Emergence of serogroup X meningococcal disease in Africa: Need for a vaccine

Vaccine

Volumn 31, Issue 27, 2013, Pages 2852-2861

  Xie, Ouli ^a,c   Pollard, Andrew J ^a,c   Mueller, Judith E ^b,c   Norheim, Gunnstein ^a,d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b EHESP SCHOOL OF PUBLIC HEALTH   (France)

^c INSTITUT PASTEUR   (France)

^d NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

Author keywords

Epidemiology; Meningococcal disease; Neisseria meningitidis; Serogroup X; Vaccines

Indexed keywords

MENINGOCOCCUS VACCINE;

AFRICA; BACTERIAL MENINGITIS; CLIMATE; DISEASE SURVEILLANCE; HUMAN; INCIDENCE; INNATE IMMUNITY; MENINGOCOCCOSIS; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; RISK FACTOR;

AFRICA SOUTH OF THE SAHARA; BIOMEDICAL RESEARCH; DISEASE OUTBREAKS; HUMANS; INCIDENCE; MENINGITIS, MENINGOCOCCAL; MENINGOCOCCAL VACCINES; NEISSERIA MENINGITIDIS; VACCINES, CONJUGATE;

EID: 84878451674     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2013.04.036     Document Type: Review

References (123)

1. Peltola H. Burden of meningitis and other severe bacterial infections of children in africa: implications for prevention. Clin Infect Dis 2001, 32:64-75.
2. Stephens D.S., Greenwood B., Brandtzaeg P. Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 2007, 369:2196-2210.
3. Ramakrishnan M., Ulland A.J., Steinhardt L.C., Moisi J.C., Were F., Levine O.S. Sequelae due to bacterial meningitis among African children: a systematic literature review. BMC Microbiol 2009, 7:47.
4. Greenwood B.M., Bradley A.K., Smith A.W., Wall R.A. Mortality from meningococcal disease during an epidemic in The Gambia, West Africa. Trans R Soc Trop Med Hyg 1987, 81:536-538.
5. Molesworth A.M., Thomson M.C., Connor S.J., Cresswell M.P., Morse A.P., Shears P., et al. Where is the meningitis belt? Defining an area at risk of epidemic meningitis in Africa. Trans R Soc Trop Med Hyg 2002, 96:242-249.
6. Lapeyssonnie L. Cerebrospinal meningitis in AFRICA. Bull World Health Organ 1963, 28(Suppl.):1-114.
7. Trotter C.L., Greenwood B.M. Meningococcal carriage in the African meningitis belt. Lancet Infect Dis 2007, 7:797-803.
8. Christensen H., May M., Bowen L., Hickman M., Trotter C.L. Meningococcal carriage by age: a systematic review and meta-analysis. Lancet Infect Dis 2010, 10:853-861.
9. Kristiansen P.A., Diomande F., Ba A.K., Sanou I., Ouedraogo A.S., Ouedraogo R., et al. Impact of the serogroup A meningococcal conjugate vaccine, MenAfriVac, on carriage and herd immunity. Clin Infect Dis 2013, 56:354-363.
10. Mueller J.E., Yaro S., Njanpop-Lafourcade B.M., Drabo A., Idohou R.S., Kroman S.S., et al. Study of a localized meningococcal meningitis epidemic in Burkina Faso: incidence, carriage, and immunity. J Infect Dis 2011, 204:1787-1795.
11. Molesworth A.M., Cuevas L.E., Connor S.J., Morse A.P., Thomson M.C. Environmental risk and meningitis epidemics in Africa. Emerg Infect Dis 2003, 9:1287-1293.
12. Mueller J.E., Gessner B.D. A hypothetical explanatory model for meningococcal meningitis in the African meningitis belt. Int J Infect Dis 2010, 14:e553-e559.
13. World Health Organization Meningitis in Chad, Niger and Nigeria: 2009 epidemic season. Wkly Epidemiol Rec 2005, 85:57-68.
14. Delrieu I., Yaro S., Tamekloe T.A., Njanpop-Lafourcade B.M., Tall H., Jaillard P., et al. Emergence of Epidemic Neisseria meningitidis Serogroup X Meningitis in Togo and Burkina Faso. PLoS ONE 2011, 6:e19513.
15. Boisier P., Nicolas P., Djibo S., Taha M.K., Jeanne I., Mainassara H.B., et al. Meningococcal meningitis: unprecedented incidence of serogroup X-related cases in 2006 in Niger. Clin Infect Dis 2007, 44:657-663.
16. Harrison O.B., Claus H., Jiang Y., Bennett J.S., Bratcher H.B., Jolley K.A., et al. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg Infect Dis 2013, (April). [03.04.2013, Internet].
17. Borel T., Rose A.M., Guillerm M., Sidikou F., Gerstl S., Djibo A., et al. High sensitivity and specificity of the Pastorex latex agglutination test for Neisseria meningitidis serogroup A during a clinical trial in Niger. Trans R Soc Trop Med Hyg 2006, 100:964-969.
18. Chanteau S., Rose A.M., Djibo S., Nato F., Boisier P. Biological diagnosis of meningococcal meningitis in the African meningitis belt: current epidemic strategy and new perspectives. Vaccine 2007, 25(Suppl. 1):A30-A36.
19. Bennett D.E., Mulhall R.M., Cafferkey M.T. PCR-based assay for detection of Neisseria meningitidis capsular serogroups 29E, X, and Z. J Clin Microbiol 2004, 42:1764-1765.
20. Mothershed E.A., Sacchi C.T., Whitney A.M., Barnett G.A., Ajello G.W., Schmink S., et al. Use of real-time PCR to resolve slide agglutination discrepancies in serogroup identification of Neisseria meningitidis. J Clin Microbiol 2004, 42:320-328.
21. Traore Y., Njanpop-Lafourcade B.M., Adjogble K.L., Lourd M., Yaro S., Nacro B., et al. The rise and fall of epidemic Neisseria meningitidis serogroup W135 meningitis in Burkina Faso, 2002-2005. Clin Infect Dis 2006, 43:817-822.
22. Rose A.M., Mueller J.E., Gerstl S., Njanpop-Lafourcade B.M., Page A.L., Nicolas P., et al. Meningitis dipstick rapid test: evaluating diagnostic performance during an urban Neisseria meningitidis serogroup A outbreak, Burkina Faso, 2007. PLoS ONE 2010, 5:e11086.
23. Rose A.M., Gerstl S., Mahamane A.E., Sidikou F., Djibo S., Bonte L., et al. Field evaluation of two rapid diagnostic tests for Neisseria meningitidis serogroup A during the 2006 outbreak in Niger. PLoS ONE 2009, 4:e7326.
24. Nicolas P., Norheim G., Garnotel E., Djibo S., Caugant D.A. 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.
25. Caugant D.A., Maiden M.C. Meningococcal carriage and disease-population biology and evolution. Vaccine 2009, 27(Suppl. 2):B64-B70.
26. Zhu P., van der Ende A., Falush D., Brieske N., Morelli G., Linz B., et al. Fit genotypes and escape variants of subgroup III Neisseria meningitidis during three pandemics of epidemic meningitis. Proc Natl Acad Sci USA 2001, 98:5234-5239.
27. Caugant D.A., Kristiansen P.A., Wang X., Mayer L.W., Taha M.K., Ouedraogo R., et al. Molecular characterization of invasive meningococcal isolates from countries in the African Meningitis Belt before Introduction of a serogroup A conjugate vaccine. PLoS ONE 2012, 7:e46019.
28. Leimkugel J., Hodgson A., Forgor A.A., Pfluger V., Dangy J.P., Smith T., 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.
29. WHO Inter Country Support Team - West Africa. Meningitis Weekly Bulletin. Week 48-52 2011. Ouagadougou, Burkina Faso; January 2012.
30. Novak R.T., Kambou J.L., Diomande F.V., Tarbangdo T.F., Ouedraogo-Traore R., Sangare L., et al. meningococcal conjugate vaccination in Burkina Faso: analysis of national surveillance data. Lancet Infect Dis 2012, 12:757-764.
31. Mueller J.E., Borrow R., Gessner B.D. Meningococcal serogroup W135 in the African meningitis belt: epidemiology, immunity and vaccines. Expert Rev Vaccines 2006, 5:319-336.
32. Greenwood B. Manson Lecture. Meningococcal meningitis in Africa. Trans R Soc Trop Med Hyg 1999, 93:341-353.
33. Whittle H., Evans-Jones G., Onyewotu I.I., Adjukiewicz A., Turunen U., Crockford J., et al. Group-C meningococcal meningitis in the northern savanna of Africa. Lancet 1975, 305:1377.
34. Broome C.V., Rugh M.A., Yada A.A., Giat L., Giat H., Zeltner J.M., et al. Epidemic group C meningococcal meningitis in Upper Volta, 1979. Bull World Health Organ 1983, 61:325-330.
35. Campagne G., Schuchat A., Djibo S., Ousseini A., Cisse L., Chippaux J.P. Epidemiology of bacterial meningitis in Niamey, Niger, 1981-96. Bull World Health Organ 1999, 77:499-508.
36. Savory E.C., Cuevas L.E., Yassin M.A., Hart C.A., Molesworth A.M., Thomson M.C. Evaluation of the meningitis epidemics risk model in Africa. Epidemiol Infect 2006, 134:1047-1051.
37. Slaterus K.W. Serological typing of meningococci by means of micro-precipitation. Antonie Van Leeuwenhoek 1961, 27:305-315.
38. Hollis D.G., Wiggins G.L., Schubert J.H. Serological studies of ungroupable Neisseria meningitidis. J Bacteriol 1968, 95:1-4.
39. WHO Inter Country Support Team - West Africa. Meningitis Weekly Bulletin. Week 48-52 2010. Ouagadougou, Burkina Faso; January 2011.
40. Tzeng Y.L., Noble C., Stephens D.S. Genetic basis for biosynthesis of the (alpha 1-->4)-linked N-acetyl-d-glucosamine 1-phosphate capsule of Neisseria meningitidis serogroup X. Infect Immun 2003, 71:6712-6720.
41. Parent dC I., Traore Y., Gessner B.D., Antignac A., Naccro B., Njanpop-Lafourcade B.M., et al. Bacterial meningitis in Burkina Faso: surveillance using field-based polymerase chain reaction testing. Clin Infect Dis 2005, 40:17-25.
42. Caugant D.A., Mocca L.F., Frasch C.E., Froholm L.O., Zollinger W.D., Selander R.K. Genetic structure of Neisseria meningitidis populations in relation to serogroup, serotype, and outer membrane protein pattern. J Bacteriol 1987, 169:2781-2792.
43. Pajon R., Fergus A.M., Koeberling O., Caugant D.A., Granoff D.M. Meningococcal factor H binding proteins in epidemic strains from Africa: implications for vaccine development. PLoS Negl Trop Dis 2011, 5:e1302.
44. Jolley KA, Maiden MC. PubMLST database. Neisseria sequence type home page; 2013. [accessed 13.03.13, Internet]. http://www.pubmlst.org/.
45. Riou J.Y., Djibo S., Sangare L., Lombart J.P., Fagot P., Chippaux J.P., et al. A predictable comeback: the second pandemic of infections caused by Neisseria meningitidis serogroup A subgroup III in Africa, 1995. Bull World Health Organ 1996, 74:181-187.
46. Orren A., Caugant D.A., Fijen C.A., Dankert J., van Schalkwyk E.J., Poolman J.T., et al. Characterization of strains of Neisseria meningitidis recovered from complement-sufficient and complement-deficient patients in the Western Cape Province, South Africa. J Clin Microbiol 1994, 32:2185-2191.
47. Coulson G.B., von G.A., du P.M., Smith A.M., de G.L., Klugman K.P. Meningococcal disease in South Africa, 1999-2002. Emerg Infect Dis 2007, 13:273-281.
48. von G.A., du P.M., Cohen C., Prentice E., Schrag S., de G.L., et al. Emergence of endemic serogroup W135 meningococcal disease associated with a high mortality rate in South Africa. Clin Infect Dis 2008, 46:377-386.
49. Mutonga D.M., Pimentel G., Muindi J., Nzioka C., Mutiso J., Klena J.D., et al. Epidemiology and risk factors for serogroup X meningococcal meningitis during an outbreak in western Kenya, 2005-2006. Am J Trop Med Hyg 2009, 80:619-624.
50. Boisier P., Djibo S., Sidikou F., Mindadou H., Kairo K.K., Djibo A., et al. Epidemiological patterns of meningococcal meningitis in Niger in 2003 and 2004: under the threat of N. meningitidis serogroup W135. Trop Med Int Health 2005, 10:435-443.
51. Lewis R. Meningococcal meningitis serogroup X: a new player in Ugandan epidemiology 2006, WHO Health Action in Crisis, p. 6.
52. Etienne J., Sperber G., Adamou A., Picq J.J. Epidemiological notes: meningococcal meningitis of serogroup X in Niamey (Niger). Med Trop (Mars) 1990, 50:227-229.
53. Djibo S., Nicolas P., Alonso J.M., Djibo A., Couret D., Riou J.Y., et al. Outbreaks of serogroup X meningococcal meningitis in Niger 1995-2000. Trop Med Int Health 2003, 8:1118-1123.
54. Materu S., Cox H.S., Isaakidis P., Baruani B., Ogaro T., Caugant D.A. Serogroup X in meningococcal disease, Western Kenya. Emerg Infect Dis 2007, 13:944-945.
55. WHO Inter Country Support Team - West Africa. Meningitis Weekly Bulletin. Week 26 2012. Ouagadougou, Burkina Faso; July 2012.
56. Trotter C.L., Ramsay M.E., Gray S., Fox A., Kaczmarski E. No evidence for capsule replacement following mass immunisation with meningococcal serogroup C conjugate vaccines in England and Wales. Lancet Infect Dis 2006, 6:616-617.
57. Alonso J.M., Gilmet G., Rouzic E.M., Nassif X., Plotkin S.A., Ramsay M., et al. Workshop on vaccine pressure and Neisseria meningitidis, Annecy, France, 9-11 March 2005. Vaccine 2007, 25:4125-4129.
58. Hansman D. Meningococcal disease in South Australia: incidence and serogroup distribution 1971-1980. J Hyg (Lond) 1983, 90:49-54.
59. Yang J., Zhang X., Xu X., Xu L., Li M., Yang L., et al. Genotypic analysis of serogroups other than A, B or C of Neisseria meningitidis in China. Scand J Infect Dis 2007, 39:819-821.
60. Chen C., Zhang T.G., He J.G., Wu J., Chen L.J., Liu J.F., et al. A first meningococcal meningitis case caused by serogroup X Neisseria meningitidis strains in China. Chin Med J (Engl) 2008, 121:664-666.
61. Kim S.A., Kim D.W., Dong B.Q., Kim J.S., Anh D.D., Kilgore P.E. An expanded age range for meningococcal meningitis: molecular diagnostic evidence from population-based surveillance in Asia. BMC Infect Dis 2012, 12:310.
62. EU-IBIS Network. Invasive Neisseria meningitidis in Europe 2006. London: HealthProtection Agency; 2006. [accessed 03.04.13, Internet]. http://www.euibis.org/.
63. Grahlow W.D., Ocklitz H.W., Mochmann H. Meningococcal infections in the German Democratic Republic 1971-1984. Infection 1986, 14:286-288.
64. Fazio C., Starnino S., Solda M.D., Sofia T., Neri A., Mastrantonio P., et al. Neisseria meningitidis serogroup X sequence type 2888, Italy. Emerg Infect Dis 2010, 16:359-360.
65. Gagneux S., Wirth T., Hodgson A., Ehrhard I., Morelli G., Kriz P., et al. Clonal groupings in serogroup X Neisseria meningitidis. Emerg Infect Dis 2002, 8:462-466.
66. del Castillo C.M., Vazquez J.A., Romero J., Pascual A. Infections by Neisseria meningitidis serogroup X in Spain. Clin Microbiol Infect 2003, 9:964-965.
67. Fijen C.A., Kuijper E.J., Tjia H.G., Daha M.R., Dankert J. Complement deficiency predisposes for meningitis due to nongroupable meningococci and Neisseria-related bacteria. Clin Infect Dis 1994, 18:780-784.
68. Kilic A., Bedir O., Basustaoglu A.C., Bratcher H.B., Jolley K.A., Mert G. Neisseria meningitidis serogroup X sequence type 767 in Turkey. J Clin Microbiol 2010, 48:4340-4341.
69. Pedro L.G., Boente R.F., Madureira D.J., Matos J.A., Rebelo C.M., Igreja R.P., et al. Diagnosis of meningococcal meningitis in Brazil by use of PCR. Scand J Infect Dis 2007, 39:28-32.
70. Ryan N.J., Hogan G.R. Severe meningococcal disease caused by serogroups X and Z. Am J Dis Child 1980, 134:1173.
71. Cohn A.C., MacNeil J.R., Harrison L.H., Hatcher C., Theodore J., Schmidt M., et al. Changes in Neisseria meningitidis disease epidemiology in the United States, 1998-2007: implications for prevention of meningococcal disease. Clin Infect Dis 2010, 50:184-191.
72. Gagneux S.P., Hodgson A., Smith T.A., Wirth T., Ehrhard I., Morelli G., et al. Prospective study of a serogroup X Neisseria meningitidis outbreak in northern Ghana. J Infect Dis 2002, 185:618-626.
73. Djibo S., Nicolas P., Campagne G., Chippaux J.P. Pharyngeal carriage of Neisseria meningitidis in a school of Niamey, Niger. Med Trop (Mars) 2004, 64:363-366.
74. Mueller J.E., Sangare L., Njanpop-Lafourcade B.M., Tarnagda Z., Traore Y., Yaro S., et al. Molecular characteristics and epidemiology of meningococcal carriage, Burkina Faso, 2003. Emerg Infect Dis 2007, 13:847-854.
75. Raghunathan P.L., Jones J.D., Tiendrebeogo S.R., Sanou I., Sangare L., Kouanda S., et al. Predictors of immunity after a major serogroup W-135 meningococcal disease epidemic, Burkina Faso, 2002. J Infect Dis 2006, 193:607-616.
76. Kristiansen P.A., Diomande F., Wei S.C., Ouedraogo R., Sangare L., Sanou I., 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.
77. Yazdankhah S.P., Caugant D.A. Neisseria meningitidis: an overview of the carriage state. J Med Microbiol 2004, 53:821-832.
78. Ibarz-Pavon A.B., MacLennan J., Andrews N.J., Gray S.J., Urwin R., Clarke S.C., et al. Changes in serogroup and genotype prevalence among carried meningococci in the United Kingdom during vaccine implementation. J Infect Dis 2011, 204:1046-1053.
79. Zhou H., Gao Y., Xu L., Li M., Li Q., Li Y., et al. Distribution of serogroups and sequence types in disease-associated and carrier strains of Neisseria meningitidis isolated in China between 2003 and 2008. Epidemiol Infect 2012, 140:1296-1303.
80. Hong E., Giuliani M.M., Deghmane A.E., Comanducci M., Brunelli B., Dull P., et al. Could the multicomponent meningococcal serogroup B vaccine (4CMenB) control Neisseria meningitidis capsular group X outbreaks in Africa?. Vaccine 2013, 31:1113-1116.
81. Beernink P.T., Caugant D.A., Welsch J.A., Koeberling O., Granoff D.M. Meningococcal factor H-binding protein variants expressed by epidemic capsular group A, W-135, and X strains from Africa. J Infect Dis 2009, 199:1360-1368.
82. Budroni S., Siena E., Dunning Hotopp J.C., Seib K.L., Serruto D., Nofroni C., et al. Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination. Proc Natl Acad Sci USA 2011, 108:4494-4499.
83. Apicella M.A., Robinson J.A. Physicochemical properties of Neisseria meningitidis group X polysaccharide antigen. Infect Immun 1972, 6:773-778.
84. Robinson J.A., Apicella M.A. Isolation and Characterization of Neisseria meningitidis Groups A, C, X, and Y Polysaccharide Antigens. Infect Immun 1970, 1:8-14.
85. Bundle D.R., Jennings H.J., Kenny C.P. An improved procedure for the isolation of meningococcal, polysaccharide antigens, and the structural determination of the antigen from serogroup X. Carbohydr Res 1973, 26:268-270.
86. Bundle D.R., Jennings H.J., Kenny C.P. Studies on the group-specific polysaccharide of Neisseria meningitidis serogroup X and an improved procedure for its isolation. J Biol Chem 1974, 249:4797-4801.
87. Bundle D.R., Smith I.C., Jennings H.J. Determination of the structure and conformation of bacterial polysaccharides by carbon 13 nuclear magnetic resonance. Studies on the group-specific antigens of Neisseria meningitidis serogroups A and X. J Biol Chem 1974, 249:2275-2281.
88. Xie O., Bolgiano B., Gao F., Lockyer K., Swann C., Jones C., et al. Characterization of size, structure and purity of serogroup X Neisseria meningitidis polysaccharide, and development of an assay for quantification of human antibodies. Vaccine 2012, 30:5812-5823.
89. Garrida R., Pyada A., Fernandeza A., Gonzaleza M., Ramirez U., Cardoso F., et al. Quantitative Proton Nuclear Magnetic Resonance evaluation and total assignment of the capsular polysaccharide Neisseria meningitidis serogroup X. J Pharm Biomed Anal 2012, 70:295-300.
90. Berti F., Romano M.R., Micoli F., Pinto V., Cappelletti E., Gavini M., et al. Relative stability of meningococcal serogroup A and X polysaccharides. Vaccine 2012, 30:6409-6415.
91. Torres-Sanchez M.I., Zaccaria C., Buzzi B., Miglio G., Lombardi G., Polito L., et al. Synthesis and biological evaluation of phosphono analogues of capsular polysaccharide fragments from Neisseria meningitidis A. Chemistry 2007, 13:6623-6635.
92. Vann WF. The Neisseria meningitidis serogroup X xcbA gene product catalyses synthesis of the bacterial capsular polysaccharide. 26th International Carbohydrate Symposium (ICS2012). 22.07.2012. Madrid, Spain. 2012, P250.
93. Gerardy-Schahn R, Mühlanhoff M, Bethe A, Stummeyer K, Freiberger F, Damerow S, inventors. Means and methods for producing artificial capsular polysaccharides of Neisseria meningitidis. U.S. patent application mumber US2013/0012471 A1. Issued 10.01.2013.
94. Morelli L., Lay L. Synthesis of Neisseria meningitidis X capsular polysaccharide. Arch Org Chem 2013, ii:166-184.
95. Borrow R., Longworth E., Gray S.J., Kaczmarski E.B. Prevalence of de-O-acetylated serogroup C meningococci before the introduction of meningococcal serogroup C conjugate vaccines in the United Kingdom. FEMS Immunol Med Microbiol 2000, 28:189-191.
96. Longworth E., Fernsten P., Mininni T.L., Vogel U., Claus H., Gray S., et al. O-Acetylation status of the capsular polysaccharides of serogroup Y and W135 meningococci isolated in the UK. FEMS Immunol Med Microbiol 2002, 32:119-123.
97. Bergfeld A.K., Claus H., Lorenzen N.K., Spielmann F., Vogel U., Muhlenhoff M. The polysialic acid-specific O-acetyltransferase OatC from Neisseria meningitidis serogroup C evolved apart from other bacterial sialate O-acetyltransferases. J Biol Chem 2009, 284:6-16.
98. Berry D.S., Lynn F., Lee C.H., Frasch C.E., Bash M.C. Effect of O acetylation of Neisseria meningitidis serogroup A capsular polysaccharide on development of functional immune responses. Infect Immun 2002, 70:3707-3713.
99. Michon F., Huang C.H., Farley E.K., Hronowski L., Di J., Fusco P.C. Structure activity studies on group C meningococcal polysaccharide-protein conjugate vaccines: effect of O-acetylation on the nature of the protective epitope. Dev Biol (Basel) 2000, 103:151-160.
100. Goldschneider I., Gotschlich E.C., Artenstein M.S. Human immunity to the meningococcus. II. Development of natural immunity. J Exp Med 1969, 129:1327-1348.
101. Glode M.P., Robbins J.B., Liu T.Y., Gotschlich E.C., Orskov I., Orskov F. Cross-antigenicity and immunogenicity between capsular polysaccharides of group C Neisseria meningitidis and of Escherichia coli K92. J Infect Dis 1977, 135:94-104.
102. Vann W.F., Liu T.Y., Robbins J.B. Bacillus pumilus polysaccharide cross-reactive with meningococcal group A polysaccharide. Infect Immun 1976, 13:1654-1662.
103. Jones G.R., Christodoulides M., Brooks J.L., Miller A.R., Cartwright K.A., Heckels J.E. Dynamics of carriage of Neisseria meningitidis in a group of military recruits: subtype stability and specificity of the immune response following colonization. J Infect Dis 1998, 178:451-459.
104. Gold R., Goldschneider I., Lepow M.L., Draper T.F., Randolph M. Carriage of Neisseria meningitidis and Neisseria lactamica in infants and children. J Infect Dis 1978, 137:112-121.
105. Frasch C.E., Borrow R., Donnelly J. Bactericidal antibody is the immunologic surrogate of protection against meningococcal disease. Vaccine 2009, 27(Suppl. 2):B112-B116.
106. Nikolaev A.V., Botvinko I.V., Ross A.J. Natural phosphoglycans containing glycosyl phosphate units: structural diversity and chemical synthesis. Carbohydr Res 2007, 342:297-344.
107. Archibald A.R., Stafford G.H. A polymer of N-acetylglucosamine 1-phosphate in the wall of Staphylococcus lactis 2102. Biochem J 1972, 130:681-690.
108. Gening M.L., Maira-Litran T., Kropec A., Skurnik D., Grout M., Tsvetkov Y.E., et al. Synthetic {beta}-(1→6)-linked N-acetylated and nonacetylated oligoglucosamines used to produce conjugate vaccines for bacterial pathogens. Infect Immun 2010, 78:764-772.
109. Chen D., Kapre S., Goel A., Suresh K., Beri S., Hickling J., et al. Thermostable formulations of a hepatitis B vaccine and a meningitis A polysaccharide conjugate vaccine produced by a spray drying method. Vaccine 2010, 28:5093-5099.
110. 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, 17:840-847.
111. Barbour M.L., Mayon-White R.T., Coles C., Crook D.W., Moxon E.R. The impact of conjugate vaccine on carriage of Haemophilus influenzae type b. J Infect Dis 1995, 171:93-98.
112. Simell B., Auranen K., Kayhty H., Goldblatt D., Dagan R., O'Brien K.L. The fundamental link between pneumococcal carriage and disease. Expert Rev Vaccines 2012, 11:841-855.
113. Romano MR, Micoli F, Balducci E, et al. Development of a serogroup X meningococcal conjugate vaccine. XVIIIth International Pathogenic Neisseria Conference 09.09.2012. Würzburg, Germany.
114. Sadarangani M., Pollard A.J. Serogroup B meningococcal vaccines-an unfinished story. Lancet Infect Dis 2010, 10:112-124.
115. Norheim G, Tunheim G, Naess LM, et al. A trivalent outer membrane vesicle (OMV) vaccine against serogroup A, W-135 and X meningococcal disease. XVIIIth International Pathogenic Neisseria Conference 09.09.2012. Würzburg, Germany.
116. Keiser P.B., Biggs-Cicatelli S., Moran E.E., Schmiel D.H., Pinto V.B., Burden R.E., et al. A phase 1 study of a meningococcal native outer membrane vesicle vaccine made from a group B strain with deleted lpxL1 and synX, over-expressed factor H binding protein, two PorAs and stabilized OpcA expression. Vaccine 2011, 29:1413-1420.
117. Zollinger W.D., Babcock J.G., Moran E.E., Brandt B.L., Matyas G.R., Wassef N.M., et al. Phase I study of a Neisseria meningitidis liposomal vaccine containing purified outer membrane proteins and detoxified lipooligosaccharide. Vaccine 2012, 30:712-721.
118. Moran E.E., Burden R., Labrie J.E., Wen Z., Wang X.M., Zollinger W.D., et al. Analysis of the bactericidal response to an experimental Neisseria meningitidis vesicle vaccine. Clin Vaccine Immunol 2012, 19:659-665.
119. Nokleby H., Aavitsland P., O'Hallahan J., Feiring B., Tilman S., Oster P. Safety review: two outer membrane vesicle (OMV) vaccines against systemic Neisseria meningitidis serogroup B disease. Vaccine 2007, 25:3080-3084.
120. Woods C.W., Armstrong G., Sackey S.O., Tetteh C., Bugri S., Perkins B.A., et al. Emergency vaccination against epidemic meningitis in Ghana: implications for the control of meningococcal disease in West Africa. Lancet 2000, 355:30-33.
121. World Health Organization and Centers for Disease Control and Prevention. Technical Guidelines for Integrated Disease Surveillance and Response in the African Region, Brazzaville, Republic of Congo and Atlanta, USA; 2010. p. 1-398.
122. World Health Organization. Managing meningitis epidemics in Africa. A quick reference guide for health authorities and health-care workers, second edition. Geneva, Switzerland: WHO/HSE/GAR/ERI/2010.4; November 2010.
123. Hedberg S.T., Fredlund H., Nicolas P., Caugant D.A., Olcen P., Unemo M. Antibiotic susceptibility and characteristics of Neisseria meningitidis isolates from the African meningitis belt, 2000 to 2006: phenotypic and genotypic perspectives. Antimicrob Agents Chemother 2009, 53:1561-1566.