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Antimicrobial Agents and Chemotherapy, July 2001, p. 2141-2143, Vol. 45, No. 7
Centre for Microbiology Research, Kenya
Medical Research Institute,1 and
Department of Medical Microbiology, Kenyatta National
Hospital,3 Nairobi, Kenya, and
Department of Medical Microbiology and Genito-Urinary
Medicine, University of Liverpool, Liverpool L69 3GA, United
Kingdom2
Received 6 December 2000/Returned for modification 20 March
2001/Accepted 21 April 2001
Nine Klebsiella pneumoniae isolates, six from blood
and three from cerebrospinal fluid of newborn babies at Kenyatta
National Hospital, Nairobi, Kenya, were analyzed for the mechanism of
cephalosporin resistance. By using pulsed-field gel electrophoresis of
XbaI-digested chromosomal DNA, all the nine isolates
were found to be clonal. PCR and direct sequencing revealed a novel
extended-spectrum Resistance to extended-spectrum
cephalosporins in the family Enterobacteriaceae has commonly
been associated with the expression of extended-spectrum TEM and SHV
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.7.2141-2143.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Molecular Characterization of a Novel Plasmid-Encoded
Cefotaximase (CTX-M-12) Found in Clinical Klebsiella
pneumoniae Isolates from Kenya
ABSTRACT
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Abstract
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-lactamase, which we designated CTX-M-12. It has a
more potent hydrolytic activity against cefotaxime than against
ceftazidime and a pI of 9.0 and is encoded on a large self-transferable
ca. 160-kbp plasmid.
TEXT
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Abstract
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-lactamases (ESBLs) (10, 14). However, since 1992, novel plasmid-mediated extended-spectrum -lactamases
the
cefotaximases, derived neither from these genes nor from AmpC
cephalosporinases but with greater homology to the chromosomally
encoded -lactamases of Klebsiella oxytoca
E23004have been described (2, 4). The
cefotaximases have more potent hydrolytic activity against cefotaxime
than against ceftazidime and belong to Ambler's class A
(1) plasmid-mediated enzymes and also within group 2be of
the Bush classification (7). To date 10 variants of the
CTX-M-type -lactamases have been described in various
enterobacterial species, including Escherichia coli, Salmonella
enterica serovar Typhimurium, Citrobacter
spp., and Enterobacter spp. (Table
1). A further six CTX-M-type
sequences are registered in international databanks (EMBL and GenBank). In the present study we report a new CTX-M-type
cefotataxime-hydrolyzing -lactamase, which we have designated
CTX-M-12.
TABLE 1.
The evolution of the CTX-M-like enzymes (cefotaximases)
isolated from various enterobacterial species from different parts
of the worlda
Patients were babies aged 1 to 7 days with suspected sepsis admitted to
the NewBorn Unit (NBU) of Kenyatta National Hospital, Nairobi, Kenya,
between July 1999 and February 2000. A total of nine isolates of
Klebsiella pneumoniae were obtained from blood (6) and cerebrospinal fluid (3), and their
identity as K. pneumoniae was confirmed by biochemical tests
using API 20E strips (bioMérieux, Basingstoke, United Kingdom).
Isolates were frozen at 
70°C on protect beads (TCS, Wirral, United
Kingdom) until analyzed.
Disk susceptibility to ampicillin (10 µg), coamoxyclav
(20:10 µg), cephradine (30 µg), cefuroxime (30 µg),
ceftazidime (30 µg), cefotaxime (30 µg), aztreonam (30 µg),
carbenicillin (100 µg), cotrimoxazole (1:25 µg), gentamicin
(10 µg), chloramphenicol (30 µg), streptomycin (10 µg),
tetracycline (30 µg), and nalidixic acid (30 µg) (Oxoid Ltd.,
Basingstoke, United Kingdom) was measured using a controlled disk
diffusion technique (23) on Iso-Sensitest agar (Oxoid). In
addition, testing of susceptibility to cefotaxime or to ceftazidime
alone (E test MIC strips; AB BioDisk, Solna, Sweden) and in combination
with clavulanic acid (E test
extended-spectrum-TEM-and-SHV--lactamase strips; AB BioDisk)
was performed on donors and E. coli K-12
transconjugants. Screening to detect phenotypic production of AmpC
-lactamases was done as described by Coudron et al. (9)
by employing both direct susceptibility testing with a cefoxitin
30-µg disk and their previously described three-dimensional extract test.
Chromosomal DNA from K. pneumoniae isolates was prepared in agarose plugs as described previously (15). DNA in agarose plugs was digested using 25 U of XbaI (Gibco Life Technologies, Paisley, United Kingdom). Pulsed-field gel electrophoresis (PFGE) was performed with a CHEF DR 11 system (Bio-Rad Laboratories, Richmond, Calif.) on a horizontal 1% agarose gel for 24 h at 120 V, with a pulse time of 1 to 40 s at 14°C. A lambda DNA digest consisting of a ladder (ca. 22 fragments) of increasing size from 48.5 to approximately 1,000 kb was included as a DNA size standard. The restriction endonuclease digest patterns were compared by the method of Tenover et al. (20).
Plasmid DNA extraction was performed using a Plasmid Mini Prep Kit (Qiagen Ltd., West Sussex, United Kingdom) according to manufacturer's instructions. Plasmids were separated by electrophoresis on horizontal 0.8% agarose gels at 100 V for 2 h. Plasmid sizes were determined by coelectrophoresis with plasmids of known sizes from E. coli strains V517 (NCTC 50193) (53.7, 7.2, 5.6, 3.9, 3.0, 2.7, and 2.1 kb) and 39R861 (NCTC 50192) (147, 63, 43.5, and 6.9 kb). DNA bands were visualized with an UV transilluminator (UVP Inc., San Gabriel, Calif.) after staining with 0.05% ethidium bromide. Mating experiments were performed in broth as described previously (22) using E. coli K-12 as recipient. Transconjugants were selected on MacConkey agar (Oxoid) supplemented with nalidixic acid (32 µg/ml) and cefotaxime (32 µg/ml).
As all nine K. pneumoniae isolates had similar antibiotic
susceptibility patterns and were indistinguishable by PFGE, three representative isolates (two from blood and one from cerebrospinal fluid) were selected for further analysis. Extraction of -lactamases was performed using the freeze-thaw method, and isoelectric focusing was performed as previously described (8) on
polyacrylamide gels containing ampholines with pI's ranging from 3.5 to 9.5 (Amersham Pharmacia Biotech, Little Chalfont, Buckinghamshire,
United Kingdom). Native proteins were applied directly, following
preincubation (15 min) with clavulanic acid (10 µg/ml). Gels were
calibrated using an isoelectric focusing calibration kit (Amersham
Pharmacia Biotech). Nitrocefin, a chromogenic cephalosporin, was used
throughout the analysis for detection of production of -lactamases.
Detection of -lactam hydrolysis by separated proteins
postelectrophoresis was done by layering the ampholine gel with agar
containing cefotaxime (0.4 µg/ml). After incubation at 37°C for
2 h, the agar was flooded with E. coli (NCTC 10418) and
reincubated overnight. E. coli strains DP38 and DP42,
encoding SHV-1 (pI 7.6) and TEM-1 (pI 5.4) -lactamases, respectively, were used additionally as controls for isoelectric focusing.
Total DNA for PCR was extracted by suspending donors or transconjugants in 5% (wt/vol) Chelex-100 slurry (Bio-Rad) in injection-grade water followed by boiling for 10 min. PCR amplification of the entire coding sequence of the blaCTX-M gene (ca. 1-kb amplicon) was done by the method described by Gniadowski et al. (13), using primers P1C (5'-TCG TCT CTT CCA GA-3') and P2D (5'-CAG CGC TTT TGC CGT CTA AG-3'). Sequence determination was performed using the PCR primers on both strands of the amplicons with a dideoxy-chain determination method using an automated DNA sequencer ABI PRISM 377 (Perkin-Elmer, Warrington, United Kingdom) and was analyzed using commercial software (Lasergene; DNAStar Inc., Madison, Wis.). The nucleotide sequence structure was compared to those of the blaCTX-M-1 gene (EMBL accession no. X92506), blaCTX-M-3 gene (EMBL accession no. Y10278), and blaSHV-1 gene (GenBank accession no. X98100) in GenBank.
All nine K. pneumoniae isolates were uniformly resistant to
ampicillin, cephradine, cefuroxime, cefotaxime, carbenicillin, imipenem, and tetracycline. However, they were susceptible to coamoxyclav, aztreonam, streptomycin, cotrimoxazole, gentamicin, and
nalidixic acid. When the E test was used, the MICs of cefotaxime and
ceftazidime were 24 and 1 µg/ml, respectively. The presence of
clavulanic acid lowered the MIC of cefotaxime 750 times to 0.032 µg/ml, indicating that resistance was due to production of
extended-spectrum -lactamases. All nine isolates gave an identical PFGE pattern and contained plasmids with molecular sizes of ca. 160 kbp. All the isolates transferred resistance to ampicillin, cephradine,
cefuroxime, cefotaxime, and tetracycline to E. coli K-12 on
the 160-kbp plasmid. A summary of the evolution of CTX-M-type -lactamases is shown in Table 1. The cefotaximase produced by the
K. pneumoniae outbreak strains and their E. coli
K-12 transconjugants had a pI of 9.0. SHV-type -lactamases were
not detected in either parent strains or E. coli K-12
transconjugants. When a PCR assay for CTX-M-type genes was used,
amplicons were detected in the parents, transconjugants, and
extracted plasmid DNA from the transconjugants. Our sequence data
indicate an open reading frame of 879 bp, corresponding to 293 amino
acid residues. The four amino acid changes previously reported between
blaCTX-M-1 and
blaCTX-M-3 were detected
(13). However, compared to
blaCTX-M-3, five silent point changes
were found at positions Ala-52 (GCA to GCG), Phe-66 (TTT to TTC),
Leu-102 (CTT to CTG), Ala-223 (GCT to GCA), and Ile-250 (ATC to
ATT) and three amino acid substitutions were found at positions 12, threonine (ACC) to alanine (GCC); 89, asparagine (AAT) to serine (AGT); and 278, valine (GTA) to isoleucine (ATA). Table
2 shows amino acid changes in CTX-M-12
compared to blaCTX-M-1 and
blaCTX-M-3. The four consensus motifs
70SXXK73,
130SDN132, E-166, and
234KTG236 typical of class
A serine -lactamases (1) were also found in the amino
acid sequence of this new -lactamase. As these substitutions are
not shared by other recorded CTX-M-type -lactamases,
the enzyme from Kenyan strains (pI 9.0) appears to be
a novel extended-spectrum -lactamase and has been
designated CTX-M-12.
|
During the study period, morbidity due to bacterial sepsis in the NBU rose to 40% with 35% mortality, compared to a morbidity rate of 17% during 1997. This rise was attributed to a steep increase in admissions to the NBU, thus increasing congestion and nosocomial spread of K. pneumoniae. Clonal spread was detected by PFGE in all nine K. pneumoniae isolates.
The cefotaxime-hydrolyzing -lactamase was encoded on a ca. 160-kbp
self-transferable plasmid, which also conferred resistance to ampicillin, cephradine, cefuroxime, carbenicillin, imipenem, and
tetracycline. These agents comprise most of the commonly available drugs in the hospital and therefore posed a major problem in the treatment and management of K. pneumoniae sepsis in the
newborn babies. Although these outbreak strains were sensitive to
ceftazidime, the cost of treatment is difficult for the majority of
patients. Previous studies have also demonstrated that cefotaximases
were found on a large self-transferable plasmid that also conferred resistance to other -lactams as well as to aminoglycosides (6, 11, 21). Although the origin of these large plasmid-encoded -lactamases is still unknown, they are closely related to the chromosomally mediated -lactamase from K. oxytoca
(18).
Previously CTX-M-type -lactamases were detected in species of the
Enterobacteriaceae from different parts of the world,
including Europe and South America. However, to our knowledge, this is
the first report from Africa of a CTX-M-type -lactamase from a
nosocomial K. pneumoniae outbreak. Although the Kenyatta
National Hospital has a functioning Infection Control Committee, the
introduction of more prudent infection control strategies in the NBU
may be helpful in the control of nosocomial K. pneumoniae
outbreaks, which have been a major problem in the hospital
(16).
Nucleotide sequence accession number. The nucleotide sequence data reported appears in the GenBank nucleotide sequence database under accession no. AF305837.
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ACKNOWLEDGMENTS |
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We thank the Director of the Kenya Medical Research Institute for permission to publish this work.
S.K. is supported by The Wellcome Trust Research Development Award in Tropical Medicine.
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FOOTNOTES |
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* Corresponding author. Mailing address: Centre for Microbiology Research, Kenya Medical Research Institute, KNH Compound, Off Ngong Rd., P.O. Box 43640, Nairobi, Kenya. Phone: 254-2-720163. Fax: 254-2-711673. E-mail: skariuki{at}wtrl.or.ke.
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Antimicrobial Agents and Chemotherapy, July 2001, p. 2141-2143, Vol. 45, No. 7
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.7.2141-2143.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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