Transmission-blocking strategies: The roadmap from laboratory bench to the community

Malaria Journal

Volumn 15, Issue 1, 2016, Pages

  Goncąlves, Daniel ^a   Hunziker, Patrick ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Gametocytocidal drugs; Malaria vaccine; Refractory mosquitoes; Transmission blocking strategies

Indexed keywords

ARTEMISININ; MALARIA VACCINE; ANTIMALARIAL AGENT;

BED NET; CELL DENSITY; CONTROL STRATEGY; GAMETOCYTE; HUMAN; MALARIA; MALARIA CONTROL; NONHUMAN; PARASITE TRANSMISSION; PLASMODIUM (LIFE CYCLE STAGE); PREVALENCE; REVIEW; ANIMAL; DRUG EFFECTS; INSECT VECTOR; MOSQUITO; PHYSIOLOGY; PLASMODIUM FALCIPARUM; TRANSMISSION;

ANIMALS; ANTIMALARIALS; CULICIDAE; INSECT VECTORS; MALARIA; PLASMODIUM FALCIPARUM;

EID: 84959573901     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/s12936-016-1163-3     Document Type: Review

References (191)

1. WHO. World malaria report 2014. Geneva: World Health Organization; 2014.
2. Guerra CA, Gikandi PW, Tatem AJ, Noor AM, Smith DL, Hay SI, et al. The limits and intensity of Plasmodium falciparum transmission: Implications for malaria control and elimination worldwide. PLoS Med. 2008;5:e38. doi: 10.1371/journal.pmed.0050038.
3. Guerra CA, Howes RE, Patil AP, Gething PW, Van Boeckel TP, Temperley WH, et al. The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl Trop Dis. 2010;4:e774. doi: 10.1371/journal.pntd.0000774.
4. Malaria Atlas Project. University of Oxford, UK. 2006. http://www.map.ox.ac.uk/explorer/Accessed 21 Aug 2015.
5. Murray CJL, 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.
6. Kantele A, Jokiranta TS. Review of cases with the emerging fifth human malaria parasite, Plasmodium knowlesi. Clin Infect Dis. 2011;52:1356-62.
7. WHO. MalERA update. World Health Organization, Geneva. http://www.who.int/malaria/elimination/maleraupdate.pdf of subordinate document. Accessed 13 June 2015.
8. EMA. First malaria vaccine receives positive scientific opinion from EMA-London, The European Medicines Agency. http://www.ema.europa.eu/docs/en-GB/document-library/Press-release/2015/07/WC500190447.pdf of subordinate document. Accessed 3 Feb 2016.
9. WHO. World malaria report 2015. Geneva: World Health Organization; 2015.
10. Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2009;361:455-67.
11. Amaratunga C, Sreng S, Suon S, Phelps ES, Stepniewska K, Lim P, et al. Artemisinin-resistant Plasmodium falciparum in Pursat province, western Cambodia: A parasite clearance rate study. Lancet Infect Dis. 2012;12:851-8.
12. Kyaw MP, Nyunt MH, Chit K, Aye MM, Aye KH, Lindegardh N, et al. Reduced susceptibility of Plasmodium falciparum to artesunate in southern Myanmar. PLoS ONE. 2013;8:e57689. doi: 10.1371/journal.pone.0057689.
13. O'Brien C, Henrich PP, Passi N, Fidock DA. Recent clinical and molecular insights into emerging artemisinin resistance in Plasmodium falciparum. Curr Opin Infect Dis. 2011;24:570-7.
14. Phyo AP, Nkhoma S, Stepniewska K, Ashley EA, Nair S, McGready R, et al. Emergence of artemisinin-resistant malaria on the western border of Thailand: A longitudinal study. Lancet. 2012;379:1960-6.
15. Hien TT, Thuy-Nhien NT, Phu NH, Boni MF, Thanh NV, Nha-Ca NT, et al. In vivo susceptibility of Plasmodium falciparum to artesunate in Binh Phuoc province, Vietnam. Malar J. 2012;11:355.
16. Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, et al. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2014;371:411-23.
17. Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control? Trends Parasitol. 2011;27:91-8.
18. Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, et al. High level of resistance in the mosquito Anopheles gambiae to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania. Malar J. 2013;12:149.
19. Toé KH, Jones CM, N'Fale S, Ismail HM, Dabiré RK, Ranson H. Increased pyrethroid resistance in malaria vectors and decreased bed net effectiveness, Burkina Faso. Emerg Infect Dis. 2014;20:1691-6.
20. Trape JF, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, et al. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: A longitudinal study. Lancet Infect Dis. 2011;11:925-32.
21. Malaria Consortium. Malaria prevention: Insecticides. http://www.malariaconsortium.org/userfiles/file/Malaria%20resources/Insecticides%202.pdf of subordinate document. Accessed 6 Sept 2015.
22. Eisele TP, Larsen D, Steketee RW. Protective efficacy of interventions for preventing malaria mortality in children in Plasmodium falciparum endemic areas. Int J Epidemiol. 2010;39:88-101.
23. Ramirez JL, Garver LS, Dimopoulos G. Challenges and approaches for mosquito targeted malaria control. Curr Mol Med. 2009;9:116-30.
24. Nwane P, Etang J, Chouaïbou M, Toto JC, Koffi A, Mimpfoundi R, et al. Multiple insecticide resistance mechanisms in Anopheles gambiae s.l. populations from Cameroon, Central Africa. Parasit Vectors. 2013;6:41.
25. Smith DL, McKenzie FE. Statics and dynamics of malaria infection in Anopheles mosquitoes. Malar J. 2004;3:13.
26. Smith DL, McKenzie FE, Snow RW, Hay SI. Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biol. 2007;5:e42. doi: 10.1371/journal.pbio.0050042.
27. Kelly-Hope LA, McKenzie FE. The multiplicity of malaria transmission: A review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Malar J. 2009;8:19.
28. Smith DL, Dushoff J, Snow RW, Hay SI. The entomological inoculation rate and Plasmodium falciparum infection in African children. Nature. 2005;438:492-5.
29. Bøgh C, Lindsay SW, Clarke SE, Dean A, Jawara M, Pinder M, Thomas CJ. High spatial resolution mapping of malaria transmission risk in the Gambia, west Africa, using LANDSAT TM satellite imagery. Am J Trop Med Hyg. 2007;76:875-81.
30. Smith T, Schapira A. Reproduction numbers in malaria and their implications. Trends Parasitol. 2012;28:3-8.
31. Blagborough AM, Churcher TS, Upton LM, Ghani AC, Gething PW, Sinden RE. Transmission-blocking interventions eliminate malaria from laboratory populations. Nat Commun. 2013;4:1812.
32. Macdonald G, Goeckel GW. The malaria parasite rate and interruption of transmission. Bull World Health Organ. 1964;31:365-77.
33. Johnston GL, Smith DL, Fidock DA. Malaria's missing number: Calculating the human component of R0 by a within-host mechanistic model of Plasmodium falciparum infection and transmission. PLoS Comput Biol. 2013;9:e1003025. doi: 10.1371/journal.pcbi.1003025.
34. Tusting LS, Bousema T, Smith DL, Drakeley C. Measuring changes in Plasmodium falciparum transmission: Precision, accuracy and costs of metrics. Adv Parasitol. 2014;84:151-208.
35. Trape JF, Lefebvre-Zante E, Legros F, Ndiaye G, Bouganali H, Druilhe P, Salem G. Vector density gradients and the epidemiology of urban malaria in Dakar, Senegal. Am J Trop Med Hyg. 1992;47:181-9.
36. Midega JT, Mbogo CM, Mwnambi H, Wilson MD, Ojwang G, Mwangangi JM, et al. Estimating dispersal and survival of Anopheles gambiae and Anopheles funestus along the Kenyan coast by using mark-release-recapture methods. J Med Entomol. 2007;44:923-9.
37. Francia ME, Striepen B. Cell division in apicomplexan parasites. Nat Rev Microbiol. 2014;12:125-36.
38. Ferreira UM, Nunes MS, Wunderlich G. Antigenic diversity and immune evasion by malaria parasites. Clin Diagn Lab Immunol. 2004;11:987-95.
39. Kirkman LA, Deitsch KW. Antigenic variation and the generation of diversity in malaria parasites. Curr Opin Microbiol. 2012;15:456-62.
40. Prudêncio M, Rodriguez A, Mota MM. The silent path to thousands of merozoites: The Plasmodium liver stage. Nat Rev Microbiol. 2006;4:849-56.
41. Miller LH, Ackerman HC, Xin-zhuan S, Wellems TE. Malaria biology and disease pathogenesis: Insights for new treatments. Nat Med. 2013;19:156-67.
42. Eichner M, Diebner HH, Molineaux L, Collins WE, Jeffery GM, Dietz K. Genesis, sequestration and survival of Plasmodium falciparum gametocytes: Parameter estimates from fitting a model to malaria therapy data. Trans R Soc Trop Med Hyg. 2001;95:497-501.
43. McGuinness D, Koram K, Bennett S, Wagner G, Nkrumah F, Riley E. Clinical case definitions for malaria: Clinical malaria associated with very low parasite densities in African infants. Trans R Soc Trop Med Hyg. 1998;92:527-31.
44. Wilairatana P, Tangpukdee N, Krudsood S. Definition of hyperparasitemia in severe falciparum malaria should be updated. Asian Pac J Trop Biomed. 2013;3:586.
45. Baton LA, Ranford-Cartwright LC. Spreading the seeds of million-murdering death: Metamorphoses of malaria in the mosquito. Trends Parasitol. 2005;21:573-80.
46. Angrisano F, Tan YH, Sturm A, McFadden GI, Baum J. Malaria parasite colonisation of the mosquito midgut-placing the Plasmodium ookinete centre stage. Int J Parasitol. 2012;42:519-27.
47. Vega-Rodríguez J, Ghosh AK, Kanzok SM, Dinglasan RR, Wang S, Bongio NJ, et al. Multiple pathways for Plasmodium ookinete invasion of the mosquito midgut. Proc Natl Acad Sci USA. 2014;111:492-500.
48. Hegedus D, Erlandson M, Gillott C, Toprak U. New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol. 2009;54:285-302.
49. Abraham EG, Jacobs-Lorena M. Mosquito midgut barriers to malaria parasite development. Insect Biochem Mol Biol. 2004;34:667-71.
50. Han YS, Thompson J, Kafatos FC, Barillas-Mury C. Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: The time bomb theory of ookinete invasion of mosquitoes. EMBO J. 2000;19:6030-40.
51. Han YS, Barillas-Mury C. Implications of time bomb model of ookinete invasion of midgut cells. Insect Biochem Mol Biol. 2002;32:1311-6.
52. Hillyer JF, Barreau C, Vernick KD. Efficiency of salivary gland invasion by malaria sporozoites is controlled by rapid sporozoite destruction in the mosquito hemocoel. Int J Parasitol. 2007;37:673-81.
53. Medica DL, Sinnis P. Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes. Infect Immun. 2005;73:4363-9.
54. Rosenberg R, Wirtz RA, Schneider I, Burge R. An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Trans R Soc Trop Med Hyg. 1990;84:209-12.
55. Amino R, Thiberge S, Martin B, Celli S, Shorte S, Frischknecht F, et al. Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med. 2006;12:220-4.
56. Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G. Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol. 2010;34:387-95.
57. Malaguarnera L, Musumeci S. The immune response to Plasmodium falciparum malaria. Lancet Infect Dis. 2002;2:472-8.
58. Hall N, Karras M, Raine JD, Carlton JM, Kooij TW, Berriman M, et al. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science. 2005;307:82-6.
59. Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M, Haynes JD, et al. A proteomic view of the Plasmodium falciparum life cycle. Nature. 2002;419:520-6.
60. Ahmed AM, Baggott SL, Maingon R, Hurd H. The costs of mounting an immune response are reflected in the reproductive fitness of the mosquito Anopheles gambiae. Oikos. 2002;97:371-7.
61. Hurd H. Manipulation of medically important insect vectors by their parasites. Annu Rev Entomol. 2003;48:141-61.
62. Sangare I, Michalakis Y, Yameogo B, Dabire R, Morlais I, Cohuet A. Studying fitness cost of Plasmodium falciparum infection in malaria vectors: Validation of an appropriate negative control. Malar J. 2013;12:2.
63. Carter R, Miller LH. Evidence for environmental modulation of gametocytogenesis in Plasmodium falciparum in continuous culture. Bull World Health Organ. 1979;57:37-52.
64. Bruce MC, Alano P, Duthie S, Carter R. Commitment of the malaria parasite Plasmodium falciparum to sexual and asexual development. Parasitology. 1990;100:191-200.
65. Smith TG, Lourenço P, Carter R, Walliker D, Ranford-Cartwright LC. Commitment to sexual differentiation in the human malaria parasite, Plasmodium falciparum. Parasitology. 2000;121:127-33.
66. Mitri C, Thiery I, Bourgouin C, Paul RE. Density-dependent impact of the human malaria parasite Plasmodium falciparum gametocyte sex ratio on mosquito infection rates. Proc Biol Sci. 2009;276:3721-6.
67. Baker DA. Malaria gametocytogenesis. Mol Biochem Parasitol. 2010;172:57-65.
68. 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;75:32-7.
69. Kuehn A, Pradel G. The coming-out of malaria gametocytes. J Biomed Biotechnol. 2010;2010:976827. doi: 10.1155/2010/976827.
70. 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.
71. Bousema T, Okell L, Shekalaghe S, Griffin JT, Omar S, Sawa P, et al. Revisiting the circulation time of Plasmodium falciparum gametocytes: Molecular detection methods to estimate the duration of gametocyte carriage and the effect of gametocytocidal drugs. Malar J. 2010;9:136.
72. Smalley ME, Sinden RE. Plasmodium falciparum gametocytes: Their longevity and infectivity. Parasitology. 1977;74:1-8.
73. Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470-4.
74. Eckhoff P. P. falciparum infection durations and infectiousness are shaped by antigenic variation and innate and adaptive host immunity in a mathematical model. PLoS ONE. 2012;7:e44950. doi: 10.1371/journal.pone.0044950.
75. Da DF, Churcher TS, Yerbanga RS, Yameógo B, Sangaré I, Ouedraogo JB, 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.
76. Bousema T, Okell L, Felger I, Drakeley C. Asymptomatic malaria infections: Detectability, transmissibility and public health relevance. Nat Rev Microbiol. 2014;12:833-40.
77. Wampfler R, Mwingira F, Javati S, Robinson L, Betuela I, Siba P, et al. Strategies for detection of Plasmodium species gametocytes. PLoS ONE. 2013;8:e76316. doi: 10.1371/journal.pone.0076316.
78. 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.
79. Karl Stephan. Comparison of three methods for detection of gametocytes in Melanesian children treated for uncomplicated malaria. Malar J. 2014;13:319.
80. WPRO. Determining cost effectiveness of malaria rapid diagnostic tests in rural areas with high prevalence-Manila. World Health Organization Western Pacific Region. http://www.wpro.who.int/malaria/NR/rdonlyres/0A45DF24-4245-4BF3-96E7-5F1150AF333B/0/DeterminingCostEffectivenessofRDTsinruralareaswithhighprevalence.pdf of subordinate document. Accessed 3 Feb 2016.
81. Hansen KS, Grieve E, Mikhail A, Mayan I, Mohammed N, Anwar M, et al. Cost-effectiveness of malaria diagnosis using rapid diagnostic tests compared to microscopy or clinical symptoms alone in Afghanistan. Malar J. 2015;14:217.
82. Ansah EK, Epokor M, Whitty CJ, Yeung S, Hansen KS. Cost-effectiveness analysis of introducing RDTs for malaria diagnosis as compared to microscopy and presumptive diagnosis in central and peripheral public health facilities in Ghana. Am J Trop Med Hyg. 2013;89:724-36.
83. Cook J, Aydin-Schmidt B, González IJ, Bell D, Edlund E, Nassor MH, et al. Loop-mediated isothermal amplification (LAMP) for point-of-care detection of asymptomatic low-density malaria parasite carriers in Zanzibar. Malar J. 2015;14:43.
84. Githeko AK, Brandling-Bennett AD, Beier M, Atieli F, Owaga M, Collins FH. The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Trans R Soc Trop Med Hyg. 1992;86:355-8.
85. 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.
86. Churcher TS, Bousema T, Walker M, Drakeley C, Schneider P, Ouédraogo AL, et al. Predicting mosquito infection from Plasmodium falciparum gametocyte density and estimating the reservoir of infection. Elife. 2013;2:e00626. doi: 10.7554/eLife.00626.
87. Drakeley CJ, Bousema JT, Akim NI, Teelen K, Roeffen W, Lensen AH, et al. Transmission-reducing immunity is inversely related to age in Plasmodium falciparum gametocyte carriers. Parasite Immunol. 2006;28:185-90.
88. Haji H, Smith T, Charlwood JD, Meuwissen JH. Absence of relationships between selected human factors and natural infectivity of Plasmodium falciparum to mosquitoes in an area of high transmission. Parasitology. 1996;113:425-31.
89. Bousema T, Churcher TS, Morlais I, Dinglasan RR. Can field-based mosquito feeding assays be used for evaluating transmission-blocking interventions? Trends Parasitol. 2013;29:53-9.
90. Pukrittayakamee S, Chotivanich K, Chantra A, Clemens R, Looareesuwan S, White NJ. Activities of artesunate and primaquine against asexual-and sexual-stage parasites in falciparum malaria. Antimicrob Agents Chemother. 2004;48:1329-34.
91. Song J, Socheat D, Tan B, Dara P, Deng C, Sokunthea S, et al. Rapid and effective malaria control in Cambodia through mass administration of artemisinin-piperaquine. Malaria J. 2010;9:57.
92. Graves PM, Gelband H, Garner P. Primaquine or other 8-aminoquinoline for reducing Plasmodium falciparum transmission. Cochrane Database Syst Rev. 2015;6:CD008152. doi: 10.1002/14651858.CD008152.pub4.
93. Maude RJ, Socheat D, Nguon C, Saroth P, Dara P, Li G, et al. Optimising strategies for Plasmodium falciparum malaria elimination in Cambodia: Primaquine, mass drug administration and artemisinin resistance. PLoS ONE. 2012;7:e37166. doi: 10.1371/journal.pone.0037166.
94. Baird JK, Surjadjaja C. Consideration of ethics in primaquine therapy against malaria transmission. Trends Parasitol. 2011;27:11-6.
95. Eziefula AC, Bousema T, Yeung S, Kamya M, Owaraganise A, Gabagaya G, et al. Single dose primaquine for clearance of Plasmodium falciparum gametocytes in children with uncomplicated malaria in Uganda: A randomised, controlled, double-blind, dose-ranging trial. Lancet Infect Dis. 2014;14:130-9.
96. WHO. Guidelines for the treatment of malaria. 3rd ed. Geneva: WHO Library Cataloguing-in-Publication Data; 2015.
97. Pukrittayakamee S, Imwong M, Singhasivanon P, Stepniewska K, Day NJ, White NJ. Effects of different antimalarial drugs on gametocyte carriage in P. vivax malaria. Am J Trop Med Hyg. 2008;79:378-84.
98. Nacher M, Silachamroon U, Singhasivanon P, Wilairatana P, Phumratanaprapin W, Fontanet A, et al. Comparison of artesunate and chloroquine activities against Plasmodium vivax gametocytes. Antimicrob Agents Chemother. 2004;48:2751-2.
99. Zeeman AM, der Wel AV, Kocken CH. Ex vivo culture of Plasmodium vivax and Plasmodium cynomolgi and in vitro culture of Plasmodium knowlesi blood stages. Methods Mol Biol. 2013;923:35-49.
100. McClean CM, Alvarado HG, Neyra V, Llanos-Cuentas A, Vinetz JM. Optimized in vitro production of Plasmodium vivax ookinetes. Am J Trop Med Hyg. 2010;83:1183-6.
101. Fivelman QL, McRobert L, Sharp S, Taylor CJ, Saeed M, Swales CA, et al. Improved synchronous production of Plasmodium falciparum gametocytes in vitro. Mol Biochem Parasitol. 2007;154:119-23.
102. Roncalés M, Vidal-Mas J, Leroy D, Herreros E. Comparison and optimization of different methods for the in vitro production of Plasmodium falciparum gametocytes. J Parasit Res. 2012;2012:927148. doi: 10.1155/2012/927148.
103. Ghosh AK, Dinglasan RR, Ikadai H, Jacobs-Lorena M. An improved method for the in vitro differentiation of Plasmodium falciparum gametocytes into ookinetes. Malar J. 2010;9:194.
104. Bounkeua V, Li F, Vinetz JM. In vitro generation of Plasmodium falciparum ookinetes. Am J Trop Med Hyg. 2010;83:1187-94.
105. Delves M, Plouffe D, Scheurer C, Meister S, Wittlin S, Winzeler EA, et al. The activities of current antimalarial drugs on the life cycle stages of Plasmodium: A comparative study with human and rodent parasites. PLoS Med. 2012;9:e1001169. doi: 10.1371/journal.pmed.1001169.
106. Peatey CL, Leroy D, Gardiner DL, Trenholme KR. Anti-malarial drugs: How effective are they against Plasmodium falciparum gametocytes. Malar J. 2012;11:34.
107. Lelièvre J, Almela MJ, Lozano S, Miguel C, Franco V, Leroy D, et al. Activity of clinically relevant antimalarial drugs on Plasmodium falciparum mature gametocytes in na ATP bioluminescence "transmission blocking" assay. PLoS ONE. 2012;7:e35019. doi: 10.1371/journal.pone.0035019.
108. Tanaka TQ, Williamson KC. A malaria gametocytocidal assay using oxidoreduction indicator, Alamar Blue. Mol Biochem Parasitol. 2011;177:160-3.
109. Duffy S, Avery VM. Identification of inhibitors of Plasmodium falciparum gametocyte development. Malar J. 2013;12:408.
110. Buchholz K, Burke TA, Williamson KC, Wiegand RC, Wirth DF, Marti M. A high-throughput screen targeting malaria transmission stages opens new avenues for drug development. J Infect Dis. 2011;203:1445-53.
111. Peatey CL, Spicer TP, Hodder PS, Trenholme KR, Gardiner DL. A high-throughput assay for the identification of drugs against late-stage Plasmodium falciparum gametocytes. Mol Biochem Parasitol. 2011;180:127-31.
112. Miguel-Blanco C, Lelièvre J, Delves MJ, Bardera AI, Presa JL, López-Barragán MJ, et al. Imaging-based high-throughput screening assay to identify new molecules with transmission-blocking potential against Plasmodium falciparum female gamete formation. Antimicrob Agents Chemother. 2015;59:3298-305.
113. Gamo FJ, Sanz LM, Vidal J, de Cozar C, Alvarez E, Lavandera JL, et al. Thousands of chemical starting points for antimalarial lead identification. Nature. 2010;465:305-10.
114. Rieckmann KH, McNamara JV, Frischer H, Stockert TA, Carson PE, Powell RD. Gametocytocidal and sporontocidal effects of primaquine and of sulfadiazine with pyrimethamine in a chloroquine-resistant strain of Plasmodium falciparum. Bull World Health Organ. 1968;38:625-32.
115. Wilairatana P, Krudsood S, Tangpukdee N. Appropriate time for primaquine treatment to reduce Plasmodium falciparum transmission in hypoendemic areas. Korean J Parasitol. 2010;48:179-82.
116. Lawpoolsri S, Klein EY, Singhasivanon P, Yimsamran S, Thanyavanich N, Maneeboonyang W, et al. Optimally timing primaquine treatment to reduce Plasmodium falciparum transmission in low endemicity Thai-Myanmar border populations. Malar J. 2009;8:159.
117. Hastings IM. Gametocytocidal activity in antimalarial drugs speeds the spread of drug resistance. Trop Med Int Health. 2006;11:1206-17.
118. Talisuna AO, Okello PE, Erhart A, Coosemans M, D'Alessandro U. Intensity of malaria transmission and the spread of Plasmodium falciparum-resistant malaria: A review of epidemiologic field evidence. Am J Trop Med Hyg. 2007;77:170-80.
119. Talisuna AO, Langi P, Bakyaita N, Egwang T, Mutabingwa TK, Watkins W, et al. Intensity of malaria transmission, antimalarial-drug use and resistance in Uganda: What is the relationship between these three factors? Trans R Soc Trop Med Hyg. 2002;96:310-7.
120. Artzy-Randrup Y, Alonso D, Pascual M. Transmission intensity and drug resistance in malaria population dynamics: Implications for climate change. PLoS ONE. 2010;5:e13588. doi: 10.1371/journal.pone.0013588.
121. Klein EY, Smith DL, Laxminarayan R, Levin S. Superinfection and the evolution of resistance to antimalarial drugs. Proc Biol Sci. 2012;279:3834-42.
122. Johnston GL, Gething PW, Hay SI, Smith DL, Fidoc DA. Modeling within-host effects of drugs on Plasmodium falciparum transmission and prospects for malaria elimination. PLoS Comput Biol. 2014;10:e1003434. doi: 10.1371/journal.pcbi.1003434.
123. WHO. Malaria Vaccine Funders Group. Malaria vaccine technology roadmap. 2013. http://www.who.int/immunization/topics/malaria/vaccine roadmap/TRM update nov13.pdf of subordinate document. Accessed 6 Sept 2015.
124. Willyard C. Malaria eradication: Blocking transmission to mosquitoes. Pharm J. 2015;294:7843-4.
125. Carter R. Transmission blocking malaria vaccines. Vaccine. 2001;19:2309-14.
126. Pradel G. Proteins of the malaria parasite sexual stages: Expression, function and potential for transmission blocking strategies. Parasitology. 2007;134:1911-29.
127. Saxena AK, Wu Y, Garboczi DN. Plasmodium p25 and p28 surface proteins: Potential transmission-blocking vaccines. Eukaryot Cell. 2007;6:1260-5.
128. Tomas AM, Margos G, Dimopoulos G, van Lin LH, de Koning-Ward TF, Sinha R, et al. P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J. 2001;20:3975-83.
129. Tsai YL, Hayward RE, Langer RC, Fidock DA, Vinetz JM. Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut. Infect Immun. 2001;69:4048-54.
130. Armistead JS, Morlais I, Mathias DK, Jardim JG, Joy J, Fridman A, et al. Antibodies to a single, conserved epitope in Anopheles APN1 inhibit universal transmission of Plasmodium falciparum and Plasmodium vivax malaria. Infect Immun. 2014;82:818-29.
131. Churcher TS, Dawes EJ, Sinden RE, Christophides GK, Koella JC, Basáñez MG. Population biology of malaria within the mosquito: Density-dependent processes and potential implications for transmission-blocking interventions. Malar J. 2010;9:311.
132. Wen EP, Ellis R, Pujar NS. Vaccine development and manufacturing. New York: Wiley; 2015.
133. Wu Y, Ellis RD, Shaffer D, Fontes E, Malkin EM, Mahantyet 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. doi: 10.1371/journal.pone.0002636.
134. Epstein JE, Richie TL. The whole parasite, pre-erythrocytic stage approach to malaria vaccine development: A review. Curr Opin Infect Dis. 2013;26:420-8.
135. Seder RA, Chang LJ, Enama ME, Zephir KL, Sarwar UN, Gordon IJ, et al. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science. 2013;341:1359-65.
136. Wu Y, Przysiecki C, Flanagan E, Bello-Irizarry SN, Ionescu R, Muratova O, et al. Sustained high-titer antibody responses induced by conjugating a malarial vaccine candidate to outer-membrane protein complex. Proc Natl Acad Sci USA. 2006;103:18243-8.
137. Cheru L, Wu Y, Diouf A, Moretz SE, Muratova OV, Song G, et al. The IC50 of anti-Pfs25 antibody in membrane feeding assay varies among species. Vaccine. 2010;28:4423-9.
138. 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;82:1453-9.
139. Theisen M, Roeffen W, Singh SK, 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;32:2623-30.
140. Kocken CH, Jansen J, Kaan AM, Beckers PJ, Ponnudurai T, Kaslow DC, 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.
141. Kaslow DC, Bathurst IC, Lensen T, Ponnudurai T, Barr PJ, Keister DB. Saccharomyces cerevisiae recombinant Pfs25 adsorbed to alum elicits antibodies that block transmission of Plasmodium falciparum. Infect Immun. 1994;62:5576-80.
142. Zou L, Miles AP, Wang J, Stowers AW. Expression of malaria transmission-blocking vaccine antigen Pfs25 in Pichia pastoris for use in human clinical trials. Vaccine. 2003;21:1650-7.
143. Jones RM, Chichester JA, Mett V, Jaje J, Tottey S, Manceva S, et al. A plant-produced Pfs25 VLP malaria vaccine candidate induces persistent transmission blocking antibodies against Plasmodium falciparum in immunized mice. PLoS ONE. 2013;8:e79538. doi: 10.1371/journal.pone.0079538.
144. Gregory JA, Mayfield SP. Developing inexpensive malaria vaccines from plants and algae. Appl Microbiol Biotechnol. 2014;98:1983-90.
145. Cherif MS, Shuaibu MN, Kodama Y, Kurosaki T, Helegbe GK, Kikuchi M, et al. Nanoparticle formulation enhanced protective immunity provoked by PYGPI8p-transamidase related protein (PyTAM) DNA vaccine in Plasmodium yoelii malaria model. Vaccine. 2014;32:1998-2006.
146. Ferraro B, Talbott KT, Balakrishnan A, Cisper N, Morrow MP, Hutnick NA, et al. Inducing humoral and cellular responses to multiple sporozoite and liver-stage malaria antigens using exogenous plasmid DNA. Infect Immun. 2013;81:3709-20.
147. Kongkasuriyachai D, Bartels-Andrews L, Stowers A, Collins WE, Sullivan J, Sattabongkot J, et al. Potent immunogenicity of DNA vaccines encoding Plasmodium vivax transmission-blocking vaccine candidates Pvs25 and Pvs28-evaluation of homologous and heterologous antigen-delivery prime-boost strategy. Vaccine. 2004;22:3205-13.
148. Doolan DL, Hoffman SL. DNA-based vaccines against malaria: Status and promise of the multi-stage malaria DNA vaccine operation. Int J Parasitol. 2001;31:753-62.
149. Nikolaeva D, Draper SJ, Biswas S. Toward the development of effective transmission blocking vaccines for malaria. Expert Rev Vaccines. 2015;14:653-80.
150. Wells TN, Burrows JN, Baird JK. Targeting the hypnozoite reservoir of Plasmodium vivax: The hidden obstacle to malaria elimination. Trends Parasitol. 2010;26:145-51.
151. Clinical trials-U.S. National Institutes of Health. Testing Pfs25-EPA/Alhydrogel as a potential malaria transmission blocking vaccine. https://clinicaltrials.gov/ct2/show/NCT01867463. Accessed 19 Sept 2015.
152. Clinical trials-U.S. National Institutes of Health. Safety and immunogenicity of plant-derived Pfs25 VLP-FhCMB malaria transmission blocking vaccine in healthy adults https://clinicaltrials.gov/ct2/show/NCT02013687. Accessed 19 Sept 2015.
153. WHO. Global malaria vaccine pipeline. World Health Oganization, Geneva. http://www.who.int/vaccine-research/links/Rainbow/en/index.html. Accessed 1 Feb 2016.
154. Kubler-Kielb J, Majadly F, Biesova Z, Mocca CP, Guo C, Nussenzweig R, et al. A bicomponent Plasmodium falciparum investigational vaccine composed of protein-peptide conjugates. Proc Natl Acad Sci USA. 2010;107:1172-7.
155. Theisen M, Roeffen W, Singh SK, 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;32:2623-30.
156. Smith TA, Chitnis N, Briët OJ, Tanner M. Uses of mosquito-stage transmission-blocking vaccines against Plasmodium falciparum. Trends Parasitol. 2011;27:190-6.
157. Nunes JK, Woods C, Carter T, Raphael T, Morin MJ, Diallo D, et al. Development of a transmission-blocking malaria vaccine: Progress, challenges, and the path forward. Vaccine. 2014;32:5531-9.
158. Luísa RC, Hendrickx K. Winged promises: Exploring the discourse on transgenic mosquitoes in Brazil. Technol Soc. 2013;35:118-28.
159. Wang S, Jacobs-Lorena M. Genetic approaches to interfere with malaria transmission by vector mosquitoes. Trends Biotechnol. 2013;31:185-93.
160. Powell JR, Tabachnick WJ. Genetic shifting: A novel approach for controlling vector-borne diseases. Trends Parasitol. 2014;30:282-8.
161. Alphey L. Genetic control of mosquitoes. Annu Rev Entomol. 2014;59:205-14.
162. Zieler H, Keister DB, Dvorak JA, Ribeiro JM. A snake venom phospholipase A(2) blocks malaria parasite development in the mosquito midgut by inhibiting ookinete association with the midgut surface. J Exp Biol. 2001;204:4157-67.
163. Ito J, Ghosh A, Moreira LA, Wimmer EA, Jacobs-Lorena M. Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature. 2002;417:452-5.
164. Knols BG, Bossin HC, Mukabana WR, Robinson AS. Transgenic mosquitoes and the fight against malaria: Managing technology push in a turbulent GMO world. Am J Trop Med Hyg. 2007;77:232-42.
165. Boëte C, Agusto FB, Reeves RG. Impact of mating behaviour on the success of malaria control through a single inundative release of transgenic mosquitoes. J Theor Biol. 2014;347:33-43.
166. Windbichler N, Menichelli M, Papathanos PA, Thyme SB, Li H, Ulge UY, et al. A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature. 2011;473:212-5.
167. Gantza VM, Jasinskiene N, Tatarenkova O, Fazekas A, Macias VM, Bier E, et al. Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc Natl Acad Sci USA. 2015;112:6736-43. doi: 10.1073/pnas.1521077112.
168. Kistler KE, Vosshall LB, Matthews BJ. Genome engineering with CRISPR-Cas9 in the mosquito Aedes aegypti. Cell Rep. 2015;11:51-60.
169. Hammond A, Galizi R, Kyrou K, Simoni A, Siniscalchi C, Katsanos D, et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat Biotechnol. 2016;34:78-83.
170. Durvasula RV, Gumbs A, Panackal A, Kruglov O, Aksoy S, Merrifield RB, et al. Prevention of insect-borne disease: An approach using transgenic symbiotic bacteria. Proc Natl Acad Sci USA. 1997;94:3274-8.
171. Riehle MA, Moreira CK, Lampe D, Lauzon C, Jacobs-Lorena M. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Int J Parasitol. 2007;37:595-603.
172. Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M. Fighting malaria with engineered symbiotic bacteria from vector mosquitoes. Proc Natl Acad Sci USA. 2012;109:12734-9.
173. Ren X, Hoiczyk E, Rasgon JL. Viral paratransgenesis in the malaria vector Anopheles gambiae. PLoS Pathog. 2008;4:e1000135. doi: 10.1371/journal.ppat.1000135.
174. Straif SC, Mbogo CN, Toure AM, Walker ED, Kaufman M, Toure YT, et al. Midgut bacteria in Anopheles gambiae and An. funestus (Diptera: Culicidae) from Kenya and Mali. J Med Entomol. 1998;35:222-6.
175. Yoshida S, Ioka D, Matsuoka H, Endo H, Ishii A. Bacteria expressing single-chain immunotoxin inhibit malaria parasite development in mosquitoes. Mol Biochem Parasitol. 2001;113:89-96.
176. Walker T, Moreira LA. Can Wolbachia be used to control malaria? Mem Inst Oswaldo Cruz. 2011;106:212-7.
177. Fang W, Vega-Rodríguez J, Ghosh AK, Jacobs-Lorena M, Kang A, St Leger RJ. Development of transgenic fungi that kill human malaria parasites in mosquitoes. Science. 2011;331:1074-7.
178. Konrad BP, Lindstrom M, Gumpinger A, Zhu J, Coombs D. Assessing the optimal virulence of malaria-targeting mosquito pathogens: A mathematical study of engineered Metarhizium anisopliae. Malar J. 2014;13:11.
179. Delrieu I, Leboulleux D, Ivinson K, Gessner BD, Malaria Transmission Blocking Vaccine Technical Consultation Group. Design of a Phase III cluster randomized trial to assess the efficacy and safety of a malaria transmission blocking vaccine. Vaccine. 2015;33:1518-26.
180. MalERA Consultative Group on Modeling. A research agenda for malaria eradication: Modeling. PLoS Med. 2011;8:e1000403. doi: 10.1371/journal.pmed.1000403.
181. White LJ, Maude RJ, Pongtavornpinyo W, Saralamba S, Aguas R, Van Effelterre T, et al. The role of simple mathematical models in malaria elimination strategy design. Malar J. 2009;8:212.
182. Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, et al. Reducing Plasmodium falciparum malaria transmission in africa: A model-based evaluation of intervention strategies. PLoS Med. 2010;7:e1000324. doi: 10.1371/journal.pmed.1000324.
183. Najera JÁ, González-Silva M, Alonso PL. Some lessons for the future from the global malaria eradication programme (1955-1969). PLoS Med. 2011;8:e1000412. doi: 10.1371/journal.pmed.1000412.
184. Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, et al. Malaria resurgence: A systematic review and assessment of its causes. Malar J. 2012;11:122.
185. Artzy-Randrup Y, Andrew P, Dobsond AP, Pascua M. Synergistic and antagonistic interactions between bednets and vaccines in the control of malaria. Proc Natl Acad Sci USA. 2015;112:3014-9.
186. Tatem AJ, Smith DL, Gething PW, Kabaria CW, Snow RW, Hay SI. Ranking of elimination feasibility between malaria-endemic countries. Lancet. 2010;376:1579-91.
187. Mills A, Lubell Y, Hanson K. Malaria eradication: The economic, financial and institutional challenge. Malar J. 2008;7:11.
188. WHO. Use of MenAfriVac™ (meningitis A vaccine) in a controlled temperature chain(CTC) during campaigns. 2013. www.who.int/immunization/documents/WHO-IVB-13.04-5-6/en/Accessed 20 Sept 2015.
189. RTS,S Clinical Trials Partnership. Efficacy and safety of RTS, S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: Final results of a phase 3, individually randomised, controlled trial. Lancet. 2015;2015(386):31-45.
190. Penny MA, Verity R, Bever CA, Sauboin C, Galactionova K, Flasche S, et al. Public health impact and cost-effectiveness of the RTS, S/AS01 malaria vaccine: A systematic comparison of predictions from four mathematical models. Lancet. 2016;387:367-75.
191. Reeves RG, Denton JA, Santucci F, Bryk J, Reed FA. Scientific standards and the regulation of genetically modified insects. PLoS Negl Trop Dis. 2012;6:e1502. doi: 10.1371/journal.pntd.0001502.