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Trends in Antimicrobial Susceptibility in Relation to Antimicrobial Usage

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Trends in Antimicrobial Susceptibility in Relation to Antimicrobial Usage Veterinary Microbiology 89 (2002) 83–94 Trends in antimicrobial susceptibility in relation to antimicrobial usage and presence of resistance genes in Staphylococcus hyicus isolated from exudative epidermitis in pigs Frank Møller Aarestrup*, Lars Bogø Jensen Danish Veterinary Institute, 27 Bu¨lowsvej, DK-1790 Copenhagen V, Denmark Received 11 March 2002; received in revised form 11 July 2002; accepted 16 July 2002 Abstract From 1996 to 2001 a total of 467 Staphylococcus hyicus isolates from exudative epidermitis (EE) in pigs in Denmark were examined for susceptibility to 13 different antimicrobial agents. The presence of selected genes encoding macrolide (erm(A), erm(B) and erm(C)), penicillin (blaZ ), streptogramin (vat, vga, vga(B), vat(B), vat(D) and vat(E)), streptomycin (aadE ) and tetracycline resistance (tet(K), tet(L), tet(M) and tet(O)) were determined in selected isolates. The occurrence of erythromycin resistance increased from 33% in 1996 to a maximum of 62% in 1997 and decreased to 26% in 2001. Resistance to sulphametazole increased from 17% in 1996 to 30% in 1998 but has since decreased to 4% in 2001. Resistance to trimethoprim increased to 51% in 1997 and decreased to 21% in 2001. Resistance to tetracycline (21–31%) remained relatively constant during 1996–2000, but increased to 47% in 2001. Resistance to penicillin (54–75%) streptomycin (33–53%) and tetracycline (21–47%) remained relatively constant over the time investigated. All 48 penicillin resistant isolates examined contained the blaZ gene and 40 (85%) of the streptomycin resistant isolates the aadE gene. It was not possible to detect any streptogramin resistance gene in four streptogramin resistant isolates. Of the 55 erythromycin resistant isolates examined, five contained erm(A), 13 erm(B), 35 erm(C) and two both erm(A) and erm(C). The presence of erm(B) was confirmed by hybridization to plasmid profiles in all 13 PCR-positive isolates. Of 52 tetracycline resistant isolates examined, two contained tet(L), 38 tet(K) and 12 both tet(K) and tet(L). # 2002 Published by Elsevier Science B.V. Keywords: Staphylococcus hyicus; Pig-bacteria; Antimicrobial agents; Genetics * Corresponding author. Tel.: þ45-35-30-01-00; fax: þ45-35-30-01-20. E-mail addresses: [email protected], [email protected] (F.M. Aarestrup). 0378-1135/02/$ – see front matter # 2002 Published by Elsevier Science B.V. PII: S 0378-1135(02)00177-3 84 F.M. Aarestrup, L.B. Jensen / Veterinary Microbiology 89 (2002) 83–94 1. Introduction Staphylococcus hyicus is the causative agent of exudative epidermitis (EE) in pigs, a generalized infection of the skin characterized by greasy exudation, exfoliation, and vesicle formation (Sompolinsky, 1953; Jones, 1961; L’Ecuyer, 1966). The disease is frequently treated with antimicrobial agents, but treatment is problematic because of the limited number of antimicrobial drugs available for this purpose. A frequent occurrence of antimicrobial resistance has previously been reported among S. hyicus in different countries (Devriese, 1977; Teranishi et al., 1987; Schwarz and Blobel, 1989; Aarestrup et al., 1998a,b). A large number of different antimicrobial agents has been used for therapy and until 1998 also for growth promotion in the production of pigs in Denmark and a frequent occurrence of resistance to these compounds has been observed among several different bacterial species (Aarestrup et al., 1998a,b). However, major changes in the usage of antimicrobial agents especially those used for growth promotion has occurred in the period 1995–1999. This has been for pig production especially, the case for tylosin that belongs to the macrolides. Among enterococci from pigs the decreased usage of tylosin has been followed by a major decrease in the occurrence of macrolide resistance (Aarestrup et al., 2001). Several studies have determined the occurrence of different genes encoding antimicro- bial resistance in staphylococci of human origin. In contrast there is only limited information about the distribution of different resistance genes in staphylococci of animal origin. This study describes the trends in antimicrobial susceptibility and presence of selected resistance genes among S. hyicus isolated from EE in Denmark. In addition, the occurrence of different genes encoding resistance to macrolides, penicillins, streptomycin, and tetracycline among selected isolates is reported. 2. Materials and methods 2.1. Sampling of bacterial species As part of the Danish monitoring for antimicrobial resistance S. hyicus isolates from diagnostic submissions are continuously isolated from cases of EE, tested for susceptibility to antimicrobial agents and stored (Aarestrup et al., 1998a). All isolates were from different herds all over Denmark. In the period of January 1996 to December 2001 a total of 467 isolates were included in the monitoring of resistance at the Danish Veterinary Institute. 2.2. Susceptibility testing Isolates collected during 1996 were, with the exception of avilamycin, tested for their susceptibility using tablet diffusion as previously described (Aarestrup et al., 1998a,b). Isolates collected during 1997–2001 were tested for susceptibility to antimicrobial agents using a commercial dehydrated MIC panel and a semiautomatic inoculation (SensiTitre, F.M. Aarestrup, L.B. Jensen / Veterinary Microbiology 89 (2002) 83–94 85 Trek Diagnostic, UK) following NCCLS guidelines (NCCLS, 2000). Susceptibility of the following antimicrobial agents was determined during the entire time-period: avilamycin, bacitracin, chloramphenicol, erythromycin, gentamicin, oxacillin, penicillin, streptomycin, sulphametoxazole, tetracycline, trimethoprim, and vancomycin. From 1996 to 1997 susceptibility was determined for the fluoroquinolone, enrofloxacin whereas susceptibility was determined for ciprofloxacin from 1998 to 2001. Susceptibility to quinupristin/dalfopristin (Q/D) was only determined from 1998 to 2001. Table 1 Primers used for detection of genes encoding resistance to erythromycin, penicillin, sreptogramin, streptomycin, and tetracycline among S. hyicus from pigs Primer Sequence (50 ! 30) Reference erm(A)-1 50-TCAAAGCCTGTCGGAATTGG-30 Jensen et al. (1998) erm(A)-2 50-AAGCGGTAAACCCCTCTGAG-30 erm(B)-1 50-CATTTAACGACGAAACTGGC-30 Jensen et al. (1998) erm(B)-2 50-GGAACATCTGTGGTATGGCG-30 erm(C)-1 50-ATCTTTGAAATCGGCTCAGG-30 Jensen et al. (1998) erm(C)-2 50-CAAACCCGTATTCCACGATT-30 vat-1 50-TGGAGTGTGACAAGATAGGC-30 Hammerum et al. (1998) vat-2 50-GTGACAACAGCTTCTGCAGC-30 vga-1 50-AGTGGTGGTGAAGTAACACG-30 Hammerum et al. (1998) vga-2 50-CTTGTCTCCTCCGCGAATAC-30 vga(B)-1 50-TGACAATATGAGTGGTGGTG-30 Hammerum et al. (1998) vga(B)-2 50-GCGACCATGAAATTGCTCTC-30 vat(B)-1 50-GGCCCTGATCCAAATAGCAT-30 Hammerum et al. (1998) vat(B)-2 50-GTGCTGACCAATCCCACCAT-30 vat(D) 50-GCTCAATAGGACCAGGTGTA-30 Hammerum et al. (1998) vat(D) 50-TCCAGCTAACATGTATGGCG-30 vat(E) 50-ACTATACCTGACGCAAATGC-30 Jensen et al. (2000) vat(E) 50-GGTTCAAATCTTGGTCCG-30 blaZ-1 50-AAGAGATTTGCCTATGCTTC-30 Vesterholm-Nielsen et al. (1999) blaZ-2 50-GCTTGACCACTTTTATCAGC-30 tet(K)-1 50-TTAGGTGAAGGGTTAGGTCC-30 Aarestrup et al. (2000) tet(K)-2 50-GCAAACTCATTCCAGAAGCA-30 tet(L)-1 50-GTTGCGCGCTATATTCCAAA-30 Aarestrup et al. (2000) tet(L)-2 50-TTAAGCAAACTCATTCCAGC-30 tet(M)-1 50-GTTAAATAGTGTTCTTGGAG-30 Aarestrup et al. (2000) tet(M)-2 50-CTAAGATATGGCTCTAACAA-30 tet(O)-1 50-GATGGCATACAGGCACAGAC-30 Aarestrup et al. (2000) tet(O)-2 50-CAATATCACCAGAGCAGGCT-30 aadE-1 50ATGGAATTATTCCCACCTGA-30 This study aadE-2 50-TCAAAACCCCTATTAAAGCC-30 86 F.M. Aarestrup, L.B. Jensen / Veterinary Microbiology 89 (2002) 83–94 2.3. Detection of genes encoding macrolide, streptogramin, streptomycin, and tetracycline resistance The presence of antimicrobial resistance genes was examined in selected resistant isolates using PCR as previously described (Hammerum et al., 1998; Jensen et al., 1999; Vesterholm-Nielsen et al., 1999; Aarestrup et al., 2000). The presence of the erm(A), erm(B) and erm(C) genes encoding macrolide resistance were examined in 55 erythro- mycin resistant isolates, the blaZ gene encoding penicillin resistance in 48 penicillin resistant isolates, the presence of the tet(K), tet(L), tet(M) and tet(O) genes encoding tetracycline resistance in 52 tetracycline resistant isolates, the vat, vga, vga(B), vat(B), vat(D) and vat(E) genes encoding streptogramin resistance in four Q/D resistant isolates and the presence of the aadE gene encoding streptomycin resistance in 47 streptomycin resistant isolates. The primers used are given in Table 1. DNA sequencing (Sears et al., 1992) verified the identity of the gene products in selected isolates. 2.4. Plasmid profiling Plasmid DNA was purified from all erythromycin resistant isolates, that gave amplicons for the erm(B) gene, using a modified protocol for the Qiagen Plasmid Midi kit (Qiagen, Cat. no. 12243). Cells from a 10 ml overnight culture were harvested in a Beckman centrifuge at 6000 Â g for 10 min and resuspended in 10 ml P1 buffer (50 mM Tris–Cl, pH 8.0; 10 mM EDTA) containing RNase (100 mg/ml) and lysozyme (20 mg/ml). The suspension was placed on a rotary shaker (250 rpm) at 37 8C for 15 min and then 10 ml P2 buffer (200 mM NaOH, 1% SDS) and 10 ml P3 buffer (3.0 M potassium acetate, pH 5.5) was added as described in the Qiagen protocol. The DNA was then purified on a Qiagen Midi column as described by the Qiagen Plasmid Midi Protocol. 2.5. Hybridization Digoxigenin-labeled DNA-probes were prepared by PCR amplification using primers for erm(B) and labeled with the Boehringer Mannheim DNA labeling kit. Southern transfer and hybridization of all plasmid profiles were performed as previously described (Jensen et al., 1998), using the erm(B) probe. 3. Results 3.1. Distribution of antimicrobial resistance using MIC-determination The susceptibility of the different S. hyicus isolates examined with MIC-determination is shown in Table 2. All isolates examined were susceptible to chloramphenicol, gentamicin, oxacillin, and vancomycin with MICs below the NCCLS break points. For avilamycin, the isolates gave one large distribution with most isolates having MICs around 2–4 mg/ml. Two isolates had a MIC above the break point chosen at 16 mg/ml.
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