A genomic appraisal of invasive Salmonella Typhimurium and associated antibiotic resistance in sub-Saharan Africa

Sandra Van Puyvelde; Tessa de Block; Sushmita Sridhar; Matt Bawn; Robert A. Kingsley; Brecht Ingelbeen; Mathew A. Beale; Barbara Barbé; Hyon Jin Jeon; Lisette Mbuyi-Kalonji; Marie France Phoba; Dadi Falay; Delphine Martiny; Olivier Vandenberg; Dissou Affolabi; Jean Pierre Rutanga; Pieter Jan Ceyssens; Wesley Mattheus; Wim L. Cuypers; Marianne A.B. van der Sande; Se Eun Park; Simon Kariuki; Kephas Otieno; John P.A. Lusingu; Joyce R. Mbwana; Samuel Adjei; Anima Sarfo; Seth O. Agyei; Kwaku P. Asante; Walter Otieno; Lucas Otieno; Marc C. Tahita; Palpouguini Lompo; Irving F. Hoffman; Tisungane Mvalo; Chisomo Msefula; Fatimah Hassan-Hanga; Stephen Obaro; Grant Mackenzie; Stijn Deborggraeve; Nicholas Feasey; Florian Marks; Calman A. MacLennan; Nicholas R. Thomson; Jan Jacobs; Gordon Dougan; Samuel Kariuki; Octavie Lunguya

doi:10.1038/s41467-023-41152-6

A genomic appraisal of invasive Salmonella Typhimurium and associated antibiotic resistance in sub-Saharan Africa

Sandra Van Puyvelde^*, Tessa de Block, Sushmita Sridhar, Matt Bawn, Robert A. Kingsley, Brecht Ingelbeen, Mathew A. Beale, Barbara Barbé, Hyon Jin Jeon, Lisette Mbuyi-Kalonji, Marie France Phoba, Dadi Falay, Delphine Martiny, Olivier Vandenberg, Dissou Affolabi, Jean Pierre Rutanga, Pieter Jan Ceyssens, Wesley Mattheus, Wim L. Cuypers, Marianne A.B. van der SandeSe Eun Park, Simon Kariuki, Kephas Otieno, John P.A. Lusingu, Joyce R. Mbwana, Samuel Adjei, Anima Sarfo, Seth O. Agyei, Kwaku P. Asante, Walter Otieno, Lucas Otieno, Marc C. Tahita, Palpouguini Lompo, Irving F. Hoffman, Tisungane Mvalo, Chisomo Msefula, Fatimah Hassan-Hanga, Stephen Obaro, Grant Mackenzie, Stijn Deborggraeve, Nicholas Feasey, Florian Marks, Calman A. MacLennan, Nicholas R. Thomson, Jan Jacobs, Gordon Dougan, Samuel Kariuki, Octavie Lunguya

^*Corresponding author for this work

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Abstract

Invasive non-typhoidal Salmonella (iNTS) disease manifesting as bloodstream infection with high mortality is responsible for a huge public health burden in sub-Saharan Africa. Salmonella enterica serovar Typhimurium (S. Typhimurium) is the main cause of iNTS disease in Africa. By analysing whole genome sequence data from 1303 S. Typhimurium isolates originating from 19 African countries and isolated between 1979 and 2017, here we show a thorough scaled appraisal of the population structure of iNTS disease caused by S. Typhimurium across many of Africa’s most impacted countries. At least six invasive S. Typhimurium clades have already emerged, with ST313 lineage 2 or ST313-L2 driving the current pandemic. ST313-L2 likely emerged in the Democratic Republic of Congo around 1980 and further spread in the mid 1990s. We observed plasmid-borne as well as chromosomally encoded fluoroquinolone resistance underlying emergences of extensive-drug and pan-drug resistance. Our work provides an overview of the evolution of invasive S. Typhimurium disease, and can be exploited to target control measures.

Original language	English
Article number	6392
Journal	Nature Communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-41152-6
Publication status	Published - 23 Oct 2023

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Van Puyvelde, S., de Block, T., Sridhar, S., Bawn, M., Kingsley, R. A., Ingelbeen, B., Beale, M. A., Barbé, B., Jeon, H. J., Mbuyi-Kalonji, L., Phoba, M. F., Falay, D., Martiny, D., Vandenberg, O., Affolabi, D., Rutanga, J. P., Ceyssens, P. J., Mattheus, W., Cuypers, W. L., ... Lunguya, O. (2023). A genomic appraisal of invasive Salmonella Typhimurium and associated antibiotic resistance in sub-Saharan Africa. Nature Communications, 14(1), Article 6392. https://doi.org/10.1038/s41467-023-41152-6

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title = "A genomic appraisal of invasive Salmonella Typhimurium and associated antibiotic resistance in sub-Saharan Africa",

abstract = "Invasive non-typhoidal Salmonella (iNTS) disease manifesting as bloodstream infection with high mortality is responsible for a huge public health burden in sub-Saharan Africa. Salmonella enterica serovar Typhimurium (S. Typhimurium) is the main cause of iNTS disease in Africa. By analysing whole genome sequence data from 1303 S. Typhimurium isolates originating from 19 African countries and isolated between 1979 and 2017, here we show a thorough scaled appraisal of the population structure of iNTS disease caused by S. Typhimurium across many of Africa{\textquoteright}s most impacted countries. At least six invasive S. Typhimurium clades have already emerged, with ST313 lineage 2 or ST313-L2 driving the current pandemic. ST313-L2 likely emerged in the Democratic Republic of Congo around 1980 and further spread in the mid 1990s. We observed plasmid-borne as well as chromosomally encoded fluoroquinolone resistance underlying emergences of extensive-drug and pan-drug resistance. Our work provides an overview of the evolution of invasive S. Typhimurium disease, and can be exploited to target control measures.",

author = "{Van Puyvelde}, Sandra and {de Block}, Tessa and Sushmita Sridhar and Matt Bawn and Kingsley, {Robert A.} and Brecht Ingelbeen and Beale, {Mathew A.} and Barbara Barb{\'e} and Jeon, {Hyon Jin} and Lisette Mbuyi-Kalonji and Phoba, {Marie France} and Dadi Falay and Delphine Martiny and Olivier Vandenberg and Dissou Affolabi and Rutanga, {Jean Pierre} and Ceyssens, {Pieter Jan} and Wesley Mattheus and Cuypers, {Wim L.} and {van der Sande}, {Marianne A.B.} and Park, {Se Eun} and Simon Kariuki and Kephas Otieno and Lusingu, {John P.A.} and Mbwana, {Joyce R.} and Samuel Adjei and Anima Sarfo and Agyei, {Seth O.} and Asante, {Kwaku P.} and Walter Otieno and Lucas Otieno and Tahita, {Marc C.} and Palpouguini Lompo and Hoffman, {Irving F.} and Tisungane Mvalo and Chisomo Msefula and Fatimah Hassan-Hanga and Stephen Obaro and Grant Mackenzie and Stijn Deborggraeve and Nicholas Feasey and Florian Marks and MacLennan, {Calman A.} and Thomson, {Nicholas R.} and Jan Jacobs and Gordon Dougan and Samuel Kariuki and Octavie Lunguya",

note = "Publisher Copyright: {\textcopyright} 2023, Springer Nature Limited.",

year = "2023",

month = oct,

day = "23",

doi = "10.1038/s41467-023-41152-6",

language = "English",

volume = "14",

journal = "Nature Communications",

issn = "2041-1723",

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Van Puyvelde, S, de Block, T, Sridhar, S, Bawn, M, Kingsley, RA, Ingelbeen, B, Beale, MA, Barbé, B, Jeon, HJ, Mbuyi-Kalonji, L, Phoba, MF, Falay, D, Martiny, D, Vandenberg, O, Affolabi, D, Rutanga, JP, Ceyssens, PJ, Mattheus, W, Cuypers, WL, van der Sande, MAB, Park, SE, Kariuki, S, Otieno, K, Lusingu, JPA, Mbwana, JR, Adjei, S, Sarfo, A, Agyei, SO, Asante, KP, Otieno, W, Otieno, L, Tahita, MC, Lompo, P, Hoffman, IF, Mvalo, T, Msefula, C, Hassan-Hanga, F, Obaro, S, Mackenzie, G, Deborggraeve, S, Feasey, N, Marks, F, MacLennan, CA, Thomson, NR, Jacobs, J, Dougan, G, Kariuki, S & Lunguya, O 2023, 'A genomic appraisal of invasive Salmonella Typhimurium and associated antibiotic resistance in sub-Saharan Africa', Nature Communications, vol. 14, no. 1, 6392. https://doi.org/10.1038/s41467-023-41152-6

TY - JOUR

T1 - A genomic appraisal of invasive Salmonella Typhimurium and associated antibiotic resistance in sub-Saharan Africa

AU - Van Puyvelde, Sandra

AU - de Block, Tessa

AU - Sridhar, Sushmita

AU - Bawn, Matt

AU - Kingsley, Robert A.

AU - Ingelbeen, Brecht

AU - Beale, Mathew A.

AU - Barbé, Barbara

AU - Jeon, Hyon Jin

AU - Mbuyi-Kalonji, Lisette

AU - Phoba, Marie France

AU - Falay, Dadi

AU - Martiny, Delphine

AU - Vandenberg, Olivier

AU - Affolabi, Dissou

AU - Rutanga, Jean Pierre

AU - Ceyssens, Pieter Jan

AU - Mattheus, Wesley

AU - Cuypers, Wim L.

AU - van der Sande, Marianne A.B.

AU - Park, Se Eun

AU - Kariuki, Simon

AU - Otieno, Kephas

AU - Lusingu, John P.A.

AU - Mbwana, Joyce R.

AU - Adjei, Samuel

AU - Sarfo, Anima

AU - Agyei, Seth O.

AU - Asante, Kwaku P.

AU - Otieno, Walter

AU - Otieno, Lucas

AU - Tahita, Marc C.

AU - Lompo, Palpouguini

AU - Hoffman, Irving F.

AU - Mvalo, Tisungane

AU - Msefula, Chisomo

AU - Hassan-Hanga, Fatimah

AU - Obaro, Stephen

AU - Mackenzie, Grant

AU - Deborggraeve, Stijn

AU - Feasey, Nicholas

AU - Marks, Florian

AU - MacLennan, Calman A.

AU - Thomson, Nicholas R.

AU - Jacobs, Jan

AU - Dougan, Gordon

AU - Kariuki, Samuel

AU - Lunguya, Octavie

PY - 2023/10/23

Y1 - 2023/10/23

N2 - Invasive non-typhoidal Salmonella (iNTS) disease manifesting as bloodstream infection with high mortality is responsible for a huge public health burden in sub-Saharan Africa. Salmonella enterica serovar Typhimurium (S. Typhimurium) is the main cause of iNTS disease in Africa. By analysing whole genome sequence data from 1303 S. Typhimurium isolates originating from 19 African countries and isolated between 1979 and 2017, here we show a thorough scaled appraisal of the population structure of iNTS disease caused by S. Typhimurium across many of Africa’s most impacted countries. At least six invasive S. Typhimurium clades have already emerged, with ST313 lineage 2 or ST313-L2 driving the current pandemic. ST313-L2 likely emerged in the Democratic Republic of Congo around 1980 and further spread in the mid 1990s. We observed plasmid-borne as well as chromosomally encoded fluoroquinolone resistance underlying emergences of extensive-drug and pan-drug resistance. Our work provides an overview of the evolution of invasive S. Typhimurium disease, and can be exploited to target control measures.

AB - Invasive non-typhoidal Salmonella (iNTS) disease manifesting as bloodstream infection with high mortality is responsible for a huge public health burden in sub-Saharan Africa. Salmonella enterica serovar Typhimurium (S. Typhimurium) is the main cause of iNTS disease in Africa. By analysing whole genome sequence data from 1303 S. Typhimurium isolates originating from 19 African countries and isolated between 1979 and 2017, here we show a thorough scaled appraisal of the population structure of iNTS disease caused by S. Typhimurium across many of Africa’s most impacted countries. At least six invasive S. Typhimurium clades have already emerged, with ST313 lineage 2 or ST313-L2 driving the current pandemic. ST313-L2 likely emerged in the Democratic Republic of Congo around 1980 and further spread in the mid 1990s. We observed plasmid-borne as well as chromosomally encoded fluoroquinolone resistance underlying emergences of extensive-drug and pan-drug resistance. Our work provides an overview of the evolution of invasive S. Typhimurium disease, and can be exploited to target control measures.

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U2 - 10.1038/s41467-023-41152-6

DO - 10.1038/s41467-023-41152-6

M3 - Article

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SN - 2041-1723

VL - 14

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 6392

ER -

A genomic appraisal of invasive Salmonella Typhimurium and associated antibiotic resistance in sub-Saharan Africa

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