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Journal of Clinical Microbiology, August 1998, p. 2187-2190, Vol. 36, No. 8
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Emergence of Vancomycin-Resistant Enterococci in
Australia: Phenotypic and Genotypic Characteristics of
Isolates
Jan M.
Bell,1,*
James C.
Paton,2 and
John
Turnidge1
National Antimicrobial Resistance
Surveillance Program at Women's and Children's
Hospital1 and
Molecular Microbiology
Unit, Women's and Children's Hospital,2 North
Adelaide, South Australia 5006, Australia
Received 29 January 1998/Returned for modification 12 March
1998/Accepted 24 April 1998
 |
ABSTRACT |
Enterococci with resistance to glycopeptides have recently emerged
in Australia. We developed multiplex PCR assays for vanA, vanB, vanC1, and vanC2 or
vanC3 in order to examine the genetic basis for vancomycin
resistance in Australian isolates of vancomycin-resistant Enterococcus faecium and E. faecalis (VRE). The
predominant genotype from human clinical E. faecium
isolates was vanB. The PCR van genotype was
consistent with the resistance phenotype in all but six cases. One
vanA E. faecalis isolate had a VanB phenotype, one
vanB E. faecium isolate had a VanA phenotype, and four
E. faecalis isolates were consistently negative for
vanA, vanB, vanC1, and
vanC2 or vanC3, even though they exhibited a
VanB phenotype. These four isolates were subsequently examined for the
presence of vanD by published methods and were found to be
negative. No vancomycin-susceptible strains produced a PCR product. On
the basis of our findings the epidemiology of VRE in Australia appears to be different from that in either the United States or Europe. Our
multiplex PCR assays gave a rapid and accurate method for determining
the genotype and confirming the identification of glycopeptide-resistant enterococci. Rapid and accurate methods are
essential, because laboratory-based surveillance is critical in
programs for the detection, control, and prevention of the transmission
of glycopeptide-resistant enterococci.
| |
INTRODUCTION |
Vancomycin-resistant
Enterococcus faecium and E. faecalis (VRE) were
first described in Britain in 1988 (22) and soon afterward were reported from other European countries and the United States (14). In the United States they have become major nosocomial pathogens, rising in incidence from 0.3% in 1989 to 7.9% in 1993, as
reported by the Centers for Disease Control and Prevention (5), and among patients in intensive care units they now
represent 14% of isolates of enterococci retrieved from cultures of
blood (5). Resistance to multiple antimicrobial agents as
well as vancomycin, especially ampicillin and high levels of
aminoglycosides, is typical of these isolates (15).
Two principal phenotypes of acquired vancomycin resistance have been
described, VanA and VanB, encoded by two distinct gene clusters, the
vanA and vanB clusters, respectively, which are carried on transposons Tn1546 and Tn1547,
respectively (3). The VanA phenotype confers high-level
resistance to both vancomycin and teicoplanin, while the VanB phenotype
confers moderate to high-level resistance to vancomycin only. A third
type of vancomycin resistance, termed VanC, has been known for many
years to be a natural (intrinsic) vancomycin resistance found in the
motile enterococci E. casseliflavus, E. gallinarum, and E. flavescens (3). VanC
confers low-level resistance to vancomycin only. Unlike E. faecalis and E. faecium, the motile enterococci are infrequent pathogens in humans.
The troublesome features of enterococci with the VanA and VanB
phenotypes include their high propensity for cross-infection and the
resistance of many strains to all conventional agents. The
demonstration that the vanA gene cluster can be transferred to Staphylococcus aureus in vitro and in vivo is further
cause for concern (18).
The rapid emergence of VRE in the United States has been attributed to
the intensive clinical use of vancomycin in both parenteral and oral
forms in that country (13) on a background of high-level usage of cephalosporins, which promote enterococcal superinfection (16, 23). In Europe, investigators have postulated an
additional role for the use of the glycopeptide avoparcin as a growth
promoter in intensive animal industries, resulting in colonization with VanA E. faecium and subsequent transmission to humans via
the food chain (1).
The first vancomycin-resistant E. faecium isolate in
Australia was isolated from a liver transplant recipient in Melbourne in 1994 (12). Since March 1996 multiple isolates of
vancomycin-resistant E. faecium and vancomycin-resistant
E. faecalis have occurred throughout Australia. Only a few
of these strains have been reported in the literature (4, 8, 9,
19).
The National Antimicrobial Resistance Surveillance Program at the
Women's and Children's Hospital in Adelaide is a referral center for
antimicrobial resistance in Australia, and we have collected isolates
from virtually all patients known to have VRE infections that have
occurred since 1994. In order to characterize these strains further we
have developed multiplex PCR assays for vanA,
vanB, vanC1, and vanC2 or
vanC3 and have used these to examine the genetic basis for
vancomycin resistance in Australian isolates of VRE. The results have
been compared to those obtained by conventional susceptibility testing
with glycopeptides.
| |
MATERIALS AND METHODS |
Bacterial strains.
Two hundred forty-eight isolates of
Enterococcus spp. referred to the National Antimicrobial
Resistance Surveillance Program were studied. Previously characterized
VRE strains were used as controls. These included E. faecalis ATCC 51299 (vanB; vancomycin MIC, 6 µg/ml;
teicoplanin MIC, 0.5 µg/ml), E. casseliflavus ATCC 25788 (vanC2; vancomycin MIC, 6 µg/ml; teicoplanin MIC, 0.75 µg/ml), E. gallinarum NCDO 2313 (vanC1;
vancomycin MIC, 12 µg/ml; teicoplanin MIC, 1 µg/ml), E. faecalis ATCC 19433 (vancomycin MIC, 1 µg/ml; teicoplanin MIC,
0.19 µg/ml), E. faecium ATCC 19434 (vancomycin MIC, 1 µg/ml; teicoplanin MIC, 0.75 µg/ml), and E. faecalis
E19 (12) (vanA; vancomycin MIC, >256
µg/ml; teicoplanin MIC, >256 µg/ml).
Identification and antimicrobial susceptibility testing.
Isolates were identified by a conventional test scheme (7).
A multiplex PCR assay based on the specific detection of genes encoding
D-alanine:D-alanine ligases (ddl)
(6) was used to confirm the identification of E. faecalis and E. faecium.
The MICs of vancomycin and teicoplanin were determined for each isolate
by the Etest (AB Biodisk, Solna, Sweden) method on Mueller-Hinton agar
(2, 11). The interpretative criteria of the National
Committee for Clinical Laboratory Standards (17) were used
to determine the susceptibilities of the isolates.
Vancomycin resistance gene typing by PCR.
Enterococci were
first grown overnight at 37°C in Todd-Hewitt broth, and then 1-ml
volumes were microcentrifuged and the pellet was resuspended in 200 µl of TE buffer (10 mM Tris-HCl, 1 mM EDTA [pH 8.0]). The
suspensions were heated at 95°C for 20 min and then microcentrifuged
for 2 min. Five-microliter volumes of the supernatant were subjected to
PCR amplification in 50-µl reaction mixtures containing each
deoxynucleoside triphosphate at a concentration of 200 µM, each
primer at a concentration of approximately 1 µM, and 1 U of
Taq polymerase (Boehringer Mannheim) in 10 mM Tris-HCl (pH
8.3)-50 mM KCl-2 mM MgCl2-0.1% gelatin-0.1% Tween
20-0.1% Nonidet P-40. The samples were subjected to 35 PCR cycles,
each consisting of 1 min of denaturation at 94°C, 2 min of annealing at 60°C, and 2 min of elongation at 72°C. PCRs were analyzed by electrophoresis on 2% agarose gels and were stained with ethidium bromide. The oligonucleotide primers used for detection of
vanA, vanB, vanC1, and
vanC2 or vanC3 sequences were designed with
reference to the sequences deposited in GenBank by P. Courvalin and
colleagues under accession numbers X56895, L06138, M75132, L29638, and
L29639, respectively. Primer sequences and specificities are presented
in Table 1. For each sample, two PCRs
were set up. One contained primers VanABF, VanAR, and VanBR, which
direct amplification of 231- and 330-bp fragments from the
vanA and vanB genes, respectively. The other
contained primers VanC1F, VanC1R, VanC23F, and VanC23R, which direct
amplification of 447- and 597-bp fragments from the vanC1
gene and either the vanC2 or the vanC3 gene,
respectively. Multiplex PCRs were tested in duplicate. Known positive
and negative controls were also included with each PCR run.
Genotype-negative VRE isolates, for which vancomycin MICs were >4
µg/ml, were also tested for the presence of
vanD by using
the primers described by Perichon et al. (
20).
| |
RESULTS |
Characterization of multiplex PCR assays for vanA,
vanB, vanC1, and vanC2 or
vanC3.
In order to confirm the specificities of the various
PCR primers listed in Table 1, representative reference VRE isolates and vancomycin-susceptible enterococci were analyzed as described in
Materials and Methods (Fig. 1). Clear PCR
products of the expected size (231, 330, 447, and 597 bp for
vanA, vanB, vanC1 and vanC2 or vanC3, respectively) were obtained. There was 100%
agreement between the PCR results and the previously published
genotypes and phenotypes.
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|
FIG. 1.
PCR analysis of VRE. Enterococci were subjected to PCR
analysis, as described in Materials and Methods, with primers VanABF,
VanAR, and VanBR (A) or VanC1F, VanC1R, VanC23F, and VanC23R (B). The
PCR mixtures were electrophoresed on 2% agarose gels and stained with
ethidium bromide. Lanes: 1, E. faecalis ATCC 51299; 2, E. faecium ATCC 19434; 3, E. faecalis 91; 4, E. faecalis 3; 5, E. faecium 143; 6, E. faecium 135; 7, E. gallinarum 129; 8, E. casseliflavus 38; 9, E. faecalis 26; 10, E. faecalis 21; 11, E. faecium 30. Lane M1,
pUC19 DNA digested with HpaII (fragments of 501 and 489, 404, 331, 242, 190, and 147 bp are visible); lane M2,
bacteriophage SPP1 DNA digested with EcoRI (fragments of
1,950, 1,860, 1,510, 1,390, 1,160, 980, 720, 480, and 360 bp are
visible.
|
|
PCR analysis of Australian enterococci.
A total of 139 VRE
isolates from 14 institutions in seven cities (Adelaide, Brisbane,
Darwin, Melbourne, Newcastle, Perth, and Sydney) throughout all
mainland states of Australia were obtained. The VRE were either human
clinical isolates (n = 41) or isolates from the
contacts of index patients (n = 63), the environment (n = 33), or animals (n = 2). Other
referred Enterococcus spp. were clinical isolates
(n = 89) or were from animals (n = 20). The results of PCR analysis of the van genotype are
presented in Table 2. PCR van
genotype results for E. faecalis and E. faecium isolates were consistent with the resistance phenotype for all but six
isolates. The discrepancies were as follows: one vanA E. faecalis isolate with the VanB phenotype, one vanB E. faecium isolate with the VanA phenotype, and four E. faecalis isolates consistently negative for vanA,
vanB, vanC1, vanC2 or
vanC3, and vanD, even though they exhibited a
VanB phenotype. No vancomycin-susceptible strains produced a PCR
product. All E. faecium (n = 133) and
E. faecalis (n = 60) isolates were correctly
identified by PCR with the ddl primers. Using the
vanC1 and vanC2 or vanC3 primers, we further confirmed the identification of 42 E. gallinarum and
9 E. casseliflavus isolates. Of the 41 VRE isolates noted as
index isolates by the sending institution, 23 (56%) were E. faecium vanB, 7 (17%) were E. faecium vanA, 6 (15%)
were E. faecalis vanB, 3 were van-negative
E. faecalis, and 2 were E. faecalis vanA.
The vancomycin and teicoplanin susceptibility results are presented in
Table
3. Interestingly, one
E. faecium isolate and
three
E. faecalis isolates with
intermediate resistance to vancomycin
(MICs, 8 to 16 µg/ml) were PCR
positive for
vanB. For the
E. faecalis vanA
isolate with the VanB phenotype referred to above, the teicoplanin
MIC
was 4 µg/ml. For the VanA
E. faecium isolate which was
vanB positive, the teicoplanin MIC was
256 µg/ml. For
the four VRE
isolates which were
van negative, the
vancomycin MICs were in
the range of 12 to 16 µg/ml.
| |
DISCUSSION |
The VRE isolated in Australia to date show considerable diversity
in their phenotypes, genotypes, and geographic locations. All four
combinations of genotype and species have been found, with the
commonest being E. faecium vanB. While the clinical profiles of VRE-affected patients appear to be similar to those recorded in the
United States and elsewhere (13), the predominance of E. faecium vanB rather than E. faecium vanA
suggests an epidemiology different from that in either Europe or the
United States.
The origin of VRE in Australia remains unclear. No strains appear to
have been imported, although one occurred in a liver transplant
recipient who was a New Zealand-born resident of Taiwan. This patient
had entered Australia specifically for transplantation a few days prior
to the procedure. E. faecalis of the VanB phenotype was
initially isolated from blood cultures after surgery. The patient was
treated with teicoplanin, but several days later a vancomycin-resistant
enterococcus was again isolated from blood cultures, with the isolate
identified as E. faecalis of the VanA phenotype. Genotyping
showed that both isolates possessed the vanB gene, and
subsequent ribotyping confirmed that the strains were identical. The
emergence of resistance to teicoplanin has been recorded previously,
albeit rarely (10).
The level of vancomycin use in Australia is relatively high and has
been increasing over the last decade. There is significant regional
variation in its use due to the variation in prevalence of
multidrug-resistant S. aureus (21). Australia is
also a high-level user of avoparcin as a growth promoter in the
intensive animal industries. It is possible that the novel epidemiology
of VRE in Australia may result from a combination of the high rates of use of vancomycin and avoparcin in humans and animals, respectively.
PCR methods have previously been used for the rapid identification of
the vancomycin resistance genotype (6). In the present study
we designed a set of PCR primers that provides for the simultaneous identification of all the major van genotypes under
identical amplification conditions. Our multiplex van PCR
assays were rapid and simple, giving clear-cut answers within 6 h.
On the basis of phenotypic analysis, no false-positive results were
generated by this test. PCR analysis also indicated that MIC
determination alone is not sufficient for the unambiguous
classification of isolates of VRE. Also, difficulties continue to occur
with commercial identification systems, and the not infrequent
occurrence of nonmotile E. gallinarum and E. casseliflavus isolates and nonpigmented E. casseliflavus isolates compounds the problem. The ddl
PCR was extremely useful for the identification of E. faecalis and E. faecium and, in combination with
vanC1 and vanC2 or vanC3 PCR, for the
identification of E. gallinarum and E. casseliflavus. It is essential to have a rapid and accurate method
for determination of the genotype and for confirmation of the
identification of glycopeptide-resistant enterococci, especially during
an outbreak or when performing surveillance for VRE. It is unlikely
that the four strains with the VanB resistance phenotype that appeared to lack vanA, vanB, vanC1, and
vanC2 or vanC3 or even the recently described
vanD (20) were false-negative isolates (e.g., had the VanB resistance phenotype due to minor sequence variations in the
primer annealing sites), because PCR analysis with independent vanA and vanB primers (6) was also
negative. All four strains (from three patients) came from a single
institution and gave two distinct pulsed-field gel electrophoresis
patterns. Our results are consistent with either the existence of a
significant variant of a current van genotype or a novel
one. The van loci of these strains are undergoing further
analysis.
| |
ACKNOWLEDGMENTS |
We thank all the contributing laboratories throughout Australia
that provided enterococci for this study; the Gram-Positive Bacteria
Typing and Research Unit at Royal Perth Hospital and Curtin University
(Geoff Coombs, Cheryll McCullough, Todd Pryce, Ian Kay, and Frances
O'Brien) for providing some of the type strains, ribotyping, and
confirming the genotype of non-vanA, non-vanB, and non-vanC E. faecalis; and Barrie Mayall for providing
strain E19.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Microbiology and
Infectious Diseases Department, Women's and Children's Hospital, 72 King William Rd., North Adelaide, SA 5006, Australia. Phone: 61-8 8204 6359. Fax: 61-8 8204 6051. E-mail:
bellj{at}mail.wch.sa.gov.au.
| |
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Journal of Clinical Microbiology, August 1998, p. 2187-2190, Vol. 36, No. 8
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
