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

doi:10.1038/ng.3644

. 2016 Oct;48(10):1211-1217.

doi: 10.1038/ng.3644. Epub 2016 Aug 22.

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

Nicholas A Feasey ^{1

2

3

4}, James Hadfield ², Karen H Keddy ^{5

6}, Timothy J Dallman ⁷, Jan Jacobs ^{8

9}, Xiangyu Deng ^{10

11}, Paul Wigley ⁴, Lars Barquist ¹², Gemma C Langridge ², Theresa Feltwell ², Simon R Harris ², Alison E Mather ², Maria Fookes ², Martin Aslett ², Chisomo Msefula ^{3

13}, Samuel Kariuki ¹⁴, Calman A Maclennan ^{2

15}, Robert S Onsare ¹⁴, François-Xavier Weill ¹⁶, Simon Le Hello ¹⁶, Anthony M Smith ⁵, Michael McClelland ¹⁷, Prerak Desai ¹⁷, Christopher M Parry ^{1

18}, John Cheesbrough ¹⁹, Neil French ⁴, Josefina Campos ²⁰, Jose A Chabalgoity ²¹, Laura Betancor ²¹, Katie L Hopkins ²², Satheesh Nair ⁷, Tom J Humphrey ²³, Octavie Lunguya ^{24

25}, Tristan A Cogan ²⁶, Milagritos D Tapia ²⁷, Samba O Sow ²⁸, Sharon M Tennant ²⁷, Kristin Bornstein ²⁷, Myron M Levine ²⁷, Lizeth Lacharme-Lora ⁴, Dean B Everett ⁴, Robert A Kingsley ^{2

29}, Julian Parkhill ², Robert S Heyderman ^{3

30}, Gordon Dougan ², Melita A Gordon ^#^{3

4}, Nicholas R Thomson ^#^{2

18}

Affiliations

¹ Liverpool School of Tropical Medicine, Liverpool, UK.
² Wellcome Trust Sanger Institute, Cambridge, UK.
³ Malawi Liverpool Wellcome Trust Clinical Research Programme, University of Malawi College of Medicine, Blantyre, Malawi.
⁴ Institute of Infection and Global Health, University of Liverpool, Liverpool, UK.
⁵ Centre for Enteric Diseases, National Institute for Communicable Diseases, Johannesburg, South Africa.
⁶ Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
⁷ Gastrointestinal Bacteria Reference Unit, Public Health England, Colindale, UK.
⁸ Institute of Tropical Medicine, Antwerp, Belgium.
⁹ Department of Microbiology and Immunology, University of Leuven, Belgium.
¹⁰ Center for Food Safety, Department of Food Science and Technology, University of Georgia.
¹¹ Centers for Disease Control and Prevention, Atlanta, USA.
¹² Institute for Molecular Infection Biology, University of Würzburg, Würzburg, Germany.
¹³ University of Malawi, The College of Medicine, Blantyre, Malawi.
¹⁴ Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya.
¹⁵ Jenner Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK.
¹⁶ Institut Pasteur, Paris, France.
¹⁷ Department of Microbiology and Molecular Genetics, University of California, Irvine, CA, USA.
¹⁸ London School of Hygiene & Tropical Medicine, London, UK.
¹⁹ Department of Epidemiology and Population Health, University of Liverpool, Liverpool, UK.
²⁰ Enteropathogen Division, Administración Nacional de Laboratorios e Institutos de Salud (ANLIS) Carlos G. Malbran Institute, Buenos Aires, Argentina.
²¹ Instituto de Higiene, Facultad de Medicina, Universidad de la Republica, Uruguay.
²² Antimicrobial Resistance and Healthcare-Associated Infections Reference Unit, Public Health England, Colindale, UK.
²³ Swansea Medical School, Swansea University, Swansea, UK.
²⁴ National Institute of Biomedical Research, Kinshasa, the Democratic Republic of the Congo.
²⁵ University Hospital of Kinshasa, Kinshasa, the Democratic Republic of the Congo.
²⁶ School of Veterinary Sciences, University of Bristol, Bristol, UK.
²⁷ Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland, USA.
²⁸ Centre pour le Développement des Vaccins, Bamako, Mali.
²⁹ Institute of Food Research, Colney, Norwich, UK.
³⁰ Division of Infection and Immunity, University College London, London, UK.

^# Contributed equally.

PMID: 27548315
PMCID: PMC5047355
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 et al. Nat Genet. 2016 Oct.

. 2016 Oct;48(10):1211-1217.

doi: 10.1038/ng.3644. Epub 2016 Aug 22.

Authors

Nicholas A Feasey ^{1

2

3

4}, James Hadfield ², Karen H Keddy ^{5

6}, Timothy J Dallman ⁷, Jan Jacobs ^{8

9}, Xiangyu Deng ^{10

11}, Paul Wigley ⁴, Lars Barquist ¹², Gemma C Langridge ², Theresa Feltwell ², Simon R Harris ², Alison E Mather ², Maria Fookes ², Martin Aslett ², Chisomo Msefula ^{3

13}, Samuel Kariuki ¹⁴, Calman A Maclennan ^{2

15}, Robert S Onsare ¹⁴, François-Xavier Weill ¹⁶, Simon Le Hello ¹⁶, Anthony M Smith ⁵, Michael McClelland ¹⁷, Prerak Desai ¹⁷, Christopher M Parry ^{1

18}, John Cheesbrough ¹⁹, Neil French ⁴, Josefina Campos ²⁰, Jose A Chabalgoity ²¹, Laura Betancor ²¹, Katie L Hopkins ²², Satheesh Nair ⁷, Tom J Humphrey ²³, Octavie Lunguya ^{24

25}, Tristan A Cogan ²⁶, Milagritos D Tapia ²⁷, Samba O Sow ²⁸, Sharon M Tennant ²⁷, Kristin Bornstein ²⁷, Myron M Levine ²⁷, Lizeth Lacharme-Lora ⁴, Dean B Everett ⁴, Robert A Kingsley ^{2

29}, Julian Parkhill ², Robert S Heyderman ^{3

30}, Gordon Dougan ², Melita A Gordon ^#^{3

4}, Nicholas R Thomson ^#^{2

18}

Affiliations

¹ Liverpool School of Tropical Medicine, Liverpool, UK.
² Wellcome Trust Sanger Institute, Cambridge, UK.
³ Malawi Liverpool Wellcome Trust Clinical Research Programme, University of Malawi College of Medicine, Blantyre, Malawi.
⁴ Institute of Infection and Global Health, University of Liverpool, Liverpool, UK.
⁵ Centre for Enteric Diseases, National Institute for Communicable Diseases, Johannesburg, South Africa.
⁶ Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
⁷ Gastrointestinal Bacteria Reference Unit, Public Health England, Colindale, UK.
⁸ Institute of Tropical Medicine, Antwerp, Belgium.
⁹ Department of Microbiology and Immunology, University of Leuven, Belgium.
¹⁰ Center for Food Safety, Department of Food Science and Technology, University of Georgia.
¹¹ Centers for Disease Control and Prevention, Atlanta, USA.
¹² Institute for Molecular Infection Biology, University of Würzburg, Würzburg, Germany.
¹³ University of Malawi, The College of Medicine, Blantyre, Malawi.
¹⁴ Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya.
¹⁵ Jenner Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK.
¹⁶ Institut Pasteur, Paris, France.
¹⁷ Department of Microbiology and Molecular Genetics, University of California, Irvine, CA, USA.
¹⁸ London School of Hygiene & Tropical Medicine, London, UK.
¹⁹ Department of Epidemiology and Population Health, University of Liverpool, Liverpool, UK.
²⁰ Enteropathogen Division, Administración Nacional de Laboratorios e Institutos de Salud (ANLIS) Carlos G. Malbran Institute, Buenos Aires, Argentina.
²¹ Instituto de Higiene, Facultad de Medicina, Universidad de la Republica, Uruguay.
²² Antimicrobial Resistance and Healthcare-Associated Infections Reference Unit, Public Health England, Colindale, UK.
²³ Swansea Medical School, Swansea University, Swansea, UK.
²⁴ National Institute of Biomedical Research, Kinshasa, the Democratic Republic of the Congo.
²⁵ University Hospital of Kinshasa, Kinshasa, the Democratic Republic of the Congo.
²⁶ School of Veterinary Sciences, University of Bristol, Bristol, UK.
²⁷ Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland, USA.
²⁸ Centre pour le Développement des Vaccins, Bamako, Mali.
²⁹ Institute of Food Research, Colney, Norwich, UK.
³⁰ Division of Infection and Immunity, University College London, London, UK.

^# Contributed equally.

PMID: 27548315
PMCID: PMC5047355
DOI: 10.1038/ng.3644

Erratum in

Erratum: Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings.
Feasey NA, Hadfield J, Keddy KH, Dallman TJ, Jacobs J, Deng X, Wigley P, Barquist L, Langridge GC, Feltwell T, Harris SR, Mather AE, Fookes M, Aslett M, Msefula C, Kariuki S, Maclennan CA, Onsare RS, Weill FX, Le Hello S, Smith AM, McClelland M, Desai P, Parry CM, Cheesbrough J, French N, Campos J, Chabalgoity JA, Betancor L, Hopkins KL, Nair S, Humphrey TJ, Lunguya O, Cogan TA, Tapia MD, Sow SO, Tennant SM, Bornstein K, Levine MM, Lacharme-Lora L, Everett DB, Kingsley RA, Parkhill J, Heyderman RS, Dougan G, Gordon MA, Thomson NR. Feasey NA, et al. Nat Genet. 2017 Mar 30;49(4):651. doi: 10.1038/ng0417-651c. Nat Genet. 2017. PMID: 28358127 No abstract available.

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.

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Conflict of interest statement

Competing financial interests: The authors declare no competing financial interests.

Figures

Figure 1

Figure 1

Maximum likelihood phylogeny of S. Enteritidis based on 675 isolates rooted to S. Gallinarum. There are 3 epidemic clades; 2 African epidemic clades and a global epidemic clade. Scale bar indicates nucleotide substitutions per site.

Figure 2

Figure 2

Differences in accessory genomes of 4 major clades. Approximate position of prophages in chromosome is depicted, although prophages are not drawn to scale

Figure 3

Figure 3

Heat map revealing changes in metabolic activity of Central/Eastern African clade isolate D7795 when compared to global epidemic isolate A1636 at 28 and 37°C. The figure also displays whether there are corresponding mutations in genes related to the affected metabolic pathway. (NSSNP=Non-synonymous single nucleotide polymorphism, HDG = Hypothetically disrupted gene)

Figure 4

Figure 4

Salmonella isolation from a chick infection model demonstrates failure of Central/Eastern African clade isolate to invade chicken spleen (4A) and liver (4B) or to colonize chicken caeca (4C) at 7 days post infection (dpi) (n=24 at this time point) compared to the global epidemic clade. Numbers are expressed as colony forming units (CFU) per gram of tissue

See this image and copyright information in PMC

Comment in

Infection: Distinct Salmonella Enteritidis lineages dictate disease in different settings.
Ray K. Ray K. Nat Rev Gastroenterol Hepatol. 2016 Oct;13(10):558. doi: 10.1038/nrgastro.2016.152. Epub 2016 Sep 14. Nat Rev Gastroenterol Hepatol. 2016. PMID: 27625196 No abstract available.

References

1. Ward LR, Threlfall J, Smith HR, O'Brien SJ. Salmonella enteritidis epidemic. Science. 2000;287:1753–4. author reply 1755-6. - PubMed
1. Jones TF, et al. Salmonellosis outcomes differ substantially by serotype. J Infect Dis. 2008;198:109–14. - PubMed
1. O'Brien SJ. The "decline and fall" of nontyphoidal salmonella in the United kingdom. Clin Infect Dis. 2013;56:705–10. - PMC - PubMed
1. Braden CR. Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis. 2006;43:512–7. - PubMed
1. Friedman CR, Malcolm G, Rigau-Perez JG, Arambulo P, 3rd, Tauxe RV. Public health risk from Salmonella-based rodenticides. Lancet. 1996;347:1705–6. - PubMed

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[1] Ward LR, Threlfall J, Smith HR, O'Brien SJ. Salmonella enteritidis epidemic. Science. 2000;287:1753–4. author reply 1755-6. - PubMed

[2] Ward LR, Threlfall J, Smith HR, O'Brien SJ. Salmonella enteritidis epidemic. Science. 2000;287:1753–4. author reply 1755-6. - PubMed

[3] Jones TF, et al. Salmonellosis outcomes differ substantially by serotype. J Infect Dis. 2008;198:109–14. - PubMed

[4] Jones TF, et al. Salmonellosis outcomes differ substantially by serotype. J Infect Dis. 2008;198:109–14. - PubMed

[5] O'Brien SJ. The "decline and fall" of nontyphoidal salmonella in the United kingdom. Clin Infect Dis. 2013;56:705–10. - PMC - PubMed

[6] O'Brien SJ. The "decline and fall" of nontyphoidal salmonella in the United kingdom. Clin Infect Dis. 2013;56:705–10. - PMC - PubMed

[7] Braden CR. Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis. 2006;43:512–7. - PubMed

[8] Braden CR. Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis. 2006;43:512–7. - PubMed

[9] Friedman CR, Malcolm G, Rigau-Perez JG, Arambulo P, 3rd, Tauxe RV. Public health risk from Salmonella-based rodenticides. Lancet. 1996;347:1705–6. - PubMed

[10] Friedman CR, Malcolm G, Rigau-Perez JG, Arambulo P, 3rd, Tauxe RV. Public health risk from Salmonella-based rodenticides. Lancet. 1996;347:1705–6. - PubMed

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

Affiliations

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

Authors

Affiliations

Erratum in

Abstract

Conflict of interest statement

Figures

Comment in

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Medical