Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings
Open accessAbstract
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.
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The single serotype Enteritidis isolate MARG-18AL-BROO belonged to the invasive MDR West African clade.
“Our single isolate of serotype Enteritidis, recovered from a beef kebab sandwich, therefore belonged to the invasive MDR West African clade (Fig 2).”
From Contamination of street food with multidrug-resistant Salmonella, in Ouagadougou, Burkina Faso (2021) · cites this paper as [15]
The Phylogeny section describes a West African S. Enteritidis clade strongly associated with invasive disease and antimicrobial resistance. It does not identify MARG-18AL-BROO or establish that the kebab-sandwich isolate belongs to that clade; that placement appears to be the citing authors’ own finding. (LLM, conf=0.85)
Experimental — accuracy not yet measuredFeasey et al. described a MDR plasmid, pSEN-BT, in the West African clade of S. enterica serotype Enteritidis.
“Feasey et al. [15] also described a MDR plasmid, pSEN-BT, in the West African clade of S. enterica serotype Enteritidis.”
From Contamination of street food with multidrug-resistant Salmonella, in Ouagadougou, Burkina Faso (2021) · cites this paper as [15]
In “Contribution of the accessory genome” (page unavailable), the paper names pSEN-BT and reports that it carries nine antimicrobial-resistance genes. But it identifies pSEN-BT as the plasmid sequenced from isolate D7795; elsewhere, D7795 is identified as belonging to the Central/Eastern African clade, not the West African clade. (LLM, conf=0.90)
Experimental — accuracy not yet measuredThe African invasive isolates showed a pattern of genomic degradation characteristic of adaptation to human hosts.
“These African invasive isolates showed a pattern of genomic degradation characteristic of adaptation to human hosts.”
From Contamination of street food with multidrug-resistant Salmonella, in Ouagadougou, Burkina Faso (2021) · cites this paper as [15]
The ‘Multiple signatures of differential host adaptation’ section reports disrupted genes in the African invasive clades and describes degradation of these pathways as a marker of a shift toward an invasive lifestyle (page unavailable). The concluding section compares their degradation with host-restricted Salmonella but leaves open whether the clades occupy different niches outside humans or behave differently within them. It therefore does not establish adaptation specifically to human hosts. (LLM, conf=0.85)
Experimental — accuracy not yet measuredFeasey et al. used WGS to study 675 isolates of S. enterica serotype Enteritidis from 45 countries, and revealed a global epidemic clade and two invasive clades restricted to different regions of Africa.
“Feasey et al. [15] used WGS to study 675 isolates of S. enterica serotype Enteritidis from 45 countries, and revealed the existence of a global epidemic clade and two invasive clades restricted to different regions of Africa.”
From Contamination of street food with multidrug-resistant Salmonella, in Ouagadougou, Burkina Faso (2021) · cites this paper as [15]
Strains from the West African clade had various antimicrobial drug resistance profiles, but their plasmids characteristically carried catA1, whereas strains from Central and East Africa carried catA2.
“Strains from this clade had various antimicrobial drug resistance profiles, but their plasmids characteristically carried the chloramphenicol resistance gene, catA1 –as observed for serotype Enteritidis in our study–whereas strains from Central and East Africa carried catA2 [15].”
From Contamination of street food with multidrug-resistant Salmonella, in Ouagadougou, Burkina Faso (2021) · cites this paper as [15]
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- Authors
- Feasey, N. A., Hadfield, J., Keddy, K. H., Dallman, T. J., Jacobs, J., Deng, X., Wigley, P., Barquist, L., Langridge, G. C., Feltwell, T., Harris, S. R., Mather, A. E., Fookes, M., Aslett, M., Msefula, C., Kariuki, S., Maclennan, C. A., Onsare, R. S., Weill, F.-X., Le Hello, S., Smith, A. M., McClelland, M., Desai, P., Parry, C. M., Cheesbrough, J., French, N., Campos, J., Chabalgoity, J. A., Betancor, L., Hopkins, K. L., Nair, S., Humphrey, T. J., Lunguya, O., Cogan, T. A., Tapia, M. D., Sow, S. O., Tennant, S. M., Bornstein, K., Levine, M. M., Lacharme-Lora, L., Everett, D. B., Kingsley, R. A., Parkhill, J., Heyderman, R. S., Dougan, G., Gordon, M. A., & Thomson, N. R.
- Affiliations
- University of Liverpool (GB)
- Wellcome Sanger Institute (GB)
- University of the Witwatersrand (ZA)
- Public Health England (GB)
- Instituut voor Tropische Geneeskunde (BE)
- Centers for Disease Control and Prevention (US)
- University of Würzburg (DE)
- University of Malawi (MW)
- Kenya Medical Research Institute (KE)
- Institut Pasteur (FR)
- National Institute for Communicable Diseases (ZA)
- University of California, Irvine (US)
- Liverpool School of Tropical Medicine (GB)
- Administración Nacional de Laboratorios e Institutos de Salud (AR)
- Universidad de la República de Uruguay (UY)
- Swansea University (GB)
- National Institute of Biomedical Research (CD)
- University of Bristol (GB)
- University of Maryland, Baltimore (US)
- Centre Pour le Développement des Vaccins-Mali (ML)
- Corresponding author
- Feasey, Nicholas A
- ORCID
- Feasey, Nicholas A
- Hadfield, James
- Keddy, Karen H
- Dallman, Timothy J
- Jacobs, Jan
- Deng, Xiangyu
- Wigley, Paul
- Barquist, Lars
- Langridge, Gemma C
- Feltwell, Theresa
- Harris, Simon R
- Mather, Alison E
- Msefula, Chisomo
- Kariuki, Samuel
- Maclennan, Calman A
- Weill, François-Xavier
- McClelland, Michael
- Desai, Prerak
- Parry, Christopher M
- French, Neil
- Campos, Josefina
- Chabalgoity, Jose A
- Hopkins, Katie L
- Nair, Satheesh
- Lunguya, Octavie
- Cogan, Tristan A
- Tapia, Milagritos D
- Sow, Samba O
- Tennant, Sharon M
- Levine, Myron M
- Everett, Dean B
- Kingsley, Robert A
- Parkhill, Julian
- Heyderman, Robert S
- Gordon, Melita A
- Thomson, Nicholas R
- Venue
- Nature Genetics
- Published
- 2016-08-22
- Volume
- 48
- Issue
- 10
- Pages
- 1211-1217
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC5047355
- OpenAlex
- W2513615729
- Semantic Scholar
- 8c0c50157e1696983b240f388e19d4fce6caae87
- Cited by
- 217
- References
- 63
- Citations by year
- 2026: 17 · 2025: 19 · 2024: 15 · 2023: 26 · 2022: 16 · 2021: 33 · 2020: 26 · 2019: 24 · 2018: 25 · 2017: 14 · 2016: 2
- FWCI
- 27.28
- Type
- journal article
- Language
- en
- Update notices
- erratum (2017-04-01)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Bristol Research (University of Bristol) (publishedVersion, other-oa)
- LSTM Online Archive (Liverpool School of Tropical Medicine) (acceptedVersion)
- UEA Digital Repository (University of East Anglia) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Explore Bristol Research (acceptedVersion, other-oa)
- LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- HAL (submittedVersion, other-oa)
- UCL Discovery (University College London) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Apollo
- Funders
- Wellcome Trust (101113, 095967/Z/11/Z, 092152, 100891, WT092152MA, 101113/Z/13/Z, 100891/Z/13/Z, 098051)
- Instituut voor Tropische Geneeskunde
- University of Cambridge
- Agence Nationale de la Recherche (10-LABX-62-IBEID, ANR‐10‐LABX‐62‐IBEID, ANR-10, ANR-10-LABX-0062, grant ANR-10-LABX-62-IBEID, ANR-10-LABX-62)
- Institut de Veille Sanitaire
- National Institutes of Health
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council (BB/M014088/1)
- National Institute of Allergy and Infectious Diseases (R01AI099525)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Life Sciences › Immunology and Microbiology › Microbiology › Bacterial Infections and Vaccines
- Keywords
- Salmonella Enteritidis, bacterial lineages, enterocolitis, sub-Saharan Africa, multidrug resistance plasmids, case fatality
- MeSH terms
- Adaptation, Biological, Animals, Chickens, Enterocolitis, Female, Humans, Income, Plasmids, Poultry Diseases, Salmonella enteritidis, Salmonella Infections, Genome, Bacterial, Sequence Analysis, DNA, Africa South of the Sahara, Epidemics
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