The success and failure of BCG - Implications for a novel tuberculosis vaccine

Nature Reviews Microbiology

Volumn 3, Issue 8, 2005, Pages 656-662

  Andersen, Peter ^a   Doherty, T Mark ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; LIPOSOME; LIVE VACCINE; RECOMBINANT VACCINE;

BACTERIAL IMMUNITY; BCG VACCINATION; CLINICAL TRIAL; DRUG CONTAMINATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG RESPONSE; DRUG SAFETY; DRUG TOLERABILITY; ENDEMIC DISEASE; ENVIRONMENTAL EXPOSURE; EPIDEMIC; HIGH RISK POPULATION; HUMAN; HYPOTHESIS; INCIDENCE; INFECTION PREVENTION; INFECTION RISK; MASS IMMUNIZATION; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SINGLE DRUG DOSE; TREATMENT FAILURE; TROPICS; TUBERCULOSIS;

ADOLESCENT; AGED; ANIMALS; ANTIBODIES, BACTERIAL; BCG VACCINE; CHILD; CHILD, PRESCHOOL; CLINICAL TRIALS; ENVIRONMENTAL EXPOSURE; HUMANS; IMMUNIZATION, SECONDARY; INFANT; INFANT, NEWBORN; MIDDLE AGED; MYCOBACTERIUM TUBERCULOSIS; TREATMENT FAILURE; TREATMENT OUTCOME; TUBERCULOSIS;

ANIMALIA; CORYNEBACTERINEAE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 22944433876     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1211     Document Type: Review

References (92)

1. Anon. Global Tuberculosis Control. WHO Report 2001. 181 (World Health Organization, Geneva, 2001).
2. Calmette, A. & Plotz, H. Protective inoculation against tuberculosis with BCG. Am. Rev. Tuberc. 19, 567-572 (1929).
3. Calmette, A. Au sujet des accidents de Lübeck chez des nourissons vaccines au BCG. Presse Med. 44, 748-749 (1930).
4. Evans, C. C. Historical background. in Clinical Tuberculosis (ed. Davies, P. D. O.) 1-19 (Chapman and Hall Medical, London, 1994).
5. Smith, P. G. BCG vaccination. in Clinical Tuberculosis (ed. Davies, P. D. O.) 297-310 (Chapman and Hall Medical, London, 1994).
6. Behr, M. A. Correlation between BCG genomics and protective efficacy. Scand. J. Infect. Dis. 33, 249-252 (2001).
7. Oettinger, T., Jorgensen, M., Ladefoged, A., Haslov, K. & Andersen, P. Development of the Mycobacterium bovis BCG vaccine: review of the historical and biochemical evidence for a genealogical tree. Tuber. Lung Dis. 79, 243-250 (1999).
8. Anon. Fifteen year follow up of trial of BCG vaccines in south India for tuberculosis prevention. Indian J. Med. Res. 110, 56-69 (1999).
9. Sterne, J. A., Rodrigues, L. C. & Guedes, I. N. Does the efficacy of BCG decline with time since vaccination? Int. J. Tuberc. Lung Dis. 2, 200-207 (1998).
10. Zodpey S. P., Shrikhande, S. N., Maldhure, B. R., Vasudeo, N. D. & Kulkarni, S. W. Effectiveness of Bacillus Calmette Guerin (BCG) vaccination in the prevention of childhood pulmonary tuberculosis: a case control study in Nagpur, India. Southeast Asian J. Trop. Med. Public Health 29, 285-288 (1998).
11. Lanckriet, C., Levy, B. D., Bingono, E., Siopathis, R. M. & Guerin, N. Efficacy of BCG vaccination of the newborn: evaluation by a follow-up study of contacts in Bangui. Int. J. Epidemiol. 24, 1042-1049 (1995).
12. Mittal, S. K., Aggarwal, V., Rastogi, A. & Saini, N. Does B.C.G. vaccination prevent or postpone the occurrence of tuberculous meningitis? Indian J. Pediatr. 63, 659-664 (1996).
13. Colditz, G. A. et al. The efficacy of bacillus Calmette-Guerin vaccination of newborns and infants in the prevention of tuberculosis: meta-analyses of the published literature. Pediatrics 96, 29-35 (1995).
14. Fine, P. E. Variation in protection by BCG: implications of and for heterologous immunity. Lancet 346, 1339-1345 (1995).
15. Kochi, A. Tuberculosis: distribution, risk factors, mortality. Immunobiology 191, 325-336 (1994).
16. Behr, M. A. & Small, P. M. Has BCG attenuated to impotence? Nature 389, 133-134 (1997).
17. Horwitz, M. A. & Harth, G. A new vaccine against tuberculosis affords greater survival after challenge than the current vaccine in the guinea pig model of pulmonary tuberculosis. Infect. Immun. 71, 1672-1679 (2003).
18. Pym, A. S. et al. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nature Med. 9, 533-539 (2003).
19. Conradt, P., Hess, J. & Kaufmann, S. H. Cytolytic T-cell responses to human dendritic cells and macrophages infected with Mycobacterium bovis BCG and recombinant BCG secreting listeriolysin. Microbes Infect. 1, 753-764 (1999).
20. Grode, L., Kursar, M., Fensterle, J., Kaufmann, S. H. & Hess, J. Cell-mediated immunity induced by recombinant Mycobacterium bovis Bacille Calmette-Guerin strains against an intracellular bacterial pathogen: importance of antigen secretion or membrane-targeted antigen display as lipoprotein for vaccine efficacy. J. Immunol. 168, 1869-1876 (2002).
21. Cole, S. T. et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544 (1998).
22. Wang, J. et al. Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis, J. Immunol. 173, 6357-6365 (2004).
23. McShane, H., Brookes, R., Gilbert, S. C. & Hill, A. V. Enhanced immunogenicity of CD4(+) T-cell responses and protective efficacy of a DNA-modified vaccinia virus Ankara prime-boost vaccination regimen for murine tuberculosis. Infect. Immun. 69, 681-686 (2001).
24. McShane, H. et al. Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nature Med. 10, 1240-1244 (2004).
25. Skeiky, Y. A. et al. Differential immune responses and protective efficacy induced by components of a tuberculosis polyprotein vaccine, Mtb72F, delivered as naked DNA or recombinant protein. J. Immunol. 172, 7618-7628 (2004).
26. Doherty, T. M. et al. Comparative analysis of different vaccine constructs expressing defined antigens from Mycobacterium tuberculosis. J. Infect. Dis. 190, 2146-2153 (2004).
27. Weinrich Olsen, A., van Pinxteren, L. A., Meng Okkels, L., Birk Rasmussen, P. & Andersen, P. Protection of mice with a tuberculosis subunit vaccine based on a fusion protein of antigen 85B and ESAT-6. Infect. Immun. 69, 2773-2778 (2001).
28. Langermans, J. A. et al. Protection of macaques against Mycobacterium tuberculosis infection by a subunit vaccine based on a fusion protein of antigen 85B and ESAT-6. Vaccine 23, 2740-2750 (2005).
29. Lingnau, K. et al. Poly-L-arginine synergizes, with oligodeoxynucleotides containing CpG-motifs (CpG-ODN) for enhanced and prolonged immune responses and prevents the CpG-ODN-induced systemic release of pro-inflammatory cytolkines. Vaccine 20, 3498-3508 (2002).
30. da Fonseca, D. P., Frerichs, J., Singh, M., Snippe, H. & Verheul, A. F. Induction of antibody and T-cell responses by immunization with ISCOMS containing the 38-kilodalton protein of Mycobacterium tuberculosis. Vaccine 19, 122-131 (2000).
31. Holten-Andersen, L., Doherty T. M., Korsholm, K. S. & Andersen, P. Combination of the cationic surfactant dimethyl dioctadecyl ammonium bromide and synthetic mycobacterial cord factor as an efficient adjuvant for tuberculosis subunit vaccines. Infect. Immun. 72, 1608-1617 (2004).
32. Aronson, N. E. et al. Long-term efficacy of BCG vaccine in American Indians and Alaska Natives: a 60-year follow-up study. JAMA 291, 2086-2091 (2004).
33. Hart, P. D. & Sutherland, I. BCG and vole bacillus vaccines in the prevention of tuberculosis in adolescence and early adult life. Br. Med. J. 2, 293-295 (1977).
34. Comstock, G. W., Woolpert, S. F. & Livesay, V. T. Tuberculosis studies in Muscogee County, Georgia. Twenty-year evaluation of a community trial of BCG vaccination, Public Health Rep. 91, 276-280 (1976).
35. Dye, C. A booster for tuberculosis vaccines. JAMA 291, 2127-2128 (2004).
36. Brooks, J. V., Frank, A. A., Keen, M. A., Belisle, J. T. & Orme, I. M. Boosting vaccine for tuberculosis. Infect. Immun. 69, 2714-2717 (2001).
37. Brandt, L. et al. The protective effect of the Mycobacterium bovis BCG vaccine is increased by coadministration with the Mycobacterium tuberculosis 72-kilodalton fusion polyprotein Mtb72F in M. tuberculosis-infected guinea pigs. Infect. Immun. 72, 6622-6632 (2004).
38. Orme, I. M. Beyond BCG: the potential for a more effective TB vaccine. Mol. Med. Today 5, 487-492 (1999).
39. Smith, D. W. Protective effect of BCG in experimental tuberculosis. Adv. Tuberc. Res. 22, 1-97 (1985).
40. Orme, I, M., McMurray, D. N. & Belisle, J. T. Tuberculosis vaccine development: recent progress, Trends Microbiol. 9, 115-118 (2001).
41. Skeiky, Y. A. et al. T cell expression cloning of a Mycobacterium tuberculosis gene encoding a protective antigen associated with the early control of infection. J. Immunol. 165, 7140-7149 (2000).
42. Olsen, A. W., Hansen, P. R., Holm, A. & Andersen, P. Efficient protection against Mycobacterium tuberculosis by vaccination with a single subdominant epitope from the ESAT-6 antigen. Eur. J. Immunol. 30, 1724-1732 (2000).
43. Wilson, M. E., Fineberg, H. V. & Colditz, G. A. Geographic latitude and the efficacy of bacillus Calmette-Guerin vaccine. Clin. Infect. Dis. 20, 982-991 (1995).
44. Colditz, G. A. et al. Efficacy of BCG vaccine in the prevention of tubeculosis. Meta-analysis of the published literature. JAMA 271, 698-702 (1994).
45. Cole, S. T. & Barrell, B. G. Analysis of the genome of Mycobacterium tuberculosis H37Rv. Novartis Found. Symp. 217, 160-172 (1998).
46. Brosch, R. et al. Comparative genomics of the mycobacteria. Int. J. Med. Microbiol. 290, 143-152 (2000).
47. Chaparas, S. D., Maloney, C. J. & Hedrick, S. R. Specificity of tuberculins and antigens from various species of mycobacteria. Am. Rev. Respir. Dis. 101, 74-83 (1970).
48. Harboe, M., Mshana, R. N., Closs, O., Kronvall, G. & Axelsen, N. H. Cross-reactions between mycobacteria. II. Crossed immunoelectrophoretic analysis of soluble antigens of BCG and comparison with other mycobacteria. Scand. J. Immunol. 9, 115-124 (1979).
49. von Reyn, C. F. et al. Skin test reactions to Mycobacterium tuberculosis purified protein derivative and Mycobacterium avium sensitin among health care workers and medical students in the United States. Int. J. Tuberc. Lung Dis. 5, 1122-1128 (2001).
50. von Reyn, C. F. et al. Dual skin testing with Mycobacterium avium sensitin and purified protein derivative to discriminate pulmonary disease due to M. avium complex from pulmonary disease due to Mycobacterium tuberculosis. J. Infect. Dis. 177, 730-736 (1998).
51. Manabe, Y. C., Scott, C. P. & Bishai, W. R. Naturally attenuated, orally administered Mycobacterium microti as a tuberculosis vaccine is better than subcutaneous Mycobacterium bovis BCG. Infect. Immun. 70, 1566-1570 (2002).
52. Brooks, R. W., Parker, B. C.. Gruft, H. & Falkinham, J. O., 3rd. Epidemiology of infection by nontuberculous mycobacteria. V. Numbers in eastern United States soils and correlation with soil characteristics. Am. Rev. Respir. Dis. 130, 630-633 (1984).
53. Kamala, T., Paramasivan, C. N., Herbert, D., Venkatesan, P. & Prabhakar, R. Immune response & modulation of immune response induced in the guinea-pigs by Mycobacterium avium complex (MAC) & M. fortuitum complex isolates from different sources in the south Indian BCG trial area. Indian J. Med. Res. 103, 201-211 (1996).
54. Black, G. F. et al. Patterns and implications of naturally acquired immune responses to environmental and tuberculous mycobacterial antigens in northern Malawi. J. Infect. Dis. 184, 322-329 (2001).
55. Black, G. F. et al. BCG-induced increase in interferon-γ response to mycobacterial antigens and efficacy of BCG vaccination in Malawi and the UK: two randomised controlled studies. Lancet 359, 1393-1401 (2002).
56. Weir, R. E. et al. Interferon-γ and skin test responses of schoolchildren in southeast England to purified protein derivatives from Mycobacterium tuberculosis and other species of mycobacteria. Clin. Exp. Immunol. 134, 285-294 (2003).
57. Floyd, S. et al. Kinetics of delayed-type hypersensitivity to tuberculin induced by bacille Calmette-Guerin vaccination in northern Malawi. J. Infect. Dis. 186, 807-814 (2002).
58. Black. G. F. et al. Relationship between IFN-γ and skin test responsiveness to Mycobacterium tuberculosis PPD in healthy, non-BCG-vaccinated young adults in Northern Malawi. Int. J. Tuberc. Lung Dis. 5, 664-672 (2001).
59. Miceli, I. et al. Evaluation of the effectiveness of BCG vaccination using the case-control method in Buenos Aires, Argentina. Int. J. Epidemiol. 17, 629-634 (1988).
60. al-Kassimi, F. A., al-Hajjaj, M. S., al-Orainey, I. O. & Bamgboye, E. A. Does the protective effect of neonatal BCG correlate with vaccine-induced tuberculin reaction? Am. J. Respir. Crit. Care Med. 152, 1575-1578 (1995).
61. Brewer, T. F. Preventing tuberculosis with bacillus Calmette-Guerin vaccine: a meta-analysis of the literature. Clin. Infect. Dis. 31, S64-S67 (2000).
62. Palmer, C. E. & Long, M. W. Effects of infection with atypical mycobacteria on BCG vaccination and tuberculosis. Am. Rev. Respir. Dis. 94, 553-568 (1966).
63. Ponnighaus, J. M. et al. Efficacy of BCG vaccine against leprosy and tuberculosis in northern Malawi. Lancet 339, 636-639 (1992).
64. Brosch, R., Gordon, S. V., Eiglmeier, K., Garnier, T. & Cole, S. T. Comparative genomics of the leprosy and tubercle bacilli. Res. Microbiol. 151, 135-142 (2000).
65. Grzybowski, S. & Dorken, E. Tuberculosis in Inuit. Ecol. Dis. 2, 145-148 (1983).
66. Brandt, L. et al. Failure of the Mycobacterium bovis BCG vaccine: some species of environmental mycobacteria block multiplication of BCG and induction of protective immunity to tuberculosis. Infect. Immun. 70, 672-678 (2002).
67. Francis, J. Natural and experimental tuberculosis in monkeys; with observations on immunization and chemotherapy. J. Comp. Pathol. 66, 123-135 (1956).
68. Sielbenmann, C. O. Effect of BCG vaccination and chemotherapy on experimental tuberculosis in mice. J. Immunol. 67, 137-149 (1951).
69. Lozes, E. et al. Cross-reactive immune responses against Mycobacterium bovis BCG in mice infected with non-tuberculous mycobacteria belonging to the MAIS-Group. Scand. J. Immunol. 46, 16-26 (1997).
70. Buddle, B. M., Wards, B. J., Aldwell, F. E., Collins, D. M. & de Lisle, G. W. Influence of sensitisation to environmental mycobacteria on subsequent vaccination against bovine tuberculosis. Vaccine 20, 1126-1133 (2002).
71. de Lisle, G. W., Wards, B. J., Buddle, B. M. & Collins, D. M. The efficacy of live tuberculosis vaccines after presensitization with Mycobacterium avium. Tuberculosis (Edinb.) 85, 73-79 (2005).
72. Demangel, C., Garnier, T., Rosenkrands, I. & Cole, S. T. Differential effects of prior exposure to environmental mycobacteria on vaccination with Mycobacterium bovis BCG or a recombinant BCG strain expressing RD1 antigens. Infect. Immun. 73, 2190-2196 (2005).
73. Palmer, C. E. BCG vaccination and tuberculin allergy. Lancet 1, 935-940 (1952).
74. Baily, G. V. Tuberculosis prevention Trial, Madras. Indian J. Med. Res. 72, S1-S74 (1980).
75. Guld, J., Waaler, H., Sundaresan, T. K., Kaufmann, P. C. & ten Dam, H. G. The duration of BCG-induced tuberculin sensitivity in children, and its irrelevance for revaccination. Results of two 5-year prospective studies. Bull. World Health Org. 39, 829-836 (1968).
76. Horwitz, O. & Bunch-Christensen, K. Correlation between tuberculin sensitivity after 2 months and 5 years among BCG vaccinated subjects. Bull. Word Health Org. 47, 49-58 (1972).
77. Fine, P. E., Sterne, J. A., Ponnighaus, J. M. & Rees, R. J. Delayed-type hypersensitivity mycobacterial vaccines and protective immunity. Lancet 344, 1245-1249 (1994).
78. Gomes, M. G., Franco, A. O., Gomes, M. C. & Medley, G. F. The reinfection threshold promotes variability in tuberculosis epidemiology and vaccine efficacy. Proc. Biol. Sci. 271, 617-623 (2004).
79. Williams, A. et al. Evaluation of vaccines in the EU TB Vaccine Cluster using a guinea pig aerosol infection model of tuberculosis. Tuberculosis (Edinb.) 85, 29-38 (2005).
80. Reed, S. G., Alderson, M. R., Dalemans, W., Lobet, Y. & Skelky, Y. A. Prospects for a better vaccine against tuberculosis. Tuberculosis (Edinb.) 83, 213-219 (2003).
81. van Rie, A. et al. Exogenous reinfection as a cause of recurrent tuberculosis after curative treatment. New Engl. J. Med. 341, 1174-1179 (1999).
82. O'Regan, A. & Joyce-Brady, M. Latent tuberculosis may persist for over 40 years. BMJ 323, 635 (2001).
83. Lillebaek, T. et al. Molecular evidence of endogenous reactivation of Mycobacterium tuberculosis after 33 years of latent infection. J. Infect. Dis. 185, 401-404 (2002).
84. Doherty, T. M. & Andersen, P. Tuberculosis vaccine development. Curr. Opin. Pulm. Med. 8, 183-187 (2002).
85. Hogarth, P. J., Jahans, K. J., Hecker, R., Hewinson, R. G. & Chambers, M. A. Evaluation of adjuvants for protein vaccines against tuberculosis in guinea pigs. Vaccine 21, 977-982 (2003).
86. Feng, C. G., Blanchard, T. J., Smith, G. L., Hill, A. V. & Britton, W. J. Induction of CD8+ T-lymphocyte responses to a secreted antigen of Mycobacterium tuberculosis by an attenuated vaccinia virus. Immunol. Cell Biol. 79, 569-575 (2001).
87. Rook, G. A. & Stanford, J. L. The Koch phenomenon and the immunopathology of tuberculosis. Curr. Top. Microbiol. Immunol. 215, 239-262 (1996).
88. Anon. New TB vaccine trials set to start in Britain [online], (2001).
89. Fruth, U. & Young, D. Prospects for new TB vaccines: Stop TB working group on TB vaccine development. Int. J. Tuberc. Lung Dis. 8, 151-155 (2004).
90. Thomson, J. New TB vaccines to be tested. Nature Med. 12, 1263 (2001).
91. Horwitz, M. A., Harth. G., Dillon, B. J. & Maslesa-Galic, S. Recombinant bacillus calmette-guerin (BCG) vaccines expressing the Mycobacterium tuberculosis 30-kDa major secretory protein induce greater protective immunity against tuberculosis than conventional BCG vaccines in a highly susceptible animal model. Proc. Natl Acad. Sci. USA 97, 13853-13858 (2000).
92. Goonetilleke, N. P. et al. Enhanced immunogenicity and protective efficacy against Mycobacterium tuberculosis of bacille Calmette-Guerin vaccine using mucosal administration and boosting with a recombinant modified vaccinia virus Ankara. J. Immunol. 171, 1602-1609 (2003).