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Published in: BMC Medicine 1/2019

Open Access 01-12-2019 | Malaria | Research article

Differential impact of malaria control interventions on P. falciparum and P. vivax infections in young Papua New Guinean children

Authors: Maria Ome-Kaius, Johanna Helena Kattenberg, Sophie Zaloumis, Matthew Siba, Benson Kiniboro, Shadrach Jally, Zahra Razook, Daisy Mantila, Desmond Sui, Jason Ginny, Anna Rosanas-Urgell, Stephan Karl, Thomas Obadia, Alyssa Barry, Stephen J. Rogerson, Moses Laman, Daniel Tisch, Ingrid Felger, James W. Kazura, Ivo Mueller, Leanne J. Robinson

Published in: BMC Medicine | Issue 1/2019

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Abstract

Introduction

As malaria transmission declines, understanding the differential impact of intensified control on Plasmodium falciparum relative to Plasmodium vivax and identifying key drivers of ongoing transmission is essential to guide future interventions.

Methods

Three longitudinal child cohorts were conducted in Papua New Guinea before (2006/2007), during (2008) and after scale-up of control interventions (2013). In each cohort, children aged 1–5 years were actively monitored for infection and illness. Incidence of malaria episodes, molecular force of blood-stage infections (molFOB) and population-averaged prevalence of infections were compared across the cohorts to investigate the impact of intensified control in young children and the key risk factors for malaria infection and illness in 2013.

Results

Between 2006 and 2008, P. falciparum infection prevalence, molFOB, and clinical malaria episodes reduced by 47%, 59% and 69%, respectively, and a further 49%, 29% and 75% from 2008 to 2013 (prevalence 41.6% to 22.1% to 11.2%; molFOB: 3.4 to 1.4 to 1.0 clones/child/year; clinical episodes incidence rate (IR) 2.6 to 0.8 to IR 0.2 episodes/child/year). P. vivax clinical episodes declined at rates comparable to P. falciparum between 2006, 2008 and 2013 (IR 2.5 to 1.1 to 0.2), while P. vivax molFOB (2006, 9.8; 2008, 12.1) and prevalence (2006, 59.6%; 2008, 65.0%) remained high in 2008. However, in 2013, P. vivax molFOB (1.2) and prevalence (19.7%) had also substantially declined. In 2013, 89% of P. falciparum and 93% of P. vivax infections were asymptomatic, 62% and 47%, respectively, were sub-microscopic. Area of residence was the major determinant of malaria infection and illness.

Conclusion

Intensified vector control and routine case management had a differential impact on rates of P. falciparum and P. vivax infections but not clinical malaria episodes in young children. This suggests comparable reductions in new mosquito-derived infections but a delayed impact on P. vivax relapsing infections due to a previously acquired reservoir of hypnozoites. This demonstrates the need to strengthen implementation of P. vivax radical cure to maximise impact of control in co-endemic areas. The high heterogeneity of malaria in 2013 highlights the importance of surveillance and targeted interventions to accelerate towards elimination.
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Literature
2.
go back to reference Coura JR, Suarez-Mutis M, Ladeia-Andrade S. A new challenge for malaria control in Brazil: asymptomatic Plasmodium infection--a review. Mem Inst Oswaldo Cruz. 2006;101(3):229–37.PubMedCrossRef Coura JR, Suarez-Mutis M, Ladeia-Andrade S. A new challenge for malaria control in Brazil: asymptomatic Plasmodium infection--a review. Mem Inst Oswaldo Cruz. 2006;101(3):229–37.PubMedCrossRef
3.
go back to reference Nguitragool W, Karl S, White M, Koepfli C, Felger I, Singhasivanon P, et al. Highly heterogeneous residual malaria risk in western Thailand. Int J Parasitol. 2019;49(6):455–62.PubMedCrossRefPubMedCentral Nguitragool W, Karl S, White M, Koepfli C, Felger I, Singhasivanon P, et al. Highly heterogeneous residual malaria risk in western Thailand. Int J Parasitol. 2019;49(6):455–62.PubMedCrossRefPubMedCentral
5.
go back to reference Harris I, Sharrock WW, Bain LM, Gray KA, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254.PubMedPubMedCentralCrossRef Harris I, Sharrock WW, Bain LM, Gray KA, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254.PubMedPubMedCentralCrossRef
6.
go back to reference Koepfli C, Ome-Kaius M, Jally S, Malau E, Maripal S, Ginny J, et al. Sustained malaria control over an 8-year period in Papua New Guinea: the challenge of low-density asymptomatic Plasmodium infections. J Infect Dis. 2017;216(11):1434–43.PubMedPubMedCentralCrossRef Koepfli C, Ome-Kaius M, Jally S, Malau E, Maripal S, Ginny J, et al. Sustained malaria control over an 8-year period in Papua New Guinea: the challenge of low-density asymptomatic Plasmodium infections. J Infect Dis. 2017;216(11):1434–43.PubMedPubMedCentralCrossRef
7.
go back to reference Waltmann A, Darcy AW, Harris I, Koepfli C, Lodo J, Vahi V, et al. 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. 2015;9(5):e0003758.PubMedPubMedCentralCrossRef Waltmann A, Darcy AW, Harris I, Koepfli C, Lodo J, Vahi V, et al. 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. 2015;9(5):e0003758.PubMedPubMedCentralCrossRef
8.
go back to reference Sattabongkot J, Suansomjit C, Nguitragool W, Sirichaisinthop J, Warit S, Tiensuwan M, et al. Prevalence of asymptomatic Plasmodium infections with sub-microscopic parasite densities in the northwestern border of Thailand: a potential threat to malaria elimination. Malar J. 2018;17(1):329.PubMedPubMedCentralCrossRef Sattabongkot J, Suansomjit C, Nguitragool W, Sirichaisinthop J, Warit S, Tiensuwan M, et al. Prevalence of asymptomatic Plasmodium infections with sub-microscopic parasite densities in the northwestern border of Thailand: a potential threat to malaria elimination. Malar J. 2018;17(1):329.PubMedPubMedCentralCrossRef
9.
go back to reference Ernst KC, Adoka SO, Kowuor DO, Wilson ML, John CC. Malaria hotspot areas in a highland Kenya site are consistent in epidemic and non-epidemic years and are associated with ecological factors. Malar J. 2006;5:78.PubMedPubMedCentralCrossRef Ernst KC, Adoka SO, Kowuor DO, Wilson ML, John CC. Malaria hotspot areas in a highland Kenya site are consistent in epidemic and non-epidemic years and are associated with ecological factors. Malar J. 2006;5:78.PubMedPubMedCentralCrossRef
10.
go back to reference Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, Mosha F, et al. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010;201(11):1764–74.PubMedCrossRef Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, Mosha F, et al. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010;201(11):1764–74.PubMedCrossRef
11.
go back to reference Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9(1):e1001165.PubMedPubMedCentralCrossRef Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9(1):e1001165.PubMedPubMedCentralCrossRef
12.
go back to reference Khantikul N, Butraporn P, Kim HS, Leemingsawat S, Tempongko MA, Suwonkerd W. Adherence to antimalarial drug therapy among vivax malaria patients in northern Thailand. J Health Popul Nutr. 2009;27(1):4–13.PubMedPubMedCentralCrossRef Khantikul N, Butraporn P, Kim HS, Leemingsawat S, Tempongko MA, Suwonkerd W. Adherence to antimalarial drug therapy among vivax malaria patients in northern Thailand. J Health Popul Nutr. 2009;27(1):4–13.PubMedPubMedCentralCrossRef
13.
go back to reference Takeuchi R, Lawpoolsri S, Imwong M, Kobayashi J, Kaewkungwal J, Pukrittayakamee S, et al. Directly-observed therapy (DOT) for the radical 14-day primaquine treatment of Plasmodium vivax malaria on the Thai-Myanmar border. Malar J. 2010;9:308.PubMedPubMedCentralCrossRef Takeuchi R, Lawpoolsri S, Imwong M, Kobayashi J, Kaewkungwal J, Pukrittayakamee S, et al. Directly-observed therapy (DOT) for the radical 14-day primaquine treatment of Plasmodium vivax malaria on the Thai-Myanmar border. Malar J. 2010;9:308.PubMedPubMedCentralCrossRef
14.
go back to reference Laman M, Aipit S, Bona C, Siba PM, Robinson LJ, Manning L, et al. Ultrasonographic assessment of splenic volume at presentation and after anti-malarial therapy in children with malarial anaemia. Malar J. 2015;14:219.PubMedPubMedCentralCrossRef Laman M, Aipit S, Bona C, Siba PM, Robinson LJ, Manning L, et al. Ultrasonographic assessment of splenic volume at presentation and after anti-malarial therapy in children with malarial anaemia. Malar J. 2015;14:219.PubMedPubMedCentralCrossRef
15.
go back to reference Mueller I, Galinski MR, Tsuboi T, Arevalo-Herrera M, Collins WE, King CL. Natural acquisition of immunity to Plasmodium vivax: epidemiological observations and potential targets. Adv Parasitol. 2013;81:77–131.PubMedCrossRef Mueller I, Galinski MR, Tsuboi T, Arevalo-Herrera M, Collins WE, King CL. Natural acquisition of immunity to Plasmodium vivax: epidemiological observations and potential targets. Adv Parasitol. 2013;81:77–131.PubMedCrossRef
16.
go back to reference Cheng Q, Cunningham J, Gatton ML. Systematic review of sub-microscopic P. vivax infections: prevalence and determining factors. PLoS Negl Trop Dis. 2015;9(1):e3413.PubMedPubMedCentralCrossRef Cheng Q, Cunningham J, Gatton ML. Systematic review of sub-microscopic P. vivax infections: prevalence and determining factors. PLoS Negl Trop Dis. 2015;9(1):e3413.PubMedPubMedCentralCrossRef
17.
go back to reference Hofmann NE, Gruenberg M, Nate E, Ura A, Rodriguez-Rodriguez D, Salib M, et al. Assessment of ultra-sensitive malaria diagnosis versus standard molecular diagnostics for malaria elimination: an in-depth molecular community cross-sectional study. Lancet Infect Dis. 2018;18(10):1108–16.PubMedCrossRef Hofmann NE, Gruenberg M, Nate E, Ura A, Rodriguez-Rodriguez D, Salib M, et al. Assessment of ultra-sensitive malaria diagnosis versus standard molecular diagnostics for malaria elimination: an in-depth molecular community cross-sectional study. Lancet Infect Dis. 2018;18(10):1108–16.PubMedCrossRef
18.
go back to reference Koepfli C, Schoepflin S, Bretscher M, Lin E, Kiniboro B, Zimmerman PA, et al. How much remains undetected? Probability of molecular detection of human plasmodia in the field. PLoS One. 2011;6(4):e19010.PubMedPubMedCentralCrossRef Koepfli C, Schoepflin S, Bretscher M, Lin E, Kiniboro B, Zimmerman PA, et al. How much remains undetected? Probability of molecular detection of human plasmodia in the field. PLoS One. 2011;6(4):e19010.PubMedPubMedCentralCrossRef
19.
go back to reference McKenzie FE, Jeffery GM, Collins WE. Plasmodium vivax blood-stage dynamics. J Parasitol. 2002;88(3):521–35.PubMedCrossRef McKenzie FE, Jeffery GM, Collins WE. Plasmodium vivax blood-stage dynamics. J Parasitol. 2002;88(3):521–35.PubMedCrossRef
20.
go back to reference Jeffery GM. The infection of mosquitoes by Plasmodium vivax (Chesson strain) during the early primary parasitemias. Am J Trop Med Hyg. 1952;1(4):612–7.PubMedCrossRef Jeffery GM. The infection of mosquitoes by Plasmodium vivax (Chesson strain) during the early primary parasitemias. Am J Trop Med Hyg. 1952;1(4):612–7.PubMedCrossRef
21.
go back to reference Bockarie MJ, Alexander N, Bockarie F, Ibam E, Barnish G, Alpers M. The late biting habit of parous Anopheles mosquitoes and pre-bedtime exposure of humans to infective female mosquitoes. Trans R Soc Trop Med Hyg. 1996;90(1):23–5.PubMedCrossRef Bockarie MJ, Alexander N, Bockarie F, Ibam E, Barnish G, Alpers M. The late biting habit of parous Anopheles mosquitoes and pre-bedtime exposure of humans to infective female mosquitoes. Trans R Soc Trop Med Hyg. 1996;90(1):23–5.PubMedCrossRef
22.
go back to reference Bockarie MJ, Dagoro H. Are insecticide-treated bednets more protective against Plasmodium falciparum than Plasmodium vivax-infected mosquitoes? Malar J. 2006;5:15.PubMedPubMedCentralCrossRef Bockarie MJ, Dagoro H. Are insecticide-treated bednets more protective against Plasmodium falciparum than Plasmodium vivax-infected mosquitoes? Malar J. 2006;5:15.PubMedPubMedCentralCrossRef
23.
go back to reference Greenwood BM. The microepidemiology of malaria and its importance to malaria control. Trans R Soc Trop Med Hyg. 1989;83(Suppl):25–9.PubMedCrossRef Greenwood BM. The microepidemiology of malaria and its importance to malaria control. Trans R Soc Trop Med Hyg. 1989;83(Suppl):25–9.PubMedCrossRef
24.
go back to reference Strickland GT, Zafar-Latif A, Fox E, Khaliq AA, Chowdhry MA. Endemic malaria in four villages of the Pakistani province of Punjab. Trans R Soc Trop Med Hyg. 1987;81(1):36–41.PubMedCrossRef Strickland GT, Zafar-Latif A, Fox E, Khaliq AA, Chowdhry MA. Endemic malaria in four villages of the Pakistani province of Punjab. Trans R Soc Trop Med Hyg. 1987;81(1):36–41.PubMedCrossRef
25.
go back to reference Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF. Human malaria transmission studies in the Anopheles punctulatus complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. Am J Trop Med Hyg. 1988;39(2):135–44.PubMedCrossRef Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF. Human malaria transmission studies in the Anopheles punctulatus complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. Am J Trop Med Hyg. 1988;39(2):135–44.PubMedCrossRef
26.
go back to reference Hii JL, Smith T, Mai A, Mellor S, Lewis D, Alexander N, et al. Spatial and temporal variation in abundance of Anopheles (Diptera:Culicidae) in a malaria endemic area in Papua New Guinea. J Med Entomol. 1997;34(2):193–205.PubMedCrossRef Hii JL, Smith T, Mai A, Mellor S, Lewis D, Alexander N, et al. Spatial and temporal variation in abundance of Anopheles (Diptera:Culicidae) in a malaria endemic area in Papua New Guinea. J Med Entomol. 1997;34(2):193–205.PubMedCrossRef
27.
go back to reference Muller I, Bockarie M, Alpers M, Smith T. The epidemiology of malaria in Papua New Guinea. Trends Parasitol. 2003;19(6):253–9.PubMedCrossRef Muller I, Bockarie M, Alpers M, Smith T. The epidemiology of malaria in Papua New Guinea. Trends Parasitol. 2003;19(6):253–9.PubMedCrossRef
28.
go back to reference Mwesigwa J, Okebe J, Affara M, Di Tanna GL, Nwakanma D, Janha O, et al. On-going malaria transmission in the Gambia despite high coverage of control interventions: a nationwide cross-sectional survey. Malar J. 2015;14:314.PubMedPubMedCentralCrossRef Mwesigwa J, Okebe J, Affara M, Di Tanna GL, Nwakanma D, Janha O, et al. On-going malaria transmission in the Gambia despite high coverage of control interventions: a nationwide cross-sectional survey. Malar J. 2015;14:314.PubMedPubMedCentralCrossRef
29.
go back to reference Roca-Feltrer A, Kwizombe CJ, Sanjoaquin MA, Sesay SS, Faragher B, Harrison J, et al. Lack of decline in childhood malaria, Malawi, 2001-2010. Emerg Infect Dis. 2012;18(2):272–8.PubMedPubMedCentralCrossRef Roca-Feltrer A, Kwizombe CJ, Sanjoaquin MA, Sesay SS, Faragher B, Harrison J, et al. Lack of decline in childhood malaria, Malawi, 2001-2010. Emerg Infect Dis. 2012;18(2):272–8.PubMedPubMedCentralCrossRef
30.
go back to reference Bautista CT, Chan AS, Ryan JR, Calampa C, Roper MH, Hightower AW, et al. Epidemiology and spatial analysis of malaria in the Northern Peruvian Amazon. Am J Trop Med Hyg. 2006;75(6):1216–22.PubMedCrossRef Bautista CT, Chan AS, Ryan JR, Calampa C, Roper MH, Hightower AW, et al. Epidemiology and spatial analysis of malaria in the Northern Peruvian Amazon. Am J Trop Med Hyg. 2006;75(6):1216–22.PubMedCrossRef
31.
go back to reference Jagannathan P, Muhindo MK, Kakuru A, Arinaitwe E, Greenhouse B, Tappero J, et al. Increasing incidence of malaria in children despite insecticide-treated bed nets and prompt anti-malarial therapy in Tororo. Uganda Malar J. 2012;11:435.PubMedCrossRef Jagannathan P, Muhindo MK, Kakuru A, Arinaitwe E, Greenhouse B, Tappero J, et al. Increasing incidence of malaria in children despite insecticide-treated bed nets and prompt anti-malarial therapy in Tororo. Uganda Malar J. 2012;11:435.PubMedCrossRef
32.
go back to reference Kazura JW, Siba PM, Betuela I, Mueller I, et al. Research Challenges and Gaps in Malaria Knowledge in Papua New Guinea. Acta Trop. 2012;121(3):274–280.PubMedCrossRef Kazura JW, Siba PM, Betuela I, Mueller I, et al. Research Challenges and Gaps in Malaria Knowledge in Papua New Guinea. Acta Trop. 2012;121(3):274–280.PubMedCrossRef
33.
go back to reference Hetzel MW, Morris H, Tarongka N, Barnadas C, Pulford J, Makita L, et al. Prevalence of malaria across Papua New Guinea after initial roll-out of insecticide-treated mosquito nets. Tropical Med Int Health. 2015;20(12):1745–55.CrossRef Hetzel MW, Morris H, Tarongka N, Barnadas C, Pulford J, Makita L, et al. Prevalence of malaria across Papua New Guinea after initial roll-out of insecticide-treated mosquito nets. Tropical Med Int Health. 2015;20(12):1745–55.CrossRef
34.
go back to reference Genton B, al-Yaman F, Beck HP, Hii J, Mellor S, Narara A, et al. The epidemiology of malaria in the Wosera area, East Sepik Province, Papua New Guinea, in preparation for vaccine trials. I. Malariometric indices and immunity. Ann Trop Med Parasitol. 1995;89(4):359–76.CrossRef Genton B, al-Yaman F, Beck HP, Hii J, Mellor S, Narara A, et al. The epidemiology of malaria in the Wosera area, East Sepik Province, Papua New Guinea, in preparation for vaccine trials. I. Malariometric indices and immunity. Ann Trop Med Parasitol. 1995;89(4):359–76.CrossRef
35.
36.
go back to reference 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. Malar J. 2012;11:192.PubMedPubMedCentralCrossRef 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. Malar J. 2012;11:192.PubMedPubMedCentralCrossRef
37.
go back to reference Hetzel MW, Pulford J, Ura Y, Jamea-Maiasa S, Tandrapah A, Tarongka N, et al. Insecticide-treated nets and malaria prevalence, Papua New Guinea, 2008-2014. Bull World Health Organ. 2017;95(10):695–705B.PubMedPubMedCentralCrossRef Hetzel MW, Pulford J, Ura Y, Jamea-Maiasa S, Tandrapah A, Tarongka N, et al. Insecticide-treated nets and malaria prevalence, Papua New Guinea, 2008-2014. Bull World Health Organ. 2017;95(10):695–705B.PubMedPubMedCentralCrossRef
38.
go back to reference Reimer LJ, Thomsen EK, Koimbu G, Keven JB, Mueller I, Siba PM, et al. Malaria transmission dynamics surrounding the first nationwide long-lasting insecticidal net distribution in Papua New Guinea. Malar J. 2016;15:25.PubMedPubMedCentralCrossRef Reimer LJ, Thomsen EK, Koimbu G, Keven JB, Mueller I, Siba PM, et al. Malaria transmission dynamics surrounding the first nationwide long-lasting insecticidal net distribution in Papua New Guinea. Malar J. 2016;15:25.PubMedPubMedCentralCrossRef
39.
go back to reference Hofmann NE, Karl S, Wampfler R, Kiniboro B, Teliki A, Iga J, et al. The complex relationship of exposure to new Plasmodium infections and incidence of clinical malaria in Papua New Guinea. Elife. 2017;6:e23708. Hofmann NE, Karl S, Wampfler R, Kiniboro B, Teliki A, Iga J, et al. The complex relationship of exposure to new Plasmodium infections and incidence of clinical malaria in Papua New Guinea. Elife. 2017;6:e23708.
40.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
41.
go back to reference Betuela I, Rosanas-Urgell A, Kiniboro B, Stanisic DI, Samol L, de Lazzari E, 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(11):1771–80.PubMedCrossRef Betuela I, Rosanas-Urgell A, Kiniboro B, Stanisic DI, Samol L, de Lazzari E, 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(11):1771–80.PubMedCrossRef
42.
go back to reference Koepfli C, Colborn KL, Kiniboro B, Lin E, Speed TP, Siba PM, et al. A high force of plasmodium vivax blood-stage infection drives the rapid acquisition of immunity in Papua new guinean children. PLoS Negl Trop Dis. 2013;7(9):e2403.PubMedPubMedCentralCrossRef Koepfli C, Colborn KL, Kiniboro B, Lin E, Speed TP, Siba PM, et al. A high force of plasmodium vivax blood-stage infection drives the rapid acquisition of immunity in Papua new guinean children. PLoS Negl Trop Dis. 2013;7(9):e2403.PubMedPubMedCentralCrossRef
43.
go back to reference Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, et al. Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Natl Acad Sci U S A. 2012;109(25):10030–5.PubMedPubMedCentralCrossRef Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, et al. Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Natl Acad Sci U S A. 2012;109(25):10030–5.PubMedPubMedCentralCrossRef
44.
go back to reference Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, et al. A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 2009;6(3):e1000048.PubMedPubMedCentralCrossRef Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, et al. A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 2009;6(3):e1000048.PubMedPubMedCentralCrossRef
45.
go back to reference Mueller I, Widmer S, Michel D, Maraga S, McNamara DT, Kiniboro B, et al. High sensitivity detection of Plasmodium species reveals positive correlations between infections of different species, shifts in age distribution and reduced local variation in Papua New Guinea. Malar J. 2009;8:41.PubMedPubMedCentralCrossRef Mueller I, Widmer S, Michel D, Maraga S, McNamara DT, Kiniboro B, et al. High sensitivity detection of Plasmodium species reveals positive correlations between infections of different species, shifts in age distribution and reduced local variation in Papua New Guinea. Malar J. 2009;8:41.PubMedPubMedCentralCrossRef
46.
go back to reference Mehlotra RK, Lorry K, Kastens W, Miller SM, Alpers MP, Bockarie M, et al. Random distribution of mixed species malaria infections in Papua New Guinea. Am J Trop Med Hyg. 2000;62(2):225–31.PubMedCrossRef Mehlotra RK, Lorry K, Kastens W, Miller SM, Alpers MP, Bockarie M, et al. Random distribution of mixed species malaria infections in Papua New Guinea. Am J Trop Med Hyg. 2000;62(2):225–31.PubMedCrossRef
47.
go back to reference Paediatric society of PNG. Standard treatment for common illness of children in Papua New Guinea: a manual for nurses, community health workers, health extension officers, and doctors. 8th ed.2006. Paediatric society of PNG. Standard treatment for common illness of children in Papua New Guinea: a manual for nurses, community health workers, health extension officers, and doctors. 8th ed.2006.
48.
go back to reference Paediatric society of PNG. Standard treatment for common illness of children in Papua New Guinea: a manual for nurses, community health workers, health extension officers, and doctors 9th ed.2011. Paediatric society of PNG. Standard treatment for common illness of children in Papua New Guinea: a manual for nurses, community health workers, health extension officers, and doctors 9th ed.2011.
49.
go back to reference 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. Malar J. 2010;9:361.PubMedPubMedCentralCrossRef 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. Malar J. 2010;9:361.PubMedPubMedCentralCrossRef
50.
go back to reference 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):e76316.PubMedPubMedCentralCrossRef 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):e76316.PubMedPubMedCentralCrossRef
51.
go back to reference White MT, Karl S, Koepfli C, Longley RJ, Hofmann NE, Wampfler R, et al. Plasmodium vivax and Plasmodium falciparum infection dynamics: re-infections, recrudescences and relapses. Malar J. 2018;17(1):170.PubMedPubMedCentralCrossRef White MT, Karl S, Koepfli C, Longley RJ, Hofmann NE, Wampfler R, et al. Plasmodium vivax and Plasmodium falciparum infection dynamics: re-infections, recrudescences and relapses. Malar J. 2018;17(1):170.PubMedPubMedCentralCrossRef
52.
go back to reference Kamya MR, Arinaitwe E, Wanzira H, Katureebe A, Barusya C, Kigozi SP, et al. Malaria transmission, infection, and disease at three sites with varied transmission intensity in Uganda: implications for malaria control. Am J Trop Med Hyg. 2015;92(5):903–12.PubMedPubMedCentralCrossRef Kamya MR, Arinaitwe E, Wanzira H, Katureebe A, Barusya C, Kigozi SP, et al. Malaria transmission, infection, and disease at three sites with varied transmission intensity in Uganda: implications for malaria control. Am J Trop Med Hyg. 2015;92(5):903–12.PubMedPubMedCentralCrossRef
53.
go back to reference Collins WE, Jeffery GM, Roberts JM. A retrospective examination of reinfection of humans with Plasmodium vivax. Am J Trop Med Hyg. 2004;70(6):642–4.PubMedCrossRef Collins WE, Jeffery GM, Roberts JM. A retrospective examination of reinfection of humans with Plasmodium vivax. Am J Trop Med Hyg. 2004;70(6):642–4.PubMedCrossRef
55.
go back to reference 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(7):934–41.PubMedCrossRef 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(7):934–41.PubMedCrossRef
56.
go back to reference Wells TN, Burrows JN, Baird JK. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol. 2010;26(3):145–51.PubMedCrossRef Wells TN, Burrows JN, Baird JK. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol. 2010;26(3):145–51.PubMedCrossRef
57.
go back to reference Cooper RD, Waterson DG, Frances SP, Beebe NW, Sweeney AW. Speciation and distribution of the members of the Anopheles punctulatus (Diptera: Culicidae) group in Papua New Guinea. J Med Entomol. 2002;39(1):16–27.PubMedCrossRef Cooper RD, Waterson DG, Frances SP, Beebe NW, Sweeney AW. Speciation and distribution of the members of the Anopheles punctulatus (Diptera: Culicidae) group in Papua New Guinea. J Med Entomol. 2002;39(1):16–27.PubMedCrossRef
58.
go back to reference Alves FP, Gil LH, Marrelli MT, Ribolla PE, Camargo EP, Da Silva LH. Asymptomatic carriers of Plasmodium spp. as infection source for malaria vector mosquitoes in the Brazilian Amazon. J Med Entomol. 2005;42(5):777–9.PubMedCrossRef Alves FP, Gil LH, Marrelli MT, Ribolla PE, Camargo EP, Da Silva LH. Asymptomatic carriers of Plasmodium spp. as infection source for malaria vector mosquitoes in the Brazilian Amazon. J Med Entomol. 2005;42(5):777–9.PubMedCrossRef
59.
go back to reference Somboon P, Lines J, Aramrattana A, Chitprarop U, Prajakwong S, Khamboonrua C. Entomological evaluation of community-wide use of lambdacyhalothrine-impregnated bed nets against malaria in a border area of north-west Thailand. Trans R Soc Trop Med Hyg. 1995;89:248–54.PubMedCrossRef Somboon P, Lines J, Aramrattana A, Chitprarop U, Prajakwong S, Khamboonrua C. Entomological evaluation of community-wide use of lambdacyhalothrine-impregnated bed nets against malaria in a border area of north-west Thailand. Trans R Soc Trop Med Hyg. 1995;89:248–54.PubMedCrossRef
60.
go back to reference Cui L, Yan G, Sattabongkot J, Cao Y, Chen B, Chen X, et al. Malaria in the greater Mekong subregion: heterogeneity and complexity. Acta Trop. 2012;121(3):227–39.PubMedCrossRef Cui L, Yan G, Sattabongkot J, Cao Y, Chen B, Chen X, et al. Malaria in the greater Mekong subregion: heterogeneity and complexity. Acta Trop. 2012;121(3):227–39.PubMedCrossRef
61.
go back to reference Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap T, Patil AP, Temperley WH, et al. The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2011;4:89.PubMedPubMedCentralCrossRef Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap T, Patil AP, Temperley WH, et al. The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2011;4:89.PubMedPubMedCentralCrossRef
62.
go back to reference Cook J, Grignard L, Al-Eryani S, Al-Selwei M, Mnzava A, Al-Yarie H, et al. High heterogeneity of malaria transmission and a large sub-patent and diverse reservoir of infection in Wusab as Safil district, Republic of Yemen. Malar J. 2016;15:193.PubMedPubMedCentralCrossRef Cook J, Grignard L, Al-Eryani S, Al-Selwei M, Mnzava A, Al-Yarie H, et al. High heterogeneity of malaria transmission and a large sub-patent and diverse reservoir of infection in Wusab as Safil district, Republic of Yemen. Malar J. 2016;15:193.PubMedPubMedCentralCrossRef
63.
go back to reference Okell LC, Ghani AC, Lyons E, Drakeley CJ. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis. 2009;200(10):1509–17.PubMedCrossRef Okell LC, Ghani AC, Lyons E, Drakeley CJ. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis. 2009;200(10):1509–17.PubMedCrossRef
64.
go back to reference Okell LC, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun. 2012;3:1237.PubMedCrossRef Okell LC, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun. 2012;3:1237.PubMedCrossRef
65.
go back to reference Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti-Infect Ther. 2013;11(6):623–39.PubMedCrossRef Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti-Infect Ther. 2013;11(6):623–39.PubMedCrossRef
Metadata
Title
Differential impact of malaria control interventions on P. falciparum and P. vivax infections in young Papua New Guinean children
Authors
Maria Ome-Kaius
Johanna Helena Kattenberg
Sophie Zaloumis
Matthew Siba
Benson Kiniboro
Shadrach Jally
Zahra Razook
Daisy Mantila
Desmond Sui
Jason Ginny
Anna Rosanas-Urgell
Stephan Karl
Thomas Obadia
Alyssa Barry
Stephen J. Rogerson
Moses Laman
Daniel Tisch
Ingrid Felger
James W. Kazura
Ivo Mueller
Leanne J. Robinson
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2019
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-019-1456-9

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