The genomic epidemiology of multi-drug resistant invasive non-typhoidal Salmonella in selected sub-Saharan African countries

Se Eun Park; Duy Thanh Pham; Gi Deok Pak; Ursula Panzner; Ligia Maria Cruz Espinoza; Vera von Kalckreuth; Justin Im; Ondari D Mogeni; Heidi Schütt-Gerowitt; John A Crump; Robert F Breiman; Yaw Adu-Sarkodie; Ellis Owusu-Dabo; Raphaël Rakotozandrindrainy; Abdramane Bassiahi Soura; Abraham Aseffa; Nagla Gasmelseed; Arvinda Sooka; Karen H Keddy; Jürgen May; Peter Aaby; Holly M Biggs; Julian T Hertz; Joel M Montgomery; Leonard Cosmas; Beatrice Olack; Barry Fields; Nimako Sarpong; Tsiriniaina Jean Luco Razafindrabe; Tiana Mirana Raminosoa; Leon Parfait Kabore; Emmanuel Sampo; Mekonnen Teferi; Biruk Yeshitela; Muna Ahmed El Tayeb; Ralf Krumkamp; Denise Myriam Dekker; Anna Jaeger; Adama Tall; Amy Gassama; Aissatou Niang; Morten Bjerregaard-Andersen; Sandra Valborg Løfberg; Jessica Fung Deerin; Jin Kyung Park; Frank Konings; Megan E Carey; Sandra Van Puyvelde; Mohammad Ali; John Clemens; Gordon Dougan; Stephen Baker; Florian Marks

doi:10.1136/bmjgh-2021-005659

The genomic epidemiology of multi-drug resistant invasive non-typhoidal Salmonella in selected sub-Saharan African countries

Se Eun Park, Duy Thanh Pham, Gi Deok Pak, Ursula Panzner, Ligia Maria Cruz Espinoza, Vera von Kalckreuth, Justin Im, Ondari D Mogeni, Heidi Schütt-Gerowitt, John A Crump, Robert F Breiman, Yaw Adu-Sarkodie, Ellis Owusu-Dabo, Raphaël Rakotozandrindrainy, Abdramane Bassiahi Soura, Abraham Aseffa, Nagla Gasmelseed, Arvinda Sooka, Karen H Keddy, Jürgen MayPeter Aaby, Holly M Biggs, Julian T Hertz, Joel M Montgomery, Leonard Cosmas, Beatrice Olack, Barry Fields, Nimako Sarpong, Tsiriniaina Jean Luco Razafindrabe, Tiana Mirana Raminosoa, Leon Parfait Kabore, Emmanuel Sampo, Mekonnen Teferi, Biruk Yeshitela, Muna Ahmed El Tayeb, Ralf Krumkamp, Denise Myriam Dekker, Anna Jaeger, Adama Tall, Amy Gassama, Aissatou Niang, Morten Bjerregaard-Andersen, Sandra Valborg Løfberg, Jessica Fung Deerin, Jin Kyung Park, Frank Konings, Megan E Carey, Sandra Van Puyvelde, Mohammad Ali, John Clemens, Gordon Dougan, Stephen Baker, Florian Marks

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Abstract

BACKGROUND: Invasive non-typhoidal Salmonella (iNTS) is one of the leading causes of bacteraemia in sub-Saharan Africa. We aimed to provide a better understanding of the genetic characteristics and transmission patterns associated with multi-drug resistant (MDR) iNTS serovars across the continent.

METHODS: A total of 166 iNTS isolates collected from a multi-centre surveillance in 10 African countries (2010-2014) and a fever study in Ghana (2007-2009) were genome sequenced to investigate the geographical distribution, antimicrobial genetic determinants and population structure of iNTS serotypes-genotypes. Phylogenetic analyses were conducted in the context of the existing genomic frameworks for various iNTS serovars. Population-based incidence of MDR-iNTS disease was estimated in each study site.

RESULTS: Salmonella Typhimurium sequence-type (ST) 313 and Salmonella Enteritidis ST11 were predominant, and both exhibited high frequencies of MDR; Salmonella Dublin ST10 was identified in West Africa only. Mutations in the gyrA gene (fluoroquinolone resistance) were identified in S. Enteritidis and S. Typhimurium in Ghana; an ST313 isolate carrying bla CTX-M-15 was found in Kenya. International transmission of MDR ST313 (lineage II) and MDR ST11 (West African clade) was observed between Ghana and neighbouring West African countries. The incidence of MDR-iNTS disease exceeded 100/100 000 person-years-of-observation in children aged <5 years in several West African countries.

CONCLUSIONS: We identified the circulation of multiple MDR iNTS serovar STs in the sampled sub-Saharan African countries. Investment in the development and deployment of iNTS vaccines coupled with intensified antimicrobial resistance surveillance are essential to limit the impact of these pathogens in Africa.

Original language	English
Article number	e005659
Journal	BMJ Global Health
Volume	6
Issue number	8
Number of pages	27
ISSN	2059-7908
DOIs	https://doi.org/10.1136/bmjgh-2021-005659
Publication status	Published - 2021

Keywords

Child
Genomics
Humans
Kenya
Pharmaceutical Preparations
Phylogeny
Salmonella typhimurium/genetics

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10.1136/bmjgh-2021-005659Licence: CC BY-NC

2021bghee005659Final published version, 1.6 MBLicence: CC BY-NC

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Park, S. E., Pham, D. T., Pak, G. D., Panzner, U., Maria Cruz Espinoza, L., von Kalckreuth, V., Im, J., Mogeni, O. D., Schütt-Gerowitt, H., Crump, J. A., Breiman, R. F., Adu-Sarkodie, Y., Owusu-Dabo, E., Rakotozandrindrainy, R., Bassiahi Soura, A., Aseffa, A., Gasmelseed, N., Sooka, A., Keddy, K. H., ... Marks, F. (2021). The genomic epidemiology of multi-drug resistant invasive non-typhoidal Salmonella in selected sub-Saharan African countries. BMJ Global Health , 6(8), Article e005659. https://doi.org/10.1136/bmjgh-2021-005659

@article{150e861ec82142658eded93b95d1912c,

title = "The genomic epidemiology of multi-drug resistant invasive non-typhoidal Salmonella in selected sub-Saharan African countries",

abstract = "BACKGROUND: Invasive non-typhoidal Salmonella (iNTS) is one of the leading causes of bacteraemia in sub-Saharan Africa. We aimed to provide a better understanding of the genetic characteristics and transmission patterns associated with multi-drug resistant (MDR) iNTS serovars across the continent.METHODS: A total of 166 iNTS isolates collected from a multi-centre surveillance in 10 African countries (2010-2014) and a fever study in Ghana (2007-2009) were genome sequenced to investigate the geographical distribution, antimicrobial genetic determinants and population structure of iNTS serotypes-genotypes. Phylogenetic analyses were conducted in the context of the existing genomic frameworks for various iNTS serovars. Population-based incidence of MDR-iNTS disease was estimated in each study site.RESULTS: Salmonella Typhimurium sequence-type (ST) 313 and Salmonella Enteritidis ST11 were predominant, and both exhibited high frequencies of MDR; Salmonella Dublin ST10 was identified in West Africa only. Mutations in the gyrA gene (fluoroquinolone resistance) were identified in S. Enteritidis and S. Typhimurium in Ghana; an ST313 isolate carrying bla CTX-M-15 was found in Kenya. International transmission of MDR ST313 (lineage II) and MDR ST11 (West African clade) was observed between Ghana and neighbouring West African countries. The incidence of MDR-iNTS disease exceeded 100/100 000 person-years-of-observation in children aged <5 years in several West African countries.CONCLUSIONS: We identified the circulation of multiple MDR iNTS serovar STs in the sampled sub-Saharan African countries. Investment in the development and deployment of iNTS vaccines coupled with intensified antimicrobial resistance surveillance are essential to limit the impact of these pathogens in Africa.",

keywords = "Child, Genomics, Humans, Kenya, Pharmaceutical Preparations, Phylogeny, Salmonella typhimurium/genetics",

author = "Park, {Se Eun} and Pham, {Duy Thanh} and Pak, {Gi Deok} and Ursula Panzner and {Maria Cruz Espinoza}, Ligia and {von Kalckreuth}, Vera and Justin Im and Mogeni, {Ondari D} and Heidi Sch{\"u}tt-Gerowitt and Crump, {John A} and Breiman, {Robert F} and Yaw Adu-Sarkodie and Ellis Owusu-Dabo and Rapha{\"e}l Rakotozandrindrainy and {Bassiahi Soura}, Abdramane and Abraham Aseffa and Nagla Gasmelseed and Arvinda Sooka and Keddy, {Karen H} and J{\"u}rgen May and Peter Aaby and Biggs, {Holly M} and Hertz, {Julian T} and Montgomery, {Joel M} and Leonard Cosmas and Beatrice Olack and Barry Fields and Nimako Sarpong and Razafindrabe, {Tsiriniaina Jean Luco} and Raminosoa, {Tiana Mirana} and Kabore, {Leon Parfait} and Emmanuel Sampo and Mekonnen Teferi and Biruk Yeshitela and {El Tayeb}, {Muna Ahmed} and Ralf Krumkamp and Dekker, {Denise Myriam} and Anna Jaeger and Adama Tall and Amy Gassama and Aissatou Niang and Morten Bjerregaard-Andersen and L{\o}fberg, {Sandra Valborg} and Deerin, {Jessica Fung} and Park, {Jin Kyung} and Frank Konings and Carey, {Megan E} and {Van Puyvelde}, Sandra and Mohammad Ali and John Clemens and Gordon Dougan and Stephen Baker and Florian Marks",

note = "FTX; DOAJ; (CC BY-NC 4.0); {\textcopyright} Author(s) (or their employer(s)) 2021. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.",

year = "2021",

doi = "10.1136/bmjgh-2021-005659",

language = "English",

volume = "6",

journal = "BMJ Global Health ",

issn = "2059-7908",

publisher = "BMJ Publishing Group",

number = "8",

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Park, SE, Pham, DT, Pak, GD, Panzner, U, Maria Cruz Espinoza, L, von Kalckreuth, V, Im, J, Mogeni, OD, Schütt-Gerowitt, H, Crump, JA, Breiman, RF, Adu-Sarkodie, Y, Owusu-Dabo, E, Rakotozandrindrainy, R, Bassiahi Soura, A, Aseffa, A, Gasmelseed, N, Sooka, A, Keddy, KH, May, J, Aaby, P, Biggs, HM, Hertz, JT, Montgomery, JM, Cosmas, L, Olack, B, Fields, B, Sarpong, N, Razafindrabe, TJL, Raminosoa, TM, Kabore, LP, Sampo, E, Teferi, M, Yeshitela, B, El Tayeb, MA, Krumkamp, R, Dekker, DM, Jaeger, A, Tall, A, Gassama, A, Niang, A, Bjerregaard-Andersen, M, Løfberg, SV, Deerin, JF, Park, JK, Konings, F, Carey, ME, Van Puyvelde, S, Ali, M, Clemens, J, Dougan, G, Baker, S & Marks, F 2021, 'The genomic epidemiology of multi-drug resistant invasive non-typhoidal Salmonella in selected sub-Saharan African countries', BMJ Global Health , vol. 6, no. 8, e005659. https://doi.org/10.1136/bmjgh-2021-005659

TY - JOUR

T1 - The genomic epidemiology of multi-drug resistant invasive non-typhoidal Salmonella in selected sub-Saharan African countries

AU - Park, Se Eun

AU - Pham, Duy Thanh

AU - Pak, Gi Deok

AU - Panzner, Ursula

AU - Maria Cruz Espinoza, Ligia

AU - von Kalckreuth, Vera

AU - Im, Justin

AU - Mogeni, Ondari D

AU - Schütt-Gerowitt, Heidi

AU - Crump, John A

AU - Breiman, Robert F

AU - Adu-Sarkodie, Yaw

AU - Owusu-Dabo, Ellis

AU - Rakotozandrindrainy, Raphaël

AU - Bassiahi Soura, Abdramane

AU - Aseffa, Abraham

AU - Gasmelseed, Nagla

AU - Sooka, Arvinda

AU - Keddy, Karen H

AU - May, Jürgen

AU - Aaby, Peter

AU - Biggs, Holly M

AU - Hertz, Julian T

AU - Montgomery, Joel M

AU - Cosmas, Leonard

AU - Olack, Beatrice

AU - Fields, Barry

AU - Sarpong, Nimako

AU - Razafindrabe, Tsiriniaina Jean Luco

AU - Raminosoa, Tiana Mirana

AU - Kabore, Leon Parfait

AU - Sampo, Emmanuel

AU - Teferi, Mekonnen

AU - Yeshitela, Biruk

AU - El Tayeb, Muna Ahmed

AU - Krumkamp, Ralf

AU - Dekker, Denise Myriam

AU - Jaeger, Anna

AU - Tall, Adama

AU - Gassama, Amy

AU - Niang, Aissatou

AU - Bjerregaard-Andersen, Morten

AU - Løfberg, Sandra Valborg

AU - Deerin, Jessica Fung

AU - Park, Jin Kyung

AU - Konings, Frank

AU - Carey, Megan E

AU - Van Puyvelde, Sandra

AU - Ali, Mohammad

AU - Clemens, John

AU - Dougan, Gordon

AU - Baker, Stephen

AU - Marks, Florian

PY - 2021

Y1 - 2021

N2 - BACKGROUND: Invasive non-typhoidal Salmonella (iNTS) is one of the leading causes of bacteraemia in sub-Saharan Africa. We aimed to provide a better understanding of the genetic characteristics and transmission patterns associated with multi-drug resistant (MDR) iNTS serovars across the continent.METHODS: A total of 166 iNTS isolates collected from a multi-centre surveillance in 10 African countries (2010-2014) and a fever study in Ghana (2007-2009) were genome sequenced to investigate the geographical distribution, antimicrobial genetic determinants and population structure of iNTS serotypes-genotypes. Phylogenetic analyses were conducted in the context of the existing genomic frameworks for various iNTS serovars. Population-based incidence of MDR-iNTS disease was estimated in each study site.RESULTS: Salmonella Typhimurium sequence-type (ST) 313 and Salmonella Enteritidis ST11 were predominant, and both exhibited high frequencies of MDR; Salmonella Dublin ST10 was identified in West Africa only. Mutations in the gyrA gene (fluoroquinolone resistance) were identified in S. Enteritidis and S. Typhimurium in Ghana; an ST313 isolate carrying bla CTX-M-15 was found in Kenya. International transmission of MDR ST313 (lineage II) and MDR ST11 (West African clade) was observed between Ghana and neighbouring West African countries. The incidence of MDR-iNTS disease exceeded 100/100 000 person-years-of-observation in children aged <5 years in several West African countries.CONCLUSIONS: We identified the circulation of multiple MDR iNTS serovar STs in the sampled sub-Saharan African countries. Investment in the development and deployment of iNTS vaccines coupled with intensified antimicrobial resistance surveillance are essential to limit the impact of these pathogens in Africa.

AB - BACKGROUND: Invasive non-typhoidal Salmonella (iNTS) is one of the leading causes of bacteraemia in sub-Saharan Africa. We aimed to provide a better understanding of the genetic characteristics and transmission patterns associated with multi-drug resistant (MDR) iNTS serovars across the continent.METHODS: A total of 166 iNTS isolates collected from a multi-centre surveillance in 10 African countries (2010-2014) and a fever study in Ghana (2007-2009) were genome sequenced to investigate the geographical distribution, antimicrobial genetic determinants and population structure of iNTS serotypes-genotypes. Phylogenetic analyses were conducted in the context of the existing genomic frameworks for various iNTS serovars. Population-based incidence of MDR-iNTS disease was estimated in each study site.RESULTS: Salmonella Typhimurium sequence-type (ST) 313 and Salmonella Enteritidis ST11 were predominant, and both exhibited high frequencies of MDR; Salmonella Dublin ST10 was identified in West Africa only. Mutations in the gyrA gene (fluoroquinolone resistance) were identified in S. Enteritidis and S. Typhimurium in Ghana; an ST313 isolate carrying bla CTX-M-15 was found in Kenya. International transmission of MDR ST313 (lineage II) and MDR ST11 (West African clade) was observed between Ghana and neighbouring West African countries. The incidence of MDR-iNTS disease exceeded 100/100 000 person-years-of-observation in children aged <5 years in several West African countries.CONCLUSIONS: We identified the circulation of multiple MDR iNTS serovar STs in the sampled sub-Saharan African countries. Investment in the development and deployment of iNTS vaccines coupled with intensified antimicrobial resistance surveillance are essential to limit the impact of these pathogens in Africa.

KW - Child

KW - Genomics

KW - Humans

KW - Kenya

KW - Pharmaceutical Preparations

KW - Phylogeny

KW - Salmonella typhimurium/genetics

U2 - 10.1136/bmjgh-2021-005659

DO - 10.1136/bmjgh-2021-005659

M3 - A1: Web of Science-article

C2 - 34341020

SN - 2059-7908

VL - 6

JO - BMJ Global Health

JF - BMJ Global Health

IS - 8

M1 - e005659

ER -

The genomic epidemiology of multi-drug resistant invasive non-typhoidal Salmonella in selected sub-Saharan African countries

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