Causes of variation in BCG vaccine efficacy: Examining evidence from the BCG REVAC cluster randomized trial to explore the masking and the blocking hypotheses

Vaccine

Volumn 32, Issue 30, 2014, Pages 3759-3764

  Barreto, Mauricio L ^a   Pilger, Daniel ^b,g   Pereira, Susan M ^a   Genser, Bernd ^a,c   Cruz, Alvaro A ^a   Cunha, Sergio S ^d   Sant'Anna, Clemax ^e   Hijjar, Miguel A ^f   Ichihara, Maria Y ^a   Rodrigues, Laura C ^b  

^a FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^e FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^f INSTITUTO OSWALDO CRUZ   (Brazil)

^g National Institute for Medical Research (Mwanza Branch)   (Tanzania)

Author keywords

BCG; Blocking; Efficacy; Geographical variation; Masking; Protection; Tuberculosis; Vaccine

Indexed keywords

BCG VACCINE;

ARTICLE; BCG VACCINATION; CHILD; CLUSTER ANALYSIS; CONTROLLED STUDY; DRUG EFFICACY; EL SALVADOR; FEMALE; HUMAN; LUNG TUBERCULOSIS; MALE; NEIGHBORHOOD; NEWBORN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REVACCINATION; SCHOOL CHILD; SOCIOECONOMICS; TUBERCULOSIS; ADOLESCENT; BRAZIL; GEOGRAPHY; IMMUNIZATION; IMMUNOLOGY; INTERVENTION STUDY; SOCIAL CLASS;

ADOLESCENT; BCG VACCINE; BRAZIL; CHILD; FEMALE; GEOGRAPHY; HUMANS; IMMUNIZATION, SECONDARY; INFANT, NEWBORN; INTERVENTION STUDIES; MALE; SOCIAL CLASS; TUBERCULOSIS;

EID: 84922231879     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2014.05.042     Document Type: Article

References (47)

1. Health Protection Agency Centre for Infections Tuberculosis in the UK: annual report on tuberculosis surveillance in the UK 2010.
2. Kaufmann S.H. Tuberculosis vaccines-a new kid on the block. Nat Med 2011, 17:159-160.
3. Rodrigues L.C., Diwan V.K., Wheeler J.G. Protective effect of BCG against tuberculous meningitis and miliary tuberculosis: a meta-analysis. Int J Epidemiol 1993, 22:1154-1158.
4. Fine P.E. Variation in protection by BCG: implications of and for heterologous immunity. Lancet 1995, 346:1339-1345.
5. Kaufmann S.H., Hussey G., Lambert P.H. New vaccines for tuberculosis. Lancet 2010, 375:2110-2119.
6. Agger E.M., Andersen P. A novel TB vaccine towards a strategy based on our understanding of BCG failure. Vaccine 2002, 21:7-14.
7. Russell D.G., Barry C.E., Flynn J.L. Tuberculosis: what we don't know can, and does, hurt us. Science 2010, 328:852-856.
8. Tameris M.D., Hatherill M., Landry B.S., Scriba T.J., Snowden M.A., Lockhart S., et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet 2013, 381:1021-1028.
9. Dye C., Fine P.E. A major event for new tuberculosis vaccines. Lancet 2013, 381:972-974.
10. Dye C. Making wider use of the world's most widely used vaccine: bacille Calmette-Guerin revaccination reconsidered. J R Soc Interface 2013, 10:20130365.
11. Fine P., Carneiro A., Milstien J., Clements C. Issues relating to the use of BCG in immunization programmes 1999, WHO, Geneva.
12. Fine P.E., Rodrigues L.C. Modern vaccines. Mycobacterial diseases. Lancet 1990, 335:1016-1020.
13. Smith D.W. Protective effect of BCG in experimental tuberculosis. Adv Tuberc Res 1985, 22:1-97.
14. Colditz G.A., Berkey C.S., Mosteller F., Brewer T.F., Wilson M.E., Burdick E., 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 1995, 96:29-35.
15. 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 1976, 91:276-280.
16. Tuberculosis Prevention Trial Trial of BCG vaccines in South India for tuberculosis prevention. Bull World Health Organ 1979, 57:819-827.
17. 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 1979, 9:115-124.
18. Brandt L., Feino Cunha J., Weinreich Olsen A., Chilima B., Hirsch P., Appelberg R., 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 2002, 70:672-678.
19. 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 2005, 73:2190-2196.
20. 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 1996, 103:201-211.
21. Hoefsloot W., van Ingen J., Andrejak C., Angeby K., Bauriaud R., Bemer P., et al. The geographic diversity of nontuberculous mycobacteria isolated from pulmonary samples: a NTM-NET collaborative study. Eur Respir J 2013, 42(6):1604-1613.
22. Andersen P., Doherty T.M. The success and failure of BCG-implications for a novel tuberculosis vaccine. Nat Rev Microbiol 2005, 3:656-662.
23. Palmer C.E., Long M.W. Effects of infection with atypical mycobacteria on BCG vaccination and tuberculosis. Am Rev Respir Dis 1966, 94:553-568.
24. Colditz G.A., Brewer T.F., Berkey C.S., Wilson M.E., Burdick E., Fineberg H.V., et al. Efficacy of BCG vaccine in the prevention of tuberculosis. Meta-analysis of the published literature. JAMA 1994, 271:698-702.
25. Lozes E., Denis O., Drowart A., Jurion F., Palfliet K., Vanonckelen A., 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 1997, 46:16-26.
26. Rodrigues L.C., Pereira S.M., Cunha S.S., Genser B., Ichihara M.Y., de Brito S.C., et al. Effect of BCG revaccination on incidence of tuberculosis in school-aged children in Brazil: the BCG-REVAC cluster-randomised trial. Lancet 2005, 366:1290-1295.
27. Pereira S.M., Barreto M.L., Pilger D., Cruz A.A., Sant'Anna C., Hijjar M.A., et al. Effectiveness and cost-effectiveness of first BCG vaccination against tuberculosis in school-age children without previous tuberculin test (BCG-REVAC trial): a cluster-randomised trial. Lancet Infect Dis 2012, 12:300-306.
28. Barreto M.L., Pereira S.M., Pilger D., Cruz A.A., Cunha S.S., Sant'Anna C., et al. Evidence of an effect of BCG revaccination on incidence of tuberculosis in school-aged children in Brazil: second report of the BCG-REVAC cluster-randomised trial. Vaccine 2011, 29:4875-4877.
29. Barreto M.L., Rodrigues L.C., Cunha S.S., Pereira S., Hijjar M.A., Ichihara M.Y., et al. Design of the Brazilian BCG-REVAC trial against tuberculosis: a large, simple randomized community trial to evaluate the impact on tuberculosis of BCG revaccination at school age. Control Clin Trials 2002, 23:540-553.
30. Pereira S.M., Bierrenbach A.L., Dourado I., Barreto M.L., Ichihara M.Y., Hijjar M.A., et al. Sensitivity and specificity of the BCG scar reading. Rev Saude Publica 2003, 37:254-259.
31. Pereira S.M., Dourado I., Barreto M.L., Cunha S.S., Ichihara M.Y., Hijjar M.A., et al. Sensitivity and specificity of BCG scar reading in Brazil. Int J Tuberc Lung Dis 2001, 5:1067-1070.
32. Barbosa T., Arruda S., Fernandes B.D., Carvalho L.P., Cardoso S., Cunha S., et al. BCG (Bacille of Calmette-Guerin) revaccination leads to improved in vitro IFN-gamma response to mycobacterial antigen independent of tuberculin sensitization in Brazilian school-age children. Vaccine 2003, 21:2152-2160.
33. Bierrenbach A.L., Cunha S.S., Barreto M.L., Pereira S.M., Rodrigues L.C. Skin test reactivity to mycobacterial antigens parallels the phylogenetic structure of their genus. Int J Tuberc Lung Dis 2001, 5:656-663.
34. Dourado I., Rios M.H., Pereira S.M., Cunha S.S., Ichihara M.Y., Goes J.C., et al. Rates of adverse reactions to first and second doses of BCG vaccination: results of a large community trial in Brazilian schoolchildren. Int J Tuberc Lung Dis 2003, 7:399-402.
35. Cunha S.S., Alexander N., Barreto M.L., Pereira E.S., Dourado I., Maroja Mde F., et al. BCG revaccination does not protect against leprosy in the Brazilian Amazon: a cluster randomised trial. PLoS Negl Trop Dis 2008, 2:e167.
36. Camargos P.A., Guimaraes M.D., Antunes C.M. Risk assessment for acquiring meningitis tuberculosis among children not vaccinated with BCG: a case-control study. Int J Epidemiol 1988, 17:193-197.
37. Nascimento-Costa M., Andrade-Mota M., Silva-Pinot L. Protective effect of intradermal BCG against tubercular meningitis. Bol Oficina Sanit Panam 1991, 110:26-32.
38. Wunsch Filho V., de Castilho E.A., Rodrigues L.C., Huttly S.R. Effectiveness of BCG vaccination against tuberculous meningitis: a case-control study in Sao Paulo, Brazil. Bull World Health Organ 1990, 68:69-74.
39. Global Programme on Tuberculosis, Global Programme on Vaccines Statement on BCG revaccination for the prevention of tuberculosis. Wkly Epidemiol Rec 1995, 70:229-231.
40. Ministerio da Saude Programa Nacional De Controle Da Tuberculose (PNCT) 2011, Available from:, [cited 29.03.11]. http://portal.saude.gov.br/.
41. Barreto M.L., Cunha S.S., Pereira S.M., Genser B., Hijjar M.A., Ichihara M.Y., et al. Neonatal BCG protection against tuberculosis lasts for 20 years in Brazil. Int J Tuberc Lung Dis 2005, 9:1171-1173.
42. Liang K.Y., Zeger S.L. Longitudinal data analysis using generalized linear models. Biometrika 1986, 73:13-22.
43. Black G.F., Weir R.E., Floyd S., Bliss L., Warndorff D.K., Crampin A.C., et al. BCG-induced increase in interferon-gamma response to mycobacterial antigens and efficacy of BCG vaccination in Malawi and the UK: two randomised controlled studies. Lancet 2002, 359:1393-1401.
44. Hernandez-Pando R., Pavon L., Arriaga K., Orozco H., Madrid-Marina V., Rook G. Pathogenesis of tuberculosis in mice exposed to low and high doses of an environmental mycobacterial saprophyte before infection. Infect Immun 1997, 65:3317-3327.
45. 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 2002, 20:1126-1133.
46. 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 2005, 85:73-79.
47. Abu-Raddad L.J., Sabatelli L., Achterberg J.T., Sugimoto J.D., Longini I.M., Dye C., et al. Epidemiological benefits of more-effective tuberculosis vaccines, drugs, and diagnostics. Proc Natl Acad Sci U S A 2009, 106:13980-13985.