Geographical migration and fitness dynamics of Streptococcus pneumoniae

The Global Pneumococcal Sequencing Consortium

doi:10.1038/s41586-024-07626-3

Geographical migration and fitness dynamics of Streptococcus pneumoniae

The Global Pneumococcal Sequencing Consortium

Department of Medical Microbiology

Parasites and Microbes Program
Wellcome Sanger Institute
Department of Genetics
University of Cambridge
Global Health Resilience
BarcelonaSupercomputing Center (BSC-CNS)
Division of Public Health Surveillance and Response
National Health Laboratory Services
School of Pathology
Department of Clinical Microbiology and Infectious Diseases
University of Bath, Department of Life Sciences
National Center for Immunization and Respiratory Diseases
Department of Science and Technology/National Research Foundation
University of the Witwatersrand
Department of Pathology
Faculty of Health Sciences
Servicio Antimicrobianos
Instituto Nacional de Enfermedades Infecciosas
International Centre for Diarrheal Diseases Research
Child Health Research Foundation
Department for Microbiology
Belarusian State Medical University
Center of Bacteriology
Adolfo Lutz Institute
Angkor Hospital for Children
Peking University People ‘s Hospital
Department of Microbiology
Chinese University of Hong Kong, Faculty of Medicine
Department of Microbiology and Carol Yu Centre for Infection
The University of Hong Kong
University of California at San Francisco
Clinical Research Center
Centre Hospitalier Intercommunal de Créteil
Université Paris-Est Créteil
Groupe de Pathologie Infectieuse Pédiatrique de la Société Française de Pédiatrie
National Reference Center for Pneumococci
Department of Clinical Microbiology
Christian Medical College, Vellore
Central Research Laboratory
Kempegowda Institute of Medical Sciences
The Shraga Segal Department of Microbiology
Ben-Gurion University of the Negev
Center for Global Health Research
Kenya Medical Research Institute
Division of Bacterial Diseases
Malawi-Liverpool-Wellcome Trust Clinical Research Programme
Department of Public Health and Epidemiology
Khalifa University of Science and Technology
Infection Research Unit
Khalifa University of Science and Technology
Faculty of Applied Sciences
UCSI University
University of Southampton
Centro de Investigação em Saúde da Manhiça (CISM)
University of Oxford
University of Sydney

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

29 Citations (Scopus)

Abstract

Streptococcus pneumoniae is a leading cause of pneumonia and meningitis worldwide. Many different serotypes co-circulate endemically in any one location^1,2. 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.

Original language	English
Pages (from-to)	386-392
Number of pages	7
Journal	Nature
Volume	631
Issue number	8020
DOIs	https://doi.org/10.1038/s41586-024-07626-3
Publication status	Published - 11 Jul 2024

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SDG 3 Good Health and Well-being

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10.1038/s41586-024-07626-3

Cite this

@article{c796d0bf003b49108978197573539c1e,

title = "Geographical migration and fitness dynamics of Streptococcus pneumoniae",

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{\textendash}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.",

author = "\{The Global Pneumococcal Sequencing Consortium\} and Sophie Belman and No{\'e}mie Lefrancq and Susan Nzenze and Sarah Downs and \{du Plessis\}, Mignon and Lo, \{Stephanie W.\} and Lesley McGee and Madhi, \{Shabir A.\} and \{von Gottberg\}, Anne and Bentley, \{Stephen D.\} and Henrik Salje and Alejandra Corso and Paula Gagetti and Brooks, \{Abdullah W.\} and Md Hasanuzzaman and Saha, \{Samir K.\} and Senjuti Saha and Alexander Davydov and Leonid Titov and Almeida, \{Samanta Cristine Grassi\} and Paul Turner and Chunjiang Zhao and Hui Wang and Margaret Ip and Ho, \{Pak Leung\} and Pierra Law and Keenan, \{Jeremy D.\} and Robert Cohen and Emmanuelle Varon and Eric Sampane-Donkor and Balaji Veeraraghavan and Geetha Nagaraj and Ravikumar, \{K. L.\} and J. Yuvaraj and \{Shamanna Noga\}, Varun and Rachel Benisty and Ron Dagan and Godfrey Bigogo and Jennifer Verani and Anmol Kiran and Everett, \{Dean B.\} and Jennifer Cornick and Maaike Alaerts and Sekaran, \{Shamala Devi\} and Clarke, \{Stuart C.\} and Benild Moiane and Betuel Sigauque and Helio Mucavele and Pollard, \{Andrew J.\} and Rama Kandasamy",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = jul,

day = "11",

doi = "10.1038/s41586-024-07626-3",

language = "English",

volume = "631",

pages = "386--392",

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T1 - Geographical migration and fitness dynamics of Streptococcus pneumoniae

AU - The Global Pneumococcal Sequencing Consortium

AU - Belman, Sophie

AU - Lefrancq, Noémie

AU - Nzenze, Susan

AU - Downs, Sarah

AU - du Plessis, Mignon

AU - Lo, Stephanie W.

AU - McGee, Lesley

AU - Madhi, Shabir A.

AU - von Gottberg, Anne

AU - Bentley, Stephen D.

AU - Salje, Henrik

AU - Corso, Alejandra

AU - Gagetti, Paula

AU - Brooks, Abdullah W.

AU - Hasanuzzaman, Md

AU - Saha, Samir K.

AU - Saha, Senjuti

AU - Davydov, Alexander

AU - Titov, Leonid

AU - Almeida, Samanta Cristine Grassi

AU - Turner, Paul

AU - Zhao, Chunjiang

AU - Wang, Hui

AU - Ip, Margaret

AU - Ho, Pak Leung

AU - Law, Pierra

AU - Keenan, Jeremy D.

AU - Cohen, Robert

AU - Varon, Emmanuelle

AU - Sampane-Donkor, Eric

AU - Veeraraghavan, Balaji

AU - Nagaraj, Geetha

AU - Ravikumar, K. L.

AU - Yuvaraj, J.

AU - Shamanna Noga, Varun

AU - Benisty, Rachel

AU - Dagan, Ron

AU - Bigogo, Godfrey

AU - Verani, Jennifer

AU - Kiran, Anmol

AU - Everett, Dean B.

AU - Cornick, Jennifer

AU - Alaerts, Maaike

AU - Sekaran, Shamala Devi

AU - Clarke, Stuart C.

AU - Moiane, Benild

AU - Sigauque, Betuel

AU - Mucavele, Helio

AU - Pollard, Andrew J.

AU - Kandasamy, Rama

PY - 2024/7/11

Y1 - 2024/7/11

N2 - 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.

AB - 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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DO - 10.1038/s41586-024-07626-3

M3 - Article

AN - SCOPUS:85197560021

SN - 0028-0836

VL - 631

SP - 386

EP - 392

JO - Nature

JF - Nature

IS - 8020

ER -

Geographical migration and fitness dynamics of Streptococcus pneumoniae

Abstract

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