Differences among group A streptococcus epidemiological landscapes: Consequences for M protein-based vaccines?

Expert Review of Vaccines

Volumn 8, Issue 12, 2009, Pages 1705-1720

  Smeesters, Pierre R ^a,b,c   McMillan, David J ^a,d   Sriprakash, Kadaba S ^a,d   Georgousakis, Melina M ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c HOP UNIV DES ENFANTS REINE FABIOLA   (Belgium)

^d Griffith Medical Research College   (Australia)

Author keywords

Group A streptococcus; M protein; M protein vaccine; Streptococcus pyogenes

Indexed keywords

BACTERIAL PROTEIN; EPITOPE; M PROTEIN; STREPTOCOCCUS VACCINE;

AMINO TERMINAL SEQUENCE; AUTOIMMUNE DISEASE; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CROSS REACTION; DRUG DESIGN; HUMAN; HUMORAL IMMUNITY; IMPETIGO; MOLECULAR EPIDEMIOLOGY; MUCOSAL IMMUNITY; NONHUMAN; PHARYNGITIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; STREPTOCOCCUS DYSGALACTIAE EQUISIMILIS; STREPTOCOCCUS EQUI; STREPTOCOCCUS GROUP A; STREPTOCOCCUS INFECTION; STREPTOCOCCUS INIAE;

ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; CARRIER PROTEINS; DRUG DESIGN; GENETIC VARIATION; HUMANS; MOLECULAR EPIDEMIOLOGY; SEVERITY OF ILLNESS INDEX; STREPTOCOCCAL INFECTIONS; STREPTOCOCCAL VACCINES; STREPTOCOCCUS PYOGENES; TREATMENT OUTCOME; WORLD HEALTH;

EID: 73849143607     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.133     Document Type: Review

References (141)

1. Carapetis JR, Steer AC, Mulholland EK, Weber M. The global burden of group A streptococcal diseases. Lancet Infect. Dis. 5(11), 685-694 (2005). •• Excellent extensive review.
2. Pfoh E, Wessels MR, Goldmann D, Lee GM. Burden and economic cost of group A streptococcal pharyngitis. Pediatrics 121(2), 229-234 (2008).
3. Lamagni TL, Efstratiou A, Dennis J, Nair P, Kearney J, George R. Increase in invasive group A streptococcal infections in England, Wales and Northern Ireland, 2008-9. Euro Surveill. 14(5), pii, 19110 (2009).
4. Efstratiou A. Group A streptococci in the 1990s. J. Antimicrob. Chemother. 45(Suppl.), 3-12 (2000).
5. Aziz RK, Kotb M. Rise and persistence of global M1T1 clone of Streptococcus pyogenes. Emerg. Infect. Dis. 14(10), 1511-1517 (2008).
6. Cunningham MW. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13(3), 470-511 (2000).
7. Shulman ST, Stollerman G, Beall B, Dale JB, Tanz RR. Temporal changes in streptococcal M protein types and the near-disappearance of acute rheumatic fever in the United States. Clin. Infect. Dis. 42(4), 441-447 (2006).
8. Carapetis JR. Rheumatic heart disease in developing countries. N. Engl. J. Med. 357(5), 439-441 (2007).
9. Singh PI, Carapetis JR, Buadromo EM, Samberkar PN, Steer AC. The high burden of rheumatic heart disease found on autopsy in Fiji. Cardiol. Young 18(1), 62-69 (2008).
10. Stollerman GH. Rheumatic fever in the 21st Century. Clin. Infect. Dis. 33(6), 806-814 (2001).
11. Smeesters PR, Vergison A, Campos D, de Aguiar E, Deyi VY, Van Melderen L. Differences between Belgian and Brazilian group A streptococcus epidemiologic landscape. PLoS ONE 1, e10 (2006).
12. Bisno AL, Brito MO, Collins CM. Molecular basis of group A streptococcal virulence. Lancet Infect. Dis. 3(4), 191-200 (2003). •• Comprehensive review of group A streptococcus (GAS) virulence factors.
13. Timoney JF, Artiushin SC, Boschwitz JS. Comparison of the sequences and functions of Streptococcus equi M-like proteins SeM and SzPSe. Infect. Immun. 65(9), 3600-3605 (1997).
14. Locke JB, Aziz RK, Vicknair MR, Nizet V, Buchanan JT. Streptococcus iniae M-like protein contributes to virulence in fish and is a target for live attenuated vaccine development. PLoS ONE 3(7), e2824 (2008).
15. Podbielski A. Three different types of organization of the vir regulon in group A streptococci. Mol. Gen. Genet. 237(1-2), 287-300 (1993).
16. Gardiner D, Hartas J, Currie B, Mathews JD, Kemp DJ, Sriprakash KS. Vir typing: a long-PCR typing method for group A streptococci. PCR Methods Appl. 4(5), 288-293 (1995).
17. Sriprakash KS, Hartas J. Lateral genetic transfers between group A and G streptococci for M-like genes are ongoing. Microb. Pathog. 20(5), 275-285 (1996).
18. Panchaud A, Guy L, Collyn F et al. M-protein and other intrinsic virulence factors of Streptococcus pyogenes are encoded on an ancient pathogenicity island. BMC Genomics 10(1), 198 (2009).
19. Smeesters PR, Mardulyn P, Vergison A, Leplae R, Van Melderen L. Genetic diversity of group A streptococcus M protein: implications for typing and vaccine development. Vaccine 26(46), 5835-5842 (2008).
20. Whatmore AM, Kapur V, Musser JM, Sullivan DJ, Kehoe MA. Variation in emm-like gene sequences in the context of the population genetic structure of group A streptococci. Dev. Biol. Stand. 85, 159-162 (1995).
21. Phillips GN Jr, Flicker PF, Cohen C, Manjula BN, Fischetti VA. Streptococcal M protein: a-helical coiled-coil structure and arrangement on the cell surface. Proc. Natl Acad. Sci. USA 78(8), 4689-4693 (1981).
22. Lancefield RC. The antigenic complex of Streptococcus hemolyticus. I. Demonstration of a type-specific substance in extracts of Streptococcus hemolyticus. J. Exp. Med. 47, 9-10 (1928).
23. Lancefield RC. Current knowledge of type-specific M antigens of group A streptococci. J. Immunol. 89, 307-313 (1962).
24. Beall B, Facklam R, Thompson T. Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci. J. Clin. Microbiol. 34(4), 953-958 (1996).
25. Facklam RF, Martin DR, Lovgren M et al. Extension of the Lancefield classification for group A streptococci by addition of 22 new M protein gene sequence types from clinical isolates: emm103 to emm124. Clin. Infect. Dis. 34(1), 28-38 (2002).
26. Johnsson E, Berggard K, Kotarsky H et al. Role of the hypervariable region in streptococcal M proteins: binding of a human complement inhibitor. J. Immunol. 161(9), 4894-4901 (1998).
27. Retnoningrum DS, Cleary PP. M12 protein from Streptococcus pyogenes is a receptor for immunoglobulin G3 and human albumin. Infect. Immun. 62(6), 2387-2394 (1994).
28. Whitnack E, Beachey EH. Antiopsonic activity of fibrinogen bound to M protein on the surface of group A streptococci. J. Clin. Invest. 69(4), 1042-1045 (1982).
29. Whitnack E, Beachey EH. Biochemical and biological properties of the binding of human fibrinogen to M protein in group A streptococci. J. Bacteriol. 164(1), 350-358 (1985).
30. Akesson P, Schmidt KH, Cooney J, Bjorck L. M1 protein and protein H: IgGFc- and albumin-binding streptococcal surface proteins encoded by adjacent genes. Biochem. J. 300(Pt 3), 877-886 (1994).
31. Cortney HS, Hasty DL, Dale JB. Anti-phagocytic mechanisms of Streptococcus pyogenes: binding of fibrinogen to M-related protein. Mol. Microbiol. 59(3), 936-947 (2006).
32. Carlsson F, Sandin C, Lindahl G. Human fibrinogen bound to Streptococcus pyogenes M protein inhibits complement deposition via the classical pathway. Mol. Microbiol. 56(1), 28-39 (2005).
33. Ringdahl U, Svensson HG, Kotarsky H, Gustafsson M, Weineisen M, Sjobring U. A role for the fibrinogen-binding regions of streptococcal M proteins in phagocytosis resistance. Mol. Microbiol. 37(6), 1318-1326 (2000).
34. Sandin C, Carlsson F, Lindahl G. Binding of human plasma proteins to Streptococcus pyogenes M protein determines the location of opsonic and non-opsonic epitopes. Mol. Microbiol. 59(1), 20-30 (2006).
35. Pahlman LI, Olin AI, Darenberg J et al. Soluble M1 protein of Streptococcus pyogenes triggers potent T cell activation. Cell. Microbiol. 10(2), 404-414 (2008).
36. Kahn F, Morgelin M, Shannon O et al. Antibodies against a surface protein of Streptococcus pyogenes promote a pathological inflammatory response. PLoS Pathog. 4(9), e1000149 (2008).
37. Cortney HS, Hasty DL, Dale JB. Molecular mechanisms of adhesion, colonization, and invasion of group A streptococci. Ann. Med. 34(2), 77-87 (2002).
38. Osterlund A, Engstrand L. Intracellular penetration and survival of Streptococcus pyogenes in respiratory epithelial-cells in vitro. Acta Oto Laryngologica 115(5), 685-688 (1995).
39. LaPenta D, Rubens C, Chi E, Cleary PP. Group A streptococci efficiently invade human respiratory epithelial cells. Proc. Natl Acad. Sci. USA 91(25), 12115-12119 (1994).
40. Jadoun J, Burstein E, Hanski E, Sela S. Proteins M6 and F1 are required for efficient invasion of group A streptococci into cultured epithelial cells. Adv. Exp. Med. Biol. 418, 511-515 (1997).
41. Guilherme L, Kalil J, Cunningham M. Molecular mimicry in the autoimmune pathogenesis of rheumatic heart disease. Autoimmunity 39(1), 31-39 (2006).
42. Fae KC, Diefenbach da Silva D, Bilate AM et al. PDIA3, HSPA5 and vimentin, proteins identified by 2-DE in the valvular tissue, are the target antigens of peripheral and heart infiltrating T cells from chronic rheumatic heart disease patients. J. Autoimmun. 31(2), 136-141 (2008).
43. Gulizia JM, Cunningham M, McManus BM. Immunoreactivity of anti-streptococcal monoclonal antibodies to human heart valves. Evidence for multiple cross-reactive epitopes. Am. J. Pathol. 138, 285-301 (1991).
44. Manjula BN, Trus BL, Fischetti VA. Presence of two distinct regions in the coiled-coil structure of the streptococcal Pep M5 protein: relationship to mammalian coiled-coil proteins and implications to its biological properties. Proc. Natl Acad. Sci. USA 82(4), 1064-1068 (1985).
45. Cunningham MW. Pathogenesis of group A streptococcal infections and their sequelae. Adv. Exp. Med. Biol. 609, 29-42 (2008).
46. Massell BF, Honikman LH, Amezcua J. Rheumatic fever following streptococcal vaccination. Report of three cases. JAMA 207(6), 1115-1119 (1969).
47. Steer AC, Kado J, Jenney AW et al. Acute rheumatic fever and rheumatic heart disease in Fiji: prospective surveillance, 2005-2007. Med. J. Aust. 190(3), 133-135 (2009).
48. Bessen DE, Carapetis JR, Beall B et al. Contrasting molecular epidemiology of group A streptococci causing tropical and nontropical infections of the skin and throat. J. Infect. Dis. 182(4), 1109-1116 (2000). • Interesting comparison between throat and skin isolates from different locations.
49. McDonald M, Currie BJ, Carapetis JR. Acute rheumatic fever: a chink in the chain that links the heart to the throat? Lancet Infect. Dis. 4(4), 240-245 (2004). •• Original and argumented questioning on the exclusive role of throat infections in the pathogenesis of rheumatic fever.
50. McGregor KF, Bilek N, Bennett A et al. Group A streptococci from a remote community have novel multilocus genotypes but share emm types and housekeeping alleles with isolates from worldwide sorces. J. Infect. Dis. 189(4), 717-723 (2004).
51. Tewodros W, Kronvall G. M protein gene (emm type) analysis of group A b-hemolytic streptococci from Ethiopia reveals unique patterns. J. Clin. Microbiol. 43(9), 4369-4376 (2005).
52. Haidan A, Talay SR, Rohde M, Sriprakash KS, Currie BJ, Chhatwal GS. Pharyngeal carriage of group C and group G streptococci and acute rheumatic fever in an Aboriginal population. Lancet 356(9236), 1167-1169 (2000).
53. Martin DR, Voss LM, Walker SJ, Lennon D. Acute rheumatic fever in Auckland, New Zealand: spectrum of associated group A streptococci different from expected. Pediatr. Infect. Dis. J. 13(4), 264-269 (1994).
54. Vlaminckx BJ, Schuren FH, Montijn RC et al. Determination of the relationship between group A streptococcal genome content, M type, and toxic shock syndrome by a mixed genome microarray. Infect. Immun. 75(5), 2603-2611 (2007).
55. O'Loughlin RE, Roberson A, Cieslak PR et al. The epidemiology of invasive group A streptococcal infection and potential vaccine implications: United States, 2000-2004. Clin. Infect. Dis. 45(7), 853-862 (2007). • Large epidemiological surveillance.
56. Pahlman LI, Olin AI, Darenberg J et al. Soluble M1 protein of Streptococcus pyogenes triggers potent T cell activation. Cell Microbiol. 10(2), 404-414 (2007).
57. Sumby P, Porcella SF, Madrigal AG et al. Evolutionary origin and emergence of a highly successful clone of serotype M1 group A streptococcus involved multiple horizontal gene transfer events. J. Infect. Dis. 192(5), 771-782 (2005).
58. Sitkiewicz I, Nagiec MJ, Sumby P, Butler SD, Cywes-Bentley C, Musser JM. Emergence of a bacterial clone with enhanced virulence by acquisition of a phage encoding a secreted phospholipase A2. Proc. Natl Acad. Sci. USA 103(43), 16009-16014 (2006).
59. Johnson DR, Wotton JT, Shet A, Kaplan EL. A comparison of group A streptococci from invasive and uncomplicated infections: are virulent clones responsible for serious streptococcal infections? J. Infect. Dis. 185(11), 1586-1595 (2002).
60. McMillan DJ, Beiko RG, Geffers R et al. Genes for the majority of group a streptococcal virulence factors and extracellular surface proteins do not confer an increased propensity to cause invasive disease. Clin. Infect. Dis. 43(7), 884-891 (2006). • Interesting study showing that the presence of most virulence factors does not increase per se the observed clinical virulence.
61. Rogers S, Commons R, Danchin MH et al. Strain prevalence, rather than innate virulence potential, is the major factor responsible for an increase in serious group A streptococcus infections. J. Infect. Dis. 195(11), 1625-1633 (2007).
62. Lamagni TL, Darenberg J, Luca-Harari B et al. Epidemiology of severe Streptococcus pyogenes disease in Europe. J. Clin. Microbiol. 46(7), 2359-2367 (2008). • Complete overview of the European epidemiology.
63. Steer AC, Magor G, Jenney AW et al. emm and C-repeat region molecular typing of b-hemolytic streptococci in a tropical country: implications for vaccine development. J. Clin. Microbiol. 47(8), 2502-2509 (2009). •• Large epidemiological study in a country with a high number of circulating emm-types.
64. Shulman ST, Tanz RR, Dale JB et al. Seven-year surveillance of North American pediatric group a streptococcal pharyngitis isolates. Clin. Infect. Dis. 49(1), 78-84 (2009). •• Recent and complete overview of North American pharyngitis epidemiology.
65. Fischetti VA, Hodges WM, Hruby DE. Protection against streptococcal pharyngeal colonization with a vaccinia: M protein recombinant. Science 244(4911), 1487-1490 (1989).
66. Lancefield RC, Perlmann GE. Preparation and properties of type-specific M antigen isolated from a group A, type 1 hemolytic streptococcus. J. Exp. Med. 96(1), 71-82 (1952).
67. Dochez AR, Avery OT, Lancefield RC. Studies on the biology of streptococcus. I. Antigenic relationships between strains of Streptococcus haemolyticus. J. Exp. Med. 30(3), 179-213 (1919).
68. D'Alessandri R, Plotkin G, Kluge RM et al. Protective studies with group A streptococcal M protein vaccine. III. Challenge of volunteers after systemic or intranasal immunization with type 3 or type 12 group A streptococcus. J. Infect. Dis. 138(6), 712-718 (1978).
69. Fox EN, Waldman RH, Wittner MK, Mauceri AA, Dorfman A. Protective study with a group-A streptococcal-M protein vaccine - infectivity challenge of human volunteers. J. Clin. Invest. 52(8), 1885-1892 (1973).
70. Watson RF, Rothbard S, Swift HF. Type-specific protection and immunity following intranasal inoculation of monkeys with group-A hemolytic streptococci. J. Exp. Med. 84(2), 127-142 (1946).
71. Facklam RR, Moody MD. Production of streptococcal M-typing antisera. I. Antigenic response in different breeds of rabbits. Appl. Microbiol. 16(12), 1822-1825 (1968).
72. O'Brien KL, Beall B, Barrett NL et al. Epidemiology of invasive group a streptococcus disease in the United States, 1995-1999. Clin. Infect. Dis. 35(3), 268-276 (2002).
73. Krisher K, Cunningham MW. Myosin - a link between streptococci and heart. Science 227(4685), 413-415 (1985).
74. Fenderson PG, Fischetti VA, Cunningham MW. Tropomyosin shares immunologic epitopes with group A streptococcal M proteins. J. Immunol. 142(7), 2475-2481 (1989).
75. Ellis NM, Li Y, Hildebrand W, Fischetti VA, Cunningham MW. T cell mimicry and epitope specificity of cross-reactive T cell clones from rheumatic heart disease. J. Immunol. 175(8), 5448-5456 (2005).
76. Ji Y, McLandsborough L, Kondagunta A, Cleary PP. C5a peptidase alters clearance and trafficking of group A streptococci by infected mice. Infect. Immun. 64(2), 503-510 (1996).
77. Guzman CA, Talay SR, Molinari G, Medina E, Chhatwal GS. Protective immune response against Streptococcus pyogenes in mice after intranasal vaccination with the fibronectin binding protein SfbI. J. Infect. Dis. 179(4), 901-906 (1999).
78. Kotloff KL, Corretti M, Palmer K et al. Safety and immunogenicity of a recombinant multivalent group a streptococcal vaccine in healthy adults: Phase 1 trial. JAMA 292(6), 709-715 (2004).
79. McNeil SA, Halperin SA, Langley JM et al. Safety and immunogenicity of 26-valent group a streptococcus vaccine in healthy adult volunteers. Clin. Infect. Dis. 41(8), 1114-1122 (2005). • Results of the 26-valent Phase I clinical trial.
80. Dale JB, Chiang EY, Lederer JW. Recombinant tetravalent group-A streptococcal M-protein vaccine. J. Immunol. 151(4), 2188-2194 (1993).
81. Dale JB. Multivalent group A streptococcal vaccine designed to optimize the immunogenicity of six tandem M protein fragments. Vaccine 17(2), 193-200 (1999).
82. Dale JB, Simmons M, Chiang EC, Chiang EY. Recombinant, octavalent group A streptococcal M protein vaccine. Vaccine 14(10), 944-948 (1996).
83. McMillan D. StreptAvax (ID Biomedical). Curr. Opin. Investig. Drugs 7(2), 186-190 (2006).
84. Hu MC, Walls MA, Stroop SD, Reddish MA, Beall B, Dale JB. Immunogenicity of a 26-valent group A streptococcal vaccine. Infect. Immun. 70(4), 2171-2177 (2002).
85. Dale JB, Penfound T, Chiang EY, Long V, Shulman ST, Beall B. Multivalent group A streptococcal vaccine elicits bactericidal antibodies against variant M subtypes. Clin. Diagn. Lab. Immunol. 12(7), 833-836 (2005).
86. Villasenor-Sierra A, McShan WM, Salmi D, Kaplan EL, Johnson DR, Stevens DL. Variable susceptibility to opsonophagocytosis of group A streptococcus M-1 strains by human immune sera. J. Infect. Dis. 180(6), 1921-1928 (1999).
87. Eriksson BK, Villasenor-Sierra A, Norgren M, Stevens DL. Opsonization of T1M1 group A streptococcus: dynamics of antibody production and strain specificity. Clin. Infect. Dis. 32(2), E24-E30 (2001).
88. Bisno AL. The concept of rheumatogenic and nonrheumatogenic group A streptococci. In: Streptococcal Disease and the Immune Response. Reed SE, Zabriskie JB (Eds). Academic Press, Inc., NY, USA, 789-803 (1980).
89. Schuchat A, Hilger T, Zell E et al. Active bacterial core surveillance of the emerging infections program network. Emerg. Infect. Dis. 7(1), 92-99 (2001).
90. Dey N, McMillan DJ, Yarwood PJ et al. High diversity of group A streptococcal emm types in an Indian community: the need to tailor multivalent vaccines. Clin. Infect. Dis. 40(1), 46-51 (2005). • Interesting paper illustrating the high number of circulating emm-types in India.
91. McDonald MI, Towers RJ, Andrews RM, Benger N, Currie BJ, Carapetis JR. Low rates of streptococcal pharyngitis and high rates of pyoderma in Australian aboriginal communities where acute rheumatic fever is hyperendemic. Clin. Infect. Dis. 43(6), 683-689 (2006).
92. Hartas J, Goodfellow AM, Currie BJ, Sriprakash KS. Characterisation of group A streptococcal isolates from tropical Australia with high prevalence of rheumatic fever: probing for signature sequences to identify members of the family of serotype 5. Microb. Pathog. 18(5), 345-354 (1995).
93. Wong SS, Lin YS, Mathew L, Rajagopal L, Sepkowitz D. Increase in group G Streptococcal infections in a community hospital, New York, USA. Emerg. Infect. Dis. 15(6), 991-993 (2009).
94. Zaoutis T, Attia M, Gross R, Klein J. The role of group C and group G streptococci in acute pharyngitis in children. Clin. Microbiol. Infect. 10(1), 37-40 (2004).
95. Davies MR, Tran TN, McMillan DJ, Gardiner DL, Currie BJ, Sriprakash KS. Inter-species genetic movement may blur the epidemiology of streptococcal diseases in endemic regions. Microbes Infect. 7(9-10), 1128-1138 (2005).
96. Alberti S, Garcia-Rey C, Garcia-Laorden MI, Dal-Re R, Garcia-de-Lomas J. Survey of emm-like gene sequences from pharyngeal isolates of group C and group G streptococci collected in Spain. J. Clin. Microbiol. 43(3), 1433-1436 (2005).
97. Ardanuy C, Tubau F, Pallares R et al. Epidemiology of invasive pneumococcal disease among adult patients in Barcelona before and after pediatric 7-valent pneumococcal conjugate vaccine introduction, 1997-2007. Clin. Infect. Dis. 48(1), 57-64 (2009).
98. Byington CL, Samore MH, Stoddard GJ et al. Temporal trends of invasive disease due to Streptococcus pneumoniae among children in the Intermountain West: emergence of nonvaccine serogroups. Clin. Infect. Dis. 41(1), 21-29 (2005).
99. Gonzalez BE, Hulten KG, Lamberth L, Kaplan SL, Mason EO; US Pediatric Multicenter Pneumococcal Surveillance Group. Streptococcus pneumonide serogroups 15 and 33 - an increasing cause of pneumococcal infections in children in the United States after the introduction of the pneumococcal 7-valent conjugate vaccine. Pediatr. Infect. Dis. J. 25(4), 301-305 (2006).
100. Dobay O, Amyes SGB, Nagy K. The effect of the 7-valent conjugate vaccine (PCV7) on the incidence of pneumococcal infections world-wide. Rev. Med. Microbiol. 19(3), 79-85 (2008).
101. Beall B, McEllistrem MC, Gertz RE et al. Pre- and postvaccination clonal compositions of invasive pneumococcal serotypes for isolates collected in the United States in 1999, 2001, and 2002. J. Clin. Microbiol. 44(3), 999-1017 (2006).
102. Dinleyici EC, Yargic ZA. Pneumococcal conjugated vaccines: impact of PCV-7 and new achievements in the postvaccine era. Expert Rev. Vaccines 7(9), 1367-1394 (2008).
103. Pruksakorn S, Currie B, Brandt E et al. Towards a vaccine for rheumatic fever: identification of a conserved target epitope on M protein of group A streptococci. Lancet 344(8923), 639-642 (1994).
104. Bolken TC, Franke CA, Jones KF et al. Analysis of factors affecting surface expression and immunogenicity of recombinant proteins expressed by Gram-positive commensal vectors. Infect. Immun. 70(5), 2487-2491 (2002).
105. Bessen D, Fischetti VA. Synthetic peptide vaccine against mucosal colonization by group A streptococci. I. Protection against a heterologous M serotype with shared C repeat region epitopes. J. Immunol. 145(4), 1251-1256 (1990).
106. Guilherme L, Fae KC, Higa F et al. Towards a vaccine against rheumatic fever. Clin. Dev. Immunol. 13(2-4), 125-132 (2006).
107. Brandt ER, Hayman WA, Currie B et al. Functional analysis of IgA antibodies specific for a conserved epitope within the M protein of group A streptococci from Australian Aboriginal endemic communities. Int. Immunol. 11(4), 569-576 (1999).
108. Pruksakorn S, Currie B, Brandt E et al. Identification of T cell autoepitopes that cross-react with the C-terminal segment of the M protein of group A streptococci. Int. Immunol. 6(8), 1235-1244 (1994).
109. Brandt ER, Hayman WA, Currie B et al. Opsonic human antibodies from an endemic population specific for a conserved epitope on the M protein of group A streptococci. Immunology 89(3), 331-337 (1996).
110. Bessen D, Fischetti VA. Influence of intranasal immunization with synthetic peptides corresponding to conserved epitopes of M protein on mucosal colonization by group A streptococci. Infect. Immun. 56(10), 2666-2672 (1988). • Pioneering studies eluding to the potential of peptides encompassing conserved M-protein epitopes as mucosally delivered vaccine antigens.
111. Pruksakorn S, Galbraith A, Houghten RA, Good MF. Conserved T and B cell epitopes on the M protein of group A streptococci. Induction of bactericidal antibodies. J. Immunol. 149(8), 2729-2735 (1992).
112. Hayman WA, Brandt ER, Relf WA, Cooper J, Saul A, Good MF. Mapping the minimal murine T cell and B cell epitopes within a peptide vaccine candidate from the conserved region of the M protein of group A streptococcus. Int. Immunol. 9(11), 1723-1733 (1997).
113. Relf WA, Cooper J, Brandt ER et al. Mapping a conserved conformational epitope from the M protein of group A streptococci. Peptide Res. 9(1), 12-20 (1996). • Describes identification of the minimal B-cell epitope within the conserved repeat region of the M protein and the strategies employed to maintain the conformation of this epitope to promote immunogenicity.
114. Batzloff M, Yan H, Davies M, Hartas J, Good M. Preclinical evaluation of a vaccine based on conserved region of M protein that prevents group A streptococcal infection. Indian J. Med. Res. 119(Suppl.), 104-107 (2004).
115. Pandey M, Batzloff MR, Good MF. Mechanism of protection induced by group A streptococcus vaccine candidate J8-DT: contribution of B and T-cells towards protection. PLoS ONE 4(4), e5147 (2009).
116. Batzloff MR, Yan H, Davies MR et al. Toward the development of an antidisease, transmission-blocking intranasal vaccine for group a streptococcus. J. Infect. Dis. 192(8), 1450-1455 (2005).
117. Nilson BH, Frick IM, Akesson P et al. Structure and stability of protein H and the M1 protein from Streptococcus pyogenes. Implications for other surface proteins of Gram-positive bacteria. Biochem. 34(41), 13688-13698 (1995).
118. Brandt ER, Sriprakash KS, Hobb RI et al. New multi-determinant strategy for a group A streptococcal vaccine designed for the Australian Aboriginal population. Nat. Med. 6(4), 455-459 (2000).
119. Saikaly PE, Stroot PG, Oerther DB. Use of 16S rRNA gene terminal restriction fragment analysis to assess the impact of solids retention time on the bacterial diversity of activated sludge. Appl. Environ. Microbiol. 71(10), 5814-5822 (2005).
120. Grundmann H, Hori S, Tanner G. Determining confidence intervals when measuring genetic diversity and the discriminatory abilities of typing methods for microorganisms. J. Clin. Microbiol. 39(11), 4190-4192 (2001).
121. Espinosa LE, Li Z, Gomez Barreto D et al. M protein gene type distribution among group A streptococcal clinical isolates recovered in Mexico City, Mexico, from 1991 to 2000, and Durango, Mexico, from 1998 to 1999: overlap with type distribution within the United States. J. Clin. Microbiol. 41(1), 373-378 (2003).
122. Abdissa A, Asrat D, Kronvall G et al. High diversity of group A streptococcal emm types among healthy schoolchildren in Ethiopia. Clin. Infect. Dis. 42(10), 1362-1367 (2006).
123. Luca-Harari B, Darenberg J, Neal S et al. Clinical and microbiological characteristics of severe Streptococcus pyogenes disease in Europe. J. Clin. Microbiol. 47(4), 1155-1165 (2009).
124. Eisner A, Leitner E, Feierl G, Kessler HH, Marth E. Prevalence of emm types and antibiotic resistance of group A streptococci in Austria. Diagn. Microbiol. Infect. Dis. 55(4), 347-350 (2006).
125. Rivera A, Rebollo M, Miro E et al. Superantigen gene profile, emm type and antibiotic resistance genes among group A streptococcal isolates from Barcelona, Spain. J. Med. Microbiol. 55(Pt 8), 1115-1123 (2006).
126. Meisal R, Hoiby EA, Aaberge IS, Caugant DA. Sequence type and emm type diversity in Streptococcus pyogenes isolates causing invasive disease in Norway between 1988 and 2003. J. Clin. Microbiol. 46(6), 2102-2105 (2008).
127. Kittang BR, Langeland N, Mylvaganam H. Distribution of emm types and subtypes among noninvasive group A, C and G streptococcal isolates in western Norway. APMIS 116(6), 457-464 (2008).
128. Mijac V, Ranin L, Markovic M, Heeg C, Reinert RR, Opavski N. Distribution of emm types among group A streptococcal isolates from Serbia. Clin. Microbiol. Infect. (2009) (Epub ahead of print).
129. Szczypa K, Sadowy E, Izdebski R, Strakova L, Hryniewicz W. Group A streptococci from invasive-disease episodes in Poland are remarkably divergent at the molecular level. J. Clin. Microbiol. 44(11), 3975-3979 (2006).
130. Nir-Paz R, Korenman Z, Ron M et al. Streptococcus pyogenes emm and T types within a decade, 1996-2005: implications for epidemiology and future vaccines. Epidemiol. Infect. 1-8 (2009) (Epub ahead of print). • Complete and interesting review of the epidemiological situation in Israel.
131. Sagar V, Bakshi DK, Nandi S, Ganguly NK, Kumar R, Chakraborti A. Molecular heterogeneity among north Indian isolates of group A streptococcus. Lett. Appl. Microbiol. 39(1), 84-88 (2004).
132. Sakota V, Fry AM, Lietman TM, Facklam RR, Li Z, Beall B. Genetically diverse group A streptococci from children in far-western Nepal share high genetic relatedness with isolates from other countries. J. Clin. Microbiol. 44(6), 2160-2166 (2006).
133. Jing HB, Ning BA, Hao HJ et al. Epidemiological analysis of group A streptococci recovered from patients in China. J. Med. Microbiol. 55(Pt 8), 1101-1107 (2006).
134. Ho PL, Johnson DR, Yue AW et al. Epidemiologic analysis of invasive and noninvasive group a streptococcal isolates in Hong Kong. J. Clin. Microbiol. 41(3), 937-942 (2003).
135. Zheng MH, Jiao ZQ, Zhang LJ et al. Genetic analysis of group A streptococcus isolates recovered during acute glomerulonephritis outbreaks in Guizhou Province of China. J. Clin. Microbiol. 47(3), 715-720 (2009).
136. Kim S, Yong Lee N. Antibiotic resistance and genotypic characteristics of group a streptococci associated with acute pharyngitis in Korea. Microb. Drug Resist. 10(4), 300-305 (2004).
137. Koh EH, Kim S. Distribution of T types and emm genotypes of Streptococcus pyogenes in Jinju, 2004. Korean J. Lab. Med. 26(4), 269-274 (2006).
138. Ikebe T, Hirasawa K, Suzuki R et al. Distribution of emm genotypes among group A streptococcus isolates from patients with severe invasive streptococcal infections in Japan, 2001-2005. Epidemiol. Infect. 135(7), 1227-1229 (2007).
139. Wajima T, Murayama SY, Sunaoshi K, Nakayama E, Sunakawa K, Ubukata K. Distribution of emm type and antibiotic susceptibility of group A streptococci causing invasive and noninvasive disease. J. Med. Microbiol. 57(Pt 11), 1383-1388 (2008).
140. McDonald MI, Towers RJ, Fagan P, Carapetis JR, Currie BJ. Molecular typing of Streptococcus pyogenes from remote Aboriginal communities where rheumatic fever is common and pyoderma is the predominant streptococcal infection. Epidemiol. Infect. 135(8), 1398-1405 (2007).
141. Valery PC, Wenitong M, Clements V et al. Skin infections among Indigenous Australians in an urban setting in far north Queensland. Epidemiol. Infect. 136(8), 1103-1108 (2008).