Histidine-rich protein (hrp) 2-based RDT false-negatives and Plasmodium falciparum hrp 2 and 3 gene deletions in low, seasonal and intense perennial transmission zones in Cameroon: a cross - sectional study.


Journal

BMC infectious diseases
ISSN: 1471-2334
Titre abrégé: BMC Infect Dis
Pays: England
ID NLM: 100968551

Informations de publication

Date de publication:
30 Sep 2024
Historique:
received: 21 06 2024
accepted: 16 09 2024
medline: 1 10 2024
pubmed: 1 10 2024
entrez: 30 9 2024
Statut: epublish

Résumé

False negative rapid diagnostic tests (RDTs) accruing to the non-detection of Plasmodium falciparum histidine-rich protein 2/3 (Pfhrp2/3) is threatening the diagnosis and management of malaria. Although regular monitoring is necessary to gauge the level of efficacy of the tool, studies in Cameroon remain limited. This study assessed Plasmodium spp. prevalence and Pfhrp2/3 gene deletions across ecological and transmission zones in Cameroon. This is a cross-sectional, multi-site, community- and hospital- based study, in 21 health facilities and 14 communities covering all five ecological settings in low seasonal (LS) and intense perennial (IPT) malaria transmission zones between 2019 and 2021. Participants were screened for malaria parasite using Pfhrp2 RDT and light microscopic examination of thick peripheral blood smears. DNA was extracted from dried blood spot using chelex A total of 3,373 participants enrolled, 1,786 Plasmodium spp. infected, with 77.4% P. falciparum. Discordant RDT and qPCR results (False negatives) were reported in 191 (15.7%) P. falciparum mono-infected samples from LS (29%, 42) and IPT (13.9%, 149). The Pfhrp2+/Pfhrp3 + genotype was most frequent, similar between LS (5.5%, 8/145) and IPT (6.0%, 65/1,076). Single Pfhrp2 and Pfhrp3 gene deletions occurred in LS (0.7%, 1/145 each) and IPT (3.6%, 39/1,076 vs. 2.9%, 31/1,076), respectively. Whilst a single sample harboured Pfhrp2-/Pfhrp3- genotype in LS, 2.4% (26/1,076) were double deleted at IPT. Pfhrp2+/Pfhrp3- (0.3%, 3/1,076) and Pfhrp2-/Pfhrp3+ (1.2%, 13/1,076) genotypes were only observed in IPT. Pfhrp2, Pfhrp3 deletions and Pfhrp2-/Pfhrp3- genotype accounted for 78.8% (26), 69.7% (23) and 63.6% (21) RDT false negatives, respectively. Plasmodium falciparum remains the most dominant and widely distributed Plasmodium species across transmission and ecological zones in Cameroon. Although the low prevalence of Pfhrp2/3 gene deletions supports the continued use of HRP2-based RDTs for routine malaria diagnosis, the high proportion of false-negatives due to gene deleted parasites necessitates continued surveillance to inform control and elimination efforts.

Sections du résumé

BACKGROUND BACKGROUND
False negative rapid diagnostic tests (RDTs) accruing to the non-detection of Plasmodium falciparum histidine-rich protein 2/3 (Pfhrp2/3) is threatening the diagnosis and management of malaria. Although regular monitoring is necessary to gauge the level of efficacy of the tool, studies in Cameroon remain limited. This study assessed Plasmodium spp. prevalence and Pfhrp2/3 gene deletions across ecological and transmission zones in Cameroon.
METHODS METHODS
This is a cross-sectional, multi-site, community- and hospital- based study, in 21 health facilities and 14 communities covering all five ecological settings in low seasonal (LS) and intense perennial (IPT) malaria transmission zones between 2019 and 2021. Participants were screened for malaria parasite using Pfhrp2 RDT and light microscopic examination of thick peripheral blood smears. DNA was extracted from dried blood spot using chelex
RESULTS RESULTS
A total of 3,373 participants enrolled, 1,786 Plasmodium spp. infected, with 77.4% P. falciparum. Discordant RDT and qPCR results (False negatives) were reported in 191 (15.7%) P. falciparum mono-infected samples from LS (29%, 42) and IPT (13.9%, 149). The Pfhrp2+/Pfhrp3 + genotype was most frequent, similar between LS (5.5%, 8/145) and IPT (6.0%, 65/1,076). Single Pfhrp2 and Pfhrp3 gene deletions occurred in LS (0.7%, 1/145 each) and IPT (3.6%, 39/1,076 vs. 2.9%, 31/1,076), respectively. Whilst a single sample harboured Pfhrp2-/Pfhrp3- genotype in LS, 2.4% (26/1,076) were double deleted at IPT. Pfhrp2+/Pfhrp3- (0.3%, 3/1,076) and Pfhrp2-/Pfhrp3+ (1.2%, 13/1,076) genotypes were only observed in IPT. Pfhrp2, Pfhrp3 deletions and Pfhrp2-/Pfhrp3- genotype accounted for 78.8% (26), 69.7% (23) and 63.6% (21) RDT false negatives, respectively.
CONCLUSION CONCLUSIONS
Plasmodium falciparum remains the most dominant and widely distributed Plasmodium species across transmission and ecological zones in Cameroon. Although the low prevalence of Pfhrp2/3 gene deletions supports the continued use of HRP2-based RDTs for routine malaria diagnosis, the high proportion of false-negatives due to gene deleted parasites necessitates continued surveillance to inform control and elimination efforts.

Identifiants

pubmed: 39350071
doi: 10.1186/s12879-024-09935-4
pii: 10.1186/s12879-024-09935-4
doi:

Substances chimiques

Protozoan Proteins 0
Antigens, Protozoan 0
HRP-2 antigen, Plasmodium falciparum 0
HRP3 protein, Plasmodium falciparum 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1080

Subventions

Organisme : H3Africa
ID : H3AFull/17/008
Organisme : H3Africa
ID : H3AFull/17/008
Organisme : DELTAS Africa Initiative
ID : 107740/Z/15/Z

Informations de copyright

© 2024. The Author(s).

Références

World Health Organization. World malaria report 2019. Geneva: World Health Organization. 2019 [cited 2024 Mar 21]. https://iris.who.int/handle/10665/330011
By-Nc-Sa C. World malaria report 2023.
Gallup J, Sachs J. The economic burden of malaria. Am J Trop Med Hyg. 2001;64:85–96.
pubmed: 11425181 doi: 10.4269/ajtmh.2001.64.85
Wang S-J, Lengeler C, Smith TA, Vounatsou P, Cissé G, Diallo DA, et al. Rapid urban malaria appraisal (RUMA) in sub-Saharan Africa. Malar J. 2005;4:40.
pubmed: 16153298 pmcid: 1249588 doi: 10.1186/1475-2875-4-40
Ndo C, Menze-Djantio B, Antonio-Nkondjio C. Awareness, attitudes and prevention of malaria in the cities of Douala and Yaoundé (Cameroon). Parasites Vectors. 2011;4:181.
pubmed: 21933411 pmcid: 3192766 doi: 10.1186/1756-3305-4-181
World malaria. Report 2020 20 years of global progress and challenges. Geneva: World Health Organization; 2020.
Antonio-Nkondjio C, Ndo C, Njiokou F, Bigoga JD, Awono-Ambene P, Etang J, et al. Review of malaria situation in Cameroon: technical viewpoint on challenges and prospects for disease elimination. Parasites Vectors. 2019;12:501.
pubmed: 31655608 pmcid: 6815446 doi: 10.1186/s13071-019-3753-8
Fru-Cho J, Bumah VV, Safeukui I, Nkuo-Akenji T, Titanji VP, Haldar K. Molecular typing reveals substantial Plasmodium vivax infection in asymptomatic adults in a rural area of Cameroon. Malar J. 2014;13:170.
pubmed: 24886496 pmcid: 4032583 doi: 10.1186/1475-2875-13-170
The world health report. 2000: Health systems: improving performance. 2000.
World Health Organization. Global malaria programme. Guidelines for the treatment of malaria. 2015.
Haditsch M. Quality and reliability of current malaria diagnostic methods. Travel Med Infect Dis. 2004;2(3–4):149–60.
pubmed: 17291976 doi: 10.1016/j.tmaid.2004.03.001
World Health Organization. Malaria microscopy quality assurance manual. Version 2. Geneva: World Health Organization; 2016.
Wilson ML. Laboratory diagnosis of malaria: conventional and rapid diagnostic methods. Arch Pathol Lab Med. 2013;137(6):805–11.
pubmed: 23721276 doi: 10.5858/arpa.2011-0602-RA
World Health Organization. World Health Organization, Global Malaria Programme. Universal access to malaria diagnostic testing: an operational manual. Geneva: World Health Organization; 2011.
Cheng Q, Gatton ML, Barnwell J, Chiodini P, McCarthy J, Bell D, et al. Plasmodium falciparum parasites lacking histidine-rich protein 2 and 3: a review and recommendations for accurate reporting. Malar J. 2014;13:283.
pubmed: 25052298 pmcid: 4115471 doi: 10.1186/1475-2875-13-283
World Health Organization. False-negative RDT results and P. Falciparum histidine-rich protein 2/3 gene deletions. WHO. 2019;10(1):12.
Akinyi S, Hayden T, Gamboa D, Torres K, Bendezu J, Abdallah JF, et al. Multiple genetic origins of histidine-rich protein 2 gene deletion in Plasmodium falciparum parasites from Peru. Sci Rep. 2013;3:2797.
pubmed: 24077522 pmcid: 3786299 doi: 10.1038/srep02797
Lee N, Baker J, Andrews KT, Gatton ML, Bell D, Cheng Q, 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):2773–8.
pubmed: 16891491 pmcid: 1594627 doi: 10.1128/JCM.02557-05
Gamboa D, Ho M-F, Bendezu J, Torres K, Chiodini PL, Barnwell JW, 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.
pubmed: 20111602 pmcid: 2810332 doi: 10.1371/journal.pone.0008091
Gatton ML, Ciketic S, Barnwell JW, Cheng Q, Chiodini PL, Incardona S et al. An assessment of false positive rates for malaria rapid diagnostic tests caused by non-Plasmodium infectious agents and immunological factors. PLoS One. 2018.13(5):e0197395.
Hosch S, Yoboue CA, Donfack OT, Guirou EA, Dangy JP, Mpina M, et al. Analysis of nucleic acids extracted from rapid diagnostic tests reveals a significant proportion of false positive test results associated with recent malaria treatment. Malar J. 2022;21:2.
doi: 10.1186/s12936-022-04043-7
Watson OJ, Sumner KM, Janko M, Goel V, Winskill P, Slater HC, et al. False-negative malaria rapid diagnostic test results and their impact on community-based malaria surveys in sub-saharan Africa. BMJ Glob Health. 2019;4:e001582.
pubmed: 31406591 pmcid: 6666813 doi: 10.1136/bmjgh-2019-001582
Baker J, Ho M-F, Pelecanos A, Gatton M, Chen N, Abdullah S 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;9:129.
Gupta H, Matambisso G, Galatas B, Cisteró P, Nhamussua L, Simone W, et al. Molecular surveillance of pfhrp2 and pfhrp3 deletions in Plasmodium falciparum isolates from Mozambique. Malar J. 2017;16:416.
pubmed: 29037193 pmcid: 5644146 doi: 10.1186/s12936-017-2061-z
Fontecha G, Mejía RE, Banegas E, Ade MP, Mendoza L, Ortiz B, et al. Deletions of pfhrp2 and pfhrp3 genes of Plasmodium falciparum from Honduras, Guatemala and Nicaragua. Malar J. 2018;17:320.
pubmed: 30170596 pmcid: 6119307 doi: 10.1186/s12936-018-2470-7
Rachid Viana GM, Akinyi Okoth S, Silva-Flannery L, Lima Barbosa DR, Macedo De Oliveira A, Goldman IF et al. Histidine-rich protein 2 (pfhrp2) and pfhrp3 gene deletions in Plasmodium falciparum isolates from select sites in Brazil and Bolivia. Gatton ML, editor. PLoS ONE. 2017;12:e0171150.
Gendrot M, Fawaz R, Dormoi J, Madamet M, Pradines B. 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;25:580–5.
pubmed: 30267926 doi: 10.1016/j.cmi.2018.09.009
Berzosa P, González V, Taravillo L, Mayor A, Romay-Barja M, García L, et al. First evidence of the deletion in the pfhrp2 and pfhrp3 genes in Plasmodium falciparum from Equatorial Guinea. Malar J. 2020;19:99.
pubmed: 32122352 pmcid: 7050119 doi: 10.1186/s12936-020-03178-9
Eyong EM, Etutu SJM, Jerome F-C, Nyasa RB, Kwenti TE, Moyeh MN. Plasmodium Falciparum histidine-rich protein 2 and 3 gene deletion in the Mount Cameroon region. IJID Reg. 2022;3:300–7.
pubmed: 35755467 pmcid: 9216387 doi: 10.1016/j.ijregi.2022.05.006
Foko LPK, Moukoko CEE, Jakhan J, Narang G, Hawadak J, Motse FDK, et al. Deletions of histidine-rich protein 2/3 genes in natural Plasmodium falciparum populations from Cameroon and India: role of asymptomatic and submicroscopic infections. Am J Trop Med Hyg. 2024;110(6):1100–9.
doi: 10.4269/ajtmh.23-0896
Nana RRD, Ngum NL, Makoge V, Amvongo-Adja N, Hawadak J, Singh V. Rapid diagnostic tests for malaria diagnosis in Cameroon: impact of histidine rich protein 2/3 deletions and lactate dehydrogenase gene polymorphism. Diagn Microbiol Infect Dis. 2024;108:1116103.
doi: 10.1016/j.diagmicrobio.2023.116103
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;19:46.
pubmed: 31992330 pmcid: 6986054 doi: 10.1186/s12936-019-3090-6
Prosser C, Gresty K, Ellis J, Meyer W, Anderson K, Lee R, et al. Plasmodium Falciparum histidine-rich protein 2 and 3 gene deletions in strains from Nigeria, Sudan, and South Sudan. Emerg Infect Dis. 2021;27:471–9.
pubmed: 33496220 pmcid: 7853540 doi: 10.3201/eid2702.191410
Beck HE, Zimmermann NE, McVicar TR, Vergopolan N, Berg A, Wood EF. Present and future Köppen-Geiger climate classification maps at 1-km resolution. Sci Data. 2018;5:180214.
pubmed: 30375988 pmcid: 6207062 doi: 10.1038/sdata.2018.214
Tangi LN, Ajonina MU, Moyeh MN, Chi HF, Ntui VN, Kwi PN, et al. Knowledge, attitude, and adherence to malaria control guidelines and the prevalence of Plasmodium species infection in localities across transmission and ecological zones in Cameroon. Front Public Health. 2023;11:1060479.
pubmed: 37181692 pmcid: 10173414 doi: 10.3389/fpubh.2023.1060479
Mbenda HGN, Awasthi G, Singh PK, Gouado I, Das A. Does malaria epidemiology project Cameroon as ‘Africa in miniature’? J Biosci. 2014;39:727–38.
pubmed: 25116627 doi: 10.1007/s12038-014-9451-y
Cheesbrough M. District laboratory practice in tropical countries. 2nd ed. Leiden: Cambridge University Press; 2006.
doi: 10.1017/CBO9780511543470
Apinjoh TO, Ntui VN, Chi HF, Moyeh MN, Toussi CT, Mayaba JM et al. Intermittent preventive treatment with sulphadoxine-pyrimethamine (IPTp-SP) is associated with protection against sub-microscopic P. falciparum infection in pregnant women during the low transmission dry season in southwestern Cameroon: a semi - longitudinal study. PLoS ONE. 2022;18.
Simon N, Shallat J, Williams Wietzikoski C, Harrington WE. Optimization of Chelex 100 resin-based extraction of genomic DNA from dried blood spots. Biology Methods Protocols. 2020;5:bpaa009.
pubmed: 32665976 pmcid: 7334876 doi: 10.1093/biomethods/bpaa009
Hofmann N, Mwingira F, Shekalaghe S, Robinson LJ, Mueller I, Felger I. Ultra-sensitive detection of Plasmodium falciparum by amplification of multi-copy subtelomeric targets. L Von Seidlein editor. PLoS Med. 2015;12:e1001788.
Daniels RF, Deme AB, Gomis JF, Dieye B, Durfee K, Thwing JI, et al. Evidence of non-plasmodium falciparum malaria infection in Kédougou, Sénégal. Malar J. 2017;16:9.
pubmed: 28049489 pmcid: 5209815 doi: 10.1186/s12936-016-1661-3
Baker J, McCarthy J, Gatton M, Kyle DE, Belizario V, Luchavez J, et al. Genetic diversity of Plasmodium falciparum histidine-rich protein 2 (PfHRP2) and its effect on the performance of PfHRP2-based. Rapid Diagnostic Tests; 2005.
Alemayehu GS, Blackburn K, Lopez K, Cambel Dieng C, Lo E, Janies D, 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.
pubmed: 33622309 pmcid: 8095343 doi: 10.1186/s12936-021-03629-x
Ali IM, Bigoga JD, Forsah DA, Cho-Ngwa F, Tchinda V, Moor VA, et al. Field evaluation of the 22 rapid diagnostic tests for community management of malaria with artemisinin combination therapy in Cameroon. Malar J. 2016;15:31.
pubmed: 26791422 pmcid: 4721050 doi: 10.1186/s12936-016-1085-0
Bamou R, Nematchoua-Weyou Z, Lontsi-Demano M, Ningahi LG, Tchoumbou MA, Defo-Talom BA, et al. Performance assessment of a widely used rapid diagnostic test CareStart
pubmed: 33665437 pmcid: 7897993 doi: 10.1016/j.heliyon.2021.e06271
By-Nc-Sa C. World malaria report 2022. 2022.
Berhane A, Anderson K, Mihreteab S, Gresty K, Rogier E, Mohamed S, et al. Major threat to malaria control programs by Plasmodium falciparum lacking histidine-rich protein 2, Eritrea. Emerg Infect Dis. 2018;24:462–70.
pubmed: 29460730 pmcid: 5823352 doi: 10.3201/eid2403.171723
Kong A, Wilson SA, Ah Y, Nace D, Rogier E, Aidoo M. 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.
pubmed: 33926477 pmcid: 8086288 doi: 10.1186/s12936-021-03739-6
Poti KE, Sullivan DJ, Dondorp AM, Woodrow CJ. HRP2: transforming malaria diagnosis, but with caveats. Trends Parasitol. 2020;36:112–26.
pubmed: 31848119 doi: 10.1016/j.pt.2019.12.004
Lee N, Gatton ML, Pelecanos A, Bubb M, Gonzalez I, Bell D, et al. Identification of optimal epitopes for Plasmodium falciparum rapid diagnostic tests that target histidine-rich proteins 2 and 3. J Clin Microbiol. 2012;50:1397–405.
pubmed: 22259210 pmcid: 3318543 doi: 10.1128/JCM.06533-11
Feufack-Donfack LB, Sarah-Matio EM, Abate LM, Bouopda Tuedom AG, Ngano Bayibéki A, Maffo Ngou C, et al. Epidemiological and entomological studies of malaria transmission in Tibati, Adamawa region of Cameroon 6 years following the introduction of long-lasting insecticide nets. Parasites Vectors. 2021;14:247.
pubmed: 33964974 pmcid: 8106832 doi: 10.1186/s13071-021-04745-y
Nguiffo-Nguete D, Nongley Nkemngo F, Ndo C, Agbor J-P, Boussougou-Sambe ST, Salako Djogbénou L, et al. Plasmodium malariae contributes to high levels of malaria transmission in a forest–savannah transition area in Cameroon. Parasites Vectors. 2023;16:31.
pubmed: 36698132 pmcid: 9875470 doi: 10.1186/s13071-022-05635-7
Sundararaman SA, Liu W, Keele BF, Learn GH, Bittinger K, Mouacha F, et al. Plasmodium falciparum -like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria. Proc Natl Acad Sci USA. 2013;110:7020–5.
pubmed: 23569255 pmcid: 3637760 doi: 10.1073/pnas.1305201110
Djeunang Dongho GB, Gunalan K, L’Episcopia M, Paganotti GM, Menegon M, Sangong RE et al. Plasmodium vivax infections detected in a large number of febrile Duffy-Negative Africans in Dschang, Cameroon. The American Journal of Tropical Medicine and Hygiene. 2022 [cited 2024 Mar 21]; https://doi.org/10.4269/ajtmh.20-1255
Ngassa Mbenda HG, Das A. Occurrence of multiple chloroquine-resistant pfcrt haplotypes and emergence of the S(agt)VMNT type in Cameroonian Plasmodium falciparum. J Antimicrob Chemother. 2014;69:400–3.
pubmed: 24092656 doi: 10.1093/jac/dkt388
McCaffery JN, Nace D, Herman C, Singh B, Sompwe EM, Nkoli PM, et al. Plasmodium Falciparum pfhrp2 and pfhrp3 gene deletions among patients in the DRC enrolled from 2017 to 2018. Sci Rep. 2021;11:22979.
pubmed: 34837020 pmcid: 8626453 doi: 10.1038/s41598-021-02452-3
Lynch E, Jensen TO, Assao B, Chihana M, Turuho T, Nyehangane D, et al. Evaluation of HRP2 and pLDH-based rapid diagnostic tests for malaria and prevalence of pfhrp2/3 deletions in Aweil, South Sudan. Malar J. 2022;21:261.
pubmed: 36085071 pmcid: 9461093 doi: 10.1186/s12936-022-04280-w
Mihreteab S, Anderson K, Pasay C, Smith D, Gatton ML, Cunningham J, 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;11:21082.
pubmed: 34702923 pmcid: 8548324 doi: 10.1038/s41598-021-00714-8
Parr JB, Anderson O, Juliano JJ, Meshnick SR, Streamlined. PCR-based testing for pfhrp2- and pfhrp3-negative Plasmodium falciparum. Malar J. 2018;17:137.
pubmed: 29609602 pmcid: 5879555 doi: 10.1186/s12936-018-2287-4
Kaaya RD, Kavishe RA, Tenu FF, Matowo JJ, Mosha FW, Drakeley C, et al. Deletions of the Plasmodium falciparum histidine-rich protein 2/3 genes are common in field isolates from north-eastern Tanzania. Sci Rep. 2022;12:5802.
pubmed: 35388127 pmcid: 8987040 doi: 10.1038/s41598-022-09878-3
Leonard CM, Assefa A, McCaffery JN, Herman C, Plucinski M, Sime H, et al. Investigation of Plasmodium falciparum pfhrp2 and pfhrp3 gene deletions and performance of a rapid diagnostic test for identifying asymptomatic malaria infection in northern Ethiopia, 2015. Malar J. 2022;21:70.
pubmed: 35246151 pmcid: 8895513 doi: 10.1186/s12936-022-04097-7
Watson OJ, Slater HC, Verity R, Parr JB, Mwandagalirwa MK, Tshefu A, et al. Modelling the drivers of the spread of Plasmodium falciparum hrp2 gene deletions in sub-Saharan Africa. eLife. 2017;6:e25008.
pubmed: 28837020 pmcid: 5602420 doi: 10.7554/eLife.25008
Rogier E, McCaffery JN, Nace D, Svigel SS, Assefa A, Hwang J, et al. Plasmodium Falciparum pfhrp2 and pfhrp3 gene deletions from persons with symptomatic malaria infection in Ethiopia, Kenya, Madagascar, and Rwanda. Emerg Infect Dis. 2022;28:608–16.
pubmed: 35201739 pmcid: 8888236 doi: 10.3201/eid2803.211499
Houzé S, Boly MD, Le Bras J, Deloron P, Faucher J-F. Pf HRP2 and pf LDH antigen detection for monitoring the efficacy of artemisinin-based combination therapy (ACT) in the treatment of uncomplicated falciparum malaria. Malar J. 2009;8:211.
pubmed: 19735557 pmcid: 2754493 doi: 10.1186/1475-2875-8-211
Grignard L, Nolder D, Sepúlveda N, Berhane A, Mihreteab S, Kaaya R, et al. 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. 2020;55:102757.
pubmed: 32403083 pmcid: 7218259 doi: 10.1016/j.ebiom.2020.102757
Apinjoh TO, Ouattara A, Titanji VPK, Djimde A, Amambua-Ngwa A. Genetic diversity and drug resistance surveillance of Plasmodium falciparum for malaria elimination: is there an ideal tool for resource-limited sub-saharan Africa? Malar J. 2019;18:217.
pubmed: 31242921 pmcid: 6595576 doi: 10.1186/s12936-019-2844-5
Nolder D, Stewart L, Tucker J, Ibrahim A, Gray A, Corrah T, et al. 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. 2021;108:137–44.
pubmed: 33991679 pmcid: 8295040 doi: 10.1016/j.ijid.2021.05.008
Thang ND, Rovira-Vallbona E, Binh NTH, Dung DV, Ngoc NTH, Long TK, et al. Surveillance of pfhrp2 and pfhrp3 gene deletions among symptomatic Plasmodium falciparum malaria patients in Central Vietnam. Malar J. 2022;21:371.
pubmed: 36471315 pmcid: 9724378 doi: 10.1186/s12936-022-04399-w
Kaaya RD, Matowo J, Kajeguka D, Tenu F, Shirima B, Mosha F, et al. The impact of submicroscopic parasitemia on malaria rapid diagnosis in Northeastern Tanzania, an area with diverse transmission patterns. Infect Disease Rep. 2022;14:798–809.
doi: 10.3390/idr14060082
Markwalter CF, Mudenda L, Leelawong M, Kimmel DW, Nourani A, Mbambara S, et al. Evidence for histidine-rich protein 2 immune complex formation in symptomatic patients in Southern Zambia. Malar J. 2018;17:256.
pubmed: 29986725 pmcid: 6038308 doi: 10.1186/s12936-018-2400-8

Auteurs

Tobias Obejum Apinjoh (TO)

Department of Biochemistry and Molecular Biology, University of Buea, Buea, Cameroon. apinjoh.tobias@ubuea.cm.
Department of Chemical and Biological Engineering, The University of Bamenda, Bambili, Cameroon. apinjoh.tobias@ubuea.cm.
Medical Research Council Unit, The Gambia at London School of Hygiene and Tropical Medicine, Fajara, The Gambia. apinjoh.tobias@ubuea.cm.

Livinus Ngu Tangi (LN)

Medical Research Council Unit, The Gambia at London School of Hygiene and Tropical Medicine, Fajara, The Gambia.
Department of Microbiology and Parasitology, University of Buea, Buea, Cameroon.

Eniyou Cheryll Oriero (EC)

Medical Research Council Unit, The Gambia at London School of Hygiene and Tropical Medicine, Fajara, The Gambia.

Sainabou Drammeh (S)

Medical Research Council Unit, The Gambia at London School of Hygiene and Tropical Medicine, Fajara, The Gambia.

Vincent Ntui Ntui-Njock (VN)

Department of Biochemistry and Molecular Biology, University of Buea, Buea, Cameroon.

Blessed Etoketim (B)

Medical Research Council Unit, The Gambia at London School of Hygiene and Tropical Medicine, Fajara, The Gambia.

Hanesh Fru Chi (HF)

Department of Microbiology and Parasitology, University of Buea, Buea, Cameroon.

Pilate Nkineh Kwi (PN)

Department of Biochemistry and Molecular Biology, University of Buea, Buea, Cameroon.

Bekai Njie (B)

Medical Research Council Unit, The Gambia at London School of Hygiene and Tropical Medicine, Fajara, The Gambia.

Mary Aigbiremo Oboh (MA)

Medical Research Council Unit, The Gambia at London School of Hygiene and Tropical Medicine, Fajara, The Gambia.

Eric Akum Achidi (EA)

Department of Biochemistry and Molecular Biology, University of Buea, Buea, Cameroon.

Alfred Amambua-Ngwa (A)

Medical Research Council Unit, The Gambia at London School of Hygiene and Tropical Medicine, Fajara, The Gambia. alfngwa@lshtm.ac.uk.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH