1887
  1. Home
  2. Eurosurveillance
  3. Volume 24, Issue 1, 03/Jan/2019
  4. Article
Research article Open Access
Like 0
Download

Abstract

Background

In 1999, the United Kingdom (UK) was the first country to introduce meningococcal group C (MenC) conjugate vaccination. This vaccination programme has evolved with further understanding, new vaccines and changing disease epidemiology.

Aim

To characterise MenC disease and population protection against MenC disease in England.

Methods

Between 1998/99–2015/16, surveillance data from England for laboratory-confirmed MenC cases were collated; using the screening method, we updated vaccine effectiveness (VE) estimates. Typing data and genomes were obtained from the Meningitis Research Foundation Meningococcus Genome Library and PubMLST database. Phylogenetic network analysis of MenC cc11 isolates was undertaken. We compared bactericidal antibody assay results using anonymised sera from 2014 to similar data from 1996–1999, 2000–2004 and 2009.

Results

MenC cases fell from 883 in 1998/99 (1.81/100,000 population) to 42 cases (0.08/100,000 population) in 2015/16. Lower VE over time since vaccination was observed after infant immunisation (p = 0.009) and a single dose at 1–4 years (p = 0.03). After vaccination at 5–18 years, high VE was sustained for ≥ 8 years; 95.0% (95% CI: 76.0– 99.5%). Only 25% (75/299) children aged 1–14 years were seroprotected against MenC disease in 2014. Recent case isolates mostly represented two cc11 strains.

Conclusion

High quality surveillance has furthered understanding of MenC vaccines and improved schedules, maximising population benefit. The UK programme provides high direct and indirect protection despite low levels of seroprotection in some age groups. High-resolution characterisation supports ongoing surveillance of distinct MenC cc11 lineages.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2019.24.1.1700818
2019-01-03
2019-09-15
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.1.1700818
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/24/1/eurosurv-24-1-3.html?itemId=/content/10.2807/1560-7917.ES.2019.24.1.1700818&mimeType=html&fmt=ahah

References

  1. Sáfadi MA, Bettinger JA, Maturana GM, Enwere G, Borrow RGlobal Meningococcal Initiative. Evolving meningococcal immunization strategies. Expert Rev Vaccines. 2015;14(4):505-17.  https://doi.org/10.1586/14760584.2015.979799  PMID: 25494168 
  2. Miller E, Salisbury D, Ramsay M. Planning, registration, and implementation of an immunisation campaign against meningococcal serogroup C disease in the UK: a success story. Vaccine. 2001;20(Suppl 1):S58-67.  https://doi.org/10.1016/S0264-410X(01)00299-7  PMID: 11587814 
  3. Whittaker R, Dias JG, Ramliden M, Ködmön C, Economopoulou A, Beer N, et al. The epidemiology of invasive meningococcal disease in EU/EEA countries, 2004-2014. Vaccine. 2017;35(16):2034-41.  https://doi.org/10.1016/j.vaccine.2017.03.007  PMID: 28314560 
  4. Ramsay ME, Andrews NJ, Trotter CL, Kaczmarski EB, Miller E. Herd immunity from meningococcal serogroup C conjugate vaccination in England: database analysis. BMJ. 2003;326(7385):365-6.  https://doi.org/10.1136/bmj.326.7385.365  PMID: 12586669 
  5. Campbell H, Andrews N, Borrow R, Trotter C, Miller E. Updated postlicensure surveillance of the meningococcal C conjugate vaccine in England and Wales: effectiveness, validation of serological correlates of protection, and modeling predictions of the duration of herd immunity. Clin Vaccine Immunol. 2010;17(5):840-7.  https://doi.org/10.1128/CVI.00529-09  PMID: 20219881 
  6. Maiden MC, Stuart JMUK Meningococcal Carraige Group. Carriage of serogroup C meningococci 1 year after meningococcal C conjugate polysaccharide vaccination. Lancet. 2002;359(9320):1829-31.  https://doi.org/10.1016/S0140-6736(02)08679-8  PMID: 12044380 
  7. Ladhani SN, Ramsay M, Borrow R, Riordan A, Watson JM, Pollard AJ. Enter B and W: two new meningococcal vaccine programmes launched. Arch Dis Child. 2016;101(1):91-5.  https://doi.org/10.1136/archdischild-2015-308928  PMID: 26672098 
  8. Trotter C, Borrow R, Andrews N, Miller E. Seroprevalence of meningococcal serogroup C bactericidal antibody in England and Wales in the pre-vaccination era. Vaccine. 2003;21(11-12):1094-8.  https://doi.org/10.1016/S0264-410X(02)00630-8  PMID: 12559785 
  9. Trotter CL, Borrow R, Findlow J, Holland A, Frankland S, Andrews NJ, et al. Seroprevalence of antibodies against serogroup C meningococci in England in the postvaccination era. Clin Vaccine Immunol. 2008;15(11):1694-8.  https://doi.org/10.1128/CVI.00279-08  PMID: 18827191 
  10. Ishola DA Jr, Borrow R, Findlow H, Findlow J, Trotter C, Ramsay ME. Prevalence of serum bactericidal antibody to serogroup C Neisseria meningitidis in England a decade after vaccine introduction. Clin Vaccine Immunol. 2012;19(8):1126-30.  https://doi.org/10.1128/CVI.05655-11  PMID: 22647271 
  11. Gray SJ, Trotter CL, Ramsay ME, Guiver M, Fox AJ, Borrow R, et al. Epidemiology of meningococcal disease in England and Wales 1993/94 to 2003/04: contribution and experiences of the Meningococcal Reference Unit. J Med Microbiol. 2006;55(Pt 7):887-96.  https://doi.org/10.1099/jmm.0.46288-0  PMID: 16772416 
  12. Ladhani SN, Waight PA, Ribeiro S, Ramsay ME. Invasive meningococcal disease in England: assessing disease burden through linkage of multiple national data sources. BMC Infect Dis. 2015;15(1):551.  https://doi.org/10.1186/s12879-015-1247-7  PMID: 26626321 
  13. Farrington CP. Estimation of vaccine effectiveness using the screening method. Int J Epidemiol. 1993;22(4):742-6.  https://doi.org/10.1093/ije/22.4.742  PMID: 8225751 
  14. National Health Service (NHS) digital. Statistics and data collections. Available from: https://digital.nhs.uk/data-and-information
  15. The Health Improvement Network (THIN). London: THIN; 2018. Available from: http://www.inps.co.uk/vision/thin/about-us
  16. Jolley KA, Maiden MC. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics. 2010;11(1):595.  https://doi.org/10.1186/1471-2105-11-595  PMID: 21143983 
  17. Hill DM, Lucidarme J, Gray SJ, Newbold LS, Ure R, Brehony C, et al. Genomic epidemiology of age-associated meningococcal lineages in national surveillance: an observational cohort study. Lancet Infect Dis. 2015;15(12):1420-8.  https://doi.org/10.1016/S1473-3099(15)00267-4  PMID: 26515523 
  18. Lucidarme J, Lekshmi A, Parikh SR, Bray JE, Hill DM, Bratcher HB, et al. Frequent capsule switching in ‘ultra-virulent’ meningococci - Are we ready for a serogroup B ST-11 complex outbreak? J Infect. 2017;75(2):95-103.  https://doi.org/10.1016/j.jinf.2017.05.015  PMID: 28579305 
  19. Huson DH. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics. 1998;14(1):68-73.  https://doi.org/10.1093/bioinformatics/14.1.68  PMID: 9520503 
  20. Osborne K, Gay N, Hesketh L, Morgan-Capner P, Miller E. Ten years of serological surveillance in England and Wales: methods, results, implications and action. Int J Epidemiol. 2000;29(2):362-8.  https://doi.org/10.1093/ije/29.2.362  PMID: 10817137 
  21. Maslanka SE, Gheesling LL, Libutti DE, Donaldson KB, Harakeh HS, Dykes JK, et al. The Multilaboratory Study Group. Standardization and a multilaboratory comparison of Neisseria meningitidis serogroup A and C serum bactericidal assays. Clin Diagn Lab Immunol. 1997;4(2):156-67. PMID: 9067649 
  22. Borrow R, Balmer P, Miller E. Meningococcal surrogates of protection--serum bactericidal antibody activity. Vaccine. 2005;23(17-18):2222-7.  https://doi.org/10.1016/j.vaccine.2005.01.051  PMID: 15755600 
  23. Neal KR, Nguyen-Van-Tam J, Monk P, O’Brien SJ, Stuart J, Ramsay M. Invasive meningococcal disease among university undergraduates: association with universities providing relatively large amounts of catered hall accommodation. Epidemiol Infect. 1999;122(3):351-7.  https://doi.org/10.1017/S0950268899002368  PMID: 10459636 
  24. Simmons RD, Kirwan P, Beebeejaun K, Riordan A, Borrow R, Ramsay ME, et al. Risk of invasive meningococcal disease in children and adults with HIV in England: a population-based cohort study. BMC Med. 2015;13(1):297.  https://doi.org/10.1186/s12916-015-0538-6  PMID: 26654248 
  25. Folaranmi TA, Kretz CB, Kamiya H, MacNeil JR, Whaley MJ, Blain A, et al. Increased Risk for Meningococcal Disease Among Men Who Have Sex With Men in the United States, 2012-2015. Clin Infect Dis. 2017;65(5):756-63.  https://doi.org/10.1093/cid/cix438  PMID: 28505234 
  26. Miglietta A, Fazio C, Neri A, Pezzotti P, Innocenti F, Azzari C, et al. Interconnected clusters of invasive meningococcal disease due to Neisseria meningitidis serogroup C ST-11 (cc11), involving bisexuals and men who have sex with men, with discos and gay-venues hotspots of transmission, Tuscany, Italy, 2015 to 2016. Euro Surveill. 2018;23(34):1700636.  https://doi.org/10.2807/1560-7917.ES.2018.23.34.1700636  PMID: 30153883 
  27. Lucidarme J, Hill DM, Bratcher HB, Gray SJ, du Plessis M, Tsang RS, et al. Genomic resolution of an aggressive, widespread, diverse and expanding meningococcal serogroup B, C and W lineage. J Infect. 2015;71(5):544-52.  https://doi.org/10.1016/j.jinf.2015.07.007  PMID: 26226598 
  28. Hill DM, Lucidarme J, Gray SJ, Newbold LS, Ure R, Brehony C, et al. Genomic epidemiology of age-associated meningococcal lineages in national surveillance: an observational cohort study. Lancet Infect Dis. 2015;15(12):1420-8.  https://doi.org/10.1016/S1473-3099(15)00267-4  PMID: 26515523 
  29. Tzeng YL, Bazan JA, Turner AN, Wang X, Retchless AC, Read TD, et al. Emergence of a new Neisseria meningitidis clonal complex 11 lineage 11.2 clade as an effective urogenital pathogen. Proc Natl Acad Sci USA. 2017;114(16):4237-42.  https://doi.org/10.1073/pnas.1620971114  PMID: 28373547 
  30. Taha MK, Claus H, Lappann M, Veyrier FJ, Otto A, Becher D, et al. Evolutionary events associated with an outbreak of meningococcal disease in men who have sex with men. PLoS One. 2016;11(5):e0154047.  https://doi.org/10.1371/journal.pone.0154047  PMID: 27167067 
  31. Kupferschmidt K. Infectious diseases. Bacterial meningitis finds new niche in gay communities. Science. 2013;341(6144):328.  https://doi.org/10.1126/science.341.6144.328  PMID: 23888010 
  32. Bazan JA, Turner AN, Kirkcaldy RD, Retchless AC, Kretz CB, Briere E, et al. Large cluster of Neisseria meningitidis urethritis in Columbus, Ohio, 2015. Clin Infect Dis. 2017;65(1):92-9.  https://doi.org/10.1093/cid/cix215  PMID: 28481980 
  33. Stoof SP, van der Klis FRM, van Rooijen DM, Knol MJ, Sanders EAM, Berbers GAM. Timing of an adolescent booster after single primary meningococcal serogroup C conjugate immunization at young age; an intervention study among Dutch teenagers. PLoS One. 2014;9(6):e100651.  https://doi.org/10.1371/journal.pone.0100651  PMID: 24963638 
  34. Parent du Chatelet I, Deghmane AE, Antona D, Hong E, Fonteneau L, Taha MK, et al. Characteristics and changes in invasive meningococcal disease epidemiology in France, 2006-2015. J Infect. 2017;74(6):564-74.  https://doi.org/10.1016/j.jinf.2017.02.011  PMID: 28279715 
  35. World Health Organisation (WHO). Continuing risk of meningitis due to Neisseria meningitidis serogroup C in Africa: revised recommendations from a WHO expert consultation. Wkly Epidemiol Rec. 2017;92(41):612-7. PMID: 29028166 
  36. Nunes AM, Ribeiro GS, Ferreira ÍE, Moura AR, Felzemburgh RD, de Lemos AP, et al. Meningococcal Carriage among Adolescents after Mass Meningococcal C Conjugate Vaccination Campaigns in Salvador, Brazil. PLoS One. 2016;11(11):e0166475.  https://doi.org/10.1371/journal.pone.0166475  PMID: 27861618 
Serogroup C Neisseria meningitidis disease epidemiology, seroprevalence, vaccine effectiveness and waning immunity, England, 1998/99 to 2015/16
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Helen+Findlow&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Findlow Helen</a>, <a href="/search?value1=Helen+Campbell&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Campbell Helen</a>, <a href="/search?value1=Jay+Lucidarme&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lucidarme Jay</a>, <a href="/search?value1=Nick+Andrews&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Andrews Nick</a>, <a href="/search?value1=Ezra+Linley&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Linley Ezra</a>, <a href="/search?value1=Shamez+Ladhani&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ladhani Shamez</a>, <a href="/search?value1=Ray+Borrow&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Borrow Ray</a></span>. Serogroup C Neisseria meningitidis disease epidemiology, seroprevalence, vaccine effectiveness and waning immunity, England, 1998/99 to 2015/16. <a href="/content/ecdc">Euro Surveill.</a> 2019;24(1):pii=1700818. <a href="https://doi.org/10.2807/1560-7917.ES.2019.24.1.1700818" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2019.24.1.1700818</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 05 Dec 2017;&nbsp;&nbsp; <span class="generated">Accepted</span>: 07 Jul 2018 </span> </p>
/content/10.2807/1560-7917.ES.2019.24.1.1700818
/content/10.2807/1560-7917.ES.2019.24.1.1700818
Loading

Data & Media loading...

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed
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