Taxed by Taxonomy? The Curious Case of the Organism Previously Known as Streptococcus bovis
Abstract & Commentary
By Ellen Jo Baron, MD, PhD, Professor of Pathology and Medicine, Stanford University; Medical School Director, Clinical Microbiology Laboratory, Stanford University Medical Center, is Associate Editor for Infectious Disease Alert.
Dr. Baron reports no financial relationships relevant to this field of study.
Synopsis: Modern taxonomy has delineated Streptococcus gallolyticus subsp. gallolyticus, S. gallolyticus subsp. pasteurianus, Streptococcus infantarius subsp. coli, and S. infantarius subsp. infantarius within the heterogeneous group of previously designated clinical Streptococcus bovis bacteria. It is recommended that both clinical microbiologists and infectious disease specialists avoid the designation S. bovis for true S. gallolyticus and S. infantarius strains in the future in order to get a clearer picture of the possible disease associations of these species.
Source: Beck M, et al. Comprehensive study of strains previously designated Streptococcus bovis consecutively isolated from human blood cultures and emended description of Streptococcus gallolyticus and Streptococcus infantarius subsp. coli. J Clin Microbiol. 2008;46:2966-2972.
Microbiologists have traditionally taken extra steps to identify non-hemolytic streptococcus-like strains isolated from blood cultures primarily to identify Enterococcus species and rule out Streptococcus bovis. S. bovis is still often identified by its colony similarity to Enterococcus species and its similar ability to hydrolyze esculin in the presence of bile, but unlike Enterococcus species, it is unable to grow in 6.5% salt broth. Like enterococci, S. bovis possesses Lancefield antigen-group D, a lipoteichoic acid and the only non-carbohydrate Lancefield antigen. Microbiologists have also traditionally added a comment to blood culture isolates displaying the characteristics cited above, suggesting an association between isolation of S. bovis from blood cultures and a possible gastrointestinal tract malignancy.5 The bovis group received a short paragraph in the most recent (9th edition) version of the American Society for Microbiology Manual of Clinical Microbiology (ASM Manual).10 As it turns out, even the name Streptococcus bovis is no longer a valid name for any species of bacteria. The relatively new species names: equinus, gallolyticus, infantarius, and alactolyticus were mentioned in the 2007 ASM Manual, as was an association of S. gallolyticus ss. gallolyticus with gastrointestinal cancer and S. gallolyticus ss. pasteurianus with meningitis. Until recently, however, I would bet that virtually no microbiologists were clued in, and they continued blithely reporting all S. bovis family isolates as S. bovis. However, now that microbial taxonomists have zeroed in on this group, we have yet another new set of names and another new set of clinical associations to contend with.
Commentary
Recently, two clinicians contacted me about receiving reports of S. gallolyticus isolates from blood. I'm sorry to admit that they were not from our laboratory, which, it still seems, is in the medieval age of reporting S. bovis. The laboratories that did report the new species, probably because of the early adoption of a newly reformatted multi-well biochemical identification card for their automated identification/susceptibility testing instrument, did not note that the organism used to be called S. bovis. If they had reported it the old way, physicians would have assumed a link to GI malignancy, and both parties could have been wrong for different reasons.
A recent study of 58 S. bovis-like blood culture isolates gathered from a number of hospitals in Germany by Beck et al has delineated the current state of the genus using state of the art molecular taxonomic methods, i.e., by sequencing of the entire 16S rRNA gene.2 Dr. Guido Funke, from whose laboratory the study emanated, is a master taxonomist. For those clinicians who resent the microbiologists' penchant to change the names of organisms at the drop of a hat, this paper provides a strong argument for splitters rather than lumpers. Taxonomists clearly fall into the splitters. If we did not have splitters, we would never have realized that Staphylococcus lugdunensis was different from other coagulase-negative staphylococci, and we would not have the information needed to appropriately treat those strains more aggressively, as their enhanced virulence warrants, nor interpret appropriately the cefoxitin disk zones or MICs to detect methicillin resistance. Oxacillin, and the related antimicrobial agent susceptibility test results for S. lugdunensis are reported as if the isolate was Staphylococcus aureus, not a coagulase-negative Staphylococcus, which technically speaking, it is. Please read additional information about S. lugdunensis in a previous issue of Infectious Disease Alert.1
S. bovis were originally designated into biotypes based on biochemical differences: biotype I fermented mannitol, biotype II/1 failed to ferment mannitol or produce beta-glucuronidase, and biotype II/2 was also mannitol negative but beta-glucuronidase positive. Laboratories rarely differentiated them in such detail. Until 1989, it was not appreciated that S. bovis variants had any special clinical correlation. At that time, Ruoff et al reported on a study of 68 blood culture isolates, 30 S. salivarius and 38 S. bovis group.9 They found that S. bovis type I was associated with endocarditis (94%) and colon cancer (71%), compared with S. bovis II and S. salivarius (18% and 17%). The paper still had little impact on reporting formats of most clinical microbiology laboratories, who continued to identify S. bovis based on growth and hydrolysis of esculin on bile media and lack of growth in salt broth, although miniaturized biochemical and chromogenic enzyme multi-well systems were commercially available. In fact, Beck et al showed that even those two major criteria used by clinical laboratories for identification of S. bovis group were not reliable.2 It is possible that many fruitless colonoscopy procedures were performed based on erroneous laboratory taxonomic lumping, physicians' trust in the reliability of the comment "associated with GI malignancy" became eroded, and that some true associations were missed because some strains failed to hydrolyze esculin.
Microbiologists today have the resources to identify S. bovis isolates quite well, even if they do not have DNA sequencing capability. Beck et al reported that both the API 20 Strep and the Rapid ID 32 Strep (bioMérieux, Marcy l'Etoile, France) did a credible job arriving at the correct identification.2 The most recent species names, their biotypes, and the known clinical correlations are listed in Table 1.1,3,5,6,7,8 One caveat is that two different groups of workers have validly published the names S. gallolyticus subsp. pasteurianus and S. pasteurianus for what appears to be the same species. This illustrates one of the problems (for microbiologists and clinicians alike) with modern molecular microbial taxonomy, as opposed to when taxonomy was based on somewhat universal methods of phenotypical characterization. Strains may appear more or less closely related depending on which genetic elements are sequenced, and when organisms' nucleic acid sequences differ at one point they may not differ elsewhere. Workers looking at one area of the genome may not appreciate these differences. Thus, a different name may be published for the same organism based on a different molecular pattern. When two names are validly published, the deciding factor as to which name gains acceptance is based on which name is used more commonly. Eventually, the lesser-used name becomes obsolete (but still valid). This happened with the organism we know primarily as Moraxella catarrhalis, but whose other name, Branhamella catarrhalis, is still valid.4 For many years, microbiologists referred to this species as Moraxella (Branhamella) catarrhalis because both names were used equally often (so neither had taken precedence).
Another problem in taxonomy is that when scientists investigate a genus carefully with new molecular tools, they may find that a similar organism has been described before with another species name. The earlier strain, deposited in the American Type Culture Collection or other organism repository, can be retrieved and retested with molecular methods and compared with the more recent organism or the type species of the organism currently in common usage. If the earlier organism is found to be virtually identical (by DNA homology) to the more recent species, the earlier name takes precedence and the more familiar name is declared invalid. This happened with S. bovis when an earlier strain, validly characterized and named S. equinus (in 1906), was found to be indistinguishable from S. bovis.7
Now that we can identify the various biotypes (and with new valid species names) of the group of organisms formerly known as S. bovis, we can report the name and the clinical association with more granularity, and clinicians will have a better idea of what the implications of our report are for their patients. This is a good thing, and microbiology laboratories should be encouraged to modify their practices for nonhemolytic, grayish colonies of streptococci isolated from blood cultures.
References
- Klein RS, et al. Association of Streptococcus bovis with carcinoma of the colon. N Engl J Med. 1977;297:800-802.
- Spellerberg, B, Brandt C. Streptococcus. Manual of Clinical Microbiology. Ed. P. Murray et al. Washington, DC: ASM Press, 2007;9:412-429.
- Beck M, et al Comprehensive study of strains previously designated Streptococcus bovis consecutively isolated from human blood cultures and emended description of Streptococcus gallolyticus and Streptococcus infantarius subsp. coli. J Clin Microbiol. 2008;46:2966-2972.
- Baron EJ. Staphylococcus lugdunensis, not your father's (or mother's) coagulase-negative staphylococcus. Infectious Disease Alert. 2003;22:193-195.
- Ruoff KL, et al. Bacteremia with Streptococcus bovis and Streptococcus salivarius: Clinical correlates of more accurate identification of isolates. J Clin Microbiol. 1989;27:305-308.
- Vandamme P, et al. Streptococcus intestinalis Robinson et al. 1989 and Streptococcus alactolyticus Farrow et al. 1984 are phenotypically indistinguishable. Int J Syst Bacteriol. 1999;49:737-741.
- Purdy RA, et al. Streptococcus bovis meningitis: Report of 2 cases. Neurology. 1990;40:1782-1784.
- Namiduru M, et al. A case of septicaemia, meningitis, and pneumonia caused by Streptococcus bovis type II. Int J Clin Pract. 2003;57:735-736.
- Enright MC, McKenzie H. Moraxella (Branhamella) catarrhalis — clinical and molecular aspects of a rediscovered pathogen. J Med Microbiol. 1997;46:360-371.
- Poyart C, et al. Taxonomic dissection of the Streptococcus bovis group by analysis of manganese-dependent superoxide dismutase gene (sodA) sequences: Reclassification of Streptococcus infantarius subsp. coli as Streptococcus lutetiensis sp. nov. and of Streptococcus bovis biotype 11.2 as Streptococcus pasteurianus sp. nov. Int J Syst Evol Microbiol. 2002;52:1247-1255.
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