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1 SHIGELLA NOMENCLATURE WILLIAM H. EWING Communicable Diseate Center,1 Public Health Service, Federal Security Agency, Atlanta, Georgia Received for publication March 14, 1949 The following proposals regarding nomenclature and usage within the genus Shigella are made for the consideration of all who work with members of the group. The problems of numbering or naming the various types are manifold and vexing but are in no way more difficult than the question of which microorgani to include in the genus and which to delete or exclude. Another difficulty is the attempt by many to make the terms Shigela and dysentery bacteria synonymous. This is improper from the standpoint of bacterial taxonomy. Proposals concerning these problems are numerous (see Weil, 1947; Neter, 1942, 1948), and others will appear in the literature soon (Ferguson and Kauffmann, 1948). Since the writer is not in accord with all the recommendations made by other authors, the following proposals are made. The views set forth are in general agreement with those of Boyd (1948). Although the schema (table 1) will be criticized, in the opinion of the author it offers, nevertheless, a simpler and more useful classification than any proposed to date. It appears to satisfy the needs of the laboratory worker, epidemiologist, practicing physician, and the taxonomist. There is little that is new in this proposal. It is merely a reorganization, based in part upon biochemical characteristics, antigenic relationships, and tradition. Tradition is abandoned, however, where it serves no useful purpose. The types are arranged within the schema so that additions can be made when other types that satisfy the generic criteria are described. The genus ShigeUa is defined as follows: gram-negative bacteria that are aerobic, nonsporulating, nonmotile, and, with a few exceptions, nonproductive of gas from fermentable substances. They do not utilize salicin, adonitol, or citrate, or hydrolyze urea, liquefy gelatin, or form acetylmethylcarbinol. Lactose is utilized by only two recognized species (Shigella sonnei and Shigella dispar), and by these only upon prolonged incubation. Several microorganisms now listed in Bergey'8 Manual (Breed et al., 1948) may be deleted from the genus Shigella on the basis of the descriptions given there: Shigella equirudli, Shigella 8epticemiae, and Shigella pfaffi. For the present, it is necessary to retain Shigella gintouensis in an appendix. Descriptions of this species are inadequate, but cultures are isolated occasionally that may belong to it (unpublished data). If this species is retained, it would be placed in group D of the schema. Shigella dysenteriae I is retained as the type species of the genus Shigella because of precedent; there seems to be little need for change. The species pre- 1 From the Enteric Bacteriology Laboratory. 633
2 634 WILLAIM H. EWING [vol. 57 TABLE 1 The genus Shigella: dysentery and related bacteria PROPOSED DESIGNATION PREVIOUS DESGNATION Group A Shigella dysenteriae I Shigella dysenteriae (Shiga), Shiga- Kruse bacillus, Bacterium shigae, etc. II Shigella schmitzii, Shigella ambigua, Bacterium ambiguu8, etc. *III Q 771 of Large-Sachs group, type 8524 (Gober et al.), Shigella arabinotarda A, (Christensen and Gowan). IV V Q 1030 VI Q 454 VII Q 902 Q 1167 of Large-Sachs group; Shigella arabinotarda B. Abbr.eviated +Boyd- drewes Weil fornmuwa na Anantigenic Wheeler and WelOther Group B Shigella flexneri I I:4,... F.I V F.I I I:46... F.I VZ F.I,III II II:4,... F.IIa W F.II II II:7,8,9... F.IIb WX F.II,VII -:7,8,9... X F.VII -:4... Y F.VIII III III :6, 7... F.III Z F.III IV IV:4... F.IV F.IV Boyd 103 IV IV:6... F.IV F. III, IV V V: F.V F.V Boyd P.119 VI VI: F.VI F.VI Boyd 88, Newcastle and Manchester bacilli, Shigella newcastle Group C Shigella boydii I B.I F.IX Boyd 170 II B.II F.X Boyd P.288 III B.III F.XI Boyd D.1 IV B.IV F.XIV Boyd P.274 V B.V F.XIII Boyd P.143 VI B.VI F.XII Boyd D.19 VII "Lavington,"1 type T, Shigella etousae
3 1949] SHIGELLA NOMENCLATURE 635 TABLE 1-Continued PROPOSED DESIGNATION PREVIOUS DESIGNATION Group D Shigella sonnei Sonne-Duval bacillus, Kruse-E-Ruhr, Shigella ceylonensis A. Shigella dispar I Serotype I, Carpenter and Stuart, Shi. gella madampensis (Castellani). II Serotype Ila, b, c, d, Carpenter and Stuart, Shigella ceylonensis B (Castellani). Group E Shigella alkalescenu Serotypes of Stuart et al., type I, De Asis * To be written with name and type designation when needed for epidemiological purposes: B., Boyd, F., Flexner. viously referred to as ShigeUa chmitzii (or Shigella ambigua) becomes Shgella dysenteriae II, and the members of the Large-Sachs group are numbered consecutively as types within the species, thus compsing ShigeUa dyeenteriae I through VII (table 1). There is little serorelation between members of this "group," but it must be remembered that neither is there any important serologic connection between these types and members of the other groups of shigellae mentioned below. The microorganims designated Shigella dy8enteriae I through VII are the shigellae that are consistently mannitol-negative. Shigella types (a) that do not utilize this substrate, (b) that may or may not be related serologically to one or more of the above serotypes, and (c) that lack important group relationships to Shigellaflezneri can be added to the list when the need arises. Two microorganisms that should be considered for possible inclusion are no (Wheeler and Stuart, 1946) and A 12 (Sachs, 1943). If, in the future, variants of members of the ShigeUa dysenteriae group are described that utilize manitol, they nevertheless should be added to the group (v. inf. mannitol-negative variants of Shigells flenere types). Separation of the mannitol-negative shigeliae into different species based upon supposed differences in pathogenicity or upon tradition is not believed to be warranted or desirable. The species name Shigella paradysenteriae is discarded and the terms ShigeUa flexnri and Shigella boydii (comb. nov.) are substituted. The former term is already in the literature (Wilson and Miles, 1946) but Shigella boydii is apparently a new combination. Members of the Flexner group B (table 1) are biochemically similar and serologically related. At present there are six serotypes of S. flexneri. These should be designated by Roman numerals referring to their type-specific or major antigens. Futher, it is recommended that the partial antigenic formula be employed in reporting the results of typing when such data are needed for epidemiological or other purposes. In this way, exact typing methods can be employed and reported without recourse to alphabetic designa-
4 636 WILLIAM H. EWING [VOL. 57 tions, subtype or race names, or other confusing terminology (e.g., Shigella flexneri I:4... and Shigellaflexre I:4, 6... for "V" and "VZ" or ShigeUa flexneri II:4... and Shigella flexneri II:6, 7... for "W" and "WX"). Undoubtedly, other antigenic types of S. flexneri will be reported, i.e., microorganisms that have antigens in common with described serotypes. The S. flexneri types characteristically are fermenters of mannitol, but variants are known that do not utilize this substrate, viz., Shigella flexnr IV (Nelson, 1947) and Shigella flexneri VI (Clayton and Warren, 1929). The microorganism described as Bacterium dysenteriae, Dudgeon and Urquhart (Hazen, 1938), is a typical S. flexneri VI (Ferguson, 1946; Ewing, unpublished data). The shigellae described by Francis (1946) as provisional Flexner VII and VIII are not included in the Shigella flexneri group. The former (Ewing, no , and no of Wheeler et al., 1946) is regarded more properly as a biochemical variant of ShigeUa dispar (Carpenter and Stuart, 1946; Ewing, in manuscript) and, although the taxonomic position of Francis' provisional type VIII is undecided, it is known to be related to S. dispar and to certain paracolon bacteria (Ewing, in manuscript). These bacteria are related, through minor antigens, to certain S. flexneri types, but to no greater extent than are Shigella sonnei or Shigella alkalescens. Shigella boydii (group C) is composed of seven antigenic types at present. These microorganisms are similar in biochemical and cultural characteristics to members of S. flexneri. Described serological relationships with members of the latter group are of a minor nature but intragroup relationships among members of group C are apparent. The serotype described previously as Shigela paradysenteriae "Lavington" (Ewing, 1946), Shigella etousae, or type "T" (Heller and Wilson, 1946; Lavington et al., 1946; Stock et al., 1947) is included as Shigella boydii VII. Present members of this group are easily distinguished by serological methods. Serotypes may be reported by recording the Roman numeral that designates the specific or major antigen together with the specific name. Again, newly described microorganisms may be added to group C when desired. Group D in the schema is composed of those microorganisms that utilize lactose after continued incubation, viz., Shigella 8onnei and Shigelka dispar. These microorganisms can be distinguished both by biochemical and serological means. S. sonnei exists in two phases, as described by Wheeler and Mickle (1946). Phase II is related antigenically to Shigela boydii VI. There are two serotypes of S. dispar (I and II), the second of which may be further subdivided into four serological varieties. These may be designated by use of their antigenic formulae (Carpenter and Stuart, 1946). Other workers would remove S. dispar and S. alkalescens from the genus Shigella but would retain S. sonnei (Ferguson and Kaufmann, 1948; Boyd, 1948). We believe that if one lactose-positive species is removed from the genus, all should be removed and placed in the genus Proshigella, as recommended by Borman et al. (1944). Members of these species contain antigens in common with certain paracolon bacteria as well as with other shigellae (Ferguson and Henderson, 1947; Ewing, in manuscript), but this does not seem to be a valid reason
5 1949] SHIGELLA NOMENCLATURE 637 for removing them from the genus Shigella. The common form of S. alkalescens is a typical member of the Shigella genus and should be retained in it. Paracolon and coliform bacteria that contain antigens in common with S. alkalescens (Stuart et al., 1943) may be reported as paracolon bacteria; their taxonomic status is beyond the scope of this paper. The three species mentioned above are retained in the genus and appear in the schema as groups D and E. Possibly in the future there will be some reason for deleting these microorganisms from the genus, but at present none is apparent. REFERENCES BORMAN, E. K., STUART, C. A., AND WHEELER, K. M Taxonomy of the family Enterobacteriaceae. J. Bact., 48, BOYD, J. S. K The classification of the dysentery bacilli. J. Trop. Med. Hyg., 51, BREED, R. S., MURRAY, E. G. D., AND HITCHENS, A. P Bergey's manual of determinative bacteriology. 6th ed. Williams & Wilkins Co., Baltimore, Md. CARPENTER, P. L., AND STUART, C. A Antigenic relationships of Shigella dispar, types I and II, to Shigella paradysenteriae, Boyd type P143. Proc. Soc. Exptl. Med., 61, CLAYTON, F. H. A., AND WARREN, S. H An unusual bacillus recovered from cases presenting symptoms of dysentery. J. Hyg., 28, EWING, W. H An additional Shigella paradysenteriae serotype. J. Bact., 51, FERGUSON, W Personal communication. FERGUSON, W., AND HENDERSON, N. D Description of C-27: a motile organism with the major antigen of Shigella sonnei phase I. J. Bact., 54, FERGUSON, W., AND KAUFFMANN, F Personal communication. HAZEN, E. L Isolation of B. dysenteriae (Dudgeon and Urquhart) in an outbreak of diarrhea. J. Infectious Diseases, 63, HELLER, G., AND WILSON, S. G A new species of Shigella. J. Path. Bact., 58, LAVINGTON, R. J., MATHESON, A. J., TAYLOR, J., AND FLEMMING, W. J. D An institutional outbreak due to a hitherto undescribed dysentery bacillus. J. Path. Bact., 58, NELSON,M. G Non-mannitol-fermenting Shigellajlexneri type 103. J. Path. Bact., 59, NETER, E The genus Shigella. Bact. Revs., 6, NETER, E The genus Shigella and shigellosis. Am. J. Digestive Diseases Nutrition, 15, SACHS, A A report of an investigation into the characteristics of new types of nonmannitol-fermenting bacilli isolated from cases of bacillary dysentery in India and Egypt. J. Roy. Army Med. Corps, 80, STOCK, A. H., EISENSTADT, I., TRIPLETT, G. W., AND CATTO, A II. Pathogenicity of a new serologic type of dysentery bacillus (T-2 Med. Lab. or Lavington I or Etousa). J. Infectious Diseases, 81, STUART, C. A., RUSTIGIAN, R., ZIMMERMAN, A., AND CORRGAN, F. V Pathogenicity, antigenic relationships and evolutionary trends of Shigella alkalescens. J. Immunol., 47, WEIL, A. J Dysentery. J. Immunol., 55, WHEELER, K. M Antigenic relationships of Shigella paradysenteriae. J. Immunol., 48,
6 638 WILLIAM H. EWING [VOL. 57 WHEELER, K. M., AND MICKLE, F. L Antigens of Shigella sonnei. J. Immunol., 51, WHEELER, K. M., AND STUART, C. A The mannitol-negative Shigella group. J. Bact., 61, WHEELER, K. M., STUART, C. A., AND EWING, W. H The antigenic complex of Shigella paradysenteriae, Boyd type P 274. J. Bact., 51, WILSON, G. S., AND MILES, A. A Topley and Wilson's principles of bacteriology and immunity. 3d ed. Williams & Wilkins Co., Baltimore, Md.
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