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Journal of Clinical Microbiology, June 2000, p. 2037-2042, Vol. 38, No. 6
0095-1137/00/$04.00+0
Comparison of Three Commercial Rapid Identification Systems
for the Unusual Gram-Positive Cocci Dolosigranulum
pigrum, Ignavigranum ruoffiae, and
Facklamia Species
Leslye L.
LaClaire and
Richard R.
Facklam*
Division of Bacterial and Mycotic Diseases,
Respiratory Disease Branch, National Center for Infectious Diseases,
Centers for Disease Control and Prevention, Atlanta, Georgia 30333
Received 22 December 1999/Returned for modification 11 February
2000/Accepted 8 March 2000
 |
ABSTRACT |
We evaluated three rapid identification systems
The Biomerieux
rapid ID 32 STREP (ID32), the BBL Crystal rapid gram-positive identification (Crystal), and the Remel IDS RapID STR (IDS)
systemsfor their ability to identify 7 strains of Alloiococcus
otitidis, 27 strains of Dolosigranulum pigrum, 3 strains of Ignavigranum ruoffiae, and 18 strains of 4 different Facklamia species. Since none of these six
species of gram-positive cocci are included in the identification
databases for these systems, the correct identification for the strains
tested should be "unacceptable ID" for the ID32 and Crystal systems
or "no choice" for the IDS system. The ID32 system identified all
27 strains of D. pigrum, 6 of 18 Facklamia
species, and 2 of 3 cultures of I. ruoffiae as
"unacceptable ID." The Crystal system identified 10 of 27 D. pigrum, 2 of 18 Facklamia species, and 2 of 3 I. ruoffiae strains as "unacceptable ID." The IDS
system identified only 1 culture of D. pigrum as "no
choice," but it also identified 2 cultures of D. pigrum
as a "questionable microcode" and 19 cultures of D. pigrum as an "inadequate ID, E. faecalis 90%,
S. intermedius 9%." A total of 2 of the 18 cultures of
Facklamia and all 3 of the I. ruoffiae
cultures were correctly identified as "no choice." The most common
misidentifications of Facklamia species by the ID32 and IDS
systems were as various Streptococcus species and as
Gemella species. In the Crystal system, the most common
erroneous identification was Micrococcus luteus. These data
indicate the need for the commercial manufacturers of these products to
update their databases to include newly described species of
gram-positive cocci.
| |
INTRODUCTION |
Since the description of the first
Facklamia species in 1997, four additional species of this
genus have been described (5-8, 17). The species
Facklamia hominis, F. ignava, F. sourekii, and F. tabacinasalis are most often arranged
in chains, whereas F. languida is most often arranged
in clusters with very little chaining. Dolosigranulum pigrum
was described in 1993 (2). This bacterium is arranged in
pairs, tetrads, and clusters. Ignavigranum ruoffiae,
recently described (9), is arranged primarily in chains. Information on the identification of these newly described bacteria is minimal, and in most cases the authors initially describing these species have used a combination of molecular characterization, conventional tests, and miniaturized rapid tests such as the API 50CH
(Biomerieux, Inc., Hazelwood, Mo.). The identification of these
bacteria is problematic since none of the rapid testing systems have
them in their databases. We also included seven strains of
Alloiococcus otitidis for comparison purposes since the
phenotypic characteristics of this organism resemble those of
Dolosigranulum, Facklamia, and
Ignavigranum strains at the genus level.
In a previous study examining 120 strains of unidentified gram-positive
cocci with phenotypic characteristics that eliminated them from the
known genera of gram-positive bacterial genera, e.g.,
Aerococcus, Enterococcus, Gemella,
Lactococcus, and Streptococcus, we identified 18 strains as Facklamia species, 27 strains of D. pigrum, and 3 strains of I. ruoffiae by using
conventional test methods (11). Rapid identification test
systems for gram-positive cocci have been used for nearly 20 years. We
evaluated three systems for their capability to correctly identify the
A. otitidis, D. pigrum, I. ruoffiae, and Facklamia species: the rapid ID 32 STREP (ID32; Biomerieux, Inc., Hazelwood, Mo.) (15), the BBL
Crystal Rapid Gram-Positive ID Kit (Crystal; BD Bioscience,
Cockeysville, Md.) (20), and the RapID STR (Remel, Inc.,
Lenexa, Kans.) (3, 16, 19). The ID32 system is a
modification of the API 20S system (16, 19). The Remel RapID
STR system is the same test kit previously distributed by Innovative
Diagnostics, Inc., as the IDS RapID STR system and is referred to here
simply as IDS.
| |
MATERIALS AND METHODS |
The 55 strains tested were taken from the culture collection of
the Streptococcus Laboratory at the Centers for Disease
Control and Prevention. All strains were identified to the genus level by previously described conventional tests (11) (see Tables 1 and 2). Seventeen of the strains were additionally identified by 16S
rRNA sequencing. The sources of these gram-positive cocci were similar
to those of the viridans streptococci; 24 cultures were isolated from
blood cultures, 6 were isolated from cultures of the eye, 4 were
isolated from nasopharyngeal swabs, 2 cultures each were from
cerebrospinal fluid and abscesses, and one each was from cultures of
bone, ear, gall bladder, gastric contents, sinus, sputum, urine,
vagina, wound, and unknown. All seven cultures of A. otitidis were isolated from inner ear cultures. Antimicrobial susceptibilities, sources, clinical diagnosis, and other demographic information on these organisms will be reported elsewhere (L. L. LaClaire and R. R. Facklam, submitted for publication).
The ID32 kit and reagents, the Crystal kit, and the IDS system were all
used according to the manufacturer's instructions provided. Most
strains were tested at least two different times. Some strains were
tested four times.
| |
RESULTS AND DISCUSSION |
Conventional tests.
Strains were first identified as potential
Dolosigranulum, Facklamia, and
Ignavigranum spp. by determining unique phenotypic characteristics in conventional tests used to identify the different genera of catalase-negative, gram-positive cocci. These three genera
are characterized as susceptible to vancomycin, with negative gas
production, positive L-pyrrolidonyl-
-naphthylamide (PYR) reactions, positive leucine aminopeptidase (LAP) reaction, growth in 6.5% NaCl broth, negative bile esculin reaction, and negative growth at 10°C and 45°C, are nonmotile, and are either
alpha-hemolytic or gamma-hemolytic on 5% sheep blood agar (Table
1). Since the arrangement of cells into
chains or clusters is not reliable and depends on the medium from which
the cells were taken for the Gram strain, identification to the genus
level must rely on the combination of tests listed in Table 1. The
combination of reactions listed above is not unique to the genus level;
Alloiococcus otitidis, D. pigrum,
Facklamia spp., and I. ruoffiae all have the
same phenotypic characteristics. A. otitidis does not grow
anaerobically, which differentiates it from the other three genera
(1, 13, 18). The cultures we described as
"Alloiococcus-like" in a previous study (18)
have since been identified as D. pigrum.
Facklamia species are differentiated from each other and
from
D. pigrum and
I. ruoffiae by the
deamination of arginine (Arg),
by hydrolysis of hippurate (Hip) and
esculin (Esc), and by acid
formation in sucrose (Suc) and sorbitol
broth (Sbl) (Table
2).
D. pigrum is positive only for Esc; all other species, including
I. ruoffiae, are negative for Esc.
I. ruoffiae and
F. languida are both negative in all
five tests; however,
I. ruoffiae has
a distinctive
sauerkraut odor on blood agar, which helps to identify
the species.
F. hominis is positive for Arg and Hip and variable
in
Suc.
F. ignava is positive only for Hip.
F. sourekii is positive
for Hip, Suc, and Sbl. The newest species,
F. tabacinasalis, not
yet documented from humans, is
positive for Suc and Sbl only.
This combination of tests identifies all
of these strains to the
species level.
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TABLE 2.
Phenotypic characteristics of D. pigrum,
I. ruoffiae, and Facklamia species as shown
by conventional biochemical tests
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|
ID32.
Since A. otitidis gave the same genus
identification as the Dolosigranulum, Facklamia,
and Ignavigranum cultures, we included seven strains in this
study for comparison purposes (Table 1). None of the A. otitidis strains were correctly identified by the ID32, Crystal,
or IDS systems. A. otitidis strains presented difficulty in
preparing satisfactory inocula for the test systems because of poor
growth and adherence properties. These strains must be grown on heart
infusion rabbit blood agar for at least 48 to 72 h.
The ID32 system correctly identified 7 (39%) of the 18
Facklamia species as "unacceptable ID." Those that were
correctly identified
were 3 of 4 strains of
F. hominis,
3 of 5 strains of
F. ignava,
none of 6 strains of
F. languida, and 1 of 3 strains of
F. sourekii (Table
3). The
F. languida strains were most often misidentified
as
Gemella morbillorum, as was one strain of
F. ignava. This misidentification
is somewhat understandable since
there is little difference between
the
Gemella spp. and
Facklamia spp.; however, the correct division
of the two
genera can be made with growth in 6.5% sodium chloride.
Only the
Facklamia species grow in broth containing 6.5% sodium
chloride. Another common misidentification was
Facklamia
species
being identified as
S. acidiminimus; this occurred
with three
different strains of
Facklamia. This, too, may be
understandable
since the Centers for Disease Control and Prevention
(CDC)
Streptococcus Laboratory has distributed several
strains previously identified
as
S. acidiminimus, which were
reidentified as
Facklamia species.
In fact, we included
these strains in previous studies of rapid
identification kits
(
10,
12,
22). This points out a need
to update the
identification of strains obtained from the CDC
Streptococcus Laboratory and to update the commercial
databases
as well.
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TABLE 3.
Identification of A. otitidis, D. pigrum, Facklamia species, and I. ruoffiae by three commercial rapid identification systems
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|
Although 46 profiles were generated from testing 27 strains of
D. pigrum in the ID32 test system, all 46 profiles resulted
in an
"unacceptable ID" (Table
3). These results were very encouraging
since the product's manufacturer would only have to include profiles
we have generated for
D. pigrum in its database to
accurately
identify this
species.
Two of the three strains of
I. ruoffiae were correctly
identified by the ID32 system. The third strain tested had a doubtful
profile. Not enough numbers of this species have been tested to
conclude that the system can be adjusted to identify the species
accurately; however, these results are
encouraging.
Crystal.
As stated above, A. otitidis was included
in this study because of the similar genus identification. Six of the
seven strains tested in the Crystal system were identified as
Micrococcus species. The seventh was identified as
Streptococcus pneumoniae (Table 3). The identification of
A. otitidis may have been compromised because of the
difficulties in preparing the inoculum as previously stated; however,
its identification may point out a more serious problem for this
system. Micrococcus species are catalase positive, whereas
most of the cultures we included in this study were catalase negative.
Some of the A. otitidis cultures are catalase positive, but
we have found that this is not true in every case. Most of the A. otitidis cultures we have examined have been very weak-to-negative catalase producers.
Like the ID32 system, the Crystal system identified seven (39%)
strains of
Facklamia species as "unacceptable ID" (Table
3).
One of four strains of
F. hominis, three of five
strains of
F. ignava, none of six strains of
F. languida, and three of three
strains of
F. sourekii were correctly identified. Of the 18 strains
of
Facklamia tested, 13 were identified as various
Micrococcus species. These misidentifications indicate the
need to include
catalase reactions in the identification schemes for
gram-positive
cocci.
Among the 27 strains of
D. pigrum, 17 "unacceptable ID"
profiles were observed with 14 different strains (Table
3). This
indicates that half of the cultures could be accurately identified
by
incorporating these newly generated profile numbers into the
Crystal
database. As with the
Facklamia species (indicating a
problem that arises by not including the catalase test into the
identification process), eight strains of
D. pigrum
generated
eight profile numbers that were identified as various
Micrococcus species. Eleven different profile numbers
identifying strains
as various streptococcal species were observed with
11 different
strains of
D. pigrum. The majority of these
profiles had low percentages
of confidence for identification (Table
3).
We observed three profiles with the three strains of
I. ruoffiae: one was an "unacceptable ID" and two were low-level
confidence
M. luteus. These misidentifications again
indicate the need to
include catalase in the identification
scheme.
IDS.
None of the A. otitidis strains were correctly
identified in the IDS system. Four strains were identified as a
probable overlap between G. morbillorum and Aerococcus
viridans, two strains were identified as implicit identification
for G. morbillorum, one was identified as an implicit
identification of S. mitis, and one was identified as a
probable S. mitis. Only 3 of 18 (17%) Facklamia
strains were identified as "no choice" (Table 3). The identification of F. hominis, F. ignava, and F. sourekii as S. acidiminimus with high levels of confidence with the IDS kit was not surprising. As explained above for the ID32 kit, strains originally identified as S. acidiminimus have been reidentified as
F. hominis. It is probable that some of the strains
that the CDC Streptococcus Laboratory had identified and
distributed as S. acidiminimus were used to generate
databases for the IDS system (22). Also, the identifications
of the various Facklamia species as G. morbillorum and as various Streptococcus species may be
interpreted as poorly growing Streptococcus species or
misidentified strains as Gemella that have been used to
generate databases. Gemella species do not grow in 6.5%
NaCl broth, so strains with profiles identical to the ones described
here should be retested for growth in 6.5% sodium chloride. We
observed only one "no choice" profile in 27 strains of D. pigrum tested. The majority of D. pigrum strains tested
(19 of 27 [70%]), generated one profile number: "inadequate ID,
Enterococcus faecalis, 90%." This is an erroneous
identification, even though the confidence level is quite low (Table
3). Other misidentifications of Streptococcus, including
group A streptococci and Enterococcus species, are inexplicable.
A discouraging point for all three test kits is the incidence of
generated profile numbers shared among different species
and genera.
The ID32 had one instance in which a single strain
of
F. hominis and
F. ignava had the same profile. This
phenomenon
occurred twice with the Crystal system among two different
strains
of
F. ignava and among three different strains
of
F. hominis.
The Crystal system also generated shared
profiles between different
genera:
F. ignava and
F. sourekii with
Alloiococcus sp. The IDS
system had three instances in which
F. sourekii and
F. ignava shared profiles, as well as two instances in
which three different
strains of
F. hominis and
F. ignava had the same
profiles.
Previous investigators have used a combination of conventional tests
and reactions from one or more of the rapid identification
systems to
describe and differentiate the newly identified genera
and species
(
2,
4-9,
17). We explored the possibility that
each one of
the three systems we evaluated could be used to identify
the species of
Alloiococcus,
Dolosigranulum,
Facklamia, and
Ignavagranulum.
When we used
conventional tests first to identify these four genera
with common
phenotypic traits, we then tested these rapid kits
to determine whether
they could identify all the species of these
genera. Although we have
included
Alloiococcus strains in these
investigations, it is
unlikely that microbiologists would confuse
this bacterium with the
other genera in Tables
4,
5, and
6.
A. otitidis is a strict aerobe and, to our knowledge, has
been
isolated only from inner ear cultures from patients with otitis.
The results of using the ID32 for differentiation of
D. pigrum and
I. ruoffiae from the
Facklamia species are presented in Table
4. Although not
perfect, combinations of reactions can identify
most of the species.
D. pigrum can be identified by positive reactions
in
arginine and
-galactosidase (
-Gar), by acidification of trehalose
and maltose, and by negative reaction in alanine-phenylalanine-proline
aryalamidase (APPA).
F. hominis can be identified by
positive
reactions in
-Gar, APPA,
-galactosidase (
-Gal), and
glycyl-tryptophane
arylamidase (GTA) and by negative reactions in
trehalose.
F. ignava is problematic because there are
too many variable reactions to
the majority of tests in the ID32
system.
F. languida is easily
identified because it is
positive in only 2 of the 14 tests: acid
formation in trehalose and
GTA.
F. sourekii is identified by acidification
of
mannitol, sorbitol, trehalose, maltose,
D-arabitol, and
saccharose
and by hydrolysis of Hip. Only a single nonhuman isolate of
F. tabacinasalis is represented in Table
4, so these
results should
be cautiously interpreted.
I. ruoffiae
is identified by positive
reactions in Arg, acidification of mannitol,
trehalose, and saccharose,
and hydrolysis of hippurate and by negative
reactions in
-Gar,
acidification of sorbitol, APPA,
-Gal, and
GTA.
The same process can be used for the Crystal system (Table
5). The
reactions of
A. otitidis overlap somewhat with the reactions
of some of the
D. pigrum and
Facklamia species.
D. pigrum is FPY
(
L-pyroglutamic acid-AMC), FTR
(
L-trytophan-7-amino-4-methylcoumarin
[AMC]) and BGL
(
p-n-p-
-
D-glucoside) positive.
F. hominis is FPR
(
L-proline-AMC), FTR, and PPG
(
p-n-p-
-galactoside and
p-n-
-
D-galactoside)
positive.
F. ignava is problematic because of the number of variable
reactions.
F. languida is identified by a positive reaction in
FPY
and negative reactions in FPR, MTT (acid formation in maltotriose),
BGL, and PPG.
F. sourekii is identified by positive
reactions
in FPY and BGL and negative reactions in MTT and PPG. Again,
only
a single strain of
F. tabacinasalis (nonhuman) was
tested, so
these reaction percentages should be interpreted cautiously.
I. ruoffiae is identified by positive reactions in FPY
and FTR and
by negative reactions in BGL and
PPG.
Attempting to apply the same interpretation to the IDS system is more
difficult because of the limited number of tests with
positive
reactions (Table
6). Cultures of
F. hominis and
I. ruoffiae appear to have unique profiles, but the
cultures of
D. pigrum and the remainder of the
Facklamia species have a common
profile.
We have previously compared various reactions included in rapid
identification tests with conventional tests and have indeed
found
differences (
14). Comparing the individual tests in these
systems to the conventional tests resulted in several interesting
observations. In the conventional disk test we use for the PYR
test
(
L-pyrrolidonyl-
-naphthylamide) all of the
D. pigrum,
Facklamia species, and
I. ruoffiae cultures were positive. However, in the
ID32 test, two
strains of
D. pigrum, one strain of
F. hominis,
four strains of
F. ignava, two strains of
F. languida, and one
strain
I. ruoffiae
were negative. These numbers were similar to
those for the Crystal and
IDS PYR tests. In the conventional test
for deamination of Arg, only
the
F. hominis and
I. ruoffiae strains
were positive. But in the ID32, Crystal, and IDS systems, 88,
79, and
79% of the
D. pigrum cultures, respectively, were positive.
Of the
F. ignava cultures, three of five, four of five,
and three
of five strains were positive for Arg in the ID32,
Crystal, and
IDS systems, respectively; none of these cultures
were positive
in the conventional Moeller's decarboxylase tests. These
results
were similar to those of West et al. (
21), who also
reported
major differences in Arg hydrolysis by viridans streptococci,
depending on the rapid test
used.
It is apparent that the manufacturers of these rapid identification
kits need to update their databases by including the identification
of
newly described genera and species of gram-positive cocci,
including
the
Dolosigranulum,
Facklamia and
Ignavigranum species.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Centers for
Disease Control and Prevention, National Center for Infectious
Diseases, Division of Bacterial and Mycotic Diseases, Respiratory
Diseases Branch, Mailstop C-02, Atlanta, GA 30333. Phone: (404)
639-1379. Fax: (404) 639-3123. E-mail: rrf2{at}cdc.gov.
| |
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Journal of Clinical Microbiology, June 2000, p. 2037-2042, Vol. 38, No. 6
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Abstract
Introduction
