94
Views
0
CrossRef citations to date
0
Altmetric
Meta-analysis

Global polymorphism of Plasmodium falciparum histidine rich proteins 2/3 and impact on malaria rapid diagnostic test detection: a systematic review and meta-analysis

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 925-943 | Received 31 May 2023, Accepted 10 Aug 2023, Published online: 21 Sep 2023

References

  • World Health Organization. World malaria report 2022. WHO/HTM/GM. Geneva: World Health Organisation; 2022.
  • Beadle C, Long GW, McElroy PD, et al. Diagnosis of malaria by detection of Plasmodium falciparum HRP-2 antigen with a rapid dipstick antigen-capture assay. Lancet. 1994;343(8897):564–568. doi: 10.1016/S0140-6736(94)91520-2
  • Poti KE, Sullivan DJ, Dondorp AM, et al. HRP2: transforming malaria diagnosis, but with caveats. Trends Parasitol. 2020;36(2):112–126. doi: 10.1016/j.pt.2019.12.004
  • Kamgain L, Assam-Assam J-P, Kojom Foko LP, et al. Prevalence of malaria infection and reliability of ACCUCARE one step malaria test® for diagnosing malaria in people living with human immunodeficiency virus infection in Cameroon. Int J Trop Dis Health. 2017;21(2):1–10. doi: 10.9734/IJTDH/2017/30277
  • WHO. Malaria rapid diagnostic test performance: results of WHO product testing of malaria RDTs: round 7 (2015-2016). WHO Publications. 2015. http://www.who.int/malaria/publications/atoz/9789241510035/en/
  • Kojom Foko LP, Pande V, Singh V. Field performances of rapid diagnostic tests detecting human Plasmodium species: a systematic review and meta-analysis in India, 1990–2020. Diagnostics. 2021;11(4):590. doi: 10.3390/diagnostics11040590
  • Kojom LP, Singh V. Prevalence of Plasmodium falciparum field isolates with deletions in histidine-rich protein 2 and 3 genes in context with sub-Saharan Africa and India: a systematic review and meta-analysis. Malar J. 2020;19(1):46. doi: 10.1186/s12936-019-3090-6
  • Luchavez J, Baker J, Alcantara S, et al. Laboratory demonstration of a prozone-like effect in HRP2-detecting malaria rapid diagnostic tests: implications for clinical management. Malar J. 2011;10(1):286. doi: 10.1186/1475-2875-10-286
  • Kong A, Wilson SA, Ah Y, et al. HRP2 and HRP3 cross-reactivity and implications for HRP2-based RDT use in regions with Plasmodium falciparum hrp2 gene deletions. Malar J. 2021;20:207. doi: 10.1186/s12936-021-03739-6
  • Gamboa D, Ho MF, Bendezu J, et al. 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. 2010;5(1):e8091. doi: 10.1371/journal.pone.0008091
  • Houze S, Pessec L, Le BJ. Combined deletions of pfhrp2 and pfhrp3 genes result in Plasmodium falciparum malaria false-negative rapid diagnostic test. J Clin Microbiol. 2011;49(7):2694–2696. doi: 10.1128/JCM.00281-11
  • Parr JB, Kieto E, Phanzu F, et al. Analysis of false-negative rapid diagnostic tests for symptomatic malaria in the Democratic Republic of the Congo. Sci Rep 2021;11:6495. doi: 10.1038/s41598-021-85913-z
  • Feleke SM, Reichert EN, Mohammed H, et al. Plasmodium falciparum is evolving to escape malaria rapid diagnostic tests in Ethiopia. Nature Microbiol 2021;6:1289–1299. doi: 10.1038/s41564-021-00962-4
  • WHO. P. falciparum hrp2/3 gene deletions. Conclusions and recommendations of a technical consultation. Geneva, Switzerland, 7–8 July 2016. In Background document for Session 7, Malaria Policy Advisory Committee Meeting; 2016 Sep 14–16; Geneva, Switzerland. Available from: https://www.who.int/publications/i
  • Berhane A, Russom M, Bahta I, et al. Rapid diagnostic tests failing to detect Plasmodium falciparum infections in Eritrea: an investigation of reported false negative RDT results. Malar J. 2017;16(1):105. doi: 10.1186/s12936-017-1752-9
  • Menegon M, L’Episcopia M, Nurahmed AM, et al. Identification of Plasmodium falciparum isolates lacking histidine-rich protein 2 and 3 in Eritrea. Infect Gen Evol. 2017;55:131–134. doi: 10.1016/j.meegid.2017.09.004
  • Mihreteab S, Anderson K, Pasay C, et al. Epidemiology of mutant Plasmodium falciparum parasites lacking histidine-rich protein 2/3 genes in Eritrea 2 years after switching from HRP2-based RDTs. Sci Rep. 2021;11(1):21082. doi: 10.1038/s41598-021-00714-8
  • Gendrot M, Fawaz R, Dormoi J, et al. Genetic diversity and deletion of Plasmodium falciparum histidine-rich protein 2 and 3: a threat to diagnosis of P. falciparum malaria. Clin Microbiol Infect. 2019;25(5):580–585. doi: 10.1016/j.cmi.2018.09.009
  • Thomson R, Parr JB, Cheng Q, et al. Prevalence of Plasmodium falciparum lacking histidine-rich proteins 2 and 3: a systematic review. Bull World Health Organ. 2020;98(8):558–568F. doi: 10.2471/BLT.20.250621
  • Singh V, Kojom LP. Deletions in the Plasmodium falciparum histidine-rich protein 2 gene: an emerging threat to the elimination of malaria in India. J Vector Borne Dis. 2019;56(1):85–86. doi: 10.4103/0972-9062.257781
  • Lee N, Baker J, Andrews KT, et al. 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. 2006;44(8):2773–2778. doi: 10.1128/JCM.02557-05
  • Lee N, Gatton ML, Pelecanos A, et al. Identification of optimal epitopes for Plasmodium falciparum rapid diagnostic tests that target histidine-rich proteins 2 and 3. J Clin Microbiol. 2012;50(4):1397–1405. doi: 10.1128/JCM.06533-11
  • Baker J, Mccarthy J, Gatton M, et al. 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. 2005;192(5):870–877. doi: 10.1086/432010
  • Baker J, Ho M-F, Pelecanos A, et al. 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. 2010;9(1):129. doi: 10.1186/1475-2875-9-129
  • Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLOS Med. 2009;6(7):e1000097. doi: 10.1371/journal.pmed.1000097
  • Munn Z, MClinSc SM, Lisy K, et al. Methodological guidance for systematic reviews of observational epidemiological studies reporting prevalence and cumulative incidence data. Int J Evidence-Based Healthcare. 2015;13(3):147–153. doi: 10.1097/XEB.0000000000000054
  • Valentine JC, Pigott TD, Rothstein HR. How many studies do you need? A primer on statistical power for meta-analysis. J Edu Behavioral Stat. 2010;35(2):215–247. doi: 10.3102/1076998609346961
  • Cochran WG. The combination of estimates from different experiments. Biometrics. 1954;10(1):101–129. doi: 10.2307/3001666
  • Reid K. Interpreting and understanding meta-analysis graphs: a practical guide. Aus Fam Phys. 2006;35:635–638.
  • Sedgwick P. Meta-analyses: heterogeneity and subgroup analysis. BMJ (Online). 2013;346:f4040. doi: 10.1136/bmj.f4040
  • Willis BH, Riley RD. Measuring the statistical validity of summary meta-analysis and meta-regression results for use in clinical practice. Stat Med. 2017;36(21):3283–3301. doi: 10.1002/sim.7372
  • Egger M, Smith GD, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–634. doi: 10.1136/bmj.315.7109.629
  • Mavridis D, Salanti G. How to assess publication bias: funnel plot, trim-and-fill method and selection models. Evid Based Mental Health. 2014;17(1):30–30. doi: 10.1136/eb-2013-101699
  • Kumar N, Singh JPN, Pande V, et al. Genetic variation in histidine rich proteins among Indian Plasmodium falciparum population: possible cause of variable sensitivity of malaria rapid diagnostic tests. Malar J. 2012;11(1):298. Available from:. doi: 10.1186/1475-2875-11-298
  • Ramutton T, Hendriksen IC, Mwanga-Amumpaire J, et al. Sequence variation does not confound the measurement of plasma PfHRP2 concentration in African children presenting with severe malaria. Malar J. 2012;11(1):276. doi: 10.1186/1475-2875-11-276
  • Wurtz N, Fall B, Bui K, et al. Pfhrp2 and pfhrp3 polymorphisms in Plasmodium falciparum isolates from Dakar, Senegal: impact on rapid malaria diagnostic tests. Malar J. 2013;12(1):34. doi: 10.1186/1475-2875-12-34
  • Wurtz N, Briolant S, Lemarié D, et al. Delayed diagnosis of Plasmodium falciparum in a soldier in Uganda: false-positive rapid diagnostic test associated with reduced repeats in pfhrp2. Médecine et Santé Tropicales. 2013;23(2):181–184. doi: 10.1684/mst.2013.0171
  • Deme AB, Park DJ, Bei AK, et al. Analysis of pfhrp2 genetic diversity in Senegal and implications for use of rapid diagnostic tests. Malar J. 2014;13(1):34. doi: 10.1186/1475-2875-13-34
  • Yang Y, Zhang J, Wang G, et al. Polymorphism analysis of Plasmodium falciparum histidine-rich protein II and III. Chinese J Parasitol Parasitic Dis. 2014;32:373–376.
  • Atroosh WM, Al-Mekhlafi HM, Al-Jasari A, et al. Genetic variation of pfhrp2 in Plasmodium falciparum isolates from Yemen and the performance of HRP2-based malaria rapid diagnostic test. Parasites Vectors Available from. 2015;8:388. doi: 10.1186/s13071-015-1008-x
  • Li P, Xing H, Zhao Z, et al. Genetic diversity of Plasmodium falciparum histidine-rich protein 2 in the China-Myanmar border area. Acta Trop. 2015;152:26–31. doi: 10.1016/j.actatropica.2015.08.003
  • Bharti PK, Chandel HS, Ahmad A, et al. Prevalence of pfhrp2 and/or pfhrp3 gene deletion in Plasmodium falciparum population in eight highly endemic states in India. PLoS One. 2016;11(8):e0157949. doi: 10.1371/journal.pone.0157949
  • Dorado EJ, Okoth SA, Montenegro LM, et al. 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. 2016;11(9):e0163137. doi: 10.1371/journal.pone.0163137
  • Dong Y, Sun A, Chen M, et al. Analysis of polymorphism of Pfhrp2 gene in Plasmodium falciparum from falciparum malaria patients in Yunnan Province. Chinese J Schistosomiasis Control. 2016;28:411–417.
  • Bharti PK, Singh Chandel H, Krishna S, et al. Sequence variation in Plasmodium falciparum histidine rich proteins 2 and 3 in Indian isolates: implications for malaria rapid diagnostic test performance. Sci Rep 2017;7:1308. doi: 10.1038/s41598-017-01506-9
  • Nima MK, Hougard T, Hossain ME, et al. Case report: a case of Plasmodium falciparum hrp2 and hrp3 gene mutation in Bangladesh. Am J Trop Med Hyg. 2017;97(4):1155–1158. doi: 10.4269/ajtmh.16-0884
  • Nderu D, Kimani F, Thiong’o K, et al. PfHRP2-PfHRP3 diversity among Kenyan isolates and comparative evaluation of PfHRP2/pLDH malaria RDT with microscopy and nested PCR methodologies. Parasitol Int. 2018;67(6):793–799. doi: 10.1016/j.parint.2018.08.007
  • Pati P, Dhangadamajhi G, Bal M, et al. High proportions of pfhrp2 gene deletion and performance of HRP2-based rapid diagnostic test in Plasmodium falciparum field isolates of Odisha. Malar J. 2018;17(1):394. doi: 10.1186/s12936-018-2502-3
  • Willie N, Mehlotra RK, Howes RE, et al. 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. Am J Trop Med Hyg. 2018;98(6):1683–1691. doi: 10.4269/ajtmh.17-0845
  • Willie N, Zimmerman PA, Mehlotra RK. Plasmodium falciparum histidine-rich protein 2 gene variation in a malaria-endemic area of Papua New Guinea. Am J Trop Med Hyg. 2018;99(3):697–703. doi: 10.4269/ajtmh.18-0137
  • Dong Y, Liu S, Deng Y, et al. Genetic polymorphism of histidine rich protein 2 in Plasmodium falciparum isolates from different infection sources in Yunnan Province, China. Malar J 2019;18:446. doi: 10.1186/s12936-019-3084-4
  • Fontecha G, Pinto A, Escobar D, et al. Genetic variability of Plasmodium falciparum histidine-rich proteins 2 and 3 in Central America. Malar J. 2019;18:31. doi: 10.1186/s12936-019-2668-3
  • Funwei R, Nderu D, Nguetse CN, et al. Molecular surveillance of pfhrp2 and pfhrp3 genes deletion in Plasmodium falciparum isolates and the implications for rapid diagnostic tests in Nigeria. Acta Trop. 2019;196:121–125. doi: 10.1016/j.actatropica.2019.05.016
  • Mussa A, Talib M, Mohamed Z, et al. Genetic diversity of Plasmodium falciparum histidine‑rich protein 2 (PfHRP2) and its effect on the performance of PfHRP2‑based rapid diagnostic tests. BMC Res Notes. 2019;12(1):334. doi: 10.1186/s13104-019-4361-6
  • Nderu D, Kimani F, Thiong’o K, et al. Plasmodium falciparum histidine-rich protein (PfHRP2 and 3) diversity in Western and Coastal Kenya. Sci Rep. 2019;9(1):1709. doi: 10.1038/s41598-018-38175-1
  • Addai-Mensah O, Dinko B, Noagbe M, et al. Plasmodium falciparum histidine-rich protein 2 diversity in Ghana. Malar J 2020;19:256. doi: 10.1186/s12936-020-03328-z
  • Lê HG, Kang J-M, Lee J, et al. Genetic variations in histidine-rich protein 2 and histidine-rich protein 3 of Myanmar Plasmodium falciparum isolates. Malar J. 2020;19(1):388. doi: 10.1186/s12936-020-03456-6
  • Pasquier G, Azoury V, Sasso M, et al. Rapid diagnostic tests failing to detect infections by Plasmodium falciparum encoding pfhrp2 and pfhrp3 genes in a non-endemic setting Malar J. 2020;19:179. doi: 10.1186/s12936-020-03251-3
  • Alemayehu GS, Messele A, Blackburn K, et al. Genetic variation of Plasmodium falciparum histidine-rich protein 2 and 3 in Assosa zone, Ethiopia: its impact on the performance of malaria rapid diagnostic tests. Malar J. 2021;20(1):394. doi: 10.1186/s12936-021-03928-3
  • Bosco AB, Anderson K, Gresty K, et al. Genetic diversity and genetic relatedness in Plasmodium falciparum parasite population in individuals with uncomplicated malaria based on microsatellite typing in Eastern and Western regions of Uganda, 2019–2020. Malar J. 2021;20(1):242. doi: 10.1186/s12936-021-03763-6
  • Costa GL, Mascarenhas MEP, Martin TOG, et al. A comprehensive analysis of the genetic diversity of Plasmodium falciparum histidine-rich protein 2 (PfHRP2) in the Brazilian Amazon. Front Cell Infect Microbiol. 2021;11:742681. doi: 10.3389/fcimb.2021.742681
  • Kumari MS, Sharma S, Bhardwaj N, et al. Pfhrp2/3 gene deletion and genetic variation in PfHRP2-based RDTs with P. falciparum positive samples from India and its implication on malaria control. Infect Genet Evol. 2022;99:105232. doi: 10.1016/j.meegid.2022.105232
  • Bredu DG, Ahadzi GK, Donu D, et al. Nationwide surveillance of Pfhrp2 exon 2 diversity in Plasmodium falciparum circulating in symptomatic malaria patients living in Ghana. Am J Trop Med Hyg. 2022;106(6):1660–1666. doi: 10.4269/ajtmh.21-1342
  • de la Fuente I M, Yimar M, García L, et al. Deletion patterns, genetic variability and protein structure of pfhrp2 and pfhrp3: implications for malaria rapid diagnostic test in Amhara region, Ethiopia. Malar J. 2022;21(1):287. Available from. doi: 10.1186/s12936-022-04306-3
  • Kaaya RD, Amour C, Matowo JJ, et al. Genetic sequence variation in the Plasmodium falciparum histidine-rich protein 2 gene from field isolates in Tanzania: impact on malaria rapid diagnosis. Genes. 2022;13(9):1642. doi: 10.3390/genes13091642
  • Duah-Quashie NO, Opoku-Agyeman P, Bruku S, et al. Genetic deletions and high diversity of Plasmodium falciparum histidine-rich proteins 2 and 3 genes in parasite populations in Ghana. Front Epidemiol. 2022;2:1011938. doi: 10.3389/fepid.2022.1011938
  • Thang ND, Vallbona ER, Thi N, et al. Surveillance of pfhrp2 and pfhrp3 gene deletions among symptomatic Plasmodium falciparum malaria patients in central Vietnam. Malar J. 2022;21(1):371. Available from. doi: 10.1186/s12936-022-04399-w
  • Alemayehu GS, Blackburn K, Lopez K, et al. Detection of high prevalence of Plasmodium falciparum histidine-rich protein 2/3 gene deletions in Assosa zone, Ethiopia: implication for malaria diagnosis. Malar J 2021;20:109. doi: 10.1186/s12936-021-03629-x
  • Volkman SK, Hartl DL, Wirth DF, et al. Excess polymorphisms in genes for membrane proteins in Plasmodium falciparum. Science. 2002;298(5591):216–218. doi: 10.1126/science.1075642
  • WHO. World malaria report. World Health Organization. Geneva: 2020. https://www.who.int/publications/i/item/9789240015791
  • Babiker HA, Lines J, Hill WG, et al. Population structure of Plasmodium falciparum in villages with different malaria endemicity in East Africa. Am J Trop Med Hyg. 1997;56(2):141–147. doi: 10.4269/ajtmh.1997.56.141
  • Jejaw Zeleke A, Hailu A, Bayih AG, et al. Plasmodium falciparum histidine-rich protein 2 and 3 genes deletion in global settings (2010–2021): a systematic review and meta-analysis. Malar J. 2022;21(1):26 doi: 10.1186/s12936-022-04051-7

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.