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Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana

BACKGROUND: Salmonella enterica serovar Enteritidis is a cause of both poultry- and egg-associated enterocolitis globally and bloodstream-invasive nontyphoidal Salmonella (iNTS) disease in sub-Saharan Africa (sSA). Distinct, multi-drug resistant genotypes associated with iNTS disease in sSA have rec...

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Autores principales: Aldrich, Cassandra, Hartman, Hassan, Feasey, Nicholas, Chattaway, Marie Anne, Dekker, Denise, Al-Emran, Hassan M., Larkin, Lesley, McCormick, Jacquelyn, Sarpong, Nimako, Le Hello, Simon, Adu-Sarkodie, Yaw, Panzner, Ursula, Park, Se Eun, Im, Justin, Marks, Florian, May, Jürgen, Dallman, Timothy J., Eibach, Daniel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6605661/
https://www.ncbi.nlm.nih.gov/pubmed/31220112
http://dx.doi.org/10.1371/journal.pntd.0007485
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author Aldrich, Cassandra
Hartman, Hassan
Feasey, Nicholas
Chattaway, Marie Anne
Dekker, Denise
Al-Emran, Hassan M.
Larkin, Lesley
McCormick, Jacquelyn
Sarpong, Nimako
Le Hello, Simon
Adu-Sarkodie, Yaw
Panzner, Ursula
Park, Se Eun
Im, Justin
Marks, Florian
May, Jürgen
Dallman, Timothy J.
Eibach, Daniel
author_facet Aldrich, Cassandra
Hartman, Hassan
Feasey, Nicholas
Chattaway, Marie Anne
Dekker, Denise
Al-Emran, Hassan M.
Larkin, Lesley
McCormick, Jacquelyn
Sarpong, Nimako
Le Hello, Simon
Adu-Sarkodie, Yaw
Panzner, Ursula
Park, Se Eun
Im, Justin
Marks, Florian
May, Jürgen
Dallman, Timothy J.
Eibach, Daniel
author_sort Aldrich, Cassandra
collection PubMed
description BACKGROUND: Salmonella enterica serovar Enteritidis is a cause of both poultry- and egg-associated enterocolitis globally and bloodstream-invasive nontyphoidal Salmonella (iNTS) disease in sub-Saharan Africa (sSA). Distinct, multi-drug resistant genotypes associated with iNTS disease in sSA have recently been described, often requiring treatment with fluoroquinolone antibiotics. In industrialised countries, antimicrobial use in poultry production has led to frequent fluoroquinolone resistance amongst globally prevalent enterocolitis-associated lineages. METHODOLOGY/PRINCIPAL FINDINGS: Twenty seven S. Enteritidis isolates from patients with iNTS disease and two poultry isolates, collected between 2007 and 2015 in the Ashanti region of Ghana, were whole-genome sequenced. These isolates, notable for a high rate of diminished ciprofloxacin susceptibility (DCS), were placed in the phyletic context of 1,067 sequences from the Public Health England (PHE) S. Enteritidis genome database to understand whether DCS was associated with African or globally-circulating clades of S. Enteritidis. Analysis showed four of the major S. Enteritidis clades were represented, two global and two African. All thirteen DCS isolates, containing a single gyrA mutation at codon 87, belonged to a global PT4-like clade responsible for epidemics of poultry-associated enterocolitis. Apart from two DCS isolates, which clustered with PHE isolates associated with travel to Spain and Brazil, the remaining DCS isolates, including one poultry isolate, belonged to two monophyletic clusters in which gyrA 87 mutations appear to have developed within the region. CONCLUSIONS/SIGNIFICANCE: Extensive phylogenetic diversity is evident amongst iNTS disease-associated S. Enteritidis in Ghana. Antimicrobial resistance profiles differed by clade, highlighting the challenges of devising empirical sepsis guidelines. The detection of fluoroquinolone resistance in phyletically-related poultry and human isolates is of major concern and surveillance and control measures within the region’s burgeoning poultry industry are required to protect a human population at high risk of iNTS disease.
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spelling pubmed-66056612019-07-12 Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana Aldrich, Cassandra Hartman, Hassan Feasey, Nicholas Chattaway, Marie Anne Dekker, Denise Al-Emran, Hassan M. Larkin, Lesley McCormick, Jacquelyn Sarpong, Nimako Le Hello, Simon Adu-Sarkodie, Yaw Panzner, Ursula Park, Se Eun Im, Justin Marks, Florian May, Jürgen Dallman, Timothy J. Eibach, Daniel PLoS Negl Trop Dis Research Article BACKGROUND: Salmonella enterica serovar Enteritidis is a cause of both poultry- and egg-associated enterocolitis globally and bloodstream-invasive nontyphoidal Salmonella (iNTS) disease in sub-Saharan Africa (sSA). Distinct, multi-drug resistant genotypes associated with iNTS disease in sSA have recently been described, often requiring treatment with fluoroquinolone antibiotics. In industrialised countries, antimicrobial use in poultry production has led to frequent fluoroquinolone resistance amongst globally prevalent enterocolitis-associated lineages. METHODOLOGY/PRINCIPAL FINDINGS: Twenty seven S. Enteritidis isolates from patients with iNTS disease and two poultry isolates, collected between 2007 and 2015 in the Ashanti region of Ghana, were whole-genome sequenced. These isolates, notable for a high rate of diminished ciprofloxacin susceptibility (DCS), were placed in the phyletic context of 1,067 sequences from the Public Health England (PHE) S. Enteritidis genome database to understand whether DCS was associated with African or globally-circulating clades of S. Enteritidis. Analysis showed four of the major S. Enteritidis clades were represented, two global and two African. All thirteen DCS isolates, containing a single gyrA mutation at codon 87, belonged to a global PT4-like clade responsible for epidemics of poultry-associated enterocolitis. Apart from two DCS isolates, which clustered with PHE isolates associated with travel to Spain and Brazil, the remaining DCS isolates, including one poultry isolate, belonged to two monophyletic clusters in which gyrA 87 mutations appear to have developed within the region. CONCLUSIONS/SIGNIFICANCE: Extensive phylogenetic diversity is evident amongst iNTS disease-associated S. Enteritidis in Ghana. Antimicrobial resistance profiles differed by clade, highlighting the challenges of devising empirical sepsis guidelines. The detection of fluoroquinolone resistance in phyletically-related poultry and human isolates is of major concern and surveillance and control measures within the region’s burgeoning poultry industry are required to protect a human population at high risk of iNTS disease. Public Library of Science 2019-06-20 /pmc/articles/PMC6605661/ /pubmed/31220112 http://dx.doi.org/10.1371/journal.pntd.0007485 Text en © 2019 Aldrich et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Aldrich, Cassandra
Hartman, Hassan
Feasey, Nicholas
Chattaway, Marie Anne
Dekker, Denise
Al-Emran, Hassan M.
Larkin, Lesley
McCormick, Jacquelyn
Sarpong, Nimako
Le Hello, Simon
Adu-Sarkodie, Yaw
Panzner, Ursula
Park, Se Eun
Im, Justin
Marks, Florian
May, Jürgen
Dallman, Timothy J.
Eibach, Daniel
Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana
title Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana
title_full Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana
title_fullStr Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana
title_full_unstemmed Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana
title_short Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana
title_sort emergence of phylogenetically diverse and fluoroquinolone resistant salmonella enteritidis as a cause of invasive nontyphoidal salmonella disease in ghana
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6605661/
https://www.ncbi.nlm.nih.gov/pubmed/31220112
http://dx.doi.org/10.1371/journal.pntd.0007485
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