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Antimicrobial Agents and Chemotherapy, June 1998, p. 1406-1411, Vol. 42, No. 6
0066-4804/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Novel Antibiotic Susceptibility Tests by the ATP-Bioluminescence
Method Using Filamentous Cell Treatment
Noriaki
Hattori,1,*
Moto-O
Nakajima,1
Koji
O'Hara,2 and
Tetsuo
Sawai2
Research and Development Division, Kikkoman
Corporation, Chiba 278-0005,1 and
Division of Microbial Chemistry, Faculty of Pharmaceutical
Sciences, Chiba University, Chiba 263-8522,2
Japan
Received 16 July 1997/Returned for modification 25 November
1997/Accepted 1 April 1998
 |
ABSTRACT |
Antimicrobial susceptibility testing by the ATP-bioluminescence
method has been noted for its speed; it provides susceptibility results
within 2 to 5 h. However, several disagreements between the ATP
method and standard methodology have been reported. The present paper
describes a novel ATP method in a 3.5-h test which overcomes these
deficiencies through the elimination of false-resistance discrepancies
in tests on gram-negative bacteria with 
-lactam agents. In
our test model using Pseudomonas aeruginosa and
piperacillin, it was shown that ATP in filamentous cells accounted for
the false resistance. We found that 0.5%
2-amino-2-methyl-1,3-propanediol (AMPD) extracted ATP from the
filamentous cells without affecting normal cells and that 0.3 U of
adenosine phosphate deaminase (APDase)/ml simultaneously digested the
extracted ATP. We used the mixture of these reagents for the
pretreatment of cells in a procedure we named filamentous cell
treatment, prior to ATP measurements. This novel ATP method with the
filamentous cell treatment eliminated false-resistance discrepancies in
tests on P. aeruginosa with -lactam agents, including
piperacillin, cefoperazone, aztreonam, imipenem-cilastatin,
ceftazidime, and cefsulodin. Furthermore, this novel methodology
produced results which agreed with those of the standard microdilution
method in other tests on gram-negative and gram-positive bacteria,
including P. aeruginosa, Escherichia coli,
Staphylococcus aureus, and Enterococcus
faecalis, for non--lactam agents, such as fosfomycin,
ofloxacin, minocycline, and aminoglycosides. MICs obtained by the novel
ATP method were also in agreement with those obtained by the agar
dilution method of susceptibility testing. From these
results, it was shown that the novel ATP method could be used
successfully to test the activities of antimicrobial agents with the
elimination of the previously reported discrepancies.
| |
INTRODUCTION |
Bacteria resistant to multiple
antibiotics, such as methicillin-resistant Staphylococcus
aureus and vancomycin-resistant Enterococcus spp., have
been isolated with increasing frequency, and health care institutions
are in need of a rapid antimicrobial susceptibility test for
therapeutic, epidemiologic, and economic reasons. Standard susceptibility methods involving liquid media or agar plates, however,
require 18 to 24 h of incubation. The ATP-bioluminescence method
is an alternative technique that has been adopted in the quest for a
methodology which produces rapid results, and it has been widely
utilized for sanitation and hygiene monitoring (3, 24, 26).
Antimicrobial susceptibility testing by the ATP-bioluminescence method,
which requires only 2 to 5 h to perform, was first described in
work originating at the U.S. National Aeronautics and Space Administration (6) and in Sweden (8) in
1976. Although this method has been noted for its speed, it is
not now widely employed due to a lack of suitable instrumentation, the
prohibitive cost of reagents, and disagreement with results obtained
with standard methodology. Pseudomonas aeruginosa is
clinically one of the most important bacteria involved in opportunistic
infection and hospital infection, and rapid susceptibility testing
allowing the selection of suitable chemotherapy would be a valuable
tool. Many other species of bacteria include an increasing number of
strains resistant to many kinds of antibiotics. These problems
demonstrate the strong need for a rapid and practical means to
determine susceptibility to antimicrobial agents. The
ATP-bioluminescence method has been applied to the susceptibility
testing of gram-negative bacteria, including P. aeruginosa;
however, several discrepancies were noted when results obtained by the
ATP-bioluminescence method were compared to those obtained by standard
methodology in tests for some -lactam agents, including those that
are considered primary choices in chemotherapy directed against
P. aeruginosa. These disagreements, in which strains were
found resistant by the ATP susceptibility method but susceptible by the
standard method, were labeled false resistance (6, 31). It
has been suggested that these disagreements may be the result of the
delayed lysis of protoplasts or spheroplasts. The objective of this
study was to develop a rapid and simple procedure to eliminate the
false-resistance discrepancies noted with gram-negative bacteria,
especially P. aeruginosa, and -lactam agents. Moreover,
the general applicability of the rapid method was evaluated by
comparing it with the standard method in tests on other bacteria and
antimicrobial agents.
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MATERIALS AND METHODS |
Bacteria and culture medium.
Four reference strains,
P. aeruginosa ATCC 27853, Escherichia coli ATCC
25922, S. aureus ATCC 25923, and Enterococcus
faecalis ATCC 29212, were used. The culture medium was prepared
from Mueller-Hinton broth (Difco Laboratories, Detroit, Mich.) to which
were added 50 mg of Ca2+ and 25 mg of Mg2+ per
liter (20).
Antimicrobial agents.
The following -lactam agents were
tested: piperacillin (Sankyo Co., Ltd., Tokyo, Japan), cefoperazone
(Pfizer, Inc., New York, N.Y.), aztreonam (Eizai Co., Ltd., Tokyo,
Japan), imipenem-cilastatin (Banyu Pharmaceutical Co., Ltd., Tokyo,
Japan), ceftazidime (Tanabe Seiyaku Co., Ltd., Osaka, Japan),
cefsulodin (Takeda Chemical Industries, Ltd., Osaka, Japan), cefazolin
(Fujisawa Pharmaceutical Co., Ltd., Tokyo, Japan), ampicillin (Meiji
Seika Kaisha Ltd., Tokyo, Japan), and aspoxicillin (Tanabe Seiyaku Co.,
Ltd.). The following non--lactam antimicrobial agents were tested:
fosfomycin (Meiji Seika Kaisha Ltd.), gentamicin (Schering-Plough
Corporation, Madison, Wis.), tobramycin (Shionogi & Co., Ltd., Tokyo,
Japan), ofloxacin (Daiichi Pharmaceutical Co., Ltd., Tokyo, Japan),
minocycline (Lederle [Japan], Ltd., Tokyo, Japan), erythromycin
(Dainabot Co., Ltd., Tokyo, Japan), and chloramphenicol (Sankyo Co.,
Ltd.).
Growth curve by the ATP-bioluminescence method.
Several
colonies of bacteria from an overnight blood agar plate (Eiken Chemical
Co., Ltd., Tokyo, Japan) culture, incubated at 37°C, were suspended
in 1 ml of sterilized saline. The density of the suspension was
adjusted to McFarland standard 0.5, corresponding to approximately
108 CFU/ml. After a further 10-fold dilution, 50 µl was
inoculated into 5 ml of broth with or without 5 µg of piperacillin
per ml and was incubated at 37°C. A luciferin-luciferase-based
bioluminescence assay of ATP was performed every hour with a Lucifer LU
plus kit (Kikkoman Corporation, Chiba, Japan) according to the
following protocol. A 100-µl sample from the culture was mixed with
an equal volume of the kit's constituent ATP extractant. After 20 s, 100 µl of bioluminescence reagent (luciferin-luciferase) was added to the mixture, and the emitted light was measured with a luminometer, Lumat LB-9501 (EG & G Berthold, Wildbad, Germany). The intensity of
the bioluminescenct light was expressed as relative light units (RLU),
and it is well established that the light intensity is proportional to
the bacterial count (2). Morphological observation was
carried out simultaneously by using an aliquot withdrawn at the same
time, which was examined under a phase-contrast microscope, model BHS
(Olympus Optical Co., Ltd., Tokyo, Japan).
Screening of specific substances for ATP extraction from
filamentous cells of P. aeruginosa.
Thirty-seven substances
which have an amphipathic property, including surfactants and
emulsifying agents, were screened for their ability to extract ATP from
filamentous cells of P. aeruginosa. The filamentous cells
were obtained by incubating P. aeruginosa in broth with 5 µg of piperacillin per ml at 37°C for 3 h. A 50-µl solution
containing one of the amphipathic extractants at a concentration of
0.005 to 0.2% (wt/vol) in 25 mM Tricine buffer (pH 7.75) was added to
100 µl of the filamentous cell cultures. The cultures were left to
stand for 30 min at room temperature, and 50 µl of bioluminescence
reagent was added to the mixture, which was measured for emitted light.
In parallel, the same procedure was performed with P. aeruginosa cells in broth cultures without piperacillin to obtain
reference values. ATP extraction was calculated according to the
following equation: percent ATP extraction = (bioluminescence after the addition of the extractant substance/bioluminescence after
the addition of the buffer alone) × 100.
Antimicrobial susceptibility test.
Testing by the novel
ATP-bioluminescence susceptibility method was performed according to
the following procedure. A 5-µl inoculum from a culture
containing approximately 107 CFU of test bacteria/ml was
added to each well of a white 96-well microtitration plate (Dynex
Technologies, Inc., Chantilly, Va.) containing 100 µl of broth with
or without antimicrobial agents. After incubation at 37°C for 3 h, 50 µl of filamentous cell treatment solution, consisting of 0.5%
2-amino-2-methyl-1,3-propanediol (AMPD), 0.3 U of adenosine phosphate
deaminase (APDase)/ml, and 5 mM EDTA in 25 mM Tricine buffer (pH 7.75),
was added, and the plate was left standing for 30 min at room
temperature. Subsequently, 50 µl of ATP extractant, consisting of
0.2% benzalkonium chloride in 25 mM Tricine buffer (pH 7.75), was
added. After a further 20 s, 50 µl of bioluminescence reagent
reconstituted in 2.5% 
-cyclodextrine solution was added, and the
emitted light was measured with a 96-well microtitration plate
luminometer, ML-3000 (Dynex Technologies, Inc.). APDase included in the
filamentous cell treatment was denatured by the benzalkonium chloride
added in the subsequent ATP extraction step, thereby protecting the ATP
extracted from normal cells. Although benzalkonium chloride would
usually denature the luciferase in the bioluminescence reagent added
later, -cyclodextrine neutralizes this effect by forming an
inclusion complex (16). The ATP-bioluminescence was
expressed as an ATP index; ATP index = (bioluminescence in broth
with antimicrobial agent/bioluminescence in broth without antimicrobial
agent) × 100. The results were classified as negative (ATP index 
40), or positive (ATP index > 40). The MIC was determined in
broth with a twofold-dilution series of antimicrobial agents in the
range of 0.1 to 100 µg/ml. The MIC was defined as the lowest concentration of antimicrobial agent which resulted in a negative ATP
index in ATP-bioluminescent testing. The values were considered equivalent when they agreed, within 2 twofold-dilution values, with
those obtained by the standard methods.
Standard ATP-bioluminescence susceptibility testing was performed in
the same way as testing by the novel ATP method described above, except
that the filamentous cell treatment was not used.
In the standard microdilution method (20), 5 µl of
inoculum from a culture containing approximately 107 CFU of
the test bacteria/ml was added to each well of a transparent 96-well
microtitration plate (Costar, Cambridge, United Kingdom) containing 100 µl of broth with or without antimicrobial agents and was incubated at
37°C for 18 to 20 h. Wells in each antibiotic dilution series,
consisting of twofold dilutions of antimicrobial agent in the range of
0.1 to 100 µg/ml, were classified as negative (no growth), or
positive (growth). The MIC was recorded as the lowest concentration of
antimicrobial agent that inhibited visible growth.
In the standard agar dilution method (
10), a bacterial
inoculum from a culture containing approximately 10
6 CFU/ml
was transferred with a multipoint inoculator to Mueller-Hinton
agar
plates containing twofold dilutions of antimicrobial agents
in the
range of 0.1 to 100 µg/ml and was incubated at 37°C for
18 to
20 h. The MIC was recorded as the lowest concentration of
antimicrobial agent that inhibited visible growth.
| |
RESULTS |
Investigation of the basis of the false resistance demonstrated by
the standard ATP method.
Growth curves of E. coli and
P. aeruginosa were determined by measurements made by the
ATP-bioluminescence method in broth containing the -lactam agent
piperacillin at 5 µg per ml (Fig. 1).
Both microorganisms had the same piperacillin MIC of 3.13 µg/ml, and
therefore the concentration of piperacillin used for this study
corresponds to about 1.5 times the MIC for both microorganisms. A
concentration near the MIC is most suitable for analyzing the mechanism
of false-resistance discrepancies in further detail. With E. coli, bioluminescence in the medium containing piperacillin paralleled that of the control culture without piperacillin for the
first 2 h of incubation; however, it then decreased with further incubation. The bioluminescence of the culture containing piperacillin, following 3 h of incubation, decreased to less than 1/10 of that without piperacillin, with a resulting ATP index of less than 10%.
E. coli was therefore classified as negative (or
susceptible) in a 3-h test. These data agreed with the result expected
from the MIC. In contrast, with P. aeruginosa,
bioluminescence in the medium containing piperacillin remained at the
same level as in the drug-free culture for 4 h and subsequently
decreased little, even after several hours of further incubation. This
result indicated false resistance when compared with that expected from
the MIC. Following 20 h of incubation, however, which is the
incubation time required for the standard methodology, the
bioluminescence of the culture containing piperacillin decreased to
about 1/100 of that without piperacillin. The resultant ATP index was
about 1%, and accordingly, the susceptibility result by the
ATP-bioluminescence method, following the extended incubation time, now
correlated with that expected from the known MIC.
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FIG. 1.
Growth curves of E. coli ATCC 25922 (A) and
P. aeruginosa ATCC 27853 (B) by the standard
ATP-bioluminescence method in broth with (solid circles) or without
(open circles) 5 µg of piperacillin per ml, corresponding to 1.5 times the MIC for both organisms.
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When we microscopically observed cultures of
P. aeruginosa
exposed to piperacillin for 3 h, we discovered filamentous cells
which were approximately 30 times longer than normal cells. The
cells
continued to elongate with extended incubation. In further
studies it
was also confirmed that other
-lactam agents, such
as cefoperazone,
aztreonam, imipenem-cilastatin, ceftazidime,
cefsulodin, cefazolin,
carbenicillin, latamoxef, cefotaxime, flomoxef,
sulbactam-cefoperazone,
and cefuzonam, induced similar filamentation
of cells. These results,
taken together, suggested that the cells
of
P. aeruginosa
remained viable for several hours following their
conversion to the
filamentous form. We therefore concluded that
false-resistance
discrepancies in rapid tests on
P. aeruginosa with
-lactam agents were due to the delayed lysis of the filamentous
cells formed in these cultures.
Elimination of ATP in filamentous cells formed by -lactam
agents.
We considered that the false-resistance discrepancies
between the ATP-bioluminescence method and the standard microdilution method could be resolved by extracting and eliminating ATP from the
filamentous cells. We examined this possibility using filamentous cells
of P. aeruginosa which resulted from exposure to 5 µg of piperacillin/ml for 3 h. We began with an investigation of whether surfactants and emulsifying agents, which destroyed cell membrane integrity, could extract ATP from filamentous cells. From the data
obtained, three substances with the desired property were selected;
these are shown in Table 1. ATP
extraction above 100% means that the substance extracted ATP from
cells in an amount exceeding that extracted by buffer alone. In a
control culture without piperacillin, ATP extraction by either Triton
X-100, Amphitol, or AMPD was almost at the same level as that obtained
by the use of buffer alone. In contrast, in a culture containing
piperacillin, the levels of ATP extraction by these substances were
about 2 to 5 times higher than that by the buffer alone. From these
results, it was shown that these substances extracted ATP selectively
from filamentous cells and not from morphologically normal cells. It was found that AMPD combined this selectivity with the greatest effectiveness, and it was therefore used in subsequent experiments.
The optimal concentration of AMPD and the time required to extract ATP
from filamentous cells were next investigated. In Fig.
2A, the results summarized show that
increasing the concentration
of AMPD past 0.5% did not enhance the
bioluminescence over the
peak levels reached at this concentration. The
final selection
of a concentration of 0.5% was further supported by
the increasing
inhibition of luciferase activity with an increased
concentration
of AMPD (data not shown). In Fig.
2B, it can be seen that
ATP
was efficiently extracted from the filamentous cells following
20 to 30 min of exposure. It was therefore concluded that treatment
for 30 min using 0.5% AMPD was well suited for extraction of ATP
from the
filamentous cells. APDase has previously been reported
as a most
effective agent for the elimination of ATP (
25). We
confirmed that 0.3 U of APDase/ml could remove the ATP extracted
from
filamentous cells by AMPD (data not shown). The combination
of reagents
and procedures outlined above provided us with a simple
and rapid
pretreatment, which we named the filamentous cell treatment,
that might
be used to provide valid results from ATP-bioluminescence
susceptibility testing.
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FIG. 2.
Determination of optimal conditions for the extraction
of ATP from filamentous cells using AMPD. The optimal concentration of
AMPD (A) and the time required for extraction of ATP by 0.5% of AMPD
(B) are shown.
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A comparison of ATP-bioluminescence results with results of the
standard microdilution method.
The speed advantage of the novel
3.5-h ATP-bioluminescence susceptibility method was of value only if
the accuracy of the modified testing could be validated. In tests on
P. aeruginosa using seven different -lactam agents, it
was investigated whether the novel ATP-bioluminescence method would
eliminate false-resistance discrepancies compared with the standard
method. The susceptibility results were compared to those obtained by
the standard ATP-bioluminescence method and those obtained by the
microdilution method, as presented in Table
2. The standard ATP-bioluminescence
susceptibility method gave positive results, indicating resistance, at
all the concentrations of the agents tested, whereas the microdilution
method indicated complete susceptibility at all concentrations of the
same agents except for cefazolin (resistance at all concentrations) and
3 µg of aztreonam/ml. These results showed that the standard
ATP-bioluminescence susceptibility method caused many
false-resistance discrepancies compared with the microdilution
method in almost all tests. It was noted that the bioluminescence from
cultures including antimicrobial agents was greater than that of those
without, and especially with piperacillin and cefsulodin, the
dose-dependent effect was not observed. With the novel
ATP-bioluminescence method, in which ATP from filamentous cells was
digested, bioluminescence reflected only the ATP from normal cells and
the dose-dependent effect was observed. The results obtained by this
novel method were in perfect agreement with those obtained by the
microdilution method.
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TABLE 2.
Antimicrobial susceptibility tests of P. aeruginosa ATCC 27853 and -lactam agents by the novel
ATP-bioluminescence method, the standard ATP-bioluminescence method,
and the microdilution method
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The correlation between the three methods was further investigated in
tests on
P. aeruginosa with non-
-lactam agents and
on
three bacteria other than
P. aeruginosa with piperacillin,
aztreonam, ampicillin, imipenem-cilastatin, minocycline, and ofloxacin
(Table
3). In tests on
P. aeruginosa using fosfomycin, false-resistance
results were noted
by the standard ATP-bioluminescence susceptibility
method, but this
false resistance was eliminated in the novel
ATP-bioluminescence
susceptibility method. This result showed
that the novel method also
has a beneficial effect in tests on
fosfomycin, a non-
-lactam agent
which inhibits cell wall synthesis
as well as
-lactams do (
7,
11,
30). With
E. coli, the
standard
ATP-bioluminescence method indicated false resistance
with positive ATP
indices at 3 and 10 µg of aztreonam/ml; however,
the novel
ATP-bioluminescence method could resolve these. In contrast,
on
the gram-positive bacteria,
S. aureus ATCC 25923 and
E. faecalis ATCC 29212, the results of the
standard ATP method were in agreement
with those of the standard
microdilution method. The results of
the novel ATP method also
correlated well with those of the standard
method.
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TABLE 3.
Antimicrobial susceptibility tests by the novel
ATP-bioluminescence method, the standard ATP-bioluminescence method,
and the microdilution method
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MICs for
P. aeruginosa determined by the novel
ATP-bioluminescence susceptibility method were compared with those
obtained
by standard procedures, including the microdilution and agar
dilution
methods (Table
4). The MICs
obtained by the novel ATP-bioluminescence
method were in agreement with
those obtained by the standard methods
within 2 twofold-dilutional
increments, with the exception of
the MIC for minocycline determined by
the standard microdilution
method. These results validated the accuracy
of the novel ATP-bioluminescence
susceptibility testing method, which,
in a 3.5-h test, could be
reliably used to determine MICs in agreement
with those obtained
by standard microdilution testing requiring
overnight incubation.
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TABLE 4.
MICs for P. aeruginosa ATCC 27853 as
determined by the novel ATP-bioluminescence method, the
microdilution method, and the agar dilution method
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| |
DISCUSSION |
Several approaches have been investigated in the past for the
performance of rapid antibiotic susceptibility testing, including ATP-bioluminescence (6, 8, 9, 15, 18, 19, 22, 29, 31, 32),
turbidimetry (1), impedance (4), conductance (23), and radiometry (5). The ATP-bioluminescence
method was notable, because several difficulties related to reagents and instrumentation had been overcome (12, 13, 27, 28, 32).
In this study, we investigated a novel method to eliminate the
remaining technical problem of disagreements between the
ATP-bioluminescence susceptibility method and standard methodology.
We noted that the disagreements involved false-resistance discrepancies
in tests on gram-negative bacteria with -lactam agents. Several
approaches to eliminating false-resistance discrepancies had already
been investigated. Wheat et al. used low-osmolality broth to induce the
lysis of Proteus mirabilis spheroplasts. A much better
correlation was achieved with ampicillin and piperacillin (31). Limb et al. extended the time of incubation to 6 h for Mycoplasma spp. tested with ciprofloxacin, and good
correlation resulted (15). These methods, however, are
unsuited to the development of a simple and rapid susceptibility test.
In our investigations we began by determining the precise cause of the
false-resistance discrepancies. We noted that P. aeruginosa cells remained viable following conversion to their
filamentous form following 3 h of incubation in the presence of
antibiotics, and elongation increased over time. It was clear that ATP
in the filamentous cells could account for the false-resistance
discrepancies. We subsequently investigated a method to eliminate this
ATP from filamentous cells and derived our unique filamentous cell
treatment. The treatment reagents consisted of 0.5% AMPD, 0.3 U of
APDase/ml, and 5 mM EDTA in 25 mM Tricine buffer (pH 7.75). This
combination digested ATP from filamentous cells only without
affecting normal cells. In antimicrobial susceptibility testing by the
novel ATP-bioluminescence method on P. aeruginosa for
-lactam agents, the filamentous cell treatment eliminated
false-resistance discrepancies. The results agreed with those
obtained by the standard microdilution method, not only in tests
on gram-negative and gram-positive bacteria, but also for
non--lactam agents. These results strongly suggested that the
novel ATP-bioluminescence method was a practical test for a
variety of bacteria and antimicrobial agents and that it maintained simplicity and speed.
Recently, the ATP-bioluminescence method has been applied to antibiotic
susceptibility tests on Mycobacterium spp. (2, 21) and on microorganisms in biofilms (14), and for
assessing the postantibiotic effect (17). In tests on
gram-negative bacteria, poor correlation between the
ATP-bioluminescence susceptibility method and standard methods
was obtained because of morphological changes such as the production
of filamentous cells and spheroplasts. It is expected that the
novel ATP-bioluminescence susceptibility method described here would
eliminate these disagreements due to the filamentous cell treatment.
The speed of this method further addresses a clinical need for early
information regarding susceptibility tests and would allow feedback of
the susceptibility data to a physician in one day, resulting in lower
health care costs and the selection of better treatment regimens for
patients. The novel ATP-bioluminescence method described in this paper
is simple to perform because this method, distinct from those
previously described, does not require the use of centrifugation
and filtration to concentrate bacterial cells. A further
advantage of the novel method is its adaptability to fully automated
and cost-efficient testing, which results from the use of 96-well
microtitration plates in the performance of the test. Such automation
has the potential to provide susceptibility results devoid of variation
arising from the performance of individual technicians. As described
above, this novel ATP-bioluminescence method appears to be a technique
ideally suited to the clinical-microbiology laboratory. Our ongoing
studies will continue to evaluate the reliability and practicality of
the novel method in expanded tests involving more species of organisms
and more antimicrobial agents.
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ACKNOWLEDGMENTS |
We thank Eiji Yoshikawa and Isami Tsuboi (BML, Inc.,
Tokyo, Japan) for technical assistance in performing some of the
assays.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Noriaki Hattori,
Research and Development Division, Kikkoman Corporation, 399 Noda, Noda
City, Chiba Pref. 278-0005, Japan. Phone: 81-471-23-5522. Fax:
81-471-23-5550. E-mail: 8345{at}mail.kikkoman.co.jp.
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Antimicrobial Agents and Chemotherapy, June 1998, p. 1406-1411, Vol. 42, No. 6
0066-4804/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
