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Download PDF (47K) NOTE Bacteriology Antimicrobial Susceptibilities of Exfoliative Toxigenic and Non-Toxigenic Staphylococcus hyicus Strains in Japan Keiko FUTAGAWA-SAITO1)*, William BA-THEIN1,2) and Tsuguaki FUKUYASU1) 1)Department of Animal Health 2, School of Veterinary Medicine, Azabu University, 1–17–71 Fuchinobe, Sagamihara, Kanagawa 229– 8501, Japan and 2)Department of Microbiology and Immunology, Shantou University Medical College, Shantou, Guangdong, 515041, P. R. China (Received 17 June 2008/Accepted 29 December 2008) ABSTRACT. Staphylococcus hyicus isolates (n=207), including 150 exfolitative toxigenic and 57 non-toxigenic strains, were examined for their susceptibility to 13 antimicrobial agents by using the dehydrated 96-well MIC panel system. The frequency of their resistance to penicillin and ampicillin was 76.8% (159/207), followed by erythromycin (56%, 116/207), trimethoprim-sulfamethoxazole (28.5%, 59/ 207), chloramphenicol (24.2%, 50/207), kanamycin (19.8%, 41/207), and doxycycline (1.4%, 3/207). Resistance to chloramphenicol and trimethoprim-sulfamethoxazole was significantly higher in toxigenic strains than non-toxigenic strains (p<0.01), whereas kanamycin and erythromycin resistance was significantly higher in non-toxigenic strains (p<0.01 and <0.05, respectively). Resistance to two or more antimicrobials was observed in 85.5% (177/207) of total strains, with a significantly higher occurrence in toxigenic strains (89.3%, 134/ 150 vs. 75.4%, 43/57; p<0.05). KEY WORDS: antimicrobial resistance, bacterial infection, staphylococcus. J. Vet. Med. Sci. 71(5): 681–684, 2009 Exfoliative toxins-producing Staphylococcus hyicus (tox- penicillin (0.06–8 g/ml), ampicillin (0.12–16 g/ml), igenic strains) have been implicated in causing porcine exu- oxacillin (0.25–4 g/ml), cefazolin (0.5–64 g/ml), dative epidermitis particularly in suckling and weaned pigs cefuroxime (0.5–64 g/ml), gentamicin (0.5–64 g/ml), [4, 9, 15]. The isolation rate of toxigenic strains is report- kanamycin (1–128 g/ml), erythromycin (0.25–32 g/ml), edly four times higher in the pigs with exudative epidermitis doxycycline (0.25–32 g/ml), vancomycin (0.5–16 g/ml), than the healthy pigs [8]. Exudative epidermitis is fre- chloramphenicol (1–128 g/ml), trimethoprim-sul- quently treated with antimicrobial agents, but successful famethoxazole (0.5 and 8–9.5 and 152 g/ml, respectively), treatment is complicated by the occurrence of antimicrobial and ofloxacin (0.12–16 g/ml). Staphylococcus aureus resistance among S. hyicus strains. Antimicrobial resistance JCM 2874 (ATCC29213) and Escherichia coli JCM 5491 of the isolates from various animals including diseased pigs (ATCC25922) were included as controls. MIC breakpoints in different countries have been reported [1–3, 14, 16, 17]. of susceptible (S), intermediate (I), and resistant (R), were However, antimicrobial resistance as to the toxin genes car- taken from the CLSI [5]. Significance of differences riage in S. hyicus is not known. between the variables was tested with the 2 test or the This study aimed to determine the antimicrobial suscepti- Fisher’s extract test. bility of toxigenic and non-toxigenic S. hyicus strains from Antimicrobial resistance profile of 207 S. hyicus strains is healthy pigs and pigs with exudative epidermitis in Japan, shown in Table 1. Intermediate resistance was observed and to investigate the association between antimicrobial only for doxycycline (1/207, 0.5%) and chloramphenicol (5/ resistance and the carriage of toxin genes. 207, 2.4%), and is therefore not shown in the table. For total A total of 207 S. hyicus strains, including 150 exfolitative S. hyicus strains, the highest frequency of resistance was toxigenic strains and 57 non-toxigenic strains from exuda- observed with penicillin and ampicillin (76.8%, 159/207), tive epidermitis and healthy pigs, isolated in 8 years followed by erythromycin (56%, 116/207), trimethoprim- between 1994 and 2002 from 17 prefectures in Japan and sulfamethoxazole (28.5%, 59/207), chloramphenicol previously studied for their exfoliative toxigenes [8] , were (24.2%, 50/207), kanamycin (19.8%, 41/207), and doxycy- included in this study. Minimal inhibitory concentration cline (1.4%, 3/207). Resistance to chloramphenicol and tri- (MIC) determination was done by broth dilution method methoprim-sulfamethoxazole was significantly higher in using the dehydrated 96-well MIC panel system (Eiken, toxigenic strains than non-toxigenic strains (p<0.01), Tokyo) following the Clinical and Laboratory Standards whereas kanamycin and erythromycin resistance was signif- Institute (CLSI) guidelines. The following antimicrobials, icantly higher in non-toxigenic strains (p<0.01 and <0.05, the representatives of commonly used drug classes in Japan, respectively). were tested (with tested ranges indicated in parentheses); Based on their antimicrobial resistance patterns, S. hyicus strains could be categorized into 14 distinctive groups (data *CORRESPONDENCE TO: FUTAGAWA-SAITO, K., Department of Animal Health 2, School of Veterinary Medicine, Azabu University, 1– not shown), with 5 predominant groups exhibiting resis- 17–71 Fuchinobe, Sagamihara, Kanagawa 229–8501, Japan. tance to at least 3 antimicrobials (Table 2). Out of five pre- e-mail: [email protected] dominant resistance patterns, penicillin/ampicillin/ 682 K. FUTAGAWA-SAITO, W. BA-THEIN AND T. FUKUYASU Table 1. Antimicrobial resistance profile of 207 S. hyicus strains Antimicrobial Antimicrobial MIC Toxigenic strains Non-toxigenic strains Total class agent resistant n=150 n=57 n=207 P (tested range in g/ml) breakpoint* MIC Range n (%) MIC Range n (%) MIC Range n (%) value** Penicillins Penicillin (0.06–8) 0.25 0.06–>8 118(78.7) 0.06–>8 41(71.9) 0.06–>8 159(76.8) 0.357 Ampicillin (0.12–16) 0.5 0.12–>16 118(78.7) 0.12–>16 41(71.9) 0.12–>16 159(76.8) 0.357 Oxacillin (0.25–4) 0.5 <0.25 0 <0.25 0 <0.25 0 – Cephalosporins Cefazolin (0.5–64) 32 0.5 0 0.5 0 0.5 0 – Cefuroxime (0.5–64) 32 0.5–2 0 0.5–1 0 0.5–2 0 – Aminoglycosides Gentamicin (0.5–64) 16 0.5 0 0.5 0 0.5 0 – Kanamycin (1–128) 64 1–>128 14(9.3) 1–>128 27(47.4) 1–>128 41(19.8) <0.01 Macrolides Erythromycin (0.25–32) 8 0.25–>32 71(47.3) 0.25–>32 45(78.9) 0.25–>32 116(56.0) <0.05 Tetracyclines Doxycycline (0.25–32) 16 0.25–16 2(1.3) 0.25–16 1(1.8) 0.25–16 3(1.4) 1 Glycopeptides Vancomycin (0.5–16) 16 0.5–1 0 0.5–1 0 0.5–1 0 – Phenicols Chloramphenicol (1–128) 32 4–64 50(33.3) 4–8 0 4–64 50 (24.2) <0.01 Folate pathway inhibitors Trimethoprim (0.5–8)– 0.5/9.5– 0.5/9.5– 0.5/9.5– 56(37.3) 3(5.3) 59(28.5) sulfamethoxazole (9.5–152) 4/76 >8/152 >8/152 >8/152 <0.01 Fluoroquinolones Ofloxacin (0.12–16) 4 0.25–1 0 0.25–1 0 0.25–1 0 – Note: MIC resistant breakpoints and ranges are in g/ml. * MIC resistant breakpoints taken from the CLSI. ** p values account for the difference in the number of resistant isolates observed between toxigenic and non-toxigenic strains. Table 2. Antimicrobial resistance patterns among 207 S. hyicus strains Number of isolates (%) Antimicrobial resistance patterns Toxigenic Non-toxigenic Total n=150 n=57 n=207 Penicillin/ampicillin/trimethoprim-sulfamethoxazole 29 (19.3) 0 29 (14.0) Penicillin/ampicillin/erythromycin/trimethoprim-sulfamethoxazole 27 (18.0) 0 27 (13.0) Penicillin/ampicillin/chloramphenicol 25 (16.7) 0 25 (12.1) Penicillin/ampicillin/kanamycin/erythromycin 9 (6.0) 24 (42.1) 33 (15.9) Penicillin/ampicillin/erythromycin 4 (2.7) 12 (21.1) 16 (7.7) Other patterns 56 (37.3) 21 (36.8) 77 (37.2) Resistance to 2 antimicrobials 134 (89.3)* 43 (75.4)* 177 (85.5) Resistance to <2 antimicrobials 16 (10.7) 14 (24.6) 30 (14.5) * p<0.05. trimethoprim-sulfamethoxazole, penicillin/ampicillin/eryth- (177/207) of total strains, with a significantly higher occur- romycin/trimethoprim-sulfamethoxazole, and penicillin/ rence in toxigenic strains (89.3%, 134/150 vs. 75.4%, 43/57; ampicillin/chloramphenicol were restricted to 16.7–19.3% p<0.05). All toxigenic and non-toxigenic strains were sus- of toxigenic strains only, whereas penicillin/ampicillin/kan- ceptible to oxacillin, cefazolin, cefuroxine, gentamicin, van- amycin/erythromycin and penicillin/ampicillin/erythromy- comycin, and ofloxacin, and all non-toxingenic strains were cin patterns were common to both toxigenic and non- susceptible to chloramphenicol. Actually, most non-toxi- toxigenic strains, with a slightly higher occurrence in non- genic strains (95%) are also susceptible to trimethoprim-sul- toxigenic strains. Resistance to two or more antimicrobials famethoxazole. Notably, all resistant strains displayed a (multi-antimicrobial resistance) was observed in 85.5% double resistance to penicillin and ampicillin. ANTIMICROBIAL SUSCEPTIBILITIES OF S. HYICUS 683 There were only a few reports about antimicrobial sus- 745–770. ceptibility of S. hyicus in the past. In a previous study from 2. Aarestrup, F. M., Bager, F., Jensen, N. E., Madsen, M., Mey- Japan in 1987 [14] , the resistance rates for penicillin, eryth- ling, A. and Wegener, H. C. 1998. Surveillance of antimicro- romycin, and doxycycline were 38.7%, 41.1%, and 55.6%, bial resistance in bacteria isolated from food animals to respectively, by using the MIC breakpoints of 1.56 g/ml antimicrobial growth promoters and related therapeutic agents in Denmark. APMIS 106: 606–622. (penicillin), 12.5 g/ml (erythromycin), and 0.39 g/ml 3. Aarestrup, F. M. and Jensen, L. B. 2002. Trends in antimicro- (doxycycline), whereas in our study, using the correspond- bial susceptibility in relation to antimicrobial usage and pres- ing MIC breakpoints of 0.25 g/ml, 8.0 g/ml, and 16.0 g/ ence of resistance genes in Staphylococcus hyicus isolated ml, the resistance rates were 76.8%, 56%, 1.4%, respec- from exudative epidermitis in pigs.
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