Whole-sporozoite malaria vaccines: where we are, where we are going.

Plasmodium falciparum Plasmodium vivax Clinical Evaluation PfSPZ Vaccination Regimens

Journal

EMBO molecular medicine
ISSN: 1757-4684
Titre abrégé: EMBO Mol Med
Pays: Germany
ID NLM: 101487380

Informations de publication

Date de publication:
16 Sep 2024
Historique:
received: 12 05 2024
accepted: 14 08 2024
revised: 07 08 2024
medline: 17 9 2024
pubmed: 17 9 2024
entrez: 16 9 2024
Statut: aheadofprint

Résumé

The malaria vaccination landscape has seen significant advancements with the recent endorsement of RTS,S/AS01 and R21/Matrix-M vaccines, which target the pre-erythrocytic stages of Plasmodium falciparum (Pf) infection. However, several challenges remain to be addressed, including the incomplete protection afforded by these vaccines, their dependence on a single Pf antigen, and the fact that they were not designed to protect against P. vivax (Pv) malaria. Injectable formulations of whole-sporozoite (WSpz) malaria vaccines offer a promising alternative to existing subunit vaccines, with recent developments including genetically engineered parasites and optimized administration regimens. Clinical evaluations demonstrate varying efficacy, influenced by factors, such as immune status, prior exposure to malaria, and age. Despite significant progress, a few hurdles persist in vaccine production, deployment, and efficacy in malaria-endemic regions, particularly in children. Concurrently, transgenic parasites expressing Pv antigens emerge as potential solutions for PvWSpz vaccine development. Ongoing clinical studies and advancements in vaccine technology, including the recently described PfSPZ-LARC2 candidate, signify a hopeful future for WSpz malaria vaccines, which hold great promise in the global fight against malaria.

Identifiants

pubmed: 39284948
doi: 10.1038/s44321-024-00131-0
pii: 10.1038/s44321-024-00131-0
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : 'la Caixa' Foundation ('la Caixa')
ID : HR21-848
Organisme : Fundacao para a ciencia e tecnologia
ID : SFRH/BD/144817/2019
Organisme : European Commission (EC)
ID : 101080744

Informations de copyright

© 2024. The Author(s).

Références

Arisue N, Palacpac NMQ (2024) Asymptomatic parasitemia and RTS,S vaccine efficacy. Lancet Infect Dis https://doi.org/10.1016/S1473-3099(24)00214-7
Asante KP, Mathanga DP, Milligan P, Akech S, Oduro A, Mwapasa V, Moore KA, Kwambai TK, Hamel MJ, Gyan T, Westercamp N, Kapito-Tembo A, Njuguna P, Ansong D, Kariuki S, Mvalo T, Snell P, Schellenberg D, Welega P, Otieno L et al (2024) Feasibility, safety, and impact of the RTS,S/AS01(E) malaria vaccine when implemented through national immunisation programmes: evaluation of cluster-randomised introduction of the vaccine in Ghana, Kenya, and Malawi. Lancet 403:1660–1670
pubmed: 38583454 doi: 10.1016/S0140-6736(24)00004-7
Bermudez M, Moreno-Perez DA, Arevalo-Pinzon G, Curtidor H, Patarroyo MA (2018) Plasmodium vivax in vitro continuous culture: the spoke in the wheel. Malar J 17:301
pubmed: 30126427 pmcid: 6102941 doi: 10.1186/s12936-018-2456-5
Bijker EM, Nganou-Makamdop K, van Gemert GJ, Zavala F, Cockburn I, Sauerwein RW (2015) Studying the effect of chloroquine on sporozoite-induced protection and immune responses in Plasmodium berghei malaria. Malar J 14:130
pubmed: 25889324 pmcid: 4389414 doi: 10.1186/s12936-015-0626-2
Bjorkman A, Benn CS, Aaby P, Schapira A (2023) RTS,S/AS01 malaria vaccine-proven safe and effective? Lancet Infect Dis 23:e318–e322
pubmed: 37086747 doi: 10.1016/S1473-3099(23)00126-3
Bowers C, Hancox L, Peissig K, Shiau JC, Vantaux A, Witkowski B, Phal S, Maher SP, Harty JT, Kyle DE, Kurup SP (2022) Cryopreservation of Plasmodium sporozoites. Pathogens 11:1487
pubmed: 36558821 pmcid: 9784981 doi: 10.3390/pathogens11121487
Clyde DF, Most H, McCarthy VC, Vanderberg JP (1973) Immunization of man against sporozite-induced falciparum malaria. Am J Med Sci 266:169–177
pubmed: 4583408 doi: 10.1097/00000441-197309000-00002
Coulibaly D, Kone AK, Traore K, Niangaly A, Kouriba B, Arama C, Zeguime A, Dolo A, Lyke KE, Plowe CV, Abebe Y, Potter GE, Kennedy JK, Galbiati SM, Nomicos E, Deye GA, Richie TL, James ER, Kc N, Sim BKL et al (2022) PfSPZ-CVac malaria vaccine demonstrates safety among malaria-experienced adults: a randomized, controlled phase 1 trial. EClinicalMedicine 52:101579
pubmed: 35928033 pmcid: 9343417 doi: 10.1016/j.eclinm.2022.101579
Cowman AF, Duraisingh MT (2001) An old enemy, a new battle plan. Perspective on combating drug-resistant malaria. EMBO Rep 2:77–79
pubmed: 11258713 pmcid: 1083828 doi: 10.1093/embo-reports/kve032
Datoo MS, Dicko A, Tinto H, Ouedraogo JB, Hamaluba M, Olotu A, Beaumont E, Ramos Lopez F, Natama HM, Weston S, Chemba M, Compaore YD, Issiaka D, Salou D, Some AM, Omenda S, Lawrie A, Bejon P, Rao H, Chandramohan D et al (2024) Safety and efficacy of malaria vaccine candidate R21/Matrix-M in African children: a multicentre, double-blind, randomised, phase 3 trial. Lancet 403:533–544
pubmed: 38310910 doi: 10.1016/S0140-6736(23)02511-4
Diawara H, Healy SA, Mwakingwe-Omari A, Issiaka D, Diallo A, Traore S, Soumbounou IH, Gaoussou S, Zaidi I, Mahamar A, Attaher O, Fried M, Wylie BJ, Mohan R, Doan V, Doritchamou JYA, Dolo A, Morrison RD, Wang J, Hu Z et al (2024) Safety and efficacy of PfSPZ Vaccine against malaria in healthy adults and women anticipating pregnancy in Mali: two randomised, double-blind, placebo-controlled, phase 1 and 2 trials. Lancet Infect Dis https://doi.org/10.1016/S1473-3099(24)00360-8
Druilhe P, Barnwell JW (2007) Pre-erythrocytic stage malaria vaccines: time for a change in path. Curr Opin Microbiol 10:371–378
pubmed: 17709281 doi: 10.1016/j.mib.2007.07.009
D’Souza J, Nderitu D (2021) Ethical considerations for introducing RTS,S/AS01 in countries with moderate to high Plasmodium falciparum malaria transmission. Lancet Glob Health 9:e1642–e1643
pubmed: 34798015 doi: 10.1016/S2214-109X(21)00498-8
Epstein JE, Paolino KM, Richie TL, Sedegah M, Singer A, Ruben AJ, Chakravarty S, Stafford A, Ruck RC, Eappen AG, Li T, Billingsley PF, Manoj A, Silva JC, Moser K, Nielsen R, Tosh D, Cicatelli S, Ganeshan H, Case J et al (2017) Protection against Plasmodium falciparum malaria by PfSPZ Vaccine. JCI Insight 2:e89154
pubmed: 28097230 pmcid: 5214067 doi: 10.1172/jci.insight.89154
Epstein JE, Tewari K, Lyke KE, Sim BK, Billingsley PF, Laurens MB, Gunasekera A, Chakravarty S, James ER, Sedegah M, Richman A, Velmurugan S, Reyes S, Li M, Tucker K, Ahumada A, Ruben AJ, Li T, Stafford R, Eappen AG et al (2011) Live attenuated malaria vaccine designed to protect through hepatic CD8(+) T cell immunity. Science 334:475–480
pubmed: 21903775 doi: 10.1126/science.1211548
Franke-Fayard B (2022) Development and clinical evaluation of genetically attenuated parasite that arrests late in the liver. Oral Presentation Tues, Nov 1, 10:45 AM, 2022 Annual Meeting of the American Society for Tropical Medicine and Hygiene
Franke-Fayard B, Marin-Mogollon C, Geurten FJA, Chevalley-Maurel S, Ramesar J, Kroeze H, Baalbergen E, Wessels E, Baron L, Soulard V, Martinson T, Aleshnick M, Huijs ATG, Subudhi AK, Miyazaki Y, Othman AS, Kolli SK, Lamers OAC, Roques M, Stanway RR et al (2022) Creation and preclinical evaluation of genetically attenuated malaria parasites arresting growth late in the liver. NPJ Vaccines 7:139
pubmed: 36333336 pmcid: 9636417 doi: 10.1038/s41541-022-00558-x
Gomez-Perez GP, Legarda A, Munoz J, Sim BK, Ballester MR, Dobano C, Moncunill G, Campo JJ, Cistero P, Jimenez A, Barrios D, Mordmuller B, Pardos J, Navarro M, Zita CJ, Nhamuave CA, Garcia-Basteiro AL, Sanz A, Aldea M, Manoj A et al (2015) Controlled human malaria infection by intramuscular and direct venous inoculation of cryopreserved Plasmodium falciparum sporozoites in malaria-naive volunteers: effect of injection volume and dose on infectivity rates. Malar J 14:306
pubmed: 26245196 pmcid: 4527105 doi: 10.1186/s12936-015-0817-x
Goswami D, Betz W, Locham NK, Parthiban C, Brager C, Schafer C, Camargo N, Nguyen T, Kennedy SY, Murphy SC, Vaughan AM, Kappe SH (2020) A replication-competent late liver stage-attenuated human malaria parasite. JCI Insight 5:1–19
doi: 10.1172/jci.insight.135589
Goswami D, Patel H, Betz W, Armstrong J, Camargo N, Patil A, Chakravarty S, Murphy SC, Sim BKL, Vaughan AM, Hoffman SL, Kappe SH (2024) A replication competent Plasmodium falciparum parasite completely attenuated by dual gene deletion. EMBO Mol Med 16:723–754
pubmed: 38514791 pmcid: 11018819 doi: 10.1038/s44321-024-00057-7
Hoffman SL, Billingsley PF, James E, Richman A, Loyevsky M, Li T, Chakravarty S, Gunasekera A, Chattopadhyay R, Li M, Stafford R, Ahumada A, Epstein JE, Sedegah M, Reyes S, Richie TL, Lyke KE, Edelman R, Laurens MB, Plowe CV et al (2010) Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Hum Vaccin 6:97–106
pubmed: 19946222 doi: 10.4161/hv.6.1.10396
James ER, Matheny S, Overby J, Sim BKL, Eappen AG, Li T, Li ML, Richie TL, Chakravarty S, Gunasekera A, Murshedkar T, Billingsley PF, Hoffman SL (2022) A first for human vaccinology: GMP compliant radiation attenuation of Plasmodium falciparum sporozoites for production of a vaccine against malaria. Front Immunol 13:851028
pubmed: 35242146 pmcid: 8886114 doi: 10.3389/fimmu.2022.851028
Jobe O, Donofrio G, Sun G, Liepinsh D, Schwenk R, Krzych U (2009) Immunization with radiation-attenuated Plasmodium berghei sporozoites induces liver cCD8alpha+DC that activate CD8+T cells against liver-stage malaria. PLoS ONE 4:e5075
pubmed: 19347042 pmcid: 2661143 doi: 10.1371/journal.pone.0005075
Jongo S, Church LWP, Milando F, Qassim M, Schindler T, Rashid M, Tumbo A, Nyaulingo G, Bakari BM, Athuman Mbaga T, Mohamed L, Kassimu K, Simon BS, Mpina M, Zaidi I, Duffy PE, Swanson 2nd PA, Seder R, Herman JD, Mendu M et al (2024) Safety and protective efficacy of PfSPZ vaccine administered to HIV-negative and -positive Tanzanian adults. J Clin Investig 134:e169060
pubmed: 38194272 pmcid: 10940097 doi: 10.1172/JCI169060
Jongo SA, Church LWP, Mtoro AT, Schindler T, Chakravarty S, Ruben AJ, Swanson PA, Kassim KR, Mpina M, Tumbo AM, Milando FA, Qassim M, Juma OA, Bakari BM, Simon B, James ER, Abebe Y, Kc N, Saverino E, Fink M et al (2020) Increase of dose associated with decrease in protection against controlled human malaria infection by PfSPZ vaccine in Tanzanian adults. Clin Infect Dis 71:2849–2857
pubmed: 31782768 doi: 10.1093/cid/ciz1152
Jongo SA, Shekalaghe SA, Church LWP, Ruben AJ, Schindler T, Zenklusen I, Rutishauser T, Rothen J, Tumbo A, Mkindi C, Mpina M, Mtoro AT, Ishizuka AS, Kassim KR, Milando FA, Qassim M, Juma OA, Mwakasungula S, Simon B, James ER et al (2018) Safety, immunogenicity, and protective efficacy against controlled human malaria infection of Plasmodium falciparum sporozoite vaccine in Tanzanian adults. Am J Trop Med Hyg 99:338–349
pubmed: 29943719 pmcid: 6090339 doi: 10.4269/ajtmh.17-1014
Juraska M, Early AM, Li L, Schaffner SF, Lievens M, Khorgade A, Simpkins B, Hejazi NS, Benkeser D, Wang Q, Mercer LD, Adjei S, Agbenyega T, Anderson S, Ansong D, Bii DK, Buabeng PBY, English S, Fitzgerald N, Grimsby J et al (2024) Genotypic analysis of RTS,S/AS01(E) malaria vaccine efficacy against parasite infection as a function of dosage regimen and baseline malaria infection status in children aged 5-17 months in Ghana and Kenya: a longitudinal phase 2b randomised controlled trial. Lancet Infect Dis 24(9):1025–1036
pubmed: 38723650 pmcid: 11339203 doi: 10.1016/S1473-3099(24)00179-8
Khan SM, Janse CJ, Kappe SH, Mikolajczak SA (2012) Genetic engineering of attenuated malaria parasites for vaccination. Curr Opin Biotechnol 23:908–916
pubmed: 22560204 doi: 10.1016/j.copbio.2012.04.003
Kublin JG, Mikolajczak SA, Sack BK, Fishbaugher ME, Seilie A, Shelton L, VonGoedert T, Firat M, Magee S, Fritzen E, Betz W, Kain HS, Dankwa DA, Steel RW, Vaughan AM, Noah Sather D, Murphy SC, Kappe SH (2017) Complete attenuation of genetically engineered Plasmodium falciparum sporozoites in human subjects. Sci Transl Med 9:1–11
doi: 10.1126/scitranslmed.aad9099
Kumari S, Sinha A (2023) Culture and transfection: two major bottlenecks in understanding Plasmodium vivax biology. Front Microbiol 14:1144453
pubmed: 37082177 pmcid: 10110902 doi: 10.3389/fmicb.2023.1144453
Laurens MB (2020) RTS,S/AS01 vaccine (Mosquirix): an overview. Hum Vaccin Immunother 16:480–489
pubmed: 31545128 doi: 10.1080/21645515.2019.1669415
Luke TC, Hoffman SL (2003) Rationale and plans for developing a non-replicating, metabolically active, radiation-attenuated Plasmodium falciparum sporozoite vaccine. J Exp Biol 206:3803–3808
pubmed: 14506215 doi: 10.1242/jeb.00644
Lyke KE, Singer A, Berry AA, Reyes S, Chakravarty S, James ER, Billingsley PF, Gunasekera A, Manoj A, Murshedkar T, Laurens MB, Church WP, Garver Baldwin LS, Sedegah M, Banania G, Ganeshan H, Guzman I, Reyes A, Wong M, Belmonte A et al (2021) Multidose priming and delayed boosting improve Plasmodium falciparum sporozoite vaccine efficacy against heterologous P. falciparum controlled human malaria infection. Clin Infect Dis 73:e2424–e2435
pubmed: 32920641 doi: 10.1093/cid/ciaa1294
Mendes AM, Machado M, Goncalves-Rosa N, Reuling IJ, Foquet L, Marques C, Salman AM, Yang ASP, Moser KA, Dwivedi A, Hermsen CC, Jimenez-Diaz B, Viera S, Santos JM, Albuquerque I, Bhatia SN, Bial J, Angulo-Barturen I, Silva JC, Leroux-Roels G et al (2018a) A Plasmodium berghei sporozoite-based vaccination platform against human malaria. NPJ Vaccines 3:33
pubmed: 30155278 pmcid: 6109154 doi: 10.1038/s41541-018-0068-2
Mendes AM, Reuling IJ, Andrade CM, Otto TD, Machado M, Teixeira F, Pissarra J, Goncalves-Rosa N, Bonaparte D, Sinfronio J, Sanders M, Janse CJ, Khan SM, Newbold CI, Berriman M, Lee CK, Wu Y, Ockenhouse CF, Sauerwein RW, Prudencio M (2018b) Pre-clinical evaluation of a P. berghei-based whole-sporozoite malaria vaccine candidate. NPJ Vaccines 3:54
pubmed: 30510775 pmcid: 6258718 doi: 10.1038/s41541-018-0091-3
Mendes AM, Scholzen A, Mueller A-K, Shahid M. Khan, Sauerwein RW, Prudêncio M (2017) Whole-sporozoite malaria vaccines. In: Mota MM, Rodriguez A (eds) Malaria. Springer, Cham, Switzerland 100–124
Miyazaki Y, Marin-Mogollon C, Imai T, Mendes AM, van der Laak R, Sturm A, Geurten FJA, Miyazaki S, Chevalley-Maurel S, Ramesar J, Kolli SK, Kroeze H, van Schuijlenburg R, Salman AM, Wilder BK, Reyes-Sandoval A, Dechering KJ, Prudencio M, Janse CJ, Khan SM et al (2020) Generation of a genetically modified chimeric Plasmodium falciparum parasite expressing Plasmodium vivax circumsporozoite protein for malaria vaccine development. Front Cell Infect Microbiol 10:591046
pubmed: 33392104 pmcid: 7773900 doi: 10.3389/fcimb.2020.591046
Moita D, Maia TG, Duarte M, Andrade CM, Albuquerque IS, Dwivedi A, Silva JC, Gonzalez-Ceron L, Janse CJ, Mendes AM, Prudencio M (2022a) A genetically modified Plasmodium berghei parasite as a surrogate for whole-sporozoite vaccination against P. vivax malaria. NPJ Vaccines 7:163
pubmed: 36526627 pmcid: 9755804 doi: 10.1038/s41541-022-00585-8
Moita D, Nunes-Cabaco H, Mendes AM, Prudencio M (2022b) A guide to investigating immune responses elicited by whole-sporozoite pre-erythrocytic vaccines against malaria. FEBS J 289:3335–3359
pubmed: 33993649 doi: 10.1111/febs.16016
Moita D, Nunes-Cabaco H, Rola C, Franke-Fayard B, Janse CJ, Mendes AM, Prudencio M (2023a) Variable long-term protection by radiation-, chemo-, and genetically-attenuated Plasmodium berghei sporozoite vaccines. Vaccine 41:7618–7625
pubmed: 38007342 doi: 10.1016/j.vaccine.2023.11.023
Moita D, Prudencio M (2024) A new malaria vaccination tool based on replication-competent Plasmodium falciparum parasites. EMBO Mol Med 16:667–669
pubmed: 38514792 pmcid: 11018615 doi: 10.1038/s44321-024-00056-8
Moita D, Rola C, Nunes-Cabaco H, Nogueira G, Maia TG, Othman AS, Franke-Fayard B, Janse CJ, Mendes AM, Prudencio M (2023b) The effect of dosage on the protective efficacy of whole-sporozoite formulations for immunization against malaria. NPJ Vaccines 8:182
pubmed: 37996533 pmcid: 10667361 doi: 10.1038/s41541-023-00778-9
Moorthy V, Binka F (2021) R21/Matrix-M: a second malaria vaccine? Lancet 397:1782–1783
pubmed: 33964224 doi: 10.1016/S0140-6736(21)01065-5
Mordmuller B, Sulyok Z, Sulyok M, Molnar Z, Lalremruata A, Calle CL, Bayon PG, Esen M, Gmeiner M, Held J, Heimann HL, Woldearegai TG, Ibanez J, Flugge J, Fendel R, Kreidenweiss A, Kc N, Murshedkar T, Chakravarty S, Riyahi P et al (2022) A PfSPZ vaccine immunization regimen equally protective against homologous and heterologous controlled human malaria infection. NPJ Vaccines 7:100
pubmed: 35999221 pmcid: 9396563 doi: 10.1038/s41541-022-00510-z
Mordmuller B, Surat G, Lagler H, Chakravarty S, Ishizuka AS, Lalremruata A, Gmeiner M, Campo JJ, Esen M, Ruben AJ, Held J, Calle CL, Mengue JB, Gebru T, Ibanez J, Sulyok M, James ER, Billingsley PF, Natasha KC, Manoj A et al (2017) Sterile protection against human malaria by chemoattenuated PfSPZ vaccine. Nature 542:445–449
pubmed: 28199305 pmcid: 10906480 doi: 10.1038/nature21060
Murphy SC, Deye GA, Sim BKL, Galbiati S, Kennedy JK, Cohen KW, Chakravarty S, Kc N, Abebe Y, James ER, Kublin JG, Hoffman SL, Richie TL, Jackson LA (2021) PfSPZ-CVac efficacy against malaria increases from 0% to 75% when administered in the absence of erythrocyte stage parasitemia: a randomized, placebo-controlled trial with controlled human malaria infection. PLoS Pathog 17:e1009594
pubmed: 34048504 pmcid: 8191919 doi: 10.1371/journal.ppat.1009594
Mwakingwe-Omari A, Healy SA, Lane J, Cook DM, Kalhori S, Wyatt C, Kolluri A, Marte-Salcedo O, Imeru A, Nason M, Ding LK, Decederfelt H, Duan J, Neal J, Raiten J, Lee G, Hume JCC, Jeon JE, Ikpeama I, Kc N et al (2021) Two chemoattenuated PfSPZ malaria vaccines induce sterile hepatic immunity. Nature 595:289–294
pubmed: 34194041 pmcid: 11127244 doi: 10.1038/s41586-021-03684-z
Neafsey DE, Juraska M, Bedford T, Benkeser D, Valim C, Griggs A, Lievens M, Abdulla S, Adjei S, Agbenyega T, Agnandji ST, Aide P, Anderson S, Ansong D, Aponte JJ, Asante KP, Bejon P, Birkett AJ, Bruls M, Connolly KM et al (2015) Genetic diversity and protective efficacy of the RTS,S/AS01 malaria vaccine. New Engl J Med 373:2025–2037
pubmed: 26488565 doi: 10.1056/NEJMoa1505819
Nunes-Cabaco H, Moita D, Prudencio M (2022) Five decades of clinical assessment of whole-sporozoite malaria vaccines. Front Immunol 13:977472
pubmed: 36159849 pmcid: 9493004 doi: 10.3389/fimmu.2022.977472
Nussenzweig RS, Vanderberg J, Most H, Orton C (1967) Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. Nature 216:160–162
pubmed: 6057225 doi: 10.1038/216160a0
Oneko M, Steinhardt LC, Yego R, Wiegand RE, Swanson PA, Kc N, Akach D, Sang T, Gutman JR, Nzuu EL, Dungani A, Kim Lee Sim B, Oloo PN, Otieno K, Bii DK, Billingsley PF, James ER, Kariuki S, Samuels AM, Jongo S et al (2021) Safety, immunogenicity and efficacy of PfSPZ Vaccine against malaria in infants in western Kenya: a double-blind, randomized, placebo-controlled phase 2 trial. Nat Med 27:1636–1645
pubmed: 34518679 doi: 10.1038/s41591-021-01470-y
Plotkin S (2014) History of vaccination. Proc Natl Acad Sci USA 111:12283–12287
pubmed: 25136134 pmcid: 4151719 doi: 10.1073/pnas.1400472111
Prudencio M, Costa JC (2020) Research funding after COVID-19. Nat Microbiol 5:986
pubmed: 32710091 doi: 10.1038/s41564-020-0768-z
Read AF, Baigent SJ, Powers C, Kgosana LB, Blackwell L, Smith LP, Kennedy DA, Walkden-Brown SW, Nair VK (2015) Imperfect vaccination can enhance the transmission of highly virulent pathogens. PLoS Biol 13:e1002198
pubmed: 26214839 pmcid: 4516275 doi: 10.1371/journal.pbio.1002198
Reuling IJ, Mendes AM, de Jong GM, Fabra-Garcia A, Nunes-Cabaco H, van Gemert GJ, Graumans W, Coffeng LE, de Vlas SJ, Yang ASP, Lee C, Wu Y, Birkett AJ, Ockenhouse CF, Koelewijn R, van Hellemond JJ, van Genderen PJJ, Sauerwein RW, Prudencio M (2020) An open-label phase 1/2a trial of a genetically modified rodent malaria parasite for immunization against Plasmodium falciparum malaria. Sci Transl Med 12:1–12
doi: 10.1126/scitranslmed.aay2578
Richie TL, Church LWP, Murshedkar T, Billingsley PF, James ER, Chen MC, Abebe Y, Natasha K, Chakravarty S, Dolberg D, Healy SA, Diawara H, Sissoko MS, Sagara I, Cook DM, Epstein JE, Mordmuller B, Kapulu M, Kreidenweiss A, Franke-Fayard B et al (2023) Sporozoite immunization: innovative translational science to support the fight against malaria. Expert Rev Vaccines 22:964–1007
pubmed: 37571809 pmcid: 10949369 doi: 10.1080/14760584.2023.2245890
Roestenberg M, Bijker EM, Sim BKL, Billingsley PF, James ER, Bastiaens GJH, Teirlinck AC, Scholzen A, Teelen K, Arens T, van der Ven A, Gunasekera A, Chakravarty S, Velmurugan S, Hermsen CC, Sauerwein RW, Hoffman SL (2013) Controlled human malaria infections by intradermal injection of cryopreserved Plasmodium falciparum sporozoites. Am J Trop Med Hyg 88:5–13
pubmed: 23149582 pmcid: 3541746 doi: 10.4269/ajtmh.2012.12-0613
Roestenberg M, Walk J, van der Boor SC, Langenberg MCC, Hoogerwerf MA, Janse JJ, Manurung M, Yap XZ, Garcia AF, Koopman JPR, Meij P, Wessels E, Teelen K, van Waardenburg YM, van de Vegte-Bolmer M, van Gemert GJ, Visser LG, van der Ven A, de Mast Q, Natasha KC et al (2020a) A double-blind, placebo-controlled phase 1/2a trial of the genetically attenuated malaria vaccine PfSPZ-GA1. Sci Transl Med 12:eaaz5629
pubmed: 32434847 doi: 10.1126/scitranslmed.aaz5629
Roestenberg M, Walk J, van der Boor SC, Langenberg MCC, Hoogerwerf MA, Janse JJ, Manurung M, Yap XZ, Garcia AF, Koopman JPR, Meij P, Wessels E, Teelen K, van Waardenburg YM, van de Vegte-Bolmer M, van Gemert GJ, Visser LG, van der Ven A, de Mast Q, Natasha KC et al (2020b) A double-blind, placebo-controlled phase 1/2a trial of the genetically attenuated malaria vaccine PfSPZ-GA1. Sci Transl Med 12:1–11
doi: 10.1126/scitranslmed.aaz5629
Ruben A, Awe A, Hoffman SL, Sim BK, Billingsley PF, Manoj A, Chakravarty S, Gunasekera A, Stafford R, Li M, James E (2013) Cryopreservation of Plasmodium falciparum sporozoites and Sanaria® PfSPZ vaccine. Cryobiology 67:1
doi: 10.1016/j.cryobiol.2013.09.163
Sahu T, Gehrke EJ, Flores-Garcia Y, Mlambo G, Romano JD, Coppens I (2021) Chemoprophylaxis vaccination with a Plasmodium liver stage autophagy mutant affords enhanced and long-lasting protection. NPJ Vaccines 6:98
pubmed: 34376691 pmcid: 8355287 doi: 10.1038/s41541-021-00360-1
Schmit N, Topazian HM, Natama HM, Bellamy D, Traore O, Some MA, Rouamba T, Tahita MC, Bonko MDA, Sourabie A, Sorgho H, Stockdale L, Provstgaard-Morys S, Aboagye J, Woods D, Rapi K, Datoo MS, Lopez FR, Charles GD, McCain K et al (2024) The public health impact and cost-effectiveness of the R21/Matrix-M malaria vaccine: a mathematical modelling study. Lancet Infect Dis 24(5):465–475
pubmed: 38342107 doi: 10.1016/S1473-3099(23)00816-2
Seder RA, Chang LJ, Enama ME, Zephir KL, Sarwar UN, Gordon IJ, Holman LA, James ER, Billingsley PF, Gunasekera A, Richman A, Chakravarty S, Manoj A, Velmurugan S, Li M, Ruben AJ, Li T, Eappen AG, Stafford RE, Plummer SH et al (2013) Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341:1359–1365
pubmed: 23929949 doi: 10.1126/science.1241800
Simon AK, Hollander GA, McMichael A (2015) Evolution of the immune system in humans from infancy to old age. Proc Biol Sci 282:20143085
pubmed: 26702035 pmcid: 4707740
Sirima SB, Ouedraogo A, Tiono AB, Kabore JM, Bougouma EC, Ouattara MS, Kargougou D, Diarra A, Henry N, Ouedraogo IN, Billingsley PF, Manoj A, Abebe Y, Kc N, Ruben A, Richie TL, James ER, Joshi S, Shrestha B, Strauss K et al (2022) A randomized controlled trial showing safety and efficacy of a whole sporozoite vaccine against endemic malaria. Sci Transl Med 14:eabj3776
pubmed: 36475905 pmcid: 10041996 doi: 10.1126/scitranslmed.abj3776
Sissoko MS, Healy SA, Katile A, Omaswa F, Zaidi I, Gabriel EE, Kamate B, Samake Y, Guindo MA, Dolo A, Niangaly A, Niare K, Zeguime A, Sissoko K, Diallo H, Thera I, Ding K, Fay MP, O’Connell EM, Nutman TB et al (2017) Safety and efficacy of PfSPZ vaccine against Plasmodium falciparum via direct venous inoculation in healthy malaria-exposed adults in Mali: a randomised, double-blind phase 1 trial. Lancet Infect Dis 17:498–509
pubmed: 28216244 pmcid: 6803168 doi: 10.1016/S1473-3099(17)30104-4
Sissoko MS, Healy SA, Katile A, Zaidi I, Hu Z, Kamate B, Samake Y, Sissoko K, Mwakingwe-Omari A, Lane J, Imeru A, Mohan R, Thera I, Guindo CO, Dolo A, Niare K, Koita F, Niangaly A, Rausch KM, Zeguime A et al (2022) Safety and efficacy of a three-dose regimen of Plasmodium falciparum sporozoite vaccine in adults during an intense malaria transmission season in Mali: a randomised, controlled phase 1 trial. Lancet Infect Dis 22:377–389
pubmed: 34801112 doi: 10.1016/S1473-3099(21)00332-7
Thomson-Luque R, Shaw Saliba K, Kocken CHM, Pasini EM (2017) A continuous, long-term Plasmodium vivax in vitro blood-stage culture: what are we missing? Trends Parasitol 33:921–924
pubmed: 28780020 doi: 10.1016/j.pt.2017.07.001
van Schaijk BC, Ploemen IH, Annoura T, Vos MW, Foquet L, van Gemert GJ, Chevalley-Maurel S, van de Vegte-Bolmer M, Sajid M, Franetich JF, Lorthiois A, Leroux-Roels G, Meuleman P, Hermsen CC, Mazier D, Hoffman SL, Janse CJ, Khan SM, Sauerwein RW (2014) A genetically attenuated malaria vaccine candidate based on P. falciparum b9/slarp gene-deficient sporozoites. eLife 3:e03582
pubmed: 25407681 pmcid: 4273440 doi: 10.7554/eLife.03582
Vanderberg JP (2009) Reflections on early malaria vaccine studies, the first successful human malaria vaccination, and beyond. Vaccine 27:2–9
pubmed: 18973784 doi: 10.1016/j.vaccine.2008.10.028
WHO (2024) Malaria vaccines (RTS,S and R21). WHO
Zavala F (2022) RTS,S: the first malaria vaccine. J Clin Investig 132:e156588
pubmed: 34981788 pmcid: 8718142 doi: 10.1172/JCI156588

Auteurs

Diana Moita (D)

Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa, Av. Prof. Egas Moniz, 1649-028, Lisboa, Portugal.

Miguel Prudêncio (M)

Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa, Av. Prof. Egas Moniz, 1649-028, Lisboa, Portugal. mprudencio@medicina.ulisboa.pt.

Classifications MeSH