TY - JOUR
T1 - Emergence of a multidrug-resistant and virulent Streptococcus pneumoniae lineage mediates serotype replacement after PCV13
T2 - an international whole-genome sequencing study
AU - The Global Pneumococcal Sequencing Consortium
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-Adams, 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
N1 - Funding Information:
The study was cofunded by the Bill & Melinda Gates Foundation (grant code OPP1034556) and the Wellcome Sanger Institute (core Wellcome grants 098051 and 206194). Particular thanks go to all members of the Global Pneumococcal Sequencing Consortium for their contributions of sample collection, processing, and collaborative spirit. We acknowledge Corinne Lévy, Naïm Ouldali, and Stéphane Béchet who manage children data collection and have helped in establishing the study sample for France. We are also grateful to Assiya El Mniai and Cécile Culeux (French National Reference Laboratory for pneumococci) for their technical assistance in preparing DNA for whole genome sequencing. We acknowledge the support from the sequencing facility and the Pathogen Informatics team at the Wellcome Sanger Institute, Hinxton, UK. The findings and conclusions detailed in this manuscript are those of the authors and do not necessarily represent the official position of the US Centers for Disease Control and Prevention.
Funding Information:
The study was cofunded by the Bill & Melinda Gates Foundation (grant code OPP1034556) and the Wellcome Sanger Institute (core Wellcome grants 098051 and 206194). Particular thanks go to all members of the Global Pneumococcal Sequencing Consortium for their contributions of sample collection, processing, and collaborative spirit. We acknowledge Corinne Lévy, Naïm Ouldali, and Stéphane Béchet who manage children data collection and have helped in establishing the study sample for France. We are also grateful to Assiya El Mniai and Cécile Culeux (French National Reference Laboratory for pneumococci) for their technical assistance in preparing DNA for whole genome sequencing. We acknowledge the support from the sequencing facility and the Pathogen Informatics team at the Wellcome Sanger Institute, Hinxton, UK. The findings and conclusions detailed in this manuscript are those of the authors and do not necessarily represent the official position of the US Centers for Disease Control and Prevention.
Publisher Copyright:
© 2022 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license
PY - 2022/10
Y1 - 2022/10
N2 - 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. Funding: Bill & Melinda Gates Foundation, Wellcome Sanger Institute, and the US Centers for Disease Control and Prevention.
AB - 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. Funding: Bill & Melinda Gates Foundation, Wellcome Sanger Institute, and the US Centers for Disease Control and Prevention.
UR - https://www.scopus.com/pages/publications/85138810713
U2 - 10.1016/S2666-5247(22)00158-6
DO - 10.1016/S2666-5247(22)00158-6
M3 - Article
AN - SCOPUS:85138810713
SN - 2666-5247
VL - 3
SP - e735-e743
JO - The Lancet Microbe
JF - The Lancet Microbe
IS - 10
ER -
SDG 3 Good Health and Well-being