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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. and Eibach, Daniel (2019): Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana.
In: PLOS Neglected Tropical Diseases 13(6), e0007485 [PDF, 1MB]


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. Author summary Salmonella enterica serovar Enteritidis is both a prominent global cause of zoonotic gastroenteritis, in association with the industrial production of eggs and poultry, and of bloodstream-invasive infection in sub-Saharan Africa, a clinical syndrome referred to as invasive nontyphoidal Salmonella (iNTS) disease. African epidemic iNTS strains are frequently multi-drug resistant, leaving fluoroquinolone antibiotics as key agents in reducing iNTS-associated morbidity and mortality. We analysed the genomes of S. Enteritidis collected in Ghana from patients with iNTS disease to investigate the emergence of fluoroquinolone resistance in the region. Extensive phylogenetic diversity was present, however, fluoroquinolone resistance was confined to a single clade causing global epidemics of poultry-associated gastroenteritis. This resistance has predominantly emerged locally, rather than being imported. We found that antimicrobial resistance patterns differed by S. Enteritidis clade, highlighting the challenges of devising empirical sepsis treatment guidelines in the absence of diagnostic microbiology facilities to monitor changes in resistance profiles. Furthermore, we detected fluoroquinolone resistance in closely related poultry and human isolates, suggesting a role of antimicrobial use within the growing local poultry industry in driving the emergence of resistance and a need for surveillance measures within this industry to protect a human population at high risk of iNTS disease.

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