Molecular Surveillance Identifies Multiple Transmissions of Typhoid in West Africa

Vanessa K. Wong; Kathryn E. Holt; Chinyere Okoro; Stephen Baker; Derek J. Pickard; Florian Marks; Andrew J. Page; Grace Olanipekun; Huda Munir; Roxanne Alter; Paul D. Fey; Nick Feasey; Francois Xavier Weill; Simon Le Hello; Peter J. Hart; Samuel Kariuki; Robert F. Breiman; Melita A. Gordon; Robert S. Heyderman; Jan Jacobs; Octavie Lunguya; Chisomo Msefula; Calman A. MacLennan; Karen H. Keddy; Anthony M. Smith; Robert S. Onsare; Elizabeth De Pinna; Satheesh Nair; Ben Amos; Gordon Dougan; Stephen Obaro; Julian Parkhill; Robert A. Kingsley; Nicholas R. Thomson; Jacqueline A. Keane; Jane Hawkey; David J. Edwards; Zoe A. Dyson; Simon R. Harris; Amy K. Cain; James Hadfield; Elizabeth J. Klemm; Conall H. Watson; W. John Edmunds; Nga Tran Vu Thieu; Mike Kama; Kylie Jenkins; Shanta Dutta; Josefina Campos; Christopher Parry

doi:10.1371/journal.pntd.0004781

Molecular Surveillance Identifies Multiple Transmissions of Typhoid in West Africa

Vanessa K. Wong
, Kathryn E. Holt
, Chinyere Okoro
, Stephen Baker
, Derek J. Pickard
, Florian Marks
, Andrew J. Page
, Grace Olanipekun
, Huda Munir
, Roxanne Alter
, Paul D. Fey
, Nick Feasey
, Francois Xavier Weill
, Simon Le Hello
, Peter J. Hart
, Samuel Kariuki
, Robert F. Breiman
, Melita A. Gordon
, Robert S. Heyderman
, Jan Jacobs

Octavie Lunguya, Chisomo Msefula, Calman A. MacLennan, Karen H. Keddy, Anthony M. Smith, Robert S. Onsare, Elizabeth De Pinna, Satheesh Nair, Ben Amos, Gordon Dougan, Stephen Obaro, Julian Parkhill, Robert A. Kingsley, Nicholas R. Thomson, Jacqueline A. Keane, Jane Hawkey, David J. Edwards, Zoe A. Dyson, Simon R. Harris, Amy K. Cain, James Hadfield, Elizabeth J. Klemm, Conall H. Watson, W. John Edmunds, Nga Tran Vu Thieu, Mike Kama, Kylie Jenkins, Shanta Dutta, Josefina Campos, Christopher Parry

Wellcome Sanger Institute
Cambridge University Hospitals NHS Foundation Trust
University of Melbourne
University of Oxford
London School of Hygiene and Tropical Medicine
International Vaccine Institute, Seoul
International Foundation Against Infectious Diseases in Nigeria
Aminu Kano Teaching Hospital
University of Nebraska Medical Center
Institut Pasteur Paris
University of Birmingham
City St George's, University of London
Kenya Medical Research Institute
Centers for Disease Control and Prevention
Emory University
University of Liverpool
University of Malawi
University College London
Institute of Tropical Medicine Antwerp
KU Leuven
National Institute for Biomedical Research
University Hospital of Kinshasa
University of the Witwatersrand
UK Health Security Agency
St Augustine’s Hospital
University of Abuja, Gwagwalada
Bingham University
Norwich Research Park
Universidad de la República
Ministry of Health
Fiji Health Sector Support Program
National Institute of Cholera and Enteric Diseases India
Administración Nacional de Laboratorios e Institutos de Salud "Dr. Carlos G. Malbrán"
Nagasaki University

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

41 Citations (Scopus)

Abstract

Background

The burden of typhoid in sub-Saharan African (SSA) countries has been difficult to estimate, in part, due to suboptimal laboratory diagnostics. However, surveillance blood cultures at two sites in Nigeria have identified typhoid associated with Salmonella enterica serovar Typhi (S. Typhi) as an important cause of bacteremia in children.

Methods

A total of 128 S. Typhi isolates from these studies in Nigeria were whole-genome sequenced, and the resulting data was used to place these Nigerian isolates into a worldwide context based on their phylogeny and carriage of molecular determinants of antibiotic resistance.

Results

Several distinct S. Typhi genotypes were identified in Nigeria that were related to other clusters of S. Typhi isolates from north, west and central regions of Africa. The rapidly expanding S. Typhi clade 4.3.1 (H58) previously associated with multiple antimicrobial resistances in Asia and in east, central and southern Africa, was not detected in this study. However, antimicrobial resistance was common amongst the Nigerian isolates and was associated with several plasmids, including the IncHI1 plasmid commonly associated with S. Typhi.

Conclusions

These data indicate that typhoid in Nigeria was established through multiple independent introductions into the country, with evidence of regional spread. MDR typhoid appears to be evolving independently of the haplotype H58 found in other typhoid endemic countries. This study highlights an urgent need for routine surveillance to monitor the epidemiology of typhoid and evolution of antimicrobial resistance within the bacterial population as a means to facilitate public health interventions to reduce the substantial morbidity and mortality of typhoid.

Original language	English
Article number	e0004781
Pages (from-to)	e0004781
Journal	PLoS Neglected Tropical Diseases
Volume	10
Issue number	9
DOIs	https://doi.org/10.1371/journal.pntd.0004781
Publication status	Published - 22 Sept 2016

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

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10.1371/journal.pntd.0004781Licence: CC0

PLoS Neg Trop 10 9 e0004781 Molecular surveillanceFinal published version, 1.45 MBLicence: CC BY

Cite this

Wong, V. K., Holt, K. E., Okoro, C., Baker, S., Pickard, D. J., Marks, F., Page, A. J., Olanipekun, G., Munir, H., Alter, R., Fey, P. D., Feasey, N., Weill, F. X., Le Hello, S., Hart, P. J., Kariuki, S., Breiman, R. F., Gordon, M. A., Heyderman, R. S., ... Parry, C. (2016). Molecular Surveillance Identifies Multiple Transmissions of Typhoid in West Africa. PLoS Neglected Tropical Diseases, 10(9), e0004781. Article e0004781. https://doi.org/10.1371/journal.pntd.0004781

@article{bb52ac10bed540dab7e7dd6c61539981,

title = "Molecular Surveillance Identifies Multiple Transmissions of Typhoid in West Africa",

abstract = "BackgroundThe burden of typhoid in sub-Saharan African (SSA) countries has been difficult to estimate, in part, due to suboptimal laboratory diagnostics. However, surveillance blood cultures at two sites in Nigeria have identified typhoid associated with Salmonella enterica serovar Typhi (S. Typhi) as an important cause of bacteremia in children.MethodsA total of 128 S. Typhi isolates from these studies in Nigeria were whole-genome sequenced, and the resulting data was used to place these Nigerian isolates into a worldwide context based on their phylogeny and carriage of molecular determinants of antibiotic resistance.ResultsSeveral distinct S. Typhi genotypes were identified in Nigeria that were related to other clusters of S. Typhi isolates from north, west and central regions of Africa. The rapidly expanding S. Typhi clade 4.3.1 (H58) previously associated with multiple antimicrobial resistances in Asia and in east, central and southern Africa, was not detected in this study. However, antimicrobial resistance was common amongst the Nigerian isolates and was associated with several plasmids, including the IncHI1 plasmid commonly associated with S. Typhi.ConclusionsThese data indicate that typhoid in Nigeria was established through multiple independent introductions into the country, with evidence of regional spread. MDR typhoid appears to be evolving independently of the haplotype H58 found in other typhoid endemic countries. This study highlights an urgent need for routine surveillance to monitor the epidemiology of typhoid and evolution of antimicrobial resistance within the bacterial population as a means to facilitate public health interventions to reduce the substantial morbidity and mortality of typhoid.",

author = "Wong, \{Vanessa K.\} and Holt, \{Kathryn E.\} and Chinyere Okoro and Stephen Baker and Pickard, \{Derek J.\} and Florian Marks and Page, \{Andrew J.\} and Grace Olanipekun and Huda Munir and Roxanne Alter and Fey, \{Paul D.\} and Nick Feasey and Weill, \{Francois Xavier\} and \{Le Hello\}, Simon and Hart, \{Peter J.\} and Samuel Kariuki and Breiman, \{Robert F.\} and Gordon, \{Melita A.\} and Heyderman, \{Robert S.\} and Jan Jacobs and Octavie Lunguya and Chisomo Msefula and MacLennan, \{Calman A.\} and Keddy, \{Karen H.\} and Smith, \{Anthony M.\} and Onsare, \{Robert S.\} and \{De Pinna\}, Elizabeth and Satheesh Nair and Ben Amos and Gordon Dougan and Stephen Obaro and Julian Parkhill and Kingsley, \{Robert A.\} and Thomson, \{Nicholas R.\} and Keane, \{Jacqueline A.\} and Jane Hawkey and Edwards, \{David J.\} and Dyson, \{Zoe A.\} and Harris, \{Simon R.\} and Cain, \{Amy K.\} and James Hadfield and Klemm, \{Elizabeth J.\} and Watson, \{Conall H.\} and \{John Edmunds\}, W. and \{Vu Thieu\}, \{Nga Tran\} and Mike Kama and Kylie Jenkins and Shanta Dutta and Josefina Campos and Christopher Parry",

year = "2016",

month = sep,

day = "22",

doi = "10.1371/journal.pntd.0004781",

language = "English",

volume = "10",

pages = "e0004781",

journal = "PLoS Neglected Tropical Diseases",

issn = "1935-2727",

publisher = "Public Library of Science",

number = "9",

}

Wong, VK, Holt, KE, Okoro, C, Baker, S, Pickard, DJ, Marks, F, Page, AJ, Olanipekun, G, Munir, H, Alter, R, Fey, PD, Feasey, N, Weill, FX, Le Hello, S, Hart, PJ, Kariuki, S, Breiman, RF, Gordon, MA, Heyderman, RS, Jacobs, J, Lunguya, O, Msefula, C, MacLennan, CA, Keddy, KH, Smith, AM, Onsare, RS, De Pinna, E, Nair, S, Amos, B, Dougan, G, Obaro, S, Parkhill, J, Kingsley, RA, Thomson, NR, Keane, JA, Hawkey, J, Edwards, DJ, Dyson, ZA, Harris, SR, Cain, AK, Hadfield, J, Klemm, EJ, Watson, CH, John Edmunds, W, Vu Thieu, NT, Kama, M, Jenkins, K, Dutta, S, Campos, J & Parry, C 2016, 'Molecular Surveillance Identifies Multiple Transmissions of Typhoid in West Africa', PLoS Neglected Tropical Diseases, vol. 10, no. 9, e0004781, pp. e0004781. https://doi.org/10.1371/journal.pntd.0004781

TY - JOUR

T1 - Molecular Surveillance Identifies Multiple Transmissions of Typhoid in West Africa

AU - Wong, Vanessa K.

AU - Holt, Kathryn E.

AU - Okoro, Chinyere

AU - Baker, Stephen

AU - Pickard, Derek J.

AU - Marks, Florian

AU - Page, Andrew J.

AU - Olanipekun, Grace

AU - Munir, Huda

AU - Alter, Roxanne

AU - Fey, Paul D.

AU - Feasey, Nick

AU - Weill, Francois Xavier

AU - Le Hello, Simon

AU - Hart, Peter J.

AU - Kariuki, Samuel

AU - Breiman, Robert F.

AU - Gordon, Melita A.

AU - Heyderman, Robert S.

AU - Jacobs, Jan

AU - Lunguya, Octavie

AU - Msefula, Chisomo

AU - MacLennan, Calman A.

AU - Keddy, Karen H.

AU - Smith, Anthony M.

AU - Onsare, Robert S.

AU - De Pinna, Elizabeth

AU - Nair, Satheesh

AU - Amos, Ben

AU - Dougan, Gordon

AU - Obaro, Stephen

AU - Parkhill, Julian

AU - Kingsley, Robert A.

AU - Thomson, Nicholas R.

AU - Keane, Jacqueline A.

AU - Hawkey, Jane

AU - Edwards, David J.

AU - Dyson, Zoe A.

AU - Harris, Simon R.

AU - Cain, Amy K.

AU - Hadfield, James

AU - Klemm, Elizabeth J.

AU - Watson, Conall H.

AU - John Edmunds, W.

AU - Vu Thieu, Nga Tran

AU - Kama, Mike

AU - Jenkins, Kylie

AU - Dutta, Shanta

AU - Campos, Josefina

AU - Parry, Christopher

PY - 2016/9/22

Y1 - 2016/9/22

N2 - BackgroundThe burden of typhoid in sub-Saharan African (SSA) countries has been difficult to estimate, in part, due to suboptimal laboratory diagnostics. However, surveillance blood cultures at two sites in Nigeria have identified typhoid associated with Salmonella enterica serovar Typhi (S. Typhi) as an important cause of bacteremia in children.MethodsA total of 128 S. Typhi isolates from these studies in Nigeria were whole-genome sequenced, and the resulting data was used to place these Nigerian isolates into a worldwide context based on their phylogeny and carriage of molecular determinants of antibiotic resistance.ResultsSeveral distinct S. Typhi genotypes were identified in Nigeria that were related to other clusters of S. Typhi isolates from north, west and central regions of Africa. The rapidly expanding S. Typhi clade 4.3.1 (H58) previously associated with multiple antimicrobial resistances in Asia and in east, central and southern Africa, was not detected in this study. However, antimicrobial resistance was common amongst the Nigerian isolates and was associated with several plasmids, including the IncHI1 plasmid commonly associated with S. Typhi.ConclusionsThese data indicate that typhoid in Nigeria was established through multiple independent introductions into the country, with evidence of regional spread. MDR typhoid appears to be evolving independently of the haplotype H58 found in other typhoid endemic countries. This study highlights an urgent need for routine surveillance to monitor the epidemiology of typhoid and evolution of antimicrobial resistance within the bacterial population as a means to facilitate public health interventions to reduce the substantial morbidity and mortality of typhoid.

AB - BackgroundThe burden of typhoid in sub-Saharan African (SSA) countries has been difficult to estimate, in part, due to suboptimal laboratory diagnostics. However, surveillance blood cultures at two sites in Nigeria have identified typhoid associated with Salmonella enterica serovar Typhi (S. Typhi) as an important cause of bacteremia in children.MethodsA total of 128 S. Typhi isolates from these studies in Nigeria were whole-genome sequenced, and the resulting data was used to place these Nigerian isolates into a worldwide context based on their phylogeny and carriage of molecular determinants of antibiotic resistance.ResultsSeveral distinct S. Typhi genotypes were identified in Nigeria that were related to other clusters of S. Typhi isolates from north, west and central regions of Africa. The rapidly expanding S. Typhi clade 4.3.1 (H58) previously associated with multiple antimicrobial resistances in Asia and in east, central and southern Africa, was not detected in this study. However, antimicrobial resistance was common amongst the Nigerian isolates and was associated with several plasmids, including the IncHI1 plasmid commonly associated with S. Typhi.ConclusionsThese data indicate that typhoid in Nigeria was established through multiple independent introductions into the country, with evidence of regional spread. MDR typhoid appears to be evolving independently of the haplotype H58 found in other typhoid endemic countries. This study highlights an urgent need for routine surveillance to monitor the epidemiology of typhoid and evolution of antimicrobial resistance within the bacterial population as a means to facilitate public health interventions to reduce the substantial morbidity and mortality of typhoid.

U2 - 10.1371/journal.pntd.0004781

DO - 10.1371/journal.pntd.0004781

M3 - Article

SN - 1935-2727

VL - 10

SP - e0004781

JO - PLoS Neglected Tropical Diseases

JF - PLoS Neglected Tropical Diseases

IS - 9

M1 - e0004781

ER -

Molecular Surveillance Identifies Multiple Transmissions of Typhoid in West Africa

Abstract

UN SDGs

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