Key features of pneumococcal isolates recovered in Central and Northwestern Russia in 2011-2018 determined through whole-genome sequencing

Ekaterina Egorova; Narender Kumar; Rebecca A Gladstone; Yulia Urban; Elena Voropaeva; A V Chaplin; Elena Rumiantseva; T S Svistunova; Paulina A Hawkins; Keith P Klugman; Robert F Breiman; Lesley McGee; Stephen D Bentley; Stephanie W Lo

doi:10.1099/mgen.0.000851

Key features of pneumococcal isolates recovered in Central and Northwestern Russia in 2011-2018 determined through whole-genome sequencing

Ekaterina Egorova, Narender Kumar, Rebecca A Gladstone, Yulia Urban, Elena Voropaeva, A V Chaplin, Elena Rumiantseva, T S Svistunova, Paulina A Hawkins, Keith P Klugman, Robert F Breiman, Lesley McGee, Stephen D Bentley, Stephanie W Lo

Department of Life Sciences

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

4 Citations (SciVal)

Abstract

Invasive pneumococcal disease remains one of the leading causes of morbidity and mortality worldwide. In Russia, 13- valent pneumococcal conjugate vaccine (PCV13) was introduced into the childhood immunization programme nationwide in 2014. As part of the Global Pneumococcal Sequencing Project (GPS), we used genome data to characterize 179 pneumococcal isolates collected from Russia in 2011-2018 to investigate the circulating pneumococcal strains using a standardized genomic definition of pneumococcal lineages (global pneumococcal sequence clusters, GPSCs), prevalent serotypes and antimicrobial resistance profiles.We observed high serotype and lineage diversity among the 179 isolates recovered from cerebrospinal fluid (n=77), nasopharyngeal swabs (n=99) and other non-sterile site swabs (n=3). Overall, 60 GPSCs were identified, including 48 clonal complexes (CCs) and 14 singletons, and expressed 42 serotypes (including non-typable). Among PCV13 serotypes, 19F, 6B and 23F were the top three serotypes while 11A, 15B/C and 8 were the top three among non-PCV13 serotypes in the collection. Two lineages (GPSC6 and GPSC47) expressed both PCV13 and non-PCV13 serotypes that caused invasive disease, and were penicillin- and multidrug-resistant (MDR), highlighting their potential to adapt and continue to cause infections under vaccine and antibiotic selective pressure. PCV13 serotypes comprised 92 % (11/12) of the CSF isolates from the children aged below 5 years; however, the prevalence of PCV13 serotype isolates dropped to 53 % (31/58) among the nasopharyngeal isolates. Our analysis showed that 59 % (105/179) of the isolates were predicted to be non-susceptible to at least one class of antibiotics and 26 % (46/179) were MDR. Four MDR lineages (GPSC1, GPSC6, GPSC10 and GPSC47) accounted for 65 % (30/46) of the MDR isolates and expressed PCV13 serotypes (93 %, 28/30).This study provides evidence of high genetic and serotype diversity contributed by a mix of globally spreading and regionally circulating lineages in Russia. The observations suggest that the PCV13 vaccine could be important in reducing both invasive disease and antimicrobial resistance. We also identify potential lineages (GPSC6 and GPSC47) that may evade the vaccine.

Original language	English
Journal	Microbial Genomics
Volume	8
Issue number	9
DOIs	https://doi.org/10.1099/mgen.0.000851
Publication status	Published - 16 Sept 2022

Bibliographical note

Funding information
This study was co-funded by the Bill and Melinda Gates Foundation (grant code OPP1034556), the Wellcome Sanger Institute (core Wellcome grants 098051 and 206194) and the US Centers for Disease Control and Prevention. The funding sources had no role in isolate selection, analysis, or data interpretation. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. The corresponding author had full access to the data and was responsible for the final decision to submit for publication.

Keywords

Anti-Bacterial Agents
Child
Humans
Penicillins
Serotyping
Streptococcus pneumoniae/genetics
Vaccines, Conjugate

UN SDGs

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

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10.1099/mgen.0.000851Licence: CC BY

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Egorova, E., Kumar, N., Gladstone, R. A., Urban, Y., Voropaeva, E., Chaplin, A. V., Rumiantseva, E., Svistunova, T. S., Hawkins, P. A., Klugman, K. P., Breiman, R. F., McGee, L., Bentley, S. D., & Lo, S. W. (2022). Key features of pneumococcal isolates recovered in Central and Northwestern Russia in 2011-2018 determined through whole-genome sequencing. Microbial Genomics, 8(9). https://doi.org/10.1099/mgen.0.000851

Egorova, E, Kumar, N, Gladstone, RA, Urban, Y, Voropaeva, E, Chaplin, AV, Rumiantseva, E, Svistunova, TS, Hawkins, PA, Klugman, KP, Breiman, RF, McGee, L, Bentley, SD & Lo, SW 2022, 'Key features of pneumococcal isolates recovered in Central and Northwestern Russia in 2011-2018 determined through whole-genome sequencing', Microbial Genomics, vol. 8, no. 9. https://doi.org/10.1099/mgen.0.000851

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abstract = "Invasive pneumococcal disease remains one of the leading causes of morbidity and mortality worldwide. In Russia, 13- valent pneumococcal conjugate vaccine (PCV13) was introduced into the childhood immunization programme nationwide in 2014. As part of the Global Pneumococcal Sequencing Project (GPS), we used genome data to characterize 179 pneumococcal isolates collected from Russia in 2011-2018 to investigate the circulating pneumococcal strains using a standardized genomic definition of pneumococcal lineages (global pneumococcal sequence clusters, GPSCs), prevalent serotypes and antimicrobial resistance profiles.We observed high serotype and lineage diversity among the 179 isolates recovered from cerebrospinal fluid (n=77), nasopharyngeal swabs (n=99) and other non-sterile site swabs (n=3). Overall, 60 GPSCs were identified, including 48 clonal complexes (CCs) and 14 singletons, and expressed 42 serotypes (including non-typable). Among PCV13 serotypes, 19F, 6B and 23F were the top three serotypes while 11A, 15B/C and 8 were the top three among non-PCV13 serotypes in the collection. Two lineages (GPSC6 and GPSC47) expressed both PCV13 and non-PCV13 serotypes that caused invasive disease, and were penicillin- and multidrug-resistant (MDR), highlighting their potential to adapt and continue to cause infections under vaccine and antibiotic selective pressure. PCV13 serotypes comprised 92 % (11/12) of the CSF isolates from the children aged below 5 years; however, the prevalence of PCV13 serotype isolates dropped to 53 % (31/58) among the nasopharyngeal isolates. Our analysis showed that 59 % (105/179) of the isolates were predicted to be non-susceptible to at least one class of antibiotics and 26 % (46/179) were MDR. Four MDR lineages (GPSC1, GPSC6, GPSC10 and GPSC47) accounted for 65 % (30/46) of the MDR isolates and expressed PCV13 serotypes (93 %, 28/30).This study provides evidence of high genetic and serotype diversity contributed by a mix of globally spreading and regionally circulating lineages in Russia. The observations suggest that the PCV13 vaccine could be important in reducing both invasive disease and antimicrobial resistance. We also identify potential lineages (GPSC6 and GPSC47) that may evade the vaccine.",

keywords = "Anti-Bacterial Agents, Child, Humans, Penicillins, Serotyping, Streptococcus pneumoniae/genetics, Vaccines, Conjugate",

author = "Ekaterina Egorova and Narender Kumar and Gladstone, {Rebecca A} and Yulia Urban and Elena Voropaeva and Chaplin, {A V} and Elena Rumiantseva and Svistunova, {T S} and Hawkins, {Paulina A} and Klugman, {Keith P} and Breiman, {Robert F} and Lesley McGee and Bentley, {Stephen D} and Lo, {Stephanie W}",

note = "Funding information This study was co-funded by the Bill and Melinda Gates Foundation (grant code OPP1034556), the Wellcome Sanger Institute (core Wellcome grants 098051 and 206194) and the US Centers for Disease Control and Prevention. The funding sources had no role in isolate selection, analysis, or data interpretation. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. The corresponding author had full access to the data and was responsible for the final decision to submit for publication.",

year = "2022",

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doi = "10.1099/mgen.0.000851",

language = "English",

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TY - JOUR

T1 - Key features of pneumococcal isolates recovered in Central and Northwestern Russia in 2011-2018 determined through whole-genome sequencing

AU - Egorova, Ekaterina

AU - Kumar, Narender

AU - Gladstone, Rebecca A

AU - Urban, Yulia

AU - Voropaeva, Elena

AU - Chaplin, A V

AU - Rumiantseva, Elena

AU - Svistunova, T S

AU - Hawkins, Paulina A

AU - Klugman, Keith P

AU - Breiman, Robert F

AU - McGee, Lesley

AU - Bentley, Stephen D

AU - Lo, Stephanie W

N1 - Funding information This study was co-funded by the Bill and Melinda Gates Foundation (grant code OPP1034556), the Wellcome Sanger Institute (core Wellcome grants 098051 and 206194) and the US Centers for Disease Control and Prevention. The funding sources had no role in isolate selection, analysis, or data interpretation. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. The corresponding author had full access to the data and was responsible for the final decision to submit for publication.

PY - 2022/9/16

Y1 - 2022/9/16

N2 - Invasive pneumococcal disease remains one of the leading causes of morbidity and mortality worldwide. In Russia, 13- valent pneumococcal conjugate vaccine (PCV13) was introduced into the childhood immunization programme nationwide in 2014. As part of the Global Pneumococcal Sequencing Project (GPS), we used genome data to characterize 179 pneumococcal isolates collected from Russia in 2011-2018 to investigate the circulating pneumococcal strains using a standardized genomic definition of pneumococcal lineages (global pneumococcal sequence clusters, GPSCs), prevalent serotypes and antimicrobial resistance profiles.We observed high serotype and lineage diversity among the 179 isolates recovered from cerebrospinal fluid (n=77), nasopharyngeal swabs (n=99) and other non-sterile site swabs (n=3). Overall, 60 GPSCs were identified, including 48 clonal complexes (CCs) and 14 singletons, and expressed 42 serotypes (including non-typable). Among PCV13 serotypes, 19F, 6B and 23F were the top three serotypes while 11A, 15B/C and 8 were the top three among non-PCV13 serotypes in the collection. Two lineages (GPSC6 and GPSC47) expressed both PCV13 and non-PCV13 serotypes that caused invasive disease, and were penicillin- and multidrug-resistant (MDR), highlighting their potential to adapt and continue to cause infections under vaccine and antibiotic selective pressure. PCV13 serotypes comprised 92 % (11/12) of the CSF isolates from the children aged below 5 years; however, the prevalence of PCV13 serotype isolates dropped to 53 % (31/58) among the nasopharyngeal isolates. Our analysis showed that 59 % (105/179) of the isolates were predicted to be non-susceptible to at least one class of antibiotics and 26 % (46/179) were MDR. Four MDR lineages (GPSC1, GPSC6, GPSC10 and GPSC47) accounted for 65 % (30/46) of the MDR isolates and expressed PCV13 serotypes (93 %, 28/30).This study provides evidence of high genetic and serotype diversity contributed by a mix of globally spreading and regionally circulating lineages in Russia. The observations suggest that the PCV13 vaccine could be important in reducing both invasive disease and antimicrobial resistance. We also identify potential lineages (GPSC6 and GPSC47) that may evade the vaccine.

AB - Invasive pneumococcal disease remains one of the leading causes of morbidity and mortality worldwide. In Russia, 13- valent pneumococcal conjugate vaccine (PCV13) was introduced into the childhood immunization programme nationwide in 2014. As part of the Global Pneumococcal Sequencing Project (GPS), we used genome data to characterize 179 pneumococcal isolates collected from Russia in 2011-2018 to investigate the circulating pneumococcal strains using a standardized genomic definition of pneumococcal lineages (global pneumococcal sequence clusters, GPSCs), prevalent serotypes and antimicrobial resistance profiles.We observed high serotype and lineage diversity among the 179 isolates recovered from cerebrospinal fluid (n=77), nasopharyngeal swabs (n=99) and other non-sterile site swabs (n=3). Overall, 60 GPSCs were identified, including 48 clonal complexes (CCs) and 14 singletons, and expressed 42 serotypes (including non-typable). Among PCV13 serotypes, 19F, 6B and 23F were the top three serotypes while 11A, 15B/C and 8 were the top three among non-PCV13 serotypes in the collection. Two lineages (GPSC6 and GPSC47) expressed both PCV13 and non-PCV13 serotypes that caused invasive disease, and were penicillin- and multidrug-resistant (MDR), highlighting their potential to adapt and continue to cause infections under vaccine and antibiotic selective pressure. PCV13 serotypes comprised 92 % (11/12) of the CSF isolates from the children aged below 5 years; however, the prevalence of PCV13 serotype isolates dropped to 53 % (31/58) among the nasopharyngeal isolates. Our analysis showed that 59 % (105/179) of the isolates were predicted to be non-susceptible to at least one class of antibiotics and 26 % (46/179) were MDR. Four MDR lineages (GPSC1, GPSC6, GPSC10 and GPSC47) accounted for 65 % (30/46) of the MDR isolates and expressed PCV13 serotypes (93 %, 28/30).This study provides evidence of high genetic and serotype diversity contributed by a mix of globally spreading and regionally circulating lineages in Russia. The observations suggest that the PCV13 vaccine could be important in reducing both invasive disease and antimicrobial resistance. We also identify potential lineages (GPSC6 and GPSC47) that may evade the vaccine.

KW - Anti-Bacterial Agents

KW - Child

KW - Humans

KW - Penicillins

KW - Serotyping

KW - Streptococcus pneumoniae/genetics

KW - Vaccines, Conjugate

U2 - 10.1099/mgen.0.000851

DO - 10.1099/mgen.0.000851

M3 - Article

C2 - 36112007

SN - 2057-5858

VL - 8

JO - Microbial Genomics

JF - Microbial Genomics

IS - 9

ER -

Key features of pneumococcal isolates recovered in Central and Northwestern Russia in 2011-2018 determined through whole-genome sequencing

Abstract

Bibliographical note

Keywords

UN SDGs

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Cite this