Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings

Nicholas A Feasey; James Hadfield; Karen H. Keddy; Timothy J Dallman; Jan Jacobs; Xiangyu Deng; Paul Wigley; Lars Barquist Barquist; Gemma C Langridge; Theresa Feltwell; Alison E Mather; Maria Fookes; Martin Aslett; Chisomo Msefula; Samuel Kariuki; Calman A Maclennan; Robert S Onsare; François-Xavier Weill; Simon Le Hello; Michael McClelland; Prerak Desai; Christopher M Parry; John Cheesbrough; Neil French; Josefina Campos; Jose A Chabalgoity; Laura Betancor; Katie L Hopkins; Satheesh Nair; Octavie Lunguya; Tristan A Cogan; Milagritos D Tapia; Samba O Sow; Sharon M Tennant; Kristin Bornstein; Myron M Levine; Dean B Everett; Robert A Kingsley; Julian Parkhill; Gordon Dougan; Melita A Gordon; Nicholas R Thomson

doi:10.1038/ng.3644

Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings

Nicholas A Feasey, James Hadfield, Karen H. Keddy, Timothy J Dallman, Jan Jacobs, Xiangyu Deng, Paul Wigley, Lars Barquist Barquist, Gemma C Langridge, Theresa Feltwell, Alison E Mather, Maria Fookes, Martin Aslett, Chisomo Msefula, Samuel Kariuki, Calman A Maclennan, Robert S Onsare, François-Xavier Weill, Simon Le Hello, Michael McClellandPrerak Desai, Christopher M Parry, John Cheesbrough, Neil French, Josefina Campos, Jose A Chabalgoity, Laura Betancor, Katie L Hopkins, Satheesh Nair, Octavie Lunguya, Tristan A Cogan, Milagritos D Tapia, Samba O Sow, Sharon M Tennant, Kristin Bornstein, Myron M Levine, Dean B Everett, Robert A Kingsley, Julian Parkhill, Gordon Dougan, Melita A Gordon, Nicholas R Thomson

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Abstract

An epidemiological paradox surrounds Salmonella enterica serovar Enteritidis. In high-income settings, it has been responsible for an epidemic of poultry-associated, self-limiting enterocolitis, whereas in sub-Saharan Africa it is a major cause of invasive nontyphoidal Salmonella disease, associated with high case fatality. By whole-genome sequence analysis of 675 isolates of S. Enteritidis from 45 countries, we show the existence of a global epidemic clade and two new clades of S. Enteritidis that are geographically restricted to distinct regions of Africa. The African isolates display genomic degradation, a novel prophage repertoire, and an expanded multidrug resistance plasmid. S. Enteritidis is a further example of a Salmonella serotype that displays niche plasticity, with distinct clades that enable it to become a prominent cause of gastroenteritis in association with the industrial production of eggs and of multidrug-resistant, bloodstream-invasive infection in Africa.

Original language	English
Pages (from-to)	1211-1217
Number of pages	7
Journal	Nature Genetics
Volume	48
Issue number	10
Early online date	22 Aug 2016
DOIs	https://doi.org/10.1038/ng.3644
Publication status	Published - Oct 2016

Keywords

Bacterial infection
Genomics
Microbial genetics

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10.1038/ng.3644

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Supplementary Information XLS - Tables
This is the author accepted manuscript (AAM). The final published version (version of record) is available online via Nature at http://www.nature.com/ng/journal/v48/n10/full/ng.3644.html. Please refer to any applicable terms of use of the publisher.
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Dr Tristan A Cogan
- Tristan.Coganbristol.acuk
- Bristol Veterinary School - Senior Lecturer in Infectious Diseases, Lecturer in Infectious Diseases
- Infection and Immunity (Including Veterinary Public Health and Meat Quality)
- Infection and Immunity
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Cite this

Feasey, N. A., Hadfield, J., Keddy, K. H., Dallman, T. J., Jacobs, J., Deng, X., Wigley, P., Barquist Barquist, L., Langridge, G. C., Feltwell, T., Mather, A. E., Fookes, M., Aslett, M., Msefula, C., Kariuki, S., Maclennan, C. A., Onsare, R. S., Weill, F-X., Le Hello, S., ... Thomson, N. R. (2016). Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings. Nature Genetics, 48(10), 1211-1217. https://doi.org/10.1038/ng.3644

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title = "Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings",

abstract = "An epidemiological paradox surrounds Salmonella enterica serovar Enteritidis. In high-income settings, it has been responsible for an epidemic of poultry-associated, self-limiting enterocolitis, whereas in sub-Saharan Africa it is a major cause of invasive nontyphoidal Salmonella disease, associated with high case fatality. By whole-genome sequence analysis of 675 isolates of S. Enteritidis from 45 countries, we show the existence of a global epidemic clade and two new clades of S. Enteritidis that are geographically restricted to distinct regions of Africa. The African isolates display genomic degradation, a novel prophage repertoire, and an expanded multidrug resistance plasmid. S. Enteritidis is a further example of a Salmonella serotype that displays niche plasticity, with distinct clades that enable it to become a prominent cause of gastroenteritis in association with the industrial production of eggs and of multidrug-resistant, bloodstream-invasive infection in Africa.",

keywords = "Bacterial infection, Genomics, Microbial genetics",

author = "Feasey, {Nicholas A} and James Hadfield and Keddy, {Karen H.} and Dallman, {Timothy J} and Jan Jacobs and Xiangyu Deng and Paul Wigley and {Barquist Barquist}, Lars and Langridge, {Gemma C} and Theresa Feltwell and Mather, {Alison E} and Maria Fookes and Martin Aslett and Chisomo Msefula and Samuel Kariuki and Maclennan, {Calman A} and Onsare, {Robert S} and Fran{\c c}ois-Xavier Weill and {Le Hello}, Simon and Michael McClelland and Prerak Desai and Parry, {Christopher M} and John Cheesbrough and Neil French and Josefina Campos and Chabalgoity, {Jose A} and Laura Betancor and Hopkins, {Katie L} and Satheesh Nair and Octavie Lunguya and Cogan, {Tristan A} and Tapia, {Milagritos D} and Sow, {Samba O} and Tennant, {Sharon M} and Kristin Bornstein and Levine, {Myron M} and Everett, {Dean B} and Kingsley, {Robert A} and Julian Parkhill and Gordon Dougan and Gordon, {Melita A} and Thomson, {Nicholas R}",

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Feasey, NA, Hadfield, J, Keddy, KH, Dallman, TJ, Jacobs, J, Deng, X, Wigley, P, Barquist Barquist, L, Langridge, GC, Feltwell, T, Mather, AE, Fookes, M, Aslett, M, Msefula, C, Kariuki, S, Maclennan, CA, Onsare, RS, Weill, F-X, Le Hello, S, McClelland, M, Desai, P, Parry, CM, Cheesbrough, J, French, N, Campos, J, Chabalgoity, JA, Betancor, L, Hopkins, KL, Nair, S, Lunguya, O, Cogan, TA, Tapia, MD, Sow, SO, Tennant, SM, Bornstein, K, Levine, MM, Everett, DB, Kingsley, RA, Parkhill, J, Dougan, G, Gordon, MA & Thomson, NR 2016, 'Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings', Nature Genetics, vol. 48, no. 10, pp. 1211-1217. https://doi.org/10.1038/ng.3644

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AU - Feasey, Nicholas A

AU - Hadfield, James

AU - Keddy, Karen H.

AU - Dallman, Timothy J

AU - Jacobs, Jan

AU - Deng, Xiangyu

AU - Wigley, Paul

AU - Barquist Barquist, Lars

AU - Langridge, Gemma C

AU - Feltwell, Theresa

AU - Mather, Alison E

AU - Fookes, Maria

AU - Aslett, Martin

AU - Msefula, Chisomo

AU - Kariuki, Samuel

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AU - Onsare, Robert S

AU - Weill, François-Xavier

AU - Le Hello, Simon

AU - McClelland, Michael

AU - Desai, Prerak

AU - Parry, Christopher M

AU - Cheesbrough, John

AU - French, Neil

AU - Campos, Josefina

AU - Chabalgoity, Jose A

AU - Betancor, Laura

AU - Hopkins, Katie L

AU - Nair, Satheesh

AU - Lunguya, Octavie

AU - Cogan, Tristan A

AU - Tapia, Milagritos D

AU - Sow, Samba O

AU - Tennant, Sharon M

AU - Bornstein, Kristin

AU - Levine, Myron M

AU - Everett, Dean B

AU - Kingsley, Robert A

AU - Parkhill, Julian

AU - Dougan, Gordon

AU - Gordon, Melita A

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N2 - An epidemiological paradox surrounds Salmonella enterica serovar Enteritidis. In high-income settings, it has been responsible for an epidemic of poultry-associated, self-limiting enterocolitis, whereas in sub-Saharan Africa it is a major cause of invasive nontyphoidal Salmonella disease, associated with high case fatality. By whole-genome sequence analysis of 675 isolates of S. Enteritidis from 45 countries, we show the existence of a global epidemic clade and two new clades of S. Enteritidis that are geographically restricted to distinct regions of Africa. The African isolates display genomic degradation, a novel prophage repertoire, and an expanded multidrug resistance plasmid. S. Enteritidis is a further example of a Salmonella serotype that displays niche plasticity, with distinct clades that enable it to become a prominent cause of gastroenteritis in association with the industrial production of eggs and of multidrug-resistant, bloodstream-invasive infection in Africa.

AB - An epidemiological paradox surrounds Salmonella enterica serovar Enteritidis. In high-income settings, it has been responsible for an epidemic of poultry-associated, self-limiting enterocolitis, whereas in sub-Saharan Africa it is a major cause of invasive nontyphoidal Salmonella disease, associated with high case fatality. By whole-genome sequence analysis of 675 isolates of S. Enteritidis from 45 countries, we show the existence of a global epidemic clade and two new clades of S. Enteritidis that are geographically restricted to distinct regions of Africa. The African isolates display genomic degradation, a novel prophage repertoire, and an expanded multidrug resistance plasmid. S. Enteritidis is a further example of a Salmonella serotype that displays niche plasticity, with distinct clades that enable it to become a prominent cause of gastroenteritis in association with the industrial production of eggs and of multidrug-resistant, bloodstream-invasive infection in Africa.

KW - Bacterial infection

KW - Genomics

KW - Microbial genetics

U2 - 10.1038/ng.3644

DO - 10.1038/ng.3644

M3 - Article (Academic Journal)

C2 - 27548315

SN - 1061-4036

VL - 48

SP - 1211

EP - 1217

JO - Nature Genetics

JF - Nature Genetics

IS - 10

ER -

Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings

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Keywords

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