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Published in: Malaria Journal 1/2021

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

Parasite genetic diversity reflects continued residual malaria transmission in Vhembe District, a hotspot in the Limpopo Province of South Africa

Authors: Hazel B. Gwarinda, Sofonias K. Tessema, Jaishree Raman, Bryan Greenhouse, Lyn-Marié Birkholtz

Published in: Malaria Journal | Issue 1/2021

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Abstract

Background

South Africa aims to eliminate malaria transmission by 2023. However, despite sustained vector control efforts and case management interventions, the Vhembe District remains a malaria transmission hotspot. To better understand Plasmodium falciparum transmission dynamics in the area, this study characterized the genetic diversity of parasites circulating within the Vhembe District.

Methods

A total of 1153 falciparum-positive rapid diagnostic tests (RDTs) were randomly collected from seven clinics within the district, over three consecutive years (2016, 2017 and 2018) during the wet and dry malaria transmission seasons. Using 26 neutral microsatellite markers, differences in genetic diversity were described using a multiparameter scale of multiplicity of infection (MOI), inbreeding metric (Fws), number of unique alleles (A), expected heterozygosity (He), multilocus linkage disequilibrium (LD) and genetic differentiation, and were associated with temporal and geospatial variances.

Results

A total of 747 (65%) samples were successfully genotyped. Moderate to high genetic diversity (mean He = 0.74 ± 0.03) was observed in the parasite population. This was ascribed to high allelic richness (mean A = 12.2 ± 1.2). The majority of samples (99%) had unique multi-locus genotypes, indicating high genetic diversity in the sample set. Complex infections were observed in 66% of samples (mean MOI = 2.13 ± 0.04), with 33% of infections showing high within-host diversity as described by the Fws metric. Low, but significant LD (standardised index of association, ISA = 0.08, P < 0.001) was observed that indicates recombination of distinct clones. Limited impact of temporal (FST range − 0.00005 to 0.0003) and spatial (FST = − 0.028 to 0.023) variation on genetic diversity existed during the sampling timeframe and study sites respectively.

Conclusions

Consistent with the Vhembe District’s classification as a ‘high’ transmission setting within South Africa, P. falciparum diversity in the area was moderate to high and complex. This study showed that genetic diversity within the parasite population reflects the continued residual transmission observed in the Vhembe District. This data can be used as a reference point for the assessment of the effectiveness of on-going interventions over time, the identification of imported cases and/or outbreaks, as well as monitoring for the potential spread of anti-malarial drug resistance.
Literature
1.
go back to reference WHO. World malaria report 2019. Geneva: World Health Organization; 2019. WHO. World malaria report 2019. Geneva: World Health Organization; 2019.
2.
go back to reference WHO. Global technical strategy for malaria 2016–2030. Geneva: World Health Organization; 2015. WHO. Global technical strategy for malaria 2016–2030. Geneva: World Health Organization; 2015.
3.
go back to reference Maharaj R, Raman J, Morris N, Moonasar D, Durrheim D, Seocharan I, et al. Epidemiology of malaria in South Africa: From control to elimination. S Afr Med J. 2013;103:779–83.PubMedCrossRef Maharaj R, Raman J, Morris N, Moonasar D, Durrheim D, Seocharan I, et al. Epidemiology of malaria in South Africa: From control to elimination. S Afr Med J. 2013;103:779–83.PubMedCrossRef
4.
go back to reference Raman J, Morris N, Frean J, Brooke B, Blumberg L, Kruger P, et al. Reviewing South Africa’s malaria elimination strategy (2012–2018): progress, challenges and priorities. Malar J. 2016;15:438.PubMedPubMedCentralCrossRef Raman J, Morris N, Frean J, Brooke B, Blumberg L, Kruger P, et al. Reviewing South Africa’s malaria elimination strategy (2012–2018): progress, challenges and priorities. Malar J. 2016;15:438.PubMedPubMedCentralCrossRef
5.
go back to reference Malaria Elimination Strategic Plan for South. Africa 2019–2023 [Internet]. South African Department of Health. 2019. Malaria Elimination Strategic Plan for South. Africa 2019–2023 [Internet]. South African Department of Health. 2019.
6.
go back to reference Moonasar D, Maharaj R, Kunene S, Candrinho B, Saute F, Ntshalintshali N, et al. Towards malaria elimination in the MOSASWA (Mozambique, South Africa and Swaziland) region. Malar J. 2016;15:419.PubMedPubMedCentralCrossRef Moonasar D, Maharaj R, Kunene S, Candrinho B, Saute F, Ntshalintshali N, et al. Towards malaria elimination in the MOSASWA (Mozambique, South Africa and Swaziland) region. Malar J. 2016;15:419.PubMedPubMedCentralCrossRef
7.
go back to reference Moonasar D, Nuthulaganti T, Kruger PS, Mabuza A, Rasiswi ES, Benson FG, et al. Malaria control in South Africa 2000–2010: beyond MDG6. Malar J. 2012;11:294.PubMedPubMedCentralCrossRef Moonasar D, Nuthulaganti T, Kruger PS, Mabuza A, Rasiswi ES, Benson FG, et al. Malaria control in South Africa 2000–2010: beyond MDG6. Malar J. 2012;11:294.PubMedPubMedCentralCrossRef
8.
go back to reference Khosa E, Kuonza LR, Kruger P, Maimela E. Towards the elimination of malaria in South Africa: a review of surveillance data in Mutale Municipality, Limpopo Province, 2005 to 2010. Malar J. 2013;12:7.PubMedPubMedCentralCrossRef Khosa E, Kuonza LR, Kruger P, Maimela E. Towards the elimination of malaria in South Africa: a review of surveillance data in Mutale Municipality, Limpopo Province, 2005 to 2010. Malar J. 2013;12:7.PubMedPubMedCentralCrossRef
9.
go back to reference Raman J, Gast L, Balawanth R, Tessema S, Brooke B, Maharaj R, et al. High levels of imported asymptomatic malaria but limited local transmission in KwaZulu-Natal, a South African malaria-endemic province nearing malaria elimination. Malar J. 2020;19:152.PubMedPubMedCentralCrossRef Raman J, Gast L, Balawanth R, Tessema S, Brooke B, Maharaj R, et al. High levels of imported asymptomatic malaria but limited local transmission in KwaZulu-Natal, a South African malaria-endemic province nearing malaria elimination. Malar J. 2020;19:152.PubMedPubMedCentralCrossRef
10.
go back to reference Adeola A, Ncongwane K, Abiodun G, Makgoale T, Rautenbach H, Botai J, et al. Rainfall trends and malaria occurrences in Limpopo Province, South Africa. Int J Environ Res Public Health. 2019;16:5156.PubMedCentralCrossRef Adeola A, Ncongwane K, Abiodun G, Makgoale T, Rautenbach H, Botai J, et al. Rainfall trends and malaria occurrences in Limpopo Province, South Africa. Int J Environ Res Public Health. 2019;16:5156.PubMedCentralCrossRef
11.
go back to reference Brooke B, Koekemoer I, Kruger P, Urbach J, Misiani E, Coetzee M. Malaria vector control in South Africa. S Afr Med J. 2013;103:784–8.PubMedCrossRef Brooke B, Koekemoer I, Kruger P, Urbach J, Misiani E, Coetzee M. Malaria vector control in South Africa. S Afr Med J. 2013;103:784–8.PubMedCrossRef
12.
go back to reference Christian R, Dahan-Moss Y, Munhenga G, Lobb L, Erlank E, Dandalo L, et al. Malaria Vector Surveillance Report, South Africa, January–December, 2017. Johannesburg: National Institute for Communicable Diseases-Bulletin; 2016. Christian R, Dahan-Moss Y, Munhenga G, Lobb L, Erlank E, Dandalo L, et al. Malaria Vector Surveillance Report, South Africa, January–December, 2017. Johannesburg: National Institute for Communicable Diseases-Bulletin; 2016.
13.
go back to reference Kyalo D, Amratia P, Mundia CW, Mbogo CM, Coetzee M, Snow RW. A geo-coded inventory of anophelines in the Afrotropical Region south of the Sahara: 1898–2016. Wellcome Open Res. 2017;2:57.PubMedPubMedCentralCrossRef Kyalo D, Amratia P, Mundia CW, Mbogo CM, Coetzee M, Snow RW. A geo-coded inventory of anophelines in the Afrotropical Region south of the Sahara: 1898–2016. Wellcome Open Res. 2017;2:57.PubMedPubMedCentralCrossRef
14.
go back to reference Samuel M, Qwabe B, Dlamini D, Mabaso N, Manyawo Z, Zhikali J, et al. Malaria Vector Surveillance Report, South Africa, January–December 2018. Johannesburg: National Institute for Communicable Diseases-Bulletin; 2018. Samuel M, Qwabe B, Dlamini D, Mabaso N, Manyawo Z, Zhikali J, et al. Malaria Vector Surveillance Report, South Africa, January–December 2018. Johannesburg: National Institute for Communicable Diseases-Bulletin; 2018.
15.
go back to reference Ukpe IS, Moonasar D, Raman J, Barnes K, Baker L, Blumberg L. Case management of malaria: treatment and chemoprophylaxis. S Afr Med J. 2013;103:793–8.CrossRef Ukpe IS, Moonasar D, Raman J, Barnes K, Baker L, Blumberg L. Case management of malaria: treatment and chemoprophylaxis. S Afr Med J. 2013;103:793–8.CrossRef
16.
go back to reference Anderson TJ, 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.PubMedCrossRef Anderson TJ, 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.PubMedCrossRef
17.
go back to reference Auburn S, Barry AE. Dissecting malaria biology and epidemiology using population genetics and genomics. Int J Parasito. 2017;47:77–85.CrossRef Auburn S, Barry AE. Dissecting malaria biology and epidemiology using population genetics and genomics. Int J Parasito. 2017;47:77–85.CrossRef
18.
go back to reference Patel JC, Taylor SM, Juliao PC, Parobek CM, Janko M, Gonzalez LD, et al. Genetic evidence of importation of drug-resistant Plasmodium falciparum to Guatemala from the Democratic Republic of the Congo. Emerg Infect Dis. 2014;20:932.PubMedPubMedCentralCrossRef Patel JC, Taylor SM, Juliao PC, Parobek CM, Janko M, Gonzalez LD, et al. Genetic evidence of importation of drug-resistant Plasmodium falciparum to Guatemala from the Democratic Republic of the Congo. Emerg Infect Dis. 2014;20:932.PubMedPubMedCentralCrossRef
19.
go back to reference Escalante AA, Ferreira MU, Vinetz JM, Volkman SK, Cui L, Gamboa D, et al. Malaria molecular epidemiology: lessons from the International Centers of Excellence for Malaria Research Network. Am J Trop Med Hyg. 2015;93:79–86.PubMedPubMedCentralCrossRef Escalante AA, Ferreira MU, Vinetz JM, Volkman SK, Cui L, Gamboa D, et al. Malaria molecular epidemiology: lessons from the International Centers of Excellence for Malaria Research Network. Am J Trop Med Hyg. 2015;93:79–86.PubMedPubMedCentralCrossRef
20.
go back to reference Carter TE, Malloy H, Existe A, Memnon G, Victor YS, Okech BA, et al. Genetic diversity of Plasmodium falciparum in Haiti: insights from microsatellite markers. PLoS One. 2015;10:e0140416.PubMedPubMedCentralCrossRef Carter TE, Malloy H, Existe A, Memnon G, Victor YS, Okech BA, et al. Genetic diversity of Plasmodium falciparum in Haiti: insights from microsatellite markers. PLoS One. 2015;10:e0140416.PubMedPubMedCentralCrossRef
21.
go back to reference Razak MRMA, Sastu UR, Norahmad NA, Abdul-Karim A, Muhammad A, Muniandy PK, et al. Genetic diversity of Plasmodium falciparum populations in malaria declining areas of Sabah, East Malaysia. PLoS One. 2016;11:e0152415.CrossRef Razak MRMA, Sastu UR, Norahmad NA, Abdul-Karim A, Muhammad A, Muniandy PK, et al. Genetic diversity of Plasmodium falciparum populations in malaria declining areas of Sabah, East Malaysia. PLoS One. 2016;11:e0152415.CrossRef
22.
go back to reference Bei AK, Niang M, Deme AB, Daniels RF, Sarr FD, Sokhna C, et al. Dramatic changes in malaria population genetic complexity in Dielmo and Ndiop, Senegal, revealed using genomic surveillance. J Infect Dis. 2018;217:622–7.PubMedPubMedCentralCrossRef Bei AK, Niang M, Deme AB, Daniels RF, Sarr FD, Sokhna C, et al. Dramatic changes in malaria population genetic complexity in Dielmo and Ndiop, Senegal, revealed using genomic surveillance. J Infect Dis. 2018;217:622–7.PubMedPubMedCentralCrossRef
23.
go back to reference Amambua-Ngwa A, Jeffries D, Amato R, Worwui A, Karim M, Ceesay S, et al. Consistent signatures of selection from genomic analysis of pairs of temporal and spatial Plasmodium falciparum populations from The Gambia. Sci Rep. 2018;8:9687.PubMedPubMedCentralCrossRef Amambua-Ngwa A, Jeffries D, Amato R, Worwui A, Karim M, Ceesay S, et al. Consistent signatures of selection from genomic analysis of pairs of temporal and spatial Plasmodium falciparum populations from The Gambia. Sci Rep. 2018;8:9687.PubMedPubMedCentralCrossRef
24.
go back to reference Daniels R, Chang H-H, Séne PD, Park DC, Neafsey DE, Schaffner SF, et al. Genetic surveillance detects both clonal and epidemic transmission of malaria following enhanced intervention in Senegal. PLoS One. 2013;8:e60780.PubMedPubMedCentralCrossRef Daniels R, Chang H-H, Séne PD, Park DC, Neafsey DE, Schaffner SF, et al. Genetic surveillance detects both clonal and epidemic transmission of malaria following enhanced intervention in Senegal. PLoS One. 2013;8:e60780.PubMedPubMedCentralCrossRef
25.
go back to reference Roh M, Tessema S, 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:e1346-54.CrossRef Roh M, Tessema S, 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:e1346-54.CrossRef
26.
go back to reference Tessema S, Wesolowski A, Chen A, Murphy M, Wilheim J, Mupiri A-R, et al. Using parasite genetic and human mobility data to infer local and cross-border malaria connectivity in Southern Africa. Elife. 2019;8:e43510.PubMedPubMedCentralCrossRef Tessema S, Wesolowski A, Chen A, Murphy M, Wilheim J, Mupiri A-R, et al. Using parasite genetic and human mobility data to infer local and cross-border malaria connectivity in Southern Africa. Elife. 2019;8:e43510.PubMedPubMedCentralCrossRef
27.
go back to reference Module M. Preparation of Rapid Diagnostic Tests (RDTs) for DNA extraction v1.1. WWARN Procedure. 2011. Module M. Preparation of Rapid Diagnostic Tests (RDTs) for DNA extraction v1.1. WWARN Procedure. 2011.
28.
go back to reference Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.PubMedCrossRef Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.PubMedCrossRef
29.
go back to reference 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. PLoS Med. 2015;12:e1001788.PubMedPubMedCentralCrossRef 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. PLoS Med. 2015;12:e1001788.PubMedPubMedCentralCrossRef
30.
go back to reference Awandu SS, Raman J, Bousema T, Birkholtz L-M. Ultralow-density Plasmodium falciparum Infections in African Settings. Clin Infect Dis. 2019;69:1463–4.PubMedPubMedCentralCrossRef Awandu SS, Raman J, Bousema T, Birkholtz L-M. Ultralow-density Plasmodium falciparum Infections in African Settings. Clin Infect Dis. 2019;69:1463–4.PubMedPubMedCentralCrossRef
31.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
32.
go back to reference Auburn S, Campino S, Miotto O, Djimde AA, Zongo I, Manske M, et al. Characterization of within-host Plasmodium falciparum diversity using next-generation sequence data. PLoS ONE. 2012;7:e32891.PubMedPubMedCentralCrossRef Auburn S, Campino S, Miotto O, Djimde AA, Zongo I, Manske M, et al. Characterization of within-host Plasmodium falciparum diversity using next-generation sequence data. PLoS ONE. 2012;7:e32891.PubMedPubMedCentralCrossRef
33.
go back to reference Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, et al. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature. 2012;487:375.PubMedPubMedCentralCrossRef Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, et al. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature. 2012;487:375.PubMedPubMedCentralCrossRef
34.
go back to reference Mobegi VA, Duffy CW, Amambua-Ngwa A, Loua KM, Laman E, Nwakanma DC, et al. Genome-wide analysis of selection on the malaria parasite Plasmodium falciparum in West African populations of differing infection endemicity. Mol Biol Evol. 2014;31:1490–9.PubMedPubMedCentralCrossRef Mobegi VA, Duffy CW, Amambua-Ngwa A, Loua KM, Laman E, Nwakanma DC, et al. Genome-wide analysis of selection on the malaria parasite Plasmodium falciparum in West African populations of differing infection endemicity. Mol Biol Evol. 2014;31:1490–9.PubMedPubMedCentralCrossRef
35.
go back to reference Agapow PM, Burt A. Indices of multilocus linkage disequilibrium. Mol Ecol Notes. 2001;1:101–2.CrossRef Agapow PM, Burt A. Indices of multilocus linkage disequilibrium. Mol Ecol Notes. 2001;1:101–2.CrossRef
36.
go back to reference Kamvar ZN, Tabima JF, Grünwald NJ. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ. 2014;2:e281.PubMedPubMedCentralCrossRef Kamvar ZN, Tabima JF, Grünwald NJ. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ. 2014;2:e281.PubMedPubMedCentralCrossRef
37.
go back to reference Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24:1403–5.CrossRefPubMed Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24:1403–5.CrossRefPubMed
38.
go back to reference Winter DJ. MMOD: an R library for the calculation of population differentiation statistics. Mol Ecol Resour. 2012;12:1158–60.PubMedCrossRef Winter DJ. MMOD: an R library for the calculation of population differentiation statistics. Mol Ecol Resour. 2012;12:1158–60.PubMedCrossRef
39.
go back to reference Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11:94.PubMedPubMedCentralCrossRef Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11:94.PubMedPubMedCentralCrossRef
40.
go back to reference Mobegi VA, Loua KM, Ahouidi AD, Satoguina J, Nwakanma DC, Amambua-Ngwa A, et al. Population genetic structure of Plasmodium falciparum across a region of diverse endemicity in West Africa. Malar J. 2012;11:223.PubMedPubMedCentralCrossRef Mobegi VA, Loua KM, Ahouidi AD, Satoguina J, Nwakanma DC, Amambua-Ngwa A, et al. Population genetic structure of Plasmodium falciparum across a region of diverse endemicity in West Africa. Malar J. 2012;11:223.PubMedPubMedCentralCrossRef
41.
go back to reference Murray L, Mobegi VA, Duffy CW, Assefa SA, Kwiatkowski DP, Laman E, et al. Microsatellite genotyping and genome-wide single nucleotide polymorphism-based indices of Plasmodium falciparum diversity within clinical infections. Malar J. 2016;15:275.PubMedPubMedCentralCrossRef Murray L, Mobegi VA, Duffy CW, Assefa SA, Kwiatkowski DP, Laman E, et al. Microsatellite genotyping and genome-wide single nucleotide polymorphism-based indices of Plasmodium falciparum diversity within clinical infections. Malar J. 2016;15:275.PubMedPubMedCentralCrossRef
42.
go back to reference Nabet C, Doumbo S, Jeddi F, Konaté S, Manciulli T, Fofana B, et al. Genetic diversity of Plasmodium falciparum in human malaria cases in Mali. Malar J. 2016;15:353.PubMedPubMedCentralCrossRef Nabet C, Doumbo S, Jeddi F, Konaté S, Manciulli T, Fofana B, et al. Genetic diversity of Plasmodium falciparum in human malaria cases in Mali. Malar J. 2016;15:353.PubMedPubMedCentralCrossRef
43.
go back to reference Conway DJ, Roper C, Oduola AM, Arnot DE, Kremsner PG, Grobusch MP, et al. High recombination rate in natural populations of Plasmodium falciparum. Proc Natl Acad Sci USA. 1999;96:4506–11.PubMedCrossRefPubMedCentral Conway DJ, Roper C, Oduola AM, Arnot DE, Kremsner PG, Grobusch MP, et al. High recombination rate in natural populations of Plasmodium falciparum. Proc Natl Acad Sci USA. 1999;96:4506–11.PubMedCrossRefPubMedCentral
44.
go back to reference Anthony TG, Conway DJ, Cox-Singh J, Matusop A, Ratnam S, Shamsul S, et al. Fragmented population structure of Plasmodium falciparum in a region of declining endemicity. J Infect Dis. 2005;191:1558–64.PubMedCrossRef Anthony TG, Conway DJ, Cox-Singh J, Matusop A, Ratnam S, Shamsul S, et al. Fragmented population structure of Plasmodium falciparum in a region of declining endemicity. J Infect Dis. 2005;191:1558–64.PubMedCrossRef
45.
go back to reference Rice BL, Golden CD, Anjaranirina EJG, Botelho CM, Volkman SK, Hartl DL. Genetic evidence that the Makira region in northeastern Madagascar is a hotspot of malaria transmission. Malar J. 2016;15:596.PubMedPubMedCentralCrossRef Rice BL, Golden CD, Anjaranirina EJG, Botelho CM, Volkman SK, Hartl DL. Genetic evidence that the Makira region in northeastern Madagascar is a hotspot of malaria transmission. Malar J. 2016;15:596.PubMedPubMedCentralCrossRef
46.
go back to reference Taylor LH, Walliker D, Read AF. Mixed–genotype infections of malaria parasites: within–host dynamics and transmission success of competing clones. Proc Biol Sci. 1997;264:927–35.PubMedPubMedCentralCrossRef Taylor LH, Walliker D, Read AF. Mixed–genotype infections of malaria parasites: within–host dynamics and transmission success of competing clones. Proc Biol Sci. 1997;264:927–35.PubMedPubMedCentralCrossRef
47.
go back to reference Sondo P, Derra K, Lefevre T, Diallo-Nakanabo S, Tarnagda Z, Zampa O, et al. Genetically diverse Plasmodium falciparum infections, within-host competition and symptomatic malaria in humans. Sci Rep. 2019;9:127.PubMedPubMedCentralCrossRef Sondo P, Derra K, Lefevre T, Diallo-Nakanabo S, Tarnagda Z, Zampa O, et al. Genetically diverse Plasmodium falciparum infections, within-host competition and symptomatic malaria in humans. Sci Rep. 2019;9:127.PubMedPubMedCentralCrossRef
48.
go back to reference Nassir E, Abdel-Muhsin A-MA, Suliaman S, Kenyon F, Kheir A, Geha H, et al. Impact of genetic complexity on longevity and gametocytogenesis of Plasmodium falciparum during the dry and transmission-free season of eastern Sudan. Int J Parasitol. 2005;35:49–55.PubMedCrossRef Nassir E, Abdel-Muhsin A-MA, Suliaman S, Kenyon F, Kheir A, Geha H, et al. Impact of genetic complexity on longevity and gametocytogenesis of Plasmodium falciparum during the dry and transmission-free season of eastern Sudan. Int J Parasitol. 2005;35:49–55.PubMedCrossRef
49.
go back to reference Bose J, Kloesener MH, Schulte RD. Multiple-genotype infections and their complex effect on virulence. Zoology. 2016;119:339–49.PubMedCrossRef Bose J, Kloesener MH, Schulte RD. Multiple-genotype infections and their complex effect on virulence. Zoology. 2016;119:339–49.PubMedCrossRef
50.
go back to reference Pollitt LC, Mideo N, Drew DR, Schneider P, Colegrave N, Reece SE. Competition and the evolution of reproductive restraint in malaria parasites. Am Nat. 2011;177:358–67.PubMedPubMedCentralCrossRef Pollitt LC, Mideo N, Drew DR, Schneider P, Colegrave N, Reece SE. Competition and the evolution of reproductive restraint in malaria parasites. Am Nat. 2011;177:358–67.PubMedPubMedCentralCrossRef
Metadata
Title
Parasite genetic diversity reflects continued residual malaria transmission in Vhembe District, a hotspot in the Limpopo Province of South Africa
Authors
Hazel B. Gwarinda
Sofonias K. Tessema
Jaishree Raman
Bryan Greenhouse
Lyn-Marié Birkholtz
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/s12936-021-03635-z

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