Assessing the cost-benefit effect of a plasmodium falciparum drug resistance mutation on parasite growth in vitro

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 2, 2013, Pages 887-892

  Fröberg, Gabrielle ^a   Ferreira, Pedro Eduardo ^a,b   Martensson, Andreas ^a   Ali, Abdullah ^c   Björkman, Anders ^b   Gilb, José Pedro ^a,d  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF ALGARVE   (Portugal)

^c Zanzibar Malaria Control Programme (ZMCP)   (Tanzania)

^d BINGHAMTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMODIAQUINE; CHLOROQUINE; DEETHYLAMODIAQUINE;

ALLELE; ANTIMALARIAL DRUG RESISTANCE; ANTIMALARIAL DRUG SUSCEPTIBILITY; ARTICLE; CLONE; CONTROLLED STUDY; COST BENEFIT ANALYSIS; DRUG CONCENTRATION; GENE; GENE MUTATION; GROWTH CURVE; IN VITRO STUDY; IN VIVO STUDY; MICROBIAL GROWTH; NONHUMAN; PARASITE DEVELOPMENT; PFMDR1 GENE; PHARMACOGENETICS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

AMODIAQUINE; ANTIMALARIALS; BIOLOGICAL TRANSPORT; CHLOROQUINE; DRUG RESISTANCE; GENETIC FITNESS; GENOTYPE; MALARIA, FALCIPARUM; MEMBRANE TRANSPORT PROTEINS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTATION; PLASMODIUM FALCIPARUM;

EID: 84872874619     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00950-12     Document Type: Article

References (42)

1. WHO. 2006. Guidelines for the treatment of malaria. WHO, Geneva, Switzerland.
2. Zwang J, Olliaro P, Barennes H, Bonnet M, Brasseur P, Bukirwa H, Cohuet S, D'Alessandro U, Djimde A, Karema C, Guthmann JP, Hamour S, Ndiaye JL, Martensson A, Rwagacondo C, Sagara I, Same-Ekobo A, Sirima SB, van den Broek I, Yeka A, Taylor WR, Dorsey G, Randrianarivelojosia M. 2009. Efficacy of artesunate-amodiaquine for treating uncomplicated falciparum malaria in sub-Saharan Africa: A multi-centre analysis. Malar J. 8:203. doi:10.1186/1475-2875-8-203.
3. Childs GE, Boudreau EF, Milhous WK, Wimonwattratee T, Pooyindee N, Pang L, Davidson DE, Jr. 1989. A comparison of the in vitro activities of amodiaquine and desethylamodiaquine against isolates of Plasmodium falciparum. Am. J. Trop. Med. Hyg. 40:7-11.
4. Olliaro P, Mussano P. 2003. Amodiaquine for treating malaria. Cochrane Database Syst. Rev. 2003:CD000016. doi:10.1002/14651858.CD000016.
5. Djimde A, Doumbo OK, Cortese JF, Kayentao K, Doumbo S, Diourte Y, Dicko A, Su XZ, Nomura T, Fidock DA, Wellems TE, Plowe CV, Coulibaly D. 2001. A molecular marker for chloroquine-resistant falciparum malaria. N. Engl. J. Med. 344:257-263.
6. Duraisingh MT, Drakeley CJ, Muller O, Bailey R, Snounou G, Targett GA, Greenwood BM, Warhurst DC. 1997. Evidence for selection for the tyrosine-86 allele of the pfmdr 1 gene of Plasmodium falciparum by chloroquine and amodiaquine. Parasitology 114(Part 3):205-211.
7. Holmgren G, Gil JP, Ferreira PM, Veiga MI, Obonyo CO, Bjorkman A. 2006. Amodiaquine resistant Plasmodium falciparum malaria in vivo is associated with selection of pfcrt 76T and pfmdr1 86Y. Infect. Genet. Evol. 6:309-314.
8. Humphreys GS, Merinopoulos I, Ahmed J, Whitty CJ, Mutabingwa TK, Sutherland CJ, Hallett RL. 2007. Amodiaquine and artemetherlumefantrine select distinct alleles of the Plasmodium falciparum mdr1 gene in Tanzanian children treated for uncomplicated malaria. Antimicrob. Agents Chemother. 51:991-997.
9. Lakshmanan V, Bray PG, Verdier-Pinard D, Johnson DJ, Horrocks P, Muhle RA, Alakpa GE, Hughes RH, Ward SA, Krogstad DJ, Sidhu AB, Fidock DA. 2005. A critical role for PfCRT K76T in Plasmodium falciparum verapamil-reversible chloroquine resistance. EMBO J. 24:2294-2305.
10. Nsobya SL, Kiggundu M, Nanyunja S, Joloba M, Greenhouse B, Rosenthal PJ. 2010. In vitro sensitivities of Plasmodium falciparum to different antimalarial drugs in Uganda. Antimicrob. Agents Chemother. 54:1200-1206.
11. Picot S, Olliaro P, de Monbrison F, Bienvenu AL, Price RN, Ringwald P. 2009. A systematic review and meta-analysis of evidence for correlation between molecular markers of parasite resistance and treatment outcome in falciparum malaria. Malar. J. 8:89. doi:10.1186/1475-2875-8-89.
12. Sidhu AB, Verdier-Pinard D, Fidock DA. 2002. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298:210-213.
13. Warhurst DC. 2003. Polymorphism in the Plasmodium falciparum chloroquine-resistance transporter protein links verapamil enhancement of chloroquine sensitivity with the clinical efficacy of amodiaquine. Malar. J. 2:31. doi:10.1186/1475-2875-2-31.
14. Holmgren G, Hamrin J, Svard J, Martensson A, Gil JP, Bjorkman A. 2007. Selection of pfmdr1 mutations after amodiaquine monotherapy and amodiaquine plus artemisinin combination therapy in East Africa. Infect. Genet. Evol. 7:562-569.
15. Orr HA. 2009. Fitness and its role in evolutionary genetics. Nat. Rev. Genet. 10:531-539.
16. Bjorkman J, Andersson DI. 2000. The cost of antibiotic resistance from a bacterial perspective. Drug Resist Updat. 3:237-245.
17. Fohl LM, Roos DS. 2003. Fitness effects of DHFR-TS mutations associated with pyrimethamine resistance in apicomplexan parasites. Mol. Microbiol. 50:1319-1327.
18. Lu J, Sista P, Giguel F, Greenberg M, Kuritzkes DR. 2004. Relative replicative fitness of human immunodeficiency virus type 1 mutants resistant to enfuvirtide (T-20). J. Virol. 78:4628-4637.
19. Mariam DH, Mengistu Y, Hoffner SE, Andersson DI. 2004. Effect of rpoB mutations conferring rifampin resistance on fitness of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 48:1289-1294.
20. Hayward R, Saliba KJ, Kirk K. 2005. pfmdr1 mutations associated with chloroquine resistance incur a fitness cost in Plasmodium falciparum. Mol. Microbiol. 55:1285-1295.
21. Ursing J, Kofoed PE, Rodrigues A, Rombo L. 2009. No seasonal accumulation of resistant P. falciparum when high-dose chloroquine is used. PLoS One 4:e6866. doi:10.1371/journal.pone.0006866.
22. Kublin JG, Cortese JF, Njunju EM, Mukadam RA, Wirima JJ, Kazembe PN, Djimde AA, Kouriba B, Taylor TE, Plowe CV. 2003. Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J. Infect. Dis. 187:1870-1875.
23. Mackinnon MJ, Hastings IM. 1998. The evolution of multiple drug resistance in malaria parasites. Trans. R. Soc. Trop. Med. Hyg. 92:188-195.
24. Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM. 2008. Evidence of artemisinin-resistant malaria in western Cambodia. N. Engl. J. Med. 359:2619-2620.
25. Wongsrichanalai C, Pickard AL, Wernsdorfer WH, Meshnick SR. 2002. Epidemiology of drug-resistant malaria. Lancet Infect. Dis. 2:209-218.
26. Reed MB, Saliba KJ, Caruana SR, Kirk K, Cowman AF. 2000. Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature 403:906-909.
27. Noedl H, Bronnert J, Yingyuen K, Attlmayr B, Kollaritsch H, Fukuda M. 2005. Simple histidine-rich protein 2 double-site sandwich enzymelinked immunosorbent assay for use in malaria drug sensitivity testing. Antimicrob. Agents Chemother. 49:3575-3577.
28. Cox-Singh J, Singh B, Alias A, Abdullah MS. 1995. Assessment of the association between three pfmdr1 point mutations and chloroquine resistance in vitro of Malaysian Plasmodium falciparum isolates. Trans. R. Soc. Trop. Med. Hyg. 89:436-437.
29. Cheesman S, Creasey A, Degnan K, Kooij T, Afonso A, Cravo P, Carter R, Hunt P. 2007. Validation of pyrosequencing for accurate and high throughput estimation of allele frequencies in malaria parasites. Mol. Biochem. Parasitol. 152:213-219.
30. Martensson A, Stromberg J, Sisowath C, Msellem MI, Gil JP, Montgomery SM, Olliaro P, Ali AS, Bjorkman A. 2005. Efficacy of artesunate plus amodiaquine versus that of artemether-lumefantrine for the treatment of uncomplicated childhood Plasmodium falciparum malaria in Zanzibar, Tanzania. Clin. Infect. Dis. 41:1079-1086.
31. Snounou G, Zhu X, Siripoon N, Jarra W, Thaithong S, Brown KN, Viriyakosol S. 1999. Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand. Trans. R. Soc. Trop. Med. Hyg. 93:369-374.
32. Hartl DL, Clark AG. 1997. Principles of population genetics Sinauer Associates, Sunderland, MA.
33. World Medical Association. 2008. WMA Declaration of Helsinki-ethical principles for medical research involving human subjects. World Medical Association. http://www.wma.net/en/30publications/10policies /b3/index.html.
34. ICH. 1996. Good clinical practice. ICH, Geneva, Switzerland. http://www .ich.org/products/guidelines/efficacy/efficacy-single/article/ good-clinical-practice.html.
35. WHO. 2011. Country antimalarial drug policies. WHO, Geneva, Switzerland.
36. Ferreira PE, Holmgren G, Veiga MI, Uhlen P, Kaneko A, Gil JP. 2011. PfMDR1: Mechanisms of transport modulation by functional polymorphisms. PLoS One 6:e23875. doi:10.1371/journal.pone.0023875.
37. Duraisingh MT, Cowman AF. 2005. Contribution of the pfmdr1 gene to antimalarial drug-resistance. Acta Trop. 94:181-190.
38. Rohrbach P, Sanchez CP, Hayton K, Friedrich O, Patel J, Sidhu AB, Ferdig MT, Fidock DA, Lanzer M. 2006. Genetic linkage of pfmdr1 with food vacuolar solute import in Plasmodium falciparum. EMBO J. 25: 3000-3011.
39. Krishna S, White NJ. 1996. Pharmacokinetics of quinine, chloroquine and amodiaquine. Clinical implications. Clin. Pharmacokinet. 30:263-299.
40. Stepniewska K, Taylor W, Sirima SB, Ouedraogo EB, Ouedraogo A, Gansane A, Simpson JA, Morgan CC, White NJ, Kiechel Jr. 2009. Population pharmacokinetics of artesunate and amodiaquine in African children. Malar J. 8:200. doi:10.1186/1475-2875-8-200.
41. Le Bras J, Durand R. 2003. The mechanisms of resistance to antimalarial drugs in Plasmodium falciparum. Fundam. Clin. Pharmacol. 17:147-153.
42. Froberg G, Jornhagen L, Morris U, Shakely D, Msellem MI, Gil JP, Bjorkman A, Martensson A. 2012. Decreased prevalence of Plasmodium falciparum resistance markers to amodiaquine despite its wide scale use as ACT partner drug in Zanzibar. Malar. J. 11:321. doi:10.1186/1475-2875-11-321.