Challenges in Antimalarial Drug Treatment for Vivax Malaria Control

Trends in Molecular Medicine

Volumn 21, Issue 12, 2015, Pages 776-788

  Popovici, Jean ^a   Ménard, Didier ^a  

^a INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

Author keywords

[No Author keywords available]

Indexed keywords

AMODIAQUINE; ANTIMALARIAL AGENT; ARTEMISININ DERIVATIVE; ATOVAQUONE; CHLOROQUINE; DIHYDROARTEMISININ PLUS PIPERAQUINE; IMIDAZOPYRAZINE DERIVATIVE; MALARIA VACCINE; MEFLOQUINE; PIPERAQUINE; PRIMAQUINE; PROGUANIL; PYRIMETHAMINE; QUININE; SULFADOXINE; TAFENOQUINE;

AFRICA; DISEASE ELIMINATION; DRUG EFFICACY; ERYTHROCYTE; HUMAN; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; INSECTICIDE RESIDUAL SPRAYING; LIVER CELL; MALARIA CONTROL; NEXT GENERATION SEQUENCING; NONHUMAN; OXIDATIVE STRESS; PARASITE; PESTICIDE SPRAYING; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PLASMODIUM VIVAX MALARIA; PRIMATE; RELAPSE; RETICULOCYTE; REVIEW; SCHIZONT; SPOROZOITE; TROPISM; VECTOR CONTROL; BIOLOGICAL MODEL; DISEASE ERADICATION; EPIDEMIC; MALARIA, VIVAX; NEGLECTED DISEASES;

ANTIMALARIALS; DISEASE ERADICATION; EPIDEMICS; HUMANS; MALARIA, VIVAX; MODELS, BIOLOGICAL; NEGLECTED DISEASES;

EID: 84949562066     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2015.10.004     Document Type: Review

References (121)

1. Price R.N., et al. Vivax malaria: neglected and not benign. Am. J. Trop. Med. Hyg. 2007, 77:79-87.
2. Battle K.E., et al. The global public health significance of Plasmodium vivax. Adv. Parasitol. 2012, 80:1-111.
3. Gething P.W., et al. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl. Trop. Dis. 2012, 6:e1814.
4. World Malaria Report 2014, WHO, WHO.
5. PATH Staying the Course? Malaria Research and Development in a Time of Economic Uncertainty 2011, PATH.
6. Carlton J.M., et al. Why Is Plasmodium vivax a neglected tropical disease?. PLoS Negl. Trop. Dis. 2011, 5:e1160.
7. Kitchen S.F. The infection of reticulocytes by Plasmodium Vivax. Am. J. Trop. Med. Hyg. 1938, s1-18:347-359.
8. Malleret B., et al. Significant biochemical, biophysical and metabolic diversity in circulating human cord blood reticulocytes. PLoS ONE 2013, 8:e76062.
9. Malleret B., et al. Plasmodium vivax: restricted tropism and rapid remodeling of CD71-positive reticulocytes. Blood 2015, 19:1314-1324.
10. Wintrobe M.M., Greer J.P. Wintrobe's Clinical Hematology 2009, Lippincott Williams & Wilkins.
11. Anstey N.M., et al. Plasmodium vivax: clinical spectrum, risk factors and pathogenesis. Adv. Parasitol. 2012, 80:151-201.
12. Barber B.E., et al. Parasite biomass-related inflammation, endothelial activation, microvascular dysfunction and disease severity in vivax malaria. PLoS Pathog. 2015, 11:e1004558.
13. Cheng Q., et al. Systematic review of sub-microscopic P. vivax infections: prevalence and determining factors. PLoS Negl. Trop. Dis. 2015, 9:e3413.
14. Abba K., et al. Rapid diagnostic tests for diagnosing uncomplicated non-falciparum or Plasmodium vivax malaria in endemic countries. Cochrane Database Syst. Rev. 2014, 12:CD011431.
15. Wongsrichanalai C., et al. A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT). Am. J. Trop. Med. Hyg. 2007, 77:119-127.
16. Arango E.M., et al. Molecular detection of malaria at delivery reveals a high frequency of submicroscopic infections and associated placental damage in pregnant women from Northwest Colombia. Am. J. Trop. Med. Hyg. 2013, 89:178-183.
17. Thanh P.V., et al. Epidemiology of forest malaria in Central Vietnam: the hidden parasite reservoir. Malar. J. 2015, 14:86.
18. Barbosa S., et al. Epidemiology of disappearing Plasmodium vivax malaria: a case study in rural Amazonia. PLoS Negl. Trop. Dis. 2014, 8:e3109.
19. Russell B., et al. A reliable ex vivo invasion assay of human reticulocytes by Plasmodium vivax. Blood 2011, 118:e74-e81.
20. Cho J-S., et al. Unambiguous determination of Plasmodium vivax reticulocyte invasion by flow cytometry. Int. J. Parasitol. 2015, Published online September 15, 2015. 10.1016/j.ijpara.2015.08.003.
21. Krotoski W.A. Discovery of the hypnozoite and a new theory of malarial relapse. Trans. R. Soc. Trop. Med. Hyg. 1985, 79:1-11.
22. White N.J., Imwong M. Relapse. Adv. Parasitol. 2012, 80:113-150.
23. Yoeli M. Non-pigmented malaria parasites in the bone marrow from a mixed infection of Leishmania and Plasmodium vivax. Trans. R. Soc. Trop. Med. Hyg. 1948, 42:99.
24. 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.
25. Douglas N.M., et al. Chemotherapeutic strategies for reducing transmission of Plasmodium vivax malaria. Adv. Parasitol. 2012, 80:271-300.
26. Pybus B., et al. The metabolism of primaquine to its active metabolite is dependent on CYP 2D6. Malar. J. 2013, 12:212.
27. Potter B.M.J., et al. Differential CYP 2D6 Metabolism alters primaquine pharmacokinetics. Antimicrob. Agents Chemother. 2015, 59:2380-2387.
28. Sistonen J., et al. CYP2D6 worldwide genetic variation shows high frequency of altered activity variants and no continental structure. Pharmacogenet. Genomics 2007, 17:93-101.
29. Bennett J.W., et al. Primaquine failure and cytochrome P-450 2D6 in Plasmodium vivax malaria. N. Engl. J. Med. 2013, 369:1381-1382.
30. Minucci A., et al. Glucose-6-phosphate dehydrogenase (G6PD) mutations database: review of the "old" and update of the new mutations. Blood Cells Mol. Dis. 2012, 48:154-165.
31. Cappellini M.D., Fiorelli G. Glucose-6-phosphate dehydrogenase deficiency. Lancet 2008, 371:64-74.
32. Kheng S., et al. Tolerability and safety of weekly primaquine against relapse of Plasmodium vivax in Cambodians with glucose-6-phosphate dehydrogenase deficiency. BMC Med. 2015, 13:203.
33. Khim N., et al. G6PD deficiency in Plasmodium falciparum and Plasmodium vivax malaria-infected Cambodian patients. Malar. J. 2013, 12:171.
34. Roca-Feltrer A., et al. Field trial evaluation of the performances of point-of-care tests for screening G6PD deficiency in Cambodia. PLoS ONE 2014, 9:e116143.
35. Louicharoen C., et al. Positively selected G6PD-mahidol mutation reduces Plasmodium vivax density in Southeast Asians. Science 2009, 326:1546-1549.
36. Baird J.K., Hoffman S.L. Primaquine therapy for malaria. Clin. Infect. Dis. 2004, 39:1336-1345.
37. John G., et al. Primaquine radical cure of Plasmodium vivax: a critical review of the literature. Malar. J. 2012, 11:280.
38. Llanos-Cuentas A., et al. Tafenoquine plus chloroquine for the treatment and relapse prevention of Plasmodium vivax malaria (DETECTIVE): a multicentre, double-blind, randomised, phase 2b dose-selection study. Lancet 2014, 383:1049-1058.
39. Vuong C., et al. Differential CYP 2D metabolism alters tafenoquine pharmacokinetics. Antimicrob. Agents Chemother. 2015, 59:3864-3869.
40. Rochford R., et al. Humanized mouse model of glucose 6-phosphate dehydrogenase deficiency for in vivo assessment of hemolytic toxicity. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:17486-17491.
41. McNamara C.W., et al. Targeting Plasmodium PI(4)K to eliminate malaria. Nature 2013, 504:248-253.
42. Takala-Harrison S., Laufer M.K. Antimalarial drug resistance in Africa: key lessons for the future. Ann. N. Y. Acad. Sci. 2015, 1342:62-67.
43. Rieckmann K., et al. Plasmodium vivax resistance to chloroquine?. Lancet 1989, 334:1183-1184.
44. Price R.N., et al. Global extent of chloroquine-resistant Plasmodium vivax: a systematic review and meta-analysis. Lancet Infect. Dis. 2014, 14:982-991.
45. Lin J.T., et al. Using amplicon deep sequencing to detect genetic signatures of Plasmodium vivax relapse. J. Infect. Dis. 2015, 212:999-1008.
46. Russell B., et al. Human ex vivo studies on asexual Plasmodium vivax: The best way forward. Int. J. Parasit. 2012, 42:1063-1070.
47. Kerlin D.H., et al. An analytical method for assessing stage-specific drug activity in Plasmodium vivax malaria: implications for ex vivo drug susceptibility testing. PLoS Negl. Trop. Dis. 2012, 6:e1772.
48. Nomura T., et al. Evidence for different mechanisms of chloroquine resistance in 2 Plasmodium species that cause human malaria. J. Infect. Dis. 2001, 183:1653-1661.
49. Barnadas C., et al. Plasmodium vivax resistance to chloroquine in Madagascar: clinical efficacy and polymorphisms in pvmdr1 and pvcrt-o genes. Antimicrob. Agents Chemother. 2008, 52:4233-4240.
50. Melo G.C., et al. Expression levels of pvcrt-o and pvmdr-1 are associated with chloroquine resistance and severe Plasmodium vivax malaria in patients of the Brazilian Amazon. PLoS ONE 2014, 9:e105922.
51. Olafson K.N., et al. Mechanisms of hematin crystallization and inhibition by the antimalarial drug chloroquine. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:4946-4951.
52. Bozdech Z., et al. The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:16290-16295.
53. Gogtay N., et al. Artemisinin-based combination therapy for treating uncomplicated Plasmodium vivax malaria. Cochrane Database Syst. Rev. 2013, 10:Cd008492.
54. Guidelines for the Treatment of Malaria 2015, WHO, WHO. 3rd edn.
55. Chitnis C., Miller L.H. Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte invasion. J. Exp. Med. 1994, 180:497-506.
56. Miller L.H., et al. The resistance factor to Plasmodium vivax in blacks. N. Engl. J. Med. 1976, 295:302-304.
57. Liu W., et al. African origin of the malaria parasite Plasmodium vivax. Nat. Commun. 2014, 5:3346.
58. Culleton R., et al. Evidence for the transmission of Plasmodium vivax in the Republic of the Congo, West Central Africa. J. Infect. Dis. 2009, 200:1465-1469.
59. Culleton R.L., Ferreira P.E. Duffy phenotype and Plasmodium vivax infections in humans and apes, Africa. Emerg. Infect. Dis. 2012, 18:1704.
60. de Cassan S.C., et al. Preclinical assessment of viral vectored and protein vaccines targeting the Duffy-binding protein region II of Plasmodium vivax. Front. Immunol. 2015, 6:348.
61. Ntumngia F.B., et al. Immunogenicity of a synthetic vaccine based on Plasmodium vivax Duffy binding protein region II. Clin. Vaccine Immunol. 2014, 21:1215-1223.
62. Chootong P., et al. The association of Duffy binding protein region II polymorphisms and its antigenicity in Plasmodium vivax isolates from Thailand. Parasitol. Int. 2014, 63:858-864.
63. Ngassa Mbenda H.G., Das A. Molecular evidence of Plasmodium vivax mono and mixed malaria parasite infections in Duffy-negative native Cameroonians. PLoS ONE 2014, 9:e103262.
64. Ménard D., et al. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:5967-5971.
65. Mendes C., et al. Duffy negative antigen is no longer a barrier to Plasmodium vivax - molecular evidences from the African West Coast (Angola and Equatorial Guinea). PLoS Negl. Trop. Dis. 2011, 5:e1192.
66. Carvalho T.A., et al. Plasmodium vivax infection in Anajas, State of Para: no differential resistance profile among Duffy-negative and Duffy-positive individuals. Malar. J. 2012, 11:430.
67. Mason S.J., et al. The Duffy blood group determinants: their role in the susceptibility of human and animal erythrocytes to Plasmodium knowlesi malaria. Br. J. Haematol. 1977, 36:327-335.
68. Menard D., et al. Whole genome sequencing of field isolates reveals a common duplication of the Duffy binding protein gene in Malagasy Plasmodium vivax strains. PLoS Negl. Trop. Dis. 2013, 7:e2489.
69. Hester J., et al. De novo assembly of a field isolate genome reveals novel Plasmodium vivax erythrocyte invasion genes. PLoS Negl. Trop. Dis. 2013, 7:e2569.
70. Devi Y.S., et al. Immunogenicity of Plasmodium vivax combination subunit vaccine formulated with human compatible adjuvants in mice. Vaccine 2007, 25:5166-5174.
71. Vicentin E.C., et al. Invasion-inhibitory antibodies elicited by immunization with Plasmodium vivax apical membrane antigen-1 expressed in Pichia pastoris yeast. Infect. Immun. 2014, 82:1296-1307.
72. Lumsden J., et al. Plasmodium vivax circumsporozoite protein specific cellular immune responses after immunization with the VMP001/AS01B candidate malaria vaccine in malaria-naive individuals. Am. J. Trop. Med. Hyg. 2011, 85(Suppl.):259.
73. Armistead J.S., et al. Antibodies to a single, conserved epitope in Anopheles APN1 inhibit universal transmission of Plasmodium falciparum and Plasmodium vivax malaria. Infect. Immun. 2014, 82:818-829.
74. Hisaeda H., 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.
75. Wu Y., et al. Phase 1 trial of malaria transmission blocking vaccine candidates Pfs25 and Pvs25 formulated with montanide ISA 51. PLoS ONE 2008, 3:e2636.
76. Joyner C.J., et al. No more monkeying around: primate malaria model systems are key to understanding Plasmodium vivax liver-stage biology, hypnozoites, and relapses. Front. Microbiol. 2015, 26:145.
77. Ng S., et al. Human iPSC-derived hepatocyte-like cells support Plasmodium liver-stage infection in vitro. Stem Cell Rep. 2015, 4:348-359.
78. March S., et al. A microscale human liver platform that supports the hepatic stages of Plasmodium falciparum and vivax. Cell Host Microbe 2013, 14:104-115.
79. Maher S.P., et al. Microphysical space of a liver sinusoid device enables simplified long-term maintenance of chimeric mouse-expanded human hepatocytes. Biomed. Microdevices 2014, 16:727-736.
80. Mikolajczak Sebastian A., et al. Plasmodium vivax liver stage development and hypnozoite persistence in human liver-chimeric mice. Cell Host Microbe 2015, 17:526-535.
81. Kaushansky A., et al. Of men in mice: the success and promise of humanized mouse models for human malaria parasite infections. Cell Microbiol. 2014, 16:602-611.
82. Cotter C., et al. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet 2013, 382:900-911.
83. Mueller I., et al. Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect. Dis. 2009, 9:555-566.
84. Noviyanti R., et al. Contrasting transmission dynamics of co-endemic Plasmodium vivax and P. falciparum: implications for malaria control and elimination. PLoS Negl. Trop. Dis. 2015, 9:e0003739.
85. Eliminating Malaria: Case Study 8. Progress Towards Elimination in Malaysia 2012, WHO, WHO.
86. Abeyasinghe R.R., et al. Malaria control and elimination in Sri Lanka: documenting progress and success factors in a conflict setting. PLoS ONE 2012, 7:e43162.
87. Eliminating Malaria: Case Study Series 2012, World Health Organization, WHO.
88. Santa-Olalla Peralta P., et al. First autochthonous malaria case due to Plasmodium vivax since eradication, Spain, October 2010. Euro Surveill. 2010, 15:19684.
89. Danis K., et al. Malaria in Greece: historical and current reflections on a re-emerging vector borne disease. Travel Med. Infect. Dis. 2013, 11:8-14.
90. Shanks G.D. Control and elimination of Plasmodium vivax. Adv. Parasitol. 2012, 80:301-341.
91. Lysenko A., Semashko I. Geography of malaria. A medico-geographic profile of an ancient disease. Itogi Nauki Medicinskaja Geografija 1968, 25-146.
92. Luo Z., et al. The biology of Plasmodium vivax explored through genomics. Ann. N. Y. Acad. Sci. 2015, 1342:53-61.
93. Neafsey D.E., et al. The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat. Genet. 2012, 44:1046-1050.
94. Baniecki M.L., et al. Development of a single nucleotide polymorphism barcode to genotype Plasmodium vivax infections. PLoS Negl. Trop. Dis. 2015, 9:e0003539.
95. Chen J-H., et al. An immunomics approach for the analysis of natural antibody responses to Plasmodium vivax infection. Mol. Biosyst. 2015, 11:2354-2363.
96. Garzón-Ospina D., et al. Inferring natural selection signals in Plasmodium vivax-encoded proteins having a potential role in merozoite invasion. Infect. Genet. Evol. 2015, 33:182-188.
97. Anderson D.C., et al. Plasmodium vivax trophozoite-stage proteomes. J. Proteomics 2015, 115:157-176.
98. Moreno-Pérez D.A., et al. Determining the Plasmodium vivax VCG-1 strain blood stage proteome. J. Proteomics 2015, 113:268-280.
99. Kitchen S.F. Malariology: a comprehensive survey of all aspects of this group of diseases from a global standpoint 1949, 966-1045. WB Saunders Company. M.F. Boyd (Ed.).
100. Rahimi B., et al. Severe vivax malaria: a systematic review and meta-analysis of clinical studies since 1900. Malaria J. 2014, 13:481.
101. Lacerda M.V.G., et al. Postmortem characterization of patients with clinical diagnosis of Plasmodium vivax malaria: to what extent does this parasite kill?. Clin. Infect. Dis. 2012, 55:e67-e74.
102. Siqueira A., et al. Characterization of Plasmodium vivax-associated admissions to reference hospitals in Brazil and India. BMC Med. 2015, 13:57.
103. Baird J.K. Evidence and implications of mortality associated with acute Plasmodium vivax malaria. Clin. Microbiol. Rev. 2013, 26:36-57.
104. Naing C., et al. Is Plasmodium vivax malaria a severe malaria?: A systematic review and meta-analysis. PLoS Negl. Trop. Dis. 2014, 8:e3071.
105. Leder K., et al. Malaria in travellers: a review of the GeoSentinel surveillance network. Clin. Infect. Dis. 2004, 39:1104-1112.
106. Broderick C., et al. Clinical, geographical, and temporal risk factors associated with presentation and outcome of vivax malaria imported into the United Kingdom over 27 years: observational study. BMJ 2015, 350:h1703.
107. Hwang J., et al. Severe morbidity and mortality risk from malaria in the United States, 1985-2011. Open forum infectious diseases 2014, Oxford University Press.
108. Adekunle A.I., et al. Modeling the dynamics of Plasmodium vivax infection and hypnozoite reactivation in vivo. PLoS Negl. Trop. Dis. 2015, 9:e0003595.
109. Douglas N.M., et al. Major burden of severe anemia from non-falciparum malaria species in Southern Papua: a hospital-based surveillance study. PLoS Med. 2013, 10:e1001575.
110. Berliner R.W., et al. Studies on the chemotherapy of the human malarias. VI. The physiological disposition, antimalarial activity, and toxicity of several derivatives of 4-aminoquinoline. J. Clin. Invest. 1948, 27(3 Pt 2):98-107.
111. Baird J.K., et al. Diagnosis of resistance to chloroquine by Plasmodium vivax: timing of recurrence and whole blood chloroquine levels. Am. J. Trop. Med. Hyg. 1997, 56:621-626.
112. Methods for surveillance of antimalarial drug efficacy 2009, WHO.
113. Diagana T.T. Supporting malaria elimination with 21st century antimalarial agent drug discovery. Drug Dis. Today 2015.
114. Leroy D., et al. Defining the biology component of the drug discovery strategy for malaria eradication. Trends Parasitol. 2014, 30:478-490.
115. Clements A.C.A., et al. Further shrinking the malaria map: how can geospatial science help to achieve malaria elimination?. Lancet Infect. Dis. 2013, 13:709-718.
116. Nájera J.A., et al. Some lessons for the future from the Global Malaria Eradication Programme (1955-1969). PLoS Med. 2011, 8:e1000412.
117. Alonso P.L., et al. A research agenda to underpin malaria eradication. PLoS Med. 2011, 8:e1000406.
118. Bhatt S., et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 2015.
119. Sinka M.E., et al. A global map of dominant malaria vectors. Parasit Vector 2012, 5:69.
120. Sutanto I., et al. Efficacy of permethrin-impregnated bed nets on malaria control in a hyperendemic area in Irian Jaya, Indonesia: influence of seasonal rainfall fluctuations. Southeast Asian J. Trop. Med. Public Health 1999, 30:432-439.
121. Luxemburger C., et al. Permethrin-impregnated bed nets for the prevention of malaria in schoolchildren on the Thai-Burmese border. Trans. Royal Soc. Trop. Med. Hyg. 1994, 88:155-159.