Genetic diversity and protective efficacy of the RTS,S/AS01 malaria vaccine

New England Journal of Medicine

Volumn 373, Issue 21, 2015, Pages 2025-2037

  Neafsey, D E ^a   Juraska, M ^d   Bedford, T ^d   Benkeser, D ^d,e   Valim, C ^a,b,d   Griggs, A ^a   Lievens, M ^f   Abdulla, S ^g   Adjei, S ⁱ   Agbenyega, T ⁱ   Agnandji, S T ^k,l   Aide, P ^m,n   Anderson, S ^a   Ansong, D ^k   Aponte, J J ^m,n   Asante, K P ^j   Bejon, P ^v   Birkett, A J ^o   Bruls, M ^f   Connolly, K M ^a   D'Alessandro, U ^p   Dobano C ^m,n   Gesase, S ^h   Greenwood, B ^j,q   Grimsby, J ^a   Tinto, H ^r   Hamel, M J ^s   Hoffman, I ^t   Kamthunzi, P ^u   Kariuki, S ^w   Kremsner, P G ^d,k,l   Leach, A ^f   Lell, B ^k,l   Lennon, N J ^a   Lusingu, J ^h   Marsh, K ^aa   Martinson, F ^u   Molel, J T ^g   Moss, E L ^a   Njuguna, P ^v   Ockenhouse, C F ^o   Ragama Ogutu, B ^x   Otieno, W ^x   Otieno, L ^x   Otieno, K ^w   Owusu Agyei, S ^j   Park, D J ^a   Pelle, K ^a,x   Robbins, D ^a   Russ, C ^a   Ryan, E M ^a   Sacarlal, J ^m   Sogoloff, B ^a   Sorgho, H ^r   Tanner, M ^y   Theander, T ^z   Valea, I ^r   Volkman, S K ^a,b,c   Yu, Q ^a   Lapierre, D ^f   Birren, B W ^a   Gilbert, P B ^d,e   Wirth, D F ^b   more..

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c SIMMONS COLLEGE   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f GSK   (Belgium)

^g Ifakara Health Institute   (Belgium)

^h NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (Tanzania)

ⁱ KWAME NKRUMAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Ghana)

^j KINTAMPO HEALTH RESEARCH CENTRE   (Ghana)

^k ALBERT SCHWEITZER HOSPITAL   (Gabon)

^l UNIVERSITY OF TÜBINGEN   (Germany)

^m Ministérioda Saúde   (Mozambique)

ⁿ CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^o PATH's Malaria Vaccine Initiative   (United States)

^p MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

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

^r Centre National de la Recherche Scientifique et Technologique   (Burkina Faso)

^s CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^t UNIVERSITY OF NORTH CAROLINA   (United States)

^u UNIVERSITY OF NORTH CAROLINA PROJECT   (Malawi)

^v KEMRI WELLCOME TRUST RESEARCH PROGRAMME   (Kenya)

^w KEMRI/CDC Research and Public Health Collaboration   (Kenya)

^x KEMRI Walter Reed Project   (Kenya)

^y SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^z UNIVERSITY OF COPENHAGEN   (Denmark)

^aa NONE

more..

Author keywords

[No Author keywords available]

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; MALARIA VACCINE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHILD; CLINICAL PROTOCOL; CONTROLLED STUDY; DNA EXTRACTION; DRUG EFFICACY; GENE LOCUS; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; INFANT; INFECTION PREVENTION; MAJOR CLINICAL STUDY; MALARIA; NEXT GENERATION SEQUENCING; OUTCOME ASSESSMENT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN POLYMORPHISM; VACCINATION; AFRICA; CLINICAL TRIAL; FEMALE; GENETICS; IMMUNOLOGY; MALARIA, FALCIPARUM; MALE; MULTICENTER STUDY; PARASITOLOGY; PHASE 3 CLINICAL TRIAL; PLASMODIUM FALCIPARUM; RANDOMIZED CONTROLLED TRIAL; TREATMENT OUTCOME;

AFRICA; FEMALE; GENETIC VARIATION; HUMANS; INFANT; MALARIA VACCINES; MALARIA, FALCIPARUM; MALE; PLASMODIUM FALCIPARUM; TREATMENT OUTCOME;

EID: 84947728417     PISSN: 00284793     EISSN: 15334406     Source Type: Journal    
DOI: 10.1056/NEJMoa1505819     Document Type: Article

References (40)

1. World malaria report 2014. Geneva: World Health Organization, 2014 (http://www.who.int/malaria/publications/world-malaria-report-2014/report/en).
2. Hall BF, Fauci AS. Malaria control, elimination, and eradication: the role of the evolving biomedical research agenda. J Infect Dis 2009; 200: 1639-43.
3. Plowe CV, Alonso P, Hoffman SL. The potential role of vaccines in the elimination of falciparum malaria and the eventual eradi cation of malaria. J Infect Dis 2009;200:1646-9.
4. Agnandji ST, Lell B, Soulanoudjingar SS, et al. First results of phase 3 trial of RTS, S/AS01 malaria vaccine in African children. N Engl J Med 2011; 365: 1863-75.
5. Agnandji ST, Lell B, Fernandes JF, et al. A phase 3 trial of RTS, S/AS01 malaria vaccine in African infants. N Engl J Med 2012;367:2284-95.
6. RTS, S Clinical Trials Partnership. Efficacy and safety of the RTS, S/AS01 malaria vaccine during 18 months after vaccination: a phase 3 randomized, controlled trial in children and young infants at 11 African sites. PLoS Med 2014; 11(7): e1001685.
7. RTS, S Clinical Trials Partnership. Efficacy and safety of RTS, S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet 2015; 386:31-45.
8. Alonso PL, Sacarlal J, Aponte JJ, et al. Efficacy of the RTS, S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 2004; 364:1411-20.
9. Bejon P, Lusingu J, Olotu A, et al. Efficacy of RTS, S/AS01E vaccine against malaria in children 5 to 17 months of age. N Engl J Med 2008; 359: 2521-32.
10. Asante KP, Abdulla S, Agnandji S, et al. Safety and efficacy of the RTS, S/AS01E candidate malaria vaccine given with expanded-programme-on-immuni-sation vaccines: 19 month follow-up of a randomised, open-label, phase 2 trial. Lancet Infect Dis 2011; 11: 741-9.
11. Abdulla S, Oberholzer R, Juma O, et al. Safety and immunogenicity of RTS, S/AS02D malaria vaccine in infants. N Engl J Med 2008;359:2533-44.
12. Aponte JJ, Aide P, Renom M, et al. Safety of the RTS, S/AS02D candidate malaria vaccine in infants living in a highly endemic area of Mozambique: a double blind randomised controlled phase I/IIb trial. Lancet 2007;370:1543-51.
13. Agnandji ST, Asante K P, Lyimo J, et al. Evaluation of the safety and immunoge-nicity of the RTS, S/AS01E malaria candidate vaccine when integrated in the expanded program of immunization. J Infect Dis 2010; 202: 1076-87.
14. Lalvani A, Moris P, Voss G, et al. Potent induction of focused Th1-type cellular and humoral immune responses by RTS, S/SBAS2, a recombinant Plasmodium falciparum malaria vaccine. J Infect Dis 1999;180:1656-64.
15. Sun P, Schwenk R, White K, et al. Protective immunity induced with malaria vaccine, RTS, S, is linked to Plasmodium falciparum circumsporozoite protein-specific CD4+ and CD8+ T cells producing IFN-gamma. J Immunol 2003; 171: 6961-7.
16. Kester KE, Cummings JF, Ofori-Anyi-nam O, et al. Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS, S/AS01B and RTS, S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J Infect Dis 2009; 200: 337-46.
17. Campo JJ, Aponte JJ, Skinner J, et al. RTS, S vaccination is associated with sero-logic evidence of decreased exposure to Plasmodium falciparum liver-and blood-stage parasites. Mol Cell Proteomics 2015; 14:519-31.
18. Weedall GD, Preston BMJ, Thomas AW, Sutherland CJ, Conway DJ. Differential evidence of natural selection on two leading sporozoite stage malaria vaccine candidate antigens. Int J Parasitol 2007; 37:77-85.
19. Esposito F, Lombardi S, Modiano D, et al. Prevalence and levels of antibodies to the circumsporozoite protein of Plas-modium falciparum in an endemic area and their relationship to resistance against malaria infection. Trans R Soc Trop Med Hyg 1988;82:827-32.
20. Gandhi K, Thera MA, Coulibaly D, et al. Next generation sequencing to detect variation in the Plasmodium falciparum circumsporozoite protein. Am J Trop Med Hyg 2012;86:775-81.
21. Bailey JA, Mvalo T, Aragam N, et al. Use of massively parallel pyrosequencing to evaluate the diversity of and selection on Plasmodium falciparum csp T-cell epi-topes in Lilongwe, Malawi. J Infect Dis 2012;206:580-7.
22. Aragam NR, Thayer KM, Nge N, et al. Diversity of T cell epitopes in Plasmodium falciparum circumsporozoite protein likely due to protein-protein interactions. PLoS One 2013;8(5):e62427.
23. Good MF, Pombo D, Quakyi IA, et al. Human T-cell recognition of the circum-sporozoite protein of Plasmodium falci-parum: immunodominant T-cell domains map to the polymorphic regions of the molecule. Proc Natl Acad Sci USA 1988; 85:1199-203.
24. Calle JM, Nardin EH, Clavijo P, et al. Recognition of different domains of the Plasmodium falciparum CS protein by the sera of naturally infected individuals compared with those of sporozoite-immu-nized volunteers. J Immunol 1992; 149: 2695-701.
25. Reece WHH, Pinder M, Gothard PK, et al. A CD4(+) T-cell immune response to a conserved epitope in the circumsporo-zoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nat Med 2004; 10: 406-10.
26. Aide P, Dobaño C, Sacarlal J, et al. Four year immunogenicity of the RTS, S/AS02(A) malaria vaccine in Mozambican children during a phase IIb trial. Vaccine 2011;29:6059-67.
27. Takala SL, Coulibaly D, Thera MA, et al. Dynamics of polymorphism in a malaria vaccine antigen at a vaccine-testing site in Mali. PLoS Med 2007; 4(3): e93.
28. Gandhi K, Thera MA, Coulibaly D, et al. Variation in the circumsporozoite protein of Plasmodium falciparum: vaccine development implications. PLoS One 2014; 9(7):e101783.
29. Thera MA, Doumbo OK, Coulibaly D, et al. A field trial to assess a blood-stage malaria vaccine. N Engl J Med 2011; 365: 1004-13.
30. Alloueche A, Milligan P, Conway DJ, et al. Protective efficacy of the RTS, S/AS02 Plasmodium falciparum malaria vaccine is not strain specific. Am J Trop Med Hyg 2003;68:97-101.
31. Enosse S, Dobaño C, Quelhas D, et al. RTS, S/AS02A malaria vaccine does not induce parasite CSP T cell epitope selection and reduces multiplicity of infection. PLoS Clin Trials 2006; 1(1): e5.
32. Waitumbi JN, Anyona SB, Hunja CW, et al. Impact of RTS, S/AS02(A) and RTS, S/AS01(B) on genotypes of P. falciparum in adults participating in a malaria vaccine clinical trial. PLoS One 2009; 4(11): e7849.
33. Gilbert PB. Comparison of competing risks failure time methods and time-independent methods for assessing strain variations in vaccine protection. Stat Med 2000;19:3065-86.
34. Edlefsen PT, Rolland M, Hertz T, et al. Comprehensive sieve analysis of breakthrough HIV-1 sequences in the RV144 vaccine efficacy trial. PLoS Comput Biol 2015;11(2):e1003973.
35. National Center for Biotechnology Information. NCBI Sequence Read Archive (ht tp://w w w.ncbi.nlm.nih.gov/sra).
36. Van Der Laan MJ, Rubin D. A doubly robust censoring unbiased transformation. Int J Biostat2007; 3: Article 4.
37. Lunn M, McNeil D. Applying Cox regression to competing risks. Biometrics 1995;51:524-32.
38. Follmann D, Proschan M, Leifer E. Multiple outputation: inference for complex clustered data by averaging analyses from independent data. Biometrics 2003; 59:420-9.
39. Holm S. A simple sequentially rejec-tive multiple test procedure. Scand J Stat 1979;6:65-70.
40. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 1995; 57: 289-300.