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Journal of Clinical Microbiology, February 2001, p. 811-815, Vol. 39, No. 2
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.2.811-815.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Vancomycin-Resistant Enterococcus
faecium Strain Carrying the vanB2 Gene Variant in a
Polish Hospital
Magdalena
Kawalec,1
Marek
Gniadkowski,1
Urszula
Zieli
ska,2
Waldemar
K
os,2 and
Waleria
Hryniewicz1,*
Sera & Vaccines Central Research Laboratory,
00-725 Warsaw,1 and Medical Center for
Postgraduate Education, 00-416 Warsaw,2
Poland
Received 23 August 2000/Returned for modification 22 October
2000/Accepted 11 November 2000
 |
ABSTRACT |
About 2.5 years after the first isolation of the VanA phenotype of
vancomycin-resistant Enterococcus faecium (VREM) in Poland, the first VREM strains with the VanB phenotype have emerged
independently in two different Warsaw hospitals. In one of these the
VREM strain was selected during the long-term antimicrobial treatment
of a patient with a wide variety of infection risk factors who died after 3 months of hospitalization. The strain was found to contain the
transferable vanB2 gene cluster variant of the polymorphic type that was identified earlier in vancomycin-resistant enterococci from several different countries. In the course of infection the strain
underwent genetic diversification due to DNA recombination.
| |
CASE REPORT |
In the middle of June 1999, a
68-year-old woman with acute pancreatitis was subjected to surgical
evacuation of necrotic tissues and extraperitoneal drainage in a Warsaw
hospital. Having developed septic shock, she was transferred from the
surgical ward to the intensive care unit (ICU). Various risk factors
for infection were identified in the patient, and these included
obesity, diabetes, adult respiratory distress syndrome, intubation,
tracheostomy, ventilation, gastric tube, intravenous central catheter,
total parenteral nutrition, continuous extraperitoneal lavage, urinary catheter, prolonged hospitalization, and intensive antibiotic therapy.
The following antimicrobials were used for the treatment in the ICU:
metronidazole, cefoperazone, imipenem, vancomycin, amikacin,
piperacillin with tazobactam, tobramycin, ciprofloxacin, ceftazidime, co-trimoxazole, and fluconazole. Several different pathogens were recovered from the patient during this period including a Klebsiella pneumoniae strain that produced an
extended-spectrum 
-lactamase, a Pseudomonas aeruginosa
strain resistant to imipenem, a methicillin-resistant
Staphylococcus aureus (MRSA) strain, a vancomycin-susceptible Enterococcus faecium strain, and a
vancomycin-resistant E. faecium (VREM) isolate. Vancomycin
was introduced into therapy on the 12th day of hospitalization, after
the first isolation of MRSA, and was used in three therapeutic courses
of at least 15 days each. The first VREM isolate was cultured from a
skin lesion at the end of August 1999, after 52 days (in total) of vancomycin therapy. The patient died after 90 days of hospitalization with symptoms of generalized infection and multiorgan failure.
Altogether four VREM isolates were collected during the treatment
(Table 1); three were identified in
clinical samples from the patient (skin lesion, peritoneum, and stool),
and one was identified from the patient's environment (the patient's
bedsheet). No vancomycin-resistant enterococci (VRE) were recovered
during the testing of other patients, medical personnel, and the entire ICU environment that was performed immediately after isolation of the
first VREM isolate. In order to prevent strain dissemination, the
patient was isolated with dedicated medical personnel, and advanced
infection control procedures were introduced into the ward according to
the guidelines of the Centers for Disease Control and Prevention
(11). The preventive action was successful, as no VRE have
been isolated in the hospital since that time.
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TABLE 1.
Selected clinical data for the clinical isolates and PFGE
typing, mating, and vanB gene sequence and
polymorphism results
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|
Microbiology.
The VREM isolates were subjected to detailed
microbiological and epidemiological analyses. Genus identification was
performed as described by Facklam and Collins (9), and the
species was identified by the API Rapid ID32 STREP test
(bioMérieux, Charbonnieres-les-Bains, France), supplemented by
potassium tellurite reduction, motility, and pigment production tests
(9). The MICs of different antimicrobial agents were
evaluated by the agar dilution method according to NCCLS guidelines
(17) and by the Etest in the case of
quinupristin-dalfopristin and linezolid (the linezolid susceptibility
data were interpreted according to the manufacturer's
recommendations). Antimicrobial standards were supplied by the
corresponding manufacturers. Enterococcus faecalis ATCC
29212, S. aureus ATCC 29213, and E. faecalis
V583, the standard VanB phenotype strain (8, 22), were
used as reference strains. The isolates were characterized by the high level of resistance to vancomycin (MICs, 128 to 256 µg/ml) and susceptibility to teicoplanin (MICs, 0.25 to 1 µg/ml), which
suggested the VanB phenotype of vancomycin resistance. Additionally,
they were resistant to penicillin (MICs, 128 µg/ml), ampicillin
(MICs, 64 µg/ml), ciprofloxacin (MICs, 16 to 64 µg/ml), and
chloramphenicol (MICs, 32 µg/ml) and also to high concentrations of
aminoglycosides (gentamicin MICs, >1,024 µg/ml; streptomycin MICs,
>2,048 µg/ml). The only antimicrobials to which the isolates were
susceptible were tetracycline (MICs, 0.25 to 0.5 µg/ml),
quinupristin-dalfopristin (MICs, 0.5 µg/ml), and linezolid (MICs, 1 µg/ml). The susceptibility testing revealed the multidrug resistance
phenotype of the VREM isolates.
The vancomycin resistance transfer experiment was carried out with the
isolates by the filter-mating procedure described by
Klare et al.
(
15).
E. faecium 64/3, which is resistant to
rifampin
and fusidic acid (
28), was used as a recipient.
The results
are listed in Table
1. All but one isolate (isolate 8672)
produced
transconjugants at an efficiency of about 10
5
per donor cell, which indicated that the vancomycin resistance
determinants were transferable and had a relatively high transmission
potential. Evaluation of the MICs for the recombinant strains
revealed
that resistance to no other drug was cotransferred with
the resistance
to vancomycin (data not
shown).
Clinical isolates were typed by pulsed-field gel electrophoresis (PFGE)
with a CHEF DRII system (Bio-Rad, Hercules, Calif.).
DNA purification
and digestion with the
SmaI restriction enzyme
(MBI
Fermentas, Vilnius, Lithuania) were performed as described
by Clark et
al. (
5), and the electrophoresis was run under
the
conditions described by de Lencastre et al. (
7). PFGE
results
were interpreted by the criteria proposed by Tenover et al.
(
26).
The results are shown in Fig.
1 and Table
1. All isolates were
found to
represent a single PFGE type; however, one of these,
isolate 8672, produced PFGE pattern a2, which differed by five
DNA bands from the
pattern for the predominant one, PFGE pattern
a1. These data suggested
that the patient was originally infected
with a single VREM strain
which underwent some genetic differentiation
with time.
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FIG. 1.
PFGE of VREM isolates and location of the
vanB gene cluster within the PFGE patterns. Total DNA of the
isolates was cut with SmaI and separated by PFGE and was
hybridized with the vanB gene cluster probe. Lanes M,
bacteriophage  ladder molecular size standard (in kilobases; New
England Biolabs, Beverly, Mass.).
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|
For the identification of vancomycin resistance genes, the total DNAs
of the isolates were purified with the Genomic DNA Prep
Plus kit (A&A
Biotechnology, Gda
sk, Poland). The
vanB gene was
detected by specific PCR with two different pairs of primers,
the
vanB and
vanB consensus primers, and the cycling
conditions
used were those described originally (
5,
6).
For all the
isolates the PCR with the
vanB primers, which
are specific for
the
vanB1 gene variant (
5,
6),
amplified products of about
1.1 kb instead of 433 bp, as predicted for
vanB1 and obtained
for the
vanB1-containing V583
E. faecalis control strain (
8,
21,
22). The
vanB consensus primers, which amplify specific
products from
all
vanB gene variants known to date (
6),
produced
amplicons of about 500 bp, which corresponded well with the
expected
size of 484 bp. These data confirmed that the isolates were of
the VanB phenotype and revealed that this phenotype was determined
by a
gene cluster variant which was different from
vanB1.
The
vanB gene-containing 1.1-kb PCR product obtained for
isolate 8672 was subjected to direct DNA sequencing. Sequencing
reactions
(
24) were performed with the use of primers
vanB (
5) supplemented
by internal primers
5'-GACAAATCACTGGCC-3' and 5'-ATGGCTTCTTGCATAGC-3'
and an ABI 310 PRISM automatic system (PE Biosystems, Foster
City,
Calif.). It was found that the PCR product encompassed the 896-bp
fragment of the
vanB coding region starting from its 5' end
(out
of 1,029 bp altogether) and the 201-bp fragment of the
vanHB reading
frame that is located directly
upstream of
vanB (with an overlap
of 8 bp). This indicated
that, similarly to known
vanB2 and
vanB3 variants
(
10,
18), the 5' primer of the
vanB primer pair
(
5)
did not anneal to the
vanB coding region;
however, it must have
been complementary to a sequence present within
the
vanHB gene,
which seems to be unique
(
6). The
vanB gene sequence was found
to be
identical to the corresponding part of one of
vanB2 variants
identified previously in Rochester, Minn. (GenBank accession no.
U94526) (
18) and differed by a single base pair from
a
vanB2 gene sequenced in Taiwan (GenBank accession no.
Z83305).
Restriction fragment length polymorphism (RFLP) analysis of the
vanB2 gene cluster was studied as proposed by Dahl et
al.
(
6). DNA fragments encompassing the
vanRB,
vanSB,
vanYB,
vanW,
vanHB,
vanB, and
vanXB genes were amplified by long PCR (L-PCR)
with the use of primer
vanB long, and the resulting L-PCR
products
were analyzed with the use of the
DraI and
PagI (an isoschizomer
of
BspHI) restriction
enzymes (MBI Fermentas). The results are
shown in Fig.
2A and Table
1. L-PCR products of the
expected
size of about 6 kb were obtained for all isolates analyzed.
The
amplified regions were found to represent a single polymorph,
which
was originally identified as RFLP-2 in
vanB2 and
vanB3 gene
clusters from
E. faecium and
E. faecalis isolates collected in
Norway, Sweden, the United Kingdom,
Germany, and the United States
(
6).
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FIG. 2.
RFLP analysis of vanB gene clusters in VREM
isolates. (A) DraI-PagI restriction analysis of
vanB gene clusters amplified by L-PCR. Lanes M1,
BstEII-digested bacteriophage molecular size standard
(in base pairs); lane M2, MspI-digested pBR322 molecular
size standards (in base pairs; T. E. Kucharczyk, Warsaw, Poland).
(B) DraI-PagI RFLP analysis of vanB
loci analyzed by hybridization of total DNA with the vanB
gene cluster probe. The arrows indicate DNA bands that distinguished
the two polymorphs of the region. The asterisk indicates the DNA band
of the BstEII-digested bacteriophage molecular size
marker (in base pairs), which results from the sticking of the 8,454-bp
fragment to the 5,686-bp fragment by the cos ends.
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|
In order to study the location of the
vanB2 gene cluster,
the total DNAs of the isolates, embedded in agarose plugs and digested
with
SmaI, were separated by PFGE (as described above),
blotted
onto a Hybond-N
+ membrane (Amersham Pharmacia
Biotech, Little Chalfont, United
Kingdom), and hybridized with the
vanB gene cluster probe. The
L-PCR amplicon of the
vanB1 gene cluster present in the
E. faecalis V583 VanB reference strain (
8,
21,
22) was used as the
probe. Probe labeling, hybridization, and signal detection were
performed with the ECL Random-Prime Labeling and Detection system
(Amersham Pharmacia Biotech). Results of the analysis are shown
in Fig.
1. Single hybridizing DNA bands were revealed for each
isolate, and in
the case of the three PFGE subtype a1 isolates,
the
vanB2
gene cluster was located within the
SmaI restriction
fragment of about 230 kb, whereas in PFGE subtype a2 isolate 8672,
this
fragment was about 150 kb. It is likely that the
vanB2 gene
cluster resided within a transposon (
4,
20) which was
inserted
into chromosomal DNA or a particularly large plasmid and which
may have possessed conjugative functions itself (
4,
19,
20).
Its horizontal transfer may also have been mediated by
plasmid
conjugation (
3,
29) or by another transferable
mobile element
(
4,
19). A rearrangement of chromosomal or
plasmid DNA, reflected
by the change in the PFGE pattern, has affected
the position of
the
vanB2 gene cluster DNA within the PFGE
pattern of isolate
8672 and might have been responsible for the loss of
its
transferability.
For a more detailed analysis of the
vanB2 locus, the total
DNAs of the isolates, purified with the Genomic DNA Prep Plus kit
(A&A
Biotechnology), were digested with the
DraI and
PagI restriction
enzymes (MBI Fermentas), electrophoresed,
blotted onto a Hybond-N
+ membrane, and hybridized with the
vanB gene cluster probe. Probe
labeling and hybridization
were performed as described above.
The results are shown in Fig.
2B.
The hybridization patterns obtained
corresponded well to the
DraI-
PagI (
BspHI) RFLP patterns of the
isolated
vanB2 gene clusters, and the only difference
observed
among the isolates was that the largest DNA fragment of the
patterns
was smaller for PFGE subtype a2 isolate 8672 (ca. 4.8 kb) than
for the remaining isolates (ca. 5.5 kb). These data suggested
that the
DNA recombination event(s) that occurred in isolate 8672
has changed
the structure of either the
vanB2 gene cluster-containing
transposon or its directly adjacent sequence
context.
VRE belong to the most dangerous nosocomial pathogens that usually
cause infections in severely debilitated patients hospitalized
for long
periods of time. The first strains of VRE were identified
in 1986 in
France (
16) and in the United Kingdom (
27),
and
since then these microorganisms have become common in many
countries
all over the world (
2,
5,
25). Until recently,
they were
not observed in Poland (
13,
30); however, in
last few years
VRE have started to emerge in different hospitals in
Poland. The
first reported incidence occurred in December 1996 in a
hospital
in Gda
sk (
12) with the identification of
VREM of the VanA
phenotype (
1). This isolation was
followed by a large and complicated
outbreak in two different
hematological wards of the center (
14,
23).
Data presented in this work document one of the first two incidences of
a VREM strain expressing the VanB phenotype (
8,
21,
22) in
Poland. The strain was isolated from a single patient
located in the
ICU of a Warsaw hospital who was particularly prone
to nosocomial
infection. Due to immediate introduction of strict
infection control
procedures (
11), the VREM strain was most
likely
eradicated from the hospital environment. The detailed
molecular
analysis revealed that its phenotype was determined
by the
vanB2 gene cluster variant, which resided within a
transferable
DNA molecule. During the infection process the strain
underwent
genetic diversification due to a DNA rearrangement that also
affected
the
vanB locus. The VanB phenotype was originally
reported by
Sahm et al. (
22) in 1989 and was described by
Quintiliani et
al. (
21) in 1993, and since then it has
spread in several countries
(
6). It is determined by a
cluster of genes located within
composite transposons that may be
horizontally transmitted between
strains either by themselves or by a
plasmid-mediated or other
conjugative element-mediated process
(
3,
4,
19,
20,
29). Several works carried out with VanB
strains of VRE from
different countries (
6,
8,
10,
18)
revealed a certain
degree of heterogeneity of the
vanB gene
sequence (
vanB1,
vanB2,
and
vanB3
variants) and of RFLP analysis of the
vanB gene cluster
(RFLP-1, -2, and -2*). Identification of the next case of infection
with the
vanB2 variant present in the context of the RFLP-2
polymorph
of the gene cluster confirms the earlier observation of the
high
degree of stability of the
vanB-region sequences and
the hypothesis
that they have a common evolutionary origin
(
6).
| |
ACKNOWLEDGMENTS |
We thank Stephen Murchan for critical reading of the manuscript;
Patrice Courvalin, who kindly provided E. faecalis V583; and
Wolfgang Witte for strain E. faecium 64/3.
This work was partially financed by a grant from the Polish Committee
for Scientific Research (grant KBN 4P05A 016 19) and by the U.S.-Poland
Maria Sklodowska-Curie Joint Found II (grant MZ/NIH-98-324).
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Sera & Vaccines
Central Research Laboratory, ul. Chemska 30/34, 00-725 Warsaw,
Poland. Phone: (48) 22-841 33 67. Fax: (48) 22-841 29 49. E-mail:
waleria{at}urania.il.waw.pl.
| |
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Journal of Clinical Microbiology, February 2001, p. 811-815, Vol. 39, No. 2
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.2.811-815.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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