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Journal of Clinical Microbiology, June 2000, p. 2108-2111, Vol. 38, No. 6
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Evaluation of a New System, VITEK 2, for
Identification and Antimicrobial Susceptibility Testing of
Enterococci
Fernando
Garcia-Garrote,
Emilia
Cercenado,* and
Emilio
Bouza
Servicio de Microbiología, Hospital
General Universitario "Gregorio Marañón," Madrid, Spain
Received 3 January 2000/Returned for modification 2 February
2000/Accepted 9 March 2000
 |
ABSTRACT |
We evaluated the new automated VITEK 2 system (bioMérieux)
for the identification and antimicrobial susceptibility testing of
enterococci. The results obtained with the VITEK 2 system were compared
to those obtained by reference methods: standard identification by the
scheme of Facklam and Sahm [R. R. Facklam and D. F. Sahm, p.
308-314, in P. R. Murray et al., ed., Manual of
Clinical Microbiology, 6th ed., 1995] and with the API 20 STREP
system and, for antimicrobial susceptibility testing, broth
microdilution and agar dilution methods by the procedures of the
National Committee for Clinical Laboratory Standards. The presence of
vanA and vanB genes was determined by PCR. A
total of 150 clinical isolates were studied, corresponding to 60 Enterococcus faecalis, 55 Enterococcus faecium, 26 Enterococcus gallinarum, 5 Enterococcus
avium, 2 Enterococcus durans, and 2 Enterococcus raffinosus isolates. Among those isolates, 131 (87%) were correctly identified to the species level with the VITEK 2 system. Approximately half of the misidentifications were for E. faecium with low-level resistance to vancomycin, identified as
E. gallinarum or E. casseliflavus; however, a
motility test solved the discrepancies and increased the agreement to
94%. Among the strains studied, 66% were vancomycin resistant (57 VanA, 16 VanB, and 26 VanC strains), 23% were ampicillin resistant
(MICs,
16 µg/ml), 31% were high-level gentamicin resistant, and
45% were high-level streptomycin resistant. Percentages of agreement for susceptibility and resistance to ampicillin, vancomycin, and teicoplanin and for high-level gentamicin resistance and high-level streptomycin resistance were 93, 95, 97, 97, and 96%, respectively. The accuracy of identification and antimicrobial susceptibility testing
of enterococci with the VITEK 2 system, together with the significant
reduction in handling time, will have a positive impact on the work
flow of the clinical microbiology laboratory.
 |
INTRODUCTION |
Enterococci are part of the normal
gastrointestinal flora of humans. Most clinical isolates of enterococci
represent colonizing rather than infecting organisms; however, they can
cause more serious infections and are sometimes responsible for
cholecystitis, cholangitis, peritonitis, septicemia, endocarditis, and
meningitis (9, 11). These infections are often difficult to
treat because of the intrinsic and acquired resistance of enterococci
to multiple antimicrobial agents (9, 12). Due to the
increasing frequency with which multidrug-resistant enterococci are
isolated from clinical specimens, there is a need for rapid reporting
of results of identification tests and tests for susceptibility to
antimicrobial agents. The contribution of rapid reporting of
microbiology results must be recognized since it provides both clinical
and financial benefits (2). The VITEK 2 system is a new
automated system designed to provide rapid and accurate identification
and susceptibility testing results for most clinical isolates including
enterococci. Identification is made on the basis of biochemical
reactions, and MIC determinations are made by applying an algorithm to
the growth kinetics monitored by the VITEK 2 system
(10; A. Bassel, R. Makkar, D. Freiner, J. L. Balzer, and D. Pincus, Abstr. 8th Eur. Congr. Clin. Microbiol. Infect.
Dis., abstr. P255, p. 53, 1997; W. H. F. Goessens, H. J. A. Van Vliet, and H. A. Verbrugh, Abstr. 9th Eur. Congr.
Clin. Microbiol. Infect. Dis., abstr. P822, p. 305, 1999).
In this study we evaluate the new automated VITEK 2 system
(bioMérieux, Marcy l'Etoile, France) for the identification and antimicrobial susceptibility testing of enterococci and compare the
results obtained with the VITEK 2 system with those obtained by
reference methods.
(This study was presented at the 39th Interscience Conference on
Antimicrobial Agents and Chemotherapy, San Francisco, Calif., 26 to 29 September 1999 [F. García-Garrote, E. Cercenado, and E. Bouza,
Abstr. 39th Intersci. Conf. Antimicrob. Agents Chemother., abstr. 882, p. 210, 1999].)
 |
MATERIALS AND METHODS |
Microorganisms.
We studied a total of 150 clinical isolates
that belong to our laboratory collection of enterococci. Among those,
125 isolates were recovered in our clinical microbiology laboratory
over a period of 10 years, and 25 were sent from other institutions in Spain. This collection studied included 60 Enterococcus
faecalis, 55 Enterococcus faecium, 26 Enterococcus gallinarum, 5 Enterococcus avium, 2 Enterococcus durans, and 2 Enterococcus
raffinosus isolates. None of the isolates were epidemiologically
related. The E. gallinarum isolates were recovered from
feces (24 isolates) and peritoneal fluid (2 isolates), and the origins
of the remaining isolates were urine (30 isolates), wounds (30 isolates), abscesses (18 isolates), blood (17 isolates), peritoneal
fluid (12 isolates), bile (7 isolates), and miscellaneous sites (10 isolates). Most of the isolates were chosen for the study for their
specific mechanisms of resistance: 66% were vancomycin resistant (57 VanA, 16 VanB, and 26 VanC isolates), 23% were ampicillin resistant
(MICs,
16 µg/ml), 31% were high-level gentamicin resistant (HLGR),
and 45% were high-level streptomycin resistant (HLSR).
Identification and susceptibility testing. (i) Standard
procedures.
All microorganisms had previously been identified by
two standard procedures: by the scheme of Facklam and Sahm
(8) and with the API 20 STREP system (bioMérieux)
(6). Disagreements between the retrospective reference
results and the VITEK 2 system results were solved by repeating the
identification with the API 20 STREP system and a motility test.
Susceptibility testing was previously performed by two methods: the
broth microdilution method and the agar dilution method with
Mueller-Hinton broth and agar, respectively, according to the
recommendations of the National Committee for Clinical Laboratory
Standards (14). The antimicrobial agents tested were
ampicillin, teicoplanin, and vancomycin at twofold concentrations from
0.25 to 256 µg/ml, gentamicin at 250 and 500 µg/ml, and
streptomycin at 1,000 and 2,000 µg/ml. Discrepancies between these
reference results and the VITEK 2 system results were solved by the
microdilution method. The presence of vanA and
vanB genes was confirmed by PCR as described previously
(4). Isolates were considered to have the VanC phenotype of
resistance to glycopeptides according to biochemical characteristics, a
positive motility test result, and low-level resistance to vancomycin
and susceptibility to teicoplanin.
(ii) VITEK 2 system.
The VITEK 2 system (bioMérieux)
is an integrated modular system that consists of a filling-sealer unit,
a reader-incubator, a computer control module, a data terminal, and a
multicopy printer. The system detects bacterial growth and metabolic
changes in the microwells of thin plastic cards by using a
fluorescence-based technology. Different microwell cards contain
antibiotics or biochemical substrates. We used the ID-GPC card of the
VITEK 2 system for identification and the AST-P516 card of the VITEK 2 system for the antimicrobial susceptibility testing of enterococci. The
ID-GPC card is a 64-well plastic card that contains 18 empty wells and 46 wells for fluorescent biochemical and inhibitory tests, as follows:
22 enzymatic tests for aminopeptidases and -osidases. Substrates used
for the detection of aminopeptidases are coupled with
7-amino-methylcoumarin (7AMC); substrates for the detection of
-osidases are usually coupled with 4-methylumbelliferone (4MU). The 22 test substrates are as follows:
4MU-
-L-arabinofuranoside, 4MU-
-D-galactoside, 4MU-
-D-glucoside,
4MU-
-D-N-acetylneuraminic acid,
4MU-
-D-galactoside, 4MU-
-D-glucoside,
4MU-
-D-glucuronide, 4MU-
-D-mannoside,
4MU-N-acetyl-
-D-glucosaminide, 4MU-phosphate, alanine-7AMC, arginine-7AMC, aurease
(butiloxicarbonyl-Val-Pro-Arg-AMC), histidine-7AMC,
-glutamic
acid-7AMC, threonine-7AMC, leucine-7AMC, lysine-7AMC,
phenylalanine-7AMC, proline-7AMC, pyroglutamic acid-7AMC, and
tyrosine-7AMC. Furthermore, the ID-GPC card includes 16 fermentation tests (for D-raffinose, amygdaline, arbutine,
D-galactose, glycerol, D-glucose,
L-arabinose, lactose, D-maltose,
D-mannitol, N-acetylglucosamine, salicin,
D-sorbitol, D-trehalose,
D-melibiose, and D-xylose), 2 decarboxylase
tests (for ornithine and arginine), and 6 miscellaneous tests (for
urease, pyruvate, optochin, novobiocin, polymyxin B sulfate, and 6.5%
NaCl). The AST-P516 card is a 64-well plastic card that contains the
following 20 antimicrobial agents with different concentrations:
ampicillin (0.5, 4, 8, and 32 µg/ml), ampicillin-sulbactam (4/2, 8/4,
16/8, and 64/16 µg/ml), benzylpenicillin (0.125, 0.25, 1, 2, 8, and
64 µg/ml), cefuroxime (4, and 8 µg/ml), ciprofloxacin (1, 2, and 4 µg/ml), clindamycin (0.5, 1, and 2 µg/ml), erythromycin (0.25, 0.5, and 2 µg/ml), gentamicin, high level (150 µg/ml), imipenem (8, 16, and 32 µg/ml), kanamycin, high level (200 µg/ml), levofloxacin
(0.25, 2, and 8 µg/ml), nitrofurantoin (16, 32, and 64 µg/ml),
norfloxacin (0.5, 1, and 4 µg/ml), ofloxacin (0.5, 2, and 4 µg/ml),
quinupristin-dalfopristin (0.25, 0.5, and 2 µg/ml), streptomycin,
high level (200 µg/ml), teicoplanin (1, 4, 8, and 16 µg/ml),
tetracycline (0.5, 1, and 2 µg/ml), trimethoprim-sulfamethoxazole (160, 320, and 640 µg/ml), and vancomycin (2, 4, and 6 µg/ml). For
this study we evaluated the performance of the VITEK 2 system for
testing of susceptibility only to ampicillin, vancomycin, and
teicoplanin and for testing for HLGR and HLSR.
Each organism suspension was prepared from the growth of pure cultures
of bacteria cultivated for 18 to 24 h on Columbia agar with 5%
sheep blood. The handling time was very short: suspensions were
prepared in sterile saline (0.45% NaCl) to a turbidity equivalent to
that of a 0.5 McFarland standard. These suspensions were used for the
inoculation of both cards (ID-GPC and AST-P516). The cards were
manually situated, as were the suspensions, in plastic racks that were
inserted in the VITEK 2 system's reader-incubator module (incubation
temperature, 35.5°C). The cards were automatically filled by a vacuum
device and were automatically sealed and subjected to a kinetic
fluorescence measurement every 15 min. The results were interpreted by
the ID-GPC database after an incubation period of 4 h, and final
results were obtained automatically after a minimum of 4 h and a
maximum of 15 h of incubation. All cards used were automatically
discarded in a waste container. The ID-GPC database contained data on
the following species of Enterococcus: E. faecalis, E. faecium, E. durans, E. avium, E. hirae, and E. casseliflavus-E.
gallinarum.
Quality control strains.
E. faecalis ATCC 29212, Staphylococcus aureus ATCC 29213, and E. faecium
GE-1 (5) were used as quality control strains every day
during the evaluation of the VITEK 2 system.
Analysis of results. (i) Agreement.
The VITEK 2 system and
the reference method were considered to be in agreement when the
species identification of the VITEK 2 system agreed exactly with the
species identification of the reference method.
(ii) Essential agreement.
MICs obtained with the VITEK 2 system and by the reference methods were considered to be in essential
agreement when the MIC obtained with the VITEK 2 system was within 1 twofold dilution of the reference MIC obtained by either the
microdilution method or the agar dilution method. In the case of
high-level resistance to aminoglycosides, "category agreement"
occurred when the categorization of high-level resistance with the
VITEK 2 system coincided with the results obtained by the reference methods.
(iii) MIC discrepancies.
MIC discrepancies were considered
"very major" (the VITEK 2 system indicated susceptible and the
reference method indicated resistant), "major" (the VITEK 2 system
indicated resistant and the reference method indicated susceptible),
and "minor" (the VITEK 2 system indicated intermediate and the
reference method indicated susceptible or resistant, or the VITEK 2 system indicated susceptible or resistant and the reference method
indicated intermediate).
 |
RESULTS |
Identification.
Among the 150 isolates, 131 were correctly
identified to the species level (agreement, 87%). For 19 strains
(13%) the species identification with the VITEK 2 system was
discrepant with the identification by the reference methods (Table
1). Approximately half of the
misidentifications were due to E. faecium with low-level resistance to vancomycin, identified as E. gallinarum-E. casseliflavus, and a simple motility test
solved the discrepancies and increased the agreement to 94%. However,
although the system flagged these identifications as "low
probability" or "acceptable," with type indices being between
0.25 and 0.66, the system nevertheless suggested complementary motility
test results. In addition, two isolates of E. raffinosus
were incorrectly identified, since the database of the system does not
include data for this species.
Susceptibility testing.
Percentages of agreement for
susceptibility and resistance to ampicillin, vancomycin, teicoplanin,
gentamicin (high level), and streptomycin (high level) (essential
agreement) were 93, 95, 97, 97, and 96%, respectively (Table
2). Among the vancomycin-resistant strains, the essential agreement was 93%. The VITEK 2 system detected 93 of 99 resistant isolates, including 96% VanA, 81% VanB, and 96%
VanC isolates. The discrepancies between the results obtained with the
VITEK 2 system and the reference method are listed in Table 2. For two
strains in which vancomycin resistance was not detected (one VanB
strain and one VanC strain), the species identifications were also
incorrect. The very major error rate ranged from 4% for vancomycin to
1.3% for ampicillin, teicoplanin, and gentamicin (high level). Nine
ampicillin-susceptible E. faecalis isolates were categorized
as ampicillin resistant by the VITEK 2 system. A
beta-lactamase-positive E. faecalis strain (13)
and an ampicillin-resistant beta-lactamase-negative E. faecalis strain (3) were not detected as resistant by
the VITEK 2 system. Two isolates that presented with HLGR were
incorrectly categorized with the system. Complete identification
results were obtained after 4 h of incubation for all except two
isolates, which required only 3 h, and complete susceptibility
testing results were obtained after a minimum of 6 h and a maximum
of 15 h of incubation. Results for 90% of isolates were complete
after 10 h of incubation (Table 3).
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TABLE 2.
Performance of the VITEK 2 system for susceptibility
testing of enterococci compared to that of the reference method
|
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[in this window]
[in a new window]
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TABLE 3.
Distribution of times needed to obtain the final results
of susceptibility testing with the VITEK 2 system
|
|
 |
DISCUSSION |
This evaluation of the VITEK 2 system for the identification and
susceptibility testing of enterococci was performed with a collection
of microorganisms that is not representative of the usual population
encountered in general in clinical laboratories, since the majority of
the microorganisms used for the evaluation of the system in this study
presented with resistance to vancomycin. In our laboratory, the
incidence of vancomycin-resistant enterococci (VRE) in the last 10 years has ranged from 0.5 to 0.7% (1 to 11% among E. faecium isolates and 0 to 1% among E. faecalis
isolates), and in a recent study of the prevalence of intestinal
colonization in our institution, the rate of colonization with VRE was
4.5% (E. Cercenado, L. Alcalá, B. Padilla, F. García-Garrote, L. Torres, and E. Bouza, Abstr. 9th Eur. Congr.
Clin. Microbiol. Infect. Dis., abstr. P147, p. 124, 1999). However, our
data suggest that the VITEK 2 system performs equally well for
susceptible and resistant isolates, and there is no evidence that the
accuracy of the results differed significantly between the susceptible and resistant groups (Table 2). The enterococcal species included in
the study (with the exception of E. raffinosus) are those
most frequently encountered in a clinical laboratory, and the rate of
accurate identification to the species level was 87%. This rate is
only acceptable, and the performance of a simple supplementary motility
test increased the agreement to 94%, which is, in our view, accurate,
although for these isolates the identification time increased by
15 h. However, the system failed to suggest a complementary
motility test, although it did flag these identifications as "low
probability." So, in order to confirm the results, we recommend
routine performance of the motility test whenever the VITEK 2 system
reports E. gallinarum or E. casseliflavus as an identification, unless future upgrades of the database will be available. The system also needs upgrades concerning the enterococcal species data in the database, since data for very few species are
included. When attempting to determine the performance of an automated
identification system, one should consider the publications that have
evaluated or compared the latest software, database, biochemical
configuration, or other performance characteristics of the system. To
our knowledge, very few studies have evaluated the VITEK 2 system for
the identification of enterococci. Our results fell within the range
obtained by others, who have demonstrated a correlation of between 83 and 95.3% for the results obtained with the VITEK 2 system compared
with those obtained by the reference methods (Bassel et al., Abstr. 8th
Eur. Congr. Clin. Microbiol. Infect. Dis.; E. Halle, I. Klare, and
U. B. Göbel, Abstr. 9th Eur. Congr. Clin. Microbiol. Infect.
Dis., abstr. P147A, addendum, 1999; K. Szczypa, M. Kawalec, A. Kuzimska, and T. Kaminska, Abstr. 9th Eur. Congr. Clin. Microbiol.
Infect. Dis., abstr. P31, p. 92, 1999).
In our study, the VITEK 2 system correctly detected 94% of
glycopeptide-resistant enterococci, including those with the VanA, VanB, and VanC phenotypes of resistance. The system failed to detect
two VanA isolates, three VanB isolates, and one VanC isolate. A few
studies have evaluated this system for the determination of the
susceptibilities of enterococci to vancomycin and teicoplanin, and the
results obtained were similar to ours (Halle et al., Abstr. 9th Eur.
Congr. Clin. Microbiol. Infect. Dis.; B. König, A. Parkner, and
A. König, Abstr. 9th Eur. Congr. Clin. Microbiol. Infect. Dis.
abstr. P32, p. 92-93, 1999; J. Rader, C. Bradford, D. Leahart, M. Ullery, and J. Gerst, Abstr. 98th Gen. Meet. Am. Soc. Microbiol. 1998, abstr. C357, p. 113, 1998; Szczypa et al., Abstr. 9th Eur. Congr. Clin.
Microbiol. Infect. Dis.), demonstrating that the VITEK 2 system
accurately detects glycopeptide resistance. The results of the VITEK 2 system for the detection of HLGR and HLSR strains were highly
correlated with those of the reference methods, with a very major error
rate (false-susceptible result for a resistant isolate) of 1.3% for
gentamicin and no very major errors for streptomycin. Previous studies
have demonstrated similar results, with very major error rates between
0 and 1.5% (W. McLaughlin, C. Schubert, R. Griffith, M. Sanders, and
M. Peyret, Abstr. 98th Gen. Meet. Am. Soc. Microbiol. 1998, abstr.
C358, p. 113, 1998; L. A. Meeh, C. Schubert, S. Weber, P. Kim, and
M. Peyret, Abstr. 98th Gen. Meet. Am. Soc. Microbiol. 1998, abstr. V66,
p. 105, 1998). The detection of ampicillin-resistant enterococci with
the VITEK 2 system was accurate. Of the two isolates with very major
errors, one was a beta-lactamase-positive strain; however, the MIC
determined by the system was correct. It is well known that
beta-lactamase detection among enterococci is inoculum dependent and
the error could be due to a low inoculum (16). On the other
hand, the classification of nine ampicillin-susceptible E. faecalis strains as resistant indicates that the system needs
further improvement. Other studies have demonstrated discrepant results
concerning the detection of ampicillin-resistant enterococci with the
VITEK 2 system, indicating that the algorithm for ampicillin must be adapted accordingly (Halle et al. and Szczypa et al., Abstr. 9th Eur.
Congr. Clin. Microbiol. Infect. Dis.). In comparison with the
AutoMicrobic system (1, 7, 15; N. Schiminsky and P. Ferrieri, Abstr. 87th Annu. Meet. Am. Soc. Microbiol. 1987, abstr. C94,
p. 339, 1987), the old version of the VITEK 2 system, the new version
has the advantage of a shorter handling time and the more rapid
identification and susceptibility testing of enterococci.
In general, the VITEK 2 system is an easy-to-handle system that
provides a rapid (4 to 15 h) and reasonably accurate means for the
identification of most commonly isolated species of
Enterococcus and accurately detects resistance to ampicillin
and glycopeptides and high-level resistance to gentamicin and
streptomycin among these species. However, the system needs further
improvement in its accuracy of identification, interpretation of
results, and database. One of the most important advantages of the
VITEK 2 system is the significant reduction in handling time, which
will have a positive impact on the work flow of the clinical
microbiology laboratory.
 |
FOOTNOTES |
*
Corresponding author. Mailing address: Servicio de
Microbiología, Hospital General Universitario "Gregorio
Marañón," Dr. Esquerdo 46, 28007 Madrid, Spain. Phone:
34-91-586-8459. Fax: 34-91-504-4906. E-mail:
fgarrote{at}efd.net.
 |
REFERENCES |
| 1.
|
Appelbaum, P. C.,
M. R. Jacobs,
J. I. Heald,
W. M. Palko,
A. Duffett,
R. Crist, and P. A. Naugle.
1984.
Comparative evaluation of the API 20S system and the AutoMicrobic system gram-positive identification card for species identification of streptococci.
J. Clin. Microbiol.
19:164-168[Abstract/Free Full Text].
|
| 2.
|
Barenfanger, J.,
C. Drake, and G. Kacich.
1999.
Clinical and financial benefits of rapid bacterial identification and antimicrobial susceptibility testing.
J. Clin. Microbiol.
37:1415-1418[Abstract/Free Full Text].
|
| 3.
|
Cercenado, E.,
M. F. Vicente,
M. D. Díaz,
C. Sánchez-Carrillo, and M. Sánchez-Rubiales.
1996.
Characterization of clinical isolates of -lactamase-negative, highly ampicillin-resistant Enterococcus faecalis.
Antimicrob. Agents Chemother.
40:2420-2422[Abstract].
|
| 4.
|
Dutka-Malen, S.,
S. Evers, and P. Courvalin.
1995.
Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR.
J. Clin. Microbiol.
33:24-27[Abstract].
|
| 5.
|
Eliopoulos, G. E.,
C. B. Wennersten,
S. Zighelboim-Daum,
E. Reiszner,
D. Goldmann, and R. C. Moellering, Jr.
1988.
High-level resistance to gentamicin in clinical isolates of Streptococcus (Enterococcus) faecium.
Antimicrob. Agents Chemother.
32:1528-1532[Abstract/Free Full Text].
|
| 6.
|
Facklam, R. R.,
D. L. Rhoden, and P. B. Smith.
1984.
Evaluation of the Rapid Strep system for the identification of clinical isolates of Streptococcus species.
J. Clin. Microbiol.
20:894-898[Abstract/Free Full Text].
|
| 7.
|
Facklam, R. R.,
G. S. Bosley,
D. Rhoden,
A. R. Franklin,
N. Weaver, and R. Schulman.
1985.
Comparative evaluation of the API 20S and AutoMicrobic gram-positive identification systems for non-beta-hemolytic streptococci and aerococci.
J. Clin. Microbiol.
21:535-541[Abstract/Free Full Text].
|
| 8.
|
Facklam, R. R., and D. F. Sahm.
1995.
Enterococcus, p. 308-314.
In
P. R. Murray, E. J. Baron, M. A. Pfaller, F. C. Tenover, and R. H. Yolken (ed.), Manual of clinical microbiology, 6th ed. American Society for Microbiology, Washington, D.C.
|
| 9.
|
French, G. L.
1998.
Enterococci and vancomycin resistance.
Clin. Infect. Dis.
27(Suppl. 1):S75-S83.
|
| 10.
|
Funke, G.,
D. Monnet,
C. deBernardis,
A. von Graevenitz, and J. Freney.
1998.
Evaluation of the VITEK 2 system for rapid identification of medically relevant gram-negative rods.
J. Clin. Microbiol.
36:1948-1952[Abstract/Free Full Text].
|
| 11.
|
Moellering, R. C., Jr.
1992.
Emergence of Enterococcus as a significant pathogen.
Clin. Infect. Dis.
14:1173-1178[Medline].
|
| 12.
|
Murray, B. E.
1990.
The life and times of the Enterococcus.
Clin. Microbiol. Rev.
3:46-65[Abstract/Free Full Text].
|
| 13.
|
Murray, B. E., and B. Mederski-Samoraj.
1983.
Transferable beta-lactamase: a new mechanism for in vitro penicillin resistance in Streptococcus faecalis.
J. Clin. Invest.
72:1168-1171.
|
| 14.
|
National Committee for Clinical Laboratory Standards.
1997.
Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 4th ed. Approved standard M7-A4.
National Committee for Clinical Laboratory Standards, Wayne, Pa.
|
| 15.
|
Ruoff, K. L.,
M. J. Ferraro,
M. E. Jerz, and J. Kissling.
1982.
Automated identification of gram-positive bacteria.
J. Clin. Microbiol.
16:1091-1095[Abstract/Free Full Text].
|
| 16.
|
Zscheck, K. Z., and B. E. Murray.
1993.
Genes involved in the regulation of beta-lactamase production in enterococci and staphylococci.
Antimicrob. Agents Chemother.
37:1966-1970[Abstract/Free Full Text].
|
Journal of Clinical Microbiology, June 2000, p. 2108-2111, Vol. 38, No. 6
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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Eigner, U., Schmid, A., Wild, U., Bertsch, D., Fahr, A.-M.
(2005). Analysis of the Comparative Workflow and Performance Characteristics of the VITEK 2 and Phoenix Systems. J. Clin. Microbiol.
43: 3829-3834
[Abstract]
[Full Text]
-
Funke, G., Funke-Kissling, P.
(2005). Performance of the New VITEK 2 GP Card for Identification of Medically Relevant Gram-Positive Cocci in a Routine Clinical Laboratory. J. Clin. Microbiol.
43: 84-88
[Abstract]
[Full Text]
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Tsai, J.-C., Hsueh, P.-R., Lin, H.-M., Chang, H.-J., Ho, S.-W., Teng, L.-J.
(2005). Identification of Clinically Relevant Enterococcus Species by Direct Sequencing of groES and Spacer Region. J. Clin. Microbiol.
43: 235-241
[Abstract]
[Full Text]
-
Kobayashi, I., Muraoka, H., Iyoda, T., Nishida, M., Hasegawa, M., Yamaguchi, K.
(2004). Antimicrobial susceptibility testing of vancomycin-resistant Enterococcus by the VITEK 2 system, and comparison with two NCCLS reference methods. J Med Microbiol
53: 1229-1232
[Abstract]
[Full Text]
-
Jackson, C. R., Fedorka-Cray, P. J., Barrett, J. B.
(2004). Use of a Genus- and Species-Specific Multiplex PCR for Identification of Enterococci. J. Clin. Microbiol.
42: 3558-3565
[Abstract]
[Full Text]
-
de Cueto, M., Ceballos, E., Martinez-Martinez, L., Perea, E. J., Pascual, A.
(2004). Use of Positive Blood Cultures for Direct Identification and Susceptibility Testing with the Vitek 2 System. J. Clin. Microbiol.
42: 3734-3738
[Abstract]
[Full Text]
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Donay, J.-L., Mathieu, D., Fernandes, P., Pregermain, C., Bruel, P., Wargnier, A., Casin, I., Weill, F. X., Lagrange, P. H., Herrmann, J. L.
(2004). Evaluation of the Automated Phoenix System for Potential Routine Use in the Clinical Microbiology Laboratory. J. Clin. Microbiol.
42: 1542-1546
[Abstract]
[Full Text]
-
Bruins, M. J., Bloembergen, P., Ruijs, G. J. H. M., Wolfhagen, M. J. H. M.
(2004). Identification and Susceptibility Testing of Enterobacteriaceae and Pseudomonas aeruginosa by Direct Inoculation from Positive BACTEC Blood Culture Bottles into Vitek 2. J. Clin. Microbiol.
42: 7-11
[Abstract]
[Full Text]
-
Fahr, A.-M., Eigner, U., Armbrust, M., Caganic, A., Dettori, G., Chezzi, C., Bertoncini, L., Benecchi, M., Menozzi, M. G.
(2003). Two-Center Collaborative Evaluation of the Performance of the BD Phoenix Automated Microbiology System for Identification and Antimicrobial Susceptibility Testing of Enterococcus spp. and Staphylococcus spp.. J. Clin. Microbiol.
41: 1135-1142
[Abstract]
[Full Text]
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Horstkotte, M. A., Knobloch, J. K.-M., Rohde, H., Dobinsky, S., Mack, D.
(2002). Rapid Detection of Methicillin Resistance in Coagulase-Negative Staphylococci with the VITEK 2 System. J. Clin. Microbiol.
40: 3291-3295
[Abstract]
[Full Text]
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Ligozzi, M., Bernini, C., Bonora, M. G., de Fatima, M., Zuliani, J., Fontana, R.
(2002). Evaluation of the VITEK 2 System for Identification and Antimicrobial Susceptibility Testing of Medically Relevant Gram-Positive Cocci. J. Clin. Microbiol.
40: 1681-1686
[Abstract]
[Full Text]
-
Teng, L.-J., Hsueh, P.-R., Wang, Y.-H., Lin, H.-M., Luh, K.-T., Ho, S.-W.
(2001). Determination of Enterococcus faecalis groESL Full-Length Sequence and Application for Species Identification. J. Clin. Microbiol.
39: 3326-3331
[Abstract]
[Full Text]
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van den Braak, N., Goessens, W., van Belkum, A., Verbrugh, H. A., Endtz, H. P.
(2001). Accuracy of the VITEK 2 System To Detect Glycopeptide Resistance in Enterococci. J. Clin. Microbiol.
39: 351-353
[Abstract]
[Full Text]