Skip to main content
Top
Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Research

Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand - molecular and serological evidence

Authors: Elisabeth Baum, Jetsumon Sattabongkot, Jeeraphat Sirichaisinthop, Kirakorn Kiattibutr, D Huw Davies, Aarti Jain, Eugenia Lo, Ming-Chieh Lee, Arlo Z Randall, Douglas M Molina, Xiaowu Liang, Liwang Cui, Philip L Felgner, Guiyun Yan

Published in: Malaria Journal | Issue 1/2015

Login to get access

Abstract

Background

Malaria is a public health problem in parts of Thailand, where Plasmodium falciparum and Plasmodium vivax are the main causes of infection. In the northwestern border province of Tak parasite prevalence is now estimated to be less than 1% by microscopy. Nonetheless, microscopy is insensitive at low-level parasitaemia. The objective of this study was to assess the current epidemiology of falciparum and vivax malaria in Tak using molecular methods to detect exposure to and infection with parasites; in particular, the prevalence of asymptomatic infections and infections with submicroscopic parasite levels.

Methods

Three-hundred microlitres of whole blood from finger-prick were collected into capillary tubes from residents of a sentinel village and from patients at a malaria clinic. Pelleted cellular fractions were screened by quantitative PCR to determine parasite prevalence, while plasma was probed on a protein microarray displaying hundreds of P. falciparum and P. vivax proteins to obtain antibody response profiles in those individuals.

Results

Of 219 samples from the village, qPCR detected 25 (11.4%) Plasmodium sp. infections, of which 92% were asymptomatic and 100% were submicroscopic. Of 61 samples from the clinic patients, 27 (44.3%) were positive by qPCR, of which 25.9% had submicroscopic parasite levels. Cryptic mixed infections, misdiagnosed as single-species infections by microscopy, were found in 7 (25.9%) malaria patients. All sample donors, parasitaemic and non-parasitaemic alike, had serological evidence of parasite exposure, with 100% seropositivity to at least 54 antigens. Antigens significantly associated with asymptomatic infections were P. falciparum MSP2, DnaJ protein, putative E1E2 ATPase, and three others.

Conclusion

These findings suggest that parasite prevalence is higher than currently estimated by local authorities based on the standard light microscopy. As transmission levels drop in Thailand, it may be necessary to employ higher throughput and sensitivity methods for parasite detection in the phase of malaria elimination.
Appendix
Available only for authorised users
Literature
1.
go back to reference Jongwutiwes S, Buppan P, Kosuvin R, Seethamchai S, Pattanawong U, Sirichaisinthop J, et al. Plasmodium knowlesi malaria in humans and macaques, Thailand. Emerg Infect Dis. 2011;17:1799–806.CrossRefPubMedCentralPubMed Jongwutiwes S, Buppan P, Kosuvin R, Seethamchai S, Pattanawong U, Sirichaisinthop J, et al. Plasmodium knowlesi malaria in humans and macaques, Thailand. Emerg Infect Dis. 2011;17:1799–806.CrossRefPubMedCentralPubMed
2.
go back to reference Putaporntip C, Hongsrimuang T, Seethamchai S, Kobasa T, Limkittikul K, Cui L, et al. Differential prevalence of Plasmodium infections and cryptic Plasmodium knowlesi malaria in humans in Thailand. J Infect Dis. 2009;199:1143–50.CrossRefPubMed Putaporntip C, Hongsrimuang T, Seethamchai S, Kobasa T, Limkittikul K, Cui L, et al. Differential prevalence of Plasmodium infections and cryptic Plasmodium knowlesi malaria in humans in Thailand. J Infect Dis. 2009;199:1143–50.CrossRefPubMed
3.
go back to reference Cui L, Yan G, Sattabongkot J, Chen B, Cao Y, Fan Q, et al. Challenges and prospects for malaria elimination in the Greater Mekong Subregion. Acta Trop. 2012;121:240–5.CrossRefPubMedCentralPubMed Cui L, Yan G, Sattabongkot J, Chen B, Cao Y, Fan Q, et al. Challenges and prospects for malaria elimination in the Greater Mekong Subregion. Acta Trop. 2012;121:240–5.CrossRefPubMedCentralPubMed
4.
go back to reference malERA Consultative Group on Diagnoses and Diagnostics. A research agenda for malaria eradication: diagnoses and diagnostics. PLoS Med. 2011;8:e1000396.CrossRef malERA Consultative Group on Diagnoses and Diagnostics. A research agenda for malaria eradication: diagnoses and diagnostics. PLoS Med. 2011;8:e1000396.CrossRef
5.
go back to reference Moonen B, Cohen JM, Snow RW, Slutsker L, Drakeley C, Smith DL, et al. Operational strategies to achieve and maintain malaria elimination. Lancet. 2010;376:1592–603.CrossRefPubMedCentralPubMed Moonen B, Cohen JM, Snow RW, Slutsker L, Drakeley C, Smith DL, et al. Operational strategies to achieve and maintain malaria elimination. Lancet. 2010;376:1592–603.CrossRefPubMedCentralPubMed
7.
go back to reference WHO. World Malaria Report 2012. Geneva: World Health Organization; 2012. WHO. World Malaria Report 2012. Geneva: World Health Organization; 2012.
8.
go back to reference Konchom S, Singhasivanon P, Kaewkungwal J, Chupraphawan S, Thimasarn K, Kidson C, et al. Trend of malaria incidence in highly endemic provinces along the Thai borders, 1991–2001. Southeast Asian J Trop Med Public Health. 2003;34:486–94.PubMed Konchom S, Singhasivanon P, Kaewkungwal J, Chupraphawan S, Thimasarn K, Kidson C, et al. Trend of malaria incidence in highly endemic provinces along the Thai borders, 1991–2001. Southeast Asian J Trop Med Public Health. 2003;34:486–94.PubMed
10.
go back to reference Zhou G, Sirichaisinthop J, Sattabongkot J, Jones J, Bjornstad ON, Yan G, et al. Spatio-temporal distribution of Plasmodium falciparum and P. vivax malaria in Thailand. Am J Trop Med Hyg. 2005;72:256–62.PubMed Zhou G, Sirichaisinthop J, Sattabongkot J, Jones J, Bjornstad ON, Yan G, et al. Spatio-temporal distribution of Plasmodium falciparum and P. vivax malaria in Thailand. Am J Trop Med Hyg. 2005;72:256–62.PubMed
11.
go back to reference Carrara VI, Sirilak S, Thonglairuam J, Rojanawatsirivet C, Proux S, Gilbos V, et al. Deployment of early diagnosis and mefloquine-artesunate treatment of falciparum malaria in Thailand: the Tak Malaria Initiative. PLoS Med. 2006;3:e183.CrossRefPubMedCentralPubMed Carrara VI, Sirilak S, Thonglairuam J, Rojanawatsirivet C, Proux S, Gilbos V, et al. Deployment of early diagnosis and mefloquine-artesunate treatment of falciparum malaria in Thailand: the Tak Malaria Initiative. PLoS Med. 2006;3:e183.CrossRefPubMedCentralPubMed
12.
go back to reference Wongsrichanalai C, Barcus MJ, Muth S, Sutamihardja A, Wernsdorfer WH. A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT). Am J Trop Med Hyg. 2007;77:119–27.PubMed Wongsrichanalai C, Barcus MJ, Muth S, Sutamihardja A, Wernsdorfer WH. A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT). Am J Trop Med Hyg. 2007;77:119–27.PubMed
13.
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;11:623–39.CrossRefPubMed Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11:623–39.CrossRefPubMed
14.
go back to reference Alves FP, Durlacher RR, Menezes MJ, Krieger H, Silva LH, Camargo EP. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am J Trop Med Hyg. 2002;66:641–8.PubMed Alves FP, Durlacher RR, Menezes MJ, Krieger H, Silva LH, Camargo EP. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am J Trop Med Hyg. 2002;66:641–8.PubMed
15.
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;200:1509–17.CrossRefPubMed 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;200:1509–17.CrossRefPubMed
16.
go back to reference Steenkeste N, Rogers WO, Okell L, Jeanne I, Incardona S, Duval L, et al. Sub-microscopic malaria cases and mixed malaria infection in a remote area of high malaria endemicity in Rattanakiri province, Cambodia: implication for malaria elimination. Malar J. 2010;9:108.CrossRefPubMedCentralPubMed Steenkeste N, Rogers WO, Okell L, Jeanne I, Incardona S, Duval L, et al. Sub-microscopic malaria cases and mixed malaria infection in a remote area of high malaria endemicity in Rattanakiri province, Cambodia: implication for malaria elimination. Malar J. 2010;9:108.CrossRefPubMedCentralPubMed
18.
go back to reference Lee PW, Liu CT, do Rosario VE, de Sousa B, Rampao HS, Shaio MF. Potential threat of malaria epidemics in a low transmission area, as exemplified by Sao Tome and Principe. Malar J. 2010;9:264.CrossRefPubMedCentralPubMed Lee PW, Liu CT, do Rosario VE, de Sousa B, Rampao HS, Shaio MF. Potential threat of malaria epidemics in a low transmission area, as exemplified by Sao Tome and Principe. Malar J. 2010;9:264.CrossRefPubMedCentralPubMed
19.
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.CrossRefPubMedCentralPubMed 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.CrossRefPubMedCentralPubMed
20.
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.CrossRefPubMedCentralPubMed 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.CrossRefPubMedCentralPubMed
21.
go back to reference 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;41:201–8.CrossRefPubMed 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;41:201–8.CrossRefPubMed
22.
go back to reference Kritsiriwuthinan K, Ngrenngarmlert W. Molecular screening of Plasmodium infections among migrant workers in Thailand. J Vector Borne Dis. 2011;48:214–8.PubMed Kritsiriwuthinan K, Ngrenngarmlert W. Molecular screening of Plasmodium infections among migrant workers in Thailand. J Vector Borne Dis. 2011;48:214–8.PubMed
23.
go back to reference Coleman RE, Maneechai N, Rachaphaew N, Kumpitak C, Miller RS, Soyseng V, et al. Comparison of field and expert laboratory microscopy for active surveillance for asymptomatic Plasmodium falciparum and Plasmodium vivax in western Thailand. Am J Trop Med Hyg. 2002;67:141–4.PubMed Coleman RE, Maneechai N, Rachaphaew N, Kumpitak C, Miller RS, Soyseng V, et al. Comparison of field and expert laboratory microscopy for active surveillance for asymptomatic Plasmodium falciparum and Plasmodium vivax in western Thailand. Am J Trop Med Hyg. 2002;67:141–4.PubMed
24.
go back to reference Rougemont M, Van Saanen M, Sahli R, Hinrikson HP, Bille J, Jaton K. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol. 2004;42:5636–43.CrossRefPubMedCentralPubMed Rougemont M, Van Saanen M, Sahli R, Hinrikson HP, Bille J, Jaton K. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol. 2004;42:5636–43.CrossRefPubMedCentralPubMed
25.
go back to reference Davies DH, Liang X, Hernandez JE, Randall A, Hirst S, Mu Y, et al. Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc Natl Acad Sci U S A. 2005;102:547–52.CrossRefPubMedCentralPubMed Davies DH, Liang X, Hernandez JE, Randall A, Hirst S, Mu Y, et al. Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc Natl Acad Sci U S A. 2005;102:547–52.CrossRefPubMedCentralPubMed
26.
go back to reference Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 2009;37:D539–43.CrossRefPubMedCentralPubMed Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 2009;37:D539–43.CrossRefPubMedCentralPubMed
28.
go back to reference Doolan DL, Mu Y, Unal B, Sundaresh S, Hirst S, Valdez C, et al. Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics. 2008;8:4680–94.CrossRefPubMedCentralPubMed Doolan DL, Mu Y, Unal B, Sundaresh S, Hirst S, Valdez C, et al. Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics. 2008;8:4680–94.CrossRefPubMedCentralPubMed
29.
go back to reference Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, et al. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci U S A. 2010;107:6958–63.CrossRefPubMedCentralPubMed Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, et al. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci U S A. 2010;107:6958–63.CrossRefPubMedCentralPubMed
31.
go back to reference Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, et al. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science. 2003;301:1503–8.CrossRefPubMed Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, et al. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science. 2003;301:1503–8.CrossRefPubMed
32.
go back to reference Baum E, Badu K, Molina DM, Liang X, Felgner PL, Yan G. Protein microarray analysis of antibody responses to Plasmodium falciparum in Western Kenyan highland sites with differing transmission levels. PLoS One. 2013;8:e82246.CrossRefPubMedCentralPubMed Baum E, Badu K, Molina DM, Liang X, Felgner PL, Yan G. Protein microarray analysis of antibody responses to Plasmodium falciparum in Western Kenyan highland sites with differing transmission levels. PLoS One. 2013;8:e82246.CrossRefPubMedCentralPubMed
33.
go back to reference Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001;98:5116–21.CrossRefPubMedCentralPubMed Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001;98:5116–21.CrossRefPubMedCentralPubMed
34.
go back to reference Osier FH, Fegan G, Polley SD, Murungi L, Verra F, Tetteh KK, et al. Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect Immun. 2008;76:2240–8.CrossRefPubMedCentralPubMed Osier FH, Fegan G, Polley SD, Murungi L, Verra F, Tetteh KK, et al. Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect Immun. 2008;76:2240–8.CrossRefPubMedCentralPubMed
35.
go back to reference Reddy SB, Anders RF, Beeson JG, Farnert A, Kironde F, Berenzon SK, et al. High affinity antibodies to Plasmodium falciparum merozoite antigens are associated with protection from malaria. PLoS One. 2012;7:e32242.CrossRefPubMedCentralPubMed Reddy SB, Anders RF, Beeson JG, Farnert A, Kironde F, Berenzon SK, et al. High affinity antibodies to Plasmodium falciparum merozoite antigens are associated with protection from malaria. PLoS One. 2012;7:e32242.CrossRefPubMedCentralPubMed
36.
go back to reference LaCount DJ, Vignali M, Chettier R, Phansalkar A, Bell R, Hesselberth JR, et al. A protein interaction network of the malaria parasite Plasmodium falciparum. Nature. 2005;438:103–7.CrossRefPubMed LaCount DJ, Vignali M, Chettier R, Phansalkar A, Bell R, Hesselberth JR, et al. A protein interaction network of the malaria parasite Plasmodium falciparum. Nature. 2005;438:103–7.CrossRefPubMed
37.
go back to reference Martin RE, Henry RI, Abbey JL, Clements JD, Kirk K. The ‘permeome’ of the malaria parasite: an overview of the membrane transport proteins of Plasmodium falciparum. Genome Biol. 2005;6:R26.CrossRefPubMedCentralPubMed Martin RE, Henry RI, Abbey JL, Clements JD, Kirk K. The ‘permeome’ of the malaria parasite: an overview of the membrane transport proteins of Plasmodium falciparum. Genome Biol. 2005;6:R26.CrossRefPubMedCentralPubMed
39.
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
40.
go back to reference Stewart L, Gosling R, Griffin J, Gesase S, Campo J, Hashim R, et al. Rapid assessment of malaria transmission using age-specific sero-conversion rates. PLoS One. 2009;4:e6083.CrossRefPubMedCentralPubMed Stewart L, Gosling R, Griffin J, Gesase S, Campo J, Hashim R, et al. Rapid assessment of malaria transmission using age-specific sero-conversion rates. PLoS One. 2009;4:e6083.CrossRefPubMedCentralPubMed
41.
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;201:1764–74.CrossRefPubMed 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;201:1764–74.CrossRefPubMed
42.
go back to reference Bousema T, Youssef RM, Cook J, Cox J, Alegana VA, Amran J, et al. Serologic markers for detecting malaria in areas of low endemicity, Somalia, 2008. Emerg Infect Dis. 2010;16:392–9.CrossRefPubMedCentralPubMed Bousema T, Youssef RM, Cook J, Cox J, Alegana VA, Amran J, et al. Serologic markers for detecting malaria in areas of low endemicity, Somalia, 2008. Emerg Infect Dis. 2010;16:392–9.CrossRefPubMedCentralPubMed
43.
go back to reference Tan X, Traore B, Kayentao K, Ongoiba A, Doumbo S, Waisberg M, et al. Hemoglobin S and C heterozygosity enhances neither the magnitude nor breadth of antibody responses to a diverse array of Plasmodium falciparum antigens. J Infect Dis. 2011;204:1750–61.CrossRefPubMedCentralPubMed Tan X, Traore B, Kayentao K, Ongoiba A, Doumbo S, Waisberg M, et al. Hemoglobin S and C heterozygosity enhances neither the magnitude nor breadth of antibody responses to a diverse array of Plasmodium falciparum antigens. J Infect Dis. 2011;204:1750–61.CrossRefPubMedCentralPubMed
44.
go back to reference Nnedu ON, O’Leary MP, Mutua D, Mutai B, Kalantari-Dehaghi M, Jasinskas A, et al. Humoral immune responses to Plasmodium falciparum among HIV-1-infected Kenyan adults. Proteomics Clin Appl. 2011;5:613–23.CrossRefPubMedCentralPubMed Nnedu ON, O’Leary MP, Mutua D, Mutai B, Kalantari-Dehaghi M, Jasinskas A, et al. Humoral immune responses to Plasmodium falciparum among HIV-1-infected Kenyan adults. Proteomics Clin Appl. 2011;5:613–23.CrossRefPubMedCentralPubMed
45.
go back to reference Barry AE, Trieu A, Fowkes FJ, Pablo J, Kalantari-Dehaghi M, Jasinskas A, et al. The stability and complexity of antibody responses to the major surface antigen of Plasmodium falciparum are associated with age in a malaria endemic area. Mol Cell Proteomics. 2011;10:M111 008326.CrossRefPubMedCentralPubMed Barry AE, Trieu A, Fowkes FJ, Pablo J, Kalantari-Dehaghi M, Jasinskas A, et al. The stability and complexity of antibody responses to the major surface antigen of Plasmodium falciparum are associated with age in a malaria endemic area. Mol Cell Proteomics. 2011;10:M111 008326.CrossRefPubMedCentralPubMed
46.
go back to reference Molina DM, Finney OC, Arevalo-Herrera M, Herrera S, Felgner PL, Gardner MJ, et al. Plasmodium vivax pre-erythrocytic-stage antigen discovery: exploiting naturally acquired humoral responses. Am J Trop Med Hyg. 2012;87:460–9.CrossRefPubMedCentralPubMed Molina DM, Finney OC, Arevalo-Herrera M, Herrera S, Felgner PL, Gardner MJ, et al. Plasmodium vivax pre-erythrocytic-stage antigen discovery: exploiting naturally acquired humoral responses. Am J Trop Med Hyg. 2012;87:460–9.CrossRefPubMedCentralPubMed
47.
go back to reference Felgner PL, Roestenberg M, Liang L, Hung C, Jain A, Pablo J, et al. Pre-erythrocytic antibody profiles induced by controlled human malaria infections in healthy volunteers under chloroquine prophylaxis. Sci Rep. 2013;3:3549.CrossRefPubMed Felgner PL, Roestenberg M, Liang L, Hung C, Jain A, Pablo J, et al. Pre-erythrocytic antibody profiles induced by controlled human malaria infections in healthy volunteers under chloroquine prophylaxis. Sci Rep. 2013;3:3549.CrossRefPubMed
48.
go back to reference Brown AE, Kain KC, Pipithkul J, Webster HK. Demonstration by the polymerase chain reaction of mixed Plasmodium falciparum and P. vivax infections undetected by conventional microscopy. Trans R Soc Trop Med Hyg. 1992;86:609–12.CrossRefPubMed Brown AE, Kain KC, Pipithkul J, Webster HK. Demonstration by the polymerase chain reaction of mixed Plasmodium falciparum and P. vivax infections undetected by conventional microscopy. Trans R Soc Trop Med Hyg. 1992;86:609–12.CrossRefPubMed
49.
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;62:225–31.PubMed 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;62:225–31.PubMed
50.
go back to reference Mayxay M, Pukritrayakamee S, Chotivanich K, Imwong M, Looareesuwan S, White NJ. Identification of cryptic coinfection with Plasmodium falciparum in patients presenting with vivax malaria. Am J Trop Med Hyg. 2001;65:588–92.PubMed Mayxay M, Pukritrayakamee S, Chotivanich K, Imwong M, Looareesuwan S, White NJ. Identification of cryptic coinfection with Plasmodium falciparum in patients presenting with vivax malaria. Am J Trop Med Hyg. 2001;65:588–92.PubMed
51.
go back to reference Siripoon N, Snounou G, Yamogkul P, Na-Bangchang K, Thaithong S. Cryptic Plasmodium falciparum parasites in clinical P. vivax blood samples from Thailand. Trans R Soc Trop Med Hyg. 2002;96:70–1.CrossRefPubMed Siripoon N, Snounou G, Yamogkul P, Na-Bangchang K, Thaithong S. Cryptic Plasmodium falciparum parasites in clinical P. vivax blood samples from Thailand. Trans R Soc Trop Med Hyg. 2002;96:70–1.CrossRefPubMed
52.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
53.
go back to reference Price RN, Simpson JA, Nosten F, Luxemburger C, Hkirjaroen L, ter Kuile F, et al. Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg. 2001;65:614–22.PubMedCentralPubMed Price RN, Simpson JA, Nosten F, Luxemburger C, Hkirjaroen L, ter Kuile F, et al. Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg. 2001;65:614–22.PubMedCentralPubMed
54.
go back to reference Lin JT, Saunders DL, Meshnick SR. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 2014;30:183–90.CrossRefPubMed Lin JT, Saunders DL, Meshnick SR. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 2014;30:183–90.CrossRefPubMed
55.
go back to reference Fowkes FJ, McGready R, Cross NJ, Hommel M, Simpson JA, Elliott SR, et al. New insights into acquisition, boosting, and longevity of immunity to malaria in pregnant women. J Infect Dis. 2012;206:1612–21.CrossRefPubMedCentralPubMed Fowkes FJ, McGready R, Cross NJ, Hommel M, Simpson JA, Elliott SR, et al. New insights into acquisition, boosting, and longevity of immunity to malaria in pregnant women. J Infect Dis. 2012;206:1612–21.CrossRefPubMedCentralPubMed
56.
go back to reference Akpogheneta OJ, Duah NO, Tetteh KK, Dunyo S, Lanar DE, Pinder M, et al. Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infect Immun. 2008;76:1748–55.CrossRefPubMedCentralPubMed Akpogheneta OJ, Duah NO, Tetteh KK, Dunyo S, Lanar DE, Pinder M, et al. Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infect Immun. 2008;76:1748–55.CrossRefPubMedCentralPubMed
57.
58.
go back to reference Kinyanjui SM, Bejon P, Osier FH, Bull PC, Marsh K. What you see is not what you get: implications of the brevity of antibody responses to malaria antigens and transmission heterogeneity in longitudinal studies of malaria immunity. Malar J. 2009;8:242.CrossRefPubMedCentralPubMed Kinyanjui SM, Bejon P, Osier FH, Bull PC, Marsh K. What you see is not what you get: implications of the brevity of antibody responses to malaria antigens and transmission heterogeneity in longitudinal studies of malaria immunity. Malar J. 2009;8:242.CrossRefPubMedCentralPubMed
59.
go back to reference Achtman AH, Bull PC, Stephens R, Langhorne J. Longevity of the immune response and memory to blood-stage malaria infection. Curr Top Microbiol Immunol. 2005;297:71–102.PubMed Achtman AH, Bull PC, Stephens R, Langhorne J. Longevity of the immune response and memory to blood-stage malaria infection. Curr Top Microbiol Immunol. 2005;297:71–102.PubMed
60.
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.CrossRefPubMedCentralPubMed 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.CrossRefPubMedCentralPubMed
61.
go back to reference Clark EH, Silva CJ, Weiss GE, Li S, Padilla C, Crompton PD, et al. Plasmodium falciparum malaria in the Peruvian Amazon, a region of low transmission, is associated with immunologic memory. Infect Immun. 2012;80:1583–92.CrossRefPubMedCentralPubMed Clark EH, Silva CJ, Weiss GE, Li S, Padilla C, Crompton PD, et al. Plasmodium falciparum malaria in the Peruvian Amazon, a region of low transmission, is associated with immunologic memory. Infect Immun. 2012;80:1583–92.CrossRefPubMedCentralPubMed
62.
go back to reference Ndungu FM, Lundblom K, Rono J, Illingworth J, Eriksson S, Farnert A. Long-lived Plasmodium falciparum specific memory B cells in naturally exposed Swedish travelers. Eur J Immunol. 2013;43:2919–29.CrossRefPubMedCentralPubMed Ndungu FM, Lundblom K, Rono J, Illingworth J, Eriksson S, Farnert A. Long-lived Plasmodium falciparum specific memory B cells in naturally exposed Swedish travelers. Eur J Immunol. 2013;43:2919–29.CrossRefPubMedCentralPubMed
63.
go back to reference Rogawski ET, Congpuong K, Sudathip P, Satimai W, Sug-aram R, Aruncharus S, et al. Active case detection with pooled real-time PCR to eliminate malaria in Trat province, Thailand. Am J Trop Med Hyg. 2012;86:789–91.CrossRefPubMedCentralPubMed Rogawski ET, Congpuong K, Sudathip P, Satimai W, Sug-aram R, Aruncharus S, et al. Active case detection with pooled real-time PCR to eliminate malaria in Trat province, Thailand. Am J Trop Med Hyg. 2012;86:789–91.CrossRefPubMedCentralPubMed
64.
go back to reference Congpuong K, Saejeng A, Sug-Aram R, Aruncharus S, Darakapong A, Meshnick SR, et al. Mass blood survey for malaria: pooling and real-time PCR combined with expert microscopy in north-west Thailand. Malar J. 2012;11:288.CrossRefPubMedCentralPubMed Congpuong K, Saejeng A, Sug-Aram R, Aruncharus S, Darakapong A, Meshnick SR, et al. Mass blood survey for malaria: pooling and real-time PCR combined with expert microscopy in north-west Thailand. Malar J. 2012;11:288.CrossRefPubMedCentralPubMed
65.
go back to reference Steenkeste N, Incardona S, Chy S, Duval L, Ekala MT, Lim P, et al. Towards high-throughput molecular detection of Plasmodium: new approaches and molecular markers. Malar J. 2009;8:86.CrossRefPubMedCentralPubMed Steenkeste N, Incardona S, Chy S, Duval L, Ekala MT, Lim P, et al. Towards high-throughput molecular detection of Plasmodium: new approaches and molecular markers. Malar J. 2009;8:86.CrossRefPubMedCentralPubMed
66.
go back to reference Kamau E, Alemayehu S, Feghali KC, Saunders D, Ockenhouse CF. Multiplex qPCR for detection and absolute quantification of malaria. PLoS One. 2013;8:e71539.CrossRefPubMedCentralPubMed Kamau E, Alemayehu S, Feghali KC, Saunders D, Ockenhouse CF. Multiplex qPCR for detection and absolute quantification of malaria. PLoS One. 2013;8:e71539.CrossRefPubMedCentralPubMed
67.
go back to reference Patel JC, Lucchi NW, Srivastava P, Lin JT, Sug-Aram R, Aruncharus S, et al. Field evaluation of a real-time fluorescence loop-mediated isothermal amplification assay, RealAmp, for the diagnosis of malaria in Thailand and India. J Infect Dis. 2014;210:1180–7.CrossRefPubMed Patel JC, Lucchi NW, Srivastava P, Lin JT, Sug-Aram R, Aruncharus S, et al. Field evaluation of a real-time fluorescence loop-mediated isothermal amplification assay, RealAmp, for the diagnosis of malaria in Thailand and India. J Infect Dis. 2014;210:1180–7.CrossRefPubMed
68.
go back to reference Drakeley C, Cook J. Potential contribution of sero-epidemiological analysis for monitoring malaria control and elimination: historical and current perspectives. Adv Parasitol. 2009;69:299–352.CrossRefPubMed Drakeley C, Cook J. Potential contribution of sero-epidemiological analysis for monitoring malaria control and elimination: historical and current perspectives. Adv Parasitol. 2009;69:299–352.CrossRefPubMed
69.
go back to reference Bruce-Chwatt LJ, Draper CC, Konfortion P. Seroepidemiological evidence of eradication of malaria from Mauritius. Lancet. 1973;2:547–51.CrossRefPubMed Bruce-Chwatt LJ, Draper CC, Konfortion P. Seroepidemiological evidence of eradication of malaria from Mauritius. Lancet. 1973;2:547–51.CrossRefPubMed
70.
go back to reference Bruce-Chwatt LJ, Draper CC, Avramidis D, Kazandzoglou O. Sero-epidemiological surveillance of disappearing malaria in Greece. J Trop Med Hyg. 1975;78:194–200.PubMed Bruce-Chwatt LJ, Draper CC, Avramidis D, Kazandzoglou O. Sero-epidemiological surveillance of disappearing malaria in Greece. J Trop Med Hyg. 1975;78:194–200.PubMed
71.
go back to reference Cook J, Reid H, Iavro J, Kuwahata M, Taleo G, Clements A, et al. Using serological measures to monitor changes in malaria transmission in Vanuatu. Malar J. 2010;9:169.CrossRefPubMedCentralPubMed Cook J, Reid H, Iavro J, Kuwahata M, Taleo G, Clements A, et al. Using serological measures to monitor changes in malaria transmission in Vanuatu. Malar J. 2010;9:169.CrossRefPubMedCentralPubMed
Metadata
Title
Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand - molecular and serological evidence
Authors
Elisabeth Baum
Jetsumon Sattabongkot
Jeeraphat Sirichaisinthop
Kirakorn Kiattibutr
D Huw Davies
Aarti Jain
Eugenia Lo
Ming-Chieh Lee
Arlo Z Randall
Douglas M Molina
Xiaowu Liang
Liwang Cui
Philip L Felgner
Guiyun Yan
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-0611-9

Other articles of this Issue 1/2015

Malaria Journal 1/2015 Go to the issue