Chloroquine resistance before and after its withdrawal in Kenya

Malaria Journal

Volumn 8, Issue 1, 2009, Pages

  Mwai, Leah ^a,b   Ochong, Edwin ^c   Abdirahman, Abdi ^a   Kiara, Steven M ^a   Ward, Steve ^c   Kokwaro, Gilbert ^a   Sasi, Philip ^a   Marsh, Kevin ^a,b   Borrmann, Steffen ^a,d   MacKinnon, Margaret ^a,e   Nzila, Alexis ^a,b,c,f  

^a KEMRI WELLCOME TRUST RESEARCH PROGRAMME   (Kenya)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; DIHYDROFOLATE REDUCTASE; FANSIDAR; ANTIMALARIAL AGENT; CARRIER PROTEIN; MDR1 PROTEIN, PLASMODIUM FALCIPARUM; MULTIDRUG RESISTANCE PROTEIN; PFCRT PROTEIN, PLASMODIUM FALCIPARUM; PROTOZOAL PROTEIN; PYRIMETHAMINE; PYRIMETHAMINE PLUS SULFADOXINE; SULFADOXINE; SULFADOXINE-PYRIMETHAMINE;

ARTICLE; CLINICAL TRIAL; CODON; CONTROLLED STUDY; DHFR GENE; DRUG WITHDRAWAL; GENE; GENE MUTATION; GENOTYPE; HUMAN; KENYA; MALARIA FALCIPARUM; MALAWI; MULTICENTER STUDY; NONHUMAN; PFCRT GENE; PFMDR1 GENE; POLYMERASE CHAIN REACTION; ANIMAL; DRUG APPROVAL; DRUG COMBINATION; DRUG EFFECT; DRUG RESISTANCE; DRUG SENSITIVITY; ENZYMOLOGY; GENETICS; METABOLISM; METHODOLOGY; PARASITOLOGY; PLASMODIUM FALCIPARUM; POINT MUTATION; RESTRICTION MAPPING; TIME;

ANIMALS; ANTIMALARIALS; CHLOROQUINE; DRUG APPROVAL; DRUG COMBINATIONS; DRUG RESISTANCE; GENOTYPE; HUMANS; KENYA; MALARIA, FALCIPARUM; MEMBRANE TRANSPORT PROTEINS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PARASITIC SENSITIVITY TESTS; PLASMODIUM FALCIPARUM; POINT MUTATION; POLYMERASE CHAIN REACTION; PROTOZOAN PROTEINS; PYRIMETHAMINE; RESTRICTION MAPPING; SULFADOXINE; TETRAHYDROFOLATE DEHYDROGENASE; TIME FACTORS;

EID: 67650685545     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-8-106     Document Type: Article

References (61)

1. Malaria. Chemoprophylaxis and chemotherapy. W Peters, BMC 1971 2 95 98 10.1136/bmj.2.5753.95
2. Making malaria-treatment policy in the face of drug resistance. PB Bloland M Ettling, Ann Trop Med Parasitol 1999 93 5 23 10.1080/00034989958753 10492667
3. Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. JG Kublin JF Cortese EM Njunju RA Mukadam JJ Wirima PN Kazembe AA Djimde B Kouriba TE Taylor CV Plowe CE Contreras A Caraballo, J Infect Dis 2003 187 1870 1875 10.1086/375419 12792863
4. Return of chloroquine antimalarial efficacy in Malawi. MK Laufer PC Thesing ND Eddington R Masonga FK Dzinjalamala SL Takala TE Taylor CV Plowe, N Engl J Med 2006 355 1959 1966 10.1056/NEJMoa062032 17093247
5. Using evidence to change antimalarial drug policy in Kenya. R Shretta J Omumbo B Rapuoda RW Snow, Trop Med Int Health 2000 5 755 764 10.1046/j.1365-3156.2000.00643.x 11123822
6. Adoption of the new antimalarial drug policy in Tanzaniaa cross-sectional study in the community. J Eriksen SE Nsimba OM Minzi AJ Sanga M Petzold LL Gustafsson MY Warsame G Tomson, Trop Med Int Health 2005 10 1038 1046 10.1111/j.1365-3156.2005.01486.x 16185239
7. Increasing antimalarial drug resistance in Uganda and revision of the national drug policy. MR Kamya NN Bakyaita AO Talisuna WM Were SG Staedke, Trop Med Int Health 2002 7 1031 1041 10.1046/j.1365-3156.2002.00974.x 12460394
8. Recovery of chloroquine sensitivity and low prevalence of the Plasmodium falciparum chloroquine resistance transporter gene mutation K76T following the discontinuance of chloroquine use in Malawi. T Mita A Kaneko JK Lum B Bwijo M Takechi IL Zungu T Tsukahara K Tanabe T Kobayakawa A Bjorkman, Am J Trop Med Hyg 2003 68 413 415 12875289 (Pubitemid 38230640)
9. Therapeutic efficacy of sulphadoxine/pyrimethamine and susceptibility in vitro of P. falciparum isolates to sulphadoxine-pyremethamine and other antimalarial drugs in Malawian children. M Takechi M Matsuo C Ziba A MacHeso D Butao IL Zungu I Chakanika MD Bustos, Trop Med Int Health 2001 6 429 434 10.1046/j.1365-3156.2001.00735.x 11422956
10. Mechanisms of resistance of malaria parasites to antifolates. A Gregson CV Plowe, Pharmacol Rev 2005 57 117 145 10.1124/pr.57.1.4 15734729
11. Pyrimethamine-sulfadoxine resistance in Plasmodium falciparum: what next? CH Sibley JE Hyde PF Sims CV Plowe JG Kublin EK Mberu AF Cowman PA Winstanley WM Watkins AM Nzila, Trends Parasitol 2001 17 582 588 10.1016/S1471-4922(01) 02085-2 11756042
12. Chlorproguanil-dapsone: effective treatment for uncomplicated falciparum malaria. E Amukoye PA Winstanley WM Watkins RW Snow J Hatcher M Mosobo E Ngumbao B Lowe M Ton G Minyiri K Marsh, Antimicrob Agents Chemother 1997 41 2261 2264 9333058 (Pubitemid 27422223)
13. Efficacy and safety of the six-dose regimen of artemether-lumefantrine in pediatrics with uncomplicated Plasmodium falciparum malaria: a pooled analysis of individual patient data. M Makanga Z Premji C Falade J Karbwang EA Mueller K Andriano P Hunt PI De Palacios, Am J Trop Med Hyg 2006 74 991 998 16760509 (Pubitemid 351627405)
14. Chlorproguanil-dapsone versus sulfadoxine-pyrimethamine for sequential episodes of uncomplicated falciparum malaria in Kenya and Malawi: a randomised clinical trial. J Sulo P Chimpeni J Hatcher JG Kublin CV Plowe ME Molyneux K Marsh TE Taylor WM Watkins PA Winstanley, Lancet 2002 360 1136 1143 10.1016/S0140-6736(02)11198-6 12387962
15. Chlorproguanil/dapsone for uncomplicated Plasmodium falciparum malaria in young children: pharmacokinetics and therapeutic range. P Winstanley W Watkins D Muhia S Szwandt E Amukoye K Marsh, Trans R Soc Trop Med Hyg 1997 91 322 327 10.1016/S0035-9203(97)90093-6 9231209
16. In vivo and in vitro efficacy of amodiaquine against Plasmodium falciparum in an area of continued use of 4-aminoquinolines in East Africa. P Sasi A Abdirahman L Mwai S Muriithi J Straimer L Schieck A Rippert M Bashraheil A Salim J Peshu K Awuondo B Lowe M Pirmohamed P Winstanley S Ward A Nzila S Borrmann, J Infect Dis 2009 199 11 1575 1582 10.1086/598862 19405863
17. In vitro antimalarial activity of tetrahydrofolate dehydrogenase inhibitors. DG Sixsmith WM Watkins JD Chulay HC Spencer, Am J Trop Med Hyg 1984 33 772 776 6385738 (Pubitemid 15201685)
18. Towards an understanding of the mechanism of pyrimethamine-sulfadoxine resistance in Plasmodium falciparum: genotyping of dihydrofolate reductase and dihydropteroate synthase of Kenyan parasites. AM Nzila EK Mberu J Sulo H Dayo PA Winstanley CH Sibley WM Watkins, Antimicrob Agents Chemother 2000 44 991 996 10722502 10.1128/AAC.44.4.991-996.2000
19. Molecular evidence of greater selective pressure for drug resistance exerted by the long-acting antifolate Pyrimethamine/Sulfadoxine compared with the shorter-acting chlorproguanil/dapsone on Kenyan Plasmodium falciparum. AM Nzila E Nduati EK Mberu C Hopkins Sibley SA Monks PA Winstanley WM Watkins, J Infect Dis 2000 181 2023 2028 10.1086/315520 10837185
20. Why has the dihydrofolate reductase 164 mutation not consistently been found in Africa yet? A Nzila E Ochong E Nduati K Gilbert P Winstanley S Ward K Marsh, Trans R Soc Trop Med Hyg 2005 99 341 346 10.1016/j.trstmh.2004.07.002 15780340
21. Molecular monitoring of the Leu-164 mutation of dihydrofolate reductase in a highly sulfadoxine/pyrimethamine-resistant area in Africa. E Ochong A Nzila S Kimani G Kokwaro T Mutabingwa W Watkins K Marsh, Malar J 2003 2 46 14675491 10.1186/1475-2875-2-46
22. Dihydrofolate reductase I164L mutations in Plasmodium falciparum isolates: clinical outcome of 14 Kenyan adults infected with parasites harbouring the I164L mutation. MJ Hamel A Poe P Bloland A McCollum Z Zhou YP Shi P Ouma K Otieno J Vulule A Escalante V Udhayakumar L Slutsker, Trans R Soc Trop Med Hyg 2008 102 338 345 10.1016/j.trstmh.2008.01.018 18321547
23. Detection of the dihydrofolate reductase-164L mutation in Plasmodium falciparum infections from Malawi by heteroduplex tracking assay. JJ Juliano P Trottman V Mwapasa SR Meshnick, Am J Trop Med Hyg 2008 78 892 894 18541765 (Pubitemid 351967805)
24. Emergence of a dhfr mutation conferring high-level drug resistance in Plasmodium falciparum populations from southwest Uganda. C Lynch R Pearce H Pota J Cox TA Abeku J Rwakimari I Naidoo J Tibenderana C Roper, J Infect Dis 2008 197 1598 1604 10.1086/587845 18471065
25. A selective sweep driven by pyrimethamine treatment in southeast asian malaria parasites. S Nair JT Williams A Brockman L Paiphun M Mayxay PN Newton JP Guthmann FM Smithuis TT Hien NJ White F Nosten TJ Anderson, Mol Biol Evol 2003 20 1526 1536 10.1093/molbev/msg162 12832643
26. Antifolate antimalarial resistance in southeast Africa: a population-based analysis. C Roper R Pearce B Bredenkamp J Gumede C Drakeley F Mosha D Chandramohan B Sharp, Lancet 2003 361 1174 1181 10.1016/S0140-6736(03) 12951-0 12686039
27. The Garki Project: Research on the Epidemiology and Control of Malaria in the Sudan Savanna of West Africa. L Molineaux G Gramiccia, Geneva: World Health Organization 1980
28. The evolution of multiple drug resistance in malaria parasites. MJ Mackinnon IM Hastings, Trans R Soc Trop Med Hyg 1998 92 188 195 10.1016/S0035-9203(98)90745-3 9764331
29. A mathematical theory of natural and artificial selection. JBS Haldane, Trans Cambridge Philos Soc 1924 19 24
30. Estimating relative fitness in asexually reproducing plant pathogen populations. H stergrd, Theor Appl Genet 1987 87 94 10.1007/BF00290089
31. Mapping drug resistance genes in Plasmodium falciparum by genome-wide association. TJ Anderson, Curr Drug Targets Infect Disord 2004 4 65 78 10.2174/1568005043480943 15032635
32. Influence of oxygen on asexual blood cycle and susceptibility of Plasmodium falciparum to chloroquine: requirement of a standardized in vitro assay. S Briolant P Parola T Fusai M Madamet-Torrentino E Baret J Mosnier JP Delmont D Parzy P Minodier C Rogier B Pradines, Malar J 2007 6 44 17437625 10.1186/1475-2875-6-44
33. Plasmodium falciparum chemoresistance. The situation in Africa in 1989. J Le Bras P Ringwald, Med Trop (Mars) 1990 50 11 16 2195277 (Pubitemid 20165525)
34. Improving malaria home treatment by training drug retailers in rural Kenya. VM Marsh WM Mutemi A Willetts K Bayah S Were A Ross K Marsh, Trop Med Int Health 2004 9 451 460 10.1111/j.1365-3156.2004.01223.x 15078263
35. Brands, costs and registration status of antimalarial drugs in the Kenyan retail sector. AA Amin RW Snow, Malar J 2005 4 36 16042815 10.1186/1475-2875-4- 36
36. Contribution of the pfmdr1 gene to antimalarial drug-resistance. MT Duraisingh AF Cowman, Acta Trop 2005 94 181 190 15876420 (Pubitemid 40720325)
37. Advances in understanding the genetic basis of antimalarial drug resistance. EH Ekland DA Fidock, Curr Opin Microbiol 2007 10 363 370 17709280 10.1016/j.mib.2007.07.007
38. Studies of antibiotic resistance within the patient, hospitals and the community using simple mathematical models. DJ Austin RM Anderson, Philos Trans R Soc Lond B Biol Sci 1999 354 721 738 10365398 10.1098/rstb.1999.0425 (Pubitemid 29365621)
39. Evolution of a bacteria/plasmid association. JE Bouma RE Lenski, Nature 1988 335 351 352 10.1038/335351a0 3047585
40. Bacterial evolution and the cost of antibiotic resistance. RE Lenski, Int Microbiol 1998 1 265 270 10943373 (Pubitemid 128731340)
41. Balancing the drug-resistance equation. SB Levy, Trends Microbiol 1994 2 341 342 10.1016/0966-842X(94)90607-6 7850197
42. The hitchhiker's guide to malaria parasite genes. D Walliker, Trends Parasitol 2005 21 489 493 10.1016/j.pt.2005.08.017 16126455
43. Withdrawing antimalarial drugs: impact on parasite resistance and implications for malaria treatment policies. MK Laufer CV Plowe, Drug Resist Updat 2004 7 279 288 10.1016/j.drup.2004.08.003 15533765
44. Decreased prevalence of the Plasmodium falciparum chloroquine resistance transporter 76T marker associated with cessation of chloroquine use against P. falciparum malaria in Hainan, People's Republic of China. X Wang J Mu G Li P Chen X Guo L Fu L Chen X Su TE Wellems, Am J Trop Med Hyg 2005 72 410 414 15827277 (Pubitemid 41278849)
45. Mutations in cytochrome b resulting in atovaquone resistance are associated with loss of fitness in Plasmodium falciparum. JM Peters N Chen M Gatton M Korsinczky EV Fowler S Manzetti A Saul Q Cheng, Antimicrob Agents Chemother 2002 46 2435 2441 12121915 10.1128/AAC.46.8.2435-2441.2002
46. Persistence of drug-resistant malaria parasites. VE Rosario R Hall D Walliker GH Beale, Lancet 1978 1 185 187 10.1016/S0140-6736(78)90616-5 74609
47. Effect of pyrimethamine resistance on sporogony in a Plasmodium berghei/Anopheles stephensi model. CJ Shinondo HN Lanners RC Lowrie Jr MF Wiser, Exp Parasitol 1994 78 194 202 10.1006/expr.1994.1019 8119374
48. Origin and dissemination of Plasmodium falciparum drug-resistance mutations in South America. JF Cortese A Caraballo CE Contreras CV Plowe, J Infect Dis 2002 186 999 1006 10.1086/342946 12232841
49. Analysis of the PfCRT K76T mutation in Plasmodium falciparum isolates from the Amazon region of Brazil. PP Vieira M das Gracas Alecrim LH da Silva I Gonzalez-Jimenez MG Zalis, J Infect Dis 2001 183 1832 1833 10.1086/320739 11372042
50. Characterization of Plasmodium falciparum isolated from the Amazon region of Brazil: evidence for quinine resistance. MG Zalis L Pang MS Silveira WK Milhous DF Wirth, Am J Trop Med Hyg 1998 58 630 637 9598453 (Pubitemid 28237263)
51. Short report: association between chloroquine and amodiaquine resistance and allelic variation in the Plasmodium falciparum multiple drug resistance 1 gene and the chloroquine resistance transporter gene in isolates from the upper Nile in southern Sudan. EO Ochong IV van den Broek K Keus A Nzila, Am J Trop Med Hyg 2003 69 184 187 13677373
52. World Antimalarial Resistance Network (WARN) II: in vitro antimalarial drug susceptibility. DJ Bacon R Jambou T Fandeur J Le Bras C Wongsrichanalai MM Fukuda P Ringwald CH Sibley DE Kyle, Malar J 2007 6 120 17822533 10.1186/1475-2875-6-120
53. Several alleles of the multidrug-resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. SJ Foote DE Kyle RK Martin AM Oduola K Forsyth DJ Kemp AF Cowman, Nature 1990 345 255 258 10.1038/345255a0 2185424
54. A critical role for PfCRT K76T in Plasmodium falciparum verapamil-reversible chloroquine resistance. V Lakshmanan PG Bray D Verdier-Pinard DJ Johnson P Horrocks RA Muhle GE Alakpa RH Hughes SA Ward DJ Krogstad AB Sidhu DA Fidock, Embo J 2005 24 2294 2305 15944738 10.1038/sj.emboj.7600681
55. Multiple transporters associated with malaria parasite responses to chloroquine and quinine. J Mu MT Ferdig X Feng DA Joy J Duan T Furuya G Subramanian L Aravind RA Cooper JC Wootton M Xiong XZ Su, Mol Microbiol 2003 49 977 989 10.1046/j.1365-2958.2003.03627.x 12890022
56. Plasmodium falciparum: induction of resistance to mefloquine in cloned strains by continuous drug exposure in vitro. AM Oduola WK Milhous NF Weatherly JH Bowdre RE Desjardins, Exp Parasitol 1988 67 354 360 10.1016/0014-4894(88) 90082-3 3056740
57. Plasmodium falciparum: cloning by single-erythrocyte micromanipulation and heterogeneity in vitro. AM Oduola NF Weatherly JH Bowdre RE Desjardins, Exp Parasitol 1988 66 86 95 10.1016/0014-4894(88)90053-7 3284758
58. Complex polymorphisms in an approximately 330 kDa protein are linked to chloroquine-resistant P. falciparum in Southeast Asia and Africa. X Su LA Kirkman H Fujioka TE Wellems, Cell 1997 91 593 603 10.1016/S0092-8674(00)80447-X 9393853 (Pubitemid 27513651)
59. Chloroquine resistant Plasmodium vivax: In vitro characterisation and association with molecular polymorphisms. R Suwanarusk B Russell M Chavchich F Chalfein E Kenangalem V Kosaisavee B Prasetyorini KA Piera M Barends A Brockman U Lek-Uthai NM Anstey E Tjitra F Nosten Q Cheng RN Price, PLoS ONE 2007 2 e1089 17971853 10.1371/journal.pone.0001089
60. Analysis of pfcrt point mutations and chloroquine susceptibility in isolates of Plasmodium falciparum. R Durand S Jafari J Vauzelle JF Delabre Z Jesic J Le Bras, Mol Biochem Parasitol 2001 114 95 102 10.1016/S0166-6851(01) 00247-X 11356518
61. Antimalarial drug resistance. NJ White, J Clin Invest 2004 113 1084 1092 15085184 (Pubitemid 38544090)