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1
The efficacy of antimalarial monotherapies, sulphadoxine-pyrimethamine and amodiaquine in east Africa: implications for sub-regional policy, 2003. Trop Med Int Health 8: 860–867.
-
2
Kublin JG, Dzinjalamala FK, Kamwendo DD, Malkin EM, Cortese JF, Martino LM, Mukadam RA, Rogerson SJ, Lescano AG, Molyneux ME, Winstanley PA, Chimpeni P, Taylor TE, Plowe CV, 2002. Molecular markers for failure of sulfadoxine-pyrimethamine and chlorproguanil-dapsone treatment of Plasmodium falciparum malaria. J Infect Dis 185 :380–388.
-
3
Kyabayinze D, Cattamanchi A, Kamya MR, Rosenthal PJ, Dorsey G, 2003. Validation of a simplified method for using molecular markers to predict sulfadoxine-pyrimethamine treatment failure in African children with falciparum malaria. Am J Trop Med Hyg 69 :247–252.
-
4
Omar SA, Adagu IS, Warhurst DC, 2001. Can pretreatment screening for dhps and dhfr point mutations in Plasmodium falciparum infections be used to predict sulfadoxine-pyrimethamine treatment failure? Trans R Soc Trop Med Hyg 95 :315–319.
-
5
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.
-
6
Djimde A, Doumbo OK, Steketee RW, Plowe CV, 2001. Application of a molecular marker for surveillance of chloroquine-resistant falciparum malaria. Lancet 358 :890–891.
-
7
Wellems TE, Plowe CV, 2001. Chloroquine-resistant malaria. J Infect Dis 184 :770–776.
-
8
Plowe CV, 2003. Monitoring antimalarial drug resistance: making the most of the tools at hand. J Exp Biol 206 :3745–3752.
-
9
Basco LK, Ndounga M, Tejiokem M, Ngane VF, Youmba JC, Ringwald P, Soula G, 2002. Molecular epidemiology of malaria in Cameroon. XI. Geographic distribution of Plasmodium falciparum isolates with dihydrofolate reductase gene mutations in southern and central Cameroon. Am J Trop Med Hyg 67 :378–382.
-
10
Duraisingh MT, Curtis J, Warhurst DC, 1998. Plasmodium falciparum: detection of polymorphisms in the dihydrofolate reductase and dihydropteroate synthetase genes by PCR and restriction digestion. Exp Parasitol 89 :1–8.
-
11
Alifrangis M, Enosse S, Khalil IF, Tarimo DS, Lemnge MM, Thompson R, Bygbjerg IC, Ronn AM, 2003. Prediction of Plasmodium falciparum resistance to sulfadoxine/pyrimethamine in vivo by mutations in the dihydrofolate reductase and dihydropteroate synthetase genes: a comparative study between sites of differing endemicity. Am J Trop Med Hyg 69 :601–606.
-
12
Pearce RJ, Drakeley C, Chandramohan D, Mosha F, Roper C, 2003. Molecular determination of point mutation haplotypes in the dihydrofolate reductase and dihydropteroate synthase of Plasmodium falciparum in three districts of northern Tanzania. Antimicrob Agents Chemother 47 :1347–1354.
-
13
Abdel-Muhsin AM, Ranford-Cartwright LC, Medani AR, Ahmed S, Suleiman S, Khan B, Hunt P, Walliker D, Babiker HA, 2002. Detection of mutations in the Plasmodium falciparum dihydrofolate reductase (dhfr) gene by dot-blot hybridization. Am J Trop Med Hyg 67 :24–27.
-
14
Mehlotra RK, Fujioka H, Roepe PD, Janneh O, Ursos LM, Jacobs-Lorena V, McNamara DT, Bockarie MJ, Kazura JW, Kyle DE, Fidock DA, Zimmerman PA, 2001. Evolution of a unique Plasmodium falciparum chloroquine-resistance phenotype in association with pfcrt polymorphism in Papua New Guinea and South America. Proc Natl Acad Sci U S A 98 :12689–12694.
-
15
Staalsoe T, Giha HA, Dodoo D, Theander TG, Hviid L, 1999. Detection of antibodies to variant antigens on Plasmodium falciparum-infected erythrocytes by flow cytometry. Cytometry 35 :329–336.
-
16
Sambrook J, Fritsch EF, Maniatis T, 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Press.
-
17
Wooden J, Kyes S, Sibley CH, 1993. PCR and Strain Identification in Plasmodium falciparum. Parasitol Today 9 :303–305.
-
18
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.
-
19
Conway DJ, Roper C, Oduola AM, Arnot DE, Kremsner PG, Grobusch MP, Curtis CF, Greenwood BM, 1999. High recombination rate in natural populations of Plasmodium falciparum. Proc Natl Acad Sci U S A 96 :4506–4511.
-
20
Hastings MD, Bates SJ, Blackstone EA, Monks SM, Mutabingwa TK, Sibley CH, 2002. Highly pyrimethamine-resistant alleles of dihydrofolate reductase in isolates of Plasmodium falciparum from Tanzania. Trans R Soc Trop Med Hyg 96 :674–676.
-
21
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.
-
22
Mita T, Kaneko A, Lum JK, Bwijo B, Takechi M, Zungu IL, Tsukahara T, Tanabe K, Kobayakawa T, Bjorkman A, 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.
-
23
Alifrangis M, Lemnge MM, Ronn AM, Segeja MD, Magesa SM, Khalil IF, Bygbjerg IC, 2003. Increasing prevalence of wild-types in the dihydrofolate reductase gene of Plasmodium falciparum in an area with high levels of sulfadoxine/pyrimethamine resistance after introduction of treated bed nets. Am J Trop Med Hyg 69 :238–243.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 985 | 814 | 304 |
| Full Text Views | 270 | 7 | 1 |
| PDF Downloads | 50 | 6 | 0 |
A SIMPLE, HIGH-THROUGHPUT METHOD TO DETECT PLASMODIUM FALCIPARUM SINGLE NUCLEOTIDE POLYMORPHISMS IN THE DIHYDROFOLATE REDUCTASE, DIHYDROPTEROATE SYNTHASE, AND P. FALCIPARUM CHLOROQUINE RESISTANCE TRANSPORTER GENES USING POLYMERASE CHAIN REACTION– AND ENZYME-LINKED IMMUNOSORBENT ASSAY–BASED TECHNOLOGY
MICHAEL ALIFRANGIS
MICHAEL ALIFRANGIS
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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SONIA ENOSSE
SONIA ENOSSE
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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RICHARD PEARCE
RICHARD PEARCE
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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CHRIS DRAKELEY
CHRIS DRAKELEY
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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CALLY ROPER
CALLY ROPER
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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INSAF F. KHALIL
INSAF F. KHALIL
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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WATOKY MMM NKYA
WATOKY MMM NKYA
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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ANITA M. RØNN
ANITA M. RØNN
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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THOR G. THEANDER
THOR G. THEANDER
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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IB C. BYGBJERG
IB C. BYGBJERG
Centre for Medical Parasitology, Institute of Medical Microbiology and Immunology, and Institute of Public Health, University of Copenhagen, Copenhagen, Denmark; Department of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark; Instituto Nacional de Saúde, Ministério de Saúde, Maputo, Mozambique; Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom; Kilimanjaro Christian Medical Centre, Moshi, Tanzania; The Joint Malaria Programme, Moshi, Tanzania
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Single nucleotide polymorphisms (SNPs) in the Plasmodium falciparum dihydrofolate reductase (dhfr), and dihydropteroate synthetase (dhps), and chloroquine resistance transporter (Pfcrt) genes are used as molecular markers of P. falciparum resistance to sulfadoxine/pyrimethamine and chloroquine. However, to be a practical tool in the surveillance of drug resistance, simpler methods for high-throughput haplotyping are warranted. Here we describe a quick and simple technique that detects dhfr, dhps, and Pfcrt SNPs using polymerase chain reaction (PCR)– and enzyme-linked immunosorbent assay (ELISA)–based technology. Biotinylated PCR products of dhfr, dhps, or Pfcrt were captured on streptavidin-coated microtiter plates and sequence-specific oligonucleotide probes (SSOPs) were hybridized with the PCR products. A stringent washing procedure enabled detection of remaining bound SSOPs and distinguished between the SNPs of dhfr, dhps, and Pfcrt with high specificity. The SSOP-ELISA compared well with a standard PCR–restriction fragment length polymorphism procedure, and gave identical positive results in more than 90% of the P. falciparum slide-positive samples tested. The SSOP-ELISA of all dhfr, dhps, or Pfcrt SNPs on 88 samples can be performed in a single day and provides quick and reproducible results. The system can potentially be modified to detect SNPs in other genes.
Author Notes
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-
1
The efficacy of antimalarial monotherapies, sulphadoxine-pyrimethamine and amodiaquine in east Africa: implications for sub-regional policy, 2003. Trop Med Int Health 8: 860–867.
-
2
Kublin JG, Dzinjalamala FK, Kamwendo DD, Malkin EM, Cortese JF, Martino LM, Mukadam RA, Rogerson SJ, Lescano AG, Molyneux ME, Winstanley PA, Chimpeni P, Taylor TE, Plowe CV, 2002. Molecular markers for failure of sulfadoxine-pyrimethamine and chlorproguanil-dapsone treatment of Plasmodium falciparum malaria. J Infect Dis 185 :380–388.
-
3
Kyabayinze D, Cattamanchi A, Kamya MR, Rosenthal PJ, Dorsey G, 2003. Validation of a simplified method for using molecular markers to predict sulfadoxine-pyrimethamine treatment failure in African children with falciparum malaria. Am J Trop Med Hyg 69 :247–252.
-
4
Omar SA, Adagu IS, Warhurst DC, 2001. Can pretreatment screening for dhps and dhfr point mutations in Plasmodium falciparum infections be used to predict sulfadoxine-pyrimethamine treatment failure? Trans R Soc Trop Med Hyg 95 :315–319.
-
5
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.
-
6
Djimde A, Doumbo OK, Steketee RW, Plowe CV, 2001. Application of a molecular marker for surveillance of chloroquine-resistant falciparum malaria. Lancet 358 :890–891.
-
7
Wellems TE, Plowe CV, 2001. Chloroquine-resistant malaria. J Infect Dis 184 :770–776.
-
8
Plowe CV, 2003. Monitoring antimalarial drug resistance: making the most of the tools at hand. J Exp Biol 206 :3745–3752.
-
9
Basco LK, Ndounga M, Tejiokem M, Ngane VF, Youmba JC, Ringwald P, Soula G, 2002. Molecular epidemiology of malaria in Cameroon. XI. Geographic distribution of Plasmodium falciparum isolates with dihydrofolate reductase gene mutations in southern and central Cameroon. Am J Trop Med Hyg 67 :378–382.
-
10
Duraisingh MT, Curtis J, Warhurst DC, 1998. Plasmodium falciparum: detection of polymorphisms in the dihydrofolate reductase and dihydropteroate synthetase genes by PCR and restriction digestion. Exp Parasitol 89 :1–8.
-
11
Alifrangis M, Enosse S, Khalil IF, Tarimo DS, Lemnge MM, Thompson R, Bygbjerg IC, Ronn AM, 2003. Prediction of Plasmodium falciparum resistance to sulfadoxine/pyrimethamine in vivo by mutations in the dihydrofolate reductase and dihydropteroate synthetase genes: a comparative study between sites of differing endemicity. Am J Trop Med Hyg 69 :601–606.
-
12
Pearce RJ, Drakeley C, Chandramohan D, Mosha F, Roper C, 2003. Molecular determination of point mutation haplotypes in the dihydrofolate reductase and dihydropteroate synthase of Plasmodium falciparum in three districts of northern Tanzania. Antimicrob Agents Chemother 47 :1347–1354.
-
13
Abdel-Muhsin AM, Ranford-Cartwright LC, Medani AR, Ahmed S, Suleiman S, Khan B, Hunt P, Walliker D, Babiker HA, 2002. Detection of mutations in the Plasmodium falciparum dihydrofolate reductase (dhfr) gene by dot-blot hybridization. Am J Trop Med Hyg 67 :24–27.
-
14
Mehlotra RK, Fujioka H, Roepe PD, Janneh O, Ursos LM, Jacobs-Lorena V, McNamara DT, Bockarie MJ, Kazura JW, Kyle DE, Fidock DA, Zimmerman PA, 2001. Evolution of a unique Plasmodium falciparum chloroquine-resistance phenotype in association with pfcrt polymorphism in Papua New Guinea and South America. Proc Natl Acad Sci U S A 98 :12689–12694.
-
15
Staalsoe T, Giha HA, Dodoo D, Theander TG, Hviid L, 1999. Detection of antibodies to variant antigens on Plasmodium falciparum-infected erythrocytes by flow cytometry. Cytometry 35 :329–336.
-
16
Sambrook J, Fritsch EF, Maniatis T, 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Press.
-
17
Wooden J, Kyes S, Sibley CH, 1993. PCR and Strain Identification in Plasmodium falciparum. Parasitol Today 9 :303–305.
-
18
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.
-
19
Conway DJ, Roper C, Oduola AM, Arnot DE, Kremsner PG, Grobusch MP, Curtis CF, Greenwood BM, 1999. High recombination rate in natural populations of Plasmodium falciparum. Proc Natl Acad Sci U S A 96 :4506–4511.
-
20
Hastings MD, Bates SJ, Blackstone EA, Monks SM, Mutabingwa TK, Sibley CH, 2002. Highly pyrimethamine-resistant alleles of dihydrofolate reductase in isolates of Plasmodium falciparum from Tanzania. Trans R Soc Trop Med Hyg 96 :674–676.
-
21
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.
-
22
Mita T, Kaneko A, Lum JK, Bwijo B, Takechi M, Zungu IL, Tsukahara T, Tanabe K, Kobayakawa T, Bjorkman A, 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.
-
23
Alifrangis M, Lemnge MM, Ronn AM, Segeja MD, Magesa SM, Khalil IF, Bygbjerg IC, 2003. Increasing prevalence of wild-types in the dihydrofolate reductase gene of Plasmodium falciparum in an area with high levels of sulfadoxine/pyrimethamine resistance after introduction of treated bed nets. Am J Trop Med Hyg 69 :238–243.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 985 | 814 | 304 |
| Full Text Views | 270 | 7 | 1 |
| PDF Downloads | 50 | 6 | 0 |