Author:
- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- STATISTICAL ANALYSES
- RESULTS
- Malaria screening.
- False-positive and false-negative mRDT results.
- Selection of samples for the evaluation of hrp2/3 deletion.
- hrp2/3 gene deletion evaluation using multiplexed qPCR.
- Histidine-rich protein 2 antigen detection using bead-based immunoassay.
- Comparison of qPCR and bead-based immunoassay 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, 2012. How do we best diagnose malaria in Africa? Am J Trop Med Hyg 86: 192–193.
-
3.
Centers for Disease Control and Prevention, 2009. CDC Malaria Rapid Diagnostic Tests. Available at: https://www.cdc.gov/malaria/malaria_worldwide/reduction/dx_rdt.html. Accessed November 12, 2023.
-
4.
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.
-
5.
Martiáñez-Vendrell X, Skjefte M, Sikka R, Gupta H, 2022. Factors affecting the performance of HRP2-based malaria rapid diagnostic tests. Trop Med Infect Dis 7: 265.
-
6.
Gatton ML, Ciketic S, Barnwell JW, Cheng Q, Chiodini PL, Incardona S, Bell D, Cunningham J, González IJ, 2018. An assessment of false positive rates for malaria rapid diagnostic tests caused by non-Plasmodium infectious agents and immunological factors. PLoS One 13: e0197395.
-
7.
Watson OJ, Sumner KM, Janko M, Goel V, Winskill P, Slater HC, Ghani A, Meshnick SR, Parr JB, 2019. False-negative malaria rapid diagnostic test results and their impact on community-based malaria surveys in sub-Saharan Africa. BMJ Glob Health 4: e001582.
-
8.
Feleke SM et al., 2021. Plasmodium falciparum is evolving to escape malaria rapid diagnostic tests in Ethiopia. Nat Microbiol 6: 1289–1299.
-
9.
Prosser C, Gresty K, Ellis J, Meyer W, Anderson K, Lee R, Cheng 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.
-
10.
Mihreteab S et al., 2023. Increasing prevalence of artemisinin-resistant HRP2-negative malaria in Eritrea. N Engl J Med 389: 1191–1202.
-
11.
Thomson R, Parr JB, Cheng Q, Chenet S, Perkins M, Cunningham J, 2020. Prevalence of Plasmodium falciparum lacking histidine-rich proteins 2 and 3: A systematic review. Bull World Health Organ 98: 558–568F.
-
12.
Markwalter CF, Ngasala B, Mowatt T, Basham C, Park Z, Loya M, Muller M, Plowe C, Nyunt M, Lin JT, 2021. Direct comparison of standard and ultrasensitive PCR for the detection of Plasmodium falciparum from dried blood spots in Bagamoyo, Tanzania. Am J Trop Med Hyg 104: 1371–1374.
-
13.
Rapp T et al., 2024. Microheterogeneity of transmission shapes submicroscopic malaria carriage in coastal Tanzania. J Infect Dis 230: 485–496.
-
14.
Teyssier NB, Chen A, Duarte EM, Sit R, Greenhouse B, Tessema SK, 2021. Optimization of whole-genome sequencing of Plasmodium falciparum from low-density dried blood spot samples. Malar J 20: 116.
-
15.
Grignard L et al., 2020. A novel multiplex qPCR assay for detection of Plasmodium falciparum with histidine-rich protein 2 and 3 (pfhrp2 and pfhrp3) deletions in polyclonal infections. EBioMedicine 55: 102757.
-
16.
Beshir KB, Parr JB, Cunningham J, Cheng Q, Rogier E, 2022. Screening strategies and laboratory assays to support Plasmodium falciparum histidine-rich protein deletion surveillance: Where we are and what is needed. Malar J 21: 201.
-
17.
Plucinski MM et al., 2019. Screening for pfhrp2/3-deleted Plasmodium falciparum, non-falciparum, and low-density malaria infections by a multiplex antigen assay. J Infect Dis 219: 437–447.
-
18.
Rogier E et al., 2017. Bead-based immunoassay allows sub-picogram detection of histidine-rich protein 2 from Plasmodium falciparum and estimates reliability of malaria rapid diagnostic tests. PLoS One 12: e0172139.
-
19.
Ngasala B et al., 2024. Evaluation of malaria rapid diagnostic test performance and pfhrp2 deletion in Tanzania school surveys, 2017. Am J Trop Med Hyg 110: 887–891.
-
20.
Kong A, Wilson SA, Ah Y, Nace D, Rogier E, Aidoo M, 2021. HRP2 and HRP3 cross-reactivity and implications for HRP2-based RDT use in regions with Plasmodium falciparum hrp2 gene deletions. Malar J 20: 207.
-
21.
World Health Organization. Statement by the Malaria Policy Advisory Group on the Urgent Need to Address the High Prevalence of pfhrp2/3 Gene Deletions in the Horn of Africa and Beyond. Available at: https://www.who.int/news/item/28-05-2021-statement-by-the-malaria-policy-advisory-group-on-the-urgent-need-to-address-the-high-prevalence-of-pfhrp2-3-gene-deletions-in-the-horn-of-africa-and-beyond. Accessed March 20, 2024.
-
22.
Badiane A, Thwing J, Williamson J, Rogier E, Diallo MA, Ndiaye D, 2022. Sensitivity and specificity for malaria classification of febrile persons by rapid diagnostic test, microscopy, parasite DNA, histidine-rich protein 2, and IgG: Dakar, Senegal 2015. Int J Infect Dis 121: 92–97.
-
23.
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.
-
24.
Rogier E et al., 2023. Plasmodium falciparum pfhrp2 and pfhrp3 gene deletions among patients enrolled at 100 health facilities throughout Tanzania: February to July 2021. Sci Rep 14: 8158.
-
25.
Poti KE, Sullivan DJ, Dondorp AM, Woodrow CJ, 2020. HRP2: Transforming malaria diagnosis, but with caveats. Trends Parasitol 36: 112–126.
-
26.
Mwesigwa J et al., 2019. Field performance of the malaria highly sensitive rapid diagnostic test in a setting of varying malaria transmission. Malar J 18: 288.
-
27.
Shankar H, Singh MP, Phookan S, Singh K, Mishra N, 2021. Diagnostic performance of rapid diagnostic test, light microscopy and polymerase chain reaction during mass survey conducted in low and high malaria-endemic areas from two North-Eastern states of India. Parasitol Res 120: 2251–2261.
-
28.
Harris I et al., 2010. 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 9: 254.
-
29.
Abeku TA, Kristan M, Jones C, Beard J, Mueller DH, Okia M, Rapuoda B, Greenwood B, Cox J, 2008. Determinants of the accuracy of rapid diagnostic tests in malaria case management: Evidence from low and moderate transmission settings in the East African highlands. Malar J 7: 202.
-
30.
Wu L, van den Hoogen LL, Slater H, Walker PGT, Ghani AC, Drakeley CJ, Okell LC, 2015. Comparison of diagnostics for the detection of asymptomatic Plasmodium falciparum infections to inform control and elimination strategies. Nature 528: S86–S93.
-
31.
Fagbamigbe AF, 2019. On the discriminatory and predictive accuracy of the RDT against the microscopy in the diagnosis of malaria among under-five children in Nigeria. Malar J 18: 46.
-
32.
Andolina C et al., 2023. Plasmodium falciparum gametocyte carriage in longitudinally monitored incident infections is associated with duration of infection and human host factors. Sci Rep 13: 7072.
-
33.
Watson OJ et al., 2024. Global Risk of Selection and Spread of Plasmodium falciparum Histidine-Rich Protein 2 and 3 Gene Deletions. Available at: https://www.medrxiv.org/content/10.1101/2023.10.21.23297352v3. Accessed March 30, 2024.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 58427 | 58427 | 31490 |
| Full Text Views | 84 | 84 | 23 |
| PDF Downloads | 66 | 66 | 19 |
Assessment of Malaria Rapid Diagnostic Tests and Histidine-Rich Protein 2 Deletions among Asymptomatic Children and Adults in Bagamoyo, Tanzania
Billy Ngasala
Billy Ngasala
Department of Parasitology and Medical Entomology, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania;
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Kofi B. Opoku
Kofi B. Opoku
Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina;
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Kano Amagai
Kano Amagai
Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina;
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Ashenafi Assefa
Ashenafi Assefa
Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina;
Ethiopian Public Health Institute, Addis Ababa, Ethiopia;
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Ethiopian Public Health Institute, Addis Ababa, Ethiopia;
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Mwajabu Loya
Mwajabu Loya
Department of Parasitology and Medical Entomology, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania;
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Mwanaidi Nyange
Mwanaidi Nyange
Department of Parasitology and Medical Entomology, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania;
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Meredith Muller
Meredith Muller
Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina;
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Hamza Said
Hamza Said
Department of Parasitology and Medical Entomology, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania;
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Christopher Basham
Christopher Basham
Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina;
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Eric Rogier
Eric Rogier
Division of Digestive Disease and Nutrition, University of Kentucky, Lexington, Kentucky
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Jonathan J. Juliano
Jonathan J. Juliano
Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina;
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Jonathan B. Parr
Jonathan B. Parr
Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina;
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Jessica T. Lin
jessica_lin@med.unc.edu
Jessica T. Lin
Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina;
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ABSTRACT.
Malaria rapid diagnostic tests (mRDTs) that detect histidine-rich protein 2 (HRP2) remain the mainstay of falciparum malaria diagnosis in Sub-Saharan Africa. Understanding their test characteristics when used for surveillance in asymptomatic populations is important. We explored the rate of false-positive and false-negative mRDT results among asymptomatic persons >5 years old screened for malaria at schools and clinics in the rural Bagamoyo District using 18S ribosomal RNA real-time polymerase chain reaction (qPCR) as the reference test. Among 5,966 persons screened using mRDTs, microscopy, and qPCR tests from 2018 to 2021, 14% (832) were mRDT-positive. Twelve percent of these (98/832) were negative by both microscopy and qPCR, with children overrepresented among those with false-positive mRDTs. Among those who were mRDT-negative, 22% (1,136/5,134) tested qPCR-positive, predominantly because of low-density parasitemia (92% had <100 p/µL by qPCR). Among mRDT-negative samples with >100 p/µL, we looked for evidence of hrp2 or histidine-rich protein 3 (hrp3) deletion using two methods, multiplexed qPCR and multiplex bead-based immunoassay. When sufficient parasite material existed for a reliable deletion assessment, 12/34 (35%) had evidence of hrp2/3 deletion by qPCR (nine hrp2–/3+ and three hrp2–/3–), and 20/52 (38%) had evidence of deletion by immunoassay. Only three isolates showed evidence of hrp2 deletion by both assays. In an area of low to moderate transmission in Tanzania, false-positive mRDTs are relatively common (12% of positive tests), and false-negative mRDTs are even more common (22% of negative tests), but hrp2/3 deletion causing false-negative mRDTs remains rare (<1% of negative tests).
- Supplemental Materials (PDF 977.40 KB)
Author Notes
Financial support: This work was supported by the
Disclosures: J. B. Parr reports research support from Gilead Sciences and nonfinancial support from Abbott Laboratories and consults for Zymeron Corporation, all of which are outside the scope of the manuscript. The other authors declare no competing interests. All participants or their guardians provided informed consent. This study was approved by the institutional review boards at the University of North Carolina, Tanzania National Institute for Medical Research, and Muhimbili University of Health and Allied Sciences. Eric Rogier was employed at the US CDC at the time of this work.
Current contact information: Billy Ngasala, Mwajabu Loya, Mwanaidi Nyange, and Hamza Said, Department of Parasitology and Medical Entomology, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania, E-mails: bngasala70@yahoo.co.uk, loyamwajabu51@gmail.com, tudypeter18@gmail.com, and hsaidy122@gmail.com. Kofi B. Opoku, Kano Amagai, Meredith Muller, Christopher Basham, Jonathan J. Juliano, Jonathan B. Parr, and Jessica T. Lin, Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, NC, E-mails: kbopoku@unc.edu, kanoama@gmail.com, meredith.smith.4.ms@gmail.com, christopher-basham@live.com, jonathan_juliano@med.unc.edu, jonathan_parr@med.unc.edu, and jessica_lin@med.unc.edu. Ashenafi Assefa, Institute of Global Health and Infectious Diseases, University of North Carolina, Chapel Hill, NC, and Ethiopian Public Health Institute, Addis Ababa, Ethiopia, E-mail: ashenafi_assefa@med.unc.edu. Eric Rogier, Division of Digestive Disease and Nutrition, University of Kentucky, Lexington, KY, E-mail: erk_rogier@msn.com.
- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- STATISTICAL ANALYSES
- RESULTS
- Malaria screening.
- False-positive and false-negative mRDT results.
- Selection of samples for the evaluation of hrp2/3 deletion.
- hrp2/3 gene deletion evaluation using multiplexed qPCR.
- Histidine-rich protein 2 antigen detection using bead-based immunoassay.
- Comparison of qPCR and bead-based immunoassay 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, 2012. How do we best diagnose malaria in Africa? Am J Trop Med Hyg 86: 192–193.
-
3.
Centers for Disease Control and Prevention, 2009. CDC Malaria Rapid Diagnostic Tests. Available at: https://www.cdc.gov/malaria/malaria_worldwide/reduction/dx_rdt.html. Accessed November 12, 2023.
-
4.
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.
-
5.
Martiáñez-Vendrell X, Skjefte M, Sikka R, Gupta H, 2022. Factors affecting the performance of HRP2-based malaria rapid diagnostic tests. Trop Med Infect Dis 7: 265.
-
6.
Gatton ML, Ciketic S, Barnwell JW, Cheng Q, Chiodini PL, Incardona S, Bell D, Cunningham J, González IJ, 2018. An assessment of false positive rates for malaria rapid diagnostic tests caused by non-Plasmodium infectious agents and immunological factors. PLoS One 13: e0197395.
-
7.
Watson OJ, Sumner KM, Janko M, Goel V, Winskill P, Slater HC, Ghani A, Meshnick SR, Parr JB, 2019. False-negative malaria rapid diagnostic test results and their impact on community-based malaria surveys in sub-Saharan Africa. BMJ Glob Health 4: e001582.
-
8.
Feleke SM et al., 2021. Plasmodium falciparum is evolving to escape malaria rapid diagnostic tests in Ethiopia. Nat Microbiol 6: 1289–1299.
-
9.
Prosser C, Gresty K, Ellis J, Meyer W, Anderson K, Lee R, Cheng 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.
-
10.
Mihreteab S et al., 2023. Increasing prevalence of artemisinin-resistant HRP2-negative malaria in Eritrea. N Engl J Med 389: 1191–1202.
-
11.
Thomson R, Parr JB, Cheng Q, Chenet S, Perkins M, Cunningham J, 2020. Prevalence of Plasmodium falciparum lacking histidine-rich proteins 2 and 3: A systematic review. Bull World Health Organ 98: 558–568F.
-
12.
Markwalter CF, Ngasala B, Mowatt T, Basham C, Park Z, Loya M, Muller M, Plowe C, Nyunt M, Lin JT, 2021. Direct comparison of standard and ultrasensitive PCR for the detection of Plasmodium falciparum from dried blood spots in Bagamoyo, Tanzania. Am J Trop Med Hyg 104: 1371–1374.
-
13.
Rapp T et al., 2024. Microheterogeneity of transmission shapes submicroscopic malaria carriage in coastal Tanzania. J Infect Dis 230: 485–496.
-
14.
Teyssier NB, Chen A, Duarte EM, Sit R, Greenhouse B, Tessema SK, 2021. Optimization of whole-genome sequencing of Plasmodium falciparum from low-density dried blood spot samples. Malar J 20: 116.
-
15.
Grignard L et al., 2020. A novel multiplex qPCR assay for detection of Plasmodium falciparum with histidine-rich protein 2 and 3 (pfhrp2 and pfhrp3) deletions in polyclonal infections. EBioMedicine 55: 102757.
-
16.
Beshir KB, Parr JB, Cunningham J, Cheng Q, Rogier E, 2022. Screening strategies and laboratory assays to support Plasmodium falciparum histidine-rich protein deletion surveillance: Where we are and what is needed. Malar J 21: 201.
-
17.
Plucinski MM et al., 2019. Screening for pfhrp2/3-deleted Plasmodium falciparum, non-falciparum, and low-density malaria infections by a multiplex antigen assay. J Infect Dis 219: 437–447.
-
18.
Rogier E et al., 2017. Bead-based immunoassay allows sub-picogram detection of histidine-rich protein 2 from Plasmodium falciparum and estimates reliability of malaria rapid diagnostic tests. PLoS One 12: e0172139.
-
19.
Ngasala B et al., 2024. Evaluation of malaria rapid diagnostic test performance and pfhrp2 deletion in Tanzania school surveys, 2017. Am J Trop Med Hyg 110: 887–891.
-
20.
Kong A, Wilson SA, Ah Y, Nace D, Rogier E, Aidoo M, 2021. HRP2 and HRP3 cross-reactivity and implications for HRP2-based RDT use in regions with Plasmodium falciparum hrp2 gene deletions. Malar J 20: 207.
-
21.
World Health Organization. Statement by the Malaria Policy Advisory Group on the Urgent Need to Address the High Prevalence of pfhrp2/3 Gene Deletions in the Horn of Africa and Beyond. Available at: https://www.who.int/news/item/28-05-2021-statement-by-the-malaria-policy-advisory-group-on-the-urgent-need-to-address-the-high-prevalence-of-pfhrp2-3-gene-deletions-in-the-horn-of-africa-and-beyond. Accessed March 20, 2024.
-
22.
Badiane A, Thwing J, Williamson J, Rogier E, Diallo MA, Ndiaye D, 2022. Sensitivity and specificity for malaria classification of febrile persons by rapid diagnostic test, microscopy, parasite DNA, histidine-rich protein 2, and IgG: Dakar, Senegal 2015. Int J Infect Dis 121: 92–97.
-
23.
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.
-
24.
Rogier E et al., 2023. Plasmodium falciparum pfhrp2 and pfhrp3 gene deletions among patients enrolled at 100 health facilities throughout Tanzania: February to July 2021. Sci Rep 14: 8158.
-
25.
Poti KE, Sullivan DJ, Dondorp AM, Woodrow CJ, 2020. HRP2: Transforming malaria diagnosis, but with caveats. Trends Parasitol 36: 112–126.
-
26.
Mwesigwa J et al., 2019. Field performance of the malaria highly sensitive rapid diagnostic test in a setting of varying malaria transmission. Malar J 18: 288.
-
27.
Shankar H, Singh MP, Phookan S, Singh K, Mishra N, 2021. Diagnostic performance of rapid diagnostic test, light microscopy and polymerase chain reaction during mass survey conducted in low and high malaria-endemic areas from two North-Eastern states of India. Parasitol Res 120: 2251–2261.
-
28.
Harris I et al., 2010. 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 9: 254.
-
29.
Abeku TA, Kristan M, Jones C, Beard J, Mueller DH, Okia M, Rapuoda B, Greenwood B, Cox J, 2008. Determinants of the accuracy of rapid diagnostic tests in malaria case management: Evidence from low and moderate transmission settings in the East African highlands. Malar J 7: 202.
-
30.
Wu L, van den Hoogen LL, Slater H, Walker PGT, Ghani AC, Drakeley CJ, Okell LC, 2015. Comparison of diagnostics for the detection of asymptomatic Plasmodium falciparum infections to inform control and elimination strategies. Nature 528: S86–S93.
-
31.
Fagbamigbe AF, 2019. On the discriminatory and predictive accuracy of the RDT against the microscopy in the diagnosis of malaria among under-five children in Nigeria. Malar J 18: 46.
-
32.
Andolina C et al., 2023. Plasmodium falciparum gametocyte carriage in longitudinally monitored incident infections is associated with duration of infection and human host factors. Sci Rep 13: 7072.
-
33.
Watson OJ et al., 2024. Global Risk of Selection and Spread of Plasmodium falciparum Histidine-Rich Protein 2 and 3 Gene Deletions. Available at: https://www.medrxiv.org/content/10.1101/2023.10.21.23297352v3. Accessed March 30, 2024.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 58427 | 58427 | 31490 |
| Full Text Views | 84 | 84 | 23 |
| PDF Downloads | 66 | 66 | 19 |