Author:
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- DISCUSSION
- Malaria transmission intensity, drug elimination half-life, and spread of resistance.
- Malaria transmission intensity and community drug use.
- Malaria transmission intensity and average number of parasite clones.
- Transmission intensity and intrahost competition.
- Transmission intensity, drug resistance, and its genetic basis.
- Malaria transmission intensity and parasite biomass.
- Malaria transmission intensity and impact of drug therapy on gametocyte carriage.
- Shedding some light on theoretical models.
- Some caveats.
- Conclusions, implications for malaria control, and future research.
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1
White NJ, Pongtavornpinyo W, 2003. The de novo selection of drug resistant malaria parasites. Proc R Soc Lond B Biol Sci 270 :545–554.
-
2
Hastings IM, Watkins WM, White NJ, 2002. The evolution of drug-resistant malaria: the role of drug elimination half-life. Philos Trans R Soc Lond B Biol Sci 357 :505–519.
-
3
Wernsdorfer WH, 1994. Epidemiology of drug resistance in malaria. Acta Trop 56 :143–156.
-
4
Paul REL, Packer MJ, Walmsley M, Lagog M, Randford-Cartwright LC, Paru R, Day KP, 1995. Mating patterns in malaria parasite populations of Papua New Guinea. Science 269 :1709–1711.
-
5
Cross AP, Singer B, 1991. Modelling the development of resistance of Plasmodium falciparum to anti-malarial drugs. Trans R Soc Trop Med Hyg 85 :349–355.
-
6
Curtis CF, Otoo LN, 1986. A simple model of the build-up of resistance to mixtures of anti-malarial drugs. Trans R Soc Trop Med Hyg 80 :889–892.
-
7
Hastings IM, 1997. A model for the origins and spread of drug-resistant malaria. Parasitology 115 :133–141.
-
8
Hastings IM, Mackinnon MJ, 1998. The emergence of drug-resistant malaria. Parasitology 117 :411–417.
-
9
Hastings IM, D’Alessandro U, 2000. Modelling a predictable disaster: the rise and spread of drug-resistant malaria. Parasitol Today 16 :340–347.
-
10
Hastings IM, 2001. Modelling parasite drug resistance: lessons for management and control strategies. Trop Med Int Health 6 :883–890.
-
11
Molyneux DH, Floyd K, Barnish G, Fevre EM, 1999. Transmission control and drug resistance in malaria: a crucial interaction. Parasitol Today 15 :238–240.
-
12
Greenwood B, 2002. The molecular epidemiology of malaria. Trop Med Int Health 7 :1012–1021.
-
13
White N, 1999. Antimalarial drug resistance and combination chemotherapy. Philos Trans R Soc Lond B Biol Sci 354 :739–749.
-
14
White NJ, 1999. Delaying antimalarial drug resistance with combination chemotherapy. Parassitologia 41 :301–308.
-
15
Mackinnon MJ, Hastings IM, 1998. The evolution of multiple drug resistance in malaria parasites. Trans R Soc Trop Med Hyg 92 :188–195.
-
16
Prudhomme-O’Meara W, Smith DL, McKenzie FE, 2006. Potential impact of intermittent preventive treatment (IPT) on spread of drug-resistant malaria. PLoS Med. 3 :e141.
-
17
Hastings IM, Watkins WM, 2005. Intensity of malaria transmission and the evolution of drug resistance. Acta Trop 94 :218–229.
-
18
Arnot D, 1998. Unstable malaria in Sudan: the influence of the dry season. Clone multiplicity of Plasmodium falciparum infections in individuals exposed to variable levels of disease transmission. Trans R Soc Trop Med Hyg 92 :580–585.
-
19
Farnert A, Rooth I, Svensson A, Snounou G, Bjorkman A, 1999. Complexity of Plasmodium falciparum infections is consistent over time and protects against clinical disease in Tanzanian children. J Infect Dis 179 :989–995.
-
20
Paganotti GM, Babiker HA, Modiano D, Sirima BS, Verra F, Konate A, Ouedraogo AL, Diarra A, Mackinnon MJ, Coluzzi M, Walliker D, 2004. Genetic complexity of Plasmodium falciparum in two ethnic groups of Burkina Faso with marked differences in susceptibility to malaria. Am J Trop Med Hyg 71 :173–178.
-
21
Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SL, Carneiro I, Malima R, Lusingu J, Manjurano A, Nkya WM, Lemnge MM, Cox J, Reyburn H, Riley EM, 2005. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA 102 :5108–5113.
-
22
Smith T, Charlwood JD, Kitua AY, Masanja H, Mwankusye S, Alonso PL, Tanner M, 1998. Relationships of malaria morbidity with exposure to Plasmodium falciparum in young children in a highly endemic area. Am J Trop Med Hyg 59 :252–257.
-
23
Talisuna OA, Langi P, Bakyaita N, Egwang T, Mutabingwa TK, Watkins W, Van Marck E, D’Alessandro U, 2002. Intensity of malaria transmission, antimalarial drug use and resistance in Uganda: what is the relationship between these three factors? Trans R Soc Trop Med Hyg 96 :310–317.
-
24
Rogier C, Diagne N, Fontenille D, Spiegel A, Trape JF, 1999. Plasmodium falciparum clinical malaria: lessons from longitudinal studies in Senegal. Parasitologia 41 :255–259.
-
25
Trape JF, Rogier C, 1996. Combating malaria morbidity and mortality by reducing transmission. Parasitol Today 12 :236–240.
-
26
World Health Organization, 1965. Resistance of Malaria Parasites to Drugs. Geneva: World Health Organization.
-
27
Francis D, Nsobya SL, Talisuna A, Yeka A, Kamya MR, Machekano R, Dokomajilar C, Rosenthal PJ, Dorsey G, 2006. Geographic differences in antimalarial drug efficacy in Uganda are explained by differences in endemicity and not by known molecular markers of drug resistance. J Infect Dis 193 :978–986.
-
28
Talisuna AO, Langi P, Mutabingwa TK, Van Marck E, Speybroeck N, Egwang TG, Watkins WM, Hastings IM, D’Alessandro U, 2003. Intensity of transmission and spread of gene mutations linked to chloroquine and sulphadoxine-pyrimethamine resistance in falciparum malaria. Int J Parasitol 33 :1051–1058.
-
29
Lee SA, Yeka A, Nsobya SL, Dokomajilar C, Rosenthal PJ, Talisuna A, Dorsey G, 2006. Complexity of Plasmodium falciparum infections and antimalarial drug efficacy at 7 sites in Uganda. J Infect Dis 193 :1160–1163.
-
30
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.
-
31
Mharakurwa S, Mutambu SL, Mudyiradima R, Chimbadzwa T, Chandiwana SK, Day KP, 2004. Association of house spraying with suppressed levels of drug resistance in Zimbabwe. Malar J 3 :35.
-
32
Diallo D, Sutherland C, Nebié I, Konaté A, Ord R, Pota H, Roper C, Ilboudo-Sanogo C, Greenwood B, Cousens S, 2007. Sustained use of insecticide treated curtains is not associated with greater circulation of drug resistant malaria parasites nor with higher risk of treatment failure among children with uncomplicated malaria in Burkina Faso. Am J Trop Med Hyg 76 :237–244.
-
33
Reyburn H, Ruanda J, Mwerinde O, Drakeley C, 2006. The contribution of microscopy to targeting antimalarial treatment in a low transmission area of Tanzania. Malar J 5 :4.
-
34
Watkins WM, Mosobo M, 1993. Treatment of Plasmodium falciparum malaria with pyrimethamine-sulfadoxine: selective pressure for resistance is a function of long elimination half-life. Trans R Soc Trop Med Hyg 87 :75–78.
-
35
Babiker A, Walliker D, 1997. Current views on the population structure of Plasmodium falciparum: implications for control. Parasitol Today 13 :262–267.
-
36
Walliker D, Quakyi IC, Wellems TE, McCutchan TF, Szarfman A, 1987. London WT, Corcoran LM, Burkot TR, Carter R. Genetic Analysis of the Human Malaria Parasite Plasmodium falciparum. Science 236 :1661–1666.
-
37
Schmidt KF, 1995. Inbred parssites may spur resistance. Science 269 :1670.
-
38
Slater M, Kiggundu M, Dokomajilar C, Kamya MR, Bakyaita N, Talisuna A, Rosenthal PJ, Dorsey G, 2005. Distinguishing recrudescences from new infections in antimalarial clinical trials: major impact of interpretation of genotyping results on estimates of drug efficacy. Am J Trop Med Hyg 73 :256–262.
-
39
Foote SJ, Kyle DE, Martin RK, Oduola AM, Forsyth K, Kemp DJ, Cowman AF, 1990. Several alleles of the multidrug-resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. Nature 345 :255–258.
-
40
Wellems TE, Panton LJ, Gluzman IY, Do RV, Gwadz RW, Walker-Jonah A, Krogstad DJ, 1990. Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature 345 :253–255.
-
41
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.
-
42
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.
-
43
Sidhu AB, Verdier-Pinard D, Fidock DA, 2002. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298 :210–213.
-
44
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.
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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 :582–588.
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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 :320–323.
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Targett G, Drakeley C, Jawara M, von Seidlein L, Coleman R, Deen J, Pinder M, Doherty T, Sutherland C, Walraven G, Milligan P, 2001. Artesunate reduces but does not prevent posttreatment transmission of Plasmodium falciparum to Anopheles gambiae. J Infect Dis 83 :1254–1259.
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Intensity of Malaria Transmission and the Spread of Plasmodium falciparum–Resistant Malaria: A Review of Epidemiologic Field Evidence
Ambrose O. Talisuna
Ambrose O. Talisuna
Uganda Ministry of Health, Epidemiological Surveillance Division; East African Network for Monitoring Antimalarial Treatment, Kampala, Uganda; Department of Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp, Belgium
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Paul E. Okello
Paul E. Okello
Uganda Ministry of Health, Epidemiological Surveillance Division; East African Network for Monitoring Antimalarial Treatment, Kampala, Uganda; Department of Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp, Belgium
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Annette Erhart
Annette Erhart
Uganda Ministry of Health, Epidemiological Surveillance Division; East African Network for Monitoring Antimalarial Treatment, Kampala, Uganda; Department of Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp, Belgium
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Marc Coosemans
Marc Coosemans
Uganda Ministry of Health, Epidemiological Surveillance Division; East African Network for Monitoring Antimalarial Treatment, Kampala, Uganda; Department of Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp, Belgium
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Umberto D’Alessandro
Umberto D’Alessandro
Uganda Ministry of Health, Epidemiological Surveillance Division; East African Network for Monitoring Antimalarial Treatment, Kampala, Uganda; Department of Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp, Belgium
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Malaria transmission intensity has been proposed, based on theoretical models, as an important factor for the spread of falciparum-resistant malaria, but the predictions obtained vary according to the assumptions inherent in the model used. We summarized the available field data on transmission intensity and the prevalence of malaria drug resistance. Resistance to chloroquine and sulphadoxine-pyrimethamine monotherapy was invariably higher where transmission was intense. Vector control interventions were associated with a better chloroquine and sulfadoxine-pyrimethamine efficacy. However, high resistance to chloroquine and also to combination therapy (chloroquine plus sulphadoxine-pyrimethamine and amodiaquine plus sulfadoxine-pyrimethamine) was also observed in very low transmission areas. Reducing transmission intensity is likely to slow the spread of drug resistance. Nevertheless, where transmission is extremely low, to limit the unnecessary use of antimalarials and a consequent paradoxical acceleration of the spread of resistance, patients should be treated only after laboratory confirmation of malaria.
Author Notes
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- DISCUSSION
- Malaria transmission intensity, drug elimination half-life, and spread of resistance.
- Malaria transmission intensity and community drug use.
- Malaria transmission intensity and average number of parasite clones.
- Transmission intensity and intrahost competition.
- Transmission intensity, drug resistance, and its genetic basis.
- Malaria transmission intensity and parasite biomass.
- Malaria transmission intensity and impact of drug therapy on gametocyte carriage.
- Shedding some light on theoretical models.
- Some caveats.
- Conclusions, implications for malaria control, and future research.
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1
White NJ, Pongtavornpinyo W, 2003. The de novo selection of drug resistant malaria parasites. Proc R Soc Lond B Biol Sci 270 :545–554.
-
2
Hastings IM, Watkins WM, White NJ, 2002. The evolution of drug-resistant malaria: the role of drug elimination half-life. Philos Trans R Soc Lond B Biol Sci 357 :505–519.
-
3
Wernsdorfer WH, 1994. Epidemiology of drug resistance in malaria. Acta Trop 56 :143–156.
-
4
Paul REL, Packer MJ, Walmsley M, Lagog M, Randford-Cartwright LC, Paru R, Day KP, 1995. Mating patterns in malaria parasite populations of Papua New Guinea. Science 269 :1709–1711.
-
5
Cross AP, Singer B, 1991. Modelling the development of resistance of Plasmodium falciparum to anti-malarial drugs. Trans R Soc Trop Med Hyg 85 :349–355.
-
6
Curtis CF, Otoo LN, 1986. A simple model of the build-up of resistance to mixtures of anti-malarial drugs. Trans R Soc Trop Med Hyg 80 :889–892.
-
7
Hastings IM, 1997. A model for the origins and spread of drug-resistant malaria. Parasitology 115 :133–141.
-
8
Hastings IM, Mackinnon MJ, 1998. The emergence of drug-resistant malaria. Parasitology 117 :411–417.
-
9
Hastings IM, D’Alessandro U, 2000. Modelling a predictable disaster: the rise and spread of drug-resistant malaria. Parasitol Today 16 :340–347.
-
10
Hastings IM, 2001. Modelling parasite drug resistance: lessons for management and control strategies. Trop Med Int Health 6 :883–890.
-
11
Molyneux DH, Floyd K, Barnish G, Fevre EM, 1999. Transmission control and drug resistance in malaria: a crucial interaction. Parasitol Today 15 :238–240.
-
12
Greenwood B, 2002. The molecular epidemiology of malaria. Trop Med Int Health 7 :1012–1021.
-
13
White N, 1999. Antimalarial drug resistance and combination chemotherapy. Philos Trans R Soc Lond B Biol Sci 354 :739–749.
-
14
White NJ, 1999. Delaying antimalarial drug resistance with combination chemotherapy. Parassitologia 41 :301–308.
-
15
Mackinnon MJ, Hastings IM, 1998. The evolution of multiple drug resistance in malaria parasites. Trans R Soc Trop Med Hyg 92 :188–195.
-
16
Prudhomme-O’Meara W, Smith DL, McKenzie FE, 2006. Potential impact of intermittent preventive treatment (IPT) on spread of drug-resistant malaria. PLoS Med. 3 :e141.
-
17
Hastings IM, Watkins WM, 2005. Intensity of malaria transmission and the evolution of drug resistance. Acta Trop 94 :218–229.
-
18
Arnot D, 1998. Unstable malaria in Sudan: the influence of the dry season. Clone multiplicity of Plasmodium falciparum infections in individuals exposed to variable levels of disease transmission. Trans R Soc Trop Med Hyg 92 :580–585.
-
19
Farnert A, Rooth I, Svensson A, Snounou G, Bjorkman A, 1999. Complexity of Plasmodium falciparum infections is consistent over time and protects against clinical disease in Tanzanian children. J Infect Dis 179 :989–995.
-
20
Paganotti GM, Babiker HA, Modiano D, Sirima BS, Verra F, Konate A, Ouedraogo AL, Diarra A, Mackinnon MJ, Coluzzi M, Walliker D, 2004. Genetic complexity of Plasmodium falciparum in two ethnic groups of Burkina Faso with marked differences in susceptibility to malaria. Am J Trop Med Hyg 71 :173–178.
-
21
Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SL, Carneiro I, Malima R, Lusingu J, Manjurano A, Nkya WM, Lemnge MM, Cox J, Reyburn H, Riley EM, 2005. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA 102 :5108–5113.
-
22
Smith T, Charlwood JD, Kitua AY, Masanja H, Mwankusye S, Alonso PL, Tanner M, 1998. Relationships of malaria morbidity with exposure to Plasmodium falciparum in young children in a highly endemic area. Am J Trop Med Hyg 59 :252–257.
-
23
Talisuna OA, Langi P, Bakyaita N, Egwang T, Mutabingwa TK, Watkins W, Van Marck E, D’Alessandro U, 2002. Intensity of malaria transmission, antimalarial drug use and resistance in Uganda: what is the relationship between these three factors? Trans R Soc Trop Med Hyg 96 :310–317.
-
24
Rogier C, Diagne N, Fontenille D, Spiegel A, Trape JF, 1999. Plasmodium falciparum clinical malaria: lessons from longitudinal studies in Senegal. Parasitologia 41 :255–259.
-
25
Trape JF, Rogier C, 1996. Combating malaria morbidity and mortality by reducing transmission. Parasitol Today 12 :236–240.
-
26
World Health Organization, 1965. Resistance of Malaria Parasites to Drugs. Geneva: World Health Organization.
-
27
Francis D, Nsobya SL, Talisuna A, Yeka A, Kamya MR, Machekano R, Dokomajilar C, Rosenthal PJ, Dorsey G, 2006. Geographic differences in antimalarial drug efficacy in Uganda are explained by differences in endemicity and not by known molecular markers of drug resistance. J Infect Dis 193 :978–986.
-
28
Talisuna AO, Langi P, Mutabingwa TK, Van Marck E, Speybroeck N, Egwang TG, Watkins WM, Hastings IM, D’Alessandro U, 2003. Intensity of transmission and spread of gene mutations linked to chloroquine and sulphadoxine-pyrimethamine resistance in falciparum malaria. Int J Parasitol 33 :1051–1058.
-
29
Lee SA, Yeka A, Nsobya SL, Dokomajilar C, Rosenthal PJ, Talisuna A, Dorsey G, 2006. Complexity of Plasmodium falciparum infections and antimalarial drug efficacy at 7 sites in Uganda. J Infect Dis 193 :1160–1163.
-
30
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.
-
31
Mharakurwa S, Mutambu SL, Mudyiradima R, Chimbadzwa T, Chandiwana SK, Day KP, 2004. Association of house spraying with suppressed levels of drug resistance in Zimbabwe. Malar J 3 :35.
-
32
Diallo D, Sutherland C, Nebié I, Konaté A, Ord R, Pota H, Roper C, Ilboudo-Sanogo C, Greenwood B, Cousens S, 2007. Sustained use of insecticide treated curtains is not associated with greater circulation of drug resistant malaria parasites nor with higher risk of treatment failure among children with uncomplicated malaria in Burkina Faso. Am J Trop Med Hyg 76 :237–244.
-
33
Reyburn H, Ruanda J, Mwerinde O, Drakeley C, 2006. The contribution of microscopy to targeting antimalarial treatment in a low transmission area of Tanzania. Malar J 5 :4.
-
34
Watkins WM, Mosobo M, 1993. Treatment of Plasmodium falciparum malaria with pyrimethamine-sulfadoxine: selective pressure for resistance is a function of long elimination half-life. Trans R Soc Trop Med Hyg 87 :75–78.
-
35
Babiker A, Walliker D, 1997. Current views on the population structure of Plasmodium falciparum: implications for control. Parasitol Today 13 :262–267.
-
36
Walliker D, Quakyi IC, Wellems TE, McCutchan TF, Szarfman A, 1987. London WT, Corcoran LM, Burkot TR, Carter R. Genetic Analysis of the Human Malaria Parasite Plasmodium falciparum. Science 236 :1661–1666.
-
37
Schmidt KF, 1995. Inbred parssites may spur resistance. Science 269 :1670.
-
38
Slater M, Kiggundu M, Dokomajilar C, Kamya MR, Bakyaita N, Talisuna A, Rosenthal PJ, Dorsey G, 2005. Distinguishing recrudescences from new infections in antimalarial clinical trials: major impact of interpretation of genotyping results on estimates of drug efficacy. Am J Trop Med Hyg 73 :256–262.
-
39
Foote SJ, Kyle DE, Martin RK, Oduola AM, Forsyth K, Kemp DJ, Cowman AF, 1990. Several alleles of the multidrug-resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. Nature 345 :255–258.
-
40
Wellems TE, Panton LJ, Gluzman IY, Do RV, Gwadz RW, Walker-Jonah A, Krogstad DJ, 1990. Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature 345 :253–255.
-
41
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.
-
42
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.
-
43
Sidhu AB, Verdier-Pinard D, Fidock DA, 2002. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298 :210–213.
-
44
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.
-
45
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