs) as
well as ESC-susceptible strains with positive indications by at least
one of the ESBL screening tests used were mated with an E. coli K-12 recipient (strain 1R716; R
Strr). Transconjugants were selected on MacConkey agar
containing streptomycin (500 µg/ml) and ceftazidime (10 µg/ml) or
ampicillin (25 µg/ml).
IEF of
-lactamases.
Isoelectric focusing (IEF) was
performed by electrophoresis of ultrasonic cell extracts on
polyacrylamide gels containing ampholytes with pHs that ranged from 3.5 to 9.5 (Amersham Pharmacia Biotech AB, Uppsala, Sweden).
-Lactamases
were visualized with a 0.2-mg/ml nitrocefin solution (Oxoid Ltd.,
Basingstoke, England) and were applied on one of two parallel focused
gels immediately and on the other after it was flooded with a 1 mM
solution of potassium clavulanate. This allowed the in situ distinction
between class C
-lactamases that were insensitive to clavulanate and plasmid-mediated enzymes that were susceptible to clavulanate (21).
ERIC2 PCR typing.
The ESC-resistant isolates were typed by
the ERIC2 PCR method (13). Extracted genomic DNA
(approximately 100 ng from each isolate) was amplified in a final
volume of 50 µl containing 20 mM Tris-HCl (pH 8.3), 50 mM KCl, 0.2 mM
(each) deoxynucleoside triphosphate, 2 mM MgCl2, 50 pmol of
the ERIC2 primer (5'-AAGTAAGTGACTGGGGTGA GCG-3'), and 0.5 U
of Taq DNA polymerase (Promega). The PCR products were
separated in 1.2% agarose.
 |
RESULTS |
By disk diffusion susceptibility testing, all of the 68 Enterobacter isolates studied were resistant to cefoxitin
and were classified into three main phenotypes according to their
susceptibilities to the ESCs and aztreonam. Eighteen (32%) of 56 E. cloacae isolates and 3 (25%) of 12 E. aerogenes isolates were susceptible to all newer
-lactams
(ESC-susceptible group). Eight (14.3%) of the E. cloacae
isolates were resistant to ceftazidime and were either intermediately
susceptible or susceptible to cefotaxime, ceftriaxone, and aztreonam
(Caz-resistant group). The remaining 30 (53.6%) E. cloacae
isolates and 9 (75%) E. aerogenes isolates were resistant to all the
-lactams listed above (ESC-resistant group). Seven of the
ESC-resistant E. cloacae isolates were also resistant to cefepime and cefpirome.
By initial screening of the isolates for ESBLs, the Vitek ESBL test was
positive for two Caz-resistant E. cloacae strains and one
ESC-susceptible E. cloacae strain. The conventional DDST with ESC and aztreonam disks at 30 mm from the disk of Amc was positive
for six isolates, including another ESC-susceptible E. cloacae isolate. By applying the same disks at 20-mm distances, the number of isolates with positive DDST results increased to 22. Finally, the use of cefepime and cefpirome at distances 30 and 20 mm
from Amc resulted in positive DDST results for 22 and 29 enterobacters,
respectively. DDST results for two representative strains are shown in
Fig. 1.

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|
FIG. 1.
Various forms of DDST for two representative isolates of
E. cloacae (TSV-287 and TSV-9) producing -lactamases of
pI 8.2 (A) and 6.9 (B), respectively. A1 and B1, tests with application
of the cephalosporin disks at a standard distance of 30 mm from the
clavulanate-containing disk (center to center); A2 and B2, tests with
proximal application of the disks at 20 mm. AMC,
amoxicillin-clavulanate; CAZ, ceftazidime; CTX, cefotaxime; CRO,
ceftriaxone; FEP, cefepime; CPO, cefpirome.
|
|
To confirm these findings, we analyzed the
-lactamase contents of
the isolates. On IEF gels, all of the ESC-susceptible enterobacters, as
well as 12 of the ESC-resistant isolates (10 E. cloacae and 2 E. aerogenes isolates) presented single
-lactamase
bands (pI range, 7.8 to 9.2) which were not inhibited by potassium
clavulanate and which were thus considered class C enzymes. The
remaining 35 isolates showed one or more additional
-lactamase bands
which focused at pIs of 6.9, 8.2, and 5.4 and which were labile to the inhibitory action of clavulanate. In conjugation experiments in which
ceftazidime was used for selection, transconjugants were obtained only
from enterobacters that possessed enzymes of pI 8.2 or 6.9, and all of
them showed respective
-lactamase bands on IEF gels. Transconjugant
clones from four strains that produced the
-lactamase of pI 5.4 alone were selected on ampicillin. Matings of the two ESC-susceptible
E. cloacae strains that were positive by ESBL screening
tests showed that they were infertile. The MICs of
-lactams for
representative clinical strains and E. coli transconjugants are presented in Table 1. The clones that
had acquired the enzyme of pI 6.9 expressed high levels of resistance
only to ceftazidime, while those that produced the
-lactamase of pI
8.2 were resistant to all ESCs and aztreonam. Both types of
tranconjugant clones were more susceptible to penicillin-clavulanic
acid combinations than to the respective penicillins alone, indicating
efficient inhibition of the
-lactamases produced by this inhibitor.
Moreover, both types of tranconjugants were positive for ESBL
production by the Vitek test as well as the conventional DDST. In all
cases, resistance to aminoglycosides, co-trimoxazole, and tetracycline had been cotransferred. On the basis of these results, both enzymes were considered to be ESBLs, and the number of ESBL producers among the
total 68 enterobacters was confirmed to be 31 (45.6%). The
-lactamase of pI 8.2 encountered in 16 (28.6%) of the E. cloacae isolates and 7 (58.3%) of the E. aerogenes
isolates and the enzyme of pI 6.9 were present in 10 (17.9%) of the
E. cloacae isolates (in 2 of them together with the enzyme
of pI 8.2).
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|
TABLE 1.
MICs of selected -lactams and -lactamase contents
for representative enterobacters and E. coli transconjugants
|
|
By ERIC2 PCR typing, all eight isolates with the Caz resistance
phenotype and the
-lactamase of pI 6.9 exhibited the same pattern.
Similarly, the majority (11 of 16) of the E. cloacae isolates that possessed the enzyme of pI 8.2 exhibited a different pattern, which was also present in four of the ESC-resistant, non-ESBL-producing E. cloacae isolates. The remaining 15 ESC-resistant isolates were distributed into three unrelated ERIC2 PCR
patterns. Of the nine ESC-resistant E. aerogenes isolates,
eight, including all those that were confirmed to be ESBL producers,
showed the same ERIC2 PCR pattern (data not shown).
The scores obtained by the various ESBL screening tests are presented
in Table 2. The more efficient tests were
the DDSTs with cefepime or aztreonam at 20 mm, which were found to be
true positive for 28 (90.3%) and 21 (67.7%) of 31 ESBL producers,
respectively, and false positive for none of the 37 isolates for which
IEF and conjugal transfer experiments failed to confirm the presence of ESBLs. DDSTs with cefpirome were generally less sensitive than those
with cefepime. The conventional DDST, as well as the Vitek ESBL
detection test, were inadequate. The Vitek test was false positive for
one strain, and the DDSTs with ceftazidime, aztreonam, and cefpirome at
30 mm were false positive for another E. cloacae strain in
the ESC-susceptible group. Two more (ESC-resistant) strains for which
the DDSTs of cefepime and cefpirome indicated the presence of ESBLs
were considered false positive, since they produced only their
chromosomal
-lactamase plus an enzyme of pI 5.4 that conferred a
penicillinase resistance phenotype on the respective E. coli
transconjugants (Table 1).
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TABLE 2.
Comparative evaluation of the Vitek ESBL detection test
and the various forms of DDSTs applied for screening of ESBLs among 56 E. cloacae and 12 E. aerogenes isolates
|
|
 |
DISCUSSION |
The results of this study showed a high frequency of ESBLs in the
sample of E. aerogenes and E. cloacae isolates
examined. The most frequently encountered ESBL of pI 8.2 is most likely the SHV-5-type
-lactamase, which is widely disseminated among clinical strains of K. pneumoniae, E. coli, and
S. marcescens isolated in Greek hospitals (9, 19,
23). The available data do not allow the assignment of the pI 6.9 enzyme to any of the known ESBL groups. However, the characterization
of this probably novel ESBL is beyond of the scope of this study. On
the basis of ERIC2 PCR typing, the ESBL-producing isolates seemed to
represent a limited number of types; nevertheless, the presence of the
same
-lactamase in strains of different types and species is
indicative of the fact that horizontal gene spread may also be
responsible for the high frequency of detection of ESBLs among
enterobacters in this setting.
Our findings support previous suggestions that the currently used ESBL
detection methods, which are based on the inhibitory effect of
clavulanic acid on the activities of ESBLs against ESCs, are inadequate
in cases of overproduction of Bush group 1
-lactamases (3,
25). The Vitek ESBL detection test and the conventional DDST were
the least sensitive methods in our setting. In a previous study, the
Vitek test was found to be efficient with E. coli and Klebsiella spp., but its reliability with
Enterobacter spp. and Serratia spp. remained
questionable (20). In a recent report, the Vitek ESBL
detection test, as well as the conventional DDST, were unable to detect
the SHV-5
-lactamase in a K. pneumoniae strain that
produced a plasmid-borne AmpC-type
-lactamase; the ESBL present in
that strain had been successfully detected by a DDST that combined Amc
with cefepime (25). In accordance with this observation, the
use of cefepime increased the sensitivity of the DDST with ESCs for the
detection of ESBLs in enterobacters from 16 to 61% when the disks were
applied at the standard distance of 30 mm from clavulanate and from 71 to 90% with closer application of the disks. The greater efficacy of
cefepime and cefpirome instead of ESCs by ESBL detection methods on the
basis of the inhibitory effect of clavulanic acid is expected, since
the former, but not the latter, retain activity against derepressed
variants of enterobacters (11). "Proximal" DDSTs with
cephalosporin disks placed 20 mm from the disk containing clavulanate
were more successful than those with disks placed the standard distance
of 30 mm.
The presence of ESBLs in enterobacters has been documented previously,
but the reported numbers of ESBL producers are generally low,
especially in E. cloacae (5, 6, 8, 10, 20). In
most of these studies, as well as in studies that have evaluated various ESBL detection methods, the DDST with ESC has been used for the
initial screening. The findings of this study indicate that the
frequency of ESBLs can easily be underestimated in populations of
enterobacters characterized by a high prevalence of derepressed variants. For such situations, the application of DDSTs that combine Amc with cefepime may increase the possibility of ESBL detection.
 |
ACKNOWLEDGMENTS |
This work was partly supported by bioMérieux.
We thank L. S. Tzouvelekis for helpful suggestions.
 |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology, Medical School, Aristotle University of Thessaloniki,
54006-Thessaloniki, Greece. Phone: 30 31 99 90 91. Fax: 30 31 99 91 49. E-mail: atsakris{at}med.auth.gr.
 |
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Journal of Clinical Microbiology, February 2000, p. 542-546, Vol. 38, No. 2
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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