Author:
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- Molecular diagnosis of Plasmodium spp. infections.
- Amplification of the pfhrp2 gene.
- Comparison with RDT analysis.
- Sequence analysis of pfhrp2 gene from cultured isolates.
- Sequence analysis of pfhrp2 gene from filter paper blood spots.
- Distribution of amino acid repeat types in pfhrp2 exon-2.
- Major epitopes in pfhrp2 exon-2 targeted by MAbs in RDTs.
- DISCUSSION
- LIMITATIONS
- Supplementary Material
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Parra ME, Evans CB, Taylor DW, 1991. Identification of Plasmodium falciparum histidine-rich protein 2 in the plasma of humans with malaria. J Clin Microbiol 29: 1629–1634.
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2.
Beadle C, Long GW, Weiss WR, McElroy PD, Maret SM, Oloo AJ, Hoffman SL, 1994. Diagnosis of malaria by detection of Plasmodium falciparum HRP-2 antigen with a rapid dipstick antigen-capture assay. Lancet 343: 564–568.
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3.
Moody A, 2002. Rapid diagnostic tests for malaria parasites. Clin Microbiol Rev 15: 66–78.
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4.
Rabarijaona LP, Ariey F, Matra R, Cot S, Raharimalala AL, Ranaivo LH, Le Bras J, Robert V, Randrianarivelojosia M, 2006. Low autochtonous urban malaria in Antananarivo (Madagascar). Malar J 5: 27.
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Randrianasolo L, Tafangy PB, Raharimalala LA, Ratsimbasoa AC, Randriamanantena A, Randrianarivelojosia M, 2007. Rapid diagnostic test for malaria: preliminary study in Madagascar in 2003. Sante 17: 69–73.
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Howes RE, Mioramalala SA, Ramiranirina B, Franchard T, Rakotorahalahy AJ, Bisanzio D, Gething PW, Zimmerman PA, Ratsimbasoa A, 2016. Contemporary epidemiological overview of malaria in Madagascar: operational utility of reported routine case data for malaria control planning. Malar J 15: 502.
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7.
Rakotonirina H, Barnadas C, Raherijafy R, Andrianantenaina H, Ratsimbasoa A, Randrianasolo L, Jahevitra M, Andriantsoanirina V, Menard D, 2008. Accuracy and reliability of malaria diagnostic techniques for guiding febrile outpatient treatment in malaria-endemic countries. Am J Trop Med Hyg 78: 217–221.
-
8.
Ratsimbasoa A, Fanazava L, Radrianjafy R, Ramilijaona J, Rafanomezantsoa H, Menard D, 2008. Evaluation of two new immunochromatographic assays for diagnosis of malaria. Am J Trop Med Hyg 79: 670–672.
-
9.
Ravaoarisoa E, Andriamiandranoro T, Raherinjafy R, Jahevitra M, Razanatsiorimalala S, Andrianaranjaka V, Randrianarivelojosia M, 2017. Evaluation of the OnSite malaria rapid test performance in Miandrivazo, Madagascar. Bull Soc Pathol Exot 110: 254–259.
-
10.
Baker J, Gatton ML, Peters J, Ho MF, McCarthy JS, Cheng Q, 2011. Transcription and expression of Plasmodium falciparum histidine-rich proteins in different stages and strains: implications for rapid diagnostic tests. PLoS One 6: e22593.
-
11.
Ho MF et al. 2014. Circulating antibodies against Plasmodium falciparum histidine-rich proteins 2 interfere with antigen detection by rapid diagnostic tests. Malar J 13: 480.
-
12.
Iqbal J, Siddique A, Jameel M, Hira PR, 2004. Persistent histidine-rich protein 2, parasite lactate dehydrogenase, and panmalarial antigen reactivity after clearance of Plasmodium falciparum monoinfection. J Clin Microbiol 42: 4237–4241.
-
13.
Cheng Q, Gatton ML, Barnwell J, Chiodini P, McCarthy J, Bell D, Cunningham J, 2014. Plasmodium falciparum parasites lacking histidine-rich protein 2 and 3: a review and recommendations for accurate reporting. Malar J 13: 283.
-
14.
Lee N, Baker J, Andrews KT, Gatton ML, Bell D, Cheng Q, McCarthy J, 2006. Effect of sequence variation in Plasmodium falciparum histidine-rich protein 2 on binding of specific monoclonal antibodies: implications for rapid diagnostic tests for malaria. J Clin Microbiol 44: 2773–2778.
-
15.
Lee N, Gatton ML, Pelecanos A, Bubb M, Gonzalez I, Bell D, Cheng Q, McCarthy JS, 2012. Identification of optimal epitopes for Plasmodium falciparum rapid diagnostic tests that target histidine-rich proteins 2 and 3. J Clin Microbiol 50: 1397–1405.
-
16.
Gamboa D et al. 2010. A large proportion of P. falciparum isolates in the Amazon region of Peru lack pfhrp2 and pfhrp3: implications for malaria rapid diagnostic tests. PLoS One 5: e8091.
-
17.
Akinyi Okoth S et al. 2015. Variation in Plasmodium falciparum histidine-rich protein 2 (pfhrp2) and Plasmodium falciparum histidine-rich protein 3 (pfhrp3) gene deletions in Guyana and Suriname. PLoS One 10: e0126805.
-
18.
Dorado EJ, Okoth SA, Montenegro LM, Diaz G, Barnwell JW, Udhayakumar V, Murillo Solano C, 2016. Genetic characterisation of Plasmodium falciparum isolates with deletion of the pfhrp2 and/or pfhrp3 genes in Colombia: the Amazon region, a challenge for malaria diagnosis and control. PLoS One 11: e0163137.
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19.
Murillo Solano C et al. 2015. Deletion of Plasmodium falciparum histidine-rich protein 2 (pfhrp2) and histidine-rich protein 3 (pfhrp3) genes in Colombian parasites. PLoS One 10: e0131576.
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20.
Rachid Viana GM et al. 2017. Histidine-rich protein 2 (pfhrp2) and pfhrp3 gene deletions in Plasmodium falciparum isolates from select sites in Brazil and Bolivia. PLoS One 12: e0171150.
-
21.
Abdallah JF et al. 2015. Prevalence of pfhrp2 and pfhrp3 gene deletions in Puerto Lempira, Honduras. Malar J 14: 19.
-
22.
Bharti PK, Chandel HS, Ahmad A, Krishna S, Udhayakumar V, Singh N, 2016. Prevalence of pfhrp2 and/or pfhrp3 gene deletion in Plasmodium falciparum population in eight highly endemic states in India. PLoS One 11: e0157949.
-
23.
Biswas S, Tomar D, Rao DN, 2005. Investigation of the kinetics of histidine-rich protein 2 and of the antibody responses to this antigen, in a group of malaria patients from India. Ann Trop Med Parasitol 99: 553–562.
-
24.
Nima MK, Hougard T, Hossain ME, Kibria MG, Mohon AN, Johora FT, Rahman R, Haque R, Alam MS, 2017. Case report: a case of Plasmodium falciparum hrp2 and hrp3 gene mutation in Bangladesh. Am J Trop Med Hyg 97: 1155–1158.
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25.
Atroosh WM et al. 2015. Genetic variation of pfhrp2 in Plasmodium falciparum isolates from Yemen and the performance of HRP2-based malaria rapid diagnostic test. Parasit Vectors 8: 388.
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26.
Amoah LE, Abankwa J, Oppong A, 2016. Plasmodium falciparum histidine rich protein-2 diversity and the implications for PfHRP 2: based malaria rapid diagnostic tests in Ghana. Malar J 15: 101.
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27.
Koita OA et al. 2012. False-negative rapid diagnostic tests for malaria and deletion of the histidine-rich repeat region of the hrp2 gene. Am J Trop Med Hyg 86: 194–198.
-
28.
Kozycki CT, Umulisa N, Rulisa S, Mwikarago EI, Musabyimana JP, Habimana JP, Karema C, Krogstad DJ, 2017. False-negative malaria rapid diagnostic tests in Rwanda: impact of Plasmodium falciparum isolates lacking hrp2 and declining malaria transmission. Malar J 16: 123.
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Parr JB et al. 2017. Pfhrp2-deleted Plasmodium falciparum parasites in the Democratic Republic of the Congo: a national cross-sectional survey. J Infect Dis 216: 36–44.
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Watson OJ, Slater HC, Verity R, Parr JB, Mwandagalirwa MK, Tshefu A, Meshnick SR, Ghani AC, 2017. Modelling the drivers of the spread of Plasmodium falciparum hrp2 gene deletions in sub-Saharan Africa. Elife 6: e25008.
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Baker J, McCarthy J, Gatton M, Kyle DE, Belizario V, Luchavez J, Bell D, Cheng Q, 2005. Genetic diversity of Plasmodium falciparum histidine-rich protein 2 (PfHRP2) and its effect on the performance of PfHRP2-based rapid diagnostic tests. J Infect Dis 192: 870–877.
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Insights into the Performance of SD Bioline Malaria Ag P.f/Pan Rapid Diagnostic Test and Plasmodium falciparum Histidine-Rich Protein 2 Gene Variation in Madagascar
Nigani Willie
Nigani Willie
Center for Global Health and Diseases, School of Medicine, Case Western Reserve University, Cleveland, Ohio;
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Rajeev K. Mehlotra
Rajeev K. Mehlotra
Center for Global Health and Diseases, School of Medicine, Case Western Reserve University, Cleveland, Ohio;
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Rosalind E. Howes
Rosalind E. Howes
Center for Global Health and Diseases, School of Medicine, Case Western Reserve University, Cleveland, Ohio;
Nuffield Department of Medicine, Oxford Big Data Institute, University of Oxford, Oxford, United Kingdom;
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Nuffield Department of Medicine, Oxford Big Data Institute, University of Oxford, Oxford, United Kingdom;
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Tovonahary A. Rakotomanga
Tovonahary A. Rakotomanga
National Malaria Control Programme, Ministry of Health, Antananarivo, Madagascar;
Faculty of Sciences, University of Antananarivo, Antananarivo, Madagascar
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Faculty of Sciences, University of Antananarivo, Antananarivo, Madagascar
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Stephanie Ramboarina
Stephanie Ramboarina
Center for Global Health and Diseases, School of Medicine, Case Western Reserve University, Cleveland, Ohio;
Faculty of Sciences, University of Antananarivo, Antananarivo, Madagascar
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Faculty of Sciences, University of Antananarivo, Antananarivo, Madagascar
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Arsène C. Ratsimbasoa
Arsène C. Ratsimbasoa
National Malaria Control Programme, Ministry of Health, Antananarivo, Madagascar;
Faculty of Sciences, University of Antananarivo, Antananarivo, Madagascar
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Faculty of Sciences, University of Antananarivo, Antananarivo, Madagascar
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Peter A. Zimmerman
Peter A. Zimmerman
Center for Global Health and Diseases, School of Medicine, Case Western Reserve University, Cleveland, Ohio;
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Plasmodium falciparum histidine-rich protein 2 (PfHRP2) forms the basis of many current malaria rapid diagnostic tests (RDTs). However, the parasites lacking part or all of the pfhrp2 gene do not express the PfHRP2 protein and are, therefore, not identifiable by PfHRP2-detecting RDTs. We evaluated the performance of the SD Bioline Malaria Ag P.f/Pan RDT together with pfhrp2 variation in Madagascar. Genomic DNA isolated from 260 patient blood samples were polymerase chain reaction (PCR)–amplified for the parasite 18S rRNA and pfhrp2 genes. Post-PCR ligation detection reaction-fluorescent microsphere assay (LDR-FMA) was performed for the identification of parasite species. Plasmodium falciparum histidine-rich protein 2 amplicons were sequenced. Polymerase chain reaction diagnosis of patient samples showed that 29% (75/260) were infected and P. falciparum was present in 95% (71/75) of these PCR-positive samples. Comparing RDT and P. falciparum detection by LDR-FMA, eight samples were RDT negative but P. falciparum positive (false negatives), all of which were pfhrp2 positive. The sensitivity and specificity of the RDT were 87% and 90%, respectively. Seventy-three samples were amplified for pfhrp2, from which nine randomly selected amplicons were sequenced, yielding 13 sequences. Amplification of pfhrp2, combined with RDT analysis and P. falciparum detection by LDR-FMA, showed that there was no indication of pfhrp2 deletion. Sequence analysis of pfhrp2 showed that the correlation between pfhrp2 sequence structure and RDT detection rates was unclear. Although the observed absence of pfhrp2 deletion from the samples screened here is encouraging, continued monitoring of the efficacy of the SD Bioline Malaria Ag P.f/Pan RDT for malaria diagnosis in Madagascar is warranted.
- Supplemental Materials (PDF 21 KB)
Author Notes
Financial support: This study was supported by a grant from the National Institutes of Health (R01 AI097366) to P. A. Z.
These authors contributed equally to this work.
Authors’ addresses: Nigani Willie, Rajeev K. Mehlotra, and Peter A. Zimmerman, Center for Global Health and Diseases, School of Medicine, Case Western Reserve University, Cleveland, OH, E-mails: nxw144@case.edu, rkm@case.edu, and paz@case.edu. Rosalind E. Howes, Center for Global Health and Diseases, School of Medicine, Case Western Reserve University, Cleveland, OH, and Nuffield Department of Medicine, Oxford Big Data Institute, University of Oxford, Oxford, United Kingdom, E-mail: rosalind.howes@bdi.ox.ac.uk. Tovonahary A. Rakotomanga, National Malaria Control Programme, Ministry of Health, Antananarivo, Madagascar, and Faculty of Sciences, University of Antananarivo, Antananarivo, Madagascar, E-mail: tovo_angelo@yahoo.fr. Stephanie Ramboarina, Center for Global Health and Diseases, School of Medicine, Case Western Reserve University, Cleveland, OH, and Faculty of Sciences, University of Antananarivo, Antananarivo, Madagascar, E-mail: sramboa@gmail.com. Arsène C. Ratsimbasoa, National Malaria Control Programme, Ministry of Health, Antananarivo, Madagascar, and Faculty of Sciences, University of Antananarivo, Antananarivo, Madagascar, E-mail: aratsimbasoa@gmail.com.
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- Molecular diagnosis of Plasmodium spp. infections.
- Amplification of the pfhrp2 gene.
- Comparison with RDT analysis.
- Sequence analysis of pfhrp2 gene from cultured isolates.
- Sequence analysis of pfhrp2 gene from filter paper blood spots.
- Distribution of amino acid repeat types in pfhrp2 exon-2.
- Major epitopes in pfhrp2 exon-2 targeted by MAbs in RDTs.
- DISCUSSION
- LIMITATIONS
- Supplementary Material
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Parra ME, Evans CB, Taylor DW, 1991. Identification of Plasmodium falciparum histidine-rich protein 2 in the plasma of humans with malaria. J Clin Microbiol 29: 1629–1634.
-
2.
Beadle C, Long GW, Weiss WR, McElroy PD, Maret SM, Oloo AJ, Hoffman SL, 1994. Diagnosis of malaria by detection of Plasmodium falciparum HRP-2 antigen with a rapid dipstick antigen-capture assay. Lancet 343: 564–568.
-
3.
Moody A, 2002. Rapid diagnostic tests for malaria parasites. Clin Microbiol Rev 15: 66–78.
-
4.
Rabarijaona LP, Ariey F, Matra R, Cot S, Raharimalala AL, Ranaivo LH, Le Bras J, Robert V, Randrianarivelojosia M, 2006. Low autochtonous urban malaria in Antananarivo (Madagascar). Malar J 5: 27.
-
5.
Randrianasolo L, Tafangy PB, Raharimalala LA, Ratsimbasoa AC, Randriamanantena A, Randrianarivelojosia M, 2007. Rapid diagnostic test for malaria: preliminary study in Madagascar in 2003. Sante 17: 69–73.
-
6.
Howes RE, Mioramalala SA, Ramiranirina B, Franchard T, Rakotorahalahy AJ, Bisanzio D, Gething PW, Zimmerman PA, Ratsimbasoa A, 2016. Contemporary epidemiological overview of malaria in Madagascar: operational utility of reported routine case data for malaria control planning. Malar J 15: 502.
-
7.
Rakotonirina H, Barnadas C, Raherijafy R, Andrianantenaina H, Ratsimbasoa A, Randrianasolo L, Jahevitra M, Andriantsoanirina V, Menard D, 2008. Accuracy and reliability of malaria diagnostic techniques for guiding febrile outpatient treatment in malaria-endemic countries. Am J Trop Med Hyg 78: 217–221.
-
8.
Ratsimbasoa A, Fanazava L, Radrianjafy R, Ramilijaona J, Rafanomezantsoa H, Menard D, 2008. Evaluation of two new immunochromatographic assays for diagnosis of malaria. Am J Trop Med Hyg 79: 670–672.
-
9.
Ravaoarisoa E, Andriamiandranoro T, Raherinjafy R, Jahevitra M, Razanatsiorimalala S, Andrianaranjaka V, Randrianarivelojosia M, 2017. Evaluation of the OnSite malaria rapid test performance in Miandrivazo, Madagascar. Bull Soc Pathol Exot 110: 254–259.
-
10.
Baker J, Gatton ML, Peters J, Ho MF, McCarthy JS, Cheng Q, 2011. Transcription and expression of Plasmodium falciparum histidine-rich proteins in different stages and strains: implications for rapid diagnostic tests. PLoS One 6: e22593.
-
11.
Ho MF et al. 2014. Circulating antibodies against Plasmodium falciparum histidine-rich proteins 2 interfere with antigen detection by rapid diagnostic tests. Malar J 13: 480.
-
12.
Iqbal J, Siddique A, Jameel M, Hira PR, 2004. Persistent histidine-rich protein 2, parasite lactate dehydrogenase, and panmalarial antigen reactivity after clearance of Plasmodium falciparum monoinfection. J Clin Microbiol 42: 4237–4241.
-
13.
Cheng Q, Gatton ML, Barnwell J, Chiodini P, McCarthy J, Bell D, Cunningham J, 2014. Plasmodium falciparum parasites lacking histidine-rich protein 2 and 3: a review and recommendations for accurate reporting. Malar J 13: 283.
-
14.
Lee N, Baker J, Andrews KT, Gatton ML, Bell D, Cheng Q, McCarthy J, 2006. Effect of sequence variation in Plasmodium falciparum histidine-rich protein 2 on binding of specific monoclonal antibodies: implications for rapid diagnostic tests for malaria. J Clin Microbiol 44: 2773–2778.
-
15.
Lee N, Gatton ML, Pelecanos A, Bubb M, Gonzalez I, Bell D, Cheng Q, McCarthy JS, 2012. Identification of optimal epitopes for Plasmodium falciparum rapid diagnostic tests that target histidine-rich proteins 2 and 3. J Clin Microbiol 50: 1397–1405.
-
16.
Gamboa D et al. 2010. A large proportion of P. falciparum isolates in the Amazon region of Peru lack pfhrp2 and pfhrp3: implications for malaria rapid diagnostic tests. PLoS One 5: e8091.
-
17.
Akinyi Okoth S et al. 2015. Variation in Plasmodium falciparum histidine-rich protein 2 (pfhrp2) and Plasmodium falciparum histidine-rich protein 3 (pfhrp3) gene deletions in Guyana and Suriname. PLoS One 10: e0126805.
-
18.
Dorado EJ, Okoth SA, Montenegro LM, Diaz G, Barnwell JW, Udhayakumar V, Murillo Solano C, 2016. Genetic characterisation of Plasmodium falciparum isolates with deletion of the pfhrp2 and/or pfhrp3 genes in Colombia: the Amazon region, a challenge for malaria diagnosis and control. PLoS One 11: e0163137.
-
19.
Murillo Solano C et al. 2015. Deletion of Plasmodium falciparum histidine-rich protein 2 (pfhrp2) and histidine-rich protein 3 (pfhrp3) genes in Colombian parasites. PLoS One 10: e0131576.
-
20.
Rachid Viana GM et al. 2017. Histidine-rich protein 2 (pfhrp2) and pfhrp3 gene deletions in Plasmodium falciparum isolates from select sites in Brazil and Bolivia. PLoS One 12: e0171150.
-
21.
Abdallah JF et al. 2015. Prevalence of pfhrp2 and pfhrp3 gene deletions in Puerto Lempira, Honduras. Malar J 14: 19.
-
22.
Bharti PK, Chandel HS, Ahmad A, Krishna S, Udhayakumar V, Singh N, 2016. Prevalence of pfhrp2 and/or pfhrp3 gene deletion in Plasmodium falciparum population in eight highly endemic states in India. PLoS One 11: e0157949.
-
23.
Biswas S, Tomar D, Rao DN, 2005. Investigation of the kinetics of histidine-rich protein 2 and of the antibody responses to this antigen, in a group of malaria patients from India. Ann Trop Med Parasitol 99: 553–562.
-
24.
Nima MK, Hougard T, Hossain ME, Kibria MG, Mohon AN, Johora FT, Rahman R, Haque R, Alam MS, 2017. Case report: a case of Plasmodium falciparum hrp2 and hrp3 gene mutation in Bangladesh. Am J Trop Med Hyg 97: 1155–1158.
-
25.
Atroosh WM et al. 2015. Genetic variation of pfhrp2 in Plasmodium falciparum isolates from Yemen and the performance of HRP2-based malaria rapid diagnostic test. Parasit Vectors 8: 388.
-
26.
Amoah LE, Abankwa J, Oppong A, 2016. Plasmodium falciparum histidine rich protein-2 diversity and the implications for PfHRP 2: based malaria rapid diagnostic tests in Ghana. Malar J 15: 101.
-
27.
Koita OA et al. 2012. False-negative rapid diagnostic tests for malaria and deletion of the histidine-rich repeat region of the hrp2 gene. Am J Trop Med Hyg 86: 194–198.
-
28.
Kozycki CT, Umulisa N, Rulisa S, Mwikarago EI, Musabyimana JP, Habimana JP, Karema C, Krogstad DJ, 2017. False-negative malaria rapid diagnostic tests in Rwanda: impact of Plasmodium falciparum isolates lacking hrp2 and declining malaria transmission. Malar J 16: 123.
-
29.
Parr JB et al. 2017. Pfhrp2-deleted Plasmodium falciparum parasites in the Democratic Republic of the Congo: a national cross-sectional survey. J Infect Dis 216: 36–44.
-
30.
Watson OJ, Slater HC, Verity R, Parr JB, Mwandagalirwa MK, Tshefu A, Meshnick SR, Ghani AC, 2017. Modelling the drivers of the spread of Plasmodium falciparum hrp2 gene deletions in sub-Saharan Africa. Elife 6: e25008.
-
31.
Wurtz N et al. 2013. Pfhrp2 and pfhrp3 polymorphisms in Plasmodium falciparum isolates from Dakar, Senegal: impact on rapid malaria diagnostic tests. Malar J 12: 34.
-
32.
Baker J et al. 2010. Global sequence variation in the histidine-rich proteins 2 and 3 of Plasmodium falciparum: implications for the performance of malaria rapid diagnostic tests. Malar J 9: 129.
-
33.
Baker J, McCarthy J, Gatton M, Kyle DE, Belizario V, Luchavez J, Bell D, Cheng Q, 2005. Genetic diversity of Plasmodium falciparum histidine-rich protein 2 (PfHRP2) and its effect on the performance of PfHRP2-based rapid diagnostic tests. J Infect Dis 192: 870–877.
-
34.
Mariette N, Barnadas C, Bouchier C, Tichit M, Menard D, 2008. Country-wide assessment of the genetic polymorphism in Plasmodium falciparum and Plasmodium vivax antigens detected with rapid diagnostic tests for malaria. Malar J 7: 219.
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