Distribution of Drug Resistance Genotypes in Plasmodium falciparum in an Area of Limited Parasite Diversity in Saudi Arabia

Saad M. Bin Dajem Department of Biochemistry, Faculty of Medicine, Sultan Qaboos University, Muscat, Oman; National Center for Training and Research, Ministry of Health, Jazan, Saudi Arabia; Department of Biological and Medical Research, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia; Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom

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Hissa M. Al-Farsi Department of Biochemistry, Faculty of Medicine, Sultan Qaboos University, Muscat, Oman; National Center for Training and Research, Ministry of Health, Jazan, Saudi Arabia; Department of Biological and Medical Research, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia; Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom

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Zainab S. Al-Hashami Department of Biochemistry, Faculty of Medicine, Sultan Qaboos University, Muscat, Oman; National Center for Training and Research, Ministry of Health, Jazan, Saudi Arabia; Department of Biological and Medical Research, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia; Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom

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Adel Ali H. Al-Sheikh Department of Biochemistry, Faculty of Medicine, Sultan Qaboos University, Muscat, Oman; National Center for Training and Research, Ministry of Health, Jazan, Saudi Arabia; Department of Biological and Medical Research, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia; Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom

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Ahmed Al-Qahtani Department of Biochemistry, Faculty of Medicine, Sultan Qaboos University, Muscat, Oman; National Center for Training and Research, Ministry of Health, Jazan, Saudi Arabia; Department of Biological and Medical Research, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia; Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom

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Hamza A. Babiker Department of Biochemistry, Faculty of Medicine, Sultan Qaboos University, Muscat, Oman; National Center for Training and Research, Ministry of Health, Jazan, Saudi Arabia; Department of Biological and Medical Research, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia; Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom

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Two hundred and three Plasmodium falciparum isolates from Jazan area, southwest Saudi Arabia, were typed for Pfcrt, Pfmdr1, dhps, and dhfr mutations associated with resistance to chloroquine, mefloquine, halofantrine, artemisinin, sulfadoxine-pyrimethamine, and the neutral polymorphic gene Pfg377. A large proportion (33%) of isolates harbored double mutant dhfr genotype (51I,59C,108N). However, only one isolate contained mutation dhps-437G. For Pfcrt, almost all examined isolates (163; 99%) harbored the mutant genotype (72C,73V,74I,75E,76T), whereas only 49 (31%) contained the mutant Pfmdr1 genotype (86Y,184F,1034S,1042N), 109 (66%) harbored the single mutant genotype (86N,184F,1034S,1042N), and no mutations were seen in codons 1034, 1042, and 1246. Nonetheless, three new single-nucleotide polymorphisms were detected at codons 182, 192, and 102. No differences were seen in distribution of drug resistance genes among Saudis and expatriates. There was a limited multiplicity (5%), mean number of clones (1.05), and two dominant multilocus genotypes among infected individuals in Jazan. A pattern consistent with limited cross-mating and recombination among local parasite was apparent.

Author Notes

*Address correspondence to Hamza A. Babiker, Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alkhod, PO Box 35, Muscat, Oman. E-mail: H.babiker@ed.ac.uk

Authors' addresses: Saad M. Bin Dajem, College of Science, King Khalid University, Abha, Kingdom of Saudi Arabia, E-mail: saad1426@gmail.com. Hissa M. Al-Farsi, Zainab S. Al-Hashami, and Hamza A. Babiker, Department of Biochemistry, Faculty of Medicine, Sultan Qaboos University, Muscat, Oman, E-mails: noornoor440@gmail.com, zainab44salam@gmail.com, and H.babiker@ed.ac.uk. Adel Ali H. Al-Sheikh, National Center for Training and Research, MOH, Jazan, Saudi Arabia, E-mail: adelalsheikh@gmail.com. Ahmed Al-Qahtani, Department of Biological and Medical Research, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia, E-mail: aqahtani@kfshrc.edu.sa.

  • 1.

    Abdel-Hameed AA, 2003. Antimalarial drug resistance in the eastern mediterranean region. East Mediterr Health J 9: 492508.

  • 2.

    Abdo-Rabbo A, Bassili A, Atta H, 2005. The quality of antimalarials available in yemen. Malar J 4: 28.

  • 3.

    Al-Mekhlafi AM, Mahdy MAK, Al-Mekhlafi HM, Azazy AA, Fong MY, 2011. High frequency of Plasmodium falciparum chloroquine resistance marker (pfcrt t76 mutation) in Yemen: an urgent need to re-examine malaria drug policy. Parasit Vectors 4: 94.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Dawoud HA, Ageely HM, El-Sheikh AH, Heiba AA, 2009. Molecular surveillance of Plasmodium falciparum chloroquine resistance transporter variant t76 in jazan area, kingdom of Saudi Arabia. J Egypt Soc Parasitol 39: 503510.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    WHO/Regional Office for the Eastern Mediterranean, 2007. Strategic plan for malaria control and elimination in the WHO Eastern Mediterranean Region 2006–2010. Cairo: World Health Organization Regional Office for the Eastern Mediterranea, 41.

    • PubMed
    • Export Citation
  • 6.

    Zaher T, Ahmadi M, Ibrahim A, El-Bahnasawy M, Gouda H, Shahat SAR, 2007. Malaria in Egypt, Saudi Arabia and Yemen: a clinical pilot study. J Egypt Soc Parasitol 37: 969976.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Al-Tawfiq JA, 2006. Epidemiology of travel-related malaria in a non-malarious areas in Saudi Arabia. Saudi Med J 27: 17811782.

  • 8.

    Bashwari LA, Mandil AM, Bahnassy AA, Al-Shamsi MA, Bukhari HA, 2001. Epidemiological profile of malaria in a university hospital in the eastern region of Saudi Arabia. Saudi Med J 22: 133138.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Bin Dajem SM, Al-Qahtani A, 2010. Analysis of gene mutations involved in chloroquine resistance in Plasmodium falciparum parasites isolated from patients in the southwest of Saudi Arabia. Ann Saudi Med 30: 187192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Malik GM, Seidi O, El-Taher A, Mohammed AS, 1998. Clinical aspects of malaria in the Asir region, Saudi Arabia. Ann Saudi Med 18: 1517.

  • 11.

    Omar MS, Malik GM, Al-Amari OM, Abdalla SE, Moosa RA, 1999. The rapid manual parasight-f test for diagnosing Plasmodium falciparum malaria in saudi arabia. Ann Saudi Med 19: 159162.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Al-Harthi SA, 2007. Detection of drug resistance markers for chloroquine and pyrimethamine-sulfadoxine in Jazan area, Saudi Arabia using PCR and restriction digestion. J Egypt Soc Parasitol 37: 1730.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    al Arishi HM, el Awad Ahmed F, al Bishi LA, 2001. Chloroquine-resistant Plasmodium falciparum malaria among children seen in a regional hospital, tabuk, Saudi Arabia. Trans R Soc Trop Med Hyg 95: 439440.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Alrajhi AA, Rahim I, Akood M, Hazmi M, 1999. Chloroquine-resistant Plasmodium falciparum cerebral malaria in a chloroquine-susceptible area. J Infect Dis 180: 17381741.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Ghalib HW, Al-Ghamdi S, Akood M, Haridi AEA, Ageel AAM, Abdalla RE, 2001. Therapeutic efficacy of chloroquine against uncomplicated, Plasmodium falciparum malaria in southwestern Saudi Arabia. Ann Trop Med Parasitol 95: 773779.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Humphreys GS, Merinopoulos I, Ahmed J, Whitty CJM, Mutabingwa TK, Sutherland CJ, Hallett RL, 2007. Amodiaquine and artemether-lumefantrine select distinct alleles of the Plasmodium falciparum mdr1 gene in Tanzanian children treated for uncomplicated malaria. Antimicrob Agents Chemother 51: 991997.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Sisowath C, Petersen I, Veiga MI, Mårtensson A, Premji Z, Björkman 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: 750757.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Bosman A, Mendis KN, 2007. A major transition in malaria treatment: the adoption and deployment of artemisinin-based combination therapies. Am J Trop Med Hyg 77: 193197.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE, 1995. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg 52: 565568.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Abdel-Muhsin AA, Mackinnon MJ, Awadalla P, Ali E, Suleiman S, Ahmed S, Walliker D, Babiker HA, 2003. Local differentiation in Plasmodium falciparum drug resistance genes in sudan. Parasitology 126: 391400.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    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: 257263.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Plowe CV, Cortese JF, Djimde A, Nwanyanwu OC, Watkins WM, Winstanley PA, Estrada-Franco JG, Mollinedo RE, Avila JC, Cespedes JL, Carter D, Doumbo OK, 1997. Mutations in Plasmodium falciparum dihydrofolate reductase and dihydropteroate synthase and epidemiologic patterns of pyrimethamine-sulfadoxine use and resistance. J Infect Dis 176: 15901596.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Alano P, Read D, Bruce M, Aikawa M, Kaido T, Tegoshi T, Bhatti S, Smith DK, Luo C, Hansra S, Carter R, Elliott JF, 1995. Cos cell expression cloning of pfg377, a Plasmodium falciparum gametocyte antigen associated with osmiophilic bodies. Mol Biochem Parasitol 74: 143156.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Nassir E, Abdel-Muhsin A-MA, Suliaman S, Kenyon F, Kheir A, Geha H, Ferguson HM, Walliker D, Babiker HA, 2005. Impact of genetic complexity on longevity and gametocytogenesis of Plasmodium falciparum during the dry and transmission-free season of eastern Sudan. Int J Parasitol 35: 4955.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Kheir A, Nwakanma D, Al-Gazali A, Akbarova Y, Al-Saai S, Swedberg G, Babiker HA, 2010. Transmission and cross-mating of high-level resistance Plasmodium falciparum dihydrofolate reductase haplotypes in the Gambia. Am J Trop Med Hyg 82: 535541.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Nwakanma D, Kheir A, Sowa M, Dunyo S, Jawara M, Pinder M, Milligan P, Walliker D, Babiker HA, 2008. High gametocyte complexity and mosquito infectivity of Plasmodium falciparum in the Gambia. Int J Parasitol 38: 219227.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Menegon M, Severini C, Sannella A, Paglia MG, Sangaré D, Abdel-Wahab A, Abdel-Muhsin AA, Babiker H, Walliker D, Alano P, 2000. Genotyping of Plasmodium falciparum gametocytes by reverse transcriptase polymerase chain reaction. Mol Biochem Parasitol 111: 153161.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Hill WG, Babiker HA, 1995. Estimation of numbers of malaria clones in blood samples. Proc Biol Sci 262: 249257.

  • 29.

    Cowman AF, Foote SJ, 1990. Chemotherapy and drug resistance in malaria. Int J Parasitol 20: 503513.

  • 30.

    Peterson DS, Milhous WK, Wellems TE, 1990. Molecular basis of differential resistance to cycloguanil and pyrimethamine in Plasmodium falciparum malaria. Proc Natl Acad Sci USA 87: 30183022.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Mixson-Hayden T, Jain V, McCollum AM, Poe A, Nagpal AC, Dash AP, Stiles JK, Udhayakumar V, Singh N, 2010. Evidence of selective sweeps in genes conferring resistance to chloroquine and pyrimethamine in Plasmodium falciparum isolates in India. Antimicrob Agents Chemother 54: 9971006.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    World Health Organization, 2008. World malaria report. Available at: http://books.google.com.om/books? P 42

  • 33.

    Alkadi HO, Al-Maktari MT, Nooman MA, 2006. Chloroquine-resistant Plasmodium falciparum local strain in taiz governorate, republic of Yemen. Chemotherapy 52: 166170.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Babiker HA, Pringle SJ, Abdel-Muhsin A, Mackinnon M, Hunt P, Walliker D, 2001. High-level chloroquine resistance in sudanese isolates of Plasmodium falciparum is associated with mutations in the chloroquine resistance transporter gene pfcrt and the multidrug resistance gene pfmdr1. J Infect Dis 183: 15351538.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Saliba KJ, Caruana SR, Reed MB, Kirk K, 2000. Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature 403: 906909.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Nzila AM, Mberu EK, Sulo J, Dayo H, Winstanley PA, Sibley CH, Watkins WM, 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: 991996.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Sibley CH, Hyde JE, Sims PF, Plowe CV, Kublin JG, Mberu EK, Cowman AF, Winstanley PA, Watkins WM, Nzila AM, 2001. Pyrimethamine-sulfadoxine resistance in Plasmodium falciparum: what next? Trends Parasitol 17: 582588.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Nair S, Williams JT, Brockman A, Paiphun L, Mayxay M, Newton PN, Guthmann J-P, Smithuis FM, Hien TT, White NJ, Nosten F, Anderson TJC, 2003. A selective sweep driven by pyrimethamine treatment in southeast Asian malaria parasites. Mol Biol Evol 20: 15261536.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Roper C, Pearce R, Nair S, Sharp B, Nosten F, Anderson T, 2004. Intercontinental spread of pyrimethamine-resistant malaria. Science 305: 1124.

  • 40.

    Babiker HA, Abdel-Muhsin ABA, Ranford-Cartwright LC, Satti G, Walliker D, 1998. Characteristics of Plasmodium falciparum parasites that survive the lengthy dry season in eastern sudan where malaria transmission is markedly seasonal. Am J Trop Med Hyg 59: 582590.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, Baruch DI, Magill AJ, Su XZ, 2002. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418: 320323.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Laufer MK, Thesing PC, Eddington ND, Masonga R, Dzinjalamala FK, Takala SL, Taylor TE, Plowe CV, 2006. Return of chloroquine antimalarial efficacy in malawi. N Engl J Med 355: 19591966.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Alifrangis M, Lusingu JP, Mmbando B, Dalgaard MB, Vestergaard LS, Ishengoma D, Khalil IF, Theander TG, Lemnge MM, Bygbjerg IC, 2009. Short report: five-year surveillance of molecular markers of Plasmodium falciparum antimalarial drug resistance in Korogwe district, Tanzania: accumulation of the 581g mutation in the P. falciparum dihydropteroate synthase gene. Am J Trop Med Hyg 80: 523527.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Mwai L, Ochong E, Abdirahman A, Kiara SM, Ward S, Kokwaro G, Sasi P, Marsh K, Borrmann S, Mackinnon M, Nzila A, 2009. Chloroquine resistance before and after its withdrawal in Kenya. Malar J 8: 106.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Ochong EO, Van den Broek IVF, Keus K, Nzila A, 2003. 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. Am J Trop Med Hyg 69: 184187.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Wang X, Mu J, Li G, Chen P, Guo X, Fu L, Chen L, Su X, Wellems TE, 2005. 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. Am J Trop Med Hyg 72: 410414.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Roper C, Walliker D, Duraisingh MT, Warhurst DC, 2000. Increased sensitivity to the antimalarials mefloquine and artemisinin is conferred by mutations in the. Mol Microbiol 36: 955961.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Pickard AL, Wongsrichanalai C, Purfield A, Kamwendo D, Emery K, Zalewski C, Kawamoto F, Miller RS, Meshnick SR, 2003. Resistance to antimalarials in southeast Asia and genetic polymorphisms in pfmdr1. Antimicrob Agents Chemother 47: 24182423.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49.

    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: 29432949.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Sidhu ABS, Uhlemann A-C, Valderramos SG, Valderramos J-C, 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: 528535.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Shah NK, Alker AP, Sem R, Susanti AI, Muth S, Maguire JD, Duong S, Ariey F, Meshnick SR, Wongsrichanalai C, 2008. Molecular surveillance for multidrug-resistant Plasmodium falciparum, Cambodia. Emerg Infect Dis 14: 16371640.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    Vathsala PG, Pramanik A, Dhanasekaran S, Devi CU, Pillai CR, Subbarao SK, Ghosh SK, Tiwari SN, Sathyanarayan TS, Deshpande PR, Mishra GC, Ranjit MR, Dash AP, Rangarajan PN, Padmanaban G, 2004. Widespread occurrence of the Plasmodium falciparum chloroquine resistance transporter (pfcrt) gene haplotype svmnt in P. falciparum malaria in India. Am J Trop Med Hyg 70: 256259.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Lekana-Douki JB, Dinzouna Boutamba SD, Zatra R, Zang Edou SE, Ekomy H, Bisvigou U, Toure-Ndouo FS, 2011. 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. Infect Genet Evol 11: 512517.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54.

    Jalousian F, Dalimi A, Samiee SM, Ghaffarifar F, Soleymanloo F, Naghizadeh R, 2008. Mutation in pfmdr1 gene in chloroquine-resistant Plasmodium falciparum isolates, southeast Iran. Int J Infect Dis 12: 630634.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55.

    Zakeri S, Afsharpad M, Kazemzadeh T, Mehdizadeh K, Shabani A, Djadid ND, 2008. Association of pfcrt but not pfmdr1 alleles with chloroquine resistance in iranian isolates of Plasmodium falciparum. Am J Trop Med Hyg 78: 633640.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56.

    Babiker HA, Walliker D, 1997. Current views on the population structure of Plasmodium falciparum: implications for control. Parasitol Today 13: 262267.

  • 57.

    Ballif M, Hii J, Marfurt J, Crameri A, Fafale A, Felger I, Beck H-P, Genton B, 2010. Monitoring of malaria parasite resistance to chloroquine and sulphadoxine-pyrimethamine in the Solomon Islands by DNA microarray technology. Malar J 9: 270.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 58.

    Huijben S, Nelson WA, Wargo AR, Sim DG, Drew DR, Read AF, 2010. Chemotherapy, within-host ecology and the fitness of drug-resistant malaria parasites. Evolution 64: 29522968.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 59.

    Wargo AR, Huijben S, de Roode JC, Shepherd J, Read AF, 2007. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc Natl Acad Sci USA 104: 1991419919.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 60.

    Mackinnon MJ, 2005. Drug resistance models for malaria. Acta Trop 94: 207217.

  • 61.

    Griffing S, Syphard L, Sridaran S, McCollum AM, Mixson-Hayden T, Vinayak S, Villegas L, Barnwell JW, Escalante AA, Udhayakumar V, 2010. Pfmdr1 amplification and fixation of pfcrt chloroquine resistance alleles in Plasmodium falciparum in Venezuela. Antimicrob Agents Chemother 54: 15721579.

    • PubMed
    • Search Google Scholar
    • Export Citation
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