Skip to main content
Top
Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Asymptomatic Plasmodium vivax infections induce robust IgG responses to multiple blood-stage proteins in a low-transmission region of western Thailand

Authors: Rhea J. Longley, Camila T. França, Michael T. White, Chalermpon Kumpitak, Patiwat Sa-angchai, Jakub Gruszczyk, Jessica B. Hostetler, Anjali Yadava, Christopher L. King, Rick M. Fairhurst, Julian C. Rayner, Wai-Hong Tham, Wang Nguitragool, Jetsumon Sattabongkot, Ivo Mueller

Published in: Malaria Journal | Issue 1/2017

Login to get access

Abstract

Background

Thailand is aiming to eliminate malaria by the year 2024. Plasmodium vivax has now become the dominant species causing malaria within the country, and a high proportion of infections are asymptomatic. A better understanding of antibody dynamics to P. vivax antigens in a low-transmission setting, where acquired immune responses are poorly characterized, will be pivotal for developing new strategies for elimination, such as improved surveillance methods and vaccines. The objective of this study was to characterize total IgG antibody levels to 11 key P. vivax proteins in a village of western Thailand.

Methods

Plasma samples from 546 volunteers enrolled in a cross-sectional survey conducted in 2012 in Kanchanaburi Province were utilized. Total IgG levels to 11 different proteins known or predicted to be involved in reticulocyte binding or invasion (ARP, GAMA, P41, P12, PVX_081550, and five members of the PvRBP family), as well as the leading pre-erythrocytic vaccine candidate (CSP) were measured using a multiplexed bead-based assay. Associations between IgG levels and infection status, age, and spatial location were explored.

Results

Individuals from a low-transmission region of western Thailand reacted to all 11 P. vivax recombinant proteins. Significantly greater IgG levels were observed in the presence of a current P. vivax infection, despite all infected individuals being asymptomatic. IgG levels were also higher in adults (18 years and older) than in children. For most of the proteins, higher IgG levels were observed in individuals living closer to the Myanmar border and further away from local health services.

Conclusions

Robust IgG responses were observed to most proteins and IgG levels correlated with surrogates of exposure, suggesting these antigens may serve as potential biomarkers of exposure, immunity, or both.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO. World malaria report. Geneva: World Health Organization; 2016. WHO. World malaria report. Geneva: World Health Organization; 2016.
2.
go back to reference Sattabongkot J, Tsuboi T, Zollner GE, Sirichaisinthop J, Cui L. Plasmodium vivax transmission: chances for control? Trends Parasitol. 2004;20:192–8.CrossRefPubMed Sattabongkot J, Tsuboi T, Zollner GE, Sirichaisinthop J, Cui L. Plasmodium vivax transmission: chances for control? Trends Parasitol. 2004;20:192–8.CrossRefPubMed
3.
go back to reference Parker DM, Matthews SA, Yan G, Zhou G, Lee MC, Sirichaisinthop J, et al. Microgeography and molecular epidemiology of malaria at the Thailand–Myanmar border in the malaria pre-elimination phase. Malar J. 2015;14:198.CrossRefPubMedPubMedCentral Parker DM, Matthews SA, Yan G, Zhou G, Lee MC, Sirichaisinthop J, et al. Microgeography and molecular epidemiology of malaria at the Thailand–Myanmar border in the malaria pre-elimination phase. Malar J. 2015;14:198.CrossRefPubMedPubMedCentral
4.
go back to reference Jennison C, Arnott A, Tessier N, Tavul L, Koepfli C, Felger I, et al. Plasmodium vivax populations are more genetically diverse and less structured than sympatric Plasmodium falciparum populations. PLoS Negl Trop Dis. 2015;9:e0003634.CrossRefPubMedPubMedCentral Jennison C, Arnott A, Tessier N, Tavul L, Koepfli C, Felger I, et al. Plasmodium vivax populations are more genetically diverse and less structured than sympatric Plasmodium falciparum populations. PLoS Negl Trop Dis. 2015;9:e0003634.CrossRefPubMedPubMedCentral
5.
go back to reference Cook J, Speybroeck N, Sochanta T, Somony H, Sokny M, Claes F, et al. Sero-epidemiological evaluation of changes in Plasmodium falciparum and Plasmodium vivax transmission patterns over the rainy season in Cambodia. Malar J. 2012;11:86.CrossRefPubMedPubMedCentral Cook J, Speybroeck N, Sochanta T, Somony H, Sokny M, Claes F, et al. Sero-epidemiological evaluation of changes in Plasmodium falciparum and Plasmodium vivax transmission patterns over the rainy season in Cambodia. Malar J. 2012;11:86.CrossRefPubMedPubMedCentral
6.
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:e0003758.CrossRefPubMedPubMedCentral 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:e0003758.CrossRefPubMedPubMedCentral
7.
go back to reference Longley RJ, Sattabongkot J, Mueller I. Insights into the naturally acquired immune response to Plasmodium vivax malaria. Parasitology. 2016;143(2):154–70.CrossRefPubMed Longley RJ, Sattabongkot J, Mueller I. Insights into the naturally acquired immune response to Plasmodium vivax malaria. Parasitology. 2016;143(2):154–70.CrossRefPubMed
8.
go back to reference Chootong P, Panichakul T, Permmongkol C, Barnes SJ, Udomsangpetch R, Adams JH. Characterization of inhibitory anti-Duffy binding protein II immunity: approach to Plasmodium vivax vaccine development in Thailand. PLoS ONE. 2012;7:e35769.CrossRefPubMedPubMedCentral Chootong P, Panichakul T, Permmongkol C, Barnes SJ, Udomsangpetch R, Adams JH. Characterization of inhibitory anti-Duffy binding protein II immunity: approach to Plasmodium vivax vaccine development in Thailand. PLoS ONE. 2012;7:e35769.CrossRefPubMedPubMedCentral
9.
go back to reference Pitabut N, Panichakorn J, Mahakunkijcharoen Y, Hirunpetcharat C, Looareesuwan S, Khusmith S. IgG antibody profile to c-terminal region of Plasmodium vivax merozoite surface protein-1 in Thai individuals exposed to malaria. Southeast Asian J Trop Med Public Health. 2007;38:1–7.PubMed Pitabut N, Panichakorn J, Mahakunkijcharoen Y, Hirunpetcharat C, Looareesuwan S, Khusmith S. IgG antibody profile to c-terminal region of Plasmodium vivax merozoite surface protein-1 in Thai individuals exposed to malaria. Southeast Asian J Trop Med Public Health. 2007;38:1–7.PubMed
10.
go back to reference Sungkapong T, Culleton R, Yahata K, Tachibana M, Ruengveerayuth R, Udomsangpetch R, et al. Humoral immune responses to Plasmodium vivax subtelomeric transmembrane proteins in Thailand. Southeast Asian J Trop Med Public Health. 2011;42:1313–21.PubMed Sungkapong T, Culleton R, Yahata K, Tachibana M, Ruengveerayuth R, Udomsangpetch R, et al. Humoral immune responses to Plasmodium vivax subtelomeric transmembrane proteins in Thailand. Southeast Asian J Trop Med Public Health. 2011;42:1313–21.PubMed
11.
go back to reference Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Davies DH, Jain A, et al. Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand—molecular and serological evidence. Malar J. 2015;14:95.CrossRefPubMedPubMedCentral Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Davies DH, Jain A, et al. Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand—molecular and serological evidence. Malar J. 2015;14:95.CrossRefPubMedPubMedCentral
12.
go back to reference Wipasa J, Suphavilai C, Okell LC, Cook J, Corran PH, Thaikla K, et al. Long-lived antibody and B Cell memory responses to the human malaria parasites, Plasmodium falciparum and Plasmodium vivax. PLoS Pathog. 2010;6:e1000770.CrossRefPubMedPubMedCentral Wipasa J, Suphavilai C, Okell LC, Cook J, Corran PH, Thaikla K, et al. Long-lived antibody and B Cell memory responses to the human malaria parasites, Plasmodium falciparum and Plasmodium vivax. PLoS Pathog. 2010;6:e1000770.CrossRefPubMedPubMedCentral
13.
go back to reference Longley RJ, Reyes-Sandoval A, Montoya-Diaz E, Dunachie S, Kumpitak C, Nguitragool W, et al. Acquisition and longevity of antibodies to Plasmodium vivax pre-erythrocytic antigens in western Thailand. Clin Vaccine Immunol. 2015;9:117–24. Longley RJ, Reyes-Sandoval A, Montoya-Diaz E, Dunachie S, Kumpitak C, Nguitragool W, et al. Acquisition and longevity of antibodies to Plasmodium vivax pre-erythrocytic antigens in western Thailand. Clin Vaccine Immunol. 2015;9:117–24.
14.
go back to reference Arumugam TU, Takeo S, Yamasaki T, Thonkukiatkul A, Miura K, Otsuki H, et al. Discovery of GAMA, a Plasmodium falciparum merozoite micronemal protein, as a novel blood-stage vaccine candidate antigen. Infect Immun. 2011;79:4523–32.CrossRefPubMedPubMedCentral Arumugam TU, Takeo S, Yamasaki T, Thonkukiatkul A, Miura K, Otsuki H, et al. Discovery of GAMA, a Plasmodium falciparum merozoite micronemal protein, as a novel blood-stage vaccine candidate antigen. Infect Immun. 2011;79:4523–32.CrossRefPubMedPubMedCentral
15.
go back to reference Garcia J, Curtidor H, Pinzon CG, Vanegas M, Moreno A, Patarroyo ME. Identification of conserved erythrocyte binding regions in members of the Plasmodium falciparum Cys6 lipid raft-associated protein family. Vaccine. 2009;27:3953–62.CrossRefPubMed Garcia J, Curtidor H, Pinzon CG, Vanegas M, Moreno A, Patarroyo ME. Identification of conserved erythrocyte binding regions in members of the Plasmodium falciparum Cys6 lipid raft-associated protein family. Vaccine. 2009;27:3953–62.CrossRefPubMed
16.
go back to reference Sanders PR, Gilson PR, Cantin GT, Greenbaum DC, Nebl T, Carucci DJ, et al. Distinct protein classes including novel merozoite surface antigens in Raft-like membranes of Plasmodium falciparum. J Biol Chem. 2005;280:40169–76.CrossRefPubMed Sanders PR, Gilson PR, Cantin GT, Greenbaum DC, Nebl T, Carucci DJ, et al. Distinct protein classes including novel merozoite surface antigens in Raft-like membranes of Plasmodium falciparum. J Biol Chem. 2005;280:40169–76.CrossRefPubMed
17.
go back to reference Wickramarachchi T, Devi YS, Mohmmed A, Chauhan VS. Identification and characterization of a novel Plasmodium falciparum merozoite apical protein involved in erythrocyte binding and invasion. PLoS ONE. 2008;3:e1732.CrossRefPubMedPubMedCentral Wickramarachchi T, Devi YS, Mohmmed A, Chauhan VS. Identification and characterization of a novel Plasmodium falciparum merozoite apical protein involved in erythrocyte binding and invasion. PLoS ONE. 2008;3:e1732.CrossRefPubMedPubMedCentral
18.
go back to reference Hietanen J, Chim-Ong A, Chiramanewong T, Gruszczyk J, Roobsoong W, Tham WH, et al. Gene models, expression repertoire, and immune response of Plasmodium vivax reticulocyte binding proteins. Infect Immun. 2015;84:677–85.CrossRefPubMed Hietanen J, Chim-Ong A, Chiramanewong T, Gruszczyk J, Roobsoong W, Tham WH, et al. Gene models, expression repertoire, and immune response of Plasmodium vivax reticulocyte binding proteins. Infect Immun. 2015;84:677–85.CrossRefPubMed
19.
go back to reference Gruszczyk J, Lim NT, Arnott A, He WQ, Nguitragool W, Roobsoong W, et al. Structurally conserved erythrocyte-binding domain in Plasmodium provides a versatile scaffold for alternate receptor engagement. Proc Natl Acad Sci USA. 2016;113:E191–200.CrossRefPubMed Gruszczyk J, Lim NT, Arnott A, He WQ, Nguitragool W, Roobsoong W, et al. Structurally conserved erythrocyte-binding domain in Plasmodium provides a versatile scaffold for alternate receptor engagement. Proc Natl Acad Sci USA. 2016;113:E191–200.CrossRefPubMed
20.
go back to reference Rts SC. Efficacy and safety of RTS, S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet. 2015;386:31–45.CrossRef Rts SC. Efficacy and safety of RTS, S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet. 2015;386:31–45.CrossRef
21.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
22.
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:e76316.CrossRefPubMedPubMedCentral 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:e76316.CrossRefPubMedPubMedCentral
23.
go back to reference Hostetler JB, Sharma S, Bartholdson SJ, Wright GJ, Fairhurst RM, Rayner JC. A library of Plasmodium vivax recombinant merozoite proteins reveals new vaccine candidates and protein–protein interactions. PLoS Negl Trop Dis. 2015;9:e0004264.CrossRefPubMedPubMedCentral Hostetler JB, Sharma S, Bartholdson SJ, Wright GJ, Fairhurst RM, Rayner JC. A library of Plasmodium vivax recombinant merozoite proteins reveals new vaccine candidates and protein–protein interactions. PLoS Negl Trop Dis. 2015;9:e0004264.CrossRefPubMedPubMedCentral
24.
go back to reference Yadava A, Sattabongkot J, Washington MA, Ware LA, Majam V, Zheng H, et al. A novel chimeric Plasmodium vivax circumsporozoite protein induces biologically functional antibodies that recognize both VK210 and VK247 sporozoites. Infect Immun. 2007;75:1177–85.CrossRefPubMed Yadava A, Sattabongkot J, Washington MA, Ware LA, Majam V, Zheng H, et al. A novel chimeric Plasmodium vivax circumsporozoite protein induces biologically functional antibodies that recognize both VK210 and VK247 sporozoites. Infect Immun. 2007;75:1177–85.CrossRefPubMed
25.
go back to reference Franca CT, He WQ, Gruszczyk J, Lim NT, Lin E, Kiniboro B, et al. Plasmodium vivax reticulocyte binding proteins are key targets of naturally acquired immunity in young Papua New Guinean children. PLoS Negl Trop Dis. 2016;10:e0005014.CrossRefPubMedPubMedCentral Franca CT, He WQ, Gruszczyk J, Lim NT, Lin E, Kiniboro B, et al. Plasmodium vivax reticulocyte binding proteins are key targets of naturally acquired immunity in young Papua New Guinean children. PLoS Negl Trop Dis. 2016;10:e0005014.CrossRefPubMedPubMedCentral
26.
go back to reference Franca CT, Hostetler JB, Sharma S, White MT, Lin E, Kiniboro B, et al. An antibody screen of a Plasmodium vivax antigen library identifies novel merozoite proteins associated with clinical protection. PLoS Negl Trop Dis. 2016;10:e0004639.CrossRefPubMedPubMedCentral Franca CT, Hostetler JB, Sharma S, White MT, Lin E, Kiniboro B, et al. An antibody screen of a Plasmodium vivax antigen library identifies novel merozoite proteins associated with clinical protection. PLoS Negl Trop Dis. 2016;10:e0004639.CrossRefPubMedPubMedCentral
27.
go back to reference Yadava A, Hall CE, Sullivan JS, Nace D, Williams T, Collins WE, et al. Protective efficacy of a Plasmodium vivax circumsporozoite protein-based vaccine in Aotus nancymaae is associated with antibodies to the repeat region. PLoS Negl Trop Dis. 2014;8:e3268.CrossRefPubMedPubMedCentral Yadava A, Hall CE, Sullivan JS, Nace D, Williams T, Collins WE, et al. Protective efficacy of a Plasmodium vivax circumsporozoite protein-based vaccine in Aotus nancymaae is associated with antibodies to the repeat region. PLoS Negl Trop Dis. 2014;8:e3268.CrossRefPubMedPubMedCentral
28.
go back to reference Crosnier C, Wanaguru M, McDade B, Osier FH, Marsh K, Rayner JC, et al. A library of functional recombinant cell-surface and secreted P. falciparum merozoite proteins. Mol Cell Proteom. 2013;12:3976–86.CrossRef Crosnier C, Wanaguru M, McDade B, Osier FH, Marsh K, Rayner JC, et al. A library of functional recombinant cell-surface and secreted P. falciparum merozoite proteins. Mol Cell Proteom. 2013;12:3976–86.CrossRef
29.
go back to reference Yman V, White MT, Rono J, Arca B, Osier FH, Troye-Blomberg M, et al. Antibody acquisition models: a new tool for serological surveillance of malaria transmission intensity. Sci Rep. 2016;6:19472.CrossRefPubMedPubMedCentral Yman V, White MT, Rono J, Arca B, Osier FH, Troye-Blomberg M, et al. Antibody acquisition models: a new tool for serological surveillance of malaria transmission intensity. Sci Rep. 2016;6:19472.CrossRefPubMedPubMedCentral
30.
go back to reference Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575–82.CrossRefPubMed Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575–82.CrossRefPubMed
31.
go back to reference King CL, Davies DH, Felgner P, Baum E, Jain A, Randall A, et al. Biosignatures of exposure/transmission and immunity. Am J Trop Med Hyg. 2015;93:16–27.CrossRefPubMedPubMedCentral King CL, Davies DH, Felgner P, Baum E, Jain A, Randall A, et al. Biosignatures of exposure/transmission and immunity. Am J Trop Med Hyg. 2015;93:16–27.CrossRefPubMedPubMedCentral
32.
go back to reference Cheng Y, Lu F, Tsuboi T, Han ET. Characterization of a novel merozoite surface protein of Plasmodium vivax, Pv41. Acta Trop. 2013;126:222–8.CrossRefPubMed Cheng Y, Lu F, Tsuboi T, Han ET. Characterization of a novel merozoite surface protein of Plasmodium vivax, Pv41. Acta Trop. 2013;126:222–8.CrossRefPubMed
34.
go back to reference van Ooij C, Withers-Martinez C, Ringel A, Cockcroft S, Haldar K, Blackman MJ. Identification of a Plasmodium falciparum phospholipid transfer protein. J Biol Chem. 2013;288:31971–83.CrossRefPubMedPubMedCentral van Ooij C, Withers-Martinez C, Ringel A, Cockcroft S, Haldar K, Blackman MJ. Identification of a Plasmodium falciparum phospholipid transfer protein. J Biol Chem. 2013;288:31971–83.CrossRefPubMedPubMedCentral
35.
go back to reference Ladeia-Andrade S, Ferreira MU, Scopel KK, Braga EM, Bastos MDS, Wunderlich G, et al. Naturally acquired antibodies to merozoite surface protein (MSP)-1(19) and cumulative exposure to Plasmodium falciparum and Plasmodium vivax in remote populations of the Amazon Basin of Brazil. Mem Inst Oswaldo Cruz. 2007;102:943–51.CrossRefPubMed Ladeia-Andrade S, Ferreira MU, Scopel KK, Braga EM, Bastos MDS, Wunderlich G, et al. Naturally acquired antibodies to merozoite surface protein (MSP)-1(19) and cumulative exposure to Plasmodium falciparum and Plasmodium vivax in remote populations of the Amazon Basin of Brazil. Mem Inst Oswaldo Cruz. 2007;102:943–51.CrossRefPubMed
36.
go back to reference Lima-Junior JC, Tran TM, Meyer EV, Singh B, De-Simone SG, Santos F, et al. Naturally acquired humoral and cellular immune responses to Plasmodium vivax merozoite surface protein 9 in Northwestern Amazon individuals. Vaccine. 2008;26:6645–54.CrossRefPubMedPubMedCentral Lima-Junior JC, Tran TM, Meyer EV, Singh B, De-Simone SG, Santos F, et al. Naturally acquired humoral and cellular immune responses to Plasmodium vivax merozoite surface protein 9 in Northwestern Amazon individuals. Vaccine. 2008;26:6645–54.CrossRefPubMedPubMedCentral
37.
go back to reference Nogueira PA, Alves FP, Fernandez-Becerra C, Pein O, Santos NR, da Silva LHP, et al. A reduced risk of infection with Plasmodium vivax and clinical protection against malaria are associated with antibodies against the N terminus but not the C terminus of merozoite surface protein 1. Infect Immun. 2006;74:2726–33.CrossRefPubMedPubMedCentral Nogueira PA, Alves FP, Fernandez-Becerra C, Pein O, Santos NR, da Silva LHP, et al. A reduced risk of infection with Plasmodium vivax and clinical protection against malaria are associated with antibodies against the N terminus but not the C terminus of merozoite surface protein 1. Infect Immun. 2006;74:2726–33.CrossRefPubMedPubMedCentral
38.
go back to reference Xainli J, Cole-Tobian JL, Baisor M, Kastens W, Bockarie M, Yazdani SS, et al. Epitope-specific humoral immunity to Plasmodium vivax Duffy binding protein. Infect Immun. 2003;71:2508–15.CrossRefPubMedPubMedCentral Xainli J, Cole-Tobian JL, Baisor M, Kastens W, Bockarie M, Yazdani SS, et al. Epitope-specific humoral immunity to Plasmodium vivax Duffy binding protein. Infect Immun. 2003;71:2508–15.CrossRefPubMedPubMedCentral
39.
go back to reference Zakeri S, Babaeekhou L, Mehrizi AA, Abbasi M, Djadid ND. Antibody responses and avidity of naturally acquired anti-Plasmodium vivax Duffy binding protein (PvDBP) antibodies in individuals from an area with unstable malaria transmission. Am J Trop Med Hyg. 2011;84:944–50.CrossRefPubMedPubMedCentral Zakeri S, Babaeekhou L, Mehrizi AA, Abbasi M, Djadid ND. Antibody responses and avidity of naturally acquired anti-Plasmodium vivax Duffy binding protein (PvDBP) antibodies in individuals from an area with unstable malaria transmission. Am J Trop Med Hyg. 2011;84:944–50.CrossRefPubMedPubMedCentral
40.
go back to reference Elliott SR, Fowkes FJ, Richards JS, Reiling L, Drew DR, Beeson JG. Research priorities for the development and implementation of serological tools for malaria surveillance. F1000Prime Rep. 2014;6:100.CrossRefPubMedPubMedCentral Elliott SR, Fowkes FJ, Richards JS, Reiling L, Drew DR, Beeson JG. Research priorities for the development and implementation of serological tools for malaria surveillance. F1000Prime Rep. 2014;6:100.CrossRefPubMedPubMedCentral
Metadata
Title
Asymptomatic Plasmodium vivax infections induce robust IgG responses to multiple blood-stage proteins in a low-transmission region of western Thailand
Authors
Rhea J. Longley
Camila T. França
Michael T. White
Chalermpon Kumpitak
Patiwat Sa-angchai
Jakub Gruszczyk
Jessica B. Hostetler
Anjali Yadava
Christopher L. King
Rick M. Fairhurst
Julian C. Rayner
Wai-Hong Tham
Wang Nguitragool
Jetsumon Sattabongkot
Ivo Mueller
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-1826-8

Other articles of this Issue 1/2017

Malaria Journal 1/2017 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.