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Differentiation and Distribution of Three Types of Exfoliative Toxin Produced

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Differentiation and Distribution of Three Types of Exfoliative Toxin Produced FEMS Immunology and Medical Microbiology 20 (1998) 301^310 Di¡erentiation and distribution of three types of exfoliative toxin produced by Staphylococcus hyicus from pigs with exudative epidermitis Lars Ole Andresen * Department of Microbiology, Danish Veterinary Laboratory, Buëlowsvej 27, DK-1790 Copenhagen V, Denmark Received 20 December 1997; revised 19 February 1998; accepted 20 February 1998 Abstract Exfoliative toxins of approximately 30 kDa produced by Staphylococcus hyicus strains NCTC 10350, 1289D-88 and 842A-88 were purified and specific polyclonal antisera were raised against each of the toxins. It was shown by immunoblot analysis and ELISA that three exfoliative toxins from S. hyicus were antigenically distinct. The three toxins were designated ExhA, ExhB and ExhC. From 60 diseased pigs, each representing an outbreak of exudative epidermitis, a total of 584 isolates of S. hyicus were phage typed and tested for production of exfoliative toxin. ExhA-, ExhB- and ExhC-producing S. hyicus isolates were found in 12 (20%), 20 (33%) and 11 (18%), respectively, of the 60 pig herds investigated. Production of the different types of exfoliative toxin was predominantly associated with certain phage groups. However, toxin production was found in all of the six phage groups defined by the phage typing system. Some changes in the distribution of isolates between phage groups were observed when the results of this study were compared to previous investigations. In this study two new antigenically distinct exfoliative toxins were isolated and tools for in vitro detection of toxin producing S. hyicus isolates and for further studies on the exfoliative toxins from S. hyicus have been provided. z 1998 Federation of European Microbiological Societies. Pub- lished by Elsevier Science B.V. Keywords: Staphylococcus hyicus; Exfoliative toxin; Exudative epidermitis; Antigenic diversity; Autogenous vaccine 1. Introduction foliative toxin has been shown to be the factor re- sponsible for the alterations of the skin in EE in pigs The disease exudative epidermitis (EE) in pigs is [4] and the production of exfoliative toxin correlates caused by infection with Staphylococcus hyicus. Stud- with the ability of the strains to induce EE in pigs ies have shown that both virulent and avirulent S. [5]. hyicus can be isolated from diseased pigs [1]. The Staphylococcal scalded skin syndrome (SSSS) in virulent strains produce an approximately 27-kDa humans is a skin disease with aspects in common [2,3] or 30-kDa [1,4] exfoliative toxin. S. hyicus ex- with EE in pigs. SSSS and EE are both generalised skin infections that a¡ect young individuals and pig- * Tel.: +45 35 30 02 82; Fax: +45 35 30 01 20; lets, respectively. Patients with SSSS are usually E-mail: [email protected] under the age of 5 years [6] and EE a¡ects piglets 0928-8244 / 98 / $19.00 ß 1998 Federation of European Microbiological Societies. Published by Elsevier Science B.V. PII S0928-8244(98)00026-1 FEMSIM 864 27-4-98 302 L.O. Andresen / FEMS Immunology and Medical Microbiology 20 (1998) 301^310 in the age of 1^5 weeks, but mild forms of the dis- genically distinct exfoliative toxins were isolated and ease can be observed among older pigs [7]. The his- designated ExhA, ExhB and ExhC, respectively. Fur- topathological alterations of the skin in the two dis- thermore, the prevalence and distribution of the dif- eases are similar [6,8] and are in both cases caused by ferent toxins among S. hyicus isolates from pigs with toxins [3,4,9]. SSSS in humans is caused by infection EE were investigated. with Staphylococcus aureus producing antigenically distinct exfoliative toxins ETA and ETB, which are the factors that cause exfoliation of the skin [9]. 2. Materials and methods Studies on S. hyicus have shown that several phage types could be isolated simultaneously from the skin 2.1. Bacterial strains, growth media and culturing of diseased pig [1,10] and it was shown that only one conditions of the clones from diseased pigs colonised by multi- ple clones of S. hyicus could induce EE [1]. During Eighteen strains of S. hyicus previously reported recent years phage typing have been used for selec- [1] to be either virulent or avirulent were used in this tion of strains for production of autogenous vaccine study (see Table 1). Furthermore, a total of 584 S. in our laboratory. Eight to 10 isolates from submit- hyicus isolates were used for investigating the preva- ted material have been phage typed and one isolate lence and distribution of the three types of exfolia- of each phage type was selected for preparation of a tive toxin among di¡erent phage groups of S. hyicus. mixed autogenous vaccine. This procedure was chos- These 584 isolates were from 60 specimens from dis- en because there was no suitable laboratory method eased pigs each representing an outbreak of EE. Iso- available for selection of disease-causing clones, e.g. lates were randomly picked from primary plates in by testing for production of exfoliative toxin, and the sets of 8^10 isolates from each piglet with EE or skin use of multiple phage types from the same specimen samples from piglets with EE submitted to the Dan- should increase the probability of including the dis- ish Veterinary Laboratory during the period Decem- ease-causing clone in the vaccine. ber 1996 to July 1997. Recently, antigenic diversity among exfoliative After isolation and identi¢cation, S. hyicus was toxins produced by S. hyicus has been reported. Ta- grown on Columbia agar base (Oxoid, Unipath nabe et al. [5] have distinguished between two types Ltd, Basingstoke, UK) plates containing 5% bovine of exfoliative toxin by immunodi¡usion using anti- blood (C-blood agar). Liquid growth medium con- sera against exfoliative toxin produced by the S. hy- sisted of 30 g l31 Trypticase soy broth (BBL 11768, icus strains P-1 and P-23. In a recent study [4] it was Becton Dickinson and Co., Cockeysville, MD, USA) shown that polyclonal and monoclonal antibodies supplemented with 10 g l31 yeast extract (Oxoid against the exfoliative toxin produced by S. hyicus L21), pH was 7.2. Liquid cultures were grown in strain 1289D-88 only reacted with two of nine well tightly closed 10-ml tubes containing 5 ml of Trypti- characterised virulent S. hyicus strains in both immu- case-yeast extract medium at 37³C with shaking at noblot analysis and indirect ELISA. These observa- 130 rpm. Strains were stored at 380³C as overnight tions are important since the need for better diagnos- culture scraped from C-blood agar plates and sus- tic tools for selection of isolates for production of pended in liquid growth medium supplemented autogenous vaccines has become more pressing as with 10% glycerol. Strains from which exfoliative the number of outbreaks of EE in Danish pig herds toxin was puri¢ed were grown under small-scale fer- has increased during the past 10 years. mentation conditions as described previously [4]. The aim of the present study was to purify the putative exfoliative toxin produced by selected viru- 2.2. Isolation and identi¢cation lent strains of S. hyicus and to raise polyclonal and monoclonal antibodies against the toxins in order to Non-pigmented colonies isolated on selective/indi- identify the exfoliative toxin from these strains and cative medium [11] as described by Wegener [12] to investigate the antigenic diversity of the exfoliative were selected for further identi¢cation. In addition toxins from di¡erent strains of S. hyicus. Three anti- to being positive for lipase, and non-haemolytic on FEMSIM 864 27-4-98 L.O. Andresen / FEMS Immunology and Medical Microbiology 20 (1998) 301^310 303 C-blood agar, isolates which were positive for hya- ammonium sulfate at 75% saturation, and the toxin luronidase [13], heat-stable nuclease [14] and catalase was puri¢ed by hydrophobic interaction chromatog- and gave a negative reaction for oxidase [15] were raphy on a phenyl-Sepharose CL-4B (Pharmacia, identi¢ed as S. hyicus. These criteria were su¤cient Uppsala, Sweden) column eluded by a gradient to distinguish S. hyicus from other relevant Sta- from 0.8 to 0.3 M (NH4)2SO4 in 25 mM KH2PO4, phylococci [16]. In particular S. hyicus was distin- pH 7.0. The exfoliative toxin was identi¢ed as a dis- guished from S. chromogenes by S. hyicus being tinct red-brown coloured band of approximately 30 able to hydrolyse Tween 80 (lipase activity) and hav- kDa in silver staining of SDS-PAGE gels [4]. Frac- ing a positive reaction for heat-stable nuclease and tions containing exfoliative toxin were pooled, dia- hyaluronidase [17]. lysed and further puri¢ed by anion exchange chro- matography on a diethylaminoethyl (DEAE)- 2.3. Phage typing Sepharose CL-6B (Pharmacia) matrix using a linear elution gradient from 0.0 to 0.2 M NaCl in 10 mM Phage typing and interpretation of phage typing NaH2PO4, pH 6.0. Fractions were analysed by SDS- results was performed according to [12] using a PAGE and proteins were visualised by silver staining phage typing system derived from a phage typing as described below. system described by Wegener [12]. Changes were that the phage typing system used in the present 2.5. Sodium dodecyl sulfate-polyacrylamide gel study comprised only 10 di¡erent lytic phages and electrophoresis (SDS-PAGE) and silver staining that the criteria for di¡erentiation between phage of proteins types were one `strong reaction di¡erence' (a `strong reaction di¡erence' being when a phage produced Analysis of the puri¢cation procedure was per- more than 50 plaques in one strain and no plaques formed by SDS-PAGE by the method of Laemmli in another strain).
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