The genetic structure of Neisseria meningitidis populations in Cuba before and after the introduction of a serogroup BC vaccine

Infection, Genetics and Evolution

Volumn 10, Issue 4, 2010, Pages 546-554

  Climent, Yanet ^a   Urwin, Rachel ^b,d   Yero, Daniel ^a   Martinez, Isabel ^a   Martín, Alejandro ^c   Sotolongo, Franklin ^a   Maiden, Martin C J ^b   Pajón, Rolando ^c,e  

^a FINLAY INSTITUTE   (Cuba)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c CENTER FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Cuba)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

Healthy carrier; Meningococcal disease; Molecular epidemiology; Multilocus sequence typing; Population structure

Indexed keywords

BACTERIAL PROTEIN; MENINGOCOCCUS VACCINE; PORIN A; PROTEIN FETA; PROTEIN PORB; UNCLASSIFIED DRUG;

ALLELE; ANALYTIC METHOD; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; CONTROLLED STUDY; CUBA; GENE FREQUENCY; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; MULTILOCUS SEQUENCE TYPING; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN VARIANT; SEQUENCE ANALYSIS; VACCINATION;

ANTIGENIC VARIATION; CARRIER STATE; CHI-SQUARE DISTRIBUTION; CUBA; DNA, BACTERIAL; GENES, BACTERIAL; GENOTYPE; HUMANS; MENINGOCOCCAL INFECTIONS; MENINGOCOCCAL VACCINES; MOLECULAR EPIDEMIOLOGY; NEISSERIA MENINGITIDIS; NUCLEIC ACID AMPLIFICATION TECHNIQUES; SEQUENCE ANALYSIS, DNA;

NEISSERIA MENINGITIDIS;

EID: 77951974753     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2010.02.002     Document Type: Article

References (58)

1. Abdillahi H., Poolman J.T. Typing of group-B Neisseria meningitidis with monoclonal antibodies in the whole-cell ELISA. J. Med. Microbiol. 1988, 26:177-180.
2. Baethgen L.F., Weidlich L., Moraes C., Klein C., Nunes L.S., Cafrune P.I., Lemos A.P., Rios S.S., Abreu M.F., Kmetzsch C., Sperb A.F., Riley L.W., Rossetti M.L., Zaha A. 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, 13:31-40.
3. Bjune G., Hoiby E.A., Gronnesby J.K., Arnesen O., Fredriksen J.H., Halstensen A., Holten E., Lindbak A.K., Nokleby H., Rosenqvist E. Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet 1991, 338:1093-1096.
4. Black J.R., Dyer D.W., Thompson M.K., Sparling P.F. Human immune response to iron-repressible outer membrane proteins of Neisseria meningitidis. Infect. Immun. 1986, 54:710-713.
5. Boslego J., Garcia J., Cruz C., Zollinger W., Brandt B., Ruiz S., Martinez M., Arthur J., Underwood P., Silva W. 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, 13:821-829.
6. Buckee C.O., Jolley K.A., Recker M., Penman B., Kriz P., Gupta S., Maiden M.C. Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:15082-15087.
7. Cartwright K., Morris R., Rumke H., Fox A., Borrow R., Begg N., Richmond P., Poolman J. Immunogenicity and reactogenicity in UK infants of a novel meningococcal vesicle vaccine containing multiple class 1 (PorA) outer membrane proteins. Vaccine 1999, 17:2612-2619.
8. Caugant D.A. Population genetics and molecular epidemiology of Neisseria meningitidis. APMIS 1998, 106:505-525.
9. Caugant D.A. Genetics and evolution of Neisseria meningitidis: importance for the epidemiology of meningococcal disease. Infect. Genet. Evol. 2008, 8:558-565.
10. 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.
11. Caugant D.A., Tzanakaki G., Kriz P. Lessons from meningococcal carriage studies. FEMS Microbiol. Rev. 2007, 31:52-63.
12. Chiou C.S., Liao J.C., Liao T.L., Li C.C., Chou C.Y., Chang H.L., Yao S.M., Lee Y.S. Molecular epidemiology and emergence of worldwide epidemic clones of Neisseria meningitidis in Taiwan. BMC Infect. Dis. 2006, 6:25.
13. Clarke S.C., Diggle M.A., Edwards G.F. Semiautomation of multilocus sequence typing for the characterization of clinical isolates of Neisseria meningitidis. J. Clin. Microbiol. 2001, 39:3066-3071.
14. de Filippis I., Vicente A.C. Multilocus sequence typing and repetitive element-based polymerase chain reaction analysis of Neisseria meningitidis isolates in Brazil reveal the emergence of 11 new sequence types genetically related to the ST-32 and ST-41/44 complexes and high prevalence of strains related to hypervirulent lineages. Diagn. Microbiol. Infect. Dis. 2005, 53:161-167.
15. de Moraes J.C., Perkins B.A., Camargo M.C., Hidalgo N.T., Barbosa H.A., Sacchi C.T., Landgraf I.M., Gattas V.L., Vasconcelos H.G. Protective efficacy of a serogroup B meningococcal vaccine in Sao Paulo. Brazil. Lancet 1992, 340:1074-1078.
16. Elias J., Claus H., Frosch M., Vogel U. Evidence for indirect nosocomial transmission of Neisseria meningitidis resulting in two cases of invasive meningococcal disease. J. Clin. Microbiol. 2006, 44:4276-4278.
17. Feavers I.M., Gray S.J., Urwin R., Russell J.E., Bygraves J.A., Kaczmarski E.B., Maiden M.C. Multilocus sequence typing and antigen gene sequencing in the investigation of a meningococcal disease outbreak. J. Clin. Microbiol. 1999, 37:3883-3887.
18. Feil E.J., Li B.C., Aanensen D.M., Hanage W.P., Spratt B.G. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 2004, 186:1518-1530.
19. Frasch C.E., Zollinger W.D., Poolman J.T. Serotype antigens of Neisseria meningitidis and a proposed scheme for designation of serotypes. Rev. Infect. Dis. 1985, 7:504-510.
20. Fraser C., Hanage W.P., Spratt B.G. Neutral microepidemic evolution of bacterial pathogens. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:1968-1973.
21. Gil J., Betancourt L.H., Sardiñas G., Yero D., Niebla O., Delgado M., García D., Pajón R., Sánchez A., González L.J., Padrón G., Campa C., Sotolongo F., Barberá R., Guillén G., Herrera L., Besada V. Proteomic study via a non-gel based approach of meningococcal outer membrane vesicle vaccine obtained from strain CU385: a road map for discovery new antigens. Hum. Vaccine 2009, 5:347-356.
22. Girard M.P., Preziosi M.P., Aguado M.T., Kieny M.P. A review of vaccine research and development: meningococcal disease. Vaccine 2006, 24:4692-4700.
23. Gupta S., Maiden M.C. Exploring the evolution of diversity in pathogen populations. Trends Microbiol. 2001, 9:181-185.
24. Harrison L.H., Jolley K.A., Shutt K.A., Marsh J.W., O'Leary M., Sanza L.T., Maiden M.C. Antigenic shift and increased incidence of meningococcal disease. J. Infect. Dis. 2006, 193:1266-1274.
25. Jacobsson S., Olcen P., Lofdahl M., Fredlund H., Molling P. Characteristics of Neisseria meningitidis isolates causing fatal disease. Scand. J. Infect. Dis. 2008, 40:734-744.
26. Jolley K.A., Brehony C., Maiden M.C. Molecular typing of meningococci: recommendations for target choice and nomenclature. FEMS Microbiol. Rev. 2007, 31:89-96.
27. Jolley K.A., Wilson D.J., Kriz P., McVean G., Maiden M.C. The influence of mutation, recombination, population history, and selection on patterns of genetic diversity in Neisseria meningitidis. Mol. Biol. Evol. 2005, 22:562-569.
28. Lancellotti M., Guiyoule A., Ruckly C., Hong E., Alonso J.M., Taha M.K. Conserved virulence of C to B capsule switched Neisseria meningitidis clinical isolates belonging to ET-37/ST-11 clonal complex. Microbes. Infect. 2006, 8:191-196.
29. Law D.K., Henderson A.M., Tsang R.S. DNA Sequence analysis of the PorB protein of nonserotypeable serogroup C ET-15 meningococci suggests a potential mutational hot spot on their serotype antigens. J. Clin. Microbiol. 2004, 42:2718-2723.
30. Maiden M.C., Bygraves J.A., Feil E., Morelli G., Russell J.E., Urwin R., Zhang Q., Zhou J., Zurth K., Caugant D.A., Feavers I.M., Achtman M., Spratt B.G. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3140-3145.
31. Martin S.L., Borrow R., van der L.P., Dawson M., Fox A.J., Cartwright K.A. Effect of sequence variation in meningococcal PorA outer membrane protein on the effectiveness of a hexavalent PorA outer membrane vesicle vaccine. Vaccine 2000, 18:2476-2481.
32. Milagres L.G., Gorla M.C., Sacchi C.T., Rodrigues M.M. Specificity of bactericidal antibody response to serogroup B meningococcal strains in Brazilian children after immunization with an outer membrane vaccine. Infect. Immun. 1998, 66:4755-4761.
33. MINSAP, 2008. [Incidence and mortality of meningococcal disease 1980-2008]. Anuario Estadístico de Salud de Cuba. (Online). http://www.sld.cu/servicios/estadisticas/.
34. Morley S.L., Cole M.J., Ison C.A., Camaraza M.A., Sotolongo F., Anwar N., Cuevas I., Carbonero M., Campa H.C., Sierra G., Levin M. Immunogenicity of a serogroup B meningococcal vaccine against multiple Neisseria meningitidis strains in infants. Pediatr. Infect. Dis. J. 2001, 20:1054-1061.
35. Noronha C.P., Struchiner C.J., Halloran M.E. Assessment of the direct effectiveness of BC meningococcal vaccine in Rio de Janeiro. Brazil: a case-control study. Int. J. Epidemiol. 1995, 24:1050-1057.
36. Oster P., Lennon D., O'Hallahan J., Mulholland K., Reid S., Martin D. MeNZB: a safe and highly immunogenic tailor-made vaccine against the New Zealand Neisseria meningitidis serogroup B disease epidemic strain. Vaccine 2005, 23:2191-2196.
37. Pace D., Cuschieri P., Galea D.A., ttard-Montalto S. Epidemiology of pathogenic Neisseria meningitidis serogroup B serosubtypes in Malta: implications for introducing PorA based vaccines. Vaccine 2008, 26:5952-5956.
38. Pettersson A., Kuipers B., Pelzer M., Verhagen E., Tiesjema R.H., Tommassen J., Poolman J.T. Monoclonal antibodies against the 70-kilodalton iron-regulated protein of Neisseria meningitidis are bactericidal and strain specific. Infect. Immun. 1990, 58:3036-3041.
39. Ramsay M.E., Andrews N.J., Trotter C.L., Kaczmarski E.B., Miller E. Herd immunity from meningococcal serogroup C conjugate vaccination in England: database analysis. BMJ 2003, 326:365-366.
40. Rodríguez A.P., Dickinson F., Baly A., Martínez R. The epidemiological impact of antimeningococcal B vaccination in Cuba. Mem. Inst. Oswaldo Cruz 1999, 94:433-440.
41. Russell J.E., Jolley K.A., Feavers I.M., Maiden M.C., Suker J. PorA variable regions of Neisseria meningitidis. Emerg. Infect. Dis. 2004, 10:674-678.
42. Russell J.E., Urwin R., Gray S.J., Fox A.J., Feavers I.M., Maiden M.C. Molecular epidemiology of meningococcal disease in England and Wales 1975-1995, before the introduction of serogroup C conjugate vaccines. Microbiology 2008, 154:1170-1177.
43. Saukkonen K., Leinonen M., Abdillahi H., Poolman J.T. Comparative evaluation of potential components for group B meningococcal vaccine by passive protection in the infant rat and in vitro bactericidal assay. Vaccine 1989, 7:325-328.
44. Sierra G.V., Campa H.C., Varcacel N.M., García I.L., Izquierdo P.L., Sotolongo P.F., Casanueva G.V., Rico C.O., Rodríguez C.R., Terry M.H. Vaccine against group B Neisseria meningitidis: protection trial and mass vaccination results in Cuba. NIPH Ann. 1991, 14:195-207.
45. Sotolongo F., Campa C., Casanueva G.V., Fajardo E.M., Cuevas I., González N. Cuban meningococcal BC vaccine: experiences & contributions from 20 years of application. MEDICC Rev. 2007, 9:16-22.
46. Suker J., Feavers I.M., Achtman M., Morelli G., Wang J.F., Maiden M.C. The porA gene in serogroup A meningococci: evolutionary stability and mechanism of genetic variation. Mol. Microbiol. 1994, 12:253-265.
47. Thompson E.A., Feavers I.M., Maiden M.C. Antigenic diversity of meningococcal enterobactin receptor FetA, a vaccine component. Microbiology 2003, 149:1849-1858.
48. ® vaccine against serogroup B of Neisseria meningitidis: Analysis of protein components by two-dimensional gel electrophoresis and mass spectrometry. Proteomics 2006, 6:3389-3399.
49. Urwin R., Feavers I.M., Jones D.M., Maiden M.C., Fox A.J. Molecular variation of meningococcal serotype 4 antigen genes. Epidemiol. Infect. 1998, 121:95-101.
50. Urwin R., Russell J.E., Thompson E.A., Holmes E.C., Feavers I.M., Maiden M.C. Distribution of surface protein variants among hyperinvasive meningococci: implications for vaccine design. Infect. Immun. 2004, 72:5955-5962.
51. van der Ley P., Heckels J.E., Virji M., Hoogerhout P., Poolman J.T. Topology of outer membrane porins in pathogenic Neisseria spp. Infect. Immun. 1991, 59:2963-2971.
52. Vicente D., Esnal O., Michaus L., Lopez de Goicoechea M.J., Cisterna R., Perez-Trallero E. Prevalence of genosubtypes (PorA types) of serogroup B invasive meningococcus in the north of Spain from 2000 to 2005. J. Med. Microbiol. 2005, 54:381-384.
53. Vipond C., Wheeler J.X., Jones C., Feavers I.M., Suker J. Characterization of the protein content of a meningococcal outer membrane vesicle vaccine by polyacrylamide gel electrophoresis and mass spectrometry. Hum. Vaccine 2005, 1:80-84.
54. Vogel U., Claus H., Frosch M., Caugant D.A. Molecular basis for distinction of the ET-15 clone within the ET-37 complex of Neisseria meningitidis. J. Clin. Microbiol. 2000, 38:941-942.
55. Wang J.F., Caugant D.A., Morelli G., Koumare B., Achtman M. Antigenic and epidemiologic properties of the ET-37 complex of Neisseria meningitidis. J. Infect. Dis. 1993, 167:1320-1329.
56. Wedege E., Hoiby E.A., Rosenqvist E., Bjune G. Immune responses against major outer membrane antigens of Neisseria meningitidis in vaccinees and controls who contracted meningococcal disease during the Norwegian serogroup B protection trial. Infect. Immun. 1998, 66:3223-3231.
57. Yang L., Zhang X., Peng J., Zhu Y., Dong J., Xu J., Jin Q. Distribution of surface-protein variants of hyperinvasive meningococci in China. J. Infect. 2009, 58:358-367.
58. Yazdankhah S.P., Kriz P., Tzanakaki G., Kremastinou J., Kalmusova J., Musilek M., Alvestad T., Jolley K.A., Wilson D.J., McCarthy N.D., Caugant D.A., Maiden M.C. 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, 42:5146-5153.