Using Amplicon Deep Sequencing to Detect Genetic Signatures of Plasmodium vivax Relapse

Journal of Infectious Diseases

Volumn 212, Issue 6, 2015, Pages 999-1008

  Lin, Jessica T ^a   Hathaway, Nicholas J ^b   Saunders, David L ^c   Lon, Chanthap ^c   Balasubramanian, Sujata ^a   Kharabora, Oksana ^a   Gosi, Panita ^c   Sriwichai, Sabaithip ^c   Kartchner, Laurel ^a   Chuor, Char Meng ^d   Satharath, Prom ^e   Lanteri, Charlotte ^c   Bailey, Jeffrey A ^b   Juliano, Jonathan J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

^d Entomology and Malaria Control   (Cambodia)

^e Royal Cambodian Armed Forces   (Cambodia)

Author keywords

amplicon sequencing; deep sequencing; genetic diversity; hypnozoite; malaria; microsatellite; multiplicity of infection; Plasmodium vivax; pvmsp1; relapse

Indexed keywords

CHLOROQUINE; DIHYDROARTEMISININ PLUS PIPERAQUINE; MEROZOITE SURFACE PROTEIN 1; PRIMAQUINE; MICROSATELLITE DNA; PROTOZOAL DNA;

ADULT; AMPLICON DEEP SEQUENCING; CAMBODIAN; CLONE; CONFERENCE PAPER; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MEROZOITE SURFACE PROTEIN 1 GENE; MICROSATELLITE MARKER; NONHUMAN; PLASMODIUM VIVAX MALARIA; PRIORITY JOURNAL; RECURRENT INFECTION; REINFECTION; RELAPSE; SEQUENCE ANALYSIS; CAMBODIA; GENE EXPRESSION REGULATION; GENETICS; MALARIA, VIVAX; METABOLISM; PARASITOLOGY; PHYLOGENY; PLASMODIUM VIVAX; RECURRENT DISEASE;

CAMBODIA; DNA, PROTOZOAN; GENE EXPRESSION REGULATION; GENETIC VARIATION; HAPLOTYPES; HUMANS; MALARIA, VIVAX; MEROZOITE SURFACE PROTEIN 1; MICROSATELLITE REPEATS; PHYLOGENY; PLASMODIUM VIVAX; RECURRENCE;

EID: 84940747421     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiv142     Document Type: Conference Paper

References (43)

1. Mueller I, Galinski MR, Baird JK, et al. Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 2009; 9:555-66.
2. Arnott A, Barry AE, Reeder JC. Understanding the population genetics of Plasmodium vivax is essential for malaria control and elimination. Malar J 2012; 11:14.
3. Cotter C, Sturrock HJW, Hsiang MS, et al. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet 2013; 382:900-11.
4. Wells TNC, Burrows JN, Baird JK. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol 2010; 26:145-51.
5. White MT, Karl S, Battle KE, Hay SI, Mueller I, Ghani AC. Modelling the contribution of the hypnozoite reservoir to Plasmodium vivax transmission. Elife 2014; 3:e04692.
6. Baird JK, Leksana B, Masbar S, et al. Diagnosis of resistance to chloroquine by Plasmodium vivax: timing of recurrence and whole blood chloroquine levels. Am J Trop Med Hyg 1997; 56:621-6.
7. Pukrittayakamee S, Clemens R, Chantra A, et al. Therapeutic responses to antibacterial drugs in vivax malaria. Trans R Soc Trop Med Hyg 2001; 95:524-8.
8. Mayxay M, Pukrittayakamee S, Newton PN, White NJ. Mixed-species malaria infections in humans. Trends Parasitol 2004; 20:233-40.
9. White NJ. Determinants of relapse periodicity in Plasmodium vivax malaria. Malar J 2011; 10:297.
10. Douglas NM, Nosten F, Ashley EA, et al. Plasmodium vivax recurrence following falciparum and mixed species malaria: risk factors and effect of antimalarial kinetics. Clin Infect Dis 2011; 52:612-20.
11. Smithuis F, Kyaw MK, Phe O, et al. Effectiveness of five artemisinin combination regimens with or without primaquine in uncomplicated falciparum malaria: an open-label randomised trial. Lancet Infect Dis 2010; 10:673-81.
12. Imwong M, Snounou G, Pukrittayakamee S, et al. Relapses of Plasmodium vivax infection usually result from activation of heterologous hypnozoites. J Infect Dis 2007; 195:927-33.
13. Chen N, Auliff A, Rieckmann K, Gatton M, Cheng Q. Relapses of Plasmodium vivax infection result from clonal hypnozoites activated at predetermined intervals. J Infect Dis 2007; 195:934-41.
14. Restrepo E, Imwong M, Rojas W, Carmona-Fonseca J, Maestre A. High genetic polymorphism of relapsing P. vivax isolates in northwest Colombia. Acta Trop 2011; 119:23-9.
15. de Araujo FCF, de Rezende AM, Fontes CJF, Carvalho LH, Alves de Brito CF. Multiple-clone activation of hypnozoites is the leading cause of relapse in Plasmodium vivax infection. PLOS ONE 2012; 7: e49871.
16. Lin JT, Patel JC, Kharabora O, et al. Plasmodium vivax isolates from Cambodia and Thailand show high genetic complexity and distinct patterns of P. vivax multidrug resistance gene 1 (pvmdr1) polymorphisms. Am J Trop Med Hyg 2013; 88:1116-23.
17. Orjuela-Sánchez P, Sá JM, Brandi MCC, et al. Higher microsatellite diversity in Plasmodium vivax than in sympatric Plasmodium falciparum populations in Pursat, Western Cambodia. Exp Parasitol 2013; 134: 318-26.
18. Thanapongpichat S, McGready R, Luxemburger C, et al. Microsatellite genotyping of Plasmodium vivax infections and their relapses in pregnant and non-pregnant patients on the Thai-Myanmar border. Malar J 2013; 12:275.
19. Lon C, Manning JE, Vanachayangkul P, et al. Efficacy of two versus three-day regimens of dihydroartemisinin-piperaquine for uncomplicated malaria in military personnel in northern Cambodia: an openlabel randomized trial. PLOS ONE 2014; 9:e93138.
20. Parobek CM, Bailey JA, Hathaway NJ, Socheat D, Rogers WO, Juliano JJ. Differing patterns of selection and geospatial genetic diversity within two leading Plasmodium vivax candidate vaccine antigens. PLOS Negl Trop Dis 2014; 8:e2796.
21. Altshuler D, Pollara VJ, Cowles CR, et al. An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 2000; 407:513-6.
22. Rezende AM, Tarazona-Santos E, Fontes CJF, et al. Microsatellite loci: determining the genetic variability of Plasmodium vivax. Trop Med Int Health 2010; 15:718-26.
23. Karunaweera ND, Ferreira MU, Hartl DL, Wirth DF. Fourteen polymorphic microsatellite DNA markers for the human malaria parasite Plasmodium vivax. Molecular Ecology Notes 2007; 7:172-5.
24. Sutton PL. A call to arms: on refining Plasmodium vivax microsatellite marker panels for comparing global diversity. Malar J 2013; 12:447.
25. Havryliuk T, Ferreira MU. A closer look at multiple-clone Plasmodium vivax infections: detection methods, prevalence and consequences. Mem Inst Oswaldo Cruz 2009; 104:67-73.
26. Mideo N, Kennedy DA, Carlton JM, Bailey JA, Juliano JJ, Read AF. Ahead of the curve: next generation estimators of drug resistance in malaria infections. Trends Parasitol 2013; 29:321-8.
27. Juliano JJ, Kwiek JJ, Cappell K, Mwapasa V, Meshnick SR. Minorityvariant pfcrt K76T mutations and chloroquine resistance, Malawi. Emerging Infect Dis 2007; 13:872-7.
28. Kwiek JJ, Alker AP, Wenink EC, Chaponda M, Kalilani LV, Meshnick SR. Estimating true antimalarial efficacy by heteroduplex tracking assay in patients with complex Plasmodium falciparum infections. Antimicrob Agents Chemother 2007; 51:521-7.
29. Norman GR, Streiner DL. Biostatistics: the bare essentials. Hamilton, Ontario: Bc Decker, 2008.
30. Orjuela-Sánchez P, da Silva NS, da Silva-Nunes M, Ferreira MU. Recurrent parasitemias and population dynamics of Plasmodium vivax polymorphisms in rural Amazonia. Am J Trop Med Hyg 2009; 81:961-8.
31. Kim J-R, Nandy A, Maji AK, et al. Genotyping of Plasmodium vivax reveals both short and long latency relapse patterns in Kolkata. PLOS ONE 2012; 7:e39645.
32. Imwong M, Boel ME, Pagornrat W, et al. The first Plasmodium vivax relapses of life are usually genetically homologous. J Infect Dis 2012; 205:680-3.
33. Nkhoma SC, Nair S, Cheeseman IH, et al. Close kinship within multiplegenotype malaria parasite infections. Proc Biol Sci 2012; 279:2589-98.
34. Conway DJ, Greenwood BM, McBride JS. The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology 1991; 103(Pt 1):1-6.
35. Bright AT, Manary MJ, Tewhey R, et al. A high resolution case study of a patient with recurrent Plasmodium vivax infections shows that relapses were caused by meiotic siblings. PLOS Negl Trop Dis 2014; 8:e2882.
36. Sutton PL, Neyra V, Hernandez JN, Branch OH. Plasmodium falciparum and Plasmodium vivax infections in the Peruvian Amazon: propagation of complex, multiple allele-type infections without superinfection. Am J Trop Med Hyg 2009; 81:950-60.
37. Givens MB, Lin JT, Lon C, et al. Development of a capillary electrophoresis-based heteroduplex tracking assay to measure in-host genetic diversity of initial and recurrent Plasmodium vivax infections in Cambodia. J Clin Microbiol 2014; 52:298-301.
38. Andrianaranjaka V, Lin JT, Golden C, Juliano JJ, Randrianarivelojosia M. Activation of minority-variant Plasmodium vivax hypnozoites following artesunate+amodiaquine treatment in a 23-year old man with relapsing malaria in Antananarivo, Madagascar. Malar J 2013; 12:177.
39. Nair S, Nkhoma SC, Serre D, et al. Single-cell genomics for dissection of complex malaria infections. Genome Res 2014; 24:1028-38.
40. Koepfli C, Schoepflin S, Bretscher M, et al. How much remains undetected? Probability of molecular detection of human Plasmodia in the field. PLOS ONE 2011; 6:e19010.
41. Betuela I, Rosanas-Urgell A, Kiniboro B, et al. 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 2012; 206: 1771-80.
42. Sutanto I, Tjahjono B, Basri H, et al. Randomized, open-label trial of primaquine against vivax malaria relapse in Indonesia. Antimicrob Agents Chemother 2013; 57:1128-35.
43. Llanos-Cuentas A, Lacerda MV, Rueangweerayut R, et al. Tafenoquine plus chloroquine for the treatment and relapse prevention of Plasmodium vivax malaria (DETECTIVE): a multicentre, doubleblind, randomised, phase 2b dose-selection study. Lancet 2014; 383:1049-58.