Controlled Human Malaria Infection Studies in Africa-Past, Present, and Future.
Journal
Current topics in microbiology and immunology
ISSN: 0070-217X
Titre abrégé: Curr Top Microbiol Immunol
Pays: Germany
ID NLM: 0110513
Informations de publication
Date de publication:
16 Jun 2022
16 Jun 2022
Historique:
entrez:
15
6
2022
pubmed:
16
6
2022
medline:
16
6
2022
Statut:
aheadofprint
Résumé
Controlled human infection studies have contributed significantly to the understanding of pathogeneses and treatment of infectious diseases. In malaria, deliberately infecting humans with malaria parasites was used as a treatment for neurosyphilis in the early 1920s. More recently, controlled human malaria infection (CHMI) has become a valuable, cost-effective tool to fast-track the development and evaluation of new anti-malarial drugs and/or vaccines. CHMI studies have also been used to define host/parasite interactions and immunological correlates of protection. CHMI involves infecting a small number of healthy volunteers with malaria parasites, monitoring their parasitemia and providing anti-malarial treatment when a set threshold is reached. In this review we discuss the introduction, development, and challenges of modern-day Plasmodium falciparum CHMI studies conducted in Africa, and the impact of naturally acquired immunity on infectivity and vaccine efficacy. CHMIs have shown to be an invaluable tool particularly in accelerating malaria vaccine research. Although there are limitations of CHMI studies for estimating public health impacts and for regulatory purposes, their strength lies in proof-of-concept efficacy data at an early stage of development, providing a faster way to select vaccines for further development and providing valuable insights in understanding the mechanisms of immunity to malarial infection.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Wellcome Trust
ID : 203077
Pays : United Kingdom
Informations de copyright
© 2022. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Abuga KM, Jones‐Warner W, Hafalla JCR (2020) Immune responses to malaria pre‐erythrocytic stages: implications for vaccine development. Parasite Immunol 1–13. https://doi.org/10.1111/pim.12795
Achan J et al (2019) Serologic markers of previous malaria exposure and functional antibodies inhibiting parasite growth are associated with parasite kinetics following a Plasmodium falciparum controlled human infection. Clin Infect Dis 1–9. https://doi.org/10.1093/cid/ciz740
Adepoju P (2019) RTS, S malaria vaccine pilots in three African countries. Lancet 393:1685
Afolabi MO et al (2016) Safety and immunogenicity of ChAd63 and MVA ME-TRAP in West African children and infants. Mol Ther 24:1470–1477
Allison AC (1954) Protection afforded by sickle-cell trait against subtertian malarial infection. Br Med J 1:290–294
Andrews L et al (2005) Quantitative real-time polymerase chain reaction for malaria diagnosis and its use in malaria vaccine clinical trials. Am J Trop Med Hyg 73:191–198
Arévalo-Herrera M et al (2016) Protective efficacy of Plasmodium vivax radiation-attenuated sporozoites in colombian volunteers: a randomized controlled trial. PLoS Negl Trop Dis 10
Auburn S, Cheng Q, Marfurt J, Price RN (2021) The changing epidemiology of Plasmodium vivax: Insights from conventional and novel surveillance tools. PLoS Med 18
Austin SC, Stolley PD, Lasky T (1992) The history of malariotherapy for neurosyphilis: modern parallels. JAMA J Am Med Assoc. https://doi.org/10.1001/jama.1992.03490040092031
doi: 10.1001/jama.1992.03490040092031
Baird JK, Schwartz E, Hoffman SL (2007) Prevention and treatment of vivax malaria. Curr Infect Dis Rep 9:39–46
Ballou WR et al (1987) Safety and efficacy of a recombinant DNA Plasmodium falciparum sporozoite vaccine. Lancet
Bastiaens GJH et al (2016) Safety, immunogenicity, and protective efficacy of intradermal immunization with aseptic, purified, cryopreserved plasmodium falciparum sporozoites in volunteers under chloroquine prophylaxis: a randomized controlled trial. Am J Trop Med Hyg 94:663–673
Battle KE et al (2019) Mapping the global endemicity and clinical burden of Plasmodium vivax, 2000–17: a spatial and temporal modelling study. Lancet 394:332–343
Bejon P et al (2005) Calculation of liver-to-blood inocula, parasite growth rates, and preerythrocytic vaccine efficacy, from serial quantitative polymerase chain reaction studies of volunteers challenged with malaria sporozoites. J Infect Dis 191:619–626
Bejon P et al (2006) Thick blood film examination for Plasmodium falciparum malaria has reduced sensitivity and underestimates parasite density. Malar J 5:5–8
Bennett JW et al (2016) Phase 1/2a trial of Plasmodium vivax malaria vaccine candidate VMP001/AS01B in malaria-naive adults: safety, immunogenicity, and efficacy. PLoS Negl Trop Dis. https://doi.org/10.1371/journal.pntd.0004423
doi: 10.1371/journal.pntd.0004423
Billingsley P et al (2014) Controlled human malaria infections using aseptic, purified cryopreserved Plasmodium falciparum sporozoites administered by needle and syringe. Malar J 13
Bray RS, Gunders AE, Burgess RW, Freeman JB, Etzel E, Guttuso C, Colussa B (1962) The inoculation of semi-immune Africans with sporozoites of Laverania falcipara (Plasmodium falciparum) in liberia. Riv. Malariol 41:199–210
Burkot TR, Williams JL, Schneider I (1984) Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Trans R Soc Trop Med Hyg 78:339–341
Casper C, Crane H, Menon M, Money D (2017) HIV/AIDS comorbidities: impact on cancer, noncommunicable diseases, and reproductive health. Dis Control Priorities, Third Ed. (Volume 6) Major Infect Dis 45–66. https://doi.org/10.1596/978-1-4648-0524-0_ch3
Cheng Q et al (1997) Measurement of Plasmodium falciparum growth rates in vivo: a test of malaria vaccines. Am J Trop Med Hyg 57:495–500
Chuang I et al (2013) DNA prime/adenovirus boost malaria vaccine encoding P. falciparum CSP and AMA1 induces sterile protection associated with cell-mediated immunity. PLoS One 8
Chulay JD et al (1986) Malaria transmitted to humans by mosquitoes infected from cultured Plasmodium falciparum. Am J Trop Med Hyg 35:66–68
Clyde DF, McCarthy VC, Miller RM, Hornick R (1973) Specificity of protection of man immunized against sporozoite‐induced falciparum malaria. Am J Med Sci
Cohen S, McGregor I, Carrington SP (1961) Gamma-globulin and aquired immunity to human malaria. Nature
Collins WE, Jeffery GM (1999) Parasitologic and clinical immunity during primary infection. Am J Trop Med Hyg 61:4–19
Collins KA et al (2020) A Plasmodium vivax experimental human infection model for evaluating efficacy of interventions. J Clin Invest 130:2920–2927
Cooper MM, Loiseau C, McCarthy JS, Doolan DL (2019) Human challenge models: tools to accelerate the development of malaria vaccines. Expert Rev Vaccines 18:241–251
Cummings JF et al (2010) Recombinant liver stage antigen-1 (LSA-1) formulated with AS01 or AS02 is safe, elicits high titer antibody and induces IFN-γ/IL-2 CD4+ T cells but does not protect against experimental Plasmodium falciparum infection. Vaccine 28:5135–5144
Dejon-Agobe JC et al (2019) Controlled human malaria infection of healthy adults with lifelong malaria exposure to assess safety, immunogenicity, and efficacy of the asexual blood stage malaria vaccine candidate GMZ2. Clin Infect Dis 69:1377–1384
Doolan DL, Doban C, Baird JK (2009) Acquired immunity to malaria. Clin Microbiol Rev 22:13–36
Douglas AD et al (2013) Comparison of modeling methods to determine liver-to-blood inocula and parasite multiplication rates during controlled human malaria infection. J Infect Dis 208:340–345
Draper SJ et al (2018) Review malaria vaccines: recent advances and new horizons. Cell Host Microbe 24:43–56
Duffy PE, Patrick Gorres J (2020) Malaria vaccines since 2000: progress, priorities, products. npj Vaccines 5:1–9
Dunachie SJ et al (2006) A DNA prime-modified vaccinia virus Ankara boost vaccine encoding thrombospondin-related adhesion protein but not circumsporozoite protein partially protects healthy malaria-naive adults against Plasmodium falciparum sporozoite challenge. Infect Immun 74:5933–5942
Duncan CJA et al (2011) Impact on malaria parasite multiplication rates in infected volunteers of the protein-in-adjuvant vaccine AMA1-C1/alhydrogel+CPG 7909. PLoS One 6
Duncan CJA, Draper SJ (2012) Review: controlled human blood stage malaria infection: current status and potential applications. Am J Trop Med Hyg 86:561–565
Epstein JE (2013) Taking a bite out of malaria: controlled human malaria infection by needle and syringe. Am J Trop Med Hyg 88:3–4
Epstein JE et al (2007) Safety and clinical outcome of experimental challenge of human volunteers with Plasmodium falciparum—infected mosquitoes: an update. J Infect Dis 196:145–154
Epstein JE et al (2017) Protection against Plasmodium falciparum malaria by PfSPZ Vaccine. JCI Insight. https://doi.org/10.1172/jci.insight.89154
doi: 10.1172/jci.insight.89154
Friedman-Klabanoff DAJ et al (2019) The controlled human malaria infection experience at the University of Maryland. Am J Trop Med Hyg 100:556–565
Goh YS, McGuire D, Rénia L (2019) Vaccination with sporozoites: models and correlates of protection. Front Immunol 10:1227
Gómez-Pérez GP et al (2015) Controlled human malaria infection by intramuscular and direct venous inoculation of cryopreserved Plasmodium falciparum sporozoites in malaria-naïve volunteers: effect of injection volume and dose on infectivity rates. Malar J 14:1–13
Griffin P et al (2016) Safety and reproducibility of a clinical trial system using induced blood stage Plasmodium vivax infection and its potential as a model to evaluate malaria transmission. PLoS Negl. Trop. Dis 10
Healy SA et al (2017) Plasmodium falciparum controlled human malaria infection in malaria exposed volunteers: can it inform malaria vaccine trials in the field. Am J Trop Med Hyg 97 (5 Supp) 368
Henderson DA (1987) Principles and lessons from the smallpox eradication programme. Bull World Health Organ 65:535–546
Herrera S et al (2009) Case report: successful sporozoite challenge model in human volunteers with Plasmodium vivax strain derived from human donors. Am J Trop Med Hyg 81:740–746
Herrera S et al (2011) Consistent safety and infectivity in sporozoite challenge model of Plasmodium vivax in malaria-naive human volunteers. Am J Trop Med Hyg 84:4–11
Herrington DA et al (1990) Human studies with synthetic peptide sporozoite vaccine (NANP ) 3-TT and immunization with irradiated sporozoites. Bull World Health Organ 37:33–37
Hill AVS (2006) Pre-erythrocytic malaria vaccines: towards greater efficacy. Nat Rev Immunol 6:21–32
Hodgson SH et al (2014) Evaluating controlled human malaria infection in Kenyan adults with varying degrees of prior exposure to Plasmodium falciparum using sporozoites administered by intramuscular injection. Front Microbiol 5:1–10
Hodgson SH et al (2016) Changes in serological immunology measures in UK and Kenyan adults post-controlled human malaria infection. Front Microbiol 7
Hodgson SH et al (2015) Evaluation of the efficacy of ChAd63-MVA vectored vaccines expressing circumsporozoite protein and ME-TRAP against controlled human malaria infection in malaria-naive individuals 211
Hoffman SL et al (2002) Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J Infect Dis 185:1155–1164
Ishizuka AS et al (2016) Protection against malaria at 1 year and immune correlates following PfSPZ vaccination. Nat Med. https://doi.org/10.1038/nm.4110
doi: 10.1038/nm.4110
John J (2009) Role of injectable and oral polio vaccines in polio eradication. Expert Rev Vaccines 8:5–8
Jongo SA 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
Jongo SA et al (2019a) Increase of dose associated with decrease in protection against controlled human malaria infection by PfSPZ vaccine in Tanzanian adults. Clin Infect Dis. https://doi.org/10.1093/cid/ciz1152
doi: 10.1093/cid/ciz1152
Jongo SA et al (2019b) Safety and differential antibody and T-cell responses to the Plasmodium falciparum sporozoite malaria vaccine, PfSPZ vaccine, by age in Tanzanian adults, adolescents, children, and infants. Am J Trop Med Hyg 100:1433–1444
Jongo SA 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
Jongo SA et al (2021) Immunogenicity and protective efficacy of radiation-attenuated and chemo-attenuated PfSPZ vaccines in equatoguinean adults. Am J Trop Med Hyg 104:283–293
Kapulu MC, Njuguna P, Hamaluba MM (2018) Controlled human malaria infection in semi-immune Kenyan adults (CHMI-SIKA): a study protocol to investigate in vivo Plasmodium falciparum malaria parasite growth in the context of pre-existing immunity. Wellcome Open Res 3:155
Kapulu MC et al (2020) Naturally acquired immunity among Kenyan adults suppresses the West African P. falciparum NF54 strain in controlled human malaria infection (CHMI). medRxiv 26
Kester KE et al (2007) A phase I/IIa safety, immunogenicity, and efficacy bridging randomized study of a two-dose regimen of liquid and lyophilized formulations of the candidate malaria vaccine RTS, S/AS02A in malaria-naïve adults. Vaccine 25:5359–5366
Kester KE et al (2008) Phase 2a trial of 0, 1, and 3 month and 0, 7, and 28 day immunization schedules of malaria vaccine RTS, S/AS02 in malaria-naïve adults at the Walter Reed Army Institute of Research. Vaccine 26:2191–2202
Kester KE et al (2009) 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 200:337–346
Lawrence G et al (2000) Effect of vaccination with 3 recombinant asexual-stage malaria antigens on initial growth rates of Plasmodium falciparum in non-immune volunteers. Vaccine 18:1925–1931
Lell B et al (2018) Impact of sickle cell trait and naturally acquired immunity on uncomplicated malaria after controlled human malaria infection in adults in Gabon. Am J Trop Med Hyg 98:508–515
Lopez-perez M et al (2016) Protective efficacy of Plasmodium vivax radiation-attenuated sporozoites in Colombian volunteers: a randomized controlled trial. PLoS Negl Trop Dis 0–19. https://doi.org/10.1371/journal.pntd.0005070 .
Lyke KE et al (2015) Optimizing intradermal administration of cryopreserved Plasmodium falciparum sporozoites in controlled human malaria infection. Am J Trop Med Hyg. https://doi.org/10.4269/ajtmh.15-0341
doi: 10.4269/ajtmh.15-0341
Lyke KE et al (2017) Attenuated PfSPZ Vaccine induces strain-transcending T cells and durable protection against heterologous controlled human malaria infection. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.1615324114
doi: 10.1073/pnas.1615324114
Lyke KE 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
Marques-Da-silva C, Peissig K, Kurup SP (2020) Pre-erythrocytic vaccines against malaria. Vaccines 8:1–16
McCarthy JS et al (2011) A pilot randomised trial of induced blood-stage Plasmodium falciparum infections in healthy volunteers for testing efficacy of new antimalarial drugs. PLoS ONE 6:6–13
McCarthy JS et al (2013) Experimentally induced blood-stage plasmodium vivax infection in healthy volunteers. J Infect Dis 208:1688–1694
Mcconkey SJ et al (2003) Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in human. Nat Med 9:729–735
Miller LH, Baruch DI, Marsh K, Doumbo OK (2002) The pathogenic basis of malaria. Nature 415:673–679
Minassian AM et al (2021) Reduced blood-stage malaria growth and immune correlates in humans following RH5 vaccination. CelPress 2:701-719.e19
Moon JE et al (2020) A phase IIa controlled human malaria infection and immunogenicity study of RTS, S/AS01E and RTS, S/AS01B delayed fractional dose regimens in malaria-naive adults. J Infect Dis 222:1681–1691
Mordmüller B et al (2015) Direct venous inoculation of Plasmodium falciparum sporozoites for controlled human malaria infection: a dose-finding trial in two centres. Malar J 14:0–10
Mordmüller B et al (2017) Sterile protection against human malaria by chemo attenuated PfSPZ vaccine. Nature 542:445–449
Moser KA et al (2020) Strains used in whole organism Plasmodium falciparum vaccine trials differ in genome structure, sequence, and immunogenic potential. Genome Med 12:1–17
Nahrendorf W, Scholzen A, Sauerwein RW, Langhorne J (2015) Cross-stage immunity for malaria vaccine development. Vaccine 33:7513–7517
Nouatin O et al (2021) Exploratory analysis of the effect of helminth infection on the immunogenicity and efficacy of the asexual blood-stage malaria vaccine candidate gmz2. PLoS Negl Trop Dis 15:1–18
Nussenzweig R, Vanderberg J, Most H (1969) Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. IV. Dose response, specificity and humoral immunity. Mil Med 134:1176–1182
Obiero JM et al (2015) Impact of malaria preexposure on antiparasite cellular and humoral immune responses after controlled human malaria infection. Infect Immun 83:2185–2196
Ockenhouse CF et al (1998) Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a poxvectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. J Infect Dis 177:1664–1673
Ockenhouse CF et al (2015) Ad35.CS.01—RTS,S/AS01 heterologous prime boost vaccine efficacy against sporozoite challenge in healthy malaria-naïve adults. PLoS One 10:1–14
Patarroyo ME, Amador R, Clavijo P, Moreno A, Guzman F, Romero P … Trujillo G (1988) A synthetic vaccine protects humans against challenge with asexual blood stages of Plasmodium falciparum malaria. Nature
Payne RO, Griffin PM, McCarthy JS, Draper SJ (2017) Plasmodium vivax controlled human malaria infection—progress and prospects. Trends Parasitol 33:141–150
Payne RO et al (2016) Demonstration of the blood-stage Plasmodium falciparum controlled human malaria infection model to assess efficacy of the P. falciparum apical membrane antigen. J Infect Dis 213:1743–1751
Pombo DJ et al (2002) Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum. Lancet 360:610–617
Ponnudurai T, Leeuwenberg DEM, Meuwissen JHE (1981) Chloriquine sensitivity of isolates of Plasmodium falciparum adapted to in vitro culture. Trop Geogr Med
Rampling T et al (2018) Safety and efficacy of novel malaria vaccine regimens of RTS,S/AS01B alone, or with concomitant ChAd63-MVA-vectored vaccines expressing ME-TRAP. npj Vaccines 3:1–9
Regules JA et al (2016) Fractional third and fourth dose of RTS, S / AS01 malaria candidate vaccine: a phase 2a controlled human malaria parasite infection and immunogenicity study 214
Richie TL et al (2015) Progress with Plasmodium falciparum sporozoite (PfSPZ)-based malaria vaccines. Vaccine 33:7452–7461
Richie TL et al (2015) Progress with P. falciparum sporozoite based malaria vaccines. Vaccine 33:7452–7461
Roestenberg M et al (2009b) Protection against a malaria challenge by sporozoite inoculation. N Engl J Med 361:468–477
Roestenberg M et al (2012) Comparison of clinical and parasitological data from controlled human malaria infection trials. PLoS ONE 7:1–8
Roestenberg M et al (2013) Controlled human malaria infections by intradermal injection of cryopreserved Plasmodium falciparum sporozoites. Am J Trop Med Hyg 88:5–13
Roestenberg M et al (2017) The frontline of controlled human malaria infections: a report from the controlled human infection models workshop in Leiden University Medical Centre 5 may 2016. Vaccine 35:7065–7069
Roestenberg M, Mccall M, Hopman J (2009a) Protection against a malaria challenge by sporozoite inoculation protection against a malaria challenge by sporozoite inoculation https://doi.org/10.1056/NEJMoa0805832
Sanaria (2012) Malaria eradication through vaccination. https://sanaria.com/
Sanderson F et al (2008) Blood-stage challenge for malaria vaccine efficacy trials: a pilot study with discussion of safety and potential value. Am J Trop Med Hyg 78:878–883
Sauerwein RW, Roestenberg M, Moorthy VS (2011) Experimental human challenge infections can accelerate clinical malaria vaccine development. Nat Rev Immunol 11:57–64
Schats R et al (2015) Heterologous protection against malaria after immunization with Plasmodium falciparum sporozoites. PLoS ONE 10:1–10
Seder RA et al (2013) Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science (80) 341:1359–1365
Sheehy SH et al (2012) ChAd63-MVA-vectored blood-stage Malaria vaccines targeting MSP1 and AMA1: assessment of efficacy against mosquito bite challenge in humans. Mol Ther 20:2355–2368
Sheehy SH et al (2013) Optimising controlled human malaria infection studies using cryopreserved P. falciparum parasites administered by needle and syringe. PLoS One 8
Shekalaghe S et al (2014) Controlled human malaria infection of Tanzanians by intradermal injection of aseptic, purified, cryopreserved plasmodium falciparum sporozoites. Am J Trop Med Hyg 91:471–480
Shekalaghe S et al (2014) Assessing efficacy of the PfSPZ vaccine by controlled human malaria infection in Tanzania. Am J Trop Med Hyg 91:203
Sinnis P, Zavala F (2012) The skin: where malaria infection and the host immune response begin. Semin Immunopathol 34:787–792
Sissoko MS 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 176:139–148
Sissoko MS et al (2021) 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. https://doi.org/10.1016/s1473-3099(21)00332-7
doi: 10.1016/s1473-3099(21)00332-7
Spence PJ, Brugat T, Langhorne J (2015) Mosquitoes reset malaria parasites. PLoS Pathog 11
Spring MD et al (2009) Phase 1/2a study of the malaria vaccine candidate apical membrane antigen-1 (AMA-l) administered in adjuvant system AS01B or AS02A. PLoS One 4
Spring M, Polhemus M, Ockenhouse C (2014) Controlled human malaria infection. J Infect Dis 209
Stanisic DI, McCall MBB (2021) Correlates of malaria vaccine efficacy. Expert Rev Vaccines 20:143–161
Stanisic DI et al (2015) Development of cultured Plasmodium falciparum blood-stage malaria cell banks for early phase in vivo clinical trial assessment of anti-malaria drugs and vaccines. Malar J 14:1–10
Stanisic DI, McCarthy JS, Good MF (2018) Controlled human malaria infection: applications, advances and challenges. Infect Immun 86:1–17
Steinhardt LC et al (2019) Safety, tolerability, and immunogenicity of Plasmodium falciparum sporozoite vaccine administered by direct venous inoculation to infants and young children: findings from an age de-escalation, dose-escalation, double-blind, randomized controlled study in Western Kenya. Clin Infect Dis 1–9. https://doi.org/10.1093/cid/ciz925
Stoute JA et al (1997) A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. N Engl J Med 336:86–91
Sulyok Z et al (2021) Heterologous protection against malaria by a simple chemoattenuated PfSPZ vaccine regimen in a randomized trial. Nat Commun 12
Tamminga C et al (2013) Human adenovirus 5-vectored Plasmodium falciparum NMRC-M3V-Ad-PfCA vaccine encoding CSP and AMA1 is safe, well-tolerated and immunogenic but does not protect against controlled human malaria infection. Hum Vaccines Immunother 9:2165–2177
Teirlinck AC et al (2013) NF135.C10: a new Plasmodium falciparum clone for controlled human malaria infections. J Infect Dis 207:656–660
Urbano V et al (2018) Safety, tolerability, immunogenicity and efficacy of PfSPZ vaccine versus PfSPZ—CVac in equatoguinean young adults 14–15
Vanderberg J (2007) Assessment of antibody protection against malaria sporozoites must be done by mosquito injection of sporozoites. Am J Pathol. https://doi.org/10.2353/ajpath.2007.070661
doi: 10.2353/ajpath.2007.070661
Verhage DF et al (2005) Clinical outcome of experimental human malaria induced by Plasmodium falciparum—infected mosquitoes. Neth J Med 63:52–58
Walk J et al (2017) Modest heterologous protection after Plasmodium falciparum sporozoite immunization: a double-blind randomized controlled clinical trial. BMC Med 15:1–12
Webster DP et al (2005) Enhanced T cell-mediated protection against malaria in human challenges by using the recombinant poxviruses FP9 and modified vaccinia virus Ankara. Proc Natl Acad Sci U S A 102:4836–4841
WHO (2010) Global report on antimalarial drug efficacy and drug resistance: 2000–2010 59:243–258
WHO (2018) Global report on insecticide resistance in malaria vectors: 2010–2016
WHO (2020) World Malaria report 2020. https://doi.org/10.1002/(SICI)1096-8628(19971128)73:1<1::AID-AJMG1>3.0.CO;2-Y
Woodford J et al (2020) An experimental human blood-stage model for studying Plasmodium malariae infection. J Infect Dis 221:948–955
Yap XZ, McCall MBB, Sauerwein RW (2020) Fast and fierce versus slow and smooth: heterogeneity in immune responses to Plasmodium in the controlled human malaria infection model. Immunol Rev 293:253–269
Zhang Y, Asante KSO, Jung A (1986) Stage-dependent inhibition of chloroquine on Plasmodium falciparum in vitro. J Parasitol 72:830–836