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Previous Article | Next Article 
Journal of Clinical Microbiology, November 2000, p. 4228-4232, Vol. 38, No. 11
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Detection of Extended-Spectrum 
-Lactamases in
Klebsiellae with the Oxoid Combination Disk Method
Michael W.
Carter,
Karen J.
Oakton,
Marina
Warner, and
David M.
Livermore*
Antibiotic Resistance Monitoring and
Reference Laboratory, Central Public Health Laboratory, London NW9
5HT, United Kingdom
Received 19 June 2000/Returned for modification 1 August
2000/Accepted 21 August 2000
 |
ABSTRACT |
The Oxoid combination disk method for detecting extended-spectrum
-lactamases (ESBLs) depends on comparing the inhibition zones of
cefpodoxime (10-µg) and cefpodoxime-plus-clavulanate (10- plus
1-µg) disks. The presence of clavulanate enlarged the zones for all
of 180 ESBL-producing klebsiellae by 
5 mm, whereas zones for
cefpodoxime-susceptible isolates and cefpodoxime-resistant isolates
with AmpC and K1 -lactamases were enlarged by 
1 mm. Good
discrimination was achieved with either the NCCLS or the British disk method.
| |
TEXT |
Extended-spectrum -lactamases
(ESBLs) are increasing sources of resistance to oxyimino-aminothiazolyl
cephalosporins, especially in klebsiellae (1, 9). Most ESBLs
are mutant TEM and SHV enzymes, but a few have different ancestries
(4). Laboratory detection can be problematic, because some
ESBLs do not confer obvious resistance to all their substrates in vitro
and up to 35% of ESBL producers continue to be reported as susceptible
to cefotaxime and ceftriaxone in Europe (1, 9). Accurate
detection nevertheless is important because clinical failures arise
even when the MICs of cephalosporins for ESBL producers are only 1 µg/ml (3, 13). Two detection strategies are in common use: (i) using ceftazidime or cefpodoxime as an indicator drug, and considering klebsiellae with reduced susceptibility to these drugs to
be resistant to all oxyimino-aminothiazolyl cephalosporins (12) or (ii) screening for synergy between extended-spectrum cephalosporins and clavulanic acid. Synergy can be detected by double-disk tests (8), although the optimum separation of
the disks is strain variable. Alternatively, commercial systems, such as Etests (5, 7) and Vitek (14), can be used. One
obvious strategy is to compare the inhibition zones of cephalosporin
disks with and without clavulanate added. This method has been used by
several researchers (see, e.g., reference 10), and
comparison of the zones given by cefotaxime (30-µg) and ceftazidime
(30-µg) disks with or without clavulanate (10 µg) added is now
advocated by the NCCLS (12). Such disks are available from
several suppliers (Becton Dickinson, MAST, and Oxoid), and an
evaluation was published recently (11). Cefpodoxime also
seems an appropriate partner agent for clavulanate in such tests, since
cefpodoxime itself is useful in ESBL screening tests. Accordingly, a
cefpodoxime-based combination disk method has been developed (Oxoid,
Basingstoke, Hampshire, United Kingdom) based on comparing the zones of
cefpodoxime (10-µg) and cefpodoxime-plus-clavulanate (10- plus
1-µg) disks. We examined whether these disks reliably detected
ESBL-positive klebsiellae and distinguished them from strains with AmpC
enzymes and from Klebsiella oxytoca strains that
hyperproduce chromosomal K1 (KOXY) -lactamase.
Bacteria.
The bacteria tested comprised Klebsiella
pneumoniae and K. oxytoca collected from intensive-care
unit (ICU) patients in multicenter surveys covering Western and
Southern Europe in 1994 and in 1997 to 1998 (1, 9). One
hundred eighty ESBL producers were included, selected on the basis of
ceftazidime/ceftazidime-plus-clavulanate MIC ratios of 16 by agar
dilution. The ESBLs produced by these isolates were partially
identified previously by isoelectric focusing and PCR-single-strand
conformation polymorphism for SHV types (15, 16), or by
isoelectric focusing and PCR-restriction fragment length polymorphism
for TEM types (16). Genes for a few of these ESBLs were
sequenced (16). Molecular studies invariably detected an
ESBL gene when the presence of an ESBL enzyme had been inferred from
synergy between ceftazidime and clavulanate (15, 16). Also
included were 19 K. oxytoca isolates that hyperproduced
their K1 chromosomal -lactamase, as demonstrated by antibiogram and kinetic studies (6), and 5 klebsiellae deduced to have AmpC -lactamases on the basis of synergy between ceftazidime and the monobactam Ro 48-1256 (9). Both of the latter groups of
isolates gave ceftazidime/ceftazidime-plus-clavulanate MIC ratios of
4 by agar dilution (9). Control strains, which were
randomly selected from the same survey collections (1, 9),
comprised 25 isolates each of K. oxytoca and K. pneumoniae that lacked ESBLs or other potent -lactamases. These
organisms were highly susceptible (MICs, 2 µg/ml) to cefotaxime,
ceftazidime, and cefpodoxime, and they gave
ceftazidime/ceftazidime-plus-clavulanate MIC ratios of 4 by agar
dilution (9).
Disk test methods.
The isolates were tested by the Oxoid
combination disk method for ESBL Detection, which depends on comparing
the inhibition zones given by cefpodoxime (CPD) (10-µg) and
cefpodoxime-plus-clavulanate (CD01) (10- plus 1-µg) disks.
Ceftazidime (CAZ) (30-µg) disks (Oxoid) were tested in parallel as a
control (8). The disk tests were performed (i) with
confluent growth on Mueller-Hinton agar (Oxoid), in accordance with the
NCCLS recommendations for nonfastidious bacteria (12), and
(ii) with semiconfluent growth on Iso-Sensitest agar (Oxoid), in
accordance with the recommendations of the British Society for
Antimicrobial Chemotherapy (BSAC Standardized Disc Sensitivity Testing
Method, Newsletter of the BSAC, Summer 1999). Zone diameters were
measured to the nearest millimeter. A difference of 5 mm between the
zones of the CD01 (10- plus 1-µg) and CPD (10-µg) disks was taken
to indicate ESBL production, as advocated by the manufacturer. The
zones of the CAZ (30-µg) and CPD (10-µg) disks additionally were
reviewed against the susceptibility criteria of the NCCLS and BSAC, and
against NCCLS criteria for predicting ESBL production (12).
Inhibition zones for ESBL producers and susceptible controls.
The distributions of inhibition zone differences (the CD01 [10- plus
1-µg] zone minus the CPD [10-µg] zone) for the ESBL producers and ESBL-negative controls by NCCLS methodology are shown in Fig. 1A; those obtained by BSAC methods are
shown in Fig. 2A. Regardless of which
method was used, all 180 ESBL producers gave zones at least 5 mm larger
with the CD01 (10- plus 1-µg) disks than with the CPD (10-µg)
disks. The differences in zone diameters between the
clavulanate-containing and non-clavulanate-containing disks were larger
by use of the BSAC methodology (mean difference, 11.6 mm; standard
deviation, 7.8 mm) than by use of the NCCLS method (mean difference,
10.0 mm; standard deviation, 4.2 mm). None of the 50 ESBL-negative
control isolates gave a difference in zone diameter of more than 1 mm
between the two disk types by either method.
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FIG. 1.
Zone distributions by NCCLS methodology. (A)
Distribution of inhibition zone differences (CD01 zone minus CPD zone)
for ESBL producers (solid bars) and non-ESBL producers (open bars). (B
and C) Zone diameters of CPD (10-µg) disks and CAZ (30-µg) disks,
respectively, for ESBL producers (solid bars) and non-ESBL producers
(open bars). Zone diameters indicating resistance, intermediate
resistance, and possible ESBL positivity according to the NCCLS are
situated to the left of the dashed, dotted-and-dashed, and solid
vertical lines, respectively.
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|
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FIG. 2.
Zone distributions by BSAC methodology. (A) Distribution
of inhibition zone differences (CD01 zone minus CPD zone) for ESBL
producers (solid bars) and non-ESBL producers (open bars). (B and C)
Zone diameters of CPD (10-µg) disks and CAZ (30-µg) disks,
respectively, for ESBL producers (solid bars) and non-ESBL producers
(open bars). Zone diameters indicating resistance according to the BSAC
are situated to the left of the solid vertical line.
|
|
The zones of CPD (10-µg) disks for ESBL producers and non-ESBL
producers were better differentiated than those of CAZ (30-µg) disks,
irrespective of whether NCCLS or BSAC methodology was used (compare
Fig. 1B and C with Fig. 2B and C). This was so despite the fact that
isolates had been categorized initially on the basis of synergy tests
between ceftazidime and clavulanate. The NCCLS criterion
(12) of predicting ESBL production from a zone of 22 mm
for a CPD (10-µg) disk correctly identified all the producers (Fig.
1B), at the expense of mistakenly inferring production in 1 of 50 susceptible controls. The alternative criterion of inferring production
from a zone of 22 mm for a CAZ (30-µg) disk identified 172 of 180 ESBL producers, without any false positives among the 50 controls (Fig.
1C). The NCCLS susceptibility criteria categorized 2 of 180 ESBL
producers as cefpodoxime susceptible, and a further 15 as intermediate;
NCCLS criteria also categorized 32 of 180 ESBL producers as ceftazidime
susceptible and a further 19 as intermediate. The BSAC resistance
breakpoint (27 mm) categorized 4 of 180 ESBL producers as susceptible
to ceftazidime, with no nonproducers categorized as resistant. The
Society makes no recommendation for CPD (10-µg) disks against
Enterobacteriaceae, as 5-µg disks are routinely used for
susceptibility testing with cefpodoxime in the United Kingdom.
Behavior of AmpC producers and of K. oxytoca strains
hyperproducing K1 -lactamase.
All five AmpC producers gave no
zones with CPD (10-µg) disks by NCCLS methodology and zones no larger
than 9 mm by the BSAC method. Zones for the CD01 (10- plus 1-µg)
disks were within 1 mm of those for the CPD (10-µg) disks for these
strains, regardless of whether NCCLS or BSAC methods were used. Zones
with CAZ (30-µg) disks for the five AmpC producers ranged from 6 to
13 mm by the NCCLS method and from 6 to 19 mm by the BSAC method. Thus,
irrespective of the method and the indicator cephalosporin, the AmpC
producers were obviously resistant, and this resistance was not
reversed by clavulanate, meaning that these strains were readily
distinguishable from ESBL producers by the combination disk test. The
behavior of the 19 K. oxytoca isolates that hyperproduced K1
-lactamase was more problematic. Twelve of these K. oxytoca isolates gave zones with CPD (10-µg) disks that
fulfilled the NCCLS criteria for predicting ESBL production (zone of
22 mm) and for intermediate resistance (20 mm); 11 gave zones
signifying frank resistance (17 mm). Using BSAC methodology, the
zones of the CPD (10-µg) disks for the 19 isolates ranged from 14 to
36 mm, with 11 of 19 isolates giving zones of 24 mm in diameter. The
isolates that appeared least resistant to cefpodoxime were identical by
both methods and corresponded to those previously found (6)
to have the least degree of -lactamase hyperproduction and to be
least resistant to cefuroxime (data not shown). The zones with the CD01 (10- plus 1-µg) disks by both the NCCLS and BSAC methods were equal
in diameter to those with the CPD (10-µg) disks, or up to 3 mm
smaller, thus distinguishing resistant hyperproducers of this
chromosomal -lactamase from strains with ESBLs. All 19 hyperproducers appeared susceptible to CAZ (30-µg) disks in both BSAC
and NCCLS tests, as anticipated for the phenotype (6).
In conclusion, comparison of the inhibition zones for the CPD (10-µg)
and CD01 (10- plus 1-µg) disks distinguished ESBL-positive klebsiellae from susceptible strains without errors, regardless of
whether the NCCLS or BSAC disk test methodology was used. M'Zali et
al. (11) recently published the findings that use of
ceftazidime (30-µg) and ceftazidime-plus-clavulanate (30- plus
10-µg) disks detected 86% of ESBL producers; that use of cefotaxime
(30-µg) and cefotaxime-plus-clavulanate (30- plus 10-µg) disks
detected 66% of producers; and that use of both disk pairs detected
93% of producers. Comparison of the two studies is tenuous, however, both because the test strains differed and because M'Zali et al. used
the ratio of the zone diameters with and without clavulanate to infer
ESBL production, rather than the difference in diameters.
In the present study, discrimination of ESBL producers and non-ESBL
producers was also achieved, with a false-positive rate of 2% and no
false negatives, by the simpler expedient of categorizing isolates as
presumptive ESBL producers on the basis of zones of <22 mm with CPD
(10-µg) disks in NCCLS tests. Application of the same criterion to
CAZ (30-µg) disks led to a false-negative rate of 4.5%. Unlike these
simpler strategies, the combination disk test additionally
distinguished ESBL producers from strains with AmpC enzymes and from
K. oxytoca isolates that overexpressed the K1 enzyme. This
discrimination is valuable for surveillance and for patient care, where
it guides the choice of further antibiotics to test (cephamycins and
-lactamase inhibitor combinations against ESBL producers,
"fourth-generation" cephalosporins (cefpirone and cefepime) against
AmpC producers, and ceftazidime against K1 hyperproducers). A
limitation, irrespective of whether NCCLS or BSAC methods were
followed, was that ca. 40% of K1 -lactamase-hyperproducing K. oxytoca isolates appeared susceptible to the CPD (10-µg) disks. These strains would not have been confused with ESBL producers, but
would have been categorized as cephalosporin susceptible unless tests
were also performed with antibiotics that are better substrates for the
K1 enzyme, notably aztreonam or cefuroxime.
| |
ACKNOWLEDGMENTS |
We are grateful to Oxoid Ltd., UK for financial support.
We thank Meifang Yuan and Gioia Babini for provision of bacterial strains.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Antibiotic
Resistance Monitoring and Reference Laboratory, Central Public Health
Laboratory, 61 Colindale Ave., London NW9 5HT, United Kingdom. Phone:
44-208-200-4400. Fax: 44-208-358-3292. E-mail:
DLivermore{at}phls.nhs.uk.
| |
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Journal of Clinical Microbiology, November 2000, p. 4228-4232, Vol. 38, No. 11
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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