Temporal and seasonal changes of genetic polymorphisms associated with altered drug susceptibility to chloroquine, lumefantrine, and quinine in Guinea-Bissau between 2003 and 2012

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 2, 2015, Pages 872-879

  Jovel, Irina Tatiana ^a,b   Kofoed, Poul Erik ^c,d   Rombo, Lars ^e   Rodrigues, Amabelia ^c   Ursing, Johan ^a,c,f  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL AUTONOMOUS UNIVERSITY OF HONDURAS   (Honduras)

^c Studies of the Epidemiology of Epilepsy in Demographic Surveillance Systems   (Guinea-Bissau)

^d KOLDING HOSPITAL   (Denmark)

^e UPPSALA CLINICAL RESEARCH CENTER   (Sweden)

^f KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMETHER PLUS BENFLUMETOL; BENFLUMETOL; CHLOROQUINE; QUININE; ANTIMALARIAL AGENT; ETHANOLAMINE DERIVATIVE; FLUORENE DERIVATIVE;

ARTICLE; BLOOD SAMPLING; CHILD; DRUG SENSITIVITY; FEMALE; GENE DOSAGE; GENE FREQUENCY; GENETIC POLYMORPHISM; GUINEA-BISSAU; HEALTH CENTER; HUMAN; MALARIA FALCIPARUM; MALE; NONHUMAN; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEASONAL VARIATION; ADOLESCENT; CLINICAL TRIAL; MALARIA, FALCIPARUM; PRESCHOOL CHILD;

ADOLESCENT; ANTIMALARIALS; CHILD; CHILD, PRESCHOOL; CHLOROQUINE; ETHANOLAMINES; FEMALE; FLUORENES; GUINEA-BISSAU; HUMANS; MALARIA, FALCIPARUM; MALE; QUININE;

EID: 84921900760     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.03554-14     Document Type: Article

References (41)

1. World Health Organization. 2012. World malaria report. World Health Organization, Geneva, Switzerland.
2. nd ed. World Health Organization, Geneva, Switzerland.
3. Ursing J, Kofoed PE, Rodrigues A, Blessborn D, Thoft-Nielsen R, Bjorkman A, Rombo L. 2011. Similar efficacy and tolerability of doubledose chloroquine and artemether-lumefantrine for treatment of Plasmodium falciparum infection in Guinea-Bissau: a randomized trial. J Infect Dis 203:109-116. http://dx.doi.org/10.1093/infdis/jiq001.
4. Kofoed PE, Co F, Johansson P, Dias F, Cabral C, Hedegaard K, Aaby P, Rombo L. 2002. Treatment of uncomplicated malaria in children in Guinea-Bissau with chloroquine, quinine, and sulfadoxinepyrimethamine. Trans R Soc Trop Med Hyg 96:304-309. http://dx.doi .org/10.1016/S0035-9203(02)90107-0.
5. Ursing J, Rombo L, Rodrigues A, Aaby P, Kofoed PE. 2014. Malaria transmission in Bissau, Guinea-Bissau, between 1995 and 2012: malaria resurgence did not negatively affect mortality. PLoS One 9:e101167. http: //dx.doi.org/10.1371/journal.pone.0101167.
6. Djimdé 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. http://dx.doi.org/10.1056 /NEJM200101253440403.
7. Malmberg M, Ferreira PE, Tarning J, Ursing J, Ngasala B, Bjorkman A, Martensson A, Gil JP. 2013. Plasmodium falciparum drug resistance phenotype as assessed by patient antimalarial drug levels and its association with pfmdr1 polymorphisms. J Infect Dis 207:842-847. http://dx.doi.org /10.1093/infdis/jis747.
8. Sisowath C, Petersen I, Veiga MI, Martensson A, Premji Z, Bjorkman A, Fidock DA, Gil JP. 2009. In vivo selection of Plasmodium falciparum parasites carrying the chloroquine-susceptible pfcrt K76 allele after treatment with artemether-lumefantrine in Africa. J Infect Dis 199:750-757. http://dx.doi.org/10.1086/596738.
9. Sisowath C, Stromberg J, Martensson A, Msellem M, Obondo C, Bjorkman A, Gil JP. 2005. In vivo selection of Plasmodium falciparum pfmdr1 86N coding alleles by artemether-lumefantrine (Coartem). J Infect Dis 191:1014-1017. http://dx.doi.org/10.1086/427997.
10. Fidock DA, Nomura T, Talley AK, Cooper RA, Dzekunov SM, Ferdig MT, Ursos LM, Sidhu AB, Naude B, Deitsch KW, Su XZ, Wootton JC, Roepe PD, Wellems TE. 2000. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 6:861-871. http://dx.doi.org/10.1016 /S1097-2765(05)00077-8.
11. Summers RL, Dave A, Dolstra TJ, Bellanca S, Marchetti RV, Nash MN, Richards SN, Goh V, Schenk RL, Stein WD, Kirk K, Sanchez CP, Lanzer M, Martin RE. 2014. Diverse mutational pathways converge on saturable chloroquine transport via the malaria parasite's chloroquine resistance transporter. Proc Natl Acad SciUSA 111:E1759-E1767. http://dx.doi.org /10.1073/pnas.1322965111.
12. Ursing J, Kofoed PE, Rodrigues A, Rombo L, Gil JP. 2007. Plasmodium falciparum genotypes associated with chloroquine and amodiaquine resistance in Guinea-Bissau. Am J Trop Med Hyg 76:844-848.
13. Ursing J, Schmidt BA, Lebbad M, Kofoed PE, Dias F, Gil JP, Rombo L. 2007. Chloroquine resistant P. falciparum prevalence is low and unchanged between 1990 and 2005 in Guinea-Bissau: an effect of high chloroquine dosage? Infect Genet Evol 7:555-561. http://dx.doi.org/10.1016/j .meegid.2007.03.006.
14. Mwai L, Kiara SM, Abdirahman A, Pole L, Rippert A, Diriye A, Bull P, Marsh K, Borrmann S, Nzila A. 2009. In vitro activities of piperaquine, lumefantrine, and dihydroartemisinin in Kenyan Plasmodium falciparum isolates and polymorphisms in pfcrt and pfmdr1. Antimicrob Agents Chemother 53:5069-5073. http://dx.doi.org/10.1128/AAC.00638-09.
15. Thomsen TT, Madsen LB, Hansson HH, Tomas EV, Charlwood D, Bygbjerg IC, Alifrangis M. 2013. Rapid selection of Plasmodium falciparum chloroquine resistance transporter gene and multidrug resistance gene-1 haplotypes associated with past chloroquine and present artemetherlumefantrine use in Inhambane District, southern Mozambique. Am J Trop Med Hyg 88:536-541. http://dx.doi.org/10.4269/ajtmh.12-0525.
16. Malmberg M, Ngasala B, Ferreira PE, Larsson E, Jovel I, Hjalmarsson A, Petzold M, Premji Z, Gil JP, Bjorkman A, Martensson A. 2013. Temporal trends of molecular markers associated with artemetherlumefantrine tolerance/resistance in Bagamoyo district, Tanzania. Malar J 12:103. http://dx.doi.org/10.1186/1475-2875-12-103.
17. Cui L, Wang Z, Miao J, Miao M, Chandra R, Jiang H, Su XZ. 2012. Mechanisms of in vitro resistance to dihydroartemisinin in Plasmodium falciparum. Mol Microbiol 86:111-128. http://dx.doi.org/10.1111/j.1365 -2958.2012.08180.x.
18. Price RN, Cassar C, Brockman A, Duraisingh M, van Vugt M, White NJ, Nosten F, Krishna S. 1999. The pfmdr1 gene is associated with a multidrug-resistant phenotype in Plasmodium falciparum from the western border of Thailand. Antimicrob Agents Chemother 43:2943-2949.
19. Sidhu AB, Uhlemann AC, Valderramos SG, Valderramos JC, Krishna S, Fidock DA. 2006. Decreasing pfmdr1 copy number in Plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin. J Infect Dis 194:528-535. http://dx.doi .org/10.1086/507115.
20. Veiga MI, Ferreira PE, Malmberg M, Jornhagen L, Bjorkman A, Nosten F, Gil JP. 2012. pfmdr1 amplification is related to increased Plasmodium falciparum in vitro sensitivity to the bisquinoline piperaquine. Antimicrob Agents Chemother 56:3615-3619. http://dx.doi.org/10.1128/AAC.06350-11.
21. 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. http://dx.doi.org/10.1038/35002615.
22. Mu J, Ferdig MT, Feng X, Joy DA, Duan J, Furuya T, Subramanian G, Aravind L, Cooper RA, Wootton JC, Xiong M, Su XZ. 2003. Multiple transporters associated with malaria parasite responses to chloroquine and quinine. Mol Microbiol 49:977-989. http://dx.doi.org/10.1046/j.1365 -2958.2003.03627.x.
23. Ord R, Alexander N, Dunyo S, Hallett R, Jawara M, Targett G, Drakeley CJ, Sutherland CJ. 2007. Seasonal carriage of pfcrt and pfmdr1 alleles in Gambian Plasmodium falciparum imply reduced fitness of chloroquineresistant parasites. J Infect Dis 196:1613-1619. http://dx.doi.org/10.1086 /522154.
24. Kofoed PE, Ursing J, Poulsen A, Rodrigues A, Bergquist Y, Aaby P, Rombo L. 2007. Different doses of amodiaquine and chloroquine for treatment of uncomplicated malaria in children in Guinea-Bissau: implications for future treatment recommendations. Trans R Soc Trop Med Hyg 101:231-238. http://dx.doi.org/10.1016/j.trstmh.2006.05.008.
25. Kofoed PE, Ursing J, Rodrigues A, Rombo L. 2011. Paracetamol versus placebo in treatment of nonsevere malaria in children in Guinea-Bissau: a randomized controlled trial. Malar J 10:148. http://dx.doi.org/10.1186 /1475-2875-10-148.
26. 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. http://dx.doi.org/10.1371/journal.pone.0006866.
27. Ursing J, Kofoed PE, Rombo L, Gil JP. 2006. No pfmdr1 amplifications in samples from Guinea-Bissau and Liberia collected between 1981 and 2004. J Infect Dis 194:716-718. http://dx.doi.org/10.1086/506456.
28. Ursing J, Kofoed PE, Rodrigues A, Bergqvist Y, Rombo L. 2009. Chloroquine is grossly overdosed and overused but well tolerated in Guinea-Bissau. Antimicrob Agents Chemother 53:180-185. http://dx.doi.org/10 .1128/AAC.01111-08.
29. Veiga MI, Ferreira PE, Bjorkman A, Gil JP. 2006. Multiplex PCR-RFLP methods for pfcrt, pfmdr1 and pfdhfr mutations in Plasmodium falciparum. Mol Cell Probes 20:100-104. http://dx.doi.org/10.1016/j.mcp.2005.10 .003.
30. 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. http://dx.doi.org/10.1016/j.meegid.2007.03.005.
31. 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. http://dx.doi.org /10.1086/375419.
32. Frosch AE, Laufer MK, Mathanga DP, Takala-Harrison S, Skarbinski J, Claassen CW, Dzinjalamala F, Plowe CV. 2014. The return of widespread chloroquine-sensitive Plasmodium falciparum to Malawi. J Infect Dis 210:1110-1114. http://dx.doi.org/10.1093/infdis/jiu216.
33. Cooper RA, Lane KD, Deng B, Mu J, Patel JJ, Wellems TE, Su X, Ferdig MT. 2007. Mutations in transmembrane domains 1, 4 and 9 of the Plasmodium falciparum chloroquine resistance transporter alter susceptibility to chloroquine, quinine and quinidine. Mol Microbiol 63:270-282. http: //dx.doi.org/10.1111/j.1365-2958.2006.05511.x.
34. Sanchez CP, Stein WD, Lanzer M. 2008. Dissecting the components of quinine accumulation in Plasmodium falciparum. Mol Microbiol 67: 1081-1093. http://dx.doi.org/10.1111/j.1365-2958.2008.06108.x.
35. Cheruiyot J, Ingasia LA, Omondi AA, Juma DW, Opot BH, Ndegwa JM, Mativo J, Cheruiyot AC, Yeda R, Okudo C, Muiruri P, Bidii NS, Chebon LJ, Angienda PO, Eyase FL, Johnson JD, Bulimo WD, Andagalu B, Akala HM, Kamau E. 2014. Polymorphisms in pfmdr1, pfcrt and pfnhe1 genes are associated with reduced in vitro activities of quinine in Plasmodium falciparum isolates from western Kenya. Antimicrob Agents Chemother 58:3737-3743. http://dx.doi.org/10.1128/AAC.02472-14.
36. Gadalla NB, Malmberg M, Adam I, Oguike MC, Beshir K, Elzaki SE, Mukhtar I, Gadalla AA, Warhurst DC, Ngasala B, Martensson A, El-Sayed BB, Gil JP, Sutherland CJ. 24 September 2014. Alternatively spliced transcripts and novel pseudogenes of the Plasmodium falciparum resistance-associated locus pfcrt detected in East African malaria patients. J Antimicrob Chemother http://dx.doi.org/10.1093/jac/dku358.
37. Ferdig MT, Cooper RA, Mu J, Deng B, Joy DA, Su XZ, Wellems TE. 2004. Dissecting the loci of low-level quinine resistance in malaria parasites. Mol Microbiol 52:985-997. http://dx.doi.org/10.1111/j.1365-2958 .2004.04035.x.
38. Duah NO, Matrevi SA, de Souza DK, Binnah DD, Tamakloe MM, Opoku VS, Onwona CO, Narh CA, Quashie NB, Abuaku B, Duplessis C, Kronmann KC, Koram KA. 2013. Increased pfmdr1 gene copy number and the decline in pfcrt and pfmdr1 resistance alleles in Ghanaian Plasmodium falciparum isolates after the change of antimalarial drug treatment policy. Malar J 12:377. http://dx.doi.org/10.1186 /1475-2875-12-377.
39. Boni MF, Smith DL, Laxminarayan R. 2008. Benefits of using multiple first-line therapies against malaria. Proc Natl Acad Sci U S A 105:14216-14221. http://dx.doi.org/10.1073/pnas.0804628105.
40. Veiga MI, Ferreira PE, Jornhagen L, Malmberg M, Kone A, Schmidt BA, Petzold M, Bjorkman A, Nosten F, Gil JP. 2011. Novel polymorphisms in Plasmodium falciparum ABC transporter genes are associated with major ACT antimalarial drug resistance. PLoS One 6:e20212. http: //dx.doi.org/10.1371/journal.pone.0020212.
41. Andriantsoanirina V, Ratsimbasoa A, Bouchier C, Jahevitra M, Rabearimanana S, Radrianjafy R, Andrianaranjaka V, Randriantsoa T, Rason MA, Tichit M, Rabarijaona LP, Mercereau-Puijalon O, Durand R, Menard D. 2009. Plasmodium falciparum drug resistance in Madagascar: facing the spread of unusual pfdhfr and pfmdr-1 haplotypes and the decrease of dihydroartemisinin susceptibility. Antimicrob Agents Chemother 53:4588-4597. doihttp://dx.doi.org/10.1128/AAC.00610-09.