Skip to main content
Top
Published in: Malaria Journal 1/2021

Open Access 01-12-2021 | Plasmodium Falciparum | Research

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

Authors: Bosco B. Agaba, Karen Anderson, Karryn Gresty, Christiane Prosser, David Smith, Joaniter I. Nankabirwa, Sam Nsobya, Adoke Yeka, Rhoda Namubiru, Emmanuel Arinaitwe, Paul Mbaka, John Kissa, Chae Seung Lim, Charles Karamagi, Joan K. Nakayaga, Moses R. Kamya, Qin Cheng

Published in: Malaria Journal | Issue 1/2021

Login to get access

Abstract

Background

Genetic diversity and parasite relatedness are essential parameters for assessing impact of interventions and understanding transmission dynamics of malaria parasites, however data on its status in Plasmodium falciparum populations in Uganda is limited. Microsatellite markers and DNA sequencing were used to determine diversity and molecular characterization of P. falciparum parasite populations in Uganda.

Methods

A total of 147 P. falciparum genomic DNA samples collected from cross-sectional surveys in symptomatic individuals of 2–10 years were characterized by genotyping of seven highly polymorphic neutral microsatellite markers (n = 85) and genetic sequencing of the Histidine Rich Protein 2 (pfhrp2) gene (n = 62). ArcGIS was used to map the geographical distribution of isolates while statistical testing was done using Student's t-test or Wilcoxon's rank-sum test and Fisher’s exact test as appropriate at P ≤ 0.05.

Results

Overall, 75.5% (95% CI 61.1–85.8) and 24.5% (95% CI14.2–38.9) of parasites examined were of multiclonal (mixed genotype) and single clone infections, respectively. Multiclonal infections occurred more frequently in the Eastern region 73.7% (95% CI 48.8–89.1), P < 0.05. Overall, multiplicity of infection (MOI) was 1.9 (95% CI 1.7–2.1), P = 0.01 that was similar between age groups (1.8 vs 1.9), P = 0.60 and regions (1.9 vs 1.8), P = 0.43 for the < 5 and ≥ 5 years and Eastern and Western regions, respectively. Genomic sequencing of the pfhrp2 exon2 revealed a high level of genetic diversity reflected in 96.8% (60/62) unique sequence types. Repeat type AHHAAAHHATD and HRP2 sequence Type C were more frequent in RDT−/PCR + samples (1.9% vs 1.5%) and (13% vs 8%), P < 0.05 respectively. Genetic relatedness analysis revealed small clusters of gene deleted parasites in Uganda, but no clustering with Eritrean parasites.

Conclusion

High level of genetic diversity of P. falciparum parasites reflected in the frequency of multiclonal infections, multiplicity of infection and variability of the pfhrp2 gene observed in this study is consistent with the high malaria transmission intensity in these settings. Parasite genetic analysis suggested spontaneous emergence and clonal expansion of pfhrp2 deleted parasites that require close monitoring to inform national malaria diagnosis and case management policies.
Appendix
Available only for authorised users
Literature
2.
go back to reference WHO. World Malaria Report 2020. Geneva. World Health Organization. WHO. World Malaria Report 2020. Geneva. World Health Organization.
4.
go back to reference DHIS2. Routine District Health Information System, Uganda. 2020. DHIS2. Routine District Health Information System, Uganda. 2020.
7.
go back to reference NMCP. Uganda Malaria strategic Plan Midterm Review. Kampala, 2017. NMCP. Uganda Malaria strategic Plan Midterm Review. Kampala, 2017.
8.
go back to reference NMCP. Uganda National Malaria Indicator Survey. Kampala, 2014. NMCP. Uganda National Malaria Indicator Survey. Kampala, 2014.
9.
go back to reference Uganda Ministry of Health. District Health Information System (DHIS2). Kampala, 2019. Uganda Ministry of Health. District Health Information System (DHIS2). Kampala, 2019.
13.
go back to reference NMCP. National Malaria Control and Elimination strategic Plan. Kampala, 2020. NMCP. National Malaria Control and Elimination strategic Plan. Kampala, 2020.
14.
go back to reference NMCP. Uganda Malaria Program Review (MPR) Report. Kampala, 2019. NMCP. Uganda Malaria Program Review (MPR) Report. Kampala, 2019.
15.
go back to reference Zhong D, Koepfli C, Cui L, Yan G. Molecular approaches to determine the multiplicity of Plasmodium infections. Malar J. 2018;17:172.CrossRef Zhong D, Koepfli C, Cui L, Yan G. Molecular approaches to determine the multiplicity of Plasmodium infections. Malar J. 2018;17:172.CrossRef
16.
go back to reference 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. J Infect Dis. 2005;192:870–7.CrossRef 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. J Infect Dis. 2005;192:870–7.CrossRef
17.
go back to reference Deme AB, Park DJ, Bei AK, Sarr O, Badiane AS, Gueye PEHO, et al. Analysis of pfhrp2 genetic diversity in Senegal and implications for use of rapid diagnostic tests. Malar J. 2014;13:34.CrossRef Deme AB, Park DJ, Bei AK, Sarr O, Badiane AS, Gueye PEHO, et al. Analysis of pfhrp2 genetic diversity in Senegal and implications for use of rapid diagnostic tests. Malar J. 2014;13:34.CrossRef
18.
go back to reference Kumar N, Singh JP, Pande V, Mishra N, Srivastava B, Kapoor R, 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;11:298.CrossRef Kumar N, Singh JP, Pande V, Mishra N, Srivastava B, Kapoor R, 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;11:298.CrossRef
19.
go back to reference Rock EP, Marsh K, Saul AJ, Wellems TE, Taylor DW, Maloy WL, et al. Comparative analysis of the Plasmodium falciparum histidine-rich proteins HRP-I, HRP-II and HRP-III in malaria parasites of diverse origin. Parasitology. 1987;95:209–27.CrossRef Rock EP, Marsh K, Saul AJ, Wellems TE, Taylor DW, Maloy WL, et al. Comparative analysis of the Plasmodium falciparum histidine-rich proteins HRP-I, HRP-II and HRP-III in malaria parasites of diverse origin. Parasitology. 1987;95:209–27.CrossRef
20.
go back to reference Baker J, Ho MF, 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.CrossRef Baker J, Ho MF, 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.CrossRef
21.
go back to reference Abukari Z, Okonu R, Nyarko SB, Lo AC, Dieng CC, Salifu SP, et al. The diversity, multiplicity of infection and population structure of P. falciparum parasites circulating in asymptomatic carriers living in high and low malaria transmission settings of Ghana. Genes (Basel). 2019;10:634.CrossRef Abukari Z, Okonu R, Nyarko SB, Lo AC, Dieng CC, Salifu SP, et al. The diversity, multiplicity of infection and population structure of P. falciparum parasites circulating in asymptomatic carriers living in high and low malaria transmission settings of Ghana. Genes (Basel). 2019;10:634.CrossRef
22.
go back to reference Gatei W, Gimnig JE, Hawley W, ter Kuile F, Odero C, Iriemenam NC, et al. Genetic diversity of Plasmodium falciparum parasite by microsatellite markers after scale-up of insecticide-treated bed nets in western Kenya. Malar J. 2015;14:495.CrossRef Gatei W, Gimnig JE, Hawley W, ter Kuile F, Odero C, Iriemenam NC, et al. Genetic diversity of Plasmodium falciparum parasite by microsatellite markers after scale-up of insecticide-treated bed nets in western Kenya. Malar J. 2015;14:495.CrossRef
23.
go back to reference Bosco AB, Anderson K, Gresty K, Prosser C, Smith D, Nankabirwa JI, et al. Molecular surveillance reveals the presence of pfhrp2 and pfhrp3 gene deletions in Plasmodium falciparum parasite populations in Uganda, 2017–2019. Malar J. 2020;19:300.CrossRef Bosco AB, Anderson K, Gresty K, Prosser C, Smith D, Nankabirwa JI, et al. Molecular surveillance reveals the presence of pfhrp2 and pfhrp3 gene deletions in Plasmodium falciparum parasite populations in Uganda, 2017–2019. Malar J. 2020;19:300.CrossRef
24.
go back to reference Gonahasa S, Maiteki-Sebuguzi C, Rugnao S, Dorsey G, Opigo J, Yeka A, et al. LLIN evaluation in Uganda project (LLINEUP): factors associated with ownership and use of long-lasting insecticidal nets in Uganda: a cross-sectional survey of 48 districts. Malar J. 2018;17:421.CrossRef Gonahasa S, Maiteki-Sebuguzi C, Rugnao S, Dorsey G, Opigo J, Yeka A, et al. LLIN evaluation in Uganda project (LLINEUP): factors associated with ownership and use of long-lasting insecticidal nets in Uganda: a cross-sectional survey of 48 districts. Malar J. 2018;17:421.CrossRef
25.
go back to reference Rugnao S, Gonahasa S, Maiteki-Sebuguzi C, Opigo J, Yeka A, Katureebe A, et al. LLIN Evaluation in Uganda Project (LLINEUP): factors associated with childhood parasitaemia and anaemia 3 years after a national long-lasting insecticidal net distribution campaign: a cross-sectional survey. Malar J. 2019;18:207.CrossRef Rugnao S, Gonahasa S, Maiteki-Sebuguzi C, Opigo J, Yeka A, Katureebe A, et al. LLIN Evaluation in Uganda Project (LLINEUP): factors associated with childhood parasitaemia and anaemia 3 years after a national long-lasting insecticidal net distribution campaign: a cross-sectional survey. Malar J. 2019;18:207.CrossRef
26.
go back to reference Staedke SG, Kamya MR, Dorsey G, Maiteki-Sebuguzi C, Gonahasa S, Yeka A, et al. LLIN evaluation in Uganda project (LLINEUP) - Impact of long-lasting insecticidal nets with, and without, piperonyl butoxide on malaria indicators in Uganda: study protocol for a cluster-randomised trial. Trials. 2019;20:321.CrossRef Staedke SG, Kamya MR, Dorsey G, Maiteki-Sebuguzi C, Gonahasa S, Yeka A, et al. LLIN evaluation in Uganda project (LLINEUP) - Impact of long-lasting insecticidal nets with, and without, piperonyl butoxide on malaria indicators in Uganda: study protocol for a cluster-randomised trial. Trials. 2019;20:321.CrossRef
27.
go back to reference 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.CrossRef 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.CrossRef
28.
go back to reference 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.CrossRef 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.CrossRef
29.
go back to reference Anderson TJC, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, et al. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol. 2000;17:1467–82.CrossRef Anderson TJC, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, et al. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol. 2000;17:1467–82.CrossRef
30.
go back to reference Anderson T, Bockarie M, Lagog M, Day K. Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999;119:113–25.CrossRef Anderson T, Bockarie M, Lagog M, Day K. Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999;119:113–25.CrossRef
31.
go back to reference Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, et al. Current trends in microsatellite genotyping. Mol Ecol Resour. 2011;11:591–611.CrossRef Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, et al. Current trends in microsatellite genotyping. Mol Ecol Resour. 2011;11:591–611.CrossRef
32.
go back to reference Liu Y, Tessema SK, Murphy M, Xu S, Schwartz A, Wang W, et al. Confirmation of the absence of local transmission and geographic assignment of imported falciparum malaria cases to China using microsatellite panel. Malar J. 2020;19:244.CrossRef Liu Y, Tessema SK, Murphy M, Xu S, Schwartz A, Wang W, et al. Confirmation of the absence of local transmission and geographic assignment of imported falciparum malaria cases to China using microsatellite panel. Malar J. 2020;19:244.CrossRef
33.
go back to reference Touray AO, Mobegi VA, Wamunyokoli F, Herren JK. Diversity and Multiplicity of P. falciparum infections among asymptomatic school children in Mbita Western Kenya. Sci Rep. 2020;10:5924.CrossRef Touray AO, Mobegi VA, Wamunyokoli F, Herren JK. Diversity and Multiplicity of P. falciparum infections among asymptomatic school children in Mbita Western Kenya. Sci Rep. 2020;10:5924.CrossRef
34.
go back to reference Durand R, Ariey F, Cojean S, Fontanet A, Ranaivo L, Ranarivelo LA, et al. Analysis of circulating populations of Plasmodium falciparum in mild and severe malaria in two different epidemiological patterns in Madagascar. Trop Med Int Health. 2008;13:1392–9.CrossRef Durand R, Ariey F, Cojean S, Fontanet A, Ranaivo L, Ranarivelo LA, et al. Analysis of circulating populations of Plasmodium falciparum in mild and severe malaria in two different epidemiological patterns in Madagascar. Trop Med Int Health. 2008;13:1392–9.CrossRef
35.
go back to reference Mohammed H, Hassen K, Assefa A, Mekete K, Tadesse G, Taye G, et al. Genetic diversity of Plasmodium falciparum isolates from patients with uncomplicated and severe malaria based on msp-1 and msp-2 genes in Gublak North West Ethiopia. Malar J. 2019;18:413.CrossRef Mohammed H, Hassen K, Assefa A, Mekete K, Tadesse G, Taye G, et al. Genetic diversity of Plasmodium falciparum isolates from patients with uncomplicated and severe malaria based on msp-1 and msp-2 genes in Gublak North West Ethiopia. Malar J. 2019;18:413.CrossRef
36.
go back to reference Roh ME, Tessema SK, Murphy M, Nhlabathi N, Mkhonta N, Vilakati S, et al. High genetic diversity of Plasmodium falciparum in the low-transmission setting of the Kingdom of Eswatini. J Infect Dis. 2019;220:1346–54.CrossRef Roh ME, Tessema SK, Murphy M, Nhlabathi N, Mkhonta N, Vilakati S, et al. High genetic diversity of Plasmodium falciparum in the low-transmission setting of the Kingdom of Eswatini. J Infect Dis. 2019;220:1346–54.CrossRef
37.
go back to reference Zhong D, Afrane Y, Githeko A, Yang Z, Cui L, Menge DM, et al. Plasmodium falciparum genetic diversity in western Kenya highlands. Am J Trop Med Hyg. 2007;77:1043–50.CrossRef Zhong D, Afrane Y, Githeko A, Yang Z, Cui L, Menge DM, et al. Plasmodium falciparum genetic diversity in western Kenya highlands. Am J Trop Med Hyg. 2007;77:1043–50.CrossRef
38.
go back to reference Pringle JC, Wesolowski A, Berube S, Kobayashi T, Gebhardt ME, Mulenga M, et al. High Plasmodium falciparum genetic diversity and temporal stability despite control efforts in high transmission settings along the international border between Zambia and the Democratic Republic of the Congo. Malar J. 2019;18:400.CrossRef Pringle JC, Wesolowski A, Berube S, Kobayashi T, Gebhardt ME, Mulenga M, et al. High Plasmodium falciparum genetic diversity and temporal stability despite control efforts in high transmission settings along the international border between Zambia and the Democratic Republic of the Congo. Malar J. 2019;18:400.CrossRef
39.
go back to reference Oyebola MK, Idowu ET, Olukosi YA, Iwalokun BA, Agomo CO, Ajibaye OO, et al. Genetic diversity and complexity of Plasmodium falciparum infections in Lagos Nigeria. Asian Pacific J Trop Biomed. 2014;4:S87–91.CrossRef Oyebola MK, Idowu ET, Olukosi YA, Iwalokun BA, Agomo CO, Ajibaye OO, et al. Genetic diversity and complexity of Plasmodium falciparum infections in Lagos Nigeria. Asian Pacific J Trop Biomed. 2014;4:S87–91.CrossRef
40.
go back to reference Mahdi Abdel Hamid M M, Elamin AF, Albsheer MMA, Abdalla AAA, Mahgoub NS, Mustafa SO, et al. Multiplicity of infection and genetic diversity of Plasmodium falciparum isolates from patients with uncomplicated and severe malaria in Gezira State Sudan. Parasit Vectors. 2016;9:362.CrossRef Mahdi Abdel Hamid M M, Elamin AF, Albsheer MMA, Abdalla AAA, Mahgoub NS, Mustafa SO, et al. Multiplicity of infection and genetic diversity of Plasmodium falciparum isolates from patients with uncomplicated and severe malaria in Gezira State Sudan. Parasit Vectors. 2016;9:362.CrossRef
41.
go back to reference Nankabirwa JI, Arinaitwe E, Rek J, Kilama M, Kizza T, Staedke SG, et al. Malaria transmission, infection, and disease following sustained indoor residual spraying of insecticide in Tororo Uganda. Am J Trop Med Hyg. 2020;103:1525–33.CrossRef Nankabirwa JI, Arinaitwe E, Rek J, Kilama M, Kizza T, Staedke SG, et al. Malaria transmission, infection, and disease following sustained indoor residual spraying of insecticide in Tororo Uganda. Am J Trop Med Hyg. 2020;103:1525–33.CrossRef
42.
go back to reference Kiwuwa MS, Ribacke U, Moll K, Byarugaba J, Lundblom K, Färnert A, et al. Genetic diversity of Plasmodium falciparum infections in mild and severe malaria of children from Kampala Uganda. Parasitol Res. 2013;112:1691–700.CrossRef Kiwuwa MS, Ribacke U, Moll K, Byarugaba J, Lundblom K, Färnert A, et al. Genetic diversity of Plasmodium falciparum infections in mild and severe malaria of children from Kampala Uganda. Parasitol Res. 2013;112:1691–700.CrossRef
43.
go back to reference Kyabayinze DJ, Karamagi C, Kiggundu M, Kamya MR, Wabwire-Mangen F, Kironde F, et al. Multiplicity of Plasmodium falciparum infection predicts antimalarial treatment outcome in Ugandan children. Afr Health Sci. 2008;8:200–5.PubMedPubMedCentral Kyabayinze DJ, Karamagi C, Kiggundu M, Kamya MR, Wabwire-Mangen F, Kironde F, et al. Multiplicity of Plasmodium falciparum infection predicts antimalarial treatment outcome in Ugandan children. Afr Health Sci. 2008;8:200–5.PubMedPubMedCentral
44.
go back to reference Bosco AB, Nankabirwa JI, Yeka A, Nsobya S, Gresty K, Anderson K, et al. Limitations of rapid diagnostic tests in malaria surveys in areas with varied transmission intensity in Uganda 2017–2019: implications for selection and use of HRP2 RDTs. PLoS ONE. 2021;15:e0244457.CrossRef Bosco AB, Nankabirwa JI, Yeka A, Nsobya S, Gresty K, Anderson K, et al. Limitations of rapid diagnostic tests in malaria surveys in areas with varied transmission intensity in Uganda 2017–2019: implications for selection and use of HRP2 RDTs. PLoS ONE. 2021;15:e0244457.CrossRef
45.
go back to reference Thomson R, Beshir KB, Cunningham J, Baiden F, Bharmal J, Bruxvoort KJ, et al. pfhrp2 and pfhrp3 gene deletions that affect malaria rapid diagnostic tests for Plasmodium falciparum: analysis of archived blood samples from 3 African countries. J Infect Dis. 2019;220:1444–52.CrossRef Thomson R, Beshir KB, Cunningham J, Baiden F, Bharmal J, Bruxvoort KJ, et al. pfhrp2 and pfhrp3 gene deletions that affect malaria rapid diagnostic tests for Plasmodium falciparum: analysis of archived blood samples from 3 African countries. J Infect Dis. 2019;220:1444–52.CrossRef
46.
go back to reference 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.CrossRef 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.CrossRef
47.
go back to reference 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.CrossRef 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.CrossRef
48.
go back to reference Addai-Mensah O, Dinko B, Noagbe M, Ameke SL, Annani-Akollor ME, Owiredu E-W, et al. Plasmodium falciparum histidine-rich protein 2 diversity in Ghana. Malar J. 2020;19:256.CrossRef Addai-Mensah O, Dinko B, Noagbe M, Ameke SL, Annani-Akollor ME, Owiredu E-W, et al. Plasmodium falciparum histidine-rich protein 2 diversity in Ghana. Malar J. 2020;19:256.CrossRef
49.
go back to reference Li P, Xing H, Zhao Z, Yang Z, Cao Y, Li W, et al. Genetic diversity of Plasmodium falciparum histidine-rich protein 2 in the China-Myanmar border area. Acta Trop. 2015;152:26–31.CrossRef Li P, Xing H, Zhao Z, Yang Z, Cao Y, Li W, et al. Genetic diversity of Plasmodium falciparum histidine-rich protein 2 in the China-Myanmar border area. Acta Trop. 2015;152:26–31.CrossRef
50.
go back to reference Metoh TN, Chen J-H, Fon-Gah P, Zhou X, Moyou-Somo R, Zhou X-N. Genetic diversity of Plasmodium falciparum and genetic profile in children affected by uncomplicated malaria in Cameroon. Malar J. 2020;19:115.CrossRef Metoh TN, Chen J-H, Fon-Gah P, Zhou X, Moyou-Somo R, Zhou X-N. Genetic diversity of Plasmodium falciparum and genetic profile in children affected by uncomplicated malaria in Cameroon. Malar J. 2020;19:115.CrossRef
51.
go back to reference Mussa A, Talib M, Mohamed Z, Hajissa K, 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;12:334.CrossRef Mussa A, Talib M, Mohamed Z, Hajissa K, 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;12:334.CrossRef
52.
go back to reference Agaba BB, Yeka A, Nsobya S, Arinaitwe E, Nankabirwa J, Opigo J, et al. Systematic review of the status of pfhrp2 and pfhrp3 gene deletion, approaches and methods used for its estimation and reporting in Plasmodium falciparum populations in Africa: review of published studies 2010–2019. Malar J. 2019;18:355.CrossRef Agaba BB, Yeka A, Nsobya S, Arinaitwe E, Nankabirwa J, Opigo J, et al. Systematic review of the status of pfhrp2 and pfhrp3 gene deletion, approaches and methods used for its estimation and reporting in Plasmodium falciparum populations in Africa: review of published studies 2010–2019. Malar J. 2019;18:355.CrossRef
53.
go back to reference 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.CrossRef 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.CrossRef
Metadata
Title
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
Authors
Bosco B. Agaba
Karen Anderson
Karryn Gresty
Christiane Prosser
David Smith
Joaniter I. Nankabirwa
Sam Nsobya
Adoke Yeka
Rhoda Namubiru
Emmanuel Arinaitwe
Paul Mbaka
John Kissa
Chae Seung Lim
Charles Karamagi
Joan K. Nakayaga
Moses R. Kamya
Qin Cheng
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2021
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-021-03763-6

Other articles of this Issue 1/2021

Malaria Journal 1/2021 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.