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

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Mobegi, Victor A ^a,b   Loua, Kovana M ^c   Ahouidi, Ambroise D ^d   Satoguina, Judith ^b   Nwakanma, Davis C ^b   Amambua Ngwa, Alfred ^b   Conway, David J ^a,b  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

^c National Institute of Public Health   (Guinea)

^d UNIVERSITÉ CHEIKH ANTA DIOP   (Senegal)

Author keywords

Microsatellite; Plasmodium falciparum; Population structure; Transmission intensity

Indexed keywords

MICROSATELLITE DNA;

ARTICLE; CONTROLLED STUDY; DISEASE TRANSMISSION; ENDEMIC DISEASE; EPIDEMIC; GAMBIA; GENETIC VARIABILITY; GENOTYPE; GUINEA; GUINEA-BISSAU; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; NAMIBIA; PLASMODIUM FALCIPARUM; POLYMORPHIC LOCUS; POPULATION GENETIC STRUCTURE; SENEGAL;

AFRICA, WESTERN; ENDEMIC DISEASES; GENETIC VARIATION; GENOTYPE; HUMANS; MALARIA, FALCIPARUM; MICROSATELLITE REPEATS; PLASMODIUM FALCIPARUM;

EID: 84865267218     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-223     Document Type: Article

References (52)

1. The global distribution of clinical episodes of Plasmodium falciparum malaria. Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI, Nature 2005 434 214 217 10.1038/nature03342 15759000 (Pubitemid 40388051)
2. WHO, World Malaria Report World Health Organization, Geneva 2010 http://www.who.int/malaria/world-malaria-report-2010/en/
3. Global malaria mortality between 1980 and 2010: a systematic analysis. Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD, Lancet 2012 379 413 431 10.1016/S0140-6736(12) 60034-8 22305225
4. Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: literature survey, Internet access and review. Hay S, Rogers D, Toomer J, Snow R, Trans R Soc Trop Med Hyg 2000 94 113 127 10.1016/S0035-9203(00)90246- 3 10897348
5. A world malaria map: Plasmodium falciparum endemicity in 2007. 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, PLoS Med 2009 6 1000048 19323591
6. Recombination hotspots and population structure in Plasmodium falciparum. Mu J, Awadalla P, Duan J, McGee KM, Joy DA, McVean GA, Su X-Z, PLoS Biol 2005 3 335 10.1371/journal.pbio.0030335 16144426 (Pubitemid 41437139)
7. Mating patterns in malaria parasite populations of Papua New Guinea. Paul REL, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, Paru R, Day KP, Science 1995 269 1709 1711 10.1126/science.7569897 7569897 (Pubitemid 26449518)
8. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. 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, Mol Biol Evol 2000 17 1467 1482 10.1093/oxfordjournals.molbev.a026247 11018154
9. Genetic structure of Plasmodium falciparum populations in the Brazilian Amazon region. Machado RLD, Pávoa MM, Calvosa VSP, Ferreira MU, Rossit ARB, dos Santos EJM, Conway DJ, J Infect Dis 2004 190 1547 1555 10.1086/424601 15478058 (Pubitemid 39411002)
10. Fragmented population structure of Plasmodium falciparum in a region of declining endemicity. Anthony T, Conway D, Cox-Singh J, Matusop A, Ratnam S, Shamsul S, Singh B, J Infect Dis 2005 191 1558 1564 10.1086/429338 15809916 (Pubitemid 40563369)
11. Case-control approach to identify Plasmodium falciparum polymorphisms associated with severe malaria. Chokejindachai W, Conway DJ, PLoS One 2009 4 5454 10.1371/journal.pone.0005454 19421327
12. Genetic diversity and population structure of Plasmodium falciparum in Thailand, a low transmission country. Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, Sitthi-Amorn C, Renaud F, Harnyuttanakorn P, Malar J 2009 8 155 10.1186/1475-2875-8-155 19602241
13. Genetic diversity and population structure of Plasmodium falciparum in the Philippines. Iwagami M, Rivera P, Villacorte E, Escueta A, Hatabu T, Kawazu S-, Hayakawa T, Tanabe K, Kano S, Malar J 2009 8 96 10.1186/1475-2875-8-96 19422722
14. Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, Nale J, Kiniboro B, Buckee CO, Tavul L, Siba PM, Reeder JC, Barry AE, Malar J 2010 9 336 10.1186/1475-2875-9-336 21092231
15. High recombination rate in natural populations of Plasmodium falciparum. Conway DJ, Roper C, Oduola AMJ, Arnot DE, Kremsner PG, Grobusch MP, Curtis CF, Greenwood BM, Proc Natl Acad Sci USA 1999 96 4506 4511 10.1073/pnas.96.8.4506 10200292 (Pubitemid 29190366)
16. Extreme geographical fixation of variation in the Plasmodium falciparum gamete surface protein gene Pfs48/45 compared with microsatellite loci. Conway DJ, Machado RLD, Singh B, Dessert P, Mikes ZS, Povoa MM, Oduola AMJ, Roper C, Mol Biochem Parasitol 2001 115 145 156 10.1016/S0166-6851(01)00278-X 11420101 (Pubitemid 32566224)
17. The transit phase of migration: circulation of malaria and its multidrug-resistant forms in Africa. Lynch C, Roper C, PLoS Med 2011 8 1001040 10.1371/journal.pmed.1001040 21655316
18. Genetic diversity and structure of African Plasmodium falciparum populations in Urban and Rural areas. 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, Am J Trop Med Hyg 2006 74 953 959 16760503 (Pubitemid 351627399)
19. Genetic Structure of Plasmodium falciparum and Elimination of Malaria, Comoros Archipelago. Rebaudet S, Bogreau H, Sila R, Lepère J-F, Bertaux L, Pradines B, Delmont J, Parola P, Rogier C, Emerg Infect Dis 2010 16 1686 1694 21029525
20. Changes in the burden of malaria in sub-Saharan Africa. O'Meara WP, Mangeni JN, Steketee R, Greenwood B, Lancet Infect Dis 2010 10 545 555 10.1016/S1473-3099(10)70096-7 20637696
21. Continued decline of malaria in The Gambia with implications for elimination. 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, PLoS One 2010 5 12242 10.1371/journal.pone.0012242 20805878
22. Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. 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, Lancet 2008 372 1545 1554 10.1016/S0140-6736(08)61654-2 18984187
23. New malaria-control policies and child mortality in Senegal: reaching Millennium Development Goal 4. Trape JF, Sauvage C, Ndiaye O, Douillot L, Marra A, Diallo A, Cisse B, Greenwood B, Milligan P, Sokhna C, Molez JF, J Infect Dis 2012 205 672 679 10.1093/infdis/jir805 22238469
24. Comparison of surveillance methods applied to a situation of low malaria prevalence at rural sites in The Gambia and Guinea Bissau. Satoguina J, Walther B, Drakeley C, Nwakanma D, Oriero E, Correa S, Corran P, Conway D, Walther M, Malar J 2009 8 274 10.1186/1475-2875-8-274 19954532
25. Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. 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, PLoS Pathog 2009 5 1000364 10.1371/journal.ppat.1000364 19343213
26. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah M, Rahman H, Am J Trop Med Hyg 1999 60 687 692 10348249 (Pubitemid 29233131)
27. Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Anderson T, Su X, Bockarie M, Lagog M, Day K, Parasitology 1999 119 113 125 10.1017/S0031182099004552 10466118 (Pubitemid 29381128)
28. Toward a high-resolution Plasmodium falciparum linkage map: Polymorphic markers from hundreds of simple sequence repeats. Su X-Z, Wellems TE, Genomics 1996 33 430 444 10.1006/geno.1996.0218 8661002 (Pubitemid 26159859)
29. FSTAT (version 1.2): a computer program to calculate F statistics. Goudet J, J Hered 1995 86 485 486
30. Application of phylogenetic networks in evolutionary studies. Huson DH, Bryant D, Mol Biol Evol 2006 23 254 267 16221896 (Pubitemid 43100040)
31. LIAN 3.0: detecting linkage disequilibrium in multilocus data. Haubold B, Hudson RR, Bioinformatics 2000 16 847 849 10.1093/bioinformatics/16.9.847 11108709
32. Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Rousset F, Mol Ecol Resources 2008 8 103 106 10.1111/j.1471-8286.2007.01931.x (Pubitemid 350231212)
33. Significant linkage disequilibrium and high genetic diversity in a population of Plasmodium falciparum from an area (Republic of The Congo) highly endemic for malaria. Durand P, Michalakis Y, Cestier S, Oury B, LeClerc MC, Tibayrenc M, Renaud F, Am J Trop Med Hyg 2003 68 345 349 12685643 (Pubitemid 38240526)
34. Plasmodium falciparum genetic diversity in western Kenya highlands. Zhong D, Afrane Y, Githeko A, Yang Z, Cui L, Menge D, Temu E, Yan G, Am J Trop Med Hyg 2007 77 1043 1050 18165519 (Pubitemid 351837790)
35. Complexity of the msp2 locus and the severity of childhood malaria, in south-western Nigeria. Amodu OK, Oyedeji SI, Ntoumi F, Orimadegun AE, Gbadegesin RA, Olumese PE, Omotade OO, Ann Trop Med Parasitol 2008 102 95 102 10.1179/136485908X252340 18318931 (Pubitemid 351767937)
36. Analysis of multiple Plasmodium falciparum infections in Tanzanian children during the phase III trial of the malaria vaccine SPf66. Beck HP, Felger I, Huber W, Steiger S, Smith T, Weiss N, Alonso P, Tanner M, J Infect Dis 1997 175 921 926 10.1086/513991 9086150 (Pubitemid 27142968)
37. Limited spatial clustering of individual Plasmodium falciparum alleles in field isolates from coastal Kenya. Kyes S, Harding R, Black G, Craig A, Peshu N, Newbold C, Marsh K, Am J Trop Med Hyg 1997 57 205 215 9288818 (Pubitemid 27360615)
38. Seasonal changes in the Plasmodium falciparum population in individuals and their relationship to clinical malaria: a longitudinal study in a Sudanese village. Roper C, Richardson W, Elhassan IM, Giha H, Hviid L, Satti GMH, Theander TG, Arnot DE, Parasitology 1998 116 501 510 10.1017/S0031182098002650 9651932 (Pubitemid 28269379)
39. No influence of age on infection complexity and allelic distribution in Plasmodium falciparum infections in Ndiop, a Senegalese village with seasonal, mesoendemic malaria. Zwetyenga J, Rogier C, Tall A, Fontenille D, Snounou G, Trape JF, Mercereau-Puijalon O, Am J Trop Med Hyg 1998 59 726 735 9840589 (Pubitemid 28524529)
40. Plasmodium falciparum: malaria morbidity is associated with specific merozoite surface antigen 2 genotypes. Engelbrecht F, Felger I, Genton B, Alpers M, Beck H-P, Exp Parasitol 1995 81 90 96 10.1006/expr.1995.1096 7628572
41. High heritability of malaria parasite clearance rate indicates a genetic basis for artemisinin resistance in western Cambodia. Anderson TJ, Nair S, Nkhoma S, Williams JT, Imwong M, Yi P, Socheat D, Das D, Chotivanich K, Day NP, White NJ, Dondorp AM, J Infect Dis 2010 201 1326 1330 10.1086/651562 20350192
42. Inferred relatedness and heritability in malaria parasites. Anderson TJ, Williams JT, Nair S, Sudimack D, Barends M, Jaidee A, Price RN, Nosten F, Proc R Soc Ser B 2010 277 2531 2540 10.1098/rspb.2010.0196
43. Close kinship within multiple-genotype malaria parasite infections. Nkhoma SC, Nair S, Cheeseman IH, Rohr-Allegrini C, Singlam S, Nosten F, Anderson TJ, Proc R Soc Ser B 2012 279 2589 2598
44. Genetic evidence for the importance of interrupted feeding by mosquitoes in the transmission of malaria. Conway DJ, McBride JS, Trans R Soc Trop Med Hyg 1991 85 454 456 10.1016/0035-9203(91)90217-M 1755049
45. Population genetics of Plasmodium falciparum within a malaria hyperendemic area. Conway DJ, McBride JS, Parasitology 1991 103 7 16 10.1017/S0031182000059229 1719468
46. How clonal are bacteria? Maynard-Smith J, Smith N, O'Rourke M, Spratt B, Proc Natl Acad Sci USA 1993 90 4384 4388 10.1073/pnas.90.10.4384 8506277 (Pubitemid 23148908)
47. Clonal population structure of the malaria agent Plasmodium falciparum in high-infection regions. Razakandrainibe FG, Durand P, Koella JC, Meeüs TD, Rousset F, Ayala FJ, Renaud F, Proc Natl Acad Sci USA 2005 102 17388 17393 10.1073/pnas.0508871102 16301534 (Pubitemid 41740876)
48. Population genetic structure of Plasmodium falciparum in the two main African vectors, Anopheles gambiae and Anopheles funestus. Annan Z, Durand P, Ayala FJ, Arnathau C, Awono-Ambene P, Simard F, Razakandrainibe FG, Koella JC, Fontenille D, Renaud F, Proc Natl Acad Sci USA 2007 104 7987 7992 10.1073/pnas.0702715104 17470800 (Pubitemid 47185863)
49. Do malaria parasites mate non-randomly in the mosquito midgut? Anderson TJC, Paul REL, Donnelly CA, Day KP, Genet Res, Camb 2000 75 285 296 10.1017/S0016672300004481 (Pubitemid 30398384)
50. Sexual population structure and genetics of the malaria agent P. falciparum. Mzilahowa T, McCall PJ, Hastings IM, PLoS One 2007 2 613 10.1371/journal.pone.0000613 17637829 (Pubitemid 351308739)
51. Random mating in a natural population of the malaria parasite Plasmodium falciparum. Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P, Teuscher T, Walliker D, Parasitology 1994 109 413 421 10.1017/S0031182000080665 7800409 (Pubitemid 24327391)
52. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. 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, Nature 2012 487 375 379 22722859