The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain

Simon Le hello; Amany Bekhit; Sophie A. Granier; Himel Barua; Janine Beutlich; Magdalena Zając; Sebastian  Münch; Vitali Sintchenko; Brahim Bouchrif; Kayode  Fashae; Jean-Louis Pinsard; Lucile Sontag; Laetitia Fabre; Martine Garnier; Véronique Guibert; Peter Howard; Rene S. Hendriksen; Jens Peter Christensen; Paritosh K. Biswas; Axel Cloeckaert; Wolfgang Rabsch; Dariusz Wasyl; Benoit Doublet; François-Xavier Weill

doi:10.3389/fmicb.2013.00395

The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain

Simon Le hello, Amany Bekhit, Sophie A. Granier, Himel Barua, Janine Beutlich, Magdalena Zając, Sebastian Münch, Vitali Sintchenko, Brahim Bouchrif, Kayode Fashae, Jean-Louis Pinsard, Lucile Sontag, Laetitia Fabre, Martine Garnier, Véronique Guibert, Peter Howard, Rene S. Hendriksen, Jens Peter Christensen, Paritosh K. Biswas, Axel CloeckaertWolfgang Rabsch, Dariusz Wasyl, Benoit Doublet, François-Xavier Weill

79 Citations (Scopus)

Abstract

While the spread of Salmonella enterica serotype Kentucky resistant to ciprofloxacin across Africa and the Middle-East has been described recently, the presence of this strain in humans, food, various animal species (livestock, pets, and wildlife) and in environment is suspected in other countries of different continents. Here, we report results of an in-depth molecular epidemiological study on a global human and non-human collection of S. Kentucky (n = 70). We performed XbaI-pulsed field gel electrophoresis and multilocus sequence typing, assessed mutations in the quinolone resistance-determining regions, detected β-lactam resistance mechanisms, and screened the presence of the Salmonella genomic island 1 (SGI1). In this study, we highlight the rapid and extensive worldwide dissemination of the ciprofloxacin-resistant S. Kentucky ST198-X1-SGI1 strain since the mid-2000s in an increasingly large number of contaminated sources, including the environment. This strain has accumulated an increasing number of chromosomal and plasmid resistance determinants and has been identified in the Indian subcontinent, Southeast Asia and Europe since 2010. The second substitution at position 87 in GyrA (replacing the amino acid Asp) appeared helpful for epidemiological studies to track the origin of contamination. This global study provides evidence leading to the conclusion that high-level resistance to ciprofloxacin in S. Kentucky is a simple microbiological trait that facilitates the identification of the epidemic clone of interest, ST198-X1-SGI1. Taking this into account is essential in order to detect and monitor it easily and to take rapid measures in livestock to ensure control of this infection.

Original language	English
Article number	395
Journal	Frontiers in Microbiology
Volume	4
Number of pages	10
ISSN	1664-302X
DOIs	https://doi.org/10.3389/fmicb.2013.00395
Publication status	Published - 2013

Keywords

Faculty of Health and Medical Sciences

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10.3389/fmicb.2013.00395

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Le hello, S., Bekhit, A., A. Granier, S., Barua, H., Beutlich, J., Zając, M., Münch, S., Sintchenko, V., Bouchrif, B., Fashae, K., Pinsard, J-L., Sontag, L., Fabre, L., Garnier, M., Guibert, V., Howard, P., Hendriksen, R. S., Christensen, J. P., Biswas, P. K., ... Weill, F-X. (2013). The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Frontiers in Microbiology, 4, [395]. https://doi.org/10.3389/fmicb.2013.00395

Le hello, S, Bekhit, A, A. Granier, S, Barua, H, Beutlich, J, Zając, M, Münch, S, Sintchenko, V, Bouchrif, B, Fashae, K, Pinsard, J-L, Sontag, L, Fabre, L, Garnier, M, Guibert, V, Howard, P, Hendriksen, RS, Christensen, JP, Biswas, PK, Cloeckaert, A, Rabsch, W, Wasyl, D, Doublet, B & Weill, F-X 2013, 'The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain', Frontiers in Microbiology, vol. 4, 395. https://doi.org/10.3389/fmicb.2013.00395

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title = "The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain",

abstract = "While the spread of Salmonella enterica serotype Kentucky resistant to ciprofloxacin across Africa and the Middle-East has been described recently, the presence of this strain in humans, food, various animal species (livestock, pets, and wildlife) and in environment is suspected in other countries of different continents. Here, we report results of an in-depth molecular epidemiological study on a global human and non-human collection of S. Kentucky (n = 70). We performed XbaI-pulsed field gel electrophoresis and multilocus sequence typing, assessed mutations in the quinolone resistance-determining regions, detected β-lactam resistance mechanisms, and screened the presence of the Salmonella genomic island 1 (SGI1). In this study, we highlight the rapid and extensive worldwide dissemination of the ciprofloxacin-resistant S. Kentucky ST198-X1-SGI1 strain since the mid-2000s in an increasingly large number of contaminated sources, including the environment. This strain has accumulated an increasing number of chromosomal and plasmid resistance determinants and has been identified in the Indian subcontinent, Southeast Asia and Europe since 2010. The second substitution at position 87 in GyrA (replacing the amino acid Asp) appeared helpful for epidemiological studies to track the origin of contamination. This global study provides evidence leading to the conclusion that high-level resistance to ciprofloxacin in S. Kentucky is a simple microbiological trait that facilitates the identification of the epidemic clone of interest, ST198-X1-SGI1. Taking this into account is essential in order to detect and monitor it easily and to take rapid measures in livestock to ensure control of this infection.",

keywords = "Faculty of Health and Medical Sciences, S. Kentucky, ST198, SGI1, QRDR, MDR Salmonella dissemination, poultry",

author = "{Le hello}, Simon and Amany Bekhit and {A. Granier}, Sophie and Himel Barua and Janine Beutlich and Magdalena Zaj{\c a}c and Sebastian M{\"u}nch and Vitali Sintchenko and Brahim Bouchrif and Kayode Fashae and Jean-Louis Pinsard and Lucile Sontag and Laetitia Fabre and Martine Garnier and V{\'e}ronique Guibert and Peter Howard and Hendriksen, {Rene S.} and Christensen, {Jens Peter} and Biswas, {Paritosh K.} and Axel Cloeckaert and Wolfgang Rabsch and Dariusz Wasyl and Benoit Doublet and Fran{\c c}ois-Xavier Weill",

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doi = "10.3389/fmicb.2013.00395",

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journal = "Frontiers in Microbiology",

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T1 - The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain

AU - Le hello, Simon

AU - Bekhit, Amany

AU - A. Granier, Sophie

AU - Barua, Himel

AU - Beutlich, Janine

AU - Zając, Magdalena

AU - Münch, Sebastian

AU - Sintchenko, Vitali

AU - Bouchrif, Brahim

AU - Fashae, Kayode

AU - Pinsard, Jean-Louis

AU - Sontag, Lucile

AU - Fabre, Laetitia

AU - Garnier, Martine

AU - Guibert, Véronique

AU - Howard, Peter

AU - Hendriksen, Rene S.

AU - Christensen, Jens Peter

AU - Biswas, Paritosh K.

AU - Cloeckaert, Axel

AU - Rabsch, Wolfgang

AU - Wasyl, Dariusz

AU - Doublet, Benoit

AU - Weill, François-Xavier

PY - 2013

Y1 - 2013

N2 - While the spread of Salmonella enterica serotype Kentucky resistant to ciprofloxacin across Africa and the Middle-East has been described recently, the presence of this strain in humans, food, various animal species (livestock, pets, and wildlife) and in environment is suspected in other countries of different continents. Here, we report results of an in-depth molecular epidemiological study on a global human and non-human collection of S. Kentucky (n = 70). We performed XbaI-pulsed field gel electrophoresis and multilocus sequence typing, assessed mutations in the quinolone resistance-determining regions, detected β-lactam resistance mechanisms, and screened the presence of the Salmonella genomic island 1 (SGI1). In this study, we highlight the rapid and extensive worldwide dissemination of the ciprofloxacin-resistant S. Kentucky ST198-X1-SGI1 strain since the mid-2000s in an increasingly large number of contaminated sources, including the environment. This strain has accumulated an increasing number of chromosomal and plasmid resistance determinants and has been identified in the Indian subcontinent, Southeast Asia and Europe since 2010. The second substitution at position 87 in GyrA (replacing the amino acid Asp) appeared helpful for epidemiological studies to track the origin of contamination. This global study provides evidence leading to the conclusion that high-level resistance to ciprofloxacin in S. Kentucky is a simple microbiological trait that facilitates the identification of the epidemic clone of interest, ST198-X1-SGI1. Taking this into account is essential in order to detect and monitor it easily and to take rapid measures in livestock to ensure control of this infection.

AB - While the spread of Salmonella enterica serotype Kentucky resistant to ciprofloxacin across Africa and the Middle-East has been described recently, the presence of this strain in humans, food, various animal species (livestock, pets, and wildlife) and in environment is suspected in other countries of different continents. Here, we report results of an in-depth molecular epidemiological study on a global human and non-human collection of S. Kentucky (n = 70). We performed XbaI-pulsed field gel electrophoresis and multilocus sequence typing, assessed mutations in the quinolone resistance-determining regions, detected β-lactam resistance mechanisms, and screened the presence of the Salmonella genomic island 1 (SGI1). In this study, we highlight the rapid and extensive worldwide dissemination of the ciprofloxacin-resistant S. Kentucky ST198-X1-SGI1 strain since the mid-2000s in an increasingly large number of contaminated sources, including the environment. This strain has accumulated an increasing number of chromosomal and plasmid resistance determinants and has been identified in the Indian subcontinent, Southeast Asia and Europe since 2010. The second substitution at position 87 in GyrA (replacing the amino acid Asp) appeared helpful for epidemiological studies to track the origin of contamination. This global study provides evidence leading to the conclusion that high-level resistance to ciprofloxacin in S. Kentucky is a simple microbiological trait that facilitates the identification of the epidemic clone of interest, ST198-X1-SGI1. Taking this into account is essential in order to detect and monitor it easily and to take rapid measures in livestock to ensure control of this infection.

KW - Faculty of Health and Medical Sciences

KW - S. Kentucky

KW - ST198

KW - SGI1

KW - QRDR

KW - MDR Salmonella dissemination

KW - poultry

U2 - 10.3389/fmicb.2013.00395

DO - 10.3389/fmicb.2013.00395

M3 - Journal article

C2 - 24385975

SN - 1664-302X

VL - 4

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

M1 - 395

ER -

The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain

Abstract

Keywords

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