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CLINICAL MICROBIOLOGY REVIEWS, Oct. 2002, p. 613–630 Vol. 15, No.

0893-8512/02/$04.00⫹0 DOI: 10.1128/CMR.15.4.613–630.2002

What Happened to the Streptococci: Overview of Taxonomic
and Nomenclature Changes
Richard Facklam*
Streptococcus Laboratory, Centers for Disease Control and Prevention,
Atlanta, Georgia 30333

INTRODUCTION .......................................................................................................................................................613
BETA-HEMOLYTIC STREPTOCOCCI..................................................................................................................614
Streptococcus pyogenes..............................................................................................................................................614
Streptococcus agalactiae ...........................................................................................................................................616
Streptococcus dysgalactiae subsp. dysgalactiae .......................................................................................................616
Streptococcus dysgalactiae subsp. equisimilis .........................................................................................................617
Streptococcus equi subsp. equi ................................................................................................................................617
Streptococcus equi subsp. zooepidemicus ................................................................................................................617
Streptococcus canis ...................................................................................................................................................617
Streptococcus anginosus Group ...............................................................................................................................617
Streptococcus constellatus subsp. pharyngis ...........................................................................................................619
Streptococcus porcinus..............................................................................................................................................619
Streptococcus iniae....................................................................................................................................................619
Streptococcus phocae and Streptococcus didelphis..................................................................................................619
NON-BETA-HEMOLYTIC STREPTOCOCCI .......................................................................................................619
Streptococcus pneumoniae ........................................................................................................................................619
Streptococcus bovis Group: S. bovis, S. equinus, S. gallolyticus, S. infantarius, S. pasteurianus,
S. lutetiensis ..........................................................................................................................................................620
Streptococcus suis .....................................................................................................................................................621
Viridans Streptococci .............................................................................................................................................621
Streptococcus mutans Group ...................................................................................................................................622
Streptococcus salivarius Group ...............................................................................................................................623
Streptococcus anginosus Group ...............................................................................................................................623
Streptococcus sanguinis Group (Formerly Known as S. sanguis).......................................................................623
Streptococcus mitis Group .......................................................................................................................................623
Options for Identification of Viridans Streptococcal Species...........................................................................624
Antimicrobial Susceptibilities of Viridans Streptococcal Species....................................................................624
Streptococcus acidominimis......................................................................................................................................625
Streptococcus pluranimalium ...................................................................................................................................626
Streptococcus thoraltensis .........................................................................................................................................626
Streptococcus uberis and Streptococcus parauberis ................................................................................................626
Streptococcus urinalis ...............................................................................................................................................626
Dolosicoccus paucivorans .........................................................................................................................................626
Facklamia species and Ignavigranum ruoffiae ......................................................................................................626
Globicatella sanguinis...............................................................................................................................................626
New Species Not Yet Tested ..................................................................................................................................626
CONCLUSIONS .........................................................................................................................................................627
ACKNOWLEDGMENTS ...........................................................................................................................................627
REFERENCES ............................................................................................................................................................627

INTRODUCTION help delineate differences in bacterial genera and species. The
1984 Bergey’s Manual of Systemic Bacteriology listed only seven
The purpose of this communication is to outline the changes
genera of faculatatively anaerobic gram-positive cocci (GPC);
in taxonomy and nomenclature of the Streptococcus genus that
have occurred in the past 15 years. These changes are the Aerococcus, Leuconostoc, Micrococcus, Pediococcus, Staphylo-
result of the application of DNA-DNA reassociation, 16S coccus, Streptococcus, and Stomatococcus (108). At present
rDNA gene sequencing, and other molecular techniques that there are 17 different genera of GPC. The discussion is limited
to the Streptococcus genus and closely related GPC that are
catalase negative and display chains in the Gram stain. Tech-
* Mailing address: Streptococcus Laboratory, Centers for Disease
Control and Prevention, Mail Stop CO-2, Atlanta, GA 30333. Phone: nically, Leuconostoc bacteria fit into this category, but discus-
(404) 639-1379. Fax: (404) 639-3123. E-mail: sions on changes in this genus are not included, because iden-


based on serogrouping. because these organisms grow slowly can be found in a review written in 1995 (52). and Ignavigranum [36]). but some changes are patient from whom the organism was isolated. the genus Strepto. 54). and G). were not salt tolerant. and two recently Sherman’s lactic division was reclassified as the Lactococcus described species. didelphis (106). One of the most included to explain changes in the Streptococcus genus. Sherman most useful phenotypic characteristics of streptococci is the proposed a scheme for placing the streptococci into four cat- reaction of the bacteria on blood agar plates. dysgalactiae is not beta-hemolytic but is included for tolerant to high-pH growth conditions. and the enterococci. The number and phenotypic characteristics to help establish the species and of Enterococcus species has increased to more than 20. Streptococcus pyogenes The classification and identification of streptococci was se- verely hampered by a hierarchical dichotomous approach re. S. S. those that were not. other character. (131). were not subsp. Investigators used a variety of techniques in- istics such as the capacity to grow in broths at high pH. Sherman’s lactic division included strains species. differentiated them from the other three divisions. 1. and by failing to grow in broth containing 6. The ma. of the species. as well as the somewhat cumbersome classification coccus was split into three genera (Enterococcus. appreciably different from that of today’s identification systems Table 1 lists all beta-hemolytic streptococci known to date. Many useful tools applied to the revision of the classification system new species of streptococci have been added to the genus. In 1937. tiae subsp. taxonomic reasons. high salt cluding DNA-DNA reassociation. identification of streptococci to the species level is and Streptococcus) (110. Vieira et al. Figure 1 depicts a phylogenetic tree of the (Abiotrophia [35]. It is the most size. This group is still known today as the and subspecies of beta-hemolytic streptococci. E. tification procedures and clinical relevance of the leuconostocs exceptions. fermentation and tolerance tests were the only tests used for differentiating many of the streptococci. dysgalactiae. The pyogenic division in. With the exception of S. They were not associated with human infections. Shortly before and may require additional factors for isolation and character- the publication of Bergey’s Manual in 1986. It is very cluded the beta-hemolytic strains with defined group antigens important that clinical and physician office laboratories accu- (A. (136). dysgalac- at 45°C. F. Changes in the Enterococcus and rarely performed in time to be relevant to the treatment of the Lactococcus genera are not detailed. Fack. and group carbohydrate antigens) that resulted pathogenic bacterium in the genus Streptococcus. These categories were organized by hemolytic reac- as a guide for managing patients as well as an aid in classifi- tion. Sherman’s four 1919 first defined the reactions of streptococci on blood agar divisions were the pyogenic division. 111). The last column gives the most common beta-hemolytic. one of the ated with the beta-hemolytic strains (88). ogist can easily place the species into groups that are pheno- The earliest attempt at differentiating the streptococci was typically related with only a few microbiologic tests. Moreover. Lactococcus species that have recently species listed in Table 1 have been isolated from human infec- been isolated from human infections have phenotypic charac. Columns 3 to 12 list 10 phenotypic characteristics that that were associated primarily with the manufacture of dairy can be used to help identify the streptococci to the species level products. tions. Before 1933. dysgalactiae streptococcal species that were not beta-hemolytic. Sherman’s viridans division included There is one exception included in this table. H.614 FACKLAM CLIN. S. Column 2 lists viridans streptococci. Table 1 was constructed based on the molecular and teristics that are not the same as those described by Sherman phenotypic characteristics described by Schleifer and Kilpper- (48. ization. cation of the bacterium to the species level. In 1933 Lancefield reported the technique of BETA-HEMOLYTIC STREPTOCOCCI demonstrating specific carbohydrate “group” antigens associ- For clinical laboratories as well as taxonomists. C. I have chosen to present the identification jority of these genera were split off the Streptococcus genus by schemes listed in the following tables based strictly on pheno- typic characteristics because I feel that the clinical microbiol- genetic and phenotypic information. equi subsp. the viridans division. concentrations. All of subspecies included in this table. Dolosicoccus [34]. 16S rDNA sequencing. and many more species have been added the Lancefield group antigens that are associated with each to this classification.5% NaCl. group carbohydrate antigens. phocae (119) and S. multilocus enzyme electrophoresis. Granulicatella [35]. Streptococcus genus. Although own unpublished results of testing all reference strains for each some of the enterococci were beta-hemolytic. All clinicians in species definitions that are often qualified by a number of should be aware that GAS is the agent that causes bacterial . This division of the streptococci is not rately identify the beta-hemolytic reactions of the streptococci. Vandamme et al. This monograph is no longer available. Globicatella [28]. hemolysis. the plates (23). pyogenes is also known as beta-hemolytic group A strep- lying on a very limited number of complex characters (colony tococcus or Lancefield’s group A strep (GAS). Column 1 in Table 1 lists all the species and did not grow at 10°C. all the genus in the mid-1980s. by having the capacity to grow at 10°C but not natural host of the species. and for the Streptococcus genus is the application of 16S rRNA six new genera of GPC that form chains have been established gene sequencing. Lactococcus. currently available sequences for the species included in the lamia [29]. Hemolysis is used egories. system. and phenotypic tests (pri. equi. the new species have phenotypic characteristics similar to those described by Sherman (54). and our and included the four species known at that time. but Brown’s lactic division. Brown in marily fermentation and tolerance tests) (116). REV. S. Sherman’s fourth division was termed the enterococci Balz (111). when hemolysis and identification of group carbohydrate an- This group differed from the pyogenic group by not being tigen fail to do so. who used blood phenotypic groups do not necessarily correlate with the groups agar to differentiate strains that were beta-hemolytic from shown in the genetic tree in Fig. J. B. These probably made in 1903 by Shottmuller (118). MICROBIOL. and a wide temperature range (10 to 45°C) whole-cell protein analysis. definitions are accurately shown in reference 122.

2002 TAXONOMIC CHANGES IN THE STREPTOCOCCI 615 FIG. The units at the bottom of the tree indicate distance between sequence pairs. The dendrogram was constructed by the clustal method using the DNASTAR program.VOL. 15. Phylogenetic relationship among 55 Streptococcus species based on analysis of 16S rRNA gene sequences. 1. .

Esc. and ␤-glucoronidase needs to be performed. This species is included Presumptive identification can be made by bacitracin suscep. C ⫺ ⫺ ⫺ ⫹ ⫺ ⫹ ⫹ ⫺ ⫺ ⫹ NA Human pharyngis S. S. Streptococcus dysgalactiae subsp. agalactiae is the in most cases the emm type reflects the M-protein serologic only Streptococcus species that has the group B antigen. Hip. Str.cdc. dysgalactiae subsp. or Lancefield’s group B streptococcus (GBS) is the type specificity of each antigen. these strains are not common. ⫺ ⫹ ⫹ ⫹ v ⫹ ⫹ ⫺ ⫹ ⫹ NA Swine. trehalose. V. In recent years. v. C. equi subsp. an alternative system called emm typing been explored for the prevention of GBS disease: the devel- has been developed. ⫹. pyogenes A ⫹ ⫹ ⫺ ⫺ ⫺ ⫹ v ⫺ ⫺ NA ⫺ Human S. intermedius. ⫺. equisimilis gives the opposite reactions. none. pyogenes (Table 1). Two major avenues of investigation have years. fish. Reference specific antisera to many of these antigens and used the anti. canisc G ⫺ ⫺ ⫹ ⫺ ⫺ ⫹ ⫹ ⫺ ⫺ v NA Dog. S. None ⫺ ⫺ ⫺ ⫹ ⫺ ⫹ ⫹ ⫺ ⫺ ⫹ NA Human S. dysgalactiae is the only species listed on tified by demonstration of the group A antigen on the cell. G. deamination of arginine. therefore. these two presumptive tests are very accurate in gen. G. pyogenes is tions. The exact composition of the taxon Streptococcus dysgalac- galactiae subsp. dysgalactiae subsp. b S. anginosus is given below tiae has been in a state of flux for the past few years. variable reaction 6 to 94% positive. which uses the sequence of the gene that opment of vaccines (115) and the screening procedures for the encodes the M-protein hyperviable region. below). anginosus group includes beta-hemolytic strains of S. impetigo. and ribose broth. hydrolysis of esculin. agalactiae. pyogenes is best iden. but from the information available to us at the Centers for Disease Control and Preven. constellatus.html. zooepidemicus C ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ v ⫹ ⫹ v NA Animals. This surface antigen is the antigen that allows the Streptococcus agalactiae GAS to avoid phagocytosis and to survive in the human host. the most common cause of neonatal sepsis (113). zone of lysis). The true incidence of non-S. VP. S. constellatus subsp. MICROBIOL. dysgalactiae subsp. Cam. cervical or vaginal carriers and sub- tween the serologic and emm typing systems is very good. porcinus E. equisimilis. canis and group G S. but not both. Voges-Proskauer reaction. human S. human new S. More information regarding the two species S. testing of ␣-galactosidase. group carbohydrate antigen. 113 is an excellent starting point for those interested in learn- sera in a capillary precipitin test to subtype the GAS (87). R. where these two species are discussed. REV. dysgalactiae subsp. not applicable. bovine S. human S. Pyr. The emm typing system can be accessed through the CDC other streptococcal species have recently been identified how- web site http://www. these tests alone are not 100% specific diseases caused by this bacterium (39). pyrrolidonylarylamidase. NA. The major (but not for S. CAMP reaction. c To differentiate between the group G S. that cross-react with commercial slide agglutination tests Methods for emm typing and the sequences of more than 120 (see the discussion of S.616 FACKLAM CLIN. porcinus. pharyngitis. dysgalactiae tion (CDC) Streptococcus laboratory. pyogenes GAS strains found the identification. This ing more about the epidemiology and types of diseases caused system is still in use in some laboratories after more than 60 by this organism. negative reaction ⬎95%. pyogenes strains Isolation of this bacterium from human infections has not been . d The S. Arg. TABLE 1. in human infections is unknown. iniae None ⫺ ⫹ ⫹ ⫺ ⫺ ⫺ ⫹ ⫹ ⫺ NA NA Dolphin. and S. Table 1 that is not beta-hemolytic. L ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫺ ⫺ ⫹ ⫹ Human. tibility or pyrrolidonylarylamidase activity. The hypervariable N-terminal portion of this protein dictates S. animals S. F. ever. exclusive) virulence factor associated with GAS is the M-pro- tein antigen. presence of GBS in anal. dys. Tre. S. Sbl. P. resistant to bacitracin. agalactiae B ⫺ ⫺ ⫹ ⫺ ⫹ ⫹ ⫺ ⫺ ⫺ NA NA Human. human S. hydrolysis of hippurate. canis is positive for ␣. Identification of the beta-hemolytic streptococcia Species Lancefield group Bac PYR Cam VP Hip Arg Esc Str Sbl Tre Rib Origin S. equisimilisc A. anginosus (group)d A. U. anginosus. dysgalactiaeb C ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ v ⫺ v ⫹ ⫹ Animals subsp. respectively. Correlation be. dysgalactiae strains are not beta-hemolytic but are included in this table for taxomonic reasons. Lancefield prepared type. Bac.and ␤-galactosidase and negative for ␤-glucoronidase. S. production of acid in sorbitol. S. and sequent antimicrobial management (112). positive reaction ⬎95%. and Rib. S. hydrolysis of starch. because of the other subspecies included in this discussion. Some of the other beta-hemolytic strepto- an excellent source of information for interested investigators cocci can also be positive in one or the other. Together with the unique hemolytic reaction (very small not the only Streptococcus that may possess the group A anti. didelphis None ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫺ ⫺ ⫺ ⫹ NA Opossum a Abbreviations: Group. ␤-galactosidase. dysgalactiae subsp. susceptible. phocae C. C. presumptively identified by the CAMP and hippurate reac- From Table 1 the reader can determine that S. and a host of other infections including are the only beta-hemolytic streptococci that are positive in severe invasive diseases. There are insufficient data to know the percentage of each of these beta-hemolytic species that contain carbohydrate antigens. The recent review by Cunningham is both of these tests. equisimilis and S. equi C ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ v ⫹ ⫺ ⫺ NA Animals subsp. GBS can also be emm-types of GAS are described in references 7 and 8. of to familiarize themselves with the severity and diversity of these tests. F ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ NA NA Seal S. Some type.

Later inves. zoo- streptococal species. and the isolation of S. equi. Whiley et al. equi subsp. intermedius. These authors also state that there tends to be an . canis is an organism that was described in 1986 as having tigations (131. equi has a protein that induces opsonic antibodies in more common than beta-hemolytic strains. dysgalactiae and S. S. it is tempting to speculate S. constellatus tend to Streptococcus equi subsp. The phenotypic tests in Table 1 should be used. equisimilis or Lance. hydrolysis of esculin (70% of strains) and starch. The organism has virulence factors similar to associated with a large outbreak of nephritis in Brazil (5. dysgalactiae should be phenotypic testing of isolates from dogs was described in 1994 placed in different category. pyogenes. and L S. thus creating two separate sub. the Lancefield group G antigen and was isolated from animals. identification of S. epidemicus has a surface-exposed protein (Szp) that is antigeni- ditional phenotypic or genetic characteristics should be used to cally variable. canis from a human with sepsis species. antigens or no group antigen. dysgalactiae. Unlike S. equisimilis) and Lancefield’s group G and L strains should be most frequently dogs (hence the name “canis”) (41). 94). the consumption of contaminated dairy products. equisimilis possess the clinical laboratories do not perform phenotypic tests on group group A antigen (15. equisimilis strains are found in human infections. lytic reaction. all of these entities were placed in the S. and S. this species has not been isolated from humans. the species known as S. that this group includes three distinct species and more sub- together with hemolytic reaction and group antigen. although these authors state that hemolysis and group antigens are of little value in differ- entiation of the species. (94) provides references to cation by determining the characteristics in Table 1 should be previous nephritis outbreaks and other infections caused by considered presumptive. equisimilis also have virulence factors similar to S. Most recently. equi is a beta-hemolytic group C strains may possess one of four different Lancefield group Streptococcus that causes strangles in horses. and identify this bacterium (61). differ. investigators have shown that frequently S. zooepidemicus be beta-hemolytic than of either S. viridans ism is a frequent cause of bovine mastitis. dysgalactiae subsp. intermedius are rarely beta-hemolytic (139. It is not rience at the CDC.. demonstration of the group C antigen. S. equi subsp. G. DNA-DNA reassociation studies clearly show that the aforementioned species are distinct taxons (83. There are Streptococcus equi subsp. may also have group C antigen (50). Since S. Determining that an alpha-hemolytic this bacterium. species (139. 136) indicated that Lancefield group C strain (S. Like S. Lancefield’s group G and L strains. Identifi. epidemicus is identified by beta-hemolysis. and halose. dysgalactiae subsp. S.g. canis is isolated from humans. equi fact that non-beta-hemolytic strains of the three species are subsp. dysgalactiae subsp. the strains possessing different group antigens of S. confusion about terminology and classification than the group The group antigen can be used only as an aid in species of organisms listed as S. intermedius were all the species possessing Lancefield’s group C antigen. 141. those of S. zooepidemicus is Isolates of S. dysgalactiae subsp. 142). e. constellatus. anginosus (Table 1). anginosus. general classification of viridans streptococci. There is no doubt identification. Genetic investigations indicated presence. including M-like proteins (133). Adding to the confusion is the edge. 2002 TAXONOMIC CHANGES IN THE STREPTOCOCCI 617 documented. Non-beta-hemo- horses and is thought to be involved in the organism’s virulence lytic varieties of each of the three species are grouped into the (125). 80). and occasional fermentation of tre- strain or S. 20). that Lancefield’s group C strain (also known as group C human fermentation of sorbitol. dysgalactiae G streptococci other than the hemolytic reaction and group subsp. dysgalactiae was Streptococcus canis the oldest officially recognized species. dysgalactiae Streptococcus anginosus Group subsp. shares certain structural features with the S. Although this protein does not have significant se- Streptococcus dysgalactiae subsp. equisimilis. group C and G strains are found much known whether human strains will have the same phenotypic more commonly in human infections than are group A and L characteristics. found in human infections. more isolates of S. anginosus or S. including emm gene homologs (17. dysgalactiae were all genetically similar and should be included in one taxon. Ad. S. 144). Identification of this subspecies is based on the hemo. S. group C antigen field’s group C Streptococcus. and the Streptococcus equi subsp. equisimilis is the revised taxonomic that Szp also plays an antiphagocytic role. The determination. The phenotypic profile given in Table 1 for the true incidence figures are difficult to estimate but in our expe. More recently. equi subsp. pyogenes M pro- tein (94).VOL. anginosus or S. Group A. stimulates opsonic protective antibodies. 142). It is not possible to estimate how subsp. equisimilis). to identify species. other non-beta-hemolytic streptococci. strains of this species. S. zoo- epithet for what was previously termed S. equi subsp. equi beta-hemolytic strains of each of the three species. (135). C. dysgalactiae was reported in 1997 (16). equisimilis quence homology to the M protein. milleri” was that it was can have the group C antigen. never accepted by the taxonomist as a confirmed taxonomic entity. Extensive grouped into one category and that S. pyo- genes. and fermentation of of chromogenic substrates for the differentiation of the three sorbitol and trehalose (Table 1). S. In addition. dysgalactiae classification (55. Most human infections can be traced back to streptococcus has group C antigen is insufficient for identifi. A total of collectively known as either S. milleri at one six different beta-hemolytic streptococcal species or subspecies time. To my knowl. The problem with the term “S. 15. have proposed an identification scheme based on degradation ences in hydrolysis of esculin and starch. 27) (see the CDC None of the beta-hemolytic streptococci has caused more web site above). This organ- cation. this organism was 142. The publication by Nicholson et al. S. canis is that of nonhuman strains. because most some strains of S.

618 FACKLAM CLIN. 70). The Fluo- Card Milleri (Key Scientific. Two enzymes that may be considered virulence factors are ␣-N-acetylneuramidase (sialidase) and hyaluronidase. and ␣-glucosidase (58). v. A. Tex. some of which corre- late with the entities listed in Table 2 (71). N fucosidase. constellatus v produces only hyaluronidase. while S. N S. col- v v umn 1 under each of the species represents a beta-hemolytic variant of each species. Column 1 under S. Identifi- Non-beta-hemolytic cation of the beta-hemolytic as well as non-beta-hemolytic S. and so all 70 strains in their study were placed Test ␤-Galactosidase N. and ␤-galactosidase (63). ⫺. Whiley’s scheme (139. France) (not available for clinical ␤-N-Acetylgalactosaminidase microbiology use in the United States) includes N-acetyl-␤- ␤-N-Acetylglucosaminidase Amygdalin (acidification) glucosaminidase. anginosus Column 3 under S. Table 2 has been con- structed from the data presented in references 1. 97% of S. Very little is known about virulence factors produced by this group of bac- Beta-hemolytic subsp. Non-beta-hemolytic S. constellatus Beta-hemolytic often have group F. N molecular documentation. and S. 141) is F. Additional variants of S. ⫺ ⫺ ⫺ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹ ⫺ ⫺ v intermedius strains. The production of these enzymes is part of the identifi- cation scheme proposed by Whiley et al. G. 139. 141. Marcy l’Etoile. pharyngis teria. 142. 14. Column 2 under each of the species listed in Table 2 ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫺ ⫺ represents the original Whiley description of the species. Limia et al. intermedius The distribution of the group antigens also shows some asso- ciation with the species. 72. Other investigators have also found similar distributions of ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫺ ⫺ N v v the three species using Whiley’s scheme and DNA reassocia- Data from references 14. Commercial iden- ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫺ ⫹ ⫹ ⫺ ⫺ tification systems that have three of the seven chromogenic v substrates suggested by Whiley et al. N cluded. variable reactions positive in 8 to 91% of strains. The hemolytic reaction and Lancefield group antigens that are commonly associated with Beta-hemolytic the three species are also included. tion as reference identification procedures (121). constellatus species are given in Table 2. Subspecies are also in- F. constellatus strains. (145). positive reactions ⱖ92% of strains. ⫹ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹ ⫹ ⫹ ⫺ ⫺ C intermedius produces both of these enzymes. constellatus TABLE 2. S. Compared to the Whiley scheme. REV. All the species and subspecies listed ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹ ⫹ in this table should have the phenotypic characteristics of the S. The Rapid ID-32 Strep system (Bio- Mérieux. Isolates of S. this system identified 98% of S. C. anginosus is the description of the “motile A. (139. angi- nosus is the description of the group of strains identified but not proposed for subspecies status by Whiley et al. 121. Identification of the S. while isolates of S. 144. Raffinose (acidification) Mannitol (acidification) ␣-N-Acetylneuramidase Lactose (acidification) These authors did not use a reference method to compare their Lancefield antigenc identification. G. and 129–135. anginosus isolates are commonly isolated from urogenital and gastrointestinal sources. anginosus group listed in Table 1. S. anginosus produces nei- ther. ␤-glucosidase. C. and column 3 represents an official or Non-beta-hemolyticb unofficial subspecies designation of that particular species.) includes ␤-D- Beta-hemolytic C. anginosus have been described based on ribotypes. and 88% of S. The a b c agreement between the genotypic method and the Rapid . no antigen. and G antigens (in order of frequen- cy). nosus strains. intermedius rarely have group antigens. Non-beta-hemolytic S. anginosus groupa v v three species and potential subspecies. S. ␤-glucosidase. 65–67. There was an 80% agreement between the genotypic method and Whiley’s method. Round Rock. intermedius ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫺ ⫺ N v v strains are commonly identified from brain and liver abscesses. ␤-D-Fucosidase into one of the three species. F. (90) evaluated the Hyaluronidase ␤-Glucosidase ␣-Glucosidase Rapid ID-32 Strep system as well as the Whiley system against Hemolysis a line blot hybridization assay. angi- Motile variant described in reference 14. 70. anginosus and S. ⫹. constellatus is often isolated from respiratory and many other sources. milleri” strains (14. are available. F. 71. MICROBIOL. and confirmation of subspecies may require additional F. positive reaction ⱕ8% of strains. 141). N considered a standard for phenotypic identification of the ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫺ ⫺ subsp. and 145. association between the clinical sources and the three species. This table should be used as a guide for identification of the species. S.

iniae were isolated from freshwa- Becton Dickinson Microbiology Crystal Gram-Positive system ter dolphins. There is no documented enzyme or toxin that affects species. sition of the medium including the type of blood and incuba- fections. but sporadic reports of this organism fication of these species has been described. While deter- that most human isolates of S. agalactiae lyse red blood cells weakly. An outbreak ␣-glucosidase. porcinus lyse red blood cells Major developments in the formulation of vaccines for adults . didelphis have not been of the redefined species and subspecies. and cause of community-acquired pneumoniae. few years for S. pharyngis lists the tests to identify the sub. anginosus group are well documented. Streptococcus pneumoniae servation of the hemolytic reaction can be a useful indicator of S. The reactions listed in Table 2 in column 3 under S. mination of the group D antigen for identification of S. has been reported (138). dans streptococci. The greening or partial destruction of red blood cells is pro- duced primarily by the production of hydrogen peroxide by the Streptococcus porcinus streptococci. intermedius (124). group C antigen (145). phocae and S. we know that beta-hemolytic strains of all species have been isolated from human infections Streptococcus phocae and Streptococcus didelphis (with and without various Lancefield antigens). 2002 TAXONOMIC CHANGES IN THE STREPTOCOCCI 619 ID-32 Strep system was 76%. suis tion group B reagent has also been reported to react with are useful. ␤-glucosidase. S. lished reports and our own testing of the type strains for these constellatus that is beta-hemolytic and carries Lancefield’s two species (Table 1). The peroxide destroys some of the red blood cells The beta-hemolytic streptococci that carry Lancefield group and releases hemoglobin into the medium surrounding the E. It is not useful to try to distinguish between alpha- under S. A third commercial system available for identification of the three species is the The original cultures of S. The compo- nosus and was not necessarily associated with pharyngeal in. Lancefield extracts of these strains non-beta-hemolytic streptococcal species. and species-specific probes (70) have all teristics listed in Table 1 for definitive identification. The incidence and the importance of molytic. Molecular technology for specific identi. pharyngis beta-hemolytic streptococci were obtained from these pub- Whiley et al. pharyngis and constellatus. but we know very little about the incidence and clinical significance of each As noted above. the other hand. agalactiae. anginosus). with identification of only 57% of the S. Nonhemolytic variants of S. cocci. occurs. and S. The latter system was particularly in an agar plate in a much larger area around colony growth inaccurate. agalactiae. porcinus (30). is of very little value for identification (50). In summary. and determination of group R or other type antigens for S. didelphis has been isolated from opossums (106). from the human genitourinary tracts of female patients of and cultures that appeared “alpha-hemolytic” will be nonhe- reproductive age (53). Slide agglutina. the DNA-DNA reassociation per. and V and four new antigens were included in a streptococcal colony that appears green-like. U. S. Streptococcus iniae ulum density and growth conditions (1). including the viri- generally do not react with CDC group B antiserum (124). second group of beta-hemolytic group C and one strain of Whether there are nonhemolytic variants of the other strepto- group G streptococci were also described in this report but not coccal species that are normally beta-hemolytic remains to be formally proposed as a subspecies (see column 1 of Table 2 determined. Pulsed-field gel have been rare at the CDC. and clinical microbiologists should be aware of the No changes in the classification have been made in the past potential for misidentification of these isolates as S. Although still within the parameters of the criteria for inclusion in the species. constellatus subspp. pyogenes. Very little information is available about the of bacteremic disease in humans who handle contaminated fish utility of this system. 15. been described. most useful characteristics for the identification of strepto- ences in the chromogenic substrate degradation are also dif. These beta-hemolytic group C strepto- cocci have a predeliction for the human throat and cause NON-BETA-HEMOLYTIC STREPTOCOCCI pharyngitis. S. A members of the S. hemolysis and no hemolysis on blood agar plates. The data for identification of these two Streptococcus constellatus subsp. and ferent for S. Phenotypic differ. porcinus. If oxygen is re- description of S. Most strains isolated from human sources react with antiserum prepared against one of the new group antigens. sequencing of specific genes (98) and 16S out group antigen should be tested for the phenotypic charac- rRNA genes (12). There have been reports that some of the problems with the Rapid ID-32 system is with preparation of the inoc. phocae has been isolated from seals (119). This system has ␤-N-fucosidase. P. S. Beta-hemolytic streptococci with- electrophoresis (6). porcinus has been isolated moved from the growth atmosphere. and the increasing colonies of GBS are surrounded by a small zone of lysis. bovis cially prepared GBS grouping antisera (124).VOL. have recently described a subspecies of S. angi. This group was closely related to S. red blood cells to produce alpha-hemolysis by streptococci. On prevalence of multidrug resistance is of great concern (147). the determination of hemolysis is one of the centages are different for the subspecies. Careful ob. determination of Lancefield antigens of all other nonhuman strains (67). typical strains of S. confirmed as being isolated from humans. and can be transmitted to humans via the fish (138). S. The value of identification of Lancefield antigens on this finding are inconclusive and are complicated by the fact non-beta-hemolytic streptococci is also limited. strains. This organism is still the leading Typical strains of S. tion atmospheres can influence whether “alpha” hemolysis constellatus subsp. As stated above. pneumoniae. peroxide is not formed. porcinus react with commer. iniae is also found in aquacultures of fish and (137).

pasteurianus and the times referred to as S. lute- ther biotype I nor biotype II of human origin was sufficiently tiensis (99). Further studies (45) confirmed that no lysin (59). gallolyticus species based on DNA techniques. infantarius subsp. bovis bovis group begin with a report published in 1984 (56). bovis II. bovis by current identification proce- been shown to improve the identification of culture-negative dures did in fact join the S. (96) demonstrated that strains isolated from the viridans Streptococcus. bovis II/2 were closely related to the S.e. MICROBIOL. optochin. pneumoniae pn ⫹ ⫹ ⫺ ⫺ ⫺ v ⫺ ⫺ ⫹ ⫺ v ⫺ ⫺ Human S. (56) identified Coykendall and Gustafson (38) and Knight and Shlaes (84) as seven different DNA groups in their study. respectively. S. 84). gallolyticus. koalas. Lancefield group antigen. whole-cell protein. human (R. BE. be identified. DNA group 2 (56) and proposed that these strains be serum or a slide agglutination test (95) or typing serum (120). dogs. man isolates of S. the same species. pneumococcal typing antiserum or Omni serum. DNA reassociation experiments showed that these hu- investigators examined a collection of strains. have human strains called S. S. bile solubility. Pyr. pasteurianus. pneu. pneumoniae in Osawa et al. infantarius subsp. bovis II/1 were a major part of the DNA group. bovis biotype I and biotype II (the latter is some. pasteurianus (S. analysis. Isolation and identification of S. human genera a Abbreviations: pn. bovis I) D ⫺ ⫺ ⫹ ⫺ ⫺ ⫹ ⫹ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹ Human. gallolyticus. nomenclature of these species is confusing and subject to de.. i. identified as S. Recent molecular bovis I and II/2 joined the S. infantarius and S. These investigators reported that the S. Sbl. The majority of strains in these described type strains of S.S. identification can be accomplished by determining sus. tion. 126). These suggestions were based on a combination of closely related to the reference type strains of the S. The importance of this change in nomenclature can species (38. Esc. mitis group. human infections in their studies. (114) and children (18) are encouraging for control of pneu.620 FACKLAM CLIN. bovis II/1 mococcal infections. Tre. S. koala bovine S. bile-esculin reaction. groups based on phenotypic characteristics determined in the Ruoff et al. and other animals belonged to the Farrow moniae is identified by a serologic technique such as omni et al. infan- are referred to throughout this section.5% NaCl broth. S. DNA homology. DNA-DNA reassociation experiments have clarified the Recently. acidification of mannitol. infantarius (S. equinus (S. refractory. Farrow et al. lutetiensis D(v) ⫺ ⫺ ⫹ ⫺ ⫺ ⫹ ⫹ ⫺ ⫺ ⫺ ⫺ v ⫺ S. pyrrolidonylarylamidase reaction. Other investigators tarius. performed DNA reassociation studies on human isolates Even more recently Poyart et al. The cultures described by DNA group.2 be renamed S. but the S. production of extracellular polysaccharide. (104) showed that S. Rapid Strep system. pneu. infantarius. bovis II/2. Ideally. These two groups were called S. bovis. bovis II/1) D(v) ⫺ ⫺ ⫺ ⫺ ⫺ v ⫹ ⫺ ⫹ ⫺ ⫺ ⫹ ⫺ Human. The human isolates of S. melibiose. such as PCR tests for targeted proteins. reaffirmed these studies using 16S rRNA probes Table 3 lists the streptococcal species included in this sec. reassociation studies. bovine S. gallolyticus (S. and S. which correlates with DNA reassociation studies. bovine S. Voges-Proskauer reaction. REV. S. ceptibility to optochin and/or bile solubility. and penicillin binding protein genes (9. pneumo. G. equinus were a single studies were isolated from humans. Man. bovis-S. C. and further suggested that two subspecies S. Strains of S. S. TABLE 3. and trehalose broths. Farrow et al. The reasons for the changes listed in Table 3 for the S.2) D ⫺ ⫺ ⫹ ⫺ ⫺ ⫹ ⫹ ⫺ ⫹ ⫺ ⫹ ⫺ ⫺ S. coli be named S. Dx. (56). See footnote in Table 2 for positive and negative reactions. infantarius subsp. S. (107) described yet another species. F. Mel. All the human isolates of S. letters. bovis and S. bovis II. have suggested that the strains termed S. bovis niques are far from perfect and identification of some strains is I strains by DNA reassociation studies. suis from viridans streptococci is by serologic typing. Opt. bovis be translated back to the association of colonic cancer and the biotype II isolates of human origin could be divided into two isolation of S. Vp. bovis I and II from used. bovis variant) and discovered that nei. Na. and sequencing of the equinus DNA group to be included in the newly described sodA gene. sorbitol. These Under most circumstances. strains identified as S. coli could bate. suisb Type 1–35 ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫺ Swine. called S. bovis II/1 are distributed in both subspecies. These experiments were done primarily by whole-cell protein Streptococcus bovis Group: S. bovis I and II/2 were suggested to be officially identified as S. equinus. The investigators also reported that the hu- moniae is still problematic since conventional culture tech. S. most of which man isolates were unique and corresponded to DNA group 4 were nonhuman isolates. BS. These group. bovis from blood cultures of these patients. (56). bovis) D ⫺ ⫺ ⫹ ⫺ ⫺ ⫹ ⫹ ⫺ ⫺ ⫺ v ⫺ ⫺ Equine. Schlegel et al. bovis-S. and reported that the phenotypically described by Farrow et al. b Note that the only way to differentiate S. if serologic techniques are not investigators also included isolates of S. ⫺ ⫺ ⫺ ⫺ ⫺ v v v v v v v v Human none Other streptococci and Unknown ⫺ ⫺ v v v v v v v v v v v Animal. growth in 6. hyrolysis of esculin. These strains were closely related to the S. hydrolysis of starch. lutetiensis Nelms et al. These DNA groups S. Identification of non-beta-hemolytic gram-positive cocci in chainsa Species or group Antigen Opt BS BE Na Pyr Esc Vp Man Mel Sbl Tre St Dx Origin S.T) Viridans streptococci A. bovis I was more commonly . gallolyticus based on gallate-degrading capacity. Phenotypic physiologic tests place S. infantarius. equinus group described by cases of pneumonia and identification of strains. (93). cows. St. taxonomic classification of this group of streptococci.

pasteurianus are isolated from blood cultures of patients with tions in pigs. gallolyticus and isolated from humans may be identical to those causing infec- S. this system. 97. S. the corrected epithets of several species are given according to the three different RAPD types were identified. 99. Some have Difficulties with the Lancefield extraction procedure. Type 2 S. Trottier et al. 45. agree with this grouping of streptococcal species. By this procedure. 107). There were 39 hemolysis-like reaction (described as alpha-hemolysis. suis in North America. Phenotypically. most individual species cannot not be identified biologists is that the only serotype identified from humans has but are placed in one of the six groupings. hyointestinalis in the pyogenic group and is the reference procedure used for demonstrating group an. alactolyticus in the S. (92) reviewed the literature and summarized organisms because many of the species do not express the 44 cases of human infections caused by S. none of the not truly represent the origin of all the species. because cultures sult in identification of S. notypic characteristics (discussed below). and dairy product first case of infection cased by S. tion of those in the salivarius group. These characteristics are leucine amin- on blood agar plates containing sheep blood (68). which contained devise a three-tier testing system for the definitive species iden- . some of them cases were from the United States. In addition. suis is found in infections among pigs in the colonic cancer more often than is S. and endocarditis. gordonii. all strains of this species are alpha-hemolytic when grown cocci listed in Table 3. and T and several other serotypes of strains with the same phenotypic characteristics of typical viridans streptococci. These two species are included in reaction used to type S. cated that the group R and group D antigens were similar but Species not yet identified from human sources are included not identical and the observed reactions were judged as cross. suis including 8 isolates of human origin.VOL. At this time. 140). Note that with and group S is type 1. the strains This translates into correct terminology that S. Bruckner and Colonna listed 15 different strepto- mally called Lancefield groups R. However. sources (S. In 1997. Statens Serum Institute in Copenhagen. S. S. Interested investigators will need to human strains were placed in RAPD type 1. streptococci” may not be the best to describe this group of Lutticken et al. later reports indi. 2002 TAXONOMIC CHANGES IN THE STREPTOCOCCI 621 associated with colonic cancer patients than was S. It is will depend on whether clinical microbiologists adopt proce. 1. and S. (24). Not all investigators been type 2 (group R). human infections. infantarius or S. Table 4 includes 26 streptococcal species that have the R. reported the originate from gastrointestinal. The important change to clinical micro. bovis are frequently found in blood antisera and group R antiserum can be obtained from the cultures of patients with bacteremia. A modified Lancefield the category termed “other streptococci” because of their phe- extraction may be used to identify type 2 by using group R. Chateillier et al. suis. 26 cultures isolated from pigs. all the species listed in Table 4 have the and produce a hemolysin on agar plates containing horse blood phenotypic characteristics described for the viridans strepto- agar. Other tion that a capsular reaction be used (66) for identification of investigators have included S. uberis in the various serotypes. parasanguinis and therefore may be misidentified. pyrrolidonylarylamidase negative. suis is the name assigned to streptococci that were for. vaginal. equinus group based on se- tigens in all other streptococci. (25) performed random reviews that summarize the molecular experiments that define the amplification polymorphic DNA (RAPD) analysis of 88 strains majority of viridans streptococcal species (37. suis) to humans has caused tional serotypes of this species (64) led to a change in the documented infections and there is no reason to believe that nomenclature of how the capsular types were identified. are bile-esculin negative. six phenotypic characteristics listed in Table 4. Twenty. 96. The discovery of addi.5% NaCl broth. Many investigators refer to gitis. the most common strain identified. quence data of the 16S rDNA gene (76) and Fig. Five of the eight rules of nomenclature (129). acidominimus and S. iniae. with the excep- streptococcal group D antigen. Care- lications just cited (38. Kilpper-Balz and coccal species that were included in the viridans streptococci Schleifer (81) determined that the strains representing group. There any of the species listed in Table 4 will not be isolated from are now 35 different antigenic carbohydrate types of the spe. sepsis. S. however. this sources. which preferred to group S. S. and S. S. bles the viridans streptococcal species S. 93. bovis-S. 84. lutetiensis. is type 2. and no also included results that some strains of this species contained growth in 6. The term “viridans precipitating antiserum (64). Early reports opeptide positive. Hope. which addition to being catalase-negative. Streptococcus suis Viridans Streptococci S. patients is unknown. Why no infections caused by this organism Whether this terminology is accepted in the medical literature have been documented among U. and T. 56. The 26 species are arranged according to the cies. because transmission of streptococcal species from nonhuman reactions in the group D antiserum. gram-positive cocci ar- they called S. suis cultures isolated from humans and pigs characteristic described in Tables 3 and 4. Nearly all species. Although some strains are beta-hemolytic ranged in chains. There are two excellent can be very similar. suis in the United States. suis resem- published criteria. cussed above) on blood agar plates. pneumoniae. possible that laboratories may not have the microbiological dures that accurately identify each of the new species with the capacity to identify the isolates. porcinus. have led to the recommenda. Denmark. Typing previously identified as S. it is proposed that the term “viridans strep- was a case of human endocarditis from a Canadian patient tococci” be used to include streptococcal species with phenotypic (128). S. ful microbiological examination of alpha-hemolytic viridans fully. 15. suis. of type 2 S. as dis- cases of meningitis and 5 cases of septicemia without menin. this designation does with raw pork meat or having contact with pigs. bovis II/1. This reaction is similar to the quellung the viridans category (12). All cases were associated with the patient having worked them as the oral streptococci. In phenotypic characteristics were a single DNA group. additional studies will be undertaken to verify these streptococci isolated from human cerebrospinal fluid may re- changes in the nomenclature of this group. sanguinis.S. United States (25). Group R. The information in Table 3 was summarized from the pub.

mutans ⫺ ⫹ ⫹ ⫹ ⫹ ⫺ Human S. and Whiley and Beighton (140) give an excellant review of the the third level needs to be similar to that described in Table 2 for species origin included in the S. vestibularius ⫺ v v ⫺ ⫺ ⫹ Human S. ⫹. macaccae ⫺ ⫹ ⫹ ⫹ ⫹ ⫺ Monkey S. infantarius ⫺ v ⫹ ⫺ ⫺ ⫺ Human S. Arg. alactolyticus ⫺ ⫹ ⫹ ⫺ ⫺ ⫺ Swine. 4. ferus ⫺ ⫹ ⫹ ⫹ ⫹ ⫺ Rat S. 105). In a previous study. tagatose. Identification of Abiotrophia and Granulicatella speciesa Species Pul Suc Tag Tre Hip Arg ␣-Gal ␤-Glu ␤-Gal Origin Abiotrophia defectiva ⫹ ⫹ v ⫹ ⫺ ⫺ ⫹ ⫺ ⫹ Human Granulicatella adiacens ⫺ ⫹ ⫹ ⫺ ⫺ ⫺ ⫺ ⫹ ⫺ Human Granulicatella para-adiacens ⫺ ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ Human Granulicatella balaenoptera ⫹ ⫺ ⫺ ⫹ ⫺ ⫹ ⫺ ⫺ ⫺ Whale Granulicatella elegans ⫺ ⫹ ⫺ ⫺ ⫹ ⫹ ⫺ ⫺ ⫺ Human a All strains are positive for pyrrolidonylarylamidase and leucine aminopeptidase and sensitive to vancomycin. is negative. . ␤-gal. Tag. According to previous reports. human S. the viridans streptococcal species group. sobrinus. human S. growth in 6. avian S. mutans and S. All strains require pyridoxal for growth and satillite around staphylococcus culture on blood agar plates. parasangunis ⫹ v ⫺ ⫺ ⫺ ⫺ Human S. hyovaginalis ⫺ ⫺ ⫹ ⫹ ⫹ ⫺ Swine Salivarius group S. MICROBIOL. All the 4). gordonii ⫹ ⫹ ⫺ ⫺ v ⫺ Human Mitis group S. cricetus ⫺ ⫹ ⫹ ⫹ ⫹ ⫺ Rat. variable reactions (16 to 84% positive). respectively. 3. Abbreviations: Pul. salivarius ⫺ ⫹ ⫹ ⫺ ⫺ v Human S. infantis ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ Human S. review were obtained from conventional tests. mutans group with the excep- the S. hyointestinalis ⫺ ⫺ ⫹ ⫺ ⫺ ⫺ Swine S. anginosus species group. ␣-gal. oralis ⫺ v ⫺ ⫺ ⫺ ⫺ Human S. No reaction on bile-esculin medium. A table similar to Table 2 using tion of S. sanguinus ⫹ ⫹ ⫺ ⫺ v ⫺ Human S. a few for differentiation of S. downei ⫺ ⫺ ⫹ ⫹ ⫹ ⫺ Monkey S. we found that 88% of blood TABLE 5. REV. sobrinus reports. intermedius ⫹ ⫹ ⫹ ⫺ ⫺ ⫺ Human Sanguinus group S.5% NaCl. production of ␤-galactosidase. Tre. production of ␣-galactosidase. v. 15% or fewer of the strains positive. deamination of arginine. (102. ⫺. S. tification. hyovaginalis.622 FACKLAM CLIN. and they show negative reactions for gas production in MRS broth. cricetus and S. orisratti ⫺ ⫹ ⫺ ⫺ ⫺ ⫺ Rat a See Table 2 for definition of positive and negative reactions. the Streptococcus mutans Group viridans streptococci group. This species is included in the mutans chromogenic substrates should be constructed for each viridans grouping because of similar phenotypic characteristics (Table species group to identify definitive species (102. however. or at 10 and 45°C. sobrinus included the additional species were described after the publication of their fermentation of melibiose. TABLE 4. mutans is positive and S. constellatus ⫹ ⫹ ⫹ ⫺ ⫺ ⫺ Human S. perois ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ Human S. the most common species phenotypic characteristics listed in Tables 1. The first determination is described in Table 3. Hip. ␤-glu. sorbinus ⫺ ⫹ ⫹ ⫹ ⫹ ⫺ Human. ratti are rarely iso- papers by Whiley and Beighton (140) and Ruoff et al. The tables in the mutans and S. acid production from pullulan. 85% or more of the strains positive. and 5 in this isolated from human sources (primarily the oral cavity) are S. rat S. S. Suc. production of ␤-glucuronidase. and trehalose broth. cristatus ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ Human S. anginosus ⫹ ⫹ ⫹ ⫺ ⫺ ⫺ Human S. mitis ⫺ ⫺ ⫺ ⫺ v ⫺ Human S. ratti ⫹ ⫹ ⫹ ⫹ ⫹ ⫺ Rat. sucrose. thermophilus ⫺ ⫺ ⫹ ⫺ ⫺ ⫺ Dairy product Anginosus group S. Identification of major groups of viridans Streptococcus speciesa Group and species Arginine Esculin Vogas-Proskauer Mannitol Sorbitol Urea Origin Mutans group S. 105) lated (11). the second determination is de- scribed in Table 4. hydrolysis of hippurate. The identification scheme devised by these authors include most of the species listed in Table 4.

mitior.VOL. some investigators have preferred to ar- isolated from the genital tracts of female swine and appear to range the viridans Streptococcus species differently from the be part of the normal flora. some have included the has not been documented. Anti. S. and there- species status (42). salivarius. Several strains of this species were As stated above. Streptococcus anginosus Group infantis have all been isolated from the human oral cavity. salivarius group. Beighton mined that these strains deserved full species status (109). as S. Table 4. S. but the dif- hemolytic streptococci. and alkaline phosphatase reactions (79). in 1997 (43). parasanguinis. positive for all strains of S. parasanguinis from S. crista. have been added to the S. S. mitis was determined to be proposed that S. 1. Fig. S. parasanguinis was split from the S. sanguinis and S. infantarius strains are bile-esculin and esculin negative. gordonii was split from the S. The Streptococcus grouping antisera ferentiation was based on percent positive reactions in 14 dif- are made for testing beta-hemolytic strains. et al. and phenotypic characteristics Streptococcus salivarius Group (140). S. vestibularius. S. DNA-DNA reassociation studies The biotype describes strains with certain phenotypic charac- demonstrated that this organism was unique and deserved teristics but does not have official taxonomic status. salivarius. peroris. According to the phenotypic characteristics listed in The S. S. bovis II/1 can be either S. Some strains of each of the species species. two more species. managing patients. formally called S. anginosus group have been more recently. bovis group. Although there are many similarities between the two investigators (56. S. exceptions. infantarius has been isolated from human infections (107). infantarius is listed in both the Streptococcus mitis Group S. the type strain for S. 2002 TAXONOMIC CHANGES IN THE STREPTOCOCCI 623 culture isolates (48 of 54) were melibiose positive. S. S. genic homology between strains of Enterococcus faecalis and gordonii but not by S. sanguinis and S. which The S. “S. thermophilus should be a subspecies of S. However. Salivarius group with streptococcal group D these species. infantis. conducted DNA-DNA re. gallolyticus group by both 16S rRNA gene their reactions in the arginine and esculin tests. 82) and S. sanguinis. bovis species names such as Streptococcus viridans and S. which indi. peroris and S. S. the S. sanguis) fections are S. For example. S. mitis group (77). antigen. The hence has some characteristics of both the S. In addi- been in question for several years. as S. S. Streptococcus sanguinis Group (Formerly Known cates that the majority of isolates from human noncaries in. ing 10 chromogenic tests) to differentiate the S. sanguis biotype II” is a common designation (50). thermophilus has fore no “type” strains are usually available for study. S. Streptococcus orisratti (151) has been added to discussed in the section describing beta-hemolytic streptococ. and its association with human infections has not been infections. inappropriate based on molecular experiments. These strains are misidentified as S. oralis. salivarius from patients with subacute bacterial endocarditis. cristatus (65). mitis. alactolyticus is included in the “S. As discussed above.” For testinalis isolated from the swine gut. association experiments under stringent conditions and deter. hyoin. D grouping antiserum. mutans (49). Even The species included in the S. mitis groups together based on 16S rRNA sequence analysis (76). Another species will establish their role in human infections. and such sera are ferent tests. sanguinis and negative for all strains molytic. II/1 by the Rapid Strep system. bovis group and the S. 15. mitis grouping (143) and possess the group D antigen. S. salivarius group react with streptococcal group protease. sanguinis and S. and some investigators tion. amygdalin. therefore. One of the problems has been the use of invalid reassociation studies. added to the complexity of the S. vestibularius was identified from the human oral cavity redefined viridans streptococcal species with specific human (146). Of the species listed in the viridans streptococcal type infections. infantarius by DNA-DNA onomists. however. bovis” group by some (79). which would seem to indicate that they S. inulin fermentation was the only test that was evaluated only with preparations of strains that are beta-he. cristatus. mitis group of viridans streptococci has caused con- excludes them from the S. lutetiensis. Accurate identification of these four there are no official reference strains which to study. mitis group. and S. to assess the association of any of the newly described and 103). presented a reasonable scheme based on 23 tests (includ- Data from the references noted in this section should be com. These bile-esculin. was originally identified example. There are analysis (140) and phenotypic characteristics (Tables 3 and 4). the most frequently identified viridans Streptococcus species and S. The authors described characteristics that helped serum is rarely if ever tested for cross-reactions with non-beta. hyovaginalis was described by Devriese et al. these two groups can be separated for the most part by bovis-S. confirmed. and this phenotypic characteristic can be used to iden- . The addition salivarius. Since then. only strains of S. sanguinis and piled to form a identification scheme for species identification. salivarius group because some S. salivarius group of bacteria is closely related to the S. sanguinis species S. oralis (21. to differentiate S. Formation of the extracellular polysaccha- that cross-react with non-beta-hemolytic streptococci. The taxonomic status of S. Schleifer et al. of S. equinus-S. problem with streptococcal group D antiserum is that this mitis groups. siderable confusion for both clinical microbiologists and tax- negative strains were identified as S. sanguinis is probably S. Identification from human sources classification listed here. S. parasanguinis also helps to differentiate members of the S. mitis groups recognized in 1991 (10). All three of these species are commonly found in antiserum has not been published. group D antiserum may contain antibodies of S. mitis group. It is difficult is commonly identified from a variety of human infections (38. Additional confusion will result Although these names may convey a meaning to physicians in light of the latest findings that S. problem has been the use of the terminology “biotypes. S. orisratti possesses Lancefield’s group A cal species. infantarius have been isolated from humans. This may not be the case. 130). they can be differentiated by immunoglobulin A1 IgA1 listed in the S. ride dextran on 5% sucrose agar by both S. they are troublesome to taxonomists in that infantarius or S.

S. The question is whether knowledge of the taxo- 13 different species in the database were correctly identified nomic identity of infecting bacteria is useful for predicting the and 56% of 15 strains of 6 species not in the database were antimicrobial susceptibility of the organism. DNA-DNA reasociation procedures at to predict potential susceptibility problems related to specific this time are not applicable for most clinical laboratories. 99). mitis was the leave much room for sequence variability that occurs in many most common species group identified and the most likely to strains. mitis grouping. a result of “unidentified” would be of gram-positive cocci. however. S. tify this species once it is determined that the strain in question length polymorphism (tDNA-PCR). One other generality can be made with the S. (78). Ruoff et al. (98. in the last two editions of the Manual of methods (2). cies are a single species. Tracy et al. sanguinis. It is not yet pos. S. Although not all these investigators used identification (101) used restriction fragment polymorphism of rRNA ri. This mon strains isolated from cultures of blood of endocarditis is in contrast to the results obtained by most other authors patients (46). wais. In view of the incorrectly identified using the Rapid ID 32 Strep system (bio. antimicrobial resis- standardized procedure. The most successful molecular human infections. be used to identify the viridans streptococcal species known at that time (102. oralis strains are the (Fig. These investigators used different detection systems. Resistance to ␤-lactam antimicrobial was reaction technology with specific primers. 16S species. Two investigations (127) used 16S rRNA sequencing to identify the species of the have been reported examining the tDNA intergenic spacer S. they were unable to differ. some generalities can be made regarding rRNA gene-sequencing procedures have been used to show susceptibilities and species. However. These tables included conventional tests Antimicrobial Susceptibilities of Viridans as well as a series of fluorogenic substrates that had to be Streptococcal Species prepared in house because they were not available from com- mercial medium sources. using this technique but would seem to point to a need for a sanguinis group as in the S. and 33% in strains from Latin America (97). (60) targeted the D. procedures that would allow identification to the species level botyping for six species and found that 91% of 53 isolates were according to today’s standards. has phenotypic characteristics consistent with the S. group. DNA-DNA reassociation and sodA sequenc. (132) did not get correlation between oralis. S. it is difficult to say exactly if it is possible correct. so that the identi. field gel electrophoresis (149). these procedures are not useful for the identifi- Clinical Microbiology included identifications tables that could cation of specific species. as opposed to the situation for 16S rRNA such as those used at CDC does not differentiate most species. Penicillin ever. In addition. gallolyticus (99). Garnier et al. gallolyticus be resistant. tions but most significantly from patients with subacute bacte- fications generated by those systems are compromised. multiple changes in taxonomy and nomenclature of this group Mérieux). gordonii. Commercially available systems do Viridans streptococci are isolated from a variety of infec- not have all the species in their databases. ther report indicated a completely successful result in differ- sible to correlate the new and revised species in this group with entiating all species tested. most common found in blood cultures of cancer patients and ing studies indicate that the type strains representing the spe. Whole-cell protein analysis is would be in the S. are the most com- their whole-cell protein profiles and species identification. are commonly resistant to ␤-lactam antimicrobials (3.624 FACKLAM CLIN. 1). 46. 87% of 156 strains of management. 73. in descending order. with different results (4. mitis 40). nei- the S. rRNA genes for the types strains of S. date is that reported for examining the sequence of the gene encoding the manganese-dependent superoxide dismutase (sodA int) (98. Probably the best one could hope for was these two instances. oralis. and various other PCR-based plished. mitis group. strict criteria for determining species have not been es. For example. This does not this study were not adequately identified. antimicrobial resistance relationships between many of the streptococcal species. gene sequencing. pneumoniae were clearly differentiated by cal species? It is apparent that the use of conventional tests sodA sequencing. how. What are the options for identifying the viridans streptococ. pulsed- successful differentiation of species has not been accom. Devising a scheme for identification of all six species in which may explain the differences in the results. First of all. mitis and S. The species distribution is thought to correlate very well with DNA-DNA reassociation. mitis group will take additional work. macedonicus. mitis. but S. Although the incidence is not as high in the S. In the latter case. but Vandamme et al. anginosus group of species. somewhat different in endocarditis patients. knowledge of the antimicrobial suscepti- reported by Kikuchi et al. at least rial endocarditis and from neutropenic patients with cancer. the identification certainly reported as one of three species. In to some extent. resistance in the viridans streptococci is as high as 48% in tablished. 45% in strains from Canada. found in 17% of the strains (91). More recently. S. mitis. the sequence identities of the 16S strains from the United States. tance is present. entiate the S. MICROBIOL. Whether any of the newly described species technique reported to identify viridans streptococcal species to are associated with human infections is unknown. When DNA homology studies bility of the infecting organisms is useful for good patient were used to confirm the identifications. REV. and S. Other studies with better identification proce- appear to be separate species based on 16S rRNA sequences dures have indicated that S. Although other technologies that may be Nearly 40 conventional tests have been used to test all the type used to study strain-to-strain relationships for epidemiologic strains as well as other reference strains of each species. applied PCR anginosus group. S. and studies include electrophoretic isoenzyme typing (62). anginosus group and found no difference in antimicrobial . however. Poyart et al. but resistance to macrolides was identified the six species. S. Specific species in pneumoniae are greater than 99% similar (76). Rudney and Larson 123). and S. is substantial in the viridans streptococci as a group. S. 99) reported differentiation Options for Identification of Viridans Streptococcal Species of 29 streptococcal species including 16 viridans species. alanine–D-Alanine ligases of six viridans species. 105). Unfortunately. oralis. and S. and S. and successfully only at the intermediate level. However.

Patients with endocarditis due reactions listed in Table 6 are those obtained from Devriese et to NVS are more difficult to treat than those infected with al. NaCl. respond to antimicrobial therapy. NVS overall is reported to cause approx. A. S. These reports finding. 75. 15. elegans in this new genus while been isolated from human infections. elegans strains among 45 endo. we have recently revised that imately 5% of all cases of endocarditis (22). The species in Table 6 have at least one reaction Streptococcus adjacens and Streptococcus defectivus (19). There appears to be antimicrobial susceptibility differences in The last group of Streptococcus species and related genera some of the other species within these groups. parauberis. balaenopterae. described better phenotypic criteria for identification (44). different from this pattern. because all been described as satelliting. VP. anginosus. examined the reference strains. other animals S. leucine aminopeptidase. Collins and Lawson malium. growth in 6. adiacens. 39. BE. vitamin B viridans streptococci are leucine aminopeptidase positive and 6-dependent. none of these six species has cens. the last species- ABIOTROPHIA AND GRANULICATELLA SPECIES group listed is “other streptococci and genera. 43 were A. Note that in Table 3. pyrrolidonylarylamidase. A. uberis/parauberis ⫹ ⫹ ⫹ ⫺ ⫹ v v ⫹ ⫹ ⫹ Bovine S. 89. 55 were G. elegans (98). acido- indicate that all the species except G. adiacens. Hip. Esc. Devriese et al. susceptibilities of the three species (S. elegans. 44). of reactions listed for the species S. See Table 2 for definition of positive and negative reactions. adia. S. and finally nutrition- pyrrolidonylarylamylase-negative and do not grow in 6. The majority been added to the Abiotrophia genus. balaenopterae have been minimus are now identified as Facklamia sourekii (86). bal. Recently. urinalis ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫺ ⫺ ⫺ Human Dolosicocccus paucivorans ⫺ ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ Human Facklamia species ⫹ ⫹ ⫹ ⫺ v v ⫺ v ⫺ v Human Ignavigranuum ⫹ ⫹ ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ Human Globicatella sanguinus ⫺ v ⫹ ⫹ ⫹ ⫺ ⫺ ⫹ ⫹ v Human a Abbreviations: LAP. para-adiacens (74). and combination therapy is tus. and A. defectiva remains in the Abiotrophia genus (35). intermedius). consists of bacterial strains that do not fit into any of the species or species groups discussed above. (42–44) and our testing of the current type strain for the viridans streptococci. Note the corrected epithets. pluranimalium ⫹ ⫺ ⫹ ⫹ ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ Bovine. Recently. bovis and S. 42. Al- cens. 2002 TAXONOMIC CHANGES IN THE STREPTOCOCCI 625 TABLE 6. Table 5 includes all the species of “NVS” Streptococcus acidominimis and an identification scheme based on the published reports (35. 13 G. In addition. The human isolates previously identified as S. which eliminates them from the NUTRITIONALLY VARIANT STREPTOCOCCI. PYR. thoraltensis ⫹ ⫺ ⫹ ⫹ ⫹ ⫹ ⫹ v ⫹ ⫹ Swine S. and 8 G. demonstrated that the two NVS species were optochin resistant (eliminating the pneumococci) and do not phylogenetically distant from the streptococci and proposed have defined group antigens (eliminating the S. para-adia. Other authors using slightly different species firmly established the correct type strain for the species. esculin hydrolysis. fied from humans in 1977 (50). Whether the same can be GRAM-POSITIVE COCCI IN CHAINS said for the other viridans groups remains to be established. 74. Identification of unusual Streptococcus species and other genera of gram-positive cocci in chainsa Species LAP PYR NaCl BE Esc Arg VP Hip Man Sbl Origin S.5% ally variant streptococci (NVS) before being reclassified as NaCl broth. that they be given new genus status. three new species have in Table 6 are a guide for potential identification. thoraltensis. that it was unnecessary to identify the infecting organism to the species level and that identification to the “milleri group” was UNUSUAL STREPTOCOCCUS SPECIES AND OTHER sufficient for patient management. urinalis further proposed that some of the Abiotrophia species were were taken from published materials (13. At this time. pyridoxal-dependent. The isolated from human infections. 9 A. The identifications based on the reactions listed Abiotrophia defectivus (75). Arg. defectiva. and S.” The species The nutritional variant group of gram-positive bacteria has listed in Table 6 are not viridans streptococci.VOL. acidominimis ⫹ ⫹ ⫺ ⫺ ⫹ ⫺ ⫺ ⫺ ⫹ ⫺ Food S. These authors expressed the opinion often recommended (22). acidominimus was identi- carditis patients (74). deamination of arginine. in our laboratory. and G. 100) and our own results examining 100 strains The type strains of S. acidominimus. only the type strain for each species has been tested establishment of the genus Granulicatella to include G. and 3 1922. S. and identification criteria found 15 G. S. constella. we have not confirmed any human iso- . cell wall-deficient (L-form). Our scribed. Voges-Proskauer reaction. uberis. bile-esculin reaction. Man and Sbl. species listed in Table 1. though it had been reported that S. and most reference strains have not had the pheno- results indicate that of 101 isolates from 97 patients (58 with typic characteristics of the original description of the species in endocarditis). In phylogenetically distinct from each other and proposed the most cases. A. hydrolysis of hippurate. acid production in mannitol and sorbitol broths. Abiotrophia adjacens and suis groups). These species are bile insoluble and Kawamura et al. and S. plurani- aenopterae (89). S. G. acidominimis have been poorly de- of NVS taken from the CDC stock culture collection (26).5% NaCl broth. defectiva. were G. 43. None of these strains are beta-hemolytic. As many as 41% of patients may fail to species.

entericus (134). and macrolide antimicrobials (85). and the bile-esculin test (S. All but F. sanguinis. uberis. urinalis has species have been described that have not yet been tested in been identified. In a recent study of 28 strains of G. S. Cultures of this species were recovered tion of cultures from human sources identified as Streptococcus from the intestinal tracts of swine. but very little clinical information was provided with collections were reidentified as S. isolates have been confirmed. uberis or S. anginosus group by both phenotypic and genetic Dolosicoccus paucivorans tests. acidominimus. as opposed to chains (G. MICROBIOL. G. F. acidominimus when using the revised identification Facklamia species and Ignavigranum ruoffiae criteria. a second isolate of S. No human Identification of the species has been recently reviewed (51). F. sepsis. and in fact from human infections. perhaps fits into the S. pluranimalium was described by Devriese glyolate broth (86). and F. all of which appear to fall single strain isolated from a case of human cystitis (31). urinalis swabs of sheep. mitis group. gallinaceus (31). Two additional cultures have been isolated from blood phenotypically resembles species in the S. acidominimus in culture cultures. sourekii. thoraltensis was also described by G. uberis previously reported from humans (50) have been be an important pathogen in humans. ovis (33). S. sanguinis). identified using the phenotypic tests listed in Table 6. sinensis (150) appears to fit into the S. samples. F. Phenotypically. isolated from chickens (34). They were called S. S. cristatus. and the because the cultures are mannitol positive. F. Yet another recently isolated from a culture of blood from a patient with pneumonia described species. sanguinis is differentiated from S. An exact position of any of these new species entiate this bacterium from the viridans streptococci (Table 6). australis was isolated Table 6. anginosus group. and canary lung and lesions (44). The appear. Streptococcus thoraltensis Globicatella sanguinis The new species S. F. plurani- the isolates (85). sanguinis. Most isolates have been from blood some of the reference strains of S. The two species S. uberis and S. phenotypi- D. 20 have been developed for identification of both species (13). the cellular arrangement of A. cannot be determined until they are tested with conventional . tabacinasalis have been isolated et al. parauberis from tract infections were associated with three urine culture iso- human infections has not been documented. pluranimalium. Species-specific probes is positive). Streptococcus uberis and Streptococcus parauberis viridans in the Gram stain is in pairs and clusters. mutans group. but the positive pyrrolidonylarylamidase Phenotypic tests indicate that this species is closely related to and negative leucine aminopeptidase reactions clearly differ. isolates should be confirmed as not being enterococci from the human oral cavity. uberis is positive) Table 6 because differentiation of the two species by conven. australis (148) appears to fit formation. ignova. hominis. peptidase negative and pyrrolidonylarylamidase positive and hydrolyze hippurate. One patient had a diagnosis of pneumonia. lan- Streptococcus pluranimalium guida is described as not forming chains. other members of this group. Presumptive identifi- phenotypic similarities. sanguinis (sanguis) was described in 1992 from a collec- Devriese et al. cervix. into the S. bovine vagina. All the isolates of lates (117). S. a trait rarely ob- other report did not include clinical information. urinalis was made on the basis of a Five new Streptococcus species. urinalis is similar to S. S. S. The strains resembled S. S. However. they may be identified fairly ance of dolosicocci on blood agar plates is similar to that of the easily. hominis. tive identification of the Facklamia and Ignavigranum genera. and because it deaminates arginine. viridans streptococci. Identification of this species uberis-like (28). but G. (44). S. served in the S. F. and tonsils. Streptococcus urinalis New Species Not Yet Tested The description of S. sanguinis tional phenotypic tests is not possible. in our hands some chains are apparent in Gram stains prepared from thio- The new species S. and one Facklamia the publication of that report. sanguinis can be reidentified as Globicatella sanguinis (see below). tabacinasalis. however. S. G. REV. ovis is has overlapping phenotypic characteristics with the entero. paucivorans was initially described based on one organism cally fits roughly into the S. miroungae (69) was isolated from an elephant seal. Confirmation of isolation S. S. Presumptive identification can Some strains exhibit decreased susceptibilies to the ␤-lactam be made on the basis of the reactions listed in Table 6. isolated from vaginal by use of the GenProbe Enterococcus probe because S. parauberis are placed in uberis by the leucine aminopeptidase test (S. our conventional test system. languida. (43). Urinary (13). and enterococci. Five species of Facklamia have been described. mitis grouping. F. and endocarditis. lates of S. uberis is negative. were isolated from cultures of blood from patients with diag- uberis can be found in up to 20% of cases of bovine mastitis noses including bacteremia. Since into the viridans Streptococcus grouping. In addition to the tests described in it most closely resembes S. S. uberis-like because of from humans has not been documented. a blood culture isolate with no additional in. sinensis was isolated from a human with endocarditis. Table 6 lists the tests necessary for presump- malium has been isolated from bovine mastitis. reported to form acid in mannitol and sorbitol broths like the cocci.626 FACKLAM CLIN. Isolates of this species are also similar cation can be made by matching reactions with those listed in to Aerococcus viridans in that both species are leucine amino- Table 6. G. These data seem to indicate that this species may S. anginosus group. isolated from cattle intestines.

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