Transmission blocking malaria vaccines: Assays and candidates in clinical development

Vaccine

Volumn 33, Issue 52, 2015, Pages 7476-7482

  Sauerwein, R W ^a   Bousema, T ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Anopheles; Elimination; Gamete; Gametocyte; Malaria; Transmission

Indexed keywords

ANAPN1 VACCINE; ANTIGEN; BLOCKING ANTIBODY; MALARIA VACCINE; PFS230 VACCINE; PFS25 VACCINE; PFS45 VACCINE; PFS48 VACCINE; PROTEIN; UNCLASSIFIED DRUG; MEMBRANE ANTIGEN; PARASITE ANTIGEN; PROTOZOON ANTIBODY;

ANOPHELES STEPHENSI; ANTIBODY TITER; ARTICLE; BIOASSAY; CLINICAL EVALUATION; DISEASE TRANSMISSION; DRUG DEVELOPMENT; DRUG EFFICACY; DRUG MANUFACTURE; GAMETOCYTE; HUMAN; IMMUNIZATION; IMMUNOASSAY; IMMUNOGENICITY; INFECTION PREVENTION; MALARIA; MALARIA CONTROL; MOSQUITO; MOSQUITO FEEDING ASSAY; NONHUMAN; PARASITE DEVELOPMENT; PHASE 1 CLINICAL TRIAL (TOPIC); PLASMODIUM (LIFE CYCLE STAGE); PLASMODIUM BERGHEI; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PUBLIC HEALTH; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); SEXUAL SPOROGONIC MOSQUITO STAGE; STANDARD MEMBRANE FEEDING ASSAY; VACCINATION; ANIMAL; ANOPHELES; BLOOD; CLINICAL TRIAL (TOPIC); DISEASE CARRIER; DISEASE ERADICATION; IMMUNOLOGY; MALARIA, FALCIPARUM; MALARIA, VIVAX; PARASITOLOGY; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; TRANSMISSION;

ANIMALS; ANOPHELES; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; ANTIGENS, SURFACE; BIOLOGICAL ASSAY; CLINICAL TRIALS AS TOPIC; DISEASE ERADICATION; HUMANS; INSECT VECTORS; MALARIA; MALARIA VACCINES; MALARIA, FALCIPARUM; MALARIA, VIVAX; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX;

EID: 84951037494     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.08.073     Document Type: Article

References (94)

1. World Health Organization World malaria report 2014 2014, World Health Organization.
2. Nunes J.K., Woods C., Carter T., Raphael T., Morin M.J., Diallo D., et al. Development of a transmission-blocking malaria vaccine: progress, challenges, and the path forward. Vaccine 2014, 32:5531-5539.
3. malERA Consultation Group on Vaccines A research agenda for malaria eradication: vaccines. PLoS Med 2011, 8:e1000398.
4. HuffC.G., Marchbank D.F., Shiroishi T. Changes in infectiousness of malarial gametocytes. II. Analysis of the possible causative factors. Exp Parasitol 1958, 7:399-417.
5. Gwadz R.W. Successful immunization against the sexual stages of Plasmodium gallinaceum. Science 1976, 193:1150-1151.
6. Carter R., Chen D.H. Malaria transmission blocked by immunisation with gametes of the malaria parasite. Nature 1976, 263:57-60.
7. Eyles D.E. Studies on Plasmodium gallinaceum. II. Factors in the blood of the vertebrate host influencing mosquito infection. Am J Hyg 1952, 55:276-290.
8. Rener J., Graves P.M., Carter R., Williams J.L., Burkot T.R. Target antigens of transmission-blocking immunity on gametes of Plasmodium falciparum. J Exp Med 1983, 158:976-981.
9. Ponnudurai T., Meuwissen J.H., Leeuwenberg A.D., Verhave J.P., Lensen A.H. The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Trans R Soc Trop Med Hyg 1982, 76:242-250.
10. Vermeulen A.N., Ponnudurai T., Beckers P.J., Verhave J.P., Smits M.A., Meuwissen J.H. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med 1985, 162:1460-1476.
11. Nikolaeva D., Draper S.J., Biswas S. Toward the development of effective transmission-blocking vaccines for malaria. Expert Rev Vaccines 2015, 14:653-680.
12. Kaslow D.C., Quakyi I.A., Syin C., Raum M.G., Keister D.B., Coligan J.E., et al. A vaccine candidate from the sexual stage of human malaria that contains EGF-like domains. Nature 1988, 333:74-76.
13. Kocken C.H., Jansen J., Kaan A.M., Beckers P.J., Ponnudurai T., Kaslow D.C., et al. Cloning and expression of the gene coding for the transmission blocking target antigen Pfs48/45 of Plasmodium falciparum. Mol Biochem Parasitol 1993, 61:59-68.
14. Williamson K.C., Criscio M.D., Kaslow D.C. Cloning and expression of the gene for Plasmodium falciparum transmission-blocking target antigen, Pfs230. Mol Biochem Parasitol 1993, 58:355-358.
15. Tsuboi T., Kaslow D.C., Gozar M.M., Tachibana M., Cao Y.M., Torii M. Sequence polymorphism in two novel Plasmodium vivax ookinete surface proteins, Pvs25 and Pvs28, that are malaria transmission-blocking vaccine candidates. Mol Med 1998, 4:772-782.
16. Carter R., Mendis K.N., Miller L.H., Molineaux L., Saul A. Malaria transmission-blocking vaccines-how can their development be supported?. Nat Med 2000, 6:241-244.
17. Birkett A.J., Moorthy V.S., Loucq C., Chitnis C.E., Kaslow D.C. Malaria vaccine R&D in the decade of vaccines: breakthroughs, challenges and opportunities. Vaccine 2013, 31(Suppl. 2):B233-B243.
18. Organization WH Malaria transmission blocking vaccines: an ideal public good. TDR/RBM/MAL/VAC/2000.1 2000, Organization WH.
19. Gwadz R.W., Koontz L.C. Plasmodium knowlesi: persistence of transmission blocking immunity in monkeys immunized with gamete antigens. Infect Immun 1984, 44:137-140.
20. Carter R., Gwadz R.W., Green I. Plasmodium gallinaceum: transmission-blocking immunity in chickens. II. The effect of antigamete antibodies in vitro and in vivo and their elaboration during infection. Exp Parasitol 1979, 47:194-208.
21. Jones S., Grignard L., Nebie I., Chilongola J., Dodoo D., Sauerwein R., et al. Naturally acquired antibody responses to recombinant Pfs230 and Pfs48/45 transmission blocking vaccine candidates. J Infect 2015, 7:117-127.
22. Carter R., Kaushal D.C. Characterization of antigens on mosquito midgut stages of Plasmodium gallinaceum. III. Changes in zygote surface proteins during transformation to mature ookinete. Mol Biochem Parasitol 1984, 13:235-241.
23. Sauerwein R.W. Malaria transmission-blocking vaccines: the bonus of effective malaria control. Microb Infect/Inst Pasteur 2007, 9:792-795.
24. Miura K., Takashima E., Deng B., Tullo G., Diouf A., Moretz S.E., et al. Functional comparison of Plasmodium falciparum transmission-blocking vaccine candidates by the standard membrane-feeding assay. Infect Immun 2013, 81:4377-4382.
25. Quakyi I.A., Carter R., Rener J., Kumar N., Good M.F. Miller LH. The 230-kDa gamete surface protein of Plasmodium falciparum is also a target for transmission-blocking antibodies. J Immunol 1987, 139:4213-4217.
26. Barr P.J., Green K.M., Gibson H.L., Bathurst I.C., Quakyi I.A., Kaslow D.C. Recombinant Pfs25 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in experimental animals. J Exp Med 1991, 174:1203-1208.
27. Hisaeda H., Stowers A.W., Tsuboi T., Collins W.E., Sattabongkot J.S., Suwanabun N., et al. Antibodies to malaria vaccine candidates Pvs25 and Pvs28 completely block the ability of Plasmodium vivax to infect mosquitoes. Infect Immun 2000, 68:6618-6623.
28. Dinglasan R.R., Kalume D.E., Kanzok S.M., Ghosh A.K., Muratova O., Pandey A., et al. Disruption of Plasmodium falciparum development by antibodies against a conserved mosquito midgut antigen. Proc Natl Acad Sci USA 2007, 104:13461-13466.
29. van Dijk M.R., Janse C.J., Thompson J., Waters A.P., Braks J.A., Dodemont H.J., et al. A central role for P48/45 in malaria parasite male gamete fertility. Cell 2001, 104:153-164.
30. Carter R., Coulson A., Bhatti S., Taylor B.J., Elliott J.F. Predicted disulfide-bonded structures for three uniquely related proteins of Plasmodium falciparum, Pfs230. Pfs48/45 and Pf12. Mol Biochem Parasitol 1995, 71:203-210.
31. Roeffen W., Lensen T., Mulder B., Teelen K., Sauerwein R., Van Druten J., et al. A comparison of transmission-blocking activity with reactivity in a Plasmodium falciparum 48/45-kD molecule-specific competition enzyme-linked immunosorbent assay. Am J Trop Med Hyg 1995, 52:60-65.
32. Outchkourov N., Vermunt A., Jansen J., Kaan A., Roeffen W., Teelen K., et al. Epitope analysis of the malaria surface antigen pfs48/45 identifies a subdomain that elicits transmission blocking antibodies. J Biol Chem 2007, 282:17148-17156.
33. Carter R., Graves P.M., Keister D.B., Quakyi I.A. Properties of epitopes of Pfs 48/45, a target of transmission blocking monoclonal antibodies, on gametes of different isolates of Plasmodium falciparum. Parasite Immunol 1990, 12:587-603.
34. Roeffen W., Teelen K., van As J., vd Vegte-Bolmer M., Eling W., Sauerwein R. Plasmodium falciparum: production and characterization of rat monoclonal antibodies specific for the sexual-stage Pfs48/45 antigen. Exp Parasitol 2001, 97:45-49.
35. Outchkourov N.S., Roeffen W., Kaan A., Jansen J., Luty A., Schuiffel D., et al. Correctly folded Pfs48/45 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in mice. Proc Natl Acad Sci USA 2008, 105:4301-4305.
36. Chowdhury D.R., Angov E., Kariuki T., Kumar N. A potent malaria transmission blocking vaccine based on codon harmonized full length Pfs48/45 expressed in Escherichia coli. PLoS ONE 2009, 4:e6352.
37. Theisen M., Roeffen W., Singh S.K., Andersen G., Amoah L., van de Vegte-Bolmer M., et al. A multi-stage malaria vaccine candidate targeting both transmission and asexual parasite life-cycle stages. Vaccine 2014, 32:2623-2630.
38. Singh S.K., Roeffen W., Andersen G., Bousema T., Christiansen M., Sauerwein R., et al. A Plasmodium falciparum 48/45 single epitope R0.6C subunit protein elicits high levels of transmission blocking antibodies. Vaccine 2015, 33:1981-1986.
39. Williamson K.C., Fujioka H., Aikawa M., Kaslow D.C. Stage-specific processing of Pfs230, a Plasmodium falciparum transmission-blocking vaccine candidate. Mol Biochem Parasitol 1996, 78:161-169.
40. Kumar N. Target antigens of malaria transmission blocking immunity exist as a stable membrane bound complex. Parasite Immunol 1987, 9:321-335.
41. Eksi S., Stump A., Fanning S.L., Shenouda M.I., Fujioka H., Williamson K.C. Targeting and sequestration of truncated Pfs230 in an intraerythrocytic compartment during Plasmodium falciparum gametocytogenesis. Mol Microbiol 2002, 44:1507-1516.
42. Roeffen W., Geeraedts F., Eling W., Beckers P., Wizel B., Kumar N., et al. Transmission blockade of Plasmodium falciparum malaria by anti-Pfs230-specific antibodies is isotype dependent. Infect Immun 1995, 63:467-471.
43. Lensen A., Mulder L., Tchuinkam T., Willemsen L., Eling W., Sauerwein R. Mechanisms that reduce transmission of Plasmodium falciparum malaria in semiimmune and nonimmune persons. J Infect Dis 1998, 177:1358-1363.
44. Read D., Lensen A.H., Begarnie S., Haley S., Raza A., Carter R. Transmission-blocking antibodies against multiple, non-variant target epitopes of the Plasmodium falciparum gamete surface antigen Pfs230 are all complement-fixing. Parasite Immunol 1994, 16:511-519.
45. Williamson K.C., Keister D.B., Muratova O., Kaslow D.C. Recombinant Pfs230 a Plasmodium falciparum gametocyte protein, induces antisera that reduce the infectivity of Plasmodium falciparum to mosquitoes. Mol Biochem Parasitol 1995, 75:33-42.
46. Williamson K.C. Pfs230: from malaria transmission-blocking vaccine candidate toward function. Parasite Immunol 2003, 25:351-359.
47. Farrance C.E., Rhee A., Jones R.M., Musiychuk K., Shamloul M., Sharma S., et al. A plant-produced Pfs230 vaccine candidate blocks transmission of Plasmodium falciparum. Clin Vaccine Immunol: CVI 2011, 18:1351-1357.
48. van Amerongen A., Sauerwein R.W., Beckers P.J., Meloen R.H., Meuwissen J.H. Identification of a peptide sequence of the 25kD surface protein of Plasmodium falciparum recognized by transmission-blocking monoclonal antibodies: implications for synthetic vaccine development. Parasite Immunol 1989, 11:425-428.
49. Kaslow D.C., Shiloach J. Production, purification and immunogenicity of a malaria transmission-blocking vaccine candidate: TBV25H expressed in yeast and purified using nickel-NTA agarose. Biotechnology 1994, 12:494-499.
50. Zou L., Miles A.P., Wang J., Stowers A.W. Expression of malaria transmission-blocking vaccine antigen Pfs25 in Pichia pastoris for use in human clinical trials. Vaccine 2003, 21:1650-1657.
51. Wu Y., Ellis R.D., Shaffer D., Fontes E., Malkin E.M., Mahanty S., et al. Phase 1 trial of malaria transmission blocking vaccine candidates Pfs25 and Pvs25 formulated with montanide ISA 51. PLoS ONE 2008, 3:e2636.
52. Malkin E.M., Durbin A.P., Diemert D.J., Sattabongkot J., Wu Y., Miura K., et al. Phase 1 vaccine trial of Pvs25H: a transmission blocking vaccine for Plasmodium vivax malaria. Vaccine 2005, 23:3131-3138.
53. Mulder B., Roeffen W., Sauerwein R., Tchuinkam T., Boudin C., Verhave J.P. Anti-Pfs25 monoclonal antibody 32F81 blocks transmission from Plasmodium falciparum gametocyte carriers in Cameroon. Trans R Soc Trop Med Hyg 1996, 90:195.
54. Kumar R., Angov E., Kumar N. Potent malaria transmission-blocking antibody responses elicited by Plasmodium falciparum Pfs25 expressed in Escherichia coli after successful protein refolding. Infect Immun 2014, 82:1453-1459.
55. Gregory J.A., Li F., Tomosada L.M., Cox C.J., Topol A.B., Vinetz J.M., et al. Algae-produced Pfs25 elicits antibodies that inhibit malaria transmission. PLoS ONE 2012, 7:e37179.
56. Biswas S., Li Y., Miura S. Enhancing antibody immunogenicity of transmission-blocking malaria vaccines. 62nd Annual meeting: American Society of Tropical Medicine and Hygiene 2013.
57. Jones R.M., Chichester J.A., Manceva S., Gibbs S.K., Musiychuk K., Shamloul M., et al. A novel plant-produced Pfs25 fusion subunit vaccine induces long-lasting transmission blocking antibody responses. Hum Vaccines Immunother 2015, 11:124-132.
58. Kubler-Kielb J., Majadly F., Wu Y., Narum D.L., Guo C., Miller L.H., et al. Long-lasting and transmission-blocking activity of antibodies to Plasmodium falciparum elicited in mice by protein conjugates of Pfs25. Proc Natl Acad Sci USA 2007, 104:293-298.
59. Dinglasan R.R., Alaganan A., Ghosh A.K., Saito A., van Kuppevelt T.H., Jacobs-Lorena M. Plasmodium falciparum ookinetes require mosquito midgut chondroitin sulfate proteoglycans for cell invasion. Proc Natl Acad Sci USA 2007, 104:15882-15887.
60. Mathias D.K., Plieskatt J.L., Armistead J.S., Bethony J.M., Abdul-Majid K.B., McMillan A., et al. Expression, immunogenicity, histopathology, and potency of a mosquito-based malaria transmission-blocking recombinant vaccine. Infect Immun 2012, 80:1606-1614.
61. Healer J., McGuinness D., Hopcroft P., Haley S., Carter R., Riley E. Complement-mediated lysis of Plasmodium falciparum gametes by malaria-immune human sera is associated with antibodies to the gamete surface antigen Pfs230. Infect Immun 1997, 65:3017-3023.
62. Ponnudurai T., Verhave J.P., Meuwissen J.H. Mosquito transmission of cultured Plasmodium falciparum. Trans R Soc Trop Med Hyg 1982, 76:278-279.
63. Bousema T., Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev 2011, 24:377-410.
64. Bell A.S., Ranford-Cartwright L.C. A real-time PCR assay for quantifying Plasmodium falciparum infections in the mosquito vector. Int J Parasitol 2004, 34:795-802.
65. Stone W.J., Eldering M., van Gemert G.J., Lanke K.H., Grignard L., van de Vegte-Bolmer M.G., et al. The relevance and applicability of oocyst prevalence as a read-out for mosquito feeding assays. Sci Rep 2013, 3:3418.
66. Kumar S., Zheng H., Deng B., Mahajan B., Grabias B., Kozakai Y., et al. A slot blot immunoassay for quantitative detection of Plasmodium falciparum circumsporozoite protein in mosquito midgut oocyst. PLoS ONE 2014, 9:e115807.
67. Delves M.J., Sinden R.E. A semi-automated method for counting fluorescent malaria oocysts increases the throughput of transmission blocking studies. Malar J 2010, 9:35.
68. Stone W.J., Churcher T.S., Graumans W., van Gemert G.J., Vos M.W., Lanke K.H., et al. A scalable assessment of Plasmodium falciparum transmission in the standard membrane-feeding assay, using transgenic parasites expressing green fluorescent protein-luciferase. J Infect Dis 2014, 210:1456-1463.
69. Lensen A., van Druten J., Bolmer M., van Gemert G., Eling W., Sauerwein R. Measurement by membrane feeding of reduction in Plasmodium falciparum transmission induced by endemic sera. Trans R Soc Trop Med Hyg 1996, 90:20-22.
70. van der Kolk M., De Vlas S.J., Saul A., van de Vegte-Bolmer M., Eling W.M., Sauerwein R.W. Evaluation of the standard membrane feeding assay (SMFA) for the determination of malaria transmission-reducing activity using empirical data. Parasitology 2005, 130:13-22.
71. Miura K., Deng B., Tullo G., Diouf A., Moretz S.E., Locke E., et al. Qualification of standard membrane-feeding assay with Plasmodium falciparum malaria and potential improvements for future assays. PLoS ONE 2013, 8:e57909.
72. Billingsley P.F. Vector-parasite interactions for vaccine development. Int J Parasitol 1994, 24:53-58.
73. Bousema T., Churcher T.S., Morlais I., Dinglasan R.R. Can field-based mosquito feeding assays be used for evaluating transmission-blocking interventions?. Trends Parasitol 2013, 29:53-59.
74. Saul A. Mosquito stage, transmission blocking vaccines for malaria. Curr Opin Infect Dis 2007, 20:476-481.
75. Saul A. Efficacy model for mosquito stage transmission blocking vaccines for malaria. Parasitology 2008, 135:1497-1506.
76. Blagborough A.M., Churcher T.S., Upton L.M., Ghani A.C., Gething P.W., Sinden R.E. Transmission-blocking interventions eliminate malaria from laboratory populations. Nat Commun 2013, 4:1812.
77. Churcher T.S., Blagborough A.M., Delves M., Ramakrishnan C., Kapulu M.C., Williams A.R., et al. Measuring the blockade of malaria transmission-an analysis of the Standard Membrane Feeding Assay. Int J Parasitol 2012, 42:1037-1044.
78. Da D.F., Churcher T.S., Yerbanga R.S., Yameogo B., Sangare I., Ouedraogo J.B., et al. Experimental study of the relationship between Plasmodium gametocyte density and infection success in mosquitoes; implications for the evaluation of malaria transmission-reducing interventions. Exp Parasitol 2015, 149:74-83.
79. Cheru L., Wu Y., Diouf A., Moretz S.E., Muratova O.V., Song G., et al. The IC(50) of anti-Pfs25 antibody in membrane-feeding assay varies among species. Vaccine 2010, 28:4423-4429.
80. Miura K., Keister D.B., Muratova O.V., Sattabongkot J., Long C.A., Saul A. Transmission-blocking activity induced by malaria vaccine candidates Pfs25/Pvs25 is a direct and predictable function of antibody titer. Malar J 2007, 6:107.
81. Smith T.A., Chitnis N., Briet O.J., Tanner M. Uses of mosquito-stage transmission-blocking vaccines against Plasmodium falciparum. Trends Parasitol 2011, 27:190-196.
82. Delrieu I., Leboulleux D., Ivinson K., Gessner B.D. Malaria transmission blocking vaccine technical consultation G. Design of a Phase III cluster randomized trial to assess the efficacy and safety of a malaria transmission blocking vaccine. Vaccine 2015, 33:1518-1526.
83. Gaye A., Bousema T., Libasse G., Ndiath M.O., Konate L., Jawara M., et al. Infectiousness of the human population to anopheles arabiensis by direct skin feeding in an area hypoendemic for malaria in Senegal. Am J Trop Med Hyg 2015, 92:648-652.
84. Poirot E., Skarbinski J., Sinclair D., Kachur S.P., Slutsker L., Hwang J. Mass drug administration for malaria. Cochrane Database Syst Rev 2013, 12:CD008846.
85. Okell L.C., Griffin J.T., Kleinschmidt I., Hollingsworth T.D., Churcher T.S., White M.J., et al. The potential contribution of mass treatment to the control of Plasmodium falciparum malaria. PLoS ONE 2011, 6:e20179.
86. Bousema T., Dinglasan R.R., Morlais I., Gouagna L.C., van Warmerdam T., Awono-Ambene P.H., et al. Mosquito feeding assays to determine the infectiousness of naturally infected Plasmodium falciparum gametocyte carriers. PLoS ONE 2012, 7:e42821.
87. Da D.F., Dixit S., Sattabonkot J., Mu J., Abate L., Ramineni B., et al. Anti-Pfs25 human plasma reduces transmission of Plasmodium falciparum isolates that have diverse genetic backgrounds. Infect Immun 2013, 81:1984-1989.
88. Moonen B., Cohen J.M., Snow R.W., Slutsker L., Drakeley C., Smith D.L., et al. Operational strategies to achieve and maintain malaria elimination. Lancet 2010, 376:1592-1603.
89. Roestenberg M., McCall M., Hopman J., Wiersma J., Luty A.J., van Gemert G.J., et al. Protection against a malaria challenge by sporozoite inoculation. N Engl J Med 2009, 361:468-477.
90. McCarthy J.S., Sekuloski S., Griffin P.M., Elliott S., Douglas N., Peatey C., et al. A pilot randomised trial of induced blood-stage Plasmodium falciparum infections in healthy volunteers for testing efficacy of new antimalarial drugs. PLoS ONE 2011, 6:e21914.
91. Spring M.D., Cummings J.F., Ockenhouse C.F., 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.
92. Kester K.E., Cummings J.F., Ockenhouse C.F., Nielsen R., Hall B.T., Gordon D.M., et al. 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-naive adults at the Walter Reed Army Institute of Research. Vaccine 2008, 26:2191-2202.
93. Schneider P., Schoone G., Schallig H., Verhage D., Telgt D., Eling W., et al. Quantification of Plasmodium falciparum gametocytes in differential stages of development by quantitative nucleic acid sequence-based amplification. Mol Biochem Parasitol 2004, 137:35-41.
94. Noor A.M., Kinyoki D.K., Mundia C.W., Kabaria C.W., Mutua J.W., Alegana V.A., et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000-10: a spatial and temporal analysis of transmission intensity. Lancet 2014, 383:1739-1747.