RTS,S malaria vaccine development: progress and considerations for postapproval introduction

References

• World Health Organisation. World Malaria Report. Switzerland:World Health Organisation; 2014.
   Google Scholar
• Aregawi MW, Ali AS, Al-mafazy AW, et al. Reductions in malaria and anaemia case and death burden at hospitals following scale-up of malaria control in Zanzibar, 1999–2008. Malar J. 2011;10:46.
   Web of Science ®Google Scholar
• Simon C, Moakofhi K, Mosweunyane T, et al. Malaria control in Botswana, 2008–2012:the path towards elimination. Malar J. 2013;12:458.
   Web of Science ®Google Scholar
• Kamuliwo M, Chanda E, Haque U, et al. The changing burden of malaria and association with vector control interventions in Zambia using district-level surveillance data, 2006–2011. Malar J. 2013;12:437.
   Web of Science ®Google Scholar
• Ashley EA, Dhorda M, Fairhurst RM, et al. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2014;371(5):411–423.
   PubMed Web of Science ®Google Scholar
• Sachs J, Malaney P. The economic and social burden of malaria. Nature. 2002;415(6872):680–685.
   PubMed Web of Science ®Google Scholar
• Morrison C. Landmark green light for Mosquirix malaria vaccine. Nat Biotechnol. 2015;;33(10):1015–6.
   PubMed Web of Science ®Google Scholar
• Nussenzweig RS, Vanderberg J, Most H, Orton C. Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. Nature. 1967;216(5111):160–162.
   PubMed Web of Science ®Google Scholar
• RTS, S ClinicalTrials Partnership, et al. 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(9988):31–45.
   Web of Science ®Google Scholar
• Kumar KA, Sano G, Boscardin S, et al. The circumsporozoite protein is an immunodominant protective antigen in irradiated sporozoites. Nature. 2006;444(7121):937–940.
   Web of Science ®Google Scholar
• Hodgson SH, Ewer KJ, Bliss CM, et al. Evaluation of the efficacy of ChAd63-MVA vectored vaccines expressing circumsporozoite protein and ME-TRAP against controlled human malaria infection in malaria-naive individuals. J Infect Dis. 2015;211(7):1076–1086.
   PubMed Web of Science ®Google Scholar
• Spring MD, Cummings JF, Ockenhouse CF, et al. Phase 1/2a study of the malaria vaccine candidate apical membrane antigen-1 (AMA-1) administered in adjuvant system AS01B or AS02A. PLoS One. 2009;4(4):e5254.
   PubMed Web of Science ®Google Scholar
• Chitnis CE, Mukherjee P, Mehta S, et al. Phase I clinical trial of a recombinant blood stage vaccine candidate for Plasmodium falciparum malaria based on MSP1 and EBA175. PLoS One. 2015;10(4):e0117820.
   Web of Science ®Google Scholar
• Seder RA, Chang LJ, Enama ME, et al. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science. 2013;341(6152):1359–1365.
   PubMed Web of Science ®Google Scholar
• Ockenhouse CF, Sun PF, Lanar DE, et al. Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. J Infect Dis. 1998;177(6):1664–1673.
   Google Scholar
• Schwartz L, Brown GV, Genton B, Moorthy VS. A review of malaria vaccine clinical projects based on the WHO rainbow table. Malar J. 2012;11:11.
   PubMed Web of Science ®Google Scholar
• Sherwood JA, Copeland RS, Taylor KA, et al. Plasmodium falciparum circumsporozoite vaccine immunogenicity and efficacy trial with natural challenge quantitation in an area of endemic human malaria of Kenya. Vaccine. 1996;14(8):817–827.
   Web of Science ®Google Scholar
• Brown AE, Singharaj P, Webster HK, et al. Safety, immunogenicity and limited efficacy study of a recombinant Plasmodium falciparum circumsporozoite vaccine in Thai soldiers. Vaccine. 1994;12(2):102–108.
   Google Scholar
• 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(9443):1411–1420.
   Google Scholar
• Leach A, Vekemans J, Lievens M, et al. Design of a phase III multicenter trial to evaluate the efficacy of the RTS,S/AS01 malaria vaccine in children across diverse transmission settings in Africa. Malar J. 2011;10:224.
   PubMed Web of Science ®Google Scholar
• 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(9598):1543–1551.
   PubMed Web of Science ®Google Scholar
• Aide P, Aponte JJ, Renom M, et al. Safety, immunogenicity and duration of protection of the RTS,S/AS02(D) malaria vaccine:one year follow-up of a randomized controlled phase I/IIb trial. PLoS One. 2010;5(11):e13838.
   PubMed Web of Science ®Google Scholar
• Leroux-Roels G, Leroux-Roels I, Clement F, et al. Evaluation of the immune response to RTS,S/AS01 and RTS,S/AS02 adjuvanted vaccines:randomized, double-blind study in malaria-naive adults. Hum Vaccin Immunother. 2014;10(8):2211–2219.
   PubMed Web of Science ®Google Scholar
• Asante KP, Abdulla S, Agnandji S, et al. Safety and efficacy of the RTS,S/AS01E candidate malaria vaccine given with expanded-programme- on-immunisation vaccines:19 month follow-up of a randomised, open-label, phase 2 trial. Lancet Infect Dis. 2011;11(10):741–749.
   PubMed Web of Science ®Google Scholar
• Bejon P, White MT, Olotu A, et al. Efficacy of RTS,S malaria vaccines:individual-participant pooled analysis of phase 2 data. Lancet Infect Dis. 2013;13(4):319–327.
   PubMed Web of Science ®Google Scholar
• Neafsey DE, Juraska M, Bedford T, et al. Genetic diversity and protective efficacy of the RTS,S/AS01 Malaria vaccine. N Engl J Med. 2015;373(21):2025–2037.
   PubMed Web of Science ®Google Scholar
• Plowe CV. Vaccine-resistant malaria. N Engl J Med. 2015;373(21):2082–2083.
   Web of Science ®Google Scholar
• Vekemans J, Guerra Y, Lievens M, et al. Pooled analysis of safety data from pediatric Phase II RTS,S/AS malaria candidate vaccine trials. Hum Vaccin. 2011;7(12):1309–1316.
   PubMed Web of Science ®Google Scholar
• 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(24):2284–2295.
   PubMed Web of Science ®Google Scholar
• RTS, S ClinicalTrials Partnership, et al. 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.
   Google Scholar
• Desai R, Oliveira LH, Parashar UD, Lopman B, Tate JE, Patel MM. Reduction in morbidity and mortality from childhood diarrhoeal disease after species A rotavirus vaccine introduction in Latin America – a review. Mem Inst Oswaldo Cruz. 2011;106(8):907–911.
   PubMed Web of Science ®Google Scholar
• Fitzwater SP, Chandran A, Santosham M, Johnson HL. The worldwide impact of the seven-valent pneumococcal conjugate vaccine. Pediatr Infect Dis J. 2012;31(5):501–508.
   PubMed Web of Science ®Google Scholar
• Moorthy VS, Hutubessy R, Newman RD, Hombach J. Decision-making on malaria vaccine introduction:the role of cost-effectiveness analyses. Bull World Health Organ. 2012;90(11):864–866.
   Web of Science ®Google Scholar
• World Health Organisation. Malaria vaccine:WHO position paper – January 2016. Wkly Epidemiol Rec. 2016;91(4):33–51.
   Google Scholar
• Chia WN, Goh YS, Renia L. Novel approaches to identify protective malaria vaccine candidates. Frontiers Microbiol. 2014;5:586.
   PubMed Web of Science ®Google Scholar
• Hodgson SH, Choudhary P, Elias SC, et al. Combining viral vectored and protein-in-adjuvant vaccines against the blood-stage malaria antigen AMA1:report on a phase 1a clinical trial. Mol Ther. 2014;22(12):2142–2154.
   PubMed Web of Science ®Google Scholar
• Garcon N, Heppner DG, Cohen J. Development of RTS,S/AS02:a purified subunit-based malaria vaccine candidate formulated with a novel adjuvant. Expert Rev Vaccines. 2003;2(2):231–238.
   PubMedGoogle Scholar
• Mettens P, Dubois PM, Demoitie MA, et al. Improved T cell responses to Plasmodium falciparum circumsporozoite protein in mice and monkeys induced by a novel formulation of RTS,S vaccine antigen. Vaccine. 2008;26(8):1072–1082.
   Google Scholar
• Ansong D, Asante KP, Vekemans J, et al. T cell responses to the RTS,S/AS01(E) and RTS,S/AS02(D) malaria candidate vaccines administered according to different schedules to Ghanaian children. PLoS One. 2011;6(4):e18891.
   PubMed Web of Science ®Google Scholar
• Owusu-Agyei S, Ansong D, Asante K, et al. Randomized controlled trial of RTS,S/AS02D and RTS,S/AS01E malaria candidate vaccines given according to different schedules in Ghanaian children. PLoS One. 2009;4(10):e7302.
   PubMed Web of Science ®Google Scholar
• Targett GA, Moorthy VS, Brown GV. Malaria vaccine research and development:the role of the WHO MALVAC committee. Malar J. 2013;12:362.
   Web of Science ®Google Scholar
• World Health Organisation. WHO Preferred Product Characteristics (PPC) for Malaria Vaccines. Switzerland:World Health Organisation; 2014.
   Google Scholar
• Fowkes FJ, Simpson JA, Beeson JG. Implications of the licensure of a partially efficacious malaria vaccine on evaluating second-generation vaccines. BMC Med. 2013;11:232.
   Web of Science ®Google Scholar
• Spring M, Polhemus M, Ockenhouse C. Controlled human malaria infection. J Infect Dis. 2014;209(Suppl 2):S40–S45.
   PubMed Web of Science ®Google Scholar
• Sauerwein RW, Roestenberg M, Moorthy VS. Experimental human challenge infections can accelerate clinical malaria vaccine development. Nat Rev Immunol 2011;11(1):57–64.
   PubMed Web of Science ®Google Scholar
• Gregory JA, Li F, Tomosada LM, et al. Algae-produced Pfs25 elicits antibodies that inhibit malaria transmission. PLoS One. 2012;7(5):e37179.
   PubMed Web of Science ®Google Scholar
• Howe LD, Manu A, Tawiah-Agyemang C, Kirkwood BR, Hill Z. Developing a community-based neonatal care intervention:a health facility assessment to inform intervention design. Paediatr Perinat Epidemiol. 2011;25(2):192–200.
   Web of Science ®Google Scholar
• Sambo LG, Kirigia JM. Investing in health systems for universal health coverage in Africa. BMC Int Health Hum Rights. 2014;14:28.
   PubMed Web of Science ®Google Scholar
• Vekemans J, Marsh K, Greenwood B, et al. Assessment of severe malaria in a multicenter, phase III, RTS, S/AS01 malaria candidate vaccine trial:case definition, standardization of data collection and patient care. Malar J. 2011;10:221.
   PubMed Web of Science ®Google Scholar
• Swysen C, Vekemans J, Bruls M, et al. Development of standardized laboratory methods and quality processes for a phase III study of the RTS, S/AS01 candidate malaria vaccine. Malar J. 2011;10:223.
   PubMed Web of Science ®Google Scholar
• Ogutu BR, Baiden R, Diallo D, Smith PG, Binka FN. Sustainable development of a GCP-compliant clinical trials platform in Africa:the malaria clinical trials alliance perspective. Malar J. 2010;9:103.
   PubMed Web of Science ®Google Scholar
• Kilama WL, Chilengi R, Wanga CL. Towards an African-driven malaria vaccine development program:history and activities of the African Malaria Network Trust (AMANET). Am J Trop Med Hyg. 2007;77(6 Suppl):282–288.
   Web of Science ®Google Scholar
• Bakshi S, Imoukhuede EB. Malaria Vectored Vaccines Consortium (MVVC). Hum Vaccin. 2010;6(6):433–434.
   Google Scholar
• Kilama WL. The 10/90 gap in sub-Saharan Africa:resolving inequities in health research. Acta Trop. 2009;112(Suppl 1):S8–S15.
   Google Scholar
• Newton S, Doku V, Geissler W, Asante KP, Cousens S. Drawing blood from young children:lessons learned from a trial in Ghana. Trans R Soc Trop Med Hyg. 2009;103(5):497–499.
   PubMed Web of Science ®Google Scholar
• Asante KP, Agyemang CT, Zandoh C, et al. Community engagement in biomedical research in an African setting:the Kintampo Health Research Centre experience. BMC Health Serv Res. 2013;13:383.
   Web of Science ®Google Scholar
• Bangha M, Diagne A, Bawah A, Sankoh O. Monitoring the millennium development goals:the potential role of the INDEPTH Network. Glob Health Action. 2010;3:5517.
   PubMed Web of Science ®Google Scholar
• Olsson S, Pal SN, Dodoo A. Pharmacovigilance in resource-limited countries. Expert Rev Clin Pharmacol. 2015;8(4):449–460.
   PubMed Web of Science ®Google Scholar
• Baiden R, Oduro A, Halidou T, et al. Prospective observational study to evaluate the clinical safety of the fixed-dose artemisinin-based combination Eurartesim(R) (dihydroartemisinin/piperaquine), in public health facilities in Burkina Faso, Mozambique, Ghana, and Tanzania. Malar J. 2015;14:160.
   PubMed Web of Science ®Google Scholar
• Bines JE, Kohl KS, Forster J, et al. Acute intussusception in infants and children as an adverse event following immunization:case definition and guidelines of data collection, analysis, and presentation. Vaccine. 2004;22(5–6):569–574.
   PubMed Web of Science ®Google Scholar
• Gardner-Medwin JM, Dolezalova P, Cummins C, Southwood TR. Incidence of Henoch-Schonlein purpura, Kawasaki disease, and rare vasculitides in children of different ethnic origins. Lancet. 2002;360(9341):1197–1202.
   PubMed Web of Science ®Google Scholar
• Kaslow DC, Biernaux S. RTS,S:toward a first landmark on the malaria vaccine technology roadmap. Vaccine. 2015;33(52):7425–7432.
   PubMed Web of Science ®Google Scholar
• Juan-Giner A, Domicent C, Langendorf C, et al. A cluster randomized non-inferiority field trial on the immunogenicity and safety of tetanus toxoid vaccine kept in controlled temperature chain compared to cold chain. Vaccine. 2014;32(47):6220–6226.
   Web of Science ®Google Scholar
• PATH. Sustainability in Vaccine Packaging. Seattle, WA:PATH; 2011.
   Google Scholar
• Jegede AS. What led to the Nigerian boycott of the polio vaccination campaign? PLoS Med. 2007;4(3):e73.
   PubMed Web of Science ®Google Scholar
• Dodoo A, Adjei S, Couper M, Hugman B, Edwards R. When rumours derail a mass deworming exercise. Lancet. 2007;370(9586):465–466.
   PubMed Web of Science ®Google Scholar
• Ojakaa DI, Ofware P, Machira YW, et al. Community perceptions of malaria and vaccines in the South Coast and Busia regions of Kenya. Malar J. 2011;10:147.
   PubMed Web of Science ®Google Scholar
• Febir LG, Asante KP, Dzorgbo DB, Senah KA, Letsa TS, Owusu-Agyei S. Community perceptions of a malaria vaccine in the Kintampo districts of Ghana. Malar J. 2013;12:156.
   PubMed Web of Science ®Google Scholar
• Bingham A, Gaspar F, Lancaster K, Conjera J, Collymore Y, Ba-Nguz A. Community perceptions of malaria and vaccines in two districts of Mozambique. Malar J. 2012;11:394.
   Web of Science ®Google Scholar
• Menaca A, Tagbor H, Adjei R, et al. Factors likely to affect community acceptance of a malaria vaccine in two districts of Ghana:a qualitative study. PLoS One. 2014;9(10):e109707.
   Web of Science ®Google Scholar
• Galactionova K, Bertram M, Lauer J, Tediosi F. Costing RTS,S introduction in Burkina Faso, Ghana, Kenya, Senegal, Tanzania, and Uganda:a generalizable approach drawing on publicly available data. Vaccine. 2015;33(48):6710–6718.
   Google Scholar