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Contrasting Transmission Dynamics of Co-endemic Plasmodium vivax and P. falciparum: Implications for Malaria Control and Elimination

DOI: 10.1371/journal.pntd.0003739

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Abstract:

Background Outside of Africa, P. falciparum and P. vivax usually coexist. In such co-endemic regions, successful malaria control programs have a greater impact on reducing falciparum malaria, resulting in P. vivax becoming the predominant species of infection. Adding to the challenges of elimination, the dormant liver stage complicates efforts to monitor the impact of ongoing interventions against P. vivax. We investigated molecular approaches to inform the respective transmission dynamics of P. falciparum and P. vivax and how these could help to prioritize public health interventions. Methodology/ Principal Findings Genotype data generated at 8 and 9 microsatellite loci were analysed in 168 P. falciparum and 166 P. vivax isolates, respectively, from four co-endemic sites in Indonesia (Bangka, Kalimantan, Sumba and West Timor). Measures of diversity, linkage disequilibrium (LD) and population structure were used to gauge the transmission dynamics of each species in each setting. Marked differences were observed in the diversity and population structure of P. vivax versus P. falciparum. In Bangka, Kalimantan and Timor, P. falciparum diversity was low, and LD patterns were consistent with unstable, epidemic transmission, amenable to targeted intervention. In contrast, P. vivax diversity was higher and transmission appeared more stable. Population differentiation was lower in P. vivax versus P. falciparum, suggesting that the hypnozoite reservoir might play an important role in sustaining local transmission and facilitating the spread of P. vivax infections in different endemic settings. P. vivax polyclonality varied with local endemicity, demonstrating potential utility in informing on transmission intensity in this species. Conclusions/ Significance Molecular approaches can provide important information on malaria transmission that is not readily available from traditional epidemiological measures. Elucidation of the transmission dynamics circulating in a given setting will have a major role in prioritising malaria control strategies, particularly against the relatively neglected non-falciparum species.

References

[1]  Guerra CA, Howes RE, Patil AP, Gething PW, Van Boeckel TP, et al. (2010) The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl Trop Dis 4: e774. doi: 10.1371/journal.pntd.0000774. pmid:20689816
[2]  Baird JK (2009) Severe and fatal vivax malaria challenges 'benign tertian malaria' dogma. Ann Trop Paediatr 29: 251–252. doi: 10.1179/027249309X12547917868808. pmid:19941746
[3]  Baird JK (2009) Resistance to therapies for infection by Plasmodium vivax. Clin Microbiol Rev 22: 508–534. doi: 10.1128/CMR.00008-09. pmid:19597012
[4]  Carlton JM, Sina BJ, Adams JH (2011) Why is Plasmodium vivax a neglected tropical disease? PLoS Negl Trop Dis 5: e1160. doi: 10.1371/journal.pntd.0001160. pmid:21738804
[5]  Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, et al. (2009) Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 9: 555–566. doi: 10.1016/S1473-3099(09)70177-X. pmid:19695492
[6]  Price RN, von Seidlein L, Valecha N, Nosten F, Baird JK, et al. (2014) Global extent of chloroquine-resistant Plasmodium vivax: a systematic review and meta-analysis. Lancet Infect Dis 14: 982–991. doi: 10.1016/S1473-3099(14)70855-2. pmid:25213732
[7]  Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, et al. (2008) Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Med 5: e128. doi: 10.1371/journal.pmed.0050128. pmid:18563962
[8]  Menard D, Barnadas C, Bouchier C, Henry-Halldin C, Gray LR, et al. (2010) Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci U S A 107: 5967–5971. doi: 10.1073/pnas.0912496107. pmid:20231434
[9]  Mendes C, Dias F, Figueiredo J, Mora VG, Cano J, et al. (2011) Duffy negative antigen is no longer a barrier to Plasmodium vivax—molecular evidences from the African West Coast (Angola and Equatorial Guinea). PLoS Negl Trop Dis 5: e1192. doi: 10.1371/journal.pntd.0001192. pmid:21713024
[10]  Ryan JR, Stoute JA, Amon J, Dunton RF, Mtalib R, et al. (2006) Evidence for transmission of Plasmodium vivax among a duffy antigen negative population in Western Kenya. Am J Trop Med Hyg 75: 575–581. pmid:17038676
[11]  Woldearegai TG, Kremsner PG, Kun JF, Mordmuller B (2013) Plasmodium vivax malaria in Duffy-negative individuals from Ethiopia. Trans R Soc Trop Med Hyg 107: 328–331. doi: 10.1093/trstmh/trt016. pmid:23584375
[12]  Cavasini CE, de Mattos LC, Couto AA, Couto VS, Gollino Y, et al. (2007) Duffy blood group gene polymorphisms among malaria vivax patients in four areas of the Brazilian Amazon region. Malar J 6: 167. pmid:18093292 doi: 10.1186/1475-2875-6-167
[13]  Feachem RG, Phillips AA, Hwang J, Cotter C, Wielgosz B, et al. (2010) Shrinking the malaria map: progress and prospects. Lancet 376: 1566–1578. doi: 10.1016/S0140-6736(10)61270-6. pmid:21035842
[14]  Hay SI, Smith DL, Snow RW (2008) Measuring malaria endemicity from intense to interrupted transmission. Lancet Infect Dis 8: 369–378. doi: 10.1016/S1473-3099(08)70069-0. pmid:18387849
[15]  Abdullah NR, Barber BE, William T, Norahmad NA, Satsu UR, et al. (2013) Plasmodium vivax population structure and transmission dynamics in Sabah Malaysia. PLoS One 8: e82553. doi: 10.1371/journal.pone.0082553. pmid:24358203
[16]  Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, et al. (2000) Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol 17: 1467–1482. pmid:11018154 doi: 10.1093/oxfordjournals.molbev.a026247
[17]  Anthony TG, Conway DJ, Cox-Singh J, Matusop A, Ratnam S, et al. (2005) Fragmented population structure of plasmodium falciparum in a region of declining endemicity. J Infect Dis 191: 1558–1564. pmid:15809916 doi: 10.1086/429338
[18]  Ferreira MU, Karunaweera ND, da Silva-Nunes M, da Silva NS, Wirth DF, et al. (2007) Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. J Infect Dis 195: 1218–1226. pmid:17357061 doi: 10.1086/512685
[19]  Gray KA, Dowd S, Bain L, Bobogare A, Wini L, et al. (2013) Population genetics of Plasmodium falciparum and Plasmodium vivax and asymptomatic malaria in Temotu Province, Solomon Islands. Malar J 12: 429. doi: 10.1186/1475-2875-12-429. pmid:24261646
[20]  Gunawardena S, Karunaweera ND, Ferreira MU, Phone-Kyaw M, Pollack RJ, et al. (2010) Geographic structure of Plasmodium vivax: microsatellite analysis of parasite populations from Sri Lanka, Myanmar, and Ethiopia. Am J Trop Med Hyg 82: 235–242. doi: 10.4269/ajtmh.2010.09-0588. pmid:20133999
[21]  Imwong M, Nair S, Pukrittayakamee S, Sudimack D, Williams JT, et al. (2007) Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. Int J Parasitol 37: 1013–1022. pmid:17442318 doi: 10.1016/j.ijpara.2007.02.010
[22]  Iwagami M, Fukumoto M, Hwang SY, Kim SH, Kho WG, et al. (2012) Population structure and transmission dynamics of Plasmodium vivax in the Republic of Korea based on microsatellite DNA analysis. PLoS Negl Trop Dis 6: e1592. doi: 10.1371/journal.pntd.0001592. pmid:22509416
[23]  Iwagami M, Rivera PT, Villacorte EA, Escueta AD, Hatabu T, et al. (2009) Genetic diversity and population structure of Plasmodium falciparum in the Philippines. Malar J 8: 96. doi: 10.1186/1475-2875-8-96. pmid:19422722
[24]  Koepfli C, Timinao L, Antao T, Barry AE, Siba P, et al. (2013) A Large Reservoir and Little Population Structure in the South Pacific. PLoS One 8: e66041. pmid:23823758 doi: 10.1371/journal.pone.0066041
[25]  Liu Y, Auburn S, Cao J, Trimarsanto H, Zhou H, et al. (2014) Genetic diversity and population structure of Plasmodium vivax in Central China. Malar J 13: 262. doi: 10.1186/1475-2875-13-262. pmid:25008859
[26]  Machado RL, Povoa MM, Calvosa VS, Ferreira MU, Rossit AR, et al. (2004) Genetic structure of Plasmodium falciparum populations in the Brazilian Amazon region. J Infect Dis 190: 1547–1555. pmid:15478058 doi: 10.1086/424601
[27]  Mobegi VA, Loua KM, Ahouidi AD, Satoguina J, Nwakanma DC, et al. (2012) Population genetic structure of Plasmodium falciparum across a region of diverse endemicity in West Africa. Malar J 11: 223. doi: 10.1186/1475-2875-11-223. pmid:22759447
[28]  Orjuela-Sanchez P, Sa JM, Brandi MC, Rodrigues PT, Bastos MS, et al. (2013) Higher microsatellite diversity in Plasmodium vivax than in sympatric Plasmodium falciparum populations in Pursat, Western Cambodia. Exp Parasitol 134: 318–326. doi: 10.1016/j.exppara.2013.03.029. pmid:23562882
[29]  Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, et al. (2009) Genetic diversity and population structure of Plasmodium falciparum in Thailand, a low transmission country. Malar J 8: 155. doi: 10.1186/1475-2875-8-155. pmid:19602241
[30]  Rebaudet S, Bogreau H, Silai R, Lepere JF, Bertaux L, et al. (2010) Genetic structure of Plasmodium falciparum and elimination of malaria, Comoros archipelago. Emerg Infect Dis 16: 1686–1694. doi: 10.3201/eid1611.100694. pmid:21029525
[31]  Rezende AM, Tarazona-Santos E, Couto AD, Fontes CJ, De Souza JM, et al. (2009) Analysis of genetic variability of Plasmodium vivax isolates from different Brazilian Amazon areas using tandem repeats. Am J Trop Med Hyg 80: 729–733. pmid:19407114
[32]  Schousboe ML, Ranjitkar S, Rajakaruna RS, Amerasinghe PH, Konradsen F, et al. (2014) Global and local genetic diversity at two microsatellite loci in Plasmodium vivax parasites from Asia, Africa and South America. Malar J 13: 392. doi: 10.1186/1475-2875-13-392. pmid:25277367
[33]  Van den Eede P, Erhart A, Van der Auwera G, Van Overmeir C, Thang ND, et al. (2010) High complexity of Plasmodium vivax infections in symptomatic patients from a rural community in central Vietnam detected by microsatellite genotyping. Am J Trop Med Hyg 82: 223–227. doi: 10.4269/ajtmh.2010.09-0458. pmid:20133996
[34]  Van den Eede P, Van der Auwera G, Delgado C, Huyse T, Soto-Calle VE, et al. (2010) Multilocus genotyping reveals high heterogeneity and strong local population structure of the Plasmodium vivax population in the Peruvian Amazon. Malar J 9: 151. doi: 10.1186/1475-2875-9-151. pmid:20525233
[35]  Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, et al. (2010) 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 9: 336. doi: 10.1186/1475-2875-9-336. pmid:21092231
[36]  Arnott A, Barry AE, Reeder JC (2012) Understanding the population genetics of Plasmodium vivax is essential for malaria control and elimination. Malar J 11: 14. doi: 10.1186/1475-2875-11-14. pmid:22233585
[37]  World Health Organization (2013) World Malaria Report 2013. World Health Organization; Geneva 2013.
[38]  Ratcliff A, Siswantoro H, Kenangalem E, Wuwung M, Brockman A, et al. (2007) Therapeutic response of multidrug-resistant Plasmodium falciparum and P. vivax to chloroquine and sulfadoxine-pyrimethamine in southern Papua, Indonesia. Trans R Soc Trop Med Hyg 101: 351–359. pmid:17028048 doi: 10.1016/j.trstmh.2006.06.008
[39]  Sumawinata IW, Bernadeta , Leksana B, Sutamihardja A, Purnomo , et al. (2003) Very high risk of therapeutic failure with chloroquine for uncomplicated Plasmodium falciparum and P. vivax malaria in Indonesian Papua. Am J Trop Med Hyg 68: 416–420. pmid:12875290
[40]  Elyazar IR, Hay SI, Baird JK (2011) Malaria distribution, prevalence, drug resistance and control in Indonesia. Adv Parasitol 74: 41–175. doi: 10.1016/B978-0-12-385897-9.00002-1. pmid:21295677
[41]  Sulistyaningsih E, Fitri LE, Loscher T, Berens-Riha N (2010) Diagnostic difficulties with Plasmodium knowlesi infection in humans. Emerg Infect Dis 16: 1033–1034. doi: 10.3201/eid1606.100022. pmid:20507769
[42]  Figtree M, Lee R, Bain L, Kennedy T, Mackertich S, et al. (2010) Plasmodium knowlesi in human, Indonesian Borneo. Emerg Infect Dis 16: 672–674. doi: 10.3201/eid1604.091624. pmid:20350383
[43]  Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T, et al. (2012) A global map of dominant malaria vectors. Parasit Vectors 5: 69. doi: 10.1186/1756-3305-5-69. pmid:22475528
[44]  Malaria Atlas Project website.
[45]  Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IR, et al. (2011) A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J 10: 378. doi: 10.1186/1475-2875-10-378. pmid:22185615
[46]  Gething PW, Elyazar IR, Moyes CL, Smith DL, Battle KE, et al. (2012) A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis 6: e1814. doi: 10.1371/journal.pntd.0001814. pmid:22970336
[47]  Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN (1993) Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol 58: 283–292. pmid:8479452 doi: 10.1016/0166-6851(93)90050-8
[48]  Boonma P, Christensen PR, Suwanarusk R, Price RN, Russell B, et al. (2007) Comparison of three molecular methods for the detection and speciation of Plasmodium vivax and Plasmodium falciparum. Malar J 6: 124. pmid:17868467 doi: 10.1186/1475-2875-6-124
[49]  Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP (1999) Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology 119 (Pt 2): 113–125. pmid:10466118 doi: 10.1017/s0031182099004552
[50]  Karunaweera ND, Ferreira MU, Munasinghe A, Barnwell JW, Collins WE, et al. (2008) Extensive microsatellite diversity in the human malaria parasite Plasmodium vivax. Gene 410: 105–112. doi: 10.1016/j.gene.2007.11.022. pmid:18226474
[51]  Koepfli C, Mueller I, Marfurt J, Goroti M, Sie A, et al. (2009) Evaluation of Plasmodium vivax genotyping markers for molecular monitoring in clinical trials. J Infect Dis 199: 1074–1080. doi: 10.1086/597303. pmid:19275476
[52]  Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564–567. doi: 10.1111/j.1755-0998.2010.02847.x. pmid:21565059
[53]  Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59: 1633–1638. pmid:16329237 doi: 10.1111/j.0014-3820.2005.tb01814.x
[54]  Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959. pmid:10835412
[55]  Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611–2620. pmid:15969739 doi: 10.1111/j.1365-294x.2005.02553.x
[56]  Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Molecular Ecology Notes 4: 137–138. doi: 10.1046/j.1471-8286.2003.00566.x
[57]  Haubold B, Hudson RR (2000) LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage Analysis. Bioinformatics 16: 847–848. pmid:11108709 doi: 10.1093/bioinformatics/16.9.847
[58]  Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, et al. (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368: 455–457. pmid:7510853 doi: 10.1038/368455a0
[59]  Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425. pmid:3447015
[60]  Paradis E, Claude J, Strimmer K (2004) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20: 289–290. pmid:14734327 doi: 10.1093/bioinformatics/btg412
[61]  Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22: 1–20.
[62]  Amodu OK, Oyedeji SI, Ntoumi F, Orimadegun AE, Gbadegesin RA, et al. (2008) Complexity of the msp2 locus and the severity of childhood malaria, in south-western Nigeria. Ann Trop Med Parasitol 102: 95–102. doi: 10.1179/136485908X252340. pmid:18318931
[63]  Beck HP, Felger I, Huber W, Steiger S, Smith T, et al. (1997) Analysis of multiple Plasmodium falciparum infections in Tanzanian children during the phase III trial of the malaria vaccine SPf66. J Infect Dis 175: 921–926. pmid:9086150 doi: 10.1086/513991
[64]  Kyes S, Harding R, Black G, Craig A, Peshu N, et al. (1997) Limited spatial clustering of individual Plasmodium falciparum alleles in field isolates from coastal Kenya. Am J Trop Med Hyg 57: 205–215. pmid:9288818
[65]  Roper C, Richardson W, Elhassan IM, Giha H, Hviid L, et al. (1998) Seasonal changes in the Plasmodium falciparum population in individuals and their relationship to clinical malaria: a longitudinal study in a Sudanese village. Parasitology 116 (Pt 6): 501–510. pmid:9651932 doi: 10.1017/s0031182098002650
[66]  Zwetyenga J, Rogier C, Tall A, Fontenille D, Snounou G, et al. (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. pmid:9840589
[67]  Gunawardena S, Ferreira MU, Kapilananda GM, Wirth DF, Karunaweera ND (2014) The Sri Lankan paradox: high genetic diversity in Plasmodium vivax populations despite decreasing levels of malaria transmission. Parasitology 141: 880–890. doi: 10.1017/S0031182013002278. pmid:24533989
[68]  Price RN, Auburn S, Marfurt J, Cheng Q (2012) Phenotypic and genotypic characterisation of drug-resistant Plasmodium vivax. Trends Parasitol 28: 522–529. doi: 10.1016/j.pt.2012.08.005. pmid:23044287

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