- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Patient population and sample collection.
- Parasite detection by microscopy and mRDT.
- Nucleic acid preparation.
- Pan-Plasmodium detection by reverse transcription qPCR.
- Standard curve for quantification of parasite density by pan-RT-qPCR.
- Identification of Plasmodium species.
- Detection of pfhrp2 and pfhrp3 deletion.
- STATISTICAL ANALYSES
- RESULTS
- DISCUSSION
- CONCLUSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization , 2022. World Malaria Report 2022. Geneva, Switzerland: WHO.
-
2.
Rosenthal PJ , 2022. Malaria in 2022: Challenges and progress. Am J Trop Med Hyg 106: 1565–1567.
-
3.
Feleke SM et al., 2021. Plasmodium falciparum is evolving to escape malaria rapid diagnostic tests in Ethiopia. Nat Microbiol 6: 1289–1299.
-
4.
Gao L , Shi Q , Liu Z , Li Z , Dong X , 2023. Impact of the COVID-19 pandemic on malaria control in Africa: A preliminary analysis. Trop Med Infect Dis 8: 67.
-
5.
Jagannathan P , Kakuru A , 2022. Malaria in 2022: Increasing challenges, cautious optimism. Nat Commun 13: 2678.
-
6.
World Health Organization , 2020. World Malaria Report 2020: 20 Years of Global Progress and Challenges. Geneva, Switzerland: WHO.
-
7.
World Health Organization , 2019. World Malaria Report 2019. Geneva, Switzerland: WHO.
-
8.
Aniweh Y et al., 2023. Comparative susceptibility of Plasmodium ovale and Plasmodium falciparum field isolates to reference and lead candidate antimalarial drugs in Ghana. Microbiol Spectr 11: e0491622.
-
9.
Herman C et al., 2023. Non-falciparum malaria infection and IgG seroprevalence among children under 15 years in Nigeria, 2018. Nat Commun 14: 1360.
-
10.
Sendor R et al., 2023. Similar prevalence of Plasmodium falciparum and non-P. falciparum malaria infections among schoolchildren, Tanzania. Emerg Infect Dis 29: 1143–1153.
-
11.
Kassile T , Lokina R , Mujinja P , Mmbando BP , 2014. Determinants of delay in care seeking among children under five with fever in Dodoma region, central Tanzania: A cross-sectional study. Malar J 13: 348.
-
12.
White NJ , Watson JA , Uyongo S , Williams TN , Maitland KM , 2022. Substantial misdiagnosis of severe malaria in African children. Lancet 400: 807.
-
13.
Tangpukdee N , Duangdee C , Wilairatana P , Krudsood S , 2009. Malaria diagnosis: A brief review. Korean J Parasitol 47: 93–102.
-
14.
Wilson ML , 2012. Malaria rapid diagnostic tests. Clin Infect Dis 54: 1637–1641.
-
15.
Houzé S , 2017. Rapid diagnostic test for malaria. Bull Soc Pathol Exot 110: 49–54.
-
16.
Wanja EW , Kuya N , Moranga C , Hickman M , Johnson JD , Moseti C , Anova L , Ogutu B , Ohrt C , 2016. Field evaluation of diagnostic performance of malaria rapid diagnostic tests in western Kenya. Malar J 15: 456.
-
17.
Wongsrichanalai C , Barcus MJ , Muth S , Sutamihardja A , Wernsdorfer WH , 2007. A review of malaria diagnostic tools: Microscopy and rapid diagnostic test (RDT). Am J Trop Med Hyg 77 (Suppl ):119–127.
-
18.
Góes L , Chamma-Siqueira N , Peres JM , Nascimento JM , Valle S , Arcanjo AR , Lacerda M , Blume L , Póvoa M , Viana G , 2020. Evaluation of histidine-rich proteins 2 and 3 gene deletions in Plasmodium falciparum in endemic areas of the Brazilian Amazon. Int J Environ Res Public Health 18: 123.
-
19.
Golassa L , Messele A , Amambua-Ngwa A , Swedberg G , 2020. High prevalence and extended deletions in Plasmodium falciparum hrp2/3 genomic loci in Ethiopia. PLoS One 15: e0241807.
-
20.
Berzosa P , González V , Taravillo L , Mayor A , Romay-Barja M , GarcÃa L , Ncogo P , Riloha M , Benito A , 2020. First evidence of the deletion in the pfhrp2 and pfhrp3 genes in Plasmodium falciparum from Equatorial Guinea. Malar J 19: 99.
-
21.
Berzosa P et al., 2018. Comparison of three diagnostic methods (microscopy, RDT, and PCR) for the detection of malaria parasites in representative samples from Equatorial Guinea. Malar J 17: 333.
-
22.
Mangold KA , Manson RU , Koay ESC , Stephens L , Regner M , Thomson RB Jr , Peterson LR , Kaul KL , 2005. Real-time PCR for detection and identification of Plasmodium spp. J Clin Microbiol 43: 2435–2440.
-
23.
Dozie U , Chukwuocha UM , 2016. Comparative evaluation of malaria rapid diagnostic test kits commercially available in parts of south eastern Nigeria. J Trop Dis 4: 201.
-
24.
Okoro C , Chukwuocha UM , Nwakwuo GC , Ukaga CN , 2015. Presumptive diagnosis and treatment of malaria in febrile children in parts of south eastern Nigeria. J Infect Dis Ther 3: 2332-0766.100240.
-
25.
Cheesbrough M , 2005. District Laboratory Practice in Tropical Countries, 2nd edition. Cambridge, United Kingdom: Cambridge University Press.
-
26.
Groger M et al., 2018. Prospective clinical trial assessing species-specific efficacy of artemether-lumefantrine for the treatment of Plasmodium malariae, Plasmodium ovale, and mixed Plasmodium malaria in Gabon. Antimicrob Agents Chemother 62: e01758-17.
-
27.
Woldearegai TG , Lalremruata A , Nguyen TT , Gmeiner M , Veletzky L , Tazemda-Kuitsouc GB , Matsiegui PB , Mordmüller B , Held J , 2019. Characterization of Plasmodium infections among inhabitants of rural areas in Gabon. Sci Rep 9: 9784.
-
28.
Bustin SA et al., 2009. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611–622.
-
29.
Kreidenweiss A et al., 2019. Monitoring the threatened utility of malaria rapid diagnostic tests by novel high-throughput detection of Plasmodium falciparum hrp2 and hrp3 deletions: A cross-sectional, diagnostic accuracy study. EBioMedicine 50: 14–22.
-
30.
World Health Organization , 2017. False-Negative RDT Results and Implications of New Reports of P. falciparum Histidine-Rich Protein 2/3 Gene Deletions. Geneva, Switzerland: WHO.
-
31.
Addai-Mensah O et al., 2020. Plasmodium falciparum histidine-rich protein 2 diversity in Ghana. Malar J 19: 256.
-
32.
Nolder D et al., 2021. Failure of rapid diagnostic tests in Plasmodium falciparum malaria cases among travelers to the UK and Ireland: Identification and characterisation of the parasites. Int J Infect Dis 108: 137–144.
-
33.
Ayogu EE , Ukwe CV , Nna EO , 2016. Assessing the reliability of microscopy and rapid diagnostic tests in malaria diagnosis in areas with varying parasite density among older children and adult patients in Nigeria. J Postgrad Med 62: 150–156.
-
34.
Azikiwe CC , Ifezulike CC , Siminialayi IM , Amazu LU , Enye JC , Nwakwunite OE , 2012. A comparative laboratory diagnosis of malaria: Microscopy versus rapid diagnostic test kits. Asian Pac J Trop Biomed 2: 307–310.
-
35.
Oboh MA , Oriero EC , Ndiaye T , Badiane AS , Ndiaye D , Amambua-Ngwa A , 2021. Comparative analysis of four malaria diagnostic tools and implications for malaria treatment in southwestern Nigeria. Int J Infect Dis 108: 377–381.
-
36.
Aribodor D , Njoku OO , Eneanya CI , Onyali IO , 2003. Studies on prevalence of malaria and management practices of the Azia community, Ihiala L.G.A., Anambra State, south-east Nigeria. Niger J Parasitol 24: 33–38.
-
37.
Nwaorgu O , Orajaka B , 2011. Prevalence of malaria among children 1–10 years old in communities in Awka north local government area, Anambra State Southeast Nigeria. Afr Res Rev 5: 264–281.
-
38.
Krueger T et al., 2023. Low prevalence of Plasmodium falciparum histidine-rich protein 2 and 3 gene deletions: A multiregional study in Central and West Africa. Pathogens 12: 455.
-
39.
Tian W , Yan P , Xu N , Chakravorty A , Liefke R , Xi Q , Wang Z , 2019. The HRP3 PWWP domain recognizes the minor groove of double-stranded DNA and recruits HRP3 to chromatin. Nucleic Acids Res 47: 5436–5448.
-
40.
Tran TM et al., 2013. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin Infect Dis 57: 40–47.
-
41.
Costa GL et al., 2021. A comprehensive analysis of the genetic diversity of Plasmodium falciparum histidine-rich protein 2 (PfHRP2) in the Brazilian Amazon. Front Cell Infect Microbiol 11: 742681.
-
42.
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.
-
43.
Beshir KB , Sepúlveda N , Bharmal J , Robinson A , Mwanguzi J , Busula AO , de Boer JG , Sutherland C , Cunningham J , Hopkins H , 2017. Plasmodium falciparum parasites with histidine-rich protein 2 (pfhrp2) and pfhrp3 gene deletions in two endemic regions of Kenya. Sci Rep 7: 14718.
-
44.
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.
-
45.
Berhane A , Russom M , Bahta I , Hagos F , Ghirmai M , Uqubay S , 2017. Rapid diagnostic tests failing to detect Plasmodium falciparum infections in Eritrea: An investigation of reported false negative RDT results. Malar J 16: 105.
-
46.
Prosser C , Gresty K , Ellis J , Meyer W , Anderson K , Lee R , Chng Q , 2021. Plasmodium falciparum histidine-rich protein 2 and 3 gene deletions in strains from Nigeria, Sudan, and South Sudan. Emerg Infect Dis 27: 471–479.
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Evaluating Malaria Rapid Diagnostic Tests and Microscopy for Detecting Plasmodium Infection and Status of Plasmodium falciparum Histidine-Rich Protein 2/3 Gene Deletions in Southeastern Nigeria
Moses Ikegbunam
Moses Ikegbunam
Department of Pharmaceutical Microbiology and Biotechnology, Nnamdi Azikiwe University, Awka, Nigeria;
Molecular Research Foundation for Students and Scientist, Nnamdi Azikiwe University, Awka, Nigeria;
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Molecular Research Foundation for Students and Scientist, Nnamdi Azikiwe University, Awka, Nigeria;
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Maike Maurer
Maike Maurer
Institute of Tropical Medicine, University of Tübingen, Germany;
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Harrison Abone
Harrison Abone
Department of Pharmaceutical Microbiology and Biotechnology, Nnamdi Azikiwe University, Awka, Nigeria;
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Dorothy Ezeagwuna
Dorothy Ezeagwuna
Departement of Parasitology and Entomology, Nnamdi Azikiwe University, Awka, Nigeria;
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Thaisa Lucas Sandri
Thaisa Lucas Sandri
Institute of Tropical Medicine, University of Tübingen, Germany;
Synovo GmbH, Tübingen, Germany;
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Synovo GmbH, Tübingen, Germany;
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Charles Esimone
Charles Esimone
Department of Pharmaceutical Microbiology and Biotechnology, Nnamdi Azikiwe University, Awka, Nigeria;
Molecular Research Foundation for Students and Scientist, Nnamdi Azikiwe University, Awka, Nigeria;
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Molecular Research Foundation for Students and Scientist, Nnamdi Azikiwe University, Awka, Nigeria;
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Olusola Ojurongbe
Olusola Ojurongbe
Department of Medical Microbiology & Parasitology, Ladoke Akintola University of Technology, Ogbomosho, Nigeria;
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Tamirat Gebru Woldearegai
Tamirat Gebru Woldearegai
Institute of Tropical Medicine, University of Tübingen, Germany;
German Center for Infection Research (DZIF), Tübingen, Germany;
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German Center for Infection Research (DZIF), Tübingen, Germany;
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Andrea Kreidenweiss
Andrea Kreidenweiss
Institute of Tropical Medicine, University of Tübingen, Germany;
German Center for Infection Research (DZIF), Tübingen, Germany;
Center de Recherches Médicales de Lambaréné (CERMEL), Gabon
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Jana Held
Jana Held
Institute of Tropical Medicine, University of Tübingen, Germany;
German Center for Infection Research (DZIF), Tübingen, Germany;
Center de Recherches Médicales de Lambaréné (CERMEL), Gabon
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Rolf Fendel
Rolf Fendel
Institute of Tropical Medicine, University of Tübingen, Germany;
German Center for Infection Research (DZIF), Tübingen, Germany;
Center de Recherches Médicales de Lambaréné (CERMEL), Gabon
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ABSTRACT.
Delays in malaria diagnosis increase treatment failures and deaths. In endemic regions, standard diagnostic methods are microscopy and malaria rapid diagnostic tests (mRDTs) detecting Plasmodium falciparum histidine-rich protein 2/3 (PFHRP2/PFHRP3), but gene deletions can allow certain parasites to remain undetected. We enlisted a cohort comprising 207 symptomatic individuals, encompassing both children and adults, at a hospital in Nnewi, Nigeria. The prevalence of parasites was determined using a highly sensitive, species-specific quantitative polymerase chain reaction (SS-qPCR). Within a subset of 132 participants, we assessed the sensitivity and specificity of microscopy and HRP2-mRDTs in comparison to SS-qPCR for the detection of P. falciparum. We also investigated the prevalence of pfhrp2/pfhrp3 gene deletions. Greater sensitivity was achieved with mRDTs (95%) compared with microscopy (77%). Also, mRDTs exhibited greater specificity (68%) than microscopy (44%). The positive predictive value of mRDTs (89%) surpassed that of microscopy (80%), suggesting a greater probability of accurately indicating the presence of infection. The negative predictive value of mRDTs (82%) was far greater than microscopy (39%). Of the 165 P. falciparum–positive samples screened for pfhrp2/pfhrp3 gene deletions, one gene deletion was detected in one sample. Regarding infection prevalence, 84% were positive for Plasmodium spp. (by reverse transcription [RT]-qPCR), with P. falciparum responsible for the majority (97%) of positive cases. Thus, exclusive reliance on microscopy in endemic areas may impede control efforts resulting from false negatives, underscoring the necessity for enhanced training and advocating for high-throughput molecular testing such as RT-qPCR or qPCR at referral centers to address limitations.
- Supplemental Materials (PDF 157.33 KB)
Author Notes
Financial support: This work was funded in part through a
Disclosure: The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. This study received ethical approval from the Ethics Review Board, Nnamdi Azikiwe University Teaching Hospital, Nnewi, southeastern Nigeria (approval no. NAUTH/CS/66/Vol.11/185/2018/118). Written informed consent was obtained from participants or parents/guardians of all participating children.
Data availability: The data sets used in this study are available at the repository of the Institute for Tropical Medicine, Germany.
Authors’ addresses: Moses Ikegbunam, Harrison Abone, and Charles Esimone, Department of Pharmaceutical Microbiology and Biotechnology, Nnamdi Azikiwe University, Awka, Nigeria, E-mails: mn.ikegbunam@unizik.edu.ng, harrisonabone@gmail.com, and co.esimone@unizik.edu.ng. Maike Maurer, Tamirat Gebru Woldearegai, Andrea Kreidenweiss, Jana Held, and Rolf Fendel, Institute of Tropical Medicine, University of Tübingen, Germany, E-mails: m.maurer94@gmx.de, tamirat-gebru.woldearegai@uni-tuebingen.de, andrea.kreidenweiss@uni-tuebingen.de, jana.held@uni-tuebingen.de, and rolf.fendel@uni-tuebingen.de. Dorothy Ezeagwuna, Department of Parasitology and Entomology, Nnamdi Azikiwe University, Awka, Nigeria, E-mail: d.ezeagwuna@unizik.edu.ng. Thaisa Lucas Sandri, Synovo GmbH, Tübingen, Germany, E-mail: thasandri81@gmail.com. Olusola Ojurongbe, Department of Medical Microbiology & Parasitology, Ladoke Akintola University of Technology, Ogbomosho, Nigeria, E-mail: oojurongbe@lautech.edu.ng.
- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Patient population and sample collection.
- Parasite detection by microscopy and mRDT.
- Nucleic acid preparation.
- Pan-Plasmodium detection by reverse transcription qPCR.
- Standard curve for quantification of parasite density by pan-RT-qPCR.
- Identification of Plasmodium species.
- Detection of pfhrp2 and pfhrp3 deletion.
- STATISTICAL ANALYSES
- RESULTS
- DISCUSSION
- CONCLUSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization , 2022. World Malaria Report 2022. Geneva, Switzerland: WHO.
-
2.
Rosenthal PJ , 2022. Malaria in 2022: Challenges and progress. Am J Trop Med Hyg 106: 1565–1567.
-
3.
Feleke SM et al., 2021. Plasmodium falciparum is evolving to escape malaria rapid diagnostic tests in Ethiopia. Nat Microbiol 6: 1289–1299.
-
4.
Gao L , Shi Q , Liu Z , Li Z , Dong X , 2023. Impact of the COVID-19 pandemic on malaria control in Africa: A preliminary analysis. Trop Med Infect Dis 8: 67.
-
5.
Jagannathan P , Kakuru A , 2022. Malaria in 2022: Increasing challenges, cautious optimism. Nat Commun 13: 2678.
-
6.
World Health Organization , 2020. World Malaria Report 2020: 20 Years of Global Progress and Challenges. Geneva, Switzerland: WHO.
-
7.
World Health Organization , 2019. World Malaria Report 2019. Geneva, Switzerland: WHO.
-
8.
Aniweh Y et al., 2023. Comparative susceptibility of Plasmodium ovale and Plasmodium falciparum field isolates to reference and lead candidate antimalarial drugs in Ghana. Microbiol Spectr 11: e0491622.
-
9.
Herman C et al., 2023. Non-falciparum malaria infection and IgG seroprevalence among children under 15 years in Nigeria, 2018. Nat Commun 14: 1360.
-
10.
Sendor R et al., 2023. Similar prevalence of Plasmodium falciparum and non-P. falciparum malaria infections among schoolchildren, Tanzania. Emerg Infect Dis 29: 1143–1153.
-
11.
Kassile T , Lokina R , Mujinja P , Mmbando BP , 2014. Determinants of delay in care seeking among children under five with fever in Dodoma region, central Tanzania: A cross-sectional study. Malar J 13: 348.
-
12.
White NJ , Watson JA , Uyongo S , Williams TN , Maitland KM , 2022. Substantial misdiagnosis of severe malaria in African children. Lancet 400: 807.
-
13.
Tangpukdee N , Duangdee C , Wilairatana P , Krudsood S , 2009. Malaria diagnosis: A brief review. Korean J Parasitol 47: 93–102.
-
14.
Wilson ML , 2012. Malaria rapid diagnostic tests. Clin Infect Dis 54: 1637–1641.
-
15.
Houzé S , 2017. Rapid diagnostic test for malaria. Bull Soc Pathol Exot 110: 49–54.
-
16.
Wanja EW , Kuya N , Moranga C , Hickman M , Johnson JD , Moseti C , Anova L , Ogutu B , Ohrt C , 2016. Field evaluation of diagnostic performance of malaria rapid diagnostic tests in western Kenya. Malar J 15: 456.
-
17.
Wongsrichanalai C , Barcus MJ , Muth S , Sutamihardja A , Wernsdorfer WH , 2007. A review of malaria diagnostic tools: Microscopy and rapid diagnostic test (RDT). Am J Trop Med Hyg 77 (Suppl ):119–127.
-
18.
Góes L , Chamma-Siqueira N , Peres JM , Nascimento JM , Valle S , Arcanjo AR , Lacerda M , Blume L , Póvoa M , Viana G , 2020. Evaluation of histidine-rich proteins 2 and 3 gene deletions in Plasmodium falciparum in endemic areas of the Brazilian Amazon. Int J Environ Res Public Health 18: 123.
-
19.
Golassa L , Messele A , Amambua-Ngwa A , Swedberg G , 2020. High prevalence and extended deletions in Plasmodium falciparum hrp2/3 genomic loci in Ethiopia. PLoS One 15: e0241807.
-
20.
Berzosa P , González V , Taravillo L , Mayor A , Romay-Barja M , GarcÃa L , Ncogo P , Riloha M , Benito A , 2020. First evidence of the deletion in the pfhrp2 and pfhrp3 genes in Plasmodium falciparum from Equatorial Guinea. Malar J 19: 99.
-
21.
Berzosa P et al., 2018. Comparison of three diagnostic methods (microscopy, RDT, and PCR) for the detection of malaria parasites in representative samples from Equatorial Guinea. Malar J 17: 333.
-
22.
Mangold KA , Manson RU , Koay ESC , Stephens L , Regner M , Thomson RB Jr , Peterson LR , Kaul KL , 2005. Real-time PCR for detection and identification of Plasmodium spp. J Clin Microbiol 43: 2435–2440.
-
23.
Dozie U , Chukwuocha UM , 2016. Comparative evaluation of malaria rapid diagnostic test kits commercially available in parts of south eastern Nigeria. J Trop Dis 4: 201.
-
24.
Okoro C , Chukwuocha UM , Nwakwuo GC , Ukaga CN , 2015. Presumptive diagnosis and treatment of malaria in febrile children in parts of south eastern Nigeria. J Infect Dis Ther 3: 2332-0766.100240.
-
25.
Cheesbrough M , 2005. District Laboratory Practice in Tropical Countries, 2nd edition. Cambridge, United Kingdom: Cambridge University Press.
-
26.
Groger M et al., 2018. Prospective clinical trial assessing species-specific efficacy of artemether-lumefantrine for the treatment of Plasmodium malariae, Plasmodium ovale, and mixed Plasmodium malaria in Gabon. Antimicrob Agents Chemother 62: e01758-17.
-
27.
Woldearegai TG , Lalremruata A , Nguyen TT , Gmeiner M , Veletzky L , Tazemda-Kuitsouc GB , Matsiegui PB , Mordmüller B , Held J , 2019. Characterization of Plasmodium infections among inhabitants of rural areas in Gabon. Sci Rep 9: 9784.
-
28.
Bustin SA et al., 2009. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611–622.
-
29.
Kreidenweiss A et al., 2019. Monitoring the threatened utility of malaria rapid diagnostic tests by novel high-throughput detection of Plasmodium falciparum hrp2 and hrp3 deletions: A cross-sectional, diagnostic accuracy study. EBioMedicine 50: 14–22.
-
30.
World Health Organization , 2017. False-Negative RDT Results and Implications of New Reports of P. falciparum Histidine-Rich Protein 2/3 Gene Deletions. Geneva, Switzerland: WHO.
-
31.
Addai-Mensah O et al., 2020. Plasmodium falciparum histidine-rich protein 2 diversity in Ghana. Malar J 19: 256.
-
32.
Nolder D et al., 2021. Failure of rapid diagnostic tests in Plasmodium falciparum malaria cases among travelers to the UK and Ireland: Identification and characterisation of the parasites. Int J Infect Dis 108: 137–144.
-
33.
Ayogu EE , Ukwe CV , Nna EO , 2016. Assessing the reliability of microscopy and rapid diagnostic tests in malaria diagnosis in areas with varying parasite density among older children and adult patients in Nigeria. J Postgrad Med 62: 150–156.
-
34.
Azikiwe CC , Ifezulike CC , Siminialayi IM , Amazu LU , Enye JC , Nwakwunite OE , 2012. A comparative laboratory diagnosis of malaria: Microscopy versus rapid diagnostic test kits. Asian Pac J Trop Biomed 2: 307–310.
-
35.
Oboh MA , Oriero EC , Ndiaye T , Badiane AS , Ndiaye D , Amambua-Ngwa A , 2021. Comparative analysis of four malaria diagnostic tools and implications for malaria treatment in southwestern Nigeria. Int J Infect Dis 108: 377–381.
-
36.
Aribodor D , Njoku OO , Eneanya CI , Onyali IO , 2003. Studies on prevalence of malaria and management practices of the Azia community, Ihiala L.G.A., Anambra State, south-east Nigeria. Niger J Parasitol 24: 33–38.
-
37.
Nwaorgu O , Orajaka B , 2011. Prevalence of malaria among children 1–10 years old in communities in Awka north local government area, Anambra State Southeast Nigeria. Afr Res Rev 5: 264–281.
-
38.
Krueger T et al., 2023. Low prevalence of Plasmodium falciparum histidine-rich protein 2 and 3 gene deletions: A multiregional study in Central and West Africa. Pathogens 12: 455.
-
39.
Tian W , Yan P , Xu N , Chakravorty A , Liefke R , Xi Q , Wang Z , 2019. The HRP3 PWWP domain recognizes the minor groove of double-stranded DNA and recruits HRP3 to chromatin. Nucleic Acids Res 47: 5436–5448.
-
40.
Tran TM et al., 2013. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin Infect Dis 57: 40–47.
-
41.
Costa GL et al., 2021. A comprehensive analysis of the genetic diversity of Plasmodium falciparum histidine-rich protein 2 (PfHRP2) in the Brazilian Amazon. Front Cell Infect Microbiol 11: 742681.
-
42.
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.
-
43.
Beshir KB , Sepúlveda N , Bharmal J , Robinson A , Mwanguzi J , Busula AO , de Boer JG , Sutherland C , Cunningham J , Hopkins H , 2017. Plasmodium falciparum parasites with histidine-rich protein 2 (pfhrp2) and pfhrp3 gene deletions in two endemic regions of Kenya. Sci Rep 7: 14718.
-
44.
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.
-
45.
Berhane A , Russom M , Bahta I , Hagos F , Ghirmai M , Uqubay S , 2017. Rapid diagnostic tests failing to detect Plasmodium falciparum infections in Eritrea: An investigation of reported false negative RDT results. Malar J 16: 105.
-
46.
Prosser C , Gresty K , Ellis J , Meyer W , Anderson K , Lee R , Chng Q , 2021. Plasmodium falciparum histidine-rich protein 2 and 3 gene deletions in strains from Nigeria, Sudan, and South Sudan. Emerg Infect Dis 27: 471–479.
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