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Volume 10, Issue 3

serotype 3 population structure in the era of conjugate vaccines, 2001–2018 Open Access

Abstract

Despite use of highly effective conjugate vaccines, invasive pneumococcal disease (IPD) remains a leading cause of morbidity and mortality and disproportionately affects Indigenous populations. Although included in the 13-valent pneumococcal conjugate vaccine (PCV13), which was introduced in 2010, serotype 3 continues to cause disease among Indigenous communities in the Southwest USA. In the Navajo Nation, serotype 3 IPD incidence increased among adults (3.8/100 000 in 2001–2009 and 6.2/100 000 in 2011–2019); in children the disease persisted although the rates dropped from 5.8/100 000 to 2.3/100 000.

We analysed the genomic epidemiology of serotype 3 isolates collected from 129 adults and 63 children with pneumococcal carriage (=61) or IPD (=131) from 2001 to 2018 of the Navajo Nation. Using whole-genome sequencing data, we determined clade membership and assessed changes in serotype 3 population structure over time.

The serotype 3 population structure was characterized by three dominant subpopulations: (=90, 46.9 %) and (=59, 30.7 %), which fall into Clonal Complex (CC) 180, and a non-CC180 clade (=43, 22.4 %). The proportion of -associated IPD cases increased significantly from 2001 to 2010 to 2011–2018 among adults (23.1–71.8 %; <0.001) but not in children (27.3–33.3 %; =0.84). Over the same period, the proportion of associated carriage increased; this was statistically significant among children (23.3–52.6 %; =0.04) but not adults (0–50.0 %, =0.08).

In this setting with persistent serotype 3 IPD and carriage, has increased since 2010. Genomic changes may be contributing to the observed trends in serotype 3 carriage and disease over time.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Indigenous , phylogeny , serotype 3 and Streptococcus pneumoniae
Funding
This study was supported by the:
  • Robert Austrian Research Award
    • Principle Award Recipient: LindsayR Grant
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-04-28
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References

  1. Weiser JN, Ferreira DM, Paton JC. Streptococcus pneumoniae: transmission, colonization and invasion. Nat Rev Microbiol 2018; 16:355–367 [View Article] [PubMed]
     [Google Scholar]
  2. Ryan G, A. Patricia W, Miwako K. Pneumococcal disease. In Hall E, Wodi AP, Hamborsky J et al. eds Centers for Disease Control and Prevention. Epidemiology and Prevention of Vaccine-Preventable Diseases, 14th ed. Washington, D.C: Public Health Foundation; 2021
     [Google Scholar]
  3. Bentley SD, Aanensen DM, Mavroidi A, Saunders D, Rabbinowitsch E et al. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2006; 2:e31 [View Article]
     [Google Scholar]
  4. Ganaie F, Saad JS, McGee L, van Tonder AJ, Bentley SD et al. A new pneumococcal capsule type, 10D, is the 100th serotype and has a large cps fragment from an oral Streptococcus. mBio 2020; 11:e00937-20 [View Article] [PubMed]
     [Google Scholar]
  5. Lees JA, Croucher NJ, Goldblatt D, Nosten F, Parkhill J et al. Genome-wide identification of lineage and locus specific variation associated with pneumococcal carriage duration. Elife 2017; 6:e26255 [View Article] [PubMed]
     [Google Scholar]
  6. Troeger C, Forouzanfar M, Rao PC, Khalil I, Brown A. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory tract infections in 195 countries: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Infect Dis 2017; 17:1133–1161 [View Article] [PubMed]
     [Google Scholar]
  7. World Health Organisation The top 10 causes of death; 2020 https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death accessed 10 July 2023
  8. McAllister DA, Liu L, Shi T, Chu Y, Reed C et al. Global, regional, and national estimates of pneumonia morbidity and mortality in children younger than 5 years between 2000 and 2015: a systematic analysis. Lancet Glob Health 2019; 7:e47–e57 [View Article] [PubMed]
     [Google Scholar]
  9. Grzesiowski P, Aguiar-Ibáñez R, Kobryń A, Durand L, Puig P-E. Cost-effectiveness of polysaccharide pneumococcal vaccination in people aged 65 and above in Poland. Hum Vaccin Immunother 2012; 8:1382–1394 [View Article] [PubMed]
     [Google Scholar]
  10. Wagenvoort GHJ, Sanders EAM, de Melker HE, van der Ende A, Vlaminckx BJ et al. Long-term mortality after IPD and bacteremic versus non-bacteremic pneumococcal pneumonia. Vaccine 2017; 35:1749–1757 [View Article]
     [Google Scholar]
  11. Verhaegen J, Flamaing J, De Backer W, Delaere B, Van Herck K et al. Epidemiology and outcome of invasive pneumococcal disease among adults in Belgium, 2009–2011. Eurosurveillance 2014; 19: [View Article]
     [Google Scholar]
  12. McLaughlin JM, Jiang Q, Gessner BD, Swerdlow DL, Sings HL et al. Pneumococcal conjugate vaccine against serotype 3 pneumococcal pneumonia in adults: a systematic review and pooled analysis. Vaccine 2019; 37:6310–6316 [View Article] [PubMed]
     [Google Scholar]
  13. 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]
  14. Ho PL, Law PYT, Chiu SS. Increase in incidence of invasive pneumococcal disease caused by serotype 3 in children eight years after the introduction of the pneumococcal conjugate vaccine in Hong Kong. Hum Vaccin Immunother 2019; 15:455–458 [View Article] [PubMed]
     [Google Scholar]
  15. Horácio AN, Silva-Costa C, Lopes JP, Ramirez M, Melo-Cristino J et al. Serotype 3 remains the leading cause of invasive pneumococcal disease in adults in Portugal (2012-2014) despite continued reductions in other 13-valent conjugate vaccine serotypes. Front Microbiol 2016; 7:1616 [View Article] [PubMed]
     [Google Scholar]
  16. ACIP October 19-20 Presentation Slides | Immunization Practices | CDC; 2022 https://www.cdc.gov/vaccines/acip/meetings/slides-2022-10-19-20.html accessed 14 May 2023
  17. Azarian T, Mitchell PK, Georgieva M, Thompson CM, Ghouila A et al. Global emergence and population dynamics of divergent serotype 3 CC180 pneumococci. PLoS Pathog 2018; 14:e1007438 [View Article]
     [Google Scholar]
  18. Groves N, Sheppard CL, Litt D, Rose S, Silva A et al. Evolution of Streptococcus pneumoniae serotype 3 in England and Wales: a major vaccine evader. Genes 2019; 10:845 [View Article] [PubMed]
     [Google Scholar]
  19. Gagetti P, Lo SW, Hawkins PA, Gladstone RA, Regueira M et al. Population genetic structure, serotype distribution and antibiotic resistance of Streptococcus pneumoniae causing invasive disease in children in Argentina. Microb Genom 2021; 7:636 [View Article] [PubMed]
     [Google Scholar]
  20. Centers for Disease Control and Prevention ACIP Pneumococcal Vaccine Recommendations; 2023 https://www.cdc.gov/vaccines/hcp/acip-recs/vacc-specific/pneumo.html accessed 20 August 2023
  21. Indian Health Service National Immunization Reporting System. Quarterly Immunization Coverage Reports; 2021 https://www.ihs.gov/epi/immunization-and-vaccine-preventable-diseases/statistics-and-reports/ accessed 12 January 2022
  22. Grant LR, Hammitt LL, O’Brien SE, Jacobs MR, Donaldson C et al. Impact of the 13-valent pneumococcal conjugate vaccine on pneumococcal carriage among American Indians. Pediatr Infect Dis J 2016; 35:907–914 [View Article] [PubMed]
     [Google Scholar]
  23. Littlepage S, Sutcliffe C, Yazzie D, Tso C, Weatherholtz R et al. Impact of Pneumococcal Conjugate Vaccines (PCV) and the COVID-19 Pandemic on Invasive Pneumococcal Disease (IPD) Among Native Americans Living on the Navajo Nation. In International Symposium of Pneumococci and Pneumococcal DiseasesToronto, Canada 2022
     [Google Scholar]
  24. Cella E, Weatherholtz R, Sutcliffe C, Littlepage S, Reid R et al. Changes in Streptococcus pneumoniae serotype 3 population structure in the context of persistent carriage and disease among Native Americans in the Southwest US. In International Symposium on Pneumococci and Pneumococcal DiseasesToronto, Canada 2022
     [Google Scholar]
  25. Weatherholtz R, Millar EV, Moulton LH, Reid R, Rudolph K et al. Invasive pneumococcal disease a decade after pneumococcal conjugate vaccine use in an American Indian population at high risk for disease. Clin Infect Dis 2010; 50:1238–1246 [View Article] [PubMed]
     [Google Scholar]
  26. Scott JR, Millar EV, Lipsitch M, Moulton LH, Weatherholtz R et al. Impact of more than a decade of pneumococcal conjugate vaccine use on carriage and invasive potential in Native American communities. J Infect Dis 2012; 205:280–288 [View Article] [PubMed]
     [Google Scholar]
  27. Littlepage SJ, Grant L, Vidal J, Jacobs M, Weatherholtz R et al. Differences in pneumococcal carriage prevalence by testing method and specimen type among Native American individuals during routine use of 13-valent pneumococcal conjugate vaccine (PCV13). In International Symposium of Pneumococci and Pneumococcal Diseases Toronto, Canada: 2022
     [Google Scholar]
  28. Grant L, Weatherholtz R, Alexander-Parrish R, Jacobs M, Good C et al. Nasopharyngeal pneumococcal carriage among American Indian children and adults during routine use of the 13-valent pneumococcal conjugate vaccine (PCV13). In International Symposium of Pneumococci and Pneumococcal Diseases Melbourne, Australia: 2018
     [Google Scholar]
  29. Cella E, Sutcliffe CG, Tso C, Paul E, Ritchie N et al. Carriage prevalence and genomic epidemiology of Staphylococcus aureus among Native American children and adults in the Southwestern USA. Microb Genom 2022; 8:806 [View Article] [PubMed]
     [Google Scholar]
  30. Chen C, Khaleel SS, Huang H, Wu CH. Software for pre-processing Illumina next-generation sequencing short read sequences. Source Code Biol Med 2014; 9:8 [View Article] [PubMed]
     [Google Scholar]
  31. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
     [Google Scholar]
  32. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
     [Google Scholar]
  33. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
     [Google Scholar]
  34. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
     [Google Scholar]
  35. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. Fast hierarchical Bayesian analysis of population structure. Nucleic Acids Res 2019; 47:5539–5549 [View Article]
     [Google Scholar]
  36. Seemann T. ABRicate: Mass Screening of Contigs for Antimicrobial and Virulence Genes GitHub;
     [Google Scholar]
  37. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 2014; 58:212–220 [View Article]
     [Google Scholar]
  38. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: hierarchical and refined dataset for big data analysis—10 years on. Nucleic Acids Res 2016; 44:D694–D697 [View Article]
     [Google Scholar]
  39. Seeman T. Scan contig files against PubMLST typing schemes; 2022 https://github.com/tseemann/mlst
  40. 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]
  41. 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]
  42. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2016; 2:vew007 [View Article]
     [Google Scholar]
  43. Volz EM, Frost SDW. Scalable relaxed clock phylogenetic dating. Virus Evol 2017; 3: [View Article]
     [Google Scholar]
  44. Hill V, Baele G. Bayesian estimation of past population dynamics in BEAST 1.10 using the skygrid coalescent model. Mol Biol Evol 2019; 36:2620–2628 [View Article] [PubMed]
     [Google Scholar]
  45. Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 2018; 4:vey016 [View Article] [PubMed]
     [Google Scholar]
  46. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol 2018; 67:901–904 [View Article] [PubMed]
     [Google Scholar]
  47. Helekal D, Ledda A, Volz E, Wyllie D, Didelot X. Bayesian inference of clonal expansions in a dated phylogeny. Syst Biol 2022; 71:1073–1087 [View Article] [PubMed]
     [Google Scholar]
  48. Gagetti P, Lo SW, Hawkins PA, Gladstone RA, Regueira M et al. Population genetic structure, serotype distribution and antibiotic resistance of Streptococcus pneumoniae causing invasive disease in children in Argentina. Microb Genom 2021; 7:636 [View Article] [PubMed]
     [Google Scholar]
  49. Hyams C, Challen R, Hettle D, Amin-Chowdhury Z, Grimes C. Trends in serotype distribution and disease severity in adults hospitalised with Streptococcus pneumoniae infection in Bristol and Bath: a retrospective cohort study, 2006-2022. Respir Med X [View Article]
     [Google Scholar]
  50. Centers for Disease Control and Prevention Active bacterial core surveillance report, emerging infections program network, Streptococcus pneumoniae; 2020
  51. Croucher NJ, Mitchell AM, Gould KA, Inverarity D, Barquist L et al. Dominant role of nucleotide substitution in the diversification of serotype 3 pneumococci over decades and during a single infection. PLoS Genet 2013; 9:e1003868 [View Article] [PubMed]
     [Google Scholar]
  52. Echániz-Aviles G, Guerreiro SI, Silva-Costa C, Mendes CI, Carriço JA et al. Streptococcus pneumoniae serotype 3 in Mexico (1994 to 2017): decrease of the unusual clonal complex 4909 lineage following PCV13 introduction. J Clin Microbiol 2019; 57: [View Article]
     [Google Scholar]
  53. Melin MM, Hollingshead SK, Briles DE, Lahdenkari MI, Kilpi TM et al. Development of antibodies to PspA families 1 and 2 in children after exposure to Streptococcus pneumoniae. Clin Vaccine Immunol 2008; 15:1529–1535 [View Article] [PubMed]
     [Google Scholar]
  54. Lucas A, Wilson M, L. Sings H, Pugh S, Jones D et al. Estimating the vaccine effectiveness against serotype 3 for the 13-valent pneumococcal conjugate vaccine: a dynamic modeling approach. IJIDT 2019; 4:56 [View Article]
     [Google Scholar]
  55. Izurieta P, Bahety P, Adegbola R, Clarke C, Hoet B. Public health impact of pneumococcal conjugate vaccine infant immunization programs: assessment of invasive pneumococcal disease burden and serotype distribution. Expert Rev Vaccines 2018; 17:479–493 [View Article] [PubMed]
     [Google Scholar]
  56. Hanquet G, Krizova P, Valentiner-Branth P, Ladhani SN, Nuorti JP et al. Effect of childhood pneumococcal conjugate vaccination on invasive disease in older adults of 10 European countries: implications for adult vaccination. Thorax 2019; 74:473–482 [View Article] [PubMed]
     [Google Scholar]
  57. Sings HL, Gessner BD, Wasserman MD, Jodar L. Pneumococcal conjugate vaccine impact on serotype 3: a review of surveillance data. Infect Dis Ther 2021; 10:521–539 [View Article] [PubMed]
     [Google Scholar]
  58. Hanage WP, Finkelstein JA, Huang SS, Pelton SI, Stevenson AE et al. Evidence that pneumococcal serotype replacement in Massachusetts following conjugate vaccination is now complete. Epidemics 2010; 2:80–84 [View Article] [PubMed]
     [Google Scholar]
  59. Azarian T, Martinez PP, Arnold BJ, Qiu X, Grant LR et al. Frequency-dependent selection can forecast evolution in Streptococcus pneumoniae. PLoS Biol 2020; 18:e3000878 [View Article] [PubMed]
     [Google Scholar]
  60. 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]
  61. Sekulovic O, Gallagher C, Lee J, Hao L, Anderson A et al. Characterization of pneumococcal serotype 3 isolates from distinct phylogenetic clades in mouse models of carriage and invasive disease. In International Symposium of Pneumococci and Pneumococcal Diseases Toronto, Canada: 2022
     [Google Scholar]
  62. Chaguza C, Andam CP, Harris SR, Cornick JE, Yang M et al. Recombination in Streptococcus pneumoniae lineages increase with carriage duration and size of the polysaccharide capsule. mBio 2016; 7:e01053–16 [View Article]
     [Google Scholar]
  63. Lin J, Zhu L, Lau GW. Disentangling competence for genetic transformation and virulence in Streptococcus pneumoniae. Curr Genet 2016; 62:97–103 [View Article] [PubMed]
     [Google Scholar]
  64. Luck JN, Tettelin H, Orihuela CJ. Sugar-coated killer: serotype 3 pneumococcal disease. Front Cell Infect Microbiol 2020; 10:613287 [View Article] [PubMed]
     [Google Scholar]
  65. Oliveira GS, Oliveira MLS, Miyaji EN, Rodrigues TC. Pneumococcal vaccines: past findings, present work, and future strategies. Vaccines (Basel) 2021; 9:1338 [View Article] [PubMed]
     [Google Scholar]
  66. Darrieux M, Goulart C, Briles D, Leite LC de C. Current status and perspectives on protein-based pneumococcal vaccines. Crit Rev Microbiol 2015; 41:190–200 [View Article] [PubMed]
     [Google Scholar]
  67. Lagousi T, Basdeki P, Routsias J, Spoulou V. Novel protein-based pneumococcal vaccines: assessing the use of distinct protein fragments instead of full-length proteins as vaccine antigens. Vaccines 2019; 7:9 [View Article] [PubMed]
     [Google Scholar]
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Streptococcus pneumoniae serotype 3 population structure in the era of conjugate vaccines, 2001–2018
M Gen 10, 001196 (2024); https://doi.org/10.1099/mgen.0.001196
/content/journal/mgen/10.1099/mgen.0.001196
/content/journal/mgen/10.1099/mgen.0.001196
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