Authors:
, , , , , , , , , , , , , , , , , and
- Introduction
- Materials and Methods
- Results
- Merozoite surface protein (MSP-1) 1 alleles in children and infected mosquitoes.
- Gametocyte-specifc protein gene (Pfg377) in infected people and mosquitoes.
- Dihydrofolate reductase (dhfr) haplotypes among infected children.
- Dihydrofolate reductase haplotypes in infected mosquitoes.
- Transmission of dhfr haplotypes within a single infection.
- Discussion
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Mackinnon MJ, Hastings IM, 1998. The evolution of multiple drug resistance in malaria parasites. Trans R Soc Trop Med Hyg 92: 188–195.
-
2.
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: 1590–1596.
-
3.
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: 1590–1596.
-
4.
Curtis J, Duraisingh MT, Warhurst DC, 1998. In vivo selection for a specific genotype of dihydropteroate synthetase of Plasmodium falciparum by pyrimethamine-sulfadoxine but not chlorproguanil-dapsone treatment. J Infect Dis 177: 1429–1433.
-
5.
Wargo A, Huijben S, de Roode JC, Shephard 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: 19914–19919.
-
6.
Hallett RL, Dunyo S, Ord R, Jawara M, Pinder M, Randall A, Alloueche A, Walraven G, Targett GA, Alexander N, Sutherland CJ, 2006. Chloroquine/sulphadoxine-pyrimethamine for Gambian children with malaria: transmission to mosquitoes of multidrug-resistant Plasmodium falciparum. PLoS Clin Trials 1: e15.
-
7.
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.
-
8.
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.
-
9.
Nair S, Williams JT, Brockman A, Paiphun L, Mayxay M, Newton PN, Guthmann JP, Smithuis FM, Hien TT, White NJ, Nosten F, Anderson T, 2003. A selective sweep driven by pyrimethamine treatment in southeast Asian malaria parasites. Mol Biol Evol 20: 1526–1536.
-
10.
Roper C, Pearce R, Bredenkamp B, Gumede J, Drakeley C, Mosha F, Chandramohan D, Sharp B, 2003. Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet 361: 1174–1181.
-
11.
McCollum AM, Poe AC, Hamel M, Huber C, Zhou Z, Shi YP, Ouma P, Vulule J, Bloland P, Slutsker L, Barnwell JW, Udhayakumar V, Escalante AA, 2006. Antifolate resistance in Plasmodium falciparum: multiple origins and identification of novel dhfr alleles. J Infect Dis 194: 189–197.
-
12.
McCollum AM, Basco LK, Tahar R, Udhayakumar V, Escalante AA, 2008. Hitchhiking and selective sweeps of Plasmodium falciparum sulfadoxine and pyrimethamine resistance alleles in a population from central Africa. Antimicrob Agents Chemother 52: 4089–4097.
-
13.
Maïga O, Djimdé AA, Hubert V, Renard E, Aubouy A, Kironde F, Nsimba B, Koram K, Doumbo OK, Le Bras J, Clain JA, 2007. A shared Asian origin of the triple-mutant dhfr allele in Plasmodium falciparum from sites across Africa. J Infect Dis 196: 165–172.
-
14.
Ndiaye D, Daily JP, Sarr O, Ndir O, Gaye O, Mboup S, Roper C, Wirth DF, 2006. Defining the origin of Plasmodium falciparum resistant dhfr isolates in Senegal. Acta Trop 99: 106–111.
-
15.
Certain LK, Briceño ML, Kiara SM, Nzila AM, Watkins WM, Sibley CH, 2008. Characteristics of Plasmodium falciparum dhfr haplotypes that confer pyrimethamine resistance Kilifi, Kenya, 1987–2006. J Infect Dis 197: 1743–1751.
-
16.
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 post-treatment transmission of Plasmodium falciparum to Anopheles gambiae. J Infect Dis 183: 1254–1259.
-
17.
Sutherland CJ, Ord R, Dunyo S, Jawara M, Drakeley CJ, Alexander N, Coleman R, Pinder M, Walraven G, Targett GA, 2005. Reduction of malaria transmission to Anopheles mosquitoes with a six-dose regimen of coartemether. PLoS Med 2: e92.
-
18.
Greenwood BM, Pickering H, 1993. A malaria control trial using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of The Gambia, West Africa. 1. A review of the epidemiology and control of malaria in The Gambia, West Africa. Trans R Soc Trop Med Hyg 87: (Suppl 2): 3–11.
-
19.
Lindsay SW, Wilkins HA, Zieler HA, Daly RJ, Petraca V, Pyass P, 1991. Ability of the Anopheles gambiae complex to transmit malaria during the dry and wet season in an area of irrigated rice cultivation in The Gambia. Am J Trop Med Hyg 94: 313–324.
-
20.
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: 219–227.
-
21.
Ranford-Cartwright L, Balfe P, Carter R, Walliker D, 1991. Genetic hybrids of Plasmodium falciparum identified by amplification of genomic DNA from single oocysts. Mol Biochem Parasitol 49: 239–243.
-
22.
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: 565–568.
-
23.
Abdel-Muhsin A, Mackinnon M, 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: 391–400.
-
24.
Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP, 2000. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol 17: 1467–1482.
-
25.
Zwetyenga J, Rogier C, Tall A, Fontenille D, Snounou G, Trape J, Mercereau-Puijalon O, 1998. No influence of age on infection complexity and allelic distribution in Plasmodium falciparum infections in Ndiop, a Senegalese village with seasonal, mesoendemic malaria. Am J Trop Med Hyg 59: 726–735.
-
26.
Roper C, Pearce R, Nair S, Sharp B, Nosten F, Anderson TJ, 2004. Intercontinental spread of pyrimethamine resistant malaria. Science 305: 1124.
-
27.
Al-Saai S, Kheir A, Abdel-Muhsin A, Al-Ghazali A, Nwakanma D, Swedberg G, Babiker HA, 2009. Distinct haplotypes of dhfr and dhps among Plasmodium falciparum isolates in an area of high level of sulfadoxine-pyrimethamine (SP) resistance in eastern Sudan. Infect Genet Evol 9: 778–783.
-
28.
Menge DM, Zhong D, Guda T, Gouagna L, Githure J, Beier J, Yan G, 2006. Quantitative trait loci controlling refractoriness to Plasmodium falciparum in natural Anopheles gambiae mosquitoes from a malaria-endemic region in western Kenya. Genetics 173: 235–241.
-
29.
Burkot TR, Williams JL, Schneider I, 1984. Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Trans R Soc Trop Med Hyg 78: 339–341.
-
30.
Graves PM, Carter R, McNeill KM, 1984. Gametocyte production in cloned lines of Plasmodium falciparum. Am J Trop Med Hyg 33: 1045–1050.
-
31.
Nassir E, Abdel-Muhsin AA, 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: 49–55.
-
32.
Hill GW, Babiker HA, 1995. Estimation of numbers of malaria clones in blood samples. Proc R Soc Lond B Biol Sci 262: 249–257.
-
33.
Babiker HA, Ranford-Cartwright L, Currie D, Charlwood D, Billingsley P, Teuscher T, Walliker D, 1994. Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology 109: 413–421.
-
34.
Paul RE, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, Paru R, Day KP, 1995. Mating patterns in malaria parasite populations of Papua New Guinea. Science 269: 1709–1711.
-
35.
Babiker HA, Lines J, Hill WG, Walliker D, 1997. Population structure of Plasmodium falciparum in villages with different malaria endemicity in east Africa. Am J Trop Med Hyg 56: 141–147.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 721 | 671 | 327 |
| Full Text Views | 202 | 13 | 4 |
| PDF Downloads | 70 | 14 | 2 |
Transmission and Cross-Mating of High-Level Resistance Plasmodium falciparum Dihydrofolate Reductase Haplotypes in The Gambia
Amani Kheir
Amani Kheir
Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden; Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alk-Khjod, Oman; Medical Research Council, Laboratories, Banjul, The Gambia; School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Davis Nwakanma
Davis Nwakanma
Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden; Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alk-Khjod, Oman; Medical Research Council, Laboratories, Banjul, The Gambia; School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Aisha Al-Gazali
Aisha Al-Gazali
Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden; Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alk-Khjod, Oman; Medical Research Council, Laboratories, Banjul, The Gambia; School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Yagut Akbarova
Yagut Akbarova
Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden; Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alk-Khjod, Oman; Medical Research Council, Laboratories, Banjul, The Gambia; School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Salma Al-Saai
Salma Al-Saai
Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden; Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alk-Khjod, Oman; Medical Research Council, Laboratories, Banjul, The Gambia; School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Göte Swedberg
Göte Swedberg
Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden; Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alk-Khjod, Oman; Medical Research Council, Laboratories, Banjul, The Gambia; School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
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Hamza A. Babiker
Hamza A. Babiker
Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden; Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alk-Khjod, Oman; Medical Research Council, Laboratories, Banjul, The Gambia; School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
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A high-level pyrimethamine resistance Plasmodium falciparum lineage with triple dihydrofolate reductase (dhfr) mutations prevails across Africa. However, additional minority lineages were seen. We examined transmission success of mutant dhfr haplotypes among 22 children in The Gambia and 60 infected Anopheles gambiae mosquitoes fed on their blood. Additional polymorphic genes of the gametocyte-specific protein (pfg377) and merozoite surface protein-1 (MSP-1) were examined. Similarities were seen between pfg377 and MSP-1 alleles in children and mosquitoes and evidence of cross-mating between different parasite genotypes was seen in some infected mosquitoes, reflecting high transmission success of existing clones. With regard to dhfr, 16 haplotypes were seen among the children: 2 carried double mutations and 14 carried triple mutations. However, only nine haplotypes, all with triple mutations, were detected among mosquitoes. A single triple-mutant dhfr haplotype, similar to that in other countries in Africa, predominated among children (42%) and mosquitoes (60%), supporting the hypothesis of migration of this haplotype across Africa. However, evidence of cross-mating between the above haplotypes signifies the role of local evolution.
Author Notes
Financial support: This work was supported by the Medical Research Council, United Kingdom; the Swedish International Development Cooperation Agency; and Sultan Qaboos University, Oman.
Authors' addresses: Amani Kheir and Göte Swedberg, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsalal, Sweden. Davis Nwakanma, Medical Research Council Laboratories, Banjul, The Gambia. Yagut Akbarova, Salma Al-Saai, and Aisha Al-Gazali, Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alk-Khjod, Oman. Hamza A. Babiker, Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alk-Khjod, Oman and School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JR, United Kingdom.
- Introduction
- Materials and Methods
- Results
- Merozoite surface protein (MSP-1) 1 alleles in children and infected mosquitoes.
- Gametocyte-specifc protein gene (Pfg377) in infected people and mosquitoes.
- Dihydrofolate reductase (dhfr) haplotypes among infected children.
- Dihydrofolate reductase haplotypes in infected mosquitoes.
- Transmission of dhfr haplotypes within a single infection.
- Discussion
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Mackinnon MJ, Hastings IM, 1998. The evolution of multiple drug resistance in malaria parasites. Trans R Soc Trop Med Hyg 92: 188–195.
-
2.
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: 1590–1596.
-
3.
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: 1590–1596.
-
4.
Curtis J, Duraisingh MT, Warhurst DC, 1998. In vivo selection for a specific genotype of dihydropteroate synthetase of Plasmodium falciparum by pyrimethamine-sulfadoxine but not chlorproguanil-dapsone treatment. J Infect Dis 177: 1429–1433.
-
5.
Wargo A, Huijben S, de Roode JC, Shephard 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: 19914–19919.
-
6.
Hallett RL, Dunyo S, Ord R, Jawara M, Pinder M, Randall A, Alloueche A, Walraven G, Targett GA, Alexander N, Sutherland CJ, 2006. Chloroquine/sulphadoxine-pyrimethamine for Gambian children with malaria: transmission to mosquitoes of multidrug-resistant Plasmodium falciparum. PLoS Clin Trials 1: e15.
-
7.
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.
-
8.
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.
-
9.
Nair S, Williams JT, Brockman A, Paiphun L, Mayxay M, Newton PN, Guthmann JP, Smithuis FM, Hien TT, White NJ, Nosten F, Anderson T, 2003. A selective sweep driven by pyrimethamine treatment in southeast Asian malaria parasites. Mol Biol Evol 20: 1526–1536.
-
10.
Roper C, Pearce R, Bredenkamp B, Gumede J, Drakeley C, Mosha F, Chandramohan D, Sharp B, 2003. Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet 361: 1174–1181.
-
11.
McCollum AM, Poe AC, Hamel M, Huber C, Zhou Z, Shi YP, Ouma P, Vulule J, Bloland P, Slutsker L, Barnwell JW, Udhayakumar V, Escalante AA, 2006. Antifolate resistance in Plasmodium falciparum: multiple origins and identification of novel dhfr alleles. J Infect Dis 194: 189–197.
-
12.
McCollum AM, Basco LK, Tahar R, Udhayakumar V, Escalante AA, 2008. Hitchhiking and selective sweeps of Plasmodium falciparum sulfadoxine and pyrimethamine resistance alleles in a population from central Africa. Antimicrob Agents Chemother 52: 4089–4097.
-
13.
Maïga O, Djimdé AA, Hubert V, Renard E, Aubouy A, Kironde F, Nsimba B, Koram K, Doumbo OK, Le Bras J, Clain JA, 2007. A shared Asian origin of the triple-mutant dhfr allele in Plasmodium falciparum from sites across Africa. J Infect Dis 196: 165–172.
-
14.
Ndiaye D, Daily JP, Sarr O, Ndir O, Gaye O, Mboup S, Roper C, Wirth DF, 2006. Defining the origin of Plasmodium falciparum resistant dhfr isolates in Senegal. Acta Trop 99: 106–111.
-
15.
Certain LK, Briceño ML, Kiara SM, Nzila AM, Watkins WM, Sibley CH, 2008. Characteristics of Plasmodium falciparum dhfr haplotypes that confer pyrimethamine resistance Kilifi, Kenya, 1987–2006. J Infect Dis 197: 1743–1751.
-
16.
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 post-treatment transmission of Plasmodium falciparum to Anopheles gambiae. J Infect Dis 183: 1254–1259.
-
17.
Sutherland CJ, Ord R, Dunyo S, Jawara M, Drakeley CJ, Alexander N, Coleman R, Pinder M, Walraven G, Targett GA, 2005. Reduction of malaria transmission to Anopheles mosquitoes with a six-dose regimen of coartemether. PLoS Med 2: e92.
-
18.
Greenwood BM, Pickering H, 1993. A malaria control trial using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of The Gambia, West Africa. 1. A review of the epidemiology and control of malaria in The Gambia, West Africa. Trans R Soc Trop Med Hyg 87: (Suppl 2): 3–11.
-
19.
Lindsay SW, Wilkins HA, Zieler HA, Daly RJ, Petraca V, Pyass P, 1991. Ability of the Anopheles gambiae complex to transmit malaria during the dry and wet season in an area of irrigated rice cultivation in The Gambia. Am J Trop Med Hyg 94: 313–324.
-
20.
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: 219–227.
-
21.
Ranford-Cartwright L, Balfe P, Carter R, Walliker D, 1991. Genetic hybrids of Plasmodium falciparum identified by amplification of genomic DNA from single oocysts. Mol Biochem Parasitol 49: 239–243.
-
22.
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: 565–568.
-
23.
Abdel-Muhsin A, Mackinnon M, 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: 391–400.
-
24.
Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP, 2000. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol 17: 1467–1482.
-
25.
Zwetyenga J, Rogier C, Tall A, Fontenille D, Snounou G, Trape J, Mercereau-Puijalon O, 1998. No influence of age on infection complexity and allelic distribution in Plasmodium falciparum infections in Ndiop, a Senegalese village with seasonal, mesoendemic malaria. Am J Trop Med Hyg 59: 726–735.
-
26.
Roper C, Pearce R, Nair S, Sharp B, Nosten F, Anderson TJ, 2004. Intercontinental spread of pyrimethamine resistant malaria. Science 305: 1124.
-
27.
Al-Saai S, Kheir A, Abdel-Muhsin A, Al-Ghazali A, Nwakanma D, Swedberg G, Babiker HA, 2009. Distinct haplotypes of dhfr and dhps among Plasmodium falciparum isolates in an area of high level of sulfadoxine-pyrimethamine (SP) resistance in eastern Sudan. Infect Genet Evol 9: 778–783.
-
28.
Menge DM, Zhong D, Guda T, Gouagna L, Githure J, Beier J, Yan G, 2006. Quantitative trait loci controlling refractoriness to Plasmodium falciparum in natural Anopheles gambiae mosquitoes from a malaria-endemic region in western Kenya. Genetics 173: 235–241.
-
29.
Burkot TR, Williams JL, Schneider I, 1984. Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Trans R Soc Trop Med Hyg 78: 339–341.
-
30.
Graves PM, Carter R, McNeill KM, 1984. Gametocyte production in cloned lines of Plasmodium falciparum. Am J Trop Med Hyg 33: 1045–1050.
-
31.
Nassir E, Abdel-Muhsin AA, 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: 49–55.
-
32.
Hill GW, Babiker HA, 1995. Estimation of numbers of malaria clones in blood samples. Proc R Soc Lond B Biol Sci 262: 249–257.
-
33.
Babiker HA, Ranford-Cartwright L, Currie D, Charlwood D, Billingsley P, Teuscher T, Walliker D, 1994. Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology 109: 413–421.
-
34.
Paul RE, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, Paru R, Day KP, 1995. Mating patterns in malaria parasite populations of Papua New Guinea. Science 269: 1709–1711.
-
35.
Babiker HA, Lines J, Hill WG, Walliker D, 1997. Population structure of Plasmodium falciparum in villages with different malaria endemicity in east Africa. Am J Trop Med Hyg 56: 141–147.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 721 | 671 | 327 |
| Full Text Views | 202 | 13 | 4 |
| PDF Downloads | 70 | 14 | 2 |