0095-1137/84/110894-05$02.00/0
Copyright© 1984,American SocietyforMicrobiology
Evaluation of the Rapid Strep
System
for the Identification of
Clinical Isolates of
Streptococcus
Species
RICHARD R. FACKLAM,l* D. L. RHODEN,- AND P. B. SMITH
Division of BacterialDiseases1 and Hospital Infections Pr-ogram,2 Centerfro Inlfectiou.s Disetases, Ceniter-s
for
Disease Control, Atlacnta, Georgia 30333Received 25June1984/Accepted 10 August 1984
A total of 247 strains of streptococci isolated from humansweretestedforidentification in the Rapid Strep system.Theidentificationratesandidentification levelsweredifferent for each Streptococcus species. Our data
indicate that the Rapid Strep system will identify nearly all the beta-hemolytic Streptococcus species if serological procedures are used in conjunction with the rapid physiological procedures. Of the group D
streptococci, 98% of the enterococci and 95% of the non-enterococci were correctly identified. Of the
commonly occurring viridans species, 85% were correctly identified, but only 10% of the less frequently
occurring viridans species were identified. A total of 90% ofthe Streptococcuspneumoniae and 60% of the
Aerococcus strainswerecorrectly identified.
The procedures used for the conventional identification and differentiation of streptococci are complex and
time-consuming.Serological methodsaregenerally usedto identi-fy thedifferentbeta-hemolytic streptococci. Although these procedures do not differentiate the beta-hemolytic strains intotruetaxonomicspecies, they doenable clinical microbi-ologists to convey useful information to physicians for managing patients. The development of slide agglutination tests for the rapid identification of beta-hemolytic
strepto-cocci hasshortened thetime required foridentification from 3 days (conventional extraction and capillary precipitin testing) to 1 day (slide agglutination testing from primary plates). Direct antigen testing of throat swabsmay shorten
the time required for group A Streptococcus identification even further (5, 11). Thus, it is not likely that any rapid
system based on physiological characteristics will compare
withserological techniques intermsof rapidity. However,as more than one species may possess a singlegroup antigen
(Streptococcus equi,S.equisimilis, and S.zooepidemicusall have thegroup C antigen), any system that can accurately
differentiatethespecieswithinaserological groupwill beof
value.
A variety of physiological tests are used to differentiate thenon-beta-hemolytic streptococci. Someof thesetestsare
highly specialized and are used only to identify certain Streptococcus species (2, 3).Theseconventional physiologi-cal tests require from 3 to 7 days of incubation, so final identification is delayed to the point that it has very little impactonpatient management. Thus,any rapid systemthat would yield accurate results and be more convenient and
time saving would be ofsignificant valueto microbiologists andphysicians.
We have used the terminology described in a recent
editorial to designate the Streptococcus milleri group of streptococci (4). S. anginosus will be used to identify the beta-hemolytic minute-colony forms of group A and C streptococci as well as the group F and beta-hemolytic Streptococcus strains withoutgroup antigens. S.
constella-tus will be used to identify strains formerly termed S. anginosus-constellatus, and S. intermedius will be used to
identify strains formally termed S. MG-intermedius. This
*Corresponding author.
terminology conforms tothelist of accepted species names
approved by the International Congress for Microbiology (10). Inthispaper wedescribeourevaluation ofa
commer-cial product, the Rapid Strep system (DMS Laboratories, Inc., Flemington, N.J.), designed to identify all species of streptococci within 24 h.
(This study was presented in part at the 84th Annual Meeting of the American Society for Microbiology [R. R. Facklam, D. L. Rhoden, A. 0. Esaias, and P. B. Smith,
Abstr. Annu. Meet. Am. Soc. Microbiol. 1984, C127, p.
257].)
MATERIALS AND METHODS
Streptococcus strains. All strains tested were clinical iso-latesfromhumansandwereselectedfrom theStreptococcus ReferenceLaboratory culture collections atthe Centers for DiseaseControl, Atlanta,Ga. All strainsweregram-positive
cocci arranged in chains or clusters. All streptococci were
catalasenegative when tested for effervescence ofhydrogen peroxide. AllAerococclus strainswerecytochrome negative
when tested for cytochromes bythebenzidenetest. Strains
werereidentified by the serologicalandphysiological
proce-duresdescribed in the ManualofClinicalMicrobiology (3). Rapid Strepevaluation.Rapid Strepstrips and all required reagents were provided by DMS Laboratories, Inc. The
majorityof the strainswereinoculatedontoColumbiasheep bloodagarplates and incubatedanaerobically at 35°C for18 to20 h. Ofthe 247 strains, 75 wereinoculated onto
Trypti-case soy (BBL Microbiology Systems, Cockeysville, Md.)
sheepbloodagarplatesand incubated inacandle extinction
jar at 35°C for 18 to 20 h. The manufacturer's instructions call for the use of Columbia sheep blood agar and an
anaerobic incubation atmosphere, but other investigators have successfully used other media and incubation
atmos-pheres for the preparation ofan inoculum (9). The individ-ualsperforming the Rapid Streptesthadnoknowledgeof the identity of the strains other than the hemolytic reaction. Strips were inoculated and read in accordance with the
manufacturer's instructions.
The Rapid Strep systemconsists ofa strip containing20
dehydratedsubstancesfordetermining physiological
charac-teristics. Thecupules containingthedehydrated substances
were inoculated with a bacterial suspension (equal to or 894
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TABLE 1. Levels of identification ofbeta-hemolytic streptococci bytheRapid Strepsystem
No.ofstrainsidentifiedatindicated levelwithin 4 h(by24 h)
Group Species (no. of strains) L
Excellent Good Acceptable Licimntow ro
discriminationEro
A S.pyogenes (12) 1 6 0 5 0
B S.agalactiae (10) 9(1) 0 0 0 0
C S.equisimilis" (10) 0 1 1 5(3) 0
G Undesignated (10) 0 6 2 2 0
C S.zooepidemicus (10) 6(4) 0 0 0 0
A S.anginosusb (4) 4 0 0 0 0
C S.anginosusb (4) 2(1) 0(1) 0 0 0
F S.anginosusb (8) 7 1 0 0 0
None S.anginosus"(7) 7 0 0 0 0
aIdentifiedbythe Rapid Strepsystem asgroup CS.equisimilis orgroupGstreptococci.
bIdentified by the Rapid Strep systemasS.milleri(see text).
greater thanaMcFarland no. 4turbiditystandard)prepared
fromtheagarplates described above. Reactionswerereadat
4 h and after overnight incubation (1). Seven-digit profile numbers were obtained by adding the numerical values for
thetestresults in the strip (see manufacturer's identification codebook for details.) Theidentification and level of identi-fication for each strainwereobtained by matching the profile
numberto theprofile identification number provided in the manufacturer's code book.
The identification of a strain is based on the similarity
between its profile and thetaxathat constitute the
computer-stored data base. The level of identification is based on a
combination of the different reaction frequencies for each taxon with each test. The computer-generated number is convertedtoapercentage, which is knownasthepercentage
identification orlevel ofidentification. Profile numbers that
werenotlisted in the code bookweresentwith conventional identificationtothemanufacturer for analysis. The manufac-turerthen provided the final identification.
The levels ofidentification that we used(see Tables1, 2, and3) corresponded roughly to the manufacturer's
sugges-tions. We combined the excellent andvery good categories
intoonecategory,excellent. Thepercentageidentificationof
ourexcellentwas equal toorgreaterthan 99.0%. The good and acceptable categories were those suggested by the
manufacturer and correspondedto90.0to98.9% and 80.0to
89.9% identification, respectively. We combined two other levels ofidentification, low discrimination andspecies iden-tification, into onecategory, lowdiscrimination. Both
cate-gories, as suggestedby the manufacturer, hadidentification
levels below 80.0% and required additional testing to
con-firm the identity of the test strain. The tests used to
discriminate between the two or three possible
identifica-tionsarelisted in the code book. Ourlast level of
identifica-tion,
error, included strains that were identified at theacceptable level or above but whoseidentity didnot
corre-spondtotheconventional identification. Theerrorlevel also included strains thatgenerated profilenumbersnotincluded in the code book and for which themanufacturerwasunable to produce an identification because ofan inadequate data base.
RESULTS
The results oftesting75 strains ofbeta-hemolytic strepto-cocci areshown in Table 1. Serologicaltestingwas
suggest-ed forconfirmatoryidentification of all strains ofgroupA,B,
C
(S. equisimilis),
and Gstreptococci, r'egardlessofthe levelofidentification. Discrimination betweengroup C S.
equisi-milis and group G streptococci is not possible by the
physiologicaltestsin theRapid Strepsystem.All 10groupC
S.
zooepidemicus
strains were identified at the excellentlevel. Serological confirmation was not suggested for these strains. The last fourlines of Table 1 include fourserological
entities of one Streptococcus species, S. anginosus. The
Rapid
Strepsystemidentified these strainsasS.milleri. Thedifferences in nomenclature between the Centers for Disease Control and the Rapid Strep systemwill be discussed later. All thegroupA, C,and Fstrains and nongroupable strains of
S.anginosuswereidentifiedatthe excellent andgoodlevels
asS. milleri type1,with theexception ofonestrain ofgroup C S. anginosus. It was identified as S. milleri type 2.
Serologicalconfirmationwasnotsuggested for these strains. Noidentificationerrors wereobservedfor the
beta-hemolyt-ic strains (Table 1), and 63 of the 75 strains (84%) were
identified within 4 h; the remainder of the strains were
identified afterovernight incubation. The profile numbers of twostrains, bothgroupCS. equisimilis,werenotincludedin the code book. The manufacturer's analysis of these two
TABLE 2. Levels ofidentification ofnon-beta-hemolytic strainsof groupB and Dstreptococciandaerococciby theRapidStrepsystem
No.ofstrains identifiedatindicatedlevel within 4 h(by24h)
Group Species (no. of strains) Low
Excellent Good Acceptable discrimination Error
B S. agalactiae(4) 2(2) 0 0 0 0
D S.faecalis(10) 0 10 0 0 0
D S.faecium (11) 4 3 0 0 (3) 0(1)
D S.durans (3) 0 0(2) 0 0(1) 0
D S.avium (10) 0 (9) 0(1) 0 0 0
D S. bovis 1(10) 8(2) 0 0 0 0
D S. bovis II(12) 9 2 0 0 0(1)
None Aerococcusspp. (10) 6 0 0 0 0(4)
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TABLE 3. Levels ofidentification of viridans streptococci andpneumococci by the Rapid Strep system
No. ofstrains identifiedatindicated levelwithin 4 h (by 24 h)
Species (no.of
strains) Excellent Good Acceptable Low Error
S. acidominimus (5) 0 0 (1) 0 0 4
S.constellatus'(10) 5 0 0 1 (1) 3
S.intermedius'(14) 5 0 (1) 0 0 (5) 3
S.mitis(10) 0 0 (10) 0 0 0
S.morbillorum(10) 0 0 0 0 10
S.mutans(10) 0 (10) 0 0 0 0
S.salivarius(10) 0 (4) 0 (3) 0 0 (1) 2
S.sanguis I (10) 1 (1) 1 (2) 0 2 (3) 0
S.sanguis II (10) 0 (2) 0 (4) 0 (2) 0 (2) 0
S. uberis(7) X0 0 0 6
S.pneumoniae (10) 1 3 0 1 (4) 1
Identifiedby the Rapid Strep system as S.milleri(see text).
numbers resulted in alow-discrimination level of identifica- The results of testing 96 strains of viridans streptococci
tion for both strains. and 10strains of pneumococci are shown in Table 3. A total
The resultsoftesting 4 strains of nonhemolytic groupB S. of10 strains of each of the viridans species weretestedwith
agalactiae,56strains of six different groupDStreptococclus the exception of S. acidominimus and S. uberis, for which
species, and 10 Aerococcus strains are shown in Table 2. only 5 and 7 strains, respectively, were available. Four The levels of identification were the same as described strains of the mannitol-positive variant of S. intermedius above. Serological testingwassuggestedforconfirmation of (unidentifiedurine isolates [9]) were also tested. Of the 106
the identities of the group B but not of the group D strains, 55 (52%) were identified at the excellent or good
streptococcal species. Of the 70 strains, 60 (86%) were level. Of the 96 viridans strains, 20 were
identified
at theidentifiedat theexcellentorgoodlevel. Of the 10Aerococ- low-discrimination level, and 29 either were not identified cus strains, 6 were identified at the excellent level, but 4 because of unsatisfactory profile pumbers or were
errone-remained unidentifiedbecause theprofilenumbersthatwere ouslyidentified. The seven correctly identified strains of S. not included in the code book and analysis of the profile constellatuswereidentified as S. milleri type 1 by the Rapid numbers by the manufacturerdidnotresult inidentification. Strep system. Of the eight correctly identified strains of S. A total of66% ofthe strains were identified within 4 h and intermedius, seven and one were identified as S. milleri theremainderof the strains (except the errors)wereidenti- types2 and 3, respectively, by the Rapid Strep system. Of
fied after overnight incubation. In addition to the profile thefourmannitol-positive strains ofS.intermedius, two and
numbers of the four unidentified Aerococcus strains, the onewereidentified asS. milleri types 3 and2,
respectively,
profilenumbers of two S.faecium, one S.avium,andoneS. by the Rapid Strep system. None ofthe 10 strains of S.
duransstrains had to beanalyzed bythemanufacturer. The morkillorum were identified by the Rapid Strep system
analysis of these latter four numbers resulted in a low- becausenodatabase existsfor this species. Confirmationof discrimination, but correct, level of identification for all of identities by testing for optochin sensitivity was suggested
the strains. for all correct identifications ofpneumococci.
TABLE 4. AnalysisofRapid Strepsystemidentificationerrors
Conventional Atypical Rapid Strep system
identification(no. of Atypical
strains)
characteristics"
Identification Identification level(%)S.faecium Arabinose - S.faecalis Excellent(98.9)
S.bovis11 Inulin + S. salivarius Low discrimination(<80.0)
Aerococcussp. (2) None Notlisted
Aerococcussp. (2) Hippurate - Notlisted
S.acidominimus (4) None Notlisted
S. constellatus None Aerococcu.ssp. Good(90.1)
S. constellatus Bile-esculin + Aerococcussp. Low discrimination (<80.0)
S. constellatus Arginine - S. initis Acceptable (87.7)
S. intermedius Arginine -, S. bovis 11 Excellent(99.9)
bile-esculin +
S.intermedius Arginine- S. bovis I1 Excellent (99.9)
S.intermedius Mannitol + S. salivarius Low discrimination (<80.0)
S. morbillorum None Not listed
S.morbillorurn Sucrose - Notlisted
S.salivarius None S.sanguis I Low discrimination(<80.0)
S. salivarius Lactose - S.
equinius
Excellent(99.9)S.uberis (5) None Notlisted
S. uberis Hippurate - Not listed
S.pneumoniae None S. sanguis I Acceptable(87.0)
-,Negative +,positive.
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Of the 106 viridans and pneumococcal strains, 77 (73%) were correctly identified, 20 (18.9%) within 4 h and 57 (53.8%) after 24 h. Only 9 (8.5%) of the viridans and pneumococcal strains were actually misidentified, and an-other 20 strains (18.9%) generated profile numbers that did not lead to an identification. In addition to the 20 profile numbers that remained unidentified, 10 other profile num-bers of viridans streptococci were sent to the manufacturer because they were not contained in the code book. Seven of these profile numbers yielded a correct identification at the low-discrimination level, and three yielded an erroneous identification.
There are variations and shared physiological characteris-tics among Streptococcus species. Some of the errors in identification can be explained on this basis. We have listed all the identification failures in our study in Table 4. We have also listed the atypical physiological characteristics of these strains as determined by conventional tests. The failure of a strain to have all the physiological characteristics of a described species should not negate its identity. There are two possible explanations for errors in identification. First,
an atypical reaction may cause an identification error be-cause the data base is too specific for the species. One test may be too heavily favored for one species. Examples are arabinose-negative strains of S.
faeciumi,
arginine-negative strains of S.conlstellatus
and S. intermedilus, and lactose-negative strains of S.salih'arius.
A second explanation is that some strains are so similar physiologically that we have used serological characteristics to make the final identification. Examples are S. bovis II and S.intermediuis.
When varia-tions in the inulin.arginine,
and bile-esculin reactions oc-curred, we used serological reactions to make the final identification. We identified inulin-positive S.bovis
II as such because we were able to demonstrate the presence of the group D antigen. S.intermediius
and S.saiviarius
strains do not have the group D antigen. We were unable to demonstrate the group D antigen in an arginine-negative, bile-esculin-positive S.intermediius
strain; therefore, we identified this strain as S. intermedius.Also listed in Table 4 are strains that did not have any atypical physiological characteristics. In most cases, the reason that we were unable to identify these strains was that a data base did not exist for these strains (S.
morbilloruim)
or that the data base was too limited to identify the majority of strains tested (S. acidominimuis and S. uiberis).There are inexplicable errors, that is, strains with no atypical physiological characteristics that were erroneously identified (S. constellatus as an Aerococcus sp., S. salivarius as S.
sanguis I,
and S. pneumoniae as S. sanguis I) or remained unidentified (two Aerococcus strains). Only five such strains were included in this study.DISCUSSION
Our evaluation of the Rapid Strep system differed from that of other investigators in that we used a broader spec-trum of Streptococcus strains for our study. Although the Rapid Strep system is designed to identify even a greater number of Streptococcuis species than we included, we chose to test only those strains that have been isolated from human infections in the United States. Two other groups of investigators (1, 12) have tested beta-hemolytic
Streptococ-clis
species,
but neither of these groups of investigatorschose to use different Streptococcus species possessing similar antigens (group A S. pyogenes and S. anginosius and group C S. eqluisimilis,S. anginoslus,and S.zooepideinicius).
Like most other investigators, we agree that serogrouping is
a more rapid, efficient, and useful technique for identifying most clinical isolates of beta-hemolytic streptococci. How-ever, serogroupingdoes not correlate with accurate species identification and in some cases may lead to erroneous assumptions concerning the pathogenicity ofthe identified strain. Beta-hemolytic strains of S. angin0osuswith group A antigen do occasionally occur(4, 6). Group A S. anginiosuis strains do not possess the same virulence factors possessed by group A S. pyogenes strains (4). We are not suggesting that the Rapid Strep system replace serogrouping proce-dures. Rather, we are suggesting that this system could be used in conjunction with serogrouping to accurately define all species of beta-hemolytic streptococci found in human infections. Our data suggest that ifserogrouping is used as suggested by the manufacturer of the Rapid Strep system to confirm the identities of S. pyogenes, S. agalactiae, S. eqiuisitnilis, and groupG streptococci, all the beta-hemolytic streptococci found in human infections would be correctly identified to the species level.
Users of the Rapid Strep system should be aware that the nomenclature used in that system is somewhatdifferent from that which we have suggested (3, 4). The term S. mu/illeni is not included in the list of accepted bacterial species names
(10). and, therefore, we chose not to use it. The beta-hemolytic strains identified as S. /illeni (type 1 or 2) by the Rapid Strep system correlate to our S. tingin0osuis (4). Serogrouping is needed to differentiate S. angin7osius or S.
u/illeii into group A. C, or F categories or nongroupable categories. The non-beta-hemolytic strains identified as S.
milleri type 1 correlate to our S. constellatus, and those identified as S. mu/illeni types 2 and 3 correlate to our S.
imitermnediius.
There is some correlation between themanni-tol-positive variant strains of S. intermediius (unidentified urine isolates, as proposed by Ruoff et al.
[9])
and S. millenitype 3. The correlation is not 100% because one typical strain ofS. intermediiuswas identified asS. milleri type 3 and one mannitol-positive variant strain of S. intermediuis was identified as S. milleri type 2. It is important that all the strains we calledS. constellatuis were called S. milleritype 1 and notS. milleri type 2 or 3. It is important because the only way the correlation between the two nomenclature systems can be made is if there is consistency in the distinction between S. milleri type 1 and S. milleri type 2 or 3. All the strains identified as S. milleri type 2 or 3 were S.
interme-dilus. Thus, there is consistency, and the correlation can be made. Hemolysis serves todifferentiate between S. angino-sus and S. constellatus in our system.
The overall identification of the group D
Streptococcuis
species by the Rapid Strep system in our study wassimilar to that in other studies (1, 9, 12). We tested strains of S. avium
and S. bovis II not included in other studies of this product. Only2 of 54 strains of group D streptococci were erroneous-ly identified. The identification of a S. faecium strain as S. faecalis was notparticularly serious because both strains are enterococci. Theidentification of a strain of S. bovis II as S. salivarius was not significant either. Both S. bovis II and S. salivarius are non-enterococci, and patient management is similar. It is particularly encouraging to note that all the S. bovis I strains were identified at the excellent level. There is increasing interest in using this Streptococcus species as an indicator ofcolon cancer (7, 8). The accuracy with which S. bovis I can be identified will be very meaningful for physi-cians using this correlation.
Our data indicate that the manufacturer should consider expanding the data base for identification of Aerococcus strains. The aerococci are difficult to identify with
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tional systems because of their diverse physiological charac-teristics. Therefore, any system that would correctly identify these species would be ofsignificant value (3).
We tested a broader spectrum of viridans Streptococcus species than did other investigators (1, 9, 12). We included the infrequently occurring strains of S. acidominimus and S.
uberisas well as strains of S. morbillorum not included in the database. The accuracy of identification by the Rapid Strep systemin identifying the viridans Streptococcus specieswas species specific. For example, all strains of S. mitis, S. mutans, S. sanguisI, and S. sanguis 11 (10 strains each) were correctly identified. However, the Rapid Strep system erro-neously identified 3 of 10, 3 of 14, and 2 of 10 strains of S. constellatus, S. intermedius, and S. salivarius,respectively. The greatest failure of the Rapid Strep system was found for
strains of S. acidominimus, S. morbillorum, and S. uberis. No actual identification errors were made with these strains,
butthe system failed to provide identification for 4 of 5, 10 of 10, and 6 of 7 strains of S. acidominimus, S. morbillorum, and S. uberis, respectively.
We did not observe the same identification problem with S. pneurnoniae that Appelbaum etal.(1) did. Of 10 strains of S. pneumoniae, 9 were correctly identified by the Rapid Strep system in our study, whereas only 11 of 24 were correctly identified in their study. We did not take any special care with the inoculum, as indicated in their study. The only error in our study was that one strain of S.
pneumoniae was identified as S.
sanguiis
I. This strain was tested again in the Rapid Strep system, as were all strains erroneously identified in our study. Repeat conventional identification assured us that the strain was S. pneumoniae. It was encouraging that none of the viridans Streptococcus species was erroneously identified as S. pneumoniae. This would be a serious error because S.pneiumoniae
is consid-ered much more virulent than any viridans streptococci.Ourdataindicate that rates and levelsof identification by the RapidStrep system are different for eachStreptococcus
species. Thus,it is not accurate to give an overall identifica-tion rate for the streptococci or, for that matter, for the
different categories of streptococci, such asbeta-hemolytic, enterococcal, viridans groups, etc. Our data indicate that the
Rapid Strep system accurately identifies nearly all the
beta-hemolyticstreptococci found in human infections when used in conjunction with serogrouping. The same may be said for the identification of group D streptococci, as 98% of the enterococcal and 95% of the non-enterococcal strains were
correctly identified. When the viridans streptococci were divided into the more frequently occurring species, S. con-stellatls, S. intermeditus, S. mitis, S. initans, S. salivarius,
S. sanguis I, and S. sanguis II, and the less frequently
occurring species, S. acidominimus, S. morbillorum, and S. uberis, the rates of identification for these two groups by the Rapid Strep system were85% and 10%, respectively. A total of 90% of the S. pneumoniae strains and 60% of the aerococci were correctly identified by the Rapid Strep system.
Weconclude from this study that the Rapid Strepsystem is more rapid and efficient than conventional identification systems, but improvement in the data base is needed for
certain Streptococcus species.
LITERATURE CITED
1. Appelbaum, P. C., P. S. Chaurushiya, M. R. Jacobs, and A. Duffett. 1984. Evaluation of the Rapid Strep system for species identificationof streptococci. J. Clin. Microbiol. 19:588-591. 2. Facklam, R. R. 1977. Physiological differentiation of viridans
streptococci. J. Clin. Microbiol. 5:184-201.
3. Facklam,R.R. 1980.Streptococciandaerococci,p.88-110. In E.H. Lennette, A. Balows,W.J.Hausler, Jr.,and J. P. Truant (ed.),Manualofclinicalmicrobiology,3rd ed. American Socie-ty forMicrobiology, Washington, D.C.
4. Facklam, R. R.1984. Themajor differencesin the American and British Streptococcus taxonomy schemes withspecialreference toStreptococcus milleri. Eur. J. Clin. Microbiol. 3:91-93. 5. Gerber, M. A. 1983. Micronitrousacid
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6. Jablon, J. M., B. Btust, and M.S. Saslaw. 1965. 3-Hemolytic streptococci with group A and type II carbohydrateantigens. J. Bacteriol. 89:529-534.
7. Klein,R. S., R. A. Recco, M. T. Catalana, S. C. Edberg, J.I. Casey, and N. H. Steigbigel. 1977. Association of Streptococcus bovis with carcinoma of the colon. N. Engl.J. Med. 297:800-802.
8. Reynolds, J. G., E. Silva, and W. M. McCormack. 1983. Association of Streptococ c us bovis bacteremia with bowel disease. J. Clin. Microbiol. 17:696-697.
9. Ruoff, K.L., and L. J. Kunz. 1983. Use of theRapid STREP system for identificatiort of viridans streptococcal species. J. Clin. Microbiol. 18:1138-1140.
10. Skerman, V. B. D., V. McGowan, and P. H. A. Sneath. 1980. Approved lists of bacterial names. Int. J. Syst. Bacteriol. 30:225-420.
11. Slifkin,M., and G.M.Gil. 1982.Serogroupingof beta-hemolyt-ic streptococci from throat swabs with nitrous acid extraction and the Phadebact streptococcus test. J. Clin. Microbiol. 15:187-189.
12. Waitkins, S. A., D. R. Anderson, and F. K. Todd. 1981. An evaluation of the API-Strep identification system. Med. Lab. Sci. 38:35-39.
