Rapid dissemination of Plasmodium falciparum drug resistance despite strictly controlled antimalarial use

PLoS ONE

Volumn 2, Issue 1, 2007, Pages

  Noranate, Nitchakarn ^a,i   Durand, Rémy ^b   Tall, Adama ^c   Marrama, Laurence ^c   Spiegel, André ^c   Sokhna, Cheikh ^d   Pradines, Bruno ^e   Cojean, Sandrine ^f   Guillotte, Micheline ^a   Bischoff, Emmanuel ^a   Ekala, Marie Théreèse ^a   Bouchier, Christiane ^g   Fandeur, Thierry ^h   Ariey, Frédéric ^h   Patarapotikul, Jintana ⁱ   Le Bras, Jacques ^f   Trape, Jean François ^d   Rogier, Christophe ^c,e   Mercereau Puijalon, Odile ^a  

^a CNRS   (France)

^b AVICENNE HOSPITAL   (France)

^c INSTITUT PASTEUR DE DAKAR   (Senegal)

^d INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (Senegal)

^e SERVICE DE SANTÉ DES ARMÉES   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g INSTITUT PASTEUR   (France)

^h INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

ⁱ MAHIDOL UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT; CHLOROQUINE; CHLOROQUINE TRANSPORTER; DIHYDROFOLATE REDUCTASE; FANSIDAR; GENE PRODUCT; HALOFANTRINE; PYRIMETHAMINE; QUINIMAX; QUININE; SULFADOXINE; UNCLASSIFIED DRUG; CARRIER PROTEIN; MICROSATELLITE DNA; PFCRT PROTEIN, PLASMODIUM FALCIPARUM; PROTOZOAL PROTEIN;

ADOLESCENT; ADULT; AGE DISTRIBUTION; ARTICLE; CHILD; CONTROLLED STUDY; DRUG EFFICACY; ENDEMIC DISEASE; ERADICATION THERAPY; FEMALE; GENE FREQUENCY; GENE SEQUENCE; GENOTYPE; HAPLOTYPE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INCIDENCE; MAJOR CLINICAL STUDY; MALARIA; MALE; MOLECULAR BEACON; MUTANT; NONHUMAN; PLASMODIUM FALCIPARUM; PREVALENCE; RETROSPECTIVE STUDY; ANIMAL; DNA SEQUENCE; DRUG EFFECT; DRUG RESISTANCE; DRUG SENSITIVITY; GENETICS; MALARIA FALCIPARUM; PHYSIOLOGY; PREGNANCY; PRESCHOOL CHILD; SENEGAL;

PLASMODIUM FALCIPARUM;

ADOLESCENT; ADULT; ANIMALS; ANTIMALARIALS; CHILD; CHILD, PRESCHOOL; CHLOROQUINE; DRUG RESISTANCE; FEMALE; GENOTYPE; HUMANS; MALARIA, FALCIPARUM; MALE; MEMBRANE TRANSPORT PROTEINS; MICROSATELLITE REPEATS; PARASITIC SENSITIVITY TESTS; PLASMODIUM FALCIPARUM; PREGNANCY; PROTOZOAN PROTEINS; PYRIMETHAMINE; RETROSPECTIVE STUDIES; SENEGAL; SEQUENCE ANALYSIS, DNA; SULFADOXINE; TETRAHYDROFOLATE DEHYDROGENASE;

EID: 34347359955     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0000139     Document Type: Article

References (54)

1. Trape JF (2001) The public health impact of chloroquine resistance in Africa. Am J Trop Med Hyg 64: 12-17.
2. Greenberg AE, Ntumbanzondo M, Ntula N, Mawa L, Howell J, et al. (1989) Hospital-based surveillance of malaria-related paediatric morbidity and mortality in Kinshasa, Zaire. Bull World Health Organ 67: 189-196.
3. Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, et al. (2002) Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418: 320-323.
4. Cortese JF, Caraballo A, Contreras CE, Plowe CV (2002) Origin and dissemination of Plasmodium falciparum drug-resistance mutations in South America. J Infect Dis 186: 999-1006.
5. Roper C, Pearce R, Bredenkamp B, Gumede J, Drakeley C, et al. (2003) Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet 361: 1174-1181.
6. Roper C, Pearce R, Nair S, Sharp B, Nosten F, et al. (2004) Intercontinental spread of pyrimethamine-resistant malaria. Science 305: 1124.
7. Fidock DA, Nomura T, Talley AK, Cooper RA, Dzekunov SM, et al. (2000) Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 6: 861-871.
8. Wellems TE (2004) Transporter of a malaria catastrophe. Nat Med 10: 1169-1171.
9. White NJ (2004) Antimalarial drug resistance. J Clin Invest 15: 1084-1092.
10. Plowe CV, Djimde A, Wellems TE, Diop S, Kouriba B, et al. (1996) Community pyrimethamine-sulfadoxine use and prevalence of resistant Plasmodium falciparum genotypes in Mali: a model for deterring resistance. Am J Trop Med Hyg 55: 467-471.
11. Depoortere E, Guthmann JP, Sipilanyambe N, Nkandu E, Fermon F, et al. (2004) Adherence to the combination of sulphadoxine-pyrimethamine and artesunate in the Maheba refugee settlement, Zambia. Trop Med Int Health 9: 62-67.
12. Depoortere E, Guthmann JP, Presse J, Sipilanyambe N, Nkandu E, et al. (2005) Efficacy and effectiveness of the combination of sulfadoxine/ pyrimethamine and a 3-day course of artesunate for the treatment of uncomplicated falciparum malaria in a refugee settlement in Zambia. Trop Med Int Health 10: 139-145.
13. Trape JF, Rogier C, Konate L, Diagne N, Bouganali H, et al. (1994) The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. Am J Trop Med Hyg 51: 123-137.
14. Trape JF, Rogier C (1996) Combating malaria morbidity and mortality by reducing transmission. Parasitol Today 12: 236-240.
15. Rogier C, Ly AB, Tall A, Cisse B, Trape JF (1999) Plasmodium falciparum clinical malaria in Dielmo, a holoendemic area in Senegal: no influence of acquired immunity on initial symptomatology and severity of malaria attacks. Am J Trop Med Hyg 60: 410-420.
16. Trape JF, Pison G, Spiegel A, Enel C, Rogier C (2002) Combating malaria in Africa. Trends Parasitol 18: 224-230.
17. Rogier C, Imbert P, Tall A, Sokhna C, Spiegel A, et al. (2003) Epidemiological and clinical aspects of blackwater fever among African children suffering frequent malaria attacks. Trans R Soc Trop Med Hyg 97: 193-197.
18. Djimde A, Doumbo OK, Cortese JF, Kayentao K, Doumbo S, et al. (2001) A molecular marker for chloroquine-resistant falciparum malaria. N Engl J Med 344: 257-263.
19. Peterson DS, Walliker D, Wellems TE (1988) Evidence that a point mutation in dihydrofolate reductase-thymidylate synthase confers resistance to pyrimethamine in falciparum malaria. Proc Natl Acad Sci U S A 85: 9114-9118.
20. Cowman AF, Morry MJ, Biggs BA, Cross GAM, Foote SJ (1988) Amino acid changes linked to pyrimethamine. resistance in the dihydrofolate reductase-thymidylate synthase gene of Plasmodium falciparum. Proc Natl Acad Sci U S A 85: 9109-9113.
21. Nzila AM, Nduati E, Mberu EK, Hopkins Sibley C, Monks SA, et al. (2000) 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. J Infect Dis 181: 2023-2028.
22. Nzila AM, Mberu EK, Sulo J, Dayo H, Winstanley PA, et al. (2000) Towards an understanding of the mechanism of pyrimethamine-sulfadoxine resistance in Plasmodium falciparum: genotyping of dihydrofolate reductase and dihydropteroate synthase of Kenyan parasites. Antimicrob Agents Chemother 44: 991-996.
23. Kublin JG, Dzinjalamala FK, Kamwendo DD, Malkin EM, Cortese JF, et al. (2002) Molecular markers for failure of sulfadoxine-pyrimethamine and chlorproguanil-dapsone treatment of Plasmodium falciparum malaria. J Infect Dis 185: 380-388.
24. Dieye A, Rogier C, Trape JF, Sarthou JL, Druilhe P (1997) HLA class I-associated resistance to severe malaria: a parasitological re-assessment. Parasitol Today 13: 48-49.
25. Sokhna CS, Rogier C, Dieye A, Trape JF (2000) Host factors affecting the delay of reappearance of Plasmodium falciparum after radical treatment among a semi-immune population exposed to intense perennial transmission. Am J Trop Med Hyg 62: 266-270.
26. Contamin H, Fandeur T, Rogier C, Bonnefoy S, Konate L, et al. (1996) Different genetic characteristics of Plasmodium falciparum isolates collected during successive clinical malaria episodes in Senegalese children. Am J Trop Med Hyg 54: 632-643.
27. Pradines B, Rogier C, Fusai T, Tall A, Trape JF, et al. (1996) In vitro sensitivity of 85 Plasmodium falciparum isolates in the Fatick region, Senegal] Med Trop (Mars) 56: 141-145.
28. Pradines B, Tall A, Parzy D, Spiegel A, Fusai T, et al. (1998) In-vitro activity of pyronaridine and amodiaquine against African isolates (Senegal) of Plasmodium falciparum in comparison with standard antimalarial agents. J Antimicrob Chemother 42: 333-339.
29. Pradines B, Tall A, Fusai T, Spiegel A, Hienne R, et al. (1999) In vitro activities of benflumetol against 158 Senegalese isolates of Plasmodium falciparum in comparison with those of standard antimalarial drugs. Antimicrob Agents Chemother 43: 418-420.
30. Contamin H, Fandeur T, Bonnefoy S, Skouri F, Ntoumi F, et al. (1995) PCR typing of field isolates of Plasmodium falciparum. J Clin Microbiol 33: 944-951.
31. Durand R, Eslahpazire J, Jafari S, Delabre JF, Marmorat-Khuong A, et al. (2000) Use of molecular beacons to detect an antifolate resistance-associated mutation in Plasmodium falciparum. Antimicrob Agents Chemother 44: 3461-3464.
32. Durand R, Huart V, Jafari S, Le Bras J (2002) Rapid detection of a molecular marker for chloroquine-resistant falciparum malaria. Antimicrob Agents Chemother 46: 2684-2686.
33. Ariey F, Fandeur T, Durand R, Randrianarivelojosia M, Jambou R, et al. (2006) Invasion of Africa by a single pfcrt allele of South East Asian type. Malar J 5: 34.
34. Khim N, Bouchier C, Ekala MT, Incardona S, Lim P, et al. (2005) Countrywide survey shows very high prevalence of Plasmodium falciparum multilocus resistance genotypes in Cambodia. Antimicrob Agents Chemother 49: 3147-3152.
35. Nair S, Williams JT, Brockman A, Paiphun L, Mayxay M, et al. (2003) A selective sweep driven by pyrimethamine treatment in Southeast Asian malaria parasites. Mol Biol Evol 20: 1526-1536.
36. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590.
37. Goudet J (1995) FSTAT (Version 1.2): A computer program to calculate F-statistics. Journal of Heredity 86: 485-486.
38. Anderson TJ, Nair S, Jacobzone C, Zavai A, Balkan S (2003) Molecular assessment of drug resistance in Plasmodium falciparum from Bahr El Gazal province, Sudan. Trop Med Int Health 8: 1068-1073.
39. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Heredity 86: 248-249.
40. Goudet J, Raymond M, De Meeüs T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144: 1933-1940.
41. Rogier C, Brau R, Tall A, Cisse B, Trape JF (1996) Reducing the oral quinine-quinidine-cinchonin (Quinimax®) treatment of uncomplicated malaria to three days does not increase the recurrence of attacks among children living in a highly endemic area of Senegal. Trans R Soc Trop Med Hyg 90: 175-178.
42. Mabuza A, Govere J, La Grange K, Mngomezulu N, Allen E, et al. (2005) Therapeutic efficacy of sulfadoxine-pyrimethamine for Plasmodium falciparum malaria. S Afr Med J 95: 346-349.
43. Ndiaye D, Daily JP, Sarr O, Ndir O, Gaye O, et al. (2005) Mutations in Plasmodium falciparum dihydrofolate reductase and dihydropteroate synthase genes in Senegal. Trop Med Int Health 10: 1176-1179.
44. Ndiaye D, Daily JP, Sarr O, Ndir O, Gaye O, et al. (2006) Defining the origin of Plasmodium falciparum resistant dhfr isolates in Senegal. Acta Tropica 99: 106-111.
45. Basco LK, Le Bras J (1997) In vitro sensitivity of Plasmodium falciparum to anti-folinic agents (trimethoprim, pyrimethamine, cycloguanil): a study of 29 African strains. Bull Soc Pathol Exot 90: 90-93.
46. Iyer JK, Milhous WK, Cortese JF, Kublin JG, Plowe CV (2001) Plasmodium falciparum cross-resistance between trimethoprim and pyrimethamine. Lancet 358: 1066-1067.
47. Thera MA, Sehdev PS, Coulibaly D, Traore K, Garba MN, et al. (2005) Impact of trimethoprim-sulfamethoxazole prophylaxis on falciparum malaria infection and disease. J Infect Dis 192: 1823-1829.
48. Chusacultanachai S, Thiensathit P, Tarnchompoo B, Sirawaraporn W, Yuthavong Y (2002) Novel antifolate resistant mutations of Plasmodium falciparum dihydrofolate reductase selected in Escherichia coli. Mol Biochem Parasitol 120: 61-72.
49. Fontenille D, Lochouarn L, Diatta M, Sokhna C, Dia I, et al. (1997) Four years' entomological study of the transmission of seasonal malaria in Senegal and the bionomics of Anopheles gambiae and A. arabiensis. Trans R Soc Trop Med Hyg 91: 647-652.
50. Mita T, Kaneko A, Lum JK, Bwijo B, Takechi M, et al. (2003) 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. Am J Trop Med Hyg 68: 413-415.
51. Laufer MK, Thesing PC, Eddington ND, Masonga R, Dzinjalamala FK, et al. (2006) Return of Chloroquine Antimalarial Efficacy in Malawi. N Engl J Med 355: 1959-66.
52. Kublin JG, Cortese JF, Njunju EM, Mukadam RA, Wirima JJ, et al. (2003) Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J Infect Dis 187: 1870-1875.
53. Mita T, Kaneko A, Lum JK, Zungu IL, Tsukahara T, et al. (2004) Expansion of wild type allele rather than back mutation in pfcrt explains the recent recovery of chloroquine sensitivity of Plasmodium falciparum in Malawi. Mol Biochem Parasitol 135: 159-163.
54. Sutherland CJ, Ord R, Dunyo S, Jawara M, Drakeley CJ, et al. (2005) Reduction of Malaria Transmission to Anopheles Mosquitoes with a Six-Dose Regimen of Co-Artemether. PLoS Med 2(4): e92 DOI: 10.1371/ journal. pmed.0020092.