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Resistance Genes, Phage Types and Pulsed Field Gel Electrophoresis Pulsotypes in Salmonella enterica Strains from Laying Hen Farms in Southern Italy
Department of Veterinary Medicine, Università di Bari, strada provinciale per Casamassima Km 3, Valenzano-Bari 70010, Italy
Department of Biology, Università di Bari "Aldo Moro", Via E. Orabona, 4 70125 Bari, Italy
Department of Infectious, Parasitic and Immuno-Mediated Diseases, Istituto Superiore di Sanità, Rome 00161, Italy
National Reference Laboratory for Salmonella, Istituto Zooprofilattico delle Venezie, Viale dell'Università 10, 35020 Legnaro (Padova), Italy
These two authors contributed equally to this work.
* Author to whom correspondence should be addressed.
Received: 13 May 2013; in revised form: 11 July 2013 / Accepted: 29 July 2013 / Published: 6 August 2013
Abstract: Twenty-four Salmonella enterica isolates (13 serovar Enteritidis and 11 Typhimurium) isolated from 5,600 samples from intensive laying hen farms in Italy in 1998–2007 were characterized for antimicrobial resistance genes, pulsotype and phage type. Most of S. Typhimurium strains were pulsotype STYMXB.0147 (81.8%), phage type DT143 and resistant to sulfamethoxazole encoded by sul2. Two multidrug resistant (MDR) strains were identified. One strain, STYMXB.0061, was resistant to ampicillin (A), chloramphenicol (C), streptomycin (S), sulfamethoxazole (Su) and tetracycline (T) encoded by the Salmonella Genomic Island SGI1. The second MDR strain, STYMXB.0110, was resistant to SSuT encoded by sul1 and sul2, aadA1 and tet(C)-flanked by an IS26 element, respectively. The tet(C) gene has been reported to confer low levels of resistance and it has very rarely been detected in S. Typhimurium from poultry. In the current study, the MIC value (32 µg/mL) was consistent with the breakpoint (³16 µg/mL) reported for Enterobacteriaceae. Most of the S. Enteritidis strains were resistant to Su (encoded by sul2). One MDR strain (ANxSSuT) was identified. With the exception of nalidixic acid (Nx), the resistances were respectively encoded by blaTEM, strAB, sul2 and tet(A) harbored by an IncN conjugative plasmid. All isolates were pulsotype SENTXB.0001 with PT14b being the most prevalent identified phage type (57.1%). In Europe, SENTXB.0001 is the predominant PFGE profile from clinical cases and the identification of PT14b has steadily been on the increase since 2001. The findings presented in this study highlight the potential spread of S. Enteritidis phage types PT14b and S. Typhimurium DT143 in a field of particular relevance for zoonoses. Additional, the presence of resistance genes and genetic elements (conjugative plasmid and IS element) underlines the need to assess routinely studies in field, such as poultry farms, relevant fot the public health and suitable for the storage and diffusion of antimicrobial resistance.
Keywords: IncN; IS26; phage types; resistance genes; Salmonella enterica; tet(C)
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Camarda, A.; Pugliese, N.; Pupillo, A.; Oliva, M.; Circella, E.; Dionisi, A.M.; Ricci, A.; Legretto, M.; Caroli, A.; Pazzani, C. Resistance Genes, Phage Types and Pulsed Field Gel Electrophoresis Pulsotypes in Salmonella enterica Strains from Laying Hen Farms in Southern Italy. Int. J. Environ. Res. Public Health 2013, 10, 3347-3362.
Camarda A, Pugliese N, Pupillo A, Oliva M, Circella E, Dionisi AM, Ricci A, Legretto M, Caroli A, Pazzani C. Resistance Genes, Phage Types and Pulsed Field Gel Electrophoresis Pulsotypes in Salmonella enterica Strains from Laying Hen Farms in Southern Italy. International Journal of Environmental Research and Public Health. 2013; 10(8):3347-3362.
Camarda, Antonio; Pugliese, Nicola; Pupillo, Antonia; Oliva, Marta; Circella, Elena; Dionisi, Anna M.; Ricci, Antonia; Legretto, Marilisa; Caroli, Anna; Pazzani, Carlo. 2013. "Resistance Genes, Phage Types and Pulsed Field Gel Electrophoresis Pulsotypes in Salmonella enterica Strains from Laying Hen Farms in Southern Italy." Int. J. Environ. Res. Public Health 10, no. 8: 3347-3362.