Changes in drug sensitivity and anti-malarial drug resistance mutations over time among Plasmodium falciparum parasites in Senegal

Malaria Journal

Volumn 12, Issue 1, 2013, Pages

  Van Tyne, Daria ^a   Dieye, Baba ^b   Valim, Clarissa ^a,c   Daniels, Rachel F ^a   Sène, Papa Diogoye ^b   Lukens, Amanda K ^a,c   Ndiaye, Mouhamadou ^b   Bei, Amy K ^a   Ndiaye, Yaye Die ^b   Hamilton, Elizabeth J ^a,d   Ndir, Omar ^b   Mboup, Souleymane ^b   Volkman, Sarah K ^a,c,e   Wirth, Dyann F ^a,c   Ndiaye, Daouda ^b  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITÉ CHEIKH ANTA DIOP   (Senegal)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d HARVARD UNIVERSITY   (United States)

^e SIMMONS COLLEGE   (United States)

Author keywords

DAPI ex vivo assay; Drug resistance monitoring; Malaria

Indexed keywords

AMODIAQUINE; ARTEMISININ; CHLOROQUINE; MEFLOQUINE;

ADOLESCENT; ADULT; ANTIMALARIAL DRUG RESISTANCE; ANTIMALARIAL DRUG SUSCEPTIBILITY; ARTICLE; CLONAL VARIATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG RESPONSE; DRUG SCREENING; DRUG TOLERANCE; EX VIVO STUDY; FEMALE; GENOTYPE; HAPLOTYPE; HEMATOCRIT; HUMAN; IC 50; MAJOR CLINICAL STUDY; MALARIA CONTROL; MALARIA FALCIPARUM; MALE; MUTATION; NONHUMAN; PARASITEMIA; PLASMODIUM FALCIPARUM; PROTOZOAL GENETICS; SENEGAL;

ADOLESCENT; ADULT; ANIMALS; ANTIMALARIALS; DRUG RESISTANCE; FEMALE; HUMANS; INHIBITORY CONCENTRATION 50; MALARIA, FALCIPARUM; MALE; PLASMODIUM FALCIPARUM; PREVALENCE; REPRODUCIBILITY OF RESULTS; SENEGAL; YOUNG ADULT;

EID: 84889005854     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-12-441     Document Type: Article

References (42)

1. A research agenda to underpin malaria eradication. Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C, Collins F, Doumbo OK, Greenwood B, Hall BF, Levine MM, Mendis K, Newman RD, Plowe CV, Rodriguez MH, Sinden R, Slutsker L, Tanner M, PLoS Med 2011 8 1000406 10.1371/journal.pmed.1000406 21311579
2. Evidence of artemisinin-resistant malaria in western Cambodia. Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM, Consortium ARiCAS, NEJM 2008 359 2619 2620 10.1056/NEJMc0805011 19064625
3. Artemisinin resistance in Plasmodium falciparum malaria. Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Lwin KM, Ariey F, Hanpithakpong W, Lee SJ, Ringwald P, Silamut K, Imwong M, Chotivanich K, Lim P, Herdman T, An SS, Yeung S, Singhasivanon P, Day NPJ, Lindegardh N, Socheat D, White NJ, NEJM 2009 361 455 467 10.1056/NEJMoa0808859 19641202
4. Mitigating the threat of artemisinin resistance in Africa: improvement of drug-resistance surveillance and response systems. Talisuna AO, Karema C, Ogutu B, Juma E, Logedi J, Nyandigisi A, Mulenga M, Mbacham WF, Roper C, Guerin PJ, D'Alessandro U, Snow RW, Lancet Infect Dis 2012 12 888 896 10.1016/S1473- 3099(12)70241-4 23099083
5. Malaria drug-sensitivity testing: new assays, new perspectives. Noedl H, Wongsrichanalai C, Wernsdorfer WH, Trends Parasitol 2003 19 175 181 10.1016/S1471-4922(03)00028-X 12689648 (Pubitemid 36411974)
6. Drug sensitivity of Plasmodium falciparum: an in vitro microtechnique. Rieckmann KH, Campbell GH, Sax LJ, Ema JE, Lancet 1978 311 22 23 10.1016/S0140-6736(78)90365-3
7. Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Desjardins RE, Canfield CJ, Haynes JD, Chulay JD, Antimicrob Agents Chemother 1979 16 710 718 10.1128/AAC.16.6.710 394674 (Pubitemid 10082023)
8. High-throughput Plasmodium falciparum growth assay for malaria drug discovery. Baniecki ML, Wirth DF, Clardy J, Antimicrob Agents Chemother 2007 51 716 723 10.1128/AAC.01144-06 17116676 (Pubitemid 46185294)
9. Novel, rapid, and inexpensive cell-based quantification of antimalarial drug efficacy. Bennett TN, Paguio M, Gligorijevic B, Seudieu C, Kosar AD, Davidson E, Roepe PD, Antimicrob Agents Chemother 2004 48 1807 1810 10.1128/AAC.48.5.1807-1810.2004 15105139 (Pubitemid 38544393)
10. Performance and reliability of the SYBR Green I based assay for the routine monitoring of susceptibility of Plasmodium falciparum clinical isolates. Rason MA, Randriantsoa T, Andrianantenaina H, Ratsimbasoa A, Menard D, Trans R Soc Trop Med Hyg 2008 102 346 351 10.1016/j.trstmh.2008.01.021 18321546
11. A non-radioactive DAPI-based high-throughput in vitro assay to assess Plasmodium falciparum responsiveness to antimalarials-increased sensitivity of P. falciparum to chloroquine in Senegal. Ndiaye D, Patel V, Demas A, LeRoux M, Ndir O, Mboup S, Clardy J, Lakshmanan V, Daily JP, Wirth DF, Am J Trop Med Hyg 2010 82 228 230 10.4269/ajtmh.2010.09-0470 20133997
12. A colorimetric in vitro drug sensitivity assay for Plasmodium falciparum based on a highly sensitive double-site lactate dehydrogenase antigen-capture enzyme-linked immunosorbent assay. Druilhe P, Moreno A, Blanc C, Brasseur PH, Jacquier P, Am J Trop Med Hyg 2001 64 233 241 11463109
13. A histidine-rich protein 2-based malaria drug sensitivity assay for field use. Noedl H, Attlmayr B, Wernsdorfer WH, Kollaritsch H, Miller RS, Am J Trop Med Hyg 2004 71 711 714 15642959 (Pubitemid 40075618)
14. Real-time PCR methods for monitoring antimalarial drug resistance. Wilson PE, Alker AP, Meshnick SR, Trends Parasitol 2005 21 278 283 10.1016/j.pt.2005.04.007 15922249 (Pubitemid 40726319)
15. A database of antimalarial drug resistance. Sibley CH, Ringwald P, Malar J 2006 5 48 10.1186/1475-2875-5-48 16774688 (Pubitemid 44211710)
16. Responding to the challenge of antimalarial drug resistance by routine monitoring to update national malaria treatment policies. Vestergaard LS, Ringwald P, Am J Trop Med Hyg 2007 77 153 159 18165488
17. Focus on Senegal. WHO, Roll Back Malaria Progress and Impact Series, Volume 4 Geneva: WHO 2010 1 56
18. Ex vivo susceptibility of Plasmodium falciparum isolates from Dakar, Senegal, to seven standard anti-malarial drugs. Fall B, Diawara S, Sow K, Baret E, Diatta B, Fall KB, Mbaye PS, Fall F, Dieme Y, Rogier C, Wade B, Bercion R, Pradines B, Malar J 2011 10 310 10.1186/1475-2875-10-310 22014157
19. Rapid, field-deployable method for genotyping and discovery of drug-resistance single nucleotide polymorphisms in Plasmodium falciparum. Daniels R, Ndiaye D, Wall M, McKinney J, Sene PD, Sabeti PC, Volkman SK, Mboup S, Wirth DF, Antimicrob Agents Chemother 2012 56 6 2976 2986 10.1128/AAC.05737-11 22430961
20. Assessment of the molecular marker of Plasmodium falciparum chloroquine resistance (pfcrt) in Senegal after several years of chloroquine withdrawal. Ndiaye M, Faye B, Tine R, Ndiaye JL, Lo A, Abiola A, Dieng Y, Ndiaye D, Hallett R, Alifrangis M, Gaye O, Am J Trop Med Hyg 2012 87 4 640 645 10.4269/ajtmh.2012.11-0709 22927495
21. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Daniels R, Volkman SK, Milner DA, Mahesh N, Neafsey DE, Park DJ, Rosen D, Angelino E, Sabeti PC, Wirth DF, Wiegand RC, Malar J 2008 7 223 10.1186/1475-2875-7-223 18959790
22. Human malaria parasites in continuous culture. Trager W, Jensen JB, Science 1976 193 673 675 10.1126/science.781840 781840
23. In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Plouffe D, Brinker A, McNamara C, Henson K, Kato N, Kuhen K, Nagle A, Adrian F, Matzen JT, Anderson P, Nam TG, Gray NS, Chatterjee A, Janes J, Yan SF, Trager R, Caldwell JS, Schultz PG, Zhou Y, Winzeler EA, Proc Natl Acad Sci U S A 2008 105 9059 9064 10.1073/pnas.0802982105 18579783
24. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. Zhang JH, Chung TD, Oldenburg KR, J Biomol Screen 1999 4 67 73 10.1177/108705719900400206 10838414 (Pubitemid 29278954)
25. 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. Mita T, Kaneko A, Lum JK, Bwijo B, Takechi M, Zungu IL, Tsukahara T, Tanabe K, Kobayakawa T, Bjorkman A, Am J Trop Med Hyg 2003 68 413 415 12875289 (Pubitemid 38230640)
26. Geographic patterns of Plasmodium falciparum drug resistance distinguished by differential responses to amodiaquine and chloroquine. Sa JM, Twu O, Hayton K, Reyes S, Fay MP, Ringwald P, Wellems TE, Proc Natl Acad Sci U S A 2009 106 18883 18889 10.1073/pnas.0911317106 19884511
27. A systematic review and meta-analysis of evidence for correlation between molecular markers of parasite resistance and treatment outcome in falciparum malaria. Picot S, Olliaro P, de Monbrison F, Bienvenu AL, Price RN, Ringwald P, Malar J 2009 8 89 10.1186/1475-2875-8-89 19413906
28. Association between mutations in Plasmodium falciparum chloroquine resistance transporter and P. falciparum multidrug resistance 1 genes and in vivo amodiaquine resistance in P. falciparum malaria-infected children in Nigeria. Happi CT, Gbotosho GO, Folarin OA, Bolaji OM, Sowunmi A, Kyle DE, Milhous W, Wirth DF, Oduola AM, Am J Trop Med Hyg 2006 75 155 161 16837724 (Pubitemid 351627586)
29. Ex vivo activity of the ACT new components pyronaridine and piperaquine in comparison with conventional ACT drugs against isolates of Plasmodium falciparum. Pascual A, Parola P, Benoit-Vical F, Simon F, Malvy D, Picot S, Delaunay P, Basset D, Maubon D, Faugere B, Menard G, Bourgeois N, Oeuvray C, Didillon E, Rogier C, Pradines B, Malar J 2012 11 45 10.1186/1475-2875-11-45 22333675
30. Selection of Plasmodium falciparum pfmdr1 alleles following therapy with artemether-lumefantrine in an area of Uganda where malaria is highly endemic. Dokomajilar C, Nsobya SL, Greenhouse B, Rosenthal PJ, Dorsey G, Antimicrob Agents Chemother 2006 50 1893 1895 10.1128/AAC.50.5.1893-1895.2006 16641472
31. Increased pfmdr1 copy number and sequence polymorphisms in Plasmodium falciparum isolates from Sudanese malaria patients treated with artemether-lumefantrine. Gadalla NB, Adam I, Elzaki SE, Bashir S, Mukhtar I, Oguike M, Gadalla A, Mansour F, Warhurst D, El-Sayed BB, Sutherland CJ, Antimicrob Agents Chemother 2011 55 5408 5411 10.1128/AAC.05102-11 21896916
32. Prevalence of molecular markers of Plasmodium falciparum drug resistance in Dakar, Senegal. Wurtz N, Fall B, Pascual A, Diawara S, Sow K, Baret E, Diatta B, Fall KB, Mbaye PS, Fall F, Dieme Y, Rogier C, Bercion R, Briolant S, Wade B, Pradines B, Malar J 2012 11 197 10.1186/1475-2875-11-197 22694921
33. Plasmodium falciparum susceptibility to anti-malarial drugs in Dakar, Senegal, in 2010: an ex vivo and drug resistance molecular markers study. Fall B, Pascual A, Sarr FD, Wurtz N, Richard V, Baret E, Dieme Y, Briolant S, Bercion R, Wade B, Tall A, Pradines B, Malar J 2013 12 107 10.1186/1475-2875-12-107 23510258
34. Multiple genetic backgrounds of the amplified Plasmodium falciparum multidrug resistance (pfmdr1) gene and selective sweep of 184F mutation in Cambodia. Vinayak S, Alam MT, Sem R, Shah NK, Susanti AI, Lim P, Muth S, Maguire JD, Rogers WO, Fandeur T, Barnwell JW, Escalante AA, Wongsrichanalai C, Ariey F, Meshnick SR, Udhayakumar V, J Infect Dis 2010 201 1551 1560 10.1086/651949 20367478
35. A thirteen-year analysis of Plasmodium falciparum populations reveals high conservation of the mutant pfcrt haplotype despite the withdrawal of chloroquine from national treatment guidelines in Gabon. Frank M, Lehners N, Mayengue PI, Gabor J, Dal-Bianco M, Kombila DU, Ngoma GM, Supan C, Lell B, Ntoumi F, Grobusch MP, Dietz K, Kremsner PG, Malar J 2011 10 304 10.1186/1475-2875-10-304 22004584
36. Molecular monitoring of Plasmodium falciparum drug susceptibility at the time of the introduction of artemisinin-based combination therapy in Yaounde, Cameroon: implications for the future. Menard S, Morlais I, Tahar R, Sayang C, Mayengue PI, Iriart X, Benoit-Vical F, Lemen B, Magnaval JF, Awono-Ambene P, Basco LK, Berry A, Malar J 2012 11 113 10.1186/1475-2875-11-113 22498364
37. Chloroquine resistance before and after its withdrawal in Kenya. Mwai L, Ochong E, Abdirahman A, Kiara SM, Ward S, Kokwaro G, Sasi P, Marsh K, Borrmann S, Mackinnon M, Nzila A, Malar J 2009 8 106 10.1186/1475-2875-8-106 19450282
38. Prevalence of single nucleotide polymorphisms in the Plasmodium falciparum multidrug resistance gene (pfmdr1) in Korogwe District in Tanzania before and after introduction of artemisinin-based combination therapy. Thomsen TT, Ishengoma DS, Mmbando BP, Lusingu JP, Vestergaard LS, Theander TG, Lemnge MM, Bygbjerg IC, Alifrangis M, Am J Trop Med Hyg 2011 85 979 983 10.4269/ajtmh.2011.11-0071 22144430
39. Increased prevalence of the Plasmodium falciparum pfmdr1 86N genotype among field isolates from Franceville, Gabon after replacement of chloroquine by artemether-lumefantrine and artesunate-mefloquine. Lekana-Douki JB, Dinzouna Boutamba SD, Zatra R, Zang Edou SE, Ekomy H, Bisvigou U, Toure-Ndouo FS, Infect Genet Evol 2011 11 512 517 10.1016/j.meegid.2011.01.003 21251998
40. A major genome region underlying artemisinin resistance in malaria. Cheeseman IH, Miller BA, Nair S, Nkhoma S, Tan A, Tan JC, Al Saai 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 TJ, Science 2012 336 79 82 10.1126/science.1215966 22491853
41. Sequence-based association and selection scans identify drug resistance loci in the Plasmodium falciparum malaria parasite. Park DJ, Lukens AK, Neafsey DE, Schaffner SF, Chang HH, Valim C, Ribacke U, Van Tyne D, Galinsky K, Galligan M, Becker JS, Ndiaye D, Mboup S, Wiegand RC, Hartl DL, Sabeti PC, Wirth DF, Volkman SK, Proc Natl Acad Sci U S A 2012 109 32 13052 13057 10.1073/pnas.1210585109 22826220
42. Genetic loci associated with delayed clearance of Plasmodium falciparum following artemisinin treatment in Southeast Asia. Takala-Harrison S, Clark TG, Jacob CG, Cummings MP, Miotto O, Dondorp AM, Fukuda MM, Nosten F, Noedl H, Imwong M, Bethell D, Se Y, Lon C, Tyner SD, Saunders DL, Socheat D, Ariey F, Phyo AP, Starzengruber P, Fuehrer HP, Swoboda P, Stepniewska K, Flegg J, Arze C, Cerqueira GC, Silva JC, Ricklefs SM, Porcella SF, Stephens RM, Adams M, et al. Proc Natl Acad Sci U S A 2013 110 240 245 10.1073/pnas.1211205110 23248304