Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events

Vanessa K. Wong; Stephen Baker; Derek J. Pickard; Julian Parkhill; Andrew J. Page; Nicholas A. Feasey; Robert A. Kingsley; Nicholas R. Thomson; Jacqueline A. Keanel; Francois-Xavier Weill; David J. Edwards; Jane Hawkey; Simon R. Harris; Alison E. Mather; Amy K. Cain; James Hadfield; Peter J. Hart; null Nga Tran Vu Thieu; Elizabeth J. Klemm; Dafni A. Glinos; Robert F. Breiman; Conall H. Watson; Samuel Kariuki; Melita A. Gordon; Robert S. Heyderman; Chinyere Okoro; Jan Jacobs; Octavie Lunguya; W. John Edmunds; Chisorno Msefula; Jose A. Chabalgoity; Mike Kama; Kylie Jenkins; Shanta Dutta; Florian Marks; Josefina Campos; Corinne Thompson; Stephen Obaro; Calman A. MacLennan; Christiane Dolecek; Karen H. Keddy; Anthony M. Smith; Christopher M. Parry; Abhilasha Karkey; E. Kim Mulholland; James I. Campbell; Sabina Dongol; Buddha Basnyat; Muriel Dufour; Don Bandaranayake; Take Toleafoa Naseri; Shalini Pravin Singh; Mochammad Hatta; Paul C D Newton; Robert S. Onsare; Lupeoletalalei Isaia; David Dance; Viengmon Davong; Guy Thwaites; Lalith Wijedoru; John A. Crump; Elizabeth De Pinna; Satheesh Nair; Eric J. Nilles; null Duy Pham Thanh; Paul Turner; Sona Soeng; Mary Valcanis; Joan Powling; Karolina Dimovski; Geoff Hogg; Jeremy Farrar; Kathryn E. Holt; Gordon Dougan

doi:10.1038/ng.3281

Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events

Vanessa K. Wong^*, Stephen Baker, Derek J. Pickard, Julian Parkhill, Andrew J. Page, Nicholas A. Feasey, Robert A. Kingsley, Nicholas R. Thomson, Jacqueline A. Keanel, Francois-Xavier Weill, David J. Edwards, Jane Hawkey, Simon R. Harris, Alison E. Mather, Amy K. Cain, James Hadfield, Peter J. Hart, Nga Tran Vu Thieu, Elizabeth J. Klemm, Dafni A. GlinosRobert F. Breiman, Conall H. Watson, Samuel Kariuki, Melita A. Gordon, Robert S. Heyderman, Chinyere Okoro, Jan Jacobs, Octavie Lunguya, W. John Edmunds, Chisorno Msefula, Jose A. Chabalgoity, Mike Kama, Kylie Jenkins, Shanta Dutta, Florian Marks, Josefina Campos, Corinne Thompson, Stephen Obaro, Calman A. MacLennan, Christiane Dolecek, Karen H. Keddy, Anthony M. Smith, Christopher M. Parry, Abhilasha Karkey, E. Kim Mulholland, James I. Campbell, Sabina Dongol, Buddha Basnyat, Muriel Dufour, Don Bandaranayake, Take Toleafoa Naseri, Shalini Pravin Singh, Mochammad Hatta, Paul C D Newton, Robert S. Onsare, Lupeoletalalei Isaia, David Dance, Viengmon Davong, Guy Thwaites, Lalith Wijedoru, John A. Crump, Elizabeth De Pinna, Satheesh Nair, Eric J. Nilles, Duy Pham Thanh, Paul Turner, Sona Soeng, Mary Valcanis, Joan Powling, Karolina Dimovski, Geoff Hogg, Jeremy Farrar, Kathryn E. Holt, Gordon Dougan

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

337 Citations (Scopus)

Abstract

The emergence of multidrug-resistant (MDR) typhoid is a major global health threat affecting many countries where the disease is endemic. Here whole-genome sequence analysis of 1,832 Salmonella enterica serovar Typhi (S. Typhi) identifies a single dominant MDR lineage, H58, that has emerged and spread throughout Asia and Africa over the last 30 years. Our analysis identifies numerous transmissions of H58, including multiple transfers from Asia to Africa and an ongoing, unrecognized MDR epidemic within Africa itself. Notably, our analysis indicates that H58 lineages are displacing antibiotic-sensitive isolates, transforming the global population structure of this pathogen. H58 isolates can harbor a complex MDR element residing either on transmissible IncHI1 plasmids or within multiple chromosomal integration sites. We also identify new mutations that define the H58 lineage. This phylogeographical analysis provides a framework to facilitate global management of MDR typhoid and is applicable to similar MDR lineages emerging in other bacterial species.

Original language	English
Pages (from-to)	632-639
Number of pages	8
Journal	Nature Genetics
Volume	47
Issue number	6
DOIs	https://doi.org/10.1038/ng.3281
Publication status	Published - 2015
Externally published	Yes

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Wong, V. K., Baker, S., Pickard, D. J., Parkhill, J., Page, A. J., Feasey, N. A., Kingsley, R. A., Thomson, N. R., Keanel, J. A., Weill, F.-X., Edwards, D. J., Hawkey, J., Harris, S. R., Mather, A. E., Cain, A. K., Hadfield, J., Hart, P. J., Nga Tran Vu Thieu, Klemm, E. J., ... Dougan, G. (2015). Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events. Nature Genetics, 47(6), 632-639. https://doi.org/10.1038/ng.3281

@article{f82fadc28470446c9216dca774a78b79,

title = "Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events",

abstract = "The emergence of multidrug-resistant (MDR) typhoid is a major global health threat affecting many countries where the disease is endemic. Here whole-genome sequence analysis of 1,832 Salmonella enterica serovar Typhi (S. Typhi) identifies a single dominant MDR lineage, H58, that has emerged and spread throughout Asia and Africa over the last 30 years. Our analysis identifies numerous transmissions of H58, including multiple transfers from Asia to Africa and an ongoing, unrecognized MDR epidemic within Africa itself. Notably, our analysis indicates that H58 lineages are displacing antibiotic-sensitive isolates, transforming the global population structure of this pathogen. H58 isolates can harbor a complex MDR element residing either on transmissible IncHI1 plasmids or within multiple chromosomal integration sites. We also identify new mutations that define the H58 lineage. This phylogeographical analysis provides a framework to facilitate global management of MDR typhoid and is applicable to similar MDR lineages emerging in other bacterial species.",

author = "Wong, {Vanessa K.} and Stephen Baker and Pickard, {Derek J.} and Julian Parkhill and Page, {Andrew J.} and Feasey, {Nicholas A.} and Kingsley, {Robert A.} and Thomson, {Nicholas R.} and Keanel, {Jacqueline A.} and Francois-Xavier Weill and Edwards, {David J.} and Jane Hawkey and Harris, {Simon R.} and Mather, {Alison E.} and Cain, {Amy K.} and James Hadfield and Hart, {Peter J.} and {Nga Tran Vu Thieu} and Klemm, {Elizabeth J.} and Glinos, {Dafni A.} and Breiman, {Robert F.} and Watson, {Conall H.} and Samuel Kariuki and Gordon, {Melita A.} and Heyderman, {Robert S.} and Chinyere Okoro and Jan Jacobs and Octavie Lunguya and Edmunds, {W. John} and Chisorno Msefula and Chabalgoity, {Jose A.} and Mike Kama and Kylie Jenkins and Shanta Dutta and Florian Marks and Josefina Campos and Corinne Thompson and Stephen Obaro and MacLennan, {Calman A.} and Christiane Dolecek and Keddy, {Karen H.} and Smith, {Anthony M.} and Parry, {Christopher M.} and Abhilasha Karkey and Mulholland, {E. Kim} and Campbell, {James I.} and Sabina Dongol and Buddha Basnyat and Muriel Dufour and Don Bandaranayake and Naseri, {Take Toleafoa} and Singh, {Shalini Pravin} and Mochammad Hatta and Newton, {Paul C D} and Onsare, {Robert S.} and Lupeoletalalei Isaia and David Dance and Viengmon Davong and Guy Thwaites and Lalith Wijedoru and Crump, {John A.} and {De Pinna}, Elizabeth and Satheesh Nair and Nilles, {Eric J.} and {Duy Pham Thanh} and Paul Turner and Sona Soeng and Mary Valcanis and Joan Powling and Karolina Dimovski and Geoff Hogg and Jeremy Farrar and Holt, {Kathryn E.} and Gordon Dougan",

year = "2015",

doi = "10.1038/ng.3281",

language = "English",

volume = "47",

pages = "632--639",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Springer, Springer Nature",

number = "6",

}

Wong, VK, Baker, S, Pickard, DJ, Parkhill, J, Page, AJ, Feasey, NA, Kingsley, RA, Thomson, NR, Keanel, JA, Weill, F-X, Edwards, DJ, Hawkey, J, Harris, SR, Mather, AE, Cain, AK, Hadfield, J, Hart, PJ, Nga Tran Vu Thieu, Klemm, EJ, Glinos, DA, Breiman, RF, Watson, CH, Kariuki, S, Gordon, MA, Heyderman, RS, Okoro, C, Jacobs, J, Lunguya, O, Edmunds, WJ, Msefula, C, Chabalgoity, JA, Kama, M, Jenkins, K, Dutta, S, Marks, F, Campos, J, Thompson, C, Obaro, S, MacLennan, CA, Dolecek, C, Keddy, KH, Smith, AM, Parry, CM, Karkey, A, Mulholland, EK, Campbell, JI, Dongol, S, Basnyat, B, Dufour, M, Bandaranayake, D, Naseri, TT, Singh, SP, Hatta, M, Newton, PCD, Onsare, RS, Isaia, L, Dance, D, Davong, V, Thwaites, G, Wijedoru, L, Crump, JA, De Pinna, E, Nair, S, Nilles, EJ, Duy Pham Thanh, Turner, P, Soeng, S, Valcanis, M, Powling, J, Dimovski, K, Hogg, G, Farrar, J, Holt, KE & Dougan, G 2015, 'Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events', Nature Genetics, vol. 47, no. 6, pp. 632-639. https://doi.org/10.1038/ng.3281

TY - JOUR

T1 - Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events

AU - Wong, Vanessa K.

AU - Baker, Stephen

AU - Pickard, Derek J.

AU - Parkhill, Julian

AU - Page, Andrew J.

AU - Feasey, Nicholas A.

AU - Kingsley, Robert A.

AU - Thomson, Nicholas R.

AU - Keanel, Jacqueline A.

AU - Weill, Francois-Xavier

AU - Edwards, David J.

AU - Hawkey, Jane

AU - Harris, Simon R.

AU - Mather, Alison E.

AU - Cain, Amy K.

AU - Hadfield, James

AU - Hart, Peter J.

AU - Nga Tran Vu Thieu, null

AU - Klemm, Elizabeth J.

AU - Glinos, Dafni A.

AU - Breiman, Robert F.

AU - Watson, Conall H.

AU - Kariuki, Samuel

AU - Gordon, Melita A.

AU - Heyderman, Robert S.

AU - Okoro, Chinyere

AU - Jacobs, Jan

AU - Lunguya, Octavie

AU - Edmunds, W. John

AU - Msefula, Chisorno

AU - Chabalgoity, Jose A.

AU - Kama, Mike

AU - Jenkins, Kylie

AU - Dutta, Shanta

AU - Marks, Florian

AU - Campos, Josefina

AU - Thompson, Corinne

AU - Obaro, Stephen

AU - MacLennan, Calman A.

AU - Dolecek, Christiane

AU - Keddy, Karen H.

AU - Smith, Anthony M.

AU - Parry, Christopher M.

AU - Karkey, Abhilasha

AU - Mulholland, E. Kim

AU - Campbell, James I.

AU - Dongol, Sabina

AU - Basnyat, Buddha

AU - Dufour, Muriel

AU - Bandaranayake, Don

AU - Naseri, Take Toleafoa

AU - Singh, Shalini Pravin

AU - Hatta, Mochammad

AU - Newton, Paul C D

AU - Onsare, Robert S.

AU - Isaia, Lupeoletalalei

AU - Dance, David

AU - Davong, Viengmon

AU - Thwaites, Guy

AU - Wijedoru, Lalith

AU - Crump, John A.

AU - De Pinna, Elizabeth

AU - Nair, Satheesh

AU - Nilles, Eric J.

AU - Duy Pham Thanh, null

AU - Turner, Paul

AU - Soeng, Sona

AU - Valcanis, Mary

AU - Powling, Joan

AU - Dimovski, Karolina

AU - Hogg, Geoff

AU - Farrar, Jeremy

AU - Holt, Kathryn E.

AU - Dougan, Gordon

PY - 2015

Y1 - 2015

N2 - The emergence of multidrug-resistant (MDR) typhoid is a major global health threat affecting many countries where the disease is endemic. Here whole-genome sequence analysis of 1,832 Salmonella enterica serovar Typhi (S. Typhi) identifies a single dominant MDR lineage, H58, that has emerged and spread throughout Asia and Africa over the last 30 years. Our analysis identifies numerous transmissions of H58, including multiple transfers from Asia to Africa and an ongoing, unrecognized MDR epidemic within Africa itself. Notably, our analysis indicates that H58 lineages are displacing antibiotic-sensitive isolates, transforming the global population structure of this pathogen. H58 isolates can harbor a complex MDR element residing either on transmissible IncHI1 plasmids or within multiple chromosomal integration sites. We also identify new mutations that define the H58 lineage. This phylogeographical analysis provides a framework to facilitate global management of MDR typhoid and is applicable to similar MDR lineages emerging in other bacterial species.

AB - The emergence of multidrug-resistant (MDR) typhoid is a major global health threat affecting many countries where the disease is endemic. Here whole-genome sequence analysis of 1,832 Salmonella enterica serovar Typhi (S. Typhi) identifies a single dominant MDR lineage, H58, that has emerged and spread throughout Asia and Africa over the last 30 years. Our analysis identifies numerous transmissions of H58, including multiple transfers from Asia to Africa and an ongoing, unrecognized MDR epidemic within Africa itself. Notably, our analysis indicates that H58 lineages are displacing antibiotic-sensitive isolates, transforming the global population structure of this pathogen. H58 isolates can harbor a complex MDR element residing either on transmissible IncHI1 plasmids or within multiple chromosomal integration sites. We also identify new mutations that define the H58 lineage. This phylogeographical analysis provides a framework to facilitate global management of MDR typhoid and is applicable to similar MDR lineages emerging in other bacterial species.

UR - http://www.scopus.com/inward/record.url?scp=84930064392&partnerID=8YFLogxK

U2 - 10.1038/ng.3281

DO - 10.1038/ng.3281

M3 - Article

C2 - 25961941

SN - 1061-4036

VL - 47

SP - 632

EP - 639

JO - Nature Genetics

JF - Nature Genetics

IS - 6

ER -

Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events

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