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1.
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Wells TNC, Burrows JN, Baird JK, 2010. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol 26: 145–151.
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Karunaweera ND, Ferreira MU, Munasinghe A, Barnwell J, Collins W, King CL, Kawamoto F, Hartl DL, Wirth DF, 2008. Extensive microsatellite diversity in the human malaria parasite Plasmodium vivax. Gene 410: 105–112.
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Zhong D, Bonizzoni M, Zhou G, Wang G, Chen B, Vardo-Zalik A, Cui L, Yan G, Zheng B, 2011. Genetic diversity of Plasmodium vivax malaria in China and Myanmar. Infect Genet Evol 11: 1419–1425.
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Ngrenngarmlert W, Kwiek JJ, Kamwendo DD, Ritola K, Swanstrom R, Wongsrichanalai C, Miller RS, Ittarat W, Meshnick SR, 2005. Measuring allelic heterogeneity in Plasmodium falciparum by a heteroduplex tracking assay. Am J Trop Med Hyg 72: 694–701.
-
14.
Juliano JJ, Kwiek JJ, Cappell K, Mwapasa V, Meshnick SR, 2007. Minority-variant pfcrt K76T mutations and chloroquine resistance, Malawi. Emerg Infect Dis 13: 872–877.
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Harrington PR, Connell MJ, Meeker RB, Johnson PR, Swanstrom R, 2007. Dynamics of simian immunodeficiency virus populations in blood and cerebrospinal fluid over the full course of infection. J Infect Dis 196: 1058–1067.
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Schnell G, Price RW, Swanstrom R, Spudich S, 2010. Compartmentalization and clonal amplification of HIV-1 variants in the cerebrospinal fluid during primary infection. J Virol 84: 2395–2407.
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Kwiek JJ, Alker AP, Wenink EC, Chaponda M, Kalilani LV, Meshnick SR, 2007. Estimating true antimalarial efficacy by heteroduplex tracking assay in patients with complex Plasmodium falciparum infections. Antimicrob Agents Chemother 51: 521–527.
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18.
Lin JT, Juliano JJ, Kharabora O, Sem R, Lin FC, Muth S, Menard D, Wongsrichanalai C, Rogers WO, Meshnick SR, 2012. Individual Pvmsp1 variants within polyclonal Plasmodium vivax infections display different propensities for relapse. J Clin Microbiol 50: 1449–1451.
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Suwanarusk R, Russell B, Chavchich M, Chavchich M, Chalfein F, Kenangalem E, Kosaisavee V, Prasetyorini B, Piera KA, Barends M, Brockman A, Lek-Uthai U, Anstey NM, Tjitra E, Nosten F, Cheng Q, Price RN, 2007. Chloroquine resistant Plasmodium vivax: in vitro characterization and association with molecular polymorphisms. PLoS ONE 2: e1089.
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Marfurt J, de Monbrison F, Brega S, Barbollat L, Mueller I, Sie A, Goroti M, Reeder JC, Beck H, Picot S, Genton B, 2008. Molecular markers of in vivo Plasmodium vivax resistance to amodiaquine plus sulfadoxine-pyrimethamine: mutations in pvdhfr and pvmdr1. J Infect Dis 198: 409–417.
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Suwanarusk R, Chavchich M, Russell B, Jaidee A, Chalfein F, Barends M, Prasetyorini B, Kenangalem E, Piera KA, Lek-Uthai U, Anstey NM, Tjitra E, Nosten F, Cheng Q, Price RN, 2008. Amplification of pvmdr1 associated with multidrug-resistant Plasmodium vivax. J Infect Dis 198: 1558–1564.
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Imwong M, Pukrittayakamee S, Pongtavornpinyo W, Nakeesathit S, Pongtavornpinyo W, Nakeesathit S, Nair S, Newton P, Nosten F, Anderson TJ, Dondorp A, Day NP, White NJ, 2008. Gene amplification of the multidrug resistance 1 gene of Plasmodium vivax isolates from Thailand, Laos, and Myanmar. Antimicrob Agents Chemother 52: 2657–2659.
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Brega S, Meslin B, de Monbrison F, Severini C, Meslin B, de Monbrison F, Severini C, Gradoni L, Udomsangpetch R, Sutanto I, Peyron F, Picot S, 2005. Identification of the Plasmodium vivax mdr-like gene (pvmdr1) and analysis of single-nucleotide polymorphisms among isolates from different areas of endemicity. J Infect Dis 191: 272–277.
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Lu F, Lim CS, Nam DH, Kim K, Lin K, Kim T, Lee H, Chen J, Wang Y, Sattabongkot J, Han E, 2011. Genetic polymorphism in pvmdr1 and pvcrt-o genes in relation to in vitro drug susceptibility of Plasmodium vivax isolates from malaria-endemic countries. Acta Trop 117: 69–75.
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Orjuela-Sánchez P, Karunaweera ND, da Silva-Nunes M, da Silva NS, Scopel KK, Goncalves RM, Amaratunga C, Sa JM, Socheat D, Fairhurst RM, Gunawardena S, Thavakodirasah T, Galapaththy GL, Abeysinghe R, Kawamoto F, Wirth DF, Ferreira MU, 2010. Single-nucleotide polymorphism, linkage disequilibrium and geographic structure in the malaria parasite Plasmodium vivax: prospects for genome-wide association studies. BMC Genet 11: 65.
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Plasmodium vivax Isolates from Cambodia and Thailand Show High Genetic Complexity and Distinct Patterns of P. vivax Multidrug Resistance Gene 1 (pvmdr1) Polymorphisms
Jessica T. Lin
Jessica T. Lin
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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Jaymin C. Patel
Jaymin C. Patel
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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Oksana Kharabora
Oksana Kharabora
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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Jetsumon Sattabongkot
Jetsumon Sattabongkot
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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Sinuon Muth
Sinuon Muth
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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Ratawan Ubalee
Ratawan Ubalee
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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Anthony L. Schuster
Anthony L. Schuster
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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William O. Rogers
William O. Rogers
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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Chansuda Wongsrichanalai
Chansuda Wongsrichanalai
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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Jonathan J. Juliano
Jonathan J. Juliano
Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, North Carolina; Department of Epidemiology, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina; Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; National Malaria Center, Phnom Penh, Cambodia; Naval Medical Research Unit #2, Phnom Penh, Cambodia
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Plasmodium vivax accounts for an increasing fraction of malaria infections in Thailand and Cambodia. We compared P. vivax genetic complexity and antimalarial resistance patterns in the two countries. Use of a heteroduplex tracking assay targeting the merozoite surface protein 1 gene revealed that vivax infections in both countries are frequently polyclonal (84%), with parasites that are highly diverse (HE = 0.86) but closely related (GST = 0.18). Following a history of different drug policies in Thailand and Cambodia, distinct patterns of antimalarial resistance have emerged: most Cambodian isolates harbor the P. vivax multidrug resistance gene 1 (pvmdr1) 976F mutation associated with chloroquine resistance (89% versus 8%, P < 0.001), whereas Thai isolates more often display increased pvmdr1 copy number (39% versus 4%, P < 0.001). Finally, genotyping of paired isolates from individuals suspected of suffering relapse supports a complex scheme of relapse whereby recurrence of multiple identical variants is sometimes accompanied by the appearance of novel variants.
Author Notes
Financial support: This work was supported by the U.S. Department of Defense Global Emerging Infections Surveillance and Response System Program and the National Institutes of Health [grant number AI089819 to J.J.J.]. J.T.L. was supported by an NIH Infectious Disease Pathogenesis Research Training Grant [grant number 5T32AI0715132] and the North Carolina Clinical and Translational Science Award [grant number UL1RR025747].
Authors' addresses: Jessica T. Lin, Oksana Kharabora, and Jonathan J. Juliano, Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, NC, E-mails: jessica_lin@med.unc.edu, kharabor@email.unc.edu, and jonthan_juliano@med.unc.edu. Jaymin C. Patel, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, E-mail: jaymin86@email.unc.edu. Jetsumon Sattabongkot, Mahidol Vivax Research Center, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand, E-mail: jetsumon.pra@mahidol.ac.th. Sinuon Muth, National Malaria Center, Phnom Penh, Cambodia, E-mail: sinuonm@cnm.gov.kh. Ratawan Ubalee and Anthony L. Schuster, Department of Entomology, USAMC Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand, E-mails: RatawanU@afrims.org and Schuster.Anthony@afrims.org. William O. Rogers, E-mail: mrogers70@yahoo.com. Chansuda Wongsrichanalai, Bangkok, Thailand, E-mail: dr.chansuda@gmail.com.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Zhou G, Sirichaisinthop J, Sattabongkot J, Jones J, Bjørnstad ON, Yan G, Cui L, 2005. Spatio-temporal distribution of Plasmodium falciparum and P. vivax malaria in Thailand. Am J Trop Med Hyg 72: 256–262.
-
2.
Snounou G, White NJ, 2004. The co-existence of Plasmodium: sidelights from falciparum and vivax malaria in Thailand. Trends Parasitol 20: 333–339.
-
3.
Wangroongsarb P, Sudathip P, Satimai W, 2012. Characteristics and malaria prevalence of migrant populations in malaria-endemic areas along the Thai-Cambodian border. Southeast Asian J Trop Med Public Health 43: 261–269.
-
4.
Sattabongkot J, Tsuboi T, Zollner GE, Sirichaisinthop J, Cui L, 2004. Plasmodium vivax transmission: chances for control? Trends Parasitol 20: 192–198.
-
5.
Wells TNC, Burrows JN, Baird JK, 2010. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol 26: 145–151.
-
6.
de Brito CFA, Ferreira MU, 2011. Molecular markers and genetic diversity of Plasmodium vivax. Mem Inst Oswaldo Cruz 106 (Suppl 1): 12–26.
-
7.
Hastings IM, Watkins WM, 2005. Intensity of malaria transmission and the evolution of drug resistance. Acta Trop 94: 218–229.
-
8.
Havryliuk T, Ferreira MU, 2009. A closer look at multiple-clone Plasmodium vivax infections: detection methods, prevalence and consequences. Mem Inst Oswaldo Cruz 104: 67–73.
-
9.
Cui L, Mascorro CN, Fan Q, Rzomp K, 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: 613–619.
-
10.
Karunaweera ND, Ferreira MU, Munasinghe A, Barnwell J, Collins W, King CL, Kawamoto F, Hartl DL, Wirth DF, 2008. Extensive microsatellite diversity in the human malaria parasite Plasmodium vivax. Gene 410: 105–112.
-
11.
Zhong D, Bonizzoni M, Zhou G, Wang G, Chen B, Vardo-Zalik A, Cui L, Yan G, Zheng B, 2011. Genetic diversity of Plasmodium vivax malaria in China and Myanmar. Infect Genet Evol 11: 1419–1425.
-
12.
Imwong M, Snounou G, Pukrittayakamee S, Tanomsing N, Kim JR, Nandy A, Guthmann J, Nosten F, Carlton J, Looareesuwan S, Nair S, Sudimack D, Day NP, Anderson TJ, White NJ, 2007. Relapses of Plasmodium vivax infection usually result from activation of heterologous hypnozoites. J Infect Dis 195: 927–933.
-
13.
Ngrenngarmlert W, Kwiek JJ, Kamwendo DD, Ritola K, Swanstrom R, Wongsrichanalai C, Miller RS, Ittarat W, Meshnick SR, 2005. Measuring allelic heterogeneity in Plasmodium falciparum by a heteroduplex tracking assay. Am J Trop Med Hyg 72: 694–701.
-
14.
Juliano JJ, Kwiek JJ, Cappell K, Mwapasa V, Meshnick SR, 2007. Minority-variant pfcrt K76T mutations and chloroquine resistance, Malawi. Emerg Infect Dis 13: 872–877.
-
15.
Harrington PR, Connell MJ, Meeker RB, Johnson PR, Swanstrom R, 2007. Dynamics of simian immunodeficiency virus populations in blood and cerebrospinal fluid over the full course of infection. J Infect Dis 196: 1058–1067.
-
16.
Schnell G, Price RW, Swanstrom R, Spudich S, 2010. Compartmentalization and clonal amplification of HIV-1 variants in the cerebrospinal fluid during primary infection. J Virol 84: 2395–2407.
-
17.
Kwiek JJ, Alker AP, Wenink EC, Chaponda M, Kalilani LV, Meshnick SR, 2007. Estimating true antimalarial efficacy by heteroduplex tracking assay in patients with complex Plasmodium falciparum infections. Antimicrob Agents Chemother 51: 521–527.
-
18.
Lin JT, Juliano JJ, Kharabora O, Sem R, Lin FC, Muth S, Menard D, Wongsrichanalai C, Rogers WO, Meshnick SR, 2012. Individual Pvmsp1 variants within polyclonal Plasmodium vivax infections display different propensities for relapse. J Clin Microbiol 50: 1449–1451.
-
19.
Suwanarusk R, Russell B, Chavchich M, Chavchich M, Chalfein F, Kenangalem E, Kosaisavee V, Prasetyorini B, Piera KA, Barends M, Brockman A, Lek-Uthai U, Anstey NM, Tjitra E, Nosten F, Cheng Q, Price RN, 2007. Chloroquine resistant Plasmodium vivax: in vitro characterization and association with molecular polymorphisms. PLoS ONE 2: e1089.
-
20.
Marfurt J, de Monbrison F, Brega S, Barbollat L, Mueller I, Sie A, Goroti M, Reeder JC, Beck H, Picot S, Genton B, 2008. Molecular markers of in vivo Plasmodium vivax resistance to amodiaquine plus sulfadoxine-pyrimethamine: mutations in pvdhfr and pvmdr1. J Infect Dis 198: 409–417.
-
21.
Suwanarusk R, Chavchich M, Russell B, Jaidee A, Chalfein F, Barends M, Prasetyorini B, Kenangalem E, Piera KA, Lek-Uthai U, Anstey NM, Tjitra E, Nosten F, Cheng Q, Price RN, 2008. Amplification of pvmdr1 associated with multidrug-resistant Plasmodium vivax. J Infect Dis 198: 1558–1564.
-
22.
Imwong M, Pukrittayakamee S, Pongtavornpinyo W, Nakeesathit S, Pongtavornpinyo W, Nakeesathit S, Nair S, Newton P, Nosten F, Anderson TJ, Dondorp A, Day NP, White NJ, 2008. Gene amplification of the multidrug resistance 1 gene of Plasmodium vivax isolates from Thailand, Laos, and Myanmar. Antimicrob Agents Chemother 52: 2657–2659.
-
23.
Brega S, Meslin B, de Monbrison F, Severini C, Meslin B, de Monbrison F, Severini C, Gradoni L, Udomsangpetch R, Sutanto I, Peyron F, Picot S, 2005. Identification of the Plasmodium vivax mdr-like gene (pvmdr1) and analysis of single-nucleotide polymorphisms among isolates from different areas of endemicity. J Infect Dis 191: 272–277.
-
24.
Lu F, Lim CS, Nam DH, Kim K, Lin K, Kim T, Lee H, Chen J, Wang Y, Sattabongkot J, Han E, 2011. Genetic polymorphism in pvmdr1 and pvcrt-o genes in relation to in vitro drug susceptibility of Plasmodium vivax isolates from malaria-endemic countries. Acta Trop 117: 69–75.
-
25.
Orjuela-Sánchez P, Karunaweera ND, da Silva-Nunes M, da Silva NS, Scopel KK, Goncalves RM, Amaratunga C, Sa JM, Socheat D, Fairhurst RM, Gunawardena S, Thavakodirasah T, Galapaththy GL, Abeysinghe R, Kawamoto F, Wirth DF, Ferreira MU, 2010. Single-nucleotide polymorphism, linkage disequilibrium and geographic structure in the malaria parasite Plasmodium vivax: prospects for genome-wide association studies. BMC Genet 11: 65.
-
26.
Vargas-RodrÃguez RC, da Silva Bastos M, Menezes MJ, Orjuela-Sánchez P, Ferreira MU, 2012. Single-nucleotide polymorphism and copy number variation of the multidrug resistance-1 locus of Plasmodium vivax: local and global patterns. Am J Trop Med Hyg 87: 813–821.
-
27.
Rogers WO, Sem R, Tero T, Chim P, Lim P, Muth S, Socheat D, Ariey F, Wongsrichanalai C, 2009. Failure of artesunate-mefloquine combination therapy for uncomplicated Plasmodium falciparum malaria in southern Cambodia. Malar J 8: 10.
-
28.
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