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Geographical migration and fitness dynamics of Streptococcus pneumoniae

Geographical migration and fitness dynamics of Streptococcus pneumoniae
Geographical migration and fitness dynamics of Streptococcus pneumoniae
Streptococcus pneumoniae is a leading cause of pneumonia and meningitis worldwide. Many different serotypes co-circulate endemically in any one location1,2. The extent and mechanisms of spread and vaccine-driven changes in fitness and antimicrobial resistance remain largely unquantified. Here using geolocated genome sequences from South Africa (n = 6,910, collected from 2000 to 2014), we developed models to reconstruct spread, pairing detailed human mobility data and genomic data. Separately, we estimated the population-level changes in fitness of strains that are included (vaccine type (VT)) and not included (non-vaccine type (NVT)) in pneumococcal conjugate vaccines, first implemented in South Africa in 2009. Differences in strain fitness between those that are and are not resistant to penicillin were also evaluated. We found that pneumococci only become homogenously mixed across South Africa after 50 years of transmission, with the slow spread driven by the focal nature of human mobility. Furthermore, in the years following vaccine implementation, the relative fitness of NVT compared with VT strains increased (relative risk of 1.68; 95% confidence interval of 1.59–1.77), with an increasing proportion of these NVT strains becoming resistant to penicillin. Our findings point to highly entrenched, slow transmission and indicate that initial vaccine-linked decreases in antimicrobial resistance may be transient.
0028-0836
386-392
Belman, Sophie
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Lefrancq, Noémie
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Nzenze, Susan
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Downs, Sarah
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du Plessis, Mignon
b142a817-ef0b-496f-ab57-7364e4b1af0c
Lo, Stephanie W.
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Clarke, Stuart C.
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McGee, Lesley
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Madhi, Shabir A.
dbe03afd-0de6-49c6-b31c-f952193ebc62
Von Gottberg, Anne
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Bentley, Stephen D
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Salje, Henrik
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The Global Pneumococcal Sequencing Consortium
Belman, Sophie
808b4418-8516-4412-b6a7-3c064ab849c1
Lefrancq, Noémie
e71373d1-f686-4a75-ac9f-24245b42e107
Nzenze, Susan
4be73003-6f35-42f5-86a7-734f197611d1
Downs, Sarah
472922be-fe3a-42d0-8745-b471c165308f
du Plessis, Mignon
b142a817-ef0b-496f-ab57-7364e4b1af0c
Lo, Stephanie W.
607ccad6-93b1-484c-ba8d-9821432fce90
Clarke, Stuart C.
f7d7f7a2-4b1f-4b36-883a-0f967e73fb17
McGee, Lesley
8b2b4ed5-fb63-4e8f-a9b1-ee14573daab0
Madhi, Shabir A.
dbe03afd-0de6-49c6-b31c-f952193ebc62
Von Gottberg, Anne
2e435fdc-f9f3-4c37-b96a-f4d5184661f0
Bentley, Stephen D
438443a4-8033-4a5d-a5a5-538dbd4e8d60
Salje, Henrik
750b91a7-336b-4d71-81cf-e0e6dead932b

Belman, Sophie, Lefrancq, Noémie, Nzenze, Susan, Downs, Sarah, du Plessis, Mignon, Lo, Stephanie W., McGee, Lesley, Madhi, Shabir A., Von Gottberg, Anne, Bentley, Stephen D and Salje, Henrik , The Global Pneumococcal Sequencing Consortium (2024) Geographical migration and fitness dynamics of Streptococcus pneumoniae. Nature, 631 (8020), 386-392. (doi:10.1038/s41586-024-07626-3).

Record type: Article

Abstract

Streptococcus pneumoniae is a leading cause of pneumonia and meningitis worldwide. Many different serotypes co-circulate endemically in any one location1,2. The extent and mechanisms of spread and vaccine-driven changes in fitness and antimicrobial resistance remain largely unquantified. Here using geolocated genome sequences from South Africa (n = 6,910, collected from 2000 to 2014), we developed models to reconstruct spread, pairing detailed human mobility data and genomic data. Separately, we estimated the population-level changes in fitness of strains that are included (vaccine type (VT)) and not included (non-vaccine type (NVT)) in pneumococcal conjugate vaccines, first implemented in South Africa in 2009. Differences in strain fitness between those that are and are not resistant to penicillin were also evaluated. We found that pneumococci only become homogenously mixed across South Africa after 50 years of transmission, with the slow spread driven by the focal nature of human mobility. Furthermore, in the years following vaccine implementation, the relative fitness of NVT compared with VT strains increased (relative risk of 1.68; 95% confidence interval of 1.59–1.77), with an increasing proportion of these NVT strains becoming resistant to penicillin. Our findings point to highly entrenched, slow transmission and indicate that initial vaccine-linked decreases in antimicrobial resistance may be transient.

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Accepted/In Press date: 30 May 2024
e-pub ahead of print date: 3 July 2024
Published date: 11 July 2024

Identifiers

Local EPrints ID: 501272
URI: http://eprints.soton.ac.uk/id/eprint/501272
ISSN: 0028-0836
PURE UUID: 15eff2a0-5d4b-4e49-b7f8-a564a9534411
ORCID for Stuart C. Clarke: ORCID iD orcid.org/0000-0002-7009-1548

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Date deposited: 28 May 2025 16:37
Last modified: 29 May 2025 01:42

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Contributors

Author: Sophie Belman
Author: Noémie Lefrancq
Author: Susan Nzenze
Author: Sarah Downs
Author: Mignon du Plessis
Author: Stephanie W. Lo
Author: Lesley McGee
Author: Shabir A. Madhi
Author: Anne Von Gottberg
Author: Stephen D Bentley
Author: Henrik Salje
Corporate Author: The Global Pneumococcal Sequencing Consortium

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