1921
Volume 96, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract

and have varying transmission dynamics that are informed by molecular epidemiology. This study aimed to determine the complexity of infection and genetic diversity of and throughout Papua New Guinea (PNG) to evaluate transmission dynamics across the country. In 2008–2009, a nationwide malaria indicator survey collected 8,936 samples from all 16 endemic provinces of PNG. Of these, 892 positive samples were genotyped at and , and 758 positive samples were genotyped at . The data were analyzed for multiplicity of infection (MOI) and genetic diversity. Overall, had higher polyclonality (71%) and mean MOI (2.32) than (20%, 1.39). These measures were significantly associated with prevalence for but not for . The genetic diversity of (: expected heterozygosity = 0.95, 0.85–0.98; : 0.78, 0.66–0.89) was higher and less variable than that of (: 0.89, 0.65–0.97). Significant associations of MOI with allelic richness (rho = 0.69, = 0.009) and expected heterozygosity (rho = 0.87, < 0.001) were observed for . Conversely, genetic diversity was not correlated with polyclonality nor mean MOI for . The results demonstrate higher complexity of infection and genetic diversity of across the country. Although shows a strong association of these parameters with prevalence, a lack of association was observed for and is consistent with higher potential for outcrossing of this species.

Loading

Article metrics loading...

The graphs shown below represent data from March 2017
/content/journals/10.4269/ajtmh.16-0716
2017-03-08
2019-01-16
Loading full text...

Full text loading...

/deliver/fulltext/14761645/96/3/630.html?itemId=/content/journals/10.4269/ajtmh.16-0716&mimeType=html&fmt=ahah

References

  1. Carlton JM, Das A, Escalante AA, , 2013. Genomics, population genetics and evolutionary history of Plasmodium vivax . Adv Parasitol 81: 203222.[Crossref] [Google Scholar]
  2. WHO, 2015. World Malaria Report. Available at: http://www.who.int/malaria/publications/world-malaria-report-2015/report/en/. Accessed December 2015. [Google Scholar]
  3. Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, Alonso PL, del Portillo HA, , 2009. Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 9: 555566.[Crossref] [Google Scholar]
  4. Guerra CA, Howes RE, Patil AP, Gething PW, Van Boeckel TP, Temperley WH, Kabaria CW, Tatem AJ, Manh BH, Elyazar IR, Baird JK, Snow RW, Hay SI, , 2010. The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl Trop Dis 4: e774.[Crossref] [Google Scholar]
  5. Vivax Working Group, 2015. Targeting vivax malaria in the Asia Pacific: the Asia Pacific Malaria Elimination Network Vivax Working Group. Malar J 14: 484.[Crossref] [Google Scholar]
  6. Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM, , 2007. Vivax malaria: neglected and not benign. Am J Trop Med Hyg 77: 7987. [Google Scholar]
  7. Noulin F, Borlon C, Van Den Abbeele J, D'Alessandro U, Erhart A, , 2013. 1912–2012: a century of research on Plasmodium vivax in vitro culture. Trends Parasitol 29: 286294.[Crossref] [Google Scholar]
  8. Battle KE, Gething PW, Elyazar IR, Moyes CL, Sinka ME, Howes RE, Guerra CA, Price RN, Baird KJ, Hay SI, , 2012. The global public health significance of Plasmodium vivax . Adv Parasitol 80: 1111.[Crossref] [Google Scholar]
  9. Shanks GD, , 2012. Control and elimination of Plasmodium vivax . Adv Parasitol 80: 301341.[Crossref] [Google Scholar]
  10. Arez AP, Pinto J, Palsson K, Snounou G, Jaenson TG, do Rosario VE, , 2003. Transmission of mixed Plasmodium species and Plasmodium falciparum genotypes. Am J Trop Med Hyg 68: 161168. [Google Scholar]
  11. Juliano JJ, Porter K, Mwapasa V, Sem R, Rogers WO, Ariey F, Wongsrichanalai C, Read A, Meshnick SR, , 2010. Exposing malaria in-host diversity and estimating population diversity by capture-recapture using massively parallel pyrosequencing. Proc Natl Acad Sci USA 107: 2013820143.[Crossref] [Google Scholar]
  12. Taylor LH, Walliker D, Read AF, , 1997. Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones. Proc Biol Sci 264: 927935.[Crossref] [Google Scholar]
  13. Roode JC, Pansini R, Cheesman SJ, Helinski ME, Huijben S, Wargo AR, , 2005. Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci USA 102: 76247628.[Crossref] [Google Scholar]
  14. de Roode JC, Helinski MEH, Anwar MA, Read AF, , 2005. Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am Nat 166: 531542. [Google Scholar]
  15. Taylor LH, Read AF, , 1998. Determinants of transmission success of individual clones from mixed-clone infections of the rodent malaria parasite, Plasmodium chabaudi . Int J Parasitol 28: 719725.[Crossref] [Google Scholar]
  16. Price RN, von Seidlein L, Valecha N, Nosten F, Baird JK, White NJ, , 2014. Global extent of chloroquine-resistant Plasmodium vivax: a systematic review and meta-analysis. Lancet Infect Dis 14: 982991.[Crossref] [Google Scholar]
  17. Lee SA, Yeka A, Nsobya SL, Dokomajilar C, Rosenthal PJ, Talisuna A, Dorsey G, , 2006. Complexity of Plasmodium falciparum infections and antimalarial drug efficacy at 7 sites in Uganda. J Infect Dis 193: 11601163.[Crossref] [Google Scholar]
  18. Nkhoma SC, Nair S, Al-Saai S, Ashley E, McGready R, Phyo AP, , 2013. Population genetic correlates of declining transmission in a human pathogen. Mol Ecol 22: 273285.[Crossref] [Google Scholar]
  19. Escalante AA, Ferreira MU, Vinetz JM, Volkman SK, Cui L, Gamboa D, Krogstad DJ, Barry AE, Carlton JM, van Eijk AM, Pradhan K, Mueller I, Greenhouse B, Pacheco MA, Vallejo AF, Herrera S, Felger I, , 2015. Malaria molecular epidemiology: lessons from the international centers of excellence for malaria research network. Am J Trop Med Hyg 93 (Suppl 3): 7986.[Crossref] [Google Scholar]
  20. Bousema T, Drakeley C, , 2011. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev 24: 377410.[Crossref] [Google Scholar]
  21. Cui L, Mascorro CN, Fan Q, Rzomp KA, Khuntirat B, Zhou G, Chen H, Yan G, Sattabongkot J, , 2003. Genetic diversity and multiple infections of Plasmodium vivax malaria in western Thailand. Am J Trop Med Hyg 68: 613619. [Google Scholar]
  22. 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: 880890.[Crossref] [Google Scholar]
  23. Barry AE, Waltmann A, Koepfli C, Barnadas C, Mueller I, , 2015. Uncovering the transmission dynamics of Plasmodium vivax using population genetics. Pathog Glob Health 109: 142152.[Crossref] [Google Scholar]
  24. Müller I, Bockarie M, Alpers M, Smith T, , 2003. The epidemiology of malaria in Papua New Guinea. Trends Parasitol 19: 253259.[Crossref] [Google Scholar]
  25. Kazura JW, Siba PM, Betuela I, Mueller I, , 2012. Research challenges and gaps in malaria knowledge in Papua New Guinea. Acta Trop 121: 274280.[Crossref] [Google Scholar]
  26. Genton B, al-Yaman F, Beck HP, Hii J, Mellor S, Rare L, Ginny M, Smith T, Alpers MP, , 1995. The epidemiology of malaria in the Wosera area, East Sepik Province, Papua New Guinea, in preparation for vaccine trials. II. Mortality and morbidity. Ann Trop Med Parasitol 89: 377390.[Crossref] [Google Scholar]
  27. Betuela I, Maraga S, Hetzel MW, Tandrapah T, Sie A, Yala S, Kundi J, Siba P, Reeder JC, Mueller I, , 2012. Epidemiology of malaria in the Papua New Guinean highlands. Trop Med Int Health 17: 11811191.[Crossref] [Google Scholar]
  28. Bruce MC, Galinski MR, Barnwell JW, Donnelly CA, Walmsley M, Alpers MP, Walliker D, Day KP, , 2000. Genetic diversity and dynamics of Plasmodium falciparum and P. vivax populations in multiply infected children with asymptomatic malaria infections in Papua New Guinea. Parasitology 121: 257272.[Crossref] [Google Scholar]
  29. Hetzel MW, Gideon G, Lote N, Makita L, Siba PM, Mueller I, , 2012. Ownership and usage of mosquito nets after four years of large-scale free distribution in Papua New Guinea. Malar J 11: 192.[Crossref] [Google Scholar]
  30. Hetzel MW, Morris H, Tarongka N, Barnadas C, Pulford J, Makita L, Siba PM, Mueller I, , 2015. Prevalence of malaria across Papua New Guinea after initial roll-out of insecticide-treated mosquito nets. Trop Med Int Health 20: 17451755.[Crossref] [Google Scholar]
  31. Gray KA, Dowd S, Bain L, Bobogare A, Wini L, Shanks GD, Cheng Q, , 2013. Population genetics of Plasmodium falciparum and Plasmodium vivax and asymptomatic malaria in Temotu Province, Solomon Islands. Malar J 12: 429.[Crossref] [Google Scholar]
  32. Neafsey DE, Galinsky K, Jiang RH, Young L, Sykes SM, Saif S, Gujja S, Goldberg JM, Young S, Zeng Q, Chapman SB, Dash AP, Anvikar AR, Sutton PL, Birren BW, Escalante AA, Barnwell JW, Carlton JM, , 2012. The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum . Nat Genet 44: 10461050.[Crossref] [Google Scholar]
  33. Noviyanti R, Coutrier F, Utami RA, Trimarsanto H, Tirta YK, Trianty L, Kusuma A, Sutanto I, Kosasih A, Kusriastuti R, Hawley WA, Laihad F, Lobo N, Marfurt J, Clark TG, Price RN, Auburn S, , 2015. Contrasting transmission dynamics of co-endemic Plasmodium vivax and P. falciparum: implications for malaria control and elimination. PLoS Negl Trop Dis 9: e0003739.[Crossref] [Google Scholar]
  34. Joy DA, Mu J, Jiang H, Su X, , 2006. Genetic diversity and population history of Plasmodium falciparum and Plasmodium vivax . Parassitologia 48: 561566. [Google Scholar]
  35. Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK, , 2012. Genotype comparison of Plasmodium vivax and Plasmodium falciparum clones from pregnant and non-pregnant populations in north-west Colombia. Malar J 11: 18.[Crossref] [Google Scholar]
  36. Lopez AC, Ortiz A, Coello J, Sosa-Ochoa W, Torres REM, Banegas EI, Jovel I, Fontecha GA, , 2012. Genetic diversity of Plasmodium vivax and Plasmodium falciparum in Honduras. Malar J 11: 391.[Crossref] [Google Scholar]
  37. Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, Nale J, Kiniboro B, Buckee CO, Tavul L, Siba PM, Reeder JC, Barry AE, , 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.[Crossref] [Google Scholar]
  38. Arnott A, Wapling J, Mueller I, Ramsland PA, Siba PM, Reeder JC, Barry AE, , 2014. Distinct patterns of diversity, population structure and evolution in the AMA1 genes of sympatric Plasmodium falciparum and Plasmodium vivax populations of Papua New Guinea from an area of similarly high transmission. Malar J 13: 233.[Crossref] [Google Scholar]
  39. Koepfli C, Ross A, Kiniboro B, Smith TA, Zimmerman PA, Siba P, Mueller I, Felger I, , 2011. Multiplicity and diversity of Plasmodium vivax infections in a highly endemic region in Papua New Guinea. PLoS Negl Trop Dis 5: e1424.[Crossref] [Google Scholar]
  40. Koepfli C, Timinao L, Antao T, Barry AE, Siba P, Mueller I, Felger I, , 2013. A large reservoir and little population structure in the south Pacific. PLoS One 8: e66041.[Crossref] [Google Scholar]
  41. Jennison C, Arnott A, Tessier N, Tavul L, Koepfli C, Felger I, Siba PM, Reeder JC, Bahlo M, Mueller I, Barry AE, , 2015. Plasmodium vivax populations are more genetically diverse and less structured than sympatric Plasmodium falciparum populations. PLoS Negl Trop Dis 9: e0003634.[Crossref] [Google Scholar]
  42. Arnott A, Barnadas C, Senn N, Siba P, Mueller I, Reeder JC, Barry AE, , 2013. High genetic diversity of Plasmodium vivax on the north coast of Papua New Guinea. Am J Trop Med Hyg 89: 188194.[Crossref] [Google Scholar]
  43. McNamara DT, Kasehagen LJ, Grimberg BT, Cole-Tobian J, Collins WE, Zimmerman PA, , 2006. Diagnosing infection levels of four human malaria parasite species by a polymerase chain reaction/ligase detection reaction fluorescent microsphere-based assay. Am J Trop Med Hyg 74: 413421. [Google Scholar]
  44. Koepfli C, Mueller I, Marfurt J, Goroti M, Sie A, Oa O, Genton B, Beck HP, Felger I, , 2009. Evaluation of Plasmodium vivax genotyping markers for molecular monitoring in clinical trials. J Infect Dis 199: 10741080.[Crossref] [Google Scholar]
  45. Falk N, Maire N, Sama W, Owusu-Agyei S, Smith T, Beck HP, Felger I, , 2006. Comparison of PCR-RFLP and Genescan-based genotyping for analyzing infection dynamics of Plasmodium falciparum . Am J Trop Med Hyg 74: 944950. [Google Scholar]
  46. Smith DL, Guerra CA, Snow RW, Hay SI, , 2007. Standardizing estimates of the Plasmodium falciparum parasite rate. Malar J 6: 131.[Crossref] [Google Scholar]
  47. Goudet J, , 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86: 485486.[Crossref] [Google Scholar]
  48. Hurlbert SH, , 1971. The nonconcept of species diversity: a critique and alternative parameters. Ecology 52: 577586.[Crossref] [Google Scholar]
  49. Barry AE, Schultz L, Senn N, Nale J, Kiniboro B, Siba PM, Mueller I, Reeder JC, , 2013. High levels of genetic diversity of Plasmodium falciparum populations in Papua New Guinea despite variable infection prevalence. Am J Trop Med Hyg 88: 718725.[Crossref] [Google Scholar]
  50. Iwagami M, Fukumoto M, Hwang S-Y, Kim S-H, Kho W-G, Kano S, , 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.[Crossref] [Google Scholar]
  51. Karunaweera ND, Ferreira MU, Munasinghe A, Barnwell JW, Collins WE, King CL, Kawamoto F, Hartl DL, Wirth DF, , 2008. Extensive microsatellite diversity in the human malaria parasite Plasmodium vivax . Gene 410: 105112.[Crossref] [Google Scholar]
  52. Orjuela-Sanchez P, Sa JM, Brandi MC, Rodrigues PT, Bastos MS, Amaratunga C, Duong S, Fairhurst RM, Ferreira MU, , 2013. Higher microsatellite diversity in Plasmodium vivax than in sympatric Plasmodium falciparum populations in Pursat, western Cambodia. Exp Parasitol 134: 318326.[Crossref] [Google Scholar]
  53. Batista CL, Barbosa S, Da Silva Bastos M, Viana SA, Ferreira MU, , 2015. Genetic diversity of Plasmodium vivax over time and space: a community-based study in rural Amazonia. Parasitology 142: 374384.[Crossref] [Google Scholar]
  54. Brito CF, Ferreira MU, , 2011. Molecular markers and genetic diversity of Plasmodium vivax . Mem Inst Oswaldo Cruz 106: 1226.[Crossref] [Google Scholar]
  55. Chan CW, Sakihama N, Tachibana S-I, Idris ZM, Lum JK, Tanabe K, Kaneko A, , 2015. Plasmodium vivax and Plasmodium falciparum at the crossroads of exchange among islands in Vanuatu: implications for malaria elimination strategies. PLoS One 10: e0119475.[Crossref] [Google Scholar]
  56. de Souza AM, de Araujo FC, Fontes CJ, Carvalho LH, de Brito CF, de Sousa TN, , 2015. Multiple-clone infections of Plasmodium vivax: definition of a panel of markers for molecular epidemiology. Malar J 14: 330.[Crossref] [Google Scholar]
  57. Li Y-C, Wang G-Z, Meng F, Zeng W, He C-H, Hu X-M, Wang S-Q, , 2015. Genetic iversity of Plasmodium vivax population before elimination of malaria in Hainan Province, China. Malar J 14: 78.[Crossref] [Google Scholar]
  58. Russell B, Suwanarusk R, Lek-Uthai U, , 2006. Plasmodium vivax genetic diversity: microsatellite length matters. Trends Parasitol 22: 399401.[Crossref] [Google Scholar]
  59. Robinson LJ, Wampfler R, Betuela I, Karl S, White MT, Li Wai Suen CS, Hofmann NE, Kinboro B, Waltmann A, Brewster J, Lorry L, Tarongka N, Samol L, Silkey M, Bassat Q, Siba PM, Schofield L, Felger I, Mueller I, , 2015. Strategies for understanding and reducing the Plasmodium vivax and Plasmodium ovale hypnozoite reservoir in Papua New Guinean children: a randomised placebo-controlled trial and mathematical model. PLoS Med 12: e1001891.[Crossref] [Google Scholar]
  60. 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.[Crossref] [Google Scholar]
  61. Pacheco MA, Lopez-Perez M, Vallejo AF, Herrera S, Arèvalo-Herrera M, Escalante AA, , 2016. Multiplicity of infection and disease severity in Plasmodium vivax . PLoS Negl Trop Dis 10: e0004355.[Crossref] [Google Scholar]
  62. Havryliuk T, Ferreira MU, , 2009. A closer look at multiple-clone Plasmodium vivax infections: detection methods, prevalence and consequences. Mem Inst Oswaldo Cruz 104: 6773.[Crossref] [Google Scholar]
  63. 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: 14671482.[Crossref] [Google Scholar]
  64. Valderrama-Aguirre A, Quintero G, Gomez A, Castellanos A, Perez Y, Mendez F, Arevalo-Herrera M, Herrera S, , 2005. Antigenicity, immunogenicity, and protective efficacy of Plasmodium vivax MSP1: a potential malaria vaccine subunit. Am J Trop Med Hyg 73: 1624. [Google Scholar]
  65. Zeyrek FY, Tachibana S, Yuksel F, Doni N, Palacpac N, Arisue N, Horii T, Coban C, Tanabe K, , 2010. Limited polymorphism of the Plasmodium vivax merozoite surface protein 1 gene in isolates from Turkey. Am J Trop Med Hyg 83: 12301237.[Crossref] [Google Scholar]
  66. Ferreira MU, Ribeiro WL, Tonon AP, Kawamoto F, Rich SM, , 2003. Sequence diversity and evolution of the malaria vaccine candidate MSP-1 of Plasmodium falciparum . Gene 304: 6575.[Crossref] [Google Scholar]
  67. Soares IS, Barnwell JW, Ferreira MU, Gomes Da Cunha M, Laurino JP, Castilho BA, Rodrigues MM, , 1999. A Plasmodium vivax vaccine candidate displays limited allele polymorphism, which does not restrict recognition by antibodies. Mol Med 5: 459470. [Google Scholar]
  68. Fernandez-Becerra C, Sanz S, Brucet M, Stanisic DI, Alves FP, Camargo EP, Alonso PL, Mueller I, del Portillo HA, , 2010. Naturally-acquired humoral immune responses against the N- and C-termini of the Plasmodium vivax MSP1 protein in endemic regions of Brazil and Papua New Guinea using a multiplex assay. Malar J 9: 29.[Crossref] [Google Scholar]
  69. Cheng Q, Cunningham J, Gatton ML, , 2015. Systematic review of sub-microscopic P. vivax infections: prevalence and determining factors. PLoS Negl Trop Dis 9: e3413.[Crossref] [Google Scholar]
  70. Koepfli C, Schoepflin S, Bretscher M, Lin E, Kiniboro B, Zimmerman PA, Siba P, Smith TA, Mueller I, Felger I, , 2011. How much remains undetected? Probability of molecular detection of human Plasmodia in the field. PLoS One 6: e19010.[Crossref] [Google Scholar]
  71. Maneerattanasak S, Gosi P, Krudsood S, Tongshoob J, Lanteri CA, Snounou G, Khusmith S, , 2016. Genetic diversity among Plasmodium vivax isolates along the Thai-Myanmar border of Thailand. Malar J 15: 75.[Crossref] [Google Scholar]
  72. Wangchuk S, Drukpa T, Penjor K, Peldon T, Dorjey Y, Dorji K, Chhetri V, Trimarsanto H, To S, Murphy A, von Seidlein L, Price RN, Thriemer K, Auburn S, , 2016. Where chloroquine still works: the genetic make-up and susceptibility of Plasmodium vivax to chloroquine plus primaquine in Bhutan. Malar J 15: 277.[Crossref] [Google Scholar]
  73. White NJ, , 2011. Determinants of relapse periodicity in Plasmodium vivax malaria. Malar J 10: 136.[Crossref] [Google Scholar]
  74. Ferreira MU, Karunaweera ND, da Silva-Nunes M, da Silva NS, Wirth DF, Hartl DL, , 2007. Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. J Infect Dis 195: 12181226.[Crossref] [Google Scholar]
  75. 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, , 2007. Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. Int J Parasitol 37: 10131022.[Crossref] [Google Scholar]
  76. Gunawardena S, Karunaweera ND, Ferreira MU, Phone-Kyaw M, Pollack RJ, Alifrangis M, Rajakaruna RS, Konradsen F, Amerasinghe PH, Schousboe ML, Galappaththy GN, Abeyasinghe RR, Hartl DL, Wirth DF, , 2010. Geographic structure of Plasmodium vivax: microsatellite analysis of parasite populations from Sri Lanka, Myanmar, and Ethiopia. Am J Trop Med Hyg 82: 235242.[Crossref] [Google Scholar]
  77. Hetzel MW, Reimer LJ, Gideon G, Koimbu G, Barnadas C, Makita L, Siba PM, Mueller I, , 2016. Changes in malaria burden and transmission in sentinel sites after the roll-out of long-lasting insecticidal nets in Papua New Guinea. Parasit Vectors 9: 340.[Crossref] [Google Scholar]
  78. Reimer LJ, Thomsen EK, Koimbu G, Keven JB, Mueller I, Siba PM, Kazura JW, Hetzel MW, Zimmerman PA, , 2016. Malaria transmission dynamics surrounding the first nationwide long-lasting insecticidal net distribution in Papua New Guinea. Malar J 15: 25.[Crossref] [Google Scholar]
  79. Getachew S, To S, Trimarsanto H, Thriemer K, Clark TG, Petros B, Aseffa A, Price RN, Auburn S, , 2015. Variation in complexity of infection and transmission stability between neighbouring populations of Plasmodium vivax in southern Ethiopia. PLoS One 10: e0140780.[Crossref] [Google Scholar]
  80. Waltmann A, Darcy AW, Harris I, Koepfli C, Lodo J, Vahi V, Piziki D, Shanks GD, Barry AE, Whittaker M, Kazura JW, Mueller I, , 2015. High rates of asymptomatic, sub-microscopic Plasmodium vivax infection and disappearing Plasmodium falciparum malaria in an area of low transmission in Solomon Islands. PLoS Negl Trop Dis 9: e0003758.[Crossref] [Google Scholar]
  81. Koepfli C, Colborn KL, Kiniboro B, Lin E, Speed TP, Siba PM, Felger I, Mueller I, , 2013. A high force of Plasmodium vivax blood-stage infection drives the rapid acquisition of immunity in Papua New Guinean children. PLoS Negl Trop Dis 7: e2403.[Crossref] [Google Scholar]
  82. Schoepflin S, Valsangiacomo F, Lin E, Kiniboro B, Mueller I, Felger I, , 2009. Comparison of Plasmodium falciparum allelic frequency distribution in different endemic settings by high-resolution genotyping. Malar J 8: 250.[Crossref] [Google Scholar]
  83. Chenet SM, Schneider KA, Villegas L, Escalante AA, , 2012. Local population structure of Plasmodium: impact on malaria control and elimination. Malar J 11: 412.[Crossref] [Google Scholar]
  84. Sutton PL, , 2013. A call to arms: on refining Plasmodium vivax microsatellite marker panels for comparing global diversity. Malar J 12: 447.[Crossref] [Google Scholar]
  85. Daniels R, Volkman SK, Milner DA, Mahesh N, Neafsey DE, Park DJ, Rosen D, Angelino E, Sabeti PC, Wirth DF, Wiegand RC, , 2008. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar J 7: 111.[Crossref] [Google Scholar]
  86. Baniecki ML, Faust AL, Schaffner SF, Park DJ, Galinsky K, Daniels RF, Hamilton E, Ferreira MU, Karunaweera ND, Serre D, Zimmerman PA, Sa JM, Wellems TE, Musset L, Legrand E, Melnikov A, Neafsey DE, Volkman SK, Wirth DF, Sabeti PC, , 2015. Development of a single nucleotide polymorphism barcode to genotype Plasmodium vivax infections. PLoS Negl Trop Dis 9: e0003539.[Crossref] [Google Scholar]
  87. Cooper RD, Waterson DG, Frances SP, Beebe NW, Pluess B, Sweeney AW, , 2009. Malaria vectors of Papua New Guinea. Int J Parasitol 39: 14951501.[Crossref] [Google Scholar]
  88. Spencer T, Spencer M, Venters D, , 1974. Malaria vectors in Papua New Guinea. P N G Med J 17: 2230. [Google Scholar]
  89. Betuela I, Rosanas-Urgell A, Kiniboro B, Stanisic DI, Samol L, de Lazzari E, Del Portillo HA, Siba P, Alonso PL, Bassat Q, Mueller I, , 2012. Relapses contribute significantly to the risk of Plasmodium vivax infection and disease in Papua New Guinean children 1–5 years of age. J Infect Dis 206: 17711780.[Crossref] [Google Scholar]
  90. White NJ, Imwong M, , 2012. Relapse. Adv Parasitol 80: 113150. [Google Scholar]
  91. Hetzel MW, Pulford J, Paul S, Tarongka N, Morris H, Tandrapah T, Reimer L, Robinson L, Siba PM, Mueller I, , 2012. Dramatic changes in malaria after the free distribution of mosquito nets in Papua New Guinea. Malar J 11: O46.[Crossref] [Google Scholar]
  92. Alemu A, Muluye D, Mihret M, Adugna M, Gebeyaw M, , 2012. Ten year trend analysis of malaria prevalence in Kola Diba, North Gondar, northwest Ethiopia. Parasit Vectors 5: 173.[Crossref] [Google Scholar]
  93. Alemu A, Tsegaye W, Golassa L, Abebe G, , 2011. Urban malaria and associated risk factors in Jimma town, south-west Ethiopia. Malar J 10: 173.[Crossref] [Google Scholar]
  94. Rosenberg R, , 2007. Plasmodium vivax in Africa: hidden in plain sight? Trends Parasitol 23: 193196.[Crossref] [Google Scholar]
  95. Genton B, Betuela I, Felger I, Al-Yaman F, Anders RF, Saul A, Rare L, Baisor M, Lorry K, Brown GV, Pye D, Irving DO, Smith TA, Beck HP, Alpers MP, , 2002. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1-2b trial in Papua New Guinea. J Infect Dis 185: 820827.[Crossref] [Google Scholar]
  96. Fluck C, Smith T, Beck HP, Irion A, Betuela I, Alpers MP, Anders R, Saul A, Genton B, Felger I, , 2004. Strain-specific humoral response to a polymorphic malaria vaccine. Infect Immun 72: 63006305.[Crossref] [Google Scholar]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.16-0716
Loading
/content/journals/10.4269/ajtmh.16-0716
Loading

Data & Media loading...

  • Received : 01 Sep 2016
  • Accepted : 19 Nov 2016

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error