A framework for assessing the risk of resistance for anti-malarials in development

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Ding, Xavier C ^a   Ubben, David ^a   Wells, Timothy Nc ^a  

^a Medicines for Malaria Venture   (Switzerland)

Author keywords

Drug development; P. falciparum; Resistance; Risk assessment

Indexed keywords

ANTIMALARIAL AGENT; ARTEMETHER PLUS BENFLUMETOL; ARTEMISININ; ATOVAQUONE; BENFLUMETOL; CHLOROQUINE; PIPERAQUINE;

ARTICLE; CROSS RESISTANCE; DRUG RESISTANCE; IC 50; IN VITRO STUDY; NONHUMAN; PARASITE CLEARANCE; PLASMODIUM FALCIPARUM; RISK ASSESSMENT;

ANTIMALARIALS; DRUG DISCOVERY; DRUG RESISTANCE; PLASMODIUM FALCIPARUM; RISK ASSESSMENT; TECHNOLOGY, PHARMACEUTICAL;

EID: 84865176348     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-292     Document Type: Article

References (74)

1. Spread and evolution of Plasmodium falciparum drug resistance. Mita T, Tanabe K, Kita K, Parasitol Int 2009 58 201 209 10.1016/j.parint.2009.04.004 19393762
2. World Health Organization, Global report on antimalarial drug efficacy and drug resistance: 2000-2010 WHO, Geneva 2010 121
3. Clinical studies of atovaquone, alone or in combination with other antimalarial drugs, for treatment of acute uncomplicated malaria in Thailand. Looareesuwan S, Viravan C, Webster HK, Kyle DE, Hutchinson DB, Canfield CJ, AmJTrop Med Hyg 1996 54 62
4. Mutations in Plasmodium falciparum cytochrome b that are associated with atovaquone resistance are located at a putative drug-binding site. Korsinczky M, Chen N, Kotecka B, Saul A, Rieckmann K, Cheng Q, Antimicrob Agents Chemother 2000 44 2100 2108 10.1128/AAC.44.8.2100-2108.2000 10898682 (Pubitemid 30484433)
5. Plasmodium sensitivity to artemisinins: magic bullets hit elusive targets. Ding XC, Beck H-P, Raso G, Trends Parasitol 2011 27 73 81 10.1016/j.pt.2010.11.006 21169061
6. Evidence of artemisinin-resistant malaria in Western Cambodia. Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM, Artemisinin Resistance in Cambodia 1 (ARC1) Study Consortium, N Engl J Med 2008 359 2619 2620 10.1056/NEJMc0805011 19064625
7. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Phyo AP, Nkhoma S, Stepniewska K, Ashley EA, Nair S, McGready R, Ler Moo C, Al-Saai S, Dondorp AM, Lwin KM, Singhasivanon P, Day NPJ, White NJ, Anderson TJC, Nosten F, Lancet 2012 379 1960 1966 10.1016/S0140-6736(12)60484-X 22484134
8. A major genome region underlying artemisinin resistance in malaria. Cheeseman IH, Miller BA, Nair S, Nkhoma S, Tan A, Tan JC, Saai Al S, Phyo AP, Moo CL, Lwin KM, McGready R, Ashley E, Imwong M, Stepniewska K, Yi P, Dondorp AM, Mayxay M, Newton PN, White NJ, Nosten F, Ferdig MT, Anderson TJC, Science 2012 336 79 82 10.1126/science.1215966 22491853
9. Increased gametocytemia after treatment: an early parasitological indicator of emerging sulfadoxine-pyrimethamine resistance in falciparum malaria. Barnes KI, Little F, Mabuza A, Mngomezulu N, Govere J, Durrheim D, Roper C, Watkins B, White NJ, J Infect Dis 2008 197 1605 1613 10.1086/587645 18471066 (Pubitemid 351706492)
10. Strategies for the prevention of antimalarial drug resistance: Rationale for combination chemotherapy for malaria. White N, Parasitol Today 1996 12 399 401 10.1016/0169-4758(96)10055-7 15275291 (Pubitemid 26306804)
11. Drug resistant falciparum malaria: clinical consequences and strategies for prevention. Price RN, Nosten F, Drug Resist Updat 2001 4 187 196 10.1054/drup.2001.0195 11768332 (Pubitemid 33089456)
12. Do we need to put society first? The potential for tragedy in antimicrobial resistance. Foster KR, Grundmann H, PLoS Med 2006 3 29 10.1371/journal.pmed.0030029 16398572 (Pubitemid 43362869)
13. Benefits of using multiple first-line therapies against malaria. Boni MF, Smith DL, Laxminarayan R, Proc Natl Acad Sci USA 2008 105 14216 14221 10.1073/pnas.0804628105 18780786
14. The de novo selection of drug-resistant malaria parasites. White NJ, Pongtavornpinyo W, Proc R Soc B: Biol Sci 2003 270 545 554 10.1098/rspb.2002. 2241 (Pubitemid 36308233)
15. The evolution of multiple drug resistance in malaria parasites. Mackinnon MJ, Hastings IM, Trans R Soc Trop Med Hyg 1998 92 188 195 10.1016/S0035- 9203(98)90745-3 9764331 (Pubitemid 28202428)
16. Prospective strategies to delay the evolution of anti-malarial drug resistance: weighing the uncertainty. Smith DL, Klein EY, McKenzie FE, Laxminarayan R, Malar J 2010 9 217 10.1186/1475-2875-9-217 20653960
17. Quantitative dissection of clone-specific growth rates in cultured malaria parasites. Reilly HB, Wang H, Steuter JA, Marx AM, Ferdig MT, Int J Parasitol 2007 37 1599 1607 10.1016/j.ijpara.2007.05.003 17585919 (Pubitemid 47538567)
18. Molecular basis of differential resistance to cycloguanil and pyrimethamine in Plasmodium falciparum malaria. Peterson DS, Milhous WK, Wellems TE, Proc Natl Acad Sci USA 1990 87 3018 3022 10.1073/pnas.87.8.3018 2183222
19. Contribution of the pfmdr1 gene to antimalarial drug-resistance. Duraisingh MT, Cowman AF, Acta Trop 2005 94 181 190 10.1016/j.actatropica.2005. 04.008 15876420 (Pubitemid 40720325)
20. Sulfadoxine resistance in the human malaria parasite Plasmodium falciparum is determined by mutations in dihydropteroate synthetase and an additional factor associated with folate utilization. Wang P, Read M, Sims PF, Hyde JE, Mol Microbiol 1997 23 979 986 10.1046/j.1365-2958.1997.2821646.x 9076734 (Pubitemid 27096733)
21. Allelic exchange at the endogenous genomic locus in Plasmodium falciparum proves the role of dihydropteroate synthase in sulfadoxine-resistant malaria. Triglia T, Wang P, Sims PF, Hyde JE, Cowman AF, EMBO J 1998 17 3807 3815 10.1093/emboj/17.14.3807 9669998 (Pubitemid 28333967)
22. Resistance to antimalarial compounds: Methods and applications. Witkowski B, Berry A, Benoit-Vical F, Drug Resist Updat 2009 12 42 50 10.1016/j.drup.2009.01.001 19285915
23. Antimalarial drug susceptibility testing of Plasmodium falciparum in Brazil using a radioisotope method. Cerutti Junior C, Marques C, Alencar FE, Durlacher RR, Alween A, Segurado AA, Pang LW, Zalis MG, Mem Inst Oswaldo Cruz 1999 94 803 809 10.1590/S0074-02761999000600017 10585659 (Pubitemid 129618929)
24. Spiroindolones, a potent compound class for the treatment of malaria. Rottmann M, McNamara C, Yeung BKS, Lee MCS, Zou B, Russell B, Seitz P, Plouffe DM, Dharia NV, Tan J, Cohen SB, Spencer KR, Gonzalez-Paez GE, Lakshminarayana SB, Goh A, Suwanarusk R, Jegla T, Schmitt EK, Beck HP, Brun R, Nosten F, Renia L, Dartois V, Keller TH, Fidock DA, Winzeler EA, Diagana TT, Science 2010 329 1175 1180 10.1126/science.1193225 20813948
25. Chloroquine sensitivity of isolates of Plasmodium falciparum adapted to in vitro culture. Ponnudurai T, Leeuwenberg AD, Meuwissen JH, Trop Geogr Med 1981 33 50 54 7018038 (Pubitemid 11091208)
26. Plasmodium falciparum: cloning by single-erythrocyte micromanipulation and heterogeneity in vitro. Oduola AM, Weatherly NF, Bowdre JH, Desjardins RE, Exp Parasitol 1988 66 86 95 10.1016/0014-4894(88)90053-7 3284758
27. Gametocyte-forming and non-gametocyte-forming clones of Plasmodium falciparum. Bhasin VK, Trager W, AmJTrop Med Hyg 1984 33 534 537 (Pubitemid 14053343)
28. Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Burkot TR, Williams JL, Schneider I, Trans R Soc Trop Med Hyg 1984 78 339 341 10.1016/0035-9203(84)90114-7 6380022
29. A developmental defect in Plasmodium falciparum male gametogenesis. Guinet F, Dvorak JA, Fujioka H, Keister DB, Muratova O, Kaslow DC, Aikawa M, Vaidya AB, Wellems TE, J Cell Biol 1996 135 269 278 10.1083/jcb.135.1.269 8858179 (Pubitemid 26337753)
30. Cloning of naturally occurring mixed infections of malaria parasites. Rosario V, Science 1981 212 1037 1038 10.1126/science.7015505 7015505 (Pubitemid 11078016)
31. Resistance of ten Thai isolates of Plasmodium falciparum to chloroquine and pyrimethamine by in vitro tests. Thaithong S, Beale GH, Trans R Soc Trop Med Hyg 1981 75 271 273 10.1016/0035-9203(81)90333-3 7029802
32. The activity of pyrimethamine and sulphadoxine against Plasmodium falciparum determined by the in vitro microtechnique. Eastham GM, Rieckmann KH, Trans R Soc Trop Med Hyg 1983 77 91 93 10.1016/0035-9203(83)90026-3 6344364 (Pubitemid 13128374)
33. Identification of a mutant PfCRT-mediated chloroquine tolerance phenotype in Plasmodium falciparum. Valderramos SG, Valderramos J-C, Musset L, Purcell LA, Mercereau-Puijalon O, Legrand E, Fidock DA, PLoS Pathog 2010 6 1000887 10.1371/journal.ppat.1000887 20485514
34. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Fidock DA, Nomura T, Talley AK, Cooper RA, Dzekunov SM, Ferdig MT, Ursos LM, Sidhu AB, Naudé B, Deitsch KW, Su XZ, Wootton JC, Roepe PD, Wellems TE, Mol Cell 2000 6 861 871 10.1016/S1097-2765(05)00077-8 11090624
35. Identification and functional validation of the novel antimalarial resistance locus PF10-0355 in Plasmodium falciparum. Van Tyne D, Park DJ, Schaffner SF, Neafsey DE, Angelino E, Cortese JF, Barnes KG, Rosen DM, Lukens AK, Daniels RF, Milner DA, Johnson CA, Shlyakhter I, Grossman SR, Becker JS, Yamins D, Karlsson EK, Ndiaye D, Sarr O, Mboup S, Happi C, Furlotte NA, Eskin E, Kang HM, Hartl DL, Birren BW, Wiegand RC, Lander ES, Wirth DF, Volkman SK, Sabeti PC, PLoS Genet 2011 7 1001383 10.1371/journal.pgen.1001383 21533027
36. Role of pfmdr1 amplification and expression in induction of resistance to artemisinin derivatives in Plasmodium falciparum. Chavchich M, Gerena L, Peters J, Chen N, Cheng Q, Kyle DE, Antimicrob Agents Chemother 2010 54 2455 2464 10.1128/AAC.00947-09 20350946
37. Genetic linkage of pfmdr1 with food vacuolar solute import in Plasmodium falciparum. Rohrbach P, Sanchez CP, Hayton K, Friedrich O, Patel J, Sidhu ABS, Ferdig MT, Fidock DA, Lanzer M, EMBO J 2006 25 3000 3011 10.1038/sj.emboj. 7601203 16794577 (Pubitemid 44106753)
38. Antifolate-resistant mutants of Plasmodium falciparum dihydrofolate reductase. Sirawaraporn W, Sathitkul T, Sirawaraporn R, Yuthavong Y, Santi DV, Proc Natl Acad Sci USA 1997 94 1124 1129 10.1073/pnas.94.4.1124 9037017 (Pubitemid 27087815)
39. Primary structure and expression of the dihydropteroate synthetase gene of Plasmodium falciparum. Triglia T, Cowman AF, Proc Natl Acad Sci USA 1994 91 7149 7153 10.1073/pnas.91.15.7149 8041761 (Pubitemid 24226820)
40. Mutations in dihydropteroate synthase are responsible for sulfone and sulfonamide resistance in Plasmodium falciparum. Triglia T, Menting JG, Wilson C, Cowman AF, Proc Natl Acad Sci USA 1997 94 13944 13949 10.1073/pnas.94.25. 13944 9391132 (Pubitemid 28009689)
41. Pyrosequencing, a high-throughput method for detecting single nucleotide polymorphisms in the dihydrofolate reductase and dihydropteroate synthetase genes of Plasmodium falciparum. Zhou Z, Poe AC, Limor J, Grady KK, Goldman I, McCollum AM, Escalante AA, Barnwell JW, Udhayakumar V, J Clin Microbiol 2006 44 3900 3910 10.1128/JCM.01209-06 16957045 (Pubitemid 44737226)
42. Ex vivo drug susceptibility of ferroquine against chloroquine-resistant isolates of Plasmodium falciparum and P. vivax. Marfurt J, Chalfein F, Prayoga P, Wabiser F, Kenangalem E, Piera KA, MacHunter B, Tjitra E, Anstey NM, Price RN, Antimicrob Agents Chemother 2011 55 4461 4464 10.1128/AAC.01375-10 21730116
43. Paget-McNicol SM, Estimation of mutation and switching rates in Plasmodium falciparum genes. PhD thesis School of Population Health, The University of Queensland 2001
44. Mutation rates in the dihydrofolate reductase gene of Plasmodium falciparum. Paget-McNicol S, Saul A, Parasitology 2001 122 497 505 11393822 (Pubitemid 32531307)
45. The population genetics of structural variation. Donald F, Conrad MEH, Nat Genet 2007 39 30 10.1038/ng2042 17597779 (Pubitemid 47014472)
46. Gene copy number variation throughout the Plasmodium falciparum genome. Cheeseman IH, Gomez-Escobar N, Carret CK, Ivens A, Stewart LB, Tetteh KK, Conway DJ, BMC Genomics 2009 10 353 10.1186/1471-2164-10-353 19653891
47. Variations in frequencies of drug resistance in Plasmodium falciparum. Rathod PK, McErlean T, Lee PC, Proc Natl Acad Sci USA 1997 94 9389 9393 10.1073/pnas.94.17.9389 9256492 (Pubitemid 27357839)
48. Validation of isoleucine utilization targets in Plasmodium falciparum. Istvan ES, Dharia NV, Bopp SE, Gluzman I, Winzeler EA, Goldberg DE, Proc Natl Acad Sci USA 2011 108 1627 10.1073/pnas.1011560108 21205898
49. Piperaquine resistance is associated with a copy number variation on chromosome 5 in drug-pressured Plasmodium falciparum parasites. Eastman RT, Dharia NV, Winzeler EA, Fidock DA, Antimicrob Agents Chemother 2011 55 3908 3916 10.1128/AAC.01793-10 21576453
50. Defective DNA repair as a potential mechanism for the rapid development of drug resistance in Plasmodium falciparum. Trotta RF, Brown ML, Terrell JC, Geyer JA, Biochemistry 2004 43 4885 4891 10.1021/bi0499258 15109245 (Pubitemid 38544442)
51. Cyclopropyl carboxamides, a chemically novel class of antimalarial agents identified in a phenotypic screen. Sanz LM, Jimenez-Diaz MB, Crespo B, De-Cozar C, Almela MJ, Angulo-Barturen I, Castaneda P, Ibanez J, Fernandez EP, Ferrer S, Herreros E, Lozano S, Martinez MS, Rueda L, Burrows JN, Garcia-Bustos JF, Gamo FJ, Antimicrob Agents Chemother 2011 55 5740 5745 10.1128/AAC.05188-11 21968362
52. Alternative mutations at position 76 of the vacuolar transmembrane protein PfCRT are associated with chloroquine resistance and unique stereospecific quinine and quinidine responses in Plasmodium falciparum. Cooper RA, Ferdig MT, Su X-Z, Ursos LMB, Mu J, Nomura T, Fujioka H, Fidock DA, Roepe PD, Wellems TE, Mol Pharmacol 2002 61 35 42 10.1124/mol.61.1.35 11752204 (Pubitemid 34049510)
53. Persistence of drug-resistant malaria parasites. Rosario VE, Hall R, Walliker D, Beale GH, Lancet 1978 1 185 187 74609
54. Fitness of drug-resistant malaria parasites. Walliker D, Hunt P, Babiker H, Acta Trop 2005 94 251 259 10.1016/j.actatropica.2005.04.005 15845348 (Pubitemid 40723640)
55. Chemotherapy, within-host ecology and the fitness of drug-resistant malaria parasites. Huijben S, Nelson WA, Wargo AR, Sim DG, Drew DR, Read AF, Evolution 2010 64 2952 2968 20584075
56. Estimating SNP proportions in populations of malaria parasites by sequencing: validation and applications. Hunt P, Fawcett R, Carter R, Walliker D, Mol Biochem Parasitol 2005 143 173 182 10.1016/j.molbiopara.2005.05.014 16061293 (Pubitemid 41206471)
57. Real-time quantitative PCR for analysis of genetically mixed infections of malaria parasites: technique validation and applications. Cheesman SJ, de Roode JC, Read AF, Carter R, Mol Biochem Parasitol 2003 131 83 91 10.1016/S0166-6851(03)00195-6 14511807 (Pubitemid 37159323)
58. Mutations in cytochrome b resulting in atovaquone resistance are associated with loss of fitness inPlasmodium falciparum. Peters JM, Chen N, Gatton M, Korsinczky M, Fowler EV, Manzetti S, Saul A, Cheng Q, Antimicrob Agents Chemother 2002 46 2435 2441 10.1128/AAC.46.8.2435-2441.2002 12121915 (Pubitemid 34793446)
59. The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites. Delves M, Plouffe D, Scheurer C, Meister S, Wittlin S, Winzeler EA, Sinden RE, Leroy D, PLoS Med 2012 9 1001169 10.1371/journal.pmed.1001169 22363211
60. The chemotherapy of rodent malaria. LVII. Drug combinations to impede the selection of drug resistance, Part 1: Which model is appropriate? Peters W, Ann Trop Med Parasitol 1999 93 569 587 10.1080/00034989958087 10707103 (Pubitemid 29438128)
61. Resistance mutations reveal the atovaquone-binding domain of cytochrome b in malaria parasites. Srivastava IK, Morrisey JM, Darrouzet E, Daldal F, Vaidya AB, Mol Microbiol 1999 33 704 711 10.1046/j.1365-2958.1999.01515.x 10447880 (Pubitemid 29392651)
62. How can we identify parasite genes that underlie antimalarial drug resistance? Anderson T, Nkhoma S, Ecker A, Fidock D, Pharmacogenomics 2011 12 59 85 10.2217/pgs.10.165 21174623
63. Use of high-density tiling microarrays to identify mutations globally and elucidate mechanisms of drug resistance in Plasmodium falciparum. Dharia NV, Sidhu ABS, Cassera MB, Westenberger SJ, Bopp SE, Eastman RT, Plouffe D, Batalov S, Park DJ, Volkman SK, Wirth DF, Zhou Y, Fidock DA, Winzeler EA, Genome Biol 2009 10 21 10.1186/gb-2009-10-2-r21 19216790
64. A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Su X, Ferdig MT, Huang Y, Huynh CQ, Liu A, You J, Wootton JC, Wellems TE, Science 1999 286 1351 1353 10.1126/science.286.5443.1351 10558988 (Pubitemid 29535893)
65. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, OBrien J, Djimdé A, Doumbo O, Zongo I, Ouédraogo JB, Michon P, Mueller I, Siba P, Nzila A, Borrmann S, Kiara SM, Marsh K, Jiang H, Su X-Z, Amaratunga C, Fairhurst R, Socheat D, Nosten F, Imwong M, White NJ, Sanders M, Anastasi E, Alcock D, Drury E, Oyola S, Quail MA, Turner DJ, Ruano-Rubio V, Jyothi D, Amenga-Etego L, Hubbart C, Jeffreys A, Rowlands K, Sutherland C, Roper C, Mangano V, Modiano D, Tan JC, Ferdig MT, Amambua-Ngwa A, Conway DJ, Takala-Harrison S, Plowe CV, Rayner JC, Rockett KA, Clark TG, Newbold CI, Berriman M, MacInnis B, Kwiatkowski DP, Nature 2012 487 375 379 22722859
66. Harnessing genomics and genome biology to understand malaria biology. Volkman SK, Neafsey DE, Schaffner SF, Park DJ, Wirth DF, Nat Rev Genet 2012 13 315 328 22495435
67. P. falciparum in vitro killing rates allow to discriminate between different antimalarial mode-of-action. Sanz LM, Crespo B, de Cozar C, Ding XC, Llergo JL, Burrows JN, Garcia-Bustos JF, Gamo F-J, PLoS One 2012 7 30949 10.1371/journal.pone.0030949 22383983
68. Optical imaging techniques for the study of malaria. Cho S, Kim S, Kim Y, Park Y, Trends Biotechnol 2012 30 71 79 10.1016/j.tibtech.2011.08.004 21930322
69. Monitoring antimalarial resistance: launching a cooperative effort. Sibley CH, Guerin PJ, Ringwald P, Trends Parasitol 2010 26 221 224 10.1016/j.pt.2010.02.008 20304706
70. Malaria: developing drug and nonvaccine biological products for treatment and prophylaxis http://www.fda.gov/downloads/Drugs/GuidanceCompliance RegulatoryInformation/Guidances/UCM071951.pdf
71. Pyramax Summary of Opinion http://www.ema.europa.eu/docs/en-GB/ document-library/Other/2012/02/WC500122945.pdf
72. Coartem Summary Review http://www.accessdata.fda.gov/drugsatfda- docs/nda/2009/022268s000-SumR.pdf
73. Eurartesim Summary of Opinion http://www.ema.europa.eu/docs/en-GB/ document-library/Summary-of-opinion-Initial-authorisation/human/001199/ WC500108010.pdf
74. Challenges in antimalarial drug discovery. Burrows JN, Leroy D, Lotharius J, Waterson D, Future Med Chem 2011 3 1401 1412 10.4155/fmc.11.91 21879844