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Previous Article | Next Article 
Journal of Clinical Microbiology, April 1998, p. 1109-1112, Vol. 36, No. 4
0095-1137/98/$00.00+0
Sensitivity and Specificity of an Improved Rapid
Latex Agglutination Test for Identification of Methicillin-Sensitive
and -Resistant Staphylococcus aureus Isolates
Sandra C.
Smole,1,2
Elyssa
Aronson,2
Annette
Durbin,3
Stephen M.
Brecher,3,4 and
Robert D.
Arbeit1,2,4,*
Departments of
Medicine1 and
Microbiology,4
Boston University
School of Medicine, and Infectious Diseases Section, Medical
Service,2 and
Pathology and Laboratory
Medicine,3 Boston Veterans Affairs Medical
Center, Boston, Massachusetts 02130
Received 29 August 1997/Returned for modification 10 October
1997/Accepted 23 December 1997
 |
ABSTRACT |
The performance of a second-generation rapid agglutination kit,
Slidex Staph Plus (SSP; bioMérieux), was compared to those of the
Slidex Staph (SS; bioMérieux), Staphaurex (SRX; Murex Diagnostics), and BBL Staphyloslide (BBL; Becton Dickinson) kits by
using 508 clinical isolates composed of 150 methicillin-sensitive Staphylococcus aureus (MSSA) organisms, 154 methicillin-resistant S. aureus (MRSA) organisms, and 204 non-S. aureus Staphylococcus spp. Of the 508 isolates
tested, 75% were fresh clinical isolates, with the remainder taken
from five different freezer collections. All four agglutination tests
had comparable sensitivities for MSSA and MRSA. However, the SS kit was
significantly less specific (93.1%) than the three other tests
(P > 0.05, McNemar test). These results demonstrate
that the new rapid latex agglutination kit, SSP, was more specific for
the identification of S. aureus than the previous version
and performed comparably to the SRX and BBL kits.
| |
TEXT |
Staphylococcus aureus
remains a pathogen of considerable clinical concern. It is responsible
for a multitude of infectious processes as well as for infections of
diverse foreign bodies, including intravenous catheters and prostheses
(4). Rapid identification is essential because S. aureus can cause significant morbidity and mortality and remains a
leading cause of nosocomial infection (6, 15). A variety of
rapid agglutination kits to facilitate both prompt identification of
S. aureus isolates and differentiation from
non-coagulase-producing staphylococci have been developed and marketed.
The classic criterion for identification of S. aureus is
that the organism can clump in plasma via the activity of extracellular free coagulase, also termed staphylocoagulase (10). Free
coagulase is thought to interact with prothrombin in plasma to produce
staphylothrombin, which converts prothrombin into an active form that
releases fibrinopeptides from fibrinogen, forming fibrin clots
(3). The tube coagulase test using rabbit plasma is based on
this reaction and is a straightforward test that is still widely used
in the clinical setting as a "gold standard." Its primary
limitation is that the tube must be examined after 4 and 24 h of
incubation to reliably detect both positive and negative reactions.
False-negative results can occur due to rare coagulase-negative
S. aureus (17, 28), while false-positive results
can be produced by some non-S. aureus staphylococci which make proteases (called pseudocoagulases) that can also initiate clotting (29). In the slide coagulase test, rabbit plasma is used to agglutinate S. aureus organisms. Originally, this
agglutination reaction was thought to be mediated by a bound form of
staphylocoagulase. However, more recently the agglutination has been
shown to be due to a fibrinogen binding cell surface receptor encoded
by the clfA gene, termed the cell wall polypeptide clumping
factor (or clumping factor, fibrinogen receptor, or fibrinogen affinity
factor) (19). Although the slide coagulase test may be
performed in <1 min, it lacks adequate sensitivity and specificity
because some S. aureus strains lack clumping factor
(28) or mask it with capsular polysaccharides
(8), while other species, such as Staphylococcus
lugdunensis and Staphylococcus schleiferi subsp. schleiferi (11), produce clumping factor. To
circumvent these problems of inadequate sensitivity and specificity for
S. aureus detection, rapid agglutination kits that bring
together two or more properties of S. aureus to achieve
clinical usefulness have been developed.
The current kits include reagents that react simultaneously with
several different surface factors specific to S. aureus. These include human fibronectin, which binds to cell wall polypeptide clumping factor; the Fc portion of human immunoglobulin G (IgG), which
binds to protein A; and antibodies which bind to specific bacterial
surface antigens (1, 20). These reagents may be adsorbed
onto the surfaces of erythrocytes or latex particles.
In this study, a second-generation rapid agglutination test, Slidex
Staph Plus, was compared to its predecessor, the original Slidex Staph
kit, and two other tests, Staphaurex and BBL Staphyloslide. All four
tests detect bound coagulase, all tests except the BBL Staphyloslide
kit detect protein A, and the Slidex Staph and Staph Plus kits detect
S. aureus cell wall-specific antigens. Because methicillin-resistant S. aureus (MRSA) and
methicillin-sensitive S. aureus (MSSA) have demonstrated
different sensitivities with some rapid agglutination assays (7,
27), we included equal numbers of MRSA and MSSA organisms, as
well as non-S. aureus staphylococci representing different
species. The sensitivities and specificities of the four rapid
agglutination tests in addition to the standard tube coagulase test
were determined and compared by using a panel of primarily fresh
staphylococcal clinical isolates from the United States.
Bacterial strains.
A total of 538 staphylococcal individual
patient isolates were tested in the study protocol. Of 508 isolates
detailed in the study analysis, 380 (75%) were fresh isolates
collected by the clinical microbiology lab at the Boston Veterans
Affairs (VA) Medical Center and the remaining 128 isolates were taken
from five frozen collections from diverse sources that have been
characterized elsewhere (5, 9, 12, 16). Of the 304 S. aureus isolates tested, 229 (75%) were fresh clinical isolates
comprising 108 (47%) MRSA and 121 MSSA organisms. Ongoing molecular
strain typing of the isolates in our medical center indicates that the
MRSA organisms represent three broad genetic lineages plus additional diverse genotypes (18) and that the MSSA organisms are
highly diverse (16, 24). The 204 coagulase-negative
staphylococci included 151 fresh isolates of which 79 (52%) were
methicillin resistant.
S. aureus identification tests.
All tests were
done on the same day in parallel from a pure subculture of the primary
isolate. Fresh clinical isolates streaked on BBL Trypticase soy agar
(TSA II) plates with 5% sheep blood (Becton Dickinson Microbiology
Systems [BD], Cockeysville, Md.) or frozen glycerol stocks were
inoculated into 16- by 150-mm borosilicate glass tubes (VWR Scientific,
Boston, Mass.) containing 0.5 ml of Trypticase soy broth (BD). Cultures
were grown to a turbidity equal to a 0.5 McFarland standard
(bioMérieux) for ~4 h at 37°C and then streaked for isolation
on TSA II plates (BD) incubated overnight at 37°C. All subsequent
testing was done according to the manufacturers' instructions. Control
strains for agglutination reactions included two positive controls, an
MSSA strain (ATCC 25923) and an MRSA strain (V 8333), and one negative
control, Staphylococcus epidermidis (ATCC 14990).
(i) Free-coagulase (tube) test.
BBL rabbit coagulase plasma
(BD) reconstituted with sterile water (0.5 ml) was dispensed in 10- by
75-mm borosilicate glass tubes (Chasma Scientific, Cambridge, Mass.)
and stored at 
20°C. For each isolate several isolated colonies were
picked with a sterile loop or wooden applicator from the TSA II plate
incubated overnight and were inoculated into plasma-containing tubes.
Isolates were placed in a 37°C water bath and were observed for clot
formation at 4 and 24 h.
(ii) MRSA and MSSA classification.
All isolates were
inoculated onto a Mueller-Hinton agar plate supplemented with 4% NaCl
and 6 mg of oxacillin (BD) per ml as recommended by the National
Committee for Clinical Laboratory Standards (21). Plates
were incubated at 35°C for a full 24 h and examined for evidence
of growth. Controls included an oxacillin-susceptible strain (S. aureus ATCC 25923) and an oxacillin-resistant strain (S. aureus ATCC 43300).
(iii) Slidex Staph kit (bioMérieux Vitek, Hazelwood,
Mo.).
The Slidex Staph reagent is a combination agglutination test
based on latex and hemagglutination components that detect bound coagulase, protein A, and specific S. aureus cell surface
antigens. This reagent includes blood cells sensitized with fibrinogen
to detect bound coagulase and latex particles sensitized with specific monoclonal antibodies. These monoclonal antibodies detect protein A by
the Fc fragment of IgG as well as specific group antigens on the
bacterial cell surface.
(iv) Slidex Staph Plus kit (bioMérieux).
The Slidex
Staph Plus is a latex agglutination kit utilizing latex particles
sensitized with human fibrinogen and S. aureus-specific monoclonal antibodies. These monoclonal antibodies detect protein A by
the Fc fragment of IgG as well as different polysaccharide antigens on
the bacterial cell surface.
(v) BBL Staphyloslide kit (BD).
The Staphyloslide kit is a
hemagglutination test that detects the activity of the cell wall
polypeptide clumping factor produced by S. aureus strains.
This polypeptide binds to fibrinogen-sensitized sheep erythrocytes.
(vi) Staphaurex kit (Murex Diagnostics Limited, Kent,
England).
The Staphaurex kit is an agglutination test that detects
the presence of bound coagulase and protein A. The test reagent is composed of latex particles coated with purified human IgG and fibrinogen.
Species identification.
The species of each staphylococcal
isolate was determined with the API STAPH kit (bioMérieux).
Colonies were picked from TSA II plates and suspended in API STAPH
medium according to the manufacturer's instructions. Twenty microwells
(19 for biochemical tests and 1 negative control) were inoculated with
the suspension and placed at 37°C for 24 h. Results were read
and were transformed into a numerical profile from which a species was
identified according to the API STAPH identification codebook, based on
the Kloos and Schleifer classification system (10a).
Isolates with identification percentages of <80% were considered
unacceptably identified as per the manufacturer's instructions for
interpretation of the numerical profile and were further tested with
the ID32 STAPH kit (bioMérieux). Of the 304 S. aureus
isolates, 4 (1.3%) were not acceptably identified with the API STAPH
kit and were subsequently typed with the ID32 STAPH kit. Three
coagulase-negative isolates typed as S. aureus with the ID32
STAPH kit and a fourth, a coagulase-negative isolate, could not be
acceptably identified. These isolates were later verified by DNA
hybridization to be S. aureus. Of the 204 non-S.
aureus staphylococcal isolates, 35 (17.2%) were not acceptably identified with the API STAPH kit and were subsequently typed with the
ID32 STAPH kit. One-third of these isolates, 11 of 35, remained
unacceptably identified. Colonies were picked and suspended to a
turbidity equal to a 0.5 McFarland standard (bioMérieux) according to the manufacturer's instructions. The suspension was inoculated into 26 cupules and incubated at 37°C for 24 h. The reactions were recorded and transformed into a numerical profile that
was matched to a species according to the ID32 STAPH identification codebook; isolates with identification percentages of <80% were considered unacceptably identified as per the manufacturer's
instructions.
Accuprobe DNA probe hybridization.
Five coagulase-negative
isolates from the completed study, four of which were identified by the
API STAPH or ID32 STAPH (bioMérieux) kit as S. aureus,
were further analyzed to determine species identification by a DNA
hybridization method. The Accuprobe S. aureus-specific culture identification test (GenProbe, Inc., San Diego, Calif.) detects
a unique rRNA sequence specific to S. aureus by DNA:RNA hybridization of the chemiluminescently labeled single-stranded DNA
probe. A single colony was picked from a TSA II plate incubated overnight and was resuspended in 50 µl of lysis reagent. Samples were
processed according to the manufacturer's instructions and the results
were read on a PAL luminometer (GenProbe, Inc.). A sample with <600
photometric light units was considered negative, and a sample with
>1,500 photometric light units was considered positive. Controls
included a positive organism (S. aureus ATCC 25923) and a
negative organism (S. epidermidis ATCC 14990).
Isolates were processed in sets of 15 to 20 such that a tube coagulase
test, four rapid agglutination tests (Slidex Staph Plus, Slidex Staph,
Staphaurex, and Staphyloslide), and a species identification test (API
STAPH or ID32 STAPH) were all performed in parallel with the same
subcultures. Isolates for which the coagulase and rapid agglutination
test results were concordant, i.e., positive (S. aureus) or
negative (non-S. aureus), were included in the final
analysis. Isolates for which the results of one or more tests were
discordant were tested again and were included in the final analysis
only if the same discordant results could be reproduced. Of the
original 538 isolates, 30 (5.6%) were not included in the final
analysis because the discordant test result was not reproducible. Since
each isolate was evaluated with five tests, this represents a technical
laboratory error rate of 1.1%. The overall rate of repeated
inconsistent results was 5.9% (32 of 538), which corresponds with the
false-negative and false-positive test results reported for the
sensitivity and specificity determinations for the 508 isolates
included in this study.
The four rapid agglutination test kits had comparable sensitivities
(97.4 to 100%) for either MRSA (n = 154) or MSSA
(n = 150) isolates (data not shown). The combined
sensitivity of the four tests ranged from 98.7 to 99.0%, and the tube
coagulase test had a sensitivity of 98.7%. The Slidex Staph Plus test
demonstrated greater specificity than the Slidex Staph test against the
204 coagulase-negative staphylococcal isolates tested (Table
1). The majority (72%) of the
coagulase-negative staphylococcal isolates were S. epidermidis (n = 147), with the remaining isolates
including Staphylococcus haemolyticus (n = 13), Staphylococcus hominis (n = 10),
Staphylococcus warneri (n = 7),
Staphylococcus capitis (n = 6),
Staphylococcus simulans (n = 4), S. lugdunensis (n = 4), Staphylococcus
equorum (n = 1), and other non-S.
aureus species (n = 12). Three of the tests had
comparable specificities for 204 coagulase-negative staphylococcal
isolates, i.e., 97.1% (Staphaurex), 97.5% (Staphyloslide), and 98.0%
(Slidex Staph Plus) (Table 1); a significant improvement was achieved
in the specificity of the Slidex Staph Plus test over the Slidex Staph
test (93.1%) (P < 0.05, McNemar test) (Table 1). The
tube coagulase test demonstrated a specificity of 100%.
The false-positive test results for the four kits are listed in Table
2 and were distributed among 18 coagulase-negative isolates, with only 1 isolate positive by all four
tests and 2 isolates positive by three of the four agglutination tests.
These 18 isolates were identified as S. epidermidis
(n = 12), S. haemolyticus (n = 1), S. lugdunensis (n = 2), and
unidentified coagulase-negative staphylococci (n = 3).
Of these 18 isolates, 50% (9 of 18) were methicillin resistant. One
isolate was positive by all four agglutination tests, was negative by
the tube coagulase test at 4 and 24 h, and was unsatisfactorily
identified by either the API STAPH or the ID32 STAPH kit. This isolate
was later identified as S. aureus by using the S. aureus-specific AccuProbe DNA probe hybridization kit.
Of the 380 fresh clinical isolates from the Boston VA Medical Center, a
total of 5 (1.3%) were eventually determined to be coagulase-negative
S. aureus. All five isolates positively agglutinated in each
of the four rapid agglutination kits, were reproducibly determined to
be coagulase negative at 4 and 24 h by the tube coagulase method,
and were methicillin sensitive. Of the five isolates, four were
identified as S. aureus by the API STAPH and ID32 STAPH
kits, with the fifth not satisfactorily identified by either kit. This
isolate was confirmed to be S. aureus only by DNA probing.
Staphylococcal species are becoming increasingly important in the
clinical microbiology laboratory and in the hospital setting due to the
continued increase in methicillin resistance and the emergence and
recognition of serious infections with coagulase-negative staphylococci
in hospitalized patients exposed to invasive procedures, central lines,
and intensive care units (2). The rapid differentiation of
staphylococcal isolates has been complicated by an inability to detect
MRSA deficient in clumping factor (14) and protein A
(22, 25) that has also been reported with some rapid
agglutination tests (13, 14, 26, 30). However, we found in
this study that there was no significant difference in the
sensitivities of the four test kits (Slidex Staph Plus, Slidex Staph,
Staphaurex, and Staphyloslide) examined for MRSA and MSSA. Modification
of second-generation agglutination tests to increase sensitivity by
addition of antibodies directed against S. aureus surface
antigens has resulted in the detection of organisms that might
otherwise go undetected, leading to false-negative results. Several
S. aureus-specific surface antigens have been targeted,
including serotype 5 and 8 capsular polysaccharides (8) and
a surface glycopolysaccharide called antigen 18 (7). It is
important to note that geographical differences can correlate with
antigenic variation and may affect an individual test's specificity
(7).
In accordance with another report (31), we confirmed that
the Slidex Staph kit was equally specific as but less sensitive than
several other commercially produced agglutination tests. In this study
we have compared the first-generation Slidex Staph kit with the
modified Slidex Staph Plus kit to demonstrate that the specificity of
the new test has been significantly increased and is now comparable to
those of several other rapid agglutination tests on the market.
Recently, the performance of the Slidex Staph Plus kit was also tested
in a French study by Personne et al. (23) in which it
exhibited an increase in both sensitivity and specificity compared to
the Slidex Staph kit. It is important to note that in our study, in
which we examined U.S. isolates, we did not find a sensitivity of 100%
for the Slidex Staph Plus kit, as was found in the French study
(23). Additionally, we found no difference in the
sensitivity of detecting MRSA (n = 154) with any of the
four kits tested in our study, in contrast to the range of
sensitivities (93.0 to 100%) found for MRSA in the French study
(23) using the Slidex Staph and Slidex Staph Plus kits.
It is also of interest that the use of the tube coagulase test as the
sole clinical laboratory test for identification of S. aureus would not have correctly identified the five confirmed clinical isolates of coagulase-negative S. aureus found in
this study. These isolates did not express sufficient free coagulase activity to be detected by the tube coagulase method. Further molecular
characterization of the nature of the free-coagulase deficiency of
these isolates was not performed for this study. Since all five of
these S. aureus isolates were positively identified with
each of the four rapid agglutination tests, verification of suspected
staphylococci negative by the tube coagulase test with a rapid
agglutination test may prove useful.
| |
ACKNOWLEDGMENTS |
We are grateful to the members of the Boston VA Medical Center
Pathology and Laboratory Medicine Service (Dianne Fitzsimmons, Elisa
Tosi, Carol Feeney, Paula Aronson, Marcie Burt, and Peggy Sylvia) for
saving the clinical isolates used in the study. In addition, we thank
Marc Leportier for his advice and Barbara Hammond for her efficient
assistance.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Research Service
(151), VA Medical Center, 150 S. Huntington Ave., Boston, MA 02130. Phone: (617) 278-4416. Fax: (617) 739-6394. E-mail:
rarbeit{at}bu.edu.
| |
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Journal of Clinical Microbiology, April 1998, p. 1109-1112, Vol. 36, No. 4
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