Emergence of a multidrug-resistant and virulent Streptococcus pneumoniae lineage mediates serotype replacement after PCV13: an international whole-genome sequencing study.

Stephanie W. Lo; Kate Mellor; Robert Cohen; Alba Redin Alonso; Sophie Belman; Narender Kumar; Paulina A. Hawkins; Rebecca A. Gladstone; Anne von Gottberg; Balaji Veeraraghavan; K. L. Ravikumar; Rama Kandasamy; Sir Andrew J. Pollard; Samir K. Saha; Godfrey Bigogo; Martin Antonio; Brenda Kwambana; Shaper Mirza; Sadia Shakoor; Imran Nisar; Jennifer E. Cornick; Deborah Lehmann; Rebecca L. Ford; Betuel Sigauque; Paul Turner; Jennifer Moïsi; Stephen K. Obaro; Ron Dagan; Idrissa Diawara; Anna Skoczyńska; Hui Wang; Philip E. Carter; Keith P. Klugman; Gail Rodgers; Robert F. Breiman; Lesley McGee; Stephen D. Bentley; Carmen Muñoz Almagro; Emmanuelle Varon; Abdullah Brooks; Alejandra Corso; Alexander Davydov; Alison Maguire; Anmol Kiran; Benild Moiane; Bernard Beall; Chunjiang Zhao; David Aanensen; Dean Everett; Diego Faccone

doi:10.1016/s2666-5247(22)00158-6

Emergence of a multidrug-resistant and virulent Streptococcus pneumoniae lineage mediates serotype replacement after PCV13: an international whole-genome sequencing study.

Stephanie W. Lo
, Kate Mellor
, Robert Cohen
, Alba Redin Alonso
, Sophie Belman
, Narender Kumar
, Paulina A. Hawkins
, Rebecca A. Gladstone
, Anne von Gottberg
, Balaji Veeraraghavan
, K. L. Ravikumar
, Rama Kandasamy
, Sir Andrew J. Pollard
, Samir K. Saha
, Godfrey Bigogo
, Martin Antonio
, Brenda Kwambana
, Shaper Mirza
, Sadia Shakoor
, Imran Nisar

Jennifer E. Cornick, Deborah Lehmann, Rebecca L. Ford, Betuel Sigauque, Paul Turner, Jennifer Moïsi, Stephen K. Obaro, Ron Dagan, Idrissa Diawara, Anna Skoczyńska, Hui Wang, Philip E. Carter, Keith P. Klugman, Gail Rodgers, Robert F. Breiman, Lesley McGee, Stephen D. Bentley, Carmen Muñoz Almagro, Emmanuelle Varon, Abdullah Brooks, Alejandra Corso, Alexander Davydov, Alison Maguire, Anmol Kiran, Benild Moiane, Bernard Beall, Chunjiang Zhao, David Aanensen, Dean Everett, Diego Faccone

Wellcome Sanger Institute
ACTIV
GPIP
AFPA
Université Paris-Est Créteil
CHI de Créteil
SJD Barcelona Children's Hospital
UIC Barcelona
Instituto de Salud Carlos III
Emory University
University of Oslo
National Health Laboratory Services
Christian Medical College
Kempegowda Institute of Medical Sciences
University of Oxford
NIHR Oxford Biomedical Research Centre
University of New South Wales
Child Health Research Foundation
Kenya Medical Research Institute
London School of Hygiene and Tropical Medicine
University College London
Lahore University of Management Sciences
Aga Khan University
Malawi-Liverpool-Wellcome Trust Clinical Research Programme
University of Liverpool
the University of Western Australia
Papua New Guinea Institute of Medical Research
Centro de investigação de Saúde de Manhiça
Angkor Hospital for Children
Agence de Médecine Préventive
University of Nebraska Medical Center
International Foundation Against Infectious Diseases in Nigeria
Ben-Gurion University of the Negev
University of Hassan II Casablanca
Mohammed VI University of Sciences and Health
National Medicines Institute, Warsaw
Peking University
ESR
Gates Foundation
Centers for Disease Control and Prevention

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

75 Citations (Scopus)

Abstract

BACKGROUND

Serotype 24F is one of the emerging pneumococcal serotypes after the introduction of pneumococcal conjugate vaccine (PCV). We aimed to identify lineages driving the increase of serotype 24F in France and place these findings into a global context.

METHODS

Whole-genome sequencing was performed on a collection of serotype 24F pneumococci from asymptomatic colonisation (n=229) and invasive disease (n=190) isolates among individuals younger than 18 years in France, from 2003 to 2018. To provide a global context, we included an additional collection of 24F isolates in the Global Pneumococcal Sequencing (GPS) project database for analysis. A Global Pneumococcal Sequence Cluster (GPSC) and a clonal complex (CC) were assigned to each genome. Phylogenetic, evolutionary, and spatiotemporal analysis were conducted using the same 24F collection and supplemented with a global collection of genomes belonging to the lineage of interest from the GPS project database (n=25 590).

FINDINGS

Serotype 24F was identified in numerous countries mainly due to the clonal spread of three lineages: GPSC10 (CC230), GPSC16 (CC156), and GPSC206 (CC7701). GPSC10 was the only multidrug-resistant lineage. GPSC10 drove the increase in 24F in France and had high invasive disease potential. The international dataset of GPSC10 (n=888) revealed that this lineage expressed 16 other serotypes, with only six included in 13-valent PCV (PCV13). All serotype 24F isolates were clustered in a single clade within the GPSC10 phylogeny and long-range transmissions were detected from Europe to other continents. Spatiotemporal analysis showed GPSC10-24F took 3-5 years to spread across France and a rapid change of serotype composition from PCV13 serotype 19A to 24F during the introduction of PCV13 was observed in neighbouring country Spain.

INTERPRETATION

Our work reveals that GPSC10 alone is a challenge for serotype-based vaccine strategy. More systematic investigation to identify lineages like GPSC10 will better inform and improve next-generation preventive strategies against pneumococcal diseases.

Original language	English
Pages (from-to)	e735-e743
Journal	The Lancet Microbe
Volume	3
Issue number	10
Early online date	16 Aug 2022
DOIs	https://doi.org/10.1016/s2666-5247(22)00158-6
Publication status	Published - 28 Sept 2022
Externally published	Yes

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

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10.1016/s2666-5247(22)00158-6Licence: CC BY

PIIS2666524722001586-2Final published version, 690 KBLicence: CC BY

Cite this

Lo, S. W., Mellor, K., Cohen, R., Alonso, A. R., Belman, S., Kumar, N., Hawkins, P. A., Gladstone, R. A., von Gottberg, A., Veeraraghavan, B., Ravikumar, K. L., Kandasamy, R., Pollard, S. A. J., Saha, S. K., Bigogo, G., Antonio, M., Kwambana, B., Mirza, S., Shakoor, S., ... Faccone, D. (2022). Emergence of a multidrug-resistant and virulent Streptococcus pneumoniae lineage mediates serotype replacement after PCV13: an international whole-genome sequencing study. The Lancet Microbe, 3(10), e735-e743. https://doi.org/10.1016/s2666-5247(22)00158-6

@article{5e067eda44c6453b8755e99caadef5af,

title = "Emergence of a multidrug-resistant and virulent Streptococcus pneumoniae lineage mediates serotype replacement after PCV13: an international whole-genome sequencing study.",

abstract = "BACKGROUNDSerotype 24F is one of the emerging pneumococcal serotypes after the introduction of pneumococcal conjugate vaccine (PCV). We aimed to identify lineages driving the increase of serotype 24F in France and place these findings into a global context.METHODSWhole-genome sequencing was performed on a collection of serotype 24F pneumococci from asymptomatic colonisation (n=229) and invasive disease (n=190) isolates among individuals younger than 18 years in France, from 2003 to 2018. To provide a global context, we included an additional collection of 24F isolates in the Global Pneumococcal Sequencing (GPS) project database for analysis. A Global Pneumococcal Sequence Cluster (GPSC) and a clonal complex (CC) were assigned to each genome. Phylogenetic, evolutionary, and spatiotemporal analysis were conducted using the same 24F collection and supplemented with a global collection of genomes belonging to the lineage of interest from the GPS project database (n=25 590).FINDINGSSerotype 24F was identified in numerous countries mainly due to the clonal spread of three lineages: GPSC10 (CC230), GPSC16 (CC156), and GPSC206 (CC7701). GPSC10 was the only multidrug-resistant lineage. GPSC10 drove the increase in 24F in France and had high invasive disease potential. The international dataset of GPSC10 (n=888) revealed that this lineage expressed 16 other serotypes, with only six included in 13-valent PCV (PCV13). All serotype 24F isolates were clustered in a single clade within the GPSC10 phylogeny and long-range transmissions were detected from Europe to other continents. Spatiotemporal analysis showed GPSC10-24F took 3-5 years to spread across France and a rapid change of serotype composition from PCV13 serotype 19A to 24F during the introduction of PCV13 was observed in neighbouring country Spain.INTERPRETATIONOur work reveals that GPSC10 alone is a challenge for serotype-based vaccine strategy. More systematic investigation to identify lineages like GPSC10 will better inform and improve next-generation preventive strategies against pneumococcal diseases.",

author = "Lo, \{Stephanie W.\} and Kate Mellor and Robert Cohen and Alonso, \{Alba Redin\} and Sophie Belman and Narender Kumar and Hawkins, \{Paulina A.\} and Gladstone, \{Rebecca A.\} and \{von Gottberg\}, Anne and Balaji Veeraraghavan and Ravikumar, \{K. L.\} and Rama Kandasamy and Pollard, \{Sir Andrew J.\} and Saha, \{Samir K.\} and Godfrey Bigogo and Martin Antonio and Brenda Kwambana and Shaper Mirza and Sadia Shakoor and Imran Nisar and Cornick, \{Jennifer E.\} and Deborah Lehmann and Ford, \{Rebecca L.\} and Betuel Sigauque and Paul Turner and Jennifer Mo{\"i}si and Obaro, \{Stephen K.\} and Ron Dagan and Idrissa Diawara and Anna Skoczy{\'n}ska and Hui Wang and Carter, \{Philip E.\} and Klugman, \{Keith P.\} and Gail Rodgers and Breiman, \{Robert F.\} and Lesley McGee and Bentley, \{Stephen D.\} and Almagro, \{Carmen Mu{\~n}oz\} and Emmanuelle Varon and Abdullah Brooks and Alejandra Corso and Alexander Davydov and Alison Maguire and Anmol Kiran and Benild Moiane and Bernard Beall and Chunjiang Zhao and David Aanensen and Dean Everett and Diego Faccone",

year = "2022",

month = sep,

day = "28",

doi = "10.1016/s2666-5247(22)00158-6",

language = "English",

volume = "3",

pages = "e735--e743",

journal = "The Lancet Microbe",

issn = "2666-5247",

publisher = "Elsevier Ltd",

number = "10",

}

Lo, SW, Mellor, K, Cohen, R, Alonso, AR, Belman, S, Kumar, N, Hawkins, PA, Gladstone, RA, von Gottberg, A, Veeraraghavan, B, Ravikumar, KL, Kandasamy, R, Pollard, SAJ, Saha, SK, Bigogo, G, Antonio, M, Kwambana, B, Mirza, S, Shakoor, S, Nisar, I, Cornick, JE, Lehmann, D, Ford, RL, Sigauque, B, Turner, P, Moïsi, J, Obaro, SK, Dagan, R, Diawara, I, Skoczyńska, A, Wang, H, Carter, PE, Klugman, KP, Rodgers, G, Breiman, RF, McGee, L, Bentley, SD, Almagro, CM, Varon, E, Brooks, A, Corso, A, Davydov, A, Maguire, A, Kiran, A, Moiane, B, Beall, B, Zhao, C, Aanensen, D, Everett, D & Faccone, D 2022, 'Emergence of a multidrug-resistant and virulent Streptococcus pneumoniae lineage mediates serotype replacement after PCV13: an international whole-genome sequencing study.', The Lancet Microbe, vol. 3, no. 10, pp. e735-e743. https://doi.org/10.1016/s2666-5247(22)00158-6

TY - JOUR

T1 - Emergence of a multidrug-resistant and virulent Streptococcus pneumoniae lineage mediates serotype replacement after PCV13: an international whole-genome sequencing study.

AU - Lo, Stephanie W.

AU - Mellor, Kate

AU - Cohen, Robert

AU - Alonso, Alba Redin

AU - Belman, Sophie

AU - Kumar, Narender

AU - Hawkins, Paulina A.

AU - Gladstone, Rebecca A.

AU - von Gottberg, Anne

AU - Veeraraghavan, Balaji

AU - Ravikumar, K. L.

AU - Kandasamy, Rama

AU - Pollard, Sir Andrew J.

AU - Saha, Samir K.

AU - Bigogo, Godfrey

AU - Antonio, Martin

AU - Kwambana, Brenda

AU - Mirza, Shaper

AU - Shakoor, Sadia

AU - Nisar, Imran

AU - Cornick, Jennifer E.

AU - Lehmann, Deborah

AU - Ford, Rebecca L.

AU - Sigauque, Betuel

AU - Turner, Paul

AU - Moïsi, Jennifer

AU - Obaro, Stephen K.

AU - Dagan, Ron

AU - Diawara, Idrissa

AU - Skoczyńska, Anna

AU - Wang, Hui

AU - Carter, Philip E.

AU - Klugman, Keith P.

AU - Rodgers, Gail

AU - Breiman, Robert F.

AU - McGee, Lesley

AU - Bentley, Stephen D.

AU - Almagro, Carmen Muñoz

AU - Varon, Emmanuelle

AU - Brooks, Abdullah

AU - Corso, Alejandra

AU - Davydov, Alexander

AU - Maguire, Alison

AU - Kiran, Anmol

AU - Moiane, Benild

AU - Beall, Bernard

AU - Zhao, Chunjiang

AU - Aanensen, David

AU - Everett, Dean

AU - Faccone, Diego

PY - 2022/9/28

Y1 - 2022/9/28

N2 - BACKGROUNDSerotype 24F is one of the emerging pneumococcal serotypes after the introduction of pneumococcal conjugate vaccine (PCV). We aimed to identify lineages driving the increase of serotype 24F in France and place these findings into a global context.METHODSWhole-genome sequencing was performed on a collection of serotype 24F pneumococci from asymptomatic colonisation (n=229) and invasive disease (n=190) isolates among individuals younger than 18 years in France, from 2003 to 2018. To provide a global context, we included an additional collection of 24F isolates in the Global Pneumococcal Sequencing (GPS) project database for analysis. A Global Pneumococcal Sequence Cluster (GPSC) and a clonal complex (CC) were assigned to each genome. Phylogenetic, evolutionary, and spatiotemporal analysis were conducted using the same 24F collection and supplemented with a global collection of genomes belonging to the lineage of interest from the GPS project database (n=25 590).FINDINGSSerotype 24F was identified in numerous countries mainly due to the clonal spread of three lineages: GPSC10 (CC230), GPSC16 (CC156), and GPSC206 (CC7701). GPSC10 was the only multidrug-resistant lineage. GPSC10 drove the increase in 24F in France and had high invasive disease potential. The international dataset of GPSC10 (n=888) revealed that this lineage expressed 16 other serotypes, with only six included in 13-valent PCV (PCV13). All serotype 24F isolates were clustered in a single clade within the GPSC10 phylogeny and long-range transmissions were detected from Europe to other continents. Spatiotemporal analysis showed GPSC10-24F took 3-5 years to spread across France and a rapid change of serotype composition from PCV13 serotype 19A to 24F during the introduction of PCV13 was observed in neighbouring country Spain.INTERPRETATIONOur work reveals that GPSC10 alone is a challenge for serotype-based vaccine strategy. More systematic investigation to identify lineages like GPSC10 will better inform and improve next-generation preventive strategies against pneumococcal diseases.

AB - BACKGROUNDSerotype 24F is one of the emerging pneumococcal serotypes after the introduction of pneumococcal conjugate vaccine (PCV). We aimed to identify lineages driving the increase of serotype 24F in France and place these findings into a global context.METHODSWhole-genome sequencing was performed on a collection of serotype 24F pneumococci from asymptomatic colonisation (n=229) and invasive disease (n=190) isolates among individuals younger than 18 years in France, from 2003 to 2018. To provide a global context, we included an additional collection of 24F isolates in the Global Pneumococcal Sequencing (GPS) project database for analysis. A Global Pneumococcal Sequence Cluster (GPSC) and a clonal complex (CC) were assigned to each genome. Phylogenetic, evolutionary, and spatiotemporal analysis were conducted using the same 24F collection and supplemented with a global collection of genomes belonging to the lineage of interest from the GPS project database (n=25 590).FINDINGSSerotype 24F was identified in numerous countries mainly due to the clonal spread of three lineages: GPSC10 (CC230), GPSC16 (CC156), and GPSC206 (CC7701). GPSC10 was the only multidrug-resistant lineage. GPSC10 drove the increase in 24F in France and had high invasive disease potential. The international dataset of GPSC10 (n=888) revealed that this lineage expressed 16 other serotypes, with only six included in 13-valent PCV (PCV13). All serotype 24F isolates were clustered in a single clade within the GPSC10 phylogeny and long-range transmissions were detected from Europe to other continents. Spatiotemporal analysis showed GPSC10-24F took 3-5 years to spread across France and a rapid change of serotype composition from PCV13 serotype 19A to 24F during the introduction of PCV13 was observed in neighbouring country Spain.INTERPRETATIONOur work reveals that GPSC10 alone is a challenge for serotype-based vaccine strategy. More systematic investigation to identify lineages like GPSC10 will better inform and improve next-generation preventive strategies against pneumococcal diseases.

U2 - 10.1016/s2666-5247(22)00158-6

DO - 10.1016/s2666-5247(22)00158-6

M3 - Article

SN - 2666-5247

VL - 3

SP - e735-e743

JO - The Lancet Microbe

JF - The Lancet Microbe

IS - 10

ER -

Emergence of a multidrug-resistant and virulent Streptococcus pneumoniae lineage mediates serotype replacement after PCV13: an international whole-genome sequencing study.

Abstract

UN SDGs

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