Blood-stage parasitaemia and age determine Plasmodium falciparum and P. vivax gametocytaemia in Papua New Guinea

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Koepfli, Cristian ^a,b   Robinson, Leanne J ^a,b,c   Rarau, Patricia ^c   Salib, Mary ^c   Sambale, Naomi ^c   Wampfler, Rahel ^d,e   Betuela, Inoni ^c   Nuitragool, Wang ^f   Barry, Alyssa E ^a,b   Siba, Peter ^c   Felger, Ingrid ^d,e   Mueller, Ivo ^a,b,g  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c PAPUA NEW GUINEA INSTITUTE OF MEDICAL RESEARCH   (Papua New Guinea)

^d SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^e UNIVERSITY OF BASEL   (Switzerland)

^f MAHIDOL UNIVERSITY   (Thailand)

^g CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT;

ADOLESCENT; ADULT; AGE DISTRIBUTION; ANEMIA; ARTICLE; BED NET; CHILD; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE TRANSMISSION; DNA EXTRACTION; FEVER; GAMETOCYTE; GENE; GENE EXPRESSION; HUMAN; MALARIA FALCIPARUM; MICROSCOPY; PAPUA NEW GUINEA; PARASITE IDENTIFICATION; PARASITEMIA; PFS25 GENE; PLASMODIUM FALCIPARUM; PLASMODIUM MALARIAE; PLASMODIUM MALARIAE INFECTION; PLASMODIUM VIVAX; PLASMODIUM VIVAX MALARIA; PREVALENCE; PVS25 GENE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; ERYTHROCYTE; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INFANT; LIFE CYCLE STAGE; MALARIA, FALCIPARUM; MALARIA, VIVAX; MALE; NEWBORN; PARASITE LOAD; PARASITOLOGY; PRESCHOOL CHILD; YOUNG ADULT;

PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX;

ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; ERYTHROCYTES; FEMALE; GENES, PROTOZOAN; HUMANS; INFANT; INFANT, NEWBORN; LIFE CYCLE STAGES; MALARIA, FALCIPARUM; MALARIA, VIVAX; MALE; PAPUA NEW GUINEA; PARASITE LOAD; PARASITEMIA; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PREVALENCE; YOUNG ADULT;

EID: 84930662379     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126747     Document Type: Article

References (49)

1. Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011; 24(2):377-410. doi: 10.1128/CMR.00051-10 PMID: 21482730
2. Garnham PCC. Malaria Parasites And Other Heamosporidia. Oxford: Blackwell Scientific Publications; 1966.
3. McCarthy JS, Griffin PM, Sekuloski S, Bright AT, Rockett R, Looke D, et al. Experimentally induced blood-stage Plasmodium vivax infection in healthy volunteers. J Infect Dis. 2013.
4. Smalley ME, Sinden RE. Plasmodium-Falciparum Gametocytes - Their Longevity and Infectivity. Parasitology. 1977; 74(Feb):1-8.
5. Bousema T, Okell L, Shekalaghe S, Griffin JT, Omar S, Sawa P, et al. Revisiting the circulation time of Plasmodium falciparum gametocytes: molecular detection methods to estimate the duration of gametocyte carriage and the effect of gametocytocidal drugs. Malaria J. 2010; 9:136.
6. Carter R, Graves PM. Gametocytes. In: Wernsdorfer WH, McGregor IA, editors. Malaria: principles and practice of malariology. Edinburgh, United Kingdom: Churchill Livingstone; 1988. p. 253-306.
7. Price R, Nosten F, Simpson JA, Luxemburger C, Phaipun L, ter Kuile F, et al. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am Journal Trop Med Hyg. 1999; 60(6):1019-23. PMID: 10403336
8. McKenzie FE, Wongsrichanalai C, Magill AJ, Forney JR, Permpanich B, Lucas C, et al. Gametocytemia in Plasmodium vivax and Plasmodium falciparum infections. J Parasitology. 2006; 92(6):1281-5. PMID: 17304807
9. Mawili-Mboumba DP, Nikiema R, Bouyou-Akotet MK, Bahamontes-Rosa N, Traore A, Kombila M. Submicroscopic gametocyte carriage in febrile children living in different areas of Gabon. Malaria J. 2013; 12:375. doi: 10.1186/1475-2875-12-375 PMID: 24168323
10. Sowunmi A, Fateye BA, Adedeji AA, Fehintola FA, Happi TC. Risk factors for gametocyte carriage in uncomplicated falciparum malaria in children. Parasitology. 2004; 129(Pt 3):255-62. PMID: 15471001
11. von Seidlein L, Drakeley C, Greenwood B, Walraven G, Targett G. Risk factors for gametocyte carriage in Gambian children. Am Journal Trop Med Hyg. 2001; 65(5):523-7. PMID: 11716108
12. Hasugian AR, Purba HL, Kenangalem E, Wuwung RM, Ebsworth EP, Maristela R, et al. Dihydroartemisinin-piperaquine versus artesunate-amodiaquine: superior efficacy and posttreatment prophylaxis against multidrug-resistant Plasmodium falciparum and Plasmodium vivax malaria. Clin Infect Dis. 2007; 44(8):1067-74. PMID: 17366451
13. Gamage-Mendis AC, Rajakaruna J, Carter R, Mendis KN. Infectious reservoir of Plasmodium vivax and Plasmodium falciparum malaria in an endemic region of Sri Lanka. Am Journal Trop Med Hyg. 1991; 45(4):479-87. PMID: 1951856
14. Douglas NM, Simpson JA, Phyo AP, Siswantoro H, Hasugian AR, Kenangalem E, et al. Gametocyte Dynamics and the Role of Drugs in Reducing the Transmission Potential of Plasmodium vivax. J Infect Dis 2013; 208(5):801-12. doi: 10.1093/infdis/jit261 PMID: 23766527
15. Huh AJ, Kwak YG, Kim ES, Lee KS, Yeom JS, Cho YK, et al. Parasitemia characteristics of Plasmodium vivax malaria patients in the Republic of Korea. J Korean Med Sci. 2011; 26(1):42-6. doi: 10.3346/jkms.2011.26.1.42 PMID: 21218028
16. Cattani JA, Tulloch JL, Vrbova H, Jolley D, Gibson FD, Moir JS, et al. The epidemiology of malaria in a population surrounding Madang, Papua New Guinea. Am J Trop Med Hyg. 1986; 35(1):3-15. PMID: 3511748
17. Gneme A, Guelbeogo WM, Riehle MM, Tiono AB, Diarra A, Kabre GB, et al. Plasmodium species occurrence, temporal distribution and interaction in a child-aged population in rural Burkina Faso. Malaria J. 2013; 12:67.
18. Bousema JT, Gouagna LC, Drakeley CJ, Meutstege AM, Okech BA, Akim IN, et al. Plasmodium falciparum gametocyte carriage in asymptomatic children in western Kenya. Malaria J. 2004; 3:18.
19. Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, et al. Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua, New Guinea. Parasitology. 1988; 96 (Pt 2):251-63. PMID: 3374964
20. Shekalaghe SA, Bousema JT, Kunei KK, Lushino P, Masokoto A, Wolters LR, et al. Submicroscopic Plasmodium falciparum gametocyte carriage is common in an area of low and seasonal transmission in Tanzania. Trop Med Int Health. 2007; 12(4):547-53. PMID: 17445146
21. Bousema JT, Schneider P, Gouagna LC, Drakeley CJ, Tostmann A, Houben R, et al. Moderate effect of artemisinin-based combination therapy on transmission of Plasmodium falciparum. J Infect Dis. 2006; 193(8):1151-9. PMID: 16544256
22. Beurskens M, Mens P, Schallig H, Syafruddin D, Asih PB, Hermsen R, et al. Quantitative determination of Plasmodium vivax gametocytes by real-time quantitative nucleic acid sequence-based amplification in clinical samples. Am J Trop Med Hyg. 2009; 81(2):366-9. PMID: 19635900
23. Ouedraogo AL, Bousema T, Schneider P, de Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PloS One. 2009; 4(12):e8410. doi: 10.1371/journal.pone.0008410 PMID: 20027314
24. Kuamsab N, Putaporntip C, Pattanawong U, Jongwutiwes S. Simultaneous detection of Plasmodium vivax and Plasmodium falciparum gametocytes in clinical isolates by multiplex-nested RT-PCR. Malaria J. 2012; 11:190. doi: 10.1186/1475-2875-11-190 PMID: 22682065
25. El-Sayed B, El-Zaki SE, Babiker H, Gadalla N, Ageep T, Mansour F, et al. A randomized open-label trial of artesunate- sulfadoxine-pyrimethamine with or without primaquine for elimination of sub-microscopic P. falciparum parasitaemia and gametocyte carriage in eastern Sudan. PloS One. 2007; 2(12): e1311. PMID: 18074034
26. Lima NF, Bastos MS, Ferreira MU. Plasmodium vivax: reverse transcriptase real-time PCR for gametocyte detection and quantitation in clinical samples. Exp Parasitol. 2012; 132(3):348-54. doi: 10.1016/j.exppara.2012.08.010 PMID: 22940017
27. Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007; 76(3):470-4. PMID: 17360869
28. Coleman RE, Kumpitak C, Ponlawat A, Maneechai N, Phunkitchar V, Rachapaew N, et al. Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in western Thailand. J Med Entomol. 2004; 41(2):201-8. PMID: 15061279
29. Sattabongkot J, Maneechai N, Rosenberg R. Plasmodium vivax: gametocyte infectivity of naturally infected Thai adults. Parasitology. 1991; 102 Pt 1:27-31. PMID: 2038501
30. Bharti AR, Chuquiyauri R, Brouwer KC, Stancil J, Lin J, Llanos-Cuentas A, et al. Experimental infection of the neotropical malaria vector Anopheles darlingi by human patient-derived Plasmodium vivax in the Peruvian Amazon. Am J Trop Med Hyg. 2006; 75(4):610-6. PMID: 17038681
31. Pethleart A, Prajakwong S, Suwonkerd W, Corthong B, Webber R, Curtis C. Infectious reservoir of Plasmodium infection in Mae Hong Son Province, north-west Thailand. Malaria J. 2004; 3:34.
32. Hetzel MW, Gideon G, Lote N, Makita L, Siba PM, Mueller I. Ownership and usage of mosquito nets after four years of large-scale free distribution in Papua New Guinea. Malaria J. 2012; 11:192. doi: 10.1186/1475-2875-11-192 PMID: 22682111
33. Wampfler R, Mwingira F, Javati S, Robinson L, Betuela I, Siba P, et al. Strategies for Detection of Plasmodium species Gametocytes. PloS One. 2013; 8(9).
34. Laman M, Moore BR, Benjamin J, Padapu N, Tarongka N, Siba P, et al. Comparison of an assumed versus measured leucocyte count in parasite density calculations in Papua New Guinean children with uncomplicated malaria. Malaria J. 2014; 13:145. doi: 10.1186/1475-2875-13-145 PMID: 24739250
35. Rosanas-Urgell A, Mueller D, Betuela I, Barnadas C, Iga J, Zimmerman PA, et al. Comparison of diagnostic methods for the detection and quantification of the four sympatric Plasmodium species in field samples from Papua New Guinea. Malaria J. 2010; 9:361.
36. Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, Nale J, et al. Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Malaria J. 2010; 9:336.
37. Arnott A, Barnadas C, Senn N, Siba P, Mueller I, Reeder JC, et al. High Genetic Diversity of Plasmodium vivax on the North Coast of Papua New Guinea. Am J Trop Med Hyg. 2013.
38. Michon P, Cole-Tobian JL, Dabod E, Schoepflin S, Igu J, Susapu M, et al. The risk of malarial infections and disease in Papua New Guinean children. Am J Trop Med Hyg. 2007; 76(6):997-1008. PMID: 17556601
39. Lin E, Kiniboro B, Gray L, Dobbie S, Robinson L, Laumaea A, et al. Differential patterns of infection and disease with P. falciparum and P. vivax in young Papua New Guinean children. PloS One. 2010; 5(2): e9047. doi: 10.1371/journal.pone.0009047 PMID: 20140220
40. Schoepflin S, Valsangiacomo F, Lin E, Kiniboro B, Mueller I, Felger I. Comparison of Plasmodium falciparum allelic frequency distribution in different endemic settings by high-resolution genotyping. Malaria J. 2009; 8:250.
41. Koepfli C, Ross A, Kiniboro B, Smith TA, Zimmerman PA, Siba P, et al. Multiplicity and Diversity of Plasmodium vivax Infections in a Highly Endemic Region in Papua New Guinea. PLoS Negl Trop Dis. 2011; 5(12):e1424. doi: 10.1371/journal.pntd.0001424 PMID: 22206027
42. Aguilar R, Magallon-Tejada A, Achtman AH, Moraleda C, Joice R, Cistero P, et al. Molecular evidence for the localization of Plasmodium falciparum immature gametocytes in bone marrow. Blood. 2014; 123 (7):959-66. doi: 10.1182/blood-2013-08-520767 PMID: 24335496
43. Pain A, Ferguson DJ, Kai O, Urban BC, Lowe B, Marsh K, et al. Platelet-mediated clumping of Plasmodium falciparum-infected erythrocytes is a common adhesive phenotype and is associated with severe malaria. Proc Natl Acad Sci USA. 2001; 98(4):1805-10. PMID: 11172032
44. Clements AN. The biology of mosquitoes, Volume 1: development, nutrition and reproduction.: CABI Publishing, United Kingdom; 2000. 511 p.
45. Ouedraogo AL, Schneider P, de Kruijf M, Nebie I, Verhave JP, Cuzin-Ouattara N, et al. Age-dependent distribution of Plasmodium falciparum gametocytes quantified by Pfs25 real-time QT-NASBA in a cross-sectional study in Burkina Faso. Am J Trop Med Hyg. 2007; 76(4):626-30. PMID: 17426160
46. Coleman RE, Kumpitak C, Ponlawat A, Maneechai N, Phunkitchar V, Rachapaew N, et al. Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in western Thailand. J Med Entomol. 2004; 41(2):201-8. PMID: 15061279
47. Sattabongkot J, Maneechai N, Rosenberg R. Plasmodium-Vivax - Gametocyte Infectivity of Naturally Infected Thai Adults. Parasitology. 1991; 102:27-31. PMID: 2038501
48. Sattabongkot J, Maneechai N, Phunkitchar V, Eikarat N, Khuntirat B, Sirichaisinthop J, et al. Comparison of artificial membrane feeding with direct skin feeding to estimate the infectiousness of Plasmodium vivax gametocyte carriers to mosquitoes. Am J Trop Med Hyg. 2003; 69(5):529-35. PMID: 14695091
49. Gamagemendis AC, Rajakaruna J, Carter R, Mendis KN. Infectious Reservoir of Plasmodium-Vivax and Plasmodium-Falciparum Malaria in an Endemic Region of Sri-Lanka. Am J Trop Med Hyg. 1991; 45(4):479-87. PMID: 1951856