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Abstract

In 2010, Burkina Faso completed the first nationwide mass-vaccination campaign of a meningococcal A conjugate vaccine, drastically reducing the incidence of disease caused by serogroup A meningococci. Since then, other strains, such as those belonging to serogroups W, X and C, have continued to cause outbreaks within the region. A carriage study was conducted in 2016 and 2017 in the country to characterize the meningococcal strains circulating among healthy individuals following the mass-vaccination campaign. Four cross-sectional carriage evaluation rounds were conducted in two districts of Burkina Faso, Kaya and Ouahigouya. Oropharyngeal swabs were collected for the detection of by culture. Confirmed isolates underwent whole-genome sequencing for molecular characterization. Among 13 758 participants, 1035 (7.5 %) . isolates were recovered. Most isolates (934/1035; 90.2 %) were non-groupable and primarily belonged to clonal complex (CC) 192 (822/934; 88 %). Groupable isolates (101/1035; 9.8 %) primarily belonged to CCs associated with recent outbreaks in the region, such as CC11 (serogroup W) and CC10217 (serogroup C); carried serogroup A isolates were not detected. Phylogenetic analysis revealed several CC11 strains circulating within the country, several of which were closely related to invasive isolates. Three sequence types (STs) were identified among eleven CC10217 carriage isolates, two of which have caused recent outbreaks in the region (ST-10217 and ST-12446). Our results show the importance of carriage studies to track the outbreak-associated strains circulating within the population in order to inform future vaccination strategies and molecular surveillance programmes.

Funding
This study was supported by the:
  • Centers for Disease Control and Prevention
    • Principle Award Recipient: NotApplicable
  • GAVI Alliance
    • Principle Award Recipient: NotApplicable
  • Bill and Melinda Gates Foundation
    • Principle Award Recipient: NotApplicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2020-12-11
2024-05-05
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References

  1. Meningococcal disease in countries of the African meningitis belt, 2012 Emerging needs and future perspectives. Wkly Epidemiol Rec 2013; 88:129–136[PubMed]
    [Google Scholar]
  2. Nicolas P, Norheim G, Garnotel E, Djibo S, Caugant DA. Molecular epidemiology of Neisseria meningitidis isolated in the African meningitis belt between 1988 and 2003 shows dominance of sequence type 5 (ST-5) and ST-11 complexes. J Clin Microbiol 2005; 43:5129–5135 [View Article][PubMed]
    [Google Scholar]
  3. Boisier P, Nicolas P, Djibo S, Taha M-K, Jeanne I et al. Meningococcal meningitis: unprecedented incidence of serogroup X-related cases in 2006 in Niger. Clin Infect Dis 2007; 44:657–663 [View Article][PubMed]
    [Google Scholar]
  4. Koumaré B, Ouedraogo-Traoré R, Sanou I, Yada AA, Sow I et al. The first large epidemic of meningococcal disease caused by serogroup W135, Burkina Faso, 2002. Vaccine 2007; 25 (Suppl. 1):A37–A41 [View Article][PubMed]
    [Google Scholar]
  5. Kretz CB, Retchless AC, Sidikou F, Issaka B, Ousmane S et al. Whole-genome characterization of epidemic Neisseria meningitidis serogroup C and resurgence of serogroup W, Niger, 2015. Emerg Infect Dis 2016; 22:17621768 [View Article][PubMed]
    [Google Scholar]
  6. Funk A, Uadiale K, Kamau C, Caugant DA, Ango U et al. Sequential outbreaks due to a new strain of Neisseria meningitidis serogroup C in northern Nigeria, 2013-14. PLoS Curr 2014; 6: [View Article][PubMed]
    [Google Scholar]
  7. Djingarey MH, Noazin S, Préziosi MP, Tiendrebéogo S, Toure K. A twenty years retrospective analysis of meningitis surveillance data from Burkina Faso, Mali and Niger. 16th International Pathogenic Neisseria Conference 2008 p P166
    [Google Scholar]
  8. Mueller JE, Sangaré L, Njanpop-Lafourcade B-M, Tarnagda Z, Traoré Y et al. Molecular characteristics and epidemiology of meningococcal carriage, Burkina Faso, 2003. Emerg Infect Dis 2007; 13:847–854 [View Article][PubMed]
    [Google Scholar]
  9. Centers for Disease Control and Prevention (CDC) Serogroup A meningococcal conjugate vaccine coverage after the first national mass immunization campaign – Burkina Faso, 2011. MMWR Morb Mortal Wkly Rep 2012; 61:1022–1024[PubMed]
    [Google Scholar]
  10. Kristiansen PA, Diomandé F, Wei SC, Ouédraogo R, Sangaré L et al. Baseline meningococcal carriage in Burkina Faso before the introduction of a meningococcal serogroup A conjugate vaccine. Clin Vaccine Immunol 2011; 18:435–443 [View Article][PubMed]
    [Google Scholar]
  11. Caugant DA, Nicolas P. Molecular surveillance of meningococcal meningitis in Africa. Vaccine 2007; 25 (Suppl. 1):A8–A11 [View Article][PubMed]
    [Google Scholar]
  12. Kristiansen PA, Diomandé F, Ba AK, Sanou I, Ouédraogo A-S et al. Impact of the serogroup A meningococcal conjugate vaccine, MenAfriVac, on carriage and herd immunity. Clin Infect Dis 2013; 56:354–363 [View Article][PubMed]
    [Google Scholar]
  13. Kristiansen PA, Ba AK, Sanou I, Ouédraogo A-S, Ouédraogo R et al. Phenotypic and genotypic characterization of meningococcal carriage and disease isolates in Burkina Faso after mass vaccination with a serogroup a conjugate vaccine. BMC Infect Dis 2013; 13:363 [View Article][PubMed]
    [Google Scholar]
  14. Kristiansen PA, Ba AK, Ouédraogo A-S, Sanou I, Ouédraogo R et al. Persistent low carriage of serogroup A Neisseria meningitidis two years after mass vaccination with the meningococcal conjugate vaccine, MenAfriVac. BMC Infect Dis 2014; 14:663 [View Article][PubMed]
    [Google Scholar]
  15. Novak RT, Kambou JL, Diomandé FV, Tarbangdo TF, Ouédraogo-Traoré R et al. Serogroup A meningococcal conjugate vaccination in Burkina Faso: analysis of national surveillance data. Lancet Infect Dis 2012; 12:757–764 [View Article][PubMed]
    [Google Scholar]
  16. Topaz N, Caugant DA, Taha M-K, Brynildsrud OB, Debech N et al. Phylogenetic relationships and regional spread of meningococcal strains in the meningitis belt, 2011–2016. EBioMedicine 2019; 41:488–496 [View Article][PubMed]
    [Google Scholar]
  17. WHO/IST-WA Weekly Feedback Bulletin on Cerebrospinal Meningitis Geneva: WHO; 2011
    [Google Scholar]
  18. MacNeil JR, Medah I, Koussoubé D, Novak RT, Cohn AC et al. Neisseria meningitidis serogroup W, Burkina Faso, 2012. Emerg Infect Dis 2014; 20:394–399 [View Article][PubMed]
    [Google Scholar]
  19. Lucidarme J, Hill DMC, Bratcher HB, Gray SJ, du Plessis M et al. Genomic resolution of an aggressive, widespread, diverse and expanding meningococcal serogroup B, C and W lineage. J Infect 2015; 71:544–552 [View Article][PubMed]
    [Google Scholar]
  20. Mbaeyi S, Sampo E, Dinanibè K, Yaméogo I, Congo-Ouédraogo M et al. Meningococcal carriage 7 years after introduction of a serogroup A meningococcal conjugate vaccine in Burkina Faso: results from four cross-sectional carriage surveys. Lancet Infect Dis 2020; 20:14181425 [View Article][PubMed]
    [Google Scholar]
  21. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 2011; 17:10–12 [View Article]
    [Google Scholar]
  22. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  23. Topaz N, Boxrud D, Retchless AC, Nichols M, Chang H-Y et al. BMScan: using whole genome similarity to rapidly and accurately identify bacterial meningitis causing species. BMC Infect Dis 2018; 18:405 [View Article][PubMed]
    [Google Scholar]
  24. Jolley KA, Maiden MCJ. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11:595 [View Article][PubMed]
    [Google Scholar]
  25. Marjuki H, Topaz N, Rodriguez-Rivera LD, Ramos E, Potts CC et al. Whole-genome sequencing for characterization of capsule locus and prediction of serogroup of invasive meningococcal isolates. J Clin Microbiol 2019; 57:e01609-18 [View Article][PubMed]
    [Google Scholar]
  26. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article][PubMed]
    [Google Scholar]
  27. 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]
  28. 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]
  29. 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]
  30. Brynildsrud OB, Eldholm V, Bohlin J, Uadiale K, Obaro S et al. Acquisition of virulence genes by a carrier strain gave rise to the ongoing epidemics of meningococcal disease in West Africa. Proc Natl Acad Sci USA 2018; 115:5510–5515 [View Article][PubMed]
    [Google Scholar]
  31. Kahler CM, Martin LE, Shih GC, Rahman MM, Carlson RW et al. The (α28)-linked polysialic acid capsule and lipooligosaccharide structure both contribute to the ability of serogroup B Neisseria meningitidis to resist the bactericidal activity of normal human serum. Infect Immun 1998; 66:5939–5947 [View Article][PubMed]
    [Google Scholar]
  32. Mackinnon FG, Borrow R, Gorringe AR, Fox AJ, Jones DM et al. Demonstration of lipooligosaccharide immunotype and capsule as virulence factors for Neisseria meningitidis using an infant mouse intranasal infection model. Microb Pathog 1993; 15:359–366 [View Article][PubMed]
    [Google Scholar]
  33. Caugant DA, Maiden MCJ. Meningococcal carriage and disease – population biology and evolution. Vaccine 2009; 27 (Suppl. 2):B64–B70 [View Article][PubMed]
    [Google Scholar]
  34. Bårnes GK, Kristiansen PA, Beyene D, Workalemahu B, Fissiha P et al. Prevalence and epidemiology of meningococcal carriage in Southern Ethiopia prior to implementation of MenAfriVac, a conjugate vaccine. BMC Infect Dis 2016; 16:639 [View Article][PubMed]
    [Google Scholar]
  35. Leimkugel J, Hodgson A, Forgor AA, Pflüger V, Dangy J-P et al. Clonal waves of Neisseria colonisation and disease in the African meningitis belt: eight- year longitudinal study in Northern Ghana. PLoS Med 2007; 4:e101 [View Article][PubMed]
    [Google Scholar]
  36. Brynildsrud OB, Eldholm V, Rakhimova A, Kristiansen PA, Caugant DA. Gauging the epidemic potential of a widely circulating non-invasive meningococcal strain in Africa. Microb Genom 2019; 5:e000290 [View Article][PubMed]
    [Google Scholar]
  37. MenAfriCar Consortium The diversity of meningococcal carriage across the African meningitis belt and the impact of vaccination with a group A meningococcal conjugate vaccine. J Infect Dis 2015; 212:1298–1307 [View Article][PubMed]
    [Google Scholar]
  38. WHO/IST-WA Weekly Feedback Bulletin on Cerebrospinal Meningitis Geneva: WHO; 2016
    [Google Scholar]
  39. WHO/IST-WA Weekly Feedback Bulletin on Cerebrospinal Meningitis Geneva: WHO; 2017
    [Google Scholar]
  40. Warren MJ, Roddam LF, Power PM, Terry TD, Jennings MP. Analysis of the role of pglI in pilin glycosylation of Neisseria meningitidis . FEMS Immunol Med Microbiol 2004; 41:43–50 [View Article][PubMed]
    [Google Scholar]
  41. Klughammer J, Dittrich M, Blom J, Mitesser V, Vogel U et al. Comparative genome sequencing reveals within-host genetic changes in Neisseria meningitidis during invasive disease. PLoS One 2017; 12:e0169892 [View Article][PubMed]
    [Google Scholar]
  42. Trivedi K, Tang CM, Exley RM. Mechanisms of meningococcal colonisation. Trends Microbiol 2011; 19:456–463 [View Article][PubMed]
    [Google Scholar]
  43. Coureuil M, Bourdoulous S, Marullo S, Nassif X. Invasive meningococcal disease: a disease of the endothelial cells. Trends Mol Med 2014; 20:571–578 [View Article][PubMed]
    [Google Scholar]
  44. Rohde KH, Gillaspy AF, Hatfield MD, Lewis LA, Dyer DW. Interactions of haemoglobin with the Neisseria meningitidis receptor HpuAB: the role of TonB and an intact proton motive force. Mol Microbiol 2002; 43:335–354 [View Article][PubMed]
    [Google Scholar]
  45. Bidmos FA, Chan H, Praekelt U, Tauseef I, Ali YM et al. Investigation into the antigenic properties and contributions to growth in blood of the meningococcal haemoglobin receptors, HpuAB and HmbR. PLoS One 2015; 10:e0133855 [View Article][PubMed]
    [Google Scholar]
  46. Tauseef I, Harrison OB, Wooldridge KG, Feavers IM, Neal KR et al. Influence of the combination and phase variation status of the haemoglobin receptors HmbR and HpuAB on meningococcal virulence. Microbiology 2011; 157:1446–1456 [View Article][PubMed]
    [Google Scholar]
  47. Jonsson AB, Nyberg G, Normark S. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J 1991; 10:477–488 [View Article][PubMed]
    [Google Scholar]
  48. Sanogo YO, Guindo I, Diarra S, Retchless AC, Abdou M et al. A new sequence type of Neisseria meningitidis serogroup C associated with a 2016 meningitis outbreak in Mali. J Infect Dis 2019; 220:S190–S197 [View Article][PubMed]
    [Google Scholar]
  49. Sidikou F, Zaneidou M, Alkassoum I, Schwartz S, Issaka B et al. Emergence of epidemic Neisseria meningitidis serogroup C in Niger, 2015: an analysis of national surveillance data. Lancet Infect Dis 2016; 16:1288–1294 [View Article][PubMed]
    [Google Scholar]
  50. MenAfriCar Consortium Household transmission of Neisseria meningitidis in the African meningitis belt: a longitudinal cohort study. Lancet Glob Health 2016; 4:e989–e995 [View Article][PubMed]
    [Google Scholar]
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