Outbreaks of meningococcal B infection and the 4CMenB vaccine: Historical and future perspectives

Expert Review of Vaccines

Volumn 14, Issue 5, 2015, Pages 713-736

  Whelan, Jane ^a   Bambini, Stefania ^b   Biolchi, Alessia ^b   Brunelli, Brunella ^b   Robert Du Ry Van Beest Holle, Mirna ^a  

^a Research and Development   (Netherlands)

^b NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

Author keywords

4CMenB; coverage; epidemiology; invasive meningococcal disease; Neisseria meningitidis, serogroup B; outbreaks; vaccine

Indexed keywords

4CMENB VACCINE; COMPLEMENT; MENINGOCOCCUS VACCINE; OUTER MEMBRANE PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; BACTERIUM ANTIBODY;

AGE DISTRIBUTION; ANTIBODY TITER; ASSAY; BACTERIAL STRAIN; BACTERIUM EXAMINATION; BACTERIUM ISOLATE; CUBA; DRUG ANTIGENICITY; EPIDEMIC; HOUSEKEEPING GENE; HUMAN; HUMAN SERUM BACTERICIDAL ASSAY; IMMUNOGENICITY; INFECTION PREVENTION; MENINGOCOCCAL ANTIGEN TYPING SYSTEM; MENINGOCOCCOSIS; MULTILOCUS ENZYME ELECTROPHORESIS; MULTILOCUS SEQUENCE TYPING; NEISSERIA MENINGITIDIS; NEW ZEALAND; NONHUMAN; NORWAY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SERUM BACTERICIDAL ACTIVITY; UNITED STATES; VACCINATION; BLOOD; HEALTH; HISTORY; IMMUNOLOGY; ISOLATION AND PURIFICATION; MENINGITIS, MENINGOCOCCAL; MICROBIOLOGY; PROCEDURES; TRENDS;

ANTIBODIES, BACTERIAL; BLOOD BACTERICIDAL ACTIVITY; DISEASE OUTBREAKS; GLOBAL HEALTH; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; MENINGITIS, MENINGOCOCCAL; MENINGOCOCCAL VACCINES; NEISSERIA MENINGITIDIS, SEROGROUP B; VACCINATION;

EID: 84927722448     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.2015.1004317     Document Type: Review

References (180)

1. Khatami A, Pollard AJ. The epidemiology of meningococcal disease and the impact of vaccines. Expert Rev Vaccines 2010;9(3): 285-98
2. Edmond K, Clark A, Korczak VS, et al. Global and regional risk of disabling sequelae from bacterial meningitis: a systematic review and meta-Analysis. Lancet Infect Dis 2010;10(5):317-28
3. Brooks R, Woods CW, Benjamin DK Jr., Rosenstein NE. Increased case-fatality rate associated with outbreaks of Neisseria meningitidis infection, compared with sporadic meningococcal disease, in the United States, 1994-2002. Clin Infect Dis 2006;43(1):49-54
4. Abbott JD, Jones DM, Painter MJ, Young SE. The epidemiology of meningococcal infections in England and Wales, 1912-1983. J infect 1985;11(3): 241-57
5. Peltola H, Jonsdottir K, Lystad A, et al. Meningococcal disease in Scandinavia. Br Med J (Clin Res Ed) 1982;284(6329): 1618-21
6. Harrison LH, Trotter CL, Ramsay ME. Global epidemiology of meningococcal disease. Vaccine 2009;27(Suppl 2):B51-63
7. World Health Organisation. Meningococcal disease control in countries of the African meningitis belt, 2013. Wkly Epidemiol Rec 2014;20(89):206-14
8. Rosenstein NE, Perkins BA, Stephens DS, et al. The changing epidemiology of meningococcal disease in the United States, 1992-1996. J Infect Dis 1999;180(6): 1894-901
9. Harrison OB, Claus H, Jiang Y, et al. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg Infect Dis 2013;19(4):566-73
10. Stephens DS, Greenwood B, Brandtzaeg P. Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 2007; 369(9580):2196-210
11. Jafri RZ, Ali A, Messonnier NE, et al. Global epidemiology of invasive meningococcal disease. Popul Health Metr 2013;11(1):17
12. Harrison LH. Epidemiological profile of meningococcal disease in the United States. Clin Infect Dis 2010;50(Suppl 2):S37-44
13. Heymann DL. Control of communicable diseases manual. American Public Health Association; Washington, DC: 2008; 746 pp
14. Health Protection Agency Meningococcus and Haemophilus Forum. Guidance for public health management of meningococcal disease in the UK. Health Protection Agency, UK; 2012
15. Ladhani S, Cordery R, Mandal S, et al. Preventing secondary cases of invasive meningococcal capsular group B (MenB) disease: benefits of offering vaccination in addition to antibiotic chemoprophylaxis to close contacts of cases in the household, educational setting, clusters and the wider community. Public Health England; London: 2014
16. Public Health Agency Canada. Guidelines for the Prevention and Control of Meningococcal Disease. Canada Communicable Disease Report, 3151. 2005
17. Cohn AC, MacNeil JR, Clark TA, et al. Prevention and control of meningococcal disease: recommendations of the Advisory Committee on Immunization Practices (ACIP). Appendix B. MMWR. Recommendations and reports : Morbidity and mortality weekly report. Recommendations and reports/Centers for Disease Control, 62(RR-2). 2013;1-28
18. Communicable Diseases Network Australia. Guidelines for the early clinical and public health management of meningococcal disease in Australia. Australian Government: Department of Health and Ageing. 2007
19. Meningococcal Outbreak Working Group Members. Interim Guidance for Control of Serogroup B Meningococcal Disease Outbreaks in Organizational Settings. Centre for Disease Prevention and Control; Atlanta: 2014
20. Kelsey J, Thompson W, Evans A. Methods in observational epidemiology. Oxford University Press; New York: 1986
21. Jarvis GA, Vedros NA. Sialic acid of group B Neisseria meningitidis regulates alternative complement pathway activation. Infect Immun 1987;55(1):174-80
22. Frasch CE, Zollinger WD, Poolman JT. Serotype antigens of Neisseria meningitidis and a proposed scheme for designation of serotypes. Rev Infect Dis 1985;7(4):504-10
23. Maiden MC, Frosch M. Molecular techniques for the investigation of meningococcal disease epidemiology. Mol Biotechnol 2001;18(2):119-34
24. Caugant DA. Population genetics and molecular epidemiology of Neisseria meningitidis. APMIS 1998;106(5):505-25
25. Maiden MC, Bygraves JA, Feil E, et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proceedings of the National Academy of Sciences of the United States of America, 1998. 95(6):3140-5
26. Jolley KA, Brehony C, Maiden MC. Molecular typing of meningococci: recommendations for target choice and nomenclature. FEMS Microbiol Rev 2007; 31(1):89-96
27. Masignani V, Comanducci M, Giuliani MM, et al. Vaccination against Neisseria meningitidis using three variants of the lipoprotein GNA1870. J Exp Med 2003;197(6):789-99
28. Serruto D, Spadafina T, Ciucchi L, et al. Neisseria meningitidis GNA2132, a heparin-binding protein that induces protective immunity in humans. Proceedings of the National Academy of Sciences of the United States of America, 2010. 107(8):3770
29. Comanducci M, Bambini S, Brunelli B, et al. NadA, a novel vaccine candidate of Neisseria meningitidis. J Exp Med 2002; 195(11):1445-54
30. Centre for Reviews and Dissemination. Systematic Reviews: CRD's guidance for undertaking reviews in health care. CRD, University of York, York. 2008
31. Howitz M, Lambertsen L, Simonsen JB, et al. Morbidity, mortality and spatial distribution of meningococcal disease, 1974-2007. Epidemiol Infect 2009;137(11): 1631-40
32. Taha MK, Deghmane AE, Antignac A, et al. The duality of virulence and transmissibility in Neisseria meningitidis. Trends Microbiol 2002;10(8):376-82
33. Stephens DS. Uncloaking the meningococcus: dynamics of carriage and disease. Lancet 1999;353(9157):941-2
34. Diermayer M, Hedberg K, Hoesly F, et al. Epidemic serogroup B meningococcal disease in Oregon: the evolving epidemiology of the ET-5 strain. JAMA 1999;281(16):1493-7
35. Caugant DA. Genetics and evolution of Neisseria meningitidis: importance for the epidemiology of meningococcal disease. Infect Genet Evol 2008;8(5):558-65
36. Brehony C, Trotter CL, Ramsay ME, et al. Implications of differential age distribution of disease-Associated meningococcal lineages for vaccine development. Clin Vaccine Immunol 2014;21(6):847-53
37. Watkins ER, Maiden MC. Persistence of hyperinvasive meningococcal strain types during global spread as recorded in the PubMLST database. PLoS One 2012 7 9 e45349
38. Yazdankhah SP, Kriz P, Tzanakaki G, et al. Distribution of serogroups and genotypes among disease-Associated and carried isolates of Neisseria meningitidis from the Czech Republic, Greece, and Norway. J Clin Microbiol 2004;42(11):5146-53
39. Caugant DA, Maiden MC. Meningococcal carriage and disease-population biology and evolution. Vaccine 2009;27(Suppl 2): B64-70
40. Bjune G, Closs O, Froholm LO, et al. Design of clinical trials with an outer membrane vesicle vaccine against systemic serogroup B meningococcal disease in Norway. NIPH Annals 1991;14(2):81-91; discussion 91-83
41. Bjune G, Hoiby EA, Gronnesby JK, et al. Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet 1991;338(8775):1093-6
42. Racloz VN, Luiz SJ. The elusive meningococcal meningitis serogroup: a systematic review of serogroup B epidemiology. BMC Infect Dis 2010;10:175
43. Verdu ME, Coll P, Vazquez JA, et al. Association between asymptomatic carriage and sporadic (endemic) meningococcal disease in an open community. Epidemiol Infect 2001;127(2):245-59
44. Caugant DA, Froholm LO, Bovre K, et al. Intercontinental spread of a genetically distinctive complex of clones of Neisseria meningitidis causing epidemic disease. Proceedings of the National Academy of Sciences of the United States of America 1986. 83(13):4927-31
45. Sierra GV, Campa HC, Varcacel NM, et al. Vaccine against group B Neisseria meningitidis: protection trial and mass vaccination results in Cuba. NIPH Annals 1991;14(2):195-207; discussion 208-110
46. Climent Y, Yero D, Martinez I, et al. Clonal distribution of disease-Associated and healthy carrier isolates of Neisseria meningitidis between 1983 and 2005 in Cuba. J Clin Microbiol 2010;48(3):802-10
47. de Filippis I, de Lemos AP, Hostetler JB, et al. Molecular epidemiology of Neisseria meningitidis serogroup B in Brazil. PLoS One 2012;7(3):e33016
48. de Moraes JC, Perkins BA, Camargo MC, et al. Protective efficacy of a serogroup B meningococcal vaccine in Sao Paulo. Brazil. Lancet 1992;340(8827):1074-8
49. Cruz C, Pavez G, Aguilar E, et al. Serotype-specific outbreak of group B meningococcal disease in Iquique, Chile. Epidemiol Infect 1990;105(1):119-26
50. Boslego J, Garcia J, Cruz C, et al. Efficacy, safety, and immunogenicity of a meningococcal group B (15:P1.3) outer membrane protein vaccine in Iquique, Chile. Chilean National Committee for Meningococcal Disease. Vaccine 1995; 13(9):821-9
51. Tappero JW, Lagos R, Ballesteros AM, et al. Immunogenicity of 2 serogroup B outer-membrane protein meningococcal vaccines: a randomized controlled trial in Chile. JAMA 1999;281(16):1520-7
52. Rouaud P, Perrocheau A, Taha MK, et al. Prolonged outbreak of B meningococcal disease in the Seine-Maritime department, France, January 2003 to June 2005. Euro Surveill 2006;11(7):178-81
53. Caron F, du Chatelet IP, Leroy JP, et al. From tailor-made to ready-to-wear meningococcal B vaccines: longitudinal study of a clonal meningococcal B outbreak. Lancet Infect Dis 2011;11(6):455-63
54. Tondella ML, Popovic T, Rosenstein NE, et al. Distribution of Neisseria meningitidis serogroup B serosubtypes and serotypes circulating in the United States. The Active Bacterial Core Surveillance Team. J Clin Microbiol 2000;38(9):3323-8
55. Wiringa AE, Shutt KA, Marsh JW, et al. Geotemporal analysis of Neisseria meningitidis clones in the United States: 2000-2005. PLoS One 2013;8(12):e82048
56. Patel M. Use of a novel serogroup B meningococcal vaccine in response to two university outbreaks in the US. In: XIX International Pathogenic Neisseria Conference (IPNC). Asheville, NC US, 2014
57. Neisseria Sequence Typing Home Page. Available from: http://pubmlst.org/neisseria/
58. Maiden MC. The impact of molecular techniques on the study of meningococcal disease. Methods Mol Med 1998;15:265-91
59. Jolley KA, Kalmusova J, Feil EJ, et al. Carried meningococci in the Czech Republic: a diverse recombining population. J Clin Microbiol 2000;38(12):4492-8
60. Scholten RJ, Poolman JT, Valkenburg HA, et al. Phenotypic and genotypic changes in a new clone complex of Neisseria meningitidis causing disease in The Netherlands, 1958-1990. J Infect Dis 1994;169(3):673-6
61. Baker MG, Martin DR, Kieft CE, Lennon D. A 10-year serogroup B meningococcal disease epidemic in New Zealand: descriptive epidemiology, 1991-2000. J Paediatr Child Health 2001; 37(5):S13-19
62. Arnold R, Galloway Y, McNicholas A, O'Hallahan J. Effectiveness of a vaccination programme for an epidemic of meningococcal B in New Zealand. Vaccine 2011;29(40):7100-6
63. Zarantonelli ML, Lancellotti M, Deghmane AE, et al. Hyperinvasive genotypes of Neisseria meningitidis in France. Clin Microbiol Infect 2008;14(5): 467-72
64. Cohn AC, MacNeil JR, Harrison LH, et al. Changes in Neisseria meningitidis disease epidemiology in the United States, 1998-2007: implications for prevention of meningococcal disease. Clin Infect Dis 2010;50(2):184-91
65. Barra GN, Araya PA, Fernandez JO, et al. Molecular characterization of invasive Neisseria meningitidis strains isolated in Chile during 2010-2011. PLoS One 2013; 8(6):e66006
66. Elias J, Schouls LM, van de Pol I, et al. Vaccine preventability of meningococcal clone, Greater Aachen Region, Germany. Emerging Infect Dis 2010;16(3):465-72
67. Cleary P. A cluster of meningococcal disease in West Cumbria. Health Protection Agency; North Wales: 2011
68. Lucidarme J, Comanducci M, Findlow J, et al. Characterization of fHbp, nhba (gna2132), nadA, porA, sequence type (ST), and genomic presence of IS1301 in group B meningococcal ST269 clonal complex isolates from England and Wales. J Clin Microbiol 2009;47(11):3577-85
69. Bertrand S, Van Meervenne E, De Baere T, et al. Detection of a geographical and endemic cluster of hyper-invasive meningococcal strains. Microbes Infect 2011;13(7):684-90
70. Delisle E, Larrieu S, Simoes J, et al. Community outbreak of group B meningococcal disease in southwest France-December 2008 to September 2009. Euro Surveill 2010;15:37
71. Law DK, Lorange M, Ringuette L, et al. Invasive meningococcal disease in Quebec, Canada, due to an emerging clone of ST-269 serogroup B meningococci with serotype antigen 17 and serosubtype antigen P1.19 (B:17:P1.19). J Clin Microbiol 2006; 44(8):2743-9
72. Zhou J, Lefebvre B, Deng S, et al. Invasive serogroup B Neisseria meningitidis in Quebec, Canada, 2003 to 2010: persistence of the ST-269 clone since it first emerged in 2003. J Clin Microbiol 2012;50(5):1545-51
73. Mandal S, Wu HM, MacNeil JR, et al. Prolonged university outbreak of meningococcal disease associated with a serogroup B strain rarely seen in the United States. Clin Infect Dis 2013;57(3):344-8
74. Yazdankhah SP, Kesanopoulos K, Tzanakaki G, et al. Variable-number tandem repeat analysis of meningococcal isolates belonging to the sequence type 162 complex. J Clin Microbiol 2005; 43(9):4865-7
75. Tzanakaki G, Kesanopoulos K, Yazdankhah SP, et al. Conventional and molecular investigation of meningococcal isolates in relation to two outbreaks in the area of Athens, Greece. Clin Microbiol Infect 2006;12(10):1024-6
76. Available from: http://pubmlst.org/
77. Seib KL, Zhao X, Rappuoli R. Developing vaccines in the era of genomics: a decade of reverse vaccinology. Clin Microbiol Infect 2012;18(Suppl 5):109-16
78. Giuliani MM, Adu-Bobie J, Comanducci M, et al. A universal vaccine for serogroup B meningococcus. Proceedings of the National Academy of Sciences of the United States of America, 2006. 103(29):10834-9
79. FDA. Available from: www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm420998.htm
80. Madico G, Welsch JA, Lewis LA, et al. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J Immunol 2006;177(1):501-10
81. Bambini S, Muzzi A, Olcen P, et al. Distribution and genetic variability of three vaccine components in a panel of strains representative of the diversity of serogroup B meningococcus. Vaccine 2009;27(21): 2794-803
82. Jacobsson S, Hedberg ST, Molling P, et al. Prevalence and sequence variations of the genes encoding the five antigens included in the novel 5CVMB vaccine covering group B meningococcal disease. Vaccine 2009; 27(10):1579-84
83. Bambini S, De Chiara M, Muzzi A, et al. Neisseria adhesin A variation and revised nomenclature scheme. Clin Vaccine Immunol 2014;21(7):966-71
84. Comanducci M, Bambini S, Caugant DA, et al. NadA diversity and carriage in Neisseria meningitidis. Infect Immun 2004; 72(7):4217-23
85. Bambini S, Piet J, Muzzi A, et al. An analysis of the sequence variability of meningococcal fHbp, NadA and NHBA over a 50-year period in the Netherlands. PLoS One 2013;8(5):e65043
86. Donnelly J, Medini D, Boccadifuoco G, et al. Qualitative and quantitative assessment of meningococcal antigens to evaluate the potential strain coverage of protein-based vaccines. Proceedings of the National Academy of Sciences of the United States of America, 2010. 107(45):19490-5
87. Goldschneider I, Gotschlich EC, Artenstein MS. Human immunity to the meningococcus. I. The role of humoral antibodies. J Exp Med 1969;129(6): 1307-26
88. Borrow R, Aaberge IS, Santos GF, et al. Interlaboratory standardization of the measurement of serum bactericidal activity by using human complement against meningococcal serogroup b, strain 44/76-SL, before and after vaccination with the Norwegian MenBvac outer membrane vesicle vaccine. Clin Diagn Lab Immunol 2005;12(8):970-6
89. Urwin R, Feavers IM, Jones DM, et al. Molecular variation of meningococcal serotype 4 antigen genes. Epidemiol Infect 1998;121(1):95-101
90. Holst J, Oster P, Arnold R, et al. Vaccines against meningococcal serogroup B disease containing outer membrane vesicles (OMV): lessons from past programs and implications for the future. Hum Vaccin Immunother 2013;9(6):1241-53
91. Gossger N, Snape MD, Yu LM, et al. Immunogenicity and tolerability of recombinant serogroup B meningococcal vaccine administered with or without routine infant vaccinations according to different immunization schedules: a randomized controlled trial. JAMA 2012; 307(6):573-82
92. Vesikari T, Esposito S, Prymula R, et al. Immunogenicity and safety of an investigational multicomponent, recombinant, meningococcal serogroup B vaccine (4CMenB) administered concomitantly with routine infant and child vaccinations: results of two randomised trials. Lancet 2013;381(9869):825-35
93. Snape MD, Dawson T, Oster P, et al. Immunogenicity of two investigational serogroup B meningococcal vaccines in the first year of life: a randomized comparative trial. Pediatr Infect Dis J 2010;29(11):e71-9
94. Kimura A, Toneatto D, Kleinschmidt A, et al. Immunogenicity and safety of a multicomponent meningococcal serogroup B vaccine and a quadrivalent meningococcal CRM197 conjugate vaccine against serogroups A, C, W-135, and Y in adults who are at increased risk for occupational exposure to meningococcal isolates. Clin Vaccine Immunol 2011;18(3):483-6
95. Santolaya ME, O'Ryan ML, Valenzuela MT, et al. Immunogenicity and tolerability of a multicomponent meningococcal serogroup B (4CMenB) vaccine in healthy adolescents in Chile: a phase 2b/3 randomised, observer-blind, placebo-controlled study. Lancet 2012;379(9816):617-24
96. Santolaya ME, O'Ryan M, Valenzuela MT, et al. Persistence of antibodies in adolescents 18-24 months after immunization with one, two, or three doses of 4CMenB meningococcal serogroup B vaccine. Hum Vaccin Immunother 2013;9(11):2304-10
97. Safety, Tolerability and Immunogenicity of Novartis Meningococcal B Recombinant Vaccine Administered to Healthy Adolescents According to Different Vaccination Schedules. Available from: https://clinicaltrials.gov/ct2/show/NCT00661713
98. De Serres G, Garie-py M, Billard M, Rouleau I. Initial Dose of a Multicomponent Serogroup B Meningococcal Vaccine in the Saguenay-Lac-Saint-Jean Region, Que-bec, Canada: An Interim Safety Surveillance Report. Institut national de sante-publique du Que-bec; Quebec, Canada: 2014
99. Vogel U, Taha MK, Vazquez JA, et al. Predicted strain coverage of a meningococcal multicomponent vaccine (4CMenB) in Europe: a qualitative and quantitative assessment. Lancet Infect Dis 2013;13(5): 416-25
100. Snape MD, Medini D, Halperin SA, et al. The challenge of post-implementation surveillance for novel meningococcal vaccines. Vaccine 2012;30(Suppl 2):B67-72
101. Biolchi A. Potential coverage of the Bexsero-vaccine on non-B meningococci (poster). In: XIXth International Pathogenic Neisseria Conference (IPNC). Asheville, NC, USA, 2014
102. Hong E, Giuliani MM, Deghmane AE, et al. Could the multicomponent meningococcal serogroup B vaccine (4CMenB) control Neisseria meningitidis capsular group X outbreaks in Africa Vaccine 2013;31(7):1113-16
103. Joint Committee on Vaccination and Immunisation (JCVI). JCVI position statement on use of Bexsero-meningococcal B vaccine in the UK. 2014
104. Meningococcal B Pilot Project Task Group. The recommended use of the multicomponent meningococcal B (4CMenB) vaccine in Canada. Public Health Agency Canada, 2014
105. Kristiansen BE, Ask E, Jenkins A, et al. Rapid diagnosis of meningococcal meningitis by polymerase chain reaction. Lancet 1991;337(8757):1568-9
106. Qian Q, Tang YW, Kolbert CP, et al. Direct identification of bacteria from positive blood cultures by amplification and sequencing of the 16S rRNA gene: evaluation of BACTEC 9240 instrument true-positive and false-positive results. J Clin Microbiol 2001;39(10):3578-82
107. Corless CE, Guiver M, Borrow R, et al. Simultaneous detection of Neisseria meningitidis, Haemophilus influenzae, and Streptococcus pneumoniae in suspected cases of meningitis and septicemia using real-time PCR. J Clin Microbiol 2001; 39(4):1553-8
108. Guiver M, Borrow R, Marsh J, et al. Evaluation of the Applied Biosystems automated Taqman polymerase chain reaction system for the detection of meningococcal DNA. FEMS Immunol Med Microbiol 2000;28(2):173-9
109. Taha MK. Simultaneous approach for nonculture PCR-based identification and serogroup prediction of Neisseria meningitidis. J Clin Microbiol 2000;38(2): 855-7
110. Bennett DE, Mulhall RM, Cafferkey MT. PCR-based assay for detection of Neisseria meningitidis capsular serogroups 29E, X, and Z. J Clin Microbiol 2004;42(4):1764-5
111. Zhu H, Wang Q, Wen L, et al. Development of a multiplex PCR assay for detection and genogrouping of Neisseria meningitidis. J Clin Microbiol 2012;50(1): 46-51
112. Neisseria PorA typing. Available from: http://pubmlst.org/neisseria/PorA/
113. Russell JE, Jolley KA, Feavers IM, et al. PorA variable regions of Neisseria meningitidis. Emerg Infect Dis 2004;10(4): 674-8
114. Neisseria FetA variable region typing. Available from: http://pubmlst.org/neisseria/FetA/
115. Thompson EA, Feavers IM, Maiden MC. Antigenic diversity of meningococcal enterobactin receptor FetA, a vaccine component. Microbiology 2003;149(Pt 7): 1849-58
116. Brehony C, Jolley KA, Maiden MC. Multilocus sequence typing for global surveillance of meningococcal disease. FEMS Microbiol Rev 2007;31(1):15-26
117. Bygraves JA, Maiden MC. Analysis of the clonal relationships between strains of Neisseria meningitidis by pulsed field gel electrophoresis. J Gen Microbiol 1992; 138(3):523-31
118. Taha MK, Vazquez JA, Hong E, et al. Target gene sequencing to characterize the penicillin G susceptibility of Neisseria meningitidis. Antimicrob Agents Chemother 2007;51(8):2784-92
119. Neisseria porB typing. Available from: http://pubmlst.org/neisseria/porB/
120. Urwin R, Kaczmarski EB, Guiver M, et al. Amplification of the meningococcal porB gene for non-culture serotype characterization. Epidemiol Infect 1998; 120(3):257-62
121. Neisseria meningitidis Home Page. Available from: http://neisseria.org/nm/
122. Budroni S, Siena E, Dunning Hotopp JC, et al. Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination. Proceedings of the National Academy of Sciences of the United States of America 2011. 108(11): 4494-9
123. Available from: http://pubmlst.org/Neisseria/fHbp
124. Available from: http://pubmlst.org/Neisseria/nhba
125. Available from: http://pubmlst.org/Neisseria/nadA
126. Bovre K, Holten E, Vik-Mo H, et al. Neisseria meningitidis infections in Northern Norway: an epidemic in 1974-1975 due mainly to group B organisms. J Infect Dis 1977;135(4):669-72
127. Bovre K, Gedde-Dahl TW. Epidemiological patterns of meningococcal disease in Norway 1975-1979. NIPH Annals 1980; 3(2):9-22
128. Lystad A, Aasen S. The epidemiology of meningococcal disease in Norway 1975-91. NIPH Annals 1991;14(2):57-65; discussion 65-56
129. Wedege E, Kolberg J, Delvig A, et al. Emergence of a new virulent clone within the electrophoretic type 5 complex of serogroup B meningococci in Norway. Clin Diagn Lab Immunol 1995;2(3):314-21
130. Iversen BG, Aavitsland P. Meningococcal disease in Norway 1992-1995. Epidemiology and fatality. Scand J Infect Dis 1996;28(3):253-9
131. Bevanger L, Bergh K, Gisnas G, et al. Identification of nasopharyngeal carriage of an outbreak strain of Neisseria meningitidis by pulsed-field gel electrophoresis versus phenotypic methods. J Med Microbiol 1998;47(11):993-8
132. Smith I, Bjornevik AT, Augland IM, et al. Variations in case fatality and fatality risk factors of meningococcal disease in Western Norway, 1985-2002. Epidemiol Infect 2006;134(1):103-10
133. Terry Molinert G, Demina AA, Valcarcel Novo M. Epidemiological characteristics of meningococcal infection in Cuba. Zhurnal Mikrobiologii, Epidemiologii, i Immunobiologii 1986(2): 54-9
134. Martinez Motas I, Sierra Gonzalez G, Nunez Gutierrez N, et al. [Characterization of Neisseria meningitidis strains isolated from carriers in Cuba during 20 years]. Rev Cubana Med Trop 2006;58(2):124-33
135. Rodriguez AP, Dickinson F, Baly A, Martinez R. The epidemiological impact of antimeningococcal B vaccination in Cuba. Mem Inst Oswaldo Cruz 1999;94(4): 433-40
136. Wylie PA, Stevens D, Drake W 3rd, et al. Epidemiology and clinical management of meningococcal disease in west Gloucestershire: retrospective, population based study. BMJ 1997;315(7111):774-9
137. Cartwright KA, Stuart JM, Noah ND. An outbreak of meningococcal disease in Gloucestershire. Lancet 1986;2(8506): 558-61
138. Fitzpatrick PE, Salmon RL, Hunter PR, et al. Risk factors for carriage of Neisseria meningitidis during an outbreak in Wales. Emerg Infect Dis 2000;6(1):65-9
139. Davies AL, O'Flanagan D, Salmon RL, Coleman TJ. Risk factors for Neisseria meningitidis carriage in a school during a community outbreak of meningococcal infection. Epidemiol Infect 1996;117(2): 259-66
140. Blackwell CC, Weir DM, James VS, et al. Secretor status, smoking and carriage of Neisseria meningitidis. Epidemiol Infect 1990;104(2):203-9
141. Castillo L, Maldonado A, Garcia J, et al. Characterization of Neisseria meningitidis isolated fron systemic infections. Chile, 1992-1993. Revista Medica de Chile 1994; 122(7):760-7
142. Sacchi CT, Pessoa LL, Ramos SR, et al. Ongoing group B Neisseria meningitidis epidemic in Sao Paulo, Brazil, due to increased prevalence of a single clone of the ET-5 complex. J Clin Microbiol 1992; 30(7):1734-8
143. Sacchi CT, de Lemos AP, Camargo MC, et al. Meningococcal disease caused by Neisseria meningitidis serogroup B serotype 4 in Sao Paulo, Brazil, 1990 to 1996. Revista do Instituto de Medicina Tropical de Sao Paulo 1998;40(2):65-70
144. Sacchi CT, Lemos AP, Popovic T, et al. Serosubtypes and PorA types of Neisseria meningitidis serogroup B isolated in Brazil during 1997-1998: overview and implications for vaccine development. J Clin Microbiol 2001;39(8):2897-903
145. Baethgen LF, Weidlich L, Moraes C, et al. Epidemiology of meningococcal disease in southern Brazil from 1995 to 2003, and molecular characterization of Neisseria meningitidis using multilocus sequence typing. Trop Med Int Health 2008;13(1): 31-40
146. Barroso DE, Carvalho DM, Casagrande ST, et al. Microbiological epidemiological history of meningococcal disease in Rio de Janeiro, Brazil. Brazilian J Infect Dis 2010; 14(3):242-51
147. Frasch CE, Mocca LF, Karpas AB. Appearance of new strains associated with group B meningococcal disease and their use for rapid vaccine development. Antonie van Leeuwenhoek 1987;53(6):395-402
148. Centers for Disease Control and Prevention (CDC). Serogroup B meningococcal disease-Oregon, 1994. MMWR Morb Mortal Wkly Rep 1995;44(7):121-4
149. Meyer S. Epidemiology of Meningococcal Disease Outbreaks in the United States. Advisory Committee on Immunization Practices. 2014
150. Le Guerrier P, Pilon P, Sauvageau C, Deshaies D. Spatio-temporal cluster of cases of invasive group B Neisseria meningitidis infections on the island of Montreal. Can Commun Dis Rep 1997;23(4):25-8
151. Taha MK, Bichier E, Perrocheau A, Alonso JM. Circumvention of herd immunity during an outbreak of meningococcal disease could be correlated to escape mutation in the porA gene of Neisseria meningitidis. Infect Immun 2001; 69(3):1971-3
152. Grodet C, Dequin PF, Watt S, et al. Outbreak in France of Neisseria meningitidis B:15:P1.12 belonging to sequence type 1403. Clin Microbiol Infect 2004;10(9):845-8
153. Caron F, Delbos V, Houivet E, et al. Evolution of immune response against Neisseria meningitidis B:14:P1.7,16 before and after the outer membrane vesicle vaccine MenBvac. Vaccine 2012;30(34): 5059-62
154. Martin DR, Walker SJ, Baker MG, Lennon DR. New Zealand epidemic of meningococcal disease identified by a strain with phenotype B:4:P1.4. J Infect Dis 1998; 177(2):497-500
155. Bremner C, Lennon D, Martin D, et al. Epidemic meningococcal disease in New Zealand: epidemiology and potential for prevention by vaccine. N Z Med J 1999; 112(1091):257-9
156. Dyet K, Devoy A, McDowell R, Martin D. New Zealand's epidemic of meningococcal disease described using molecular analysis: implications for vaccine delivery. Vaccine 2005;23(17-18):2228-30
157. Devoy AF, Dyet KH, Martin DR. Stability of PorA during a meningococcal disease epidemic. J Clin Microbiol 2005;43(2): 832-7
158. Dyet KH, Martin DR. Clonal analysis of the serogroup B meningococci causing New Zealand's epidemic. Epidemiol Infect 2006; 134(2):377-83
159. Kelly C, Arnold R, Galloway Y, O'Hallahan J. A prospective study of the effectiveness of the New Zealand meningococcal B vaccine. Am J Epidemiol 2007;166(7):817-23
160. Hosking J, Rasanathan K, Mow FC, et al. Immunogenicity, reactogenicity, and safety of a P1.7b,4 strain-specific serogroup B meningococcal vaccine given to preteens. Clin Vaccine Immunol 2007;14(11):1393-9
161. Galloway Y, Stehr-Green P, McNicholas A, O'Hallahan J. Use of an observational cohort study to estimate the effectiveness of the New Zealand group B meningococcal vaccine in children aged under 5 years. Int J Epidemiol 2009;38(2):413-18
162. O'Hallahan J, McNicholas A, Galloway Y, et al. Delivering a safe and effective strain-specific vaccine to control an epidemic of group B meningococcal disease. N Z Med J 2009;122(1291):48-59
163. Wong SH, Lennon DR, Jackson CM, et al. Immunogenicity and tolerability in infants of a New Zealand epidemic strain meningococcal B outer membrane vesicle vaccine. Pediatr Infect Dis J 2009;28(5): 385-90
164. Lopez L, Sexton K, Carter P. The Epidemiology of Meningococcal Disease in New Zealand in 2011. Institute of Environmental Science and Research Ltd (ESR; Wellington, New Zealand: 2012
165. Gilca R, Deceuninck G, Lefebvre B, et al. The changing epidemiology of meningococcal disease in Quebec, Canada, 1991-2011: potential implications of emergence of new strains. PLoS One 2012; 7(11):e50659
166. Bettinger JA, Scheifele DW, Le Saux N, et al. The disease burden of invasive meningococcal serogroup B disease in Canada. Pediatr Infect Dis J 2013;32(1): e20-5
167. Ya L, Tsang R, Desai S, Deehan H. Enhanced surveillance of invasive meningococcal disease in Canada, 2006-2011. Can Commun Dis Rep 2014; 40:9
168. Perez-Trallero E, Vicente D, Montes M, Cisterna R. Positive effect of meningococcal C vaccination on serogroup replacement in Neisseria meningitidis. Lancet 2002; 360(9337):953
169. Trotter CL, Ramsay ME. Vaccination against meningococcal disease in Europe: review and recommendations for the use of conjugate vaccines. FEMS Microbiol Rev 2007;31(1):101-7
170. Brundage JF, Ryan MA, Feighner BH, Erdtmann FJ. Meningococcal disease among United States military service members in relation to routine uses of vaccines with different serogroup-specific components, 1964-1998. Clin Infect Dis 2002;35(11): 1376-81
171. Ashton FE, Ryan JA, Borczyk A, et al. Emergence of a virulent clone of Neisseria meningitidis serotype 2a that is associated with meningococcal group C disease in Canada. J Clin Microbiol 1991;29(11): 2489-93
172. Krizova P, Musilek M. Changing epidemiology of meningococcal invasive disease in the Czech republic caused by new clone Neisseria meningitidis C:2a:P1.2 (P1.5), ET-15/37. Cent Eur J Public Health 1995;3(4):189-94
173. Ramsay ME, Collins M, Rush M, Kaczmarksi E. The epidemiology of meningococcal disease in England and Wales, 1996 and 1997. Euro Surveill 1997; 2(10):74-5
174. Chacon-Cruz E, Espinosa-De Los Monteros LE, Navarro-Alvarez S, et al. An outbreak of serogroup C (ST-11) meningococcal disease in Tijuana, Mexico. Ther Adv Vaccines 2014;2(3):71-6
175. Mayer LW, Reeves MW, Al-Hamdan N, et al. Outbreak of W135 meningococcal disease in 2000: not emergence of a new W135 strain but clonal expansion within the electophoretic type-37 complex. J Infect Dis 2002;185(11):1596-605
176. Sorhouet-Pereira C, Efron A, Gagetti P, et al. Phenotypic and genotypic characteristics of Neisseria meningitidis disease-causing strains in Argentina, 2010. PLoS One 2013;8(3):e58065
177. Berron S, De La Fuente L, Martin E, Vazquez JA. Increasing incidence of meningococcal disease in Spain associated with a new variant of serogroup C. Eur J Clin Microbiol Infect Dis 1998;17(2):85-9
178. de Lemos AP, Yara TY, Gorla MC, et al. Clonal distribution of invasive Neisseria meningitidis serogroup C strains circulating from 1976 to 2005 in greater Sao Paulo, Brazil. J Clin Microbiol 2007;45(4): 1266-73
179. Alcala B, Salcedo C, Arreaza L, et al. The epidemic wave of meningococcal disease in Spain in 1996-1997: probably a consequence of strain displacement. J Med Microbiol 2002;51(12):1102-6
180. Cano R, Larrauri A, Mateo S, et al. Impact of the meningococcal C conjugate vaccine in Spain: an epidemiological and microbiological decision. Euro Surveill 2004;9(7):11-15