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Published in: Malaria Journal 1/2012

Open Access 01-12-2012 | Research

Local population structure of Plasmodium: impact on malaria control and elimination

Authors: Stella M Chenet, Kristan A Schneider, Leopoldo Villegas, Ananias A Escalante

Published in: Malaria Journal | Issue 1/2012

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Abstract

Background

Regardless of the growing interest in detecting population structures in malarial parasites, there have been limited discussions on how to use this concept in control programmes. In such context, the effects of the parasite population structures will depend on interventions’ spatial or temporal scales. This investigation explores the problem of identifying genetic markers, in this case microsatellites, to unveil Plasmodium genetic structures that could affect decisions in the context of elimination. The study was performed in a low-transmission area, which offers a good proxy to better understand problems associated with surveillance at the final stages of malaria elimination.

Methods

Plasmodium vivax samples collected in Tumeremo, Venezuela, between March 2003 and November 2004 were analysed. Since Plasmodium falciparum also circulates in many low endemic areas, P. falciparum samples from the same locality and time period were included for comparison. Plasmodium vivax samples were assayed for an original set of 25 microsatellites and P. falciparum samples were assayed for 12 microsatellites.

Results

Not all microsatellite loci assayed offered reliable local data. A complex temporal-cluster dynamics is found in both P. vivax and P. falciparum. Such dynamics affect the numbers and the type of microsatellites required for identifying individual parasites or parasite clusters when performing cross-sectional studies. The minimum number of microsatellites required to differentiate circulating P. vivax clusters differs from the minimum number of hyper-variable microsatellites required to distinguish individuals within these clusters. Regardless the extended number of microsatellites used in P. vivax, it was not possible to separate all individual infections.

Conclusions

Molecular surveillance has great potential; however, it requires preliminary local studies in order to properly interpret the emerging patterns in the context of elimination. Clonal expansions and clusters turnovers need to be taken into account when using molecular markers. Those affect the number and type of microsatellite markers, as well as, the expected genetic patterns in the context of operational investigations. By considering the local dynamics, elimination programmes could cost-effectively use molecular markers. However, population level studies need to consider the local limitations of a given set of loci in terms of providing epidemiologically relevant information.
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Literature
1.
go back to reference Imwong M, Nair S, Pukrittayakamee S, Sudimack D, Williams JT, Mayxay M, Newton PN, Kim JR, Nandy A, Osorio L, Carlton JM, White NJ, Day NP, Anderson TJ: Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. Int J Parasitol. 2007, 37: 1013-1022. 10.1016/j.ijpara.2007.02.010.CrossRefPubMed Imwong M, Nair S, Pukrittayakamee S, Sudimack D, Williams JT, Mayxay M, Newton PN, Kim JR, Nandy A, Osorio L, Carlton JM, White NJ, Day NP, Anderson TJ: Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. Int J Parasitol. 2007, 37: 1013-1022. 10.1016/j.ijpara.2007.02.010.CrossRefPubMed
2.
go back to reference Van den Eede P, Van der Auwera G, Delgado C, Huyse T, Soto-Calle VE, Gamboa D, Grande T, Rodriguez H, Llanos A, Anné J, Erhart A, D'Alessandro U: Multilocus genotyping reveals high heterogeneity and strong local population structure of the Plasmodium vivax population in the Peruvian Amazon. Malar J. 2010, 9: 151-10.1186/1475-2875-9-151.PubMedCentralCrossRefPubMed Van den Eede P, Van der Auwera G, Delgado C, Huyse T, Soto-Calle VE, Gamboa D, Grande T, Rodriguez H, Llanos A, Anné J, Erhart A, D'Alessandro U: Multilocus genotyping reveals high heterogeneity and strong local population structure of the Plasmodium vivax population in the Peruvian Amazon. Malar J. 2010, 9: 151-10.1186/1475-2875-9-151.PubMedCentralCrossRefPubMed
3.
go back to reference Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, Sitthi-Amorn C, Renaud F, Harnyuttanakorn P: Genetic diversity and population structure of Plasmodium falciparum in Thailand, a low transmission country. Malar J. 2009, 8: 155-10.1186/1475-2875-8-155.PubMedCentralCrossRefPubMed Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, Sitthi-Amorn C, Renaud F, Harnyuttanakorn P: Genetic diversity and population structure of Plasmodium falciparum in Thailand, a low transmission country. Malar J. 2009, 8: 155-10.1186/1475-2875-8-155.PubMedCentralCrossRefPubMed
4.
go back to reference Griffing SM, Mixson-Hayden T, Sridaran S, Alam MT, McCollum AM, Cabezas C, Marquiño Quezada W, Barnwell JW, De Oliveira AM, Lucas C, Arrospide N, Escalante AA, Bacon DJ, Udhayakumar V: South American Plasmodium falciparum after the malaria eradication era: clonal population expansion and survival of the fittest hybrids. PLoS One. 2011, 6: e23486-10.1371/journal.pone.0023486.PubMedCentralCrossRefPubMed Griffing SM, Mixson-Hayden T, Sridaran S, Alam MT, McCollum AM, Cabezas C, Marquiño Quezada W, Barnwell JW, De Oliveira AM, Lucas C, Arrospide N, Escalante AA, Bacon DJ, Udhayakumar V: South American Plasmodium falciparum after the malaria eradication era: clonal population expansion and survival of the fittest hybrids. PLoS One. 2011, 6: e23486-10.1371/journal.pone.0023486.PubMedCentralCrossRefPubMed
5.
go back to reference Arnott A, Barry AE, Reeder JC: Understanding the population genetics of Plasmodium vivax is essential for malaria control and elimination. Malar J. 2012, 10: 11- Arnott A, Barry AE, Reeder JC: Understanding the population genetics of Plasmodium vivax is essential for malaria control and elimination. Malar J. 2012, 10: 11-
6.
go back to reference Chenet SM, Tapia LL, Escalante AA, Durand S, Lucas C, Bacon DJ: Genetic diversity and population structure of genes encoding vaccine candidate antigens of Plasmodium vivax. Malar J. 2012, 11: 68-10.1186/1475-2875-11-68.PubMedCentralCrossRefPubMed Chenet SM, Tapia LL, Escalante AA, Durand S, Lucas C, Bacon DJ: Genetic diversity and population structure of genes encoding vaccine candidate antigens of Plasmodium vivax. Malar J. 2012, 11: 68-10.1186/1475-2875-11-68.PubMedCentralCrossRefPubMed
7.
go back to reference Iwagami M, Fukumoto M, Hwang SY, Kim SH, Kho WG, Kano S: Population structure and transmission dynamics of Plasmodium vivax in the Republic of Korea based on microsatellite DNA analysis. PLoS Negl Trop Dis. 2012, 6: e1592-10.1371/journal.pntd.0001592.PubMedCentralCrossRefPubMed Iwagami M, Fukumoto M, Hwang SY, Kim SH, Kho WG, Kano S: Population structure and transmission dynamics of Plasmodium vivax in the Republic of Korea based on microsatellite DNA analysis. PLoS Negl Trop Dis. 2012, 6: e1592-10.1371/journal.pntd.0001592.PubMedCentralCrossRefPubMed
8.
go back to reference Wright S: Isolation by distance. Genetics. 1943, 2: 114-38. Wright S: Isolation by distance. Genetics. 1943, 2: 114-38.
9.
go back to reference Meirmans PG: The trouble with isolation by distance. Mol Ecol. 2012, 21: 2839-46. 10.1111/j.1365-294X.2012.05578.x.CrossRefPubMed Meirmans PG: The trouble with isolation by distance. Mol Ecol. 2012, 21: 2839-46. 10.1111/j.1365-294X.2012.05578.x.CrossRefPubMed
10.
go back to reference Gauthier C, Tibayrenc M: Population structure of malaria parasites: the driving epidemiological forces. Acta Trop. 2005, 3: 241-250.CrossRef Gauthier C, Tibayrenc M: Population structure of malaria parasites: the driving epidemiological forces. Acta Trop. 2005, 3: 241-250.CrossRef
11.
go back to reference Mu J, Awadalla P, Duan J, McGee KM, Joy DA, McVean GA, Su XZ: Recombination hotspots and population structure in Plasmodium falciparum. PLoS Biol. 2005, 3: e335-10.1371/journal.pbio.0030335.PubMedCentralCrossRefPubMed Mu J, Awadalla P, Duan J, McGee KM, Joy DA, McVean GA, Su XZ: Recombination hotspots and population structure in Plasmodium falciparum. PLoS Biol. 2005, 3: e335-10.1371/journal.pbio.0030335.PubMedCentralCrossRefPubMed
12.
go back to reference Volkman SK, Sabeti PC, DeCaprio D, Neafsey DE, Schaffner SF, Milner DA, Daily JP, Sarr O, Ndiaye D, Ndir O, Mboup S, Duraisingh MT, Lukens A, Derr A, Stange-Thomann N, Waggoner S, Onofrio R, Ziaugra L, Mauceli E, Gnerre S, Jaffe DB, Zainoun J, Wiegand RC, Birren BW, Hartl DL, Galagan JE, Lander ES, Wirth DF: A genome-wide map of diversity in Plasmodium falciparum. Nat Genet. 2007, 39: 113-119. 10.1038/ng1930.CrossRefPubMed Volkman SK, Sabeti PC, DeCaprio D, Neafsey DE, Schaffner SF, Milner DA, Daily JP, Sarr O, Ndiaye D, Ndir O, Mboup S, Duraisingh MT, Lukens A, Derr A, Stange-Thomann N, Waggoner S, Onofrio R, Ziaugra L, Mauceli E, Gnerre S, Jaffe DB, Zainoun J, Wiegand RC, Birren BW, Hartl DL, Galagan JE, Lander ES, Wirth DF: A genome-wide map of diversity in Plasmodium falciparum. Nat Genet. 2007, 39: 113-119. 10.1038/ng1930.CrossRefPubMed
13.
go back to reference Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P, Milner DA, Lukens A, Rosen D, Daniels R, Houde N, Cortese JF, Tyndall E, Gates C, Stange-Thomann N, Sarr O, Ndiaye D, Ndir O, Mboup S, Ferreira MU, Moraes Sdo L, Dash AP, Chitnis CE, Wiegand RC, Hartl DL, Birren BW, Lander ES, Sabeti PC, Wirth DF: Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol. 2008, 9: R171-10.1186/gb-2008-9-12-r171.PubMedCentralCrossRefPubMed Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P, Milner DA, Lukens A, Rosen D, Daniels R, Houde N, Cortese JF, Tyndall E, Gates C, Stange-Thomann N, Sarr O, Ndiaye D, Ndir O, Mboup S, Ferreira MU, Moraes Sdo L, Dash AP, Chitnis CE, Wiegand RC, Hartl DL, Birren BW, Lander ES, Sabeti PC, Wirth DF: Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol. 2008, 9: R171-10.1186/gb-2008-9-12-r171.PubMedCentralCrossRefPubMed
14.
go back to reference Cheeseman IH, Miller BA, Nair S, Nkhoma S, Tan A, Tan JC, Al Saai S, Phyo AP, Moo CL, Lwin KM, McGready R, Ashley E, Imwong M, Stepniewska K, Yi P, Dondorp AM, Mayxay M, Newton PN, White NJ, Nosten F, Ferdig MT, Anderson TJ: A major genome region underlying artemisinin resistance in malaria. Science. 2012, 336: 79-82. 10.1126/science.1215966.PubMedCentralCrossRefPubMed Cheeseman IH, Miller BA, Nair S, Nkhoma S, Tan A, Tan JC, Al Saai S, Phyo AP, Moo CL, Lwin KM, McGready R, Ashley E, Imwong M, Stepniewska K, Yi P, Dondorp AM, Mayxay M, Newton PN, White NJ, Nosten F, Ferdig MT, Anderson TJ: A major genome region underlying artemisinin resistance in malaria. Science. 2012, 336: 79-82. 10.1126/science.1215966.PubMedCentralCrossRefPubMed
15.
go back to reference Orjuela-Sánchez P, Karunaweera ND, da Silva-Nunes M, da Silva NS, Scopel KK, Gonçalves RM, Amaratunga C, Sá JM, Socheat D, Fairhust RM, Gunawardena S, Thavakodirasah T, Galapaththy GL, Abeysinghe R, Kawamoto F, Wirth DF, Ferreira MU: Single-nucleotide polymorphism, linkage disequilibrium and geographic structure in the malaria parasite Plasmodium vivax: prospects for genome-wide association studies. BMC Genet. 2010, 11: 65-PubMedCentralCrossRefPubMed Orjuela-Sánchez P, Karunaweera ND, da Silva-Nunes M, da Silva NS, Scopel KK, Gonçalves RM, Amaratunga C, Sá JM, Socheat D, Fairhust RM, Gunawardena S, Thavakodirasah T, Galapaththy GL, Abeysinghe R, Kawamoto F, Wirth DF, Ferreira MU: Single-nucleotide polymorphism, linkage disequilibrium and geographic structure in the malaria parasite Plasmodium vivax: prospects for genome-wide association studies. BMC Genet. 2010, 11: 65-PubMedCentralCrossRefPubMed
16.
17.
go back to reference Russell B, Suwanarusk R, Lek-Uthai U: Plasmodium vivax genetic diversity: microsatellite length matters. Trends Parasitol. 2006, 22: 399-401. 10.1016/j.pt.2006.06.013.CrossRefPubMed Russell B, Suwanarusk R, Lek-Uthai U: Plasmodium vivax genetic diversity: microsatellite length matters. Trends Parasitol. 2006, 22: 399-401. 10.1016/j.pt.2006.06.013.CrossRefPubMed
18.
go back to reference Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, Baruch DI, Magill AJ, Su XZ: Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature. 2002, 418: 320-323. 10.1038/nature00813.CrossRefPubMed Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, Baruch DI, Magill AJ, Su XZ: Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature. 2002, 418: 320-323. 10.1038/nature00813.CrossRefPubMed
19.
go back to reference McCollum AM, Basco LK, Tahar R, Udhayakumar V, Escalante AA: Hitchhiking and selective sweeps of Plasmodium falciparum sulfadoxine and pyrimethamine resistance alleles in a population from central Africa. Antimicrob Agents Chemother. 2008, 52: 4089-4097. 10.1128/AAC.00623-08.PubMedCentralCrossRefPubMed McCollum AM, Basco LK, Tahar R, Udhayakumar V, Escalante AA: Hitchhiking and selective sweeps of Plasmodium falciparum sulfadoxine and pyrimethamine resistance alleles in a population from central Africa. Antimicrob Agents Chemother. 2008, 52: 4089-4097. 10.1128/AAC.00623-08.PubMedCentralCrossRefPubMed
20.
go back to reference McCollum AM, Schneider KA, Griffing SM, Zhou Z, Kariuki S, Ter-Kuile F, Shi YP, Slutsker L, Lal AA, Udhayakumar V, Escalante AA: Differences in selective pressure on dhps and dhfr drug resistant mutations in western Kenya. Malar J. 2012, 11: 77-10.1186/1475-2875-11-77.PubMedCentralCrossRefPubMed McCollum AM, Schneider KA, Griffing SM, Zhou Z, Kariuki S, Ter-Kuile F, Shi YP, Slutsker L, Lal AA, Udhayakumar V, Escalante AA: Differences in selective pressure on dhps and dhfr drug resistant mutations in western Kenya. Malar J. 2012, 11: 77-10.1186/1475-2875-11-77.PubMedCentralCrossRefPubMed
21.
go back to reference Nyachieo A, VAN Overmeir C, Laurent T, Dujardin JC, D'Alessandro U: Plasmodium falciparum genotyping by microsatellites as a method to distinguish between recrudescent and new infections. AmJTrop Med Hyg. 2005, 73: 210-3. Nyachieo A, VAN Overmeir C, Laurent T, Dujardin JC, D'Alessandro U: Plasmodium falciparum genotyping by microsatellites as a method to distinguish between recrudescent and new infections. AmJTrop Med Hyg. 2005, 73: 210-3.
22.
go back to reference Greenhouse B, Myrick A, Dokomajilar C, Woo JM, Carlson EJ, Rosenthal PJ, Dorsey G: Validation of microsatellite markers for use in genotyping polyclonal Plasmodium falciparum infections. AmJTrop Med Hyg. 2006, 75: 836-842. Greenhouse B, Myrick A, Dokomajilar C, Woo JM, Carlson EJ, Rosenthal PJ, Dorsey G: Validation of microsatellite markers for use in genotyping polyclonal Plasmodium falciparum infections. AmJTrop Med Hyg. 2006, 75: 836-842.
23.
go back to reference Orjuela-Sánchez P, da Silva NS, da Silva-Nunes M, Ferreira MU: Recurrent parasitemias and population dynamics of Plasmodium vivax polymorphisms in rural Amazonia. AmJTrop Med Hyg. 2009, 81: 961-968. 10.4269/ajtmh.2009.09-0337.CrossRef Orjuela-Sánchez P, da Silva NS, da Silva-Nunes M, Ferreira MU: Recurrent parasitemias and population dynamics of Plasmodium vivax polymorphisms in rural Amazonia. AmJTrop Med Hyg. 2009, 81: 961-968. 10.4269/ajtmh.2009.09-0337.CrossRef
24.
go back to reference Restrepo E, Imwong M, Rojas W, Carmona-Fonseca J, Maestre A: High genetic polymorphism of relapsing P. vivax isolates in northwest Colombia. Acta Trop. 2011, 119: 23-29. 10.1016/j.actatropica.2011.03.012.PubMedCentralCrossRefPubMed Restrepo E, Imwong M, Rojas W, Carmona-Fonseca J, Maestre A: High genetic polymorphism of relapsing P. vivax isolates in northwest Colombia. Acta Trop. 2011, 119: 23-29. 10.1016/j.actatropica.2011.03.012.PubMedCentralCrossRefPubMed
25.
go back to reference Sunnucks P: Efficient genetic markers for population biology. Trends Ecol Evol. 2000, 15: 199-203. 10.1016/S0169-5347(00)01825-5.CrossRefPubMed Sunnucks P: Efficient genetic markers for population biology. Trends Ecol Evol. 2000, 15: 199-203. 10.1016/S0169-5347(00)01825-5.CrossRefPubMed
26.
go back to reference Mwangi JM, Omar SA, Ranford-Cartwright LC: Comparison of microsatellite and antigen-coding loci for differentiating recrudescing Plasmodium falciparum infections from reinfections in Kenya. Int J Parasitol. 2006, 36: 329-336. 10.1016/j.ijpara.2005.10.013.CrossRefPubMed Mwangi JM, Omar SA, Ranford-Cartwright LC: Comparison of microsatellite and antigen-coding loci for differentiating recrudescing Plasmodium falciparum infections from reinfections in Kenya. Int J Parasitol. 2006, 36: 329-336. 10.1016/j.ijpara.2005.10.013.CrossRefPubMed
27.
go back to reference Schneider KA, Kim Y: An analytical model for genetic hitchhiking in the evolution of antimalarial drug resistance. Theor Popul Biol. 2010, 78: 93-108. 10.1016/j.tpb.2010.06.005.PubMedCentralCrossRefPubMed Schneider KA, Kim Y: An analytical model for genetic hitchhiking in the evolution of antimalarial drug resistance. Theor Popul Biol. 2010, 78: 93-108. 10.1016/j.tpb.2010.06.005.PubMedCentralCrossRefPubMed
28.
go back to reference McCollum AM, Mueller K, Villegas L, Udhayakumar V, Escalante AA: Common origin and fixation of Plasmodium falciparum dhfr and dhps mutations associated with sulfadoxine-pyrimethamine resistance in a low-transmission area in South America. Antimicrob Agents Chemother. 2007, 51: 2085-2091. 10.1128/AAC.01228-06.PubMedCentralCrossRefPubMed McCollum AM, Mueller K, Villegas L, Udhayakumar V, Escalante AA: Common origin and fixation of Plasmodium falciparum dhfr and dhps mutations associated with sulfadoxine-pyrimethamine resistance in a low-transmission area in South America. Antimicrob Agents Chemother. 2007, 51: 2085-2091. 10.1128/AAC.01228-06.PubMedCentralCrossRefPubMed
29.
go back to reference Schneider KA, Kim Y: Approximations for the hitchhiking effect caused by the evolution of antimalarial-drug resistance. J Math Biol. 2011, 62: 789-832. 10.1007/s00285-010-0353-9.PubMedCentralCrossRefPubMed Schneider KA, Kim Y: Approximations for the hitchhiking effect caused by the evolution of antimalarial-drug resistance. J Math Biol. 2011, 62: 789-832. 10.1007/s00285-010-0353-9.PubMedCentralCrossRefPubMed
30.
go back to reference Moreno JE, Rubio-Palis Y, Páez E, Pérez E, Sánchez V: Abundance, biting behaviour and parous rate of anopheline mosquito species in relation to malaria incidence in gold-mining areas of southern Venezuela. Med Vet Entomol. 2007, 21: 339-349. 10.1111/j.1365-2915.2007.00704.x.CrossRefPubMed Moreno JE, Rubio-Palis Y, Páez E, Pérez E, Sánchez V: Abundance, biting behaviour and parous rate of anopheline mosquito species in relation to malaria incidence in gold-mining areas of southern Venezuela. Med Vet Entomol. 2007, 21: 339-349. 10.1111/j.1365-2915.2007.00704.x.CrossRefPubMed
31.
go back to reference Imwong M, Sudimack D, Pukrittayakamee S, Osorio L, Carlton JM, Day NP, White NJ, Anderson TJ: Microsatellite variation, repeat array length, and population history of Plasmodium vivax. Mol Biol Evol. 2006, 23: 1016-1018. 10.1093/molbev/msj116.CrossRefPubMed Imwong M, Sudimack D, Pukrittayakamee S, Osorio L, Carlton JM, Day NP, White NJ, Anderson TJ: Microsatellite variation, repeat array length, and population history of Plasmodium vivax. Mol Biol Evol. 2006, 23: 1016-1018. 10.1093/molbev/msj116.CrossRefPubMed
32.
go back to reference Karunaweera ND, Ferreira MU, Munasinghe A, Barnwell JW, Collins WE, King CL, Kawamoto F, Hartl DL, Wirth DF: Extensive microsatellite diversity in the human malaria parasite Plasmodium vivax. Gene. 2008, 410: 105-112. 10.1016/j.gene.2007.11.022.CrossRefPubMed Karunaweera ND, Ferreira MU, Munasinghe A, Barnwell JW, Collins WE, King CL, Kawamoto F, Hartl DL, Wirth DF: Extensive microsatellite diversity in the human malaria parasite Plasmodium vivax. Gene. 2008, 410: 105-112. 10.1016/j.gene.2007.11.022.CrossRefPubMed
33.
go back to reference Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP: Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999, 119: 113-125. 10.1017/S0031182099004552.CrossRefPubMed Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP: Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999, 119: 113-125. 10.1017/S0031182099004552.CrossRefPubMed
35.
go back to reference Nash D, Nair S, Mayxay M, Newton PN, Guthmann JP, Nosten F, Anderson TJ: Selection strength and hitchhiking around two anti-malarial resistance genes. Proc Biol Sci. 2005, 272: 1153-1161. 10.1098/rspb.2004.3026.PubMedCentralCrossRefPubMed Nash D, Nair S, Mayxay M, Newton PN, Guthmann JP, Nosten F, Anderson TJ: Selection strength and hitchhiking around two anti-malarial resistance genes. Proc Biol Sci. 2005, 272: 1153-1161. 10.1098/rspb.2004.3026.PubMedCentralCrossRefPubMed
41.
go back to reference Laval EG, Schneider S: Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform. 2005, 1: 47-50. Laval EG, Schneider S: Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform. 2005, 1: 47-50.
43.
go back to reference Maruyama T: Stochastic integrals and their application to population genetics. Molecular Evolution, Protein Polymorphism and the Neutral Theory. Edited by: Kimura M. 1982, Tokyo: Japan Scientific Societies Press, 151-166. Maruyama T: Stochastic integrals and their application to population genetics. Molecular Evolution, Protein Polymorphism and the Neutral Theory. Edited by: Kimura M. 1982, Tokyo: Japan Scientific Societies Press, 151-166.
44.
go back to reference Freeman GH, Halton JH: Note on an Exact Treatment of Contingency, Goodness of Fit and Other Problems of Significance. Biometrika. 1951, 38: 141-149.CrossRefPubMed Freeman GH, Halton JH: Note on an Exact Treatment of Contingency, Goodness of Fit and Other Problems of Significance. Biometrika. 1951, 38: 141-149.CrossRefPubMed
45.
46.
go back to reference Ferreira MU, Karunaweera ND, da Silva-Nunes M, da Silva NS, Wirth DF, Hartl DL: Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. J Infect Dis. 2007, 195: 1218-1226. 10.1086/512685.CrossRefPubMed Ferreira MU, Karunaweera ND, da Silva-Nunes M, da Silva NS, Wirth DF, Hartl DL: Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. J Infect Dis. 2007, 195: 1218-1226. 10.1086/512685.CrossRefPubMed
47.
go back to reference Urdaneta L, Lal A, Barnabe C, Oury B, Goldman I, Ayala FJ, Tibayrenc M: Evidence for clonal propagation in natural isolates of Plasmodium falciparum from Venezuela. Proc Natl Acad Sci USA. 2001, 98: 6725-6729. 10.1073/pnas.111144998.PubMedCentralCrossRefPubMed Urdaneta L, Lal A, Barnabe C, Oury B, Goldman I, Ayala FJ, Tibayrenc M: Evidence for clonal propagation in natural isolates of Plasmodium falciparum from Venezuela. Proc Natl Acad Sci USA. 2001, 98: 6725-6729. 10.1073/pnas.111144998.PubMedCentralCrossRefPubMed
48.
go back to reference Razakandrainibe FG, Durand P, Koella JC, De Meeüs T, Rousset F, Ayala FJ, Renaud F: "Clonal" population structure of the malaria agent Plasmodium falciparum in high-infection regions. Proc Natl Acad Sci USA. 2005, 102: 17388-93. 10.1073/pnas.0508871102.PubMedCentralCrossRefPubMed Razakandrainibe FG, Durand P, Koella JC, De Meeüs T, Rousset F, Ayala FJ, Renaud F: "Clonal" population structure of the malaria agent Plasmodium falciparum in high-infection regions. Proc Natl Acad Sci USA. 2005, 102: 17388-93. 10.1073/pnas.0508871102.PubMedCentralCrossRefPubMed
Metadata
Title
Local population structure of Plasmodium: impact on malaria control and elimination
Authors
Stella M Chenet
Kristan A Schneider
Leopoldo Villegas
Ananias A Escalante
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2012
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-11-412

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