Modeling Within-Host Effects of Drugs on Plasmodium falciparum Transmission and Prospects for Malaria Elimination

PLoS Computational Biology

Volumn 10, Issue 1, 2014, Pages

  Johnston, Geoffrey L ^a,b,c   Gething, Peter W ^d   Hay, Simon I ^d   Smith, David L ^c   Fidock, David A ^a  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONTROLLED DRUG DELIVERY; CYTOLOGY; ESTIMATION; TARGETED DRUG DELIVERY;

ARTEMISININ; AT-RISK POPULATION; COMBINATION THERAPY; MECHANISTICS; MOSQUITO VECTORS; PLASMODIUM FALCIPARUM; PLASMODIUM PARASITES; SOUTHEAST ASIA; THEORETICAL FOUNDATIONS; TRANSMISSION REDUCTION;

DISEASES;

ARTEMISININ DERIVATIVE; BENFLUMETOL; CHLOROQUINE; MEFLOQUINE; PRIMAQUINE;

AFRICA SOUTH OF THE SAHARA; ARTICLE; ASEXUAL REPRODUCTION; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; FEVER; GAMETOCYTE; HIGH RISK POPULATION; HOST RANGE; INFECTION RATE; INFECTION RISK; LIFE CYCLE STAGE; MALARIA FALCIPARUM; MATHEMATICAL MODEL; PARASITE CLEARANCE; PARASITE TRANSMISSION; PHARMACODYNAMICS; PHARMACOKINETICS; PLASMODIUM FALCIPARUM; PREDICTION; SIMULATION; SOUTHEAST ASIA;

ALGORITHMS; ANIMALS; ANTIMALARIALS; ASIA, SOUTHEASTERN; COMMUNICABLE DISEASE CONTROL; COMPUTER SIMULATION; CULICIDAE; GEOGRAPHY; HUMANS; MALARIA, FALCIPARUM; MODELS, THEORETICAL; PLASMODIUM FALCIPARUM; SOFTWARE;

EID: 84896703184     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003434     Document Type: Article

References (90)

1. WHO (2012) World malaria report: 2012. Switzerland: WHO Press.
2. Hay SI, Okiro EA, Gething PW, Patil AP, Tatem AJ, et al. (2010) Estimating the global clinical burden of Plasmodium falciparum malaria in 2007. PLoS Med 7: e1000290.
3. Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, et al. (2012) Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413-431.
4. Eastman RT, Fidock DA, (2009) Artemisinin-based combination therapies: a vital tool in efforts to eliminate malaria. Nat Rev Microbiol 7: 864-874.
5. White NJ, (2008) Qinghaosu (artemisinin): the price of success. Science 320: 330-334.
6. Smith DL, Cohen JM, Moonen B, Tatem AJ, Sabot OJ, et al. (2011) Infectious disease. Solving the Sisyphean problem of malaria in Zanzibar. Science 332: 1384-1385.
7. Chiyaka C, Tatem A, Cohen J, (2013) The stability of malaria elimination. Science 339: 909-910.
8. Feachem R, Sabot O, (2008) A new global malaria eradication strategy. Lancet 371: 1633-1635.
9. Feachem RG, Phillips AA, Targett GA, Snow RW, (2010) Call to action: priorities for malaria elimination. Lancet 376: 1517-1521.
10. Dondorp AM, Fairhurst RM, Slutsker L, Macarthur JR, M DJ, et al. (2011) The threat of artemisinin-resistant malaria. N Engl J Med 365: 1073-1075.
11. Trape JF, Tall A, Diagne N, Ndiath O, Ly AB, et al. (2011) Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis 11: 925-932.
12. Paul RE, Hackford I, Brockman A, Muller-Graf C, Price R, et al. (1998) Transmission intensity and Plasmodium falciparum diversity on the northwestern border of Thailand. Am J Trop Med Hyg 58: 195-203.
13. Pigott DM, Atun R, Moyes CL, Hay SI, Gething PW, (2012) Funding for malaria control 2006-2010: A comprehensive global assessment. Malaria J 11: 246.
14. Greenwood BM, Fidock DA, Kyle DE, Kappe SH, Alonso PL, et al. (2008) Malaria: progress, perils, and prospects for eradication. The Journal of clinical investigation 118: 1266-1276.
15. Cohen JM, Moonen B, Snow RW, Smith DL, (2010) How absolute is zero? An evaluation of historical and current definitions of malaria elimination. Malaria J 9: 213.
16. Sabot O, Cohen JML, Hsiang MS, Kahn JG, Basu S, et al. (2010) Costs and financial feasibility of malaria elimination. Lancet 376: 1604-1615.
17. Tatem AJ, Smith DL, Gething PW, Kabaria CW, Snow RW, et al. (2010) Ranking of elimination feasibility between malaria-endemic countries. Lancet 376: 1579-1591.
18. Anonymous (2011) The MalERA Consultative Group on Modeling. A research agenda for malaria eradication: modeling. PLoS Med 8: e1000403.
19. White NJ, (2008) The role of anti-malarial drugs in eliminating malaria. Malaria J 7 Suppl 1: S8.
20. Vale N, Moreira R, Gomes P, (2009) Primaquine revisited six decades after its discovery. Eur J Med Chem 44: 937-953.
21. Adjalley SH, Johnston GL, Li T, Eastman RT, Ekland EH, et al. (2011) Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proc Natl Acad Sci USA 108: E1214-1223.
22. Muller O, Mockenhaupt FP, Marks B, Meissner P, Coulibaly B, et al. (2013) Haemolysis risk in methylene blue treatment of G6PD-sufficient and G6PD-deficient West-African children with uncomplicated falciparum malaria: a synopsis of four RCTs. Pharmacoepidemiology and drug safety 22: 376-385.
23. Johnston GL, Smith DL, Fidock DA, (2013) 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 9: e1003025.
24. Yeung S, Van Damme W, Socheat DD, White NJ, Mills A, (2008) Access to artemisinin combination therapy for malaria in remote areas of Cambodia. Malaria J 7: 96.
25. Wells TN, Alonso PL, Gutteridge WE, (2009) New medicines to improve control and contribute to the eradication of malaria. Nature reviews Drug discovery 8: 879-891.
26. Bousema T, Drakeley C, (2011) Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clinical microbiology reviews 24: 377-410.
27. Bousema T, Okell LC, Shekalaghe S, Griffin JT, Omar SA, et al. (2010) Revisiting the circulation time of Plasmodium falciparum gametocytes: molecular detection methods to estimate the duration of gametocyte carriage and the effect of gametocytocidal drugs. Malaria J 9: 136.
28. Bousema JT, Schneider P, Gouagna LC, Drakeley CJ, Tostmann A, et al. (2006) Moderate effect of artemisinin-based combination therapy on transmission of Plasmodium falciparum. J Infect Dis 193: 1151-1159.
29. Molineaux L, Diebner HH, Eichner M, Collins WE, Jeffery GM, et al. (2001) Plasmodium falciparum parasitaemia described by a new mathematical model. Parasitology 122: 379-391.
30. Targett G, Drakeley C, Jawara M, von Seidlein L, Coleman R, et al. (2001) Artesunate reduces but does not prevent posttreatment transmission of Plasmodium falciparum to Anopheles gambiae. J Infect Dis 183: 1254-1259.
31. Drakeley CJ, Jawara M, Targett GaT, Walraven G, Obisike U, et al. (2004) Addition of artesunate to chloroquine for treatment of Plasmodium falciparum malaria in Gambian children causes a significant but short-lived reduction in infectiousness for mosquitoes. Trop Med Int Health 9: 53-61.
32. Sutherland CJ, Ord R, Dunyo S, Jawara M, Drakeley CJ, et al. (2005) Reduction of malaria transmission to Anopheles mosquitoes with a six-dose regimen of co-artemether. PLoS Med 2: e92.
33. Hallett R, Dunyo S, Ord R, Jawara M, Pinder M, et al. (2006) Chloroquine/sulphadoxine-pyrimethamine for Gambian children with malaria: transmission to mosquitoes of multidrug-resistant Plasmodium falciparum. PLoS Clin Trials 1: E14.
34. Piyaphanee W, Krudsood S, Tangpukdee N, Thanachartwet W, Silachamroon U, et al. (2006) Emergence and clearance of gametocytes in uncomplicated Plasmodium falciparum malaria. Am J Trop Med Hyg 74: 432-435.
35. Shekalaghe S, Drakeley C, Gosling R, Ndaro A, van Meegeren M, et al. (2007) Primaquine clears submicroscopic Plasmodium falciparum gametocytes that persist after treatment with sulphadoxine-pyrimethamine and artesunate. PLoS ONE 2: 1-8.
36. Smithuis F, Kyaw MK, Phe O, Win T, Aung PP, et al. (2010) Effectiveness of five artemisinin combination regimens with or without primaquine in uncomplicated falciparum malaria: an open-label randomised trial. Lancet Infect Dis 10: 673-681.
37. Sawa P, Shekalaghe Sa, Drakeley CJ, Sutherland CJ, Mweresa CK, et al. (2013) Malaria transmission after artemether-lumefantrine and dihydroartemisinin-piperaquine: a randomized trial. J Infect Dis 10.1093/infdis/jit077: 1-9.
38. Sutanto I, Suprijanto S, Kosasih A, Dahlan MS, Syafruddin D, et al. (2013) The effect of primaquine on gametocyte development and clearance in the treatment of uncomplicated falciparum malaria with dihydroartemisinin-piperaquine in South sumatra, Western indonesia: an open-label, randomized, controlled trial. Clin Infect Dis 56: 685-693.
39. Lawpoolsri S, Klein EY, Singhasivanon P, Yimsamran S, Thanyavanich N, et al. (2009) Optimally timing primaquine treatment to reduce Plasmodium falciparum transmission in low endemicity Thai-Myanmar border populations. Malaria J 8: 159.
40. Smith T, Ross A, Maire N, Chitnis N, Studer A, et al. (2012) Ensemble modeling of the likely public health impact of a pre-erythrocytic malaria vaccine. PLoS Med 9: e1001157.
41. Gurarie D, Karl S, Zimmerman Pa, King CH, St Pierre TG, et al. (2012) Mathematical modeling of malaria infection with innate and adaptive immunity in individuals and agent-based communities. PLoS ONE 7: e34040.
42. Okell LC, Ghani AC, Lyons E, Drakeley CJ, (2009) Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis 200: 1509-1517.
43. White NJ, Qiao LG, Qi G, Luzzatto L, (2012) Rationale for recommending a lower dose of primaquine as a Plasmodium falciparum gametocytocide in populations where G6PD deficiency is common. Malaria J 11: 418.
44. White NJ, (2013) Primaquine to prevent transmission of falciparum malaria. Lancet Infect Dis 13: 175-181.
45. Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IR, et al. (2011) A new world malaria map: Plasmodium falciparum endemicity in 2010. Malaria J 10: 378.
46. Smith DL, Hay SI, (2009) Endemicity response timelines for Plasmodium falciparum elimination. Malaria J 8: 87.
47. Smith DL, McKenzie FE, Snow RW, Hay SI, (2007) Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS biology 5: e42.
48. Luxemburger C, Ricci F, Nosten F, Raimond D, Bathet S, et al. (1997) The epidemiology of severe malaria in an area of low transmission in Thailand. Trans R Soc Trop Med Hyg 91: 256-262.
49. Verhage DF, Telgt DSC, Bousema JT, Hermsen CC, van Gemert GJA, et al. (2005) Clinical outcome of experimental human malaria induced by Plasmodium falciparum-infected mosquitoes. Neth J Med 63: 52-58.
50. Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, et al. (2010) Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med 7: e1000324.
51. Maude RJ, Socheat D, Nguon C, Saroth P, Dara P, et al. (2012) Optimising strategies for Plasmodium falciparum malaria elimination in Cambodia: primaquine, mass drug administration and artemisinin resistance. PLoS One 7: e37166.
52. Phyo AP, Nkhoma S, Stepniewska K, Ashley EA, Nair S, et al. (2012) Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet 379: 1960-1966.
53. Fidock DA, (2013) Malaria elimination. Science 340: 1531-1533.
54. Diebner HH, Eichner M, Molineaux L, Collins WE, Jeffery GM, et al. (2000) Modelling the transition of asexual blood stages of Plasmodium falciparum to gametocytes. J Theor Biol 202: 113-127.
55. Eichner M, Diebner HH, Molineaux L, Collins WE, Jeffery GM, et al. (2001) Genesis, sequestration and survival of Plasmodium falciparum gametocytes: parameter estimates from fitting a model to malariatherapy data. Trans R Soc Trop Med Hyg 95: 497-501.
56. Smith TA, Killeen GF, Maire N, Ross A, Molineaux L, et al. (2006) Mathematical modeling of the impact of malaria vaccines on the clinical epidemiology and natural history of Plasmodium falciparum malaria: overview. Am J Trop Med Hyg 75: 1-10.
57. Crooks L, (2008) Problems with continuous-time malaria models in describing gametocytogenesis. Parasitology 135: 881-896.
58. Kay K, Hastings IM, (2013) Improving pharmacokinetic-pharmacodynamic modeling to investigate anti-infective chemotherapy with application to the current generation of antimalarial drugs. PLoS Comput Biol 9: e1003151.
59. Winter K, Hastings IM, (2011) Development, evaluation, and application of an in silico model for antimalarial drug treatment and failure. Antimicrob Agents Chemother 55: 3380-3392.
60. Karunajeewa HA, Ilett KF, Mueller I, Siba P, Law I, et al. (2008) Pharmacokinetics and efficacy of piperaquine and chloroquine in Melanesian children with uncomplicated malaria. Antimicrob Agents Chemother 52: 237-243.
61. Ezzet F, van Vugt M, Nosten F, Looareesuwan S, White NJ, (2000) Pharmacokinetics and pharmacodynamics of lumefantrine (benflumetol) in acute falciparum malaria. Antimicrob Agents Chemother 44: 697-704.
62. Krudsood S, Looareesuwan S, Tangpukdee N, Wilairatana P, Phumratanaprapin W, et al. (2010) New fixed-dose artesunate-mefloquine formulation against multidrug-resistant Plasmodium falciparum in adults: a comparative phase IIb safety and pharmacokinetic study with standard-dose nonfixed artesunate plus mefloquine. Antimicrob Agents Chemother 54: 3730-3737.
63. Gutman J, Green M, Durand S, Rojas OV, Ganguly B, et al. (2009) Mefloquine pharmacokinetics and mefloquine-artesunate effectiveness in Peruvian patients with uncomplicated Plasmodium falciparum malaria. Malaria J 8: 58.
64. Prinz H, (2010) Hill coefficients, dose-response curves and allosteric mechanisms. J Chem Biol 3: 37-44.
65. Simpson JAA, Watkins ERR, Price RNN, Aarons L, Kyle DEE, et al. (2000) Mefloquine pharmacokinetic-pharmacodynamic models: implications for dosing and resistance. Antimicrob Agents Chemother 44: 3414.
66. Hoshen MB, Stein WD, Ginsburg HD, (2001) Pharmacokinetic-pharmacodynamic modelling of the antimalarial activity of mefloquine. Parasitology 123: 337-346.
67. Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, et al. (2012) Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med 9: e1001165.
68. Beavogui A, Djimde A, Gregson A, (2010) Low infectivity of Plasmodium falciparum gametocytes to Anopheles gambiae following treatment with sulfadoxine-pyrimethamine in Mali. Int J Parasitol 40: 1213-1220.
69. Kone A, van de Vegte-Bolmer M, Siebelink-Stoter R, van Gemert G-J, Dara A, et al. (2010) Sulfadoxine-pyrimethamine impairs Plasmodium falciparum gametocyte infectivity and Anopheles mosquito survival. Int J Parasitol 40: 1221-1228.
70. Delves M, Plouffe D, Scheurer C, Meister S, Wittlin S, et al. (2012) The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites. PLoS Med 9: e1001169.
71. Ezzet F, Mull R, Karbwang J, (1998) Population pharmacokinetics and therapeutic response of CGP 56697 (artemether+benflumetol) in malaria patients. Brit J Clin Pharmacol 46: 553-561.
72. White NJ, van Vugt M, Ezzet F, (1999) Clinical pharmacokinetics and pharmacodynamics and pharmacodynamics of artemether-lumefantrine. Clin Pharmacokinet 37: 105-125.
73. Newton P, Suputtamongkol Y, Teja-Isavadharm P, Pukrittayakamee S, Navaratnam V, et al. (2000) Antimalarial bioavailability and disposition of artesunate in acute falciparum malaria. Antimicrob Agents Chemother 44: 972-977.
74. van Vugt M, Brockman A, Gemperli B, Luxemburger C, Gathmann I, et al. (1998) Randomized comparison of artemether-benflumetol and artesunate-mefloquine in treatment of multidrug-resistant falciparum malaria. Antimicrob Agents Chemother 42: 135-139.
75. Lefevre G, Looareesuwan S, Treeprasertsuk S, Krudsood S, Silachamroon U, et al. (2001) A clinical and pharmacokinetic trial of six doses of artemether-lumefantrine for multidrug-resistant Plasmodium falciparum malaria in Thailand. Am J Trop Med Hyg 64: 247-256.
76. Lefevre G, Bindschedler M, Ezzet F, Schaeffer N, Meyer I, et al. (2000) Pharmacokinetic interaction trial between co-artemether and mefloquine. Eur J Pharm Sci 10: 141-151.
77. Ashley EA, Stepniewska K, Lindegardh N, McGready R, Hutagalung R, et al. (2006) Population pharmacokinetic assessment of a new regimen of mefloquine used in combination treatment of uncomplicated falciparum malaria. Antimicrob Agents Chemother 50: 2281-2285.
78. Thummers B, (2006) DataThiefIII.
79. Bertrand J, Mentre F (2008) Mathematical expressions of the pharmacokinetic and pharmacodynamic models implemented in the Monolix software. Available at: http://wwwfacmuclacbe/cooperation/Vietnam/WBI-Vietnam-October-2011/Modelling/Monolix32_PKPD_librarypdf.
80. Price RN, Uhlemann AC, van Vugt M, Brockman A, Hutagalung R, et al. (2006) Molecular and pharmacological determinants of the therapeutic response to artemether-lumefantrine in multidrug-resistant Plasmodium falciparum malaria. Clin Infect Dis 42: 1570-1577.
81. Hoshen MB, Stein WD, Ginsburg H, (1998) Modelling the chloroquine chemotherapy of falciparum malaria: the value of spacing a split dose. Parasitology 116 (Pt 5):: 407-416.
82. Sidhu AB, Verdier-Pinard D, Fidock DA, (2002) Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298: 210-213.
83. Bustos MD, Gay F, Diquet B, (1994) In vitro tests on Philippine isolates of Plasmodium falciparum against four standard antimalarials and four qinghaosu derivatives. Bull WHO 72: 729-735.
84. van Agtmael MA, Cheng-Qi S, Qing JX, Mull R, van Boxtel CJ, (1999) Multiple dose pharmacokinetics of artemether in Chinese patients with uncomplicated falciparum malaria. Int J Antimicrob Agents 12: 151-158.
85. Cousin M, Kummerer S, Lefevre G, Marrast AC, Stein D, et al. (2008) Anti-infective drugs advisory committee meeting: Coartem (artemether-lumefantrine) tablets for the treatment of malaria in patients with acute, uncomplicated infections due to Plasmodium falciparum or mixed infections including P. falciparum. Available at: http://wwwfdagov/ohrms/dockets/ac/08/briefing/2008-4388b1-02-Novartispdf [Accessed November 1, 2012]: 117.
86. ter Kuile FO, Nosten F, Thieren M, Luxemburger C, Edstein MD, et al. (1992) High-dose mefloquine in the treatment of multidrug-resistant falciparum malaria. J Infect Dis 166: 1393-1400.
87. White NJ, (1997) Assessment of the pharmacodynamic properties of antimalarial drugs in vivo. Antimicrob Agents Chemother 41: 1413-1422.
88. Okell LC, Drakeley CJ, Ghani AC, Bousema T, Sutherland CJ, (2008) Reduction of transmission from malaria patients by artemisinin combination therapies: a pooled analysis of six randomized trials. Malaria J 7: 125.
89. Hallett RL, Sutherland CJ, Alexander N, Ord R, Jawara M, et al. (2004) Combination therapy counteracts the enhanced transmission of drug-resistant malaria parasites to mosquitoes. Antimicrob Agents Chemother 48: 3940-3943.
90. van Pelt-Koops JC, Pett HE, Graumans W, van der Vegte-Bolmer M, van Gemert GJ, et al. (2012) The spiroindolone drug candidate NITD609 potently inhibits gametocytogenesis and blocks Plasmodium falciparum transmission to anopheles mosquito vector. Antimicrob Agents Chemother 56: 3544-3548.