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Published in: Malaria Journal 1/2012

Open Access 01-12-2012 | Research

Population genetic structure of Plasmodium falciparum across a region of diverse endemicity in West Africa

Authors: Victor A Mobegi, Kovana M Loua, Ambroise D Ahouidi, Judith Satoguina, Davis C Nwakanma, Alfred Amambua-Ngwa, David J Conway

Published in: Malaria Journal | Issue 1/2012

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Abstract

Background

Malaria parasite population genetic structure varies among areas of differing endemicity, but this has not been systematically studied across Plasmodium falciparum populations in Africa where most infections occur.

Methods

Ten polymorphic P. falciparum microsatellite loci were genotyped in 268 infections from eight locations in four West African countries (Republic of Guinea, Guinea Bissau, The Gambia and Senegal), spanning a highly endemic forested region in the south to a low endemic Sahelian region in the north. Analysis was performed on proportions of mixed genotype infections, genotypic diversity among isolates, multilocus standardized index of association, and inter-population differentiation.

Results

Each location had similar levels of pairwise genotypic diversity among isolates, although there were many more mixed parasite genotype infections in the south. Apart from a few isolates that were virtually identical, the multilocus index of association was not significant in any population. Genetic differentiation between populations was low (most pairwise FST values < 0.03), and an overall test for isolation by distance was not significant.

Conclusions

Although proportions of mixed genotype infections varied with endemicity as expected, population genetic structure was similar across the diverse sites. Very substantial reduction in transmission would be needed to cause fragmented or epidemic sub-structure in this region.
Appendix
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Literature
1.
go back to reference Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI: The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005, 434: 214-217. 10.1038/nature03342.PubMedCentralCrossRefPubMed Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI: The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005, 434: 214-217. 10.1038/nature03342.PubMedCentralCrossRefPubMed
3.
go back to reference Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD: Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet. 2012, 379: 413-431. 10.1016/S0140-6736(12)60034-8.CrossRefPubMed Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD: Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet. 2012, 379: 413-431. 10.1016/S0140-6736(12)60034-8.CrossRefPubMed
4.
go back to reference Hay S, Rogers D, Toomer J, Snow R: Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: literature survey, Internet access and review. Trans R Soc Trop Med Hyg. 2000, 94: 113-127. 10.1016/S0035-9203(00)90246-3.PubMedCentralCrossRefPubMed Hay S, Rogers D, Toomer J, Snow R: Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: literature survey, Internet access and review. Trans R Soc Trop Med Hyg. 2000, 94: 113-127. 10.1016/S0035-9203(00)90246-3.PubMedCentralCrossRefPubMed
5.
go back to reference Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker S, Smith DL, Moyeed RA, Snow RW: A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 2009, 6: e1000048-PubMedCentralCrossRefPubMed Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker S, Smith DL, Moyeed RA, Snow RW: A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 2009, 6: e1000048-PubMedCentralCrossRefPubMed
6.
go back to reference Mu J, Awadalla P, Duan J, McGee KM, Joy DA, McVean GA, Su X-Z: 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 X-Z: Recombination hotspots and population structure in Plasmodium falciparum. PLoS Biol. 2005, 3: e335-10.1371/journal.pbio.0030335.PubMedCentralCrossRefPubMed
7.
go back to reference Paul REL, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, Paru R, Day KP: Mating patterns in malaria parasite populations of Papua New Guinea. Science. 1995, 269: 1709-1711. 10.1126/science.7569897.CrossRefPubMed Paul REL, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, Paru R, Day KP: Mating patterns in malaria parasite populations of Papua New Guinea. Science. 1995, 269: 1709-1711. 10.1126/science.7569897.CrossRefPubMed
8.
go back to reference Anderson TJC, 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: Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol. 2000, 17: 1467-1482. 10.1093/oxfordjournals.molbev.a026247.CrossRefPubMed Anderson TJC, 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: Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol. 2000, 17: 1467-1482. 10.1093/oxfordjournals.molbev.a026247.CrossRefPubMed
9.
go back to reference Machado RLD, Póvoa MM, Calvosa VSP, Ferreira MU, Rossit ARB, dos Santos EJM, Conway DJ: Genetic structure of Plasmodium falciparum populations in the Brazilian Amazon region. J Infect Dis. 2004, 190: 1547-1555. 10.1086/424601.CrossRefPubMed Machado RLD, Póvoa MM, Calvosa VSP, Ferreira MU, Rossit ARB, dos Santos EJM, Conway DJ: Genetic structure of Plasmodium falciparum populations in the Brazilian Amazon region. J Infect Dis. 2004, 190: 1547-1555. 10.1086/424601.CrossRefPubMed
10.
go back to reference Anthony T, Conway D, Cox-Singh J, Matusop A, Ratnam S, Shamsul S, Singh B: Fragmented population structure of Plasmodium falciparum in a region of declining endemicity. J Infect Dis. 2005, 191: 1558-1564. 10.1086/429338.CrossRefPubMed Anthony T, Conway D, Cox-Singh J, Matusop A, Ratnam S, Shamsul S, Singh B: Fragmented population structure of Plasmodium falciparum in a region of declining endemicity. J Infect Dis. 2005, 191: 1558-1564. 10.1086/429338.CrossRefPubMed
11.
go back to reference Chokejindachai W, Conway DJ: Case–control approach to identify Plasmodium falciparum polymorphisms associated with severe malaria. PLoS One. 2009, 4: e5454-10.1371/journal.pone.0005454.PubMedCentralCrossRefPubMed Chokejindachai W, Conway DJ: Case–control approach to identify Plasmodium falciparum polymorphisms associated with severe malaria. PLoS One. 2009, 4: e5454-10.1371/journal.pone.0005454.PubMedCentralCrossRefPubMed
12.
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
13.
go back to reference Iwagami M, Rivera P, Villacorte E, Escueta A, Hatabu T, Kawazu S-, Hayakawa T, Tanabe K, Kano S: Genetic diversity and population structure of Plasmodium falciparum in the Philippines. Malar J. 2009, 8: 96-10.1186/1475-2875-8-96.PubMedCentralCrossRefPubMed Iwagami M, Rivera P, Villacorte E, Escueta A, Hatabu T, Kawazu S-, Hayakawa T, Tanabe K, Kano S: Genetic diversity and population structure of Plasmodium falciparum in the Philippines. Malar J. 2009, 8: 96-10.1186/1475-2875-8-96.PubMedCentralCrossRefPubMed
14.
go back to reference Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, Nale J, Kiniboro B, Buckee CO, Tavul L, Siba PM, Reeder JC, Barry AE: Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Malar J. 2010, 9: 336-10.1186/1475-2875-9-336.PubMedCentralCrossRefPubMed Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, Nale J, Kiniboro B, Buckee CO, Tavul L, Siba PM, Reeder JC, Barry AE: Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Malar J. 2010, 9: 336-10.1186/1475-2875-9-336.PubMedCentralCrossRefPubMed
15.
go back to reference Conway DJ, Roper C, Oduola AMJ, Arnot DE, Kremsner PG, Grobusch MP, Curtis CF, Greenwood BM: High recombination rate in natural populations of Plasmodium falciparum. Proc Natl Acad Sci USA. 1999, 96: 4506-4511. 10.1073/pnas.96.8.4506.PubMedCentralCrossRefPubMed Conway DJ, Roper C, Oduola AMJ, Arnot DE, Kremsner PG, Grobusch MP, Curtis CF, Greenwood BM: High recombination rate in natural populations of Plasmodium falciparum. Proc Natl Acad Sci USA. 1999, 96: 4506-4511. 10.1073/pnas.96.8.4506.PubMedCentralCrossRefPubMed
16.
go back to reference Conway DJ, Machado RLD, Singh B, Dessert P, Mikes ZS, Povoa MM, Oduola AMJ, Roper C: Extreme geographical fixation of variation in the Plasmodium falciparum gamete surface protein gene Pfs48/45 compared with microsatellite loci. Mol Biochem Parasitol. 2001, 115: 145-156. 10.1016/S0166-6851(01)00278-X.CrossRefPubMed Conway DJ, Machado RLD, Singh B, Dessert P, Mikes ZS, Povoa MM, Oduola AMJ, Roper C: Extreme geographical fixation of variation in the Plasmodium falciparum gamete surface protein gene Pfs48/45 compared with microsatellite loci. Mol Biochem Parasitol. 2001, 115: 145-156. 10.1016/S0166-6851(01)00278-X.CrossRefPubMed
17.
go back to reference Lynch C, Roper C: The transit phase of migration: circulation of malaria and its multidrug-resistant forms in Africa. PLoS Med. 2011, 8: e1001040-10.1371/journal.pmed.1001040.PubMedCentralCrossRefPubMed Lynch C, Roper C: The transit phase of migration: circulation of malaria and its multidrug-resistant forms in Africa. PLoS Med. 2011, 8: e1001040-10.1371/journal.pmed.1001040.PubMedCentralCrossRefPubMed
18.
go back to reference Bogreau H, Renaud F, Bouchiba H, Durand P, Assi S-B, Henry M-C, Garnotel E, Pradines B, Fusai T, Wade B, Adehossi E, Parola P, Kamil MA, Puijalon O, Rogier C: Genetic diversity and structure of African Plasmodium falciparum populations in Urban and Rural areas. Am J Trop Med Hyg. 2006, 74: 953-959.PubMed Bogreau H, Renaud F, Bouchiba H, Durand P, Assi S-B, Henry M-C, Garnotel E, Pradines B, Fusai T, Wade B, Adehossi E, Parola P, Kamil MA, Puijalon O, Rogier C: Genetic diversity and structure of African Plasmodium falciparum populations in Urban and Rural areas. Am J Trop Med Hyg. 2006, 74: 953-959.PubMed
19.
go back to reference Rebaudet S, Bogreau H, Silaï R, Lepère J-F, Bertaux L, Pradines B, Delmont J, Parola P, Rogier C: Genetic Structure of Plasmodium falciparum and Elimination of Malaria, Comoros Archipelago. Emerg Infect Dis. 2010, 16: 1686-1694.PubMedCentralCrossRefPubMed Rebaudet S, Bogreau H, Silaï R, Lepère J-F, Bertaux L, Pradines B, Delmont J, Parola P, Rogier C: Genetic Structure of Plasmodium falciparum and Elimination of Malaria, Comoros Archipelago. Emerg Infect Dis. 2010, 16: 1686-1694.PubMedCentralCrossRefPubMed
20.
go back to reference O'Meara WP, Mangeni JN, Steketee R, Greenwood B: Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis. 2010, 10: 545-555. 10.1016/S1473-3099(10)70096-7.CrossRefPubMed O'Meara WP, Mangeni JN, Steketee R, Greenwood B: Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis. 2010, 10: 545-555. 10.1016/S1473-3099(10)70096-7.CrossRefPubMed
21.
go back to reference Ceesay SJ, Casals-Pascual C, Nwakanma DC, Walther M, Gomez-Escobar N, Fulford AJC, Takem EN, Nogaro S, Bojang KA, Corrah T, Jaye MC, Taal MA, Sonko AA, Conway DJ: Continued decline of malaria in The Gambia with implications for elimination. PLoS One. 2010, 5: e12242-10.1371/journal.pone.0012242.PubMedCentralCrossRefPubMed Ceesay SJ, Casals-Pascual C, Nwakanma DC, Walther M, Gomez-Escobar N, Fulford AJC, Takem EN, Nogaro S, Bojang KA, Corrah T, Jaye MC, Taal MA, Sonko AA, Conway DJ: Continued decline of malaria in The Gambia with implications for elimination. PLoS One. 2010, 5: e12242-10.1371/journal.pone.0012242.PubMedCentralCrossRefPubMed
22.
go back to reference Ceesay SJ, Climent C-P, Jamie E, Samuel EA, Nancy OD, Anthony JCF, Sanie SSS, Ismaela A, Samuel D, Omar S, Palmer A, Fofana M, Corrah T, Bojang KA, Whittle HC, Greenwood BM, Conway DJ: Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet. 2008, 372: 1545-1554. 10.1016/S0140-6736(08)61654-2.PubMedCentralCrossRefPubMed Ceesay SJ, Climent C-P, Jamie E, Samuel EA, Nancy OD, Anthony JCF, Sanie SSS, Ismaela A, Samuel D, Omar S, Palmer A, Fofana M, Corrah T, Bojang KA, Whittle HC, Greenwood BM, Conway DJ: Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet. 2008, 372: 1545-1554. 10.1016/S0140-6736(08)61654-2.PubMedCentralCrossRefPubMed
23.
go back to reference Trape JF, Sauvage C, Ndiaye O, Douillot L, Marra A, Diallo A, Cisse B, Greenwood B, Milligan P, Sokhna C, Molez JF: New malaria-control policies and child mortality in Senegal: reaching Millennium Development Goal 4. J Infect Dis. 2012, 205: 672-679. 10.1093/infdis/jir805.PubMedCentralCrossRefPubMed Trape JF, Sauvage C, Ndiaye O, Douillot L, Marra A, Diallo A, Cisse B, Greenwood B, Milligan P, Sokhna C, Molez JF: New malaria-control policies and child mortality in Senegal: reaching Millennium Development Goal 4. J Infect Dis. 2012, 205: 672-679. 10.1093/infdis/jir805.PubMedCentralCrossRefPubMed
24.
go back to reference Satoguina J, Walther B, Drakeley C, Nwakanma D, Oriero E, Correa S, Corran P, Conway D, Walther M: Comparison of surveillance methods applied to a situation of low malaria prevalence at rural sites in The Gambia and Guinea Bissau. Malar J. 2009, 8: 274-10.1186/1475-2875-8-274.PubMedCentralCrossRefPubMed Satoguina J, Walther B, Drakeley C, Nwakanma D, Oriero E, Correa S, Corran P, Conway D, Walther M: Comparison of surveillance methods applied to a situation of low malaria prevalence at rural sites in The Gambia and Guinea Bissau. Malar J. 2009, 8: 274-10.1186/1475-2875-8-274.PubMedCentralCrossRefPubMed
25.
go back to reference Walther M, Jeffries D, Finney OC, Njie M, Ebonyi A, Deininger S, Lawrence E, Ngwa-Amambua A, Jayasooriya S, Cheeseman IH, Gomez-Escobar N, Okebe J, Conway DJ, Riley EM: Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog. 2009, 5: e1000364-10.1371/journal.ppat.1000364.PubMedCentralCrossRefPubMed Walther M, Jeffries D, Finney OC, Njie M, Ebonyi A, Deininger S, Lawrence E, Ngwa-Amambua A, Jayasooriya S, Cheeseman IH, Gomez-Escobar N, Okebe J, Conway DJ, Riley EM: Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog. 2009, 5: e1000364-10.1371/journal.ppat.1000364.PubMedCentralCrossRefPubMed
26.
go back to reference Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah M, Rahman H: A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999, 60: 687-692.PubMed Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah M, Rahman H: A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999, 60: 687-692.PubMed
27.
go back to reference Anderson T, Su X, Bockarie M, Lagog M, Day K: Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999, 119: 113-125. 10.1017/S0031182099004552.CrossRefPubMed Anderson T, Su X, Bockarie M, Lagog M, Day K: Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999, 119: 113-125. 10.1017/S0031182099004552.CrossRefPubMed
28.
go back to reference Su X-Z, Wellems TE: Toward a high-resolution Plasmodium falciparum linkage map: Polymorphic markers from hundreds of simple sequence repeats. Genomics. 1996, 33: 430-444. 10.1006/geno.1996.0218.CrossRefPubMed Su X-Z, Wellems TE: Toward a high-resolution Plasmodium falciparum linkage map: Polymorphic markers from hundreds of simple sequence repeats. Genomics. 1996, 33: 430-444. 10.1006/geno.1996.0218.CrossRefPubMed
29.
go back to reference Goudet J: FSTAT (version 1.2): a computer program to calculate F statistics. J Hered. 1995, 86: 485-486. Goudet J: FSTAT (version 1.2): a computer program to calculate F statistics. J Hered. 1995, 86: 485-486.
30.
go back to reference Huson DH, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006, 23: 254-267.CrossRefPubMed Huson DH, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006, 23: 254-267.CrossRefPubMed
31.
go back to reference Haubold B, Hudson RR: LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics. 2000, 16: 847-849. 10.1093/bioinformatics/16.9.847.CrossRefPubMed Haubold B, Hudson RR: LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics. 2000, 16: 847-849. 10.1093/bioinformatics/16.9.847.CrossRefPubMed
32.
go back to reference Rousset F: Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resources. 2008, 8: 103-106. 10.1111/j.1471-8286.2007.01931.x.CrossRef Rousset F: Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resources. 2008, 8: 103-106. 10.1111/j.1471-8286.2007.01931.x.CrossRef
33.
go back to reference Durand P, Michalakis Y, Cestier S, Oury B, LeClerc MC, Tibayrenc M, Renaud F: Significant linkage disequilibrium and high genetic diversity in a population of Plasmodium falciparum from an area (Republic of The Congo) highly endemic for malaria. Am J Trop Med Hyg. 2003, 68: 345-349.PubMed Durand P, Michalakis Y, Cestier S, Oury B, LeClerc MC, Tibayrenc M, Renaud F: Significant linkage disequilibrium and high genetic diversity in a population of Plasmodium falciparum from an area (Republic of The Congo) highly endemic for malaria. Am J Trop Med Hyg. 2003, 68: 345-349.PubMed
34.
go back to reference Zhong D, Afrane Y, Githeko A, Yang Z, Cui L, Menge D, Temu E, Yan G: Plasmodium falciparum genetic diversity in western Kenya highlands. Am J Trop Med Hyg. 2007, 77: 1043-1050.PubMed Zhong D, Afrane Y, Githeko A, Yang Z, Cui L, Menge D, Temu E, Yan G: Plasmodium falciparum genetic diversity in western Kenya highlands. Am J Trop Med Hyg. 2007, 77: 1043-1050.PubMed
35.
go back to reference Amodu OK, Oyedeji SI, Ntoumi F, Orimadegun AE, Gbadegesin RA, Olumese PE, Omotade OO: Complexity of the msp2 locus and the severity of childhood malaria, in south-western Nigeria. Ann Trop Med Parasitol. 2008, 102: 95-102. 10.1179/136485908X252340.CrossRefPubMed Amodu OK, Oyedeji SI, Ntoumi F, Orimadegun AE, Gbadegesin RA, Olumese PE, Omotade OO: Complexity of the msp2 locus and the severity of childhood malaria, in south-western Nigeria. Ann Trop Med Parasitol. 2008, 102: 95-102. 10.1179/136485908X252340.CrossRefPubMed
36.
go back to reference Beck HP, Felger I, Huber W, Steiger S, Smith T, Weiss N, Alonso P, Tanner M: Analysis of multiple Plasmodium falciparum infections in Tanzanian children during the phase III trial of the malaria vaccine SPf66. J Infect Dis. 1997, 175: 921-926. 10.1086/513991.CrossRefPubMed Beck HP, Felger I, Huber W, Steiger S, Smith T, Weiss N, Alonso P, Tanner M: Analysis of multiple Plasmodium falciparum infections in Tanzanian children during the phase III trial of the malaria vaccine SPf66. J Infect Dis. 1997, 175: 921-926. 10.1086/513991.CrossRefPubMed
37.
go back to reference Kyes S, Harding R, Black G, Craig A, Peshu N, Newbold C, Marsh K: Limited spatial clustering of individual Plasmodium falciparum alleles in field isolates from coastal Kenya. Am J Trop Med Hyg. 1997, 57: 205-215.PubMed Kyes S, Harding R, Black G, Craig A, Peshu N, Newbold C, Marsh K: Limited spatial clustering of individual Plasmodium falciparum alleles in field isolates from coastal Kenya. Am J Trop Med Hyg. 1997, 57: 205-215.PubMed
38.
go back to reference Roper C, Richardson W, Elhassan IM, Giha H, Hviid L, Satti GMH, Theander TG, Arnot DE: Seasonal changes in the Plasmodium falciparum population in individuals and their relationship to clinical malaria: a longitudinal study in a Sudanese village. Parasitology. 1998, 116: 501-510. 10.1017/S0031182098002650.CrossRefPubMed Roper C, Richardson W, Elhassan IM, Giha H, Hviid L, Satti GMH, Theander TG, Arnot DE: Seasonal changes in the Plasmodium falciparum population in individuals and their relationship to clinical malaria: a longitudinal study in a Sudanese village. Parasitology. 1998, 116: 501-510. 10.1017/S0031182098002650.CrossRefPubMed
39.
go back to reference Zwetyenga J, Rogier C, Tall A, Fontenille D, Snounou G, Trape JF, Mercereau-Puijalon O: 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. 1998, 59: 726-735.PubMed Zwetyenga J, Rogier C, Tall A, Fontenille D, Snounou G, Trape JF, Mercereau-Puijalon O: 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. 1998, 59: 726-735.PubMed
40.
go back to reference Engelbrecht F, Felger I, Genton B, Alpers M, Beck H-P: Plasmodium falciparum: malaria morbidity is associated with specific merozoite surface antigen 2 genotypes. Exp Parasitol. 1995, 81: 90-96. 10.1006/expr.1995.1096.CrossRefPubMed Engelbrecht F, Felger I, Genton B, Alpers M, Beck H-P: Plasmodium falciparum: malaria morbidity is associated with specific merozoite surface antigen 2 genotypes. Exp Parasitol. 1995, 81: 90-96. 10.1006/expr.1995.1096.CrossRefPubMed
41.
go back to reference Anderson TJ, Nair S, Nkhoma S, Williams JT, Imwong M, Yi P, Socheat D, Das D, Chotivanich K, Day NP, White NJ, Dondorp AM: High heritability of malaria parasite clearance rate indicates a genetic basis for artemisinin resistance in western Cambodia. J Infect Dis. 2010, 201: 1326-1330. 10.1086/651562.PubMedCentralCrossRefPubMed Anderson TJ, Nair S, Nkhoma S, Williams JT, Imwong M, Yi P, Socheat D, Das D, Chotivanich K, Day NP, White NJ, Dondorp AM: High heritability of malaria parasite clearance rate indicates a genetic basis for artemisinin resistance in western Cambodia. J Infect Dis. 2010, 201: 1326-1330. 10.1086/651562.PubMedCentralCrossRefPubMed
42.
go back to reference Anderson TJ, Williams JT, Nair S, Sudimack D, Barends M, Jaidee A, Price RN, Nosten F: Inferred relatedness and heritability in malaria parasites. Proc R Soc Ser B. 2010, 277: 2531-2540. 10.1098/rspb.2010.0196.CrossRef Anderson TJ, Williams JT, Nair S, Sudimack D, Barends M, Jaidee A, Price RN, Nosten F: Inferred relatedness and heritability in malaria parasites. Proc R Soc Ser B. 2010, 277: 2531-2540. 10.1098/rspb.2010.0196.CrossRef
43.
go back to reference Nkhoma SC, Nair S, Cheeseman IH, Rohr-Allegrini C, Singlam S, Nosten F, Anderson TJ: Close kinship within multiple-genotype malaria parasite infections. Proc R Soc Ser B. 2012, 279: 2589-2598.CrossRef Nkhoma SC, Nair S, Cheeseman IH, Rohr-Allegrini C, Singlam S, Nosten F, Anderson TJ: Close kinship within multiple-genotype malaria parasite infections. Proc R Soc Ser B. 2012, 279: 2589-2598.CrossRef
44.
go back to reference Conway DJ, McBride JS: Genetic evidence for the importance of interrupted feeding by mosquitoes in the transmission of malaria. Trans R Soc Trop Med Hyg. 1991, 85: 454-456. 10.1016/0035-9203(91)90217-M.CrossRefPubMed Conway DJ, McBride JS: Genetic evidence for the importance of interrupted feeding by mosquitoes in the transmission of malaria. Trans R Soc Trop Med Hyg. 1991, 85: 454-456. 10.1016/0035-9203(91)90217-M.CrossRefPubMed
45.
go back to reference Conway DJ, McBride JS: Population genetics of Plasmodium falciparum within a malaria hyperendemic area. Parasitology. 1991, 103: 7-16. 10.1017/S0031182000059229.CrossRefPubMed Conway DJ, McBride JS: Population genetics of Plasmodium falciparum within a malaria hyperendemic area. Parasitology. 1991, 103: 7-16. 10.1017/S0031182000059229.CrossRefPubMed
46.
go back to reference Maynard-Smith J, Smith N, O'Rourke M, Spratt B: How clonal are bacteria?. Proc Natl Acad Sci USA. 1993, 90: 4384-4388. 10.1073/pnas.90.10.4384.CrossRef Maynard-Smith J, Smith N, O'Rourke M, Spratt B: How clonal are bacteria?. Proc Natl Acad Sci USA. 1993, 90: 4384-4388. 10.1073/pnas.90.10.4384.CrossRef
47.
go back to reference Razakandrainibe FG, Durand P, Koella JC, Meeüs TD, 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: 17388-17393. 10.1073/pnas.0508871102.PubMedCentralCrossRefPubMed Razakandrainibe FG, Durand P, Koella JC, Meeüs TD, 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: 17388-17393. 10.1073/pnas.0508871102.PubMedCentralCrossRefPubMed
48.
go back to reference Annan Z, Durand P, Ayala FJ, Arnathau C, Awono-Ambene P, Simard F, Razakandrainibe FG, Koella JC, Fontenille D, Renaud F: Population genetic structure of Plasmodium falciparum in the two main African vectors, Anopheles gambiae and Anopheles funestus. Proc Natl Acad Sci USA. 2007, 104: 7987-7992. 10.1073/pnas.0702715104.PubMedCentralCrossRefPubMed Annan Z, Durand P, Ayala FJ, Arnathau C, Awono-Ambene P, Simard F, Razakandrainibe FG, Koella JC, Fontenille D, Renaud F: Population genetic structure of Plasmodium falciparum in the two main African vectors, Anopheles gambiae and Anopheles funestus. Proc Natl Acad Sci USA. 2007, 104: 7987-7992. 10.1073/pnas.0702715104.PubMedCentralCrossRefPubMed
49.
go back to reference Anderson TJC, Paul REL, Donnelly CA, Day KP: Do malaria parasites mate non-randomly in the mosquito midgut?. Genet Res, Camb. 2000, 75: 285-296. 10.1017/S0016672300004481.CrossRef Anderson TJC, Paul REL, Donnelly CA, Day KP: Do malaria parasites mate non-randomly in the mosquito midgut?. Genet Res, Camb. 2000, 75: 285-296. 10.1017/S0016672300004481.CrossRef
50.
go back to reference Mzilahowa T, McCall PJ, Hastings IM: “Sexual” population structure and genetics of the malaria agent P. falciparum. PLoS One. 2007, 2: e613-10.1371/journal.pone.0000613.PubMedCentralCrossRefPubMed Mzilahowa T, McCall PJ, Hastings IM: “Sexual” population structure and genetics of the malaria agent P. falciparum. PLoS One. 2007, 2: e613-10.1371/journal.pone.0000613.PubMedCentralCrossRefPubMed
51.
go back to reference Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P, Teuscher T, Walliker D: Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology. 1994, 109: 413-421. 10.1017/S0031182000080665.CrossRefPubMed Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P, Teuscher T, Walliker D: Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology. 1994, 109: 413-421. 10.1017/S0031182000080665.CrossRefPubMed
52.
go back to reference Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, O'Brien J, Djimde A, Doumbo O, Zongo I, Ouedraogo J-B, Michon P, Mueller I, Siba P, Nzila A, Borrmann S, Kiara SM, Marsh K, Jiang H, Su X-Z, Amaratunga C, Fairhurst R, Socheat D, Nosten F, Imwong M, White NJ, Sanders M, Anastasi E, Alcock D, Drury E, Oyola S, Quail MA, Turner DJ, Ruano-Rubio V, Jyothi D, Amenga-Etego L, Hubbart C, Jeffreys A, Rowlands K, Sutherland C, Roper C, Mangano V, Modiano D, Tan JC, Ferdig MT, Amambua-Ngwa A, Conway DJ, Takala-Harrison S, Plowe CV, Rayner JC, Rockett KA, Clark TG, Newbold CI, Berriman M, MacInnis B, Kwiatkowski DP: Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature. 2012, 487: 375-379.PubMedCentralCrossRefPubMed Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, O'Brien J, Djimde A, Doumbo O, Zongo I, Ouedraogo J-B, Michon P, Mueller I, Siba P, Nzila A, Borrmann S, Kiara SM, Marsh K, Jiang H, Su X-Z, Amaratunga C, Fairhurst R, Socheat D, Nosten F, Imwong M, White NJ, Sanders M, Anastasi E, Alcock D, Drury E, Oyola S, Quail MA, Turner DJ, Ruano-Rubio V, Jyothi D, Amenga-Etego L, Hubbart C, Jeffreys A, Rowlands K, Sutherland C, Roper C, Mangano V, Modiano D, Tan JC, Ferdig MT, Amambua-Ngwa A, Conway DJ, Takala-Harrison S, Plowe CV, Rayner JC, Rockett KA, Clark TG, Newbold CI, Berriman M, MacInnis B, Kwiatkowski DP: Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature. 2012, 487: 375-379.PubMedCentralCrossRefPubMed
Metadata
Title
Population genetic structure of Plasmodium falciparum across a region of diverse endemicity in West Africa
Authors
Victor A Mobegi
Kovana M Loua
Ambroise D Ahouidi
Judith Satoguina
Davis C Nwakanma
Alfred Amambua-Ngwa
David J Conway
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2012
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-11-223

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