Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa

Chinyere K. Okoro; Robert A. Kingsley; Thomas R. Connor; Simon R. Harris; Christopher M. Parry; Manar N. Al-Mashhadani; Samuel Kariuki; Chisomo L. Msefula; Melita A. Gordon; Elizabeth De Pinna; John Wain; Robert S. Heyderman; Stephen Obaro; Pedro L. Alonso; Inacio Mandomando; Calman A. MacLennan; Milagritos D. Tapia; Myron M. Levine; Sharon M. Tennant; Julian Parkhill; Gordon Dougan

doi:10.1038/ng.2423

Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa

Chinyere K. Okoro, Robert A. Kingsley, Thomas R. Connor, Simon R. Harris, Christopher M. Parry, Manar N. Al-Mashhadani, Samuel Kariuki, Chisomo L. Msefula, Melita A. Gordon, Elizabeth De Pinna, John Wain, Robert S. Heyderman, Stephen Obaro, Pedro L. Alonso, Inacio Mandomando, Calman A. MacLennan, Milagritos D. Tapia, Myron M. Levine, Sharon M. Tennant, Julian ParkhillGordon Dougan^*

^*Corresponding author for this work

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

322 Citations (Scopus)

Abstract

A highly invasive form of non-typhoidal Salmonella (iNTS) disease has recently been documented in many countries in sub-Saharan Africa. The most common Salmonella enterica serovar causing this disease is Typhimurium (Salmonella Typhimurium). We applied whole-genome sequence-based phylogenetic methods to define the population structure of sub-Saharan African invasive Salmonella Typhimurium isolates and compared these to global Salmonella Typhimurium populations. Notably, the vast majority of sub-Saharan invasive Salmonella Typhimurium isolates fell within two closely related, highly clustered phylogenetic lineages that we estimate emerged independently ∼52 and ∼35 years ago in close temporal association with the current HIV pandemic. Clonal replacement of isolates from lineage I by those from lineage II was potentially influenced by the use of chloramphenicol for the treatment of iNTS disease. Our analysis suggests that iNTS disease is in part an epidemic in sub-Saharan Africa caused by highly related Salmonella Typhimurium lineages that may have occupied new niches associated with a compromised human population and antibiotic treatment.

Original language	English
Pages (from-to)	1215-1221
Number of pages	7
Journal	Nature Genetics
Volume	44
Issue number	11
DOIs	https://doi.org/10.1038/ng.2423
Publication status	Published - Nov 2012

Bibliographical note

Funding Information:
We thank J. Cheesborough for providing the DRC isolates, M. Okong, N. French and the Medical Research Council, Uganda, for providing the Uganda isolates, S. Nair for providing the Health Protection Agency (HPA) isolates, L. Barquist for modeling the pre-1990 HIV prevalence data and the Sequencing team at the Wellcome Trust Sanger Institute. This work was funded by a Wellcome Trust grant (098051). C.A.M. was supported by a Tropical Research Fellowship from the Wellcome Trust and a Clinical Research Fellowship from GlaxoSmithKline.

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10.1038/ng.2423

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Okoro, C. K., Kingsley, R. A., Connor, T. R., Harris, S. R., Parry, C. M., Al-Mashhadani, M. N., Kariuki, S., Msefula, C. L., Gordon, M. A., De Pinna, E., Wain, J., Heyderman, R. S., Obaro, S., Alonso, P. L., Mandomando, I., MacLennan, C. A., Tapia, M. D., Levine, M. M., Tennant, S. M., ... Dougan, G. (2012). Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nature Genetics, 44(11), 1215-1221. https://doi.org/10.1038/ng.2423

@article{5d076a70a7e4495e95bf011cb77b1e7a,

title = "Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa",

abstract = "A highly invasive form of non-typhoidal Salmonella (iNTS) disease has recently been documented in many countries in sub-Saharan Africa. The most common Salmonella enterica serovar causing this disease is Typhimurium (Salmonella Typhimurium). We applied whole-genome sequence-based phylogenetic methods to define the population structure of sub-Saharan African invasive Salmonella Typhimurium isolates and compared these to global Salmonella Typhimurium populations. Notably, the vast majority of sub-Saharan invasive Salmonella Typhimurium isolates fell within two closely related, highly clustered phylogenetic lineages that we estimate emerged independently ∼52 and ∼35 years ago in close temporal association with the current HIV pandemic. Clonal replacement of isolates from lineage I by those from lineage II was potentially influenced by the use of chloramphenicol for the treatment of iNTS disease. Our analysis suggests that iNTS disease is in part an epidemic in sub-Saharan Africa caused by highly related Salmonella Typhimurium lineages that may have occupied new niches associated with a compromised human population and antibiotic treatment.",

author = "Okoro, {Chinyere K.} and Kingsley, {Robert A.} and Connor, {Thomas R.} and Harris, {Simon R.} and Parry, {Christopher M.} and Al-Mashhadani, {Manar N.} and Samuel Kariuki and Msefula, {Chisomo L.} and Gordon, {Melita A.} and {De Pinna}, Elizabeth and John Wain and Heyderman, {Robert S.} and Stephen Obaro and Alonso, {Pedro L.} and Inacio Mandomando and MacLennan, {Calman A.} and Tapia, {Milagritos D.} and Levine, {Myron M.} and Tennant, {Sharon M.} and Julian Parkhill and Gordon Dougan",

note = "Funding Information: We thank J. Cheesborough for providing the DRC isolates, M. Okong, N. French and the Medical Research Council, Uganda, for providing the Uganda isolates, S. Nair for providing the Health Protection Agency (HPA) isolates, L. Barquist for modeling the pre-1990 HIV prevalence data and the Sequencing team at the Wellcome Trust Sanger Institute. This work was funded by a Wellcome Trust grant (098051). C.A.M. was supported by a Tropical Research Fellowship from the Wellcome Trust and a Clinical Research Fellowship from GlaxoSmithKline.",

year = "2012",

month = nov,

doi = "10.1038/ng.2423",

language = "English",

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Okoro, CK, Kingsley, RA, Connor, TR, Harris, SR, Parry, CM, Al-Mashhadani, MN, Kariuki, S, Msefula, CL, Gordon, MA, De Pinna, E, Wain, J, Heyderman, RS, Obaro, S, Alonso, PL, Mandomando, I, MacLennan, CA, Tapia, MD, Levine, MM, Tennant, SM, Parkhill, J & Dougan, G 2012, 'Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa', Nature Genetics, vol. 44, no. 11, pp. 1215-1221. https://doi.org/10.1038/ng.2423

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AU - Okoro, Chinyere K.

AU - Kingsley, Robert A.

AU - Connor, Thomas R.

AU - Harris, Simon R.

AU - Parry, Christopher M.

AU - Al-Mashhadani, Manar N.

AU - Kariuki, Samuel

AU - Msefula, Chisomo L.

AU - Gordon, Melita A.

AU - De Pinna, Elizabeth

AU - Wain, John

AU - Heyderman, Robert S.

AU - Obaro, Stephen

AU - Alonso, Pedro L.

AU - Mandomando, Inacio

AU - MacLennan, Calman A.

AU - Tapia, Milagritos D.

AU - Levine, Myron M.

AU - Tennant, Sharon M.

AU - Parkhill, Julian

AU - Dougan, Gordon

N1 - Funding Information: We thank J. Cheesborough for providing the DRC isolates, M. Okong, N. French and the Medical Research Council, Uganda, for providing the Uganda isolates, S. Nair for providing the Health Protection Agency (HPA) isolates, L. Barquist for modeling the pre-1990 HIV prevalence data and the Sequencing team at the Wellcome Trust Sanger Institute. This work was funded by a Wellcome Trust grant (098051). C.A.M. was supported by a Tropical Research Fellowship from the Wellcome Trust and a Clinical Research Fellowship from GlaxoSmithKline.

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N2 - A highly invasive form of non-typhoidal Salmonella (iNTS) disease has recently been documented in many countries in sub-Saharan Africa. The most common Salmonella enterica serovar causing this disease is Typhimurium (Salmonella Typhimurium). We applied whole-genome sequence-based phylogenetic methods to define the population structure of sub-Saharan African invasive Salmonella Typhimurium isolates and compared these to global Salmonella Typhimurium populations. Notably, the vast majority of sub-Saharan invasive Salmonella Typhimurium isolates fell within two closely related, highly clustered phylogenetic lineages that we estimate emerged independently ∼52 and ∼35 years ago in close temporal association with the current HIV pandemic. Clonal replacement of isolates from lineage I by those from lineage II was potentially influenced by the use of chloramphenicol for the treatment of iNTS disease. Our analysis suggests that iNTS disease is in part an epidemic in sub-Saharan Africa caused by highly related Salmonella Typhimurium lineages that may have occupied new niches associated with a compromised human population and antibiotic treatment.

AB - A highly invasive form of non-typhoidal Salmonella (iNTS) disease has recently been documented in many countries in sub-Saharan Africa. The most common Salmonella enterica serovar causing this disease is Typhimurium (Salmonella Typhimurium). We applied whole-genome sequence-based phylogenetic methods to define the population structure of sub-Saharan African invasive Salmonella Typhimurium isolates and compared these to global Salmonella Typhimurium populations. Notably, the vast majority of sub-Saharan invasive Salmonella Typhimurium isolates fell within two closely related, highly clustered phylogenetic lineages that we estimate emerged independently ∼52 and ∼35 years ago in close temporal association with the current HIV pandemic. Clonal replacement of isolates from lineage I by those from lineage II was potentially influenced by the use of chloramphenicol for the treatment of iNTS disease. Our analysis suggests that iNTS disease is in part an epidemic in sub-Saharan Africa caused by highly related Salmonella Typhimurium lineages that may have occupied new niches associated with a compromised human population and antibiotic treatment.

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Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa

Abstract

Bibliographical note

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