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Journal of Clinical Microbiology, September 1998, p. 2759-2762, Vol. 36, No. 9
Department of Internal
Medicine1 and
Laboratory of Clinical
Microbiology,2 Shalu Tungs' Memorial Hospital,
Shalu, Taiwan, Republic of China
Received 9 February 1998/Returned for modification 25 March
1998/Accepted 15 June 1998
Thirty-one of 104 clinical isolates of Klebsiella
pneumoniae collected over a period of 8 months were found to be
putative extended-spectrum The introduction of
extended-spectrum cephalosporins has facilitated effective treatment of
severe infections caused by gram-negative bacteria. However, increasing
use of these agents has been associated with the emergence of resistant
bacterial strains (18). In 1983, Knothe et al.
(13) described for the first time transferable resistance to
broad-spectrum cephalosporins in clinical isolates of Klebsiella
pneumoniae and Serratia marcescens. This new resistance phenotype was due to production of an extended-spectrum In 1997, we noticed a marked increase in the number of
ceftazidime-resistant K. pneumoniae strains isolated in our
hospital, a 450-bed district teaching hospital in Taiwan. To analyze
the epidemiologies of these putative ESBL-producing isolates, we used various molecular techniques to delineate their genetic relationships and identify their ESBL patterns. This is the first report of a study
of the epidemiology of ESBL-producing K. pneumoniae isolates in a Taiwan hospital.
From January to August 1997, 104 nonrepetitive (one per patient)
clinical isolates of K. pneumoniae were isolated
consecutively from hospitalized patients. Among these, 31 were reported
to be intermediate or resistant to either ceftazidime, cefotaxime, or aztreonam by our clinical microbiology laboratory (Table
1). These 31 resistant isolates were
included in this study. Isolates were identified by using the API
system (BioMerieux, Marcy l'Etoile, France). Production of ESBLs
by these isolates was tested by an agar dilution method
(16), the Etest ESBL screen (AB BIODISK, Piscataway, N.J.),
and the double-disk synergy test (25).
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Molecular Epidemiology of Extended-Spectrum
-Lactamase-Producing Klebsiella pneumoniae Isolates in a
District Hospital in Taiwan
ABSTRACT
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-lactamase (ESBL) producers. Isoelectric
focusing and an iodine overlay agar method were used for preliminary
identification of the ESBLs. They were further identified by DNA
sequencing. Seventy-one percent of the isolates were found to produce
SHV-5. The variation in the ESBL patterns of these isolates was slight, with only five patterns being identified. The strains were typed by
pulsed-field gel electrophoresis (PFGE), and 16 different genotypes were identified. When the PFGE patterns were analyzed by the
algorithmic clustering method called the unweighted-pair group method
using arithmetic averages, five clusters were found. However,
significant genetic variations were found among 11 isolates and between
each cluster. A plasmid of 36 kb was found in all clinical isolates and
in the transconjugants. Our results indicate that the increase in the
number of ESBL-producing K. pneumoniae isolates in this hospital is due mainly to the dissemination of a resistance plasmid rather than to the clonal spread of a few epidemic strains.
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-lactamase (ESBL), SHV-2, which evolved from the well-known SHV-1 enzyme (12). Subsequently, strains producing the TEM-derived ESBL
CTX-1 were isolated in several French hospitals. Since then there have been rapid increases in the number and variety of ESBLs. Bacterial strains, especially K. pneumoniae strains, producing various
types of ESBLs have spread, or independently evolved, worldwide
(9, 15). Widespread dissemination of such strains within
hospitals is reported with increasing frequency (9, 15).
Recent surveys of hospital isolates of K. pneumoniae in
England (14) and France (22) show that 14 to 16%
produce ESBLs. Hospital colonization by these ESBL-producing strains
usually is a complex phenomenon involving different mechanisms:
dissemination of several epidemic strains (1, 2, 7, 10, 26),
dissemination of plasmids and resistance genes (3, 11,
19-21), or concurrent dissemination of genes, plasmids, and
strains (5). Moreover, identical ESBLs have evolved
independently in different places at different times (8)
and, occasionally, single isolates have carried multiple ESBLs
(4).
TABLE 1.
Characteristics of 31 clinical isolates of
ESBL-producing K. pneumoniae
Pulsed-field gel electrophoresis (PFGE) was performed with a contour-clamped homogeneous electric field DRII apparatus from Bio-Rad Laboratories (Richmond, Calif.) as described previously (7). The chromosomal DNA was digested overnight with XbaI (GIBCO-BRL, Life Technologies, Gaithersburg, Md.). DNA was electrophoresed in 1.2% SeaKem GTG agarose (FMC) at 6 V/cm for 24 h; the pulse time was increased from 5 to 40 s. Because a single base mutation in the chromosomal DNA of an isolate is sufficient to introduce differences in three fragments in its restriction pattern, isolates with restriction patterns showing the same differences in one to three fragments were considered to belong to the same genotype (23). The PFGE patterns were also analyzed with the computer software Gelcompar for Windows version 3.1b (Applied Math, Kortrijk, Belgium). The PFGE patterns were compared by the algorithmic clustering method called the unweighted-pair group method using arithmetic averages) with the Dice coefficient of similarity (2 × number of matching bands/total number of bands in both strains). Isolates were considered to be within a cluster if the coefficient of similarity was >80%.
Analytical isoelectric focusing was performed with polyacrylamide gels
(17) on crude cell-free sonic extracts. -Lactamase activity was detected by the chromogenic nitrocefin test. Standard enzymes (including TEM-1, TEM-2, TEM-10, SHV-1, SHV-2, SHV-3, SHV-4,
and SHV-5) were used as pI markers. In case more than one enzyme was
found in the gels, the ESBL enzymes were identified by their ability to
hydrolyze cefotaxime or ceftazidime in an agar overlay and by their
susceptibility to inhibition by clavulanate (15). Molten
Mueller-Hinton agar, containing 0.6% (wt/vol) ceftazidime or
cefotaxime, 6% (wt/vol) potassium iodide, and 0.6% (wt/vol) iodine,
was poured onto the isoelectric focusing gel and allowed to solidify
and form an agar layer about 2 mm thick. The bands corresponding to
ESBLs produced clear halos in the black background of agar within 30 min. The formation of these halos was inhibited when the molten
Mueller-Hinton agar mixture was supplemented with clavulanate (2 mg/liter).
In case more than one ESBL was found in the same strain, plasmid transconjugation was performed to try to separate the plasmids bearing genes encoding different ESBLs. Escherichia coli K-12 J53-2 rif was used as a recipient for conjugation of the plasmids bearing genes encoding the ESBLs. Transconjugants were selected on plates containing Mueller-Hinton agar supplemented with ceftazidime or cefotaxime (2 mg/liter) and rifampin (250 mg/liter).
Plasmid-borne DNAs of clinical isolates and transconjugants were extracted with a plasmid extraction kit (Qiagen, Hilden, Germany) according to the manufacturer's instructions. Plasmid DNA electrophoresis was performed with 0.6% agarose gel and visualized with ethidium bromide under UV light.
Plasmid DNA templates for PCR were prepared from the putative ESBL producers and the transconjugants as reported previously (24). PCR was used to amplify an SHV-specific product by using the following primers: 5'-TCAGCGAAAAACACCTTG-3' and 5'-TCCCGCAGATAAATCACCA-3'. PCR conditions were those suggested by Perkin-Elmer (Applied Biosystems Division, Foster City, Calif.) for preparation of single-stranded DNA for automated sequencing, in which AmpliTaq DNA polymerase was used. Amplification was performed with a Perkin-Elmer DNA thermocycler, model 9600. DNA sequencing of both strands of the PCR products was performed with an ABI PRISM 310 Genetic Auto-analyzer (Perkin-Elmer).
Production of ESBLs was inferred in all 31 clinical isolates of K. pneumoniae on the basis of synergy between ceftazidime and clavulanate by the agar dilution method, double-disk synergy test, and Etest ESBL screen. All of these tests were found to be equally good for the detection of ESBL producers. The production of ESBLs of these isolates was further confirmed by isoelectric focusing and the agar overlay method. The iodine agar overlay method was found to be both sensitive and specific for the detection and preliminary identification of ESBLs (data not shown). About 30% (31 of 104) of the hospital isolates of K. pneumoniae were found to be ESBL producers. The prevalence rate is quite high compared with those of other reports (3.5 to 20%) (6, 14, 16, 22, 25). Until now, no significant information on the prevalance of ESBL-producing strains in other Asian countries has been available.
Because all ESBLs detected in these isolates have pIs above 7.0, we
speculated that they are SHV derived. The SHV-specific genes of these
isolates were amplified by PCR for DNA sequencing. Twenty-two isolates
(71%) were found to harbor the gene encoding SHV-5, and two
isolates (6%) were found to harbor the gene encoding SHV-2.
Seven isolates were found to produce two unknown ESBLs (with pIs of 7.9 and 7.75). Because their -lactamase-encoding genes could not be
amplified by PCR with SHV-specific primers, they are not SHV
derivatives. Plasmid transconjugation failed to separate the plasmids
bearing the genes encoding these two enzymes, though these
plasmids were successfully transferred to the E. coli
recipients. These two enzymes may be encoded by genes located on the
same plasmid or they may represent satellite bands of only one enzyme.
There were another three isolates which produced an ESBL with a pI of
8.25. Similarly, they are also not SHV derived. The identification of
these unknown ESBLs requires further molecular cloning and DNA
sequencing.
PFGE analysis of these 31 isolates with XbaI revealed 16 distinct genotypes. The patterns obtained with XbaI are
shown in Fig. 1, and the results are
summarized in Table 1. Figure 2 is a
computer-generated dendrogram that shows relatedness of the isolates by
PFGE patterns. Five clusters, each containing isolates with
coefficients of similarity of more than 80%, were identified among 20 isolates. A high level of genetic heterogeneity was found among the
remaining 11 isolates and between each cluster. In the isolates from
the Medical Intensive-Care Unit (MICU) where an outbreak of
ESBL-producing K. pneumoniae was suspected, 10 genotypes were identified among 14 clinical isolates. Most strains were genetically unrelated, and no definite epidemic strain was found. On
the contrary, the variation in ESBL patterns (Table 1) among these 31 isolates was minor, with only five patterns being identified. This
suggests that an increase in the number of ESBL-producing K. pneumoniae isolates in this hospital is due mainly to
dissemination of resistance plasmids or mutations in existing
plasmid-mediated -lactamases under the selective pressure produced
by the overuse of third-generation cephalosporins. In contrast to our
findings, the findings of previous studies indicated that the
dissemination of strains producing SHV-derived ESBLs, especially SHV-5,
in a hospital was due mainly to clonal spread (1, 2, 10).
The epidemiological result of plasmid profile analysis of the clinical isolates was quite compatible with that of PFGE (Table 1). A plasmid of
36 kb was detected in all clinical isolates and transconjugants. This
36-kb conjugative plasmid may be responsible for the production of
ESBLs in these strains. This result further supports the hypothesis that the increase of ESBL-producing K. pneumoniae in this
hospital is due to dissemination of an epidemic plasmid. TEM-derived
ESBLs seem to be rare in K. pneumoniae strains isolated in
Taiwan. Our study also confirms that PFGE, when it is combined with
plasmid profile analysis, is an effective tool for investigating the
epidemiologies of ESBL-producing K. pneumoniae isolates.
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ACKNOWLEDGMENTS |
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We thank Woa-Ling Wu for her assistance in technical work.
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FOOTNOTES |
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* Corresponding author. Mailing address: Number 30, Ching-Cheng 20th St., Taichung City, Taiwan, Republic of China. Phone and fax: 886-4-4632425. E-mail: liu712{at}top2.ficnet.net.tw.
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Journal of Clinical Microbiology, September 1998, p. 2759-2762, Vol. 36, No. 9
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Copyright © 1998, American Society for Microbiology. All rights reserved.
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