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Antimicrobial Agents and Chemotherapy, June 2000, p. 1438-1442, Vol. 44, No. 6
Department of
Pathology,1 National Cheng Kung University
Medical Center, and Department of Medical
Technology,2 National Cheng Kung University
Medical College, Tainan, Taiwan
Received 19 October 1999/Returned for modification 26 January
2000/Accepted 29 February 2000
Twenty (8.5%) of 234 nonrepetitive clinical isolates of
Klebsiella pneumoniae from southern Taiwan were found to
produce extended-spectrum Resistance to the extended-spectrum
cephalosporins among members of the family
Enterobacteriaceae has become a growing worldwide problem
(1, 10, 13, 16, 21, 24). Such resistance is often associated
with transferable plasmid-encoded extended-spectrum Bacterial isolates.
Between April and September 1998, a
total of 234 nonrepetitive clinical isolates of K. pneumoniae were consecutively collected in the Department of
Pathology, National Cheng Kung University Hospital, a 900-bed
university hospital in southern Taiwan. All isolates were identified by
using the conventional techniques (8) and/or the API 20E
system (bioMérieux, Marcy l'Etoile, France).
Detection of ESBL producers and susceptibility testing.
EBSL
production was detected by means of double-disk synergy tests
(13) and phenotypic confirmatory tests as recommended by the
National Committee for Clinical Laboratory Standards (NCCLS) (20). ESBL producers detected by either of these two tests
were investigated further. The MICs of antibiotics were determined by
using E Test strips including ampicillin, amoxicillin-clavulanic acid,
cefotaxime, ceftazidime, and imipenem (AB Biodisk, Solna, Sweden), and
the results were interpreted by using the NCCLS criteria (20).
IEF analysis and enzyme inhibition assay.
Crude preparations
of Conjugation experiments and plasmid analysis.
Conjugation
experiments were performed as described previously (26) with
streptomycin-resistant E. coli C600 as the recipient (2). Transconjugants were selected on tryptic soy agar
plates supplemented by streptomycin (500 µg/ml; Sigma) and
ceftazidime (10 µg/ml; Glaxo, Greenford, United Kingdom), cefotaxime
(10 µg/ml; Hoechst-Roussel Pharmaceuticals Inc., Somerville, N.J.) or
cefoxitin (64 µg/ml; Sigma). ESBL production in transconjugants was
confirmed by the NCCLS confirmatory test. Plasmids from clinical
isolates and transconjugants were extracted by a rapid alkaline lysis
procedure (29). For the restriction enzyme analysis of
transconjugant plasmids, EcoRI and PstI (Roche
Molecular Biochemicals, Mannheim, Germany) were used. Digested and
nondigested DNA samples were analyzed by electrophoresis on 0.8%
agarose gels. The plasmid sizes of transconjugants were estimated by
adding up restriction fragments.
PCR amplification and DNA sequencing.
To amplify TEM- and
SHV-related genes from clinical isolates and their transconjugants, the
following oligonucleotide primers were used for PCR: for
blaTEM genes, forward primer
(5'-CCCCTATTTGTTTATTTTTC-3') and reverse primer
(5'-GACAGTTACCAATGCTTAATCA-3') (17),
corresponding to nucleotides 112 to 130 and 1074 to 1053, respectively,
of Sutcliffe (28); for blaSHV genes,
forward primer (5'-GCCGGGTTATTCTTATTTGTCGC-3') and reverse
primer (5'-TCTTTCCGATGCCGCCGCCAGTCA-3') (22),
corresponding to nucleotides 55 to 77 and 1067 to 1044, respectively,
of Mercier and Levesque (19). The primers used for
amplification of blaCMY-1-related genes are
shown in Fig. 1. PCR amplification was
performed as described elsewhere (14, 17, 22) and the
amplicons were totally included in these three
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Prevalence of SHV-12 among Clinical Isolates of
Klebsiella pneumoniae Producing Extended-Spectrum
-Lactamases and Identification of a Novel AmpC Enzyme
(CMY-8) in Southern Taiwan
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
-lactamases (ESBLs): 10 strains produced
SHV-12, 4 produced SHV-5, 2 produced a non-TEM non-SHV ESBL with a pI
of 8.3, 3 produced a novel AmpC -lactamase designated CMY-8 with a
pI of 8.25, and 1 produced SHV-12 and an unidentified AmpC enzyme with
a pI of 8.2. The CMY-8 enzyme confers a resistance phenotype similar to CMY-1 and MOX-1, and sequence comparisons showed high homologies (>95%) of nucleotide and amino acid sequences among these three enzymes. Plasmid and pulse-field gel electrophoresis analyses revealed
that all isolates harboring an SHV-derived ESBL were genetically
unrelated, indicating that dissemination of resistance plasmids is
responsible for the spread of SHV ESBLs among K. pneumoniae in this area. All three isolates carrying CMY-8 had identical genotypic
patterns, suggesting the presence of an epidemic strain.
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
-lactamases
(ESBLs) (13, 24). Most ESBLs from Escherichia coli and Klebsiella pneumoniae are derived from TEM- or
SHV-type -lactamases by one or more amino acid substitutions which
confer resistance to extended-spectrum cephalosporins (13,
24). Resistance to cephamycins and broad-spectrum cephalosporins
has also arisen in K. pneumoniae and E. coli via
acquisition of plasmids containing the chromosomally encoded AmpC
-lactamase found in Enterobacter spp., Pseudomonas
aeruginosa, and Citrobacter spp. (3, 4, 9, 11,
30). Unlike class A ESBLs, the activities of these enzymes are
not inhibited by clavulanic acid or tazobactam (3, 4, 21).
In the Far-Eastern countries, two closely related plasmid-mediated AmpC
enzymes have been found in K. pneumoniae: MOX-1 from Japan
(9) and CMY-1 from Korea (4, 14). The prevalence
rates of ESBL among clinical isolates of K. pneumoniae in
Taiwan have been reported to range from 10.7 to 30% (12, 15). SHV-5 has been shown to be the most-common ESBL
(15). The present study was conducted to determine the
prevalence and types of ESBLs among K. pneumoniae in the
southern part of the country. We also describe a novel AmpC enzyme in
this report.
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
-lactamases (5) from clinical isolates and their
transconjugants were subjected to isoelectric focusing (IEF) analysis
by the method of Matthew et al. (18) with an LKB Multiphor
apparatus on prepared Ampholine PAG plate gels (pH 3.5 to 9.5;
Pharmacia Biotech Asia Pacific, Hong Kong, China). Gels were developed
with 0.5 mM nitrocefin (Oxoid, Basingstoke, United Kingdom). Inhibition
assays were carried out by overlaying gels with 0.5 mM nitrocefin and
0.3 mM cloxacillin (Sigma, St. Louis, Mo.) or 0.3 mM clavulanic acid
(SmithKline Beecham Pharma, Munich, Germany) (7).
-lactamase structural
genes. The amplicons were purified with PCR Clean Up kits (Roche), and both strands were sequenced with the same primers for PCR and sequencing primers on an ABI PRISM 377 Sequencer Analyzer (Applied Biosystems, Foster City, Calif.). The sequencing primers for
blaTEM and blaSHV genes
were synthesized as described elsewhere (17, 27), and for
blaCMY-1-related genes are also shown in Fig. 1.
View larger version (52K):
[in a new window]
FIG. 1.
Complete nucleotide sequence and predicted amino acid
sequence of the blaCMY-8 -lactamase gene. The
primers for amplification of the gene were synthesized according to the
nucleotide sequence of CMY-1 (4, 14) and are double
underlined. DNA sequencing was performed with a sequencing primer
(underlined) and the PCR primers as well. Arrows indicate the
directions of DNA sequencing. The stop codon is indicated with three
asterisks. The -lactamase active site S-V-S-K, the conserved triad
K-T-G, and the class C typical motif Y-X-N are underlined.
PFGE analysis. Genomic DNAs prepared by the procedure of Piggot et al. (25) were digested overnight with 10 U of XbaI (New England Biolabs, Beverly, Mass.) and subjected to pulsed-field gel electrophoresis (PFGE) with the Pulsaphor plus system (Pharmacia) as described previously (6). DNA fragments were separated in a 1% agarose gel in 0.5× Tris-borate-EDTA (TBE) buffer at 150 V for 30 h, with pulse times ranging from 5 to 35 s.
Nucleotide sequence accession number.
The sequence of a
novel AmpC -lactamase has been submitted to GenBank database under
the accession no. AF167990.
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
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Prevalence of ESBL-producing isolates in K. pneumoniae. Among 234 nonrepetitive clinical isolates of K. pneumoniae, production of ESBL was inferred in 20 (8.5%) isolates by the NCCLS confirmatory test for ESBL. The double-disk synergy test showed clavulanic acid synergy in 15 (75%) of the 20 ESBL-producing isolates.
Resistance phenotypes.
On the basis of susceptibilities to
cefotaxime, ceftazidime and cefoxitin, the ESBL producers were
classified into four resistance phenotypes (Table
1). The resistance phenotype groups I and
II involved high-level resistance to ceftazidime and cefotaxime, respectively. Group III involved high-level resistance to cefoxitin and
cefotaxime, while group IV showed high-level resistance to cefoxitin
and ceftazidime.
|
IEF analysis and enzyme inhibition test.
The results of IEF
are summarized in Table 2. On IEF gels,
the -lactamases with a pI of 8.25 were inhibited by cloxacillin but
not by clavulanic acid, suggesting that they were AmpC enzymes. The pI
8.2 -lactamase of the isolate in group IV, O787, was not inhibited
by 0.3 mM cloxacillin and 0.3 mM clavulanic acid. All other enzymes
with pIs of 5.4, 7.6, 8.2, or 8.3 were inhibited by clavulanic acid but
not cloxacillin.
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Transfer of resistance.
Resistance to extended-spectrum
-lactams was successfully transferred from 17 of 20 ESBL producers
to E. coli. The transconjugants revealed similar resistance
phenotypes to their donors. The susceptibility tests of the
transconjugants are summarized in Table 1. It is noteworthy that the
transconjugant of isolate O787 in group IV was resistant to both
cefoxitin and ceftazidime, but only the pI 8.2 -lactamase, which was
not inhibited by clavulanic acid and cloxacillin, was detected on an
IEF gel. The sizes of the resistance plasmids transferred to E. coli are shown in Table 2.
Sequence analysis.
The results of PCR amplification and
nucleotide sequencing are summarized in Table 2. The
blaSHV genes were amplified from all clinical
isolates of K. pneumoniae and 12 of 17 transconjugants. Of
15 isolates producing a pI 8.2 enzyme, 4 carried an SHV-5 enzyme and 11 harbored an SHV-12 enzyme. Except for isolate O787 with group IV
resistance phenotype, all isolates carrying SHV-5 or SHV-12 were
distributed in group I. The SHV genotypes of the E. coli
transconjugants were consistent with those of their donors. All
clinical isolates in groups II and III carried SHV-11, which was
consistent with the -lactamase with a pI of 7.6, but their transconjugants gave a negative PCR result. The
blaTEM genes were amplified from all 16 ESBL-producing isolates carrying a pI 5.4 -lactamase and from none
of their E. coli transconjugants. DNA sequencing of the
amplicons showed that all of them were TEM-1.
-lactamase. DNA
sequencing of the amplicons revealed the same nucleotide sequence among
these 3 isolates. Sequence comparison with other known -lactamases
deposited in GenBank showed a close relationship to two AmpC
-lactamases, CMY-1 (accession no. X92508) and MOX-1 (accession no.
D13304). The enzyme, now designated CMY-8, contains the -lactamase
active site S-V-S-K, the conserved triad K-T-G, and the class C typical motif Y-X-N on the basis of its deduced amino acid sequence (Fig. 1).
Comparisons among CMY-8, CMY-1 (4) and MOX-1 (9)
by using the GAP program of the Genetics Computer Group software package showed that CMY-8 shares 98.6 and 98.1% nucleotide identities, and 98.6 and 95.2% amino acid identities with CMY-1 and MOX-1, respectively. Multiple sequence alignments of the amino acid sequences of these three enzymes were performed with the PILEUP program of the
Genetics Computer Group package and the result is shown in Fig.
2.
|
Plasmid analysis and PFGE.
The results of plasmid and PFGE
analyses are summarized in Table 2 and shown in Fig.
3. Overall, 20 clinical isolates of ESBL
producers gave 15 and 18 different types of plasmid and PFGE profiles,
respectively. All 14 isolates in group I showed different PFGE
patterns, while all 3 isolates in group III had the same plasmid and
PFGE profiles.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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The prevalence rate of ESBL producers among clinical isolates of K. pneumoniae in this study was 8.5%, which is similar to those reported in many other parts of the world (13, 16, 21, 24). Among 20 ESBL producers, 15 (75%) carried SHV-derived ESBLs, and 11 (55%) of them harbored SHV-12. SHV-12, identified in 1997 by Nüesch-Inderbinen et al. (23), has rarely been found in countries other than Korea (14). This report adds Taiwan to the list of countries where SHV-12 is prevalent. Another report from a district hospital in central Taiwan showed that the prevalence rate of ESBL-producing K. pneumoniae was 30% and that SHV-5 was the most common type of ESBL (18). The differences in the prevalence and types of ESBLs between different hospitals within a country may reflect variations in patient population, hospital care practices, and infection control activities.
The phenotype of group III involved high-level resistance to cefotaxime
and cefoxitin (Table 1). The conjugation experiment and IEF analysis
revealed a plasmid-mediated -lactamase with a pI of 8.25 responsible
for the resistance. The enzyme, designated CMY-8, could be inhibited by
cloxacillin but not by clavulanic acid. Sequence analysis revealed the
class C-specific amino acid motif Y-X-N and active-site serine at
position 64 in the deduced amino acid sequence of the enzyme (Fig. 1).
These data indicate that the enzyme is an AmpC -lactamase. The
alignments of the nucleotide and amino acid sequences showed that CMY-8
has a high degree of similarity with CMY-1 and MOX-1 (Fig. 1), two
plasmid-mediated AmpC enzymes found in Korea (4) and Japan
(9), respectively, suggesting that they might have a common
origin. These three enzymes also have a similar resistance phenotype:
high-level resistance to cefotaxime as well as cofoxitin.
Both isolates in group II produced -lactamases with pIs of 5.4, 7.6, and 8.3 (Table 2). PCR and sequence analysis revealed nucleotide
sequences identical to those of TEM-1 and SHV-11, which were consistent
with the pI 5.4 and 7.6 enzymes, respectively. The resistance phenotype
was transferable and their transconjugants showed no amplification of
the blaTEM and blaSHV
genes. Since SHV-11 and TEM-1 are not ESBLs, the pI 8.3 lactamase must
be responsible for resistance to extended-spectrum -lactams in both
isolates and should be a non-TEM and non-SHV enzyme.
The isolate in group IV had three bands reflecting pI values of 5.4, 7.6, and 8.2 on an IEF gel. The transconjugant acquiring the pI 8.2 enzyme expressed a resistance phenotype similar to that of the isolate
(Table 1). The activity of the pI 8.2 -lactamase could not be
inhibited by cloxacillin or clavulanic acid. SHV-12 was detected in the
isolate and its transconjugant by PCR and DNA sequencing. Since SHV-12
does not confer resistance to cefoxitin (15, 23), our
findings suggest that an AmpC -lactamase with a pI equal to or very
close to 8.2 is coexistent with SHV-12 on the same plasmid in this
isolate. More studies such as molecular cloning and DNA sequencing are
needed to clarify the paradoxical findings.
The blaTEM genes were amplified from 80% of
ESBL-producing K. pneumoniae isolates. IEF and sequence
analyses showed that all TEM enzymes in these isolates were TEM-1. Our
data indicate that TEM-derived -lactamases do not play an important
role in resistance to extended-spectrum -lactams among K. pneumoniae in this area despite the prevalence of TEM-1.
All 15 isolates harboring an SHV-derived ESBL revealed different PFGE
profiles (Table 2), indicating that dissemination of resistance
plasmids was responsible for the spreading of SHV-derived enzymes at
this hospital. All three isolates carrying CMY-8 had identical PFGE and
plasmid profiles (Table 2 and Fig. 3), suggesting the presence of an
epidemic strain harboring CMY-8 at this hospital. Surveillance of
dissemination of this epidemic strain is important because of its
high-level resistance to cephamycins as well as extended-spectrum
-lactams.
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ACKNOWLEDGMENTS |
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We kindly thank J. Kim, Dankook University, Korea, for provision of a K. pneumoniae strain carrying CMY-1.
This work was partially supported by grants NCKUH89-054 from National Cheng Kung University Hospital and NSC89-2314-B-006-031 from the National Science Council, Republic of China.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Medical Technology, National Cheng Kung University Medical College, No. 1 University Rd., Tainan, Taiwan 70101, Taiwan. Phone: 886-6-2353535, ext. 5775. Fax: 886-6-2363956. E-mail: jjwu{at}mail.ncku.edu.tw.
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Abstract
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Antimicrobial Agents and Chemotherapy, June 2000, p. 1438-1442, Vol. 44, No. 6
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Su, L.-H., Chen, H.-L., Chia, J.-H., Liu, S.-Y., Chu, C., Wu, T.-L., Chiu, C.-H.
(2006). Distribution of a transposon-like element carrying blaCMY-2 among Salmonella and other Enterobacteriaceae. J Antimicrob Chemother
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Wachino, J.-i., Kurokawa, H., Suzuki, S., Yamane, K., Shibata, N., Kimura, K., Ike, Y., Arakawa, Y.
(2006). Horizontal Transfer of blaCMY-Bearing Plasmids among Clinical Escherichia coli and Klebsiella pneumoniae Isolates and Emergence of Cefepime-Hydrolyzing CMY-19. Antimicrob. Agents Chemother.
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Chia, J.-H., Chu, C., Su, L.-H., Chiu, C.-H., Kuo, A.-J., Sun, C.-F., Wu, T.-L.
(2005). Development of a Multiplex PCR and SHV Melting-Curve Mutation Detection System for Detection of Some SHV and CTX-M {beta}-Lactamases of Escherichia coli, Klebsiella pneumoniae, and Enterobacter cloacae in Taiwan. J. Clin. Microbiol.
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(2004). Complexity of Klebsiella pneumoniae Isolates Resistant to Both Cephamycins and Extended-Spectrum Cephalosporins at a Teaching Hospital in Taiwan. J. Clin. Microbiol.
42: 5337-5340
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(2004). SHV-12-Like Extended-Spectrum-{beta}-Lactamase-Producing Strains of Salmonella enterica Serotypes Babelsberg and Enteritidis Isolated in France among Infants Adopted from Mali. J. Clin. Microbiol.
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Heritage, J., Chambers, P. A., Tyndall, C., Buescher, E. S.
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Wu, T.-L., Chia, J.-H., Su, L.-H., Kuo, A.-J., Chu, C., Chiu, C.-H.
(2003). Dissemination of Extended-Spectrum {beta}-Lactamase-Producing Enterobacteriaceae in Pediatric Intensive Care Units. J. Clin. Microbiol.
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(2003). Extended-Spectrum {beta}-Lactamases in Ireland, Including a Novel Enzyme, TEM-102. Antimicrob. Agents Chemother.
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Cao, V., Lambert, T., Nhu, D. Q., Loan, H. K., Hoang, N. K., Arlet, G., Courvalin, P.
(2002). Distribution of Extended-Spectrum {beta}-Lactamases in Clinical Isolates of Enterobacteriaceae in Vietnam. Antimicrob. Agents Chemother.
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Decre, D., Verdet, C., Raskine, L., Blanchard, H., Burghoffer, B., Philippon, A., Sanson-Le-Pors, M. J., Petit, J. C., Arlet, G.
(2002). Characterization of CMY-type {beta}-lactamases in clinical strains of Proteus mirabilis and Klebsiella pneumoniae isolated in four hospitals in the Paris area. J Antimicrob Chemother
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Yan, J.-J., Ko, W.-C., Jung, Y.-C., Chuang, C.-L., Wu, J.-J.
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40: 3121-3126
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Yu, W. L., Winokur, P. L., Von Stein, D. L., Pfaller, M. A., Wang, J. H., Jones, R. N.
(2002). First Description of Klebsiella pneumoniae Harboring CTX-M {beta}-Lactamases (CTX-M-14 and CTX-M-3) in Taiwan. Antimicrob. Agents Chemother.
46: 1098-1100
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Chanawong, A., M'Zali, F. H., Heritage, J., Xiong, J.-H., Hawkey, P. M.
(2002). Three Cefotaximases, CTX-M-9, CTX-M-13, and CTX-M-14, among Enterobacteriaceae in the People's Republic of China. Antimicrob. Agents Chemother.
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Howard, C., van Daal, A., Kelly, G., Schooneveldt, J., Nimmo, G., Giffard, P. M.
(2002). Identification and Minisequencing-Based Discrimination of SHV {beta}-Lactamases in Nosocomial Infection-Associated Klebsiella pneumoniae in Brisbane, Australia. Antimicrob. Agents Chemother.
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Barlow, M., Hall, B. G.
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Chanawong, A., M'Zali, F. H., Heritage, J., Lulitanond, A., Hawkey, P. M.
(2001). SHV-12, SHV-5, SHV-2a and VEB-1 extended-spectrum {beta}-lactamases in Gram-negative bacteria isolated in a university hospital in Thailand. J Antimicrob Chemother
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Yan, J.-J., Ko, W.-C., Tsai, S.-H., Wu, H.-M., Wu, J.-J.
(2001). Outbreak of Infection with Multidrug-Resistant Klebsiella pneumoniae Carrying blaIMP-8 in a University Medical Center in Taiwan. J. Clin. Microbiol.
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Yan, J.-J., Hsueh, P.-R., Ko, W.-C., Luh, K.-T., Tsai, S.-H., Wu, H.-M., Wu, J.-J.
(2001). Metallo-{beta}-Lactamases in Clinical Pseudomonas Isolates in Taiwan and Identification of VIM-3, a Novel Variant of the VIM-2 Enzyme. Antimicrob. Agents Chemother.
45: 2224-2228
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Yan, J.-J., Ko, W.-C., Wu, J.-J.
(2001). Identification of a Plasmid Encoding SHV-12, TEM-1, and a Variant of IMP-2 Metallo-{beta}-Lactamase, IMP-8, from a Clinical Isolate of Klebsiella pneumoniae. Antimicrob. Agents Chemother.
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Vahaboglu, H., Fuzi, M., Cetin, S., Gundes, S., Ujhelyi, E., Coskunkan, F., Tansel, O.
(2001). Characterization of Extended-Spectrum {beta}-Lactamase (TEM-52)-Producing Strains of Salmonella enterica Serovar Typhimurium with Diverse Resistance Phenotypes. J. Clin. Microbiol.
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Girlich, D., Poirel, L., Leelaporn, A., Karim, A., Tribuddharat, C., Fennewald, M., Nordmann, P.
(2001). Molecular Epidemiology of the Integron-Located VEB-1 Extended-Spectrum {beta}-Lactamase in Nosocomial Enterobacterial Isolates in Bangkok, Thailand. J. Clin. Microbiol.
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Teshager, T., Domínguez, L., Moreno, M. A., Saénz, Y., Torres, C., Cardeñosa, S.
(2000). Isolation of an SHV-12 beta -Lactamase-Producing Escherichia coli Strain from a Dog with Recurrent Urinary Tract Infections. Antimicrob. Agents Chemother.
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38: 4320-4325
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