1887

Microbial Genomics logo

Volume 8, Issue 9

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

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 (=77), nasopharyngeal swabs (=99) and other non-sterile site swabs (=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.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antimicrobial resistance , global pneumococcal sequence cluster (GPSC) , Russia , serotypes , Streptococcus pneumoniae and WGS (whole-genome sequencing)
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000851
2022-09-16
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/9/mgen000851.html?itemId=/content/journal/mgen/10.1099/mgen.0.000851&mimeType=html&fmt=ahah

References

  1. Koelman DLH, Brouwer MC, van de Beek D. Resurgence of ppneumococcal meningitis in europe and northern america. Clin Microbiol Infect 2020; 26:199–204 [View Article]
     [Google Scholar]
  2. Ngocho JS, Magoma B, Olomi GA, Mahande MJ, Msuya SE et al. Effectiveness of Pneumococcal conjugate vaccines against invasive pneumococcal disease among children under five years of age in Africa: A systematic review. PLoS One 2019; 14:e0212295 [View Article] [PubMed]
     [Google Scholar]
  3. WHO (World Health Organization) Estimated Hib and pneumococcal deaths for children under 5 years of age [Internet]. www.who.int. 2013 [cited 2019 Jun 10]; 2008 https://www.who.int/immunization/monitiring_surveillance/burden/estimates/Pneumo_hib/en/
  4. Wahl B, O’Brien KL, Greenbaum A, Majumder A, Liu L et al. Burden of Streptococcus pneumoniae and Haemophilus influenzae type b disease in children in the era of conjugate vaccines: global, regional, and national estimates for 2000-15. Lancet Glob Health 2018; 6:e744–e757 [View Article] [PubMed]
     [Google Scholar]
  5. WHO WHO. Measuring impact of Streptococcus pneumoniae and Haemophilus influenzae type b conjugate vaccination [Internet]. 2012 [cited 2019] p. 10(7):477–477; 2012 www.who.int/vaccines-documents/
  6. Savulescu C, Krizova P, Lepoutre A, Mereckiene J, Vestrheim DF et al. Effect of high-valency pneumococcal conjugate vaccines on invasive pneumococcal disease in children in SpIDnet countries: an observational multicentre study. Lancet Respir Med 2017; 5:648–656 [View Article] [PubMed]
     [Google Scholar]
  7. Ladhani SN, Collins S, Djennad A, Sheppard CL, Borrow R et al. Rapid increase in non-vaccine serotypes causing invasive pneumococcal disease in England and Wales, 2000-17: a prospective national observational cohort study. Lancet Infect Dis 2018; 18:441–451 [View Article] [PubMed]
     [Google Scholar]
  8. Mackenzie GA, Hill PC, Jeffries DJ, Hossain I, Uchendu U et al. Effect of the introduction of pneumococcal conjugate vaccination on invasive pneumococcal disease in The Gambia: a population-based surveillance study. Lancet Infect Dis 2016; 16:703–711 [View Article] [PubMed]
     [Google Scholar]
  9. Gessner BD, Jiang Q, Van Werkhoven CH, Sings HL, Webber C et al. A post-hoc analysis of serotype-specific vaccine efficacy of 13-valent pneumococcal conjugate vaccine against clinical community acquired pneumonia from A randomized clinical trial in the Netherlands. Vaccine 2019; 37:4147–4154 [View Article] [PubMed]
     [Google Scholar]
  10. Sings HL, De Wals P, Gessner BD, Isturiz R, Laferriere C et al. Effectiveness of 13-Valent Pneumococcal Conjugate Vaccine Against Invasive Disease Caused by Serotype 3 in Children: A Systematic Review and Meta-analysis of Observational Studies. Clin Infect Dis 2019; 68:2135–2143 [View Article] [PubMed]
     [Google Scholar]
  11. Feldman C, Anderson R. Recent advances in the epidemiology and prevention of Streptococcus pneumoniae infections. F1000Res 2020; 9:F1000 Faculty Rev-338 [View Article] [PubMed]
     [Google Scholar]
  12. Kandasamy R, Voysey M, Collins S, Berbers G, Robinson H et al. Persistent circulation of vaccine serotypes and serotype replacement after 5 years of infant immunization with 13-valent pneumococcal conjugate vaccine in the United Kingdom. J Infect Dis 2020; 221:1361–1370 [View Article] [PubMed]
     [Google Scholar]
  13. Ben-Shimol S, Givon-Lavi N, Grisaru-Soen G, Megged O, Greenberg D et al. Comparative incidence dynamics and serotypes of meningitis, bacteremic pneumonia and other-IPD in young children in the PCV era: Insights from Israeli surveillance studies. Vaccine 2018; 36:5477–5484 [View Article] [PubMed]
     [Google Scholar]
  14. Whitney CG, Goldblatt D, O’Brien KL. Dosing schedules for pneumococcal conjugate vaccine internet]; 33(suppl 2 optimum dosing of pneumococcal conjugate vaccine for infants 0 A landscape analysis of evidence supportin g different schedules):S172. available fromdosing schedules for pneumococcal conjugate vaccine. Pediatr Infect Dis J 2014; 33:S172–S181 [View Article] [PubMed]
     [Google Scholar]
  15. Russian Federation: WHO and UNICEF estimates of immunization coverage: 2019 revision [Internet]. https://www.WHO.int/. 2020 [cited 2021 Dec 2]; 2020 https://www.who.int/immunization/monitoring_surveillance/data/rus.pdf
  16. Briko NI, Korshunov VA, Namazova-Baranova LS, Lobzin JV, Baranov AA et al. The results of a three-year pneumococcal vaccination of children in Russia. Pediatr farmakol 2018; 15:287–299 [View Article]
     [Google Scholar]
  17. Ceyhan M, Dagan R, Sayiner A, Chernyshova L, Dinleyici EÇ et al. Surveillance of pneumococcal diseases in Central and Eastern Europe. Hum Vaccin Immunother 2016; 12:2124–2134 [View Article]
     [Google Scholar]
  18. Sidorenko S, Rennert W, Lobzin Y, Briko N, Kozlov R et al. Multicenter study of serotype distribution of Streptococcus pneumoniae nasopharyngeal isolates from healthy children in the Russian Federation after introduction of PCV13 into the National Vaccination Calendar. Diagn Microbiol Infect Dis 2020; 96:114914 [View Article]
     [Google Scholar]
  19. Tatochenko V, Sidorenko S, Namazova-Baranova L, Mayanskiy N, Kulichenko T et al. Streptococcus pneumoniae serotype distribution in children in the Russian Federation before the introduction of pneumococcal conjugate vaccines into the National Immunization Program. Expert Rev Vaccines 2014; 13:257–264 [View Article]
     [Google Scholar]
  20. Sidorenko SV, Savinova TA, Il’ina EN, Syrochkina MA. Population pattern of pneumococci with lower susceptibility to penicillin and prospects of antipneumococcal vaccination to control antibiotic resistance distribution. Antibiot Khimioter 2011; 56:11–18 [PubMed]
     [Google Scholar]
  21. Kalinogorskaya OS, Belanov SS, Volkova MO, Gostev VV, Sidorenko SV. Antibiotic resistance and serotype pattern of Streptococcus pneumoniae Isolated from Children in St. Petersburg in 2010-2013. Antibiot Khimioter 2015; 60:10–18 [PubMed]
     [Google Scholar]
  22. Vorobieva S Jensen V, Furberg A-S, Slotved H-C, Bazhukova T, Haldorsen B et al. EpidemiologicalEpidemiological and molecular characterization of Streptococcus pneumoniae carriage strains in pre-school children in Arkhangelsk, northern European Russia, prior to the introduction of conjugate pneumococcal vaccines. BMC Infect Dis 2020; 20:279 [View Article] [PubMed]
     [Google Scholar]
  23. Mayanskiy N, Kulichenko T, Alyabieva N, Brzhozovskaya E, Ponomarenko O et al. Changing serotype distribution and resistance patterns among pediatric nasopharyngeal pneumococci collected in Moscow, 2010-2017. Diagn Microbiol Infect Dis 2019; 94:385–390 [View Article]
     [Google Scholar]
  24. Mironov KO, Korchagin VI, Mikhailova YV, Yanushevich YG, Shelenkov AA et al. Characterization of Streptococcus pneumoniae strains causing invasive infections using whole-genome sequencing. Zhurnal mikrobiologii, èpidemiologii i immunobiologii 2020; 97:113–118 [View Article]
     [Google Scholar]
  25. Gladstone RA, Lo SW, Lees JA, Croucher NJ, van Tonder AJ et al. International genomic definition of Pneumococcal lineages, to contextualise disease, antibiotic resistance and vaccine impact. EBioMedicine 2019; 43:338–346 [View Article] [PubMed]
     [Google Scholar]
  26. World Health Organization & Centers for Disease Control and Prevention (‎U.S.) Laboratory Methods for the Diagnosis of Meningitis Caused by Neisseria Meningitidis, Streptococcus Pneumoniae, and Haemophilus Influenzae: WHO Manual, 2nd ed World Health Organization; 2011 https://apps.who.int/iris/handle/10665/70765 [PubMed]
     [Google Scholar]
  27. Sørensen UB. Typing of pneumococci by using 12 pooled antisera. J Clin Microbiol 1993; 31:2097–2100 [View Article] [PubMed]
     [Google Scholar]
  28. Slotved H-C, Kaltoft M, Skovsted IC, Kerrn MB, Espersen F. Simple, rapid latex agglutination test for serotyping of pneumococci (Pneumotest-Latex. J Clin Microbiol 2004; 42:2518–2522 [View Article] [PubMed]
     [Google Scholar]
  29. CLSI Performance standards for antimicrobial susceptibility testing. In CLSI Supplement M100, 28th ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2018
     [Google Scholar]
  30. Hawkins PA, Akpaka PE, Nurse-Lucas M, Gladstone R, Bentley SD et al. Antimicrobial resistance determinants and susceptibility profiles of pneumococcal isolates recovered in Trinidad and Tobago. J Glob Antimicrob Resist 2017; 11:148–151 [View Article] [PubMed]
     [Google Scholar]
  31. Epping L, van Tonder AJ, Gladstone RA, Bentley SD, Page AJ et al. SeroBA: rapid high-throughput serotyping of Streptococcus pneumoniae from whole genome sequence data. Bioinformatics 2017 [View Article]
     [Google Scholar]
  32. J. Page A, Taylor B, A. Keane J. Multilocus sequence typing by blast from de novo assemblies against PubMLST. JOSS 2016; 1:118 [View Article]
     [Google Scholar]
  33. github [Internet] GitHub. 2017 [cited 2021]; 2017 https://github.com/BenJamesMetcalf/Sanger_SPN_Scripts-Ref
  34. Metcalf BJ, Chochua S, Gertz RE, Li Z, Walker H et al. Using whole genome sequencing to identify resistance determinants and predict antimicrobial resistance phenotypes for year 2015 invasive pneumococcal disease isolates recovered in the United States. Clin Microbiol Infect 2016; 22:1002 [View Article] [PubMed]
     [Google Scholar]
  35. Li Y, Metcalf BJ, Chochua S, Li Z, Gertz RE et al. Validation of β-lactam minimum inhibitory concentration predictions for pneumococcal isolates with newly encountered penicillin binding protein (PBP) sequences. BMC Genomics 2017; 18:621 [View Article] [PubMed]
     [Google Scholar]
  36. Lees JA, Harris SR, Tonkin-Hill G, Gladstone RA, Lo SW et al. Fast and flexible bacterial genomic epidemiology with PopPUNK. Genome Res 2019; 29:304–316 [View Article] [PubMed]
     [Google Scholar]
  37. Gladstone RA, Lo SW, Goater R, Yeats C, Taylor B et al. Visualizing variation within Global Pneumococcal Sequence Clusters (GPSCs) and country population snapshots to contextualize pneumococcal isolates. Microb Genom 2020; 6: [View Article] [PubMed]
     [Google Scholar]
  38. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
     [Google Scholar]
  39. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
     [Google Scholar]
  40. Cohen J. Statistical Power Analysis for the Behavioral Sciences, 2nd ed. Hillsdale, NJ: Lawrence Erlbaum; 1988
     [Google Scholar]
  41. Balsells E, Dagan R, Yildirim I, Gounder PP, Steens A et al. The relative invasive disease potential of Streptococcus pneumoniae among children after PCV introduction: a systematic review and meta-analysis. J Infect 2018; 77:368–378 [View Article]
     [Google Scholar]
  42. Merck.com U.S. FDA Accepts for Priority Review the Biologics License Application for V114, Merck’S Investigational 15-valent Pneumococcal Conjugate Vaccine, for Use in Adults 18 Years of Age and Older; 2021 https://www.merck.com/news/u-s-fda-accepts-for-priority-review-the-biologics-license-application-for-v114-mercks-investigational-15-valent-pneumococcal-conjugate-vaccine-for-use-in-adults-18-years-of-age-and-older/
  43. pfizer.com U.S. FDA Approves PREVNAR 20TM, Pfizer’s Pneumococcal 20-valent Conjugate Vaccine for Adults Ages 18 Years or Older; 2021 https://www.pfizer.com/news/press-release/press-release-detail/us-fda-approves-prevnar-20tm-pfizers-pneumococcal-20-valent
  44. Wyres KL, Lambertsen LM, Croucher NJ, McGee L, von Gottberg A et al. Pneumococcal capsular switching: a historical perspective. J Infect Dis 2013; 207:439–449 [View Article] [PubMed]
     [Google Scholar]
  45. Mayanskiy N, Alyabieva N, Ponomarenko O, Lazareva A, Katosova L et al. Serotypes and antibiotic resistance of non-invasive Streptococcus pneumoniae circulating in pediatric hospitals in Moscow, Russia. Int J Infect Dis 2014; 20:58–62 [View Article] [PubMed]
     [Google Scholar]
  46. Chernyshova LI, Gilfanova AM, Bondarenko AV, Yanovskaya VV, Yakimovich SA. PDF) problems of treatment and prevention of pneumococcus infection in children. Actual Infectology 2018; 6:89–94
     [Google Scholar]
  47. Usonis V, Stacevičienė I, Petraitienė S, Vaičiūnienė D, Alasevičius T et al. Streptococcus pneumoniae nasopharyngeal colonisation in children aged under six years with acute respiratory tract infection in Lithuania, February 2012 to March 2013. Euro Surveill 2015; 20:34–41 [View Article]
     [Google Scholar]
  48. Petraitiene S, Alasevicius T, Staceviciene I, Vaiciuniene D, Kacergius T et al. The influence of Streptococcus pneumoniae nasopharyngeal colonization on the clinical outcome of the respiratory tract infections in preschool children. BMC Infect Dis 2015; 15:403 [View Article] [PubMed]
     [Google Scholar]
  49. Polkowska A, Skoczyńska A, Paradowska-Stankiewicz I, Stefanoff P, Hryniewicz W et al. Pneumococcal meningitis before the introduction of 10-valent pneumococcal conjugate vaccine into the National Childhood Immunization Program in Poland. Vaccine 2019; 37:1365–1373 [View Article] [PubMed]
     [Google Scholar]
  50. Kaur R, Casey JR, Pichichero ME. Emerging Streptococcus pneumoniae strains colonizing the nasopharynx in children after 13-valent pneumococcal conjugate vaccination in comparison to the 7-valent era, 2006-2015. Pediatr Infect Dis J 2016; 35:901–906 [View Article] [PubMed]
     [Google Scholar]
  51. Tin Tin Htar M, Christopoulou D, Schmitt H-J. Pneumococcal serotype evolution in Western Europe. BMC Infect Dis 2015; 15:419 [View Article] [PubMed]
     [Google Scholar]
  52. Yildirim I, Little BA, Finkelstein J, Lee G, Hanage WP et al. Surveillance of pneumococcal colonization and invasive pneumococcal disease reveals shift in prevalent carriage serotypes in Massachusetts’ children to relatively low invasiveness. Vaccine 2017; 35:4002–4009 [View Article] [PubMed]
     [Google Scholar]
  53. Lo SW, Gladstone RA, van Tonder AJ, Lees JA, du Plessis M et al. Pneumococcal lineages associated with serotype replacement and antibiotic resistance in childhood invasive pneumococcal disease in the post-PCV13 era: an international whole-genome sequencing study. Lancet Infect Dis 2019; 19:759–769 [View Article] [PubMed]
     [Google Scholar]
  54. Hansen CB, Fuursted K, Valentiner-Branth P, Dalby T, Jørgensen CS et al. Molecular characterization and epidemiology of Streptococcus pneumoniae serotype 8 in Denmark. BMC Infect Dis 2021; 21:421 [View Article] [PubMed]
     [Google Scholar]
  55. Sanz JC, Rodríguez-Avial I, Ríos E, García-Comas L, Ordobás M et al. Increase of serotype 8, ST53 clone, as the prevalent strain of Streptococcus pneumoniae causing invasive disease in Madrid, Spain (2012-2015). Enferm Infecc Microbiol Clin (Engl Ed) 2020; 38:105–110 [View Article] [PubMed]
     [Google Scholar]
  56. WHO WHO. Global Antimicrobial Resistance and Use Surveillance System (GLASS) Report [Internet]. WHO; 2020 https://apps.who.int/iris/bitstream/handle/10665/332081/9789240005587-eng.pdf?ua=1
  57. Kuzmenkov AY, Trushin IV, Vinogradova AG, Avramenko AA, Sukhorukova MV et al. AMRmap: An interactive web platform for analysis of antimicrobial resistance surveillance data in Russia. Front Microbiol 2021; 12:620002 [View Article] [PubMed]
     [Google Scholar]
  58. Klugman KP, Black S. Impact of existing vaccines in reducing antibiotic resistance: Primary and secondary effects. Proc Natl Acad Sci U S A 2018; 115:12896–12901 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000851
Loading
Key features of pneumococcal isolates recovered in Central and Northwestern Russia in 2011–2018 determined through whole-genome sequencing
M Gen 8, 000851 (2022); https://doi.org/10.1099/mgen.0.000851
/content/journal/mgen/10.1099/mgen.0.000851
/content/journal/mgen/10.1099/mgen.0.000851
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error