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Profiles of Yersinia Enterocolitica-Like Strains

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Profiles of Yersinia Enterocolitica-Like Strains J. Med. Microbiol. Ð Vol. 51 62002), 56±69 # 2002 The Society for General Microbiology ISSN 0022-2615 ANTIMICROBIAL AGENTS Natural antibiotic susceptibility and biochemical pro®les of Yersinia enterocolitica-like strains: Y. bercovieri, Y. mollaretii, Y. aldovae and `Y. ruckeri' INGO STOCK, BEATE HENRICHFREISE and BERND WIEDEMANN Institute of Medical Microbiology and Immunology, Pharmaceutical Microbiology, University of Bonn, Germany The natural susceptibility of 54 Yersinia enterocolitica-like strains of Y. bercovieri for- merly Y. enterocolitica biovar 3B, n 17), Y. mollaretii formerly Y. enterocolitica biovar 3A, n 12), Y. aldovae formerly Y. enterocolitica-like group X2, n 10) and `Y. ruckeri' n 15) was tested to 69 antibiotics. MIC values were determined with a microdilution procedure in IsoSensitest broth for all strains and in cation-adjusted Mueller Hinton broth for some strains. All yersiniae tested showed uniform MIC distributions to most antibiotics and were naturally sensitive or intermediate to aminoglycosides, several cephalosporins, and penicillins, carbapenems, aztreonam, quinolones, tetracyclines, antifolates, chloramphenicol and nitrofurantoin, and naturally resistant to benzylpeni- cillin, oxacillin, all macrolides except azithromycin, lincosamides, streptogramins, glycopeptides, rifampicin and fusidic acid. Signi®cant differences in susceptibility affecting clinical assessment criteria were seen with aminopenicillins in the presence and absence of â-lactamase inhibitors), some cephalosporins e.g., cefoxitin) and fosfomycin. Whereas strains of Y. aldovae and `Y. ruckeri' were naturally sensitive or intermediate to amoxicillin and amoxicillin/clavulanate, strains of Y. bercovieri and Y. mollaretii were naturally resistant or naturally resistant or intermediate, respectively. Strains of the two latter species were also highly susceptible to fosfomycin. These data can be valuable for the validation of routine susceptibility test results. â-Lactam MICs suggest that Y. bercovieri and Y. mollaretii strains express chromosomally encoded AmpC â-lactamases and that most Y. aldovae and `Y. ruckeri' strains express no, or only small amounts, of enzyme. An evaluation of 30 biochemical tests that determined phenotypic identi®cation to the Yersinia species level is presented. Introduction spp. [4±9] and some strains of several species cause human disease [2, 10, 11]. There is evidence that Yersinia enterocolitica is a well-known human patho- failure to detect `environmental' strains acting as agents gen that causes various gastrointestinal and systemic of human infections is because of their biochemical syndromes [1]. It has been shown previously that sev- similarity. Most commercially available identi®cation eral strains previously labelled as Y. enterocolitica or Y. systems are unable to identify `non-pathogenic' Yersi- enterocolitica-like were distinct species. Today eight nia spp. to the species level; in most cases they are `new' Yersinia species are known which were primarily misidenti®ed as Y. enterocolitica [12]. Because there is assigned to the Y. enterocolitica complex. Although the only little information on the antibiotic susceptibility clinical signi®cance of these species has been discussed patterns of the `new' Yersinia spp., this study focused controversially, there is strong evidence that they are on the antibiotic susceptibility of four of them. Y. mol- implicated in human disease. Most of the `new' species laretii and Y. bercovieri have been described most can be found in water, soil and different animals, but recently [13] and were formerly called Y. enterocolitica all have been isolated from human clinical samples biovars 3Aand 3B, respectively. Strains of the latter [2, 3]. Moreover, in recent years virulence markers species produce a novel heat-stable enterotoxin [8], and have been found in these `non-pathogenic' Yersinia some Y. mollaretii strains also display enterotoxin activity [7]. Y. aldovae strains were formerly desig- Received 13 June 2001; accepted 23 July 2001. nated Y. enterocolitica-like group X2 [14]. They, like Y. Corresponding author: Dr I. Stock 6e-mail:ingostock@ mollaretii and Y. bercovieri have been isolated from hotmail.com). human faeces [3, 13]. Some isolates of Y. aldovae also CHARACTERISATION OF Y. ENTEROCOLITICA-LIKE STRAINS 57 produce enterotoxin [5]. `Y. ruckeri', one of the the following sugars: cellobiose, fucose, á-methyl-D- `classical' agents of red mouth disease in salmon and glucoside, lactose, maltose, melibiose, raf®nose, and trout, was shown to be taxonomically distinct from sorbose 6all Fluka Chemie, Buchs, Switzerland). Yersinia spp. [15±17]. Strains of this species have been Salicin fermentation was tested in Salicin broth 6Fluka found occasionally in human patients [2, 3]. Chemie) with salicin 0.5%. All tests were incubated at 288C and read after 24 h. Tube and plate tests were also The aim of the study was to establish a database for the read after 48 h and 7 days. natural susceptibility to a wide range of antibiotics of Y. bercovieri, Y. mollaretii, Y. aldovae and `Y. ruckeri' Antibiotics and antibiotic susceptibility testing strains and determine whether there are differences in natural susceptibility, which could be valuable for the Antibiotic susceptibility was tested with a microdilu- validation of routine susceptibility test results and tion procedure in IsoSensitest Broth 6Oxoid). Five might contribute to the identi®cation of these bacteria. strains of each species were also tested in cation- adjusted Mueller Hinton Broth 6CAMHB; Difco). After inoculation of antibiotic-containing microtitration Material and methods plates 6Merlin-Diagnostika) with 100 ìl of bacterial suspension, 63±7) 3 105 cfu=ml, and incubation for Bacterial strains 22 h at 378C, MIC values were determined with a Atotal of 54 Yersinia strains was examined, of which photometer for microtitration plates 6Labystems Multi- 33 strains ± Y. aldovae 68), Y. bercovieri 610), Y. scan Multisoft, Helsinki, Finland). MIC data were mollaretii 611) and `Y. ruckeri' 64) were kindly evaluated with EXCEL 6Microsoft). All antibiotics provided by Heinrich Neubauer, Munich, and came were kindly provided by the manufacturers to Merlin- from the Hygiene-Institut of Hamburg, Germany and Diagnostika who produced the antibiotic-containing included isolates from clinical specimens, mammals, plates. aquatic sources and different soils. Three further `Y. ruckeri' strains from the culture collection of A. Evaluation of natural antibiotic susceptibility Rodloff, Leipzig, were isolated from clinical sources. Five strains of Y. bercovieri from human specimens The evaluation of natural antibiotic susceptibility was were kindly provided by Marisa Dolina, Lugano, performed as described previously [20±22]. Clinical Switzerland 63) and Gerda Stempfel, Weingarten, breakpoints for apramycin, lividomycin Aand ribosta- Germany 62). Y. aldovae ATCC 35236 6isolated from mycin were de®ned as proposed recently [23]. water, Czech Republic), Y. bercovieri ATCC 43970 6isolated from human faeces, USA) and Y. mollaretii ATCC 43969 6isolated from soil, France) were obtained Results from the American Type Culture Collection 6Rockville, Identi®cation MD, USA). Y. aldovae ATCC 35237 6isolated from ®sh, USA), Y. bercovieri CCUG 26330 6isolated from The identi®cation of all the strains submitted was food, France), `Y. ruckeri' ATCC 29473 and CCUG con®rmed to both the genus and the species level. 21537 6isolated from rainbow trout in France and the In most cases the data were in agreement with the Czech Republic) were provided by the Culture Collec- literature. However, for several tests 6â-galactosidase, tion of the University of GoÈteborg, Sweden. Most of ornithine decarboxylase, urease, citrate assimilation, six further `Y. ruckeri' strains from the USAwere from fermentation of myo-inositol, rhamnose and xylose), rainbow trout; they were obtained from the Bacteria and some species, the percentages of positive reactions Culture Collection in Gent, Belgium. Escherichia coli were signi®cantly higher than the data of Farmer [19] ATCC 25922 and Y. pseudotuberculosis ATCC 29833 6Table 1). Surprisingly, the test results of the Voges served as controls for antibiotic susceptibility testing. Proskauer reaction and the fermentation results of cellobiose, melibiose and lactose for strains of Y. aldovae disagreed with the data of Neubauer et al. Identi®cation [18], but were similar to the data of Farmer [19] 6Table Strains were identi®ed to the genus level with a com- 1). mercial identi®cation system for Enterobacteriaceae 6Micronaut-E, Merlin-Diagnostika, Bornheim, Ger- Antibiotic susceptibility, natural sensitivities and many). The inoculum for the test reactions was a resistances suspension in physiological saline solution at 1 3 106 cfu/ml from an overnight culture on IsoSensitest Agar An overview of the antibiotic susceptibilities of the 6Oxoid). Identi®cation to species level was by conven- strains is shown in Table 2. Natural antibiotic sen- tional tests with discriminating features of Yersinia spp. sitivities and resistances are summarised in Table 3. [2, 18, 19]. Sugar fermentation tests were performed in plates on bromcresol-purple-agar 6Difco Laboratories, Although there were some species-related differences Detroit, MI, USA) supplemented to 0.5% with one of in susceptibility, all species were naturally sensitive or 58 I. STOCK, B. HENRICHFREISE AND B. WIEDEMANN Table 1. Biochemical features of the Yersinia strains tested Positive
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