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Review

Challenges of assessing the clinical efficacy of asexual blood-stage Plasmodium falciparum malaria vaccines

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Pages 1831-1840 | Received 26 Feb 2013, Accepted 13 Jun 2013, Published online: 18 Jun 2013

References

  • WHO.. World Malaria Report. 2011.
  • Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012; 379:413 - 31; http://dx.doi.org/10.1016/S0140-6736(12)60034-8; PMID: 22305225
  • Das P, Horton R. Malaria elimination: worthy, challenging, and just possible. Lancet 2010; 376:1515 - 7; http://dx.doi.org/10.1016/S0140-6736(10)61551-6; PMID: 21035845
  • Roberts L, Enserink M. Malaria. Did they really say ... eradication?. Science 2007; 318:1544 - 5; http://dx.doi.org/10.1126/science.318.5856.1544; PMID: 18063766
  • WHO.. Malaria Vaccine Technology Roadmap2006.
  • WHO. Malaria Vaccine Technology Roadmap: Update of Vision and Strategic Goal Underway. 2012.
  • Greenwood B, Targett G. Do we still need a malaria vaccine?. Parasite Immunol 2009; 31:582 - 6; http://dx.doi.org/10.1111/j.1365-3024.2009.01140.x; PMID: 19691561
  • Agnandji ST, Lell B, Fernandes JF, Abossolo BP, Methogo BG, Kabwende AL, et al, RTS,S Clinical Trials Partnership. A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. N Engl J Med 2012; 367:2284 - 95; http://dx.doi.org/10.1056/NEJMoa1208394; PMID: 23136909
  • Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol 2006; 22:424 - 30; http://dx.doi.org/10.1016/j.pt.2006.07.001; PMID: 16846756
  • Bonnet S, Gouagna LC, Paul RE, Safeukui I, Meunier JY, Boudin C. Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Trans R Soc Trop Med Hyg 2003; 97:53 - 9; http://dx.doi.org/10.1016/S0035-9203(03)90022-8; PMID: 12886806
  • Ross A, Killeen G, Smith T. Relationships between host infectivity to mosquitoes and asexual parasite density in Plasmodium falciparum. Am J Trop Med Hyg 2006; 75:Suppl 32 - 7; PMID: 16931813
  • Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, et al. Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet 2008; 372:1545 - 54; http://dx.doi.org/10.1016/S0140-6736(08)61654-2; PMID: 18984187
  • O’Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, et al. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 2008; 372:1555 - 62; http://dx.doi.org/10.1016/S0140-6736(08)61655-4; PMID: 18984188
  • Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS One 2010; 5:e8988; http://dx.doi.org/10.1371/journal.pone.0008988; PMID: 20126547
  • Plowe CV, Alonso P, Hoffman SL. The potential role of vaccines in the elimination of falciparum malaria and the eventual eradication of malaria. J Infect Dis 2009; 200:1646 - 9; http://dx.doi.org/10.1086/646613; PMID: 19877844
  • Goodman AL, Draper SJ. Blood-stage malaria vaccines - recent progress and future challenges. Ann Trop Med Parasitol 2010; 104:189 - 211; http://dx.doi.org/10.1179/136485910X12647085215534; PMID: 20507694
  • Crompton PD, Pierce SK, Miller LH. Advances and challenges in malaria vaccine development. J Clin Invest 2010; 120:4168 - 78; http://dx.doi.org/10.1172/JCI44423; PMID: 21123952
  • Moorthy VS, Diggs C, Ferro S, Good MF, Herrera S, Hill AV, et al. Report of a consultation on the optimization of clinical challenge trials for evaluation of candidate blood stage malaria vaccines, 18-19 March 2009, Bethesda, MD, USA. Vaccine 2009; 27:5719 - 25; http://dx.doi.org/10.1016/j.vaccine.2009.07.049; PMID: 19654061
  • Moll K, Pettersson F, Vogt AM, Jonsson C, Rasti N, Ahuja S, et al. Generation of cross-protective antibodies against Plasmodium falciparum sequestration by immunization with an erythrocyte membrane protein 1-duffy binding-like 1 alpha domain. Infect Immun 2007; 75:211 - 9; http://dx.doi.org/10.1128/IAI.00749-06; PMID: 17074852
  • Ghumra A, Semblat JP, Ataide R, Kifude C, Adams Y, Claessens A, et al. Induction of strain-transcending antibodies against Group A PfEMP1 surface antigens from virulent malaria parasites. PLoS Pathog 2012; 8:e1002665; http://dx.doi.org/10.1371/journal.ppat.1002665; PMID: 22532802
  • Sheehy SH, Duncan CJ, Elias SC, Choudhary P, Biswas S, Halstead FD, et al. ChAd63-MVA-vectored blood-stage malaria vaccines targeting MSP1 and AMA1: assessment of efficacy against mosquito bite challenge in humans. Mol Ther 2012; 20:2355 - 68; http://dx.doi.org/10.1038/mt.2012.223; PMID: 23089736
  • Pinzon-Charry A, Good MF. Malaria vaccines: the case for a whole-organism approach. Expert Opin Biol Ther 2008; 8:441 - 8; http://dx.doi.org/10.1517/14712598.8.4.441; PMID: 18352848
  • Pombo DJ, Lawrence G, Hirunpetcharat C, Rzepczyk C, Bryden M, Cloonan N, et al. Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum. Lancet 2002; 360:610 - 7; http://dx.doi.org/10.1016/S0140-6736(02)09784-2; PMID: 12241933
  • McCarthy JS, Good MF. Whole parasite blood stage malaria vaccines: a convergence of evidence. Hum Vaccin 2010; 6:114 - 23; http://dx.doi.org/10.4161/hv.6.1.10394; PMID: 19946204
  • Ellis RD, Sagara I, Doumbo O, Wu Y. Blood stage vaccines for Plasmodium falciparum: current status and the way forward. Hum Vaccin 2010; 6:627 - 34; http://dx.doi.org/10.4161/hv.6.8.11446; PMID: 20519960
  • Craig AG, Grau GE, Janse C, Kazura JW, Milner D, Barnwell JW, et al, participants of the Hinxton Retreat meeting on Animal Models for Research on Severe Malaria. The role of animal models for research on severe malaria. PLoS Pathog 2012; 8:e1002401; http://dx.doi.org/10.1371/journal.ppat.1002401; PMID: 22319438
  • Stowers AW, Miller LH. Are trials in New World monkeys on the critical path for blood-stage malaria vaccine development?. Trends Parasitol 2001; 17:415 - 9; http://dx.doi.org/10.1016/S1471-4922(01)02011-6; PMID: 11530352
  • Langhorne J, Quin SJ, Sanni LA. Mouse models of blood-stage malaria infections: immune responses and cytokines involved in protection and pathology. Chem Immunol 2002; 80:204 - 28; http://dx.doi.org/10.1159/000058845; PMID: 12058640
  • Dutta S, Sullivan JS, Grady KK, Haynes JD, Komisar J, Batchelor AH, et al. High antibody titer against apical membrane antigen-1 is required to protect against malaria in the Aotus model. PLoS One 2009; 4:e8138; http://dx.doi.org/10.1371/journal.pone.0008138; PMID: 19997632
  • Singh S, Miura K, Zhou H, Muratova O, Keegan B, Miles A, et al. Immunity to recombinant plasmodium falciparum merozoite surface protein 1 (MSP1): protection in Aotus nancymai monkeys strongly correlates with anti-MSP1 antibody titer and in vitro parasite-inhibitory activity. Infect Immun 2006; 74:4573 - 80; http://dx.doi.org/10.1128/IAI.01679-05; PMID: 16861644
  • Hisaeda H, Saul A, Reece JJ, Kennedy MC, Long CA, Miller LH, et al. Merozoite surface protein 3 and protection against malaria in Aotus nancymai monkeys. J Infect Dis 2002; 185:657 - 64; http://dx.doi.org/10.1086/339187; PMID: 11865423
  • Biswas S, Spencer AJ, Forbes EK, Gilbert SC, Holder AA, Hill AV, et al. Recombinant viral-vectored vaccines expressing Plasmodium chabaudi AS apical membrane antigen 1: mechanisms of vaccine-induced blood-stage protection. J Immunol 2012; 188:5041 - 53; http://dx.doi.org/10.4049/jimmunol.1101106; PMID: 22504652
  • Draper SJ, Goodman AL, Biswas S, Forbes EK, Moore AC, Gilbert SC, et al. Recombinant viral vaccines expressing merozoite surface protein-1 induce antibody- and T cell-mediated multistage protection against malaria. Cell Host Microbe 2009; 5:95 - 105; http://dx.doi.org/10.1016/j.chom.2008.12.004; PMID: 19154991
  • Fowkes FJ, Richards JS, Simpson JA, Beeson JG. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: A systematic review and meta-analysis. PLoS Med 2010; 7:e1000218; http://dx.doi.org/10.1371/journal.pmed.1000218; PMID: 20098724
  • Sirima SB, Cousens S, Druilhe P. Protection against malaria by MSP3 candidate vaccine. N Engl J Med 2011; 365:1062 - 4; http://dx.doi.org/10.1056/NEJMc1100670; PMID: 21916656
  • Thompson FM, Porter DW, Okitsu SL, Westerfeld N, Vogel D, Todryk S, et al. Evidence of blood stage efficacy with a virosomal malaria vaccine in a phase IIa clinical trial. PLoS One 2008; 3:e1493; http://dx.doi.org/10.1371/journal.pone.0001493; PMID: 18231580
  • Genton B, Betuela I, Felger I, Al-Yaman F, Anders RF, Saul A, et al. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1-2b trial in Papua New Guinea. J Infect Dis 2002; 185:820 - 7; http://dx.doi.org/10.1086/339342; PMID: 11920300
  • Spring MD, Cummings JF, Ockenhouse CF, Dutta S, Reidler R, Angov E, 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:e5254; http://dx.doi.org/10.1371/journal.pone.0005254; PMID: 19390585
  • Thera MA, Doumbo OK, Coulibaly D, Laurens MB, Ouattara A, Kone AK, et al. A field trial to assess a blood-stage malaria vaccine. N Engl J Med 2011; 365:1004 - 13; http://dx.doi.org/10.1056/NEJMoa1008115; PMID: 21916638
  • Cech PG, Aebi T, Abdallah MS, Mpina M, Machunda EB, Westerfeld N, et al. Virosome-formulated Plasmodium falciparum AMA-1 & CSP derived peptides as malaria vaccine: randomized phase 1b trial in semi-immune adults & children. PLoS One 2011; 6:e22273; http://dx.doi.org/10.1371/journal.pone.0022273; PMID: 21799810
  • WHO. . Tables of Malaria Vaccine Projects Globally. 2012.
  • Coppel RL. Vaccinating with the genome: a Sisyphean task?. Trends Parasitol 2009; 25:205 - 12; http://dx.doi.org/10.1016/j.pt.2009.02.006; PMID: 19359219
  • Takala SL, Coulibaly D, Thera MA, Batchelor AH, Cummings MP, Escalante AA, et al. Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci Transl Med 2009; 1:ra5; http://dx.doi.org/10.1126/scitranslmed.3000257; PMID: 20165550
  • Lyon JA, Angov E, Fay MP, Sullivan JS, Girourd AS, Robinson SJ, et al. Protection induced by Plasmodium falciparum MSP1(42) is strain-specific, antigen and adjuvant dependent, and correlates with antibody responses. PLoS One 2008; 3:e2830; http://dx.doi.org/10.1371/journal.pone.0002830; PMID: 18665258
  • Good MF, Engwerda C. Defying malaria: Arming T cells to halt malaria. Nat Med 2011; 17:49 - 51; http://dx.doi.org/10.1038/nm0111-49; PMID: 21217684
  • Langhorne J, Ndungu FM, Sponaas AM, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol 2008; 9:725 - 32; http://dx.doi.org/10.1038/ni.f.205; PMID: 18563083
  • Douradinha B, Doolan DL. Harnessing immune responses against Plasmodium for rational vaccine design. Trends Parasitol 2011; 27:274 - 83; http://dx.doi.org/10.1016/j.pt.2011.01.002; PMID: 21531627
  • Coler RN, Carter D, Friede M, Reed SG. Adjuvants for malaria vaccines. Parasite Immunol 2009; 31:520 - 8; http://dx.doi.org/10.1111/j.1365-3024.2009.01142.x; PMID: 19691556
  • Malkin EM, Diemert DJ, McArthur JH, Perreault JR, Miles AP, Giersing BK, et al. Phase 1 clinical trial of apical membrane antigen 1: an asexual blood-stage vaccine for Plasmodium falciparum malaria. Infect Immun 2005; 73:3677 - 85; http://dx.doi.org/10.1128/IAI.73.6.3677-3685.2005; PMID: 15908397
  • Duncan CJ, Hill AV, Ellis RD. Can growth inhibition assays (GIA) predict blood-stage malaria vaccine efficacy?. Hum Vaccin Immunother 2012; 8:706 - 14; http://dx.doi.org/10.4161/hv.19712; PMID: 22508415
  • Bergmann-Leitner ES, Duncan EH, Mullen GE, Burge JR, Khan F, Long CA, et al. Critical evaluation of different methods for measuring the functional activity of antibodies against malaria blood stage antigens. Am J Trop Med Hyg 2006; 75:437 - 42; PMID: 16968918
  • Bergmann-Leitner ES, Duncan EH, Burge JR, Spring M, Angov E. Miniaturization of a high-throughput pLDH-based Plasmodium falciparum growth inhibition assay for small volume samples from preclinical and clinical vaccine trials. Am J Trop Med Hyg 2008; 78:468 - 71; PMID: 18337345
  • Bergmann-Leitner ES, Duncan EH, Mullen GE, Burge JR, Khan F, Long CA, et al. Critical evaluation of different methods for measuring the functional activity of antibodies against malaria blood stage antigens. Am J Trop Med Hyg 2006; 75:437 - 42; PMID: 16968918
  • Theron M, Hesketh RL, Subramanian S, Rayner JC. An adaptable two-color flow cytometric assay to quantitate the invasion of erythrocytes by Plasmodium falciparum parasites. Cytometry A 2010; 77:1067 - 74; http://dx.doi.org/10.1002/cyto.a.20972; PMID: 20872885
  • Persson KEM, McCallum FJ, Reiling L, Lister NA, Stubbs J, Cowman AF, et al. Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J Clin Invest 2008; 118:342 - 51; http://dx.doi.org/10.1172/JCI32138; PMID: 18064303
  • Mahdi Abdel Hamid M, Remarque EJ, van Duivenvoorde LM, van der Werff N, Walraven V, Faber BW, et al. Vaccination with Plasmodium knowlesi AMA1 formulated in the novel adjuvant co-vaccine HT™ protects against blood-stage challenge in rhesus macaques. PLoS One 2011; 6:e20547; http://dx.doi.org/10.1371/journal.pone.0020547; PMID: 21655233
  • Duncan CJ, Sheehy SH, Ewer KJ, Douglas AD, Collins KA, Halstead FD, et al. Impact on malaria parasite multiplication rates in infected volunteers of the protein-in-adjuvant vaccine AMA1-C1/Alhydrogel+CPG 7909. PLoS One 2011; 6:e22271; http://dx.doi.org/10.1371/journal.pone.0022271; PMID: 21799809
  • Douglas AD, Williams AR, Illingworth JJ, Kamuyu G, Biswas S, Goodman AL, et al. The blood-stage malaria antigen PfRH5 is susceptible to vaccine-inducible cross-strain neutralizing antibody. Nat Commun 2011; 2:601; http://dx.doi.org/10.1038/ncomms1615; PMID: 22186897
  • Miura K, Zhou H, Diouf A, Moretz SE, Fay MP, Miller LH, et al. Anti-apical-membrane-antigen-1 antibody is more effective than anti-42-kilodalton-merozoite-surface-protein-1 antibody in inhibiting plasmodium falciparum growth, as determined by the in vitro growth inhibition assay. Clin Vaccine Immunol 2009; 16:963 - 8; http://dx.doi.org/10.1128/CVI.00042-09; PMID: 19439523
  • Jiang L, Gaur D, Mu J, Zhou H, Long CA, Miller LH. Evidence for erythrocyte-binding antigen 175 as a component of a ligand-blocking blood-stage malaria vaccine. Proc Natl Acad Sci U S A 2011; 108:7553 - 8; http://dx.doi.org/10.1073/pnas.1104050108; PMID: 21502513
  • Lunel F, Druilhe P. Effector cells involved in nonspecific and antibody-dependent mechanisms directed against Plasmodium falciparum blood stages in vitro. Infect Immun 1989; 57:2043 - 9; PMID: 2659533
  • Bouharoun-Tayoun H, Attanath P, Sabchareon A, Chongsuphajaisiddhi T, Druilhe P. Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J Exp Med 1990; 172:1633 - 41; http://dx.doi.org/10.1084/jem.172.6.1633; PMID: 2258697
  • Druilhe P, Spertini F, Soesoe D, Corradin G, Mejia P, Singh S, et al. A malaria vaccine that elicits in humans antibodies able to kill Plasmodium falciparum. PLoS Med 2005; 2:e344; http://dx.doi.org/10.1371/journal.pmed.0020344; PMID: 16262450
  • Badell E, Oeuvray C, Moreno A, Soe S, van Rooijen N, Bouzidi A, et al. Human malaria in immunocompromised mice: an in vivo model to study defense mechanisms against Plasmodium falciparum. J Exp Med 2000; 192:1653 - 60; http://dx.doi.org/10.1084/jem.192.11.1653; PMID: 11104807
  • Hill DL, Eriksson EM, Carmagnac AB, Wilson DW, Cowman AF, Hansen DS, et al. Efficient measurement of opsonising antibodies to Plasmodium falciparum merozoites. PLoS One 2012; 7:e51692; http://dx.doi.org/10.1371/journal.pone.0051692; PMID: 23300556
  • Greve B, Lehman LG, Lell B, Luckner D, Schmidt-Ott R, Kremsner PG. High oxygen radical production is associated with fast parasite clearance in children with Plasmodium falciparum malaria. J Infect Dis 1999; 179:1584 - 6; http://dx.doi.org/10.1086/314780; PMID: 10228089
  • Joos C, Marrama L, Polson HE, Corre S, Diatta AM, Diouf B, et al. Clinical protection from falciparum malaria correlates with neutrophil respiratory bursts induced by merozoites opsonized with human serum antibodies. PLoS One 2010; 5:e9871; http://dx.doi.org/10.1371/journal.pone.0009871; PMID: 20360847
  • Sauerwein RW, Roestenberg M, Moorthy VS. Experimental human challenge infections can accelerate clinical malaria vaccine development. Nat Rev Immunol 2011; 11:57 - 64; http://dx.doi.org/10.1038/nri2902; PMID: 21179119
  • Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, et al. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 2012; 487:375 - 9; http://dx.doi.org/10.1038/nature11174; PMID: 22722859
  • Duncan CJ, Draper SJ. Controlled human blood stage malaria infection: current status and potential applications. Am J Trop Med Hyg 2012; 86:561 - 5; http://dx.doi.org/10.4269/ajtmh.2012.11-0504; PMID: 22492136
  • Engwerda CR, Minigo G, Amante FH, McCarthy JS. Experimentally induced blood stage malaria infection as a tool for clinical research. Trends Parasitol 2012; 28:515 - 21; http://dx.doi.org/10.1016/j.pt.2012.09.001; PMID: 23041118
  • Roestenberg M, de Vlas SJ, Nieman AE, Sauerwein RW, Hermsen CC. Efficacy of preerythrocytic and blood-stage malaria vaccines can be assessed in small sporozoite challenge trials in human volunteers. J Infect Dis 2012; 206:319 - 23; http://dx.doi.org/10.1093/infdis/jis355; PMID: 22615322
  • Douglas AD, Edwards NJ, Duncan CJ, Thompson FM, Sheehy SH, O’Hara GA, et al. Comparison of Modeling Methods to Determine Liver-to-blood Inocula and Parasite Multiplication Rates During Controlled Human Malaria Infection. J Infect Dis 2013; In press http://dx.doi.org/10.1093/infdis/jit156; PMID: 23570846
  • Bejon P, Andrews L, Andersen RF, Dunachie S, Webster D, Walther M, et al. 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 2005; 191:619 - 26; http://dx.doi.org/10.1086/427243; PMID: 15655787
  • Hermsen CC, de Vlas SJ, van Gemert GJ, Telgt DS, Verhage DF, Sauerwein RW. Testing vaccines in human experimental malaria: statistical analysis of parasitemia measured by a quantitative real-time polymerase chain reaction. Am J Trop Med Hyg 2004; 71:196 - 201; PMID: 15306710
  • Pollard AJ, Savulescu J, Oxford J, Hill AV, Levine MM, Lewis DJ, et al. Human microbial challenge: the ultimate animal model. Lancet Infect Dis 2012; 12:903 - 5; http://dx.doi.org/10.1016/S1473-3099(12)70292-X; PMID: 23174372
  • Kester KE, Cummings JF, Ofori-Anyinam O, Ockenhouse CF, Krzych U, Moris P, et al, RTS,S Vaccine Evaluation Group. 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; http://dx.doi.org/10.1086/600120; PMID: 19569965
  • Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, Conzelmann C, et al, RTS,S Clinical Trials Partnership. First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N Engl J Med 2011; 365:1863 - 75; http://dx.doi.org/10.1056/NEJMoa1102287; PMID: 22007715
  • Lawrence G, Cheng QQ, Reed C, Taylor D, Stowers A, Cloonan N, et al. Effect of vaccination with 3 recombinant asexual-stage malaria antigens on initial growth rates of Plasmodium falciparum in non-immune volunteers. Vaccine 2000; 18:1925 - 31; http://dx.doi.org/10.1016/S0264-410X(99)00444-2; PMID: 10699342
  • Roestenberg M, O’Hara GA, Duncan CJ, Epstein JE, Edwards NJ, Scholzen A, et al. Comparison of clinical and parasitological data from controlled human malaria infection trials. PLoS One 2012; 7:e38434; http://dx.doi.org/10.1371/journal.pone.0038434; PMID: 22701640
  • Ota MO, Odutola AA, Owiafe PK, Donkor S, Owolabi OA, Brittain NJ, et al. Immunogenicity of the tuberculosis vaccine MVA85A is reduced by coadministration with EPI vaccines in a randomized controlled trial in Gambian infants. Sci Transl Med 2011; 3:88ra56; http://dx.doi.org/10.1126/scitranslmed.3002461; PMID: 21697532
  • Silvie O, Franetich JF, Charrin S, Mueller MS, Siau A, Bodescot M, et al. A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J Biol Chem 2004; 279:9490 - 6; http://dx.doi.org/10.1074/jbc.M311331200; PMID: 14676185
  • Epstein JE. Taking a bite out of malaria: controlled human malaria infection by needle and syringe. Am J Trop Med Hyg 2013; 88:3 - 4; http://dx.doi.org/10.4269/ajtmh.2013.12-0715; PMID: 23303797
  • Roestenberg M, Bijker EM, Sim BK, Billingsley PF, James ER, Bastiaens GJ, et al. Controlled human malaria infections by intradermal injection of cryopreserved Plasmodium falciparum sporozoites. Am J Trop Med Hyg 2013; 88:5 - 13; http://dx.doi.org/10.4269/ajtmh.2012.12-0613; PMID: 23149582
  • Sheehy S, Spencer AJ, Douglas AD, Sim B, Longley KL, Edwards RJ, et al. Optimising Controlled Human Malaria Infection studies using cryopreserved P. falciparum Parasites administered by needle and syringe. PLoS ONE 2013; In press
  • Cheng Q, Lawrence G, Reed C, Stowers A, Ranford-Cartwright L, Creasey A, et al. Measurement of Plasmodium falciparum growth rates in vivo: a test of malaria vaccines. Am J Trop Med Hyg 1997; 57:495 - 500; PMID: 9347970
  • Sanderson F, Andrews L, Douglas AD, Hunt-Cooke A, Bejon P, Hill AV. Blood-stage challenge for malaria vaccine efficacy trials: a pilot study with discussion of safety and potential value. Am J Trop Med Hyg 2008; 78:878 - 83; PMID: 18541763
  • Bijker EM, Bastiaens GJ, Teirlinck AC, van Gemert GJ, Graumans W, van de Vegte-Bolmer M, et al. Protection against malaria after immunization by chloroquine prophylaxis and sporozoites is mediated by preerythrocytic immunity. Proc Natl Acad Sci U S A 2013; 110:7862 - 7; http://dx.doi.org/10.1073/pnas.1220360110; PMID: 23599283
  • Baer K, Klotz C, Kappe SH, Schnieder T, Frevert U. Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLoS Pathog 2007; 3:e171; http://dx.doi.org/10.1371/journal.ppat.0030171; PMID: 17997605
  • Cervia JS, Wenz B, Ortolano GA. Leukocyte reduction’s role in the attenuation of infection risks among transfusion recipients. Clin Infect Dis 2007; 45:1008 - 13; http://dx.doi.org/10.1086/521896; PMID: 17879916
  • Laurens MB, Duncan CJ, Epstein JE, Hill AV, Komisar JL, Lyke KE, et al, Consensus Group on Design of Clinical Trials of Controlled Human Malaria Infection. A consultation on the optimization of controlled human malaria infection by mosquito bite for evaluation of candidate malaria vaccines. Vaccine 2012; 30:5302 - 4; http://dx.doi.org/10.1016/j.vaccine.2012.04.088; PMID: 22659449
  • Andrews L, Andersen RF, Webster D, Dunachie S, Walther RM, Bejon P, et al. Quantitative real-time polymerase chain reaction for malaria diagnosis and its use in malaria vaccine clinical trials. Am J Trop Med Hyg 2005; 73:191 - 8; PMID: 16014857
  • Hermsen CC, Telgt DS, Linders EH, van de Locht LA, Eling WM, Mensink EJ, et al. Detection of Plasmodium falciparum malaria parasites in vivo by real-time quantitative PCR. Mol Biochem Parasitol 2001; 118:247 - 51; http://dx.doi.org/10.1016/S0166-6851(01)00379-6; PMID: 11738714
  • Murphy SC, Prentice JL, Williamson K, Wallis CK, Fang FC, Fried M, et al. Real-time quantitative reverse transcription PCR for monitoring of blood-stage Plasmodium falciparum infections in malaria human challenge trials. Am J Trop Med Hyg 2012; 86:383 - 94; http://dx.doi.org/10.4269/ajtmh.2012.10-0658; PMID: 22403305
  • Douglas AD, Andrews L, Draper SJ, Bojang K, Milligan P, Gilbert SC, et al. Substantially reduced pre-patent parasite multiplication rates are associated with naturally acquired immunity to Plasmodium falciparum. J Infect Dis 2011; 203:1337 - 40; http://dx.doi.org/10.1093/infdis/jir033; PMID: 21459819
  • Pandey AK, Reddy KS, Sahar T, Gupta S, Singh H, Reddy EJ, et al. Identification of a potent combination of key Plasmodium falciparum merozoite antigens that elicit strain-transcending parasite-neutralizing antibodies. Infect Immun 2013; 81:441 - 51; http://dx.doi.org/10.1128/IAI.01107-12; PMID: 23184525
  • Lopaticki S, Maier AG, Thompson J, Wilson DW, Tham WH, Triglia T, et al. Reticulocyte and erythrocyte binding-like proteins function cooperatively in invasion of human erythrocytes by malaria parasites. Infect Immun 2011; 79:1107 - 17; http://dx.doi.org/10.1128/IAI.01021-10; PMID: 21149582