Incidence and Genomic Background of Antibiotic Resistance in Food-Borne and Clinical Isolates of <i>Salmonella enterica</i> Serovar Derby from Spain

<i>Salmonella enterica</i> serovar Derby (<i>S</i>. Derby) ranks fifth among nontyphoidal <i>Salmonella</i> serovars causing human infections in the European Union. <i>S</i>. Derby isolates (36) collected between 2006 and 2018 in a Spanish region (Astu...

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Main Authors: Xenia Vázquez, Raquel García-Fierro, Javier Fernández, Margarita Bances, Ana Herrero-Fresno, John E. Olsen, Rosaura Rodicio, Víctor Ladero, Vanesa García, M. Rosario Rodicio
Format: Article
Language:English
Published: MDPI AG 2023-07-01
Series:Antibiotics
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Online Access:https://www.mdpi.com/2079-6382/12/7/1204
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author Xenia Vázquez
Raquel García-Fierro
Javier Fernández
Margarita Bances
Ana Herrero-Fresno
John E. Olsen
Rosaura Rodicio
Víctor Ladero
Vanesa García
M. Rosario Rodicio
author_facet Xenia Vázquez
Raquel García-Fierro
Javier Fernández
Margarita Bances
Ana Herrero-Fresno
John E. Olsen
Rosaura Rodicio
Víctor Ladero
Vanesa García
M. Rosario Rodicio
author_sort Xenia Vázquez
collection DOAJ
description <i>Salmonella enterica</i> serovar Derby (<i>S</i>. Derby) ranks fifth among nontyphoidal <i>Salmonella</i> serovars causing human infections in the European Union. <i>S</i>. Derby isolates (36) collected between 2006 and 2018 in a Spanish region (Asturias) from human clinical samples (20) as well as from pig carcasses, pork- or pork and beef-derived products, or wild boar (16) were phenotypically characterized with regard to resistance, and 22 (12 derived from humans and 10 from food-related samples) were also subjected to whole genome sequence analysis. The sequenced isolates belonged to ST40, a common <i>S</i>. Derby sequence type, and were positive for SPI-23, a <i>Salmonella</i> pathogenicity island involved in adherence and invasion of the porcine jejune enterocytes. Isolates were either susceptible (30.6%), or resistant to one or more of the 19 antibiotics tested for (69.4%). Resistances to tetracycline [<i>tet</i>(A), <i>tet</i>(B) and <i>tet</i>(C)], streptomycin (<i>aadA2</i>), sulfonamides (<i>sul1</i>), nalidixic acid [<i>gyrA</i> (Asp87 to Asn)] and ampicillin (<i>bla</i><sub>TEM-1</sub>-like) were detected, with frequencies ranging from 8.3% to 66.7%, and were higher in clinical than in food-borne isolates. The <i>fosA7.3</i> gene was present in all sequenced isolates. The most common phenotype was that conferred by the <i>tet</i>(A), <i>aadA2</i> and <i>sul1</i> genes, located within identical or closely related variants of <i>Salmonella</i> Genomic Island 1 (SGI1), where mercury resistance genes were also present. Diverse IncI1-I(α) plasmids belonging to distinct STs provided antibiotic [<i>bla</i><sub>TEM-1</sub>, <i>tet</i>(A) and/or <i>tet</i>(B)] and heavy metal resistance genes (copper and silver), while small pSC101-like plasmids carried <i>tet</i>(C). Regardless of their location, most resistance genes were associated with genetic elements involved in DNA mobility, including a class one integron, multiple insertion sequences and several intact or truncated transposons. By phylogenetic analysis, the isolates were distributed into two distinct clades, both including food-borne and clinical isolates. One of these clades included all SGI1-like positive isolates, which were found in both kinds of samples throughout the entire period of study. Although the frequency of <i>S</i>. Derby in Asturias was very low (0.5% and 3.1% of the total clinical and food isolates of <i>S. enterica</i> recovered along the period of study), it still represents a burden to human health linked to transmission across the food chain. The information generated in the present study can support further epidemiological surveillance aimed to control this zoonotic pathogen.
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spelling doaj.art-92395d3eef034a0fb33fb9d5c675f1b12023-11-18T18:03:44ZengMDPI AGAntibiotics2079-63822023-07-01127120410.3390/antibiotics12071204Incidence and Genomic Background of Antibiotic Resistance in Food-Borne and Clinical Isolates of <i>Salmonella enterica</i> Serovar Derby from SpainXenia Vázquez0Raquel García-Fierro1Javier Fernández2Margarita Bances3Ana Herrero-Fresno4John E. Olsen5Rosaura Rodicio6Víctor Ladero7Vanesa García8M. Rosario Rodicio9Departamento de Biología Funcional, Área de Microbiología, Universidad de Oviedo (UO), 33006 Oviedo, SpainDepartamento de Biología Funcional, Área de Microbiología, Universidad de Oviedo (UO), 33006 Oviedo, SpainGrupo de Microbiología Traslacional, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), 33011 Oviedo, SpainLaboratorio de Salud Pública, Dirección General de Salud Pública, Consejería de Salud del Principado de Asturias, 33011 Oviedo, SpainDepartment of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg, DenmarkDepartment of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg, DenmarkGrupo de Microbiología Traslacional, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), 33011 Oviedo, SpainInstituto de Productos Lácteos de Asturias (IPLA), Consejo Superior de Investigaciones Científicas (CSIC), 33300 Villaviciosa, SpainLaboratorio de Referencia de Escherichia coli (LREC), Departamento de Microbioloxía e Parasitoloxía, Facultade de Veterinaria, Campus Terra, Universidade de Santiago de Compostela, 27002 Lugo, SpainDepartamento de Biología Funcional, Área de Microbiología, Universidad de Oviedo (UO), 33006 Oviedo, Spain<i>Salmonella enterica</i> serovar Derby (<i>S</i>. Derby) ranks fifth among nontyphoidal <i>Salmonella</i> serovars causing human infections in the European Union. <i>S</i>. Derby isolates (36) collected between 2006 and 2018 in a Spanish region (Asturias) from human clinical samples (20) as well as from pig carcasses, pork- or pork and beef-derived products, or wild boar (16) were phenotypically characterized with regard to resistance, and 22 (12 derived from humans and 10 from food-related samples) were also subjected to whole genome sequence analysis. The sequenced isolates belonged to ST40, a common <i>S</i>. Derby sequence type, and were positive for SPI-23, a <i>Salmonella</i> pathogenicity island involved in adherence and invasion of the porcine jejune enterocytes. Isolates were either susceptible (30.6%), or resistant to one or more of the 19 antibiotics tested for (69.4%). Resistances to tetracycline [<i>tet</i>(A), <i>tet</i>(B) and <i>tet</i>(C)], streptomycin (<i>aadA2</i>), sulfonamides (<i>sul1</i>), nalidixic acid [<i>gyrA</i> (Asp87 to Asn)] and ampicillin (<i>bla</i><sub>TEM-1</sub>-like) were detected, with frequencies ranging from 8.3% to 66.7%, and were higher in clinical than in food-borne isolates. The <i>fosA7.3</i> gene was present in all sequenced isolates. The most common phenotype was that conferred by the <i>tet</i>(A), <i>aadA2</i> and <i>sul1</i> genes, located within identical or closely related variants of <i>Salmonella</i> Genomic Island 1 (SGI1), where mercury resistance genes were also present. Diverse IncI1-I(α) plasmids belonging to distinct STs provided antibiotic [<i>bla</i><sub>TEM-1</sub>, <i>tet</i>(A) and/or <i>tet</i>(B)] and heavy metal resistance genes (copper and silver), while small pSC101-like plasmids carried <i>tet</i>(C). Regardless of their location, most resistance genes were associated with genetic elements involved in DNA mobility, including a class one integron, multiple insertion sequences and several intact or truncated transposons. By phylogenetic analysis, the isolates were distributed into two distinct clades, both including food-borne and clinical isolates. One of these clades included all SGI1-like positive isolates, which were found in both kinds of samples throughout the entire period of study. Although the frequency of <i>S</i>. Derby in Asturias was very low (0.5% and 3.1% of the total clinical and food isolates of <i>S. enterica</i> recovered along the period of study), it still represents a burden to human health linked to transmission across the food chain. The information generated in the present study can support further epidemiological surveillance aimed to control this zoonotic pathogen.https://www.mdpi.com/2079-6382/12/7/1204<i>Salmonella enterica</i> serovar DerbyST40SPI-23antimicrobial drug resistance<i>fosA7.3</i>SGI1-like
spellingShingle Xenia Vázquez
Raquel García-Fierro
Javier Fernández
Margarita Bances
Ana Herrero-Fresno
John E. Olsen
Rosaura Rodicio
Víctor Ladero
Vanesa García
M. Rosario Rodicio
Incidence and Genomic Background of Antibiotic Resistance in Food-Borne and Clinical Isolates of <i>Salmonella enterica</i> Serovar Derby from Spain
Antibiotics
<i>Salmonella enterica</i> serovar Derby
ST40
SPI-23
antimicrobial drug resistance
<i>fosA7.3</i>
SGI1-like
title Incidence and Genomic Background of Antibiotic Resistance in Food-Borne and Clinical Isolates of <i>Salmonella enterica</i> Serovar Derby from Spain
title_full Incidence and Genomic Background of Antibiotic Resistance in Food-Borne and Clinical Isolates of <i>Salmonella enterica</i> Serovar Derby from Spain
title_fullStr Incidence and Genomic Background of Antibiotic Resistance in Food-Borne and Clinical Isolates of <i>Salmonella enterica</i> Serovar Derby from Spain
title_full_unstemmed Incidence and Genomic Background of Antibiotic Resistance in Food-Borne and Clinical Isolates of <i>Salmonella enterica</i> Serovar Derby from Spain
title_short Incidence and Genomic Background of Antibiotic Resistance in Food-Borne and Clinical Isolates of <i>Salmonella enterica</i> Serovar Derby from Spain
title_sort incidence and genomic background of antibiotic resistance in food borne and clinical isolates of i salmonella enterica i serovar derby from spain
topic <i>Salmonella enterica</i> serovar Derby
ST40
SPI-23
antimicrobial drug resistance
<i>fosA7.3</i>
SGI1-like
url https://www.mdpi.com/2079-6382/12/7/1204
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