RESEARCH LETTER

Evaluation of a multiplex PCR for detection of serotypes K1, K2 and

K5 in Klebsiella sp. and comparison of isolates within these
serotypes
Jane F. Turton1, Hatice Baklan2, L.K. Siu3, Mary E. Kaufmann1 & Tyrone L. Pitt1
1

Laboratory of HealthCare Associated Infection, Centre for Infections, Health Protection Agency, London, UK; 2National Blood Service, London, UK; and
Division of Clinical Research, National Health Research Institutes, Taiwan, Republic of China

Correspondence: Jane F. Turton, Laboratory

of HealthCare Associated Infection, Centre
for Infections, Health Protection Agency, 61,
Colindale Avenue, London NW9 5EQ, UK.
Tel.: 144 0 208 327 7276; fax: 144 0 208
200 7449; e-mail: jane.turton@hpa.org.uk
Received 10 January 2008; accepted 20 April
2008.
First published online 27 May 2008.
DOI:10.1111/j.1574-6968.2008.01208.x
Editor: Stefan Schwarz

Abstract
A multiplex PCR using targets within the serotype-specific region of the capsular
polysaccharide synthesis gene cluster of serotypes K1, K2 and K5 was evaluated
using the 77 reference serotype strains of Klebsiella, and a panel of clinical isolates
subjected previously to conventional serotyping. The PCR was highly specific for
these serotypes, which are those most associated with virulence in humans and
horses. PCR confirmed that isolates of the K5 serotype had cross-reacted with
antiserum for other serotypes, particularly for K7. K5 isolates received by our
laboratory were almost exclusively from thoroughbred horses, and were submitted
for screening prior to breeding programmes. Most, including a reference strain
isolated in 1955, belonged to a cluster of genetically similar isolates of sequence
type (ST) 60. K1 isolates, all from humans, belonged to a previously identified
cluster of ST 23.

Keywords
serotyping; multiplex PCR; capsular
polysaccharide synthesis gene cluster;
Klebsiella ; pulsed-field gel electrophoresis.

Introduction
The genus Klebsiella is ubiquitous in the natural environment, and naturally colonises a number of mammals,
including humans and horses. In humans, Klebsiella is
associated with both community-acquired and nosocomial
infections, including pneumonia, urinary tract infections,
septicaemia and wound infections (Podschun & Ullmann,
1992; Keynan & Rubinstein, 2007). Klebsiella is commonly
isolated from the genital tract of horses where it is generally
of little pathological significance. However, a minority of
strains appear to be more pathogenic than others and cause
endometriosis in mares, resulting in markedly decreased
foaling rates in affected mares. Recognition of these strains
in racing stallions and mares leads to their mandatory
withdrawal from breeding programmes.
Klebsiella isolates develop prominent capsular structures
composed of complex acidic polysaccharides. To date, 82
capsular antigens have been identified, but 77 form the basis
of an internationally recognized serotyping scheme (rskov
& Fife-Asbury, 1977). The capsule is considered to be a
FEMS Microbiol Lett 284 (2008) 247252

major virulence factor for Klebsiella, and there are important

differences in virulence between the serotypes. It is widely held
that serotypes K1K6 are more associated with severe respiratory infection and septicaemia in humans than the higher
numbered serotypes (Simoons-Smit et al., 1985; Kabha et al.,
1995). Serotype K1, and to a lesser extent K2, are associated
with highly invasive disease (Fang et al., 2004, 2007). Serotype
K2 predominates in human infection, but is very rarely
identified in the natural environment. In horses, serotypes
K2, K5 and K7 are considered among the most pathogenic
and specific screens for these types are carried out by breeders
of thoroughbreds (Crouch et al., 1972). However, inclusion of
serotype K7 is questionable, because a study showed that
strains of this serotype carried by healthy stallions did not
cause disease in mares (Platt et al., 1976). Reliable identification of these particular serotypes would therefore be highly
valuable for screening of horses in breeding programmes and
for detecting isolates of invasive serotypes from humans.
Conventional serotyping suffers from a number of drawbacks. Antisera to the 77 serotypes are raised in rabbits
against whole cells and are generally of a low titre. Some
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248

serotypes are characterized by extensive cross-reactions with

others. The preparation and maintenance of the antisera and
the routine serotyping methodologies are cumbersome,
labour intensive and may be subjective in their interpretation (Ayling-Smith & Pitt, 1990). DNA-based approaches
are therefore increasingly being used. The capsular polysaccharide synthesis (cps) gene cluster consists of a serotypespecific region with genes that are relatively conserved
between serotypes on either side (Chuang et al., 2006).
Brisse et al. (2004) described a molecular serotyping scheme
involving amplification of the cps cluster, followed by
restriction digestion of the amplicon. However, this scheme
requires amplification of a very large product (418 kb),
which can be problematic. An alternative approach is
detection of the various serotypes using serotype-specific
targets within the cps cluster. The magA gene, in the
serotype-specific region of the K1 cps, is now a well-accepted
target for the detection of this important serotype (Struve
et al., 2005). Specific detection of serotype K2 has also been
achieved in a similar way (Gierczynski et al., 2007; Yu et al.,
2007). Primers have been described for detection of K5, K20,
K54 and K57 serotypes (Fang et al., 2007). Here, we describe
a multiplex PCR for detection of serotypes K1, K2 and K5
using serotype-specific targets. Our laboratory receives isolates from hospitals in the United Kingdom for typing, and
also provides a serotyping service for horse breeders. Previous work in our laboratory and others identified a cluster
of genetically related isolates among K1 isolates, of multilocus sequence typing (MLST) sequence type (ST) 23, found
in three continents (Lau et al., 2000; Turton et al., 2007).
PCR-positive isolates of each of the above serotypes received
by our laboratory between November 2003 and the end of
2007 were therefore compared using pulsed-field gel electrophoresis (PFGE), to see whether similar relationships
existed among K2 and K5 isolates.

Materials and methods

Isolates
All 77 capsular serotype reference strains, described by
rskov & rskov (1984) and obtained from the National
Collection of Type Cultures (NCTC), NCTC 9660 (K5) and
96K1990 (K7) were subjected to multiplex PCR. A panel of
50 isolates, including most of those received by the Laboratory of HealthCare Associated Infection between November
2003 and June 2007 that had reacted with antisera for K1, K5
or K7 by countercurrent immunoelectrophoresis (CIE)
or Quellung reaction, was also tested. The panel included
isolates reacting with antisera for K1, K2, K3, K4, K5, K6,
K7, K8, K13, K14, K21, K25, K41, K46, K55, K62, K64,
K68, K81 and K82. Subsequently, PCR screening of all
Klebsiella isolates received was continued throughout 2007,
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J.F. Turton et al.

which identified further isolates of K1 and K2 serotypes.

Identification was by biochemical testing (Ayling-Smith &
Pitt, 1990).

Serotyping
Serotyping was carried out using a combination of CIE and
capsule swelling reactions with K antisera (Ayling-Smith &
Pitt, 1990), raised inhouse by injecting rabbits with capsular
serotype reference strains, as described previously (Edmonson
& Cooke, 1979).

Multiplex PCR
Multiplex PCR for serotype-specific targets within the K1,
K2 and K5 cps clusters was carried out using the primers in
Table 1. Primers for the K5 serotype were designed from
GenBank accession numbers AB289645 and AB289646. PCR
reactions were carried out as described previously (Turton
et al., 2007) using 1  PCR buffer (containing 1.5 mM
MgCl2) (Qiagen), 10 pmole of each primer, 200 mM each
dNTP and 1.5 U Taq DNA polymerase in a total reaction
volume of 25 mL. Primers for rmpA (associated with hypermucoviscosity) (Nadasy et al., 2007), giving a band of
516 bp, may also be included in the multiplex. Thermocycler
conditions were: 94 1C for 1 min, followed by 30 cycles of
94 1C for 30 s, 59 1C for 45 s, 72 1C for 1 min 30 s and a final
extension at 72 1C for 6 min. PCR products were separated
in a 1.5% (w/v) agarose gel or a 2% E-gel (Invitrogen,
Paisley, UK).

PFGE
PFGE of XbaI digested genomic DNA was performed as
described previously (Turton et al., 2007). Gel images were
analysed by BIONUMERICS (Applied Maths) and dendrograms
prepared using the Dice coefficient.

MLST and ompA sequencing

MLST was performed following the method of Diancourt
et al. (2005), as described previously (Turton et al., 2007).
Sequences were compared with those on the MLST website
(http://pubmlst.org/kpneumoniae/) developed by Keith Jolley
and sited at the University of Oxford (Jolley et al., 2004),
funded by the Wellcome Trust. Sequencing of the ompA gene
was carried out using primers ompAF260 5 0 -TGGCATA
TAAAGGCAGCG-3 0 and ompAR900 5 0 -GATGCCTTTAG
CAACCAGGTA-3 0 designed from GenBank accession number AJ000998. An annealing temperature of 57 1C was used
to amplify the ompA fragment with these primers, which
were also used for sequencing. Sequences of alleles 1 and 2
(285804 nt relative to AJ000998) are deposited in GenBank
under accession numbers EU264157 and EU264158,
respectively.
FEMS Microbiol Lett 284 (2008) 247252

249

Multiplex PCR for K1, K2 and K5 serotypes of Klebsiella

Table 1. Primers used in the multiplex PCR

Serotype

Primer
w

K1

MagAF1
MagAR1
Wzy-F1
Wzy-R1
K5wzxF360
K5wzxR639

K2
K5

Sequence (5 0 3 0 )

Tm 

Product size (bp)

GGTGCTCTTTACATCATTGC
GCAATGGCCATTTGCGTTAG
GACCCGATATTCATACTTGACAGAG
CCTGAAGTAAAATCGTAAATAGATGGC
TGGTAGTGATGCTCGCGA
CCTGAACCCACCCCAATC

59.7
67.2
63.5
64.3
64.4
65.2

1283
641
280

T , melting temperature.
m
w

Primers designed by Fang et al. (2004).

1230

K1

Size (bp)

984
738
K2
615
369
246

K5

123
Fig. 1. Multiplex PCR for K1, K2 and K5 serotypes. Isolates were: lane 1,
K1 type strain (NCTC 5054) (K1), lane 2, K2 type strain (NCTC 5055) (K2)
and lane 3, NCTC 9660 (K5). M is a 123-bp size ladder.

Results and discussion

Of the 77 serotype reference strains, only the K1, K2 and K5
strains gave bands in the multiplex PCR, the sizes being as
expected for the serotype (Fig. 1). The specificity was therefore 100%. Among the panel isolates, nine gave a band
corresponding to the K5 serotype (K5EQ1-8 and K5H1).
These isolates had all reacted with antiserum to K5, but most
had also cross-reacted with antiserum for K7, and some to
antiserum for K6 (Table 2). All but one of these isolates was
from horses; the only human isolate was from a batch of
isolates received from an Australian hospital (AUSH). Both
K5 reference strains (NCTC 5051 and NCTC 9660) gave the
expected band of 280 bp for the K5 serotype; both K7
reference strains (NCTC 9127 and 96K1990) and the isolate
in the panel that had reacted only with K7 antiserum (isolate
9) failed to give a band in the PCR. These results provide
strong evidence in support of our conclusion that isolates
giving a band for the K5-specific target in the PCR were
indeed K5, despite having also reacted with K7 antiserum.
The PCR identified 11 K2 isolates and eight K1 isolates
among the panel. Again, all had reacted with the appropriate
antiserum, although there were some cross-reactions, particularly between K1 isolates and K5 and K6 antisera. These
FEMS Microbiol Lett 284 (2008) 247252

isolates were all from humans. Eight isolates had reacted

with either K2 or K5 antiserum, either by CIE or Quellung,
but did not give a band in the PCR (Table 2, isolates 18).
All had, however, reacted with multiple antisera, at least one
of which would be expected to give a negative response in
the PCR. The remaining 14 isolates (which included isolates
9 and 10) had reacted with either K7, K21, K25, K41 or K55
antiserum or up to three of K3, K4, K7, K8, K68, K81 and
K82 antisera, but had not reacted with K1, K2 or K5
antisera; all gave no band in the PCR. The vast majority
of isolates that had reacted with K1, K2, K5 or K7 antisera
were identified as Klebsiella pneumoniae ssp. pneumoniae
(Table 2).
Of the three serotypes sought, K2 was the most common
among isolates received by our laboratory. In 2007, the
laboratory received 7, 18 and 3 PCR confirmed isolates of
serotypes K1, K2 and K5, respectively, with the K1 and K2
isolates all being from humans, and the K5 isolates all being
from horses, out of 449 total submissions of Klebsiella, of
which 21 were from horses. During the entire time period
investigated (over three and a half years), we received only
one isolate that reacted with K7 antiserum alone. Most
isolates that had reacted with K7 antiserum had also reacted
with K5 antiserum, and were found to be PCR positive for
serotype K5. Serotype K7 has been described as being
relatively nonpathogenic (Platt et al., 1976; Podschun &
Ullmann, 1992) and its association with disease may only be
a consequence of it cross-reacting with antisera for other
serotypes, particularly K5. Because it appears to be very rare,
and its significance is debatable, its omission from the PCR
should not be a serious limitation. As further cps sequences
become available, further primers can be added to allow
detection of other serotypes. Such primers have already been
described for K20, K54 and K57 serotypes (Fang et al.,
2007).
Comparison of the isolates by PFGE showed that most of
the K1 isolates, including all seven new to this study,
belonged to a previously identified cluster that has been
shown by MLST to be of ST 23 (Turton et al., 2007). This
cluster includes isolates from three continents. Epidemiologically related K2 isolates received from the same hospital
usually represented the same strain (e.g. K2J and K2M from
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J.F. Turton et al.

Table 2. Comparison of results obtained by conventional and PCR serotyping of panel isolates that had reacted with K1, K2, K5 or K7 antisera
Isolate

Source

Centre

PCR

CIE

Quellung

PFGE

K1H1
K1H2
K1H3
K1H4
K1H5
K1H6
K1H7
K1H8
K2TW1
K2A
K2B
K2C
K2D
K2E
K2F
K2G
K2H
K2I
K2J
K5EQ1
K5EQ2
K5EQ3
K5EQ4
K5H1
K5EQ5
K5EQ6
K5EQ7
K5EQ8
1

Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Horse
Horse
Horse
Horse
Human
Horse
Horse
Horse
Horse
Horse

11
6
12
IS1
13
14
6
6
TW1
1
2
3
3
4
5
6
7
8
5
UK1
UK2
UK3
UK4
AUSH
UK5
UK6
UK7
UK7
UK8

K1
K1
K1
K1
K1
K1
K1
K1
K2
K2
K2
K2
K2
K2
K2
K2
K2
K2
K2
K5
K5
K5
K5
K5
K5
K5
K5
K5
Negative

K1
K1 K5 K6
K1
K1
K1 K5 K6
K1 K4 K5 K6
K1 K6
K1
K2
K2
K2
K2
K2
K2
K2 K13
K2
K2
K2
K2
K5
K5 K7
K5 K6 K7
K5 K7
K5 K7
K5 K7
K5 K7
K5 K7
K5 K6 K7
K13

K1
K1
K1
K1
K1 K5 K6
K1
K1 K6
K1
NT
NT
NT
NT
NT
NT
NT
NT
NT
NT
NT
K5 K7
K5 K7
K5 K7
K5 K7
K5 K7
K5 K7
K5
K5
Negative
K2

2
3
4
5
6
7
8
9
10

Horse
Human
Horse
Human
Horse
Horse
Horse
Horse
Human

UK6
15
UK7
6
UK2
UK1
UK8
UK9
16

Negative
Negative
Negative
Negative
Negative
Negative
Negative
Negative
Negative

K14 K64 K62

K5 K6 K7 K8 K82
K5 K7
K5 K7 K66 K69
Negative
Negative
K7 K8 K82
K7
K7 K8 K81

K5
NT
K5 K7
NT
K5
K5
K5 K7
K7
K7 K8

K1 cluster
Unique
K1 cluster
K1 cluster
K1 cluster
K1 cluster
K1 cluster
K1 cluster
NT
Unique
Unique
3KL-1
3KL-1
Unique
5KL-1
Unique
Unique
Unique
5KL-1
Strain A
K5 cluster
K5 cluster
Strain A
K5 cluster
K5 cluster
K5 cluster
K5 cluster
K5 cluster
PFGE only carried out on
PCR confirmed isolates of
K1, K2 and K5 serotypes

Known K1 isolates from a previous study (Turton et al., 2007; UK1, UK3, UK5 and IS1).
NT, not tested.
The multiplex PCR includes primers for serotype specific targets in the K1, K2 and K5 capsular polysaccharide gene clusters. All isolates were identified as
Klebsiella pneumoniae ssp. pneumoniae with the exception of isolates K5H1 and isolate 7 (identified only as Klebsiella sp.). Centres 116 are hospitals in
the United Kingdom; TW1, IS1 and AUSH are hospitals in Taiwan, Israel and Australia, respectively.

hospital 5), but comparison between these strains showed

that each was distinct from one another (Fig. 2a). A cluster
(consisting of two subclusters), related within 76% similarity using our analysis conditions, was identified among the
K5 isolates, many of which were received from different
centres, and had been isolated up to 3 years apart (Fig. 2b).
The cluster included the reference strain NCTC 9660,
isolated in 1955 in Atlanta. That these isolates were genetically related was confirmed by MLST, which showed that all
the isolates in this PFGE-defined cluster were of ST 60 (rpoB
4, gapA 2, mdh 2, pgi 1, phoE 4, infB 1 and tonB 8); in
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addition, all shared the same ompA allele, which has been
given the designation allele 1. This ompA allele was also
found in isolates belonging to the K1 cluster. The two
similar isolates outside the cluster (K5EQ1 and K5EQ4,
designated strain A) had different alleles at three of the
MLST loci (phoE, rpoB and tonB) and their ompA allele also
differed from that of the cluster; this has been given the
designation allele 2. Despite six of the K5 isolates investigated displaying hypermucoviscosity i.e. forming a string
when touched with a loop, none were PCR positive for the
rmpA (a regulator of mucoid phenotype A) gene. These
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Multiplex PCR for K1, K2 and K5 serotypes of Klebsiella

Fig. 2. Dendrograms showing percentage similarity between PFGE profiles of XbaI-digested genomic DNA of isolates of (a) K2 and (b) K5 serotypes. All
K2 isolates were from UK hospitals (110). Isolates K2KK2M were identified by PCR screening, and are additional to those described in Table 2. Note
the isolates clustering within 76% (indicated by the dotted line), found to be of MLST ST 60, among the K5 isolates.

isolates had been received for screening, and there is no

evidence that they were associated with disease in these
horses. Nevertheless, it is tempting to speculate that the
association of K5 with endometriosis in horses may be
attributable to the ST 60 clonal lineage. Our data suggest
that the K5 serotype is rarely associated with disease in
humans.
This multiplex PCR represents a rapid and reliable
method of screening isolates for the three most significant
serotypes of Klebsiella associated with disease in both humans and horses. A DNA-based approach has the great
advantage that it does not suffer from cross-reactions that
sometimes render the results of conventional serotyping
highly ambiguous. Clusters among epidemiologically unrelated isolates of serotype K1 and of K5 suggest that the
disease manifestations associated with these serotypes may
be attributable to particular lineages.

Acknowledgements
We are grateful to Hilary Englender and Susannah Yarde for
carrying out the conventional serotyping on these isolates.
FEMS Microbiol Lett 284 (2008) 247252

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Supplementary material
The following supplementary material is available for this
article online:
Fig. S1. Pulsed-field gel electrophoresis profiles of XbaI
digested genomic DNA of isolates of serotype K1 received
during 2007, together with those of two isolates (K1H1 and
K1H2) from a previous study.
This material is available as part of the online article from:
http://www.blackwell-synergy.com/doi/abs/10.1111/j. 15746968.2008.01208.x (This link will take you to the article
abstract).
Please note: Blackwell Publishing is not responsible for
the content or functionality of any supplementary materials
supplied by the authors. Any queries (other than missing
material) should be directed to the corresponding author for
the article.

FEMS Microbiol Lett 284 (2008) 247252